Skip to main content

Advertisement

SpringerLink
Log in

Nanoscale delivery systems for microRNAs in cancer therapy

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Concomitant with advances in research regarding the role of miRNAs in sustaining carcinogenesis, major concerns about their delivery options for anticancer therapies have been raised. The answer to this problem may come from the world of nanoparticles such as liposomes, exosomes, polymers, dendrimers, mesoporous silica nanoparticles, quantum dots and metal-based nanoparticles which have been proved as versatile and valuable vehicles for many biomolecules including miRNAs. In another train of thoughts, the general scheme of miRNA modulation consists in inhibition of oncomiRNA expression and restoration of tumor suppressor ones. The codelivery of two miRNAs or miRNAs in combination with chemotherapeutics or small molecules was also proposed. The present review presents the latest advancements in miRNA delivery based on nanoparticle-related strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Reprinted (adapted) with permission from Yang et al. [50]

Fig. 5

Reprinted (adapted) with the permission from Lopez-Bertoni et al. [79]

Fig. 6

Reprinted (adapted) with permission from Djaker et al. [140]

Similar content being viewed by others

References

  1. Dinger ME, Pang KC, Mercer TR, Mattick JS (2008) Differentiating protein-coding and noncoding RNA: challenges and ambiguities. PLoS Comput Biol 4(11):e1000176

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Starega-Roslan J, Krol J, Koscianska E, Kozlowski P, Szlachcic WJ, Sobczak K et al (2011) Structural basis of microRNA length variety. Nucleic Acids Res 39(1):257–268

    Article  CAS  PubMed  Google Scholar 

  3. Gulei D, Irimie AI, Cojocneanu-Petric R, Schultze JL, Berindan-Neagoe I (2018) Exosomes-small players big sound. Bioconjugate Chem 29(3):635–648

    Article  CAS  Google Scholar 

  4. Braicu C, Catana C, Calin GA, Berindan-Neagoe I (2014) NCRNA combined therapy as future treatment option for cancer. Curr Pharm Des 20(42):6565–6574

    Article  CAS  PubMed  Google Scholar 

  5. Hashimoto Y, Akiyama Y, Yuasa Y (2013) Multiple-to-multiple relationships between microRNAs and target genes in gastric cancer. PLoS ONE 8(5):e62589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120(1):15–20

    Article  CAS  PubMed  Google Scholar 

  7. Gulei D, Mehterov N, Nabavi SM, Atanasov AG, Berindan-Neagoe I (2018) Targeting ncRNAs by plant secondary metabolites: the ncRNAs game in the balance towards malignancy inhibition. Biotechnol Adv 36(6):1779–1799

    Article  CAS  PubMed  Google Scholar 

  8. Garzon R, Marcucci G, Croce CM (2010) Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov 9(10):775–789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Redis RS, Berindan-Neagoe I, Pop VI, Calin GA (2012) Non-coding RNAs as theranostics in human cancers. J Cell Biochem 113(5):1451–1459

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Braicu C, Calin GA, Berindan-Neagoe I (2013) MicroRNAs and cancer therapy—from bystanders to major players. Curr Med Chem 20(29):3561–3573

    Article  CAS  PubMed  Google Scholar 

  11. Svoronos AA, Engelman DM, Slack FJ (2016) OncomiR or Tumor Suppressor? The Duplicity of MicroRNAs in Cancer. Cancer Res 76(13):3666–3670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Irimie AI, Braicu C, Sonea L, Zimta AA, Cojocneanu-Petric R, Tonchev K et al (2017) A looking-glass of non-coding RNAs in oral cancer. Int J Mol Sci 18(12):E2620

    Article  PubMed  CAS  Google Scholar 

  13. Pop-Bica C, Pintea S, Cojocneanu-Petric R, Del Sal G, Piazza S, Wu ZH et al (2018) MiR-181 family-specific behavior in different cancers: a meta-analysis view. Cancer Metastasis Rev 37(1):17–32

    Article  CAS  PubMed  Google Scholar 

  14. Shah MY, Ferrajoli A, Sood AK, Lopez-Berestein G, Calin GA (2016) microRNA therapeutics in cancer—an emerging concept. EBioMedicine 12:34–42

    Article  PubMed  PubMed Central  Google Scholar 

  15. Shah MY, Calin GA (2014) MicroRNAs as therapeutic targets in human cancers. Wiley Interdiscip Rev RNA 5(4):537–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Van Roosbroeck K, Fanini F, Setoyama T, Ivan C, Rodriguez-Aguayo C, Fuentes-Mattei E et al (2017) Combining anti-Mir-155 with chemotherapy for the treatment of lung Cancers. Clin Cancer Res 23(11):2891–2904

    Article  PubMed  CAS  Google Scholar 

  17. Chen Y, Zhao H, Tan Z, Zhang C, Fu X (2015) Bottleneck limitations for microRNA-based therapeutics from bench to the bedside. Pharmazie 70(3):147–154

    CAS  PubMed  Google Scholar 

  18. Baumann V, Winkler J (2014) miRNA-based therapies: strategies and delivery platforms for oligonucleotide and non-oligonucleotide agents. Future Med Chem 6(17):1967–1984

    Article  CAS  PubMed  Google Scholar 

  19. Johannes L, Lucchino M (2018) Current challenges in delivery and cytosolic translocation of therapeutic RNAs. Nucl Acid Ther 28(3):178–193

    Article  CAS  Google Scholar 

  20. Xu C, Haque F, Jasinski DL, Binzel DW, Shu D, Guo P (2018) Favorable biodistribution, specific targeting and conditional endosomal escape of RNA nanoparticles in cancer therapy. Cancer Lett 414:57–70

    Article  CAS  PubMed  Google Scholar 

  21. Ben-Shushan D, Markovsky E, Gibori H, Tiram G, Scomparin A, Satchi-Fainaro R (2014) Overcoming obstacles in microRNA delivery towards improved cancer therapy. Drug Deliv Transl Res 4(1):38–49

    Article  CAS  PubMed  Google Scholar 

  22. Jurj A, Braicu C, Pop LA, Tomuleasa C, Gherman CD, Berindan-Neagoe I (2017) The new era of nanotechnology, an alternative to change cancer treatment. Drug Des Dev Therapy 11:2871–2890

    Article  CAS  Google Scholar 

  23. Czauderna F, Fechtner M, Dames S, Aygun H, Klippel A, Pronk GJ et al (2003) Structural variations and stabilising modifications of synthetic siRNAs in mammalian cells. Nucleic Acids Res 31(11):2705–2716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Yoo BH, Bochkareva E, Bochkarev A, Mou TC, Gray DM (2004) 2′-O-methyl-modified phosphorothioate antisense oligonucleotides have reduced non-specific effects in vitro. Nucleic Acids Res 32(6):2008–2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Wahlestedt C, Salmi P, Good L, Kela J, Johnsson T, Hokfelt T et al (2000) Potent and nontoxic antisense oligonucleotides containing locked nucleic acids. Proc Natl Acad Sci U S A 97(10):5633–5638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hyrup B, Nielsen PE (1996) Peptide nucleic acids (PNA): synthesis, properties and potential applications. Bioorg Med Chem 4(1):5–23

    Article  CAS  PubMed  Google Scholar 

  27. Pallan PS, Greene EM, Jicman PA, Pandey RK, Manoharan M, Rozners E et al (2011) Unexpected origins of the enhanced pairing affinity of 2′-fluoro-modified RNA. Nucleic Acids Res 39(8):3482–3495

    Article  CAS  PubMed  Google Scholar 

  28. Blanco E, Shen H, Ferrari M (2015) Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol 33(9):941–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Tomuleasa C, Braicu C, Irimie A, Craciun L, Berindan-Neagoe I (2014) Nanopharmacology in translational hematology and oncology. Int J Nanomed 9:3465–3479

    CAS  Google Scholar 

  30. Stylianopoulos T (2013) EPR-effect: utilizing size-dependent nanoparticle delivery to solid tumors. Ther Del 4(4):421–423

    Article  CAS  Google Scholar 

  31. Hobbs SK, Monsky WL, Yuan F, Roberts WG, Griffith L, Torchilin VP et al (1998) Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc Natl Acad Sci USA 95(8):4607–4612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Sarin H (2010) Physiologic upper limits of pore size of different blood capillary types and another perspective on the dual pore theory of microvascular permeability. J Angiogenesis Res 2:14

    Article  CAS  Google Scholar 

  33. Fröhlich E (2012) The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int J Nanomed 7:5577–5591

    Article  Google Scholar 

  34. Bahadar H, Maqbool F, Niaz K, Abdollahi M (2016) Toxicity of Nanoparticles and an Overview of Current Experimental Models. Iranian biomedical journal. 20(1):1–11

    PubMed  PubMed Central  Google Scholar 

  35. Behzadi S, Serpooshan V, Tao W, Hamaly MA, Alkawareek MY, Dreaden EC et al (2017) Cellular uptake of nanoparticles: journey inside the cell. Chem Soc Rev 46(14):4218–4244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Rappoport J, Preece J, Chipman K (2011) How do manufactured nanoparticles enter cells? UK Mathematics-in-Medicine Study Group Reading 2011, pp 1–33

  37. Zhao J, Stenzel M (2017) Entry of nanoparticles into cells: the importance of nanoparticle properties. Polym Chem 9:259–272

    Google Scholar 

  38. Urban-Morlan Z, Ganem-Rondero A, Melgoza-Contreras LM, Escobar-Chavez JJ, Nava-Arzaluz MG, Quintanar-Guerrero D (2010) Preparation and characterization of solid lipid nanoparticles containing cyclosporine by the emulsification-diffusion method. Int J Nanomed 5:611–620

    CAS  Google Scholar 

  39. Ozpolat B, Sood AK, Lopez-Berestein G (2014) Liposomal siRNA nanocarriers for cancer therapy. Adv Drug Deliv Rev 66:110–116

    Article  CAS  PubMed  Google Scholar 

  40. Braicu C, Pileczki V, Irimie A, Berindan-Neagoe I (2013) p53siRNA therapy reduces cell proliferation, migration and induces apoptosis in triple negative breast cancer cells. Mol Cell Biochem 381(1–2):61–68

    Article  CAS  PubMed  Google Scholar 

  41. Endo-Takahashi Y, Negishi Y, Nakamura A, Ukai S, Ooaku K, Oda Y et al (2014) Systemic delivery of miR-126 by miRNA-loaded bubble liposomes for the treatment of hindlimb ischemia. Sci Rep 4:3883

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Lee HY, Mohammed KA, Kaye F, Sharma P, Moudgil BM, Clapp WL et al (2013) Targeted delivery of let-7a microRNA encapsulated ephrin-A1 conjugated liposomal nanoparticles inhibit tumor growth in lung cancer. Int J Nanomed 8:4481–4494

    Google Scholar 

  43. Wu SY, Putral LN, Liang M, Chang HI, Davies NM, McMillan NA (2009) Development of a novel method for formulating stable siRNA-loaded lipid particles for in vivo use. Pharm Res 26(3):512–522

    Article  CAS  PubMed  Google Scholar 

  44. Maroof H, Islam F, Dong L, Ajjikuttira P, Gopalan V, McMillan NAJ et al (2018) Liposomal delivery of miR-34b-5p induced cancer cell death in thyroid carcinoma. Cells 7(12):265

    Article  CAS  PubMed Central  Google Scholar 

  45. Piao L, Zhang M, Datta J, Xie X, Su T, Li H et al (2012) Lipid-based nanoparticle delivery of Pre-miR-107 inhibits the tumorigenicity of head and neck squamous cell carcinoma. Mol Therapy 20(6):1261–1269

    Article  CAS  Google Scholar 

  46. Beg MS, Brenner AJ, Sachdev J, Borad M, Kang YK, Stoudemire J et al (2017) Phase I study of MRX34, a liposomal miR-34a mimic, administered twice weekly in patients with advanced solid tumors. Invest New Drugs 35(2):180–188

    Article  CAS  PubMed  Google Scholar 

  47. Tolcher AW, Rodrigueza WV, Rasco DW, Patnaik A, Papadopoulos KP, Amaya A et al (2014) A phase 1 study of the BCL2-targeted deoxyribonucleic acid inhibitor (DNAi) PNT2258 in patients with advanced solid tumors. Cancer Chemother Pharmacol 73(2):363–371

    Article  CAS  PubMed  Google Scholar 

  48. Hatakeyama H, Murata M, Sato Y, Takahashi M, Minakawa N, Matsuda A et al (2014) The systemic administration of an anti-miRNA oligonucleotide encapsulated pH-sensitive liposome results in reduced level of hepatic microRNA-122 in mice. J Controlled Release 173:43–50

    Article  CAS  Google Scholar 

  49. Zhang W, Peng F, Zhou T, Huang Y, Zhang L, Ye P et al (2015) Targeted delivery of chemically modified anti-miR-221 to hepatocellular carcinoma with negatively charged liposomes. Int J Nanomed 10:4825–4836

    CAS  Google Scholar 

  50. Yang T, Zhao P, Rong Z, Li B, Xue H, You J et al (2016) Anti-tumor efficiency of lipid-coated cisplatin nanoparticles co-loaded with MicroRNA-375. Theranostics 6(1):142–154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Xu F, Liao JZ, Xiang GY, Zhao PX, Ye F, Zhao Q et al (2017) MiR-101 and doxorubicin codelivered by liposomes suppressing malignant properties of hepatocellular carcinoma. Cancer Med 6(3):651–661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Yin Y, Ornell KJ, Beliveau A, Jain A (2016) Modulation of MicroRNAs 34a and 21 affects viability, senescence, and invasion in glioblastoma multiforme. J Biomed Nanotechnol 12(9):1782–1797

    Article  CAS  PubMed  Google Scholar 

  53. Ando H, Asai T, Koide H, Okamoto A, Maeda N, Tomita K et al (2014) Advanced cancer therapy by integrative antitumor actions via systemic administration of miR-499. J Controlled Release 181:32–39

    Article  CAS  Google Scholar 

  54. Yung BC, Li J, Zhang M, Cheng X, Li H, Yung EM et al (2016) Lipid nanoparticles composed of quaternary amine-tertiary amine cationic lipid combination (QTsome) for therapeutic delivery of AntimiR-21 for lung cancer. Mol Pharm 13(2):653–662

    Article  CAS  PubMed  Google Scholar 

  55. Xu S, Zhao N, Hui L, Song M, Miao ZW, Jiang XJ (2016) MicroRNA-124-3p inhibits the growth and metastasis of nasopharyngeal carcinoma cells by targeting STAT3. Oncol Rep 35(3):1385–1394

    Article  CAS  PubMed  Google Scholar 

  56. Sharma S, Rajendran V, Kulshreshtha R, Ghosh PC (2017) Enhanced efficacy of anti-miR-191 delivery through stearylamine liposome formulation for the treatment of breast cancer cells. Int J Pharm 530(1–2):387–400

    Article  CAS  PubMed  Google Scholar 

  57. Keller S, Ridinger J, Rupp AK, Janssen JW, Altevogt P (2011) Body fluid derived exosomes as a novel template for clinical diagnostics. J Transl Med 9:86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Li M, Zeringer E, Barta T, Schageman J, Cheng A, Vlassov AV (2014) Analysis of the RNA content of the exosomes derived from blood serum and urine and its potential as biomarkers. Philos Trans R Soc Lond Ser B Biol Sci 369(1652):20130502

    Article  CAS  Google Scholar 

  59. Srinivasan S, Vannberg FO, Dixon JB (2016) Lymphatic transport of exosomes as a rapid route of information dissemination to the lymph node. Sci Rep 6:24436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Zhang J, Li S, Li L, Li M, Guo C, Yao J et al (2015) Exosome and exosomal microRNA: trafficking, sorting, and function. Genom Proteom Bioinf 13(1):17–24

    Article  CAS  Google Scholar 

  61. Rana S, Zoller M (2011) Exosome target cell selection and the importance of exosomal tetraspanins: a hypothesis. Biochem Soc Trans 39(2):559–562

    Article  CAS  PubMed  Google Scholar 

  62. Sempere LF, Keto J, Fabbri M (2017) Exosomal MicroRNAs in breast cancer towards diagnostic and therapeutic applications. Cancers (Basel). 9(7)

  63. Pan JH, Zhou H, Zhao XX, Ding H, Li W, Qin L et al (2018) Role of exosomes and exosomal microRNAs in hepatocellular carcinoma: potential in diagnosis and antitumour treatments (Review). Int J Mol Med 41(4):1809–1816

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Ha D, Yang N, Nadithe V (2016) Exosomes as therapeutic drug carriers and delivery vehicles across biological membranes: current perspectives and future challenges. Acta Pharm Sin B 6(4):287–296

    Article  PubMed  PubMed Central  Google Scholar 

  65. Stremersch S, Vandenbroucke RE, Van Wonterghem E, Hendrix A, De Smedt SC, Raemdonck K (2016) Comparing exosome-like vesicles with liposomes for the functional cellular delivery of small RNAs. J Controlled Release 232:51–61

    Article  CAS  Google Scholar 

  66. Lang FM, Hossain A, Gumin J, Momin EN, Shimizu Y, Ledbetter D et al (2018) Mesenchymal stem cells as natural biofactories for exosomes carrying miR-124a in the treatment of gliomas. Neuro Oncol 20(3):380–390

    Article  CAS  PubMed  Google Scholar 

  67. O’Brien K, Lowry MC, Corcoran C, Martinez VG, Daly M, Rani S et al (2015) miR-134 in extracellular vesicles reduces triple-negative breast cancer aggression and increases drug sensitivity. Oncotarget 6(32):32774–32789

    Article  PubMed  PubMed Central  Google Scholar 

  68. Momen-Heravi F, Bala S, Bukong T, Szabo G (2014) Exosome-mediated delivery of functionally active miRNA-155 inhibitor to macrophages. Nanomedicine 10(7):1517–1527

    Article  CAS  PubMed  Google Scholar 

  69. Liang G, Kan S, Zhu Y, Feng S, Feng W, Gao S (2018) Engineered exosome-mediated delivery of functionally active miR-26a and its enhanced suppression effect in HepG2 cells. Int J Nanomed 13:585–599

    Article  CAS  Google Scholar 

  70. Ferrante SC, Nadler EP, Pillai DK, Hubal MJ, Wang Z, Wang JM et al (2015) Adipocyte-derived exosomal miRNAs: a novel mechanism for obesity-related disease. Pediatr Res 77(3):447–454

    Article  CAS  PubMed  Google Scholar 

  71. Ohno S, Takanashi M, Sudo K, Ueda S, Ishikawa A, Matsuyama N et al (2013) Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 21(1):185–191

    Article  CAS  PubMed  Google Scholar 

  72. Moreno-Vega A-I, Mez-Quintero T, Nuez-Anita R-E et al (2012) Polymeric and ceramic nanoparticles in biomedical applications. J Nanotechnol 2012:10

    Article  CAS  Google Scholar 

  73. Mohamed A, Kunda NK, Ross K, Hutcheon GA, Saleem IY (2019) Polymeric nanoparticles for the delivery of miRNA to treat chronic obstructive pulmonary disease (COPD). Eur J Pharm Biopharm 136:1–8

    Article  CAS  PubMed  Google Scholar 

  74. Zhang X, Li Y, Chen YE, Chen J, Ma PX (2016) Cell-free 3D scaffold with two-stage delivery of miRNA-26a to regenerate critical-sized bone defects. Nat Commun 7:10376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Mathew AP, Cho KH, Uthaman S, Cho CS, Park IK (2017) Stimuli-regulated smart polymeric systems for gene therapy. Polymers 9(4):E152

    Article  PubMed  CAS  Google Scholar 

  76. Lu XY, Wu DC, Li ZJ, Chen GQ (2011) Polymer nanoparticles. Prog Mol Biol Transl Sci 104:299–323

    Article  CAS  PubMed  Google Scholar 

  77. Chiou GY, Cherng JY, Hsu HS, Wang ML, Tsai CM, Lu KH et al (2012) Cationic polyurethanes-short branch PEI-mediated delivery of Mir145 inhibited epithelial-mesenchymal transdifferentiation and cancer stem-like properties and in lung adenocarcinoma. J Controlled Release 159(2):240–250

    Article  CAS  Google Scholar 

  78. Bolhassani A, Javanzad S, Saleh T, Hashemi M, Aghasadeghi MR, Sadat SM (2014) Polymeric nanoparticles: potent vectors for vaccine delivery targeting cancer and infectious diseases. Hum Vaccines Immunother 10(2):321–332

    Article  CAS  Google Scholar 

  79. Lopez-Bertoni H, Kozielski KL, Rui Y, Lal B, Vaughan H, Wilson DR et al (2018) bioreducible polymeric nanoparticles containing multiplexed cancer stem cell regulating miRNAs inhibit glioblastoma growth and prolong survival. Nano Lett 18(7):4086–4094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Malhotra M, Sekar TV, Ananta JS, Devulapally R, Afjei R, Babikir HA et al (2018) Targeted nanoparticle delivery of therapeutic antisense microRNAs presensitizes glioblastoma cells to lower effective doses of temozolomide in vitro and in a mouse model. Oncotarget 9(30):21478–21494

    Article  PubMed  PubMed Central  Google Scholar 

  81. Abbasi E, Aval SF, Akbarzadeh A, Milani M, Nasrabadi HT, Joo SW et al (2014) Dendrimers: synthesis, applications, and properties. Nanoscale Res Lett 9(1):247

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Madaan K, Kumar S, Poonia N, Lather V, Pandita D (2014) Dendrimers in drug delivery and targeting: drug-dendrimer interactions and toxicity issues. J Pharm Bioallied Sci 6(3):139–150

    Article  PubMed  PubMed Central  Google Scholar 

  83. Palmerston Mendes L, Pan J, Torchilin VP (2017) Dendrimers as nanocarriers for nucleic acid and drug delivery in cancer therapy. Molecules 22(9):E1401

    Article  PubMed  CAS  Google Scholar 

  84. Jain K, Kesharwani P, Gupta U, Jain NK (2010) Dendrimer toxicity: let’s meet the challenge. Int J Pharm 394(1–2):122–142

    Article  CAS  PubMed  Google Scholar 

  85. Duncan R, Izzo L (2005) Dendrimer biocompatibility and toxicity. Adv Drug Deliv Rev 57(15):2215–2237

    Article  CAS  PubMed  Google Scholar 

  86. Agrawal P, Gupta U, Jain NK (2007) Glycoconjugated peptide dendrimers-based nanoparticulate system for the delivery of chloroquine phosphate. Biomaterials 28(22):3349–3359

    Article  CAS  PubMed  Google Scholar 

  87. Jevprasesphant R, Penny J, Jalal R, Attwood D, McKeown NB, D’Emanuele A (2003) The influence of surface modification on the cytotoxicity of PAMAM dendrimers. Int J Pharm 252(1–2):263–266

    Article  CAS  PubMed  Google Scholar 

  88. Luo D, Haverstick K, Belcheva N, Han E, Saltzman W (2002) Poly(ethylene glycol)-conjugated PAMAM dendrimer for biocompatible, high-efficiency DNA Deliv

  89. Gajbhiye V, Vijayaraj Kumar P, Tekade RK, Jain NK (2009) PEGylated PPI dendritic architectures for sustained delivery of H2 receptor antagonist. Eur J Med Chem 44(3):1155–1166

    Article  CAS  PubMed  Google Scholar 

  90. Bhadra D, Yadav AK, Bhadra S, Jain NK (2005) Glycodendrimeric nanoparticulate carriers of primaquine phosphate for liver targeting. Int J Pharm 295(1–2):221–233

    Article  CAS  PubMed  Google Scholar 

  91. Bhadra D, Bhadra S, Jain S, Jain NK (2003) A PEGylated dendritic nanoparticulate carrier of fluorouracil. Int J Pharm 257(1–2):111–124

    Article  CAS  PubMed  Google Scholar 

  92. Konda SD, Aref M, Wang S, Brechbiel M, Wiener EC (2001) Specific targeting of folate-dendrimer MRI contrast agents to the high affinity folate receptor expressed in ovarian tumor xenografts. Magma 12(2–3):104–113

    Article  CAS  PubMed  Google Scholar 

  93. Agarwal A, Gupta U, Asthana A, Jain NK (2009) Dextran conjugated dendritic nanoconstructs as potential vectors for anti-cancer agent. Biomaterials 30(21):3588–3596

    Article  CAS  PubMed  Google Scholar 

  94. Conde J, Oliva N, Atilano M, Song HS, Artzi N (2016) Self-assembled RNA-triple-helix hydrogel scaffold for microRNA modulation in the tumour microenvironment. Nat Mater 15(3):353–363

    Article  CAS  PubMed  Google Scholar 

  95. Liu X, Li G, Su Z, Jiang Z, Chen L, Wang J et al (2013) Poly(amido amine) is an ideal carrier of miR-7 for enhancing gene silencing effects on the EGFR pathway in U251 glioma cells. Oncol Rep 29(4):1387–1394

    Article  CAS  PubMed  Google Scholar 

  96. Keefe AD, Pai S, Ellington A (2010) Aptamers as therapeutics. Nat Rev Drug Discov 9(7):537–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Tahiri-Alaoui A, Frigotto L, Manville N, Ibrahim J, Romby P, James W (2002) High affinity nucleic acid aptamers for streptavidin incorporated into bi-specific capture ligands. Nucleic Acids Res 30(10):e45

    Article  PubMed  PubMed Central  Google Scholar 

  98. Tan W, Wang H, Chen Y, Zhang X, Zhu H, Yang C et al (2011) Molecular aptamers for drug delivery. Trends Biotechnol 29(12):634–640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Song KM, Lee S, Ban C (2012) Aptamers and their biological applications. Sensors. 12(1):612–631

    Article  PubMed  PubMed Central  Google Scholar 

  100. Wang H, Zhao X, Guo C, Ren D, Zhao Y, Xiao W et al (2015) Aptamer-dendrimer bioconjugates for targeted Delivery of miR-34a expressing plasmid and antitumor effects in non-small cell lung cancer cells. PLoS ONE 10(9):e0139136

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  101. Beavers KR, Werfel TA, Shen T, Kavanaugh TE, Kilchrist KV, Mares JW et al (2016) Porous silicon and polymer nanocomposites for delivery of peptide nucleic acids as anti-MicroRNA therapies. Adv Mater 28(36):7984–7992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Maleki A, Kettiger H, Schoubben A, Rosenholm JM, Ambrogi V, Hamidi M (2017) Mesoporous silica materials: from physico-chemical properties to enhanced dissolution of poorly water-soluble drugs. J Controlled Release 262:329–347

    Article  CAS  Google Scholar 

  103. Wang Y, Zhao Q, Han N, Bai L, Li J, Liu J et al (2015) Mesoporous silica nanoparticles in drug delivery and biomedical applications. Nanomed Nanotechnol Biol Med 11(2):313–327

    Article  CAS  Google Scholar 

  104. Mellaerts R, Aerts CA, Van Humbeeck J, Augustijns P, Van den Mooter G, Martens JA (2007) Enhanced release of itraconazole from ordered mesoporous SBA-15 silica materials. Chem Commun 13:1375–1377

    Article  CAS  Google Scholar 

  105. Heikkila T, Salonen J, Tuura J, Kumar N, Salmi T, Murzin DY et al (2007) Evaluation of mesoporous TCPSi, MCM-41, SBA-15, and TUD-1 materials as API carriers for oral drug delivery. Drug Delivery 14(6):337–347

    Article  CAS  PubMed  Google Scholar 

  106. Kumar D, Sailaja Chirravuri SV, Shastri NR (2014) Impact of surface area of silica particles on dissolution rate and oral bioavailability of poorly water soluble drugs: a case study with aceclofenac. Int J Pharm 461(1–2):459–468

    Article  CAS  PubMed  Google Scholar 

  107. Eren Z, Tunçer S, Gezer G, Yildirim L, Banerjee S, Yilmaz A (2016) Improved solubility of celecoxib by inclusion in SBA-15 mesoporous silica: Drug loading in different solvents and release. Microporous Mesoporous Mater 235:211–223

    Article  CAS  Google Scholar 

  108. Jambhrunkar S, Qu Z, Popat A, Karmakar S, Xu C, Yu C (2014) Modulating in vitro release and solubility of griseofulvin using functionalized mesoporous silica nanoparticles. J Colloid Interface Sci 434:218–225

    Article  CAS  PubMed  Google Scholar 

  109. Guo Z, Liu XM, Ma L, Li J, Zhang H, Gao YP et al (2013) Effects of particle morphology, pore size and surface coating of mesoporous silica on Naproxen dissolution rate enhancement. Colloids Surf B 101:228–235

    Article  CAS  Google Scholar 

  110. Heidegger S, Gossl D, Schmidt A, Niedermayer S, Argyo C, Endres S et al (2016) Immune response to functionalized mesoporous silica nanoparticles for targeted drug delivery. Nanoscale. 8(2):938–948

    Article  CAS  PubMed  Google Scholar 

  111. Watermann A, Brieger J (2017) Mesoporous silica nanoparticles as drug delivery vehicles in cancer. Nanomaterials 7(7):E189

    Article  PubMed  CAS  Google Scholar 

  112. Zhou Y, Quan G, Wu Q, Zhang X, Niu B, Wu B et al (2018) Mesoporous silica nanoparticles for drug and gene delivery. Acta pharmaceutica Sinica B. 8(2):165–177

    Article  PubMed  PubMed Central  Google Scholar 

  113. Li Y, Duo Y, Bi J, Zeng X, Mei L, Bao S et al (2018) Targeted delivery of anti-miR-155 by functionalized mesoporous silica nanoparticles for colorectal cancer therapy. Int J Nanomed 13:1241–1256

    Article  CAS  Google Scholar 

  114. Bertucci A, Prasetyanto EA, Septiadi D, Manicardi A, Brognara E, Gambari R et al (2015) Combined delivery of temozolomide and anti-miR221 PNA using mesoporous silica nanoparticles induces apoptosis in resistant glioma cells. Small 11(42):5687–5695

    Article  CAS  PubMed  Google Scholar 

  115. Li Y, Duo Y, Zhai P, He L, Zhong K, Zhang Y et al (2018) Dual targeting delivery of miR-328 by functionalized mesoporous silica nanoparticles for colorectal cancer therapy. Nanomedicine (Lond Engl)

  116. Deng K, Zhang Y, Tong X (2018) Sensitive electrochemical detection of microRNA-21 based on propylamine-functionalized mesoporous silica with glucometer readout. Anal Bioanal Chem 410(7):1863–1871

    Article  CAS  PubMed  Google Scholar 

  117. Xue H, Yu Z, Liu Y, Yuan W, Yang T, You J et al (2017) Delivery of miR-375 and doxorubicin hydrochloride by lipid-coated hollow mesoporous silica nanoparticles to overcome multiple drug resistance in hepatocellular carcinoma. Int J Nanomed 12:5271–5287

    Article  CAS  Google Scholar 

  118. Gupta B, Ruttala HB, Poudel BK, Pathak S, Regmi S, Gautam M et al (2018) Polyamino acid layer-by-layer (LbL) constructed silica-supported mesoporous titania nanocarriers for stimuli-responsive delivery of microRNA 708 and paclitaxel for combined chemotherapy. ACS Appl Mater Interfaces 10(29):24392–24405

    Article  CAS  PubMed  Google Scholar 

  119. Wu F-G, Zhang X, Chen X, Sun W, Bao Y-W, Hua X-W et al (2018) Quantum dots for cancer therapy and bioimaging. In: Gonçalves G, Tobias G (eds) Nanooncology, Nanomedicine and Nanotoxicology, Springer, Cham

    Google Scholar 

  120. Vu TQ, Lam WY, Hatch EW, Lidke DS (2015) Quantum dots for quantitative imaging: from single molecules to tissue. Cell Tissue Res 360(1):71–86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Zhou J, Yang Y, Zhang CY (2015) Toward biocompatible semiconductor quantum dots: from biosynthesis and bioconjugation to biomedical application. Chem Rev 115(21):11669–11717

    Article  CAS  PubMed  Google Scholar 

  122. Gao X, Cui Y, Levenson RM, Chung LW, Nie S (2004) In vivo cancer targeting and imaging with semiconductor quantum dots. Nat Biotechnol 22(8):969–976

    Article  CAS  PubMed  Google Scholar 

  123. Zhou Y, Shi L, Li Q, Jiang H, Lv G, Zhao J et al (2010) Imaging and inhibition of multi-drug resistance in cancer cells via specific association with negatively charged CdTe quantum dots. Biomaterials 31(18):4958–4963

    Article  CAS  PubMed  Google Scholar 

  124. Ye DX, Ma YY, Zhao W, Cao HM, Kong JL, Xiong HM et al (2016) ZnO-based nanoplatforms for labeling and treatment of mouse tumors without detectable toxic side effects. ACS Nano 10(4):4294–4300

    Article  CAS  PubMed  Google Scholar 

  125. Daneshpour M, Karimi B, Omidfar K (2018) Simultaneous detection of gastric cancer-involved miR-106a and let-7a through a dual-signal-marked electrochemical nanobiosensor. Biosens Bioelectron 109:197–205

    Article  CAS  PubMed  Google Scholar 

  126. Qu X, Jin H, Liu Y, Sun Q (2018) Strand displacement amplification reaction on quantum dot-encoded silica bead for visual detection of multiplex MicroRNAs. Anal Chem 90(5):3482–3489

    Article  CAS  PubMed  Google Scholar 

  127. Geng Y, Lin D, Shao L, Yan F, Ju H (2013) Cellular delivery of quantum dot-bound hybridization probe for detection of intracellular pre-MicroRNA using chitosan/Poly(γ-Glutamic Acid) complex as a carrier. PLoS ONE 8(6):e65540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Zeng X, Yuan Y, Wang T, Wang H, Hu X, Fu Z et al (2017) Targeted imaging and induction of apoptosis of drug-resistant hepatoma cells by miR-122-loaded graphene-InP nanocompounds. J Nanobiotechnol 15(1):9

    Article  CAS  Google Scholar 

  129. Zheng X, Zhang F, Zhao Y, Zhang J, Dawulieti J, Pan Y et al (2018) Self-assembled dual fluorescence nanoparticles for CD44-targeted delivery of anti-miR-27a in liver cancer theranostics. Theranostics 8(14):3808–3823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Stanley Rosarin F, Mirunalini S (2011) Nobel metallic nanoparticles with novel biomedical properties. J Bioanal Biomed 3:085–091

    CAS  Google Scholar 

  131. Singla R, Guliani A, Kumari A (2016) Yadav S. Toxicity issues and applications in medicine, Met Nanoparticles, pp 41–80

    Google Scholar 

  132. Petrushev B, Boca S, Simon T, Berce C, Frinc I, Dima D et al (2016) Gold nanoparticles enhance the effect of tyrosine kinase inhibitors in acute myeloid leukemia therapy. Int J Nanomed 11:641–660

    CAS  Google Scholar 

  133. Nagy-Simon T, Tatar AS, Craciun AM, Vulpoi A, Jurj MA, Florea A et al (2017) Antibody conjugated, raman tagged hollow gold-silver nanospheres for specific targeting and multimodal dark-field/SERS/two photon-FLIM imaging of CD19(+) B lymphoblasts. ACS Appl Mater Interfaces 9(25):21155–21168

    Article  CAS  PubMed  Google Scholar 

  134. Boca-Farcau S, Potara M, Simon T, Juhem A, Baldeck P, Astilean S (2014) Folic acid-conjugated, SERS-labeled silver nanotriangles for multimodal detection and targeted photothermal treatment on human ovarian cancer cells. Mol Pharm 11(2):391–399

    Article  CAS  PubMed  Google Scholar 

  135. Boca S, Rugina D, Pintea A, Barbu-Tudoran L, Astilean S (2011) Flower-shaped gold nanoparticles: synthesis, characterization and their application as SERS-active tags inside living cells. Nanotechnology 22(5):055702

    Article  PubMed  CAS  Google Scholar 

  136. Tiwari PM, Vig K, Dennis VA, Singh SR (2011) Functionalized Gold Nanoparticles and Their Biomedical Applications. Nanomaterials. 1(1):31–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Satomi T, Nagasaki Y, Kobayashi H, Otsuka H, Kataoka K (2007) Density control of poly(ethylene glycol) layer to regulate cellular attachment. Langmuir 23(12):6698–6703

    Article  CAS  PubMed  Google Scholar 

  138. Thakkar KN, Mhatre SS, Parikh RY (2010) Biological synthesis of metallic nanoparticles. Nanomed Nanotechnol Biol Med 6(2):257–262

    Article  CAS  Google Scholar 

  139. Boca SC, Astilean S (2010) Detoxification of gold nanorods by conjugation with thiolated poly(ethylene glycol) and their assessment as SERS-active carriers of Raman tags. Nanotechnology. 21(23):235601

    Article  PubMed  CAS  Google Scholar 

  140. Djaker N, Sultana S, Issaad D, Boca S, Moustaoui H, Spadavecchia J et al (2016) Spherical and flower-shaped gold nanoparticles characterization by scattering correlation spectroscopy. J Phys Chem C. 120(21):11700–11708

    Article  CAS  Google Scholar 

  141. Jen C-P, Chen Y-H, Fan C-S, Yeh C-S, Lin Y-C, Shieh D-B et al (2004) A Nonviral transfection approach in vitro: the design of a gold nanoparticle vector joint with microelectromechanical systems. Langmuir 20(4):1369–1374

    Article  CAS  PubMed  Google Scholar 

  142. Coradeghini R, Gioria S, Garcia CP, Nativo P, Franchini F, Gilliland D et al (2013) Size-dependent toxicity and cell interaction mechanisms of gold nanoparticles on mouse fibroblasts. Toxicol Lett 217(3):205–216

    Article  CAS  PubMed  Google Scholar 

  143. Soenen SJ, Manshian B, Montenegro JM, Amin F, Meermann B, Thiron T et al (2012) Cytotoxic effects of gold nanoparticles: a multiparametric study. ACS Nano 6(7):5767–5783

    Article  CAS  PubMed  Google Scholar 

  144. Sultana S, Djaker N, Boca-Farcau S, Salerno M, Charnaux N, Astilean S et al (2015) Comparative toxicity evaluation of flower-shaped and spherical gold nanoparticles on human endothelial cells. Nanotechnology 26(5):055101

    Article  PubMed  CAS  Google Scholar 

  145. Natarajan A, Venugopal SK, DeNardo SJ, Zern MA, editors. Breast cancer targeting novel microRNA-nanoparticles for imaging. SPIE BiOS; 2009: SPIE

  146. Hao L, Patel PC, Alhasan AH, Giljohann DA, Mirkin CA (2011) Nucleic acid-gold nanoparticle conjugates as mimics of microRNA. Small 7(22):3158–3162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Xue HY, Liu Y, Liao JZ, Lin JS, Li B, Yuan WG et al (2016) Gold nanoparticles delivered miR-375 for treatment of hepatocellular carcinoma. Oncotarget 7(52):86675–86686

    Article  PubMed  PubMed Central  Google Scholar 

  148. Ghosh R, Singh LC, Shohet JM, Gunaratne PH (2013) A gold nanoparticle platform for the delivery of functional microRNAs into cancer cells. Biomaterials 34(3):807–816

    Article  CAS  PubMed  Google Scholar 

  149. Ghosh R, Singh LC, Shohet JM, Gunaratne PH (2013) A gold nanoparticle platform for the delivery of functional microRNAs into cancer cells. Biomaterials 34(3):807–816

    Article  CAS  PubMed  Google Scholar 

  150. Lino MM, Simoes S, Vilaca A, Antunes H, Zonari A, Ferreira L (2018) Modulation of angiogenic activity by light-activatable miRNA-loaded nanocarriers. ACS Nano

  151. Fan L, Yang Q, Tan J, Qiao Y, Wang Q, He J et al (2015) Dual loading miR-218 mimics and Temozolomide using AuCOOH@FA-CS drug delivery system: promising targeted anti-tumor drug delivery system with sequential release functions. J Exp Clin Cancer Res 34:106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  152. Benisvy-Aharonovich E, Shimanovich U, Kronfeld N, Giladi N, Bier A, Kazimirsky G et al (2014) Pre-miRNA expressing plasmid delivery for anti-cancer therapy. MedChemComm 5(4):459–462

    Article  CAS  Google Scholar 

  153. Cai L, Li J, Zhang X, Lu Y, Wang J, Lyu X et al (2015) Gold nano-particles (AuNPs) carrying anti-EBV-miR-BART7-3p inhibit growth of EBV-positive nasopharyngeal carcinoma. Oncotarget 6(10):7838–7850

    Article  PubMed  PubMed Central  Google Scholar 

  154. Guo J, O’Driscoll CM, Holmes JD, Rahme K (2016) Bioconjugated gold nanoparticles enhance cellular uptake: a proof of concept study for siRNA delivery in prostate cancer cells. Int J Pharm 509(1–2):16–27

    Article  CAS  PubMed  Google Scholar 

  155. Ali A, Zafar H, Zia M, Ul Haq I, Phull AR, Ali JS et al (2016) Synthesis, characterization, applications, and challenges of iron oxide nanoparticles. Nanotechnol Sci Appl 9:49–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Li Y, Chen Y, Li J, Zhang Z, Huang C, Lian G et al (2017) Co-delivery of microRNA-21 antisense oligonucleotides and gemcitabine using nanomedicine for pancreatic cancer therapy. Cancer Sci 108(7):1493–1503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Setua S, Khan S, Yallapu MM, Behrman SW, Sikander M, Khan SS et al (2017) Restitution of Tumor Suppressor MicroRNA-145 Using Magnetic Nanoformulation for Pancreatic Cancer Therapy. J Gastrointest Surg 21(1):94–105

    Article  PubMed  Google Scholar 

  158. Ghosh Chaudhuri R, Paria S (2012) Core/shell nanoparticles: classes, properties, synthesis mechanisms, characterization, and applications. Chem Rev 112(4):2373–2433

    Article  CAS  PubMed  Google Scholar 

  159. Spain E, Adamson K, Elshahawy M, Bray I, Keyes TE, Stallings RL et al (2017) Hemispherical platinum: silver core: shell nanoparticles for miRNA detection. Anal 142(5):752–762

    Article  CAS  Google Scholar 

  160. Yin PT, Pongkulapa T, Cho HY, Han J, Pasquale NJ, Rabie H et al (2018) Overcoming chemoresistance in cancer via combined MicroRNA therapeutics with anticancer drugs using multifunctional magnetic core-shell nanoparticles. ACS Appl Mater Interfaces 10(32):26954–26963

    Article  CAS  PubMed  Google Scholar 

  161. Assali A, Akhavan O, Adeli M, Razzazan S, Dinarvand R, Zanganeh S et al (2018) Multifunctional core-shell nanoplatforms (gold@graphene oxide) with mediated NIR thermal therapy to promote miRNA delivery. Nanomedicine 14(6):1891–1903

    Article  CAS  PubMed  Google Scholar 

  162. Ren Y, Wang R, Gao L, Li K, Zhou X, Guo H et al (2016) Sequential co-delivery of miR-21 inhibitor followed by burst release doxorubicin using NIR-responsive hollow gold nanoparticle to enhance anticancer efficacy. Journal of Controlled Release 228:74–86

    Article  CAS  PubMed  Google Scholar 

  163. Nagesh PKB, Chowdhury P, Hatami E, Boya VKN, Kashyap VK, Khan S et al (2018) miRNA-205 nanoformulation sensitizes prostate cancer cells to chemotherapy. Cancers (Basel) 10(9)

  164. Seeman NC (2010) Nanomaterials based on DNA. Annu Rev Biochem 79:65–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Rothemund PW (2006) Folding DNA to create nanoscale shapes and patterns. Nature 440(7082):297–302

    Article  CAS  PubMed  Google Scholar 

  166. Seeman NC, Sleiman HF (2017) DNA nanotechnology. Nat Rev Mater 3:17068

    Article  CAS  Google Scholar 

  167. Conway JW, McLaughlin CK, Castor KJ, Sleiman H (2013) DNA nanostructure serum stability: greater than the sum of its parts. Chem Commun 49(12):1172–1174

    Article  CAS  Google Scholar 

  168. Mei Q, Wei X, Su F, Liu Y, Youngbull C, Johnson R et al (2011) Stability of DNA origami nanoarrays in cell lysate. Nano Lett 11(4):1477–1482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Hahn J, Wickham SF, Shih WM, Perrault SD (2014) Addressing the instability of DNA nanostructures in tissue culture. ACS Nano 8(9):8765–8775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Jiang Q, Song C, Nangreave J, Liu X, Lin L, Qiu D et al (2012) DNA origami as a carrier for circumvention of drug resistance. J Am Chem Soc 134(32):13396–13403

    Article  CAS  PubMed  Google Scholar 

  171. Lee H, Lytton-Jean AKR, Chen Y, Love KT, Park AI, Karagiannis ED et al (2012) Molecularly self-assembled nucleic acid nanoparticles for targeted in vivo siRNA delivery. Nat Nanotechnol 7:389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Douglas SM, Bachelet I, Church GM (2012) A logic-gated nanorobot for targeted transport of molecular payloads. Science 335(6070):831–834

    Article  CAS  PubMed  Google Scholar 

  173. Bujold KE, Hsu JCC, Sleiman HF (2016) Optimized DNA “nanosuitcases” for encapsulation and conditional release of siRNA. J Am Chem Soc 138(42):14030–14038

    Article  CAS  PubMed  Google Scholar 

  174. Kamaly N, Yameen B, Wu J, Farokhzad OC (2016) Degradable controlled-release polymers and polymeric nanoparticles: mechanisms of controlling drug release. Chem Rev 116(4):2602–2663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Gulei D, Berindan-Neagoe I (2018) Combined Therapy in Cancer: the Non-coding Approach. Molecular therapy Nucleic acids. 12:787–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Wen MM (2016) Getting miRNA therapeutics into the target cells for neurodegenerative diseases: a mini-review. Front Mol Neurosci 9:129

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  177. Chaudhary V, Jangra S, Yadav NR (2018) Nanotechnology based approaches for detection and delivery of microRNA in healthcare and crop protection. J Nanobiotechnol 16(1):40

    Article  CAS  Google Scholar 

  178. Babar IA, Cheng CJ, Booth CJ, Liang X, Weidhaas JB, Saltzman WM et al (2012) Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc Natl Acad Sci USA 109(26):E1695–E1704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Kamaly N, Yameen B, Wu J, Farokhzad OC (2016) Degradable controlled-release polymers and polymeric nanoparticles: mechanisms of controlling drug release. Chem Rev 116(4):2602–2663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Lu Y, Sun W, Gu Z (2014) Stimuli-responsive nanomaterials for therapeutic protein delivery. J Controlled Release 194:1–19

    Article  CAS  Google Scholar 

  181. Samal SK, Dash M, Van Vlierberghe S, Kaplan DL, Chiellini E, van Blitterswijk C et al (2012) Cationic polymers and their therapeutic potential. Chem Soc Rev 41(21):7147–7194

    Article  CAS  PubMed  Google Scholar 

  182. Li Y, Gao J, Zhang C, Cao Z, Cheng D, Liu J et al (2017) Stimuli-responsive polymeric nanocarriers for efficient gene delivery. Top Curr Chem 375(2):27

    Article  CAS  Google Scholar 

  183. Wang LL, Burdick JA (2017) Engineered hydrogels for local and sustained delivery of RNA-interference therapies. Adv Healthc Mater 6(1)

  184. Louw AM, Kolar MK, Novikova LN, Kingham PJ, Wiberg M, Kjems J et al (2016) Chitosan polyplex mediated delivery of miRNA-124 reduces activation of microglial cells in vitro and in rat models of spinal cord injury. Nanomed Nanotechnol Biol Med 12(3):643–653

    Article  CAS  Google Scholar 

  185. Zhao QQ, Chen JL, Lv TF, He CX, Tang GP, Liang WQ et al (2009) N/P ratio significantly influences the transfection efficiency and cytotoxicity of a polyethylenimine/chitosan/DNA complex. Biol Pharm Bull 32(4):706–710

    Article  CAS  PubMed  Google Scholar 

  186. Han HD, Mora EM, Roh JW, Nishimura M, Lee SJ, Stone RL et al (2011) Chitosan hydrogel for localized gene silencing. Cancer Biol Ther 11(9):839–845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Gourevich D, Gerold B, Arditti F, Xu D, Liu D, Volovick A et al (2012) Ultrasound activated nano-encapsulated targeted drug delivery and tumour cell poration. Adv Exp Med Biol 733:135–144

    Article  CAS  PubMed  Google Scholar 

  188. Wang TY, Choe JW, Pu K, Devulapally R, Bachawal S, Machtaler S et al (2015) Ultrasound-guided delivery of microRNA loaded nanoparticles into cancer. Journal of Controlled Release 203:99–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Scherer F, Anton M, Schillinger U, Henke J, Bergemann C, Kruger A et al (2002) Magnetofection: enhancing and targeting gene delivery by magnetic force in vitro and in vivo. Gene Ther 9(2):102–109

    Article  CAS  PubMed  Google Scholar 

  190. Prosen L, Prijic S, Music B, Lavrencak J, Cemazar M, Sersa G (2013) Magnetofection: a reproducible method for gene delivery to melanoma cells. Biomed Res Int 2013:209452

    Article  PubMed  PubMed Central  Google Scholar 

  191. Laurentt N, Sapet C, Le Gourrierec L, Bertosio E, Zelphati O (2011) Nucleic acid delivery using magnetic nanoparticles: the Magnetofection technology. Therapeutic delivery. 2(4):471–482

    Article  PubMed  CAS  Google Scholar 

  192. Oral O, Cikim T, Zuvin M, Unal O, Yagci-Acar H, Gozuacik D et al (2015) Effect of varying magnetic fields on targeted gene delivery of nucleic acid-based molecules. Ann Biomed Eng 43(11):2816–2826

    Article  PubMed  Google Scholar 

  193. Jiang S, Eltoukhy AA, Love KT, Langer R, Anderson DG (2013) Lipidoid-coated iron oxide nanoparticles for efficient DNA and siRNA delivery. Nano Lett 13(3):1059–1064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Sun C, Lee JS, Zhang M (2008) Magnetic nanoparticles in MR imaging and drug delivery. Adv Drug Deliv Rev 60(11):1252–1265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  195. Srinoi P, Chen Y-T, Vittur V, Marquez M (2018) Randall Lee T. Enhanced magnetic and optical properties for emerging biological applications, Bimet Nanoparticles, p 1106

    Google Scholar 

  196. Sun S, Zeng H, Robinson DB, Raoux S, Rice PM, Wang SX et al (2004) Monodisperse MFe2O4 (M=Fe Co, Mn) nanoparticles. J Am Chem Soc 126(1):273–279

    Article  CAS  PubMed  Google Scholar 

  197. Sun J, Li Y, Liang XJ, Wang PC (2011) Bacterial magnetosome: a novel biogenetic magnetic targeted drug carrier with potential multifunctions. J Nanomater 2011(2011):469031–469043

    PubMed  PubMed Central  Google Scholar 

  198. Nappini S, Fogli S, Castroflorio B, Bonini M, Bombelli F, Baglioni P (2015) Magnetic field responsive drug release from magnetoliposomes in biological fluids. J Mater Chem B 4:716

    Article  CAS  Google Scholar 

  199. Li J, Mo L, Lu CH, Fu T, Yang HH, Tan W (2016) Functional nucleic acid-based hydrogels for bioanalytical and biomedical applications. Chem Soc Rev 45(5):1410–1431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Jalili NA, Muscarello M, Gaharwar AK (2016) Nanoengineered thermoresponsive magnetic hydrogels for biomedical applications. Bioeng Transl Med 1(3):297–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Ge J, Neofytou E, Cahill TJ 3rd, Beygui RE, Zare RN (2012) Drug release from electric-field-responsive nanoparticles. ACS Nano 6(1):227–233

    Article  CAS  PubMed  Google Scholar 

  202. Jeon G, Yang SY, Byun J, Kim JK (2011) Electrically actuatable smart nanoporous membrane for pulsatile drug release. Nano Lett 11(3):1284–1288

    Article  CAS  PubMed  Google Scholar 

  203. Servant A, Bussy C, Al-Jamal K, Kostarelos K (2013) Design, engineering and structural integrity of electro-responsive carbon nanotube- based hydrogels for pulsatile drug release. J Mater Chem B 1:4593–4600

    Article  CAS  PubMed  Google Scholar 

  204. Mura S, Nicolas J, Couvreur P (2013) Stimuli-responsive nanocarriers for drug delivery. Nat Mater 12(11):991–1003

    Article  CAS  PubMed  Google Scholar 

  205. Brudno Y, Mooney DJ (2015) On-demand drug delivery from local depots. Journal of Controlled Release 219:8–17

    Article  CAS  PubMed  Google Scholar 

  206. Linsley CS, Wu BM (2017) Recent advances in light-responsive on-demand drug-delivery systems. Ther Deliv 8(2):89–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. Zhao H, Sterner ES, Bryan Coughlin E, Theato P (2012) o-Nitrobenzyl alcohol derivatives: opportunities in polymer and materials science. Macromolecules 45(4):1723–1736

    Article  CAS  Google Scholar 

  208. Pelliccioli AP, Wirz J (2002) Photoremovable protecting groups: reaction mechanisms and applications. Photochem Photobiol Sci 1(7):441–458

    Article  PubMed  Google Scholar 

  209. Wang H, Zhang W, Gao C (2015) Shape transformation of light-responsive pyrene-containing micelles and their influence on cytoviability. Biomacromol 16(8):2276–2281

    Article  CAS  Google Scholar 

  210. Weissleder R (2001) A clearer vision for in vivo imaging. Nat Biotechnol 19(4):316–317

    Article  CAS  PubMed  Google Scholar 

  211. Puri A (2013) Phototriggerable liposomes: current research and future perspectives. Pharmaceutics 6(1):1–25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  212. Huang Y, Dong R, Zhu X, Yan D (2014) Photo-responsive polymeric micelles. Soft Matter 10(33):6121–6138

    Article  CAS  PubMed  Google Scholar 

  213. Bleger D, Hecht S (2015) Visible-light-activated molecular switches. Angew Chem 54(39):11338–11349

    Article  CAS  Google Scholar 

  214. Cui ZK, Phoeung T, Rousseau PA, Rydzek G, Zhang Q, Bazuin CG et al (2014) Nonphospholipid fluid liposomes with switchable photocontrolled release. Langmuir ACS J Surf Colloids 30(36):10818–10825

    Article  CAS  Google Scholar 

  215. Shen H, Zhou M, Zhang Q, Keller A, Shen Y (2015) Zwitterionic light-responsive polymeric micelles for controlled drug delivery. Colloid Polym Sci 293:1685

    Article  CAS  Google Scholar 

  216. Liu J, Bu W, Pan L, Shi J (2013) NIR-triggered anticancer drug delivery by upconverting nanoparticles with integrated azobenzene-modified mesoporous silica. Angew Chem 52(16):4375–4379

    Article  CAS  Google Scholar 

  217. Dong M, Babalhavaeji A, Samanta S, Beharry AA, Woolley GA (2015) Red-shifting azobenzene photoswitches for in vivo use. Acc Chem Res 48(10):2662–2670

    Article  CAS  PubMed  Google Scholar 

  218. Yao C, Wang P, Li X, Hu X, Hou J, Wang L et al (2016) Near-infrared-triggered azobenzene-liposome/upconversion nanoparticle hybrid vesicles for remotely controlled drug delivery to overcome cancer multidrug resistance. Adv Mater 28(42):9341–9348

    Article  CAS  PubMed  Google Scholar 

  219. Moratz J, Samanta A, Voskuhl J, Mohan Nalluri SK, Ravoo BJ (2015) Light-triggered capture and release of DNA and proteins by host-guest binding and electrostatic interaction. Chemistry 21(8):3271–3277

    Article  CAS  PubMed  Google Scholar 

  220. National Toxicology P (1979) Bioassay of azobenzene for possible carcinogenicity. Natl Cancer Inst Carcinog Tech Rep Ser 154:1–131

    Google Scholar 

  221. Leung SJ, Kachur XM, Bobnick MC, Romanowski M (2011) Wavelength-selective light-induced release from plasmon resonant liposomes. Adv Func Mater 21(6):1113–1121

    Article  CAS  Google Scholar 

  222. Mathiyazhakan M, Wiraja C, Xu C (2018) A concise review of gold nanoparticles-based photo-responsive liposomes for controlled drug delivery. Nano-micro Lett 10(1):10

    Article  CAS  Google Scholar 

  223. Florentsen CD, West AV, Danielsen HMD, Semsey S, Bendix PM, Oddershede LB (2018) Quantification of loading and laser-assisted release of RNA from single gold nanoparticles. Langmuir ACS J Surf Colloids 34(49):14891–14898

    Article  CAS  Google Scholar 

  224. Zhang P, Wang C, Zhao J, Xiao A, Shen Q, Li L et al (2016) Near infrared-guided smart nanocarriers for MicroRNA-controlled release of doxorubicin/siRNA with intracellular ATP as fuel. ACS Nano 10(3):3637–3647

    Article  CAS  PubMed  Google Scholar 

  225. Iturrioz-Rodriguez N, Correa-Duarte MA, Fanarraga ML (2019) Controlled drug delivery systems for cancer based on mesoporous silica nanoparticles. Int J Nanomed 14:3389–3401

    Article  CAS  Google Scholar 

  226. Wang F, Zhang L, Bai X, Cao X, Jiao X, Huang Y et al (2018) Stimuli-responsive nanocarrier for co-delivery of MiR-31 and doxorubicin to suppress high MtEF4 cancer. ACS Appl Mater Interfaces 10(26):22767–22775

    Article  CAS  PubMed  Google Scholar 

  227. Ma N, Li Y, Xu H, Wang Z, Zhang X (2010) Dual redox responsive assemblies formed from diselenide block copolymers. J Am Chem Soc 132(2):442–443

    Article  CAS  PubMed  Google Scholar 

  228. Deng X, Yin Z, Lu J, Li X, Shao L, Zhao C et al (2018) In situ monitoring of MicroRNA replacement efficacy and accurate imaging-guided cancer therapy through light-up inter-polyelectrolyte nanocomplexes. Adv Sci 5(4):1700542

    Article  CAS  Google Scholar 

  229. Kang Y, Lu L, Lan J, Ding Y, Yang J, Zhang Y et al (2018) Redox-responsive polymeric micelles formed by conjugating gambogic acid with bioreducible poly(amido amine)s for the co-delivery of docetaxel and MMP-9 shRNA. Acta Biomater 68:137–153

    Article  CAS  PubMed  Google Scholar 

  230. Ulijn VR (2006) Enzyme-responsive materials: a new class of smart biomaterials. J Mater Chem 16:2217–2225

    Article  CAS  Google Scholar 

  231. Li L, Wang J, Kong H, Zeng Y, Liu G (2018) Functional biomimetic nanoparticles for drug delivery and theranostic applications in cancer treatment. Sci Technol Adv Mater 19(1):771–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Zhu L, Perche F, Wang T, Torchilin VP (2014) Matrix metalloproteinase 2-sensitive multifunctional polymeric micelles for tumor-specific co-delivery of siRNA and hydrophobic drugs. Biomaterials 35(13):4213–4222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  233. Liu X, Tan N, Zhou Y, Wei H, Ren S, Yu F et al (2017) Delivery of antagomiR204-conjugated gold nanoparticles from PLGA sheets and its implication in promoting osseointegration of titanium implant in type 2 diabetes mellitus. Int J Nanomed 12:7089–7101

    Article  CAS  Google Scholar 

  234. Wu K, Song W, Zhao L, Liu M, Yan J, Andersen MO et al (2013) MicroRNA functionalized microporous titanium oxide surface by lyophilization with enhanced osteogenic activity. ACS Appl Mater Interfaces 5(7):2733–2744

    Article  CAS  PubMed  Google Scholar 

  235. Wang Z, Wu G, Feng Z, Bai S, Dong Y, Wu G et al (2015) Microarc-oxidized titanium surfaces functionalized with microRNA-21-loaded chitosan/hyaluronic acid nanoparticles promote the osteogenic differentiation of human bone marrow mesenchymal stem cells. Int J Nanomed 10:6675–6687

    CAS  Google Scholar 

  236. Chen Y, Gao DY, Huang L (2015) In vivo delivery of miRNAs for cancer therapy: challenges and strategies. Adv Drug Deliv Rev 81:128–141

    Article  CAS  PubMed  Google Scholar 

  237. Sahle FF, Gulfam M, Lowe TL (2018) Design strategies for physical-stimuli-responsive programmable nanotherapeutics. Drug Discov Today 23(5):992–1006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  238. Gilam A, Conde J, Weissglas-Volkov D, Oliva N, Friedman E, Artzi N et al (2016) Local microRNA delivery targets Palladin and prevents metastatic breast cancer. Nat Commun 7:12868

    Article  PubMed  PubMed Central  Google Scholar 

  239. Griffin S, Masood MI, Nasim MJ, Sarfraz M, Ebokaiwe AP, Schafer KH et al (2017) Natural nanoparticles: a particular matter inspired by nature. Antioxidants 7(1):3

    Article  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by Competitivity Operational Program, 2014-2020, entitled “Clinical and economical impact of personalized targeted anti-microRNA therapies in reconverting lung cancer chemoresistance”—CANTEMIR, no. 35/01.09.2016, MySMIS 103375, Project PN-III-P1-1.2-PCCDI-2017-0782 entitled “Advanced innovative approaches for predictive regenerative medicine”- REGMED, no. 65PCCDI/2018 and project PNCDI III 2015-2020 entitled “Increasing the performance of scientific research and technology transfer in translational medicine through the formation of a new generation of young researchers” – ECHITAS, no. 29PFE/18.10.2018 and project CNFIS-FDI-2019-0666, entitled “Sustenance and valorification of research of excellence in the domain of personalized medicine by internationalization and increasement of research activities visibility”.

Author information

Author notes

  1. Sanda Boca, Diana Gulei and Alina-Andreea Zimta contributed equally to this work.

Authors and Affiliations

  1. Nanobiophotonics and Laser Microspectroscopy Center, Interdisciplinary Research Institute on Bio-Nano-Sciences, Babes-Bolyai University, 42 T. Laurian, 400271, Cluj-Napoca, Romania

    Sanda Boca

  2. Research Center for Functional Genomics, Biomedicine and Translational Medicine, “Iuliu Hatieganu”, University of Medicine and Pharmacy, 23 Marinescu Street, 400337, Cluj-Napoca, Romania

    Sanda Boca, Lorand Magdo & Ioana Berindan-Neagoe

  3. MEDFUTURE-Research Center for Advanced Medicine, “Iuliu-Hatieganu” University of Medicine and Pharmacy, 23 Marinescu Street, Cluj-Napoca, Romania

    Diana Gulei, Alina-Andreea Zimta, Anca Onaciu, Adrian Bogdan Tigu & Ioana Berindan-Neagoe

  4. 5th Surgical Department, Municipal Hospital, Cluj-Napoca, Romania

    Calin Ionescu

  5. “Iuliu Hatieganu” University of Medicine and Pharmacy, Cluj-Napoca, Romania

    Calin Ionescu

  6. Department of Oncological Surgery and Gynecological Oncology, 400015, Cluj-Napoca, Romania

    Alexandru Irimie

  7. Department of Surgery, The Oncology Institute “Prof. Dr. Ion Chiricuta”, 400015, Cluj-Napoca, Romania

    Alexandru Irimie

  8. Department of Pathology, “Prof Dr. Ion Chiricuta” Oncology Institute, Cluj-Napoca, Romania

    Rares Buiga

  9. Department of Functional Genomics and Experimental Pathology, The Oncology Institute “Prof. Dr. Ion Chiricuta”, 34-36 Republicii Street, Cluj-Napoca, Romania

    Ioana Berindan-Neagoe

Authors
  1. Sanda Boca
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diana Gulei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alina-Andreea Zimta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anca Onaciu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lorand Magdo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Adrian Bogdan Tigu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Calin Ionescu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alexandru Irimie
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rares Buiga
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ioana Berindan-Neagoe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Rares Buiga or Ioana Berindan-Neagoe.

Ethics declarations

Conflict of interest

Authors have no conflicts of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boca, S., Gulei, D., Zimta, AA. et al. Nanoscale delivery systems for microRNAs in cancer therapy. Cell. Mol. Life Sci. 77, 1059–1086 (2020). https://doi.org/10.1007/s00018-019-03317-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-019-03317-9

Keywords

Search

Navigation