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Cadmium nanoclusters in a protein matrix: Synthesis, characterization, and application in targeted drug delivery and cellular imaging

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A Publisher's Erratum to this article was published on 20 August 2018

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Abstract

Biotemplated metal nanoclusters have garnered much attention owing to their wide range of potential applications in biosensing, bioimaging, catalysis, and nanomedicine. Here, we report the synthesis of stable, biocompatible, water-soluble, and highly fluorescent bovine serum albumin-templated cadmium nanoclusters (CdNCs) through a facile one-pot green method. We covalently conjugated hyaluronic acid (HA) to the CdNCs to form a pH-responsive, tumortargeting theranostic nanocarrier with a sustained release profile for doxorubicin (DOX), a model anticancer drug. The nanocarrier showed a DOX encapsulation efficiency of about 75.6%. DOX release profiles revealed that 74% of DOX was released at pH 5.3, while less than 26% of DOX was released at pH 7.4 within the same 24-h period. The nanocarrier selectively recognized MCF-7 breast cancer cells expressing CD44, a cell surface receptor for HA, whereas no such recognition was observed with HA receptor-negative HEK293 cells. Biocompatibility of the nanocarrier was evaluated through cytotoxicity assays with HEK293 and MCF-7 cells. The nanocarrier exhibited very low to no cytotoxicity, whereas the DOX-loaded nanocarrier showed considerable cellular uptake and enhanced MCF-7 breast cancer cell-killing ability. We also confirmed the feasibility of using the highly fluorescent nanoconjugate for bioimaging of MCF-7 and HeLa cells. The superior targeted drug delivery efficacy, cellular imaging capability, and low cytotoxicity position this nanoconjugate as an exciting new nanoplatform with promising biomedical applications.

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  • 20 August 2018

    The Electronic Supplementary Material available online erroneously only contains the first six pages of the entire supplementary material file. You will find the entire supplementary material file online linked to this publisher?s erratum. The publisher apologizes to the authors and readers for this mistake.

References

  1. Pelaz, B.; Jaber, S.; de Aberasturi, D. J.; Wulf, V.; Aida, T.; de la Fuente, J. M.; Feldmann, J.; Gaub, H. E.; Josephson, L.; Kagan, C. R. et al. The state of nanoparticle-based nanoscience and biotechnology: Progress, promises, and challenges. ACS Nano 2012, 6, 8468–8483.

    Article  Google Scholar 

  2. Ye, E. Y.; Regulacio, M. D.; Zhang, S. Y.; Loh, X. J.; Han, M. Y. Anisotropically branched metal nanostructures. Chem. Soc. Rev. 2015, 44, 6001–6017.

    Article  Google Scholar 

  3. Pendashteh, A.; Mousavi, M. F.; Rahmanifar, M. S. Fabrication of anchored copper oxide nanoparticles on graphene oxide nanosheets via an electrostatic coprecipitation and its application as supercapacitor. Electrochim. Acta 2013, 88, 347–357.

    Article  Google Scholar 

  4. Kumar, A.; Kumar, V. Biotemplated inorganic nanostructures: Supramolecular directed nanosystems of semiconductor(s)/ metal(s) mediated by nucleic acids and their properties. Chem. Rev. 2014, 114, 7044–7078.

    Article  Google Scholar 

  5. Mehdinla, A.; Mousavi, M. F. Enhancing extraction rate in solid-phase microextraction by using nano-structured polyaniline coating. J. Sep. Sci. 2008, 31, 3565–3572.

    Article  Google Scholar 

  6. Ghanbari, K.; Bathaie, S. Z.; Mousavi, M. F. Electrochemically fabricated polypyrrole nanofiber-modified electrode as a new electrochemical DNA biosensor. Biosens. Bioelectron. 2008, 23, 1825–1831.

    Article  Google Scholar 

  7. Yousef Elahi, M.; Bathaie, S. Z.; Kazemi, S. H.; Mousavi, M. F. DNA immobilization on a polypyrrole nanofiber modified electrode and its interaction with salicylic acid/aspirin. Anal. Biochem. 2011, 411, 176–184.

    Article  Google Scholar 

  8. Yousef Elahi, M.; Bathaie, S. Z.; Mousavi, M. F.; Hoshyar, R.; Ghasemi, S. A new DNA-nanobiosensor based on G-quadruplex immobilized on carbon nanotubes modified glassy carbon electrode. Electrochim. Acta 2012, 82, 143–151.

    Google Scholar 

  9. Ilkhani, H.; Sarparast, M.; Noori, A.; Bathaie, S. Z.; Mousavi, M. F. Electrochemical aptamer/antibody based sandwich immunosensor for the detection of EGFR, a cancer biomarker, using gold nanoparticles as a signaling probe. Biosens. Bioelectron. 2015, 74, 491–497.

    Article  Google Scholar 

  10. Moradi, N.; Mousavi, M. F.; Mehrgardi, M. A.; Noori, A. Preparation of a new electrochemical biosensor for single base mismatch detection in DNA. Anal. Methods 2013, 5, 6531–6538.

    Article  Google Scholar 

  11. Wu, N. Q.; Fu, L.; Su, M.; Aslam, M.; Wong, K. C.; Dravid, V. P. Interaction of fatty acid monolayers with cobalt nanoparticles. Nano Lett. 2004, 4, 383–386.

    Article  Google Scholar 

  12. Bagheryan, Z.; Noori, A.; Bathaie, S. Z.; Yousef-Elahi, M.; Mousavi, M. F. Preparation of a new nanobiosensor for the determination of some biogenic polyamines and investigation of their interaction with DNA. Biosens. Bioelectron. 2016, 77, 767–773.

    Article  Google Scholar 

  13. Xue, T.; Peng, B.; Xue, M.; Zhong, X.; Chiu, C. Y.; Yang, S.; Qu, Y. Q.; Ruan, L. Y.; Jiang, S.; Dubin, S. et al. Integration of molecular and enzymatic catalysts on graphene for biomimetic generation of antithrombotic species. Nat. Commun. 2014, 5, 3200.

    Google Scholar 

  14. Song, H. Metal hybrid nanoparticles for catalytic organic and photochemical transformations. Acc. Chem. Res. 2015, 48, 491–499.

    Article  Google Scholar 

  15. Bao, G.; Mitragotri, S.; Tong, S. Multifunctional nanoparticles for drug delivery and molecular imaging. Annu. Rev. Biomed. Eng. 2013, 15, 253–282.

    Article  Google Scholar 

  16. Doane, T. L.; Burda, C. The unique role of nanoparticles in nanomedicine: Imaging, drug delivery and therapy. Chem. Soc. Rev. 2012, 41, 2885–2911.

    Article  Google Scholar 

  17. Hong, A. J.; Song, E. B.; Yu, H. S.; Allen, M. J.; Kim, J.; Fowler, J. D.; Wassei, J. K.; Park, Y.; Wang, Y.; Zou, J. et al. Graphene flash memory. ACS Nano 2011, 5, 7812–7817.

    Article  Google Scholar 

  18. Olivieri, A.; Chen, C. K.; Hassan, S.; Lisicka-Skrzek, E.; Tait, R. N.; Berini, P. Plasmonic nanostructured metaloxide- semiconductor reflection modulators. Nano Lett. 2015, 15, 2304–2311.

    Article  Google Scholar 

  19. Shao, Y. L.; El-Kady, M. F.; Wang, L. J.; Zhang, Q. H.; Li, Y. G.; Wang, H. Z.; Mousavi, M. F.; Kaner, R. B. Graphenebased materials for flexible supercapacitors. Chem. Soc. Rev. 2015, 44, 3639–3665.

    Article  Google Scholar 

  20. Lu, Y. Z.; Chen, W. Sub-nanometre sized metal clusters: From synthetic challenges to the unique property discoveries. Chem. Soc. Rev. 2012, 41, 3594–3623.

    Article  Google Scholar 

  21. Wen, X. M.; Yu, P.; Toh, Y.-R.; Tang, J. Quantum confined stark effect in Au8 and Au25 nanoclusters. J. Phys. Chem. C 2013, 117, 3621–3626.

    Article  Google Scholar 

  22. Ghosh, R.; Sahoo, A. K.; Ghosh, S. S.; Paul, A.; Chattopadhyay, A. Blue-emitting copper nanoclusters synthesized in the presence of lysozyme as candidates for cell labeling. ACS Appl. Mater. Interfaces 2014, 6, 3822–3828.

    Article  Google Scholar 

  23. Mathew, A.; Pradeep, T. Noble metal clusters: Applications in energy, environment, and biology. Part. Part. Syst. Charact. 2014, 31, 1017–1053.

    Article  Google Scholar 

  24. Molaabasi, F.; Hosseinkhani, S.; Moosavi-Movahedi, A. A.; Shamsipur, M. Hydrogen peroxide sensitive hemoglobincapped gold nanoclusters as a fluorescence enhancing sensor for the label-free detection of glucose. RSC Adv. 2015, 5, 33123–33135.

    Article  Google Scholar 

  25. Tiwari, J. N.; Nath, K.; Kumar, S.; Tiwari, R. N.; Kemp, K. C.; Le, N. H.; Youn, D. H.; Lee, J. S.; Kim, K. S. Stable platinum nanoclusters on genomic DNA-graphene oxide with a high oxygen reduction reaction activity. Nat. Commun. 2013, 4, 2221.

    Article  Google Scholar 

  26. Qin, W.; Lohrman, J.; Ren, S. Q. Magnetic and optoelectronic properties of gold nanocluster-thiophene assembly. Angew Chem., Int. Ed. 2014, 53, 7316–7319.

    Article  Google Scholar 

  27. Khandelia, R.; Bhandari, S.; Pan, U. N.; Ghosh, S. S.; Chattopadhyay, A. Gold nanocluster embedded albumin nanoparticles for two-photon imaging of cancer cells accompanying drug delivery. Small 2015, 11, 4075–4081.

    Article  Google Scholar 

  28. Jin, R. C. Atomically precise metal nanoclusters: Stable sizes and optical properties. Nanoscale 2015, 7, 1549–1565.

    Article  Google Scholar 

  29. Wu, Z. K.; Jin, R. C. On the ligand's role in the fluorescence of gold nanoclusters. Nano Lett. 2010, 10, 2568–2573.

    Article  Google Scholar 

  30. Wan, X. K.; Lin, Z. W.; Wang, Q. M. Au20 nanocluster protected by hemilabile phosphines. J. Am. Chem. Soc. 2012, 134, 14750–14752.

    Article  Google Scholar 

  31. Tanaka, S. I.; Miyazaki, J.; Tiwari, D. K.; Jin, T.; Inouye, Y. Fluorescent platinum nanoclusters: Synthesis, purification, characterization, and application to bioimaging. Angew Chem., Int. Ed. 2011, 50, 431–435.

    Article  Google Scholar 

  32. Zhang, Y.; Zhu, C. F.; Zhang, L.; Tan, C. L.; Yang, J.; Chen, B.; Wang, L. H.; Zhang, H. DNA-templated silver nanoclusters for multiplexed fluorescent DNA detection. Small 2015, 11, 1385–1389.

    Article  Google Scholar 

  33. Jia, X. F.; Li, J.; Han, L.; Ren, J. T.; Yang, X.; Wang, E. K. DNA-hosted copper nanoclusters for fluorescent identification of single nucleotide polymorphisms. ACS Nano 2012, 6, 3311–3317.

    Article  Google Scholar 

  34. Cui, Y. Y.; Wang, Y. L.; Liu, R. L.; Sun, Z. P.; Wei, Y. T.; Zhao, Y. L.; Gao, X. Y. Serial silver clusters biomineralized by one peptide. ACS Nano 2011, 5, 8684–8689.

    Article  Google Scholar 

  35. Song, W.; Liang, R. P.; Wang, Y.; Zhang, L.; Qiu, J. D. Green synthesis of peptide-templated gold nanoclusters as novel fluorescence probes for detecting protein kinase activity. Chem. Commun. 2015, 51, 10006–10009.

    Article  Google Scholar 

  36. Chen, H.; Lin, L.; Li, H. F.; Li, J. Z.; Lin, J. M. Aggregation-induced structure transition of protein-stabilized zinc/copper nanoclusters for amplified chemiluminescence. ACS Nano 2015, 9, 2173–2183.

    Article  Google Scholar 

  37. Wang, Y. L.; Chen, J. J.; Irudayaraj, J. Nuclear targeting dynamics of gold nanoclusters for enhanced therapy of HER2+ breast cancer. ACS Nano 2011, 5, 9718–9725.

    Article  Google Scholar 

  38. Goswami, N.; Zheng, K. Y.; Xie, J. P. Bio-NCs—The marriage of ultrasmall metal nanoclusters with biomolecules. Nanoscale 2014, 6, 13328–13347.

    Article  Google Scholar 

  39. Xu, Y. L.; Sherwood, J.; Qin, Y.; Crowley, D.; Bonizzoni, M.; Bao, Y. P. The role of protein characteristics in the formation and fluorescence of Au nanoclusters. Nanoscale 2014, 6, 1515–1524.

    Article  Google Scholar 

  40. Goswami, N.; Baksi, A.; Giri, A.; Xavier, P. L.; Basu, G.; Pradeep, T.; Pal, S. K. Luminescent iron clusters in solution. Nanoscale 2014, 6, 1848–1854.

    Article  Google Scholar 

  41. Le Guével, X.; Hötzer, B.; Jung, G.; Hollemeyer, K.; Trouillet, V.; Schneider, M. Formation of fluorescent metal (Au, Ag) nanoclusters capped in bovine serum albumin followed by fluorescence and spectroscopy. J. Phys. Chem. C 2011, 115, 10955–10963.

    Article  Google Scholar 

  42. Chen, Y. N.; Chen, P. C.; Wang, C. W.; Lin, Y. S.; Ou, C. M.; Ho, L. C.; Chang, H. T. One-pot synthesis of fluorescent BSA-Ce/Au nanoclusters as ratiometric pH probes. Chem. Commun. 2014, 50, 8571–8574.

    Article  Google Scholar 

  43. Dong, L. Y.; Li, M. L.; Zhang, S.; Li, J.; Shen, G. X.; Tu, Y. T.; Zhu, J. T.; Tao, J. Cytotoxicity of BSA-stabilized gold nanoclusters: In vitro and in vivo study. Small 2015, 11, 2571–2581.

    Article  Google Scholar 

  44. Ghosh, S.; Das, N. K.; Anand, U.; Mukherjee, S. Photostable copper nanoclusters: Compatible Förster resonance energytransfer assays and a nanothermometer. J. Phys. Chem. Lett. 2015, 6, 1293–1298.

    Article  Google Scholar 

  45. Abbaspour, A.; Noori, A. Electrochemical detection of individual single nucleotide polymorphisms using monobasemodified apoferritin-encapsulated nanoparticles. Biosens. Bioelectron. 2012, 37, 11–18.

    Article  Google Scholar 

  46. Chen, T.; Xu, S.; Zhao, T.; Zhu, L.; Wei, D. F.; Li, Y. Y.; Zhang, H. X.; Zhao, C. Y. Gold nanocluster-conjugated amphiphilic block copolymer for tumor-targeted drug delivery. ACS Appl. Mater. Interfaces 2012, 4, 5766–5774.

    Article  Google Scholar 

  47. Zhang, P.; Yang, X. X.; Wang, Y.; Zhao, N. W.; Xiong, Z. H.; Huang, C. Z. Rapid synthesis of highly luminescent and stable Au20 nanoclusters for active tumor-targeted imaging in vitro and in vivo. Nanoscale 2014, 6, 2261–2269.

    Article  Google Scholar 

  48. Weng, J. F.; Ren, J. C. Luminescent quantum dots: A very attractive and promising tool in biomedicine. Curr. Med. Chem. 2006, 13, 897–909.

    Article  Google Scholar 

  49. Das, T.; Ghosh, P.; Shanavas, M. S.; Maity, A.; Mondal, S.; Purkayastha, P. Protein-templated gold nanoclusters: Size dependent inversion of fluorescence emission in the presence of molecular oxygen. Nanoscale 2012, 4, 6018–6024.

    Article  Google Scholar 

  50. Zhou, W. J.; Cao, Y. Q.; Sui, D. D.; Guan, W. J.; Lu, C.; Xie, J. P. Ultrastable BSA-capped gold nanoclusters with a polymer-like shielding layer against reactive oxygen species in living cells. Nanoscale 2016, 8, 9614–9620.

    Article  Google Scholar 

  51. Chou, L. Y. T.; Chan, W. C. W. Nanotoxicology: No signs of illness. Nat. Nanotechnol. 2012, 7, 416–417.

    Article  Google Scholar 

  52. Xia, X. D.; Zhang, Y.; Wang, J. X. Novel fabrication of highly fluorescent Pt nanoclusters and their applications in hypochlorite assay. RSC Adv. 2014, 4, 25365–25368.

    Article  Google Scholar 

  53. Ji, J. W.; Wang, G.; Wang, T. W.; You, X. Z.; Xu, X. X. Thiolate-protected Ni39 and Ni41 nanoclusters: Synthesis, self-assembly and magnetic properties. Nanoscale 2014, 6, 9185–9191.

    Article  Google Scholar 

  54. Goswami, N.; Giri, A.; Bootharaju, M. S.; Xavier, P. L.; Pradeep, T.; Pal, S. K. Copper quantum clusters in protein matrix: Potential sensor of Pb2+ ion. Anal. Chem. 2011, 83, 9676–9680.

    Article  Google Scholar 

  55. Ghosh, S. C.; Neslihan Alpay, S.; Klostergaard, J. CD44: A validated target for improved delivery of cancer therapeutics. Expert Opin. Ther. Targets 2012, 16, 635–650.

    Article  Google Scholar 

  56. Zhang, L. W.; Gao, S.; Zhang, F.; Yang, K.; Ma, Q. J.; Zhu, L. Activatable hyaluronic acid nanoparticle as a theranostic agent for optical/photoacoustic image-guided photothermal therapy. ACS Nano 2014, 8, 12250–12258.

    Article  Google Scholar 

  57. Wei, X.; Senanayake, T. H.; Warren, G.; Vinogradov, S. V. Hyaluronic acid-based nanogel-drug conjugates with enhanced anticancer activity designed for the targeting of CD44-positive and drug-resistant tumors. Bioconjug. Chem. 2013, 24, 658–668.

    Article  Google Scholar 

  58. Kim, K. S.; Hur, W.; Park, S. J.; Hong, S. W.; Choi, J. E.; Goh, E. J.; Yoon, S. K.; Hahn, S. K. Bioimaging for targeted delivery of hyaluronic Acid derivatives to the livers in cirrhotic mice using quantum dots. ACS Nano 2010, 4, 3005–3014.

    Article  Google Scholar 

  59. Abdullah-Al-Nahain J.-E.; Lee, J.-E.; In, I.; Lee, H.; Lee, K. D.; Jeong, J. H.; Park, S. Y. Target delivery and cell imaging using hyaluronic acid-functionalized graphene quantum dots. Mol. Pharm. 2013, 10, 3736–3744.

    Article  Google Scholar 

  60. Lim, E.-K.; Kim, H.-O.; Jang, E.; Park, J.; Lee, K.; Suh, J.-S.; Huh, Y.-M.; Haam, S. Hyaluronan-modified magnetic nanoclusters for detection of CD44-overexpressing breast cancer by MRimaging. Biomaterials 2011, 32, 7941–7950.

    Article  Google Scholar 

  61. Lee, T.; Lim, E.-K.; Lee, J.; Kang, B.; Choi, J.; Park, H. S.; Suh, J.-S.; Huh, Y.-M.; Haam, S. Efficient CD44-targeted magnetic resonance imaging (MRI) of breast cancer cells using hyaluronic acid (HA)-modified MnFe2O4 nanocrystals. Nanoscale Res. Lett. 2013, 8, 149.

    Article  Google Scholar 

  62. Walter, M.; Akola, J.; Lopez-Acevedo, O.; Jadzinsky, P. D.; Calero, G.; Ackerson, C. J.; Whetten, R. L.; Grö nbeck, H.; Hä kkinen, H. A unified view of ligand-protected gold clusters as superatom complexes. Proc. Natl. Acad. Sci. USA 2008, 105, 9157–9162.

    Article  Google Scholar 

  63. Greenfield, N. J. Using circular dichroism spectra to estimate protein secondary structure. Nat. Protoc. 2006, 1, 2876–2890.

    Article  Google Scholar 

  64. Baksi, A.; Xavier, P. L.; Chaudhari, K.; Goswami, N.; Pal, S. K.; Pradeep, T. Protein-encapsulated gold cluster aggregates: The case of lysozyme. Nanoscale 2013, 5, 2009–2016.

    Article  Google Scholar 

  65. Xie, J. P.; Zheng, Y. G.; Ying, J. Y. Protein-directed synthesis of highly fluorescent gold nanoclusters. J. Am. Chem. Soc. 2009, 131, 888–889.

    Article  Google Scholar 

  66. Wang, C. S.; Li, J. Y.; Amatore, C.; Chen, Y.; Jiang, H.; Wang, X. M. Gold nanoclusters and graphene nanocomposites for drug delivery and imaging of cancer cells. Angew Chem., Int. Ed. 2011, 50, 11644–11648.

    Article  Google Scholar 

  67. Mohanty, P.; Park, J.; Lee, G.; Kim, B. Fabrication of single crystalline cadmium nanowires by a facile low temperature vapor phase method. J. Nanosci. Nanotechnol. 2006, 6, 3376–3379.

    Article  Google Scholar 

  68. Chaudhari, K.; Xavier, P. L.; Pradeep, T. Understanding the evolution of luminescent gold quantum clusters in protein templates. ACS Nano 2011, 5, 8816–8827.

    Article  Google Scholar 

  69. Nanda, J.; Kuruvilla, B. A.; Sarma, D. D. Photoelectron spectroscopic study of CdS nanocrystallites. Phys. Rev. B 1999, 59, 7473–7479.

    Article  Google Scholar 

  70. Peterson, M. D.; Jensen, S. C.; Weinberg, D. J.; Weiss, E. A. Mechanisms for adsorption of methyl viologen on CdS quantum dots. ACS Nano 2014, 8, 2826–2837.

    Article  Google Scholar 

  71. Trinh, T. T.; Mott, D.; Thanh, N. T. K.; Maenosono, S. One-pot synthesis and characterization of well defined core–shell structure of FePt@ CdSe nanoparticles. RSC Adv. 2011, 1, 100–108.

    Article  Google Scholar 

  72. Moholkar, A. V.; Agawane, G. L.; Sim, K.-U.; Kwon, Y.-B.; Choi, D. S.; Rajpure, K. Y.; Kim, J. H. Temperature dependent structural, luminescent and XPS studies of CdO: Ga thin films deposited by spray pyrolysis. J. Alloys Compd. 2010, 506, 794–799.

    Article  Google Scholar 

  73. Mohanty, J. S.; Xavier, P. L.; Chaudhari, K.; Bootharaju, M. S.; Goswami, N.; Pal, S. K.; Pradeep, T. Luminescent, bimetallic AuAg alloy quantum clusters in protein templates. Nanoscale 2012, 4, 4255–4262.

    Article  Google Scholar 

  74. Luo, Z. M.; Yang, D. L.; Qi, G. Q.; Shang, J. Z.; Yang, H. P.; Wang, Y. L.; Yuwen, L. H.; Yu, T.; Huang, W.; Wang, L. H. Microwave-assisted solvothermal preparation of nitrogen and sulfur co-doped reduced graphene oxide and graphene quantum dots hybrids for highly efficient oxygen reduction. J. Mater. Chem. A 2014, 2, 20605–20611.

    Article  Google Scholar 

  75. Makarova, A. A.; Grachova, E. V.; Neudachina, V. S.; Yashina, L. V.; Blü her, A.; Molodtsov, S. L.; Mertig, M.; Ehrlich, H.; Adamchuk, V. K.; Laubschat, C. et al. Insight into bio-metal interface formation in vacuo: Interplay of S-layer protein with copper and iron. Sci. Rep. 2015, 5, 8710.

    Article  Google Scholar 

  76. Wagner, A. J.; Wolfe, G. M.; Fairbrother, D. H. Reactivity of vapor-deposited metal atoms with nitrogen-containing polymers and organic surfaces studied by in situ XPS. Appl. Surf. Sci. 2003, 219, 317–328.

    Article  Google Scholar 

  77. Cho, K.; Wang, X.; Nie, S. M.; Chen, Z.; Shin, D. M. Therapeutic nanoparticles for drug delivery in cancer. Clin. Cancer Res. 2008, 14, 1310–1316.

    Article  Google Scholar 

  78. Zhang, C. L.; Li, C.; Liu, Y. L.; Zhang, J. P.; Bao, C. C.; Liang, S. J.; Wang, Q.; Yang, Y.; Fu, H. L.; Wang, K. et al. Gold nanoclusters-based nanoprobes for simultaneous fluorescence imaging and targeted photodynamic therapy with superior penetration and retention behavior in tumors. Adv. Funct. Mater. 2015, 25, 1314–1325.

    Article  Google Scholar 

  79. Albanese, A.; Tang, P. S.; Chan, W. C. W. The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu. Rev. Biomed. Eng. 2012, 14, 1–16.

    Article  Google Scholar 

  80. Zhou, M.; Li, J. J.; Liang, S.; Sood, A. K.; Liang, D.; Li, C. CuS nanodots with ultrahigh efficient renal clearance for positron emission tomography imaging and image-guided photothermal therapy. ACS Nano 2015, 9, 7085–7096.

    Article  Google Scholar 

  81. Knop, K.; Hoogenboom, R.; Fischer, D.; Schubert, U. S. Poly(ethylene glycol) in drug delivery: Pros and cons as well as potential alternatives. Angew. Chem., Int. Ed. 2010, 49, 6288–6308.

    Article  Google Scholar 

  82. Song, E. Q.; Han, W. Y.; Li, C.; Cheng, D.; Li, L. R.; Liu, L. C.; Zhu, G. Z.; Song, Y.; Tan, W. H. Hyaluronic acid-decorated graphene oxide nanohybrids as nanocarriers for targeted and pH-responsive anticancer drug delivery. ACS Appl. Mater. Interfaces 2014, 6, 11882–11890.

    Article  Google Scholar 

  83. Yu, M. H.; Jambhrunkar, S.; Thorn, P.; Chen, J. Z.; Gu, W. Y.; Yu, C. Z. Hyaluronic acid modified mesoporous silica nanoparticles for targeted drug delivery to CD44-overexpressing cancer cells. Nanoscale 2013, 5, 178–183.

    Article  Google Scholar 

  84. Jayakumar, R.; Nair, A.; Rejinold, N. S.; Maya, S.; Nair, S. V. Doxorubicin-loaded pH-responsive chitin nanogels for drug delivery to cancer cells. Carbohydr. Polym. 2012, 87, 2352–2356.

    Article  Google Scholar 

  85. Zhou, Q.; Guo, X.; Chen, T.; Zhang, Z.; Shao, S. J.; Luo, C.; Li, J. R.; Zhou, S. B. Target-specific cellular uptake of folate-decorated biodegradable polymer micelles. J. Phys. Chem. B 2011, 115, 12662–12670.

    Article  Google Scholar 

  86. Palanikumar, L.; Choi, E. S.; Cheon, J. Y.; Joo, S. H.; Ryu, J. H. Noncovalent polymer-gatekeeper in mesoporous silica nanoparticles as a targeted drug delivery platform. Adv. Funct. Mater. 2015, 25, 957–965.

    Article  Google Scholar 

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Correspondence to Richard B. Kaner or Mir F. Mousavi.

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12274_2016_1201_MOESM1_ESM.pdf

Cadmium nanoclusters in a protein matrix: Synthesis, characterization, and application in targeted drug delivery and cellular imaging

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Sarparast, M., Noori, A., Ilkhani, H. et al. Cadmium nanoclusters in a protein matrix: Synthesis, characterization, and application in targeted drug delivery and cellular imaging. Nano Res. 9, 3229–3246 (2016). https://doi.org/10.1007/s12274-016-1201-z

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