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Advances in nanomaterial based optical biosensing and bioimaging of apoptosis via caspase-3 activity: a review

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Abstract

Caspase-3 plays a vital role in intrinsic and extrinsic pathways of programed cell death and in cell proliferation. Its detection is an important tool for early detection of some cancers and apoptosis-related diseases, and for monitoring the efficacy of pharmaceuticals and of chemo- and radiotherapy of cancers. This review (with 72 references) summarizes nanomaterial based methods for signal amplification in optical methods for the determination of caspase-3 activity. Following an introduction into the field, a first large section covers optical assays, with subsections on luminescent and chemiluminescence, fluorometric (including FRET based), and colorimetric assays. Further section summarize methods for bioimaging of caspase-3. A concluding section covers current challenges and future perspectives.

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References

  1. Shi H, Kwok RTK, Liu J, Xing B, Tang BZ, Liu B (2012) Real-Time Monitoring of Cell Apoptosis and Drug Screening Using Fluorescent Light-Up Probe with Aggregation-Induced Emission Characteristics. J Am Chem Soc 134(43):17972–17981. https://doi.org/10.1021/ja3064588

    Article  CAS  PubMed  Google Scholar 

  2. Hu X, Su D, Du Z, Huang X, Dong C, Ren J (2016) A single particle method for direct determination of molar concentrations of gold nanoparticles, and its application to the determination of the activity of caspase 3 and drug-induced cell apoptosis. Microchim Acta 183(8):2457–2465. https://doi.org/10.1007/s00604-016-1891-7

    Article  CAS  Google Scholar 

  3. D'Amelio M, Cavallucci V, Cecconi F (2009) Neuronal caspase-3 signaling: not only cell death. Cell Death Differ 17:1104. https://doi.org/10.1038/cdd.2009.180

    Article  CAS  PubMed  Google Scholar 

  4. Wang H, Zhang Q, Chu X, Chen T, Ge J, Yu R (2011) Graphene oxide–peptide conjugate as an intracellular protease sensor for caspase-3 activation imaging in live cells. Angew Chem Int Ed 50(31):7065–7069

    Article  CAS  Google Scholar 

  5. Zhang Y, Mu Y, Zhou C, Song Q, Jin W, Jin Q (2012) Detection of mismatched caspase-3 DNA oligonucleotides with an SPR biosensor following amplification by Taq polymerase. Microchim Acta 177(3):435–441. https://doi.org/10.1007/s00604-012-0799-0

    Article  CAS  Google Scholar 

  6. Khalilzadeh B, Shadjou N, Charoudeh HN, Rashidi M-R (2017) Recent advances in electrochemical and electrochemiluminescence based determination of the activity of caspase-3. Microchim Acta 184(10):3651–3662. https://doi.org/10.1007/s00604-017-2466-y

    Article  CAS  Google Scholar 

  7. Borisov SM, Wolfbeis OS (2008) Optical Biosensors. Chem Rev 108(2):423–461. https://doi.org/10.1021/cr068105t

    Article  CAS  PubMed  Google Scholar 

  8. Yoo SM, Lee SY (2016) Optical Biosensors for the Detection of Pathogenic Microorganisms. Trends Biotechnol 34(1):7–25. https://doi.org/10.1016/j.tibtech.2015.09.012

    Article  CAS  PubMed  Google Scholar 

  9. Afsharan H, Khalilzadeh B, Tajalli H, Mollabashi M, Navaeipour F, Rashidi M-R (2016) A sandwich type immunosensor for ultrasensitive electrochemical quantification of p53 protein based on gold nanoparticles/graphene oxide. Electrochim Acta 188:153–164. https://doi.org/10.1016/j.electacta.2015.11.133

    Article  CAS  Google Scholar 

  10. Afsharan H, Navaeipour F, Khalilzadeh B, Tajalli H, Mollabashi M, Ahar MJ, Rashidi M-R (2016) Highly sensitive electrochemiluminescence detection of p53 protein using functionalized Ru–silica nanoporous@gold nanocomposite. Biosens Bioelectron 80:146–153. https://doi.org/10.1016/j.bios.2016.01.030

    Article  CAS  PubMed  Google Scholar 

  11. Khalilzadeh B, Charoudeh HN, Shadjou N, Mohammad-Rezaei R, Omidi Y, Velaei K, Aliyari Z, Rashidi M-R (2016) Ultrasensitive caspase-3 activity detection using an electrochemical biosensor engineered by gold nanoparticle functionalized MCM-41: Its application during stem cell differentiation. Sensors Actuators B Chem 231:561–575. https://doi.org/10.1016/j.snb.2016.03.043

    Article  CAS  Google Scholar 

  12. Khalilzadeh B, Shadjou N, Afsharan H, Eskandani M, Nozad Charoudeh H, Rashidi M-R (2016) Reduced graphene oxide decorated with gold nanoparticle as signal amplification element on ultra-sensitive electrochemiluminescence determination of caspase-3 activity and apoptosis using peptide based biosensor. Bioimpacts 6(3):135–147. https://doi.org/10.15171/bi.2016.20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Khalilzadeh B, Shadjou N, Eskandani M, Charoudeh HN, Omidi Y, Rashidi M-R (2015) A reliable self-assembled peptide based electrochemical biosensor for detection of caspase 3 activity and apoptosis. RSC Advances 5(72):58316–58326. https://doi.org/10.1039/C5RA08561F

    Article  CAS  Google Scholar 

  14. Boeneman K, Mei BC, Dennis AM, Bao G, Deschamps JR, Mattoussi H, Medintz IL (2009) Sensing Caspase 3 Activity with Quantum Dot−Fluorescent Protein Assemblies. J Am Chem Soc 131(11):3828–3829. https://doi.org/10.1021/ja809721j

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Eskandani M, Barar J, Ezzati Nazhad Dolatabadi J, Hamishehkar H, Nazemiyeh H (2015) Formulation, characterization, and geno/cytotoxicity studies of galbanic acid-loaded solid lipid nanoparticles. Pharm Biol 53(10):1525–1538. https://doi.org/10.3109/13880209.2014.991836

    Article  CAS  PubMed  Google Scholar 

  16. Balal K, Mohammad H, Bahareh B, Ali B, Maryam H, Mozhgan Z (2009) Zeolite Nanoparticle Modified Carbon Paste Electrode as a Biosensor for Simultaneous Determination of Dopamine and Tryptophan. J Chin Chem Soc 56(4):789–796. https://doi.org/10.1002/jccs.200900117

    Article  CAS  Google Scholar 

  17. Karim-Nezhad G, Hasanzadeh M, Saghatforoush L, Shadjou N, Khalilzadeh B, Ershad S (2009) Electro-oxidation of ascorbic acid catalyzed on cobalt hydroxide-modified glassy carbon electrode. J Serb Chem Soc 74(5):581–593

    Article  CAS  Google Scholar 

  18. Khalilzadeh B, Hasanzadeh M, Sanati S, Saghatforoush L, Shadjou N, Dolatabadi JEN, Sheikhzadeh P (2011) Preparation of a new electrochemical sensor based on cadmium oxide nanoparticles and application for determination of penicillamine. Int J Electrochem Sci 6:4164–4175

    CAS  Google Scholar 

  19. Saghatforoush L, Hasanzadeh M, Karim-Nezhad G, Ershad S, Shadjou N, Khalilzadeh B, Hajjizadeh M (2009) Kinetic study of the electrooxidation of mefenamic acid and indomethacin catalysed on cobalt hydroxide modified glassy carbon electrode. Bull Kor Chem Soc 30(6):1341–1348

    Article  CAS  Google Scholar 

  20. Pan Y, Guo M, Nie Z, Huang Y, Peng Y, Liu A, Qing M, Yao S (2012) Colorimetric detection of apoptosis based on caspase-3 activity assay using unmodified gold nanoparticles. Chem Commun 48(7):997–999. https://doi.org/10.1039/C1CC15407A

    Article  CAS  Google Scholar 

  21. Prasuhn DE, Feltz A, Blanco-Canosa JB, Susumu K, Stewart MH, Mei BC, Yakovlev AV, Loukou C, Mallet J-M, Oheim M, Dawson PE, Medintz IL (2010) Quantum Dot Peptide Biosensors for Monitoring Caspase 3 Proteolysis and Calcium Ions. ACS Nano 4(9):5487–5497. https://doi.org/10.1021/nn1016132

    Article  CAS  PubMed  Google Scholar 

  22. BØtter-Jensen L (1997) Luminescence techniques: instrumentation and methods. Radiat Meas 27(5):749–768. https://doi.org/10.1016/S1350-4487(97)00206-0

    Article  Google Scholar 

  23. Jimenez AM, Navas MJ (2002) Chemiluminescence methods (present and future). Grasas y Aceites 53(1):64–57. https://doi.org/10.3989/gya.2002.v53.i1.290

  24. Torkzadeh-Mahani M, Ataei F, Nikkhah M, Hosseinkhani S (2012) Design and development of a whole-cell luminescent biosensor for detection of early-stage of apoptosis. Biosens Bioelectron 38(1):362–368. https://doi.org/10.1016/j.bios.2012.06.034

    Article  CAS  PubMed  Google Scholar 

  25. Chen J, Stefflova K, Niedre MJ, Wilson BC, Chance B, Glickson JD, Zheng G (2004) Protease-Triggered Photosensitizing Beacon Based on Singlet Oxygen Quenching and Activation. J Am Chem Soc 126(37):11450–11451. https://doi.org/10.1021/ja047392k

    Article  CAS  PubMed  Google Scholar 

  26. Lin S-Y, Chen N-T, Sun S-P, Chang JC, Wang Y-C, Yang C-S, Lo L-W (2010) The Protease-Mediated Nucleus Shuttles of Subnanometer Gold Quantum Dots for Real-Time Monitoring of Apoptotic Cell Death. J Am Chem Soc 132(24):8309–8315. https://doi.org/10.1021/ja100561k

    Article  CAS  PubMed  Google Scholar 

  27. Richard J-A, Jean L, Romieu A, Massonneau M, Noack-Fraissignes P, Renard P-Y (2007) Chemiluminescent Probe for the in Vitro Detection of Protease Activity. Org Lett 9(23):4853–4855. https://doi.org/10.1021/ol702190y

    Article  CAS  PubMed  Google Scholar 

  28. Richard J-A, Jean L, Schenkels C, Massonneau M, Romieu A, Renard P-Y (2009) Self-cleavable chemiluminescent probes suitable for protease sensing. Org Biomol Chem 7(14):2941–2957. https://doi.org/10.1039/B905725K

    Article  CAS  PubMed  Google Scholar 

  29. Li Y (2012) Chemiluminescent determination of the activity of caspase-3 using a specific peptide substrate and magnetic beads. Microchim Acta 177(3-4):443–447. https://doi.org/10.1007/s00604-012-0798-1

    Article  CAS  Google Scholar 

  30. Huang X, Liang Y, Ruan L, Ren J (2014) Chemiluminescent detection of cell apoptosis enzyme by gold nanoparticle-based resonance energy transfer assay. Anal Bioanal Chem 406(23):5677–5684. https://doi.org/10.1007/s00216-013-7611-9

    Article  CAS  PubMed  Google Scholar 

  31. Kumaraswamy S, Bergstedt T, Shi X, Rininsland F, Kushon S, Xia W, Ley K, Achyuthan K, McBranch D, Whitten D (2004) Fluorescent-conjugated polymer superquenching facilitates highly sensitive detection of proteases. Proc Natl Acad Sci U S A 101(20):7511–7515. https://doi.org/10.1073/pnas.0402367101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Wang H, Zhang Q, Chu X, Chen T, Ge J, Yu R (2011) Graphene Oxide–Peptide Conjugate as an Intracellular Protease Sensor for Caspase-3 Activation Imaging in Live Cells. Angew Chem Int Ed 50(31):7065–7069. https://doi.org/10.1002/anie.201101351

    Article  CAS  Google Scholar 

  33. Rahman MS, Kabashima T, Yasmin H, Shibata T, Kai M (2013) A novel fluorescence reaction for N-terminal Ser-containing peptides and its application to assay caspase activity. Anal Biochem 433(2):79–85. https://doi.org/10.1016/j.ab.2012.10.018

    Article  CAS  PubMed  Google Scholar 

  34. Saito K, Wada I, Tamura M, Kinjo M (2004) Direct detection of caspase-3 activation in single live cells by cross-correlation analysis. Biochem Biophys Res Commun 324(2):849–854. https://doi.org/10.1016/j.bbrc.2004.09.126

    Article  CAS  PubMed  Google Scholar 

  35. Zhang J, Wang X, Cui W, Wang W, Zhang H, Liu L, Zhang Z, Li Z, Ying G, Zhang N, Li B (2013) Visualization of caspase-3-like activity in cells using a genetically encoded fluorescent biosensor activated by protein cleavage. Nat Commun 4. https://doi.org/10.1038/ncomms3157

  36. Li J, Li X, Shi X, He X, Wei W, Ma N, Chen H (2013) Highly Sensitive Detection of Caspase-3 Activities via a Nonconjugated Gold Nanoparticle–Quantum Dot Pair Mediated by an Inner-Filter Effect. ACS Appl Mater Interfaces 5(19):9798–9802. https://doi.org/10.1021/am4029735

    Article  CAS  PubMed  Google Scholar 

  37. Cárdenas-Maestre JM, Pérez-López AM, Bradley M, Sánchez-Martín RM (2014) Microsphere-Based Intracellular Sensing of Caspase-3/7 in Apoptotic Living Cells. Macromol Biosci 14(7):923–928. https://doi.org/10.1002/mabi.201300525

    Article  CAS  PubMed  Google Scholar 

  38. Jixiang L, Bhalgat M, Zhang C, Zhenjun D, Hoyland B, Klaubert DH (1999) Fluorescent molecular probes V: A sensitive caspase-3 substrate for fluorometric assays. Bioorg Med Chem Lett 9(22):3231–3236. https://doi.org/10.1016/S0960-894X(99)00566-1

    Article  Google Scholar 

  39. Huang R, Wang X, Wang D, Liu F, Mei B, Tang A, Jiang J, Liang G (2013) Multifunctional Fluorescent Probe for Sequential Detections of Glutathione and Caspase-3 in Vitro and in Cells. Anal Chemistry 85(13):6203–6207. https://doi.org/10.1021/ac4014012

    Article  CAS  Google Scholar 

  40. Maxwell D, Chang Q, Zhang X, Barnett EM, Piwnica-Worms D (2009) An Improved Cell-Penetrating, Caspase-Activatable, Near-Infrared Fluorescent Peptide for Apoptosis Imaging. Bioconjug Chem 20(4):702–709. https://doi.org/10.1021/bc800516n

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Dai N, Guo J, Teo YN, Kool ET (2011) Protease Probes Built from DNA: Multispectral Fluorescent DNA–Peptide Conjugates as Caspase Chemosensors. Angew Chem Int Ed 50(22):5105–5109. https://doi.org/10.1002/anie.201007805

    Article  CAS  Google Scholar 

  42. Hu M, Li L, Wu H, Su Y, Yang P-Y, Uttamchandani M, Xu Q-H, Yao SQ (2011) Multicolor, One- and Two-Photon Imaging of Enzymatic Activities in Live Cells with Fluorescently Quenched Activity-Based Probes (qABPs). J Am Chem Soc 133(31):12009–12020. https://doi.org/10.1021/ja200808y

    Article  CAS  PubMed  Google Scholar 

  43. Bardet P-L, Kolahgar G, Mynett A, Miguel-Aliaga I, Briscoe J, Meier P, Vincent J-P (2008) A fluorescent reporter of caspase activity for live imaging. Proc Natl Acad Sci 105(37):13901–13905. https://doi.org/10.1073/pnas.0806983105

    Article  PubMed  Google Scholar 

  44. Zhang H-Z, Kasibhatla S, Guastella J, Tseng B, Drewe J, Cai SX (2003) N-Ac-DEVD-N‘-(Polyfluorobenzoyl)−R110: Novel Cell-Permeable Fluorogenic Caspase Substrates for the Detection of Caspase Activity and Apoptosis. Bioconjugate Chemistry 14(2):458–463. https://doi.org/10.1021/bc0256188

    Article  CAS  PubMed  Google Scholar 

  45. Sun I-C, Lee S, Koo H, Kwon IC, Choi K, Ahn C-H, Kim K (2010) Caspase Sensitive Gold Nanoparticle for Apoptosis Imaging in Live Cells. Bioconjug Chem 21(11):1939–1942. https://doi.org/10.1021/bc1003026

    Article  CAS  PubMed  Google Scholar 

  46. Free P, Shaw CP, Levy R (2009) PEGylation modulates the interfacial kinetics of proteases on peptide-capped gold nanoparticles. Chem Commun (33):5009–5011. https://doi.org/10.1039/B910657J

  47. Angres B, Steuer H, Weber P, Wagner M, Schneckenburger H (2009) A membrane-bound FRET-based caspase sensor for detection of apoptosis using fluorescence lifetime and total internal reflection microscopy. Cytometry Part A 75A(5):420–427. https://doi.org/10.1002/cyto.a.20698

    Article  CAS  Google Scholar 

  48. Wu Y, Xing D, Luo S, Tang Y, Chen Q (2006) Detection of caspase-3 activation in single cells by fluorescence resonance energy transfer during photodynamic therapy induced apoptosis. Cancer Lett 235(2):239–247. https://doi.org/10.1016/j.canlet.2005.04.036

    Article  CAS  PubMed  Google Scholar 

  49. Gu Z, Biswas A, Joo K-I, Hu B, Wang P, Tang Y (2010) Probing protease activity by single-fluorescent-protein nanocapsules. Chem Commun 46(35):6467–6469. https://doi.org/10.1039/C0CC01439G

    Article  CAS  Google Scholar 

  50. Ding Y, Ai H-w, Hoi H, Campbell RE (2011) Förster Resonance Energy Transfer-Based Biosensors for Multiparameter Ratiometric Imaging of Ca2+ Dynamics and Caspase-3 Activity in Single Cells. Anal Chem 83(24):9687–9693. https://doi.org/10.1021/ac202595g

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Han Q-B, Yu T, Lai F, Zhou Y, Feng C, Wang W-N, Fu X-H, Lau CB-S, Luo KQ, Xu H-X, Sun H-D, Fung K-P, Leung P-C (2010) Quick identification of apoptosis inducer from Isodon eriocalyx by a drug discovery platform composed of analytical high-speed counter-current chromatography and the fluorescence-based caspase-3 biosensor detection. Talanta 82(4):1521–1527. https://doi.org/10.1016/j.talanta.2010.07.036

    Article  CAS  PubMed  Google Scholar 

  52. Elphick LM, Meinander A, Mikhailov A, Richard M, Toms NJ, Eriksson JE, Kass GEN (2006) Live cell detection of caspase-3 activation by a Discosoma-red-fluorescent-protein-based fluorescence resonance energy transfer construct. Anal Biochem 349(1):148–155. https://doi.org/10.1016/j.ab.2005.11.031

    Article  CAS  PubMed  Google Scholar 

  53. Perez JM, Josephson L, O'Loughlin T, Hogemann D, Weissleder R (2002) Magnetic relaxation switches capable of sensing molecular interactions. Nat Biotech 20(8):816–820

    Article  CAS  Google Scholar 

  54. Ai H-W, Hazelwood KL, Davidson MW, Campbell RE (2008) Fluorescent protein FRET pairs for ratiometric imaging of dual biosensors. Nat Meth 5(5):401–403 http://www.nature.com/nmeth/journal/v5/n5/suppinfo/nmeth.1207_S1.html

    Article  CAS  Google Scholar 

  55. Heeres JT, Kim S-H, Leslie BJ, Lidstone EA, Cunningham BT, Hergenrother PJ (2009) Identifying Modulators of Protein−Protein Interactions Using Photonic Crystal Biosensors. J Am Chem Soc 131(51):18202–18203. https://doi.org/10.1021/ja907066r

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Zhang L, Lei J, Liu J, Ma F, Ju H (2015) Persistent luminescence nanoprobe for biosensing and lifetime imaging of cell apoptosis via time-resolved fluorescence resonance energy transfer. Biomaterials 67:323–334. https://doi.org/10.1016/j.biomaterials.2015.07.037

    Article  CAS  PubMed  Google Scholar 

  57. Oishi M, Tamura A, Nakamura T, Nagasaki Y (2009) A Smart Nanoprobe Based On Fluorescence-Quenching PEGylated Nanogels Containing Gold Nanoparticles for Monitoring the Response to Cancer Therapy. Adv Funct Mater 19(6):827–834. https://doi.org/10.1002/adfm.200801164

    Article  CAS  Google Scholar 

  58. Shi Y, Yi C, Zhang Z, Zhang H, Li M, Yang M, Jiang Q (2013) Peptide-Bridged Assembly of Hybrid Nanomaterial and Its Application for Caspase-3 Detection. ACS Appl Mater Interfaces 5(14):6494–6501. https://doi.org/10.1021/am401935y

    Article  CAS  PubMed  Google Scholar 

  59. Gurtu V, Kain SR, Zhang G (1997) Fluorometric and Colorimetric Detection of Caspase Activity Associated with Apoptosis. Anal Biochem 251(1):98–102. https://doi.org/10.1006/abio.1997.2220

    Article  CAS  PubMed  Google Scholar 

  60. Zhou S, Zheng T, Chen Y, Zhang J, Li L, Lu F, Zhu J-J (2014) Toward therapeutic effects evaluation of chronic myeloid leukemia drug: Electrochemical platform for caspase-3 activity sensing. Biosens Bioelectron 61(0):648–654. https://doi.org/10.1016/j.bios.2014.05.064

    Article  CAS  PubMed  Google Scholar 

  61. Zhou Z, Peng L, Wang X, Xiang Y, Tong A (2014) A new colorimetric strategy for monitoring caspase 3 activity by HRP-mimicking DNAzyme-peptide conjugates. Analyst 139(5):1178–1183. https://doi.org/10.1039/C3AN02028B

    Article  CAS  PubMed  Google Scholar 

  62. Kim K, Lee M, Park H, Kim J-H, Kim S, Chung H, Choi K, Kim I-S, Seong BL, Kwon IC (2006) Cell-Permeable and Biocompatible Polymeric Nanoparticles for Apoptosis Imaging. J Am Chem Soc 128(11):3490–3491. https://doi.org/10.1021/ja057712f

    Article  CAS  PubMed  Google Scholar 

  63. Jun Y-w, Sheikholeslami S, Hostetter DR, Tajon C, Craik CS, Alivisatos AP (2009) Continuous imaging of plasmon rulers in live cells reveals early-stage caspase-3 activation at the single-molecule level. Proc Natl Acad Sci 106(42):17735–17740. https://doi.org/10.1073/pnas.0907367106

    Article  PubMed  Google Scholar 

  64. Chen N, Huang Y, Yang L, Liu R, Yang JJ (2009) Designing Caspase-3 Sensors for Imaging of Apoptosis in Living Cells. Chem – A Eur J 15(37):9311–9314. https://doi.org/10.1002/chem.200901439

    Article  CAS  Google Scholar 

  65. Ray P, De A, Patel M, Gambhir SS (2008) Monitoring Caspase-3 Activation with a Multimodality Imaging Sensor in Living Subjects. Clin Cancer Res 14(18):5801–5809. https://doi.org/10.1158/1078-0432.ccr-07-5244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Huang X, Swierczewska M, Choi KY, Zhu L, Bhirde A, Park J, Kim K, Xie J, Niu G, Lee KC, Lee S, Chen X (2012) Multiplex Imaging of an Intracellular Proteolytic Cascade by using a Broad-Spectrum Nanoquencher. Angew Chem Int Ed 51(7):1625–1630. https://doi.org/10.1002/anie.201107795

    Article  CAS  Google Scholar 

  67. Laxman B, Hall DE, Bhojani MS, Hamstra DA, Chenevert TL, Ross BD, Rehemtulla A (2002) Noninvasive real-time imaging of apoptosis. Proc Natl Acad Sci 99(26):16551–16555. https://doi.org/10.1073/pnas.252644499

    Article  CAS  PubMed  Google Scholar 

  68. Kanno A, Yamanaka Y, Hirano H, Umezawa Y, Ozawa T (2007) Cyclic Luciferase for Real-Time Sensing of Caspase-3 Activities in Living Mammals. Angew Chem Int Ed 46(40):7595–7599. https://doi.org/10.1002/anie.200700538

    Article  CAS  Google Scholar 

  69. Lee S, Choi KY, Chung H, Ryu JH, Lee A, Koo H, Youn I-C, Park JH, Kim I-S, Kim SY, Chen X, Jeong SY, Kwon IC, Kim K, Choi K (2011) Real Time, High Resolution Video Imaging of Apoptosis in Single Cells with a Polymeric Nanoprobe. Bioconjug Chem 22(2):125–131. https://doi.org/10.1021/bc1004119

    Article  CAS  PubMed  Google Scholar 

  70. Mizukami S, Kikuchi K, Higuchi T, Urano Y, Mashima T, Tsuruo T, Nagano T (1999) Imaging of caspase-3 activation in HeLa cells stimulated with etoposide using a novel fluorescent probe. FEBS Lett 453(3):356–360. https://doi.org/10.1016/S0014-5793(99)00755-3

    Article  CAS  PubMed  Google Scholar 

  71. Bullok K, Piwnica-Worms D (2005) Synthesis and Characterization of a Small, Membrane-Permeant, Caspase-Activatable Far-Red Fluorescent Peptide for Imaging Apoptosis. J Med Chem 48(17):5404–5407. https://doi.org/10.1021/jm050008p

    Article  CAS  PubMed  Google Scholar 

  72. Park K, Jeong J, Chung BH (2012) Cascade imaging of proteolytic pathways in cancer cells using fluorescent protein-conjugated gold nanoquenchers. Chem Commun 48(85):10547–10549. https://doi.org/10.1039/C2CC35687B

    Article  CAS  Google Scholar 

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Acknowledgements

We gratefully thanks for financial support of this work by stem cell research center, Tabriz University of Medical Sciences, Tabriz, Iran.

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Correspondence to Balal Khalilzadeh or Nasrin Shadjou.

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Khalilzadeh, B., Shadjou, N., Kanberoglu, G.S. et al. Advances in nanomaterial based optical biosensing and bioimaging of apoptosis via caspase-3 activity: a review. Microchim Acta 185, 434 (2018). https://doi.org/10.1007/s00604-018-2980-6

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