Activatable Ferritin Nanocomplex for Real-Time Monitoring of Caspase-3 Activation during Photodynamic Therapy

ACS Applied Materials and Interfaces

Volumn 7, Issue 41, 2015, Pages 23248-23256

  Wang, Jingjing ^a   Zhang, Liwen ^a   Chen, Minglong ^b   Gao, Shi ^b   Zhu, Lei ^a  

^a XIAMEN UNIVERSITY   (China)

^b JILIN UNIVERSITY   (China)

Author keywords

activatable probe; apoptosis; caspase 3; ferritin; photodynamic therapy

Indexed keywords

CELL DEATH; CHEMICAL ACTIVATION; INFRARED DEVICES; PHOTOSENSITIZERS; PROBES; VISUALIZATION;

CASPASE-3; CASPASE-3 ACTIVATION; FERRITIN; PHOTODYNAMIC THERAPY (PDT); REAL TIME MONITORING; REAL TIME VISUALIZATION; SIMULTANEOUS IMAGING; THERAPEUTIC OUTCOMES;

PHOTODYNAMIC THERAPY;

CASPASE 3; FERRITIN; INDOLE DERIVATIVE; MOLECULAR PROBE; NANOPARTICLE; ORGANOMETALLIC COMPOUND; ZINC(II) PHTHALOCYANINE TRISULFONIC ACID;

3T3 CELL LINE; ANIMAL; APOPTOSIS; CHEMISTRY; DRUG EFFECTS; ENDOCYTOSIS; ENZYME ACTIVATION; HUMAN; METABOLISM; MOLECULAR PROBE; MOUSE; PHOTOCHEMOTHERAPY; TUMOR CELL LINE; ULTRAVIOLET SPECTROPHOTOMETRY;

ANIMALS; APOPTOSIS; CASPASE 3; CELL LINE, TUMOR; ENDOCYTOSIS; ENZYME ACTIVATION; FERRITINS; HUMANS; INDOLES; MICE; MOLECULAR PROBES; NANOPARTICLES; NIH 3T3 CELLS; ORGANOMETALLIC COMPOUNDS; PHOTOCHEMOTHERAPY; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 84945368806     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b07316     Document Type: Article

References (49)

1. Sokolovski, G.; Goltsov, A.; Pourreyron, C.; South, P.; Rafailov, U. Infrared Laser Pulse Triggers Increased Singlet Oxygen Production in Tumour Cells Sci. Rep. 2013, 3, 3484 10.1038/srep03484
2. Dolmans, E.; Fukumura, D.; Jain, K. Photodynamic Therapy for Cancer Nat. Rev. Cancer 2003, 3, 380-387 10.1038/nrc1071
3. Celli, J. P.; Spring, B. Q.; Rizvi, I.; Evans, C. L.; Samkoe, K. S.; Verma, S.; Pogue, B. W.; Hasan, T. Imaging and Photodynamic Therapy: Mechanisms, Monitoring, and Optimization Chem. Rev. 2010, 110, 2795-2838 10.1021/cr900300p
4. Elich, D.; Lagarias, C. Phytochrome Chromophore Biosynthesis: Both 5-Aminolevulinic Acid and Biliverdin Overcome Inhibition by Gabaculine in Etiolated Avena Sativa L Plant Physiol. 1987, 84, 304-310 10.1104/pp.84.2.304
5. Tanaka, M.; Kataoka, H.; Yano, S.; Ohi, H.; Moriwaki, K.; Akashi, H.; Taguchi, T.; Hayashi, N.; Hamano, S.; Mori, Y.; Kubota, E.; Tanida, S.; Joh, T. Antitumor Effects in Gastrointestinal Stromal Tumors Using Photodynamic Therapy with a Novel Glucose-Conjugated Chlorin Mol. Cancer Ther. 2014, 13, 767-775 10.1158/1535-7163.MCT-13-0393
6. Rizvi, I.; Anbil, S.; Alagic, N.; Celli, J.; Zheng, L. Z.; Palanisami, A.; Glidden, D.; Pogue, W.; Hasan, T. Pdt Dose Parameters Impact Tumoricidal Durability and Cell Death Pathways in a 3D Ovarian Cancer Model Photochem. Photobiol. 2013, 89, 942-952 10.1111/php.12065
7. Fan, Y.; Bergmann, A. Apoptosis-Induced Compensatory Proliferation. The Cell Is Dead. Long Live the Cell Trends Cell Biol. 2008, 18, 467-473 10.1016/j.tcb.2008.08.001
8. Zheng, X.; Wang, X.; Mao, H.; Wu, W.; Liu, B.; Jiang, X. Hypoxia-Specific Ultrasensitive Detection of Tumours and Cancer Cells in Vivo Nat. Commun. 2015, 6, 5834 10.1038/ncomms6834
9. Casas, A.; Di Venosa, G.; Hasan, T. Mechanisms of Resistance to Photodynamic Therapy Curr. Med. Chem. 2011, 18, 2486-2515 10.2174/092986711795843272
10. Vickers, J.; Gonzalez-Paez, E.; Wolan, W. Discovery of a Highly Selective Caspase-3 Substrate for Imaging Live Cells ACS Chem. Biol. 2014, 9, 2199-2203 10.1021/cb500586p
11. Wang, L.; Chen, T.; Qu, J.; Wei, X. Quantitative Analysis of Caspase-3 Activation by Fitting Fluorescence Emission Spectra in Living Cells Micron 2009, 40, 811-820 10.1016/j.micron.2009.07.001
12. Zhu, L.; Huang, X.; Choi, Y.; Ma, Y.; Zhang, F.; Liu, G.; Lee, S.; Chen, X. Real-Time Monitoring of Caspase Cascade Activation in Living Cells J. Controlled Release 2012, 163, 55-62 10.1016/j.jconrel.2012.05.044
13. Kalluru, P.; Vankayala, R.; Chiang, C. S.; Hwang, K. C. Photosensitization of Singlet Oxygen and in Vivo Photodynamic Therapeutic Effects Mediated by Pegylated W(18)O(49) Nanowires Angew. Chem., Int. Ed. 2013, 52, 12332-12336 10.1002/anie.201307358
14. Zhen, Z.; Tang, W.; Guo, C.; Chen, H.; Lin, X.; Liu, G.; Fei, B.; Chen, X.; Xu, B.; Xie, J. Ferritin Nanocages to Encapsulate and Deliver Photosensitizers for Efficient Photodynamic Therapy against Cancer ACS Nano 2013, 7, 6988-6996 10.1021/nn402199g
15. Zhen, Z.; Tang, W.; Chuang, J.; Todd, T.; Zhang, W.; Lin, X.; Niu, G.; Liu, G.; Wang, L.; Pan, Z.; Chen, X.; Xie, J. Tumor Vasculature Targeted Photodynamic Therapy for Enhanced Delivery of Nanoparticles ACS Nano 2014, 8, 6004-6013 10.1021/nn501134q
16. Ge, J.; Lan, M.; Zhou, B.; Liu, W.; Guo, L.; Wang, H.; Jia, Q.; Niu, G.; Huang, X.; Zhou, H.; Meng, X.; Wang, P.; Lee, S.; Zhang, W.; Han, X. A Graphene Quantum Dot Photodynamic Therapy Agent with High Singlet Oxygen Generation Nat. Commun. 2014, 5, 4596 10.1038/ncomms5596
17. Niu, G.; Chen, X. Apoptosis Imaging: Beyond Annexin V J. Nucl. Med. 2010, 51, 1659-1662 10.2967/jnumed.110.078584
18. Fan, T. J.; Han, H.; Cong, S.; Liang, J. Caspase Family Proteases and Apoptosis Acta Biochim. Biophys. Sin. 2005, 37, 719-727 10.1111/j.1745-7270.2005.00108.x
19. McIlwain, R.; Berger, T.; Mak, W. Caspase Functions in Cell Death and Disease Cold Spring Harbor Perspect. Biol. 2013, 5, a008656 10.1101/cshperspect.a008656
20. Chang, Y.; Yang, L. Proteases for Cell Suicide: Functions and Regulation of Caspases Microbiol Mol. Biol. Rev. 2000, 64, 821-846 10.1128/MMBR.64.4.821-846.2000
21. Courtiade, J.; Pauchet, Y.; Vogel, H.; Heckel, D. G. A Comprehensive Characterization of the Caspase Gene Family in Insects from the Order Lepidoptera BMC Genomics 2011, 12, 357 10.1186/1471-2164-12-357
22. Perez-Hernandez, M.; Del Pino, P.; Mitchell, G.; Moros, M.; Stepien, G.; Pelaz, B.; Parak, J.; Galvez, M.; Pardo, J.; de la Fuente, M. Dissecting the Molecular Mechanism of Apoptosis During Photothermal Therapy Using Gold Nanoprisms ACS Nano 2015, 9, 52-61 10.1021/nn505468v
23. Louie, A. Multimodality Imaging Probes: Design and Challenges Chem. Rev. 2010, 110, 3146-3195 10.1021/cr9003538
24. Min, Y.; Li, J.; Liu, F.; Yeow, K.; Xing, B. Near-Infrared Light-Mediated Photoactivation of a Platinum Antitumor Prodrug and Simultaneous Cellular Apoptosis Imaging by Upconversion-Luminescent Nanoparticles Angew. Chem., Int. Ed. 2014, 53, 1012-1016 10.1002/anie.201308834
25. Huang, X.; Lee, S.; Chen, X. Design of "Smart" Probes for Optical Imaging of Apoptosis Am. J. Nucl. Med. Mol. Imaging 2011, 1, 3-17
26. Barnett, M.; Zhang, X.; Maxwell, D.; Chang, Q.; Piwnica-Worms, D. Single-Cell Imaging of Retinal Ganglion Cell Apoptosis with a Cell-Penetrating, Activatable Peptide Probe in an in Vivo Glaucoma Model Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 9391-9396 10.1073/pnas.0812884106
27. Zhu, L.; Zhang, F.; Ma, Y.; Liu, G.; Kim, K.; Fang, X.; Lee, S.; Chen, X. In Vivo Optical Imaging of Membrane-Type Matrix Metalloproteinase (MT-MMP) Activity Mol. Pharmaceutics 2011, 8, 2331-2338 10.1021/mp2002297
28. Zhang, L.; Gao, S.; Zhang, F.; Yang, K.; Ma, Q.; Zhu, L. Activatable Hyaluronic Acid Nanoparticle as a Theranostic Agent for Optical/Photoacoustic Image-Guided Photothermal Therapy ACS Nano 2014, 8, 12250-12258 10.1021/nn506130t
29. Huang, X.; Swierczewska, M.; Choi, Y.; Zhu, L.; Bhirde, A.; Park, J.; Kim, K.; Xie, J.; Niu, G.; Lee, C.; Lee, S.; Chen, X. Multiplex Imaging of an Intracellular Proteolytic Cascade by Using a Broad-Spectrum Nanoquencher Angew. Chem., Int. Ed. 2012, 51, 1625-1630 10.1002/anie.201107795
30. Ye, D.; Shuhendler, J.; Cui, L.; Tong, L.; Tee, S.; Tikhomirov, G.; Felsher, W.; Rao, J. Bioorthogonal Cyclization-Mediated in Situ Self-Assembly of Small-Molecule Probes for Imaging Caspase Activity in Vivo Nat. Chem. 2014, 6, 519-526 10.1038/nchem.1920
31. Shah, K.; Tang, Y.; Breakefield, X.; Weissleder, R. Real-Time Imaging of Trail-Induced Apoptosis of Glioma Tumors in Vivo Oncogene 2003, 22, 6865-6872 10.1038/sj.onc.1206748
32. Niu, G.; Zhu, L.; Ho, N.; Zhang, F.; Gao, H.; Quan, Q.; Hida, N.; Ozawa, T.; Liu, G.; Chen, X. Longitudinal Bioluminescence Imaging of the Dynamics of Doxorubicin Induced Apoptosis Theranostics 2013, 3, 190-200 10.7150/thno.5825
33. Laxman, B.; Hall, E.; Bhojani, S.; Hamstra, A.; Chenevert, L.; Ross, D.; Rehemtulla, A. Noninvasive Real-Time Imaging of Apoptosis Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 16551-16555 10.1073/pnas.252644499
34. Wu, Y.; Xing, D.; Chen, W. R. Single Cell Fret Imaging for Determination of Pathway of Tumor Cell Apoptosis Induced by Photofrin-PDT Cell Cycle 2006, 5, 729-734 10.4161/cc.5.7.2630
35. Stefflova, K.; Chen, J.; Li, H.; Zheng, G. Targeted Photodynamic Therapy Agent with a Built-in Apoptosis Sensor for in Vivo near-Infrared Imaging of Tumor Apoptosis Triggered by Its Photosensitization in Situ Mol. Imaging 2006, 5, 520-532
36. Lovell, J. F.; Chan, W.; Qi, Q.; Chen, J.; Zheng, G. Porphyrin Fret Acceptors for Apoptosis Induction and Monitoring J. Am. Chem. Soc. 2011, 133, 18580-18582 10.1021/ja2083569
37. Stefflova, K.; Chen, J.; Zheng, G. Killer Beacons for Combined Cancer Imaging and Therapy Curr. Med. Chem. 2007, 14, 2110-2125 10.2174/092986707781389655
38. Yogo, T.; Urano, Y.; Ishitsuka, Y.; Maniwa, F.; Nagano, T. Highly Efficient and Photostable Photosensitizer Based on Bodipy Chromophore J. Am. Chem. Soc. 2005, 127, 12162-12163 10.1021/ja0528533
39. Uzdensky, B.; Iani, V.; Ma, L. W.; Moan, J. Photobleaching of Hypericin Bound to Human Serum Albumin, Cultured Adenocarcinoma Cells and Nude Mice Skin Photochem. Photobiol. 2002, 76, 320-328 10.1562/0031-8655(2002)0760320POHBTH2.0.CO2
40. Lin, X.; Xie, J.; Zhu, L.; Lee, S.; Niu, G.; Ma, Y.; Kim, K.; Chen, X. Hybrid Ferritin Nanoparticles as Activatable Probes for Tumor Imaging Angew. Chem., Int. Ed. 2011, 50, 1569-1572 10.1002/anie.201006757
41. Tian, J.; Ding, L.; Xu, H. J.; Shen, Z.; Ju, H.; Jia, L.; Bao, L.; Yu, J. S. Cell-Specific and Ph-Activatable Rubyrin-Loaded Nanoparticles for Highly Selective near-Infrared Photodynamic Therapy against Cancer J. Am. Chem. Soc. 2013, 135, 18850-18858 10.1021/ja408286k
42. O'Donnell, K. A.; Yu, D.; Zeller, K. I.; Kim, J. W.; Racke, F.; Thomas-Tikhonenko, A.; Dang, C. V. Activation of Transferrin Receptor 1 by C-Myc Enhances Cellular Proliferation and Tumorigenesis Mol. Cell. Biol. 2006, 26, 2373-2386 10.1128/MCB.26.6.2373-2386.2006
43. Gatter, C.; Brown, G.; Trowbridge, S.; Woolston, E.; Mason, D. Y. Transferrin Receptors in Human Tissues: Their Distribution and Possible Clinical Relevance J. Clin. Pathol. 1983, 36, 539-545 10.1136/jcp.36.5.539
44. Niitsu, Y.; Kohgo, Y.; Nishisato, T.; Kondo, H.; Kato, J.; Urushizaki, Y.; Urushizaki, I. Transferrin Receptors in Human Cancerous Tissues Tohoku Tohoku J. Exp. Med. 1987, 153, 239-243 10.1620/tjem.153.239
45. Liang, M.; Fan, K.; Zhou, M.; Duan, D.; Zheng, J.; Yang, D.; Feng, J.; Yan, X. H-Ferritin-Nanocaged Doxorubicin Nanoparticles Specifically Target and Kill Tumors with a Single-Dose Injection Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 14900-14905 10.1073/pnas.1407808111
46. Gatter, K. C.; Brown, G.; Trowbridge, I. S.; Woolston, R. E.; Mason, D. Y. Transferrin Receptors in Human Tissues: Their Distribution and Possible Clinical Relevance J. Clin. Pathol. 1983, 36, 539-545 10.1136/jcp.36.5.539
47. Stefflova, K.; Chen, J.; Marotta, D.; Li, H.; Zheng, G. Photodynamic Therapy Agent with a Built-in Apoptosis Sensor for Evaluating Its Own Therapeutic Outcome in Situ J. Med. Chem. 2006, 49, 3850-3856 10.1021/jm060146u
48. Chen, J.; Stefflova, K.; Niedre, J.; Wilson, C.; Chance, B.; Glickson, D.; Zheng, G. Protease-Triggered Photosensitizing Beacon Based on Singlet Oxygen Quenching and Activation J. Am. Chem. Soc. 2004, 126, 11450-11451 10.1021/ja047392k
49. Lee, S.; Mortensen, J.; Lin, P.; Tung, C. An Authentic Imaging Probe to Track Cell Fate from Beginning to End Nat. Commun. 2014, 5, 5216 10.1038/ncomms6216