Protease-Activable Cell-Penetrating Peptide-Protoporphyrin Conjugate for Targeted Photodynamic Therapy in Vivo

ACS Applied Materials and Interfaces

Volumn 7, Issue 51, 2015, Pages 28319-28329

  Li, Shi Ying ^a   Cheng, Hong ^a   Qiu, Wen Xiu ^a   Liu, Li Han ^a   Chen, Si ^a   Hu, Ying ^a   Xie, Bo Ru ^a   Li, Bin ^a   Zhang, Xian Zheng ^a,b  

^a WUHAN UNIVERSITY   (China)

^b Hubei Provincial Cooperative Innovation Center of Industrial Fermentation   (China)

Author keywords

cell penetrating peptide; matrix metalloproteinases 2; photodynamic therapy; theranostic; tumor targeting

Indexed keywords

CELLS; CYTOLOGY; DIAGNOSIS; PEPTIDES; TUMORS;

CELL-PENETRATING PEPTIDE; ELECTROSTATIC ATTRACTIONS; FLUORESCENCE ENHANCEMENT; MATRIX METALLOPROTEINASES; PHOTODYNAMIC THERAPY (PDT); TAIL VEIN INJECTIONS; THERANOSTIC; TUMOR TARGETING;

PHOTODYNAMIC THERAPY;

CELL PENETRATING PEPTIDE; GELATINASE A; PROTOPORPHYRIN;

ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; ENZYMOLOGY; HUMAN; METABOLISM; NEOPLASMS; NUDE MOUSE; PHOTOCHEMOTHERAPY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL-PENETRATING PEPTIDES; HUMANS; MATRIX METALLOPROTEINASE 2; MICE, INBRED BALB C; MICE, NUDE; NEOPLASMS; PHOTOCHEMOTHERAPY; PROTOPORPHYRINS;

EID: 84952925842     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b08637     Document Type: Article

References (43)

1. Dolmans, D. E. J. G. J.; Fukumura, D.; Jain, R. K. TIMELINE: Photodynamic Therapy for Cancer Nat. Rev. Cancer 2003, 3, 380-387 10.1038/nrc1071
2. Hopper, C. Photodynamic Therapy: a Clinical Reality in The Treatment of Cancer Lancet Oncol. 2000, 1, 212-219 10.1016/S1470-2045(00)00166-2
3. Ethirajan, M.; Chen, Y. H.; Joshi, P.; Pandey, R. K. The Role of Porphyrin Chemistry in Tumor Imaging and Photodynamic Therapy Chem. Soc. Rev. 2011, 40, 340-362 10.1039/B915149B
4. Reinhard, A.; Sandborn, W. J.; Melhem, H.; Bolotine, L.; Chamaillard, M.; Peyrin-Biroulet, L. Photodynamic Therapy as a New Treatment Modality for Inflammatory and Infectious Conditions Expert Rev. Clin. Immunol. 2015, 11, 637-657 10.1586/1744666X.2015.1032256
5. 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
6. Guillemard, V.; Saragovi, H. U. Taxane-Antibody Conjugates Afford Potent Cytotoxicity, Enhanced Solubility, and Tumor Target Selectivity Cancer Res. 2001, 61, 694-9
7. Ding, H. Y.; Sumer, B. D.; Kessinger, C. W.; Dong, Y.; Huang, G.; Boothman, D. A.; Gao, J. M. Nanoscopic Micelle Delivery Improves the Photophysical Properties and Efficacy of Photodynamic Therapy of Protoporphyrin IX J. Controlled Release 2011, 151, 271-277 10.1016/j.jconrel.2011.01.004
8. Sun, Y.; Chen, Z.; Yang, X.; Huang, P.; Zhou, X.; Du, X. Magnetic Chitosan Nanoparticles as a Drug Delivery System for Targeting Photodynamic Therapy Nanotechnology 2009, 20, 135102 10.1088/0957-4484/20/13/135102
9. Zheng, G.; Chen, J.; Stefflova, K.; Jarvi, M.; Li, H.; Wilson, B. C. Photodynamic Molecular Beacon as an Activatable Photosensitizer Based on Protease-Controlled Singlet Oxygen Quenching and Activation Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 8989-8994 10.1073/pnas.0611142104
10. Tian, J. W.; Ding, L. L.; Ju, H. X.; Yang, Y. C.; Li, X. L.; Shen, Z.; Zhu, Z.; Yu, J. S.; Yang, C. J. A Multifunctional Nanomicelle for Real-Time Targeted Imaging and Precise Near-Infrared Cancer Therapy Angew. Chem., Int. Ed. 2014, 53, 9544-9549 10.1002/anie.201405490
11. Robertson, C. A.; Evans, D. H.; Abrahamse, H. Photodynamic therapy (PDT): A short review on cellular mechanisms and cancer research applications for PDT J. Photochem. Photobiol., B 2009, 96, 1-8 10.1016/j.jphotobiol.2009.04.001
12. Han, K.; Lei, Q.; Jia, H. Z.; Wang, S. B.; Yin, W. N.; Chen, W. H.; Cheng, S. X.; Zhang, X. Z. A Tumor Targeted Chimeric Peptide for Synergistic Endosomal Escape and Therapy by Dual-Stage Light Manipulation Adv. Funct. Mater. 2015, 25, 1248-1257 10.1002/adfm.201403190
13. Lindgren, M.; Hällbrink, M.; Prochiantz, A.; Langel, U. Cell-Penetrating Peptides Trends Pharmacol. Sci. 2000, 21, 99-103 10.1016/S0165-6147(00)01447-4
14. Zorko, M.; Langel, U. Cell-Penetrating Peptides: Mechanism and Kinetics of Cargo Delivery Adv. Drug Delivery Rev. 2005, 57, 529-545 10.1016/j.addr.2004.10.010
15. Gupta, B.; Levchenko, T. S.; Torchilin, V. P. Intracellular Delivery of Large Molecules and Small Particles by Cell-Penetrating Proteins and Peptides Adv. Drug Delivery Rev. 2005, 57, 637-651 10.1016/j.addr.2004.10.007
16. Fu, J. Q.; Yu, C. M.; Li, L.; Yao, S. Q. Intracellular Delivery of Functional Proteins and Native Drugs by Cell-Penetrating Poly(disulfide)s J. Am. Chem. Soc. 2015, 137, 12153-12160 10.1021/jacs.5b08130
17. Zhang, Q. Y.; Gao, H. L.; He, Q. Taming Cell Penetrating Peptides: Never Too Old To Teach Old Dogs New Tricks Mol. Pharmaceutics 2015, 12, 3105-3118 10.1021/acs.molpharmaceut.5b00428
18. Sarko, D.; Beijer, B.; Boy, R. G.; Nothelfer, E.-M.; Leotta, K.; Eisenhut, M.; Altmann, A.; Haberkorn, U.; Mier, W. The Pharmacokinetics of Cell-Penetrating Peptides Mol. Pharmaceutics 2010, 7, 2224-2231 10.1021/mp100223d
19. Kondo, E.; Saito, K.; Tashiro, Y.; Kamide, K.; Uno, S.; Furuya, T.; Mashita, M.; Nakajima, K.; Tsumuraya, T.; Kobayashi, N.; Nishibori, M.; Tanimoto, M.; Matsushita, M. Tumour Lineage-Homing Cell-Penetrating Peptides as Anticancer Molecular Delivery Systems Nat. Commun. 2012, 3, 951 10.1038/ncomms1952
20. Jin, E.; Zhang, B.; Sun, X. R.; Zhou, Z. X.; Ma, X. P.; Sun, Q. H.; Tang, J. B.; Shen, Y. Q.; Van Kirk, E.; Murdoch, W. J.; Radosz, M. Acid-Active Cell-Penetrating Peptides for In Vivo Tumor-Targeted Drug Delivery J. Am. Chem. Soc. 2013, 135, 933-940 10.1021/ja311180x
21. Shi, N. Q.; Gao, W.; Xiang, B.; Qi, X. R. Enhancing Cellular Uptake of Activable Cell-Penetrating Peptide-Doxorubicin Conjugate by Enzymatic Cleavage Int. J. Nanomed. 2012, 7, 1613-1621 10.2147/IJN.S30104
22. Cheng, H.; Zhu, J. Y.; Xu, X. D.; Qiu, W. X.; Lei, Q.; Han, K.; Cheng, Y. J.; Zhang, X. Z. Activable Cell-Penetrating Peptide Conjugated Prodrug for Tumor Targeted Drug Delivery ACS Appl. Mater. Interfaces 2015, 7, 16061-16069 10.1021/acsami.5b04517
23. Liu, Z.; Xiong, M.; Gong, J. B.; Zhang, Y.; Bai, N.; Luo, Y. P.; Li, L. Y.; Wei, Y. Q.; Liu, Y.; Tan, X.; Xiang, R. Legumain Protease-Activated TAT-Liposome Cargo for Targeting Tumours and Their Microenvironment Nat. Commun. 2014, 5, 4280 10.1038/ncomms5280
24. Jiang, T.; Olson, E. S.; Nguyen, Q. T.; Roy, M.; Jennings, P. A.; Tsien, R. Y. Tumor imaging by means of proteolytic activation of cell-penetrating peptides Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 17867-17872 10.1073/pnas.0408191101
25. Whitney, M.; Savariar, E. N.; Friedman, B.; Levin, R. A.; Crisp, J. L.; Glasgow, H. L.; Lefkowitz, R.; Adams, S. R.; Steinbach, P.; Nashi, N.; Nguyen, Q. T.; Tsien, R. Y. Ratiometric Activatable Cell-Penetrating Peptides Provide Rapid In Vivo Readout of Thrombin Activation Angew. Chem., Int. Ed. 2013, 52, 325-330 10.1002/anie.201205721
26. Weinstain, R.; Savariar, E. N.; Felsen, C. N.; Tsien, R. Y. In Vivo Targeting of Hydrogen Peroxide by Activatable Cell Penetrating Peptides J. Am. Chem. Soc. 2014, 136, 874-877 10.1021/ja411547j
27. Cheetham, A. G.; Zhang, P. C.; Lin, Y. A.; Lock, L. L.; Cui, H. G. Supramolecular Nanostructures Formed by Anticancer Drug Assembly J. Am. Chem. Soc. 2013, 135, 2907-2910 10.1021/ja3115983
28. Huang, P.; Wang, D. L.; Su, Y.; Huang, W.; Zhou, Y. F.; Cui, D. X.; Zhu, X. Y.; Yan, D. Y. Combination of Small Molecule Prodrug and Nanodrug Delivery: Amphiphilic Drug-Drug Conjugate for Cancer Therapy J. Am. Chem. Soc. 2014, 136, 11748-11756 10.1021/ja505212y
29. Gramberg, D.; Robinson, J. A. Design and Synthesis of a Cis-Gly-Pro, Type-VI Turn, Dipeptide Mimetic and Its Sse in Fmoc-Solid Phase Peptide Synthesis Tetrahedron Lett. 1994, 35, 861-864 10.1016/S0040-4039(00)75983-1
30. Mroz, P.; Huang, Y. Y.; Szokalska, A.; Zhiyentayev, T.; Janjua, S.; Nifli, A. P.; Sherwood, M. E.; Ruzie, C.; Borbas, K. B.; Fan, D. Z.; Krayer, M.; Balasubramanian, T.; Yang, E.; Kee, H. L.; Kirmaier, C.; Diers, J. R.; Bocian, D. F.; Holten, D.; Lindsey, J. S.; Hamblin, M. R. Stable synthetic bacteriochlorins overcome the resistance of melanoma to photodynamic therapy FASEB J. 2010, 24, 3160-1370 10.1096/fj.09-152587
31. Savariar, E. N.; Felsen, C. N.; Nashi, N.; Jiang, T.; Ellies, L. G.; Steinbach, P.; Tsien, R. Y.; Nguyen, Q. T. Real-time In Vivo Molecular Detection of Primary Tumors and Metastases with Ratiometric Activatable Cell-Penetrating Peptides Cancer Res. 2013, 73, 855-864 10.1158/0008-5472.CAN-12-2969
32. Lee, S.; Cha, E.-J.; Park, K.; Lee, S.-Y.; Hong, J.-K.; Sun, I.-C.; Kim, S. Y.; Choi, K.; Kwon, I. K.; Kim, K.; Ahn, C.-H. A Near-Infrared-Fluorescence-Quenched Gold-Nanoparticle Imaging Probe for In Vivo Drug Screening and Protease Activity Determination Angew. Chem., Int. Ed. 2008, 47, 2804-2807 10.1002/anie.200705240
33. Zhu, L.; Kate, P.; Torchilin, V. P. Matrix Metalloprotease-2 Responsive Multifunctional Liposomal Nanocarrier for Enhanced Tumor Targeting ACS Nano 2012, 6, 3491-3498 10.1021/nn300524f
34. Zhang, J.; Yuan, Z. F.; Wang, Y.; Chen, W. H.; Luo, G. F.; Cheng, S. X.; Zhuo, R. X.; Zhang, X. Z. Multifunctional Envelope-Type Mesoporous Silica Nanoparticles for Tumor-Triggered Targeting Drug Delivery J. Am. Chem. Soc. 2013, 135, 5068-5073 10.1021/ja312004m
35. Han, K.; Wang, S. B.; Lei, Q.; Zhu, J. Y.; Zhang, X. Z. Ratiometric Biosensor for Aggregation-Induced Emission-Guided Precise Photodynamic Therapy ACS Nano 2015, 9, 10268-10277 10.1021/acsnano.5b04243
36. Giambernardi, T. A.; Grant, G. M.; Taylor, G. P.; Hay, R. J.; Maher, V. M.; Mccormick, J. J.; Klebe, R. J. Overview of Matrix Metalloproteinase Expression in Cultured Human Cells Matrix Biol. 1998, 16, 483-496 10.1016/S0945-053X(98)90019-1
37. Lebel, R.; Lepage, M. A comprehensive review on controls in molecular imaging: lessons from MMP-2 imaging Contrast Media Mol. Imaging 2014, 9, 187-210 10.1002/cmmi.1555
38. 2-photosensitized ROS Generation in Cultured Human Skin Fibroblasts Photochem. Photobiol. 2006, 82, 5-12 10.1562/2005-05-29-RA-551
39. Burns, K. E.; Robinson, M. K.; Thévenin, D. Inhibition of Cancer Cell Proliferation and Breast Tumor Targeting of pHLIP-Monomethyl Auristatin E Conjugates Mol. Pharmaceutics 2015, 12, 1250-1258 10.1021/mp500779k
40. Li, S. Y.; Liu, L. H.; Cheng, H.; Li, B.; Qiu, W. X.; Zhang, X. Z. A Dual-FRET-Based Fluorescence Probe for the Sequential Detection of MMP-2 and Caspase-3 Chem. Commun. 2015, 51, 14520-14523 10.1039/C5CC04962H
41. Kessel, D.; Luo, Y.; Deng, Y.; Chang, C. K. The Role of Subcellular Localization in Initiation of Apoptosis by Photodynamic Therapy Photochem. Photobiol. 1997, 65, 422-426 10.1111/j.1751-1097.1997.tb08581.x
42. Oleinick, N. L.; Morris, R. L.; Belichenko, I. The Role of Apoptosis in Response to Photodynamic Therapy: What, Where, Why, and How Photochem. Photobiol. Sci. 2002, 1, 1-21 10.1039/b108586g
43. Castano, A. P.; Mroz, P.; Hamblin, M. R. Photodynamic Therapy and Anti-Tumour Immunity Nat. Rev. Cancer 2006, 6, 535-545 10.1038/nrc1894