Photodynamic Molecular Beacons triggered by MMP-2 and MMP-9: Influence of the distance between photosensitizer and quencher onto photophysical properties and enzymatic activation

Current Medicinal Chemistry

Volumn 19, Issue 32, 2012, Pages 5580-5594

  Verhille, M ^a,b,c   Benachour, H ^a,d   Ibrahim, A ^e   Achard, M ^a,c   Arnoux, P ^a,b   Barberi Heyob, M ^a,d,f,g   Andre J C ^a,b   Allonas, X ^e   Baros, F ^a,b   Vanderesse, R ^a,c,f   Frochot, C ^a,f  

^a UNIVERSITÉ DE LORRAINE   (France)

^b UNIVERSITÉ DE LORRAINE   (France)

^c LAB DE CHIM PHYS MACROMOLECULAIRE   (France)

^d CENTRE DE RECHERCHE EN AUTOMATIQUE DE NANCY   (France)

^e UNIVERSITÉ DE HAUTE ALSACE   (France)

^f GdR CNRS 3049 Médicaments Photoactivables Photochimiothérapie PHOTOMED France GdR CNRS 3049 Médicaments Photoactivables Photochimiothérapie PHOTOMED   (France)

^g CENTRE ALEXIS VAUTRIN   (France)

Author keywords

Energy transfer; Matrix metalloproteinases activities; Molecular beacon; Photodynamic therapy; Photosensitizer; Quenching; Targeting

Indexed keywords

5 (4 AMINOPHENYL) 10,15,20 TRIPHENYL PORPHYRIN; 5 (4 CARBOXYPHENYL SUCCINIMIDE ESTER) 10,15,20 TRIPHENYL 21,23 H CHLORIN; 5 (4 CARBOXYPHENYL) 10,15,20 TRIPHENYL 21,23 H CHLORIN; 5 (4 CARBOXYPHENYL) 10,15,20 TRIPHENYL PORPHYRIN; 5 [[(4 PHENYLCARBAMOYL)METHOXY] ACETIC ACID] 10,15,20 TRIPHENYL 21,23 H CHLORIN; 5 [[(4 PHENYLCARBAMOYL)METHOXY] ACETIC ACID] 10,15,20 TRIPHENYL PORPHYRIN; CHLORINE DERIVATIVE; GELATINASE A; GELATINASE B; PHOTOSENSITIZING AGENT; PORPHYRIN DERIVATIVE; TETRAPHENYLPORPHYRIN; UNCLASSIFIED DRUG;

ABSORPTION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; MOLECULAR BEACON; PHOTOCHEMICAL QUENCHING; PHOTODYNAMIC THERAPY; PROTEIN CLEAVAGE; SPECTROFLUOROMETRY; ULTRAVIOLET SPECTROPHOTOMETRY;

MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; OLIGOPEPTIDES; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; RECOMBINANT PROTEINS;

EID: 84870417623     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/092986712803833128     Document Type: Article

References (69)

1. Dougherty, T. J.; Dougherty, T. J.; Gomer, C. J.; Jori, G.; Kessel, D.; Korbelik, M.; Moan, J.; Peng, Q. Photodynamic Therapy. JNCI J Natl Cancer Inst 1998, 90, 889-905.
2. Macdonald, I. J.; Dougherty, T. J. Basic principles of photodynamic therapy. Journal of Porphyrins and Phthalocyanines 2001, 5, 105-129.
3. Weishaupt, K. R.; Gomer, C. J.; Dougherty, T. J. Identification of singlet oxygen as the cytotoxic agent in photoinactivation of a murine tumor. Cancer Res. 1976, 36, 2326-2329.
4. Mitchell, J. B.; McPherson, S.; DeGraff, W.; Gamson, J.; Zabell, A.; Russo, A. Oxygen dependence of hematoporphyrin derivative-induced photoinactivation of Chinese hamster cells. Cancer Res. 1985, 45, 2008-2011.
5. Berdowska, I. Cysteine proteases as disease markers. Clin. Chim. Acta 2004, 342, 41-69.
6. Duffy, M. J.; Duggan, C. The urokinase plasminogen activator system: a rich source of tumour markers for the individualised management of patients with cancer. Clin. Biochem. 2004, 37, 541-548.
7. Overall, C. M.; Kleifeld, O. Validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nature Reviews Cancer 2006, 6, 227-239.
8. van Kempen, L. C. L.; de Visser, K. E.; Coussens, L. M. Inflammation, proteases and cancer. European Journal of Cancer 2006, 42, 728-734.
9. DeClerck, Y. A.; Mercurio, A. M.; Stack, M. S.; Chapman, H. A.; Zutter, M. M.; Muschel, R. J.; Raz, A.; Matrisian, L. M.; Sloane, B. F.; Noel, A.; Hendrix, M. J.; Coussens, L.; Padarathsingh, M. Proteases, extracellular matrix, and cancer: a workshop of the path B study section. Am. J. Pathol. 2004, 164, 1131-1139.
10. Koblinski, J. E.; Ahram, M.; Sloane, B. F. Unraveling the role of proteases in cancer. Clin. Chim. Acta 2000, 291, 113-135.
11. Lynch, C. C.; Matrisian, L. M. Matrix metalloproteinases in tumor-host cell communication. Differentiation 2002, 70, 561-573.
12. Folkman, J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Medicine 1995, 1, 27-30.
13. Kurohane, K.; Tominaga, A.; Sato, K.; North, J. R.; Namba, Y.; Oku, N. Photodynamic therapy targeted to tumor-induced angiogenic vessels. Cancer Letters 167, 49-56.
14. Chen, B.; Pogue, B. W.; Luna, J. M.; Hardman, R. L.; Hoopes, P. J.; Hasan, T. Tumor vascular permeabilization by vascular-targeting photosensitization: effects, mechanism, and therapeutic implications. Clin. Cancer Res. 2006, 12, 917-923.
15. Fingar, V. H.; Taber, S. W.; Haydon, P. S.; Harrison, L. T.; Kempf, S. J.; Wieman, T. J. Vascular damage after photodynamic therapy of solid tumors: a view and comparison of effect in pre-clinical and clinical models at the University of Louisville. In Vivo 2000, 14, 93-100.
16. Fingar, V. H.; Wieman, T. J.; Wiehle, S. A.; Cerrito, P. B. The role of microvascular damage in photodynamic therapy: the effect of treatment on vessel constriction, permeability, and leukocyte adhesion. Cancer Res. 1992, 52, 4914-4921.
17. Frochot, C.; Di Stasio, B.; Vanderesse, R.; Belgy, M.-J.; Dodeller, M.; Guillemin, F.; Viriot, M.-L.; Barberi-Heyob, M. Interest of RGD-containing linear or cyclic peptide targeted tetraphenylchlorin as novel photosensitizers for selective photodynamic activity. Bioorg. Chem. 2007, 35, 205-220.
18. Huang, Z.; Chen, Q.; Luck, D.; Beckers, J.; Wilson, B. C.; Trncic, N.; Larue, S. M.; Blanc, D.; Hetzel, F. W. Studies of a vascular-acting photosensitizer, Pd-bacteriopheophorbide (Tookad), in normal canine prostate and spontaneous canine prostate cancer. Lasers Surg Med 2005, 36, 390-397.
19. McMahon, K. S.; Wieman, T. J.; Moore, P. H.; Fingar, V. H. Effects of photodynamic therapy using mono-L-aspartyl chlorin e6 on vessel constriction, vessel leakage, and tumor response. Cancer Res. 1994, 54, 5374-5379.
20. Wieman, T. J.; Mang, T. S.; Fingar, V. H.; Hill, T. G.; Reed, M. W.; Corey, T. S.; Nguyen, V. Q.; Render, E. R., Jr Effect of photodynamic therapy on blood flow in normal and tumor vessels. Surgery 1988, 104, 512-517.
21. Verhille, M.; Couleaud, P.; Vanderesse, R.; Brault, D.; Barberi-Heyob, M.; Frochot, C. Modulation of photosensitization processes for an improved targeted photodynamic therapy. Curr. Med. Chem. 2010, 17, 3925-3943.
22. Verma, R. P.; Hansch, C. Matrix metalloproteinases (MMPs): chemicalbiological functions and (Q)SARs. Bioorg. Med. Chem. 2007, 15, 2223-2268.
23. Berthelot, T.; Lasne, M.-C.; Déléris, G. New trends in molecular imaging of tumor angiogenesis. Anticancer Agents Med Chem 2008, 8, 497-522.
24. Brown, S.; Bernardo, M. M.; Li, Z.-H.; Kotra, L. P.; Tanaka, Y.; Fridman, R.; Mobashery, S. Potent and Selective Mechanism-Based Inhibition of Gelatinases. J. Am. Chem. Soc. 2000, 122, 6799-6800.
25. Mook, O. R. F.; Frederiks, W. M.; Van Noorden, C. J. F. The role of gelatinases in colorectal cancer progression and metastasis. Biochim. Biophys. Acta 2004, 1705, 69-89.
26. Kline, T.; Torgov, M. Y.; Mendelsohn, B. A.; Cerveny, C. G.; Senter, P. D. Novel antitumor prodrugs designed for activation by matrix metalloproteinases-2 and -9. Mol. Pharm. 2004, 1, 9-22.
27. Stefflova, K.; Chen, J.; Zheng, G. Using molecular beacons for cancer imaging and treatment. Front. Biosci. 2007, 12, 4709-4721.
28. Chen, J.; Stefflova, K.; Niedre, M. J.; Wilson, B. C.; Chance, B.; Glickson, J. D.; Zheng, G. Protease-Triggered Photosensitizing Beacon Based on Singlet Oxygen Quenching and Activation. J. Am. Chem. Soc. 2004, 126, 11450-11451.
29. 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.
30. Chen, J.; Jarvi, M.; Lo, P.-C.; Stefflova, K.; Wilson, B. C.; Zheng, G. Using the singlet oxygen scavenging property of carotenoid in photodynamic molecular beacons to minimize photodamage to non-targeted cells. Photochem. Photobiol. Sci. 2007, 6, 1311-1317.
31. Lovell, J. F.; Chen, J.; Jarvi, M. T.; Cao, W.-G.; Allen, A. D.; Liu, Y.; Tidwell, T. T.; Wilson, B. C.; Zheng, G. FRET Quenching of Photosensitizer Singlet Oxygen Generation. J. Phys. Chem. B 2009, 113, 3203-3211.
32. Lo, P.-C.; Chen, J.; Stefflova, K.; Warren, M. S.; Navab, R.; Bandarchi, B.; Mullins, S.; Tsao, M.; Cheng, J. D.; Zheng, G. Photodynamic molecular beacon triggered by fibroblast activation protein on cancer-associated fibroblasts for diagnosis and treatment of epithelial cancers. J. Med. Chem. 2009, 52, 358-368.
33. Chen, J.; Liu, T. W. B.; Lo, P.-C.; Wilson, B. C.; Zheng, G. "Zipper" molecular beacons: a generalized strategy to optimize the performance of activatable protease probes. Bioconjug. Chem. 2009, 20, 1836-1842.
34. Lovell, J. F.; Chen, J.; Huynh, E.; Jarvi, M. T.; Wilson, B. C.; Zheng, G. Facile synthesis of advanced photodynamic molecular beacon architectures. Bioconjug. Chem. 2010, 21, 1023-1025.
35. Popov, A. V.; Mawn, T. M.; Kim, S.; Zheng, G.; Delikatny, E. J. Design and Synthesis of Phospholipase C and A2-Activatable Near-Infrared Fluorescent Smart Probes. Bioconjugate Chem. 2010, 21, 1724-1727.
36. Nakajima, M.; Welch, D. R.; Belloni, P. N.; Nicolson, G. L. Degradation of basement membrane type IV collagen and lung subendothelial matrix by rat mammary adenocarcinoma cell clones of differing metastatic potentials. Cancer Res. 1987, 47, 4869-4876.
37. Sreenath, T.; Matrisian, L. M.; Stetler-Stevenson, W.; Gattoni-Celli, S.; Pozzatti, R. O. Expression of matrix metalloproteinase genes in transformed rat cell lines of high and low metastatic potential. Cancer Res. 1992, 52, 4942-4947.
38. Nikkola, J.; Vihinen, P.; Vuoristo, M.-S.; Kellokumpu-Lehtinen, P.; Kähäri, V.-M.; Pyrhönen, S. High serum levels of matrix metalloproteinase-9 and matrix metalloproteinase-1 are associated with rapid progression in patients with metastatic melanoma. Clin. Cancer Res. 2005, 11, 5158-5166.
39. Coussens, L. M.; Fingleton, B.; Matrisian, L. M. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002, 295, 2387-2392.
40. Mansour, A. M.; Drevs, J.; Esser, N.; Hamada, F. M.; Badary, O. A.; Unger, C.; Fichtner, I.; Kratz, F. A new approach for the treatment of malignant melanoma: enhanced antitumor efficacy of an albumin-binding doxorubicin prodrug that is cleaved by matrix metalloproteinase 2. Cancer Res. 2003, 63, 4062-4066.
41. Kratz, F.; Drevs, J.; Bing, G.; Stockmar, C.; Scheuermann, K.; Lazar, P.; Unger, C. Development and in vitro efficacy of novel MMP2 and MMP9 specific doxorubicin albumin conjugates. Bioorg. Med. Chem. Lett. 2001, 11, 2001-2006.
42. Terada, T.; Iwai, M.; Kawakami, S.; Yamashita, F.; Hashida, M. Novel PEGmatrix metalloproteinase-2 cleavable peptide-lipid containing galactosylated liposomes for hepatocellular carcinoma-selective targeting. J Control Release 2006, 111, 333-342.
43. Netzel-Arnett, S.; Sang, Q. X.; Moore, W. G.; Navre, M.; Birkedal-Hansen, H.; Van Wart, H. E. Comparative sequence specificities of human 72- and 92-kDa gelatinases (type IV collagenases) and PUMP (matrilysin). Biochemistry 1993, 32, 6427-6432.
44. Jang, J. H.; Kim, M. Y.; Lee, J.-W.; Kim, S. C.; Cho, J. H. Enhancement of the cancer targeting specificity of buforin IIb by fusion with an anionic peptide via a matrix metalloproteinases-cleavable linker. Peptides 2011, 32, 895-899.
45. Seybold, P. G.; Gouterman, M. Porphyrins: XIII: Fluorescence spectra and quantum yields. Journal of Molecular Spectroscopy 1969, 31, 1-13.
46. Redmond, R. W.; Gamlin, J. N. A compilation of singlet oxygen yields from biologically relevant molecules. Photochem. Photobiol. 1999, 70, 391-475.
47. Dale, R. E.; Eisinger, J.; Blumberg, W. E. The orientational freedom of molecular probes. The orientation factor in intramolecular energy transfer. Biophys. J. 1979, 26, 161-193.
48. Knight, C. G.; Willenbrock, F.; Murphy, G. A novel coumarin-labelled peptide for sensitive continuous assays of the matrix metalloproteinases. FEBS Lett. 1992, 296, 263-266.
49. Di Stasio, B.; Frochot, C.; Dumas, D.; Even, P.; Zwier, J.; Müller, A.; Didelon, J.; Guillemin, F.; Viriot, M.-L.; Barberi-Heyob, M. The 2-aminoglucosamide motif improves cellular uptake and photodynamic activity of tetraphenylporphyrin. Eur J Med Chem 2005, 40, 1111-1122.
50. Lindsey, J. S.; Hsu, H. C.; Schreiman, I. C. Synthesis of tetraphenylporphyrins under very mild conditions. Tetrahedron Letters 1986, 27, 4969-4970.
51. Whitlock, H. W.; Hanauer, R.; Oester, M. Y.; Bower, B. K. Diimide reduction of porphyrins. J. Am. Chem. Soc. 1969, 91, 7485-7489.
52. Sibrian-Vazquez, M.; Jensen, T. J.; Hammer, R. P.; Vicente, M. G. H. Peptide-mediated cell transport of water soluble porphyrin conjugates. J. Med. Chem. 2006, 49, 1364-1372.
53. Valanne, A.; Malmi, P.; Appelblom, H.; Niemelä, P.; Soukka, T. A dual-step fluorescence resonance energy transfer-based quenching assay for screening of caspase-3 inhibitors. Anal. Biochem. 2008, 375, 71-81.
54. Murov, S. L.; Hug, G. L.; Carmichael, I. Handbook Of Photochemistry; M. Dekker, 1993.
55. Weissleder, R.; Tung, C.-H.; Mahmood, U.; Bogdanov, A. In vivo imaging of tumors with protease-activated near-infrared fluorescent probes. Nature Biotechnology 1999, 17, 375-378.
56. Tung, C. H.; Bredow, S.; Mahmood, U.; Weissleder, R. Preparation of a cathepsin D sensitive near-infrared fluorescence probe for imaging. Bioconjug. Chem. 1999, 10, 892-896.
57. Tung, C.-H.; Mahmood, U.; Bredow, S.; Weissleder, R. In Vivo Imaging of Proteolytic Enzyme Activity Using a Novel Molecular Reporter. Cancer Res 2000, 60, 4953-4958.
58. Campo, M. A.; Gabriel, D.; Kucera, P.; Gurny, R.; Lange, N. Polymeric photosensitizer prodrugs for photodynamic therapy. Photochem. Photobiol. 2007, 83, 958-965.
59. Gabriel, D.; Campo, M. A.; Gurny, R.; Lange, N. Tailoring protease-sensitive photodynamic agents to specific disease-associated enzymes. Bioconjug. Chem. 2007, 18, 1070-1077.
60. Gabriel, D.; Zuluaga, M.-F.; Martinez, M.-N.; Campo, M. A.; Lange, N. Urokinase-plasminogen-activator sensitive polymeric photosensitizer prodrugs: Design, synthesis and in vitro evaluation. J. Drug Delivery Sci. Technol. 2009, 19, 15-24.
61. Forsyth, P. A.; Wong, H.; Laing, T. D.; Rewcastle, N. B.; Morris, D. G.; Muzik, H.; Leco, K. J.; Johnston, R. N.; Brasher, P. M.; Sutherland, G.; Edwards, D. R. Gelatinase-A (MMP-2), gelatinase-B (MMP-9) and membrane type matrix metalloproteinase-1 (MT1-MMP) are involved in different aspects of the pathophysiology of malignant gliomas. Br. J. Cancer 1999, 79, 1828-1835.
62. Tirand, L.; Frochot, C.; Vanderesse, R.; Thomas, N.; Trinquet, E.; Pinel, S.; Viriot, M.-L.; Guillemin, F.; Barberi-Heyob, M. A peptide competing with VEGF165 binding on neuropilin-1 mediates targeting of a chlorin-type photosensitizer and potentiates its photodynamic activity in human endothelial cells. J Control Release 2006, 111, 153-164.
63. Couleaud, P.; Bechet, D.; Vanderesse, R.; Barberi-Heyob, M.; Faure, A.-C.; Roux, S.; Tillement, O.; Porhel, S.; Guillemin, F.; Frochot, C. Functionalized silica-based nanoparticles for photodynamic therapy. Nanomedicine (Lond) 2011, 6, 995-1009.
64. Bauvois, B. New facets of matrix metalloproteinases MMP-2 and MMP-9 as cell surface transducers: outside-in signaling and relationship to tumor progression. Biochim. Biophys. Acta 2012, 1825, 29-36.
65. Redondo-Muñoz, J.; Ugarte-Berzal, E.; Terol, M. J.; Van den Steen, P. E.; Hernández del Cerro, M.; Roderfeld, M.; Roeb, E.; Opdenakker, G.; García- Marco, J. A.; García-Pardo, A. Matrix metalloproteinase-9 promotes chronic lymphocytic leukemia b cell survival through its hemopexin domain. Cancer Cell 2010, 17, 160-172.
66. Medina, O. P.; Pillarsetty, N.; Glekas, A.; Punzalan, B.; Longo, V.; Gönen, M.; Zanzonico, P.; Smith-Jones, P.; Larson, S. M. Optimizing tumor targeting of the lipophilic EGFR-binding radiotracer SKI 243 using a liposomal nanoparticle delivery system. J Control Release 2011, 149, 292-298.
67. Jang, B.; Choi, Y. Photosensitizer-Conjugated Gold Nanorods for Enzyme- Activatable Fluorescence Imaging and Photodynamic Therapy. Theranostics 2012, 2, 190-197.
68. Zhang, Y.; Gemeinhart, R. A. Improving matrix metalloproteinase-2 specific response of a hydrogel system using electrophoresis. Int J Pharm 2012, 429, 31-37.
69. Singh, H. D.; Bushnak, I.; Unsworth, L. D. Engineered peptides with enzymatically cleavable domains for controlling the release of model protein drug from "soft" nanoparticles. Acta Biomater 2012, 8, 636-645.