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On the cutting edge: protease-sensitive prodrugs for the delivery of photoactive compounds

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Abstract

Most invasive diseases such as cancer or rheumatoid arthritis are characterized by the upregulation of diverse proteases. Since the early 1970s this phenomenon has been exploited for the selective delivery of a variety of drugs. However, only recently have we and others tried to translate this concept into photomedicine. After a short overview of proteases and the proteolytic imbalance in cancer, we will discuss strategies, their potential and limitations to exploit upregulation of proteases for the selective delivery of in vivo fluorescence reporters and photosensitizers. These strategies can be roughly divided into horizontal, i.e. peptide-based, and vertical, i.e. macromolecular approaches. In the former, a short peptide-based substrate is directly tagged to the photoactive compound or used as a linker between the photoactive compound and a substance that alters its photoactivity. In the latter, the protease sensitive sequence serves as linker between a polymeric carrier and the photoactive payload. Such a macromolecular approach may further benefit from passive targeting through the enhanced penetration and retention effect.

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References

  1. C. Lopez-Otin and J. S. Bond, J. Biol. Chem., 2008, 283, 30433–30437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. C. Seife, Science, 1997, 277, 1602–1603.

    Article  CAS  PubMed  Google Scholar 

  3. L. C. van Kempen, K. E. de Visser and L. M. Coussens, Eur. J. Cancer, 2006, 42, 728–734.

    Article  PubMed  CAS  Google Scholar 

  4. A. Garcia-Touchard, T. D. Henry, G. Sangiorgi, L. G. Spagnoli, A. Mauriello, C. Conover and R. S. Schwartz, Arterioscler., Thromb., Vasc. Biol., 2005, 25, 1119–1127.

    Article  CAS  Google Scholar 

  5. S. P. Lutgens, K. B. Cleutjens, M. J. Daemen and S. Heeneman, FASEB J., 2007, 21, 3029–3041.

    Article  CAS  PubMed  Google Scholar 

  6. Q. Wu, H. C. Kuo and G. G. Deng, Biochim. Biophys. Acta, Proteins Proteomics, 2005, 1751, 82–94.

    Article  CAS  Google Scholar 

  7. A. J. Turner and N. N. Nalivaeva, Int. Rev. Neurobiol., 2007, 82, 113–135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. A. Haque, N. L. Banik and S. K. Ray, CNS Neurol. Disord.: Drug Targets, 2008, 7, 270–277.

    Article  CAS  Google Scholar 

  9. C. T. Supuran, A. Scozzafava and B. W. Clare, Med. Res. Rev., 2002, 22, 329–372.

    Article  CAS  PubMed  Google Scholar 

  10. L. Tong, Chem. Rev., 2002, 102, 4609–4626.

    Article  CAS  PubMed  Google Scholar 

  11. J. H. McKerrow, C. Caffrey, B. Kelly, P. Loke and M. Sajid, Annu. Rev. Pathol.: Mech. Dis., 2006, 1, 497–536.

    Article  CAS  Google Scholar 

  12. B. Turk, Nat. Rev. Drug Discovery, 2006, 5, 785–799.

    Article  CAS  PubMed  Google Scholar 

  13. G. Fear, S. Komarnytsky and I. Raskin, Pharmacol. Ther., 2007, 113, 354–368.

    Article  CAS  PubMed  Google Scholar 

  14. A. J. Docherty, T. Crabbe, J. P. O’Connell and C. R. Groom, Biochem. Soc. Symp., 2003, 147–161.

    Google Scholar 

  15. W. A. Denny, Cancer Invest., 2004, 22, 604–619.

    Article  CAS  PubMed  Google Scholar 

  16. J. M. Atkinson, C. S. Siller and J. H. Gill, Br. J. Pharmacol., 2009, 153, 1344–1352.

    Article  CAS  Google Scholar 

  17. M. J. Vicent, H. Ringsdorf and R. Duncan, Adv. Drug Delivery Rev., 2009, 61, 1117–1120.

    Article  CAS  Google Scholar 

  18. R. Duncan, Nat. Rev. Cancer, 2006, 6, 688–701.

    Article  CAS  PubMed  Google Scholar 

  19. R. Duncan, Nat. Rev. Drug Discovery, 2003, 2, 347–360.

    Article  CAS  PubMed  Google Scholar 

  20. A. Carmel, M. Zur, A. Yaron and E. Katchalski, FEBS Lett., 1973, 30, 11–14.

    Article  CAS  PubMed  Google Scholar 

  21. S. A. Latt, D. S. Auld and B. L. Vallee, Anal. Biochem., 1972, 50, 56–62.

    Article  CAS  PubMed  Google Scholar 

  22. R. Weissleder and M. J. Pittet, Nature, 2008, 452, 580–589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. J. Neefjes and N. P. Dantuma, Nat. Rev. Drug Discovery, 2004, 3, 58–69.

    Article  CAS  PubMed  Google Scholar 

  24. U. Mahmood and R. Weissleder, Mol. Cancer Ther., 2003, 2, 489–496.

    CAS  PubMed  Google Scholar 

  25. J. O. McIntyre and L. M. Matrisian, J. Cell. Biochem., 2003, 90, 1087–1097.

    Article  CAS  PubMed  Google Scholar 

  26. X. S. Puente, L. M. Sanchez, A. Gutierrez-Fernandez, G. Velasco and C. Lopez-Otin, Biochem. Soc. Trans., 2005, 33, 331–334.

    Article  CAS  PubMed  Google Scholar 

  27. C. B. Basbaum and Z. Werb, Curr. Opin. Cell Biol., 1996, 8, 731–738.

    Article  CAS  PubMed  Google Scholar 

  28. R. Ramachandran and M. D. Hollenberg, Br. J. Pharmacol., 2008, 153 Suppl. 1, S263–282.

    Article  CAS  Google Scholar 

  29. M. D. Hollenberg, Trends Pharmacol. Sci., 1996, 17, 3–6.

    Article  CAS  PubMed  Google Scholar 

  30. M. J. Page and E. Di Cera, Cell. Mol. Life Sci., 2008, 65, 1220–1236.

    Article  CAS  PubMed  Google Scholar 

  31. A. Barth, K. Frost, M. Wahab, W. Brandt, H. D. Schadler and R. Franke, Drug Des. Discov., 1994, 12, 89–111.

    CAS  PubMed  Google Scholar 

  32. K. Dass, A. Ahmad, A. S. Azmi, S. H. Sarkar and F. H. Sarkar, Cancer Treat. Rev., 2008, 34, 122–136.

    Article  CAS  PubMed  Google Scholar 

  33. T. Syrovets and T. Simmet, Cell. Mol. Life Sci., 2004, 61, 873–885.

    Article  CAS  PubMed  Google Scholar 

  34. N. Sidenius and F. Blasi, Cancer Metastasis Rev., 2003, 22, 205–222.

    Article  CAS  PubMed  Google Scholar 

  35. P. A. Andreasen, L. Kjoller, L. Christensen and M. J. Duffy, Int. J. Cancer, 1997, 72, 1–22.

    Article  CAS  PubMed  Google Scholar 

  36. T. D. Kim, K. S. Song, G. Li, H. Choi, H. D. Park, K. Lim, B. D. Hwang and W. H. Yoon, BMC Cancer, 2006, 6, 211.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. L. Herszenyi, M. Plebani, P. Carraro, M. De Paoli, G. Roveroni, R. Cardin, F. Foschia, Z. Tulassay, R. Naccarato and F. Farinati, Clin. Chim. Acta, 2000, 291, 171–187.

    Article  CAS  PubMed  Google Scholar 

  38. P. J. Cozzi, J. Wang, W. Delprado, M. C. Madigan, S. Fairy, P. J. Russell and Y. Li, Hum. Pathol., 2006, 37, 1442–1451.

    Article  CAS  PubMed  Google Scholar 

  39. A. Daneri-Navarro, G. Macias-Lopez, A. Oceguera-Villanueva, S. Del Toro-Arreola, A. Bravo-Cuellar, R. Perez-Montfort and S. Orbach-Arbouys, Eur. J. Cancer, 1998, 34, 566–569.

    Article  CAS  PubMed  Google Scholar 

  40. S. F. Shariat, J. A. Karam, V. Margulis and P. I. Karakiewicz, BJU Int., 2008, 101, 675–683.

    Article  CAS  PubMed  Google Scholar 

  41. S. R. Denmeade, L. J. Sokoll, D. W. Chan, S. R. Khan and J. T. Isaacs, Prostate, 2001, 48, 1–6.

    Article  CAS  PubMed  Google Scholar 

  42. M. A. Reynolds, K. Kastury, J. Groskopf, J. A. Schalken and H. Rittenhouse, Cancer Lett., 2007, 249, 5–13.

    Article  CAS  PubMed  Google Scholar 

  43. K. Brix, A. Dunkhorst, K. Mayer and S. Jordans, Biochimie, 2008, 90, 194–207.

    Article  CAS  PubMed  Google Scholar 

  44. M. M. Mohamed and B. F. Sloane, Nat.Rev.Cancer, 2006, 6, 764–775.

    Article  CAS  PubMed  Google Scholar 

  45. B. Turk and V. Stoka, FEBS Lett., 2007, 581, 2761–2767.

    Article  CAS  PubMed  Google Scholar 

  46. I. Berdowska, Clin. Chim. Acta, 2004, 342, 41–69.

    Article  CAS  PubMed  Google Scholar 

  47. S. Roshy, B. F. Sloane and K. Moin, Cancer Metastasis Rev., 2003, 22, 271–286.

    Article  CAS  PubMed  Google Scholar 

  48. V. Gocheva and J. A. Joyce, Cell Cycle, 2007, 6, 60–64.

    Article  CAS  PubMed  Google Scholar 

  49. A. Staack, D. Tolic, G. Kristiansen, D. Schnorr, S. A. Loening and K. Jung, Urology, 2004, 63, 1089–1094.

    Article  PubMed  Google Scholar 

  50. T. T. Lah, G. Calaf, E. Kalman, B. G. Shinde, J. Russo, D. Jarosz, J. Zabrecky, R. Somers and I. Daskal, Biol. Chem. Hoppe Seyler, 1995, 376, 357–363.

    Article  CAS  PubMed  Google Scholar 

  51. T. T. Lah, M. Kokalj-Kunovar, M. Drobnic-Kosorok, J. Babnik, R. Golouh, I. Vrhovec and V. Turk, Biol. Chem. Hoppe Seyler, 1992, 373, 595–604.

    Article  CAS  PubMed  Google Scholar 

  52. N. M. Linnerth, K. Sirbovan and R. A. Moorehead, Int. J. Cancer, 2005, 114, 977–982.

    Article  CAS  PubMed  Google Scholar 

  53. L. G. Hazen, F. E. Bleeker, B. Lauritzen, S. Bahns, J. Song, A. Jonker, B. E. Van Driel, H. Lyon, U. Hansen, A. Kohler and C. J. Van Noorden, J. Histochem. Cytochem., 2000, 48, 1421–1430.

    Article  CAS  PubMed  Google Scholar 

  54. A. Adenis, G. Huet, F. Zerimech, B. Hecquet, M. Balduyck and J. P. Peyrat, Cancer Lett., 1995, 96, 267–275.

    Article  CAS  PubMed  Google Scholar 

  55. S. Shuja, K. Sheahan and M. J. Murnane, Int. J. Cancer, 1991, 49, 341–346.

    Article  CAS  PubMed  Google Scholar 

  56. W. Bode, F. X. Gomis-Ruth and W. Stockler, FEBS Lett., 1993, 331, 134–140.

    Article  CAS  PubMed  Google Scholar 

  57. G. Murphy and H. Nagase, Mol. Aspects Med., 2008, 29, 290–308.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. C. J. Malemud, Front. Biosci., 2006, 11, 1696–1701.

    Article  CAS  PubMed  Google Scholar 

  59. H. E. Van Wart and H. Birkedal-Hansen, Proc. Natl. Acad. Sci. U. S. A., 1990, 87, 5578–5582.

    Article  PubMed  PubMed Central  Google Scholar 

  60. L. A. Liotta, K. Tryggvason, S. Garbisa, I. Hart, C. M. Foltz and S. Shafie, Nature, 1980, 284, 67–68.

    Article  CAS  PubMed  Google Scholar 

  61. M. J. Duffy, D. J. Lynn, A. T. Lloyd and C. M. O’Shea, Thromb. Haemost., 2003, 89, 622–631.

    Article  CAS  PubMed  Google Scholar 

  62. D. F. Seals and S. A. Courtneidge, Genes Dev., 2003, 17, 7–30.

    Article  CAS  PubMed  Google Scholar 

  63. L. J. McCawley and L. M. Matrisian, Curr. Opin. Cell Biol., 2001, 13, 534–540.

    Article  CAS  PubMed  Google Scholar 

  64. E. I. Deryugina and J. P. Quigley, Cancer Metastasis Rev., 2006, 25, 9–34.

    Article  CAS  PubMed  Google Scholar 

  65. R. Hoekstra, F. A. Eskens and J. Verweij, Oncologist, 2001, 6, 415–427.

    Article  CAS  PubMed  Google Scholar 

  66. C. E. Brinckerhoff, J. L. Rutter and U. Benbow, Clin. Cancer Res., 2000, 6, 4823–4830.

    CAS  PubMed  Google Scholar 

  67. M. Pesta, L. Holubec, Jr., O. Topolcan, M. Cerna, K. Rupert, L. S. Holubec, V. Treska, S. Kormunda, L. Elgrova, J. Finek and R. Cerny, Anticancer Res., 2005, 25, 3387–3391.

    CAS  PubMed  Google Scholar 

  68. O. Schwandner, A. Schlamp, R. Broll and H. P. Bruch, Int. J. Colorectal Dis., 2006, 22, 127–136.

    Article  PubMed  Google Scholar 

  69. S. Zucker and J. Vacirca, Cancer Metastasis Rev., 2004, 23, 101–117.

    Article  CAS  PubMed  Google Scholar 

  70. S. L. Parsons, S. A. Watson, H. M. Collins, N. R. Griffin, P. A. Clarke and R. J. Steele, Br. J. Cancer, 1998, 78, 1495–1502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. D. W. Visscher, M. Hoyhtya, S. K. Ottosen, C. M. Liang, F. H. Sarkar, J. D. Crissman and R. Fridman, Int. J. Cancer, 1994, 59, 339–344.

    Article  CAS  PubMed  Google Scholar 

  72. F. J. Vizoso, L. O. Gonzalez, M. D. Corte, J. C. Rodriguez, J. Vazquez, M. L. Lamelas, S. Junquera, A. M. Merino and J. L. Garcia-Muniz, Br. J. Cancer, 2007, 96, 903–911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. B. Davies, J. Waxman, H. Wasan, P. Abel, G. Williams, T. Krausz, D. Neal, D. Thomas, A. Hanby and F. Balkwill, Cancer Res., 1993, 53, 5365–5369.

    CAS  PubMed  Google Scholar 

  74. X. Zhang, S. Zhu, G. Luo, L. Zheng, J. Wei, J. Zhu, Q. Mu and N. Xu, Anticancer Res., 2007, 27, 2791–2795.

    CAS  PubMed  Google Scholar 

  75. D. Liu, J. Nakano, S. Ishikawa, H. Yokomise, M. Ueno, K. Kadota, M. Urushihara and C. L. Huang, Lung Cancer, 2007, 58, 384–391.

    Article  PubMed  Google Scholar 

  76. L. E. Guagliardi, B. Koppelman, J. S. Blum, M. S. Marks, P. Cresswell and F. M. Brodsky, Nature, 1990, 343, 133–139.

    Article  CAS  PubMed  Google Scholar 

  77. N. M. Hooper, Essays Biochem., 2002, 38, 1–8.

    Article  CAS  PubMed  Google Scholar 

  78. B. M. Dunn, Current Protocols in Protein Science, 2001, Chapter 21, Unit 21 23.

    Google Scholar 

  79. P. B. Szecsi, Scand. J. Clin. Lab. Invest., 1992, 210, 5–22.

    Article  CAS  Google Scholar 

  80. S. Aziz, S. Pervez, S. Khan, N. Kayani and M. Rahbar, Pathol., Res. Prac., 2001, 197, 551–557.

    Article  CAS  Google Scholar 

  81. L. B. Riley, M. K. Lange, R. J. Browne, P. J. Cochrane, I. J. Choi, B. Davis, S. Arcona and J. A. Alhadeff, Breast Cancer Res. Treat., 2000, 60, 173–179.

    Article  CAS  PubMed  Google Scholar 

  82. A. K. Tandon, G. M. Clark, G. C. Chamness, J. M. Chirgwin and W. L. McGuire, N. Engl. J. Med., 1990, 322, 297–302.

    Article  CAS  PubMed  Google Scholar 

  83. J. P. Cherry, J. A. Mordente, J. R. Chapman, M. S. Choudhury, H. Tazaki, C. Mallouh and S. Konno, J. Urol., 1998, 160, 2223–2228.

    Article  CAS  PubMed  Google Scholar 

  84. R. Makar, A. Mason, J. M. Kittelson, G. T. Bowden, A. E. Cress and R. B. Nagle, Mod. Pathol., 1994, 7, 747–751.

    CAS  PubMed  Google Scholar 

  85. P. K. Lipponen, J. Pathol., 1996, 178, 59–64.

    Article  CAS  PubMed  Google Scholar 

  86. R. Vassar, D. M. Kovacs, R. Yan and P. C. Wong, J. Neurosci., 2009, 29, 12787–12794.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. J. Rao, A. Dragulescu-Andrasi and H. Yao, Curr. Opin. Biotechnol., 2007, 18, 17–25.

    Article  CAS  PubMed  Google Scholar 

  88. P. Jichlinski, L. Guillou, S. J. Karlsen, P. U. Malmstrom, D. Jocham, B. Brennhovd, E. Johansson, T. Gartner, N. Lange, H. van den Bergh and H. J. Leisinger, J. Urol., 2003, 170, 226–229.

    Article  PubMed  Google Scholar 

  89. N. Lange, P. Jichlinski, M. Zellweger, M. Forrer, A. Marti, L. Guillou, P. Kucera, G. Wagnieres and H. van den Bergh, Br. J. Cancer, 1999, 80, 185–193.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. A. Stenzl, M. Burger, Y. Fradet, L. A. Mynderse, M. S. Soloway, J. A. Witjes, M. Kriegmair, A. Karl, Y. Shen and H. B. Grossman, J. Urol., 2010, 184, 1907–1913.

    Article  PubMed  PubMed Central  Google Scholar 

  91. S. Folli, P. Westermann, D. Braichotte, A. Pelegrin, G. Wagnieres, H. van den Bergh and J. P. Mach, Cancer Res., 1994, 54, 2643–2649.

    CAS  PubMed  Google Scholar 

  92. A. Pelegrin, S. Folli, F. Buchegger, J. P. Mach, G. Wagnieres and H. van den Bergh, Cancer, 1991, 67, 2529–2537.

    Article  CAS  PubMed  Google Scholar 

  93. T. Förster, Discuss. Faraday Soc., 1959, 27. 94 P. R. Selvin, Nat. Struct. Biol., 2000, 7, 730–734.

    Google Scholar 

  94. E. D. Matayoshi, G. T. Wang, G. A. Krafft and J. Erickson, Science, 1990, 247, 954–958.

    Article  CAS  PubMed  Google Scholar 

  95. C. G. Knight, Methods Enzymol., 1995, 248, 18–34.

    Article  CAS  PubMed  Google Scholar 

  96. T. Jiang, E. S. Olson, Q. T. Nguyen, M. Roy, P. A. Jennings and R. Y. Tsien, Proc. Natl. Acad. Sci. U. S. A., 2004, 101, 17867–17872.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. L. J. Jones, R. H. Upson, R. P. Haugland, N. Panchuk-Voloshina and M. Zhou, Anal. Biochem., 1997, 251, 144–152.

    Article  CAS  PubMed  Google Scholar 

  98. M. Sameni, J. Dosescu, K. Moin and B. F. Sloane, Mol. Imaging, 2003, 2, 159–175.

    Article  PubMed  Google Scholar 

  99. M. Sameni, J. Dosescu and B. F. Sloane, Biol. Chem., 2001, 382, 785–788.

    Article  CAS  PubMed  Google Scholar 

  100. M. Sameni, K. Moin and B. F. Sloane, Neoplasia, 2000, 2, 496–504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. E. Marecos, R. Weissleder and A. Bogdanov, Jr., Bioconjugate Chem., 1998, 9, 184–191.

    Article  CAS  Google Scholar 

  102. A. A. Bogdanov, Jr., R. Weissleder and T. J. Brady, ed. V. P. Torchilin, CRC, Boca Raton, Fla, 1995, pp. 501–522.

  103. R. J. Callahan, A. Bogdanov, Jr., A. J. Fischman, T. J. Brady and R. Weissleder, AJR Am. J. Roentgenol., 1998, 171, 137–143.

    Article  CAS  PubMed  Google Scholar 

  104. R. Weissleder, H. C. Cheng, E. Marecos, K. Kwong and A. Bogdanov, Jr., Eur. J. Cancer, 1998, 34, 1448–1454.

    Article  CAS  PubMed  Google Scholar 

  105. R. Weissleder, C. H. Tung, U. Mahmood and A. Bogdanov, Jr., Nat. Biotechnol., 1999, 17, 375–378.

    Article  CAS  PubMed  Google Scholar 

  106. A. A. Bogdanov, Jr., C. P. Lin, M. Simonova, L. Matuszewski and R. Weissleder, Neoplasia, 2002, 4, 228–236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. A. Wunder, C. H. Tung, U. Muller-Ladner, R. Weissleder and U. Mahmood, Arthritis Rheum., 2004, 50, 2459–2465.

    Article  CAS  PubMed  Google Scholar 

  108. E. S. Izmailova, N. Paz, H. Alencar, M. Chun, L. Schopf, M. Hepperle, J. H. Lane, G. Harriman, Y. Xu, T. Ocain, R. Weissleder, U. Mahmood, A. M. Healy and B. Jaffee, Arthritis Rheum., 2007, 56, 117–128.

    Article  CAS  PubMed  Google Scholar 

  109. C. P. Schultz and R. Weissleder, Siemens Medical Magazine, 2007, December 2007, 3–7.

    Google Scholar 

  110. E. Gounaris, C. H. Tung, C. Restaino, R. Maehr, R. Kohler, J. A. Joyce, H. L. Ploegh, T. A. Barrett, R. Weissleder and K. Khazaie, PLoS One, 2008, 3, e2916.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  111. J. Chen, C. H. Tung, U. Mahmood, V. Ntziachristos, R. Gyurko, M. C. Fishman, P. L. Huang and R. Weissleder, Circulation, 2002, 105, 2766–2771.

    Article  PubMed  Google Scholar 

  112. C. Bremer, V. Ntziachristos, B. Weitkamp, G. Theilmeier, W. Heindel and R. Weissleder, Invest. Radiol., 2005, 40, 321–327.

    Article  CAS  PubMed  Google Scholar 

  113. C. Bremer, C. H. Tung, A. Bogdanov, Jr. and R. Weissleder, Radiology, 2002, 222, 814–818.

    Article  PubMed  Google Scholar 

  114. C. H. Tung, S. Bredow, U. Mahmood and R. Weissleder, Bioconjugate Chem., 1999, 10, 892–896.

    Article  CAS  Google Scholar 

  115. C. H. Tung, U. Mahmood, S. Bredow and R. Weissleder, Cancer Res., 2000, 60, 4953–4958.

    CAS  PubMed  Google Scholar 

  116. C. Bremer, S. Bredow, U. Mahmood, R. Weissleder and C. H. Tung, Radiology, 2001, 221, 523–529.

    Article  CAS  PubMed  Google Scholar 

  117. C. Bremer, C. H. Tung and R. Weissleder, Nat.Med., 2001, 7, 743–748.

    Article  CAS  PubMed  Google Scholar 

  118. J. O. McIntyre, B. Fingleton, K. S. Wells, D. W. Piston, C. C. Lynch, S. Gautam and L. M. Matrisian, Biochem. J., 2004, 377, 617–628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. G. Zheng, J. Chen, K. Stefflova, M. Jarvi, H. Li and B. C. Wilson, Proc. Natl. Acad. Sci. U. S. A., 2007, 104, 8989–8994.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. J. O. Deguchi, M. Aikawa, C. H. Tung, E. Aikawa, D. E. Kim, V. Ntziachristos, R. Weissleder and P. Libby, Circulation, 2006, 114, 55–62.

    Article  PubMed  Google Scholar 

  121. Q. T. Nguyen, E. S. Olson, T. A. Aguilera, T. Jiang, M. Scadeng, L. G. Ellies and R. Y. Tsien, Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 4317–4322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. E. S. Olson, T. Jiang, T. A. Aguilera, Q. T. Nguyen, L. G. Ellies, M. Scadeng and R. Y. Tsien, Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 4311–4316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. J. K. Hsiao, B. Law, R. Weissleder and C. H. Tung, J. Biomed. Opt., 2006, 11, 34013.

    Article  PubMed  CAS  Google Scholar 

  124. B. Law, A. Curino, T. H. Bugge, R. Weissleder and C. H. Tung, Chem. Biol., 2004, 11, 99–106.

    Article  CAS  PubMed  Google Scholar 

  125. D. Gabriel, M. F. Zuluaga, M. N. Martinez, M. A. Campo and N. Lange, J. Drug Deliv. Sci. Technol., 2009, 19, 15–24.

    Article  CAS  Google Scholar 

  126. D. Gabriel, N. Busso, A. So, H. van den Bergh, R. Gurny and N. Lange, J. Controlled Release, 2009, 138, 225–234.

    Article  CAS  Google Scholar 

  127. F. A. Jaffer, C. H. Tung, R. E. Gerszten and R. Weissleder, Arterioscler., Thromb., Vasc. Biol., 2002, 22, 1929–1935.

    Article  CAS  Google Scholar 

  128. C. H. Tung, R. E. Gerszten, F. A. Jaffer and R. Weissleder, ChemBioChem, 2002, 3, 207–211.

    Article  CAS  PubMed  Google Scholar 

  129. J. Chen, K. Stefflova, M. J. Niedre, B. C. Wilson, B. Chance, J. D. Glickson and G. Zheng, J. Am. Chem. Soc., 2004, 126, 11450–11451.

    Article  CAS  PubMed  Google Scholar 

  130. S. M. Messerli, S. Prabhakar, Y. Tang, K. Shah, M. L. Cortes, V. Murthy, R. Weissleder, X. O. Breakefield and C. H. Tung, Neoplasia, 2004, 6, 95–105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. K. Kim, M. Lee, H. Park, J. H. Kim, S. Kim, H. Chung, K. Choi, I. S. Kim, B. L. Seong and I. C. Kwon, J. Am. Chem. Soc., 2006, 128, 3490–3491.

    Article  CAS  PubMed  Google Scholar 

  132. P. C. Lo, J. Chen, K. Stefflova, M. S. Warren, R. Navab, B. Bandarchi, S. Mullins, M. Tsao, J. D. Cheng and G. Zheng, J. Med. Chem., 2009, 52, 358–368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. D. Gabriel, M. A. Campo, R. Gurny and N. Lange, Bioconjugate Chem., 2007, 18, 1070–1077.

    Article  CAS  Google Scholar 

  134. K. Shah, C. H. Tung, C. H. Chang, E. Slootweg, T. O’Loughlin, X. O. Breakefield and R. Weissleder, Cancer Res., 2004, 64, 273–278.

    Article  CAS  PubMed  Google Scholar 

  135. K. M. Kozloff, L. Quinti, C. Tung, R. Weissleder and U. Mahmood, J. Musculoskeletal Neuronal Interact., 2006, 6, 353.

    CAS  Google Scholar 

  136. K. Shah, C. H. Tung, K. Yang, R. Weissleder and X. O. Breakefield, Cancer Res., 2004, 64, 3236–3242.

    Article  CAS  PubMed  Google Scholar 

  137. Y. P. Kim, Y. H. Oh, E. Oh, S. Ko, M. K. Han and H. S. Kim, Anal. Chem., 2008, 80, 4634–4641.

    Article  CAS  PubMed  Google Scholar 

  138. I. L. Medintz, A. R. Clapp, F. M. Brunel, T. Tiefenbrunn, H. T. Uyeda, E. L. Chang, J. R. Deschamps, P. E. Dawson and H. Mattoussi, Nat. Mater., 2006, 5, 581–589.

    Article  CAS  PubMed  Google Scholar 

  139. C. J. Mu, D. A. Lavan, R. S. Langer and B. R. Zetter, ACS Nano, 2010, 4, 1511–1520.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. J. F. Lovell, J. Chen, M. T. Jarvi, W. G. Cao, A. D. Allen, Y. Liu, T. T. Tidwell, B. C. Wilson and G. Zheng, J. Phys. Chem. B, 2009, 113, 3203–3211.

    Article  CAS  PubMed  Google Scholar 

  141. J. R. McCarthy, J. M. Perez, C. Bruckner and R. Weissleder, Nano Lett., 2005, 5, 2552–2556.

    Article  CAS  PubMed  Google Scholar 

  142. S. Hackbarth, E. A. Ermilov and B. Roder, Opt. Commun., 2005, 248, 295–306.

    Article  CAS  Google Scholar 

  143. F. Ito, Y. Ishibashi, S. R. Khan, H. Miyasaka, K. Kameyama, M. Morisue, A. Satake, K. Ogawa and Y. Kobuke, J. Phys. Chem. A, 2006, 110, 12734–12742.

    Article  CAS  PubMed  Google Scholar 

  144. M. Maes, H. Sasabe, N. Kihara, Y. Araki, Y. Furusho, K. Mizuno, T. Takata and O. Ito, J. Porphyrins Phthalocyanines, 2005, 9, 724–734.

    Article  CAS  Google Scholar 

  145. G. Zheng, M. Aoudia, M. A. Lee, K. M. Rodgers, T. J. Smith, T. J. Dougherty and R. K. Pandey, J. Chem. Soc., Perkin Trans. 1, 2000, 3113–3121.

    Article  Google Scholar 

  146. K. Stefflova, J. Chen, H. Li and G. Zheng, Mol. Imaging, 2006, 5, 520–532.

    Article  PubMed  Google Scholar 

  147. J. Chen, T. W. Liu, P. C. Lo, B. C. Wilson and G. Zheng, Bioconjugate Chem., 2009.

    Google Scholar 

  148. N. S. Soukos, M. R. Hamblin and T. Hasan, Photochem. Photobiol., 1997, 65, 723–729.

    Article  CAS  PubMed  Google Scholar 

  149. M. R. Hamblin, J. L. Miller, I. Rizvi, H. G. Loew and T. Hasan, Br. J. Cancer, 2003, 89, 937–943.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. M. R. Hamblin, J. L. Miller, I. Rizvi, B. Ortel, E. V. Maytin and T. Hasan, Cancer Res., 2001, 61, 7155–7162.

    CAS  PubMed  Google Scholar 

  151. Y. Choi, R. Weissleder and C. H. Tung, ChemMedChem, 2006, 1, 698–701.

    Article  CAS  PubMed  Google Scholar 

  152. Y. Choi, R. Weissleder and C. H. Tung, Cancer Res., 2006, 66, 7225–7229.

    Article  CAS  PubMed  Google Scholar 

  153. M. A. Campo, D. Gabriel, P. Kucera, R. Gurny and N. Lange, Photochem. Photobiol., 2007, 83, 958–965.

    Article  CAS  PubMed  Google Scholar 

  154. B. C. Bae and K. Na, Biomaterials, 2010, 31, 6325–6335.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. School of Pharmaceutical Sciences, University of Lausanne, University of Geneva, 30, Quai Ernest Ansermet, CH 1211, Geneva, Switzerland

    Doris Gabriel, Maria Fernanda Zuluaga & Norbert Lange

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  1. Doris Gabriel
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  2. Maria Fernanda Zuluaga
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  3. Norbert Lange
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Correspondence to Norbert Lange.

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This article is published as part of a themed issue on immunological aspects and drug delivery technologies in PDT.

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Gabriel, D., Zuluaga, M.F. & Lange, N. On the cutting edge: protease-sensitive prodrugs for the delivery of photoactive compounds. Photochem Photobiol Sci 10, 689–703 (2011). https://doi.org/10.1039/c0pp00341g

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