Photochemical internalization (PCI) in cancer therapy: From bench towards bedside medicine

Journal of Photochemistry and Photobiology B: Biology

Volumn 96, Issue 2, 2009, Pages 83-92

  Norum, Ole Jacob ^a,b   Selbo, Pål Kristian ^a   Weyergang, Anette ^a   Giercksky, Karl Erik ^b   Berg, Kristian ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Bleomycin; Cancer therapy; Photochemical internalization; Photodynamic therapy; Phthalocyanine

Indexed keywords

ADENOVIRUS VECTOR; ALUMINUM PHTHALOCYANINE DISULFONATE; AMINOLEVULINIC ACID; AMINOLEVULINIC ACID METHYL ESTER; ANTINEOPLASTIC AGENT; BLEOMYCIN; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; HEMATOPORPHYRIN DERIVATIVE; IMMUNOTOXIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY MOC31; NUCLEIC ACID; PARVOVIRUS VECTOR; PHOTOFRIN; PHOTOFRIN II; PHOTOSENSITIZING AGENT; POLYMER; PROTEIN DERIVATIVE; PROTEIN TYROSINE KINASE INHIBITOR; REACTIVE OXYGEN METABOLITE; RIBOSOME INACTIVATING PROTEIN; RIBOSOME INACTIVATING PROTEIN 1; SAPORIN; SMALL INTERFERING RNA; TEMOPORFIN; TETRAKIS(3 HYDROXYPHENYL)CHLORIN; TETRAPHENYLPORPHINE DISULFONATE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ACTINIC KERATOSIS; ADVANCED CANCER; BASAL CELL CARCINOMA; BLADDER CANCER; BOWEN DISEASE; BRACHYTHERAPY; CANCER GENE THERAPY; CANCER PALLIATIVE THERAPY; CARCINOMA IN SITU; CAUTERIZATION; CELL ACTIVATION; CELL VACUOLE; CLINICAL EFFECTIVENESS; CLINICAL TRIAL; CRYOTHERAPY; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG POTENCY; DRUG STRUCTURE; DRUG SYNTHESIS; ENDOCYTOSIS; ESOPHAGUS CANCER; ESOPHAGUS CARCINOMA; ESOPHAGUS RESECTION; FIBROSARCOMA; HEAD AND NECK CANCER; HUMAN; IMMUNE RESPONSE; IMMUNOSTIMULATION; LOW LEVEL LASER THERAPY; LUNG CANCER; LYSOSOME; MACROMOLECULE; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; PHOTOCHEMICAL INTERNALIZATION; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; RADIOFREQUENCY ABLATION; REVIEW; SKIN CANCER; SOLID TUMOR; STOMACH CANCER; TARGET CELL DESTRUCTION; UNSPECIFIED SIDE EFFECT; UTERINE CERVIX CARCINOMA IN SITU; VIRAL GENE DELIVERY SYSTEM; VULVA CANCER;

ANIMALS; CHEMISTRY, PHARMACEUTICAL; HUMANS; MEDICINE; NEOPLASMS; PHOTOSENSITIZING AGENTS;

ANIMALIA;

EID: 67649662212     PISSN: 10111344     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2009.04.012     Document Type: Review

References (82)

1. Dolmans D.E., Fukumura D., and Jain R.K. Photodynamic therapy for cancer. Nat. Rev. Cancer. 3 (2003) 380-387
2. Castano A.P., Mroz P., and Hamblin M.R. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer. 6 (2006) 535-545
3. Brown S.B., Brown E.A., and Walker I. The present and future role of photodynamic therapy in cancer treatment. Lancet Oncol. 5 (2004) 497-508
4. Hopper C. Photodynamic therapy: a clinical reality in the treatment of cancer. Lancet Oncol. 1 (2000) 212-219
5. Triesscheijn M., Baas P., Schellens J.H., and Stewart F.A. Photodynamic therapy in oncology. The Oncologist 11 (2006) 1034-1044
6. Wilson B.C., and Patterson M.S. The physics, biophysics and technology of photodynamic therapy. Phys. Med. Biol. 53 (2008) R61-R109
7. Juzeniene A., Peng Q., and Moan J. Milestones in the development of photodynamic therapy and fluorescence diagnosis. Photochem. Photobiol. Sci. 6 (2007) 1234-1245
8. Stewart F., Baas P., and Star W. What does photodynamic therapy have to offer radiation oncologists (or their cancer patients)?. Radiother. Oncol. 48 (1998) 233-248
9. Hornung R., Walt H., Crompton N.E., Keefe K.A., Jentsch B., Perewusnyk G., Haller U., and Kochli O.R. m-THPC-mediated photodynamic therapy (PDT) does not induce resistance to chemotherapy, radiotherapy or PDT on human breast cancer cells in vitro. Photochem. Photobiol. 68 (1998) 569-574
10. Radu A., Grosjean P., Fontolliet C., Wagnieres G., Woodtli A., Bergh H.V., and Monnier P. Photodynamic therapy for 101 early cancers of the upper aerodigestive tract, the esophagus, and the bronchi: a single-institution experience. Diagn. Ther. Endosc. 5 (1999) 145-154
11. Mackenzie G.D., Jamieson N.F., Novelli M.R., Mosse C.A., Clark B.R., Thorpe S.M., Bown S.G., and Lovat L.B. How light dosimetry influences the efficacy of photodynamic therapy with 5-aminolaevulinic acid for ablation of high-grade dysplasia in Barrett's esophagus. Lasers Med. Sci. 23 (2008) 203-210
12. Pouw R.E., Gondrie J.J., Sondermeijer C.M., ten Kate F.J., van Gulik T.M., Krishnadath K.K., Fockens P., Weusten B.L., and Bergman J.J. Eradication of Barrett esophagus with early neoplasia by radiofrequency ablation, with or without endoscopic resection. J. Gastrointest. Surg. 12 (2008) 1627-1636
13. Sheski F.D., and Mathur P.N. Endoscopic treatment of early-stage lung cancer. Cancer Control 7 (2000) 35-44
14. Zoepf T. Photodynamic therapy of cholangiocarcinoma. HPB 10 (2008) 161-163 (Oxford)
15. Moghissi K., Dixon K., Stringer M., Freeman T., Thorpe A., and Brown S. The place of bronchoscopic photodynamic therapy in advanced unresectable lung cancer: experience of 100 cases. Eur. J. Cardiothorac. Surg. 15 (1999) 1-6
16. Lou P.J., Jager H.R., Jones L., Theodossy T., Bown S.G., and Hopper C. Interstitial photodynamic therapy as salvage treatment for recurrent head and neck cancer. Brit. J. Cancer. 91 (2004) 441-446
17. Friedberg J.S., Mick R., Stevenson J., Metz J., Zhu T., Buyske J., Sterman D.H., Pass H.I., Glatstein E., and Hahn S.M. A phase I study of Foscan-mediated photodynamic therapy and surgery in patients with mesothelioma. Ann. Thorac. Surg. 75 (2003) 952-959
18. Friedberg J.S., Mick R., Stevenson J.P., Zhu T., Busch T.M., Shin D., Smith D., Culligan M., Dimofte A., Glatstein E., and Hahn S.M. Phase II trial of pleural photodynamic therapy and surgery for patients with non-small-cell lung cancer with pleural spread. J. Clin. Oncol. 22 (2004) 2192-2201
19. Hahn S.M., Fraker D.L., Mick R., Metz J., Busch T.M., Smith D., Zhu T., Rodriguez C., Dimofte A., Spitz F., Putt M., Rubin S.C., Menon C., Wang H.W., Shin D., Yodh A., and Glatstein E. A phase II trial of intraperitoneal photodynamic therapy for patients with peritoneal carcinomatosis and sarcomatosis. Clin. Cancer Res. 12 (2006) 2517-2525
20. Stylli S.S., Kaye A.H., MacGregor L., Howes M., and Rajendra P. Photodynamic therapy of high grade glioma - long term survival. J. Clin. Neurosci. 12 (2005) 389-398
21. Usuda J., Kato H., Okunaka T., Furukawa K., Tsutsui H., Yamada K., Suga Y., Honda H., Nagatsuka Y., Ohira T., Tsuboi M., and Hirano T. Photodynamic therapy (PDT) for lung cancers. J. Thorac. Oncol. 1 (2006) 489-493
22. Wang J.B., and Liu L.X. Use of photodynamic therapy in malignant lesions of stomach, bile duct, pancreas, colon and rectum. Hepatogastroenterology 54 (2007) 718-724
23. Nakamura T., Kusuzaki K., Matsubara T., Matsumine A., Murata H., and Uchida A. A new limb salvage surgery in cases of high-grade soft tissue sarcoma using photodynamic surgery, followed by photo- and radiodynamic therapy with acridine orange. J. Surg. Oncol. 97 (2008) 523-528
24. Jerjes W., Upile T., Betz C.S., El M.M., Abbas S., Wright A., and Hopper C. The application of photodynamic therapy in the head and neck. Dent. Update 34 (2007) 478-480
25. Ortner M.E., Caca K., Berr F., Liebetruth J., Mansmann U., Huster D., Voderholzer W., Schachschal G., Mossner J., and Lochs H. Successful photodynamic therapy for nonresectable cholangiocarcinoma: a randomized prospective study. Gastroenterology 125 (2003) 1355-1363
26. Cuenca R.E., Allison R.R., Sibata C., and Downie G.H. Breast cancer with chest wall progression: treatment with photodynamic therapy. Ann. Surg. Oncol. 11 (2004) 322-327
27. Pass H.I., Temeck B.K., Kranda K., Thomas G., Russo A., Smith P., Friauf W., and Steinberg S.M. Phase III randomized trial of surgery with or without intraoperative photodynamic therapy and postoperative immunochemotherapy for malignant pleural mesothelioma. Ann. Surg. Oncol. 4 (1997) 628-633
28. Ris H.B. Photodynamic therapy as an adjunct to surgery for malignant pleural mesothelioma. Lung Cancer 49 Suppl. 1 (2005) S65-S68
29. Berg K., Selbo P.K., Prasmickaite L., Tjelle T.E., Sandvig K., Moan J., Gaudernack G., Fodstad O., Kjolsrud S., Anholt H., Rodal G.H., Rodal S.K., and Hogset A. Photochemical internalization: a novel technology for delivery of macromolecules into cytosol. Cancer Res. 59 (1999) 1180-1183
30. Selbo P.K., Sivam G., Fodstad O., Sandvig K., and Berg K. In vivo documentation of photochemical internalization, a novel approach to site specific cancer therapy. Int. J. Cancer 92 (2001) 761-766
31. Norum O.J., Gaustad J.-V., Angell-Pettersen E., Rofstad E.K., Peng Q., Giercksky K.-E., and Berg K. Photochemical internalization of bleomycin is superior to photodynamic therapy due to the therapeutic effect in the tumor periphery. Photochem. Photobiol. 85 (2009) 740-749
32. Mukherjee S., Ghosh R.N., and Maxfield F.R. Endocytosis. Physiol Rev. 77 (1997) 759-803
33. Lloyd J.B. Lysosome membrane permeability: implications for drug delivery. Adv. Drug Deliv. Rev. 41 (2000) 189-200
34. Hatz S., Poulsen L., and Ogilby P.R. Time-resolved singlet oxygen phosphorescence measurements from photosensitized experiments in single cells: effects of oxygen diffusion and oxygen concentration. Photochem. Photobiol. 84 (2008) 1284-1290
35. Moan J., and Berg K. The photodegradation of porphyrins in cells can be used to estimate the lifetime of singlet oxygen. Photochem. Photobiol. 53 (1991) 549-553
36. Niedre M.J., Patterson M.S., Giles A., and Wilson B.C. Imaging of photodynamically generated singlet oxygen luminescence in vivo. Photochem. Photobiol. 81 (2005) 941-943
37. Jimenez-Banzo A., Sagrista M.L., Mora M., and Nonell S. Kinetics of singlet oxygen photosensitization in human skin fibroblasts. Free Radic. Biol. Med. 44 (2008) 1926-1934
38. Prasmickaite L., Hogset A., and Berg K. Evaluation of different photosensitizers for use in photochemical gene transfection. Photochem. Photobiol. 73 (2001) 388-395
39. Prasmickaite L., Hogset A., Selbo P.K., Engesaeter B.O., Hellum M., and Berg K. Photochemical disruption of endocytic vesicles before delivery of drugs: a new strategy for cancer therapy. Brit. J. Cancer. 86 (2002) 652-657
40. Berg K., and Moan J. Lysosomes as photochemical targets. Int. J. Cancer. 59 (1994) 814-822
41. Thrush G.R., Lark L.R., Clinchy B.C., and Vitetta E.S. Immunotoxins: an update. Annu. Rev. Immunol. 14 (1996) 49-71
42. Berg K., Prasmickaite L., Selbo P.K., Hellum M., Bonsted A., and Hogset A. Photochemical internalization (PCI) - a novel technology for release of macromolecules from endocytic vesicles. Oftalmologia 56 (2003) 67-71
43. Selbo P.K., Sandvig K., Kirveliene V., and Berg K. Release of gelonin from endosomes and lysosomes to cytosol by photochemical internalization. Biochim. Biophys. Acta. 1475 (2000) 307-313
44. Dietze A., Peng Q., Selbo P.K., Kaalhus O., Muller C., Bown S., and Berg K. Enhanced photodynamic destruction of a transplantable fibrosarcoma using photochemical internalisation of gelonin. Brit. J. Cancer 92 (2005) 2004-2009
45. Wu M. Enhancement of immunotoxin activity using chemical and biological reagents. Brit. J. Cancer 75 (1997) 1347-1355
46. Selbo P.K., Sivam G., Fodstad O., Sandvig K., and Berg K. Photochemical internalisation increases the cytotoxic effect of the immunotoxin MOC31-gelonin. Int. J. Cancer 87 (2000) 853-859
47. Baselga J. The EGFR as a target for anticancer therapy - focus on cetuximab. Eur. J. Cancer 37 Suppl. 4 (2001) S16-S22
48. Castillo L., Etienne-Grimaldi M.C., Fischel J.L., Formento P., Magne N., and Milano G. Pharmacological background of EGFR targeting. Ann. Oncol. 15 (2004) 1007-1012
49. Weyergang A., Selbo P.K., and Berg K. Photochemically stimulated drug delivery increases the cytotoxicity and specificity of EGF-saporin. J. Control Release 111 (2006) 165-173
50. Yip W.L., Weyergang A., Berg K., Tonnesen H.H., and Selbo P.K. Targeted delivery and enhanced cytotoxicity of cetuximab-saporin by photochemical internalization in EGFR-positive cancer cells. Mol. Pharm. 4 (2007) 241-251
51. Hogset A., Prasmickaite L., Selbo P.K., Hellum M., Engesaeter B.O., Bonsted A., and Berg K. Photochemical internalisation in drug and gene delivery. Adv. Drug Deliv. Rev. 56 (2004) 95-115
52. Somia N., and Verma I.M. Gene therapy: trials and tribulations. Nat. Rev. Genet. 1 (2000) 91-99
53. Prasmickaite L., Hogset A., Olsen V.M., Kaalhus O., Mikalsen S.O., and Berg K. Photochemically enhanced gene transfection increases the cytotoxicity of the herpes simplex virus thymidine kinase gene combined with ganciclovir. Cancer Gene Ther. 11 (2004) 514-523
54. Oliveira S., Fretz M.M., Hogset A., Storm G., and Schiffelers R.M. Photochemical internalization enhances silencing of epidermal growth factor receptor through improved endosomal escape of siRNA. Biochim. Biophys. Acta. 1768 (2007) 1211-1217
55. Folini M., Berg K., Millo E., Villa R., Prasmickaite L., Daidone M.G., Benatti U., and Zaffaroni N. Photochemical internalization of a peptide nucleic acid targeting the catalytic subunit of human telomerase. Cancer Res. 63 (2003) 3490-3494
56. Bonsted A., Wagner E., Prasmickaite L., Hogset A., and Berg K. Photochemical enhancement of DNA delivery by EGF receptor targeted polyplexes. Methods Mol. Biol. 434 (2008) 171-181
57. Pron G., Mahrour N., Orlowski S., Tounekti O., Poddevin B., Belehradek Jr. J., and Mir L.M. Internalisation of the bleomycin molecules responsible for bleomycin toxicity: a receptor-mediated endocytosis mechanism. Biochem. Pharmacol. 57 (1999) 45-56
58. Berg K., Dietze A., Kaalhus O., and Hogset A. Site-specific drug delivery by photochemical internalization enhances the antitumor effect of bleomycin. Clin. Cancer Res. 11 (2005) 8476-8485
59. Lou P.J., Lai P.S., Shieh M.J., MacRobert A.J., Berg K., and Bown S.G. Reversal of doxorubicin resistance in breast cancer cells by photochemical internalization. Int. J. Cancer 119 (2006) 2692-2698
60. Cabral H., Nakanishi M., Kumagai M., Jang W.D., Nishiyama N., and Kataoka K. A photo-activated targeting chemotherapy using glutathione sensitive camptothecin-loaded polymeric micelles. Pharm. Res. (2008)
61. Shieh M.J., Peng C.L., Lou P.J., Chiu C.H., Tsai T.Y., Hsu C.Y., Yeh C.Y., and Lai P.S. Non-toxic phototriggered gene transfection by PAMAM-porphyrin conjugates. J. Control Release 129 (2008) 200-206
62. Ndoye A., Dolivet G., Hogset A., Leroux A., Fifre A., Erbacher P., Berg K., Behr J.P., Guillemin F., and Merlin J.L. Eradication of p53-mutated head and neck squamous cell carcinoma xenografts using nonviral p53 gene therapy and photochemical internalization. Mol. Ther. 13 (2006) 1156-1162
63. Dietze A., Selbo P.K., Prasmickaite L., Weyergang A., Bonsted A., Engesaeter B., Hogset A., and Berg K. Photochemical internalization (PCI): a new modality for light activation of endocytosed therapeuticals. J. Environ. Pathol. Toxicol. Oncol. 25 (2006) 521-536
64. Chen B., Crane C., He C., Gondek D., Agharkar P., Savellano M.D., Hoopes P.J., and Pogue B.W. Disparity between prostate tumor interior versus peripheral vasculature in response to verteporfin-mediated vascular-targeting therapy. Int. J. Cancer 123 (2008) 695-701
65. Graschew G., and Shopova M. Photodynamic therapy and gamma-irradiation of tumors: effect on tumor-cell reoxygenation. Lasers Med. Sci. 1 (1986) 193-195
66. Kostron H., Swartz M.R., Miller D.C., and Martuza R.L. The interaction of hematoporphyrin derivative, light, and ionizing radiation in a rat glioma model. Cancer 57 (1986) 964-970
67. Luksiene Z., Kalvelyte A., and Supino R. On the combination of photodynamic therapy with ionizing radiation. J. Photochem. Photobiol. B. 52 (1999) 35-42
68. Allman R., Cowburn P., and Mason M. Effect of photodynamic therapy in combination with ionizing radiation on human squamous cell carcinoma cell lines of the head and neck. Brit. J. Cancer 83 (2000) 655-661
69. Berg K., Luksiene Z., Moan J., and Ma L. Combined treatment of ionizing radiation and photosensitization by 5-aminolevulinic acid-induced protoporphyrin IX. Radiat. Res. 142 (1995) 340-346
70. Madsen S.J., Sun C.H., Tromberg B.J., Yeh A.T., Sanchez R., and Hirschberg H. Effects of combined photodynamic therapy and ionizing radiation on human glioma spheroids. Photochem. Photobiol. 76 (2002) 411-416
71. Molin J., Sogaard P.E., and Overgaard J. Experimental studies on the radiation-modifying effect of bleomycin in malignant and normal mouse tissue in vivo. Cancer Treat. Rep. 65 (1981) 583-589
72. Lelieveld P., Scoles M.A., Brown J.M., and Kallman R.F. The effect of treatment in fractionated schedules with the combination of X-irradiation and six cytotoxic drugs on the RIF-1 tumor and normal mouse skin. Int. J. Radiat. Oncol. Biol. Phys. 11 (1985) 111-121
73. Fu K.K., Phillips T.L., Silverberg I.J., Jacobs C., Goffinet D.R., Chun C., Friedman M.A., Kohler M., McWhirter K., and Carter S.K. Combined radiotherapy and chemotherapy with bleomycin and methotrexate for advanced inoperable head and neck cancer: update of a Northern California Oncology Group randomized trial. J. Clin. Oncol. 5 (1987) 1410-1418
74. Vermund H., Kaalhus O., Winther F., Trausjo J., Thorud E., and Harang R. Bleomycin and radiation therapy in squamous cell carcinoma of the upper aero-digestive tract: a phase III clinical trial. Int. J. Radiat. Oncol. Biol. Phys. 11 (1985) 1877-1886
75. Ng C.S., Lee T.W., Wan S., Wan I.Y., Sihoe A.D., Arifi A.A., and Yim A.P. Thoracotomy is associated with significantly more profound suppression in lymphocytes and natural killer cells than video-assisted thoracic surgery following major lung resections for cancer. J. Invest Surg. 18 (2005) 81-88
76. Korbelik M. PDT-associated host response and its role in the therapy outcome. Lasers Surg. Med. 38 (2006) 500-508
77. bdel-Hady E.S., Martin-Hirsch P., Duggan-Keen M., Stern P.L., Moore J.V., Corbitt G., Kitchener H.C., and Hampson I.N. Immunological and viral factors associated with the response of vulval intraepithelial neoplasia to photodynamic therapy. Cancer Res. 61 (2001) 192-196
78. Yanai H., Kuroiwa Y., Shimizu N., Matsubara Y., Okamoto T., Hirano A., Nakamura Y., Okita K., and Sekine T. The pilot experience of immunotherapy-combined photodynamic therapy for advanced gastric cancer in elderly patients. Int. J. Gastrointest. Cancer 32 (2002) 139-142
79. Henderson B.W., Gollnick S.O., Snyder J.W., Busch T.M., Kousis P.C., Cheney R.T., and Morgan J. Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors. Cancer Res. 64 (2004) 2120-2126
80. Gollnick S.O., Vaughan L., and Henderson B.W. Generation of effective antitumor vaccines using photodynamic therapy. Cancer Res. 62 (2002) 1604-1608
81. Korbelik M., Krosl G., Krosl J., and Dougherty G.J. The role of host lymphoid populations in the response of mouse EMT6 tumor to photodynamic therapy. Cancer Res. 56 (1996) 5647-5652
82. Canti G., Lattuada D., Nicolin A., Taroni P., Valentini G., and Cubeddu R. Antitumor immunity induced by photodynamic therapy with aluminum disulfonated phthalocyanines and laser light. Anticancer Drugs 5 (1994) 443-447