Developing strategies to predict photodynamic therapy outcome: the role of melanoma microenvironment

Tumor Biology

Volumn 36, Issue 12, 2015, Pages 9127-9136

  Vera, Renzo Emanuel ^a   Lamberti, María Julia ^a   Rivarola, Viviana Alicia ^a   Rumie Vittar, Natalia Belén ^a  

^a DEPARTAMENTO DE QUÍMICA   (Argentina)

Author keywords

Melanoma; Monolayer; Photodynamic therapy; Spheroids; Tumor microenvironment

Indexed keywords

AMINOLEVULINIC ACID; BACTERIOCHLOROPHYLL SERINE; CHLORIN E6; HEMATOPORPHYRIN DERIVATIVE; IMIQUIMOD; INDOCYANINE GREEN; INTERFERON; INTERLEUKIN 2; IPILIMUMAB; METHYLAMINOLEVULINIC ACID; METHYLENE BLUE; PHOTOSAN III; PHOTOSENSITIZING AGENT; REACTIVE OXYGEN METABOLITE; TETRAKIS(4 CARBORANYLTHIOTETRAFLUOROPHENYL)CHLORIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

CANCER RESISTANCE; COCULTURE; CUTANEOUS MELANOMA; DIODE LASER; HUMAN; KERATINOCYTE; MELANOMA CELL; METASTATIC MELANOMA; NEUTRON CAPTURE THERAPY; NONHUMAN; OXIDATIVE STRESS; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; RED LIGHT; REVIEW; TUMOR MICROENVIRONMENT; TUMOR MODEL; TUMOR RECURRENCE; TUMOR REGRESSION; TUMOR SPHEROID; APOPTOSIS; DRUG EFFECTS; GENETICS; MELANOMA; METABOLISM; MULTICELLULAR SPHEROID; PATHOLOGY; PHOTOCHEMOTHERAPY; RADIATION RESPONSE; TREATMENT OUTCOME;

APOPTOSIS; HUMANS; MELANOMA; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; REACTIVE OXYGEN SPECIES; SPHEROIDS, CELLULAR; TREATMENT OUTCOME; TUMOR MICROENVIRONMENT;

EID: 84952870679     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-015-4059-x     Document Type: Review

References (74)

1. Lo J, Fisher D. The melanoma revolution: from UV carcinogenesis to a new era in therapeutic. Science. 2014;346:945–9.
2. Chang C, Murzaku E, Penn L, Abbasi N, Davis P, Berwick M, et al. More skin, more sun, more tan, more melanoma. Am J Public Health. 2014;104:e92–9.
3. Diao D, Lee T. Sun-protective behaviors in populations at high risk for skin cancer. Psychol Res Behav Manag. 2014;7:9–18.
4. De Giorgi V, Sestini S, Massi D, Lotti T. Melanocytic aggregation in the skin: diagnostic clues from lentigines to melanoma. Dermatol Clin. 2007;25:303–20. vii – viii.
5. Bastian B. The molecular pathology of melanoma: an integrated taxonomy of melanocytic, neoplasia. Annu Rev Pathol. 2014;9:239–71.
6. Miller AJ, Mihm MC. Mechanisms of disease Melanoma. N Engl J Med. 2006;51–65.
7. Markovic SN, Erickson LA, Rao RD, Weenig RH, Pockaj BA, Bardia A, et al. Malignant melanoma in the 21st century, part 2: staging, prognosis, and treatment. Mayo Clin Proc. 2007;82:490–513.
8. Markovic SN, Erickson LA, Rao RD, Weenig RH, Pockaj BA, Bardia A, et al. Malignant melanoma in the 21st century, part 1: epidemiology, risk factors, screening, prevention, and diagnosis. Mayo Clin Proc. 2007;82:364–80.
9. Curtin JA, Fridlyand J, Kageshita T, Patel HN, Busam KJ, Kutzner H, et al. Distinct sets of genetic alterations in melanoma. N Engl J Med. 2005;353:2135–47.
10. Dar AA, Majid S, De Semir D, Nosrati M, Bezrookove V, Kashani-Sabet M. miRNA-205 suppresses melanoma cell proliferation and induces senescence via regulation of E2F1 protein. J Biol Chem. 2011;286:16606–14.
11. Van den Hurk K, Niessen HEC, Veeck J, van den Oord JJ, van Steensel MAM, Zur Hausen A, et al. Genetics and epigenetics of cutaneous malignant melanoma: a concert out of tune. Biochim Biophys Acta. 1826;2012:89–102.
12. Lee JT, Herlyn M. Microenvironmental influences in melanoma progression. J Cell Biochem. 2007;101:862–72.
13. Bhatia S, Tykodi S, Thompson J. Treatment of metastatic melanoma: an overview. Oncol (willist Park). 2009;23:488–96.
14. Agostinis P, Berg K, Cengel K, Foster T, Girotti A, Gollnick S, et al. Photodynamic therapy of cancer: an update. CA Cancer J Clin. 2011;61:250–81.
15. Morton C, Szeimies R, Sidoroff A, Braathen L. European guidelines for topical photodynamic therapy part 1: treatment delivery and current indications - actinic keratoses, Bowen’s disease, basal cell carcinoma. J Eur Acad Dermatol Venereol. 2013;27:536–44.
16. Dougherty T, Kaufman J, Goldfarb A, Weishaupt K, Boyle D, Mittleman A. Photoradiation therapy for the treatment of malignant tumors. Cancer Res. 1978;38:2628–35.
17. Sheleg S, Zhavrid E, Khodina T, Kochubeev G, Istomin Y, Chalov V, et al. Photodynamic therapy with chlorin e(6) for skin metastases of melanoma. Photodermatol Photoimmunol Photomed. 2004;20:21–6.
18. Chetty N, Osborne V, Harland C. Amelanotic melanoma in situ: lack of sustained response to photodynamic therapy. Clin Exp Dermatol. 2008;33:204–6.
19. Koderhold G, Jindra R, Koren H, Alth G, Schenk G. Experiences of photodynamic therapy in dermatology. J Photochem Photobiol B. 1996;36:221–3.
20. Nelson J, McCullough J, Berns M. Photodynamic therapy of human malignant melanoma xenografts in athymic nude mice. J Natl Cancer Inst. 1988;80:56–60.
21. Young A. Chromophores in human skin. Phys Med Biol. 1997;42:789–802.
22. Witz IP. The tumor microenvironment: the making of a paradigm. Cancer Microenviron. 2009;2:9–17.
23. Li X, Naylor M, Le H, Nordquist R, Teague T, Howard C, et al. Clinical effects of in situ photoimmunotherapy on late-stage melanoma patients: a preliminary study. Cancer Biol Ther. 2010;10:1081–7.
24. Naylor M, Chen W, Teague T, Perry L, Nordquist R. In situ photoimmunotherapy: a tumour-directed treatment for melanoma. Br J Dermatol. 2006;155:1287–92.
25. Paiva M, Joo J, Abrahao M, Ribeiro J, Cervantes O, Sercarz J. Update on laser photochemotherapy: an alternative for cancer treatment. Anticancer Agents Med Chem. 2011;11:772–9.
26. Huang Y, Vecchio D, Avci P, Yin R, Garcia-diaz M, Hamblin MR. Melanoma resistance to photodynamic therapy: new insights. Biol Chem. 2014;394:239–50.
27. Duc GHT, editor. Melanomas | From Early Detection to Treatment. InTech; 2013.
28. Maduray K, Karsten A, Odhav B, Nyokong T. In vitro toxicity testing of zinc tetrasulfophthalocyanines in fibroblast and keratinocyte cells for the treatment of melanoma cancer by photodynamic therapy. J Photochem Photobiol B Biol. 2011;103:98–104.
29. Krestyn E, Kolarova H, Bajgar R, Tomankova K. Photodynamic properties of ZnTPPS4, ClAlPcS2 and ALA in human melanoma G361 cells. Toxicol InVitro. 2010;24:286–91.
30. Kolarova H, Tomankova K, Bajgar R, Kolar P, Kubinek R. Photodynamic and sonodynamic treatment by phthalocyanine on cancer cell lines. Ultrasound Med Biol. 2009;35:1397–404.
31. Karmakova T, Feofanov A, Nazarova A, Grichine A, Yakubovskaya R, Luk’yanets E, et al. Distribution of metal-free sulfonated phthalocyanine in subcutaneously transplanted murine tumors. J Photochem Photobiol B Biol. 2004;75:81–7.
32. Barge J, Decréau R, Julliard M, Hubaud JC, Sabatier AS, Grob JJ, et al. Killing efficacy of a new silicon phthalocyanine in human melanoma cells treated with photodynamic therapy by early activation of mitochondrion-mediated apoptosis. Exp Dermatol. 2004;13:33–44.
33. Sparsa A, Bellaton S, Naves T, Jauberteau M, Bonnetblanc J, Sol V, et al. Photodynamic treatment induces cell death by apoptosis or autophagy depending on the melanin content in two B16 melanoma cell lines. Oncol Rep. 2013;29:1196–200.
34. Breusing N, Grimm S, Mvondo D, Flaccus A, Biesalski HK, Grune T. Light-induced cytotoxicity after aminolevulinic acid treatment is mediated by heme and not by iron. J Photochem Photobiol B Biol. 2010;99:36–43.
35. Ickowicz Schwartz D, Gozlan Y, Greenbaum L, Babushkina T, Katcoff DJ, Malik Z. Differentiationdependent photodynamic therapy regulated by porphobilinogen deaminase in B16 melanoma. Br J Cancer. 2004;90:1833–41.
36. Da̧browski JM, Pereira MM, Arnaut LG, Monteiro CJP, Peixoto AF, Karocki A, et al. Synthesis, photophysical studies and anticancer activity of a new halogenated water-soluble porphyrin. Photochem Photobiol. 2007;83:897–903.
37. Nowak-Sliwinska P, Karocki A, Elas M, Pawlak A, Stochel G, Urbanska K. Verteporfin, photofrin II, and merocyanine 540 as PDT photosensitizers against melanoma cells. Biochem Biophys Res Commun. 2006;349:549–55.
38. Kolarova H, Macecek J, Nevrelova P, Huf M, Tomecka M, Bajgar R, et al. Photodynamic therapy with zinc-tetra(p-sulfophenyl)porphyrin bound to cyclodextrin induces single strand breaks of cellular DNA in G361 melanoma cells. Toxicol In Vitro. 2005;19:971–4.
39. Szurko A, Krämer-Marek G, Wideł M, Ratuszna A, Habdas J, Kuś P. Photodynamic effects of two water soluble porphyrins evaluated on human malignant melanoma cells in vitro. Acta Biochim Pol. 2003;50:1165–74.
40. Ježek P, Nekvasil M, Škobisová E, Urbánková E, Jirsa M, Zadinová M, et al. Experimental photodynamic therapy with meso-tetrakisphenylporphyrin (TPP) in liposomes leads to disintegration of human amelanotic melanoma implanted to nude mice. Int J Cancer. 2003;103:693–702.
41. Chang C, Yu J, Wei F. In vitro and in vivo photosensitizing applications of Photofrin® in malignant melanoma cells. Chang Gung Med J. 2007;31:260–7.
42. Kleemann B, Loos B, Lang D, Scriba T, Davids L. St John’s Wort (Hypericum perforatum L.) photomedicine: hypericin-photodynamic therapy induces metastatic melanoma cell death. PLoS ONE. 2014;9(7), e103762.
43. Mazor O, Brandis A, Plaks V, Neumark E, Rosenbach-Belkin V, Salomon Y, et al. WST11, a novel watersoluble bacteriochlorophyll derivative; cellular uptake, pharmacokinetics, biodistribution and vasculartargeted photodynamic activity using melanoma tumors as a model. Photochem Photobiol. 2005;81:342–51.
44. Nagata S, Obana A, Gohto Y, Nakajima S. Necrotic and apoptotic cell death of human malignant melanoma cells following photodynamic therapy using an amphiphilic photosensitizer, ATX-S10(Na). Lasers Surg Med. 2003;33:64–70.
45. Ropp S, Guy J, Berl V, Bischoff P, Lepoittevin J-P. Synthesis and photocytotoxic activity of new α-methylene-γ-butyrolactone-psoralen heterodimers. Bioorg Med Chem. 2004;12:3619–25.
46. Donnelly R, McCarron P, Woolfson A. Derivatives of 5-aminolevulinic Acid for photodynamic therapy. Perspect Med Chem. 2008;1:49–63.
47. Haddad R, Kaplan O, Greenberg R, Siegal A, Skornick Y, Kashtan H. Photodynamic therapy of murine colon cancer and melanoma using systemic aminolevulinic acid as a photosensitizer. Int J Surg Investig. 2000;2:171–8.
48. Robertson CA, Abrahamse H, Evans D. The in vitro PDT efficacy of a novel metallophthalocyanine (MPc) derivative and established 5-ALA photosensitizing dyes against human metastatic melanoma cells. Lasers Surg Med. 2010;42:766–76.
49. Lr B, Weissenberger J, Vallan C, Kato M. Bern C-. 5-aminolaevulinic acid photodynamic therapy in a transgenic mouse model of skin melanoma. Exp Dermatol. 2005;14:429–37.
50. Chen Y, Zheng W, Li Y, Zhong J, Ji J, Shen P. Apoptosis induced by methylene-blue-mediated photodynamic therapy in melanomas and the involvement of mitochondrial dysfunction revealed by proteomics. Cancer Sci. 2008;99:2019–27.
51. Wagner M, Suarez ER, Theodoro TR, Machado Filho CDAS, Gama MFM, Tardivo JP, et al. Methylene blue photodynamic therapy in malignant melanoma decreases expression of proliferating cell nuclear antigen and heparanases. Clin Exp Dermatol. 2012;37:527–33.
52. Rapozzi V, Zorzet S, Zacchigna M, Della Pietra E, Cogoi S, Xodo LE. Anticancer activity of cationic porphyrins in melanoma tumour-bearing mice and mechanistic in vitro studies. Mol Cancer. 2014;13:75.
53. Hao E, Friso E, Miotto G, Jori G, Soncin M, Fabris C, et al. Synthesis and biological investigations of tetrakis(p-carboranylthio-tetrafluorophenyl)chlorin (TPFC). Org Biomol Chem. 2008;6:3732–40.
54. Chen L, Fiedorl L, Pavlofsky F, Brumfeldl V, Salomon Y, Scherz A. Serine conjugates of chlorophyll and bacteriochlorophyll: photocytotoxicity in witro and tissue distribution in mice bearing melanoma tumors. Photochem Photobiol. 1996;64:174–81.
55. Zilbersteins J, Bromberg A, Frantz A, Rosenbach-belkin V, Kritzmann A. Light-dependent oxygen consumption in bacteriochlorophyll-serine-treated melanoma tumors: on-line determination using a tissue-inserted oxygen microsensor. Photochem Photobiol. 1997;65:1012–9.
56. Toledo F, Wahl G. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer. 2006;6:909–23.
57. Beaumont K, Mohana-Kumaran N, Haass N. Modeling melanoma in vitro and in vivo. Healthcare. 2013;2:27–46.
58. Fabris C, Vicente MGH, Hao E, Friso E, Borsetto L, Jori G, et al. Tumour-localizing and -photosensitising properties of meso-tetra(4-nido-carboranylphenyl)porphyrin (H2TCP). J Photochem Photobiol B Biol. 2007;89:131–8.
59. Tsai T, Ji H, Chiang P, Chou R, Chang W, Chen C. ALA-PDT results in phenotypic changes and decreased cellular invasion in surviving cancer cells. Lasers Surg Med. 2009;41:305–15.
60. Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA. Spheroid-based drug screen: considerations and practical approach. Nat Protoc. 2009;4:309–24.
61. Fennema E, Rivron N, Rouwkema J, van Blitterswijk C, de Boer J. Spheroid culture as a tool for creating 3D complex tissues. Trends Biotechnol. 2013;31:108–15.
62. Rofstad E, Wahl A, Brustad T. Radiation response of multicellular spheroids initiated from five human melanoma xenograft lines. Relationship to the radioresponsiveness in vivo. Br J Radiol. 1986;59:1023–9.
63. Kastl A, Dieckmann S, Wähler K, Völker T, Kastl L, Merkel A, et al. Rhenium complexes with visible-lightinduced anticancer activity. ChemMedChem. 2013;8:924–7.
64. Barbugli P a., Alves CP, Espreafico EM, Tedesco AC. Photodynamic therapy utilizing liposomal ClAlPc in human melanoma 3D cell cultures. Exp Dermatol. 2015;70:n/a – n/a.
65. Ungefroren H, Sebens S, Seidl D, Lehnert H, Hass R. Interaction of tumor cells with the microenvironment. Cell Commun Signal. 2011;9:18.
66. Ruiter D, Bogenrieder T, Elder D, Herlyn M. Melanoma-stroma interactions: structural and functional aspects. Lancet Oncol. 2002;3:35–43.
67. Labrousse A, Ntayi C, Hornebeck W, Bernard P. Stromal reaction in cutaneous melanoma. Crit Rev Oncol Hematol. 2004;49:269–75.
68. Villanueva J, Herlyn M. Melanoma and the tumor microenvironment. Curr Oncol Rep. 2008;10:439–46.
69. Hsu M, Meier F, Herlyn M. Melanoma development and progression: a conspiracy between tumor and host. Differentiation. 2002;70:522–36.
70. Rumie Vittar N, Lamberti M, Pansa M, Vera R, Rodriguez M, Cogno I, et al. Ecological photodynamic therapy: new trend to disrupt the intricate networks within tumor ecosystem. Biochim Biophys Acta. 1835;2013:86–9.
71. Haass N, Smalley K, Li L, Herlyn M. Adhesion, migration and communication in melanocytes and melanoma. Pigment Cell Res. 2005;18:150–9.
72. Kästle M, Grimm S, Nagel R, Breusing N, Grune T. Combination of PDT and inhibitor treatment affects melanoma cells and spares keratinocytes. Free Radic Biol Med. 2011;50:305–12.
73. Berking C, Herlyn M. Human skin reconstruct models: a new application for studies of melanocyte and melanoma biology. Histol Histopathol. 2001;16:669–74.
74. Vörsmann H, Groeber F, Walles H, Busch S, Beissert S, Walczak H, et al. Development of a human three-dimensional organotypic skin-melanoma spheroid model for in vitro drug testing. Cell Death Dis. 2013;4, e719.