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

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• 作者：Renzo Emanuel Vera ; María Julia Lamberti ; Viviana Alicia Rivarola…
• 关键词：Melanoma ; Photodynamic therapy ; Tumor microenvironment ; Monolayer ; Spheroids
• 刊名：Tumor Biology
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：36
• 期：12
• 页码：9127-9136
• 全文大小：839 KB
• 参考文献：1.Lo J, Fisher D. The melanoma revolution: from UV carcinogenesis to a new era in therapeutic. Science. 2014;346:945–9.PubMed CrossRef
  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.PubMed PubMedCentral CrossRef
  3.Diao D, Lee T. Sun-protective behaviors in populations at high risk for skin cancer. Psychol Res Behav Manag. 2014;7:9–18.PubMedCentral
  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.PubMed CrossRef
  5.Bastian B. The molecular pathology of melanoma: an integrated taxonomy of melanocytic, neoplasia. Annu Rev Pathol. 2014;9:239–71.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed PubMedCentral CrossRef
  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.PubMed CrossRef
  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.PubMed PubMedCentral CrossRef
  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.PubMed CrossRef
  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.PubMed
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  21.Young A. Chromophores in human skin. Phys Med Biol. 1997;42:789–802.PubMed CrossRef
  22.Witz IP. The tumor microenvironment: the making of a paradigm. Cancer Microenviron. 2009;2:9–17.PubMed PubMedCentral CrossRef
  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.PubMed PubMedCentral CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.CrossRef
  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.CrossRef
  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.PubMed CrossRef
  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.CrossRef
  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.PubMed CrossRef
  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.PubMed
  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.CrossRef
  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.PubMed PubMedCentral
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed
  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.PubMed CrossRef
  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.PubMed PubMedCentral CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed
  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.PubMed CrossRef
  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.CrossRef
  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.PubMed
  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.PubMed CrossRef
  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.PubMed PubMedCentral CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.CrossRef
  56.Toledo F, Wahl G. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer. 2006;6:909–23.PubMed CrossRef
  57.Beaumont K, Mohana-Kumaran N, Haass N. Modeling melanoma in vitro and in vivo. Healthcare. 2013;2:27–46.CrossRef
  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.CrossRef
  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.PubMed CrossRef
  60.Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA. Spheroid-based drug screen: considerations and practical approach. Nat Protoc. 2009;4:309–24.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed PubMedCentral CrossRef
  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.PubMed PubMedCentral CrossRef
  66.Ruiter D, Bogenrieder T, Elder D, Herlyn M. Melanoma-stroma interactions: structural and functional aspects. Lancet Oncol. 2002;3:35–43.PubMed CrossRef
  67.Labrousse A, Ntayi C, Hornebeck W, Bernard P. Stromal reaction in cutaneous melanoma. Crit Rev Oncol Hematol. 2004;49:269–75.PubMed CrossRef
  68.Villanueva J, Herlyn M. Melanoma and the tumor microenvironment. Curr Oncol Rep. 2008;10:439–46.PubMed CrossRef
  69.Hsu M, Meier F, Herlyn M. Melanoma development and progression: a conspiracy between tumor and host. Differentiation. 2002;70:522–36.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed CrossRef
  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.PubMed
  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.PubMed PubMedCentral CrossRef
  
• 作者单位：Renzo Emanuel Vera (1)
  María Julia Lamberti (1)
  Viviana Alicia Rivarola (1)
  Natalia Belén Rumie Vittar (1)
  
  1. Biología Molecular, Universidad Nacional de Río Cuarto, Ruta 36 Km 601, Río Cuarto, 5800, Córdoba, Argentina
  
• 刊物主题：Cancer Research;
• 出版者：Springer Netherlands
• ISSN：1423-0380

文摘

Melanoma is among the most aggressive and treatment-resistant human skin cancer. Photodynamic therapy (PDT), a minimally invasive therapeutic modality, is a promising approach to treating melanoma. It combines a non-toxic photoactivatable drug called photosensitizer with harmless visible light to generate reactive oxygen species which mediate the antitumor effects. The aim of this review was to compile the available data about PDT on melanoma. Our comparative analysis revealed a disconnection between several hypotheses generated by in vitro therapeutic studies and in vivo and clinical assays. This fact led us to highlight new preclinical experimental platforms that mimic the complexity of tumor biology. The tumor and its stromal microenvironment have a dynamic and reciprocal interaction that plays a critical role in tumor resistance, and these interactions can be exploited for novel therapeutic targets. In this sense, we review two strategies used by photodynamic researchers: (a) developing 3D culture systems which mimic tumor architecture and (b) heterotypic cultures that resemble tumor microenvironment to favor therapeutic regimen design. After this comprehensive review of the literature, we suggest that new complementary preclinical models are required to better optimize the clinical outcome of PDT on skin melanoma. Keywords Melanoma Photodynamic therapy Tumor microenvironment Monolayer Spheroids