Role of TGF-β in melanoma

Current Pharmaceutical Biotechnology

Volumn 12, Issue 12, 2011, Pages 2165-2175

  Busse, A ^a   Keilholz, U ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Angiogenesis; Growth resistance; Immunosuppression; Invasion; Melanoma; Metastasis; References; TGF

Indexed keywords

2 (5 CHLORO 2 FLUOROPHENYL) 4 (4 PYRIDINYLAMINO)PTERIDINE; 4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; CD11B ANTIGEN; ENDOGLIN; FRESOLIMUMAB; INTERLEUKIN 8; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOPONTIN; SMAD PROTEIN; STAT4 PROTEIN; TRABEDERSEN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3;

ANGIOGENESIS; ARTICLE; CANCER GROWTH; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER INVASION; CANCER SURVIVAL; CELL DIFFERENTIATION; CELL INVASION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; DRUG TARGETING; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; HUMAN; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; INTRACELLULAR SIGNALING; MELANOCYTE; MELANOMA; METASTASIS; NONHUMAN; PLEIOTROPY; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

ANIMALS; HUMANS; IMMUNOSUPPRESSION; MELANOMA; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; SKIN NEOPLASMS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84855242402     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920111798808437     Document Type: Article

References (137)

1. Javelaud, D.; Mauviel, A. Mammalian transforming growth factorbetas: Smad signaling and physio-pathological roles. Int. J. Biochem. Cell Biol., 2004, 36(7), 1161-1165.
2. Kaminska, B.; Wesolowska, A.; Danilkiewicz, M. TGF beta signalling and its role in tumour pathogenesis. Acta Biochim. Pol., 2005, 52(2), 329-337.
3. Elliott, R. L.; Blobe, G. C. Role of transforming growth factor Beta in human cancer. J. Clin. Oncol., 2005, 23(9), 2078-2093.
4. Wakefield, L. M.; Roberts, A. B. TGF-beta signaling: positive and negative effects on tumorigenesis. Curr. Opin. Genet. Dev., 2002, 12(1), 22-29.
5. Massague, J.; Gomis, R. R. The logic of TGFbeta signaling. FEBS Lett., 2006, 580(12), 2811-2820.
6. Leivonen, S. K.; Kahari, V. M. Transforming growth factor-beta signaling in cancer invasion and metastasis. Int. J. Cancer, 2007, 121(10), 2119-2124.
7. Wan, Y. Y.; Flavell, R. A. 'Yin-Yang' functions of transforming growth factor-beta and T regulatory cells in immune regulation. Immunol. Rev., 2007, 220, 199-213.
8. Jemal, A.; Siegel, R.; Xu, J.; Ward, E. Cancer Statistics. CA Cancer J Clin., 2010, 60, 277-300
9. Erickson, C.; Driscoll, M. S. Melanoma epidemic: Facts and controversies. Clin. Dermatol., 28(3), 281-286.
10. Balch, C. M.; Buzaid, A. C.; Soong, S. J.; Atkins, M. B.; Cascinelli, N.; Coit, D. G.; Fleming, I. D.; Gershenwald, J. E.; Houghton, A. Jr.; Kirkwood, J. M.; McMasters, K. M.; Mihm, M. F.; Morton, D. L.; Reintgen, D. S.; Ross, M. I.; Sober, A.; Thompson, J. A.; Thompson, J. F. Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J. Clin. Oncol., 2001, 19(16), 3635-3648.
11. Krasagakis, K.; Garbe, C.; Schrier, P. I.; Orfanos, C. E. Paracrine and autocrine regulation of human melanocyte and melanoma cell growth by transforming growth factor beta in vitro. Anticancer Res., 1994, 14(6B), 2565-2571.
12. Rodeck, U.; Bossler, A.; Graeven, U.; Fox, F. E.; Nowell, P. C.; Knabbe, C.; Kari, C. Transforming growth factor beta production and responsiveness in normal human melanocytes and melanoma cells. Cancer Res., 1994, 54(2), 575-581.
13. Moretti, S.; Pinzi, C.; Berti, E.; Spallanzani, A.; Chiarugi, A.; Boddi, V.; Reali, U. M.; Giannotti, B. rIn situ expression of transforming growth factor beta is associated with melanoma progression and correlates with Ki67, HLA-DR and beta 3 integrin expression. Melanoma Res., 1997, 7(4), 313-321.
14. Van Belle, P.; Rodeck, U.; Nuamah, I.; Halpern, A. C.; Elder, D. E. Melanoma-associated expression of transforming growth factorbeta isoforms. Am. J. Pathol., 1996, 148(6), 1887-1894.
15. Luscher, U.; Filgueira, L.; Juretic, A.; Zuber, M.; Luscher, N. J.; Heberer, M.; Spagnoli, G. C. The pattern of cytokine gene expression in freshly excised human metastatic melanoma suggests a state of reversible anergy of tumor-infiltrating lymphocytes. Int. J. Cancer, 1994, 57(4), 612-619.
16. Reed, J. A.; McNutt, N. S.; Prieto, V. G.; Albino, A. P. Expression of transforming growth factor-beta 2 in malignant melanoma correlates with the depth of tumor invasion. Implications for tumor progression. Am. J. Pathol., 1994, 145(1), 97-104.
17. Schmid, P.; Itin, P.; Rufli, T. In situ analysis of transforming growth factor-beta s (TGF-beta 1, TGF-beta 2, TGF-beta 3), and TGF-beta type II receptor expression in malignant melanoma. Carcinogenesis, 1995, 16(7), 1499-1503.
18. Rodeck, U.; Melber, K.; Kath, R.; Menssen, H. D.; Varello, M.; Atkinson, B.; Herlyn, M. Constitutive expression of multiple growth factor genes by melanoma cells but not normal melanocytes. J. Invest. Dermatol., 1991, 97(1), 20-26.
19. Albino, A. P.; Davis, B. M.; Nanus, D. M. Induction of growth factor RNA expression in human malignant melanoma: markers of transformation. Cancer Res., 1991, 51(18), 4815-4820.
20. Krasagakis, K.; Tholke, D.; Farthmann, B.; Eberle, J.; Mansmann, U.; Orfanos, C. E. Elevated plasma levels of transforming growth factor (TGF)-beta1 and TGF-beta2 in patients with disseminated malignant melanoma. Br. J. Cancer, 1998, 77(9), 1492-1494.
21. Tas, F.; Duranyildiz, D.; Oguz, H.; Camlica, H.; Yasasever, V.; Topuz, E. Circulating serum levels of angiogenic factors and vascular endothelial growth factor receptors 1 and 2 in melanoma patients. Melanoma Res., 2006, 16(5), 405-411.
22. Moretti, S.; Pinzi, C.; Berti, E.; Spallanzani, A.; Chiarugi, A.; Boddi, V.; Reali, U. M.; Giannotti, B. In situ expression of transforming growth factor beta is associated with melanoma progression and correlates with Ki67, HLA-DR and beta 3 integrin expression. Melanoma Res., 1997, 7(4), 313-321.
23. Altomonte, M.; Montagner, R.; Fonsatti, E.; Colizzi, F.; Cattarossi, I.; Brasoveanu, L. I.; Nicotra, M. R.; Cattelan, A.; Natali, P. G.; Maio, M. Expression and structural features of endoglin (CD105), a transforming growth factor beta1 and beta3 binding protein, in human melanoma. Br. J. Cancer, 1996, 74(10), 1586-1591.
24. Shi, Y.; Massague, J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell, 2003, 113(6), 685-700.
25. Massague, J.; Chen, Y. G. Controlling TGF-beta signaling. Genes Dev., 2000, 14(6), 627-644.
26. Massague, J.; Wotton, D. Transcriptional control by the TGFbeta/ Smad signaling system. Embo. J., 2000, 19(8), 1745-1754.
27. Derynck, R.; Zhang, Y. E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature, 2003, 425(6958), 577-584.
28. Medrano, E. E. Repression of TGF-beta signaling by the oncogenic protein SKI in human melanomas: consequences for proliferation, survival, and metastasis. Oncogene, 2003, 22(20), 3123-3129.
29. Reed, J. A.; Bales, E.; Xu, W.; Okan, N. A.; Bandyopadhyay, D.; Medrano, E. E. Cytoplasmic localization of the oncogenic protein Ski in human cutaneous melanomas in vivo: functional implications for transforming growth factor beta signaling. Cancer Res., 2001, 61(22), 8074-8078.
30. Boone, B.; Haspeslagh, M.; Brochez, L. Clinical significance of the expression of c-Ski and SnoN, possible mediators in TGF-beta resistance, in primary cutaneous melanoma. J. Dermatol. Sci., 2009, 53(1), 26-33.
31. Lopez-Casillas, F.; Wrana, J. L.; Massague, J. Betaglycan presents ligand to the TGF beta signaling receptor. Cell, 1993, 73(7), 1435-1444.
32. Lyons, R. M.; Miller, D. A.; Graycar, J. L.; Moses, H. L.; Derynck, R. Differential binding of transforming growth factor-beta 1, -beta 2, and -beta 3 by fibroblasts and epithelial cells measured by affinity cross-linking of cell surface receptors. Mol. Endocrinol., 1991, 5(12), 1887-1896.
33. Cheifetz, S.; Bellon, T.; Cales, C.; Vera, S.; Bernabeu, C.; Massague, J.; Letarte, M. Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J. Biol. Chem., 1992, 267(27), 19027-19030.
34. Yamashita, H.; Ichijo, H.; Grimsby, S.; Moren, A.; ten Dijke, P.; Miyazono, K. Endoglin forms a heteromeric complex with the signaling receptors for transforming growth factor-beta. J. Biol. Chem., 1994, 269(3), 1995-2001.
35. Bodey, B.; Bodey, B. Jr.; Siegel, S. E.; Kaiser, H. E. Immunocytochemical detection of endoglin is indicative of angiogenesis in malignant melanoma. Anticancer Res., 1998, 18(4A), 2701-2710.
36. Goumans, M. J.; Valdimarsdottir, G.; Itoh, S.; Rosendahl, A.; Sideras, P.; ten Dijke, P. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. Embo J., 2002, 21(7), 1743-1753.
37. Javelaud, D.; Alexaki, V. I.; Mauviel, A. Transforming growth factor-beta in cutaneous melanoma. Pigment Cell Melanoma Res., 2008, 21(2), 123-132.
38. Javelaud, D.; Mauviel, A. Crosstalk mechanisms between the mitogen- activated protein kinase pathways and Smad signaling downstream of TGF-beta: implications for carcinogenesis. Oncogene, 2005, 24(37), 5742-5750.
39. Hannon, G. J.; Beach, D. p15INK4B is a potential effector of TGFbeta- induced cell cycle arrest. Nature, 1994, 371(6494), 257-261.
40. Reynisdottir, I.; Polyak, K.; Iavarone, A.; Massague, J. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev., 1995, 9(15), 1831-1845.
41. Kretzschmar, M.; Doody, J.; Timokhina, I.; Massague, J. A mechanism of repression of TGFbeta/ Smad signaling by oncogenic Ras. Genes Dev., 1999, 13(7), 804-816.
42. Daniotti, M.; Oggionni, M.; Ranzani, T.; Vallacchi, V.; Campi, V.; Di Stasi, D.; Torre, G. D.; Perrone, F.; Luoni, C.; Suardi, S.; Frattini, M.; Pilotti, S.; Anichini, A.; Tragni, G.; Parmiani, G.; Pierotti, M. A.; Rodolfo, M. BRAF alterations are associated with complex mutational profiles in malignant melanoma. Oncogene, 2004, 23(35), 5968-5977.
43. Libra, M.; Malaponte, G.; Navolanic, P. M.; Gangemi, P.; Bevelacqua, V.; Proietti, L.; Bruni, B.; Stivala, F.; Mazzarino, M. C.; Travali, S.; McCubrey, J. A. Analysis of BRAF mutation in primary and metastatic melanoma. Cell Cycle, 2005, 4(10), 1382-1384.
44. Maldonado, J. L.; Fridlyand, J.; Patel, H.; Jain, A. N.; Busam, K.; Kageshita, T.; Ono, T.; Albertson, D. G.; Pinkel, D.; Bastian, B. C. Determinants of BRAF mutations in primary melanomas. J. Natl. Cancer Inst., 2003, 95(24), 1878-1890.
45. Uribe, P.; Wistuba, II; Gonzalez, S. BRAF mutation: a frequent event in benign, atypical, and malignant melanocytic lesions of the skin. Am. J. Dermatopathol., 2003, 25(5), 365-370.
46. Bloethner, S.; Chen, B.; Hemminki, K.; Muller-Berghaus, J.; Ugurel, S.; Schadendorf, D.; Kumar, R. Effect of common B-RAF and N-RAS mutations on global gene expression in melanoma cell lines. Carcinogenesis, 2005, 26(7), 1224-1232.
47. van Elsas, A.; Zerp, S.; van der Flier, S.; Kruse-Wolters, M.; Vacca, A.; Ruiter, D. J.; Schrier, P. Analysis of N-ras mutations in human cutaneous melanoma: tumor heterogeneity detected by polymerase chain reaction/single-stranded conformation polymorphism analysis. Recent Results Cancer Res., 1995, 139, 57-67.
48. Platz, A.; Ringborg, U.; Brahme, E. M.; Lagerlof, B. Melanoma metastases from patients with hereditary cutaneous malignant melanoma contain a high frequency of N-ras activating mutations. Melanoma Res., 1994, 4(3), 169-177.
49. Goydos, J. S.; Mann, B.; Kim, H. J.; Gabriel, E. M.; Alsina, J.; Germino, F. J.; Shih, W.; Gorski, D. H. Detection of B-RAF and NRAS mutations in human melanoma. J. Am. Coll Surg., 2005, 200,(3), 362-370.
50. Lopez-Bergami, P.; Huang, C.; Goydos, J. S.; Yip, D.; Bar-Eli, M.; Herlyn, M.; Smalley, K. S.; Mahale, A.; Eroshkin, A.; Aaronson, S.; Ronai, Z. Rewired ERK-JNK signaling pathways in melanoma. Cancer Cell, 2007, 11(5), 447-460.
51. Alexaki, V. I.; Javelaud, D.; Mauviel, A. JNK supports survival in melanoma cells by controlling cell cycle arrest and apoptosis. Pigment Cell Melanoma Res., 2008, 21(4), 429-438.
52. de Caestecker, M. The transforming growth factor-beta superfamily of receptors. Cytokine Growth Factor Rev., 2004, 15(1), 1-11.
53. Krasagakis, K.; Kruger-Krasagakes, S.; Fimmel, S.; Eberle, J.; Tholke, D.; von der Ohe, M.; Mansmann, U.; Orfanos, C. E. Desensitization of melanoma cells to autocrine TGF-beta isoforms. J. Cell Physiol., 1999, 178(2), 179-187.
54. Rodeck, U.; Nishiyama, T.; Mauviel, A. Independent regulation of growth and SMAD-mediated transcription by transforming growth factor beta in human melanoma cells. Cancer Res., 1999, 59(3), 547-550.
55. Poser, I.; Rothhammer, T.; Dooley, S.; Weiskirchen, R.; Bosserhoff, A. K. Characterization of Sno expression in malignant melanoma. Int. J. Oncol., 2005, 26(5), 1411-1417.
56. Janji, B.; Melchior, C.; Gouon, V.; Vallar, L.; Kieffer, N. Autocrine TGF-beta-regulated expression of adhesion receptors and integrinlinked kinase in HT-144 melanoma cells correlates with their metastatic phenotype. Int. J. Cancer, 1999, 83(2), 255-262.
57. Park, S. S.; Li, L.; Korn, T. S.; Mitra, M. M.; Niederkorn, J. Y. Effect of transforming growth factor-beta on plasminogen activator production of cultured human uveal melanoma cells. Curr. Eye Res., 1996, 15(7), 755-763.
58. Liu, G.; Zhang, F.; Lee, J.; Dong, Z. Selective induction of interleukin- 8 expression in metastatic melanoma cells by transforming growth factor-beta 1. Cytokine, 2005, 31(3), 241-249.
59. Schadendorf, D.; Moller, A.; Algermissen, B.; Worm, M.; Sticherling, M.; Czarnetzki, B. M. IL-8 produced by human malignant melanoma cells in vitro is an essential autocrine growth factor. J. Immunol.,1993, 151(5), 2667-2675.
60. Hoek, K. S.; Schlegel, N. C.; Brafford, P.; Sucker, A.; Ugurel, S.; Kumar, R.; Weber, B. L.; Nathanson, K. L.; Phillips, D. J.; Herlyn, M.; Schadendorf, D.; Dummer, R. Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature. Pigment. Cell Res., 2006, 19(4), 290-302.
61. Javelaud, D.; Mohammad, K. S.; McKenna, C. R.; Fournier, P.; Luciani, F.; Niewolna, M.; Andre, J.; Delmas, V.; Larue, L.; Guise, T. A.; Mauviel, A. Stable overexpression of Smad7 in human melanoma cells impairs bone metastasis. Cancer Res., 2007, 67(5), 2317-2324.
62. Javelaud, D.; Delmas, V.; Moller, M.; Sextius, P.; Andre, J.; Menashi, S.; Larue, L.; Mauviel, A. Stable overexpression of Smad7 in human melanoma cells inhibits their tumorigenicity in vitro and in vivo. Oncogene, 2005, 24(51), 7624-7629.
63. Mauviel, A.; Javelaud, D.; Mohammad, K. S.; Stebbins, E. G.; Niewolna, M.; McKenna, C. R.; Peng, X.; Kingsley, L. A.; Fournier, P. G. J.; Higgins, L. S.; Wong, D. H.; Guise, T. A.;, The transforming growth factor beta receptor I kinase inhibitor SD-208 reduces the development and progression of melanoma bone metastasis. J. Investig. Dermatol., 2007, 127(Suppl. 2), S48.
64. Erickson, A. C.; Barcellos-Hoff, M. H. The not-so innocent bystander: the microenvironment as a therapeutic target in cancer. Expert Opin. Ther. Targets, 2003, 7(1), 71-88.
65. Hofmann, U. B.; Westphal, J. R.; Van Muijen, G. N.; Ruiter, D. J. Matrix metalloproteinases in human melanoma. J. Invest. Dermatol., 2000, 115(3), 337-344.
66. Schnaeker, E. M.; Ossig, R.; Ludwig, T.; Dreier, R.; Oberleithner, H.; Wilhelmi, M.; Schneider, S. W. Microtubule-dependent matrix metalloproteinase-2/matrix metalloproteinase-9 exocytosis: prerequisite in human melanoma cell invasion. Cancer Res., 2004, 64(24), 8924-8931.
67. Berking, C.; Takemoto, R.; Schaider, H.; Showe, L.; Satyamoorthy, K.; Robbins, P.; Herlyn, M. Transforming growth factor-beta1 increases survival of human melanoma through stroma remodeling. Cancer Res., 2001, 61(22), 8306-8316.
68. Xouri, G.; Christian, S. Origin and function of tumor stroma fibroblasts. Semin. Cell Dev. Biol., 21(1), 40-46.
69. Li, G.; Satyamoorthy, K.; Meier, F.; Berking, C.; Bogenrieder, T.; Herlyn, M. Function and regulation of melanoma-stromal fibroblast interactions: when seeds meet soil. Oncogene, 2003, 22(20), 3162-3171.
70. Alonso, S. R.; Tracey, L.; Ortiz, P.; Perez-Gomez, B.; Palacios, J.; Pollan, M.; Linares, J.; Serrano, S.; Saez-Castillo, A. I.; Sanchez, L.; Pajares, R.; Sanchez-Aguilera, A.; Artiga, M. J.; Piris, M. A.; Rodriguez-Peralto, J. L. A high-throughput study in melanoma identifies epithelial-mesenchymal transition as a major determinant of metastasis. Cancer Res., 2007, 67(7), 3450-3460.
71. Fuxe, J.; Vincent, T.; de Herreros, A. G. Transcriptional crosstalk between TGFbeta and stem cell pathways in tumor cell invasion: Role of EMT promoting Smad complexes. Cell Cycle, 2010, 9(12) [Epub ahead of print]
72. Singh, A.; Settleman, J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene, 2010, 29(34), 4741-4751.
73. Frank, N. Y.; Margaryan, A.; Huang, Y.; Schatton, T.; Waaga- Gasser, A. M.; Gasser, M.; Sayegh, M. H.; Sadee, W.; Frank, M. H. ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res., 2005, 65(10), 4320-4333.
74. Singh, R. K.; Varney, M. L.; Bucana, C. D.; Johansson, S. L. Expression of interleukin-8 in primary and metastatic malignant melanoma of the skin. Melanoma Res., 1999, 9(4), 383-387.
75. Ugurel, S.; Rappl, G.; Tilgen, W.; Reinhold, U. Increased serum concentration of angiogenic factors in malignant melanoma patients correlates with tumor progression and survival. J. Clin. Oncol., 2001, 19(2), 577-583.
76. Koch, A. E.; Polverini, P. J.; Kunkel, S. L.; Harlow, L. A.; DiPietro, L. A.; Elner, V. M.; Elner, S. G.; Strieter, R. M. Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science, 1992, 258(5089), 1798-1801.
77. Brat, D. J.; Bellail, A. C.; Van Meir, E. G. The role of interleukin-8 and its receptors in gliomagenesis and tumoral angiogenesis. Neuro. Oncol., 2005, 7(2), 122-133.
78. Peng, H. H.; Liang, S.; Henderson, A. J.; Dong, C. Regulation of interleukin-8 expression in melanoma-stimulated neutrophil inflammatory response. Exp. Cell Res., 2007, 313,(3), 551-559.
79. Gebhardt, C.; Averbeck, M.; Viertel, A.; Kauer, F.; Saalbach, A.; Anderegg, U.; Simon, J. C. Ultraviolet-B irradiation enhances melanoma cell motility via induction of autocrine interleukin 8 secretion. Exp. Dermatol., 2007, 16(8), 636-643.
80. Chakrabarti, S.; Patel, K. D. Regulation of matrix metalloproteinase- 9 release from IL-8-stimulated human neutrophils. J. Leukoc. Biol., 2005, 78(1), 279-288.
81. Ria, R.; Reale, A.; Castrovilli, A.; Mangialardi, G.; Dammacco, F.; Ribatti, D.; Vacca, A. Angiogenesis and progression in human melanoma. Dermatol. Res. Pract., 2010, 185687.
82. Lebrin, F.; Goumans, M. J.; Jonker, L.; Carvalho, R. L.; Valdimarsdottir, G.; Thorikay, M.; Mummery, C.; Arthur, H. M.; ten Dijke, P. Endoglin promotes endothelial cell proliferation and TGFbeta/ ALK1 signal transduction. Embo. J., 2004, 23(20), 4018-4028.
83. Gougos, A.; Letarte, M. Primary structure of endoglin, an RGDcontaining glycoprotein of human endothelial cells. J. Biol. Chem., 1990, 265(15), 8361-8364.
84. Ijland, S. A.; Jager, M. J.; Heijdra, B. M.; Westphal, J. R.; Peek, R. Expression of angiogenic and immunosuppressive factors by uveal melanoma cell lines. Melanoma Res. 1999, 9(5), 445-450.
85. Sugano, Y.; Matsuzaki, K.; Tahashi, Y.; Furukawa, F.; Mori, S.; Yamagata, H.; Yoshida, K.; Matsushita, M.; Nishizawa, M.; Fujisawa, J.; Inoue, K. Distortion of autocrine transforming growth factor beta signal accelerates malignant potential by enhancing cell growth as well as PAI-1 and VEGF production in human hepatocellular carcinoma cells. Oncogene, 2003, 22(15), 2309-2321.
86. Wang, L.; Kwak, J. H.; Kim, S. I.; He, Y.; Choi, M. E. Transforming growth factor-beta1 stimulates vascular endothelial growth factor 164 via mitogen-activated protein kinase kinase 3-p38alpha and p38delta mitogen-activated protein kinase-dependent pathway in murine mesangial cells. J. Biol. Chem., 2004, 279(32), 33213-33219.
87. Huh, S. J.; Chung, C. Y.; Sharma, A.; Robertson, G. P. Macrophage inhibitory cytokine-1 regulates melanoma vascular development. Am. J. Pathol., 176(6), 2948-2957.
88. Ono, M. Molecular links between tumor angiogenesis and inflammation: inflammatory stimuli of macrophages and cancer cells as targets for therapeutic strategy. Cancer Sci., 2008, 99(8), 1501-1506.
89. Goldstein, L. J.; Chen, H.; Bauer, R. J.; Bauer, S. M.; Velazquez, O. C. Normal human fibroblasts enable melanoma cells to induce angiogenesis in type I collagen. Surgery, 2005, 138(3), 439-449.
90. Riker, A. I.; Radfar, S.; Liu, S.; Wang, Y.; Khong, H. T. Immunotherapy of melanoma: a critical review of current concepts and future strategies. Expert Opin. Biol. Ther., 2007, 7(3), 345-358.
91. Schadendorf, D.; Algarra, S. M.; Bastholt, L.; Cinat, G.; Dreno, B.; Eggermont, A. M.; Espinosa, E.; Guo, J.; Hauschild, A.; Petrella, T.; Schachter, J.; Hersey, P. Immunotherapy of distant metastatic disease. Ann. Oncol., 2009, 20 (Suppl 6), vi41-50.
92. Lee, K. H.; Panelli, M. C.; Kim, C. J.; Riker, A. I.; Bettinotti, M. P.; Roden, M. M.; Fetsch, P.; Abati, A.; Rosenberg, S. A.; Marincola, F. M. Functional dissociation between local and systemic immune response during anti-melanoma peptide vaccination. J. Immunol., 1998, 161(8), 4183-4194.
93. Letsch, A.; Keilholz, U.; Fluck, M.; Nagorsen, D.; Asemissen, A. M.; Schmittel, A.; Thiel, E.; Scheibenbogen, C. Peptide vaccination after repeated resection of metastases can induce a prolonged relapse- free interval in melanoma patients. Int. J. Cancer, 2005, 114,(6), 936-941.
94. Letsch, A.; Keilholz, U.; Kern, F.; Asemissen, A. M.; Thiel, E.; Scheibenbogen, C. Specific central memory T cells in the bone marrow of patients immunized against tyrosinase peptides. J. Immunother., 2006, 29(2), 201-207.
95. Mortarini, R.; Piris, A.; Maurichi, A.; Molla, A.; Bersani, I.; Bono, A.; Bartoli, C.; Santinami, M.; Lombardo, C.; Ravagnani, F.; Cascinelli, N.; Parmiani, G.; Anichini, A. Lack of terminally differentiated tumor-specific CD8+ T cells at tumor site in spite of antitu mor immunity to self-antigens in human metastatic melanoma. Cancer Res., 2003, 63(10), 2535-2545.
96. Appay, V.; Jandus, C.; Voelter, V.; Reynard, S.; Coupland, S. E.; Rimoldi, D.; Lienard, D.; Guillaume, P.; Krieg, A. M.; Cerottini, J. C.; Romero, P.; Leyvraz, S.; Rufer, N.; Speiser, D. E. New generation vaccine induces effective melanoma-specific CD8+ T cells in the circulation but not in the tumor site. J. Immunol., 2006, 177(3), 1670-1678.
97. Gajewski, T. F. Identifying and overcoming immune resistance mechanisms in the melanoma tumor microenvironment. Clin. Cancer Res., 2006, 12(7 Pt 2), 2326s-2330s.
98. Real, L. M.; Jimenez, P.; Kirkin, A.; Serrano, A.; Garcia, A.; Canton, J.; Zeuthen, J.; Garrido, F.; Ruiz-Cabello, F. Multiple mechanisms of immune evasion can coexist in melanoma tumor cell lines derived from the same patient. Cancer Immunol. Immunother., 2001, 49(11), 621-628.
99. Mendez, R.; Ruiz-Cabello, F.; Rodriguez, T.; Del Campo, A.; Paschen, A.; Schadendorf, D.; Garrido, F. Identification of different tumor escape mechanisms in several metastases from a melanoma patient undergoing immunotherapy. Cancer Immunol. Immunother., 2007, 56(1), 88-94.
100. Polak, M. E.; Borthwick, N. J.; Gabriel, F. G.; Johnson, P.; Higgins, B.; Hurren, J.; McCormick, D.; Jager, M. J.; Cree, I. A. Mechanisms of local immunosuppression in cutaneous melanoma. Br. J. Cancer, 2007, 96(12), 1879-1887.
101. Ahmadzadeh, M.; Rosenberg, S. A. TGF-beta 1 attenuates the acquisition and expression of effector function by tumor antigenspecific human memory CD8 T cells. J. Immunol., 2005, 174(9), 5215-5223.
102. Park, I. K.; Shultz, L. D.; Letterio, J. J.; Gorham, J. D. TGF-beta1 inhibits T-bet induction by IFN-gamma in murine CD4+ T cells through the protein tyrosine phosphatase Src homology region 2 domain-containing phosphatase-1. J. Immunol., 2005, 175(9), 5666-5674.
103. Park, I. K.; Letterio, J. J.; Gorham, J. D. TGF-beta 1 inhibition of IFN-gamma-induced signaling and Th1 gene expression in CD4+ T cells is Smad3 independent but MAP kinase dependent. Mol. Immunol., 2007, 44(13), 3283-3290.
104. McCarter, M. D.; Baumgartner, J.; Escobar, G. A.; Richter, D.; Lewis, K.; Robinson, W.; Wilson, C.; Palmer, B. E.; Gonzalez, R. Immunosuppressive dendritic and regulatory T cells are upregulated in melanoma patients. Ann. Surg. Oncol., 2007, 14(10), 2854-2860.
105. Nakamura, K.; Kitani, A.; Strober, W. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J. Exp. Med., 2001, 194(5), 629-644.
106. Sakaguchi, S. The origin of FOXP3-expressing CD4+ regulatory T cells: thymus or periphery. J. Clin. Invest, 2003, 112(9), 1310-1312.
107. Ebert, L. M.; Tan, B. S.; Browning, J.; Svobodova, S.; Russell, S. E.; Kirkpatrick, N.; Gedye, C.; Moss, D.; Ng, S. P.; MacGregor, D.; Davis, I. D.; Cebon, J.; Chen, W. The regulatory T cellassociated transcription factor FoxP3 is expressed by tumor cells. Cancer Res., 2008, 68,(8), 3001-3009.
108. Hinz, S.; Pagerols-Raluy, L.; Oberg, H. H.; Ammerpohl, O.; Grussel, S.; Sipos, B.; Grutzmann, R.; Pilarsky, C.; Ungefroren, H.; Saeger, H. D.; Kloppel, G.; Kabelitz, D.; Kalthoff, H. Foxp3 expression in pancreatic carcinoma cells as a novel mechanism of immune evasion in cancer. Cancer Res., 2007, 67(17), 8344-8350.
109. Stockis, J.; Colau, D.; Coulie, P. G.; Lucas, S. Membrane protein GARP is a receptor for latent TGF-beta on the surface of activated human Treg. Eur. J. Immunol., 2009, 39(12), 3315-3322.
110. Tran, D. Q.; Andersson, J.; Wang, R.; Ramsey, H.; Unutmaz, D.; Shevach, E. M. GARP (LRRC32) is essential for the surface expression of latent TGF-beta on platelets and activated FOXP3+ regulatory T cells. Proc. Natl. Acad. Sci. USA, 2009, 106(32), 13445-13450.
111. Mourmouras, V.; Fimiani, M.; Rubegni, P.; Epistolato, M. C.; Malagnino, V.; Cardone, C.; Cosci, E.; Nisi, M. C.; Miracco, C. Evaluation of tumour-infiltrating CD4+CD25+FOXP3+ regulatory T cells in human cutaneous benign and atypical naevi, melanomas and melanoma metastases. Br. J. Dermatol., 2007, 157(3), 531-539.
112. Jandus, C.; Bioley, G.; Speiser, D. E.; Romero, P. Selective accumulation of differentiated FOXP3(+) CD4 (+) T cells in metastatic tumor lesions from melanoma patients compared to peripheral blood. Cancer Immunol. Immunother., 2008, 57(12), 1795-1805.
113. Cesana, G. C.; DeRaffele, G.; Cohen, S.; Moroziewicz, D.; Mitcham, J.; Stoutenburg, J.; Cheung, K.; Hesdorffer, C.; Kim- Schulze, S.; Kaufman, H. L. Characterization of CD4+CD25+ regulatory T cells in patients treated with high-dose interleukin-2 for metastatic melanoma or renal cell carcinoma. J. Clin. Oncol., 2006, 24(7), 1169-1177.
114. Correll, A.; Tuettenberg, A.; Becker, C.; Jonuleit, H. Increased regulatory T-cell frequencies in patients with advanced melanoma correlate with a generally impaired T-cell responsiveness and are restored after dendritic cell-based vaccination. Exp. Dermatol., 19(8), e213-221.
115. Viguier, M.; Lemaitre, F.; Verola, O.; Cho, M. S.; Gorochov, G.; Dubertret, L.; Bachelez, H.; Kourilsky, P.; Ferradini, L. Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J. Immunol., 2004, 173(2), 1444-1453.
116. Baumgartner, J. M.; Gonzalez, R.; Lewis, K. D.; Robinson, W. A.; Richter, D. A.; Palmer, B. E.; Wilson, C. C.; McCarter, M. D. Increased survival from stage IV melanoma associated with fewer regulatory T Cells. J. Surg. Res., 2009, 154(1), 13-20.
117. Mantovani, A.; Sica, A.; Allavena, P.; Garlanda, C.; Locati, M. Tumor-associated macrophages and the related myeloid-derived suppressor cells as a paradigm of the diversity of macrophage activation. Hum. Immunol., 2009, 70(5), 325-330.
118. Marigo, I.; Dolcetti, L.; Serafini, P.; Zanovello, P.; Bronte, V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol. Rev., 2008, 222, 162-179.
119. Young, M. R.; Newby, M.; Wepsic, H. T. Hematopoiesis and suppressor bone marrow cells in mice bearing large metastatic Lewis lung carcinoma tumors. Cancer Res., 1987, 47(1), 100-105.
120. Kusmartsev, S.; Su, Z.; Heiser, A.; Dannull, J.; Eruslanov, E.; Kubler, H.; Yancey, D.; Dahm, P.; Vieweg, J. Reversal of myeloid cell-mediated immunosuppression in patients with metastatic renal cell carcinoma. Clin. Cancer Res., 2008, 14(24), 8270-8278.
121. Rodriguez, P. C.; Ernstoff, M. S.; Hernandez, C.; Atkins, M.; Zabaleta, J.; Sierra, R.; Ochoa, A. C. Arginase I-producing myeloidderived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res., 2009, 69(4), 1553-1560.
122. Filipazzi, P.; Valenti, R.; Huber, V.; Pilla, L.; Canese, P.; Iero, M.; Castelli, C.; Mariani, L.; Parmiani, G.; Rivoltini, L. Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocyte-macrophage colony-stimulation factor-based antitumor vaccine. J. Clin. Oncol., 2007, 25(18), 2546-2553.
123. Vermi, W.; Bonecchi, R.; Facchetti, F.; Bianchi, D.; Sozzani, S.; Festa, S.; Berenzi, A.; Cella, M.; Colonna, M. Recruitment of immature plasmacytoid dendritic cells (plasmacytoid monocytes) and myeloid dendritic cells in primary cutaneous melanomas. J. Pathol., 2003, 200(2), 255-268.
124. Valenti, R.; Huber, V.; Filipazzi, P.; Pilla, L.; Sovena, G.; Villa, A.; Corbelli, A.; Fais, S.; Parmiani, G.; Rivoltini, L. Human tumorreleased microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res., 2006, 66(18), 9290-9298.
125. Sinha, P.; Clements, V. K.; Bunt, S. K.; Albelda, S. M.; Ostrand- Rosenberg, S. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J. Immunol., 2007, 179(2), 977-983.
126. Mourskaia, A. A.; Northey, J. J.; Siegel, P. M. Targeting aberrant TGF-beta signaling in pre-clinical models of cancer. Anticancer Agents Med. Chem., 2007, 7(5), 504-514.
127. Akhurst, R. J. Large- and small-molecule inhibitors of transforming growth factor-beta signaling. Curr. Opin. Investig. Drugs, 2006, 7(6), 513-521.
128. Lahn, M.; Kloeker, S.; Berry, B. S. TGF-beta inhibitors for the treatment of cancer. Expert Opin. Investig. Drugs, 2005, 14(6), 629-643.
129. Schlingensiepen, K. H.; Fischer-Blass, B.; Schmaus, S.; Ludwig, S. Antisense therapeutics for tumor treatment: the TGF-beta2 inhibitor AP 12009 in clinical development against malignant tumors. Recent Results Cancer Res., 2008, 177, 137-150.
130. Llopiz, D.; Dotor, J.; Casares, N.; Bezunartea, J.; Diaz-Valdes, N.; Ruiz, M.; Aranda, F.; Berraondo, P.; Prieto, J.; Lasarte, J. J.; Borras- Cuesta, F.; Sarobe, P. Peptide inhibitors of transforming growth factor-beta enhance the efficacy of antitumor immunotherapy. Int. J. Cancer, 2009, 125(11), 2614-2623.
131. Wrzesinski, S. H.; Wan, Y. Y.; Flavell, R. A. Transforming growth factor-beta and the immune response: implications for anticancer therapy. Clin. Cancer Res., 2007, 13(18 Pt 1), 5262-5270.
132. Yang, Y. A.; Dukhanina, O.; Tang, B.; Mamura, M.; Letterio, J. J.; MacGregor, J.; Patel, S. C.; Khozin, S.; Liu, Z. Y.; Green, J.; Anver, M. R.; Merlino, G.; Wakefield, L. M. Lifetime exposure to a soluble TGF-beta antagonist protects mice against metastasis without adverse side effects. J. Clin. Invest., 2002, 109(12), 1607-1615.
133. Halder, S. K.; Beauchamp, R. D.; Datta, P. K. A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia, 2005, 7(5), 509-521.
134. Wojtowicz-Praga, S.; Verma, U. N.; Wakefield, L.; Esteban, J. M.; Hartmann, D.; Mazumder, A. Modulation of B16 melanoma growth and metastasis by anti-transforming growth factor beta antibody and interleukin-2. J. Immunother. Emphasis Tumor Immunol., 1996, 19(3), 169-175.
135. Gorelik, L.; Flavell, R. A. Immune-mediated eradication of tumors through the blockade of transforming growth factor-beta signaling in T cells. Nat. Med., 2001, 7(10), 1118-1122.
136. Busse, A.; Asemissen, A.; Nonnenmacher, A.; Ochsenreither, S.; Fusi, A.; F. B. Stahter, D.; Schmittel, A.; Miller, D.; Thiel, E.; Keilholz, U. Systemic immune tuning in renal cell carcinoma: favorable prognostic impact of TGF-beta 1 mRNA expression in peripheral blood mononuclear cells. J. Immunother., 2010, 34(1),113-119.
137. Shellman, Y. G.; Chapman, J. T.; Fujita, M.; Norris, D. A.; Maxwell, I. H. Expression of activated N-ras in a primary melanoma cell line counteracts growth inhibition by transforming growth factor- beta. J. Invest. Dermatol., 2000, 114(6), 1200-1204.