Growth and progression of melanoma and non-melanoma skin cancers regulated by ubiquitination

Pigment Cell and Melanoma Research

Volumn 23, Issue 3, 2010, Pages 338-351

  Nakayama, Koh ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Basal cell carcinoma; Melanoma; Squamous cell carcinoma; SUMO; Ubiquitin

Indexed keywords

BETA CATENIN; CASPASE; HYPOXIA INDUCIBLE FACTOR; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; NEDD8 PROTEIN; NOTCH RECEPTOR; PROTEIN P27; PROTEIN P53; PROTEIN SIAH2; S PHASE KINASE ASSOCIATED PROTEIN 2; SMAD PROTEIN; SOMATOMEDIN RECEPTOR; SONIC HEDGEHOG PROTEIN; SUMO PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXM1; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR GLI3; UBIQUITIN; UBIQUITIN CARBOXY TERMINAL HYDROLASE L1; UBIQUITIN PROTEIN LIGASE; UBIQUITIN THIOLESTERASE; UNCLASSIFIED DRUG;

BASAL CELL CARCINOMA; CANCER GROWTH; GROWTH REGULATION; HUMAN; MELANOMA; METASTASIS; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; SKIN CANCER; SKIN CARCINOGENESIS; SQUAMOUS CELL CARCINOMA; SUMOYLATION; UBIQUITINATION;

ANIMALS; CELL PROLIFERATION; DISEASE PROGRESSION; HUMANS; MELANOMA; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; UBIQUITINATION;

EID: 77952571560     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/j.1755-148X.2010.00692.x     Document Type: Review

References (135)

1. Ahmed, A.U., Schmidt, R.L., Park, C.H. et al. (2008). Effect of disrupting seven-in-absentia homolog 2 function on lung cancer cell growth. J. Natl Cancer Inst. 100, 1606 1629.
2. Akhurst, R.J. Derynck, R. (2001). TGF-beta signaling in cancer - a double-edged sword. Trends Cell Biol. 11, S44 S51.
3. Amiri, K.I. Richmond, A. (2005). Role of nuclear factor-kappa B in melanoma. Cancer Metastasis Rev. 24, 301 313.
4. Amiri, K.I., Horton, L.W., LaFleur, B.J., Sosman, J.A. Richmond, A. (2004). Augmenting chemosensitivity of malignant melanoma tumors via proteasome inhibition: implication for bortezomib (VELCADE, PS-341) as a therapeutic agent for malignant melanoma. Cancer Res. 64, 4912 4918.
5. Aza-Blanc, P., Ramirez-Weber, F.A., Laget, M.P., Schwartz, C. Kornberg, T.B. (1997). Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89, 1043 1053.
6. Bales, E.S., Dietrich, C., Bandyopadhyay, D. et al. (1999). High levels of expression of p27KIP1 and cyclin E in invasive primary malignant melanomas. J. Invest. Dermatol. 113, 1039 1046.
7. Balint, K., Xiao, M., Pinnix, C.C., Soma, A., Veres, I., Juhasz, I., Brown, E.J., Capobianco, A.J., Herlyn, M. Liu, Z.J. (2005). Activation of Notch1 signaling is required for beta-catenin-mediated human primary melanoma progression. J. Clin. Invest. 115, 3166 3176.
8. Bardeesy, N., Bastian, B.C., Hezel, A., Pinkel, D., DePinho, R.A. Chin, L. (2001). Dual inactivation of RB and p53 pathways in RAS-induced melanomas. Mol. Cell. Biol. 21, 2144 2153.
9. Bashir, T. Pagano, M. (2003). Aberrant ubiquitin-mediated proteolysis of cell cycle regulatory proteins and oncogenesis. Adv. Cancer Res. 88, 101 144.
10. Bentley, N.J., Eisen, T. Goding, C.R. (1994). Melanocyte-specific expression of the human tyrosinase promoter: activation by the microphthalmia gene product and role of the initiator. Mol. Cell. Biol. 14, 7996 8006.
11. Bhatia, N., Thiyagarajan, S., Elcheva, I., Saleem, M., Dlugosz, A., Mukhtar, H. Spiegelman, V.S. (2006). Gli2 is targeted for ubiquitination and degradation by beta-TrCP ubiquitin ligase. J. Biol. Chem. 281, 19320 19326.
12. Bhatt, K.V., Spofford, L.S., Aram, G., McMullen, M., Pumiglia, K. Aplin, A.E. (2005). Adhesion control of cyclin D1 and p27Kip1 levels is deregulated in melanoma cells through BRAF-MEK-ERK signaling. Oncogene 24, 3459 3471.
13. Bhatt, K.V., Hu, R., Spofford, L.S. Aplin, A.E. (2007). Mutant B-RAF signaling and cyclin D1 regulate Cks1/S-phase kinase-associated protein 2-mediated degradation of p27Kip1 in human melanoma cells. Oncogene 26, 1056 1066.
14. Bowden, G.T. (2004). Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling. Nat. Rev. Cancer 4, 23 35.
15. Busca, R., Berra, E., Gaggioli, C. et al. (2005). Hypoxia-inducible factor 1{alpha} is a new target of microphthalmia-associated transcription factor (MITF) in melanoma cells. J. Cell Biol. 170, 49 59.
16. Caamano, J., Zhang, S.Y., Rosvold, E.A., Bauer, B. Klein-Szanto, A.J. (1993). p53 alterations in human squamous cell carcinomas and carcinoma cell lines. Am. J. Pathol. 142, 1131 1139.
17. Chen, Z., Malhotra, P.S., Thomas, G.R. et al. (1999). Expression of proinflammatory and proangiogenic cytokines in patients with head and neck cancer. Clin. Cancer Res. 5, 1369 1379.
18. Chen, M.F., Lee, K.D., Lu, M.S., Chen, C.C., Hsieh, M.J., Liu, Y.H., Lin, P.Y. Chen, W.C. (2009). The predictive role of E2-EPF ubiquitin carrier protein in esophageal squamous cell carcinoma. J. Mol. Med. 87, 307 320.
19. Chien, A.J., Moore, E.C., Lonsdorf, A.S., Kulikauskas, R.M., Rothberg, B.G., Berger, A.J., Major, M.B., Hwang, S.T., Rimm, D.L. Moon, R.T. (2009). Activated Wnt/beta-catenin signaling in melanoma is associated with decreased proliferation in patient tumors and a murine melanoma model. Proc. Natl Acad. Sci. USA 106, 1193 1198.
20. Dai, P., Akimaru, H., Tanaka, Y., Maekawa, T., Nakafuku, M. Ishii, S. (1999). Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J. Biol. Chem. 274, 8143 8152.
21. Davies, H., Bignell, G.R., Cox, C. et al. (2002). Mutations of the BRAF gene in human cancer. Nature 417, 949 954.
22. De Fabo, E.C., Noonan, F.P., Fears, T. Merlino, G. (2004). Ultraviolet B but not ultraviolet A radiation initiates melanoma. Cancer Res. 64, 6372 6376.
23. Delmas, V., Beermann, F., Martinozzi, S. et al. (2007). Beta-catenin induces immortalization of melanocytes by suppressing p16INK4a expression and cooperates with N-Ras in melanoma development. Genes Dev. 21, 2923 2935.
24. Di Marcotullio, L., Ferretti, E., Greco, A. et al. (2006). Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination. Nat. Cell Biol. 8, 1415 1423.
25. DiGiovanni, J., Bol, D.K., Wilker, E., Beltran, L., Carbajal, S., Moats, S., Ramirez, A., Jorcano, J. Kiguchi, K. (2000). Constitutive expression of insulin-like growth factor-1 in epidermal basal cells of transgenic mice leads to spontaneous tumor promotion. Cancer Res. 60, 1561 1570.
26. Ding, X., Sun, J., Wang, L., Li, G., Shen, Y., Zhou, X. Chen, W. (2008). Overexpression of SENP5 in oral squamous cell carcinoma and its association with differentiation. Oncol. Rep. 20, 1041 1045.
27. Elcheva, I., Tarapore, R.S., Bhatia, N. Spiegelman, V.S. (2008). Overexpression of mRNA-binding protein CRD-BP in malignant melanomas. Oncogene 27, 5069 5074.
28. Eppert, K., Scherer, S.W., Ozcelik, H. et al. (1996). MADR2 maps to 18q21 and encodes a TGFbeta-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86, 543 552.
29. Epstein, E.H. (2008). Basal cell carcinomas: attack of the hedgehog. Nat. Rev. Cancer 8, 743 754.
30. Frescas, D. Pagano, M. (2008). Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat. Rev. Cancer 8, 438 449.
31. Fuchs, S.Y., Adler, V., Buschmann, T., Wu, X. Ronai, Z. (1998). Mdm2 association with p53 targets its ubiquitination. Oncogene 17, 2543 2547.
32. Fukuchi, M., Fukai, Y., Masuda, N., Miyazaki, T., Nakajima, M., Sohda, M., Manda, R., Tsukada, K., Kato, H. Kuwano, H. (2002). High-level expression of the Smad ubiquitin ligase Smurf2 correlates with poor prognosis in patients with esophageal squamous cell carcinoma. Cancer Res. 62, 7162 7165.
33. Fukuchi, M., Nakajima, M., Miyazaki, T., Masuda, N., Osawa, H., Manda, R., Tsukada, K., Kato, H. Kuwano, H. (2006). Lack of activated Smad2 in transforming growth factor-beta signaling is an unfavorable prognostic factor in patients with esophageal squamous cell carcinoma. J. Surg. Oncol. 94, 51 56.
34. Gailani, M.R., Bale, S.J., Leffell, D.J. et al. (1992). Developmental defects in Gorlin syndrome related to a putative tumor suppressor gene on chromosome 9. Cell 69, 111 117.
35. Ganesan, A.K., Kho, Y., Kim, S.C., Chen, Y., Zhao, Y. White, M.A. (2007). Broad spectrum identification of SUMO substrates in melanoma cells. Proteomics 7, 2216 2221.
36. Garraway, L.A., Widlund, H.R., Rubin, M.A. et al. (2005). Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436, 117 122.
37. Girard, M. Goossens, M. (2006). Sumoylation of the SOX10 transcription factor regulates its transcriptional activity. FEBS Lett. 580, 1635 1641.
38. Girnita, L., Girnita, A. Larsson, O. (2003). Mdm2-dependent ubiquitination and degradation of the insulin-like growth factor 1 receptor. Proc. Natl Acad. Sci. USA 100, 8247 8252.
39. Girnita, L., Shenoy, S.K., Sehat, B., Vasilcanu, R., Girnita, A., Lefkowitz, R.J. Larsson, O. (2005). {beta}-Arrestin is crucial for ubiquitination and down-regulation of the insulin-like growth factor-1 receptor by acting as adaptor for the MDM2 E3 ligase. J. Biol. Chem. 280, 24412 24419.
40. Gupta-Rossi, N., Le Bail, O., Gonen, H., Brou, C., Logeat, F., Six, E., Ciechanover, A. Israel, A. (2001). Functional interaction between SEL-10, an F-box protein, and the nuclear form of activated Notch1 receptor. J. Biol. Chem. 276, 34371 34378.
41. Hahn, H., Wicking, C., Zaphiropoulous, P.G. et al. (1996). Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 85, 841 851.
42. Han, J., Cox, D.G., Colditz, G.A. Hunter, D.J. (2006). The p53 codon 72 polymorphism, sunburns, and risk of skin cancer in US Caucasian women. Mol. Carcinog. 45, 694 700.
43. Hibi, K., Westra, W.H., Borges, M., Goodman, S., Sidransky, D. Jen, J. (1999). PGP9.5 as a candidate tumor marker for non-small-cell lung cancer. Am. J. Pathol. 155, 711 715.
44. Hockel, M. Vaupel, P. (2001). Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J. Natl Cancer Inst. 93, 266 276.
45. Hu, R. Aplin, A.E. (2008). Skp2 regulates G2/M progression in a p53-dependent manner. Mol. Biol. Cell 19, 4602 4610.
46. Huntzicker, E.G., Estay, I.S., Zhen, H., Lokteva, L.A., Jackson, P.K. Oro, A.E. (2006). Dual degradation signals control Gli protein stability and tumor formation. Genes Dev. 20, 276 281.
47. Hutchin, M.E., Kariapper, M.S., Grachtchouk, M., Wang, A., Wei, L., Cummings, D., Liu, J., Michael, L.E., Glick, A. Dlugosz, A.A. (2005). Sustained Hedgehog signaling is required for basal cell carcinoma proliferation and survival: conditional skin tumorigenesis recapitulates the hair growth cycle. Genes Dev. 19, 214 223.
48. Itoh, M., Kim, C.H., Palardy, G. et al. (2003). Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 4, 67 82.
49. Jiang, J. (2006). Regulation of Hh/Gli signaling by dual ubiquitin pathways. Cell Cycle 5, 2457 2463.
50. Jiang, J. Struhl, G. (1998). Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb. Nature 391, 493 496.
51. Johnson, R.L., Rothman, A.L., Xie, J. et al. (1996). Human homolog of patched, a candidate gene for the basal cell nevus syndrome. Science 272, 1668 1671.
52. Jokilehto, T., Rantanen, K., Luukkaa, M., Heikkinen, P., Grenman, R., Minn, H., Kronqvist, P. Jaakkola, P.M. (2006). Overexpression and nuclear translocation of hypoxia-inducible factor prolyl hydroxylase PHD2 in head and neck squamous cell carcinoma is associated with tumor aggressiveness. Clin. Cancer Res. 12, 1080 1087.
53. Kaesler, S., Luscher, B. Ruther, U. (2000). Transcriptional activity of GLI1 is negatively regulated by protein kinase A. Biol. Chem. 381, 545 551.
54. Katagiri, Y., Hozumi, Y. Kondo, S. (2006). Knockdown of Skp2 by siRNA inhibits melanoma cell growth in vitro and in vivo. J. Dermatol. Sci. 42, 215 224.
55. Katayama, A., Ogino, T., Bandoh, N., Takahara, M., Kishibe, K., Nonaka, S. Harabuchi, Y. (2007). Overexpression of small ubiquitin-related modifier-1 and sumoylated Mdm2 in oral squamous cell carcinoma: possible involvement in tumor proliferation and prognosis. Int. J. Oncol. 31, 517 524.
56. Kim, A.Y., Bommelje, C.C., Lee, B.E. et al. (2008). SCCRO (DCUN1D1) is an essential component of the E3 complex for NEDDylation. J. Biol. Chem. 283, 33211 33220.
57. Kim, H.J., Kim, Y.M., Lim, S., Nam, Y.K., Jeong, J. Lee, K.J. (2009). Ubiquitin C-terminal hydrolase-L1 is a key regulator of tumor cell invasion and metastasis. Oncogene 28, 117 127.
58. Kinzler, K.W., Ruppert, J.M., Bigner, S.H. Vogelstein, B. (1988). The GLI gene is a member of the Kruppel family of zinc finger proteins. Nature 332, 371 374.
59. Kitajima, S., Kudo, Y., Ogawa, I., Bashir, T., Kitagawa, M., Miyauchi, M., Pagano, M. Takata, T. (2004). Role of Cks1 overexpression in oral squamous cell carcinomas: cooperation with Skp2 in promoting p27 degradation. Am. J. Pathol. 165, 2147 2155.
60. Kudo, Y., Kitajima, S., Sato, S., Miyauchi, M., Ogawa, I. Takata, T. (2001). High expression of S-phase kinase-interacting protein 2, human F-box protein, correlates with poor prognosis in oral squamous cell carcinomas. Cancer Res. 61, 7044 7047.
61. Kudo, Y., Kitajima, S., Ogawa, I., Miyauchi, M. Takata, T. (2005). Down-regulation of Cdk inhibitor p27 in oral squamous cell carcinoma. Oral Oncol. 41, 105 116.
62. Lain, S. Lane, D. (2003). Improving cancer therapy by non-genotoxic activation of p53. Eur. J. Cancer 39, 1053 1060. (Pubitemid 36555861)
63. Larribere, L., Hilmi, C., Khaled, M., Gaggioli, C., Bille, K., Auberger, P., Ortonne, J.P., Ballotti, R. Bertolotto, C. (2005). The cleavage of microphthalmia-associated transcription factor, MITF, by caspases plays an essential role in melanocyte and melanoma cell apoptosis. Genes Dev. 19, 1980 1985.
64. Larsen, C.N., Krantz, B.A. Wilkinson, K.D. (1998). Substrate specificity of deubiquitinating enzymes: ubiquitin C-terminal hydrolases. Biochemistry 37, 3358 3368.
65. Le Borgne, R. Schweisguth, F. (2003). Notch signaling: endocytosis makes delta signal better. Curr. Biol. 13, R273 R275.
66. Levy, C., Khaled, M. Fisher, D.E. (2006). MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol. Med. 12, 406 414.
67. Li, Q., Murphy, M., Ross, J., Sheehan, C. Carlson, J.A. (2004). Skp2 and p27kip1 expression in melanocytic nevi and melanoma: an inverse relationship. J. Cutan. Pathol. 31, 633 642.
68. Lim, K.P., Sharifah, H., Lau, S.H., Teo, S.H. Cheong, S.C. (2005). Alterations of the p14ARF-p53-MDM2 pathway in oral squamous cell carcinoma: MDM2 overexpression is a common event. Oncol. Rep. 14, 963 968.
69. Lin, X., Liang, M. Feng, X.H. (2000). Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signaling. J. Biol. Chem. 275, 36818 36822.
70. Liu, Y., Fallon, L., Lashuel, H.A., Liu, Z. Lansbury Jr., P.T. (2002). The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson's disease susceptibility. Cell 111, 209 218.
71. Liu, J., Suresh Kumar, K.G., Yu, D., Molton, S.A., McMahon, M., Herlyn, M., Thomas-Tikhonenko, A. Fuchs, S.Y. (2007). Oncogenic BRAF regulates beta-Trcp expression and NF-kappaB activity in human melanoma cells. Oncogene 26, 1954 1958.
72. Massague, J. (2000). How cells read TGF-beta signals. Nat. Rev. Mol. Cell Biol. 1, 169 178.
73. McGill, G.G., Horstmann, M., Widlund, H.R. et al. (2002). Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 109, 707 718.
74. Miller, A.J., Levy, C., Davis, I.J., Razin, E. Fisher, D.E. (2005). Sumoylation of MITF and its related family members TFE3 and TFEB. J. Biol. Chem. 280, 146 155.
75. Mo, J.S., Kim, M.Y., Han, S.O. et al. (2007). Integrin-linked kinase controls Notch1 signaling by down-regulation of protein stability through Fbw7 ubiquitin ligase. Mol. Cell. Biol. 27, 5565 5574.
76. Murakami, H. Arnheiter, H. (2005). Sumoylation modulates transcriptional activity of MITF in a promoter-specific manner. Pigment Cell Res. 18, 265 277.
77. Myatt, S.S. Lam, E.W. (2007). The emerging roles of forkhead box (Fox) proteins in cancer. Nat. Rev. Cancer 7, 847 859.
78. Nakayama, K., Qi, J. Ronai, Z. (2009). The ubiquitin ligase Siah2 and the hypoxia response. Mol. Cancer Res. 7, 443 451.
79. Nalepa, G., Rolfe, M. Harper, J.W. (2006). Drug discovery in the ubiquitin-proteasome system. Nat. Rev. Drug Discov. 5, 596 613.
80. Nicolas, M., Wolfer, A., Raj, K., Kummer, J.A., Mill, P., van Noort, M., Hui, C.C., Clevers, H., Dotto, G.P. Radtke, F. (2003). Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet. 33, 416 421.
81. Nilsson, M., Unden, A.B., Krause, D., Malmqwist, U., Raza, K., Zaphiropoulos, P.G. Toftgard, R. (2000). Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1. Proc. Natl Acad. Sci. USA 97, 3438 3443.
82. Noubissi, F.K., Elcheva, I., Bhatia, N., Shakoori, A., Ougolkov, A., Liu, J., Minamoto, T., Ross, J., Fuchs, S.Y. Spiegelman, V.S. (2006). CRD-BP mediates stabilization of betaTrCP1 and c-myc mRNA in response to beta-catenin signalling. Nature 441, 898 901.
83. Oberg, C., Li, J., Pauley, A., Wolf, E., Gurney, M. Lendahl, U. (2001). The Notch intracellular domain is ubiquitinated and negatively regulated by the mammalian Sel-10 homolog. J. Biol. Chem. 276, 35847 35853.
84. Omholt, K., Platz, A., Ringborg, U. Hansson, J. (2001). Cytoplasmic and nuclear accumulation of beta-catenin is rarely caused by CTNNB1 exon 3 mutations in cutaneous malignant melanoma. Int. J. Cancer 92, 839 842.
85. Orlowski, R.Z. Kuhn, D.J. (2008). Proteasome inhibitors in cancer therapy: lessons from the first decade. Clin. Cancer Res. 14, 1649 1657.
86. Oro, A.E., Higgins, K.M., Hu, Z., Bonifas, J.M., Epstein Jr., E.H. Scott, M.P. (1997). Basal cell carcinomas in mice overexpressing sonic hedgehog. Science 276, 817 821.
87. Pan, Y., Bai, C.B., Joyner, A.L. Wang, B. (2006). Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol. Cell. Biol., 26, 3365 3377.
88. Park, H.J., Costa, R.H., Lau, L.F., Tyner, A.L. Raychaudhuri, P. (2008). Anaphase-promoting complex/cyclosome-CDH1-mediated proteolysis of the forkhead box M1 transcription factor is critical for regulated entry into S phase. Mol. Cell. Biol. 28, 5162 5171.
89. Perkins, N.D. (2007). Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat. Rev. Mol. Cell Biol. 8, 49 62.
90. Polsky, D., Bastian, B.C., Hazan, C., Melzer, K., Pack, J., Houghton, A., Busam, K., Cordon-Cardo, C. Osman, I. (2001). HDM2 protein overexpression, but not gene amplification, is related to tumorigenesis of cutaneous melanoma. Cancer Res. 61, 7642 7646.
91. Prunier, C., Ferrand, N., Frottier, B., Pessah, M. Atfi, A. (2001). Mechanism for mutational inactivation of the tumor suppressor Smad2. Mol. Cell. Biol. 21, 3302 3313.
92. Qi, J., Nakayama, K., Gaitonde, S., Goydos, J.S., Krajewski, S., Eroshkin, A., Bar-Sagi, D., Bowtell, D. Ronai, Z. (2008). The ubiquitin ligase Siah2 regulates tumorigenesis and metastasis by HIF-dependent and -independent pathways. Proc. Natl Acad. Sci. USA 105, 16713 16718.
93. Qin, J.Z., Ziffra, J., Stennett, L. et al. (2005). Proteasome inhibitors trigger NOXA-mediated apoptosis in melanoma and myeloma cells. Cancer Res. 65, 6282 6293.
94. Rabut, G. Peter, M. (2008). Function and regulation of protein NEDDylation. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep. 9, 969 976.
95. Reyes-Turcu, F.E., Ventii, K.H. Wilkinson, K.D. (2009). Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 78, 363 397.
96. Ricker, J.L., Chen, Z., Yang, X.P., Pribluda, V.S., Swartz, G.M. Van Waes, C. (2004). 2-methoxyestradiol inhibits hypoxia-inducible factor 1alpha, tumor growth, and angiogenesis and augments paclitaxel efficacy in head and neck squamous cell carcinoma. Clin. Cancer Res. 10, 8665 8673.
97. Rimm, D.L., Caca, K., Hu, G., Harrison, F.B. Fearon, E.R. (1999). Frequent nuclear/cytoplasmic localization of beta-catenin without exon 3 mutations in malignant melanoma. Am. J. Pathol. 154, 325 329.
98. Ronen, O., Malone, J.P., Kay, P., Bivens, C., Hall, K., Paruchuri, L.P., Mo, Y.Y., Robbins, K.T. Ran, S. (2009). Expression of a novel marker, Ubc9, in squamous cell carcinoma of the head and neck. Head Neck 31, 845 855.
99. Rubinfeld, B., Robbins, P., El-Gamil, M., Albert, I., Porfiri, E. Polakis, P. (1997). Stabilization of beta-catenin by genetic defects in melanoma cell lines. Science 275, 1790 1792.
100. Sarkaria, I., Charoenrat, P.O., Talbot, S.G. et al. (2006). Squamous cell carcinoma related oncogene/DCUN1D1 is highly conserved and activated by amplification in squamous cell carcinomas. Cancer Res. 66, 9437 9444.
101. Schmidt, R.L., Park, C.H., Ahmed, A.U., Gundelach, J.H., Reed, N.R., Cheng, S., Knudsen, B.E. Tang, A.H. (2007). Inhibition of RAS-mediated transformation and tumorigenesis by targeting the downstream E3 ubiquitin ligase seven in absentia homologue. Cancer Res. 67, 11798 11810.
102. Semenza, G.L. (2002). HIF-1 and tumor progression: pathophysiology and therapeutics. Trends Mol. Med. 8, S62 S67.
103. Semenza, G.L. (2003). Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721 732.
104. Setlow, R.B., Woodhead, A.D. Grist, E. (1989). Animal model for ultraviolet radiation-induced melanoma: platyfish-swordtail hybrid. Proc. Natl Acad. Sci. USA 86, 8922 8926.
105. Soldatenkov, V.A., Dritschilo, A., Ronai, Z. Fuchs, S.Y. (1999). Inhibition of homologue of Slimb (HOS) function sensitizes human melanoma cells for apoptosis. Cancer Res. 59, 5085 5088.
106. Sparrow, L.E., Soong, R., Dawkins, H.J., Iacopetta, B.J. Heenan, P.J. (1995). p53 gene mutation and expression in naevi and melanomas. Melanoma Res. 5, 93 100.
107. Stracke, M.L., Engel, J.D., Wilson, L.W., Rechler, M.M., Liotta, L.A. Schiffmann, E. (1989). The type I insulin-like growth factor receptor is a motility receptor in human melanoma cells. J. Biol. Chem. 264, 21544 21549.
108. Sumimoto, H., Hirata, K., Yamagata, S., Miyoshi, H., Miyagishi, M., Taira, K. Kawakami, Y. (2006). Effective inhibition of cell growth and invasion of melanoma by combined suppression of BRAF (V599E) and Skp2 with lentiviral RNAi. Int. J. Cancer 118, 472 476.
109. Sunwoo, J.B., Chen, Z., Dong, G., Yeh, N., Crowl Bancroft, C., Sausville, E., Adams, J., Elliott, P. Van Waes, C. (2001). Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-kappa B, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma. Clin. Cancer Res. 7, 1419 1428.
110. Takeuchi, T., Adachi, Y., Sonobe, H., Furihata, M. Ohtsuki, Y. (2006). A ubiquitin ligase, skeletrophin, is a negative regulator of melanoma invasion. Oncogene 25, 7059 7069.
111. Teh, M.T., Wong, S.T., Neill, G.W., Ghali, L.R., Philpott, M.P. Quinn, A.G. (2002). FOXM1 is a downstream target of Gli1 in basal cell carcinomas. Cancer Res. 62, 4773 4780.
112. Tempe, D., Casas, M., Karaz, S., Blanchet-Tournier, M.F. Concordet, J.P. (2006). Multisite protein kinase A and glycogen synthase kinase 3beta phosphorylation leads to Gli3 ubiquitination by SCFbetaTrCP. Mol. Cell. Biol. 26, 4316 4326.
113. Tezel, E., Hibi, K., Nagasaka, T. Nakao, A. (2000). PGP9.5 as a prognostic factor in pancreatic cancer. Clin. Cancer Res. 6, 4764 4767.
114. Tokumaru, Y., Yamashita, K., Osada, M., Nomoto, S., Sun, D.I., Xiao, Y., Hoque, M.O., Westra, W.H., Califano, J.A. Sidransky, D. (2004). Inverse correlation between cyclin A1 hypermethylation and p53 mutation in head and neck cancer identified by reversal of epigenetic silencing. Cancer Res. 64, 5982 5987.
115. Tokumaru, Y., Yamashita, K., Kim, M.S., Park, H.L., Osada, M., Mori, M. Sidransky, D. (2008). The role of PGP9.5 as a tumor suppressor gene in human cancer. Int. J. Cancer 123, 753 759.
116. Uchida, K., Nagatake, M., Osada, H., Yatabe, Y., Kondo, M., Mitsudomi, T., Masuda, A. Takahashi, T. (1996). Somatic in vivo alterations of the JV18-1 gene at 18q21 in human lung cancers. Cancer Res. 56, 5583 5585. (Pubitemid 26422155)
117. Uehara, M., Sano, K., Ikeda, H., Nonaka, M. Asahina, I. (2009). Hypoxia-inducible factor 1 alpha in oral squamous cell carcinoma and its relation to prognosis. Oral Oncol. 45, 241 246.
118. Vazquez, A., Bond, E.E., Levine, A.J. Bond, G.L. (2008). The genetics of the p53 pathway, apoptosis and cancer therapy. Nat. Rev. Drug Discov. 7, 979 987.
119. Wang, B. Li, Y. (2006). Evidence for the direct involvement of {beta}TrCP in Gli3 protein processing. Proc. Natl Acad. Sci. USA 103, 33 38.
120. Wang, I.C., Chen, Y.J., Hughes, D., Petrovic, V., Major, M.L., Park, H.J., Tan, Y., Ackerson, T. Costa, R.H. (2005). Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol. Cell. Biol. 25, 10875 10894.
121. Welchman, R.L., Gordon, C. Mayer, R.J. (2005). Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat. Rev. Mol. Cell Biol. 6, 599 609.
122. Widlund, H.R., Horstmann, M.A., Price, E.R., Cui, J., Lessnick, S.L., Wu, M., He, X. Fisher, D.E. (2002). Beta-catenin-induced melanoma growth requires the downstream target Microphthalmia-associated transcription factor. J. Cell Biol. 158, 1079 1087.
123. Wigfield, S.M., Winter, S.C., Giatromanolaki, A., Taylor, J., Koukourakis, M.L. Harris, A.L. (2008). PDK-1 regulates lactate production in hypoxia and is associated with poor prognosis in head and neck squamous cancer. Br. J. Cancer 98, 1975 1984.
124. Wilson, P.O., Barber, P.C., Hamid, Q.A., Power, B.F., Dhillon, A.P., Rode, J., Day, I.N., Thompson, R.J. Polak, J.M. (1988). The immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies. Br. J. Exp. Pathol. 69, 91 104.
125. Winston, J.T., Strack, P., Beer-Romero, P., Chu, C.Y., Elledge, S.J. Harper, J.W. (1999). The SCFbeta-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IkappaBalpha and beta-catenin and stimulates IkappaBalpha ubiquitination in vitro. Genes Dev. 13, 270 283.
126. Woenckhaus, C., Maile, S., Uffmann, S., Bansemir, M., Dittberner, T., Poetsch, M. Giebel, J. (2005). Expression of Skp2 and p27KIP1 in naevi and malignant melanoma of the skin and its relation to clinical outcome. Histol. Histopathol. 20, 501 508.
127. Wu, M., Hemesath, T.J., Takemoto, C.M., Horstmann, M.A., Wells, A.G., Price, E.R., Fisher, D.Z. Fisher, D.E. (2000). c-Kit triggers dual phosphorylations, which couple activation and degradation of the essential melanocyte factor Mi. Genes Dev. 14, 301 312.
128. Wu, G., Lyapina, S., Das, I., Li, J., Gurney, M., Pauley, A., Chui, I., Deshaies, R.J. Kitajewski, J. (2001). SEL-10 is an inhibitor of notch signaling that targets notch for ubiquitin-mediated protein degradation. Mol. Cell. Biol. 21, 7403 7415.
129. Xu, W., Gong, L., Haddad, M.M., Bischof, O., Campisi, J., Yeh, E.T. Medrano, E.E. (2000). Regulation of microphthalmia-associated transcription factor MITF protein levels by association with the ubiquitin-conjugating enzyme hUBC9. Exp. Cell Res. 255, 135 143.
130. Yamazaki, T., Hibi, K., Takase, T., Tezel, E., Nakayama, H., Kasai, Y., Ito, K., Akiyama, S., Nagasaka, T. Nakao, A. (2002). PGP9.5 as a marker for invasive colorectal cancer. Clin. Cancer Res. 8, 192 195.
131. Yasumoto, K., Yokoyama, K., Shibata, K., Tomita, Y. Shibahara, S. (1994). Microphthalmia-associated transcription factor as a regulator for melanocyte-specific transcription of the human tyrosinase gene. Mol. Cell. Biol. 14, 8058 8070.
132. Yasumoto, K., Yokoyama, K., Takahashi, K., Tomita, Y. Shibahara, S. (1997). Functional analysis of microphthalmia-associated transcription factor in pigment cell-specific transcription of the human tyrosinase family genes. J. Biol. Chem. 272, 503 509.
133. Yue, S., Chen, Y. Cheng, S.Y. (2009). Hedgehog signaling promotes the degradation of tumor suppressor Sufu through the ubiquitin-proteasome pathway. Oncogene 28, 492 499.
134. Zhang, L. Hill, R.P. (2004). Hypoxia enhances metastatic efficiency by up-regulating Mdm2 in KHT cells and increasing resistance to apoptosis. Cancer Res. 64, 4180 4189.
135. Zhang, Q., Shi, Q., Chen, Y., Yue, T., Li, S., Wang, B. Jiang, J. (2009). Multiple Ser/Thr-rich degrons mediate the degradation of Ci/Gli by the Cul3-HIB/SPOP E3 ubiquitin ligase. Proc. Natl Acad. Sci. USA 106, 21191 21196.