β-Catenin Signaling Controls Metastasis in Braf-Activated Pten-Deficient Melanomas

Cancer Cell

Volumn 20, Issue 6, 2011, Pages 741-754

  Damsky, William E ^a,b   Curley, David P ^b,c   Santhanakrishnan, Manjula ^a   Rosenbaum, Lara E ^a   Platt, James T ^a   Gould Rothberg, Bonnie E ^a   Taketo, Makoto M ^d   Dankort, David ^e   Rimm, David L ^a   McMahon, Martin ^f,g,h   Bosenberg, Marcus ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e MCGILL UNIVERSITY   (Canada)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; BETA CATENIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; WNT PROTEIN;

ANIMAL MODEL; ARTICLE; CANCER CONTROL; ENZYME REGULATION; GENE LOSS; HUMAN; HUMAN CELL; LUNG METASTASIS; LYMPH NODE METASTASIS; MELANOMA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN STABILITY; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; TUMOR DIFFERENTIATION;

EID: 83455171909     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2011.10.030     Document Type: Article

References (51)

1. Bedrosian I., Faries M.B., Guerry D., Elenitsas R., Schuchter L., Mick R., Spitz F.R., Bucky L.P., Alavi A., Elder D.E., et al. Incidence of sentinel node metastasis in patients with thin primary melanoma (< or = 1 mm) with vertical growth phase. Ann. Surg. Oncol. 2000, 7:262-267.
2. Bennett D.C., Dexter T.J., Ormerod E.J., Hart I.R. Increased experimental metastatic capacity of a murine melanoma following induction of differentiation. Cancer Res. 1986, 46:3239-3244.
3. Boussadia O., Kutsch S., Hierholzer A., Delmas V., Kemler R. E-cadherin is a survival factor for the lactating mouse mammary gland. Mech. Dev. 2002, 115:53-62.
4. Brault V., Moore R., Kutsch S., Ishibashi M., Rowitch D.H., McMahon A.P., Sommer L., Boussadia O., Kemler R. Inactivation of the β-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001, 128:1253-1264.
5. Chapman P.B., Hauschild A., Robert C., Haanen J.B., Ascierto P., Larkin J., Dummer R., Garbe C., Testori A., Maio M., et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N. Engl. J. Med. 2011, 364:2507-2516. BRIM-3 Study Group.
6. Cheli Y., Ohanna M., Ballotti R., Bertolotto C. Fifteen-year quest for microphthalmia-associated transcription factor target genes. Pigment Cell Melanoma Res. 2010, 23:27-40.
7. Cheung M., Sharma A., Madhunapantula S.V., Robertson G.P. Akt3 and mutant V600E B-Raf cooperate to promote early melanoma development. Cancer Res. 2008, 68:3429-3439.
8. 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. Activated Wnt/β-catenin signaling in melanoma is associated with decreased proliferation in patient tumors and a murine melanoma model. Proc. Natl. Acad. Sci. USA 2009, 106:1193-1198.
9. Chin L., Tam A., Pomerantz J., Wong M., Holash J., Bardeesy N., Shen Q., O'Hagan R., Pantginis J., Zhou H., et al. Essential role for oncogenic Ras in tumour maintenance. Nature 1999, 400:468-472.
10. Curtin J.A., Fridlyand J., Kageshita T., Patel H.N., Busam K.J., Kutzner H., Cho K.H., Aiba S., Bröcker E.B., LeBoit P.E., et al. Distinct sets of genetic alterations in melanoma. N. Engl. J. Med. 2005, 353:2135-2147.
11. Dankort D., Curley D.P., Cartlidge R.A., Nelson B., Karnezis A.N., Damsky W.E., You M.J., DePinho R.A., McMahon M., Bosenberg M. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 2009, 41:544-552.
12. Delmas V., Beermann F., Martinozzi S., Carreira S., Ackermann J., Kumasaka M., Denat L., Goodall J., Luciani F., Viros A., et al. Beta-catenin induces immortalization of melanocytes by suppressing p16INK4a expression and cooperates with N-Ras in melanoma development. Genes Dev. 2007, 21:2923-2935.
13. Demunter A., Libbrecht L., Degreef H., De Wolf-Peeters C., van den Oord J.J. Loss of membranous expression of β-catenin is associated with tumor progression in cutaneous melanoma and rarely caused by exon 3 mutations. Mod. Pathol. 2002, 15:454-461.
14. Dry J.R., Pavey S., Pratilas C.A., Harbron C., Runswick S., Hodgson D., Chresta C., McCormack R., Byrne N., Cockerill M., et al. Transcriptional pathway signatures predict MEK addiction and response to selumetinib (AZD6244). Cancer Res. 2010, 70:2264-2273.
15. Forbes S.A., Tang G., Bindal N., Bamford S., Dawson E., Cole C., Kok C.Y., Jia M., Ewing R., Menzies A., et al. COSMIC (the Catalogue of Somatic Mutations in Cancer): a resource to investigate acquired mutations in human cancer. Nucleic Acids Res. 2010, 38(Database issue):D652-D657.
16. Garraway L.A., Widlund H.R., Rubin M.A., Getz G., Berger A.J., Ramaswamy S., Beroukhim R., Milner D.A., Granter S.R., Du J., et al. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 2005, 436:117-122.
17. Girardini J.E., Napoli M., Piazza S., Rustighi A., Marotta C., Radaelli E., Capaci V., Jordan L., Quinlan P., Thompson A., et al. A Pin1/mutant p53 axis promotes aggressiveness in breast cancer. Cancer Cell 2011, 20:79-91.
18. Guertin D.A., Sabatini D.M. Defining the role of mTOR in cancer. Cancer Cell 2007, 12:9-22.
19. Gupta P.B., Kuperwasser C., Brunet J.P., Ramaswamy S., Kuo W.L., Gray J.W., Naber S.P., Weinberg R.A. The melanocyte differentiation program predisposes to metastasis after neoplastic transformation. Nat. Genet. 2005, 37:1047-1054.
20. Han C.Y., Hien T.T., Lim S.C., Kang K.W. Role of Pin1 in UVA-induced cell proliferation and malignant transformation in epidermal cells. Biochem. Biophys. Res. Commun. 2011, 410:68-74.
21. Harada N., Tamai Y., Ishikawa T., Sauer B., Takaku K., Oshima M., Taketo M.M. Intestinal polyposis in mice with a dominant stable mutation of the β-catenin gene. EMBO J. 1999, 18:5931-5942.
22. Hari L., Brault V., Kléber M., Lee H.Y., Ille F., Leimeroth R., Paratore C., Suter U., Kemler R., Sommer L. Lineage-specific requirements of β-catenin in neural crest development. J. Cell Biol. 2002, 159:867-880.
23. Hodi F.S., O'Day S.J., McDermott D.F., Weber R.W., Sosman J.A., Haanen J.B., Gonzalez R., Robert C., Schadendorf D., Hassel J.C., et al. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 2010, 363:711-723.
24. Kageshita T., Hamby C.V., Ishihara T., Matsumoto K., Saida T., Ono T. Loss of β-catenin expression associated with disease progression in malignant melanoma. Br. J. Dermatol. 2001, 145:210-216.
25. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119:1420-1428.
26. Khaled M., Levy C., Fisher D.E. Control of melanocyte differentiation by a MITF-PDE4D3 homeostatic circuit. Genes Dev. 2010, 24:2276-2281.
27. Kielhorn E., Provost E., Olsen D., D'Aquila T.G., Smith B.L., Camp R.L., Rimm D.L. Tissue microarray-based analysis shows phospho-β-catenin expression in malignant melanoma is associated with poor outcome. Int. J. Cancer 2003, 103:652-656.
28. Kreizenbeck G.M., Berger A.J., Subtil A., Rimm D.L., Gould Rothberg B.E. Prognostic significance of cadherin-based adhesion molecules in cutaneous malignant melanoma. Cancer Epidemiol. Biomarkers Prev. 2008, 17:949-958.
29. Larue L., Delmas V. The WNT/β-catenin pathway in melanoma. Front. Biosci. 2006, 11:733-742.
30. Li H., Wang S., Zhu T., Zhou J., Xu Q., Lu Y., Ma D. Pin1 contributes to cervical tumorigenesis by regulating cyclin D1 expression. Oncol. Rep. 2006, 16:491-496.
31. Liao Y., Wei Y., Zhou X., Yang J.Y., Dai C., Chen Y.J., Agarwal N.K., Sarbassov D., Shi D., Yu D., Hung M.C. Peptidyl-prolyl cis/trans isomerase Pin1 is critical for the regulation of PKB/Akt stability and activation phosphorylation. Oncogene 2009, 28:2436-2445.
32. MacDonald B.T., Tamai K., He X. Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 2009, 17:9-26.
33. Nakatsu Y., Sakoda H., Kushiyama A., Zhang J., Ono H., Fujishiro M., Kikuchi T., Fukushima T., Yoneda M., Ohno H., et al. Peptidyl-prolyl cis/trans isomerase NIMA-interacting 1 associates with insulin receptor substrate-1 and enhances insulin actions and adipogenesis. J. Biol. Chem. 2011, 286:20812-20822.
34. Nazarian R.M., Prieto V.G., Elder D.E., Duncan L.M. Melanoma biomarker expression in melanocytic tumor progression: a tissue microarray study. J. Cutan. Pathol. 2010, 37(Suppl 1):41-47.
35. Oh W.J., Wu C.C., Kim S.J., Facchinetti V., Julien L.A., Finlan M., Roux P.P., Su B., Jacinto E. mTORC2 can associate with ribosomes to promote cotranslational phosphorylation and stability of nascent Akt polypeptide. EMBO J. 2010, 29:3939-3951.
36. Omholt K., Platz A., Ringborg U., Hansson J. Cytoplasmic and nuclear accumulation of β-catenin is rarely caused by CTNNB1 exon 3 mutations in cutaneous malignant melanoma. Int. J. Cancer 2001, 92:839-842.
37. Packer L.M., East P., Reis-Filho J.S., Marais R. Identification of direct transcriptional targets of (V600E)BRAF/MEK signalling in melanoma. Pigment Cell Melanoma Res. 2009, 22:785-798.
38. Purdue M.P., Freeman L.E., Anderson W.F., Tucker M.A. Recent trends in incidence of cutaneous melanoma among US Caucasian young adults. J. Invest. Dermatol. 2008, 128:2905-2908.
39. Reifenberger J., Knobbe C.B., Wolter M., Blaschke B., Schulte K.W., Pietsch T., Ruzicka T., Reifenberger G. Molecular genetic analysis of malignant melanomas for aberrations of the WNT signaling pathway genes CTNNB1, APC, ICAT and BTRC. Int. J. Cancer 2002, 100:549-556.
40. Rimm D.L., Caca K., Hu G., Harrison F.B., Fearon E.R. Frequent nuclear/cytoplasmic localization of β-catenin without exon 3 mutations in malignant melanoma. Am. J. Pathol. 1999, 154:325-329.
41. Rubinfeld B., Robbins P., El-Gamil M., Albert I., Porfiri E., Polakis P. Stabilization of β-catenin by genetic defects in melanoma cell lines. Science 1997, 275:1790-1792.
42. Sanders D.S., Blessing K., Hassan G.A., Bruton R., Marsden J.R., Jankowski J. Alterations in cadherin and catenin expression during the biological progression of melanocytic tumours. MP, Mol. Pathol. 1999, 52:151-157.
43. Silye R., Karayiannakis A.J., Syrigos K.N., Poole S., van Noorden S., Batchelor W., Regele H., Sega W., Boesmueller H., Krausz T., Pignatelli M. E-cadherin/catenin complex in benign and malignant melanocytic lesions. J. Pathol. 1998, 186:350-355.
44. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
45. Tucci M.G., Lucarini G., Brancorsini D., Zizzi A., Pugnaloni A., Giacchetti A., Ricotti G., Biagini G. Involvement of E-cadherin, β-catenin, Cdc42 and CXCR4 in the progression and prognosis of cutaneous melanoma. Br. J. Dermatol. 2007, 157:1212-1216.
46. Tsao H., Goel V., Wu H., Yang G., Haluska F.G. Genetic interaction between NRAS and BRAF mutations and PTEN/MMAC1 inactivation in melanoma. J. Invest. Dermatol. 2004, 122:337-341.
47. Ugurel S., Houben R., Schrama D., Voigt H., Zapatka M., Schadendorf D., Bröcker E.B., Becker J.C. Microphthalmia-associated transcription factor gene amplification in metastatic melanoma is a prognostic marker for patient survival, but not a predictive marker for chemosensitivity and chemotherapy response. Clin. Cancer Res. 2007, 13:6344-6350.
48. Wang R., Ferrell L.D., Faouzi S., Maher J.J., Bishop J.M. Activation of the Met receptor by cell attachment induces and sustains hepatocellular carcinomas in transgenic mice. J. Cell Biol. 2001, 153:1023-1034.
49. Wellbrock C., Rana S., Paterson H., Pickersgill H., Brummelkamp T., Marais R. Oncogenic BRAF regulates melanoma proliferation through the lineage specific factor MITF. PLoS ONE 2008, 3:e2734.
50. Widlund H.R., Horstmann M.A., Price E.R., Cui J., Lessnick S.L., Wu M., He X., Fisher D.E. β-catenin-induced melanoma growth requires the downstream target Microphthalmia-associated transcription factor. J. Cell Biol. 2002, 158:1079-1087.
51. Zhang D., O'neil M.F., Cunningham M.T., Fan F., Olyaee M., Li L. Abnormal Wnt signaling and stem cell activation in reactive lymphoid tissue and low-grade marginal zone lymphoma. Leuk. Lymphoma 2010, 51:906-910.