The role of the Hippo pathway in melanocytes and melanoma

Frontiers in Oncology

Volumn 3 MAY, Issue , 2013, Pages

  Kim, Ji Eun ^a,b   Finlay, Graeme J ^a   Baguley, Bruce C ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cell proliferation; Cytoskeleton; E cadherin; Epidermal melanocytes; Merlin

Indexed keywords

B RAF KINASE; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; F ACTIN; G PROTEIN COUPLED RECEPTOR; MATRIGEL; METABOTROPIC RECEPTOR; NERVE CELL ADHESION MOLECULE; PROTEIN P16; PROTEIN TYROSINE KINASE; RAC1 PROTEIN; TRANSCRIPTION FACTOR YAP1; UVOMORULIN;

APOPTOSIS; ARTICLE; BASEMENT MEMBRANE; CELL CYCLE G2 PHASE; CELL MIGRATION; CELL PROLIFERATION; EPIDERMIS; GENE MUTATION; HIPPO SIGNALING PATHWAY; HUMAN; INFLAMMATION; KERATINOCYTE; LANGERHANS CELL; MELANOCYTE; MELANOMA; MITOSIS; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 84891111818     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00123     Document Type: Article

References (63)

1. Alexaki, V. I., Javelaud, D., Van Kempen, L. C., Mohammad, K. S., Dennler, S., Luciani, F., et al. (2010). GLI2-mediated melanoma invasion and metastasis. J. Natl. Cancer Inst. 102, 1148-1159.
2. Arck, P. C., Overall, R., Spatz, K., Liezman, C., Handjiski, B., Klapp, B. F., et al. (2006). Towards a "free radical theory of graying": melanocyte apoptosis in the aging human hair follicle is an indicator of oxidative stress induced tissue damage. FASEB J. 20, 1567-1569.
3. Avruch, J., Zhou, D., Fitamant, J., and Bardeesy, N. (2011). Mst1/2 signalling to Yap: gatekeeper for liver size and tumour development. Br. J. Cancer 104, 24-32.
4. Azzolin, L., Zanconato, F., Bresolin, S., Forcato, M., Basso, G., Bicciato, S., et al. (2012). Role of TAZ as mediator of Wnt signaling. Cell 151, 1443-1456.
5. Badouel, C., Gardano, L., Amin, N., Garg, A., Rosenfeld, R., Le Bihan, T., et al. (2009). The FERM-domain protein Expanded regulates Hippo pathway activity via direct interactions with the transcriptional activator Yorkie. Dev. Cell 16, 411-420.
6. Braig, S., Wallner, S., Junglas, B., Fuchshofer, R., and Bosserhoff, A. K. (2011). CTGF is overexpressed in malignant melanoma and promotes cell invasion and migration. Br. J. Cancer 105, 231-238.
7. Cao, X., Pfaff, S. L., and Gage, F. H. (2008). YAP regulates neural progenitor cell number via the TEA domain transcription factor. Genes Dev. 22, 3320-3334.
8. Chan, E. H., Nousiainen, M., Chalamalasetty, R. B., Schafer, A., Nigg, E. A., and Sillje, H. H. (2005). The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 24, 2076-2086.
9. Charters, G. A., Stones, C. J., Shelling, A. N., Baguley, B. C., and Finlay, G. J. (2011). Centrosomal dysregulation in human metastatic melanoma cell lines. Cancer Genet. 204, 477-485.
10. Dick, F. A., and Mymryk, J. S. (2011). Sweet DREAMs for Hippo. Genes Dev. 25, 889-894.
11. Fried, L., and Arbiser, J. L. (2008). The reactive oxygen-driven tumor: relevance to melanoma. Pigment Cell Melanoma Res. 21, 117-122.
12. Fukunaga-Kalabis, M., Martinez, G., Liu, Z. J., Kalabis, J., Mrass, P., Weninger, W., et al. (2006). CCN3 controls 3D spatial localization of melanocytes in the human skin through DDR1. J. Cell Biol. 175, 563-569.
13. Gilchrest, B. A., Blog, F. B., and Szabo, G. (1979). Effects of aging and chronic sun exposure on melanocytes in human skin. J. Invest. Dermatol. 73, 141-143.
14. Haass, N. K., Smalley, K. S., Li, L., and Herlyn, M. (2005). Adhesion, migration and communication in melanocytes and melanoma. Pigment Cell Res. 18, 150-159.
15. Hafner, C., Lopez-Knowles, E., Luis, N. M., Toll, A., Baselga, E., Fernandez-Casado, A., et al. (2007). Oncogenic PIK3CA mutations occur in epidermal nevi and seborrheic keratoses with a characteristic mutation pattern. Proc. Natl. Acad. Sci. U.S.A. 104, 13450-13454.
16. Halder, G., Dupont, S., and Piccolo, S. (2012). Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat. Rev. Mol. Cell Biol. 13, 591-600.
17. Hamaratoglu, F., Willecke, M., Kango-Singh, M., Nolo, R., Hyun, E., Tao, C., et al. (2006). The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat. Cell Biol. 8, 27-36.
18. Hao, Y., Chun, A., Cheung, K., Rashidi, B., and Yang, X. (2008). Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J. Biol. Chem. 283, 5496-5509.
19. Hari, A., Flach, T. L., Shi, Y., and Mydlarski, P. R. (2010). Toll-like receptors: role in dermatological disease. Mediators Inflamm. 2010, 437246.
20. Hauser, S., Ulrich, T., Wurster, S., Schmitt, K., Reichert, N., and Gaubatz, S. (2012). Loss of LIN9, a member of the DREAM complex, cooperates with SV40 large T antigen to induce genomic instability and anchorage-independent growth. Oncogene 31, 1859-1868.
21. Hoogduijn, M. J. I., Hitchcock, S., Smit, N. P., Gillbro, J. M., Schallreuter, K. U., and Genever, P. G. (2006). Glutamate receptors on human melanocytes regulate the expression of MiTF. Pigment Cell Res. 19, 58-67.
22. Kang, W., Tong, J. H., Chan, A. W., Lee, T. L., Lung, R. W., Leung, P. P., et al. (2011). Yes-associated protein 1 exhibits oncogenic property in gastric cancer and its nuclear accumulation associates with poor prognosis. Clin. Cancer Res. 17, 2130-2139.
23. Katoh, M. (2012). Function and cancer genomics of FAT family genes (review). Int. J. Oncol. 41, 1913-1918.
24. Khokhlatchev, A., Rabizadeh, S., Xavier, R., Nedwidek, M., Chen, T., Zhang, X. F., et al. (2002). Identification of a novel Ras-regulated proapoptotic pathway. Curr. Biol. 12, 253-265.
25. Kim, J. E., Stones, C., Joseph, W. R., Leung, E., Finlay, G. J., Shelling, A. N., et al. (2012). Comparison of growth factor signalling pathway utilisation in cultured normal melanocytes and melanoma cell lines. BMC Cancer 12:141.
26. Koo, C. Y., Muir, K. W., and Lam, E. W. (2012). FOXM1: from cancer initiation to progression and treatment. Biochim. Biophys. Acta 1819, 28-37.
27. Krauthammer, M., Kong, Y., Ha, B. H., Evans, P., Bacchiocchi, A., McCusker, J. P., et al. (2012). Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat. Genet. 44, 1006-1014.
28. Lamar, J. M., Stern, P., Liu, H., Schindler, J. W., Jiang, Z. G., and Hynes, R. O. (2012). The Hippo pathway target, YAP, promotes metastasis through its TEAD-interaction domain. Proc. Natl. Acad. Sci. U.S.A. 109, E2441-E2450.
29. Larue, L., Kumasaka, M., and Goding, C. R. (2003). Beta-catenin in the melanocyte lineage. Pigment Cell Res. 16, 312-317.
30. Lee, S. J., Lee, M. H., Kim, D. W., Lee, S., Huang, S., Ryu, M. J., et al. (2011). Cross-regulation between oncogenic BRAF(V600E) kinase and the MST1 pathway in papillary thyroid carcinoma. PLoS ONE 6:e16180.
31. Li, W., Cooper, J., Karajannis, M. A., and Giancotti, F. G. (2012). Merlin: a tumour suppressor with functions at the cell cortex and in the nucleus. EMBO Rep. 13, 204-215.
32. Manzow, S., Brancolini, C., Marks, F., and Richter, K. H. (1996). Expression of growth arrest-specific (Gas) genes in murine keratinocytes: Gas2 is specifically regulated. Exp. Cell Res. 224, 200-203.
33. Mareel, M., Boterberg, T., Noe, V., Van Hoorde, L., Vermeulen, S., Bruyneel, E., et al. (1997). E-cadherin/catenin/cytoskeleton complex: a regulator of cancer invasion. J. Cell. Physiol. 173, 271-274.
34. Marshall, E. S., Holdaway, K. M., Shaw, J. H., Finlay, G. J., Matthews, J. H., and Baguley, B. C. (1993). Anticancer drug sensitivity profiles of new and established melanoma cell lines. Oncol. Res. 5, 301-309.
35. Marshall, E. S., Matthews, J. H., Shaw, J. H., Nixon, J., Tumewu, P., Finlay, G. J., et al. (1994). Radiosensitivity of new and established human melanoma cell lines: comparison of [3H]thymidine incorporation and soft agar clonogenic assays. Eur. J. Cancer 30A, 1370-1376.
36. Mizuno, T., Murakami, H., Fujii, M., Ishiguro, F., Tanaka, I., Kondo, Y., et al. (2012). YAP induces malignant mesothelioma cell proliferation by upregulating transcription of cell cycle-promoting genes. Oncogene 31, 5117-5122.
37. Moleirinho, S., Chang, N., Sims, A. H., Tilston-Lunel, A. M., Angus, L., Steele, A., et al. (2013). KIBRA exhibits MST-independent functional regulation of the Hippo signaling pathway in mammals. Oncogene 32, 1821-1830.
38. Monaghan-Benson, E., and Burridge, K. (2013). Mutant B-RAF regulates a Rac-dependent cadherin switch in melanoma. Oncogene (in press).
39. Murray, L. B., Lau, Y. K., and Yu, Q. (2012). Merlin is a negative regulator of human melanoma growth. PLoS ONE 7:e43295.
40. Noonan, F. P., and De Fabo, E. C. (2009). UVB and UVA initiate different pathways to p53-dependent apoptosis in melanocytes. J. Invest. Dermatol. 129, 1608-1610.
41. Norris, D. A. (2011). "Structure and function of the skin," in Cecil Medicine, ed. L. Goldman (Philadephia: Elsevier), 2498-2503.
42. Pan, D. (2012). The hippo signaling pathway in development and cancer. Dev. Cell 19, 491-505.
43. Pollock, P. M., Harper, U. L., Hansen, K. S., Yudt, L. M., Stark, M., Robbins, C. M., et al. (2003). High frequency of BRAF mutations in nevi. Nat. Genet. 33, 19-20.
44. Qi, J., Chen, N., Wang, J., and Siu, C. H. (2005). Transendothelial migration of melanoma cells involves N-cadherin-mediated adhesion and activation of the beta-catenin signaling pathway. Mol. Biol. Cell 16, 4386-4397.
45. Richter, A. M., Pfeifer, G. P., and Dammann, R. H. (2009). The RASSF proteins in cancer; from epigenetic silencing to functional characterization. Biochim. Biophys. Acta 1796, 114-128.
46. Scott, G. A., and Cassidy, L. (1998). Rac1 mediates dendrite formation in response to melanocyte stimulating hormone and ultraviolet light in a murine melanoma model. J. Invest. Dermatol. 111, 243-250.
47. Sensi, M., Catani, M., Castellano, G., Nicolini, G., Alciato, F., Tragni, G., et al. (2011). Human cutaneous melanomas lacking MITF and melanocyte differentiation antigens express a functional Axl receptor kinase. J. Invest. Dermatol. 131, 2448-2457.
48. Shapiro, L., and Weis, W. I. (2009). Structure and biochemistry of cadherins and catenins. Cold Spring Harb. Perspect. Biol. 1, a003053.
49. Song, Z., He, C. D., Liu, J., Sun, C., Lu, P., Li, L., et al. (2012). Blocking glutamate-mediated signalling inhibits human melanoma growth and migration. Exp. Dermatol. 21, 926-931.
50. Spugnardi, M., Tommasi, S., Dammann, R., Pfeifer, G. P., and Hoon, D. S. (2003). Epigenetic inactivation of RAS association domain family protein 1 (RASSF1A) in malignant cutaneous melanoma. Cancer Res. 63, 1639-1643.
51. Tschop, K., Conery, A. R., Litovchick, L., DeCaprio, J. A., Settleman, J., Harlow, E., et al. (2011). A kinase shRNA screen links LATS2 and the pRB tumor suppressor. Genes Dev. 25, 814-830.
52. Varelas, X., Miller, B. W., Sopko, R., Song, S., Gregorieff, A., Fellouse, F. A., et al. (2010). The Hippo pathway regulates Wnt/beta-catenin signaling. Dev. Cell 18, 579-591.
53. Wei, X., Walia, V., Lin, J. C., Teer, J. K., Prickett, T. D., Gartner, J., et al. (2012). Exome sequencing identifies GRIN2A as frequently mutated in melanoma. Nat. Genet. 43, 442-446.
54. Wu, S., Huang, J., Dong, J., and Pan, D. (2003). Hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114, 445-456.
55. Xiao, L., Chen, Y., Ji, M., and Dong, J. (2011). KIBRA regulates Hippo signaling activity via interactions with large tumor suppressor kinases. J. Biol. Chem. 286, 7788-7796.
56. Xu, M. Z., Chan, S. W., Liu, A. M., Wong, K. F., Fan, S. T., Chen, J., et al. (2011). AXL receptor kinase is a mediator of YAP-dependent oncogenic functions in hepatocellular carcinoma. Oncogene 30, 1229-1240.
57. Yu, F. X., Zhao, B., Panupinthu, N., Jewell, J. L., Lian, I., Wang, L. H., et al. (2011). Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150, 780-791.
58. Yu, J., Zheng, Y., Dong, J., Klusza, S., Deng, W. M., and Pan, D. (2010). Kibra functions as a tumor suppressor protein that regulates Hippo signaling in conjunction with Merlin and Expanded. Dev. Cell 18, 288-299.
59. Zhao, B., Li, L., Tumaneng, K., Wang, C. Y., and Guan, K. L. (2010). A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev. 24, 72-85.
60. Zhao, B., Li, L., Wang, L., Wang, C. Y., Yu, J., and Guan, K. L. (2012). Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 26, 54-68.
61. Zhao, B., Tumaneng, K., and Guan, K. L. (2011). The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat. Cell Biol. 13, 877-883.
62. Zhao, B., Wei, X., Li, W., Udan, R. S., Yang, Q., Kim, J., et al. (2007). Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21, 2747-2761.
63. Zhao, L., Ching, L. M., Kestell, P., Kelland, L. R., and Baguley, B. C. (2005). Mechanisms of tumor vascular shut-down induced by 5,6-dimethylxanthenone-4-acetic acid (DMXAA); increased tumor vascular permeability. Int. J. Cancer 116, 322-326.