RAB7 Controls Melanoma Progression by Exploiting a Lineage-Specific Wiring of the Endolysosomal Pathway

Cancer Cell

Volumn 26, Issue 1, 2014, Pages 61-76

  Alonso Curbelo, Direna ^a   Riveiro Falkenbach, Erica ^a   Pérez Guijarro, Eva ^a   Cifdaloz, Metehan ^a   Karras, Panagiotis ^a   Osterloh, Lisa ^a   Megías, Diego ^a   Cañón, Estela ^a   Calvo, TonantzinG ^a   Olmeda, David ^a   Gómez López, Gonzalo ^a   Graña, Osvaldo ^a   Sánchez ArévaloLobo, VíctorJavier ^a   Pisano, DavidG ^a   Wang, Hao Wei ^b   Ortiz Romero, Pablo ^c   Tormo, Damià ^a   Hoek, Keith ^d   Rodríguez Peralto, JoséL ^c   Joyce, JohannaA ^b   Soengas, MaríaS ^a   more..

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; RAB7 PROTEIN; TRANSCRIPTION FACTOR SOX10;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PROGNOSIS; CELL LINEAGE; CONTROLLED STUDY; ENDOSOME; GENE CLUSTER; HUMAN; HUMAN CELL; HUMAN TISSUE; LYSOSOME; MELANOCYTE; MELANOMA; MELANOMA CELL; METASTASIS; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR INVASION;

ANIMALS; CELL LINE, TUMOR; CELL LINEAGE; CELL MOVEMENT; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYSOSOMES; MELANOMA; MICE; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-MYC; RAB GTP-BINDING PROTEINS; RNA INTERFERENCE; SKIN NEOPLASMS; SOXE TRANSCRIPTION FACTORS; TIME FACTORS; TRANSFECTION; TUMOR MARKERS, BIOLOGICAL;

EID: 84904346902     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2014.04.030     Document Type: Article

References (49)

1. Akavia U.D., Litvin O., Kim J., Sanchez-Garcia F., Kotliar D., Causton H.C., Pochanard P., Mozes E., Garraway L.A., Pe'er D. An integrated approach to uncover drivers of cancer. Cell 2010, 143:1005-1017.
2. Alonso S.R., Tracey L., Ortiz P., Pérez-Gómez B., Palacios J., Pollán M., Linares J., Serrano S., Sáez-Castillo A.I., Sánchez L., et al. A high-throughput study in melanoma identifies epithelial-mesenchymal transition as a major determinant of metastasis. Cancer Res. 2007, 67:3450-3460.
3. Barretina J., Caponigro G., Stransky N., Venkatesan K., Margolin A.A., Kim S., Wilson C.J., Lehár J., Kryukov G.V., Sonkin D., et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012, 483:603-607.
4. Bell R.E., Levy C. The three M's: melanoma, microphthalmia-associated transcription factor and microRNA. Pigment Cell Melanoma Res. 2011, 24:1088-1106.
5. Bucci C., Thomsen P., Nicoziani P., McCarthy J., van Deurs B. Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 2000, 11:467-480.
6. Caramel J., Papadogeorgakis E., Hill L., Browne G.J., Richard G., Wierinckx A., Saldanha G., Osborne J., Hutchinson P., Tse G., et al. A switch in the expression of embryonic EMT-inducers drives the development of malignant melanoma. Cancer Cell 2013, 24:466-480.
7. Checinska A., Soengas M.S. The gluttonous side of malignant melanoma: basic and clinical implications of macroautophagy. Pigment Cell Melanoma Res. 2011, 24:1116-1132.
8. 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.
9. Dang C.V. MYC on the path to cancer. Cell 2012, 149:22-35.
10. de Duve C. The lysosome turns fifty. Nat. Cell Biol. 2005, 7:847-849.
11. Doe M.R., Ascano J.M., Kaur M., Cole M.D. Myc posttranscriptionally induces HIF1 protein and target gene expression in normal and cancer cells. Cancer Res. 2012, 72:949-957.
12. Edinger A.L., Cinalli R.M., Thompson C.B. Rab7 prevents growth factor-independent survival by inhibiting cell-autonomous nutrient transporter expression. Dev. Cell 2003, 5:571-582.
13. Garraway L.A., Sellers W.R. Lineage dependency and lineage-survival oncogenes in human cancer. Nat. Rev. Cancer 2006, 6:593-602.
14. Garraway L.A., Lander E.S. Lessons from the cancer genome. Cell 2013, 153:17-37.
15. Goldenring J.R. A central role for vesicle trafficking in epithelial neoplasia: intracellular highways to carcinogenesis. Nat. Rev. Cancer 2013, 13:813-820.
16. Gomez P.F., Luo D., Hirosaki K., Shinoda K., Yamashita T., Suzuki J., Otsu K., Ishikawa K., Jimbow K. Identification of rab7 as a melanosome-associated protein involved in the intracellular transport of tyrosinase-related protein 1. J.Invest. Dermatol. 2001, 117:81-90.
17. Greene M.H., Mead G.D., Reimer R.R., Bergfeld W.F., Fraumeni J.F. Malignant melanoma and Charcot-Marie-Tooth disease. Am. J. Med. Genet. 1980, 5:69-71.
18. Gupta P.B., Kuperwasser C., Brunet J.P., Ramaswamy S., Kuo W.L., Gray J.W., Naber S.P., Weinberg R.A. The melanocyte differentiationprogram predisposes to metastasis after neoplastic transformation. Nat. Genet. 2005, 37:1047-1054.
19. Halaban R., Cheng E., Smicun Y., Germino J. Deregulated E2F transcriptional activity in autonomously growing melanoma cells. J.Exp. Med. 2000, 191:1005-1016.
20. Haq R., Shoag J., Andreu-Perez P., Yokoyama S., Edelman H., Rowe G.C., Frederick D.T., Hurley A.D., Nellore A., Kung A.L., et al. Oncogenic BRAF regulates oxidative metabolism via PGC1α and MITF. Cancer Cell 2013, 23:302-315.
21. Haq R., Yokoyama S., Hawryluk E.B., Jönsson G.B., Frederick D.T., McHenry K., Porter D., Tran T.N., Love K.T., Langer R., et al. BCL2A1 is a lineage-specific antiapoptotic melanoma oncogene that confers resistance to BRAF inhibition. Proc. Natl. Acad. Sci. USA 2013, 110:4321-4326.
22. Hoek K.S., Eichhoff O.M., Schlegel N.C., Döbbeling U., Kobert N., Schaerer L., Hemmi S., Dummer R. Invivo switching of human melanoma cells between proliferative and invasive states. Cancer Res. 2008, 68:650-656.
23. Javelaud D., Alexaki V.I., Pierrat M.J., Hoek K.S., Dennler S., Van Kempen L., Bertolotto C., Ballotti R., Saule S., Delmas V., Mauviel A. GLI2 and M-MITF transcription factors control exclusive gene expression programs and inversely regulate invasion in human melanoma cells. Pigment Cell Melanoma Res. 2011, 24:932-943.
24. Koludrovic D., Davidson I. MITF, the Janus transcription factor of melanoma. Future Oncol. 2013, 9:235-244.
25. Lawrence M.S., Stojanov P., Polak P., Kryukov G.V., Cibulskis K., Sivachenko A., Carter S.L., Stewart C., Mermel C.H., Roberts S.A., et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 2013, 499:214-218.
26. Mason S.D., Joyce J.A. Proteolytic networks in cancer. Trends Cell Biol. 2011, 21:228-237.
27. McCray B.A., Skordalakes E., Taylor J.P. Disease mutations in Rab7 result in unregulated nucleotide exchange and inappropriate activation. Hum. Mol. Genet. 2010, 19:1033-1047.
28. Pinner S., Jordan P., Sharrock K., Bazley L., Collinson L., Marais R., Bonvin E., Goding C., Sahai E. Intravital imaging reveals transient changes in pigment production and Brn2 expression during metastatic melanoma dissemination. Cancer Res. 2009, 69:7969-7977.
29. Polsky D., Cordon-Cardo C. Oncogenes in melanoma. Oncogene 2003, 22:3087-3091.
30. Raposo G., Marks M.S. Melanosomes-dark organelles enlighten endosomal membrane transport. Nat. Rev. Mol. Cell Biol. 2007, 8:786-797.
31. Roesch A., Fukunaga-Kalabis M., Schmidt E.C., Zabierowski S.E., Brafford P.A., Vultur A., Basu D., Gimotty P., Vogt T., Herlyn M. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 2010, 141:583-594.
32. Roy S.G., Stevens M.W., So L., Edinger A.L. Reciprocal effects of rab7 deletion in activated and neglected Tcells. Autophagy 2013, 9:1009-1023.
33. Scherf U., Ross D.T., Waltham M., Smith L.H., Lee J.K., Tanabe L., Kohn K.W., Reinhold W.C., Myers T.G., Andrews D.T., et al. A gene expression database for the molecular pharmacology of cancer. Nat. Genet. 2000, 24:236-244.
34. Settembre C., Di Malta C., Polito V.A., Garcia Arencibia M., Vetrini F., Erdin S., Erdin S.U., Huynh T., Medina D., Colella P., et al. TFEB links autophagy to lysosomal biogenesis. Science 2011, 332:1429-1433.
35. Shakhova O., Zingg D., Schaefer S.M., Hari L., Civenni G., Blunschi J., Claudinot S., Okoniewski M., Beermann F., Mihic-Probst D., et al. Sox10 promotes the formation and maintenance of giant congenital naevi and melanoma. Nat. Cell Biol. 2012, 14:882-890.
36. Shankavaram U.T., Reinhold W.C., Nishizuka S., Major S., Morita D., Chary K.K., Reimers M.A., Scherf U., Kahn A., Dolginow D., et al. Transcript and protein expression profiles of the NCI-60 cancer cell panel: an integromic microarray study. Mol. Cancer Ther. 2007, 6:820-832.
37. Steffan J.J., Cardelli J.A. Thiazolidinediones induce Rab7-RILP-MAPK-dependent juxtanuclear lysosome aggregation and reduce tumor cell invasion. Traffic 2010, 11:274-286.
38. Steffan J.J., Dykes S.S., Coleman D.T., Adams L.K., Rogers D., Carroll J.L., Williams B.J., Cardelli J.A. Supporting a role for the GTPase Rab7 in prostate cancer progression. PLoS ONE 2014, 9:e87882.
39. Thies A., Moll I., Berger J., Wagener C., Brümmer J., Schulze H.J., Brunner G., Schumacher U. CEACAM1 expression in cutaneous malignant melanoma predicts the development of metastatic disease. J.Clin. Oncol. 2002, 20:2530-2536.
40. Thurber A.E., Douglas G., Sturm E.C., Zabierowski S.E., Smit D.J., Ramakrishnan S.N., Hacker E., Leonard J.H., Herlyn M., Sturm R.A. Inverse expression states of the BRN2 and MITF transcription factors in melanoma spheres and tumour xenografts regulate the NOTCH pathway. Oncogene 2011, 30:3036-3048.
41. Tsao H., Chin L., Garraway L.A., Fisher D.E. Melanoma: from mutations to medicine. Genes Dev. 2012, 26:1131-1155.
42. Vazquez F., Lim J.H., Chim H., Bhalla K., Girnun G., Pierce K., Clish C.B., Granter S.R., Widlund H.R., Spiegelman B.M., Puigserver P. PGC1α expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress. Cancer Cell 2013, 23:287-301.
43. Wang T., Ming Z., Xiaochun W., Hong W. Rab7: role of its protein interaction cascades in endo-lysosomal traffic. Cell. Signal. 2011, 23:516-521.
44. Wang T., Zhang M., Ma Z., Guo K., Tergaonkar V., Zeng Q., Hong W. A role of Rab7 in stabilizing EGFR-Her2 and in sustaining Akt survival signal. J.Cell. Physiol. 2012, 227:2788-2797.
45. Widmer D.S., Cheng P.F., Eichhoff O.M., Belloni B.C., Zipser M.C., Schlegel N.C., Javelaud D., Mauviel A., Dummer R., Hoek K.S. Systematic classification of melanoma cells by phenotype-specific gene expression mapping. Pigment Cell Melanoma Res. 2012, 25:343-353.
46. Williams K.C., Coppolino M.G. Phosphorylation of membrane type 1-matrix metalloproteinase (MT1-MMP) and its vesicle-associated membrane protein 7 (VAMP7)-dependent trafficking facilitate cell invasion and migration. J.Biol. Chem. 2011, 286:43405-43416.
47. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2001, 2:107-117.
48. Zhang M., Chen L., Wang S., Wang T. Rab7: roles in membrane trafficking and disease. Biosci. Rep. 2009, 29:193-209.
49. Zhuang D., Mannava S., Grachtchouk V., Tang W.H., Patil S., Wawrzyniak J.A., Berman A.E., Giordano T.J., Prochownik E.V., Soengas M.S., Nikiforov M.A. C-MYC overexpression is required for continuous suppression of oncogene-induced senescence in melanoma cells. Oncogene 2008, 27:6623-6634.