Interactions of Melanoma Cells with Distal Keratinocytes Trigger Metastasis via Notch Signaling Inhibition of MITF

Molecular Cell

Volumn 59, Issue 4, 2015, Pages 664-676

  Golan, Tamar ^a   Messer, Arielle R ^a   Amitai Lange, Aya ^b   Melamed, Ze'ev ^a   Ohana, Reut ^a   Bell, Rachel E ^a   Kapitansky, Oxana ^a   Lerman, Galya ^c   Greenberger, Shoshana ^d   Khaled, Mehdi ^e   Amar, Nira ^a   Albrengues, Jean ^f   Gaggioli, Cedric ^f   Gonen, Pinchas ^a   Tabach, Yuval ^g   Sprinzak, David ^a   Shalom Feuerstein, Ruby ^b   Levy, Carmit ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c Cancer Research Center   (Israel)

^d SHEBA MEDICAL CENTER   (Israel)

^e INSTITUT GUSTAVE ROUSSY   (France)

^f UNIVERSITÉ CÔTE D'AZUR   (France)

^g HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MICRORNA 221; MICRORNA 222; NOTCH RECEPTOR; MICRORNA; MIRN221 MICRORNA, HUMAN; MIRN222 MICRORNA, HUMAN; MITF PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ARTICLE; CANCER GROWTH; CELL DIFFERENTIATION; CELL INVASION; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; KERATINOCYTE; MELANOMA CELL; MELANOMA CELL LINE; MELANOMA METASTASIS; MICROENVIRONMENT; MOUSE; NONHUMAN; NORMAL HUMAN; PROMOTER REGION; REPORTER GENE; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BINDING SITE; CANCER TRANSPLANTATION; CELL COMMUNICATION; COCULTURE; EXPERIMENTAL MELANOMA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NONOBESE DIABETIC MOUSE; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHYSIOLOGY; RNA INTERFERENCE; SCID MOUSE; SECONDARY; SKIN TUMOR; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL COMMUNICATION; CELL LINE, TUMOR; COCULTURE TECHNIQUES; GENE EXPRESSION REGULATION, NEOPLASTIC; KERATINOCYTES; MELANOMA, EXPERIMENTAL; MICE, INBRED NOD; MICE, SCID; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; PROMOTER REGIONS, GENETIC; RECEPTORS, NOTCH; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKIN NEOPLASMS;

EID: 84939575032     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.06.028     Document Type: Article

References (38)

1. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
2. Balint K., Xiao M., Pinnix C.C., Soma A., Veres I., Juhasz I., Brown E.J., Capobianco A.J., Herlyn M., Liu Z.J. Activation of Notch1 signaling is required for beta-catenin-mediated human primary melanoma progression. J. Clin. Invest. 2005, 115:3166-3176.
3. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
4. Bell R.E., Khaled M., Netanely D., Schubert S., Golan T., Buxbaum A., Janas M.M., Postolsky B., Goldberg M.S., Shamir R., Levy C. Transcription factor/microRNA axis blocks melanoma invasion program by miR-211 targeting NUAK1. J. Invest. Dermatol. 2014, 134:441-451.
5. Carreira S., Goodall J., Denat L., Rodriguez M., Nuciforo P., Hoek K.S., Testori A., Larue L., Goding C.R. Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. Genes Dev. 2006, 20:3426-3439.
6. Chang P.J., Boonsiri J., Wang S.S., Chen L.Y., Miller G. Binding of RBP-Jkappa (CSL) protein to the promoter of the Kaposi's sarcoma-associated herpesvirus ORF47 (gL) gene is a critical but not sufficient determinant of transactivation by ORF50 protein. Virology 2010, 398:38-48.
7. Dynek J.N., Chan S.M., Liu J., Zha J., Fairbrother W.J., Vucic D. Microphthalmia-associated transcription factor is a critical transcriptional regulator of melanoma inhibitor of apoptosis in melanomas. Cancer Res. 2008, 68:3124-3132.
8. Edgar R., Domrachev M., Lash A.E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30:207-210.
9. Felicetti F., Errico M.C., Segnalini P., Mattia G., Carè A. MicroRNA-221 and -222 pathway controls melanoma progression. Expert Rev. Anticancer Ther. 2008, 8:1759-1765.
10. Fuchs E. Scratching the surface of skin development. Nature 2007, 445:834-842.
11. Gaggioli C., Sahai E. Melanoma invasion - current knowledge and future directions. Pigment Cell Res. 2007, 20:161-172.
12. 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.
13. Guruharsha K.G., Kankel M.W., Artavanis-Tsakonas S. The Notch signalling system: recent insights into the complexity of a conserved pathway. Nat. Rev. Genet. 2012, 13:654-666.
14. Hoek K., Rimm D.L., Williams K.R., Zhao H., Ariyan S., Lin A., Kluger H.M., Berger A.J., Cheng E., Trombetta E.S., et al. Expression profiling reveals novel pathways in the transformation of melanocytes to melanomas. Cancer Res. 2004, 64:5270-5282.
15. Howard J.D., Moriarty W.F., Park J., Riedy K., Panova I.P., Chung C.H., Suh K.Y., Levchenko A., Alani R.M. Notch signaling mediates melanoma-endothelial cell communication and melanoma cell migration. Pigment Cell Melanoma Res 2013, 26:697-707.
16. Hsu M.Y., Meier F., Herlyn M. Melanoma development and progression: a conspiracy between tumor and host. Differentiation 2002, 70:522-536.
17. Klose R.J., Yan Q., Tothova Z., Yamane K., Erdjument-Bromage H., Tempst P., Gilliland D.G., Zhang Y., Kaelin W.G. The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell 2007, 128:889-900.
18. Levy C., Fisher D.E. Dual roles of lineage restricted transcription factors: the case of MITF in melanocytes. Transcription 2011, 2:19-22.
19. Levy C., Khaled M., Fisher D.E. MITF: master regulator of melanocyte development and melanoma oncogene. Trends Mol. Med. 2006, 12:406-414.
20. Levy C., Khaled M., Iliopoulos D., Janas M.M., Schubert S., Pinner S., Chen P.H., Li S., Fletcher A.L., Yokoyama S., et al. Intronic miR-211 assumes the tumor suppressive function of its host gene in melanoma. Mol. Cell 2010, 40:841-849.
21. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
22. Liefke R., Oswald F., Alvarado C., Ferres-Marco D., Mittler G., Rodriguez P., Dominguez M., Borggrefe T. Histone demethylase KDM5A is an integral part of the core Notch-RBP-J repressor complex. Genes Dev. 2010, 24:590-601.
23. Lin W.M., Baker A.C., Beroukhim R., Winckler W., Feng W., Marmion J.M., Laine E., Greulich H., Tseng H., Gates C., et al. Modeling genomic diversity and tumor dependency in malignant melanoma. Cancer Res. 2008, 68:664-673.
24. Osawa M., Fisher D.E. Notch and melanocytes: diverse outcomes from a single signal. J. Invest. Dermatol. 2008, 128:2571-2574.
25. Ozsolak F., Song J.S., Liu X.S., Fisher D.E. High-throughput mapping of the chromatin structure of human promoters. Nat. Biotechnol. 2007, 25:244-248.
26. Ozsolak F., Poling L.L., Wang Z., Liu H., Liu X.S., Roeder R.G., Zhang X., Song J.S., Fisher D.E. Chromatin structure analyses identify miRNA promoters. Genes Dev. 2008, 22:3172-3183.
27. 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.
28. Pinnix C.C., Herlyn M. The many faces of Notch signaling in skin-derived cells. Pigment Cell Res. 2007, 20:458-465.
29. Satyamoorthy K., Li G., Vaidya B., Patel D., Herlyn M. Insulin-like growth factor-1 induces survival and growth of biologically early melanoma cells through both the mitogen-activated protein kinase and beta-catenin pathways. Cancer Res. 2001, 61:7318-7324.
30. Smith A.P., Hoek K., Becker D. Whole-genome expression profiling of the melanoma progression pathway reveals marked molecular differences between nevi/melanoma in situ and advanced-stage melanomas. Cancer Biol. Ther. 2005, 4:1018-1029.
31. Sprinzak D., Lakhanpal A., Lebon L., Santat L.A., Fontes M.E., Anderson G.A., Garcia-Ojalvo J., Elowitz M.B. Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 2010, 465:86-90.
32. Stinson S., Lackner M.R., Adai A.T., Yu N., Kim H.J., O'Brien C., Spoerke J., Jhunjhunwala S., Boyd Z., Januario T., et al. TRPS1 targeting by miR-221/222 promotes the epithelial-to-mesenchymal transition in breast cancer. Sci. Signal. 2011, 4:ra41.
33. Tabach Y., Golan T., Hernández-Hernández A., Messer A.R., Fukuda T., Kouznetsova A., Liu J.G., Lilienthal I., Levy C., Ruvkun G. Human disease locus discovery and mapping to molecular pathways through phylogenetic profiling. Mol. Syst. Biol. 2013, 9:692.
34. 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.
35. Van Kilsdonk J.W., Bergers M., Van Kempen L.C., Schalkwijk J., Swart G.W. Keratinocytes drive melanoma invasion in a reconstructed skin model. Melanoma Res. 2010, 20:372-380.
36. Vecchione A., Marchese A., Henry P., Rotin D., Morrione A. The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor. Mol. Cell. Biol. 2003, 23:3363-3372.
37. Watt F.M., Estrach S., Ambler C.A. Epidermal Notch signalling: differentiation, cancer and adhesion. Curr. Opin. Cell Biol. 2008, 20:171-179.
38. Zhao J.J., Lin J., Yang H., Kong W., He L., Ma X., Coppola D., Cheng J.Q. MicroRNA-221/222 negatively regulates estrogen receptor alpha and is associated with tamoxifen resistance in breast cancer. J. Biol. Chem. 2008, 283:31079-31086.