The MITF family of transcription factors: Role in endolysosomal biogenesis, Wnt signaling, and oncogenesis

Pharmacological Research

Volumn 99, Issue , 2015, Pages 36-43

  Ploper, Diego ^a,b   De Robertis, Edward M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chloroquine; GSK3 inhibitors; Lysosome; Melanoma; MITF; Multivesicular bodies; TFE3; TFEB; TFEC; Wnt STOP

Indexed keywords

BAFILOMYCIN A1; BETA CATENIN; CHLOROQUINE; ENZYME INHIBITOR; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; HYDROXYCHLOROQUINE; LY 2090314; LYS 0569; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MONENSIN; MYC PROTEIN; PROTEIN C JUN; TRANSCRIPTION FACTOR E BOX; TRANSCRIPTION FACTOR E3; TRANSCRIPTION FACTOR EC; UNCLASSIFIED DRUG; WNT PROTEIN; WORTMANNIN; ANTINEOPLASTIC AGENT;

ALVEOLAR SOFT PART SARCOMA; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGOSOME; BIOGENESIS; CARCINOGENESIS; ENDOLYSOSOME; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENE TARGETING; HUMAN; KIDNEY CARCINOMA; LYSOSOME MEMBRANE; MACROAUTOPHAGY; MELANOMA; METASTATIC PANCREATIC CANCER; MICROARRAY ANALYSIS; NONHUMAN; PANCREAS CANCER; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; UPREGULATION; WNT SIGNALING PATHWAY; AMINO ACID SEQUENCE; ANIMAL; AUTOPHAGY; BIOLOGICAL MODEL; CHEMISTRY; DRUG EFFECTS; ENDOSOME; GENETICS; LYSOSOME; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; CARCINOGENESIS; ENDOSOMES; GLYCOGEN SYNTHASE KINASE 3; HUMANS; LYSOSOMES; MELANOMA; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; WNT SIGNALING PATHWAY;

EID: 84930664305     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2015.04.006     Document Type: Article

References (99)

1. H. Clevers, and R. Nusse Wnt/β-catenin signaling and disease Cell 149 2012 1192 1205 10.1016/j.cell.2012.05.012
2. H. Hikasa, and S.Y. Sokol Wnt signaling in vertebrate axis specification Cold Spring Harb. Perspect. Biol. 5 2013 a007955 10.1101/cshperspect.a007955
3. J.D. Holland, A. Klaus, A.N. Garratt, and W. Birchmeier Wnt signaling in stem and cancer stem cells Curr. Opin. Cell Biol. 25 2013 254 264 10.1016/j.ceb.2013.01.004
4. J.N. Anastas, and R.T. Moon WNT signalling pathways as therapeutic targets in cancer Nat. Rev. Cancer 13 2013 11 26 10.1038/nrc3419
5. J. Bilić, Y.-L. Huang, G. Davidson, T. Zimmermann, C.-M. Cruciat, and M. Bienz Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation Science 316 2007 1619 1622 10.1126/science.1137065
6. V.F. Taelman, R. Dobrowolski, J.-L. Plouhinec, L.C. Fuentealba, P.P. Vorwald, and I. Gumper Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes Cell 143 2010 1136 1148 10.1016/j.cell.2010.11.034
7. M. Vinyoles, B. Del Valle-Pérez, J. Curto, R. Viñas-Castells, L. Alba-Castellón, and A. García de Herreros Multivesicular GSK3 sequestration upon Wnt signaling is controlled by p120-catenin/cadherin interaction with LRP5/6 Mol. Cell 53 2014 444 457 10.1016/j.molcel.2013.12.010
8. D. Ploper, V.F. Taelman, L. Robert, B.S. Perez, B. Titz, and H.-W. Chen MITF drives endolysosomal biogenesis and potentiates Wnt signaling in melanoma cells Proc. Natl. Acad. Sci. U. S. A. 112 2015 E420 E429 10.1073/pnas.1424576112
9. R. Dobrowolski, and E.M. De Robertis Endocytic control of growth factor signalling: multivesicular bodies as signalling organelles Nat. Rev. Mol. Cell Biol. 13 2011 53 60
10. N.-G. Kim, C. Xu, and B.M. Gumbiner Identification of targets of the Wnt pathway destruction complex in addition to β-catenin Proc. Natl. Acad. Sci. U. S. A. 106 2009 5165 5170
11. S.P. Acebron, E. Karaulanov, B.S. Berger, Y.-L. Huang, and C. Niehrs Mitotic Wnt signaling promotes protein stabilization and regulates cell size Mol. Cell 54 2014 663 674 10.1016/j.molcel.2014.04.014
12. G. Davidson, J. Shen, Y.-L. Huang, Y. Su, E. Karaulanov, and K. Bartscherer Cell cycle control of Wnt receptor activation Dev. Cell 17 2009 788 799 10.1016/j.devcel.2009.11.006
13. E. Steingrímsson, N.G. Copeland, and N.A. Jenkins Melanocytes and the microphthalmia transcription factor network Annu. Rev. Genet. 38 2004 365 411 10.1146/annurev.genet.38.072902.092717
14. S. Carreira, J. Goodall, L. Denat, M. Rodriguez, P. Nuciforo, and K.S. Hoek Mitf regulation of Dia1 controls melanoma proliferation and invasiveness Genes Dev. 20 2006 3426 3439 10.1101/gad.406406
15. T. Strub, S. Giuliano, T. Ye, C. Bonet, C. Keime, and D. Kobi Essential role of microphthalmia transcription factor for DNA replication, mitosis and genomic stability in melanoma Oncogene 30 2011 2319 2332
16. H. Arnheiter, L. Hou, M.-T.T. Nguyen, K. Bismuth, T. Csermely, and H. Murakami MITF - a matter of life and death for developing melanocytes V.J. Hearing, S.P.L. Leong, From Melanocytes to Melanoma: The Progression to Malignancy 2007 Humana Totowa, NJ 27 49
17. T.J. Hemesath, E. Steingrímsson, G. McGill, M.J. Hansen, J. Vaught, and C.A. Hodgkinson Microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family Genes Dev. 8 1994 2770 2780 10.1101/gad.8.22.2770
18. V. Pogenberg, M.H. Ogmundsdottir, K. Bergsteinsdottir, A. Schepsky, B. Phung, and V. Deineko Restricted leucine zipper dimerization and specificity of DNA recognition of the melanocyte master regulator MITF Genes Dev. 26 2012 2647 2658 10.1101/gad.198192.112
19. J. Betschinger, J. Nichols, S. Dietmann, P.D. Corrin, P.J. Paddison, and A. Smith Exit from pluripotency is gated by intracellular redistribution of the bHLH transcription factor Tfe3 Cell 153 2013 335 347 10.1016/j.cell.2013.03.012
20. C. Settembre, and A. Ballabio Lysosomal adaptation: how the lysosome responds to external cues Cold Spring Harb. Perspect. Biol. 2014 a016907
21. R. Haq, and D.E. Fisher Biology and clinical relevance of the micropthalmia family of transcription factors in human cancer J. Clin. Oncol. 29 2011 3474 3482 10.1200/JCO.2010.32.6223
22. J.H. Hallsson, B.S. Haflidadóttir, C. Stivers, W. Odenwald, H. Arnheiter, and F. Pignoni The basic helix-loop-helix leucine zipper transcription factor Mitf is conserved in Drosophila and functions in eye development Genetics 167 2004 233 241
23. P. Hertwig Neue mutationen und kopplungsgruppen bei der hausmaus Z. Indukt. Abstamm. Vererbungsl. 80 1942 220 246
24. K. Takeda, K. Yasumoto, N. Kawaguchi, T. Udono, K. Watanabe, and H. Saito Mitf-D, a newly identified isoform, expressed in the retinal pigment epithelium and monocyte-lineage cells affected by Mitf mutations Biochim. Biophys. Acta: Gene Struct. Expr. 1574 2002 15 23 10.1016/S0167-4781(01)00339-6
25. C.M. Takemoto, Y.-J. Yoon, and D.E. Fisher The identification and functional characterization of a novel mast cell isoform of the microphthalmia-associated transcription factor J. Biol. Chem. 277 2002 30244 30252 10.1074/jbc.M201441200
26. A.P. Read, and V.E. Newton Waardenburg syndrome J. Med. Genet. 34 1997 656 665 10.1136/jmg.34.8.656
27. S.D. Smith, P.M. Kelley, J.B. Kenyon, and D. Hoover Tietz syndrome (hypopigmentation/deafness) caused by mutation of MITF J. Med. Genet. 37 2000 446 448 10.1136/jmg.37.6.446
28. L.A. Garraway, H.R. Widlund, M.A. Rubin, G. Getz, A.J. Berger, and S. Ramaswamy Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma Nature 436 2005 117 122 10.1038/nature03664
29. M. Palmieri, S. Impey, H. Kang, A. di Ronza, C. Pelz, and M. Sardiello Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways Hum. Mol. Genet. 20 2011 3852 3866 10.1093/hmg/ddr306
30. C. Settembre, A. Fraldi, D.L. Medina, and A. Ballabio Signals from the lysosome: a control centre for cellular clearance and energy metabolism Nat. Rev. Mol. Cell Biol. 14 2013 283 296 10.1038/nrm3565
31. M. Sardiello, M. Palmieri, A. di Ronza, D.L. Medina, M. Valenza, and V.A. Gennarino A gene network regulating lysosomal biogenesis and function Science 325 2009 473 477 10.1126/science.1174447
32. C. Settembre, C. Di Malta, V.A. Polito, M.G. Arencibia, F. Vetrini, and S. Erdin TFEB links autophagy to lysosomal biogenesis Science 332 2011 1429 1433 10.1126/science.1204592
33. D.L. Medina, A. Fraldi, V. Bouche, F. Annunziata, G. Mansueto, and C. Spampanato Transcriptional activation of lysosomal exocytosis promotes cellular clearance Dev. Cell 21 2011 421 430 10.1016/j.devcel.2011.07.016
34. C. Settembre, R. De Cegli, G. Mansueto, P.K. Saha, F. Vetrini, and O. Visvikis TFEB controls cellular lipid metabolism through a starvation-induced autoregulatory loop Nat. Cell Biol. 15 2013 647 658 10.1038/ncb2718
35. M. Sardiello, and A. Ballabio Lysosomal enhancement: a CLEAR answer to cellular degradative needs Cell Cycle 8 2009 4021 4022 10.4161/cc.8.24.10263
36. J.A. Martina, H.I. Diab, H. Li, and R. Puertollano Novel roles for the MiTF/TFE family of transcription factors in organelle biogenesis, nutrient sensing, and energy homeostasis Cell. Mol. Life Sci. 71 2014 2483 2497 10.1007/s00018-014-1565-8
37. J.A. Martina, H.I. Diab, L. Lishu, L. Jeong-A, S. Patange, and N. Raben The nutrient-responsive transcription factor TFE3 promotes autophagy, lysosomal biogenesis, and clearance of cellular debris Sci. Signal. 7 2014 ra9 10.1126/scisignal.2004754
38. S.-B. Hong, H. Oh, V.A. Valera, M. Baba, L.S. Schmidt, and W.M. Linehan Inactivation of the FLCN tumor suppressor gene induces TFE3 transcriptional activity by increasing its nuclear localization PLoS ONE 5 2010 e15793 10.1371/journal.pone.0015793
39. M. Rehli, A. Lichanska, A.I. Cassady, M.C. Ostrowski, and D.A. Hume TFEC is a macrophage-restricted member of the microphthalmia-TFE subfamily of basic helix-loop-helix leucine zipper transcription factors J. Immunol. 162 1999 1559 1565
40. G.Q. Zhao, Q. Zhao, X. Zhou, M.G. Mattei, and B. de. Crombrugghe TFEC, a basic helix-loop-helix protein, forms heterodimers with TFE3 and inhibits TFE3-dependent transcription activation Mol. Cell. Biol. 13 1993 4505 4512 10.1128/MCB.13.8.4505
41. M. Rehli, N. Den Elzen, A.I. Cassady, M.C. Ostrowski, and D.A. Hume Cloning and characterization of the murine genes for bHLH-ZIP transcription factors TFEC and TFEB reveal a common gene organization for all MiT subfamily members Genomics 56 1999 111 120 10.1006/geno.1998.5588
42. K. Yasumoto, and S. Shibahara Molecular cloning of cDNA encoding a human TFEC isoform, a newly identified transcriptional regulator Biochim. Biophys. Acta 1353 1997 23 31
43. J.A. Martina, and R. Puertollano Rag GTPases mediate amino acid-dependent recruitment of TFEB and MITF to lysosomes J. Cell Biol. 200 2013 475 491 10.1083/jcb.201209135
44. A. Efeyan, W.C. Comb, and D.M. Sabatini Nutrient sensing mechanisms and pathways Nature 517 2015 302 310 10.1038/nature14190
45. C. Settembre, R. Zoncu, D.L. Medina, F. Vetrini, S. Erdin, and S. Erdin A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB EMBO J. 31 2012 1095 1108 10.1038/emboj.2012.32
46. A. Roczniak-Ferguson, C.S. Petit, F. Froehlich, S. Qian, J. Ky, and B. Angarola The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis Sci. Signal. 5 2012 ra42
47. A. Bronisz, S.M. Sharma, R. Hu, J. Godlewski, G. Tzivion, and K.C. Mansky Microphthalmia-associated transcription factor interactions with 14-3-3 modulate differentiation of committed myeloid precursors Mol. Biol. Cell 17 2006 3897 3906
48. A. Subramanian, P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, and M.A. Gillette Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. U. S. A. 102 2005 15545 15550 10.1073/pnas.0506580102
49. I. Aksan, and C.R. Goding Targeting the microphthalmia basic helix-loop-helix-leucine zipper transcription factor to a subset of E-Box elements in vitro and in vivo Mol. Cell. Biol. 18 1998 6930 6938
50. K.S. Hoek, N.C. Schlegel, O.M. Eichhoff, D.S. Widmer, C. Praetorius, and S.O. Einarsson Novel MITF targets identified using a two-step DNA microarray strategy Pigment Cell Melanoma Res. 21 2008 665 676 10.1111/j.1755-148X.2008.00505.x
51. A. Luchin, G. Purdom, K. Murphy, M.-Y. Clark, N. Angel, and A.I. Cassady The Microphthalmia transcription factor regulates expression of the tartrate-resistant acid phosphatase gene during terminal differentiation of osteoclasts J. Bone Miner. Res. 15 2000 451 460
52. N.A. Meadows, S.M. Sharma, G.J. Faulkner, M.C. Ostrowski, D.A. Hume, and A.I. Cassady The expression of Clcn7 and Ostm1 in osteoclasts is coregulated by microphthalmia transcription factor J. Biol. Chem. 282 2007 1891 1904 10.1074/jbc.M608572200
53. G. Motyckova, K.N. Weilbaecher, M. Horstmann, D.J. Rieman, D.Z. Fisher, and D.E. Fisher Linking osteopetrosis and pycnodysostosis: regulation of cathepsin K expression by the microphthalmia transcription factor family Proc. Natl. Acad. Sci. U. S. A. 98 2001 5798 5803
54. T. Lübke, P. Lobel, and D.E. Sleat Proteomics of the lysosome Biochim. Biophys. Acta: Mol. Cell Res. 1793 2009 625 635 10.1016/j.bbamcr.2008.09.018
55. A. Chi, J.C. Valencia, Z.-Z. Hu, H. Watabe, H. Yamaguchi, and N.J. Mangini Proteomic and bioinformatic characterization of the biogenesis and function of melanosomes J. Proteome Res. 5 2006 3135 3144 10.1021/pr060363j
56. G. Raposo, D. Tenza, D.M. Murphy, J.F. Berson, and M.S. Marks Distinct protein sorting and localization to premelanosomes, melanosomes, and lysosomes in pigmented melanocytic cells J. Cell Biol. 152 2001 809 824
57. G. Raposo, and M.S. Marks Melanosomes - dark organelles enlighten endosomal membrane transport Nat. Rev. Mol. Cell Biol. 8 2007 786 797 10.1038/nrm2258
58. E. Steingrímsson, L. Tessarollo, B. Pathak, L. Hou, H. Arnheiter, and N.G. Copeland Mitf and Tfe3, two members of the Mitf-Tfe family of bHLH-Zip transcription factors, have important but functionally redundant roles in osteoclast development Proc. Natl. Acad. Sci. U. S. A. 99 2002 4477 4482 10.1073/pnas.072071099
59. B. Gunawan, A. von Heydebreck, T. Fritsch, W. Huber, R.-H. Ringert, and G. Jakse Cytogenetic and morphologic typing of 58 papillary renal cell carcinomas evidence for a cytogenetic evolution of Type 2 from Type 1 tumors Cancer Res. 63 2003 6200 6205
60. R. Ramphal, A. Pappo, M. Zielenska, R. Grant, and B.-Y. Ngan Pediatric renal cell carcinoma clinical, pathologic, and molecular abnormalities associated with the members of the MiT transcription factor family Am. J. Clin. Pathol. 126 2006 349 364 10.1309/98YE9E442AR7LX2X
61. L.A. Garraway, and E.S. Lander Lessons from the cancer genome Cell 153 2013 17 37 10.1016/j.cell.2013.03.002
62. S. Yokoyama, S.L. Woods, G.M. Boyle, L.G. Aoude, S. MacGregor, and V. Zismann A novel recurrent mutation in MITF predisposes to familial and sporadic melanoma Nature 480 2011 99 103 10.1038/nature10630
63. C. Bertolotto, F. Lesueur, S. Giuliano, T. Strub, M. de Lichy, and K. Bille A SUMOylation-defective MITF germline mutation predisposes to melanoma and renal carcinoma Nature 480 2011 94 98 10.1038/nature10539
64. J. Zucman, O. Delattre, C. Desmaze, A.L. Epstein, G. Stenman, and F. Speleman EWS and ATF-1 gene fusion induced by t(12;22) translocation in malignant melanoma of soft parts Nat. Genet. 4 1993 341 345 10.1038/ng0893-341
65. I.J. Davis, J.J. Kim, F. Ozsolak, H.R. Widlund, O. Rozenblatt-Rosen, and S.R. Granter Oncogenic MITF dysregulation in clear cell sarcoma: defining the MiT family of human cancers Cancer Cell 9 2006 473 484 10.1016/j.ccr.2006.04.021
66. D. Alonso-Curbelo, E. Riveiro-Falkenbach, E. Pérez-Guijarro, M. Cifdaloz, P. Karras, and L. Osterloh RAB7 controls melanoma progression by exploiting a lineage-specific wiring of the endolysosomal pathway Cancer Cell 26 2014 61 76 10.1016/j.ccr.2014.04.030
67. R.P. Kuiper, M. Schepens, J. Thijssen, M. van Asseldonk, E. van den Berg, and J. Bridge Upregulation of the transcription factor TFEB in t(6;11)(p21;q13)-positive renal cell carcinomas due to promoter substitution Hum. Mol. Genet. 12 2003 1661 1669 10.1093/hmg/ddg178
68. B. Marchand, D. Arsenault, A. Raymond-Fleury, F.-M. Boisvert, and M.-J. Boucher Glycogen Synthase Kinase-3 (GSK3) inhibition induces prosurvival autophagic signals in human pancreatic cancer cells J. Biol. Chem. 290 2015 5592 5605 10.1074/jbc.M114.616714
69. T. Kallunki, O.D. Olsen, and M. Jäättelä Cancer-associated lysosomal changes: friends or foes? Oncogene 32 2012 1995 2004
70. C. Bucci, P. Thomsen, P. Nicoziani, J. McCarthy, and B. van Deurs Rab7: a key to lysosome biogenesis Mol. Biol. Cell 11 2000 467 480
71. M. Zerial, and H. McBride Rab proteins as membrane organizers Nat. Rev. Mol. Cell Biol. 2 2001 107 117 10.1038/35052055
72. M. Zhang, L. Chen, S. Wang, and T. Wang Rab7: roles in membrane trafficking and disease Biosci. Rep. 29 2009 193 10.1042/BSR20090032
73. N. Mizushima, and M. Komatsu Autophagy renovation of cells and tissues Cell 147 2011 728 741 10.1016/j.cell.2011.10.026
74. J. Kubisch, D. Türei, L. Földvári-Nagy, Z.A. Dunai, L. Zsákai, and M. Varga Complex regulation of autophagy in cancer - integrated approaches to discover the networks that hold a double-edged sword Semin. Cancer Biol. 23 2013 252 261 10.1016/j.semcancer.2013.06.009
75. L. Galluzzi, F. Pietrocola, J.M.B.-S. Pedro, R.K. Amaravadi, E.H. Baehrecke, and F. Cecconi Autophagy in malignant transformation and cancer progression EMBO J. 2015 e201490784 10.15252/embj.201490784
76. E. White Deconvoluting the context-dependent role for autophagy in cancer Nat. Rev. Cancer 12 2012 401 410 10.1038/nrc3262
77. E. White The role for autophagy in cancer J. Clin. Invest. 125 2015 42 46 10.1172/JCI73941
78. N. Mizushima Autophagy: process and function Genes Dev. 21 2007 2861 2873 10.1101/gad.1599207
79. H. Liu, Z. He, T. von Rütte, S. Yousefi, R.E. Hunger, and H.-U. Simon Down-regulation of autophagy-related protein 5 (ATG5) contributes to the pathogenesis of early-stage cutaneous melanoma Sci. Transl. Med. 5 2013 202ra123 10.1126/scitranslmed.3005864
80. H. Liu, Z. He, and H.-U. Simon Autophagy suppresses melanoma tumorigenesis by inducing senescence Autophagy 10 2014 372 373 10.4161/auto.27163
81. H. Liu, Z. He, and H.-U. Simon Protective role of autophagy and autophagy-related protein 5 in early tumorigenesis J. Mol. Med. 93 2014 159 164 10.1007/s00109-014-1241-3
82. S. Giuliano, Y. Cheli, M. Ohanna, C. Bonet, L. Beuret, and K. Bille Microphthalmia-associated transcription factor controls the DNA damage response and a lineage-specific senescence program in melanomas Cancer Res. 70 2010 3813 3822 10.1158/0008-5472.CAN-09-2913
83. S. Giuliano, M. Ohanna, R. Ballotti, and C. Bertolotto Advances in melanoma senescence and potential clinical application: senescence in melanoma cells Pigment Cell Melanoma Res. 24 2011 295 308 10.1111/j.1755-148X.2010.00820.x
84. T.L. Biechele, R.M. Kulikauskas, R.A. Toroni, O.M. Lucero, R.D. Swift, and R.G. James Wnt/β-catenin signaling and AXIN1 regulate apoptosis triggered by inhibition of the mutant kinase BRAFV600E in human melanoma Sci. Signal. 5 2012 ra3 10.1126/scisignal.2002274
85. K.V. Rote, and M. Rechsteiner Degradation of microinjected proteins: effects of lysosomotropic agents and inhibitors of autophagy J. Cell. Physiol. 116.1 1983 103 110
86. R. Dobrowolski, P. Vick, D. Ploper, I. Gumper, H. Snitkin, and D.D. Sabatini Presenilin deficiency or lysosomal inhibition enhances Wnt signaling through relocalization of GSK3 to the late-endosomal compartment Cell Rep. 2 2012 1316 1328 10.1016/j.celrep.2012.09.026
87. G. Manic, F. Obrist, G. Kroemer, I. Vitale, and L. Galluzzi Chloroquine and hydroxychloroquine for cancer therapy Mol. Cell. Oncol. 1 2014 e29911 10.4161/mco.29911
88. X.H. Liang, S. Jackson, M. Seaman, K. Brown, B. Kempkes, and H. Hibshoosh Induction of autophagy and inhibition of tumorigenesis by beclin 1 Nature 402 1999 672 676 10.1038/45257
89. X. Qu, J. Yu, G. Bhagat, N. Furuya, H. Hibshoosh, and A. Troxel Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene J. Clin. Invest. 112 2003 1809 1820 10.1172/JCI20039
90. Z. Yue, S. Jin, C. Yang, A.J. Levine, and N. Heintz Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor Proc. Natl. Acad. Sci. U. S. A. 100 2003 15077 15082 10.1073/pnas.2436255100
91. A. Maria Cuervo Autophagy: in sickness and in health Trends Cell Biol. 14 2004 70 77 10.1016/j.tcb.2003.12.002
92. M. Corazzari, G.M. Fimia, P. Lovat, and M. Piacentini Why is autophagy important for melanoma? Molecular mechanisms and therapeutic implications Semin. Cancer Biol. 23 2013 337 343 10.1016/j.semcancer.2013.07.001
93. C. Wellbrock, and I. Arozarena MITF in melanoma development and MAP-kinase pathway targeted therapy Pigment Cell Melanoma Res. 2015 10.1111/pcmr.12370
94. K.S. Hoek, O.M. Eichhoff, N.C. Schlegel, U. Döbbeling, N. Kobert, and L. Schaerer In vivo switching of human melanoma cells between proliferative and invasive states Cancer Res. 68 2008 650 656
95. M. Sáez-Ayala, M.F. Montenegro, L. Sánchez-del-Campo, M.P. Fernández-Pérez, S. Chazarra, and R. Freter Directed phenotype switching as an effective antimelanoma strategy Cancer Cell 24 2013 105 119 10.1016/j.ccr.2013.05.009
96. K. Takeda, K. Yasumoto, R. Takada, S. Takada, K. Watanabe, and T. Udono Induction of melanocyte-specific microphthalmia-associated transcription factor by Wnt-3a J. Biol. Chem. 275 2000 14013 14016
97. J.A. McCubrey, L.S. Steelman, F.E. Bertrand, N.M. Davis, M. Sokolosky, and S.L. Abrams GSK-3 as potential target for therapeutic intervention in cancer Oncotarget 5 2014 2881 2911
98. K. Miyashita, M. Nakada, A. Shakoori, Y. Ishigaki, T. Shimasaki, and Y. Motoo An emerging strategy for cancer treatment targeting aberrant glycogen synthase kinase 3 beta Anti-Cancer Agents Med. Chem. 9 2009 1114 1122 10.2174/187152009789734982
99. K.T. Flaherty, F.S. Hodi, and D.E. Fisher From genes to drugs: targeted strategies for melanoma Nat. Rev. Cancer 12 2012 349 361 10.1038/nrc3218