Hypoxia-induced transcriptional repression of the melanoma-associated oncogene MITF

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 43, 2011, Pages

  Feige, Erez ^a,e   Yokoyama, Satoru ^a,b,f   Levy, Carmit ^a,b,g   Khaled, Mehdi ^a,b   Igras, Vivien ^a,b   Lin, Richard J ^a,h   Lee, Stephen ^c   Widlund, Hans R ^a,d   Granter, Scott R ^d   Kung, Andrew L ^a   Fisher, David E ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF OTTAWA   (Canada)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e VBL Therapeutics   (Israel)

^f UNIVERSITY OF TOYAMA   (Japan)

^g TEL AVIV UNIVERSITY   (Israel)

^h WEILL CORNELL MEDICAL CENTER   (United States)

Author keywords

Cancer; Pigmentation; Signal transduction

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DEC1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL HYPOXIA; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; GENE AMPLIFICATION; GENETIC ASSOCIATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MELANOMA; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANALYSIS OF VARIANCE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; CELL HYPOXIA; CHROMATIN IMMUNOPRECIPITATION; DNA PRIMERS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; IMMUNOHISTOCHEMISTRY; MELANOCYTES; MELANOMA; MICE; MICE, NUDE; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; PLASMIDS; REAL-TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

EID: 80055074901     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1106351108     Document Type: Article

References (59)

1. Steingrímsson E, Copeland NG, Jenkins NA (2004) Melanocytes and the microphthalmia transcription factor network. Annu Rev Genet 38:365-411. (Pubitemid 40013733)
2. Levy C, Khaled M, Fisher DE (2006) MITF: Master regulator of melanocyte development and melanoma oncogene. Trends Mol Med 12:406-414. (Pubitemid 44291572)
3. Hughes AE, Newton VE, Liu XZ, Read AP (1994) A gene for Waardenburg syndrome type 2 maps close to the human homologue of the microphthalmia gene at chromosome 3p12-p14.1. Nat Genet 7:509-512. (Pubitemid 24308338)
4. Tassabehji M, Newton VE, Read AP (1994) Waardenburg syndrome type 2 caused by mutations in the human microphthalmia (MITF) gene. Nat Genet 8:251-255. (Pubitemid 24338736)
5. Tachibana M (1997) Evidence to suggest that expression of MITF induces melanocyte differentiation and haploinsufficiency of MITF causes Waardenburg syndrome type 2A. Pigment Cell Res 10:25-33.
6. Steingrímsson E, et al. (1994) Molecular basis of mouse microphthalmia (mi) mutations helps explain their developmental and phenotypic consequences. Nat Genet 8:256-263. (Pubitemid 24338737)
7. Hodgkinson CA, et al. (1993) Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix-loop-helix- zipper protein. Cell 74:395-404. (Pubitemid 23221714)
8. Nishimura EK, Granter SR, Fisher DE (2005) Mechanisms of hair graying: Incomplete melanocyte stem cell maintenance in the niche. Science 307:720-724. (Pubitemid 40194641)
9. Levy C, et al. (2010) Lineage-specific transcriptional regulation of DICER by MITF in melanocytes. Cell 141:994-1005.
10. Khaled M, Levy C, Fisher DE (2010) Control of melanocyte differentiation by a MITF-PDE4D3 homeostatic circuit. Genes Dev 24:2276-2281.
11. Levy C, Fisher DE (2011) Dual roles of lineage restricted transcription factors: The case of MITF in melanocytes. Transcr 2:19-22.
12. Hemesath TJ, et al. (1994) microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family. Genes Dev 8:2770-2780. (Pubitemid 24375425)
13. Argani P, et al. (2003) A novel CLTC-TFE3 gene fusion in pediatric renal adenocarcinoma with t(X;17)(p11.2;q23). Oncogene 22:5374-5378. (Pubitemid 37056101)
14. Heimann P, et al. (2001) Fusion of a novel gene, RCC17, to the TFE3 gene in t(X;17)(p11.2;q25.3)-bearing papillary renal cell carcinomas. Cancer Res 61:4130-4135. (Pubitemid 32720981)
15. Ladanyi M, et al. (2001) The der(17)t(X;17)(p11;q25) of human alveolar soft part sarcoma fuses the TFE3 transcription factor gene to ASPL, a novel gene at 17q25. Oncogene 20:48-57. (Pubitemid 32142337)
16. Clark J, et al. (1997) Fusion of splicing factor genes PSF and NonO (p54nrb) to the TFE3 gene in papillary renal cell carcinoma. Oncogene 15:2233-2239. (Pubitemid 27493913)
17. Weterman MA, Wilbrink M, Geurts van Kessel A (1996) Fusion of the transcription factor TFE3 gene to a novel gene, PRCC, in t(X;1)(p11;q21)- positive papillary renal cell carcinomas. Proc Natl Acad Sci USA 93:15294-15298.
18. Kuiper RP, et al. (2003) Upregulation of the transcription factor TFEB in t(6;11)(p21;q13)-positive renal cell carcinomas due to promoter substitution. Hum Mol Genet 12:1661-1669. (Pubitemid 36896659)
19. Davis IJ, et al. (2003) Cloning of an Alpha-TFEB fusion in renal tumors harboring the t(6;11)(p21;q13) chromosome translocation. Proc Natl Acad Sci USA 100:6051-6056. (Pubitemid 36576929)
20. Garraway LA, et al. (2005) Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436:117-122. (Pubitemid 40966196)
21. Davis IJ, et al. (2006) Oncogenic MITF dysregulation in clear cell sarcoma: Defining the MiT family of human cancers. Cancer Cell 9:473-484. (Pubitemid 43832189)
22. Giordano FJ, Johnson RS (2001) Angiogenesis: The role of the microenvironment in flipping the switch. Curr Opin Genet Dev 11:35-40. (Pubitemid 32119275)
23. Covello KL, Simon MC (2004) HIFs, hypoxia, and vascular development. Curr Top Dev Biol 62:37-54. (Pubitemid 39752374)
24. Kaelin WG (2005) Proline hydroxylation and gene expression. Annu Rev Biochem 74:115-128.
25. Ivan M, et al. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464-468. (Pubitemid 32335941)
26. Jaakkola P, et al. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292:468-472. (Pubitemid 32335942)
27. Yu F, White SB, Zhao Q, Lee FS (2001) HIF-1alpha binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc Natl Acad Sci USA 98:9630-9635. (Pubitemid 32769354)
28. Bruick RK, McKnight SL (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294:1337-1340. (Pubitemid 33063099)
29. Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5:343-354. (Pubitemid 38579472)
30. Chi JT, et al. (2006) Gene expression programs in response to hypoxia: Cell type specificity and prognostic significance in human cancers. PLoS Med 3:e47.
31. Manalo DJ, et al. (2005) Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105:659-669. (Pubitemid 40070750)
32. Paul SA, Simons JW, Mabjeesh NJ (2004) HIF at the crossroads between ischemia and carcinogenesis. J Cell Physiol 200:20-30. (Pubitemid 38720618)
33. King R, et al. (1999) Microphthalmia transcription factor. A sensitive and specific melanocyte marker for melanoma diagnosis. Am J Pathol 155:731-738. (Pubitemid 29426819)
34. Du J, et al. (2003) MLANA/MART1 and SILV/PMEL17/GP100 are transcriptionally regulated by MITF in melanocytes and melanoma. Am J Pathol 163:333-343. (Pubitemid 36759618)
35. Dorvault CC, et al. (2001) Microphthalmia transcription factor: A sensitive and specific marker for malignant melanoma in cytologic specimens. Cancer 93:337-343. (Pubitemid 32995218)
36. Salti GI, et al. (2000) Micropthalmia transcription factor: a new prognostic marker in intermediate-thickness cutaneous malignant melanoma. Cancer Res 60:5012-5016.
37. Granter SR, Weilbaecher KN, Quigley C, Fisher DE (2002) Role for microphthalmia transcription factor in the diagnosis of metastatic malignant melanoma. Appl Immunohistochem Mol Morphol 10:47-51. (Pubitemid 34178276)
38. Lin WM, et al. (2008) Modeling genomic diversity and tumor dependency in malignant melanoma. Cancer Res 68:664-673. (Pubitemid 351206741)
39. Wykoff CC, Pugh CW, Maxwell PH, Harris AL, Ratcliffe PJ (2000) Identification of novel hypoxia dependent and independent target genes of the von Hippel-Lindau (VHL) tumour suppressor by mRNA differential expression profiling. Oncogene 19:6297-6305. (Pubitemid 32641843)
40. Yoon DY, et al. (2001) Identification of genes differentially induced by hypoxia in pancreatic cancer cells. Biochem Biophys Res Commun 288:882-886. (Pubitemid 33140965)
41. Yun Z, Maecker HL, Johnson RS, Giaccia AJ (2002) Inhibition of PPAR gamma 2 gene expression by the HIF-1-regulated gene DEC1/Stra13: A mechanism for regulation of adipogenesis by hypoxia. Dev Cell 2:331-341. (Pubitemid 34266118)
42. Groulx I, Lee S (2002) Oxygen-dependent ubiquitination and degradation of hypoxia-inducible factor requires nuclear-cytoplasmic trafficking of the von Hippel-Lindau tumor suppressor protein. Mol Cell Biol 22:5319-5336. (Pubitemid 34755745)
43. Turley H, et al. (2004) The hypoxia-regulated transcription factor DEC1 (Stra13, SHARP-2) and its expression in human tissues and tumours. J Pathol 203:808-813. (Pubitemid 38961567)
44. Chakrabarti J, et al. (2004) The transcription factor DEC1 (stra13, SHARP2) is associated with the hypoxic response and high tumour grade in human breast cancers. Br J Cancer 91:954-958. (Pubitemid 39273790)
45. Yunokawa M, et al. (2007) Differential regulation of DEC2 among hypoxia-inducible genes in endometrial carcinomas. Oncol Rep 17:871-878.
46. Katoh M, Katoh M (2007) Integrative genomic analyses on HES/HEY family: Notch-independent HES1, HES3 transcription in undifferentiated ES cells, and Notch-dependent HES1, HES5, HEY1, HEY2, HEYL transcription in fetal tissues, adult tissues, or cancer. Int J Oncol 31:461-466.
47. Olbryt M, et al. (2006) Gene expression profile of B 16(F10) murine melanoma cells exposed to hypoxic conditions in vitro. Gene Expr 13:191-203. (Pubitemid 351426384)
48. Shen M, et al. (2001) Induction of basic helix-loop-helix protein DEC1 (BHLHB2)/Stra13/Sharp2 in response to the cyclic adenosine monophosphate pathway. Eur J Cell Biol 80:329-334. (Pubitemid 32514827)
49. Li Y, et al. (2002) Abundant expression of Dec1/stra13/sharp2 in colon carcinoma: Its antagonizing role in serum deprivation-induced apoptosis and selective inhibition of procaspase activation. Biochem J 367:413-422. (Pubitemid 35216815)
50. Buscà R, et al. (2005) Hypoxia-inducible factor 1alpha is a new target of microphthalmia-associated transcription factor (MITF) in melanoma cells. J Cell Biol 170:49-59. (Pubitemid 40994095)
51. Eichhoff OM, et al. (2010) The immunohistochemistry of invasive and proliferative phenotype switching in melanoma: A case report. Melanoma Res 20:349-355.
52. Bedogni B, et al. (2005) The hypoxic microenvironment of the skin contributes to Akt-mediated melanocyte transformation. Cancer Cell 8:443-454. (Pubitemid 41773448)
53. Hershey CL, Fisher DE (2005) Genomic analysis of the Microphthalmia locus and identification of the MITF-J/Mitf-J isoform. Gene 347:73-82. (Pubitemid 40348702)
54. Du J, et al. (2004) Critical role of CDK2 for melanoma growth linked to its melanocyte-specific transcriptional regulation by MITF. Cancer Cell 6:565-576. (Pubitemid 40017700)
55. Widlund HR, Fisher DE (2003) Microphthalamia-associated transcription factor: a critical regulator of pigment cell development and survival. Oncogene 22:3035-3041. (Pubitemid 36713753)
56. McGill GG, et al. (2002) Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell 109:707-718. (Pubitemid 34722267)
57. von Willebrand M, Zacksenhaus E, Cheng E, Glazer P, Halaban R (2003) The tyrphostin AG1024 accelerates the degradation of phosphorylated forms of retinoblastoma protein (pRb) and restores pRb tumor suppressive function in melanoma cells. Cancer Res 63:1420-1429. (Pubitemid 36348726)
58. Miller AJ, et al. (2004) Transcriptional regulation of the melanoma prognostic marker melastatin (TRPM1) by MITF in melanocytes and melanoma. Cancer Res 64:509-516. (Pubitemid 38120889)
59. Widlund HR, et al. (2002) Beta-catenin-induced melanoma growth requires the downstream target Microphthalmia-associated transcription factor. J Cell Biol 158:1079-1087.