The multifaceted von Hippel-Lindau tumour suppressor protein

FEBS Letters

Volumn 588, Issue 16, 2014, Pages 2704-2711

  Robinson, Claire M ^a   Ohh, Michael ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Clear cell renal cell carcinoma (ccRCC); Epigenetics; Hypoxia inducible factor (HIF); von Hippel Lindau protein (pVHL)

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; VON HIPPEL LINDAU PROTEIN;

CARCINOGENESIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DISEASE ASSOCIATION; DNA METHYLATION; EPIGENETICS; GENETIC TRANSCRIPTION; HISTONE MODIFICATION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; REVIEW; TRANSCRIPTION REGULATION; VON HIPPEL LINDAU DISEASE; VON HIPPEL LINDAU GENE;

CLEAR-CELL RENAL CELL CARCINOMA (CCRCC); EPIGENETICS; HYPOXIA-INDUCIBLE FACTOR (HIF); VON HIPPEL-LINDAU PROTEIN (PVHL);

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DISEASE PROGRESSION; EPIGENESIS, GENETIC; HUMANS; NEOPLASMS; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN;

EID: 84905079134     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.02.026     Document Type: Review

References (87)

1. E. von Hippel Ueber eine sehr seltene erkrankung der nethaut Graefe Arch. Ophthalmol. 59 1904 83 106
2. A. Lindau Zur frage der angiomatosis retinai und ihrer hirncomplikation Acta Ophthalmol. 4 1927 193 226
3. A.G. Knudson Jr. Mutation and cancer: statistical study of retinoblastoma Proc. Natl. Acad. Sci. USA 68 4 1971 820 823
4. W.Y. Kim, and W.G. Kaelin Role of VHL gene mutation in human cancer J. Clin. Oncol. 22 24 2004 4991 5004
5. M.M. Baldewijns et al. Genetics and epigenetics of renal cell cancer Biochim. Biophys. Acta 1785 2 2008 133 155
6. L.E. Moore et al. Von Hippel-Lindau (VHL) inactivation in sporadic clear cell renal cancer: associations with germline VHL polymorphisms and etiologic risk factors PLoS Genet. 7 10 2011 e1002312
7. K.P. van Houwelingen et al. Prevalence of von Hippel-Lindau gene mutations in sporadic renal cell carcinoma: results from The Netherlands cohort study BMC Cancer 5 2005 57
8. T. Shuin et al. Frequent somatic mutations and loss of heterozygosity of the von Hippel-Lindau tumor suppressor gene in primary human renal cell carcinomas Cancer Res. 54 11 1994 2852 2855
9. H. Kanno et al. Somatic mutations of the von Hippel-Lindau tumor suppressor gene in sporadic central nervous system hemangioblastomas Cancer Res. 54 18 1994 4845 4847
10. J. Oberstrass et al. Mutation of the Von Hippel-Lindau tumour suppressor gene in capillary haemangioblastomas of the central nervous system J. Pathol. 179 2 1996 151 156
11. J.R. Gnarra et al. Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice Proc. Natl. Acad. Sci. USA 94 17 1997 9102 9107
12. V.H. Haase et al. Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor Proc. Natl. Acad. Sci. USA 98 4 2001 1583 1588
13. H.C. Shen et al. Deciphering von Hippel-Lindau (VHL/Vhl)-associated pancreatic manifestations by inactivating Vhl in specific pancreatic cell populations PLoS One 4 4 2009 e4897
14. E.B. Rankin, J.E. Tomaszewski, and V.H. Haase Renal cyst development in mice with conditional inactivation of the von Hippel-Lindau tumor suppressor Cancer Res. 66 5 2006 2576 2583
15. O. Iliopoulos et al. Tumour suppression by the human von Hippel-Lindau gene product Nat. Med. 1 8 1995 822 826
16. F. Latif et al. Identification of the von Hippel-Lindau disease tumor suppressor gene Science 260 5112 1993 1317 1320
17. O. Iliopoulos, M. Ohh, and W.G. Kaelin Jr. PVHL19 is a biologically active product of the von Hippel-Lindau gene arising from internal translation initiation Proc. Natl. Acad. Sci. USA 95 20 1998 11661 11666
18. C. Blankenship et al. Alternate choice of initiation codon produces a biologically active product of the von Hippel Lindau gene with tumor suppressor activity Oncogene 18 8 1999 1529 1535
19. A. Kibel et al. Binding of the von Hippel-Lindau tumor suppressor protein to Elongin B and C Science 269 5229 1995 1444 1446
20. P. Heir et al. DCNL1 functions as a substrate sensor and activator of cullin 2-RING ligase Mol. Cell. Biol. 33 8 2013 1621 1631
21. A. Pause et al. The von Hippel-Lindau tumor-suppressor gene product forms a stable complex with human CUL-2, a member of the Cdc53 family of proteins Proc. Natl. Acad. Sci. USA 94 6 1997 2156 2161
22. K. Iwai et al. Identification of the von Hippel-lindau tumor-suppressor protein as part of an active E3 ubiquitin ligase complex Proc. Natl. Acad. Sci. USA 96 22 1999 12436 12441
23. H. Okuda et al. The von Hippel-Lindau tumor suppressor protein mediates ubiquitination of activated atypical protein kinase C J. Biol. Chem. 276 47 2001 43611 43617
24. S. Lee et al. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer Cancer Cell 8 2 2005 155 167
25. A.V. Kuznetsova et al. Von Hippel-Lindau protein binds hyperphosphorylated large subunit of RNA polymerase II through a proline hydroxylation motif and targets it for ubiquitination Proc. Natl. Acad. Sci. USA 100 5 2003 2706 2711
26. M.A. Hoffman et al. Von Hippel-Lindau protein mutants linked to type 2C VHL disease preserve the ability to downregulate HIF Hum. Mol. Genet. 10 10 2001 1019 1027
27. M. Ohh et al. The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix Mol. Cell 1 7 1998 959 968
28. M. Feijoo-Cuaresma et al. Inadequate activation of the GTPase RhoA contributes to the lack of fibronectin matrix assembly in von Hippel-Lindau protein-defective renal cancer cells J. Biol. Chem. 283 36 2008 24982 24990
29. A. Grosfeld et al. Interaction of hydroxylated collagen IV with the von hippel-lindau tumor suppressor J. Biol. Chem. 282 18 2007 13264 13269
30. G. Kurban et al. Collagen matrix assembly is driven by the interaction of von Hippel-Lindau tumor suppressor protein with hydroxylated collagen IV alpha 2 Oncogene 27 7 2008 1004 1012
31. A. Hergovich et al. Regulation of microtubule stability by the von Hippel-Lindau tumour suppressor protein pVHL Nat. Cell Biol. 5 1 2003 64 70
32. C.R. Thoma et al. VHL loss causes spindle misorientation and chromosome instability Nat. Cell Biol. 11 8 2009 994 1001
33. B. Schermer et al. The von Hippel-Lindau tumor suppressor protein controls ciliogenesis by orienting microtubule growth J. Cell Biol. 175 4 2006 547 554
34. J.S. Roe, and H.D. Youn The positive regulation of p53 by the tumor suppressor VHL Cell Cycle 5 18 2006 2054 2056
35. J.S. Roe et al. Von Hippel-Lindau protein promotes Skp2 destabilization on DNA damage Oncogene 30 28 2011 3127 3138
36. W. Ji et al. PVHL acts as a downstream target of E2F1 to suppress E2F1 activity Biochem. J. 457 1 2014 185 195
37. J.L. Metcalf et al. K63-Ubiquitylation of VHL by SOCS1 mediates DNA double-strand break repair Oncogene 2013
38. A.M. Roberts et al. Suppression of hypoxia-inducible factor 2alpha restores p53 activity via Hdm2 and reverses chemoresistance of renal carcinoma cells Cancer Res. 69 23 2009 9056 9064
39. H. Yang et al. PVHL acts as an adaptor to promote the inhibitory phosphorylation of the NF-kappaB agonist Card9 by CK2 Mol. Cell 28 1 2007 15 27
40. J. Wang et al. The von hippel-lindau protein suppresses androgen receptor activity Mol. Endocrinol. 28 2 2014 239 248
41. L.A. Polyakova Familial erythrocytosis among inhabitants of the Chuvash ASSR Problemi Gematologii i Perelivaniya Krovi 10 1974 30 36
42. S.O. Ang et al. Disruption of oxygen homeostasis underlies congenital Chuvash polycythemia Nat. Genet. 32 4 2002 614 621
43. R.C. Russell et al. Loss of JAK2 regulation via a heterodimeric VHL-SOCS1 E3 ubiquitin ligase underlies Chuvash polycythemia Nat. Med. 17 7 2011 845 853
44. M. Ohh et al. Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein Nat. Cell Biol. 2 7 2000 423 427
45. P.H. Maxwell et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis Nature 399 6733 1999 271 275
46. M. Ivan et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing Science 292 5516 2001 464 468
47. A.C. Epstein et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation Cell 107 1 2001 43 54
48. K. Tanimoto et al. Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein EMBO J. 19 16 2000 4298 4309
49. P. Vaupel et al. Oxygenation of human tumors: evaluation of tissue oxygen distribution in breast cancers by computerized O2 tension measurements Cancer Res. 51 12 1991 3316 3322
50. Z. Arany et al. An essential role for p300/CBP in the cellular response to hypoxia Proc. Natl. Acad. Sci. USA 93 23 1996 12969 12973
51. P.C. Mahon, K. Hirota, and G.L. Semenza FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity Genes Dev. 15 20 2001 2675 2686
52. J. Schodel et al. High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq Blood 117 23 2011 e207 e217
53. X. Xia et al. Integrative analysis of HIF binding and transactivation reveals its role in maintaining histone methylation homeostasis Proc. Natl. Acad. Sci. USA 106 11 2009 4260 4265
54. R.H. Wenger, D.P. Stiehl, and G. Camenisch Integration of oxygen signaling at the consensus HRE Sci. STKE 306 2005 re12
55. X. Na et al. Overproduction of vascular endothelial growth factor related to von Hippel-Lindau tumor suppressor gene mutations and hypoxia-inducible factor-1 alpha expression in renal cell carcinomas J. Urol. 170 2 Pt 1 2003 588 592
56. M. Krieg, H.H. Marti, and K.H. Plate Coexpression of erythropoietin and vascular endothelial growth factor in nervous system tumors associated with von Hippel-Lindau tumor suppressor gene loss of function Blood 92 9 1998 3388 3393
57. O. Warburg On the origin of cancer cells Science 123 3191 1956 309 314
58. B. Krishnamachary et al. Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal cell carcinoma mediated by TCF3, ZFHX1A, and ZFHX1B Cancer Res. 66 5 2006 2725 2731
59. S.K. Harten et al. Regulation of renal epithelial tight junctions by the von Hippel-Lindau tumor suppressor gene involves occludin and claudin 1 and is independent of E-cadherin Mol. Biol. Cell 20 3 2009 1089 1101
60. P. Staller et al. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL Nature 425 6955 2003 307 311
61. G.L. Semenza Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy Trends Pharmacol. Sci. 33 4 2012 207 214
62. B. Keith, R.S. Johnson, and M.C. Simon HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression Nat. Rev. Cancer 12 1 2012 9 22
63. N. Kroeger et al. Deletions of chromosomes 3p and 14q molecularly subclassify clear cell renal cell carcinoma Cancer 119 8 2013 1547 1554
64. S. Biswas et al. Effects of HIF-1alpha and HIF2alpha on growth and metabolism of clear-cell renal cell carcinoma 786-0 xenografts J. Oncol. 2010 2010 757908
65. R.R. Raval et al. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma Mol. Cell. Biol. 25 13 2005 5675 5686
66. J.A. Watson et al. Epigenetics, the epicenter of the hypoxic response Epigenetics 5 4 2010 293 296
67. I. Varela et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma Nature 469 7331 2011 539 542
68. G.L. Dalgliesh et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes Nature 463 7279 2010 360 363
69. G. van Haaften et al. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer Nat. Genet. 41 5 2009 521 523
70. N.S. Kenneth et al. SWI/SNF regulates the cellular response to hypoxia J. Biol. Chem. 284 7 2009 4123 4131
71. A. Melvin, and S. Rocha Chromatin as an oxygen sensor and active player in the hypoxia response Cell. Signal. 24 1 2012 35 43
72. Cancer Genome Atlas Research, N. Comprehensive molecular characterization of clear cell renal cell carcinoma Nature 499 7456 2013 43 49
73. F.E. McRonald et al. CpG methylation profiling in VHL related and VHL unrelated renal cell carcinoma Mol. Cancer 8 2009 31
74. S. Shahrzad et al. Induction of DNA hypomethylation by tumor hypoxia Epigenetics 2 2 2007 119 125
75. J.A. Watson et al. Generation of an epigenetic signature by chronic hypoxia in prostate cells Hum. Mol. Genet. 18 19 2009 3594 3604
76. C.M. Robinson et al. Hypoxia-induced DNA hypermethylation in human pulmonary fibroblasts is associated with Thy-1 promoter methylation and the development of a pro-fibrotic phenotype Respir. Res. 13 2012 74
77. K. Skowronski et al. Ischemia dysregulates DNA methyltransferases and p16INK4a methylation in human colorectal cancer cells Epigenetics 5 6 2010 547 556
78. C.J. Watson et al. Hypoxia-induced epigenetic modifications are associated with cardiac tissue fibrosis and the development of a myofibroblast-like phenotype Hum. Mol. Genet. 2013
79. D.M. Franchini, K.M. Schmitz, and S.K. Petersen-Mahrt 5-Methylcytosine DNA demethylation: more than losing a methyl group Annu. Rev. Genet. 46 2012 419 441
80. K.P. Koh et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells Cell Stem Cell 8 2 2011 200 213
81. G.P. Pfeifer, S. Kadam, and S.G. Jin 5-Hydroxymethylcytosine and its potential roles in development and cancer Epigenetics Chromatin 6 1 2013 10
82. R.H. Wenger et al. Oxygen-regulated erythropoietin gene expression is dependent on a CpG methylation-free hypoxia-inducible factor-1 DNA-binding site Eur. J. Biochem. 253 3 1998 771 777
83. J. Nakamura et al. Expression of hypoxic marker CA IX is regulated by site-specific DNA methylation and is associated with the histology of gastric cancer Am. J. Pathol. 178 2 2011 515 524
84. S. Vanharanta et al. Epigenetic expansion of VHL-HIF signal output drives multiorgan metastasis in renal cancer Nat. Med. 19 1 2013 50 56
85. P.J. Pollard et al. Regulation of Jumonji-domain-containing histone demethylases by hypoxia-inducible factor (HIF)-1alpha Biochem. J. 416 3 2008 387 394
86. S. Beyer et al. The histone demethylases JMJD1A and JMJD2B are transcriptional targets of hypoxia-inducible factor HIF J. Biol. Chem. 283 52 2008 36542 36552
87. W. Luo et al. Histone demethylase JMJD2C is a coactivator for hypoxia-inducible factor 1 that is required for breast cancer progression Proc. Natl. Acad. Sci. USA 109 49 2012 E3367 E3376