The phosphorylation status of PAS-B distinguishes HIF-1α from HIF-2α in NBS1 repression

EMBO Journal

Volumn 25, Issue 20, 2006, Pages 4784-4794

  To, Kenneth K W ^a   Sedelnikova, Olga A ^a   Samons, Melissa ^a   Bonner, William M ^a   Huang, L Eric ^a,b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Double strand break; Hypoxia; NBS1; PAS B; PKD1

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; NIBRIN;

ARTICLE; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA REPAIR; GENE FUNCTION; GENE REPRESSION; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; PHOSPHORYLATION; PRIORITY JOURNAL; TUMOR GROWTH;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL CYCLE PROTEINS; CELL LINE; CHROMOSOMAL INSTABILITY; DNA REPAIR; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MULTIPROTEIN COMPLEXES; NEOPLASM PROTEINS; NEOPLASMS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RABBITS;

EID: 33750202279     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601369     Document Type: Article

References (63)

1. Acker T, Diez-Juan A, Aragones J, Tjwa M, Brusselmans K, Moons L, Fukumura D, Moreno-Murciano MP, Herbert JM, Burger A, Riedel J, Elvert G, Flamme I, Maxwell PH, Collen D, Dewerchin M, Jain RK, Plate KH, Carmeliet P (2005) Genetic evidence for a tumor suppressor role of HIF-2alpha. Cancer Cell 8: 131-141
2. Bindra RS, Gibson SL, Meng A, Westermark U, Jasin M, Pierce AJ, Bristow RG, Classon MK, Glazer PM (2005) Hypoxia-induced down-regulation of BRCA1 expression by E2Fs. Cancer Res 65: 11597-11604
3. Bindra RS, Glazer PM (2005) Genetic instability and the tumor microenvironment: towards the concept of microenvironment-induced mutagenesis. Mutat Res 569: 75-85
4. Bindra RS, Schaffer PJ, Meng A, Woo J, Maseide K, Roth ME, Lizardi P, Hedley DW, Bristow RG, Glazer PM (2004) Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol Cell Biol 24: 8504-8518
5. Blancher C, Moore JW, Talks KL, Houlbrook S, Harris AL (2000) Relationship of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression to vascular endothelial growth factor induction and hypoxia survival in human breast cancer cell lines. Cancer Res 60: 7106-7113
6. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshet E (1998) Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394: 485-490
7. Carney JP, Maser RS, Olivares H, Davis EM, Le Beau M, Yates III JR, Hays L, Morgan WF, Petrini JH (1998) The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93: 477-486
8. Chiang YC, Teng SC, Su YN, Hsieh FJ, Wu KJ (2003) c-Myc directly regulates the transcription of the NBS1 gene involved in DNA double-strand break repair. J Biol Chem 278: 19286-19291
9. Compernolle V, Brusselmans K, Acker T, Hoet P, Tjwa M, Beck H, Plaisance S, Dor Y, Keshet E, Lupu F, Nemery B, Dewerchin M, Van Veldhoven P, Plate K, Moons L, Collen D, Carmeliet P (2002) Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 8: 702-710
10. Coquelle A, Toledo F, Stern S, Bieth A, Debatisse M (1998) A new role for hypoxia in tumor progression: induction of fragile site triggering genomic rearrangements and formation of complex DMs and HSRs. Mol Cell 2: 259-265
11. Covello KL, Kehler J, Yu H, Gordan JD, Arsham AM, Hu CJ, Labosky PA, Simon MC, Keith B (2006) HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev 20: 557-570
12. Covello KL, Simon MC, Keith B (2005) Targeted replacement of hypoxia-inducible factor-1alpha by a hypoxia-inducible factor-2alpha knock-in allele promotes tumor growth. Cancer Res 65: 2277-2286
13. D'Amours D, Jackson SP (2002) The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat Rev Mol Cell Biol 3: 317-327
14. Erbel PJ, Card PB, Karakuzu O, Bruick RK, Gardner KH (2003) Structural basis for PAS domain heterodimerization in the basic helix-loop-helix-PAS transcription factor hypoxia-inducible factor. Proc Natl Acad Sci USA 100: 15504-15509
15. Frappart PO, Tong WM, Demuth I, Radovanovic I, Herceg Z, Aguzzi A, Digweed M, Wang ZQ (2005) An essential function for NBS1 in the prevention of ataxia and cerebellar defects. Nat Med 11: 538-544
16. Friedberg EC (2003) DNA damage and repair. Nature 421: 436-440
17. Giaccia A, Siim BG, Johnson RS (2003) HIF-1 as a target for drug development. Nat Rev Drug Discov 2: 803-811
18. Goda N, Ryan HE, Khadivi B, McNulty W, Rickert RC, Johnson RS (2003) Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia. Mol Cell Biol 23: 359-369
19. Gu J, Milligan J, Huang LE (2001) Molecular mechanism of hypoxia-inducible factor 1alpha-p300 interaction. A leucine-rich interface regulated by a single cysteine. J Biol Chem 276: 3550-3554
20. Hammond EM, Denko NC, Dorie MJ, Abraham RT, Giaccia AJ (2002) Hypoxia links ATR and p53 through replication arrest. Mol Cell Biol 22: 1834-1843
21. Hammond EM, Dorie MJ, Giaccia AJ (2003) ATR/ATM targets are phosphorylated by ATR in response to hypoxia and ATM in response to reoxygenation. J Biol Chem 278: 12207-12213
22. Hammond EM, Dorie MJ, Giaccia AJ (2004) Inhibition of ATR leads to increased sensitivity to hypoxia/reoxygenation. Cancer Res 64: 6556-6562
23. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC (2003) Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 23: 9361-9374
24. Huang LE (2004) Targeting HIF-alpha: when a magic arrow hits the bull's eye. Drug Discov Today 9: 869
25. Huang LE, Bunn HF (2003) Hypoxia-inducible factor and its biomedical relevance. J Biol Chem 278: 19575-19578
26. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 95: 7987-7992
27. Huang LE, Pete EA, Schau M, Milligan J, Gu J (2002) Leu-574 of HIF-1alpha is essential for the von Hippel-Lindau (VHL)-mediated degradation pathway. J Biol Chem 277: 41750-41755
28. Kaelin WG (2005) Proline hydroxylation and gene expression. Annu Rev Biochem 74: 115-128
29. Kim JW, Tchernyshyov I, Semenza GL, Dang CV (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3: 177-185
30. Kobayashi J, Tauchi H, Sakamoto S, Nakamura A, Morishima K, Matsuura S, Kobayashi T, Tamai K, Tanimoto K, Komatsu K (2002) NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr Biol 12: 1846-1851
31. Kondo K, Klco J, Nakamura E, Lechpammer M, Kaelin WG (2002) Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein. Cancer Cell 1: 237-246
32. Koshiji M, Kageyama Y, Pete EA, Horikawa I, Barrett JC, Huang LE (2004) HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 23: 1949-1956
33. Koshiji M, To KK, Hammer S, Kumamoto K, Harris AL, Modrich P, Huang LE (2005) HIF-1alpha induces genetic instability by transcriptionally downregulating MutSalpha expression. Mol Cell 17: 793-803
34. Lengauer C, Kinzler KW, Vogelstein B (1998) Genetic instabilities in human cancers. Nature 396: 643-649
35. Mack FA, Patel JH, Biju MP, Haase VH, Simon MC (2005) Decreased growth of Vhl-/- fibrosarcomas is associated with elevated levels of cyclin kinase inhibitors p21 and p27. Mol Cell Biol 25: 4565-4578
36. Maranchie JK, Vasselli JR, Riss J, Bonifacino JS, Linehan WM, Klausner RD (2002) The contribution of VHL substrate binding and HIF1-alpha to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 1: 247-255
37. Matsuura S, Tauchi H, Nakamura A, Kondo N, Sakamoto S, Endo S, Smeets D, Solder B, Belohradsky BH, Der Kaloustian VM, Oshimura M, Isomura M, Nakamura Y, Komatsu K (1998) Positional cloning of the gene for Nijmegen breakage syndrome. Nat Genet 19: 179-181
38. Mihaylova VT, Bindra RS, Yuan J, Campisi D, Narayanan L, Jensen R, Giordano F, Johnson RS, Rockwell S, Glazer PM (2003) Decreased expression of the DNA mismatch repair gene Mlh1 under hypoxic stress in mammalian cells. Mol Cell Biol 23: 3265-3273
39. Nelson DA, Tan TT, Rabson AB, Anderson D, Degenhardt K, White E (2004) Hypoxia and defective apoptosis drive genomic instability and tumorigenesis. Genes Dev 18: 2095-2107
40. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC (2006) HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 3: 187-197
41. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10: 886-895
42. Poellinger L, Johnson RS (2004) HIF-1 and hypoxic response: the plot thickens. Curr Opin Genet Dev 14: 81-85
43. Pugh CW, Ratcliffe PJ (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9: 677-684
44. Raval RR, Lau KW, Tran MG, Sowter HM, Mandriota SJ, Li JL, Pugh CW, Maxwell PH, Harris AL, Ratcliffe PJ (2005) Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol 25: 5675-5686
45. Rogakou EP, Boon C, Redon C, Bonner WM (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916
46. Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM (2000) Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 275: 9390-9395
47. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868
48. Rykx A, De Kimpe L, Mikhalap S, Vantus T, Seufferlein T, Vandenheede JR, Van Lint J (2003) Protein kinase D: a family affair. FEBS Lett 546: 81-86
49. Schultz LB, Chehab NH, Malikzay A, Halazonetis TD (2000) p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J Cell Biol 151: 1381-1390
50. Scortegagna M, Ding K, Oktay Y, Gaur A, Thurmond F, Yan LJ, Marck BT, Matsumoto AM, Shelton JM, Richardson JA, Bennett MJ, Garcia JA (2003) Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/- mice. Nat Genet 35: 331-340
51. Semenza GL (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732
52. Storz P, Doppler H, Johannes FJ, Toker A (2003) Tyrosine phosphorylation of protein kinase D in the pleckstrin homology domain leads to activation. J Biol Chem 278: 17969-17976
53. Stracker TH, Carson CT, Weitzman MD (2002) Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 418: 348-352
54. Talks KL, Turley H, Gatter KC, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL (2000) The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor- associated macrophages. Am J Pathol 157: 411-421
55. Tauchi H, Kobayashi J, Morishima K, van Gent DC, Shiraishi T, Verkaik NS, vanHeems D, Ito E, Nakamura A, Sonoda E, Takata M, Takeda S, Matsuura S, Komatsu K (2002) Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature 420: 93-98
56. Tian H, Hammer RE, Matsumoto AM, Russell DW, McKnight SL (1998) The hypoxia-responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development. Genes Dev 12: 3320-3324
57. To KK, Koshiji M, Hammer S, Huang LE (2005) Genetic instability: the dark side of the hypoxic response. Cell Cycle 4: 881-882
58. Varon R, Vissinga C, Platzer M, Cerosaletti KM, Chrzanowska KH, Saar K, Beckmann G, Seemanova E, Cooper PR, Nowak NJ, Stumm M, Weemaes CM, Gatti RA, Wilson RK, Digweed M, Rosenthal A, Sperling K, Concannon P, Reis A (1998) Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 93: 467-476
59. Vogelstein B, Kinzler KW (2004) Cancer genes and the pathways they control. Nat Med 10: 789-799
60. 2-regulated gene expression. FASEB J 16: 1151-1162
61. Wiesener MS, Turley H, Allen WE, Willam C, Eckardt KU, Talks KL, Wood SM, Gatter KC, Harris AL, Pugh CW, Ratcliffe PJ, Maxwell PH (1998) Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha. Blood 92: 2260-2268
62. Yaffe MB, Leparc GG, Lai J, Obata T, Volinia S, Cantley LC (2001) A motif-based profile scanning approach for genomewide prediction of signaling pathways. Nat Biotechnol 19: 348-353
63. Zhou BB, Elledge SJ (2000) The DNA damage response: putting checkpoints in perspective. Nature 408: 433-439