Oxygen sensing by H+: Implications for HIF and hypoxic cell memory

Cell Cycle

Volumn 3, Issue 8, 2004, Pages 1025-1027

  Mekhail, Karim ^a   Khacho, Mireille ^a   Gunaratnam, Lakshman ^a   Lee, Stephen ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Acidosis; Cancer; Cardiac arrest; HIF; Hypoxia; Nucleolus; pH; Stroke; VHL

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; LACTIC ACID; OXYGEN; PROTON; TUMOR SUPPRESSOR PROTEIN; VASCULOTROPIN; VON HIPPEL LINDAU PROTEIN;

ACIDOSIS; ANAEROBIC METABOLISM; CANCER; GENE ACTIVATION; HYPOXIA; HYPOXIC CELL; NUCLEOLUS; OXYGEN SENSING; OXYGEN TENSION; PH; PROTEIN DEGRADATION; PROTEIN STABILITY; REVIEW; STROKE;

EID: 13944277272     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.3.8.1075     Document Type: Review

References (49)

1. Semenza GL. HIF-1 and human disease: One highly involved factor. Genes Dev 2000; 14:1983-91.
2. Wagner PD. Skeletal muscle angiogenesis. A possible role for hypoxia. Adv Exp Med Biol 2001; 502:21-38.
3. 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. Loss of HIF-2α and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 2002; 8:702-10.
4. Kojima H, Gu H, Nomura S, Caldwell CC, Kobata T, Carmeliet P, et al. Abnormal B lymphocyte development and autoimmunity in hypoxia-inducible factor 1α-deficient chimeric mice. Proc Natl Acad Sci USA 2002; 99:2170-4.
5. Semenza GL. Targeting HIF-1 for cancer therapy. Nature Rev Cancer 2003; 3:721-32.
6. Harris AL. Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2002; 2:38-47.
7. Gunaratnam L, Morley M, Franovic A, de Paulsen N, Mekhail K, Parolin DA, et al. Hypoxia inducible factor activates the transforming growth factor-α/epidermal growth factor receptor growth stimulatory pathway in VHL (-/-) renal cell carcinoma cells. J Biol Chem 2003; 278:44966-74.
8. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, et al. HIFα targeted for VHL-mediated destruction by proline hydroxylation: Implications for O2 sensing. Science 2001; 292:464-8.
9. 2-regulated prolyl hydroxylation. Science 2001; 292:468-72.
10. Yu F, White SB, Zhao Q, Lee FS. HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc Natl Acad Sci USA 2001; 98:9630-5.
11. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, et al. C. Elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001; 107:43-54.
12. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001; 294:1337-40.
13. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999; 399:271-5.
14. Groulx I, Lee S. Oxygen-dependent ubiquitination and degradation of hypoxia-inducible factor requires nuclear-cytoplasmic trafficking of the von Hippel-Lindau tumor suppressor protein. Mol Cell Biol 2002; 22:5319-36.
15. Lee S, Neumann M, Stearman R, Stauber R, Pause A, Pavlakis GN, et al. Transcription-dependent nuclear-cytoplasmic trafficking is required for the function of the von Hippel-Lindau tumor suppressor protein. Mol Cell Biol 1999; 19:1486-97.
16. Kibel A, Iliopoulos O, DeCaprio JA, Kaelin Jr WG. Binding of the von Hippel-Lindau tumor suppressor protein to Elongin B and C. Science 1995; 269:1444-6.
17. Pause A, Lee S, Worrell RA, Chen DY, Burgess WH, Linehan WM, 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 1997; 94:2156-61.
18. Lonergan KM, Iliopoulos O, Ohh M, Kamura T, Conaway RC, Conaway JW, et al. Regulation of hypoxia-inducible mRNAs by the von Hippel-Lindau-tumor suppressor protein requires binding to complexes containing elongins B/C and Cul2. Mol Cell Biol 1998; 18:732-41.
19. Lisztwan J, Imbert G, Wirbelauer C, Gstaiger M, Krek W. The von Hippel-Lindau tumor suppressor protein is a component of an E3 ubiquitin-protein ligase activity. Genes Dev 1999; 13:1822-33.
20. Iwai K, Yamanaka K, Kamura T, Minato N, Conaway RC, Conaway JW, 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 1999; 96:12436-41.
21. Pause A, Peterson B, Schaffar G, Stearman R, Klausner RD. Studying interactions of four proteins in the yeast two-hybrid system: Structural resemblance of the pVHL/elongin BC/hCUL-2 complex with the ubiquitin ligase complex SKP1/cullin/F-box protein. Proc Natl Acad Sci USA 1999; 96:9533-8.
22. Kamura T, Sato S, Iwai K, Czyzyk-Krzeska M, Conaway RC, Conaway JW. Activation of HIF1α ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc Natl Acad Sci USA 2000; 97:10430-5.
23. Ohh M, Park CW, Ivan M, Hoffman MA, Kim TY, Huang LE, et al. Ubiquitination of hypoxia-inducible factor requires direct binding to the β-domain of the von Hippel-Lindau protein. Nat Cell Biol 2000; 2:423-7.
24. Tanimoto K, Makino Y, Pereira T, Poellinger L. Mechanism of regulation of the hypoxia-inducible factor-1 α by the von Hippel-Lindau tumor suppressor protein. EMBO J 2000; 19:4298-309.
25. Kaelin Jr WG. Molecular basis of the VHL hereditary cancer syndrome. Nat Rev Cancer 2002; 2:673-82.
26. Schofield CJ, Zhang Z. Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes. Curr Opin Struct Biol 1999; 9:722-31.
27. Kivirikko KI, Myllyharju J. Prolyl 4-hydroxylases and their protein disulfide isomerase subunit. Matrix Biol 1998; 16:357-68.
28. Currin RT, Gores GJ, Thurman RG, Lemasters JJ. Protection by acidotic pH against anoxic cell killing in perfused rat liver: Evidence for a pH paradox. Faseb J 1991; 5:207-10.
29. Kaku DA, Giffard RG, Choi DW. Neuroprotective effects of glutamate antagonists and extracellular acidity. Science 1993; 260:1516-8.
30. Giffard RG, Monyer H, Christine CW, Choi DW. Acidosis reduces NMDA receptor activation, glutamate neurotoxicity, and oxygen-glucose deprivation neuronal injury in cortical cultures. Brain Res 1990; 506:339-42.
31. Morimoto Y, Kemmotsu O, Alojado ES. Extracellular acidosis delays cell death against glucose-oxygen deprivation in neuroblastoma x glioma hybrid cells. Crit Care Med 1997; 25:841-7.
32. Nielsen OB, de Paoli F, Overgaard K. Protective effects of lactic acid on force production in rat skeletal muscle. J Physiol 2001; 536:161-6.
33. Mekhail K, Gunaratnam L, Bonicalzi ME, Lee S. HIF activation by pH-dependent nucleolar sequestration of VHL. Nat Cell Biol 2004; 6:642-7.
34. Warburg O. The metabolism of tumors. New York: R. R Smith 1931:129-63.
35. Warburg O. On the origin of cancer cells. Science 1956; 123:309-14.
36. Chavez JC, LaManna JC. Activation of hypoxia-inducible factor-1 in the rat cerebral cortex after transient global ischemia: Potential role of insulin-like growth factor-1. J Neurosci 2002; 22:8922-31.
37. Sun Y, Jin K, Xie L, Childs J, Mao XO, Logvinova A, et al. VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J Clin Invest 2003; 111:1843-51.
38. Gladden LB. Lactic acid: New roles in a new millennium. Proc Natl Acad Sci USA 2001; 98:395-7.
39. Ohh M, Yauch RL, Lonergan KM, Whaley JM, Stemmer-Rachamimov AO, Louis DN, et al. The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol Cell 1998; 1:959-68.
40. Hoffman MA, Ohh M, Yang H, Klco JM, Ivan M, Kaelin Jr WG. von Hippel-Lindau protein mutants linked to type 2C VHL disease preserve the ability to downregulate HIF. Hum Mol Genet 2001; 10:1019-27.
41. Bonicalzi ME, Groulx I, de Paulsen N, Lee S. Role of exon 2-encoded β-domain of the von Hippel-Lindau tumor suppressor protein. J Biol Chem 2001; 276:1407-16.
42. Stickle NH, Chung J, Klco JM, Hill RP, Kaelin Jr WG, Ohh M. pVHL modification by NEDD8 is required for fibronectin matrix assembly and suppression of tumor development. Mol Cell Biol 2004; 24:3251-61.
43. Webb SD, Sherratt JA, Fish RG. Alterations in proteolytic activity at low pH and its association with invasion: A theoretical model. Clin Exp Metastasis 1999; 17:397-407.
44. Patel AA, Gawlinski ET, Lemieux SK, Gatenby RA. A cellular automaton model of early tumor growth and invasion. J Theor Biol 2001; 213:315-31.
45. Bachant JB, Elledge SJ. Mitotic treasures in the nucleolus. Nature 1999; 398:757-8.
46. Weber JD, Taylor LJ, Roussel MF, Sherr CJ, Bar-Sagi D. Nucleolar Arf sequesters Mdm2 and activates p53. Nat Cell Biol 1999; 1:20-6.
47. Lohrum MA, Ludwig RL, Kubbutat MH, Hanlon M, Vousden KH. Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 2003; 3:577-87.
48. Bernardi R, Scaglioni PP, Bergmann S, Horn HF, Vousden KH, Pandolfi PP. PML regulates p53 stability by sequestering Mdm2 to the nucleolus. Nat Cell Biol 2004; 6:665-72.
49. Fabbro M, Henderson BR. Regulation of tumor suppressors by nuclear-cytoplasmic shuttling. Exp Cell Res 2003; 282:59-69.