Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-α prolyl hydroxylase

Cancer Cell

Volumn 7, Issue 1, 2005, Pages 77-85

  Selak, Mary A ^a   Armour, Sean M ^b   MacKenzie, Elaine D ^a   Boulahbel, Houda ^a   Watson, David G ^c   Mansfield, Kyle D ^b   Pan, Yi ^b   Simon, M Celeste ^b   Thompson, Craig B ^b   Gottlieb, Eyal ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; SUCCINIC ACID; TRICARBOXYLIC ACID;

ARTICLE; CARCINOGENESIS; CITRIC ACID CYCLE; CONTROLLED STUDY; CYTOSOL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME STABILITY; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; SOMATIC MUTATION;

EID: 19944433653     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2004.11.022     Document Type: Article

References (43)

1. Appelhoff R.J., Tian Y.M., Raval R.R., Turley H., Harris A.L., Pugh C.W., Ratcliffe P.J., Gleadle J.M. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J. Biol. Chem. 279:2004;38458-38465
2. Baysal B.E. On the association of succinate dehydrogenase mutations with hereditary paraganglioma. Trends Endocrinol. Metab. 14:2003;453-459
3. Beasley N.J., Leek R., Alam M., Turley H., Cox G.J., Gatter K., Millard P., Fuggle S., Harris A.L. Hypoxia-inducible factors HIF-1α and HIF-2α in head and neck cancer. Relationship to tumor biology and treatment outcome in surgically resected patients Cancer Res. 62:2002;2493-2497
4. Bruick R.K., McKnight S.L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science. 294:2001;1337-1340
5. Brusselmans K., Bono F., Maxwell P., Dor Y., Dewerchin M., Collen D., Herbert J.M., Carmeliet P. Hypoxia-inducible factor-2α (HIF-2α) is involved in the apoptotic response to hypoglycemia but not to hypoxia. J. Biol. Chem. 276:2001;39192-39196
6. Chandel N.S., McClintock D.S., Feliciano C.E., Wood T.M., Melendez J.A., Rodriguez A.M., Schumacker P.T. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia. A mechanism of O2 sensing J. Biol. Chem. 275:2000;25130-25138
7. Eng C., Kiuru M., Fernandez M.J., Aaltonen L.A. A role for mitochondrial enzymes in inherited neoplasia and beyond. Nat. Rev. Cancer. 3:2003;193-202
8. Epstein A.C., Gleadle J.M., McNeill L.A., Hewitson K.S., O'Rourke J., Mole D.R., Mukherji M., Metzen E., Wilson M.I., Dhanda A., et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell. 107:2001;43-54
9. Fox C.J., Hammerman P.S., Cinalli R.M., Master S.R., Chodosh L.A., Thompson C.B. The serine/threonine kinase Pim-2 is a transcriptionally regulated apoptotic inhibitor. Genes Dev. 17:2003;1841-1854
10. Frederiksen C.M., Knudsen S., Laurberg S., Orntoft T.F. Classification of Dukes' B and C colorectal cancers using expression arrays. J. Cancer Res. Clin. Oncol. 129:2003;263-271
11. Gimenez-Roqueplo A.P., Favier J., Rustin P., Mourad J.J., Plouin P.F., Corvol P., Rotig A., Jeunemaitre X. The R22X mutation of the SDHD gene in hereditary paraganglioma abolishes the enzymatic activity of complex II in the mitochondrial respiratory chain and activates the hypoxia pathway. Am. J. Hum. Genet. 69:2001;1186-1197
12. Habano W., Sugai T., Nakamura S., Uesugi N., Higuchi T., Terashima M., Horiuchi S. Reduced expression and loss of heterozygosity of the SDHD gene in colorectal and gastric cancer. Oncol. Rep. 10:2003;1375-1380
13. Hagen T., Taylor C.T., Lam F., Moncada S. Redistribution of intracellular oxygen in hypoxia by nitric oxide. Effect on HIF1α Science. 302:2003;1975-1978
14. He W., Miao F.J., Lin D.C., Schwandner R.T., Wang Z., Gao J., Chen J.L., Tian H., Ling L. Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors. Nature. 429:2004;188-193
15. Hewitson K.S., McNeill L.A., Riordan M.V., Tian Y.M., Bullock A.N., Welford R.W., Elkins J.M., Oldham N.J., Bhattacharya S., Gleadle J.M., et al. Hypoxia-inducible factor (HIF) asparagine hydroxylase is identical to factor inhibiting HIF (FIH) and is related to the cupin structural family. J. Biol. Chem. 277:2002;26351-26355
16. Holme E. A kinetic study of thymine 7-hydroxylase from neurospora crassa. Biochemistry. 14:1975;4999-5003
17. Hon W.C., Wilson M.I., Harlos K., Claridge T.D., Schofield C.J., Pugh C.W., Maxwell P.H., Ratcliffe P.J., Stuart D.I., Jones E.Y. Structural basis for the recognition of hydroxyproline in HIF-1α by pVHL. Nature. 417:2002;975-978
18. Huang J., Zhao Q., Mooney S.M., Lee F.S. Sequence determinants in hypoxia-inducible factor-1α for hydroxylation by the prolyl hydroxylases PHD1, PHD2, and PHD3. J. Biol. Chem. 277:2002;39792-39800
19. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J.M., Lane W.S., Kaelin W.G. Jr. HIFα targeted for VHL-mediated destruction by proline hydroxylation. Implications for O2 sensing Science. 292:2001;464-468
20. Ivan M., Haberberger T., Gervasi D.C., Michelson K.S., Gunzler V., Kondo K., Yang H., Sorokina I., Conaway R.C., Conaway J.W., Kaelin W.G. Jr. Biochemical purification and pharmacological inhibition of a mammalian prolyl hydroxylase acting on hypoxia-inducible factor. Proc. Natl. Acad. Sci. USA. 99:2002;13459-13464
21. Jaakkola P., Mole D.R., Tian Y.M., Wilson M.I., Gielbert J., Gaskell S.J., Kriegsheim A., Hebestreit H.F., Mukherji M., Schofield C.J., et al. Targeting of HIF-α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. 292:2001;468-472
22. Kaelin W.G. Jr. Molecular basis of the VHL hereditary cancer syndrome. Nat. Rev. Cancer. 2:2002;673-682
23. Lando D., Peet D.J., Gorman J.J., Whelan D.A., Whitelaw M.L., Bruick R.K. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16:2002;1466-1471. a
24. Lando D., Peet D.J., Whelan D.A., Gorman J.J., Whitelaw M.L. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science. 295:2002;858-861. b
25. Min J.H., Yang H., Ivan M., Gertler F., Kaelin W.G. Jr., Pavletich N.P. Structure of an HIF-1α-pVHL complex. Hydroxyproline recognition in signaling Science. 296:2002;1886-1889
26. Myllyla R., Tuderman L., Kivirikko K.I. Mechanism of the prolyl hydroxylase reaction. 2. Kinetic analysis of the reaction sequence. Eur. J. Biochem. 80:1977;349-357
27. Neumann H.P., Pawlu C., Peczkowska M., Bausch B., McWhinney S.R., Muresan M., Buchta M., Franke G., Klisch J., Bley T.A., et al. Distinct clinical features of paraganglioma syndromes associated with SDHB and SDHD gene mutations. JAMA. 292:2004;943-951
28. Paddenberg R., Ishaq B., Goldenberg A., Faulhammer P., Rose F., Weissmann N., Braun-Dullaeus R.C., Kummer W. Essential role of complex II of the respiratory chain in hypoxia-induced ROS generation in the pulmonary vasculature. Am. J. Physiol. Lung Cell. Mol. Physiol. 284:2003;L710-L719
29. Pennacchietti S., Michieli P., Galluzzo M., Mazzone M., Giordano S., Comoglio P.M. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell. 3:2003;347-361
30. Pollard P.J., Wortham N.C., Tomlinson I.P. The TCA cycle and tumorigenesis. The examples of fumarate hydratase and succinate dehydrogenase Ann. Med. 35:2003;632-639
31. Polyak K., Xia Y., Zweier J.L., Kinzler K.W., Vogelstein B. A model for p53-induced apoptosis. Nature. 389:1997;300-305
32. Pugh C.W., Ratcliffe P.J. Regulation of angiogenesis by hypoxia. Role of the HIF system Nat. Med. 9:2003;677-684
33. Rustin P., Rotig A. Inborn errors of complex II-unusual human mitochondrial diseases. Biochim. Biophys. Acta. 1553:2002;117-122
34. Safran M., Kaelin W.G. Jr. HIF hydroxylation and the mammalian oxygen-sensing pathway. J. Clin. Invest. 111:2003;779-783
35. Schofield C.J., Ratcliffe P.J. Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5:2004;343-354
36. Schofield C.J., Zhang Z. Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes. Curr. Opin. Struct. Biol. 9:1999;722-731
37. Semenza G.L. HIF-1 and tumor progression. Pathophysiology and therapeutics Trends Mol. Med. 8:2002;S62-S67
38. Senoo-Matsuda N., Yasuda K., Tsuda M., Ohkubo T., Yoshimura S., Nakazawa H., Hartman P.S., Ishii N. A defect in the cytochrome b large subunit in complex II causes both superoxide anion overproduction and abnormal energy metabolism in Caenorhabditis elegans. J. Biol. Chem. 276:2001;41553-41558
39. Sowter H.M., Ratcliffe P.J., Watson P., Greenberg A.H., Harris A.L. HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res. 61:2001;6669-6673
40. Staller P., Sulitkova J., Lisztwan J., Moch H., Oakeley E.J., Krek W. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature. 425:2003;307-311
41. Trounce I.A., Kim Y.L., Jun A.S., Wallace D.C. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol. 264:1996;484-509
42. Yankovskaya V., Horsefield R., Tornroth S., Luna-Chavez C., Miyoshi H., Leger C., Byrne B., Cecchini G., Iwata S. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science. 299:2003;700-704
43. Yu F., White S.B., Zhao Q., Lee F.S. HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc. Natl. Acad. Sci. USA. 98:2001;9630-9635