Human CHCHD4 mitochondrial proteins regulate cellular oxygen consumption rate and metabolism and provide a critical role in hypoxia signaling and tumor progression

Journal of Clinical Investigation

Volumn 122, Issue 2, 2012, Pages 600-611

  Yang, Jun ^a,d   Staples, Oliver ^a   Thomas, Luke W ^a   Briston, Thomas ^a   Robson, Mathew ^b   Poon, Evon ^a   Simões, Maria L ^a   El Emir, Ethaar ^b   Buffa, Francesca M ^c   Ahmed, Afshan ^a   Annear, Nicholas P ^a   Shukla, Deepa ^a   Pedley, Barbara R ^b   Maxwell, Patrick H ^a   Harris, Adrian L ^c   Ashcroft, Margaret ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOCHONDRIAL PROTEIN; PROTEIN CHCHD4.1; PROTEIN CHCHD4.2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HYPOXIA; CELL METABOLISM; FEMALE; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; TUMOR GROWTH;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANOXIA; CELL LINE, TUMOR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICROARRAY ANALYSIS; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; NEOPLASMS; OXYGEN; OXYGEN CONSUMPTION; PROTEIN ISOFORMS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

EID: 84863011566     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI58780     Document Type: Article

References (43)

1. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008;30(4):393-402. (Pubitemid 351681994)
2. Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A. 1995;92(12):5510-5514.
3. Poon E, Harris AL, Ashcroft M. Targeting the hypoxia-inducible factor (HIF) pathway in cancer. Expert Rev Mol Med. 2009;11:e26.
4. Ivan M, et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science. 2001;292(5516):464-468. (Pubitemid 32335941)
5. Jaakkola P, et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. 2001;292(5516):468-472. (Pubitemid 32335942)
6. Yu F, White SB, Zhao Q, Lee FS. HIF-1alpha binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc Natl Acad Sci U S A. 2001;98(17):9630-9635. (Pubitemid 32769354)
7. Maxwell PH, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature. 1999;399(6733):271-275. (Pubitemid 29246458)
8. Agani FH, Pichiule P, Chavez JC, LaManna JC. The role of mitochondria in the regulation of hypoxia-inducible factor 1 expression during hypoxia. J Biol Chem. 2000;275(46):35863-35867.
9. Chandel NS, et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000;275(33):25130-25138.
10. Hagen T, Taylor CT, Lam F, Moncada S. Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1alpha. Science. 2003;302(5652):1975-1978. (Pubitemid 37523507)
11. Guzy RD, et al. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 2005;1(6):401-408. (Pubitemid 43960623)
12. Lin X, et al. A chemical genomics screen highlights the essential role of mitochondria in HIF-1 regulation. Proc Natl Acad Sci U S A. 2008;105(1):174-179.
13. Mansfield KD, et al. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab. 2005;1(6):393-399. (Pubitemid 43960625)
14. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A. 1998;95(20):11715-11720. (Pubitemid 28460480)
15. Pan Y, et al. Multiple factors affecting cellular redox status and energy metabolism modulate hypoxia-inducible factor prolyl hydroxylase activity in vivo and in vitro. Mol Cell Biol. 2007;27(3):912-925. (Pubitemid 46174556)
16. Agani FH, Pichiule P, Carlos Chavez J, LaManna JC. Inhibitors of mitochondrial complex I attenuate the accumulation of hypoxia-inducible factor-1 during hypoxia in Hep3B cells. Comp Biochem Physiol A Mol Integr Physiol. 2002;132(1):107-109. (Pubitemid 34327738)
17. Brown ST, Nurse CA. Induction of HIF-2alpha is dependent on mitochondrial O2 consumption in an O2-sensitive adrenomedullary chromaffin cell line. Am J Physiol Cell Physiol. 2008;294(6):C1305-C1312.
18. Doege K, Heine S, Jensen I, Jelkmann W, Metzen E. Inhibition of mitochondrial respiration elevates oxygen concentration but leaves regulation of hypoxia-inducible factor (HIF) intact. Blood. 2005;106(7):2311-2317. (Pubitemid 41510801)
19. Chua YL, et al. Stabilization of hypoxia-inducible factor-1alpha protein in hypoxia occurs independently of mitochondrial reactive oxygen species production. J Biol Chem. 2010;285(41):31277-31284.
20. Eisenberg D, Marcotte EM, Xenarios I, Yeates TO. Protein function in the post-genomic era. Nature. 2000;405(6788):823-826.
21. Date SV. Estimating protein function using protein-protein relationships. Methods Mol Biol. 2007;408:109-127.
22. Date SV. The Rosetta stone method. Methods Mol Biol. 2008;453:169-180.
23. Hofmann S, Rothbauer U, Muhlenbein N, Baiker K, Hell K, Bauer MF. Functional and mutational characterization of human MIA40 acting during import into the mitochondrial intermembrane space. J Mol Biol. 2005;353(3):517-528. (Pubitemid 41414731)
24. Banci L, et al. MIA40 is an oxidoreductase that catalyzes oxidative protein folding in mitochondria. Nat Struct Mol Biol. 2009;16(2):198-206.
25. Longen S, et al. Systematic analysis of the twin cx(9)c protein family. J Mol Biol. 2009;393(2):356-368.
26. Hetz C, et al. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science. 2006;312(5773):572- 576.
27. Bihlmaier K, Mesecke N, Terziyska N, Bien M, Hell K, Herrmann JM. The disulfide relay system of mitochondria is connected to the respiratory chain. J Cell Biol. 2007;179(3):389-395. (Pubitemid 350074784)
28. Bien M, Longen S, Wagener N, Chwalla I, Herrmann JM, Riemer J. Mitochondrial disulfide bond formation is driven by intersubunit electron transfer in Erv1 and proofread by glutathione. Mol Cell. 2010;37(4):516-528.
29. Fukuda R, Zhang H, Kim JW, Shimoda L, Dang CV, Semenza GL. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell. 2007;129(1):111-122. (Pubitemid 46507584)
30. Chacinska A, et al. Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. Embo J. 2004;23(19):3735-3746. (Pubitemid 39389705)
31. Terziyska N, et al. Mia40, a novel factor for protein import into the intermembrane space of mitochondria is able to bind metal ions. FEBS Lett. 2005;579(1):179-184. (Pubitemid 40023393)
32. Semenza GL. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene. 2010;29(5):625-634.
33. Miller LD, et al. An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc Natl Acad Sci U S A. 2005;102(38):13550-13555. (Pubitemid 41420886)
34. Winter SC, et al. Relation of a hypoxia metagene derived from head and neck cancer to prognosis of multiple cancers. Cancer Res. 2007;67(7):3441-3449. (Pubitemid 46724885)
35. Ishikawa M, et al. Experimental trial for diagnosis of pancreatic ductal carcinoma based on gene expression profiles of pancreatic ductal cells. Cancer Sci. 2005;96(7):387-393. (Pubitemid 41179739)
36. Ma XJ, et al. A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell. 2004;5(6):607-616.
37. Kotliarov Y, et al. High-resolution global genomic survey of 178 gliomas reveals novel regions of copy number alteration and allelic imbalances. Cancer Res. 2006;66(19):9428-9436. (Pubitemid 44623639)
38. Gao P, et al. HIF-dependent antitumorigenic effect of antioxidants in vivo. Cancer Cell. 2007;12(3):230-238. (Pubitemid 47333417)
39. Jiang BH, Semenza GL, Bauer C, Marti HH. Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am J Physiol. 1996;271(4 pt 1):C1172-C1180.
40. Hirsila M, Koivunen P, Gunzler V, Kivirikko KI, Myllyharju J. Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J Biol Chem. 2003;278(33):30772-30780. (Pubitemid 36994584)
41. Mesecke N, et al. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell. 2005;121(7):1059-1069. (Pubitemid 40884396)
42. Carroll VA, Ashcroft M. Role of hypoxia-inducible factor (HIF)-1alpha versus HIF-2alpha in the regulation of HIF target genes in response to hypoxia, insulin-like growth factor-I, or loss of von Hippel-Lindau function: implications for targeting the HIF pathway. Cancer Res. 2006;66(12):6264-6270.
43. El Emir E, et al. Predicting response to radioimmunotherapy from the tumor microenvironment of colorectal carcinomas. Cancer Res. 2007;67(24):11896-11905.