Absence of the Birt-Hogg-Dubé gene product is associated with increased hypoxia-inducible factor transcriptional activity and a loss of metabolic flexibility

Oncogene

Volumn 30, Issue 10, 2011, Pages 1159-1173

  Preston, R S ^a   Philp, A ^b   Claessens, T ^c   Gijezen, L ^c   Dydensborg, A B ^d   Dunlop, E A ^a   Harper, K T ^a   Brinkhuizen, T ^c   Menko, F H ^e   Davies, D M ^a   Land, S C ^f   Pause, A ^d   Baar, K ^b   Van Steensel, M A M ^c   Tee, A R ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d MCGILL UNIVERSITY   (Canada)

^e VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Birt Hogg Dub ; folliculin; HIF; warburg effect

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; DEOXYGLUCOSE; ESTRONE; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; LACTATE DEHYDROGENASE; LACTIC ACID; MESSENGER RNA; MONOCARBOXYLATE TRANSPORTER 1; PROTEIN BNIP3; PYRUVATE DEHYDROGENASE KINASE; PYRUVATE KINASE; SHORT HAIRPIN RNA; VASCULOTROPIN;

ARTICLE; BIRT HOGG DUBE SYNDROME; CELL GROWTH; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENETIC TRANSCRIPTION; GLYCOLYSIS; HUMAN; HUMAN CELL; HYPOXIA; KIDNEY CARCINOMA; KIDNEY CELL; KIDNEY INJURY; LIPID METABOLISM; PRIORITY JOURNAL; UPREGULATION;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIRT-HOGG-DUBE SYNDROME; BLOTTING, WESTERN; CARCINOMA, RENAL CELL; CELL LINE, TUMOR; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLYCOLYSIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; KIDNEY NEOPLASMS; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 79952536485     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.497     Document Type: Article

References (44)

1. Baba M, Hong S-B, Sharma N, Warren MB, Nickerson ML, Iwamatsu A et al. (2006). Folliculin encoded by the BHD gene interacts with a binding protein, FNIP1, and AMPK, and is involved in AMPK and mTOR signalling. P Natl Acad Sci USA 103: 15552-15557. (Pubitemid 44625630)
2. Bratslavsky G, Sudarshan S, Neckers L, Linehan WM. (2007). Pseudohypoxic pathways in renal cell carcinoma. Clin Cancer Res 13: 4667-4671. (Pubitemid 47294771)
3. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M et al. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622.
4. Chen Z, Lu W, Garcia-Prieto C, Huang P. (2007). The Warburg effect and its cancer therapeutic implications. J Bioenerg Biomembr 39: 267-274. (Pubitemid 47619379)
5. Deldicque L, Theisen D, Bertrand L, Hespel P, Hue L, Francaux M. (2007). Creatine enhances differentiation of myogenic C2C12 cells by activating both p38 and Akt/PKB pathways. Am J Physiol 293: 1263-1271.
6. Dunlop EA, Tee AR. (2009). Mammalian target of rapamycin complex 1: signalling inputs, substrates and feedback mechanisms. Cell Signal 21: 827-835.
7. 0 enhancer. Proc Natl Acad Sci USA 91: 6496-6500.
8. Galgani JE, Moro C, Ravussin E. (2008). Metabolic flexibility and insulin resistance. Am J Physiol 295: 1009-1017.
9. Gao L, Mejias R, Echevarria M, Lopez-Barneo J. (2004). Induction of the glucose-6-phosphate dehydrogenase gene expression by chronic hypoxia in PC12 cells. FEBS Lett 569: 256-260. (Pubitemid 38844628)
10. Garcia CK, Brown MS, Pathak RK, Goldstein JL. (1995). cDNA cloning of MCT2, a second monocarboxylate transporter expressed in different cells than MCT1. J Biol Chem 270: 1843-1849.
11. Guo K, Searfoss G, Krolikowski D, Pagnoni M, Franks C, Clark K et al. (2001). Hypoxia induces the expression of the pro-apoptotic gene BNIP3. Cell Death Differ 8: 367-376. (Pubitemid 32409607)
12. Gwinn DM, Shackelford DB, Egan DF, Mihaylova NM, Mery A, Vasquez DS et al. (2008). AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell Biol 30: 214-226. (Pubitemid 351626684)
13. Harrington LS, Findlay GM, Gray A, Tolkacheva T, Wigfield S, Rebholz H et al. (2004). The TSC1-2 tumour suppressor controls insulin-PI3K signaling via regulation of IRS proteins. J Cell Biol 166: 213-223. (Pubitemid 38988774)
14. Hartman TR, Nicolas E, Klein-Szanto A, Al-Saleem T, Cash TP, Simon MC et al. (2009). The role of the Birt-Hogg-Dube protein in mTOR activation and renal tumourigenesis. Oncogene 28: 1594-1604.
15. Hasumi Y, Baba M, Ailma R, Linehan W. (2009). Homozygous loss of BHD causes early embryonic lethality and kidney tumour development with activation of mTORC1 and mTORC2. Proc Natl Acad Sci USA 106: 18722-18727.
16. Hemminki K, Jiang Y, Ma X, Yang K, Egevand L, Lindbland P. (2002). Molecular epidemiology of VHL gene mutations in renal cell carcinoma patients: relation to dietary and other factors. Carcino-genesis 23: 809-815. (Pubitemid 34567520)
17. Hudson CC, Liu M, Chiang GG, Otterness DM, Loomis DC, Kaper F et al. (2002). Regulation of hypoxia-inducible factor 1alpha expression and function by the mammalian target of rapamycin. Mol Cell Biol 22: 7004-7014.
18. Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X et al. (2006). TSC2 integrates wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126: 955-968. (Pubitemid 44310775)
19. Isaacs JS, Jung YJ, Mole DR, Lee S, Torres-Cabala C, Chung Y-L et al. (2005). HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell 8: 143-153. (Pubitemid 41132743)
20. Kaelin WG. (2005). The von Hippel-Lindau protein, HIF hydroxy-lation, and oxygen sensing. Biochem Bioph Res Commun 338: 627-638.
21. Khoo SK, Giraud S, Kahnoski K, Chen J, Motorna O, Nickolov R et al. (2002). Clinical and genetic studies of Birt-Hogg-Dube syndrome. Med Genet 39: 906-912. (Pubitemid 36009152)
22. Kiuru M, Launonen V. (2004). Hereditary leiomyomatosis and renal cell cancer (HLRCC). Curr Mol Med 4: 869-875. (Pubitemid 39585732)
23. Land S, Tee A. (2007). Hypoxia-inducible factor 1alpha is regulated by the mammalian target of rapamycin (mTOR) via an mTOR signalling motif. J Biol Chem 282: 20534-20543. (Pubitemid 47100043)
24. Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S et al. (2009). Hypoxia-inducible factors regulate tumourigenic capacity of glioma stem cells. Cancer Cell 15: 501-513.
25. Liu MY, Poellinger L, Walker CL. (2003). Up-regulation of hypoxia-inducible factor 2 in renal cell carcinoma associated with loss of Tsc-2 tumour suppressor gene. Cancer Res 63: 2675-2680. (Pubitemid 36605212)
26. Maxwell PH. (2005). The HIF pathway in cancer. Semin Cell Dev Biol 16: 523-530. (Pubitemid 41247875)
27. Pelicano H, Martin DS, Xu R-H, Huang P. (2006). Glycolysis inhibition for anticancer treatment. Oncogene 25: 4633-4646. (Pubitemid 44187614)
28. Rapisarda A, Uranchimeg B, Scudiero DA, Selby M, Sausville EA, Shoemaker RH et al. (2002). Identification of small molecule inhibitors of hypoxia-inducible factor 1 transcriptional activation pathway. Cancer Res 62: 4316-4324. (Pubitemid 34827288)
29. Robey RB, Hay N. (2005). Akt, hexokinase, mTOR: targeting cellular energy metabolism for cancer therapy. Drug Discov Today 2: 239-246.
30. Roland I, Minet E, Ernest I, Pascal T, Michel G, Remacle J et al. (2000). Identification of hypoxia-responsive messengers expressed in human microvascular endothelial cells using differential display RT-PCR. Eur J Biochem 267: 3567-3574. (Pubitemid 30423017)
31. Semenza G. (2004). Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 19: 176-182. (Pubitemid 39481932)
32. Shah OJ, Hunter T. (2006). Turnover of the active fraction of IRS1 involves raptor-mTOR- and S6K1-dependent serine phosphory-lation in cell culture models of tuberous sclerosis. Mol Cell Biol 26: 6425-6434. (Pubitemid 44277883)
33. Slegtenhorst MV, Khabibullin D, Hartman TR, Nicolas E, Kruger WD, Henske EP. (2007). The Birt-Hogg-Dube and tuberous sclerosis complex homologs have opposing roles in amino acid homeostasis in schizosaccharomyces pombe. J Biol Chem 282: 24583-24590. (Pubitemid 47347553)
34. Sonveaux P, Vegran F, Schroeder T, Wergin MC, Verrax J, Rabbani ZN et al. (2008). Targeting lactate-fueled respiration selectively kills hypoxic tumour cells in mice. J Clin Invest 118: 3930-3942.
35. Suarez RK, Brown GS, Hochachka PW. (1986). Metabolic sources of energy for hummingbird flight. Am J Physiol 251: 537-542.
36. Sudarshan S, Sourbier C, Kong H-S, Block K, Romero VV, Yang Y et al. (2009). Fumarate hydratase deficiency in renal cancer induces glycolytic addiction and HIF-1 stabilisation by glucose-dependent generation of reactive oxygen species. Mol Cell Biol 29: 4080-4090.
37. Treins C, Murdaca J, Obberghen EV, Giorgetti-Peraldi S. (2006). AMPK activation inhibits the expression of HIF-1a induced by insulin and IGF-1. Biochem Bioph Res Commun 342: 1197-1202.
38. Van der Heiden MG, Cantley LC, Thompson CB. (2009). Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033.
39. Van de Velde C, Cizeau J, Dubik D, Alimonti J, Brown T, Israels S et al. (2000). BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol Cell Biol 20: 5454-5468. (Pubitemid 30482883)
40. Warburg O. (1956). The origin of cells. Science 123: 309-314.
41. Warburg O, Posener K, Negelein E. (1924). On the metabolism of tumours. Biochem Z 152: 319-344.
42. Wigfield SM, Winter SC, Giatromanolaki A, Taylor J, Koukourakis ML, Harris AL. (2008). PDK-1 regulates lactate production in hypoxia and is associated with poor prognosis in head and neck squamous cancer. Brit J Cancer 98: 1975-1984. (Pubitemid 351821556)
43. Woodward ER, Ricketts C, Killick P, Gad S, Morris MR, Kavalier F et al. (2008). Familial non-VHL clear cell (conventional) renal cell carcinoma: clinical features, segregation analysis, and mutation analysis of FLCN. Clin Cancer Res 14: 5925-5930.
44. Yang Y, Padilla-Nash HM, Vira MA, Abu-Asab MS, Val D, Worrell R et al. (2007). The UOK 257 cell line: a novel model for studies of the human Birt-Hogg-Dube gene pathway. Cancer Genet Cytogen 96: 336-340.