The Warburg effect is genetically determined in inherited pheochromocytomas

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Favier, Judith ^a,b,c,d   Brière, Jean Jacques ^e,f   Burnichon, Nelly ^a,b,c,d   Rivière, Julie ^a,b,c,d   Vescovo, Laure ^g   Benit, Paule ^e   Giscos Douriez, Isabelle ^a,b,c   De Reyniès, Aurélien ^g   Bertherat, Jérôme ^c,h,i   Badoual, Cécile ^c,d   Tissier, Frédérique ^c,h   Amar, Laurence ^d   Libé, Rosella ^h   Plouin, Pierre François ^a,c,d,i   Jeunemaitre, Xavier ^a,b,c,d   Rustin, Pierre ^e   Gimenez Roqueplo, Anne Paule ^a,b,c,d,i  

^a PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^b l'alimentation et l'Environnement   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^e HÔPITAL ROBERT DEBRÉ   (France)

^f René Diderot University   (France)

^g Programme Cartes d'Identite des Tumeurs CIT   (France)

^h Service d'Anatomo Pathologie ^*  (France)

ⁱ INSTITUT NATIONAL DU CANCER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROFIBROMIN; PROTEIN P53; PROTEIN RET; SUCCINATE DEHYDROGENASE; VON HIPPEL LINDAU PROTEIN;

ADOLESCENT; ADULT; AGED; ARTICLE; CELL FUNCTION; CHILD; CONTROLLED STUDY; ENERGY METABOLISM; FEMALE; GENE MUTATION; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; HUMAN; HUMAN TISSUE; HYPOXIA; MALE; MICROARRAY ANALYSIS; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; PHEOCHROMOCYTOMA; PROTEIN EXPRESSION; TUMOR VASCULARIZATION; VON HIPPEL LINDAU DISEASE; WARBURG EFFECT; ANOXIA; DNA MICROARRAY; ELECTRON TRANSPORT; GENETICS; GLYCOLYSIS; METABOLISM; MIDDLE AGED; MITOCHONDRION; MUTATION; NEOVASCULARIZATION (PATHOLOGY); OXIDATIVE PHOSPHORYLATION; PATHOPHYSIOLOGY; TUMOR SUPPRESSOR GENE;

ADOLESCENT; ADULT; AGED; ANOXIA; CHILD; ELECTRON TRANSPORT; FEMALE; GENES, P53; GERM-LINE MUTATION; GLYCOLYSIS; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIA; NEOVASCULARIZATION, PATHOLOGIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE PHOSPHORYLATION; PHEOCHROMOCYTOMA;

EID: 70349472696     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007094     Document Type: Article

References (42)

1. Warburg O (1930) Ueber den stoffwechsel der tumoren. Constable, London.
2. Warburg O (1956) On respiratory impairment in cancer cells. Science 124: 269-270.
3. Rustin P, Kroemer G (2007) Mitochondria and cancer. Ernst Shering Res Found Workshop 62.
4. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033.
5. Samudio I, Fiegl M, Andreeff M (2009) Mitochondrial uncoupling and the Warburg effect: molecular basis for the reprogramming of cancer cell metabolism. Cancer Res 69: 2163-2166.
6. Unwin RD, Craven RA, Harnden P, Hanrahan S, Totty N, et al. (2003) Proteomic changes in renal cancer and co-ordinate demonstration of both the glycolytic and mitochondrial aspects of the Warburg effect. Proteomics 3: 1620-1632.
7. Kim WY, Kaelin WG (2004) Role of VHL gene mutation in human cancer. J Clin Oncol 22: 4991-5004.
8. Hervouet E, Demont J, Pecina P, Vojtiskova A, Houstek J, et al. (2005) A new role for the von Hippel-Lindau tumor suppressor protein: stimulation of mitochondrial oxidative phosphorylation complex biogenesis. Carcinogenesis 26: 531-539.
9. Craven RA, Stanley AJ, Hanrahan S, Dods J, Unwin R, et al. (2006) Proteomic analysis of primary cell lines identifies protein changes present in renal cell carcinoma. Proteomics 6: 2853-2864.
10. Amar L, Bertherat J, Baudin E, Ajzenberg C, Bressac-de Paillerets B, et al. (2005) Genetic testing in pheochromocytoma or functional paraganglioma. J Clin Oncol 23: 8812-8818.
11. Favier J, Briere JJ, Strompf L, Amar L, Filali M, et al. (2005) Hereditary paraganglioma/pheochromocytoma and inherited succinate dehydrogenase deficiency. Horm Res 63: 171-179.
12. King A, Selak MA, Gottlieb E (2006) Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer. Oncogene 25: 4675-4682.
13. Eisenhofer G, Huynh TT, Pacak K, Brouwers FM, Walther MM, et al. (2004) Distinct gene expression profiles in norepinephrine- and epinephrine-producing hereditary and sporadic pheochromocytomas: activation of hypoxia-driven angiogenic pathways in von Hippel-Lindau syndrome. Endocr Relat Cancer 11: 897-911.
14. Dahia PL, Ross KN, Wright ME, Hayashida CY, Santagata S, et al. (2005) A HIF1alpha regulatory loop links hypoxia and mitochondrial signals in pheochromocytomas. PLoS Genet 1: 72-80.
15. Briere JJ, Favier J, Benit P, El Ghouzzi V, Lorenzato A, et al. (2005) Mitochondrial succinate is instrumental for HIF1alpha nuclear translocation in SDHA-mutant fibroblasts under normoxic conditions. Hum Mol Genet 14: 3263-3269.
16. Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, et al. (2005) Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7: 77-85.
17. Yeung SJ, Pan J, Lee MH (2008) Roles of p53, MYC and HIF-1 in regulating glycolysis - the seventh hallmark of cancer. Cell Mol Life Sci 65: 3981-3999.
18. van Nederveen FH, Gaal J, Favier J, Korpershoek E, Oldenburg RA, et al. (2009) An immunohistochemical procedure to detect patients with paraganglioma and phaeochromocytoma with germline SDHB, SDHC, or SDHD gene mutations: a retrospective and prospective analysis. Lancet Oncol.
19. Mathupala SP, Ko YH, Pedersen PL (2009) Hexokinase-2 bound to mitochondria: cancer's stygian link to the "Warburg Effect" and a pivotal target for effective therapy. Semin Cancer Biol 19: 17-24.
20. Roe JS, Kim H, Lee SM, Kim ST, Cho EJ, et al. (2006) p53 stabilization and transactivation by a von Hippel-Lindau protein. Mol Cell 22: 395-405.
21. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, et al. (2006) TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126: 107-120.
22. Semenza GL (2003) Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732.
23. Zhang H, Gao P, Fukuda R, Kumar G, Krishnamachary B, et al. (2007) HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 11: 407-420.
24. Uldry M, Yang W, St-Pierre J, Lin J, Seale P, et al. (2006) Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab 3: 333-341.
25. Kim JW, Gao P, Liu YC, Semenza GL, Dang CV (2007) Hypoxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1. Mol Cell Biol 27: 7381-7393.
26. Fukuda R, Zhang H, Kim JW, Shimoda L, Dang CV, et al. (2007) HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129: 111-122.
27. Fredlund E, Ovenberger M, Borg K, Pahlman S (2008) Transcriptional adaptation of neuroblastoma cells to hypoxia. Biochem Biophys Res Commun 366: 1054-1060.
28. Zelinka T, Timmers HJ, Kozupa A, Chen CC, Carrasquillo JA, et al. (2008) Role of positron emission tomography and bone scintigraphy in the evaluation of bone involvement in metastatic pheochromocytoma and paraganglioma: specific implications for succinate dehydrogenase enzyme subunit B gene mutations. Endocr Relat Cancer 15: 311-323.
29. Hu CJ, Iyer S, Sataur A, Covello KL, Chodosh LA, et al. (2006) Differential regulation of the transcriptional activities of hypoxia-inducible factor 1 alpha (HIF-1alpha) and HIF-2alpha in stem cells. Mol Cell Biol 26: 3514-3526.
30. Pollard PJ, El-Bahrawy M, Poulsom R, Elia G, Killick P, et al. (2006) Expression of HIF-1alpha, HIF-2alpha (EPAS1), and their target genes in paraganglioma and pheochromocytoma with VHL and SDH mutations. J Clin Endocrinol Metab 91: 4593-4598.
31. Favier J, Kempf H, Corvol P, Gasc J (1999) Cloning and expression pattern of EPAS1 in the chicken embryo. Colocalization with tyrosine hydroxylase. FEBS Lett 462: 19-24.
32. Nilsson H, Jogi A, Beckman S, Harris AL, Poellinger L, et al. (2005) HIF-2alpha expression in human fetal paraganglia and neuroblastoma: relation to sympathetic differentiation, glucose deficiency, and hypoxia. Exp Cell Res 303: 447-456.
33. 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.
34. Lebedeva MA, Eaton JS, Shadel GS (2009) Loss of p53 causes mitochondrial DNA depletion and altered mitochondrial reactive oxygen species homeostasis. Biochim Biophys Acta 1787: 328-334.
35. Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, et al. (2006) p53 regulates mitochondrial respiration. Science 312: 1650-1653.
36. Herfarth KK, Wick MR, Marshall HN, Gartner E, Lum S, et al. (1997) Absence of TP53 alterations in pheochromocytomas and medullary thyroid carcinomas. Genes Chromosomes Cancer 20: 24-29.
37. Petri BJ, Speel EJ, Korpershoek E, Claessen SM, van Nederveen FH, et al. (2008) Frequent loss of 17p, but no p53 mutations or protein overexpression in benign and malignant pheochromocytomas. Mod Pathol 21: 407-413.
38. Yoshimoto T, Naruse M, Zeng Z, Nishikawa T, Kasajima T, et al. (1998) The relatively high frequency of p53 gene mutations in multiple and malignant phaeochromocytomas. J Endocrinol 159: 247-255.
39. Amar L, Baudin E, Burnichon N, Peyrard S, Silvera S, et al. (2007) Succinate dehydrogenase B gene mutations predict survival in patients with malignant pheochromocytomas or paragangliomas. J Clin Endocrinol Metab 92: 3822-3828.
40. Benit P, Goncalves S, Philippe Dassa E, Briere JJ, Martin G, et al. (2006) Three spectrophotometric assays for the measurement of the five respiratory chain complexes in minuscule biological samples. Clin Chim Acta 374: 81-86.
41. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
42. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.