Pheochromocytomas: From genetic diversity to New Paradigms

Hormone and Metabolic Research

Volumn 41, Issue 9, 2009, Pages 664-671

  Qin, Y ^a   Buddavarapu, K ^a   Dahia, P L M ^a,b,c  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c University of Texas Health Science Center at San Antonio   (United States)

Author keywords

Adrenal medulla; Adrenal tumor; Hereditary cancer syndromes; Paraganglioma; Pheochromocytoma; Tumor suppressor gene

Indexed keywords

SUCCINATE DEHYDROGENASE;

APOPTOSIS; BIOENERGY; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CELL LINEAGE; CHROMAFFIN CELL; COMPLEX II DEFICIENCY; ENERGY METABOLISM; GENE MUTATION; GENETIC VARIABILITY; GLYCOLYSIS; HOMEOSTASIS; HUMAN; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PATHOGENESIS; PHENOTYPE; PHEOCHROMOCYTOMA; PRIORITY JOURNAL; PROTEIN DEPLETION; REVIEW;

ADRENAL GLAND NEOPLASMS; GENETIC VARIATION; HUMANS; MUTATION; PHEOCHROMOCYTOMA; SUCCINATE DEHYDROGENASE;

EID: 70350391394     PISSN: 00185043     EISSN: 14394286     Source Type: Journal    
DOI: 10.1055/s-0029-1215590     Document Type: Review

References (67)

1. Bravo EL. Pheochromocytoma. Cardiol Rev 2002 10 44-50
2. Mulligan LM, Kwok JBJ, Healey CS, Elsdon MJ, Eng C, Gardner E, Love DR, Mole SE, Moore JK, Papi L, Ponder MA, Telenius H, Tunnacliffe A, Ponder BAJ. Germline mutations of the RET proto-oncogene in multiple endocrine neoplasia type 2A. Nature 1993 363 458-460
3. Latif F, Tory K, Gnarra J, Yao M, Duh F-M, Orcutt M-L, Stackhouse T, Kuzmin I, Modi W, Geil L, Schmidt L, Zhou F, Weng Y, Duan DR, Dean M, Glavac D, Richards FM, Crossey PA, Ferguson-Smith MA, Le Paslier D, Chumakov I, Cohen D, Chinault CA, Maher ER, Linehan WM, Zbar B, Lerman MI. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 1993 260 1317-1320
4. Viskochil D, Buchberg AM, Xu G, Cawthon RM, Stevens J, Wolff RK, Culver M, Carey JC, Copeland NG, Jenkins NA, White R, OConnell P. Deletions and translocation interrupt a cloned gene at the neurofibromatosis type 1 locus. Cell 1990 62 187-192
5. Astuti D, Latif F, Dallol A, Dahia PL, Douglas F, George E, Skoldberg F, Husebye ES, Eng C, Maher ER. Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am J Hum Genet 2001 69 49-54
6. Niemann S, Muller U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat Genet 2000 26 268-270
7. Baysal BE, Ferrell RE, Willett-Brozick JE, Lawrence EC, Myssiorek D, Bosch A, van der Mey A, Taschner PE, Rubinstein WS, Myers EN, Richard CW, Cornelisse CJ, Devilee P, Devlin B. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 2000 287 848-851
8. Dahia PLM, Ross K, Wright ME, Hayashida CY, Santagata S, Barontini M, Kung AL, Sanso G, Powers JF, Tischler AS, Hodin R, Heitritter S, Moore F Jr, Dluhy R, Sosa JA, IT O, Benn DE, Marsh DJ, Robinson BG, Schneider K, Garber J, Arum SM, Korbonits M, Grossman A, Pigny P, Toledo SPA, Nosé V, Li C, Stiles CD. A HIF1a regulatory loop links hypoxia and mitochondrial signals in pheochromocytomas. PLoS Genet 2005 1 e8
9. Eisenhofer G, Siegert G, Kotzerke J, Bornstein SR, Pacak K. Current progress and future challenges in the biochemical diagnosis and treatment of pheochromocytomas and paragangliomas. Horm Metab Res 2008 40 329-337
10. Dahia PLM, Hao K, Rogus J, Colin C, Pujana MAG, Ross K, Magoffin D, Aronin N, Cascon A, Hayashida CY, Li C, Toledo SPA, Stiles CD, Consortium ftFP. Novel pheochromocytoma susceptibility loci identified by integrative genomics. Cancer Res 2005 65 9651-9658
11. Gottlieb E, Tomlinson IP. Mitochondrial tumour suppressors: a genetic and biochemical update. Nat Rev Cancer 2005 5 857-866
12. Gimenez-Roqueplo AP, Favier J, Rustin P, Rieubland C, Crespin M, Nau V, Van Kien PK, Corvol P, Plouin PF, Jeunemaitre X. Mutations in the SDHB gene are associated with extra-adrenal and/or malignant phaeochromocytomas. Cancer Res 2003 63 5615-5621
13. Amar L, Baudin E, Burnichon N, Peyrard S, Silvera S, Bertherat J, Bertagna X, Schlumberger M, Jeunemaitre X, Gimenez-Roqueplo AP, Plouin PF. Succinate dehydrogenase B gene mutations predict survival in patients with malignant pheochromocytomas or paragangliomas. J Clin Endocrinol Metab 2007 92 3822-3828
14. Gimenez-Roqueplo AP, Favier J, Rustin P, Mourad JJ, Plouin PF, 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 2001 69 1186-1197
15. Gimenez-Roqueplo AP, Favier J, Rustin P, Rieubland C, Kerlan V, Plouin PF, Rotig A, Jeunemaitre X. Functional consequences of a SDHB gene mutation in an apparently sporadic pheochromocytoma. J Clin Endocrinol Metab 2002 87 4771-4774
16. Pollard PJ, Briere JJ, Alam NA, Barwell J, Barclay E, Wortham NC, Hunt T, Mitchell M, Olpin S, Moat SJ, Hargreaves IP, Heales SJ, Chung YL, Griffiths JR, Dalgleish A, McGrath JA, Gleeson MJ, Hodgson SV, Poulsom R, Rustin P, Tomlinson IP. Accumulation of Krebs cycle intermediates and over-expression of HIF1alpha in tumours which result from germline FH and SDH mutations. Hum Mol Genet 2005 14 2231-2239
17. Selak MA, Armour SM, Mackenzie ED, Boulahbel H, Watson DG, Mansfield KD, Pan Y, Simon MC, Thompson CB, Gottlieb E. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 2005 7 77-85
18. Lee S, Nakamura E, Yang H, Wei W, Linggi MS, Sajan MP, Farese RV, Freeman RS, Carter BD, Kaelin WG Jr, Schlisio S. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: Developmental culling and cancer. Cancer Cell 2005 8 155-167
19. Ishii T, Yasuda K, Akatsuka A, Hino O, Hartman PS, Ishii N. A mutation in the SDHC gene of complex II increases oxidative stress, resulting in apoptosis and tumorigenesis. Cancer Res 2005 65 203-209
20. Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT. Loss of the SdhB, but Not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol Cell Biol 2008 28 718-731
21. Smith EH, Janknecht R, Maher LJ 3rd. Succinate inhibition of {alpha}-ketoglutarate-dependent enzymes in a yeast model of paraganglioma. Hum Mol Genet 2007 16 3136-3148
22. Cervera AM, Apostolova N, Crespo FL, Mata M, MacCreath KJ. Cells silenced for SDHB expression display characteristic features of the tumor phenotype. Cancer Res 2008 68 4058-4067
23. Guo J, Lemire BD. The ubiquinone-binding site of the Saccharomyces cerevisiae succinate-ubiquinone oxidoreductase is a source of superoxide. J Biol Chem 2003 278 47629-47635
24. Piruat JI, Pintado CO, Ortega-Saenz P, Roche M, Lopez-Barneo J. The mitochondrial SDHD gene is required for early embryogenesis, and its partial deficiency results in persistent carotid body glomus cell activation with full responsiveness to hypoxia. Mol Cell Biol 2004 24 10933-10940
25. Timmers HJ, Kozupa A, Chen CC, Carrasquillo JA, Ling A, Eisenhofer G, Adams KT, Solis D, Lenders JW, Pacak K. Superiority of fluorodeoxyglucose positron emission tomography to other functional imaging techniques in the evaluation of metastatic SDHB-associated pheochromocytoma and paraganglioma. J Clin Oncol 2007 25 2262-2269
26. Pelicano H, Martin DS, Xu RH, Huang P. Glycolysis inhibition for anticancer treatment. Oncogene 2006 25 4633-4646
27. Fantin VR, St-Pierre J, Leder P. Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 2006 9 425-434
28. Bonnet S, Archer SL, Allalunis-Turner J, Haromy A, Beaulieu C, Thompson R, Lee CT, Lopaschuk GD, Puttagunta L, Harry G, Hashimoto K, Porter CJ, Andrade MA, Thebaud B, Michelakis ED. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 2007 11 37-51
29. Kondo K, Kim WY, Lechpammer M, Kaelin WG Jr. Inhibition of HIF2alpha Is Sufficient to Suppress pVHL-Defective Tumor Growth. PLoS Biol 2003 1 E83
30. Kondo K, Klco J, Nakamura E, Lechpammer M, William G, Kaelin WG Jr. Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein. Cancer Cell 2002 1 237-246
31. Eisenhofer G, Huynh T-T, Pacak K, Brouwers FM, Walther MM, Linehan WM, Munson PJ, Mannelli M, Goldstein D S, Elkahloun AG. 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 2004 11 897-911
32. Maranchie JK, Vasselli JR, Riss J, Bonifacino JS, Linehan WM, Klausner RD. The contribution of VHL substrate binding and HIF1- to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell 2002 1 247-255
33. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 2006 3 187-197
34. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: A metabolic switch required for cellular adaptation to hypoxia. Cell Metab 2006 3 177-185
35. Gordan JD, Thompson CB, Simon MC. HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 2007 12 108-113
36. Kim JW, Gao P, Liu YC, Semenza GL, Dang CV. 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 2007 27 7381-7393
37. Korpershoek E, Van Nederveen FH, Dannenberg H, Petri BJ, Komminoth P, Perren A, Lenders JW, Verhofstad AA, De Herder WW, De Krijger RR, Dinjens WN. Genetic analyses of apparently sporadic pheochromocytomas: the Rotterdam experience. Ann N Y Acad Sci 2006 1073 138-148
38. Maris JM, Weiss MJ, Mosse Y, Hii G, Guo C, White PS, Hogarty MD, Mirensky T, Brodeur GM, Rebbeck TR, Urbanek M, Shusterman S. Evidence for a hereditary neuroblastoma predisposition locus at chromosome 16p12-13. Cancer Res 2002 62 6651-6658
39. Gimenez-Roqueplo AP, Burnichon N, Amar L, Favier J, Jeunemaitre X, Plouin PF. Recent advances in the genetics of phaeochromocytoma and functional paraganglioma. Clin Exp Pharmacol Physiol 2008 35 376-379
40. Bornstein SR, Gimenez-Roqueplo AP. Genetic testing in pheochromocytoma: increasing importance for clinical decision making. Ann N Y Acad Sci 2006 1073 94-103
41. Bausch B, Boedeker CC, Berlis A, Brink I, Cybulla M, Walz MK, Januszewicz A, Letizia C, Opocher G, Eng C, Neumann HP. Genetic and clinical investigation of pheochromocytoma: a 22-year experience, from Freiburg, Germany to international effort. Ann N Y Acad Sci 2006 1073 122-137
42. Ladroue C, Carcenac R, Leporrier M, Gad S, Le Hello C, Galateau-Salle F, Feunteun J, Pouyssegur J, Richard S, Gardie B. PHD2 mutation and congenital erythrocytosis with paraganglioma. N Engl J Med 2008 359 2685-2692
43. Schlisio S, Kenchappa RS, Vredeveld LC, George RE, Stewart R, Greulich H, Shahriari K, Nguyen NV, Pigny P, Dahia PL, Pomeroy SL, Maris JM, Look AT, Meyerson M, Peeper DS, Carter BD, Kaelin Jr WG. The kinesin KIF1Bbeta acts downstream from EglN3 to induce apoptosis and is a potential 1p36 tumor suppressor. Genes Dev 2008 22 884-893
44. Zhao C, Takita J, Tanaka Y, Setou M, Nakagawa T, Takeda S, Yang HW, Terada S, Nakata T, Takei Y, Saito M, Tsuji S, Hayashi Y, Hirokawa N. Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta. Cell 2001 105 587-597
45. Benn DE, Dwight T, Richardson AL, Delbridge L, Bambach CP, Stowasser M, Gordon RD, Marsh DJ, Robinson BG. Sporadic and familial pheochromocytomas are associated with loss of at least two discrete intervals on chromosome 1p. Cancer Res 2000 60 7048-7051
46. Yeh IT, Lenci RE, Qin Y, Buddavarapu K, Ligon AH, Leteurtre E, Cao CD, Cardot-Bauters C, Pigny P, Dahia PL. A germline mutation of the KIF1Bbeta gene on 1p36 in a family with neural and nonneural tumors. Hum Genet 2008
47. Munirajan AK, Ando K, Mukai A, Takahashi M, Suenaga Y, Ohira M, Koda T, Hirota T, Ozaki T, Nakagawara A. KIF1Bbeta functions as a haploinsufficient tumor suppressor gene mapped to chromosome 1p36.2 by inducing apoptotic cell death. J Biol Chem 2008 283 24426-24434
48. Mullighan CG, Goorha S, Radtke I, Miller CB, Coustan-Smith E, Dalton JD, Girtman K, Mathew S, Ma J, Pounds SB, Su X, Pui CH, Relling MV, Evans WE, Shurtleff SA, Downing JR. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 2007 446 758-764
49. Ebert BL, Pretz J, Bosco J, Chang CY, Tamayo P, Galili N, Raza A, Root DE, Attar E, Ellis SR, Golub TR. Identification of RPS14 as a 5q- syndrome gene by RNA interference screen. 2008 451 335-339
50. Mannelli M, Simi L, Gagliano MS, Opocher G, Ercolino T, Becherini L, Parenti G. Genetics and biology of pheochromocytoma. Exp Clin Endocrinol Diabetes 2007 115 160-165
51. Walther MM, Herring J, Enquist E, Keiser HR, Linehan WM. von Recklinghausen's disease and pheochromocytomas. J Urol 1999 162 1582-1586
52. Vanharanta S, Buchta M, MacWhinney SR, Virta SK, Peczkowska M, Morrison CD, Lehtonen R, Januszewicz A, Jarvinen H, Juhola M, Mecklin JP, Pukkala E, Herva R, Kiuru M, Nupponen NN, Aaltonen LA, Neumann HP, Eng C. Early-onset renal cell carcinoma as a novel extraparaganglial component of SDHB-associated heritable paraganglioma. Am J Hum Genet 2004 74 153-159
53. Ricketts C, Woodward ER, Killick P, Morris MR, Astuti D, Latif F, Maher ER. Germline SDHB mutations and familial renal cell carcinoma. J Natl Cancer Inst 2008 100 1260-1262
54. MacWhinney SR, Pasini B, Stratakis CA, The International Carney Triad Carney-Stratakis Syndrome Consortium. Familial Gastrointestinal Stromal Tumors and Germ-Line Mutations. N Engl J Med 2007 357 1054-1056
55. Zbuk KM, Patocs A, Shealy A, Sylvester H, Miesfeldt S, Eng C. Germline mutations in PTEN and SDHC in a woman with epithelial thyroid cancer and carotid paraganglioma. Nat Clin Pract Oncol 2007 4 608-612
56. Benn DE, Gimenez-Roqueplo AP, Reilly JR, Bertherat J, Burgess J, Byth K, Croxson M, Dahia PL, Elston M, Gimm O, Henley D, Herman P, Murday V, Niccoli-Sire P, Pasieka JL, Rohmer V, Tucker K, Jeunemaitre X, Marsh DJ, Plouin PF, Robinson BG. Clinical presentation and penetrance of Pheochromocytoma/ Paraganglioma syndromes. J Clin Endocrinol Metab 2006 91 827-836
57. Cascon A, Landa I, Lopez-Jimenez E, Diez-Hernandez A, Buchta M, Montero-Conde C, Leskela S, Leandro-Garcia LJ, Leton R, Rodriguez-Antona C, Eng C, Neumann HP, Robledo M. Molecular characterisation of a common SDHB deletion in paraganglioma patients. J Med Genet 2008 45 233-238
58. Ni Y, Zbuk KM, Sadler T, Patocs A, Lobo G, Edelman E, Platzer P, Orloff MS, Waite KA, Eng C. Germline mutations and variants in the succinate dehydrogenase genes in Cowden and Cowden-like syndromes. Am J Hum Genet 2008 83 261-268
59. Brannan CI, Perkins AS, Vogel KS, Ratner N, Nordlund ML, Reid SW, Buchberg AM, Jenkins NA, Parada LF, Copeland NG. Targeted disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev 1994 8 1019-1029
60. Jacks T, Shih TS, Schmitt EM, Bronson RT, Bernards A, Weinberg RA. Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nat Genet 1994 7 353-361
61. Vogel KS, Brannan CI, Jenkins NA, Copeland NG, Parada LF. Loss of neurofibromin results in neurotrophin-independent survival of embryonic sensory and sympathetic neurons. Cell 1995 82 733-742
62. Bishop T, Gallagher D, Pascual A, Lygate CA, de Bono JP, Nicholls LG, Ortega-Saenz P, Oster H, Wijeyekoon B, Sutherland AI, Grosfeld A, Aragones J, Schneider M, van Geyte K, Teixeira D, Diez-Juan A, Lopez-Barneo J, Channon KM, Maxwell PH, Pugh CW, Davies AM, Carmeliet P, Ratcliffe PJ. Abnormal sympathoadrenal development and systemic hypotension in PHD3-/- mice. Mol Cell Biol 2008 28 3386-3400
63. Quartu M, Serra MP, Boi M, Ferretti MT, Lai ML, Del Fiacco M. Tissue distribution of Ret, GFRalpha-1, GFRalpha-2 and GFRalpha-3 receptors in the human brainstem at fetal, neonatal and adult age. Brain Res 2007 1173 36-52 (Pubitemid 47449691)
64. Kim WY, Sharpless NE. VHL Inactivation: A New Road to Senescence. Cancer Cell 2008 13 295-297
65. Campisi J, dAdda di Fagagna F. Cellular senescence: when bad things happen to good cells. 2007 8 729-740
66. Young AP, Schlisio S, Minamishima YA, Zhang Q, Li L, Grisanzio C, Signoretti S, Kaelin Jr WG. VHL loss actuates a HIF-independent senescence programme mediated by Rb and p400. Nat Cell Biol 2008 10 361-369
67. Pasini B, MacWhinney SR, Bei T, Matyakhina L, Stergiopoulos S, Muchow M, Boikos SA, Ferrando B, Pacak K, Assie G, Baudin E, Chompret A, Ellison JW, Briere JJ, Rustin P, Gimenez-Roqueplo AP, Eng C, Carney JA, Stratakis CA. Clinical and molecular genetics of patients with the Carney-Stratakis syndrome and germline mutations of the genes coding for the succinate dehydrogenase subunits SDHB, SDHC, and SDHD. Eur J Hum Genet 2008 16 79-88