Clinical and molecular progress in hereditary paraganglioma

Journal of Medical Genetics

Volumn 45, Issue 11, 2008, Pages 689-694

  Baysal, Bora E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; REACTIVE OXYGEN METABOLITE; SUCCINATE DEHYDROGENASE; SUCCINIC ACID; VON HIPPEL LINDAU PROTEIN;

ADRENAL MEDULLA TUMOR; CARCINOGENESIS; CHROMOSOME 11Q; GENE MUTATION; GENETIC PREDISPOSITION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENOTYPE PHENOTYPE CORRELATION; HEAD AND NECK TUMOR; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; OXYGEN SENSING; PARAGANGLIOMA; PENETRANCE; PHEOCHROMOCYTOMA; PREVALENCE; PRIORITY JOURNAL; REVIEW; TUMOR SUPPRESSOR GENE; VASCULAR TUMOR;

ADRENAL GLAND NEOPLASMS; GERM-LINE MUTATION; HEAD AND NECK NEOPLASMS; HUMANS; PARAGANGLIOMA; SUCCINATE DEHYDROGENASE;

EID: 56049122457     PISSN: 00222593     EISSN: 14686244     Source Type: Journal    
DOI: 10.1136/jmg.2008.058560     Document Type: Review

References (61)

1. Gonzalez C, Almaraz L, Obeso A, Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev 1994;74:829-98.
2. Baysal BE. Hereditary paraganglioma targets diverse paraganglia. J Med Genet 2002;39:617-22.
3. Baysal BE, Ferrell RE, Willett-Brozick JE, Lawrence EC, Myssiorek D, Bosch A, van der MA, Taschner PE, Rubinstein WS, Myers EN, Richard CW, III, Cornelisse CJ, Devilee P, Devlin B. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 2000;287:848-51.
4. Niemann S, Muller U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat Genet 2000;26:268-70.
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 pheochromocytorna and to familial paraganglioma. Am J Hum Genet 2001;69:49-54.
6. Bourgeron T, Rustin P, Chretien D, Birch-Machin M, Bourgeois M, Viegas-Pequignot E, Munnich A, Rotig A. Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nat Genet 1995;11:144-9.
7. Baysal BE, Willett-Brozick JE, Lawrence EC, Drovdlic CM, Savul SA, McLeod DR, Yee HA, Brackmann DE, Slattery WH, III, Myers EN, Ferrell RE, Rubinstein WS. Prevalence of SDHB, SDHC, and SDHD germline mutations in clinic patients with head and neck paragangliomas. J Med Genet 2002;39:178-83.
8. Baysal BE, Willett-Brozick JE, Filho PA, Lawrence EC, Myers EN, Ferrell RE. An Alumediated partial SDHC deletion causes familial and sporadic paraganglioma. J Med Genet 2004;41:703-9.
9. Taschner PE, Jansen JC, Baysal BE, Bosch A, Rosenberg EH, Brocker-Vriends AH, Der May AG, van Ommen GJ, Cornelisse CJ, Devilee P. Nearly all hereditary paragangliomas in the Netherlands are caused by two founder mutations in the SDHD gene. Genes Chromosomes Cancer 2001;31:274-81.
10. Bayley JP, van M, I, Weiss MM, Jansen JC, Oomen PH, Menko FH, Pasini B, Ferrando B, Wong N, Alpert LC, Williams R, Blair E, Devilee P, Taschner PE. Mutation analysis of SDHB and SDHC: novel germline mutations in sporadic head and neck paraganglioma and familial paraganglioma and/or pheochromocytoma. BMC Med Genet 2006; 7:1.
11. Badenhop RF, Jansen JC, Fagan PA, Lord RS, Wang ZG, Foster WJ, Schofield PR. The prevalence of SDHB, SDHC, and SDHD mutations in patients with head and neck paragangliorna and association of mutations with clinical features. J Med Genet 2004; 41:e99.
12. Astuti D, Hart-Holden N, Latif F, Lalloo F, Black GC, Lim C, Moran A, Grossman AB, Hodgson SV, Freemont A, Ramsden R, Eng C, Evans DG, Maher ER. Genetic analysis of mitochondrial complex II subunits SDHD, SDHB and SDHC in paraganglioma and phaeochromocytoma susceptibility. Clin Endocrinol (Oxf) 2003;59:728-33.
13. Lima J, Feijao T, Ferreira dS, Pereira-Castro I, Fernandez-Ballester G, Maximo V, Herrero A, Serrano L, Sobrinho-Simoes M, Garcia-Rostan G. High frequency of germline succinate dehydrogenase mutations in sporadic cervical paragangliomas in northern Spain: mitochondrial succinate dehydrogenase structure-function relationships and clinical-pathological correlations. J Clin Endocrinol Metab 2007;92:4853-864.
14. Fakhry N, Niccoli-Sire P, Barlier-Seti A, Giorgi R, Giovanni A, Zanaret M. Cervical paragangliomas: is SDH genetic analysis systematically required? Eur Arch Otorhinolaryngol 2008; 265:557-63.
15. Schiavi F, Savvoukidis T, Trabalzini F, Grego F, Piazza M, Amista P, Dematte S, Del Piano A, Cecchini ME, Erlic Z, De Lazzari P, Mantero F, Opocher G. Paraganglioma syndrome: SDHB, SDHC, and SDHD mutations in head and neck paragangliomas, Ann N Y Acad Sci 2006;1073:190-7.
16. Neumann HP, Bausch B, McWhinney SR, Bender BU, Gimm O, Franke G, Schipper J, Klisch J, Altehoefer C, Zerres K, Januszewicz A, Eng C, Smith WM, Munk R, Manz T, Glaesker S, Apel TW, Treier M, Reineke M, Walz MK, Hoang-Vu C, Brauckhoff M, Klein-Franke A, Klose P, Schmidt H, Maier-Woelfle M, Peczkowska M, Szmigielski C, Eng C. Germ-line mutations in nonsyndromic pheochromocytoma. N Engl J Med 2002; 346:1459-66
17. Amar L, Bertherat J, Baudin E, Ajzenberg C, Bressac-de Paillerets B, Chabre O, Chamontin B, Delemer B, Giraud S, Murat A, Niccoli-Sire P, Richard S, Rohmer V, Sadoul JL, Strompf L, Schlumberger M, Bertagna X, Plouin PF, Jeunemaitre X, Gimenez-Roqueplo AP. Genetic testing in pheochromocytoma or functional paraganglioma. J Clin Oncol 2005; 23:8812-18.
18. Korpershoek E, Petri BJ, van Nederveen FH, Dinjens WN, Verhofstad AA, de Herder WW, Schmid S, Perren A, Komminoth P, de Krijger RR. Candidate gene mutation analysis in bilateral adrenal pheochromocytoma and sympathetic paraganglioma. Endocr Relat Cancer 2007; 14:453-62.
19. Castellano M, Mori L, Giacche M, Agliozzo E, Tosini R, Panarotto A, Cappelli C, Mulatero P, Cumetti O, Veglio F, Agabiti-Rosei E. Genetic mutation screening in an italian cohort of nonsyndromic pheochromocytoma/ paraganglioma patients. Ann N Y Acad Sci 2006;1073:156-65.
20. Isobe K, Minowada S, Tatsuno I, Suzukawa K, Nissato S, Nanmoku T, Hara H, Yashiro T, Kawakami Y, Takekoshi K. Novel germline mutations in the SDHB and SDHD genes in Japanese pheochromocytomas. Horm Res 2007;68:68-71.
21. Schiavi F, Boedeker CC, Bausch B, Peczkowska M, Gomez CF, Strassburg T, Pawlu C, Buchta M, Salzmann M, Hoffmann MM, Berlis A, Brink I, Cybulla M, Muresan M, Walter MA, Forrer F, Valimaki M, Kawecki A, Szutkowski Z, Schipper J, Walz MK, Pigny P, Bauters C, Willet-Brozick JE, Baysal BE, Januszewicz A, Eng C, Opocher G, Neumann HP. Predictors and prevalence of paraganglioma syndrome associated with mutations of the SDHC gene. JAMA 2005;294:2057-63.
22. Mannelli M, Ercolino T, Giache V, Simi L, Cirami C, Parenti G. Genetic screening for pheochromocytoma: should SDHC gene analysis be included? J Med Genet 2007;44:586-7.
23. McWhinney SR, Pilarski RT, Forrester SR, Schneider MC, Sarquis MM, Dias EP, Eng C. Large germline deletions of mitochondrial complex II subunits SDHB and SDHD in hereditary paraganglioma. J Clin Endocrinol Metab 2004;89:5694-9.
24. Cascon A, Montero-Conde C, Ruiz-Llorente S, Mercadillo F, Leton R, Rodriguez-Antona C, Martinez-Delgado B, Delgado M, Diez A, Rovira A, Diaz JA, Robledo M. Gross SDHB deletions in patients with paraganglioma detected by multiplex PCR: a possible hot spot? Genes Chromosomes Cancer 2006;45:213-19.
25. Pigny P, Vincent A, Bauters CC, Bertrand M, de Montpreville VT, Crepin M, Porchet N, Caron P. Paraganglioma after maternal transmission of a succinate dehydrogenase gene mutation. J Clin Endocrinol Metab 2008;93:1609-15.
26. 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 pheochromacytoma/paraganglioma syndromes. J Clin Endocrinol Metab 2006;91:827-36.
27. Neumann HP, Pawlu C, Peczkowska M, Bausch B, McWhinney SR, Muresan M, Buchta M, Franke G, Klisch J, Bley TA, Hoegerle S, Boedeker CC, Opocher G, Schipper J, Januszewicz A, Eng C. Distinct clinical features of paraganglioma syndromes associated with SDHB and SDHD gene mutations. JAMA 2004;292:943-51.
28. Timmers HJ, Kozupa A, Eisenhofer G, Raygada M, Adams KT, Solis D, Lenders JW, Pacak K. Clinical presentations, biochemical phenotypes, and genotype-phenotype correlations in patients with succinate dehydrogenase subunit B-associated pheochromocytomas and paragangliomas. J Clin Endocrinol Metab 2007:92:779-86.
29. Brouwers FM, Eisenhofer G, Tao JJ, Kant JA, Adams KT, Linehan WM, Pacak K. High frequency of SDHB germline mutations in patients with malignant catecholamine-producing paragangliomas: implications for genetic testing. J Clin Endocrinol Metab 2006;91:4505-9.
30. Astrom K, Cohen JE, Willett-Brozick JE, Aston CE, Baysal BE. Altitude is a phenotypic modifier in hereditary paraganglioma type 1: evidence for an oxygen-sensing defect. Hum Genet 2003; 113:228-37.
31. Pasini B, McWhinney SR, Bei T, Matyakhina L, Stergiopoulos S, Muchow M, Boikos SA, Fernando B, Pacak K, Assie G, Baudin E, Chompret A, Ellison JW, Briere JJ, Rustin P, Gimenez-Roqueplo AP, Eng C, Camey 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.
32. Baysal BE. A recurrent stop-codon mutation in succinate dehydrogenase subunit B gene in normal peripheral blood and childhood T-cell acute leukemia. PLoS ONE 2007;2:e436.
33. Rodriguez-Cuevas S, Lopez-Garza J, Labastida-Almendaro S. Carotid body tumors in inhabitants of altitudes higher than 2000 meters above sea level. Head Neck 1998;20:374-8.
34. Jech M, Alvarado-Cabrero I, Albores-Saavedra J, Dahia PL, Tischler AS. Genetic analysis of high altitude paraganglionnas. Endocr Pathol 2006;17:201-2.
35. Cohen JE, Small C. Hypsographic demography: the distribution of human population by altitude. Proc Natl Acad Sci U S A 1998; 95:14009-14.
36. Dannenberg H, Dinjens WN, Abbou M, Van Urk H, Pauw BK, Mouwen D, Mooi WJ, de Krijger RR. Frequent germ-line succinate dehydrogenase subunit O gene mutations in patients with apparently sporadic parasympathetic paraganglioma. Clin Cancer Res 2002; 8:2061-6.
37. Baysal BE. Bole of mitochondrial mutations in cancer. Endocr Pathol 2006;17:203-212.
38. Tomlinson IP, Alam NA, Bowan AJ, Barclay E, Jaeger EE, Kelsell D, Leigh I, Gorman P, Lamlum H, Bahman S, Roylance RR, Olpin S, Bevan S, Barker K, Hearle N, Houlston BS, Kiuru M, Lehtonen R, Karhu A, Vilkki S, Laiho P, Eklund C, Vierimaa O, Aittomaki K, Hietala M, Sistonen P, Paetau A, Salovaara R, Herva R, Launonen V, Aaltonen LA. Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer. Nat Genet 2002;30:406-10.
39. Dahia PL, Ross KN, Wright ME, Hayashida CY, Santagata S, Barrontini M, Kung AL, Sanso G, Powers JF, Tischler AS, Hodin R, Heitritter S, Moore F, Dluhy R, Sosa JA, Ocal IT, Benn DE, Marsh DJ, Robinson BG, Schneider K, Garber J, Arum SM, Korbonits M, Grossman A, Pigny P, Toledo SP, Nose V, Li C, Stiles CD. A HIF1alpha regulatory loop links hypoxia and mitochondrial signals in pheochromocytomas. PLoS Genet 2005;1:72-80.
40. Pollard PJ, El Bahrawy M, Poulsom R, Elia G, Killick P, Kelly G, Hunt T, Jeffery R, Seedhar P, Barwell J, Latif F, Gleason MJ, Hodgson SV, Stamp GW, Tomlinson IP, Maher ER. Expression of HIF-1alpha, HIF-2alpha (EPAS1), and their target genes in paraganglionna and pheochromocytorna with VHL and SDH mutations. J Clin Endocrinol Metab 2006;91:4593-8.
41. Schofield CJ, Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 2004;5:343-54.
42. Selak MA, Armour SM, MacKenzie ED, Boulahlbel 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.
43. Isaacs JS, Jung YJ, Mole DR, Lee S, Torres-Cabala C, Chung YL, Merino M, Trepel J, Zbar B, Toro J, Ratcliffe PJ, Linehan WM, Neckers L. HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell 2005;8:143-53.
44. 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, Gleason MJ, Hodgson SV, Poulsom B, 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; 14:2231-9.
45. Vanharanta S, Pollard PJ, Lehtonen HJ, Laiho P, Sjoberg J, Leminen A, Aittomaki K, Arola J, Kruhoffer M, Orntoft TF, Tomlinson IP, Kiuru M, Arango D, Aaltonen LA. Distinct expression profile in fumarate-hydratase-deficient uterine fibroids. Hum Mol Genet 2006;15:97-103.
46. Catherine WH, Mayers CM, Mantzouris T, Armstrong AY, Linehan WM, Segars JH. Compensatory alterations in energy homeostasis characterized in uterine tumors from hereditary leiomyomatosis and renal cell cancer. Fertil Steril 2007;88:1039-48.
47. Smith EH, Janknecht B, Maher LJ, III. Succinate inhibition of α-ketoglutarate-dependent enzymes in a yeast model of paraganglionna. Hum Mol Genet 2007;16:3136-48.
48. Ishii N, Fujii M, Hartman PS, Tsuda M, Yasuda K, Senoo-Matsuda N, Yanase S, Ayusawa D, Suzuki K. A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature 1998;394:694-7.
49. Slane BG, Aykin-Burns N, Smith BJ, Kalen AL, Goswami PC, Domann FE, Spitz DR. Mutation of succinate dehydrogenase subunit C results in increased O2.-, oxidative stress, and genomic instability. Cancer Res 2006;66:7615-20.
50. Piruat JI, Pintado CO, Ortega-Saenz P, Roche M, Lopez-Barneo J. The mitochondrial SDHD gene is required for early embryagenesis, and its partial deficiency results in persistent carotid body glomus cell activation with full responsiveness to hypoxia. Mol Cell Biol 2004;24:10933-40.
51. Szeto SS, Reinke SN, Sykes ED, Lemire BD. Ubiquinone-binding site mutations in the Saccharomyces cerevisiae succinate dehydrogenase generate superoxide and lead to the accumulation of succinate. J Biol Chem 2007;282:27518-26.
52. 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;28:718-31.
53. Lee S, Nakamura E, Yang H, Wei W, Linggi MIS, Sajan MP, Farese RV, Freeman RS, Carter BD, Kaelin WG, Jr., Schlisio S. Neuronal apoptosis linked to EgIN3 prolyl hydroxylase and familial pheochromocytorna genes: developmental culling and cancer. Cancer Cell 2005; 8:155-67.
54. Hansen EF, Jordanova ES, van Minderhout J, Hogendoom PC, Taschner PE, van der Mey AG, Devilee P, Corneisse CJ. Somatic loss of maternal chromosome 11 causes parent-of-origin-dependent inheritance in SDHD-linked paraganglioma and phaeochromocytoma families. Oncogene 2004;23:4076-83.
55. Baysal BE, Lawrence EC, Ferrell RE. Sequence variation in human succinate dehydrogenase genes: evidence for long-term balancing selection on SDHA. BMC Biol 2007;5:12.
56. Briere JJ, Favier J, Benit P, El G, V, Lorenzato A, Rabier D, Di Renzo MF, Gimenez-Roqueplo AP, Rustin P. Mitochondrial succinate is instrumental for HIF1alpha nuclear translocation in SDHA-mutant fibroblasts under normoxic conditions. Hum Mol Genet 2005; 14:3263-9.
57. Yankovskaya V, Horsefield R, Tornnoth S, Luna-Chavez C, Miyoshi H, Leger C, Byrne B, Cecchini G, Iwata S. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 2003;299:7004.
58. Sun F, Huo X, Zhai Y, Wang A, Xu J, Su D, Bartlam M, Hao Z. Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 2005;121:1043-57.
59. Tran QM, Rothery RA, Maklashina E, Cecchini G, Weiner JH. Escherichia coli succinate dehydrogenase variant lacking the heme b. Proc Natt Acad Sci U S A 2007;104:18007-12.
60. Oyedotun KS, Sit CS, Lemire BD. The Saccharomyces cerevisiae succinate dehydrogenase does not require heme for ubiquinone reduction. Biochim Biophys Acta 2007;1767:1436-45.
61. Baysal BE. A phenotypic perspective on Mammalian oxygen sensor candidates. Ann N Y Acad Sci 2006;1073:221-233.