Genetics of pheochromocytomas and paragangliomas

Best Practice and Research: Clinical Endocrinology and Metabolism

Volumn 24, Issue 6, 2010, Pages 943-956

  Opocher, Giuseppe ^a,b   Schiavi, Francesca ^a  

^a VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

Adrenal; Apoptosis; Genetics; Paraganglioma; Pheochromocytoma

Indexed keywords

CATECHOLAMINE; KIF1B BETA PROTEIN; NEUROFIBROMIN; PHENYLETHANOLAMINE N METHYLTRANSFERASE; PROLYL HYDROXYLASE 2; PROTEIN; PROTEIN RET; SDHAF2 PROTEIN; SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE B; SUCCINATE DEHYDROGENASE C; SUCCINATE DEHYDROGENASE D; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

CANCER RISK; FAMILIAL CANCER; GENE MUTATION; GENETIC ASSOCIATION; GENETIC PREDISPOSITION; GENETICS; HEMANGIOBLASTOMA; HUMAN; KIDNEY CARCINOMA; NEURAL CREST CELL; NEUROFIBROMATOSIS; PARAGANGLIOMA; PHEOCHROMOCYTOMA; PRIMARY HYPERPARATHYROIDISM; REVIEW; THYROID MEDULLARY CARCINOMA; VON HIPPEL LINDAU DISEASE;

ADRENAL GLAND NEOPLASMS; HUMANS; PARAGANGLIOMA; PHEOCHROMOCYTOMA;

EID: 78649663716     PISSN: 1521690X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.beem.2010.05.001     Document Type: Review

References (59)

1. B.E. Baysal Hereditary paraganglioma targets diverse paraganglia Journal of Medical Genetics 39 9 2002 617 622
2. F.G. Zak, and W. Lawson Anatomy and topography The paraganglionic chemoreceptor system 1982 Springer-Verlag 15 49
3. E.E. Lack Anatomy and physiology of peripheral arterial chemoreceptors E.E. Lack, Pathology of adrenal and extra-adrenal paraganglia 1994 W.B. Saunders 1 14
4. O. Gimm, C.A. Koch, A. Januszewicz, G. Opocher, and H.P. Neumann The genetic basis of pheochromocytoma Frontiers of Hormone Research 31 2004 45 60
5. C.S. Gujrathi, and P.J. Donald Current trends in the diagnosis and management of head and neck paragangliomas Current Opinion in Otolaryngology & Head and Neck Surgery 13 6 2005 339 342
6. S. Grufferman, M.W. Gillman, L.R. Pasternak, C.L. Peterson, and W.G. Young Jr. Familial carotid body tumors: case report and epidemiologic review Cancer 46 9 1980 2116 2122
7. C.M. Drovdlic, E.N. Myers, J.A. Peters, B.E. Baysal, D.E. Brackmann, W.H. Slattery 3rd, and W.S. Rubinstein Proportion of heritable paraganglioma cases and associated clinical characteristics Laryngoscope 111 10 2001 1822 1827
8. A.G. van der Mey, P.D. Maaswinkel-Mooy, C.J. Cornelisse, P.H. Schmidt, and J.J. van de Kamp Genomic imprinting in hereditary glomus tumours: evidence for new genetic theory Lancet 2 8675 1989 1291 1294
9. J. Arias-Stella, and J. Valcarcel Chief cell hyperplasia in the human carotid body at high altitudes; physiologic and pathologic significance Human Pathology 7 4 1976 361 373
10. K. Arstrom, J.E. Cohen, C. Willet-Brozick, E. Aston, and B. Baysal Altitude is a phenotypic modifier in hereditary paraganglioma type 1: evidence for an oxygen-sensing defect Human Genetics 113 2003 228 237
11. B.E. Baysal, J.E. Willett-Brozick, P.A. Filho, E.C. Lawrence, E.N. Myers, and R.E. Ferrell An Alu-mediated partial SDHC deletion causes familial and sporadic paraganglioma Journal of Medical Genetics 41 9 2004 703 709
12. E.E. Lack Hyperplasia of vagal and carotid body paraganglia in patients with chronic hypoxemia American Journal of Pathology 91 3 1978 497 516
13. E.L. Bravo, and R.W. Gifford Jr. Current concepts. Pheochromocytoma: diagnosis, localization and management The New England Journal of Medicine 311 20 1984 1298 1303
14. B.E. Baysal, R.E. Ferrell, J.E. Willett-Brozick, E.C. Lawrence, D. Myssiorek, A. Bosch, A. van der Mey, P.E. Taschner, W.S. Rubinstein, E.N. Myers, C.W. Richard 3rd, C.J. Cornelisse, P. Devilee, and B. Devlin Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma Science 287 5454 2000 848 851
15. D. Astuti, F. Douglas, T.W.J. Lennard, I. Agaliaganis, E.R. Woodward, D.G.R. Evans, C. Eng, F. Latif, and E.R. Maher Germline SDHD mutation in familial phaeochromocytoma Lancet 357 2001 1181 1182
16. D. Astuti, F. Latif, A. Dallol, P.L.M. Dahia, F. Douglas, E. George, F. Sköldberg, E.S. Husebye, C. Eng, and E.R. Maher Mutations in the mitochondrial complex II subunit SDHB cause susceptibility to familial paraganglioma and pheochromocytoma American Journal of Human Genetics 69 2001 49 54
17. S. Niemann, and U. Muller Mutations in SDHC cause autosomal dominant paraganglioma, type 3 Nature Genetics 26 3 2000 268 270
18. H.P.H. Neumann, B. Bausch, S.R. Mcwhinney, B.U. Bender, O. Gimm, G. Franke, J. Schipper, J. Klisch, C. Altehoefer, K. Zerres, A. Januszewicz, and C. Eng Germ-line mutations in non syndromic pheochromocytoma The New England Journal of Medicine 346 2002 1459 1466
19. H.X. Hao, O. Khalimonchuk, M. Schraders, N. Dephoure, J.P. Bayley, H. Kunst, P. Devilee, C.W. Cremers, J.D. Schiffman, B.G. Bentz, S.P. Gygi, D.R. Winge, H. Kremer, and J. Rutter SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma Science 325 5944 2009 1139 1142
20. H.P.H. Neumann, C. Pawlu, M. Peczkowska, B. Bausch, S.R. McWhinney, M. Muresan, M. Buchta, G. Franke, J. Klisch, T.A. Bley, S. Hoegerle, C.C. Boedeker, G. Opocher, J. Schipper, A. Januszewicz, and C. Eng Distinct clinical features of paraganglioma syndromes associated with SDHB and SDHD gene mutations The Journal Of the American Medical Association 292 2004 943 951
21. D.E. Benn, A.P. Gimenez-Roqueplo, J.R. Reilly, J. Bertherat, J. Burgess, K. Byth, M. Croxson, P.L. Dahia, M. Elston, O. Gimm, D. Henley, P. Herman, V. Murday, P. Niccoli-Sire, J.L. Pasieka, V. Rohmer, K. Tucker, X. Jeunemaitre, D.J. Marsh, P.F. Plouin, and B.G. Robinson Clinical presentation and penetrance of pheochromocytoma/paraganglioma syndromes The Journal of Clinical Endocrinology & Metabolism 91 3 2006 827 836
22. F. Schiavi, C.C. Boedeker, B. Bausch, M. Pezkowska, C.F. Gomez, T. Strassburg, C. Pawlu, M. Buchta, M. Salzmann, M.M. Hoffmann, A. Berlis, I. Brink, M. Cybulla, M. Muresan, M.A. Walter, F. Forrer, M. Välimäki, A. Kawecki, Z. Szutkowski, J. Schipper, M.K. Walz, P. Pigny, C. Bauters, J.E. Willet-Brozick, B.E. Baysal, A. Januszewicz, C. Eng, G. Opocher, H.P. Neumann, and European-American Paraganglioma Study Group Predictors and prevalence of paraganglioma syndrome associated with mutations of the SDHC gene The Journal Of the American Medical Association 294 16 2005 2057 2063
23. L. Amar, J. Bertherat, E. Baudin, C. Ajzenberg, B. Bressac-de Paillerets, O. Chabre, B. Chamontin, B. Delemer, S. Giraud, A. Murat, P. Niccoli-Sire, S. Richard, V. Rohmer, J.L. Sadoul, L. Strompf, M. Schlumberger, X. Bertagna, P.F. Plouin, X. Jeunemaitre, and A.P. Gimenez-Roqueplo Genetic testing in pheochromocytoma or functional paraganglioma Journal of Clinical Oncology 23 2008 8812 8818
24. F. Fränkel Ein Fall von doppelseitigem, völlig latent verlaufenen Nebennierentumor und gleichzeitiger Nephritis mit Veränderungen am Circulationsapparat und Retinitis Virchows Archiv für pathologische Anatomie und Physiologie und für klinische Medizin 103 1886 244 263
25. H.P. Neumann, A. Vortmeyer, D. Schmidt, M. Werner, Z. Erlic, A. Cascon, B. Bausch, A. Januszewicz, and C. Eng Evidence of MEN-2 in the original description of classic pheochromocytoma The New England Journal of Medicine 357 13 2007 1311 1315
26. W.G. Kaelin Jr. Molecular basis of the VHL hereditary cancer syndrome Nature Reviews Cancer 2 9 2002 673 682
27. P.A. Crossey, K. Foster, F.M. Richards, M.E. Phipps, F. Latif, K. Tory, M.H. Jones, E. Bentley, R. Kumar, and M.I. Lerman Molecular genetic investigations of the mechanism of tumourigenesis in von Hippel-Lindau disease: analysis of allele loss in VHL tumours Human Genetics 93 1 1994 53 58
28. A.G. Knudson Jr. Mutation and cancer: statistical study of retinoblastoma Proceedings of the National Academy of Sciences USA 68 4 1971 820 823
29. B.U. Bender, M. Gutsche, S. Glasker, B. Muller, G. Kirste, C. Eng, and H.P. Neumann Differential genetic alterations in von Hippel-Lindau syndrome-associated and sporadic pheochromocytomas The Journal of Clinical Endocrinology & Metabolism 85 12 2000 4568 4574
30. W.O. Lui, J. Chen, S. Glasker, B.U. Bender, C. Madura, S.K. Khoo, E. Kort, C. Larsson, H.P. Neumann, and B.T. Teh Selective loss of chromosome 11 in pheochromocytomas associated with the VHL syndrome Oncogene 21 7 2002 1117 1122
31. F. Chen, T. Kishida, M. Yao, T. Hustad, D. Glavac, M. Dean, J.R. Gnarra, M.L. Orcutt, F.M. Duh, G. Glenn, J. Green, Y.E. Hsia, J. Lamiell, H. Li, M.H. Wei, L. Schmidt, K. Tory, I. Kuzman, T. Stackhouse, F. Latif, W.M. Linehan, M. Lerman, and B. Zbar Germline mutations in the von Hippel-Lindau disease tumor suppressor gene: correlations with phenotype Human Mutation 5 1995 66 75
32. F.J. Hes, J.W. Hoppener, and C.J. Lips Clinical review 155: pheochromocytoma in Von Hippel-Lindau disease The Journal of Clinical Endocrinology & Metabolism 88 3 2003 969 974
33. M.M. Walther, J. Herring, E. Enquist, H.R. Keiser, and W.M. Linehan von Recklinghausen's disease and pheochromocytomas The Journal of Urology 162 5 1999 1582 1586
34. B. Bausch, W. Borozdin, V.F. Mautner, M.M. Hoffmann, D. Boehm, M. Robledo, A. Cascon, T. Harenberg, F. Schiavi, C. Pawlu, M. Peczkowska, C. Letizia, S. Calvieri, G. Arnaldi, R.D. Klingenberg-Noftz, N. Reisch, A. Fassina, L. Brunaud, M.A. Walter, M. Mannelli, G. MacGregor, F.F. Palazzo, M. Barontini, M.K. Walz, B. Kremens, G. Brabant, R. Pfäffle, A.C. Koschker, F. Lohoefner, M. Mohaupt, O. Gimm, B. Jarzab, S.R. McWhinney, G. Opocher, A. Januszewicz, J. Kohlhase, C. Eng, H.P. Neumann, and European-American Phaeochromocytoma Registry Study Group Germline NF1 mutational spectra and loss-of-heterozygosity analyses in patients with pheochromocytoma and neurofibromatosis type 1 The Journal of Clinical Endocrinology & Metabolism 92 7 2007 2784 2792
35. A. Machens, and H. Dralle Genotype-phenotype based surgical concept of hereditary medullary thyroid carcinoma World Journal of Surgery 31 5 2007 957 968
36. A. Machens, M. Brauckhoff, H.J. Holzhausen, P.N. Thanh, H. Lehnert, and H. Dralle Codon-specific development of pheochromocytoma in multiple endocrine neoplasia type 2 The Journal of Clinical Endocrinology & Metabolism 90 7 2005 3999 4003
37. N. Burnichon, V. Rohmer, L. Amar, P. Herman, S. Leboulleux, V. Darrouzet, P. Niccoli, D. Gaillard, G. Chabrier, F. Chabolle, I. Coupier, P. Thieblot, P. Lecomte, J. Bertherat, N. Wion-Barbot, A. Murat, A. Venisse, P.F. Plouin, X. Jeunemaitre, A.P. Gimenez-Roqueplo, and PGL.NET network The succinate dehydrogenase genetic testing in a large prospective series of patients with paragangliomas The Journal of Clinical Endocrinology & Metabolism 94 8 2009 2817 2827
38. E.F. Hensen, E.S. Jordanova, I.J.H.M. van Minderhout, P.C.W. Hogendoorn, P.E.M. Taschner, A.G.L. van der Mey, P. Devilee, and C.J. Cornelisse Somatic loss of maternal chromosome 11 causes parent-of-origin-dependent inheritance in SDHD-linked paraganglioma and phaeochromocytoma families Oncogene 23 2004 4076 4083
39. H. Hirawake, M. Taniwaki, A. Tamura, S. Kojima, and K. Kita Cytochrome b in human complex II (succinate-ubiquinone oxidoreductase): cDNA cloning of the components in liver mitochondria and chromosome assignment of the genes for the large (SDHC) and small (SDHD) subunits to 1q21 and 11q23 Cytogenetics and Cell Genetics 79 1-2 1997 132 138
40. O. Gimm, M. Armanios, H. Dziema, H.P. Neumann, and C. Eng Somatic and occult germ-line mutations in SDHD, a mitochondrial complex II gene, in nonfamilial pheochromocytoma Cancer Research 60 24 2000 6822 6825
41. A.P. Gimenez-Roqueplo, J. Favier, P. Rustin, J.J. Mourad, P.F. Plouin, P. Corvol, A. Rotig, and X. Jeunemaitre 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 American Journal of Human Genetics 69 6 2001 1186 1197
42. S. Niemann, D. Steinberger, and U. Muller PGL3, a third, not maternally imprinted locus in autosomal dominant paraganglioma Neurogenetics 2 1999 167 170
43. A. Elbehti-Green, H.C. Au, J.T. Mascarello, D. Ream-Robinson, and I.E. Scheffler Characterization of the human SDHC gene encoding of the integral membrane proteins of succinate-quinone oxidoreductase in mitochondria Gene 213 1-2 1998 133 140
44. H.C. Au, D. Ream-Robinson, L.A. Bellew, P.L. Broomfield, M. Saghbini, and I.E. Scheffler Structural organization of the gene encoding the human iron-sulfur subunit of succinate dehydrogenase Gene 159 2 1995 249 253
45. S. Schlisio, R.S. Kenchappa, L.C. Vredeveld, R.E. George, R. Stewart, H. Greulich, K. Shahriari, N.V. Nguyen, P. Pigny, P.L. Dahia, S.L. Pomeroy, J.M. Maris, A.T. Look, M. Meyerson, D.S. Peeper, B.D. Carter, and W.G. Kaelin Jr. The kinesin KIF1Bbeta acts downstream from EglN3 to induce apoptosis and is a potential 1p36 tumor suppressor Genes & Development 22 7 2008 884 893
46. I.T. Yeh, R.E. Lenci, Y. Qin, K. Buddavarapu, A.H. Ligon, E. Leteurtre, C. Do Cao, C. Cardot-Bauters, P. Pigny, and P.L. Dahia A germline mutation of the KIF1B beta gene on 1p36 in a family with neural and nonneural tumors Human Genetics 124 3 2008 279 285
47. C. Ladroue, R. Carcenac, M. Leporrier, S. Gad, C. Le Hello, F. Galateau-Salle, J. Feunteun, J. Pouysségur, S. Richard, and B. Gardie PHD2 mutation and congenital erythrocytosis with paraganglioma The New England Journal of Medicine 359 25 2008 2685 2692
48. S. Lee, E. Nakamura, H. Yang, W. Wei, M.S. Linggi, M.P. Sajan, R.V. Farese, R.S. Freeman, B.D. Carter, W.G. Kaelin Jr., and S. Schlisio Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer Cancer Cell 8 2 2005 155 167
49. K.S. Vogel, C.I. Brannan, N.A. Jenkins, N.G. Copeland, and L.F. Parada Loss of neurofibromin results in neurotrophin-independent survival of embryonic sensory and sympathetic neurons Cell 82 5 1995 733 742
50. P.L. Dahia, and Familial Pheochromocytoma Consortium Transcription association of VHL and SDH mutations link hypoxia and oxidoreductase signals in pheochromocytomas Annals of the New York Academy of Sciences 1073 2006 208 220
51. G. Eisenhofer, T.T. Huynh, K. Pacak, F.M. Brouwers, M.M. Walther, W.M. Linehan, P.J. Munson, M. Mannelli, D.S. Goldstein, and A.G. Elkahloun Distinct gene expression profiles in norepinephrine- and epinephrine-producing hereditary and sporadic pheochromocytomas: activation of hypoxia-driven angiogenic pathways in von Hippel-Lindau syndrome Endocrine-Related Cancer 11 4 2004 897 911
52. G. Eisenhofer, M.M. Walther, T.T. Huynh, S.T. Li, S.R. Bornstein, A. Vortmeyer, M. Mannelli, D.S. Goldstein, W.M. Linehan, J.W. Lenders, and K. Pacak Pheochromocytomas in von Hippel-Lindau syndrome and multiple endocrine neoplasia type 2 display distinct biochemical and clinical phenotypes The Journal of Clinical Endocrinology & Metabolism 86 5 2001 1999 2008
53. H.J. Timmers, A.P. Gimenez-Roqueplo, M. Mannelli, and K. Pacak Clinical aspects of SDHx-related pheochromocytoma and paraganglioma Endocrine-Related Cancer 16 2 2009 391 400
54. A. Cascón, E. López-Jiménez, I. Landa, S. Leskelä, L.J. Leandro-García, A. Maliszewska, R. Letón, L. de la Vega, M.J. García-Barcina, C. Sanabria, C. Alvarez-Escolá, C. Rodríguez-Antona, and M. Robledo Rationalization of genetic testing in patients with apparently sporadic pheochromocytoma/paraganglioma Hormone and Metabolic Research 41 9 2009 672 675
55. M. Mannelli, M. Castellano, F. Schiavi, S. Filetti, M. Giacch, L. Mori, V. Pignataro, G. Bernini, V. Giach, A. Bacca, B. Biondi, G. Corona, G. Di Trapani, E. Grossrubatscher, G. Reimondo, G. Arnaldi, G. Giacchetti, F. Veglio, P. Loli, A. Colao, M.R. Ambrosio, M. Terzolo, C. Letizia, T. Ercolino, G. Opocher, and the Italian Pheochromocytoma/Paraganglioma Network Clinically guided genetic screening in a large cohort of Italian patients with pheochromocytomas and/or functional or non-functional paragangliomas The Journal of Clinical Endocrinology & Metabolism 94 5 2009 1541 1547
56. H.P. Neumann, Z. Erlic, C.C. Boedeker, L.A. Rybicki, M. Robledo, M. Hermsen, F. Schiavi, M. Falcioni, P. Kwok, C. Bauters, K. Lampe, M. Fischer, E. Edelman, D.E. Benn, B.G. Robinson, S. Wiegand, G. Rasp, B.A. Stuck, M.M. Hoffmann, M. Sullivan, M.A. Sevilla, M.M. Weiss, M. Peczkowska, A. Kubaszek, P. Pigny, R.L. Ward, D. Learoyd, M. Croxson, D. Zabolotny, S. Yaremchuk, W. Draf, M. Muresan, R.R. Lorenz, S. Knipping, M. Strohm, G. Dyckhoff, C. Matthias, N. Reisch, S.F. Preuss, D. Esser, M.A. Walter, H. Kaftan, T. Stöver, C. Fottner, H. Gorgulla, M. Malekpour, M.M. Zarandy, J. Schipper, C. Brase, A. Glien, M. Kühnemund, S. Koscielny, P. Schwerdtfeger, M. Välimäki, W. Szyfter, U. Finckh, K. Zerres, A. Cascon, G. Opocher, G.J. Ridder, A. Januszewicz, C. Suarez, and C. Eng Clinical predictors for germline mutations in head and neck paraganglioma patients: cost reduction strategy in genetic diagnostic process as fall-out Cancer Research 69 8 2009 3650 3656
57. Z. Erlic, L. Rybicki, M. Peczkowska, H. Golcher, P.H. Kann, M. Brauckhoff, K. Müssig, M. Muresan, A. Schäffler, N. Reisch, M. Schott, M. Fassnacht, G. Opocher, S. Klose, C. Fottner, F. Forrer, U. Plöckinger, S. Petersenn, D. Zabolotny, O. Kollukch, S. Yaremchuk, A. Januszewicz, M.K. Walz, C. Eng, H.P. Neumann, and European-American Pheochromocytoma Study Group Clinical predictors and algorithm for the genetic diagnosis of pheochromocytoma patients Clinical Cancer Research 15 20 2009 6378 6385
58. F.H. van Nederveen, J. Gaal, J. Favier, E. Korpershoek, R.A. Oldenburg, E.M. de Bruyn, H.F. Sleddens, P. Derkx, J. Rivire, H. Dannenberg, B.J. Petri, P. Komminoth, K. Pacak, W.C. Hop, P.J. Pollard, M. Mannelli, J.P. Bayley, A. Perren, S. Niemann, A.A. Verhofstad, A.P. de Bruïne, E.R. Maher, F. Tissier, T. Méatchi, C. Badoual, J. Bertherat, L. Amar, D. Alataki, E. Van Marck, F. Ferrau, J. Franois, W.W. de Herder, M.P. Peeters, A. van Linge, J.W. Lenders, A.P. Gimenez-Roqueplo, R.R. de Krijger, and W.N. Dinjens An immunohistochemical procedure to detect patients with paraganglioma and phaeochromocytoma with germline SDHB, SDHC, or SDHD gene mutations: a retrospective and prospective analysis The Lancet Oncology 10 8 2009 764 771
59. Y. Qin, L. Yao, E.E. King, K. Buddavarapu, R.E. Lenci, E.S. Chocron, J.D. Lechleiter, M. Sass, N. Aronin, F. Schiavi, F. Boaretto, G. Opocher, R.A. Toledo, S.P. Toledo, C. Stiles, R.C. Aguiar, and P.L. Dahia Germline mutations in TMEM127 confer susceptibility to pheochromocytoma Nature Genetics 42 3 2010 229 233