Tumoral EPAS1 (HIF2A) mutations explain sporadic pheochromocytoma and paraganglioma in the absence of erythrocytosis

Human Molecular Genetics

Volumn 22, Issue 11, 2013, Pages 2169-2176

  Comino Méndez, Iñaki ^a   de Cubas, Aguirre A ^a   Bernal, Carmen ^b   Álvarez Escolá, Cristina ^c   Sánchez Malo, Carolina ^d   Ramírez Tortosa, César L ^e   Pedrinaci, Susana ^f   Rapizzi, Elena ^g,h   Ercolino, Tonino ⁱ   Bernini, Giampaolo ^j   Bacca, Alessandra ^j   Letón, Rocío ^a   Pita, Guillermoó ^a   Alonso, María R ^a   Leandro García, Luis J ^a   Gómez Graña, Álvaro ^a   Inglada Pérez, Lucía ^a,k   Mancikova, Veronika ^a   Rodríguez Antona, Cristina ^a,k   Mannelli, Massimo ^g,h   Robledo, Mercedes ^a,k   Cascón, Alberto ^a,k   more..

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

^c HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

^d Endocrinology and Nutrition Unit   (Spain)

^e Pathology Service   (Spain)

^f HOSPITAL UNIVERSITARIO VIRGEN DE LAS NIEVES   (Spain)

^g UNIVERSITY OF FLORENCE   (Italy)

^h ISTITUTO TOSCANO TUMORI   (Italy)

ⁱ CAREGGI UNIVERSITY HOSPITAL   (Italy)

^j UNIVERSITY OF PISA   (Italy)

^k CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GNA14 PROTEIN; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MESSENGER RNA; PCSK6 PROTEIN; SUCCINATE DEHYDROGENASE; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN;

ADOLESCENT; ADULT; AGED; ARTICLE; CANCER PATIENT; CANCER SCREENING; CHROMOSOME 2P; CLINICAL ASSESSMENT; CLINICAL FEATURE; CONTROLLED STUDY; ERYTHROCYTOSIS; FEMALE; GAIN OF FUNCTION MUTATION; GENE DOSAGE; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; GENETIC ANALYSIS; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MOLECULAR GENETICS; MULTIPLEX POLYMERASE CHAIN REACTION; NUCLEOTIDE SEQUENCE; PARAGANGLIOMA; PHEOCHROMOCYTOMA; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR UPREGULATION; SINGLE NUCLEOTIDE POLYMORPHISM;

ADOLESCENT; ADULT; AGED; AMINO ACID SEQUENCE; ANOXIA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CHROMOSOME ABERRATIONS; CHROMOSOMES, HUMAN, PAIR 2; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MIDDLE AGED; MUTATION; PARAGANGLIOMA, EXTRA-ADRENAL; PHEOCHROMOCYTOMA; POLYCYTHEMIA; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN INTERACTION DOMAINS AND MOTIFS; YOUNG ADULT;

EID: 84877906693     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt069     Document Type: Article

References (39)

1. Latif, F., Tory, K., Gnarra, J., Yao, M., Duh, F.M., Orcutt, M.L., Stackhouse, T., Kuzmin, I., Modi, W., Geil, L. et al. (1993) Identification of the von Hippel-Lindau disease tumor suppressor gene. Science, 260, 1317-1320.
2. Mulligan, L.M., Kwok, J.B., Healey, C.S., Elsdon, M.J., Eng, C., Gardner, E., Love, D.R., Mole, S.E., Moore, J.K., Papi, L. et al. (1993) Germ-line mutations of the RET proto-oncogene in multiple endocrine neoplasia type 2A. Nature, 363, 458-460.
3. Wallace, M.R., Andersen, L.B., Saulino, A.M., Gregory, P.E., Glover, T.W. and Collins, F.S. (1991) A de novo Alu insertion results in neurofibromatosis type 1. Nature, 353, 864-866.
4. Hao, H.X., Khalimonchuk, O., Schraders, M., Dephoure, N., Bayley, J.P., Kunst, H., Devilee, P., Cremers, C.W., Schiffman, J.D., Bentz, B.G. et al. (2009) SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science, 325, 1139-1142.
5. Burnichon, N., Briere, J.J., Libe, R., Vescovo, L., Riviere, J., Tissier, F., Jouanno, E., Jeunemaitre, X., Benit, P., Tzagoloff, A. et al. (2010) SDHA is a tumor suppressor gene causing paraganglioma. Hum. Mol. Genet., 19, 3011-3020.
6. Comino-Mendez, I., Gracia-Aznarez, F.J., Schiavi, F., Landa, I., Leandro-Garcia, L.J., Leton, R., Honrado, E., Ramos-Medina, R., Caronia, D., Pita, G. et al. (2011) Exome sequencing identifies MAX mutations as a cause of hereditary pheochromocytoma. Nat. Genet., 43, 663-667.
7. Qin, Y., Yao, L., King, E.E., Buddavarapu, K., Lenci, R.E., Chocron, E.S., Lechleiter, J.D., Sass, M., Aronin, N., Schiavi, F. et al. (2010) Germline mutations in TMEM127 confer susceptibility to pheochromocytoma. Nat. Genet., 42, 229-233.
8. Baysal, B.E., Ferrell, R.E., Willett-Brozick, J.E., Lawrence, E.C., Myssiorek, D., Bosch, A., van der Mey, A., Taschner, P.E., Rubinstein, W.S., Myers, E.N. et al. (2000) Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science, 287, 848-851.
9. Astuti, D., Latif, F., Dallol, A., Dahia, P.L., Douglas, F., George, E., Skoldberg, F., Husebye, E.S., Eng, C. and Maher, E.R. (2001) Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am. J. Hum. Genet., 69, 49-54.
10. Niemann, S. and Muller, U. (2000) Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat. Genet., 26, 268-270.
11. Burnichon, N., Buffet, A., Parfait, B., Letouze, E., Laurendeau, I., Loriot, C., Pasmant, E., Abermil, N., Valeyrie-Allanore, L., Bertherat, J. et al. (2012) Somatic NF1 inactivation is a frequent event in sporadic pheochromocytoma. Hum. Mol. Genet, 21, 5397-5405
12. Zhuang, Z., Yang, C., Lorenzo, F., Merino, M., Fojo, T., Kebebew, E., Popovic, V., Stratakis, C.A., Prchal, J.T. and Pacak, K. (2012) Somatic HIF2A gain-of-function mutations in paraganglioma with polycythemia. N. Engl. J. Med., 367, 922-930.
13. Tian, H., McKnight, S.L. and Russell, D.W. (1997) Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev., 11, 72-82.
14. Percy, M.J., Furlow, P.W., Lucas, G.S., Li, X., Lappin, T.R., McMullin, M.F. and Lee, F.S. (2008) A gain-of-function mutation in the HIF2A gene in familial erythrocytosis. N. Engl. J. Med., 358, 162-168.
15. Percy, M.J., Chung, Y.J., Harrison, C., Mercieca, J., Hoffbrand, A.V., Dinardo, C.L., Santos, P.C., Fonseca, G.H., Gualandro, S.F., Pereira, A.C. et al. (2012) Two new mutations in the HIF2A gene associated with erythrocytosis. Am. J. Hematol., 87, 439-442.
16. Percy, M.J., Beer, P.A., Campbell, G., Dekker, A.W., Green, A.R., Oscier, D., Rainey, M.G., van Wijk, R., Wood, M., Lappin, T.R. et al. (2008) Novel exon 12 mutations in the HIF2A gene associated with erythrocytosis. Blood, 111, 5400-5402.
17. Lee, F.S. and Percy, M.J. (2011) The HIF pathway and erythrocytosis. Annu. Rev. Pathol., 6, 165-192.
18. Dahia, P.L., Ross, K.N., Wright, M.E., Hayashida, C.Y., Santagata, S., Barontini, M., Kung, A.L., Sanso, G., Powers, J.F., Tischler, A.S. et al. (2005) A HIF1alpha regulatory loop links hypoxia and mitochondrial signals in pheochromocytomas. PLoS Genet., 1, 72-80.
19. Maxwell, P.H. (2005) A common pathway for genetic events leading to pheochromocytoma. Cancer Cell, 8, 91-93.
20. Holmquist-Mengelbier, L., Fredlund, E., Lofstedt, T., Noguera, R., Navarro, S., Nilsson, H., Pietras, A., Vallon-Christersson, J., Borg, A., Gradin, K. et al. (2006) Recruitment of HIF-1alpha and HIF-2alpha to common target genes is differentially regulated in neuroblastoma: HIF-2alpha promotes an aggressive phenotype. Cancer Cell, 10, 413-423.
21. Lopez-Jimenez, E., Gomez-Lopez, G., Leandro-Garcia, L.J., Munoz, I., Schiavi, F., Montero-Conde, C., de Cubas, A.A., Ramires, R., Landa, I., Leskela, S. et al. (2010) Research resource: transcriptional profiling reveals different pseudohypoxic signatures in SDHB and VHL-related pheochromocytomas. Mol. Endocrinol., 24, 2382-2391.
22. Martin-Rendon, E., Hale, S.J., Ryan, D., Baban, D., Forde, S.P., Roubelakis, M., Sweeney, D., Moukayed, M., Harris, A.L., Davies, K. et al. (2007) Transcriptional profiling of human cord blood CD133+ and cultured bone marrow mesenchymal stem cells in response to hypoxia. Stem Cells, 25, 1003-1012.
23. Egger, M., Schgoer, W., Beer, A.G., Jeschke, J., Leierer, J., Theurl, M., Frauscher, S., Tepper, O.M., Niederwanger, A., Ritsch, A. et al. (2007) Hypoxia up-regulates the angiogenic cytokine secretoneurin via an HIF-1alpha- and basic FGF-dependent pathway in muscle cells. FASEB J., 21, 2906-2917.
24. Chen, H.H., Schock, S.C., Xu, J., Safarpour, F., Thompson, C.S. and Stewart, A.F. (2007) Extracellular ATP-dependent upregulation of the transcription cofactor LMO4 promotes neuron survival from hypoxia. Exp. Cell. Res., 313, 3106-3116.
25. Welander, J., Larsson, C., Backdahl, M., Hareni, N., Sivler, T., Brauckhoff, M., Soderkvist, P. and Gimm, O. (2012) Integrative genomics reveals frequent somatic NF1 mutations in sporadic pheochromocytomas. Hum. Mol. Genet, 21, 5406-5416
26. van Wijk, R., Sutherland, S., Van Wesel, A.C., Huizinga, E.G., Percy, M.J., Bierings, M. and Lee, F.S. (2010) Erythrocytosis associated with a novel missense mutation in the HIF2A gene. Haematologica, 95, 829-832.
27. van Nederveen, F.H., Gaal, J., Favier, J., Korpershoek, E., Oldenburg, R.A., de Bruyn, E.M., Sleddens, H.F., Derkx, P., Riviere, J., Dannenberg, H. 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., 10, 764-771.
28. Huang, S.C., Koch, C.A., Vortmeyer, A.O., Pack, S.D., Lichtenauer, U.D., Mannan, P., Lubensky, I.A., Chrousos, G.P., Gagel, R.F., Pacak, K. et al. (2000) Duplication of the mutant RET allele in trisomy 10 or loss of the wild-type allele in multiple endocrine neoplasia type 2-associated pheochromocytomas. Cancer Res., 60, 6223-6226.
29. Lo, R.K. and Wong, Y.H. (2004) Signal transducer and activator of transcription 3 activation by the delta-opioid receptor via Galpha14 involves multiple intermediates. Mol. Pharmacol., 65, 1427-1439.
30. Bassi, D.E., Lopez De Cicco, R., Cenna, J., Litwin, S., Cukierman, E. and Klein-Szanto, A.J. (2005) PACE4 expression in mouse basal keratinocytes results in basement membrane disruption and acceleration of tumor progression. Cancer Res., 65, 7310-7319.
31. Delic, S., Lottmann, N., Jetschke, K., Reifenberger, G. and Riemenschneider, M.J. (2012) Identification and functional validation of CDH11, PCSK6 and SH3GL3 as novel glioma invasion-associated candidate genes. Neuropathol. Appl. Neurobiol., 38, 201-212.
32. Favier, J., Kempf, H., Corvol, P. and Gasc, J.M. (1999) Cloning and expression pattern of EPAS1 in the chicken embryo. Colocalization with tyrosine hydroxylase. FEBS Lett., 462, 19-24.
33. Maranchie, J.K., Vasselli, J.R., Riss, J., Bonifacino, J.S., Linehan, W.M. and Klausner, R.D. (2002) The contribution of VHL substrate binding and HIF1-alpha to the phenotype of VHL loss in renal cell carcinoma. Cancer Cell, 1, 247-255.
34. Purdue, M.P., Johansson, M., Zelenika, D., Toro, J.R., Scelo, G., Moore, L.E., Prokhortchouk, E., Wu, X., Kiemeney, L.A., Gaborieau, V. et al. (2011) Genome-wide association study of renal cell carcinoma identifies two susceptibility loci on 2p21 and 11q13.3. Nat. Genet., 43, 60-65.
35. Sambrook, J., Maniatis, T. and Fritsch, E.F. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
36. Simon-Sanchez, J., Scholz, S., Fung, H.C., Matarin, M., Hernandez, D., Gibbs, J.R., Britton, A., de Vrieze, F.W., Peckham, E., Gwinn-Hardy, K. et al. (2007) Genome-wide SNP assay reveals structural genomic variation, extended homozygosity and cell-line induced alterations in normal individuals. Hum. Mol. Genet., 16, 1-14.
37. Cascon, A., Montero-Conde, C., Ruiz-Llorente, S., Mercadillo, F., Leton, R., Rodriguez-Antona, C., Martinez-Delgado, B., Delgado, M., Diez, A., Rovira, A. et al. (2006) Gross SDHB deletions in patients with paraganglioma detected by multiplex PCR: a possible hot spot? Genes Chromosomes Cancer, 45, 213-219.
38. Morrissey, E.R. and Diaz-Uriarte, R. (2009) Pomelo II: finding differentially expressed genes. Nucleic Acids Res, 37, W581-W586.
39. Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N. and Golani, I. (2001) Controlling the false discovery rate in behavior genetics research. Behav. Brain Res., 125, 279-284.