Novel candidate genes for 46,XY gonadal dysgenesis identified by a customized 1M array-CGH platform

European Journal of Medical Genetics

Volumn 56, Issue 12, 2013, Pages 661-668

  Norling, Ameli ^a   Lindén Hirschberg, Angelica ^a   Iwarsson, Erik ^a   Persson, Bengt ^b,c   Wedell, Anna ^a   Barbaro, Michela ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Array CGH; C2ORF80; Disorders of sex development; Gonadal dysgenesis; PIP5K1B; SUPT3H

Indexed keywords

ARTICLE; CLINICAL ARTICLE; COMPARATIVE GENOMIC HYBRIDIZATION; COPY NUMBER VARIATION; GENE DELETION; GENE DUPLICATION; GENE IDENTIFICATION; GENE LOCATION; GENE LOCUS; GENOME ANALYSIS; GONADAL DYSGENESIS; HAPLOINSUFFICIENCY; HUMAN; MALE; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SEX DIFFERENTIATION DISORDER; TESTIS;

MUS;

ARRAY-CGH; C2ORF80; DISORDERS OF SEX DEVELOPMENT; GONADAL DYSGENESIS; PIP5K1B; SUPT3H;

COMPARATIVE GENOMIC HYBRIDIZATION; FEMALE; GENE DELETION; GENE DUPLICATION; GONADAL DYSGENESIS, 46,XY; HUMANS; MALE; TRANSCRIPTION FACTORS;

EID: 84888071813     PISSN: 17697212     EISSN: 18780849     Source Type: Journal    
DOI: 10.1016/j.ejmg.2013.09.003     Document Type: Article

References (53)

1. Cederroth C.R., Pitetti J.L., Papaioannou M.D., Nef S. Genetic programs that regulate testicular and ovarian development. Mol. Cell Endocrinol. 2007, 265-266:3-9.
2. Maatouk D.M., DiNapoli L., Alvers A., Parker K.L., Taketo M.M., Capel B. Stabilization of beta-catenin in XY gonads causes male-to-female sex-reversal. Hum. Mol. Genet. 2008, 17:2949-2955.
3. Kent J., Wheatley S.C., Andrews J.E., Sinclair A.H., Koopman P. Amale-specific role for SOX9 in vertebrate sex determination. Development 1996, 122:2813-2822.
4. Morais da Silva S., Hacker A., Harley V., Goodfellow P., Swain A., Lovell-Badge R. Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat. Genet. 1996, 14:62-68.
5. Soder O. Sexual dimorphism of gonadal development. Best Pract. Res. Clin. Endocrinol. Metab. 2007, 21:381-391.
6. Hiort O. The differential role of androgens in early human sex development. BMC Med. 2013, 11:152.
7. MacLaughlin D.T., Donahoe P.K. Sex determination and differentiation. N.Engl. J. Med. 2004, 350:367-378.
8. Looijenga L.H., Hersmus R., Oosterhuis J.W., Cools M., Drop S.L., Wolffenbuttel K.P. Tumor risk in disorders of sex development (DSD). Best Pract. Res. Clin. Endocrinol. Metab. 2007, 21:480-495.
9. Cools M., Wolffenbuttel K.P., Drop S.L., Oosterhuis J.W., Looijenga L.H. Gonadal development and tumor formation at the crossroads of male and female sex determination. Sex Dev. 2011, 5:167-180.
10. Kersemaekers A.M., Honecker F., Stoop H., Cools M., Molier M., Wolffenbuttel K., Bokemeyer C., Li Y., Lau Y.F., Oosterhuis J.W., Looijenga L.H. Identification of germ cells at risk for neoplastic transformation in gonadoblastoma: an immunohistochemical study for OCT3/4 and TSPY. Hum. Pathol. 2005, 36:512-521.
11. Cameron F.J., Sinclair A.H. Mutations in SRY and SOX9: testis-determining genes. Hum. Mutat. 1997, 9:388-395.
12. Wagner T., Wirth J., Meyer J., Zabel B., Held M., Zimmer J., Pasantes J., Bricarelli F.D., Keutel J., Hustert E., Wolf U., Tommerup N., Schempp W., Scherer G. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 1994, 79:1111-1120.
13. Achermann J.C., Ito M., Hindmarsh P.C., Jameson J.L. Amutation in the gene encoding steroidogenic factor-1 causes XY sex reversal and adrenal failure in humans. Nat. Genet. 1999, 22:125-126.
14. Call K.M., Glaser T., Ito C.Y., Buckler A.J., Pelletier J., Haber D.A., Rose E.A., Kral A., Yeger H., Lewis W.H., et al. Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell 1990, 60:509-520.
15. Allali S., Muller J.B., Brauner R., Lourenco D., Boudjenah R., Karageorgou V., Trivin C., Lottmann H., Lortat-Jacob S., Nihoul-Fekete C., De Dreuzy O., McElreavey K., Bashamboo A. Mutation analysis of NR5A1 encoding steroidogenic factor 1 in 77 patients with 46, XY disorders of sex development (DSD) including hypospadias. PLoS One 2011, 6:e24117.
16. Canto P., Soderlund D., Reyes E., Mendez J.P. Mutations in the desert hedgehog (DHH) gene in patients with 46, XY complete pure gonadal dysgenesis. J.Clin. Endocrinol. Metab. 2004, 89:4480-4483.
17. Puffenberger E.G., Hu-Lince D., Parod J.M., Craig D.W., Dobrin S.E., Conway A.R., Donarum E.A., Strauss K.A., Dunckley T., Cardenas J.F., Melmed K.R., Wright C.A., Liang W., Stafford P., Flynn C.R., Morton D.H., Stephan D.A. Mapping of sudden infant death with dysgenesis of the testes syndrome (SIDDT) by a SNP genome scan and identification of TSPYL loss of function. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11689-11694.
18. Barbaro M., Oscarson M., Schoumans J., Staaf J., Ivarsson S.A., Wedell A. Isolated 46, XY gonadal dysgenesis in two sisters caused by a Xp21.2 interstitial duplication containing the DAX1 gene. J.Clin. Endocrinol. Metab. 2007, 92:3305-3313.
19. Ogata T., Matsuo N. Sex determining gene on the X chromosome short arm: dosage sensitive sex reversal. Acta Paediatr. Jpn. 1996, 38:390-398.
20. Jordan B.K., Mohammed M., Ching S.T., Delot E., Chen X.N., Dewing P., Swain A., Rao P.N., Elejalde B.R., Vilain E. Up-regulation of WNT-4 signaling and dosage-sensitive sex reversal in humans. Am. J. Hum. Genet. 2001, 68:1102-1109.
21. Calvari V., Bertini V., De Grandi A., Peverali G., Zuffardi O., Ferguson-Smith M., Knudtzon J., Camerino G., Borsani G., Guioli S. Anew submicroscopic deletion that refines the 9p region for sex reversal. Genomics 2000, 65:203-212.
22. Hughes I.A., Houk C., Ahmed S.F., Lee P.A. Consensus statement on management of intersex disorders. Arch. Dis. Child 2006, 91:554-563.
23. White S., Ohnesorg T., Notini A., Roeszler K., Hewitt J., Daggag H., Smith C., Turbitt E., Gustin S., van den Bergen J., Miles D., Western P., Arboleda V., Schumacher V., Gordon L., Bell K., Bengtsson H., Speed T., Hutson J., Warne G., Harley V., Koopman P., Vilain E., Sinclair A. Copy number variation in patients with disorders of sex development due to 46, XY gonadal dysgenesis. PLoS One 2011, 6:e17793.
24. Sekido R., Lovell-Badge R. Genetic control of testis development. Sex Dev. 2012.
25. Barbaro M., Cools M., Looijenga L.H., Drop S.L., Wedell A. Partial deletion of the NR5A1 (SF1) gene detected by synthetic probe MLPA in a patient with XY gonadal disorder of sex development. Sex Dev. 2011, 5:181-187.
26. Ledig S., Hiort O., Wunsch L., Wieacker P. Partial deletion of DMRT1 causes 46, XY ovotesticular disorder of sexual development. Eur. J. Endocrinol. 2012, 167:119-124.
27. Vinci G., Chantot-Bastaraud S., El Houate B., Lortat-Jacob S., Brauner R., McElreavey K. Association of deletion 9p, 46, XY gonadal dysgenesis and autistic spectrum disorder. Mol. Hum. Reprod. 2007, 13:685-689.
28. Ledig S., Hiort O., Scherer G., Hoffmann M., Wolff G., Morlot S., Kuechler A., Wieacker P. Array-CGH analysis in patients with syndromic and non-syndromic XY gonadal dysgenesis: evaluation of array CGH as diagnostic tool and search for new candidate loci. Hum. Reprod. 2010, 25:2637-2646.
29. Tannour-Louet M., Han S., Corbett S.T., Louet J.F., Yatsenko S., Meyers L., Shaw C.A., Kang S.H., Cheung S.W., Lamb D.J. Identification of de novo copy number variants associated with human disorders of sexual development. PLoS One 2010, 5:e15392.
30. Barbaro M., Cicognani A., Balsamo A., Löfgren A., Baldazzi L., Wedell A., Oscarson M. Gene dosage imbalances in patients with 46, XY gonadal DSD detected by an in-house-designed synthetic probe set for multiplex ligation-dependent probe amplification analysis. Clin. Genet. 2008, 73:453-464.
31. Barbaro M., Balsamo A., Anderlid B.M., Myhre A.G., Gennari M., Nicoletti A., Pittalis M.C., Oscarson M., Wedell A. Characterization of deletions at 9p affecting the candidate regions for sex reversal and deletion 9p syndrome by MLPA. Eur. J. Hum. Genet. 2009, 17:1439-1447.
32. Zhang J., Feuk L., Duggan G.E., Khaja R., Scherer S.W. Development of bioinformatics resources for display and analysis of copy number and other structural variants in the human genome. Cytogenet. Genome Res. 2006, 115:205-214.
33. Iafrate A.J., Feuk L., Rivera M.N., Listewnik M.L., Donahoe P.K., Qi Y., Scherer S.W., Lee C. Detection of large-scale variation in the human genome. Nat. Genet. 2004, 36:949-951.
34. Dreszer T.R., Karolchik D., Zweig A.S., Hinrichs A.S., Raney B.J., Kuhn R.M., Meyer L.R., Wong M., Sloan C.A., Rosenbloom K.R., Roe G., Rhead B., Pohl A., Malladi V.S., Li C.H., Learned K., Kirkup V., Hsu F., Harte R.A., Guruvadoo L., Goldman M., Giardine B.M., Fujita P.A., Diekhans M., Cline M.S., Clawson H., Barber G.P., Haussler D., James Kent W. The UCSC Genome Browser database: extensions and updates 2011. Nucleic Acids Res. 2012, 40:D918-D923.
35. Uhlen M., Oksvold P., Fagerberg L., Lundberg E., Jonasson K., Forsberg M., Zwahlen M., Kampf C., Wester K., Hober S., Wernerus H., Bjorling L., Ponten F. Towards a knowledge-based human protein atlas. Nat. Biotechnol. 2010, 28:1248-1250.
36. Nef S., Schaad O., Stallings N.R., Cederroth C.R., Pitetti J.L., Schaer G., Malki S., Dubois-Dauphin M., Boizet-Bonhoure B., Descombes P., Parker K.L., Vassalli J.D. Gene expression during sex determination reveals a robust female genetic program at the onset of ovarian development. Dev. Biol. 2005, 287:361-377.
37. Firth H.V., Richards S.M., Bevan A.P., Clayton S., Corpas M., Rajan D., Van Vooren S., Moreau Y., Pettett R.M., Carter N.P. DECIPHER: database of chromosomal imbalance and phenotype in humans using Ensembl resources. Am. J. Hum. Genet. 2009, 84:524-533.
38. Schouten J.P., McElgunn C.J., Waaijer R., Zwijnenburg D., Diepvens F., Pals G. Relative quantification of 40 nucleic acid sequences by multiplex ligation-dependent probe amplification. Nucleic Acids Res. 2002, 30:e57.
39. Stern R.F., Roberts R.G., Mann K., Yau S.C., Berg J., Ogilvie C.M. Multiplex ligation-dependent probe amplification using a completely synthetic probe set. Biotechniques 2004, 37:399-405.
40. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 2000, 132:365-386.
41. Barbaro M., Cook J., Lagerstedt-Robinson K., Wedell A. Multigeneration inheritance through fertile XX carriers of an NR0B1 (DAX1) locus duplication in a kindred of females with isolated XY gonadal dysgenesis. Int. J. Endocrinol. 2012, 2012:504904.
42. Eisenmann D.M., Arndt K.M., Ricupero S.L., Rooney J.W., Winston F. SPT3 interacts with TFIID to allow normal transcription in Saccharomyces cerevisiae. Genes Dev. 1992, 6:1319-1331.
43. Hirschhorn J.N., Winston F. SPT3 is required for normal levels of a-factor and alpha-factor expression in Saccharomyces cerevisiae. Mol. Cell Biol. 1988, 8:822-827.
44. Yu J., Madison J.M., Mundlos S., Winston F., Olsen B.R. Characterization of a human homologue of the Saccharomyces cerevisiae transcription factor spt3 (SUPT3H). Genomics 1998, 53:90-96.
45. Martinez E., Palhan V.B., Tjernberg A., Lymar E.S., Gamper A.M., Kundu T.K., Chait B.T., Roeder R.G. Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors invivo. Mol. Cell Biol. 2001, 21:6782-6795.
46. N. DiDonato, DECIPHER information regarding patient 254783 in personal e-mail correspondence, 2013.
47. Yariz K.O., Duman D., Seco C.Z., Dallman J., Huang M., Peters T.A., Sirmaci A., Lu N., Schraders M., Skromne I., Oostrik J., Diaz-Horta O., Young J.I., Tokgoz-Yilmaz S., Konukseven O., Shahin H., Hetterschijt L., Kanaan M., Oonk A.M., Edwards Y.J., Li H., Atalay S., Blanton S., Desmidt A.A., Liu X.Z., Pennings R.J., Lu Z., Chen Z.Y., Kremer H., Tekin M. Mutations in OTOGL, encoding the inner ear protein otogelin-like, cause moderate sensorineural hearing loss. Am. J. Hum. Genet. 2012, 91:872-882.
48. Online Mendelian Inheritance in Man, OMIM®, Johns Hopkins University, Baltimore, MD, MIM Number: {233300}: {11/02/2011}, World Wide Web URL: http://omim.org/.
49. Hasegawa H., Noguchi J., Yamashita M., Okada R., Sugimoto R., Furuya M., Unoki T., Funakoshi Y., Baba T., Kanaho Y. Phosphatidylinositol 4-phosphate 5-kinase is indispensable for mouse spermatogenesis. Biol. Reprod. 2012, 86. 136, 131-112.
50. Ishihara H., Shibasaki Y., Kizuki N., Katagiri H., Yazaki Y., Asano T., Oka Y. Cloning of cDNAs encoding two isoforms of 68-kDa type I phosphatidylinositol-4-phosphate 5-kinase. J.Biol. Chem. 1996, 271:23611-23614.
51. Beebe S.J., Oyen O., Sandberg M., Froysa A., Hansson V., Jahnsen T. Molecular cloning of a tissue-specific protein kinase (C gamma) from human testis-representing a third isoform for the catalytic subunit of cAMP-dependent protein kinase. Mol. Endocrinol. 1990, 4:465-475.
52. Reinton N., Haugen T.B., Orstavik S., Skalhegg B.S., Hansson V., Jahnsen T., Tasken K. The gene encoding the C gamma catalytic subunit of cAMP-dependent protein kinase is a transcribed retroposon. Genomics 1998, 49:290-297.
53. Walsh T., Pierce S.B., Lenz D.R., Brownstein Z., Dagan-Rosenfeld O., Shahin H., Roeb W., McCarthy S., Nord A.S., Gordon C.R., Ben-Neriah Z., Sebat J., Kanaan M., Lee M.K., Frydman M., King M.C., Avraham K.B. Genomic duplication and overexpression of TJP2/ZO-2 leads to altered expression of apoptosis genes in progressive nonsyndromic hearing loss DFNA51. Am. J. Hum. Genet. 2010, 87:101-109.