A novel follicle-stimulating hormone receptor mutation causing primary ovarian failure: a fertility application of whole exome sequencing

Human Reproduction

Volumn 31, Issue 4, 2016, Pages 905-914

  Bramble, Matthew S ^a   Goldstein, Ellen H ^a,b   Lipson, Allen ^a   Ngun, Tuck ^a   Eskin, Ascia ^a   Gosschalk, Jason E ^a   Roach, Lara ^a   Vashist, Neerja ^a   Barseghyan, Hayk ^a   Lee, Eric ^a   Arboleda, Valerie A ^a   Vaiman, Daniel ^c   Yuksel, Zafer ^d   Fellous, Marc ^c   Vilain, Eric ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SORBONNE UNIVERSITÉ   (France)

^d NONE   (Turkey)

Author keywords

follicle stimulating hormone receptor; premature ovarian failure; primary amenorrhea; resistant ovary syndrome; whole exome sequencing

Indexed keywords

CYCLIC AMP; FOLLITROPIN RECEPTOR; MUTANT PROTEIN; RECOMBINANT PROTEIN;

ADULT; ARTICLE; CASE REPORT; CELL MIGRATION; CONSANGUINEOUS MARRIAGE; CONTROLLED STUDY; EXOME; FEMALE; FLOW CYTOMETRY; GENETIC VARIABILITY; HOMOZYGOSITY; HUMAN; IN VITRO STUDY; INFERTILITY THERAPY; MISSENSE MUTATION; MOLECULAR PATHOLOGY; NEXT GENERATION SEQUENCING; OVARY INSUFFICIENCY; PERSONALIZED MEDICINE; PHENOTYPE; PRIMARY AMENORRHEA; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SIGNAL DETECTION; STEROIDOGENESIS; TRANSIENT TRANSFECTION; XX GONADAL DYSGENESIS; CHEMISTRY; CONSANGUINITY; DNA SEQUENCE; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HEK293 CELL LINE; HOMOZYGOTE; METABOLISM; MOLECULAR MODEL; PREMATURE OVARIAN FAILURE; PROTEIN TRANSPORT; SIBLING; TURKEY; VALIDATION STUDY; YOUNG ADULT;

ADULT; CONSANGUINITY; EXOME; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HEK293 CELLS; HOMOZYGOTE; HUMANS; MODELS, MOLECULAR; MUTATION, MISSENSE; PRIMARY OVARIAN INSUFFICIENCY; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; RECEPTORS, FSH; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA; SIBLINGS; TURKEY; YOUNG ADULT;

EID: 84963954442     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dew025     Document Type: Article

References (51)

1. Aittomaki K, Lucena JL, Pakarinen P, Sistonen P, Tapanainen J, Gromoll J, Kaskikari R, Sankila EM, Lehvaslaiho H, Engel AR et al. Mutation in the follicle-stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure. Cell 1995; 82: 959-968
2. Aittomaki K, Herva R, Stenman UH, Juntunen K, Ylostalo P, Hovatta O, De la Chapelle A. Clinical features of primary ovarian failure caused by a point mutation in the follicle-stimulating hormone receptor gene. J Clin Endocrinol Metab 1996; 81: 3722-3726
3. AlAsiri S, Basit S, Wood-Trageser MA, Yatsenko SA, Jeffries EP, Surti U, Ketterer DM, Afzal S, Ramzan K, Faiyaz-Ul Haque M et al. Exome sequencing reveals MCM8 mutation underlies ovarian failure and chromosomal instability. J Clin Invest 2015; 125: 258-262
4. Allen LA, Achermann JC, Pakarinen P, Kotlar TJ, Huhtaniemi IT, Jameson JL, Cheetham TD, Ball SG. A novel loss of function mutation in exon 10 of the FSH receptor gene causing hypergonadotrophic hypogonadism: clinical and molecular characteristics. Hum Reprod 2003; 18: 251-256
5. Arboleda VA, Lee H, Sanchez FJ, Delot EC, Sandberg DE, Grody WW, Nelson SF, Vilain E. Targeted massively parallel sequencing provides comprehensive genetic diagnosis for patients with disorders of sex development. Clin Genet 2013; 83: 35-43
6. Baxter RM, Arboleda VA, Lee H, Barseghyan H, Adam MP, Fechner PY, Bargman R, Keegan C, Travers S, Schelley S et al. Exome sequencing for the diagnosis of 46, XY disorders of sex development. J Clin Endocrinol Metab 2015; 100: E333-E344
7. Beau I, Touraine P, Meduri G, Gougeon A, Desroches A, Matuchansky C, Milgrom E, Kuttenn F, Misrahi M. A novel phenotype related to partial loss of function mutations of the follicle stimulating hormone receptor. J Clin Invest 1998; 102: 1352-1359
8. Caburet S, Arboleda VA, Llano E, Overbeek PA, Barbero JL, Oka K, Harrison W, Vaiman D, Ben-Neriah Z, Garcia-Tunon I et al. Mutant cohesin in premature ovarian failure. N Engl J Med 2014; 370: 943-949
9. Chang EM, Song HS, Lee DR, LeeWS, YoonTK. In vitro maturation of human oocytes: its role in infertility treatment and new possibilities. Clin Exp Reprod Med 2014; 41: 41-46
10. Channing CP, Schaerf FW, Anderson LD, Tsafriri A. Ovarian follicular and luteal physiology. Int Rev Physiol 1980; 22: 117-201
11. Chian RC, Lim JH, Tan SL. State of the art in in vitro oocyte maturation. Curr Opin Obstet Gynecol 2004; 16: 211-219
12. De Leener A, Montanelli L, Van Durme J, Chae H, Smits G, Vassart G, Costagliola S. Presence and absence of follicle-stimulating hormone receptor mutations provide some insights into spontaneous ovarian hyperstimulation syndrome physiopathology. J Clin Endocrinol Metab 2006; 91: 555-562
13. De Vries L, Behar DM, Smirin-Yosef P, Lagovsky I, Tzur S, Basel-Vanagaite L. Exome sequencing reveals SYCE1 mutation associated with autosomal recessive primary ovarian insufficiency. J Clin Endocrinol Metab 2014; 99: E2129-E2132
14. Doherty E, Pakarinen P, Tiitinen A, Kiilavuori A, Huhtaniemi I, Forrest S, Aittomaki K. A Novel mutation in the FSH receptor inhibiting signal transduction and causing primary ovarian failure. J Clin Endocrinol Metab 2002; 87: 1151-1155
15. Fonseca DJ, Patino LC, Suarez YC, De Jesus Rodriguez A, Mateus HE, Jimenez KM, Ortega-Recalde O, Diaz-Yamal I, Laissue P. Next generation sequencing in women affected by nonsyndromic premature ovarian failure displays new potential causative genes and mutations. Fertil Steril 2015; 104: 154-162 e152
16. Garcia-Velasco JA, Rodriguez S, Agudo D, Pacheco A, Schneider J, Pellicer A. FSH receptor in vitro modulation by testosterone and hCG in human luteinized granulosa cells. Eur J Obstet Gynecol Reprod Biol 2012; 165: 259-264
17. Ghadami M, Salama SA, Khatoon N, Chilvers R, Nagamani M, Chedrese PJ, Al-Hendy A. Toward gene therapy of primary ovarian failure: adenovirus expressing human FSH receptor corrects the Finnish C566T mutation. Mol Hum Reprod 2008; 14: 9-15
18. Ghadami M, El-Demerdash E, Salama SA, Binhazim AA, Archibong AE, Chen X, Ballard BR, Sairam MR, Al-Hendy A. Toward gene therapy of premature ovarian failure: intraovarian injection of adenovirus expressing human FSH receptor restores folliculogenesis in FSHR(-/-) FORKO mice. Mol Hum Reprod 2010; 16: 241-250
19. Gilissen C, Hoischen A, Brunner HG, Veltman JA. Unlocking Mendelian disease using exome sequencing. Genome Biol 2011; 12: 228
20. Gromoll J, Simoni M, Nordhoff V, Behre HM, De Geyter C, Nieschlag E. Functional and clinical consequences of mutations in the FSH receptor. Mol Cell Endocrinol 1996; 125: 177-182
21. Huhtaniemi IT, Aittomaki K. Mutations of follicle-stimulating hormone and its receptor: effects on gonadal function. Eur J Endocrinol 1998; 138: 473-481
22. Janovick JA, Maya-NunezG, Ulloa-AguirreA, Huhtaniemi IT, Dias JA, Verbost P, Conn PM. Increased plasma membrane expression of human folliclestimulating hormone receptor by a small molecule thienopyr(im)idine. Mol Cell Endocrinol 2009; 298: 84-88
23. Jiang X, Dias JA, He X. Structural biology of glycoprotein hormones and their receptors: insights to signaling. Mol Cell Endocrinol 2014; 382: 424-451
24. Kallberg M, Wang H, Wang S, Peng J, Wang Z, Lu H, Xu J. Template-based protein structure modeling using the RaptorXweb server. Nat Protoc 2012; 7: 1511-1522
25. Kallio S, Aittomaki K, Piltonen T, Veijola R, Liakka A, Vaskivuo TE, Dunkel L, Tapanainen JS. Anti-Mullerian hormone as a predictor of follicular reserve in ovarian insufficiency: special emphasis on FSH-resistant ovaries. Hum Reprod 2012; 27: 854-860
26. Katari S, Wood-Trageser MA, Jiang H, Kalynchuk E, Muzumdar R, Yatsenko SA, Rajkovic A. Novel inactivating mutation of the FSH receptor in two siblings of Indian origin with premature ovarian failure. J Clin Endocrinol Metab 2015; 100: 2154-2157
27. Ku CS, Naidoo N, Pawitan Y. Revisiting Mendelian disorders through exome sequencing. Hum Genet 2011; 129: 351-370
28. Kuechler A, Hauffa BP, Koninger A, Kleinau G, Albrecht B, Horsthemke B, Gromoll J. An unbalanced translocation unmasks a recessive mutation in the follicle-stimulating hormone receptor (FSHR) gene and causes FSH resistance. Eur J Hum Genet 2010; 18: 656-661
29. Le Quesne Stabej P, Williams HJ, James C, Tekman M, Stanescu HC, Kleta R, Ocaka L, Lescai F, Storr HL, Bitner-Glindzicz M et al. STAG3. truncating variant as the cause of primary ovarian insufficiency. Eur J Hum Genet 2015; 24: 135-138
30. Lee H, Deignan JL, Dorrani N, Strom SP, Kantarci S, Quintero-Rivera F, Das K, Toy T, Harry B, Yourshaw M et al. Clinical exome sequencing for genetic identification of rare Mendelian disorders. J Am Med Assoc 2014; 312: 1880-1887
31. MaJ, Wang S, Zhao F, XuJ. Protein threading using context-specific alignment potential. Bioinformatics 2013; 29: i257-i265
32. Meduri G, Touraine P, Beau I, Lahuna O, Desroches A, Vacher-Lavenu MC, Kuttenn F, Misrahi M. Delayed puberty and primary amenorrhea associated with a novel mutation of the human follicle-stimulating hormone receptor: clinical, histological, and molecular studies. J Clin Endocrinol Metab 2003; 88: 3491-3498
33. Nakamura Y, Maekawa R, YamagataY, Tamura I, Sugino N.Anovel mutation in exon8 of the follicle-stimulating hormone receptor in a woman with primary amenorrhea. Gynecol Endocrinol 2008; 24: 708-712
34. Nogueira D, Sadeu JC, Montagut J. In vitro oocyte maturation: current status. Semin Reprod Med 2012; 30: 199-213
35. Oktay K, Briggs D, Gosden RG. Ontogeny of follicle-stimulating hormone receptor gene expression in isolated human ovarian follicles. J Clin Endocrinol Metab 1997; 82: 3748-3751
36. Patsoula E, LoutradisD, DrakakisP, Michalas L, BletsaR, Michalas S.Messenger RNA expression for the follicle-stimulating hormone receptor and luteinizing hormone receptor in human oocytes and preimplantationstage embryos. Fertil Steril 2003; 79: 1187-1193
37. Peng J, Xu J. A multiple-Template approach to protein threading. Proteins 2011a; 79: 1930-1939
38. Peng J, Xu J. RaptorX: exploiting structure information for protein alignment by statistical inference. Proteins 2011b; 79(Suppl 10): 161-171
39. Persani L, Rossetti R, Cacciatore C. Genes involved in human premature ovarian failure. J Mol Endocrinol 2010; 45: 257-279
40. Pierce SB, Gersak K, Michaelson-Cohen R, Walsh T, Lee MK, Malach D, Klevit RE, King MC, Levy-Lahad E. Mutations in LARS2, encoding mitochondrial leucyl-TRNA synthetase, lead to premature ovarian failure and hearing loss in Perrault syndrome.Am JHumGenet 2013; 92: 614-620
41. PracticeCommittees of the American Society for Reproductive Medicine and the Society for Assisted Reproductive Technology. In vitro maturation: a committee opinion. Fertil Steril 2013; 99: 663-666
42. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, De Bakker PI, Daly MJ et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007; 81: 559-575
43. Rabbani B, Mahdieh N, Hosomichi K, Nakaoka H, Inoue I. Next-generation sequencing: impact of exome sequencing in characterizing Mendelian disorders. J Hum Genet 2012; 57: 621-632
44. Richards CS, Bale S, Bellissimo DB, Das S, GrodyWW, Hegde MR, Lyon E, Ward BE. Molecular Subcommittee of the ALQAC. ACMG recommendations for standards for interpretation and reporting of sequence variations: Revisions 2007. Genet Med 2008; 10: 294-300
45. Smith KR, Bromhead CJ, Hildebrand MS, Shearer AE, Lockhart PJ, Najmabadi H, Leventer RJ, McGillivray G, Amor DJ, Smith RJ et al. Reducing the exome search space for Mendelian diseases using genetic linkage analysis of exome genotypes. Genome Biol 2011; 12: R85
46. Sridharan R, Zuber J, Connelly SM, Mathew E, Dumont ME. Fluorescent approaches for understanding interactions of ligands with G protein coupled receptors. Biochim Biophys Acta 2014; 1838: 15-33
47. Touraine P, Beau I, GougeonA, MeduriG, Desroches A, PichardC, Detoeuf M, Paniel B, Prieur M, Zorn JR et al. New natural inactivating mutations of the follicle-stimulating hormone receptor: correlations between receptor function and phenotype. Mol Endocrinol 1999; 13: 1844-1854
48. Wood-Trageser MA, Gurbuz F, Yatsenko SA, Jeffries EP, Kotan LD, Surti U, Ketterer DM, Matic J, Chipkin J, Jiang H et al. MCM9 mutations are associated with ovarian failure, short stature, and chromosomal instability. Am J Hum Genet 2014; 95: 754-762
49. Yang Y, Muzny DM, Reid JG, Bainbridge MN, Willis A, Ward PA, Braxton A, Beuten J, Xia F, Niu Z et al. Clinical whole-exome sequencing for the diagnosis of Mendelian disorders. N Engl J Med 2013; 369: 1502-1511
50. Yariz KO, Walsh T, Uzak A, Spiliopoulos M, Duman D, Onalan G, King MC, Tekin M. Inherited mutation of the luteinizing hormone/choriogonadotropin receptor (LHCGR) in empty follicle syndrome. Fertil Steril 2011; 96: e125-e130
51. Yourshaw M, Taylor SP, Rao AR, Martin MG, Nelson SF. Rich annotation of DNA sequencing variants by leveraging the Ensembl Variant Effect Predictor with plugins. Brief Bioinform 2014; 16: 255-264