Gene dosage as a relevant mechanism contributing to the determination of ovarian function in Turner syndrome

Human Reproduction

Volumn 29, Issue 2, 2014, Pages 368-379

  Castronovo, Chiara ^a   Rossetti, Raffaella ^b   Rusconi, Daniela ^a   Recalcati, Maria P ^a   Cacciatore, Chiara ^a,b   Beccaria, Elena ^a   Calcaterra, Valeria ^c   Invernizzi, Pietro ^d   Larizza, Daniela ^c   Finelli, Palma ^a,b   Persani, Luca ^a,b  

^a ISTITUTO AUXOLOGICO ITALIANO   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

^d HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

BMP15; Copy number variations; Ovary; Turner syndrome; X chromosome

Indexed keywords

BONE MORPHOGENETIC PROTEIN 15; GENOMIC DNA;

ADOLESCENT; ADULT; ARTICLE; CHILD; CHROMOSOME ANALYSIS; CHROMOSOME DELETION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FEMALE FERTILITY; GENE DOSAGE; GENE DUPLICATION; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; KARYOTYPING; MICROARRAY KIT; OVARY FUNCTION; PILOT STUDY; PRIMARY AMENORRHEA; REAL TIME POLYMERASE CHAIN REACTION; SCHOOL CHILD; SEX CHROMOSOME MOSAICISM; TURNER SYNDROME; YOUNG ADULT;

BMP15; COPY NUMBER VARIATIONS; OVARY; TURNER SYNDROME; X CHROMOSOME;

ADOLESCENT; CHILD; CHROMOSOMES, HUMAN, X; COMPARATIVE GENOMIC HYBRIDIZATION; FEMALE; FERTILITY; GENE DOSAGE; HUMANS; KARYOTYPING; MENARCHE; MOSAICISM; OVARIAN DISEASES; OVARY; PUBERTY; TURNER SYNDROME;

EID: 84893065856     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/det436     Document Type: Article

References (50)

1. Aboura A, Dupas C, Tachdjian G, Portnoí MF, Bourcigaux N, Dewailly D, Frydman R, Fauser B, Ronci-Chaix N, Donadille B. et al.: Array comparative genomic hybridization profiling analysis reveals deoxyribonucleic acid copy number variations associated with premature ovarian failure. J Clin Endocrinol Metab 2009;9411:4540-4546.
2. Aso K, Koto S, Higuchi A, Ariyasu D, IzawaM, Miyamoto Igaki J, Hasegawa Y. Serum FSH level below 10 mIU/mL at twelve years old is an index of spontaneous and cyclical menstruation in Turner syndrome. Endocr J 2010;57:909-913.
3. Ballif BC, Rorem EA, Sundin K, Lincicum M, Gaskin S, Coppinger J, Kashork CD, Shaffer LG, Bejjani BA. Detection of low-level mosaicism by array CGH in routine diagnostic specimens. Am J Med Genet A 2006; 140:2757-2767.
4. Chiu YL, Greene WC. The APOBEC3 cytidine deaminases: An innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu Rev Immunol 2008;26:317-353.
5. Choi J, Hwang YK, Choi YJ, YooKE, Kim JH, NamSJ, Yang JH, Lee SJ, Yoo KH, Sung KWet al. Neuronal apoptosis inhibitory protein is overexpressed in patients with unfavourable prognostic factors in breast cancer. J Korean Med Sci 2007;22(Suppl):S17-S23.
6. Di Pasquale E, Beck-Peccoz P, Persani L. Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am J Hum Genet 2004;75:106-111.
7. Dube JL, Wang P, Elvin J, Lyons KM, Celeste AJ, Matzuk MM. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol 1998;12:1809-1817.
8. Dudding TE, Lawrence O, Winship I, Froyen G, Vandewalle J, Scott R, Shelling AN. Array comparative genomic hybridization for the detection of submicroscopic copy number variations of the X chromosome in women with premature ovarian failure. Hum Reprod 2010;25: 3159-3160.
9. Fechner PY, Davenport ML, Qualy RL, Ross JL, Gunther DF, Eugster EA, Huseman C, Zagar AJ, Quigley CA; Toddler Turner Study Group. Differences in follicle-stimulating hormone secretion between 45, X monosomy Turner syndrome and 45, X/46, XX mosaicism are evident at an early age. J Clin Endocrinol Metab 2006;91:4896-4902.
10. Galloway SM, McNatty KP, Cambridge LM, Laitinen MP, Juengel JL, Jokiranta JL, McLaren RJ, Luiro K, Dodds KG, Montgomery GW. et al.: Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet 2000;25:279-283.
11. Gleicher N, Weghofer A, Barad DH. The role of androgens in follicle maturation and ovulation induction: Friend or foe of infertility treatment? Reprod Biol Endocrinol 2011;9:116.
12. Gracia Bouthelier R, Oliver Iguacel A, Gonzalez Casado I, Alcalde de Alvaré A. Optimization of treatment in Turner's syndrome. J Pediatr Endocrinol Metab 2004;17:427-434.
13. Hagen CP, Main KM, Kjaergaard S, Juul A. FSH, LH, inhibin B and estradiol levels in Turner syndrome depend on age and karyotype: Longitudinal study of 70 Turner girls with or without spontaneous puberty. Hum Reprod 2010;25:3134-3141.
14. Hanrahan JP, Gregan SM, Mulsant P, Mullen M, Davis GH, Powell R, Galloway SM. Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol Reprod 2004; 70:900-909.
15. Held KR, Kerber S, Kaminsky E, Singh S, Goetz P, Seemanova E, Goedde HW. Mosaicism in 45, X Turner syndrome: Does survival in early pregnancy depend on the presence of two sex chromosomes? Hum Genet 1992; 88:288-294.
16. Kallio S, Aittomäki 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.
17. Kim J, Bagchi IC, Bagchi MK. Control of ovulation in mice by progesterone receptor-regulated gene networks. Mol Hum Reprod 2011;15: 821-828.
18. Koning FA, Newman EN, Kim EY, Kunstman KJ, Wolinsky SM, Malim MH. Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J Virol 2009;83:9474-9485.
19. Ledig S, Röpke A, Wieacker P. Copy number variants in premature ovarian failure and ovarian dysgenesis. Sex Dev 2010;4:225-232.
20. Liao C, Fu F, Yang X, Sun YM, Li DZ. Analysis of Chinesewomenwith primary ovarian insufficiency by high resolution array-comparative genomic hybridization. Chin Med J 2011;124:1739-1742.
21. Lichter P, Cremer T. Chromosome analysis by non-isotopic in situ hybridization. In Rooney DE, Czepulkowski BH (eds). Human Cytogenetics. A Practical Approach. Oxford: IRL Press at Oxford University Press, 1992, 157-192.
22. Lichter P, Tang CJ, Call K, Hermanson G, Evans GA, Housman D, Ward DC. High resolution mapping of human chromosome 11 by in situ hybridization with cosmid clones. Science 1990;247:64-69.
23. Martín Campagne E, Roa LlamazaresC. Spontaneous puberty and menarche in a patient with Turner syndrome and 45X monosomy. An Pediatr 2008; 70:200-202.
24. McGuire MM, Bowden W, Engel NJ, Ahn HW, Kovanci E, Rajkovic A. Genomic analysis using high-resolution single-nucleotide polymorphism arrays reveals novel microdeletions associated with premature ovarian failure. Fertil Steril 2011;95:1595-1600.
25. McNatty KP, Moore LG, Hudson NL, Quirke LD, Lawrence SB, Reader K, Hanrahan JP, Smith P, Groome NP, Laitinen M. et al.: The oocyte and its role in regulating ovulation rate: A new paradigm in reproductive biology. Reproduction 2004;128:379-386.
26. Nyegaard M, Overgaard MT, Su YQ, Hamilton AE, Kwintkiewicz J, Hsieh M, Nayak NR, Conti M, Conover CA, Giudice LC. Lack of functional pregnancy-Associated plasma protein-A (PAPPA) compromises mouse ovarian steroidogenesis and female fertility. Biol Reprod 2010; 82:1129-1138.
27. Ogata T, Matsuo N. Turner syndrome and female sex chromosome aberrations: Deduction of the principal factors involved in the development of clinical features. Hum Genet 1995;95:607-629.
28. Ohnishi J, Ohnishi E, Shibuya H, Takahashi T. Functions for proteinases in the ovulatory process. Biochim Biophys Acta 2005;1751:95-109.
29. Pasquino AM, Passeri F, Pucarelli I, Segni M, Municchi G. Spontaneous pubertal development in Turner's syndrome. Italian Study Group for Turner's Syndrome. J Clin Endocrinol Metab 1997;82:1810-1813.
30. Persani L, Rossetti R, CacciatoreC, Bonomi M. Primary ovarian insufficiency: X chromosome defects and autoimmunity. J Autoimmun 2009;33:35-41.
31. Persani L, Rossetti R, Cacciatore C. Genes involved in human premature ovarian failure. J Mol Endocrinol 2010;45:405.
32. Persani L, Rossetti R, Cacciatore C, Fabre S. Genetic defects of ovarian TGF-b-like factors and premature ovarian failure. J Endocrinol Invest 2011;34:244-251.
33. Prakash S, GuoD, Maslen CL, Silberbach M, Milewicz D, BondyCA;GenTAC Investigators. Single-nucleotide polymorphism array genotyping is equivalent to metaphase cytogenetics for diagnosis of Turner syndrome. Genet Med. June 6 2013. doi:10.1038/gim.2013.77.
34. Quilter CR, Karcanias AC, Bagga MR, Duncan S, Murray A, Conway GS, Sargent CA, Affara NA. Analysis of X chromosome genomic DNA sequence copy number variation associated with premature ovarian failure (POF). Hum Reprod 2010;258:2139-2150.
35. Ranke MB, Saenger P. Turner's syndrome. Lancet 2001;358:309-314.
36. Reddy KS, Mak L. Mosaic unbalanced structural abnormalities confirmed using FISH on buccal mucosal cells. Ann Genet 2001;44:37-40.
37. Reynaud K, Cortvrindt R, Verlinde F, De Schepper J, Bourgain C, Smitz J. Number of ovarian follicles in human fetuses with the 45, X karyotype. Fertil Steril 2004;81:1112-1119.
38. Rossetti R, Di Pasquale E, Marozzi A, Bione S, Toniolo D, Grammatico P, Nelson LM, Beck-Peccoz P, Persani L. BMP15 mutations associated with primary ovarian insufficiency cause a defective production of bioactive protein. Hum Mutat 2009;30:804-810.
39. Saenger P. Turner's syndrome. N Engl J Med 1996;335:1749-1754.
40. Sasseville M, Albuz FK, Cô té N, Guillemette C, Gilchrist RB, Richard FJ. Characterization of novel phosphodiesterases in the bovine ovarian follicle. Biol Reprod 2009;81:415-425.
41. Sekine Y, Ikeda O, Hayakawa Y, Tsuji S, Imoto S, Aoki N, Sugiyama K, Matsuda T. DUSP22/LMW-DSP2 regulates estrogen receptor-Alphamediated signaling through dephosphorylation of Ser-118. Oncogene 2007;26:6038-6049.
42. Sun QY, Miao YL, Schatten H. Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 2009; 1:2741-2747.
43. Sybert VP, McCauley E. Turner's syndrome. N Engl J Med 2004; 351:1227-1238.
44. Toniolo D. X-linked premature ovarian failure: A complex disease. Curr Opin Genet Dev 2006;6:293-300.
45. Turner EC, Hughes J, Wilson H, Clay M, Mylonas KJ. Conditional ablation of macrophages disrupts ovarian vasculature. Reproduction 2011; 141:821-831.
46. Wang C, Prossnitz ER, Roy SK. G protein-coupled receptor 30 expression is required for estrogen stimulation of primordial follicle formation in the hamster ovary. Endocrinology 2008;149:4452-4461.
47. Wang B, Wen Q, Ni F, Zhou S, Wang J, Cao Y, Ma X. Analyses of growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) mutation in Chinese women with premature ovarian failure. Clin Endocrinol 2010;72:135-136.
48. Wu R, Van der Hoek KH, Ryan NK, Norman RJ, Robker RL. Macrophage contributions to ovarian function. Hum Reprod Update 2004;10:119-133.
49. Zimmermann B, Chiorini JA, Ma Y, Kotin RM, Herberg FW. PrKX is a novel catalytic subunit of the cAMP-dependent protein kinase regulated by the regulatory subunit type I. J Biol Chem 1999;274:5370-5378.
50. Zinn AR, Ross JL. Turner syndrome and haploinsufficiency. Curr Opin Genet Dev 1998;8:322-327.