Variable expression of the Fragile X Mental Retardation 1 (FMR1) gene in patients with premature ovarian failure syndrome is not dependent on number of (CGG)n triplets in exon 1

Human Reproduction

Volumn 26, Issue 5, 2011, Pages 1241-1251

  Schuettler, J ^a,c   Peng, Z ^a   Zimmer, J ^a   Sinn, P ^b   Von Hagens, C ^a   Strowitzki, T ^a   Vogt, P H ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b Dept Gynaecological Endocrinol R   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

(CGG) triplet numbers; Fragile X Mental Retardation 1 gene expression; ovarian reserve; premature ovarian failure risk

Indexed keywords

DNA; FRAGILE X MENTAL RETARDATION PROTEIN; MESSENGER RNA; RNA;

ADULT; ARTICLE; CONTROLLED STUDY; DNA ISOLATION; EXON; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GRANULOSA CELL; HUMAN; IMMUNOHISTOCHEMISTRY; LEUKOCYTE; MAJOR CLINICAL STUDY; OVARY FOLLICLE DEVELOPMENT; PREMATURE OVARIAN FAILURE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RNA ISOLATION; TISSUE SECTION;

EID: 79955423649     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/der018     Document Type: Article

References (82)

1. Albright F, Smith PH, Fraser R. A syndrome characterized by primary ovarian insufficiency and decreased stature: report of 11 cases with a digression on hormonal control of axillary and pubic hair. Am J Med Sci 1942;204:625-648.
2. Allen EG, He W, Yadav-Shah M. A Study of the distributional characteristics of FMR1 transcript levels in 238 individuals. Hum Genet 2004;114:439-447. (Pubitemid 38678921)
3. Allen EG, Sullivan AK, Marcus M, Small C, Dominguez C, Epstein MP, Charen K, He W, Taylor KC, Sherman SL. Examination of reproductive aging milestones among women who carry the FMR1 premutation. Hum Reprod 2007;8:2142-2152. (Pubitemid 47241859)
4. Allingham-Hawkins DJ, Babul-Hirji R, Chitayat D, Holden JJ, Yang KT, Lee C, Hudson R, Gorwill H, Nolin SL, Glicksman A et al. Fragile X premutation is a significant risk factor for premature ovarian failure: the International Collaborative POF in Fragile X study-preliminary data. Am J Med Genet 1999;83:322-325. (Pubitemid 29162637)
5. Baechner D, Manca A, Steinbach P, Wöhle D, Just W, Vogel W, Hameister H, Poustka A. Enhanced expresssion of the murine FMR1 gene during germ cell proliferation suggests a spezial function in both the male and the female gonad. Hum Mol Genet 1993;12:2043-2050. (Pubitemid 24003396)
6. Beilina A, Tassone F, Schwartz PH, Sahota P, Hagerman PJ. Redistribution of transcription start sites within the FMR1 promoter region with expansion of the downstream CGG-repeat element. Hum Mol Genet 2004;13:543-549. (Pubitemid 38313213)
7. Bennett CE, Conway GS, Macpherson JN, Jacobs PA, Murray A. Intermediate sized CGG repeats are not a common cause of idiopathic premature ovarian failure. Hum Reprod 2010;5:1335-1338.
8. Binelli M, Murphy BD. Coordinated regulation of folllicle development by germ and somatic cells. Reprod Fertil Dev 2009;22:1-12.
9. Bodega B, Bione S, Dalpra L, Toniolo D, Ornaghi F, Vegetti W, Ginelli E, Marozzi A. Influence of intermediate and uninterrupted FMR1 CGG expansions in premature ovarian failure manifestation. Hum Reprod 2006;21:952-957.
10. Bretherick KL, Fluker MR, Robinson WP. FMR1 repeat sizes in the gray zone and high end of the normal range are associated with premature ovarian failure. Hum Genet 2005;117:376-382. (Pubitemid 41194564)
11. Chatterjee S, Maitra A, Kadam S, Patel Z, Gokral J, Meherji P. Archived issues. Reprod Biomed Online 2009;2:281-286.
12. n repeat element within the 5' untranslated region of the FMR1 message provides both positive and negative cis effects on in vivo translation of a downstream reporter. Hum Mol Genet 2003; 23:3067-3074. (Pubitemid 37508879)
13. Coffee B, Zhang F, Ceman S, Warren S, Reines D. Histone Modifications depict an aberrantly heterochromatinized FMR1 gene in fragile X syndrome. Am J Hum Genet 2002;71:923-932. (Pubitemid 135750522)
14. Conway GS, Payne NN, Webb J, Murray A, Jacobs PA. Fragile X premutation screening in women with premature ovarian failure. Hum Reprod 1999;14:573-575. (Pubitemid 29097424)
15. Cooper AR, Baker VL, Sterlin EW, Ryan ME, Woodruff TK, Nelson LM. The time is now for a new approach to primary ovarian insufficiency. Fertil Steril 2010. doi:10.1016/j.fertnstert.2010.01.016.
16. Coulam CB, Stringfellow S, Hoefnagel D. Evidence for a genetic factor in the etiology of premature ovarian failure. Fertil Steril 1983; 40:693-695. (Pubitemid 14238517)
17. Coulam CB, Adamson SC, Annegers JF. Incidence of premature ovarian failure. Obstet Gynecol 1986;67:604-606. (Pubitemid 16116286)
18. Cronister A, DiMaio M, Mohoney MJ, Donnenfeld AE, Hallam S. Fragile X syndrome carrier screening in the prenatal genetic counselling setting. Genet Med 2005;7:246-250. (Pubitemid 40638070)
19. Davison RM, Fox M, Conway GS. Mapping of the POF1 locus and identification of putative genes for premature ovarian failure. Mol Hum Reprod 2000;6:314-318. (Pubitemid 30171517)
20. Dixit H, Rao L, Padmalatha V, Raseswari T, Kapu AK, Panda B, Murthy K, Tosh D, Nallari P, Deenadayal M et al. Genes governing premature ovarian failure. Repr Biomed Online 2010;20:724-740.
21. Fassnacht W, Mempel A, Strowitzki T, Vogt PH. Premature ovarian failure (POF) syndrome: towards the molecular clinical analysis of its genetic complexity. Curr Med Chem 2006;13: 1397-1410.
22. Fu YH, Kuhl DP, Pizzuti A, Pieretti M, Sutcliffe JS, Richards S, Verkerk AJ, Holden JJ, Fenwick RG Jr, Warren ST et al. Variation of the CGG repeat at the fragile X site results in genetic instability: resolution of the Sherman paradox. Cell 1991;67:1047-1058. (Pubitemid 121001519)
23. Garća-Alegŕa E, Ibáñez B, Ḿnguez M, Poch M, Valiente A, Sanz-Parra A, Martinez-Bouzas C, Beristain E, Tejada MI. Analysis of FMR1 gene expression in female premutation carriers using robust segmented linear regression models. RNA 2007;13:756-762. (Pubitemid 46641535)
24. Garcia-Arocena D, Hagerman PJ. Advances in understanding the molecular basis of FXTAS. Hum Mol Genet 2010;19:83-89.
25. Gheldof N, Tabuchi TM, Dekker J. The active FMR1 promoter is associated with a large domain of altered chromatin conformation with embedded local histone modifications. PNAS 2006; 33:12463-12468. (Pubitemid 44267282)
26. Gilad Y, Rifkin SA, Pritchard JK. Revealing the architecture of gene regulation: the promise of eQTL studies. Cell 2008.
27. Gleicher N, Barad DH. Can the FMR1 gene predict early ovarian aging? Womens Health 2010;6:165-169.
28. Gleicher N, Weghofer A, Oktay K, Barad DH. Relevance of triple CGG repeats in the FMR1 gene to ovarian reserve. Reprod Biomed Online 2009;19:385-390.
29. Gleicher N, Weghofer A, Barad DH. Ovarian reserve determinations suggest new function of FMR1 (fragile X gene) in regulating ovarian ageing. Reprod Biomed Online 2010;20:768-775.
30. Godler DE, Tassone F, Loesch DZ, Kimball Taylor A, Gehling F, Jenssen Hagerman R, Brugess T, Ganesamoorthy D, Hennerich D, Gordon L et al. Methylation of novel markers of fragile X alleles is inversely correlated with FMRP expression and FMR1 activation ratio. Hum Mol Genet 2010;8:1618-1632.
31. Goswami D, Conway G. Premature ovarian failure. Hum Reprod Update 2005;4:391-410. (Pubitemid 40895467)
32. Gougeon A. Human ovarian follicular development: from activation of resting follicles to preovulatory maturation. Ann Endorinol 2010; 71:132-143.
33. Jin P, Zarnescu DC, Ceman S, Nakamoto M, Mowrey J, Jongens TA, Nelson DL, Moses K, Warren ST. Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat Neurosci 2004;7:113-117. (Pubitemid 38129786)
34. van Kasteren YM, Hundscheid RD, Smits AP, Cremers FP, Van Zonneveld P, Braat DD. Familial idiopathic premature ovarian failure: an overrated and underestimated genetic disease. Hum Reprod 1999; 14:2455-2459. (Pubitemid 29473910)
35. Kenneson A, Cramer DW, Warren ST. Fragile X premutations are not a major cause of early menopause. Am J Hum Genet 1997; 61:1362-1369. (Pubitemid 28046913)
36. Kenneson A, Zhang F, Hagedorn CH, Warren ST. Reduced FMRP and increased FMR1 transcription is proportionally associated with CGG repeat number in intermediate-length and premutation carriers. Hum Mol Genet 2001;10:1449-1454. (Pubitemid 32684886)
37. Krauss CM, Turksoy RN, Atkins L, McLaughlin C, Brown LG, Page DC. Familial premature ovarian failure due to an interstitial deletion of the long arm of the X chromosome. N Engl J Med 1987;317:125-131. (Pubitemid 17092148)
38. Krysko DV, Diez-Fraile A, Criel G, Svistunov A, Vandenabeele P, D'Herde K. Life and death of female gametes during oogenesis and folliculogenesis. Apoptosis 2008;13:1065-1087.
39. Laggerbauer B, Ostareck D, Keidel EM, Ostareck-Lederer A, Fischer U. Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum Mol Genet 2001;4:329-338. (Pubitemid 32166544)
40. Laml T, Preyer O, Umek W, Hengstschlager M, Hanzal H. Genetic disorders in premature ovarian failure. Hum Reprod Update 2002; 8:483-491. (Pubitemid 35175208)
41. Marozzi A, Manfredini E, Tibiletti MG, Furlan D, Villa N, Vegetti W, Crosignani PG, Ginelli E, Meneveri R, Dalpra L. Molecular definition of Xq common-deleted region in patients affected by premature ovarian failure. Hum Genet 2000;107:304-311.
42. McNatty KP, Juengel JL, Reader KL, Lun S, Myllymaa S, Lawrence SB, Westren A, Meerasahib MF, Mottershead DG, Groome NG et al. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulare granulosa cell function. Reproduction 2005; 129:473-480. (Pubitemid 40542173)
43. Miyoshi T, Otsuka F, Suzuki J, Takeda M, Inagaki K, Kano Y, Otani H, Mimura Y, Ogura T, Makino H. Mutual regulation of follicle-stimulating hormone signalling and bone morphogenetic protein system in human granulosa cells. Biol Reprod 2006;74:1073-1082. (Pubitemid 47394284)
44. n-3'-binding protein is targeted to the nucleus and affects the activity of the FMR1 promoter. J Biol Chem 2000;9:6447-6452. (Pubitemid 30129942)
45. Nelson LM, Anasti JN, Kimzey LM. Development of luteinized graafian follicles in patients with karyotypically normal spontaneous premature ovarian failure. J Clin Endocrinol Metab 1994;79:1470-1475. (Pubitemid 24369868)
46. Nelson LM. Clinical practice. Primary ovarian insufficiency. N Engl J Med 2009;360:606-614.
47. Oostra BA, Willemsen R. A fragile balance: FMR1 expression levels. Hum Mol Genet 2003;15:R249-R257. (Pubitemid 37259339)
48. Ozgur O, Oktay K. The Ovary-anatomy and function throughout human life. Ann N Y Acad Sci 2008;1127:1-9. (Pubitemid 351563102)
49. Perlhoff WH, Schneeberg NG. The premature climacterium. Am Pract 1957;8:1950.
50. Pietrobono R, Pomponi MG, Tabolacci E, Oostra B, Chiurazzi P, Neri G. Quantitative analysis of DNA demethylation and transcriptional reactivation of the FMR1 gene in fragile X cells treated with 5-azadeoxycytidine. Nucl Acids Res 2002;14:3278-3285. (Pubitemid 34846192)
51. Powell CM, Taggart RT, Drumheller TC, Wangsa D, Qian C, Nelson LM, White BJ. Molecular and cytogenetic studies of an X; autosome translocation in a patient with premature ovarian failure and review of the literature. Am J Med Genet 1994;52:19-26. (Pubitemid 24237325)
52. Primerano B, Tassone F, Hagerman RJ, Hagerman P, Amaldi F, Bagni C. Reduced FMR1 mRNA translation efficiency in fragile X patients with premutations. RNA 2002;8:1482-1488. (Pubitemid 36009019)
53. Prueitt RL, Ross JL, Zinn AR. Physical mapping of nine Xq translocation breakpoints and identification of XPNPEP2 as a premature ovarian failure gene. Cytogenet Cell Genet 2000;89:44-50. (Pubitemid 30435255)
54. Rao L, Babu A, Padmalatha V, Kanakavalli M, Deenadayal M, Singh L. Novel X-chromosomal defect associated with abnormal ovarian function. J Obstet Gyn Res 2005;1:12-15. (Pubitemid 40364140)
55. Rife M, Nadal A, Mila M, Willemsen R. Immunohistochemical FMRP studies in a full mutated female fetus. Am J Med Genet 2004;124A:129-132. (Pubitemid 38036584)
56. Rizzolio F, Bione S, Sala C, Goegan M, Gentile M, Gregato G, Rossi E, Pramparo T, Zuffardi O, Toniolo D. Chromosomal rearrangements in Xq and premature ovarian failure: mapping of 25 new cases and review of the literature. Hum Reprod 2006;21:1477-1483. (Pubitemid 44445025)
57. Sala C, Arrigo G, Torri G, Martinazzi F, Riva P, Larizza L, Philippe C, Jonveaux P, Sloan F, Labella T et al. Eleven X chromosome breakpoints assosiated with premature ovarian failure (POF) map to a 15-Mb YAG contig spanning Xq21. Genomics 1997;40:123-131. (Pubitemid 27108256)
58. Sang HY, Young MC, Min AH, Byung MK, Jin JK, Eung GM, Jung GK, Shin YM. X chromosome inactivation patterns in patients with idiopathic premature ovarian failure. Hum Reprod 2008;3:688-692.
59. Schaeffer C, Baroni B, Mandel JL, Ehresmann B, Ehresmann C, Moine J. The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO 2001;17:4803-4813. (Pubitemid 32848632)
60. Schaeffer C, Beaulande M, Ehresmann C, Ehresmann B, Moine H. The RNA binding protein FMRP: new connections and missing links. Biol Cell 2003;95:221-228. (Pubitemid 36889223)
61. Schlessinger D, Herrera L, Crisponi L, Mumm S, Percesepe A, Pellegrini M, Pilia G, Forabosco A. Genes and translocations involved in POF. Am J Med Genet 2002;111:328-333. (Pubitemid 34815460)
62. Sherman SL. Premature ovarian failure in the fragile X syndrome. Am J Med Genet 2000;97:189-194. (Pubitemid 32059206)
63. Southern EM. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 1975;98:503-517.
64. Stoyanova V, Oostra BA. Trinucleotide repeat protocols. Methods Mol Biol 2004;277:173-184.
65. Streuli I, Fraisse T, Ivecheole V, Moix I, Morris MA, de Ziegler D. Intermediate and premutation FMR1 alleles in women with occult primary ovarian insufficiency. Fertil Steril 2009;2:464-470.
66. Sullivan AK, Marcus M, Epstein MP, Allen EC, Anido AE, Paquin JJ, Yadav-Shah M, Sherman SL. Association of FMR1 repeat size with ovarian dysfunction. Hum Reprod 2005;2:402-412. (Pubitemid 40277608)
67. Tarleton J, Kenneson A, Taylor AK, Crandall K, Fletcher R, Casey R, Hart PS, Fisch G, Warren ST. A single base alteration in the CGG repeat region of FMR1: possible effects on gene expression and phenotype. J Med Genet 2002;39:196-200. (Pubitemid 34252558)
68. Tassone F, Hagerman PJ. Expression of the FMR1 gene. Cytogenet Gen Res 2003;100:124-128. (Pubitemid 37467798)
69. Tassone F, Longshore J, Zunich J, Steinbach P, Salat U, Taylor AK. Tissue-specific methylation differences in a fragile X premutation carrier. Clin Genet 1999;55:346-351. (Pubitemid 29295328)
70. Tassone F, Hagerman RJ, Taylor AK, Gane LW, Godfrey TE, Hagerman PJ. Elevated levels of FMR1 mRNA in carrier males: a new mechanism of involvement in the fragile-X syndrome. Am J Hum Genet 2000a; 66:6-15. (Pubitemid 30481464)
71. Tassone F, Hagerman RJ, Taylor AK, Mills JB, Harris SW, Gane LW, Hagerman PJ. Clinical involvement and protein expression in individuals with the FMR1 premutation. Am J Med Genet 2000b; 91:144-152. (Pubitemid 30133654)
72. Tassone F, Hagerman RJ, Chamberlain WD, Hagerman PJ. Transcription of the FMR1 gene in individuals with fragile X syndrome. Am J Med Genet 2000c;97:195-203. (Pubitemid 32059207)
73. Tassone F, Beilina A, Carosi C, Albertosi S, Bagni C, Li L, Glover K, Bentley D, Hagerman PJ. Elevated FMR1 mRNA in premutation carriers is due to increased transcription. RNA 2007; 13:555-562. (Pubitemid 46506938)
74. Tejada MI, Garća-Alegŕa E, Bilbao A, Mart́nez-Bouzas C, Beristain E, Poch M, Ramos-Arroyo MA, López B, Fernandez Carvajal I, Ribate MP et al. Analysis of the molecular parameters that could predict the risk of manifesting premature ovarian failure in female premutation carriers of fragile X syndrome. Menopause 2008; 15:945-949.
75. Till SM. The developmental roles of FMRP. Biochem Soc Trans 2010; 38:507-510.
76. Toniolo D, Rizzolio F. X chromosome and ovarian failure. Curr Opin Genet Dev 2006;16:293-300.
77. Van Asselt KM, Kok HS, Putter H, Wijmenga C, Peeters PH, Van der Schouw YT, Grobbee DE, te Velde ER, Mosselman S, Pearson PL. Linkage analysis of extremely discordant and concordant sibling pairs identifies quantitative trait loci influencing variation in human menopausal age. Am J Hum Genet 2004;74:444-453. (Pubitemid 38325915)
78. Vegetti W, Grazia-Tibletti M, Testa G, de Lauretis Y, Alanga F, Castoldi E, Tabolerelli M, Motta T, Bolis PF, Dalpra L et al. Inheritance in idiopathic premature ovarian failure: analysis of 71 cases. Hum Reprod 1998; 13:1796-1800.
79. Welt CK. Primary ovarian insufficiency: a more accurate term for premature ovarian failure. Clin Endocr 2008;68:499-509. (Pubitemid 351388699)
80. Wilcoxon F. Individual comparisons by ranking methods. Biometrics Bull 1945;1:80-83.
81. Wittenberger MD, Hagerman RJ, Sherman S, McConkie-Rosell A, Wlt CK, Rebar RW, Corrigan EC, Simpson JL, Nelson LM. The FMR1 premutation and reproduction. Fertil Steril 2007;3:456-465. (Pubitemid 46394554)
82. Zinn AR, Tonk VS, Chen Z. Evidence for a Turner Syndrome locus or loci at Xp11.2-p22.1. Am J Hum Genet 1998;63:1757-1766. (Pubitemid 30415739)