Expression of fragile X mental retardation protein and Fmr1 mRNA during folliculogenesis in the rat

Reproduction

Volumn 145, Issue 4, 2013, Pages 335-343

  Ferder, Ianina ^a   Parborell, Fernanda ^a   Sundblad, Victoria ^a   Chiauzzi, Violeta ^a   Gómez, Karina ^b   Charreau, Eduardo H ^a   Tesone, Marta ^a,c   Dain, Liliana ^a,d  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b INSTITUTO DE INVESTIGACIONES EN INGENIERÍA GENÉTICA Y BIOLOGÍA MOLECULAR   (Argentina)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^d Administracion Nacional de Laboratorios E Institutos de Salud Dr Carlos G Malbran   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CYTOPLASM; FEMALE; GERM CELL; GRANULOSA CELL; IMMUNOHISTOCHEMISTRY; NONHUMAN; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TESTIS; THECA CELL;

ANIMALS; FEMALE; FRAGILE X MENTAL RETARDATION PROTEIN; OVARIAN FOLLICLE; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 84877288365     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-12-0305     Document Type: Article

References (69)

1. Abramovich D, Rodriguez Celin A, Hernandez F, Tesone M & Parborell F 2009 Spatiotemporal analysis of the protein expression of angiogenic factors and their related receptors during folliculogenesis in rats with and without hormonal treatment. Reproduction 137 309-320. (doi:10.1530/REP-08-0130)
2. Allingham-Hawkins DJ, Babul-Hirji R, Chitayat D, Holden JJ, Yang KT, Lee C, Hudson R, Gorwill H, Nolin SL, Glicksman A et al. 1999 Fragile X premutation is a significant risk factor for premature ovarian failure: the International Collaborative POF in fragile X study - preliminary data. American Journal of Medical Genetics 83 322-325. (doi:10.1002/(SICI)1096-8628(19990402)83:4<322:: AID-AJMG17>3.0.CO;2-B)
3. Ashley CT, Sutcliffe JS, Kunst CB, Leiner HA, Eichler EE, Nelson DL & Warren ST 1993 Human and murine FMR-1: alternative splicing and translational initiation downstream of the CGG-repeat. Nature Genetics 4 244-251. (doi:10.1038/ng0793-244)
4. Bachner D, Manca A, Steinbach P, Wohrle D, Just W, Vogel W, Hameister H & Poustka A 1993 Enhanced expression of the murine FMR1 gene during germ cell proliferation suggests a special function in both the male and the female gonad. Human Molecular Genetics 2 2043-2050. (doi:10.1093/hmg/2.12.2043)
5. Bakker CE, de Diego Otero Y, Bontekoe C, Raghoe P, Luteijn T, Hoogeveen AT, Oostra BA & Willemsen R 2000 Immunocytochemical and biochemical characterization of FMRP, FXR1P, and FXR2P in the mouse. Experimental Cell Research 258 162-170. (doi:10.1006/excr. 2000.4932)
6. Bell MV, Hirst MC, Nakahori Y, MacKinnon RN, Roche A, Flint TJ, Jacobs PA, Tommerup N, Tranebjaerg L, Froster-Iskenius U et al. 1991 Physical mapping across the fragile X: hypermethylation and clinical expression of the fragile X syndrome. Cell 64 861-866. (doi:10.1016/0092-8674(91)90514-Y)
7. Billig H, Furuta I & Hsueh AJ 1993 Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology 133 2204-2212. (doi:10.1210/en.133.5.2204)
8. Blackwell E & Ceman S 2012 Arginine methylation of RNA-binding proteins regulates cell function and differentiation. Molecular Reproduction and Development 79 163-175. (doi:10.1002/mrd.22024)
9. Blackwell E, Zhang X & Ceman S 2010 Arginines of the RGG box regulate FMRP association with polyribosomes and mRNA. Human Molecular Genetics 19 1314-1323. (doi:10.1093/hmg/ddq007)
10. Brouwer JR, Mientjes EJ, Bakker CE, Nieuwenhuizen IM, Severijnen LA, Van der Linde HC, Nelson DL, Oostra BA & Willemsen R 2007 Elevated Fmr1 mRNA levels and reduced protein expression in a mouse model with an unmethylated fragile X full mutation. Experimental Cell Research 313 244-253. (doi:10.1016/j.yexcr.2006.10.002)
11. Brown V, Jin P, Ceman S, Darnell JC, O'Donnell WT, Tenenbaum SA, Jin X, Feng Y, Wilkinson KD, Keene JD et al. 2001 Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107 477-487. (doi:10.1016/S0092-8674 (01)00568-2)
12. Carletti MZ & Christenson LK 2009 MicroRNA in the ovary and female reproductive tract. Journal of Animal Science 87 E29-E38. (doi:10.2527/jas.2008- 1331)
13. Caudy AA, Myers M, Hannon GJ & Hammond SM 2002 Fragile X-related protein and VIG associate with the RNA interference machinery. Genes and Development 16 2491-2496. (doi:10.1101/gad.1025202)
14. Ceman S, Brown V & Warren ST 1999 Isolation of an FMRP-associated messenger ribonucleoprotein particle and identification of nucleolin and the fragile X-related proteins as components of the complex. Molecular and Cellular Biology 19 7925-7932.
15. Ceman S, Nelson R & Warren ST 2000 Identification of mouse YB1/p50 as a component of the FMRP-associated mRNP particle. Biochemical and Biophysical Research Communications 279 904-908. (doi:10.1006/bbrc.2000.4035)
16. Ceman S, O'Donnell WT, Reed M, Patton S, Pohl J & Warren ST 2003 Phosphorylation influences the translation state of FMRP-associated polyribosomes. Human Molecular Genetics 12 3295-3305. (doi:10.1093/hmg/ddg350)
17. Cheever A & Ceman S 2009 Phosphorylation of FMRP inhibits association with Dicer. RNA 15 362-366. (doi:10.1261/rna.1500809)
18. Christenson LK 2010 MicroRNA control of ovarian function. Animal Reproduction 7 129-133.
19. Chun SY, Eisenhauer KM, Minami S, Billig H, Perlas E & Hsueh AJ 1996 Hormonal regulation of apoptosis in early antral follicles: follicle-stimulating hormone as a major survival factor. Endocrinology 137 1447-1456. (doi:10.1210/en.137.4.1447)
20. Costa A, Wang Y, Dockendorff TC, Erdjument-Bromage H, Tempst P, Schedl P & Jongens TA 2005 The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway. Developmental Cell 8 331-342. (doi:10.1016/j.devcel.2005.01.011)
21. Darnell JC, Jensen KB, Jin P, Brown V, Warren ST & Darnell RB 2001 Fragile X mental retardation protein targetsG quartet mRNAs important for neuronal function. Cell 107 489-499. (doi:10.1016/S0092-8674(01)00566-9)
22. Denman RB 2002 Methylation of the arginine-glycine-rich region in the fragile X mental retardation protein FMRP differentially affects RNA binding. Cellular & Molecular Biology Letters 7 877-883.
23. Denman RB & Sung YJ 2002 Species-specific and isoform-specific RNA binding of human and mouse fragile X mental retardation proteins. Biochemical and Biophysical Research Communications 292 1063-1069. (doi:10.1006/bbrc.2002. 6768)
24. De Rubeis S & Bagni C 2010 Fragile X mental retardation protein control of neuronal mRNA metabolism: insights into mRNA stability. Molecular and Cellular Neurosciences 43 43-50. (doi:10.1016/j.mcn.2009.09.013)
25. De Rubeis S & Bagni C 2011 Regulation ofmolecular pathwaysinthe fragile X syndrome: insights into autism spectrum disorders. Journal of Neurodeve-lopmental Disorders 3 257-269. (doi:10.1007/s11689-011-9087-2)
26. Devys D, Lutz Y, Rouyer N, Bellocq JP & Mandel JL 1993 The FMR-1 protein is cytoplasmic, most abundant in neurons and appears normal in carriers of a fragile X premutation. Nature Genetics 4 335-340. (doi:10.1038/ng0893-335)
27. Didiot MC, Tian Z, Schaeffer C, Subramanian M, Mandel JL & Moine H 2008 The G-quartet containing FMRP binding site in FMR1 mRNA is a potent exonic splicing enhancer. Nucleic Acids Research 36 4902-4912. (doi:10.1093/nar/gkn472)
28. Dolzhanskaya N, Merz G, Aletta JM & Denman RB 2006 Methylation regulates the intracellular protein-protein and protein-RNA interactions of FMRP. Journal of Cell Science 119 1933-1946. (doi:10.1242/jcs.02882)
29. Eberhart DE, Malter HE, Feng Y & Warren ST 1996 The fragile X mental retardation protein is a ribonucleoprotein containing both nuclear localization and nuclear export signals. Human Molecular Genetics 5 1083-1091. (doi:10.1093/hmg/5.8.1083)
30. Eichler EE, Richards S, Gibbs RA & Nelson DL 1993 Fine structure of the human FMR1 gene. Human Molecular Genetics 2 1147-1153. (doi:10.1093/hmg/2.8. 1147)
31. Epstein AM, Bauer CR, Ho A, Bosco G & Zarnescu DC 2009 Drosophila fragile X protein controls cellular proliferation by regulating cbl levels in the ovary. Developmental Biology 330 83-92. (doi:10.1016/j.ydbio. 2009.03.011)
32. Feng Y, Gutekunst CA, Eberhart DE, Yi H, Warren ST & Hersch SM 1997 Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. Journal of Neuroscience 17 1539-1547.
33. Fiedler SD, Carletti MZ, Hong X & Christenson LK 2008 Hormonal regulation of MicroRNA expression in periovulatory mouse mural granulosa cells. Biology of Reproduction 79 1030-1037. (doi:10.1095/biolreprod.108.069690)
34. Flaws JA, Doerr JK, Sipes IG & Hoyer PB 1994 Destruction of preantral follicles in adult rats by 4-vinyl-1-cyclohexene diepoxide. Reproductive Toxicology 8 509-514. (doi:10.1016/0890-6238(94)90033-7)
35. Fu YH, Kuhl DP, Pizzuti A, Pieretti M, Sutcliffe JS, Richards S, Verkerk AJ, Holden JJ, Fenwick RG Jr, Warren ST et al. 1991 Variation of the CGG repeat at the fragile X site results in genetic instability: resolution of the Sherman paradox. Cell 67 1047-1058. (doi:10.1016/0092-8674(91)90283-5)
36. Garcia-Arocena D & Hagerman PJ 2010 Advances in understanding the molecular basis of FXTAS. Human Molecular Genetics 19 R83-R89. (doi:10.1093/hmg/ddq166)
37. Hirshfield AN 1991 Development of follicles in the mammalian ovary. International Review of Cytology 124 43-101.
38. Hirshfield AN & Midgley AR Jr 1978 Morphometric analysis of follicular development in the rat. Biology of Reproduction 19 597-605. (doi:10.1095/biolreprod19.3.597)
39. Hoffman GE, Le WW, Entezam A, Otsuka N, Tong ZB, Nelson L, Flaws JA, McDonald JH, Jafar S & Usdin K 2012 Ovarian abnormalities in a mouse model of fragile X primary ovarian insufficiency. Journal of Histochemistry and Cytochemistry 60 439-456. (doi:10.1369/0022155412441002)
40. Hvid H, Ekstrom CT, Vienberg S, Oleksiewicz MB & Klopfleisch R 2011 Identification of stable and oestrus cycle-independent housekeeping genes in the rat mammary gland and other tissues. Veterinary Journal 190 103-108. (doi:10.1016/j.tvjl.2010.09.002)
41. Ishizuka A, Siomi MC & Siomi H 2002 A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes and Development 16 2497-2508. (doi:10.1101/gad.1022002)
42. Jin P, Zarnescu DC, Ceman S, Nakamoto M, Mowrey J, Jongens TA, Nelson DL, Moses K & Warren ST 2004 Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nature Neuroscience 7 113-117. (doi:10.1038/nn1174)
43. Karakji EG & Tsang BK 1995 Follicular stage-dependent regulation of rat granulosa cell plasminogen activator system by transforming growth factor-α in vitro. Biology of Reproduction 52 411-418. (doi:10.1095/biolreprod52.2.411)
44. Khandjian EW, Bardoni B, Corbin F, Sittler A, Giroux S, Heitz D, Tremblay S, Pinset C, Montarras D, Rousseau F et al. 1998 Novel isoforms of the fragile X related protein FXR1Pare expressed during myogenesis. Human Molecular Genetics 7 2121-2128. (doi:10.1093/hmg/7.13.2121)
45. Laggerbauer B, Ostareck D, Keidel EM, Ostareck-Lederer A & Fischer U 2001 Evidence that fragile X mental retardation protein is a negative regulator of translation. Human Molecular Genetics 10 329-338. (doi:10.1093/hmg/10.4.329)
46. Li J, Kim JM, Liston P, Li M, Miyazaki T, Mackenzie AE, Korneluk RG & Tsang BK 1998 Expression of inhibitor of apoptosis proteins (IAPs) in rat granulosa cells during ovarian follicular development and atresia. Endocrinology 139 1321-1328. (doi:10.1210/en.139.3.1321)
47. Lu C, Lin L, Tan H, Wu H, Sherman SL, Gao F, Jin P & Chen D 2012 Fragile X premutationRNAissufficienttocause primary ovarian insufficiencyinmice. Human Molecular Genetics 21 5039-5047. (doi:10.1093/hmg/dds348)
48. Mazroui R, Huot ME, Tremblay S, Filion C, Labelle Y & Khandjian EW 2002 Trapping of messenger RNA by fragile X mental retardation protein into cytoplasmic granules induces translation repression. Human Molecular Genetics 11 3007-3017. (doi:10.1093/hmg/11.24.3007)
49. Megosh HB, Cox DN, Campbell C & Lin H 2006 The role of PIWI and the miRNA machinery in Drosophila germline determination. Current Biology 16 1884-1894. (doi:10.1016/j.cub.2006.08.051)
50. Oberle I, Rousseau F, Heitz D, Kretz C, Devys D, Hanauer A, Boue J, Bertheas M & Mandel J 1991 Instability of a 550-base pair DNA segment and abnormal methylation in fragile X syndrome. Science 252 1097-1102. (doi:10.1126/science.252.5009.1097)
51. O'Donnell WT & Warren ST 2002 A decade of molecular studies offragile X syndrome. Annual Review of Neuroscience 25 315-338. (doi:10.1146/annurev. neuro.25.112701.142909)
52. Parborell F, Pecci A, Gonzalez O, Vitale A & Tesone M 2002 Effects of a gonadotropin-releasing hormone agonist on rat ovarian follicle apoptosis: regulation by epidermal growth factor and the expression of Bcl-2-related genes. Biology of Reproduction 67 481-486. (doi:10. 1095/biolreprod67.2.481)
53. Rani CS, Nordenstrom K, Norjavaara E & Ahren K 1983 Development of catecholamine responsiveness in granulosa cells from preovulatory rat follicles - dependence on preovulatory luteinizing hormone surge. Biology of Reproduction 28 1021-1031. (doi:10.1095/biolreprod28.5.1021)
54. Rousseau F, Rouillard P, Morel ML, Khandjian EW & Morgan K 1995 Prevalence of carriers of premutation-size alleles of the FMRI gene - and implications for the population genetics of the fragile X syndrome. American Journal of Human Genetics 57 1006-1018.
55. Schaeffer C, Bardoni B, Mandel JL, Ehresmann B, Ehresmann C & Moine H 2001 The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO Journal 20 4803-4813. (doi:10.1093/emboj/20.17. 4803)
56. Schuettler J, Peng Z, Zimmer J, Sinn P, von Hagens C, Strowitzki T & Vogt PH 2011 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 26 1241-1251. (doi:10.1093/humrep/der018)
57. Sherman SL 2000 Premature ovarian failure in the fragile X syndrome. American Journal of Medical Genetics 97 189-194. (doi:10.1002/1096-8628(200023) 97:3<189::AID-AJMG1036>3.0.CO;2-J)
58. Siomi MC, Higashijima K, Ishizuka A & Siomi H 2002 Casein kinase II phosphorylates the fragile X mental retardation protein and modulates its biological properties. Molecular and Cellular Biology 22 8438-8447. (doi:10.1128/MCB.22.24.8438-8447.2002)
59. Sittler A, Devys D, Weber C & Mandel JL 1996 Alternative splicing ofexon 14 determines nuclear or cytoplasmic localisation of fmr1 protein isoforms. Human Molecular Genetics 5 95-102. (doi:10.1093/hmg/5.1.95)
60. Stetler A, Winograd C, Sayegh J, Cheever A, Patton E, Zhang X, Clarke S & Ceman S 2006 Identification and characterization of the methyl arginines in the fragile X mental retardation protein Fmrp. Human Molecular Genetics 15 87-96. (doi:10.1093/hmg/ddi429)
61. Tamanini F, Meijer N, Verheij C, Willems PJ, Galjaard H, Oostra BA & Hoogeveen AT 1996 FMRP is associated to the ribosomes via RNA. Human Molecular Genetics 5 809-813. (doi:10.1093/hmg/5.6.809)
62. Tamanini F, Willemsen R, van Unen L, Bontekoe C, Galjaard H, Oostra BA & Hoogeveen AT 1997 Differential expression of FMR1, FXR1 and FXR2 proteins in human brain and testis. Human Molecular Genetics 6 1315-1322. (doi:10.1093/hmg/6.8.1315)
63. Tassone F, Hagerman RJ, Taylor AK, Gane LW, Godfrey TE & Hagerman PJ 2000 Elevated levels of FMR1 mRNA in carrier males: a new mechanism of involvement in the fragile-X syndrome. American Journal of Human Genetics 66 6-15. (doi:10.1086/302720)
64. Tassone F, Beilina A, Carosi C, Albertosi S, Bagni C, Li L, Glover K, Bentley D & Hagerman PJ 2007 Elevated FMR1 mRNA in premutation carriers is due to increased transcription. RNA 13 555-562. (doi:10.1261/rna.280807)
65. Todd PK, Malter JS & Mack KJ 2003 Whisker stimulation-dependent translation of FMRP in the barrel cortex requires activation of type I metabotropic glutamate receptors. Brain Research. Molecular Brain Research 110 267-278. (doi:10.1016/S0169-328X(02)00657-5)
66. Verkerk AJ, de Graaff E, De Boulle K, Eichler EE, Konecki DS, Reyniers E, Manca A, Poustka A, Willems PJ, Nelson DL et al. 1993 Alternative splicing in the fragile X gene FMR1. Human Molecular Genetics 2 399-404. (doi:10.1093/hmg/2.4.399)
67. Willemsen R, Levenga J & Oostra BA 2011 CGG repeat in the FMR1 gene: size matters. Clinical Genetics 80 214-225. (doi:10.1111/j.1399-0004. 2011.01723.x)
68. Yang L, Duan R, Chen D, Wang J & Jin P 2007 Fragile X mental retardation protein modulates the fate of germline stem cells in Drosophila. Human Molecular Genetics 16 1814-1820. (doi:10.1093/hmg/ddm129)
69. Zhang CP, Yang JL, Zhang J, Li L, Huang L, Ji SY, Hu ZY, Gao F & Liu YX 2011 Notch signaling is involved in ovarian follicle development by regulating granulosa cell proliferation. Endocrinology 152 2437-2447. (doi:10.1210/en.2010-1182)