Inactivation of the Celf1 Gene that Encodes an RNA-Binding Protein Delays the First Wave of Spermatogenesis in Mice

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Cibois, Marie ^a,b,c   Boulanger, Gaella ^a,b   Audic, Yann ^a,b   Paillard, Luc ^a,b   Gautier Courteille, Carole ^a,b  

^a UNIVERSITÉ DE RENNES 1   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

RNA BINDING PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELF1 GENE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CONTROLLED STUDY; GENE; GENE DISRUPTION; GENE INACTIVATION; GERM CELL; LEYDIG CELL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREPUBERTY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPERMATOGENESIS; STEROIDOGENESIS; TESTIS;

ANIMALS; GENE EXPRESSION PROFILING; GENE SILENCING; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; RNA-BINDING PROTEINS; SPERMATOGENESIS;

MAMMALIA; MUS;

EID: 84866991953     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046337     Document Type: Article

References (37)

1. Russell L, Ettlin R, SinhaHikim A, Clegg E (1990) Histological and histopathological evaluation of the testis. St Louis: Cache River Press.
2. Yan W, (2009) Male infertility caused by spermiogenic defects: lessons from gene knockouts. Mol Cell Endocrinol 306: 24-32.
3. Chalmel F, Rolland AD, Niederhauser-Wiederkehr C, Chung SS, Demougin P, et al. (2007) The conserved transcriptome in human and rodent male gametogenesis. Proc Natl Acad Sci U S A 104: 8346-8351.
4. Itman C, Mendis S, Barakat B, Loveland KL, (2006) All in the family: TGF-beta family action in testis development. Reproduction 132: 233-246.
5. Shima JE, McLean DJ, McCarrey JR, Griswold MD, (2004) The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod 71: 319-330.
6. Schultz N, Hamra FK, Garbers DL, (2003) A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc Natl Acad Sci U S A 100: 12201-12206.
7. Lalancette C, Platts AE, Lu Y, Lu S, Krawetz SA, (2008) Computational identification of transcription frameworks of early committed spermatogenic cells. Mol Genet Genomics 280: 263-274.
8. Paronetto MP, Sette C, (2009) Role of RNA-binding proteins in mammalian spermatogenesis. Int J Androl 33: 2-12.
9. Grosso AR, Gomes AQ, Barbosa-Morais NL, Caldeira S, Thorne NP, et al. (2008) Tissue-specific splicing factor gene expression signatures. Nucleic Acids Res 36: 4823-4832.
10. Yeo G, Holste D, Kreiman G, Burge CB, (2004) Variation in alternative splicing across human tissues. Genome Biol 5: R74.
11. Iguchi N, Tobias JW, Hecht NB, (2006) Expression profiling reveals meiotic male germ cell mRNAs that are translationally up- and down-regulated. Proc Natl Acad Sci U S A 103: 7712-7717.
12. Barreau C, Paillard L, Mereau A, Osborne HB, (2006) Mammalian CELF/Bruno-like RNA-binding proteins: molecular characteristics and biological functions. Biochimie 88: 515-525.
13. Vlasova IA, Tahoe NM, Fan D, Larsson O, Rattenbacher B, et al. (2008) Conserved GU-Rich Elements Mediate mRNA Decay by Binding to CUG-Binding Protein 1. Mol Cell 29: 263-270.
14. Dasgupta T, Ladd AN, (2012) The importance of CELF control: molecular and biological roles of the CUG-BP, Elav-like family of RNA-binding proteins. Wiley Interdiscip Rev RNA 3: 104-121.
15. Gautier-Courteille C, Le Clainche C, Barreau C, Audic Y, Graindorge A, et al. (2004) EDEN-BP-dependent post-transcriptional regulation of gene expression in Xenopus somitic segmentation. Development 131: 6107-6117.
16. Ezzeddine N, Paillard L, Capri M, Maniey D, Bassez T, et al. (2002) EDEN dependent translational repression of maternal mRNAs is conserved between Xenopus and Drosophila. Proc Natl Acad Sci U S A 99: 257-262.
17. Cibois M, Gautier-Courteille C, Vallee A, Paillard L, (2010) A strategy to analyze the phenotypic consequences of inhibiting the association of an RNA-binding protein with a specific RNA. Rna 16: 10-15.
18. Kress C, Gautier-Courteille C, Osborne HB, Babinet C, Paillard L, (2007) Inactivation of CUG-BP1/CELF1 causes growth, viability, and spermatogenesis defects in mice. Mol Cell Biol 27: 1146-1157.
19. de Rooij DG, Russell LD, (2000) All you wanted to know about spermatogonia but were afraid to ask. J Androl 21: 776-798.
20. Xiao X, Zuo X, Davis AA, McMillan DR, Curry BB, et al. (1999) HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. Embo J 18: 5943-5952.
21. Sofikitis N, Giotitsas N, Tsounapi P, Baltogiannis D, Giannakis D, et al. (2008) Hormonal regulation of spermatogenesis and spermiogenesis. J Steroid Biochem Mol Biol 109: 323-330.
22. O'Shaughnessy PJ, Willerton L, Baker PJ, (2002) Changes in Leydig cell gene expression during development in the mouse. Biol Reprod 66: 966-975.
23. Ibanez L, de Zegher F, (2006) Puberty and prenatal growth. Mol Cell Endocrinol 254-255: 22-25.
24. Chandrashekar V, Zaczek D, Bartke A, (2004) The consequences of altered somatotropic system on reproduction. Biol Reprod 71: 17-27.
25. Sorensen K, Aksglaede L, Petersen JH, Leffers H, Juul A, (2010) The exon 3 deleted growth hormone receptor gene is associated with small birth size and early pubertal onset in healthy boys. J Clin Endocrinol Metab 95: 2819-2826.
26. Keene DE, Suescun MO, Bostwick MG, Chandrashekar V, Bartke A, et al. (2002) Puberty is delayed in male growth hormone receptor gene-disrupted mice. J Androl 23: 661-668.
27. Kanzaki M, Morris PL, (1999) Growth hormone regulates steroidogenic acute regulatory protein expression and steroidogenesis in Leydig cell progenitors. Endocrinology 140: 1681-1686.
28. Wang GM, O'Shaughnessy PJ, Chubb C, Robaire B, Hardy MP, (2003) Effects of insulin-like growth factor I on steroidogenic enzyme expression levels in mouse leydig cells. Endocrinology 144: 5058-5064.
29. Lukk M, Kapushesky M, Nikkilä J, Parkinson H, Goncalves A, et al. (2010) A global map of human gene expression. Nature Biotech 28: 322-4.
30. Zhang FP, Poutanen M, Wilbertz J, Huhtaniemi I, (2001) Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Mol Endocrinol 15: 172-183.
31. Zhang FP, Pakarainen T, Zhu F, Poutanen M, Huhtaniemi I, (2004) Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice. Endocrinology 145: 1453-1463.
32. Xu Q, Lin HY, Yeh SD, Yu IC, Wang RS, et al. (2007) Infertility with defective spermatogenesis and steroidogenesis in male mice lacking androgen receptor in Leydig cells. Endocrine 32: 96-106.
33. Rodriguez I, Ody C, Araki K, Garcia I, Vassalli P, (1997) An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. Embo J 16: 2262-2270.
34. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
35. Lu JY, Sadri N, Schneider RJ, (2006) Endotoxic shock in AUF1 knockout mice mediated by failure to degrade proinflammatory cytokine mRNAs. Genes Dev 20: 3174-3184.
36. Hecht NB, (1998) Molecular mechanisms of male germ cell differentiation. Bioessays 20: 555-561.
37. Eacker SM, Agrawal N, Qian K, Dichek HL, Gong EY, et al. (2008) Hormonal regulation of testicular steroid and cholesterol homeostasis. Mol Endocrinol 22: 623-635.