The RNA-binding protein ELAVL1/HuR is essential for mouse spermatogenesis, acting both at meiotic and postmeiotic stages

Molecular Biology of the Cell

Volumn 22, Issue 16, 2011, Pages 2875-2885

  Chi, Mai Nguyen ^a   Auriol, Jacques ^a   Jégou, Bernard ^b   Kontoyiannis, Dimitris L ^c   Turner, James M A ^d   De Rooij, Dirk G ^e   Morello, Dominique ^a  

^a Institut d'Exploration Fonctionnelle des Genomes   (France)

^b INSERM   (France)

^c BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^e UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 70; HUR PROTEIN; MESSENGER RNA; RNA BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; GAMETOGENESIS; GENE DELETION; GENE OVEREXPRESSION; GENE TARGETING; GERM CELL; LOSS OF FUNCTION MUTATION; MEIOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SPERMATOCYTE; SPERMATOGENESIS; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

ANIMALS; ANTIGENS, SURFACE; CELL CYCLE CHECKPOINTS; CELL DIFFERENTIATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; HSP70 HEAT-SHOCK PROTEINS; INFERTILITY, MALE; MALE; MEIOSIS; MICE; MICE, TRANSGENIC; RNA-BINDING PROTEINS; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS; TESTIS;

MUS;

EID: 80051693551     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-03-0212     Document Type: Article

References (42)

1. Bevilacqua A, Ceriani MC, Capaccioli S, Nicolin A (2003). Post-transcriptional regulation of gene expression by degradation of messenger RNAs. J Cell Physiol 195, 356-372. (Pubitemid 36529864)
2. de Boer J et al. (2003). Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur J Immunol 33, 314-325. (Pubitemid 36267595)
3. Deng W, Lin H (2002). miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2, 819-830. (Pubitemid 34650077)
4. Dix DJ, Allen JW, Collins BW, Mori C, Nakamura N, Poorman-Allen P, Goulding EH, Eddy EM (1996). Targeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility. Proc Natl Acad Sci USA 93, 3264-3268. (Pubitemid 26125606)
5. Dix DJ, Allen JW, Collins BW, Poorman-Allen P, Mori C, Blizard DR, Brown PR, Goulding EH, Strong BD, Eddy EM (1997). HSP70-2 is required for desynapsis of synaptonemal complexes during meiotic prophase in juvenile and adult mouse spermatocytes. Development 124, 4595-4603. (Pubitemid 27519254)
6. Eddy EM (1999). Role of heat shock protein HSP70-2 in spermatogenesis. Rev Reprod 4, 23-30.
7. Galban S et al. (2008). RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1alpha. Mol Cell Biol 28, 93-107.
8. Gallardo T, Shirley L, John GB, Castrillon DH (2007). Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre. Genesis 45, 413-417. (Pubitemid 47015328)
9. Ghosh M, Aguila HL, Michaud J, Ai Y, Wu MT, Hemmes A, Ristimaki A, Guo C, Furneaux H, Hla T (2009). Essential role of the RNA-binding protein HuR in progenitor cell survival in mice. J Clin Invest 119, 3530-3543.
10. Gouble A, Grazide S, Meggetto F, Mercier P, Delsol G, Morello D (2002). A new player in oncogenesis: AUF1/hnRNPD overexpression leads to tumorigenesis in transgenic mice. Cancer Res 62, 1489-1495. (Pubitemid 34407812)
11. Govin J, Caron C, Escoffier E, Ferro M, Kuhn L, Rousseaux S, Eddy EM, Garin J, Khochbin S (2006). Post-meiotic shifts in HSPA2/HSP70.2 chaperone activity during mouse spermatogenesis. J Biol Chem 281, 37888-37892. (Pubitemid 46042092)
12. Grivna ST, Pyhtila B, Lin H (2006). MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci USA 103, 13415-13420. (Pubitemid 44380122)
13. Honke K et al. (2002). Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc Natl Acad Sci USA 99, 4227-4232. (Pubitemid 34285968)
14. 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 USA 103, 7712-7717.
15. Katsanou V, Milatos S, Yiakouvaki A, Sgantzis N, Kotsoni A, Alexiou M, Harokopos V, Aidinis V, Hemberger M, Kontoyiannis DL (2009). The RNA-binding protein Elavl1/HuR is essential for placental branching morphogenesis and embryonic development. Mol Cell Biol 29, 2762-2776.
16. Katsanou V, Papadaki O, Milatos S, Blackshear PJ, Anderson P, Kollias G, Kontoyiannis DL (2005). HuR as a negative posttranscriptional modulator in inflammation. Mol Cell 19, 777-789. (Pubitemid 41316672)
17. Kawamata M, Nishimori K (2006). Mice deficient in Dmrt7 show infertility with spermatogenic arrest at pachytene stage. FEBS Lett 580, 6442-6446. (Pubitemid 44750942)
18. Kimmins S, Sassone-Corsi P (2005). Chromatin remodelling and epigenetic features of germ cells. Nature 434, 583-589. (Pubitemid 40488544)
19. Kotaja N, Bhattacharyya SN, Jaskiewicz L, Kimmins S, Parvinen M, Filipowicz W, Sassone-Corsi P (2006). The chromatoid body of male germ cells: similarity with processing bodies and presence of Dicer and microRNA pathway components. Proc Natl Acad Sci USA 103, 2647-2652.
20. Kotaja N, Kimmins S, Brancorsini S, Hentsch D, Vonesch JL, Davidson I, Parvinen M, Sassone-Corsi P (2004). Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis. Nat Methods 1, 249-254.
21. 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. (Pubitemid 46174574)
22. Kuznetsov S et al. (2007). RAD51C deficiency in mice results in early prophase I arrest in males and sister chromatid separation at metaphase II in females. J Cell Biol 176, 581-592. (Pubitemid 46333974)
23. Lammers JH, Offenberg HH, van Aalderen M, Vink AC, Dietrich AJ, Heyting C (1994). The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol Cell Biol 14, 1137-1146. (Pubitemid 24036564)
24. Levadoux-Martin M, Gouble A, Jegou B, Vallet-Erdtmann V, Auriol J, Mercier P, Morello D (2003). Impaired gametogenesis in mice that overexpress the RNA-binding protein HuR. EMBO Rep 4, 394-399. (Pubitemid 36622005)
25. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P, Wolgemuth DJ (1998). Cyclin A1 is required for meiosis in the male mouse. Nat Genet 20, 377-380. (Pubitemid 28541638)
26. Lopez de Silanes I, Zhan M, Lal A, Yang X, Gorospe M (2004). Identification of a target RNA motif for RNA-binding protein HuR. Proc Natl Acad Sci USA 101, 2987-2992. (Pubitemid 38327723)
27. Ma WJ, Cheng S, Campbell C, Wright A, Furneaux H (1996). Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J Biol Chem 5, 8144-8151. (Pubitemid 26108641)
28. Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, Blanco-Rodriguez J, Jasin M, Keeney S, Bonner WM, Burgoyne PS (2001). Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27, 271-276. (Pubitemid 32201847)
29. Matzuk MM, Lamb DJ (2008). The biology of infertility: research advances and clinical challenges. Nat Med 14, 1197-1213.
30. Mukherjee N, Lager PJ, Friedersdorf MB, Thompson MA, Keene JD (2009). Coordinated posttranscriptional mRNA population dynamics during T-cell activation. Mol Syst Biol 5, 288.
31. Myer VE, Fan XC, Steitz JA (1997). Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J 16, 2130-2139. (Pubitemid 27170973)
32. Nguyen Chi M, Chalmel F, Agius E, Vanzo N, Khabar KS, Jegou B, Morello D (2009). Temporally regulated traffic of HuR and its associated ARE-containing mRNAs from the chromatoid body to polysomes during mouse spermatogenesis. PLoS One 4, e4900.
33. Nickerson HD, Joshi A, Wolgemuth DJ (2007). Cyclin A1-deficient mice lack histone H3 serine 10 phosphorylation and exhibit altered aurora B dynamics in late prophase of male meiosis. Dev Biol 306, 725-735. (Pubitemid 46873547)
34. Parvinen M (2005). The chromatoid body in spermatogenesis. Int J Androl 28, 189-201.
35. Quenet D, Mark M, Govin J, van Dorsselear A, Schreiber V, Khochbin S, Dantzer F (2009). Parp2 is required for the differentiation of post-meiotic germ cells: identification of a spermatid-specific complex containing Parp1, Parp2, TP2 and HSPA2. Exp Cell Res 315, 2824-2834.
36. Steger K (1999). Transcriptional and translational regulation of gene expression in haploid spermatids. Anat Embryol (Berl) 199, 471-487.
37. Steger K (2001). Haploid spermatids exhibit translationally repressed mRNAs. Anat Embryol (Berl) 203, 323-334.
38. Tsai-Morris CH, Sheng Y, Lee E, Lei KJ, Dufau ML (2004). Gonadotropin-regulated testicular RNA helicase (GRTH/Ddx25) is essential for spermatid development and completion of spermatogenesis. Proc Natl Acad Sci USA 101, 6373-6378. (Pubitemid 38585981)
39. Turner JM, Burgoyne PS, Singh PB (2001). M31 and macroH2A1.2 colocalise at the pseudoautosomal region during mouse meiosis. J Cell Sci 114, 3367-3375. (Pubitemid 32998912)
40. Vidal F, Sage J, Cuzin F, Rassoulzadegan M (1998). Cre expression in primary spermatocytes: a tool for genetic engineering of the germ line. Mol Reprod Dev 51, 274-280. (Pubitemid 28445407)
41. Yang G, Zhang YL, Buchold GM, Jetten AM, O'Brien DA (2003). Analysis of germ cell nuclear factor transcripts and protein expression during spermatogenesis. Biol Reprod 68, 1620-1630. (Pubitemid 36519765)
42. Yang J, Medvedev S, Yu J, Tang LC, Agno JE, Matzuk MM, Schultz RM, Hecht NB (2005). Absence of the DNA-/RNA-binding protein MSY2 results in male and female infertility. Proc Natl Acad Sci USA 102, 5755-5760. (Pubitemid 40559632)