Advertisement

RNA Processing pp 123-151 | Cite as

Roles of RNA-binding Proteins and Post-transcriptional Regulation in Driving Male Germ Cell Development in the Mouse

  • Donny D. LicatalosiEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 907)

Abstract

Tissue development and homeostasis are dependent on highly regulated gene expression programs in which cell-specific combinations of regulatory factors determine which genes are expressed and the post-transcriptional fate of the resulting RNA transcripts. Post-transcriptional regulation of gene expression by RNA-binding proteins has critical roles in tissue development—allowing individual genes to generate multiple RNA and protein products, and the timing, location, and abundance of protein synthesis to be finely controlled. Extensive post-transcriptional regulation occurs during mammalian gametogenesis, including high levels of alternative mRNA expression, stage-specific expression of mRNA variants, broad translational repression, and stage-specific activation of mRNA translation. In this chapter, an overview of the roles of RNA-binding proteins and the importance of post-transcriptional regulation in male germ cell development in the mouse is presented.

Keywords

Post-transcriptional regulation Alternative mRNA processing Splicing Polyadenylation Translational control RNA-binding proteins Gametogenesis 

References

  1. 1.
    Cooper TA, Wan L, Dreyfuss G (2009) RNA and disease. Cell 136:777–793PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Nilsen TW, Graveley BR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463:457–463PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Kleene KC (2003) Patterns, mechanisms, and functions of translation regulation in mammalian spermatogenic cells. Cytogenet Genome Res 103:217–224PubMedGoogle Scholar
  4. 4.
    Ramskold D, Wang ET, Burge CB, Sandberg R (2009) An abundance of ubiquitously expressed genes revealed by tissue transcriptome sequence data. PLoS Comput Biol 5, e1000598PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Kleene KC (2001) A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mech Dev 106:3–23PubMedCrossRefGoogle Scholar
  6. 6.
    Kleene KC (2013) Connecting cis-elements and trans-factors with mechanisms of developmental regulation of mRNA translation in meiotic and haploid mammalian spermatogenic cells. Reproduction 146:R1–R19PubMedCrossRefGoogle Scholar
  7. 7.
    Cooke HJ, Saunders PT (2002) Mouse models of male infertility. Nat Rev Genet 3:790–801PubMedCrossRefGoogle Scholar
  8. 8.
    Jamsai D, O’Bryan MK (2011) Mouse models in male fertility research. Asian J Androl 13:139–151PubMedCrossRefGoogle Scholar
  9. 9.
    Rossi P, Dolci S (2013) Paracrine Mechanisms Involved in the Control of Early Stages of Mammalian Spermatogenesis. Front Endocrinol (Lausanne) 4:181Google Scholar
  10. 10.
    Ginsburg M, Snow MH, McLaren A (1990) Primordial germ cells in the mouse embryo during gastrulation. Development 110:521–528PubMedGoogle Scholar
  11. 11.
    McLaren A (2001) Mammalian germ cells: birth, sex, and immortality. Cell Struct Funct 26:119–122PubMedCrossRefGoogle Scholar
  12. 12.
    Nagano R, Tabata S, Nakanishi Y, Ohsako S, Kurohmaru M, Hayashi Y (2000) Reproliferation and relocation of mouse male germ cells (gonocytes) during prespermatogenesis. Anat Rec 258:210–220PubMedCrossRefGoogle Scholar
  13. 13.
    Kopera IA, Bilinska B, Cheng CY, Mruk DD (2010) Sertoli-germ cell junctions in the testis: a review of recent data. Philos Trans R Soc Lond B Biol Sci 365:1593–1605PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    de Rooij DG, Griswold MD (2012) Questions about spermatogonia posed and answered since 2000. J Androl 33:1085–1095PubMedCrossRefGoogle Scholar
  15. 15.
    Song HW, Wilkinson MF (2014) Transcriptional control of spermatogonial maintenance and differentiation. Semin Cell Dev Biol 30:14–26PubMedCrossRefGoogle Scholar
  16. 16.
    Yoshida S (2008) Spermatogenic stem cell system in the mouse testis. Cold Spring Harb Symp Quant Biol 73:25–32PubMedCrossRefGoogle Scholar
  17. 17.
    Youds JL, Boulton SJ (2011) The choice in meiosis—defining the factors that influence crossover or non-crossover formation. J Cell Sci 124:501–513PubMedCrossRefGoogle Scholar
  18. 18.
    Gupta SK, Bhandari B (2011) Acrosome reaction: relevance of zona pellucida glycoproteins. Asian J Androl 13:97–105PubMedCrossRefGoogle Scholar
  19. 19.
    Monesi V, Geremia R, D’Agostino A, Boitani C (1978) Biochemistry of male germ cell differentiation in mammals: RNA synthesis in meiotic and postmeiotic cells. Curr Top Dev Biol 12:11–36PubMedCrossRefGoogle Scholar
  20. 20.
    Kierszenbaum AL, Tres LL (1975) Structural and transcriptional features of the mouse spermatid genome. J Cell Biol 65:258–270PubMedCrossRefGoogle Scholar
  21. 21.
    Upadhyay RD, Kumar AV, Ganeshan M, Balasinor NH (2012) Tubulobulbar complex: cytoskeletal remodeling to release spermatozoa. Reprod Biol Endocrinol 10:27PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Gilbert W (1978) Why genes in pieces? Nature 271:501PubMedCrossRefGoogle Scholar
  23. 23.
    Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40:1413–1415PubMedCrossRefGoogle Scholar
  24. 24.
    Wang ET, Sandberg R, Luo S et al (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456:470–476PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Barbosa-Morais NL, Irimia M, Pan Q et al (2012) The evolutionary landscape of alternative splicing in vertebrate species. Science 338:1587–1593PubMedCrossRefGoogle Scholar
  26. 26.
    Merkin J, Russell C, Chen P, Burge CB (2012) Evolutionary dynamics of gene and isoform regulation in Mammalian tissues. Science 338:1593–1599PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Miura K, Fujibuchi W, Unno M (2012) Splice variants in apoptotic pathway. Exp Oncol 34:212–217PubMedGoogle Scholar
  28. 28.
    Zhang C, Frias MA, Mele A et al (2010) Integrative modeling defines the Nova splicing-regulatory network and its combinatorial controls. Science 329:439–443PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Ellis JD, Barrios-Rodiles M, Colak R et al (2012) Tissue-specific alternative splicing remodels protein-protein interaction networks. Mol Cell 46:884–892PubMedCrossRefGoogle Scholar
  30. 30.
    Buljan M, Chalancon G, Eustermann S et al (2012) Tissue-specific splicing of disordered segments that embed binding motifs rewires protein interaction networks. Mol Cell 46:871–883PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    McGlincy NJ, Smith CW (2008) Alternative splicing resulting in nonsense-mediated mRNA decay: what is the meaning of nonsense? Trends Biochem Sci 33:385–393PubMedCrossRefGoogle Scholar
  32. 32.
    Proudfoot NJ (2011) Ending the message: poly(A) signals then and now. Genes Dev 25:1770–1782PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Bentley DL (2014) Coupling mRNA processing with transcription in time and space. Nat Rev Genet 15:163–175PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Shi Y (2012) Alternative polyadenylation: new insights from global analyses. RNA 18:2105–2117PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Rouget C, Papin C, Boureux A et al (2010) Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 467:1128–1132PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Mayr C, Bartel DP (2009) Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138:673–684PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Sandberg R, Neilson JR, Sarma A, Sharp PA, Burge CB (2008) Proliferating cells express mRNAs with shortened 3′ untranslated regions and fewer microRNA target sites. Science 320:1643–1647PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Ghosh T, Soni K, Scaria V, Halimani M, Bhattacharjee C, Pillai B (2008) MicroRNA-mediated up-regulation of an alternatively polyadenylated variant of the mouse cytoplasmic {beta}-actin gene. Nucleic Acids Res 36:6318–6332PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Mignone F, Gissi C, Liuni S, Pesole G (2002) Untranslated regions of mRNAs. Genome Biol 3, REVIEWS0004PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Tian B, Hu J, Zhang H, Lutz CS (2005) A large-scale analysis of mRNA polyadenylation of human and mouse genes. Nucleic Acids Res 33:201–212PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Tian B, Manley JL (2013) Alternative cleavage and polyadenylation: the long and short of it. Trends Biochem Sci 38:312–320PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Flavell SW, Kim TK, Gray JM et al (2008) Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 60:1022–1038PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Zhang H, Lee JY, Tian B (2005) Biased alternative polyadenylation in human tissues. Genome Biol 6:R100PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Ji Z, Lee JY, Pan Z, Jiang B, Tian B (2009) Progressive lengthening of 3′ untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development. Proc Natl Acad Sci U S A 106:7028–7033PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Liu D, Brockman JM, Dass B et al (2007) Systematic variation in mRNA 3′-processing signals during mouse spermatogenesis. Nucleic Acids Res 35:234–246PubMedCrossRefGoogle Scholar
  46. 46.
    McMahon KW, Hirsch BA, MacDonald CC (2006) Differences in polyadenylation site choice between somatic and male germ cells. BMC Mol Biol 7:35PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Wang H, Sartini BL, Millette CF, Kilpatrick DL (2006) A developmental switch in transcription factor isoforms during spermatogenesis controlled by alternative messenger RNA 3′-end formation. Biol Reprod 75:318–323PubMedCrossRefGoogle Scholar
  48. 48.
    O’Brien DA, Welch JE, Fulcher KD, Eddy EM (1994) Expression of mannose 6-phosphate receptor messenger ribonucleic acids in mouse spermatogenic and Sertoli cells. Biol Reprod 50:429–435PubMedCrossRefGoogle Scholar
  49. 49.
    Shaper NL, Wright WW, Shaper JH (1990) Murine beta 1,4-galactosyltransferase: both the amounts and structure of the mRNA are regulated during spermatogenesis. Proc Natl Acad Sci U S A 87:791–795PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Yeo G, Holste D, Kreiman G, Burge CB (2004) Variation in alternative splicing across human tissues. Genome Biol 5:R74PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Clark TA, Schweitzer AC, Chen TX et al (2007) Discovery of tissue-specific exons using comprehensive human exon microarrays. Genome Biol 8:R64PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Grosso AR, Gomes AQ, Barbosa-Morais NL et al (2008) Tissue-specific splicing factor gene expression signatures. Nucleic Acids Res 36:4823–4832PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    de la Grange P, Gratadou L, Delord M, Dutertre M, Auboeuf D (2010) Splicing factor and exon profiling across human tissues. Nucleic Acids Res 38:2825–2838PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Soumillon M, Necsulea A, Weier M et al (2013) Cellular source and mechanisms of high transcriptome complexity in the mammalian testis. Cell Rep 3:2179–2190PubMedCrossRefGoogle Scholar
  55. 55.
    Mackey ZB, Ramos W, Levin DS, Walter CA, McCarrey JR, Tomkinson AE (1997) An alternative splicing event which occurs in mouse pachytene spermatocytes generates a form of DNA ligase III with distinct biochemical properties that may function in meiotic recombination. Mol Cell Biol 17:989–998PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Nash RA, Caldecott KW, Barnes DE, Lindahl T (1997) XRCC1 protein interacts with one of two distinct forms of DNA ligase III. Biochemistry 36:5207–5211PubMedCrossRefGoogle Scholar
  57. 57.
    Kanai Y, Kanai-Azuma M, Noce T et al (1996) Identification of two Sox17 messenger RNA isoforms, with and without the high mobility group box region, and their differential expression in mouse spermatogenesis. J Cell Biol 133:667–681PubMedCrossRefGoogle Scholar
  58. 58.
    Foulkes NS, Borrelli E, Sassone-Corsi P (1991) CREM gene: use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription. Cell 64:739–749PubMedCrossRefGoogle Scholar
  59. 59.
    Foulkes NS, Mellstrom B, Benusiglio E, Sassone-Corsi P (1992) Developmental switch of CREM function during spermatogenesis: from antagonist to activator. Nature 355:80–84PubMedCrossRefGoogle Scholar
  60. 60.
    Foulkes NS, Schlotter F, Pevet P, Sassone-Corsi P (1993) Pituitary hormone FSH directs the CREM functional switch during spermatogenesis. Nature 362:264–267PubMedCrossRefGoogle Scholar
  61. 61.
    Nantel F, Monaco L, Foulkes NS et al (1996) Spermiogenesis deficiency and germ-cell apoptosis in CREM-mutant mice. Nature 380:159–162PubMedCrossRefGoogle Scholar
  62. 62.
    Blendy JA, Kaestner KH, Weinbauer GF, Nieschlag E, Schutz G (1996) Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature 380:162–165PubMedCrossRefGoogle Scholar
  63. 63.
    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 68:1620–1630PubMedCrossRefGoogle Scholar
  64. 64.
    Groocock LM, Nie M, Prudden J et al (2014) RNF4 interacts with both SUMO and nucleosomes to promote the DNA damage response. EMBO Rep 15:601–608PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Pero R, Lembo F, Chieffi P et al (2003) Translational regulation of a novel testis-specific RNF4 transcript. Mol Reprod Dev 66:1–7PubMedCrossRefGoogle Scholar
  66. 66.
    Hsu LC, Chen HY, Lin YW et al (2008) DAZAP1, an hnRNP protein, is required for normal growth and spermatogenesis in mice. RNA 14:1814–1822PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Yang CK, Yen P (2013) Differential translation of Dazap1 transcripts during spermatogenesis. PLoS One 8, e60873PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Schmidt EE, Hanson ES, Capecchi MR (1999) Sequence-independent assembly of spermatid mRNAs into messenger ribonucleoprotein particles. Mol Cell Biol 19:3904–3915PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Cataldo L, Mastrangelo MA, Kleene KC (1999) A quantitative sucrose gradient analysis of the translational activity of 18 mRNA species in testes from adult mice. Mol Hum Reprod 5:206–213PubMedCrossRefGoogle Scholar
  70. 70.
    Gold B, Stern L, Bradley FM, Hecht NB (1983) Gene expression during mammalian spermatogenesis. II. Evidence for stage-specific differences in mRNA populations. J Exp Zool 225:123–134PubMedCrossRefGoogle Scholar
  71. 71.
    Stern L, Kleene KC, Gold B, Hecht NB (1983) Gene expression during mammalian spermatogenesis. III. Changes in populations of mRNA during spermiogenesis. Exp Cell Res 143:247–255PubMedCrossRefGoogle Scholar
  72. 72.
    Gold B, Hecht NB (1981) Differential compartmentalization of messenger ribonucleic acid in murine testis. Biochemistry 20:4871–4877PubMedCrossRefGoogle Scholar
  73. 73.
    Cagney G, Park S, Chung C et al (2005) Human tissue profiling with multidimensional protein identification technology. J Proteome Res 4:1757–1767PubMedCrossRefGoogle Scholar
  74. 74.
    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 71:319–330PubMedCrossRefGoogle Scholar
  75. 75.
    Chappell VA, Busada JT, Keiper BD, Geyer CB (2013) Translational activation of developmental messenger RNAs during neonatal mouse testis development. Biol Reprod 89:61PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    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 103:7712–7717PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Braun RE (1998) Post-transcriptional control of gene expression during spermatogenesis. Semin Cell Dev Biol 9:483–489PubMedCrossRefGoogle Scholar
  78. 78.
    Steger K (2001) Haploid spermatids exhibit translationally repressed mRNAs. Anat Embryol (Berl) 203:323–334CrossRefGoogle Scholar
  79. 79.
    Braun RE (2000) Temporal control of protein synthesis during spermatogenesis. Int J Androl 23(Suppl 2):92–94PubMedCrossRefGoogle Scholar
  80. 80.
    Hecht NB (1998) Molecular mechanisms of male germ cell differentiation. Bioessays 20:555–561PubMedCrossRefGoogle Scholar
  81. 81.
    Yu YE, Zhang Y, Unni E et al (2000) Abnormal spermatogenesis and reduced fertility in transition nuclear protein 1-deficient mice. Proc Natl Acad Sci U S A 97:4683–4688PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Zhao M, Shirley CR, Yu YE et al (2001) Targeted disruption of the transition protein 2 gene affects sperm chromatin structure and reduces fertility in mice. Mol Cell Biol 21:7243–7255PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Adham IM, Nayernia K, Burkhardt-Gottges E et al (2001) Teratozoospermia in mice lacking the transition protein 2 (Tnp2). Mol Hum Reprod 7:513–520PubMedCrossRefGoogle Scholar
  84. 84.
    Cho C, Willis WD, Goulding EH et al (2001) Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat Genet 28:82–86PubMedGoogle Scholar
  85. 85.
    Nayernia K, Adham IM, Burkhardt-Gottges E et al (2002) Asthenozoospermia in mice with targeted deletion of the sperm mitochondrion-associated cysteine-rich protein (Smcp) gene. Mol Cell Biol 22:3046–3052PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Kleene KC (1989) Poly(A) shortening accompanies the activation of translation of five mRNAs during spermiogenesis in the mouse. Development 106:367–373PubMedGoogle Scholar
  87. 87.
    Mali P, Kaipia A, Kangasniemi M et al (1989) Stage-specific expression of nucleoprotein mRNAs during rat and mouse spermiogenesis. Reprod Fertil Dev 1:369–382PubMedCrossRefGoogle Scholar
  88. 88.
    Kleene KC, Distel RJ, Hecht NB (1984) Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse. Dev Biol 105:71–79PubMedCrossRefGoogle Scholar
  89. 89.
    Shih DM, Kleene KC (1992) A study by in situ hybridization of the stage of appearance and disappearance of the transition protein 2 and the mitochondrial capsule seleno-protein mRNAs during spermatogenesis in the mouse. Mol Reprod Dev 33:222–227PubMedCrossRefGoogle Scholar
  90. 90.
    Lee K, Haugen HS, Clegg CH, Braun RE (1995) Premature translation of protamine 1 mRNA causes precocious nuclear condensation and arrests spermatid differentiation in mice. Proc Natl Acad Sci U S A 92:12451–12455PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Tseden K, Topaloglu O, Meinhardt A et al (2007) Premature translation of transition protein 2 mRNA causes sperm abnormalities and male infertility. Mol Reprod Dev 74:273–279PubMedCrossRefGoogle Scholar
  92. 92.
    Bagarova J, Chowdhury TA, Kimura M, Kleene KC (2010) Identification of elements in the Smcp 5′ and 3′ UTR that repress translation and promote the formation of heavy inactive mRNPs in spermatids by analysis of mutations in transgenic mice. Reproduction 140:853–864PubMedCrossRefGoogle Scholar
  93. 93.
    Hawthorne SK, Busanelli RR, Kleene KC (2006) The 5′ UTR and 3′ UTR of the sperm mitochondria-associated cysteine-rich protein mRNA regulate translation in spermatids by multiple mechanisms in transgenic mice. Dev Biol 297:118–126PubMedCrossRefGoogle Scholar
  94. 94.
    Fajardo MA, Haugen HS, Clegg CH, Braun RE (1997) Separate elements in the 3′ untranslated region of the mouse protamine 1 mRNA regulate translational repression and activation during murine spermatogenesis. Dev Biol 191:42–52PubMedCrossRefGoogle Scholar
  95. 95.
    Zhong J, Peters AH, Kafer K, Braun RE (2001) A highly conserved sequence essential for translational repression of the protamine 1 messenger rna in murine spermatids. Biol Reprod 64:1784–1789PubMedCrossRefGoogle Scholar
  96. 96.
    Giorgini F, Davies HG, Braun RE (2001) MSY2 and MSY4 bind a conserved sequence in the 3′ untranslated region of protamine 1 mRNA in vitro and in vivo. Mol Cell Biol 21:7010–7019PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Braun RE, Peschon JJ, Behringer RR, Brinster RL, Palmiter RD (1989) Protamine 3′-untranslated sequences regulate temporal translational control and subcellular localization of growth hormone in spermatids of transgenic mice. Genes Dev 3:793–802PubMedCrossRefGoogle Scholar
  98. 98.
    Nipper RW, Chennothukuzhi V, Tutuncu L, Williams CJ, Gerton GL, Moss SB (2005) Differential RNA expression and polyribosome loading of alternative transcripts of the Akap4 gene in murine spermatids. Mol Reprod Dev 70:397–405PubMedCrossRefGoogle Scholar
  99. 99.
    Schmidt EE, Schibler U (1997) Developmental testis-specific regulation of mRNA levels and mRNA translational efficiencies for TATA-binding protein mRNA isoforms. Dev Biol 184:138–149PubMedCrossRefGoogle Scholar
  100. 100.
    Gu W, Morales C, Hecht NB (1995) In male mouse germ cells, copper-zinc superoxide dismutase utilizes alternative promoters that produce multiple transcripts with different translation potential. J Biol Chem 270:236–243PubMedCrossRefGoogle Scholar
  101. 101.
    Weill L, Belloc E, Bava FA, Mendez R (2012) Translational control by changes in poly(A) tail length: recycling mRNAs. Nat Struct Mol Biol 19:577–585PubMedCrossRefGoogle Scholar
  102. 102.
    Eckmann CR, Rammelt C, Wahle E (2011) Control of poly(A) tail length. Wiley Interdiscip Rev RNA 2:348–361PubMedCrossRefGoogle Scholar
  103. 103.
    Doidge R, Mittal S, Aslam A, Winkler GS (2012) Deadenylation of cytoplasmic mRNA by the mammalian Ccr4-Not complex. Biochem Soc Trans 40:896–901PubMedCrossRefGoogle Scholar
  104. 104.
    Kashiwabara S, Noguchi J, Zhuang T et al (2002) Regulation of spermatogenesis by testis-specific, cytoplasmic poly(A) polymerase TPAP. Science 298:1999–2002PubMedCrossRefGoogle Scholar
  105. 105.
    Tay J, Richter JD (2001) Germ cell differentiation and synaptonemal complex formation are disrupted in CPEB knockout mice. Dev Cell 1:201–213PubMedCrossRefGoogle Scholar
  106. 106.
    Yanagiya A, Delbes G, Svitkin YV, Robaire B, Sonenberg N (2010) The poly(A)-binding protein partner Paip2a controls translation during late spermiogenesis in mice. J Clin Invest 120:3389–3400PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Gu W, Kwon YK, Hecht NB (1996) In postmeiotic male germ cells poly (A) shortening accompanies translation of mRNA encoding gamma enteric actin but not cytoplasmic beta and gamma actin mRNAs. Mol Reprod Dev 44:141–145PubMedCrossRefGoogle Scholar
  108. 108.
    Licatalosi DD, Darnell RB (2010) RNA processing and its regulation: global insights into biological networks. Nat Rev Genet 11:75–87PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Colwill K, Pawson T, Andrews B et al (1996) The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J 15:265–275PubMedPubMedCentralGoogle Scholar
  110. 110.
    Duncan PI, Stojdl DF, Marius RM, Bell JC (1997) In Vivo regulation of alternative pre-mRNA splicing by the Clk1 protein kinase. Mol Cell Biol 17:5996–6001PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Prasad J, Colwill K, Pawson T, Manley JL (1999) The protein kinase Clk/Sty directly modulates SR protein activity: both hyper- and hypophosphorylation inhibit splicing. Mol Cell Biol 19:6991–7000PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Howell BW, Afar DE, Lew J et al (1991) STY, a tyrosine-phosphorylating enzyme with sequence homology to serine/threonine kinases. Mol Cell Biol 11:568–572PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Nayler O, Stamm S, Ullrich A (1997) Characterization and comparison of four serine- and arginine-rich (SR) protein kinases. Biochem J 326:693–700PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Arkov AL, Ramos A (2010) Building RNA-protein granules: insight from the germline. Trends Cell Biol 20:482–490PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Kotaja N, Sassone-Corsi P (2007) The chromatoid body: a germ-cell-specific RNA-processing centre. Nat Rev Mol Cell Biol 8:85–90PubMedCrossRefGoogle Scholar
  116. 116.
    Putnam AA, Jankowsky E (1829) DEAD-box helicases as integrators of RNA, nucleotide and protein binding. Biochim Biophys Acta 2013:884–893Google Scholar
  117. 117.
    Kleene KC, Cullinane DL (2011) Maybe repressed mRNAs are not stored in the chromatoid body in mammalian spermatids. Reproduction 142:383–388PubMedCrossRefGoogle Scholar
  118. 118.
    Meikar O, Da Ros M, Korhonen H, Kotaja N (2011) Chromatoid body and small RNAs in male germ cells. Reproduction 142:195–209PubMedCrossRefGoogle Scholar
  119. 119.
    Pascale A, Govoni S (2012) The complex world of post-transcriptional mechanisms: is their deregulation a common link for diseases? Focus on ELAV-like RNA-binding proteins. Cell Mol Life Sci 69:501–517PubMedCrossRefGoogle Scholar
  120. 120.
    Ince-Dunn G, Okano HJ, Jensen KB et al (2012) Neuronal Elav-like (Hu) proteins regulate RNA splicing and abundance to control glutamate levels and neuronal excitability. Neuron 75:1067–1080PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Mukherjee N, Corcoran DL, Nusbaum JD et al (2011) Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell 43:327–339PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Lebedeva S, Jens M, Theil K et al (2011) Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell 43:340–352PubMedCrossRefGoogle Scholar
  123. 123.
    Chi MN, Auriol J, Jegou B et al (2011) The RNA-binding protein ELAVL1/HuR is essential for mouse spermatogenesis, acting both at meiotic and postmeiotic stages. Mol Biol Cell 22:2875–2885PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Vlasova-St Louis I, Dickson AM, Bohjanen PR, Wilusz CJ (1829) CELFish ways to modulate mRNA decay. Biochim Biophys Acta 2013:695–707Google Scholar
  125. 125.
    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 3:104–121PubMedCrossRefGoogle Scholar
  126. 126.
    Vlasova-St Louis I, Bohjanen PR (2011) Coordinate regulation of mRNA decay networks by GU-rich elements and CELF1. Curr Opin Genet Dev 21:444–451PubMedCrossRefGoogle Scholar
  127. 127.
    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 27:1146–1157PubMedCrossRefGoogle Scholar
  128. 128.
    Sanchez-Jimenez F, Sanchez-Margalet V (2013) Role of Sam68 in post-transcriptional gene regulation. Int J Mol Sci 14:23402–23419PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Iijima T, Wu K, Witte H et al (2011) SAM68 regulates neuronal activity-dependent alternative splicing of neurexin-1. Cell 147:1601–1614PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Missler M, Sudhof TC (1998) Neurexins: three genes and 1001 products. Trends Genet 14:20–26PubMedCrossRefGoogle Scholar
  131. 131.
    Ehrmann I, Dalgliesh C, Liu Y et al (2013) The tissue-specific RNA-binding protein T-STAR controls regional splicing patterns of neurexin pre-mRNAs in the brain. PLoS Genet 9, e1003474PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Paronetto MP, Zalfa F, Botti F, Geremia R, Bagni C, Sette C (2006) The nuclear RNA-binding protein Sam68 translocates to the cytoplasm and associates with the polysomes in mouse spermatocytes. Mol Biol Cell 17:14–24PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Paronetto MP, Messina V, Bianchi E et al (2009) Sam68 regulates translation of target mRNAs in male germ cells, necessary for mouse spermatogenesis. J Cell Biol 185:235–249PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Paronetto MP, Messina V, Barchi M, Geremia R, Richard S, Sette C (2011) Sam68 marks the transcriptionally active stages of spermatogenesis and modulates alternative splicing in male germ cells. Nucleic Acids Res 39:4961–4974PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Sawicka K, Bushell M, Spriggs KA, Willis AE (2008) Polypyrimidine-tract-binding protein: a multifunctional RNA-binding protein. Biochem Soc Trans 36:641–647PubMedCrossRefGoogle Scholar
  136. 136.
    Xu M, Hecht NB (2007) Polypyrimidine tract binding protein 2 stabilizes phosphoglycerate kinase 2 mRNA in murine male germ cells by binding to its 3′UTR. Biol Reprod 76:1025–1033PubMedCrossRefGoogle Scholar
  137. 137.
    Schmid R, Grellscheid SN, Ehrmann I et al (2013) The splicing landscape is globally reprogrammed during male meiosis. Nucleic Acids Res 41:10170–10184PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Licatalosi DD, Yano M, Fak JJ et al (2012) Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain. Genes Dev 26:1626–1642PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Wallace AM, Denison TL, Attaya EN, MacDonald CC (2004) Developmental distribution of the polyadenylation protein CstF-64 and the variant tauCstF-64 in mouse and rat testis. Biol Reprod 70:1080–1087PubMedCrossRefGoogle Scholar
  140. 140.
    Yao C, Choi EA, Weng L et al (2013) Overlapping and distinct functions of CstF64 and CstF64tau in mammalian mRNA 3′ processing. RNA 19:1781–1790PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Yao C, Biesinger J, Wan J et al (2012) Transcriptome-wide analyses of CstF64-RNA interactions in global regulation of mRNA alternative polyadenylation. Proc Natl Acad Sci U S A 109:18773–18778PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Martin G, Gruber AR, Keller W, Zavolan M (2012) Genome-wide analysis of pre-mRNA 3′ end processing reveals a decisive role of human cleavage factor I in the regulation of 3′ UTR length. Cell Rep 1:753–763PubMedCrossRefGoogle Scholar
  143. 143.
    Berkovits BD, Wang L, Guarnieri P, Wolgemuth DJ (2012) The testis-specific double bromodomain-containing protein BRDT forms a complex with multiple spliceosome components and is required for mRNA splicing and 3′-UTR truncation in round spermatids. Nucleic Acids Res 40:7162–7175PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Tardif S, Akrofi AS, Dass B, Hardy DM, MacDonald CC (2010) Infertility with impaired zona pellucida adhesion of spermatozoa from mice lacking TauCstF-64. Biol Reprod 83:464–472PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Dass B, Tardif S, Park JY et al (2007) Loss of polyadenylation protein tauCstF-64 causes spermatogenic defects and male infertility. Proc Natl Acad Sci U S A 104:20374–20379PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Giorgini F, Davies HG, Braun RE (2002) Translational repression by MSY4 inhibits spermatid differentiation in mice. Development 129:3669–3679PubMedGoogle Scholar
  147. 147.
    Yang J, Medvedev S, Yu J, Schultz RM, Hecht NB (2006) Deletion of the DNA/RNA-binding protein MSY2 leads to post-meiotic arrest. Mol Cell Endocrinol 250:20–24PubMedCrossRefGoogle Scholar
  148. 148.
    Yang J, Morales CR, Medvedev S, Schultz RM, Hecht NB (2007) In the absence of the mouse DNA/RNA-binding protein MSY2, messenger RNA instability leads to spermatogenic arrest. Biol Reprod 76:48–54PubMedCrossRefGoogle Scholar
  149. 149.
    Tafuri SR, Familari M, Wolffe AP (1993) A mouse Y box protein, MSY1, is associated with paternal mRNA in spermatocytes. J Biol Chem 268:12213–12220PubMedGoogle Scholar
  150. 150.
    Mendez R, Murthy KG, Ryan K, Manley JL, Richter JD (2000) Phosphorylation of CPEB by Eg2 mediates the recruitment of CPSF into an active cytoplasmic polyadenylation complex. Mol Cell 6:1253–1259PubMedCrossRefGoogle Scholar
  151. 151.
    Hosoda N, Funakoshi Y, Hirasawa M et al (2011) Anti-proliferative protein Tob negatively regulates CPEB3 target by recruiting Caf1 deadenylase. EMBO J 30:1311–1323PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Pique M, Lopez JM, Foissac S, Guigo R, Mendez R (2008) A combinatorial code for CPE-mediated translational control. Cell 132:434–448PubMedCrossRefGoogle Scholar
  153. 153.
    Campbell ZT, Menichelli E, Friend K et al (2012) Identification of a conserved interface between PUF and CPEB proteins. J Biol Chem 287:18854–18862PubMedPubMedCentralCrossRefGoogle Scholar
  154. 154.
    Kurihara Y, Tokuriki M, Myojin R et al (2003) CPEB2, a novel putative translational regulator in mouse haploid germ cells. Biol Reprod 69:261–268PubMedCrossRefGoogle Scholar
  155. 155.
    Spassov DS, Jurecic R (2002) Cloning and comparative sequence analysis of PUM1 and PUM2 genes, human members of the Pumilio family of RNA-binding proteins. Gene 299:195–204PubMedCrossRefGoogle Scholar
  156. 156.
    Zamore PD, Williamson JR, Lehmann R (1997) The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. RNA 3:1421–1433PubMedPubMedCentralGoogle Scholar
  157. 157.
    Xu EY, Chang R, Salmon NA, Reijo Pera RA (2007) A gene trap mutation of a murine homolog of the Drosophila stem cell factor Pumilio results in smaller testes but does not affect litter size or fertility. Mol Reprod Dev 74:912–921PubMedCrossRefGoogle Scholar
  158. 158.
    Chen D, Zheng W, Lin A, Uyhazi K, Zhao H, Lin H (2012) Pumilio 1 suppresses multiple activators of p53 to safeguard spermatogenesis. Curr Biol 22:420–425PubMedPubMedCentralCrossRefGoogle Scholar
  159. 159.
    Suzuki A, Igarashi K, Aisaki K, Kanno J, Saga Y (2010) NANOS2 interacts with the CCR4-NOT deadenylation complex and leads to suppression of specific RNAs. Proc Natl Acad Sci U S A 107:3594–3599PubMedPubMedCentralCrossRefGoogle Scholar
  160. 160.
    Saga Y (2010) Function of Nanos2 in the male germ cell lineage in mice. Cell Mol Life Sci 67:3815–3822PubMedCrossRefGoogle Scholar
  161. 161.
    Tsuda M, Sasaoka Y, Kiso M et al (2003) Conserved role of nanos proteins in germ cell development. Science 301:1239–1241PubMedCrossRefGoogle Scholar
  162. 162.
    Beck AR, Miller IJ, Anderson P, Streuli M (1998) RNA-binding protein TIAR is essential for primordial germ cell development. Proc Natl Acad Sci U S A 95:2331–2336PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Youngren KK, Coveney D, Peng X et al (2005) The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 435:360–364PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Sada A, Suzuki A, Suzuki H, Saga Y (2009) The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 325:1394–1398PubMedCrossRefGoogle Scholar
  165. 165.
    Reynolds N, Cooke HJ (2005) Role of the DAZ genes in male fertility. Reprod Biomed Online 10:72–80PubMedCrossRefGoogle Scholar
  166. 166.
    VanGompel MJW, Xu EY (2011) The roles of the DAZ family in spermatogenesis: more than just translation? Spermatogenesis 1:36–46PubMedPubMedCentralCrossRefGoogle Scholar
  167. 167.
    Vogel T, Speed RM, Ross A, Cooke HJ (2002) Partial rescue of the Dazl knockout mouse by the human DAZL gene. Mol Hum Reprod 8:797–804PubMedCrossRefGoogle Scholar
  168. 168.
    Saunders PT, Turner JM, Ruggiu M et al (2003) Absence of mDazl produces a final block on germ cell development at meiosis. Reproduction 126:589–597PubMedCrossRefGoogle Scholar
  169. 169.
    Schrans-Stassen BH, Saunders PT, Cooke HJ, de Rooij DG (2001) Nature of the spermatogenic arrest in Dazl −/− mice. Biol Reprod 65:771–776PubMedCrossRefGoogle Scholar
  170. 170.
    Ruggiu M, Speed R, Taggart M et al (1997) The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 389:73–77PubMedCrossRefGoogle Scholar
  171. 171.
    Lin Y, Page DC (2005) Dazl deficiency leads to embryonic arrest of germ cell development in XY C57BL/6 mice. Dev Biol 288:309–316PubMedCrossRefGoogle Scholar
  172. 172.
    Reynolds N, Collier B, Bingham V, Gray NK, Cooke HJ (2007) Translation of the synaptonemal complex component Sycp3 is enhanced in vivo by the germ cell specific regulator Dazl. RNA 13:974–981PubMedPubMedCentralCrossRefGoogle Scholar
  173. 173.
    Reynolds N, Collier B, Maratou K et al (2005) Dazl binds in vivo to specific transcripts and can regulate the pre-meiotic translation of Mvh in germ cells. Hum Mol Genet 14:3899–3909PubMedCrossRefGoogle Scholar
  174. 174.
    Xu X, Tan X, Lin Q, Schmidt B, Engel W, Pantakani DV (1829) Mouse Dazl and its novel splice variant functions in translational repression of target mRNAs in embryonic stem cells. Biochim Biophys Acta 2013:425–435Google Scholar
  175. 175.
    Tsui S, Dai T, Warren ST, Salido EC, Yen PH (2000) Association of the mouse infertility factor DAZL1 with actively translating polyribosomes. Biol Reprod 62:1655–1660PubMedCrossRefGoogle Scholar
  176. 176.
    Kim B, Cooke HJ, Rhee K (2012) DAZL is essential for stress granule formation implicated in germ cell survival upon heat stress. Development 139:568–578PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Center for RNA Molecular Biology, Case Western Reserve UniversityClevelandUSA

Personalised recommendations