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Repression and Activation of Protamine mRNA Translation During Murine Spermatogenesis

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Germ Cell Development, Division, Disruption and Death

Part of the book series: Serono Symposia USA Norwell, Massachusetts ((SERONOSYMP))

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Abstract

Murine spermatogenesis initiates a few days after birth and continues for the duration of the sexual life of the animal. Spermatogenesis takes approximately 35 days and consists of the mitotic proliferation of spermatogonial cells, meiosis, and spermiogenesis, the haploid spermatid differentiation stage (Fig. 11.1). Transcription is ongoing throughout spermatogonial proliferation, meiosis, and the early spermiogenesis. In fact, unlike spermatogenesis in Drosophila where there is no postmeiotic transcription, in the mouse there is considerable elevation in the transcriptional apparatus shortly after meiosis (1). Transcription continues until the transition from the round to the elongating spermatid, and then ceases several days before to the completion of spermiogenesis (2, 3). The study of transcriptional activity has relied primarily on metabolic labeling studies, which are limited in their sensitivity. The available data do not allow us to distinguish between transcriptional silencing at the transition from round spermatid to elongating spermatid (about step 9), or the elongating spermatid to elongated spermatid transition (about step 13). Distinguishing between these two possibilities is important if one is to understand the reason for transcriptional silencing. Cessation of transcription at step 9 would likely involve developmental changes in the transcriptional apparatus, whereas transcriptional arrest at step 13 could be attributed to changes in chromatin structure that occur as chromosome condensation commences.

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References

  1. Schmidt EE, Schibier U. High accumulation of components of the RNA polymerase II transcription machinery in rodent spermatids. Development (Camb) 1995; 121:2373–83.

    CAS  Google Scholar 

  2. Kierszenbaum AL, Tres IL. Structural and transcriptional features of the mouse spermatid genome. J Cell Biol 1975;65:258–70.

    Article  PubMed  CAS  Google Scholar 

  3. Monesi V. Ribonucleic acid synthesis during mitosis and meiosis in the mouse testis. J Cell Biol 1964;22:521–32.

    Article  PubMed  CAS  Google Scholar 

  4. Bellve AR. The molecular biology of mammalian spermatogenesis. In: Finn CA, ed. Oxford reviews of reproductive biology. Oxford University Press: London, 1979:159–261.

    Google Scholar 

  5. Balhorn R, Weston S, Thomas C, Wyrobek AJ. DNA packaging in mouse spermatids. Synthesis of protamine variants and four transition proteins. Exp Cell Res 1984; 150: 298–308.

    Article  PubMed  CAS  Google Scholar 

  6. Kleene KC, Distel RJ, Hecht NB. Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse. Dev Biol 1984;105:71–9.

    Article  PubMed  CAS  Google Scholar 

  7. Kleene KC, Flynn J. Translation of mouse testis poly(A)+ mRNAs for testis-specific protein, protamine 1, and the precursor for protamine 2. Dev Biol 1987;123:125–35.

    Article  PubMed  CAS  Google Scholar 

  8. Mali P, Kaipia A, Kangasniemi M, Toppari J, Sandberg M, Hecht NB, et al. Stage-specific expression of nucleoprotein mRNAs during rat and mouse spermiogenesis. Reprod Fertil Dev 1989;1:369–82.

    Article  PubMed  CAS  Google Scholar 

  9. Schumacher JM, Lee K, Edelhoff S, Braun RE. Spnr, a murine RNA-binding protein that is localized to cytoplasmic microtubules. J Cell Biol 1995;129:1023–32.

    Article  PubMed  CAS  Google Scholar 

  10. Schumacher JM, Lee K, Edelhoff S, Braun RE. Distribution of Tenr, an RNA binding protein, in a lattice-like network within the spermatid nucleus in the mouse. Biol Reprod 1995;52:1274–83.

    Article  PubMed  CAS  Google Scholar 

  11. Braun RE, Peschon JJ, Behringer RR, Brinster RL, Palmiter RD. Protamine 3′-untranslated sequences regulate temporal translational control and subcellular localization of growth hormone in spermatids of transgenic mice. Genes Dev 1989;3:793–802.

    Article  PubMed  CAS  Google Scholar 

  12. Lee K, Haugen HS, Clegg CH, Braun RE. Premature translation of protamine 1 mRNA causes precocious nuclear condensation and arrests spermatid differentiation in mice. Proc Natl Acad Sci USA 1995;92:12451–5.

    Article  PubMed  CAS  Google Scholar 

  13. Braun RE, Behringer RR, Peschon JJ, Brinster RL, Palmiter RD. Genetically haploid spermatids are phenotypically diploid. Nature (Lond) 1989;337:373–6.

    Article  CAS  Google Scholar 

  14. Burgos MH, Fawcett DW. Studies on the fine structure of the mammalian testis. I. Differentiation of the spermatids in the cat (Felis domestica). J Biophys Biochem Cytol 1955;1:287–300.

    Article  PubMed  CAS  Google Scholar 

  15. Peschon JJ, Behringer RB, Brinster RL, Palmiter RD. Spermatid-specific expression of protamine 1 in transgenic mice. Proc Natl Acad Sci USA 1987;84:5316–9.

    Article  PubMed  CAS  Google Scholar 

  16. Zambrowicz BP, Harendza CJ, Zimmermann JW, Brinster RL, Palmiter RD. Analysis of the mouse protamine 1 promoter in transgenic mice. Proc Natl Acad Sci USA 1993;90:5071–5.

    Article  PubMed  CAS  Google Scholar 

  17. Meistrich ML. Histone and basic nuclear protein transitions in mammalian spermatogenesis. In: Hnilica G, Stein G, Stein J, eds. Histones and other basic nuclear proteins. Orlando: CRC Press, 1989:165–82.

    Google Scholar 

  18. Carré Eusebe D, Lederer F, Le KH, Elsevier SM. Processing of the precursor of protamine P2 in mouse. Peptide mapping and N-terminal sequence analysis of intermediates. Biochem J 1991;277:39–45.

    Google Scholar 

  19. Chauviere M, Martinage A, Debarle M, Alimi E, Sautiere P, Chevaillier P. Purification and characterization of precursors of mouse protamine mP2. C R Acad Sci III Life Sci 1991;313:107–12.

    CAS  Google Scholar 

  20. Morales CR, Kwon YK, Hecht NB. Cytoplasmic localization during storage and translation of the mRNAs of transition protein 1 and protamine 1, two translationally regulated transcripts of the mammalian testis. J Cell Sci 1991;100:119–31.

    PubMed  CAS  Google Scholar 

  21. Tarun SZ Jr, Sachs AB. A common function for mRNA 5′ and 3′ ends in translation initiation in yeast. Genes Dev 1995;9:2997–3007.

    Article  PubMed  CAS  Google Scholar 

  22. Tarun SZ Jr, Sachs AB. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J 1996;15:7168–77.

    PubMed  CAS  Google Scholar 

  23. Fajardo MA, Butner KA, Lee K, Braun RE. Germ cell-specific proteins interact with the 3′ untranslated regions of Prm-1 and Prm-2 mRNA. Dev Biol 1994;166:643–53.

    Article  PubMed  CAS  Google Scholar 

  24. Braun RE. Temporal translational regulation of the protamine 1 gene during mouse spermatogenesis. Enzyme (Basel) 1990;44:120–8.

    CAS  Google Scholar 

  25. SenGupta DJ, Zhang B, Kraemer B, Pochart P, Fields S, Wickens M. A three-hybrid system to detect RNA-protein interactions in vivo. Proc Natl Acad Sci USA 1996;93: 8496–501.

    Article  PubMed  CAS  Google Scholar 

  26. Wolffe AP. Structural and functional properties of the evolutionarily ancient Y-box family of nucleic acid binding proteins. Bioessays 1994;16:245–51.

    Article  PubMed  CAS  Google Scholar 

  27. Bouvet P, Matsumoto K, Wolffe AP. Sequence-specific RNA recognition by the Xenopus Y-box proteins. An essential role for the cold shock domain. J Biol Chem 1995;270:28297–303.

    Article  PubMed  CAS  Google Scholar 

  28. Lee K, Fajardo MA, Braun RE. A testis cytoplasmic RNA-binding protein that has the properties of a translational repressor. Mol Cell Biol 1996;16:3023–34.

    PubMed  CAS  Google Scholar 

  29. Gatignol A, Buckler-White A, Berkhout B, Jeang KT. Characterization of a human TAR RNA-binding protein that activates the HIV-1 LTR. Science 1991;251:1597–600.

    Article  PubMed  CAS  Google Scholar 

  30. Park H, Davies MV, Langland JO, Chang H, Nam YS, Tartaglia J, et al. TAR RNA-binding protein is an inhibitor of the interferon-induced protein kinase PKR. Proc Natl Acad Sci USA 1994;9:4713–7.

    Article  Google Scholar 

  31. Green SR, Mathews MB. Two RNA-binding motifs in the double-stranded RNA-activated protein kinase, DAI. Genes Dev 1992;6:2478–90.

    Article  PubMed  CAS  Google Scholar 

  32. St-Johnston D, Brown NH, Gal JG, Jantsch M. A conserved double-stranded RNA-binding domain. Proc Natl Acad Sci USA 1992;89:10979–83.

    Article  PubMed  CAS  Google Scholar 

  33. Farrell PJ, Balkow T, Hunt T, Jackson RJ. Phosphorylation of initiation factor elF-2 and the control of reticulocyte protein synthesis. Cell 1977;11:187–200.

    Article  PubMed  CAS  Google Scholar 

  34. Levin D, London IM. Regulation of protein synthesis: activation by double-stranded RNA of a protein kinase that phosphorylates eukaryotic initiation factor 2. Proc Natl Acad Sci USA 1978;75:1121–5.

    Article  PubMed  CAS  Google Scholar 

  35. Hershey JW. Translational control in mammalian cells. Annu Rev Biochem 1991;60: 717–55.

    Article  PubMed  CAS  Google Scholar 

  36. Chang HW, Watson JC, Jacobs BL. The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. Proc Natl Acad Sci USA 1992;89:4825–9.

    Article  PubMed  CAS  Google Scholar 

  37. Cosentino GP, Venkatesan S, Serluca FC, Green SR, Mathews MB, Sonenberg N. Double-stranded-RNA-dependent protein kinase and TAR RNA-binding protein form homo- and heterodimers in vivo. Proc Natl Acad Sci USA 1995;92:9445–9.

    Article  PubMed  CAS  Google Scholar 

  38. Fajardo MF, Haugen HS, Clegg CH, Braun RE. Separate elements in the 3′ untranslated region of the mouse protamine 1 mRNA regulate translational repression and activation during murine spermatogenesis. Dev Biol 1997;191:42–52.

    Article  PubMed  CAS  Google Scholar 

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Braun, R.E. (1998). Repression and Activation of Protamine mRNA Translation During Murine Spermatogenesis. In: Zirkin, B.R. (eds) Germ Cell Development, Division, Disruption and Death. Serono Symposia USA Norwell, Massachusetts. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-2206-4_11

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  • DOI: https://doi.org/10.1007/978-1-4612-2206-4_11

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4612-7458-2

  • Online ISBN: 978-1-4612-2206-4

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