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PMID: 8618919 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Premature translation of protamine 1 mRNA causes precocious nuclear condensation and arrests spermatid differentiation in mice.

Lee K, Haugen HS, Clegg CH, Braun RE

Abstract

Translational control is a major form of regulating gene expression during gametogenesis and early development in many organisms. We sought to determine whether the translational repression of the protamine 1 (Prm1) mRNA is necessary for normal spermatid differentiation in mice. To accomplish this we generated transgenic animals that carry a Prm1 transgene lacking its normal 3' untranslated region. Premature translation of Prm1 mRNA caused precocious condensation of spermatid nuclear DNA, abnormal head morphogenesis, and incomplete processing of Prm2 protein. Premature accumulation of Prm1 within syncytial spermatids in mice hemizygous for the transgene caused dominant male sterility, which in some cases was accompanied by a complete arrest in spermatid differentiation. These results demonstrate that correct temporal synthesis of Prm1 is necessary for the transition from nucleohistones to nucleoprotamines.

MeSH Terms
Animals Cell Differentiation Cell Nucleus/physiology,ultrastructure Fertility Gene Expression Regulation Infertility, Male Male Mice Mice, Transgenic Morphogenesis Mosaicism Nuclear Proteins/isolation & purification,metabolism Protamines/genetics,metabolism Protein Biosynthesis RNA, Messenger/metabolism Spermatids/cytology,metabolism,physiology Testis/cytology,pathology,physiology
Chemicals
Nuclear Proteins Prm1 protein, mouse Protamines RNA, Messenger
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Lee K
University of Washington, Department of Genetics, Seattle 98195-7360, USA.
Haugen H S
Clegg C H
Braun R E
References (28)
28 references, click to expand
  1. Morphogenetic factors influencing the shape of the sperm head.
    Dev Biol. 1971 Oct;26(2):220-51 PMID: 5168310
  2. High resolution acrylamide gel electrophoresis of histones.
    Arch Biochem Biophys. 1969 Mar;130(1):337-46 PMID: 5778650
  3. Changes sperm culei during sperimogensis and epidymal maturation.
    Exp Cell Res. 1976 Apr;99(1):72-8 PMID: 1261617
  4. Low-molecular-weight basic proteins in spermatids.
    Methods Cell Biol. 1977;16:297-316 PMID: 886984
  5. Human growth hormone DNA sequence and mRNA structure: possible alternative splicing.
    Nucleic Acids Res. 1981 Aug 11;9(15):3719-30 PMID: 6269091
  6. DNA packaging in mouse spermatids. Synthesis of protamine variants and four transition proteins.
    Exp Cell Res. 1984 Feb;150(2):298-308 PMID: 6692853
  7. Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse.
    Dev Biol. 1984 Sep;105(1):71-9 PMID: 6468765
  8. Factors affecting the efficiency of introducing foreign DNA into mice by microinjecting eggs.
    Proc Natl Acad Sci U S A. 1985 Jul;82(13):4438-42 PMID: 3892534
  9. The amino acid sequence of human sperm protamine P1.
    Biosci Rep. 1985 May;5(5):383-91 PMID: 4027356
  10. Structural function of the basic nuclear proteins in ram spermatids.
    J Ultrastruct Res. 1984 Mar;86(3):262-72 PMID: 6544864
  11. Spermatid-specific expression of protamine 1 in transgenic mice.
    Proc Natl Acad Sci U S A. 1987 Aug;84(15):5316-9 PMID: 3037541
  12. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  13. Translation of mouse testis poly(A)+ mRNAs for testis-specific protein, protamine 1, and the precursor for protamine 2.
    Dev Biol. 1987 Sep;123(1):125-35 PMID: 2442049
  14. Genetically haploid spermatids are phenotypically diploid.
    Nature. 1989 Jan 26;337(6205):373-6 PMID: 2911388
  15. Protamine 3'-untranslated sequences regulate temporal translational control and subcellular localization of growth hormone in spermatids of transgenic mice.
    Genes Dev. 1989 Jun;3(6):793-802 PMID: 2744463
  16. Mouse transition protein 1 is translationally regulated during the postmeiotic stages of spermatogenesis.
    Mol Reprod Dev. 1989;1(3):193-200 PMID: 2627368
  17. Protamine transcript sharing among postmeiotic spermatids.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2407-11 PMID: 2006178
  18. Cytoplasmic protein binding to highly conserved sequences in the 3' untranslated region of mouse protamine 2 mRNA, a translationally regulated transcript of male germ cells.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3584-8 PMID: 2023906
  19. Processing of the precursor of protamine P2 in mouse. Peptide mapping and N-terminal sequence analysis of intermediates.
    Biochem J. 1991 Jul 1;277 ( Pt 1):39-45 PMID: 1854346
  20. [Purification and characterization of precursors of mouse protamine mP2].
    C R Acad Sci III. 1991;313(2):107-12 PMID: 1913252
  21. Temporal translational regulation of the protamine 1 gene during mouse spermatogenesis.
    Enzyme. 1990;44(1-4):120-8 PMID: 2133645
  22. Analysis of the mouse protamine 1 promoter in transgenic mice.
    Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5071-5 PMID: 8389466
  23. Purification, culture, and fractionation of spermatogenic cells.
    Methods Enzymol. 1993;225:84-113 PMID: 8231890
  24. Identification of the binding site of two monoclonal antibodies to human protamine.
    Mol Immunol. 1993 Dec;30(18):1633-8 PMID: 7505880
  25. Germ cell-specific proteins interact with the 3' untranslated regions of Prm-1 and Prm-2 mRNA.
    Dev Biol. 1994 Dec;166(2):643-53 PMID: 7813783
  26. A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal.
    Am J Anat. 1956 Nov;99(3):391-413 PMID: 13402725
  27. RIBONUCLEIC ACID SYNTHESIS DURING MITOSIS AND MEIOSIS IN THE MOUSE TESTIS.
    J Cell Biol. 1964 Sep;22:521-32 PMID: 14206420
  28. Structural and transcriptional features of the mouse spermatid genome.
    J Cell Biol. 1975 May;65(2):258-70 PMID: 1127016
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1995-12-19
Pages
12451-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC40375
Subset
IM
Grants
NICHD NIH HHS · HD27215 · United States
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