Advertisement
Journal Articles
Nuclear envelope remodelling during rat spermiogenesis: distribution and expression pattern of LAP2/thymopoietins
M. Alsheimer, E. Fecher, R. Benavente
Journal of Cell Science 1998 111: 2227-2234;

Summary

Lamina-associated polypeptide 2 (LAP2) and the thymopoietins (TPs) are a family of proteins described in somatic cells of mammals, which are derived by alternative splicing from a single gene. For one of the members of the family (LAP2 = TPbeta) it has been shown that this integral membrane protein locates to the inner membrane of the nuclear envelope, and that it binds to chromatin and B-type lamins. In the present study, we observed that during the third phase of spermatogenesis (i.e. spermiogenesis), TP-labelling shifted progressively to one half of the nuclear periphery in round spermatids. In the elongating spermatid the signal then becomes restricted to one spot located at the posterior (centriolar) pole of the nucleus. Changes in localization are accompanied by the disappearance, first of TPgamma, and later on of LAP2/TPbeta. TPalpha is the only member of the family detectable in the mature sperm. Concomitantly, lamin B1, the only nuclear lamina protein known to be expressed in mammalian spermatids, showed a similar behaviour, i.e. shifted progressively to the centriolar pole of spermatid nuclei before it became undetectable in fully differentiated mature sperms. These results are the first demonstration that expression and localization patterns of TPs are coordinately and differentially regulated with lamins during a differentiation process.

REFERENCES

    1. Alsheimer M. and
    2. Benavente R.
    (1996). Change of karyoskeleton during mammalian spermatogenesis: expression pattern of nuclear lamin C2 and its regulation. Exp. Cell Res 228, 181–188
    OpenUrlCrossRefPubMedWeb of Science
    1. Benavente R. and
    2. Krohne G.
    (1985). Change of karyoskeleton during spermatogenesis of Xenopus: expression of lamin LIV, a nuclear lamina protein specific for the male germ line. Proc. Nat. Acad. Sci. USA 82, 6176–6180
    OpenUrlAbstract/FREE Full Text
    1. Benavente R. and
    2. Krohne G.
    (1986). Involvement of nuclear lamins in postmitotic reorganization of chromatin as demonstrated by microinjection of lamin antibodies. J. Cell Biol 103, 1847–1854
    OpenUrlAbstract/FREE Full Text
    1. Berger R.,
    2. Theodor L.,
    3. Shoham J.,
    4. Gokkel E.,
    5. Brok-Simoni F.,
    6. Avraham K. B.,
    7. Copeland N. G.,
    8. Jenkins N. A.,
    9. Rechavi G. and
    10. Simon A. J.
    (1996). The characterization and localization of the mouse thymopoietin/lamina-associated polypeptide 2 gene and its alternatively spliced products. Genome Res 6, 361–370
    OpenUrlAbstract/FREE Full Text
    1. Collas P. and
    2. Poccia D.
    (1995). Lipophilic structures of sperm nuclei target membrane vesicle binding and are incorporated into the nuclear envelope. Dev. Biol 169, 123–135
    OpenUrlCrossRefPubMed
    1. Collas P. and
    2. Poccia D.
    (1996). Conserved binding recognition elements of sperm chromatin, sperm lipophilic structures and nuclear envelope precursor vesicles. Eur. J. Cell Biol 71, 22–32
    OpenUrlPubMed
    1. Collas P.,
    2. Courvalin J. C. and
    3. Poccia D.
    (1996). Targeting of membranes to sea urchin sperm chromatin is mediated by a lamin B receptor-like integral membrane protein. J. Cell Biol 135, 1715–1725
    OpenUrlAbstract/FREE Full Text
    1. Cowin P. and
    2. Burke B.
    (1996). Cytoskeleton-membrane interactions. Curr. Opin. Cell Biol 8, 56–65
    OpenUrlCrossRefPubMedWeb of Science
    1. Erickson R. P.
    (1990). Post-meiotic gene expression. Trends Genet 6, 264–269
    OpenUrlCrossRefPubMedWeb of Science
    1. Foisner R. and
    2. Gerace L.
    (1993). Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 73, 1267–1279
    OpenUrlCrossRefPubMedWeb of Science
    1. Franke W. W.,
    2. Schmid E.,
    3. Vanderkerckhove J. and
    4. Weber K.
    (1980). A permanently proliferating rat vascular smooth cell with maintained expression of smooth muscle characteristics, including actin of the smooth muscle type. J. Cell Biol 87, 594–600
    OpenUrlAbstract/FREE Full Text
    1. Furukawa K. and
    2. Hotta Y.
    (1993). cDNA cloning of a germ cell-specific lamin B3 from mouse spermatocytes and analysis of its ectopic expression in somatic cells. EMBO J 12, 97–106
    OpenUrlPubMedWeb of Science
    1. Furukawa K.,
    2. Inagaki H. and
    3. Hotta Y.
    (1994). Identification and cloning of an mRNA coding for a germ cell-specific A-type lamin in mice. Exp. Cell Res 212, 426–430
    OpenUrlCrossRefPubMedWeb of Science
    1. Furukawa K.,
    2. Pante N.,
    3. Aebi U. and
    4. Gerace L.
    (1995). Cloning and cDNA for lamina-associated polypeptide 2 (LAP2) and identification of regions that specify targeting to nuclear envelope. EMBO J 14, 1626–1636
    OpenUrlPubMedWeb of Science
    1. Furukawa K.,
    2. Fritze C. E. and
    3. Gerace L.
    (1998). The major nuclear envelope targeting domain of LAP2 coincides with its lamin binding region but is distinct from its chromatin interaction domain. J. Biol. Chem 273, 4213–4219
    OpenUrlAbstract/FREE Full Text
    1. Georgatos S.,
    2. Meier J. and
    3. Simons G.
    (1994). Lamins and lamin-associated proteins. Curr. Opin. Cell Biol 6, 347–353
    OpenUrlCrossRefPubMedWeb of Science
    1. Goldberg M.,
    2. Jenkins H.,
    3. Allen T.,
    4. Whitfield W. G. G. and
    5. Hutchison C. J.
    (1995). Xenopus lamin B3 has a direct role in the assembly of replication competent nucleus: evidence from cell-free extracts. J. Cell Sci 108, 3451–3461
    OpenUrlAbstract/FREE Full Text
    1. Harris C. A.,
    2. Andryuk P. J.,
    3. Cline S. C.,
    4. Natarajan A.,
    5. Siekierka J. J. and
    6. Goldstein G.
    (1994). Three distinct human thymopoietins are derived from alternatively spliced mRNAs. Proc. Nat. Acad. Sci. USA 91, 6283–6287
    OpenUrlAbstract/FREE Full Text
    1. Harris C. A.,
    2. Andryuk P. J.,
    3. Cline S. C.,
    4. Mathew S.,
    5. Siekierka J. J. and
    6. Goldstein G.
    (1995). Structure and mapping of the human thymopoietin (TMPO) gene and relationship of human TMPO to rat lamin-associated polypeptide 2. Genomics 28, 198–205
    OpenUrlCrossRefPubMedWeb of Science
    1. Hecht N. B.
    (1995). The making of a spermatozoon: a molecular perspective. Dev. Genet 16, 95–103
    OpenUrlCrossRefPubMedWeb of Science
    1. Heyting C. and
    2. Dietrich A. J. J.
    (1991). Meiotic chromosome preparation and protein labelling. Meth. Cell Biol 35, 177–202
    OpenUrlPubMed
    1. Ishijima Y.,
    2. Toda T.,
    3. Matsuhita H.,
    4. Yoshida M. and
    5. Kimura N.
    (1996). Expression of thymopoietin/lamina-associated polypeptide 2 (TP /LAP2) and its family proteins as revealed by specific antibody induced against recombinant human thymopoietin. Biochem. Biophys. Res. Commun 226, 431–438
    OpenUrlCrossRefPubMed
    1. Kaufmann S. H.
    (1989). Additional members of the rat lamin polypeptide family. Structural and immunological characterization. J. Biol. Chem 264, 13946–13955
    OpenUrlAbstract/FREE Full Text
    1. Koken M. H.,
    2. Hoogerbrugge J. W.,
    3. Jasper-Dekker J.,
    4. De Wit J.,
    5. Willemsen R.,
    6. Roest H. P.,
    7. Grootegoed J. A. and
    8. Hoeijmakers J. H.
    (1996). Expression of the ubiquitin-conjugating DNA repair enzymes HHR6A and B suggests a role in spermatogenesis and chromatin modification. Dev. Biol 173, 119–132
    OpenUrlCrossRefPubMedWeb of Science
    1. Longo F. J.,
    2. Krohne G. and
    3. Franke W. W.
    (1987). Basic protein of the perinuclear theca of mammalian spermatozoa and spermatids: a novel class of cytoskeletal elements. J. Cell Biol 105, 1105–1120
    OpenUrlAbstract/FREE Full Text
    1. Matsudaira P. T.
    (1987). Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J. Biol. Chem 262, 10035–10038
    OpenUrlAbstract/FREE Full Text
    1. Meier J.,
    2. Campbell K. H. S.,
    3. Ford C. C.,
    4. Stick R. and
    5. Hutchison C. J.
    (1991). The role of lamin L III in nuclear assembly and DNA replication in cell-free extracts of Xenopus eggs. J. Cell Sci 98, 271–279
    OpenUrlAbstract/FREE Full Text
    1. Meistrich M. L.
    (1977). Separation of spermatogenic cells and nuclei from rodent testes. Meth. Cell Biol 15, 15–54
    OpenUrlCrossRefPubMed
    1. Newport J. W.,
    2. Wilson K. L. and
    3. Dunphy W. G.
    (1990). A lamin-independent pathway for nuclear envelope assembly. J. Cell Biol 111, 2247–2259
    OpenUrlAbstract/FREE Full Text
    1. Poccia D. and
    2. Collas P.
    (1997). Nuclear envelope dynamics during male pronuclear development. Dev. Growth Differ 39, 541–550
    OpenUrlCrossRefPubMedWeb of Science
    1. Rivkin E.,
    2. Cullinan E. B.,
    3. Tres L. L. and
    4. Kierszenbaum A. L.
    (1997). A protein associated with the manchette during rat spermiogenesis is encoded by a gene of the TBP-1-like subfamily with highly conserved ATPase and protease domains. Mol. Reprod. Dev 48, 77–89
    OpenUrlCrossRefPubMed
    1. Smith A. and
    2. Benavente R.
    (1992). Identification of a short lamin proteinselectively expressed during meiotic stages of rat spermatogenesis. Differentiation 52, 55–60
    OpenUrlPubMedWeb of Science
    1. Smith A. and
    2. Benavente R.
    (1992). Identification of a structural protein component of rat synaptonemal complexes. Exp. Cell Res 198, 291–297
    OpenUrlCrossRefPubMed
    1. Spann T. P.,
    2. Moir R. D.,
    3. Goldman A. E.,
    4. Stick R. and
    5. Goldman R. D.
    (1997). Disruption of nuclear laming organization alters the distribution of replication factors and inhibits DNA synthesis. J. Cell Biol 136, 1201–1212
    OpenUrlAbstract/FREE Full Text
    1. Thomas J. O. and
    2. Kornberg R. D.
    (1975). An octamere of histones in chromatin and free solution. Proc. Nat. Acad. Sci. USA 72, 2626–2630
    OpenUrlAbstract/FREE Full Text
    1. Vester B.,
    2. Smith A.,
    3. Krohne G. and
    4. Benavente R.
    (1993). Presence of a nuclear lamina in pachytene spermatocytes of the rat. J. Cell Sci 104, 557–563
    OpenUrlAbstract/FREE Full Text
    1. Ward W. S.,
    2. Partin A. W. and
    3. Coffey D. S.
    (1989). DNA loop domains in mammalian spermatozoa. Chromosoma 98, 157–159
    OpenUrl
    1. Wing S. S.,
    2. Bedard N.,
    3. Morales C.,
    4. Hingamp P. and
    5. Trasler J.
    (1996). A novel rat homolog of Saccharomyces cerevisiae ubiquitin-conjugating enzymes UBC4 and UBC5 with distinct biochemical features is induced during spermatogenesis. Mol. Cell. Biol 16, 4064–4072
    OpenUrlAbstract/FREE Full Text
    1. Ye O. and
    2. Worman H. J.
    (1996). Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J. Biol. Chem 271, 14653–14656
    OpenUrlAbstract/FREE Full Text
    1. Yang L.,
    2. Guan T. and
    3. Gerace L.
    (1997). Lamin-binding fragment of LAP2 inhibits increase in nuclear volume during the cell cycle and progression into S phase. J. Cell Biol 139, 1077–1087
    OpenUrlAbstract/FREE Full Text
    1. Zalenski A. O.,
    2. Allen M. J.,
    3. Kobayashi A.,
    4. Zalenskaya I. A.,
    5. Balhorn R. and
    6. Bradbury E. M.
    (1995). Well-defined genome architecture in the human sperm nucleus. Chromosoma 103, 577–590
    OpenUrlPubMedWeb of Science
    1. Zalenski A. O.,
    2. Tomilin N. V.,
    3. Zalenskaya I. A.,
    4. Teplitz R. L. and
    5. Bradbury E. B.
    (1997). Telomere-telomere interactions and candidate telomere binding protein(s) in mammalian sperm cells. Exp. Cell Res 232, 29–41
    OpenUrlCrossRefPubMedWeb of Science
Back to top

 Download PDF

Email
Journal Articles
Nuclear envelope remodelling during rat spermiogenesis: distribution and expression pattern of LAP2/thymopoietins
M. Alsheimer, E. Fecher, R. Benavente
Journal of Cell Science 1998 111: 2227-2234;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

First Person interviews

Photo collage of Chen Yu, Sushmita Chatterjee, Ruiqi Wang and Lotte Vanheer.

Have you seen our First Person interviews with the early-career first authors of our papers? The authors talk about their work in and out of the lab, the journeys that led them to where they are now and the scientists who inspired them along the way. Recently, we caught up with first authors Maitreyi Rathod, Sushmita Chatterjee, Lotte Vanheer, Rachel Furlong, Pamela Adami, Ruiqi Wang and Chen Yu.

Travelling Fellowship – New imaging approach unveils a bigger picture

Highlights from Travelling Fellowship trips

Find out how Pamela Imperadore’s Travelling Fellowship grant from The Company of Biologists took her to Germany, where she used new imaging techniques to investigate the cellular machinery underlying octopus arm regeneration. Don’t miss the next application deadline for 2020 travel, coming up on 29 November. Where will your research take you?

preLights – Meet the preLighters: an interview with Maiko Kitaoka

Maiko Kitaoka

Maiko Kitaoka is a graduate student in the lab of Rebecca Heald at the University of California, Berkeley. Here she studies the cause of chromosome mis-segregation defects in Xenopus hybrids. We caught up with Maiko to discuss her research, science communication, ballet, preprints and more.

Journal Meeting – Cell Dynamics: Host-Pathogen Interface

Registration is now open for the third instalment of the highly successful Cellular Dynamics Meeting Series, and will focus on ‘Host-Pathogen Interface’. The meeting will take place 17-20 May 2020, and further information is available here.

Cell Science at a Glance – Adaptor protein complexes and disease at a glance

A new poster from the Robinson lab summarises what is known about the five adaptor protein complexes and discuss how this helps to explain the clinical features of different genetic disorders.

JCS joins the Review Commons initiative

Journal of Cell Science is pleased to be a part of the new and exciting Review Commons initiative, launched by EMBO and ASAPbio. Streamlining the publishing process, Review Commons enables high-quality peer review to take place before journal submission. Papers submitted to Review Commons will be assessed independently of any journal, focusing solely on the paper’s scientific rigor and merit.