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Presence of a highly specific histone H1-like protein in the chromatin of the sperm of the bivalve mollusks

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Abstract

Chromatin organization in the sperm of the bivalve mollusks results from the interaction between a discrete number of protamine-like proteins (PL) and DNA. A small variable amount of histones is also present. An extensive study carried out on a relatively large number of species, within the class Bivalvia, has shown that it is possible to arrange these mollusks into five major categories on the basis of their PL composition (Ausio, J. Comp. Biochem. Physiol. 85, 439–449, (1986) [1]). In the present work, we have extended this analysis to a larger number of species and found that in spite of the inter- and intra-specific similarity of all PL proteins in their chemical composition, they exhibit different degrees of structural variability. Moreover one of these PL proteins is present in all the species analyzed, and bears an enormous resemblance to histones of the H1 family. The evolutionary significance of this finding is discussed.

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References

  1. Ausio J: Structural variability and compositional homology of the protamine-like components of the sperm from the bivalve mollusks. Comp Biochem Physiol 85: 439–449, 1986

    Google Scholar 

  2. Ausio J, Subirana JA: Conformational study and determination of the molecular weight of highly charged basic proteins by sedimentation equilibrium and gel electrophoresis. Biochemistry 21: 5910–5918, 1982b

    Google Scholar 

  3. Ausio J, Toumadje A, McParland R, Becker RR, Johnson WC Jr, Van Holde KE: Structural characterization of the trypsin resistant core in the nuclear sperm-specific protein from Spisula solidissima. Biochemistry 26: 975–982, 1987

    Google Scholar 

  4. Ausio J: An unusual cysteine-containing histone H1-like protein and two protamine-like proteins are the major nuclear proteins of the Sperm of the bivalve mollusk: Macoma nasuta. J Biol Chem 263: 10141–10150, 1988

    Google Scholar 

  5. Jutglar L, Borrell I, Ausio J: Primary, secondary and tertiary structure of the core of a histone H1-like protein from the sperm of Mytilus. J Biol Chem 266: 8184–8191, 1991

    Google Scholar 

  6. Ausio J: Purification and biochemical characterization of the nuclear sperm-specific proteins of the bivalve mollusks: Agriodesma saxicola and Mytilimeria nuttalli. Biol But; 182: 31–40, 1992

    Google Scholar 

  7. Odintsova NA, Rozov SM, Zalenskaya IA: The chromosomal proteins from the sperm of the bivalve mollusks Swiftopecten swifty and Glycymerys yesonensis. Comp Biochem Physiol 93-B: 163–167, 1989

    Google Scholar 

  8. Giancotti V, Russo E, Gasparini M, Serrano D, Del Piero D, Thorne AW, Cary PD, Crane-Robinson C: Proteins from the sperm of the bivalve mollusk: Ensis minor. Eur J Biochem 136: 509–516, 1983

    Google Scholar 

  9. Panyim S, Chalkley R: High resolution acrylamide gel electrophoresis of histones. Arch Biochem Biophys 130: 337–346, 1969

    Google Scholar 

  10. Hurley C: Electrophoresis of histones: A modified Pamyim and Chalkley system for slab gels. Anal Biochem 80: 624–626, 1977

    Google Scholar 

  11. Zalenskaya IA, Odintsova NA, Vorb'ev IV: Chromatin from sperm of Bivalvia mollusks. FEBS Lett 188: 243–247, 1985

    Google Scholar 

  12. Zalensky AO, Zalenskaya IA: Basic chromosomal proteins of marine invertebrates III. The proteins from the sperm of Bivalvia mollusks. Comp Biochem Physiol 66b: 415–419, 1980

    Google Scholar 

  13. Subirana JA, Cozcolluela C, Palau J, Unzeta M: Protamines and other basic proteins from spermatozoa of mollusks. Biochem Biophys Acta 317: 364–379, 1973

    Google Scholar 

  14. Ausio J, Van Holde KE: A dual chromatin organization in the sperm of the Bivalve mollusk: Spisula solidissima. Eur J Biochem 165: 363–371, 1987

    Google Scholar 

  15. Colom J, Subirana JA: Protamines and related proteins from spermatozoa of mollusks characterization and molecular weight determination by gel electrophoresis. Biochem Biophys Acta 581: 217–227, 1979

    Google Scholar 

  16. Ausio J, Subirana JA: A high molecular weight nuclear basic protein from the bivalve mollusk Spisula solidissima. J Biol Chem 257: 2802–2805, 1982a

    Google Scholar 

  17. Olivares C, Ganz H, Inostroza DC: A comparative study of the basic nuclear proteins from sperm of Bivalve mollusks. Comp Biochem Physiol 83B: 185–189, 1986a

    Google Scholar 

  18. Subirana JA, Colom J: Comparison of protamines from freshwater and marine bivalve mollusks: Evolutionary implications. FEBS Lett 220: 193–196, 1981

    Google Scholar 

  19. Zalensky AO, Avromova ZV: Nucleosomal organization of a part of chromatin in mollusks sperm nuclei with a mixed basic protein composition. Mol Biol Rep 10: 69–74, 1984

    Google Scholar 

  20. Ausio J, Subirana JA, Nuclear proteins and the organization of chromatin in spermatozoa of Mytilus edulis. Exp Cell Res 141: 39–45, 1982c

    Google Scholar 

  21. Odintsova NA, Suirnarchuk, Zalensakaya IA, Zalensky AO: Partial fractionation and certain characteristics of the basic chromatin proteins of Bivalve mollusk sperm. Biochemistry (USSR) 46: 404–410, 1981

    Google Scholar 

  22. Olivares C, Ruiz S, Comudella L: Characterization of histone and protamine variants in sperm of the bivalve mollusk: Aulacomya ater. FEBS Lett 205: 195–199, 1986b

    Google Scholar 

  23. Olivares C, Ruiz S: Nucleosomal organization of chromatin in sperm nuclei of the bivalve mollusk Aulacomya ater. Mol Cell Biochem 101: 93–99, 1991

    Google Scholar 

  24. Mogensen C, Carlos S, Ausio J: Microheterogeneity and interspecific variability of the nuclear sperm proteins from Mytilus. FEBS Lett 282: 273–276, 1991

    Google Scholar 

  25. Allan J, Hartman PG, Crane-Robinson L, Aviles FX: The structure of histone H1 and its location in chromatin. Nature 288: 675–679, 1980

    Google Scholar 

  26. Sellos D: The histones isolated from the sperm of the oyster Crassostrea gigas. Cell Diff 17: 183–192, 1985

    Google Scholar 

  27. Uschewa A, Patriotis C, Avramova J: An H1-like protein from the sperm chromatin of Mytilus galloprovincialis. Cell Biol Int Rep 9: 253–263, 1985

    Google Scholar 

  28. Ausio J, Greulich KO, Haas E, Wachtel E: Characterization of the florescence of the protamine thynnine and studies of its binding to double stranded DNA. Biopolymers 23: 2559–2571, 1984

    Google Scholar 

  29. Poccia D: Remodeling of nucleoproteins during gametogenesis, fertilization and early development. Int Rev Cytol 105: 1–65, 1986

    Google Scholar 

  30. Poccia D: Regulation of chromatin condensation and decondensation in sea urchin pronuclei. In: R Schlegel, MS Halleck, PN Rao (ed.) Molecular Regulation of Nuclear Events in Mitosis and Meiosis. Academic Press Inc, 1987, pp 149–177

  31. Porter DC, Moy GW, Vacquier VD: C-AMP-dependent protein kinase of sea urchin sperm phosphorylates sperm histone H1 on a single site. J Biol Chem 263: 2750–2755, 1988

    Google Scholar 

  32. Isenberg I: Histones, In: H. Busch (ed.) The Cell Nucleus Vol. 4, Part A. Academic Press, N. Y., 1978, pp 135–154

    Google Scholar 

  33. Cole RD: A minireview of microheterogeneity of H1 histone and its possible significance. Anal Biochem 336: 24–30, 1984

    Google Scholar 

  34. Libertini L, Ausio J, Van Holde KE, Small E: Highly cooperative binding to DNA by a histone-like sperm-specific protein from Spisula solidissima. Biopolymers 27: 1459–1477, 1988

    Google Scholar 

  35. Von Holt C, Strickland WN, Brandt WF, Strickland MS: More histone structures. FEBS Lett 100: 201–218, 1979

    Google Scholar 

  36. Subirana JA: Nuclear proteins in spermatozoa and their interactions with DNA. The sperm cell, proceedings of the Fourth International Symposium on spermatology, Seillac, France. In: André J (ed.) Martinus Nijhoff Pub, The Hague, 1983

    Google Scholar 

  37. Subirana JA: On the biological role of basic proteins in spermatozoa and during spermiogenesis. In: Duckett JG, Racey PA (ed.) The Biology of the Male Gamete (supplement 1 to the Biological Journal of the Linnean Society), Vol. 7, 1975, pp 239–244

  38. Kuhn-Schnyder E, Rieber H: Handbook of Paleozoology. The Johns Hopkins University Press, Baltimore and London, 1986

    Google Scholar 

  39. Mayes ELV, Johns EW: In: Johns (ed.) The HMG Chromosomal Proteins. Academic Press, New York, 1982, pp 223–247

    Google Scholar 

  40. Barfod NM, Larsen N: Polymeritization of protamine sulphate by carbodiimide and interaction of isolated protamine polymers with human red blood cells. Biochem Biophys Acta 427: 197–207, 1976

    Google Scholar 

  41. Briand G, Kmiecik D, Santiere P, Wouters D, Borie-Loy O, Biserte G, Mazen A, Champagne M: Chicken erthrocyte histone H5. FEBS Lett 112: 197–151, 1980

    Google Scholar 

  42. Liao LW, Cole RD: The amino acid sequence of residues 1–104 of CTL-1, a bovine H1 histone. J Biol Chem 256: 3024–3029, 1981

    Google Scholar 

  43. Kmiecik D, Sellos D, Belaiche D, Santiere P: Primary structure of the two variants of a sperm-specific histone H1 from the annelid Platynereis dumerilii. Eur J Biochem 150: 359–370, 1985

    Google Scholar 

  44. Strickland WN, Strickland M, Brandt WF, Van-Holt C, Lehmann A, Wittmann-Liebold B: The primary structure of histone Hl from sperm of the sea urchin Parechinus angulosus. Eur J Biochem 104: 567–578, 1980

    Google Scholar 

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Ausio, J. Presence of a highly specific histone H1-like protein in the chromatin of the sperm of the bivalve mollusks. Mol Cell Biochem 115, 163–172 (1992). https://doi.org/10.1007/BF00230327

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  • DOI: https://doi.org/10.1007/BF00230327

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