Protamines, not histones, are the predominant basic proteins in sperm nuclei of solitary ascidian tunicates
M. Chiva
Departament d'Enginyeria Quimica, Universitat Politecnica de Catalunya, 08028, Barcelona, Spain
Search for more papers by this authorF. Lafargue
Laboratoire Arago, Université Pierre et Marie Curie, 66650 Banyuls-sur-Mer, France
Search for more papers by this authorE. Rosenberg
Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4
Bamfield Marine Station, Bamfield, British Columbia, Canada V0R 1B0
Search for more papers by this authorCorresponding Author
Dr. H. E. Kasinsky
Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4
Bamfield Marine Station, Bamfield, British Columbia, Canada V0R 1B0
Department of Zoology, University of British Columbia, Vancouver, B.C., Canada, V6T 1Z4===Search for more papers by this authorM. Chiva
Departament d'Enginyeria Quimica, Universitat Politecnica de Catalunya, 08028, Barcelona, Spain
Search for more papers by this authorF. Lafargue
Laboratoire Arago, Université Pierre et Marie Curie, 66650 Banyuls-sur-Mer, France
Search for more papers by this authorE. Rosenberg
Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4
Bamfield Marine Station, Bamfield, British Columbia, Canada V0R 1B0
Search for more papers by this authorCorresponding Author
Dr. H. E. Kasinsky
Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4
Bamfield Marine Station, Bamfield, British Columbia, Canada V0R 1B0
Department of Zoology, University of British Columbia, Vancouver, B.C., Canada, V6T 1Z4===Search for more papers by this authorAbstract
In this work we study the protein content in sperm nuclei from 10 species of ascidian tunicates. The 7 species that we have investigated cytochemically show type 3 intermediate sperm basic proteins, as observed previously for the solitary tunicate Styela montereyensis (Chiva, Rosenberg, and Kasinsky, J. Exp. Zool., 253:7–19, 1990). We have focused this study on two specific points: the presence of protamines and the presence of somatic histones. In 4 species belonging to the suborder Phlebobranchiata, sperm nuclei contain only a protein more basic than histones (protamine). This protamine has an electrophoretic mobility similar to core histone H4. The nuclei of sperm in the species belonging to the suborder Phlebobranchiata are also characterized by their complete lack of somatic histones. In 5 species from the suborder Stolidobranchiata, sperm nuclei contain a similar protamine. However, 2 species from the genus Styela contain additionally other protamines with different electrophoretic mobilities. For all species belonging to the suborder Stolidobranchiata, we also have found very small quantities of residual somatic histones. We conclude that during the process of spermiogenesis in ascidian tunicates protamines replace histones either completely (Phlebobranchiata) or almost completely (Stolidobranchiata). In this respect spermiogenesis in tunicates (class Ascidiacea) is similar to that in vertebrates which, in general, also display the substitution of somatic histones by protamines. On the other hand, this model is different from that in echinoderms, where the protein content of sperm nuclei consists mainly of somatic histones and sperm-specific variants of histones. © 1992 Wiley-Liss, Inc.
Literature Cited
- Ausio, J., and R. McParland (1989) Sequence and characterization of the sperm-specific protein from Mytilus californianus. Eur. J. Biochem., 182: 569–576.
-
Balhorn, R.
(1989)
Mammalian protamines: Structure and molecular interactions. In:
Molecular Biology of Chromosome Function.
K. W. Adolph, ed.
Springer-Verlag, New York,
pp. 366–395.
10.1007/978-1-4612-3652-8_17 Google Scholar
- Barnes, R. D. (1987) Invertebrate Zoology, 5th ed. Saunders College, Philadelphia.
- Berrill, N. J. (1950) The Tunicata, with an Account of British Species. Vol. 133. Ray Society, London.
- Bloch, D. P. (1969) A catalog of sperm histones. Genetics (Suppl.), 61: 93–111.
-
Bloch, D. P.
(1976)
Histones of sperm. In:
Handbook of Genetics.
R. C. King, ed.
Plenum Press, New York,
Vol. 5,
pp. 139–167.
10.1007/978-1-4615-7148-3_5 Google Scholar
- Bols, N. C., M. Mann, and H. E. Kasinsky (1986) Detection of sperm histone diversity among vertebrates by alkaline fast green staining. Stain Tech., 61: 111–119.
- Brien, P. (1948) Embranchement des tunicieres: Morphologie et reproduction. In: Traité de Zoologie. P. P. Grassé, ed. Masson et a Cie, Paris, Vol. 11, pp. 553–894.
- Chauvière, M., A. Martinage, P. Sautière, and P. Chevaillier (1990) Les protéines nucleaires basiques de transition au cours de la spermiogenèse de la roussette Scylliorhinus caniculus. Reprod. Nutr. Dev., 30: 349–354.
-
Chevaillier, P.
(1983)
Some aspects of chromatin organization in sperm nuclei. In:
The Sperm Cell.
J. André., ed.
Martinus Nijhoff, The Hague,
pp. 179–196.
10.1007/978-94-009-7675-7_37 Google Scholar
- Chevaillier, P., A. Martinage, A. Arkhis, and P. Sautière (1990) Les précurseurs des protamines dans le spematozoide humain. Reprod. Nutr. Dev., 30: 343–347.
- Chiva, M., H. E. Kasinsky, M. Mann, and J. A. Subirana (1988) On the diversity of sperm basic proteins in vertebrates: VI. Cytochemical and biochemical analysis in birds. J. Exp. Zool., 245: 304–317.
- Chiva, M., H. E. Kasinsky, and J. A. Subirana (1987) Characterization of protamines from four avian species. Febs Lett., 215: 237–240.
- Chiva, M., and C. Mezquita (1983) Quantitative changes of high mobility group non-histone chromosomal proteins HMG-1 and HMG-2 during rooster spermatogenesis. Febs Lett., 162: 324–328.
- Chiva, M., E. Rosenberg, and H. E. Kasinsky (1990) Nuclear basic proteins in mature testis of the ascidian tunicate Styela montereyensis. J. Exp. Zool., 253: 7–19.
- Christensen, M. E., J. B. Rattner, and G. H. Dixon (1984) Hyperacetylation of histone H4 promotes chromatin decondensation prior to histone replacement by protamines during spermatogenesis in rainbow trout. Nucleic Acid Res., 12: 4575–4592.
- Daban, M., M. Chiva, E. Rosenberg, H. E. Kasinsky, and J. A. Subirana (1991) Protamines in prosobranchian gastropods (Mollusca) vary with different modes of reproduction. J. Exp. Zool., 257: 265–283.
- Daban, M., M. Chiva, J. A. Subirana, D. Kulak, E. Rosenberg, and H. E. Kasinsky (1988) Characterization of sperm basic proteins in gastropod molluscs, barnacles and tunicates. J. Cell Biol., 107: 168.
- Daban, M., H. E. Kasinsky, E. Morriconi, and M. Chiva (1990) Characterization of nuclear sperm basic proteins in one archaeogastropod: Comparison of protamines between species. Comp. Biochem. Physiol. [B.], 96: 123–127.
- Franzén, A. (1977) Sperm structure with regard to fertilization biology and phylogenetics. Verh. Dtsch. Zool. Ges., 123–138.
- Franzén, A. (1987) Spermatogenesis. In: Reproduction of Marine Invertebrates. Vol. 10: General Aspects: Seeking Unity in Diversity. R. C. King, J. S. Pearse, and V. B. Pearse, eds. Blackwell, Palo Alto, CA, pp. 1–47.
- Grimes, S. R. (1986) Nuclear proteins in spermatogenesis. Comp. Biochem. Physiol. [B.], 83: 495–500.
- Grimes, S. R., and N. Henderson (1984) Hyperacetylation of histone H4 in rat testis spermatids. Exp. Cell Res., 152: 91–97.
- Hecht, N. B. (1989) Mammalian protamines and their expression. In: Histones and Other Basic Nuclear Proteins. L. Hnilica, G. Stein, and J. Stein, eds. CRC Press, Boca Raton, FL, pp. 347–373.
- Hiyoshi, H., S. Uno, T. Yokota, C. Katagiri, H. Nishida, M. Takai, K. Agata, G. Eguchi, and S. Abé (1991) Isolation of cDNA for a Xenopus laevis basic nuclear protein (SP4) mRNA in primary spermatocytes. Exp. Cell Res., 194: 95–99.
- Holland, L. Z. (1991) The phylogenetic significance of tunicate sperm morphology. In: Proceedings of Sixth International Congress of Spermatology, Siena. B. Baccetti, ed. Raven Press, pp. 961–965.
- Iaotru, K., and G. H. Dixon (1978) Protamine messenger RNA: Its life history during spermatogenesis in rainbow trout. Proc. Fed. Am. Soc. Exp. Biol., 37: 2526–2533.
- Kasinsky, H. E. (1989) Specificity and distribution of sperm basic proteins. In: Histones and Other Basic Nuclear Proteins. L. Hnilica, G. Stein, and J. Stein, eds. CRC Press, Boca Raton, FL, pp. 73–163.
-
Kasinsky, H. E.,
M. Mann,
M. Lemke, and
S. Y. Huang
(1985)
Diversity of sperm basic chromosomal proteins in the vertebrates: A phylogenetic point of view. In:
Chromosomal Proteins and Gene Expression.
G. R. Reeck,
G. H. Goodwin, and
P. Puigdomènech, eds.
Plenum Press, New York,
pp. 333–352.
10.1007/978-1-4684-7615-6_21 Google Scholar
- Kistler, W. S. (1989) Structures of testis-specific histones, spermatid transition proteins and their genes in mammals. In: Histones and Other Basic Nuclear Proteins. L. Hnilica, G. Stein, and J. Stein, eds. CRC Press, Boca Raton, FL, pp. 331–345.
- Koch, R. A., and C. C. Lambert (1990) Ultrastructure of sperm, spermiogenesis, and sperm-egg interactions in selected invertebrates and lower vertebrates which use external fertilization. J. Electron Microsc. Tech., 16: 115–154.
- Kozloff, E. N. (1983) Seashore Life of the Northern Pacific Coast. Douglas and McIntyre, Vancouver.
- Kozloff, E. N. (1987) Marine Invertebrates of the Pacific Northwest. University of Washington Press, Seattle, pp. 469–470.
- Kozloff, E. N. (1990) Invertebrates. Saunders College, Philadelphia, pp. 796–821.
- Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227: 680–685.
- Lambert, C. C. (1982) The ascidian sperm reaction. Am. Zool., 22: 841–849.
- Martin-Ponthieu, A., D. Wouters-Tyrou, D. Bélaïche, P. Sautière, P. Schindler, and A. Van Dorsselaer (1991) Cuttlefish sperm protamines. I. Amino acid sequences of two distinct variants. Eur. J. Biochem., 193: 611–619.
- Meistrich, M. L. (1989) Histone and basic nuclear protein transitions in mammalian spermatogenesis. In: Histones and Other Basic Nuclear Proteins. L. Hnilica, G. Stein, and J. Stein, eds. CRC Press, Boca Raton, FL, pp. 165–182.
- Mezquita, C., and C. S. Teng (1977) Studies on sex-organ development. Changes in nuclear and chromatin composition and genomic activity during spermatogenesis in the maturing rooster testis. Biochem. J., 164: 99–111.
- Millar, R. H. (1966) Evolution in ascidians. In: Some Contemporary Studies in Marine Science. H. Barnes, ed. George Allen and Unwin, London, pp. 519–534.
- Okamoto, Y., E. Muta, and S. Ota (1987) Primary structures of M6 and M17 of mugiline β (Mugil japonicus). J. Biochem., 101: 1017–1021.
- Oliva, R., and G. H. Dixon (1990) Vertebrate protamine gene evolution. I. Sequence alignment and gene structure. J. Mol. Evol., 30: 333–346.
- Oliva, R., and G. H. Dixon (1991) Vertebrate protamine genes and the histone-to-protamine replacement reaction. Prog. Nucleic Acid Res. Mol. Biol., 40: 25–94.
- Oliva, R., and C. Mezquita (1982) Histone H4 hyperacetylation and rapid turnover of its acetyl groups in transcriptionally inactive rooster testis spermatids. Nucleic Acid Res., 10: 8049–8059.
- Panyim, S., and R. Chalkley (1969) High resolution acrylamide gel electrophoresis in histones. Arch. Biochem. Biophys., 130: 337–346.
- Pearse, A. G. E. (1968) Histochemistry: Theoretical and Applied, 3rd ed. J. and A. Churchill, London, p. 601.
- Poccia, D. (1986) Remodelling of nucleoproteins during gametogenesis, fertilization, and early development. Int. Rev. Cytol., 105: 1–65.
- Poccia, D. L., M. V. Simpson, and G. R. Green (1987) Transactions in histone variants during sea urchin spermatogenesis. Dev. Biol., 121: 445–453.
- Prats, E., L. Cornudella, and A. Ruiz-Carrillo (1989) Nucleotide sequence of a cDNA for ⊘0, a histone to protamine transition protein from sea cucumbers spermatozoa. Nucleic Acids Res., 17: 10097.
- Risley, M. S., and R. A. Eckhardt (1979) Dissociation and separation of Xenopus laevis spermatogenic cells. J. Exp. Zool., 207: 93–106.
- Rosenberg, E., D. Kulak, M. Chiva, and H. E. Kasinsky (1991) Cytochemical investigation of sperm basic proteins. In: Sixth International Congress of Spermatology, B. Baccetti, ed. Raven Press, pp. 77–82.
- Rothschild, L. (1961) A Classification of Living Animals. John Wiley, New York, pp. 34–35.
- Sellos, D., and D. Kmiecik (1985) Characterization of the histones and protamines from the sperm of the marine worm Platynereis dumerilii. Comp. Biochem. Physiol [B.], 80: 119–126.
-
Subirana, J. A.
(1983)
Nuclear proteins in spermatozoa and their interactions with DNA. In:
The Sperm Cell.
J. André, ed.
Martinus Nijhoff, The Hague,
pp. 197–213.
10.1007/978-94-009-7675-7_38 Google Scholar
- Subirana, J. A., C. Cozcolluela, J. Palau, and M. Unzeta (1973) Protamines and other basic proteins from spermatozoa of molluscs. Biochim. Biophys. Acta., 317: 364–379.
- Takamune, K., H. Nishida, M. Takai, and C. Katagiri (1991) Primary structure of toad sperm protamines and nucleotide sequence of their cDNAs. Eur. J. Biochem., 196: 401–406.
- Villa, L. (1981) An electron microscopic study of spermiogenesis and spermatozoa of Molgula impura and Styela plicata (Ascidiacea, Tunicata). Acta Embryol. Morphol. Exp., 752: 69–85.
- Von Holt, C., P. de Groot, S. Schwager, and W. F. Brandt (1984) The structure of sea urchin histones and consideration of their function. In: Histones Genes: Structure, Organization and Regulation. G. S. Stein, J. L. Stein, and W. F. Marzluff, eds. John Wiley, New York, pp. 65–105.
