Abstract
Protamine of the archaeogastropod mollusc Monodonta turbinata has been isolated and characterized. With a mass of 13,476 Da, it is the largest known prolamine. Amino acid sequence of this protamine (106 residues) was established from data provided by automated sequence analysis and mass spectrometry of the protein and of its fragments. The primary structure of the NH2-terminal region exhibits repetitive sequence motifs “Basic-Ser” (mainly R-S) and both central and COOH-terminal regions are composed by arginine clusters. The amino acid sequence of Monodonta turbinata protamine shows structural similarities with other protamines from invertebrates and from birds and mammals.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Ausió J (1988) An unusual cysteine-containing histone H1-like protein and two protamine-like proteins are the major nuclear proteins of the sperm of the bivalve mollusc Macoma nasuta. J Biol Chem 263:10141–10150
Ausió J, McParland R (1989) Sequence and characterization of the sperm-specific protein ø3 from Mytilus californianus. Eur J Biochem 182:569–576
Bloch DP (1969) A catalog of sperm histones. Genetics (Suppl) 61: 93–111
Carlos S, Jutglar L, Borrell I, Hunt DF, Ausió J (1993a) Sequence and characterization of a sperm-specific histone H1-like protein of Mytilus californianus. J Biol Chem 268:185–194
Carlos S, Hunt DF, Rocchini C, Arnott DP, Ausió J (1993b) Post-translational cleavage of a histone H1-like protein in the sperm of Mytilus. J Biol Chem 268:195–199
Chiva M, Kulak D, Kasinsky HE (1989) Sperm basic proteins in the turtle Chrysemis picta: characterization and evolutionary implications. J Exp Zool 249:329–333
Chiva M, Rosenberg E, Kasinsky HE (1990) Nuclear basic proteins in mature testis of the ascidian tunicate Styela montereyensis. J Exp Zool 253:7–19
Chiva M, Daban M, Rosenberg E, Kasinsky HE (1991) Protamines in polyplacophors and gastropods as a model for evolutionary changes in molluscan sperm basic proteins. In: Baccetti B (ed) Comparative spermatology 20 years after. Serono Symp Publications from Raven Press, vol 75, pp 27–30
Chiva M, Kulak D, Rosenberg E, Kasinsky HE (1992) A protamine in a crustacean Balanus nubilus (Cirripedia, Thoracica) and its coexistence with acidic proteins in sperm nuclei. Comp Biochem Physiol 10213:935–939
Colom J, Subirana JA (1981) Presence of H2B histone in spermatozoa from marine gastropods. Exp Cell Res 131:462–465
Daban M, Morriconi E, Kasinsky HE, Chiva M (1990) Characterization of the nuclear sperm basic proteins in one archaeogastropod: comparison of protamines between species. Comp Biochem Physiol 9613:123–127
Daban M, Kasinsky HE, Lafargue F, Chiva M (1991a) Nuclear sperm basic proteins (protamines) in chitons (Polyplacophora). Compositional and structural analogies with protamines of other molluscs. Comp Biochem Physiol 9813:437–443
Daban M, Chiva M, Rosenberg E, Kasinsky HE, Subirana JA (1991b) Protamines in prosobranchian gastropods (Mollusca) vary with different modes of reproduction. J Exp Zool 257:265–283
Giancotti V, Buratti E, Santucci A, Neri P, Crane-Robinson C (1992) Molluscan sperm proteins: Ensis minor. Biochim Biophys Acta 1119:296–302
Kasinsky HE, Huang SY, Mann M, Roca J, Subirana JA (1985) On the diversity of sperm histones in the vertebrates. IV. Cytochemical and amino acid analysis in Anura. J Exp Zool 234:33–46
Kasinsky HE (1989) Specificity and distribution of sperm basic proteins. In: Histones and other basic nuclear proteins. CRC Press, Boca Raton, FL
Kouach M, Jaquinod M, Belaïche D, Sautière P, van Dorsselaer A, Chevaillier P, Briand G (1993) A corrected primary structure for dog-fish Scylliorhinus caniculus protamine Z3. Biochim Biophys Acta 1162:99–104
Martin-Ponthieu A, Wouters-Tyrou D, Belaiche D, Sautiére P, Schindler P, Van Dorsselaer A (1991) Cuttlefish sperm protamines. 1. Amino acid sequences of two distinct variants. Eur J Biochem 195:611–619
Miescher F (1874) Das protamin, eine neue organische base aus den samenfades des rheinlachses. Ber 7:376–379
Mogensen C, Carlos S, Ausió J (1991) Microheterogeneity and interspecific variability of the nuclear sperm proteins from Mytilus. FEBS Lett 282:273–276
Oliva R, Dixon GH (1991) Vertebrate protamine genes and the histoneto-protamine replacement reaction. Prog Nucleic Acid Res Mol Biol 40:25–94
Panyim S, Chalkley R (1969) High resolution acrylamide gel electrophoresis of histones. Arch Biochem Biophys 130:337–346
Poccia D (1986) Remodeling of nucleoprotamines during gametogenesis, fertilization, and early development. Int Rev Cytol 105:1–65
Retief JD, Dixon GH (1993) Evolution of pro-protamine P2 genes in primates. Eur J Biochem 214:609–615
Retief JD, Winkfein RJ, Dixon GH, Adroer R, Queralt R, Ballabriga J, Oliva R (1993) Evolution of protamine P1 genes in primates. J Mol Evol 37:426–434
Ruiz-Lara S, Prats E, Casas MT, Cornudella L (1993) Molecular cloning and sequence of a cDNA for the sperm-specific protein ø1 from the mussel Mytilus edulis. Nucleic Acids Res 21:2774
Saperas N, Chiva M, Ausió J (1992) Purification and characterization of the protamines and related proteins from the sperm of a tunicate Styela plicata. Comp Biochem Physiol 103B:969–974
Sautière P, Martinage A, Belaiche D, Arkhis A, Chevaillier P (1988) Comparison of the amino acid sequences of human prolamines HP2 and HP3 and of intermediate basic nuclear proteins HPS 1 and HPS2. Structural evidence that HPS1 and HPS2 are proprotamines. J Biol Chem 263:11059–11062
Schindler P, Bitsch F, Klarskov K, Roepstorff P, Briand G, WoutersTyrou D, Sautière P, Van Dorsselaer A (1991) Cuttlefish sperm protamines. 2. Mass spectrometry of protamines and related peptides. Eur J Biochem 195:621–629
Subirana JA (1983) Nuclear proteins in spermatozoa and their interactions with DNA. In: Andre J (ed) The sperm cell. Martinus Nijhoff, The Hague
Subirana JA (1990) Analysis of the charge distribution in the C-terminal region of histone H1 as related to its interaction with DNA. Biopolymers 29:1351–1357
Subirana JA, Cozcolluela C, Palau J, Unzeta M (1973) Protamines and other basic proteins from spermatozoa of molluscs. Biochim Biophys Acta 317:364–379
Takamune K, Nishida H, Takai M, Katagiri C (1991) Primary structure of toal sperm protamines and nucleotide sequence of their cDNAs. Eur J Biochem 196:401–406
Wouters-Tyrou D, Chartier-Harlin MC, Martin-Ponthieu A, Boutillon C, Van Dorsselaer A, Sautière P (1991) Cuttlefish spermatid-specific protein T. Molecular characterization of two variants T1 and T2, putative precursors of sperm protamine variants Sp1 and Sp2. J Biol Chem 266:17388–17395
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Daban, M., Martinage, A., Kouach, M. et al. Sequence analysis and structural features of the largest known protamine isolated from the sperm of the archaeogastropod Monodonta turbinata . J Mol Evol 40, 663–670 (1995). https://doi.org/10.1007/BF00160515
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00160515