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The primary structure of a chondrichthyan protamine: A new apparent contradiction in protamine evolution

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Abstract

We have determined the primary structure of protamine R3 from ratfish (Hydrolagus colliei), a species belonging to the order Chimaeriformes (an old phylogenetic line among the chondrichthyes). Protamine R3 contains 48 residues organized as follows: ARRRH SMKKK RKSVR RRKTR KNQRK RKNSL GRSFK (Q/A)HGFL KQPPR FRP. Comparison of this sequence with both protamine Z3 fromScyliorhinus canicula (a chondrichthyan) and typical protamines from bony fish generates an apparent contradiction: Two relatively close species (H. colhei andS. canicula, both chondichthyes) display different protamines, whereas species more distant in evolution (S. canicula and bony fish) contain very similar protamine molecules. We note that this is not an isolated case in the evolution of sperm nuclear basic proteins (SNBPs) and discuss the possible significance of this fact.

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References

  • Ando T, Watanabe S (1969) A new method for fractionation of protamine and the amino acid sequence of one component of salmine and the three components of iridine. Int J Protein Res 1:221–224

    CAS  PubMed  Google Scholar 

  • Ausio J (1986) Structural variability and compositional homology of the protamine-like components of the sperm from the bivalve mollusks. Comp Biochem Physiol [B] 85:439–449

    Google Scholar 

  • Ausio J (1992) Presence of a highly specific histone Hl-like protein in the chromatin of the sperm of the bivalve mollusks. Mol Cell Biochem 115:163–172

    Article  CAS  PubMed  Google Scholar 

  • Ausio J (1995) Histone H1 and the evolution of the nuclear sperm-specific proteins. In: Jamieson BGM, Ausio J, Justine IL (eds) Advances in spermatozoal phylogeny and taxonomy. Mém Mus Natn Hist Nat 166:447–462

  • Ausio J, Greulick KO, Haas E, Wachtel E (1984) Characterization of the fluorescence of the protamine thynnine and studies of binding to double-stranded DNA. Biopolymers 23:2559–2571

    CAS  PubMed  Google Scholar 

  • Bols NC, Kasinsky HE (1973) An electrophoretic comparison of histories in anuran testes. Can J Zool 51(2):203–208

    CAS  Google Scholar 

  • Benton J (1990) Vertebrate paleontology. Unwinthyman, London, pp 1–377

    Google Scholar 

  • Chevaillier Ph., Martinage A, Gusse M, Sautiere P (1987) Amino acid sequence of scylliorhinine Z1 and comparison of the primary structure of the protamines of the dogfishScylliorhinus caniculus. Biochim Biophys Acta 914:19–27

    CAS  Google Scholar 

  • Chiva M, Kasinsky HE, Mann M, Subirana JA (1988) On the diversity of sperm basic proteins in the vertebrates: VI. Cytochemical and biochemical analysis in birds. J Exp Zool 245:304–317

    Article  CAS  Google Scholar 

  • 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, vol 75. Serono Symp, Raven Press, pp 27–30

  • Chiva M, Saperas N, Cdceres C, Ausio J (1995) Nuclear basic proteins from the sperm of tunicates, cephalochordates, agnathans and fish. In: Jamieson BGM, Ausio J, Justine JL (eds) Advances in spermatozoal phylogeny and taxonomy. Mem Mus Nam Hist Nat 166: 501–514

  • Compagno LJV (1991) The evolution and diversity of sharks. In: Gruber SH (ed) Discovering sharks. American Littoral Society, Highlands, NJ, pp 15–22

    Google Scholar 

  • Daban M, Martinage A, Kouach M, Chiva M, Subirana JA, Sautière P (1995) Sequence analysis and structural features of the largest known protamine isolated from the sperm of the ArchaeogastropodMonodonta turbinata. J Mol Evol 40:663–670

    Article  CAS  PubMed  Google Scholar 

  • Doolittle RF (1979) Protein evolution. In: Neurath H, Hill RL (eds) The proteins, vol 4. Academic Press, New York, pp 1–118

    Google Scholar 

  • Doolittle RF (1986) Of Urfs and Orfs. A primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley, CA, USA

    Google Scholar 

  • Doolittle RF (1992) Reconstructing history with amino acid sequences. Protein Sci 1:191–200

    CAS  PubMed  Google Scholar 

  • Doolittle RF, Feng DF, Johnson MS, McClure MA (1986) Relationships of human protein sequences to those of other organisms. Cold Spring Harb Symp Quant Biol 51(1):447–455

    CAS  PubMed  Google Scholar 

  • Gusse M, Sautiere P, Chauviere M, Chevaillier Ph (1983) Extraction, purification and characterization of the sperm protamines of the dogfishScylliorhinus caniculus. Biochim Biophys Acta 748:93–98

    CAS  PubMed  Google Scholar 

  • Hélène C, Lancelot G (1982) Interactions between functional groups in protein-nucleic acid association. Prog Biophys Mol Biol 39:1–68

    PubMed  Google Scholar 

  • Kasinsky HE (1989) Specificity and distribution of sperm basic proteins. In: Hnilica LS, Stein GS, Stein JL (eds) Histones and other basic nuclear proteins. CRC Press, Boca Raton, FL, pp 73–163

    Google Scholar 

  • Kasinsky HE, Huang SY, Kawuk S, Mann M, Sweeney MAJ, Yee B (1978) On the diversity of sperm histones in the vertebrates. III. Electrophoretic variability of testis-specific historic patterns in Anura contrasts with relative constancy in Squamata. J Exp Zool 203:109–126

    Article  CAS  Google Scholar 

  • Kasinsky HE, Mann M, Lemke M, Huang SY (1985a) Diversity of sperm basic chromosomal proteins in the vertebrates: a phylogenetic point of view. In: Reeck GR, Goodwin GH, Puigdomènech P (eds) Chromosomal proteins and gene expression. Plenum Press, New York, pp 333–352

    Google Scholar 

  • Kasinsky HE, Huang SY, Mann M, Roca J, Subirana JA (1985b) On the diversity of sperm histones in the vertebrates. IV. Cytochemical and amino acid analysis in Anura. J Exp Zool 234:33–46

    Article  CAS  Google Scholar 

  • Kouach M, Jaquinod M, Bélaiche D, Sautìere P, van Dorsselaer A, Chevaillier Ph., Briand G (1993) A corrected primary structure for dog-fishScylliorhinus caniculus protamine Z3. Biochim Biophys Acta 1162:99–104

    CAS  PubMed  Google Scholar 

  • Martinage A, Gusse M, Bélaiche D, Sautiere P, Chevaillier Ph (1985) Amino acid sequence of a cysteine-rich, arginine-rich sperm protamine of the dogfishScylliorhinus caniculus. Biochim Biophys Acta 831:172–178

    CAS  Google Scholar 

  • Oliva R, Dixon GH (1991) Vertebrate protamine genes and the histoneto-protamine replacement reaction. Prog Nucleic Acid Res Mol Biol 40:25–94

    CAS  PubMed  Google Scholar 

  • Olivares C, Valdivia R, Lafuente N, Kulak D, Kasinsky HE (1990) Electrophoretic analysis of sperm basic proteins inSchroederychthys chilensis and comparison with other cartilaginous fish. Rev Biol Mar Valparaiso 25:99–108

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Saperas N, Lloris D, Chiva M (1993a) Sporadic appearance of histones, histone-like proteins, and protamines in sperm chromatin of bony fish. J Exp Zool 265:575–586

    CAS  Google Scholar 

  • Saperas N, Chiva M, Bols NC, Kulak D, Kasinsky HE (1993b) Spermspecific basic proteins in the holocephalan fishHydrolagus colliei (Chondrychthyes, Chimaeriformes) and comparison with protamines from an elasmobranch. Biol Bull 185:186–196

    Google Scholar 

  • Saperas N, Ausió J, Lloris D, Chiva M (1994) On the evolution of protamines in bony fish: alternatives to the “retroviral horizontal transmission” hypothesis. J Mol Evol 39:282–295

    Article  CAS  PubMed  Google Scholar 

  • Sautière P, Briand G, Gusse M, Chevaillier Ph (1981) Primary structure of a protamine isolated from the sperm of the dogfishScylliorhinus caniculus. Eur J Biochem 119:251–255

    PubMed  Google Scholar 

  • Sautière P, Gusse M, Briand, Martinage A, Chevaillier Ph. (1984) Primary structure of scylliorhinine S4, a protamine isolated from sperm nuclei of the dogfishScylliorhinus caniculus. Biochim Biophys Acta 791:82–86

    Google Scholar 

  • Sostoa A (1990) Origen i evolució dels grans grups d'agnats i pisciformes gnatostomats. In: Enciclopèdia Catalana (ed) Història Natural dels Països Catalans, vol 11. Peixos, pp 95–110

  • Speckert W, Kennedy B, Daisley StL, Davies P (1983) Primary structure of protamine from the Northern pikeEsox lucius. Eur J Biochem 136:283–289

    Article  CAS  PubMed  Google Scholar 

  • Subirana JA (1975) On the biological role of basic proteins in spermatozoa and during spermiogenesis. In: Duckett JC, Racey PA (eds) The biology of the male gamete. Academic Press, New York, pp 239–244

    Google Scholar 

  • Subirana JA (1983) Nuclear proteins in spermatozoa and their interactions with DNA. In: Andre J (ed) The sperm cell. Martinus Nijhoff, The Hague, pp 197–213

    Google Scholar 

  • Subirana JA, Cozcolluela C, Palau J, Unzeta M (1973) Protamines and other basic proteins from spermatozoa of molluscs. Biochim Biophys Acta 317:364–379

    CAS  Google Scholar 

  • Willmitzer L, Wagner KG (1980) The binding of protamines to DNA; role of protamine phosphorylation. Biophys Struct Mech 6:95–110

    Article  CAS  PubMed  Google Scholar 

  • Yulikova EP, Rybin VK, Silaev AB (1979) The primary structure of stelline A. Bioorg Khim 5:5–10

    CAS  Google Scholar 

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Authors and Affiliations

  1. Departament d'Enginyeria Química, ETSEIB, UPC, Diagonal 647, E-08028, Barcelona, Spain

    Núria Saperas & Manel Chival

  2. Flanders Institute of Biotechnology, Department of Biochemistry, Faculty of Medicine, University of Gent, Ledeganchstraat 35, B-9000, Gent, Belgium

    Carlos Buesa & Jöel Vandekerckhove

  3. Department of Medical Bioanalysis, CID, CSIC, Jordi Girona 18-26, E-08034, Barcelona, Spain

    Joaquin Abián

  4. Department of Zoology, University of British Columbia, V6T 1Z4, Vancouver, BC, Canada

    Harold E. Kasinsky

Authors
  1. Núria Saperas
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  2. Carlos Buesa
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  3. Joaquin Abián
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  4. Jöel Vandekerckhove
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  5. Harold E. Kasinsky
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  6. Manel Chival
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Correspondence to: M. Chiva

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Saperas, N., Buesa, C., Abián, J. et al. The primary structure of a chondrichthyan protamine: A new apparent contradiction in protamine evolution. J Mol Evol 43, 528–535 (1996). https://doi.org/10.1007/BF02337524

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  • DOI: https://doi.org/10.1007/BF02337524

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