Abstract
Phylogenetic analysis, based on the primary structures of mammalian pancreatic-type ribonucleases, indicated that gene duplication events, which occurred during the evolution of ancestral ruminants, gave rise to the three paralogous enzymes present in the bovine species. Herein we report data that demonstrate the existence of the orthologues of the bovine pancreatic, seminal, and cerebral ribonucleases coding sequences in the genomes of giraffe and sheep. The “seminal” sequence is a pseudogene in both species. We also report an analysis of the transcriptional expression of ribonuclease genes in sheep tissues. The data presented support a model for positive selection acting on the molecular evolution of ruminant ribonuclease genes.
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References
Beintema JJ, Schuller C, Irie M, Carsana A (1988) Molecular evolution of the ribonuclease superfamily. Prog Biophys Mol Biol 51:165–192
Blackburn P, Moore S (1982) Pancreatic ribonuclease. In: Boyer PD (ed) The enzymes, vol 15. Academic Press, New York, 317–433
Breukelman HJ, Beintema JJ, Confalone E, Costanzo C, Sasso MP, Carsana A, Palmieri M, Furia A (1993) Sequences related to the ox pancreatic ribonuclease coding region in the genomic DNA of mammalian species. J Mol Evol 37:29–35
Capasso S, Giordano F, Mania CA, Mazzarella L, Zagari A (1983) Refinement of the structure of bovine seminal ribonuclease. Biopolymers 22:327–332
Carsana A, Confalone E, Palmieri M, Libonati M, Furia A (1988) Structure of the bovine pancreatic ribonuclease gene: the unique intervening sequence in the 5′ untranslated region contains a promoter-like element. Nucleic Acids Res 16:5491–5502
Chirgwin SM, Przybyla AE, Mac Donald RS, Rutter W (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294–5299
D'Alessio G, Di Donato A, Parente A, Piccoli R (1991) Seminal RNase: a unique member of the ribonuclease superfamily. Trends Biochem Sci 16:104–106
Farina B, Carsana A, Quesada P, De Prisco R, Leone E (1973) Ribonucleasi di vescichette seminali di bufalo. Boll Soc Ital Biol Sper 49:1450–1455
Fitch WM, Beintema JJ (1990) Correcting parsimonious trees for unseen nucleotide substitutions: the effect of dense branching as exemplified by ribonuclease. Mol Biol Evol 7:438–443
Furia A, Palmieri M, Libonati M (1983) Bovine seminal ribonuclease precursor synthesized in vitro. Biochim Biophys Acta 741:303–307
Gaastra W, Gruen G, Welling GW, Beintema JJ (1974) The primary structure of giraffe pancreatic ribonuclease. FEBS Lett 41:227–233
Jollès J, Jollès P, Bowman BH, Prager EM, Stewart CB, Wilson AC (1989) Episodic evolution in the stomach lysozymes of ruminants. J Mol Evol 28:528–533
Kobayashi R, Hirs CHW (1973) The amino acid sequence of ovine pancreatic ribonuclease A. J Biol Chem 248:7833–7837
Laccetti P, Portella G, Mastronicola MR, Russo A, Piccoli R, D'Alessio G, Vecchio G (1992) In vivo and in vitro growth-inhibitory effect of bovine seminal ribonuclease on a system of rat thyroid epithelial cells and tumors. Cancer Res 52:4582–4586
Maschhoff K, White CL, Jennings LW, Morrison-Bogorad MR (1989) Ribonuclease activities and distribution in Alzheimer's and control brains. J Neurochem 52:1071–1078
Matousek J, Pavlok A, Dostal J, Grozdanovic J (1973a) Some biological properties of bull seminal vesicle aspermatogenic substance and its effect on mice. J Reprod Fertil 34:9–22
Matousek J, Fulka J, Pavlok A (1973b) Effect of ribonuclease fractions isolated from bull seminal vesicle fluid on embryonic mortality in guinea pigs, rabbits and pigs. Int J Fertil 18:13–16
Matousek J, Grozdanovic J (1973c) Specific effect of bull seminal ribonuclease (AS RNase) on cell system in mice. Comp Biochem Physiol 46A:241–248
Mazzarella L, Mattia CA, Capasso S, Di Lorenzo G (1987) Composite active sites in bovine seminal ribonuclease. Gazz Chim Ital 117: 91–97
Mazzarella L, Capasso S, Demasi D, Di Lorenzo G, Mania CA, Zagari A (1993) Bovine Seminal ribonuclease: structure at 1.9 A resolution. Acta Crystallogr D 49:389–402.
Palmieri M, Carsana A, Furia A, Libonati M (1985) Sequence analysis of a cloned cDNA coding for bovine seminal ribonuclease. Eur J Biochem 152:275–277
Preuß KD, Wagner S, Freudenstein J, Scheit KH (1990) Cloning of cDNA encoding the complete precursor for bovine seminal ribonuclease. Nucleic Acids Res 18:1057
Sasso MP, Carsana A, Confalone E, Cosi C, Sorrentino S, Viola M, Palmieri M, Russo E, Furia A (1991) Molecular cloning of the gene encoding the bovine brain ribonuclease and its expression in different regions of the brain. Nucleic Acids Res 19:6469–6474
Schuller C, Nijssen HMJ, Kok R, Beintema JJ (1990) Evolution of nucleic acids coding for ribonucleases: the mRNA sequence of mouse pancreatic ribonuclease. Mol Biol Evol 7:29–44
Shulz-Harder B, Graf v Keyserlingk D (1988) Comparison of brain ribonuclease of rabbit, guinea pig, rat, mouse and gerbil. Histochemistry 88:587–594
Soucek J, Chudomel V, Potmesilova I, Novak J (1986) Effect of ribonucleases on cell-mediated lympholysis reaction and on GM-CFC colonies in bone marrow culture. Nat Immun Cell Growth Regul 5:250–258
Suzuki H, Parente A, Farina B, Greco L, La Montagna R, Leone E (1987) Complete amino-acid sequence of bovine seminal ribonuclease, a dimeric protein from seminal plasma. Biol Chem Hoppe Seyler 368:1305–1312
Tamburrini M, Scala G, Verde C, Ruocco MR, Parente A, Venuta S, D'Alessio G (1990) Immunosuppressive activity of bovine seminal RNase on T-cell proliferation. Eur J Biochem 190:145–148
Vescia S, Tramontano D, Augusti-Tocco G, D'Alessio G (1980) In vitro studies on selective inhibition of tumor cell growth by seminal ribonuclease. Cancer Res 40:3740–3744
Watanabe H, Katoh H, Ishii M, Komoda Y, Sanda A, Takizawa Y, Ohgi K, Irie M (1988) Primary structure of a ribonuclease from bovine brain. J Biochem 104:939–945
Welling GW, Scheffer AJ, Beintema JJ (1974) The primary structure of goat and sheep pancreatic ribonucleases. FEBS Lett 41:58–61
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Correspondence to: A. Furia
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Confalone, E., Beintema, J.J., Sasso, M.P. et al. Molecular evolution of genes encoding ribonucleases in ruminant species. J Mol Evol 41, 850–858 (1995). https://doi.org/10.1007/BF00173164
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DOI: https://doi.org/10.1007/BF00173164