The expansion and functional diversification of the mammalian ribonuclease a superfamily epitomizes the efficiency of multigene families at generating biological novelty

Genome Biology and Evolution

Volumn 5, Issue 11, 2013, Pages 2124-2140

  Goo, Stephen M ^a   Cho, Soochin ^a  

^a CREIGHTON UNIVERSITY   (United States)

Author keywords

Adaptive evolution; Angiogenin; Gene duplication; Gene sorting; Host defense; Positive selection

Indexed keywords

ANGIOGENIN; PANCREATIC RIBONUCLEASE; REPETITIVE DNA;

ADAPTIVE EVOLUTION; ANIMAL; ARTICLE; CLASSIFICATION; GENE DUPLICATION; GENE SORTING; GENETIC SELECTION; GENETICS; HOST RESISTANCE; HUMAN; MAMMAL; MOLECULAR EVOLUTION; MULTIGENE FAMILY; PHYLOGENY; POSITIVE SELECTION;

ADAPTIVE EVOLUTION; ANGIOGENIN; GENE DUPLICATION; GENE SORTING; HOST DEFENSE; POSITIVE SELECTION;

ANIMALS; DNA REPEAT EXPANSION; EVOLUTION, MOLECULAR; GENE DUPLICATION; HUMANS; MAMMALS; MULTIGENE FAMILY; PHYLOGENY; RIBONUCLEASE, PANCREATIC; SELECTION, GENETIC;

EID: 84892650593     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evt161     Document Type: Article

References (66)

1. Barclay R. 1982. Night roosting behavior of the little brown bat, Myotis lucifugus. J Mammal. 63:464-474.
2. Barnard EA. 1969. Biological function of pancreatic ribonuclease. Nature 221:340-344.
3. Beintema JJ. 1990. The primary structure of langur (Presbytis entellus) pancreatic ribonuclease: adaptive features in digestive enzymes in mammals. Mol Biol Evol. 7:470-477.
4. Beintema JJ, Kleineidam RG. 1998. The ribonuclease A superfamily: general discussion. Cell Mol Life Sci. 54:825-832.
5. Beintema JJ, Scheffer AJ, van Dijk H, Welling GW, Zwiers H. 1973. Pancreatic ribonuclease distribution and comparisons in mammals. Nat New Biol. 241:76-78.
6. Brown WE, Nobile V, Subramanian V, Shapiro R. 1995. The mouse angiogenin gene family: structures of an angiogenin-related protein gene and two pseudogenes. Genomics 29:200-206.
7. Castella S, et al. 2004. Identification of a member of a new RNase a family specifically secreted by epididymal caput epithelium. Biol Reprod. 70:319-328.
8. Cheng G-Z, Li J-Y, Li F, Wang H-Y, Shi G-X. 2009. Human ribonuclease 9, a member of ribonuclease A superfamily, specifically expressed in epididymis, is a novel sperm-binding protein. Asian J Androl. 11:240-251.
9. Cho S, Beintema JJ, Zhang J. 2005. The ribonuclease A superfamily of mammals and birds: identifying new members and tracing evolutionary histories. Genomics 85:208-220.
10. Cho S, Zhang J. 2006. Ancient expansion of the ribonuclease A superfamily revealed by genomic analysis of placental and marsupial mammals. Gene 373:116-125.
11. Cho S, Zhang J. 2007. Zebrafish ribonucleases are bactericidal: implications for the origin of the vertebrate RNase A superfamily. Mol Biol Evol. 24:1259-1268.
12. Devor EJ, Moffat-Wilson KA, Galbraith JJ. 2004. LOC 390443 (RNase 9) on chromosome 14q11.2 is related to the RNase A superfamily and contains a unique amino-terminal preproteinlike sequence. Hum Biol. 76:921-935.
13. Domachowske JB, Dyer KD, Adams AG, Leto TL, Rosenberg HF. 1998. Eosinophil cationic protein/RNase 3 is another RNase A-family ribonuclease with direct antiviral activity. Nucleic Acids Res. 26:3358-3363.
14. Dubois J-YF, Ursing BM, Kolkman JA, Beintema JJ. 2003. Molecular evolution of mammalian ribonucleases 1. Mol Phylogenet Evol. 27:453-463.
15. Dubois J-YF, et al. 2002. Pancreatic-type ribonuclease 1 gene duplications in rat species. J Mol Evol. 55:522-533.
16. Dyer KD, Rosenberg HF. 2006. The RNase a superfamily: generation of diversity and innate host defense. Mol Divers. 10:585-597.
17. Epstein CJ. 1967. Non-randomness of amino-acid changes in the evolution of homologous proteins. Nature 215:355-359.
18. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
19. Frick WF, et al. 2010. An emerging disease causes regional population collapse of a common North American bat species. Science 329:679-682.
20. Groenen MAM, et al. 2012. Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491:393-398.
21. Gupta SK, Haigh BJ, Griffin FJ, Wheeler TT. 2013. The mammalian secreted RNases: mechanisms of action in host defence. Innate Immun. 19:86-97.
22. Innan H, Kondrashov F. 2010. The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet. 11:97-108.
23. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 16:111-120.
24. Kondrashov FA. 2012. Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc Biol Sci. 279:5048-5057.
25. Krutskikh A, et al. 2012. Epididymal protein Rnase10 is required for posttesticular sperm maturation and male fertility. FASEB J. 26:4198-4209.
26. Kumar S, Hedges SB. 2011. TimeTree2: species divergence times on the iPhone. Bioinformatics 27:2023-2024.
27. Lindblad-Toh K, et al. 2011. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478:476-482.
28. Liu J, et al. 2008. Cloning, expression and location of RNase9 in human epididymis. BMC Res Notes. 1:111.
29. Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R. 2013. Gene duplication as a major force in evolution. J Genet. 92:155-161.
30. Meredith RW, et al. 2011. Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334:521-524.
31. Nei M, Gu X, Sitnikova T. 1997. Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci U S A. 94:7799-7806.
32. Nei M, Kumar S. 2000. Molecular evolution and phylogenetics. New York: Oxford University Press.
33. Nitto T, Dyer KD, Czapiga M, Rosenberg HF. 2006. Evolution and function of leukocyte RNase A ribonucleases of the avian species, Gallus gallus. J Biol Chem. 281:25622-25634.
34. Nitto T, Lin C, Dyer KD, Wagner RA, Rosenberg HF. 2005. Characterization of a ribonuclease gene and encoded protein from the reptile, Iguana iguana. Gene 352:36-44.
35. Ohno S. 1970. Evolution by gene duplication. London: George Alien & Unwin Ltd.
36. Penttinen J, Pujianto DA, Sipila P, Huhtaniemi I, Poutanen M. 2003. Discovery in silico and characterization in vitro of novel genes exclusively expressed in the mouse epididymis. Mol Endocrinol. 17:2138-2151.
37. Pizzo E, et al. 2006. Ribonucleases and angiogenins from fish. J Biol Chem. 281:27454-27460.
38. Pizzo E, et al. 2008. Ribonucleases with angiogenic and bactericidal activities from the Atlantic salmon. FEBS J. 275:1283-1295.
39. Pizzo E, et al. 2011. A new RNase sheds light on the RNase/angiogenin subfamily from zebrafish. Biochem J. 433:345-355.
40. Raines RT. 1998. Ribonuclease A. Chem Rev. 98:1045-1066.
41. Rosenberg HF. 2008a. Eosinophil-derived neurotoxin/RNase 2: connecting the past, the present and the future. Curr Pharm Biotechnol. 9:135-140.
42. Rosenberg HF. 2008b. RNase A ribonucleases and host defense: an evolving story. J Leukoc Biol. 83:1079-1087.
43. Rosenberg HF, Ackerman SJ, Tenen DG. 1989. Human eosinophil cationic protein. Molecular cloning of a cytotoxin and helminthotoxin with ribonuclease activity. J Exp Med. 170:163-176.
44. Rosenberg HF, Dyer KD. 1995. Eosinophil cationic protein and eosinophilderived neurotoxin. Evolution of novel function in a primate ribonuclease gene family. J Biol Chem. 270:21539-21544.
45. Rosenberg HF, Dyer KD. 1996. Molecular cloning and characterization of a novel human ribonuclease (RNase k6): increasing diversity in the enlarging ribonuclease gene family. Nucleic Acids Res. 24:3507-3513.
46. Rosenberg HF, Dyer KD, Tiffany HL, Gonzalez M. 1995. Rapid evolution of a unique family of primate ribonuclease genes. Nat Genet. 10:219-223.
47. Rosenberg HF, Zhang J, Liao YD, Dyer KD. 2001. Rapid diversification of RNase A superfamily ribonucleases from the bullfrog, Rana catesbeiana. J Mol Evol. 53:31-38.
48. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 4:406-425.
49. Scott DT, Duszynski DW. 1997. Eimeria from bats of the world: two new species from Myotis spp. (Chiroptera: Vespertilionidae). J Parasitol. 83:495-501.
50. Sorrentino S. 2010. The eight human "canonical" ribonucleases: molecular diversity, catalytic properties, and special biological actions of the enzyme proteins. FEBS Lett. 584:2194-2200.
51. Tamura K, et al. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28:2731-2739.
52. Tao F, Fan M, Zhao W, Lin Q, Ma R. 2011. A novel cationic ribonuclease with antimicrobial activity from Rana dybowskii. Biochem Genet. 49:369-384.
53. Thompson JD, Gibson TJ, Higgins DG. 2002. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics. Chapter 2: Unit 2.3.
54. Torrent M, Navarro S, Moussaoui M, Nogues MV, Boix E. 2008. Eosinophil cationic protein high-affinity binding to bacteria-wall lipopolysaccharides and peptidoglycans. Biochemistry 47:3544-3555.
55. van den Berg A, Beintema JJ. 1975. Non-constant evolution rates in amino acid sequences of guinea pig, chinchilla and coypu pancreatic ribonucleases. Nature 253:207-210.
56. van den Berg A, Van den Hende-Timmer L, Hofsteenge J, Gaastra W, Beintema JJ. 1977. Guinea-pig pancreatic ribonucleases. Isolation, properties, primary structure and glycosidation. Eur J Biochem. 75:91-100.
57. Warren WC, et al. 2008. Genome analysis of the platypus reveals unique signatures of evolution. Nature 453:175-183.
58. Wheeler TT, Maqbool NJ, Gupta SK. 2012. Mapping, phylogenetic and expression analysis of the RNase (RNaseA) locus in cattle. J Mol Evol. 74:237-248.
59. Xu H, et al. 2013. Multiple bursts of pancreatic ribonuclease gene duplication in insect-eating bats. Gene 526:112-117.
60. Zhang G, et al. 2013. Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339:456-460.
61. Zhang J. 2007. Disulfide-bond reshuffling in the evolution of an ape placental ribonuclease. Mol Biol Evol. 24:505-512.
62. Zhang J, Dyer KD, Rosenberg HF. 2000. Evolution of the rodent eosinophil-associated RNase gene family by rapid gene sorting and positive selection. Proc Natl Acad Sci U S A. 97:4701-4706.
63. Zhang J, Dyer KD, Rosenberg HF. 2002. RNase 8, a novel RNase A superfamily ribonuclease expressed uniquely in placenta. Nucleic Acids Res. 30:1169-1175.
64. Zhang J, Rosenberg HF, Nei M. 1998. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci U S A. 95:3708-3713.
65. Zhao W, et al. 2001. Ruminant brain ribonucleases: expression and evolution. Biochim Biophys Acta. 1547:95-103.
66. Zhu C-F, et al. 2007. RNase9, an androgen-dependent member of the RNase A family, is specifically expressed in the rat epididymis. Biol Reprod. 76:63-73.