Proteomics and comparative genomic investigations reveal heterogeneity in evolutionary rate of male reproductive proteins in mice (Mus domesticus)

Molecular Biology and Evolution

Volumn 26, Issue 8, 2009, Pages 1733-1743

  Dean, Matthew D ^a   Clark, Nathaniel L ^b,c   Findlay, Geoffrey D ^b   Karn, Robert C ^b   Yi, Xianhua ^b,d   Swanson, Willie J ^b   MacCoss, Michael J ^b   Nachman, Michael W ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Department of Molecular Biology and Genetics   (United States)

^d Momenta Pharmaceuticals Inc   (United States)

Author keywords

Mus; Proteomics; Reproduction

Indexed keywords

ARTICLE; BULBOURETHRAL GLAND; EVOLUTIONARY RATE; GENOMICS; HUMAN; MALE; MALE GENITAL SYSTEM; MOUSE; NONHUMAN; PROSTATE; PROSTATE VENTRAL LOBE; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEOMICS; REPRODUCTION; SEMINAL PLASMA; SEMINAL VESICLE; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY;

ANIMALS; EVOLUTION, MOLECULAR; GENITALIA, MALE; HUMANS; MALE; MICE; PROSTATE; PROTEOMICS; SEMEN; SEMINAL PLASMA PROTEINS; SEMINAL VESICLES;

MAMMALIA; MUS; MUS MUSCULUS DOMESTICUS;

EID: 67749135498     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp094     Document Type: Article

References (101)

1. Aagaard JE, Yi X, MacCoss MJ, Swanson WJ. 2006. Rapidly evolving zona pellucida domain proteins are a major component of the vitelline envelope of abalone eggs. Proc Natl Acad Sci USA. 103:17302-17307.
2. Abbott DE, Pritchard C, Clegg NJ, Ferguson C, Dumpit R, Sikes RA, Nelson PS. 2003. Expressed sequence tag profiling identifies developmental and anatomic partitioning of gene expression in the mouse prostate. Genome Biol. 4:R79.
3. Agrawal Y, Vanha-Perttula T. 1987. Effect of secretory particles in bovine seminal vesicle secretion on sperm motility and acrosome reaction. J Reprod Fertil. 79:409-419.
4. Alghamdi AS, Foster DN. 2005. Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps. Biol Reprod. 73:1174-1181.
5. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Evol. 215:403-410.
6. Anderson DJ, Tarter TH. 1982. Immunosuppressive effects of mouse seminal plasma components in vivo and in vitro. J Immunol. 128:535-539.
7. Ashburner M, Ball CA, Blake JA, et al. (20 co-authors). 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 25:25-29.
8. Baines JF, Harr B. 2007. Reduced X-linked diversity in derived populations of house mice. Genetics. 175:1911-1921.
9. Berquin IM, Min Y, Wu R, Wu H, Chen YQ. 2005. Expression signature of the mouse prostate. J Biol Chem. 280:36442-36451.
10. Carballada R, Esponda P. 1991. Electrophoretic pattern of rodent seminal vesicle proteins as revealed by silver staining. Int J Androl. 14:52-57.
11. Carballada R, Esponda P. 1997. Fate and distribution of seminal plasma proteins in the genital tract of the female rat after natural mating. J Reprod Fertil. 109:325-335.
12. Carballada R, Esponda P. 1998. Binding of seminal vesicle proteins to the plasma membrane of rat spermatozoa in vivo and in vitro. Int J Androl. 21:19-28.
13. Carballada R, Esponda P. 1999. Effect of antibodies against seminal vesicle secretion on fertility in the rat. Zygote. 7:223-231.
14. Carter CS, Schein MW. 1971. Sexual receptivity and exhaustion in the female golden hamster. Horm Behav. 4:191-200.
15. Castillo-Davis CI, Kondrashov FA, Hartl DL, Kulathinal RJ. 2004. The functional genomic distribution of protein divergence in two animal phyla: coevolution, genomic conflict, and constraint. Genome Res. 14:802-811.
16. Clark NL, Aagaard JE, Swanson WJ. 2006. Evolution of reproductive proteins from animals and plants. Reprod Fertil Dev. 131:11-22.
17. Dean MD, Ardlie KG, Nachman MW. 2006. The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol Ecol. 15: 4141-4151.
18. Dean MD, Good JM, Nachman MW. 2008. Adaptive evolution of proteins secreted during sperm maturation: an analysis of the mouse epididymal transcriptome. Mol Biol Evol. 25:383-392.
19. Dean MD, Nachman MW. 2009. Faster fertilization rate in conspecific versus heterospecific matings in house mice. Evolution. 63:20-28.
20. Dixson AF, Anderson MJ. 2002. Sexual selection, seminal coagulation and copulatory plug formation in primates. Folia Primatol. 73:63-69.
21. Dlouhy SR, Nichols WC, Karn RC. 1986. Production of an antibody to mouse salivary androgen binding protein (ABP) and its use in identifying a prostate protein produced by a gene distinct from Abp. Biochem Genet. 24:743-763.
22. Eng JK, McCormack AL, Yates JR. 1994. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectr. 5:976-989.
23. Findlay GD, MacCoss MJ, Swanson WJ. 2009. Proteomic discovery of previously unannotated, rapidly evolving seminal fluid genes in Drosophila. Genome Res. 19:886-896.
24. Findlay GD, Yi X, MacCoss MJ, Swanson WJ. 2008. Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. PLoS Biol. 6:e178.
25. Firman RC, Simmons LW. 2008. The frequency of multiple paternity predicts variation in testes size among island populations of house mice. J Evol Biol.
26. Frazer KA, Eskin E, Kang HM, et al. (16 co-authors). 2007. A sequence-based variation map of 8.27 million SNPs in inbred mouse strains. Nature. 448:1050-1053.
27. Fujimoto N, Akimoto Y, Suzuki T, Kitamura S, Ohta S. 2006. Identification of prostatic-secreted proteins in mice by mass spectrometric analysis and evaluation of lobe-specific and androgen-dependent mRNA expression. J Endocrinol. 190:793-803.
28. Geraldes A, Basset P, Gibson B, Smith KL, Harr B, Yu HT, Bulatova N, Ziv Y, Nachman MW. 2008. Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Mol Ecol. 17: 5349-5363.
29. Gibbs RA, Weinstock GM, Metzker ML, et al. (228 co-authors). 2004. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature. 428:493-521.
30. Goldfoot DA, Goy RW. 1970. Abbreviation of behavioral estrus in guinea pigs by coital and vagino-cervical stimulation. J Comp Physiol Psychol. 72:426-434.
31. Goldman N, Yang Z. 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences: a maximum likelihood approach. J Mol Evol. 40:725-736.
32. Good JM, Handel MA, Nachman MW. 2007. Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution. 62:50-65.
33. Good JM, Nachman MW. 2005. Rates of protein evolution are positively correlated with developmental timing of expression during mouse spermatogenesis. Mol Biol Evol. 22: 1044-1052.
34. Hardy DF, DeBold JF. 1972. Effects of coital stimulation upon behavior of the female rat. J Comp Physiol Psychol. 78:400-408.
35. Hartung TG, Dewsbury DA. 1978. A comparative analysis of copulatory plugs in muroid rodents and their relationship to copulatory behavior. J Mammalogy. 59:717-723.
36. Hayashi N, Sugimura Y, Kawamura J, Donjacour AA, Cunha GR. 1991. Morphological and functional heterogeneity in the rat prostatic gland. Biol Reprod. 45:308-321.
37. Henault MA, Killian GJ, Kavanaugh JF, Griel LC Jr. 1995. Effect of accessory sex gland fluid from bulls of differing fertilities on the ability of cauda epididymal sperm to penetrate zona-free bovine oocytes. Biol Reprod. 52:390-397.
38. Huang YH, Chu ST, Chen YH. 2000. A seminal vesicle autoantigen of mouse is able to suppress sperm capacitation-related events stimulated by serum albumin. Biol Reprod. 63:1562-1566.
39. Hurle B, Swanson W, Green ED. 2007. Comparative sequence analyses reveal rapid and divergent evolutionary changes of the WFDC locus in the primate lineage. Genome Res. 17: 276-286.
40. Irwin M, Nicholson N, Haywood JT, Poirier GR. 1983. Immunofluorescent localization of a murine seminal vesicle proteinase inhibitor. Biol Reprod. 28:1201-1206.
41. Jelinsky SA, Turner TT, Bang HJ, Finger JN, Solarz MK, Wilson E, Brown EL, Kopf GS, Johnston DS. 2007. The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides. Biol Reprod. 76:561-570.
42. Johnston DS, Jelinsky SA, Bang HJ, Dicandeloro P, Wilson E, Kopf GS, Turner TT. 2005. The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol Reprod. 73:404-413.
43. Karn RC, Clark NL, Nguyen ED, Swanson WJ. 2008. Adaptive evolution in rodent seminal vesicle secretion proteins. Mol Biol Evol. 25:2301-2310.
44. Karn RC, Laukaitis CM. 2003. Characterization of two forms of mouse salivary androgen-binding protein (ABP): implications for evolutionary relationships and ligand-binding function. Biochemistry. 42:7162-7170.
45. Kawano N, Yoshida M. 2007. Semen-coagulating protein, SVS2, in mouse seminal plasma controls sperm fertility. Biol Reprod. 76:353-361.
46. Kelleher ES, Swanson WJ, Markow TA. 2007. Gene duplication and adaptive evolution of digestive proteases in Drosophila arizonae female reproductive tracts. PLoS Genet. 3:e148.
47. Kent WJ. 2002. BLAT - the BLAST-like alignment tool. Genome Res. 12:656-664.
48. Klammer AA, Wu CC, MacCoss MJ, Noble WS. 2005. Peptide charge state determination for low-resolution tandem mass spectra. Proc IEEE Comput Syst Bioinform Conf. 175-185.
49. Kosakovsky Pond SL, Frost SDW. 2005. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol. 22:1208-1222.
50. Kosakovsky Pond SL, Frost SDW, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics. 21:676-679.
51. Laukaitis CM, Dlouhy SR, Emes RD, Ponting CP, Karn RC. 2005. Diverse spatial, temporal, and sexual expression of recently duplicated androgen-binding protein genes in Mus musculus. BMC Evol Biol. 5:40.
52. Lawniczak MKN, Begun DJ. 2007. Molecular population genetics of female-expressed mating-induced serine proteases in Drosophila melanogaster. Mol Biol Evol. 24: 1944-1951.
53. Lilja H. 1985. A kallikrein-like serine protease in prostatic fluid cleaves the predominant seminal vesicle protein. J Clin Invest. 76:1899-1903.
54. Lin H-J, Luo C-W, Chen Y-H. 2002. Localization of the transglutaminase cross-linking site in SVS III, a novel glycoprotein secreted from mouse seminal vesicle. J Biol Chem. 277:3632-3639.
55. Liu H, Sadygov RG, Yates JR 3rd. 2004. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem. 76:4193-4201.
56. Lundwall A, Clauss A, Olsson AY. 2006. Evolution of kallikrein-related peptidases in mammals and identification of a genetic locus encoding potential regulatory inhibitors. Biol Chem. 387:243-249.
57. Lundwall A, Peter , JLovgren , H Lilja , J Malm . 1997. Chemical characterization of the predominant proteins secreted by mouse seminal vesicles. Eur J Biochem. 249:39-44.
58. Mann T, Lutwak-Mann C. 1981. Male reproductive function and semen. New York: Springer-Verlag.
59. Mueller JL, Ravi Ram K, McGraw LA, Bloch Qazi MC, Siggia ED, Clark AG, Aquadro CF, Wolfner MF. 2005. Cross-species comparison of Drosophila male accessory gland protein genes. Genetics. 171:131-143.
60. Nagy A, Gertsenstein M, Vintersten K, Behringer R. 2003. Manipulating the mouse embryo. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
61. Nei M, Li W-H. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA. 76:5269-5273.
62. Nielsen R, Bustamante C, Clark AG, et al. (13 co-authors). 2005. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol. 3:e170.
63. O WS, Chen HQ, Chow PH. 1988. Effects of male accessory sex gland secretions on early embryonic development in the golden hamster. J Reprod Fertil. 84:341-344.
64. Pang SF, Chow PH, Wong TM. 1979. The role of the seminal vesicles, coagulating glands and prostate glands on the fertility and fecundity of mice. J Reprod Fertil. 56:129-132.
65. Panhuis TM, Swanson WJ. 2006. Molecular evolution and population genetic analysis of candidate female reproductive genes in Drosophila. Genetics. 173:2039-2047.
66. Peitz B. 1988. Effects of seminal vesicle fluid components on sperm motility in the house mouse. J Reprod Fertil. 83:169-176.
67. Peitz B, Bennett D. 1981. Inhibition of complement-mediated cytotoxicity of antisera by fluid secreted by the seminal vesicle of the house mouse. J Reprod Immunol. 3:109-116.
68. Peitz B, Olds-Clarke P. 1986. Effects of seminal vesicle removal on fertility and uterine sperm motility in the house mouse. Biol Reprod. 35:608-617.
69. Pilch B, Mann M. 2006. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol. 7:R40.
70. Platz RD, Wolfe HG. 1969. Mouse seminal vesicle proteins. The inheritance of electrophoretic variants. J Hered. 60:187-192.
71. Price TAR, Hodgson DJ, Lewis Z, Hurst GDD, Wedell N. 2008. Selfish genetic elements promote polyandry in a fly. Science. 322:1241-1243.
72. Prout T, Clark AG. 2000. Seminal fluid causes temporarily reduced egg hatch in previously mated females. Proc Roy Soc Lond B Biol Sci. 267:201-203.
73. Queen K, Dhabuwala CB, Pierrepoint CG. 1981. The effect of the removal of the various accessory sex glands on the fertility of male rats. J Reprod Fertil. 62:423-426.
74. Ramm SA, Oliver PL, Ponting CP, Stockley P, Emes RD. 2008. Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Mol Biol Evol. 25:207-219.
75. Ramm SA, Parker GA, Stockley P. 2005. Sperm competition and the evolution of male reproductive anatomy in rodents. Proc Biol Sci. 272:949-955.
76. Rice WR. 1984. Sex chromosomes and the evolution of sexual dimorphism. Evolution. 38:735-742.
77. Robinson PN, Wollstein A, Bohme U, Beattie B. 2004. Ontologizing gene-expression microarray data: characterizing clusters with gene ontology. Bioinformatics. 20:979-981.
78. Robinson R, Richardson R, Hinds K, Clayton D, Poirier GR. 1987. Features of a seminal proteinase inhibitor-zona pellucida binding component on murine spermatozoa. Gamete Res. 16:217-228.
79. Schmidt JA, Oatley JM, Brinster RL. 2009. Female mice delay reproductive aging in males. Biol Reprod. 80:1009-1014.
80. Shivaji S, Scheit K-H, Bhargava PM. 1990. Proteins of seminal plasma. New York: John Wiley & Sons.
81. Silver L. 1995. Mouse genetics: concepts and applications. New York: Oxford University Press.
82. Snyder RL. 1966. Collection of mouse semen by electroejaculation. Anat Rec. 155:11-14.
83. Snyder RL. 1967. Fertility and reproductive performance of grouped male mice. In: Benirschke K, editor. Comparative aspects of reproductive failure. New York: Springer-Verlag. p. 458-472.
84. Su AI, Cooke MP, Ching KA, et al. (14 co-authors). 2002. Large-scale analysis of the human and mouse transcriptomes. Proc Natl Acad Sci USA. 99:4465-4470.
85. Swanson WJ, Nielsen R, Yang Q. 2003. Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol. 20:18-20.
86. Swanson WJ, Wong A, Wolfner MF, Aquadro CF. 2004. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics. 168:1457-1465.
87. Swofford DL. 2002. PAUP*. Sinaeur Associates, Sunderland, Massachusetts.
88. Tabb DL, McDonald WH, Yates JR 3rd. 2002. DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res. 1:21-26.
89. Tecirlioglu RT, Hayes ES, Trounson AO. 2002. Semen collection from mice: electroejaculation. Reprod Fertil Dev. 14:363-371.
90. Thaler CJ. 1989. Immunological role for seminal plasma in insemination and pregnancy. Am J Reprod Immunol. 21:147-150.
91. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
92. Turner LM, Chuong EB, Hoekstra HE. 2008. Comparative analysis of testis protein evolution in rodents. Genetics. 179:2075-2089.
93. Vicoso B, Charlesworth B. 2006. Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet. 7:645-653.
94. Wade CM, Kulbokas EJ 3rd, Kirby AW, Zody MC, Mullikin JC, Lander ES, Lindblad-Toh K, Daly MJ. 2002. The mosaic structure of variation in the laboratory mouse genome. Nature. 420:574-578.
95. Wartha F, Beiter K, Normark S, Henriques-Normark B. 2007. Neutrophil extracellular traps: casting the NET over pathogenesis. Curr Opin Microbiol. 10:52-56.
96. Waterston RH, Lindblad-Toh K, Birney E, et al. (222 coauthors). 2002. Initial sequencing and comparative analysis of the mouse genome. Nature. 420:520-562.
97. Wernersson R, Pedersen AG. 2003. RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res. 31:3537-3539.
98. Wong A, Albright SN, Giebel JD, Ram KR, Ji S, Fiumera AC, Wolfner MF. 2008. A role for Acp29AB, a predicted seminal fluid lectin, in female sperm storage in Drosophila melanogaster. Genetics. 180:921-931.
99. Yang H, Bell TA, Churchill GA, Pardo-Manuel de Villena F. 2007. On the subspecific origin of the laboratory mouse. Nat Genet. 39:1100-1107.
100. Yang Z. 1997. PAML, a program package for phylogenetic analysis by maximum likelihood. CABIOS. 13:555-556.
101. Yang Z, Nielsen R, Goldman N, Pedersen A-MK. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics. 155:431-449.