Home LiteratureArticle Details
PMID: 20080865 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Sperm proteomics reveals intensified selection on mouse sperm membrane and acrosome genes.

Molecular biology and evolution ·Vol. 27 ·No. 6 ·2010-06-00 ·Pages 1235-46

Dorus S, Wasbrough ER, Busby J, Wilkin EC, Karr TL

Abstract

Spermatozoa are a focal point for the impact of sexual selection due to sperm competition and sperm-female interactions in a wide range of sexually reproducing organisms. In-depth molecular investigation of the ramifications of these selective regimes has been limited due to a lack of information concerning the molecular composition of sperm. In this study, we utilize three previously published proteomic data sets in conjunction with our whole mouse sperm proteomic analysis to delineate cellular regions of sperm most impacted by positive selection. Interspecific analysis reveals robust evolutionary acceleration of sperm cell membrane genes (which include genes encoding acrosomal and sperm cell surface proteins) relative to other sperm genes, and evidence for positive selection in approximately 22% of sperm cell membrane components was obtained using maximum likelihood models. The selective forces driving the accelerated evolution of these membrane proteins may occur at a number of locations during sperm development, maturation, and transit through the female reproductive tract where the sperm cell membrane and eventually the acrosome are exposed to the extracellular milieu and available for direct cell-cell interactions.

MeSH Terms
Acrosome/metabolism Animals Chromatography, High Pressure Liquid Databases, Protein Evolution, Molecular Male Membrane Proteins/genetics Mice Mice, Inbred BALB C Models, Statistical Organ Specificity Phenotype Proteome/genetics Proteomics/methods Spermatozoa/metabolism,physiology Statistics, Nonparametric Testis/metabolism
Chemicals
Membrane Proteins Proteome
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Dorus Steve
Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom.
Wasbrough Elizabeth R
Busby Jennifer
Wilkin Elaine C
Karr Timothy L
References (69)
69 references, click to expand
  1. Molecular population genetics of the gene encoding the human fertilization protein zonadhesin reveals rapid adaptive evolution.
    Am J Hum Genet. 2006 Nov;79(5):820-30 PMID: 17033959
  2. Galactosyltransferase function during mammalian fertilization.
    Cells Tissues Organs. 2001;168(1-2):46-57 PMID: 11114586
  3. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search.
    Anal Chem. 2002 Oct 15;74(20):5383-92 PMID: 12403597
  4. Molecular models for murine sperm-egg binding.
    J Biol Chem. 2006 May 19;281(20):13853-6 PMID: 16455664
  5. The seminal fluid proteome of the honeybee Apis mellifera.
    Proteomics. 2009 Apr;9(8):2085-97 PMID: 19322787
  6. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals.
    Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2509-14 PMID: 11226269
  7. SPEED: a molecular-evolution-based database of mammalian orthologous groups.
    Bioinformatics. 2006 Nov 15;22(22):2835-7 PMID: 16966361
  8. Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate.
    Mol Biol Evol. 2000 Jan;17(1):68-74 PMID: 10666707
  9. Proteomic analysis of sperm regions that mediate sperm-egg interactions.
    Proteomics. 2006 Jun;6(12):3533-43 PMID: 16758446
  10. Adaptive evolution in rodent seminal vesicle secretion proteins.
    Mol Biol Evol. 2008 Nov;25(11):2301-10 PMID: 18718917
  11. The mouse sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identification.
    Proteomics. 2008 Apr;8(8):1720-30 PMID: 18340633
  12. Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins.
    Evolution. 2003 May;57(5):1049-60 PMID: 12836822
  13. Rapid evolution of male reproductive genes in the descent of man.
    Nature. 2000 Jan 20;403(6767):304-9 PMID: 10659848
  14. Dynamic evolution of the innate immune system in Drosophila.
    Nat Genet. 2007 Dec;39(12):1461-8 PMID: 17987029
  15. Natural selection drives Drosophila immune system evolution.
    Genetics. 2003 Aug;164(4):1471-80 PMID: 12930753
  16. Adaptive evolution of proteins secreted during sperm maturation: an analysis of the mouse epididymal transcriptome.
    Mol Biol Evol. 2008 Feb;25(2):383-92 PMID: 18056076
  17. The rapid evolution of reproductive proteins.
    Nat Rev Genet. 2002 Feb;3(2):137-44 PMID: 11836507
  18. Positive selection in the egg receptor for abalone sperm lysin.
    Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4639-43 PMID: 12676995
  19. Toward a comprehensive genetic analysis of male fertility in Drosophila melanogaster.
    Genetics. 2004 May;167(1):207-16 PMID: 15166148
  20. Inhibition of acrosin by serpins. A suicide substrate mechanism.
    Biochemistry. 1995 Mar 21;34(11):3678-85 PMID: 7893664
  21. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites.
    Genetics. 2004 Oct;168(2):1041-51 PMID: 15514074
  22. Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes.
    J Theor Biol. 1982 May 21;96(2):281-94 PMID: 7121030
  23. Mouse models of male infertility.
    Nat Rev Genet. 2002 Oct;3(10):790-801 PMID: 12360237
  24. Pervasive adaptive evolution in mammalian fertilization proteins.
    Mol Biol Evol. 2003 Jan;20(1):18-20 PMID: 12519901
  25. Mammalian sperm proteins are rapidly evolving: evidence of positive selection in functionally diverse genes.
    Mol Biol Evol. 2002 Nov;19(11):1973-80 PMID: 12411606
  26. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages.
    Mol Biol Evol. 2002 Jun;19(6):908-17 PMID: 12032247
  27. The ADAMs family of metalloproteases: multidomain proteins with multiple functions.
    Genes Dev. 2003 Jan 1;17(1):7-30 PMID: 12514095
  28. Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding.
    Nature. 1992 Jun 18;357(6379):589-93 PMID: 1608469
  29. ADAMs: modulators of cell-cell and cell-matrix interactions.
    Curr Opin Cell Biol. 2003 Oct;15(5):598-606 PMID: 14519395
  30. Analysis of mouse fertilin in wild-type and fertilin beta(-/-) sperm: evidence for C-terminal modification, alpha/beta dimerization, and lack of essential role of fertilin alpha in sperm-egg fusion.
    Dev Biol. 2000 Jun 15;222(2):289-95 PMID: 10837118
  31. Complement and complement regulators in the male reproductive system.
    Mol Immunol. 2006 Jan;43(1-2):57-67 PMID: 16023728
  32. Rapid evolution of genomic Acp complement in the melanogaster subgroup of Drosophila.
    Mol Biol Evol. 2005 Oct;22(10):2010-21 PMID: 15987879
  33. A gene atlas of the mouse and human protein-encoding transcriptomes.
    Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):6062-7 PMID: 15075390
  34. The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs.
    Nature. 2005 Mar 10;434(7030):234-8 PMID: 15759005
  35. Polymorphism in abalone fertilization proteins is consistent with the neutral evolution of the egg's receptor for lysin (VERL) and positive darwinian selection of sperm lysin.
    Mol Biol Evol. 2001 Mar;18(3):376-83 PMID: 11230538
  36. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.
    Nat Genet. 2000 May;25(1):25-9 PMID: 10802651
  37. PAML 4: phylogenetic analysis by maximum likelihood.
    Mol Biol Evol. 2007 Aug;24(8):1586-91 PMID: 17483113
  38. Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating.
    PLoS Biol. 2008 Jul 29;6(7):e178 PMID: 18666829
  39. Human sperm-egg binding is inhibited by peptides corresponding to core region of an acrosomal serine protease inhibitor.
    Mol Reprod Dev. 1993 Mar;34(3):280-91 PMID: 8471250
  40. The molecular players of sperm-egg fusion in mammals.
    Semin Cell Dev Biol. 2006 Apr;17(2):254-63 PMID: 16574441
  41. Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae.
    Nat Biotechnol. 2002 Mar;20(3):301-5 PMID: 11875433
  42. The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus).
    Mol Ecol. 2006 Nov;15(13):4141-51 PMID: 17054508
  43. Sexual selection and the adaptive evolution of mammalian ejaculate proteins.
    Mol Biol Evol. 2008 Jan;25(1):207-19 PMID: 18032407
  44. Functional diversification of a protease inhibitor gene in the genus Drosophila and its molecular basis.
    Gene. 2008 May 31;415(1-2):23-31 PMID: 18395367
  45. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.
    Mol Biol Evol. 1986 Sep;3(5):418-26 PMID: 3444411
  46. Genomic and functional evolution of the Drosophila melanogaster sperm proteome.
    Nat Genet. 2006 Dec;38(12):1440-5 PMID: 17099714
  47. Sperm competition enhances functional capacity of mammalian spermatozoa.
    Proc Natl Acad Sci U S A. 2006 Oct 10;103(41):15113-7 PMID: 16990431
  48. High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species.
    J Mol Evol. 1995 Dec;41(6):1085-95 PMID: 8587107
  49. Positive selection at reproductive ADAM genes with potential intercellular binding activity.
    Mol Biol Evol. 2004 May;21(5):851-9 PMID: 14963094
  50. The rat sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identification.
    Proteomics. 2008 Jun;8(11):2312-21 PMID: 18528845
  51. Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity.
    Nat Genet. 2004 Dec;36(12):1326-9 PMID: 15531881
  52. Functional processing of fertilin: evidence for a critical role of proteolysis in sperm maturation and activation.
    Rev Reprod. 2000 May;5(2):75-83 PMID: 10864851
  53. Comprehensive analysis of reproductive ADAMs: relationship of ADAM4 and ADAM6 with an ADAM complex required for fertilization in mice.
    Biol Reprod. 2009 May;80(5):1001-8 PMID: 19129510
  54. PAML: a program package for phylogenetic analysis by maximum likelihood.
    Comput Appl Biosci. 1997 Oct;13(5):555-6 PMID: 9367129
  55. Proteomics and comparative genomic investigations reveal heterogeneity in evolutionary rate of male reproductive proteins in mice (Mus domesticus).
    Mol Biol Evol. 2009 Aug;26(8):1733-43 PMID: 19420050
  56. The role of X-chromosome inactivation during spermatogenesis (Drosophila-allocycly-chromosome evolution-male sterility-dosage compensation).
    Proc Natl Acad Sci U S A. 1972 Jan;69(1):182-6 PMID: 4621547
  57. Positive selection within sperm-egg adhesion domains of fertilin: an ADAM gene with a potential role in fertilization.
    Mol Biol Evol. 2003 Jan;20(1):21-9 PMID: 12519902
  58. Recent origins of sperm genes in Drosophila.
    Mol Biol Evol. 2008 Oct;25(10):2157-66 PMID: 18653731
  59. Genome sequence of the Brown Norway rat yields insights into mammalian evolution.
    Nature. 2004 Apr 1;428(6982):493-521 PMID: 15057822
  60. Protein-carbohydrate complementarity in mammalian gamete recognition.
    Gamete Res. 1988 May;20(1):93-109 PMID: 2853128
  61. Proteomic profiling of accessory structures from the mouse sperm flagellum.
    Mol Cell Proteomics. 2006 May;5(5):801-10 PMID: 16452089
  62. Sperm guidance in mammals - an unpaved road to the egg.
    Nat Rev Mol Cell Biol. 2006 Apr;7(4):276-85 PMID: 16607290
  63. Evolutionary history of the sex-peptide (Acp70A) gene region in Drosophila melanogaster.
    Genetics. 1997 Sep;147(1):189-97 PMID: 9286679
  64. Speciation and the evolution of gamete recognition genes: pattern and process.
    Heredity (Edinb). 2009 Jan;102(1):66-76 PMID: 19018273
  65. Disruption of mouse CD46 causes an accelerated spontaneous acrosome reaction in sperm.
    Mol Cell Biol. 2003 Apr;23(7):2614-22 PMID: 12640142
  66. Pervasive adaptive evolution in primate seminal proteins.
    PLoS Genet. 2005 Sep;1(3):e35 PMID: 16170411
  67. The molecular basis of sperm-oocyte membrane interactions during mammalian fertilization.
    Hum Reprod Update. 2002 Jul-Aug;8(4):297-311 PMID: 12206465
  68. Functionally active protein C inhibitor/plasminogen activator inhibitor-3 (PCI/PAI-3) is secreted in seminal vesicles, occurs at high concentrations in human seminal plasma and complexes with prostate-specific antigen.
    Thromb Res. 1991 Nov 1;64(3):309-20 PMID: 1725227
  69. Maximum-likelihood analysis of molecular adaptation in abalone sperm lysin reveals variable selective pressures among lineages and sites.
    Mol Biol Evol. 2000 Oct;17(10):1446-55 PMID: 11018152
Article Info
Journal
Molecular biology and evolution
Abbr.
Mol Biol Evol
ISSN
1537-1719
Published
2010-06-00
Epub
2010-00-15
Pages
1235-46
Language
English
Region
United States
NLM ID
8501455
PMCID
PMC2877994
Subset
IM
Grants
NIGMS NIH HHS · F32 GM076913 · United States
NIGMS NIH HHS · F32GM076913-03 · United States
Biotechnology and Biological Sciences Research Council · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]