Evolutionary conservation of mammalian sperm proteins associates with overall, not tyrosine, phosphorylation in human spermatozoa

Journal of Proteome Research

Volumn 12, Issue 12, 2013, Pages 5370-5382

  Schumacher, Julia ^a   Ramljak, Sanja ^b   Asif, Abdul R ^c   Schaffrath, Michael ^a   Zischler, Hans ^a   Herlyn, Holger ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b Institute for Clinical Research IKFE   (Germany)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

2DE; dN dS; evolution; fertility; functional constraint; mass spectrometry; phosphorylation; primates; selection; spermatozoa

Indexed keywords

AMINO ACID; PHOSPHOPROTEIN; SERINE; THREONINE; TYROSINE;

ADULT; AMINO ACID SEQUENCE; ARTICLE; CORRELATION ANALYSIS; GENETIC CONSERVATION; HUMAN; HUMAN EXPERIMENT; IMMUNOBLOTTING; MALE; MASS SPECTROMETRY; NONHUMAN; NORMAL HUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SPERM; SPERMATOZOON; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE; TWO DIMENSIONAL GEL ELECTROPHORESIS; ANIMAL; FERTILITY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PROTEIN PROCESSING; SEQUENCE HOMOLOGY; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; CONSERVED SEQUENCE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EVOLUTION, MOLECULAR; FERTILITY; GENE EXPRESSION REGULATION; HUMANS; MALE; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE HOMOLOGY, AMINO ACID; SERINE; SPERMATOZOA; THREONINE; TYROSINE;

EID: 84890053597     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400228c     Document Type: Article

References (83)

1. Cohen, P. The regulation of protein function by multisite phosphorylation-A 25 year update Trends Biochem. Sci. 2000, 25 (12) 596-601
2. Mann, M.; Ong, S. E.; Grønborg, M.; Steen, H.; Jensen, O. N.; Pandey, A. Analysis of protein phosphorylation using mass spectrometry: Deciphering the phosphoproteome Trends Biotechnol. 2002, 20 (6) 261-268
3. de Lichtenberg, U.; Jensen, L. J.; Brunak, S.; Bork, P. Dynamic complex formation during the yeast cell cycle Science 2005, 307 (5710) 724-727
4. Cieśla, J.; FraÌ̈czyk, T.; Rode, W. Phosphorylation of basic amino acid residues in proteins: Important but easily missed Acta Biochim. Pol. 2011, 58 (2) 137-147
5. Law, L. J.; Ilkow, C. S.; Tzeng, W. P.; Rawluk, M.; Stuart, D. T.; Frey, T. K.; Hobman, T. C. Analyses of phosphorylation events in the rubella virus capsid protein: Role in early replication events J. Virol. 2006, 80 (14) 6917-6925
6. Macek, B.; Gnad, F.; Soufi, B.; Kumar, C.; Olsen, J. V.; Mijakovic, I.; Mann, M. Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation Mol. Cell. Proteomics 2008, 7 (2) 299-307
7. Hunter, T. Tyrosine phosphorylation: Thirty years and counting Curr. Opin. Cell Biol. 2009, 21 (2) 140-146
8. Lienhard, G. E. Non-functional phosphorylations? Trends Biochem. Sci. 2008, 33 (8) 351-352
9. Visconti, P. E.; Bailey, J. L.; Moore, G. D.; Pan, D.; Olds-Clarke, P.; Kopf, G. S. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation Development 1995, 121 (4) 1129-1137
10. Ficarro, S.; Chertihin, O.; Westbrook, V. A.; White, F.; Jayes, F.; Kalab, P.; Marto, J. A.; Shabanowitz, J.; Herr, J. C.; Hunt, D. F.; Visconti, P. E. Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation J. Biol. Chem. 2003, 278 (13) 11579-11589
11. Sidhu, K. S.; Mate, K. E.; Gunasekera, T.; Veal, D.; Hetherington, L.; Baker, M. A.; Aitken, R. J.; Rodger, J. C. A flow cytometric assay for global estimation of tyrosine phosphorylation associated with capacitation of spermatozoa from two marsupial species, the tammar wallaby (Macropus eugenii) and the brushtail possum (Trichosurus vulpecula) Reproduction 2004, 127 (1) 95-103
12. Baker, M. A.; Smith, N. D.; Hetherington, L.; Taubman, K.; Graham, M. E.; Robinson, P. J.; Aitken, R. J. Label-free quantitation of phosphopeptide changes during rat sperm capacitation J. Proteome Res. 2009, 9 (2) 718-729
13. Kota, V.; Dhople, V. M.; Shivaji, S. Tyrosine phosphoproteome of hamster spermatozoa: Role of glycerol-3-phosphate dehydrogenase 2 in sperm capacitation Proteomics 2009, 9 (7) 1809-1826
14. Platt, M. D.; Salicioni, A. M.; Hunt, D. F.; Visconti, P. E. Use of differential isotopic labeling and mass spectrometry to analyze capacitation-associated changes in the phosphorylation status of mouse sperm proteins J. Proteome Res. 2009, 8 (3) 1431-1440
15. Fàbrega, A.; Puigmulé, M.; Yeste, M.; Casas, I.; Bonet, S.; Pinart, E. Impact of epididymal maturation, ejaculation and in vitro capacitation on tyrosine phosphorylation patterns exhibited of boar (Sus domesticus) spermatozoa Theriogenology 2011, 76 (7) 1356-1366
16. Horowitz, J. A.; Toeg, H.; Orr, G. A. Characterization and localization of cAMP-dependent protein kinases in rat caudal epididymal sperm J. Biol. Chem. 1984, 259 (2) 832-838
17. Vijayaraghavan, S.; Goueli, S. A.; Davey, M. P.; Carr, D. W. Protein kinase A-anchoring inhibitor peptides arrest mammalian sperm motility J. Biol. Chem. 1997, 272 (8) 4747-4752
18. González-Fernández, L.; Ortega-Ferrusola, C.; Macias-Garcia, B.; Salido, G. M.; Peña, F. J.; Tapia, J. A. Identification of protein tyrosine phosphatases and dual-specificity phosphatases in mammalian spermatozoa and their role in sperm motility and protein tyrosine phosphorylation Biol. Reprod. 2009, 80 (6) 1239-1252
19. Moos, J.; Pěknicová, J.; Geussova, G.; Philimonenko, V.; Hozák, P. Association of protein kinase A type I with detergent-resistant structures of mammalian sperm cells Mol. Reprod. Dev. 1998, 50 (1) 79-85
20. Si, Y.; Okuno, M. Regulation of microtubule sliding by a 36-kDa phosphoprotein in hamster sperm flagella Mol. Reprod. Dev. 1999, 52 (3) 328-334
21. Chan, C. C.; Shui, H. A.; Wu, C. H.; Wang, C. Y.; Sun, G. H.; Chen, H. M.; Wu, G. J. Motility and protein phosphorylation in healthy and asthenozoospermic sperm J. Proteome Res. 2009, 8 (11) 5382-5386
22. E) reveals altered proteomic signatures in asthenozoospermia J. Proteomics 2012, 75 (18) 5861-5871
23. Buffone, M. G.; Calamera, J. C.; Verstraeten, S. V.; Doncel, G. F. Capacitation-associated protein tyrosine phosphorylation and membrane fluidity changes are impaired in the spermatozoa of asthenozoospermic patients Reproduction 2005, 129 (6) 697-705
24. Yunes, R.; Fernández, P.; Doncel, G. F.; Acosta, A. A. Cyclic nucleotide phosphodiesterase inhibition increases tyrosine phosphorylation and hyper motility in normal and pathological human spermatozoa Biocell 2005, 29 (3) 287-293
25. Naz, R. K.; Rajesh, P. B. Role of tyrosine phosphorylation in sperm capacitation/acrosome reaction Reprod. Biol. Endocrinol. 2004, 2, 75
26. Ubersax, J. A.; Ferrell, J. E. Mechanisms of specificity in protein phosphorylation Nat. Rev. Mol. Cell Biol. 2007, 8 (7) 530-541
27. Manning, G.; Plowman, G. D.; Hunter, T.; Sudarsanam, S. Evolution of protein kinase signaling from yeast to man Trends Biochem. Sci. 2002, 27 (10) 514-520
28. Boekhorst, J.; van Breukelen, B.; Heck, A. J. R.; Snel, B. Comparative phosphoproteomics reveals evolutionary and functional conservation of phosphorylation across eukaryotes Genome Biol. 2008, 9 (10) R144
29. Malik, R.; Nigg, E. A.; Körner, R. Comparative conservation analysis of the human mitotic phosphoproteome Bioinformatics 2008, 24 (12) 1426-1432
30. Chen, S. C.; Chen, F. C.; Li, W. H. Phosphorylated and nonphosphorylated serine and threonine residues evolve at different rates in mammals Mol. Biol. Evol. 2010, 27 (11) 2548-2554
31. Gnad, F.; Forner, F.; Zielinska, D. F.; Birney, E.; Gunawardena, J.; Mann, M. Evolutionary constraints of phosphorylation in eukaryotes, prokaryotes, and mitochondria Mol. Cell. Proteomics 2010, 9 (12) 2642-2653
32. Nguyen, B. A. N.; Moses, A. M. Evolution of characterized phosphorylation sites in budding yeast Mol. Biol. Evol. 2010, 27 (9) 2027-2037
33. Gray, V. E.; Kumar, S. Rampant purifying selection conserves positions with posttranslational modifications in human proteins Mol. Biol. Evol. 2011, 28 (5) 1565-1568
34. Vener, A. V. Protein phosphorylation: A motive force for adaptive evolution BioSystems 1990, 24 (1) 53-59
35. Tan, C. S.; Pasculescu, A.; Lim, W. A.; Pawson, T.; Bader, G. D.; Linding, R. Positive selection of tyrosine loss in metazoan evolution Science 2009, 325 (5948) 1686-1688
36. Kaganovich, M.; Snyder, M. Phosphorylation of yeast transcription factors correlates with the evolution of novel sequence and function J. Proteome Res. 2012, 11 (1) 261-268
37. Amoutzias, G. D.; He, Y.; Gordon, J.; Mossialos, D.; Oliver, S. G.; Van de Peer, Y. Posttranslational regulation impacts the fate of duplicated genes Proc. Natl. Acad. Sci. U.S.A. 2010, 107 (7) 2967-2971
38. Huyck, L.; Van Troys, M.; Ampe, C. Phosphosite conservation in single domain orthologs versus paralogs: A way to combine differential regulation with redundant core functions FEBS Lett. 2012, 586 (4) 296-302
39. de Oliveira, T.; Salemi, M.; Gordon, M.; Vandamme, A. M.; van Rensburg, E. J.; Engelbrecht, S.; Coovadia, H. M.; Cassol, S. Mapping sites of positive selection and amino acid diversification in the HIV genome: An alternative approach to vaccine design? Genetics 2004, 167 (3) 1047-1058
40. Seet, B. T.; Dikic, I.; Zhou, M. M.; Pawson, T. Reading protein modifications with interaction domains Nat. Rev. Mol. Cell Biol. 2006, 7 (7) 473-483
41. Herlyn, H.; Zischler, H. The molecular evolution of sperm zonadhesin Int. J. Dev. Biol. 2008, 52 (5-6) 781-790
42. Clark, N. L.; Gasper, J.; Sekino, M.; Springer, S. A.; Aquadro, C. F.; Swanson, W. J. Coevolution of interacting fertilization proteins PLoS Genet. 2009, 5 (7) e1000570
43. Good, J. M.; Wiebe, V.; Albert, F. W.; Burbano, H. A.; Kircher, M.; Green, R. E.; Halbwax, M.; André, C.; Atencia, R.; Fischer, A.; Pääbo, S. Comparative population genomics of the ejaculate in humans and the great apes Mol. Biol. Evol. 2013, 30 (4) 964-976
44. Swanson, W. J.; Nielsen, R.; Yang, Q. Pervasive adaptive evolution in mammalian fertilization proteins Mol. Biol. Evol. 2003, 20 (1) 18-20
45. Ramm, S. A.; Oliver, P. L.; Ponting, C. P.; Stockley, P.; Emes, R. D. Sexual selection and the adaptive evolution of mammalian ejaculate proteins Mol. Biol. Evol. 2008, 25 (1) 207-219
46. Turner, L. M.; Chuong, E. B.; Hoekstra, H. E. Comparative analysis of testis protein evolution in rodents Genetics 2008, 179 (4) 2075-2089
47. Dorus, S.; Wasbrough, E. R.; Busby, J.; Wilkin, E. C.; Karr, T. L. Sperm proteomics reveals intensified selection on mouse sperm membrane and acrosome genes Mol. Biol. Evol. 2010, 27 (6) 1235-1246
48. Dean, M. D.; Clark, N. L.; Findlay, G. D.; Karn, R. C.; Yi, X.; Swanson, W. J.; MacCoss, M. J.; Nachman, M. W. Proteomics and comparative genomic investigations reveal heterogeneity in evolutionary rate of male reproductive proteins in mice (Mus domesticus) Mol. Biol. Evol. 2009, 26 (8) 1733-1743
49. Jeong, H.; Mason, S. P.; Barabási, A. L.; Oltvai, Z. N. Lethality and centrality in protein networks Nature 2001, 411 (6833) 41-42
50. Fraser, H. B.; Hirsh, A. E.; Steinmetz, L. M.; Scharfe, C.; Feldman, M. W. Evolutionary rate in the protein interaction network Science 2002, 296 (5568) 750-752
51. Batada, N. N.; Reguly, T.; Breitkreutz, A.; Boucher, L.; Breitkreutz, B. J.; Hurst, L. D.; Tyers, M. Still stratus not altocumulus: Further evidence against the date/party hub distinction PLoS Biol. 2007, 5 (6) e154
52. Brown, K. R.; Jurisica, I. Unequal evolutionary conservation of human protein interactions in interologous networks Genome Biol. 2007, 8 (5) R95
53. Kim, P. M.; Korbel, J. O.; Gerstein, M. B. Positive selection at the protein network periphery: Evaluation in terms of structural constraints and cellular context Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (51) 20274-20279
54. World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen, 5 th ed.; World Health Organization: Geneva, Switzerland, 2010.
55. Secciani, F.; Bianchi, L.; Ermini, L.; Cianti, R.; Armini, A.; La Sala, G. B.; Focarelli, R.; Bini, L.; Rosati, F. Protein profile of capacitated versus ejaculated human sperm J. Proteome Res. 2009, 8 (7) 3377-3389
56. Grasa, P.; Colas, C.; Gallego, M.; Monteagudo, L.; Muiño-Blanco, T.; Cebrián-Pérez, J. A. Changes in content and localization of proteins phosphorylated at tyrosine, serine and threonine residues during ram sperm capacitation and acrosome reaction Reproduction 2009, 137 (4) 655-667
57. Asif, A. R.; Oellerich, M.; Amstrong, V. W.; Riemenschneider, B.; Monod, M.; Reichard, U. Proteome of conidial surface associated proteins of Aspergillus fumigatus reflecting potential vaccine candidates and allergens J. Proteome Res. 2006, 5 (4) 954-962
58. Dinkel, H.; Chica, C.; Via, A.; Gould, C. M.; Jensen, L. J.; Gibson, T. J.; Diella, F. Phospho.ELM: A database of phosphorylation sites-update 2011. Nucleic Acids Res. 2010, 39 (Database issue), D261-267.
59. Bodenmiller, B.; Campbell, D.; Gerrits, B.; Lam, H.; Jovanovic, M.; Picotti, P.; Schlapbach, R.; Aebersold, R. PhosphoPep-A database of protein phosphorylation sites in model organisms Nat. Biotechnol. 2008, 26 (12) 1339-1340
60. Blom, N.; Gammeltoft, S.; Brunak, S. Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites J. Mol. Biol. 1999, 294 (5) 1351-1362
61. Penn, O.; Privman, E.; Ashkenazy, H.; Landan, G.; Graur, D.; Pupko, T. GUIDANCE: A web server for assessing alignment confidence scores. Nucleic Acids Res. 2010, 38 (Web Server issue), W23-28.
62. Yang, Z. PAML 4: Phylogenetic analysis by maximum likelihood Mol. Biol. Evol. 2007, 24 (8) 1586-1591
63. Jones, D. T.; Taylor, W. R.; Thornton, J. M. The rapid generation of mutation data matrices from protein sequences CABIOS, Comput. Appl. Biosci. 1992, 8 (3) 275-282
64. Kumar, S.; Suleski, M. P.; Markov, G. J.; Lawrence, S.; Marco, A.; Filipski, A. J. Positional conservation and amino acids shape the correct diagnosis and population frequencies of benign and damaging personal amino acid mutations Genome Res. 2009, 19 (9) 1562-1569
65. Hedges, S. B.; Dudley, J.; Kumar, S. TimeTree: A public knowledge-base of divergence times among organisms Bioinformatics 2006, 22 (23) 2971-2972
66. Martínez-Heredia, J.; Estanyol, J. M.; Ballescà, J. L.; Oliva, R. Proteomic identification of human sperm proteins Proteomics 2006, 6 (15) 4356-4369
67. Landry, C. R.; Levy, E. D.; Michnick, S. W. Weak functional constraints on phosphoproteomes Trends Genet. 2009, 25 (5) 193-197
68. Wang, Z.; Ding, G.; Geistlinger, L.; Li, H.; Liu, L.; Zeng, R.; Tateno, Y.; Li, Y. Evolution of protein phosphorylation for distinct functional modules in vertebrate genomes Mol. Biol. Evol. 2011, 28 (3) 1131-1140
69. Guyonnet, B.; Zabet-Moghaddam, M.; Sanfrancisco, S.; Cornwall, G. A. Isolation and proteomic characterization of the mouse sperm acrosomal matrix Mol. Cell. Proteomics 2012, 11 (9) 758-774
70. Metz, E. C.; Palumbi, S. R. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin Mol. Biol. Evol. 1996, 13 (2) 397-406
71. Swanson, W. J.; Vacquier, V. D. The rapid evolution of reproductive proteins Nat. Rev. Genet. 2002, 3 (2) 137-144
72. Torgerson, D. G.; Kulathinal, R. J.; Singh, R. S. Mammalian sperm proteins are rapidly evolving: Evidence of positive selection in functionally diverse genes Mol. Biol. Evol. 2002, 19 (11) 1973-1980
73. Dorus, S.; Busby, S. A.; Gerike, U.; Shabanowitz, J.; Hunt, D. F.; Karr, T. L. Genomic and functional evolution of the Drosophila melanogaster sperm proteome Nat. Genet. 2006, 38 (12) 1440-1445
74. Hurst, L. D.; Smith, N. G. C. Do essential genes evolve slowly? Curr. Biol. 1999, 9 (14) 747-750
75. Jordan, I. K.; Rogozin, I. B.; Wolf, Y. I.; Koonin, E. V. Essential genes are more evolutionarily conserved than are nonessential genes in bacteria Genome Res. 2002, 12 (6) 962-968
76. Amoutzias, G. D.; He, Y.; Lilley, K. S.; Van de Peer, Y.; Oliver, S. G. Evaluation and properties of the budding yeast phosphoproteome Mol. Cell. Proteomics 2012, 11 (6) M111.009555
77. Lovell, S. C.; Robertson, D. L. An integrated view of molecular coevolution in protein-protein interactions Mol. Biol. Evol. 2010, 27 (11) 2567-2575
78. Zimmerman, S.; Sutovsky, P. The sperm proteasome during sperm capacitation and fertilization J. Reprod. Immunol. 2009, 83 (1-2) 19-25
79. Hughes, A. L. Evolution of the proteasome components Immunogenetics 1997, 46 (2) 82-92
80. Gille, C.; Goede, A.; Schlötelburg, C.; Preissner, R.; Kloetzel, P. M.; Göbel, U. B.; Frömmel, C. A comprehensive view on proteasomal sequences: Implications for the evolution of the proteasome J. Mol. Biol. 2003, 326 (5) 1437-1448
81. Torgerson, D. G.; Singh, R. S. Rapid evolution through gene duplication and subfunctionalization of the testes-specific alpha4 proteasome subunits in Drosophila Genetics 2004, 168 (3) 1421-1432
82. Rooney, A. P.; Zhang, J.; Nei, M. An unusual form of purifying selection in a sperm protein Mol. Biol. Evol. 2000, 17 (2) 278-283
83. Glassey, B.; Civetta, A. Positive selection at reproductive ADAM genes with potential intercellular binding activity Mol. Biol. Evol. 2004, 21 (5) 851-859