Long-term survival of high quality sperm: Insights into the sperm proteome of the honeybee Apis mellifera

Journal of Proteome Research

Volumn 12, Issue 11, 2013, Pages 5180-5188

  Zareie, Reza ^a   Eubel, Holger ^a,b   Millar, A Harvey ^a   Baer, Boris ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

comparative proteomics; sperm proteins; sperm senescence; sperm viability

Indexed keywords

CYTOSKELETON PROTEIN; GUANOSINE TRIPHOSPHATASE; MITOCHONDRIAL PROTEIN; NUCLEOSIDE TRIPHOSPHATASE; PEPTIDASE; PROTEOME;

ADAPTATION; APIS MELLIFERA; ARTICLE; BIOINFORMATICS; DROSOPHILA; DROSOPHILA MELANOGASTER; ENZYME REGULATION; LONG TERM SURVIVAL; MALE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEOMICS; SPERM; TANDEM MASS SPECTROMETRY;

ADAPTATION, BIOLOGICAL; ANIMALS; BEES; CELL SURVIVAL; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; MALE; MASS SPECTROMETRY; PROTEOME; PROTEOMICS; SPERMATOZOA; WESTERN AUSTRALIA;

EID: 84887233746     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr4004773     Document Type: Article

References (59)

1. Birkhead, T. R.; Hosken, D. J.; Pitnick, S. Sperm Biology: An Evolutionary Perspective; Elsevier: Amsterdam, 2009; p 642.
2. Ainsworth, C. The secret life of sperm Nature 2005, 436, 770-771
3. Jamieson, B. G. M. The Ultrastructure and Phylogeny of Insect Spermatozoa; Cambridge University Press: New York, Cambridge, 1987; p 320.
4. Jamieson, B. G. M.; Dallai, R.; Afzelius, B. A. Insects: Their Spermatozoa and Phylogeny; Scientific Publishers: Enfield, NH, 1999; p 564.
5. Baer, B. Sexual selection in Apis bees Apidologie 2005, 36, 187-200
6. Baer, B. The copulation biology of ants (Hymenoptera: Formicidae) Myrmecol. News 2011, 14, 55-68
7. Hölldobler, B.; Bartz, S. H. Sociobiology of reproduction in ants. In Experimental Behavioural Ecology and Sociobiology; Hölldobler, B.; Lindauer, M., Eds.; Gustav Fischer Verlag: Stuttgart, 1985; pp 237-257.
8. Boomsma, J. J.; Baer, B.; Heinze, J. The evolution of male traits in social insects Annu. Rev. Entomol. 2005, 50, 395-420
9. Pamilo, P. Life span of queens in the ant Formica exsecta Insectes Soc. 1991, 38 (2) 111-120
10. den Boer, S. P. A.; Baer, B.; Dreier, S.; Aron, S.; Nash, D. R.; Boomsma, J. J. Prudent sperm use by leaf-cutter ant queens Proc. R. Soc. B 2009, 276 (1675) 3945-3953
11. Tschinkel, W. R.; Porter, S. D. Efficiency of sperm use in queens of the fire ant, Solenopsis invicta (Hymenoptera: Formicidae) Ann. Entomol. Soc. Am. 1988, 81 (5) 777-781
12. Hunter, F. M.; Birkhead, T. R. Sperm viability and sperm competition in insects Curr. Biol. 2002, 12 (2) 121-123
13. den Boer, S. P. A.; Boomsma, J. J.; Baer, B. Seminal fluid enhances sperm viability in the leafcutter ant Atta colombica Behav. Ecol. Sociobiol. 2008, 62, 1843-1849
14. Fjerdingstad, E. J.; Boomsma, J. J. Variation in size and sperm content of sexuals in the leafcutter ant Atta colombica Insectes Soc. 1997, 44 (3) 209-218
15. Weber, N. A. Gardening Ants: The Attines. The American Philosophical Society: Philadelphia, 1972; p 146.
16. Baer, B.; Armitage, S. A. O.; Boomsma, J. J. Sperm storage induces an immunity cost in ants Nature 2006, 441, 872-875
17. Baer, B.; Heazlewood, J. L.; Taylor, N. L.; Eubel, H.; Millar, A. H. The seminal fluid proteome of the honeybee Apis mellifera Proteomics 2009, 9, 2085-2097
18. Baer, B.; Eubel, H.; Taylor, N. L.; O'Toole, N.; Millar, A. H. Insights into female sperm storage from the spermathecal fluid proteome of the honeybee Apis mellifera Genome Biol. 2009, 10, R 67
19. den Boer, S. P. A.; Baer, B.; Boomsma, J. J. Seminal fluid mediates ejaculate competition in social insects Science 2010, 327, 1506-1509
20. Poland, V.; Eubel, H.; King, M.; Solheim, C.; Millar, A. H.; Baer, B. Stored sperm differs from ejaculated sperm by proteome alterations associated with energy metabolism in the honeybee Apis mellifera Mol. Ecol. 2011, 20, 2643-2654
21. Ruttner, F. The Instrumental Insemination of the Queen Bee, 2 nd ed.; Apimondia: Bucharest, 1976; p 123.
22. Chan, Q. W. T.; Parker, R.; Sun, Z.; Deutsch, E. W.; Foster, L. J. A honey bee (Apis mellifera L.) PeptideAtlas crossing castes and tissues BMC Genomics 2011, 12
23. 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
24. Wasbrough, E. R.; Dorus, S.; Hester, S.; Howard-Murkin, J.; Lilley, K.; Wilkin, E.; Polpitiya, A.; Petritis, K.; Karr, T. L. The Drosophila melanogaster sperm proteome-II (DmSP-II) J. Proteomics 2010, 73 (11) 2171-2185
25. Baker, M. A.; Reeves, G.; Hetherington, L.; Muller, J.; Baur, I.; Aitken, R. J. Identification of gene products present in Triton X-100 soluble and insoluble fractions of human spermatozoa lysates using LC-MS/MS analysis Proteomics: Clin. Appl. 2007, 1 (5) 524-532
26. van Iersel, M. P.; Pico, A. R.; Kelder, T.; Gao, J. J.; Ho, I.; Hanspers, K.; Conklin, B. R.; Evelo, C. T. The BridgeDb framework: standardized access to gene, protein and metabolite identifier mapping services BMC Bioinf. 2010, 10.1186/1471-2105-11-5
27. Cote, R. G.; Jones, P.; Martens, L.; Kerrien, S.; Reisinger, F.; Lin, Q.; Leinonen, R.; Apweiler, R.; Hermjakob, H., The Protein Identifier Cross-Referencing (PICR) service: reconciling protein identifiers across multiple source databases. BMC Bioinf. 2007, 8.
28. Alcivar, A. A.; Hake, L. E.; Millette, C. F.; Trasler, J. M.; Hecht, N. B. Mitochodrial gene expression in male germ cells of the mouse Dev. Biol. 1989, 135 (2) 263-271
29. Ostermeier, G. C.; Dix, D. J.; Miller, D.; Khatri, P.; Krawetz, S. A. Spermatozoal RNA profiles of normal fertile men Lancet 2002, 360 (9335) 772-777
30. Yang, C. C.; Lin, Y. S.; Hsu, C. C.; Wu, S. C.; Lin, E. C.; Cheng, W. T. K. Identification and sequencing of remnant messenger RNAs found in domestic swine (Sus scrofa) fresh ejaculated spermatozoa Anim. Reprod. Sci. 2009, 113 (1-4) 143-155
31. Bonache, S.; Mata, A.; Ramos, M. D.; Bassas, L.; Larriba, S. Sperm gene expression profile is related to pregnancy rate after insemination and is predictive of low fecundity in normozoospermic men Hum. Reprod. 2012, 27 (6) 1556-1567
32. Liu, W. M.; Pang, R. T. K.; Chiu, P. C. N.; Wong, B. P. C.; Lao, K. Q.; Lee, K. F.; Yeung, W. S. B. Sperm-borne microRNA-34c is required for the first cleavage division in mouse Proc. Natl. Acad. Sci. U.S.A. 2012, 109 (2) 490-494
33. Hecht, N. B.; Williams, J. L. Synthesis of RNA by separated heads and tails from bovine spermatozoa Biol. Reprod. 1978, 19 (3) 573-579
34. Wang, L. B.; Fan, J. S.; Yu, M. J.; Zheng, S. Y.; Zhao, Y. J. Association of goat (Capra hircus) CD4 gene exon 6 polymorphisms with ability of sperm internalizing exogenous DNA Mol. Biol. Rep. 2011, 38 (3) 1621-1628
35. Gur, Y.; Breitbart, H. Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes Genes Dev. 2006, 20, 411-416
36. Gur, Y.; Breitbart, H. Protein synthesis in sperm: Dialog between mitochondria and cytoplasm Mol. Cell. Endocrinol. 2008, 282 (1-2) 45-55
37. Poole, H. K.; Taber, S. In-vitro preservation of honeybee (Hymenoptera Apidae) semen enhanced by storage at 13-15 degrees C Ann. Entomol. Soc. Am. 1970, 63 (6) 1673-1674
38. 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
39. Krapf, D.; Arcelay, E.; Wertheimer, E. V.; Sanjay, A.; Pilder, S. H.; Salicioni, A. M.; Visconti, P. E. Inhibition of Ser/Thr phosphatases induces capacitation-associated signaling in the presence of Src kinase inhibitors J. Biol. Chem. 2010, 285 (11) 7977-7985
40. Salicioni, A. M.; Platt, M. D.; Wertheimer, E. V.; Arcelay, E.; Allaire, A.; Sosnik, J.; Visconti, P. E. Signalling pathways involved in sperm capacitation Soc. Reprod. Fertil. Suppl. 2007, 65, 245-259
41. Breitbart, H.; Spungin, B. The biochemistry of the acrosome reaction Mol. Hum. Reprod. 1997, 3 (3) 195-202
42. De Blas, G. A.; Roggero, C. M.; Tomes, C. N.; Mayorga, L. S. Dynamics of SNARE assembly and disassembly during sperm acrosomal exocytosis PLoS Biol. 2005, 3 (10) 1801-1812
43. Branham, M. T.; Bustos, M. A.; De Blas, G. A.; Rehmann, H.; Zarelli, V. E. P.; Trevino, C. L.; Darszon, A.; Mayorga, L. S.; Tomes, C. N. Epac activates the small G proteins Rap1 and Rab3A to achieve exocytosis J. Biol. Chem. 2009, 284 (37) 24825-24839
44. Eklund, H.; Uhlin, U.; Färnegårdh, M.; Logan, D. T.; Nordlund, P. Structure and function of the radical enzyme ribonucleotide reductase Prog. Biophys. Mol. Biol. 2001, 77 (3) 177-268
45. Tanaka, T.; Hosokawa, M.; Vagin, V. V. Tudor domain containing 7 (Tdrd7) is essential for dynamic ribonucleoprotein (RNP) remodeling of chromatoid bodies during spermatogenesis Proc. Natl. Acad. Sci. U.S.A. 2011, 108 (26) 10579-10584
46. Low, M. G. Glycosyl-phosphatidylinositol: a versatile anchor for cell surface proteins FASEB J. 1989, 3 (5) 1600-1605
47. Toha, Y. K.; Kamariaha, N.; Maurer-Stroh, S. Structural insight into the glycosylphosphatidylinositol transamidase subunits PIG-K and PIG-S from yeast J. Struct. Biol. 2011, 173 (2) 271-281
48. Smale, S. T. Pioneer factors in embryonic stem cells and differentiation Curr. Opin. Genet. Dev. 2010, 20, 519-526
49. Thomas, P. D; Kejariwal, A.; Guo, N.; Mi, H.; Campbell, M. J.; Muruganujan, A.; Lazareva-Ulitsky, B. Applications for protein sequence-function evolution data: mRNA/protein expression analysis and coding SNP scoring tools Nucleic Acid Res. 2006, 34, W645-W650
50. Lachke, S. A.; Alkuraya, F. S.; Kneeland, S. C.; Ohn, T. Mutations in the RNA granule component TDRD7 cause cataract and glaucoma Science 2011, 331 (6024) 1571-157
51. Kessner, D.; Chambers, M.; Burke, R.; Agus, D.; Mallick, P. ProteoWizard: open source software for rapid proteomics tools development Bioinformatics 2008, 24 (21) 2534-2536
52. Collins, A. M.; Williams, V.; Evans, J. D. Sperm storage and antioxidative enzyme expression in the honey bee Apis mellifera Insect Mol. Biol. 2004, 13, 141-146
53. Ribou, A. C.; Reinhardt, K. Reduced metabolic rate and oxygen radicals production in stored insect sperm Proc. R. Soc. B 2011, 1098, 2422-2426
54. Deutsch, E. W.; Mendoza, L.; Shteynberg, D.; Farrah, T.; Lam, H.; Tasman, N.; Nilsson, E.; Pratt, B.; Prazen, B.; Eng, J. K.; Martin, D. B.; Nesvizhskii, A. I.; Aebersold, R. A guided tour of the Trans-Proteomic Pipeline Proteomics 2010, 10 (6) 1150-1159
55. Shteynberg, D.; Deutsch, E. W.; Lam, H.; Eng, J. K.; Sun, Z.; Tasman, N.; Mendoza, L.; Moritz, R. L.; Aebersold, R.; Nesvizhskii, A. I. iProphet: multi-level integrative analysis of shotgun proteomic data improves peptide and protein identification rates and error estimates Mol. Cell. Proteomics 2011, 10 (12) M111.007690
56. Kapp, E. A.; Schütz, F.; Connolly, L. M.; Chakel, J. A.; Meza, J. E.; Miller, C. A.; Fenyo, D.; Eng, J. K.; Adkins, J. N.; Omenn, G. S.; Simpson, R. J. An evaluation, comparison, and accurate benchmarking of several publicly available MS/MS search algorithms: sensitivity and specificity analysis Proteomics 2005, 5 (13) 3475-3490
57. Baer, B.; Zareie, R.; Paynter, E.; Poland, V.; Millar, A. H. Seminal fluid proteins differ in abundance between genetic lineages of honeybees J. Proteomics 2012, 75 (18) 5646-5653
58. Elsik, C. G.; Mackey, A. J.; Reese, J. T.; Milshina, N. V.; Roos, D. S.; Weinstock, G. M. Creating a honey bee consensus gene set Genome Biol. 2007, 8 (1) R13
59. Collins, A. M.; Caperna, T. J.; Williams, V.; Garrett, W. M.; Evans, J. D. Proteomic analyses of male contributions to honey bee sperm storage and mating Insect Mol. Biol. 2006, 15 (5) 541-549