Proteomic revolution to improve tools for evaluating male fertility in animals

Journal of Proteome Research

Volumn 12, Issue 11, 2013, Pages 4738-4747

  Park, Yoo Jin ^a   Kim, Jin ^a   You, Young Ah ^a   Pang, Myung Geol ^a  

^a Chung Ang University   (South Korea)

Author keywords

biomarker; infertility; protein profiling; semen analysis; sperm physiology; spermatozoa; subfertility

Indexed keywords

ACROSIN; ALDEHYDE REDUCTASE; ALKALINE PHOSPHATASE; ARGIPRESSIN RECEPTOR; CASEIN KINASE; CHAPERONE; CHAPERONIN CONTAINING TCP1; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYTOCHROME C OXIDASE; DIPEPTIDYL CARBOXYPEPTIDASE; GLUTATHIONE TRANSFERASE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; IDITOL DEHYDROGENASE; LACTATE DEHYDROGENASE; LIPOCORTIN 2; PEROXIREDOXIN 4; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PHOSPHOGLYCERATE MUTASE; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; PROTEIN P53; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE DEHYDROGENASE; PYRUVATE KINASE; TRIOSEPHOSPHATE ISOMERASE; VOLTAGE DEPENDENT ANION CHANNEL 2;

ACROSOME REACTION; CELL INTERACTION; ENERGY METABOLISM; ION TRANSPORT; MALE FERTILITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; REVIEW; SEMEN ANALYSIS; SEMINAL PLASMA; SIGNAL TRANSDUCTION; SPERM; SPERMATOZOON; SPERMATOZOON MATURATION;

ANIMALS; BREEDING; FERTILITY; INFERTILITY, MALE; MALE; PROTEOMICS; SEMEN ANALYSIS; SEMINAL PLASMA PROTEINS; SIGNAL TRANSDUCTION; SPERMATOZOA;

EID: 84887260860     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400639x     Document Type: Review

References (88)

1. Peddinti, D.; Nanduri, B.; Kaya, A.; Feugang, J. M.; Burgess, S. C.; Memili, E. Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility BMC Syst. Biol. 2008, 2, 19
2. Amann, R. P.; Hammerstedt, R. H. In vitro evaluation of sperm quality: an opinion J. Androl. 1993, 14, 397-406
3. Gadea, J.; Matas, C. Sperm factors related to in vitro penetration of porcine oocytes Theriogenology 2000, 54, 1343-1357
4. Rodriguez-Martinez, H. Laboratory semen assessment and prediction of fertility: still utopia? Reprod. Domest. Anim. 2003, 38, 312-318
5. Aitken, R. J. Sperm function tests and fertility Int. J. Androl. 2006, 29, 69-75
6. Corner, J. S.; Barratt, C. L. R. Genomic and Proteomic Approaches to Defineing Sperm. In The Sperm Cell De Jonge, C. J., Barratt, C. L. R., Eds.; Cambridge University Press: Cambridge, U.K., 2006, pp 49-71.
7. Lalancette, C.; Faure, R. L.; Leclerc, P. Identification of the proteins present in the bull sperm cytosolic fraction enriched in tyrosine kinase activity: a proteomic approach Proteomics 2006, 6 (16) 4523-4540
8. Oliva, R.; de Mateo, S.; Estanyol, J. M. Sperm cell proteomics Proteomics 2009, 9, 1004-1017
9. Park, Y. J.; Kwon, W. S.; Oh, S. A.; Pang, M. G. Fertility-related proteomic profiling bull spermatozoa separated by Percoll J. Proteome Res. 2012, 11, 4162-4168
10. Bissonnette, N.; Lévesque-Sergerie, J. P.; Thibault, C.; Boissonneault, G. Spermatozoal transcriptome profiling for bull sperm motility: a potential tool to evaluate semen quality Reproduction 2009, 138, 65-80
11. Aitken, R. J.; Baker, M. A. The role of proteomics in understanding sperm cell biology Int. J. Androl. 2008, 31, 295-302
12. Januskauskas, A.; Johannisson, A.; Rodriguez-Martinez, H. Subtle membrane changes in cryopreserved bull semen in relation with sperm viability, chromatin structure, and field fertility Theriogenology 2003, 60, 743-758
13. Wood, P. D.; Foulkes, J. A.; Shaw, R. C.; Melrose, D. R. Semen assessment, fertility and the selection of Hereford bulls for use in AI J. Reprod. Fertil. 1986, 6, 783-795
14. Budworth, P. R.; Amann, R. P.; Chapman, P. L. Relationships between computerized measurements of motion of frozen-thawed bull spermatozoa and fertility J. Androl. 1988, 9, 41-54
15. Bonde, J. P.; Ernst, E.; Jensen, T. K.; Hjollund, N. H.; Kolstad, H.; Henriksen, T. B.; Scheike, T.; Giwercman, A.; Olsen, J.; Skakkebaek, N. E. Relation between semen quality and fertility: a population-based study of 430 first-pregnancy planners Lancet 1998, 352, 1172-1177
16. Galli, A.; Basetti, M.; Balduzzi, D.; Martignoni, M.; Bornaghi, V.; Maffii, M. Frozen bovine semen quality and bovine cervical mucus penetration test Theriogenology 1991, 35, 837-844
17. Verberckmoes, S.; Van Soom, A.; De Pauw, I.; Dewulf, J.; de Kruif, A. Migration of bovine spermatozoa in a synthetic medium and its relation to in vivo bull fertility Theriogenology 2002, 58, 1027-1037
18. Sharara, F. I.; Illions, E. H.; Coddington, C. C.; Scott, R. T. Evaluation of the Tru-Trax cervical mucus penetration test in predicting fertilization and pregnancy rates in in-vitro fertilization Hum. Reprod. 1995, 10, 1481-1485
19. Thundathil, J.; Gil, J.; Januskauskas, A.; Larsson, B.; Soderquist, L.; Mapletoft, R.; Rodriguez-Martinez, H. Relationship between the proportion of capacitated spermatozoa present in frozen-thawed bull semen and fertility with artificial insemination Int. J. Androl. 1999, 22, 366-373
20. Kjaestad, H.; Ropstad, E.; Berg, K. A. Evaluation of spermatological parameters used to predict the fertility of frozen bull semen Acta. Vet. Scand. 1993, 34, 299-303
21. Söderquist, L.; Rodriguez-Martinez, H.; Janson, L. Post-thaw motility, ATP content and cytochrome C oxidase activity of A.I. bull spermatozoa in relation to fertility Zentralbl. Veterinaermed., Reihe A 1991, 38, 165-174
22. Kruip, T. A.; Wurth, Y. A.; den Daas, N. Homologous Oocyte Penetration in Vitro: A Reliable Parameter for the Fertilizing Potency of Bull Semen? Proc. Int. Congr. Anim. Reprod., 12th 1992, 2 (16) 653-655
23. Xu, X.; Ding, J.; Seth, P. C.; Harbison, D. S.; Foxcroft, G. R. In vitro fertilization of in vitro matured pig oocytes: effects of boar and ejaculate fraction Theriogenology 1996, 45, 745-755
24. Zhang, B. R.; Larsson, B.; Lundeheim, N.; Håård, M. G.; Rodriguez-Martinez, H. Prediction of bull fertility by combined in vitro assessments of frozen-thawed semen from young dairy bulls entering an AI-programme Int. J. Androl. 1999, 22, 253-260
25. Brahmkshtri, B. P.; Edwin, M. J.; John, M. C.; Nainar, A. M.; Krishnan, A. R. Relative efficacy of conventional sperm parameters and sperm penetration bioassay to assess bull fertility in vitro Anim. Reprod. Sci. 1999, 54, 159-168
26. Schneider, C. S.; Ellington, J. E.; Wright, R. W., Jr. Relationship between bull field fertility and in vitro embryo production using sperm preparation methods with and without somatic cell co-culture Theriogenology 1999, 51, 1085-1098
27. Evenson, D. P.; Thompson, L.; Jost, L. Flow cytometric evaluation of boar semen by the sperm chromatin structure assay as related to cryopreservation and fertility Theriogenology 1994, 41, 637-651
28. Hirai, M.; Boersma, A.; Hoeflich, A.; Wolf, E.; Foll, J.; Aumüller, T. R.; Braun, J. Objectively measured sperm motility and sperm head morphometry in boars (Sus scrofa): relation to fertility and seminal plasma growth factors J. Androl. 2001, 22, 104-110
29. Oh, S. A.; Park, Y. J; You, Y. A.; Mohamed, E. A.; Pang, M. G. Capacitation status of stored boar spermatozoa is related to litter size of sows Anim. Reprod. Sci. 2010, 121, 131-138
30. Gadea, J. Sperm factors related to in vitro and in vivo porcine fertility Theriogenology 2005, 63, 431-444
31. Corson, S. L.; Batzer, F. R.; Marmar, J.; Maislin, G. The human sperm-hamster egg penetration assay: prognostic value Fertil. Steril. 1988, 49, 328-334
32. Eaglesome, M. D.; Garcia, M. M. The effect of Mycoplasma bovis on fertilization processes in vitro with bull spermatozoa and zona-free hamster oocytes Vet. Microbiol. 1990, 21, 329-337
33. Mohamed, E. A.; Song, W. H.; Oh, S. A.; Park, Y. J.; You, Y. A.; Lee, S.; Choi, J. Y.; Kim, Y. J.; Jo, I.; Pang, M. G. The transgenerational impact of benzo(a)pyrene on murine male fertility Hum. Reprod. 2010, 25, 2427-2433
34. Oh, S. A.; You, Y. A.; Park, Y. J.; Pang, M. G. The sperm penetration assay predicts the litter size in pigs Int. J. Androl. 2010, 33, 604-612
35. Park, Y. J.; Mohamed, el-S. A.; Oh, S. A.; Yoon, S. J.; Kwon, W. S.; Kim, H. R.; Lee, M. S.; Lee, K.; Pang, M. G. Sperm penetration assay as an indicator of bull fertility J. Reprod. Dev. 2012, 58, 461-466
36. Baker, M. A.; Witherdin, R.; Hetherington, L.; Cunningham-Smith, K.; Aitken, R. J. Identification of post-translational modifications that occur during sperm maturation using difference in two-dimensional gel electrophoresis Proteomics 2005, 5, 1003-1012
37. de Mateo, S.; Martínez-Heredia, J.; Estanyol, J. M.; Domínguez-Fandos, D.; Vidal-Taboada, J. M.; Ballescà, J. L.; Oliva, R. Marked correlations in protein expression identified by proteomic analysis of human spermatozoa Proteomics 2007, 7, 4264-4277
38. Silvestri, E.; Lombardi, A.; de Lange, P.; Glinni, D.; Senese, R.; Cioffi, F.; Lanni, A.; Goglia, F.; Moreno, M. Studies of complex biological systems with applications to molecular medicine: the need to integrate transcriptomic and proteomic approaches J. Biomed. Biotechnol. 2011, 810242
39. Aebersold, R.; Mann, M. Mass spectrometry-based proteomics Nature 2003, 422, 198-207
40. Domon, B.; Aebersold, R. Mass spectrometry and protein analysis Science 2006, 312, 212-217
41. De Jonge, C. Biological basis for human capacitation Hum. Reprod. Update 2005, 11, 205-214
42. Dacheux, J. L.; Gatti, J. L.; Dacheux, F. Contribution of epididymal secretory proteins for spermatozoa maturation Microsc. Res. Tech. 2003, 61, 7-17
43. Kelly, V. C.; Kuy, S.; Palmer, D. J.; Xu, Z.; Davis, S. R.; Cooper, G. J. Characterization of bovine seminal plasma by proteomics Proteomics 2006, 6, 5826-5833
44. Curi, S. M.; Ariagno, J. I.; Chenlo, P. H.; Mendeluk, G. R.; Pugliese, M. N.; Sardi Segovia, L. M.; Repetto, H. E.; Blanco, A. M. Asthenozoospermia: analysis of a large population Arch. Androl. 2003, 49, 343-349
45. Chen, H.; Cheung, M. P.; Chow, P. H.; Cheung, A. L; Liu, W.; O, W. S. Protection of sperm DNA against oxidative stress in vivo by accessory sex gland secretions in male hamsters Reproduction 2002, 124, 491-499
46. Einspanier, R.; Amselgruber, W.; Sinowatz, F.; Henle, T.; Röpke, R.; Schams, D. Localization and concentration of a new bioactive acetic seminal fluid protein (aSFP) in bulls (Bos taurus) J. Reprod. Fertil. 1993, 98, 241-244
47. Yuan, Y. Y.; Chen, W. Y.; Shi, Q. X.; Mao, L. Z.; Yu, S. Q.; Fang, X.; Roldan, E. R. Zona pellucida induces activation of phospholipase A2 during acrosomal exocytosis in guinea pig spermatozoa Biol. Reprod. 2003, 68, 904-913
48. Thérien, I.; Moreau, R.; Manjunath, P. Bovine seminal plasma phospholipid-binding proteins stimulate phospholipid efflux from epididymal sperm Biol. Reprod. 1999, 61, 590-598
49. Killian, G. J.; Chapman, D. A.; Rogowski, L. A. Fertility-associated proteins in Holstein bull seminal plasma Biol. Reprod. 1993, 49, 1202-1207
50. Moura, A. A.; Chapman, D. A.; Koc, H.; Killian, G. J. A comprehensive proteomic analysis of the accessory sex gland fluid from mature Holstein bulls Anim. Reprod. Sci. 2007, 98, 169-188
51. Brandon, C. I.; Heusner, G. L.; Caudle, A. B.; Fayrer-Hosken, R. A. Two-dimensional polyacrylamide gel electrophoresis of equine seminal plasma proteins and their correlation with fertility Theriogenology 1999, 52, 863-873
52. Russell, L. D.; Peterson, R. N.; Hunt, W.; Strack, L. E. Posttesticular surface modifications and contributions of reproductive tract fluids to the surface polypeptide composition of boar spermatozoa Biol. Reprod. 1984, 30, 959-978
53. Cornwall, G. A. New insights into epididymal biology and function Hum. Reprod. Update 2009, 15, 213-227
54. Aitken, R. J.; Nixon, B.; Lin, M.; Koppers, A. J.; Lee, Y. H.; Baker, M. A. Proteomic changes in mammalian spermatozoa during epididymal maturation Asian J. Androl. 2007, 9, 554-564
55. Dacheux, J. L.; Belleannée, C.; Jones, R.; Labas, V.; Belghazi, M.; Guyonnet, B.; Druart, X.; Gatti, J. L.; Dacheux, F. Mammalian epididymal proteome Mol. Cell. Endocrinol. 2009, 306, 45-50
56. Yuan, H.; Liu, A.; Zhang, L.; Zhou, H.; Wang, Y.; Zhang, H.; Wang, G.; Zeng, R.; Zhang, Y.; Chen, Z. Proteomic profiling of regionalized proteins in rat epididymis indicates consistency between specialized distribution and protein functions J. Proteome Res. 2006, 5, 299-307
57. Belleannee, C.; Belghazi, M.; Labas, V.; Teixeira-Gomes, A. P.; Gatti, J. L.; Dacheux, J. L.; Dacheux, F. Purification and identification of sperm surface proteins and changes during epididymal maturation Proteomics 2011, 11, 1952-1964
58. Ijiri, T. W.; Merdiushev, T.; Cao, W.; Gerton, G. L. Identification and validation of mouse sperm proteins correlated with epididymal maturation Proteomics 2011, 11, 4047-4062
59. Baker, M. A.; Nixon, B.; Naumovski, N.; Aitken, R. J. Proteomic insights into the maturation and capacitation of mammalian spermatozoa Syst. Biol. Reprod. Med. 2012, 58, 211-217
60. Jones, R. C. Evolution of the Epididymis. In The Epididymis from Molecules to Clinical Practice. A Comprehensive Survey of the Efferent Ducts, the Epididymis and the Vas Deferens; Robaire, B.; Hinton, B. T., Eds.; Kluwer Academic-Plenum Publishers: New York, 2002; pp 11-33.
61. Puigmulé, M.; Fàbrega, A.; Yeste, M.; Bonet, S.; Pinart, E. Study of the proacrosin-acrosin system in epididymal, ejaculated and in vitro capacitated boar spermatozoa Reprod. Fertil. Dev. 2011, 23, 837-845
62. Frenette, G.; Lessard, C.; Madore, E.; Fortier, M. A.; Sullivan, R. Aldose reductase and macrophage migration inhibitory factor are associated with epididymosomes and spermatozoa in the bovine epididymis Biol. Reprod. 2003, 69, 1586-1592
63. Gatti, J. L.; Druart, X.; Guérin, Y.; Dacheux, F.; Dacheux, J. L. A 105- to 94-kilodalton protein in the epididymal fluids of domestic mammals is angiotensin I-converting enzyme (ACE); evidence that sperm are the source of this ACE Biol. Reprod. 1999, 60, 937-945
64. Kwon, W. S.; Park, Y. J.; Kim, Y. H.; You, Y. A.; Kim, I. C.; Pang, M. G. Vasopressin effectively suppresses male fertility PLoS One 2013, 8, e54192
65. Meistrich, M. L.; Trostle, P. K.; Frapart, M.; Erickson, R. P. Biosynthesis and localization of lactate dehydrogenase X in pachytene spermatocytes and spermatids of mouse testes Dev. Biol. 1977, 60, 428-441
66. Oliva, R.; Martínez-Heredia, J.; de Mateo, S.; Gázquez, C.; Oriola, J.; Estanyol, J. M.; Guimerà, M.; Balasch, J.; Ballescà, J. L. Proteomics of human spermatozoa, protamine content and assisted reproduction outcome Soc. Reprod. Fertil. Suppl. 2007, 65, 527-530
67. Pixton, K. L.; Deeks, E. D.; Flesch, F. M.; Moseley, F. L.; Björndahl, L.; Ashton, P. R.; Barratt, C. L.; Brewis, I. A. Sperm proteome mapping of a patient who experienced failed fertilization at IVF reveals altered expression of at least 20 proteins compared with fertile donors: case report Hum. Reprod. 2004, 19, 1438-1447
68. Zhao, C.; Huo, R.; Wang, F. Q.; Lin, M.; Zhou, Z. M.; Sha, J. H. Identification of several proteins involved in regulation of sperm motility by proteomic analysis Fertil. Steril. 2007, 87, 436-438
69. D'Amours, O.; Frenette, G.; Fortier, M.; Leclerc, P.; Sullivan, R. Proteomic comparison of detergent-extracted sperm proteins from bulls with different fertility indexes Reproduction 2010, 39, 545-556
70. Urner, F.; Sakkas, D. Characterization of glycolysis and pentose phosphate pathway activity during sperm entry into the mouse oocyte Biol. Reprod. 1999, 60, 973-978
71. Travis, A. J.; Tutuncu, L.; Jorgez, C. J.; Ord, T. S.; Jones, B. H.; Kopf, G. S.; Williams, C. J. Requirements for glucose beyond sperm capacitation during in vitro fertilization in the mouse Biol. Reprod. 2004, 71, 139-145
72. Austin, C. R. Observations on the penetration of the sperm in the mammalian egg Aust. J. Sci. Res., Ser. B 1951, 4, 581-596
73. Chang, M. C. Fertilizing capacity of spermatozoa deposited into the fallopian tubes Nature 1951, 168, 697-698
74. Gadella, B. M. Sperm membrane physiology and relevance for fertilization Anim. Reprod. Sci. 2008, 107, 229-236
75. 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, 1129-1137
76. Visconti, P. E.; Moore, G. D.; Bailey, J. L.; Leclerc, P.; Connors, S. A.; Pan, D.; Olds-Clarke, P.; Kopf, G. S. Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway Development 1995, 121, 1139-1150
77. Galantino-Homer, H. L.; Visconti, P. E.; Kopf, G. S. Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3′5′-monophosphate-dependent pathway Biol. Reprod. 1997, 56, 707-719
78. Handrow, R. R.; First, N. L.; Parrish, J. J. Calcium requirement and increased association with bovine sperm during capacitation by heparin J. Exp. Zool. 1989, 252, 174-182
79. Mahony, M. C.; Gwathmey, T. Protein tyrosine phosphorylation during hyperactivated motility of cynomolgus monkey (Macaca fascicularis) spermatozoa Biol. Reprod. 1999, 60, 1239-1243
80. Nassar, A.; Mahony, M.; Morshedi, M.; Lin, M. H.; Srisombut, C.; Oehninger, S. Modulation of sperm tail protein tyrosine phosphorylation by pentoxifylline and its correlation with hyperactivated motility Fertil. Steril. 1999, 71, 919-923
81. Naz, R. K.; Ahmad, K.; Kumar, R. Role of membrane phosphotyrosine proteins in human spermatozoal function J. Cell Sci. 1991, 99, 157-165
82. Flesch, F. M.; Colenbrander, B.; van Golde, L. M.; Gadella, B. M. Capacitation induces tyrosine phosphorylation of proteins in the boar sperm plasma membrane Biochem. Biophys. Res. Commun. 1999, 262, 787-792
83. 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, 11579-11589
84. 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, 1431-1440
85. Baker, M. A.; Reeves, G.; Hetherington, L.; Aitken, R. J. Analysis of proteomic changes associated with sperm capacitation through the combined use of IPG-strip pre-fractionation followed by RP chromatography LC-MS/MS analysis Proteomics 2010, 10, 482-495
86. 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, 1809-1826
87. Jagan Mohanarao, G.; Atreja, S. K. Identification of capacitation associated tyrosine phosphoproteins in buffalo (Bubalus bubalis) and cattle spermatozoa Anim. Reprod. Sci. 2011, 123, 40-47
88. de Lamirande, E.; Gagnon, C. Impact of reactive oxygen species on spermatozoa: a balancing between beneficial and detrimental effects Hum. Reprod. 1995, 10, 15-21