Epididymal protein markers and fertility

Animal Reproduction Science

Volumn 169, Issue , 2016, Pages 76-87

  Dacheux, Jean Louis ^a   Dacheux, Françoise ^a   Druart, Xavier ^a  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

Author keywords

Epididymis; Male fertility; Male fertility markers; Sperm maturation

Indexed keywords

BIOLOGICAL MARKER;

ANIMAL; CELL DIFFERENTIATION; EPIDIDYMIS; GENE EXPRESSION REGULATION; MALE; METABOLISM; PHYSIOLOGY; SPECIES DIFFERENCE; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON MATURATION; SPERMATOZOON MIGRATION; SPERMATOZOON MOTILITY;

ANIMALS; BIOMARKERS; CELL DIFFERENTIATION; EPIDIDYMIS; GENE EXPRESSION REGULATION; MALE; SPECIES SPECIFICITY; SPERM MATURATION; SPERM MOTILITY; SPERM TRANSPORT; SPERMATOGENESIS; SPERMATOZOA;

EID: 84959511063     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2016.02.034     Document Type: Article

References (77)

1. Amann R.P., Johnson L., Thompson D.L.J., Pickett B.W. Daily spermatozoal production, epididymal spermatozoal reserves and transit time of spermatozoa through the epididymis of the rhesus monkey. Biol. Reprod. 1976, 15:586-592.
2. Barrier-Battut I., Dacheux J.L., Gatti J.L., Rouviere P., Stanciu C., Dacheux F., Vidament M. Seminal plasma proteins and semen characteristics in relation with fertility in the stallion. Anim. Reprod. Sci. 2005, 89:255-258.
3. 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.
4. Belleannee C., Labas V., Teixeira-Gomes A.P., Gatti J.L., Dacheux J.L., Dacheux F. Identification of luminal and secreted proteins in bull epididymis. J. Proteom. 2011, 74:59-78.
5. Belleannee C., Calvo E., Thimon V., Cyr D.G., Legare C., Garneau L., Sullivan R. Role of microRNAs in controlling gene expression in different segments of the human epididymis. PLoS One 2012, 7:e34996.
6. Brooks D.E., Means A.R., Wright E.J., Singh S.P., Tiver K.K. Molecular cloning of the cDNA for androgen- dependent sperm-coating glycoproteins secreted by the rat epididymis. Eur. J. Biochem. 1986, 161:13-18.
7. Brooks D.E. Epididymal and testicular temperature in the unrestrained conscious rat. J. Reprod. Fertil. 1973, 35:157-160.
8. Buffone M.G., Doncel G.F., Marin Briggiler C.I., Vazquez-Levin M.H., Calamera J.C. Human sperm subpopulations: relationship between functional quality and protein tyrosine phosphorylation. Hum. Reprod. 2004, 19:139-146.
9. Busso D., Onate-Alvarado M.J., Balboa E., Castro J., Lizama C., Morales G., Vargas S., Hartel S., Moreno R.D., Zanlungo S. Spermatozoa from mice deficient in Niemann-Pick disease type C2 (NPC2) protein have defective cholesterol content and reduced in vitro fertilising ability. Reprod. Fertil. Dev. 2014, 26:609-621.
10. Cancel A.M., Chapman D.A., Killian G.J. Osteopontin is the 55-kilodalton fertility-associated protein in Holstein bull seminal plasma. Biol. Reprod. 1997, 57:1293-1301.
11. Castella S., Benedetti H., de Llorens R., Dacheux J.L., Dacheux F. Train A, an RNase A-like protein without RNase activity, is secreted and reabsorbed by the same epididymal cells under testicular control. Biol. Reprod. 2004, 71:1677-1687.
12. Castella S., Fouchecourt S., Teixeira-Gomes A.P., Vinh J., Belghazi M., Dacheux F., Dacheux J.L. Identification of a member of a new RNase a family specifically secreted by epididymal caput epithelium. Biol. Reprod. 2004, 70:319-328.
13. Chandler J.E., Painter C.L., Adkison R.W., Memon M.A., Hoyt P.G. Semen quality characteristics of dairy goats. J. Dairy Sci. 1988, 71:1638-1646.
14. Clulow J., Jones R.C., Hansen L.A. Micropuncture and cannulation studies of fluid composition and transport in the ductuli efferentes testis of the rat: comparisons with the homologous metanephric proximal tubule. Exp. Physiol. 1994, 79:915-928.
15. Colas G. Seasonal variations of sperm quality in adult Ile-de-France rams: II. Fertilizing ability and its relation to qualitative criteria in vitro. Reprod. Nutr. Dev. 1981, 21:399-407.
16. 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, 139:545-556.
17. D'Amours O., Bordeleau L.J., Frenette G., Blondin P., Leclerc P., Sullivan R. Binder of sperm 1 and epididymal sperm binding protein 1 are associated with different bull sperm subpopulations. Reproduction 2012, 143:759-771.
18. Dacheux J.L., Dacheux F. New insights into epididymal function in relation to sperm maturation. Reproduction 2014, 147:R27-R42.
19. Dacheux J.L., Voglmayr J.K. Sequence of sperm cell surface differentiation and its relationship to exogenous fluid proteins in the ram epididymis. Biol. Reprod. 1983, 29:1033-1046.
20. Dacheux J.L., Castella S., Gatti J.L., Dacheux F. Epididymal cell secretory activities and the role of proteins in boar sperm maturation. Theriogenology 2005, 63:319-341.
21. Dacheux J.L., Belleannee C., Guyonnet B., Labas V., Teixeira-Gomes A.P., Ecroyd H., Druart X., Gatti J.L., Dacheux F. The contribution of proteomics to understanding epididymal maturation of mammalian spermatozoa. Syst. Biol. Reprod. Med. 2012, 58:197-210.
22. Dacheux J.L. An in vitro luminal perfusion technique to study epididymal secretion. I.R.C.S. Med. Sci. 1980, 8:137.
23. David I., Kohnke P., Lagriffoul G., Praud O., Plouarboue F., Degond P., Druart X. Mass sperm motility is associated with fertility in sheep. Anim. Reprod. Sci. 2015, 161:75-81.
24. Ecroyd H., Sarradin P., Dacheux J.L., Gatti J.L. Compartmentalization of prion isoforms within the reproductive tract of the ram. Biol. Reprod. 2004, 71:993-1001.
25. Ecroyd H., Belghazi M., Dacheux J.L., Gatti J.L. The epididymal soluble prion protein forms a high- molecular-mass complex in association with hydrophobic proteins. Biochem. J. 2005, 392:211-219.
26. Fernandez Abella D., Da Costa M., Guerin Y., Dacheux J.L. Fertility of undiluted ram epididymal spermatozoa stored for several days at 4 °C. Anim.: Int. J. Anim. Biosci. 2015, 9:313-319.
27. Fouchecourt S., Dacheux F., Dacheux J.L. Glutathione- independent prostaglandin D2 synthase in ram and stallion epididymal fluids: origin and regulation. Biol. Reprod. 1999, 60:558-566.
28. Fouchecourt S., Metayer S., Locatelli A., Dacheux F., Dacheux J.L. Stallion epididymal fluid proteome: qualitative and quantitative characterization; secretion and dynamic changes of major proteins. Biol. Reprod. 2000, 62:1790-1803.
29. Free M.J., Schluntz G.A., Jaffe R.A. Respiratory gas tensions in tissues and fluids of the male rat reproductive tract. Biol. Reprod. 1976, 14:481-488.
30. Frenette G., Lessard C., Sullivan R. Selected proteins of prostasome-like particles from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol. Reprod. 2002, 67:308-313.
31. Fujihara Y., Tokuhiro K., Muro Y., Kondoh G., Araki Y., Ikawa M., Okabe M. Expression of TEX101, regulated by ACE, is essential for the production of fertile mouse spermatozoa. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:8111-8116.
32. Gatti J.L., Druart X., Guerin 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.
33. Gatti J.L., Metayer S., Belghazi M., Dacheux F., Dacheux J.L. Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol. Reprod. 2005, 72:1452-1465.
34. Gerena R.L., Irikura D., Urade Y., Eguchi N., Chapman D.A., Killian G.J. Identification of a fertility-associated protein in bull seminal plasma as lipocalin-type prostaglandin D synthase. Biol. Reprod. 1998, 58:826-833.
35. Gregory M., Cyr D.G. The blood-epididymis barrier and inflammation. Spermatogenesis 2014, 4:e979619.
36. Guyonnet B., Marot G., Dacheux J.L., Mercat M.J., Schwob S., Jaffrezic F., Gatti J.L. The adult boar testicular and epididymal transcriptomes. BMC Genomics 2009, 10:369.
37. Guyonnet B., Dacheux F., Dacheux J.L., Gatti J.L. The epididymal transcriptome and proteome provide some insights into new epididymal regulations. J. Androl. 2011, 32:651-664.
38. Hamann H., Jude R., Sieme H., Mertens U., Topfer-Petersen E., Distl O., Leeb T. A polymorphism within the equine CRISP3 gene is associated with stallion fertility in Hanoverian warmblood horses. Anim. Genet. 2007, 38:259-264.
39. Hermo L., Jacks D. Nature's ingenuity: bypassing the classical secretory route via apocrine secretion. Mol. Reprod. Dev. 2002, 63:394-410.
40. Holt W.V. Is semen analysis useful to predict the odds that the sperm will meet the egg?. Reprod. Domest. Anim. 2009, 44(Suppl. 3):31-38.
41. Ilio K.Y., Hess R.A. Structure and function of the ductuli efferentes: a review. Microsc. Res. Tech. 1994, 29:432-467.
42. Jelinsky S.A., Turner T.T., Bang H.J., Finger J.N., Solarz M.K., Wilson E., Brown E.L., Kopf G.S., Johnston D.S. The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides. Biol. Reprod. 2007, 76:561-570.
43. Johnston D.S., Jelinsky S.A., Bang H.J., Dicandeloro P., Wilson E., Kopf G.S., Turner T.T. The murine epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol. Reprod. 2005, 73:404-413.
44. Johnston D.S., Turner T.T., Finger J.N., Owtscharuk T.L., Kopf G.S., Jelinsky S.A. Identification of epididymis-specific transcripts in the mouse and rat by transcriptional profiling. Asian J. Androl. 2007, 9:522-527.
45. Jones R.C., Murdoch R.N. Regulation of the motility and metabolism of spermatozoa for storage in the epididymis of eutherian and marsupial mammals. Reprod. Fertil. Dev. 1996, 8:553-568.
46. Jones R.C., Dacheux J.L., Nixon B., Ecroyd H.W. Role of the epididymis in sperm competition. Asian J. Androl. 2007, 9:493-499.
47. Jones R.C. To store or mature spermatozoa? The primary role of the epididymis. Int. J. Androl. 1999, 22:57-67.
48. Kirchhoff C. CD52 is the 'major maturation-associated' sperm membrane antigen. Mol. Hum. Reprod. 1996, 2:9-17.
49. Kondoh G., Tojo H., Nakatani Y., Komazawa N., Murata C., Yamagata K., Maeda Y., Kinoshita T., Okabe M., Taguchi R., Takeda J. Angiotensin- converting enzyme is a GPI-anchored protein releasing factor crucial for fertilization. Nat. Med. 2005, 11:160-166.
50. Kwon W.S., Oh S.A., Kim Y.J., Rahman M.S., Park Y.J., Pang M.G. Proteomic approaches for profiling negative fertility markers in inferior boar spermatozoa. Sci. Rep. 2015, 5:13821.
51. Kwon W.S., Rahman M.S., Lee J.S., Yoon S.J., Park Y.J., Pang M.G. Discovery of predictive biomarkers for litter size in boar spermatozoa. Mol. Cell. Proteomics 2015, 14:1230-1240.
52. Labas V., Grasseau I., Cahier K., Gargaros A., Harichaux G., Teixeira-Gomes A.P., Alves S., Bourin M., Gerard N., Blesbois E. Qualitative and quantitative peptidomic and proteomic approaches to phenotyping chicken semen. J. Proteom. 2015, 112:313-335.
53. Labas V., Spina L., Belleannee C., Teixeira-Gomes A.P., Gargaros A., Dacheux F., Dacheux J.L. Analysis of epididymal sperm maturation by MALDI profiling and top-down mass spectrometry. J. Proteom. 2015, 113:226-243.
54. Li J.Y., Wang H.Y., Liu J., Liu Q., Zhang J.S., Wan F.C., Liu F.J., Jin S.H., Zhang Y.L. Transcriptome analysis of a cDNA library from adult human epididymis. DNA Res. 2008, 15:115-122.
55. Ma W., Xie S., Ni M., Huang X., Hu S., Liu Q., Liu A., Zhang J., Zhang Y. MicroRNA-29a inhibited epididymal epithelial cell proliferation by targeting nuclear autoantigenic sperm protein (NASP). J. Biol. Chem. 2012, 287:10189-10199.
56. Mieusset R., Quintana Casares P.I., Sanchez-Partida L.G., Sowerbutts S.F., Zupp J.L., Setchell B.P. The effects of moderate heating of the testes and epididymides of rams by scrotal insulation on body temperature, respiratory rate, spermatozoa output and motility, and on fertility and embryonic survival in ewes inseminated with frozen semen. Ann. N. Y. Acad. Sci. 1991, 637:445-458.
57. Milardi D., Grande G., Vincenzoni F., Castagnola M., Marana R. Proteomics of human seminal plasma: identification of biomarker candidates for fertility and infertility and the evolution of technology. Mol. Reprod. Dev. 2013, 80:350-357.
58. Nixon B., Stanger S.J., Mihalas B.P., Reilly J.N., Anderson A.L., Dun M.D., Tyagi S., Holt J.E., McLaughlin E.A. Next generation sequencing analysis reveals segmental patterns of microRNA expression in mouse epididymal epithelial cells. PLoS One 2015, 10:e0135605.
59. Nixon B., Stanger S.J., Mihalas B.P., Reilly J.N., Anderson A.L., Tyagi S., Holt J.E., McLaughlin E.A. The MicroRNA signature of mouse spermatozoa is substantially modified during epididymal maturation. Biol. Reprod. 2015, 93:91.
60. Parent S., Lefièvre L., Brindle Y., Sullivan R. Bull subfertility is associated with low levels of a sperm membrane antigen. Mol. Reprod. Dev. 1999, 52:57-65.
61. 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.
62. 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.
63. Penttinen J., Pujianto D.A., Sipila P., Huhtaniemi I., Poutanen M. Discovery in silico and characterization in vitro of novel genes exclusively expressed in the mouse epididymis. Mol. Endocrinol. 2003, 17:2138-2151.
64. Rickard J.P., Leahy T., Soleilhavoup C., Tsikis G., Labas V., Harichaux G., Lynch G.W., Druart X., de Graaf S.P. The identification of proteomic markers of sperm freezing resilience in ram seminal plasma. J. Proteom. 2015, 126:303-311.
65. Roncoletta M., Morani Eda S., Esper C.R., Barnabe V.H., Franceschini P.H. Fertility-associated proteins in Nelore bull sperm membranes. Anim. Reprod. Sci. 2006, 91:77-87.
66. Scott T.W., Wales R.G., Wallace J.C., White I.G. Composition of ram epididymal and testicular fluid and the biosynthesis of glycerylphosphorylcholine by the rabbit epididymis. J. Reprod. Fertil. 1963, 141:49-59.
67. Scott T.W., Voglmayr J.K., Setchell B.P. Lipid composition and metabolism in testicular and ejaculated ram spermatozoa. Biochem. J. 1967, 102:456-461.
68. Sharma U., Conine C.C., Shea J.M., Boskovic A., Derr A.G., Bing X.Y., Belleannee C., Kucukural A., Serra R.W., Sun F., Song L., Carone B.R., Ricci E.P., Li X.Z., Fauquier L., Moore M.J., Sullivan R., Mello C.C., Garber M., Rando O.J. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 2016, 351:391-396.
69. Soggiu A., Piras C., Hussein H.A., De Canio M., Gaviraghi A., Galli A., Urbani A., Bonizzi L., Roncada P. Unravelling the bull fertility proteome. Mol. Biosyst. 2013, 9:1188-1195.
70. Soleilhavoup C., Tsikis G., Labas V., Harichaux G., Kohnke P.L., Dacheux J.L., Guerin Y., Gatti J.L., de Graaf S.P., Druart X. Ram seminal plasma proteome and its impact on liquid preservation of spermatozoa. J. Proteom. 2014, 109:245-260.
71. Sullivan R. Male fertility markers, myth or reality. Anim. Reprod. Sci. 2004, 82-83:341-347.
72. Sullivan R. Epididymosomes: a heterogeneous population of microvesicles with multiple functions in sperm maturation and storage. Asian J. Androl. 2015, 17:726-729.
73. Thimon V., Metayer S., Belghazi M., Dacheux F., Dacheux J.L., Gatti J.L. Shedding of the germinal angiotensin I-converting enzyme (gACE) involves a serine protease and is activated by epididymal fluid. Biol. Reprod. 2005, 73:881-890.
74. Thimon V., Koukoui O., Calvo E., Sullivan R. Region-specific gene expression profiling along the human epididymis. Mol. Hum. Reprod. 2007, 13:691-704.
75. Turner T.T., Miller D.W., Avery E.A. Protein synthesis and secretion by the rat caput epididymidis in vivo: influence of the luminal microenvironment. Biol. Reprod. 1995, 52:1012-1019.
76. Vicente-Fiel S., Palacin I., Santolaria P., Yaniz J.L. A comparative study of sperm morphometric subpopulations in cattle, goat, sheep and pigs using a computer-assisted fluorescence method (CASMA-F). Anim. Reprod. Sci. 2013, 139:182-189.
77. Zhang J.S., Liu Q., Li Y.M., Hall S.H., French F.S., Zhang Y.L. Genome-wide profiling of segmental-regulated transcriptomes in human epididymis using oligo microarray. Mol. Cell. Endocrinol. 2006, 250:169-177.