Combined albumin and bicarbonate induces head-to-head sperm agglutination which physically prevents equine sperm-oviduct binding

Reproduction

Volumn 151, Issue 4, 2016, Pages 313-330

  Leemans, Bart ^a   Gadella, Bart M ^b,c   Stout, Tom A E ^b   Sostaric, Edita ^b   De Schauwer, Catharina ^a   Nelis, Hilde ^a   Hoogewijs, Maarten ^a   Van Soom, Ann ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; BICARBONATE; CALCIUM; CARBOHYDRATE; GLUCOSE; GLYCOSAMINOGLYCAN; GLYCOSAMINOGLYCAN POLYSULFATE; GLYCOSIDASE; LECTIN; MANNOSE; N ACETYLGALACTOSAMINE; N ACETYLNEURAMINIC ACID; ALBUMINOID; BUFFER;

ANIMAL CELL; ANTIGEN ANTIBODY REACTION; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; EJACULATION; EQUIDAE; FEMALE; FERTILIZATION; HEAD TO HEAD SPERM AGGLUTINATION; IN VITRO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SEMEN ANALYSIS; SPERM OVIDUCT BINDING; SPERMATOZOON CAPACITATION; SPERMATOZOON DENSITY; SPERMATOZOON HEAD; SPERMATOZOON TAIL; UTERINE TUBE MUCOSA; ANIMAL; DRUG EFFECTS; HORSE; METABOLISM; OVIDUCT;

ALBUMINS; ANIMALS; BICARBONATES; BUFFERS; FEMALE; HORSES; MALE; OVIDUCTS; SPERM AGGLUTINATION; SPERM CAPACITATION; SPERM HEAD;

EID: 84962480720     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-15-0471     Document Type: Article

References (82)

1. Aitken RJ, Gibb Z, Mitchell LA, Lambourne SR, Connaughton HS & De Iuliis GN 2012 Sperm motility is lost in vitro as a consequence of mitochondrial free radical production and the generation of electrophilic aldehydes but can be significantly rescued by the presence of nucleophilic thiols. Biology of Reproduction 87 110. (doi:10.1095/biolreprod.112.102020)
2. Bader H 1982 An investigation of sperm migration into the oviducts of the mare. Journal of Reproduction and Fertility. Supplement 32 59-64.
3. Ball BA, Dobrinski I, Fagnan MS & Thomas PG 1997 Distribution of glycoconjugates in the uterine tube (oviduct) of horses. American Journal of Veterinary Research 58 816-822.
4. Bedford JM 1970 Observations on some properties of a potent sperm-head agglutinin in the semen of a fertile rabbit. Journal of Reproduction and Fertility 22 193-198. (doi:10.1530/jrf.0.0220193)
5. Bergqvist AS, Ballester J, Johannisson A, Lundeheim N & Rodriguez-Martinez H 2007 Heparin and dermatan sulphate induced capacitation of frozen-thawed bull spermatozoa measured by merocyanine-540. Zygote 15 225-232. (doi:10.1017/S0967199407004182)
6. Boilard M, Bailey J, Collin S, Dufour M & Sirard MA 2002 Effect of bovine oviduct epithelial cell apical plasma membranes on sperm function assessed by a novel flow cytometric approach. Biology of Reproduction 67 1125-1132. (doi:10.1095/biolreprod67.4.1125)
7. Dam TK, Gabius HJ, Andre S, Kaltner H, Lensch M & Brewer CF 2005 Galectins bind to the multivalent glycoprotein asialofetuin with enhanced affinities and a gradient of decreasing binding constants. Biochemistry 44 12564-12571. (doi:10.1021/bi051144z)
8. De Mott RP, Lefebvre R & Suarez SS 1995 Carbohydrates mediate the adherence of hamster sperm to oviductal epithelium. Biology of Reproduction 52 1395-1403. (doi:10.1095/biolreprod52.6.1395)
9. Desantis S, Acone F, Corriero A, Deflorio M, Zubani D, Ventriglia G, Palmieri G & De Metrio G 2004 Distribution of sialoglycoconjugates in the oviductal isthmus of the horse during anoestrus, oestrus and pregnancy: a lectin histochemistry study. European Journal of Histochemistry 48 403-412. (doi:10.4081/914)
10. Desantis S, Ventriglia G, Zubani D, Corriero A, Deflorio M, Acone F, Palmieri G & De Metrio G 2005 Differential lectin binding patterns in the oviductal ampulla of the horse during oestrus. European Journal of Histochemistry 49 139-149.
11. Dobrinski I, Ignotz GG, Thomas PG & Ball BA 1996a Role of carbohydrates in the attachment of equine spermatozoa to uterine tubal (oviductal) epithelial cells in vitro. American Journal of Veterinary Research 57 1635-1639.
12. Dobrinski I, Suarez SS & Ball BA 1996b Intracellular calcium concentration in equine spermatozoa attached to oviductal epithelial cells in vitro. Biology of Reproduction 54 783-788. (doi:10.1095/biolreprod54.4.783)
13. Dobrinski I, Smith TT, Suarez SS & Ball BA 1997 Membrane contact with oviductal epithelium modulates the intracellular calcium concentration of equine spermatozoa in vitro. Biology of Reproduction 56 861-869. (doi:10.1095/biolreprod56.4.861)
14. Dobrinski I, Jacob JR, Tennant BC & Ball BA 1999 Generation of an equine oviductal epithelial cell line for the study of sperm-oviduct interactions. Theriogenology 52 875-885. (doi:10.1016/S0093-691X (99) 00179-X)
15. Dott HM & Walton A 1960 Effects of dilution and washing on ram spermatozoa studied by the flow dialysis technique. Journal of Reproduction and Fertility 1 350-367. (doi:10.1530/jrf.0.0010350)
16. Ellington JE, Ignotz GG, Varner DD, Marcucio RS, Mathison P & Ball BA 1993 In vitro interaction between oviduct epithelial and equine sperm. Archives of Andrology 31 79-86. (doi:10.3109/01485019308988384)
17. Flesch FM, Voorhout WF, Colenbrander B, Van Golde LM & Gadella BM 1998 Use of lectins to characterize plasma membrane preparations from boar spermatozoa: a novel technique for monitoring membrane purity and quantity. Biology of Reproduction 59 1530-1539. (doi:10.1095/biolreprod59.6.1530)
18. Flesch FM, Brouwers JF, Nievelstein PF, Verkleij AJ, Van Golde LM, Colenbrander B & Gadella BM 2001 Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. Journal of Cell Science 114 3543-3555.
19. Van Gestel RA, Brewis IA, Ashton PR, Helms JB, Brouwers JF & Gadella BM 2005 Capacitation-dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells. Molecular Human Reproduction 11 583-590. (doi:10.1093/molehr/gah200)
20. Van Gestel RA, Brewis IA, Ashton PR, Brouwers JF & Gadella BM 2007 Multiple proteins present in purified porcine sperm apical plasma membranes interact with the zona pellucida of the oocyte. Molecular Human Reproduction 13 445-454. (doi:10.1093/molehr/gam030)
21. Gualtieri R & Talevi R 2000 In vitro-cultured bovine oviductal cells bind acrosome-intact sperm and retain this ability upon sperm release. Biology of Reproduction 62 1754-1762. (doi:10.1095/biolreprod62. 6.1754)
22. Gualtieri R, Boni R, Tosti E, Zagami M & Talevi R 2005 Intracellular calcium and protein tyrosine phosphorylation during the release of bovine sperm adhering to the fallopian tube epithelium in vitro. Reproduction 129 51-60. (doi:10.1530/rep. 1.00374)
23. Gualtieri R, Mollo V, Duma G & Talevi R 2009 Redox control of surface protein sulphhydryls in bovine spermatozoa reversibly modulates sperm adhesion to the oviductal epithelium and capacitation. Reproduction 138 33-43. (doi:10.1530/REP-08-0514)
24. Gualtieri R, Mollo V, Barbato V & Talevi R 2010 Ability of sulfated glycoconjugates and disulfide-reductants to release bovine epididymal sperm bound to the oviductal epithelium in vitro. Theriogenology 73 1037-1043. (doi:10.1016/j.theriogenology.2009.11.030)
25. Harayama H, Kato S & Hammerstedt RH 1996 Electrophoretic characterization of boar epididymal antiagglutinin. Biology of Reproduction 55 325-332. (doi:10.1095/biolreprod55.2.325)
26. Harayama H, Miyake M, Shidara O, Iwamoto E & Kato S 1998 Effects of calcium and bicarbonate on head-to-head agglutination in ejaculated boar spermatozoa. Reproduction, Fertility, and Development 10 445-450. (doi:10.1071/RD98124)
27. Harayama H, Magargee SF, Kunze E, Shidara O, Iwamoto E, Arikawa S, Miyake M, Kato S & Hammerstedt RH 1999 Changes in epididymal protein anti-agglutinin on ejaculated boar spermatozoa during capacitation in vitro. Reproduction, Fertility, and Development 11 193-199. (doi:10.1071/RD99056)
28. Harayama H, Liao PC, Gage DA, Miyake M, Kato S & Hammerstedt RH 2000a Biochemical characterization of sialoprotein "anti-agglutinin" purified from boar epididymal and seminal plasma. Molecular Reproduction and Development 55 96-103. (doi:10.1002/(SICI) 1098-2795 (200001) 55:1<96::AID-MRD13>3.0. CO;2-J)
29. Harayama H, Miyake M & Kato S 2000b Role of cyclic adenosine 3', 5'-monophosphate and serum albumin in head-to-head agglutination of boar spermatozoa. Reproduction, Fertility, and Development 12 307-318. (doi:10.1071/RD00030)
30. Harper MJ 1973 Stimulation of sperm movement from the isthmus to the site of fertilization in the rabbit oviduct. Biology of Reproduction 8 369-377.
31. Hayase T, Rice KG, Dziegielewska KM, Kuhlenschmidt M, Reilly T & Lee YC 1992 Comparison of N-glycosides of fetuins from different species and human a 2-HS-glycoprotein. Biochemistry 31 4915-4921. (doi:10.1021/bi00135a024)
32. Holt WV 2011 Mechanisms of sperm storage in the female reproductive tract: an interspecies comparison. Reproduction in Domestic Animals 46(Suppl 2) 68-74. (doi:10.1111/j.1439-0531.2011.01862.x)
33. Hunter RH 1981 Sperm transport and reservoirs in the pig oviduct in relation to the time of ovulation. Journal of Reproduction and Fertility 63 109-117. (doi:10.1530/jrf.0.0630109)
34. Hunter RH 2003 Reflections upon sperm-endosalpingeal and sperm-zona pellucida interactions in vivo and in vitro. Reproduction in Domestic Animals 38 147-154. (doi:10.1046/j.1439-0531.2003.00402.x)
35. Hunter RH 2011 Sperm head binding to epithelium of the oviduct isthmus is not an essential preliminary to mammalian fertilization - review. Zygote 19 265-269. (doi:10.1017/S0967199410000341)
36. Hunter RH & Nichol R 1983 Transport of spermatozoa in the sheep oviduct: preovulatory sequestering of cells in the caudal isthmus. Journal of Experimental Zoology 228 121-128. (doi:10.1002/jez.1402280113)
37. Hunter RH & Wilmut I 1984 Sperm transport in the cow: peri-ovulatory redistribution of viable cells within the oviduct. Reproduction, Nutrition, Development 24 597-608. (doi:10.1051/rnd:19840508)
38. Hunter RH, Flechon B & Flechon JE 1991 Distribution, morphology and epithelial interactions of bovine spermatozoa in the oviduct before and after ovulation: a scanning electron microscope study. Tissue Cell 23 641-656. (doi:10.1016/0040-8166 (91) 90020-T)
39. Kadirvel G, Machado SA, Korneli C, Collins E, Miller P, Bess KN, Aoki K, Tiemeyer M, Bovin N & Miller DJ 2002 Porcine sperm bind to specific 6-sialylated biantennary glycans to form the oviduct reservoir. Biology of Reproduction 87 147. (doi:10.1095/biolreprod.112.103879)
40. Leemans B, Gadella BM, Sostaric E, Nelis H, Stout TA, Hoogewijs M & Van Soom A 2014 Oviduct binding and elevated environmental ph induce protein tyrosine phosphorylation in stallion spermatozoa. Biology of Reproduction 91 13. (doi:10.1095/biolreprod.113.116418)
41. Leemans B, Gadella BM, Stout TA, Nelis H, Hoogewijs M & Van Soom A 2015 An alkaline follicular fluid fraction induces capacitation and limited release of oviduct epithelium-bound stallion sperm. Reproduction 150 193-208. (doi:10.1530/REP-15-0178)
42. Lefebvre R, Chenoweth PJ, Drost M, Le Clear CT, MacCubbin M, Dutton JT & Suarez SS 1995a Characterization of the oviductal sperm reservoir in cattle. Biology of Reproduction 53 1066-1074. (doi:10.1095/biolreprod53.5.1066)
43. Lefebvre R, De Mott R, Suarez S & Samper J 1995b Specific inhibition of equine sperm binding to oviductal epithelium. In Equine Reproduction VI (Biology of Reproduction Monograph 1), pp 689-696. Eds D Sharp & FW Bazer. Madison, WI: Society for the Study of Reproduction.
44. Lefebvre R, Lo MC & Suarez SS 1997 Bovine sperm binding to oviductal epithelium involves fucose recognition. Biology of Reproduction 56 1198-1204. (doi:10.1095/biolreprod56.5.1198)
45. Lindahl PE 1966 Sperm agglutinating and anti-agglutinating factors in normal follicular fluid from cattle. International Journal of Fertility 11 297-305.
46. Lindahl PE 1973 Activators of the ATP-dependent surface reaction in the apical cell membrane of the bull-sperm head, causing head-to-head association. Experimental Cell Research 81 413-431. (doi:10.1016/0014-4827 (73) 90531-4)
47. Lindahl PE & Sjoblom P 1981 On mechanisms of head-to-head association in bovine spermatozoa. Biology of Reproduction 25 29-43. (doi:10.1095/biolreprod25.1.29)
48. Loux SC, Crawford KR, Ing NH, Gonzalez-Fernandez L, Macias-Garcia B, Love CC, Varner DD, Velez IC, Choi YH & Hinrichs K 2003 CatSper and the relationship of hyperactivated motility to intracellular calcium and pH kinetics in equine sperm. Biology of Reproduction 89 123. (doi:10.1095/biolreprod.113.111708)
49. McPartlin LA, Littell J, Mark E, Nelson JL, Travis AJ & Bedford-Guaus SJ 2008 A defined medium supports changes consistent with capacitation in stallion sperm, as evidenced by increases in protein tyrosine phosphorylation and high rates of acrosomal exocytosis. Theriogenology 69 639-650. (doi:10.1016/j.theriogenology.2007.11.016)
50. Motoyama K, Nakashima Y, Aramaki Y, Hirayama F, Uekama K & Arima H 2011 In Vitro gene delivery mediated by asialofetuin-appended cationic liposomes associated with g-cyclodextrin into hepatocytes. Journal of Drug Delivery 2011 476137. (doi:10.1155/2011/476137)
51. Nelis H, D'Herde K, Goossens K, Vandenberghe L, Leemans B, Forier K, Smits K, Braeckmans K, Peelman L & Van Soom A 2004 Equine oviduct explant culture: a basic model to decipher embryo-maternal communication. Reproduction, Fertility, and Development 26 954-966. (doi:10.1071/RD13089)
52. Parrish JJ 2014 Bovine in vitro fertilization: in vitro oocyte maturation and sperm capacitation with heparin. Theriogenology 81 67-73. (doi:10.1016/j.theriogenology.2013.08.005)
53. Parrish JJ, Susko-Parrish J, Winer MA & First NL 1988 Capacitation of bovine sperm by heparin. Biology of Reproduction 38 1171-1180. (doi:10.1095/biolreprod38.5.1171)
54. Parrish JJ, Susko-Parrish JL & First NL 1989a Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH. Biology of Reproduction 41 683-699. (doi:10.1095/biolreprod41.4.683)
55. Parrish JJ, Susko-Parrish JL, Handrow RR, Sims MM & First NL 1989b Capacitation of bovine spermatozoa by oviduct fluid. Biology of Reproduction 40 1020-1025. (doi:10.1095/biolreprod40.5.1020)
56. Rath D, Long CR, Dobrinsky JR, Welch GR, Schreier LL & Johnson LA 1999 In vitro production of sexed embryos for gender preselection: high-speed sorting of X-chromosome-bearing sperm to produce pigs after embryo transfer. Journal of Animal Science 77 3346-3352.
57. Reeve L, Ledger WL & Pacey AA 2003 Does the Arg-Gly-Asp (RGD) adhesion sequence play a role in mediating sperm interaction with the human endosalpinx? Human Reproduction 18 1461-1468. (doi:10.1093/humrep/deg296)
58. Roth J 2002 Protein N-glycosylation along the secretory pathway: relationship toorganelle topography and function, protein quality control, cell interactions. Chemical Reviews 102 285-303. (doi:10.1021/cr000423j)
59. Sabeur K & Ball BA 2007 Characterization of galactose-binding proteins in equine testis and spermatozoa. Animal Reproduction Science 101 74-84. (doi:10.1016/j.anireprosci.2006.08.028)
60. Scott MA, Liu IK, Overstreet JW & Enders AC 2000 The structural morphology and epithelial association of spermatozoa at the uterotubal junction: a descriptive study of equine spermatozoa in situ using scanning electron microscopy. Journal of Reproduction and Fertility. Supplement 415-421.
61. Senger PL & Saacke RG 1976 Serum-induced head-to-head agglutination of bovine spermatozoa. Journal of Reproduction and Fertility 47 215-219. (doi:10.1530/jrf.0.0470215)
62. Smith TT & Nothnick WB 1997 Role of direct contact between spermatozoa and oviductal epithelial cells in maintaining rabbit sperm viability. Biology of Reproduction 56 83-89. (doi:10.1095/biolreprod56.1.83)
63. Sorensen MB, Stoltenberg M, Danscher G & Ernst E 1999 Chelation of intracellular zinc ions affects human sperm cell motility. Molecular Human Reproduction 5 338-341. (doi:10.1093/molehr/5.4.338)
64. Sostaric E, Van De Lest CH, Colenbrander B & Gadella BM 2005 Dynamics of carbohydrate affinities at the cell surface of capacitating bovine sperm cells. Biology of Reproduction 72 346-357. (doi:10.1095/biolreprod. 104.029330)
65. Sostaric E, Dieleman SJ, Van De Lest CH, Colenbrander B, Vos PL, Garcia-Gil N & Gadella BM 2008 Sperm binding properties and secretory activity of the bovine oviduct immediately before and after ovulation. Molecular Reproduction and Development 75 60-74. (doi:10.1002/mrd.20766)
66. Suarez SS 1987 Sperm transport and motility in the mouse oviduct: observations in situ. Biology of Reproduction 36 203-210. (doi:10.1095/biolreprod36.1.203)
67. Suarez SS 1998 The oviductal sperm reservoir in mammals: mechanisms of formation. Biology of Reproduction 58 1105-1107. (doi:10.1095/biolreprod58.5.1105)
68. Suarez SS 2001 Carbohydrate-mediated formation of the oviductal sperm reservoir in mammals. Cells, Tissues, Organs 168 105-112. (doi:10.1159/000016811)
69. Suarez SS 2008a Control of hyperactivation in sperm. Human Reproduction Update 14 647-657. (doi:10.1093/humupd/dmn029)
70. Suarez SS 2008b Regulation of sperm storage and movement in the mammalian oviduct. International Journal of Developmental Biology 52 455-462. (doi:10.1387/ijdb.072527ss)
71. Suarez SS, Revah I, Lo M & Kolle S 1998 Bull sperm binding to oviductal epithelium is mediated by a Ca2+-dependent lectin on sperm that recognizes Lewis-a trisaccharide. Biology of Reproduction 59 39-44. (doi:10.1095/biolreprod59.1.39)
72. Takasaki S, Mizuochi T & Kobata A 1982 Hydrazinolysis of asparaginelinked sugar chains to produce free oligosaccharides. Methods in Enzymology 83 263-268.
73. Talevi R & Gualtieri R 2001 Sulfated glycoconjugates are powerful modulators of bovine sperm adhesion and release from the oviductal epithelium in vitro. Biology of Reproduction 64 491-498. (doi:10.1095/biolreprod64.2.491)
74. Tarentino AL & Plummer TH Jr 1987 Peptide-N4-(N-acetyl-β-glucosaminyl) asparagine amidase and endo-β-N-acetylglucosaminidase from Flavobacterium meningosepticum. Methods in Enzymology 138 770-778.
75. Thomas PGA, Ignotz GG, Ball BA, Miller PG, Brinsko SP & Currie B 1995 Isolation, culture, and characterization of equine oviduct epithelial-cells in-vitro. Molecular Reproduction and Development 41 468-478. (doi:10.1002/mrd.1080410409)
76. Tremoleda JL, Stout TA, Lagutina I, Lazzari G, Bevers MM, Colenbrander B & Galli C 2003 Effects of in vitro production on horse embryo morphology, cytoskeletal characteristics, and blastocyst capsule formation. Biology of Reproduction 69 1895-1906.
77. Tsai PS, Garcia-Gil N, Van Haeften T & Gadella BM 2010 How pig sperm prepares to fertilize: stable acrosome docking to the plasma membrane. PLoS ONE 5 e11204. (doi:10.1371/journal.pone.0011204)
78. Tsai PS, Brewis IA, Van Maaren J & Gadella BM 2012 Involvement of complexin 2 in docking, locking and unlocking of different SNARE complexes during sperm capacitation and induced acrosomal exocytosis. PLoS ONE 7 e32603. (doi:10.1371/journal.pone.0032603)
79. Varner DD, Forrest DW, Fuentes F, Taylor TS, Hooper RN, Brinsko SP & Blanchard TL 1991 Measurements of glycosaminoglycans in follicular, oviductal and uterine fluids of mares. Journal of Reproduction and Fertility. Supplement 44 297-306.
80. Yanagimachi R & Chang MC 1963 Sperm ascent through the oviduct of the hamster and rabbit in relation to the time of ovulation. Journal of Reproduction and Fertility 6 413-420. (doi:10.1530/jrf.0.0060413)
81. Yang DH, McMillan AG, Standley NT, Shannon P & Xu ZZ 2012 Extracellular calcium is involved in egg yolk-induced head-to-head agglutination of bull sperm. Theriogenology 78 1476-1486. (doi:10. 1016/j.theriogenology.2012.06.021)
82. Zhang H, Li XJ, Martin DB & Aebersold R 2003 Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nature Biotechnology 21 660-666. (doi:10.1038/nbt827)