Effect of recombinant and native buffalo OVGP1 on sperm functions and in vitro embryo development: a comparative study
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摘要
Background: An oviduct-specific glycoprotein, OVGP1, is synthesized and secreted by non-ciliated epithelial cells of the mammalian oviduct which provides an essential milieu for reproductive functions. The present study reports the effects of recombinant buffalo OVGP1 that lacks post-translational modifications, and native Buffalo OVGP1 isolated from oviductal tissue, on frozen-thawed sperm functions and in vitro embryo development.Results: The proportion of viable sperms was greater(P < 0.05) in the recombinant OVGP1-treated group compared to the native OVGP1-treated group at 2 h, 3 h, and 4 h of incubation. The proportion of motile sperms at3 h and 4 h of incubation; and membrane-intact sperms at 4 h was greater(P < 0.05) in the native OVGP1-treated group compared to the control and recombinant OVGP1-treated groups. The proportion of capacitated and acrosome-reacted sperms was greater(P < 0.05) in the native OVGP1-treated group compared to the recombinant OVGP1 group at 4 h. The rates of cleavage of embryos and their development to the blastocyst stage were greater(P < 0.05) in the presence of either native or recombinant OVGP1 in comparison to control at 10 μg/mL concentration as compared to 5 or 20 μg/mL.Conclusions: The study suggests that both native and recombinant OVGP1 impart a positive effect on various sperm features and in vitro embryo development. However, native OVGP1 was found to have a more pronounced effect in comparison to recombinant non-glycosylated OVGP1 on various sperm functions except viability. Hence,our current findings infer that glycosylation of OVGP1 might be essential in sustaining the sperm functions but not the in vitro embryo development.
Background: An oviduct-specific glycoprotein, OVGP1, is synthesized and secreted by non-ciliated epithelial cells of the mammalian oviduct which provides an essential milieu for reproductive functions. The present study reports the effects of recombinant buffalo OVGP1 that lacks post-translational modifications, and native Buffalo OVGP1 isolated from oviductal tissue, on frozen-thawed sperm functions and in vitro embryo development.Results: The proportion of viable sperms was greater(P < 0.05) in the recombinant OVGP1-treated group compared to the native OVGP1-treated group at 2 h, 3 h, and 4 h of incubation. The proportion of motile sperms at3 h and 4 h of incubation; and membrane-intact sperms at 4 h was greater(P < 0.05) in the native OVGP1-treated group compared to the control and recombinant OVGP1-treated groups. The proportion of capacitated and acrosome-reacted sperms was greater(P < 0.05) in the native OVGP1-treated group compared to the recombinant OVGP1 group at 4 h. The rates of cleavage of embryos and their development to the blastocyst stage were greater(P < 0.05) in the presence of either native or recombinant OVGP1 in comparison to control at 10 μg/mL concentration as compared to 5 or 20 μg/mL.Conclusions: The study suggests that both native and recombinant OVGP1 impart a positive effect on various sperm features and in vitro embryo development. However, native OVGP1 was found to have a more pronounced effect in comparison to recombinant non-glycosylated OVGP1 on various sperm functions except viability. Hence,our current findings infer that glycosylation of OVGP1 might be essential in sustaining the sperm functions but not the in vitro embryo development.
Background: An oviduct-specific glycoprotein, OVGP1, is synthesized and secreted by non-ciliated epithelial cells of the mammalian oviduct which provides an essential milieu for reproductive functions. The present study reports the effects of recombinant buffalo OVGP1 that lacks post-translational modifications, and native Buffalo OVGP1 isolated from oviductal tissue, on frozen-thawed sperm functions and in vitro embryo development.Results: The proportion of viable sperms was greater(P < 0.05) in the recombinant OVGP1-treated group compared to the native OVGP1-treated group at 2 h, 3 h, and 4 h of incubation. The proportion of motile sperms at3 h and 4 h of incubation; and membrane-intact sperms at 4 h was greater(P < 0.05) in the native OVGP1-treated group compared to the control and recombinant OVGP1-treated groups. The proportion of capacitated and acrosome-reacted sperms was greater(P < 0.05) in the native OVGP1-treated group compared to the recombinant OVGP1 group at 4 h. The rates of cleavage of embryos and their development to the blastocyst stage were greater(P < 0.05) in the presence of either native or recombinant OVGP1 in comparison to control at 10 μg/mL concentration as compared to 5 or 20 μg/mL.Conclusions: The study suggests that both native and recombinant OVGP1 impart a positive effect on various sperm features and in vitro embryo development. However, native OVGP1 was found to have a more pronounced effect in comparison to recombinant non-glycosylated OVGP1 on various sperm functions except viability. Hence,our current findings infer that glycosylation of OVGP1 might be essential in sustaining the sperm functions but not the in vitro embryo development.
引文
1.Buhi WC.Characterization and biological roles of oviduct-specific,oestrogen-dependent glycoprotein.Reproduction.2002;123:355-62.
2.Buhi WC,Alvarez IM,Kouba AJ.Secreted proteins of the oviduct.Cells Tissues Organs.2000;166:165-79.
3.Sutton R,Nancarrow CD,Wallace ALC,Rigby NW.Identification of an oestrus associated glycoprotein in oviducal fluid of the sheep.J Reprod Fertil.1984;72:415-22.
4.Robitaille G,St-Jacques S,Potier M,Bleau G.Characterization of an oviductal glycoprotein associated with the ovulated hamster oocyte.Biol Reprod.1988;38:687-94.
5.Verhage HG,Fazleabas AT,Donnelly K.The in vitro synthesis and release of proteins by the human oviduct.Endocrinology.1988;122:1639-45.
6.Kapur RP,Johnson LV.Ultrastructural evidence that specialized regions of the murine oviduct contribute a glycoprotein to the extracellular matrix of mouse oocytes.Anat Rec.1988;221:720-9.
7.Boice ML,Geisert RD,Blair RM,Verhage HG.Identification and characterization of bovine oviductal glycoproteins synthesized at estrus.Biol Reprod.1990;43:457-65.
8.Buhi WC,Alvarez IM,Sudhipong V,Dones-Smith MM.Identification and characterization of de novo-synthesized porcine oviductal secretory protein.Biol Reprod.1990;43:929-38.
9.Abe H,Onodera M,Sugawara S.Immunological detection and characterization of an estrus-associated antigen in the goat oviduct.J Exp Zool.1995;272:134-41.
10.Verhage HG,Fazleabas AT,Mavrogianis PA,O’Day-Bowman MB,Donnelly KM,Arias EB,et al.The baboon oviduct:characteristics of an oestradiol-dependent oviduct-specific glycoprotein.Hum Reprod Update.1997;3:541-52.
11.Verhage HG,Mavrogianis PA,Boomsma RA,Schmidt A,Brenner RM,Slayden OV,et al.Immunologic and molecular characterization of an estrogendependent glycoprotein in the rhesus(Macaca mulatta)oviduct.Biol Reprod.1997;57:525-31.
12.Oliphant G,Reynolds AB,Smith PF,Ross PR,Marta JS.Immunocytochemical localization and determination of hormone induced synthesis of the sulfated oviductal glycoproteins.Biol Reprod.1984;31:165-74.
13.Buhi WC,O’Brien B,Alvarez IM,Erdos G,Dubois D.Immunogold localization of porcine oviductal secretory proteins within the zona pellucida,perivitelline space,and plasma membrane of oviductal and uterine oocytes and early embryos.Biol Reprod.1993;48:1274-83.
14.Boice ML,Mc Carthy TJ,Mavrogianis PA,Fazleabas AT,Verhage HG.Localization of oviductal glycoproteins within the zona pellucida and perivitelline space of ovulated ova and early embryos inbaboons(Papio anubis).Biol Reprod.1990;43:340-6.
15.Gandolfi F,Modina S,Brevini TAL,Galli C,Moor RM,Lauria A.Oviduct ampullary epithelium contributes a glycoprotein to the zona pellucida,perivitelline space and blastomeres membrane of sheep embryos.Eur JBasic Appl Histochem.1991;35:383-92.
16.Kan FWK,Roux E,Bleau G.Immunolocalization of oviductin in endocytic compartments in the blastomeres of developing embryos in the golden hamster.Biol Reprod.1993;48:77-88.
17.O’Day-Bowman MB,Mavrogianis PA,Reuter LM,Johnson DE,Fazleabas AT,Verhage HG.Association of oviduct specific glycoproteins with human and baboon(Papio anubis)ovarian oocytes and enhancement of human sperm binding to human hemizonae following in vitro incubation.Biol Reprod.1996;54:60-9.
18.Pradeep MA,Jagadeesh J,De AK,Kaushik JK,Malakar D,Kumar S,et al.Purification,sequence characterization and effect of goat oviduct-specific glycoprotein on in vitro embryo development.Theriogenology.2011;75:1005-15.
19.Martus NS,Verhage HG,Mavrogianis PA,Thibodeaux JK.Enhancement of bovine oocyte fertilization in vitro with a bovine oviductal specific glycoprotein.J Reprod Fertil.1998;113:323-9.
20.Kumaresan A,Ansari MR,Abhishek G.Effect of buffalo oviductal and follicular fluid proteins on in vitro sperm capacitation.Indian J Anim Sci.2006;76:204-7.
21.Kumaresan A,Johannisson A,Humblot P,Bergqvist AS.Oviductal fluid modulates the dynamics of tyrosine phosphorylation in cryopreserved boar spermatozoa during capacitation.Mol Reprod Dev.2012;79(8):525-40.
22.Kumaresan A,Johannisson A,Bergqvist AS.Sperm function during incubation with oestrus oviductal fluid differs in bulls with different fertility.Reprod Fertil Dev.2016;doi:10.1071/RD15474.[Epub ahead of print].
23.Kumaresan A,González R,Johannisson A,Berqvist A-S.Dynamic quantification of intracellular calcium and protein tyrosine phosphorylation in cryopreserved boar spermatozoa during short-time incubation with oviductal fluid.Theriogenology.2014;82(8):1145-53.
24.Satoh T,Abe H,Sendai Y,Iwata H,Hoshi H.Biochemical characterization of a bovine oviduct-specific sialo-glycoprotein that sustains sperm viability in vitro.Biochim Biophys Acta.1995;1266:117-23.
25.Algarra B,Han L,Soriano-úbeda C,Avilés M,Coy P,Jovine L,et al.The C-terminal region of OVGP1 remodels the zona pellucida and modifies fertility parameters.Sci Rep.2016;6:32556.
26.Srivastava AK,Kumaresan A,Manimaram A,Prasad S.Mastitis in dairy animals an update.India:Satish Serial Publishing;2014.
27.Yang X,Kubota C,Suzuki H,Taneja M,Bols PE,Presicce GA.Control of oocyte maturation in cows-biological factors.Theriogenology.1998;49:471-82.
28.Hasler JF.The current status of oocyte recovery,in vitro embryo production,and embryo transfer in domestic animals,with an emphasis on the bovine.J Anim Sci.1998;76(3):52-74.
29.Anand T,Kumar D,Chauhan MS,Manik RS,Palta P.Cysteamine supplementation of in vitro maturation medium,in vitro culture medium or both media promotes in vitro development of buffalo(Bubalus bubalis)embryos.Reprod Fertil Dev.2008;20:253-7.
30.Janjanam J,Singh S,Choudhary S,Pradeep MA,Kumar S,Kumaresan A,et al.Molecular cloning,sequence characterization and heterologous expression of buffalo(Bubalus bubalis)oviduct-specific glycoprotein in E.coli.Mol Biol Rep.2012;39:10031-43.
31.Sendai Y,Abe H,Kikuchi M,Satoh T,Hoshi H.Purification and molecular cloning of bovine oviduct-specific glycoprotein.Biol Reprod.1994;50:927-34.
32.Garner DL,Johnson LA.Viability assessment of mammalian sperm using SYBR-14 and propidium iodide.Biol Reprod.1995;53(2):276-84.
33.Singh RK,Kumaresan A,Chhillar S,Rajak SK,Tripathi UK,Nayak S,et al.Identification of suitable combinations of in vitro sperm-function test for the prediction of fertility in buffalo bull.Theriogenology.2016;86(9):2263-71.
34.Wang WH,Abeydeera LR,Fraser LR,Niwa K.Functional analysis using chlortetracycline fluorescence and in vitro fertilization of frozen-thawed ejaculated boar spermatozoa incubated in a protein-free chemically defined medium.J Reprod Fertil.1995;104:305-13.
35.Keefer CL,Stice SL,Matihews DL.Bovine inner cell mass cells as donor nuclei in the production of nuclear transfer embryos and calves.Biol Reprod.1994;50:935-9.
36.Brackett BG,Oliphant G.Capacitation of rabbit spermatozoa in vitro.Biol Reprod.1975;12:260-74.
37.Chauhan MS,Singla SK,Palta P,Manik RS,Madan ML.In vitro maturation and fertilization,and subsequent development of buffalo(Bubalus bubalis)embryos:effect of oocyte quality and type of serum.Reprod Fert Dev.1998;10:173-7.
38.Kumar D,Palta P,Manik RS,Singla SK,Chauhan MS.Effect of culture media and serum supplementation on the development of in vitro fertilized buffalo embryos.Indian J Anim Sci.2007;77:697-701.
39.Hribal R,Hachen A,Jewgenow K,Zahmel J,Fernandez-Gonzalez L,Braun BC.The influence of recombinant feline Oviductin on different aspects of domestic cat(Felis catus)IVF and embryo quality.Theriogenology.2014;82:742-9.
40.Kumaresan A,Ansari MR,Garg A.Modulation of post thaw sperm functions with oviductal proteins in buffaloes.Anim Reprod Sci.2005;90:73-84.
41.Kumaresan A,Ansari MR,Abhishek G,Meena K.Effect of oviductal proteins on sperm functions and lipid peroxidation levels during cryopreservation in buffaloes.Anim Reprod Sci.2006;93:246-57.
42.Mc Nutt TL,Olds-Clarke P,Way AL,Suarez SS,Killian GJ.Effect of follicular or oviductal fluids on movement characteristics of bovine sperm during capacitation in vitro.J Androl.1994;15:328-36.
43.Imam S,Ansari MR,Ahmed N,Kumaresan A.Effect of oviductal fluid proteins on buffalo sperm characteristics during cryopreservation.Theriogenology.2008;69(8):925-31.
44.Kumaresan A,Garg A,Suresh V,Ansari MR.Effect of follicular protein on post-thaw characteristics of buffalo spermatozoa.Indian J Anim Reprod.2003;24:103-5.
45.Prathalingam NS,Watson PF,Revel SG,Busby J,Holt WV.The response of bovine spermatozoa to bicarbonate and its use to assess the influence of added oviductal epithelial proteins on cryopreservation.J Androl.2007;28(3):407-15.
46.Kan FWK,Esperanzate PWB.Surface mapping of binding of Oviductin to the plasma membrane of golden hamster spermatozoa during in-vitro capacitation and acrosome reaction.Mol Reprod Dev.2006;73:756-66.
47.Yang X,Zhao Y,Yang X,Kan FW.Recombinant hamster Oviductin is biologically active and exerts positive effects on sperm functions and sperm-oocyte binding.PLo S One.2015;10(4):e0123003.
48.Zhao Y,Yang X,Jia Z,Reid RL,Leclerc P,Kan FW.Recombinant human oviductin regulates protein tyrosine phosphorylation and acrosome reaction.Reproduction.2016;152(5):561-73.
49.Mc Bride DS,Boisvert C,Bleau G,Kan FW.Detection of nascent and/or mature forms of Oviductin in the female reproductive tract and postovulatory oocytes by use of a polyclonal antibody against recombinant hamster Oviductin.J Histochem Cytochem.2004;52:1001-9.
50.Mc Bride DS,Brockhausen I,Kan FW.Detection of glycosyltransferases in the golden hamster(Mesocricetusauratus)oviduct and evidence for the regulation of O-glycan biosynthesis during the estrous cycle.Biochim Biophys Acta.2005;1721:107-15.
51.Coy P,Canovas S,Mondejar I,Saavedra MD,Romar R,Grullon L,et al.Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy.Proc Natl Acad Sci U S A.2008;105(41):15809-14.
52.Ballester L,Romero-Aguirregomezcorta J,Soriano-úbeda C,Matás C,Romar R,Coy P.Timing of oviductal fluid collection,steroid concentrations,and sperm preservation method affect porcine in vitro fertilization efficiency.Fertil Steril.2014;102:1762-8.
53.Kouba AJ,Abeydeera LR,Alvarez IM,Day BN,Buhi WC.Effects of the porcine oviduct-specific glycoprotein on fertilization,polyspermy,and embryonic development in vitro.Biol Reprod.2000;63:242-50.
2.Buhi WC,Alvarez IM,Kouba AJ.Secreted proteins of the oviduct.Cells Tissues Organs.2000;166:165-79.
3.Sutton R,Nancarrow CD,Wallace ALC,Rigby NW.Identification of an oestrus associated glycoprotein in oviducal fluid of the sheep.J Reprod Fertil.1984;72:415-22.
4.Robitaille G,St-Jacques S,Potier M,Bleau G.Characterization of an oviductal glycoprotein associated with the ovulated hamster oocyte.Biol Reprod.1988;38:687-94.
5.Verhage HG,Fazleabas AT,Donnelly K.The in vitro synthesis and release of proteins by the human oviduct.Endocrinology.1988;122:1639-45.
6.Kapur RP,Johnson LV.Ultrastructural evidence that specialized regions of the murine oviduct contribute a glycoprotein to the extracellular matrix of mouse oocytes.Anat Rec.1988;221:720-9.
7.Boice ML,Geisert RD,Blair RM,Verhage HG.Identification and characterization of bovine oviductal glycoproteins synthesized at estrus.Biol Reprod.1990;43:457-65.
8.Buhi WC,Alvarez IM,Sudhipong V,Dones-Smith MM.Identification and characterization of de novo-synthesized porcine oviductal secretory protein.Biol Reprod.1990;43:929-38.
9.Abe H,Onodera M,Sugawara S.Immunological detection and characterization of an estrus-associated antigen in the goat oviduct.J Exp Zool.1995;272:134-41.
10.Verhage HG,Fazleabas AT,Mavrogianis PA,O’Day-Bowman MB,Donnelly KM,Arias EB,et al.The baboon oviduct:characteristics of an oestradiol-dependent oviduct-specific glycoprotein.Hum Reprod Update.1997;3:541-52.
11.Verhage HG,Mavrogianis PA,Boomsma RA,Schmidt A,Brenner RM,Slayden OV,et al.Immunologic and molecular characterization of an estrogendependent glycoprotein in the rhesus(Macaca mulatta)oviduct.Biol Reprod.1997;57:525-31.
12.Oliphant G,Reynolds AB,Smith PF,Ross PR,Marta JS.Immunocytochemical localization and determination of hormone induced synthesis of the sulfated oviductal glycoproteins.Biol Reprod.1984;31:165-74.
13.Buhi WC,O’Brien B,Alvarez IM,Erdos G,Dubois D.Immunogold localization of porcine oviductal secretory proteins within the zona pellucida,perivitelline space,and plasma membrane of oviductal and uterine oocytes and early embryos.Biol Reprod.1993;48:1274-83.
14.Boice ML,Mc Carthy TJ,Mavrogianis PA,Fazleabas AT,Verhage HG.Localization of oviductal glycoproteins within the zona pellucida and perivitelline space of ovulated ova and early embryos inbaboons(Papio anubis).Biol Reprod.1990;43:340-6.
15.Gandolfi F,Modina S,Brevini TAL,Galli C,Moor RM,Lauria A.Oviduct ampullary epithelium contributes a glycoprotein to the zona pellucida,perivitelline space and blastomeres membrane of sheep embryos.Eur JBasic Appl Histochem.1991;35:383-92.
16.Kan FWK,Roux E,Bleau G.Immunolocalization of oviductin in endocytic compartments in the blastomeres of developing embryos in the golden hamster.Biol Reprod.1993;48:77-88.
17.O’Day-Bowman MB,Mavrogianis PA,Reuter LM,Johnson DE,Fazleabas AT,Verhage HG.Association of oviduct specific glycoproteins with human and baboon(Papio anubis)ovarian oocytes and enhancement of human sperm binding to human hemizonae following in vitro incubation.Biol Reprod.1996;54:60-9.
18.Pradeep MA,Jagadeesh J,De AK,Kaushik JK,Malakar D,Kumar S,et al.Purification,sequence characterization and effect of goat oviduct-specific glycoprotein on in vitro embryo development.Theriogenology.2011;75:1005-15.
19.Martus NS,Verhage HG,Mavrogianis PA,Thibodeaux JK.Enhancement of bovine oocyte fertilization in vitro with a bovine oviductal specific glycoprotein.J Reprod Fertil.1998;113:323-9.
20.Kumaresan A,Ansari MR,Abhishek G.Effect of buffalo oviductal and follicular fluid proteins on in vitro sperm capacitation.Indian J Anim Sci.2006;76:204-7.
21.Kumaresan A,Johannisson A,Humblot P,Bergqvist AS.Oviductal fluid modulates the dynamics of tyrosine phosphorylation in cryopreserved boar spermatozoa during capacitation.Mol Reprod Dev.2012;79(8):525-40.
22.Kumaresan A,Johannisson A,Bergqvist AS.Sperm function during incubation with oestrus oviductal fluid differs in bulls with different fertility.Reprod Fertil Dev.2016;doi:10.1071/RD15474.[Epub ahead of print].
23.Kumaresan A,González R,Johannisson A,Berqvist A-S.Dynamic quantification of intracellular calcium and protein tyrosine phosphorylation in cryopreserved boar spermatozoa during short-time incubation with oviductal fluid.Theriogenology.2014;82(8):1145-53.
24.Satoh T,Abe H,Sendai Y,Iwata H,Hoshi H.Biochemical characterization of a bovine oviduct-specific sialo-glycoprotein that sustains sperm viability in vitro.Biochim Biophys Acta.1995;1266:117-23.
25.Algarra B,Han L,Soriano-úbeda C,Avilés M,Coy P,Jovine L,et al.The C-terminal region of OVGP1 remodels the zona pellucida and modifies fertility parameters.Sci Rep.2016;6:32556.
26.Srivastava AK,Kumaresan A,Manimaram A,Prasad S.Mastitis in dairy animals an update.India:Satish Serial Publishing;2014.
27.Yang X,Kubota C,Suzuki H,Taneja M,Bols PE,Presicce GA.Control of oocyte maturation in cows-biological factors.Theriogenology.1998;49:471-82.
28.Hasler JF.The current status of oocyte recovery,in vitro embryo production,and embryo transfer in domestic animals,with an emphasis on the bovine.J Anim Sci.1998;76(3):52-74.
29.Anand T,Kumar D,Chauhan MS,Manik RS,Palta P.Cysteamine supplementation of in vitro maturation medium,in vitro culture medium or both media promotes in vitro development of buffalo(Bubalus bubalis)embryos.Reprod Fertil Dev.2008;20:253-7.
30.Janjanam J,Singh S,Choudhary S,Pradeep MA,Kumar S,Kumaresan A,et al.Molecular cloning,sequence characterization and heterologous expression of buffalo(Bubalus bubalis)oviduct-specific glycoprotein in E.coli.Mol Biol Rep.2012;39:10031-43.
31.Sendai Y,Abe H,Kikuchi M,Satoh T,Hoshi H.Purification and molecular cloning of bovine oviduct-specific glycoprotein.Biol Reprod.1994;50:927-34.
32.Garner DL,Johnson LA.Viability assessment of mammalian sperm using SYBR-14 and propidium iodide.Biol Reprod.1995;53(2):276-84.
33.Singh RK,Kumaresan A,Chhillar S,Rajak SK,Tripathi UK,Nayak S,et al.Identification of suitable combinations of in vitro sperm-function test for the prediction of fertility in buffalo bull.Theriogenology.2016;86(9):2263-71.
34.Wang WH,Abeydeera LR,Fraser LR,Niwa K.Functional analysis using chlortetracycline fluorescence and in vitro fertilization of frozen-thawed ejaculated boar spermatozoa incubated in a protein-free chemically defined medium.J Reprod Fertil.1995;104:305-13.
35.Keefer CL,Stice SL,Matihews DL.Bovine inner cell mass cells as donor nuclei in the production of nuclear transfer embryos and calves.Biol Reprod.1994;50:935-9.
36.Brackett BG,Oliphant G.Capacitation of rabbit spermatozoa in vitro.Biol Reprod.1975;12:260-74.
37.Chauhan MS,Singla SK,Palta P,Manik RS,Madan ML.In vitro maturation and fertilization,and subsequent development of buffalo(Bubalus bubalis)embryos:effect of oocyte quality and type of serum.Reprod Fert Dev.1998;10:173-7.
38.Kumar D,Palta P,Manik RS,Singla SK,Chauhan MS.Effect of culture media and serum supplementation on the development of in vitro fertilized buffalo embryos.Indian J Anim Sci.2007;77:697-701.
39.Hribal R,Hachen A,Jewgenow K,Zahmel J,Fernandez-Gonzalez L,Braun BC.The influence of recombinant feline Oviductin on different aspects of domestic cat(Felis catus)IVF and embryo quality.Theriogenology.2014;82:742-9.
40.Kumaresan A,Ansari MR,Garg A.Modulation of post thaw sperm functions with oviductal proteins in buffaloes.Anim Reprod Sci.2005;90:73-84.
41.Kumaresan A,Ansari MR,Abhishek G,Meena K.Effect of oviductal proteins on sperm functions and lipid peroxidation levels during cryopreservation in buffaloes.Anim Reprod Sci.2006;93:246-57.
42.Mc Nutt TL,Olds-Clarke P,Way AL,Suarez SS,Killian GJ.Effect of follicular or oviductal fluids on movement characteristics of bovine sperm during capacitation in vitro.J Androl.1994;15:328-36.
43.Imam S,Ansari MR,Ahmed N,Kumaresan A.Effect of oviductal fluid proteins on buffalo sperm characteristics during cryopreservation.Theriogenology.2008;69(8):925-31.
44.Kumaresan A,Garg A,Suresh V,Ansari MR.Effect of follicular protein on post-thaw characteristics of buffalo spermatozoa.Indian J Anim Reprod.2003;24:103-5.
45.Prathalingam NS,Watson PF,Revel SG,Busby J,Holt WV.The response of bovine spermatozoa to bicarbonate and its use to assess the influence of added oviductal epithelial proteins on cryopreservation.J Androl.2007;28(3):407-15.
46.Kan FWK,Esperanzate PWB.Surface mapping of binding of Oviductin to the plasma membrane of golden hamster spermatozoa during in-vitro capacitation and acrosome reaction.Mol Reprod Dev.2006;73:756-66.
47.Yang X,Zhao Y,Yang X,Kan FW.Recombinant hamster Oviductin is biologically active and exerts positive effects on sperm functions and sperm-oocyte binding.PLo S One.2015;10(4):e0123003.
48.Zhao Y,Yang X,Jia Z,Reid RL,Leclerc P,Kan FW.Recombinant human oviductin regulates protein tyrosine phosphorylation and acrosome reaction.Reproduction.2016;152(5):561-73.
49.Mc Bride DS,Boisvert C,Bleau G,Kan FW.Detection of nascent and/or mature forms of Oviductin in the female reproductive tract and postovulatory oocytes by use of a polyclonal antibody against recombinant hamster Oviductin.J Histochem Cytochem.2004;52:1001-9.
50.Mc Bride DS,Brockhausen I,Kan FW.Detection of glycosyltransferases in the golden hamster(Mesocricetusauratus)oviduct and evidence for the regulation of O-glycan biosynthesis during the estrous cycle.Biochim Biophys Acta.2005;1721:107-15.
51.Coy P,Canovas S,Mondejar I,Saavedra MD,Romar R,Grullon L,et al.Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy.Proc Natl Acad Sci U S A.2008;105(41):15809-14.
52.Ballester L,Romero-Aguirregomezcorta J,Soriano-úbeda C,Matás C,Romar R,Coy P.Timing of oviductal fluid collection,steroid concentrations,and sperm preservation method affect porcine in vitro fertilization efficiency.Fertil Steril.2014;102:1762-8.
53.Kouba AJ,Abeydeera LR,Alvarez IM,Day BN,Buhi WC.Effects of the porcine oviduct-specific glycoprotein on fertilization,polyspermy,and embryonic development in vitro.Biol Reprod.2000;63:242-50.