Skip to main content Accessibility help
×
Home
Hostname: page-component-59b7f5684b-vh8gq Total loading time: 0.581 Render date: 2022-09-24T17:43:54.570Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "displayNetworkTab": true, "displayNetworkMapGraph": false, "useSa": true } hasContentIssue true

Article contents

Proteins from male and female reproductive tracts involved in sperm function regulation

Published online by Cambridge University Press:  09 January 2019

Gabriela Hernández-Silva
Affiliation:
Departamento de Biología de la Reproducción, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City 14080, México Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Av. Ciudad Universitaria 3000, Coyoacán 04360, México City, México
Mayel Chirinos*
Affiliation:
Departamento de Biología de la Reproducción, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, México City 14080, México
*
Address for correspondence: Mayel Chirinos. Departamento de Biología de la Reproducción, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Vasco de Quiroga 15, Col. Belisario Domínguez Sección XVI, Tlalpan 14080, México City, México. Tel: +52 55 54870900, ext. 2417. E-mail: mayel.chirinose@incmnsz.mx

Summary

Spermatogenesis is a dynamic process that culminates in the production of mature spermatozoa in the seminiferous tubules of sexually mature animals. Although sperm leaving the testis are fully differentiated, they must further undergo two additional maturation steps before acquiring the capability to fertilize the egg. Such processes take place during the epididymal residency and transport in the seminal fluid during ejaculation and, after delivery into the female reproductive tract, during the journey aiming the encountering the egg in the oviduct. Throughout this trip, spermatozoa are exposed to different reproductive fluids whose molecular compositions regulate the progress towards obtaining a fertilized competent cell. This review summarizes the evidence obtained so far supporting the participation of male and female reproductive tract-derived proteins in the modulation of sperm fertilizing ability and discusses the mechanisms by which such regulation may be accomplished.

Type
Review Article
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abe, H, Sendai, Y, Satoh, T and Hoshi, H (1995) Bovine oviduct-specific glycoprotein: a potent factor for maintenance of viability and motility of bovine spermatozoa in vitro . Mol Reprod Dev 42, 226232.CrossRefGoogle ScholarPubMed
Abou-haila, A and Tulsiani, DR (2009) Signal transduction pathways that regulate sperm capacitation and the acrosome reaction. Arch Biochem Biophys 485, 7281.CrossRefGoogle ScholarPubMed
Adeoya-Osiguwa, SA and Fraser, LR (1996) Evidence for Ca2+-dependent ATPase activity, stimulated by decapacitation factor and calmodulin, in mouse sperm. Mol Reprod Dev 44, 111120.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Aitken, RJ, Nixon, B, Lin, M, Koppers, AJ, Lee, YH and Baker, MA (2007) Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J Androl 9, 554564.CrossRefGoogle ScholarPubMed
Akintayo, A, Legare, C and Sullivan, R (2015) Dicarbonyl l-xylulose reductase (DCXR), a “moonlighting protein” in the bovine epididymis. PLoS One 10, e0120869.CrossRefGoogle ScholarPubMed
Al-Dossary, AA, Strehler, EE and Martin-Deleon, PA (2013) Expression and secretion of plasma membrane Ca2+-ATPase 4a (PMCA4a) during murine estrus: association with oviductal exosomes and uptake in sperm. PLoS One 8, e80181.CrossRefGoogle ScholarPubMed
Al-Dossary, AA, Bathala, P, Caplan, JL and Martin-DeLeon, PA (2015) Oviductosome-sperm membrane interaction in cargo delivery: detection of fusion and underlying molecular players using three-dimensional super-resolution structured illumination microscopy (SR-SIM). J Biol Chem 290, 1771017723.CrossRefGoogle Scholar
Austin, CR (1952) The capacitation of the mammalian sperm. Nature 170, 326.CrossRefGoogle ScholarPubMed
Banerjee, M and Chowdhury, M (1994) Purification and characterization of a sperm-binding glycoprotein from human endometrium. Hum Reprod 9, 14971504.CrossRefGoogle ScholarPubMed
Banerjee, M and Chowdhury, M (1995) Induction of capacitation in human spermatozoa in vitro by an endometrial sialic acid-binding protein. Hum Reprod 10, 31473153.CrossRefGoogle ScholarPubMed
Banerjee, M and Chowdhury, M (1997) Localization of a 25 kDa human sperm surface protein: its role in in-vitro human sperm capacitation. Mol Hum Reprod 3, 109114.CrossRefGoogle ScholarPubMed
Bechoua, S, Rieu, I, Sion, B and Grizard, G (2011) Prostasomes as potential modulators of tyrosine phosphorylation in human spermatozoa. Syst Biol Reprod Med 57, 139148.CrossRefGoogle ScholarPubMed
Belleannee, C (2015) Extracellular microRNAs from the epididymis as potential mediators of cell-to-cell communication. Asian J Androl 17, 730736.Google ScholarPubMed
Blackmore, PF (1993) Rapid non-genomic actions of progesterone stimulate Ca2+ influx and the acrosome reaction in human sperm. Cell Signal 5, 531538.CrossRefGoogle ScholarPubMed
Boettger-Tong, H, Aarons, D, Biegler, B, Lee, T and Poirier, GR (1992) Competition between zonae pellucidae and a proteinase inhibitor for sperm binding. Biol Reprod 47, 716722.CrossRefGoogle Scholar
Boilard, M, Reyes-Moreno, C, Lachance, C, Massicotte, L, Bailey, JL, Sirard, MA and Leclerc, P (2004) Localization of the chaperone proteins GRP78 and HSP60 on the luminal surface of bovine oviduct epithelial cells and their association with spermatozoa. Biol Reprod 71, 18791889.CrossRefGoogle ScholarPubMed
Bolton, AE, Pockley, AG, Clough, KJ, Mowles, EA, Stoker, RJ, Westwood, OM and Chapman, MG (1987) Identification of placental protein 14 as an immunosuppressive factor in human reproduction. Lancet 1, 593595.CrossRefGoogle ScholarPubMed
Briton-Jones, C, Lok, IH, Yuen, PM, Chiu, TT, Cheung, LP and Haines, C (2001) Regulation of human oviductin mRNA expression in vivo . Fertil Steril 75, 942946.CrossRefGoogle ScholarPubMed
Caballero, I, Vazquez, JM, Mayor, GM, Alminana, C, Calvete, JJ, Sanz, L, Roca, J and Martinez, EA (2009) PSP-I/PSP-II spermadhesin exert a decapacitation effect on highly extended boar spermatozoa. Int J Androl 32, 505513.CrossRefGoogle ScholarPubMed
Calvete, JJ, Carrera, E, Sanz, L and Topfer-Petersen, E (1996) Boar spermadhesins AQN-1 and AQN-3: oligosaccharide and zona pellucida binding characteristics. Biol Chem 377, 521527.Google ScholarPubMed
Calvo, L, Vantman, D, Banks, SM, Tezon, J, Koukoulis, GN, Dennison, L and Sherins, RJ (1989) Follicular fluid-induced acrosome reaction distinguishes a subgroup of men with unexplained infertility not identified by semen analysis. Fertil Steril 52, 10481054.CrossRefGoogle Scholar
Capkova, J, Elzeinova, F and Novak, P (2007) Increased expression of secretory actin-binding protein on human spermatozoa is associated with poor semen quality. Hum Reprod 22, 13961404.CrossRefGoogle ScholarPubMed
Carlsson, L, Ronquist, G, Eliasson, R, Egberg, N and Larsson, A (2011) Association of cystatin C with prostasomes in human seminal plasma. Int J Androl 34, 363368.CrossRefGoogle ScholarPubMed
Cohen, DJ, Ellerman, DA and Cuasnicu, PS (2000a) Mammalian sperm–egg fusion: evidence that epididymal protein DE plays a role in mouse gamete fusion. Biol Reprod 63, 462468.CrossRefGoogle Scholar
Cohen, DJ, Rochwerger, L, Ellerman, DA, Morgenfeld, MM, Busso, D and Cuasnicu, PS (2000b) Relationship between the association of rat epididymal protein “DE” with spermatozoa and the behavior and function of the protein. Mol Reprod Dev 56, 180188.3.0.CO;2-4>CrossRefGoogle Scholar
Cohen, DJ, Maldera, JA, Vasen, G, Ernesto, JI, Munoz, MW, Battistone, MA and Cuasnicu, PS (2011) Epididymal protein CRISP1 plays different roles during the fertilization process. J Androl 32, 672678.CrossRefGoogle ScholarPubMed
Cornwall, GA (2009) New insights into epididymal biology and function. Hum Reprod Update 15, 213227.CrossRefGoogle ScholarPubMed
Costello, S, Michelangeli, F, Nash, K, Lefievre, L, Morris, J, Machado-Oliveira, G, Barratt, C, Kirkman-Brown, J and Publicover, S (2009) Ca2+-stores in sperm: their identities and functions. Reproduction 138, 425437.CrossRefGoogle ScholarPubMed
Chang, MC (1951) Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168, 697698.CrossRefGoogle ScholarPubMed
Chen, LY, Lin, YH, Lai, ML and Chen, YH (1998) Developmental profile of a caltrin-like protease inhibitor, P12, in mouse seminal vesicle and characterization of its binding sites on sperm surface. Biol Reprod 59, 14981505.CrossRefGoogle ScholarPubMed
Cherr, GN, Yudin, AI, Li, MW, Vines, CA and Overstreet, JW (1999) Hyaluronic acid and the cumulus extracellular matrix induce increases in intracellular calcium in macaque sperm via the plasma membrane protein PH-20. Zygote 7, 211222.CrossRefGoogle ScholarPubMed
Chirinos, M, Durand, M, Gonzalez-Gonzalez, ME, Hernandez-Silva, G, Maldonado-Rosas, I, Lopez, P and Larrea, F (2017) Uterine flushings from women treated with levonorgestrel affect sperm functionality in vitro . Reproduction 154, 607614.CrossRefGoogle ScholarPubMed
Chiu, PC, Koistinen, R, Koistinen, H, Seppala, M, Lee, KF and Yeung, WS (2003) Binding of zona binding inhibitory factor-1 (ZIF-1) from human follicular fluid on spermatozoa. J Biol Chem 278, 1357013577.CrossRefGoogle ScholarPubMed
Chiu, PC, Chung, MK, Tsang, HY, Koistinen, R, Koistinen, H, Seppala, M, Lee, KF and Yeung, WS (2005) Glycodelin-S in human seminal plasma reduces cholesterol efflux and inhibits capacitation of spermatozoa. J Biol Chem 280, 2558025589.CrossRefGoogle ScholarPubMed
Chiu, PC, Chung, MK, Koistinen, R, Koistinen, H, Seppala, M, Ho, PC, Ng, EH, Lee, KF and Yeung, WS (2007) Cumulus oophorus-associated glycodelin-C displaces sperm-bound glycodelin-A and -F and stimulates spermatozoa-zona pellucida binding. J Biol Chem 282, 53785388.CrossRefGoogle Scholar
Da Ros, VG, Munoz, MW, Battistone, MA, Brukman, NG, Carvajal, G, Curci, L, Gomez-ElIas, MD, Cohen, DB and Cuasnicu, PS (2015) From the epididymis to the egg: participation of CRISP proteins in mammalian fertilization. Asian J Androl 17, 711715.Google ScholarPubMed
Dacheux, JL, Belghazi, M, Lanson, Y and Dacheux, F (2006) Human epididymal secretome and proteome. Mol Cell Endocrinol 250, 3642.CrossRefGoogle ScholarPubMed
Dacheux, JL, Belleannee, C, Jones, R, Labas, V, Belghazi, M, Guyonnet, B, Druart, X, Gatti, JL and Dacheux, F (2009) Mammalian epididymal proteome. Mol Cell Endocrinol 306, 4550.CrossRefGoogle ScholarPubMed
DasGupta, S, Mills, CL and Fraser, LR (1994) A possible role for Ca2+-ATPase in human sperm capacitation. J Reprod Fertil 102, 107116.CrossRefGoogle ScholarPubMed
Davis, BK (1979) Studies on the mechanism of capacitation. II. Evidence for lipid transfer between plasma membrane of rat sperm and serum albumin during capacitation in vitro . Biochim Biophys Acta 558, 257266.CrossRefGoogle ScholarPubMed
De Jonge, C (2005) Biological basis for human capacitation. Hum Reprod Update 11, 205214.CrossRefGoogle ScholarPubMed
de Lamirande, E and Gagnon, C (1995) Capacitation-associated production of superoxide anion by human spermatozoa. Free Rad Biol Med 18, 487495.CrossRefGoogle ScholarPubMed
de Lamirande, E, Yoshida, K, Yoshiike, TM, Iwamoto, T and Gagnon, C (2001) Semenogelin, the main protein of semen coagulum, inhibits human sperm capacitation by interfering with the superoxide anion generated during this process. J Androl 22, 672679.Google ScholarPubMed
Demott, RP and Suarez, SS (1992) Hyperactivated sperm progress in the mouse oviduct. Biol Reprod 46, 779785.CrossRefGoogle ScholarPubMed
Desnoyers, L and Manjunath, P (1992) Major proteins of bovine seminal plasma exhibit novel interactions with phospholipid. J Biol Chem 267, 1014910155.Google ScholarPubMed
Dostalova, Z, Calvete, JJ, Sanz, L and Topfer-Petersen, E (1994) Quantitation of boar spermadhesins in accessory sex gland fluids and on the surface of epididymal, ejaculated and capacitated spermatozoa. Biochim Biophys Acta 1200, 4854.CrossRefGoogle ScholarPubMed
Durand, M, Koistinen, R, Chirinos, M, Rodriguez, JL, Zambrano, E, Seppala, M and Larrea, F (2010) Hormonal evaluation and midcycle detection of intrauterine glycodelin in women treated with levonorgestrel as in emergency contraception. Contraception 82, 526533.CrossRefGoogle ScholarPubMed
Ellington, JE, Evenson, DP, Wright, RW Jr, Jones, AE, Schneider, CS, Hiss, GA and Brisbois, RS (1999) Higher-quality human sperm in a sample selectively attach to oviduct (fallopian tube) epithelial cells in vitro . Fertil Steril 71, 924929.CrossRefGoogle Scholar
Ensslin, MA, Lyng, R, Raymond, A, Copland, S and Shur, BD (2007) Novel gamete receptors that facilitate sperm adhesion to the egg coat. Soc Reprod Fertil Suppl 63, 367383.Google ScholarPubMed
Ernesto, JI, Weigel Munoz, M, Battistone, MA, Vasen, G, Martinez-Lopez, P, Orta, G, Figueiras-Fierro, D, De la Vega-Beltran, JL, Moreno, IA, Guidobaldi, HA, Giojalas, L, Darszon, A, Cohen, DJ and Cuasnicu, PS (2015) CRISP1 as a novel CatSper regulator that modulates sperm motility and orientation during fertilization. J Cell Biol 210, 12131214.CrossRefGoogle ScholarPubMed
Fan, J, Lefebvre, J and Manjunath, P (2006) Bovine seminal plasma proteins and their relatives: A new expanding superfamily in mammals. Gene 375, 6374.CrossRefGoogle ScholarPubMed
Feki, NC, Therond, P, Couturier, M, Limea, G, Legrand, A, Jouannet, P and Auger, J (2004) Human sperm lipid content is modified after migration into human cervical mucus. Mol Hum Reprod 10, 137142.CrossRefGoogle ScholarPubMed
Franchi, A, Cubilla, M, Guidobaldi, HA, Bravo, AA and Giojalas, LC (2016) Uterosome-like vesicles prompt human sperm fertilizing capability. Mol Hum Reprod 22, 833841.Google ScholarPubMed
Fraser, LR (1984) Mouse sperm capacitation in vitro involves loss of a surface-associated inhibitory component. J Reprod Fertil 72, 373384.CrossRefGoogle ScholarPubMed
Fraser, LR (1998) Interactions between a decapacitation factor and mouse spermatozoa appear to involve fucose residues and a GPI-anchored receptor. Mol Reprod Dev 51, 193202.3.0.CO;2-L>CrossRefGoogle Scholar
Fraser, LR, Harrison, RA and Herod, JE (1990) Characterization of a decapacitation factor associated with epididymal mouse spermatozoa. J Reprod Fertil 89, 135148.CrossRefGoogle ScholarPubMed
Fusi, FM, Vignali, M, Gailit, J and Bronson, RA (1993) Mammalian oocytes exhibit specific recognition of the RGD (Arg–Gly–Asp) tripeptide and express oolemmal integrins. Mol Reprod Dev 36, 212219.CrossRefGoogle ScholarPubMed
Fusi, FM, Tamburini, C, Mangili, F, Montesano, M, Ferrari, A and Bronson, RA (1996) The expression of αv, α5, β1, and β3 integrin chains on ejaculated human spermatozoa varies with their functional state. Mol Hum Reprod 2, 169175.CrossRefGoogle ScholarPubMed
Garenaux, E, Kanagawa, M, Tsuchiyama, T, Hori, K, Kanazawa, T, Goshima, A, Chiba, M, Yasue, H, Ikeda, A, Yamaguchi, Y, Sato, C and Kitajima, K (2015) Discovery, primary, and crystal structures and capacitation-related properties of a prostate-derived heparin-binding protein WGA16 from boar sperm. J Biol Chem 290, 54845501.CrossRefGoogle ScholarPubMed
Ghersevich, S, Massa, E and Zumoffen, C (2015) Oviductal secretion and gamete interaction. Reproduction 149, R1R14.CrossRefGoogle ScholarPubMed
Gibbons, R, Adeoya-Osiguwa, SA and Fraser, LR (2005) A mouse sperm decapacitation factor receptor is phosphatidylethanolamine-binding protein 1. Reproduction 130, 497508.CrossRefGoogle ScholarPubMed
Gould, JE, Overstreet, JW and Hanson, FW (1984) Assessment of human sperm function after recovery from the female reproductive tract. Biol Reprod 31, 888894.CrossRefGoogle ScholarPubMed
Griffiths, GS, Galileo, DS, Reese, K and Martin-Deleon, PA (2008a) Investigating the role of murine epididymosomes and uterosomes in GPI-linked protein transfer to sperm using SPAM1 as a model. Mol Reprod Dev 75, 16271636.CrossRefGoogle Scholar
Griffiths, GS, Miller, KA, Galileo, DS and Martin-DeLeon, PA (2008b) Murine SPAM1 is secreted by the estrous uterus and oviduct in a form that can bind to sperm during capacitation: acquisition enhances hyaluronic acid-binding ability and cumulus dispersal efficiency. Reproduction 135, 293301.CrossRefGoogle Scholar
Gwathmey, TM, Ignotz, GG and Suarez, SS (2003) PDC-109 (BSP-A1/A2) promotes bull sperm binding to oviductal epithelium in vitro and may be involved in forming the oviductal sperm reservoir. Biol Reprod 69, 809815.CrossRefGoogle ScholarPubMed
Hernández-Silva, G, Durand, M, Larrea, F and Chirinos, M (2018) Proteomic changes in uterine flushings after levonorgestrel treatment and effects on sperm function. Reproduction 156, 477486.CrossRefGoogle Scholar
Hu, J, Merriner, DJ, O’Connor, AE, Houston, BJ, Furic, L, Hedger, MP and O’Bryan, MK (2018) Epididymal cysteine-rich secretory proteins are required for epididymal sperm maturation and optimal sperm function. Mol Hum Reprod 24, 111122.CrossRefGoogle ScholarPubMed
Hu, ZH, Liu, Q, Shang, Q, Zheng, M, Yang, J and Zhang, YL (2002) Identification and characterization of a new member of serpin family – HongrES1 in rat epididymis. Cell Res 12, 407410.CrossRefGoogle ScholarPubMed
Huang, VW, Zhao, W, Lee, CL, Lee, CY, Lam, KK, Ko, JK, Yeung, WS, Ho, PC and Chiu, PC (2013) Cell membrane proteins from oviductal epithelial cell line protect human spermatozoa from oxidative damage. Fertil Steril 99, 14441452 e1443.CrossRefGoogle ScholarPubMed
Huang, YH, Chu, ST and Chen, YH (1999) Seminal vesicle autoantigen, a novel phospholipid-binding protein secreted from luminal epithelium of mouse seminal vesicle, exhibits the ability to suppress mouse sperm motility. Biochem J 343 Pt 1, 241248.CrossRefGoogle ScholarPubMed
Huang, YH, Chu, ST and Chen, YH (2000) A seminal vesicle autoantigen of mouse is able to suppress sperm capacitation-related events stimulated by serum albumin. Biol Reprod 63, 15621566.CrossRefGoogle ScholarPubMed
Hung, PH and Suarez, SS (2012) Alterations to the bull sperm surface proteins that bind sperm to oviductal epithelium. Biol Reprod 87, 88.Google ScholarPubMed
Jeulin, C, Soumah, A and Jouannet, P (1985) Morphological factors influencing the penetration of human sperm into cervical mucus in vitro . Int J Androl 8, 215223.CrossRefGoogle ScholarPubMed
Julkunen, M, Wahlstrom, T, Seppala, M, Koistinen, R, Koskimies, A, Stenman, UH and Bohn, H (1984) Detection and localization of placental protein 14-like protein in human seminal plasma and in the male genital tract. Archives Androl 12 Suppl, 5967.Google ScholarPubMed
Juyena, NS and Stelletta, C (2012) Seminal plasma: an essential attribute to spermatozoa. J Androl 33, 536551.CrossRefGoogle ScholarPubMed
Kawano, N and Yoshida, M (2007) Semen-coagulating protein, SVS2, in mouse seminal plasma controls sperm fertility. Biol Reprod 76, 353361.CrossRefGoogle ScholarPubMed
Kawano, N, Yoshida, K, Iwamoto, T and Yoshida, M (2008) Ganglioside GM1 mediates decapacitation effects of SVS2 on murine spermatozoa. Biol Reprod 79, 11531159.CrossRefGoogle ScholarPubMed
Kervancioglu, ME, Djahanbakhch, O and Aitken, RJ (1994) Epithelial cell coculture and the induction of sperm capacitation. Fertil Steril 61, 11031108.CrossRefGoogle ScholarPubMed
Kimura, H, Matsuda, J, Ogura, A, Asano, T and Naiki, M (1994) Affinity binding of hamster oviductin to spermatozoa and its influence on in vitro fertilization. Mol Reprod Dev 39, 322327.CrossRefGoogle ScholarPubMed
King, RS and Killian, GJ (1994) Purification of bovine estrus-associated protein and localization of binding on sperm. Biol Reprod 51, 3442.CrossRefGoogle ScholarPubMed
Kirkman-Brown, JC, Bray, C, Stewart, PM, Barratt, CL and Publicover, SJ (2000) Biphasic elevation of [Ca2+]i in individual human spermatozoa exposed to progesterone. Dev Biol 222, 326335.CrossRefGoogle Scholar
Koppers, AJ, Reddy, T and O’Bryan, MK (2011) The role of cysteine-rich secretory proteins in male fertility. Asian J Androl 13, 111117.CrossRefGoogle ScholarPubMed
Kouba, AJ, Abeydeera, LR, Alvarez, IM, Day, BN and Buhi, WC (2000) Effects of the porcine oviduct-specific glycoprotein on fertilization, polyspermy, and embryonic development in vitro . Biol Reprod 63, 242250.CrossRefGoogle ScholarPubMed
Lachance, C, Bailey, JL and Leclerc, P (2007) Expression of Hsp60 and Grp78 in the human endometrium and oviduct, and their effect on sperm functions. Hum Reprod 22, 26062614.CrossRefGoogle ScholarPubMed
Laflamme, J, Akoum, A and Leclerc, P (2005) Induction of human sperm capacitation and protein tyrosine phosphorylation by endometrial cells and interleukin-6. Mol Hum Reprod 11, 141150.CrossRefGoogle ScholarPubMed
Lee, RK, Tseng, HC, Hwu, YM, Fan, CC, Lin, MH, Yu, JJ, Yeh, LY and Li, SH (2018) Expression of cystatin C in the female reproductive tract and its effect on human sperm capacitation. Reprod Biol Endocrinol 16, 8.CrossRefGoogle ScholarPubMed
Lin, MH, Lee, RK, Hwu, YM, Lu, CH, Chu, SL, Chen, YJ, Chang, WC and Li, SH (2008) SPINKL, a Kazal-type serine protease inhibitor-like protein purified from mouse seminal vesicle fluid, is able to inhibit sperm capacitation. Reproduction 136, 559571.CrossRefGoogle ScholarPubMed
Lin, Y, Mahan, K, Lathrop, WF, Myles, DG and Primakoff, P (1994) A hyaluronidase activity of the sperm plasma membrane protein PH-20 enables sperm to penetrate the cumulus cell layer surrounding the egg. J Cell Biol 125, 11571163.CrossRefGoogle Scholar
Lok, IH, Briton-Jones, CM, Yuen, PM and Haines, CJ (2002) Variable expression of oviductin mRNA at different stages of human reproductive cycle. J Assist Reprod Genetics 19, 569576.CrossRefGoogle ScholarPubMed
Lundwall, A (1996) The cloning of a rapidly evolving seminal-vesicle-transcribed gene encoding the major clot-forming protein of mouse semen. Eur J Biochem 235, 424430.CrossRefGoogle ScholarPubMed
Lyng, R and Shur, BD (2009) Mouse oviduct-specific glycoprotein is an egg-associated ZP3-independent sperm-adhesion ligand. J Cell Sci 122, 38943906.CrossRefGoogle ScholarPubMed
Makrigiannakis, A, Karamouti, M, Petsas, G, Makris, N, Nikas, G and Antsaklis, A (2009) The expression of receptivity markers in the fallopian tube epithelium. Histochemistry and cell biology, 132, 159167.CrossRefGoogle ScholarPubMed
Maldera, JA, Weigel Muñoz, M, Chirinos, M, Busso, D, Raffo, FGE, Battistone, MA, Blaquier, JA, Larrea, F and Cuasnicu, PS (2014) Human fertilization: epididymal hCRISP1 mediates sperm–zona pellucida binding through its interaction with ZP3. Mol Hum Reprod 20, 341349.CrossRefGoogle ScholarPubMed
Malm, J, Hellman, J, Hogg, P and Lilja, H (2000) Enzymatic action of prostate-specific antigen (PSA or hK3): substrate specificity and regulation by Zn2+, a tight-binding inhibitor. The Prostate 45, 132139.3.0.CO;2-3>CrossRefGoogle Scholar
Manjunath, P and Thérien, I (2002) Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. J Reprod Immunol 53, 109119.CrossRefGoogle ScholarPubMed
Manjunath, P, Chandonnet, L, Leblond, E and Desnoyers, L (1994) Major proteins of bovine seminal vesicles bind to spermatozoa. Biol Reprod 50, 2737.CrossRefGoogle ScholarPubMed
Marin-Briggiler, CI, Gonzalez-Echeverria, MF, Munuce, MJ, Ghersevich, S, Caille, AM, Hellman, U, Corrigall, VM and Vazquez-Levin, MH (2010) Glucose-regulated protein 78 (Grp78/BiP) is secreted by human oviduct epithelial cells and the recombinant protein modulates sperm-zona pellucida binding. Fertil Steril 93, 15741584.CrossRefGoogle ScholarPubMed
Marini, PE and Cabada, MO (2003) One step purification and biochemical characterization of a spermatozoa-binding protein from porcine oviductal epithelial cells. Mol Reprod Dev 66, 383390.CrossRefGoogle ScholarPubMed
Martin-DeLeon, PA (2015) Epididymosomes: transfer of fertility-modulating proteins to the sperm surface. Asian J Androl 17, 720725.Google ScholarPubMed
Martin-DeLeon, PA (2016) Uterosomes: exosomal cargo during the estrus cycle and interaction with sperm. Front Biosci (Schol Ed) 8, 115122.Google Scholar
Martus, NS, Verhage, HG, Mavrogianis, PA and Thibodeaux, JK (1998) Enhancement of bovine oocyte fertilization in vitro with a bovine oviductal specific glycoprotein. J Reprod Fertil 113, 323329.CrossRefGoogle ScholarPubMed
Mitra, A, Richardson, RT and O’Rand, MG (2010) Analysis of recombinant human semenogelin as an inhibitor of human sperm motility. Biol Reprod 82, 489496.CrossRefGoogle ScholarPubMed
Morales, P, Palma, V, Salgado, AM and Villalon, M (1996) Sperm interaction with human oviductal cells in vitro . Hum Reprod 11, 15041509.CrossRefGoogle ScholarPubMed
Murray, SC and Smith, TT (1997) Sperm interaction with fallopian tube apical membrane enhances sperm motility and delays capacitation. Fertil Steril 68, 351357.CrossRefGoogle ScholarPubMed
Naz, RK and Kaplan, P (1994) Interleukin-6 enhances the fertilizing capacity of human sperm by increasing capacitation and acrosome reaction. J Androl 15, 228233.Google ScholarPubMed
Ni, Y, Zhou, Y, Chen, WY, Zheng, M, Yu, J, Li, C, Zhang, Y and Shi, QX (2009) HongrES1, a cauda epididymis-specific protein, is involved in capacitation of guinea pig sperm. Mol Reprod Dev 76, 984993.CrossRefGoogle ScholarPubMed
Nixon, B, MacIntyre, DA, Mitchell, LA, Gibbs, GM, O’Bryan, M and Aitken, RJ (2006) The identification of mouse sperm-surface-associated proteins and characterization of their ability to act as decapacitation factors. Biol Reprod 74, 275287.CrossRefGoogle ScholarPubMed
O’Bryan, MK, Sebire, K, Meinhardt, A, Edgar, K, Keah, HH, Hearn, MT and De Kretser, DM (2001) Tpx-1 is a component of the outer dense fibers and acrosome of rat spermatozoa. Mol Reprod Dev 58, 116125.3.0.CO;2-8>CrossRefGoogle ScholarPubMed
O’Rand, MG and Widgren, EE (2012) Loss of calcium in human spermatozoa via EPPIN, the semenogelin receptor. Biol Reprod 86, 55.Google ScholarPubMed
O’Rand, MG, Widgren, EE, Wang, Z and Richardson, RT (2006) Eppin: an effective target for male contraception. Mol Cell Endocrinol 250, 157162.CrossRefGoogle ScholarPubMed
Oehninger, S, Coddington, CC, Hodgen, GD and Seppala, M (1995) Factors affecting fertilization: endometrial placental protein 14 reduces the capacity of human spermatozoa to bind to the human zona pellucida. Fertil Steril 63, 377383.CrossRefGoogle ScholarPubMed
Osycka-Salut, CE, Castellano, L, Fornes, D, Beltrame, JS, Alonso, CAI, Jawerbaum, A, Franchi, A, Diaz, ES and Perez Martinez, S (2017) Fibronectin from oviductal cells fluctuates during the estrous cycle and contributes to sperm-oviduct interaction in cattle. J Cell Biochem 118, 40954108.CrossRefGoogle ScholarPubMed
Perez, FA, Roma, SM, Cabada, MO and Marini, PE (2006) Sperm binding glycoprotein is differentially present surrounding the lumen of isthmus and ampulla of the pig’s oviduct. Anat Embryol 211, 619624.CrossRefGoogle ScholarPubMed
Perry, RL, Barratt, CL, Warren, MA and Cooke, ID (1996) Comparative study of the effect of human cervical mucus and a cervical mucus substitute, Healonid, on capacitation and the acrosome reaction of human spermatozoa in vitro . Hum Reprod 11, 10551062.CrossRefGoogle Scholar
Plante, G and Manjunath, P (2015a) Epididymal binder of sperm genes and proteins: what do we know a decade later? Andrology 3, 817824.CrossRefGoogle Scholar
Plante, G and Manjunath, P (2015b) Murine binder of sperm protein homolog 1: a new player in HDL-induced capacitation. Reproduction 149, 367376.CrossRefGoogle Scholar
Plante, G, Prud’homme, B, Fan, J, Lafleur, M and Manjunath, P (2016) Evolution and function of mammalian binder of sperm proteins. Cell Tissue Res 363, 105127.CrossRefGoogle ScholarPubMed
Pons-Rejraji, H, Artonne, C, Sion, B, Brugnon, F, Canis, M, Janny, L and Grizard, G (2011) Prostasomes: inhibitors of capacitation and modulators of cellular signalling in human sperm. Int J Androl 34, 568580.CrossRefGoogle ScholarPubMed
Reddy, T, Gibbs, GM, Merriner, DJ, Kerr, JB, O’Bryan, MK (2008) Cysteine-rich secretory proteins are not exclusively expressed in the male reproductive tract. Dev Dynam 237, 33133323.CrossRefGoogle Scholar
Robert, M and Gagnon, C (1996) Purification and characterization of the active precursor of a human sperm motility inhibitor secreted by the seminal vesicles: identity with semenogelin. Biol Reprod 55, 813821.CrossRefGoogle ScholarPubMed
Roberts, KP, Wamstad, JA, Ensrud, KM and Hamilton, DW (2003) Inhibition of capacitation-associated tyrosine phosphorylation signaling in rat sperm by epididymal protein Crisp-1. Biol Reprod 69, 572581.CrossRefGoogle ScholarPubMed
Rochwerger, L, Cohen, DJ and Cuasnicu, PS (1992) Mammalian sperm-egg fusion: the rat egg has complementary sites for a sperm protein that mediates gamete fusion. Dev Biol 153, 8390.CrossRefGoogle ScholarPubMed
Ronquist, G (2015) Prostasomes: their characterisation: implications for human reproduction: prostasomes and human reproduction. Adv Exp Med Biol 868, 191209.CrossRefGoogle ScholarPubMed
Ronquist, KG, Ronquist, G, Carlsson, L and Larsson, A (2009) Human prostasomes contain chromosomal DNA. The Prostate 69, 737743.CrossRefGoogle ScholarPubMed
Sabeur, K, Cherr, GN, Yudin, AI and Overstreet, JW (1998) Hyaluronic acid enhances induction of the acrosome reaction of human sperm through interaction with the PH-20 protein. Zygote 6, 103111.CrossRefGoogle ScholarPubMed
Saucedo, L, Sobarzo, C, Brukman, NG, Guidobaldi, HA, Lustig, L, Giojalas, LC, Buffone, MG, Vazquez-Levin, MH and Marin-Briggiler, C (2018) Involvement of fibroblast growth factor 2 (FGF2) and its receptors in the regulation of mouse sperm physiology. Reproduction 156, 163172.CrossRefGoogle ScholarPubMed
Seppala, M, Koistinen, H, Koistinen, R, Chiu, PC and Yeung, WS (2007) Glycosylation related actions of glycodelin: gamete, cumulus cell, immune cell and clinical associations. Hum Reprod Update 13, 275287.CrossRefGoogle ScholarPubMed
Suarez, SS (2008) Regulation of sperm storage and movement in the mammalian oviduct. Int J Dev Biol 52, 455462.CrossRefGoogle ScholarPubMed
Sundsfjord, JA, Forsdahl, F and Thibault, G (1989) Physiological levels of immunoreactive ANH-like peptides in human follicular fluid. Acta Endocrinol 121, 578580.CrossRefGoogle ScholarPubMed
Sutovsky, P, Flechon, JE and Pavlok, A (1995) F-actin is involved in control of bovine cumulus expansion. Mol Reprod Dev 41, 521529.CrossRefGoogle ScholarPubMed
Tabibzadeh, S and Sun, XZ (1992) Cytokine expression in human endometrium throughout the menstrual cycle. Hum Reprod 7, 12141221.CrossRefGoogle ScholarPubMed
Tanghe, S, Van Soom, A, Duchateau, L, Nauwynck, H and de Kruif, A (2004) Carbohydrates and glycoproteins involved in bovine fertilization in vitro . Mol Reprod Dev 68, 492499.CrossRefGoogle ScholarPubMed
Teijeiro, JM, Cabada, MO and Marini, PE (2008) Sperm binding glycoprotein (SBG) produces calcium and bicarbonate dependent alteration of acrosome morphology and protein tyrosine phosphorylation on boar sperm. J Cell Biochem 103, 14131423.CrossRefGoogle ScholarPubMed
Teng, CT, Gladwell, W, Beard, C, Walmer, D, Teng, CS and Brenner, R (2002) Lactoferrin gene expression is estrogen responsive in human and rhesus monkey endometrium. Mol Hum Reprod 8, 5867.CrossRefGoogle ScholarPubMed
Therien, I, Moreau, R and Manjunath, P (1999) Bovine seminal plasma phospholipid-binding proteins stimulate phospholipid efflux from epididymal sperm. Biol Reprod 61, 590598.CrossRefGoogle ScholarPubMed
Thimon, V, Frenette, G, Saez, F, Thabet, M and Sullivan, R (2008) Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach. Hum Reprod 23, 16981707.CrossRefGoogle ScholarPubMed
Thys, M, Nauwynck, H, Maes, D, Hoogewijs, M, Vercauteren, D, Rijsselaere, T, Favoreel, H and Van Soom, A (2009) Expression and putative function of fibronectin and its receptor (integrin α5β1) in male and female gametes during bovine fertilization in vitro . Reproduction 138, 471482.CrossRefGoogle ScholarPubMed
Tomar, AK, Sooch, BS, Raj, I, Singh, S and Yadav, S (2013) Interaction analysis identifies semenogelin I fragments as new binding partners of PIP in human seminal plasma. Int J Biol Macromol 52, 296299.CrossRefGoogle ScholarPubMed
Utleg, AG, Yi, EC, Xie, T, Shannon, P, White, JT, Goodlett, DR, Hood, L and Lin, B (2003) Proteomic analysis of human prostasomes. The Prostate 56, 150161.CrossRefGoogle ScholarPubMed
Visconti, PE, Bailey, JL, Moore, GD, Pan, D, Olds-Clarke, P and Kopf, GS (1995a) Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121, 11291137.Google Scholar
Visconti, PE, Moore, GD, Bailey, JL, Leclerc, P, Connors, SA, Pan, D, Olds-Clarke, P and Kopf, GS (1995b) Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121, 11391150.Google Scholar
Wang, Z, Widgren, EE, Sivashanmugam, P, O’Rand, MG and Richardson, RT (2005) Association of eppin with semenogelin on human spermatozoa. Biol Reprod 72, 10641070.CrossRefGoogle ScholarPubMed
Wang, Z, Widgren, EE, Richardson, RT and O’Rand, MG (2007) Characterization of an eppin protein complex from human semen and spermatozoa. Biol Reprod 77, 476484.CrossRefGoogle ScholarPubMed
Wergin, WP (1985) Interactions between spermatozoa and the crypts, cilia, and mucus of the cervix in the ewe. Scan Electron Microsc 11911199.Google ScholarPubMed
Yeung, WS, Lee, KF, Koistinen, R, Koistinen, H, Seppala, M and Chiu, PC (2009) Effects of glycodelins on functional competence of spermatozoa. J Reprod Immunol 83, 2630.CrossRefGoogle ScholarPubMed
Yoshida, M, Kaneko, M, Kurachi, H and Osawa, M (2001) Identification of two rodent genes encoding homologues to seminal vesicle autoantigen: a gene family including the gene for prolactin-inducible protein. Biochem Biophys Res Commun 281, 94100.CrossRefGoogle ScholarPubMed
Zhang, M, Hong, H, Zhou, B, Jin, S, Wang, C, Fu, M, Wang, S and Xia, G (2006) The expression of atrial natriuretic peptide in the oviduct and its functions in pig spermatozoa. J Endocrinol 189, 493507.CrossRefGoogle ScholarPubMed
Zhao, Y, Yang, X, Jia, Z, Reid, RL, Leclerc, P and Kan, FW (2016) Recombinant human oviductin regulates protein tyrosine phosphorylation and acrosome reaction. Reproduction 152, 561573.CrossRefGoogle ScholarPubMed
Zhou, Y, Zheng, M, Shi, Q, Zhang, L, Zhen, W, Chen, W, Zhang, Y (2008) An epididymis-specific secretory protein HongrES 1 critically regulates sperm capacitation and male fertility. PLoS One 3, 112.CrossRefGoogle Scholar
Zijlstra, C and Stoorvogel, W (2016) Prostasomes as a source of diagnostic biomarkers for prostate cancer. J Clin Invest 126, 11441151.CrossRefGoogle ScholarPubMed
Zumoffen, CM, Caille, AM, Munuce, MJ, Cabada, MO and Ghersevich, SA (2010) Proteins from human oviductal tissue-conditioned medium modulate sperm capacitation. Hum Reprod 25, 15041512.CrossRefGoogle ScholarPubMed
Zumoffen, CM, Gil, R, Caille, AM, Morente, C, Munuce, MJ and Ghersevich, SA (2013) A protein isolated from human oviductal tissue in vitro secretion, identified as human lactoferrin, interacts with spermatozoa and oocytes and modulates gamete interaction. Hum Reprod 28, 12971308.CrossRefGoogle ScholarPubMed
Zumoffen, CM, Massa, E, Caille, AM, Munuce, MJ and Ghersevich, SA (2015) Effects of lactoferrin, a protein present in the female reproductive tract, on parameters of human sperm capacitation and gamete interaction. Andrology 3, 10681075.CrossRefGoogle ScholarPubMed
15
Cited by