How, where and when is SPINK3 bound and removed from mouse sperm?

in Reproduction
Authors:
Anabella R NicolliInstituto de Investigaciones Biológicas (IIB-FCEyN/CONICET), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Mar del Plata, Argentina

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Carlos A I AlonsoDepartment of Pharmacology and Therapeutics, McGill University, Montréal, Canada

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Catalina OtamendiInstituto de Investigaciones Biológicas (IIB-FCEyN/CONICET), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Mar del Plata, Argentina

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Micaela CerlettiInstituto de Investigaciones Biológicas (IIB-FCEyN/CONICET), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Mar del Plata, Argentina

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Ansgar PoetschPlant Biochemistry, Ruhr University Bochum, Bochum, Germany
Queen Mary School, Medical College, Nanchang University, Nanchang, China
College of Marine Life Sciences, Ocean University of China, Qingdao, China

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Vikram SharmaSchool of Biomedical Science, University of Plymouth, Plymouth, UK

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Lucia ZalazarInstituto de Investigaciones Biológicas (IIB-FCEyN/CONICET), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Mar del Plata, Argentina

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Silvina Perez-MartinezCentro de Estudios Farmacológicos y Botánicos (CEFYBO-UBA/CONICET), Facultad de Medicina, Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas Técnicas, Buenos Aires, Argentina

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Andreina CesariInstituto de Investigaciones Biológicas (IIB-FCEyN/CONICET), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Mar del Plata, Argentina

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Correspondence should be addressed to A R Nicolli; Email: anabellanicolli@gmail.com
DOI:
https://doi.org/10.1530/REP-21-0195
Volume/Issue:
Volume 163: Issue 5
Page Range:
251–266
Article Type:
Research Article
Online Publication Date:
14 Mar 2022
Copyright:
© Society for Reproduction and Fertility 2022
Restricted access

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Sperm capacitation in mammals is a fundamental requirement to acquire their fertilizing capacity. Little is known about the action mechanism of the molecules that prevent capacitation from occurring prematurely. These molecules are known as decapacitation factors (DFs) and they must be removed from the sperm surface for capacitation to occur successfully. Serine protease inhibitor Kazal type 3 (SPINK3) has been proposed as one of these DFs. Here, we evaluate how this protein binds to mouse sperm and its removal kinetics. We describe that SPINK3 is capable of binding to the membrane of mature epididymal sperm through protein–lipid interactions, specifically to lipid rafts subcellular fraction. Moreover, cholera toxin subunit b (CTB) avoids SPINK3 binding. We observe that SPINK3 is removed from the sperm under in vitro capacitating conditions and by the uterine fluid from estrus females. Our ex vivo studies show the removal kinetics of this protein within the female tract, losing SPINK3 formerly from the apical region of the sperm in the uterus and later from the flagellar region within the oviduct. The presence of acrosome-reacted sperm in the female duct concurs with the absence of SPINK3 over its surface.

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Print ISSN:
1470-1626
Online ISSN:
1741-7899

  • Aarons D, Robinson R, Richardson R & Poirier GR 1985 Competition between seminal and exogenous proteinase inhibitors for sites on murine epididymal sperm. Contraception 31 177–184. (https://doi.org/10.1016/0010-7824(8590032-0)

    • Search Google Scholar
    • Export Citation

  • Asano A, Selvaraj V, Buttke DE, Nelson JL, Green KM, Evans JE & Travis AJ 2009 Biochemical characterization of membrane fractions in murine sperm: identification of three distinct sub-types of membrane rafts. Journal of Cellular Physiology 218 537–548. (https://doi.org/10.1002/jcp.21623)

    • Search Google Scholar
    • Export Citation

  • Asano A, Nelson JL, Zhang S & Travis AJ 2010 Characterization of the proteomes associating with three distinct membrane raft sub-types in murine sperm. Proteomics 10 3494–3505. (https://doi.org/10.1002/pmic.201000002)

    • Search Google Scholar
    • Export Citation

  • Assis DM, Zalazar L, Aparecida Juliano MA, De Castro R & Cesari A 2013 Novel inhibitory activity for serine protease inhibitor Kazal type-3 (Spink3) on human recombinant kallikreins. Protein and Peptide Letters 20 1098–1107. (https://doi.org/10.2174/0929866511320100003)

    • Search Google Scholar
    • Export Citation

  • Austin CR 1952 The ‘capacitation’ of the mammalian sperm. Nature 170 326–326. (https://doi.org/10.1038/170326a0)

  • Bedford JM & Chang MC 1962 Removal of decapacitation factor from seminal plasma by high-speed centrifugation. American Journal of Physiology 202 179–181. (https://doi.org/10.1152/ajplegacy.1962.202.1.179)

    • Search Google Scholar
    • Export Citation

  • Bligh EG & Dyer WJ 1959 A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37 911–917. (https://doi.org/10.1139/o59-099)

    • Search Google Scholar
    • Export Citation

  • Boettger-Tong HL, Aarons DJ, Biegler BE, George B & Poirier GR 1993 Binding of a murine proteinase inhibitor to the acrosome region of the human sperm head. Molecular Reproduction and Development 36 346–353. (https://doi.org/10.1002/mrd.1080360310)

    • Search Google Scholar
    • Export Citation

  • Brewis IA & Gadella BM 2009 Sperm surface proteomics: from protein lists to biological function. MHR: Basic Science of Reproductive Medicine 16 68–79. (https://doi.org/10.1093/molehr/gap077)

    • Search Google Scholar
    • Export Citation

  • Byers SL, Wiles MV, Dunn SL & Taft RA 2012 Mouse estrous cycle identification tool and images. PLoS ONE 7 e35538. (https://doi.org/10.1371/journal.pone.0035538)

    • Search Google Scholar
    • Export Citation

  • Cerletti M, Paggi R, Troetschel C, Ferrari MC, Guevara CR, Albaum S, Poetsch A & De Castro R 2018a LonB protease is a novel regulator of carotenogenesis controlling degradation of phytoene synthase in Haloferax volcanii. Journal of Proteome Research 17 1158–1171. (https://doi.org/10.1021/acs.jproteome.7b00809)

    • Search Google Scholar
    • Export Citation

  • Cerletti M, Giménez MI, Tröetschel C, D’Alessandro C, Poetsch A, De Castro RE & Paggi RA 2018b Proteomic study of the exponential–stationary growth phase transition in the haloarchaea Natrialba magadii and Haloferax volcanii. Proteomics 18 e1800116. (https://doi.org/10.1002/pmic.201800116) 29888524.

    • Search Google Scholar
    • Export Citation

  • Cesari A, de los Angeles Monclus Mde L, Tejón GP, Clementi M & Fornes MW 2010 Regulated serine proteinase lytic system on mammalian sperm surface: there must be a role. Theriogenology 74 699 .e1–711.e1. (https://doi.org/10.1016/j.theriogenology.2010.03.029)

    • Search Google Scholar
    • Export Citation

  • Chang MC 1951 Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168 697–698. (https://doi.org/10.1038/168697b0)

    • Search Google Scholar
    • Export Citation

  • Chang MC 1957 A detrimental effect of seminal plasma on the fertilizing capacity of sperm. Nature 179 258–259. (https://doi.org/10.1038/179258a0)

    • Search Google Scholar
    • Export Citation

  • Chen LY, Lin YH, Lai ML & 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. Biology of Reproduction 59 1498–1505. (https://doi.org/10.1095/biolreprod59.6.1498)

    • Search Google Scholar
    • Export Citation

  • Chiu PC, Chung MK, Tsang HY, Koistinen R, Koistinen H, Seppala M, Lee KF & Yeung WS 2005 Glycodelin-S in human seminal plasma reduces cholesterol efflux andInhibits capacitation ofSpermatozoa. Journal of Biological Chemistry 280 25580–25589. (https://doi.org/10.1074/jbc.M504103200)

    • Search Google Scholar
    • Export Citation

  • Chung JJ, Shim SH, Everley RA, Gygi SP, Zhuang X & Clapham DE 2014 Structurally distinct Ca2+ signaling domains of sperm flagella orchestrate tyrosine phosphorylation and motility. Cell 157 808–822. (https://doi.org/10.1016/j.cell.2014.02.056)

    • Search Google Scholar
    • Export Citation

  • Coronel CE, Winnica DE, Novella ML & Lardy HA 1992 Purification, structure, and characterization of caltrin proteins from seminal vesicle of the rat and mouse. Journal of Biological Chemistry 267 20909–20915. (https://doi.org/10.1016/S0021-9258(1936774-2)

    • Search Google Scholar
    • Export Citation

  • Cross NL 2004 Reorganization of lipid rafts during capacitation of human sperm. Biology of Reproduction 71 1367–1373. (https://doi.org/10.1095/biolreprod.104.030502)

    • Search Google Scholar
    • Export Citation

  • de Lamirande E, Yoshida K, Yoshiike TM, Iwamoto T & Gagnon C 2001 Semenogelin, the main protein of semen coagulum, inhibits human sperm capacitation by interfering with the superoxide anion generated during this process. Journal of Andrology 22 672–679. (https://doi.org/10.1002/j.1939-4640.2001.tb02228.x)

    • Search Google Scholar
    • Export Citation

  • Dematteis A, Miranda SD, Novella ML, Maldonado C, Ponce RH, Maldera JA, Cuasnicu PS & Coronel CE 2008 Rat caltrin protein modulates the acrosomal exocytosis during sperm capacitation. Biology of Reproduction 79 493–500. (https://doi.org/10.1095/biolreprod.107.067538)

    • Search Google Scholar
    • Export Citation

  • Dietl T, Kruck J, Schill WB & Fritz H 1976 Localization of seminal plasma proteinase inhibitors in human spermatozoa as revealed by the indirect immunofluorescence technique. Hoppe-Seyler’s Zeitschrift für Physiologische Chemie 357 1333–1337. (https://doi.org/10.1515/bchm2.1976.357.2.1333)

    • Search Google Scholar
    • Export Citation

  • Fraser LR 1984 Mouse sperm capacitation in vitro involves loss of a surface-associated inhibitory component. Journal of Reproduction and Fertility 72 373–384. (https://doi.org/10.1530/jrf.0.0720373)

    • Search Google Scholar
    • Export Citation

  • Fraser LR, Harrison RAP & Herod JE 1990 Characterization of a decapacitation factor associated with epididymal mouse spermatozoa. Journal of Reproduction and Fertility 89 135–148. (https://doi.org/10.1530/jrf.0.0890135)

    • Search Google Scholar
    • Export Citation

  • Gimeno BF, Bariani MV, Laiz-Quiroga L, Martínez-León E, Von-Meyeren M, Rey O, Mutto AÁ & Osycka-Salut CE 2021 Effects of in vitro interactions of oviduct epithelial cells with frozen–thawed stallion spermatozoa on their motility, viability and capacitation status. Animals 11 74. (https://doi.org/10.3390/ani11010074)

    • Search Google Scholar
    • Export Citation

  • Glomset JA 1999 Lipids protein-lipid interactions on the surfaces of cell membranes. Current Opinion in Structural Biology 9 425–427. (https://doi.org/10.1016/s0959-440x(9980058-x)

    • Search Google Scholar
    • Export Citation

  • Graf CB, Ritagliati C, Stival C, Luque GM, Gentile I, Buffone MG & Krapf D 2020 Everything you ever wanted to know about PKA regulation and its involvement in mammalian sperm capacitation. Molecular and Cellular Endocrinology 518 110992. (https://doi.org/10.1016/j.mce.2020.110992)

    • Search Google Scholar
    • Export Citation

  • Harrison RA & Gadella BM 2005 Bicarbonate-induced membrane processing in sperm capacitation. Theriogenology 63 342–351. (https://doi.org/10.1016/j.theriogenology.2004.09.016)

    • Search Google Scholar
    • Export Citation

  • Huang YH, Chu ST & Chen YH 2000 A seminal vesicle autoantigen of mouse is able to suppress sperm capacitation-related events stimulated by serum albumin. Biology of Reproduction 63 1562–1566. (https://doi.org/10.1095/biolreprod63.5.1562)

    • Search Google Scholar
    • Export Citation

  • Hummel KM, Penheiter AR, Gathman AC & Lilly WW 1996 Anomalous estimation of protease molecular weights using gelatin-containing SDS–PAGE. Analytical Biochemistry 233 140–142. (https://doi.org/10.1006/abio.1996.0019)

    • Search Google Scholar
    • Export Citation

  • Hwang JY, Mannowetz N, Zhang Y, Everley RA, Gygi SP, Bewersdorf J, Lishko PV & Chung JJ 2019 Dual sensing of physiologic pH and calcium by EFCAB9 regulates sperm motility. Cell 177 1480 .e19–1494.e19. (https://doi.org/10.1016/j.cell.2019.03.047)

    • Search Google Scholar
    • Export Citation

  • Irwin M, Nicholson N, Haywood JT & Poirier GR 1983 Immunofluorescent localization of a murine seminal vesicle proteinase inhibitor. Biology of Reproduction 28 1201–1206. (https://doi.org/10.1095/biolreprod28.5.1201)

    • Search Google Scholar
    • Export Citation

  • Ishii H, Mori T, Shiratsuchi A, Nakai Y, Shimada Y, Ohno-Iwashita Y & Nakanishi Y 2005 Distinct localization of lipid rafts and externalized phosphatidylserine at the surface of apoptotic cells. Biochemical and Biophysical Research Communications 327 94–99. (https://doi.org/10.1016/j.bbrc.2004.11.135)

    • Search Google Scholar
    • Export Citation

  • Jalkanen J, Kotimäki M, Huhtaniemi I & Poutanen M 2006 Novel epididymal protease inhibitors with Kazal or WAP family domain. Biochemical and Biophysical Research Communications 349 245–254. (https://doi.org/10.1016/j.bbrc.2006.08.023)

    • Search Google Scholar
    • Export Citation

  • Kawano N, Yoshida K, Iwamoto T & Yoshida M 2008 Ganglioside GM1 mediates decapacitation effects of SVS2 on murine spermatozoa. Biology of Reproduction 79 1153–1159. (https://doi.org/10.1095/biolreprod.108.069054)

    • Search Google Scholar
    • Export Citation

  • Kazal LA, Spicer DS & Brahinsky RA 1948 Isolation of a crystalline trypsin inhibitor-anticoagulant protein from Pancreas1a. Journal of the American Chemical Society 70 3034–3040. (https://doi.org/10.1021/ja01189a060)

    • Search Google Scholar
    • Export Citation

  • Kherraf ZE, Christou-Kent M, Karaouzene T, Amiri-Yekta A, Martinez G, Vargas AS, Lambert E, Borel C, Dorphin B & Aknin-Seifer I et al.2017 SPINK 2 deficiency causes infertility by inducing sperm defects in heterozygotes and azoospermia in homozygotes. EMBO Molecular Medicine 9 1132–1149. (https://doi.org/10.15252/emmm.201607461)

    • Search Google Scholar
    • Export Citation

  • Kutty MVH, Remya V, Shyma VH, Radhika S, Shende AM & Bhure SK 2014 An overview on binder of sperm proteins of cattle. International Journal of Livestock Research 4 1–11. (https://doi.org/10.5455/ijlr.20140629034437)

    • Search Google Scholar
    • Export Citation

  • La Spina FA, Molina LCP, Romarowski A, Vitale AM, Falzone TL, Krapf D, Hirohashi N & Buffone MG 2016 Mouse sperm begin to undergo acrosomal exocytosis in the upper isthmus of the oviduct. Developmental Biology 411 172–182. (https://doi.org/10.1016/j.ydbio.2016.02.006)

    • Search Google Scholar
    • Export Citation

  • Laemmli UK, Beguin F & Gujer-Kellenberger G 1970 A factor preventing the major head protein of bacteriophage T4 from random aggregation. Journal of Molecular Biology 47 69–85. (https://doi.org/10.1016/0022-2836(7090402-X)

    • Search Google Scholar
    • Export Citation

  • Leahy T & Gadella BM 2011 Sperm surface changes and physiological consequences induced by sperm handling and storage. Reproduction 142 759–778. (https://doi.org/10.1530/REP-11-0310)

    • Search Google Scholar
    • Export Citation

  • Lenth RV 2016 Least-squares means: the R package lsmeans. Journal of Statistical Software 69 1–33. (https://doi.org/10.18637/jss.v069.i01)

    • Search Google Scholar
    • Export Citation

  • Lin MH, Lee RKK, Hwu YM, Lu CH, Chu SL, Chen YJ, Chang WC & 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 136 559–571. (https://doi.org/10.1530/REP-07-0375)

    • Search Google Scholar
    • Export Citation

  • Lu CH, Lee RKK, Hwu YM, Chu SL, Chen YJ, Chang WC, Lin SP & Li SH 2011 SERPINE2, a serine protease inhibitor extensively expressed in adult male mouse reproductive tissues, may serve as a murine sperm decapacitation factor. Biology of Reproduction 84 514–525. (https://doi.org/10.1095/biolreprod.110.085100)

    • Search Google Scholar
    • Export Citation

  • Manchenko GP 2002 Handbook of Detection of Enzymes on Electrophoretic Gels. CRC Press. (https://doi.org/10.1201/9781420040531)

  • Manjunath P & Thérien I 2002 Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. Journal of Reproductive Immunology 53 109–119. (https://doi.org/10.1016/S0165-0378(0100098-5)

    • Search Google Scholar
    • Export Citation

  • Monclus MA, Cesari A, Cabrillana ME, Borelli PV, Vincenti AE, Burgos MH & Fornés MW 2007 Mouse sperm rosette: assembling during epididymal transit, in vitro disassemble, and oligosaccharide participation in the linkage material. Anatomical Record 290 814–824. (https://doi.org/10.1002/ar.20555)

    • Search Google Scholar
    • Export Citation

  • Navarro B, Kirichok Y & Clapham DE 2007 KSper, a pH-sensitive K+ current that controls sperm membrane potential. PNAS 104 7688–7692. (https://doi.org/10.1073/pnas.0702018104)

    • Search Google Scholar
    • Export Citation

  • Nixon B, MacIntyre DA, Mitchell LA, Gibbs GM, O’Bryan M & Aitken RJ 2006 The identification of mouse sperm-surface-associated proteins and characterization of their ability to act as decapacitation factors. Biology of Reproduction 74 275–287. (https://doi.org/10.1095/biolreprod.105.044644)

    • Search Google Scholar
    • Export Citation

  • Noda T & Ikawa M 2019 Physiological function of seminal vesicle secretions on male fecundity. Reproductive Medicine and Biology 18 241–246. (https://doi.org/10.1002/rmb2.12282)

    • Search Google Scholar
    • Export Citation

  • Odet F, Verot A & Le Magueresse-Battistoni B 2006 The mouse testis is the source of various serine proteases and serine proteinase inhibitors (serpins): serine proteases and serpins identified in Leydig cells are under gonadotropin regulation. Endocrinology 147 4374–4383. (https://doi.org/10.1210/en.2006-0484)

    • Search Google Scholar
    • Export Citation

  • O’Rand MG, Widgren EE, Hamil KG, Silva EJ & Richardson RT 2011 Epididymal protein targets: a brief history of the development of epididymal protease inhibitor as a contraceptive. Journal of Andrology 32 698–704. (https://doi.org/10.2164/jandrol.110.012781)

    • Search Google Scholar
    • Export Citation

  • Ou CM, Tang JB, Huang MS, Sudhakar Gandhi PS, Geetha S, Li SH & Chen YH 2012 The mode of reproductive-derived Spink (serine protease inhibitor Kazal-type) action in the modulation of mammalian sperm activity. International Journal of Andrology 35 52–62. (https://doi.org/10.1111/j.1365-2605.2011.01159.x)

    • Search Google Scholar
    • Export Citation

  • Pinheiro J, Bates D, DebRoy S, Sarkar D & R Core Team 2007 nlme: Linear and nonlinear mixed effects models. R package version 3.1-155, (https://CRAN.R-project.org/package=nlme)

    • Search Google Scholar
    • Export Citation

  • Puga Molina LC, Luque GM, Balestrini PA, Marín-Briggiler CI, Romarowski A & Buffone MG 2018 Molecular basis of human sperm capacitation. Frontiers in Cell and Developmental Biology 6 72. (https://doi.org/10.3389/fcell.2018.00072)

    • Search Google Scholar
    • Export Citation

  • Ramachandran SS, Balu R, Vilwanathan R, Jeyaraman J & Paramasivam SG 2021 A mouse testis serine protease, TESP1, as the potential SPINK3 receptor protein on mouse sperm acrosome. Molecular Human Reproduction 27 gaab059. (https://doi.org/10.1093/molehr/gaab059)

    • Search Google Scholar
    • Export Citation

  • Raterman D & Springer MS 2008 The molecular evolution of acrosin in placental mammals. Molecular Reproduction and Development 75 1196–1207. (https://doi.org/10.1002/mrd.20868)

    • Search Google Scholar
    • Export Citation

  • Ritagliati C, Graf CB, Stival C & Krapf D 2018 Regulation mechanisms and implications of sperm membrane hyperpolarization. Mechanisms of Development 154 33–43. (https://doi.org/10.1016/j.mod.2018.04.004)

    • Search Google Scholar
    • Export Citation

  • Rival CM, Xu W, Shankman LS, Morioka S, Arandjelovic S, Lee CS, Wheeler KM, Smith RP, Haney LB & Isakson BE et al.2019 Phosphatidylserine on viable sperm and phagocytic machinery in oocytes regulate mammalian fertilization. Nature Communications 10 4456. (https://doi.org/10.1038/s41467-019-12406-z)

    • Search Google Scholar
    • Export Citation

  • Roberts KP, Wamstad JA, Ensrud KM & Hamilton DW 2003 Inhibition of capacitation-associated tyrosine phosphorylation signaling in rat sperm by epididymal protein Crisp-1. Biology of Reproduction 69 572–581. (https://doi.org/10.1095/biolreprod.102.013771)

    • Search Google Scholar
    • Export Citation

  • Samanta L, Parida R, Dias TR & Agarwal A 2018 The enigmatic seminal plasma: a proteomics insight from ejaculation to fertilization. Reproductive Biology and Endocrinology 16 41. (https://doi.org/10.1186/s12958-018-0358-6)

    • Search Google Scholar
    • Export Citation

  • Sanllorenti PM, Tardivo DB & Conde RD 1992 Dietary level of protein regulates glyceraldehyde-3-phosphate dehydrogenase content and synthesis rate in mouse liver cytosol. Molecular and Cellular Biochemistry 115 117–128. (https://doi.org/10.1007/BF00230321)

    • Search Google Scholar
    • Export Citation

  • Schill WB, Heimburger N, Schiessler H, Stolla R & Fritz H 1975 Reversible attachment and localization of the acid-stable seminal plasma acrosin-trypsin inhibitors on boar spermatozoa as revealed by the indirect immunofluorescent staining technique. Hoppe-Seyler’s Zeitschrift fur physiologische Chemie 356 1473–1476.

    • Search Google Scholar
    • Export Citation

  • Schröter F, Müller K, Müller P, Krause E & Braun BC 2017 Recombinant expression of porcine spermadhesin AWN and its phospholipid interaction: indication for a novel lipid binding property. Reproduction in Domestic Animals 52 585–595. (https://doi.org/10.1111/rda.12953)

    • Search Google Scholar
    • Export Citation

  • Shang X, Shen C, Liu J, Tang L, Zhang H, Wang Y, Wu W, Chi J, Zhuang H & Fei J et al.2018 Serine protease PRSS55 is crucial for male mouse fertility via affecting sperm migration and sperm–egg binding. Cellular and Molecular Life Sciences 75 4371–4384. (https://doi.org/10.1007/s00018-018-2878-9)

    • Search Google Scholar
    • Export Citation

  • Sipila P, Jalkanen J, Huhtaniemi IT & Poutanen M 2009 Novel epididymal proteins as targets for the development of post-testicular male contraception. Reproduction 137 379–389. (https://doi.org/10.1530/REP-08-0132)

    • Search Google Scholar
    • Export Citation

  • Stival C, La Spina FA, Graf CB, Arcelay E, Arranz SE, Ferreira JJ, Le Grand S, Dzikunu VA, Santi CM & Visconti PE et al.2015 Src kinase is the connecting player between protein kinase A (PKA) activation and hyperpolarization through SLO3 potassium channel regulation in mouse sperm. Journal of Biological Chemistry 290 18855–18864. (https://doi.org/10.1074/jbc.M115.640326)

    • Search Google Scholar
    • Export Citation

  • Töpfer-Petersen E, Romero A, Varela PF, Ekhlasi-Hundrieser M, Dostalova Z, Sanz L & Calvete JJ 1998 Spermadhesins: a new protein family. Facts, hypotheses and perspectives. Andrologia 30 217–224. (https://doi.org/10.1111/j.1439-0272.1998.tb01163.x)

    • Search Google Scholar
    • Export Citation

  • Tseng HC, Lee RKK, Hwu YM, Lu CH, Lin MH & Li SH 2013 Mechanisms underlying the inhibition of murine sperm capacitation by the seminal protein, SPINKL. Journal of Cellular Biochemistry 114 888–898. (https://doi.org/10.1002/jcb.24428)

    • Search Google Scholar
    • Export Citation

  • Turpeinen U, Koivunen E & Stenman UH 1988 Reaction of a tumour-associated trypsin inhibitor with serine proteinases associated with coagulation and tumour invasion. Biochemical Journal 254 911–914. (https://doi.org/10.1042/bj2540911)

    • Search Google Scholar
    • Export Citation

  • Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M & Cox J 2016 The Perseus computational platform for comprehensive analysis of (prote) omics data. Nature Methods 13 731–740. (https://doi.org/10.1038/nmeth.3901)

    • Search Google Scholar
    • Export Citation

  • Veselský L & Čechová D 1980 Distribution of acrosin inhibitors in bull reproductive tissues and spermatozoa. Hoppe-Seyler’s Zeitschrift fur Physiologische Chemie 361 715–722. (https://doi.org/10.1515/bchm2.1980.361.1.715)

    • Search Google Scholar
    • Export Citation

  • Yamashita M, Honda A, Ogura A, Kashiwabara SI, Fukami K & Baba T 2008 Reduced fertility of mouse epididymal sperm lacking Prss21/Tesp5 is rescued by sperm exposure to uterine microenvironment. Genes to Cells 13 1001–1013. (https://doi.org/10.1111/j.1365-2443.2008.01222.x)

    • Search Google Scholar
    • Export Citation

  • Yanagimachi R 1994 Fertility of mammalian spermatozoa: its development and relativity. Zygote 2 371–372. (https://doi.org/10.1017/S0967199400002240)

    • Search Google Scholar
    • Export Citation

  • Zalazar L, Saez Lancellotti TE, Clementi M, Lombardo C, Lamattina L, De Castro R, Fornes MW & Cesari A 2012 SPINK3 modulates mouse sperm physiology through the reduction of nitric oxide level independently of its trypsin inhibitory activity. Reproduction 143 281–295. (https://doi.org/10.1530/REP-11-0107)

    • Search Google Scholar
    • Export Citation

  • Zalazar L, Alonso CAI, De Castro RE & Cesari A 2014 An alternative easy method for antibody purification and analysis of protein–protein interaction using GST fusion proteins immobilized onto glutathione–agarose. Analytical and Bioanalytical Chemistry 406 911–914. (https://doi.org/10.1007/s00216-013-7533-6)

    • Search Google Scholar
    • Export Citation

  • Zalazar L, Stival C, Nicolli AR, De Blas GA, Krapf D & Cesari A 2020 Male decapacitation factor SPINK3 blocks membrane hyperpolarization and calcium entry in mouse sperm. Frontiers in Cell and Developmental Biology 8 575126. (https://doi.org/10.3389/fcell.2020.575126)

    • Search Google Scholar
    • Export Citation

  • Zhou Y, Zheng M, Shi Q, Zhang L, Zhen W, Chen W & Zhang Y 2008 An epididymis-specific secretory protein HongrES1 critically regulates sperm capacitation and male fertility. PLoS ONE 3 e4106. (https://doi.org/10.1371/journal.pone.0004106)

    • Search Google Scholar
    • Export Citation

  • Zigo M, Manaskova-Postlerova P, Jonakova V, Kerns K & Sutovsky P 2019 Compartmentalization of the proteasome-interacting proteins during sperm capacitation. Scientific Reports 9 12583. (https://doi.org/10.1038/s41598-019-49024-0)

    • Search Google Scholar
    • Export Citation

  • Zuur AF, Ieno EN, Walker N, Saveliev AA & Smith GM 2009 Mixed Effects Models and Extensions in Ecology with R. New York: SpringerGoogle Scholar.