Synergism between albumin, bicarbonate and cAMP upregulation for cholesterol efflux from ram sperm

in Reproduction
Authors:
Naomi C Bernecic School of Life and Environmental Sciences, Faculty of Science, The University of Sydney, New South Wales, Australia

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Bart M Gadella Department of Biochemistry & Cell Biology, Utrecht University, Utrecht, The Netherlands
Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands

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Simon P de Graaf School of Life and Environmental Sciences, Faculty of Science, The University of Sydney, New South Wales, Australia

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Tamara Leahy School of Life and Environmental Sciences, Faculty of Science, The University of Sydney, New South Wales, Australia

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Correspondence should be addressed to N C Bernecic; Email: Naomi.Bernecic@ul.ie
DOI:
https://doi.org/10.1530/REP-19-0430
Volume/Issue:
Volume 160: Issue 2
Page Range:
269–280
Article Type:
Research Article
Online Publication Date:
Aug 2020
Copyright:
© 2020 Society for Reproduction and Fertility 2020
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Compared to other mammalian species, ram spermatozoa are difficult to capacitate in vitro. Dibutyryl cAMP (db-cAMP) and the phosphodiesterase (PDE) inhibitors, caffeine and theophylline (cAMP up-regulators), must be added to traditional capacitation media (containing bicarbonate, calcium and BSA) to elicit a capacitation response. In this exploratory study, we assessed whether bicarbonate was still required for ram spermatozoa if cAMP is up-regulated by the addition of db-cAMP and PDE inhibitors and what role BSA plays in cholesterol efflux under these conditions. In this study, the validated BODIPY-cholesterol assay was used for the first time in ram spermatozoa to quantify cholesterol efflux by tracking the loss of BODIPY-cholesterol from the sperm plasma membrane using flow cytometry. The results show that under cAMP up-regulated conditions, an increase in membrane fluidity and tyrosine phosphorylation of sperm proteins remain as bicarbonate-dependent processes. In fact, the supplementation of bicarbonate under these conditions was necessary to further enhance cAMP production in ram spermatozoa, which correlated with the presence of these capacitation-related processes. When BSA was supplemented with cAMP up-regulators (as well as bicarbonate), there was a loss of approximately 20–23% of BODIPY-cholesterol (79.5 ± 30.5% to 76.9 ± 12.3% remaining from 10 min), indicating that BSA is essential for mediating cholesterol efflux in ram spermatozoa as measured by the BODIPY-cholesterol assay. The current study identifies the functional relationship between bicarbonate, BSA and cAMP up-regulators that is required to support capacitation-related processes in ram spermatozoa, specifically cholesterol efflux.

Supplementary Materials

    • Supplementary Table 1. Motility and kinematic parameters assessed using computer-assisted sperm analysis (CASA) following exposure to media with or without bicarbonate and cAMP-regulators (BSA present in all conditions) for up to 3 h (180 min).
    • Supplementary Table 2. Motility and kinematic parameters assessed using computer-assisted sperm analysis (CASA) following exposure to media with or without BSA and cAMP-regulators (bicarbonate present in all conditions) for up to 3 h (180 min).
    • Supplementary Figure 1. The percentage of PI- and PI+ acrosome intact (A and B) and PI+ acrosome reacted (C) spermatozoa following exposure to conditions with or without bicarbonate and cAMP up-regulators (db-cAMP, caffeine and theophylline) for up to 3h (180 min). Membrane and acrosome integrity were assessed with flow cytometry using propidium iodide and PNA-FITC, respectively. Data correspond to mean ± S.D. (A and C) or geometric mean ± 95% confidence interval (B) for ten independent samples. **P<0.01 and ***P<0.001 indicate significant differences from TALP (bicarbonate and BSA)
    • Supplementary Figure 2. The percentage of PI- and PI+ acrosome intact (A and B) and PI+ acrosome reacted (C) spermatozoa following exposure to conditions with or without BSA and cAMP up-regulators (db-cAMP, caffeine and theophylline) for up to 3h (180 min). Membrane and acrosome integrity were assessed with flow cytometry using propidium iodide and PNA-FITC, respectively. Data correspond to mean ± S.D. (A and C) or geometric mean ± 95% confidence interval (B) for seven independent samples. *P<0.05, **P<0.01 and ***P<0.001 indicate significant differences from TALP (bicarbonate and BSA).
    • Supplementary Figure 3. The percentage of Yo-Pro-1- spermatozoa with high (A) and low (B) membrane fluidity following exposure to conditions with or without bicarbonate and cAMP up-regulators (db-cAMP, caffeine and theophylline) for up to 3h (180 min). Membrane fluidity and integrity were assessed with flow cytometry using merocyanine 540 (M540) and Yo-Pro, respectively. Data correspond to geometric mean ± 95% confidence interval (A) or mean ± S.D. (B) for ten independent samples. ***P<0.001 indicate significant differences from TALP (bicarbonate and BSA).
    • Supplementary Figure 4. The percentage of Yo-Pro-1- spermatozoa with high (A) and low (B) membrane fluidity following exposure to conditions with or without BSA and cAMP up-regulators (db-cAMP, caffeine and theophylline) for up to 3h (180 min). Membrane fluidity and integrity were assessed with flow cytometry using merocyanine 540 (M540) and Yo-Pro, respectively. Data correspond to geometric mean ± 95% confidence interval (A) or mean ± S.D. (B) for seven independent samples. *P<0.05 and ***P<0.001 indicate significant differences from TALP (bicarbonate and BSA).

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Print ISSN:
1470-1626
Online ISSN:
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  • Aitken RJ & Nixon B 2013 Sperm capacitation: a distant landscape glimpsed but unexplored. Molecular Human Reproduction 19 785–793. (https://doi.org/10.1093/molehr/gat067)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Alonso CAI, Osycka-Salut CE, Castellano L, Cesari A, Di Siervi N, Mutto A, Johannisson A, Morrell JM, Davio C & Perez-Martinez S 2017 Extracellular cAMP activates molecular signalling pathways associated with sperm capacitation in bovines. Molecular Human Reproduction 23 521–534. (https://doi.org/10.1093/molehr/gax030)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Arnoult C, Kazam IG, Visconti PE, Kopf GS, Villaz M & Florman HM 1999 Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. PNAS 96 6757–6762. (https://doi.org/10.1073/pnas.96.12.6757)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Austin CR 1951 Observations on the penetration of the sperm in the mammalian egg. Australian Journal of Scientific Research B 4 581–596. (https://doi.org/10.1071/bi9510581)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bailey JL 2010 Factors regulating sperm capacitation. Systems Biology in Reproductive Medicine 56 334–348. (https://doi.org/10.3109/19396368.2010.512377)

  • Bajpai M, Fiedler SE, Huang Z, Vijayaraghavan S, Olson GE, Livera G, Conti M & Carr DW 2006 AKAP3 selectively binds PDE4A isoforms in bovine spermatozoa. Biology of Reproduction 74 109–118. (https://doi.org/10.1095/biolreprod.105.043588)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Battistone MA, Da Ros VG, Salicioni AM, Navarrete FA, Krapf D, Visconti PE & Cuasnicu PS 2013 Functional human sperm capacitation requires both bicarbonate-dependent PKA activation and down-regulation of Ser/Thr phosphatases by Src family kinases. Molecular Human Reproduction 19 570–580. (https://doi.org/10.1093/molehr/gat033)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Baxendale RW & Fraser LR 2005 Mammalian sperm phosphodiesterases and their involvement in receptor-mediated cell signaling important for capacitation. Molecular Reproduction and Development 71 495–508. (https://doi.org/10.1002/mrd.20265)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bergeron A, Aragon JP, Guillemette C, Hébert A, Sullivan R, Blondin P & Richard FJ 2016 Characterization of cAMP-phosphodiesterase activity in bovine seminal plasma. Andrology 4 1123–1130. (https://doi.org/10.1111/andr.12267)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bernecic NC, Zhang M, Gadella BM, Brouwers JFHM, Jansen JWA, Arkesteijn GJA, de Graaf SP & Leahy T 2019 BODIPY-cholesterol can be reliably used to monitor cholesterol efflux from capacitating mammalian spermatozoa. Scientific Reports 9 9804. (https://doi.org/10.1038/s41598-019-45831-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bromfield EG, Aitken RJ, Gibb Z, Lambourne SR & Nixon B 2014 Capacitation in the presence of methyl-beta-cyclodextrin results in enhanced zona pellucida-binding ability of stallion spermatozoa. Reproduction 147 153–166. (https://doi.org/10.1530/REP-13-0393)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Buffone MG, Wertheimer EV, Visconti PE & Krapf D 2014 Central role of soluble adenylyl cyclase and cAMP in sperm physiology. Biochimica et Biophysica Acta 1842 2610–2620. (https://doi.org/10.1016/j.bbadis.2014.07.013)

    • PubMed
    • 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)

  • Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR & Buck J 2000 Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289 625–628. (https://doi.org/10.1126/science.289.5479.625)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Colas C, James P, Howes L, Jones R, Cebrian-Perez JA & Muiño-Blanco T 2008 Cyclic-AMP initiates protein tyrosine phosphorylation independent of cholesterol efflux during ram sperm capacitation. Reproduction, Fertility, and Development 20 649–658. (https://doi.org/10.1071/RD08023)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dacheux JL & Dacheux F 2014 New insights into epididymal function in relation to sperm maturation. Reproduction 147 R27–R42. (https://doi.org/10.1530/REP-13-0420)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Darin-Bennett A & White IG 1977 Influence of the cholesterol content of mammalian spermatozoa on susceptibility to cold-shock. Cryobiology 14 466–470. (https://doi.org/10.1016/0011-2240(77)90008-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • de Vries KJ, Wiedmer T, Sims PJ & Gadella BM 2003 Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells. Biology of Reproduction 68 2122–2134. (https://doi.org/10.1095/biolreprod.102.012500)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Demarco IA, Espinosa F, Edwards J, Sosnik J, De la Vega-Beltrán JL, Hockensmith JW, Kopf GS, Darszon A & Visconti PE 2003 Involvement of a Na+/HCO3 – cotransporter in mouse sperm capacitation. Journal of Biological Chemistry 278 7001–7009. (https://doi.org/10.1074/jbc.M206284200)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Dimitriadis F, Giannakis D, Pardalidis N, Zikopoulos K, Paraskevaidis E, Giotitsas N, Kalaboki V, Tsounapi P, Baltogiannis D & Georgiou I et al.2008 Effects of phosphodiesterase 5 inhibitors on sperm parameters and fertilizing capacity. Asian Journal of Andrology 10 115–133. (https://doi.org/10.1111/j.1745-7262.2008.00373.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Evans G 1987 Salamon’s Artificial Insemination of Sheep and Goats. Sydney: Butterworths.

  • Fisch JD, Behr B & Conti M 1998 Enhancement of motility and acrosome reaction in human spermatozoa: differential activation by type-specific phosphodiesterase inhibitors. Human Reproduction 13 1248–1254. (https://doi.org/10.1093/humrep/13.5.1248)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Flesch FM, Brouwers JFHM, Nievelstein PFEM, Verkleij AJ, van Golde LMG, 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.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gadella BM & Harrison RAP 2000 The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane. Development 127 2407–2420.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gadella BM & Harrison RAP 2002 Capacitation induces cyclic adenosine 3′,5′-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biology of Reproduction 67 340–350. (https://doi.org/10.1095/biolreprod67.1.340)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gadella BM, Tsai PS, Boerke A & Brewis IA 2008 Sperm head membrane reorganisation during capacitation. International Journal of Developmental Biology 52 473–480. (https://doi.org/10.1387/ijdb.082583bg)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Galantino-Homer HL, Visconti PE & Kopf GS 1997 Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3',5'-monophosphate-dependent pathway. Biology of Reproduction 56 707–719. (https://doi.org/10.1095/biolreprod56.3.707)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Galantino-Homer HL, Florman HM, Storey BT, Dobrinski I & Kopf GS 2004 Bovine sperm capacitation: assessment of phosphodiesterase activity and intracellular alkalinization on capacitation-associated protein tyrosine phosphorylation. Molecular Reproduction and Development 67 487–500. (https://doi.org/10.1002/mrd.20034)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Grasa P, Cebrián-Pérez JA & Muiño-Blanco T 2006 Signal transduction mechanisms involved in ram sperm capacitation. Reproduction 132 721–732. (https://doi.org/10.1530/rep.1.00770)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Grasa P, Perez-Pe R, Baguena O, Forcada F, Abecia A, Cebrian-Perez JA & Muino-Blanco T 2004 Ram sperm selection by a dextran/swim-up procedure increases fertilization rates following intrauterine insemination in superovulated ewes. Journal of Andrology 25 982–990. (https://doi.org/10.1002/j.1939-4640.2004.tb03171.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

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

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Harrison RAP & Miller NGA 2000 cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm. Molecular Reproduction and Development 55 220–228. (https://doi.org/10.1002/(SICI)1098-2795(200002)55:2<220::AID-MRD12>3.0.CO;2-I)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Harrison RAP, Ashworth PJC & Miller NGA 1996 Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Molecular Reproduction and Development 45 378–391. (https://doi.org/10.1002/(SICI)1098-2795(199611)45:3<378::AID-MRD16>3.0.CO;2-V)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hess KC, Jones BH, Marquez B, Chen Y, Ord TS, Kamenetsky M, Miyamoto C, Zippin JH, Kopf GS & Suarez SS et al.2005 The ‘soluble’ adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Developmental Cell 9 249–259. (https://doi.org/10.1016/j.devcel.2005.06.007)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hölttä-Vuori M, Uronen RL, Repakova J, Salonen E, Vattulainen I, Panula P, Li Z, Bittman R & Ikonen E 2008 BODIPY-cholesterol: a new tool to visualize sterol trafficking in living cells and organisms. Traffic 9 1839–1849. (https://doi.org/10.1111/j.1600-0854.2008.00801.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kerns K, Zigo M, Drobnis EZ, Sutovsky M & Sutovsky P 2018 Zinc ion flux during mammalian sperm capacitation. Nature Communications 9 2061. (https://doi.org/10.1038/s41467-018-04523-y)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Leahy T & Gadella BM 2015 New insights into the regulation of cholesterol efflux from the sperm membrane. Asian Journal of Andrology 17 561–567. (https://doi.org/10.4103/1008-682X.153309)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Leahy T, Rickard JP, Aitken RJ & de Graaf SP 2016 Penicillamine prevents ram sperm agglutination in media that support capacitation. Reproduction 151 167–177. (https://doi.org/10.1530/REP-15-0413)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Leclerc P, de Lamirande E & Gagnon C 1996 Cyclic adenosine 3',5'monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biology of Reproduction 55 684–692. (https://doi.org/10.1095/biolreprod55.3.684)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Leemans B, Stout TAE, De Schauwer C, Heras S, Nelis H, Hoogewijs M, Van Soom A & Gadella BM 2019 Update on mammalian sperm capacitation: how much does the horse differ from other species? Reproduction 157 R181–R197. (https://doi.org/10.1530/REP-18-0541)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lefievre L, de Lamirande E & Gagnon C 2000 The cyclic GMP-specific phosphodiesterase inhibitor, sildenafil, stimulates human sperm motility and capacitation but not acrosome reaction. Journal of Andrology 21 929–937. (https://doi.org/10.1002/j.1939-4640.2000.tb03424.x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Monks NJ & Fraser LR 1987 Phosphodiesterase activity of mouse sperm incubated under conditions that modulate fertilizing potential in vitro. Gamete Research 18 85–96. (https://doi.org/10.1002/mrd.1120180110)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • MyAssays Ltd. 2018 ‘Four parameter logistic curve’ online analysis tool. (available at: http://www.myassays.com/four-parameter-logistic-curve.assay)

  • Okamura N, Tajima Y, Soejima A, Masuda H & Sugita Y 1985 Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylate cyclase. Journal of Biological Chemistry 260 9699–9705.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Osheroff JE, Visconti PE, Valenzuela JP, Travis AJ, Alvarez J & Kopf GS 1999 Regulation of human sperm capacitation by a cholesterol efflux- stimulated signal transduction pathway leading to protein kinase A-mediated up-regulation of protein tyrosine phosphorylation. Molecular Human Reproduction 5 1017–1026. (https://doi.org/10.1093/molehr/5.11.1017)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Osycka-Salut CE, Diez F, Burdet J, Gervasi MG, Franchi A, Bianciotti LG, Davio C & Perez-Martinez S 2014 Cyclic AMP efflux, via MRPs and A I adenosine receptors, is critical for bovine sperm capacitation. Molecular Human Reproduction 20 89–99. (https://doi.org/10.1093/molehr/gat053)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Parrish JJ, Susko-Parrish JL, Winer MA & First NL 1988 Capacitation of bovine sperm by heparin. Biology of Reproduction 38 1171–1180. (https://doi.org/10.1095/biolreprod38.5.1171)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Parrish JJ, Susko-Parrish JL & Graham JK 1999 In vitro capacitation of bovine spermatozoa: role of intracellular calcium. Theriogenology 51 461–472. (https://doi.org/10.1016/S0093-691X(98)00240-4)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pérez-Pé R, Grasa P, Fernández-Juan M, Peleato ML, Cebrián-Pérez JA & Muiño-Blanco T 2002 Seminal plasma proteins reduce protein tyrosine phosphorylation in the plasma membrane of cold-shocked ram spermatozoa. Molecular Reproduction and Development 61 226–233. (https://doi.org/10.1002/mrd.1152)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Pini T, de Graaf SP, Druart X, Tsikis G, Labas V, Teixeira-Gomes AP, Gadella BM & Leahy T 2018 Binder of sperm proteins 1 and 5 have contrasting effects on the capacitation of ram spermatozoa. Biology of Reproduction 98 765–775. (https://doi.org/10.1093/biolre/ioy032)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Richter W, Dettmer D & Glander HJ 1999 Detection of mRNA transcripts of cyclic nucleotide phosphodiesterase subtypes in ejaculated human spermatozoa. Molecular Human Reproduction 5 732–736. (https://doi.org/10.1093/molehr/5.8.732)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sankaranarayanan S, Kellner-Weibel G, De La Llera-Moya M, Phillips MC, Asztalos BF, Bittman R & Rothblat GH 2011 A sensitive assay for ABCA1-mediated cholesterol efflux using BODIPY-cholesterol. Journal of Lipid Research 52 2332–2340. (https://doi.org/10.1194/jlr.D018051)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Shadan S, James PS, Howes EA & Jones R 2004 Cholesterol efflux alters lipid raft stability and distribution during capacitation of boar spermatozoa. Biology of Reproduction 71 253–265. (https://doi.org/10.1095/biolreprod.103.026435)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Soriano-Úbeda C, Romero-Aguirregomezcorta J, Matás C, Visconti PE & García-Vázquez FA 2019 Manipulation of bicarbonate concentration in sperm capacitation media improves in vitro fertilisation output in porcine species. Journal of Animal Science and Biotechnology 10 19. (https://doi.org/10.1186/s40104-019-0324-y)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Suarez SS & Dai X 1995 Intracellular calcium reaches different levels of elevation in hyperactivated and acrosome-reacted hamster sperm. Molecular Reproduction and Development 42 325–333. (https://doi.org/10.1002/mrd.1080420310)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Suarez SS, Varosi SM & Dai X 1993 Intracellular calcium increases with hyperactivation in intact, moving hamster sperm and oscillates with the flagellar beat cycle. PNAS 90 4660–4664. (https://doi.org/10.1073/pnas.90.10.4660)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Takeo T, Hoshii T, Kondo Y, Toyodome H, Arima H, Yamamura K-i, Irie T & Nakagata N 2008 Methyl-beta-cyclodextrin improves fertilizing ability of C57BL/6 mouse sperm after freezing and thawing by facilitating cholesterol efflux from the cells. Biology of Reproduction 78 546–551. (https://doi.org/10.1095/biolreprod.107.065359)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tash JS 1976 Investigations on adenosine 3',5'-monophosphate phosphodiesterase in ram semen and initial characterization of a sperm specific isoenzyme. Journal of Reproduction and Fertility 47 63–72. (https://doi.org/10.1530/jrf.0.0470063)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • van Gestel RA, Brewis IA, Ashton PR, Helms JB, Brouwers JFHM & 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. (https://doi.org/10.1093/molehr/gah200)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P & Kopf GS 1995a Capacitation of mouse spermatozoa. 1. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121 1129–1137.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, Olds-Clarke P & Kopf GS 1995b Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121 1139–1150.

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Visconti PE, Ning X, Fornés MW, Alvarez JG, Stein P, Connors SA & Kopf GS 1999 Cholesterol efflux-mediated signal transduction in mammalian sperm: cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation. Developmental Biology 214 429–443. (https://doi.org/10.1006/dbio.1999.9428)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Xie F, Garcia MA, Carlson AE, Schuh SM, Babcock DF, Jaiswal BS, Gossen JA, Esposito G, van Duin M & Conti M 2006 Soluble adenylyl cyclase (sAC) is indispensable for sperm function and fertilization. Developmental Biology 296 353–362. (https://doi.org/10.1016/j.ydbio.2006.05.038)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yanagimachi R 1994 Mammalian fertilization. In The Physiology of Reproduction, pp. 189–317. Eds Knobil E & Neill JD. New York: Raven Press.

  • Yanagimachi R 2011 Mammalian sperm acrosome reaction: where does it begin before fertilization? Biology of Reproduction 85 4–5. (https://doi.org/10.1095/biolreprod.111.092601)

    • PubMed
    • Search Google Scholar
    • Export Citation