Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0122
Animal Reproduction (AR)
Conference papers

Different approaches for assessing sperm function

Diego Bucci, Marcella Spinaci, Giovanna Galeati, Carlo Tamanini

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Abstract

Different approaches can be used to assess sperm function in different conditions, i.e. sperm storage, freezing-thawing or activation by induction of capacitation and acrosome reaction. In this review we will focus on the assays routinely performed in our laboratories, giving a literature support to critically analyse different approaches. In fact, researchers usually tend to look for the “one shot” parameter that could explain itself a specific process; it is our conviction that a multiparametric approach is still more valid, as some changes in sperm function are very complex and could be explained only by operating in different ways. Sperm motility, the most evident sperm characteristic, should be assessed by computer-aided sperm analysers that permit an objective evaluation of the motility and its kinematic parameters. Commercial and open source instruments are available and could be profitably used together with specific statistical approaches. The use of microscopy, and particularly fluorescent microscopy, could be a very useful tool to assess different parameters in sperm cells both by fluorophores that give indication of a determined function, and by immunolocalization of proteins, that permits the discover of new features or to explain particular sperm functions. The same substrates could be used also in flow cytometry: the difference is that it permits to study wider sperm populations (and their sub-population distribution). Flow cytometry is undergoing a very wide use in spermatology and technical and experimental rigor is needed to obtain reliable results. Metabolic assessment of sperm features, particularly energetic supply, ATP formation and other enzyme activities, could represent a very important challenge to acquire new information and complete/integrate those derived from other techniques. Finally, functional assays such as oocyte binding and in vitro fertilization, represent a very strong tool to assess sperm function in vitro, as they could evidence the functional intactness of some pathways.

Keywords

sperm function, multiparametric approach.

References

Aitken RJ, Wingate JK, De Iuliis GN, McLaughlin EA. 2007. Analysis of lipid peroxidation in human spermatozoa using BODIPY C11. Mol Hum Reprod, 13, 203-211.

Albarracín JL, Fernández-Novell JM, Ballester J, Rauch MC, Quintero-Moreno A, Peña A, Mogas T, Rigau T, Yañez A, Guinovart JJ, Slebe JC, Concha II, Rodríguez-Gil JE. 2004. Gluconeogenesis-linked glycogen metabolism is important in the achievement of in vitro capacitation of dog spermatozoa in a medium without glucose. Biol Reprod, 71, 1437-1445.

Alkmin DV, Martinez-Alborcia MJ, Parrilla I, Vazquez JM, Martinez EA, Roca J. 2013. The nuclear DNA longevity in cryopreserved boar spermatozoa assessed using the Sperm-Sus-Halomax. Theriogenology, 79:1294-1300.

Amann RP, Katz DF. 2004. Andrology lab corner: reflections on CASA after 25 years. J Androl, 25:317-325.

Amann RP, Waberski D. 2014. Computer-assisted sperm analysis (CASA): Capabilities and potential developments. Theriogenology, 81:5-17.

Angulo C, Rauch MC, Droppelmann A, Reyes AM, Slebe JC, Delgado-López F, Guaiquil VH, Vera JC, Concha II. 1998. Hexose transporter expression and function in mammalian spermatozoa: cellular localization and transport of hexoses and vitamin C. J Cell Biochem, 71:189-203.

Balao da Silva CM, Spinaci M, Bucci D, Giaretta E, Peña FJ, Mari G, Galeati G. 2013. Effect of sex sorting on stallion spermatozoa: Heterologous oocyte binding, tyrosine phosphorylation and acrosome reaction assay. Anim Reprod Sci, 141:68-74.

Ballester J, Fernández-Novell JM, Rutllant J, García-Rocha M, Jesús Palomo M, Mogas T, Peña A, Rigau T, Guinovart JJ, Rodríguez-Gil JE. 2000. Evidence for a functional glycogen metabolism in mature mammalian spermatozoa. Mol Reprod Dev, 56:207-219.

Barrier Battut I, Kempfer A, Becker J, Lebailly L, Camugli S, Chevrier L. 2016. Development of a new fertility prediction model for stallion semen, including flow cytometry. Theriogenology, 86:1111-1131.

Battut IB, Kempfer A, Lemasson N, Chevrier L, Camugl S. 2017. Prediction of the fertility of stallion frozen-thawed semen using a combination of computer-assisted motility analysis, microscopical observation and flow cytometry. Theriogenology, 97:186-200.

Boryshpolets S, Kowalski RK, Dietrich GJ, Dzyuba B, Ciereszko A. 2013. Different computer-assisted sperm analysis (CASA) systems highly influence sperm motility parameters. Theriogenology, 80:758-765.

Boryshpolets S, Pérez-Cerezales S, Eisenbach M. 2015. Behavioral mechanism of human sperm in thermotaxis: A role for hyperactivation. Hum Reprod, 30:884-892.

Brener E. 2002. Remodeling of the actin cytoskeleton during mammalian sperm capacitation and acrosome reaction. Biol Reprod, 68:837-845.

Bucci D, Isani G, Spinaci M, Tamanini C, Mari G, Zambelli D, Galeati G. 2010a. Comparative immunolocalization of GLUTs 1, 2, 3 and 5 in boar, stallion and dog spermatozoa. Reprod Domest Anim, 45:315-322.

Bucci D, Spinaci M, Vallorani C, Contri A, Carluccio A, Isani G, Tamanini C, Galeati G. 2010b. Detection and localization of GLUTs 1, 2, 3 and 5 in donkey spermatozoa. Reprod Domest Anim, 45:e217-20.

Bucci D, Rodríguez-Gil JE, Vallorani C, Spinaci M, Galeati G, Tamanini C. 2011. GLUTs and mammalian sperm metabolism. J Androl, 32, 348-355.

Bucci D, Galeati G, Tamanini C, Vallorani C, Rodriguez-Gil JE, Spinaci M. 2012. Effect of sex sorting on CTC staining, actin cytoskeleton and tyrosine phosphorylation in bull and boar spermatozoa. Theriogenology, 77:1206-1216.

Bucci D, Isani G, Giaretta E, Spinaci M, Tamanini C, Ferlizza E, Galeati G. 2014. Alkaline phosphatase in boar sperm function. Andrology, 2:100-106.

Bucci D, Giaretta E, Spinaci M, Rizzato G, Isani G, Mislei B, Mari G, Tamanini C, Galeati G. 2016. Characterization of alkaline phosphatase activity in seminal plasma and in fresh and frozen-thawed stallion spermatozoa. Theriogenology, 85:288-295.

Bucci D, Giaretta E, Merlo B, Iacono E, Spinaci M, Gadani B, Mari G, Tamanini C, Galeati G. 2017. Alkaline phosphatase added to capacitating medium enhances horse sperm-zona pellucida binding. Theriogenology, 87:72-78.

Bucci D, Spinaci M, Yeste M, Mislei B, Gadani B, Prieto N, Love C, Mari G, Tamanini C, Galeati G. 2018. Combined effects of resveratrol and epigallocatechin-3-gallate on post thaw boar sperm and IVF parameters. Theriogenology, 117:16-25.

Burant CF. 1992. Fructose transporter in human spermatozoa and small intestine is GLUTS. J. Biol. Chem. 267, 14523-14526.

Cocchia N, Pasolini MP, Mancini R, Petrazzuolo O, Cristofaro I, Rosapane I, Sica A, Tortora G, Lorizio R, Paraggio G, Mancini A. 2011. Effect of sod

(superoxide dismutase) protein supplementation in semen extenders on motility, viability, acrosome status and ERK (extracellular signal-regulated kinase) protein phosphorylation of chilled stallion spermatozoa. Theriogenology, 75:1201-1210.

Contri A, Valorz C, Faustini M, Wegher L, Carluccio A. 2010. Effect of semen preparation on casa motility results in cryopreserved bull spermatozoa. Theriogenology, 74:424-435.

Davila MP, Muñoz PM, Tapia JA, Ferrusola CO, Da Silva C CB, Peña FJ. 2015. Inhibition of mitochondrial complex I leads to decreased motility and membrane integrity related to increased hydrogen peroxide and reduced ATP production, while the inhibition of glycolysis has less impact on sperm motility. PLoS One, 10:e0138777.

De Ambrogi M, Spinaci M, Galeati G, Tamanini C. 2006. Viability and DNA fragmentation in differently sorted boar spermatozoa. Theriogenology, 66:1994-2000.

Didion BA, Kasperson KM, Wixon RL, Evenson DP. 2009. Boar fertility and sperm chromatin structure status: A retrospective report. J Androl, 30:655-660.

Fernández-Novell JM, Ballester J, Medrano A, Otaegui PJ, Rigau T, Guinovart JJ, Rodríguez-Gil JE. 2004. The presence of a high-Km hexokinase activity in dog, but not in boar, sperm. FEBS Lett, 570:211-216.

Flesch FM, Brouwers JF, Nievelstein PF, Verkleij AJ, van Golde LM, Colenbrander B, Gadella BM. 2001. Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J Cell Sci, 114:3543-3555.

Flores E, Cifuentes D, Fernández-Novell JM, Medrano A, Bonet S, Briz MD, Pinart E, Peña A, Rigau T, Rodríguez-Gil JE. 2008. Freeze-thawing induces alterations in the protamine-1/DNA overall structure in boar sperm. Theriogenology, 69:1083-1094.

Flores E, Fernández-Novell JM, Peña A, Rigau T, Rodríguez-Gil JE. 2010. Cryopreservation-induced alterations in boar spermatozoa mitochondrial function are related to changes in the expression and location of midpiece mitofusin-2 and actin network. Theriogenology, 74:354-363.

Flores E,Ramió-Lluch L, Bucci D, Fernández-Novell JM, Peña A, Rodríguez-Gil JE. 2011. Freezing-thawing induces alterations in histone H1-DNA binding and the breaking of protein-DNA disulfide bonds in boar sperm. Theriogenology, 76:1450-1464.

Ford WCL. 2006. Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round? Hum Reprod Update, 12:269-274.

Funahashi H, Cantley TC, Day BN. 1997. Preincubation of cumulus-oocyte complexes before exposure to gonadotropins improves the developmental competence of porcine embryos matured and fertilized in vitro. Theriogenology, 47:679-686.

Gadani B, Bucci D, Spinaci M, Tamanini C, Galeati G. 2017. Resveratrol and Epigallocatechin-3-gallate addition to thawed boar sperm improves in vitro fertilization. Theriogenology, 90:88-93.

Gadella BM. 2008. Sperm membrane physiology and relevance for fertilization. Anim Reprod Sci, 107:229-236.

Giaretta E, Bucci D, Mari G, Galeati G, Love CC, Tamanini C, Spinaci M. 2014. Is resveratrol effective in protecting stallion cooled semen? J Equine Vet Sci, 34:1307-1312.

Giaretta E, Estrada E, Bucci D, Spinaci M, Rodríguez-Gil JE, Yeste M. 2015. Combining reduced glutathione and ascorbic acid has supplementary beneficial effects on boar sperm cryotolerance. Theriogenology, 83:399-407.

Giaretta E, Munerato M, Yeste M, Galeati G, Spinaci M, Tamanini C, Mari G, Bucci D. 2017. Implementing an open-access CASA software for the assessment of stallion sperm motility: Relationship with other sperm quality parameters. Anim Reprod Sci, 176:11-19.

Gibb Z, Lambourne SR, Aitken RJ. 2014. The Paradoxical Relationship Between Stallion Fertility and Oxidative Stress. Biol Reprod, 91:1-10.

Gibb Z, Lambourne SR, Quadrelli J, Smith ND, Aitken RJ. 2015. L-Carnitine and pyruvate are prosurvival factors during the storage of stallion spermatozoa at room temperature. Biol Reprod, 93:104.

Gibb Z, Aitken RJ. 2016. The impact of sperm metabolism during in vitro storage: the stallion as a model. BioMed Reseach Int, 2016:8p.

Glogowski J, Danforth DR, Ciereszko A. 2002. Inhibition of alkaline phosphatase activity of boar semen by pentoxifylline, caffeine, and theophylline. J Androl, 23:783-792.

Gonzalez-Fernandez L, Macias-Garcia B, Velez IC, Varner DD, Hinrichs K. 2012. Calcium-calmodulin and pH regulate protein tyrosine phosphorylation in stallion sperm. Reproduction, 144:411-422.

González-Fernández L, Macías-García B, Loux SC, Varner DD, Hinrichs K. 2013. Focal adhesion kinases and calcium/calmodulin-dependent protein kinases regulate protein tyrosine phosphorylation in stallion sperm. Biol Reprod, 88:1-12.

Grasa P, Colas C, Gallego M, Monteagudo L, Muiño-Blanco T, Cebrián-Pérez JA. 2009. Changes in content and localization of proteins phosphorylated at tyrosine, serine and threonine residues during ram sperm capacitation and acrosome reaction. Reproduction, 137:655-667.

Gravance CG, Garner D, Baumber J, Ball B. 2000. Assessment of equine sperm mitochondrial function using JC-1. Theriogenology, 53:1691-1703.

Green CE, Watson PF. 2001. Comparison of the capacitation-like state of cooled boar spermatozoa with true capacitation. Reproduction, 122:889-898.

Gürler H, Malama E, Heppelmann M, Calisici O, Leiding C, Kastelic JP, Bollwein H. 2015. Effects of cryopreservation on sperm viability, synthesis of reactive oxygen species, and DNA damage of bovine sperm. Theriogenology, 86:562-571.

Guthrie HD, Welch GR. 2007. Use of fluorescence-activated flow cytometry to determine membrane lipid peroxidation during hypothermic liquid storage and freeze-thawing of viable boar sperm loaded with 4, 4-

difluoro-5-(4-phenyl-1,3-butadienyl)-4-bora-3a,4a-diaza- s-indacene-3-undecano. J Anim Sci, 85:1402-1411.

Guthrie HD, Welch GR, Long JA. 2008. Mitochondrial function and reactive oxygen species action in relation to boar motility. Theriogenology, 70:1209-1215.

Harayama H, Sasaki K, Miyake M. 2004. A unique mechanism for cyclic adenosine 3',5'-monophosphate-induced increase of 32-kDatyrosine-phosphorylated protein in boar spermatozoa. Mol Reprod Dev, 69:194-204.

Hoogewijs MK, De Vliegher SP, Govaere JL, De Schauwer C, De Kruif A, Van Soom A. 2012. Influence of counting chamber type on CASA outcomes of equine semen analysis. Equine Vet J, 44:542-549.

Hossain MS, Johannisson A, Wallgren M, Nagy S, Siqueira AP, Rodriguez-Martinez H. 2011. Flow cytometry for the assessment of animal sperm integrity and functionality: state of the art. Asian J Androl, 13:406-419.

Hurtado De Llera A, Martin-Hidalgo D, Rodriguez-Gil JE, Gil MC, Garcia-Marin LJ, Bragado MJ. 2013. AMP-activated kinase, AMPK, is involved in the maintenance of plasma membrane organization in boar spermatozoa. Biochim. Biophys. Acta - Biomembr, 1828:2143-2151.

Jones R, James PS, Oxley D, Coadwell J, Suzuki-Toyota F, Howes EA. 2008. The equatorial subsegment in mammalian spermatozoa is enriched in tyrosine phosphorylated proteins. Biol. Reprod, 79:421-431.

Kareskoski M, Sankari S, Johannisson A, Kindahl H, Andersson M, Katila T. 2011. The association of the presence of seminal plasma and its components with sperm longevity in fractionated stallion ejaculates. Reprod Domest Anim, 46:1073-1081.

Kim S, Lee YJ, Kim YJ. 2011. Changes in sperm membrane and ROS following cryopreservation of liquid boar semen stored at 15°C. Anim Reprod Sci, 124:118-124.

Koppers AJ,De Iuliis GN, Finnie JM, McLaughlin EA, Aitken RJ. 2008. Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J Clin Endocrinol, Metab, 93:3199-3207.

Krisfalusi M, Miki K, Magyar PL, O'Brien DA. 2006. Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol Reprod, 75:270-278.

Kumaresan A, Siqueira AP, Hossain MS, Bergqvist AS. 2011. Cryopreservation-induced alterations in protein tyrosine phosphorylation of spermatozoa from different portions of the boar ejaculate. Cryobiology, 63:137-144.

Leahy T, Gadella BM. 2011. Capacitation and capacitation-like sperm surface changes induced by handling boar semen. Reprod Domest Anim, 46:7-13.

Lee JA, Spidlen J, Boyce K, Cai J, Crosbie N, Dalphin M, Furlong J, Gasparetto M, Goldberg M, Goralczyk EM, Hyun B, Jansen K, Kollmann T, Kong M, Leif R, McWeeney S, Moloshok TD, Moore W, Nolan G, Nolan J, Nikolich-Zugich J, Parrish D, Purcell B, Qian Y, Selvaraj B, Smith C, Tchuvatkina O, Wertheimer A, Wilkinson P, Wilson C, Wood J, Zigon R, International Society for Advancement of Cytometry Data Standards Task Force, Scheuermann RH, Brinkman RR. 2009. MIFlowCyt: the minimum information about a flow cytometry experiment. Cytometry, 73:926-930.

Love CC. 2011. Relationship between sperm motility, morphology and the fertility of stallions. Theriogenology, 76:547-557.

Maccarrone M, Barboni B, Paradisi A, Bernabò N, Gasperi V, Pistilli MG, Fezza F, Lucidi P, Mattioli M. 2005. Characterization of the endocannabinoid system in boar spermatozoa and implications for sperm capacitation and acrosome reaction. J Cell Sci, 118:4393-4404.

Mari G, Rizzato G, Merlo B, Iacono E, Bucci D, Seren E, Tamanini C, Galeati G, Spinaci M. 2010. Quality and fertilizing ability in vivo of sex-sorted stallion spermatozoa. Reprod Domest Anim, 45:331-335.

Marin S, Chiang K, Bassilian S, Lee W-NP, Boros LG, Fernández-Novell JM, Centelles JJ, Medrano A, Rodriguez-Gil JE, Cascante M. 2003. Metabolic strategy of boar spermatozoa revealed by a metabolomic characterization. FEBS Lett, 554:342-346.

Martìnez-Pastor F, Mata-Campuzano M, Alvarez-Rodrìguez M, Alvarez M, Anel L, de Paz P. 2010. Probes and techniques for sperm evaluation by flow cytometry. Reprod Domest Anim, 45:67-78.

Martínez-Pastor F, Tizado EJ, Garde JJ, Anel L, de Paz P. 2011. Statistical series: Opportunities and challenges of sperm motility subpopulation analysis. Theriogenology, 75:783-795.

Mattioli M, Barboni B, Lucidi P, Seren E. 1996. Identification of capacitation in boar spermatozoa by chlortetracycline staining. Theriogenology, 45:373-381.

Maxwell WM, Johnson LA. 1997. Chlortetracycline analysis of boar spermatozoa after incubation, flow cytometric sorting, cooling, or cryopreservation. Mol Reprod Dev, 46:408-418.

McPartlin LA, Littell J, Mark E, Nelson JL, Travis AJ, Bedford-Guaus SJ. 2008. A defined medium supports changes consistent with capacitation in stallion sperm, as evidenced by increases in protein tyrosine phosphorylation and high rates of acrosomal exocytosis. Theriogenology, 69:639-650.

Medrano A, Peña A, Rigau T, Rodrìguez-Gil JE. 2005. Variations in the proportion of glycolytic/non-glycolytic energy substrates modulate sperm membrane integrity and function in diluted boar samples stored at 15-17 degrees C. Reprod Domest Anim, 40:448-553.

Medrano A, Fernández-Novell JM, Ramió L, Alvarez J, Goldberg E, Montserrat Rivera M, Guinovart JJ, Rigau T, Rodríguez-Gil JE. 2006. Utilization of citrate and lactate through a lactate dehydrogenase and ATP-regulated pathway in boar spermatozoa. Mol Reprod Dev, 73:369-378.

Morrell JM. 2006. Update on semen technologies for animal breeding. Reprod Domest Anim, 41:63-67.

Mortimer ST. 2000. CASA--practical aspects. J Androl, 21:515-524.

 

Mugnier S, Dell'Aquila ME, Pelaez J, Douet C, Ambruosi B, De Santis T, Lacalandra GM, Lebos C, Sizaret PY, Delaleu B, Monget P, Mermillod P, Magistrini M, Meyers SA, Goudet G. 2009. New insights into the mechanisms of fertilization: comparison of the fertilization steps, composition, and structure of the zona pellucida between horses and pigs. Biol Reprod, 81:856-870.

Mukai C, Okuno, M. 2004. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod, 71:540-547.

Ortega Ferrusola C, González Fernández L, Morrell JM, Salazar Sandoval C, Macías García B, Rodríguez-Martinez H, Tapia JA, Peña FJ. 2009. Lipid peroxidation, assessed with BODIPY-C 11, increases after cryopreservation of stallion spermatozoa, is stallion-dependent and is related to apoptotic-like changes. Reproduction, 138:55-63.

Peña FJ, Plaza Davila M, Ball BA, Squires EL, Martin Muñoz P, Ortega Ferrusola C, Balao da Silva C. 2015. The Impact of Reproductive Technologies on Stallion Mitochondrial Function. Reprod Domest Anim, 50(4):529-537.

Pesch S, Bergmann M, Bostedt H. 2006. Determination of some enzymes and macro- and microelements in stallion seminal plasma and their correlations to semen quality. Theriogenology, 66:307-313.

Petrunkina AM, Harrison RAP. 2010. Systematic misestimation of cell subpopulations by flow cytometry: A mathematical analysis. Theriogenology, 73:839-847.

Petrunkina AM, Waberski D, Bollwein H, Sieme H. 2010. Identifying non-sperm particles during flow cytometric physiological assessment: a simple approach. Theriogenology, 73:995-1000.

Piehler E, Petrunkina AM, Ekhlasi-Hundrieser M, Töpfer-Petersen E. 2006. Dynamic quantification of the tyrosine phosphorylation of the sperm surface proteins during capacitation. Cytometry A, 69:1062-1070.

Pinart E, Yeste M, Bonet S. 2015. Acrosin activity is a good predictor of boar sperm freezability. Theriogenology, 83:1525-1533.

Plaza Dávila M, Bucci D, Galeati G, Peña F, Mari G, Giaretta E, Tamanini C, Spinaci M. 2015. Epigallocatechin-3-Gallate (EGCG) reduces rotenone effect on stallion sperm-Zona Pellucida Heterologous binding. Reprod Domest Anim, 50:1011-1016.

Quintero-Moreno A, Rigau T, Rodríguez-Gil JE. 2004. Regression analyses and motile sperm subpopulation structure study as improving tools in boar semen quality analysis. Theriogenology, 61:673-690.

Ramió-Lluch L, Fernández-Novell JM, Peña A, Ramírez A, Concha II, Rodríguez-Gil JE. 2011a. In vitro capacitation and further in vitro progesterone-induced acrosome exocytosis are linkedto specific changes in the expression and acrosome location of protein phosphorylation in serineresidues of boar spermatozoa. Reprod Domest Anim, 47:766-776. 

Ramió-Lluch L, Fernández-Novell JM, Peña A, Colás C, Cebrián-Pérez JA, Muiño-Blanco T, Ramírez A, Concha II, Rigau T, Rodríguez-Gil JE. 2011b. In vitro capacitation and acrosome reaction are concomitant with specific changes in mitochondrial activity in boar sperm: evidence for a nucleated mitochondrial activation and for the existence of a capacitation-sensitive subpopulational structure. Reprod Domest Anim, 46:664-673.

Ramió-Lluch L, Fernández-Novell JM, Peña A, Bucci D, Rigau T, Rodríguez-Gil JE. 2012. In vitro capacitation and subsequent acrosome reaction are related to changes in the expression and location of midpiece actin and mitofusin-2 in boar spermatozoa. Theriogenology, 77:979-988.

Ramió-Lluch L, Yeste M, Fernández-Novell JM, Estrada E, Rocha L, Cebrián-Pérez JA, Muiño-Blanco T, Concha II, Ramírez A, Rodríguez-Gil JE. 2014. Oligomycin A-induced inhibition of mitochondrial ATP-synthase activity suppresses boar sperm motility and in vitro capacitation achievement without modifying overall sperm energy levels. Reprod Fertil Dev, 26:883-897.

Rathi R, Colenbrander B, Bevers MM, Gadella BM. 2001. Evaluation of in vitro capacitation of stallion spermatozoa. Biol Reprod, 65:462-470.

Rigau T, Farré M, Ballester J, Mogas T, Peña A. 2001. Effects of glucose and fructose on motility patterns of dog spermatozoa from fresh ejaculates. Theriogenology, 56:601-615.

Rigau T, Rivera M, Palomo MJ, Fernández-Novell JM, Mogas T, Ballester J, Peña  a Otaegui PJ, Guinovart JJ, Rodríguez-Gil JE. 2002. Differential effects of glucose and fructose on hexose metabolism in dog spermatozoa. Reproduction, 123:579-591.

Rijsselaere T, Van Soom A, Tanghe S, Coryn M, Maes D, De Kruif A. 2005. New techniques for the assessment of canine semen quality: A review. Theriogenology, 64:706-719.

Robles V, Martínez-Pastor F. 2013. Flow cytometric methods for sperm assessment. Methods Mol Biol, 927:175-186.

Rodriguez-Gil J. 2006. Mammalian sperm energy resources management and survival during conservation in refrigeration. Reprod Domest Anim, 41:11-20.

Rodríguez-Gil JE, Bonet S. 2016. Current knowledge on boar sperm metabolism: Comparison with other mammalian species. Theriogenology, 85:4-11.

Sancho S, Casas I, Ekwall H, Saravia F, Rodriguez-Martinez H, Rodriguez-Gil J.E, Flores E, Pinart E, Briz M, Garcia-Gil N, Bassols J, Pruneda A, Bussalleu E, Yeste M, Bonet S. 2007. Effects of cryopreservation on semen quality and the expression of sperm membrane hexose transporters in the spermatozoa of Iberian pigs. Reproduction, 134:111-121.

Satorre MM, Breininger E, Beconi MT, Beorlegui NB. 2009. Protein tyrosine phosphorylation under capacitating conditions in porcine fresh spermatozoa and sperm cryopreserved with and without alpha tocopherol. Andrologia, 41:184-192.

Schmidt H, Kamp G. 2004. Induced hyperactivity in boar spermatozoa and its evaluation by computer-assisted sperm analysis. Reproduction, 128:171-179. Silva PFN, Gadella BM. 2006. Detection of damage in

mammalian sperm cells. Theriogenology, 65:958-978.

Sinowatz F, Wessa E, Neumüller C, Palma G. 2003. On the species specificity of sperm binding and sperm penetration of the zona pellucida. Reprod Domest Anim, 38:141-146.

Spinaci M, De Ambrogi M, Volpe S, Galeati G, Tamanini C, Seren E. 2005a. Effect of staining and sorting on boar sperm membrane integrity, mitochondrial activity and in vitro blastocyst development. Theriogenology, 64:191-201.

Spinaci M, Volpe S, Bernardini C, De Ambrogi M, Tamanini C, Seren E, Galeati G. 2005b. Immunolocalization of heat shock protein 70 (Hsp 70) in boar spermatozoa and its role during fertilization. Mol Reprod Dev, 72:534-541.

Spinaci M, Volpe S, Bernardini C, de Ambrogi M, Tamanini C, Seren E, Galeati G. 2006. Sperm sorting procedure induces a redistribution of Hsp70 but not Hsp60 and Hsp90 in boar spermatozoa. J Androl, 27:899-907.

Spinaci M, Bucci D, Chlapanidas T, Vallorani C, Perteghella S, Communod R, Vigo D, Tamanini C, Galeati G, Faustini M, Torre ML. 2013. Boar sperm changes after sorting and encapsulation in barium alginate membranes. Theriogenology, 80:526-532.

Spinaci M, Bucci D, Mazzoni M, Giaretta E, Bernardini C, Vallorani C, Tamanini C, Clavenzani P, Galeati G. 2014. Expression of α-gustducin and α-transducin, G proteins coupled with taste receptors, in boar sperm. Theriogenology, 82:144-151.

Spinaci M, Bucci D, Gadani B, Porcu E, Tamanini C, Galeati G. 2017. Pig sperm preincubation and gamete coincubation with glutamate enhance sperm-oocyte binding and in vitro fertilization. Theriogenology, 95:149-153.

Spinaci M, Muccilli V, Bucci D, Cardullo N, Gadani B, Tringali C, Tamanini C, Galeati G. 2018. Biological effects of polyphenol-rich extract and fractions from an oenological oak-derived tannin on in vitro swine sperm capacitation and fertilizing ability. Theriogenology, 108:284-290.

Storey BT. 2008. Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol, 52:427-437.

Suarez SS. 1996. Hyperactivated Motility in Sperm. J Androl, 17:331-335.

Suarez SS, Pacey AA. 2006. Sperm transport in the female reproductive tract. Hum Reprod Update, 12:23-37.

Suarez SS. 2008. Control of hyperactivation in sperm. Hum Reprod Update, 14:647-657.

Terrell KA, Wildt DE, Anthony NM, Bavister BD, Leibo SP, Penfold LM, Marker LL, Crosier AE. 2011. Glycolytic enzyme activity is essential for domestic cat (Felis catus) and cheetah (Acinonyx jubatus) sperm motility and viability in a sugar-free medium. Biol Reprod, 84:1198-1206.

Tsai P-S, Garcia-Gi, N, van Haeften T, Gadella BM. 2010. How pig sperm prepares to fertilize: stable acrosome docking to the plasma membrane. PLoS One, 5:e11204.

Turner RMO, McDonnell SM. 2003. Alkaline phosphatase in stallion semen: characterization and clinical applications. Theriogenology, 60:1-10.

Urner F, Sakkas D. 2005. Involvement of the pentose phosphate pathway and redox regulation in fertilization in the mouse. Mol Reprod Dev, 70:494-503.

Vallorani C, Spinaci M, Bucci D, Tamanini C, Galeati, G. 2010. Effects of antioxidants on boar spermatozoa during sorting and storage. Anim Reprod Sci, 122:58-65.

Varner DD, Gibb Z, Aitken RJ. 2015. Stallion fertility: A focus on the spermatozoon. Equine Vet J, 47:16-24.

Wilson-Leedy JG, Ingermann RL. 2007. Development of a novel CASA system based on open source software for characterization of zebrafish sperm motility parameters. Theriogenology, 67:661-672.

Yeste M, Estrada E, Rivera Del Álamo MM, Bonet S, Rigau T, Rodríguez-Gil JE. 2014. The increase in phosphorylation levels of serine residues of protein HSP70 during holding time at 17°C is concomitant with a higher cryotolerance of boar spermatozoa. PLoS One, 9:e90887. 

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