Abstract
The aim of this study was to examine the biochemical components and the parameters of antioxidant protection in the seminal plasma (SP) of boars, as well as their relationship with semen quality parameters. Thirty-six boars were included in the study, whose ejaculates were divided into two groups: Group I (good quality semen, > 70% progressively motile sperm, < 20% spermatozoa with abnormal morphology, n = 16), and Group II (poor quality semen, < 70% progressively motile sperm, > 20% spermatozoa with abnormal morphology, n = 20). Significantly higher concentrations of ionized calcium (iCa), total cholesterol (TC), lactate-dehydrogenase (LDH) activity, as well as significantly higher values of antioxidant protection parameters: thiol groups (-SH), paraoxonase 1 (PON1), and total antioxidant capacity (TAC) ) were found in the good quality semen, while higher phosphorus (P) concentrations and increased alkaline-phosphatase (ALP) activity were found in the semen of poor quality. A negative correlation of total and progressive sperm motility with P and ALP was found in all examined semen samples, while a positive correlation was found with PON1 and TAC. The percentage of fast sperm cells positively correlated with iCa, chlorine (Cl), lactate, LDH and TAC, while a negative correlation was found with P, magnesium (Mg) and the enzyme creatine-kinase (CK). The percentage of immobile sperm positively correlated with P and ALP, and negatively correlated with TC, CK, PON1 and TAC. Elevated values of PON1 and TAC in SP and a positive correlation with sperm motility indicate the possible use of these parameters as sensitive biomarkers of boar semen quality. To the best of our knowledge there are no published data on association between PON1 activity and boar semen quality.
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The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Aitken RJ, Buckingham DW, Carreras A, Stewart Irvine D (1996) Superoxide dismutase in human sperm suspensions: relationship with cellular composition, oxidative stress, and sperm function. Free Radical Bio Med 21:495–504. https://doi.org/10.1016/0891-5849(96)00119-0
Alapati SV, Mihas AA (1999) When to suspect ischemic colitis: why is this condition so often missed or misdiagnosed? Postgrad Med 105:177–187. https://doi.org/10.3810/pgm.1999.04.684
Aljabari B, Calogero AE, Perdichizzi A, Vicari E, Karaki R, Lahloub T, Zatari R, El-Abed K, Nicoletti F, Miller EJ, Pavlov VA, Al-Abed Y (2007) Imbalance in seminal fluid MIF indicates male infertility. Mol Med 13:199–202. https://doi.org/10.2119/2006-00114
Am-in N, Kirkwood RN, Techakumphu M, Tantasuparuk W (2011) Lipid profiles of sperm and seminal plasma from boars having normal or low sperm motility. Theriogenology 75:897–903. https://doi.org/10.1016/j.theriogenology.2010.10.032
Asadpour R (2012) Relationship between mineral composition of seminal plasma and semen quality in various ram breeds. Acta Sci Vet 40:1–8 Online ISSN 1679–9216
Banihani SA, Abu-Alhayjaa RF (2016) The activity of seminal creatine kinase is increased in the presence of pentoxifylline. Andrologia 48:603–604. https://doi.org/10.1111/and.12486
Barranco I, Tvarijonaviciute A, Perez-Patiño C, Parrilla I, Ceron JJ, Martinez EA, Rodriguez-Martinez H, Roca J (2015) High total antioxidant capacity of the porcine seminal plasma (SP-TAC) relates to sperm survival and fertility. Sci Rep 5:18538. https://doi.org/10.1038/srep18538
Barranco I, Padilla L, Tvarijonaviciute A, Parrilla I, Martínez EA, Rodriguez-Martinez H, Yeste M, Roca J (2019) Levels of activity of superoxide dismutase in seminal plasma do not predict fertility of pig AI-semen doses. Theriogenology 140:18–24. https://doi.org/10.1016/j.theriogenology.2019.08.010
Barranco I, Rubio CP, Tvarijonaviciute A, Rodriguez-Martinez H, Roca J (2021) Measurement of oxidative stress index in seminal plasma can predict in vivo fertility of liquid-stored porcine artificial insemination semen doses. Antioxidants 140:18–24. https://doi.org/10.3390/antiox10081203
Bathgate R (2011) Antioxidant mechanisms and their benefit on post-thaw boar sperm quality. Reprod Domest Anim 46:23–25. https://doi.org/10.1111/j.1439-0531.2011.01826.x
Betarelli RP, Rocco M, Yeste M, Fernández-Novell JM, Placci A, Azevedo Pereira B, Castillo-Martín M, Estrada E, Peña A, Zangeronimo MG, Rodríguez-Gil JE (2018) The achievement of boar sperm in vitro capacitation is related to an increase of disrupted disulphide bonds and intracellular reactive oxygen species levels. Andrology 6:781–797. https://doi.org/10.1111/andr.12514
Brezezinska-Slebodzinska E, Slebodzinski AB, Pietras B, Wieczorek G (1995) Antioxidant effect of vitamin E and glutathione on lipid peroxidation in boar semen plasma. Biol Trace Elem Res 47:69–74. https://doi.org/10.1007/BF02790102
Caballero I, Vazquez JM, García EM, Parrilla I, Roca J, Calvete JJ, Martinez EA (2008) Major proteins of boar seminal plasma as a tool for biotechnological preservation of spermatozoa. Theriogenology 70:1352–1355. https://doi.org/10.2164/jandrol.109.007583
Cannarella R, Crafa A, Barbagallo F, Mongioì LM, Condorelli RA, Aversa A, Calogero AE, La Vignera S (2020) Seminal plasma proteomic biomarkers of oxidative stress. Int J Mol Sci 21:2–13. https://doi.org/10.3390/ijms21239113
Cerolini S, Maldjian A, Surai P, Noble R (2000) Viability, susceptibility to peroxidation and fatty acid composition of boar semen during liquid storage. Anim Reprod Sci 58:99–111. https://doi.org/10.1016/s0378-4320(99)00035-4
Chaves BR, Pinoti Pavaneli AP, Blanco-Prieto O, Pinart E, Bonet S, Zangeronimo MG, Rodríguez-Gil JE, Yeste M (2021) Exogenous albumin is crucial for pig sperm to elicit in vitro capacitation whereas bicarbonate only modulates its efficiency. Biology 10(11):1105. https://doi.org/10.3390/biology10111105
Clements KM, Shipley CF, Coleman DA, Ehrhart EJ, Haschek WM, Clark SG (2010) Azoospermia in an 8-month-old boar due to bilateral obstruction at the testis/epididymis interface. Can Vet J 51:1130–1134
Collodel G, Nerucci F, Signorini C, Iacoponi F, Moretti E (2019) Associations between biochemical components of human semen with seminal conditions. Syst Biol Reprod Med 65:155–163. https://doi.org/10.1080/19396368.2018.1548668
Dott HM, Foster GC (1972) A technique for studying the morphology of mammalian spermatozoa which are eosinophilic in a differential “life-dead” stain. J Reprod Fertil 29:443–445
Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A (2006) Biomarkers of oxidative damge in human disease. Clin Chem 52:601–623. https://doi.org/10.1373/clinchem.2005.061408
Dar MR, Singh M, Sharma R, Thakur S, Sheikh AA, Bhat SA (2018) Bovine fertility as regulated by sperm binding proteins: a review. Asian J Anim Vet Adv 13:6–13. https://doi.org/10.3923/ajava.2018.6.13
Diaconescu C, Matei M, Talpu G, Tapaloaga P (2014) Comparative physicochemical and biochemical characterization of bull and boar semen. Anim Sci J 57:141–145 ISSN-L
Dyck MK, Foxcroft GR, Novak S, Ruiz-Sanchez A, Patterson J, Dixon WT (2011) Biological markers of boar fertility. Reprod Domest Anim 46:55–58. https://doi.org/10.1111/j.1439-0531.2011.01837.x
Eghbali M, Alavi SS, Asri RS, Khadem AM (2010) Calcium, magnesium and total antioxidant capacity (TAC) in seminal plasma of water buffalo (Bubalus Bubalis) bulls and their relationships with semen characteristics. Vet Res Forum 1:12–20
Ellman GK (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77. https://doi.org/10.1016/0003-9861(59)90090-6
Evans JD (1996) Straightforward statistics for the behavioral sciences. Brooks/Cole Publishing, Pacific Grove, CA
Fu J, Li Y, Wang L, Zhen L, Yang Q, Li P, Li X (2017) Bovine serum albumin and skim-milk improve boar sperm motility by enhancing energy metabolism and protein modifications during liquid storage at 17 ºC. Theriogenology 102:87–97. https://doi.org/10.1016/j.theriogenology.2017.07.020
Funahashi H, Sano T (2005) Select antioxidants improve the function of extended boar semen stored at 10 degrees C. Theriogenology 63:1605–1616. https://doi.org/10.1016/j.theriogenology.2004.06.016
Gadea J (2003) Semen extenders used in artificial insemination of swine. Span Agric Res 1:17–27. https://doi.org/10.5424/sjar/2003012-17
González-Cadavid V, Martins JA, Moreno FB, Andrade TS, Santos AC, Monteiro-Moreira AC, Moreira RA, Moura AA (2014) Seminal plasma proteins of adult boars and correlations with sperm parameters. Theriogenology 82:697–707. https://doi.org/10.1016/j.theriogenology.2014.05.024
Gosalvez J, Tvrda E, Agarwal A (2017) Free radical and superoxide reactivity detection in semen quality assessment: past, present, and future. J Assist Reprod Genet 34:697–707. https://doi.org/10.1007/s10815-017-0912-8
Gugliucci A, Caccavello R, Kotani K, Sakane N, Kimura S (2013) Enzymatic assessment of paraoxonase 1 activity on HDL subclasses: a practical zymogram method to assess HDL function. Clin Chim Acta 415:162–168. https://doi.org/10.1016/j.cca.2012.10.044
Guo H, Chang Z, Zhang Z, Zhao Y, Jiang X, Yu H, Zhang Y, Zhao R, He B (2019) Extracellular ATPs produced in seminal plasma exosomes regulate boar sperm motility and mitochondrial metabolism. Theriogenology 139:113–120. https://doi.org/10.1016/j.theriogenology.2019.08.003
Hernández M, Roca J, Calvete JJ, Sanz L, Muiño-Blanco T, Cebrián-Pérez JA, Vázquez JM, Martínez EA (2007) Cryosurvival and in vitro fertilizing capacity postthaw is improved when boar spermatozoa are frozen in the presence of seminal plasma from good freezer boars. J Androl 28:689–697. https://doi.org/10.2164/jandrol.107.002725
Holt WV, Harrison RA (2002) Bicarbonate stimulation of boar sperm motility via a protein kinase A-dependent pathway: between-cell and between-ejaculate differences are not due to deficiencies in protein kinase A activation. J Androl 23:557–565 PMID: 12065464
Johnson LA, Weitz KF, Fiser P, Maxwell WMC (2000) Storage of boar semen. Anim Reprod Sci 62:143–172. https://doi.org/10.1016/s0378-4320(00)00157-3
Juyena NS, Stelletta C (2012) Seminal plasma and essential attribute to spermatozoa. J Androl 33:536–551. https://doi.org/10.2164/jandrol.110.012583
Kasperczyk A, Dobrakowski M, Horak S, Zalejska-Fiolka J, Birkner E (2015) The influence of macro and trace elements on sperm quality. J Trace Elem Med Biol 30:153–159. https://doi.org/10.1016/j.jtemb.2014.12.007
Kong L, Cui X, Jin H, Wu J, Du H, Xiong T (2009) Mechanochemical synthesis of sodium borohydride by recycling sodium metaborate. Energy fuels 23:5049–5054. https://doi.org/10.1021/ef900619y
Kumosani TA, Elshal MF, Al-Jonaid AA, Abduljabar HS (2008) The influence of smoking on semen quality, seminal microelements and Ca2+- ATPase activity among infertile and fertile men. Clin Biochem 41:1199–1203
Li J, Barranco I, Tvarijonaviciute A, Molina MF, Martinez EA, Rodriguez-Martinez H, Parrilla I, Roca J (2018) Seminal plasma antioxidants are directly involved in boar sperm cryotolerance. Theriogenology 107:27–35. https://doi.org/10.1016/j.theriogenology.2017.10.035
López Rodríguez A, Rijsselaere T, Beek J, Vyt P, Van Soom A, Maes D (2013) Boar seminal plasma components and their relation with semen quality. Syst Biol Reprod Med 59:5–12. https://doi.org/10.3109/19396368.2012.725120
Luconi M, Francavilla F, Porazzi I, Macerola B, Forti G, Baldi E (2004) Human spermatozoa as a model for studying membrane receptors mediating rapid nongenomic effects of progesterone and estrogens. Steroids 69:553–559. https://doi.org/10.1016/j.steroids.2004.05.013
Massanyi P, Trandzik J, Nad P, Toman R, Skalick M, Kornekov B (2003) Seminal concentrations of trace elements in various animals and their correla- tions. Asian J Androl 5:101–104
Modi DN, Shah C, Puri CP (2007) Non-genomic membrane progesterone receptors on human spermatozoa. Soc Reprod Fertil Suppl 63:515–529 PMID: 17566296
Novak S, Ruiz Sánchez A, Dixon WT, Foxcroft GR, Dyck MK (2010) Seminal plasma proteins as potential markers of relative fertility in boars. J Androl 31:188–200. https://doi.org/10.2164/jandrol.109.007583
Ostojic SM, Stea TH, Engeset D (2022) Creatine as a promising component of paternal preconception diet. Nutrients 14:586. https://doi.org/10.3390/nu14030586
Owen DH, Katz DF (2005) A review of the physical and chemical properties of human semen and the formulation of a semen simulant. J Androl 26:459–469. https://doi.org/10.2164/jandrol.04104
Parks JE, Lynch DV (1992) Lipid composition and thermotropic phase behavior of boar, bull, stallion, and rooster sperm membranes. Cryobiology 29:255–266. https://doi.org/10.1016/0011-2240(92)90024-v
Parrilla I, Perez-Patiño C, Li J, Barranco I, Padilla L, Rodriguez-Martinez H, Martinez EA, Roca J (2019) Boar semen proteomics and sperm preservation. Theriogenology 137:23–29. https://doi.org/10.1016/j.theriogenology.2019.05.033
Pérez-Patiño C, Parrilla I, Li J, Barranco I, Martínez EA, Rodriguez-Martínez H, Roca J (2019) The proteome of pig spermatozoa is remodeled during ejaculation. Mol Cell Proteomics 18:41–50. https://doi.org/10.1074/mcp.ra118.000840
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. https://doi.org/10.1016/j.theriogenology.2005.11.015
Piomboni P, Stendardi A, Gambera L, Tatone C, Coppola L, De Leo V, Focarelli R (2012) Protein modification as oxidative stress marker in normal and pathological human seminal plasma. Redox Rep 17:227–232. https://doi.org/10.1179/1351000212y.0000000014
Pipan MZ, Mrkun J, Strajn BJ, Vrtač KP, Kos J, Pišlar A, Zrimšek P (2017) The influence of macro- and microelements in seminal plasma on diluted boar sperm quality. Acta Vet Scand 59(1):11. https://doi.org/10.1186/s13028-017-0279-y
Price PA, Toroian D, Chan WS (2009) Tissue-nonspecific alkaline phosphatase is required for the calcification of collagen in serum: a possible mechanism for biomineralization. J Biol Chem 284:4594–4604. https://doi.org/10.1074/jbc.m803205200
Prien SD, Lox CD, Messer RH, DeLeon FD (1990) Seminal concentssrations of total and ionized calcium from men with normal and decreased motility. Fertil Steril 54:171–172 PMID: 2358084
Radomil L, Pettitt MJ, Merkies KM, Hickey KD, Buhr MM (2011) Stress and dietary factors modify boar sperm for processing. Reprod Domest 2:39–44. https://doi.org/10.1111/j.1439-0531.2011.01865.x
Roca J, Broekhuijse ML, Parrilla I, Rodriguez-Martinez H, Martinez EA, Bolarin A (2015) Boar differences in artificial insemination outcomes: can they be minimized? Reprod Domest Anim 2:48–55. https://doi.org/10.1111/rda.12530
Roca J, Perez-Patiño C, Barranco I, Padilla LC, Martínez EA, Rodriguez-Martinez H, Parrilla I (2020) Proteomics in fresh and preserved pig semen: recent achievements and future challenges. Theriogenology 150:41–47. https://doi.org/10.1016/j.theriogenology.2020.01.066
Rocco M, Betarelli R, Placci A, Fernández-Novell JM, Spinaci M, Casao A, Muiño-Blanco T, Cebrián-Pérez JA, Peña A, Rigau T, Bonet S, Castillo-Martín M, Yeste M, Rodríguez-Gil JE (2018) Melatonin affects the motility and adhesiveness of in vitro capacitated boar spermatozoa via a mechanism that does not depend on intracellular ROS levels. Andrology 6:720–736. https://doi.org/10.1111/andr.12504
Rodríguez-Martínez H, Kvist U, Ernerudh J, Sanz L, Calvete JJ (2011) Seminal plasma proteins: what role do they play? Am J Reprod Immunol 66:11–22. https://doi.org/10.1111/j.1600-0897.2011.01033.x
Shipley CF (1999) Breeding soundness examination in the boar. Swine Health Prod 7:117–120
Sopková D, Andrejcakova Z, Vlckova R, Danisova O, Supuka P, Ondrasovicova S, Petrilla V (2015) Lactate dehydrogenase as a possible indicator of reproductive capacity of boars. Indian J Anim Sci 85:143–147. https://doi.org/10.1590/1984-3143-AR2020-0022
Stival C, Puga Molina Ldel C, Paudel B, Buffone MG, Visconti PE, Krapf D (2016) Sperm capacitation and acrosome reaction in mammalian sperm. Adv Anat Embryol Cell Biol 220:93–106. https://doi.org/10.1007/978-3-319-30567-7_5
Strzezek J, Fraser L, Hołody D, Wysocki P (1998) Biochemical properties and usefulness of boar semen for liquid preservation following atropine administration. Zentralbl Veterinarmed A 45:459–470. https://doi.org/10.1111/j.1439-0442.1998.tb00849.x
Szcześniak-Fabiańczyk B, Bochenek M, Smorag Z, Ryszka F (2003) Effect of antioxidants added to boar semen extender on the semen survival time and sperm chromatin structure. Reprod Biol 3:81–87 PMID: 14666145
Thapoing K, Boonprakob U, Crosby K, Cisneros-Zevallos L, Byrne HD (2006) Comparison of ABTS, DPPH, FRAP and ORAC assays for estimating antioxidant activity from guava fruit extracts. J Food Comp Anal 19:669–675. https://doi.org/10.1016/j.jfca.2006.01.003
Tsakmakidis IA, Lymberopoulos AG, Khalifa TA (2010) Relationship between sperm quality traits and field-fertility of porcine semen. J Vet Sci 11:151–154. https://doi.org/10.4142/jvs.2010.11.2.151
Visconti PE (2009) Understanding the molecular basis of sperm capacitation through kinase design. Proc Natl Acad Sci USA 106:667–668. https://doi.org/10.1073/pnas.0811895106
Wysocki P, Strzezek J (2006) Isolation and biochemical characteristics of a molecular form of epididymal acid phosphatase of boar seminal plasma. Theriogenology 66:2152–2159. https://doi.org/10.1016/j.theriogenology.2006.07.002
Yeste M, Fernández-Novell JM, Ramió-Lluch L, Estrada E, Rocha LG, Cebrián-Pérez JA, Muiño-Blanco T, Concha II, Ramírez A, Rodríguez-Gil JE (2015) Intracellular calcium movements of boar spermatozoa during ‘ in vitro’ capacitation and subsequent acrosome exocytosis follow a multiple-storage place, extracellular calcium-dependent model. Andrology 3:729–747. https://doi.org/10.1111/andr.12054
Žaja I, Samardžija M, Vince S, Majić-Balić I, Vilić M, Đuričić D, Milinković-Tur S (2016) Influence of boar breeds or hybrid genetic composition on semen quality and seminal plasma biochemical variables. Anim Reprod Sci 164:169–176. https://doi.org/10.1016/j.anireprosci.2015.11.027
Zhang XG, Yan GJ, Hong JY, Su ZZ, Yang GS, Li QW, Hu JH (2015) Effects of bovine serum albumin on boar sperm quality during liquid storage at 17 C. Reprod Domest Anim 50:263–269. https://doi.org/10.1111/rda.12481
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The study was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Contract number 451-03-68/2022-14/200143).
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Svetlana Nedić: Conceptualization, Methodology, Visualisation, Writing, Miloje Đurić: Methodology, Slobodanka Vakanjac: Conceptualization, Visualisation, Writing, Sveta Arsić: Methodology, Sreten Nedić: Methodology, Marko Samardžija: Visualisation, Sunčica Borozan: Conceptualization, Methodology, Visualisation, Writing. All authors approved the final version of this article.
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Nedić, S., Đurić, M., Vakanjac, S. et al. Relationship between biochemical parameters and paraoxonase 1 activity of boar seminal plasma and semen quality. Vet Res Commun 47, 1243–1253 (2023). https://doi.org/10.1007/s11259-022-10066-x
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DOI: https://doi.org/10.1007/s11259-022-10066-x