Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2022-0039
Animal Reproduction (AR)
ORIGINAL ARTICLE

Paraoxonase 1 activity in the sperm-rich portion of boar ejaculates is positively associated with sperm quality

Matheus Schardong Lucca; Karina Lemos Goularte; Monique Tomazele Rovani; Augusto Schneider; Bernardo Garziera Gasperin; Thomaz Lucia Júnior; Carlos Augusto Rigon Rossi

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Abstract

Associations of the activity of the paraoxonase 1 (PON1) enzyme with boar sperm quality still needs to be characterized, since boar ejaculates present distinct portions with differences in sperm concentration and quality. This study evaluated PON1 activity in the serum, in the distinct portions of boar ejaculates and estimated correlations with sperm quality parameters. Ejaculates and blood samples were collected from six boars for three weeks (two per week per boar; n = 36). Serum and post-spermatic portion PON1 activities were positively correlated (P = 0.01) but were both uncorrelated with the PON1 activity in the sperm-rich portion and in the whole ejaculate (P > 0.05). Differences in PON1 activity among boars were only observed in the sperm-rich portion of the ejaculate (P < 0.05). The PON1 activity in the serum and in the post-spermatic portion was generally negatively correlated with parameters of spermatozoa kinetics (P < 0.05). In the sperm-rich portion, PON1 activity was positively correlated with sperm concentration (P < 0.0001), curvilinear distance and velocity (both P < 0.05) and DNA integrity (P < 0.05), but negatively correlated with straightness and linearity (P < 0.05). Thus, boar ejaculates with increased PON1 activity in the sperm-rich portion may present increased concentration and spermatozoa with acceptable curvilinear velocity and distance and DNA integrity, which suggests that PON1 activity may be a biomarker for potential fertility.

Keywords

PON1, spermatozoa kinetics, membrane integrity, DNA integrity

References

Aitken R, De Iuliis G. On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod. 2010;16(1):3-13. http://dx.doi.org/10.1093/molehr/gap059. PMid:19648152.

Aşkar T, Büyükleblebici O. Paraoxonase: a new biochemical marker of oxidant-antioxidant status in atherosclerosis. In: Lushchak V, Semchyshyn H, editors. Oxidative stress: molecular mechanisms and biological effects. Croacia: InTech; 2012. p. 145-54.

Awda BJ, Mackenzie-Bell M, Buhr MM. Reactive oxygen species and boar sperm function. Biol Reprod. 2009;81(3):553-61. http://dx.doi.org/10.1095/biolreprod.109.076471. PMid:19357363.

Barranco I, Perez-Patiño C, Tvarijonaviciute A, Parrilla I, Vicente-Carrillo A, Alvarez-Rodriguez M, Ceron JJ, Martinez E, Rodriguez-Martinez H, Roca J. Active paraoxonase 1 is synthesised throughout the internal boar genital organs. Reproduction. 2017;154(3):237-43. http://dx.doi.org/10.1530/REP-17-0300. PMid:28611113.

Barranco I, Roca J, Tvarijonaviciute A, Rubér M, Vicente‐Carrillo A, Atikuzzaman M, Ceron JJ, Martinez EA, Rodriguez‐Martinez H. Measurement of activity and concentration of paraoxonase 1 (PON‐1) in seminal plasma and identification of PON‐2 in the sperm of boar ejaculates. Mol Reprod Dev. 2015a;82(1):58-65. http://dx.doi.org/10.1002/mrd.22444. PMid:25487823.

Barranco I, Tvarijonaviciute A, Perez-Patiño C, Alkmin DV, Ceron JJ, Martinez EA, Rodriguez‐Martinez H, Roca J. The activity of paraoxonase type 1 (PON‐1) in boar seminal plasma and its relationship with sperm quality, functionality, and in vivo fertility. Andrology. 2015b;3(2):315-20. http://dx.doi.org/10.1111/andr.309. PMid:25598515.

Broekhuijse M, Feitsma H, Gadella B. Field data analysis of boar semen quality. Reprod Domest Anim. 2011;46(Suppl. 2):59-63. http://dx.doi.org/10.1111/j.1439-0531.2011.01861.x. PMid:21884280.

Broekhuijse M, Feitsma H, Gadella B. Artificial insemination in pigs: predicting male fertility. Vet Q. 2012a;32(3-4):151-7. http://dx.doi.org/10.1080/01652176.2012.735126. PMid:23092203.

Broekhuijse M, Šoštarić E, Feitsma H, Gadella B. Application of computer-assisted semen analysis to explain variations in pig fertility. J Anim Sci. 2012b;90(3):779-89. http://dx.doi.org/10.2527/jas.2011-4311. PMid:22064743.

Browne RW, Koury ST, Marion S, Wilding G, Muti P, Trevisan M. Accuracy and biological variation of human serum paraoxonase 1 activity and polymorphism (Q192R) by kinetic enzyme assay. Clin Chem. 2007;53(2):310-7. http://dx.doi.org/10.1373/clinchem.2006.074559. PMid:17185369.

Brezezińska-Slebodzińska E, Slebodziński AB, Pietras B, Wieczorek G. Antioxidant effect of vitamin E and glutathione on lipid peroxidation in boar semen plasma. Biol Trace Elem Res. 1995;47(1-3):69-74. http://dx.doi.org/10.1007/BF02790102. PMid:7779577.

Centola G. Comparison of manual microscopic and computer-assisted methods for analysis of sperm count and motility. Arch Androl. 1996;36(1):1-7. http://dx.doi.org/10.3109/01485019608987878. PMid:8824662.

Cerolini S, Maldjian A, Surai P, Noble R. Viability, susceptibility to peroxidation and fatty acid composition of boar semen during liquid storage. Anim Reprod Sci. 2000;58(1):99-111. http://dx.doi.org/10.1016/S0378-4320(99)00035-4. PMid:10700648.

Corcini C, Varela A Jr, Pigozzo R, Rambo G, Goularte K, Calderam K, Leon P, Bongalhardo D, Lucia T Jr. Pre-freezing and post-thawing quality of boar sperm for distinct portions of the ejaculate and as a function of protein bands present in seminal plasma. Livest Sci. 2012;145(1-3):28-33. http://dx.doi.org/10.1016/j.livsci.2011.12.016.

Dyck M, Foxcroft G, Novak S, Ruiz‐Sanchez A, Patterson J, Dixon W. Biological markers of boar fertility. Reprod Domest Anim. 2011;46(Suppl. 2):55-8. http://dx.doi.org/10.1111/j.1439-0531.2011.01837.x. PMid:21884279.

Efrat M, Stein A, Pinkas H, Breitbart H, Unger R, Birk R. Paraoxonase 1 (PON1) attenuates sperm hyperactivity and spontaneous acrosome reaction. Andrology. 2019;7(1):24-30. http://dx.doi.org/10.1111/andr.12552. PMid:30225889.

Evenson D, Jost L, Marshall D, Zinaman M, Clegg E, Purvis K, De Angelis P, Claussen O. Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod. 1999;14(4):1039-49. http://dx.doi.org/10.1093/humrep/14.4.1039. PMid:10221239.

Ferré N, Camps J, Prats E, Vilella E, Paul A, Figuera L, Joven J. Serum paraoxonase activity: a new additional test for the improved evaluation of chronic liver damage. Clin Chem. 2002;48(2):261-8. http://dx.doi.org/10.1093/clinchem/48.2.261. PMid:11805006.

Ferreira C, Haas C, Goularte K, Rovani M, Cardoso F, Schneider A, Gasperin B, Lucia T Jr. Expression of paraoxonase types 1, 2 and 3 in reproductive tissues and activity of paraoxonase type 1 in the serum and seminal plasma of bulls. Andrologia. 2018;50(3):e12923. http://dx.doi.org/10.1111/and.12923. PMid:29143963.

Ferreira C, Sávio D, Guarise A, Flach M, Gastal G, Gonçalves A, Dellagostin O, Alonso R, Bianchi I, Corcini C, Lucia T. Contribution of boars to reproductive performance and paternity after homospermic and heterospermic artificial insemination. Reprod Fertil Dev. 2015;27(7):1012-9. http://dx.doi.org/10.1071/RD13418. PMid:25483612.

Garner DL, Thomas CA, Joerg HW, Dejarnette JM, Marshall CE. Fluorometric assessments of mitochondrial function and viability in cryopreserved bovine spermatozoa. Biol Reprod. 1997;57(6):1401-6. http://dx.doi.org/10.1095/biolreprod57.6.1401. PMid:9408246.

González-Marín C, Gosálvez J, Roy R. Types, causes, detection and repair of DNA fragmentation in animal and human sperm cells. Int J Mol Sci. 2012;13(12):14026-52. http://dx.doi.org/10.3390/ijms131114026. PMid:23203048.

Gulum M, Gumus K, Yeni E, Dogantekin E, Ciftci H, Akin Y, Savas M, Altunkol A. Blood and semen paraoxonase-arylesterase activities in normozoospermic and azoospermic men. Andrologia. 2017;49(9):e12752. http://dx.doi.org/10.1111/and.12752. PMid:28000956.

Guthrie H, Welch G. Effects of reactive oxygen species on sperm function. Theriogenology. 2012;78(8):1700-8. http://dx.doi.org/10.1016/j.theriogenology.2012.05.002. PMid:22704396.

Harrison R, Vickers SE. Use of fluorescent probes to assess membrane integrity in mammalian spermatozoa. J Reprod Fertil. 1990;88(1):343-52. http://dx.doi.org/10.1530/jrf.0.0880343. PMid:1690300.

Ji G, Gu A, Wang Y, Huang C, Hu F, Zhou Y, Song L, Wang X. Genetic variants in antioxidant genes are associated with sperm DNA damage and risk of male infertility in a Chinese population. Free Radic Biol Med. 2012;52(4):775-80. http://dx.doi.org/10.1016/j.freeradbiomed.2011.11.032. PMid:22206979.

Jung M, Rüdiger K, Schulze M. In vitro measures for assessing boar semen fertility. Reprod Domest Anim. 2015;50(Suppl. 2):20-4. http://dx.doi.org/10.1111/rda.12533. PMid:26174915.

Kawamoto A, Ohashi K, Kishikawa H, Zhu L-Q, Azuma C, Murata Y. Two-color fluorescence staining of lectin and anti-CD46 antibody to assess acrosomal status. Fertil Steril. 1999;71(3):497-501. http://dx.doi.org/10.1016/S0015-0282(98)00507-X. PMid:10065788.

Khan R, Laudadio V, Tufarelli V. Semen traits and seminal plasma biochemical parameters in white leghorn layer breeders. Reprod Domest Anim. 2012;47(2):190-5. http://dx.doi.org/10.1111/j.1439-0531.2011.01821.x. PMid:21645128.

Knox RV. Artificial insemination in pigs today. Theriogenology. 2016;85(1):83-93. http://dx.doi.org/10.1016/j.theriogenology.2015.07.009. PMid:26253434.

Li J, Barranco I, Tvarijonaviciute A, Molina MF, Martinez EA, Rodriguez-Martinez H, Parrilla I, Roca J. Seminal plasma antioxidants are directly involved in boar sperm cryotolerance. Theriogenology. 2018;107:27-35. http://dx.doi.org/10.1016/j.theriogenology.2017.10.035. PMid:29128698.

Mackness B, Durrington PN, Mackness MI. Human serum paraoxonase. General Pharmacology: The Vascular System. 1998;31(3):329-36. http://dx.doi.org/10.1016/S0306-3623(98)00028-7. PMid:9703197.

Ozer OF, Akbulut H, Guler EM, Caglar HG, Gevher F, Koktasoglu F, Selek S. Oxidative stress and phenotype frequencies of paraoxonase‐1 in teratozoospermia. Andrologia. 2019;51(8):e13299. http://dx.doi.org/10.1111/and.13299. PMid:31012132.

Peña FJ, Johannisson A, Wallgren M, Rodriguez Martinez H. Antioxidant supplementation of boar spermatozoa from different fractions of the ejaculate improves cryopreservation: changes in sperm membrane lipid architecture. Zygote. 2004;12(2):117-24. http://dx.doi.org/10.1017/S096719940400262X. PMid:15460106.

Peña FJ, Saravia F, Núñez-Martínez I, Johannisson A, Wallgren M, Rodriguez Martinez H. Do different portions of the boar ejaculate vary in their ability to sustain cryopreservation? Anim Reprod Sci. 2006;93(1-2):101-13. http://dx.doi.org/10.1016/j.anireprosci.2005.06.028. PMid:16084673.

Ponce-Ruiz N, Murillo-González FE, Rojas-García AE, Bernal Hernández YY, Mackness M, Ponce-Gallegos J, Barrón-Vivanco BS, Hernández-Ochoa I, González-Arias CA, Ortega Cervantes L, Cardoso-Saldaña G, Medina-Díaz IM. Phenotypes and concentration of PON1 in cardiovascular disease: the role of nutrient intake. Nutr Metab Cardiovasc Dis. 2020;30(1):40-8. http://dx.doi.org/10.1016/j.numecd.2019.08.013. PMid:31757567.

Précourt L-P, Amre D, Denis M-C, Lavoie J-C, Delvin E, Seidman E, Levy E. The three-gene paraoxonase family: physiologic roles, actions and regulation. Atherosclerosis. 2011;214(1):20-36. http://dx.doi.org/10.1016/j.atherosclerosis.2010.08.076. PMid:20934178.

Siqueira AP, Wallgren M, Hossain M, Johannisson A, Sanz L, Calvete J, Rodriguez-Martinez H. Quality of boar spermatozoa from the sperm-peak portion of the ejaculate after simplified freezing in MiniFlatpacks compared to the remaining spermatozoa of the sperm-rich fraction. Theriogenology. 2011;75(7):1175-84. http://dx.doi.org/10.1016/j.theriogenology.2010.11.024. PMid:21316750.

Statistix®. Statistix® 10 analytical software. Tallahassee, FL, USA; 2013.

Su T-W, Xue L, Ozcan A. High-throughput lensfree 3D tracking of human sperms reveals rare statistics of helical trajectories. Proc Natl Acad Sci USA. 2012;109(40):16018-22. http://dx.doi.org/10.1073/pnas.1212506109. PMid:22988076.

Verit FF, Verit A, Ciftci H, Erel O, Çelik H. Paraoxonase‐1 activity in subfertile men and relationship to sperm parameters. J Androl. 2009;30(2):183-9. http://dx.doi.org/10.2164/jandrol.108.004929. PMid:18930907.

Verstegen J, Iguer-Ouada M, Onclin K. Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology. 2002;57(1):149-79. http://dx.doi.org/10.1016/S0093-691X(01)00664-1. PMid:11775967.

Waberski D, Riesenbeck A, Schulze M, Weitze KF, Johnson L. Application of preserved boar semen for artificial insemination: past, present and future challenges. Theriogenology. 2019;137:2-7. http://dx.doi.org/10.1016/j.theriogenology.2019.05.030. PMid:31186127.
 


Submitted date:
03/22/2022

Accepted date:
08/03/2022

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