Antisperm antibodies and sperm function in bulls undergoing scrotal insulation

in Reproduction
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  • 1 Department of Large Animal Medicine, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA
  • 2 Department of Population Health, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USA

Correspondence should be addressed to M S Ferrer; Email: msferrer@uga.edu

(J H Bittar is now at Department of Large Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, Florida, USA)

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Bovine antisperm antibodies (ASAs) have been associated with teratospermia and asthenospermia. It was hypothesized here that scrotal insulation induces the formation of ASAs and deterioration of sperm function. Scrotal insulation bags were placed in 10 bulls for 8 days. Semen was collected on days −29, −22 and −2, twice weekly from days 5 to 54, and thereafter weekly until day 96 (day 0 = first day of scrotal insulation). On each collection day, scrotal circumference, sperm motility, morphology, membrane integrity, acrosome integrity, apoptosis, lipid peroxidation, mitochondrial membrane potential, ASA binding and DNA integrity were evaluated. The percentage of IgG- and IgA-bound sperm increased between days 12 and 96 (P < 0.0001), in association with poor motility (days 19–30, P < 0.005) and morphology (days 8–40, P < 0.0001). Mean scrotal circumference decreased between days 15 and 75 (P < 0.0001). There was also a deterioration in sperm membrane integrity (days 19–40, P < 0.0001), acrosome integrity (days 26–89, P < 0.0001), lipid peroxidation (days 5–12, P < 0.0001), and mitochondrial membrane potential (days 12–96, P = 0.001). In contrast, a decrease in apoptotic cells (days 37–83, P = 0.0002) and lipid peroxidation (days 19–96, P < 0.0001) was noticed. Most bulls recovered normospermia by day 96. However, the persistence of ASAs, acrosomal damage and dysfunctional mitochondria suggest a long term effect of scrotal insulation on sperm function and the homeostasis of the reproductive immune system.

 

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  • Aitken RJ & Baker MA 2013 Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development. Int ernational J ournal of Dev elopmental Biol ogy 57 265272. (https://doi.org/10.1387/ijdb.130146ja)

    • Search Google Scholar
    • Export Citation
  • Aitken RJ & Clarkson JS 1987 Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J ournal of Reprod uction and Fert ility 81 459469. (https://doi.org/10.1530/jrf.0.0810459)

    • Search Google Scholar
    • Export Citation
  • Aitken RJ, Wingate JK, De Iuliis GN & McLaughlin EA 2007 Analysis of lipid peroxidation in human spermatozoa using BODIPY C11. Mol ecular Human Reprod uction 13 203211. (https://doi.org/10.1093/molehr/gal119)

    • Search Google Scholar
    • Export Citation
  • Argov N, Sklan D, Zeron Y & Roth Z 2007 Association between seasonal changes in fatty-acid composition, expression of VLDL receptor and bovine sperm quality. Theriogenology 67 878885. (https://doi.org/10.1016/j.theriogenology.2006.10.018)

    • Search Google Scholar
    • Export Citation
  • Argov-Argaman N, Mahgrefthe K, Zeron Y & Roth Z 2013 Season-induced variation in lipid composition is associated with semen quality in Holstein bulls. Reproduction 145 479489. (https://doi.org/10.1530/REP-12-0498)

    • Search Google Scholar
    • Export Citation
  • Arteaga AA, Barth AD & Brito LFC 2005 Relationship between semen quality and pixel–intensity of testicular ultrasonograms after scrotal insulation in beef bulls. Theriogenology 64 408415. (https://doi.org/10.1016/j.theriogenology.2004.12.008)

    • Search Google Scholar
    • Export Citation
  • Barth A 2015 Testicular degeneration. In Bovine Reproduction, pp. 104108. Ed Hopper. Ames, Iowa: Wiley Blackwell.

  • Barth AD & Bowman PA 1994 The sequential appearance of sperm abnormalities after scrotal insulation or dexamethasone treatment in bulls. Can adian Vet erinary J ournal 35 93102.

    • Search Google Scholar
    • Export Citation
  • Boe‐Hansen GB, Rêgo JPA, Satake N, Venus B, Sadowski P, Nouwens A, Li Y & McGowan M 2020 Effects of increased scrotal temperature on semen quality and seminal plasma proteins in Brahman bulls. Mol ecular Reprod uction and Dev elopment 87 574597. (https://doi.org/10.1002/mrd.23328)

    • Search Google Scholar
    • Export Citation
  • Brito LFC, Silva AEDF, Barbosa RT, Unanian MM & Kastelic JP 2003 Effects of scrotal insulation on sperm production, semen quality, and testicular echotexture in Bos indicus and Bos indicus × Bos taurus bulls. Anim al Reprod uction Sci ence 79 115. (https://doi.org/10.1016/s0378-4320(03)00082-4)

    • Search Google Scholar
    • Export Citation
  • Duramayanthi D, Agarwal A & Ong C 2015 Causes, effects and molecular mechanisms of testicular heat stress. Reprod uctive Biomed icine Online 30 1427. (https://doi.org/10.1016/j.rbmo.2014.09.018)

    • Search Google Scholar
    • Export Citation
  • Evenson DP 2016 The Sperm chromatin Structure Assay (SCSA®) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility. Anim al Reprod uction Sci ence 169 5675. (https://doi.org/10.1016/j.anireprosci.2016.01.017)

    • Search Google Scholar
    • Export Citation
  • Fernandes CE, Dode MAN, Pereira D & Silva AEDF 2008 Effects of scrotal insulation in Nellore bulls (Bos taurus indicus) on seminal quality and its relationship with in vitro fertilizing ability. Theriogenology 70 15601568. (https://doi.org/10.1016/j.theriogenology.2008.07.005)

    • Search Google Scholar
    • Export Citation
  • Ferrer MS, Laflin S, Anderson DE, Miesner MD, Wilkerson MJ, George A, Miller LMJ, Larson R & Garcia Flores EO 2015 Prevalence of bovine sperm-bound antisperm antibodies and their association with semen quality. Theriogenology 84 94100. (https://doi.org/10.1016/j.theriogenology.2015.02.017)

    • Search Google Scholar
    • Export Citation
  • Ferrer MS, Anderson DE, Miller LMJ, George A, Miesner M & Wilkerson M 2016 Effect of bovine sperm-bound antisperm antibodies on oviductal binding index. Reprod uction in Dom estic Anim als 51 287293. (https://doi.org/10.1111/rda.12679)

    • Search Google Scholar
    • Export Citation
  • Ferrer MS, Klabnik-Bradford J, Anderson DE, Bullington AC, Palomares RA, Miller LMJ, Stawicki R & Miesner M 2017 Sperm-bound antisperm antibodies prevent capacitation of bovine spermatozoa. Theriogenology 89 5867. (https://doi.org/10.1016/j.theriogenology.2016.10.012)

    • Search Google Scholar
    • Export Citation
  • Fijak M, Iosub R, Schneider E, Linder M, Respondek K, Klug J & Meinhardt A 2005 Identification of immunodominant autoantigens in rat autoimmune orchitis. J ournal of Pathol ogy 207 127138. (https://doi.org/10.1002/path.1828)

    • Search Google Scholar
    • Export Citation
  • Flowers WL 2013 Triennial reproduction symposium: sperm characteristics that limit success of fertilization. J ournal of Anim al Sci ence 91 30223029. (https://doi.org/10.2527/jas.2012-5945)

    • Search Google Scholar
    • Export Citation
  • Freitas MJ, Vijayaraghavan S & Fardilha M 2017 Signaling mechanisms in mammalian sperm motility. Biol ogy of Reprod uction 96 212. (https://doi.org/10.1095/biolreprod.116.144337)

    • Search Google Scholar
    • Export Citation
  • Hedger MP 2011 Toll-like receptors and signalling in spermatogenesis and testicular responses to inflammation – a perspective. J ournal of Reprod uctive Immunol ogy 88 130141. (https://doi.org/10.1016/j.jri.2011.01.010)

    • Search Google Scholar
    • Export Citation
  • Hegazi AG & Ezzo O 1995 Serum auto antibodies in buffaloes and cattle naturally infected with IBRV and Brucella. Buffalo J ournal 3 3253 3 0.

    • Search Google Scholar
    • Export Citation
  • Hunter AG & Hafs HD 1964 Antigenicity and cross-reactions of bovine spermatozoa. J ournal of Reprod uction and Fertil ity 7 357365. (https://doi.org/10.1530/jrf.0.0070357)

    • Search Google Scholar
    • Export Citation
  • Kanter M, Aktas C & Erboga M 2013 Heat stress decreases testicular germ cell proliferation and increases apoptosis in short term: an immunohistochemical and ultrastructural study. Toxicology and Industrial Health 29 99113. (https://doi.org/10.1177/0748233711425082)

    • Search Google Scholar
    • Export Citation
  • Karabinus DS, Vogler CJ, Saacke RG & Evenson DP 1997 Chromatin structural changes in sperm after scrotal insulation of Holstein bulls. J ournal of Androl ogy 18 549555.

    • Search Google Scholar
    • Export Citation
  • Kastelic JP 2015 Thermoregulation of the testes. In Bovine Reproduction, pp. 2629. Ed Hopper R. Ames, Iowa: Wiley Blackwell.

  • Kaur S & Bansal MP 2015 Protective role of dietary-supplemented selenium and vitamin E in heat-induced apoptosis and oxidative stress in mice testes. Andrologia 47 11091119. (https://doi.org/10.1111/and.12390)

    • Search Google Scholar
    • Export Citation
  • Kim CA, Parrish JJ, Momont HW & Lunn DP 1999 Effects of experimentally generated bull antisperm antibodies on in vitro fertilization. Biol ogy of Reprod uction 60 128512 91. (https://doi.org/10.1095/biolreprod60.6.1285)

    • Search Google Scholar
    • Export Citation
  • Koziol JH & Armstrong CL 2018 Society for Theriogenology Manual for Breeding Soundness Examination of Bulls, 2nd ed.

  • Kuntareddi C, Kumaresan A, Saraf KK, Nag P, Paul N, Kurati SP, Selvaraju S, Jeyakumar S, Manimaran A & Ramesha KP 2020 Characterization of antisperm antibody binding patterns in relation to sperm phenotypic attributes and field fertility in dairy bulls. Theriogenology 141 161167. (https://doi.org/10.1016/j.theriogenology.2019.09.022)

    • Search Google Scholar
    • Export Citation
  • Landsteiner K 1899 Zur Kenntnis der sperzitich auf Blutkörperchen wirkenden sera. Centralbl J Bakt 25 546.

  • Liu Z, Zhao S, Chen Q, Yan K, Liu P, Li N, Cheng CY, Lee WM & Han D 2015 Roles of toll-like receptors 2 and 4 in mediating experimental autoimmune orchitis induction in mice. Biol ogy of Reprod uction 92 63. (https://doi.org/10.1095/biolreprod.114.123901)

    • Search Google Scholar
    • Export Citation
  • Losano JDA, Padín JF, Méndez-López I, Angrimani DSR, García AG, Barnabe VH & Nichi M 2017 The stimulated glycolytic pathway is able to maintain ATP levels and kinetic patterns of bovine epididymal sperm subjected to mitochondrial uncoupling. Oxidative Medicine and Cellular Longevity 2017 Article ID 1682393. (https://doi.org/10.1155/2017/1682393)

    • Search Google Scholar
    • Export Citation
  • Losano JDA, Angrimani DSR, Dalmazzo A, Rocha CC, Brito MM, Perez EGA, Tsunoda RH, Góes PAA, Mendes CM & Assumpção MEOA 2018 Effect of vitamin E and polyunsaturated fatty acids on cryopreserved sperm quality in Bos taurus bulls under testicular heat stress. Animal Biotechnology 29 100109. (https://doi.org/10.1080/10495398.2017.1322973)

    • Search Google Scholar
    • Export Citation
  • Losos GJ, Winter AJ & McEntee K 1968 Induction of testicular degeneration in bulls by isoimmunization. Am erican J ournal of Vet erinary Res earch 29 22952306.

    • Search Google Scholar
    • Export Citation
  • Menge AC & Christian JJ 1971 Effects of auto- and iso-immunization of bulls with semen and testis. Int ernational J ournal of Fert ility 16 130138.

    • Search Google Scholar
    • Export Citation
  • Menge AC, Stone WH, Tyler WJ & Casida LE 1962 Immunological studies on fertility and sterility. IV. Reproduction 3 3313 41. (https://doi.org/10.1530/jrf.0.0030331)

    • Search Google Scholar
    • Export Citation
  • Parsonson IM, Winter AJ & McEntee K 1971 Allergic epididymo-orchitis in guinea pigs and bulls. Vet erinary Pathol ogy 8 333351. (https://doi.org/10.1177/030098587100800405)

    • Search Google Scholar
    • Export Citation
  • Paul C, Teng S & Saunders PTK 2009 A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol ogy of Reprod uction 80 913919. (https://doi.org/10.1095/biolreprod.108.071779)

    • Search Google Scholar
    • Export Citation
  • Perez T & Cuellar Carrasco LW 1964 Autoinmunizacion espermática en sementales bovinos como causa de subfertilidad. In IVth International Congress on Animal Reproduction and Artificial Insemination, vol. 5, p. 527.

    • Search Google Scholar
    • Export Citation
  • Rahman MB, Vandaele L, Rijsselaere T, Maes D, Hoogewijs M, Frijters A, Noordman J, Granados A, Dernelle E & Shamsuddin M 2011 Scrotal insulation and its relationship to abnormal morphology, chromatin protamination and nuclear shape of spermatozoa in Holstein-Friesian and Belgian Blue bulls. Theriogenology 76 12461257. (https://doi.org/10.1016/j.theriogenology.2011.05.031)

    • Search Google Scholar
    • Export Citation
  • Ramamohana Rao AR, Bane A & Gustaffson BK 1980 Changes in the morphology of spermatozoa during their passage through the genital tract in dairy bulls with normal and impaired spermatogenesis. Theriogenology 14 112. (https://doi.org/10.1016/0093-691x(80)90129-6)

    • Search Google Scholar
    • Export Citation
  • Sinowatz F, Wrobel KH, Sinowatz S & Kugler P 1979 Ultrastructural evidence of phagocytosis of spermatozoa in the bovine rete testis and testicular straight tubules. J ournal of Reprod uction and Fert ility 57 14. (https://doi.org/10.1530/jrf.0.0570001)

    • Search Google Scholar
    • Export Citation
  • Vlok I, Ferrer M, Sardoy M & Anderson D 2009 Serum anti-sperm antibodies associated with orchitis in a bull. Clinical Theriogenology 1 251.

  • Vogler CJ, Saacke RG, Bame JH, Dwarnette JM & McGilliard ML 1991 Effects of scrotal insulation on viability characteristics of cryopreserved bovine semen. J ournal of Dairy Sci ence 74 38273835. (https://doi.org/10.3168/jds.S0022-0302(91)78575-5)

    • Search Google Scholar
    • Export Citation
  • Wildeus S & Entwistle KW 1983 Spermiogram and sperm reserves in hybrid Bos indicus x Bos taurus bulls after scrotal insulation. J ournal of Reprod uction and Fert ility 69 711716. (https://doi.org/10.1530/jrf.0.0690711)

    • Search Google Scholar
    • Export Citation
  • Wright PJ 1980 Serum spermagglutinins and semen quality in the bull. Australian Vet erinary J ournal 56 1013. (https://doi.org/10.1111/j.1751-0813.1980.tb02530.x)

    • Search Google Scholar
    • Export Citation
  • Zralý Z, Benová J, Šišák M, Diblíková I, Švecová D, Zajícová A & Vêžník Z 1998 Occurrence of antibodies to sperms in blood sera of bulls and boars. Veterinary Medicine : Czech 43 197204.

    • Search Google Scholar
    • Export Citation
  • Zralý Z, Benová J, Diblíková I, Švecová D, Kummer V, Mašková J & Vêžník Z 2002 Antisperm antibodies in blood sera of bulls and correlations with age, breed and ejaculate quality. Acta Vet erinaria Brno 71 30330 8. (https://doi.org/10.2754/avb200271030303)

    • Search Google Scholar
    • Export Citation