Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2020-0018
Animal Reproduction (AR)
Thematic Section: 36th Annual Meeting of the Association of Embryo Technology in Europe (AETE)

Defining the male contribution to embryo quality and offspring health in assisted reproduction in farm animals

Hannah Louise Morgan; Nader Eid; Afsaneh Khoshkerdar; Adam John Watkins

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Abstract

Abstract: Assisted reproductive technologies such as artificial insemination have delivered significant benefits for farm animal reproduction. However, as with humans, assisted reproduction in livestock requires the manipulation of the gametes and preimplantation embryo. The significance of this ‘periconception’ period is that it represents the transition from parental genome regulation to that of the newly formed embryo. Environmental perturbations during these early developmental stages can result in persistent changes in embryonic gene expression, fetal organ development and ultimately the long-term health of the offspring. While associations between maternal health and offspring wellbeing are well-defined, the significance of paternal health for the quality of his semen and the post-conception development of his offspring have largely been overlooked. Human and animal model studies have identified sperm epigenetic status (DNA methylation levels, histone modifications and RNA profiles) and seminal plasma-mediated maternal uterine immunological, inflammatory and vascular responses as the two central mechanisms capable of linking paternal health and post-fertilisation development. However, there is a significant knowledge gap about the father’s contribution to the long-term health of his offspring, especially with regard to farm animals. Such insights are essential to ensure the safety of widely used assisted reproductive practices and to gain better understanding of the role of paternal health for the well-being of his offspring. In this article, we will outline the impact of male health on semen quality (both sperm and seminal plasma), reproductive fitness and post-fertilisation offspring development and explore the mechanisms underlying the paternal programming of offspring health in farm animals.

Keywords

assisted reproductive technologies, fetal programming, semen quality

References

Alghamdi AS, Foster DN, Troedsson MH. Equine seminal plasma reduces sperm binding to polymorphonuclear neutrophils (PMNs) and improves the fertility of fresh semen inseminated into inflamed uteri. Reproduction. 2004;127(5):593-600. http://dx.doi.org/10.1530/rep.1.00096. PMid:15129015.

Argov-Argaman N, Mahgrefthe K, Zeron Y, Roth Z. Variation in lipid profiles within semen compartments—the bovine model of aging. Theriogenology. 2013;80(7):712-21. http://dx.doi.org/10.1016/j.theriogenology.2013.05.024. PMid:23830232.

Asbury AC, Hansen PJ. Effects of susceptibility of mares to endometritis and stage of cycle on phagocytic activity of uterine-derived neutrophils. J Reprod Fertil Suppl. 1987;35:311-6. PMid:3479586.

Balic IM, Milinkovic-Tur S, Samardžija M, Vince S. Effect of age and environmental factors on semen quality, glutathione peroxidase activity and oxidative parameters in Simmental bulls. Theriogenology. 2012;78(2):423-31. http://dx.doi.org/10.1016/j.theriogenology.2012.02.022. PMid:22538001.

Barakat R, Seymore T, Lin PP, Park CJ, Ko CJ. Prenatal exposure to an environmentally relevant phthalate mixture disrupts testicular steroidogenesis in adult male mice. Environ Res. 2019;172:194-201. http://dx.doi.org/10.1016/j.envres.2019.02.017. PMid:30802670.

Barcelo-Fimbres M, Campos-Chillon LF, Seidel GE Jr. In vitro fertilization using non-sexed and sexed bovine sperm: sperm concentration, sorter pressure, and bull effects. Reprod Domest Anim. 2011;46(3):495-502. http://dx.doi.org/10.1111/j.1439-0531.2010.01696.x. PMid:20946538.

Barker DJ, Eriksson JG, Forsén T, Osmond C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol. 2002;31(6):1235-9. http://dx.doi.org/10.1093/ije/31.6.1235. PMid:12540728.

Barker DJP, Osmond C, Winter PD, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;2(8663):577-80. http://dx.doi.org/10.1016/S0140-6736(89)90710-1. PMid:2570282.

Barth AD, Brito LF, Kastelic JP. The effect of nutrition on sexual development of bulls. Theriogenology. 2008;70(3):485-94. http://dx.doi.org/10.1016/j.theriogenology.2008.05.031. PMid:18539319.

Bastepe M. The GNAS Locus: Quintessential Complex Gene Encoding Gsalpha, XLalphas, and other Imprinted Transcripts. Curr Genomics. 2007;8(6):398-414. http://dx.doi.org/10.2174/138920207783406488. PMid:19412439.

Binder NK, Beard SA, Kaitu’u-Lino TJ, Tong S, Hannan NJ, Gardner DK. Paternal obesity in a rodent model affects placental gene expression in a sex-specific manner. Reproduction. 2015;149(5):435-44. http://dx.doi.org/10.1530/REP-14-0676. PMid:25725082.

Binder NK, Hannan NJ, Gardner DK. Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLoS One. 2012;7(12):e52304. http://dx.doi.org/10.1371/journal.pone.0052304. PMid:23300638.

Braunschweig M, Jagannathan V, Gutzwiller A, Bee G. Investigations on transgenerational epigenetic response down the male line in F2 pigs. PLoS One. 2012;7(2):e30583. http://dx.doi.org/10.1371/journal.pone.0030583. PMid:22359544.

Bromfield JJ, Schjenken JE, Chin PY, Care AS, Jasper MJ, Robertson SA. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci USA. 2014;111(6):2200-5. http://dx.doi.org/10.1073/pnas.1305609111. PMid:24469827.

Buckley F, Mee J, O’Sullivan K, Evans R, Berry D, Dillon P. Insemination factors affecting the conception rate in seasonal calving Holstein-Friesian cows. Reprod Nutr Dev. 2003;43(6):543-55. http://dx.doi.org/10.1051/rnd:2004002. PMid:15141438.

Card CJ, Anderson EJ, Zamberlan S, Krieger KE, Kaproth M, Sartini BL. Cryopreserved bovine spermatozoal transcript profile as revealed by high-throughput ribonucleic acid sequencing. Biol Reprod. 2013;88(2):49. http://dx.doi.org/10.1095/biolreprod.112.103788. PMid:23303677.

Castellini C, Lattaioli P, Dal Bosco A, Minelli A, Mugnai C. Oxidative status and semen characteristics of rabbit buck as affected by dietary vitamin E, C and n-3 fatty acids. Reprod Nutr Dev. 2003;43(1):91-103. http://dx.doi.org/10.1051/rnd:2003008. PMid:12785452.

Chen Q, Yan M, Cao Z, Li X, Zhang Y, Shi J, Feng GH, Peng H, Zhang X, Zhang Y, Qian J, Duan E, Zhai Q, Zhou Q. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science. 2016;351(6271):397-400. http://dx.doi.org/10.1126/science.aad7977. PMid:26721680.

Chutia T, Biswas RK, Tamuli MK, Deka BC, Sinha S, Goswami J, Banik S, Kayastha RB. Effect of holding of semen and washing of seminal plasma on quality and fertility of Hampshire boar semen preserved at liquid state. Anim Reprod Sci. 2014;145(3-4):141-9. http://dx.doi.org/10.1016/j.anireprosci.2014.01.007. PMid:24559728.

Colaco S, Sakkas D. Paternal factors contributing to embryo quality. J Assist Reprod Genet. 2018;35(11):1953-68. http://dx.doi.org/10.1007/s10815-018-1304-4. PMid:30206748.

Congras A, Yerle-Bouissou M, Pinton A, Vignoles F, Liaubet L, Ferchaud S, Acloque H. Sperm DNA methylation analysis in swine reveals conserved and species-specific methylation patterns and highlights an altered methylation at the GNAS locus in infertile boars. Biol Reprod. 2014;91(6):137. http://dx.doi.org/10.1095/biolreprod.114.119610. PMid:25320151.

Coulam CB, Stern JJ. Effect of seminal plasma on implantation rates. Early Pregnancy. 1995;1(1):33-6. PMid:9363233.

D’Amours O, Frenette G, Fortier M, Leclerc P, Sullivan R. Proteomic comparison of detergent-extracted sperm proteins from bulls with different fertility indexes. Reproduction. 2010;139(3):545-56. http://dx.doi.org/10.1530/REP-09-0375. PMid:19952166.

Davalieva K, Kiprijanovska S, Noveski P, Plaseski T, Kocevska B, Broussard C, Plaseska-Karanfilska D. Proteomic analysis of seminal plasma in men with different spermatogenic impairment. Andrologia. 2012;44(4):256-64. http://dx.doi.org/10.1111/j.1439-0272.2012.01275.x. PMid:22288839.

De Leeuw FE, Chen HC, Colenbrander B, Verkleij AJ. Cold-induced ultrastructural changes in bull and boar sperm plasma membranes. Cryobiology. 1990;27(2):171-83. http://dx.doi.org/10.1016/0011-2240(90)90009-S. PMid:2331890.

DeAngelis, A. M., Martini, A. E., & Owen, C. M. (2018). Assisted reproductive technology and epigenetics. Semin Reprod Med. 36(3-4), 221-32. http://dx.doi.org/10.1055/s-0038-1675780.

Dogan S, Vargovic P, Oliveira R, Belser LE, Kaya A, Moura A, Sutovsky P, Parrish J, Topper E, Memili E. Sperm protamine-status correlates to the fertility of breeding bulls. Biol Reprod. 2015;92(4):92. http://dx.doi.org/10.1095/biolreprod.114.124255. PMid:25673563.

Ealy AD, Wooldridge LK, McCoski SR. BOARD INVITED REVIEW: post-transfer consequences of in vitro-produced embryos in cattle. J Anim Sci. 2019;97(6):2555-68. http://dx.doi.org/10.1093/jas/skz116. PMid:30968113.

Eaton SA, Hough T, Fischer-Colbrie R, Peters J. Maternal inheritance of the Gnas cluster mutation Ex1A-T affects size, implicating NESP55 in growth. Mamm Genome. 2013;24(7-8):276-85. http://dx.doi.org/10.1007/s00335-013-9462-2. PMid:23839232.

Fang L, Jiang J, Li B, Zhou Y, Freebern E, Vanraden PM, Cole JB, Liu GE, Ma L. Genetic and epigenetic architecture of paternal origin contribute to gestation length in cattle. Commun Biol. 2019;2(1):100. http://dx.doi.org/10.1038/s42003-019-0341-6. PMid:30886909.

Faulkner LC, Hopwood ML, Wiltbank JN. Seminal vesiculectomy in bulls. II. Seminal characteristics and breeding trials. J Reprod Fertil. 1968;16(2):179-82. http://dx.doi.org/10.1530/jrf.0.0160179. PMid:5660277.

Fedorka CE, Scoggin KE, Woodward EM, Squires EL, Ball BA, Troedsson M. The effect of select seminal plasma proteins on endometrial mRNA cytokine expression in mares susceptible to persistent mating-induced endometritis. Reprod Domest Anim. 2017;52(1):89-96. http://dx.doi.org/10.1111/rda.12813. PMid:27686063.

Felicioni F, Pereira AD, Caldeira-Brant AL, Santos TG, Paula TMD, Magnabosco D, Bortolozzo FP, Tsoi S, Dyck MK, Dixon W, Martinelli PM, Jorge EC, Chiarini-Garcia H, Almeida FRCL. Postnatal development of skeletal muscle in pigs with intrauterine growth restriction: morphofunctional phenotype and molecular mechanisms. J Anat. 2020;236(5):840-53. http://dx.doi.org/10.1111/joa.13152. PMid:31997379.

Feugang JM, Rodriguez-Osorio N, Kaya A, Wang H, Page G, Ostermeier GC, Topper EK, Memili E. Transcriptome analysis of bull spermatozoa: implications for male fertility. Reprod Biomed Online. 2010;21(3):312-24. http://dx.doi.org/10.1016/j.rbmo.2010.06.022. PMid:20638337.

Fleming TP, Watkins AJ, Velazquez MA, Mathers JC, Prentice AM, Stephenson J, Barker M, Saffery R, Yajnik CS, Eckert JJ, Hanson MA, Forrester T, Gluckman PD, Godfrey KM. Origins of lifetime health around the time of conception: causes and consequences. Lancet. 2018;391(10132):1842-52. http://dx.doi.org/10.1016/S0140-6736(18)30312-X. PMid:29673874.

Flowers WL. Triennial Reproduction Symposium: sperm characteristics that limit success of fertilization. J Anim Sci. 2013;91(7):3022-9. http://dx.doi.org/10.2527/jas.2012-5945. PMid:23307855.

Fraser L, Strzezek J. Is there a relationship between the chromatin status and DNA fragmentation of boar spermatozoa following freezing-thawing? Theriogenology. 2007;68(2):248-57. http://dx.doi.org/10.1016/j.theriogenology.2007.05.001. PMid:17543381.

Fullston T, McPherson NO, Zander-Fox D, Lane M. The most common vices of men can damage fertility and the health of the next generation. J Endocrinol. 2017;234(2):F1-6. http://dx.doi.org/10.1530/JOE-16-0382. PMid:28500085.

Fullston T, Shehadeh H, Sandeman LY, Kang WX, Wu LL, Robker RL, McPherson NO, Lane M. Female offspring sired by diet induced obese male mice display impaired blastocyst development with molecular alterations to their ovaries, oocytes and cumulus cells. J Assist Reprod Genet. 2015;32(5):725-35. http://dx.doi.org/10.1007/s10815-015-0470-x. PMid:25854657.

Garner DL, Seidel GE Jr. History of commercializing sexed semen for cattle. Theriogenology. 2008;69(7):886-95. http://dx.doi.org/10.1016/j.theriogenology.2008.01.006. PMid:18343491.

Garner DL, Thomas CA, Gravance CG, Marshall CE, DeJarnette JM, Allen CH. Seminal plasma addition attenuates the dilution effect in bovine sperm. Theriogenology. 2001;56(1):31-40. http://dx.doi.org/10.1016/S0093-691X(01)00540-4. PMid:11467516.

Gliozzi TM, Zaniboni L, Cerolini S. DNA fragmentation in chicken spermatozoa during cryopreservation. Theriogenology. 2011;75(9):1613-22. http://dx.doi.org/10.1016/j.theriogenology.2011.01.001. PMid:21396690.

Grandjean V, Fourre S, De Abreu DA, Derieppe MA, Remy JJ, Rassoulzadegan M. RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Sci Rep. 2015;5(1):18193. http://dx.doi.org/10.1038/srep18193. PMid:26658372.

Guerrero-Bosagna C, Skinner MK. Environmentally induced epigenetic transgenerational inheritance of phenotype and disease. Mol Cell Endocrinol. 2012;354(1-2):3-8. http://dx.doi.org/10.1016/j.mce.2011.10.004. PMid:22020198.

Hammoud SS, Nix DA, Hammoud AO, Gibson M, Cairns BR, Carrell DT. Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men. Hum Reprod. 2011;26(9):2558-69. http://dx.doi.org/10.1093/humrep/der192. PMid:21685136.

Heshmat SM, Mullen JB, Jarvi KA, Soosaipillai A, Diamandis EP, Hamilton RJ, Lo KC. Seminal plasma lipocalin-type prostaglandin D synthase: a potential new marker for the diagnosis of obstructive azoospermia. J Urol. 2008;179(3):1077-80. http://dx.doi.org/10.1016/j.juro.2007.10.070. PMid:18206953.

Hori N, Nagai M, Hirayama M, Hirai T, Matsuda K, Hayashi M, Tanaka T, Ozawa T, Horike S. Aberrant CpG methylation of the imprinting control region KvDMR1 detected in assisted reproductive technology-produced calves and pathogenesis of large offspring syndrome. Anim Reprod Sci. 2010;122(3-4):303-12. http://dx.doi.org/10.1016/j.anireprosci.2010.09.008. PMid:21035970.

Ilacqua A, Izzo G, Emerenziani GP, Baldari C, Aversa A. Lifestyle and fertility: the influence of stress and quality of life on male fertility. Reprod Biol Endocrinol. 2018;16(1):115. http://dx.doi.org/10.1186/s12958-018-0436-9. PMid:30474562.

Inaba Y, Abe R, Geshi M, Matoba S, Nagai T, Somfai T. Sex-sorting of spermatozoa affects developmental competence of in vitro fertilized oocytes in a bull-dependent manner. J Reprod Dev. 2016;62(5):451-6. http://dx.doi.org/10.1262/jrd.2016-032. PMid:27301424.

Kaka A, Wahid H, Rosnina Y, Yimer N, Khumran AM, Sarsaifi K, Behan AA, Kaka U, Ebrahimi M. alpha-Linolenic acid supplementation in BioXcell® extender can improve the quality of post-cooling and frozen-thawed bovine sperm. Anim Reprod Sci. 2015;153:1-7. http://dx.doi.org/10.1016/j.anireprosci.2014.12.001. PMid:25544152.

Kastelic JP, Byrne Cook R, Coulter GH. Scrotal/testicular thermoregulation and the effects of increased testicular temperature in the bull. Vet Clin North Am Food Anim Pract. 1997;13(2):271-82. http://dx.doi.org/10.1016/S0749-0720(15)30340-6. PMid:9216048.

Killian GJ, Chapman DA, Rogowski LA. Fertility-associated proteins in Holstein bull seminal plasma. Biol Reprod. 1993;49(6):1202-7. http://dx.doi.org/10.1095/biolreprod49.6.1202. PMid:8286602.

Koivisto MB, Costa MT, Perri SH, Vicente WR. The effect of season on semen characteristics and freezability in Bos indicus and Bos taurus bulls in the southeastern region of Brazil. Reprod Domest Anim. 2009;44(4):587-92. http://dx.doi.org/10.1111/j.1439-0531.2008.01023.x. PMid:19090817.

Kotilainen T, Huhtinen M, Katila T. Sperm-induced leukocytosis in the equine uterus. Theriogenology. 1994;41(3):629-36. http://dx.doi.org/10.1016/0093-691X(94)90173-G. PMid:16727418.

Kropp J, Carrillo JA, Namous H, Daniels A, Salih SM, Song J, Khatib H. Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos. BMC Genomics. 2017;18(1):280. http://dx.doi.org/10.1186/s12864-017-3673-y. PMid:28381255.

Kutchy NA, Menezes ESB, Chiappetta A, Tan W, Wills RW, Kaya A, Topper E, Moura AA, Perkins AD, Memili E. Acetylation and methylation of sperm histone 3 lysine 27 (H3K27ac and H3K27me3) are associated with bull fertility. Andrologia. 2018;50(3):e12915. http://dx.doi.org/10.1111/and.12915. PMid:29057498.

Lambert S, Blondin P, Vigneault C, Labrecque R, Dufort I, Sirard MA. Spermatozoa DNA methylation patterns differ due to peripubertal age in bulls. Theriogenology. 2018;106:21-9. http://dx.doi.org/10.1016/j.theriogenology.2017.10.006. PMid:29031946.

Lambrot R, Xu C, Saint-Phar S, Chountalos G, Cohen T, Paquet M, Suderman M, Hallett M, Kimmins S. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat Commun. 2013;4(1):2889. http://dx.doi.org/10.1038/ncomms3889. PMid:24326934.

Lewis SE, Aitken RJ. DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res. 2005;322(1):33-41. http://dx.doi.org/10.1007/s00441-005-1097-5. PMid:15912407.

Liu Q, Zhou YF, Duan RJ, Wei HK, Jiang SW, Peng J. Effects of dietary n-6:n-3 fatty acid ratio and vitamin E on semen quality, fatty acid composition and antioxidant status in boars. Anim Reprod Sci. 2015;162:11-9. http://dx.doi.org/10.1016/j.anireprosci.2015.08.012. PMid:26417649.

Llamas Luceno N, Angrimani DSR, Bicudo LC, Szymanska KJ, Van Poucke M, Demeyere K, Meyer E, Peelman L, Mullaart E, Broekhuijse MLWJ, Van Soom A. Exposing dairy bulls to high temperature-humidity index during spermatogenesis compromises subsequent embryo development in vitro. Theriogenology. 2020;141:16-25. http://dx.doi.org/10.1016/j.theriogenology.2019.08.034. PMid:31494458.

Marconi G, Auge L, Oses R, Quintana R, Raffo F, Young E. Does sexual intercourse improve pregnancy rates in gamete intrafallopian transfer? Fertil Steril. 1989;51(2):357-9. http://dx.doi.org/10.1016/S0015-0282(16)60507-1. PMid:2643533.

Maxwell WM, de Graaf SP, Ghaoui R-H, Evans G. Seminal plasma effects on sperm handling and female fertility. Soc Reprod Fertil Suppl. 2007;64(1):13-38. http://dx.doi.org/10.5661/RDR-VI-13. PMid:17491139.

Maxwell WM, Welch GR, Johnson LA. Viability and membrane integrity of spermatozoa after dilution and flow cytometric sorting in the presence or absence of seminal plasma. Reprod Fertil Dev. 1996;8(8):1165-78. http://dx.doi.org/10.1071/RD9961165. PMid:8981641.

McCarthy MJ, Baumber J, Kass PH, Meyers SA. Osmotic stress induces oxidative cell damage to rhesus macaque spermatozoa. Biol Reprod. 2010;82(3):644-51. http://dx.doi.org/10.1095/biolreprod.109.080507. PMid:19846599.

McPherson NO, Fullston T, Bakos HW, Setchell BP, Lane M. Obese father’s metabolic state, adiposity, and reproductive capacity indicate son’s reproductive health. Fertil Steril. 2014;101(3):865-73. http://dx.doi.org/10.1016/j.fertnstert.2013.12.007. PMid:24424359.

Milardi, D., Grande, G., Vincenzoni, F., Messana, I., Pontecorvi, A., Marinis, L., Castagnola M, Marana, R. (2012). Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertil Steril. 97(1), 67-73.e1. http://dx.doi.org/10.1016/j.fertnstert.2011.10.013.

Morgan HL, Paganopoulou P, Akhtar S, Urquhart N, Philomin R, Dickinson Y, Watkins AJ. Paternal diet impairs F1 and F2 offspring vascular function through sperm and seminal plasma specific mechanisms in mice. J Physiol. 2020;598(4):699-715. http://dx.doi.org/10.1113/JP278270. PMid:31617219.

Murphy EM, Kelly AK, O’Meara C, Eivers B, Lonergan P, Fair S. Influence of bull age, ejaculate number, and season of collection on semen production and sperm motility parameters in Holstein Friesian bulls in a commercial artificial insemination centre. J Anim Sci. 2018;96(6):2408-18. http://dx.doi.org/10.1093/jas/sky130. PMid:29767722.

O’Leary S, Jasper MJ, Warnes GM, Armstrong DT, Robertson SA. Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig. Reproduction. 2004;128(2):237-47. http://dx.doi.org/10.1530/rep.1.00160. PMid:15280563.

Odhiambo JF, Poole DH, Hughes L, Dejarnette JM, Inskeep EK, Dailey RA. Pregnancy outcome in dairy and beef cattle after artificial insemination and treatment with seminal plasma or transforming growth factor beta-1. Theriogenology. 2009;72(4):566-71. http://dx.doi.org/10.1016/j.theriogenology.2009.04.013. PMid:19501392.

Oliveira RV, Dogan S, Belser LE, Kaya A, Topper E, Moura A, Thibaudeau G, Memili E. Molecular morphology and function of bull spermatozoa linked to histones and associated with fertility. Reproduction. 2013;146(3):263-72. http://dx.doi.org/10.1530/REP-12-0399. PMid:23904564.

Palma GA, Olivier NS, Neumuller C, Sinowatz F. Effects of sex-sorted spermatozoa on the efficiency of in vitro fertilization and ultrastructure of in vitro produced bovine blastocysts. Anat Histol Embryol. 2008;37(1):67-73. http://dx.doi.org/10.1111/j.1439-0264.2007.00795.x. PMid:18197903.

Pellegrino CA, Morotti F, Untura RM, Pontes JH, Pellegrino MF, Campolina JP, Seneda MM, Barbosa FA, Henry M. Use of sexed sorted semen for fixed-time artificial insemination or fixed-time embryo transfer of in vitro-produced embryos in cattle. Theriogenology. 2016;86(3):888-93. http://dx.doi.org/10.1016/j.theriogenology.2016.03.010. PMid:27068357.

Rahman MB, Kamal MM, Rijsselaere T, Vandaele L, Shamsuddin M, Van Soom A. Altered chromatin condensation of heat-stressed spermatozoa perturbs the dynamics of DNA methylation reprogramming in the paternal genome after in vitro fertilisation in cattle. Reprod Fertil Dev. 2014;26(8):1107-16. http://dx.doi.org/10.1071/RD13218. PMid:24041366.

Rahman MB, Schellander K, Luceno NL, Van Soom A. Heat stress responses in spermatozoa: mechanisms and consequences for cattle fertility. Theriogenology. 2018;113:102-12. http://dx.doi.org/10.1016/j.theriogenology.2018.02.012. PMid:29477908.

Reilly JN, McLaughlin EA, Stanger SJ, Anderson AL, Hutcheon K, Church K, Mihalas BP, Tyagi S, Holt JE, Eamens AL, Nixon B. Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome. Sci Rep. 2016;6(1):31794. http://dx.doi.org/10.1038/srep31794. PMid:27549865.

Rhoads RP, Baumgard LH, Suagee JK, Sanders SR. Nutritional interventions to alleviate the negative consequences of heat stress. Adv Nutr. 2013;4(3):267-76. http://dx.doi.org/10.3945/an.112.003376. PMid:23674792.

Robbins KM, Chen Z, Wells KD, Rivera RM. Expression of KCNQ1OT1, CDKN1C, H19, and PLAGL1 and the methylation patterns at the KvDMR1 and H19/IGF2 imprinting control regions is conserved between human and bovine. J Biomed Sci. 2012;19(1):95. http://dx.doi.org/10.1186/1423-0127-19-95. PMid:23153226.

Robertson SA, Care AS, Moldenhauer LM. Regulatory T cells in embryo implantation and the immune response to pregnancy. J Clin Invest. 2018;128(10):4224-35. http://dx.doi.org/10.1172/JCI122182. PMid:30272581.

Robertson SA, Mau VJ, Tremellen KP, Seamark RF. Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J Reprod Fertil. 1996;107(2):265-77. http://dx.doi.org/10.1530/jrf.0.1070265. PMid:8882294.

Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci. 2013;33(21):9003-12. http://dx.doi.org/10.1523/JNEUROSCI.0914-13.2013. PMid:23699511.

Roseboom TJ. Developmental plasticity and its relevance to assisted human reproduction. Hum Reprod. 2018;33(4):546-52. http://dx.doi.org/10.1093/humrep/dey034. PMid:29474550.

Ryan DP, Henzel KS, Pearson BL, Siwek ME, Papazoglou A, Guo L, Paesler K, Yu M, Müller R, Xie K, Schröder S, Becker L, Garrett L, Hölter SM, Neff F, Rácz I, Rathkolb B, Rozman J, Ehninger G, Klingenspor M, Klopstock T, Wolf E, Wurst W, Zimmer A, Fuchs H, Gailus-Durner V, Hrabě de Angelis M, Sidiropoulou K, Weiergräber M, Zhou Y, Ehninger D. A paternal methyl donor-rich diet altered cognitive and neural functions in offspring mice. Mol Psychiatry. 2018;23(5):1345-55. http://dx.doi.org/10.1038/mp.2017.53. PMid:28373690.

Sabes-Alsina M, Johannisson A, Lundeheim N, Lopez-Bejar M, Morrell JM. Effects of season on bull sperm quality in thawed samples in northern Spain. Vet Rec. 2017;180(10):251. http://dx.doi.org/10.1136/vr.103897. PMid:28100767.

Seidel GE Jr. Sexing mammalian sperm - Where do we go from here? J Reprod Dev. 2012;58(5):505-9. http://dx.doi.org/10.1262/jrd.2012-077. PMid:23124700.

Sharkey DJ, Tremellen KP, Jasper MJ, Gemzell-Danielsson K, Robertson SA. Seminal fluid induces leukocyte recruitment and cytokine and chemokine mRNA expression in the human cervix after coitus. J Immunol. 2012;188(5):2445-54. http://dx.doi.org/10.4049/jimmunol.1102736. PMid:22271649.

Sharma U. Paternal contributions to offspring health: role of sperm small RNAs in intergenerational transmission of epigenetic information. Front Cell Dev Biol. 2019;7:215. http://dx.doi.org/10.3389/fcell.2019.00215. PMid:31681757.

Skinner JD, Louw GN. Heat stress and spermatogenesis in Bos indicus and Bos taurus cattle. J Appl Physiol. 1966;21(6):1784-90. http://dx.doi.org/10.1152/jappl.1966.21.6.1784. PMid:5951717.

Steele H, Makri D, Maalouf WE, Reese S, Kolle S. Bovine sperm sexing alters sperm morphokinetics and subsequent early embryonic development. Sci Rep. 2020;10(1):6255. http://dx.doi.org/10.1038/s41598-020-63077-6. PMid:32277124.

Surai PF, Noble RC, Sparks NH, Speake BK. Effect of long-term supplementation with arachidonic or docosahexaenoic acids on sperm production in the broiler chicken. J Reprod Fertil. 2000;120(2):257-64. http://dx.doi.org/10.1530/jrf.0.1200257. PMid:11058441.

Thomsen H, Lee HK, Rothschild MF, Malek M, Dekkers JC. Characterization of quantitative trait loci for growth and meat quality in a cross between commercial breeds of swine. J Anim Sci. 2004;82(8):2213-28. http://dx.doi.org/10.2527/2004.8282213x. PMid:15318717.

Thundathil JC, Dance AL, Kastelic JP. Fertility management of bulls to improve beef cattle productivity. Theriogenology. 2016;86(1):397-405. http://dx.doi.org/10.1016/j.theriogenology.2016.04.054. PMid:27173954.

Tremellen KP, Valbuena D, Landeras J, Ballesteros A, Martinez J, Mendoza S, Norman RJ, Robertson SA, Simón C. The effect of intercourse on pregnancy rates during assisted human reproduction. Hum Reprod. 2000;15(12):2653-8. http://dx.doi.org/10.1093/humrep/15.12.2653. PMid:11098040.

Troedsson MH, Loset K, Alghamdi AM, Dahms B, Crabo BG. Interaction between equine semen and the endometrium: the inflammatory response to semen. Anim Reprod Sci. 2001;68(3-4):273-8. http://dx.doi.org/10.1016/S0378-4320(01)00164-6. PMid:11744271.

Ugur MR, Saber Abdelrahman A, Evans HC, Gilmore AA, Hitit M, Arifiantini RI, Purwantara B, Kaya A, Memili E. Advances in Cryopreservation of Bull Sperm. Front Vet Sci. 2019;6:268. http://dx.doi.org/10.3389/fvets.2019.00268. PMid:31552277.

van der Heijden GW, Ramos L, Baart EB, van den Berg IM, Derijck AA, van der Vlag J, Martini E, de Boer P. Sperm-derived histones contribute to zygotic chromatin in humans. BMC Dev Biol. 2008;8(1):34. http://dx.doi.org/10.1186/1471-213X-8-34. PMid:18377649.

Van Tran L, Malla BA, Kumar S, Tyagi AK. Polyunsaturated fatty acids in male ruminant reproduction - a review. Asian-Australas J Anim Sci. 2017;30(5):622-37. http://dx.doi.org/10.5713/ajas.15.1034. PMid:26954196.

Velazquez MA, Fleming TP, Watkins AJ. Periconceptional environment and the developmental origins of disease. J Endocrinol. 2019;242(1):T33-49. http://dx.doi.org/10.1530/JOE-18-0676. PMid:30707679.

Verma, A., Rajput, S., De, S., Kumar, R., Chakravarty, A. K., & Datta, T. K. (2014). Genome-wide profiling of sperm DNA methylation in relation to buffalo (Bubalus bubalis) bull fertility. Theriogenology. 82(5), 750-9. e1. http://dx.doi.org/10.1016/j.theriogenology.2014.06.012.

Vilés K, Rabanal R, Rodríguez-Prado M, Miró J. Influence of seminal plasma on leucocyte migration and amount of COX-2 protein in the jenny endometrium after insemination with frozen-thawed semen. Anim Reprod Sci. 2013;143(1-4):57-63. http://dx.doi.org/10.1016/j.anireprosci.2013.11.002. PMid:24280633.

Vojtech L, Woo S, Hughes S, Levy C, Ballweber L, Sauteraud RP, Strobl J, Westerberg K, Gottardo R, Tewari M, Hladik F. Exosomes in human semen carry a distinctive repertoire of small non-coding RNAs with potential regulatory functions. Nucleic Acids Res. 2014;42(11):7290-304. http://dx.doi.org/10.1093/nar/gku347. PMid:24838567.

Waberski D, Schafer J, Bolling A, Scheld M, Henning H, Hambruch N, Schuberth HJ, Pfarrer C, Wrenzycki C, Hunter RHF. Seminal plasma modulates the immune-cytokine network in the porcine uterine tissue and pre-ovulatory follicles. PLoS One. 2018;13(8):e0202654. http://dx.doi.org/10.1371/journal.pone.0202654. PMid:30153288.

Wallace JM, Milne JS, Aitken BW, Aitken RP, Adam CL. Ovine prenatal growth-restriction and sex influence fetal adipose tissue phenotype and impact postnatal lipid metabolism and adiposity in vivo from birth until adulthood. PLoS One. 2020;15(2):e0228732. http://dx.doi.org/10.1371/journal.pone.0228732. PMid:32059008.

Watkins AJ, Dias I, Tsuro H, Allen D, Emes RD, Moreton J, Wilson R, Ingram RJM, Sinclair KD. Paternal diet programs offspring health through sperm- and seminal plasma-specific pathways in mice. Proc Natl Acad Sci USA. 2018;115(40):10064-9. http://dx.doi.org/10.1073/pnas.1806333115. PMid:30150380.
 


Submitted date:
03/02/2020

Accepted date:
05/19/2020

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