Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2023-0076
Animal Reproduction (AR)
Thematic Section: 36th Annual Meeting of the Brazilian Embryo Technology Society (SBTE)

Paternal effects on fetal programming

Carl Robertson Dahlen; Samat Amat; Joel S. Caton; Matthew S. Crouse; Wellison Jarles Da Silva Diniz; Lawrence P. Reynolds

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Abstract

Paternal programming is the concept that the environmental signals from the sire’s experiences leading up to mating can alter semen and ultimately affect the phenotype of resulting offspring. Potential mechanisms carrying the paternal effects to offspring can be associated with epigenetic signatures (DNA methylation, histone modification and non-coding RNAs), oxidative stress, cytokines, and the seminal microbiome. Several opportunities exist for sperm/semen to be influenced during development; these opportunities are within the testicle, the epididymis, or accessory sex glands. Epigenetic signatures of sperm can be impacted during the pre-natal and pre-pubertal periods, during sexual maturity and with advancing sire age. Sperm are susceptible to alterations as dictated by their developmental stage at the time of the perturbation, and sperm and seminal plasma likely have both dependent and independent effects on offspring. Research using rodent models has revealed that many factors including over/under nutrition, dietary fat, protein, and ingredient composition (e.g., macro- or micronutrients), stress, exercise, and exposure to drugs, alcohol, and endocrine disruptors all elicit paternal programming responses that are evident in offspring phenotype. Research using livestock species has also revealed that sire age, fertility level, plane of nutrition, and heat stress can induce alterations in the epigenetic, oxidative stress, cytokine, and microbiome profiles of sperm and/or seminal plasma. In addition, recent findings in pigs, sheep, and cattle have indicated programming effects in blastocysts post-fertilization with some continuing into post-natal life of the offspring. Our research group is focused on understanding the effects of common management scenarios of plane of nutrition and growth rates in bulls and rams on mechanisms resulting in paternal programming and subsequent offspring outcomes. Understanding the implication of paternal programming is imperative as short-term feeding and management decisions have the potential to impact productivity and profitability of our herds for generations to come.

Keywords

fetal programming, sire, epigenetics, offspring outcomes, paternal programming

References

Aiken CE, Ozanne SE. Transgenerational developmental programming. Hum Reprod Update. 2014;20(1):63-75. http://dx.doi.org/10.1093/humupd/dmt043. PMid:24082037.

Aitken RJ. Impact of oxidative stress on male and female germ cells: implications for fertility. Reproduction. 2020;159(4):R189-201. http://dx.doi.org/10.1530/REP-19-0452. PMid:31846434.

Alves MBR, Arruda RP, Batissaco L, Garcia-Oliveros LN, Gonzaga VHG, Nogueira VJM, Almeida FDS, Pinto SCC, Andrade GM, Perecin F, Silveira JC, Celeghini ECC. Changes in miRNA levels of sperm and small extracellular vesicles of seminal plasma are associated with transient scrotal heat stress in bulls. Theriogenology. 2021;161:26-40. http://dx.doi.org/10.1016/j.theriogenology.2020.11.015. PMid:33278692.

Ashapkin V, Suvorov A, Pilsner JR, Krawetz SA, Sergeyev O. Age-associated epigenetic changes in mammalian sperm: implications for offspring health and development. Hum Reprod Update. 2023;29(1):24-44. http://dx.doi.org/10.1093/humupd/dmac033. PMid:36066418.

Ayad B, Omolaoye TS, Louw N, Ramsunder Y, Skosana BT, Oyeipo PI, Du Plessis SS. Oxidative stress and male infertility: evidence from a research perspective. Front Reprod Health. 2022;4:822257. http://dx.doi.org/10.3389/frph.2022.822257. PMid:36303652.

Bailey JL, Dalvai M, Lessard M, Herst PM, Charest PL, Navarro P. Beyond fertilisation: how the paternal environment influences future generations. Anim Reprod Sci. 2020;220:106503. http://dx.doi.org/10.1016/j.anireprosci.2020.106503. PMid:32536524.

Barker DJ, Clark PM. Fetal undernutrition and disease in later life. Rev Reprod. 1997;2(2):105-12. http://dx.doi.org/10.1530/ror.0.0020105. PMid:9414472.

Billah MM, Khatiwada S, Morris MJ, Maloney CA. Effects of paternal overnutrition and interventions on future generations. Int J Obes. 2022;46(5):901-17. http://dx.doi.org/10.1038/s41366-021-01042-7. PMid:35022547.

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.

Braz CU, Taylor T, Namous H, Townsend J, Crenshaw T, Khatib H. Paternal diet induces transgenerational epigenetic inheritance of DNA methylation signatures and phenotypes in sheep model. PNAS Nexus. 2022;1(2):pgac040. http://dx.doi.org/10.1093/pnasnexus/pgac040. PMid:36713326.

Bromfield JJ. A role for seminal plasma in modulating pregnancy outcomes in domestic species. Reproduction. 2016;152(6):R223-32. http://dx.doi.org/10.1530/REP-16-0313. PMid:27601714.

Champroux A, Cocquet J, Henry-Berger J, Drevet JR, Kocer A. A decade of exploring the mammalian sperm epigenome: paternal epigenetic and transgenerational inheritance. Front Cell Dev Biol. 2018;6:50. http://dx.doi.org/10.3389/fcell.2018.00050. PMid:29868581.

Chan JC, Morgan CP, Leu NA, Shetty A, Cisse YM, Nugent BM, Morrison KE, Jašarević E, Huang W, Kanyuch N, Rodgers AB, Bhanu NV, Berger DS, Garcia BA, Ament S, Kane M, Epperson CN, Bale TL. Reproductive tract extracellular vesicles are sufficient to transmit intergenerational stress and program neurodevelopment. Nat Commun. 2020;11(1):1499. http://dx.doi.org/10.1038/s41467-020-15305-w. PMid:32198406.

Chukrallah LG, Badrinath A, Seltzer K, Snyder EM. Of rodents and ruminants: a comparison of small noncoding RNA requirements in mouse and bovine reproduction. J Anim Sci. 2021;99(3):skaa388. http://dx.doi.org/10.1093/jas/skaa388. PMid:33677580.

Claycombe-Larson KG, Bundy AN, Roemmich JN. Paternal high-fat diet and exercise regulate sperm miRNA and histone methylation to modify placental inflammation, nutrient transporter mRNA expression and fetal weight in a sex-dependent manner. J Nutr Biochem. 2020;81:108373. http://dx.doi.org/10.1016/j.jnutbio.2020.108373. PMid:32422425.

Costes V, Chaulot-Talmon A, Sellem E, Perrier JP, Aubert-Frambourg A, Jouneau L, Pontlevoy C, Hozé C, Fritz S, Boussaha M, Le Danvic C, Sanchez MP, Boichard D, Schibler L, Jammes H, Jaffrézic F, Kiefer H. Predicting male fertility from the sperm methylome: application to 120 bulls with hundreds of artificial insemination records. Clin Epigenetics. 2022;14(1):54. http://dx.doi.org/10.1186/s13148-022-01275-x. PMid:35477426.

Dahlen CR, Borowicz PP, Ward AK, Caton JS, Czernik M, Palazzese L, Loi P, Reynolds LP. Programming of embryonic development. Int J Mol Sci. 2021;22(21):11668. http://dx.doi.org/10.3390/ijms222111668. PMid:34769097.

Duffy KA, Bale TL, Epperson CN. Germ cell drivers: transmission of preconception stress across generations. Front Hum Neurosci. 2021;15:642762. http://dx.doi.org/10.3389/fnhum.2021.642762. PMid:34322003.

Fair T. The contribution of the maternal immune system to the establishment of pregnancy in cattle. Front Immunol. 2015;6:7. http://dx.doi.org/10.3389/fimmu.2015.00007. PMid:25674085.

Gapp K, Parada GE, Gross F, Corcoba A, Kaur J, Grau E, Hemberg M, Bohacek J, Miska EA. Single paternal dexamethasone challenge programs offspring metabolism and reveals multiple candidates in RNA-mediated inheritance. iScience. 2021;24(8):102870. http://dx.doi.org/10.1016/j.isci.2021.102870. PMid:34386731.

Garcia-Oliveros LN, Arruda RP, Batissaco L, Gonzaga VHG, Nogueira VJM, Florez-Rodriguez SA, Almeida FDS, Alves MBR, Pinto SCC, Nichi M, Losano JDA, Kawai GKV, Celeghini ECC. Chronological characterization of sperm morpho-functional damage and recovery after testicular heat stress in Nellore bulls. J Therm Biol. 2022;106:103237. http://dx.doi.org/10.1016/j.jtherbio.2022.103237. PMid:35636895.

Godfrey KM, Barker DJ. Fetal programming and adult health. Public Health Nutr. 2001;4(2B):611-24. http://dx.doi.org/10.1079/PHN2001145. PMid:11683554.

Gross N, Taylor T, Crenshaw T, Khatib H. The intergenerational impacts of paternal diet on DNA methylation and offspring phenotypes in sheep. Front Genet. 2020;11:597943. http://dx.doi.org/10.3389/fgene.2020.597943. PMid:33250925.

Guan Y, Liang G, Hawken PAR, Malecki IA, Cozens G, Vercoe PE, Martin GB, Guan LL. Roles of small RNAs in the effects of nutrition on apoptosis and spermatogenesis in the adult testis. Sci Rep. 2015;5(1):10372. http://dx.doi.org/10.1038/srep10372. PMid:25996545.

Guan Y, Liang G, Martin GB, Guan LL. Functional changes in mRNA expression and alternative pre-mRNA splicing associated with the effects of nutrition on apoptosis and spermatogenesis in the adult testis. BMC Genomics. 2017;18(1):64. http://dx.doi.org/10.1186/s12864-016-3385-8. PMid:28068922.

Guan Y, Malecki IA, Hawken PAR, Linden MD, Martin GB. Under-nutrition reduces spermatogenic efficiency and sperm velocity, and increases sperm DNA damage in sexually mature male sheep. Anim Reprod Sci. 2014;149(3-4):163-72. http://dx.doi.org/10.1016/j.anireprosci.2014.07.014. PMid:25086661.

Hammer CJ, Caton JS, Dahlen CR, Ward AK, Borowicz PP, Reynolds LP. DOHaD: a menagerie of adaptations and perspectives: large animal models of developmental programming: sustenance, stress, and sex matter. Reproduction. 2023;165(6):F1-13. http://dx.doi.org/10.1530/REP-22-0453. PMid:36951791.

Harrison TD, Chaney EM, Brandt KJ, Ault-Seay TB, Payton RR, Schneider LG, Strickland LG, Schrick FN, McLean KJ. The effects of nutritional level and body condition score on cytokines in seminal plasma of beef bulls. Front Anim Sci. 2023;3:1078960. http://dx.doi.org/10.3389/fanim.2022.1078960.

Hur SS, Cropley JE, Suter CM. Paternal epigenetic programming: evolving metabolic disease risk. J Mol Endocrinol. 2017;58(3):R159-68. http://dx.doi.org/10.1530/JME-16-0236. PMid:28100703.

Ibeagha-Awemu EM, Khatib H. Epigenetics of livestock health, production, and breeding. In: Tollefsbol TO, editor. Handbook of epigenetics. 3rd ed. Amsterdam: Academic Press; 2023. p. 569-610. http://dx.doi.org/10.1016/B978-0-323-91909-8.00041-4.

Johnson C, Kiefer H, Chaulot-Talmon A, Dance A, Sellem E, Jouneau L, Jammes H, Kastelic J, Thundathil J. Prepubertal nutritional modulation in the bull and its impact on sperm DNA methylation. Cell Tissue Res. 2022;389(3):587-601. http://dx.doi.org/10.1007/s00441-022-03659-0. PMid:35779136.

Kalo D, Reches D, Netta N, Komsky-Elbaz A, Zeron Y, Moallem U, Roth Z. Carryover effects of feeding bulls with an omega-3-enriched-diet: from spermatozoa to developed embryos. PLoS One. 2022;17(3):e0265650. http://dx.doi.org/10.1371/journal.pone.0265650. PMid:35324945.

Kiefer H, Sellem E, Bonnet-Garnier A, Pannetier M, Costes V, Schibler L, Jammes H. The epigenome of male germ cells and the programming of phenotypes in cattle. Anim Front. 2021;11(6):28-38. http://dx.doi.org/10.1093/af/vfab062. PMid:34934527.

Koziol JH, Sheets T, Wickware CL, Johnson TA. Composition and diversity of the seminal microbiota in bulls and its association with semen parameters. Theriogenology. 2022;182:17-25. http://dx.doi.org/10.1016/j.theriogenology.2022.01.029. PMid:35123307.

Kretschmer M, Gapp K. Deciphering the RNA universe in sperm in its role as a vertical information carrier. Environ Epigenet. 2022;8(1):dvac011. http://dx.doi.org/10.1093/eep/dvac011. PMid:35633894.

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.

Kusuyama J, Alves-Wagner AB, Makarewicz NS, Goodyear LJ. Effects of maternal and paternal exercise on offspring metabolism. Nat Metab. 2020;2(9):858-72. http://dx.doi.org/10.1038/s42255-020-00274-7. PMid:32929233.

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 M-A. 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.

Lee HJ, Ryu J-S, Choi NY, Park YS, Kim YI, Han DW, Ko K, Shin CY, Hwang HS, Kang K-S, Ko K. Transgenerational effects of paternal alcohol exposure in mouse offspring. Anim Cells Syst. 2013;17(6):429-34. http://dx.doi.org/10.1080/19768354.2013.865675.

Lima AO, Afonso J, Edson J, Marcellin E, Palfreyman R, Porto-Neto LR, Reverter A, Fortes MRS. Network analyses predict small RNAs that might modulate gene expression in the testis and epididymis of Bos indicus bulls. Front Genet. 2021;12:610116. http://dx.doi.org/10.3389/fgene.2021.610116. PMid:33995471.

Lismer A, Kimmins S. Emerging evidence that the mammalian sperm epigenome serves as a template for embryo development. Nat Commun. 2023;14(1):2142. http://dx.doi.org/10.1038/s41467-023-37820-2. PMid:37059740.

Liu J, Shi J, Hernandez R, Li X, Konchadi P, Miyake Y, Chen Q, Zhou T, Zhou C. Paternal phthalate exposure-elicited offspring metabolic disorders are associated with altered sperm small RNAs in mice. Environ Int. 2023;172:107769. http://dx.doi.org/10.1016/j.envint.2023.107769. PMid:36709676.

Luecke SM, Webb EM, Dahlen CR, Reynolds LP, Amat S. Seminal and vagino-uterine microbiome and their individual and interactive effects on cattle fertility. Front Microbiol. 2022;13:1029128. http://dx.doi.org/10.3389/fmicb.2022.1029128. PMid:36425035.

Marcho C, Oluwayiose OA, Pilsner JR. The preconception environment and sperm epigenetics. Andrology. 2020;8(4):924-42. http://dx.doi.org/10.1111/andr.12753. PMid:31901222.

Marey MA, Ezz MA, Akthar I, Yousef MS, Imakawa K, Shimada M, Miyamoto A. Sensing sperm via maternal immune system: a potential mechanism for controlling microenvironment for fertility in the cow. J Anim Sci. 2020;98(Suppl 1):S88-95. http://dx.doi.org/10.1093/jas/skaa147. PMid:32810249.

Marey MA, Ma D, Yoshino H, Elesh IF, Zinnah MA, Fiorenza MF, Moriyasu S, Miyamoto A. Sperm induce proinflammatory responses in the uterus and peripheral blood immune cells of artificially inseminated cows. J Reprod Dev. 2023;69(2):95-102. http://dx.doi.org/10.1262/jrd.2022-124. PMid:36775285.

Mateo-Otero Y, Sánchez JM, Recuero S, Bagés-Arnal S, McDonald M, Kenny DA, Yeste M, Lonergan P, Fernandez-Fuertes B. Effect of exposure to seminal plasma through natural mating in cattle on conceptus length and gene expression. Front Cell Dev Biol. 2020;8:341. http://dx.doi.org/10.3389/fcell.2020.00341. PMid:32478076.

Moreira BP, Oliveira PF, Alves MG. Molecular mechanisms controlled by mTOR in male reproductive system. Int J Mol Sci. 2019;20(7):1633. http://dx.doi.org/10.3390/ijms20071633. PMid:30986927.

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.

Morgan HL, Watkins AJ. The influence of seminal plasma on offspring development and health. Semin Cell Dev Biol. 2020;97:131-7. http://dx.doi.org/10.1016/j.semcdb.2019.06.008. PMid:31254609.

Moura FH, Macias-Franco A, Pena-Bello CA, Archilia EC, Batalha IM, Silva AE, Moreira GM, Norris AB, Schütz LF, Fonseca MA. Sperm DNA 5-methyl cytosine and RNA N 6-methyladenosine methylation are differently affected during periods of body weight losses and body weight gain of young and mature breeding bulls. J Anim Sci. 2022;100(2):skab362. http://dx.doi.org/10.1093/jas/skab362. PMid:34902028.

Nongbua T, Guo Y, Ntallaris T, Rubér M, Rodriguez-Martinez H, Humblot P, Morrell JM. Bull seminal plasma stimulates in vitro production of TGF-β, IL-6 and IL-8 from bovine endometrial epithelial cells, depending on dose and bull fertility. J Reprod Immunol. 2020;142:103179. http://dx.doi.org/10.1016/j.jri.2020.103179. PMid:32717675.

Ortiz WG, Rizo JA, Carvalheira LR, Ahmed BMS, Estrada-Cortes E, Harstine BR, Bromfield JJ, Hansen PJ. Effects of intrauterine infusion of seminal plasma at artificial insemination on fertility of lactating Holstein cows. J Dairy Sci. 2019;102(7):6587-94. http://dx.doi.org/10.3168/jds.2019-16251. PMid:31103294.

Perrier JP, Kenny DA, Chaulot-Talmon A, Byrne CJ, Sellem E, Jouneau L, Aubert-Frambourg A, Schibler L, Jammes H, Lonergan P, Fair S, Kiefer H. Accelerating onset of puberty through modification of early life nutrition induces modest but persistent changes in bull sperm DNA methylation profiles post-puberty. Front Genet. 2020;11:945. http://dx.doi.org/10.3389/fgene.2020.00945. PMid:33005172.

Phillips N, Taylor L, Bachmann G. Maternal, infant and childhood risks associated with advanced paternal age: the need for comprehensive counseling for men. Maturitas. 2019;125:81-4. http://dx.doi.org/10.1016/j.maturitas.2019.03.020. PMid:31133222.

Radford EJ, Ito M, Shi H, Corish JA, Yamazawa K, Isganaitis E, Seisenberger S, Hore TA, Reik W, Erkek S, Peters AHFM, Patti ME, Ferguson-Smith AC. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science. 2014;345(6198):1255903. http://dx.doi.org/10.1126/science.1255903. PMid:25011554.

Rahman MB, Schellander K, Luceño 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.

Rahman MB, Vandaele L, Rijsselaere T, Maes D, Hoogewijs M, Frijters A, Noordman J, Granados A, Dernelle E, Shamsuddin M, Parrish JJ, Van Soom A. Scrotal insulation and its relationship to abnormal morphology, chromatin protamination and nuclear shape of spermatozoa in Holstein-Friesian and Belgian Blue bulls. Theriogenology. 2011;76(7):1246-57. http://dx.doi.org/10.1016/j.theriogenology.2011.05.031. PMid:21777969.

Reynolds LP, Borowicz PP, Caton JS, Vonnahme KA, Luther JS, Hammer CJ, Carlin KRM, Grazul-Bilska AT, Redmer DA. Developmental programming: the concept, large animal models, and the key role of uteroplacental vascular development. J Anim Sci. 2010;88(Suppl 13):E61-72. http://dx.doi.org/10.2527/jas.2009-2359. PMid:20023136.

Roca J, Rodriguez-Martinez H, Padilla L, Lucas X, Barranco I. Extracellular vesicles in seminal fluid and effects on male reproduction. An overview in farm animals and pets. Anim Reprod Sci. 2022;246:106853. http://dx.doi.org/10.1016/j.anireprosci.2021.106853. PMid:34556398.

Roseboom TJ. Epidemiological evidence for the developmental origins of health and disease: effects of prenatal undernutrition in humans. J Endocrinol. 2019;242(1):T135-44. http://dx.doi.org/10.1530/JOE-18-0683. PMid:31207580.

Rumph JT, Stephens VR, Ameli S, Brown LK, Rayford KJ, Nde PN, Osteen KG, Bruner-Tran KL. A paternal fish oil diet preconception reduces lung inflammation in a toxicant-driven murine model of new bronchopulmonary dysplasia. Mar Drugs. 2023;21(3):161. http://dx.doi.org/10.3390/md21030161. PMid:36976210.

Rumph JT, Stephens VR, Ameli S, Gaines PN, Osteen KG, Bruner-Tran KL, Nde PN. A paternal fish oil diet preconception modulates the gut microbiome and attenuates necrotizing enterocolitis in neonatal mice. Mar Drugs. 2022;20(6):390. http://dx.doi.org/10.3390/md20060390. PMid:35736193.

Sabei L, Bernardino T, Parada Sarmiento M, Barbosa BS, Farias SS, Ghantous GF, Lima CG, Poletto R, Zanella AJ. Life experiences of boars can shape the survival, aggression, and nociception responses of their offspring. Front Anim Sci. 2023;4:1142628. http://dx.doi.org/10.3389/fanim.2023.1142628.

Schoenmakers S, Steegers-Theunissen R, Faas M. The matter of the reproductive microbiome. Obstet Med. 2019;12(3):107-15. http://dx.doi.org/10.1177/1753495X18775899. PMid:31523266.

Sellem E, Marthey S, Rau A, Jouneau L, Bonnet A, Le Danvic C, Guyonnet B, Kiefer H, Jammes H, Schibler L. Dynamics of cattle sperm sncRNAs during maturation, from testis to ejaculated sperm. Epigenetics Chromatin. 2021;14(1):24. http://dx.doi.org/10.1186/s13072-021-00397-5. PMid:34030709.

Senger P. Pathways to pregnancy and parturition. 3rd ed. Redmond: Current Conceptions, Inc., 2012.

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.

Staub C, Johnson L. Review: spermatogenesis in the bull. Animal. 2018;12(Suppl 1):s27-35. http://dx.doi.org/10.1017/S1751731118000435. PMid:29882505.

Toschi P, Capra E, Anzalone DA, Lazzari B, Turri F, Pizzi F, Scapolo PA, Stella A, Williams JL, Marsan PA, Loi P. Maternal peri-conceptional undernourishment perturbs offspring sperm methylome. Reproduction. 2020;159(5):513-23. http://dx.doi.org/10.1530/REP-19-0549. PMid:32103819.

Toussaint AB, Ellis AS, Bongiovanni AR, Peterson DR, Bavley CC, Karbalaei R, Mayberry HL, Bhakta S, Dressler CC, Imperio CG, Maurer JJ, Schmidt HD, Chen C, Bland K, Liu-Chen LY, Wimmer ME. Paternal morphine exposure enhances morphine self-administration and induces region-specific neural adaptations in reward-related brain regions of male offspring. bioRxiv. In press 2023. PMid:36711571.

Wang Y, Chen Z-P, Hu H, Lei J, Zhou Z, Yao B, Chen L, Liang G, Zhan S, Zhu X, Jin F, Ma R, Zhang J, Liang H, Xing M, Chen XR, Zhang CY, Zhu JN, Chen X. Sperm microRNAs confer depression susceptibility to offspring. Sci Adv. 2021;7(7):eabd7605. http://dx.doi.org/10.1126/sciadv.abd7605. PMid:33568480.

Watkins AJ, Sirovica S, Stokes B, Isaacs M, Addison O, Martin RA. Paternal low protein diet programs preimplantation embryo gene expression, fetal growth and skeletal development in mice. Biochim Biophys Acta Mol Basis Dis. 2017;1863(6):1371-81. http://dx.doi.org/10.1016/j.bbadis.2017.02.009. PMid:28189722.

Webb EM, Holman DB, Schmidt KN, Crouse MS, Dahlen CR, Cushman RA, Snider AP, McCarthy KL, Amat S. A longitudinal characterization of the seminal microbiota and antibiotic resistance in yearling beef bulls subjected to different rates of gain. Microbiol Spectr. 2023;11(2):e0518022. http://dx.doi.org/10.1128/spectrum.05180-22. PMid:36916922.

Werry N, Russell SJ, Gillis DJ, Miller S, Hickey K, Larmer S, Lohuis M, Librach C, LaMarre J. Characteristics of miRNAs present in bovine sperm and associations with differences in fertility. Front Endocrinol. 2022;13:874371. http://dx.doi.org/10.3389/fendo.2022.874371. PMid:35663333.

Wu C, Blondin P, Vigneault C, Labrecque R, Sirard M-A. Sperm miRNAs- potential mediators of bull age and early embryo development. BMC Genomics. 2020a;21(1):798. http://dx.doi.org/10.1186/s12864-020-07206-5. PMid:33198638.

Wu C, Blondin P, Vigneault C, Labrecque R, Sirard M-A. The age of the bull influences the transcriptome and epigenome of blastocysts produced by IVF. Theriogenology. 2020b;144:122-31. http://dx.doi.org/10.1016/j.theriogenology.2019.12.020. PMid:31951983.

Wu C, Wang C, Zhai B, Zhao Y, Zhao Z, Yuan Z, Zhang M, Tian K, Fu X. Study of microRNA expression profile in different regions of ram epididymis. Reprod Domest Anim. 2021;56(9):1209-19. http://dx.doi.org/10.1111/rda.13978. PMid:34169586.

Wu G, Bazer FW, Wallace JM, Spencer TE. Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci. 2006;84(9):2316-37. http://dx.doi.org/10.2527/jas.2006-156. PMid:16908634.

Xia W, Mruk DD, Cheng CY. C-type natriuretic peptide regulates blood–testis barrier dynamics in adult rat testes. Proc Natl Acad Sci USA. 2007;104(10):3841-6. http://dx.doi.org/10.1073/pnas.0610100104. PMid:17360440.

Yockey LJ, Iwasaki A. Interferons and proinflammatory cytokines in pregnancy and fetal development. Immunity. 2018;49(3):397-412. http://dx.doi.org/10.1016/j.immuni.2018.07.017. PMid:30231982.

Zhao L, Liu X, Gomez NA, Gao Y, Son JS, Chae SA, Zhu MJ, Du M. Stage-specific nutritional management and developmental programming to optimize meat production. J Anim Sci Biotechnol. 2023;14(1):2. http://dx.doi.org/10.1186/s40104-022-00805-0. PMid:36597116.
 


Submitted date:
05/26/2023

Accepted date:
07/18/2023

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