Paternal Impact on the Developmental Programming of Sexual Dimorphism

Overview

Journal Front Cell Dev Biol

Specialty Cell Biology

Date 2024 Dec 23

PMID 39712575

Authors

Shefa M Aljabali

Shruta Pai

Raffaele Teperino

Affiliations

Soon will be listed here.

Abstract

Sexual dimorphism involves distinct anatomical, physiological, behavioral, and developmental differences between males and females of the same species, influenced by factors prior to conception and during early development. These sex-specific traits contribute to varied phenotypes and individual disease risks within and across generations and understanding them is essential in mammalian studies. Hormones, sex chromosomes, and imprinted genes drive this dimorphism, with over half of quantitative traits in wildtype mice showing sex-based variation. This review focuses on the impact of paternal non-genetic factors on sexual dimorphism. We synthesize current research on how paternal health before conception affects offspring phenotypes in a sex-specific manner, examining mechanisms such as DNA methylation, paternally imprinted genes, sperm RNA, and seminal plasma. Additionally, we explore how paternal influences indirectly shape offspring through maternal behavior, uterine environment, and placental changes, affecting males and females differently. We propose mechanisms modulating sexual dimorphism during development, underscoring the need for sex-specific documentation in animal studies.

References

Pinheiro I, Dejager L, Libert C . X-chromosome-located microRNAs in immunity: might they explain male/female differences? The X chromosome-genomic context may affect X-located miRNAs and downstream signaling, thereby contributing to the enhanced immune response of females. Bioessays. 2011; 33(11):791-802. DOI: 10.1002/bies.201100047. View

Thivisol U, Ho P, Li B, Trompke M, Hoffmann L, Hannan A . Paternal early life stress exerts intergenerational effects on male C57Bl/6J offspring risk-taking behaviors and predator scent-induced c-Fos expression. Neuronal Signal. 2023; 7(2):NS20220097. PMC: 10154287. DOI: 10.1042/NS20220097. View

Skuse D . Imprinting, the X-chromosome, and the male brain: explaining sex differences in the liability to autism. Pediatr Res. 2000; 47(1):9-16. DOI: 10.1203/00006450-200001000-00006. View

Billah M, Khatiwada S, Morris M, Maloney C . Effects of paternal overnutrition and interventions on future generations. Int J Obes (Lond). 2022; 46(5):901-917. PMC: 9050512. DOI: 10.1038/s41366-021-01042-7. View

Nohara K, Suzuki T, Okamura K . Gestational arsenic exposure and paternal intergenerational epigenetic inheritance. Toxicol Appl Pharmacol. 2020; 409:115319. DOI: 10.1016/j.taap.2020.115319. View

McCombe P, Greer J, Mackay I . Sexual dimorphism in autoimmune disease. Curr Mol Med. 2009; 9(9):1058-79. DOI: 10.2174/156652409789839116. View

Gregg C, Zhang J, Butler J, Haig D, Dulac C . Sex-specific parent-of-origin allelic expression in the mouse brain. Science. 2010; 329(5992):682-5. PMC: 2997643. DOI: 10.1126/science.1190831. View

Tucci V, Isles A, Kelsey G, Ferguson-Smith A . Genomic Imprinting and Physiological Processes in Mammals. Cell. 2019; 176(5):952-965. DOI: 10.1016/j.cell.2019.01.043. View

Ma J, Malladi S, Beck A . Systematic Analysis of Sex-Linked Molecular Alterations and Therapies in Cancer. Sci Rep. 2016; 6:19119. PMC: 4709570. DOI: 10.1038/srep19119. View

10.

Cisse Y, Chan J, Nugent B, Banducci C, Bale T . Brain and placental transcriptional responses as a readout of maternal and paternal preconception stress are fetal sex specific. Placenta. 2020; 100:164-170. PMC: 7525040. DOI: 10.1016/j.placenta.2020.06.019. View

11.

Lempradl A . Germ cell-mediated mechanisms of epigenetic inheritance. Semin Cell Dev Biol. 2019; 97:116-122. DOI: 10.1016/j.semcdb.2019.07.012. View

12.

Avner P, Heard E . X-chromosome inactivation: counting, choice and initiation. Nat Rev Genet. 2001; 2(1):59-67. DOI: 10.1038/35047580. View

13.

Morgan H, Paganopoulou P, Akhtar S, Urquhart N, Philomin R, Dickinson Y . Paternal diet impairs F1 and F2 offspring vascular function through sperm and seminal plasma specific mechanisms in mice. J Physiol. 2019; 598(4):699-715. DOI: 10.1113/JP278270. View

14.

Zeender V, Sbilordo S, Roy J, Lupold S . Paternal condition affects offspring reproduction and life history in a sex-specific manner in Drosophila melanogaster. Evolution. 2023; 77(2):467-481. DOI: 10.1093/evolut/qpac051. View

15.

Watkins A, Dias I, Tsuro H, Allen D, Emes R, Moreton J . Paternal diet programs offspring health through sperm- and seminal plasma-specific pathways in mice. Proc Natl Acad Sci U S A. 2018; 115(40):10064-10069. PMC: 6176621. DOI: 10.1073/pnas.1806333115. View

16.

Froberg J, Yang L, Lee J . Guided by RNAs: X-inactivation as a model for lncRNA function. J Mol Biol. 2013; 425(19):3698-706. PMC: 3771680. DOI: 10.1016/j.jmb.2013.06.031. View

17.

Cambiasso M, Gotfryd L, Stinson M, Birolo S, Salamone G, Romanato M . Paternal alcohol consumption has intergenerational consequences in male offspring. J Assist Reprod Genet. 2022; 39(2):441-459. PMC: 8956782. DOI: 10.1007/s10815-021-02373-0. View

18.

Reddy K, Oliver B . Sexual dimorphism in chronic respiratory diseases. Cell Biosci. 2023; 13(1):47. PMC: 9993607. DOI: 10.1186/s13578-023-00998-5. View

19.

Jalali Z, Bahrampour S, Khalili P, Khademalhosseini M, Nadimi A . Cohort-based analysis of paternal opioid use in relation to offspring's BMI and plasma lipid profile. Sci Rep. 2021; 11(1):9462. PMC: 8096835. DOI: 10.1038/s41598-021-88781-9. View

20.

Christians J . The Placenta's Role in Sexually Dimorphic Fetal Growth Strategies. Reprod Sci. 2021; 29(6):1895-1907. DOI: 10.1007/s43032-021-00780-3. View