Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content - PubMed (original) (raw)
. 2013 Oct;27(10):4226-43.
doi: 10.1096/fj.12-224048. Epub 2013 Jul 11.
Affiliations
- PMID: 23845863
- DOI: 10.1096/fj.12-224048
Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content
Tod Fullston et al. FASEB J. 2013 Oct.
Abstract
Obesity is highly prevalent, and its incidence is increasing. The previous study showing a major effect of paternal obesity on metabolic health of offspring is confounded by comorbidity with diabetes. Therefore, we investigated the effect of diet-induced paternal obesity, in the absence of diabetes, on the metabolic health of two resultant generations and the molecular profiles of the testes and sperm. Founder (F0) male C57BL6 mice were fed either a high-fat diet (HFD) or a control diet (CD); n = 10/diet for a period of 10 wk. Testis expression of mRNA/microRNAs was analyzed by microarray and qPCR and sperm microRNA abundance by qPCR. Two subsequent generations were generated by mating F0 and then F1 mice to CD mice, and their metabolic health was investigated. All mice, other than F0 males, were maintained on a CD. HFD feeding induced paternal obesity with a 21% increase in adiposity, but not overt diabetes, and initiated intergenerational transmission of obesity and insulin resistance in two generations of offspring. This distinct phenotypic constellation is either partially or fully transmitted to both female and male F1 offspring and further transmitted through both parental lineages to the F2 generation, with a heightened effect on female F1 offspring (+67% in adiposity) and their F2 sons (+24% in adiposity). Founder male obesity altered the testes expression of 414 mRNAs by microarray and 11 microRNAs by qPCR, concomitant with alterations in sperm microRNA content and a 25% reduction in global methylation of germ cell DNA. Diet-induced paternal obesity modulates sperm microRNA content and germ cell methylation status, which are potential signals that program offspring health and initiate the transmission of obesity and impaired metabolic health to future generations. This study implicates paternal obesity in the transgenerational amplification of obesity and type 2 diabetes in humans.
Keywords: DNA damage; ROS; epigenetic alteration; methylation; nongenetic transmission.
Comment in
- Obesity: Effects of paternal obesity.
Wilson C. Wilson C. Nat Rev Endocrinol. 2013 Oct;9(10):565. doi: 10.1038/nrendo.2013.152. Epub 2013 Jul 30. Nat Rev Endocrinol. 2013. PMID: 23897172 No abstract available.
Similar articles
- Sperm microRNA Content Is Altered in a Mouse Model of Male Obesity, but the Same Suite of microRNAs Are Not Altered in Offspring's Sperm.
Fullston T, Ohlsson-Teague EM, Print CG, Sandeman LY, Lane M. Fullston T, et al. PLoS One. 2016 Nov 4;11(11):e0166076. doi: 10.1371/journal.pone.0166076. eCollection 2016. PLoS One. 2016. PMID: 27814400 Free PMC article. - Diet-induced obesity leads to metabolic dysregulation in offspring via endoplasmic reticulum stress in a sex-specific manner.
Park JH, Yoo Y, Cho M, Lim J, Lindroth AM, Park YJ. Park JH, et al. Int J Obes (Lond). 2018 Feb;42(2):244-251. doi: 10.1038/ijo.2017.203. Epub 2017 Aug 16. Int J Obes (Lond). 2018. PMID: 28811650 - Sperm histone H3 lysine 4 tri-methylation serves as a metabolic sensor of paternal obesity and is associated with the inheritance of metabolic dysfunction.
Pepin AS, Lafleur C, Lambrot R, Dumeaux V, Kimmins S. Pepin AS, et al. Mol Metab. 2022 May;59:101463. doi: 10.1016/j.molmet.2022.101463. Epub 2022 Feb 17. Mol Metab. 2022. PMID: 35183795 Free PMC article. - Paternal obesity, interventions, and mechanistic pathways to impaired health in offspring.
McPherson NO, Fullston T, Aitken RJ, Lane M. McPherson NO, et al. Ann Nutr Metab. 2014;64(3-4):231-8. doi: 10.1159/000365026. Epub 2014 Oct 2. Ann Nutr Metab. 2014. PMID: 25300265 Review. - Diet-Induced Modification of the Sperm Epigenome Programs Metabolism and Behavior.
Bodden C, Hannan AJ, Reichelt AC. Bodden C, et al. Trends Endocrinol Metab. 2020 Feb;31(2):131-149. doi: 10.1016/j.tem.2019.10.005. Epub 2019 Nov 16. Trends Endocrinol Metab. 2020. PMID: 31744784 Review.
Cited by
- N-acetyl-L-cysteine reduces testis ROS in obese fathers but fails in protecting offspring from acquisition of epigenetic traits at cyp19a1 and IGF11/H19 ICR loci.
Pastore A, Badolati N, Manfrevola F, Sagliocchi S, Laurenzi V, Musto G, Porreca V, Murolo M, Chioccarelli T, Ciampaglia R, Vellecco V, Bucci M, Dentice M, Cobellis G, Stornaiuolo M. Pastore A, et al. Front Cell Dev Biol. 2024 Oct 18;12:1450580. doi: 10.3389/fcell.2024.1450580. eCollection 2024. Front Cell Dev Biol. 2024. PMID: 39493346 Free PMC article. - Obesity in children: inheritance and treatment - state of art 2024.
Wójcik M, Zachurzok A. Wójcik M, et al. Pediatr Endocrinol Diabetes Metab. 2024;30(3):112-115. doi: 10.5114/pedm.2024.144042. Pediatr Endocrinol Diabetes Metab. 2024. PMID: 39451183 Free PMC article. No abstract available. - Relationship between paternal excessive weight and neonatal anthropometry in a clinical trial of nutritional counseling for pregnant women with overweight.
Carvalho MR, Miranda DEGA, Baroni NF, Santos IDS, Carreira NP, Crivellenti LC, Sartorelli DS. Carvalho MR, et al. Int J Obes (Lond). 2024 Sep 24. doi: 10.1038/s41366-024-01639-8. Online ahead of print. Int J Obes (Lond). 2024. PMID: 39317700 - Multifaceted paternal exposures before conception and their epigenetic impact on offspring.
Wu X, Zhang W, Chen H, Weng J. Wu X, et al. J Assist Reprod Genet. 2024 Sep 4. doi: 10.1007/s10815-024-03243-1. Online ahead of print. J Assist Reprod Genet. 2024. PMID: 39230664 Review. - Paternal high-fat diet affects weight and DNA methylation of their offspring.
Haberman M, Menashe T, Cohen N, Kisliouk T, Yadid T, Marco A, Meiri N, Weller A. Haberman M, et al. Sci Rep. 2024 Aug 27;14(1):19874. doi: 10.1038/s41598-024-70438-y. Sci Rep. 2024. PMID: 39191806 Free PMC article.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical
Miscellaneous