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. 2020 Apr 30;31(5):119–133. doi: 10.1007/s00335-020-09839-z

Table 1.

Studies in rodents examining diet-related effects and their epigenetic inheritance

Inheritance Species Nutritional exposure Exposed parent Analyzed generation Analyzed sex Inheritance lineage IVF Epigenetic mark References
F0 —> F1 F1 —> F2 F2 —> F3
In utero Rat LPD M F1 m + f M N Sayer et al. (2001)
Rat LPD M F0–F1 m M N Passos et al. (2000)
Rat CR M F0–F1 m + f M N Desai et al. (2007)
Mouse LPD M F1 m M N Crossland et al. (2017)
Mouse LPD M F1 m M N meDNA Balasa et al. (2011)
Rat LPD M F1 m M N Cavariani et al. (2019)
Rat LPD M F1 m M N Rodriguez-Gonzalez et al. (2014)
Rat LPD M F1 m M N Toledo et al. (2011)
Mouse CR M F1 m + f M N Jimenez-Chillaron et al. (2005)
Mouse HFD M F1 m + f M N meHistone, acHistone Masuyama and Hiramatsu (2012)
Rat HFD M + P F1 m P N Buckley et al. (2005)
Mouse HFD M F1 m M N meDNA Cannon et al. (2014)
Mouse HFD M F0–F1 m + f M N meDNA Ge et al. (2014)
Mouse Methyl supplementation M F1 m + f M N Wolff et al. (1998)
Mouse CR M F1 m M N meDNA, acHistone Zelko et al. (2019)
Rat CR M F1 m M N acHistone Zhu et al. (2016)
Intergenerational Mouse LPD P F1 m + f P N meDNA Carone et al. (2010)
Mouse CR M F1–F2 m M P N meDNA Radford et al. (2014)
Mouse CR M F1–F2 m + f M M, P, M + P N Jimenez-Chillaron et al. (2009)
Mouse CR M F1–F2 m + f M M, P, M + P N Kaczmarek et al. (2016)
Rat CR M F1–F2 m + f M M, P N Harper et al. (2014)
Mouse LPD P F0–F1 m P Y smallRNA Sharma et al. (2016)
Mouse HFD M F1–F2 f M M N meHistone, acHistone Masuyama et al. (2015)
Mouse HFD M F0–F2 m M M N Graus-Nunes et al. (2015)
Rat HFD M F0–F2 m + f M M N Huang et al. (2017)
Rat HFD P F0–F1 f P N meDNA Ng et al. (2010)
Rat HFD P F1 f P N Ng et al. (2014)
Mouse HFD P F0–F1 m P N Fullston et al. (2015)
Mouse HFD P F1 m + f P N meDNA Wei et al. (2014)
Mouse HFD M + P F0–F1 m + f M, P, M + P Y Huypens et al. (2016)
Mouse HFD M F0–F2 m + f M M, P, M + P N meDNA Dunn and Bale (2009)
Mouse  ± folic acid M F0–F2 m M P N meDNA Ly et al. (2017)
Rat Methyl depletion P F1 m P N McCoy et al. (2018)
Mouse Methyl supplementation M F0–F2 m + f M P N Cropley et al. (2006)
Mouse HFD M F1–F2 m + f M P Y tsRNAs Sarker et al. (2019)
Mouse HFD P F0–F1 m P N lncRNAs An et al. (2017)
Transgenerational Mouse LPD M F1–F3 m M M M N Frantz et al. (2011)
Rat CR M F1–F3 f M M M N Nowacka-Woszuk et al. (2018)
Rat LPD + CR M + P  > 50 generations m + f F0 —> F50 M + P N meHistone, acHistone Hardikar et al. (2015)
Mouse HFD M F3 m + f M P P N Dunn and Bale (2011)
Mouse HFD P F0–F3 m + f M P P Y meDNA Sarker et al. (2018)
Mouse HFD P F0–F2 m + f P M, P N meDNA Fullston et al. (2013)
Mouse HFD P F0–F2 m + f P M, P N Fullston et al. (2012)
Rat HFD P F0–F2 m + f P P N meDNA, sncRNAs de Castro et al.(2016)
Rat HFD P F2 f P P N de Castro et al. (2019)
Mouse HFD/HSD M F0–F3 m + f M P P Y Ferey et al. (2019)
Rat Vinclozolin M F0–F3 m M P P N acHistone, meDNA, sncRNA Ben Maamar et al. (2018)
Rat BPA M F1–F3 m + f M M + P M + P N meDNA Manikkam et al. (2013)
Rat BPA M F1–F3 m M P P N Salian et al. (2009)

Comprehensive overview of published studies that examine inter- and transgenerational inheritance of diet-related effects in rodent models and selection of studies of in utero effects

HFD high-fat diet, LPD isocaloric low protein diet, CR caloric restriction, BPA bisphenol A, HFD/HSD high-fat and high sugar diet, M maternal, P paternal, M + P parental, m males, f females, m + f males and females, Y yes, N no, meDNA DNA methylation, meHistone Histone methylation, acHistone Histone acetylation, sncRNA small non-coding RNA, tsRNA tRNA derived small RNA, lncRNA long non-coding RNA