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