Table 1.
Selection of studies providing evidence of transgenerational epigenetic inheritance in murine models.
| Author, year | Intervention | Species, generations investigated | Epigenetic marks studied | Technique(s) used |
|---|---|---|---|---|
| Carone et al., 2010 | Paternal low-protein diet before conception | Mouse, F0 + F1 | Sperm, F0: DNA methylation and small ncRNA Liver, F1: DNA methylation, small ncRNA |
Sperm, F0: MeDIP-seq, bisulfite seq, RNA microarray Liver, F1: DNA microarray, RRBS, bisulfite seq, HT-seq of miRNA |
| Radford et al., 2014 | Maternal caloric restriction during gestation (F0) | Mouse, (F0) + F1 + F2 | Sperm, F1: DNA Methylation Liver/brain, F2: DNA methylation |
Sperm, F1: MeDIP-seq, bisulfite pyrovateseq F2, liver/brain: Bisulfite pyrovateseq |
| de castro Barbosa et al., 2016 | Paternal high-fat diet before conception | Rat, F0+F1+F2 | Sperm, F0+F1+F2: DNA methylation, small ncRNA Metabolic tissues, F1+F2: small ncRNA |
Sperm, F0+F1+F2: MBD-seq, RNA-seq Metabolic tissue, F1+F2: RNA-seq |
| Dias & Ressler, 2014 | Paternal odor fear conditioning | Mouse, F0+F1+F2 Cross-fostering, IVF |
Sperm, F0+F1: DNA methylation, chromatin | Sperm, F0+F1: Bisulfite seq Sperm, F0: Native-ChIP Main olfactory epithelium, F1+F2: Bisulfite seq |
| Manikkam et al., 2013 | Maternal exposure to endocrine disruptors during gestation (F0) | Rat, F0+F1+F3 | Sperm, F3: DNA methylation | Sperm, F3: MeDIP-Chip |
| McPherson et al., 2015 | Paternal exposure to high-fat diet and/or exercise before conception | Mouse, F0+F1 | Sperm, F0: microRNA | Sperm, F0: MicroRNA Array |
| Wei et al., 2014 | Paternal high-fat diet + low-dose streptozodocin before conception | Mouse, F0+F1+F2 | Sperm, F0: DNA methylation Pancreas, F1: DNA methylation Pancreas, F2: DNA methylation |
Sperm, F0: MeDIP-Seq, bisulfite seq Pancreas, F1: MeDIP-Seq, bisulfite seq Pancreas, F2: MeDIP-qPCR |
| Gapp et al., 2014 | Paternal traumatic stress in early life | Mouse, F0+F1+F2 Microinjection of sperm RNA into ctrl zygotes |
Sperm, F0+F1+F2: Small ncRNA Brain + serum, F0+F1+F2: Small ncRNA |
RNA-seq (all tissues) |
| Sharma et al., 2016 | Paternal low-protein diet before ceonception | Mouse, F0+F1 IVF, ICSI/microinjection of specific RNA into ctrl zygote |
Sperm, epididymis, testis, F0: ncRNA Single embryo, F1: ncRNA |
Sperm, epididymis, testis F0: RNA-seq Single embryo, F1: RNA-seq |
| Chen et al., 2016 | Paternal high-fat diet before conception | Mouse, F0+F1 Microinjection of sperm head/total RNA/specific RNA into ctrl zygotes |
Sperm, F0: ncRNA Pancreas, embryo/blastocyst, F1: ncRNA, DNA methylation |
Sperm, F0: RNA-seq Pancreas, F1: RNA-seq, RRBS Single embryo/blastocyst: RNA-seq |
| Grandjean et al., 2009 | Microinjection of specific microRNA into ctrl zygotes | Mouse, Microinjection of specific microRNA into ctrl zygotes (F1)+F2+F3 | Embryo + adult tissue, F1: Specific microRNA, chromatin | Embryo + adult tissue, F1: RT-qPCR, ChIP |
| Wagner et al., 2008 | Microinjection of specific microRNA into ctrl zygotes | Mouse, Microinjection of specific microRNA into ctrl zygotes (F1) | F1, heart: Specific microRNA | Heart, F1: RT-qPCR |
| Cropley et al., 2016 | Paternal congenic obesity/pre-diabetes mouse model | Mouse, F0+F1+F2+F3 | Sperm, F1: ncRNA | Sperm, F1: RNA-seq |
| Grandjean et al., 2015 | Paternal high-fat/high-sugar diet before conception | Microinjection of testis and sperm total RNA/specific microRNA into ctrl zygotes (F1) | Testis, sperm, F0: ncRNA | Testis, F0: RNA-seq Testis, sperm, F0: RT-qPCR |
Seq = sequencing; MeDIP = Methylated DNA immunoprecipitation; RRBS = Reduced representative bisulfite sequencing; (RT-)qPCR: (reverse transcription) quantitative polymerase chain reaction; MBD = Methyl binding domain; ChIP: Chromatin immunoprecipitation.