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Table 1 Gene implicated in neurodevelopment and learning/memory abilities were differentially methylated in brain tissue of FA-D male offspring compared with the FA-N male offspring

From: Maternal folic acid impacts DNA methylation profile in male rat offspring implicated in neurodevelopment and learning/memory abilities

GO term (BP)

DMGs associated

Dorsal/ventral neural tube patterning

5 genes: Psen1 (hypermethylated), Gsc, Kif3a, Pax7, Ptch1 (hypomethylated)

Neural crest cell migration

14 genes: Pax6, Coro1c, Sema5a, Sema6d, Sema3b (hypermethylated), Ret, Efnb1, Kitlg, Isl1, Sox8, Sema6c, Sema7a, Gbx2, Sema4b (hypomethylated)

Brain development, hippocampus development, orbitofrontal cortex development, cerebellum development

59 genes: Fgfr1, Stk36, Hmgcs1, Pax6, Ptprs, Cdk5, Tp73, Bbs2, Casp3, Acat2, Cttnbp2, Ace, Ndrg4, Synj2, Ntf3, Gsx2, Ak2, Ager, Notch1, Psen1, Snrpb, Pygo2 (hypermethylated), Cast, Pfkfb3, Phlpp2, Lmx1a, Ogdh, Igf1r, Atp2b4, Akap5, Dclk2, Lhx5, Reln, Pafah1b1, Rara, Eif2b4, Fgfr2, Sstr1, Glud1, Gbx2, Sdf4, Rere, Dmrta2, Tmem57, Cxcr4, Sharpin, Unc5c, Irs2, Col4a1, Mdga1, Gabra5, Dpysl2, Pcdh19, Ddit4, Ptpn11, Hes5, Abcb1b, Ptch1, Cln5 (hypomethylated)

Neuron differentiation, neuron projection development, positive regulation of neuron projection development, negative regulation of neuron projection development, axonogenesis, negative regulation of axonogenesis, axon guidance, negative regulation of axon extension involved in axon guidance, axon regeneration, negative regulation of axon regeneration, negative regulation of dendrite development

112 genes: Wnt10a, Wnt5b, Cebpb, Fgfr1, Ncdn, Ager, Cdk5, Wnt7b, Cd44, Prkci, Kidins220, Fam134c, Nme2, Ndrg4, Ntrk1, Neu1, Tmem30a, Lrp1, Actb, Erbb3, Lrtm2, Flot1, Pax6, Slitrk2, Notch1, Gas7, Casp3, Sema5a, Sema6d, Sema3b, Dhfr, Folr1, Klk8, Fat3, Cyth2, Bag1, Psen1, Mbp, Ntf3, Kif5a, Etv1, B3gnt2 (hypermethylated), Ret, Sox11, Neurog1, Pld2, Ptprm, Vapa, Rb1, Itgb1, Pten, Uhmk1, Igf1r, Lingo1, App, Sema7a, Camsap1, Map4, Runx3, Arsb, Ltk, Katnb1, Ankrd1, Kif3c, Bcl11a, Ntrk2, Adamts1, Reln, Ngfr, Scarb2, Bag5, Mag, Fkbp4, Adcy5, Cspg4, Lrig2, Pafah1b1, Paqr3, Fgfr2, Adcy1, Atl1, Stk11, Nkx2-8, Lrrn3, Rtn4r, Ptpn11, Picalm, Lmx1a, Isl1, Ddit4, Wnt3, Kdm2a, Sema6c, Sema4b, Jak2, Ctnna1, Epha4, Arf6, Hes5, Ppia, Acsl4, Runx2, Wnt7a, Lrp4, Efna2, Efnb1, Dpysl2, Ttc8, Gbx2, Unc5c, Kif26a, Kif26b (hypomethylated)

Astrocyte differentiation, oligodendrocyte differentiation

11 genes: Notch1, S100b, Pax6, Bnip3, Cdk5 (hypermethylated), Hes5, Ptprj, Ntrk2, Olig1, Sox8, Nkx6-1 (hypomethylated)

Synapse organization

7 genes: Sncg, Wnt7b, Klk8 (hypermethylated), LRRTM1, Lmx1a, Wnt7a, Lrp4 (hypomethylated)

Synaptic transmission, glutamatergic, positive regulation of synaptic transmission, glutamatergic

13 genes: P2rx1, Cnih2, Grin2d, Grin1, Cdk5, Egfr, Cckbr, Ntrk1 (hypermethylated), Clcn3, Unc13b, Ntrk2, Reln, Ngfr (hypomethylated)

Learning or memory, memory, associative learning

29 genes: Egfr, Casp3, Sts, Psen1, S100b, Dyx1c1, Prkar1b, Ntrk1, Grin1, Abca7, Klk8, Cebpb, Paip2, Th, Nrgn, Cdk5 (hypermethylated), Pafah1b1, Pten, Igf2, Lmx1a, Itpr3, Sorcs3, Adrb1, Plk2, Reln, Chrnb2, Cacna1d, Gabra5, Neurod2 (hypomethylated)

  1. The MeDIP-Chip assay was performed on brain tissue from folic acid-deficient (FA-D) and folic acid-normal (FA-N) male offspring (n = 3/group). Enriched biological processes (BP) of GO terms by DAVID were used to identify the differentially methylated genes (DMGs) associated with neurodevelopment and learning/memory abilities