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Table 2 Effects of prenatal exposure to famine on (epi)genome-wide DNA methylation of the offspring

From: The association between prenatal famine, DNA methylation and mental disorders: a systematic review and meta-analysis

References

Cohort

Sample description of groups with prenatal, non-prenatal or non-exposure

Chromosome

Gene

No. CpG

DNA methylation analysis from blood

Main results

Li et al. [65]

Chinese Famine*a

Prenatal exposure N = 79, ♀ = 49, mean age 57

–

–

–

Illumina

Infinium

Methylation

EPIC

BeadChip

No significant differences in DNA methylation (DMRs and CpGs) between prenatal exposure and non-exposure after controlling for multiple testing

Non-exposure N = 105, ♀ = 31, mean age 53

Jiang et al. [63]

Chinese Famine*a

Prenatal exposure N = 46, ♀ = 24, mean age 52

–

–

–

Illumina

Infinium

Human

Methylation

850 K

BeadChip

601 DMRs with significant* hypermethylation and 360 DMRs with significant* hypomethylation after prenatal exposure compared to time controls (for more details, see Fig. 1 in [63])

Time controls N = 46, ♀ = 24, mean age 53

He et al. [58]

Chinese Famine*a

Early prenatal exposure N = 25, ♀ = 15, mean age 50

chr3:48481268–48481793

CCDC51/TMA7

13

Illumina

Infinium

Human

Methylation

450 BeadChip

613 DMRs with significant methylation (significance and direction of effect not stated): specifically, hypomethylation of CCDC51/TMA7***, ENO2*** and ZNF226** after early prenatal exposure compared to non-exposure

Non-exposure N = 54, ♀ = 33, mean age 47

chr12:7023752–7024121

ENO2

4

 

chr19:44669146–44669354

ZNF226

5

Tobi et al. [64]d

Dutch Famine*b

Prenatal exposure N = 348, ♀ = 188, mean age 59

chr21:43655316

ABCG1

1

Illumina

Infinium

Human

Methylation

450 BeadChip

Of 342,596 CpGs, 17 CpGs with significant differences in methylation between prenatal exposure and sibling controls: hypermethylation of ABCG1**, CCDC155***, FAM150B***, METTL8*, PNPO***, PPAP2C***, SLC38A2***, SYNGR1**, TACC1*** and ZNF385A*** and hypomethylation of CRELD2**, LRRC8D***, LOC100132354***, OSBPL5/MRGPRG***, TXNIP** and PFKFB3*

chr19:49891270

CCDC155

1

Sibling controls N = 463, ♀ = 264, mean age 58

chr19:49891574

CCDC155

1

chr22:50327986

CRELD2

1

chr2:366113

FAM150B

1

chr6:43894639

LOC100132354

1

chr1:90288099

LRRC8D

1

chr2:172203847

METTL8

1

chr11:3225076

OSBPL5/MRGPRG

1

chr10:6214026

PFKFB3

1

chr17:46022809

PNPO

1

chr19:292167

PPAP2C

1

chr12:46737123

SLC38A2

1

chr22:39759864

SYNGR1

1

chr1:145441552

TXNIP

1

chr8:38586183

TACC1

1

chr12:54764265

ZNF385A

1

Finer et al. [59]

Bangladesh Famine*c

Prenatal exposure N = 40

Non-prenatal exposure N = 49

Non-exposure N = 54

–

–

–

Illumina

Infinium

Human

Methylation

450 BeadChip

No significant differences in DNA methylation between prenatal exposure, non-prenatal exposure and non-exposure

Tobi et al. [60]d

Dutch Famine*b

Prenatal exposure during any week N = 348, ♀ = 188, mean age 59; conception N = 74, ♀ not stated; weeks 1–10 = 73, ♀ = 39; weeks 11–20 = 123, ♀ = 66; weeks 21–30 = 143, ♀ = 72; weeks 31-delivery = 128, ♀ = 66

chr2:366113

FAM150B/TMEM18

1

Illumina

Infinium

Human

Methylation

450 BeadChip

Hypomethylation of TMEM105/SLC38A10* after exposure during conception compared to time and sibling controls; hypermethylation of FAM150B/TMEM18**, PPAP2C*, SLC38A2** and hypomethylation of OSBPL5/ MRGPRG* after exposure during weeks 1–10 compared to time and sibling controls; hypermethylation of ZNF385A* and TACC1* after exposure during any week compared to time and sibling controls

chr11:3225076

OSBPL5/MRGPRG

1

chr19:292167

PPAP2C

1

chr12:46737123

SLC38A2

1

chr8:38586183

TACC1

1

chr17:79283915

TMEM105/SLC38A10

1

chr12:54764265

ZNF385A

1

Time controls N = 160, ♀ = 88, mean age 59

   

Sibling controls N = 303, ♀ = 176, mean age 57

   

Tobi et al. [61]

Dutch Famine*b

Periconceptional exposure N = 24, ♀ = 12, mean age 58

–

–

–

RRBS

181 DMRs with 60.8% significantly hypermethylated and 39.2% hypomethylated after periconceptional exposure compared to sibling controls (for more details and significance see S1 in [61])

Sibling controls N = 24, ♀ = 12, mean age 57

Tobi et al. [66]

Dutch Famine*b

Periconceptional exposure N = 60, ♀ = 32, mean age 58

–

LINE-1e

–

Pyrosequencing

No significant difference in global DNA methylation between periconceptional exposure and sibling controls

Sibling controls N = 60, ♀ = 32, mean age 57

Lumey et al. [62]

Dutch Famine*b

Prenatal exposure N = 350, ♀ = 189, mean age 59

chr17

Sat2

–

MethyLight

No significant differences in global DNA methylation between prenatal exposure and time and sibling controls

Time controls N = 290, ♀ = 154, mean age 59

–

LINE-1e

 

Pyrosequencing

Sibling controls N = 307, ♀ = 175, mean age 57

   

LUMA

  1. *aChinese Famine: 1959–1961, *bDutch Famine: 1944–1945; *cBangladesh Famine: 1974–1975, dsample overlap between [60, 64], eestimate of global methylation; ABCG1 ATP Binding Cassette Subfamily G Member 1, CCDC51 Coiled-Coil Domain Containing 51, CCDC155 Coiled-Coil Domain Containing 155, CRELD2 Cysteine Rich with EGF-Like Domains 2, DMR Differentially Methylated Region, ENO2 Enolase 2, FAM150B Family with sequence similarity 150 member B, LINE-1 Long interspersed nucleotide element-1, LOC100132354 LOC100132354, LRRC8D Leucine Rich Repeat Containing 8 VRAC Subunit D, LUMA Luminometric methylation assay, METTL8 Methyltransferase 8, MRGPRG MAS-related GPR family member G, OSBPL5 Oxysterol binding protein-like 5, PFKFB3 6-Phosphofructo-2-Kinase/Fructose-2,6-Biphosphatase 3, PNPO Pyridoxamine 5′-Phosphate Oxidase, PPAP2C Phosphatidic acid phosphatase 2c, RRBS Reduced representation bisulfite sequencing, Sat2 Satellite repeat-2, SLC38A2 Solute carrier family 38 member 2, SLC38A10 Solute Carrier Family 38 Member 10, SYNGR1 Synaptogyrin 1, TACC1 Transforming Acidic Coiled-Coil Containing Protein 1, TMA7 Translation machinery-associated protein 7, TMEM18 Transmembrane protein 18, TMEM105 TMEM105 long non-coding RNA, TXNIP Thioredoxin Interacting Protein, ZNF226 Zinc finger protein 226, ZNF385A Zinc finger protein 385A; *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001
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Clinical Epigenetics

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