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Differential DNA methylation of steatosis and non-alcoholic fatty liver disease in adolescence

Differential DNA methylation of steatosis and non-alcoholic fatty liver disease in adolescence
Differential DNA methylation of steatosis and non-alcoholic fatty liver disease in adolescence
Background and aims: Epigenetic modifications are associated with hepatic fat accumulation and non-alcoholic fatty liver disease (NAFLD). However, few epigenetic modifications directly implicated in such processes have been identified during adolescence, a critical developmental window where physiological changes could influence future disease trajectory. To investigate the association between DNA methylation and NAFLD in adolescence, we undertook discovery and validation of novel methylation marks, alongside replication of previously reported marks.
Approach and results: We performed a DNA methylation epigenome-wide association study (EWAS) on DNA from whole blood from 707 Raine Study adolescents phenotyped for steatosis score and NAFLD by ultrasound at age 17. Next, we performed pyrosequencing validation of loci within the most 100 strongly associated differentially methylated CpG sites (dmCpGs) for which ≥ 2 probes per gene remained significant across four statistical models with a nominal p value < 0.007. EWAS identified dmCpGs related to three genes (ANK1, MIR10a, PTPRN2) that met our criteria for pyrosequencing. Of the dmCpGs and surrounding loci that were pyrosequenced (ANK1 n = 6, MIR10a n = 7, PTPRN2 n = 3), three dmCpGs in ANK1 and two in MIR10a were significantly associated with NAFLD in adolescence. After adjustment for waist circumference only dmCpGs in ANK1 remained significant. These ANK1 CpGs were also associated with γ-glutamyl transferase and alanine aminotransferase concentrations. Three of twenty-two differentially methylated dmCpGs previously associated with adult NAFLD were associated with NAFLD in adolescence (all adjusted p < 2.3 × 10–3).
Conclusions: We identified novel DNA methylation loci associated with NAFLD and serum liver biochemistry markers during adolescence, implicating putative dmCpG/gene regulatory pathways and providing insights for future mechanistic studies
ANK1, EWAS, Epigenetics, MIR10A, PTPRN2
1936-0533
584-594
Melton, Phillip E.
0d57b167-a10c-4b22-83da-b983f378966f
Burton, Mark
250319ad-90dc-4651-b118-d5dbe5eaafa6
Lillycrop, Karen
eeaaa78d-0c4d-4033-a178-60ce7345a2cc
Godfrey, Keith
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Rauschert, Sebastian
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Anderson, D
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Burdge, Graham
09d60a07-8ca1-4351-9bf1-de6ffcfb2159
Mori, Trevor A.
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Beilin, L. J.
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Ayonrinde, O.T.
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Craig, J.M.
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Olynyk, J K
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Holbrook, Joanna D
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Pennell, Craig E.
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Oddy, Wendy H.
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Moses, E. K.
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Adams, L.A.
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Huang, Rae-Chi
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et al.
Melton, Phillip E.
0d57b167-a10c-4b22-83da-b983f378966f
Burton, Mark
250319ad-90dc-4651-b118-d5dbe5eaafa6
Lillycrop, Karen
eeaaa78d-0c4d-4033-a178-60ce7345a2cc
Godfrey, Keith
0931701e-fe2c-44b5-8f0d-ec5c7477a6fd
Rauschert, Sebastian
4d4cf3e0-3a95-4223-a49c-c3c5227785d0
Anderson, D
134fe9be-6af5-41bc-aa2e-0ebae9e0395f
Burdge, Graham
09d60a07-8ca1-4351-9bf1-de6ffcfb2159
Mori, Trevor A.
182e02e5-0b4a-44c2-81c6-f910c7a4d0e6
Beilin, L. J.
7728e5b8-3049-4273-bb16-d4f95088d91a
Ayonrinde, O.T.
25789c5f-d3d6-438d-8aa8-e3577df5c0df
Craig, J.M.
34883fb4-710b-4ee4-8a43-2a53ed92b825
Olynyk, J K
66ef4ef6-2011-4a93-8201-ee708daba6d5
Holbrook, Joanna D
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Pennell, Craig E.
4edfcf23-0f2c-4b30-bdff-af57116d673c
Oddy, Wendy H.
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Moses, E. K.
250e5ac7-f82a-4375-8bfc-dbb815f2660f
Adams, L.A.
2be50723-3824-4a3d-829e-678b47a98564
Huang, Rae-Chi
d39aca4d-8017-48c3-8f40-0aa2e52dbf66

Melton, Phillip E., Burton, Mark, Lillycrop, Karen, Godfrey, Keith, Burdge, Graham and Holbrook, Joanna D , et al. (2023) Differential DNA methylation of steatosis and non-alcoholic fatty liver disease in adolescence. Hepatology International, 17 (3), 584-594. (doi:10.1007/s12072-022-10469-7).

Record type: Article

Abstract

Background and aims: Epigenetic modifications are associated with hepatic fat accumulation and non-alcoholic fatty liver disease (NAFLD). However, few epigenetic modifications directly implicated in such processes have been identified during adolescence, a critical developmental window where physiological changes could influence future disease trajectory. To investigate the association between DNA methylation and NAFLD in adolescence, we undertook discovery and validation of novel methylation marks, alongside replication of previously reported marks.
Approach and results: We performed a DNA methylation epigenome-wide association study (EWAS) on DNA from whole blood from 707 Raine Study adolescents phenotyped for steatosis score and NAFLD by ultrasound at age 17. Next, we performed pyrosequencing validation of loci within the most 100 strongly associated differentially methylated CpG sites (dmCpGs) for which ≥ 2 probes per gene remained significant across four statistical models with a nominal p value < 0.007. EWAS identified dmCpGs related to three genes (ANK1, MIR10a, PTPRN2) that met our criteria for pyrosequencing. Of the dmCpGs and surrounding loci that were pyrosequenced (ANK1 n = 6, MIR10a n = 7, PTPRN2 n = 3), three dmCpGs in ANK1 and two in MIR10a were significantly associated with NAFLD in adolescence. After adjustment for waist circumference only dmCpGs in ANK1 remained significant. These ANK1 CpGs were also associated with γ-glutamyl transferase and alanine aminotransferase concentrations. Three of twenty-two differentially methylated dmCpGs previously associated with adult NAFLD were associated with NAFLD in adolescence (all adjusted p < 2.3 × 10–3).
Conclusions: We identified novel DNA methylation loci associated with NAFLD and serum liver biochemistry markers during adolescence, implicating putative dmCpG/gene regulatory pathways and providing insights for future mechanistic studies

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Accepted/In Press date: 11 December 2022
e-pub ahead of print date: 3 February 2023
Published date: 1 June 2023
Additional Information: The DNA methylation supported by National and Medical Research Council (NHMRC) Australia grant 1059711. The Raine Study Gen2-17 follow-up supported by NHMRC Program grant (#353514) and Project grant (#403981). Ultrasound assessment was supported by grants from the Fremantle Hospital Research Foundation and the Gastroenterology Society of Australia. R.C.H. and T.A.M. are supported by NHMRC Fellowships (grant #1053384 and #1136046, respectively). SR is supported by NHMRC-EU grant (#1142858) and the Department of Health, Western Australia FutureHealth fund in connection with the European Union's Horizon2020 grant (#733206). K.M.G. is supported by the UK Medical Research Council (MC_UU_12011/4), the National Institute for Health Research (NIHR Senior Investigator (NF-SI-0515–10042) and the NIHR Southampton Biomedical Research Centre)
Keywords: ANK1, EWAS, Epigenetics, MIR10A, PTPRN2

Identifiers

Local EPrints ID: 474099
URI: http://eprints.soton.ac.uk/id/eprint/474099
ISSN: 1936-0533
PURE UUID: 3da345b1-8adc-4185-9703-54a49a86229f
ORCID for Mark Burton: ORCID iD orcid.org/0000-0002-7117-8151
ORCID for Karen Lillycrop: ORCID iD orcid.org/0000-0001-7350-5489
ORCID for Keith Godfrey: ORCID iD orcid.org/0000-0002-4643-0618
ORCID for Graham Burdge: ORCID iD orcid.org/0000-0002-7665-2967
ORCID for Joanna D Holbrook: ORCID iD orcid.org/0000-0003-1791-6894

Catalogue record

Date deposited: 13 Feb 2023 18:07
Last modified: 17 Aug 2024 01:52

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Contributors

Author: Phillip E. Melton
Author: Mark Burton ORCID iD
Author: Karen Lillycrop ORCID iD
Author: Keith Godfrey ORCID iD
Author: Sebastian Rauschert
Author: D Anderson
Author: Graham Burdge ORCID iD
Author: Trevor A. Mori
Author: L. J. Beilin
Author: O.T. Ayonrinde
Author: J.M. Craig
Author: J K Olynyk
Author: Joanna D Holbrook ORCID iD
Author: Craig E. Pennell
Author: Wendy H. Oddy
Author: E. K. Moses
Author: L.A. Adams
Author: Rae-Chi Huang
Corporate Author: et al.

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