Epigenome-wide association meta-analysis of DNA methylation with coffee and tea consumption

Irma Karabegovic; Eliana Portilla-Fernandez; Yang Li; Jiantao Ma; Silvana C. E. Maas; Daokun Sun; Emily A. Hu; Brigitte Kuhnel; Yan Zhang; Srikant Ambatipudi; Giovanni Fiorito; Jian Huang; Juan E. Castillo-Fernandez; Kerri L. Wiggins; Niek de Klein; Sara Grioni; Brenton R. Swenson; Silvia Polidoro; Jorien L. Treur; Cyrille Cuenin; Pei-Chien Tsai; Ricardo Costeira; Veronique Chajes; Kim Braun; Niek Verweij; Anja Kretschmer; Lude Franke; Joyce B. J. van Meurs; Andre G. Uitterlinden; Robert J. de Knegt; M. Arfan Ikram; Abbas Dehghan; Annette Peters; Ben Schottker; Sina A. Gharib; Nona Sotoodehnia; Jordana T. Bell; Paul Elliott; Paolo Vineis; Caroline Relton; Zdenko Herceg; Hermann Brenner; Melanie Waldenberger; Casey M. Rebholz; Trudy Voortman; Qiuwei Pan; Myriam Fornage; Daniel Levy; Manfred Kayser; Mohsen Ghanbari

doi:10.1038/s41467-021-22752-6

Epigenome-wide association meta-analysis of DNA methylation with coffee and tea consumption

Irma Karabegovic, Eliana Portilla-Fernandez, Yang Li, Jiantao Ma, Silvana C. E. Maas, Daokun Sun, Emily A. Hu, Brigitte Kuhnel, Yan Zhang, Srikant Ambatipudi, Giovanni Fiorito, Jian Huang, Juan E. Castillo-Fernandez, Kerri L. Wiggins, Niek de Klein, Sara Grioni, Brenton R. Swenson, Silvia Polidoro, Jorien L. Treur, Cyrille CueninPei-Chien Tsai, Ricardo Costeira, Veronique Chajes, Kim Braun, Niek Verweij, Anja Kretschmer, Lude Franke, Joyce B. J. van Meurs, Andre G. Uitterlinden, Robert J. de Knegt, M. Arfan Ikram, Abbas Dehghan, Annette Peters, Ben Schottker, Sina A. Gharib, Nona Sotoodehnia, Jordana T. Bell, Paul Elliott, Paolo Vineis, Caroline Relton, Zdenko Herceg, Hermann Brenner, Melanie Waldenberger, Casey M. Rebholz, Trudy Voortman, Qiuwei Pan, Myriam Fornage, Daniel Levy, Manfred Kayser, Mohsen Ghanbari^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

Coffee and tea are extensively consumed beverages worldwide which have received considerable attention regarding health. Intake of these beverages is consistently linked to, among others, reduced risk of diabetes and liver diseases; however, the mechanisms of action remain elusive. Epigenetics is suggested as a mechanism mediating the effects of dietary and lifestyle factors on disease onset. Here we report the results from epigenome-wide association studies (EWAS) on coffee and tea consumption in 15,789 participants of European and African-American ancestries from 15 cohorts. EWAS meta-analysis of coffee consumption reveals 11 CpGs surpassing the epigenome-wide significance threshold (P-value <1.1×10-7), which annotated to the AHRR, F2RL3, FLJ43663, HDAC4, GFI1 and PHGDH genes. Among them, cg14476101 is significantly associated with expression of the PHGDH and risk of fatty liver disease. Knockdown of PHGDH expression in liver cells shows a correlation with expression levels of genes associated with circulating lipids, suggesting a role of PHGDH in hepatic-lipid metabolism. EWAS meta-analysis on tea consumption reveals no significant association, only two CpGs annotated to CACNA1A and PRDM16 genes show suggestive association (P-value <5.0×10-6). These findings indicate that coffee-associated changes in DNA methylation levels may explain the mechanism of action of coffee consumption in conferring risk of diseases.

Original language	English
Article number	2830
Number of pages	13
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-22752-6
Publication status	Published - 14-May-2021

Keywords

POLYCYCLIC AROMATIC-HYDROCARBONS
ACTIVATED RECEPTOR 4
MENDELIAN RANDOMIZATION
EPIGENETICS
RISK
POPULATION
CAFFEINE
DISEASE
DESIGN
CANCER

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Karabegovic, I., Portilla-Fernandez, E., Li, Y., Ma, J., Maas, S. C. E., Sun, D., Hu, E. A., Kuhnel, B., Zhang, Y., Ambatipudi, S., Fiorito, G., Huang, J., Castillo-Fernandez, J. E., Wiggins, K. L., de Klein, N., Grioni, S., Swenson, B. R., Polidoro, S., Treur, J. L., ... Ghanbari, M. (2021). Epigenome-wide association meta-analysis of DNA methylation with coffee and tea consumption. Nature Communications, 12(1), [2830]. https://doi.org/10.1038/s41467-021-22752-6

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title = "Epigenome-wide association meta-analysis of DNA methylation with coffee and tea consumption",

abstract = "Coffee and tea are extensively consumed beverages worldwide which have received considerable attention regarding health. Intake of these beverages is consistently linked to, among others, reduced risk of diabetes and liver diseases; however, the mechanisms of action remain elusive. Epigenetics is suggested as a mechanism mediating the effects of dietary and lifestyle factors on disease onset. Here we report the results from epigenome-wide association studies (EWAS) on coffee and tea consumption in 15,789 participants of European and African-American ancestries from 15 cohorts. EWAS meta-analysis of coffee consumption reveals 11 CpGs surpassing the epigenome-wide significance threshold (P-value <1.1×10-7), which annotated to the AHRR, F2RL3, FLJ43663, HDAC4, GFI1 and PHGDH genes. Among them, cg14476101 is significantly associated with expression of the PHGDH and risk of fatty liver disease. Knockdown of PHGDH expression in liver cells shows a correlation with expression levels of genes associated with circulating lipids, suggesting a role of PHGDH in hepatic-lipid metabolism. EWAS meta-analysis on tea consumption reveals no significant association, only two CpGs annotated to CACNA1A and PRDM16 genes show suggestive association (P-value <5.0×10-6). These findings indicate that coffee-associated changes in DNA methylation levels may explain the mechanism of action of coffee consumption in conferring risk of diseases.",

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author = "Irma Karabegovic and Eliana Portilla-Fernandez and Yang Li and Jiantao Ma and Maas, {Silvana C. E.} and Daokun Sun and Hu, {Emily A.} and Brigitte Kuhnel and Yan Zhang and Srikant Ambatipudi and Giovanni Fiorito and Jian Huang and Castillo-Fernandez, {Juan E.} and Wiggins, {Kerri L.} and {de Klein}, Niek and Sara Grioni and Swenson, {Brenton R.} and Silvia Polidoro and Treur, {Jorien L.} and Cyrille Cuenin and Pei-Chien Tsai and Ricardo Costeira and Veronique Chajes and Kim Braun and Niek Verweij and Anja Kretschmer and Lude Franke and {van Meurs}, {Joyce B. J.} and Uitterlinden, {Andre G.} and {de Knegt}, {Robert J.} and Ikram, {M. Arfan} and Abbas Dehghan and Annette Peters and Ben Schottker and Gharib, {Sina A.} and Nona Sotoodehnia and Bell, {Jordana T.} and Paul Elliott and Paolo Vineis and Caroline Relton and Zdenko Herceg and Hermann Brenner and Melanie Waldenberger and Rebholz, {Casey M.} and Trudy Voortman and Qiuwei Pan and Myriam Fornage and Daniel Levy and Manfred Kayser and Mohsen Ghanbari",

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Karabegovic, I, Portilla-Fernandez, E, Li, Y, Ma, J, Maas, SCE, Sun, D, Hu, EA, Kuhnel, B, Zhang, Y, Ambatipudi, S, Fiorito, G, Huang, J, Castillo-Fernandez, JE, Wiggins, KL, de Klein, N, Grioni, S, Swenson, BR, Polidoro, S, Treur, JL, Cuenin, C, Tsai, P-C, Costeira, R, Chajes, V, Braun, K, Verweij, N, Kretschmer, A, Franke, L, van Meurs, JBJ, Uitterlinden, AG, de Knegt, RJ, Ikram, MA, Dehghan, A, Peters, A, Schottker, B, Gharib, SA, Sotoodehnia, N, Bell, JT, Elliott, P, Vineis, P, Relton, C, Herceg, Z, Brenner, H, Waldenberger, M, Rebholz, CM, Voortman, T, Pan, Q, Fornage, M, Levy, D, Kayser, M & Ghanbari, M 2021, 'Epigenome-wide association meta-analysis of DNA methylation with coffee and tea consumption', Nature Communications, vol. 12, no. 1, 2830. https://doi.org/10.1038/s41467-021-22752-6

TY - JOUR

T1 - Epigenome-wide association meta-analysis of DNA methylation with coffee and tea consumption

AU - Karabegovic, Irma

AU - Portilla-Fernandez, Eliana

AU - Li, Yang

AU - Ma, Jiantao

AU - Maas, Silvana C. E.

AU - Sun, Daokun

AU - Hu, Emily A.

AU - Kuhnel, Brigitte

AU - Zhang, Yan

AU - Ambatipudi, Srikant

AU - Fiorito, Giovanni

AU - Huang, Jian

AU - Castillo-Fernandez, Juan E.

AU - Wiggins, Kerri L.

AU - de Klein, Niek

AU - Grioni, Sara

AU - Swenson, Brenton R.

AU - Polidoro, Silvia

AU - Treur, Jorien L.

AU - Cuenin, Cyrille

AU - Tsai, Pei-Chien

AU - Costeira, Ricardo

AU - Chajes, Veronique

AU - Braun, Kim

AU - Verweij, Niek

AU - Kretschmer, Anja

AU - Franke, Lude

AU - van Meurs, Joyce B. J.

AU - Uitterlinden, Andre G.

AU - de Knegt, Robert J.

AU - Ikram, M. Arfan

AU - Dehghan, Abbas

AU - Peters, Annette

AU - Schottker, Ben

AU - Gharib, Sina A.

AU - Sotoodehnia, Nona

AU - Bell, Jordana T.

AU - Elliott, Paul

AU - Vineis, Paolo

AU - Relton, Caroline

AU - Herceg, Zdenko

AU - Brenner, Hermann

AU - Waldenberger, Melanie

AU - Rebholz, Casey M.

AU - Voortman, Trudy

AU - Pan, Qiuwei

AU - Fornage, Myriam

AU - Levy, Daniel

AU - Kayser, Manfred

AU - Ghanbari, Mohsen

PY - 2021/5/14

Y1 - 2021/5/14

N2 - Coffee and tea are extensively consumed beverages worldwide which have received considerable attention regarding health. Intake of these beverages is consistently linked to, among others, reduced risk of diabetes and liver diseases; however, the mechanisms of action remain elusive. Epigenetics is suggested as a mechanism mediating the effects of dietary and lifestyle factors on disease onset. Here we report the results from epigenome-wide association studies (EWAS) on coffee and tea consumption in 15,789 participants of European and African-American ancestries from 15 cohorts. EWAS meta-analysis of coffee consumption reveals 11 CpGs surpassing the epigenome-wide significance threshold (P-value <1.1×10-7), which annotated to the AHRR, F2RL3, FLJ43663, HDAC4, GFI1 and PHGDH genes. Among them, cg14476101 is significantly associated with expression of the PHGDH and risk of fatty liver disease. Knockdown of PHGDH expression in liver cells shows a correlation with expression levels of genes associated with circulating lipids, suggesting a role of PHGDH in hepatic-lipid metabolism. EWAS meta-analysis on tea consumption reveals no significant association, only two CpGs annotated to CACNA1A and PRDM16 genes show suggestive association (P-value <5.0×10-6). These findings indicate that coffee-associated changes in DNA methylation levels may explain the mechanism of action of coffee consumption in conferring risk of diseases.

AB - Coffee and tea are extensively consumed beverages worldwide which have received considerable attention regarding health. Intake of these beverages is consistently linked to, among others, reduced risk of diabetes and liver diseases; however, the mechanisms of action remain elusive. Epigenetics is suggested as a mechanism mediating the effects of dietary and lifestyle factors on disease onset. Here we report the results from epigenome-wide association studies (EWAS) on coffee and tea consumption in 15,789 participants of European and African-American ancestries from 15 cohorts. EWAS meta-analysis of coffee consumption reveals 11 CpGs surpassing the epigenome-wide significance threshold (P-value <1.1×10-7), which annotated to the AHRR, F2RL3, FLJ43663, HDAC4, GFI1 and PHGDH genes. Among them, cg14476101 is significantly associated with expression of the PHGDH and risk of fatty liver disease. Knockdown of PHGDH expression in liver cells shows a correlation with expression levels of genes associated with circulating lipids, suggesting a role of PHGDH in hepatic-lipid metabolism. EWAS meta-analysis on tea consumption reveals no significant association, only two CpGs annotated to CACNA1A and PRDM16 genes show suggestive association (P-value <5.0×10-6). These findings indicate that coffee-associated changes in DNA methylation levels may explain the mechanism of action of coffee consumption in conferring risk of diseases.

KW - POLYCYCLIC AROMATIC-HYDROCARBONS

KW - ACTIVATED RECEPTOR 4

KW - MENDELIAN RANDOMIZATION

KW - EPIGENETICS

KW - RISK

KW - POPULATION

KW - CAFFEINE

KW - DISEASE

KW - DESIGN

KW - CANCER

U2 - 10.1038/s41467-021-22752-6

DO - 10.1038/s41467-021-22752-6

M3 - Article

C2 - 33990564

SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 2830

ER -