Analysis of DNA methylation at birth and in childhood reveals changes associated with season of birth and latitude

Research output: Contribution to journalJournal articleResearchpeer-review

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Analysis of DNA methylation at birth and in childhood reveals changes associated with season of birth and latitude. / Kadalayil, Latha; Alam, Md Zahangir; White, Cory Haley; Ghantous, Akram; Walton, Esther; Gruzieva, Olena; Merid, Simon Kebede; Kumar, Ashish; Roy, Ritu P.; Solomon, Olivia; Huen, Karen; Eskenazi, Brenda; Rzehak, Peter; Grote, Veit; Langhendries, Jean Paul; Verduci, Elvira; Ferre, Natalia; Gruszfeld, Darek; Gao, Lu; Guan, Weihua; Zeng, Xuehuo; Schisterman, Enrique F.; Dou, John F.; Bakulski, Kelly M.; Feinberg, Jason I.; Soomro, Munawar Hussain; Pesce, Giancarlo; Baiz, Nour; Isaevska, Elena; Plusquin, Michelle; Vafeiadi, Marina; Roumeliotaki, Theano; Langie, Sabine A.S.; Standaert, Arnout; Allard, Catherine; Perron, Patrice; Bouchard, Luigi; van Meel, Evelien R.; Felix, Janine F.; Jaddoe, Vincent W.V.; Yousefi, Paul D.; Ramlau-Hansen, Cecilia H.; Relton, Caroline L.; Tobi, Elmar W.; Starling, Anne P.; Yang, Ivana V.; Llambrich, Maria; Santorelli, Gillian; Lepeule, Johanna; Salas, Lucas A.; Bustamante, Mariona; Ewart, Susan L.; Zhang, Hongmei; Karmaus, Wilfried; Röder, Stefan; Zenclussen, Ana Claudia; Jin, Jianping; Nystad, Wenche; Page, Christian M.; Magnus, Maria; Jima, Dereje D.; Hoyo, Cathrine; Maguire, Rachel L.; Kvist, Tuomas; Czamara, Darina; Räikkönen, Katri; Gong, Tong; Ullemar, Vilhelmina; Rifas-Shiman, Sheryl L.; Oken, Emily; Almqvist, Catarina; Karlsson, Robert; Lahti, Jari; Murphy, Susan K.; Håberg, Siri E.; London, Stephanie; Herberth, Gunda; Arshad, Hasan; Sunyer, Jordi; Grazuleviciene, Regina; Dabelea, Dana; Steegers-Theunissen, Régine P.M.; Nohr, Ellen A.; Sørensen, Thorkild I.A.; Duijts, Liesbeth; Hivert, Marie France; Nelen, Vera; Popovic, Maja; Kogevinas, Manolis; Nawrot, Tim S.; Herceg, Zdenko; Annesi-Maesano, Isabella; Fallin, M. Daniele; Yeung, Edwina; Breton, Carrie V.; Koletzko, Berthold; Holland, Nina; Wiemels, Joseph L.; Melén, Erik; Sharp, Gemma C.; Silver, Matt J.; Rezwan, Faisal I.; Holloway, John W.

In: Clinical Epigenetics, Vol. 15, 148, 2023.

Research output: Contribution to journalJournal articleResearchpeer-review

Harvard

Kadalayil, L, Alam, MZ, White, CH, Ghantous, A, Walton, E, Gruzieva, O, Merid, SK, Kumar, A, Roy, RP, Solomon, O, Huen, K, Eskenazi, B, Rzehak, P, Grote, V, Langhendries, JP, Verduci, E, Ferre, N, Gruszfeld, D, Gao, L, Guan, W, Zeng, X, Schisterman, EF, Dou, JF, Bakulski, KM, Feinberg, JI, Soomro, MH, Pesce, G, Baiz, N, Isaevska, E, Plusquin, M, Vafeiadi, M, Roumeliotaki, T, Langie, SAS, Standaert, A, Allard, C, Perron, P, Bouchard, L, van Meel, ER, Felix, JF, Jaddoe, VWV, Yousefi, PD, Ramlau-Hansen, CH, Relton, CL, Tobi, EW, Starling, AP, Yang, IV, Llambrich, M, Santorelli, G, Lepeule, J, Salas, LA, Bustamante, M, Ewart, SL, Zhang, H, Karmaus, W, Röder, S, Zenclussen, AC, Jin, J, Nystad, W, Page, CM, Magnus, M, Jima, DD, Hoyo, C, Maguire, RL, Kvist, T, Czamara, D, Räikkönen, K, Gong, T, Ullemar, V, Rifas-Shiman, SL, Oken, E, Almqvist, C, Karlsson, R, Lahti, J, Murphy, SK, Håberg, SE, London, S, Herberth, G, Arshad, H, Sunyer, J, Grazuleviciene, R, Dabelea, D, Steegers-Theunissen, RPM, Nohr, EA, Sørensen, TIA, Duijts, L, Hivert, MF, Nelen, V, Popovic, M, Kogevinas, M, Nawrot, TS, Herceg, Z, Annesi-Maesano, I, Fallin, MD, Yeung, E, Breton, CV, Koletzko, B, Holland, N, Wiemels, JL, Melén, E, Sharp, GC, Silver, MJ, Rezwan, FI & Holloway, JW 2023, 'Analysis of DNA methylation at birth and in childhood reveals changes associated with season of birth and latitude', Clinical Epigenetics, vol. 15, 148. https://doi.org/10.1186/s13148-023-01542-5

APA

Kadalayil, L., Alam, M. Z., White, C. H., Ghantous, A., Walton, E., Gruzieva, O., Merid, S. K., Kumar, A., Roy, R. P., Solomon, O., Huen, K., Eskenazi, B., Rzehak, P., Grote, V., Langhendries, J. P., Verduci, E., Ferre, N., Gruszfeld, D., Gao, L., ... Holloway, J. W. (2023). Analysis of DNA methylation at birth and in childhood reveals changes associated with season of birth and latitude. Clinical Epigenetics, 15, [148]. https://doi.org/10.1186/s13148-023-01542-5

Vancouver

Kadalayil L, Alam MZ, White CH, Ghantous A, Walton E, Gruzieva O et al. Analysis of DNA methylation at birth and in childhood reveals changes associated with season of birth and latitude. Clinical Epigenetics. 2023;15. 148. https://doi.org/10.1186/s13148-023-01542-5

Author

Kadalayil, Latha ; Alam, Md Zahangir ; White, Cory Haley ; Ghantous, Akram ; Walton, Esther ; Gruzieva, Olena ; Merid, Simon Kebede ; Kumar, Ashish ; Roy, Ritu P. ; Solomon, Olivia ; Huen, Karen ; Eskenazi, Brenda ; Rzehak, Peter ; Grote, Veit ; Langhendries, Jean Paul ; Verduci, Elvira ; Ferre, Natalia ; Gruszfeld, Darek ; Gao, Lu ; Guan, Weihua ; Zeng, Xuehuo ; Schisterman, Enrique F. ; Dou, John F. ; Bakulski, Kelly M. ; Feinberg, Jason I. ; Soomro, Munawar Hussain ; Pesce, Giancarlo ; Baiz, Nour ; Isaevska, Elena ; Plusquin, Michelle ; Vafeiadi, Marina ; Roumeliotaki, Theano ; Langie, Sabine A.S. ; Standaert, Arnout ; Allard, Catherine ; Perron, Patrice ; Bouchard, Luigi ; van Meel, Evelien R. ; Felix, Janine F. ; Jaddoe, Vincent W.V. ; Yousefi, Paul D. ; Ramlau-Hansen, Cecilia H. ; Relton, Caroline L. ; Tobi, Elmar W. ; Starling, Anne P. ; Yang, Ivana V. ; Llambrich, Maria ; Santorelli, Gillian ; Lepeule, Johanna ; Salas, Lucas A. ; Bustamante, Mariona ; Ewart, Susan L. ; Zhang, Hongmei ; Karmaus, Wilfried ; Röder, Stefan ; Zenclussen, Ana Claudia ; Jin, Jianping ; Nystad, Wenche ; Page, Christian M. ; Magnus, Maria ; Jima, Dereje D. ; Hoyo, Cathrine ; Maguire, Rachel L. ; Kvist, Tuomas ; Czamara, Darina ; Räikkönen, Katri ; Gong, Tong ; Ullemar, Vilhelmina ; Rifas-Shiman, Sheryl L. ; Oken, Emily ; Almqvist, Catarina ; Karlsson, Robert ; Lahti, Jari ; Murphy, Susan K. ; Håberg, Siri E. ; London, Stephanie ; Herberth, Gunda ; Arshad, Hasan ; Sunyer, Jordi ; Grazuleviciene, Regina ; Dabelea, Dana ; Steegers-Theunissen, Régine P.M. ; Nohr, Ellen A. ; Sørensen, Thorkild I.A. ; Duijts, Liesbeth ; Hivert, Marie France ; Nelen, Vera ; Popovic, Maja ; Kogevinas, Manolis ; Nawrot, Tim S. ; Herceg, Zdenko ; Annesi-Maesano, Isabella ; Fallin, M. Daniele ; Yeung, Edwina ; Breton, Carrie V. ; Koletzko, Berthold ; Holland, Nina ; Wiemels, Joseph L. ; Melén, Erik ; Sharp, Gemma C. ; Silver, Matt J. ; Rezwan, Faisal I. ; Holloway, John W. / Analysis of DNA methylation at birth and in childhood reveals changes associated with season of birth and latitude. In: Clinical Epigenetics. 2023 ; Vol. 15.

Bibtex

@article{6e286bc07057437d85c7beac7a775a88,
title = "Analysis of DNA methylation at birth and in childhood reveals changes associated with season of birth and latitude",
abstract = "Background: Seasonal variations in environmental exposures at birth or during gestation are associated with numerous adult traits and health outcomes later in life. Whether DNA methylation (DNAm) plays a role in the molecular mechanisms underlying the associations between birth season and lifelong phenotypes remains unclear. Methods: We carried out epigenome-wide meta-analyses within the Pregnancy And Childhood Epigenetic Consortium to identify associations of DNAm with birth season, both at differentially methylated probes (DMPs) and regions (DMRs). Associations were examined at two time points: at birth (21 cohorts, N = 9358) and in children aged 1–11 years (12 cohorts, N = 3610). We conducted meta-analyses to assess the impact of latitude on birth season-specific associations at both time points. Results: We identified associations between birth season and DNAm (False Discovery Rate-adjusted p values < 0.05) at two CpGs at birth (winter-born) and four in the childhood (summer-born) analyses when compared to children born in autumn. Furthermore, we identified twenty-six differentially methylated regions (DMR) at birth (winter-born: 8, spring-born: 15, summer-born: 3) and thirty-two in childhood (winter-born: 12, spring and summer: 10 each) meta-analyses with few overlapping DMRs between the birth seasons or the two time points. The DMRs were associated with genes of known functions in tumorigenesis, psychiatric/neurological disorders, inflammation, or immunity, amongst others. Latitude-stratified meta-analyses [higher (≥ 50°N), lower (< 50°N, northern hemisphere only)] revealed differences in associations between birth season and DNAm by birth latitude. DMR analysis implicated genes with previously reported links to schizophrenia (LAX1), skin disorders (PSORS1C, LTB4R), and airway inflammation including asthma (LTB4R), present only at birth in the higher latitudes (≥ 50°N). Conclusions: In this large epigenome-wide meta-analysis study, we provide evidence for (i) associations between DNAm and season of birth that are unique for the seasons of the year (temporal effect) and (ii) latitude-dependent variations in the seasonal associations (spatial effect). DNAm could play a role in the molecular mechanisms underlying the effect of birth season on adult health outcomes.",
keywords = "Birth season, Differentially methylated regions (DMR), DNA methylation, Latitude, Meta-analysis, PACE",
author = "Latha Kadalayil and Alam, {Md Zahangir} and White, {Cory Haley} and Akram Ghantous and Esther Walton and Olena Gruzieva and Merid, {Simon Kebede} and Ashish Kumar and Roy, {Ritu P.} and Olivia Solomon and Karen Huen and Brenda Eskenazi and Peter Rzehak and Veit Grote and Langhendries, {Jean Paul} and Elvira Verduci and Natalia Ferre and Darek Gruszfeld and Lu Gao and Weihua Guan and Xuehuo Zeng and Schisterman, {Enrique F.} and Dou, {John F.} and Bakulski, {Kelly M.} and Feinberg, {Jason I.} and Soomro, {Munawar Hussain} and Giancarlo Pesce and Nour Baiz and Elena Isaevska and Michelle Plusquin and Marina Vafeiadi and Theano Roumeliotaki and Langie, {Sabine A.S.} and Arnout Standaert and Catherine Allard and Patrice Perron and Luigi Bouchard and {van Meel}, {Evelien R.} and Felix, {Janine F.} and Jaddoe, {Vincent W.V.} and Yousefi, {Paul D.} and Ramlau-Hansen, {Cecilia H.} and Relton, {Caroline L.} and Tobi, {Elmar W.} and Starling, {Anne P.} and Yang, {Ivana V.} and Maria Llambrich and Gillian Santorelli and Johanna Lepeule and Salas, {Lucas A.} and Mariona Bustamante and Ewart, {Susan L.} and Hongmei Zhang and Wilfried Karmaus and Stefan R{\"o}der and Zenclussen, {Ana Claudia} and Jianping Jin and Wenche Nystad and Page, {Christian M.} and Maria Magnus and Jima, {Dereje D.} and Cathrine Hoyo and Maguire, {Rachel L.} and Tuomas Kvist and Darina Czamara and Katri R{\"a}ikk{\"o}nen and Tong Gong and Vilhelmina Ullemar and Rifas-Shiman, {Sheryl L.} and Emily Oken and Catarina Almqvist and Robert Karlsson and Jari Lahti and Murphy, {Susan K.} and H{\aa}berg, {Siri E.} and Stephanie London and Gunda Herberth and Hasan Arshad and Jordi Sunyer and Regina Grazuleviciene and Dana Dabelea and Steegers-Theunissen, {R{\'e}gine P.M.} and Nohr, {Ellen A.} and S{\o}rensen, {Thorkild I.A.} and Liesbeth Duijts and Hivert, {Marie France} and Vera Nelen and Maja Popovic and Manolis Kogevinas and Nawrot, {Tim S.} and Zdenko Herceg and Isabella Annesi-Maesano and Fallin, {M. Daniele} and Edwina Yeung and Breton, {Carrie V.} and Berthold Koletzko and Nina Holland and Wiemels, {Joseph L.} and Erik Mel{\'e}n and Sharp, {Gemma C.} and Silver, {Matt J.} and Rezwan, {Faisal I.} and Holloway, {John W.}",
note = "Publisher Copyright: {\textcopyright} 2023, BioMed Central Ltd., part of Springer Nature.",
year = "2023",
doi = "10.1186/s13148-023-01542-5",
language = "English",
volume = "15",
journal = "Clinical Epigenetics (Print)",
issn = "1868-7075",
publisher = "BioMed Central Ltd.",

}

RIS

TY - JOUR

T1 - Analysis of DNA methylation at birth and in childhood reveals changes associated with season of birth and latitude

AU - Kadalayil, Latha

AU - Alam, Md Zahangir

AU - White, Cory Haley

AU - Ghantous, Akram

AU - Walton, Esther

AU - Gruzieva, Olena

AU - Merid, Simon Kebede

AU - Kumar, Ashish

AU - Roy, Ritu P.

AU - Solomon, Olivia

AU - Huen, Karen

AU - Eskenazi, Brenda

AU - Rzehak, Peter

AU - Grote, Veit

AU - Langhendries, Jean Paul

AU - Verduci, Elvira

AU - Ferre, Natalia

AU - Gruszfeld, Darek

AU - Gao, Lu

AU - Guan, Weihua

AU - Zeng, Xuehuo

AU - Schisterman, Enrique F.

AU - Dou, John F.

AU - Bakulski, Kelly M.

AU - Feinberg, Jason I.

AU - Soomro, Munawar Hussain

AU - Pesce, Giancarlo

AU - Baiz, Nour

AU - Isaevska, Elena

AU - Plusquin, Michelle

AU - Vafeiadi, Marina

AU - Roumeliotaki, Theano

AU - Langie, Sabine A.S.

AU - Standaert, Arnout

AU - Allard, Catherine

AU - Perron, Patrice

AU - Bouchard, Luigi

AU - van Meel, Evelien R.

AU - Felix, Janine F.

AU - Jaddoe, Vincent W.V.

AU - Yousefi, Paul D.

AU - Ramlau-Hansen, Cecilia H.

AU - Relton, Caroline L.

AU - Tobi, Elmar W.

AU - Starling, Anne P.

AU - Yang, Ivana V.

AU - Llambrich, Maria

AU - Santorelli, Gillian

AU - Lepeule, Johanna

AU - Salas, Lucas A.

AU - Bustamante, Mariona

AU - Ewart, Susan L.

AU - Zhang, Hongmei

AU - Karmaus, Wilfried

AU - Röder, Stefan

AU - Zenclussen, Ana Claudia

AU - Jin, Jianping

AU - Nystad, Wenche

AU - Page, Christian M.

AU - Magnus, Maria

AU - Jima, Dereje D.

AU - Hoyo, Cathrine

AU - Maguire, Rachel L.

AU - Kvist, Tuomas

AU - Czamara, Darina

AU - Räikkönen, Katri

AU - Gong, Tong

AU - Ullemar, Vilhelmina

AU - Rifas-Shiman, Sheryl L.

AU - Oken, Emily

AU - Almqvist, Catarina

AU - Karlsson, Robert

AU - Lahti, Jari

AU - Murphy, Susan K.

AU - Håberg, Siri E.

AU - London, Stephanie

AU - Herberth, Gunda

AU - Arshad, Hasan

AU - Sunyer, Jordi

AU - Grazuleviciene, Regina

AU - Dabelea, Dana

AU - Steegers-Theunissen, Régine P.M.

AU - Nohr, Ellen A.

AU - Sørensen, Thorkild I.A.

AU - Duijts, Liesbeth

AU - Hivert, Marie France

AU - Nelen, Vera

AU - Popovic, Maja

AU - Kogevinas, Manolis

AU - Nawrot, Tim S.

AU - Herceg, Zdenko

AU - Annesi-Maesano, Isabella

AU - Fallin, M. Daniele

AU - Yeung, Edwina

AU - Breton, Carrie V.

AU - Koletzko, Berthold

AU - Holland, Nina

AU - Wiemels, Joseph L.

AU - Melén, Erik

AU - Sharp, Gemma C.

AU - Silver, Matt J.

AU - Rezwan, Faisal I.

AU - Holloway, John W.

N1 - Publisher Copyright: © 2023, BioMed Central Ltd., part of Springer Nature.

PY - 2023

Y1 - 2023

N2 - Background: Seasonal variations in environmental exposures at birth or during gestation are associated with numerous adult traits and health outcomes later in life. Whether DNA methylation (DNAm) plays a role in the molecular mechanisms underlying the associations between birth season and lifelong phenotypes remains unclear. Methods: We carried out epigenome-wide meta-analyses within the Pregnancy And Childhood Epigenetic Consortium to identify associations of DNAm with birth season, both at differentially methylated probes (DMPs) and regions (DMRs). Associations were examined at two time points: at birth (21 cohorts, N = 9358) and in children aged 1–11 years (12 cohorts, N = 3610). We conducted meta-analyses to assess the impact of latitude on birth season-specific associations at both time points. Results: We identified associations between birth season and DNAm (False Discovery Rate-adjusted p values < 0.05) at two CpGs at birth (winter-born) and four in the childhood (summer-born) analyses when compared to children born in autumn. Furthermore, we identified twenty-six differentially methylated regions (DMR) at birth (winter-born: 8, spring-born: 15, summer-born: 3) and thirty-two in childhood (winter-born: 12, spring and summer: 10 each) meta-analyses with few overlapping DMRs between the birth seasons or the two time points. The DMRs were associated with genes of known functions in tumorigenesis, psychiatric/neurological disorders, inflammation, or immunity, amongst others. Latitude-stratified meta-analyses [higher (≥ 50°N), lower (< 50°N, northern hemisphere only)] revealed differences in associations between birth season and DNAm by birth latitude. DMR analysis implicated genes with previously reported links to schizophrenia (LAX1), skin disorders (PSORS1C, LTB4R), and airway inflammation including asthma (LTB4R), present only at birth in the higher latitudes (≥ 50°N). Conclusions: In this large epigenome-wide meta-analysis study, we provide evidence for (i) associations between DNAm and season of birth that are unique for the seasons of the year (temporal effect) and (ii) latitude-dependent variations in the seasonal associations (spatial effect). DNAm could play a role in the molecular mechanisms underlying the effect of birth season on adult health outcomes.

AB - Background: Seasonal variations in environmental exposures at birth or during gestation are associated with numerous adult traits and health outcomes later in life. Whether DNA methylation (DNAm) plays a role in the molecular mechanisms underlying the associations between birth season and lifelong phenotypes remains unclear. Methods: We carried out epigenome-wide meta-analyses within the Pregnancy And Childhood Epigenetic Consortium to identify associations of DNAm with birth season, both at differentially methylated probes (DMPs) and regions (DMRs). Associations were examined at two time points: at birth (21 cohorts, N = 9358) and in children aged 1–11 years (12 cohorts, N = 3610). We conducted meta-analyses to assess the impact of latitude on birth season-specific associations at both time points. Results: We identified associations between birth season and DNAm (False Discovery Rate-adjusted p values < 0.05) at two CpGs at birth (winter-born) and four in the childhood (summer-born) analyses when compared to children born in autumn. Furthermore, we identified twenty-six differentially methylated regions (DMR) at birth (winter-born: 8, spring-born: 15, summer-born: 3) and thirty-two in childhood (winter-born: 12, spring and summer: 10 each) meta-analyses with few overlapping DMRs between the birth seasons or the two time points. The DMRs were associated with genes of known functions in tumorigenesis, psychiatric/neurological disorders, inflammation, or immunity, amongst others. Latitude-stratified meta-analyses [higher (≥ 50°N), lower (< 50°N, northern hemisphere only)] revealed differences in associations between birth season and DNAm by birth latitude. DMR analysis implicated genes with previously reported links to schizophrenia (LAX1), skin disorders (PSORS1C, LTB4R), and airway inflammation including asthma (LTB4R), present only at birth in the higher latitudes (≥ 50°N). Conclusions: In this large epigenome-wide meta-analysis study, we provide evidence for (i) associations between DNAm and season of birth that are unique for the seasons of the year (temporal effect) and (ii) latitude-dependent variations in the seasonal associations (spatial effect). DNAm could play a role in the molecular mechanisms underlying the effect of birth season on adult health outcomes.

KW - Birth season

KW - Differentially methylated regions (DMR)

KW - DNA methylation

KW - Latitude

KW - Meta-analysis

KW - PACE

U2 - 10.1186/s13148-023-01542-5

DO - 10.1186/s13148-023-01542-5

M3 - Journal article

C2 - 37697338

AN - SCOPUS:85170627066

VL - 15

JO - Clinical Epigenetics (Print)

JF - Clinical Epigenetics (Print)

SN - 1868-7075

M1 - 148

ER -

ID: 368251492