Paternal tobacco smoke correlated to offspring asthma and prenatal epigenetic programming

Chih Chiang Wu; Te Yao Hsu; Jen Chieh Chang; Chia Yu Ou; Ho Chang Kuo; Chieh An Liu; Chih Lu Wang; Hau Chuang; Chie Pein Chen; Kuender D. Yang

doi:10.3389/fgene.2019.00471

Paternal tobacco smoke correlated to offspring asthma and prenatal epigenetic programming

Chih Chiang Wu, Te Yao Hsu, Jen Chieh Chang, Chia Yu Ou, Ho Chang Kuo, Chieh An Liu, Chih Lu Wang, Hau Chuang, Chie Pein Chen, Kuender D. Yang^*

^*Corresponding author for this work

School of Medicine

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

40 Scopus citations

Abstract

Rationale: Little is known about effects of paternal tobacco smoke (PTS) on the offspring's asthma and its prenatal epigenetic programming. Objective: To investigate whether PTS exposure was associated with the offspring's asthma and correlated to epigenetic CG methylation of potential tobacco-related immune genes: LMO2, GSTM1 or/and IL-10 genes. Measurements and Main Results: In a birth cohort of 1,629 newborns, we measured exposure rates of PTS (23%) and maternal tobacco smoke (MTS, 0.2%), cord blood DNA methylation, infant respiratory tract infection, childhood DNA methylation, and childhood allergic diseases. Infants with prenatal PTS exposure had a significantly higher risk of asthma by the age of 6 than those without (p = 0.026). The PTS exposure doses at 0, <20, and ≧20 cigarettes per day were significantly associated with the trend of childhood asthma and the increase of LMO2-E148 (p = 0.006), and IL10_P325 (p = 0.008) CG methylation. The combination of higher CG methylation levels of LMO2_E148, IL10_P325, and GSTM1_P266 corresponded to the highest risk of asthma by 43.48%, compared to other combinations (16.67-23.08%) in the 3-way multi-factor dimensionality reduction (MDR) analysis. The LMO2_P794 and GSTM1_P266 CG methylation levels at age 0 were significantly correlated to those at age of 6. Conclusions: Prenatal PTS exposure increases CG methylation contents of immune genes, such as LMO2 and IL-10, which significantly retained from newborn stage to 6 years of age and correlated to development of childhood asthma. Modulation of the LMO2 and IL-10 CG methylation and/or their gene expression may provide a regimen for early prevention of PTS-associated childhood asthma.

Original language	English
Article number	471
Journal	Frontiers in Genetics
Volume	10
Issue number	MAY
DOIs	https://doi.org/10.3389/fgene.2019.00471
State	Published - 2019

Bibliographical note

Publisher Copyright:
Copyright © 2019 Wu, Hsu, Chang, Ou, Kuo, Liu, Wang, Chuang, Chen and Yang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

Keywords

Asthma development
CG methylation
GSTM1
IL-10
LMO2
Paternal tobacco smoke
Prenatal tobacco smoke exposure

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10.3389/fgene.2019.00471

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@article{b098ab4dd17d4fe89ed0525093963f77,

title = "Paternal tobacco smoke correlated to offspring asthma and prenatal epigenetic programming",

abstract = "Rationale: Little is known about effects of paternal tobacco smoke (PTS) on the offspring's asthma and its prenatal epigenetic programming. Objective: To investigate whether PTS exposure was associated with the offspring's asthma and correlated to epigenetic CG methylation of potential tobacco-related immune genes: LMO2, GSTM1 or/and IL-10 genes. Measurements and Main Results: In a birth cohort of 1,629 newborns, we measured exposure rates of PTS (23%) and maternal tobacco smoke (MTS, 0.2%), cord blood DNA methylation, infant respiratory tract infection, childhood DNA methylation, and childhood allergic diseases. Infants with prenatal PTS exposure had a significantly higher risk of asthma by the age of 6 than those without (p = 0.026). The PTS exposure doses at 0, <20, and ≧20 cigarettes per day were significantly associated with the trend of childhood asthma and the increase of LMO2-E148 (p = 0.006), and IL10_P325 (p = 0.008) CG methylation. The combination of higher CG methylation levels of LMO2_E148, IL10_P325, and GSTM1_P266 corresponded to the highest risk of asthma by 43.48%, compared to other combinations (16.67-23.08%) in the 3-way multi-factor dimensionality reduction (MDR) analysis. The LMO2_P794 and GSTM1_P266 CG methylation levels at age 0 were significantly correlated to those at age of 6. Conclusions: Prenatal PTS exposure increases CG methylation contents of immune genes, such as LMO2 and IL-10, which significantly retained from newborn stage to 6 years of age and correlated to development of childhood asthma. Modulation of the LMO2 and IL-10 CG methylation and/or their gene expression may provide a regimen for early prevention of PTS-associated childhood asthma.",

keywords = "Asthma development, CG methylation, GSTM1, IL-10, LMO2, Paternal tobacco smoke, Prenatal tobacco smoke exposure",

author = "Wu, {Chih Chiang} and Hsu, {Te Yao} and Chang, {Jen Chieh} and Ou, {Chia Yu} and Kuo, {Ho Chang} and Liu, {Chieh An} and Wang, {Chih Lu} and Hau Chuang and Chen, {Chie Pein} and Yang, {Kuender D.}",

note = "Publisher Copyright: Copyright {\textcopyright} 2019 Wu, Hsu, Chang, Ou, Kuo, Liu, Wang, Chuang, Chen and Yang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.",

year = "2019",

doi = "10.3389/fgene.2019.00471",

language = "英语",

volume = "10",

journal = "Frontiers in Genetics",

issn = "1664-8021",

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T1 - Paternal tobacco smoke correlated to offspring asthma and prenatal epigenetic programming

AU - Wu, Chih Chiang

AU - Hsu, Te Yao

AU - Chang, Jen Chieh

AU - Ou, Chia Yu

AU - Kuo, Ho Chang

AU - Liu, Chieh An

AU - Wang, Chih Lu

AU - Chuang, Hau

AU - Chen, Chie Pein

AU - Yang, Kuender D.

N1 - Publisher Copyright: Copyright © 2019 Wu, Hsu, Chang, Ou, Kuo, Liu, Wang, Chuang, Chen and Yang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

PY - 2019

Y1 - 2019

N2 - Rationale: Little is known about effects of paternal tobacco smoke (PTS) on the offspring's asthma and its prenatal epigenetic programming. Objective: To investigate whether PTS exposure was associated with the offspring's asthma and correlated to epigenetic CG methylation of potential tobacco-related immune genes: LMO2, GSTM1 or/and IL-10 genes. Measurements and Main Results: In a birth cohort of 1,629 newborns, we measured exposure rates of PTS (23%) and maternal tobacco smoke (MTS, 0.2%), cord blood DNA methylation, infant respiratory tract infection, childhood DNA methylation, and childhood allergic diseases. Infants with prenatal PTS exposure had a significantly higher risk of asthma by the age of 6 than those without (p = 0.026). The PTS exposure doses at 0, <20, and ≧20 cigarettes per day were significantly associated with the trend of childhood asthma and the increase of LMO2-E148 (p = 0.006), and IL10_P325 (p = 0.008) CG methylation. The combination of higher CG methylation levels of LMO2_E148, IL10_P325, and GSTM1_P266 corresponded to the highest risk of asthma by 43.48%, compared to other combinations (16.67-23.08%) in the 3-way multi-factor dimensionality reduction (MDR) analysis. The LMO2_P794 and GSTM1_P266 CG methylation levels at age 0 were significantly correlated to those at age of 6. Conclusions: Prenatal PTS exposure increases CG methylation contents of immune genes, such as LMO2 and IL-10, which significantly retained from newborn stage to 6 years of age and correlated to development of childhood asthma. Modulation of the LMO2 and IL-10 CG methylation and/or their gene expression may provide a regimen for early prevention of PTS-associated childhood asthma.

AB - Rationale: Little is known about effects of paternal tobacco smoke (PTS) on the offspring's asthma and its prenatal epigenetic programming. Objective: To investigate whether PTS exposure was associated with the offspring's asthma and correlated to epigenetic CG methylation of potential tobacco-related immune genes: LMO2, GSTM1 or/and IL-10 genes. Measurements and Main Results: In a birth cohort of 1,629 newborns, we measured exposure rates of PTS (23%) and maternal tobacco smoke (MTS, 0.2%), cord blood DNA methylation, infant respiratory tract infection, childhood DNA methylation, and childhood allergic diseases. Infants with prenatal PTS exposure had a significantly higher risk of asthma by the age of 6 than those without (p = 0.026). The PTS exposure doses at 0, <20, and ≧20 cigarettes per day were significantly associated with the trend of childhood asthma and the increase of LMO2-E148 (p = 0.006), and IL10_P325 (p = 0.008) CG methylation. The combination of higher CG methylation levels of LMO2_E148, IL10_P325, and GSTM1_P266 corresponded to the highest risk of asthma by 43.48%, compared to other combinations (16.67-23.08%) in the 3-way multi-factor dimensionality reduction (MDR) analysis. The LMO2_P794 and GSTM1_P266 CG methylation levels at age 0 were significantly correlated to those at age of 6. Conclusions: Prenatal PTS exposure increases CG methylation contents of immune genes, such as LMO2 and IL-10, which significantly retained from newborn stage to 6 years of age and correlated to development of childhood asthma. Modulation of the LMO2 and IL-10 CG methylation and/or their gene expression may provide a regimen for early prevention of PTS-associated childhood asthma.

KW - Asthma development

KW - CG methylation

KW - GSTM1

KW - IL-10

KW - LMO2

KW - Paternal tobacco smoke

KW - Prenatal tobacco smoke exposure

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U2 - 10.3389/fgene.2019.00471

DO - 10.3389/fgene.2019.00471

M3 - 文章

AN - SCOPUS:85067870791

SN - 1664-8021

VL - 10

JO - Frontiers in Genetics

JF - Frontiers in Genetics

IS - MAY

M1 - 471

ER -

Paternal tobacco smoke correlated to offspring asthma and prenatal epigenetic programming

Abstract

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Keywords

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