Cited by 102Epigenetics and DNA MethylationSmoking Behavior and CessationBirth, Development, and Health

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Fetal lung and placental methylation is associated with in utero nicotine exposure

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Chhabra, Divya, Sharma, Sunita, Kho, Alvin T, Gaedigk, Roger, Vyhlidal, Carrie A, Leeder, J Steven, Morrow, Jarrett, Carey, Vincent J, Weiss, Scott T, Tantisira, Kelan G, DeMeo, Dawn L·2014·Epigenetics

DOI 10.4161/15592294.2014.971593PMC PMC4623268

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Abstract

In utero smoke exposure has been shown to have detrimental effects on lung function and to be associated with persistent wheezing and asthma in children. One potential mechanism of IUS effects could be alterations in DNA methylation, which may have life-long implications. The goal of this study was to examine the association between DNA methylation and nicotine exposure in fetal lung and placental tissue in early development; nicotine exposure in this analysis represents a likely surrogate for in-utero smoke. We performed an epigenome-wide analysis of DNA methylation in fetal lung tissue (n = 85, 41 smoke exposed (48%), 44 controls) and the corresponding placental tissue samples (n = 80, 39 smoke exposed (49%), 41 controls) using the Illumina HumanMethylation450 BeadChip array. Differential methylation analyses were conducted to evaluate the variation associated with nicotine exposure. The most significant CpG sites in the fetal lung analysis mapped to the PKP3 (P = 2.94 × 10(-03)), ANKRD33B (P = 3.12 × 10(-03)), CNTD2 (P = 4.9 × 10(-03)) and DPP10 (P = 5.43 × 10(-03)) genes. In the placental methylome, the most significant CpG sites mapped to the GTF2H2C and GTF2H2D genes (P = 2.87 × 10(-06) - 3.48 × 10(-05)). One hundred and one unique CpG sites with P-values < 0.05 were concordant between lung and placental tissue analyses. Gene Set Enrichment Analysis demonstrated enrichment of specific disorders, such as asthma and immune disorders. Our findings demonstrate an association between in utero nicotine exposure and variable DNA methylation in fetal lung and placental tissues, suggesting a role for DNA methylation variation in the fetal origins of chronic diseases.

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Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625
KEGG: Kyoto Encyclopedia of Genes and Genomes
Kanehisa, M. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.1.27 · Cited by 37,077
KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232
The <tt>sva</tt> package for removing batch effects and other unwanted variation in high-throughput experiments
Leek, J. T., Johnson, W. E., Parker, H. S., Jaffe, A. E., & Storey, J. D. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts034 · Cited by 6,231
Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays
Aryee, M. J., Jaffe, A. E., Bravo, H. C., Ladd‐Acosta, C., Feinberg, A. P., Hansen, K. D., & Irizarry, R. A. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu049 · Cited by 4,389
Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders
Baxter, E. J., Scott, L. M., Campbell, P. J., East, C., Fourouclas, N., Swanton, S., Vassiliou, G. S., Bench, A. J., Boyd, E. M., Curtin, N., et al. (2005) · The Lancet · doi:10.1016/s0140-6736(05)71142-9 · Cited by 3,548
A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera
James, C., Ugo, V., Couedic, J. P. L., Staerk, J., Delhommeau, F., Lacout, C., Garçon, L., Raslová, H., Berger, R., Griscelli, A. B., et al. (2005) · Nature · doi:10.1038/nature03546 · Cited by 3,542
Bioinformatics and Computational Biology Solutions Using R and Bioconductor
Gentleman, R. C., Carey, V. J., Huber, W. K., Irizarry, R. A., & Dudoit, S. (2005) · Statistics in the health sciences · doi:10.1007/0-387-29362-0 · Cited by 3,470
Self-citation
Journal of Biological Chemistry
Kurkinensp, M., CondongT, M. R., Blumberg, B., Barlow, D. P., Quiñones, S., Sausg, J., & Pihlajaniemisyy, T. (2021) · Journal of Biological Chemistry · doi:10.1074/jbc · Cited by 3,427
Current Cigarette Smoking Among Adults — United States, 2016
Jamal, A., Phillips, E., Gentzke, A. S., Homa, D. M., Babb, S. D., King, B. A., & Neff, L. J. (2018) · MMWR Morbidity and Mortality Weekly Report · doi:10.15585/mmwr.mm6702a1 · Cited by 3,079

Show all 71 references

Research works printed but not linked: 2

Centers for Disease Control and Prevention (CDC), 2012, MMWR Morb Mortal Wkly Rep, 61, 889
Jia RZ, 2012, Int J Mol Med, 30, 133

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Additional file 1 of Impact of vitamin C supplementation on placental DNA methylation changes related to maternal smoking: association with gene expression and respiratory outcomes
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Additional file 3 of Impact of vitamin C supplementation on placental DNA methylation changes related to maternal smoking: association with gene expression and respiratory outcomes
Shorey‐Kendrick, L. E., McEvoy, C. T., O’Sullivan, S. M., Milner, K. F., Vuylsteke, B., Tepper, R. S., Haas, D. M., Park, B., Gao, L., Vu, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16641922
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Novoloaca, A. (2020) · theses.fr (ABES) · doi:10.70675/4286201fz357fz4b0ez8dbfzdc0b44a46cae
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Authors: Chhabra, D., Sharma, S., Kho, A. T., Gaedigk, R., Vyhlidal, C. A., Leeder, J. S., Morrow, J., Carey, V. J., Weiss, S. T., Tantisira, K. G., & DeMeo, D. L.
Affiliations: Brigham and Women's Hospital (US)
Children's Mercy Hospital (US)
Corresponding author: DeMeo, Dawn L
ORCID: Chhabra, Divya
Kho, Alvin T
Gaedigk, Roger
Leeder, J Steven
Morrow, Jarrett
Carey, Vincent J
Weiss, Scott T
Tantisira, Kelan G
DeMeo, Dawn L
Venue: Epigenetics
Publisher: Informa UK Limited
Published: 2014-11-02
Volume: 9
Issue: 11
Pages: 1473-1484
ISSN: 1559-2294 (ISSN-L)
1559-2308
DOI: 10.4161/15592294.2014.971593
PMC: PMC4623268
OpenAlex: W2051268137
Cited by: 102
References: 71
Citations by year: 2026: 3 · 2025: 4 · 2024: 10 · 2023: 7 · 2022: 6 · 2021: 10 · 2020: 12 · 2019: 11 · 2018: 13 · 2017: 10 · 2016: 10 · 2015: 6
FWCI: 3.56
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Epigenetics (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5R24 HD0008836, HL007427, HL083069)
National Heart, Lung, and Blood Institute (K25HL091124, R21HL107927, R01HL089438, R01HL097144, P01HL083069, K08HL096833, T32HL007427)
U.S. National Library of Medicine (T15LM011271)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Smoking Behavior and Cessation
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Keywords: maternal smoking, fetal lung, placenta, DNA methylation, epigenome-wide association study, PKP3, DPP10, asthma, immune disorders
MeSH terms: Dipeptidyl-Peptidases and Tripeptidyl-Peptidases, Female, Humans, Lung, Male, Nicotine, Placenta, Pregnancy, Case-Control Studies, Maternal Exposure, CpG Islands, DNA Methylation, Genome-Wide Association Study

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Fetal lung and placental methylation is associated with in utero nicotine exposure

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