Smoking during pregnancy increases chemerin expression in neonatal tissue

Leryn J. Reynolds; Niraj R. Chavan; Logan B. DeHoff; Joshua D. Preston; Hannah F. Maddox; John M. O'Brien; David A. Armstrong; Carmen J. Marsit; Kevin J. Pearson

doi:10.1113/EP087307

Smoking during pregnancy increases chemerin expression in neonatal tissue

Leryn J. Reynolds, Niraj R. Chavan, Logan B. DeHoff, Joshua D. Preston, Hannah F. Maddox, John M. O'Brien, David A. Armstrong, Carmen J. Marsit, Kevin J. Pearson

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

4 Scopus citations

Abstract

New Findings: What is the central question of this study? Is chemerin, an adipokine implicated in obesity, increased in neonates following in utero cigarette smoke exposure. What is the main finding and its importance? Chemerin mRNA expression was increased and chemerin DNA methylation was decreased in babies born to mothers who smoked during pregnancy. These data provide a potential mechanism that may be mediating the increased obesity risk in individuals that are born to mothers who smoked during pregnancy. Abstract: It has been shown that in utero tobacco exposure increases offspring risk for obesity, but the mechanisms responsible for this increased risk are not well understood. Chemerin is an adipokine that regulates adipocyte differentiation. This chemokine is elevated in obese individuals and with smoke exposure, but its levels have not been measured in neonates exposed to cigarette smoke in utero. We examined chemerin gene expression [n = 31 non-smoker (NS) and 15 smoker (S)] and DNA methylation (n = 28 NS and n = 11 S) in skin collected from babies born to mothers who smoked during pregnancy as compared to non-smoking controls. Quality RNA and DNA were isolated from foreskin tissue following circumcision, and chemerin gene expression and DNA methylation were assessed. Further, in a second cohort, we utilized primary dermal foreskin fibroblasts as a functional measure of adipogenesis in living cells (n = 11 NS and n = 8 S). Cells were stimulated with an adipogenic cocktail, mRNA was isolated from cells after 14 days, and chemerin gene expression assessed via real-time PCR. Chemerin mRNA was elevated in both whole tissue (NS: 2409.20 ± 555.28 counts and S: 2966.72 ± 636.84 counts; P < 0.01) and primary fibroblasts (NS: 1.12 ± 0.55 2^ΔΔCT and S: 2.13 ± 1.34 2^ΔΔCT; P = 0.04) collected from infants born to smoking mothers. Chemerin DNA methylation was reduced in whole tissue of offspring born to smokers (NS: 4.18 ± 1.28 and S: 3.07 ± 1.31%; P = 0.02), which may contribute to the increased gene expression. Neonates born to mothers who smoke during pregnancy exhibit distinct changes in chemerin gene expression in response to in utero tobacco smoke exposure which are regulated in part by epigenetic alterations.

Original language	English
Pages (from-to)	93-99
Number of pages	7
Journal	Experimental Physiology
Volume	104
Issue number	1
DOIs	https://doi.org/10.1113/EP087307
State	Published - Jan 1 2019

Bibliographical note

Publisher Copyright:
© 2018 The Authors. Experimental Physiology © 2018 The Physiological Society

Funding

Funding was provided by the National Institutes of Health (1R56ES025188 to K.J.P. and R01ES022223toC.J.M).L.J.R.wassupported by an American Heart Association Post-Doctoral Fellowship (15POST25110002). informationFunding was provided by the National Institutes of Health (1R56ES025188 to K.J.P. and R01ES022223 to C.J.M). L.J.R. was supported by an American Heart Association Post-Doctoral Fellowship (15POST25110002).We would like to also thank R. Pollack, MD, for assistance with tissue collection. The experiments were conducted by K.J.P.?s Laboratory at the University of Kentucky, Department of Pharmacology and Nutritional Sciences or by the Laboratory of C.J.M. (DNA methylation assays). L.J.R., N.R.C and K.J.P contributed to the conception and design of the study; L.J.R., N.R.C., L.B.D., J.D.P, J.M.O, D.A.A., C.J.M., H.F.M. and K.J.P contributed to the collection, analysis and/or interpretation of the data collected; and L.J.R., N.R.C., L.B.D., J.D.P, J.M.O, D.A.A., C.J.M., H.F.M. and K.J.P, contributed to drafting of the manuscript and/or revising critically for important intellectual content. All authors have approved the final version of the manuscript. All authors agree to be accountable for all aspects of the manuscript in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All persons designated as authors qualify for authorship, and all those who qualify for authorship are listed. The authors have no conflicts of interest to report.

Funders	Funder number
National Institutes of Health (NIH)	R01ES022223toC.J.M
National Institute of Environmental Health Sciences (NIEHS)	R56ES025188
American Heart Association	15POST25110002

Keywords

cigarette
developmental programming
foreskin

ASJC Scopus subject areas

Physiology
Nutrition and Dietetics
Physiology (medical)

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1113/EP087307

Cite this

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title = "Smoking during pregnancy increases chemerin expression in neonatal tissue",

abstract = "New Findings: What is the central question of this study? Is chemerin, an adipokine implicated in obesity, increased in neonates following in utero cigarette smoke exposure. What is the main finding and its importance? Chemerin mRNA expression was increased and chemerin DNA methylation was decreased in babies born to mothers who smoked during pregnancy. These data provide a potential mechanism that may be mediating the increased obesity risk in individuals that are born to mothers who smoked during pregnancy. Abstract: It has been shown that in utero tobacco exposure increases offspring risk for obesity, but the mechanisms responsible for this increased risk are not well understood. Chemerin is an adipokine that regulates adipocyte differentiation. This chemokine is elevated in obese individuals and with smoke exposure, but its levels have not been measured in neonates exposed to cigarette smoke in utero. We examined chemerin gene expression [n = 31 non-smoker (NS) and 15 smoker (S)] and DNA methylation (n = 28 NS and n = 11 S) in skin collected from babies born to mothers who smoked during pregnancy as compared to non-smoking controls. Quality RNA and DNA were isolated from foreskin tissue following circumcision, and chemerin gene expression and DNA methylation were assessed. Further, in a second cohort, we utilized primary dermal foreskin fibroblasts as a functional measure of adipogenesis in living cells (n = 11 NS and n = 8 S). Cells were stimulated with an adipogenic cocktail, mRNA was isolated from cells after 14 days, and chemerin gene expression assessed via real-time PCR. Chemerin mRNA was elevated in both whole tissue (NS: 2409.20 ± 555.28 counts and S: 2966.72 ± 636.84 counts; P < 0.01) and primary fibroblasts (NS: 1.12 ± 0.55 2ΔΔCT and S: 2.13 ± 1.34 2ΔΔCT; P = 0.04) collected from infants born to smoking mothers. Chemerin DNA methylation was reduced in whole tissue of offspring born to smokers (NS: 4.18 ± 1.28 and S: 3.07 ± 1.31%; P = 0.02), which may contribute to the increased gene expression. Neonates born to mothers who smoke during pregnancy exhibit distinct changes in chemerin gene expression in response to in utero tobacco smoke exposure which are regulated in part by epigenetic alterations.",

keywords = "cigarette, developmental programming, foreskin",

author = "Reynolds, {Leryn J.} and Chavan, {Niraj R.} and DeHoff, {Logan B.} and Preston, {Joshua D.} and Maddox, {Hannah F.} and O'Brien, {John M.} and Armstrong, {David A.} and Marsit, {Carmen J.} and Pearson, {Kevin J.}",

note = "Publisher Copyright: {\textcopyright} 2018 The Authors. Experimental Physiology {\textcopyright} 2018 The Physiological Society",

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AU - Reynolds, Leryn J.

AU - Chavan, Niraj R.

AU - DeHoff, Logan B.

AU - Preston, Joshua D.

AU - Maddox, Hannah F.

AU - O'Brien, John M.

AU - Armstrong, David A.

AU - Marsit, Carmen J.

AU - Pearson, Kevin J.

PY - 2019/1/1

Y1 - 2019/1/1

N2 - New Findings: What is the central question of this study? Is chemerin, an adipokine implicated in obesity, increased in neonates following in utero cigarette smoke exposure. What is the main finding and its importance? Chemerin mRNA expression was increased and chemerin DNA methylation was decreased in babies born to mothers who smoked during pregnancy. These data provide a potential mechanism that may be mediating the increased obesity risk in individuals that are born to mothers who smoked during pregnancy. Abstract: It has been shown that in utero tobacco exposure increases offspring risk for obesity, but the mechanisms responsible for this increased risk are not well understood. Chemerin is an adipokine that regulates adipocyte differentiation. This chemokine is elevated in obese individuals and with smoke exposure, but its levels have not been measured in neonates exposed to cigarette smoke in utero. We examined chemerin gene expression [n = 31 non-smoker (NS) and 15 smoker (S)] and DNA methylation (n = 28 NS and n = 11 S) in skin collected from babies born to mothers who smoked during pregnancy as compared to non-smoking controls. Quality RNA and DNA were isolated from foreskin tissue following circumcision, and chemerin gene expression and DNA methylation were assessed. Further, in a second cohort, we utilized primary dermal foreskin fibroblasts as a functional measure of adipogenesis in living cells (n = 11 NS and n = 8 S). Cells were stimulated with an adipogenic cocktail, mRNA was isolated from cells after 14 days, and chemerin gene expression assessed via real-time PCR. Chemerin mRNA was elevated in both whole tissue (NS: 2409.20 ± 555.28 counts and S: 2966.72 ± 636.84 counts; P < 0.01) and primary fibroblasts (NS: 1.12 ± 0.55 2ΔΔCT and S: 2.13 ± 1.34 2ΔΔCT; P = 0.04) collected from infants born to smoking mothers. Chemerin DNA methylation was reduced in whole tissue of offspring born to smokers (NS: 4.18 ± 1.28 and S: 3.07 ± 1.31%; P = 0.02), which may contribute to the increased gene expression. Neonates born to mothers who smoke during pregnancy exhibit distinct changes in chemerin gene expression in response to in utero tobacco smoke exposure which are regulated in part by epigenetic alterations.

AB - New Findings: What is the central question of this study? Is chemerin, an adipokine implicated in obesity, increased in neonates following in utero cigarette smoke exposure. What is the main finding and its importance? Chemerin mRNA expression was increased and chemerin DNA methylation was decreased in babies born to mothers who smoked during pregnancy. These data provide a potential mechanism that may be mediating the increased obesity risk in individuals that are born to mothers who smoked during pregnancy. Abstract: It has been shown that in utero tobacco exposure increases offspring risk for obesity, but the mechanisms responsible for this increased risk are not well understood. Chemerin is an adipokine that regulates adipocyte differentiation. This chemokine is elevated in obese individuals and with smoke exposure, but its levels have not been measured in neonates exposed to cigarette smoke in utero. We examined chemerin gene expression [n = 31 non-smoker (NS) and 15 smoker (S)] and DNA methylation (n = 28 NS and n = 11 S) in skin collected from babies born to mothers who smoked during pregnancy as compared to non-smoking controls. Quality RNA and DNA were isolated from foreskin tissue following circumcision, and chemerin gene expression and DNA methylation were assessed. Further, in a second cohort, we utilized primary dermal foreskin fibroblasts as a functional measure of adipogenesis in living cells (n = 11 NS and n = 8 S). Cells were stimulated with an adipogenic cocktail, mRNA was isolated from cells after 14 days, and chemerin gene expression assessed via real-time PCR. Chemerin mRNA was elevated in both whole tissue (NS: 2409.20 ± 555.28 counts and S: 2966.72 ± 636.84 counts; P < 0.01) and primary fibroblasts (NS: 1.12 ± 0.55 2ΔΔCT and S: 2.13 ± 1.34 2ΔΔCT; P = 0.04) collected from infants born to smoking mothers. Chemerin DNA methylation was reduced in whole tissue of offspring born to smokers (NS: 4.18 ± 1.28 and S: 3.07 ± 1.31%; P = 0.02), which may contribute to the increased gene expression. Neonates born to mothers who smoke during pregnancy exhibit distinct changes in chemerin gene expression in response to in utero tobacco smoke exposure which are regulated in part by epigenetic alterations.

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Smoking during pregnancy increases chemerin expression in neonatal tissue

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

UN SDGs

Access to Document

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