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Research ArticleArticle

Identification and Characterization of Poly(I:C)-induced Molecular Responses Attenuated by Nicotine in Mouse Macrophages

Wen-Yan Cui, Shufang Zhao, Renata Polanowska-Grabowska, Ju Wang, Jinxue Wei, Bhagirathi Dash, Sulie L. Chang, Jeffrey J. Saucerman, Jun Gu and Ming D. Li
Molecular Pharmacology January 2013, 83 (1) 61-72; DOI: https://doi.org/10.1124/mol.112.081497
Wen-Yan Cui
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China (W.-Y.C., M.D.L.); National Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China (W.-Y.C., J.G.); College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China (S.Z.); Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, Virginia (W.-Y.C., J.Wa., J.We., B.D., M.D.L.); Institute of NeuroImmune Pharmacology and Department of Biology, Seton Hall University, South Orange, New Jersey (S.L.C.); and Department of Biomedical Engineering, Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, Virginia (R.P., J.J.S.)
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Shufang Zhao
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China (W.-Y.C., M.D.L.); National Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China (W.-Y.C., J.G.); College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China (S.Z.); Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, Virginia (W.-Y.C., J.Wa., J.We., B.D., M.D.L.); Institute of NeuroImmune Pharmacology and Department of Biology, Seton Hall University, South Orange, New Jersey (S.L.C.); and Department of Biomedical Engineering, Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, Virginia (R.P., J.J.S.)
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Renata Polanowska-Grabowska
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China (W.-Y.C., M.D.L.); National Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China (W.-Y.C., J.G.); College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China (S.Z.); Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, Virginia (W.-Y.C., J.Wa., J.We., B.D., M.D.L.); Institute of NeuroImmune Pharmacology and Department of Biology, Seton Hall University, South Orange, New Jersey (S.L.C.); and Department of Biomedical Engineering, Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, Virginia (R.P., J.J.S.)
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Ju Wang
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China (W.-Y.C., M.D.L.); National Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China (W.-Y.C., J.G.); College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China (S.Z.); Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, Virginia (W.-Y.C., J.Wa., J.We., B.D., M.D.L.); Institute of NeuroImmune Pharmacology and Department of Biology, Seton Hall University, South Orange, New Jersey (S.L.C.); and Department of Biomedical Engineering, Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, Virginia (R.P., J.J.S.)
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Jinxue Wei
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China (W.-Y.C., M.D.L.); National Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China (W.-Y.C., J.G.); College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China (S.Z.); Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, Virginia (W.-Y.C., J.Wa., J.We., B.D., M.D.L.); Institute of NeuroImmune Pharmacology and Department of Biology, Seton Hall University, South Orange, New Jersey (S.L.C.); and Department of Biomedical Engineering, Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, Virginia (R.P., J.J.S.)
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Bhagirathi Dash
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China (W.-Y.C., M.D.L.); National Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China (W.-Y.C., J.G.); College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China (S.Z.); Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, Virginia (W.-Y.C., J.Wa., J.We., B.D., M.D.L.); Institute of NeuroImmune Pharmacology and Department of Biology, Seton Hall University, South Orange, New Jersey (S.L.C.); and Department of Biomedical Engineering, Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, Virginia (R.P., J.J.S.)
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Sulie L. Chang
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China (W.-Y.C., M.D.L.); National Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China (W.-Y.C., J.G.); College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China (S.Z.); Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, Virginia (W.-Y.C., J.Wa., J.We., B.D., M.D.L.); Institute of NeuroImmune Pharmacology and Department of Biology, Seton Hall University, South Orange, New Jersey (S.L.C.); and Department of Biomedical Engineering, Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, Virginia (R.P., J.J.S.)
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Jeffrey J. Saucerman
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China (W.-Y.C., M.D.L.); National Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China (W.-Y.C., J.G.); College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China (S.Z.); Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, Virginia (W.-Y.C., J.Wa., J.We., B.D., M.D.L.); Institute of NeuroImmune Pharmacology and Department of Biology, Seton Hall University, South Orange, New Jersey (S.L.C.); and Department of Biomedical Engineering, Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, Virginia (R.P., J.J.S.)
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Jun Gu
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China (W.-Y.C., M.D.L.); National Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China (W.-Y.C., J.G.); College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China (S.Z.); Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, Virginia (W.-Y.C., J.Wa., J.We., B.D., M.D.L.); Institute of NeuroImmune Pharmacology and Department of Biology, Seton Hall University, South Orange, New Jersey (S.L.C.); and Department of Biomedical Engineering, Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, Virginia (R.P., J.J.S.)
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Ming D. Li
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China (W.-Y.C., M.D.L.); National Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing, China (W.-Y.C., J.G.); College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China (S.Z.); Department of Psychiatry and Neurobehavioral Sciences, University of Virginia, Charlottesville, Virginia (W.-Y.C., J.Wa., J.We., B.D., M.D.L.); Institute of NeuroImmune Pharmacology and Department of Biology, Seton Hall University, South Orange, New Jersey (S.L.C.); and Department of Biomedical Engineering, Robert M. Berne Cardiovascular Research Center, University of Virginia, Charlottesville, Virginia (R.P., J.J.S.)
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Abstract

To further our understanding of the effects of nicotine on the molecular responses of macrophages during virus or virus-like infections, poly(I:C)-stimulated macrophage-like RAW264.2 cells or mouse primary peritoneal macrophages were challenged with nicotine; and their molecular responses were evaluated using a qRT-PCR array, antibody array, ELISA, Western blotting, and Ca2+ imaging. Of 51 genes expressed in the Toll-like receptor (TLR) and RIG-I-like receptor (RLR) pathways, mRNA expression of 15 genes in RAW264.7 cells was attenuated by nicotine, of which mRNA expression of IL-6, TNF-α, and IL-1β was confirmed to be attenuated in peritoneal macrophages. Concurrently, nicotine treatment attenuated the release of IL-6 and TNF-α from poly(I:C)-stimulated macrophages. However, when poly(I:C)-stimulated macrophages were challenged with nicotine plus α-bungarotoxin (α-BTX), secretion of IL-6 and TNF-α was found to be in a level seen with poly(I:C) stimulation only, indicating that α7-nAChR, a highly Ca2+ permeable ion channel sensitive to blockade by α-BTX, is involved in this process. Furthermore, results from an antibody array indicated that nicotine treatment attenuated the phosphorylation of 82 sites, including Thr286 on CaMKIIα, from poly(I:C)-stimulated RAW264.7 cells, of which 28 are expressed in the downstream cascade of Ca2+ signaling. Coincidentally, poly(I:C)-stimulated macrophages showed attenuated expression of phosphorylated CaMKIIα when pretreated with nicotine. In addition, nicotine attenuated intracellular Ca2+ signal from poly(I:C)-stimulated RAW264.7 cells. Collectively, these results indicate that poly(I:C)-induced molecular responses of macrophages could be significantly attenuated by nicotine.

Footnotes

  • The project was supported in part by the National Institutes of Health National Institute on Drug Abuse [Grants R01DA013783, R01DA016149, R01DA026356]; and the National Natural Science Foundation of China [Grant 81273223]. W.-Y.C. was partially supported by the China Scholarship Council.

  • dx.doi.org/10.1124/mol.112.081497.

  • Received July 25, 2012.
  • Accepted October 1, 2012.
  • Copyright © 2013 by The American Society for Pharmacology and Experimental Therapeutics
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Molecular Pharmacology: 83 (1)
Molecular Pharmacology
Vol. 83, Issue 1
1 Jan 2013
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Research ArticleArticle

Nicotine Regulation of TLR3-Mediated Inflammation

Wen-Yan Cui, Shufang Zhao, Renata Polanowska-Grabowska, Ju Wang, Jinxue Wei, Bhagirathi Dash, Sulie L. Chang, Jeffrey J. Saucerman, Jun Gu and Ming D. Li
Molecular Pharmacology January 1, 2013, 83 (1) 61-72; DOI: https://doi.org/10.1124/mol.112.081497

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Research ArticleArticle

Nicotine Regulation of TLR3-Mediated Inflammation

Wen-Yan Cui, Shufang Zhao, Renata Polanowska-Grabowska, Ju Wang, Jinxue Wei, Bhagirathi Dash, Sulie L. Chang, Jeffrey J. Saucerman, Jun Gu and Ming D. Li
Molecular Pharmacology January 1, 2013, 83 (1) 61-72; DOI: https://doi.org/10.1124/mol.112.081497
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