The Nicotinic Receptor Alpha7 Impacts the Mouse Lung Response to LPS through Multiple Mechanisms

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Enioutina, Elena Y ^a,b   Myers, Elizabeth J ^a,b   Tvrdik, Petr ^b   Hoidal, John R ^b,c   Rogers, Scott W ^a,b   Gahring, Lorise C ^b  

^a GERIATRIC RESEARCH EDUCATION AND CLINICAL CENTER   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BUNGAROTOXIN RECEPTOR; CALCIUM ION; CD45 ANTIGEN; CHEMOKINE; CYTOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLUTAMIC ACID; INTERLEUKIN 13; INTERLEUKIN 1ALPHA; LIPOPOLYSACCHARIDE; MONOCYTE CHEMOTACTIC PROTEIN 1; RNA; TUMOR NECROSIS FACTOR ALPHA; PTPRC PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BLOOD FLOW; BONE MARROW CELL; CELL COMPOSITION; HEMATOPOIETIC CELL; HOMOLOGOUS RECOMBINATION; INFLAMMATORY CELL; ION CONDUCTANCE; KNOCKOUT MOUSE; LUNG ALVEOLUS; LUNG INTERSTITIUM; MALE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PLEIOTROPY; POINT MUTATION; REGULATORY MECHANISM; RESPIRATORY TRACT INFLAMMATION; SIGNAL TRANSDUCTION; TISSUE REACTION; ANIMAL; BRONCHOALVEOLAR LAVAGE FLUID; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; PNEUMONIA;

MUS;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; ANTIGENS, CD45; BRONCHOALVEOLAR LAVAGE FLUID; CELLS, CULTURED; CYTOKINES; GENE EXPRESSION; LIPOPOLYSACCHARIDES; LUNG; MICE; MICE, KNOCKOUT; PNEUMONIA; POINT MUTATION;

EID: 84925625551     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121128     Document Type: Article

References (41)

1. Gahring LC, Rogers SW (2005) Neuronal nicotinic acetylcholine receptor expression and function on nonneuronal cells. Aaps J 7: E885-894. PMID: 16594641
2. Pavlov VA, Tracey KJ (2005) The cholinergic anti-inflammatory pathway. Brain Behav Immun 19: 493-499. PMID: 15922555
3. Rosas-Ballina M, Tracey KJ (2009) Cholinergic control of inflammation. J Intern Med 265: 663-679. doi: 10.1111/j.1365-2796.2009.02098.x PMID: 19493060
4. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89: 73-120. doi: 10.1152/physrev.00015.2008 PMID: 19126755
5. Wang Y, Pereira EF, Maus AD, Ostlie NS, Navaneetham D, Lei S, et al. (2001) Human bronchial epithelial and endothelial cells express alpha7 nicotinic acetylcholine receptors. Mol Pharmacol 60: 1201-1209. PMID: 11723227
6. Improgo MR, Tapper AR, Gardner PD (2011) Nicotinic acetylcholine receptor-mediated mechanisms in lung cancer. Biochem Pharmacol 82: 1015-1021. doi: 10.1016/j.bcp.2011.05.020 PMID: 21640716
7. Horiguchi K, Horiguchi S, Yamashita N, Irie K, Masuda J, Takano-Ohmuro H, et al. (2009) Expression of SLURP-1, an endogenous alpha7 nicotinic acetylcholine receptor allosteric ligand, in murine bronchial epithelial cells. J Neurosci Res 87: 2740-2747. doi: 10.1002/jnr.22102 PMID: 19396877
8. Brown KC, Perry HE, Lau JK, Jones DV, Pulliam JF, Thornhill BA, et al. (2013) Nicotine induces the upregulation of the alpha7-nicotinic receptor (alpha7-nAChR) in human squamous cell lung cancer cells via the Sp1/GATA protein pathway. J Biol Chem 288: 33049-33059. doi: 10.1074/jbc.M113.501601 PMID: 24089524
9. Pavlov VA, Tracey KJ (2012) The vagus nerve and the inflammatory reflex-linking immunity and metabolism. Nat Rev Endocrinol 8: 743-754. doi: 10.1038/nrendo.2012.189 PMID: 23169440
10. Papke RL (2014) Merging old and new perspectives on nicotinic acetylcholine receptors. Biochem Pharmacol 89: 1-11. doi: 10.1016/j.bcp.2014.01.029 PMID: 24486571
11. Osborne-Hereford AV, Rogers SW, Gahring LC (2008) Neuronal nicotinic alpha7 receptors modulate inflammatory cytokine production in the skin following ultraviolet radiation. J Neuroimmunol 193: 130-139. PMID: 18077004
12. Gahring LC, Osborne AV, Reed M, Rogers SW (2010) Neuronal nicotinic alpha7 receptors modulate early neutrophil infiltration to sites of skin inflammation. J Neuroinflammation 7: 38. doi: 10.1186/1742-2094-7-38 PMID: 20624304
13. Martelli D, McKinley MJ, McAllen RM (2014) The cholinergic anti-inflammatory pathway: a critical review. Auton Neurosci 182: 65-69. doi: 10.1016/j.autneu.2013.12.007 PMID: 24411268
14. Kurzen H, Wessler I, Kirkpatrick CJ, Kawashima K, Grando SA (2007) The non-neuronal cholinergic system of human skin. Horm Metab Res 39: 125-135. PMID: 17326008
15. Zia S, Ndoye A, Nguyen VT, Grando SA (1997) Nicotine enhances expression of the alpha 3, alpha 4, alpha 5, and alpha 7 nicotinic receptors modulating calcium metabolism and regulating adhesion and motility of respiratory epithelial cells. Res Commun Mol Pathol Pharmacol 97: 243-262. PMID: 9387186
16. Sekhon HS, Jia Y, Raab R, Kuryatov A, Pankow JF, Whitsett JA, et al. (1999) Prenatal nicotine increases pulmonary alpha7 nicotinic receptor expression and alters fetal lung development in monkeys. J Clin Invest 103: 637-647. PMID: 10074480
17. Su X, Lee JW, Matthay ZA, Mednick G, Uchida T, Fang X, et al. (2007) Activation of the alpha7 nAChR reduces acid-induced acute lung injury in mice and rats. Am J Respir Cell Mol Biol 37: 186-192. PMID: 17431097
18. Aggarwal NR, King LS, D'Alessio FR (2014) Diverse macrophage populations mediate acute lung inflammation and resolution. Am J Physiol Lung Cell Mol Physiol 306: L709-725. doi: 10.1152/ajplung. 00341.2013 PMID: 24508730
19. Schneider C, Nobs SP, Heer AK, Kurrer M, Klinke G, van Rooijen N, et al. (2014) Alveolar macrophages are essential for protection from respiratory failure and associated morbidity following influenza virus infection. PLoS Pathog 10: e1004053. doi: 10.1371/journal.ppat.1004053 PMID: 24699679
20. Ji WJ, Ma YQ, Zhou X, Zhang YD, Lu RY, Sun HY, et al. (2014) Temporal and spatial characterization of mononuclear phagocytes in circulating, lung alveolar and interstitial compartments in a mouse model of bleomycin-induced pulmonary injury. J Immunol Methods 403: 7-16. doi: 10.1016/j.jim.2013.11.012 PMID: 24280595
21. Kasahara K, Matsumura Y, Ui K, Komatsu Y, Mikasa K, Kita E (2012) Intranasal priming of newborn mice with microbial extracts increases opsonic factors and mature CD11c+ cells in the airway. Am J Physiol Lung Cell Mol Physiol 303: L834-843. doi: 10.1152/ajplung.00031.2012 PMID: 22923643
22. Araz O, Demirci E, Yilmazel Ucar E, Calik M, Pulur D, Karaman A, et al. (2013) Comparison of reducing effect on lung injury of dexamethasone and bosentan in acute lung injury: an experimental study. Multidiscip Respir Med 8: 74. doi: 10.1186/2049-6958-8-74 PMID: 24342001
23. Maouche K, Medjber K, Zahm JM, Delavoie F, Terryn C, Coraux C, et al. (2013) Contribution of alpha7 nicotinic receptor to airway epithelium dysfunction under nicotine exposure. Proc Natl Acad Sci U S A 110: 4099-4104. doi: 10.1073/pnas.1216939110 PMID: 23431157
24. Lavezzi AM, Corna MF, Alfonsi G, Matturri L (2014) Possible role of the alpha7 nicotinic receptors in mediating nicotine's effect on developing lung-implications in unexplained human perinatal death. BMC Pulm Med 14: 11. doi: 10.1186/1471-2466-14-11 PMID: 24484641
25. Maouche K, Polette M, Jolly T, Medjber K, Cloez-Tayarani I, Changeux JP, et al. (2009) {alpha}7 nicotinic acetylcholine receptor regulates airway epithelium differentiation by controlling basal cell proliferation. Am J Pathol 175: 1868-1882. doi: 10.2353/ajpath.2009.090212 PMID: 19808646
26. Rogers SW, Tvrdik P, Capecchi MR, Gahring LC (2012) Prenatal ablation of nicotinic receptor alpha7 cell lineages produces lumbosacral spina bifida the severity of which is modified by choline and nicotine exposure. Am J Med Genet A 158A: 1135-1144. doi: 10.1002/ajmg.a.35372 PMID: 22473653
27. Gahring LC, Enioutina EY, Myers EJ, Spangrude GJ, Efimova OV, Kelly TW, et al. (2013) Nicotinic Receptor Alpha7 Expression Identifies a Novel Hematopoietic Progenitor Lineage. PlosOne 8: e57481. doi: 10.1371/journal.pone.0057481 PMID: 23469197
28. Rogers SW, Gahring LC (2012) Nicotinic receptor Alpha7 expression during tooth morphogenesis reveals functional pleiotropy. PLoS One 7: e36467. doi: 10.1371/journal.pone.0036467 PMID: 22666322
29. Rogers SW, Gahring LC (2012) The Expression of Nicotinic Receptor alpha7 During Cochlear Development. Brain and Behavior 2: 628-639. doi: 10.1002/brb3.84 PMID: 23139908
30. Bertrand D, Galzi JL, Devillers-Thiery A, Bertrand S, Changeux JP (1993) Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal alpha 7 nicotinic receptor. Proc Natl Acad Sci U S A 90: 6971-6975. PMID: 7688468
31. Corringer PJ, Bertrand S, Galzi JL, Devillers-Thiery A, Changeux JP, Bertrand D (1999) Molecular basis of the charge selectivity of nicotinic acetylcholine receptor and related ligand-gated ion channels. Novartis Found Symp 225: 215-224; discussion 224-230. PMID: 10472058
32. Corringer PJ, Bertrand S, Galzi JL, Devillers-Thiery A, Changeux JP, Bertrand D (1999) Mutational analysis of the charge selectivity filter of the alpha7 nicotinic acetylcholine receptor. Neuron 22: 831-843. PMID: 10230802
33. Eddins D, Lyford LK, Lee JW, Desai SA, Rosenberg RL (2002) Permeant but not impermeant divalent cations enhance activation of nondesensitizing alpha(7) nicotinic receptors. Am J Physiol Cell Physiol 282: C796-804. PMID: 11880268
34. Gahring LC, Meyer EL, Rogers SW (2003) Nicotine-induced neuroprotection against N-methyl-D-aspartic acid or beta-amyloid peptide occur through independent mechanisms distinguished by proinflammatory cytokines. J Neurochem 87: 1125-1136. PMID: 14622092
35. Morrison TB, Weis JJ, Wittwer CT (1998) Quantification of low-copy transcripts by continuous SYBR Green I monitoring during amplification. Biotechniques 24: 954-958, 960, 962. PMID: 9631186
36. Van Dyken SJ, Locksley RM (2013) Interleukin-4- and interleukin-13-mediated alternatively activated macrophages: roles in homeostasis and disease. Annu Rev Immunol 31: 317-343. doi: 10.1146/ annurev-immunol-032712-095906 PMID: 23298208
37. Gundavarapu S, Wilder JA, Mishra NC, Rir-Sima-Ah J, Langley RJ, Singh SP, et al. (2012) Role of nicotinic receptors and acetylcholine in mucous cell metaplasia, hyperplasia, and airway mucus formation in vitro and in vivo. J Allergy Clin Immunol 130: 770-780 e711. doi: 10.1016/j.jaci.2012.04.002 PMID: 22578901
38. Siegelman MH, DeGrendele HC, Estess P (1999) Activation and interaction of CD44 and hyaluronan in immunological systems. J Leukoc Biol 66: 315-321. PMID: 10449175
39. Lesley J, Hascall VC, Tammi M, Hyman R (2000) Hyaluronan binding by cell surface CD44. J Biol Chem 275: 26967-26975. PMID: 10871609
40. Nandi A, Estess P, Siegelman M (2004) Bimolecular complex between rolling and firm adhesion receptors required for cell arrest; CD44 association with VLA-4 in T cell extravasation. Immunity 20: 455-465. PMID: 15084274
41. Engleka KA, Gitler AD, Zhang M, Zhou DD, High FA, Epstein JA (2005) Insertion of Cre into the Pax3 locus creates a new allele of Splotch and identifies unexpected Pax3 derivatives. Dev Biol 280: 396-406. PMID: 15882581