Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 283525, 20 pages
http://dx.doi.org/10.1155/2014/283525
Review Article

Vagus Nerve through 7 nAChR Modulates Lung Infection and Inflammation: Models, Cells, and Signals

Unit of Respiratory Infection and Immunity, Institut Pasteur of Shanghai, Chinese Academy of Sciences, B104, Life Science Research Building, 320 Yueyang Road, Shanghai 200031, China

Received 27 January 2014; Revised 8 May 2014; Accepted 15 May 2014; Published 20 July 2014

Academic Editor: Talma Brenner

Copyright © 2014 Haiya Wu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. V. Borovikova, S. Ivanova, M. Zhang et al., “Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin,” Nature, vol. 405, no. 6785, pp. 458–462, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Wang, M. Yu, M. Ochani et al., “Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation,” Nature, vol. 421, no. 6921, pp. 384–388, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Rosas-Ballina, P. S. Olofsson, M. Ochani et al., “Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit,” Science, vol. 334, no. 6052, pp. 98–101, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. L. B. Ware and M. A. Matthay, “The acute respiratory distress syndrome,” The New England Journal of Medicine, vol. 342, no. 18, pp. 1334–1349, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. X. Su, W. L. Jae, Z. A. Matthay et al., “Activation of the α7 nAChR reduces acid-induced acute lung injury in mice and rats,” American Journal of Respiratory Cell and Molecular Biology, vol. 37, no. 2, pp. 186–192, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Matteoli, P. J. Gomez-Pinilla, A. Nemethova et al., “A distinct vagal anti-inflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen,” Gut, vol. 63, no. 6, pp. 938–948, 2014. View at Publisher · View at Google Scholar
  7. K. J. Tracey, “The inflammatory reflex,” Nature, vol. 420, no. 6917, pp. 853–859, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. A. A. Romanovsky, “The inflammatory reflex: the current model should be revised,” Experimental Physiology, vol. 97, no. 11, pp. 1178–1179, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. J. M. Huston, M. Ochani, M. Rosas-Ballina et al., “Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis,” Journal of Experimental Medicine, vol. 203, no. 7, pp. 1623–1629, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Rosas-Ballina, M. Ochani, W. R. Parrish et al., “Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 31, pp. 11008–11013, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. U. Andersson and K. J. Tracey, “Neural reflexes in inflammation and immunity,” Journal of Experimental Medicine, vol. 209, no. 6, pp. 1057–1068, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. U. Andersson and K. J. Tracey, “Reflex principles of immunological homeostasis,” Annual Review of Immunology, vol. 30, pp. 313–335, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. V. A. Pavlov and K. J. Tracey, “The vagus nerve and the inflammatory reflex—linking immunity and metabolism,” Nature Reviews Endocrinology, vol. 8, no. 12, pp. 743–754, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. W. J. de Jonge, E. P. van der Zanden, F. O. The et al., “Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway,” Nature Immunology, vol. 6, no. 8, pp. 844–851, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Rosas-Ballina and K. J. Tracey, “The neurology of the immune system: neural reflexes regulate immunity,” Neuron, vol. 64, no. 1, pp. 28–32, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Wang, H. Liao, M. Ochani et al., “Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis,” Nature Medicine, vol. 10, no. 11, pp. 1216–1221, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. B. O. Bratton, D. Martelli, M. J. Mckinley, D. Trevaks, C. R. Anderson, and R. M. Mcallen, “Neural regulation of inflammation: no neural connection from the vagus to splenic sympathetic neurons,” Experimental Physiology, vol. 97, no. 11, pp. 1180–1185, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Martelli, S. T. Yao, M. J. McKinley, and R. M. McAllen, “Reflex control of inflammation by sympathetic nerves, not the vagus,” The Journal of Physiology, vol. 592, part 7, pp. 1677–1686, 2014. View at Google Scholar
  19. D. Martelli, M. J. McKinley, and R. M. McAllen, “The cholinergic anti-inflammatory pathway: a critical review,” Autonomic Neuroscience, vol. 182, pp. 65–69, 2014. View at Google Scholar
  20. R. Torres-Rosas, G. Yehia, G. Pena et al., “Dopamine mediates vagal modulation of the immune system by electroacupuncture,” Nature Medicine, vol. 20, no. 3, pp. 291–295, 2014. View at Publisher · View at Google Scholar
  21. S. Ogbonnaya and C. Kaliaperumal, “Vagal nerve stimulator: evolving trends,” Journal of Natural Science, Biology and Medicine, vol. 4, no. 1, pp. 8–13, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. V. A. Pavlov and K. J. Tracey, “Neural regulators of innate immune responses and inflammation,” Cellular and Molecular Life Sciences, vol. 61, no. 18, pp. 2322–2331, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. J. K. Elmquist, M. R. Ackermann, K. B. Register, R. B. Rimler, L. R. Ross, and C. D. Jacobson, “Induction of Fos-like immunoreactivity in the rat brain following Pasteurella multocida endotoxin administration,” Endocrinology, vol. 133, no. 6, pp. 3054–3057, 1993. View at Publisher · View at Google Scholar · View at Scopus
  24. L. E. Goehler, R. P. A. Gaykema, S. E. HamMacK, S. F. Maier, and L. R. Watkins, “Interleukin-1 induces c-Fos immunoreactivity in primary afferent neurons of the vagus nerve,” Brain Research, vol. 804, no. 2, pp. 306–310, 1998. View at Publisher · View at Google Scholar · View at Scopus
  25. Y.-P. Li, E. E. Baetge, and L. B. Hersh, “Cyclic AMP regulation of the human choline acetyltransferase gene,” Neurochemical Research, vol. 18, no. 3, pp. 271–275, 1993. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Irannejad, J. C. Tomshine, J. R. Tomshine et al., “Conformational biosensors reveal GPCR signalling from endosomes,” Nature, vol. 495, no. 7442, pp. 534–538, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Vida, G. Pena, E. A. Deitch, and L. Ulloa, “α7-cholinergic receptor mediates vagal induction of splenic norepinephrine,” Journal of Immunology, vol. 186, no. 7, pp. 4340–4346, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. X. Su, X. Feng, N. Terrando et al., “Dysfunction of inflammation-resolving pathways is associated with exaggerated postoperative cognitive decline in a rat model of the metabolic syndrome,” Molecular Medicine, vol. 18, no. 12, pp. 1481–1490, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. M. A. Matthay and E. Abraham, “β-adrenergic agonist therapy as a potential treatment for acute lung injury,” American Journal of Respiratory and Critical Care Medicine, vol. 173, no. 3, pp. 254–255, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. M. A. Matthay and J. Lee, “β2 adrenergic agonist therapy may enhance alveolar epithelial repair in patients with acute lung injury,” Thorax, vol. 63, no. 3, pp. 189–190, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Bosmann, J. J. Grailer, K. Zhu et al., “Anti-inflammatory effects of β2 adrenergic receptor agonists in experimental acute lung injury,” FASEB Journal, vol. 26, no. 5, pp. 2137–2144, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Song and E. R. Spindel, “Basic and clinical aspects of non-neuronal acetylcholine: expression of non-neuronal acetylcholine in lung cancer provides a new target for cancer therapy,” Journal of Pharmacological Sciences, vol. 106, no. 2, pp. 180–185, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. W. Kummer, K. S. Lips, and U. Pfeil, “The epithelial cholinergic system of the airways,” Histochemistry and Cell Biology, vol. 130, no. 2, pp. 219–234, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Kawashima and T. Fujii, “Expression of non-neuronal acetylcholine in lymphocytes and its contribution to the regulation of immune function,” Frontiers in Bioscience, vol. 9, pp. 2063–2085, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. K. S. Lips, A. Lührmann, T. Tschernig et al., “Down-regulation of the non-neuronal acetylcholine synthesis and release machinery in acute allergic airway inflammation of rat and mouse,” Life Sciences, vol. 80, no. 24-25, pp. 2263–2269, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. S. M. Ferguson, M. Bazalakova, V. Savchenko, J. C. Tapia, J. Wright, and R. D. Blakely, “Lethal impairment of cholinergic neurotransmission in hemicholinium-3-sensitive choline transporter knockout mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 23, pp. 8762–8767, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Matsuo, J. Bellier, M. Nishimura, O. Yasuhara, N. Saito, and H. Kimura, “Nuclear choline acetyltransferase activates transcription of a high-affinity choline transporter,” The Journal of Biological Chemistry, vol. 286, no. 7, pp. 5836–5845, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. J. P. Wiener-Kronish, M. A. Gropper, and M. A. Matthay, “The adult respiratory distress syndrome: definition and prognosis, pathogenesis and treatment,” British Journal of Anaesthesia, vol. 65, no. 1, pp. 107–129, 1990. View at Publisher · View at Google Scholar · View at Scopus
  39. J. F. Pittet, R. C. Mackersie, T. R. Martin, and M. A. Matthay, “Biological markers of acute lung injury: prognostic and pathogenetic significance,” The American Journal of Respiratory and Critical Care Medicine, vol. 155, no. 4, pp. 1187–1205, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. R. A. Kaslovsky, K. Parker, A. Siflinger-Birnboim, and A. B. Malik, “Increased endothelial permeability after neutrophil activation occurs by a diffusion-dependent mechanism,” Microvascular Research, vol. 49, no. 2, pp. 227–232, 1995. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Gardinali, E. Borrelli, O. Chiara et al., “Inhibition of CD11-CD18 complex prevents acute lung injury and reduces mortality after peritonitis in rabbits,” The American Journal of Respiratory and Critical Care Medicine, vol. 161, no. 3, part 1, pp. 1022–1029, 2000. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Y. Zhou, S. K. Lo, M. Bergenfeldt et al., “In vivo expression of neutrophil inhibitory factor via gene transfer prevents lipopolysaccharide-induced lung neutrophil infiltration and injury by a beta2 integrin-dependent mechanism,” The Journal of Clinical Investigation, vol. 101, no. 11, pp. 2427–2437, 1998. View at Google Scholar
  43. A. A. Fowler, R. F. Hamman, J. T. Good et al., “Adult respiratory distress syndrome: risk with common predispositions,” Annals of Internal Medicine, vol. 98, no. 5, pp. 593–597, 1983. View at Publisher · View at Google Scholar · View at Scopus
  44. L. D. Hudson, J. A. Milberg, D. Anardi, and R. J. Maunder, “Clinical risks for development of the acute respiratory distress syndrome,” American Journal of Respiratory and Critical Care Medicine, vol. 151, no. 2, part 1, pp. 293–301, 1995. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Madjdpour, S. Kneller, C. Booy, T. Pasch, R. C. Schimmer, and B. Beck-Schimmer, “Acid-induced lung injury: role of nuclear factor-κB,” Anesthesiology, vol. 99, no. 6, pp. 1323–1332, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. M. A. Matthay and J. P. Wiener-Kronish, “Intact epithelial barrier function is critical for the resolution of alveolar edema in humans,” American Review of Respiratory Disease, vol. 142, no. 6, pp. 1250–1257, 1990. View at Publisher · View at Google Scholar · View at Scopus
  47. L. B. Ware and M. A. Matthay, “Alveolar fluid clearance is impaired in the majority of patients with acute lung injury and the acute respiratory distress syndrome,” The American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 6, pp. 1376–1383, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Rezaiguia, C. Garat, C. Delclaux et al., “Acute bacterial pneumonia in rats increases alveolar epithelial fluid clearance by a tumor necrosis factor-alpha-dependent mechanism,” The Journal of Clinical Investigation, vol. 99, no. 2, pp. 325–335, 1997. View at Publisher · View at Google Scholar · View at Scopus
  49. X. Su and M. A. Matthay, “Role of protease activated receptor 2 in experimental acute lung injury and lung fibrosis,” Anatomical Record, vol. 292, no. 4, pp. 580–586, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. X. Su, M. A. Matthay, and A. B. Malik, “Requisite role of the cholinergic α7 nicotinic acetylcholine receptor pathway in suppressing gram-negative sepsis-induced acute lung inflammatory injury,” Journal of Immunology, vol. 184, no. 1, pp. 401–410, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Zhao, E. M. Su, X. Yang et al., “Important role of platelets in modulating endotoxin-induced lung inflammation in CFTR-deficient mice,” PLoS ONE, vol. 8, no. 12, Article ID e82683, 2013. View at Publisher · View at Google Scholar
  52. F. Brégeon, F. Xeridat, N. Andreotti et al., “Activation of nicotinic cholinergic receptors prevents ventilator-induced lung injury in rats,” PLoS ONE, vol. 6, no. 8, Article ID e22386, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Kox, J. C. Pompe, E. Peters et al., “α7 Nicotinic acetylcholine receptor agonist GTS-21 attenuates ventilator-induced tumour necrosis factor-α production and lung injury,” British Journal of Anaesthesia, vol. 107, no. 4, pp. 559–566, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. C. C. dos Santos, Y. Shan, A. Akram, A. S. Slutsky, and J. J. Haitsma, “Neuroimmune regulation of ventilator-induced lung injury,” The American Journal of Respiratory and Critical Care Medicine, vol. 183, no. 4, pp. 471–482, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. X. Su, M. R. Looney, N. Gupta, and M. A. Matthay, “Receptor for advanced glycation end-products (RAGE) is an indicator of direct lung injury in models of experimental lung injury,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 297, no. 1, pp. L1–L5, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. X. Su, C. Bai, Q. Hong et al., “Effect of continuous hemofiltration on hemodynamics, lung inflammation and pulmonary edema in a canine model of acute lung injury,” Intensive Care Medicine, vol. 29, no. 11, pp. 2034–2042, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. L. Wang, D. M. Zhu, X. Su, C. X. Bai, L. B. Ware, and M. A. Matthay, “Acute cardiopulmonary effects of a dual-endothelin receptor antagonist on oleic acid-induced pulmonary arterial hypertension in dogs,” Experimental Lung Research, vol. 30, no. 1, pp. 31–42, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. M. R. Looney, X. Su, J. A. van Ziffle, C. A. Lowell, and M. A. Matthay, “Neutrophils and their Fcγ receptors are essential in a mouse model of transfusion-related acute lung injury,” Journal of Clinical Investigation, vol. 116, no. 6, pp. 1615–1623, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Hall, A. Kumaria, and A. Belli, “The role of vagus nerve overactivity in the increased incidence of pneumonia following traumatic brain injury,” British Journal of Neurosurgery, vol. 28, no. 2, pp. 181–186, 2014. View at Google Scholar
  60. J. D. Tutor, C. M. Mason, E. Dobard, R. C. Beckerman, W. R. Summer, and S. Nelson, “Loss of compartmentalization of alveolar tumor necrosis factor after lung injury,” The American Journal of Respiratory and Critical Care Medicine, vol. 149, no. 5, pp. 1107–1111, 1994. View at Publisher · View at Google Scholar · View at Scopus
  61. P. Zhang, S. Nelson, M. C. Holmes, W. R. Summer, and G. J. Bagby, “Compartmentalization of macrophage inflammatory protein-2, but not cytokine-induced neutrophil chemoattractant, in rats challenged with intratracheal endotoxin,” Shock, vol. 17, no. 2, pp. 104–108, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Inoue, S. Horio, M. Ichinose et al., “Changes in bronchial reactivity to acetylcholine with Type C influenza virus infection in dogs,” American Review of Respiratory Disease, vol. 133, no. 3, pp. 367–371, 1986. View at Google Scholar · View at Scopus
  63. K. Matsuda, C. H. Park, Y. Sunden et al., “The vagus nerve is one route of transneural invasion for intranasally inoculated influenza A virus in mice,” Veterinary Pathology, vol. 41, no. 2, pp. 101–107, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Razani-Boroujerdi, S. P. Singh, C. Knall et al., “Chronic nicotine inhibits inflammation and promotes influenza infection,” Cellular Immunology, vol. 230, no. 1, pp. 1–9, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. I. A. J. Giebelen, M. Leendertse, S. Florquin, and T. van der Poll, “Stimulation of acetylcholine receptors impairs host defence during pneumococcal pneumonia,” European Respiratory Journal, vol. 33, no. 2, pp. 375–381, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Rosas-Ballina, R. S. Goldstein, M. Gallowitsch-Puerta et al., “The selective α7 agonist GTS-21 attenuates cytokine production in human whole blood and human monocytes activated by ligands for TLR2, TLR3, TLR4, TLR9, and RAGE,” Molecular Medicine, vol. 15, no. 7-8, pp. 195–202, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Lafargue, L. Xu, M. Carlès et al., “Stroke-induced activation of the α7 nicotinic receptor increases Pseudomonas aeruginosa lung injury,” FASEB Journal, vol. 26, no. 7, pp. 2919–2929, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. G. Matute-Bello, C. W. Frevert, and T. R. Martin, “Animal models of acute lung injury,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 295, no. 3, pp. L379–L399, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. X. Yang, C. Zhao, Z. Gao, and X. Su, “A novel regulator of lung inflammation and immunity: pulmonary parasympathetic inflammatory reflex,” Quarterly Journal of Medicine, 2014. View at Publisher · View at Google Scholar
  70. B. Fox, T. B. Bull, and A. Guz, “Innervation of alveolar walls in the human lung: an electron microscopic study,” Journal of Anatomy, vol. 131, part 4, pp. 683–692, 1980. View at Google Scholar · View at Scopus
  71. M. S. Hertweck and K. S. Hung, “Ultrastructural evidence for the innervation of human pulmonary alveoli,” Experientia, vol. 36, no. 1, pp. 112–113, 1980. View at Publisher · View at Google Scholar · View at Scopus
  72. T. Hosoi, Y. Okuma, T. Matsuda, and Y. Nomura, “Novel pathway for LPS-induced afferent vagus nerve activation: possible role of nodose ganglion,” Autonomic Neuroscience, vol. 120, no. 1-2, pp. 104–107, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. A. Diogenes, C. C. R. Ferraz, A. N. Akopian, M. A. Henry, and K. M. Hargreaves, “LPS sensitizes TRPV1 via activation of TLR4 in trigeminal sensory neurons,” Journal of Dental Research, vol. 90, no. 6, pp. 759–764, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. T. Liu, Y. Gao, and R. Ji, “Emerging role of Toll-like receptors in the control of pain and itch,” Neuroscience Bulletin, vol. 28, no. 2, pp. 131–144, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. N. J. Domnik and E. Cutz, “Pulmonary neuroepithelial bodies as airway sensors: putative role in the generation of dyspnea,” Current Opinion in Pharmacology, vol. 11, no. 3, pp. 211–217, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. X. Su, “Leading neutrophils to the alveoli: who is the guider?” American Journal of Respiratory and Critical Care Medicine, vol. 186, no. 6, pp. 472–473, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. C. Reardon, G. S. Duncan, A. Brüstle et al., “Lymphocyte-derived ACh regulates local innate but not adaptive immunity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 4, pp. 1410–1415, 2013. View at Publisher · View at Google Scholar · View at Scopus
  78. W. F. Xiao, J. Lindstrom, and E. R. Spindel, “Nicotine activates and up-regulates nicotinic acetylcholine receptors in bronchial epithelial cells,” The American Journal of Respiratory Cell and Molecular Biology, vol. 41, no. 1, pp. 93–99, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. Y. Wang, E. F. R. Pereira, A. D. J. Maus et al., “Human bronchial epithelial and endothelial cells express α7 nicotinic acetylcholine receptors,” Molecular Pharmacology, vol. 60, no. 6, pp. 1201–1209, 2001. View at Google Scholar · View at Scopus
  80. X. Su, M. Johansen, M. R. Looney, E. J. Brown, and M. A. Matthay, “CD47 deficiency protects mice from lipopolysaccharide-induced acute lung injury and Escherichia coli pneumonia,” Journal of Immunology, vol. 180, no. 10, pp. 6947–6953, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. N. Gupta, X. Su, B. Popov, W. L. Jae, V. Serikov, and M. A. Matthay, “Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice,” Journal of Immunology, vol. 179, no. 3, pp. 1855–1863, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. L. C. Gahring, E. Y. Enioutina, E. J. Myers et al., “Nicotinic receptor α7 expression identifies a novel hematopoietic progenitor lineage,” PLoS ONE, vol. 8, no. 3, Article ID e57481, 2013. View at Publisher · View at Google Scholar · View at Scopus
  83. J. M. Huston, M. Rosas-Ballina, X. Xue et al., “Cholinergic neural signals to the spleen down-regulate leukocyte trafficking via CD11b,” Journal of Immunology, vol. 183, no. 1, pp. 552–559, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. F. K. Swirski, M. Nahrendorf, M. Etzrodt et al., “Identification of splenic reservoir monocytes and their deployment to inflammatory sites,” Science, vol. 325, no. 5940, pp. 612–616, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. E. Abraham, “Neutrophils and acute lung injury,” Critical Care Medicine, vol. 31, no. 4, supplement, pp. S195–S199, 2003. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Matthay and X. Su, “Deficiency of AKT1 worsens acute lung inflammation and injury and decreases survival in mice,” American Journal of Respiratory and Critical Care Medicine, vol. 183, article A1109, 2011. View at Google Scholar
  87. N. J. Meyer, Y. Huang, P. A. Singleton et al., “GADD45a is a novel candidate gene in inflammatory lung injury via influences on Akt signaling,” The FASEB Journal, vol. 23, no. 5, pp. 1325–1337, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. G. Liu, Y. Bi, R. Wang et al., “Kinase AKT1 negatively controls neutrophil recruitment and function in mice,” Journal of Immunology, vol. 191, no. 5, pp. 2680–2690, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. M. Severgnini, S. Takahashi, L. M. Rozo et al., “Activation of the STAT pathway in acute lung injury,” American Journal of Physiology: Lung Cellular and Molecular Physiology, vol. 286, no. 6, pp. L1282–L1292, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. H. Gao, R. Gou, C. L. Speyer et al., “Stat3 activation in acute lung injury,” Journal of Immunology, vol. 172, no. 12, pp. 7703–7712, 2004. View at Publisher · View at Google Scholar · View at Scopus
  91. H. Yoshikawa, M. Kurokawa, N. Ozaki et al., “Nicotine inhibits the production of proinflammatory mediators in human monocytes by suppression of I-κB phosphorylation and nuclear factor-κB transcriptional activity through nicotinic acetylcholine receptor α7,” Clinical and Experimental Immunology, vol. 146, no. 1, pp. 116–123, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. R. Hamano, H. K. Takahashi, H. Iwagaki, T. Yoshino, M. Nishibori, and N. Tanaka, “Stimulation of α7 nicotinic acetylcholine receptor inhibits CD14 and the toll-like receptor 4 expression in human monocytes,” Shock, vol. 26, no. 4, pp. 358–364, 2006. View at Publisher · View at Google Scholar · View at Scopus
  93. X.-M. Song, J.-G. Li, Y.-L. Wang et al., “The protective effect of the cholinergic anti-inflammatory pathway against septic shock in rats,” Shock, vol. 30, no. 4, pp. 468–472, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. M. Kox, J. F. van Velzen, J. C. Pompe, C. W. Hoedemaekers, J. G. van der Hoeven, and P. Pickkers, “GTS-21 inhibits pro-inflammatory cytokine release independent of the Toll-like receptor stimulated via a transcriptional mechanism involving JAK2 activation,” Biochemical Pharmacology, vol. 78, no. 7, pp. 863–872, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. P. K. Chatterjee, Y. Al-Abed, B. Sherry, and C. N. Metz, “Cholinergic agonists regulate JAK2/STAT3 signaling to suppress endothelial cell activation,” The American Journal of Physiology—Cell Physiology, vol. 297, no. 5, pp. C1294–C1306, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. C. Leib, S. Göser, D. Lüthje et al., “Role of the cholinergic antiinflammatory pathway in murine autoimmune myocarditis,” Circulation Research, vol. 109, no. 2, pp. 130–140, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. G. Peña, B. Cai, J. Liu et al., “Unphosphorylated STAT3 modulates alpha7 nicotinic receptor signaling and cytokine production in sepsis,” European Journal of Immunology, vol. 40, no. 9, pp. 2580–2589, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. J. Oshikawa, Y. Toya, T. Fujita et al., “Nicotinic acetylcholine receptor α7 regulates cAMP signal within lipid rafts,” American Journal of Physiology: Cell Physiology, vol. 285, no. 3, pp. C567–C574, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. N. Ray, M. Kuwahara, Y. Takada et al., “c-Fos suppresses systemic inflammatory response to endotoxin,” International Immunology, vol. 18, no. 5, pp. 671–677, 2006. View at Publisher · View at Google Scholar · View at Scopus
  100. Y. F. Ni, F. Tian, Z. F. Lu et al., “Protective effect of nicotine on lipopolysaccharide-induced acute lung injury in mice,” Respiration, vol. 81, no. 1, pp. 39–46, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. J. Mabley, S. Gordon, and P. Pacher, “Nicotine exerts an anti-inflammatory effect in a murine model of acute lung injury,” Inflammation, vol. 34, no. 4, pp. 231–237, 2011. View at Publisher · View at Google Scholar · View at Scopus
  102. I. A. J. Giebelen, D. J. van Westerloo, G. J. LaRosa, A. F. de vos, and T. van der Poll, “Local stimulation of α7 cholinergic receptors inhibits LPS-induced TNF-α release in the mouse lung,” Shock, vol. 28, no. 6, pp. 700–703, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. C. Boland, V. Collet, E. Laterre, C. Lecuivre, X. Wittebole, and P. Laterre, “Electrical vagus nerve stimulation and nicotine effects in peritonitis-induced acute lung injury in rats,” Inflammation, vol. 34, no. 1, pp. 29–35, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. M. Kox, M. Vaneker, J. G. van der Hoeven, G. Scheffer, C. W. Hoedemaekers, and P. Pickkers, “Effects of vagus nerve stimulation and vagotomy on systemic and pulmonary inflammation in a two-hit model in rats,” PLoS ONE, vol. 7, no. 4, Article ID e34431, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. H. L. Du, Y. Yamada, R. Orii, K. Suwa, and K. Hanaoka, “Vagal and sympathetic denervation in the development of oleic acid-induced pulmonary edema,” Respiration Physiology, vol. 107, no. 3, pp. 251–261, 1997. View at Publisher · View at Google Scholar · View at Scopus
  106. H. K. Takahashi, K. Liu, H. Wake et al., “Effect of nicotine on advanced glycation end product-induced immune response in human monocytes,” Journal of Pharmacology and Experimental Therapeutics, vol. 332, no. 3, pp. 1013–1021, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. H. J. Jin, H. T. Li, H. X. Sui et al., “Nicotine stimulated bone marrow-derived dendritic cells could augment HBV specific CTL priming by activating PI3K-Akt pathway,” Immunology Letters, vol. 146, no. 1-2, pp. 40–49, 2012. View at Publisher · View at Google Scholar · View at Scopus
  108. P. S. Olofsson, D. A. Katz, M. Rosas-Ballina et al., “α7 nicotinic acetylcholine receptor (α7nAChR) expression in bone marrow-derived non-T cells is required for the inflammatory reflex,” Molecular Medicine, vol. 18, no. 1, pp. 539–543, 2012. View at Google Scholar · View at Scopus
  109. G. Vida, G. Peña, A. Kanashiro et al., “β2-adrenoreceptors of regulatory lymphocytes are essential for vagal neuromodulation of the innate immune system,” The FASEB Journal, vol. 25, no. 12, pp. 4476–4485, 2011. View at Publisher · View at Google Scholar · View at Scopus
  110. C. O'Mahony, H. van der Kleij, J. Bienenstock, F. Shanahan, and L. O'Mahony, “Loss of vagal anti-inflammatory effect: in vivo visualization and adoptive transfer,” American Journal of Physiology: Regulatory Integrative and Comparative Physiology, vol. 297, no. 4, pp. R1118–R1126, 2009. View at Publisher · View at Google Scholar · View at Scopus
  111. H. Yamaguchi, H. Friedman, and Y. Yamamoto, “Involvement of nicotinic acetylcholine receptors in controlling Chlamydia pneumoniae growth in epithelial HEp-2 cells,” Infection and Immunity, vol. 71, no. 6, pp. 3645–3647, 2003. View at Publisher · View at Google Scholar · View at Scopus
  112. K. A. Radek, P. M. Elias, L. Taupenot, S. K. Mahata, D. T. O'Connor, and R. L. Gallo, “Neuroendocrine nicotinic receptor activation increases susceptibility to bacterial infections by suppressing antimicrobial peptide production,” Cell Host and Microbe, vol. 7, no. 4, pp. 277–289, 2010. View at Publisher · View at Google Scholar · View at Scopus
  113. J. Roman and M. Koval, “Control of lung epithelial growth by a nicotinic acetylcholine receptor: the other side of the coin,” American Journal of Pathology, vol. 175, no. 5, pp. 1799–1801, 2009. View at Publisher · View at Google Scholar · View at Scopus
  114. R. W. Saeed, S. Varma, T. Peng-Nemeroff et al., “Cholinergic stimulation blocks endothelial cell activation and leukocyte recruitment during inflammation,” Journal of Experimental Medicine, vol. 201, no. 7, pp. 1113–1123, 2005. View at Publisher · View at Google Scholar · View at Scopus
  115. V. B. A. Peña, I. C. Bonini, S. S. Antollini, T. Kobayashi, and F. J. Barrantes, “α7-type acetylcholine receptor localization and its modulation by nicotine and cholesterol in vascular endothelial cells,” Journal of Cellular Biochemistry, vol. 112, no. 11, pp. 3276–3288, 2011. View at Publisher · View at Google Scholar · View at Scopus
  116. J. P. Cooke and Y. T. Ghebremariam, “Endothelial nicotinic acetylcholine receptors and angiogenesis,” Trends in Cardiovascular Medicine, vol. 18, no. 7, pp. 247–253, 2008. View at Publisher · View at Google Scholar · View at Scopus
  117. M. J. Hoogduijn, A. Cheng, and P. G. Genever, “Functional nicotinic and muscarinic receptors on mesenchymal stem cells,” Stem Cells and Development, vol. 18, no. 1, pp. 103–112, 2009. View at Publisher · View at Google Scholar · View at Scopus
  118. I. U. Schraufstatter, R. G. DiScipio, and S. K. Khaldoyanidi, “Alpha 7 subunit of nAChR regulates migration of human mesenchymal stem cells,” Journal of Stem Cells, vol. 4, no. 4, pp. 203–215, 2009. View at Google Scholar · View at Scopus
  119. M. Yu, Q. Liu, J. Sun, K. Yi, L. Wu, and X. Tan, “Nicotine improves the functional activity of late endothelial progenitor cells via nicotinic acetylcholine receptors,” Biochemistry and Cell Biology, vol. 89, no. 4, pp. 405–410, 2011. View at Publisher · View at Google Scholar · View at Scopus
  120. C. Heeschen, E. Chang, A. Aicher, and J. P. Cooke, “Endothelial progenitor cells participate in nicotine-mediated angiogenesis,” Journal of the American College of Cardiology, vol. 48, no. 12, pp. 2553–2560, 2006. View at Publisher · View at Google Scholar · View at Scopus
  121. M. Westman, M. Engström, A. I. Catrina, and J. Lampa, “Cell specific synovial expression of nicotinic alpha 7 acetylcholine receptor in rheumatoid arthritis and psoriatic arthritis,” Scandinavian Journal of Immunology, vol. 70, no. 2, pp. 136–140, 2009. View at Publisher · View at Google Scholar · View at Scopus
  122. M. A. van Maanen, S. P. Stoof, G. J. LaRosa, M. J. Vervoordeldonk, and P. P. Tak, “Role of the cholinergic nervous system in rheumatoid arthritis: aggravation of arthritis in nicotinic acetylcholine receptor α7 subunit gene knockout mice,” Annals of the Rheumatic Diseases, vol. 69, no. 9, pp. 1717–1723, 2010. View at Publisher · View at Google Scholar · View at Scopus
  123. Q. Li, X. D. Zhou, V. P. Kolosov, and J. M. Perelman, “Nicotine reduces TNF-α expression through a α7 nAChR/MyD88/NF-κB pathway in HBE16 airway epithelial cells,” Cellular Physiology and Biochemistry, vol. 27, no. 5, pp. 605–612, 2011. View at Publisher · View at Google Scholar · View at Scopus
  124. W. R. Parrish, M. Rosas-Ballina, M. Gallowitsch-Puerta et al., “Modulation of TNF release by choline requires α7 subunit nicotinic acetylcholine receptor-mediated signaling,” Molecular Medicine, vol. 14, no. 9-10, pp. 567–574, 2008. View at Publisher · View at Google Scholar · View at Scopus
  125. V. A. Pavlov, M. Ochani, L. Yang et al., “Selective α7-nicotinic acetylcholine receptor agonist GTS-21 improves survival in murine endotoxemia and severe sepsis,” Critical Care Medicine, vol. 35, no. 4, pp. 1139–1144, 2007. View at Publisher · View at Google Scholar · View at Scopus
  126. Y. Sun, Q. Li, H. Gui et al., “MicroRNA-124 mediates the cholinergic anti-inflammatory action through inhibiting the production of pro-inflammatory cytokines,” Cell Research, vol. 23, no. 11, pp. 1270–1283, 2013. View at Publisher · View at Google Scholar · View at Scopus
  127. T. Kihara, S. Shimohama, H. Sawada et al., “α7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block A beta-amyloid-induced neurotoxicity,” The Journal of Biological Chemistry, vol. 276, no. 17, pp. 13541–13546, 2001. View at Google Scholar · View at Scopus
  128. T. H. Kim, S. J. Kim, and S. M. Lee, “Stimulation of the α7 nicotinic acetylcholine receptor protects against sepsis by inhibiting Toll-like receptor via phosphoinositide 3-kinase activation,” The Journal of Infectious Diseases, vol. 209, no. 10, pp. 1668–1677, 2014. View at Publisher · View at Google Scholar
  129. M. Blanchet, E. Israël-Assayag, P. Daleau, M. Beaulieu, and Y. Cormier, “Dimethyphenylpiperazinium, a nicotinic receptor agonist, downregulates inflammation in monocytes/macrophages through PI3K and PLC chronic activation,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 291, no. 4, pp. L757–L763, 2006. View at Publisher · View at Google Scholar · View at Scopus
  130. S. Shaw, M. Bencherif, and M. B. Marrero, “Janus kinase 2, an early target of α7 nicotinic acetylcholine receptor-mediated neuroprotection against Aβ-(1–42) amyloid,” The Journal of Biological Chemistry, vol. 277, no. 47, pp. 44920–44924, 2002. View at Publisher · View at Google Scholar · View at Scopus
  131. E. J. Gubbins, M. Gopalakrishnan, and J. Li, “α7 nAChR-mediated activation of MAP kinase pathways in PC12 cells,” Brain Research, vol. 1328, pp. 1–11, 2010. View at Publisher · View at Google Scholar · View at Scopus
  132. W. Cui, J. Wang, J. Wei et al., “Modulation of innate immune-related pathways in nicotine-treated SH-SY5Y cells,” Amino Acids, vol. 43, no. 3, pp. 1157–1169, 2012. View at Publisher · View at Google Scholar · View at Scopus
  133. R. E. L. Kouhen, M. Hu, D. J. Anderson, J. Li, and M. Gopalakrishnan, “Pharmacology of α7 nicotinic acetylcholine receptor mediated extracellular signal-regulated kinase signalling in PC12 cells,” British Journal of Pharmacology, vol. 156, no. 4, pp. 638–648, 2009. View at Publisher · View at Google Scholar · View at Scopus