Vagal influences in rheumatoid arthritis

References

• Smolen JS, Aletaha D, McInnes IB. Rheumatoid arthritis. Lancet 2016;6736:1–16.
   Google Scholar
• Alamanos Y, Drosos AA. Epidemiology of adult rheumatoid arthritis. Autoimmun Rev 2005;4:130–6.
   PubMed Web of Science ®Google Scholar
• Silman AJ, Pearson JE. Epidemiology and genetics of rheumatoid arthritis. Arthritis Res 2002;4(Suppl 3):S265–72.
   PubMedGoogle Scholar
• Pedersen M, Jacobsen S, Garred P, Madsen HO, Klarlund M, Svejgaard A, et al. Strong combined gene-environment effects in anti-cyclic citrullinated peptide-positive rheumatoid arthritis: a nationwide case-control study in Denmark. Arthritis Rheum 2007;56:1446–53.
   PubMed Web of Science ®Google Scholar
• Bang SY, Lee KH, Cho SK, Lee HS, Lee KW, Bae SC. Smoking increases rheumatoid arthritis susceptibility in individuals carrying the HLA-DRB1 shared epitope, regardless of rheumatoid factor or anti-cyclic citrullinated peptide antibody status. Arthritis Rheum 2010;62:369–77.
   PubMed Web of Science ®Google Scholar
• Williams JP, Meyers JA. Immune-mediated inflammatory disorders (I.M.I.D.s): the economic and clinical costs. Am J Manag Care 2002;8(Suppl 21):S664–81; quiz S682-5.
   PubMed Web of Science ®Google Scholar
• Depont F, Berenbaum F, Filippi J, Le Maitre M, Nataf H, Paul C, et al. Interventions to improve adherence in patients with immune-mediated inflammatory disorders: a systematic review. PLoS One 2015;10:e0145076.
   PubMed Web of Science ®Google Scholar
• Nielsen PR, Kragstrup TW, Deleuran BW, Benros ME. Infections as risk factor for autoimmune diseases - a nationwide study. J Autoimmun 2016;74:176–81.
   PubMed Web of Science ®Google Scholar
• Kuek A, Hazleman BL, Ostör AJK. Immune-mediated inflammatory diseases (IMIDs) and biologic therapy: a medical revolution. Postgrad Med J 2007;83:251–60.
   PubMed Web of Science ®Google Scholar
• Smolen J, Landewé R, Breedveld F, Buch M, Burmester G, Dougados M, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2013 update. Ann Rheum Dis 2014;73:492–509.
   PubMed Web of Science ®Google Scholar
• Duru N, van der Goes MC, Jacobs JW, Andrews T, Boers M, Buttgereit F, et al. EULAR evidence-based and consensus-based recommendations on the management of medium to high-dose glucocorticoid therapy in rheumatic diseases. Ann Rheum Dis 2013;72:1905–13.
   PubMed Web of Science ®Google Scholar
• Levine YA, Koopman FA, Faltys M, Caravaca A, Bendele A, Zitnik R, et al. Neurostimulation of the cholinergic anti-inflammatory pathway ameliorates disease in rat collagen-induced arthritis. PLoS One 2014;9:e104530.
   PubMed Web of Science ®Google Scholar
• Mertens M, Singh JA. Anakinra for rheumatoid arthritis. Cochrane Database Syst Rev 2009:CD005121.
   PubMed Web of Science ®Google Scholar
• Bonaz B, Sinniger V, Pellissier S. Anti-inflammatory properties of the vagus nerve: potential therapeutic implications of vagus nerve stimulation. J Physiol 2016;594:5781–90.
   PubMed Web of Science ®Google Scholar
• Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000;405:458–62.
   PubMed Web of Science ®Google Scholar
• Majoie HJM, Rijkers K, Berfelo MW, Hulsman JARJ, Myint A, Schwarz M, et al. Vagus nerve stimulation in refractory epilepsy: effects on pro-and anti-inflammatory cytokines in peripheral blood. Neuroimmunomodulation 2011;18:52–6.
   PubMed Web of Science ®Google Scholar
• da Silva MD, Bobinski F, Sato KL, Kolker SJ, Sluka KA, Santos ARS. IL-10 cytokine released from M2 macrophages is crucial for analgesic and anti-inflammatory effects of acupuncture in a model of inflammatory muscle pain. Mol Neurobiol 2015;51:19–31.
   PubMed Web of Science ®Google Scholar
• Wu S, Luo H, Xiao X, Zhang H, Li T, Zuo X. Attenuation of collagen induced arthritis via suppression on Th17 response by activating cholinergic anti-inflammatory pathway with nicotine. Eur J Pharmacol 2014;735:97–104.
   PubMed Web of Science ®Google Scholar
• Lopez NE, Krzyzaniak M, Costantini TW, De Maio A, Baird A, Eliceiri BP, et al. Vagal nerve stimulation blocks peritoneal macrophage inflammatory responsiveness after severe burn injury. Shock 2012;38:294–300.
   PubMed Web of Science ®Google Scholar
• Li J, Hsu HC, Mountz JD. Managing macrophages in rheumatoid arthritis by reform or removal. Curr Rheumatol Rep 2012;14:445–54.
   PubMed Web of Science ®Google Scholar
• MacGregor AJ, Snieder H, Rigby AS, Koskenvuo M, Kaprio J, Aho K, et al. Characterizing the quantitative genetic contribution to rheumatoid arthritis using data from twins. Arthritis Rheum 2000;43:30–7.
   PubMed Web of Science ®Google Scholar
• Silman AJ, MacGregor AJ, Thomson W, Holligan S, Carthy D, Farhan A, et al. Twin concordance rates for rheumatoid arthritis: results from a nationwide study. Br J Rheumatol 1993;32:903–7.
   PubMedGoogle Scholar
• Okada Y, Wu D, Trynka G, Raj T, Terao C, Ikari K, et al. Genetics of rheumatoid arthritis contributes to biology and drug discovery. Nature 2014;506:376–81.
   PubMed Web of Science ®Google Scholar
• Salmond RJ, Brownlie RJ, Morrison VL, Zamoyska R. The tyrosine phosphatase PTPN22 discriminates weak self peptides from strong agonist TCR signals. Nat Immunol 2014;15:875–83.
   PubMed Web of Science ®Google Scholar
• Karimi K, Bienenstock J, Wang L, Forsythe P. The vagus nerve modulates CD4+ T cell activity. Brain Behav Immun 2010;24:316–23.
   PubMed Web of Science ®Google Scholar
• Svendsen AJ, Holm NV, Kyvik K, Petersen PH, Junker P. Relative importance of genetic effects in rheumatoid arthritis: historical cohort study of Danish nationwide twin population. BMJ 2002;324:264–6.
   PubMed Web of Science ®Google Scholar
• McInnes I. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011;365:2205–19.
   PubMed Web of Science ®Google Scholar
• Mikuls TR, Payne JB, Reinhardt RA, Thiele GM, Maziarz E, Cannella AC, et al. Antibody responses to Porphyromonas gingivalis (P. gingivalis) in subjects with rheumatoid arthritis and periodontitis. Int Immunopharmacol 2009;9:38–42.
   PubMed Web of Science ®Google Scholar
• Klareskog L, Malmström V, Lundberg K, Padyukov L, Alfredsson L. Smoking, citrullination and genetic variability in the immunopathogenesis of rheumatoid arthritis. Semin Immunol 2011;23:92–8.
   PubMed Web of Science ®Google Scholar
• Edwards JCW, Szczepański L, Szechiński J, Filipowicz-Sosnowska A, Emery P, Close DR, et al. Efficacy of B-cell–targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004;350:2572–81.
   PubMed Web of Science ®Google Scholar
• Mina-Osorio P, Rosas-Ballina M, Valdes-Ferrer SI, Al-Abed Y, Tracey KJ, Diamond B. Neural signaling in the spleen controls B-cell responses to blood-borne antigen. Mol Med 2012;18:618–27.
   PubMed Web of Science ®Google Scholar
• Gottwald T, Lhoták S, Stead RH. Effect of truncal vagotomy and capsaicin on mast cells and IgA-positive plasma cells in rat jejunal mucosa. Neurogastroenterol Motil 1997;9:25–32.
   PubMed Web of Science ®Google Scholar
• Skok M, Grailhe R, Changeux J-P. Nicotinic receptors regulate B lymphocyte activation and immune response. Eur J Pharmacol 2005;517:246–51.
   PubMed Web of Science ®Google Scholar
• Smolen JS, Steiner G. Therapeutic strategies for rheumatoid arthritis. Nat Rev Drug Discov 2003;2:473–88.
   PubMed Web of Science ®Google Scholar
• Choy E. Understanding the dynamics: pathways involved in the pathogenesis of rheumatoid arthritis. Rheumatology (Oxford) 2012;51(Suppl 5):v3–11.
   PubMed Web of Science ®Google Scholar
• Smolen JS, Landewé R, Breedveld FC, Buch M, Burmester G, Dougados M, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs. Ann Rheum Dis 2010;69:964–75.
   PubMed Web of Science ®Google Scholar
• Yoshikawa H, Kurokawa M, Ozaki N, Nara K, Atou K, Takada E, 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. Clin Exp Immunol 2006;146:116–23.
   PubMed Web of Science ®Google Scholar
• Li T, Wu S, Zhang H, Wang Y, Luo H, Zuo X, et al. Activation of nicotinic receptors inhibits TNF-α-induced production of pro-inflammatory mediators through the JAK2/STAT3 signaling pathway in fibroblast-like synoviocytes. Inflammation 2015;38:1424–33.
   PubMed Web of Science ®Google Scholar
• Villablanca AC. Nicotine stimulates DNA synthesis and proliferation in vascular endothelial cells in vitro. J Appl Physiol 1998;84:2089–98.
   PubMed Web of Science ®Google Scholar
• Heeschen C, Weis M, Cooke JP. Nicotine promotes arteriogenesis. J Am Coll Cardiol 2003;41:489–96.
   PubMed Web of Science ®Google Scholar
• Lourido L, Calamia V, Fernández-Puente P, Mateos J, Oreiro N, Blanco FJ, et al. Secretome analysis of human articular chondrocytes unravels catabolic effects of nicotine on the joint. Proteomics Clin Appl 2016;10:671–80.
   PubMed Web of Science ®Google Scholar
• Deng Y, Cao H, Cu F, Xu D, Lei Y, Tan Y, et al. Nicotine-induced retardation of chondrogenesis through down-regulation of IGF-1 signaling pathway to inhibit matrix synthesis of growth plate chondrocytes in fetal rats. Toxicol Appl Pharmacol 2013;269:25–33.
   PubMed Web of Science ®Google Scholar
• Cunnane G, Fitzgerald O, Beeton C, Cawston TE, Bresnihan B. Early joint erosions and serum levels of matrix metalloproteinase 1, matrix metalloproteinase 3, and tissue inhibitor of metalloproteinases 1 in rheumatoid arthritis. Arthritis Rheum 2001;44:2263–74.
   PubMed Web of Science ®Google Scholar
• Feldmann M, Maini RN. Anti-TNF alpha therapy of rheumatoid arthritis: what have we learned? Annu Rev Immunol 2001;19:163–96.
   PubMed Web of Science ®Google Scholar
• Mandl P, Hayer S, Karonitsch T, Scholze P, Győri D, Sykoutri D, et al. Nicotinic acetylcholine receptors modulate osteoclastogenesis. Arthritis Res Ther. Published online: 12 March 2016. doi:10.1186/s13075-016-0961-x.
   Web of Science ®Google Scholar
• Yi C, Zhang C, Hu X, Li Y, Jiang H, Xu W, et al. Vagus nerve stimulation attenuates myocardial ischemia/reperfusion injury by inhibiting the expression of interleukin-17A. Exp Ther Med 2016;11:171–6.
   PubMed Web of Science ®Google Scholar
• Zhang P, Han D, Tang T, Zhang X, Dai K. Inhibition of the development of collagen-induced arthritis in Wistar rats through vagus nerve suspension: a 3-month observation. Inflamm Res 2008;57:322–8.
   PubMed Web of Science ®Google Scholar
• Hori T, Katafuchi T, Take S, Shimizu N, Niijima A. The autonomic nervous system as a communication channel between the brain and the immune system. Neuroimmunomodulation 1995;2:203–15.
   PubMed Web of Science ®Google Scholar
• Kenney MJ, Ganta CK. Autonomic nervous system and immune system interactions. Compr Physiol 2015;4:1177–200.
   Web of Science ®Google Scholar
• Martelli D, Farmer DGS, Yao ST. The splanchnic anti-inflammatory pathway: could it be the efferent arm of the inflammatory reflex? Exp Physiol 2016;101:1245–52.
   PubMed Web of Science ®Google Scholar
• Bonaz B, Sinniger V, Pellissier S. Vagal tone: effects on sensitivity, motility, and inflammation. Neurogastroenterol Motil 2016;28:455–62.
   PubMed Web of Science ®Google Scholar
• Watkins LR, Maier SF, Goehler LE. Cytokine-to-brain communication: a review & analysis of alternative mechanisms. Life Sci 1995;57:1011–26.
   PubMed Web of Science ®Google Scholar
• Hosoi T, Okuma Y, Matsuda T, Nomura Y. Novel pathway for LPS-induced afferent vagus nerve activation: possible role of nodose ganglion. Auton Neurosci 2005;120:104–7.
   PubMed Web of Science ®Google Scholar
• Fleshner M, Goehler LE, Hermann J, Relton JK, Maier SF, Watkins LR. Interleukin-1β induced corticosterone elevation and hypothalamic NE depletion is vagally mediated. Brain Res Bull 1995;37:605–10.
   PubMed Web of Science ®Google Scholar
• Martelli D, McKinley MJ, McAllen RM. The cholinergic anti-inflammatory pathway: a critical review. Auton Neurosci 2014;182:65–9.
   PubMed Web of Science ®Google Scholar
• Tracey KJ. The inflammatory reflex. Nature 2002;420:853–9.
   PubMed Web of Science ®Google Scholar
• Borovikova LV, Ivanova S, Nardi D, Zhang M, Yang H, Ombrellino M, et al. Role of vagus nerve signaling in CNI-1493-mediated suppression of acute inflammation. Auton Neurosci 2000;85:141–7.
   PubMed Web of Science ®Google Scholar
• Bernik TR, Friedman SG, Ochani M, DiRaimo R, Ulloa L, Yang H, et al. Pharmacological stimulation of the cholinergic antiinflammatory pathway. J Exp Med 2002;195:781–8.
   PubMed Web of Science ®Google Scholar
• Pavlov VA, Tracey KJ. Controlling inflammation: the cholinergic anti-inflammatory pathway. Biochem Soc Trans 2006;34:1037–40.
   PubMed Web of Science ®Google Scholar
• Martelli D, Yao ST, Mancera J, McKinley MJ, McAllen RM. Reflex control of inflammation by the splanchnic anti-inflammatory pathway is sustained and independent of anesthesia. Am J Physiol Regul Integr Comp Physiol 2014;307:R1085–91.
   PubMed Web of Science ®Google Scholar
• Wang H, Yu M, Ochani M, Amella CA, Susarla S, Li JH, et al. Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation. Nature 2003;421:384–8.
   PubMed Web of Science ®Google Scholar
• Vida G, Peña G, Deitch EA, Ulloa L. α7-cholinergic receptor mediates vagal induction of splenic norepinephrine. J Immunol 2011;186:4340–6.
   PubMed Web of Science ®Google Scholar
• van Maanen MA, Stoof SP, van der Zanden EP, de Jonge WJ, Janssen RA, Fischer DF, et al. The alpha7 nicotinic acetylcholine receptor on fibroblast-like synoviocytes and in synovial tissue from rheumatoid arthritis patients: a possible role for a key neurotransmitter in synovial inflammation. Arthritis Rheum 2009;60:1272–81.
   PubMed Web of Science ®Google Scholar
• Huston JM, Ochani M, Rosas-Ballina M, Liao H, Ochani K, Pavlov VA, et al. Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. J Exp Med 2006;203:1623–8.
   PubMed Web of Science ®Google Scholar
• Rosas-Ballina M, Ochani M, Parrish WR, Ochani K, Harris YT, Huston JM, et al. Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. Proc Natl Acad Sci U S A 2008;105:11008–13.
   PubMed Web of Science ®Google Scholar
• Izeboud CA, Mocking JA, Monshouwer M, van Miert AS, Witkamp RF. Participation of beta-adrenergic receptors on macrophages in modulation of LPS-induced cytokine release. J Recept Signal Transduct Res 1999;19:191–202.
   PubMed Web of Science ®Google Scholar
• Bratton BO, Martelli D, McKinley MJ, Trevaks D, Anderson CR, McAllen RM. Neural regulation of inflammation: no neural connection from the vagus to splenic sympathetic neurons. Exp Physiol 2012;97:1180–5.
   PubMed Web of Science ®Google Scholar
• Rosas-Ballina M, Olofsson PS, Ochani M, Valdes-Ferrer SI, Levine YA, Reardon C, et al. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 2011;334:98–101.
   PubMed Web of Science ®Google Scholar
• Matteoli G, Gomez-Pinilla PJ, Nemethova A, Di Giovangiulio M, Cailotto C, van Bree SH, et al. A distinct vagal anti-inflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen. Gut 2013;63:938–48.
   PubMed Web of Science ®Google Scholar
• van Maanen MA, Lebre MC, van der Poll T, LaRosa GJ, Elbaum D, Vervoordeldonk MJ, et al. Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice. Arthritis Rheum 2009;60:114–22.
   PubMed Web of Science ®Google Scholar
• Li T, Zuo X, Zhou Y, Wang Y, Zhuang H, Zhang L, et al. The vagus nerve and nicotinic receptors involve inhibition of HMGB1 release and early pro-inflammatory cytokines function in collagen-induced arthritis. J Clin Immunol 2010;30:213–20.
   PubMed Web of Science ®Google Scholar
• van Maanen MA, Stoof SP, Larosa GJ, Vervoordeldonk MJ, Tak PP. Role of the cholinergic nervous system in rheumatoid arthritis: aggravation of arthritis in nicotinic acetylcholine receptor alpha7 subunit gene knockout mice. Ann Rheum Dis 2010;69:1717–23.
   PubMed Web of Science ®Google Scholar
• Miossec P, Korn T, Kuchroo VK. Interleukin-17 and type 17 helper T cells. N Engl J Med 2009;361:888–98.
   PubMed Web of Science ®Google Scholar
• Lubberts E. IL-17/Th17 targeting: on the road to prevent chronic destructive arthritis? Cytokine 2008;41:84–91.
   PubMed Web of Science ®Google Scholar
• Lubberts E, Joosten LAB, Oppers B, van den Bersselaar L, Coenen-de Roo CJJ, Kolls JK, et al. IL-1-independent role of IL-17 in synovial inflammation and joint destruction during collagen-induced arthritis. J Immunol 2001;167:1004–13.
   PubMed Web of Science ®Google Scholar
• Evrengul H, Dursunoglu D, Cobankara V, Polat B, Seleci D, Kabukcu S, et al. Heart rate variability in patients with rheumatoid arthritis. Rheumatol Int 2004;24:198–202.
   PubMed Web of Science ®Google Scholar
• Stein KS, McFarlane IC, Goldberg N, Ginzler EM. Heart rate variability in patients with systemic lupus erythematosus. Lupus 1996;5:44–8.
   PubMed Web of Science ®Google Scholar
• Westman M, Engström M, Catrina AI, Lampa J. Cell specific synovial expression of nicotinic alpha 7 acetylcholine receptor in rheumatoid arthritis and psoriatic arthritis. Scand J Immunol 2009;70:136–40.
   PubMed Web of Science ®Google Scholar
• Yuan H, Silberstein SD. Vagus nerve and vagus nerve stimulation, a comprehensive review: part II. Headache 2015;56:259–66.
   PubMed Web of Science ®Google Scholar
• Farmer AD, Albu-Soda A, Aziz Q. Vagus nerve stimulation in clinical practice. Br J Hosp Med (Lond) 2016;77:645–51.
   PubMed Web of Science ®Google Scholar
• Koopman FA, Chavan SS, Miljko S, Grazio S, Sokolovic S, Schuurman PR, et al. Vagus nerve stimulation inhibits cytokine production and attenuates disease severity in rheumatoid arthritis. Proc Natl Acad Sci 2016;113:8284–9.
   PubMed Web of Science ®Google Scholar
• Frøkjær JB, Bergmann S, Brock C, Madzak A, Farmer AD, Ellrich J, et al. Modulation of vagal tone enhances gastroduodenal motility and reduces somatic pain sensitivity. Neurogastroenterol Motil 2016;28:592–8.
   PubMed Web of Science ®Google Scholar
• Brock C, Brock B, Aziz Q, Møller HJ, Jensen MP, Drewes AM, et al. Transcutaneous cervical vagal nerve stimulation modulates cardiac vagal tone and tumor necrosis factor-alpha. Neurogastroenterol Motil 2017;29:1–4. in press. doi:10.1111/nmo.12999.
   Web of Science ®Google Scholar