From Neuroimunomodulation to Bioelectronic Treatment of Rheumatoid Arthritis

References

• Firestein GS . Evolving concepts of rheumatoid arthritis . Nature423, 356 – 361 (2003).
   PubMed Web of Science ®Google Scholar
• Silman AJ , PearsonJE . Epidemiology and genetics of rheumatoid arthritis . Arthritis Res.4, S265 (2002).
   PubMedGoogle Scholar
• Edrees AF , MisraSN, AbdouNI . Anti-tumor necrosis factor (TNF) therapy in rheumatoid arthritis: correlation of TNF-α serum level with clinical response and benefit from changing dose or frequency of infliximab infusions . Clin. Exp. Rheumatol.23, 469 – 474 .
   PubMed Web of Science ®Google Scholar
• Inui K , KoikeT . Combination therapy with biologic agents in rheumatic diseases: current and future prospects . Ther. Adv. Musculoskelet. Dis.8, 192 – 202 (2016).
   PubMed Web of Science ®Google Scholar
• Upchurch KS , KayJ . Evolution of treatment for rheumatoid arthritisRheumatology (Oxford)51 (Suppl. 6), vi28 – vi36 (2012).
   PubMed Web of Science ®Google Scholar
• Mertens M , SinghJA . Anakinra for rheumatoid arthritis: a systematic review . J. Rheumatol.36, 1118 – 1125 (2009).
   PubMed Web of Science ®Google Scholar
• Singh JA , ChristensenR, WellsGAet al. Biologics for rheumatoid arthritis: an overview of Cochrane reviews . In : Cochrane Database of Systematic Reviews . SinghJA ( Ed.). John Wiley & Sons, Ltd, Chichester, UK, p CD007848 (2009).
   Google Scholar
• Raimondo MG , BiggioggeroM, CrottiC, BeccioliniA, FavalliEG . Profile of sarilumab and its potential in the treatment of rheumatoid arthritis . Drug Des. Devel. Ther.11, 1593 – 1603 (2017).
   PubMed Web of Science ®Google Scholar
• Tanaka T , NarazakiM, KishimotoT . Interleukin (IL-6) immunotherapy . Cold Spring Harb. Perspect. Biol.a028456 (2017).
   Web of Science ®Google Scholar
• Emery P , KeystoneE, TonyHPet al. IL-6 receptor inhibition with tocilizumab improves treatment outcomes in patients with rheumatoid arthritis refractory to anti-tumour necrosis factor biologicals: results from a 24-week multicentre randomised placebo-controlled trial . Ann. Rheum. Dis.67, 1516 – 1523 (2008).
   PubMed Web of Science ®Google Scholar
• Favalli EG , DesiatiF, AtzeniFet al. Serious infections during anti-TNFα treatment in rheumatoid arthritis patients . Autoimmun. Rev.8, 266 – 273 (2009).
   PubMed Web of Science ®Google Scholar
• Inanc N , DireskeneliH . Serious infections under treatment with TNF-α antagonists compared to traditional DMARDs in patients with rheumatoid arthritis . Rheumatol. Int.27, 67 – 71 (2006).
   PubMed Web of Science ®Google Scholar
• Yamanaka H . TNF as a target of inflammation in rheumatoid arthritis . Endocr. Metab. Immune Disord. Drug Targets15, 129 – 134 (2015).
   PubMed Web of Science ®Google Scholar
• Ulloa L , Quiroz-GonzalezS, Torres-RosasR . Nerve stimulation: immunomodulation and control of inflammation . Trends Mol. Med.23, 1103 – 1120 (2017).
   PubMed Web of Science ®Google Scholar
• Tracey KJ . The inflammatory reflex . Nature420, 853 – 859 (2002).
   PubMed Web of Science ®Google Scholar
• Chavan SS , PavlovVA, TraceyKJ . Mechanisms and therapeutic relevance of neuro-immune communication . Immunity46, 927 – 942 (2017).
   PubMed Web of Science ®Google Scholar
• Hoover DB . Cholinergic modulation of the immune system presents new approaches for treating inflammation . Pharmacol. Ther.179, 1 – 16 (2017).
   PubMed Web of Science ®Google Scholar
• Waldburger J-M , FiresteinGS . Regulation of peripheral inflammation by the central nervous system . Curr. Rheumatol. Rep.12, 370 – 378 (2010).
   PubMedGoogle Scholar
• Borovikova LV , IvanovaS, ZhangMet al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin . Nature405, 458 – 462 (2000).
   PubMed Web of Science ®Google Scholar
• Bonaz B , SinnigerV, PellissierS . Vagus nerve stimulation: a new promising therapeutic tool in inflammatory bowel disease . J. Intern. Med.282, 46 – 63 (2017).
   PubMed Web of Science ®Google Scholar
• De Herdt V , PuimegeL, De WaeleJet al. Increased rat serum corticosterone suggests immunomodulation by stimulation of the vagal nerve . J. Neuroimmunol.212, 102 – 105 (2009).
   PubMed Web of Science ®Google Scholar
• Koopman FA , van MaanenMA, VervoordeldonkMJ, TakPP . Balancing the autonomic nervous system to reduce inflammation in rheumatoid arthritis . J. Intern. Med.282, 64 – 75 (2017).
   PubMed Web of Science ®Google Scholar
• van Maanen MA , VervoordeldonkMJ, TakPP . The cholinergic anti-inflammatory pathway: towards innovative treatment of rheumatoid arthritis . Nat. Rev. Rheumatol.5, 229 – 232 (2009).
   PubMed Web of Science ®Google Scholar
• Bassi GS , DiasDPM, FranchinMet al. Modulation of experimental arthritis by vagal sensory and central brain stimulation . Brain, Behav. Immun.64, 330 – 343 (2017).
   PubMed Web of Science ®Google Scholar
• Tak PP . Interview with Paul-Peter Tak: stimulating the vagus nerve to treat rheumatoid arthritis . Bioelectron. Med.1 (1), 17 – 20 (2018).
   Google Scholar
• Levine YA , KoopmanFA, FaltysMet al. Neurostimulation of the cholinergic anti-inflammatory pathway ameliorates disease in rat collagen-induced arthritis . PloS ONE9, e104530 (2014).
   PubMed Web of Science ®Google Scholar
• Koopman FA , ChavanSS, MiljkoSet al. Vagus nerve stimulation inhibits cytokine production and attenuates disease severity in rheumatoid arthritis . Proc. Natl Acad. Sci. USA113, 8284 – 8289 (2016).
   PubMed Web of Science ®Google Scholar
• Martelli D , McKinleyMJ, McAllenRM . The cholinergic anti-inflammatory pathway: a critical review . Auton. Neurosci.182, 65 – 69 (2014).
   PubMed Web of Science ®Google Scholar
• Bassi GS , UlloaL, SantosVRet al. Cortical stimulation in conscious rats controls joint inflammation. Progress in neuro-psychopharmacology and biological psychiatry . 84, 201 – 213 (2018).
   Google Scholar
• Cai B , DongW, SharpeS, DeitchEA, UlloaL . Survival and inflammatory responses in experimental models of hemorrhage . J. Surg. Res.169, 257 – 266 (2011).
   PubMed Web of Science ®Google Scholar
• Ulloa L , DeitchEA . Neuroimmune perspectives in sepsis . Crit. Care13, 133 (2009).
   PubMed Web of Science ®Google Scholar
• Ulloa L , TraceyKJ . The ‘cytokine profile’: a code for sepsis . Trends Mol. Med.11, 56 – 63 (2005).
   PubMed Web of Science ®Google Scholar
• Kanashiro A , SônegoF, FerreiraRGet al. Therapeutic potential and limitations of cholinergic anti-inflammatory pathway in sepsis . Pharmacol. Res.117, 1 – 8 (2017).
   PubMed Web of Science ®Google Scholar
• Cai B , DeitchEA, UlloaL . Novel insights for systemic inflammation in sepsis and hemorrhage . Mediators Inflamm.2010, 1 – 10 (2010).
   Web of Science ®Google Scholar
• Ulloa L . The vagus nerve and the nicotinic anti-inflammatory pathway . Nat. Rev. Drug Discov.4, 673 – 684 (2005).
   PubMed Web of Science ®Google Scholar
• Rasmussen SE , Pfeiffer-JensenM, DrewesAMet al. Vagal influences in rheumatoid arthritis . Scand. J. Rheumatol.47, 1 – 11 (2018).
   PubMed Web of Science ®Google Scholar
• Zhang Q , LuY, BianH, GuoL, ZhuH . Activation of the α7 nicotinic receptor promotes lipopolysaccharide-induced conversion of M1 microglia to M2 . Am. J. Transl. Res.9, 971 – 985 (2017).
   PubMed Web of Science ®Google Scholar
• Pinheiro NM , SantanaFPR, AlmeidaRRet al. Acute lung injury is reduced by the α7nAChR agonist PNU-282987 through changes in the macrophage profile . FASEB J.31, 320 – 332 (2017).
   PubMed Web of Science ®Google Scholar
• Watkins LR , GoehlerLE, ReltonJKet al. Blockade of interleukin-1 induced hyperthermia by subdiaphragmatic vagotomy: evidence for vagal mediation of immune-brain communication . Neurosci. Lett.183, 27 – 31 (1995).
   PubMed Web of Science ®Google Scholar
• Ardell JL , RajendranPS, NierHA, KenKnightBH, ArmourJA . Central-peripheral neural network interactions evoked by vagus nerve stimulation: functional consequences on control of cardiac function . Am. J. Physiol. Heart Circ. Physiol.309, H1740-52 (2015).
   PubMed Web of Science ®Google Scholar
• Kember G , ArdellJL, ArmourJA, ZamirM . Vagal nerve stimulation therapy: what is being stimulated?PLoS ONE9, e114498 (2014).
   PubMed Web of Science ®Google Scholar
• Rosas-Ballina M , OlofssonPS, OchaniMet al. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit . Science334, 98 – 101 (2011).
   PubMed Web of Science ®Google Scholar
• Rosas-Ballina M , OchaniM, ParrishWRet al. Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia . Proc. Natl Acad. Sci. USA105, 11008 – 11013 (2008).
   PubMed Web of Science ®Google Scholar
• Bratton BO , MartelliD, McKinleyMJ, TrevaksD, AndersonCR, McAllenRM . Neural regulation of inflammation: no neural connection from the vagus to splenic sympathetic neurons . Exp. Physiol.97, 1180 – 1185 (2012).
   PubMed Web of Science ®Google Scholar
• Romanovsky AA . The inflammatory reflex: the current model should be revised . Exp. Physiol.97, 1178 – 1179 (2012).
   PubMed Web of Science ®Google Scholar
• Grimsholm O , Rantapää-DahlqvistS, DalénT, ForsgrenS . Unexpected finding of a marked non-neuronal cholinergic system in human knee joint synovial tissue . Neurosci. Lett.442, 128 – 133 (2008).
   PubMed Web of Science ®Google Scholar
• Vida G , PeñaG, DeitchEA, UlloaL . α7-cholinergic receptor mediates vagal induction of splenic norepinephrine . J. Immunol.186, 4340 – 4346 (2011).
   PubMed Web of Science ®Google Scholar
• Vida G , PeñaG, KanashiroAet al. β2-adrenoreceptors of regulatory lymphocytes are essential for vagal neuromodulation of the innate immune system . FASEB J.25, 4476 – 4485 (2011).
   PubMed Web of Science ®Google Scholar
• Pena G , CaiB, RamosL, VidaG, DeitchEA, UlloaL . Cholinergic regulatory lymphocytes re-establish neuromodulation of innate immune responses in sepsis . J. Immunol.187, 718 – 725 (2011).
   PubMed Web of Science ®Google Scholar
• Pavlov VA , TraceyKJ . Neural circuitry and immunity . Immunol. Res.63, 38 – 57 (2015).
   PubMed Web of Science ®Google Scholar
• Huston JM , OchaniM, Rosas-BallinaMet al. Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis . J. Exp. Med.203, 1623 – 1628 (2006).
   PubMed Web of Science ®Google Scholar
• Wang H , YuM, OchaniMet al. Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation . Nature421, 384 – 388 (2002).
   PubMed Web of Science ®Google Scholar
• Bernik TR , FriedmanSG, OchaniMet al. Cholinergic antiinflammatory pathway inhibition of tumor necrosis factor during ischemia reperfusion . J. Vas. Surg.36, 1231 – 1236 (2002).
   PubMed Web of Science ®Google Scholar
• Altavilla D , GuariniS, BittoAet al. Activation of the cholinergic anti-inflammatory pathway reduces NF-κB activation, blunts TNF-α production, and protects againts splanchic artery occlusion shock . Shock25, 500 – 506 (2006).
   PubMed Web of Science ®Google Scholar
• Cai B , ChenF, JiYet al. Alpha7 cholinergic-agonist prevents systemic inflammation and improves survival during resuscitation . J. Cell. Mol. Med.13, 3774 – 3785 (2009).
   PubMed Web of Science ®Google Scholar
• Grech D , LiZ, MorcilloPet al. Intraoperative low-frequency electroacupuncture under general anesthesia improves postoperative recovery in a randomized trial . J. Acupunct. Meridian Stud.9, 234 – 241 (2016).
   PubMedGoogle Scholar
• van Westerloo DJ , GiebelenIA, FlorquinSet al. The vagus nerve and nicotinic receptors modulate experimental pancreatitis severity in mice . Gastroenterology130, 1822 – 1830 (2006).
   PubMed Web of Science ®Google Scholar
• Wang H , LiaoH, OchaniMet al. Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis . Nat. Med.10, 1216 – 1221 (2004).
   PubMed Web of Science ®Google Scholar
• van Westerloo DJ , GiebelenIAJ, FlorquinSet al. The cholinergic anti-inflammatory pathway regulates the host response during septic peritonitis . J. Infect. Dis.191, 2138 – 2148 (2005).
   PubMed Web of Science ®Google Scholar
• Tracey KJ , FongY, HesseDGet al. Anti-cachectin/TNF monoclonal antibodies prevent septic shock during lethal bacteraemia . Nature330, 662 – 664 (1987).
   PubMed Web of Science ®Google Scholar
• Carré JE , SingerM . Cellular energetic metabolism in sepsis: the need for a systems approach . Biochim. Biophys. Acta1777, 763 – 771 (2008).
   PubMed Web of Science ®Google Scholar
• Remick D , ManoharP, BolgosG, RodriguezJ, MoldawerL, WollenbergG . Blockade of tumor necrosis factor reduces lipopolysaccharide lethality, but not the lethality of cecal ligation and puncture . Shock4, 89 – 95 (1995).
   PubMed Web of Science ®Google Scholar
• Eskandari MK , BolgosG, MillerC, NguyenDT, DeForgeLE, RemickDG . Anti-tumor necrosis factor antibody therapy fails to prevent lethality after cecal ligation and puncture or endotoxemia . J. Immunol.148, 2724 – 2730 (1992).
   PubMed Web of Science ®Google Scholar
• Peña G , CaiB, LiuJet al. Unphosphorylated STAT3 modulates alpha7 nicotinic receptor signaling and cytokine production in sepsis . Eur. J. Immunol.40, 2580 – 2589 (2010).
   PubMed Web of Science ®Google Scholar
• Peña G , CaiB, DeitchEA, UlloaL . JAK2 inhibition prevents innate immune responses and rescues animals from sepsis . J. Mol. Med.88, 851 – 859 (2010).
   PubMed Web of Science ®Google Scholar
• Ulloa L . The cholinergic anti-inflammatory pathway meets microRNA . Cell Res.23, 1249 – 1250 (2013).
   PubMed Web of Science ®Google Scholar
• Pullan RD , RhodesJ, GaneshSet al. Transdermal nicotine for active ulcerative colitis . N. Engl. J. Med.330, 811 – 815 (1994).
   PubMed Web of Science ®Google Scholar
• Cho Y-G , ChoM-L, MinS-Y, KimH-Y . Type II collagen autoimmunity in a mouse model of human rheumatoid arthritis . Autoimmun. Rev.7, 65 – 70 (2007).
   PubMed Web of Science ®Google Scholar
• Lindblad SS , MydelP, JonssonI-M, SeniorRM, TarkowskiA, BokarewaM . Smoking and nicotine exposure delay development of collagen-induced arthritis in mice . Arthritis Res. Ther.11, R88 (2009).
   PubMed Web of Science ®Google Scholar
• van Maanen MA , LebreMC, van der PollTet al. Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice . Arthritis Rheum.60, 114 – 122 (2009).
   PubMed Web of Science ®Google Scholar
• Li T , ZuoX, ZhouYet 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.30, 213 – 220 (2010).
   PubMed Web of Science ®Google Scholar
• van Maanen MA , StoofSP, LaRosaGJ, VervoordeldonkMJ, TakPP . Role of the cholinergic nervous system in rheumatoid arthritis: aggravation of arthritis in nicotinic acetylcholine receptor 7 subunit gene knockout mice . Ann. Rheum. Dis.69, 1717 – 1723 (2010).
   PubMed Web of Science ®Google Scholar
• Bruchfeld A , GoldsteinRS, ChavanSet al. Whole blood cytokine attenuation by cholinergic agonists ex vivo and relationship to vagus nerve activity in rheumatoid arthritis . J. Intern. Med.268, 94 – 101 (2010).
   PubMed Web of Science ®Google Scholar
• Waldburger J-M , BoyleDL, PavlovVA, TraceyKJ, FiresteinGS . Acetylcholine regulation of synoviocyte cytokine expression by the alpha7 nicotinic receptor . Arthritis Rheum.58, 3439 – 3449 (2008).
   PubMedGoogle Scholar
• Wu S , LuoH, XiaoX, ZhangH, LiT, ZuoX . Attenuation of collagen induced arthritis via suppression on Th17 response by activating cholinergic anti-inflammatory pathway with nicotine . Eur. J. Pharmacol.735, 97 – 104 (2014).
   PubMed Web of Science ®Google Scholar
• Yang Y , YangY, YangJ, XieR, RenY, FanH . Regulatory effect of nicotine on collagen-induced arthritis and on the induction and function of in vitro-cultured Th17 cells . Mod. Rheumatol.24, 781 – 787 (2014).
   PubMed Web of Science ®Google Scholar
• Li S , ZhouB, LiuBet al. Activation of the cholinergic anti-inflammatory system by nicotine attenuates arthritis via suppression of macrophage migration . Mol. Med. Rep.14, 5057 – 5064 (2016).
   PubMed Web of Science ®Google Scholar
• Kotake S , UdagawaN, TakahashiNet al. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis . J. Clin. Invest.103, 1345 – 1352 (1999).
   PubMed Web of Science ®Google Scholar
• Shahrara S , PickensSR, DorfleutnerA, PopeRM . IL-17 induces monocyte migration in rheumatoid arthritis . J. Immunol.182, 3884 – 3891 (2009).
   PubMed Web of Science ®Google Scholar
• Ziolkowska M , KocA, LuszczykiewiczGet al. High levels of IL-17 in rheumatoid arthritis patients: IL-15 triggers in vitro IL-17 production via cyclosporin A-sensitive mechanism . J. Immunol.164, 2832 – 2838 (2000).
   PubMed Web of Science ®Google Scholar
• Ivanov II , McKenzieBS, ZhouLet al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells . Cell126, 1121 – 1133 (2006).
   PubMed Web of Science ®Google Scholar
• Park H , LiZ, YangXOet al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17 . Nat. immunol.6, 1133 – 1141 (2005).
   PubMed Web of Science ®Google Scholar
• Harrington LE , HattonRD, ManganPRet al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages . Nat. Immunol.6, 1123 – 1132 (2005).
   PubMed Web of Science ®Google Scholar
• Bettelli E , CarrierY, GaoWet al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells . Nature441, 235 – 238 (2006).
   PubMed Web of Science ®Google Scholar
• Hoeve MA , SavageNDL, de BoerTet al. Divergent effects of IL-12 and IL-23 on the production of IL-17 by human T cells . Eur. J. Immunol.36, 661 – 670 (2006).
   PubMed Web of Science ®Google Scholar
• Wang D , ZhouR, YaoYet al. Stimulation of α7 nicotinic acetylcholine receptor by nicotine increases suppressive capacity of naturally occurring CD4+CD25+ regulatory T cells in mice in vitro . J. Pharmacol. Exp. Ther.335, 553 – 561 (2010).
   PubMed Web of Science ®Google Scholar
• Grando SA , PittelkowMR, SchallreuterKU . Adrenergic and cholinergic control in the biology of epidermis: physiological and clinical significance . J. Investig. Dermatol.126, 1948 – 1965 (2006).
   PubMed Web of Science ®Google Scholar
• Leite PEC , GandíaL, de PascualRet al. Selective activation of α7 nicotinic acetylcholine receptor (nAChRα7) inhibits muscular degeneration in mdx dystrophic mice . Brain Res.1573, 27 – 36 (2014).
   PubMed Web of Science ®Google Scholar
• Kurzen H , BergerH, JägerCet al. Phenotypical and molecular profiling of the extraneuronal cholinergic system of the skin . J. Investig. Dermatol.123, 937 – 949 (2004).
   PubMed Web of Science ®Google Scholar
• Pereira MR , LeitePEC . The involvement of parasympathetic and sympathetic nerve in the inflammatory reflex . J. Cell. Physiol.231, 1862 – 1869 (2016).
   PubMed Web of Science ®Google Scholar
• Westman M , EngströmM, CatrinaAI, LampaJ . Cell specific synovial expression of nicotinic alpha 7 acetylcholine receptor in rheumatoid arthritis and psoriatic arthritis . Scand. J. Immunol.70, 136 – 140 (2009).
   PubMed Web of Science ®Google Scholar
• Van Maanen MA , StoofSP, Van Der ZandenEPet al. The α7 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.60, 1272 – 1281 (2009).
   PubMedGoogle Scholar
• Zhou Y , ZuoX, LiY, WangY, ZhaoH, XiaoX . Nicotine inhibits tumor necrosis factor-α induced IL-6 and IL-8 secretion in fibroblast-like synoviocytes from patients with rheumatoid arthritis . Rheumatol. Int.32, 97 – 104 (2012).
   PubMed Web of Science ®Google Scholar
• Hosseinzadeh A , ThompsonPR, SegalBH, UrbanCF . Nicotine induces neutrophil extracellular traps . J. Leukoc. Biol.100, 1105 – 1112 (2016).
   PubMed Web of Science ®Google Scholar
• Lee J , LuriaA, RhodesCet al. Nicotine drives neutrophil extracellular traps formation and accelerates collagen-induced arthritis . Rheumatology (Oxford)56, kew449 (2016).
   Web of Science ®Google Scholar
• Baka Z , BuzásE, NagyG . Rheumatoid arthritis and smoking: putting the pieces together . Arthritis Res. Ther.11, 238 (2009).
   PubMed Web of Science ®Google Scholar
• Yu H , YangY-H, RajaiahR, MoudgilKD . Nicotine-induced differential modulation of autoimmune arthritis in the Lewis rat involves changes in interleukin-17 and anti-cyclic citrullinated peptide antibodies . Arthritis Rheum.63, 981 – 991 (2011).
   PubMedGoogle Scholar
• Härle P , MöbiusD, CarrDJJ, SchölmerichJ, StraubRH . An opposing time-dependent immune-modulating effect of the sympathetic nervous system conferred by altering the cytokine profile in the local lymph nodes and spleen of mice with type II collagen-induced arthritis . Arthritis Rheum.52, 1305 – 1313 (2005).
   PubMed Web of Science ®Google Scholar
• Härle P , PongratzG, AlbrechtJ, TarnerIH, StraubRH . An early sympathetic nervous system influence exacerbates collagen-induced arthritis via CD4+CD25+ cells . Arthritis Rheum.58, 2347 – 2355 (2008).
   PubMedGoogle Scholar
• Miller LE , JüstenHP, SchölmerichJ, StraubRH . The loss of sympathetic nerve fibers in the synovial tissue of patients with rheumatoid arthritis is accompanied by increased norepinephrine release from synovial macrophages . FASEB J.14, 2097 – 2107 (2000).
   PubMed Web of Science ®Google Scholar
• Capellino S , CosentinoM, WolffCet al. Catecholamine-producing cells in the synovial tissue during arthritis: modulation of sympathetic neurotransmitters as new therapeutic target . Ann. Rheum. Dis.69, 1853 – 1860 (2010).
   PubMed Web of Science ®Google Scholar
• Pongratz G , MelzerM, StraubRH . The sympathetic nervous system stimulates anti-inflammatory B cells in collagen-type II-induced arthritis . Ann. Rheum. Dis.71, 432 – 439 (2012).
   PubMed Web of Science ®Google Scholar
• Buijs RM , van der VlietJ, GaridouM-L, HuitingaI, EscobarC . Spleen vagal denervation inhibits the production of antibodies to circulating antigens . PLoS ONE3, e3152 (2008).
   PubMed Web of Science ®Google Scholar
• McAllen RM , CookAD, KhiewHW, MartelliD, HamiltonJA . The interface between cholinergic pathways and the immune system and its relevance to arthritis . Arthritis Res. Ther.17, 87 (2015).
   PubMed Web of Science ®Google Scholar
• Li T , ZuoX, ZhouYet 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.30, 213 – 220 (2010).
   PubMed Web of Science ®Google Scholar
• Simons CT , KulchitskyVA, SugimotoN, HomerLD, SzékelyM, RomanovskyAA . Signaling the brain in systemic inflammation: which vagal branch is involved in fever genesis?Am. J. Physiol.275, R63-R68 (1998).
   Google Scholar
• Kimpel D , DaytonT, FuselerJet al. Splenectomy attenuates streptococcal cell wall-induced arthritis and alters leukocyte activation . Arthritis Rheum.48, 3557 – 3567 (2003).
   PubMedGoogle Scholar
• Rahman J , StainesNA . Contribution of the spleen, lymph nodes and bone marrow to the antibody response in collagen-induced arthritis in the rat . Clin. Exp. Immunol.85, 48 – 54 (1991).
   PubMed Web of Science ®Google Scholar
• Bassi GS , BrognaraF, CastaniaJAet al. Baroreflex activation in conscious rats modulates the joint inflammatory response via sympathetic function . Brain Behav. Immun.49, 140 – 147 (2015).
   PubMed Web of Science ®Google Scholar
• Balint GP , BalintPV . Felty's syndrome . Best pract. Res. Clin. Rheumatol.18, 631 – 645 (2004).
   PubMed Web of Science ®Google Scholar
• Bradley JD , PinalsRS . Felty's syndrome presenting without arthritis . Clin. Exp. Rheumatol.1, 257 – 259 (1983).
   PubMed Web of Science ®Google Scholar
• Uluhan A , SagerD, JasinHE . Juvenile rheumatoid arthritis and common variable hypogammaglobulinemia . J. Rheumatol.25, 1205 – 1210 (1998).
   PubMedGoogle Scholar
• Matteoli G , Gomez-PinillaPJ, NemethovaAet al. A distinct vagal anti-inflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen . Gut63, 938 – 948 (2014).
   PubMed Web of Science ®Google Scholar
• Olofsson PS , LavineY, CaravacaAet al. Single-pulse and unidirectional electrical activation of the cervical vagus nerve reduces tumor necrosis factor in endotoxemia . Bioelectron. Med.2, 37 – 42 (2015).
   Google Scholar
• Inoue T , AbeC, SungSJet al. Vagus nerve stimulation mediates protection from kidney ischemia-reperfusion injury through α7nAChR+ splenocytes . J. Clin. Investig.126, 1939 – 1952 (2016).
   PubMed Web of Science ®Google Scholar
• Verlinden TJM , RijkersK, HooglandG, HerrlerA . Morphology of the human cervical vagus nerve: implications for vagus nerve stimulation treatment . Acta Neurol. Scand.133, 173 – 182 (2016).
   PubMed Web of Science ®Google Scholar
• Seki A , GreenHR, LeeTDet al. Sympathetic nerve fibers in human cervical and thoracic vagus nerves . Heart Rhythm11, 1411 – 1417 (2014).
   PubMed Web of Science ®Google Scholar
• Kox M , van EijkLT, ZwaagJet al. Voluntary activation of the sympathetic nervous system and attenuation of the innate immune response in humans . Proc. Natl Acad. Sci. USA111, 7379 – 7384 (2014).
   PubMed Web of Science ®Google Scholar
• Martelli D , YaoST, ManceraJ, McKinleyMJ, McAllenRM . Reflex control of inflammation by the splanchnic anti-inflammatory pathway is sustained and independent of anesthesia . Am. J. Physiol. Regul. Integr. Comp. Physiol.307, R1085 – R1091 (2014).
   PubMed Web of Science ®Google Scholar
• Elenkov IJ , HaskóG, KovácsKJ, ViziES . Modulation of lipopolysaccharide-induced tumor necrosis factor-alpha production by selective alpha- and beta-adrenergic drugs in mice . J. Neuroimmunol.61, 123 – 131 (1995).
   PubMed Web of Science ®Google Scholar
• Abe C , InoueT, InglisMAet al. C1 neurons mediate a stress-induced anti-inflammatory reflex in mice . Nat. Neurosci.20, 700 – 707 (2017).
   PubMed Web of Science ®Google Scholar
• Clark KB , NaritokuDK, SmithDC, BrowningRA, JensenRA . Enhanced recognition memory following vagus nerve stimulation in human subjects . Nat. Neurosci.2, 94 – 98 (1999).
   PubMed Web of Science ®Google Scholar
• Barnes A , DuncanR, ChisholmJAet al. Investigation into the mechanisms of vagus nerve stimulation for the treatment of intractable epilepsy, using 99mTc-HMPAO SPET brain images . Eur. J. Nucl. Med. Mol. Imaging30, 301 – 305 (2003).
   PubMed Web of Science ®Google Scholar
• Henry TR , BakayRA, VotawJRet al. Brain blood flow alterations induced by therapeutic vagus nerve stimulation in partial epilepsy: I. Acute effects at high and low levels of stimulation . Epilepsia39, 983 – 990 (1998).
   PubMed Web of Science ®Google Scholar
• Naritoku DK , TerryWJ, HelfertRH . Regional induction of fos immunoreactivity in the brain by anticonvulsant stimulation of the vagus nerve . Epilepsy Res.22, 53 – 62 (1995).
   PubMed Web of Science ®Google Scholar
• Cunningham JT , MifflinSW, GouldGG, FrazerA . Induction of c-Fos and DeltaFosB immunoreactivity in rat brain by vagal nerve stimulation . Neuropsychopharmacology33, 1884 – 1895 (2008).
   PubMed Web of Science ®Google Scholar
• Thompson M , BywatersEG . Unilateral rheumatoid arthritis following hemiplegia . Ann. Rheum. Dis.21, 370 – 377 (1962).
   PubMed Web of Science ®Google Scholar
• Glick EN . Asymmetrical rheumatoid arthritis after poliomyelitis . BMJ3, 26 – 28 (1967).
   PubMed Web of Science ®Google Scholar
• Hamilton S . Unilateral rheumatoid arthritis in hemiplegia . J. Can. Assoc. Radiol.34, 49 – 50 (1983).
   PubMedGoogle Scholar
• Lapadula G , IannoneF, ZuccaroC, CovelliM, GrattaglianoV, PipitoneV . Recovery of erosive rheumatoid arthritis after human immunodeficiency virus-1 infection and hemiplegia . J. Rheumatol.24, 747 – 751 (1997).
   PubMed Web of Science ®Google Scholar
• Stangenberg L , BurzynD, BinstadtBAet al. Denervation protects limbs from inflammatory arthritis via an impact on the microvasculature . Proc. Natl Acad. Sci. USA111, 11419 – 11424 (2014).
   PubMed Web of Science ®Google Scholar
• Coderre TJ , ChanAK, HelmsC, BasbaumAI, LevineJD . Increasing sympathetic nerve terminal-dependent plasma extravasation correlates with decreased arthritic joint injury in rats . Neuroscience40, 185 – 189 (1991).
   PubMed Web of Science ®Google Scholar
• Green PG , MiaoFJ, JänigW, LevineJD . Negative feedback neuroendocrine control of the inflammatory response in rats . The J. Neurosci.15, 4678 – 4686 (1995).
   PubMed Web of Science ®Google Scholar
• Miao FJ , JänigW, LevineJD . Vagal branches involved in inhibition of bradykinin-induced synovial plasma extravasation by intrathecal nicotine and noxious stimulation in the rat . J. Physiol.498 (Pt 2), 473 – 481 (1997).
   PubMed Web of Science ®Google Scholar
• Miao FJ , GreenPG, CoderreTJ, JänigW, LevineJD . Sympathetic-dependence in bradykinin-induced synovial plasma extravasation is dose-related . Neurosci. Lett.205, 165 – 168 (1996).
   PubMed Web of Science ®Google Scholar
• Miao FJ , JänigW, DallmanMFet al. Role of vagal afferents and spinal pathways modulating inhibition of bradykinin-induced plasma extravasation by intrathecal nicotine . J. Neurophysiol.72, 1199 – 1207 (1994).
   PubMed Web of Science ®Google Scholar
• Martelli D , YaoST, McKinleyMJ, McAllenRM . Reflex control of inflammation by sympathetic nerves, not the vagus . J. Physiol.592, 1677 – 1686 (2014).
   PubMed Web of Science ®Google Scholar
• Willemze RA , LuyerMD, BuurmanWA, de JongeWJ . Neural reflex pathways in intestinal inflammation: hypotheses to viable therapy . Nat. Rev. Gastroenterol. Hepatol.12, 353 – 362 (2015).
   PubMed Web of Science ®Google Scholar
• Levine YA , KoopmanFA, FaltysMet al. Neurostimulation of the cholinergic anti-inflammatory pathway ameliorates disease in rat collagen-induced arthritis . PLoS ONE9, e104530 (2014).
   PubMed Web of Science ®Google Scholar
• Schaible H-G , StraubRH . Function of the sympathetic supply in acute and chronic experimental joint inflammation . Auton. Neurosci.182, 55 – 64 (2014).
   PubMed Web of Science ®Google Scholar
• Sato Y , SchaibleHG . Discharge characteristics of sympathetic efferents to the knee joint of the cat . J. Auton. Nerv. Sys.19, 95 – 103 (1987).
   PubMedGoogle Scholar
• Benarroch EE . The arterial baroreflex: functional organization and involvement in neurologic disease . Neurology71, 1733 – 1738 (2008).
   PubMed Web of Science ®Google Scholar
• Vitale F , LittB . Bioelectronics: the promise of leveraging the body's circuitry to treat disease . Bioelectron. Med.1, 3 – 7 (2018).
   Google Scholar
• Rehman AA , ElmoreKB, MatteiTA . The effects of alternating electric fields in glioblastoma: current evidence on therapeutic mechanisms and clinical outcomes . Neurosurg. focus38, E14 (2015).
   PubMed Web of Science ®Google Scholar
• Shawki MM , FaridA . Low electric field parameters required to induce death of cancer cells . Electromagn. Biol. Med.33, 159 – 163 (2014).
   PubMed Web of Science ®Google Scholar
• Birmingham K , GradinaruV, AnikeevaPet al. Bioelectronic medicines: a research roadmap . Nat. Rev. Drug Dis.13, 399 – 400 (2014).
   PubMed Web of Science ®Google Scholar
• Suzuki K , NakaiA . Immune modulation by neuronal electric shock waves . J. Allergy Clin. Immunol. doi: 10.1016/j.jaci.2018.02.027 (2018) ( Epub ahead of print).
   Web of Science ®Google Scholar
• Murray K , ReardonC . The cholinergic anti-inflammatory pathway revisited . Neurogastroenterol. Motil.30, e13288 (2018).
   Web of Science ®Google Scholar
• Botha C , FarmerAD, NilssonMet al. Preliminary report: modulation of parasympathetic nervous system tone influences oesophageal pain hypersensitivity . Gut64, 611 – 617 (2015).
   PubMed Web of Science ®Google Scholar
• Wheless JW , BaumgartnerJ . Vagus nerve stimulation therapy . Drugs Today40, 501 – 515 (2004).
   PubMed Web of Science ®Google Scholar
• Carreno FR , FrazerA . Vagal nerve stimulation for treatment-resistant depression . Neurotherapeutics14, 716 – 727 (2017).
   PubMed Web of Science ®Google Scholar
• Mwamburi M , LieblerEJ, TenagliaAT . Review of non-invasive vagus nerve stimulation (gammaCore): efficacy, safety, potential impact on comorbidities, and economic burden for episodic and chronic cluster headache . Am. J. Manag. Care23, S317 – S325 (2017).
   PubMed Web of Science ®Google Scholar
• Simon B , BlakeJ . Mechanism of action of non-invasive cervical vagus nerve stimulation for the treatment of primary headaches . Am. J. Manag. care23, S312 – S316 (2017).
   PubMedGoogle Scholar
• Stefan H , KreiselmeyerG, KerlingFet al. Transcutaneous vagus nerve stimulation (t-VNS) in pharmacoresistant epilepsies: a proof of concept trial . Epilepsia53, e115 – e118 (2012).
   PubMed Web of Science ®Google Scholar
• Lerman I , HaugerR, SorkinLet al. Noninvasive transcutaneous vagus nerve stimulation decreases whole blood culture-derived cytokines and chemokines: a randomized, blinded, healthy control pilot trial . Neuromodulation19, 283 – 290 (2016).
   PubMed Web of Science ®Google Scholar
• Brock C , BrockB, AzizQet al. Transcutaneous cervical vagal nerve stimulation modulates cardiac vagal tone and tumor necrosis factor-alpha . Neurogastroenterol. Motil.29, e12999 (2017).
   Web of Science ®Google Scholar
• Zhao YX , HeW, JingXHet al. Transcutaneous auricular vagus nerve stimulation protects endotoxemic rat from lipopolysaccharide-induced inflammation . Evid.-Based Complementary Altern. Med.2012, 1 – 10 (2012).
   Web of Science ®Google Scholar
• Nakai A , HayanoY, FurutaF, NodaM, SuzukiK . Control of lymphocyte egress from lymph nodes through β 2 -adrenergic receptors . J. Exp. Med.211, 2583 – 2598 (2014).
   PubMed Web of Science ®Google Scholar
• Kanashiro A , TalbotJ, PeresRSet al. Neutrophil recruitment and articular hyperalgesia in antigen-induced arthritis are modulated by the cholinergic anti-inflammatory pathway . Basic Clin. Pharmacol. Toxicol.119, 453 – 457 (2016).
   PubMed Web of Science ®Google Scholar
• Gowayed MA , RefaatR, AhmedWM, El-AbharHS . Effect of galantamine on adjuvant-induced arthritis in rats . Eur. J. Pharmacol.764, 547 – 553 (2015).
   PubMed Web of Science ®Google Scholar
• Malfait AM , MalikAS, Marinova-MutafchievaL, ButlerDM, MainiRN, FeldmannM . The beta2-adrenergic agonist salbutamol is a potent suppressor of established collagen-induced arthritis: mechanisms of action . J. Immunol.162, 6278 – 6283 (1999).
   PubMed Web of Science ®Google Scholar
• Cobelens PM , KavelaarsA, VroonAet al. The beta 2-adrenergic agonist salbutamol potentiates oral induction of tolerance, suppressing adjuvant arthritis and antigen-specific immunity . J. Immunol.169, 5028 – 5035 (2002).
   PubMed Web of Science ®Google Scholar
• Pavlov VA , OchaniM, Gallowitsch-PuertaMet al. Central muscarinic cholinergic regulation of the systemic inflammatory response during endotoxemia . Proc. Natl Acad. Sci. USA103, 5219 – 5223 (2006).
   PubMed Web of Science ®Google Scholar
• Beckmann J , DittmannN, SchützI, KleinJ, LipsKS . Effect of M3 muscarinic acetylcholine receptor deficiency on collagen antibody-induced arthritis . Arthritis Res. Ther.18, 17 (2016).
   PubMed Web of Science ®Google Scholar
• Delgado M , AbadC, MartinezCet al. Vasoactive intestinal peptide in the immune system: potential therapeutic role in inflammatory and autoimmune diseases . J. Mol. Med.80, 16 – 24 (2002).
   PubMed Web of Science ®Google Scholar
• Kanashiro A , FranchinM, BassiGSet al. Inhibition of spinal p38 MAPK prevents articular neutrophil infiltration in experimental arthritis via sympathetic activation . Fundam. Clin. Pharmacol.32, 155 – 162 (2017).
   PubMed Web of Science ®Google Scholar
• Bassi GS , do C MalvarD, CunhaTM, CunhaFQ, KanashiroA . Spinal GABA-B receptor modulates neutrophil recruitment to the knee joint in zymosan-induced arthritis . Naunyn Schmiedeberg Arc. Pharmacol.389, 851 – 861 (2016).
   Google Scholar
• Boyle DL , JonesTL, HammakerDet al. Regulation of peripheral inflammation by spinal p38 MAP kinase in rats . PLoS Med.3, e338 (2016).
   Google Scholar
• Bruchfeld A , GoldsteinRS, ChavanSet al. Whole blood cytokine attenuation by cholinergic agonists ex vivo and relationship to vagus nerve activity in rheumatoid arthritis . J. Intern. Med.268, 94 – 101 (2010).
   PubMed Web of Science ®Google Scholar
• Evrengul H , DursunogluD, CobankaraVet al. Heart rate variability in patients with rheumatoid arthritis . Rheumatol. Int.24, 198 – 202 (2004).
   PubMed Web of Science ®Google Scholar
• Goldstein RS , BruchfeldA, YangLet al. Cholinergic anti-inflammatory pathway activity and High Mobility Group Box-1 (HMGB1) serum levels in patients with rheumatoid arthritis . Mol. Med.13, 210 – 215 (2007).
   PubMed Web of Science ®Google Scholar
• Koopman FA , TangMW, VermeijJet al. Autonomic dysfunction precedes development of rheumatoid arthritis: a prospective cohort study . EBioMedicine6, 231 – 237 (2016).
   PubMed Web of Science ®Google Scholar
• Holman AJ , NgE . Heart rate variability predicts anti-tumor necrosis factor therapy response for inflammatory arthritis . Auton. Neurosci.143, 58 – 67 (2008).
   PubMed Web of Science ®Google Scholar
• Gigliotti JC , HuangL, YeHet al. Ultrasound prevents renal ischemia-reperfusion injury by stimulating the splenic cholinergic anti-inflammatory pathway . J. Am. Soc. Nephrol.24, 1451 – 1460 (2013).
   PubMed Web of Science ®Google Scholar
• Torres-Rosas R , YehiaG, PenaGet al. Dopamine mediates vagal modulation of the immune system by electroacupuncture . Nat. Med.20, 291 – 295 (2014).
   PubMed Web of Science ®Google Scholar
• Zhu J , ChenX-Y, LiL-Bet al. Electroacupuncture attenuates collagen-induced arthritis in rats through vasoactive intestinal peptide signalling-dependent re-establishment of the regulatory T cell/T-helper 17 cell balance . Acupunct. Med.33, 305 – 311 (2015).
   PubMed Web of Science ®Google Scholar
• Li J , LiJ, ChenR, CaiG . Targeting NF-κB and TNF-α activation by electroacupuncture to suppress collagen-induced rheumatoid arthritis in model rats . Altern. Ther. Health Med.21, 26 – 34 (2015).
   PubMed Web of Science ®Google Scholar
• Dong Z-Q , ZhuJ, LuD, ChenQ, XuY . Effect of electroacupuncture in ‘Zusanli’ and ‘Kunlun’ acupoints on TLR4 signaling pathway of adjuvant arthritis rats . Am. J. Ther.25, 314 – 319 (2018).
   Web of Science ®Google Scholar
• Ouyang B , GaoJ, CheJet al. Effect of electro-acupuncture on tumor necrosis factor-α and vascular endothelial growth factor in peripheral blood and joint synovia of patients with rheumatoid arthritis . Chin. J. Integr. Med.17, 505 – 509 (2011).
   PubMed Web of Science ®Google Scholar
• Lu J-H , LiuY-Q, DengQ-W, PengY-P, QiuY-H . Dopamine D2 receptor is involved in alleviation of Type II collagen-induced arthritis in mice . BioMed Res. Int.2015, 496759 (2015).
   PubMed Web of Science ®Google Scholar
• Révész D , RydenhagB, Ben-MenachemE . Complications and safety of vagus nerve stimulation: 25 years of experience at a single center . J. Neurosurg. Pediatr.18, 97 – 104 (2016).
   PubMed Web of Science ®Google Scholar
• Kahlow H , OlivecronaM . Complications of vagal nerve stimulation for drug-resistant epilepsy . Seizure22, 827 – 833 (2013).
   PubMed Web of Science ®Google Scholar
• Engel O , AkyüzL, da Costa GoncalvesACet al. Cholinergic pathway suppresses pulmonary innate immunity facilitating pneumonia after stroke . Stroke46, 3232 – 3240 (2015).
   PubMed Web of Science ®Google Scholar
• Prass K , MeiselC, HöflichCet al. Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell Type 1–like immunostimulation . J. Exp. Med.198, 725 – 736 (2003).
   PubMed Web of Science ®Google Scholar
• Wong CHY , JenneCN, LeeW-Y, LégerC, KubesP . Functional innervation of hepatic iNKT cells is immunosuppressive following stroke . Science334, 101 – 105 (2011).
   PubMed Web of Science ®Google Scholar
• Irmler IM , GajdaM, KamradtT . Amelioration of experimental arthritis by stroke-induced immunosuppression is independent of Treg cell function . Ann. Rheum. Dis.73, 2183 – 2191 (2014).
   PubMed Web of Science ®Google Scholar