Vagus nerve stimulation inhibits cytokine production and attenuates disease severity in Rheumatoid arthritis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 29, 2016, Pages 8284-8289

  Koopman, Frieda A ^a   Chavan, Sangeeta S ^b   Miljko, Sanda ^c   Grazio, Simeon ^d   Sokolovic, Sekib ^e   Schuurman, P Richard ^a   Mehta, Ashesh D ^f   Levine, Yaakov A ^g   Faltys, Michael ^g   Zitnik, Ralph ^g   Tracey, Kevin J ^b   Tak, Paul P ^a,h,i,j  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c UNIVERSITY CLINICAL HOSPITAL MOSTAR   (Bosnia and Herzegovina)

^d SESTRE MILOSRDNICE UNIVERSITY HOSPITAL   (Croatia)

^e UNIVERSITY OF SARAJEVO   (Bosnia and Herzegovina)

^f DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

^g Setpoint Medical Corporation   (United States)

^h UNIVERSITY OF CAMBRIDGE   (United Kingdom)

ⁱ GHENT UNIVERSITY   (Belgium)

^j GLAXOSMITHKLINE   (United Kingdom)

more..

Author keywords

Cytokines; Inflammatory reflex; Rheumatoid arthritis; Tumor necrosis factor; Vagus nerve

Indexed keywords

BIOLOGICAL PRODUCT; C REACTIVE PROTEIN; CYTOKINE; DISEASE MODIFYING ANTIRHEUMATIC DRUG; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 8; LYMPHOTOXIN; METHOTREXATE; PREDNISONE; TUMOR NECROSIS FACTOR;

ADULT; AGED; BIOLOGICAL THERAPY; CLINICAL ARTICLE; CONFERENCE PAPER; CORTICOSTEROID THERAPY; CYTOKINE PRODUCTION; DAS28; DISEASE SEVERITY; DRUG RESISTANT EPILEPSY; ELECTRODE; FEMALE; HUMAN; IMMUNOMODULATION; IMPLANTED VAGUS NERVE STIMULATOR; MALE; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; TREATMENT RESPONSE; VAGUS NERVE STIMULATION; ANTAGONISTS AND INHIBITORS; BLOOD; CLINICAL TRIAL; EPILEPSY; IMMUNOLOGY; MIDDLE AGED; MULTICENTER STUDY;

ADULT; AGED; ARTHRITIS, RHEUMATOID; CYTOKINES; EPILEPSY; FEMALE; HUMANS; MALE; MIDDLE AGED; VAGUS NERVE STIMULATION;

EID: 84978826731     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1605635113     Document Type: Article

References (35)

1. Smolen JS, Aletaha D, McInnes IB (May 3, 2016) Rheumatoid arthritis. Lancet, 10.1016/S0140-6736 (16) 30173-8.
2. Birnbaum H, et al. (2010) Societal cost of rheumatoid arthritis patients in the US. Curr Med Res Opin 26(1):77-90.
3. Helmick CG, et al.; National Arthritis Data Workgroup (2008) Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part I. Arthritis Rheum 58(1):15-25.
4. Tak PP, Kalden JR (2011) Advances in rheumatology: New targeted therapeutics. Arthritis Res Ther 13(Suppl 1):S1-S5.
5. McInnes IB, Schett G (2011) The pathogenesis of rheumatoid arthritis. N Engl J Med 365(23):2205-2219.
6. Chorus AM, Miedema HS, Boonen A, Van Der Linden S (2003) Quality of life and work in patients with rheumatoid arthritis and ankylosing spondylitis of working age. Ann Rheum Dis 62(12):1178-1184.
7. Andersson U, Tracey KJ (2012) Neural reflexes in inflammation and immunity. J Exp Med 209(6):1057-1068.
8. Andersson U, Tracey KJ (2012) Reflex principles of immunological homeostasis. Annu Rev Immunol 30:313-335.
9. Rosas-Ballina M, et al. (2011) Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 334(6052):98-101.
10. Waldburger JM, Boyle DL, Pavlov VA, Tracey KJ, Firestein GS (2008) Acetylcholine regulation of synoviocyte cytokine expression by the alpha7 nicotinic receptor. Arthritis Rheum 58(11):3439-3449.
11. van Maanen MA, et al. (2009) 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 60(5):1272-1281.
12. Lu B, et al. (2014) α7 nicotinic acetylcholine receptor signaling inhibits inflammasome activation by preventing mitochondrial DNA release. Mol Med 20:350-358.
13. Rosas-Ballina M, et al. (2009) The selective alpha7 agonist GTS-21 attenuates cytokine production in human whole blood and human monocytes activated by ligands for TLR2, TLR3, TLR4, TLR9, and RAGE. Mol Med 15(7-8):195-202.
14. Borovikova LV, et al. (2000) Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405(6785):458-462.
15. Huston JM, et al. (2006) Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. J Exp Med 203(7):1623-1628.
16. Meregnani J, et al. (2011) Anti-inflammatory effect of vagus nerve stimulation in a rat model of inflammatory bowel disease. Auton Neurosci 160(1-2):82-89.
17. van Maanen MA, et al. (2009) Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice. Arthritis Rheum 60(1):114-122.
18. van Maanen MA, Stoof SP, Larosa GJ, Vervoordeldonk MJ, Tak PP (2010) Role of the cholinergic nervous system in rheumatoid arthritis: Aggravation of arthritis in nicotinic acetylcholine receptor α7 subunit gene knockout mice. Ann Rheum Dis 69(9):1717-1723.
19. Levine YA, et al. (2014) Neurostimulation of the cholinergic anti-inflammatory pathway ameliorates disease in rat collagen-induced arthritis. PLoS One 9(8):e104530.
20. van Maanen MA, Vervoordeldonk MJ, Tak PP (2009) The cholinergic anti-inflammatory pathway: Towards innovative treatment of rheumatoid arthritis. Nat Rev Rheumatol 5(4):229-232.
21. Beekwilder JP, Beems T (2010) Overview of the clinical applications of vagus nerve stimulation. J Clin Neurophysiol 27(2):130-138.
22. Ben-Menachem E (2001) Vagus nerve stimulation, side effects, and long-term safety. J Clin Neurophysiol 18(5):415-418.
23. Huston JM, et al. (2007) Transcutaneous vagus nerve stimulation reduces serum high mobility group box 1 levels and improves survival in murine sepsis. Crit Care Med 35(12):2762-2768.
24. Fransen J, van Riel PL (2005) The Disease Activity Score and the EULAR response criteria. Clin Exp Rheumatol 23(5, Suppl 39):S93-S99.
25. Fransen J, Stucki G, van Riel PLC M (2003) Rheumatoid arthritis measures: Disease Activity Score (DAS), Disease Activity Score-28(DAS28), Rapid Assessment of Disease Activity in Rheumatology (RADAR), and Rheumatoid Arthritis Disease Activity Index (RADAI). Arthritis Care Res 49(S5):S214-S224.
26. Levine YA, Koopman F, Faltys M, Zitnik R, Tak P-P (2014) Using traditional preclinical models to guide development of an untraditional inflammation therapy: neurostimulation of the cholinergic anti-inflammatory pathway in rheumatoid arthritis and inflammatory bowel disease. Bioelectronic Medicine 1:34-43.
27. Olofsson PS, Levine YA, et al. (2015) Single-pulse and unidirectional electrical activation of the cervical vagus nerve reduces tumor necrosis factor in endotoxemia. Bioelectronic Medicine 2:37-42.
28. Choi IY, Gerlag DM, Holzinger D, Roth J, Tak PP (2014) From synovial tissue to peripheral blood: Myeloid related protein 8/14 is a sensitive biomarker for effective treatment in early drug development in patients with rheumatoid arthritis. PLoS One 9(8):e106253.
29. Gerlag DM, et al. (2004) Effects of oral prednisolone on biomarkers in synovial tissue and clinical improvement in rheumatoid arthritis. Arthritis Rheum 50(12):3783-3791.
30. Bonaz B, et al. (2016) Chronic vagus nerve stimulation in Crohn's disease: A 6-month follow-up pilot study. Neurogastroenterol Motil 28(6):948-953.
31. Koopman FA, et al. (2016) Autonomic dysfunction precedes development of rheumatoid arthritis: A prospective cohort study. EBioMedicine 6:231-237.
32. Tracey KJ (2015) Shock medicine. Sci Am 312(3):28-35.
33. Bruchfeld A, et al. (2010) Whole blood cytokine attenuation by cholinergic agonists ex vivo and relationship to vagus nerve activity in rheumatoid arthritis. J Intern Med 268(1):94-101.
34. Aletaha D, et al. (2010) 2010 Rheumatoid arthritis classification criteria: An American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum 62(9):2569-2581.
35. Hochberg MC, et al. (1992) The American College of Rheumatology 1991 revised criteria for the classification of global functional status in rheumatoid arthritis. Arthritis Rheum 35(5):498-502.