The sympathetic nervous response in inflammation
Open accessAbstract
Over the past decades evidence has accumulated clearly demonstrating a pivotal role for the sympathetic nervous system (SNS) and its neurotransmitters in regulating inflammation. The first part of this review provides the reader with an overview showing that the interaction of the SNS with the immune system to control inflammation is strongly context-dependent (for example, depending on the activation state of the immune cell or neuro-transmitter concentration). In the second part we focus on autoimmune arthritis as a well investigated example for sympathetically controlled inflammation to show that the SNS and catecholamines play a differential role depending on the time point of ongoing disease. A model will be developed to explain the proinflammatory effects of the SNS in the early phase and the anti-inflammatory effects of catecholamines in the later phase of autoimmune arthritis. In the final part, a conceptual framework is discussed that shows that a major purpose of increased SNS activity is nourishment of a continuously activated immune system at a systemic level using energy-rich fuels (glucose, amino acids, lipids), while uncoupling from central nervous regulation occurs at sites of inflammation by repulsion of sympathetic fibers and local adrenoceptor regulation. This creates zones of ‘permitted local inflammation’. However, if this ‘inflammatory configuration’ persists and is strong, as in autoimmunity, the effects are detrimental because of the resultant chronic catabolic state, leading to cachexia, high blood pressure, insulin resistance, and increased cardiovascular mortality, and so on. Today, the challenge is to translate this conceptual knowledge into clinical benefit.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Adrenergic signalling can have both anti-inflammatory and pro-inflammatory effects, depending on adrenergic receptor subtype, level of activation of specific cell types, and stage of disease progression.
“Both anti-inflammatory and pro-inflammatory effects of adrenergic signalling have been demonstrated, depending upon the subtype of adrenergic receptors expressed167, the level of activation of specific cell types and the stage of disease progression168.”
From The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease (2018) · cites this paper as [167]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Immunoregulatory Feedback Between Interleukin-1 and Glucocorticoid Hormones
Besedovsky, H., del Rey, A., Sorkin, E., & Dinarello, C. A. (1986) · Science · doi:10.1126/science.3014662 · Cited by 1,519 · see citing works
Prass, K., Meisel, C., Höflich, C., Braun, J., Halle, E., Wolf, T., Ruscher, K., Victorov, I. V., Priller, J., Dirnagl, U., et al. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021098 · Cited by 926 · see citing works
Autonomic innervation and regulation of the immune system (1987–2007)
Nance, D. M., & Sanders, V. M. (2007) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.03.008 · Cited by 855 · see citing works
Noradrenergic Sympathetic Neural Interactions with the Immune System: Structure and Function
Felten, D. L., Felten, S. Y., Bellinger, D. L., Carlson, S. L., Ackerman, K. D., Madden, K. S., Olschowki, J. A., & Livnat, S. (1987) · Immunological Reviews · doi:10.1111/j.1600-065x.1987.tb00534.x · Cited by 746 · see citing works
Cyclic adenosine monophosphate is a key component of regulatory T cell–mediated suppression
Bopp, T., Becker, C., Klein, M., Klein‐Hessling, S., Palmetshofer, A., Serfling, E., Heib, V., Becker, M., Kubach, J., Schmitt, S., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20062129 · Cited by 659 · see citing works
Powell, N. D., Sloan, E. K., Bailey, M. T., Arevalo, J. M. G., Miller, G. E., Chen, E., Kobor, M. S., Reader, B. F., Sheridan, J. F., & Cole, S. W. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310655110 · Cited by 588 · see citing works
Adrenergic Nerves Govern Circadian Leukocyte Recruitment to Tissues
Scheiermann, C., Kunisaki, Y., Lucas, D., Chow, A. T., Jang, J.-E., Zhang, D., Hashimoto, D., Mérad, M., & Frenette, P. S. (2012) · Immunity · doi:10.1016/j.immuni.2012.05.021 · Cited by 535 · see citing works
Phagocyte-derived catecholamines enhance acute inflammatory injury
Flierl, M. A., Rittirsch, D., Nadeau, B. A., Chen, A. J., Sarma, J. V., Zetoune, F. S., McGuire, S. R., List, R. P., Day, D. E., Hoesel, L. M., et al. (2007) · Nature · doi:10.1038/nature06185 · Cited by 475 · see citing works
Apremilast mechanism of action and application to psoriasis and psoriatic arthritis
Schafer, P. H. (2012) · Biochemical Pharmacology · doi:10.1016/j.bcp.2012.01.001 · Cited by 440 · see citing works
Stress and inflammation in exacerbations of asthma
Chen, E., & Miller, G. E. (2007) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.03.009 · Cited by 394 · see citing works
Rethinking inflammation: neural circuits in the regulation of immunity
Olofsson, P. S., Rosas‐Ballina, M., Levine, Y. A., & Tracey, K. J. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01138.x · Cited by 393 · see citing works
The cholinergic anti-inflammatory pathway: A critical review
Martelli, D., McKinley, M. J., & McAllen, R. M. (2013) · Autonomic Neuroscience · doi:10.1016/j.autneu.2013.12.007 · Cited by 388 · see citing works
Spengler, R. N., Allen, R., Remick, D. G., Strieter, R. M., & Kunkel, S. L. (1990) · The Journal of Immunology · doi:10.4049/jimmunol.145.5.1430 · Cited by 388 · see citing works
Regulation of tumor necrosis factor production by adrenaline and beta-adrenergic agonists
Severn, A., Rapson, N. T., Hunter, C. A., & Liew, F. Y. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.11.3441 · Cited by 382 · see citing works
Energy regulation and neuroendocrine–immune control in chronic inflammatory diseases
Straub, R. H., Cutolo, M., Buttgereit, F., & Pongratz, G. (2010) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2010.02218.x · Cited by 382 · see citing works
Self-citationLevine, J., Dardick, S., Roizen, M. F., et al. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-12-03423.1986 · Cited by 347 · see citing works
Goehler, L. E., Relton, J. K., Dripps, D. J., Kiechle, R., Tartaglia, N. R., Maier, S. F., & Watkins, L. R. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00020-8 · Cited by 326 · see citing works
Cosentino, M., Fietta, A. M., Ferrari, M., Rasini, E., Bombelli, R., Carcano, E., Saporiti, F., Meloni, F., Marino, F., & Lecchini, S. (2006) · Blood · doi:10.1182/blood-2006-01-028423 · Cited by 318 · see citing works
Miller, L. E., Jüsten, H., Schcölmerich, J., & Straub, R. H. (2000) · The FASEB Journal · doi:10.1096/fj.99-1082com · Cited by 294 · see citing works
Self-citationReflex control of inflammation by sympathetic nerves, not the vagus
Martelli, D., Yao, S. T., McKinley, M. J., & McAllen, R. M. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2013.268573 · Cited by 241 · see citing works
The beta2-adrenergic receptor on T and B lymphocytes: Do we understand it yet?
Sanders, V. M. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.08.001 · Cited by 238 · see citing works
Unilateral Rheumatoid Arthritis following Hemiplegia
Thompson, M., & Bywaters, E. G. L. (1962) · Annals of the Rheumatic Diseases · doi:10.1136/ard.21.4.370 · Cited by 210 · see citing works
IFN-γ Production by Th1 Cells Generated from Naive CD4+ T Cells Exposed to Norepinephrine
Swanson-Mungerson, M. A., Lee, W. T., & Sanders, V. M. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.1.232 · Cited by 207 · see citing works
Bratton, B. O., Martelli, D., McKinley, M. J., Trevaks, D., Anderson, C. R., & McAllen, R. M. (2012) · Experimental Physiology · doi:10.1113/expphysiol.2011.061531 · Cited by 206 · see citing works
The contribution of neurogenic inflammation in experimental arthritis
Levine, J., Moskowitz, M. A., & Basbaum, A. I. (1985) · The Journal of Immunology · doi:10.4049/jimmunol.135.2.843 · Cited by 186 · see citing works
Guereschi, M. G., Araújo, L. P., Maricato, J. T., Takenaka, M. C., Nascimento, V. M., Vivanco, B. C., dos Reis, V. O., Keller, A. C., Brum, P. C., & Basso, A. S. (2013) · European Journal of Immunology · doi:10.1002/eji.201243005 · Cited by 174 · see citing works
Prösch, S., Wendt, C. E. C., Reinke, P., Priemer, C., Oppert, M., Krüger, D. H., Volk, H., & Döcke, W. (2000) · Virology · doi:10.1006/viro.2000.0367 · Cited by 163 · see citing works
Grailer, J. J., Haggadone, M. D., Sarma, J. V., Zetoune, F. S., & Ward, P. A. (2014) · Journal of Innate Immunity · doi:10.1159/000358524 · Cited by 157 · see citing works
Sympathetic Nervous System Modulation of Inflammation and Remodeling in the Hypertensive Heart
Levick, S. P., Murray, D. B., Janicki, J. S., et al. (2010) · Hypertension · doi:10.1161/hypertensionaha.109.142042 · Cited by 155 · see citing works
Härle, P., Möbius, D., Carr, D. J. J., Schölmerich, J., & Straub, R. H. (2005) · Arthritis & Rheumatism · doi:10.1002/art.20987 · Cited by 151 · see citing works
Self-citationAnti-inflammatory role of sympathetic nerves in chronic intestinal inflammation
Straub, R. H., Grum, F., Strauch, U., Capellino, S., Bataille, F., Bleich, A., Falk, W., Schölmerich, J., & Obermeier, F. (2008) · Gut · doi:10.1136/gut.2007.125401 · Cited by 145 · see citing works
Self-citationSzabó, C., Haskó, G., Zingarelli, B., Nemeth, Z. H., Salzman, A. L., Kvetan, V., Pastores, S. M., & Vizi, E. S. (1997) · Immunology · doi:10.1046/j.1365-2567.1997.00137.x · Cited by 132 · see citing works
Imbalance between sympathetic and sensory innervation in peritoneal endometriosis
Arnold, J., Barcena de Arellano, M. L., Rüster, C., Vercellino, G. F., Chiantera, V., Schneider, A., & Mechsner, S. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2011.08.004 · Cited by 132 · see citing works
Szelényi, J., Kiss, J., & Vizi, E. S. (2000) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00234-9 · Cited by 131 · see citing works
Grebe, K. M., Takeda, K., Hickman, H. D., Bailey, A. M., Embry, A. C., Bennink, J. R., & Yewdell, J. W. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903395 · Cited by 130 · see citing works
Capellino, S., Cosentino, M., Wolff, C., Schmidt, M., Grifka, J. K., & Straub, R. H. (2010) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2009.119701 · Cited by 125 · see citing works
Self-citationImpaired sympathetic nerve function in the inflamed rat intestine
Swain, M. G., Blennerhassett, P. A., & Collins, S. M. (1991) · Gastroenterology · doi:10.1016/0016-5085(91)80011-w · Cited by 122 · see citing works
Differential Effects of Neuropeptides on Cytokine Production by Mouse Helper T Cell Subsets
Kawamura, N., Tamura, H., Obana, S., Wenner, M., Ishikawa, T., Nakata, A., & Yamamoto, H. (1998) · NeuroImmunoModulation · doi:10.1159/000026321 · Cited by 119 · see citing works
Aloe, L., Tuveri, M. A., & Levi‐Montalcini, R. (1992) · Rheumatology International · doi:10.1007/bf00302155 · Cited by 111 · see citing works
Claxson, A. W. D., Morris, C. J., Blake, D. R., et al. (1990) · Inflammation Research · doi:10.1007/bf01964724 · Cited by 110 · see citing works
Evolutionary medicine and chronic inflammatory state—known and new concepts in pathophysiology
Straub, R. H. (2012) · Journal of Molecular Medicine · doi:10.1007/s00109-012-0861-8 · Cited by 105 · see citing works
Self-citationClinical response to regional intravenous guanethidine in patients with rheumatoid arthritis.
Levine, J. D., Fye, K. H., Heller, P. H., et al. (1986) · PubMed · Cited by 97 · see citing works
Zielinski, M. R., Dunbrasky, D. L., Taishi, P., Souza, G., & Krueger, J. M. (2013) · Sleep · doi:10.5665/sleep.2892 · Cited by 94 · see citing works
Inflammation in CRPS: Role of the sympathetic supply
Schlereth, T., Drummond, P. D., & Birklein, F. (2013) · Autonomic Neuroscience · doi:10.1016/j.autneu.2013.12.011 · Cited by 90 · see citing works
Birklein, F., Künzel, W. W. F., & Sieweke, N. (2001) · Pain · doi:10.1016/s0304-3959(01)00309-8 · Cited by 87 · see citing works
Neuropeptide Y upregulates the adhesiveness of human endothelial cells for leukocytes.
Sung, C. P., Arleth, A. J., & FEUERSTEIN, G. Z. (1991) · Circulation Research · doi:10.1161/01.res.68.1.314 · Cited by 82 · see citing works
Cytokine Production by Naive and Primary Effector CD4+ T Cells Exposed to Norepinephrine
Ramer-Quinn, D. S., Swanson-Mungerson, M. A., Lee, W. T., & Sanders, V. M. (2000) · Brain Behavior and Immunity · doi:10.1006/brbi.2000.0603 · Cited by 81 · see citing works
Selective Regulation of Mature IgG1 Transcription by CD86 and β2-Adrenergic Receptor Stimulation
Podojil, J. R., & Sanders, V. M. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.10.5143 · Cited by 80 · see citing works
Dekkers, J. C., Geenen, R., Godaert, G. L. R., Bijlsma, J. W. J., & van Doornen, L. J. P. (2004) · PubMed · Cited by 79 · see citing works
Norepinephrine modulates human dendritic cell activation by altering cytokine release
Goyarts, E. C., Matsui, M. S., Mammone, T., Bender, A. M., Wagner, J. A., Maes, D. H., & Granstein, R. D. (2008) · Experimental Dermatology · doi:10.1111/j.1600-0625.2007.00677.x · Cited by 73 · see citing works
Adrenergic Modulation of Survival and Cellular Immune Functions during Polymicrobial Sepsis
Oberbeck, R., Schmitz, D., Wilsenack, K., et al. (2004) · NeuroImmunoModulation · doi:10.1159/000078439 · Cited by 72 · see citing works
Regulation of noradrenergic function by inflammatory cytokines and depolarization
Li, W., Knowlton, D. L., Woodward, W. R., et al. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01890.x · Cited by 71 · see citing works
Apremilast: First Global Approval
Poole, R. M., & Ballantyne, A. D. (2014) · Drugs · doi:10.1007/s40265-014-0218-4 · Cited by 70 · see citing works
Lorton, D., Lubahn, C. L., Klein, N., Schaller, J. A., & Bellinger, D. L. (1999) · Brain Behavior and Immunity · doi:10.1006/brbi.1999.0564 · Cited by 69 · see citing works
Disrupted brain–immune system–joint communication during experimental arthritis
del Rey, A., Wolff, C., Wildmann, J., Randolf, A., Hahnel, A., Besedovsky, H. O., & Straub, R. H. (2008) · Arthritis & Rheumatism · doi:10.1002/art.23869 · Cited by 68 · see citing works
Self-citationFaßold, A., Falk, W., Anders, S., Hirsch, T., Mirsky, V. M., & Straub, R. H. (2009) · Arthritis & Rheumatism · doi:10.1002/art.24860 · Cited by 68 · see citing works
Self-citationYanagawa, Y., Matsumoto, M., & Togashi, H. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001899 · Cited by 68 · see citing works
Ebbinghaus, M., Gajda, M. R., Boettger, M. K., Schaible, H., & Bräuer, R. (2011) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2011.150318 · Cited by 68 · see citing works
Pongratz, G., McAlees, J. W., Conrad, D. H., Erbe, R. S., Haas, K. M., & Sanders, V. M. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.5.2926 · Cited by 67 · see citing works
Self-citationExpression of α1-adrenoceptors on peripheral nociceptive neurons
Dawson, L. F., Phillips, J. K., Finch, P. M., Inglis, J. J., & Drummond, P. D. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.11.064 · Cited by 65 · see citing works
Härle, P., Pongratz, G., Albrecht, J., Tarner, I. H., & Straub, R. H. (2008) · Arthritis & Rheumatism · doi:10.1002/art.23628 · Cited by 62 · see citing works
Self-citationStraub, R. H., Rauch, L., Faßold, A., Lowin, T., & Pongratz, G. (2008) · Arthritis & Rheumatism · doi:10.1002/art.24030 · Cited by 62 · see citing works
Self-citationCotransmission in the autonomic nervous system
Burnstock, G. (2013) · Handbook of clinical neurology · doi:10.1016/b978-0-444-53491-0.00003-1 · Cited by 62 · see citing works
Deo, S. H., Jenkins, N. T., Padilla, J., Parrish, A. R., & Fadel, P. J. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00347.2013 · Cited by 60 · see citing works
Jenei‐Lanzl, Z., Capellino, S., Kees, F., Fleck, M., Lowin, T., & Straub, R. H. (2013) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2013-203925 · Cited by 60 · see citing works
Self-citationTodorov, L. D., Mihaylova‐Todorova, S. T., Bjur, R. A., et al. (1999) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)34890-6 · Cited by 57 · see citing works
Stress of different types increases the proinflammatory load in rheumatoid arthritis
Straub, R. H., & Kalden, J. R. (2009) · Arthritis Research & Therapy · doi:10.1186/ar2712 · Cited by 57 · see citing works
Self-citationManni, M., Granstein, R. D., & Maestroni, G. J. M. (2011) · Cytokine · doi:10.1016/j.cyto.2011.05.013 · Cited by 56 · see citing works
Straub, R. H., Pongratz, G., Weidler, C., Linde, H., Kirschning, C. J., Glück, T., Schölmerich, J., & Falk, W. (2005) · The Journal of Infectious Diseases · doi:10.1086/432134 · Cited by 55 · see citing works
Self-citationLorton, D., Lubahn, C., & Bellinger, D. (2003) · Current Drug Target -Inflammation & Allergy · doi:10.2174/1568010033344499 · Cited by 54 · cited 1× · see citing works
“The net effect of stimulating ARs on immune cells is not straightforward because it strongly depends on the context of exposure of receptive cells to sympathetic neurotransmitters; for example, the activation state of the cell [45,51], the proximity of the cell to the source of neurotransmitters (since this determines…”
BackgroundBeta blockers, norepinephrine, and cancer: an epidemiological viewpoint
Fitzgerald, P. J. (2012) · Clinical Epidemiology · doi:10.2147/clep.s33695 · Cited by 54 · see citing works
Capellino, S., Weber, K., Gelder, M., Härle, P., & Straub, R. H. (2011) · Arthritis & Rheumatism · doi:10.1002/art.33431 · Cited by 54 · see citing works
Self-citationAdrenoceptor-mediated enhancement of interleukin-33 production by dendritic cells
Yanagawa, Y., Matsumoto, M., & Togashi, H. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.04.012 · Cited by 53 · see citing works
Hermann, G. E., Beck, F. M., Tovar, C. A., Malarkey, W. B., Allen, C. M., & Sheridan, J. F. (1994) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)90027-2 · Cited by 52 · see citing works
Central sympatholytic therapy has anti-inflammatory properties in hypertensive postmenopausal women
Pöyhönen‐Alho, M., Manhem, K., Katzman, P., Kibarskis, A., Antikaínen, R., Erkkola, R. U., Tuomilehto, J. O., Ebeling, P. E., & Kaaja, R. (2008) · Journal of Hypertension · doi:10.1097/hjh.0b013e328311cf37 · Cited by 51 · see citing works
Lateralization of T-Lymphocyte Responses in Patients With Stroke
Tarkowski, E., Naver, H., Wallin, B. G., et al. (1995) · Stroke · doi:10.1161/01.str.26.1.57 · Cited by 49 · see citing works
Buxton, I. L. O., & Brunton, L. L. (1986) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1986.251.2.h307 · Cited by 49 · see citing works
Norepinephrine Inhibits Macrophage Migration by Decreasing CCR2 Expression
Xiu, F., Stanojcic, M., & Jeschke, M. G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069167 · Cited by 44 · see citing works
Effect of three animal models of inflammation on nerve fibres in the synovium.
Mapp, P. I., Walsh, D. A., Garrett, N. E., Kidd, B. L., Cruwys, S., Polak, J. M., & Blake, D. R. (1994) · Annals of the Rheumatic Diseases · doi:10.1136/ard.53.4.240 · Cited by 44 · see citing works
Howarth, D. M., Burstal, R., Hayes, C., LAN, L., & Lantry, G. (1999) · Clinical Nuclear Medicine · doi:10.1097/00003072-199906000-00001 · Cited by 44 · see citing works
Wirth, T., Westendorf, A. M., Bloemker, D., Wildmann, J., Engler, H., Mollérus, S., Wadwa, M., Schäfer, M. K.-H., Schedlowski, M., & del Rey, A. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.01.007 · Cited by 40 · see citing works
Strack, I., Schulte, S., Varnholt, H., et al. (2010) · Laboratory Investigation · doi:10.1038/labinvest.2010.162 · Cited by 40 · see citing works
Carr, D. J. J., & Blalock, J. E. (1991) · Elsevier eBooks · doi:10.1016/b978-0-12-043780-1.50026-9 · Cited by 39 · see citing works
Stohl, L. L., Zang, J. B., Ding, W., Manni, M., Zhou, X. K., & Granstein, R. D. (2013) · Cytokine · doi:10.1016/j.cyto.2013.08.005 · Cited by 39 · see citing works
Zhou, J., Zhang, L., Wei, H., Wang, X., Ni, H., Yang, F., Zhang, T., & Jiang, C. (2013) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2013.04.005 · Cited by 38 · see citing works
Bernstein, I. M., Damron, D. P., Schonberg, A. L., & Shapiro, R. E. (2009) · Reproductive Sciences · doi:10.1177/1933719109338876 · Cited by 37 · see citing works
Role of the sympathetic nervous system in chronic joint pain and inflammation.
Kidd, B. L., Cruwys, S., Mapp, P. I., et al. (1992) · Annals of the Rheumatic Diseases · doi:10.1136/ard.51.11.1188 · Cited by 37 · see citing works
Seeley, E. J., Barry, S. S., Narala, S., Matthay, M. A., & Wolters, P. J. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300027 · Cited by 35 · see citing works
Sympathetic neurotransmission modulates expression of inflammatory markers in the rat retina
Steinle, J. J. (2006) · Experimental Eye Research · doi:10.1016/j.exer.2006.09.006 · Cited by 34 · see citing works
Manni, M., & Maestroni, G. J. M. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.06.016 · Cited by 34 · see citing works
Pongratz, G., Melzer, M., & Straub, R. H. (2011) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2011.153056 · Cited by 34 · see citing works
Self-citationVega, J. L., Keino, H., & Masli, S. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2009.090264 · Cited by 32 · see citing works
Zhou, M., Simms, H. H., & Wang, P. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2004.03.008 · Cited by 32 · see citing works
Saunders, P. R., Miceli, P. C., Vallance, B. A., Wang, L., Pinto, S., Tougas, G. H., Kamath, M., & Jacobson, K. (2006) · Autonomic Neuroscience · doi:10.1016/j.autneu.2005.12.002 · Cited by 31 · see citing works
Machado, M. P. R., Rocha, A. M., de Oliveira, L. F., de Cuba, M. B., Loss, I. D. O., Castellano, L. R. C., da Silva, M. V., Machado, J. R., Nascentes, G. A. N., de Paiva, L. H., et al. (2012) · Experimental Physiology · doi:10.1113/expphysiol.2012.066431 · Cited by 27 · see citing works
Pongratz, G., Anthofer, J., Melzer, M., Anders, S., Grässel, S., & Straub, R. H. (2013) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2012-202944 · Cited by 26 · see citing works
Self-citationTarkowski, E., Naver, H., Wallin, B. G., et al. (1996) · Journal of Neuroimmunology · doi:10.1016/0165-5728(96)00011-2 · Cited by 25 · see citing works
Age-related changes in sympathetic modulation of sensory nerve activity in rat skin
Merhi, M., Helme, R. D., & Khalil, Z. G. (1998) · Inflammation Research · doi:10.1007/s000110050324 · Cited by 24 · see citing works
Stanojević, S., Dimitrijević, M., Kuštrimović, N. Z., Mitić, K. V., Vujić, V., & Leposavić, G. (2012) · Experimental Physiology · doi:10.1113/expphysiol.2012.070524 · Cited by 18 · see citing works
Bradykinin-induced neurogenic migration of neutrophils into the rat knee joint
Lo, E. J., Green, P. G., Miao, F. J., et al. (1999) · Neuroreport · doi:10.1097/00001756-199912160-00018 · Cited by 15 · see citing works
Donoso, M. V., Gómez, C. R., Orriantia, M. Á., Pérez, V., Torres, C. A., Coddou, C., Nelson, P., Maisey, K. R., Morales, B., Fernández, R., et al. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2008.09.018 · Cited by 14 · see citing works
Drummond, P. D. (2001) · European Journal of Pain · doi:10.1053/eujp.2001.0224 · Cited by 12 · see citing works
Meltzer, S. J., & Meltzer, C. (1903) · PubMed · Cited by 7 · see citing works
James Reilly and the autonomic nervous system. A prophet unheeded?
Hopkin, D. A. B., & Laplane, R. (1978) · PubMed · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease
Yang, T., Richards, E. M., Pepine, C. J., & Raizada, M. K. (2018) · Nature Reviews Nephrology · doi:10.1038/s41581-018-0018-2 · Cited by 753 · see citing works
Short sleep duration and cardiometabolic risk: from pathophysiology to clinical evidence
Tobaldini, E., Fiorelli, E. M., Solbiati, M., Costantino, G., Nobili, L., & Montano, N. (2019) · Nature Reviews Cardiology · doi:10.1038/s41569-018-0109-6 · Cited by 357 · see citing works
Coxon, L., Horne, A. W., & Vincent, K. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.01.014 · Cited by 170 · see citing works
Effects of SSRIs on Peripheral Inflammatory Cytokines in Patients with Generalized Anxiety Disorder
Hou, R., Ye, G., Liu, Y., Chen, X., Pan, M., Zhu, F., Fu, J., Fu, T., Liu, Q., Gao, Z., et al. (2019) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2019.06.001 · Cited by 97 · see citing works
Role of the autonomic nervous system in osteoarthritis
Courties, A., Sellam, J., & Berenbaum, F. (2017) · Best Practice & Research Clinical Rheumatology · doi:10.1016/j.berh.2018.04.001 · Cited by 66 · see citing works
Saha, D., Dutta, P., & Chakraborty, A. (2025) · Immuno · doi:10.3390/immuno5040045 · Cited by 3 · see citing works
- Authors
- Pongratz, G., & Straub, R. H.
- Affiliations
- University Hospital Regensburg (DE)
- Corresponding author
- Pongratz, Georg
- Venue
- Arthritis Research & Therapy
- Published
- 2014-12-12
- Volume
- 16
- Issue
- 6
- Pages
- 504-504
- ISSN
- 1478-6354 (ISSN-L)
- PMC
- PMC4396833
- OpenAlex
- W2128414222
- Cited by
- 427
- References
- 104
- Citations by year
- 2026: 36 · 2025: 57 · 2024: 41 · 2023: 50 · 2022: 50 · 2021: 52 · 2020: 31 · 2019: 35 · 2018: 35 · 2017: 14 · 2016: 21 · 2015: 4 · 2013: 1
- FWCI
- 1.05
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Arthritis Research & Therapy (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Rheumatology › Rheumatoid Arthritis Research and Therapies
- Keywords
- sympathetic nervous system, inflammation, autoimmune arthritis, catecholamines, neuroimmune interactions, adrenergic receptors, cachexia, insulin resistance, cardiovascular mortality
- MeSH terms
- Animals, Arthritis, Humans, Inflammation, Sympathetic Nervous System, Autoimmunity, Inflammation Mediators
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review