Skip to main content
SpringerLink
Log in

Relevance of Immune-Sympathetic Nervous System Interplay for the Development of Hypertension

  • Chapter
  • First Online:
Pathophysiology of Respiration

Part of the book series: Advances in Experimental Medicine and Biology ((NR,volume 884))

Abstract

Historically, the sympathetic nervous system (SNS) has been mostly associated with the ‘fight or flight’ response and the regulation of cardiovascular function. However, evidence over the past 30 years suggests that SNS may also influence the function of immune cells. In this review we describe the basic research being done in the area of SNS regulation of immune function. Further, we show that the SNS-immune interplay during circadian rhythm may modulate the robustness of the inflammatory response, critical for survival during periods of increased activity. Finally, new concepts of a close relationship between these systems in the pathogenesis of hypertension are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Andreou I, Tousoulis D, Tentolouris C, Antoniades C, Stefanadis C (2006) Potential role of endothelial progenitor cells in the pathophysiology of heart failure: clinical implications and perspectives. Atherosclerosis 189:247–254

    Article  CAS  PubMed  Google Scholar 

  • Arjona A, Sarkar DK (2005) Circadian oscillations of clock genes, cytolytic factors, and cytokines in rat NK cells. J Immunol 174:7618–7624

    Article  CAS  PubMed  Google Scholar 

  • Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85:221–228

    Article  CAS  PubMed  Google Scholar 

  • Bellinger DL, Millar BA, Perez S, Carter J, Wood C, Thyaga-Rajan S, Molinaro C, Lubahn C, Lorton D (2008) Sympathetic modulation of immunity: relevance to disease. Cell Immunol 252:27–56

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bishopric NH, Cohen HJ, Lefkowitz RJ (1980) Beta adrenergic receptors in lymphocyte subpopulations. J Allergy Clin Immunol 65:29–33

    Article  CAS  PubMed  Google Scholar 

  • Boudreau P, Brouse CJ, Dumont GA, Boivin DB (2012) Sleep-wake and circadian-dependent variation of cardiorespiratory coherence. Conf Proc IEEE Eng Med Biol Soc 2012:3817–3820

    PubMed  Google Scholar 

  • Byron JW (1972) Evidence for a -adrenergic receptor initiating DNA synthesis in haemopoietic stem cells. Exp Cell Res 71:228–232

    Article  CAS  PubMed  Google Scholar 

  • Byron JW, Fox M (1969) Adrenergic receptor blocking agents modifying the radioprotective action of T. A. B. Br J Radiol 42:400

    CAS  PubMed  Google Scholar 

  • Cohen DP, Rothstein TL (1989) Adenosine 3′,5′-cyclic monophosphate modulates the mitogenic responses of murine B lymphocytes. Cell Immunol 121:113–124

    Article  CAS  PubMed  Google Scholar 

  • Coller BS (2005) Leukocytosis and ischemic vascular disease morbidity and mortality: is it time to intervene? Arterioscler Thromb Vasc Biol 25:658–670

    Article  CAS  PubMed  Google Scholar 

  • Colombari E, Colombari DS, Li H, Shi P, Dong Y, Jiang N, Raizada MK, Sumners C, Murphy D, Paton JF (2010) Macrophage migration inhibitory factor in the paraventricular nucleus plays a major role in the sympathoexcitatory response to salt. Hypertension 56:956–963

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cook-Mills JM, Cohen RL, Perlman RL, Chambers DA (1995) Inhibition of lymphocyte activation by catecholamines: evidence for a non-classical mechanism of catecholamine action. Immunology 85:544–549

    PubMed Central  CAS  PubMed  Google Scholar 

  • de Kloet AD, Krause EG, Shi PD, Zubcevic J, Raizada MK, Sumners C (2013) Neuroimmune communication in hypertension and obesity: a new therapeutic angle? Pharmacol Ther 138:428–440

    Article  PubMed Central  PubMed  Google Scholar 

  • Diamantstein T, Ulmer A (1975) The antagonistic action of cyclic GMP and cyclic AMP on proliferation of B and T lymphocytes. Immunology 28:113–119

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dokur M, Boyadjieva N, Sarkar DK (2004) Catecholaminergic control of NK cell cytolytic activity regulatory factors in the spleen. J Neuroimmunol 151:148–157

    Article  CAS  PubMed  Google Scholar 

  • Dresch C, Minc J, Poirier O, Bouvet D (1981) Effect of beta adrenergic agonists and beta blocking agents on hemopoiesis in human bone marrow. Biomedicine 34:93–98

    CAS  PubMed  Google Scholar 

  • Durant S (1986) In vivo effects of catecholamines and glucocorticoids on mouse thymic cAMP content and thymolysis. Cell Immunol 102:136–143

    Article  CAS  PubMed  Google Scholar 

  • Feitelson JB, Kulenovic E, Beck DJ, Harris PD, Passmore JC, Malkani AL, Fleming JT (2002) Endogenous norepinephrine regulates blood flow to the intact rat tibia. J Orthop Res 20:391–396

    Article  CAS  PubMed  Google Scholar 

  • Felder RB (2010) Mineralocorticoid receptors, inflammation and sympathetic drive in a rat model of systolic heart failure. Exp Physiol 95:19–25

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Felder RB, Yu Y, Zhang ZH, Wei SG (2009) Pharmacological treatment for heart failure: a view from the brain. Clin Pharmacol Ther 86:216–220

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Felten DL, Gibson-Berry K, Wu JH (1996) Innervation of bone marrow by tyrosine hydroxylase-immunoreactive nerve fibers and hemopoiesis-modulating activity of a β-adrenergic agonist in mouse. Mol Biol Hematopoiesis 5:627–636

    Article  Google Scholar 

  • Feuerer M, Beckhove P, Garbi N, Mahnke Y, Limmer A, Hommel M, Hämmerling GJ, Kyewski B, Hamann A, Umansky V, Schirrmacher V (2003) Bone marrow as a priming site for T-cell responses to blood-borne antigen. Nat Med 9:1151–1157

    Article  CAS  PubMed  Google Scholar 

  • Fuchs BA, Albright JW, Albright JF (1988) Beta-adrenergic receptors on murine lymphocytes: density varies with cell maturity and lymphocyte subtype and is decreased after antigen administration. Cell Immunol 114:231–245

    Article  CAS  PubMed  Google Scholar 

  • Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, Harrison DG (2007) Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 204:2449–2460

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hristov M, Zernecke A, Liehn EA, Weber C (2007) Regulation of endothelial progenitor cell homing after arterial injury. Thromb Haemost 98:274–277

    CAS  PubMed  Google Scholar 

  • Kees MG, Pongratz G, Kees F, Schölmerich J, Straub RH (2003) Via beta-adrenoceptors, stimulation of extrasplenic sympathetic nerve fibers inhibits lipopolysaccharide-induced TNF secretion in perfused rat spleen. J Neuroimmunol 145:77–85

    Article  CAS  PubMed  Google Scholar 

  • Kendall MD, al-Shawaf AA (1991) Innervation of the rat thymus gland. Brain Behav Immun 5:9–28

    Article  CAS  PubMed  Google Scholar 

  • Kohm AP, Mozaffarian A, Sanders VM (2002) B cell receptor- and beta 2-adrenergic receptor-induced regulation of B7-2 (CD86) expression in B cells. J Immunol 168:6314–6322

    Article  CAS  PubMed  Google Scholar 

  • Lipski S (1980) Effect of beta-adrenergic stimulation by isoprenaline on proliferation and differentiation of mouse bone marrow cells in vivo. Pol J Pharmacol Pharm 32:281–287

    CAS  PubMed  Google Scholar 

  • Logan RW, Arjona A, Sarkar DK (2011) Role of sympathetic nervous system in the entrainment of circadian natural-killer cell function. Brain Behav Immun 25:101–109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maestroni GJ (1995) Adrenergic regulation of haematopoiesis. Pharmacol Res 32:249–253

    Article  CAS  PubMed  Google Scholar 

  • Maestroni GJ, Conti A (1994) Noradrenergic modulation of lymphohematopoiesis. Int J Immunopharmacol 16:117–122

    Article  CAS  PubMed  Google Scholar 

  • McConkey DJ, Orrenius S, Jondal M (1990) Agents that elevate cAMP stimulate DNA fragmentation in thymocytes. J Immunol 145:1227–1230

    CAS  PubMed  Google Scholar 

  • Meltzer JC, MacNeil BJ, Sanders V, Pylypas S, Jansen AH, Greenberg AH, Nance DM (2004) Stress-induced suppression of in vivo splenic cytokine production in the rat by neural and hormonal mechanisms. Brain Behav Immun 18:262–273

    Article  CAS  PubMed  Google Scholar 

  • Molina PE (2001) Noradrenergic inhibition of TNF upregulation in hemorrhagic shock. Neuroimmunomodulation 9:125–133

    Article  CAS  PubMed  Google Scholar 

  • Morgan IJ, Wigham CG, Perris AD (1984) The promotion of mitosis in cultured thymic lymphocytes by acetylcholine and catecholamines. J Pharm Pharmacol 36:511–515

    Article  CAS  PubMed  Google Scholar 

  • Rabelink TJ, de Boer HC, de Koning EJ, van Zonneveld AJ (2004) Endothelial progenitor cells: more than an inflammatory response? Arterioscler Thromb Vasc Biol 24:834–838

    Article  CAS  PubMed  Google Scholar 

  • Radojcic T, Baird S, Darko D, Smith D, Bulloch K (1991) Changes in beta-adrenergic receptor distribution on immunocytes during differentiation: an analysis of T cells and macrophages. J Neurosci Res 30:328–335

    Article  CAS  PubMed  Google Scholar 

  • Ramer-Quinn DS, Baker RA, Sanders VM (1997) Activated T helper 1 and T helper 2 cells differentially express the beta-2-adrenergic receptor: a mechanism for selective modulation of T helper 1 cell cytokine production. J Immunol 159:4857–4867

    CAS  PubMed  Google Scholar 

  • Reavey M, Saner H, Paccaud F, Marques-Vidal P (2013) Exploring the periodicity of cardiovascular events in Switzerland: variation in deaths and hospitalizations across seasons, day of the week and hour of the day. Int J Cardiol 168:2195–2200

    Article  PubMed  Google Scholar 

  • Sanders VM, Munson AE (1984a) Beta adrenoceptor mediation of the enhancing effect of norepinephrine on the murine primary antibody response in vitro. J Pharmacol Exp Ther 230:183–192

    CAS  PubMed  Google Scholar 

  • Sanders VM, Munson AE (1984b) Kinetics of the enhancing effect produced by norepinephrine and terbutaline on the murine primary antibody response in vitro. J Pharmacol Exp Ther 231:527–531

    CAS  PubMed  Google Scholar 

  • Sanders VM, Baker RA, Ramer-Quinn DS, Kasprowicz DJ, Fuchs BA, Street NE (1997) Differential expression of the beta2-adrenergic receptor by Th1 and Th2 clones: implications for cytokine production and B cell help. J Immunol 158:4200–4210

    CAS  PubMed  Google Scholar 

  • Santisteban MM, Zubcevic J, Baekey DM, Raizada MK (2013) Dysfunctional brain-bone marrow communication: a paradigm shift in the pathophysiology of hypertension. Curr Hypertens Rep 15:377–389

    Article  PubMed Central  PubMed  Google Scholar 

  • Scheiermann C, Kunisaki Y, Lucas D, Chow A, Jang JE, Zhang D, Hashimoto D, Merad M, Frenette PS (2012) Adrenergic nerves govern circadian leukocyte recruitment to tissues. Immunity 37:290–301

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shi Z, Gan XB, Fan ZD, Zhang F, Zhou YB, Gao XY, De W, Zhu GQ (2011) Inflammatory cytokines in paraventricular nucleus modulate sympathetic activity and cardiac sympathetic afferent reflex in rats. Acta Physiol 203:289–297

    Article  CAS  Google Scholar 

  • Singh U (1985) Lymphopoiesis in the nude fetal thymus following sympathectomy. Cell Immunol 93:222–228

    Article  CAS  PubMed  Google Scholar 

  • Singh U, Owen JJ (1975) Studies on the effect of various agents on the maturation of thymus stem cells. Eur J Immunol 5:286–288

    Article  CAS  PubMed  Google Scholar 

  • Singh U, Owen JJ (1976) Studies on the maturation of thymus stem cells. The effects of catecholamines, histamine and peptide hormones on the expression of T cell alloantigens. Eur J Immunol 6:59–62

    Article  CAS  PubMed  Google Scholar 

  • Sudo N, Yu XN, Sogawa H, Kubo C (1997) Restraint stress causes tissue-specific changes in the immune cell distribution. Neuroimmunomodulation 4:113–119

    CAS  PubMed  Google Scholar 

  • Swanson MA, Lee WT, Sanders VM (2001) IFN-gamma production by Th1 cells generated from naive CD4+ T cells exposed to norepinephrine. J Immunol 166:232–2340

    Article  CAS  PubMed  Google Scholar 

  • Vischer TL (1976) The differential effect of cyclic AMP on lymphocyte stimulation by T- or B-cell mitogens. Immunology 30:735–739

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wei SG, Zhang ZH, Beltz TG, Yu Y, Johnson AK, Felder RB (2013) Subfornical organ mediates sympathetic and hemodynamic responses to blood-borne proinflammatory cytokines. Hypertension 62:118–125

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whisler RL, Beiqing L, Grants IS, Newhouse YG (1992) Cyclic AMP modulation of human B cell proliferative responses: role of cAMP-dependent protein kinases in enhancing B cell responses to phorbol diesters and ionomycin. Cell Immunol 142:398–415

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Kang YM, Zhang ZH, Wei SG, Chu Y, Weiss RM, Felder RB (2007) Increased cyclooxygenase-2 expression in hypothalamic paraventricular nucleus in rats with heart failure: role of nuclear factor kappaB. Hypertension 49:511–518

    Article  CAS  PubMed  Google Scholar 

  • Zhu S, Deng S, Ma Q, Zhang T, Jia C, Zhuo D, Yang F, Wei J, Wang L, Dykxhoorn DM, Hare JM, Goldschmidt-Clermont PJ, Dong C (2013) MicroRNA-10A and microRNA-21 modulate endothelial progenitor cell senescence via suppressing high-mobility group A2. Circ Res 112:152–164

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zubcevic J, Waki H, Raizada MK, Paton JF (2011) Autonomic-immune-vascular interaction: an emerging concept for neurogenic hypertension. Hypertension 57:1026–1033

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Conflicts of Interest

The authors declare no conflicts of interest in relation to this article.

Author information

Authors and Affiliations

  1. Institute of Human Physiology, Medical University of Gdansk, 15 Tuwima St., 80-210, Gdansk, Poland

    Pawel J. Winklewski

  2. Department of Immunopathology of Infectious and Parasitic Diseases, Medical University of Warsaw, Warsaw, Poland

    Marek Radkowski

  3. Department of Laboratory Diagnostics and Clinical Immunology of Developmental Age, Medical University of Warsaw, Warsaw, Poland

    Urszula Demkow

Authors
  1. Pawel J. Winklewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marek Radkowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Urszula Demkow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pawel J. Winklewski .

Editor information

Editors and Affiliations

  1. Institute of Nursing, Public Higher Medical Professional School in Opole, Opole, Poland

    Mieczyslaw Pokorski

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Winklewski, P.J., Radkowski, M., Demkow, U. (2015). Relevance of Immune-Sympathetic Nervous System Interplay for the Development of Hypertension. In: Pokorski, M. (eds) Pathophysiology of Respiration. Advances in Experimental Medicine and Biology(), vol 884. Springer, Cham. https://doi.org/10.1007/5584_2015_169

Download citation

Publish with us

Policies and ethics

Search

Navigation