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Vol. 52, Issue 4, 595-638, December 2000
An Integrative Interface between Two
Supersystems: The Brain and the Immune System
Inflammatory Joint Diseases Section, Arthritis and Rheumatism
Branch, National Institute of Arthritis and Musculoskeletal and Skin
Diseases, National Institutes of Health, Bethesda, Maryland (I.J.E.,
R.L.W.); Pediatric Endocrinology Section, Developmental Endocrinology
Branch, National Institute of Child Health and Human Development,
National Institutes of Health, Bethesda, Maryland (I.J.E., G.P.C.);
Department of Pharmacology, Institute of Experimental Medicine,
Hungarian Academy of Sciences, Budapest, Hungary (E.S.V.); and
Department of Pharmacology and Pharmacotherapy, Semmelweis University,
Budapest, Hungary (E.S.V.)
I. Introduction
A. Overview
B. Historical Perspectives
II. Anatomy and Physiology of the Autonomic Nervous System
A. Organization of the Autonomic/Sympathetic Nervous System
B. Role of Sympathetic Nervous System and
Hypothalamo-Pituitary-Adrenal Axis in Maintaining Basal and
Stress-Related Homeostasis
III. Autonomic/Sympathetic Innervation of Lymphoid Organs:
Nonsynaptic Communication
A. Innervation of the Thymus
B. Innervation of the Spleen
C. Innervation of Lymph Nodes and Tonsils
D. Innervation of the Bone Marrow
E. Innervation of Mucosa-Associated Lymphoid Tissues
F. Coexistence Patterns
G. General Pattern of the Autonomic/Sympathetic Innervation
of Lymphoid Organs
H. Spatial Relationships with Peptidergic Innervation
I. Neuroimmune Connection in Nonorganized Lymphoid Compartments
IV. Nonsynaptic Release of Norepinephrine in Lymphoid Organs:
Presynaptic Modulation and Effect of Drugs
A. Evidence for Neural Release of Norepinephrine (and Dopamine) in
Lymphoid Organs
B. Norepinephrine Is Released and Affects Immune Cells
Nonsynaptically
C. Presynaptic Modulation of Norepinephrine Release in Lymphoid
Organs: Effect of Drugs
D. Release of Neuropeptide Y and Its Action on Immune Cells
V. Systemic and Local Effects of Cytokines on Sympathetic Nervous
System Activity
A. Systemic Effects: Long Feedback Loop between the Immune System
and the Brain
B. Local Effects of Tumor Necrosis Factor-
and Interleukin-1
VI. Expression of Adrenoreceptors on Lymphoid Cells: Signal
Transduction
A. Expression and Distribution of Adrenoreceptors on Lymphoid Cells
B. Signal Pathways and Molecular Aspects of Catecholamines Actions
1. Cyclic Adenosine 5'-Monophosphate.
2. Intracellular Ca2+.
VII. Role of Sympathetic Innervation in Immune System Development
and Hematopoiesis
A. Immune System Development
B. Hematopoiesis
C. Thymocyte Development
VIII. Sympathetic Control of Lymphocyte Traffic and Circulation
IX. Modulation of Lymphocyte Proliferation and K+
Channel Conductance
A. T Lymphocytes Express a Plethora of Ion Channels
X. Modulation of cellular and humoral immunity by catecholamines
A. T Helper 1/T Helper 2 Paradigm: Role of Type 1 and Type 2 Cytokines
B. Effects of Catecholamines and Drugs (2- and
2-Adrenoreceptor Agonists and Antagonists,
Phosphodiesterase Type IV Inhibitors) on the Production of Type 1 and
Type 2 Cytokines
1. Effect on Antigen-Presenting Cells.
2. Effect on T Helper 1 Cells.
3. In Vivo Effects.
4. Local Responses.
C. Effect of Catecholamines on Chemokine Production
D. Effects of Catecholamines and Drugs on the Cellular Components
of Immunity
1. Natural Killer Cell Activity.
2. Macrophage Activity.
3. T Cytotoxic Lytic Activity.
4. Neutrophil Functions.
E. Effect of Catecholamines and Drugs on Antibody Production
(Humoral Immunity)
XI. Role of Growth Factors in Sympathetic Nervous System
Development and Modulation of the Immune Response
XII. Physiologic Control of the Sympathetic-Immune Interface:
-Adrenergic Receptor Expression, Coupling, and Desensitization
XIII. Clinical Implications
A. Infections
B. Major Injury
C. Adrenergic Agents, Sepsis, and Nitric Oxide Generation
D. Autoimmunity
E. Fibromyalgia and Chronic Fatigue Syndrome
F. Tumor Growth
XIV. Pharmacological Manipulation of the Sympathetic-Immune
Interface
XV. Conclusions
References
The brain and the immune system are the two major adaptive systems
of the body. During an immune response the brain and the immune system
"talk to each other" and this process is essential for maintaining
homeostasis. Two major pathway systems are involved in
this cross-talk: the hypothalamic-pituitary-adrenal
(HPA) axis and the sympathetic nervous system (SNS). This overview
focuses on the role of SNS in neuroimmune interactions, an area that
has received much less attention than the role of HPA axis. Evidence accumulated over the last 20 years suggests that norepinephrine (NE)
fulfills the criteria for neurotransmitter/neuromodulator in lymphoid
organs. Thus, primary and secondary lymphoid organs receive extensive
sympathetic/noradrenergic innervation. Under stimulation, NE is
released from the sympathetic nerve terminals in these organs, and the
target immune cells express adrenoreceptors. Through stimulation of
these receptors, locally released NE, or circulating catecholamines
such as epinephrine, affect lymphocyte traffic, circulation, and
proliferation, and modulate cytokine production and the functional
activity of different lymphoid cells. Although there exists substantial
sympathetic innervation in the bone marrow, and particularly in the
thymus and mucosal tissues, our knowledge about the effect of the
sympathetic neural input on hematopoiesis, thymocyte development, and
mucosal immunity is extremely modest. In addition, recent evidence is
discussed that NE and epinephrine, through stimulation of the
2-adrenoreceptor-cAMP-protein kinase A pathway,
inhibit the production of type 1/proinflammatory cytokines, such as
interleukin (IL-12), tumor necrosis factor-, and interferon-
by
antigen-presenting cells and T helper (Th) 1 cells, whereas they
stimulate the production of type 2/anti-inflammatory cytokines such as
IL-10 and transforming growth factor-. Through this mechanism,
systemically, endogenous catecholamines may cause a selective
suppression of Th1 responses and cellular immunity, and a Th2 shift
toward dominance of humoral immunity. On the other hand, in certain
local responses, and under certain conditions, catecholamines may
actually boost regional immune responses, through induction of IL-1,
tumor necrosis factor-, and primarily IL-8 production. Thus, the
activation of SNS during an immune response might be aimed to localize
the inflammatory response, through induction of neutrophil accumulation
and stimulation of more specific humoral immune responses, although
systemically it may suppress Th1 responses, and, thus protect the
organism from the detrimental effects of proinflammatory cytokines and
other products of activated macrophages. The above-mentioned
immunomodulatory effects of catecholamines and the role of SNS are also
discussed in the context of their clinical implication in certain
infections, major injury and sepsis, autoimmunity, chronic pain and
fatigue syndromes, and tumor growth. Finally, the pharmacological
manipulation of the sympathetic-immune interface is reviewed with focus
on new therapeutic strategies using selective 2- and
2-adrenoreceptor agonists and antagonists and inhibitors
of phosphodiesterase type IV in the treatment of experimental models of
autoimmune diseases, fibromyalgia, and chronic fatigue syndrome.
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 L. Dyugovskaya, P. Lavie, and L. Lavie Phenotypic and Functional Characterization of Blood {gamma}{delta} T Cells in Sleep Apnea Am. J. Respir. Crit. Care Med., July 15, 2003; 168(2): 242 - 249. [Abstract] [Full Text] [PDF]
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 F. A. Jain, L.-h. Zhao, M. K. Selig, and R. L. Kradin, Epinephrine promotes pulmonary angiitis: evidence for a {beta}1-adrenoreceptor-mediated mechanism Am J Physiol Lung Cell Mol Physiol, July 1, 2003; 285(1): L232 - L239. [Abstract] [Full Text] [PDF]
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C.-M. Hogerkorp, S. Bilke, T. Breslin, S. Ingvarsson, and C. A. K. Borrebaeck CD44-stimulated human B cells express transcripts specifically involved in immunomodulation and inflammation as analyzed by DNA microarrays Blood, March 15, 2003; 101(6): 2307 - 2313. [Abstract] [Full Text] [PDF]
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C.-Y. Li, T.-C. Chou, C.-H. Lee, C.-S. Tsai, S.-H. Loh, and C.-S. Wong Adrenaline Inhibits Lipopolysaccharide-Induced Macrophage Inflammatory Protein-1{alpha} in Human Monocytes: The Role of {beta}-Adrenergic Receptors Anesth. Analg., February 1, 2003; 96(2): 518 - 523. [Abstract] [Full Text] [PDF]
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 G. L. Kovacs and E. Toldy BASAL AND ISOPROTERENOL-STIMULATED CYCLIC-ADENOSINE MONOPHOSPHATE LEVELS IN MOUSE HIPPOCAMPUS AND LYMPHOCYTES DURING ALCOHOL TOLERANCE AND WITHDRAWAL Alcohol Alcohol., January 1, 2003; 38(1): 11 - 17. [Abstract] [Full Text] [PDF]
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 M. U. GOEBEL, A. E. TREBST, J. STEINER, Y. F. XIE, M. S. EXTON, S. FREDE, A. E. CANBAY, M. C. MICHEL, U. HEEMANN, and M. SCHEDLOWSKI Behavioral conditioning of immunosuppression is possible in humans FASEB J, December 1, 2002; 16(14): 1869 - 1873. [Abstract] [Full Text] [PDF]
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M. Mirani, I. Elenkov, S. Volpi, N. Hiroi, G. P. Chrousos, and T. Kino HIV-1 Protein Vpr Suppresses IL-12 Production from Human Monocytes by Enhancing Glucocorticoid Action: Potential Implications of Vpr Coactivator Activity for the Innate and Cellular Immunity Deficits Observed in HIV-1 Infection J. Immunol., December 1, 2002; 169(11): 6361 - 6368. [Abstract] [Full Text] [PDF]
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P. M. Cobelens, A. Kavelaars, A. Vroon, M. Ringeling, R. van der Zee, W. van Eden, and C. J. Heijnen The {beta}2-Adrenergic Agonist Salbutamol Potentiates Oral Induction of Tolerance, Suppressing Adjuvant Arthritis and Antigen-Specific Immunity J. Immunol., November 1, 2002; 169(9): 5028 - 5035. [Abstract] [Full Text] [PDF]
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 E. M. Sternberg Walter B. Cannon and " 'Voodoo' Death": A Perspective From 60 Years On Am J Public Health, October 1, 2002; 92(10): 1564 - 1566. [Full Text] [PDF]
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 A. Buske-Kirschbaum, A. Geiben, H. Hollig, E. Morschhauser, and D. Hellhammer Altered Responsiveness of the Hypothalamus-Pituitary-Adrenal Axis and the Sympathetic Adrenomedullary System to Stress in Patients with Atopic Dermatitis J. Clin. Endocrinol. Metab., September 1, 2002; 87(9): 4245 - 4251. [Abstract] [Full Text] [PDF]
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J. M. Kittner, R. Jacobs, C. R. Pawlak, C. J. Heijnen, M. Schedlowski, and R. E. Schmidt Adrenaline-induced immunological changes are altered in patients with rheumatoid arthritis Rheumatology, September 1, 2002; 41(9): 1031 - 1039. [Abstract] [Full Text] [PDF]
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M. D'Arbe, R. Einstein, and N. A. Lavidis Stressful animal housing conditions and their potential effect on sympathetic neurotransmission in mice Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2002; 282(5): R1422 - R1428. [Abstract] [Full Text] [PDF]
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 T. J. Bartness, C. K. Song, and G. E. Demas SCN Efferents to Peripheral Tissues: Implications for Biological Rhythms J Biol Rhythms, June 1, 2001; 16(3): 196 - 204. [Abstract] [PDF]
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