Cited by 1,025Neuropeptides and Animal PhysiologyVagus Nerve Stimulation ResearchT-cell and B-cell Immunology

The DOI matches its Crossref record.

Noradrenergic and peptidergic innervation of lymphoid tissue

Felten, D L, Felten, S Y, Carlson, S L, Olschowka, J A, Livnat, S·1985·The Journal of Immunology

Open this paper in CoChat — free account

Abstract

Sympathetic noradrenergic nerve fibers innervate both the vasculature and parenchymal fields of lymphocytes and associated cells in several lymphoid organs, including the thymus, spleen, lymph nodes, gut-associated lymphoid tissue (GALT), and bone marrow, in a variety of mammalian species. This innervation is both regional and specific, and generally is directed into zones of T lymphocytes and plasma cells rather than into nodular regions or B lymphocyte regions. In the thymus, noradrenergic fibers enter with nerve bundles and plexuses around blood vessels, travel into the cortex from subcapsular plexuses and with the vasculature, and branch into the parenchyma of the thymic cortex. The vasculature and parenchymal regions of both the outer and deep cortex are innervated by these fibers. In the spleen, noradrenergic fibers enter with the vasculature, travel along the trabeculae and along the branching vasculature, and are distributed mainly in the white pulp along the central artery and associated periarterial lymphatic sheath. Fibers branch from a dense plexus around the central artery and travel into the parenchyma, where they end among fields of lymphocytes and other cell types. In lymph nodes, noradrenergic fibers enter at the hilus, travel along the vasculature and in a subcapsular plexus, and branch into the parenchyma in paracortical and cortical regions, where they end among lymphocytes. In the GALT, represented in these studies by rabbit appendix, sacculus rotundus, and Peyer’s patches, noradrenergic fibers enter at the serosal surface, travel longitudinally with the muscularis interna, turn radially into internodular plexuses, plunge directly through the thymus-dependent zones, and ramify profusely among lymphocytes, enterochromaffin cells, and plasma cells in the interdomal regions. In the bone marrow, noradrenergic fibers enter with blood vessels, distribute deeply into the marrow on those vessels, and branch sparsely into the substance of the marrow. Immunocytochemical observations revealed the presence of neuro-peptide-like immuno-reactivity in the thymus and spleen. Vasoactive intestinal peptide (VIP)-like immunoreactivity is found in varicose profiles in the thymus within the cortex. In the spleen, immunoreactive profiles showing neuropeptide Y-like, Met-enkephalin-like, cholecystokinin-8 (CCK)-like, and neurotensin-like immunoreactivity are present along the central artery of the white pulp and its smaller branches, with only sparse fibers of most of these peptides entering the parenchyma. CCK-like profiles are present in abundance in the white pulp among parenchymal elements. The presence of noradrenergic innervation and possible peptidergic innervation of a variety of lymphoid tissues suggests that these nerves may serve as an important link between the nervous system and elements of the immune system. Neural modulation of immune responses could utilize a number of possible mechanisms to influence the function of individual cells. Resolution of these mechanisms will require both in vitro testing of individual transmitters or modulators singly and in combination, and in vivo studies that take into account the local microenvironment and temporal influences of hormones and transmitters on specific cell types.

Integrity signals

Registry

Crossref · 10.4049/jimmunol.135.2.755

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Sorted by citations

Items 501–600 of 998

Neuronal regulation of B-cell immunity: Anticipatory immune posturing?
You, Z., Liu, B., & Qi, H. (2022) · Neuron · doi:10.1016/j.neuron.2022.10.014 · Cited by 25
Psychological Factors in Healing: A New Perspective on an Old Debate
Myers, S. S., & Benson, H. (1992) · Behavioral Medicine · doi:10.1080/08964289.1992.10544235 · Cited by 24
Effects of Catecholamines on the Immune Response
Elenkov, I. J. (2007) · Neuroimmune biology · doi:10.1016/s1567-7443(07)00210-4 · Cited by 25
Effect of catecholamines on IL-2 production and NK cytotoxicity of rats in vitro.
Peng, Y.-P., Qiu, Y., Jiang, J., & Wang, J. (2004) · PubMed · Cited by 24
Effects of footshock stress upon spleen and peripheral blood lymphocyte mitogenic responses in rats with lesions of the paraventricular nuclei
Pezzone, M. A., Dohanics, J., & Rabin, B. S. (1994) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)90062-0 · Cited by 24
Noninvasive Assessment of Vascular Function
Higashi, Y. (2024) · JACC Asia · doi:10.1016/j.jacasi.2024.09.015 · Cited by 27
T Cells Plead for Rejuvenation and Amplification; With the Brain’s Neurotransmitters and Neuropeptides We Can Make It Happen
Levite, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.617658 · Cited by 23
Cellular and Nerve Fibre Catecholaminergic Thymic Network: Steroid Hormone Dependent Activity
Leposavić, G., Pilipović, I., & Nanut, M. P. (2011) · Physiological Research · doi:10.33549/physiolres.932175 · Cited by 23
“The thymus receives extensive sympathetic innervation (Williams and Felten 1981, Felten et al. 1985, Novotny et al. 1990, Vizi et al. 1995, Cavallotti et al. 1999, Nance and Sanders 2007).”
Background
Pharmacology and Biochemistry of Synaptic Transmission
Deutch, A. Y., & Roth, R. H. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397179-1.00007-5 · Cited by 23
Substance P – a potent risk factor in childhood lymphoblastic leukaemia
Nowicki, M. O., & Miśkowiak, B. (2003) · Leukemia · doi:10.1038/sj.leu.2402920 · Cited by 23
Neural Modulation of Immunity: Conditioning Phenomena and the Adaptability of Lymphoid Cells
Grossman, Z., Herberman, R. B., & Livnat, S. (1992) · International Journal of Neuroscience · doi:10.3109/00207459209000555 · Cited by 23
Self-citation
Neuroendocrinology of Interleukin-1
BERKENBOSCH, F., de Rijk, R., del Rey, A., & Besedovsky, H. O. (1990) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-5799-5_19 · Cited by 23
Emotions, Brain, Immunity, and Health: A Review
Melnechuk, T. (1988) · Springer eBooks · doi:10.1007/978-1-4757-1987-1_8 · Cited by 23
Differential immune responsiveness in mouse lines selectively bred for high and low sensitivity to ethanol
Petitto, J. M., McIntyre, T. D., McRae, B. L., et al. (1990) · Brain Behavior and Immunity · doi:10.1016/0889-1591(90)90005-b · Cited by 23
Treatment of the mucosa with local anaesthetics in ulcerative colitis
Björck, S., Dahlström, A. B., Johansson, L., et al. (1992) · Inflammation Research · doi:10.1007/bf01991026 · Cited by 23
“In lymphoid tissue adrenergic nerves appear to participate in the homing of certain subsets of T-lymphocytes, and lymphocytes are known to carry adrenoceptors as well as peptide receptors [12].”
Background
End-point effector stress mediators in neuroimmune interactions: their role in immune system homeostasis and autoimmune pathology
Dimitrijević, M., Stanojević, S., Kuštrimović, N. Z., & Leposavić, G. (2012) · Immunologic Research · doi:10.1007/s12026-012-8275-9 · Cited by 20
“Neuropeptide Y (NPY), which is co-released with NE from the sympathetic nerve endings and adrenomedullary cells upon stress-induced activation of the sympatho-adrenal system [4], also constitutes a component of this system [5].”
Background
Pancreatic hormone and glutamic acid decarboxylase expression in the mouse thymus: a real-time PCR study.
Pléau, J., Esling, A., Geutkens, S., Dardenne, M., & Homo-Delarche, F. (2001) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1006/bbrc.2001.4884 · Cited by 22
Sympathetic nerve destruction in spleen in murine AIDS
Kelley, S. P., Moynihan, J. A., Stevens, S. Y., et al. (2003) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(02)00101-0 · Cited by 22
Self-citation
Psychoneuroimmunology: past, present, and future.
Kiecolt‐Glaser, J. K., & Galser, R. (1989) · PubMed · Cited by 22
The Cholinergic and Adrenergic Innervation of the Rat Thymus
Kendall, M. D., al-Shawaf, A. A., & Zaidi, S. A. A. (1988) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-5535-9_39 · Cited by 22
Models and mechanisms of neuroendocrine-immune interactions during ontogeny
Provinciali, M., & Fabris, Ν. (1991) · Advances in Neuroimmunology · doi:10.1016/s0960-5428(06)80217-2 · Cited by 22
The thymus gland as a major target for the central nervous system and the neuroendocrine system: Neuroendocrine modulation of thymic β2-Adrenergic receptor distribution as revealed by in vitro autoradiography
Marchetti, B., Morale, M. C., & Pelletier, G. (1990) · Molecular and Cellular Neuroscience · doi:10.1016/1044-7431(90)90037-5 · Cited by 22
Distribution of somatostatin-immunoreactive nerve fibres in Peyer's patches.
Fehér, É., Fodor, M., & Burnstock, G. (1992) · Gut · doi:10.1136/gut.33.9.1195 · Cited by 22
Infection in the Developing Brain: The Role of Unique Systemic Immune Vulnerabilities
Singh, G., Tucker, E. W., & Rohlwink, U. K. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2021.805643 · Cited by 25
“” Catecholamines, such as norepinephrine and adrenaline, are neurotransmitters released from the sympathetic and parasympathetic nerve fibers of the autonomic nervous system regulate the immune system both locally and systemically (208, 209).”
Background
On the Role of Psychoneuroimmunology in Oral Medicine
Seizer, L., & Schubert, C. (2022) · International Dental Journal · doi:10.1016/j.identj.2022.07.002 · Cited by 24
Intact noradrenaline transporter is needed for the sympathetic fine-tuning of cytokine balance
Selmeczy, Z., Szelényi, J., & Vizi, E. S. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01721-7 · Cited by 21
Expression of α1-adrenoceptors on thymic cells and their role in fine tuning of thymopoiesis
Pešić, V., Kosec, D. J., Radojević, K., Pilipović, I., Nanut, M. P., Vidić‐Danković, B., & Leposavić, G. (2009) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2009.06.018 · Cited by 21
Interleukin-12 promotes neurite outgrowth in mouse sympathetic superior cervical ganglion neurons
Lin, H., Hikawa, N., Takenaka, T., et al. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00913-1 · Cited by 21
“Lymphoid tissues, including spleen and thymus, are innervated by the sympathetic nervous system and the sympathetic nerve terminals form synaptic-like contacts with lymphocytes in the spleen [5,6].”
Individual Differences in Disease Susceptibility as a Possible Factor in the Population Dynamics of Rats and Mice
Koolhaas, J. M., & van Oortmerssen, G. A. (1987) · Netherlands Journal of Zoology · doi:10.1163/156854288x00076 · Cited by 21
“This relation-120 ship between social position and the immune system is not surprising since recent developments in the field of psychoneuroimmunology emphasize the significance of various neuroendocrine systems and the autonomic nervous system in immune functioning (FELTEN et al., 1985).”
Background
Acute Down-Regulation of Antibody Production Following Spinal Cord Injury: Role of Systemic Catecholamines
Vega, J. L., Ganea, D., & Jonakait, G. M. (2003) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/62.8.848 · Cited by 21
“For example, a rich supply of sympathetic fibers can be found in the parenchyma of lymphatic organs (6), and a portion of these fibers make classical-type synapses with lymphocytes (7).”
Background
Multiple nitric oxide synthase systems in adult rat thymus revealed using NADPH diaphorase histochemistry.
Downing, J. R. (1994) · PubMed · Cited by 21
Capsaicin-induced inhibition of mitogen and interleukin-2-stimulated T cell proliferation: its reversal by in vivo substance P administration
Santoni, G., Perfumi, M. C., Bressan, A., & Piccoli, M. (1996) · Journal of Neuroimmunology · doi:10.1016/0165-5728(96)00081-1 · Cited by 20
Neuropeptide-immunoreactive cells in human thymus
Piantelli, M., Maggiano, N., Larocca, L. M., et al. (1990) · Brain Behavior and Immunity · doi:10.1016/0889-1591(90)90022-i · Cited by 21
Neural architecture in lymphoid organs: Hard‐wired antigen presenting cells and neurite networks in antigen entrance areas
Wülfing, C., Schuran, F. A., Urban, J., Oehlmann, J., & Günther, H. S. (2018) · Immunity Inflammation and Disease · doi:10.1002/iid3.223 · Cited by 20
Splenic Denervation Attenuates Repeated Social Defeat Stress-Induced T Lymphocyte Inflammation
Elkhatib, S. K., Moshfegh, C. M., Watson, G. F., Schwab, A. D., Katsurada, K., Patel, K. P., & Case, A. J. (2021) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2021.05.004 · Cited by 18
Innate and adaptive immune system consequences of post-traumatic stress disorder
Lauten, T. H., Natour, T., & Case, A. J. (2024) · Autonomic Neuroscience · doi:10.1016/j.autneu.2024.103159 · Cited by 22
“The culmination of this body of work, combined with newer evidence such as the innervation of the lymphoid organs (Felten et al., 1985) and the discovery of immune cells expressing neurotransmitter receptors (Had-den et al., 1970; Pert et al., 1985), underscores the mounting evidence suggesting a…”
TH17/Treg lymphocyte balance is regulated by beta adrenergic and cAMP signaling
Lauten, T. H., Elkhatib, S. K., Natour, T., Reed, E. C., Jojo, C. N., & Case, A. J. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.11.013 · Cited by 20
“…neuroimmune communication was the finding that lymphoid organs appear to be innervated exclusively by sympathetic nerve fibers (Felten et al., 1987; Felten et al., 1985; Felten and Olschowka, 1987; Livnat et al., 1987), which suggested a potential role for catecholamine-mediated immune regulation.”
Immunofluorescent characterization of innervation and nerve-immune cell neighborhood in mouse thymus
Al-Shalan, H. A. M., Hu, D., Nicholls, P. K., Greene, W. K., & Ma, B. (2019) · Cell and Tissue Research · doi:10.1007/s00441-019-03052-4 · Cited by 20
“Numerous studies involving the use of retrograde tracers/ virus and histochemical/immunohistochemical techniques have demonstrated the sensory and autonomic innervation of the thymus across a few species, including mouse, rat and human (Felten et al. 1985; Tollefson and Bulloch 1990; Mićić et al. 1992; Anagnostou et a…”
BackgroundMethodResultInfluential
Innervation of the thymus in normal and bone marrow reconstituted severe combined immunodeficient (SCID) mice
Mitchell, B., Kendall, M. D., Adam, E. C., et al. (1997) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(96)00227-5 · Cited by 20
“In contrast, sympathetic innervation is in association with the stellate and thoracic paravertebral Ž .ganglia Felten et al., 1985 .”
Background
Changes in lymphocyte subsets after short-term pharmacotherapy in patients with panic disorder
Kim, Y., Park, Q., & Yu, B. (2004) · Psychiatry Research · doi:10.1016/j.psychres.2004.05.015 · Cited by 20
“Norepinephrine and epinephrine are well-known immunity modulators (Besedovsky et al., 1979; Felten et al., 1985).”
Background
Functional Characterization of Neurotensin Receptors in Human Cutaneous T Cell Lymphoma Malignant Lymphocytes
Ramez, M., Bagot, M., Nikolova, M. H., et al. (2001) · Journal of Investigative Dermatology · doi:10.1046/j.0022-202x.2001.01439.x · Cited by 20
Chemical destruction of brain noradrenergic neurons affects splenic cytokine production
Engler, H., Doenlen, R., Riether, C., Engler, A., Besedovsky, H. O., del Rey, A., Pacheco‐López, G., & Schedlowski, M. (2010) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2009.12.001 · Cited by 20
“Primary and secondary lymphoid organs are richly innervated by sympathetic nerve fibers and noradrenergic terminals are found in the close vicinity of lymphocytes and macrophages, forming synapse-like contacts (Felten et al., 1985).”
Histamine H3 Receptor Integrates Peripheral Inflammatory Signals in the Neurogenic Control of Immune Responses and Autoimmune Disease Susceptibility
Krementsov, D. N., Wall, E. H., Martin, R. A., Subramanian, M., Noubade, R., del Río, R., Mawe, G. M., Bond, J. P., Poynter, M. E., Blankenhorn, E. P., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062743 · Cited by 21
“However, in contrast to what has been reported for the LNs of other species, where nerve fibers have been shown to branch into the parenchyma in paracortical and cortical regions [57], only sparse innervation was detected in the mouse LN.”
Result
Immune response in cold exposures of different types
Владимировна, К. Т., & Eliseeva, L. S. (2000) · Journal of Thermal Biology · doi:10.1016/s0306-4565(99)00113-8 · Cited by 20
Physiology of Prevertebral Sympathetic Ganglia
Szurszewski, J. H., & Linden, D. R. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-382026-6.00020-8 · Cited by 20
Relationships between monoaminergic and cholinergic innervation of the rat thymus during aging
Mićić, M., Leposavić, G., & Ugrešić, N. D. (1994) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)90197-x · Cited by 20
Immunological Alterations in Cluster Headache During Remission and Cluster Period. Comparison with Low Back Pain Patients
Bussone, G., Salmaggi, A., Leone, M., et al. (1992) · Cephalalgia · doi:10.1046/j.1468-2982.1992.1204250.x · Cited by 20
“The recently provided evidence for autonomic innervation of lymphoid organs (9) suggests that hypothalamic structures can influence the immune system not only via the neuroendocrine pathway but also via sympathetic outflow.”
Background
Cyclosporine and alpha-interferon do not attenuate morphine withdrawal in rats but do impair thermoregulation
Dantzer, R., Satinoff, E., & Kelley, K. W. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90158-2 · Cited by 20
Vasoactive intestinal peptide receptors in rat spleen and brain: A shared communication network
Wiedermann, C. J., Sertl, K., Zipser, B., et al. (1988) · Peptides · doi:10.1016/0196-9781(88)90218-5 · Cited by 20
Neuropeptides and the Immune System: Substance P Receptors in Bronchus‐Associated Lymphoid Tissue of Rat
Wiedermann, C. J., Sertl, K., & Pert, C. B. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb35767.x · Cited by 20
Early postnatal castration affects thymic and thymocyte noradrenaline levels and β-adrenoceptor-mediated influence on the thymopoiesis in adult rats
Leposavić, G., Radojević, K., Vidić‐Danković, B., et al. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2006.10.004 · Cited by 19
“It is now clear that in the thymus there is innervation of sympathetic nerves (Williams et al., 1981; Felten et al., 1985; Kendall and AlShawaf, 1991; Elenkov et al., 2000).”
Background
Scientific and Regulatory Policy Committee Review
Fikes, J. D., Patrick, D. J., Francke, S., Frazier, K. S., Reindel, J. F., Romeike, A., Spaet, R. H., Tomlinson, L., & Schafer, K. A. (2015) · Toxicologic Pathology · doi:10.1177/0192623315596382 · Cited by 19
Natural Killer (NK) Cell Functionality after human Spinal Cord Injury (SCI): protocol of a prospective, longitudinal study
Laginha, I., Kopp, M. A., Druschel, C., Schaser, K., Brommer, B., Hellmann, R. C., Watzlawick, R., Saidy, R. R. O., Prüß, H., Failli, V., et al. (2016) · BMC Neurology · doi:10.1186/s12883-016-0681-5 · Cited by 20
“Efferent sympathetic noradrenergic/peptidergic fibers are present in the parenchyma of primary and secondary lymphoid organs including the bone marrow where they travel along vasculature ending in close proximity to precursor and hematopoietic cells [12, 13, 15].”
Background
Hypothermia-enhanced splenic cytokine gene expression is independent of the sympathetic nervous system
Ganta, C. K., Helwig, B. G., Blecha, F., Ganta, R. R., Cober, R. E., Parimi, S., Musch, T. I., Fels, R. J., & Kenney, M. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00846.2005 · Cited by 19
“Sympathetic innervation to the spleen provides a connection between central sympathetic neural circuits and immunocompetent cells in the spleen (1, 6, 9, 16, 17).”
Background
Differential effects of chronic propranolol treatment on the phenotypic profile of thymocytes from immature and adult rats
Leposavić, G., Plećaš, B., & Kosec, D. J. (2000) · Immunopharmacology · doi:10.1016/s0162-3109(99)00160-5 · Cited by 19
Thymopoiesis Following Chronic Blockade of β‐Adrenoceptors
Rauški, A., Kosec, D. J., Vidić‐Danković, B., et al. (2003) · Immunopharmacology and Immunotoxicology · doi:10.1081/iph-120026437 · Cited by 19
“It has been clearly demonstrated that sympathetic=noradrenergic postganglionic nerve fibers innervate both the smooth muscle of the thymus vasculature and the parenchyma of specific compartments of the organ.([1]) These fibers enter the thymus along with blood vessels, distribute to the capsular and septal system and…”
Background
Metchnikoff, the Modern Immunologist
Tauber, A. I. (1990) · Journal of Leukocyte Biology · doi:10.1002/jlb.47.6.561 · Cited by 19
Immune depression induced by protein calorie malnutrition can be suppressed by lesioning central noradrenaline systems
Schlesinger, L., Arévalo, M., Simon, V., et al. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)00151-d · Cited by 19
Effects of a primary immune response to T-cell dependent antigen on serotonin metabolism in frontal cortex: in vivo microdialysis study in freely moving Fischer 344 rat
Gardier, A. M., Kachaner, S., Shaghaghi, E. K., et al. (1994) · Brain Research · doi:10.1016/0006-8993(94)91648-9 · Cited by 19
Localization of atrial natriuretic peptide, ANP-(99–126) binding sites in the rat thymus and spleen with quantitative autoradiography
Kurihara, M., Shigematsu, K., & Saavedra, J. M. (1986) · Regulatory Peptides · doi:10.1016/0167-0115(86)90164-3 · Cited by 19
Vasoactive Intestinal Peptide (VIP) Inhibits Substrate Adherence Capacity of Rat Peritoneal Macrophages by a Mechanism That Involves cAMP
Segura-Egea, J. J., Guerrero, J. M., López-González, M. A., et al. (1993) · Cell Communication & Adhesion · doi:10.3109/15419069309097255 · Cited by 19
Adrenal hormone deprivation affects macrophage catecholamine metabolism and β2‐adrenoceptor density, but not propranolol stimulation of tumour necrosis factor‐α production
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
Cholinergic Activation Enhances Resistance to Oral Salmonella Infection by Modulating Innate Immune Defense Mechanisms at the Intestinal Barrier
Al-Barazie, R., Bashir, G. H., Qureshi, M. M., Mohamed, Y. A., Al-Sbiei, A., Tariq, S., Lammers, W. J. E. P., al-Ramadi, B. K., & Fernández-Cabezudo, M. J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00551 · Cited by 19
“Specifically, noradrenergic fibers from the sympathetic nervous system have been found in the proximity of DCs in the PPs (9), plasma cells and T cells (10).”
Background
Effects of catecholamines on thymocyte apoptosis and proliferation depend on thymocyte microenvironment
Radojević, K., Rakin, A. K., Pilipović, I., et al. (2014) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2014.04.010 · Cited by 18
“In rodent thymus, there is extensive network of sympathetic noradrenergic nerves extending from interlobulary septa into parenchyma (Williams and Felten, 1981; Felten et al., 1985; Leposavić et al., 1992), which represents main communication channel between central nervous system and thymus.”
Background
Role of nonsynaptic communication in regulating the immune response
Selmeczy, Z., Vizi, E. S., Csóka, B., Pacher, P., & Haskó, G. (2007) · Neurochemistry International · doi:10.1016/j.neuint.2007.06.001 · Cited by 18
“…evidence of nonsynaptic transmission Vizi (1968) Demonstration of the presence of noradrenergic fibers in immune organs Vizi et al. (1995), Felten et al. (1985), Novotny et al. (1990), Weihe et al. (1991) and others Forming of hypothesis of nonsynaptical transmission Vizi (1984)…”
Background
Interferon‐γ and Interleukin‐12 Genes are Preferentially Expressed During Early Experimental African Trypanosomiasis and Suppressed by Denervation of the Spleen
Liu, Ragaa, Li, et al. (1999) · Scandinavian Journal of Immunology · doi:10.1046/j.1365-3083.1999.00639.x · Cited by 18
Neuroenteric peptides affect natural killer activity by intestinal lamina propria mononuclear cells
van Tol, E. A. F., Verspaget, H. W., Hansen, B. E., et al. (1993) · Journal of Neuroimmunology · doi:10.1016/0165-5728(93)90003-h · Cited by 18
Nerves and Neuropeptides in the Regulation of Mucosal Immunity
Bienenstock, J., Croitoru, K., Ernst, P. B., et al. (1989) · Advances in experimental medicine and biology · doi:10.1007/978-1-4684-5712-4_4 · Cited by 18
Physical exercise provokes platelet desensitization in men who smoke cigarettes - involvement of sympathoadrenergic mechanisms - a study of monozygotic twin pairs discordant for smoking
Lassila, R., & Laustiola, K. (1988) · Thrombosis Research · doi:10.1016/0049-3848(88)90058-8 · Cited by 18
Cholinergic agonists selectively induce proliferative responses in the mature subpopulation of murine thymocytes
Rossi, A., Tria, M. A., Baschieri, S., et al. (1989) · Journal of Neuroscience Research · doi:10.1002/jnr.490240305 · Cited by 18
Immunofluorescent Localization of Non-myelinating Schwann Cells and Their Interactions With Immune Cells in Mouse Thymus
Hu, D., Nicholls, P. K., Yin, C., Kelman, K. R., Yuan, Q., Greene, W. K., Shi, Z., & Ma, B. (2018) · Journal of Histochemistry & Cytochemistry · doi:10.1369/0022155418778543 · Cited by 17
Clenbuterol, a Selective β2-Adrenergic Receptor Agonist, Inhibits or Limits Post-Stroke Pneumonia, but Increases Infarct Volume in MCAO Mice
Xu, Y., Ge, Y., Zhou, M., & Zhang, Z. (2022) · Journal of Inflammation Research · doi:10.2147/jir.s344521 · Cited by 17
“It was proposed that splenic atrophy is an essential feature of stroke-induced peripheral immunodepression, and spleen size reduction is correlated to immunodepression.(38,39) To testify whether CLEN influ-”
Background
Physiologic roles of P2 receptors in leukocytes
Alberto, A. V. P., Ferreira, N. C. D. S., Bonavita, A. G. C., Nihei, O. K., de Farias, F. P., Bisaggio, R. D. C., Albuquerque, C., Savino, W., Coutinho‐Silva, R., Persechini, P. M., et al. (2022) · Journal of Leukocyte Biology · doi:10.1002/jlb.2ru0421-226rr · Cited by 19
Disturbances of the gut microbiota-derived tryptophan metabolites as key actors in vagotomy-induced mastitis in mice
He, Y., Zhao, C., Su, N., Yang, W., Yang, H., Yuan, C., Zhang, N., Hu, X., & Fu, Y. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114585 · Cited by 20
Depletion of Neural Crest–Derived Cells Leads to Reduction in Plasma Noradrenaline and Alters B Lymphopoiesis
Tsunokuma, N., Yamane, T., Matsumoto, C., Tsuneto, M., Isono, K., Imanaka‐Yoshida, K., & Yamazaki, H. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502592 · Cited by 17
“Several studies have shown that noradrenergic nerves may innervate a wide variety of lymphoid tissues, including BM (33, 62).”
Background
S100+ cells: A new neuro-immune cross-talkers in lymph organs
Huang, J., Zhu, C., Zhang, P., Zhu, Q., Liu, Y., Zhu, Z., Wang, M., Li, W., Yang, G., Dong, N., et al. (2013) · Scientific Reports · doi:10.1038/srep01114 · Cited by 18
Heroin-associated environmental stimuli modulate the expression of inducible nitric oxide synthase in the rat
Lysle, D. T., & Ijames, S. G. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1208-x · Cited by 17
“organs are innervated by sympathetic nerve fibers (Felten et al. 1985) and immunocytes express functional a- and b-adrenergic receptors with which the sympathetic neu-”
BackgroundInfluential
AKI and the Neuroimmune Axis
Tanaka, S., & Okusa, M. D. (2018) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2018.10.008 · Cited by 17
Molecular characterization of immune derived proenkephalin mRNA and the involvement of the adrenergic system in its expression in rat lymphoid cells
Ovadia, H., Magenheim, Y., Behar, O., & Rosen, H. (1996) · Journal of Neuroimmunology · doi:10.1016/0165-5728(96)00071-9 · Cited by 17
“We were aware of the fact that most of the adrenergic effects on rat lymphoid cells are mediated by ~ adrenergic agonists via ~ adrenergic receptors (Luecken and Lysle, 1992; Felsner et al., 1995; Wiegmann et al., 1995; Felten et al., 1985).”
Background
Age-related effect of peptide YY (PYY) on paw edema in the rat: The function of Y1 receptors on inflammatory cells
Stanojević, S., Vujić, V., Kovačević‐Jovanović, V., et al. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.05.012 · Cited by 17
The predicting role of substance P in the neoplastic transformation of the hypoplastic bone marrow
Nowicki, M. O., Ostalska‐Nowicka, D., Konwerska, A., et al. (2006) · Journal of Clinical Pathology · doi:10.1136/jcp.2005.034629 · Cited by 17
Opioids, Opioid Receptors, and the Immune System
Gomez‐Flores, R., & Weber, R. J. (1998) · CRC Press eBooks · doi:10.1201/9781420048193.ch20 · Cited by 18
A cocaine-sensitive active dopamine transport in human lymphocytes
Faraj, B. A., Olkowski, Z. L., & Jackson, R. T. (1995) · Biochemical Pharmacology · doi:10.1016/0006-2952(95)00230-w · Cited by 17
Properties of vasoactive‐intestinal‐peptide receptors and β‐adrenoceptors in the murine radiation leukemia‐virus‐induced lymphoma cell line BL/VL3
Abello, J., Damien, C., NEEF, P. D., et al. (1989) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1989.tb14922.x · Cited by 17
Acute Inhibition of Inflammation Mediated by Sympathetic Nerves: The Inflammatory Reflex
Occhinegro, A., McAllen, R. M., McKinley, M. J., & Martelli, D. (2023) · NeuroImmunoModulation · doi:10.1159/000531469 · Cited by 18
“Several lines of evidence seem to support this theory: (1) sympathetic nerves extensively innervate primary and secondary lymphoid organs [8] as well as the adrenal gland, which can release catecholamines into the bloodstream when pregan-glionic splanchnic sympathetic ﬁ bres are activated; (2) all…”
Result
Exploring the complex interplay: gut microbiome, stress, and leptospirosis
Petakh, P., Oksenych, V., Kamyshna, I. I., Boisak, I., Lyubomirskaya, K., & Kamyshnyi, O. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1345684 · Cited by 16
“In the spleen, sympathetic innervation is regional and specific, primarily found in the white pulp surrounding central arteries, which predominantly comprises T-lymphocytes (Felten et al., 1985; Kraal, 1992).”
Background
Studying brain-regulation of immunity with optogenetics and chemogenetics; A new experimental platform
Ben-Shaanan, T. L., Schiller, M., & Rolls, A. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.11.024 · Cited by 16
Neuroimmune interactions and kidney disease
Hasegawa, S., Inoue, T., & Inagi, R. (2019) · Kidney Research and Clinical Practice · doi:10.23876/j.krcp.19.014 · Cited by 17
“[6] Felten DL, Felten SY, Carlson SL, Olschowka JA, Livnat S.”
Background
The role of tachykinins on bacterial infections
David, W. (2004) · Frontiers in bioscience · doi:10.2741/1473 · Cited by 16
“This close approximation between lymphocytes and nerve fibers (67, 89, 90), especially mucosal sites in the gut, provides physical evidence for cross-communication between the immune and nervous systems.”
Background
Occurrence of adrenergic nerve fibers in human thymus during immune response
Cavallotti, D., Artico, M., Iannetti, G. D., et al. (2002) · Neurochemistry International · doi:10.1016/s0197-0186(01)00074-2 · Cited by 16
Nicotinic Neuronal Acetylcholine Receptor α‐3 Subunit Transcription in Normal and Myasthenic Thymusa
Mihovilovic, M., Hulette, C., MITTELSTAEDT, J., et al. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb22872.x · Cited by 16
Pharmacological effects of fermented red pepper
Choi, Y., & Suh, H. J. (2004) · Phytotherapy Research · doi:10.1002/ptr.1490 · Cited by 16
“Sensory nerve fibers have been clearly demonstrated within primary and secondary lymphoid organs including thymus, spleen, tonsils and lymph nodes (Lorton et al., 1991; Felten et al., 1992).”
Background
MIND-BODY THERAPIES FOR PRIMARY CARE PHYSICIANS
Chiaramonte, D. R. (1997) · Primary Care Clinics in Office Practice · doi:10.1016/s0095-4543(05)70310-9 · Cited by 16
Pharmacology and Biochemistry of Synaptic Transmission: Classic Transmitters
Deutch, A. Y., & Roth, R. H. (2004) · Elsevier eBooks · doi:10.1016/b978-012148660-0/50010-x · Cited by 22
Sensory innervation of conjunctival lymph follicles in cynomolgus monkeys.
Ruskell, G. L., & VanderWerf, F. (1997) · PubMed · Cited by 16
Immunological stress in rats induces bodily alterations in saline-treated conspecifics
Fernandes, G. A. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00226-7 · Cited by 16
Involvement of central opioidergic and nonopioidergic neuroendocrine systems in the suppressive effect of acupuncture on delayed type hypersensitivity in mice.
Kasahara, T., Amemiya, M., Wu, Y.-X., & Oguchi, K. (1993) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(93)90064-6 · Cited by 13
Inhibitory effect of vasoactive intestinal peptide (VIP) on phagocytosis in mouse peritoneal macrophages
Ichinose, M., Sawada, M., & Maeno, T. (1994) · Regulatory Peptides · doi:10.1016/0167-0115(94)90543-6 · Cited by 16
Impairment of rat thymocyte differentiation and functions by neonatal capsaicin treatment is associated with induction of apoptosis
Santoni, G., Perfumi, M. C., Pompei, P., et al. (2000) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00249-0 · Cited by 16
“This receptor, named vanilloid receptor subtype 1 lymphoid organs (Felten et al., 1985; Geppetti et al., 1987; (VR1), is a non-selective cation channel structurally Felten and Felten, 1989; Bellinger et al., 1990; Lorton et related to members of the transient receptor potential al., 1990).”
Background
Immunoreactivity of Neural Crest-Derived Cells in Thymic Tissue Developing under the Rat Kidney Capsule
Jones, G. V., Botham, C. A., Clarke, A. G., et al. (1998) · Brain Behavior and Immunity · doi:10.1006/brbi.1998.0528 · Cited by 16

Authors: Felten, D. L., Felten, S. Y., Carlson, S. L., Olschowka, J. A., & Livnat, S.
Affiliations: University of Rochester Medicine (US)
ORCID: Carlson, S L
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 1985-08-01
Volume: 135
Issue: 2
Pages: 755-765
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.135.2.755
OpenAlex: W79466244
Cited by: 1,025
References: 0
Citations by year: 2026: 15 · 2025: 13 · 2024: 15 · 2023: 17 · 2022: 23 · 2021: 23 · 2020: 13 · 2019: 21 · 2018: 26 · 2017: 12 · 2016: 23 · 2015: 16 · 2014: 22 · 2013: 20 · 2012: 24
FWCI: 12.00
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: noradrenergic innervation, sympathetic nerve fibers, lymphoid tissue, thymus, spleen, lymph nodes, gut-associated lymphoid tissue, bone marrow, vasoactive intestinal peptide, neuropeptide Y, substance P, neurokinin-1 receptor, neurokinin-2 receptor, neurokinin-3 receptor, neurotensin, substance P antagonist
MeSH terms: Adrenergic Fibers, Animals, Appendix, Bone Marrow, Intestines, Lymph Nodes, Lymphocytes, Lymphoid Tissue, Nerve Tissue Proteins, Norepinephrine, Rabbits, Spleen, Thymus Gland, Neurotransmitter Agents, Mice, Rats

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

Noradrenergic and peptidergic innervation of lymphoid tissue

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cited by

Related

Metadata

Record

About these checks