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Noradrenergic and peptidergic innervation of lymphoid tissue
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.
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Antibody response to vaccination and psychosocial stress in humans: relationships and mechanisms
Burns, V. E., Carroll, D., Ring, C., & Drayson, M. T. (2003) · Vaccine · doi:10.1016/s0264-410x(03)00041-0 · Cited by 76
“The sympathetic nervous system provides another possible link between stress and immune function, either in the form of catecholamine secretion or via the direct innervation of the lymphoid organs [73].”
BackgroundNeuropeptides and gastrointestinal immunity
O'Dorisio, M. S. (1986) · The American Journal of Medicine · doi:10.1016/0002-9343(86)90587-5 · Cited by 74
Venlafaxine exhibits an anti-inflammatory effect in an inflammatory co-culture model
Vollmar, P., Haghikia, A., Dermietzel, R., & Faustmann, P. M. (2007) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145707007729 · Cited by 75
Gomariz, R. P., Lorenzo, M. J. V., Cacicedo, L., et al. (1990) · Brain Behavior and Immunity · doi:10.1016/0889-1591(90)90017-k · Cited by 75
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Jarillo‐Luna, A., Rivera‐Aguilar, V., Reyna-Garfias, H., Lara‐Padilla, E., Kormanovski, A., & Campos-Rodrı́guez, R. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.04.009 · Cited by 74
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BackgroundNeuroendocrine-immune interactions in teleost fish
Kemenade, B. M. L. V.-V., Stolte, E. H., Metz, J. R., & Chadzińska, M. (2009) · Cited by 74
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Wagner, F. M., Fink, R., Hart, R., et al. (1987) · Regulatory Peptides · doi:10.1016/0167-0115(87)90177-7 · Cited by 74
Wei, Y., Xu, J., Miao, S., Wei, K., Peng, L., Wang, Y., & Wei, X. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2048291 · Cited by 73
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Seifert, H. A., & Offner, H. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1239-9 · Cited by 73
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BackgroundKulkarni‐Narla, A., Beitz, A. J., & Brown, D. R. (1999) · Cell and Tissue Research · doi:10.1007/s004419900096 · Cited by 73
Schiller, M., Azulay‐Debby, H., Boshnak, N., Elyahu, Y., Korin, B., Ben-Shaanan, T. L., Koren, T., Krot, M., Hakim, F., & Rolls, A. (2021) · Immunity · doi:10.1016/j.immuni.2021.04.007 · Cited by 73
Qiu, Y., Peng, Y.-P., Jiang, J., et al. (2004) · NeuroImmunoModulation · doi:10.1159/000075316 · Cited by 72
Opioid-induced immunosuppression: is it centrally mediated or peripherally mediated?
Wei, G., Moss, J., & Yuan, C.-S. (2003) · Biochemical Pharmacology · doi:10.1016/s0006-2952(03)00085-6 · Cited by 72
Lorton, D., Bellinger, D. L., Felten, S. Y., et al. (1991) · Brain Behavior and Immunity · doi:10.1016/0889-1591(91)90005-u · Cited by 72
Self-citationDecreased sympathetic innervation of spleen in aged fischer 344 rats
Felten, S. Y., Bellinger, D. L., Collier, T. J., et al. (1987) · Neurobiology of Aging · doi:10.1016/0197-4580(87)90026-1 · Cited by 72
Self-citationNeuroimmunomodulation: facts and dilemmas
Janković, B. D. (1989) · Immunology Letters · doi:10.1016/0165-2478(89)90046-1 · Cited by 72
Cosentino, M., Marino, F., & Maestroni, G. J. M. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00302 · Cited by 63
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BackgroundChronic morphine treatment selectively suppresses macrophage colony formation in bone marrow
Roy, S., Ramakrishnan, S., Loh, H. H., et al. (1991) · European Journal of Pharmacology · doi:10.1016/0014-2999(91)90476-7 · Cited by 71
Yanagawa, Y., Matsumoto, M., & Togashi, H. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001899 · Cited by 68
“organs, including thymus, spleen, lymph nodes, GALT, and bone marrow (6).”
BackgroundSympathetic nervous system interaction with the immune system
Sanders, V. M., & Kohm, A. P. (2002) · International review of neurobiology · doi:10.1016/s0074-7742(02)52004-3 · Cited by 73
Neural control of immune cell trafficking
Mueller, S. N. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20211604 · Cited by 72
Adaptive immunity, chronic inflammation and the clock
Gray, K. J., & Gibbs, J. E. (2022) · Seminars in Immunopathology · doi:10.1007/s00281-022-00919-7 · Cited by 69
“1 3 (including primary and secondary lymphoid organs [104]), providing highly localised signals [105].”
BackgroundRegulatory mechanisms in lymphatic vessel contraction under normal and inflammatory conditions
von der Weid, P., & Muthuchamy, M. (2009) · Pathophysiology · doi:10.1016/j.pathophys.2009.10.005 · Cited by 70
“[109] D.”
BackgroundChiocchetti, R., Mazzuoli‐Weber, G., Albanese, V., Mazzoni, M., Clavenzani, P., Lalatta‐Costerbosa, G., Lucchi, M. L., Guardo, G. D., Marruchella, G., & Furness, J. B. (2008) · Cell and Tissue Research · doi:10.1007/s00441-008-0583-y · Cited by 69
“Bars 800 μm (a, b), 400 μm (c), 200 μm (d), 100 μm (e, h), 50 μm (f, g, i, j, k) R phoid organs provides an important functional link between the nervous and immune systems and may be involved in regulating immune development (Felten et al. 1985, 1987, 1988; Sharkey 1992).”
BackgroundEgan, C. L., Viglione‐Schneck, M. J., Walsh, L. J., et al. (1998) · Journal of Cutaneous Pathology · doi:10.1111/j.1600-0560.1998.tb01685.x · Cited by 69
Disease-associated PrP in the enteric nervous system of scrapie-affected Suffolk sheep
Heggebø, R., González, L., Press, C. M., Gunnes, G., Espenes, A., & Jeffrey, M. (2003) · Journal of General Virology · doi:10.1099/vir.0.18874-0 · Cited by 68
“Immunocytochemical studies of the innervation of mammalian lymphoid tissue have mostly been done in rodents and have shown that B-cell-dominated germinal centres contain few or no nerve fibres in contrast to the rich network in the surrounding T-cell regions (Felten et al., 1985; Felten & Felten, 1988; Lorton et al.,…”
BackgroundInfluentialAckerman, K. D., Felten, S. Y., Bellinger, D. L., & Felten, D. L. (1987) · Journal of Neuroscience Research · doi:10.1002/jnr.490180109 · Cited by 66
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Madsen, C. B., Claësson, M. H., & Röpke, C. (1996) · Toxicology · doi:10.1016/0300-483x(95)03244-a · Cited by 69
Regulation of the immune system by sympathetic neural mechanisms
Livnat, S., Madden, K. S., Felten, D. L., & Felten, S. Y. (1987) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(87)90052-2 · Cited by 69
Self-citationVasoactive intestinal peptide-containing nerves in Peyer's patches
Ottaway, C. A., Lewis, D. L., & Asa, S. L. (1987) · Brain Behavior and Immunity · doi:10.1016/0889-1591(87)90017-1 · Cited by 67
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Scicchitano, R., Dazin, P. F., Bienenstock, J., et al. (1987) · Brain Behavior and Immunity · doi:10.1016/0889-1591(87)90019-5 · Cited by 68
Delgado, M., Garrido, E. A. R., Martinez, C., Leceta, J., & Gomariz, R. (1996) · Blood · doi:10.1182/blood.v87.12.5152.bloodjournal87125152 · Cited by 69
Neuroendocrine Regulation of Skin Dendritic Cells
Seiffert-Sinha, K., & Granstein, R. D. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1366.011 · Cited by 69
Martelli, D., Farmer, D., McKinley, M. J., Yao, S. T., & McAllen, R. M. (2018) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00298.2018 · Cited by 67
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BackgroundChapter 20 Neural-immune interactions
Felten, S. Y., & Felten, D. L. (1994) · Progress in brain research · doi:10.1016/s0079-6123(08)60781-5 · Cited by 67
Self-citationGruber, B. L., HALL, N. R. S., Hersh, S. P., & Dubois, P. (1988) · Scandinavian Journal of Behaviour Therapy · doi:10.1080/16506078809455814 · Cited by 67
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Haugen, P., & Letourneau, P. C. (1990) · Journal of Neuroscience Research · doi:10.1002/jnr.490250402 · Cited by 67
Alterations in sympathetic innervation of thymus and spleen in aged mice
Madden, K. S., Bellinger, D. L., Felten, S. Y., et al. (1997) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(96)01858-1 · Cited by 66
Self-citationDistribution of NGF receptors in normal and pathologic human lymphoid tissues
Labouyrie, E., Parrens, M., de Mascarel, A., Bloch, B., & Merlio, J. (1997) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(97)00055-6 · Cited by 67
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Sisó, S., González, L., & Jeffrey, M. (2010) · Interdisciplinary Perspectives on Infectious Diseases · doi:10.1155/2010/747892 · Cited by 65
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BackgroundCharacterization of opiate binding sites on membranes of rat lymphocytes
Ovadia, H., Nitsan, P., & Abramsky, O. (1989) · Journal of Neuroimmunology · doi:10.1016/0165-5728(89)90165-3 · Cited by 65
Hasegawa‐Ishii, S., Inaba, M., Umegaki, H., Unno, K., Wakabayashi, K., & Shimada, A. (2016) · Scientific Reports · doi:10.1038/srep25457 · Cited by 65
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Rajda, C., Bencsik, K., Vécsei, L., et al. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00002-4 · Cited by 64
Dawidson, I., Angmar-Månsson, B., Blom, M., et al. (1998) · Neuropeptides · doi:10.1016/s0143-4179(98)90083-x · Cited by 64
Mota, C. M. D., & Madden, C. J. (2022) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00151.2022 · Cited by 67
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“Post-ganglionic neurons innervate all primary and secondary lymphoid organs where norepinephrine is stored within the nerve terminals [64, 65].”
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Hall, D. M., Suo, J.-L., & Weber, R. J. (1998) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(97)00218-x · Cited by 63
Preproenkephalin mRNA in T‐Cells, macrophages, and mast cells
Martin, J. S., Prystowsky, M. B., & Angeletti, R. H. (1987) · Journal of Neuroscience Research · doi:10.1002/jnr.490180114 · Cited by 63
Bellinger, D. L., Felten, S. Y., & Felten, D. L. (1988) · Brain Behavior and Immunity · doi:10.1016/0889-1591(88)90014-1 · Cited by 62
Self-citationBuckley, T. L., & Nijkamp, F. P. (1994) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.149.2.8306037 · Cited by 62
Hasegawa, S., Inoue, T., Nakamura, Y., Fukaya, D., Uni, R., Wu, C.-H., Fujii, R., Peerapanyasut, W., Taguchi, A., Kohro, T., et al. (2021) · Journal of the American Society of Nephrology · doi:10.1681/asn.2020121723 · Cited by 62
Parallel development of noradrenergic innervation and cellular compartmentation in the rat spleen
Ackerman, K. D., Felten, S. Y., Dijkstra, C. D., et al. (1989) · Experimental Neurology · doi:10.1016/0014-4886(89)90048-4 · Cited by 61
Self-citationAdrenergic Modulation of Hematopoiesis
Maestroni, G. J. M. (2019) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-019-09840-7 · Cited by 61
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Rameshwar, P., Gascón, P., & Ganea, D. (1992) · Journal of Neuroimmunology · doi:10.1016/0165-5728(92)90156-f · Cited by 60
Delgado, M., Pozo, D., Martínez, C., et al. (1996) · Regulatory Peptides · doi:10.1016/0167-0115(96)00024-9 · Cited by 60
Elenkov, I. J., & Vizi, E. S. (1991) · Neuropharmacology · doi:10.1016/0028-3908(91)90029-b · Cited by 60
Gottesfeld, Z., Christie, R. H., Felten, D. L., et al. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90133-o · Cited by 60
Self-citationNeuroendocrine regulation of innate lymphoid cells
Quatrini, L., Vivier, É., & Ugolini, S. (2018) · Immunological Reviews · doi:10.1111/imr.12707 · Cited by 58
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Saurer, T. B., Ijames, S. G., & Lysle, D. T. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2006.05.002 · Cited by 59
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Sharkey, K. A., & Savidge, T. (2013) · Autonomic Neuroscience · doi:10.1016/j.autneu.2013.12.006 · Cited by 62
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Leach, S., & Suzuki, K. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01235 · Cited by 57
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BackgroundMurine hematopoietic stem cells and progenitors express adrenergic receptors
Muthu, K., Iyer, S., He, L.-K., Szilágyi, A., Gamelli, R. L., Shankar, R., & Jones, S. B. (2007) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2007.02.007 · Cited by 58
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BackgroundStress‐Induced Immune Suppression Role of the Autonomic Nervous Systema
Irwin, M. R. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb49933.x · Cited by 56
Rícci, A., Veglio, F., & Amenta, F. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(95)00004-l · Cited by 58
Expression of the myelin proteolipid protein gene in the human fetal thymus
Pribyl, T. M., Campagnoni, C. W., Kampf, K., et al. (1996) · Journal of Neuroimmunology · doi:10.1016/0165-5728(96)00058-6 · Cited by 58
Kim, B.-J., & Jones, H. P. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.05.003 · Cited by 57
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BackgroundMa, B., von Wasielewski, R., Lindenmaier, W., & Dittmar, K. E. J. (2007) · Anatomia Histologia Embryologia · doi:10.1111/j.1439-0264.2006.00741.x · Cited by 60
“For example, the noradrenergic and peptidergic innervation of various lymphoid tissues have been investigated by several approaches (Felten et al., 1985).”
BackgroundInfluentialA Molecular Basis for Interactions Between the Immune and Neuroendocrine Systems
Smith, E. M., & Blalock, J. E. (1988) · International Journal of Neuroscience · doi:10.3109/00207458808990706 · Cited by 57
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Garssen, J., Buckley, T. L., & Loveren, H. V. (1998) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.1998.tb02490.x · Cited by 57
Neuroendocrine-Immune Crosstalk Shapes Sex-Specific Brain Development
Arambula, S. E., & McCarthy, M. M. (2020) · Endocrinology · doi:10.1210/endocr/bqaa055 · Cited by 55
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BackgroundDynamic norepinephrine alterations in bone marrow: evidence of functional innervation
Tang, Y., Shankar, R., Gamelli, R. L., & Jones, S. B. (1999) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00032-6 · Cited by 55
“Varicose noradrenergic nerve fibers, however, are reported to enter the bone marrow compartment as arteriolar plexuses which then distribute in surrounding parenchyma and end among Žhemato- and lymphopoietic cells Felten et al., 1985; .”
BackgroundThe immune system and integrated homeostasis
Husband, A. J. (1995) · Immunology and Cell Biology · doi:10.1038/icb.1995.58 · Cited by 57
Topography of the enteric nervous system in Peyer's patches of the porcine small intestine
Krammer, H.-J., & K�hnel, W. (1993) · Cell and Tissue Research · doi:10.1007/bf00302732 · Cited by 54
“vation of the pr imary and secondary lymphoid organs (Felten et al. 1985; Kendall et al. 1988; Ackerman et al. 1986; Madden et al. 1989; Van Tits et al. 1990).”
BackgroundSubstance P-like immunoreactivity in capsaicin-sensitive structures of the rat thymus
Geppetti, P., Maggi, C. A., Zecchi‐Orlandini, S., et al. (1987) · Regulatory Peptides · doi:10.1016/0167-0115(87)90189-3 · Cited by 56
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/bf01996098 · Cited by 56
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BackgroundRegulation of the Autonomic Nervous System on Intestine
Duan, H., Cai, X., Luan, Y., Yang, S., Yang, J., Dong, H. F., Zeng, H., & Shao, L. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.700129 · Cited by 62
D’Ambrosio, F., Caggiano, M., Schiavo, L., Savarese, G., Carpinelli, L., Amato, A., & Iandolo, A. (2022) · Dentistry Journal · doi:10.3390/dj10030049 · Cited by 55
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BackgroundNeuroimmunology of the gut: physiology, pathology, and pharmacology
Ben‐Horin, S., & Chowers, Y. (2008) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.07.010 · Cited by 55
Bencsics, A., Elenkov, I. J., & Vizi, E. S. (1997) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(96)00163-4 · Cited by 55
Janković, B. D., & Radulović, J. (1992) · International Journal of Neuroscience · doi:10.3109/00207459208994788 · Cited by 55
Kraneveld, A. D., Rijnierse, A., Nijkamp, F. P., & Garssen, J. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.02.095 · Cited by 57
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BackgroundRoth, N., Beyreiss, J., Schlenzka, K., et al. (1991) · Research on Child and Adolescent Psychopathology · doi:10.1007/bf00910561 · Cited by 55
Xin, Z., Tang, H., & Ganea, D. (1994) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)90231-3 · Cited by 55
Ganea, D., & Lei, S. (1993) · Journal of Neuroimmunology · doi:10.1016/0165-5728(93)90025-t · Cited by 55
Transneuronal mapping of the CNS network controlling sympathetic outflow to the rat thymus
Trotter, R. N., Stornetta, R. L., Guyenet, P. G., & Roberts, M. R. (2006) · Autonomic Neuroscience · doi:10.1016/j.autneu.2006.06.001 · Cited by 54
Adrenoceptor-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 57
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BackgroundInsular Cortex Lesions Impair the Acquisition of Conditioned Immunosuppression
Ramı́rez-Amaya, V., Alvarez-Borda, B., Ormsby, C. E., Martı́nez, R. D., Pérez‐Montfort, R., & Bermúdez‐Rattoni, F. (1996) · Brain Behavior and Immunity · doi:10.1006/brbi.1996.0011 · Cited by 55
Nöhr, D., & Weihe, E. (1991) · Brain Behavior and Immunity · doi:10.1016/0889-1591(91)90009-y · Cited by 54
Fleshner, M., Watkins, L. R., Lockwood, L. L., Bellgrau, D., Laudenslager, M. L., & Maier, S. F. (1992) · Journal of Neuroimmunology · doi:10.1016/0165-5728(92)90063-q · Cited by 54
Histochemical and molecular overview of the thymus as site for T-cells development
Rezzani, R., Bonomini, F., & Rodella, L. F. (2008) · Progress in Histochemistry and Cytochemistry · doi:10.1016/j.proghi.2008.03.001 · Cited by 55
Leposavić, G., Pilipović, I., Radojević, K., Pešić, V., Nanut, M. P., & Kosec, D. J. (2008) · Autonomic Neuroscience · doi:10.1016/j.autneu.2008.09.003 · Cited by 53
Dhawan, S., Palma, G. D., Willemze, R., Hilbers, F., Verseijden, C., Luyer, M., Nuding, S., Wehkamp, J., Souwer, Y., de Jong, E. C., et al. (2016) · American Journal of Physiology - Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00114.2016 · Cited by 48
“As we demonstrate, the presence of this cell population is not restricted to the spleen but can also be found in other lymphoid structures such as Peyer’s patches or MLNs that present with a comparable distribution of adrenergic fibers (13).”
BackgroundResultNeuroendocrine influences in psychoimmunology and neoplasia: A review
Antoni, M. H. (1987) · Psychology and Health · doi:10.1080/08870448708400311 · Cited by 52
Conditioned medium from activated splenocytes increases substance P in sympathetic ganglia
Jonakait, G. M., & SCHOTLAND, S. (1990) · Journal of Neuroscience Research · doi:10.1002/jnr.490260104 · Cited by 51
A Clinical Approach for the Use of VIP Axis in Inflammatory and Autoimmune Diseases
Martínez, C., Juarranz, Y., Gutiérrez‐Cañas, I., Carrión, M., Pérez‐García, S., Villanueva‐Romero, R., Castro, D. M., Lamana, A., Mellado, M., González‐Álvaro, I., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms21010065 · Cited by 52
“Although synovitis is usually localized and may be asymptomatic in OA [24], synovial activation causes the release of inflammatory mediators and proteases that accelerate the progression of the disease [2,25,26].”
BackgroundLorton, D., Hewitt, D., Bellinger, D. L., et al. (1990) · Brain Behavior and Immunity · doi:10.1016/0889-1591(90)90023-j · Cited by 51
“…S. Felten, Lorton, & D. Felten, 1989a; Bellinger, S. Felten, Lorton, & D. Felten, 1989b), spleen (Williams & Felten, 1981; Williams et al. 1981; D. Felten et al., 1985; S. Felten et al., 1988b; D. Felten, Ackerman, Wiegand, & S. Felten, 1987a; S. Felten & Olschowka, 1987; Ackerman, S. Felten,…”
Self-citationDopamine D1-like receptor subtypes in human peripheral blood lymphocytes
Rícci, A., Bronzetti, E., Mignini, F., Tayebati, S. K., Zaccheo, D., & Amenta, F. (1999) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00042-9 · Cited by 51
Adrenergic innervation in reactive human lymph nodes
Panuncio, A., de la Peña, S., Gualco, G., & Reissenweber, N. J. (1999) · Journal of Anatomy · doi:10.1046/j.1469-7580.1999.19410143.x · Cited by 50
“The distribution of nerve fibres in normal lymph nodes has been demonstrated in mice and rats (Felten et al. 1984, 1985; Novotny & Kliche, 1986; Villaro et al. 1987; Novotny et al. 1993, 1994, 1995a, b), but little information is available about the innervation of human lymph nodes (Volik, 1965;…”
BackgroundTreatment of Distal Colitis with Local Anaesthetic Agents
Björck, S., Dahlström, A. B., & Ahlman, H. (2002) · Pharmacology & Toxicology · doi:10.1034/j.1600-0773.2002.900401.x · Cited by 51
Metadata
- 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
- 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
- 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
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