Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Open Medicine

formerly Central European Journal of Medicine

Editor-in-Chief: Darzynkiewicz, Zbigniew


IMPACT FACTOR 2018: 1.221

CiteScore 2018: 1.01

SCImago Journal Rank (SJR) 2018: 0.329
Source Normalized Impact per Paper (SNIP) 2018: 0.479

ICV 2017: 152.94

Open Access
Online
ISSN
2391-5463
See all formats and pricing
More options …
Volume 1, Issue 4

Issues

Volume 10 (2015)

Sympathetic nervous system and neurotransmitters: their possible role in neuroimmunomodulation of multiple sclerosis and some other autoimmune diseases

Vladimir Markelov / Maxim Trushin
  • Laboratory of Molecular Pathogenesis, Kazan Institute of Biochemistry and Biophysics, P.O. Box 30, 420111, Kazan, Russia
  • Department of Genetics, Kazan State University, 420008, Kazan, Russia
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2006-09-26 | DOI: https://doi.org/10.2478/s11536-006-0031-x

Abstract

Multiple sclerosis is still a disease without a cure. Although intensive research efforts have led to the development of drugs that modify the activity of the disease, most of them have various side effects and are expensive. At the same time it is becoming apparent that some remedies usually used to treat somatic and psychic disorders also have immunomodulating properties, and may help manage multiple sclerosis and other autoimmune diseases. We describe here the role of the sympathetic nervous system in the neuro-immune interaction in multiple sclerosis and other immune diseases with increased cellular immunity as well as neurochemical disturbances that take place in these disorders.

Keywords: Multiple sclerosis; neuroimmunomodulation; sympathetic nervous system; adrenoreceptor; neurotransmitter; autoimmune disease

  • [1] S.Y. Felten, D.L. Felten, D.L. Bellinger, S.L. Carlson, K.D. Ackerman, K.S. Madden, J.A. Ol-schowka and S. Livnat: “Noradrenergic sympathetic innervation of lymphoid organs”, Prog. Allergy., Vol. 43, (1988), pp. 14–36. Google Scholar

  • [2] K.S. Madden, V.M. Sanders and D.L. Felten: “Catecholamine influences and sympathetic neural modulation of immune responsiveness”, Annu. Rev. Pharmacol. Toxicol., Vol. 35, (1995), pp. 417–448. CrossrefGoogle Scholar

  • [3] A.B. Dahlstro and B.E.M. Zetterstrom: “Noradrenaline stores in nerve terminals of the spleen: changes during hemorrhagic shock”, Science (Wash DC), Vol. 147, (1965), pp. 1583–1585. CrossrefGoogle Scholar

  • [4] B.E. Zetterstrom, T. Hokfelt, K.A. Norberg and P. Olsson: “Possibilities of a direct adrenergic influence on blood elements in the dog spleen”, Acta Chir. Scand., Vol. 139, (1973), pp. 117–122. Google Scholar

  • [5] F.D. Reilly, R.S. McCuskey and H.A. Meineke: “Studies of the hemopoietic microenvironment. VIII. Andrenergic and cholinergic innervation of the murine spleen”, Anat. Rec., Vol. 185, (1976), pp. 109–117. Google Scholar

  • [6] F.D. Reilly, P.A. McCuskey, M.L. Miller, R.S. McCuskey and H.A. Meineke: “Innervation of the periarteriolar lymphatic sheath of the spleen”, Tissue Cell, Vol. 11, (1979), pp. 121–126. Google Scholar

  • [7] M.G. Blennerhassett and J. Bienenstock: “Sympathetic nerve contact causes maturation of mast cells in vitro”, J. Neurobiol., Vol. 35, (1998), pp. 173–182. CrossrefGoogle Scholar

  • [8] A.S. Maisel, T. Harris, C.A. Rearden and M.C. Michel: “Beta-adrenergic receptors in lymphocyte subsets after exercise. Alterations in normal individuals and pa-tients with congestive heart failure”, Circulation, Vol. 2, (1990), pp. 2003–2010. CrossrefGoogle Scholar

  • [9] M.M. Khan, P. Sansoni, E.D. Silverman, E.G. Engleman and K.L. Melmon: “Beta-adrenergic receptors on human suppressor, helper, and cytolytic lymphocytes”, Biochem. Pharmacol., Vol. 35, (1986), pp. 1137–1142. CrossrefGoogle Scholar

  • [10] Z. Zidek: “Adenosine-cyclic AMP pathways and cytokine expression”, Eur. Cytokine Netw., Vol. 10, (1999), pp. 319–328. PubMedGoogle Scholar

  • [11] I.J. Elenkov, G. Hasko, K.J. Kovacs and E.S. Vizi: “Modulation of lipopolysaccharide-induced tumor necrosis factor-alpha production by selective alpha-and betaadrenergic drugs in mice”, J. Neuroimmunol., Vol. 61, (1995), pp. 123–131. CrossrefGoogle Scholar

  • [12] I.J. Elenkov, D.A. Papanicolaou, R.L. Wilder and G.P. Chrousos: “Modulatory effects of glucocorticoids and catecholamines on human interleukin-12 and interleukin-10 production: clinical implications”, Proc. Assoc. Am. Physicians, Vol. 108, (1996), pp. 374–381. Google Scholar

  • [13] I.J. Elenkov, E. Webster, D.A. Papanicolaou, T.A. Fleisher, G.P. Chrousos and R.L. Wilder: “Histamine potently suppresses human IL-12 and stimulates IL-10 production via H2 receptors”, J. Immunol., Vol. 161, (1998), pp. 2586–2593. Google Scholar

  • [14] T.C. van der Pouw Kraan, L.C. Boeije, R.J. Smeenk, J. Wijdenes and L.A. Aarden: “Prostaglandin-E2 is a potent inhibitor of human interleukin 12 production”, J. Exp. Med., Vol. 181, (1995), pp. 775–779. Google Scholar

  • [15] G. Hasko, C. Szabo, Z.H. Nemeth, V. Kvetan, S.M. Pastores, E.S. Vizi: “Adenosine receptor agonists differentially regulate IL-10, TNF-alpha, and nitric oxide productionin RAW 264.7 macrophages and in endotoxemic mice”, J. Immunol., Vol. 157, (1996), pp. 4634–4640. Google Scholar

  • [16] A.A. Link, T. Kino, J.A. Worth, J.L. McGuire, M.L. Crane, G.P. Chrousos, R.L. Wilder and I.J. Elenkov: “Ligand-activation of the adenosine A2a receptors inhibits IL-12 production by human monocytes”, J. Immunol., Vol. 164, (2000), pp. 436–442. CrossrefGoogle Scholar

  • [17] M.M. Bartik, W.H. Brooks and T.L. Roszman: “Modulation of T cell proliferation by stimulation of the beta-adrenergic receptor: lack of correlation between inhibition of T cell proliferation and cAMP accumulation”, Cell. Immunol., Vol. 148, (1993), pp. 408–421. CrossrefGoogle Scholar

  • [18] P. Panina-Bordignon, D. Mazzeo, P.D. Lucia, D. D’Ambrosio, R. Lang, L. Fabbri, C. Self and F. Sinigaglia: “Beta2-agonists prevent Th1 development by selective inhibition of interleukin 12”, J. Clin. Invest., Vol. 100, (1997), pp. 1513–1519. CrossrefGoogle Scholar

  • [19] G. Hasko, Z.H. Nemeth, C. Szabo, G. Zsilla, A.L. Salzman and E.S. Vizi: “Isoproterenol inhibits Il-10, TNF-alpha, and nitric oxide production in RAW 264.7 macrophages”, Brain Res. Bull., Vol. 45, (1998), pp. 183–187. CrossrefGoogle Scholar

  • [20] R.T. Johnson: “The virology of demyelinating diseases”, Ann. Neurol., Vol. 36 (Suppl.), (1994), pp. S54–60. Google Scholar

  • [21] S.S. Soldan, T.P. Leist, K.N. Juhng, H.F. Mc-Farland and S. Jacobson: “Increased lymphoproliferative response to human herpesvirus type 6A variant in multiple sclerosis patients”, Ann. Neurol., Vol. 47, (2000), pp. 306–313. Google Scholar

  • [22] S.S. Soldan and S. Jacobson: “Role of viruses in etiology and pathogenesis of multiple sclerosis”, Adv. Virus Res., Vol. 56, (2001), pp. 517–555. CrossrefGoogle Scholar

  • [23] K.P. Wandinger, W. Jabs, A. Siekhaus, S. Bubel and P. Trillenberg: “Association between clinical disease activity and Epstein-Barr virus reactivation in MS”, Neurology, Vol. 55, (2000), pp. 178–184. CrossrefGoogle Scholar

  • [24] C.N. Martyn, M. Cruddas, D.A. Compston: “Symptomatic Epstein-Barr virus infection and multiple sclerosis”, J. Neurol. Neurosurg. Psychiatry, Vol. 56, (1993), pp. 167–168. CrossrefGoogle Scholar

  • [25] S. Sriram, W. Mitchell and C. Stratton: “Multiple sclerosis associated with Chlamydia pneumoniae infection of the CNS”, Neurology, Vol. 50, (1998), pp. 571–572. CrossrefGoogle Scholar

  • [26] S. Sriram, C.W. Stratton, S. Yao, A. Tharp and L. Ding: “Chlamydia pneumoniae infection of the central nervous system in multiple sclerosis”, Ann. Neurol., Vol. 46, (1999), pp. 6–14. Google Scholar

  • [27] E. Maida: “Immunological reactions against Mycoplasma pneumoniae in multiple sclerosis: preliminary findings”, J. Neurol., Vol. 229, (1983), pp. 103–111. CrossrefGoogle Scholar

  • [28] D.A. Dyment, G.C. Ebers and A.D. Sadovnick: “Genetics of multiple sclerosis”, Lancet Neurol., Vol. 3, (2004), pp. 104–110. CrossrefGoogle Scholar

  • [29] J.L. Haines, Y. Bradford, M.E. Garcia and A.D. Reed, E. Neumeister: “Multiple susceptibility loci for multiple sclerosis”, Hum. Mol. Genet., Vol. 11, (2002), pp. 2251–2256. Google Scholar

  • [30] U. Christen, D. Benke, T. Wolfe, E. Rodrigo, A. Rhode, A.C. Hughes and M.B. Oldstone: “Cure of prediabetic mice by viral infections involves lymphocyte recruitment along an IP-10 gradient”, J. Clin. Invest., Vol. 113, (2004), pp. 74–84. CrossrefGoogle Scholar

  • [31] U. Christen and M.G. Von Herrath: “Infections and autoimmunity — good or bad?”, J. Immunol., Vol. 174, (2005), pp. 7481–7486. CrossrefGoogle Scholar

  • [32] P.D. Katsikis, S.B. Cohen, M. Londei and M. Feldman: “Are CD4+ Th1 cells proin-flammatory or anti-inflammatory? The ratio of IL-10 to INF-gamma or IL-2 determines their function”, Int. Immunol., Vol. 7, (1995), pp. 1287–1294. Google Scholar

  • [33] P.B. Carrieri, V. Provitera, T. De Rosa, G. Tartaglia, F. Gorga and O. Perrella: “Profile of cerebrospinal fluid and serum cytokines in patients with relapsing-remitting multiple sclerosis: a correlation with clinical of IRS activation, such as T cell activation increased activity”, Immunopharmacol. Immunotoxicol., Vol. 20, (1998), pp. 373–382. http://dx.doi.org/10.3109/08923979809034820CrossrefGoogle Scholar

  • [34] P. Hautecoeur, G. Forzy, P. Gallois, V. Demirbilek and O. Feugas: “Variations of IL2, IL6, TNF alpha plasmatic levels in relapsing remitting multiple sclerosis”, Acta Neurol. Belg., Vol. 97, (1997), pp. 240–243. Google Scholar

  • [35] O. Mikova, R. Yakimova, E. Bosmans, G. Kenis and M. Maes: “Increased serum tumor necrosis factor alpha concentrations in major depression and multiple sclerosis”, Eur. Neuropsychopharmacol., Vol. 11, (2001), pp. 203–208. CrossrefGoogle Scholar

  • [36] R.L. Wilder: “Neuroendocrine-immune system interactions and autoimmunity”, Annu. Rev. Immunol., Vol. 13. (1995), pp. 307–338. CrossrefGoogle Scholar

  • [37] J.W. Karaszewski, A.T. Reder, R. Maselli, M. Brown and B.G. Arnason: “Sympathetic skin responses are decreased and lymphocyte beta-adrenergic receptors are increased in progressive multiple sclerosis”, Ann. Neurol., Vol. 27, (1990), pp. 366–372. Google Scholar

  • [38] E. Chelmicka-Schorr, M.N. Kwasniewski, B.E. Thomas and B.G. Arnason: “The beta-adrenergic agonist isoproterenol suppresses experimental allergic encephalomyelitis in Lewis rats”, J. Neuroimmunol., Vol. 25, (1989), pp. 203–207. CrossrefGoogle Scholar

  • [39] K. Wiegmann, S. Muthyala, D.H. Kim, B.G. Arnason and E. Chelmicka-Schorr: “Beta-adrenergic agonists suppress chronic/relapsing experimental allergic encephalomyelitis (CREAE) in Lewis rats”, J. Neuroimmunol., Vol. 56, (1995), pp. 201–206. CrossrefGoogle Scholar

  • [40] S.E. Ross, R.O. Williams, L.J. Mason, C. Mauri, L. Marinova-Mutafchieva, A.M. Malfait, R.N. Maini and M. Feldmann: “Suppression of TNF-alpha expression, inhibition of Th1 activity, and amelioration of collagen-induced arthritis by rolipram”, J. Immunol., Vol. 159, (1997), pp. 6253–6259. Google Scholar

  • [41] L. Liang, E. Beshay and G.J. Prud’homme: “The phosphodiesterase inhibitors pentoxifylline and rolipram prevent diabetes in NOD mice”, Diabetes, Vol. 47, (1998), pp. 570–575. CrossrefGoogle Scholar

  • [42] W.B. Essmann: “Serotonin distribution in tissue and fluids”, In: W.B. Essmann (Ed.): Serotonin in health and disease, Vol. 1, Spectrum, New York. Google Scholar

  • [43] T.M. Aune, K.M. McGrath, T. Sarr, Bombara and K.A. Kelley: “Expression of 5HT1a receptors on activated human T cells”, J. Immunol., Vol. 151, (1993), pp. 1175–1183. Google Scholar

  • [44] M.R.I. Young, J.L. Kut, M.P. Coogan, M.A. Wright, M.E. Young and J. Matthews: “Stimulation of splenic T-lymphocyte function by endgenuous serotonin and by low-dose exogenous serotonin”, Immunology, Vol. 80, (1993), pp. 395–400. Google Scholar

  • [45] M.R.I. Young and J.P. Matthews: “Serotonin regulation of T-cell subpopulations and of macro-phage accessory function”, Immunology, Vol. 84, (1995), pp. 148–152. Google Scholar

  • [46] M. Freire-Garabal, M.J. Nunez, J. Balboa, P. Lopez-Delgado, R. Gallego, T. Garcia-Caballero, M.D. Fernandez-Roel, J. Brenlla and M. Rey-Mendez: “Serotonin upregulates the activity of phagocytosis through 5-HT1A receptors”, Br. J. Pharmacol., Vol. 139, (2003), pp. 457–463. Google Scholar

  • [47] T.M. Aune, H.W. Golden and K.M. McGrath: “Inhibitors of serotonin synthesis and antagonists of serotonin 1A receptors inhibit T lymphocyte function in vitro and cell-mediated immunity in vivo”, J. Immunol., Vol. 153, (1994), pp. 489–498. Google Scholar

  • [48] D. Davidson, I.A. Pullar, C. Mawdsley, N. Kinloch and C.M. Yates: “Monoamine metabolites in cerebrospinal fluid in multiple sclerosis”, J. Neurol. Neurosur. Psychiatry, Vol. 40, (1977), pp. 741–745. CrossrefGoogle Scholar

  • [49] B. Johansson and B.E. Ross: “5-hydroxyindoleacetic acid and homovanillic acid in CSF of patients with neurological disease”, Eur. Neurol., Vol. 11, (1977), pp. 37–45. Google Scholar

  • [50] V. Sonnien, P. Riekkinen and U.K. Rinne: “Acid monoamine metabolites in cerebrospinal fluid in multiple sclerosis”, Neurology, Vol. 23, (1973), pp. 760–763. CrossrefGoogle Scholar

  • [51] J.E. Blalock: “The syntax of immune-neuroendocrine communication”, Immunol. Today, Vol. 15, (1994), pp. 504–511. Google Scholar

  • [52] W. Savino, E. Arzt and M. Dardenne: “Immunoneuroendocrine connectivity: the paradigm of the thymus-hypothalamus-pituitary axis”, Neuroimmunomodulation, Vol. 6, (1999), pp. 126–136. CrossrefGoogle Scholar

  • [53] O.J.G. Schiepers, M.C. Wichers and M. Maes: “Cytokines and major depression”, Prog. Neuro-Psychopharmacol. Biol. Psychiatry, Vol. 29, (2005), pp. 201–217. Google Scholar

  • [54] M. Maes, R. Verkerk, S. Bonaccorso, W. Ombelet, E. Bosmans and S. Scharpe: “Depressive and anxiety symptoms in the early puerperium are related to increased degradation of tryptophan into kynurenine, a phenomenon which is related to immune activation”, Life Sci., Vol. 71, (2002), pp. 1837–1848. CrossrefGoogle Scholar

  • [55] M. Wichers and M. Maes: “The role of indoleamine 2,3 dioxygenase (IDO) in the pathophysiology of interferon-alpha-induced depression”, J. Psychiatry. Neurosci., Vol. 29, (2004), pp. 11–17. Google Scholar

  • [56] A. Mangoni: “The kynurenine shunt and depression”, Adv. Biochem. Psychopharmacol., Vol. 11, (1974), pp. 293–298. Google Scholar

  • [57] J.J.A. Hendriks, C.E. Teunissen, H.E. de Vries and C.D. Dijkstra: “Macrophages and neurodegeneration”, Brain Res. Rev., Vol. 48, (2005), pp. 185–195. CrossrefGoogle Scholar

  • [58] M. Salter and C.I. Pogson: “The role of tryptophan 2,3-dioxygenase in the hormonal control of tryptophan metabolism in isolated rat liver cells. Effects of glucocorticoids and experimental diabetes”, Biochem. J., Vol. 229, (1985), pp. 499–504. Google Scholar

  • [59] J.M. Loftis and P. Hauser: “The phenomenology and treatment of interferon-induced depression”, J. Affect. Disord., Vol. 82, (2004), pp. 175–90. CrossrefGoogle Scholar

  • [60] A. Amirkhani, C. Rajda, B. Arvidsson, K. Bencsik, K. Boda, E. Seres, K.E. Markides, L. Vecsei and J. Bergquist: “Interferon-beta affects the tryptophan metabolism in multiple sclerosis patients”, Eur. J. Neurol., Vol. 12, (2005), pp. 625–631. CrossrefGoogle Scholar

  • [61] Z. Hartai, P. Klivenyi, T. Janaky, B. Penke, L. Dux and L. Vecsei: “Kynurenine metabolism in multiple sclerosis”, Acta Neurol. Scand., Vol. 112, (2005), pp. 93–96. CrossrefGoogle Scholar

  • [62] E. Kwidzinski, J. Bunse, O. Aktas, D. Richter, L. Mutlu, F. Zipp, R. Nitsch and I. Bechmann: “Indolamine 2,3-dioxygenase is expressed in the CNS and down-regulates autoimmune inflammation”, FASEB J., Vol. 19, (2005), pp. 1347–1349. Google Scholar

  • [63] F.E. Bloom, J. Rossier, E.L.F. Battenberg, A. Bayon, E. French, S.J. Hendriksen, G.R. Siggins, D. Segal, R. Browne, N. Ling and R. Guillemin: “Beta endorphin: cellular localization, electrophysiological and behavioral effects”, Adv. Biochem. Psychopharmacol., Vol. 18, (1978), pp. 89–109. Google Scholar

  • [64] L.G. Roda, L. Bongiorno, E. Trani, A. Urbani and M. Marini: “Positive and negative immunomodulation by opioid peptides”, Int. J. Immunopharmacol., Vol. 18, (1996), pp. 1–16. CrossrefGoogle Scholar

  • [65] A. Kavelaars, R.E. Ballieux and C.J. Heijnen: Differential effects of beta-endorphin on cAMP levels in human peripheral blood mononuclear cells”, Brain Behav. Immun., Vol. 4, (1990), pp. 171–179. CrossrefGoogle Scholar

  • [66] R. Przewlocki, A.H. Hassan, W. Lason, C. Epplen, A. Herz, C. Stein: “Gene expression and localization of opioid peptides in immune cells of inflamed tissue: functional role in antinociception”, Neuroscience, Vol. 48, (1992), pp. 491–500. CrossrefGoogle Scholar

  • [67] J.E. Blalock: “A molecular basis for bidirectional communication between the immune and neuroendocrine systems”, Physiol. Rev., Vol. 69, (1989), pp. 1–32. Google Scholar

  • [68] M. Gironi, V. Martinelli and E. Brambilla: “Beta-endorphin concentrations in peripheral blood mononuclear cells of patients with multiple sclerosis”, Arch. Neurol., Vol. 57, (2000), pp. 1178–1181. CrossrefGoogle Scholar

  • [69] M. Gironi, R. Furlan, M. Rovaris, G. Comi, M. Filippi, A.E. Panerai and P. Sacerdote: “ß endorphin concentrations in PBMC of patients with different clinical phenotypes of multiple sclerosis”, J. Neurol. Neurosurg. Psychiatry, Vol. 74, (2003), pp. 495–497. CrossrefGoogle Scholar

  • [70] P. Sacerdote, B. Manfredi and L. Gaspani: “The opioid antagonist naloxone induces a shift from type 2 to type 1 cytokine pattern in BALB/cJ mice”, Blood, Vol. 95, (2000), pp. 2031–2036. Google Scholar

  • [71] J. Hosoi, H. Ozawa, R.D. Granstein: “Beta-endorphin binding and regulation of cytokine expression in Langerhans cells”, Ann. N.Y. Acad. Sci., Vol. 885, (1999), pp. 405–413. http://dx.doi.org/10.1111/j.1749-6632.1999.tb08700.xCrossrefGoogle Scholar

  • [72] D.R. Smith, K.E. Balashov, D.A. Hafler, S.J. Khoury and H.I. Weiner: “Immune deviation following pulse cyclophosphamide/methylprednisolone treatment of multiple sclerosis: increased interleukin-4 production and associated eosinophilia”, Ann. Neurol., Vol. 42, (1997), pp. 313–318. Google Scholar

  • [73] H.C. Nousari, A.K. Asadi and F.A. Tausk: “Subacute cutaneous lupus erythomatosus associated with interferon beta 1a”, Lancet, Vol. 352, (1998), pp. 1825–1826. Google Scholar

  • [74] Y. Kreiss, O. Cohen, E. Pras and A. Achiron: “Subacute thyroiditis in a patient with multiple sclerosis treated with interferon beta 1a”, Neurology, Vol. 53, (1999), pp. 1606–1611. Google Scholar

  • [75] M. Rotondi, G. Mazziotti, B. Biondi, G. Mangallena, A.D. Del Buono and P. Montella: “Long term treatment with interferon beta therapy for multiple sclerosis and occurrence of graves disease”, J. Endocrinol. Invest., Vol. 23, (2000), pp. 321–324. CrossrefGoogle Scholar

  • [76] J.L. Goeb, C. Even, G. Nicolas, B. Gohier, F. Dubas and J.B. Garre: “Psychiatric side effects of interferon-beta in multiple sclerosis”, Eur. Psychiatry, Vol. 21, (2006), pp. 186–193. CrossrefGoogle Scholar

  • [77] W. Haymaker: Bing’s local diagnosis in neurological diseases, The C.V. Mosby Company, Saint Louis, 1969. Google Scholar

  • [78] R. Sandyk: “Demyelination as an epiphenomenon in multiple sclerosis”, Int. J. Neurosci., Vol. 72, (1993), pp. 141–148. Google Scholar

  • [79] D.S. Russel: “Trauma and multiple sclerosis”, Lancet, Vol. 1, (1964), p. 978. CrossrefGoogle Scholar

  • [80] N.R. Ghatak, A. Hirano, H. Lijtmaer and H.M. Zimmerman: “Asymptomatic demyelinated plaque in the spinal cord”, Arch. Neurol., Vol. 30, (1974), pp. 484–486. CrossrefGoogle Scholar

  • [81] J.G. Phadke and P.V. Best: “A typical and clinically silent multiple sclerosis: a report of 12 cases discovered unexpectedly at necropsy”, J. Neurol. Neurosurg. Psychiatry, Vol. 46, (1983), pp. 414–420. http://dx.doi.org/10.1136/jnnp.46.5.414CrossrefGoogle Scholar

  • [82] S.G. Lynch, J.W. Rose, W. Smoker and J.H. Petajan: “MRL in familial multiple sclerosis”, Neurology, Vol. 40, (1990), pp. 900–903. CrossrefGoogle Scholar

  • [83] A.L. Traboulsee and D.K. Li: “The role of MRI in the diagnosis of multiple sclerosis”, Adv. Neurol., Vol. 98, (2006), pp. 125–146. Google Scholar

  • [84] A. Theodoridou and L. Settas: “Demyelination in rheumatic diseases”, J. Neurol. Neurosurg. Psychiatry, Vol. 77, (2006), pp. 290–295. Google Scholar

  • [85] A. Geissler, T. Andus and M. Roth: “Focal white-matter lesions in brain of patients with inflammatory bowel disease”, Lancet, Vol. 345, (1995), pp. 897–898. Google Scholar

  • [86] P. Whiting, R. Harbord, C. Main, J.J. Deeks, G. Filippini, M. Egger and J.A.C. Sterne: “Accuracy of magnetic resonance imaging for the diagnosis of multiple sclerosis: systematic review”, Br. Med. J., Vol. 332, (2006), pp. 875–884. CrossrefGoogle Scholar

  • [87] M.T. Hyyppa, T. Jolma, P. Riekkinen and U.K. Rinne: “Effects of L-tryptophan on central indoleamine metabolism and short-lasting neurologic disturbances in multiple sclerosis”, J. Neural. Transm., Vol. 37, (1975), pp. 297–304. CrossrefGoogle Scholar

  • [88] R.T. Joffe: “Depression and multiple sclerosis: a potential way to understand the biology of major depressive illness”, J. Psychiatry Neurosci., Vol. 30, (2005), pp. 9–10. Google Scholar

  • [89] D.C. Mohr, D.E. Goodkin, J. Islar, L. Hauser and C.P. Genain: “Treatment of depression is associated with suppression of nonspecific and antigen-specific Th1 responses in multiple sclerosis”, Arch. Neurol., Vol. 58, (2001), pp. 1081–1086. CrossrefGoogle Scholar

  • [90] D.C. Mohr, L. Stacey, A. Hart and A. Golberg: “Effects of treatment for depression on fatigue in multiple sclerosis”, Psychosom. Med., Vol. 65, (2003), pp. 542–547. Google Scholar

  • [91] S. Hart, I. Fonareva, N. Merluzzi and D.C. Mohr: “Treatment for depression and its relationship to improvement in quality of life and psychological well-being in multiple sclerosis patients”, Qual. Life Res., Vol. 14, (2005), pp. 695–703. CrossrefGoogle Scholar

  • [92] A.C. Jung, T. Staiger and M. Sullivan: “The efficacy of selective serotonin reuptake inhibitors for the management of chronic pain”, J. Gen. Intern. Med., Vol. 12, (1997), pp. 384–389. CrossrefGoogle Scholar

  • [93] E.N. Duman, M. Kesim, M. Kadioglu, E. Yaris, N.I. Kalyoncu and N. Erciyes: “Possible involvement of opioidergic and serotonergic mechanisms in antinociceptive effect of paroxetine in acute pain”, J. Pharmacol. Sci., Vol. 94, (2004), pp. 161–165. CrossrefGoogle Scholar

  • [94] M. Kesim, E.N. Duman, M. Kadioglu, E. Yaris, N.I. Kalyoncu, N. Erciyes: “The different roles of 5-HT(2) and 5-HT(3) receptors on antinociceptive effect of paroxetine in chemical stimuli in mice”, J. Pharmacol. Sci., Vol. 97, (2005), pp. 61–66. CrossrefGoogle Scholar

  • [95] F. Lechin, B. van der Dijs and M.E. Lechin (Ed.): Neurocircuitry and Neuroautonomic Disorders: Reviews and Therapeutic Strategies, Karger, Basel, 2002. Google Scholar

  • [96] F. Lechin, B. van der Dijs and A.E. Lechin: “Treatment of bronchial asthma with tianeptine”, Methods Find. Exp. Clin. Pharmacol., Vol. 26, (2004), pp. 697–701. CrossrefGoogle Scholar

  • [97] F. Lechin, B. van der Dijs, B. Orozco, E. Jahn, S. Rodriguez and S. Baez: “Neuropharmacological treatment of refractory idiopathic thrombocytopenic purpura: roles of circulating catecholamines and serotonin”, Thromb. Haemost., Vol. 91, (2004), pp. 1254–1256. Google Scholar

  • [98] F. Lechin and B. van der Dijs: “Neuropharmacological therapy of carcinoid syndrome”, Neuroendocrinology, Vol. 81, (2005), pp. 137–138. CrossrefGoogle Scholar

  • [99] F. Lechin, B. van der Dijs, B. Orozco, G. Hernandez-Adrian, S. Rodriguez and S. Baez: “Similar autonomic nervous system disorders underlying cystic fibrosis and pancreatic cysts allowed common neuropharmacological therapy: Report of four cases”, J. Appl. Res., Vol. 5, (2005b), pp. 299–304. Google Scholar

  • [100] F. Lechin, B. van der Dijs, B. Orozco, S. Rodriguez and S. Baez: “Neuropharmacological therapy of polycythemia vera: roles of circulating catecholamines and serotonin”, Thromb. Hemost., Vol. 93, (2005), pp. 175–177. Google Scholar

  • [101] T.C. Birdsall: “5-Hydroxytryptophan: a clinically-effective serotonin precursor”, Altern. Med. Rev., Vol. 3, (1998), pp. 271–280. Google Scholar

  • [102] E.H. Turner and A.D. Blackwell: “5-Hydroxytryptophan plus SSRIs for interferoninduced depression: Synergistic mechanisms for normalizing synaptic serotonin”, Med. Hypoth., Vol. 65, (2005), pp. 138–144. CrossrefGoogle Scholar

  • [103] E.H. Turner, J.M. Loftis and A.D. Blackwell: “Serotonin a la carte: Supplementation with the serotonin precursor 5-hydroxytryptophan”, Pharmacol. Ther., Vol. 109, (2005), pp. 325–338. Google Scholar

  • [104] M. Kubera, A. Lin, G. Kenis, E. Bosmans, D. van Bockstaele and M. Maes: “Anti-inflammatory effects of antidepressants through suppression of the interferongamma/interleukin-10 production ratio”, J. Clin. Psychopharmacol., Vol. 21, (2001), pp. 199–206. CrossrefGoogle Scholar

  • [105] M. Kubera, G. Kenis, E. Bosmans, S. Scharpe and M. Maes: “Effects of serotonin and serotonergic agonists and antagonists on the production of interferon-g and interleukin-10”, Neuropsychopharmacology, Vol. 23, (2000), pp. 89–98. CrossrefGoogle Scholar

  • [106] M. Maes, C. Song, A.-H. Lin, S. Bonaccorso and G. Kenis: “Negative immunoregulatory effects of antidepressants: inhibition of interferon-g and stimulation of interleukin-10 secretion”, Neuropsychopharmacology, Vol. 20, (1999), pp. 370–379. Google Scholar

  • [107] M. Maes: “The immunoregulatory effects of antidepressants”, Hum. Psychopharmacol., Vol. 16, (2001), pp. 95–103. CrossrefGoogle Scholar

  • [108] M. Maes, G. Kenis and M. Kubera: “The negative immunoregulatory effects of fluoxetine in relation to the camp-dependent PKA pathway”, Int. Immunopharmacol., Vol. 5, (2005), pp. 609–618. CrossrefGoogle Scholar

  • [109] H. Iwata, H. Okamoto and S. Ko: “Effects of various drugs on serum free and total tryptophan levels and brain tryptophan metabolism in rats”, Jpn. J. Pharmacol., Vol. 25, (1975), pp. 303–310. Google Scholar

  • [110] A.A. Badawy: “Mechanisms of elevation of rat brain tryptophan concentration by various doses of salicylate”, Br. J. Pharmacol., Vol. 76, (1982), pp. 211–213. Google Scholar

  • [111] A. Groppetti, P.C. Braga, G. Biella, M. Parenti, L. Rusconi and P. Mantegazza: “Effect of aspirin on serotonin and metenkephalin in brain: correlation with the antinociceptive activity of the drug”, Neuropharmacology, Vol. 27, (1988), pp. 499–505. CrossrefGoogle Scholar

  • [112] M. Sandrini, G. Vitale and L.A. Pini: “Central antinociceptive activity of acetylsalicylic acid is modulated by brain serotonin receptor subtypes”, Pharmacology, Vol. 65, (2002), pp. 193–197. CrossrefGoogle Scholar

  • [113] K. Schroecksnadel, C. Winkler, B. Wirleitner, H. Schennach and D. Fuchs: “Aspirin down-regulates tryptophan degradation in stimulated human peripheral blood mononuclear cells in vitro”, Clin. Exp. Immunol., Vol. 140, (2005), pp. 41–45. CrossrefGoogle Scholar

  • [114] D. Martinez, A. Broft and M. Laruelle: “Pindolol augmentation of antidepressant treatment: recent contributions from brain imaging studies”, Biol. Psychiatry, Vol. 48, (2000), pp. 844–853. CrossrefGoogle Scholar

  • [115] E.B. Perry, R.M. Berman, G. Sanacora, A. Anand, K. Lynch-Colonese and D.S. Charney: “Pindolol augmentation in depressed patients resistant to selective serotonin reuptake inhibitors: a double-blind, randomized, controlled trial”, J. Clin. Psychiatry, Vol. 65, (2004), pp. 238–243. http://dx.doi.org/10.4088/JCP.v65n0215CrossrefGoogle Scholar

  • [116] C.F. Scott Jr, N. Cashman and L.E. Spitler: “Experimental allergic encephalitis; treatment with drugs which alter CNS serotonin levels”, J. Immunopharmacol., Vol. 4, (1982-83), pp. 153–162. CrossrefGoogle Scholar

  • [117] M. Freire-Garabal, M.J. Nunez, J. Balboa, L.A. Garci, S. Argibay, E. Rodrigo and M. Rey-Mendez: “Administration of the 5-hydroxytryptamine(1A) receptor antagonist WAY100635 suppresses acute experimental allergic encephalomyelitis in Lewis rats”, Neurosci. Lett., Vol. 342, (2003), pp. 33–36. Google Scholar

  • [118] H.H. Hofstetter, R. Mossner, K.P. Lesch, R.A. Linker, K.V. Toyka and R. Gold: “Absence of reuptake of serotonin influences susceptibility to clinical autoimmune disease and neuroantigen-specific interferon-gamma production in mouse EAE”, Clin. Exp. Immunol., Vol. 142, (2005), pp. 39–44. CrossrefGoogle Scholar

  • [119] F. Lechin, B. van der Dijs, G. Hernandez-Adrian: “Dorsal raphe vs. median raphe serotonergic antagonism. Anatomical, physiological, behavioral, neuroendocrinological, neuropharmacological and clinical evidences: Relevance for neuropharmacological therapy”, Prog. Neuropsychopharmacol. Biol. Psychiatry, Vol. 30, (2006), pp. 565–585. CrossrefGoogle Scholar

  • [120] S.S. Mosko and B.L. Jacobs: “Midbrain raphe neurons: sensitivity to glucocorticoids and ACTH in the rat”, Brain Res., Vol. (89), (1975), pp. 368–375. Google Scholar

  • [121] G. Bagdy, A.E. Calogero, K. Szemeredi, M.T. Gomez, D.L. Murphy and G.P. Chrousos: “Beta-endorphin responses to different serotonin agonists: involvement of corticotropin-releasing hormone, vasopresin, and direct pituitary action”, Brain Res., Vol. 537, (1990), pp. 227–232. Google Scholar

  • [122] N. Laaris, E. Le Poul, M. Hamon and L. Lanfumey: “Stress-induced alterations of somatodendritic 5-HT1A autoreceptor sensitivity in the rat dorsal raphe nucleus — in vitro electrophysiological evidence”, Fundam. Clin. Pharmacol., Vol. 11, (1997), pp. 206–214. http://dx.doi.org/10.1111/j.1472-8206.1997.tb00187.xCrossrefGoogle Scholar

  • [123] I. Huitinga, Z.A. Erkut, D. van Beurden and D.F. Swaab: “Impaired hypothalamuspituitary-adrenal axis activity and more severe multiple sclerosis with hypothalamic lesions”, Ann. Neurol., Vol. 55, (2004), pp. 37–45. Google Scholar

  • [124] S.E. Drewes, J. George and F. Khan: “Recent findings on natural products with erectile-dysfunction activity”, Phytochemistry, Vol. 62, (2003), pp. 1019–1025. CrossrefGoogle Scholar

  • [125] A.T. Guay, R.F. Spark and J. Jacobson: “Yohimbine treatment of organic erectile dysfunction in a dose-escalation trial”, Int. J. Impot. Res., Vol. 14, (2002), pp. 25–31. CrossrefGoogle Scholar

  • [126] J.M. Baraban and G.K. Aghajanian: “Noradrenergic innervation of serotonergic neurons in the dorsal raphe: demonstration by electron microscopic autoradiography”, Brain Res., Vol. 204, (1981), pp. 1–11. CrossrefGoogle Scholar

  • [127] L. Ferraro, K. Fuxe, S. Tanganelli, M. Fernandez, F.A. Rambert and T. Antonelli: “Amplification of cortical serotonin release: a further neurochemical action of the vigilance-promoting drug modafinil”, Neuropharmacology, Vol. 39, (2000), pp. 1974–1983. CrossrefGoogle Scholar

  • [128] S Caccia: “Metabolism of the newer antidepressants. An overview of the pharmacological and pharmacokinetic implications”, Clin. Pharmacokinet. Vol. 34, (1998), pp. 281–302. CrossrefGoogle Scholar

  • [129] B.S. McEwen and S. Chattarji: “Molecular mechanisms of neuroplasticity and pharmacological implications: the example of tianeptine”, Eur. Neuropsychopharmacol., Vol. 14 (Suppl 5), (2004), pp. S497–502. CrossrefGoogle Scholar

  • [130] W. Binder, S.A. Mousa, N. Sitte, M. Kaiser, C. Stein and M. Schafer: “Sympathetic activation triggers endogenous opioid release and analgesia within peripheral inflamed tissue”, Eur. J. Neurosci., Vol. 20, (2004), pp. 92–100. CrossrefGoogle Scholar

  • [131] G.M. Rose, A. Hopper, M. De Vivo and A. Tehim: “Phosphodiesterase inhibitors for cognitive enhancement”, Curr. Pharm. Des., Vol. 11, (2005), pp. 3329–3334. Google Scholar

  • [132] D. Djurovic, J. Milic-Askrabic and N. Majkic-Singh: “Serum beta-endorphin level in patients with depression on fluvoxamine”, Farmaco, Vol. 54, (1999), pp. 130–113. CrossrefGoogle Scholar

  • [133] A. Zangen, R. Nakash and G. Yadid: “Serotonin-mediated increases in the extracellular levels of beta-endorphin in the arcuate nucleus and nucleus accumbens: a microdialysis study”, J. Neurochem., Vol. 73, (1999), pp. 2569–2574. Google Scholar

  • [134] R. Jadric, I. Zulic, S. Hasic, E. Kiseljakovic, B. Zecevic, J. Radovanovic, E. Icindic-Nakas, M. Winterhalter-Jadric: “Trazodone influence on rat sera beta-endorphins level”, Bosn. J. Basic. Med. Sci., Vol. 4, (2004), pp. 33–36. Google Scholar

  • [135] A. Zangen, R. Nakash, I. Roth-Deri, D.H. Overstreet and G. Yadid: “Impaired release of beta-endorphin in response to serotonin in a rat model of depression”, Neuroscience, Vol. 110, (2002), pp. 389–393. CrossrefGoogle Scholar

  • [136] G. Moalem and D.J. Tracey: “Immune and inflammatory mechanisms in neuropathic pain”, Brain Res. Brain Res. Rev., Vol. 51, (2006), pp. 240–264. CrossrefGoogle Scholar

  • [137] W. Puehler and C. Stein: “Controlling pain by influencing neurogenic pathways”, Rheum. Dis. Clin. North. Am., Vol. 31, (2005), pp. 103–113. CrossrefGoogle Scholar

  • [138] Y.P. Agrawal: “Low dose naltrexone therapy in multiple sclerosis”, Med. Hypotheses, Vol. 64, (2005), pp. 721–724. CrossrefGoogle Scholar

  • [139] M. Dokur, C.P. Chen, J.P. Advis and D.K. Sarkar: “Beta-endorphin modulation of interferon-gamma, perforin and granzyme B levels in splenic NK cells: effects of ethanol”, J. Neuroimmunol., Vol. 166, (2005), pp. 29–38. CrossrefGoogle Scholar

  • [140] P. Lissoni, F. Malugani and O. Malysheva: “Neuroimmunotherapy of untreatable metastatic solid tumors with subcutaneous low-dose interleukin-2, melatonin and naltrexone: modulation of interleukin-2-induced antitumor immunity by blocking the opioid system”, Neuro. Endocrinol. Lett., Vol. 23, (2002), pp. 341–344. Google Scholar

  • [141] I.S. Zagon and P.J. McLaughlin: “Opioids and the apoptotic pathway in human cancer cells”, Neuropeptides, Vol. 37, (2003), pp. 79–88. CrossrefGoogle Scholar

  • [142] I.S. Zagon and P.J. McLaughlin: “Opioids and differentiation in human cancer cells”, Neuropeptides, Vol. 39, (2005), pp. 495–505. CrossrefGoogle Scholar

  • [143] B.M. Berkson, D.M. Rubin and A.J. Berkson: “The long-term survival of a patient with pancreatic cancer with metastases to the liver after treatment with the intravenous α-lipoic acid/low-dose naltrexone protocol”, Integr. Cancer. Ther., Vol. 5, (2006), pp. 83–89. Google Scholar

  • [144] K. Makhlouf, M. Comabella and J. Imitola: “Oral salbutamol decreases IL-12 in patients with secondary progressive multiple sclerosis”, J. Neuroimmunol., Vol. 117, (2001), pp. 156–165. CrossrefGoogle Scholar

  • [145] K. Makhlouf, H.L. Weiner and S.J. Khoury: “Potential of b2-adrenoceptor agonists as add-on therapy for multiple sclerosis: focus on salbutamol (albuterol)”, CNS Drugs, Vol. 16, (2002), pp. 1–8. Google Scholar

  • [146] G. Ristori, M.G. Buzzi and U. Sabatini: “Use of Bacille Calmette-Guerin (BCG) in multiple sclerosis”, Neurology, Vol. 53, (1999), pp. 1588–1589. CrossrefGoogle Scholar

  • [147] R.K. Davis and A.S. Maslow: “Multiple sclerosis in pregnancy: a review”, Obstet. Gynecol. Surv., Vol. 47, (1992), pp. 290–296. CrossrefGoogle Scholar

  • [148] S. Sanchez-Ramon, A.J. Navarro and C. Aristimuno: “Pregnancy-induced expansion of regulatory T-lymphocytes may mediate protection to multiple sclerosis activity”, Immunol. Lett., Vol. 96, (2005), pp. 195–201. Google Scholar

  • [149] M. Minagawa, J. Narita, T. Tada, S. Maruyama, T. Shimizu, M. Bannai, H. Oya, K. Hatakeyama and T. Abo: “Mechanisms underlying immunologic states during pregnancy: possible association of the sympathetic nervous system”, Cell. Immunol., Vol. 196, (1999), pp. 1–13. CrossrefGoogle Scholar

About the article

Published Online: 2006-09-26

Published in Print: 2006-12-01


Citation Information: Open Medicine, Volume 1, Issue 4, Pages 313–329, ISSN (Online) 2391-5463, DOI: https://doi.org/10.2478/s11536-006-0031-x.

Export Citation

© 2006 Versita Warsaw. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Comments (0)

Please log in or register to comment.
Log in