Chemical destruction of brain noradrenergic neurons affects splenic cytokine production

Journal of Neuroimmunology

Volumn 219, Issue 1-2, 2010, Pages 75-80

  Engler, Harald ^a,b   Doenlen, Raphael ^a   Riether, Carsten ^a   Engler, Andrea ^a   Besedovsky, Hugo O ^c   del Rey, Adriana ^c   Pacheco López, Gustavo ^a   Schedlowski, Manfred ^a,b  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b ETH ZURICH   (Switzerland)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Brainstem; Cytokine; DSP 4; Locus coeruleus; Noradrenaline; Spleen

Indexed keywords

2 BROMO N (2 CHLOROETHYL) N ETHYLBENZYLAMINE; CD3 ANTIBODY; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY MASS; CELL SUBPOPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; LEUKOCYTE; LOCUS CERULEUS; MACROPHAGE; MALE; MONOCYTE; NATURAL KILLER CELL; NONHUMAN; NORADRENERGIC NERVE; PRIORITY JOURNAL; RAT; SPLEEN CELL; T LYMPHOCYTE;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD3; BENZYLAMINES; BODY MASS INDEX; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOKINES; ELECTROCHEMISTRY; LEUKOCYTES; LIPOPOLYSACCHARIDES; MALE; NEURONS; NEUROTOXINS; NOREPINEPHRINE; RATS; RATS, INBRED F344; SPLEEN; TYROSINE 3-MONOOXYGENASE;

EID: 77249152138     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2009.12.001     Document Type: Article

References (59)

1. Archer T., Ogren S.O., Johansson G., Ross S.B. DSP4-induced two-way active avoidance impairment in rats: involvement of central and not peripheral noradrenaline depletion. Psychopharmacology (Berl) 1982, 76:303-309.
2. Arima K., Akashi T. Involvement of the locus coeruleus in Pick's disease with or without Pick body formation. Acta Neuropathol. 1990, 79:629-633.
3. Bellinger D.L., Stevens S.Y., Thyaga Rajan S., Lorton D., Madden K.S. Aging and sympathetic modulation of immune function in Fischer 344 rats: effects of chemical sympathectomy on primary antibody response. J. Neuroimmunol. 2005, 165:21-32.
4. Benarroch E., Schmeichel A., Low P., Sandroni P., Parisi J. Loss of A5 noradrenergic neurons in multiple system atrophy. Acta Neuropathol. 2008, 115:629-634.
5. Benschop R.J., Jacobs R., Sommer B., Schurmeyer T.H., Raab J.R., Schmidt R.E., Schedlowski M. Modulation of the immunologic response to acute stress in humans by beta-blockade or benzodiazepines. Faseb J. 1996, 10:517-524.
6. Besedovsky H.O., del Rey A. Immune-neuro-endocrine interactions: facts and hypotheses. Endocr. Rev. 1996, 17:64-102.
7. Besedovsky H.O., del Rey A., Sorkin E., Da Prada M., Keller H.H. Immunoregulation mediated by the sympathetic nervous system. Cell. Immunol. 1979, 48:346-355.
8. Buijs R.M., van der Vliet J., Garidou M.L., Huitinga I., Escobar C. Spleen vagal denervation inhibits the production of antibodies to circulating antigens. PLoS ONE 2008, 3:e3152.
9. Callahan T.A., Moynihan J.A. Contrasting pattern of cytokines in antigen- versus mitogen-stimulated splenocyte cultures from chemically denervated mice. Brain Behav. Immun. 2002, 16:764-773.
10. Cano G., Sved A.F., Rinaman L., Rabin B.S., Card J.P. Characterization of the central nervous system innervation of the rat spleen using viral transneuronal tracing. J. Comp. Neurol. 2001, 439:1-18.
11. Chan-Palay V., Asan E. Alterations in catecholamine neurons of the locus coeruleus in senile dementia of the Alzheimer type and in Parkinson's disease with and without dementia and depression. J. Comp. Neurol. 1989, 287:373-392.
12. Chrobak J.J., DeHaven D.L., Walsh T.J. Depletion of brain norepinephrine with DSP-4 does not alter acquisition or performance of a radial-arm maze task. Behav. Neural. Biol. 1985, 44:144-150.
13. Cross R.J., Roszman T.L. Central catecholamine depletion impairs in vivo immunity but not in vitro lymphocyte activation. J. Neuroimmunol. 1988, 19:33-45.
14. Cross R.J., Jackson J.C., Brooks W.H., Sparks D.L., Markesbery W.R., Roszman T.L. Neuroimmunomodulation: impairment of humoral immune responsiveness by 6-hydroxydopamine treatment. Immunology 1986, 57:145-152.
15. De Luigi A., Pizzimenti S., Quadri P., Lucca U., Tettamanti M., Fragiacomo C., De Simoni M.G. Peripheral inflammatory response in Alzheimer's Disease and Multiinfarct Dementia. Neurobiol. Dis. 2002, 11:308-314.
16. del Rey A., Roggero E., Kabiersch A., Schafer M., Besedovsky H.O. The role of noradrenergic nerves in the development of the lymphoproliferative disease in Fas-deficient, lpr/lpr Mice. J. Immunol. 2006, 176:7079-7086.
17. Dudley M.W., Howard B.D., Cho A.K. The interaction of the beta-haloethyl benzylamines, xylamine, and DSP-4 with catecholaminergic neurons. Annu. Rev. Pharmacol. Toxicol. 1990, 30:387-403.
18. Elenkov I.J., Wilder R.L., Chrousos G.P., Vizi E.S. The sympathetic nerve - an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev. 2000, 52:595-638.
19. Engler H., Dawils L., Hoves S., Kurth S., Stevenson J.R., Schauenstein K., Stefanski V. Effects of social stress on blood leukocyte distribution: the role of alpha- and beta-adrenergic mechanisms. J. Neuroimmunol. 2004, 156:153-162.
20. Engler H., Doenlen R., Riether C., Engler A., Niemi M.B., Besedovsky H.O., del Rey A., Pacheco-López G., Feldon J., Schedlowski M. Time-dependent alterations of peripheral immune parameters after nigrostriatal dopamine depletion in a rat model of Parkinson's disease. Brain Behav. Immun. 2009, 23:518-526.
21. Felten S.Y., Olschowka J. Noradrenergic sympathetic innervation of the spleen: II. Tyrosine hydroxylase (TH)-positive nerve terminals form synapticlike contacts on lymphocytes in the splenic white pulp. J. Neurosci. Res. 1987, 18:37-48.
22. Felten D.L., Felten S.Y., Carlson S.L., Olschowka J.A., Livnat S. Noradrenergic and peptidergic innervation of lymphoid tissue. J. Immunol. 1985, 135:755s-765s.
23. Fety R., Misere V., Lambas-Senas L., Renaud B. Central and peripheral changes in catecholamine-synthesizing enzyme activities after systemic administration of the neurotoxin DSP-4. Eur. J. Pharmacol. 1986, 124:197-202.
24. Fornai F., Bassi L., Torracca M.T., Alessandri M.G., Scalori V., Corsini G.U. Region- and neurotransmitter-dependent species and strain differences in DSP-4-induced monoamine depletion in rodents. Neurodegeneration 1996, 5:241-249.
25. Fritschy J.M., Grzanna R. Experimentally-induced neuron loss in the locus coeruleus of adult rats. Exp. Neurol. 1991, 111:123-127.
26. Fritschy J.M., Grzanna R. Restoration of ascending noradrenergic projections by residual locus coeruleus neurons: compensatory response to neurotoxin-induced cell death in the adult rat brain. J. Comp. Neurol. 1992, 321:421-441.
27. German D.C., Manaye K.F., White C.L., Woodward D.J., McIntire D.D., Smith W.K., Kalaria R.N., Mann D.M. Disease-specific patterns of locus coeruleus cell loss. Ann. Neurol. 1992, 32:667-676.
28. Handa K., Suzuki R., Matsui H., Shimizu Y., Kumagai K. Natural killer (NK) cells as a responder to interleukin 2 (IL-2). II. IL-2-induced interferon gamma production. J. Immunol. 1983, 130:988-992.
29. Hasegawa Y., Inagaki T., Sawada M., Suzumura A. Impaired cytokine production by peripheral blood mononuclear cells and monocytes/macrophages in Parkinson's disease. Acta Neurol. Scand. 2000, 101:159-164.
30. Howard C.V., Reed M.G. Unbiased stereology 2005, BIOS Scientific Publishers, Oxford.
31. Jaim-Etcheverry G., Zieher L.M. DSP-4: a novel compound with neurotoxic effects on noradrenergic neurons of adult and developing rats. Brain Res. 1980, 188:513-523.
32. Jones B.E., Moore R.Y. Ascending projections of the locus coeruleus in the rat. II. Autoradiographic study. Brain Res. 1977, 127:25-53.
33. Jonsson G., Hallman H., Ponzio F., Ross S. DSP-4 (N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine) - A useful denervation tool for central and peripheral noradrenaline neurons. Eur. J. Pharmacol. 1981, 72:173-188.
34. Jovanova-Nesic K., Nikolic V., Jankovic B.D. Locus ceruleus and immunity. II. Suppression of experimental allergic encephalomyelitis and hypersensitivity skin reactions in rats with lesioned locus ceruleus. Int. J. Neurosci. 1993, 68:289-294.
35. Kin N.W., Sanders V.M. It takes nerve to tell T and B cells what to do. J. Leukoc. Biol. 2006, 79:1093-1104.
36. Lohr J.B., Jeste D.V. Locus ceruleus morphometry in aging and schizophrenia. Acta Psychiatr. Scand. 1988, 77:689-697.
37. Madden K.S., Felten S.Y., Felten D.L., Sundaresan P.R., Livnat S. Sympathetic neural modulation of the immune system. I. Depression of T cell immunity in vivo and vitro following chemical sympathectomy. Brain Behav. Immun. 1989, 3:72-89.
38. Madden K.S., Stevens S.Y., Felten D.L., Bellinger D.L. Alterations in T lymphocyte activity following chemical sympathectomy in young and old Fischer 344 rats. J. Neuroimmunol. 2000, 103:131-145.
39. Mann D.M. The locus coeruleus and its possible role in ageing and degenerative disease of the human central nervous system. Mech. Ageing Dev. 1983, 23:73-94.
40. Marien M.R., Colpaert F.C., Rosenquist A.C. Noradrenergic mechanisms in neurodegenerative diseases: a theory. Brain Res. Brain Res. Rev. 2004, 45:38-78.
41. Martin G.E., Elgin R.J. Effects of cerebral depletion of norepinephrine on conditioned avoidance responding in Sprague-Dawley and Fischer rats. Pharmacol. Biochem. Behav. 1988, 30:137-142.
42. Matthews K.L., Chen C.P., Esiri M.M., Keene J., Minger S.L., Francis P.T. Noradrenergic changes, aggressive behavior, and cognition in patients with dementia. Biol. Psychiatry 2002, 51:407-416.
43. Nance D.M., Sanders V.M. Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav. Immun. 2007, 21:736-745.
44. Nikolic V., Jovanova-Nesic K., Jankovic B.D. Locus ceruleus and immunity. I. Suppression of plaque-forming cell response and antibody production in rats with lesioned locus ceruleus. Int. J. Neurosci. 1993, 68:283-287.
45. Ögren S.O., Archer T., Ross S.B. Evidence for a role of the locus coeruleus noradrenaline system in learning. Neurosci. Lett. 1980, 20:351-356.
46. Pacheco-López G., Niemi M.-B., Kou W., Bildhäuser A., Gross C.M., Goebel M.U., del Rey A., Besedovsky H.O., Schedlowski M. Central catecholamine depletion inhibits peripheral lymphocyte responsiveness in spleen and blood. J. Neurochem. 2003, 86:1024-1031.
47. Panda A., Arjona A., Sapey E., Bai F., Fikrig E., Montgomery R.R., Lord J.M., Shaw A.C. Human innate immunosenescence: causes and consequences for immunity in old age. Trends Immunol. 2009, 30:325-333.
48. Penix L., Weaver W.M., Pang Y., Young H.A., Wilson C.B. Two essential regulatory elements in the human interferon gamma promoter confer activation specific expression in T cells. J. Exp. Med. 1993, 178:1483-1496.
49. Ressler K.J., Nemeroff C.B. Role of norepinephrine in the pathophysiology and treatment of mood disorders. Biol. Psychiatry 1999, 46:1219-1233.
50. Richartz E., Stransky E., Batra A., Simon P., Lewczuk P., Buchkremer G., Bartels M., Schott K. Decline of immune responsiveness: a pathogenetic factor in Alzheimer's disease?. J. Psychiatr. Res. 2005, 39:535-543.
51. Sanders V.M., Straub R.H. Norepinephrine, the beta-adrenergic receptor, and immunity. Brain Behav. Immun. 2002, 16:290-332.
52. Sara S.J. The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. Neurosci. 2009, 10:211-223.
53. Schedlowski M., Falk A., Rohne A., Wagner T.O., Jacobs R., Tewes U., Schmidt R.E. Catecholamines induce alterations of distribution and activity of human natural killer (NK) cells. J. Clin. Immunol. 1993, 13:344-351.
54. Schedlowski M., Hosch W., Oberbeck R., Benschop R.J., Jacobs R., Raab H.R., Schmidt R.E. Catecholamines modulate human NK cell circulation and function via spleen-independent beta 2-adrenergic mechanisms. J. Immunol. 1996, 156:93-99.
55. Shirokawa T., Ishida Y., Isobe K. Differential effects of DSP-4 on noradrenaline level in the parietal cortex, spleen, and adrenal medulla. Neurosci. Res. Commun. 2000, 27:67-74.
56. Srinivasan J., Schmidt W.J. Behavioral and neurochemical effects of noradrenergic depletions with N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine in 6-hydroxydopamine-induced rat model of Parkinson's disease. Behav. Brain Res. 2004, 151:191-199.
57. Sternberg E.M. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat. Rev. Immunol. 2006, 6:318-328.
58. Torres K.C., Antonelli L.R., Souza A.L., Teixeira M.M., Dutra W.O., Gollob K.J. Norepinephrine, dopamine and dexamethasone modulate discrete leukocyte subpopulations and cytokine profiles from human PBMC. J. Neuroimmunol. 2005, 166:144-157.
59. Zarow C., Lyness S.A., Mortimer J.A., Chui H.C. Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch. Neurol. 2003, 60:337-341.