Sympathetic nerve destruction in spleen in murine AIDS

Brain, Behavior, and Immunity

Volumn 17, Issue 2, 2003, Pages 94-109

  Kelley, Sheila P ^a   Moynihan, Jan A ^a   Stevens, Suzanne Y ^a   Grota, Lee J ^a   Felten, David L ^b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Desipramine; LP BM5; MAIDS; Murine AIDS; Norepinephrine; Spleen; Sympathetic nervous system

Indexed keywords

DESIPRAMINE; NORADRENALIN; NORADRENALIN UPTAKE INHIBITOR; ADRENERGIC RECEPTOR AFFECTING AGENT;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; IMMUNOCYTOCHEMISTRY; INOCULATION; MALE; MOUSE; NERVE FIBER; NERVE INJURY; NONHUMAN; NORADRENALIN RELEASE; PRIORITY JOURNAL; PROTEIN DEPLETION; RODENT DISEASE; SPLEEN; SPLENOMEGALY; SYMPATHETIC NERVE; ANIMAL; AUTONOMIC NEUROPATHY; C57BL MOUSE; DISEASE COURSE; INNERVATION; METABOLISM; OXIDATION REDUCTION REACTION; VIROLOGY;

ADRENERGIC UPTAKE INHIBITORS; ANIMALS; AUTONOMIC NERVOUS SYSTEM DISEASES; DESIPRAMINE; DISEASE PROGRESSION; MALE; MICE; MICE, INBRED C57BL; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; NOREPINEPHRINE; OXIDATION-REDUCTION; SPLEEN;

EID: 0037381151     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0889-1591(02)00101-0     Document Type: Article

References (97)

1. Adle-Biassette H., Levy Y., Colombel M., Poron F., Natchev S., Keohane C., Gray F. Neuronal apoptosis in HIV infection in adults. Neuropathol. Appl. Neurobiol. 21:1995;218-227.
2. Akiyoshi M., Shimizu Y., Saito M. Interleukin-1 increases norepinephrine turnover in the spleen and lung in rats. Biochem. Biophys. Res. Commun. 173(3):1990;1266-1270.
3. Alaniz R.C., Thomas S.A., Perez-Melgosa M., Mueller K., Farr A.G., Palmiter R.D., Wilson C.B. Dopamine β-hydroxylase deficiency impairs cellular immunity. Proc. Natl. Acad. Sci. USA. 96(5):1999;2274-2278.
4. Axelrod J., Kopin I.J. The uptake, storage, release, and metabolism of noradrenaline in sympathetic nerves. Prog. Brain Res. 31:1969;21-32.
5. Bachmann M.F., Zinkernagel R.M. Neutralizing antiviral B cell responses. Ann. Rev. Immunol. 15:1997;235-270.
6. Balant-Gorgia A.E., Gex-Fabry M., Balant L.P. Clinical pharmacokinetics of clomipramine. Clin. Pharmacokinet. 20(6):1991;447-462.
7. Barzilai A., Zilkha-Falb R., Daily D., Stern N., Offen D., Ziv I., Melamed E., Shirvan A. The molecular mechanism of dopamine-induced apoptosis: Identification and characterization of genes that mediate dopamine toxicity. J. Neural Transm. Suppl. 60:2000;59-76.
8. Batman P.A., Miller A.R.O., Sedgwick P.M., Griffin G.E. Autonomic denervation in jejunal mucosa of homosexual men infected with HIV. AIDS. 5:1991;1247-1252.
9. Becker K., Gorlach I., Frieling T., Haussinger D. Characterization and natural course of cardiac autonomic nervous dysfunction in HIV-infected patients. AIDS. 11:1997;751-757.
10. Bougerolle A.M., Chabard J.L., Eschalier A., Aumaitre O., Fialip J., Dordain G., Petit J., Berger J.A. Pharmacokinetics of metapramine and its demethylated metabolites in plasma and brain of mice. Fundam. Clin. Pharmacol. 3(5):1989;515-525.
11. Bradley W.G., Ogata N., Good R.A., Day N.K. Alteration of in vivo cytokine gene expression in mice infected with a molecular clone of the defective MAIDS virus. J. Acquir. Immune Defic. Syndr. 7:1994;1-9.
12. Cheung S.C., Chattopadhyay S.K., Morse H.C. III, Pitha P.M. Expression of defective virus and cytokine genes in murine AIDS. J. Virol. 65(2):1991;823-828.
13. Cohen J.A., Laudenslager M. Autonomic nervous system involvement in patients with human immunodeficiency virus infection. Neurology. 39:1989;1111-1112.
14. Coudore F., Fialip J., Eschalier A., Lavarenne J. Mice plasma and brain pharmacokinetics of amitriptyline and its demethylated and hydroxylated metabolites after half-life repeated administration: Comparison with acute administration. Fundam. Clin. Pharmacol. 8(6):1994;525-531.
15. Dailey M.O. The Immune Functions of the Spleen. Bowdler A.J. The complete spleen: Structure, function, and clinical disorders. 2nd ed. 2002;51-69 Humana Press, Totowa, New Jersey.
16. DeLuigi A., Terreni L., Sironi M., DeSimoni M.G. The sympathetic nervous system tonically inhibits peripheral interleukin-. 1β and interleukin-6 induction by central lipopolysaccharide Neuroscience. 83(4):1998;1245-1250.
17. Dobbs C.M., Vasquez M., Glaser R., Sheridan J.F. Mechanisms of stress-induced modulation of viral pathogenesis and immunity. J. Neuroimmunol. 48:1993;151-160.
18. Elfvin L.-G., Aldskogius H., Johansson J. Splenic primary sensory afferents in the guinea pig demonstrated with anterogradely transported wheat-germ agglutinin conjugated to horseradish peroxidase. Cell Tissue Res. 269:1992;229-234.
19. Eschalier A., Fialip J., Varoquaux O., Makambila M.C., Marty H., Bastide P. Pharmacokinetic patterns of repeated administration of antidepressants in animals. I. Implications for antinociceptive action of clomipramine in mice. J. Pharmacol. Exp. Ther. 245:1988;963-968.
20. Esler M. Clinical application of noradrenaline spillover methodology: Delineation of regional human sympathetic nervous responses. Pharmacol. Toxicol. 73:1993;243-253.
21. Esler M., Jennings G., Leonard P., Sacharias N., Burke F., Johns J., Blombery P. Contribution of individual organs to total noradrenaline release in humans. Acta Physiol. Scand. Suppl. 527:1984;11-16.
22. Espey M.G., Basile A.S. Glutamate augments retrovirus-induced immunodeficiency through chronic stimulation of the hypothalamic-pituitary-adrenal axis. J. Immunol. 162(8):1999;4998-5002.
23. Espey M.G., Kustova Y., Sei Y., Basile A.S. LP-BM5 MuLV infection: Impact on the immune and central nervous systems. Wong P.K.Y., Lynn W.S. Neuroimmunodegeneration. 1998;95-114 Springer-Verlag, Berlin.
24. Fahn S., Cohen G. The oxidative stress hypothesis in Parkinson's disease: Evidence supporting it. Ann. Neurol. 32(6):1992;804-812.
25. Felten D.L., Ackerman K.D., Wiegand S.J., Felten S.Y. Noradrenergic sympathetic innervation of the spleen: I. Nerve fibers associate with lymphocytes and macrophages in specific compartments of the splenic white pulp. J. Neurosci. Res. 18:1987;28-36.
26. Felten D.L., Felten S.Y., Bellinger D.L., Carlson S.L., Ackerman K.D., Madden K.S., Olschowka J.A., Livnat S. Noradrenergic sympathetic neural interactions with the immune system: Structure and function. Immunol. Rev. 100:1987;225-260.
27. Felten D.L., Felten S.Y., Carlson S.L., Olschowka J.A., Livnat S. Noradrenergic and peptidergic innervation of lymphoid tissue. J. Immunol. 135(2):1985;755s-765s.
28. Felten S.Y., Felten D.L., Bellinger D.L., Olschowka J.A. Noradrenergic and peptidergic innervation of lymphoid organs. Chem. Immunol. 52:1992;25-48.
29. Foley P., Reiderer P. Influence of neurotoxins and oxidative stress on the onset and progression of Parkinson's disease. J. Neurol. 247(Suppl. 2):2000;82-94.
30. Fraternale A., Casabianca A., Tonelli A., Chiarantini L., Brandi G., Magnani M. New drug combinations for the treatment of murine AIDS and macrophage protection. Eur. J. Clin. Invest. 31(3):2001;190-192.
31. Fujimoto E., Mizoguchi A., Hanada K., Yajima M., Ide C. Basic fibroblast growth factor promotes extension of regenerating axons of peripheral nerve. In vivo experiments using a Schwann cell basal lamina tube model. J. Neurocytol. 26:1997;511-528.
32. Furokawa K., Sasaki H., Pollard R.B., Suzuki F. Lanoconazole, a new imidazole antimycotic compound, protects MAIDS mice against encephalitis caused by Cryptococcus neoformans. J. Antimicrob. Chemother. 46(3):2000;443-450.
33. Garland W.A., Min B.H., Birkett D.J. The kinetics of amitriptyline following single oral dose administration to man. Res. Commun. Chem. Pathol. Pharmacol. 22(3):1978;475-484.
34. Gelbard H.A., James H.J., Sharer L.R., Perry S.W., Saito Y., Kazee A.M., Blumberg B.M., Epstein L.G. Apoptotic neurons in brains from pediatric patients with HIV-1 encephalitis and progressive encephalopathy. Neuropathol. Appl. Neurobiol. 21:1995;208-217.
35. Giese N.A., Gazzinelli R.T., Actor J.K., Morawetz R.A., Sarzotti M. Retrovirus-elicited interleukin-12 and tumor necrosis factor-α as inducers of interferon-γ-mediated pathology in mouse AIDS. Immunology. 87:1996;467-474.
36. Goldstein D.S., Eisenhofer G., Garty M., Folio C.J., Stull R., Brush J.E. Jr., Sax F.L., Keiser H.R., Kopin I.J. Implications of plasma levels of catechols in the evaluation of sympathoadrenomedullary function. Am. J. Hypertens. 2(3 Pt 2):1989;133S-139S.
37. Gottesfeld Z., Simpson S., Maier M. Exposure to alcohol in utero blunts splenic sympathetic neural response to endotoxin and interleukin-. 1β in the rat J. Neuroimmunol. 78:1997;180-183.
38. Graham D.G. Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol. Pharmacol. 14:1978;633-643.
39. Graham D.G., Tiffany S.M., Bell W.R. Jr., Gutknect W.F. Autoxidation versus covalent binding of quinones as the mechanism of toxicity of dopamine, 6-hydroxydopamine, and related compounds toward C1300 neuroblastoma cells in vitro. Mol. Pharmacol. 14:1978;644-653.
40. Griffin G.E., Miller A., Batman P., Forster S.M., Pinching A.J., Harris J.R., Mathan M.M. Damage to jejunal intrinsic autonomic nerves in HIV infection. AIDS. 2(5):1988;379-382.
41. Griffin J.W., Wesselingh S.L., Griffin D.E., Glass J.D., McArthur J.C. Peripheral nerve disorders in HIV infection. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 72:1994;159-182.
42. Haas M., Meshorer A. Reticulum cell neoplasms induced in C57BL/6 mice by cultured virus grown in stromal hematopoietic cell lines. J. Natl. Cancer Inst. 63(2):1979;427-436.
43. Hartley J.W., Fredrickson T.N., Yetter R.A., Makino M., Morse H.C. III Retrovirus-induced murine acquired immunodeficiency syndrome: Natural history of infection and differing susceptibility of inbred mouse strains. J. Virol. 63(3):1989;1223-1231.
44. Hastings T.G., Zigmund M.J. Loss of dopaminergic neurons in parkinsonism: Possible role of reactive dopamine metabolites. J. Neural Transm. 49(Suppl.):1997;103-110.
45. Hermann G., Beck F.M., Tovar C.A., Malarkey W.B., Allen C., Sheridan J.F. Stress-induced changes attributable to the sympathetic nervous system during experimental influenza viral infection in DBA/2 inbred mouse strain. J. Neuroimmunol. 53:1994;173-180.
46. Himura Y., Felten S.Y., Kashiki M., Lewandowski T.J., Delehanty J.M., Liang C.S. Cardiac noradrenergic nerve terminal abnormalities in dogs with experimental congestive heart failure. Circulation. 88:1993;1299-1309.
47. Iga K., Himura Y., Izumi C., Miyamoto T., Kijima K., Gen H., Konishi T. Reversible left ventricular dysfunction associated with Guillain-Barre syndrome - an expression of catecholamine cardiotoxicity? Jpn. Circ. J. 59(4):1995;236-240.
48. Iida R., Yamada K., Mamiya T., Saito K., Seishima M., Nabeshima T. Characterization of learning and memory deficits in C57BL/6 mice infected with LP-BM5, a murine model of AIDS. J. Neuroimmunol. 95:1999;65-72.
49. Iversen L.L. The uptake and storage of noradrenaline in sympathetic nerves. 1967;Cambridge University Press, London.
50. Iversen L.L. Uptake mechanisms for neurotransmitter amines. Biochem. Pharmacol. 23:1974;1927-1935.
51. Kelley S.P., Moynihan J.A., Stevens S.Y., Grota L.J., Felten D.L. Chemical sympathectomy has no effect on the severity of murine AIDS: Murine AIDS alone depletes norepinephrine levels in infected spleen. Brain Behav. Immun. 16:2002;118-139.
52. Kostrzewa R.M., Jacobowitz D.M. Pharmacological actions of 6-hydroxydopamine. Pharmacol. Rev. 26:1974;199-288.
53. Kruszewska B., Felten D.L., Stevens S.Y., Moynihan J.A. Sympathectomy-induced immune changes are not abrogated by the glucocorticoid receptor blocker RU-486. Brain Behav. Immun. 12:1998;181-200.
54. Kruszewska B., Felten S.Y., Moynihan J.A. Alterations in cytokine and antibody production following chemical sympathectomy in two strains of mice. J. Immunol. 155:1995;4613-4620.
55. Kustova Y., Espey M.G., Sung E., Morse D., Sei Y., Basile A.S. Evidence of neuronal degeneration in C57BL/6 mice infected with the LP-BM5 leukemia retrovirus mixture. Mol. Chem. Neuropathol. 35:1998;39-59.
56. Kustova Y., Sei Y., Goping G., Basile A.S. Gliosis in the LP-BM5 murine leukemia virus-infected mouse: An animal model of retrovirus-induced dementia. Brain Res. 742:1996;271-282.
57. Kvetnansky R., Sun C.L., Lake C.R., Thoa N., Torda T., Kopin I.J. Effect of handling and forced immobilization on rat plasma levels of epinephrine, norepinephrine, and dopamine-β-hydroxylase. Endocrinology. 103(5):1978;1868-1874.
58. Lake C.R., Chernow B., Feuerstein G., Goldstein D.S., Ziegler M.G. The sympathetic nervous system in man: Its evaluation and the measurement of plasma NE. Ziegler M.G., Lake C.R. Norepinephrine. 1984;1-26 Williams and Wilkins, Baltimore.
59. Lee B., English J.A., Paul I.A. LP-BM5 infection impairs spatial working memory in C57BL/6 mice in the Morris water maze. Brain Res. 856:2000;129-134.
60. Lorton D., Hewitt D., Bellinger D.L., Felten S.Y., Felten D.L. Noradrenergic reinnervation of the rat spleen following chemical sympathectomy with6-hydroxydopamine: Pattern and time course of reinnervation. Brain Behav. Immun. 4:1990;198-222.
61. Lund A., Mjellem-Joly N., Hole K. Chronic administration of desipramine and zimelidine changes the behavioural response in the formalin test in rats. Neuropharmacology. 30(5):1991;481-487.
62. Lund A., Tjolsen A., Hole K. Desipramine in low doses induces antinociception in the increasing temperature hot plate test. Neuropharmacology. 28:1989;1169-1173.
63. Madden K.S., Bellinger D.L., Felten S.Y., Snyder E., Maida M.E., Felten D.L. Alterations in sympathetic innervation of thymus and spleen in aged mice. Mech. Ageing Dev. 94:1997;165-175.
64. Madden K.S., Sanders V.M., Felten D.L. Catecholamine influences and sympathetic neural modulation of immune responsiveness. Annu. Rev. Pharmacol. Toxicol. 35:1995;417-448.
65. 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. 103:2000;131-145.
66. Madden K.S., ThyagaRajan S., Bellinger D.L., Felten S.Y., Felten D.L. Age-associated alterations in sympathetic neural interactions with the immune system. Dev. Comp. Immunol. 21(6):1997;479-486.
67. Mjellem N., Lund A., Hole K. Reduction of NMDA-induced behaviour after acute and chronic administration of desipramine in mice. Neuropharmacology. 32(6):1993;591-595.
68. Morse H.C. III, Chattopadhyay S.K., Makino M., Fredrickson T.N., Hugin A.W., Hartley J.W. Retrovirus-induced immunodeficiency in the mouse: MAIDS as a model for AIDS. AIDS. 6:1992;607-621.
69. Mosier D.E., Yetter R.A., Morse H.C. III Retroviral induction of acute lymphoproliferative disease and profound immunosuppression in adult C57BL/6 mice. J. Exp. Med. 161:1985;766-784.
70. Newton H.B. Common neurologic complications of HIV-1 infection and AIDS. Am. Fam. Physician. 51(2):1995;387-398.
71. Ochsenbein A.F., Pinschewer D.D., Odermatt B., Ciurea A., Hengartner H., Zinkernagel R.M. Correlation of T cell independence of antibody responses with antigen dose reaching secondary lymphoid organs: Implications for splenectomized patients and vaccine design. J. Immunol. 164:2000;6296-6302.
72. Paul W.E. Fundamental immunology. 4th ed. 1999;Lippincott-Raven, Philadelphia.
73. Rahmouni S., Aandahl E.M., Treback M., Boniver J., Tasken K., Moutschen M. Increased cAMP levels and protein kinase (PKA) type I activation in CD4+ T cells and B cells contribute to retrovirus-induced immunodeficiency of mice (MAIDS): A useful in vivo model for drug testing. FASEB J. 15(8):2001;1466-1468.
74. 3H -desipramine binding in the peripheral and central nervous system: A specific site associated with the neuronal uptake of noradrenaline Eur. J. Pharmacol. 78:1982;345-351.
75. Rice P.A., Boehm G.W., Moynihan J.A., Bellinger D.L., Stevens S.Y. Chemical sympathectomy increases the innate immune response and decreases the specific immune response in the spleen to infection with Listeria monocytogenes. J. Neuroimmunol. 114:2001;19-27.
76. Rizzuto N., Cavallaro T., Monaco S., Morbin M., Bonetti B., Ferrari S., Galiazzo-Rizzuto S., Zanette G., Bertolasi L. Role of HIV in the pathogenesis of distal symmetrical peripheral neuropathy. Acta Neuropathol. 90(3):1995;244-250.
77. Rosenberg P.A. Catecholamine toxicity in cerebral cortex in dissociated cell culture. J. Neurosci. 8(8):1988;2887-2894.
78. Rubin P.C., Reid J.L. Strategies for dynamic assessment of sympathetic activity from plasma catecholamine measurements. Ziegler M.G., Lake C.R. Norepinephrine. 1984;209-216 Williams and Wilkins, Baltimore.
79. Saito M., Akiyoshi M., Shimizu Y. Possible role of the sympathetic nervous system in responses to interleukin-1. Brain Res. Bull. 27:1991;305-308.
80. Sall J., Lehman A. JMP Start Statistics: A guide to statistical and data analysis using JMP and JMP IN software. 1996;Wadsworth Publishing Co, Belmont, CA.
81. Sei Y., Kustova Y., Li Y., Morse H. III, Skolnick P., Basile A. The encephalopathy associated with murine acquired immunodeficiency syndrome (MAIDS). Ann. N. Y. Acad. Sci. 840:1998;822-834.
82. Sei Y., Makino M., Vitkovic L., Chattopadhyay S.K., Hartley J.W., Arora P.K. Central nervous system infection in a murine retrovirus-induced immunodeficiency syndrome. J. Neuroimmunol. 37:1992;131-140.
83. Shimizu N., Hori T., Nakane H. An interleukin-. 1β -induced noradrenaline release in the spleen is mediated by brain corticotropin-releasing factor: An in vivo microdialysis study in conscious rats Brain Behav. Immun. 8:1994;14-23.
84. Spina E., Avenoso A., Campo G.M., Caputi A.P., Perucca E. The effect of carbamazepine on the 2-hydroxylation of desipramine. Psychopharmacology (Berl.). 117(4):1995;413-416.
85. Spina E., Pollicino A.M., Avenoso A., Campo G.M., Perucca E., Caputi A.P. Effect of fluvoxamine on the pharmacokinetics of imipramine and desipramine in healthy subjects. Ther. Drug Monit. 15(3):1993;243-246.
86. Takahashi K., Wesselingh S.L., Griffin D.E., McArthur J.C., Johnson R.T., Glass J.D. Localization of HIV-1 in human brain using polymerase chain reaction/in situ hybridization and immunocytochemistry. Ann. Neurol. 39:1996;705-711.
87. Teixeira A.A., Azevedo I., Branco D., Rodriques-Pereira E., Osswald W. Sympathetic denervation caused by long-term noradrenaline infusions; prevention by desipramine and superoxide dismutase. Br. J. Pharmacol. 97:1989;95-102.
88. Thompson R.J., Doran J.F., Jackson P., Dhillon A.P., Rode J. PGP 9.5: A new marker of vertebrate neurons and neuroendocrine cells. Brain Res. 278:1983;224-228.
89. Timens W. The human spleen and the immune system: Not just another lymphoid organ. Res. Immunol. 142:1991;316-320.
90. Verma A. Epidemiology and clinical features of HIV-1 associated neuropathies. J. Peripher. Nerv. Syst. 6:2001;8-13.
91. Villa A., Foresti V., Confalonieri F. Autonomic neuropathy and prolongation of QT interval in human immunodeficiency virus infection. Clin. Auton. Res. 5(1):1995;48-52.
92. Wallin B.G. Sympathetic activity in human extremity nerves and its relationship to plasma NE. Ziegler M.G., Lake C.R. Norepinephrine. 1984;431-438 Williams and Wilkins, Baltimore.
93. Weibel E.R. Stereological methods: Vol. 1. Practical methods for biological morphometry. 1979;Academic Press, London.
94. Weingarten P., Zhou Q.-Y. Protection of intracellular dopamine cytotoxicity by dopamine disposition and metabolism factors. J. Neurochem. 77:2001;776-785.
95. Welby S.B., Rogerson S.J., Beeching N.J. Autonomic neuropathy is common in human immunodeficiency virus infection. J. Infect. 23(2):1991;123-128.
96. Wilson P.O.G., Barber P.C., Hamid Q.A., Power B.F., Dhillon A.P., Rode J., Day I.N.M., Thompson R.J., Polak J.M. The immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies. Br. J. Exp. Pathol. 69:1988;91-104.
97. Wulff E.A., Wang A.K., Simpson D.M. HIV-associated peripheral neuropathy: Epidemiology, pathophysiology, and treatment. Drugs. 59(6):2000;1251-1260.