Modulation of innate immunity by copolymer-1 leads to neuroprotection in murine HIV-1 encephalitis

GLIA

Volumn 56, Issue 2, 2008, Pages 223-232

  Gorantla, Santhi ^a,b   Liu, Jianuo ^a,b   Wang, Tong ^a,b   Holguin, Adelina ^a,b   Sneller, Hannah M ^a,b   Dou, Huanyu ^a,b   Kipnis, Jonathan ^a,b   Poluektova, Larisa ^a,b   Gendelman, Howard E ^a,b,c  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Anti inflammatory; Copolymer 1; HIV encephalitis; Human immunodeficiency virus; Microglia; Neuroprotection; Severe combined immunodeficient mice

Indexed keywords

ANTIINFLAMMATORY AGENT; BRAIN DERIVED NEUROTROPHIC FACTOR; GLATIRAMER; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; MICROTUBULE ASSOCIATED PROTEIN 2; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BASAL GANGLION; BRAIN REGION; C57BL 6 MOUSE; CONTROLLED STUDY; EMBRYO; FEMALE; FETUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INNATE IMMUNITY; MACROPHAGE; MALE; MONOCYTE; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCID MOUSE; VIRUS ENCEPHALITIS;

ANIMALS; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENCEPHALITIS, VIRAL; GENE EXPRESSION REGULATION, VIRAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HIV INFECTIONS; HUMANS; IMMUNITY, NATURAL; IMMUNOSUPPRESSIVE AGENTS; IN SITU NICK-END LABELING; MALE; MICE; MICE, SCID; NEUROGLIA; NEURONS; PEPTIDES; TIME FACTORS;

EID: 37349043738     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20607     Document Type: Article

References (55)

1. Adorini L. 2004. Immunotherapeutic approaches in multiple sclerosis. J Neurol Sci 223:13-24.
2. Aharoni R, Kayhan B, Eilam R, Sela M, Arnon R. 2003. Glatiramer acetate-specific T cells in the brain express T helper 2/3 cytokines and brain-derived neurotrophic factor in situ. Proc Natl Acad Sci USA 100:14157-14162.
3. Aharoni R, Teitelbaum D, Leitner O, Meshorer A, Sela M, Arnon R. 2000. Specific Th2 cells accumulate in the central nervous system of mice protected against experimental autoimmune encephalomyelitis by copolymer 1. Proc Natl Acad Sci USA 97:11472-11477.
4. Aharoni R, Teitelbaum D, Sela M, Arnon R. 1997. Copolymer 1 induces T cells of the T helper type 2 that crossreact with myelin basic protein and suppress experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 94:10821-10826.
5. Aksenov MY, Hasselrot U, Wu G, Nath A, Anderson C, Mactutus CF, Booze RM. 2003. Temporal relationships between HIV-1 Tat-induced neuronal degeneration, OX-42 immunoreactivity, reactive astrocytosis, and protein oxidation in the rat striatum. Brain Res 987:1-9.
6. Arnon R, Aharoni R. 2004. Mechanism of action of glatiramer acetate in multiple sclerosis and its potential for the development of new applications. Proc Natl Acad Sci USA 101 (Suppl 2): 14593-14598.
7. Arnon R, Sela M. 2003. Immunomodulation by the copolymer glatiramer acetate. J Mol Recogn 16:412-421.
8. Benner EJ, Mosley RL, Destache CJ, Lewis TB, Jackson-Lewis V, Gorantla S, Nemachek C, Green SR, Przedborski S, Gendelman HE. 2004. Therapeutic immunization protects dopaminergic neurons in a mouse model of Parkinson's disease. Proc Natl Acad Sci USA 101: 9435-9440.
9. Butovsky O, Landa G, Kunis G, Ziv Y, Avidan H, Greenberg N, Schwartz A, Smirnov I, Pollack A, Jung S, Swhartz M. 2006. Induction and blockage of oligodendrogenesis by differently activated microglia in an animal model of multiple sclerosis. J Clin Invest 116: 905-915.
10. Dou H, Birusingh K, Faraci J, Gorantla S, Poluektova LY, Maggirwar SB, Dewhurst S, Gelbard HA, Gendelman HE. 2003. Neuroprotective activities of sodium valproate in a murine model of human immunodeficiency virus-1 encephalitis. J Neurosci 23:9162-9170.
11. Dou H, Ellison B, Bradley J, Kasiyanov A, Poluektova LY, Xiong H, Maggirwar S, Dewhurst S, Gelbard HA, Gendelman HE. 2005. Neuroprotective mechanisms of lithium in murine human immunodeficiency virus-1 encephalitis. J Neurosci 25:8375-8385.
12. Dou H, Kingsley JD, Mosley RL, Gelbard HA, Gendelman HE. 2004. Neuroprotective strategies for HIV-1 associated dementia. Neurotox Res 6:503-521.
13. Frenkel D, Huang Z, Maron R, Koldzic DN, Hancock WW, Moskowitz MA, Weiner HL. 2003. Nasal vaccination with myelin oligodendrocyte glycoprotein reduces stroke size by inducing IL-10-producing CD4+ T cells. J Immunol 171:6549-6555.
14. Frenkel D, Maron R, Burt DS, Weiner HL. 2005. Nasal vaccination with a proteosome-based adjuvant and glatiramer acetate clears β-amyloid in a mouse model of Alzheimer disease. J Clin Invest 115: 2423-2433.
15. Garden GA. 2002. Microglia in human immunodeficiency virus-associated neurodegeneration. Glia 40:240-251.
16. Gendelman HE, Diesing S, Gelbard H, Swindells S. 2004. The neuropathogenesis of HIV-1 infection. In: Wormser GP, editor. AIDS and other manifestations of HIV infection. Amsterdam: Elsevier. pp 95-116.
17. Gendelman HE, Orenstein JM, Martin MA, Ferrua C, Mitra R, Phipps T, Wahl LA, Lane HC, Fauci AS, Burke DS, et al. 1988. Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-treated monocytes. J Exp Med 167:1428-1441.
18. Gorantla S, Liu J, Sneller H, Dou H, Holguin A, Smith L, Ikezu T, Volsky DJ, Poluektova L, Gendelman HE. 2007. Copolymer-1 induces adaptive immune anti-inflammatory glial and neuroprotective responses in a murine model of HIV-1 encephalitis. J Immunol 179: 4345-4356.
19. Gordon PH, Doorish C, Montes J, Mosley RL, Diamond B, Macarthur RB, Weimer LH, Kaufmann P, Hays AP, Rowland LP, Gendelman HE, Przedboski S, Mitsumoto H. 2006. Randomized controlled phase II trial of glatiramer acetate in ALS. Neurology 66:1117-1119.
20. Gray F, Adle-Biassette H, Chretien F, Lorin de la Grandmaison G, Force G, Keohane C. 2001. Neuropathology and neurodegeneration in human immunodeficiency virus infection. Pathogenesis of HIV-induced lesions of the brain, correlations with HIV-associated disorders and modifications according to treatments. Clin Neuropathol 20:146-155.
21. Jung S, Siglienti I, Grauer O, Magnus T, Scarlato G, Toyka K. 2004. Induction of IL-10 in rat peritoneal macrophages and dendritic cells by glatiramer acetate. J Neuroimmunol 148:63-73.
22. Kadiu I, Glanzer JG, Kipnis J, Gendelman HE, Thomas MP. 2005. Mononuclear phagocytes in the pathogenesis of neurodegenerative diseases. Neurotox Res 8:25-50.
23. Kalams SA, Walker BD. 1995. Cytotoxic T lymphocytes and HIV-1 related neurologic disorders. Curr Top Microbiol Immunol 202:79-88.
24. Kanmogne GD, Kennedy RC, Grammas P. 2002. HIV-1 gp120 proteins and gp160 peptides are toxic to brain endothelial cells and neurons: Possible pathway for HIV entry into the brain and HIV-associated dementia. J Neuropathol Exp Neurol 61:992-1000.
25. Kaul M, Lipton SA. 2005. Experimental and potential future therapeutic approaches for HIV-1 associated dementia targeting receptors for chemokines, glutamate and erythropoietin. Neurotox Res 8:167-186.
26. Kim HJ, Ifergan I, Antel JP, Seguin R, Duddy M, Lapierre Y, Jalili F, Bar-Or A. 2004. Type 2 monocyte and microglia differentiation mediated by glatiramer acetate therapy in patients with multiple sclerosis. J Immunol 172:7144-7153.
27. Kipnis J, Nevo U, Panikashvili D, Alexandrovich A, Yoles E, Akselrod S, Shohami E, Schwartz M. 2003. Therapeutic vaccination for closed head injury. J Neurotrauma 20:559-569.
28. Kipnis J, Yoles E, Porat Z, Cohen A, Mor F, Sela M, Cohen IR, Schwartz M. 2000. T cell immunity to copolymer 1 confers neuroprotection on the damaged optic nerve: Possible therapy for optic neuropathies. Proc Natl Acad Sci USA 97:7446-7451.
29. Li Q, Milo R, Panitch H, Swoveland P, Bever CT Jr. 1998. Glatiramer acetate blocks the activation of THP-1 cells by interferon-γ. Eur J Pharmacol 342:303-310.
30. Li QQ, Bever CT. 2001. Glatiramer acetate blocks interleukin-1-dependent nuclear factor-κB activation and RANTES expression in human U-251 MG astroglial cells. Brain Res Mol Brain Res 87:48-60.
31. Li QQ, Burt DR, Bever CT. 2001. Glatiramer acetate inhibition of tumor necrosis factor-α-induced RANTES expression and release from U-251 MG human astrocytic cells. J Neurochem 77:1208-1217.
32. Liu J, Johnson TV, Lin J, Ramirez SH, Bronich TK, Caplan S, Persidsky Y, Gendelman HE, Kipnis J. 2007. T cell independent mechanism for copolymer-1-induced neuroprotection. Eur J Immunol 37:3143-3154.
33. Lokensgard JR, Gekker G, Ehrlich LC, Hu S, Chao CC, Peterson PK. 1997. Proinflammatory cytokines inhibit HIV-1(SF162) expression in acutely infected human brain cell cultures. J Immunol 158:2449-2455.
34. Losy J, Michalowska-Wender G, Wender M. 2002. Interleukin 12 and interleukin 10 are affected differentially by treatment of multiple sclerosis with glatiramer acetate (Copaxone). Folia Neuropathol 40: 173-175.
35. McArthur JC. 2004. HIV dementia: An evolving disease. J Neuroimmunol 157:3-10.
36. McArthur JC, Brew BJ, Nath A. 2005. Neurological complications of HIV infection. Lancet Neurol 4:543-555.
37. Miller A, Shapiro S, Gershtein R, Kinarty A, Rawashdeh H, Honigman S, Lahat N. 1998. Treatment of multiple sclerosis with copolymer-1 (Copaxone): Implicating mechanisms of Th1 to Th2/Th3 immune-deviation. J Neuroimmunol 92:113-121.
38. Mosley RL, Gordon PH, Hasiak CM, Van Wetering FJ, Mitsumoto H, Gendelman HE. 2007. Glatiramer acetate immunization induces specific antibody and cytokine responses in ALS patients. Amyotroph Lateral Scler 8:235-242.
39. Navia BA, Rostasy K. 2005. The AIDS dementia complex: Clinical and basic neuroscience with implications for novel molecular therapies. Neurotox Res 8:3-24.
40. Persidsky Y, Buttini M, Limoges J, Bock P, Gendelman HE. 1997. An analysis of HIV-1-associated inflammatory products in brain tissue of humans and SCID mice with HIV-1 encephalitis. J Neurovirol 3:401-416.
41. Persidsky Y, Gendelman HE. 2002. Murine models for human immunodeficiency virus type 1-associated dementia: The development of new treatment testing paradigms. J Neurovirol 8 (Suppl 2):49-52.
42. Persidsky Y, Limoges J, McComb R, Bock P, Baldwin T, Tyor W, Patil A, Nottet HS, Epstein L, Gelbard H, Flanagan E, Reinhard J, Pirruccelo SJ, Gendelman HE. 1996. Human immunodeficiency virus encephalitis in SCID mice. Am J Pathol 149:1027-1053.
43. Poli G, Kinter AL, Justement JS, Bressler P, Kehrl JH, Fauci AS. 1991. Transforming growth factor beta suppresses human immunodeficiency virus expression and replication in infected cells of the monocyte/macrophage lineage. J Exp Med 173:589-597.
44. Rostasy K, Monti L, Lipton SA, Hedreen JC, Gonzalez RG, Navia BA. 2005. HIV leucoencephalopathy and TNFα expression in neurones. J Neurol Neurosurg Psychiatry 76:960-964.
45. Rostasy KM. 2005. Inflammation and neuroaxonal injury in multiple sclerosis and AIDS dementia complex: Implications for neuroprotective treatment. Neuropediatrics 36:230-239.
46. Sanders VJ, Pittman CA, White MG, Wang G, Wiley CA, Achim CL. 1998. Chemokines and receptors in HIV encephalitis. AIDS 12:1021-1026.
47. Schifitto G, Peterson DR, Zhong J, Ni H, Cruttenden K, Gaugh M, Gendelman HE, Boska M, Gelbard H. 2006. Valproic acid adjunctive therapy for HIV-associated cognitive impairment: A first report. Neurology 66:919-921.
48. Smith DG, Guillemin GJ, Pemberton L, Kerr S, Nath A, Smythe GA, Brew BJ. 2001. Quinolinic acid is produced by macrophages stimulated by platelet activating factor, Nef and Tat. J Neurovirol 7:56-60.
49. Sopper S, Sauer U, Hemm S, Demuth M, Muller J, Stahl-Hennig C, Hunsmann G, ter Meulen V, Dorries R. 1998. Protective role of the virus-specific immune response for development of severe neurologic signs in simian immunodeficiency virus-infected macaques. J Virol 72:9940-9947.
50. Tyor WR, Power C, Gendelman HE, Markham RB. 1993. A model of human immunodeficiency virus encephalitis in scid mice. Proc Natl Acad Sci USA 90:8658-8662.
51. Vieira PL, Heystek HC, Wormmeester J, Wierenga EA, Kapsenberg ML. 2003. Glatiramer acetate (copolymer-1, Copaxone) promotes Th2 cell development and increased IL-10 production through modulation of dendritic cells. J Immunol 170:4483-4488.
52. Weber MS, Prod'homme T, Youssef S, Dunn SE, Rundle CD, Lee L, Patarroyo JC, Stuve O, Sobel RA, Steinman L, Zamvil SS. 2007. Type II monocytes modulate T cell-mediated central nervous system autoimmune disease. Nat Med 13:935-943.
53. Wolinsky JS. 2004. Glatiramer acetate for the treatment of multiple sclerosis. Expert Opin Pharmacother 5:875-891.
54. Zink WE, Anderson E, Boyle J, Hock L, Rodriguez-Sierra J, Xiong H, Gendelman HE, Persidsky Y. 2002. Impaired spatial cognition and synaptic potentiation in a murine model of human immunodeficiency virus type 1 encephalitis. J Neurosci 22:2096-2105.
55. Zink WE, Boyle J, Persidsky Y, Xiong H, Gendelman HE. 2001. Model systems for assessing cognitive function: Implications for HIV-1 infection and drugs of abuse. Adv Exp Med Biol 493:7-27.