Copolymer-1 induces adaptive immune anti-inflammatory glial and neuroprotective responses in a murine model of HIV-1 encephalitis

Journal of Immunology

Volumn 179, Issue 7, 2007, Pages 4345-4356

  Gorantla, Santhi ^a,b   Liu, Jianou ^a,b   Sneller, Hannah ^a,b   Dou, Huanyu ^a,b   Holguin, Adelina ^a,b   Smith, Lynette ^b   Ikezu, Tsuneya ^a,b   Volsky, David J ^c   Poluektova, Larisa ^a,b   Gendelman, Howard E ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLATIRAMER;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTOSIS; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; VIRUS ENCEPHALITIS;

ADAPTATION, BIOLOGICAL; ANIMALS; DISEASE MODELS, ANIMAL; ENCEPHALITIS; HIV INFECTIONS; MALE; MICE; MICE, INBRED C57BL; NEUROGLIA; NEUROPROTECTIVE AGENTS; NEUTROPHILS; PEPTIDES; T-LYMPHOCYTES;

EID: 36248955601     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.7.4345     Document Type: Article

References (86)

1. McArthur, J. C., N. Haughey, S. Gartner, K. Conant, C. Pardo, A. Nath, and N. Sacktor. 2003. Human immunodeficiency virus-associated dementia: an evolving disease. J. Neurovirol. 9: 205-221.
2. Kalams, S. A., and B. D. Walker. 1995. Cytotoxic T lymphocytes and HIV-1 related neurologic disorders. Curr. Top. Microbiol. Immunol. 202: 79-88.
3. Sopper, S., U. Sauer, S. Hemm, M. Demuth, J. Muller, C. Stahl-Hennig, G. Hunsmann, V. ter Meulen, and R. Dorries. 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.
4. Everall, I. P., L. A. Hansen, and E. Masliah. 2005. The shifting patterns of HIV encephalitis neuropathology. Neurotox. Res. 8: 51-61.
5. Anthony, I. C., S. N. Ramage, F. W. Carnie, P. Simmonds, and J. E. Bell. 2005. Influence of HAART on HIV-related CNS disease and neuroinflammation. J. Neuropathol. Exp. Neurol. 64: 529-536.
6. Navia, B. A., and K. Rostasy. 2005. The AIDS dementia complex: clinical and basic neuroscience with implications for novel molecular therapies. Neurotox. Res. 8: 3-24.
7. Resnick, L., J. R. Berger, P. Shapshak, and W. W. Tourtellotte. 1988. Early penetration of the blood-brain-barrier by HIV. Neurology 38: 9-14.
8. Appleman, M. E., D. W. Marshall, R. L. Brey, R. W. Houk, D. C. Beatty, R. E. Winn, G. P. Melcher, M. G. Wise, C. V. Sumaya, and R. N. Boswell. 1988. Cerebrospinal fluid abnormalities in patients without AIDS who are seropositive for the human immunodeficiency virus. J. Infect. Dis. 158: 193-199.
9. Poluektova, L. Y., D. H. Munn, Y. Persidsky, and H. E. Gendelman. 2002. Generation of cytotoxic T cells against virus-infected human brain macrophages in a murine model of HIV-1 encephalitis. J. Immunol. 168: 3941-3949.
10. Poluektova, L., S. Gorantla, J. Faraci, K. Birusingh, H. Dou, and H. E. Gendelman. 2004. Neuroregulatory events follow adaptive immune-mediated elimination of HIV-1-infected macrophages: studies in a murine model of viral encephalitis. J. Immunol. 172: 7610-7617.
11. Gimsa, U., S. A. Wolf, D. Haas, I. Bechmann, and R. Nitsch. 2001. Th2 cells support intrinsic anti-inflammatory properties of the brain. J. Neuroimmunol. 119: 73-80.
12. Seguin, R., K. Biernacki, A. Prat, K. Wosik, H. J. Kim, M. Blain, E. McCrea, A. Bar-Or, and J. P. Antel. 2003. Differential effects of Th1 and Th2 lymphocyte supernatants on human microglia. Glia 42: 36-45.
13. Paglinawan, R., U. Malipiero, R. Schlapbach, K. Frei, W. Reith, and A. Fontana. 2003. TGFβ directs gene expression of activated microglia to an anti-inflammatory phenotype strongly focusing on chemokine genes and cell migratory genes. Glia 44: 219-231.
14. Aharoni, R., B. Kayhan, R. Eilam, M. Sela, and R. Arnon. 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.
15. Aharoni, R., R. Arnon, and R. Eilam. 2005. Neurogenesis and neuroprotection induced by peripheral immunomodulatory treatment of experimental autoimmune encephalomyelitis. J. Neurosci. 25: 8217-8228.
16. Ziv, Y., N. Ron, O. Butovsky, G. Landa, E. Sudai, N. Greenberg, H. Cohen, J. Kipnis, and M. Schwartz. 2006. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 9: 268-275.
17. Frenkel, D., R. Maron, D. S. Burt, and H. L. Weiner. 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.
18. + T cells. Eur. J. Immunol. 34: 3434-3445.
19. Masliah, E., E. Rockenstein, A. Adame, M. Alford, L. Crews, M. Hashimoto, P. Seubert, M. Lee, J. Goldstein, T. Chilcote, et al. 2005. Effects of α-synuclein immunization in a mouse model of Parkinson's disease. Neuron 46: 857-868.
20. Arnon, R., and R. Aharoni. 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.
21. Arnon, R., and M. Sela. 2003. Immunomodulation by the copolymer glatiramer acetate. J. Mol. Recognit. 16: 412-421.
22. Kipnis, J., E. Yoles, Z. Porat, A. Cohen, F. Mor, M. Sela, I. R. Cohen, and M. Schwartz. 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.
23. Benner, E. J., R. L. Mosley, C. J. Destache, T. B. Lewis, V. Jackson-Lewis, S. Gorantla, C. Nemachek, S. R. Green, S. Przedborski, and H. E. Gendelman. 2004. Therapeutic immunization protects dopaminergic neurons in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. USA 101: 9435-9440.
24. Aharoni, R., D. Teitelbaum, M. Sela, and R. Arnon. 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.
25. Miller, A., S. Shapiro, R. Gershtein, A. Kinarty, H. Rawashdeh, S. Honigman, and N. Lahat. 1998. Treatment of multiple sclerosis with copolymer-1 (copaxone): implicating mechanisms of Th1 to Th2/Th3 immune-deviation. J. Neuroimmunol. 92: 113-121.
26. Aharoni, R., D. Teitelbaum, M. Sela, and R. Arnon. 1998. Bystander suppression of experimental autoimmune encephalomyelitis by T cell lines and clones of the Th2 type induced by copolymer 1. J. Neuroimmunol. 91: 135-146.
27. Aharoni, R., D. Teitelbaum, O. Leitner, A. Meshorer, M. Sela, and R. Arnon. 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.
28. Nitkiewicz, J., W. Chao, G. Bentsman, J. Li, S. Y. Kim, S. Y. Choi, G. Grunig, H. Gelbard, M. J. Potash, and D. J. Volsky. 2004. Productive infection of primary murine astrocytes, lymphocytes, and macrophages by human immunodeficiency virus type 1 in culture. J. Neurovirol. 10: 400-408.
29. Fouchier, R. A., B. E. Meyer, J. H. Simon, U. Fischer, and M. H. Malim. 1997. HIV-1 infection of non-dividing cells: evidence that the amino-terminal basic region of the viral matrix protein is important for Gag processing but not for post-entry nuclear import. EMBO J. 16: 4531-4539.
30. Gendelman, H. E., T. R. Moench, O. Narayan, and D. E. Griffin. 1983. Selection of a fixative for identifying T cell subsets, B cells, and macrophages in paraffinembedded mouse spleen. J. Immunol. Methods 65: 137-145.
31. Persidsky, Y., J. Limoges, R. McComb, P. Bock, T. Baldwin, W. Tyor, A. Patil, H. S. Nottet, L. Epstein, H. Gelbard, et al. 1996. Human immunodeficiency virus encephalitis in SCID mice. Am. J. Pathol. 149: 1027-1053.
32. Dou, H., J. Morehead, J. Bradley, S. Gorantla, B. Ellison, J. Kingsley, L. M. Smith, W. Chao, G. Bentsman, D. J. Volsky, and H. E. Gendelman. 2006. Neuropathologic and neuroinflammatory activities of HIV-1-infected human astrocytes in murine brain. Glia 54: 81-93.
33. Hamberger, A., Y. L. Huang, H. Zhu, F. Bao, M. Ding, K. Blennow, A. Olsson, H. A. Hansson, D. Viano, and K. G. Haglid. 2003. Redistribution of neurofilaments and accumulation of β-amyloid protein after brain injury by rotational acceleration of the head. J. Neurotrauma 20: 169-178.
34. Aharoni, R., R. Eilam, H. Domev, G. Labunskay, M. Sela, and R. Arnon. 2005. The immunomodulator glatiramer acetate augments the expression of neurotrophic factors in brains of experimental autoimmune encephalomyelitis mice. Proc. Natl. Acad. Sci. USA 102: 19045-19050.
35. Campana, D., S. Yokota, E. Coustan-Smith, T. E. Hansen-Hagge, G. Janossy, and C. R. Bartram. 1990. The detection of residual acute lymphoblastic leukemia cells with immunologic methods and polymerase chain reaction: a comparative study. Leukemia 4: 609-614.
36. Gallard, A., G. Foucras, C. Coureau, and J. C. Guery. 2002. Tracking T cell clonotypes in complex T lymphocyte populations by real-time quantitative PCR using fluorogenic complementarity-determining region-3-specific probes. J. Immunol. Methods 270: 269-280.
37. Poluektova, L., V. Meyer, L. Walters, X. Paez, and H. E. Gendelman. 2005. Macrophage-induced inflammation affects hippocampal plasticity and neuronal development in a murine model of HIV-1 encephalitis. Glia 52: 344-353.
38. Gendelman, H. E., S. Diesing, H. Gelbard, and S. Swindells. 2004. The neuropathogenesis of HIV-1 infection. In AIDS and Other Manifestations of HIV Infection, 4th Ed. G. P. Wormser, ed. Elsevier, Amsterdam, pp. 95-116.
39. Garden, G. A. 2002. Microglia in human immunodeficiency virus-associated neurodegeneration. Glia 40: 240-251.
40. Kanmogne, G. D., R. C. Kennedy, and P. Grammas. 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.
41. Aksenov, M. Y., U. Hasselrot, G. Wu, A. Nath, C. Anderson, C. F. Mactutus, and R. M. Booze. 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.
42. Smith, D. G., G. J. Guillemin, L. Pemberton, S. Kerr, A. Nath, G. A. Smythe, and B. J. Brew. 2001. Quinolinic acid is produced by macrophages stimulated by platelet activating factor, Nef and Tat. J. Neurovirol. 7: 56-60.
43. Kaul, M., and S. A. Lipton. 2005. Experimental and potential future therapeutic approaches for HIV-1 associated dementia targeting receptors for chemokines, glutamate and erythropoietin. Neurotox. Res. 8: 167-186.
44. Rostasy, K., L. Monti, S. A. Lipton, J. C. Hedreen, R. G. Gonzalez, and B. A. Navia. 2005. HIV leucoencephalopathy and TNFα expression in neurones. J. Neurol. Neurosurg. Psychiatry 76: 960-964.
45. Schifitto, G., N. Sacktor, K. Marder, M. P. McDermott, J. C. McArthur, K. Kieburtz, S. Small, and L. G. Epstein. 1999. Randomized trial of the platelet-activating factor antagonist lexipafant in HIV-associated cognitive impairment: Neurological AIDS Research Consortium. Neurology 53: 391-396.
46. Perry, S. W., J. P. Norman, and H. A. Gelbard. 2005. Adjunctive therapies for HIV-1 associated neurologic disease. Neurotox. Res. 8: 161-166.
47. Zink, M. C., J. Uhrlaub, J. DeWitt, T. Voelker, B. Bullock, J. Mankowski, P. Tarwater, J. Clements, and S. Barber. 2005. Neuroprotective and anti-human immunodeficiency virus activity of minocycline. J. Am. Med. Assoc. 293: 2003-2011.
48. Bell, J. E. 1998. The neuropathology of adult HIV infection. Rev. Neurol. 154: 816-829.
49. Budka, H. 1991. Neuropathology of human immunodeficiency virus infection. Brain Pathol. 1: 163-175.
50. Gray, F., R. Gherardi, and F. Scaravilli. 1988. The neuropathology of the acquired immune deficiency syndrome (AIDS). A review. Brain 111: 245-266.
51. Navia, B. A., and R. W. Price. 2005. An overview of the clinical and biological features of the AIDS dementia complex. In The Neurology of AIDS, 2nd Ed. H. E. Gendelman, I. Grant, I. P. Everall, S. Lipton, and S. Swindells, eds. Oxford University Press, New York.
52. Budka, H. 2005. The neuropathology of HIV-associated brain disease. In The Neurology of AIDS, 2nd Ed. H. E. Gendelman, I. Grant, I. P. Everall, S. Lipton, and S. Swindells, eds. Oxford University Press, New York.
53. Ances, B. M., and R. J. Ellis. 2007. Dementia and neurocognitive disorders due to HIV-1 infection. Semin. Neurol. 27: 86-92.
54. Villa, G., D. Monteleone, C. Marra, A. Bartoli, A. Antinori, F. Pallavicini, E. Tamburrini, and I. Izzi. 1993. Neuropsychological abnormalities in AIDS and asymptomatic HIV seropositive patients. J. Neurol. Neurosurg. Psychiatry 56: 878-884.
55. Sahakian, B. J., R. Elliott, N. Low, M. Mehta, R. T. Clark, and A. L. Pozniak. 1995. Neuropsychological deficits in tests of executive function in asymptomatic and symptomatic HIV-1 seropositive men. Psychol. Med. 25: 1233-1246.
56. Stern, Y., M. P. McDermott, S. Albert, D. Palumbo, O. A. Selnes, J. McArthur, N. Sacktor, G. Schifitto, K. Kieburtz, L. Epstein, and K. S. Marder. 2001. Factors associated with incident human immunodeficiency virus-dementia. Arch. Neurol. 58: 473-479.
57. Chang, L., T. Ernst, M. D. Witt, N. Ames, M. Gaiefsky, and E. Miller. 2002. Relationships among brain metabolites, cognitive function, and viral loads in antiretroviral-naive HIV patients. Neuroimage 17: 1638-1648.
58. + T cells in the brain correlate with early central nervous system dysfunction in simian immunodeficiency virus infection. J. Immunol. 167: 5429-5438.
59. + T cell deficits in cytokine secretion profile are dependent on monkey origin. Viral Immunol. 19: 679-689.
60. + cells in simian immunodeficiency virus infection. AIDS 17: 1605-1611.
61. + cells accumulate in the brains of acquired immunodeficiency syndrome patients with human immunodeficiency virus encephalitis. J. Neurovirol. 9: 36-44.
62. + T cells in association with central nervous system vessels and virus. J. Neurovirol. 10: 315-325.
63. + and cytotoxic T lymphocytes are associated with, and may be specific for, human immunodeficiency virus type 1 encephalitis in patients with acquired immunodeficiency syndrome. J. Neurovirol. 12: 272-283.
64. Roberts, E. S., S. Huitron-Resendiz, M. A. Taffe, M. C. Marcondes, C. T. Flynn, C. M. Lanigan, J. A. Hammond, S. R. Head, S. J. Henriksen, and H. S. Fox. 2006. Host response and dysfunction in the CNS during chronic simian immunodeficiency virus infection. J. Neurosci. 26: 4577-4585.
65. Ryan, G., T. Grimes, B. Brankin, M. J. Mabruk, M. J. Hosie, O. Jarrett, and J. J. Callanan. 2005. Neuropathology associated with feline immunodeficiency virus infection highlights prominent lymphocyte trafficking through both the blood-brain and blood-choroid plexus barriers. J. Neurovirol. 11: 337-345.
66. + lymphocytosis in HIV-1 infected patients with immune restoration induced by HAART. Acta Neuropathol. 108: 17-23.
67. Gray, F., C. Bazille, H. Adle-Biassette, J. Mikol, A. Moulignier, and F. Scaravilli. 2005. Central nervous system immune reconstitution disease in acquired immunodeficiency syndrome patients receiving highly active antiretroviral treatment. J. Neurovirol. 11 (Suppl. 3): 16-22.
68. McCrossan, M., M. Marsden, F. W. Carnie, S. Minnis, B. Hansoti, I. C. Anthony, R. P. Brettle, J. E. Bell, and P. Simmonds. 2006. An immune control model for viral replication in the CNS during presymptomatic HIV infection. Brain 129: 503-516.
69. Gendelman, H. E., I. Grant, I. P. Everall, S. Lipton, and S. Swindells. 2005. Overview: a panel discussion: critical topics in the neurology of AIDS. In The Neurology of AIDS, 2nd Ed. H. E. Gendelman, I. Grant, I. P. Everall, S. Lipton, and S. Swindells, eds. Oxford University Press, New York.
70. Gray, F., and C. Keohane. 2003. The neuropathology of HIV infection in the era of highly active antiretroviral therapy (HAART). Brain Pathol. 13: 79-83.
71. Potash, M. J., W. Chao, G. Bentsman, N. Paris, M. Saini, J. Nitkiewicz, P. Belem, L. Sharer, A. I. Brooks, and D. J. Volsky. 2005. A mouse model for study of systemic HIV-1 infection, antiviral immune responses, and neuroinvasiveness. Proc. Natl. Acad. Sci. USA 102: 3760-3765.
72. Dou, H., K. Birusingh, J. Faraci, S. Gorantla, L. Y. Poluektova, S. B. Maggirwar, S. Dewhurst, H. A. Gelbard, and H. E. Gendelman. 2003. Neuroprotective activities of sodium valproate in a murine model of human immunodeficiency virus-1 encephalitis. J. Neurosci. 23: 9162-9170.
73. Kipnis, J., H. Cohen, M. Cardon, Y. Ziv, and M. Schwartz. 2004. T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions. Proc. Natl. Acad. Sci. USA 101: 8180-8185.
74. Adorini, L. 2004. Immunotherapeutic approaches in multiple sclerosis. J. Neurol. Sci. 223: 13-24.
75. Bakalash, S., A. Kessler, T. Mizrahi, R. Nussenblatt, and M. Schwartz. 2003. Antigenic specificity of immunoprotective therapeutic vaccination for glaucoma. Invest. Ophthalmol. Visual Sci. 44: 3374-3381.
76. Angelov, D. N., S. Waibel, O. Guntinas-Lichius, M. Lenzen, W. F. Neiss, T. L. Tomov, E. Yoles, J. Kipnis, H. Schori, A. Reuter, et al. 2003. Therapeutic vaccine for acute and chronic motor neuron diseases: implications for amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA 100: 4790-4795.
77. Wiesemann, E., J. Klatt, D. Sonmez, R. Blasczyk, F. Heidenreich, and A. Windhagen. 2001. Glatiramer acetate (COP-1) induces IL-13/IL-5 secretion in naive T cells. J. Neuroimmunol. 119: 137-144.
78. Dabbert, D., S. Rosner, M. Kramer, U. Scholl, H. Tumani, M. Mader, and F. Weber. 2000. Glatiramer acetate (copolymer-1)-specific, human T cell lines: cytokine profile and suppression of T cell lines reactive against myelin basic protein. Neurosci. Lett. 289: 205-208.
79. Kipnis, J., E. Yoles, H. Schori, E. Hauben, I. Shaked, and M. Schwartz. 2001. Neuronal survival after CNS insult is determined by a genetically encoded autoimmune response. J. Neurosci. 21: 4564-4571.
80. Schori, H., E. Robenshtok, M. Schwartz, and A. Hourvitz. 2005. Post-intoxication vaccination for protection of neurons against the toxicity of nerve agents. Toxicol. Sci. 87: 163-168.
81. Teitelbaum, D., R. Aharoni, E. Klinger, R. Kreitman, E. Raymond, A. Malley, R. Shofti, M. Sela, and R. Arnon. 2004. Oral glatiramer acetate in experimental autoimmune encephalomyelitis: clinical and immunological studies. Ann. NY Acad. Sci. 1029: 239-249.
82. Teitelbaum, D., R. Arnon, and M. Sela. 1999. Immunomodulation of experimental autoimmune encephalomyelitis by oral administration of copolymer 1. Proc. Natl. Acad. Sci. USA 96: 3842-3847.
83. + regulatory T cells by copolymer-I through activation of transcription factor Foxp3. Proc. Natl. Acad. Sci. USA 102: 6449-6454.
84. + regulatory T cells in neurodegeneration: a dialogue with microglia. Proc. Natl. Acad. Sci. USA 101 (Suppl. 2): 14663-14669.
85. high T regulatory cells and their IL-10 production in multiple sclerosis. J. Neuroimmunol. 144: 125-131.
86. Monje, M. L., H. Toda, and T. D. Palmer. 2003. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765.