Regulation of lentivirus neurovirulence by lipopolysaccharide conditioning: Suppression of CXCL10 in the brain by IL-10

Journal of Immunology

Volumn 184, Issue 3, 2010, Pages 1566-1574

  Maingat, Ferdinand ^a   Viappiani, Serena ^a   Zhu, Yu ^a   Vivithanaporn, Pornpun ^a,d   Ellestad, Kristofor K ^a   Holden, Janet ^c   Silva, Claudia ^c   Power, Christopher ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c ST PAUL S HOSPITAL   (Canada)

^d MAHIDOL UNIVERSITY   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANZYME A; LIPOPOLYSACCHARIDE; RECOMBINANT INTERLEUKIN 10; INTERLEUKIN 10; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; COGNITION; CONTROLLED STUDY; FELINE IMMUNODEFICIENCY VIRUS; GENE EXPRESSION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; INNATE IMMUNITY; LENTIVIRINAE; LENTIVIRUS INFECTION; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MONOCYTE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SUPERNATANT; T LYMPHOCYTE; VIRUS CELL INTERACTION; VIRUS LOAD; VIRUS VIRULENCE; ANIMAL; CAT; CELL CULTURE; CELL MOTION; DRUG ANTAGONISM; GROWTH, DEVELOPMENT AND AGING; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; VIROLOGY; VIRULENCE;

ANIMALS; BRAIN; CATS; CELL LINE, TUMOR; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CXCL10; HIV INFECTIONS; HIV-1; HUMANS; IMMUNODEFICIENCY VIRUS, FELINE; INTERLEUKIN-10; LENTIVIRUS INFECTIONS; LIPOPOLYSACCHARIDES; NEURONS; NEUROPROTECTIVE AGENTS; VIRAL LOAD; VIRULENCE;

EID: 77949327634     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902575     Document Type: Article

References (66)

1. Patrick, M. K., J. B. Johnston, and C. Power. 2002. Lentiviral neuropathogenesis: comparative neuroinvasion, neurotropism, neurovirulence, and host neurosusceptibility. J. Virol. 76: 7923-7931.
2. González-Scarano, F., and J. Martín-García. 2005. The neuropathogenesis of AIDS. Nat. Rev. Immunol. 5: 69-81.
3. McArthur, J. C., B. J. Brew, and A. Nath. 2005. Neurological complications of HIV infection. Lancet Neurol. 4: 543-555.
4. Jones, G., and C. Power. 2006. Regulation of neural cell survival by HIV-1 infection. Neurobiol. Dis. 21: 1-17.
5. Li, M., and R. M. Ransohoff. 2008. Multiple roles of chemokine CXCL12 in the central nervous system: a migration from immunology to neurobiology. Prog. Neurobiol. 84: 116-131.
6. Kaul, M., and S. A. Lipton. 2006. Mechanisms of neuroimmunity and neurodegeneration associated with HIV-1 infection and AIDS. J. Neuroimmune Pharmacol. 1: 138-151. (Pubitemid 44257489)
7. Dhillon, N. K., F. Peng, R. M. Ransohoff, and S. Buch. 2007. PDGF synergistically enhances IFN-γ-induced expression of CXCL10 in blood-derived macrophages: implications for HIV dementia. J. Immunol. 179: 2722-2730.
8. Sui, Y., L. Stehno-Bittel, S. Li, R. Loganathan, N. K. Dhillon, D. Pinson, A. Nath, D. Kolson, O. Narayan, and S. Buch. 2006. CXCL10-induced cell death in neurons: role of calcium dysregulation. Eur. J. Pharmacol. 23: 957-964.
9. Vergote, D., G. S. Butler, M. Ooms, J. H. Cox, C. Silva, M. D. Hollenberg, J. H. Jhamandas, C. M. Overall, and C. Power. 2006. Proteolytic processing of SDF-1alpha reveals a change in receptor specificity mediating HIV-associated neurodegeneration. Proc. Natl. Acad. Sci. U.S.A. 103: 19182-19187.
10. Lackner, A. A., M. Mohan, and R. S. Veazey. 2009. The gastrointestinal tract and AIDS pathogenesis. Gastroenterology 136: 1965-1978.
11. Douek, D. 2007. HIV disease progression: immune activation, microbes, and a leaky gut. Top. HIV Med. 15: 114-117.
12. Brenchley, J. M., D. A. Price, T. W. Schacker, T. E. Asher, G. Silvestri, S. Rao, Z. Kazzaz, E. Bornstein, O. Lambotte, D. Altmann, et al. 2006. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12: 1365-1371.
13. Hofer, U., and R. F. Speck. 2009. Disturbance of the gut-associated lymphoid tissue is associated with disease progression in chronic HIV infection. Semin. Immunopathol. 31: 257-266.
14. Ancuta, P., A. Kamat, K. J. Kunstman, E. Y. Kim, P. Autissier, A. Wurcel, T. Zaman, D. Stone, M. Mefford, S. Morgello, et al. 2008. Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS One 3: e2516.
15. Ellestad, K. K., S. Tsutsui, F. Noorbakhsh, K. G. Warren, V. W. Yong, Q. J. Pittman, and C. Power. 2009. Early life exposure to lipopolysaccharide suppresses experimental autoimmune encephalomyelitis by promoting tolerogenic dendritic cells and regulatory T cells. J. Immunol. 183: 298-309.
16. Correale, J., and M. Farez. 2007. Association between parasite infection and immune responses in multiple sclerosis. Ann. Neurol. 61: 97-108.
17. Block, M. L., and J. S. Hong. 2005. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 76: 77-98.
18. Perry, V. H., C. Cunningham, and C. Holmes. 2007. Systemic infections and inflammation affect chronic neurodegeneration. Nat. Rev. Immunol. 7: 161-167.
19. Minghetti, L., M. A. Ajmone-Cat, M. A. De Berardinis, and R. De Simone. 2005. Microglial activation in chronic neurodegenerative diseases: roles of apoptotic neurons and chronic stimulation. Brain Res. Brain Res. Rev. 48: 251-256.
20. Masur, H., and J. Kaplan. 2001. Current status of opportunistic infections in patients with HIV infection in the era of highly active antiretroviral therapy. Curr. Clin. Top. Infect. Dis. 21: 64-82.
21. Zhu, Y., D. Vergote, C. Pardo, F. Noorbakhsh, J. C. McArthur, M. D. Hollenberg, C. M. Overall, and C. Power. 2009. CXCR3 activation by lentivirus infection suppresses neuronal autophagy: neuroprotective effects of antiretroviral therapy. FASEB J. 23: 2928-2941.
22. Power, C., R. Buist, J. B. Johnston, M. R. Del Bigio, W. Ni, M. R. Dawood, and J. Peeling. 1998. Neurovirulence in feline immunodeficiency virus-infected neonatal cats is viral strain specific and dependent on systemic immune suppression. J. Virol. 72: 9109-9115. (Pubitemid 28471855)
23. Power, C., J. C. McArthur, A. Nath, K. Wehrly, M. Mayne, J. Nishio, T. Langelier, R. T. Johnson, and B. Chesebro. 1998. Neuronal death induced by brain-derived human immunodeficiency virus type 1 envelope genes differs between demented and nondemented AIDS patients. J. Virol. 72: 9045-9053. (Pubitemid 28471848)
24. Noorbakhsh, F., N. Vergnolle, J. C. McArthur, C. Silva, M. Vodjgani, P. Andrade-Gordon, M. D. Hollenberg, and C. Power. 2005. Proteinase-activated receptor-2 induction by neuroinflammation prevents neuronal death during HIV infection. J. Immunol. 174: 7320-7329. (Pubitemid 40705702)
25. Johnston, J. B., C. Silva, T. Hiebert, R. Buist, M. R. Dawood, J. Peeling, and C. Power. 2002. Neurovirulence depends on virus input titer in brain in feline immunodeficiency virus infection: evidence for activation of innate immunity and neuronal injury. J. Neurovirol. 8: 420-431.
26. van Marle, G., J. M. Antony, C. Silva, A. Sullivan, and C. Power. 2005. Aberrant cortical neurogenesis in a pediatric neuroAIDS model: neurotrophic effects of growth hormone. AIDS 19: 1781-1791.
27. Zhu, Y., G. Jones, S. Tsutsui, W. Opii, S. Liu, C. Silva, D. A. Butterfield, and C. Power. 2005. Lentivirus infection causes neuroinflammation and neuronal injury in dorsal root ganglia: pathogenic effects of STAT-1 and inducible nitric oxide synthase. J. Immunol. 175: 1118-1126. (Pubitemid 41094998)
28. Kennedy, J. M., A. Hoke, Y. Zhu, J. B. Johnston, G. van Marle, C. Silva, D. W. Zochodne, and C. Power. 2004. Peripheral neuropathy in lentivirus infection: evidence of inflammation and axonal injury. AIDS 18: 1241-1250.
29. Boven, L. A., F. Noorbakhsh, G. Bouma, R. van der Zee, D. L. Vargas, C. Pardo, J. C. McArthur, H. S. L. M. Nottet, and C. Power. 2007. Brain-derived human immunodeficiency virus-1 Tat exerts differential effects on LTR transactivation and neuroimmune activation. J. Neurovirol. 13: 173-184.
30. Power, C., S. Henry, M. R. Del Bigio, P. H. Larsen, D. Corbett, Y. Imai, V. W. Yong, and J. Peeling. 2003. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann. Neurol. 53: 731-742.
31. Afkhami-Goli, A., F. Noorbakhsh, A. J. Keller, N. Vergnolle, D. Westaway, J. H. Jhamandas, P. Andrade-Gordon, M. D. Hollenberg, H. Arab, R. H. Dyck, and C. Power. 2007. Proteinase-activated receptor-2 exerts protective and pathogenic cell type-specific effects in Alzheimer's disease. J. Immunol. 179: 5493-5503.
32. Johnston, J., and C. Power. 1999. Productive infection of human peripheral blood mononuclear cells by feline immunodeficiency virus: implications for vector development. J. Virol. 73: 2491-2498. (Pubitemid 29098156)
33. Tsutsui, S., D. Vergote, N. Shariat, K. Warren, S. S. Ferguson, and C. Power. 2008. Glucocorticoids regulate innate immunity in a model of multiple sclerosis: reciprocal interactions between the A1 adenosine receptor and β-arrestin-1 in monocytoid cells. FASEB J. 22: 786-796.
34. Navia, B. A., E. S. Cho, C. K. Petito, and R. W. Price. 1986. The AIDS dementia complex: II. Neuropathology. Ann. Neurol. 19: 525-535.
35. Petito, C. K., B. Adkins, M. McCarthy, B. Roberts, and I. Khamis. 2003. CD4+ and CD8+ cells accumulate in the brains of acquired immunodeficiency syndrome patients with human immunodeficiency virus encephalitis. J. Neurovirol. 9: 36-44.
36. van Marle, G., S. Henry, T. Todoruk, A. Sullivan, C. Silva, S. B. Rourke, J. Holden, J. C. McArthur, M. J. Gill, and C. Power. 2004. Human immunodeficiency virus type 1 Nef protein mediates neural cell death: a neurotoxic role for IP-10. Virology 329: 302-318.
37. Guha, M., and N. Mackman. 2001. LPS induction of gene expression in human monocytes. Cell. Signal. 13: 85-94.
38. Maingat, F., P. Vivithanaporn, Y. Zhu, A. Taylor, G. Baker, K. Pearson, and C. Power. 2009. Neurobehavioral performance in feline immunodeficiency virus infection: integrated analysis of viral burden, neuroinflammation, and neuronal injury in cortex. J. Neurosci. 29: 8429-8437.
39. Elder, J. H., M. Sundstrom, S. de Rozieres, A. de Parseval, C. K. Grant, and Y. C. Lin. 2008. Molecular mechanisms of FIV infection. Vet. Immunol. Immunopathol. 123: 3-13.
40. Power, C., T. Moench, J. Peeling, P. A. Kong, and T. Langelier. 1997. Feline immunodeficiency virus causes increased glutamate levels and neuronal loss in brain. Neuroscience 77: 1175-1185.
41. Poli, A., M. Pistello, M. A. Carli, F. Abramo, G. Mancuso, E. Nicoletti, and M. Bendinelli. 1999. Tumor necrosis factor-α and virus expression in the central nervous system of cats infected with feline immunodeficiency virus. J. Neurovirol. 5: 465-473.
42. Zink, M. C., V. A. Laast, K. L. Helke, A. K. Brice, S. A. Barber, J. E. Clements, and J. L. Mankowski. 2006. From mice to macaques - animal models of HIV nervous system disease. Curr. HIV Res. 4: 293-305.
43. Miller, R. J., W. Rostene, E. Apartis, G. Banisadr, K. Biber, E. D. Milligan, F. A. White, and J. Zhang. 2008. Chemokine action in the nervous system. J. Neurosci. 28: 11792-11795.
44. Chaitanya, G. V., M. Kolli, and P. P. Babu. 2009. Granzyme-b mediated cell death in the spinal cord-injured rat model. Neuropathology 29: 270-279.
45. Huang, X., A. D. Reynolds, R. L. Mosley, and H. E. Gendelman. 2009. CD 4+ T cells in the pathobiology of neurodegenerative disorders. J. Neuroimmunol. 211: 3-15.
46. Napoli, I., and H. Neumann. 2009. Microglial clearance function in health and disease. Neuroscience 158: 1030-1038.
47. Mandl, J. N., A. P. Barry, T. H. Vanderford, N. Kozyr, R. Chavan, S. Klucking, F. J. Barrat, R. L. Coffman, S. I. Staprans, and M. B. Feinberg. 2008. Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat. Med. 14: 1077-1087.
48. Rho, M. B., S Wesselingh, J. D. Glass, J. C. McArthur, S. Choi, J. Griffin, and W. R. Tyor. 1995. A potential role for interferon-alpha in the pathogenesis of HIV-associated dementia. Brain Behav. Immun. 9: 366-377.
49. Westmoreland, S. V., D. Kolson, and F. González-Scarano. 1996. Toxicity of TNF α and platelet activating factor for human NT2N neurons: a tissue culture model for human immunodeficiency virus dementia. J. Neurovirol. 2: 118-126.
50. Li, B., Y. S. Guo, M. M. Sun, H. Dong, S. Y. Wu, D. X. Wu, and C. Y. Li. 2008. The NADPH oxidase is involved in lipopolysaccharide-mediated motor neuron injury. Brain Res. 1226: 199-208.
51. Lin, H. Y., C. C. Huang, and K. F. Chang. 2009. Lipopolysaccharide preconditioning reduces neuroinflammation against hypoxic ischemia and provides long-term outcome of neuroprotection in neonatal rat. Pediatr. Res. 66: 254-259.
52. Ikeda, T., L. Yang, T. Ikenoue, C. Mallard, and H. Hagberg. 2006. Endotoxin-induced hypoxic-ischemic tolerance is mediated by up-regulation of corticosterone in neonatal rat. Pediatr. Res. 59: 56-60.
53. Stevens, S. L., T. M. Ciesielski, B. J. Marsh, T. Yang, D. S. Homen, J. L. Boule, N. S. Lessov, R. P. Simon, and M. P. Stenzel-Poore. 2008. Toll-like receptor 9: a new target of ischemic preconditioning in the brain. J. Cereb. Blood Flow Metab. 28: 1040-1047.
54. Pytel, P., and J. J. Alexander. 2009. Pathogenesis of septic encephalopathy. Curr. Opin. Neurol. 22: 283-287.
55. Katsikis, P. D., S. B. Cohen, M. Londei, and M. Feldmann. 1995. Are CD4+ Th1 cells pro-inflammatory or anti-inflammatory? The ratio of IL-10 to IFN-γ or IL-2 determines their function. Int. Immunol. 7: 1287-1294.
56. Hamilton, T. A., Y. Ohmori, J. M. Tebo, and R. Kishore. 1999. Regulation of macrophage gene expression by pro- and anti-inflammatory cytokines. Pathobiology 67: 241-244.
57. Ajmone-Cat, M. A., A. Nicolini, and L. Minghetti. 2003. Prolonged exposure of microglia to lipopolysaccharide modifies the intracellular signaling pathways and selectively promotes prostaglandin E2 synthesis. J. Neurochem. 87: 1193-1203.
58. Mosser, D. M., and X. Zhang. 2008. Interleukin-10: new perspectives on an old cytokine. Immunol. Rev. 226: 205-218.
59. Adler, M. W., and T. J. Rogers. 2005. Are chemokines the third major system in the brain? J. Leukoc. Biol. 78: 1204-1209.
60. Foley, J. F., C. R. Yu, R. Solow, M. Yacobucci, K. W. Peden, and J. M. Farber. 2005. Roles for CXC chemokine ligands 10 and 11 in recruiting CD4+ T cells to HIV-1-infected monocyte-derived macrophages, dendritic cells, and lymph nodes. J. Immunol. 174: 4892-4900.
61. Biber, K., I. Dijkstra, C. Trebst, C. J. De Groot, R. M. Ransohoff, and H. W. Boddeke. 2002. Functional expression of CXCR3 in cultured mouse and human astrocytes and microglia. Neuroscience 112: 487-497.
62. Gonzalez, P., F. Burgaya, L. Acarin, H. Peluffo, B. Castellano, and B. Gonzalez. 2009. Interleukin-10 and interleukin-10 receptor-I are upregulated in glial cells after an excitotoxic injury to the postnatal rat brain. J. Neuropathol. Exp. Neurol. 68: 391-403.
63. Zhou, Z., X. Peng, R. Insolera, D. J. Fink, and M. Mata. 2009. Interleukin-10 provides direct trophic support to neurons. J. Neurochem. 110: 1617-1627.
64. McGuckin, M. A., R. Eri, L. A. Simms, T. H. Florin, and G. Radford-Smith. 2009. Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm. Bowel Dis. 15: 100-113.
65. Johansson, J. E., and T. Ekman. 2007. Gut toxicity during hemopoietic stem cell transplantation may predict acute graft-versus-host disease severity in patients. Dig. Dis. Sci. 52: 2340-2345.
66. Radhakrishnan, K., and S. G. Rockson. 2008. The clinical spectrum of lymphatic disease. Ann. N. Y. Acad. Sci. 1131: 155-184.