HIV-induced metalloproteinase processing of the chemokine stromal cell derived factor-1 causes neurodegeneration

Nature Neuroscience

Volumn 6, Issue 10, 2003, Pages 1064-1071

  Zhang, Kunyan ^a   McQuibban, G Angus ^b   Silva, Claudia ^a   Butler, Georgina S ^b   Johnston, James B ^a   Holden, Janet ^b   Clark Lewis, Ian ^b   Overall, Christopher M ^b   Power, Christopher ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; ENZYME PRECURSOR; GELATINASE A; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE INHIBITOR; NEUTRALIZING ANTIBODY; STROMAL CELL DERIVED FACTOR 1ALPHA;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; ASTROCYTE; BASAL GANGLION; CONTROLLED STUDY; CYTOKINE RELEASE; DEMENTIA; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFLAMMATION; MACROPHAGE; NERVE CELL NECROSIS; NERVE DEGENERATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING;

AIDS DEMENTIA COMPLEX; ANIMALS; ANTIBODIES; ASTROCYTES; CELL LINE; CHEMOKINES, CXC; DISEASE MODELS, ANIMAL; ENCEPHALITIS; ENZYME INHIBITORS; HIV-1; HUMANS; MACROPHAGES; MATRIX METALLOPROTEINASE 2; MICE; NEOSTRIATUM; NERVE DEGENERATION; NEUROTOXINS; PEPTIDE FRAGMENTS;

EID: 0141653868     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1127     Document Type: Article

References (47)

1. Power, C. Retroviral diseases of the nervous system: pathogenic host response or viral gene-mediated neurovirulence? Trends Neurosci. 24, 162-169 (2001).
2. Rossi, D. & Zlotnik, A. The biology of chemokines and their receptors. Annu. Rev. Immunol. 18, 217-242 (2000).
3. Ransohoff, R.M. & Tani, M. Do chemokines mediate leukocyte recruitment in post-traumatic CNS inflammation? Trends Neurosci. 21, 154-159 (1998).
4. Oberlin, E. et al. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 382, 833-835 (1996).
5. Bleul, C.C. et al. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382, 829-833 (1996).
6. Nagasawa, T., Tachibana, K. & Kawabata, K. A CXC chemokine SDF-1/PBSF: a ligand for a HIV coreceptor, CXCR4. Adv. Immunol. 71, 211-228 (1999).
7. Ohtani, Y. et al. Expression of stromal cell-derived factor-1 and CXCR4 chemokine receptor mRNAs in cultured rat glial and neuronal cells. Neurosci. Lett. 249, 163-166 (1998).
8. Asensio, V.C. & Campbell, I.L. Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci. 22, 504-512 (1999).
9. Miller, R.J. & Meucci, O. AIDS and the brain: is there a chemokine connection. Trends Neurosci. 22, 471-479 (1999).
10. Epstein, L.G. & Gendelman, H.E. Human immunodeficiency virus type 1 infection of the nervous system: pathogenetic mechanisms [see comments]. Ann. Neurol. 33, 429-436 (1993).
11. Gonzalez-Scarano, F. & Baltuch, G. Microglia as mediators of inflammatory and degenerative diseases. Annu. Rev. Neurosci. 22, 219-240 (1999).
12. Kaul, M., Garden, G.A. & Lipton, S.A. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410, 988-994 (2001).
13. Sisodia, S.S. Alzheimer's disease: perspectives for the new millennium. J. Clin. Invest. 104, 1169-1170 (1999).
14. Hook, Y.H. & Mende-Mueller, L. Proteolysis in neurodegenerative diseases, in Molecular Mechanisms of Neurodegenerative Diseases (ed. Chesselet, M.) 111-129 (Humana, Totowa, New Jersey, 2000).
15. Conant, K. et al. Cerebrospinal fluid levels of MMP-2, 7, and 9 are elevated in association with human immunodeficiency virus dementia. Ann. Neurol. 46, 391-398 (1999).
16. Johnston, J.B. et al. Lentiviral infection in the brain induce matrix metalloproteinase expression: the role of envelope diversity. J. Virol. 74, 7211-7220 (2000).
17. Yong, V.W., Power, C., Forsyth, P. & Edwards, D. Metalloproteinases in the biology and pathology of the nervous system. Nat. Rev. Neurosci. 2, 502-511 (2001).
18. Anthony, D.C. et al. Matrix metal loproteinase expression in ah an experimentally-induced DTH model of multiple sclerosis in the rat CNS. J. Neuroimmunol. 87, 62-72 (1998).
19. McCawley, L.J. & Matrisian, L.M. Matrix metalloproteinases: they're not just for matrix anymore! Curr. Opin. Cell Biol. 13, 534-540 (2001).
20. Lopez-Otin, C. & Overall, C.M. Protease degradomics: a new challenge for proteomics. Nat. Rev. Mol. Cell. Biol. 3, 509-519 (2002).
21. McQuibban, G.A. et al. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3, Science 289, 1202-1206 (2000).
22. Opdenakker, G. et al, Gelatinase B functions as regulator and effector in leukocyte biology. J. Leukoc. Biol. 69, 851-859 (2001),
23. McQuibban, G.A. et al. Matrix metalloproteinase cleavage of the chemokine stromal cell derived factor-1 results An loss of chemokine activity. J. Biol. Chem. 276, 43503-43508 (2001).
24. Lipton, S.A. & Gendelman, H.E. Seminars in medicine of the Beth Israel Hospital, Boston. Dementia associated with the acquired immunodeficiency syndrome. N. Engl. J. Med. 332, 934-940 (1995).
25. Zhang, K. et al. Human immunodeficiency virus type 1 Clade A and neurotropis: molecular evolution, recombination and co-receptor utilization. Virology 283, 19-30 (2001).
26. Power, C. et al. 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 (1998).
27. verall, C.M. & Lopez-Otin, C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat. Rev. Cancer 2, 657-672 (2002).
28. Bigg, H.F. et al. Tissue inhibitor of metalloproteinases-4 inhibits but does not support the activation of gelatinase A via efficient inhibition of membrane type 1-matrix metalloproteinase. Cancer Res. 61, 3610-3618 (2001).
29. Horuk, R. Chemokines beyond inflammation. Nature 393, 524-525 (1998).
30. Catani, M.V. et al. gp120 induces cell death in human neuroblastoma cells through the CXCR4 and CCR5 chemokine receptors. J. Neurochem, 74, 2373-2379 (2000).
31. Gong, J.H. & Clark-Lewis, I. Antagonists of monocyte hemoattractant protein 1 identified by modification of functionally critical NH2-terminal residues. J. Exp. Med. 181, 631-640 (1995).
32. Ungerstedt, U. & Arbuthnott, G.W. Quantitative recording of rotational behaviour in rats after 6-hydroxy-dopamine lesions of nigrostriatal dopamine system. Brain Res. 24, 485-493 (1970).
33. Glass, J.D., Fedor, H., Wesselingh, S.L. & McArthur, J.C. Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann. Neurol. 38, 755-762 (1995).
34. Patrick, M.K., Johnston, J.B. & Power, C. Lentiviral neuropathogenesis: comparative neuroinvasion, neurotropism, neurovirulence and host neurosusceptibility. J. Virol. 76, 7923-7931 (2002).
35. Johnston, J.B., Silva, C. & Power, C. Envelope gene-mediated neurovirulence in feline immunodeficiency virus infection induction of matrix metaloproteinases and neuronal injury. J. Virol, 76, 2622-2633 (2002).
36. Berman, N.E. et al. Microglial activation and neurological symptoms in the SIV model of NeuroAIDS: association of MHC-II and MMP-9 expression with behavioral deficits and evoked potential changes. Neurobiol. Dis. 6, 486-498 (1999).
37. Sanders, V.J. et al. Chemokines and receptors in HIV encephalitis. Aids 12, 1021-1026 (1998).
38. Kaul, M. & Lipton, S.A. Chemokines and activated macrophages in HIV gp120-induced neuronal apoptosis. Proc. Natl. Acad. Sci. USA 96, 8212-8216 (1999).
39. Shrikant, P., Benos, D.J., Tang, L.P. & Benveniste, E. N. HIV glycoprotein 120 enhances intercellular adhesion molecule-1 gene expression in glial cells. Involvement of Janus kinase/signal transducer and activator of transcription and protein kinase C signaling pathways. J. Immunol. 156, 1307-1314 (1996).
40. Nath, A. Pathobiology of human immunodeficiency virus dementia. Semin. Neurol. 19, 113-127 (1999).
41. Johnston, J.B. et al. HIV-1 Tat neurotoxicity is prevented by matrix metalloproteinase inhibitors. Ann. Neurol. 49, 230-241 (2001).
42. Langford, D., Sanders, V.J., Mallory, M., Kaul, M. & Masliah, E. Expression of stromal cell-derived factor lalpha protein in HIV encephalitis. J. Neuroimmunol. 127, 115-126 (2002).
43. Coussens, L.M., Fingleton, B. & Matrisian, L.M. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295, 2387-2392 (2002).
44. Chesebro, B. et al. Identification of human immunodeficiency virus envelope gene sequences influencing viral entry into CD4-positive HeLa cells, T-leukemia cells and macrophages. J. Virol. 65, 5782-5789 (1991).
45. Mayne, M. et al. Antisense oligodeoxynucleoide inhibition of tumor necrosis factor is neuroprotective following intracerebral hemorrhage. Stroke 32, 240-248 (2001).
46. Power, C. et al. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann. Neurol. 53, 731-742 (2003).
47. Imai, Y., Ibata, I., Ito, D., Ohsawa, K. & Kohsaka, S. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem. Biophys. Res. Commun. 224, 855-862 (1996).