Absence of functional alternative complement pathway alleviates lupus cerebritis

European Journal of Immunology

Volumn 37, Issue 6, 2007, Pages 1691-1701

  Alexander, Jessy J ^a   Jacob, Alexander ^a   Vezina, Paul ^a   Sekine, Hideharu ^b   Gilkeson, Gary S ^b   Quigg, Richard J ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Apoptosis; Brain; Complement factor B; Extracellular matrix; MRL lpr mice

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; CASPASE 3; COLLAGEN TYPE 4; COMPLEMENT COMPONENT C3; FIBRONECTIN; IMMUNOGLOBULIN G; LAMININ; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; COMPLEMENT ACTIVATION; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT SYSTEM; CONTROLLED STUDY; DISEASE COURSE; ENCEPHALITIS; ENZYME ACTIVITY; IMMUNOPATHOGENESIS; MOUSE; NEUROPROTECTION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN TARGETING; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIGEN-ANTIBODY COMPLEX; APOPTOSIS; BEHAVIOR, ANIMAL; BRAIN; BRAIN CHEMISTRY; CASPASE 3; CEREBRAL CORTEX; COMPLEMENT C3; COMPLEMENT C3D; COMPLEMENT FACTOR B; COMPLEMENT PATHWAY, ALTERNATIVE; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOGLOBULIN G; LUPUS VASCULITIS, CENTRAL NERVOUS SYSTEM; MICE; MICE, INBRED MRL LPR; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 34250635913     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200636638     Document Type: Article

References (56)

1. Pickering, M. C., Botto, M., Taylor, P. R., Lachmann, P. J. and Walport, M. J., Systemic lupus erythematosus, complement deficiency, and apoptosis. Adv. Immunol. 2000. 76: 227-324.
2. Jongen, P. J., Doesburg, W. H., Ibrahim-Stappers, J. L., Lemmens, W. A., Hommes, O. R. and Lamers, K. J., Cerebrospinal fluid C3 and C4 indexes in immunological disorders of the central nervous system. Acta Neurol. Scand. 2000. 101: 116-121.
3. Hopkins, P., Belmont, H. M., Buyon, J., Philips, M., Weissmann, G. and Abramson, S. B., Increased levels of plasma anaphylatoxins in systemic lupus erythematosus predict flares of the disease and may elicit vascular injury in lupus cerebritis. Arthritis Rheum. 1988. 31: 632-641.
4. Alexander, J. J., Bao, L., Jacob, A., Kraus, D. M., Holers, V. M. and Quigg, R. J., Administration of the soluble complement inhibitor, Crry-Ig, reduces inflammation and aquaporin 4 expression in lupus cerebritis. Biochim. Biophys. Acta 2003. 1639: 169-176.
5. Alexander, J. J., Jacob, A., Bao, L., MacDonald, R. L. and Quigg, R. J., Complement-dependent apoptosis and inflammatory gene changes in murine lupus cerebritis. J. Immunol. 2005. 175: 8312-8319.
6. Segurado, O. G., Gomez-Reino, J. and Arnaiz-Villena, A., Factor B activation in systemic lupus erythematosus. Arthritis Rheum. 1990. 33: 1598-1599.
7. Watanabe, H., Garnier, G., Circolo, A., Wetsel, R. A., Ruiz, P., Holers, V. M., Boackle, S. A. et al., Modulation of renal disease in MRL/lpr mice genetically deficient in the alternative complement pathway factor B. J. Immunol. 2000. 164: 786-794.
8. Passwell, J., Schreiner, G. F., Nonaka, M., Beuscher, H. U. and Colten, H. R., Local extrahepatic expression of complement genes C3, factor B, C2, and C4 is increased in murine lupus nephritis. J. Clin. Invest. 1988. 82: 1676-1684.
9. Passwell, J. H., Schreiner, G. F., Wetsel, R. A. and Colten, H. R., Complement gene expression in hepatic and extrahepatic tissues of NZB and NZB x W (F1) mouse strains. Immunology 1990. 71: 290-294.
10. Takahashi, M., Takahashi, S. and Hirose, S., Solubilization of antigen-antibody complexes: A new function of complement as a regulator of immune reactions. Prog. Allergy 1980. 27: 134-166.
11. Peters, M. G., Ambrus, J. L., Jr., Fauci, A. S. and Brown, E. J., The Bb fragment of complement factor B acts as a B cell growth factor. J. Exp. Med. 1988. 168: 1225-1235.
12. Hall, R. E., Blaese, R. M., Davis, A. E., III, Decker, J. M., Tack B. F., Colten, H. R. and Muchmore, A. V., Cooperative interaction of factor B and other complement components with mononuclear cells in the antibody-independent lysis of xenogeneic erythrocytes. J. Exp. Med. 1982. 156: 834-843.
13. Thomas, A., Gasque, P., Vaudry, D., Gonzalez, B. and Fontaine, M., Expression of a complete and functional complement system by human neuronal cells in vitro. Int. Immunol. 2000. 12: 1015-1023.
14. Adam, C., Thoua, Y., Ronco, P., Verroust P., Tovey, M. and Morel-Maroger, L., The effect of exogenous interferon: Acceleration of autoimmune and renal diseases in (NZB/W) F1 mice. Clin. Exp. Immunol. 1980. 40: 373-382.
15. Falus, A., Beuscher, H. U., Auerbach, H. S. and Coften, H. R., Constitutive and IL 1-regulated murine complement gene expression is strain and tissue specific. J. Immunol. 1987. 138: 856-860.
16. Thurman, J. M., Ljubanovic, D., Edelstein, C. L., Gilkeson, G. S. and Holers, V. M., Lack of a functional alternative complement pathway ameliorates ischemic acute renal failure in mice. J. Immunol. 2003. 170: 1517-1523.
17. Uwai, M., Terui, Y., Mishima, Y., Tomizuka, H., Ikeda, M., Itoh, T., Mori, M., Ueda, M. et al., A new apoptotic pathway for the complement factor B-derived fragment Bb. J. Cell. Physiol. 2000. 185: 280-292.
18. Sakic, B., Maric, I., Koeberle, P. D., Millward, J. M., Szechtman, H., Maric, D. and Denburg, J. A., Increased TUNEL staining in brains of autoimmune Fas-deficient mice. J. Neuroimmunol. 2000. 104: 147-154.
19. Mahler, M., Ben-Ari, Y. and Represa, A., Differential expression of fibronectin, tenascin-C and NCAMs in cultured hippocampal astrocytes activated by kainate, bacterial lipopolysaccharide or basic fibroblast growth factor. Brain Res. 1997. 775: 63-73.
20. Fawcett, J. W. and Asher, R. A., The glial scar and central nervous system repair. Brain Res. Bull. 1999. 49: 377-391.
21. Vosko, M. R., Rother, J., Friedl, B., Bultemeier, G., Kloss, C. U. and Hamann, G. F., Microvascular damage following experimental sinus-vein thrombosis in rats. Acta Neuropathol. 2003. 106: 501-505.
22. Morales-Ruiz, M., Fulton, D., Sowa, G., Languino, L. R., Fujio, Y., Walsh, K. and Sessa, W. C., Vascular endothelial growth factor-stimulated actin reorganization and migration of endothelial cells is regulated via the serine/threonine kinase Akt. Circ. Res. 2000. 86: 892-896.
23. Fujio, Y. and Walsh, K., Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J. Biol. Chem. 1999. 274: 16349-16354.
24. Gary, D. S. and Mattson, M. P., PTEN regulates Akt kinase activity in hippocampal neurons and increases their sensitivity to glutamate and apoptosis. Neuromol. Med. 2002. 2: 261-269.
25. Sakic, B., Szechtman, H. and Denburg, J. A., Neurobehavioral alterations in autoimmune mice. Neurosci. Biobehav. Rev. 1997. 21: 327-340.
26. Diamond, B. and Volpe, B., On the track of neuropsychiatric lupus. Arthritis Rheum. 2003. 48: 2710-2712.
27. Kowal, C., Degiorgio, L. A., Nakaoka, T., Hetherington, H., Huerta, P. T., Diamond, B. and Volpe, B. T., Cognition and immunity; antibody impairs memory. Immunity 2004. 21: 179-188.
28. Adachi, M., Watanabe-Fukunaga, R. and Nagata, S., Aberrant transcription caused by the insertion of an early transposable element in an intron of the Fas antigen gene of lpr mice. Proc. Natl. Acad. Sci. USA 1993. 90: 1756-1760.
29. Theofilopoulos, A. N. and Dixon, F. J., Murine models of systemic lupus erythematosus. Adv. Immunol. 1985. 37: 269-390.
30. Matsumoto, M., Fukuda, W., Circolo, A., Goellner, J., Strauss-Schoenberger, J., Wang, X., Fujita, S. et al., Abrogation of the alternative complement pathway by targeted deletion of murine factor B. Proc. Natl. Acad. Sci. USA 1997. 94: 8720-8725.
31. Sekine, H., Graham, K. L., Zhao, S., Elliott, M. K., Ruiz, P., Utz, P. J. and Gilkeson, G. S., Role of MHC-linked genes in autoantigen selection and renal disease in a murine model of systemic lupus erythematosus. J. Immunol. 2006. 177: 7423-7434.
32. James, W. G., Hutchinson, P., Bullard, D. C. and Hickey, M. J., Cerebral leucocyte infiltration in lupus-prone MRL/MpJ-fas lpr mice - roles of intercellular adhesion molecule-1 and P-selectin. Clin. Exp. Immunol. 2006. 144: 299-308.
33. Heneka, M. T., Loschmann, P. A., Gleichmann, M., Weller, M., Schulz, J. B., Wullner, U. and Klockgether, T., Induction of nitric oxide synthase and nitric oxide-mediated apoptosis in neuronal PC12 cells after stimulation with tumor necrosis factor-alpha/lipopolysaccharide. J. Neurochem. 1998. 71: 88-94.
34. Leist, M., Volbracht, C., Kuhnle, S., Fava, E., Ferrando-May, E. and Nicotera, P., Caspase-mediated apoptosis in neuronal excitotoxicity triggered by nitric oxide. Mol. Med. 1997. 3: 750-764.
35. Sobel, R. A. and Mitchell, M. E., Fibronectin in multiple sclerosis lesions. Am. J. Pathol. 1989. 135: 161-168.
36. Robson, M. G. and Walport, M. J., Pathogenesis of systemic lupus erythematosus (SLE). Clin. Exp. Allergy 2001. 31: 678-685.
37. Zameer, A. and Hoffman, S. A., Increased ICAM-1 and VCAM-1 expression in the brains of autoimmune mice. J. Neuroimmunol. 2003. 142: 67-74.
38. Abbott, N. J., Mendonca, L. L. and Dolman, D. E., The blood-brain barrier in systemic lupus erythematosus. Lupus 2003. 12: 908-915.
39. Napirei, M., Karsunky, H., Zevnik, B., Stephan, H., Mannherz, H. G. and Moroy, T., Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 2000. 25: 177-181.
40. Rabchevsky, A. G., Degos, J. D. and Dreyfus, P. A., Peripheral injections of Freund's adjuvant in mice provoke leakage of serum proteins through the blood-brain barrier without inducing reactive gliosis. Brain Res. 1999. 832: 84-96.
41. Degiorgio, L. A., Konstantinov, K. N., Lee, S. C., Hardin, J. A., Volpe, B. T. and Diamond, B., A subset of lupus anti-DNA antibodies cross-reacts with the NR2 glutamate receptor in systemic lupus erythematosus. Nat. Med. 2001. 7: 1189-1193.
42. 14C-labeled cells during acute, chronic, and relapsing experimental allergic encephalomyelitis. Lab. Invest. 1990. 63: 162-170.
43. Raine, C. S., Cannella, B., Duijvestijn, A. M. and Cross, A. H., Horning to central nervous system vasculature by antigen-specific lymphocytes. II. Lymphocyte/endothelial cell adhesion during the initial stages of autoimmune demyelination. Lab. Invest. 1990. 63: 476-489.
44. Bohatschek, M., Werner, A. and Raivich, G., Systemic LPS injection leads to granulocyte influx into normal and injured brain: Effects of ICAM-1 deficiency. Exp. Neurol. 2001. 172: 137-152.
45. Raivich, G., Bohatschek, M., Werner, A., Jones, L. L., Galiano, M., Kloss, C. U., Zhu, X. Z. et al., Lymphocyte infiltration in the injured brain: Role of proinflammatory cytokines. J. Neurosci. Res. 2003. 72: 726-733.
46. Zaccagni, H., Fried, J., Cornell, J., Padilla, P. and Brey, R. L., Soluble adhesion molecule levels, neuropsychiatric lupus and lupus-related damage. Front. Biosci. 2004. 9: 1654-1659.
47. Brey, R. L., Amato, A. A., Kagan-Hallet, K., Rhine, C. B. and Stallworth, C. L., Anti-intercellular adhesion molecule-1 (ICAM-1) antibody treatment prevents central and peripheral nervous system disease in autoimmune-prone mice. Lupus 1997. 6: 645-651.
48. Scheid, M. P. and Woodgett, J. R., PKB/AKT: Functional insights from genetic models. Nat. Rev. Mol. Cell Biol. 2001. 2: 760-768.
49. Scheid, M. P. and Woodgett, J. R., Unravelling the activation mechanisms of protein kinase B/Akt. FEBS Lett. 2003. 546: 108-112.
50. Sulis, M. L. and Parsons, R., PTEN: From pathology to biology. Trends Cell Biol. 2003. 13: 478-483.
51. Sofroniew, M. V., Reactive astrocytes in neural repair and protection. Neuroscientist 2005. 11: 400-407.
52. Wright, J. W., Kramar, E. A., Meighan, S. E. and Harding, J. W., Extracellular matrix molecules, long-term potentiation, memory consolidation and the brain angiotensin system. Peptides 2002. 23: 221-246.
53. Chintala, S. K., Sawaya, R., Gokaslan, Z. L., Fuller, G. and Rao, J. S., Immunohistochemical localization of extracellular matrix proteins in human glioma, both in vivo and in vitro. Cancer Lett. 1996. 101: 107-114.
54. Sobel, R. A. and Mitchell, M. E., Fibronectin in multiple sclerosis lesions. Am. J. Pathol. 1989. 135: 161-168.
55. Sakic, B., Hanna, S. E. and Millward, J. M., Behavioral heterogeneity in an animal model of neuropsychiatric lupus. Biol. Psychiatry 2005, 57: 679-687.
56. Zalcman, S. S., Interleukin-2-induced increases in climbing behavior: Inhibition by dopamine D-1 and D-2 receptor antagonists. Brain Res. 2002. 944: 157-164.