Complement-dependent apoptosis and inflammatory gene changes in murine lupus cerebritis

Journal of Immunology

Volumn 175, Issue 12, 2005, Pages 8312-8319

  Alexander, Jessy J ^a   Jacob, Alexander ^a   Bao, Lihua ^a   Macdonald, R Loch ^a   Quigg, Richard J ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CLASSICAL COMPLEMENT PATHWAY C3 C5 CONVERTASE; CRRY IMMUNOGLOBULIN; DNA; ENZYME INHIBITOR; GLUTAMATE RECEPTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DNA MICROARRAY; ENCEPHALITIS; GENE OVEREXPRESSION; INFLAMMATION; LUPUS ERYTHEMATOSUS; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; TRANSGENE; VALIDATION PROCESS;

EID: 29144480517     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.12.8312     Document Type: Article

References (60)

1. Brey, R. L., B. Sakic, H. Szechtman, and J. A. Denburg. 1997. Animal models for nervous system disease in systemic lupus erythematosus. Ann. NY Acad. Sci. 823: 97-106.
2. Scolding, N. J., and F. G. Joseph. 2002. The neuropathology and pathogenesis of systemic lupus erythematosus. Neuropathol. Appl. Neurobiol. 28: 173-189.
3. Nataf, S., P. F. Stahel, N. Davoust, and S. R. Barnum. 1999. Complement anaphylatoxin receptors on neurons: new tricks for old receptors? Trends Neurosci. 22: 397-402.
4. Jagels, M. A., P. J. Daffern, and T. E. Hugli. 2000. C3a and C5a enhance granulocyte adhesion to endothelial and epithelial cell monolayers: epithelial and endothelial priming is required for C3a-induced eosinophil adhesion. Immunopharmacology 46: 209-222.
5. Nicholson-Weller, A., and J. A. Halperin. 1993. Membrane signaling by complement C5b-9, the membrane attack complex. Immunol. Res. 12: 244-257.
6. Xiong, Z. Q., W. Qian, K. Suzuki, and J. O. McNamara. 2003. Formation of complement membrane attack complex in mammalian cerebral cortex evokes seizures and neurodegeneration. J. Neurosci. 23: 955-960.
7. Liszewski, M. K., and J. P. Atkinson. 1993. The complement system. In Fundamental Immunology. W. E. Paul, ed. Raven Press, New York, pp. 917-939.
8. Foley, S., B. Li, M. Dehoff, H. Molina, and V. M. Holers. 1993. Mouse Crry/p65 is a regulator of the alternative pathway of complement activation. Eur. J. Immunol. 23: 1381-1384.
9. Kim, Y. U., T. Kinoshita, H. Molina, D. Hourcade, T. Seya, L. M. Wagner, and V. M. Holers. 1995. Mouse complement regulatory protein Crry/p65 uses the specific mechanisms of both human decay-accelerating factor and membrane cofactor protein. J. Exp. Med. 181: 151-159.
10. Jongen, P. J., W. H. Doesburg, J. L. Ibrahim-Stappers, W. A. Lemmens, O. R. Hommes, and K. J. Lamers. 2000. Cerebrospinal fluid C3 and C4 indexes in immunological disorders of the central nervous system. Acta Neurol. Scand. 101: 116-121.
11. Jongen, P. J., A. M. Boerbooms, K. J. Lamers, B. C. Raes, and G. Vierwinden. 1990. Diffuse CNS involvement in systemic lupus erythematosus: intrathecal synthesis of the 4th component of complement. Neurology 40: 1593-1596.
12. Hopkins, P., H. M. Belmont, J. Buyon, M. Philips, G. Weissmann, and S. B. Abramson. 1988. Increased levels of plasma anaphylatoxins in systemic lupus erythematosus predict flares of the disease and may elicit vascular injury in lupus cerebritis. Arthritis Rheum. 31: 632-641.
13. Nauta, A. J., M. R. Daha, O. Tijsma, W. B. van de, F. Tedesco, and A. Roos. 2002. The membrane attack complex of complement induces caspase activation and apoptosis. Eur. J. Immunol. 32: 783-792.
14. Sato, T., M. G. van-Dixhoorn, F. A. Prins, A. Mooney, N. Verhagen, Y. Muizert, J. Savill, L. A. Van Es, and M. R. Daha. 1999. The terminal sequence of complement plays an essential role in antibody-mediated renal cell apoptosis. J. Am. Soc. Nephrol. 10: 1242-1252.
15. Sakic, B., I. Maric, P. D. Koeberle, J. M. Millward, H. Szechtman, D. Maric, and J. A. Denburg. 2000. Increased TUNEL staining in brains of autoimmune Fas-deficient mice. J. Neuroimmunol. 104: 147-154.
16. Levy, O., R. M. Jean-Jacques, C. Cywes, R. B. Sisson, K. A. Zarember, P. J. Godowski, J. L. Christianson, H. K. Guttormsen, M. C. Carroll, A. Nicholson-Weller, et al. 2003. Critical role of the complement system in group B streptococcus-induced tumor necrosis factor α release. Infect. Immun. 71: 6344-6353.
17. Svenungsson, E., G. Z. Fei, K. Jensen-Urstad, U. de Faire, A. Hamsten, and J. Frostegard. 2003. TNF-α: a link between hypertriglyceridaemia and inflammation in SLE patients with cardiovascular disease. Lupus 12: 454-461.
18. Studnicka-Benke, A., G. Steiner, P. Petera, and J. S. Smolen. 1996. Tumour necrosis factor α and its soluble receptors parallel clinical disease and autoimmune activity in systemic lupus erythematosus. Br. J. Rheumatol. 35: 1067-1074.
19. Gabay, C., N. Cakir, F. Moral, P. Roux-Lombard, O. Meyer, J. M. Dayer, T. Vischer, H. Yazici, and P. A. Guerne. 1997. Circulating levels of tumor necrosis factor soluble receptors in systemic lupus erythematosus are significantly higher than in other rheumatic diseases and correlate with disease activity. J. Rheumatol. 24: 303-308.
20. Ballestas, M. E., and E. N. Benveniste. 1995. Interleukin 1-β- and tumor necrosis factor-α-mediated regulation of ICAM-1 gene expression in astrocytes requires protein kinase C activity. Glia 14: 267-278.
21. Springer, T. A. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76: 301-314.
22. Spatz, M., N. Kawai, N. Merkel, J. Bembry, and R. M. McCarron. 1997. Functional properties of cultured endothelial cells derived from large microvessels of human brain. Am. J. Physiol. 272: C231-C239.
23. Chopp, M., Y. Li, N. Jiang, R. L. Zhang, and J. Prostak. 1996. Antibodies against adhesion molecules reduce apoptosis after transient middle cerebral artery occlusion in rat brain. J. Cereb. Blood Flow Metab. 16: 578-584.
24. Marcus, J. S., S. L. Karackattu, M. A. Fleegal, and C. Sumners. 2003. Cytokine-stimulated inducible nitric oxide synthase expression in astroglia: role of Erk mitogen-activated protein kinase and NF-κB. Glia 41: 152-160.
25. Brown, G. C., and A. Bal-Price. 2003. Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria. Mol. Neurobiol. 27: 325-355.
26. Yu, Z., G. Cheng, X. Wen, G. D. Wu, W. T. Lee, and D. Pleasure. 2002. Tumor necrosis factor α increases neuronal vulnerability to excitotoxic necrosis by inducing expression of the AMPA-glutamate receptor subunit GluR1 via an acid sphingomyelinase- and NF-κB-dependent mechanism. Neurobiol. Dis. 11: 199-213.
27. Rego, A. C., N. M. Monteiro, A. P. Silva, J. Gil, J. O. Malva, and C. R. Oliveira. 2003. Mitochondrial apoptotic cell death and moderate superoxide generation upon selective activation of non-desensitizing AMPA receptors in hippocampal cultures. J. Neurochem. 86: 792-804.
28. Osaka, H., P. Mukherjee, P. S. Aisen, and G. M. Pasinetti. 1999. Complement-derived anaphylatoxin C5a protects against glutamate-mediated neurotoxicity. J. Cell Biochem. 73: 303-311.
29. Martinez-Palma, L., M. Pehar, P. Cassina, H. Peluffo, R. Castellanos, G. Anesetti, J. S. Beckman, and L. Barbeito. 2003. Involvement of nitric oxide on kainate-induced toxicity in oligodendrocyte precursors. Neurotox. Res. 5: 399-406.
30. Baltrons, M. A., and A. Garcia. 1997. AMPA receptors are coupled to the nitric oxide/cyclic GMP pathway in cerebellar astroglial cells. Eur. J. Neurosci. 9: 2497-2501.
31. Adachi, M., R. Watanabe-Fukunaga, and S. Nagata. 1993. 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 90: 1756-1760.
32. Watanabe-Fukunaga, R., C. I. Brannan, N. G. Copeland, N. A. Jenkins, and S. Nagata. 1992. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356: 314-317.
33. Quigg, R. J., C. He, A. Lim, D. Berthiaume, J. J. Alexander, D. Kraus, and V. M. Holers. 1998. Transgenic mice overexpressing the complement inhibitor crry as a soluble protein are protected from antibody-induced glomerular injury. J. Exp. Med 188: 1321-1331.
34. Quigg, R. J., Y. Kozono, D. Berthiaume, A. Lim, D. J. Salant, A. Weinfeld, P. Griffin, E. Kremmer, and V. M. Holers. 1998. Blockade of antibody-induced glomerulonephritis with Crry-Ig, a soluble murine complement inhibitor. J. Immunol. 160: 4553-4560.
35. Bao, L., M. Haas, S. A. Boackle, D. M. Kraus, P. N. Cunningham, P. Park, J. J. Alexander, R. K. Anderson, K. Culhane, V. M. Holers, et al. 2002. Transgenic expression of a soluble complement inhibitor protects against renal disease and promotes survival in MRL/lpr mice. J. Immunol. 168: 3601-3607.
36. Schiller, B., P. N. Cunningham, J. J. Alexander, L. Bao, V. M. Holers, and R. J. Quigg. 2001. Expression of a soluble complement inhibitor protects transgenic mice from antibody-induced acute renal failure. J. Am. Soc. Nephrol. 12: 71-79.
37. Bao, L., M. Haas, D. M. Kraus, B. K. Hack, J. K. Rakstang, V. M. Holers, and R. J. Quigg. 2003. Administration of a soluble recombinant complement C3 inhibitor protects against renal disease in MRL/lpr mice. J. Am. Soc. Nephrol 14: 670-679.
38. Alexander, J. J., A. Lim, C. He, R. L. MacDonald, V. M. Holers, and R. J. Quigg. 1999. Renal, central nervous system and pancreatic overexpression of recombinant soluble Crry in transgenic mice: a novel means of protection from complement-mediated injury. Immunopharmacology 42: 245-254.
39. Goswami, R., J. Kilkus, S. A. Dawson, and G. Dawson. 1999. Overexpression of Akt (protein kinase B) confers protection against apoptosis and prevents formation of ceramide in response to pro-apoptotic stimuli. J. Neurosci. Res. 57: 884-893.
40. Nicholson, D. W., A. Ali, N. A. Thornberry, J. P. Vaillancourt, C. K. Ding, M. Gallant, Y. Gareau, P. R. Griffin, M. Labelle, Y. A. Lazebnik, et al. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376: 37-43.
41. Yokoyama, H., M. Takaeda, T. Wada, S. Ohta, Y. Hisada, C. Segawa, K. Furuichi, and K. Kobayashi. 1997. Glomerular ICAM-1 expression related to circulating TNF-α in human glomerulonephritis. Nephron 76: 425-433.
42. Jennings, J. E., P. C. Sundgren, J. Attwood, J. McCune, and P. Maly. 2004. Value of MRI of the brain in patients with systemic lupus erythematosus and neurologic disturbance. Neuroradiology 46: 15-21.
43. Szechtman, H., B. Sakic, and J. A. Denburg. 1997. Behaviour of MRL mice: an animal model of disturbed behaviour in systemic autoimmune disease. Lupus 6: 223-229.
44. Sakic, B., H. Szechtman, J. A. Denburg, G. Gorny, B. Kolb, and I. Q. Whishaw. 1998. Progressive atrophy of pyramidal neuron dendrites in autoimmune MRL-lpr mice. J. Neuroimmunol. 87: 162-170.
45. Vogelweid, C. M., G. C. Johnson, C. L. Besch-Williford, J. Basler, and S. E. Walker. 1991. Inflammatory central nervous system disease in lupus-prone MRL/lpr mice: comparative histologic and immunohistochemical findings. J. Neuroimmunol. 35: 89-99.
46. Alexander, J. J., L. Bao, A. Jacob, D. M. Kraus, V. M. Holers, and R. J. Quigg. 2003. Administration of the soluble complement inhibitor, Crry-Ig, reduces inflammation and aquaporin 4 expression in lupus cerebritis. Biochim. Biophys. Acta 1639: 169-176.
47. Gasque, P., Y. D. Dean, E. P. McGreal, J. VanBeek, and B. P. Morgan. 2000. Complement components of the innate immune system in health and disease in the CNS. Immunopharmacology 49: 171-186.
48. Kang, H. J., L. Bao, Y. Xu, R. J. Quigg, P. C. Giclas, and V. M. Holers. 2004. Increased serum C3 levels in Crry transgenic mice partially abrogates its complement inhibitory effects. Clin. Exp. Immunol. 136: 194-199.
49. Davoust, N., S. Nataf, V. M. Holers, and S. R. Barnum. 1999. Expression of the murine complement regulatory protein crry by glial cells and neurons. Glia 27: 162-170.
50. Abbott, N. J., L. L. Mendonca, and D. E. Dolman. 2003. The blood-brain barrier in systemic lupus erythematosus. Lupus 12: 908-915.
51. Riedemann, N. C., R. F. Guo, I. J. Laudes, K. Keller, V. J. Sarma, V. Padgaonkar, and P. A. Ward. 2002. C5a receptor and thymocyte apoptosis in sepsis. FASEB J. 16: 887-888.
52. Uwai, M., Y. Terui, Y. Mishima, H. Tomizuka, M. Ikeda, T. Itoh, M. Mori, M. Ueda, R. Inoue, M. Yamada, et al. 2000. A new apoptotic pathway for the complement factor B-derived fragment Bb. J. Cell Physiol 185: 280-292.
53. Strachan, A. J., T. M. Woodruff, G. Haaima, D. P. Fairlie, and S. M. Taylor. 2000. A new small molecule C5a receptor antagonist inhibits the reverse-passive Arthus reaction and endotoxic shock in rats. J. Immunol. 164: 6560-6565.
54. Takabayashi, T., E. Vannier, J. F. Burke, R. G. Tompkins, J. A. Gelfand, and B. D. Clark. 1998. Both C3a and C3a(desArg) regulate interleukin-6 synthesis in human peripheral blood mononuclear cells. J. Infect. Dis. 177: 1622-1628.
55. Belmont, H. M., D. Levartovsky, A. Goel, A. Amin, R. Giorno, J. Rediske, M. L. Skovron, and S. B. Abramson. 1997. Increased nitric oxide production accompanied by the up-regulation of inducible nitric oxide synthase in vascular endothelium from patients with systemic lupus erythematosus. Arthritis Rheum. 40: 1810-1816.
56. Freyer, D., R. Manz, A. Ziegenhorn, M. Weih, K. Angstwurm, W. D. Docke, A. Meisel, R. R. Schumann, G. Schonfelder, U. Dirnagl, et al. 1999. Cerebral endothelial cells release TNF-α after stimulation with cell walls of Streptococcus pneumoniae and regulate inducible nitric oxide synthase and ICAM-1 expression via autocrine loops. J. Immunol. 163: 4308-4314.
57. Zameer, A., and S. A. Hoffman. 2003. Increased ICAM-1 and VCAM-1 expression in the brains of autoimmune mice. J. Neuroimmunol. 142: 67-74.
58. Greenwood, J., C. L. Amos, C. E. Walters, P. O. Couraud, R. Lyck, B. Engelhardt, and P. Adamson. 2003. Intracellular domain of brain endothelial intercellular adhesion molecule-1 is essential for T lymphocyte-mediated signaling and migration. J. Immunol. 171: 2099-2108.
59. Leuchtmann, E. A., A. E. Ratner, R. Vijitruth, Y. Qu, and J. W. McDonald. 2003. AMPA receptors are the major mediators of excitotoxic death in mature oligodendrocytes. Neurobiol. Dis. 14: 336-348.
60. Jablonski, E. M., A. N. Webb, N. A. McConnell, M. C. Riley, and F. M. Hughes, Jr. 2004. Plasma membrane aquaporin activity can affect the rate of apoptosis but is inhibited after apoptotic volume decrease. Am. J. Physiol. 286: C975-C985.