Intracerebroventricular injection of the terminal complement complex causes inflammatory reaction in the rat brain

European Journal of Immunology

Volumn 33, Issue 5, 2003, Pages 1260-1270

  Casarsa, Claudia ^a   De Luigi, Ada ^b   Pausa, Mario ^a   De Simoni, Maria Grazia ^b   Tedesco, Francesco ^a  

^a UNIVERSITY OF TRIESTE   (Italy)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

Animal model; Central nervous system; Inflammation; Terminal complement complex

Indexed keywords

COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5B; COMPLEMENT COMPONENT C7; COMPLEMENT COMPONENT C8; COMPLEMENT COMPONENT C9; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOACCUMULATION; BRAIN REGION; CELL GROWTH; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID; CHOROID PLEXUS; CONTROLLED STUDY; CYTOLYSIS; ENCEPHALITIS; HISTOPATHOLOGY; IN VIVO STUDY; LATERAL BRAIN VENTRICLE; LEUKOCYTE; LEUKOCYTE MIGRATION; MALE; MENINX; MONONUCLEAR CELL; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ACUTE DISEASE; ANIMALS; BRAIN; CHEMOKINE CCL2; COMPLEMENT C5A; COMPLEMENT MEMBRANE ATTACK COMPLEX; CYTOKINES; HUMANS; INFLAMMATION; INJECTIONS, INTRAVENTRICULAR; LEUKOCYTES; LIPOPOLYSACCHARIDES; MALE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0038297283     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200323574     Document Type: Article

References (40)

1. Gasque, P., Dean, Y. D., McGreal, E. P., VanBeek, J. and Morgan, B. P., Complement components of the innate immune system in health and disease in the CNS. Immunopharmacology 2000. 49: 171-186.
2. Stahel, P. F., Morganti-Kossmann, M. C. and Kossmann, T., The role of the complement system in traumatic brain injury. Brain Res. Rev. 1998. 27: 243-256.
3. Broadwell, R. D. and Sofroniew, M. V., Serum proteins bypass the blood-brain fluid barriers for extracellular entry to the central nervous system. Exp. Neurol. 1993. 120: 245-263.
4. Morgan, B. P. and Gasque, P., Expression of complement in the brain: role in health and disease. Immunol. Today 1996. 17: 461-466.
5. Sanders, M. E., Koski, C. L., Robbins, D., Shin, M. L., Frank, M. M. and Joiner, K. A., Activated terminal complement in cerebrospinal fluid in Guillain-Barre syndrome and multiple sclerosis. J. Immunol. 1986. 136: 4456-4459.
6. Mollnes, T. E., Vandvik, B., Lea, T. and Vartdal, F., Intrathecal complement activation in neurological diseases evaluated by analysis of the terminal complement complex. J. Neurol. Sci. 1987. 78: 17-28.
7. Hartung, H. P., Schwenke, C., Bitter-Suermann, D. and Toyka, K. V., Guillain-Barre syndrome: activated complement components C3a and C5a in CSF. Neurology 1987. 37: 1006-1009.
8. Compston, D. A., Morgan, B. P., Campbell, A. K., Wilkins, P., Cole, G., Thomas, N. D. and Jasani, B., Immunocytochemical localization of the terminal complement complex in multiple sclerosis. Neuropathol. Appl. Neurobiol. 1989. 15: 307-316.
9. Lindsberg, P. J., Ohman, J., Lehto, T., Karjalainen-Lindsberg, M. L., Paetau, A., Wuorimaa, T., Carpen, O., Kaste, M. and Meri, S., Complement activation in the central nervous system following blood- brain barrier damage in man. Ann. Neurol. 1996. 40: 587-596.
10. Piddlesden, S. J., Storch, M. K., Hibbs, M., Freeman, A. M., Lassmann, H. and Morgan, B. P., Soluble recombinant complement receptor 1 inhibits inflammation and demyelination in antibody-mediated demyelinating experimental allergic encephalomyelitis. J. Immunol. 1994. 152: 5477-5484.
11. Linington, C., Morgan, B. P., Scolding, N. J., Wilkins, P., Piddlesden, S. and Compston, D. A., The role of complement in the pathogenesis of experimental allergic encephalomyelitis. Brain 1989. 112: 895-911.
12. Itagaki, S., Akiyama, H., Saito, H. and McGeer, P. L., Ultra-structural localization of complement membrane attack complex (MAC)-like immunoreactivity in brains of patients with Alzheimer's disease. Brain Res. 1994. 645: 78-84.
13. Piddlesden, S. J. and Morgan, B. P., Killing of rat glial cells by complement: deficiency of the rat analogue of CD59 is the cause of oligodendrocyte susceptibility to lysis. J. Neuroimmunol. 1993. 48: 169-175.
14. Zajicek, J., Wing, M., Skepper, J. and Compston, A., Human oligodendrocytes are not sensitive to complement. A study of CD59 expression in the human central nervous system. Lab. Invest. 1995. 73: 128-138.
15. Wing, M. G., Zajicek, J., Seilly, D. J., Compston, D. A. and Lachmann, P. J., Oligodendrocytes lack glycolipid anchored proteins which protect them against complement lysis. Restoration of resistance to lysis by incorporation of CD59. Immunology 1992. 76: 140-145.
16. Monaco, S., Bonetti, B., Ferrari, S., Moretto, G., Nardelli, E., Tedesco, F., Mollnes, T. E., Nobile-Orazio, E., Manfredini, E., Bonazzi, L. et al., Complement-mediated demyelination in patients with IgM monoclonal gammopathy and polyneuropathy. N. Engl. J. Med. 1990. 322: 649-652.
17. Monaco, S., Ferrari, S., Bonetti, B., Moretto, G., Kirshfink, M., Nardelli, E., Nobile-Orazio, E., Zanusso, G., Rizzuto, N. and Tedesco, F., Experimental induction of myelin changes by anti-MAG antibodies and terminal complement complex. J. Neuropathol. Exp. Neurol. 1995. 54: 96-104.
18. Morgan, B. P., Complement membrane attack on nucleated cells: resistance, recovery and non-lethal effects. Biochem. J. 1989. 264: 1-14.
19. Kilgore, K. S., Flory, C. M., Miller, B. F., Evans, V. M. and Warren, J. S., The membrane attack complex of complement induces interleukin-8 and monocyte chemoattractant protein-1 secretion from human umbilical vein endothelial cells. Am. J. Pathol. 1996. 149: 953-961.
20. Tedesco, F., Pausa, M., Nardon, E., Introna, M., Mantovani, A. and Dobrina, A., The cytolytically inactive terminal complement complex activates endothelial cells to express adhesion molecules and tissue factor procoagulant activity. J. Exp. Med. 1997. 185: 1619-1627.
21. Mead, R. J., Singhrao, S. K., Neal, J. W., Lassmann, H. and Morgan, B. P., The membrane attack complex of complement causes severe demyelination associated with acute axonal injury. J. Immunol. 2002. 168: 458-465.
22. Dobrina, A., Pausa, M., Fischetti, F., Bulla, R., Vecile, E., Ferrero, E., Mantovani, A. and Tedesco, F., Cytolytically inactive terminal complement complex causes transendothelial migration of polymorphonuclear leukocytes in vitro and in vivo. Blood 2002. 99: 185-192.
23. Steffen, B. J., Breier, G., Butcher, E. C., Schulz, M. and Engelhardt, B., ICAM-1, VCAM-1, and MAdCAM-1 are expressed on choroid plexus epithelium but not endothelium and mediate binding of lymphocytes in vitro. Am. J. Pathol. 1996. 148: 1819-1838.
24. De Simoni, M. G., Del Bo, R., De Luigi, A., Simard, S. and Forloni, G., Central endotoxin induces different patterns of interleukin (IL)-1 beta and IL-6 messenger ribonucleic acid expression and IL-6 secretion in the brain and periphery. Endocrinology 1995. 136: 897-902.
25. Lachmann, P. J. and Thompson, R. A., Reactive lysis: the complement-mediated lysis of unsensitized cells. II. The characterization of activated reactor as C56 and the participation of C8 and C9. J. Exp. Med. 1970. 131: 643-657.
26. Czermak, B. J., Lentsch, A. B., Bless, N. M., Schmal, H., Friedl, H. P. and Ward, P. A., Synergistic enhancement of chemokine generation and lung injury by C5a or the membrane attack complex of complement. Am. J. Pathol. 1999. 154: 1513-1524.
27. Reese, T. S., Feder, N. and Brightman, M. W., Electron microscopic study of the blood-brain and blood-cerebrospinal fluid barriers with microperoxidase. J. Neuropathol. Exp. Neurol. 1971. 30: 137-138.
28. Faustmann, P. M., Krause, D., Dux, R. and Dermietzel, R., Morphological study in the early stages of complement C5a fragment-induced experimental meningitis: activation of macrophages and astrocytes. Acta Neuropathol. 1995. 89: 239-247.
29. Mukherjee, P. and Pasinetti, G. M., Complement anaphylatoxin C5a neuroprotects through mitogen-activated protein kinase-dependent inhibition of caspase 3. J. Neurochem. 2001. 77: 43-49.
30. Gasque, P., Chan, P., Fontaine, M., Ischenko, A., Lamacz, M., Gotze, O. and Morgan, B. P., Identification and characterization of the complement C5a anaphylatoxin receptor on human astrocytes. J. Immunol. 1995. 155: 4882-4889.
31. Lacy, M., Jones, J., Whittemore, S. R., Haviland, D. L., Wetsel, R. A. and Barnum, S. R., Expression of the receptors for the C5a anaphylatoxin, interleukin-8 and FMLP by human astrocytes and microglia. J. Neuroimmunol. 1995. 61: 71-78.
32. O'Barr, S. A., Caguioa, J., Gruol, D., Perkins, G., Ember, J. A., Hugli, T. and Cooper, N. R., Neuronal expression of a functional receptor for the C5a complement activation fragment. J. Immunol. 2001. 166: 4154-4162.
33. Nataf, S., Stahel, P. F., Davoust, N. and Barnum, S. R., Complement anaphylatoxin receptors on neurons: new tricks for old receptors? Trends Neurosci. 1999. 22: 397-402.
34. Montero-Menei, C. N., Sindji, L., Pouplard-Barthelaix, A., Jehan, F., Denechaud, L. and Darcy, F., Lipopolysaccharide intracerebral administration induces minimal inflammatory reaction in rat brain. Brain Res. 1994. 653: 101-111.
35. Kilgore, K. S., Shen, J. P., Miller, B. F., Ward, P. A. and Warren, J. S., Enhancement by the complement membrane attack complex of tumor necrosis factor-alpha-induced endothelial cell expression of E-selectin and ICAM- 1. J. Immunol. 1995. 155: 1434-1441.
36. Endo, H., Sasaki, K., Tonosaki, A. and Kayama, T., Three-dimensional and ultrastructural ICAM-1 distribution in the choroid plexus, arachnoid membrane and dural sinus of inflammatory rats induced by LPS injection in the lateral ventricles. Brain Res. 1998. 793: 297-301.
37. Del Maschio, A., De Luigi, A., Martin-Padura, I., Brockhaus, M., Bartfai, T., Fruscella, P., Adorini, L., Martino, G., Furlan, R., De Simoni, M. G. and Dejana, E., Leukocyte recruitment in the cerebrospinal fluid of mice with experimental meningitis is inhibited by an antibody to junctional adhesion molecule (JAM). J. Exp. Med. 1999. 190: 1351-1356.
38. Marzari, R., Sblattero, D., Macor, P., Fischetti, F., Gennaro, R., Marks, J. D., Bradbury, A. and Tedesco, F., The cleavage site of C5 from man and animals as a common target for neutralizing human monoclonal antibodies: in vitro and in vivo studies. Eur. J. Immunol. 2002. 32: 2773-2782.
39. Langeggen, H., Pausa, M., Johnson, E., Casarsa, C. and Tedesco, F., The endothelium is an extrahepatic site of synthesis of the seventh component of the complement system. Clin. Exp. Immunol. 2000: 121: 69-76.
40. Harrison, R. A. and Lachmann, P. J., In Weir, D. M., Herzenberg, L. A., Blackwell, C. and Herzenberg, L. A. (Eds.), Handbook of Experimental Immunology, Blackwell, Oxford 1986, p. 39.1.