Phagocytosis of apoptotic inflammatory cells downregulates microglial chemoattractive function and migration of encephalitogenic T cells

Journal of Neuroscience Research

Volumn 84, Issue 6, 2006, Pages 1217-1224

  Chan, Andrew ^a,b   Hummel, Vera ^b   Weilbach, Franz X ^b   Kieseier, Bernd C ^c   Gold, Ralf ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Apoptosis; Chemotaxis; Phagocytosis

Indexed keywords

CHEMOKINE; GELATINASE; GELATINASE A; MATRIX METALLOPROTEINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES;

APOPTOSIS; ARTICLE; CELL CULTURE; CENTRAL NERVOUS SYSTEM; CHEMOTAXIS; EXPERIMENTAL MODEL; INFLAMMATORY CELL; MICROGLIA; MIGRATION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; T LYMPHOCYTE; ZYMOGRAPHY;

ANIMALS; APOPTOSIS; CELL MOVEMENT; CHEMOKINE CCL2; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; DOWN-REGULATION; ENCEPHALITIS; GELATINASES; LIPOPOLYSACCHARIDES; MICROGLIA; PHAGOCYTOSIS; RANTES; RATS; RATS, INBRED LEW; T-LYMPHOCYTES;

EID: 33750492578     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21029     Document Type: Article

References (33)

1. Ambrosini E, Aloisi F. 2004. Chemokines and glial cells: a complex network in the central nervous system. Neurochem Res 5:1017-1038.
2. Ambrosini E, Columba-Cazebas B, Serafini B, Aloisi F. 2002. Migration of different leukocyte subsets in response to chemokines secreted by activated microglia and astrocytes. Glia 38:S75-S75.
3. Anders HJ, Frink M, Linde Y, Banas B, Wörnle M, Cohen CD, Vielhauer V, Nelson PJ, Gröne HJ, Schlöndorff D. 2003. CC chemokine ligand 5/RANTES chemokine antagonists aggravate glomerulonephritis despite reduction of glomerular leukocyte infiltration. J Immunol 170:5658-5666.
4. Appay V, Rowland-Jones SL. 2001. RANTES: a versatile and controversial chemokine. Trends Immunol 22:83-87.
5. Chan A, Magnus T, Gold R. 2001. Phagocytosis of apoptotic inflammatory cells by microglia and modulation by different cytokines: mechanism for removal of apoptotic cells in the inflamed nervous system. Glia 33:87-95.
6. Chan A, Seguin R, Magnus T, Papadimitriou C, Toyka KV, Antel JP, Gold R. 2003. Phagocytosis of apoptotic inflammatory cells by microglia and its therapeutic implications: termination of CNS-autoimmune inflammation and modulation by Interferon-beta. Glia 43:231-242.
7. Cross AK, Woodroofe MN. 1999. Chemokine modulation of matrix metalloproteinase and TIMP production in adult rat brain microglia and a human microglial cell line in vitro. Glia 28:183-189.
8. Frevert CW, Wong VA, Goodman RB, Goodwin R, Martin TR. 1998. Rapid fluorescence-based measurement of neutrophil migration in vitro. J Immunol Methods 213:41-52.
9. Gold R, Hartung HP, Lassmann H. 1997. T cell apoptosis in autoimmune diseases: termination of inflammation in the nervous system and other sites with specialized immune-defense mechanisms. TINS 20:399-404.
10. Hirt UA, Leist M. 2003. Rapid, noninflammatory and PS-dependent phagocyte clearance of necrotic cells. Cell Death Differ 10:1156-1164.
11. Huang D, Han Y, Sandhya Rani MR, Glabinski A, Trebst C, Sorensen T, Tani M, Wang J, Chien P, O'Bryan S, Bielecki B, Zhou ZL, Majumder S, Ransohoff RM. 2000. Chemokines and chemokine receptors in inflammation of the nervous system: manifold roles and exquisite regulation. Immunol Reviews 177:52-67.
12. Kauppinen TM, Swanson RA. 2005. Poly(ADP-ribose) polymerase-1 promotes microglial activation, proliferation, and matrix metalloproteinase-9-mediated neuron death. J Immunol 174:2288-2296.
13. Kieseier BC, Kiefer R, Clements JM, Miller K, Wells GMA, Schweitzer T, Gearing AJH, Hartung HP. 1998. Matrix metalloproteinase-9 and -7 are regulated in experimental autoimmune encephalomyelitis. Brain 121:159-166.
14. Lauber K, Bohn E, Krober SM, Xiao YJ, Blumenthal SG, Lindemann RK, Marini P, Wiedig C, Zobywalski A, Baksh S, Xu Y, Autenrieth IB, Schulze-Osthoff K, Belka C, Stuhler G, Wesselborg S. 2003. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113:717-730.
15. Liu LP, Huang DR, Matsui M, He TT, Hu T, DeMartino J, Lu B, Gerard C, Ransohoff RM. 2006. Severe disease, unaltered leukocyte migration, and reduced IFN-g production in CXCR3 -/- mice with experimental autoimmune encephalomyelitis. J Immunol 176:4399-4409.
16. Maderna P, Godson C. 2003. Phagocytosis of apoptotic cells and the resolution of inflammation. Biochim Biophys Acta 1639:141-151.
17. Magnus T, Chan A, Grauer O, Toyka KV, Gold R. 2001. Microglial phagocytosis of apoptotic inflammatory T cells leads to down-regulation of microglial immune activation. J Immunol 167:5004-5010.
18. McDonald PP, Fadok VA, Bratton D, Henson PM. 1999. Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-beta in macrophages that have ingested apoptotic cells. J Immunol 163:6164-6172.
19. Middleton J, Patterson AM, Gardner L, Schmutz C, Ashton BA. 2002. Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood 100:3853-3860.
20. Nguyen KB, Pender MP. 1998. Phagocytosis of apoptotic lymphocytes by oligodendrocytes in experimental autoimmune encephalomyelitis. Acta Neuropathol 95:40-46.
21. Opdenakker G, Van-Damme J. 2003. Functional roles and therapeutic targeting of gelatinase B and chemokines in multiple sclerosis. Lancet Neurol 2:747-756.
22. Paglinawan R, Malipiero U, Schlapbach R, Frei K, Reith W, Fontana A. 2003. TGFbeta directs gene expression of activated microglia to an antiinflammatory phenotype strongly focusing on chemokine genes and cell migratory genes. Glia 44:219-231.
23. Parks WC, Wilson CL, Lopez-Boado YS. 2004. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 4:617-629.
24. Pender MP, Rist MJ. 2001. Apoptosis of inflammatory cells in immune control of the nervous system: role of glia. Glia 36:137-144.
25. Platten M, Steinman L. 2005. Multiple sclerosis: trapped in deadly glue. Nature Med 11:252-253.
26. Raivich G, Banati R. 2004. Brain microglia and blood-derived macrophages; molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease. Brain Res Brain Res Rev 46:261-281.
27. Ransohoff R, Kivisäkk P, Kidd G. 2003. Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 3:569-581.
28. Rosenberg GA. 2002. Matrix metalloproteinases in neuroinflammation. Glia 39:279-291.
29. Savill J, Dransfield I, Gregory C, Haslett C. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2:965-975.
30. Schmidt J, Gold R, Zettl UK, Hartung HP, Toyka KV. 2000. T cell apoptosis in situ in experimental autoimmune encephalomyelitis following methylprednisolone pulse therapy. Brain 123:1431-1441.
31. Sellebjerg F, Sorensen TL. 2003. Chemokines and matrix metalloproteinase-9 in leukocyte recruitment to the central nervous system. Brain Res Bull 61:347-355.
32. Serhan CN, Savill J. 2005. Resolution of inflammation: the beginning programs the end. Nat Immunol 6:1191-1197.
33. Takahashi K, Rochford CD, Neumann H. 2005. Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 201:647-657.