Systemic inflammation modulates Fc receptor expression on microglia during chronic neurodegeneration

Journal of Immunology

Volumn 186, Issue 12, 2011, Pages 7215-7224

  Lunnon, Katie ^a,b   Teeling, Jessica L ^a   Tutt, Alison L ^c   Cragg, Mark S ^c   Glennie, Martin J ^c   Perry, V Hugh ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD200 RECEPTOR; CYTOKINE; FC GAMMA RECEPTOR 2; FC GAMMA RECEPTOR 4; FC RECEPTOR; IMMUNOGLOBULIN G; LIPOPOLYSACCHARIDE; MEMBRANE RECEPTOR; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE COURSE; DISEASE SEVERITY; FEMALE; GENE SWITCHING; INFLAMMATION; MACROPHAGE ACTIVATION; MICROGLIA; MOLECULAR DYNAMICS; MOUSE; NERVE DEGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PARENCHYMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANTIBODIES; CHRONIC DISEASE; DISEASE PROGRESSION; INFLAMMATION; MACROPHAGE ACTIVATION; MICROGLIA; NERVE DEGENERATION; PHENOTYPE; RECEPTORS, FC; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 79959569662     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903833     Document Type: Article

References (55)

1. Dheen, S. T., C. Kaur, and E. A. Ling. 2007. Microglial activation and its implications in the brain diseases. Curr. Med. Chem. 14: 1189-1197.
2. ADAPT Research Group, C. L Meinert, L. D. McCaffrey, and J. C. Breitner. 2009. Alzheimer's Disease Anti-inflammatory Prevention Trial: design, methods, and baseline results. Alzheimers Dement. 5: 93-104.
3. Neumann, H., M. R. Kotter, and R. J. Franklin. 2009. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 132: 288-295.
4. Betmouni, S., V. H. Perry, and J. L. Gordon. 1996. Evidence for an early inflammatory response in the central nervous system of mice with scrapie. Neuroscience 74: 1-5.
5. Cunningham, C., R. M. Deacon, K. Chan, D. Boche, J. N. Rawlins, and V. H. Perry. 2005. Neuropathologically distinct prion strains give rise to similar temporal profiles of behavioral deficits. Neurobiol. Dis. 18: 258-269.
6. Cunningham, C., D. C. Wilcockson, D. Boche, and V. H. Perry. 2005. Comparison of inflammatory and acute-phase responses in the brain and peripheral organs of the ME7 model of prion disease. J. Virol. 79: 5174-5184.
7. Boche, D., C. Cunningham, J. Gauldie, and V. H. Perry. 2003. Transforming growth factor-beta 1-mediated neuroprotection against excitotoxic injury in vivo. J. Cereb. Blood Flow Metab. 23: 1174-1182.
8. Minghetti, L., A. Greco, F. Cardone, M. Puopolo, A. Ladogana, S. Almonti, C. Cunningham, V. H. Perry, M. Pocchiari, and G. Levi. 2000. Increased brain synthesis of prostaglandin E2 and F2-isoprostane in human and experimental transmissible spongiform encephalopathies. J. Neuropathol. Exp. Neurol. 59: 866-871.
9. Walsh, D. T., V. H. Perry, and L. Minghetti. 2000. Cyclooxygenase-2 is highly expressed in microglial-like cells in a murine model of prion disease. Glia 29: 392-396. (Pubitemid 30121429)
10. Cunningham, C., R. Deacon, H. Wells, D. Boche, S. Waters, C. P. Diniz, H. Scott, J. N. Rawlins, and V. H. Perry. 2003. Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur. J. Neurosci. 17: 2147-2155.
11. Fadok, V. A., D. L. Bratton, A. Konowal, P. W. Freed, J. Y. Westcott, and P. M. Henson. 1998. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 101: 890-898. (Pubitemid 28096086)
12. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2: 965-975.
13. Dantzer, R., and K. W. Kelley. 2007. Twenty years of research on cytokine-induced sickness behavior. Brain Behav. Immun. 21: 153-160.
14. Cunningham, C., S. Campion, K. Lunnon, C. L. Murray, J. F. Woods, R. M. Deacon, J. N. Rawlins, and V. H. Perry. 2009. Systemic inflammation induces acute behavioral and cognitive changes and accelerates neurodegenerative disease. Biol. Psychiatry 65: 304-312.
15. Cunningham, C., D. C. Wilcockson, S. Campion, K. Lunnon, and V. H. Perry. 2005. Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J. Neurosci. 25: 9275-9284.
16. Godbout, J. P., J. Chen, J. Abraham, A. F. Richwine, B. M. Berg, K. W. Kelley, and R. W. Johnson. 2005. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 19: 1329-1331.
17. Palin, K., C. Cunningham, P. Forse, V. H. Perry, and N. Platt. 2008. Systemic inflammation switches the inflammatory cytokine profile in CNS Wallerian degeneration. Neurobiol. Dis. 30: 19-29.
18. Nguyen, M. D., T. D'Aigle, G. Gowing, J. P. Julien, and S. Rivest. 2004. Exacerbation of motor neuron disease by chronic stimulation of innate immunity in a mouse model of amyotrophic lateral sclerosis. J. Neurosci. 24: 1340-1349. (Pubitemid 38222984)
19. McColl, B. W., N. J. Rothwell, and S. M. Allan. 2007. Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1- and neutrophildependent mechanisms. J. Neurosci. 27: 4403-4412.
20. McColl, B. W., N. J. Rothwell, and S. M. Allan. 2008. Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J. Neurosci. 28: 9451-9462.
21. Buljevac, D., H. Z. Flach, W. C. Hop, D. Hijdra, J. D. Laman, H. F. Savelkoul, F. G. van Der Meché, P. A. van Doorn, and R. Q. Hintzen. 2002. Prospective study on the relationship between infections and multiple sclerosis exacerbations. Brain 125: 952-960.
22. Dunn, N., M. Mullee, V. H. Perry, and C. Holmes. 2005. Association between dementia and infectious disease: evidence from a case-control study. Alzheimer Dis. Assoc. Disord. 19: 91-94.
23. Johnston, K. C., J. Y. Li, P. D. Lyden, S. K. Hanson, T. E. Feasby, R. J. Adams, R. E. Faught, Jr., E. C. Haley Jr.; RANTTAS Investigators. 1998. Medical and neurological complications of ischemic stroke: experience from the RANTTAS trial. Stroke 29: 447-453. (Pubitemid 28086690)
24. Teeling, J. L., and V. H. Perry. 2009. Systemic infection and inflammation in acute CNS injury and chronic neurodegeneration: underlying mechanisms. Neuroscience 158: 1062-1073.
25. Beers, S. A., R. R. French, H. T. Chan, S. H. Lim, T. C. Jarrett, R. M. Vidal, S. S. Wijayaweera, S. V. Dixon, H. J. Kim, K. L. Cox, et al. 2010. Antigenic modulation limits the efficacy of anti-CD20 antibodies: implications for antibody selection. Blood 115: 5191-5201.
26. Jain, N., J. Thatte, T. Braciale, K. Ley, M. O'Connell, and J. K. Lee. 2003. Local-pooled-error test for identifying differentially expressed genes with a small number of replicated microarrays. Bioinformatics 19: 1945-1951.
27. Teeling, J. L., C. Cunningham, T. A. Newman, and V. H. Perry. 2010. The effect of non-steroidal anti-inflammatory agents on behavioural changes and cytokine production following systemic inflammation: Implications for a role of COX-1. Brain Behav. Immun. 24: 409-419.
28. Wisniewski, H. M., A. S. Lossinsky, R. C. Moretz, A. W. Vorbrodt, H. Lassmann, and R. I. Carp. 1983. Increased blood-brain barrier permeability in scrapie-infected mice. J. Neuropathol. Exp. Neurol. 42: 615-626.
29. Guenther, K., R. M. Deacon, V. H. Perry, and J. N. Rawlins. 2001. Early behavioural changes in scrapie-affected mice and the influence of dapsone. Eur. J. Neurosci. 14: 401-409.
30. Combrinck, M. I., V. H. Perry, and C. Cunningham. 2002. Peripheral infection evokes exaggerated sickness behaviour in pre-clinical murine prion disease. Neuroscience 112: 7-11. (Pubitemid 34603493)
31. Hughes, M. M., R. H. Field, V. H. Perry, C. L. Murray, and C. Cunningham. 2010. Microglia in the degenerating brain are capable of phagocytosis of beads and of apoptotic cells, but do not efficiently remove PrPSc, even upon LPS stimulation. Glia 58: 2017-2030.
32. Billadeau, D. D., and P. J. Leibson. 2002. ITAMs versus ITIMs: striking a balance during cell regulation. J. Clin. Invest. 109: 161-168.
33. Clynes, R., J. S. Maizes, R. Guinamard, M. Ono, T. Takai, and J. V. Ravetch. 1999. Modulation of immune complex-induced inflammation in vivo by the coordinate expression of activation and inhibitory Fc receptors. J. Exp. Med. 189: 179-185.
34. Peress, N. S., H. B. Fleit, E. Perillo, R. Kuljis, and C. Pezzullo. 1993. Identification of Fc gamma RI, II and III on normal human brain ramified microglia and on microglia in senile plaques in Alzheimer's disease. J. Neuroimmunol. 48: 71-79.
35. Piccio, L., C. Buonsanti, M. Mariani, M. Cella, S. Gilfillan, A. H. Cross, M. Colonna, and P. Panina-Bordignon. 2007. Blockade of TREM-2 exacerbates experimental autoimmune encephalomyelitis. Eur. J. Immunol. 37: 1290-1301.
36. Walker, D. G., J. E. Dalsing-Hernandez, N. A. Campbell, and L. F. Lue. 2009. Decreased expression of CD200 and CD200 receptor in Alzheimer's disease: a potential mechanism leading to chronic inflammation. Exp. Neurol. 215: 5-19.
37. Frank, S., G. J. Burbach, M. Bonin, M. Walter, W. Streit, I. Bechmann, and T. Deller. 2008. TREM2 is upregulated in amyloid plaque-associated microglia in aged APP23 transgenic mice. Glia 56: 1438-1447.
38. Castells, M. C. 1994. Surface makers for mast cell subtypes: low affinity IgG receptors and gp49 family. Allerg. Immunol. (Paris) 26: 127-131.
39. Nimmerjahn, F., and J. V. Ravetch. 2006. Fcgamma receptors: old friends and new family members. Immunity 24: 19-28.
40. Ravetch, J. V., and S. Bolland. 2001. IgG Fc receptors. Annu. Rev. Immunol. 19: 275-290.
41. Ravetch, J. V., and L. L. Lanier. 2000. Immune inhibitory receptors. Science 290: 84-89.
42. Vedeler, C., E. Ulvestad, I. Grundt, G. Conti, H. Nyland, R. Matre, and D. Pleasure. 1994. Fc receptor for IgG (FcR) on rat microglia. J. Neuroimmunol. 49: 19-24. (Pubitemid 24071749)
43. Loughlin, A. J., M. N. Woodroofe, and M. L. Cuzner. 1992. Regulation of Fc receptor and major histocompatibility complex antigen expression on isolated rat microglia by tumour necrosis factor, interleukin-1 and lipopolysaccharide: effects on interferon-gamma induced activation. Immunology 75: 170-175.
44. Herber, D. L., J. L. Maloney, L. M. Roth, M. J. Freeman, D. Morgan, and M. N. Gordon. 2006. Diverse microglial responses after intrahippocampal administration of lipopolysaccharide. Glia 53: 382-391.
45. Li, Y. N., X. J. Qin, F. Kuang, R. Wu, X. L. Duan, G. Ju, and B. R. Wang. 2008. Alterations of Fc gamma receptor I and Toll-like receptor 4 mediate the anti-inflammatory actions of microglia and astrocytes after adrenaline-induced blood-brain barrier opening in rats. J. Neurosci. Res. 86: 3556-3565.
46. Breij, E. C., B. P. Brink, R. Veerhuis, C. van den Berg, R. Vloet, R. Yan, C. D. Dijkstra, P. van der Valk, and L. Bö. 2008. Homogeneity of active demyelinating lesions in established multiple sclerosis. Ann. Neurol. 63: 16-25.
47. Ulvestad, E., K. Williams, C. Vedeler, J. Antel, H. Nyland, S. Mørk, and R. Matre. 1994. Reactive microglia in multiple sclerosis lesions have an increased expression of receptors for the Fc part of IgG. J. Neurol. Sci. 121: 125-131.
48. Urich, E., I. Gutcher, M. Prinz, and B. Becher. 2006. Autoantibody-mediated demyelination depends on complement activation but not activatory Fc-receptors. Proc. Natl. Acad. Sci. USA 103: 18697-18702.
49. Klein, M. A., P. S. Kaeser, P. Schwarz, H. Weyd, I. Xenarios, R. M. Zinkernagel, M. C. Carroll, J. S. Verbeek, M. Botto, M. J. Walport, et al. 2001. Complement facilitates early prion pathogenesis. Nat. Med. 7: 488-492.
50. Chicheportiche, Y., and P. Vassalli. 1994. Tumor necrosis factor induces a block in the cotranslation of Fc gamma RIIb mRNA in mouse peritoneal macrophages. J. Biol. Chem. 269: 20134-20138.
51. Le, W., D. Rowe, W. Xie, I. Ortiz, Y. He, and S. H. Appel. 2001. Microglial activation and dopaminergic cell injury: an in vitro model relevant to Parkinson's disease. J. Neurosci. 21: 8447-8455.
52. Boche, D., E. Zotova, R. O. Weller, S. Love, J. W. Neal, R. M. Pickering, D. Wilkinson, C. Holmes, and J. A. Nicoll. 2008. Consequence of Abeta immunization on the vasculature of human Alzheimer's disease brain. Brain 131: 3299-3310.
53. Wilcock, D. M., P. T. Jantzen, Q. Li, D. Morgan, and M. N. Gordon. 2007. Amyloid-beta vaccination, but not nitro-nonsteroidal anti-inflammatory drug treatment, increases vascular amyloid and microhemorrhage while both reduce parenchymal amyloid. Neuroscience 144: 950-960.
54. Pfeifer, M., S. Boncristiano, L. Bondolfi, A. Stalder, T. Deller, M. Staufenbiel, P. M. Mathews, and M. Jucker. 2002. Cerebral hemorrhage after passive anti-Abeta immunotherapy. Science 298: 1379. (Pubitemid 35346131)
55. Racke, M. M., L. I. Boone, D. L. Hepburn, M. Parsadainian, M. T. Bryan, D. K. Ness, K. S. Piroozi, W. H. Jordan, D. D. Brown, W. P. Hoffman, et al. 2005. Exacerbation of cerebral amyloid angiopathy-associated microhemorrhage in amyloid precursor protein transgenic mice by immunotherapy is dependent on antibody recognition of deposited forms of amyloid beta. J. Neurosci. 25: 629-636.