Microglial C5aR (CD88) expression correlates with amyloid-β deposition in murine models of Alzheimer's disease

Journal of Neurochemistry

Volumn 113, Issue 2, 2010, Pages 389-401

  Ager, Rahasson R ^a   Fonseca, Maria I ^a   Chu, Shu Hui ^a   Sanderson, Sam D ^b   Taylor, Stephen M ^c   Woodruff, Trent M ^c   Tenner, Andrea J ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF NEBRASKA AT OMAHA   (United States)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's Disease; C5a receptor; Complement; Microglia; Murine models; Neuroinflammation

Indexed keywords

AMYLOID BETA PROTEIN; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C4; COMPLEMENT COMPONENT C5A RECEPTOR; THIOFLAVINE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; ASTROCYTE; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM; CONTROLLED STUDY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; WESTERN BLOTTING;

AGE FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANIMALS, NEWBORN; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MUTATION; NEURONS; PEPTIDES, CYCLIC; RECEPTOR, ANAPHYLATOXIN C5A; STATISTICS AS TOPIC;

MURINAE; MUS MUSCULUS;

EID: 77949725218     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06595.x     Document Type: Article

References (57)

1. Afagh A., Cummings B. J., Cribbs D. H., Cotman C. W. Tenner A. J. (1996) Localization and cell association of C1q in Alzheimer's disease brain. Exp. Neurol. 138, 22 32.
2. Bao L., Osawe I., Puri T., Lambris J. D., Haas M. Quigg R. J. (2005) C5a promotes development of experimental lupus nephritis which can be blocked with a specific receptor antagonist. Eur. J. Immunol. 35, 2496 2506.
3. Blurton-Jones M., Kitazawa M., Martinez-Coria H., Castello N. A., Muller F. J., Loring J. F., Yamasaki T. R., Poon W. W., Green K. N. LaFerla F. M. (2009) Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc. Natl Acad. Sci. USA 106, 13594 13599.
4. Bonifati D. M. Kishore U. (2007) Role of complement in neurodegeneration and neuroinflammation. Mol. Immunol. 44, 999 1010.
5. Botto M., Dell'agnola C., Bygrave A. E., Thompson E. M., Cook H. T., Petry F., Loos M., Pandolfi P. P. Walport M. J. (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19, 56 59.
6. Bradt B. M., Kolb W. P. Cooper N. R. (1998) Complement-dependent proinflammatory properties of the Alzheimer's disease β-peptide. J. Exp. Med. 188, 431 438.
7. Cheng I. H., Palop J. J., Esposito L. A., Bien-Ly N., Yan F. Mucke L. (2004) Aggressive amyloidosis in mice expressing human amyloid peptides with the Arctic mutation. Nat. Med. 10, 1190 1192.
8. Eikelenboom P. Stam F. C. (1982) Immunoglobulins and complement factors in senile plaques. Acta Neuropathol. 57, 239 242.
9. Eikelenboom P., Hack C. E., Rozemuller J. M. Stam F. C. (1989) Complement activation in amyloid plaques in Alzheimer's dementia. Virchows Arch. B Cell Pathol. 56, 259 262.
10. Fan R. Tenner A. J. (2004) Complement C1q expression induced by Abeta in rat hippocampal organotypic slice cultures. Exp. Neurol. 185, 241 253.
11. Farkas I., Baranyi L., Takahashi M., Fukuda A., Liposits Z., Yamamoto T. Okada H. (1998) A neuronal C5a receptor and an associated apoptotic signal transduction pathway. J. Physiol. 507 (Pt 3 679 687.
12. Farkas I., Takahashi M., Fukuda A., Yamamoto N., Akatsu H., Baranyi L., Tateyama H., Yamamoto T., Okada N. Okada H. (2003) Complement C5a receptor-mediated signaling may be involved in neurodegeneration in Alzheimer's disease. J. Immunol. 170, 5764 5771.
13. Fassbender K., Walter S., Kuhl S. et al. (2004) The LPS receptor (CD14) links innate immunity with Alzheimer's disease. FASEB J. 18, 203 205.
14. Flaherty P., Radhakrishnan M. L., Dinh T., Rebres R. A., Roach T. I., Jordan M. I. Arkin A. P. (2008) A dual receptor crosstalk model of G-protein-coupled signal transduction. PLoS Comput. Biol. 4, e1000185.
15. Fonseca M. I., Zhou J., Botto M. Tenner A. J. (2004) Absence of C1q leads to less neuropathology in transgenic mouse models of Alzheimer's disease. J. Neurosci. 24, 6457 6465.
16. Fonseca M. I., Ager R. R., Chu S. H., Yazan O., Sanderson S. D., LaFerla F. M., Taylor S. M., Woodruff T. M. Tenner A. J. (2009) Treatment with a C5aR antagonist decreases pathology and enhances behavioral performance in murine models of Alzheimer's disease. J. Immunol. 183, 1375 1383.
17. Fraser D. A., Pisalyaput K. Tenner A. J. (2010) C1q enhances microglial clearance of apoptotic neurons and neuronal blebs, and modulates subsequent inflammatory cytokine production. J. Neurochem. 112, 733 743.
18. Gasque P., Singhrao S. K., Neal J. W., Gotze O. Morgan B. P. (1997) Expression of the receptor for complement C5a (CD88) is up-regulated on reactive astrocytes, microglia, and endothelial cells in the inflamed human central nervous system. Am. J. Pathol. 150, 31 41.
19. Hardy J. (2009) The amyloid hypothesis for Alzheimer's disease: a critical reappraisal. J. Neurochem. 110, 1129 1134.
20. Hawlisch H., Belkaid Y., Baelder R., Hildeman D., Gerard C. Kohl J. (2005) C5a negatively regulates toll-like receptor 4-induced immune responses. Immunity 22, 415 426.
21. Herber D. L., Severance E. G., Cuevas J., Morgan D. Gordon M. N. (2004) Biochemical and histochemical evidence of nonspecific binding of alpha7nAChR antibodies to mouse brain tissue. J. Histochem. Cytochem. 52, 1367 1376.
22. Hollmann T. J., Mueller-Ortiz S. L., Braun M. C. Wetsel R. A. (2008) Disruption of the C5a receptor gene increases resistance to acute Gram-negative bacteremia and endotoxic shock: Opposing roles of C3a and C5a. Mol. Immunol. 45, 1907 1915.
23. Hopken U. E., Lu B., Gerard N. P. Gerard C. (1996) The C5a chemoattractant receptor mediates mucosal defence to infection. Nature 383, 86 89.
24. Hsiao K. K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F. Cole G. (1996) Correlative memory deficits, Aβ elevations, and amyloid plaques in transgenic mice. Science 274, 99 102.
25. Jana M., Palencia C. A. Pahan K. (2008) Fibrillar amyloid-beta peptides activate microglia via TLR2: implications for Alzheimer's disease. J. Immunol. 181, 7254 7262.
26. Kiafard Z., Tschernig T., Schweyer S., Bley A., Neumann D. Zwirner J. (2007) Use of monoclonal antibodies to assess expression of anaphylatoxin receptors in tubular epithelial cells of human, murine and rat kidneys. Immunobiology 212, 129 139.
27. Lacy M., Jones J., Whittemore S. R., Haviland D. L., Wetsel R. A. Barnum S. R. (1995) Expression of the receptors for the C5a anaphylatoxin, interleukin-8 and FMLP by human astrocytes and microglia. J. Neuroimmunol. 61, 71 78.
28. Li M., Pisalyaput K., Galvan M. Tenner A. J. (2004) Macrophage colony stimulatory factor and interferon-gamma trigger distinct mechanisms for augmentation of beta-amyloid-induced microglia-mediated neurotoxicity. J. Neurochem. 91, 623 633.
29. Maier M., Peng Y., Jiang L., Seabrook T. J., Carroll M. C. Lemere C. A. (2008) Complement C3 deficiency leads to accelerated amyloid beta plaque deposition and neurodegeneration and modulation of the microglia/macrophage phenotype in amyloid precursor protein transgenic mice. J. Neurosci. 28, 6333 6341.
30. McGeer P. L. McGeer E. G. (2002) Local neuroinflammation and the progression of Alzheimer's disease. J. Neurovirol. 8, 529 538.
31. Moser N., Mechawar N., Jones I. et al. (2007) Evaluating the suitability of nicotinic acetylcholine receptor antibodies for standard immunodetection procedures. J. Neurochem. 102, 479 492.
32. Nataf S., Davoust N. Barnum S. R. (1998) Kinetics of anaphylatoxin C5a receptor expression during experimental allergic encephalomyelitis. J. Neuroimmunol. 91, 147 155.
33. O'Barr S. Cooper N. R. (2000) The C5a complement activation peptide increases IL-1beta and IL-6 release from amyloid-beta primed human monocytes: implications for Alzheimer's disease. J. Neuroimmunol. 109, 87 94.
34. O'Barr S. A., Caguioa J., Gruol D., Perkins G., Ember J. A., Hugli T. Cooper N. R. (2001) Neuronal expression of a functional receptor for the C5a complement activation fragment. J. Immunol. 166, 4154 4162.
35. Oddo S., Caccamo A., Shepherd J. D., Murphy M. P., Golde T. E., Kayed R., Metherate R., Mattson M. P., Akbari Y. LaFerla F. M. (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39, 409 421.
36. Paradisis P. M., Campbell I. L. Barnum S. R. (1998) Elevated complement C5a receptor expression on neurons and glia in astrocyte-targeted interleukin-3 transgenic mice. Glia 24, 338 345.
37. Patel S. N., Berghout J., Lovegrove F. E. et al. (2008) C5 deficiency and C5a or C5aR blockade protects against cerebral malaria. J. Exp. Med. 205, 1133 1143.
38. Pimplikar S. W. (2009) Reassessing the amyloid cascade hypothesis of Alzheimer's disease. Int. J. Biochem. Cell Biol. 41, 1261 1268.
39. Pisalyaput K. Tenner A. J. (2008) Complement component C1q inhibits beta-amyloid- and serum amyloid P-induced neurotoxicity via caspase- and calpain-independent mechanisms. J. Neurochem. 104, 696 707.
40. Rogers J., Cooper N. R., Webster S. et al. (1992) Complement activation by beta-amyloid in Alzheimer disease. Proc. Natl Acad. Sci. 89, 10016 10020.
41. Seelen M. A., Roos A. Daha M. R. (2005) Role of complement in innate and autoimmunity. J. Nephrol. 18, 642 653.
42. Selkoe D. J. Schenk D. (2003) Alzheimer's disease: molecular understanding predicts amyloid-based therapeutics. Annu. Rev. Pharmacol. Toxicol. 43, 545 584.
43. Stahel P. F., Frei K., Eugster H. P., Fontana A., Hummel K. M., Wetsel R. A., Ames R. S. Barnum S. R. (1997) TNF-alpha-mediated expression of the receptor for anaphylatoxin C5a on neurons in experimental Listeria meningoencephalitis. J. Immunol. 159, 861 869.
44. Strohmeyer R., Shen Y. Rogers J. (2000) Detection of complement alternative pathway mRNA and proteins in the Alzheimer's disease brain. Brain Res. Mol. Brain Res. 81, 7 18.
45. Tenner A. J. Fonseca M. I. (2006) The double-edged flower: roles of complement protein C1q in neurodegenerative diseases. Adv. Exp. Med. Biol. 586, 153 176.
46. Terry R. D., Masliah E., Salmon D. P., Butters N., DeTeresa R., Hill R., Hansen L. A. Katzman R. (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572 580.
47. Tschernig T., Kiafard Z., Dibbert C., Neumann D. Zwirner J. (2007) Use of monoclonal antibodies to assess expression of anaphylatoxin receptors in rat and murine models of lung inflammation. Exp. Toxicol. Pathol. 58, 419 425.
48. Van B. J., Bernaudin M., Petit E., Gasque P., Nouvelot A., MacKenzie E. T. Fontaine M. (2000) Expression of receptors for complement anaphylatoxins C3a and C5a following permanent focal cerebral ischemia in the mouse. Exp. Neurol. 161, 373 382.
49. Walter S., Letiembre M., Liu Y. et al. (2007) Role of the toll-like receptor 4 in neuroinflammation in Alzheimer's disease. Cell Physiol. Biochem. 20, 947 956.
50. Woodruff T. M., Costantini K. J., Crane J. W., Atkin J. D., Monk P. N., Taylor S. M. Noakes P. G. (2008) The complement factor C5a contributes to pathology in a rat model of amyotrophic lateral sclerosis. J. Immunol. 181, 8727 8734.
51. Woodruff T. M., Ager R. R., Tenner A. J., Noakes P. G. Taylor S. M. (2009) The Role of the Complement System and the Activation Fragment C5a in the Central Nervous System. Neuromolecular Med. doi :.
52. Wyss-Coray T., Yan F., Lin A. H., Lambris J. D., Alexander J. J., Quigg R. J. Masliah E. (2002) Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice. Proc. Natl Acad. Sci. USA 99, 10837 10842.
53. Yao J., Harvath L., Gilbert D. L. Colton C. A. (1990) Chemotaxis by a CNS macrophage, the microglia. J. Neurosci. Res. 27, 36 42.
54. Yasojima K., Schwab C., McGeer E. G. McGeer P. L. (1999) Up-regulated production and activation of the complement system in Alzheimer's disease brain. Am. J. Pathol. 154, 927 936.
55. Zanjani H., Finch C. E., Kemper C., Atkinson J., McKeel D., Morris J. C. Price J. L. (2005) Complement activation in very early Alzheimer disease. Alzheimer Dis. Assoc. Disord. 19, 55 66.
56. Zhang X., Kimura Y., Fang C., Zhou L., Sfyroera G., Lambris J. D., Wetsel R. A., Miwa T. Song W. C. (2007) Regulation of Toll-like receptor-mediated inflammatory response by complement in vivo. Blood 110, 228 236.
57. Zhou J., Fonseca M. I., Pisalyaput K. Tenner A. J. (2008) Complement C3 and C4 expression in C1q sufficient and deficient mouse models of Alzheimer's disease. J. Neurochem. 106, 2080 2092.