A shift in microglial β-amyloid binding in Alzheimer's disease is associated with cerebral amyloid angiopathy

Brain Pathology

Volumn 23, Issue 4, 2013, Pages 390-401

  Zabel, Matthew ^a   Schrag, Matthew ^a,b   Crofton, Andrew ^a   Tung, Spencer ^c   Beaufond, Pierre ^a   Van Ornam, Jon ^a   Dininni, Angie ^a   Vinters, Harry V ^c   Coppola, Giovanni ^c   Kirsch, Wolff M ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

M 2; ApoE E4; CR1; CR3; Mac 1; morphology

Indexed keywords

ALPHA 2 MACROGLOBULIN; AMYLOID BETA PROTEIN; APOLIPOPROTEIN E4; CD11B ANTIGEN; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C3B RECEPTOR; COMPLEMENT MEMBRANE ATTACK COMPLEX;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; AUTOPSY; BRAIN BLOOD VESSEL; BRAIN HOMOGENATE; CLINICAL ARTICLE; COMPLEMENT ACTIVATION; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOLYSIS; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOPRECIPITATION; MALE; MICROGLIA; MICROVASCULATURE; OCCIPITAL CORTEX; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; VASCULAR AMYLOIDOSIS;

ACTINS; ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID; AMYLOID BETA-PEPTIDES; ANALYSIS OF VARIANCE; ANTIGENS, CD; ANTIGENS, CD11B; BRAIN; CEREBRAL AMYLOID ANGIOPATHY; COMPLEMENT MEMBRANE ATTACK COMPLEX; FEMALE; HUMANS; IMMUNOPRECIPITATION; MALE; MICROGLIA; MICROVESSELS; MIDDLE AGED; PEPTIDE FRAGMENTS; RECEPTORS, COMPLEMENT;

EID: 84879246476     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/bpa.12005     Document Type: Article

References (51)

1. Adolfsson O, Pihlgren M, Toni N, Varisco Y, Buccarello AL, Antoniello K, et al (2012) An effector-reduced anti-beta-amyloid (Abeta) antibody with unique abeta binding properties promotes neuroprotection and glial engulfment of Abeta. J Neurosci 32: 9677-9689.
2. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21: 383-421.
3. Akiyama H, McGeer PL, (1990) Brain microglia constitutively express beta-2 integrins. J Neuroimmunol 30: 81-93.
4. Bell RD, Deane R, Chow N, Long X, Sagare A, Singh I, et al (2009) SRF and myocardin regulate LRP-mediated amyloid-beta clearance in brain vascular cells. Nat Cell Biol 11: 143-153.
5. Biffi A, Shulman JM, Jagiella JM, Cortellini L, Ayres AM, Schwab K, et al (2012) Genetic variation at CR1 increases risk of cerebral amyloid angiopathy. Neurology 78: 334-341.
6. Braak H, Braak E, (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82: 239-259.
7. Bradt BM, Kolb WP, Cooper NR, (1998) Complement-dependent proinflammatory properties of the Alzheimer's disease beta-peptide. J Exp Med 188: 431-438.
8. Choucair-Jaafar N, Laporte V, Levy R, Poindron P, Lombard Y, Gies JP, (2010) Complement receptor 3 (CD11b/CD18) is implicated in the elimination of beta-amyloid peptides. Fundam Clin Pharmacol 25: 115-122.
9. Donahue JE, Flaherty SL, Johanson CE, Duncan JA, 3rd, Silverberg GD, Miller MC, et al (2006) RAGE, LRP-1, and amyloid-beta protein in Alzheimer's disease. Acta Neuropathol 112: 405-415.
10. Gallagher JJ, Finnegan ME, Grehan B, Dobson J, Collingwood JF, Lynch MA, (2011) Modest amyloid deposition is associated with iron dysregulation, microglial activation, and oxidative stress. J Alzheimers Dis 28: 147-161.
11. Graeber MB, Streit WJ, (2010) Microglia: biology and pathology. Acta Neuropathol 119: 89-105.
12. Greenberg SM, Vonsattel JP, (1997) Diagnosis of cerebral amyloid angiopathy. Sensitivity and specificity of cortical biopsy. Stroke 28: 1418-1422.
13. Hanisch UK, Kettenmann H, (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394.
14. Hughes SR, Khorkova O, Goyal S, Knaeblein J, Heroux J, Riedel NG, Sahasrabudhe S, (1998) Alpha2-macroglobulin associates with beta-amyloid peptide and prevents fibril formation. Proc Natl Acad Sci U S A 95: 3275-3280.
15. Jellinger KA, Attems J, (2005) Prevalence and pathogenic role of cerebrovascular lesions in Alzheimer disease. J Neurol Sci 229-230: 37-41.
16. Johnson KA, Gregas M, Becker JA, Kinnecom C, Salat DH, Moran EK, et al (2007) Imaging of amyloid burden and distribution in cerebral amyloid angiopathy. Ann Neurol 62: 229-234.
17. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A, (2011) Physiology of microglia. Physiol Rev 91: 461-553.
18. Khera R, Das N, (2009) Complement receptor 1: disease associations and therapeutic implications. Mol Immunol 46: 761-772.
19. Kirsch W, McAuley G, Holshouser B, Petersen F, Ayaz M, Vinters HV, et al (2009) Serial susceptibility weighted MRI measures brain iron and microbleeds in dementia. J Alzheimers Dis 17: 599-609.
20. Kolev MV, Tediose T, Sivasankar B, Harris CL, Thome J, Morgan BP, Donev RM, (2010) Upregulating CD59: a new strategy for protection of neurons from complement-mediated degeneration. Pharmacogenomics J 10: 12-19.
21. Lauer D, Reichenbach A, Birkenmeier G, (2001) Alpha 2-macroglobulin- mediated degradation of amyloid beta 1-42: a mechanism to enhance amyloid beta catabolism. Exp Neurol 167: 385-392.
22. Liu Z, Condello C, Schain A, Harb R, Grutzendler J, (2010) CX3CR1 in microglia regulates brain amyloid deposition through selective protofibrillar amyloid-beta phagocytosis. J Neurosci 30: 17091-17101.
23. Lopes KO, Sparks DL, Streit WJ, (2008) Microglial dystrophy in the aged and Alzheimer's disease brain is associated with ferritin immunoreactivity. Glia 56: 1048-1060.
24. Maier M, Peng Y, Jiang L, Seabrook TJ, Carroll MC, Lemere CA, (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.
25. McGeer PL, McGeer EG, (2002) The possible role of complement activation in Alzheimer disease. Trends Mol Med 8: 519-523.
26. McGeer PL, Walker DG, Pitas RE, Mahley RW, McGeer EG, (1997) Apolipoprotein E4 (ApoE4) but not ApoE3 or ApoE2 potentiates beta-amyloid protein activation of complement in vitro. Brain Res 749: 135-138.
27. Mikhailenko I, Battey FD, Migliorini M, Ruiz JF, Argraves K, Moayeri M, Strickland DK, (2001) Recognition of alpha 2-macroglobulin by the low density lipoprotein receptor-related protein requires the cooperation of two ligand binding cluster regions. J Biol Chem 276: 39484-39491.
28. Narita M, Holtzman DM, Schwartz AL, Bu G, (1997) Alpha2-macroglobulin complexes with and mediates the endocytosis of beta-amyloid peptide via cell surface low-density lipoprotein receptor-related protein. J Neurochem 69: 1904-1911.
29. Nicoll JA, Yamada M, Frackowiak J, Mazur-Kolecka B, Weller RO, (2004) Cerebral amyloid angiopathy plays a direct role in the pathogenesis of Alzheimer's disease. Pro-CAA position statement. Neurobiol Aging 25: 589-597. discussion 603-4.
30. Perry VH, O'Connor V, (2008) C1q: the perfect complement for a synaptic feast? Nat Rev Neurosci 9: 807-811.
31. Pfeifer M, Boncristiano S, Bondolfi L, Stalder A, Deller T, Staufenbiel M, et al (2002) Cerebral hemorrhage after passive anti-Abeta immunotherapy. Science 298: 1379.
32. Racke MM, Boone LI, Hepburn DL, Parsadainian M, Bryan MT, Ness DK, 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.
33. Ramaglia V, Hughes TR, Donev RM, Ruseva MM, Wu X, Huitinga I, et al (2012) C3-dependent mechanism of microglial priming relevant to multiple sclerosis. Proc Natl Acad Sci U S A 109: 965-970.
34. Rogers J, Cooper NR, Webster S, Schultz J, McGeer PL, Styren SD, et al (1992) Complement activation by beta-amyloid in Alzheimer disease. Proc Natl Acad Sci U S A 89: 10016-10020.
35. Rogers J, Li R, Mastroeni D, Grover A, Leonard B, Ahern G, et al (2006) Peripheral clearance of amyloid beta peptide by complement C3-dependent adherence to erythrocytes. Neurobiol Aging 27: 1733-1739.
36. Schrag M, McAuley G, Pomakian J, Jiffry A, Tung S, Mueller C, et al (2009) Correlation of hypointensities in susceptibility-weighted images to tissue histology in dementia patients with cerebral amyloid angiopathy: a postmortem MRI study. Acta Neuropathol 119: 291-302.
37. Shibata M, Yamada S, Kumar SR, Calero M, Bading J, Frangione B, et al (2000) Clearance of Alzheimer's amyloid-ss(1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J Clin Invest 106: 1489-1499.
38. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, et al (2010) Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7: 483-495.
39. Soontornniyomkij V, Lynch MD, Mermash S, Pomakian J, Badkoobehi H, Clare R, Vinters HV, (2010) Cerebral microinfarcts associated with severe cerebral beta-amyloid angiopathy. Brain Pathol 20: 459-467.
40. Streit WJ, Braak H, Xue QS, Bechmann I, (2009) Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer's disease. Acta Neuropathol 118: 475-485.
41. Tremblay ME, Stevens B, Sierra A, Wake H, Bessis A, Nimmerjahn A, (2011) The role of microglia in the healthy brain. J Neurosci 31: 16064-16069.
42. Vinters HV, (1987) Cerebral amyloid angiopathy. A critical review. Stroke 18: 311-324.
43. Vinters HV, Gilbert JJ, (1983) Cerebral amyloid angiopathy: incidence and complications in the aging brain. II. The distribution of amyloid vascular changes. Stroke 14: 924-928.
44. Webster S, Bradt B, Rogers J, Cooper N, (1997) Aggregation state-dependent activation of the classical complement pathway by the amyloid beta peptide. J Neurochem 69: 388-398.
45. Weller RO, Boche D, Nicoll JA, (2009) Microvasculature changes and cerebral amyloid angiopathy in Alzheimer's disease and their potential impact on therapy. Acta Neuropathol 118: 87-102.
46. Wilcock DM, Colton CA, (2009) Immunotherapy, vascular pathology, and microhemorrhages in transgenic mice. CNS Neurol Disord Drug Targets 8: 50-64.
47. Wirenfeldt M, Babcock AA, Vinters HV, (2011) Microglia-insights into immune system structure, function, and reactivity in the central nervous system. Histol Histopathol 26: 519-530.
48. Wyss-Coray T, Yan F, Lin AH, Lambris JD, Alexander JJ, Quigg RJ, Masliah E, (2002) Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice. Proc Natl Acad Sci U S A 99: 10837-10842.
49. Yang LB, Li R, Meri S, Rogers J, Shen Y, (2000) Deficiency of complement defense protein CD59 may contribute to neurodegeneration in Alzheimer's disease. J Neurosci 20: 7505-7509.
50. Yasojima K, McGeer EG, McGeer PL, (1999) Complement regulators C1 inhibitor and CD59 do not significantly inhibit complement activation in Alzheimer disease. Brain Res 833: 297-301.
51. Yerbury JJ, Kumita JR, Meehan S, Dobson CM, Wilson MR, (2009) alpha2-Macroglobulin and haptoglobin suppress amyloid formation by interacting with prefibrillar protein species. J Biol Chem 284: 4246-4254.