Scara1 deficiency impairs clearance of soluble amyloid-β by mononuclear phagocytes and accelerates Alzheimer's-like disease progression

Nature Communications

Volumn 4, Issue , 2013, Pages

  Frenkel, Dan ^a   Wilkinson, Kim ^b   Zhao, Lingzhi ^b   Hickman, Suzanne E ^b   Means, Terry K ^b   Puckett, Lindsay ^b   Farfara, Dorit ^a   Kingery, Nathan D ^b   Weiner, Howard L ^c   El Khoury, Joseph ^b,d  

^a TEL AVIV UNIVERSITY   (Israel)

^b Center for Immunology and Inflammatory Diseases   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; SCAVENGER RECEPTOR; SHORT HAIRPIN RNA; CD36 ANTIGEN; CYSTEINE PROTEINASE; LIPOPOLYSACCHARIDE; MSR1 PROTEIN, MOUSE; PRESENILIN 1; PROTOLLIN; SCAVENGER RECEPTOR A; SMALL INTERFERING RNA; DRUG COMBINATION;

ADULT; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOACCUMULATION; BONE MARROW CELL; CLEARANCE; CONTROLLED STUDY; DISEASE COURSE; GENE EXPRESSION REGULATION; IN VIVO STUDY; MICROGLIA; MONONUCLEAR PHAGOCYTE; MORTALITY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RECEPTOR GENE; SCARA1 GENE; UPREGULATION; ANIMAL; CELL STRAIN HEK293; DRUG COMBINATION; DRUG EFFECT; HUMAN; MACROPHAGE; METABOLISM; MONONUCLEAR CELL; PATHOLOGY; PHAGOCYTE; PROTEIN DEGRADATION; SOLUBILITY; SURVIVAL; DEFICIENCY; DRUG EFFECTS; HEK293 CELL LINE;

MUS;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANTIGENS, CD36; CYSTEINE ENDOPEPTIDASES; DISEASE PROGRESSION; DRUG COMBINATIONS; HEK293 CELLS; HUMANS; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICROGLIA; PHAGOCYTES; PRESENILIN-1; PROTEOLYSIS; RNA, SMALL INTERFERING; SCAVENGER RECEPTORS, CLASS A; SOLUBILITY; SURVIVAL ANALYSIS; UP-REGULATION;

EID: 84883361779     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3030     Document Type: Article

References (39)

1. El Khoury, J. et al. Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat. Med. 13, 432-438 (2007).
2. Hawkes, C. A. & McLaurin, J. Selective targeting of perivascular macrophages for clearance of beta-amyloid in cerebral amyloid angiopathy. Proc. Natl Acad. Sci. USA 106, 1261-1266 (2009).
3. Town, T. et al. Blocking TGF-beta-Smad2/3 innate immune signalling mitigates Alzheimer-like pathology. Nat. Med. 14, 681-687 (2008).
4. Hickman, S. E., Allison, E. K. & El Khoury, J. Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J. Neurosci. 28, 8354-8360 (2008).
5. El Khoury, J. B. et al. CD36 mediates the innate host response to beta-amyloid. J. Exp. Med. 197, 1657-1666 (2003).
6. Lue, L. F. et al. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155, 853-862 (1999).
7. McLean, C. A. et al. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 46, 860-866 (1999).
8. Wang, J., Dickson, D. W., Trojanowski, J. Q. & Lee, V. M. The levels of soluble versus insoluble brain Abeta distinguish Alzheimer's disease from normal and pathologic aging. Exp. Neurol. 158, 328-337 (1999).
9. Haass, C. & Selkoe, D. J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat. Rev. Mol. Cell. Biol. 8, 101-112 (2007).
10. Sakono, M. & Zako, T. Amyloid oligomers: formation and toxicity of Abeta oligomers. FEBS J. 277, 1348-1358 (2010).
11. Lesne, S. et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440, 352-357 (2006).
12. Walsh, D. M. et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539 (2002).
13. Nimmerjahn, A., Kirchhoff, F. & Helmchen, F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314-1318 (2005).
14. El Khoury, J. et al. Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils. Nature 382, 716-719 (1996).
15. Coraci, I. S. et al. CD36, a class B scavenger receptor, is expressed on microglia in Alzheimer's disease brains and can mediate production of reactive oxygen species in response to beta-amyloid fibrils. Am. J. Pathol. 160, 101-112 (2002).
16. Yan, S. D. et al. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 382, 685-691 (1996).
17. El Khoury Joseph, Hickman Suzanne E. Mechanisms of Amyloid B Clearance in Alzheimer's Disease (Nova Biomedical Books, New York, 2009).
18. Moffat, J. et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124, 1283-1298 (2006).
19. Means, T. K. et al. Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. J. Exp. Med. 206, 637-653 (2009).
20. Wilkinson, K., Boyd, J. D., Glicksman, M., Moore, K. J. & El Khoury, J. A high-content drug screen identifies ursolic acid as an inhibitor of amyloid-{beta} interactions with its receptor CD36. J. Biol. Chem. 286, 34914-34922 (2011).
21. Stewart, C. R. et al. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 11, 155-161 (2010).
22. Maxeiner, H. et al. Complementary roles for scavenger receptor A and CD36 of human monocyte-derived macrophages in adhesion to surfaces coated with oxidized low-density lipoproteins and in secretion of H2O2. J. Exp. Med. 188, 2257-2265 (1998).
23. Fries, L. F. et al. Safety and immunogenicity of a proteosome-Shigella flexneri 2a lipopolysaccharide vaccine administered intranasally to healthy adults. Infect. Immun. 69, 4545-4553 (2001).
24. Frenkel, D., Maron, R., Burt, D. S. & Weiner, H. L. Nasal vaccination with a proteosome-based adjuvant and glatiramer acetate clears beta-amyloid in a mouse model of Alzheimer disease. J. Clin. Invest. 115, 2423-2433 (2005).
25. Frenkel, D. et al. A nasal proteosome adjuvant activates microglia and prevents amyloid deposition. Ann. Neurol. 63, 591-601 (2008).
26. Wyss-Coray, T. et al. Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat. Med. 9, 453-457 (2003).
27. El Khoury, J. Neurodegeneration and the neuroimmune system. Nat. Med. 16, 1369-1370.
28. Grathwohl, S. A. et al. Formation and maintenance of Alzheimer's disease beta-amyloid plaques in the absence of microglia. Nat. Neurosci. 12, 1361-1363 (2009).
29. Bruban, J. et al. CCR2/CCL2-mediated inflammation protects photoreceptor cells from amyloid-beta-induced apoptosis. Neurobiol. Dis. 42, 55-72 (2011).
30. Reed-Geaghan, E. G., Reed, Q. W., Cramer, P. E. & Landreth, G. E. Deletion of CD14 attenuates Alzheimer's disease pathology by influencing the brain's inflammatory milieu. J. Neurosci. 30, 15369-15373 (2010).
31. Song, M. et al. TLR4 mutation reduces microglial activation, increases Abeta deposits and exacerbates cognitive deficits in a mouse model of Alzheimer's disease. J. Neuroinflammation 8, 92 (2011).
32. Mildner, A. et al. Distinct and non-redundant roles of microglia and myeloid subsets in mouse models of Alzheimer's disease. J. Neurosci. 31, 11159-11171 (2011).
33. Borchelt, D. R. et al. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19, 939-945 (1997).
34. Jankowsky, J. L. et al. Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol. Eng. 17, 157-165 (2001).
35. Thomas, C. A. et al. Protection from lethal gram-positive infection by macrophage scavenger receptor-dependent phagocytosis. J. Exp. Med. 191, 147-156 (2000).
36. Mehta, J. L. et al. Deletion of LOX-1 reduces atherogenesis in LDLR knockout mice fed high cholesterol diet. Circ. Res. 100, 1634-1642 (2007).
37. Yonekura, H., Yamamoto, Y., Sakurai, S., Watanabe, T. & Yamamoto, H. Roles of the receptor for advanced glycation endproducts in diabetes-induced vascular injury. J. Pharmacol. Sci. 97, 305-311 (2005).
38. el Khoury, J. et al. Macrophages adhere to glucose-modified basement membrane collagen IV via their scavenger receptors. J. Biol. Chem. 269, 10197-10200 (1994).
39. Hickman, S. E., el Khoury, J., Greenberg, S., Schieren, I. & Silverstein, S. C. P2Z adenosine triphosphate receptor activity in cultured human monocyte-derived macrophages. Blood 84, 2452-2456 (1994).