A cell surface receptor complex for fibrillar β-amyloid mediates microglial activation

Journal of Neuroscience

Volumn 23, Issue 7, 2003, Pages 2665-2674

  Bamberger, Maria E ^a   Harris, Meera E ^a   McDonald, Douglas R ^b   Husemann, Jens ^c   Landreth, Gary E ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c Columbia Univ Coll of Phys/Surgs ^*  (United States)

Author keywords

Alzheimer's disease; CD36; CD47; Microglia; Receptors; Scavenger receptor; Signal transduction; THP 1 monocytes; Tyr kinase; 6 1 integrin; amyloid

Indexed keywords

ALPHA6 INTEGRIN; AMYLOID BETA PROTEIN; BETA1 INTEGRIN; CD36 ANTIGEN; CD47 ANTIGEN; CELL SURFACE RECEPTOR; INTERLEUKIN 1BETA; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; SCAVENGER RECEPTOR;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL ADHESION; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; INFLAMMATION; INFLAMMATORY CELL; MICROGLIA; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENILE PLAQUE; SIGNAL TRANSDUCTION;

EID: 0037387147     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-07-02665.2003     Document Type: Article

References (74)

1. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyoma I, Van Muiswinkel FL, Veerhuis R, Walker D, Webster S, Wegrzyniak B, Wenk G, Wyss-Coray T (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21:383-421.
2. Araujo DM, Cotman CW (1992) Beta-amyloid stimulates glial cells in vitro to produce growth factors that accumulate in senile plaques in Alzheimer's disease. Brain Res 569:141-145.
3. Babic I, Schallhorn A, Lindberg FP, Jirik FR (2000) SHPS-1 induces aggregation of Ba/F3 pro-B cells via an interaction with CD47. J Immunol 164:3652-3658.
4. Bianca VD, Dusi S, Bianchini E, Dal Pra I, Rossi F (1999) beta-amyloid activates the O-2 forming NADPH oxidase in microglia, monocytes, and neutrophils: a possible inflammatory mechanism of neuronal damage in Alzheimer's disease. J Biol Chem 274:15493-15499.
5. Boland K, Behrens M, Choi D, Manias K, Perlmutter DH (1996) The serpinenzyme complex receptor recognizes soluble, nontoxic amyloid-β peptide but not aggregated, cytotoxic amyloid-β peptide. J Biol Chem 271:18032-18044.
6. Bornstein P (1995) Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol 130:503-506.
7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
8. Breitner JC (1996) The role of anti-inflammatory drugs in the prevention and treatment of Alzheimer's disease. Annu Rev Med 47:401-411.
9. Brown EJ, Frazier WA (2001) Integrin-associated protein (CD47) and its ligands. Trends Cell Biol 11:130-135.
10. Bull HA, Brickell PM, Dowd PM (1994) Src-related protein tyrosine kinases are physically associated with the surface antigen CD36 in human dermal microvascular endothelial cells. FEBS Lett 351:41-44.
11. Burdick D, Soreghan B, Kwon M, Kosmoski J, Knauer M, Henschen A, Yates J, Cotman C, Glabe C (1992) Assembly and aggregation properties of synthetic Alzheimer's A4/beta amyloid peptide analogs. J Biol Chem 267:546-554.
12. Chen LM, Bailey D, Fernandez-Valle C (2000) Association of beta 1 integrin with focal adhesion kinase and paxillin in differentiating Schwann cells. J Neurosci 20:3776-3784.
13. Chung J, Gao AG, Frazier WA (1997) Thrombospondin acts via integrinassociated protein to activate the platelet integrin alphaIIbbeta3. J Biol Chem 272:14740-14746.
14. Chung J, Wang XQ, Lindberg FP, Frazier WA (1999) Thrombospondin-1 acts via IAP/CD47 to synergize with collagen in alpha2beta1-mediated platelet activation. Blood 94:642-648.
15. Combs CK, Johnson DJ, Cannady SB, Lehman TM, Landreth GE (1999) Identification of microglial signal transduction pathways mediating a neurotoxic response to amyloidogenic fragments of β-amyloid and prion proteins. J Neurosci 19:928-939.
16. Combs CK, Johnson DE, Karlo JC, Cannady SB, Landreth GE (2000) Inflammatory mechanisms in Alzheimer's disease: inhibition of β-amyloidstimulated proinflammatory responses and neurotoxicity by PPARgamma agonists J. Neurosci 20:558-567.
17. Combs CK, Karlo JC, Kao SC, Landreth GE (2001) β-Amyloid stimulation of microglia and monocytes results in TNFα-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J Neurosci 21:1179-1188.
18. Coraci IS, Husemann J, Berman JW, Hulette C, Dufour JH, Campanella G, Luster AD, Silverstein SC, El Khoury J (2002) 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 betaamyloid fibrils. Am J Pathol 160:101-112.
19. Dineley KT, Westerman M, Bui D, Bell K, Ashe KH, Sweatt JD (2001) Betaamyloid activates the mitogen-activated protein kinase cascade via hippocampal α7 nicotinic acetylcholine receptors: in vitro and in vivo mechanisms related to Alzheimer's disease. J Neurosci 21:4125-4133.
20. El Khoury J, Hickman SE, Thomas CA, Cao L, Silverstein SC, Loike JD (1996) Scavenger receptor-mediated adhesion of microglia to β-amyloid fibrils. Nature 382:716-719.
21. Fiala M, Zhang L, Gan X, Sherry, B, Taub D, Graves MC, Hama S, Way D, Weinand M, Witte M, Lorton D, Kuo YM, Roher AE (1998) Amyloidbeta induces chemokine secretion and monocyte migration across a human blood-brain barrier model. Mol Med 4:480-489.
22. Frazier WA, Gao AG, Dimitry J, Chung J, Brown EJ, Lindberg FP, Linder ME (1999) The thrombospondin receptor integrin-associated protein (CD47) functionally couples to heterotrimeric Gi. J Biol Chem 274:8554-8560.
23. Gao AG, Lindberg FP, Finn MB, Blystone SD, Brown EJ, Frazier WA (1996) Integrin-associated protein is a receptor for the C-terminal domain of thrombospondin. J Biol Chem 271:21-24.
24. Ghiso J, Rostagno A, Gardella JE, Liem L, Gorevic PD, Frangione B (1992) A 109-amino-acid C-terminal fragment of Alzheimer's-disease amyloid precursor protein contains a sequence, -RHDS-, that promotes cell adhesion. Biochem J 288:1053-1059.
25. Giulian D, Haverkamp LJ, Yu J, Karshin W, Tom D, Li J, Kazanskaia A, Kirkpatrick J, Roher AE (1998) The HHQK domain of beta-amyloid provides a structural basis for the immunopathology of Alzheimer's disease. J Biol Chem 273:29719-29726.
26. Hartung HP, Kladetzky RG, Melnik B, Hennerici M (1986) Stimulation of the scavenger receptor on monocytes-macrophages evokes release of arachidonic acid metabolites and reduced oxygen species. Lab Invest 55:209-216.
27. Hsu HY, Nicholson AC, Hajjar DP (1996) Inhibition of macrophage scavenger receptor activity by tumor necrosis factor-a is transcriptionally and post-transcriptionally regulated. J Biol Chem 271:7767-7773.
28. Huang F, Buttini M, Wyss-Coray T, McCoulogue L, Kodama T, Pitas RE, Mucke L (1999) Elimination ofthe class A scavenger receptor does not affect amyloid plaque formation or neurodegeneration in transgenic mice expressing human amyloid protein precursors. Am J Pathol 155:1741-1747.
29. Huang MM, Bolen JB, Barnwell JW, Shattil SJ, Brugge JS (1991) Membrane glycoprotein IV (CD36) is physically associated with the Fyn, Lyn, and Yes protein-tyrosine kinases in human platelets. Proc Natl Acad Sci USA 88:7844-7848.
30. Husemann J, Loike JD, Kodama T, Silverstein SC (2001) Scavenger receptor class B type I (SR-BI) mediates adhesion of neonatal murine microglia to fibrillar beta-amyloid. J Neuroimmunol 114:142-150.
31. in't Veld BA, Ruitenberg A, Hofman A, Stricker BH, Breteler MM (2001) Antihypertensive drugs and incidence of dementia: the Rotterdam Study. Neurobiol Aging 22:407-412.
32. Ishibashi Y, Claus S, Relman DA (1994) Bordetella pertussis filamentous hemagglutinin interacts with a leukocyte signal transduction complex and stimulates bacterial adherence to monocyte CR3 (CD11b/CD18). J Exp Med 180:1225-1233.
33. Jiang P, Lagenaur CF, Narayanan V (1999) Integrin-associated protein is a ligand for the P84 neural adhesion molecule. J Biol Chem 274:559-562.
34. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6:41-48.
35. Klegeris A, Walker DG, McGeer PL (1994) Activation of macrophages by Alzheimer beta amyloid peptide. Biochem Biophys Res Commun 199:984-991.
36. Kloss CU, Bohatschek M, Kreutzberg GW, Raivich G (2001) Effect of lipopolysaccharide on the morphology and integrin immunoreactivity of ramified microglia in the mouse brain and in cell culture. Exp Neurol 168:32-46.
37. Krieger M, Herz J (1994) Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LRP). Annu Rev Biochem 63:601-637.
38. Le Y, Gong W, Tiffany HL, Tumanov A, Nedospasov S, Shen W, Dunlop NM, Gao JL, Murphy PM, Oppenheim JJ, Wang JM (2001) Amyloid (beta)42 activates a G-protein-coupled chemoattractant receptor, FPR-like-1. J Neurosci 21:RC123(1-5).
39. Lin TH, Rosales C, Mondal K, Bolen JB, Haskill S, Juliano RL (1995) Integrin-mediated tyrosine phosphorylation and cytokine message induction in monocytic cells: a possible signaling role for the Syk-tyrosine kinase. J Biol Chem 270:16189-16197.
40. Lorenzo A, Yankner BA (1994) Beta-amyloid neurotoxicity requires fibril formation and is inhibited by Congo red. Proc Natl Acad Sci USA 91:12243-12247.
41. Lorton D (1997) Beta-amyloid-induced IL-1 beta release from an activated human monocyte cell line is calcium- and G-protein-dependent. Mech Aging Dev 94:199-211.
42. Lorton D, Kocsis JM, King L, Madden K, Brunden KR (1996) Beta-amyloid induces increased release of interleukin-1 beta from lipopolysaccharideactivated human monocytes. J Neuroimmunol 67:21-29.
43. Lue LF, Walker DG, Brachova L, Beach TG, Rogers J, Schmidt AM, Stern DM, Yan SD (2001) Involvement ofmicroglial receptor for advanced glycation end products (RAGE) in Alzheimer's disease: identification of a cellular activation mechanism. Exp Neurol 171:29-45.
44. Mackenzie IR, Munoz DG (1998) Non steroidal anti-inflammatory drug use and Alzheimer-type pathology in aging. Neurology 50:986-990.
45. Matter ML, Zhang Z, Nordstedt C, Ruoslahti E (1998) The alpha5beta1 integrin mediates elimination of amyloid-beta peptide and protects against apoptosis. J Cell Biol 141:1019-1030.
46. 2. J Exp Med 188:2257-2265.
47. McDonald D, Bamberger M, Combs C, Landreth G (1998) β-Amyloid fibril activate parallel mitogen-activated protein kinase pathways in microglia and THP-1 monocytes. J Neurosci 18:4451-4460.
48. McDonald DR, Brunden KR, Landreth GE (1997) Amyloid fibrils activate tyrosine kinase-dependent signaling and superoxide production in microglia. J Neurosci 17:2284-2294.
49. Meda L, Cassatella MA, Szendrei GI, Otvos L, Baron P, Villalba M, Ferrari D, Rossi F (1995) Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374:647-650.
50. Meda L, Bernasconi S, Bonaiuto C, Sozzani S, Zhou D, Otvos Jr L, Mantovani A, Rossi F, Cassatella MA (1996) Beta-amyloid (25-35) peptide and IFN-gamma synergistically induce the production of the chemotactic cytokine MCP-1/JE in monocytes and microglial cells. J Immunol 157:1213-1218.
51. Meda L, Baron P, Prat E, Scarpini E, Scarlato G, Cassatella MA, Rossi F (1999) Proinflammatory profile of cytokine production by human monocytes and murine microglia stimulated with beta-amyloid[25-35]. J Neuroimmunol 93:45-52.
52. Miao WM, Vasile E, Lane WS, Lawler J (2001) CD36 associates with CD9 and integrins on human blood platelets. Blood 97:1689-1696.
53. Moore KJ, El Khoury J, Medeiros LA, Terada K, Geula C, Luster AD, Freeman MW (2002) A CD36-initiated signaling cascade mediates inflammatory effects of beta-amyloid. J Biol Chem 277:49982-49988.
54. Murphy Jr GM, Yang L, Cordell B (1998) Macrophage colony-stimulating factor augments beta-amyloid-induced interleukin-1, interleukin-6, and nitric oxide production by microglial cells. J Biol Chem 273:20967-20971.
55. Paresce DM, Ghosh RN, Maxfield FR (1996) Microglial cells internalize aggregates of the Alzheimer's disease amyloid beta-protein via a scavenger receptor. Neuron 17:553-565.
56. Pearce SFA, Wu J, Silverstein RL (1995) Recombinant GST/CD36 fusion proteins define a thrombospondin binding domain: evidence for a single calcium-dependent binding site on CD36. J Biol Chem 270:2981-2986.
57. Pettit DL, Shao Z, Yakel JL (2001) β-Amyloid(1-42) peptide directly modulates nicotinic receptors in the rat hippocampal slice. J Neurosci 21:RC120(1-5).
58. Pick E (1986) Microassays for superoxide and hydrogen peroxide production and nitroblue tetrazolium reduction using an enzyme immunoassay microplate reader. Methods Enzymol 132:407-421.
59. Pike CJ, Burdick D, Walencewicz AJ, Glabe CG, Cotman CW (1993) Neurodegeneration induced by β-amyloid peptides in vitro: the role of peptide assembly state. J Neurosci 13:1676-1687.
60. Porter JC, Hogg N (1998) Integrins take partners: cross-talk between integrins and other membrane receptors. Trends Cell Biol 8:390-396.
61. Rich JB, Rasmusson DX, Folstein MF, Carson KA, Kawas C, Brandt J (1995) Nonsteroidal anti-inflammatory drugs in Alzheimer's disease. Neurology 45:51-55.
62. Scharnagl H, Tisljar U, Winkler K, Huttinger M, Nauck MA, Gross W, Wieland H, Ohm TG, Marz W (1999) The betaA4 amyloid peptide complexes to and enhances the uptake of beta-very low density lipoproteins by the low density lipoprotein receptor-related protein and heparan sulfate proteoglycans pathway. Lab Invest 79:1271-1286.
63. Stewart WF, Kawas C, Corrada M, Metter EJ (1997) Risk of Alzheimer's disease and duration of NSAID use. Neurology 48:626-632.
64. Terzi E, Holzemann G, Seelig J (1994) Alzheimer beta-amyloid peptide 2535: electrostatic interactions with phospholipid membranes. Biochemistry 33:7434-7441.
65. Thorne RF, Marshall JF, Shafren DR, Gibson PG, Hart IR, Burns GF (2000) The integrins alpha3beta1 and alpha6beta1 physically and functionally associate with CD36 in human melanoma cells: requirement for the extracellular domain OF CD36. J Biol Chem 275:35264-35275.
66. Tontonoz P, Nagy L, Alvarez JG, Thomazy VA, Evans RM (1998) PPARgamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93:241-252.
67. Van Muiswinkel FL, Raupp SF, de Vos NM, Smits HA, Verhoef J, Eikelenboom P, Nottet HS (1999) The amino-terminus of the amyloid-beta protein is critical for the cellular binding and consequent activation of the respiratory burst of human macrophages. J Neuroimmunol 96:121-130.
68. Wang XQ, Frazier WA (1998) The thrombospondin receptor CD47 (IAP) modulates and associates with alpha2 beta1 integrin in vascular smooth muscle cells. Mol Biol Cell 9:865-874.
69. Wang XQ, Lindberg FP, Frazier WA (1999) Integrin-associated protein stimulates alpha2beta1-dependent chemotaxis via Gi-mediated inhibition of adenylate cyclase and extracellular-regulated kinases. J Cell Biol 147:389-400.
70. Wong WS, Simon DI, Rosoff PM, Rao NK, Chapman HA (1996) Mechanisms of pertussis toxin-induced myelomonocytic cell adhesion: role of Mac-1(CD11b/CD18) and urokinase receptor (CD87). Immunology 88:90-97.
71. Wood JG, Zinsmeister P (1991) Tyrosine phosphorylation systems in Alzheimer's disease pathology. Neurosci Lett 121:12-16.
72. Woods ML, Shimizu Y (2001) Signaling networks regulating beta1 integrinmediated adhesion of T lymphocytes to extracellular matrix. J Leukoc Biol 69:874-880.
73. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, Migheli A, Nawroth P, Stern D, Schmidt AM (1996) RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 382:685-691.
74. Yates SL, Burgess LH, Kocsis-Angle J, Antal JM, Dority MD, Embury PB, Piotrkowski AM, Brunden KR (2000) Amyloid beta and amylin fibrils induce increases in proinflammatory cytokine and chemokine production by THP-1 cells and murine microglia. J Neurochem 74:1017-1025.