Uptake of Aβ 1-40- and Aβ 1-42-coated yeast by microglial cells: A role for LRP

Journal of Leukocyte Biology

Volumn 76, Issue 2, 2004, Pages 451-461

  Laporte, Vincent ^a   Lombard, Yves ^a   Levy Benezra, Rachel ^a   Tranchant, Christine ^a   Poindron, Philippe ^a   Warter, Jean Marie ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Alzheimer's disease; Amyloid protein; Endocytosis; Phagocytosis; Scavenger receptor A; Senile plaque

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; SCAVENGER RECEPTOR; UNCLASSIFIED DRUG; CELL RECEPTOR; PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; ANIMAL CELL; CONFERENCE PAPER; CONTROLLED STUDY; HEATING; INTERNALIZATION; MICROGLIA; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; OPSONIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; SENILE PLAQUE; YEAST; ANIMAL; ARTICLE; METABOLISM; SACCHAROMYCES CEREVISIAE; TIME;

ANIMALIA;

AMYLOID BETA-PROTEIN; ANIMALS; MICE; MICROGLIA; PEPTIDE FRAGMENTS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SACCHAROMYCES CEREVISIAE; TIME FACTORS;

EID: 3442888778     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1203620     Document Type: Conference Paper

References (57)

1. Selkoe, D. J. (1991) The molecular pathology of Alzheimer's disease. Neuron 6, 487-498.
2. Higgins, L. S., Murphy Jr., G. M., Forno, L. S., Catalano, R., Cordell, B. (1996) P3 β-amyloid peptide has a unique and potentially pathogenic immunohistochemical profile in Alzheimer's disease brain. Am. J. Pathol. 149, 585-596.
3. Iwatsubo, T., Odaka, A., Suzuki, N., Mizusawa, H., Nukina, N., Ihara, Y. (1994) Visualization of A β 42(43) and A β 40 in senile plaques with end-specific A β monoclonals: evidence that an initially deposited species is A β 42(43). Neuron 13, 45-53.
4. Selkoe, D. J. (2001) Clearing the brain's amyloid cobwebs. Neuron 32, 177-180.
5. Shibata, M., Yamada, S., Kuniar, S. R., Calero, M., Bading, J., Frangione, B., Holtzman, D. M., Miller, C. A., Strickland, D. K., Ghiso, J., Zlokovic, B. V. (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.
6. Li, R., Shen, Y., Yang, L. B., Lue, L. F., Finch, C., Rogers, J. (2000) Estrogen enhances uptake of amyloid β-protein by microglia derived from the human cortex. J. Neurochem. 75, 1447-1454.
7. Qiu, W. Q., Walsh, D. M., Ye, Z., Vekrellis, K., Zhang, J., Podlisny, M. B., Rosner, M. R., Safavi, A., Hersh, L. B., Selkoe, D. J. (1998) Insulin-degrading enzyme regulates extracellular levels of amyloid β-protein by degradation. J. Biol. Chem. 273, 32730-32738.
8. Iwata, N., Tsubuki, S., Takaki, Y., Shirotani, K., Lu, B., Gerard, N. P., Gerard, C., Hama, E., Lee, H. J., Saido, T. C. (2001) Metabolic regulation of brain Aβ by neprilysin. Science 292, 1550-1552.
9. Chung, H., Brazil, M. I., Soe, T. T., Maxfield, F. R. (1999) Uptake, degradation, and release of fibrillar and soluble forms of Alzheimer's amyloid β-peptide by microglial cells. J. Biol. Chem. 274, 32301-32308.
10. Glabe, C. (2000) Does Alzheimer disease tilt the scales of amyloid degradation versus accumulation? Nat. Med. 6, 133-134.
11. Wegiel, J., Wisniewski, H. M. (1990) The complex of microglial cells and amyloid star in three-dimensional reconstruction. Acta Neuropathol. (Berl.) 81, 116-124.
12. Szczepanik, A. M., Funes, S., Petko, W., Ringheim, G. E. (2001) IL-4, IL-10 and IL-13 modulate A β(1-42)-induced cytokine and chemokine production in primary murine microglia and a human monocyte cell line. J. Neuroimmunol. 113, 49-62.
13. Kingham, P. J., Pocock, J. M. (2001) Microglial secreted cathepsin B induces neuronal apoptosis. J. Neurochem. 76, 1475-1484.
14. Weldon, D. T., Rogers, S. D., Ghilardi, J. R., Finke, M. P., Cleary, J. P., O'Hare, E., Esler, W. P., Maggio, J. E., Mantyh, P. W. (1998) Fibrillar β-amyloid induces microglial phagocytosis, expression of inducible nitric oxide synthase, and loss of a select population of neurons in the rat CNS in vivo. J. Neurosci. 18, 2161-2173.
15. Smith, M. E., van der Maesen, K., Somera, F. P., Sobel, R. A. (1998) Effects of phorbol myristate acetate (PMA) on functions of macrophages and microglia in vitro. Neurochem. Res. 23, 427-434.
16. Ard, M. D., Cole, G. M., Wei, J., Mehrle, A. P., Fratkin, J. D. (1996) Scavenging of Alzheimer's amyloid β-protein by microglia in culture. J. Neurosci. Res. 43, 190-202.
17. Paresce, D. M., Ghosh, R. N., Maxfield, F. R. (1996) Microglial cells internalize aggregates of the Alzheimer's disease amyloid β-protein via a scavenger receptor. Neuron 17, 553-565.
18. DeWitt, D. A., Perry, G., Cohen, M., Doller, C., Silver, J. (1998) Astrocytes regulate microglial phagocytosis of senile plaque cores of Alzheimer's disease. Exp. Neurol. 149, 329-340.
19. Webster, S. D., Yang, A. J., Margol, L., Garzon-Rodriguez, W., Glabe, C. G., Tenner, A. J. (2000) Complement component C1q modulates the phagocytosis of Aβ by microglia. Exp. Neurol. 161, 127-138.
20. Itagaki, S., McGeer, P. L., Akiyama, H., Zhu, S., Selkoe, D. (1989) Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J. Neuroimmunol. 24, 173-182.
21. McGeer, P. L., Akiyama, H., Kawamata, T., Yamada, T., Walker, D. G., Ishii, T. (1992) Immunohistochemical localization of β-amyloid precursor protein sequences in Alzheimer and normal brain tissue by light and electron microscopy. J. Neurosci. Res. 31, 428-442.
22. Akiyama, H., Mori, H., Saido, T., Kondo, H., Ikeda, K., McGeer, P. L. (1999) Occurrence of the diffuse amyloid β-protein (Aβ) deposits with numerous Aβ-containing glial cells in the cerebral cortex of patients with Alzheimer's disease. Glia 25, 324-331.
23. Akiyama, H., Schwab, C., Kondo, H., Mori, H., Kametani, F., Ikeda, K., McGeer, P. L. (1996) Granules in glial cells of patients with Alzheimer's disease are immunopositive for C-terminal sequences of β-amyloid protein. Neurosci. Lett. 206, 169-172.
24. Bard, F., Cannon, C., Barbour, R., Burke, R. L., Games, D., Grajeda, H., Guido, T., Hu, K., Huang, J., Johnson-Wood, K., Khan, K., Kholodenko, D., Lee, M., Lieberburg, I., Motter, R., Nguyen, M., Soriano, F., Vasquez, N., Weiss, K., Welch, B., Seubert, P., Schenk, D., Yednock, T. (2000) Peripherally administered antibodies against amyloid β-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat. Med. 6, 916-919.
25. Qiu, Z., Strickland, D. K., Hyman, B. T., Rebeck, G. W. (1999) α2-Macroglobulin enhances the clearance of endogenous soluble β-amyloid peptide via low-density lipoprotein receptor-related protein in cortical neurons. J. Neurochem. 73, 1393-1398.
26. Yang, D. S., Small, D. H., Seydel, U., Smith, J. D., Hallmayer, J., Gandy, S. E., Martins, R. N. (1999) Apolipoprotein E promotes the binding and uptake of β-amyloid into Chinese hamster ovary cells in an isoform-specific manner. Neuroscience 90, 1217-1226.
27. Klunk, W. E., Jacob, R. F., Mason, R. P. (1999) Quantifying amyloid by Congo red spectral shift assay. Methods Enzymol. 309, 285-305.
28. Lombard, Y., Ulrich, B., Poindron, P. (1985) In vitro multiplication and apparently indefinite subcultures of normal mouse resident peritoneal macrophages. Biol. Cell. 53, 219-230.
29. Streit, W. J. (1990) An improved staining method for rat microglial cells using the lectin from Griffonia simplicifolia (GSA I-B4). J. Histochem. Cytochem. 38, 1683-1686.
30. Giaimis, J., Lombard, Y., Fonteneau, P., Muller, C. D., Levy, R., Makaya-Kumba, M., Lazdins, J., Poindron, P. (1993) Both mannose and β-glucan receptors are involved in phagocytosis of unopsonized, heat-killed Saccharomyces cerevisiae by murine macrophages. J. Leukoc. Biol. 54, 564-571.
31. Giaimis, J., Lombard, Y., Makaya-Kumba, M., Fonteneau, P., Poindron, P. (1992) A new and simple method for studying the binding and ingestion steps in the phagocytosis of yeasts. J. Immunol. Methods 154, 185-193.
32. Peiser, L., Gordon, S. (2001) The function of scavenger receptors expressed by macrophages and their role in the regulation of inflammation. Microbes Infect. 3, 149-159.
33. Axline, S. G., Reaven, E. P. (1974) Inhibition of phagocytosis and plasma membrane mobility of the cultivated macrophage by cytochalasin B. Role of subplasmalemmal microfilaments. J. Cell Biol. 62, 647-659.
34. Inoue, S., Kuroiwa, M., Kisilevsky, R. (1999) Basement membranes, microfibrils and β amyloid fibrillogenesis in Alzheimer's disease: high resolution ultrastructural findings. Brain Res. Brain Res. Rev. 29, 218-231.
35. Simonsen, A., Wurmser, A. E., Emr, S. D., Stenmark, H. (2001) The role of phosphoinositides in membrane transport. Curr. Opin. Cell Biol. 13, 485-492.
36. Hewlett, L. J., Prescott, A. R., Watts, C. (1994) The coated pit and macropinocytic pathways serve distinct endosome populations. J. Cell Biol. 124, 689-703.
37. Urmoneit, B., Prikulis, I., Wihl, G., D'Urso, D., Frank, R., Heeren, J., Beisiegel, U., Prior, R. (1997) Cerebrovascular smooth muscle cells internalize Alzheimer amyloid β protein via a lipoprotein pathway: implications for cerebral amyloid angiopathy. Lab. Invest. 77, 157-166.
38. Ida, N., Masters, C. L., Beyreuther, K. (1996) Rapid cellular uptake of Alzheimer amyloid βA4 peptide by cultured human neuroblastoma cells. FEBS Lett. 394, 174-178.
39. Weltzien, R. B., Pachter, J. S. (2000) Visualization of β-amyloid peptide (Aβ) phagocytosis by human mononuclear phagocytes: dependency on Aβ aggregate size. J. Neurosci. Res. 59, 522-527.
40. Shaffer, L. M., Dority, M. D., Gupta-Bansal, R., Frederickson, R. C., Younkin, S. G., Brunden, K. R. (1995) Amyloid β protein (A β) removal by neuroglial cells in culture. Neurobiol. Aging 16, 737-745.
41. Frackowiak, J., Wisniewski, H. M., Wegiel, J., Merz, G. S., Iqbal, K., Wang, K. C. (1992) Ultrastructure of the microglia that phagocytose amyloid and the microglia that produce β-amyloid fibrils. Acta Neuropathol. (Berl.) 84, 225-233.
42. Antic, A., Dzenko, K. A., Pachter, J. S. (2000) Engagement of the scavenger receptor is not responsible for β-amyloid stimulation of monocytes to a neurocytopathic state. Exp. Neurol. 161, 96-101.
43. Huang, F., Buttini, M., Wyss-Coray, T., McConlogue, L., Kodama, T., Pitas, R. E., Mucke, L. (1999) Elimination of the 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.
44. Lorton, D., Schaller, J., Lala, A., De Nardin, E. (2000) Chemotactic-like receptors and Aβ peptide induced responses in Alzheimer's disease. Neurobiol. Aging 21, 463-473.
45. Lue, L. F., Walker, D. G., Brachova, L., Beach, T. G., Rogers, J., Schmidt, A. M., Stern, D. M., Yan, S. D. (2001) Involvement of microglial receptor for advanced glycation endproducts (RAGE) in Alzheimer's disease: identification of a cellular activation mechanism. Exp. Neurol. 171, 29-45.
46. Mitrasinovic, O. M., Vincent, V. A., Simsek, D., Murphy Jr., G. M. (2003) Macrophage colony stimulating factor promotes phagocytosis by murine microglia. Neurosci. Lett. 344, 185-188.
47. Rogers, J., Strohmeyer, R., Kovelowski, C. J., Li, R. (2002) Microglia and inflammatory mechanisms in the clearance of amyloid β peptide. Glia 40, 260-269.
48. Marzolo, M. P., von Bernhardi, R., Bu, G., Inestrosa, N. C. (2000) Expression of α(2)-macroglobulin receptor/low density lipoprotein receptor-related protein (LRP) in rat microglial cells. J. Neurosci. Res. 60, 401-411.
49. Kounnas, M. Z., Moir, R. D., Rebeck, G. W., Bush, A. I., Argraves, W. S., Tanzi, R. E., Hyman, B. T., Strickland, D. K. (1995) LDL receptor-related protein, a multifunctional ApoE receptor, binds secreted β-amyloid precursor protein and mediates its degradation. Cell 82, 331-340.
50. Beffert, U., Arguin, C., Poirier, J. (1999) The polymorphism in exon 3 of the low density lipoprotein receptor-related protein gene is weakly associated with Alzheimer's disease. Neurosci. Lett. 259, 29-32.
51. Wavrant-DeVrieze, F., Lambert, J. C., Stas, L., Crook, R., Cottel, D., Pasquier, F., Frigard, B., Lambrechts, M., Thiry, E., Amouyel, P., Tur, J. P., Chartier-Harlin, M. C., Hardy, J., Van Leuven, F. (1999) Association between coding variability in the LRP gene and the risk of late-onset Alzheimer's disease. Hum. Genet. 104, 432-434.
52. Strittmatter, W. J., Roses, A. D. (1995) Apolipoprotein E and Alzheimer disease. Proc. Natl. Acad. Sci. USA 92, 4725-4727.
53. Blacker, D., Wilcox, M. A., Laird, N. M., Rodes, L., Horvath, S. M., Go, R. C., Perry, R., Watson Jr., B., Bassett, S. S., McInnis, M. G., Albert, M. S., Hyman, B. T., Tanzi, R. E. (1998) α-2 Macroglobulin is genetically associated with Alzheimer disease. Nat. Genet. 19, 357-360.
54. Liao, A., Nitsch, R. M., Greenberg, S. M., Finckh, U., Blacker, D., Albert, M., Rebeck, G. W., Gomez-Isla, T., Clatworthy, A., Binetti, G., Hock, C., Mueller-Thomsen, T., Mann, U., Zuchowski, K., Beisiegel, U., Staehelin, H., Growdon, J. H., Tanzi, R. E., Hyman B. T. (1998) Genetic association of an α2-macroglobulin (Val1000lle) polymorphism and Alzheimer's disease. Hum. Mol. Genet. 7, 1953-1956.
55. Namba, Y., Tomonaga, M., Kawasaki, H., Otomo, E., Ikeda, K. (1991) Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer's disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Res. 541, 163-166.
56. Rebeck, G. W., Harr, S. D., Strickland, D. K., Hyman, B. T. (1995) Multiple, diverse senile plaque-associated proteins are ligands of an apolipoprotein E receptor, the α 2-macroglobulin receptor/low-density- lipoprotein receptor-related protein. Ann. Neurol. 37, 211-217.
57. Kang, D. E., Pietrzik, C. U., Baum, L., Chevallier, N., Merriam, D. E., Kounnas, M. Z., Wagner, S. L., Troncoso, J. C., Kawas, C. H., Katzman, R., Koo, E. H. (2000) Modulation of amyloid β-protein clearance and Alzheimer's disease susceptibility by the LDL receptor-related protein pathway. J. Clin. Invest. 106, 1159-1166.