Astrocytes regulate microglial phagocytosis of senile plaque cores of Alzheimer's disease

Experimental Neurology

Volumn 149, Issue 2, 1998, Pages 329-340

  Dewitt, David A ^a   Perry, George ^a   Cohen, Mark ^a   Doller, Catherine ^a   Silver, Jerry ^a  

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

Author keywords

Beta amyloid; CNS injury; Debris removal; Macrophages; Neurodegenerative diseases; Reactive gliosis

Indexed keywords

AMYLOID BETA PROTEIN; LATEX;

ALZHEIMER DISEASE; ARTICLE; ASTROCYTE; BRAIN INJURY; CLINICAL ARTICLE; GLIOSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MICROGLIA; NERVE DEGENERATION; PHAGOCYTOSIS; PRIORITY JOURNAL; SENILE PLAQUE;

EID: 18144453796     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1997.6738     Document Type: Article

References (72)

1. Abd-El-Basset E., Fedoroff S. Effect of bacterial wall lipopolysaccharide (LPS) on morphology, motility and cytoskeletal organization of microglia in cultures. J. Neurosci. Res. 41:1995;222-237.
2. Araujo D. M., Cotman C. W. β-Amyloid stimulates glial cells in vitro to produce growth factors that accumulate in senile plaques in Alzheimer's disease. Brain Res. 569:1992;141-145.
3. Ard M. D., Cole G. M., Wei J., Mehrle A. P., Fratkin J. D. Scavenging of Alzheimer's amyloid β-protein by microglia in culture. J. Neurosci. Res. 43:1996;190-202.
4. Ashwell K. Development of microglia in the albino rabbit retina. J. Comp. Neurol. 287:1989;286-301.
5. Bell M. D., Lopez-Gonzalez R., Lawson L., Hughes D., Fraser I., Gordon S., Perry V. H. Upregulation of the macrophage scavenger receptor in response to different forms of injury in the CNS. J. Neurocytol. 23:1994;605-613.
6. Berbel P., Innocenti G. M. The development of the corpus callosum in cats: A light and electron-microscopic study. J. Comp. Neurol. 276:1988;132-156.
7. Bignami A., Asher R., Perides G. Brain extracellular matrix and nerve regeneration. Adv. Exp. Med. Biol. 296:1991;197-206.
8. Cai X. D., Golde T. E., Younkin S. G. Release of excess amyloid beta protein from a mutant amyloid beta protein precursor. Science. 259:1993;514-516.
9. Canning D. R., McKeon R. J., DeWitt D. A., Perry G., Wujek J., Fredrickson R., Silver J. β-amyloid of Alzheimer's disease induces reactive gliosis that inhibits axon outgrowth. Exp. Neurol. 124:1993;289-298.
10. Chamak B., Mallat M. Fibronectin and laminin regulate the in vitro differentiation of microglial cells. Neuroscience. 45:1991;513-527.
11. Christie R. H., Freeman M., Hyman B. T. Expression of the macrophage scavenger receptor, a multifunctional lipoprotein receptor, in microglia associated with senile plaques in Alzheimer's disease. Am. J. Pathol. 148:1996;399-403.
12. Cras P., Kawai M., Siedlak S., Mulvihill P., Gambetti P., Lowery D., Gonzalez-DeWhitt D. P., Greenberg B., Perry G. Neuronal and microglial involvement in β-amyloid protein deposition in Alzheimer's disease. Am. J. Pathol. 137:1990;241-246.
13. Davis E. J., Foster T. D., Thomas W. E. Cellular Forms and Functions of Brain Microglia. Brain Res. Bull. 34:1994;73-78.
14. Elkabes S., DiCicco-Bloom E. M., Black I. B. Brain microglia/macrophages express neurotrophins that selectively regulate microglia proliferation and function. J. Neurosci. 16:1996;2508-2521.
15. Ferrer I., Bernet E., Soriano E., Del Rio T., Fonseca M. Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes. Neuroscience. 39:1990;451-458.
16. Frackowiak J., Wisniewski H. M., Wegiel J., Merz S., Iqbal K., Wang K. C. Ultrastructure of the microglia that phagocytose amyloid and the microglia that produce β-amyloid fibrils. Acta Neuropathol. 84:1992;225-233.
17. Frank M., Wolburg H. Cellular reaction at the lesion site after crushing of the rat optic nerve. Glia. 16:1996;227-240.
18. Frautschy S. A., Cole G. M., Baird A. Phagocytosis and deposition of vascular beta-amyloid in rat brains injected with Alzheimer beta amyloid. Am. J. Pathol. 140:1992;1389-1399.
19. Games D., Adams D., Alessandrini R., Barbour R., Berthelette P., Blackwell C., Carr T., Clemens J., Donaldson T., Gillespie F., Guido T., Hagopian S., Johnson-Wood K., Khan K., Lee M., Leibowitz P., Lieberburg I., Little S., Masliah E., McConiogue L., Montoya-Zavala M., Mucke L., Paganini L., Penniman E., Power M., Schenk D., Seubert P., Snyder B., Soriano F., Tan H., Vitale J., Wadsworth S., Wolozin B., Zhao J. Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature. 373:1995;523-527.
20. Gehrmann J., Kreutzberg G. Microglia in experimental neuropathology. Neuroglia. 1995;Oxford UP, New York. p. 885-904.
21. Gehrmann J., Matsumoto Y., Kreutzberg G. W. Microglia: Intrinsic immunoeffector cell of the brain. Brain Res. Rev. 20:1995;269-287.
22. Giordana M. T., Attanasio A., Cavalla P., Migheli A., Vigliani M. C., Schiffer D. Reactive Cell Proliferation and microglia following injury to the rat brain. Neuropathol. Applied Neurobiol. 20:1994;163-174.
23. Giulian D., Baker T. J. Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci. 6:1986;2163-2178.
24. Giulian D., Chen J., Ingeman J. E., George J. K., Naponen M. The role of mononuclear phagocytes in wound healing after traumatic injury to adult mammalian brain. J. Neurosci. 9:1989;4416-4429.
25. Giulian D., Haverkamp L. J., Li J., Karshin W. L., Yu J., Tom D., Li X., Kirkpatrick J. B. Senile plaques stimulate microglia to release a neurotoxin found in Alzheimer's brain. Neurochem. Int. 27:1995;119-137.
26. Giulian D., Li J., Bartel S., Broker J., Li X., Kirkpatrick J. B. Cell surface morphology identifies microglia as a distinct class of mononuclear phagocyte. J. Neurosci. 15:1995;7712-7726.
27. Hachimi K. H. E., Foncin J. F. Do microglial cells phagocyte the β/A4-amyloid senile plaque core of Alzheimer disease. C. R. Acad. Sci. III. 317:1994;445-451.
28. Haga S., Akai K., Ishii T. Demonstration of microglia cells in and around senile (neuritic) plaques in the Alzheimer brain: An immunohistochemical study using a novel monoclonal antibody. Acta Neuropathol. 77:1989;569-575.
29. Haga S., Ikeda K., Sato M., Ishii T. Synthetic Alzheimer amyloid beta/A4 peptides enhance production of complement C3 component by cultured microglial cells. Brain Res. 601:1993;88-94.
30. Hume D. A., Perry V. H., Gordon S. Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J. Cell Biol. 97:1983;253-257.
31. Hyman B. T., Marzloff K., Arriagada P. V. The lack of accumulation of senile plaques or amyloid burden in Alzheimer's disease suggests a dynamic balance between amyloid deposition and resolution. J. Neuropathol. Exp. Neurol. 52:1993;594-600.
32. Innocenti G. M., Koppel H., Clarke S. Transitory macrophages in the white matter of the developing visual cortex I. Light and electron microscopic characteristics and distribution. Brain Res. 313:1983;39-53.
33. Innocenti G. M., Clarke S., Koppel H. Transitory macrophages in the white matter of the developing visual cortex. II. Development and relations with axonal pathways. Brain Res. 313:1983;55-66.
34. Itagaki S., McGeer P. L., Akiyama H., Zhu S., Selkoe D. Relationship of microglia and Astrocytes to amyloid deposits of Alzheimer disease. J. Neuroimmunol. 24:1989;173-182.
35. Killackey H. P. Glia and the elimination of transient cortical projections. Trends Neurosci. 7:1984;225-226.
36. Kim K. S., Miller D. F., Sapienza V. J., Chen C. J., Bai C., Grundke-Iqbal I., Currie J. R., Wisniewski H. M. Production and characterization of monoclonal antibodies reactive to synthetic cerebrovascular amyloid peptide. Neurosci. Res. Commun. 2:1988;121-130.
37. Lawson L. J., Frost L., Risbridger J., Fearn S., Perry V. H. Quantification of the mononuclear phagocyte response to Wallerian degeneration of the optic nerve. J. Neurocytol. 23:1994;729-744.
38. Linden R., Cavalcante L. A., Barradas P. C. Mononuclear phagocytes in the retina of developing rats. Histochemistry. 85:1986;335-339.
39. Liu W., Brosnan C. F., Dickson D. W., Lee S. C. Macrophage colony-stimulating factor mediates astrocyte-induced microglial ramification in human fetal central nervous system culture. Am. J. Pathol. 145:1994;48-53.
40. Liu X. Z., Xu X. M., Hu R., Du C., Zhang S. X., McDonald J. W., Dong H. X., Wu Y. J., Fan G. S., Jacquin M. F., Hsu C. Y., Choi D. W. Neuronal and glial apoptosis after traumatic spinal cord injury. J. Neurosci. 17:1997;5395-5406.
41. Mackenzie I. R., Hao C., Munoz D. G. Role of microglia in senile plaque formation. Neurobiol. Aging. 16:1995;797-804.
42. Mandybur T. I., Chuirazzi C. C. Astrocytes and the plaques of Alzheimer's disease. Neurology. 40:1990;635-639.
43. McGeer P. L., Itagaki S., Tago H., McGeer E. G. Reactive microglia in patients with senile dementia of the Alzheimer type are positive for the histocompatibility glycoprotein HLA-DR. Neurosci. Lett. 79:1987;195-200.
44. McMillian M. K., Thai L., Hong J. S., O'Callaghan J. P., Pennypacker K. R. Brain injury in a dish: A model for reactive gliosis. Trends Neurosci. 17:1994;138-142.
45. Milligan C. E., Cunningham T. J., Levitt P. Differential immunocytochemical markers reveal the normal distribution of brain macrophages and microglia in the developing rat brain. J. Comp. Neurol. 314:1991;125-135.
46. Naruse S., Igarashi S., Kobayashi H., Aoki D., Inuzuka T., Kaneko K., Shimizu T., Iihara K., Kojima T., Miyatake. Mis-sense mutation Val-Ile in exon 17 of the amyloid precursor protein gene in Japanese familial Alzheimer's disease. Lancet. 337:1991;978-979.
47. Nieto-Sampedro M., Mora F. Active microglia, sick astroglia and Alzheimer type dementias. Neuroreport. 5:1994;375-380.
48. Paresce D. M., Ghosh R. N., Maxfield F. R. Microglial cells internalize aggregates of the Alzheimer's disease Amyloid β-Protein via a scavenger receptor. Neuron. 17:1996;553-565.
49. Perlmutter L. S., Scott S. A., Barron E., Chui H. C. MHC class II-positive microglia in human brain: association with Alzheimer lesions. J. Neurosci. Res. 33:1992;549-558.
50. Perry V. H., Brown M. C., Gordon S. The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration. J. Exp. Med. 165:1987;1218-1223.
51. Perry V. H., Gordon S. Macrophages and microglia in the nervous system. Trends Neuroci. 11:1987;273-277.
52. Pike C. J., Cummings B. J., Cotman C. W. Early association of reactive astrocytes with senile plaques in Alzheimer's disease. Exp. Neurol. 132:1995;172-179.
53. Rogers J., Cooper N. R., Webster S., Schultz J., McGeer P. L., Styren S. D., Civin W. H., Brachova L., Bradt B., Ward P., Lieberburg I. Complement activation by β-amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. USA. 89:1992;10016-10020.
54. Rosana G. R., Swanson J. A. Microtubules can modulate pseudopod activity from a distance inside macrophages. Cell Motil. Cytoskeleton. 34:1996;230-245.
55. Selkoe D. J. The molecular pathology of Alzheimer's disease. Neuron. 6:1991;487-498.
56. Selkoe D. J., Abraham C. R., Podlisny M. B., Duffy L. K. Isolation of low-molecular-weight proteins from the amyloid plaque fibers in Alzheimer's disease. J. Neurochem. 46:1986;1820-1834.
57. Shaffer L. M., Dority M. D., Gupta-Bansal R., Frederickson R. C. A., Younkin S. G., Brunden K. R. Amyloid β protein (Aβ) removal by neuroglial cells in culture. Neurobiol. Aging. 16:1995;737-745.
58. Sievers J., Parwaresch R., Wottge H. U. Blood monocytes and spleen macrophages differentiate into microglia-like cells on monolayers of Astrocytes: Morphology. Glia. 12:1994;245-258.
59. Sternberger L. A. Immunocytochemistry. 1986;Wiley, New York.
60. Stoll G., Trapp B. D., Griffin J. W. Macrophage function during Wallerian degeneration of rat brain optic nerve: Clearance of degenerating myelin and Ia expression. J. Neurosci. 9:1989;2327-2335.
61. 4. J. Histochem. Cytochem. 38:1990;1683-1686.
62. Streit W. J. Microglial Cells. Kettenman H., Ransom B. Neuroglia. 1995;885-904 Oxford UP, New York.
63. Streit W. J., Kreutzberg G. W. Response of endogenous glial cells to motor neuron degeneration induced by toxin ricin. J. Comp. Neurol. 268:1988;248-263.
64. Suzuki N., Cheung T. T., Cai X. D., Odaka A., Otvos L., Eckman C., Golde T. E., Younkin S. G. An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta APP717) mutants. Science. 264:1994;1336-1340.
65. Suzumura A., Marunouchi T., Yamamoto H. Morphological transformation of microgliain vitro. Brain Res. 545:1991;301-306.
66. Suzumura A., Sawada M., Yamamoto H., Marunouchi T. Transforming Growth Factor-β Suppresses Activation and Proliferation of microgliain vitro. J. Immunol. 151:1993;2150-2158.
67. Tanaka J., Maeda N. Microglial ramification requires nondiffusible factors derived from astrocytes. Exp. Neurol. 137:1996;367-375.
68. Thomas W. E. Brain macrophages: evaluation of microglia and their functions. Brain Res. Rev. 17:1992;61-74.
69. Ward S. A., Ransom P. A., Booth P. L., Thomas W. E. Characterization of ramified microglia in tissue culture: Pinocytosis and motility. J. Neurosci. Res. 29:1991;13-28.
70. 4. Acta Neuropathol. 81:1991;588-590.
71. Wisniewski H. M., Weigel J. Migration of perivascular cells into the neuropil and their involvement in β-amyloid plaque formation. Acta Neuropathol. 85:1993;586-595.
72. Wood G. W., Gollahon K. A., Tilzer S. A., Vats T., Morantz R. A. The failure of microglia in normal brain to exhibit mononuclear phagocyte markers. J. Neuropathol. Exp. Neurol. 38:1979;369-376.