Microglia in the degenerating brain are capable of phagocytosis of beads asncd of apoptotic cells, but do not efficiently remove PrPSc, even upon LPS stimulation

GLIA

Volumn 58, Issue 16, 2010, Pages 2017-2030

  Hughes, Martina M ^a   Field, Robert H ^a   Perry, V Hugh ^b   Murray, Carol L ^a   Cunningham, Colm ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Activation; Alzheimer's disease; Amyloid; Apoptosis; Microglia; Phagocytosis; Priming; Prion disease

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CATHEPSIN; INTERLEUKIN 1BETA; MATRIX METALLOPROTEINASE; OXIDOREDUCTASE; PRION PROTEIN; SCAVENGER RECEPTOR; STROMELYSIN; UROKINASE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEGENERATION; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MICROGLIA; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; TRANSCRIPTION INITIATION;

ANIMALS; APOPTOSIS; BRAIN; ENCEPHALITIS; FEMALE; GENE EXPRESSION REGULATION; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICROGLIA; MICROSPHERES; PHAGOCYTOSIS; PHENOTYPE; PRION DISEASES; PRPSC PROTEINS; UP-REGULATION;

EID: 78649434414     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21070     Document Type: Article

References (73)

1. Akahoshi N, Murashima YL, Himi T, Ishizaki Y, Ishii I. 2007. Increased expression of the lysosomal protease cathepsin S in hippocampal microglia following kainate-induced seizures. Neurosci Lett 429:136-141.
2. Akiyama H, McGeer PL. 2004. Specificity of mechanisms for plaque removal after A beta immunotherapy for Alzheimer disease. Nat Med 10:117-118; author reply118-119.
3. Baker CA, Lu ZY, Zaitsev I, Manuelidis L. 1999. Microglial activation varies in different models of Creutzfeldt-Jakob disease. J Virol 73:5089-5097.
4. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE. 2003. A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J Neurosci 23:2665-2674.
5. Betmouni S, Perry VH, Gordon JL. 1996. Evidence for an early inflammatory response in the central nervous system of mice with scrapie. Neuroscience 74:1-5.
6. Botto M, Hawkins PN, Bickerstaff MC, Herbert J, Bygrave AE, McBride A, Hutchinson WL, Tennent GA, Walport MJ, Pepys MB. 1997. Amyloid deposition is delayed in mice with targeted deletion of the serum amyloid P component gene. Nat Med 3:855-859.
7. Brown AR, Webb J, Rebus S, Walker R, Williams A, Fazakerley JK. 2003. Inducible cytokine gene expression in the brain in the ME7/CV mouse model of scrapie is highly restricted, is at a strikingly low level relative to the degree of gliosis and occurs only late in disease. J Gen Virol 84 (Part 9):2605-2611.
8. Cagnin A, Brooks DJ, Kennedy AM, Gunn RN, Myers R, Turkheimer FE, Jones T, Banati RB. 2001. In-vivo measurement of activated microglia in dementia. Lancet 358:461-467.
9. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA. 2008. A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function. J Neurosci 28:264-278.
10. Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JA, Perry VH, Weller RO. 2008. Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: Significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol Appl Neurobiol 34:131-144.
11. Choi DH, Kim EM, Son HJ, Joh TH, Kim YS, Kim D, Flint Beal M, Hwang O. 2008. A novel intracellular role of matrix metalloproteinase-3 during apoptosis of dopaminergic cells. J Neurochem 106:405- 415.
12. Ciesielski-Treska J, Grant NJ, Ulrich G, Corrotte M, Bailly Y, Haeberle AM, Chasserot-Golaz S, Bader MF. 2004. Fibrillar prion peptide (106-126) and scrapie prion protein hamper phagocytosis in microglia. Glia 46:101-115.
13. Cunningham C, Boche D, Perry VH. 2002. Transforming growth factor beta1, the dominant cytokine in murine prion disease: Influence on inflammatory cytokine synthesis and alteration of vascular extracellular matrix. Neuropathol Appl Neurobiol 28:107-119.
14. Cunningham C, Campion S, Lunnon K, Murray CL, Woods JF, Deacon RM, Rawlins JN, Perry VH. 2009a. Systemic inflammation induces acute behavioral and cognitive changes and accelerates neurodegenerative disease. Biol Psychiatry 65:304-312.
15. Cunningham C, Deacon R, Wells H, Boche D, Waters S, Diniz CP, Scott H, Rawlins JN, Perry VH. 2003. Synaptic changes characterize early behavioral changes in the ME7 model of murine prion disease. Eur J Neurosci 17:2147-2155.
16. Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH. 2005. Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 25:9275-9284.
17. Cunningham O, Campion S, Perry VH, Murray C, Sidenius N, Docagne F, Cunningham C. 2009b. Microglia and the urokinase plasminogen activator receptor/uPA system in innate brain inflammation. Glia 57:1802-1814.
18. D'Mello V, Singh S, Wu Y, Birge RB. 2009. The urokinase plasminogen activator receptor promotes efferocytosis of apoptotic cells. J Biol Chem 284:17030-17038.
19. De Simone R, Ajmone-Cat MA, Minghetti L. 2004. Atypical antiinflammatory activation of microglia induced by apoptotic neurons: Possible role of phosphatidylserine-phosphatidylserine receptor interaction. Mol Neurobiol 29:197-212.
20. De Simone R, Ajmone-Cat MA, Tirassa P, Minghetti L. 2003. Apoptotic PC12 cells exposing phosphatidylserine promote the production of anti-inflammatory and neuroprotective molecules by microglial cells. J Neuropathol Exp Neurol 62:208-216.
21. DeArmond SJ. 1993. Alzheimer's disease and Creutzfeldt-Jakob disease: Overlap of pathogenic mechanisms. Curr Opin Neurol 6:872- 881.
22. DiCarlo G, Wilcock D, Henderson D, Gordon M, Morgan D. 2001. Intrahippocampal LPS injections reduce Abeta load in APP+PS1 transgenic mice. Neurobiol Aging 22:1007-1012.
23. El Khoury JB, Moore KJ, Means TK, Leung J, Terada K, Toft M, Freeman MW, Luster AD. 2003. CD36 mediates the innate host response to beta-amyloid. J Exp Med 197:1657-1666.
24. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM. 1998. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 101:890-898.
25. Falcone S, Cocucci E, Podini P, Kirchhausen T, Clementi E, Meldolesi J. 2006. Macropinocytosis: Regulated coordination of endocytic and exocytic membrane traffic events. J Cell Sci 119 (Part 22):4758-4769.
26. Flannery T, Gibson D, Mirakhur M, McQuaid S, Greenan C, Trimble A, Walker B, McCormick D, Johnston PG. 2003. The clinical significance of cathepsin S expression in human astrocytomas. Am J Pathol 163:175-182.
27. Frank S, Burbach GJ, Bonin M, Walter M, Streit W, Bechmann I, Deller T. 2008. TREM2 is upregulated in amyloid plaque-associated microglia in aged APP23 transgenic mice. Glia 56:1438-1447.
28. Grathwohl SA, Kalin RE, Bolmont T, Prokop S, Winkelmann G, Kaeser SA, Odenthal J, Radde R, Eldh T, Gandy S, Aguzzi A, Staufenbiel M, Mathews PM, Wolburg H, Heppner FL, Jucker M. 2009. Formation and maintenance of Alzheimer's disease beta-amyloid plaques in the absence of microglia. Nat Neurosci 12:1361-1363.
29. Herber DL, Mercer M, Roth LM, Symmonds K, Maloney J, Wilson N, Freeman MJ, Morgan D, Gordon MN. 2007. Microglial activation is required for Abeta clearance after intracranial injection of lipopolysaccharide in APP transgenic mice. J Neuroimmune Pharmacol 2:222-231.
30. Herber DL, Roth LM, Wilson D, Wilson N, Mason JE, Morgan D, Gordon MN. 2004. Time-dependent reduction in Abeta levels after intracranial LPS administration in APP transgenic mice. Exp Neurol 190:245-253.
31. Hewlett LJ, Prescott AR, Watts C. 1994. The coated pit and macropinocytic pathways serve distinct endosome populations. J Cell Biol 124:689-703.
32. Holmes C, Boche D, Wilkinson D, Yadegarfar G, Hopkins V, Bayer A, Jones RW, Bullock R, Love S, Neal JW, Zotova E, Nicoll JA. 2008. Long-term effects of Abeta42 immunisation in Alzheimer's disease: Follow-up of a randomized, placebo-controlled phase I trial. Lancet 372:216-223.
33. Holmes C, Cunningham C, Zotova E, Woolford J, Dean C, Kerr S, Culliford D, Perry VH. 2009. Systemic inflammation and disease progression in Alzheimer's disease. Neurology 73:768-774.
34. Husemann J, Loike JD, Anankov R, Febbraio M, Silverstein SC. 2002. Scavenger receptors in neurobiology and neuropathology: Their role on microglia and other cells of the nervous system. Glia 40:195- 205.
35. Jucker M, Heppner FL. 2008. Cerebral and peripheral amyloid phagocytes-An old liaison with a new twist. Neuron 59:8-10.
36. Kim YS, Kim SS, Cho JJ, Choi DH, Hwang O, Shin DH, Chun HS, Beal MF, Joh TH. 2005. Matrix metalloproteinase-3: A novel signaling proteinase from apoptotic neuronal cells that activates microglia. J Neurosci 25:3701-3711.
37. Kominami E, Tsukahara T, Bando Y, Katunuma N. 1985. Distribution of cathepsins B, H in rat tissues and peripheral blood cells. J Biochem 98:87-93.
38. Lucin KM, Wyss-Coray T. 2009. Immune activation in brain aging and neurodegeneration: Too much or too little? Neuron 64:110-122.
39. Lue LF, Yan SD, Stern DM, Walker DG. 2005. Preventing activation of receptor for advanced glycation endproducts in Alzheimer's disease. Curr Drug Targets CNS Neurol Disord 4:249-266.
40. Malm TM, Magga J, Kuh GF, Vatanen T, Koistinaho M, Koistinaho J. 2008. Minocycline reduces engraftment and activation of bone marrow-derived cells but sustains their phagocytic activity in a mouse model of Alzheimer's disease. Glia 56:1767-1779.
41. Masocha W. 2009. Systemic lipopolysaccharide (LPS)-induced microglial activation results in different temporal reduction of CD200 and CD200 receptor gene expression in the brain. J Neuroimmunol 214:78-82.
42. McClain JA, Phillips LL, Fillmore HL. 2009. Increased MMP-3 and CTGF expression during lipopolysaccharide-induced dopaminergic neurodegeneration. Neurosci Lett 460:27-31.
43. Minghetti L, Ajmone-Cat MA, De Berardinis MA, De Simone R. 2005. Microglial activation in chronic neurodegenerative diseases: Roles of apoptotic neurons and chronic stimulation. Brain Res Brain Res Rev 48:251-256.
44. Mun-Bryce S, Lukes A, Wallace J, Lukes-Marx M, Rosenberg GA. 2002. Stromelysin-1 and gelatinase A are upregulated before TNF-alpha in LPS-stimulated neuroinflammation. Brain Res 933:42-49.
45. Nakanishi H. 2003. Neuronal and microglial cathepsins in aging and age-related diseases. Ageing Res Rev 2:367-381.
46. Napoli I, Neumann H. 2009. Microglial clearance function in health and disease. Neuroscience 158:1030-1038.
47. Nicoll JA, Wilkinson D, Holmes C, Steart P, Markham H, Weller RO. 2003. Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: A case report. Nat Med 9:448-452.
48. Nimmerjahn A, Kirchhoff F, Helmchen F. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314-1318.
49. Nixon RA, Cataldo AM, Mathews PM. 2000. The endosomal-lysosomal system of neurons in Alzheimer's disease pathogenesis: a review. Neurochem Res 25:1161-1172.
50. Noh EM, Kim JS, Hur H, Park BH, Song EK, Han MK, Kwon KB, Yoo WH, Shim IK, Lee SJ, Youn HJ, Lee YR. 2009. Cordycepin inhibits IL-1beta-induced MMP-1 and MMP-3 expression in rheumatoid arthritis synovial fibroblasts. Rheumatology (Oxford) 48:45-48.
51. Palin K, Cunningham C, Forse P, Perry VH, Platt N. 2008. Systemic inflammation switches the inflammatory cytokine profile in CNS Wallerian degeneration. Neurobiol Dis 30:19-29.
52. Perry VH, Cunningham C, Boche D. 2002. Atypical inflammation in the central nervous system in prion disease. Curr Opin Neurol 15:349- 354.
53. Platt N, da Silva RP, Gordon S. 1998. Class A scavenger receptors and the phagocytosis of apoptotic cells. Biochem Soc Trans 26:639-644.
54. Puyal J, Vaslin A, Mottier V, Clarke PG. 2009. Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann Neurol 66:378-389.
55. Raivich G, Bohatschek M, Kloss CU, Werner A, Jones LL, Kreutzberg GW. 1999. Neuroglial activation repertoire in the injured brain: Graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev 30:77-105.
56. Ransohoff RM, Perry VH. 2009. Microglial physiology: Unique stimuli, specialized responses. Annu Rev Immunol 27:119-145.
57. Rovere P, Peri G, Fazzini F, Bottazzi B, Doni A, Bondanza A, Zimmermann VS, Garlanda C, Fascio U, Sabbadini MG, Rugarli C, Mantovani A, Manfredi AA. 2000. The long pentraxin PTX3 binds to apoptotic cells and regulates their clearance by antigen-presenting dendritic cells. Blood 96:4300-4306.
58. Savill J, Dransfield I, Gregory C, Haslett C. 2002. A blast from the past: Clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2:965-975.
59. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S. 2006. Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49:489-502.
60. Siskova Z, Page A, O'Connor V, Perry VH. 2009. Degenerating synaptic boutons in prion disease: Microglia activation without synaptic stripping. Am J Pathol 175:1610-1621.
61. Sly LM, Krzesicki RF, Brashler JR, Buhl AE, McKinley DD, Carter DB, Chin JE. 2001. Endogenous brain cytokine mRNA and inflammatory responses to lipopolysaccharide are elevated in the Tg2576 transgenic mouse model of Alzheimer's disease. Brain Res Bull 56:581-588.
62. Soto C, Volkel D, Zimmermann K, Zerr I, Lindner T, Bodemer M, Poser S, Schwarz HP. 2003. Unfolding the role of protein misfolding in neurodegenerative diseases. Nat Rev Neurosci 4:49-60.
63. Streit WJ, Walter SA, Pennell NA. 1999. Reactive microgliosis. Prog Neurobiol 57:563-581.
64. Sun GY, Horrocks LA, Farooqui AA. 2007. The roles of NADPH oxidase and phophosipases A2 in oxidative and inflammatory responses in neuro degenerative diseases. J Neurochem 103:1-16.
65. Swanson JA, Watts C. 1995. Macropinocytosis. Trends Cell Biol 5:424- 428.
66. Takahashi K, Rochford CD, Neumann H. 2005. Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2. J Exp Med 201:647-657.
67. Tennent GA, Lovat LB, Pepys MB. 1995. Serum amyloid P component prevents proteolysis of the amyloid fibrils of Alzheimer disease and systemic amyloidosis. Proc Natl Acad Sci USA 92:4299-4303.
68. Walker EJ, Rosenberg GA. 2009. TIMP-3 and MMP-3 contribute to delayed inflammation and hippocampal neuronal death following global ischemia. Exp Neurol 216:122-131.
69. Walsh DT, Betmouni S, Perry VH. 2001. Absence of detectable IL-1beta production in murine prion disease: A model of chronic neurodegeneration. J Neuropathol Exp Neurol 60:173-182.
70. Walsh DT, Perry VH, Minghetti L. 2000. Cyclooxygenase-2 is highly expressed in microglial-like cells in a murine model of prion disease. Glia 29:392-396.
71. Wendt W, Lubbert H, Stichel CC. 2008. Upregulation of cathepsin S in the aging and pathological nervous system of mice. Brain Res 1232:7-20.
72. Williams AE, Lawson LJ, Perry VH, Fraser H. 1994. Characterization of the microglial response in murine scrapie. Neuropathol Appl Neurobiol 20:47-55.
73. Wisniewski HM, Barcikowska M, Kida E. 1991. Phagocytosis of beta/A4 amyloid fibrils of the neuritic neocortical plaques. Acta Neuropathol 81:588-590.