Lack of alpha-synuclein modulates microglial phenotype in vitro

Neurochemical Research

Volumn 36, Issue 6, 2011, Pages 994-1004

  Austin, Susan A ^a   Rojanathammanee, Lalida ^a   Golovko, Mikhail Y ^a   Murphy, Eric J ^a   Combs, Colin K ^a  

^a UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

Synuclein; Cytokine; Microglia; Parkinson; Phagocytosis; Phospholipase D

Indexed keywords

ALPHA SYNUCLEIN; BUTANOL; CYCLOOXYGENASE 2; CYTOSOLIC PHOSPHOLIPASE A2; PHOSPHOLIPASE D2; PROSTAGLANDIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME INHIBITION; IN VITRO STUDY; MICROGLIA; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ALPHA-SYNUCLEIN; ANIMALS; BLOTTING, WESTERN; MICE; MICE, KNOCKOUT; MICROGLIA;

MUS;

EID: 79955704402     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-011-0439-9     Document Type: Article

References (75)

1. Larsen KE, Schmitz Y, Troyer MD, Mosharov E, Dietrich P, Quazi AZ, Savalle M, Nemani V, Chaudhry FA, Edwards RH, Stefanis L, Sulzer D (2006) Alpha-synuclein overexpression in PC12 and chromaffin cells impairs catecholamine release by interfering with a late step in exocytosis. J Neurosci 26:11915-11922 (Pubitemid 44772102)
2. Gitler AD, Bevis BJ, Shorter J, Strathearn KE, Hamamichi S, Su LJ, Caldwell KA, Caldwell GA, Rochet JC, McCaffery JM, Barlowe C, Lindquist S (2008) The Parkinson's disease protein alpha-synuclein disrupts cellular Rab homeostasis. Proc Natl Acad Sci U S A 105:145-150
3. Maroteaux L, Campanelli JT, Scheller RH (1988) Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J Neurosci 8:2804-2815
4. Shibayama-Imazu T, Okahashi I, Omata K, Nakajo S, Ochiai H, Nakai Y, Hama T, Nakamura Y, Nakaya K (1993) Cell and tissue distribution and developmental change of neuron specific 14 kDa protein (phosphoneuroprotein 14). Brain Res 622:17-25 (Pubitemid 23264942)
5. Ahn BH, Rhim H, Kim SY, Sung YM, Lee MY, Choi JY, Wolozin B, Chang JS, Lee YH, Kwon TK, Chung KC, Yoon SH, Hahn SJ, Kim MS, Jo YH, Min DS (2002) alpha-Synuclein interacts with phospholipase D isozymes and inhibits pervanadate-induced phospholipase D activation in human embryonic kidney-293 cells. J Biol Chem 277:12334-12342 (Pubitemid 34952804)
6. Peng J, Stevenson FF, Doctrow SR, Andersen JK (2005) Superoxide dismutase/catalase mimetics are neuroprotective against selective paraquat-mediated dopaminergic neuron death in the substantial nigra: implications for Parkinson disease. J Biol Chem 280:29194-29198 (Pubitemid 41161371)
7. Meulener MC, Graves CL, Sampathu DM, Armstrong-Gold CE, Bonini NM, Giasson BI (2005) DJ-1 is present in a large molecular complex in human brain tissue and interacts with alpha-synuclein. J Neurochem 93:1524-1532 (Pubitemid 40853275)
8. Murphy DD, Rueter SM, Trojanowski JQ, Lee VM (2000) Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J Neurosci 20:3214-3220 (Pubitemid 30263139)
9. Castagnet PI, Golovko MY, Barcelo-Coblijn GC, Nussbaum RL, Murphy EJ (2005) Fatty acid incorporation is decreased in astrocytes cultured from alpha-synuclein gene-ablated mice. J Neurochem 94:839-849 (Pubitemid 41098515)
10. Golovko MY, Faergeman NJ, Cole NB, Castagnet PI, Nussbaum RL, Murphy EJ (2005) Alpha-synuclein gene deletion decreases brain palmitate uptake and alters the palmitate metabolism in the absence of alpha-synuclein palmitate binding. Biochemistry 44:8251-8259 (Pubitemid 40799905)
11. Golovko MY, Barcelo-Coblijn G, Castagnet PI, Austin S, Combs CK, Murphy EJ (2009) The role of alpha-synuclein in brain lipid metabolism: a downstream impact on brain inflammatory response. Mol Cell Biochem 326:55-66
12. Golovko MY, Murphy EJ (2008) Brain prostaglandin formation is increased by alpha-synuclein gene-ablation during global ischemia. Neurosci Lett 432:243-247
13. Wislet-Gendebien S, D'Souza C, Kawarai T, St George-Hyslop P, Westaway D, Fraser P, Tandon A (2006) Cytosolic proteins regulate alpha-synuclein dissociation from presynaptic membranes. J Biol Chem 281:32148-32155 (Pubitemid 46036769)
14. Richter-Landsberg C, Gorath M, Trojanowski JQ, Lee VM (2000) alpha-Synuclein is developmentally expressed in cultured rat brain oligodendrocytes. J Neurosci Res 62:9-14
15. Mori S (2002) Responses to donepezil in Alzheimer's disease and Parkinson's disease. Ann N Y Acad Sci 977:493-500
16. Cheng SY, Trombetta LD (2004) The induction of amyloid precursor protein and alpha-synuclein in rat hippocampal astrocytes by diethyldithiocarbamate and copper with or without glutathione. Toxicol Lett 146:139-149 (Pubitemid 37487828)
17. Austin SA, Floden AM, Murphy EJ, Combs CK (2006) Alpha-synuclein expression modulates microglial activation phenotype. J Neurosci 26:10558-10563 (Pubitemid 44564607)
18. Kim S, Cho SH, Kim KY, Shin KY, Kim HS, Park CH, Chang KA, Lee SH, Cho D, Suh YH (2009) Alpha-synuclein induces migration of BV-2 microglial cells by up-regulation of CD44 and MT1-MMP. J Neurochem 109:1483-1496
19. Zhang F, Zhao G, Dong Z (2001) Phosphatidylcholine-specific phospholipase C and D in stimulation of RAW264.7 mouse macrophage-like cells by lipopolysaccharide. Int Immunopharmacol 1:1375-1384 (Pubitemid 32522989)
20. Sethu S, Mendez-Corao G, Melendez AJ (2008) Phospholipase D1 plays a key role in TNF-alpha signaling. J Immunol 180:6027-6034
21. De Valck D, Beyaert R, Van Roy F, Fiers W (1993) Tumor necrosis factor cytotoxicity is associated with phospholipase D activation. Eur J Biochem 212:491-497 (Pubitemid 23076118)
22. Iyer SS, Barton JA, Bourgoin S, Kusner DJ (2004) Phospholipases D1 and D2 coordinately regulate macrophage phagocytosis. J Immunol 173:2615-2623 (Pubitemid 39063121)
23. Jenco JM, Rawlingson A, Daniels B, Morris AJ (1998) Regulation of phospholipase D2: selective inhibition of mammalian phospholipase D isoenzymes by alpha- and beta-synucleins. Biochemistry 37:4901-4909 (Pubitemid 28175972)
24. Outeiro TF, Lindquist S (2003) Yeast cells provide insight into alpha-synuclein biology and pathobiology. Science 302:1772-1775 (Pubitemid 37505742)
25. Payton JE, Perrin RJ, Woods WS, George JM (2004) Structural determinants of PLD2 inhibition by alpha-synuclein. J Mol Biol 337:1001-1009 (Pubitemid 38368940)
26. Cabin DE, Shimazu K, Murphy D, Cole NB, Gottschalk W, McIlwain KL, Orrison B, Chen A, Ellis CE, Paylor R, Lu B, Nussbaum RL (2002) Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking alpha-synuclein. J Neurosci 22:8797-8807 (Pubitemid 35379049)
27. Jara JH, Singh BB, Floden AM, Combs CK (2007) Tumor necrosis factor alpha stimulates NMDA receptor activity in mouse cortical neurons resulting in ERK-dependent death. J Neurochem 100:1407-1420
28. Sondag CM, Combs CK (2010) Adhesion of monocytes to type I collagen stimulates an APP-dependent proinflammatory signaling response and release of Abeta1-40. J Neuroinflammation 7:22
29. Sondag CM, Combs CK (2004) Amyloid precursor protein mediates proinflammatory activation of monocytic lineage cells. J Biol Chem 279:14456-14463 (Pubitemid 38468988)
30. Austin SA, Combs CK (2008) Amyloid precursor protein mediates monocyte adhesion in AD tissue and apoE(-)/(-) mice. Neurobiol Aging 31:1854-1866
31. Golovko MY, Murphy EJ (2008) An improved LC-MS/MS procedure for brain prostanoid analysis using brain fixation with head-focused microwave irradiation and liquid-liquid extraction. J Lipid Res 49:893-902
32. Barcelo-Coblijn G, Golovko MY, Weinhofer I, Berger J, Murphy EJ (2007) Brain neutral lipids mass is increased in alpha-synuclein gene-ablated mice. J Neurochem 101:132-141 (Pubitemid 46426471)
33. Golovko MY, Rosenberger TA, Feddersen S, Faergeman NJ, Murphy EJ (2007) Alpha-synuclein gene ablation increases docosahexaenoic acid incorporation and turnover in brain phospholipids. J Neurochem 101:201-211 (Pubitemid 46426477)
34. Golovko MY, Rosenberger TA, Faergeman NJ, Feddersen S, Cole NB, Pribill I, Berger J, Nussbaum RL, Murphy EJ (2006) Acyl-CoA synthetase activity links wild-type but not mutant alpha-synuclein to brain arachidonate metabolism. Biochemistry 45:6956-6966 (Pubitemid 43856680)
35. Bodner CR, Maltsev AS, Dobson CM, Bax A (2010) Differential phospholipid binding of alpha-synuclein variants implicated in Parkinson's disease revealed by solution NMR spectroscopy. Biochemistry 49:862-871
36. Trexler AJ, Rhoades E (2009) Alpha-synuclein binds large unilamellar vesicles as an extended helix. Biochemistry 48:2304-2306
37. Perrin RJ, Woods WS, Clayton DF, George JM (2000) Interaction of human alpha-Synuclein and Parkinson's disease variants with phospholipids. Structural analysis using site-directed mutagenesis. J Biol Chem 275:34393-34398
38. Fujita K, Murakami M, Yamashita F, Amemiya K, Kudo I (1996) Phospholipase D is involved in cytosolic phospholipase A2-dependent selective release of arachidonic acid by fMLP-stimulated rat neutrophils. FEBS Lett 395:293-298 (Pubitemid 26356204)
39. Bauldry SA, Wooten RE (1997) Induction of cytosolic phospholipase A2 activity by phosphatidic acid and diglycerides in permeabilized human neutrophils: interrelationship between phospholipases D and A2. Biochem J 322(Pt 2):353-363 (Pubitemid 27116557)
40. Lee SD, Lee BD, Han JM, Kim JH, Kim Y, Suh PG, Ryu SH (2000) Phospholipase D2 activity suppresses hydrogen peroxide-induced apoptosis in PC12 cells. J Neurochem 75:1053-1059 (Pubitemid 30660493)
41. Hamdi SM, Cariven C, Coronas S, Malet N, Chap H, Perret B, Salles JP, Record M (2008) Potential role of phospholipase D2 in increasing interleukin-2 production by T-lymphocytes through activation of mitogen-activated protein kinases ERK1/ERK2. Biochim Biophys Acta 1781:263-269
42. Combs CK, Karlo JC, Kao SC, Landreth GE (2001) beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J Neurosci 21:1179-1188 (Pubitemid 32128763)
43. Wilms H, Rosenstiel P, Romero-Ramos M, Arlt A, Schafer H, Seegert D, Kahle PJ, Odoy S, Claasen JH, Holzknecht C, Brandenburg LO, Deuschl G, Schreiber S, Kirik D, Lucius R (2009) Suppression of MAP kinases inhibits microglial activation and attenuates neuronal cell death induced by alpha-synuclein protofibrils. Int J Immunopathol Pharmacol 22:897-909
44. Lee SB, Park SM, Ahn KJ, Chung KC, Paik SR, Kim J (2009) Identification of the amino acid sequence motif of alpha-synuclein responsible for macrophage activation. Biochem Biophys Res Commun 381:39-43
45. Reynolds AD, Stone DK, Mosley RL, Gendelman HE (2009) Nitrated {alpha}-synuclein-induced alterations in microglial immunity are regulated by CD4+ T cell subsets. J Immunol 182:4137-4149
46. Su X, Maguire-Zeiss KA, Giuliano R, Prifti L, Venkatesh K, Federoff HJ (2008) Synuclein activates microglia in a model of Parkinson's disease. Neurobiol Aging 29:1690-1701
47. Zhang W, Wang T, Pei Z, Miller DS, Wu X, Block ML, Wilson B, Zhou Y, Hong JS, Zhang J (2005) Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. Faseb J 19:533-542 (Pubitemid 40471244)
48. Zhang W, Dallas S, Zhang D, Guo JP, Pang H, Wilson B, Miller DS, Chen B, McGeer PL, Hong JS, Zhang J (2007) Microglial PHOX and Mac-1 are essential to the enhanced dopaminergic neurodegeneration elicited by A30P and A53T mutant alpha-synuclein. Glia 55:1178-1188 (Pubitemid 47204209)
49. Klegeris A, Pelech S, Giasson BI, Maguire J, Zhang H, McGeer EG, McGeer PL (2008) Alpha-synuclein activates stress signaling protein kinases in THP-1 cells and microglia. Neurobiol Aging 29:739-752 (Pubitemid 351400820)
50. Klegeris A, Giasson BI, Zhang H, Maguire J, Pelech S, McGeer PL (2006) Alpha-synuclein and its disease-causing mutants induce ICAM-1 and IL-6 in human astrocytes and astrocytoma cells. FASEB J 20:2000-2008 (Pubitemid 44953900)
51. Jin J, Shie FS, Liu J, Wang Y, Davis J, Schantz AM, Montine KS, Montine TJ, Zhang J (2007) Prostaglandin E2 receptor subtype 2 (EP2) regulates microglial activation and associated neurotoxicity induced by aggregated alpha-synuclein. J Neuroinflammation 4:2
52. Sanchez-Guajardo V, Febbraro F, Kirik D, Romero-Ramos M (2010) Microglia acquire distinct activation profiles depending on the degree of alpha-synuclein neuropathology in a rAAV based model of Parkinson's disease. PLoS One 5:e8784
53. El-Agnaf OM, Walsh DM, Allsop D (2003) Soluble oligomers for the diagnosis of neurodegenerative diseases. Lancet Neurol 2:461-462 (Pubitemid 36876102)
54. Lee HJ, Patel S, Lee SJ (2005) Intravesicular localization and exocytosis of alpha-synuclein and its aggregates. J Neurosci 25:6016-6024 (Pubitemid 40911433)
55. Lee JK, Tran T, Tansey MG (2009) Neuroinflammation in Parkinson's disease. J Neuroimmune Pharmacol 4:419-429
56. Ramakrishnan M, Jensen PH, Marsh D (2006) Association of alpha-synuclein and mutants with lipid membranes: spin-label ESR and polarized IR. Biochemistry 45:3386-3395 (Pubitemid 43376357)
57. Locati M, Riboldi E, Bonecchi R, Transidico P, Bernasconi S, Haribabu B, Morris AJ, Mantovani A, Sozzani S (2001) Selective induction of phospholipase D1 in pathogen-activated human monocytes. Biochem J 358:119-125 (Pubitemid 32778105)
58. Kim JH, Lee BD, Kim Y, Lee SD, Suh PG, Ryu SH (1999) Cytosolic phospholipase A2-mediated regulation of phospholipase D2 in leukocyte cell lines. J Immunol 163:5462-5470
59. Corrotte M, Chasserot-Golaz S, Huang P, Du G, Ktistakis NT, Frohman MA, Vitale N, Bader MF, Grant NJ (2006) Dynamics and function of phospholipase D and phosphatidic acid during phagocytosis. Traffic 7:365-377 (Pubitemid 43323962)
60. Gomez-Cambronero J, Horwitz J, Sha'afi RI (2003) Measurements of phospholipases A2, C, and D (PLA2, PLC, and PLD). In vitro microassays, analysis of enzyme isoforms, and intact-cell assays. Methods Mol Biol 218:155-176
61. Maxfield FR, McGraw TE (2004) Endocytic recycling. Nat Rev Mol Cell Biol 5:121-132 (Pubitemid 38160255)
62. Kirchhausen T (2000) Three ways to make a vesicle. Nat Rev Mol Cell Biol 1:187-198
63. Liu J, Zhang JP, Shi M, Quinn T, Bradner J, Beyer R, Chen S, Zhang J (2009) Rab11a and HSP90 regulate recycling of extracellular alpha-synuclein. J Neurosci 29:1480-1485
64. Minghetti L, Polazzi E, Nicolini A, Creminon C, Levi G (1997) Up-regulation of cyclooxygenase-2 expression in cultured microglia by prostaglandin E2, cyclic AMP and non-steroidal anti-inflammatory drugs. Eur J Neurosci 9:934-940
65. Nagano T, Kimura SH, Takemura M (2010) Prostaglandin E(2) reduces amyloid beta-induced phagocytosis in cultured rat microglia. Brain Res 1323:11-17
66. Ben Gedalya T, Loeb V, Israeli E, Altschuler Y, Selkoe DJ, Sharon R (2009) Alpha-synuclein and polyunsaturated fatty acids promote clathrin-mediated endocytosis and synaptic vesicle recycling. Traffic 10:218-234
67. Yang X, Du L, Tang X, Jung SY, Zheng B, Soh BY, Kim SY, Gu Q, Park H (2009) Brevicompanine E reduces lipopolysaccharide-induced production of proinflammatory cytokines and enzymes in microglia by inhibiting activation of activator protein-1 and nuclear factor-kappaB. J Neuroimmunol 216:32-38
68. Sugama S, Takenouchi T, Cho BP, Joh TH, Hashimoto M, Kitani H (2009) Possible roles of microglial cells for neurotoxicity in clinical neurodegenerative diseases and experimental animal models. Inflamm Allergy Drug Targets 8:277-284
69. Ock J, Kim S, Yi KY, Kim NJ, Han HS, Cho JY, Suk K (2010) A novel anti-neuroinflammatory pyridylimidazole compound KR-31360. Biochem Pharmacol 79:596-609
70. McGeer PL, McGeer EG (2004) Inflammation and neurodegeneration in Parkinson's disease. Parkinsonism Relat Disord 10(Suppl 1):S3-S7 (Pubitemid 38510423)
71. Teismann P, Schulz JB (2004) Cellular pathology of Parkinson's disease: astrocytes, microglia and inflammation. Cell Tissue Res 318:149-161 (Pubitemid 39362635)
72. Croisier E, Moran LB, Dexter DT, Pearce RK, Graeber MB (2005) Microglial inflammation in the parkinsonian substantia nigra: relationship to alpha-synuclein deposition. J Neuroinflammation 2:14
73. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, Di Iorio G, Golbe LI, Nussbaum RL (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276:2045-2047 (Pubitemid 27443610)
74. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, Epplen JT, Schols L, Riess O (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 18:106-108
75. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, Peuralinna T, Dutra A, Nussbaum R, Lincoln S, Crawley A, Hanson M, Maraganore D, Adler C, Cookson MR, Muenter M, Baptista M, Miller D, Blancato J, Hardy J, Gwinn-Hardy K (2003) alpha-Synuclein locus triplication causes Parkinson's disease. Science 302:841 (Pubitemid 37339619)