Identification of a specific α-synuclein peptide (α-Syn 29-40) capable of eliciting microglial superoxide production to damage dopaminergic neurons

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Wang, Shijun ^a,b   Chu, Chun Hsien ^b,c   Guo, Mingri ^b,d   Jiang, Lulu ^b,e   Nie, Hui ^b   Zhang, Wei ^f   Wilson, Belinda ^b   Yang, Li ^a   Stewart, Tessandra ^a   Hong, Jau Shyong ^b   Zhang, Jing ^a,g  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d TIANJIN MEDICAL UNIVERSITY   (China)

^e SHANDONG UNIVERSITY   (China)

^f CAPITAL MEDICAL UNIVERSITY   (China)

^g PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

gp91phox; Microglia; Neuronal damage; Superoxide; Synuclein

Indexed keywords

ALPHA SYNUCLEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; ACTIN BINDING PROTEIN; AIF1 PROTEIN, MOUSE; CALCIUM BINDING PROTEIN; CYBB PROTEIN, MOUSE; HLA ANTIGEN CLASS 2; IMMUNOGLOBULIN RECEPTOR; MEMBRANE PROTEIN; PEPTIDE FRAGMENT; PIRB PROTEIN, MOUSE; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CATALYSIS; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; GENE TRANSLOCATION; IMMUNOCHEMISTRY; MICROGLIA; MOUSE; NONHUMAN; OXIDATION; PEPTIDE ANALYSIS; PEPTIDE SYNTHESIS; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; CHEMISTRY; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETICS; GLIA; KNOCKOUT MOUSE; MAMMALIAN EMBRYO; MAPK SIGNALING; METABOLISM; NEWBORN; PROTEIN TRANSPORT;

ALPHA-SYNUCLEIN; ANIMALS; ANIMALS, NEWBORN; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; EMBRYO, MAMMALIAN; HISTOCOMPATIBILITY ANTIGENS CLASS II; MAP KINASE SIGNALING SYSTEM; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; NADPH OXIDASE; NEUROGLIA; PEPTIDE FRAGMENTS; PROTEIN TRANSPORT; RECEPTORS, IMMUNOLOGIC; SUPEROXIDES; TYROSINE 3-MONOOXYGENASE;

EID: 84978992714     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0606-7     Document Type: Article

References (46)

1. Maries E, Dass B, Collier TJ, Kordower JH, Steece-Collier K. The role of alpha-synuclein in Parkinson's disease: insights from animal models. Nat Rev Neurosci. 2003;4(9):727-38.
2. Irwin DJ, Lee VM, Trojanowski JQ. Parkinson's disease dementia: convergence of alpha-synuclein, tau and amyloid-beta pathologies. Nat Rev Neurosci. 2013;14(9):626-36.
3. Kim C, Ho DH, Suk JE, You S, Michael S, Kang J, Joong Lee S, Masliah E, Hwang D, Lee HJ, et al. Neuron-released oligomeric alpha-synuclein is an endogenous agonist of TLR2 for paracrine activation of microglia. Nat Commun. 2013;4:1562.
4. Zhang W, Wang T, Pei Z, Miller DS, Wu X, Block ML, Wilson B, Zhang W, Zhou Y, Hong JS, et al. Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J. 2005;19(6):533-42.
5. Lee HJ, Bae EJ, Lee SJ. Extracellular alpha-synuclein-a novel and crucial factor in Lewy body diseases. Nat Rev Neurol. 2014;10(2):92-8.
6. Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH. Mechanisms underlying inflammation in neurodegeneration. Cell. 2010;140(6):918-34.
7. Ueda K, Fukushima H, Masliah E, Xia Y, Iwai A, Yoshimoto M, Otero DA, Kondo J, Ihara Y, Saitoh T. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc Natl Acad Sci U S A. 1993;90(23):11282-6.
8. Bartels T, Choi JG, Selkoe DJ. Alpha-synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature. 2011;477(7362):107-10.
9. Burre J, Sharma M, Tsetsenis T, Buchman V, Etherton MR, Sudhof TC. Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science. 2010;329(5999):1663-7.
10. Giasson BI, Murray IV, Trojanowski JQ, Lee VM. A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly. J Biol Chem. 2001;276(4):2380-6.
11. Wood SJ, Wypych J, Steavenson S, Louis JC, Citron M, Biere AL. alpha-synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J Biol Chem. 1999;274(28):19509-12.
12. Bisaglia M, Trolio A, Bellanda M, Bergantino E, Bubacco L, Mammi S. Structure and topology of the non-amyloid-beta component fragment of human alpha-synuclein bound to micelles: implications for the aggregation process. Protein Sci. 2006;15(6):1408-16.
13. Li J, Uversky VN, Fink AL. Conformational behavior of human alpha-synuclein is modulated by familial Parkinson's disease point mutations A30P and A53T. Neurotoxicol. 2002;23(4-5):553-67.
14. Li J, Uversky VN, Fink AL. Effect of familial Parkinson's disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human alpha-synuclein. Biochem. 2001;40(38):11604-13.
15. Conway KA, Lee SJ, Rochet JC, Ding TT, Williamson RE, Lansbury Jr PT. Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc Natl Acad Sci U S A. 2000;97(2):571-6.
16. Zhang W, Dallas S, Zhang D, Guo JP, Pang H, Wilson B, Miller DS, Chen B, Zhang W, McGeer PL, et al. Microglial PHOX and Mac-1 are essential to the enhanced dopaminergic neurodegeneration elicited by A30P and A53T mutant alpha-synuclein. Glia. 2007;55(11):1178-88.
17. Wang S, Chu CH, Stewart T, Ginghina C, Wang Y, Nie H, Guo M, Wilson B, Hong JS, Zhang J. Alpha-synuclein, a chemoattractant, directs microglial migration via H2O2-dependent Lyn phosphorylation. Proc Natl Acad Sci U S A. 2015;112(15):E1926-35.
18. Chen SH, Oyarzabal EA, Hong JS. Preparation of rodent primary cultures for neuron-glia, mixed glia, enriched microglia, and reconstituted cultures with microglia. Methods Mol Biol. 2013;1041:231-40.
19. Tan AS, Berridge MV. Superoxide produced by activated neutrophils efficiently reduces the tetrazolium salt, WST-1 to produce a soluble formazan: a simple colorimetric assay for measuring respiratory burst activation and for screening anti-inflammatory agents. J Immunol Methods. 2000;238(1-2):59-68.
20. Wang S, Cao C, Chen Z, Bankaitis V, Tzima E, Sheibani N, Burridge K. Pericytes regulate vascular basement membrane remodeling and govern neutrophil extravasation during inflammation. PLoS One. 2012;7(9):e45499.
21. Qian L, Wei SJ, Zhang D, Hu X, Xu Z, Wilson B, El-Benna J, Hong JS, Flood PM. Potent anti-inflammatory and neuroprotective effects of TGF-beta1 are mediated through the inhibition of ERK and p47phox-Ser345 phosphorylation and translocation in microglia. J Immunol. 2008;181(1):660-8.
22. Taschenberger G, Garrido M, Tereshchenko Y, Bahr M, Zweckstetter M, Kugler S. Aggregation of alphaSynuclein promotes progressive in vivo neurotoxicity in adult rat dopaminergic neurons. Acta Neuropathol. 2012;123(5):671-83.
23. Friedman L, Mytilineou C. The toxicity of MPTP to dopamine neurons in culture is reduced at high concentrations. Neurosci Lett. 1987;79(1-2):65-72.
24. Casper D, Mytilineou C, Blum M. EGF enhances the survival of dopamine neurons in rat embryonic mesencephalon primary cell culture. J Neurosci Res. 1991;30(2):372-81.
25. Bronstein DM, Perez-Otano I, Sun V, Mullis Sawin SB, Chan J, Wu GC, Hudson PM, Kong LY, Hong JS, McMillian MK. Glia-dependent neurotoxicity and neuroprotection in mesencephalic cultures. Brain Res. 1995;704(1):112-6.
26. Hines DJ, Choi HB, Hines RM, Phillips AG, MacVicar BA. Prevention of LPS-induced microglia activation, cytokine production and sickness behavior with TLR4 receptor interfering peptides. PLoS One. 2013;8(3):e60388.
27. Raad H, Paclet MH, Boussetta T, Kroviarski Y, Morel F, Quinn MT, Gougerot-Pocidalo MA, Dang PM, El-Benna J. Regulation of the phagocyte NADPH oxidase activity: phosphorylation of gp91phox/NOX2 by protein kinase C enhances its diaphorase activity and binding to Rac2, p67phox, and p47phox. FASEB J. 2009;23(4):1011-22.
28. Wang Q, Chu CH, Qian L, Chen SH, Wilson B, Oyarzabal E, Jiang L, Ali S, Robinson B, Kim HC, et al. Substance P exacerbates dopaminergic neurodegeneration through neurokinin-1 receptor-independent activation of microglial NADPH oxidase. J Neurosci. 2014;34(37):12490-503.
29. Zhou H, Zhang F, Chen SH, Zhang D, Wilson B, Hong JS, Gao HM. Rotenone activates phagocyte NADPH oxidase by binding to its membrane subunit gp91phox. Free Radic Biol Med. 2012;52(2):303-13.
30. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87(1):245-313.
31. Dewas C, Fay M, Gougerot-Pocidalo MA, El-Benna J. The mitogen-activated protein kinase extracellular signal-regulated kinase 1/2 pathway is involved in formyl-methionyl-leucyl-phenylalanine-induced p47phox phosphorylation in human neutrophils. J Immunol. 2000;165(9):5238-44.
32. Namura S, Iihara K, Takami S, Nagata I, Kikuchi H, Matsushita K, Moskowitz MA, Bonventre JV, Alessandrini A. Intravenous administration of MEK inhibitor U0126 affords brain protection against forebrain ischemia and focal cerebral ischemia. Proc Natl Acad Sci U S A. 2001;98(20):11569-74.
33. Nielsen F, Mikkelsen BB, Nielsen JB, Andersen HR, Grandjean P. Plasma malondialdehyde as biomarker for oxidative stress: reference interval and effects of life-style factors. Clin Chem. 1997;43(7):1209-14.
34. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, Epplen JT, Schols L, Riess O. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet. 1998;18(2):106-8.
35. Lashuel HA, Overk CR, Oueslati A, Masliah E. The many faces of alpha-synuclein: from structure and toxicity to therapeutic target. Nat Rev Neurosci. 2013;14(1):38-48.
36. Kloetzel PM. Antigen processing by the proteasome. Nat Rev Mol Cell Biol. 2001;2(3):179-87.
37. Deleidi M, Maetzler W. Protein clearance mechanisms of alpha-synuclein and amyloid-Beta in lewy body disorders. Int J Alzheimer's Dis. 2012;2012:391438.
38. Smith LM, Schiess MC, Coffey MP, Klaver AC, Loeffler DA. Alpha-synuclein and anti-alpha-synuclein antibodies in Parkinson's disease, atypical Parkinson syndromes, REM sleep behavior disorder, and healthy controls. PLoS One. 2012;7(12):e52285.
39. Appel SH. CD4+ T cells mediate cytotoxicity in neurodegenerative diseases. J Clin Invest. 2009;119(1):13-5.
40. Brochard V, Combadiere B, Prigent A, Laouar Y, Perrin A, Beray-Berthat V, Bonduelle O, Alvarez-Fischer D, Callebert J, Launay JM, et al. Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J Clin Invest. 2009;119(1):182-92.
41. Cebrian C, Zucca FA, Mauri P, Steinbeck JA, Studer L, Scherzer CR, Kanter E, Budhu S, Mandelbaum J, Vonsattel JP, et al. MHC-I expression renders catecholaminergic neurons susceptible to T-cell-mediated degeneration. Nat Commun. 2014;5:3633.
42. Mosley RL, Hutter-Saunders JA, Stone DK, Gendelman HE. Inflammation and adaptive immunity in Parkinson's disease. Cold Spring Harbor Perspect Med. 2012;2(1):a009381.
43. Zhang D, Hu X, Qian L, Chen SH, Zhou H, Wilson B, Miller DS, Hong JS. Microglial MAC1 receptor and PI3K are essential in mediating beta-amyloid peptide-induced microglial activation and subsequent neurotoxicity. J Neuroinflammation. 2011;8(1):3.
44. Burgoyne JR, Madhani M, Cuello F, Charles RL, Brennan JP, Schroder E, Browning DD, Eaton P. Cysteine redox sensor in PKGIa enables oxidant-induced activation. Science. 2007;317(5843):1393-7.
45. Kemble DJ, Sun G. Direct and specific inactivation of protein tyrosine kinases in the Src and FGFR families by reversible cysteine oxidation. Proc Natl Acad Sci U S A. 2009;106(13):5070-5.
46. Chang F, Steelman LS, Lee JT, Shelton JG, Navolanic PM, Blalock WL, Franklin RA, McCubrey JA. Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention. Leukemia. 2003;17(7):1263-93.