Fractalkine over expression suppresses α-synuclein-mediated neurodegeneration

Molecular Therapy

Volumn 23, Issue 1, 2015, Pages 17-23

  Nash, Kevin R ^a   Moran, Peter ^a   Finneran, Dylan J ^a   Hudson, Charles ^b   Robinson, Jesse ^a   Morgan, Dave ^a   Bickford, Paula C ^b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; FRACTALKINE; GLIAL FIBRILLARY ACIDIC PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PARVOVIRUS VECTOR; TYROSINE 3 MONOOXYGENASE; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; CX3CL1 PROTEIN, MOUSE; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; HLA ANTIGEN CLASS 2; NERVE PROTEIN; OXIDOPAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DRUG MECHANISM; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; NERVE DEGENERATION; NONHUMAN; PROMOTER REGION; RAT; STEREOLOGY; SUBSTANTIA NIGRA; VIRAL GENE THERAPY; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; ANTIGEN PRESENTATION; CHEMICALLY INDUCED; DEPENDOPARVOVIRUS; GENE EXPRESSION REGULATION; GENE THERAPY; GENE VECTOR; GENETICS; METABOLISM; MICROGLIA; MOUSE; NERVE CELL; PARKINSON DISEASE, SECONDARY; PARKINSONIAN DISORDERS; PATHOLOGY; PROCEDURES; SIGNAL TRANSDUCTION;

ANIMALIA; MUS; RATTUS;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ALPHA-SYNUCLEIN; ANIMALS; ANTIGEN PRESENTATION; ASTROCYTES; CHEMOKINE CX3CL1; DEPENDOVIRUS; GENE EXPRESSION REGULATION; GENETIC THERAPY; GENETIC VECTORS; HISTOCOMPATIBILITY ANTIGENS CLASS II; MALE; MICE; MICROGLIA; NERVE TISSUE PROTEINS; NEURONS; OXIDOPAMINE; PARKINSON DISEASE, SECONDARY; PARKINSONIAN DISORDERS; PROMOTER REGIONS, GENETIC; RATS; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE;

EID: 84920628654     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.175     Document Type: Article

References (49)

1. Reynolds, AD, Banerjee, R, Liu, J, Gendelman, HE and Mosley, RL (2007). Neuroprotective activities of CD4+CD25+ regulatory T cells in an animal model of Parkinson's disease. J Leukoc Biol 82: 1083-1094.
2. Zhang, W, Wang, T, Pei, Z, Miller, DS, Wu, X, Block, ML et al. (2005). Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J 19: 533-542.
3. Blandini, F (2013). Neural and immune mechanisms in the pathogenesis of Parkinson's disease. J Neuroimmune Pharmacol 8: 189-201.
4. Béraud, D, Hathaway, HA, Trecki, J, Chasovskikh, S, Johnson, DA, Johnson, JA et al. (2013). Microglial activation and antioxidant responses induced by the Parkinson's disease protein α-synuclein. J Neuroimmune Pharmacol 8: 94-117.
5. Biber, K, Vinet, J and Boddeke, HW (2008). Neuron-microglia signaling: chemokines as versatile messengers. J Neuroimmunol 198: 69-74.
6. Hanisch, UK and Kettenmann, H (2007). Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10: 1387-1394.
7. Schwartz, M, Butovsky, O, Brück, W and Hanisch, UK (2006). Microglial phenotype: is the commitment reversible? Trends Neurosci 29: 68-74.
8. Biber, K, Neumann, H, Inoue, K and Boddeke, HW (2007). Neuronal 'On' and 'Off' signals control microglia. Trends Neurosci 30: 596-602.
9. Galea, I, Bechmann, I and Perry, VH (2007). What is immune privilege (not)? Trends Immunol 28: 12-18.
10. Bachstetter, AD, Morganti, JM, Jernberg, J, Schlunk, A, Mitchell, SH, Brewster, KW et al. (2011). Fractalkine and CX 3 CR1 regulate hippocampal neurogenesis in adult and aged rats. Neurobiol Aging 32: 2030-2044.
11. Pabon, MM, Bachstetter, AD, Hudson, CE, Gemma, C and Bickford, PC (2011). CX3CL1 reduces neurotoxicity and microglial activation in a rat model of Parkinson's disease. J Neuroinfammation 8: 9.
12. Harrison, JK, Jiang, Y, Chen, S, Xia, Y, Maciejewski, D, McNamara, RK et al. (1998). Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci USA 95: 10896-10901.
13. Ransohoff, RM, Liu, L and Cardona, AE (2007). Chemokines and chemokine receptors: multipurpose players in neuroinfammation. Int Rev Neurobiol 82: 187-204.
14. Wynne, AM, Henry, CJ, Huang, Y, Cleland, A and Godbout, JP (2010). Protracted downregulation of CX3CR1 on microglia of aged mice after lipopolysaccharide challenge. Brain Behav Immun 24: 1190-1201.
15. Mizutani, N, Sakurai, T, Shibata, T, Uchida, K, Fujita, J, Kawashima, R et al. (2007). Dose-dependent differential regulation of cytokine secretion from macrophages by fractalkine. J Immunol 179: 7478-7487.
16. Lyons, A, Lynch, AM, Downer, EJ, Hanley, R, O'Sullivan, JB, Smith, A et al. (2009). Fractalkine-induced activation of the phosphatidylinositol-3 kinase pathway attentuates microglial activation in vivo and in vitro. J Neurochem 110: 1547-1556.
17. Maciejewski-Lenoir, D, Chen, S, Feng, L, Maki, R and Bacon, KB (1999). Characterization of fractalkine in rat brain cells: migratory and activation signals for CX3CR-1-expressing microglia. J Immunol 163: 1628-1635.
18. Ré, DB and Przedborski, S (2006). Fractalkine: moving from chemotaxis to neuroprotection. Nat Neurosci 9: 859-861.
19. Zujovic, V, Benavides, J, Vigé, X, Carter, C and Taupin, V (2000). Fractalkine modulates TNF-alpha secretion and neurotoxicity induced by microglial activation. Glia 29: 305-315.
20. Garcia, GE, Xia, Y, Chen, S, Wang, Y, Ye, RD, Harrison, JK et al. (2000). NF-kappaB-dependent fractalkine induction in rat aortic endothelial cells stimulated by IL-1beta, TNF-alpha, and LPS. J Leukoc Biol 67: 577-584.
21. Ludwig, A and Weber, C (2007). Transmembrane chemokines: versatile 'special agents' in vascular infammation. Thromb Haemost 97: 694-703.
22. Garton, KJ, Gough, PJ, Blobel, CP, Murphy, G, Greaves, DR, Dempsey, PJ et al. (2001). Tumor necrosis factor-alpha-converting enzyme (ADAM17) mediates the cleavage and shedding of fractalkine (CX3CL1). J Biol Chem 276: 37993-38001.
23. Hundhausen, C, Misztela, D, Berkhout, TA, Broadway, N, Saftig, P, Reiss, K et al. (2003). The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood 102: 1186-1195.
24. Chapman, GA, Moores, K, Harrison, D, Campbell, CA, Stewart, BR and Strijbos, PJ (2000). Fractalkine cleavage from neuronal membranes represents an acute event in the infammatory response to excitotoxic brain damage. J Neurosci 20: RC87.
25. Imai, T, Hieshima, K, Haskell, C, Baba, M, Nagira, M, Nishimura, M et al. (1997). Identifcation and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion. Cell 91: 521-530.
26. Kim, KW, Vallon-Eberhard, A, Zigmond, E, Farache, J, Shezen, E, Shakhar, G et al. (2011). In vivo structure/function and expression analysis of the CX3C chemokine fractalkine. Blood 118: e156-e167.
27. Yoneda, O, Imai, T, Nishimura, M, Miyaji, M, Mimori, T, Okazaki, T et al. (2003). Membrane-bound form of fractalkine induces IFN-gamma production by NK cells. Eur J Immunol 33: 53-58.
28. Lee, S, Varvel, NH, Konerth, ME, Xu, G, Cardona, AE, Ransohoff, RM et al. (2010). CX3CR1 defciency alters microglial activation and reduces beta-amyloid deposition in two Alzheimer's disease mouse models. Am J Pathol 177: 2549-2562.
29. Bhaskar, K, Konerth, M, Kokiko-Cochran, ON, Cardona, A, Ransohoff, RM and Lamb, BT (2010). Regulation of tau pathology by the microglial fractalkine receptor. Neuron 68: 19-31.
30. Nash, KR, Lee, DC, Hunt, JB Jr, Morganti, JM, Selenica, ML, Moran, P et al. (2013). Fractalkine overexpression suppresses tau pathology in a mouse model of tauopathy. Neurobiol Aging 34: 1540-1548.
31. Morganti, JM, Nash, KR, Grimmig, BA, Ranjit, S, Small, B, Bickford, PC et al. (2012). The soluble isoform of CX3CL1 is necessary for neuroprotection in a mouse model of Parkinson's disease. J Neurosci 32: 14592-14601.
32. Gorbatyuk, OS, Li, S, Sullivan, LF, Chen, W, Kondrikova, G, Manfredsson, FP et al. (2008). The phosphorylation state of Ser-129 in human alpha-synuclein determines neurodegeneration in a rat model of Parkinson disease. Proc Natl Acad Sci USA 105: 763-768.
33. Pabon, MM, Jernberg, JN, Morganti, J, Contreras, J, Hudson, CE, Klein, RL et al. (2012). A spirulina-enhanced diet provides neuroprotection in an α-synuclein model of Parkinson's disease. PLoS One 7: e45256.
34. Carty, N, Lee, D, Dickey, C, Ceballos-Diaz, C, Jansen-West, K, Golde, TE et al. (2010). Convection-enhanced delivery and systemic mannitol increase gene product distribution of AAV vectors 5, 8, and 9 and increase gene product in the adult mouse brain. J Neurosci Methods 194: 144-153.
35. Burger, C, Gorbatyuk, OS, Velardo, MJ, Peden, CS, Williams, P, Zolotukhin, S et al. (2004). Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential effciency and cell tropism after delivery to different regions of the central nervous system. Mol Ther 10: 302-317.
36. Klein, RL, Dayton, RD, Tatom, JB, Henderson, KM and Henning, PP (2008). AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purifcation method. Mol Ther 16: 89-96.
37. Cardona, AE, Pioro, EP, Sasse, ME, Kostenko, V, Cardona, SM, Dijkstra, IM et al. (2006). Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9: 917-924.
38. Morganti, JM, Nash, KR, Grimmig, BA, Ranjit, S, Small, B, Bickford, PC et al. (2012). The soluble isoform of CX3CL1 is necessary for neuroprotection in a mouse model of Parkinson's disease. J Neurosci 32: 14592-14601.
39. Hjortø, GM, Hansen, M, Larsen, NB and Kledal, TN (2009). Generating substrate bound functional chemokine gradients in vitro. Biomaterials 30: 5305-5311.
40. Lawlor, PA, Bland, RJ, Mouravlev, A, Young, D and During, MJ (2009). Effcient gene delivery and selective transduction of glial cells in the mammalian brain by AAV serotypes isolated from nonhuman primates. Mol Ther 17: 1692-1702.
41. von Jonquieres, G, Mersmann, N, Klugmann, CB, Harasta, AE, Lutz, B, Teahan, O et al. (2013). Glial promoter selectivity following AAV-delivery to the immature brain. PLoS One 8: e65646.
42. Lee, DC, Ruiz, CR, Lebson, L, Selenica, ML, Rizer, J, Hunt, JB Jr et al. (2013). Aging enhances classical activation but mitigates alternative activation in the central nervous system. Neurobiol Aging 34: 1610-1620.
43. Polazzi, E and Monti, B (2010). Microglia and neuroprotection: from in vitro studies to therapeutic applications. Prog Neurobiol 92: 293-315.
44. Streit, WJ (2005). Microglia and neuroprotection: implications for Alzheimer's disease. Brain Res Brain Res Rev 48: 234-239.
45. Kordower, JH and Bjorklund, A (2013). Trophic factor gene therapy for Parkinson's disease. Mov Disord 28: 96-109.
46. Lo Bianco, C, Déglon, N, Pralong, W and Aebischer, P (2004). Lentiviral nigral delivery of GDNF does not prevent neurodegeneration in a genetic rat model of Parkinson's disease. Neurobiol Dis 17: 283-289.
47. Decressac, M, Ulusoy, A, Mattsson, B, Georgievska, B, Romero-Ramos, M, Kirik, D et al. (2011). GDNF fails to exert neuroprotection in a rat α-synuclein model of Parkinson's disease. Brain 134(Pt 8): 2302-2311.
48. Chesselet, MF (2008). In vivo alpha-synuclein overexpression in rodents: a useful model of Parkinson's disease? Exp Neurol 209: 22-27.
49. Gorbatyuk, OS, Li, S, Nash, K, Gorbatyuk, M, Lewin, AS, Sullivan, LF et al. (2010). In vivo RNAi-mediated alpha-synuclein silencing induces nigrostriatal degeneration. Mol Ther 18: 1450-1457.