CX3CL1 is neuroprotective in permanent focal cerebral ischemia in rodents

Journal of Neuroscience

Volumn 31, Issue 45, 2011, Pages 16327-16335

  Cipriani, Raffaela ^a   Villa, Pia ^b,c   Chece, Giuseppina ^a   Lauro, Clotilde ^a   Paladini, Alessandra ^c   Micotti, Edoardo ^c   Perego, Carlo ^c   de Simoni, Maria Grazia ^c   Fredholm, Bertil B ^d   Eusebi, Fabrizio ^a,e   Limatola, Cristina ^a,e  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b CNR   (Italy)

^c MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^d KAROLINSKA INSTITUTE   (Sweden)

^e IRCCS NEUROMED   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE A1 RECEPTOR; CASPASE 3; CHEMOKINE RECEPTOR CX3CR1; FRACTALKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; CULTURE MEDIUM; DRUG MECHANISM; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL CULTURE; NEUROLOGIC DISEASE; NEUROPROTECTION; NEWBORN; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; RAT;

ADENOSINE A1 RECEPTOR ANTAGONISTS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANIMALS, NEWBORN; ANOXIA; BRAIN INFARCTION; CELLS, CULTURED; CEREBRAL CORTEX; CHEMOKINE CX3CL1; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLUCOSE; GREEN FLUORESCENT PROTEINS; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; NERVOUS SYSTEM DISEASES; NEURONS; PHAGOCYTOSIS; RATS; RECEPTORS, CHEMOKINE; RECEPTORS, PURINERGIC P1; XANTHINES;

EID: 80755127243     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3611-11.2011     Document Type: Article

References (50)

1. Barone FC, Schmidt DB, Hillegass LM, Price WJ, White RF, Feuerstein GZ, Clark RK, Lee EV, Griswold DE, Sarau HM (1992) Reperfusion increases neutrophils and leukotriene B4 receptor binding in rat focal ischemia. Stroke 23:1337-1348.
2. Bhaskar K, Konerth M, Kokiko-Cochran ON, Cardona A, Ransohoff RM, Lamb BT (2010) Regulation of tau pathology by the microglial fractalkine receptor. Neuron 68:19-31.
3. Biber K, Neumann H, Inoue K, Boddeke HW (2007) WGMNeuronal "On" and "Off" signals control microglia. Trends Neurosci 30:596-602.
4. Block ML, Zecca L, Hong JS (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8:57-69.
5. Broughton BR, Reutens DC, Sobey CG (2009) Apoptotic mechanisms after cerebral ischemia. Stroke 40:e331-e339.
6. Burguillos MA, Deierborg T, Kavanagh E, Persson A, Hajji N, Garcia-Quintanilla A, Cano J, Brundin P, Englund E, Venero JL, Joseph B (2011) Caspase signalling controls microglia activation and neurotoxicity. Nature 472:319-324.
7. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM (2006) Control of microglia neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917-924.
8. Chapman GA, Moores K, Harrison D, Campbell CA, Stewart BR, Strijbos PJ (2000) Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. J Neurosci 20:RC87(1-5).
9. Cook DN, Chen SC, Sullivan LM, Manfra DJ, Wiekowski MT, Prosser DM, Vassileva G, Lira SA (2001) Generation and analysis of mice lacking the chemokine fractalkine. Mol Cell Biol 21:3159-3165.
10. Cunha RA (2005) Neuroprotection by adenosine in the brain: from A1 receptor activation to A2A receptor blockade. Purinergic Signal 1:111-134.
11. Dénes A, Ferenczi S, Halász J, Környei Z, Kovács KJ (2008) Role of CX3CR1 (fractalkine receptor) in brain damage and inflammation induced by focal cerebral ischemia in mouse. J Cereb Blood Flow Metab 28:1707-1721.
12. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischemic stroke: an integrated view. Trends Neurosci 22:391-397.
13. Fredholm BB (2007) Adenosine, an endogenous distress signal, modulates tissue damage and repair. Cell Death Differ 14:1315-1323.
14. Fuhrmann M, Bittner T, Jung CK, Burgold S, Page RM, Mitteregger G, Haass C, LaFerla FM, Kretzschmar H, Herms J (2010) Microglial CX3CR1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nat Neurosci 13:411-413.
15. Harrison JK, Jiang Y, Chen S, Xia Y, Maciejewski D, McNamara RK, Streit WJ, Salafranca MN, Adhikari S, Thompson DA, Botti P, Bacon KB, Feng L (1998) Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci U S A 95:10896-10901.
16. Imai F, Suzuki H, Oda J, Ninomiya T, Ono K, Sano H, Sawada M (2007) Neuroprotective effect of exogenous microglia in global brain ischemia. J Cereb Blood Flow Metab 27:488-500.
17. Johansson B, Halldner L, Dunwiddie TV, Masino SA, Poelchen W, Giménez- Llort L, Escorihuela RM, Fernández-Teruel A, Wiesenfeld-Hallin Z, Xu XJ, Hårdemark A, Betsholtz C, Herlenius E, Fredholm BB (2001) Hyperalgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor. Proc Natl Acad Sci U S A 98:9407-9412.
18. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20:4106-4114.
19. Labuzek K, Liber S, Gabryel B, Adamczyk J, Okopień B (2010) Metformin increases phagocytosis and acidifies lysosomal/endosomal compartments in AMPK-dependent manner in rat primary microglia. Naunyn Schmied Arch Pharmacol 381:171-186.
20. Lai AY, Todd KG (2008) Differential regulation of trophic and proinflammatory microglial effectors is dependent on severity of neuronal injury. Glia 56:259-270.
21. Lalancette-Hébert M, Gowing G, Simard A, Weng YC, Kriz J (2007) Selective Ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 27:2596-2605.
22. Lambertsen KL, Clausen BH, Babcock AA, Gregersen R, Fenger C, Nielsen HH, Haugaard LS, Wirenfeldt M, Nielsen M, Dagnaes-Hansen F, Bluethmann H, Faergeman NJ, Meldgaard M, Deierborg T, Finsen B (2009) Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 29:1319-1330.
23. Lauro C, Cipriani R, Catalano M, Trettel F, Chece G, Brusadin V, Antonilli L, van Rooijen N, Eusebi F, Fredholm BB, Limatola C (2010) AdenosineA1 receptors and microglial cells mediate CX3CL1-induced protection of hippocampal neurons against Glu-induced death. Neuropsychopharmacology 35:1550-1559.
24. Lauro C, Di Angelantonio S, Cipriani R, Sobrero F, Antonilli L, Brusadin V, Ragozzino D, Limatola C (2008) Activity of adenosine receptor type 1 is required for CX3CL1-mediated neuroprotection and neuromodulation in hippocampal neurons. J Immunol 180:7590-7596.
25. Lee S, Varvel NH, Konerth ME, Xu G, Cardona AE, Ransohoff RM, Lamb BT (2010) CX3CR1 deficiency alters microglia activation and reduces betaamyloid deposition in two Alzheimer's disease mouse models. Am J Pathol 177:2549-2562.
26. Limatola C, Lauro C, Catalano M, Ciotti MT, Bertollini C, Di Angelantonio S, Ragozzino D, Eusebi F (2005) Chemokine CX3CL1 protects rat hippocampal neurons against glutamate-mediated excitotoxicity. J Neuroimmunol 166:19-28.
27. Liu Z, Condello C, Schain A, Harb R, Grutzendler J (2010) CX3CR1 in microglia regulates brain amyloid deposition through selective protofibrillar amyloid-β phagocytosis. J Neurosci 30:17091-17101.
28. Lyons A, Lynch AM, Downer EJ, Hanley R, O'Sullivan JB, Smith A, Lynch MA (2009) Fractalkine-induced activation of the phosphatidylinositol-3 kinase pathway attenuates microglial activation in vivo and in vitro. J Neurochem 110:1547-1556.
29. Mizuno T, Kawanokuchi J, Numata K, Suzumura A (2003) Production and neuroprotective functions of Fractalkine in the central nervous system. Brain Res 979:65-70.
30. Nakamura M, Nakakimura K, Matsumoto M, Sakabe T (2002) Rapid tolerance to focal cerebral ischemia in rats is attenuated by Adenosine A1 receptor antagonist. J Cereb Blood Flow Metab 22:161-170.
31. Namura S, Zhu J, Fink K, Endres M, Srinivasan A, Tomaselli KJ, Yuan J, Moskowitz MA (1998) Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J Neurosci 18:3659-3668.
32. Narantuya D, Nagai A, Sheikh AM, Masuda J, Kobayashi S, Yamaguchi S, Kim SU (2010) Human microglia transplanted in rat focal ischemia brain induce neuroprotection and behavioral improvement. PLoS One 5:e11746.
33. Neher JJ, Neniskyte U, Zhao JW, Bal-Price A, Tolkovsky AM, Brown GC (2011) Inhibition of microglial phagocytosis is sufficient to prevent inflammatory neuronal death. J Immunol 186:4973-4983.
34. Noda M, Doi Y, Liang J, Kawanokuchi J, Sonobe Y, Takeuchi H, Mizuno T, Suzumura A (2011) Fractalkine attenuates excite-neurotoxicity via microglia clearance of damaged neurons and antioxidant enzyme Heme Oxigenase-1 expression. J Biol Chem 286:2308-2319.
35. Olsson T, Cronberg T, Rytter A, Asztély F, Fredholm BB, Smith ML, Wieloch T (2004) Effects of adenosine A1 receptor gene deletion in neuronal damage following global cerebral ischemia in mouse in vivo and in vitro. Eur J Neurosci 20:1197-1204.
36. Pabon MM, Bachstetter AD, Hudson CE, Gemma C, Bickford PC (2011) CX3CL1 reduces neurotoxicity and microglial activation in a rat model of Parkinson's disease. J Neuroinflammation 8:9.
37. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. San Diego: Academic.
38. Pearson T, Damian K, Lynas RE, Frenguelli BG (2006) Sustained elevation of extracellular adenosine and activation of A1 receptors underline the post-ischemic inhibition of neuronal function in rat hippocampus in vitro. J Neurochem 97:1357-1368.
39. Phillis JW (1995) The effects of selective A 1 and A 2a adenosine receptor antagonists on cerebral ischemic injury in the gerbil. Brain Res 705:79-84.
40. Sood R, Yang Y, Taheri S, Candelario-Jalil E, Estrada EY, Walker EJ, Thompson J, Rosenberg GA (2009) Increased apparent diffusion coefficients on MRI linked with matrix metalloproteinases and edema in white matter after bilateral carotid artery occlusion in rats. J Cereb Blood Flow Metab 29:308-316.
41. Soriano SG, Amaravadi LS, Wang YF, Zhou H, Yu GX, Tonra JR, Fairchild- Huntress V, Fang Q, Dunmore JH, Huszar D, Pan Y (2002) Mice deficient in fractalkine are less susceptible to cerebral ischemia-reperfusion injury. J Neuroimmunol 125:59-65.
42. Storini C, Bergamaschini L, Gesuete R, Rossi E, Maiocchi D, De Simoni MG (2006) Selective inhibition of plasma kallikrein protects brain from reperfusion injury. J Pharmacol Exp Ther 318:849-854.
43. Tarozzo G, Campanella M, Ghiani M, Bulfone A, Beltramo M (2002) Expression of fractalkine and its receptor, CX3CR1, in response to ischaemiareperfusion brain injury in the rat. Eur J Neurosci 15:1663-1668.
44. Villa P, Triulzi S, Cavalieri B, Di Bitondo R, Bertini R, Barbera S, Bigini P, Mennini T, Gelosa P, Tremoli E, Sironi L, Ghezzi P (2007) The interleukin-8 (IL(/CXCL8) receptor inhibitor reparixin improves neurological deficits and reduces long-term inflammation in permanent and transient cerebral ischemia in rats. Mol Med 13:125-133.
45. Von Lubitz DK, Beenhakker M, Lin RC, Carter MF, Paul IA, Bischofberger N, Jacobson KA (1996) Reduction of postischemic brain damage and memory deficits following treatment with the selective adenosine A1 receptor agonist. Eur J Pharmacol 302:43-48.
46. Wang Q, Xiong L, Chen S, Liu Y, Zhu X (2005) Rapid tolerance to focal cerebral ischemia in rats is induced by preconditioning with electroacupuncture: window of protection and the role of adenosine. Neurosci Lett 381:158-162.
47. Yoshida M, Nakakimura K, Cui YJ, Matsumoto M, Sakabe T (2004) Adenosine A(1) receptor antagonist and mitochondrial ATP-sensitive potassium channel blocker attenuate the tolerance to focal cerebral ischemia in rats. J Cereb Blood Flow Metab 24:771-779.
48. Yrjänheikki J, Keinänen R, Pellikka M, Hökfelt T, Koistinaho J (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci U S A 95:15769-15774.
49. Zhu J, Zhou Z, Liu Y, Zheng J (2009) Fractalkine and CX3CR1 are involved in the migration of intravenously grafted human bone marrow stromal cells toward ischemic brain lesion in rats. Brain Res 1287:173-183.
50. Zujovic V, Benavides J, Vigé X, Carter C, Taupin V (2000) Fractalkine modulates TNF-α secretion and neurotoxicity induced by microglial activation. Glia 29:305-315.