Modulation of post-stroke degenerative and regenerative processes and subacute protection by site-targeted inhibition of the alternative pathway of complement

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Alawieh, Ali ^a   Elvington, Andrew ^a   Zhu, Hong ^b   Yu, Jin ^b   Kindy, Mark S ^b,c   Atkinson, Carl ^a   Tomlinson, Stephen ^a,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

Complement inhibition; Ischemic stroke; Neuroinflammation; Neuroprotection

Indexed keywords

CIPROFLOXACIN; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C5 INHIBITOR; COMPLEMENT COMPONENT C5A; COMPLEMENT INHIBITOR; CR2 CRRY; CR2 FH; UNCLASSIFIED DRUG; VASCULOTROPIN; COMPLEMENT COMPONENT C3D RECEPTOR;

ACUTE PHASE RESPONSE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BRAIN INFARCTION SIZE; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT INHIBITION; CONTROLLED STUDY; DOWN REGULATION; DRUG SELECTIVITY; DRUG TARGETING; GENE EXPRESSION REGULATION; IMMUNE RESPONSE; LEUKOCYTE ACTIVATION; LOCOMOTION; MACROPHAGE ACTIVATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PASSIVE AVOIDANCE; PROTEIN EXPRESSION; PROTEIN TARGETING; SINGLE DRUG DOSE; SPATIAL LEARNING; SUBACUTE PHASE RESPONSE; TRANSIENT ISCHEMIC ATTACK; UPREGULATION; ANIMAL; C57BL MOUSE; DEFICIENCY; GENE TARGETING; GENETICS; KNOCKOUT MOUSE; METABOLISM; MICROGLIA; PHYSIOLOGY; PROCEDURES; REGENERATION; STROKE;

ANIMALS; COMPLEMENT PATHWAY, ALTERNATIVE; GENE TARGETING; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROGLIA; RECEPTORS, COMPLEMENT 3D; REGENERATION; STROKE;

EID: 84951994142     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0464-8     Document Type: Article

References (40)

1. Komotar RJ, Kim GH, Otten ML, Hassid B, Mocco J, Sughrue ME, et al. The role of complement in stroke therapy. Adv Exp Med Biol. 2008;632:23-33.
2. Gorsuch WB, Chrysanthou E, Schwaeble WJ, Stahl GL. The complement system in ischemia-reperfusion injuries. Immunobiology. 2012;217:1026-33.
3. Alawieh A, Elvington A, Tomlinson S. Complement in the homeostatic and ischemic brain. Front Immunol. 2015;6:417.
4. Elvington A, Atkinson C, Zhu H, Yu J, Takahashi K, Stahl GL, et al. The alternative complement pathway propagates inflammation and injury in murine ischemic stroke. J Immunol. 2012;189:4640-7.
5. Orsini F, Villa P, Parrella S, Zangari R, Zanier ER, Gesuete R, et al. Targeting mannose-binding lectin confers long-lasting protection with a surprisingly wide therapeutic window in cerebral ischemia. Circulation. 2012;126:1484-94.
6. Cervera A, Planas AM, Justicia C, Urra X, Jensenius JC, Torres F, et al. Genetically-defined deficiency of mannose-binding lectin is associated with protection after experimental stroke in mice and outcome in human stroke. PLoS One. 2010;5:e8433.
7. Morrison H, Frye J, Davis-Gorman G, Funk J, McDonagh P, Stahl G, et al. The contribution of mannose binding lectin to reperfusion injury after ischemic stroke. Curr Neurovasc Res. 2011;8:52-63.
8. Gesuete R, Storini C, Fantin A, Stravalaci M, Zanier ER, Orsini F, et al. Recombinant C1 inhibitor in brain ischemic injury. Ann Neurol. 2009;66:332-42.
9. Brennan FH, Anderson AJ, Taylor SM, Woodruff TM, Ruitenberg MJ. Complement activation in the injured central nervous system. Another dual-edged sword? J Neuroinflammation. 2012;9:137.
10. Gasque P, Neal JW, Singhrao SK, McGreal EP, Dean YD, Van BJ, et al. Roles of the complement system in human neurodegenerative disorders: pro-inflammatory and tissue remodeling activities. Mol Neurobiol. 2002;25:1-17.
11. Ducruet AF, Sosunov SA, Zacharia BE, Gorski J, Yeh ML, Derosa P, et al. The neuroprotective effect of genetic mannose-binding lectin deficiency is not sustained in the sub-acute phase of stroke. Trans Stroke Res. 2011;2:588-99.
12. Mocco J, Mack WJ, Ducruet AF, Sosunov SA, Sughrue ME, Hassid BG, et al. Complement component C3 mediates inflammatory injury following focal cerebral ischemia. Circ Res. 2006;99:209-17.
13. Atkinson C, Zhu H, Qiao F, Varela JC, Yu J, Song H, et al. Complement-dependent P-selectin expression and injury following ischemic stroke. J Immunol. 2006;177:7266-74.
14. Rahpeymai Y, Hietala MA, Wilhelmsson U, Fotheringham A, Davies I, Nilsson AK, et al. Complement: a novel factor in basal and ischemia-induced neurogenesis. EMBO J. 2006;25:1364-74.
15. Huang Y, Qiao F, Atkinson C, Holers VM, Tomlinson S. A novel targeted inhibitor of the alternative pathway of complement and its therapeutic application in ischemia/reperfusion injury. J Immunol. 2008;181:8068-76.
16. Atkinson C, Song H, Lu B, Qiao F, Burns TA, Holers VM, et al. Targeted complement inhibition by C3d recognition ameliorates tissue injury without apparent increase in susceptibility to infection. J Clin Invest. 2005;115:2444-53.
17. Quigg RA, Kozono Y, Berthiaume D, Lim A, Salant J, Weinfeld A, et al. Blockade of antibody-induced glomerulonephritis with Crry-Ig, a soluble murine complement inhibitor. J Immunol. 1998;160:4553-60.
18. Hata R, Mies G, Wiessner C, Fritze K, Hesselbarth D, Brinker G, et al. A reproducible model of middle cerebral artery occlusion in mice. Hemodynamic, biochemical, and magnetic resonance imaging. J Cereb Blood Flow Metab. 1998;18:367-75.
19. Patil SS, Sunyer B, Hoger H, Lubec G. Evaluation of spatial memory of C57BL/6 J and CD1 mice in the Barnes maze, the Multiple T-maze and in the Morris water maze. Behav Brain Res. 2009;198:58-68.
20. Bederson JB, Pitts LH, Germano SM, Nishimura MC, Davis RL, Bartkowski HM. Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke. 1986;17:1304-8.
21. Geiss GK, Bumgarner RE, Birditt B, Dahl T, Dowidar N, Dunaway DL, et al. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol. 2008;26:317-25.
22. Zhang RL, Zhang ZG, Zhang L, Chopp M. Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience. 2001;105:33-41.
23. Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, et al. Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the post-stroke striatum. Stem Cells. 2010;28:545-54.
24. Ducruet AF, Zacharia BE, Sosunov SA, Gigante PR, Yeh ML, Gorski JW, et al. Complement inhibition promotes endogenous neurogenesis and sustained anti-inflammatory neuroprotection following reperfused stroke. PLoS One. 2012;7:e38664.
25. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci. 2002;99:11946-50.
26. Georg Kuhn H, Blomgren K. Developmental dysregulation of adult neurogenesis. Eur J Neurosci. 2011;33:1115-22.
27. Langhorne P, Stott DJ, Robertson L, MacDonald J, Jones L, McAlpine C, et al. Medical complications after stroke: a multicenter study. Stroke. 2000;31:1223-9.
28. Grau AJ, Buggle F, Schnitzler P, Spiel M, Lichy C, Hacke W. Fever and infection early after ischemic stroke. J Neurol Sci. 1999;171:115-20.
29. Meisel C, Prass K, Braun J, Victorov I, Wolf T, Megow D, et al. Preventive antibacterial treatment improves the general medical and neurological outcome in a mouse model of stroke. Stroke. 2004;35:2-6.
30. Mukherjee P, Thomas S, Pasinetti GM. Complement anaphylatoxin C5a neuroprotects through regulation of glutamate receptor subunit 2 in vitro and in vivo. J Neuroinflammation. 2008;5:5.
31. Osaka H, Mukherjee P, Aisen PS, Pasinetti GM. Complement-derived anaphylatoxin C5a protects against glutamate-mediated neurotoxicity. J Cell Biochem. 1999;73:303-11.
32. van Beek J, Nicole O, Ali C, Ischenko A, MacKenzie ET, Buisson A, et al. Complement anaphylatoxin C3a is selectively protective against NMDA-induced neuronal cell death. Neuroreport. 2001;12:289-93.
33. Jarlestedt K, Rousset CI, Stahlberg A, Sourkova H, Atkins AL, Thornton C, et al. Receptor for complement peptide C3a. a therapeutic target for neonatal hypoxic-ischemic brain injury. FASEB J. 2013;27:3797-804.
34. Ten VS, Yao J, Ratner V, Sosunov S, Fraser DA, Botto M, et al. Complement component c1q mediates mitochondria-driven oxidative stress in neonatal hypoxic-ischemic brain injury. J Neurosci. 2010;30:2077-87.
35. Fishelson Z, Attali G, Mevorach D. Complement and apoptosis. Mol Immunol. 2001;38:207-19.
36. Shinjyo N, Stahlberg A, Dragunow M, Pekny M, Pekna M. Complement-derived anaphylatoxin C3a regulates in vitro differentiation and migration of neural progenitor cells. Stem Cells. 2009;27:2824-32.
37. Litvack ML, Palaniyar N. Review. Soluble innate immune pattern-recognition proteins for clearing dying cells and cellular components: implications on exacerbating or resolving inflammation. Innate Immun. 2010;16:191-200.
38. Hoarau JJ, Krejbich-Trotot P, Jaffar-Bandjee MC, Das T, Thon-Hon GV, Kumar S, et al. Activation and control of CNS innate immune responses in health and diseases: a balancing act finely tuned by neuroimmune regulators (NIReg). CNS Neurol Disord Drug Targets. 2011;10:25-43.
39. Nozaki M, Raisler BJ, Sakurai E, Sarma JV, Barnum SR, Lambris JD, et al. Drusen complement components C3a and C5a promote choroidal neovascularization. Proc Natl Acad Sci. 2006;103:2328-33.
40. Moriyama M, Fukuhara T, Britschgi M, He Y, Narasimhan R, Villeda S, et al. Complement receptor 2 is expressed in neural progenitor cells and regulates adult hippocampal neurogenesis. J Neurosci. 2011;31:3981-9.