Astrocytes are primed by chronic neurodegeneration to produce exaggerated chemokine and cell infiltration responses to acute stimulation with the cytokines IL-1β and TNF-α

Journal of Neuroscience

Volumn 35, Issue 22, 2015, Pages 8411-8422

  Hennessy, Edel ^a   Griffin, Eádaoin W ^a   Cunningham, Colm ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Astrocyte; Chemokine; Cytokine; Microglia; Neurodegeneration; Neuroinflammation

Indexed keywords

CD3 ANTIGEN; CD68 ANTIGEN; CHEMOKINE; COMPLEMENTARY DNA; CXCL1 CHEMOKINE; CYTOKINE; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1BETA; MEMBRANE PROTEIN; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PENTRAXIN 3; RANTES; STEAP4 PROTEIN; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL ACTIVATION; CELL INFILTRATION; CELL PRIMING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; LYMPHOCYTIC INFILTRATION; MACROPHAGE MIGRATION; MICROGLIA; MONOCYTE; MOUSE; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS REGULATION; T LYMPHOCYTE; ANIMAL; C57BL MOUSE; CHRONIC DISEASE; DISEASE MODEL; DRUG EFFECTS; HIPPOCAMPUS; METABOLISM; PATHOLOGY; PRION DISEASES;

ANIMALS; ASTROCYTES; CHEMOKINES; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; FEMALE; HIPPOCAMPUS; INTERLEUKIN-1BETA; MICE; MICE, INBRED C57BL; MONOCYTES; NEUTROPHIL INFILTRATION; PRION DISEASES; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84930435742     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2745-14.2015     Document Type: Article

References (41)

1. An Y, Chen Q, Quan N (2011) Interleukin-1 exerts distinct actions on different cell types of the brain in vitro. J Inflamm Res 2011:11–20. Medline
2. Andersson PB, Perry VH, Gordon S (1992) Intracerebral injection of proinflammatory cytokines or leukocyte chemotaxins induces minimal myelomonocytic cell recruitment to the parenchyma of the central nervous system. J Exp Med 176:255–259. CrossRef Medline
3. Blond D, Campbell SJ, Butchart AG, Perry VH, Anthony DC (2002) Differential induction of interleukin-1beta and tumour necrosis factor-alpha may account for specific patterns of leukocyte recruitment in the brain. Brain Res 958:89–99. CrossRef Medline
4. Brambilla R, Bracchi-Ricard V, Hu WH, Frydel B, Bramwell A, Karmally S, Green EJ, Bethea JR (2005) Inhibition of astroglial nuclear factor kappaB reduces inflammation and improves functional recovery after spinal cord injury. J Exp Med 202:145–156. CrossRef Medline
5. Brambilla R, Morton PD, Ashbaugh JJ, Karmally S, Lambertsen KL, Bethea JR (2014) Astrocytes play a key role in EAE pathophysiology by orchestrating in the CNS the inflammatory response of resident and peripheral immune cells and by suppressing remyelination. Glia 62:452–467. CrossRef Medline
6. Bruhl H, Cihak J, Plachý J, Kunz-Schughart L, Niedermeier M, Denzel A, Rodriguez Gomez M, Talke Y, Luckow B, Stangassinger M, Mack M (2007) Targeting of Gr-1+, CCR2+ monocytes in collagen-induced arthritis. Arthritis Rheum 56:2975–2985. CrossRef Medline
7. Campbell SJ, Wilcockson DC, Butchart AG, Perry VH, Anthony DC (2002) Altered chemokine expression in the spinal cord and brain contributes to differential interleukin-1beta-induced neutrophil recruitment. J Neurochem 83:432–441. CrossRef Medline
8. Campbell SJ, Perry VH, Pitossi FJ, Butchart AG, Chertoff M, Waters S, Dempster R, Anthony DC (2005) Central nervous system injury triggers hepaticCCandCXCchemokine expression that is associated with leukocyte mobilization and recruitment to both the central nervous system and the liver. Am J Pathol 166:1487–1497. CrossRef Medline
9. Chen J, Buchanan JB, Sparkman NL, Godbout JP, Freund GG, Johnson RW (2008) Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system. Brain Behav Immun 22:301–311. CrossRef Medline
10. Choi K, Ni L, Jonakait GM (2011) Fas ligation and tumor necrosis factor alpha activation of murine astrocytes promote heat shock factor-1 activation and heat shock protein expression leading to chemokine induction and cell survival. J Neurochem 116:438–448. CrossRef Medline
11. Chung IY, Benveniste EN (1990) Tumor necrosis factor-alpha production by astrocytes. Induction by lipopolysaccharide, IFN-gamma, and IL-1 beta. J Immunol 144:2999–3007. Medline
12. Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH (2005) Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 25:9275–9284. CrossRef Medline
13. Fouillet A, Mawson J, Suliman O, Sharrack B, Romero IA, Woodroofe MN (2012) CCL2 binding is CCR2 independent in primary adult human astrocytes. Brain Res 1437:115–126. CrossRef Medline
14. Godbout JP, Chen J, Abraham J, Richwine AF, Berg BM, Kelley KW, Johnson RW (2005) Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J 19:1329–1331. Medline
15. Gómez-Nicola D, Fransen NL, Suzzi S, Perry VH (2013) Regulation of microglial proliferation during chronic neurodegeneration. J Neurosci 33: 2481–2493. CrossRef Medline
16. Henn A, Kirner S, Leist M (2011) TLR2 hypersensitivity of astrocytes as functional consequence of previous inflammatory episodes. J Immunol 186:3237–3247. CrossRef Medline
17. Hughes MM, Field RH, Perry VH, Murray CL, Cunningham C (2010) Microglia in the degenerating brain are capable of phagocytosis of beads and of apoptotic cells, but do not efficiently remove PrPSc, even upon LPS stimulation. Glia 58:2017–2030. CrossRef Medline
18. Jing T, Wu L, Borgmann K, Surendran S, Ghorpade A, Liu J, Xiong H (2010) Soluble factors from IL-1beta-stimulated astrocytes activate NR1a/NR2B receptors: implications for HIV-1-induced neurodegeneration. Biochem Biophys Res Commun 402:241–246. CrossRef Medline
19. Khorooshi R, Babcock AA, Owens T (2008) NF-kappaB-driven STAT2 and CCL2 expression in astrocytes in response to brain injury. J Immunol 181:7284–7291. CrossRef Medline
20. Kim JM, Oh YK, Lee JH, Im DY, Kim YJ, Youn J, Lee CH, Son H, Lee YS, Park JY, Choi IH (2005) Induction of proinflammatory mediators requires activation of the TRAF, NIK, IKK and NF-kappaB signal transduction pathway in astrocytes infected with Escherichia coli. Clin Exp Immunol 140:450–460. CrossRef Medline
21. Lee YH, Kim SH, Kim Y, Lim Y, Ha K, Shin SY (2012) Inhibitory effect of the antidepressant imipramine on NF-kappaB-dependent CXCL1 expression in TNFalpha-exposed astrocytes. Int Immunopharmacol 12:547–555. CrossRef Medline
22. McColl BW, Rothwell NJ, Allan SM (2008) Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J Neurosci 28:9451–9462. CrossRef Medline
23. McKimmie CS, Graham GJ (2010) Astrocytes modulate the chemokine network in a pathogen-specific manner. Biochem Biophys Res Commun 394:1006–1011. CrossRef Medline
24. Moreno M, Bannerman P, Ma J, Guo F, Miers L, Soulika AM, Pleasure D (2014) Conditional ablation of astroglial CCL2 suppresses CNS accumulation ofM1macrophages and preserves axons in mice withMOGpeptide EAE. J Neurosci 34:8175–8185. CrossRef Medline
25. Morganti JM, Jopson TD, Liu S, Riparip LK, Guandique CK, Gupta N, Ferguson AR, Rosi S (2015) CCR2 antagonism alters brain macrophage polarization and ameliorates cognitive dysfunction induced by traumatic brain injury. J Neurosci 35:748–760. CrossRef Medline
26. Murray C, Sanderson DJ, Barkus C, Deacon RM, Rawlins JN, Bannerman DM, Cunningham C (2012) Systemic inflammation induces acute working memory deficits in the primed brain: relevance for delirium. Neurobiol Aging 33:603–616.e3. CrossRef Medline
27. Pace JL, Russell SW, Torres BA, Johnson HM, Gray PW (1983) Recombinant mouse gamma interferon induces the priming step in macrophage activation for tumor cell killing. J Immunol 130:2011–2013. Medline
28. Pott Godoy MC, Tarelli R, Ferrari CC, Sarchi MI, Pitossi FJ (2008) Central and systemic IL-1 exacerbates neurodegeneration and motor symptoms in a model of Parkinson’s disease. Brain 131:1880–1894. CrossRef Medline
29. Ritter L, Davidson L, Henry M, Davis-Gorman G, Morrison H, Frye JB, Cohen Z, Chandler S, McDonagh P, Funk JL (2011) Exaggerated neutrophil-mediated reperfusion injury after ischemic stroke in a rodent model of type 2 diabetes. Microcirculation 18:552–561. CrossRef Medline
30. Schnell L, Fearn S, Schwab ME, Perry VH, Anthony DC (1999) Cytokineinduced acute inflammation in the brain and spinal cord. J Neuropathol Exp Neurol 58:245–254. CrossRef Medline
31. Semple BD, Bye N, Ziebell JM, Morganti-Kossmann MC (2010) Deficiency of the chemokine receptor CXCR2 attenuates neutrophil infiltration and cortical damage following closed head injury. Neurobiol Dis 40:394–403. CrossRef Medline
32. Shultz SR, Bao F, Weaver LC, Cain DP, Brown A (2013) Treatment with an anti-CD11 d integrin antibody reduces neuroinflammation and improves outcome in a rat model of repeated concussion. J Neuroinflammation 10:26. CrossRef Medline
33. Sly LM, Krzesicki RF, Brashler JR, Buhl AE, McKinley DD, Carter DB, Chin JE (2001) Endogenous brain cytokine mRNA and inflammatory responses to lipopolysaccharide are elevated in the Tg2576 transgenic mouse model of Alzheimer’s disease. Brain Res Bull 56:581–588. CrossRef Medline
34. Stamatovic SM, Dimitrijevic OB, Keep RF, Andjelkovic AV (2006) Protein kinase Calpha-RhoA cross-talk in CCL2-induced alterations in brain endothelial permeability. J Biol Chem 281:8379–8388. CrossRef Medline
35. Thompson WL, Van Eldik LJ (2009) Inflammatory cytokines stimulate the chemokines CCL2/MCP-1 and CCL7/MCP-3 through NFkB and MAPK dependent pathways in rat astrocytes [corrected]. Brain Res 1287:47–57. CrossRef Medline
36. Thornton P, McColl BW, Greenhalgh A, Denes A, Allan SM, Rothwell NJ (2010) Platelet interleukin-1alpha drives cerebrovascular inflammation. Blood 115:3632–3639. CrossRef Medline
37. Wang Y, Luo W, Reiser G (2007) The role of calcium in protease-activated receptor-induced secretion of chemokine GRO/CINC-1 in rat brain astrocytes. J Neurochem 103:814–819. CrossRef Medline
38. Yao Y, Tsirka SE (2011) Truncation of monocyte chemoattractant protein 1 by plasmin promotes blood-brain barrier disruption. J Cell Sci 124:1486–1495. CrossRef Medline
39. Yona S, Kim KW, Wolf Y, Mildner A, Varol D, Breker M, Strauss-Ayali D, Viukov S, Guilliams M, Misharin A, Hume DA, Perlman H, Malissen B, Zelzer E, Jung S (2013) Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38: 79–91. CrossRef Medline
40. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG, Barres BA (2012) Genomic analysis of reactive astrogliosis. J Neurosci 32:6391–6410. CrossRef Medline
41. Zhang ZJ, Cao DL, Zhang X, Ji RR, Gao YJ (2013) Chemokine contribution to neuropathic pain: respective induction of CXCL1 and CXCR2 in spinal cord astrocytes and neurons. Pain 154:2185–2197. CrossRef Medline