IL-10 deficiency exacerbates the brain inflammatory response to permanent ischemia without preventing resolution of the lesion

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 12, 2013, Pages 1955-1966

  Pérez De Puig, Isabel ^a,b   Miró, Francesc ^b   Salas Perdomo, Angélica ^a,b   Bonfill Teixidor, Ester ^a,b   Ferrer Ferrer, Maura ^b   Márquez Kisinousky, Leonardo ^a   Planas, Anna M ^a,b  

^a INST D INVESTIGACIONS B   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

Cytokines; IL 10; Inflammation; Microglia; Myeloid cells; Stroke

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CYCLOOXYGENASE 2; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; FRACTALKINE; GELATINASE B; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; SOMATOMEDIN C; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL MATURATION; COLITIS; CONTROLLED STUDY; DISEASE EXACERBATION; ENCEPHALITIS; GENE EXPRESSION; IMMUNOMODULATION; KNOCKOUT MOUSE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MORTALITY; MOUSE; NEUROIMAGING; NEUROLOGIC DISEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; WILD TYPE;

ANIMALS; BRAIN; BRAIN EDEMA; GENE KNOCKOUT TECHNIQUES; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; INTERLEUKIN-10; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-10; UP-REGULATION;

EID: 84889095882     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.155     Document Type: Article

References (40)

1. Lee JW, Bae SH, Jeong JW, Kim SH, Kim KW. Hypoxia-inducible factor (HIF-1)alpha: its protein stability and biological functions. Exp Mol Med 2004; 36: 1-12.
2. Geiger K, Leiherer A, Muendlein A, Stark N, Geller-Rhomberg S, Saely CH et al. Identification of hypoxia-induced genes in human SGBS adipocytes by microarray analysis. PLoS ONE 2011; 6: e26465.
3. Li F, Wang L, Li JW, Gong M, He L, Feng R et al. Hypoxia induced amoeboid microglial cell activation in postnatal rat brain is mediated by ATP receptor P2×4. BMC Neurosci 2011; 12: 111.
4. Feinman R, Deitch EA, Watkins AC, Abungu B, Colorado I, Kannan KB et al. HIF-1 mediates pathogenic inflammatory responses to intestinal ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 2010; 299: G833-G843.
5. Kim SY, Choi YJ, Joung SM, Lee BH, Jung YS, Lee JY. Hypoxic stress up-regulates the expression of Toll-like receptor 4 in macrophages via hypoxia-inducible factor. Immunology 2010; 129: 516-524.
6. Tafani M, Schito L, Pellegrini L, Villanova L, Marfe G, Anwar T et al. Hypoxiaincreased RAGE and P2×7R expression regulates tumor cell invasion through phosphorylation of Erk1/2 and Akt and nuclear translocation of NF-{kappa}B. Carcinogenesis 2011; 32: 1167-1175.
7. Johnson GB, Brunn GJ, Platt JL. Activation of mammalian Toll-like receptors by endogenous agonists. Crit Rev Immunol 2003; 23: 15-44. (Pubitemid 36875472)
8. Gorina R, Font-Nieves M, Marquez-Kisinousky L, Santalucia T, Planas AM. Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkB signaling, MAPK and Jak1/Stat1 pathways. Glia 2011; 59: 242-255.
9. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 2007; 8: 57-69. (Pubitemid 46011999)
10. Amantea D, Nappi G, Bernardi G, Bagetta G, Corasaniti MT. Post-ischemic brain damage: pathophysiology and role of inflammatory mediators. FEBS J 2009; 276: 13-26.
11. Serhan CN, Savill J. Resolution of inflammation: the beginning programs the end. Nat Immunol 2005; 6: 1191-1197. (Pubitemid 43045627)
12. de Bilbao F, Arsenijevic D, Moll T, Garcia-Gabay I, Vallet P, Langhans W et al. In vivo over-expression of interleukin-10 increases resistance to focal brain ischemia in mice. J Neurochem 2009; 110: 12-22.
13. Ooboshi H, Ibayashi S, Shichita T, Kumai Y, Takada J, Ago T et al. Postischemic gene transfer of interleukin-10 protects against both focal and global brain ischemia. Circulation 2005; 111: 913-919. (Pubitemid 40279894)
14. Grilli M, Barbieri I, Basudev H, Brusa R, Casati C, Lozza G et al. Interleukin-10 modulates neuronal threshold of vulnerability to ischaemic damage. Eur J Neurosci 2000; 12: 2265-2272. (Pubitemid 30497024)
15. Vila N, Castillo J, Dávalos A, Esteve A, Planas AM, Chamorro A. Levels of anti-inflammatory cytokines and neurological worsening in acute ischemic stroke. Stroke 2003; 34: 671-675. (Pubitemid 36307391)
16. Kullberg MC, Ward JM, Gorelick PL, Caspar P, Hieny S, Cheever A et al. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12-and gamma interferon-dependent mechanism. Infect Immun 1998; 66: 5157-5166. (Pubitemid 29044604)
17. Bouet V, Boulouard M, Toutain J, Divoux D, Bernaudin M, Schumann-Bard P et al. The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nature Prot 2009; 4: 1560-1564.
18. Saura J, Tusell JM, Serratosa J. High-yield isolation of murine microglia by mild trypsinization. Glia 2003; 44: 183-189. (Pubitemid 37484470)
19. Li HL, Kostulas N, Huang YM, Xiao BG, van der Meide P, Kostulas V et al. IL-17 and IFN-gamma mRNA expression is increased in the brain and systemically after permanent middle cerebral artery occlusion in the rat. J Neuroimmunol 2001; 116: 5-14. (Pubitemid 32322634)
20. McColl BW, Rothwell NJ, Allan SM. Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1-and neutrophil-dependent mechanisms. J Neurosci 2007; 27: 4403-4412. (Pubitemid 46640725)
21. Henrich-Noack P, Baldauf K, Reiser G, Reymann KG. Pattern of time-dependent reduction of histologically determined infarct volume after focal ischaemia in mice. Neurosci Lett 2008; 432: 141-145.
22. Pialat JB, Cho TH, Beuf O, Joye E, Moucharrafie S, Langlois JB et al. MRI monitoring of focal cerebral ischemia in peroxisome proliferator-activated receptor (PPAR)-deficient mice. NMR Biomed 2007; 20: 335-342. (Pubitemid 46824533)
23. Cervera A, Planas AM, Justicia C, Urra X, Jensenius JC, Torres F et al. Geneticallydefined deficiency of mannose-binding lectin is associated with protection after experimental stroke in mice and outcome in human stroke. PLoS ONE 2010; 5: e8433.
24. Lambertsen KL, Biber K, Finsen B. Inflammatory cytokines in experimental and human stroke. J Cereb Blood Flow Metab 2012; 32: 1677-1698.
25. Iwama A, Wang MH, Yamaguchi N, Ohno N, Okano K, Sudo T et al. Terminal differentiation of murine resident peritoneal macrophages is characterized by expression of the STK protein tyrosine kinase, a receptor for macrophage-stimulating protein. Blood 1995; 86: 3394-3403.
26. Koscsó B, Csóka B, Selmeczy Z, Himer L, Pacher P, Virág L et al. Adenosine augments IL-10 production by microglial cells through an A2B adenosine receptor-mediated process. J Immunol 2012; 188: 445-453.
27. Seo DR, Kim SY, Kim KY, Lee HG, Moon JH, Lee JS et al. Cross talk between P2 purinergic receptors modulates extracellular ATP-mediated interleukin-10 production in rat microglial cells. Exp Mol Med 2008; 40: 19-26.
28. Ledeboer A, Brevé JJ, Wierinckx A, van der Jagt S, Bristow AF, Leysen JE et al. Expression and regulation of interleukin-10 and interleukin-10 receptor in rat astroglial and microglial cells. Eur J Neurosci 2002; 16: 1175-1185. (Pubitemid 35340841)
29. Lalancette-Hébert M, Gowing G, Simard A, Weng YC, Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 2007; 27: 2596-2605. (Pubitemid 46393607)
30. Faustino JV, Wang X, Johnson CE, Klibanov A, Derugin N, Wendland MF et al. Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke. J Neurosci 2011; 31: 12992-13001.
31. Harris HE, Raucci A. Alarmin(g) news about danger: workshop on innate danger signals and HMGB1. EMBO Rep 2006; 7: 774-778. (Pubitemid 44275393)
32. Caso JR, Pradillo JM, Hurtado O, Lorenzo P, Moro MA, Lizasoain I. Toll-like receptor 4 is involved in brain damage and inflammation after experimental stroke. Circulation 2007; 115: 1599-1608. (Pubitemid 46648645)
33. Genovese T, Esposito E, Mazzon E, Di Paola R, Caminiti R, Bramanti P et al. Absence of endogenous interleukin-10 enhances secondary inflammatory process after spinal cord compression injury in mice. J Neurochem 2009; 108: 1360-1372.
34. Deckert M, Soltek S, Geginat G, Lütjen S, Montesinos-Rongen M, Hof H et al. Endogenous interleukin-10 is required for prevention of a hyperinflammatory intracerebral immune response in Listeria monocytogenes meningoencephalitis. Infect Immun 2001; 69: 4561-4571. (Pubitemid 32574458)
35. Ransohoff RM, Brown MA. Innate immunity in the central nervous system. J Clin Invest 2012; 122: 1164-1171.
36. Schwartz M. Tissue-repairing' blood-derived macrophages are essential for healing of the injured spinal cord: From skin-activated macrophages to infiltrating blood-derived cells? Brain Behav Immun 2010; 24: 1054-1057.
37. Zoglmeier C, Bauer H, Nörenberg D, Wedekind G, Bittner P, Sandholzer N et al. CpG blocks immunosuppression by myeloid-derived suppressor cells in tumorbearing mice. Clin Cancer Res 2011; 17: 1765-1775.
38. Zhang X, Majlessi L, Deriaud E, Leclerc C, Lo-Man R. Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 2009; 31: 761-771.
39. Liesz A, Suri-Payer E, Veltkamp C, Doerr H, Sommer C, Rivest S et al. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat Med 2009; 15: 192-199.
40. Ertelt JM, Buyukbasaran EZ, Jiang TT, Rowe JH, Xin L, Way SS. B7-1/B7-2 blockade overrides the activation of protective CD8 T cells stimulated in the absence of Foxp3+ regulatory T cells. J Leukoc Biol 2013; 94: 367-376.