Lack of macrophage migration inhibitory factor in mice does not affect hallmarks of the inflammatory/immune response during the first week after stroke

Journal of Neuroinflammation

Volumn 8, Issue , 2011, Pages

  Inácio, Ana R ^a   Bucala, Richard ^b   Deierborg, Tomas ^a  

^a LUND UNIVERSITY   (Sweden)

^b YALE UNIVERSITY   (United States)

Author keywords

Cluster of differentiation 74 (CD74); Cytokines; Glial fibrillary acidic protein (GFAP)galectin 3 (Gal 3) Mac 2; Macrophage migration inhibitory factor (MIF); Transient middle cerebral artery occlusion (tMCAo)

Indexed keywords

CD74 ANTIGEN; CXCL1 CHEMOKINE; CYTOKINE RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; MACROPHAGE MIGRATION INHIBITION FACTOR; MACROPHAGE MIGRATION INHIBITION FACTOR RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AUTACOID; B LYMPHOCYTE ANTIGEN; CHEMOKINE; CYTOKINE; HLA ANTIGEN CLASS 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BIOACCUMULATION; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN LEVEL; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE DURATION; ENCEPHALITIS; HEMISPHERE; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE COUNT; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL; NEUROPATHOLOGY; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SHAM PROCEDURE; SPLEEN WEIGHT; WILD TYPE; ANIMAL; BLOOD; BRAIN; C57BL MOUSE; CEREBRAL ARTERY DISEASE; CYTOLOGY; GENETICS; HISTOLOGY; IMMUNOLOGY; INFLAMMATION; INVARIANT CHAIN; METABOLISM; MOUSE MUTANT; PATHOLOGY; SPLEEN; STROKE;

ANIMALS; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; BRAIN; CHEMOKINES; CYTOKINES; HISTOCOMPATIBILITY ANTIGENS CLASS II; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; INFLAMMATION MEDIATORS; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; SPLEEN; STROKE;

EID: 79959642545     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-8-75     Document Type: Article

References (45)

1. Endres M, Engelhardt B, Koistinaho J, Lindvall O, Meairs S, Mohr JP, Planas A, Rothwell N, Schwaninger M, Schwab ME, Vivien D, Wieloch T, Dirnagl U. Improving outcome after stroke: overcoming the translational roadblock. Cerebrovasc Dis 2008, 25:268-78. 10.1159/000118039, 18292653.
2. Wang Q, Tang XN, Yenari MA. The inflammatory response in stroke. J Neuroimmunol 2007, 184:53-68. 10.1016/j.jneuroim.2006.11.014, 1868538, 17188755.
3. Denes A, Thornton P, Rothwell NJ, Allan SM. Inflammation and brain injury: acute cerebral ischaemia, peripheral and central inflammation. Brain Behav Immun 2010, 24:708-23. 10.1016/j.bbi.2009.09.010, 19770034.
4. Liu T, McDonnell PC, Young PR, White RF, Siren AL, Hallenbeck JM, Barone FC, Feurestein GZ. Interleukin-1 beta mRNA expression in ischemic rat cortex. Stroke 1993, 24:1746-50.
5. Yamasaki Y, Matsuura N, Shozuhara H, Onodera H, Itoyama Y, Kogure K. Interleukin-1 as a pathogenetic mediator of ischemic brain damage in rats. Stroke 1995, 26:676-80.
6. Boutin H, LeFeuvre RA, Horai R, Asano M, Iwakura Y, Rothwell NJ. Role of IL-1 alpha and IL-1 beta in ischemic brain damage. J Neurosci 2001, 21:5528-34.
7. Ruscher K, Johannesson E, Brugiere E, Erickson A, Rickhag M, Wieloch T. Enriched environment reduces apolipoprotein E (ApoE) in reactive astrocytes and attenuates inflammation of the peri-infarct tissue after experimental stroke. J Cereb Blood Flow Metab 2009, 29:1796-805. 10.1038/jcbfm.2009.96, 19623195.
8. 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. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 2009, 29:1319-30. 10.1523/JNEUROSCI.5505-08.2009, 19193879.
9. Tarkowski E, Rosengren L, Blomstrand C, Wikkelso C, Jensen C, Ekholm S, Tarkowski A. Early intrathecal production of interleukin-6 predicts the size of brain lesion in stroke. Stroke 1995, 26:1393-8.
10. Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 2009, 32:638-47. 10.1016/j.tins.2009.08.002, 2787735, 19782411.
11. Nygren J, Wieloch T, Pesic J, Brundin P, Deierborg T. Enriched environment attenuates cell genesis in subventricular zone after focal ischemia in mice and decreases migration of newborn cells to the striatum. Stroke 2006, 37:2824-9. 10.1161/01.STR.0000244769.39952.90, 17008628.
12. Schwartz M, Butovsky O, Bruck W, Hanisch UK. Microglial phenotype: is the commitment reversible?. Trends Neurosci 2006, 29:68-74. 10.1016/j.tins.2005.12.005, 16406093.
13. Lalancette-Hebert M, Gowing G, Simard A, Weng YC, Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 2007, 27:2596-605. 10.1523/JNEUROSCI.5360-06.2007, 17344397.
14. Deierborg T, Roybon L, Inacio AR, Pesic J, Brundin P. Brain injury activates microglia that induce neural stem cell proliferation ex vivo and promote differentiation of neurosphere-derived cells into neurons and oligodendrocytes. Neuroscience 2010, 171:1386-96. 10.1016/j.neuroscience.2010.09.045, 20883748.
15. Liesz A, Suri-Payer E, Veltkamp C, Doerr H, Sommer C, Rivest S, Giese T, Veltkamp R. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat Med 2009, 15:192-9. 10.1038/nm.1927, 19169263.
16. Dirnagl U, Klehmet J, Braun JS, Harms H, Meisel C, Ziemssen T, Prass K, Meisel A. Stroke-induced immunodepression: experimental evidence and clinical relevance. Stroke 2007, 38(2 Suppl):770-3.
17. Prass K, Meisel C, Hoflich C, Braun J, Halle E, Wolf T, Ruscher K, Victorov IV, Priller J, Dirnagl U, Volk HD, Meisel A. Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J Exp Med 2003, 198:725-36. 10.1084/jem.20021098, 2194193, 12939340.
18. Offner H, Subramanian S, Parker SM, Wang C, Afentoulis ME, Lewis A, Vandenbark AA, Hurn PD. Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. J Immunol 2006, 176:6523-31.
19. Calandra T, Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 2003, 3:791-800. 10.1038/nri1200, 14502271.
20. Baugh JA, Chitnis S, Donnelly SC, Monteiro J, Lin X, Plant BJ, Wolfe F, Gregersen PK, Bucala R. A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis. Genes Immun 2002, 3:170-6. 10.1038/sj.gene.6363867, 12070782.
21. Morand EF, Leech M, Bernhagen J. MIF: a new cytokine link between rheumatoid arthritis and atherosclerosis. Nat Rev Drug Discov 2006, 5:399-410. 10.1038/nrd2029, 16628200.
22. Bernhagen J, Calandra T, Mitchell RA, Martin SB, Tracey KJ, Voelter W, Manogue KR, Cerami A, Bucala R. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 1993, 365:756-9. 10.1038/365756a0, 8413654.
23. Hudson JD, Shoaibi MA, Maestro R, Carnero A, Hannon GJ, Beach DH. A proinflammatory cytokine inhibits p53 tumor suppressor activity. J Exp Med 1999, 190:1375-82. 10.1084/jem.190.10.1375, 2195698, 10562313.
24. Mitchell RA, Liao H, Chesney J, Fingerle-Rowson G, Baugh J, David J, Bucala R. Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci USA 2002, 99:345-50. 10.1073/pnas.012511599, 117563, 11756671.
25. Bacher M, Weihe E, Dietzschold B, Meinhardt A, Vedder H, Gemsa D, Bette M. Borna disease virus-induced accumulation of macrophage migration inhibitory factor in rat brain astrocytes is associated with inhibition of macrophage infiltration. Glia 2002, 37:291-306. 10.1002/glia.10013, 11870869.
26. Arjona A, Foellmer HG, Town T, Leng L, McDonald C, Wang T, Wong SJ, Montgomery RR, Fikrig E, Bucala R. Abrogation of macrophage migration inhibitory factor decreases West Nile virus lethality by limiting viral neuroinvasion. J Clin Invest 2007, 117:3059-66. 10.1172/JCI32218, 1994625, 17909632.
27. Kithcart AP, Cox GM, Sielecki T, Short A, Pruitt J, Papenfuss T, Shawler T, Gienapp I, Satoskar AR, Whitacre CC. A small-molecule inhibitor of macrophage migration inhibitory factor for the treatment of inflammatory disease. FASEB J 2010, 24:4459-66. 10.1096/fj.10-162347, 20624927.
28. Wang L, Zis O, Ma G, Shan Z, Zhang X, Wang S, Dai C, Zhao J, Lin Q, Lin S, Song W. Upregulation of macrophage migration inhibitory factor gene expression in stroke. Stroke 2009, 40:973-6. 10.1161/STROKEAHA.108.530535, 19131653.
29. Inacio AR, Ruscher K, Leng L, Bucala R, Deierborg T. Macrophage migration inhibitory factor promotes cell death and aggravates neurologic deficits after experimental stroke. J Cereb Blood Flow Metab 2011, 31:1093-106. 10.1038/jcbfm.2010.194, 21063426.
30. Inacio AR, Ruscher K, Wieloch T. Enriched environment downregulates macrophage migration inhibitory factor and increases parvalbumin in the brain following experimental stroke. Neurobiol Dis 2011, 41:270-8. 10.1016/j.nbd.2010.09.015, 20883785.
31. Nishio Y, Koda M, Hashimoto M, Kamada T, Koshizuka S, Yoshinaga K, Onodera S, Nishihira J, Okawa A, Yamazaki M. Deletion of macrophage migration inhibitory factor attenuates neuronal death and promotes functional recovery after compression-induced spinal cord injury in mice. Acta Neuropathol 2009, 117:321-8. 10.1007/s00401-008-0476-x, 19125256.
32. Sun C, Li H, Leng L, Raizada MK, Bucala R, Sumners C. Macrophage migration inhibitory factor: an intracellular inhibitor of angiotensin II-induced increases in neuronal activity. J Neurosci 2004, 24:9944-52. 10.1523/JNEUROSCI.2856-04.2004, 15525779.
33. Bozza M, Satoskar AR, Lin G, Lu B, Humbles AA, Gerard C, David JR. Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J Exp Med 1999, 189:341-6. 10.1084/jem.189.2.341, 2192995, 9892616.
34. Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA, Bucala R. MIF signal transduction initiated by binding to CD74. J Exp Med 2003, 197:1467-76. 10.1084/jem.20030286, 2193907, 12782713.
35. Henne C, Schwenk F, Koch N, Moller P. Surface expression of the invariant chain (CD74) is independent of concomitant expression of major histocompatibility complex class II antigens. Immunology 1995, 84:177-82. 1415095, 7750992.
36. Ishizaki T, Erickson A, Kuric E, Shamloo M, Hara-Nishimura I, Inacio AR, Wieloch T, Ruscher K. The asparaginyl endopeptidase legumain after experimental stroke. J Cereb Blood Flow Metab 2010, 30:1756-66. 10.1038/jcbfm.2010.39, 20234379.
37. Chapman KZ, Dale VQ, Denes A, Bennett G, Rothwell NJ, Allan SM, McColl BW. A rapid and transient peripheral inflammatory response precedes brain inflammation after experimental stroke. J Cereb Blood Flow Metab 2009, 29:1764-8. 10.1038/jcbfm.2009.113, 19654587.
38. Koebernick H, Grode L, David JR, Rohde W, Rolph MS, Mittrucker HW, Kaufmann SH. Macrophage migration inhibitory factor (MIF) plays a pivotal role in immunity against Salmonella typhimurium. Proc Natl Acad Sci USA 2002, 99:13681-6. 10.1073/pnas.212488699, 129741, 12271144.
39. Gao XM, Liu Y, White D, Su Y, Drew BG, Bruce CR, Kiriazis H, Xu Q, Jennings N, Bobik A, Febbraio MA, Kingwell BA, Dart AM, Morand EF, Du XJ. Deletion of macrophage migration inhibitory factor protects the heart from severe ischemia-reperfusion injury: A predominant role of anti-inflammation. J Mol Cell Cardiol 2011, 50:991-9. 10.1016/j.yjmcc.2010.12.022, 21215754.
40. Lue H, Kleemann R, Calandra T, Roger T, Bernhagen J. Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes Infect 2002, 4:449-60. 10.1016/S1286-4579(02)01560-5, 11932196.
41. Baugh JA, Gantier M, Li L, Byrne A, Buckley A, Donnelly SC. Dual regulation of macrophage migration inhibitory factor (MIF) expression in hypoxia by CREB and HIF-1. Biochem Biophys Res Commun 2006, 347:895-903. 10.1016/j.bbrc.2006.06.148, 16854377.
42. Calandra T, Bernhagen J, Mitchell RA, Bucala R. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 1994, 179:1895-902. 10.1084/jem.179.6.1895, 2191507, 8195715.
43. Ruscher K, Shamloo M, Rickhag M, Ladunga I, Soriano L, Gisselsson L, Toresson H, Ruslim-Litrus L, Oksenberg D, Urfer R, Johansson BB, Nikolich K, Wieloch T. The sigma-1 receptor enhances brain plasticity and functional recovery after experimental stroke. Brain 2011, 134:732-46. 10.1093/brain/awq367, 21278085.
44. Manoonkitiwongsa PS, Jackson-Friedman C, McMillan PJ, Schultz RL, Lyden PD. Angiogenesis after stroke is correlated with increased numbers of macrophages: the clean-up hypothesis. J Cereb Blood Flow Metab 2001, 21:1223-31.
45. Schori H, Shechter R, Shachar I, Schwartz M. Genetic manipulation of CD74 in mouse strains of different backgrounds can result in opposite responses to central nervous system injury. J Immunol 2007, 178:163-71.