Macrophage migration inhibitory factor (MIF) expression in human malignant gliomas contributes to immune escape and tumour progression

Acta Neuropathologica

Volumn 122, Issue 3, 2011, Pages 353-365

  Mittelbronn, Michel ^a   Platten, Michael ^b,c   Zeiner, Pia ^a   Dombrowski, Yvonne ^d   Frank, Brigitte ^e   Zachskorn, Cornelia ^a   Harter, Patrick N ^a   Weller, Michael ^f   Wischhusen, Jörg ^d  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Glioma; Immunology; MIF; NK cells; NKG2D

Indexed keywords

MACROPHAGE MIGRATION INHIBITION FACTOR; MESSENGER RNA; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN P53; SHORT HAIRPIN RNA;

ARTICLE; ASTROCYTE; CANCER GRADING; CANCER GROWTH; CD8+ T LYMPHOCYTE; CELL LYSATE; CONTROLLED STUDY; DISEASE ACTIVITY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENETIC TRANSFECTION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IMMUNOSURVEILLANCE; IN VIVO STUDY; MAJOR CLINICAL STUDY; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TUMOR ESCAPE; WILD TYPE; WORLD HEALTH ORGANIZATION;

ANTIGENS, CD; ANTIGENS, CD31; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BRAIN NEOPLASMS; CELL LINE, TUMOR; DISEASE PROGRESSION; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOMA; HUMANS; KILLER CELLS, NATURAL; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MICROARRAY ANALYSIS; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; RNA, MESSENGER; TUMOR ESCAPE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 80054703162     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-011-0858-3     Document Type: Article

References (58)

1. Y Al Abed D Dabideen B Aljabari, et al. 2005 ISO-1 binding to the tautomerase active site of MIF inhibits its pro-inflammatory activity and increases survival in severe sepsis J Biol Chem 280 36541 36544 16115897 10.1074/jbc.C500243200 1:CAS:528:DC%2BD2MXhtFKht7bO (Pubitemid 41587728)
2. Y Al-Abed CN Metz KF Cheng, et al. 2011 Thyroxine is a potential endogenous antagonist of macrophage migration inhibitory factor (MIF) activity Proc Natl Acad Sci USA 108 20 8224 8227 21536912 10.1073/pnas.1017624108 1:CAS:528:DC%2BC3MXmsF2jsb4%3D
3. MA Amin OV Volpert JM Woods P Kumar LA Harlow AE Koch 2003 Migration inhibitory factor mediates angiogenesis via mitogen-activated protein kinase and phosphatidylinositol kinase Circ Res 93 4 321 329 12881477 10.1161/01.RES. 0000087641.56024.DA 1:CAS:528:DC%2BD3sXmt1Ohs7w%3D (Pubitemid 37048244)
4. RS Apte D Sinha E Mayhew GJ Wistow JY Niederkorn 1998 Cutting edge: role of macrophage migration inhibitory factor in inhibiting NK cell activity and preserving immune privilege J Immunol 160 12 5693 5696 9637476 1:CAS:528:DyaK1cXjvVWkurs%3D (Pubitemid 28298023)
5. JP Bach O Deuster M Balzer-Geldsetzer B Meyer R Dodel M Bacher 2009 The role of macrophage inhibitory factor in tumourigenesis and central nervous system tumours Cancer 115 2031 2040 19326434 10.1002/cncr.24245 1:CAS:528:DC%2BD1MXlvFOiu7w%3D
6. M Bacher O Deuster B Aljabari, et al. 2010 The role of macrophage migration inhibitory factor in Alzheimer's disease Mol Med 16 3-4 116 121 20200619 1:CAS:528:DC%2BC3cXjtV2gsLo%3D
7. M Bacher A Meinhardt HY Lan, et al. 1998 MIF expression in the rat brain: implications for neuronal function Mol Med 4 4 217 230 9606175 1:CAS:528:DyaK1cXjs1Kqtrw%3D (Pubitemid 28331239)
8. M Bacher J Schrader N Thompson, et al. 2003 Up-regulation of macrophage migration inhibitory factor gene and protein expression in glial tumour cells during hypoxic and hypoglycemic stress indicates a critical role for angiogenesis in glioblastoma multiforme Am J Pathol 162 1 11 17 12507885 10.1016/S0002-9440(10)63793-5 1:CAS:528:DC%2BD3sXlsFyrtg%3D%3D (Pubitemid 36041985)
9. N Baron O Deuster C Noelker, et al. 2011 Role of macrophage migration inhibitory factor in primary glioblastoma multiforme cells J Neurosci Res 89 711 717 21360573 10.1002/jnr.22595 1:CAS:528:DC%2BC3MXivFCitb4%3D
10. S Bauer V Groh J Wu, et al. 1999 Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA Science 285 727 729 10426993 10.1126/science.285.5428.727 1:CAS:528:DyaK1MXltVehsro%3D (Pubitemid 29484539)
11. R Baumann C Casaulta D Simon S Conus S Yousefi HU Simon 2003 Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria-dependent death pathway FASEB J 17 15 2221 2230 14656984 10.1096/fj.03-0110com 1:CAS:528:DC%2BD3sXpvVSmtrk%3D (Pubitemid 37509578)
12. J Bernhagen R Krohn H Lue, et al. 2007 MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment Nat Med 13 587 596 17435771 10.1038/nm1567 1:CAS:528:DC%2BD2sXkvVOhu7s%3D (Pubitemid 46828480)
13. BR Bloom B Bennett 1966 Mechanism of a reaction in vitro associated with delayed-type hypersensitivity Science 153 80 82 5938421 10.1126/science.153. 3731.80 1:CAS:528:DyaF28XksVWmt7g%3D
14. R Bucala SC Donnelly 2007 Macrophage migration inhibitory factor: a probable link between inflammation and cancer Immunity 26 281 285 17376392 10.1016/j.immuni.2007.03.005 1:CAS:528:DC%2BD2sXjvVSns7w%3D (Pubitemid 46413914)
15. T Calandra T Roger 2003 Macrophage migration inhibitory factor: a regulator of innate immunity Nat Rev Immunol 3 791 800 14502271 10.1038/nri1200 1:CAS:528:DC%2BD3sXntlWnsLY%3D (Pubitemid 37328657)
16. S Cludts C Decaestecker B Johnson, et al. 2010 Increased expression of macrophage migration inhibitory factor during progression to hypopharyngeal squamous cell carcinoma Anticancer Res 30 9 3313 3319 20944103
17. H Conroy L Mawhinney SC Donnelly 2010 Inflammation and cancer: macrophage migration inhibitory factor (MIF)-the potential missing link QJM 103 831 836 20805118 10.1093/qjmed/hcq148 1:CAS:528:DC%2BC3cXhtlSgtLzJ
18. R Craig-Schapiro M Kuhn C Xiong, et al. 2011 Multiplexed immunoassay panel identifies novel CSF biomarkers for Alzheimer's disease diagnosis and prognosis PLoS One 6 4 e18850 21526197 10.1371/journal.pone.0018850 1:CAS:528:DC%2BC3MXlt1aisL8%3D
19. JM Daun JG Cannon 2000 Macrophage migration inhibitory factor antagonizes hydrocortisone-induced increases in cytosolic IκBα Am J Physiol Regul Integr Comp Physiol 279 R1043 R1049 10956264 1:CAS:528: DC%2BD3cXmvFSjsr0%3D
20. Dumitru CA, Gholaman H, Trellakis S et al (2011) Tumour-derived macrophage migration inhibitory factor modulates the biology of head and neck cancer cells via neutrophil activation. Int J Cancer. doi: 10.1002/ijc.25991
21. G Eisele J Wischhusen M Mittelbronn, et al. 2006 TGF-β and metalloproteinases differentially suppress NKG2D ligand surface expression on malignant glioma cells Brain 129 2416 2425 16891318 10.1093/brain/awl205 (Pubitemid 44522126)
22. T Engelhorn NE Savaskan MA Schwarz, et al. 2009 Cellular characterization of the peritumoural edema zone in malignant brain tumours Cancer Sci 100 10 1856 1862 19681905 10.1111/j.1349-7006.2009.01259.x 1:CAS:528:DC%2BD1MXht12qs7jP
23. G Fingerle-Rowson O Petrenko CN Metz, et al. 2003 The p53-dependent effects of macrophage migration inhibitory factor revealed by gene targeting Proc Natl Acad Sci USA 100 16 9354 9359 12878730 10.1073/pnas.1533295100 1:CAS:528:DC%2BD3sXmtlyktL0%3D (Pubitemid 37033932)
24. MA Friese J Wischhusen W Wick, et al. 2004 RNA interference targeting transforming growth factor-beta enhances NKG2D-mediated antiglioma immune response, inhibits glioma cell migration and invasiveness, and abrogates tumourigenicity in vivo Cancer Res 64 7596 7603 15492287 10.1158/0008-5472.CAN- 04-1627 1:CAS:528:DC%2BD2cXosFynu7Y%3D (Pubitemid 39372105)
25. V Groh R Rhinehart H Secrist S Bauer KH Grabstein T Spies 1999 Broad tumour-associated expression and recognition by tumour-derived γδT cells of MICA and MICB Proc Natl Acad Sci USA 96 6879 6884 10359807 10.1073/pnas.96.12.6879 1:CAS:528:DyaK1MXks1Wktro%3D (Pubitemid 29274978)
26. JD Hudson MA Shoaibi R Maestro A Carnero GJ Hannon DH Beach 1999 A proinflammatory cytokine inhibits p53 tumour suppressor activity J Exp Med 190 10 1375 1382 10562313 10.1084/jem.190.10.1375 1:CAS:528:DyaK1MXnsVams7w%3D
27. H Jung HA Seong H Ha 2008 Direct interaction between NM23-H1 and macrophage migration inhibitory factor (MIF) is critical for alleviation of MIF-mediated suppression of p53 activity J Biol Chem 283 47 32669 32679 18815136 10.1074/jbc.M806225200 1:CAS:528:DC%2BD1cXhtlOjtLvJ
28. M Koda Y Nishio M Hashimoto, et al. 2004 Up-regulation of macrophage migration-inhibitory factor expression after compression-induced spinal cord injury in rats Acta Neuropathol 108 31 36 15067555 10.1007/s00401-004-0853-z 1:CAS:528:DC%2BD2cXks1Citr8%3D (Pubitemid 38961070)
29. M Krockenberger Y Dombrowski C Weidler, et al. 2008 Macrophage migration inhibitory factor contributes to the immune escape of ovarian cancer by down-regulating NKG2D J Immunol 180 11 7338 7348 18490733 1:CAS:528: DC%2BD1cXmtVanur0%3D
30. H Legendre C Decaestecker N Nagy, et al. 2003 Prognostic values of galectin-3 and the macrophage migration inhibitory factor (MIF) in human colorectal cancers Mod Pathol 16 5 491 504 12748256 10.1097/01.MP.0000068235. 45178.C1 (Pubitemid 36618470)
31. L Leng CN Metz Y Fang, et al. 2003 MIF signal transduction initiated by binding to CD74 J Exp Med 197 1467 1476 12782713 10.1084/jem.20030286 1:CAS:528:DC%2BD3sXksVOit7o%3D (Pubitemid 36686708)
32. H Liao R Bucala RA Mitchell 2003 Adhesion-dependent signaling by macrophage migration inhibitory factor (MIF) J Biol Chem 278 76 81 12297513 10.1074/jbc.M208820200 1:CAS:528:DC%2BD38XpvVWnsL8%3D (Pubitemid 36043546)
33. J Matsunaga D Sinha L Pannell, et al. 1999 Enzyme activity of macrophage migration inhibitory factor toward oxidized catecholamines J Biol Chem 274 6 3268 3271 9920865 10.1074/jbc.274.6.3268 1:CAS:528:DyaK1MXhtVenu7o%3D (Pubitemid 29077160)
34. J Matsunaga D Sinha F Solano C Santis G Wistow V Hearing 1999 Macrophage migration inhibitory factor (MIF)-its role in catecholamine metabolism Cell Mol Biol 45 7 1035 1040 10644007 1:CAS:528:DC%2BD3cXmtF2qtQ%3D%3D
35. RA Mitchell 2004 Mechanisms and effectors of MIF-dependent promotion of tumourigenesis Cell Signal 16 13 19 14607271 10.1016/j.cellsig.2003.07.002 1:CAS:528:DC%2BD3sXos1OlsLk%3D (Pubitemid 37357187)
36. RA Mitchell R Bucala 2000 Tumour growth-promoting properties of macrophage migration inhibitory factor (MIF) Semin Cancer Biol 10 359 366 11100884 10.1006/scbi.2000.0328 1:CAS:528:DC%2BD3cXovVaqsr4%3D
37. EF Morand M Leech J Bernhagen 2006 MIF: a new cytokine link between rheumatoid arthritis and atherosclerosis Nat Rev Drug Discov 5 399 410 16628200 10.1038/nrd2029 1:CAS:528:DC%2BD28XktVGmsbc%3D (Pubitemid 43904932)
38. C Munaut J Boniver JM Foidart M Deprez 2002 Macrophage migration inhibitory factor (MIF) expression in human glioblastomas correlates with vascular endothelial growth factor (VEGF) expression Neuropathol Appl Neurobiol 28 6 452 460 12445161 10.1046/j.1365-2990.2002.00416.x 1:CAS:528: DC%2BD38Xps1yjtLg%3D (Pubitemid 35425598)
39. M Nishibori N Nakaya S Mori K Saeki 1997 Immunohistochemical localization of macrophage migration inhibitory factor (MIF) in tanycytes, subcommissural organ and choroid plexus in the rat brain Brain Res 758 259 262 9203559 10.1016/S0006-8993(97)00342-9 1:CAS:528:DyaK2sXjtlWgtL4%3D (Pubitemid 27310668)
40. S Oda T Oda K Nishi, et al. 2008 Macrophage migration inhibitory factor activates hypoxia-inducible factor in a p53-dependent manner PLoS One 3 5 e2215 18493321 10.1371/journal.pone.0002215
41. H Ogawa J Nishihira Y Sato, et al. 2000 An antibody for macrophage migration inhibitory factor suppresses tumour growth and inhibits tumour-associated angiogenesis Cytokine 12 4 309 314 10805210 10.1006/cyto.1999.0562 1:CAS:528:DC%2BD3cXit1Cnt78%3D (Pubitemid 30449820)
42. H Ohgaki P Kleihues 2005 Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas J Neuropathol Exp Neurol 64 6 479 489 15977639 1:CAS:528:DC%2BD2MXlvVSgsbg%3D (Pubitemid 40781150)
43. T Ohkawara J Nishihira H Takeda M Asaka T Sugiyama 2005 Pathophysiological roles of macrophage migration inhibitory factor in gastrointestinal, hepatic, and pancreatic disorders J Gastroenterol 40 2 117 122 15770393 10.1007/s00535-004-1526-3 1:CAS:528:DC%2BD2MXit1Oks7s%3D (Pubitemid 40425197)
44. C ∅stergaard T Benfield 2009 Macrophage migration inhibitory factor in cerebrospinal fluid from patients with central nervous system infection Crit Care 13 3 R101 19558639 10.1186/cc7933
45. O Petrenko G Fingerle-Rowson T Peng RA Mitchell CN Metz 2003 Macrophage migration inhibitory factor deficiency is associated with altered cell growth and reduced susceptibility to Ras-mediated transformation J Biol Chem 278 11078 11085 12538581 10.1074/jbc.M211985200 1:CAS:528:DC%2BD3sXit1Kgs74%3D (Pubitemid 36792659)
46. C Piette M Deprez T Roger A Noël JM Foidart C Munaut 2009 The dexamethasone-induced inhibition of proliferation, migration, and invasion in glioma cell lines is antagonized by macrophage migration inhibitory factor (MIF) and can be enhanced by specific MIF inhibitors J Biol Chem 284 47 32483 32492 19759012 10.1074/jbc.M109.014589 1:CAS:528:DC%2BD1MXhsVSmur%2FE
47. J Popp M Bacher H Kölsch, et al. 2009 Macrophage migration inhibitory factor in mild cognitive impairment and Alzheimer's disease J Psychiatr Res 43 8 749 753 19038405 10.1016/j.jpsychires.2008.10.006
48. BE Rendon T Roger I Teneng, et al. 2007 Regulation of human lung adenocarcinoma cell migration and invasion by macrophage migration inhibitory factor J Biol Chem 282 41 29910 29918 17709373 10.1074/jbc.M704898200 1:CAS:528:DC%2BD2sXhtFagtbrJ (Pubitemid 350035289)
49. AC Repp ES Mayhew S Apte JY Niederkorn 2000 Human uveal melanoma cells produce macrophage migration-inhibitory factor to prevent lysis by NK cells J Immunol 165 710 715 10878343 1:CAS:528:DC%2BD3cXkvFWis7g%3D (Pubitemid 30484736)
50. Y Sasaki K Kasuya J Nishihira, et al. 2002 Suppression of tumour growth through introduction of an antisense plasmid of macrophage migration inhibitory factor Int J Mol Med 10 5 579 583 12373295 1:CAS:528:DC%2BD38XosFSqsr8%3D
51. J Schrader O Deuster B Rinn, et al. 2009 Restoration of contact inhibition in human glioblastoma cell lines after MIF knockdown BMC Cancer 9 464 20038293 10.1186/1471-2407-9-464
52. T Seike K Fujita Y Yamakawa, et al. 2011 Interaction between lung cancer cells and astrocytes via specific inflammatory cytokines in the microenvironment of brain metastasis Clin Exp Metastasis 28 13 25 20953899 10.1007/s10585-010- 9354-8 1:CAS:528:DC%2BC3cXhsFCru7zI
53. X Shi L Leng T Wang, et al. 2006 CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex Immunity 25 595 606 17045821 10.1016/j.immuni.2006.08.020 1:CAS:528:DC%2BD28XhtFemtbvI (Pubitemid 44529040)
54. M Tarnowski K Grymula R Liu, et al. 2010 Macrophage migration inhibitory factor is secreted by rhabdomyosarcoma cells, modulates tumour metastasis by binding to CXCR4 and CXCR7 receptors and inhibits recruitment of cancer-associated fibroblasts Mol Cancer Res 8 10 1328 1343 20861157 10.1158/1541-7786.MCR-10-0288 1:CAS:528:DC%2BC3cXht12ksLnP
55. H Vedder JC Krieg B Gerlach D Gemsa M Bacher 2000 Expression and glucocorticoid regulation of macrophage migration inhibitory factor (MIF) in hippocampal and neocortical rat brain cells in culture Brain Res 869 1-2 25 30 10865055 10.1016/S0006-8993(00)02336-2 1:CAS:528:DC%2BD3cXktFCgt78%3D (Pubitemid 30345771)
56. ES White KR Flaherty S Carskadon, et al. 2003 Macrophage migration inhibitory factor and CXC chemokine expression in non-small cell lung cancer: role in angiogenesis and prognosis Clin Cancer Res 9 2 853 860 12576459 1:CAS:528:DC%2BD3sXhtVKktrw%3D (Pubitemid 36182624)
57. J Wischhusen U Naumann H Ohgaki F Rastinejad M Weller 2003 CP-31398, a novel p53-stabilizing agent, induces p53-dependent and p53-independent glioma cell death Oncogene 22 8233 8245 14614447 10.1038/sj.onc.1207198 1:CAS:528:DC%2BD3sXovVymsLw%3D (Pubitemid 37485516)
58. HH Xia Y Yang KM Chu, et al. 2009 Serum macrophage migration-inhibitory factor as a diagnostic and prognostic biomarker for gastric cancer Cancer 115 23 5441 5449 19685530 10.1002/cncr.24609 1:CAS:528:DC%2BD1MXhsFOmsb%2FE