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Journal of Neuroinflammation
Published in: Journal of Neuroinflammation 1/2024

Open Access 01-12-2024 | Multiple Sclerosis | Review

MIF contribution to progressive brain diseases

Authors: Agata Matejuk, Gil Benedek, Richard Bucala, Szymon Matejuk, Halina Offner, Arthur A. Vandenbark

Published in: Journal of Neuroinflammation | Issue 1/2024

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Abstract

Progressive brain diseases create a huge social and economic burden on modern societies as a major cause of disability and death. Incidence of brain diseases has a significantly increasing trend and merits new therapeutic strategies. At the base of many progressive brain malfunctions is a process of unresolved, chronic inflammation. Macrophage migration inhibitory factor, MIF, is an inflammatory mediator that recently gained interest of neuro-researchers due to its varied effects on the CNS such as participation of nervous system development, neuroendocrine functions, and modulation of neuroinflammation. MIF appears to be a candidate as a new biomarker and target of novel therapeutics against numerous neurologic diseases ranging from cancer, autoimmune diseases, vascular diseases, neurodegenerative pathology to psychiatric disorders. In this review, we will focus on MIF’s crucial role in neurological diseases such as multiple sclerosis (MS), Alzheimer’s disease (AD) and glioblastoma (GBM).
Literature
1.
Bloom BR, Bennett B. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science. 1966;153(3731):80–2.PubMedCrossRef
2.
David JR. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc Natl Acad Sci U S A. 1966;56(1):72–7.PubMedPubMedCentralCrossRef
3.
Weiser WY, Temple PA, Witek-Giannotti JS, Remold HG, Clark SC, David JR. Molecular cloning of a cDNA encoding a human macrophage migration inhibitory factor. Proc Natl Acad Sci U S A. 1989;86(19):7522–6.PubMedPubMedCentralCrossRef
4.
Bernhagen J, Krohn R, Lue H, Gregory JL, Zernecke A, Koenen RR, et al. MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med. 2007;13(5):587–96.PubMedCrossRef
5.
Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Oksvold P, Mardinoglu A, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015;347(6220):1260419.PubMedCrossRef
6.
Thul PJ, Åkesson L, Wiking M, Mahdessian D, Geladaki A, Ait Blal H, Alm T, Asplund A, Björk L, Breckels LM, Bäckström A, Danielsson F, Fagerberg L, Fall J, Gatto L, Gnann C, Hober S, Hjelmare M, Johansson F, Lee S, Lindskog C, Mulder J, Mulvey CM, Nilsson P, Oksvold P, Rockberg J, Schutten R, Schwenk JM, Sivertsson Å, Sjöstedt E, Skogs M, Stadler C, Sullivan DP, Tegel H, Winsnes C, Zhang C, Zwahlen M, Mardinoglu A, Pontén F, von Feilitzen K, Lilley KS, Uhlén M, Lundberg E. A subcellular map of the human proteome. Science. 2017;356(6340):eaal3321. https://​doi.​org/​10.​1126/​science.​aal3321.
7.
Uhlen M, Zhang C, Lee S, Sjöstedt E, Fagerberg L, Bidkhori G, Benfeitas R, Arif M, Liu Z, Edfors F, Sanli K, von Feilitzen K, Oksvold P, Lundberg E, Hober S, Nilsson P, Mattsson J, Schwenk JM, Brunnström H, Glimelius B, Sjöblom T, Edqvist PH, Djureinovic D, Micke P, Lindskog C, Mardinoglu A, Ponten F. A pathology atlas of the human cancer transcriptome. Science. 2017;357(6352):eaan2507. https://​doi.​org/​10.​1126/​science.​aan2507.
8.
Calandra T, Bucala R. Macrophage migration inhibitory factor (MIF): a glucocorticoid counter-regulator within the immune system. Crit Rev Immunol. 2017;37(2–6):359–70.PubMedCrossRef
9.
Michell-Robinson MA, Touil H, Healy LM, Owen DR, Durafourt BA, Bar-Or A, et al. Roles of microglia in brain development, tissue maintenance and repair. Brain. 2015;138(Pt 5):1138–59.PubMedPubMedCentralCrossRef
10.
Su Y, Wang Y, Zhou Y, Zhu Z, Zhang Q, Zhang X, et al. Macrophage migration inhibitory factor activates inflammatory responses of astrocytes through interaction with CD74 receptor. Oncotarget. 2017;8(2):2719–30.PubMedCrossRef
11.
Sumaiya K, Langford D, Natarajaseenivasan K, Shanmughapriya S. Macrophage migration inhibitory factor (MIF): a multifaceted cytokine regulated by genetic and physiological strategies. Pharmacol Ther. 2022;233: 108024.PubMedCrossRef
12.
Song S, Xiao Z, Dekker FJ, Poelarends GJ, Melgert BN. Macrophage migration inhibitory factor family proteins are multitasking cytokines in tissue injury. Cell Mol Life Sci. 2022;79(2):105.PubMedPubMedCentralCrossRef
13.
Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, et al. MIF as a glucocorticoid-induced modulator of cytokine production. Nature. 1995;377(6544):68–71.PubMedCrossRef
14.
Bacher M, Metz CN, Calandra T, Mayer K, Chesney J, Lohoff M, et al. An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc Natl Acad Sci U S A. 1996;93(15):7849–54.PubMedPubMedCentralCrossRef
15.
Yao J, Leng L, Fu W, Li J, Bronner C, Bucala R. ICBP90 regulates MIF expression, glucocorticoid sensitivity, and apoptosis at the MIF immune susceptibility locus. Arthritis Rheumatol. 2021;73(10):1931–42.PubMedCrossRef
16.
Bernhagen J, Calandra T, Cerami A, Bucala R. Macrophage migration inhibitory factor is a neuroendocrine mediator of endotoxaemia. Trends Microbiol. 1994;2(6):198–201.PubMedCrossRef
17.
Bernhagen J, Calandra T, Mitchell RA, Martin SB, Tracey KJ, Voelter W, et al. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature. 1993;365(6448):756–9.PubMedCrossRef
18.
Lerch JK, Puga DA, Bloom O, Popovich PG. Glucocorticoids and macrophage migration inhibitory factor (MIF) are neuroendocrine modulators of inflammation and neuropathic pain after spinal cord injury. Semin Immunol. 2014;26(5):409–14.PubMedCrossRef
19.
Mitchell RA, Metz CN, Peng T, Bucala R. Sustained mitogen-activated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF). Regulatory role in cell proliferation and glucocorticoid action. J Biol Chem. 1999;274(25):18100–6.PubMedCrossRef
20.
Kleemann R, Hausser A, Geiger G, Mischke R, Burger-Kentischer A, Flieger O, et al. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature. 2000;408(6809):211–6.PubMedCrossRef
21.
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(10):1375–82.PubMedPubMedCentralCrossRef
22.
Su H, Na N, Zhang X, Zhao Y. The biological function and significance of CD74 in immune diseases. Inflamm Res. 2017;66(3):209–16.PubMedCrossRef
23.
Sanchez-Nino MD, Sanz AB, Ruiz-Andres O, Poveda J, Izquierdo MC, Selgas R, et al. MIF, CD74 and other partners in kidney disease: tales of a promiscuous couple. Cytokine Growth Factor Rev. 2013;24(1):23–40.PubMedCrossRef
24.
Kleemann R, Grell M, Mischke R, Zimmermann G, Bernhagen J. Receptor binding and cellular uptake studies of macrophage migration inhibitory factor (MIF): use of biologically active labeled MIF derivatives. J Interferon Cytokine Res. 2002;22(3):351–63.PubMedCrossRef
25.
26.
Bucala R, Shachar I. The integral role of CD74 in antigen presentation, MIF signal transduction, and B cell survival and homeostasis. Mini Rev Med Chem. 2014;14(14):1132–8.PubMedCrossRef
27.
Gil-Yarom N, Radomir L, Sever L, Kramer MP, Lewinsky H, Bornstein C, et al. CD74 is a novel transcription regulator. Proc Natl Acad Sci U S A. 2017;114(3):562–7.PubMedCrossRef
28.
Kim BS, Tilstam PV, Hwang SS, Simons D, Schulte W, Leng L, et al. D-dopachrome tautomerase in adipose tissue inflammation and wound repair. J Cell Mol Med. 2017;21(1):35–45.PubMedCrossRef
29.
30.
Yao J, Leng L, Sauler M, Fu W, Zheng J, Zhang Y, et al. Transcription factor ICBP90 regulates the MIF promoter and immune susceptibility locus. J Clin Invest. 2016;126(2):732–44.PubMedPubMedCentralCrossRef
31.
Radstake TR, Sweep FC, Welsing P, Franke B, Vermeulen SH, Geurts-Moespot A, et al. Correlation of rheumatoid arthritis severity with the genetic functional variants and circulating levels of macrophage migration inhibitory factor. Arthritis Rheum. 2005;52(10):3020–9.PubMedCrossRef
32.
Mizue Y, Ghani S, Leng L, McDonald C, Kong P, Baugh J, et al. Role for macrophage migration inhibitory factor in asthma. Proc Natl Acad Sci U S A. 2005;102(40):14410–5.PubMedPubMedCentralCrossRef
33.
Mitchell RA, Bucala R. Tumor growth-promoting properties of macrophage migration inhibitory factor (MIF). Semin Cancer Biol. 2000;10(5):359–66.PubMedCrossRef
34.
O’Reilly C, Doroudian M, Mawhinney L, Donnelly SC. Targeting MIF in cancer: therapeutic strategies, current developments, and future opportunities. Med Res Rev. 2016;36(3):440–60.PubMedCrossRef
35.
Bucala R. MIF, MIF alleles, and prospects for therapeutic intervention in autoimmunity. J Clin Immunol. 2013;33(Suppl 1):S72–8.PubMedCrossRef
36.
Leyton-Jaimes MF, Kahn J, Israelson A. Macrophage migration inhibitory factor: a multifaceted cytokine implicated in multiple neurological diseases. Exp Neurol. 2018;301(Pt B):83–91.PubMedCrossRef
37.
Li S, Nie K, Zhang Q, Guo M, Qiu Y, Li Y, et al. Macrophage migration inhibitory factor mediates neuroprotective effects by regulating inflammation, apoptosis and autophagy in Parkinson’s disease. Neuroscience. 2019;416:50–62.PubMedCrossRef
38.
Israelson A, Ditsworth D, Sun S, Song S, Liang J, Hruska-Plochan M, et al. Macrophage migration inhibitory factor as a chaperone inhibiting accumulation of misfolded SOD1. Neuron. 2015;86(1):218–32.PubMedPubMedCentralCrossRef
39.
40.
Dendrou CA, Fugger L, Friese MA. Immunopathology of multiple sclerosis. Nat Rev Immunol. 2015;15(9):545–58.PubMedCrossRef
41.
Barzegar M, Najdaghi S, Afshari-Safavi A, Nehzat N, Mirmosayyeb O, Shaygannejad V. Early predictors of conversion to secondary progressive multiple sclerosis. Mult Scler Relat Disord. 2021;54: 103115.PubMedCrossRef
42.
Liu YC, Tsai YH, Tang SC, Liou HC, Kang KH, Liou HH, et al. Cytokine MIF enhances blood-brain barrier permeability: impact for therapy in ischemic stroke. Sci Rep. 2018;8(1):743.PubMedPubMedCentralCrossRef
43.
Niino M, Ogata A, Kikuchi S, Tashiro K, Nishihira J. Macrophage migration inhibitory factor in the cerebrospinal fluid of patients with conventional and optic-spinal forms of multiple sclerosis and neuro-Behcet’s disease. J Neurol Sci. 2000;179(S 1–2):127–31.PubMedCrossRef
44.
Rinta S, Kuusisto H, Raunio M, Paalavuo R, Levula M, Lehtimaki T, et al. Apoptosis-related molecules in blood in multiple sclerosis. J Neuroimmunol. 2008;205(1–2):135–41.PubMedCrossRef
45.
Hagman S, Raunio M, Rossi M, Dastidar P, Elovaara I. Disease-associated inflammatory biomarker profiles in blood in different subtypes of multiple sclerosis: prospective clinical and MRI follow-up study. J Neuroimmunol. 2011;234(1–2):141–7.PubMedCrossRef
46.
Cavalli E, Mazzon E, Basile MS, Mangano K, Di Marco R, Bramanti P, Nicoletti F, Fagone P, Petralia MC. Upregulated Expression of Macrophage Migration Inhibitory Factor, Its Analogue D-Dopachrome Tautomerase, and the CD44 Receptor in Peripheral CD4 T Cells from Clinically Isolated Syndrome Patients with Rapid Conversion to Clinical Defined Multiple Sclerosis. Medicina (Kaunas). 2019;55(10):667. https://​doi.​org/​10.​3390/​medicina55100667​.
47.
Rijvers L, Melief MJ, van der Vuurst de Vries RM, Stephant M, van Langelaar J, Wierenga-Wolf AF, et al. The macrophage migration inhibitory factor pathway in human B cells is tightly controlled and dysregulated in multiple sclerosis. Eur J Immunol. 2018;48(11):1861–71.PubMedPubMedCentralCrossRef
48.
Cox GM, Kithcart AP, Pitt D, Guan Z, Alexander J, Williams JL, et al. Macrophage migration inhibitory factor potentiates autoimmune-mediated neuroinflammation. J Immunol. 2013;191(3):1043–54.PubMedCrossRef
49.
Khaibullin T, Ivanova V, Martynova E, Cherepnev G, Khabirov F, Granatov E, et al. Elevated levels of proinflammatory cytokines in cerebrospinal fluid of multiple sclerosis patients. Front Immunol. 2017;8:531.PubMedPubMedCentralCrossRef
50.
Hjaeresen S, Sejbaek T, Axelsson M, Mortensen SK, Vinslov-Jensen H, Pihl-Jensen G, et al. MIF in the cerebrospinal fluid is decreased during relapsing-remitting while increased in secondary progressive multiple sclerosis. J Neurol Sci. 2022;439: 120320.PubMedCrossRef
51.
Benedek G, Chaudhary P, Meza-Romero R, Calkins E, Kent G, Offner H, et al. Sex-dependent treatment of chronic EAE with partial MHC class II constructs. J Neuroinflamm. 2017;14(1):100.CrossRef
52.
Benedek G, Meza-Romero R, Jordan K, Zhang Y, Nguyen H, Kent G, et al. MIF and D-DT are potential disease severity modifiers in male MS subjects. Proc Natl Acad Sci U S A. 2017;114(40):E8421–9.PubMedPubMedCentralCrossRef
53.
De la Cruz-Mosso U, Bucala R, Palafox-Sanchez CA, Parra-Rojas I, Padilla-Gutierrez JR, Pereira-Suarez AL, et al. Macrophage migration inhibitory factor: association of -794 CATT5-8 and -173 G>C polymorphisms with TNF-alpha in systemic lupus erythematosus. Hum Immunol. 2014;75(5):433–9.PubMedPubMedCentralCrossRef
54.
Llamas-Covarrubias MA, Valle Y, Bucala R, Navarro-Hernandez RE, Palafox-Sanchez CA, Padilla-Gutierrez JR, et al. Macrophage migration inhibitory factor (MIF): genetic evidence for participation in early onset and early stage rheumatoid arthritis. Cytokine. 2013;61(3):759–65.PubMedPubMedCentralCrossRef
55.
Baugh JA, Chitnis S, Donnelly SC, Monteiro J, Lin X, Plant BJ, et al. A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis. Genes Immun. 2002;3(3):170–6.PubMedCrossRef
56.
Sreih A, Ezzeddine R, Leng L, LaChance A, Yu G, Mizue Y, et al. Dual effect of the macrophage migration inhibitory factor gene on the development and severity of human systemic lupus erythematosus. Arthritis Rheum. 2011;63(12):3942–51.PubMedPubMedCentralCrossRef
57.
Morales-Zambrano R, Bautista-Herrera LA, De la Cruz-Mosso U, Villanueva-Quintero GD, Padilla-Gutierrez JR, Valle Y, et al. Macrophage migration inhibitory factor (MIF) promoter polymorphisms (-794 CATT5-8 and -173 G>C): association with MIF and TNFalpha in psoriatic arthritis. Int J Clin Exp Med. 2014;7(9):2605–14.PubMedPubMedCentral
58.
Akcali A, Pehlivan S, Pehlivan M, Sever T, Neyal M. Association of macrophage migration inhibitory factor gene promoter polymorphisms with multiple sclerosis in Turkish patients. J Int Med Res. 2010;38(1):69–77.PubMedCrossRef
59.
Cevik B, Yigit S, Karakus N, Aksoy D, Ates O, Kurt S. Lack of association between MIF gene -173G>C polymorphism with multiple sclerosis. In Vivo. 2015;29(1):71–6.PubMed
60.
Castaneda Moreno VA, Muñoz-Valle JF, Torres Carrillo N, Gonzalez Perez OP, Macias Islas MA, Ruiz Sandoval JL, Padilla De La Torre O, Trujillo Trujillo XA, Huerta Vieyra M. A case-control study on the association of MIF-794 CATT5-8 and-173 G> C polymorphisms and its serum levels and the clinical severity of multiple sclerosis in Mexican patients. Front Immunol. 2015. https://​doi.​org/​10.​3389/​conf.​fimmu.​2015.​05.​00227.
61.
Castaneda-Moreno VA, De la Cruz-Mosso U, Torres-Carrillo N, Macias-Islas MA, Padilla-De la Torre O, Mireles-Ramirez MA, et al. MIF functional polymorphisms (-794 CATT(5–8) and -173 G>C) are associated with MIF serum levels, severity and progression in male multiple sclerosis from western Mexican population. J Neuroimmunol. 2018;320:117–24.PubMedCrossRef
62.
Han Z, Qu J, Zhao J, Zou X. Genetic variant rs755622 regulates expression of the multiple sclerosis severity modifier D-dopachrome tautomerase in a sex-specific way. Biomed Res Int. 2018;2018:8285653.PubMedPubMedCentralCrossRef
63.
Fagone P, Mazzon E, Cavalli E, Bramanti A, Petralia MC, Mangano K, et al. Contribution of the macrophage migration inhibitory factor superfamily of cytokines in the pathogenesis of preclinical and human multiple sclerosis: in silico and in vivo evidences. J Neuroimmunol. 2018;322:46–56.PubMedCrossRef
64.
Powell ND, Papenfuss TL, McClain MA, Gienapp IE, Shawler TM, Satoskar AR, et al. Cutting edge: macrophage migration inhibitory factor is necessary for progression of experimental autoimmune encephalomyelitis. J Immunol. 2005;175(9):5611–4.PubMedCrossRef
65.
Benedek G, Meza-Romero R, Andrew S, Leng L, Burrows GG, Bourdette D, et al. Partial MHC class II constructs inhibit MIF/CD74 binding and downstream effects. Eur J Immunol. 2013;43(5):1309–21.PubMedPubMedCentralCrossRef
66.
Meza-Romero R, Benedek G, Yu X, Mooney JL, Dahan R, Duvshani N, et al. HLA-DRalpha1 constructs block CD74 expression and MIF effects in experimental autoimmune encephalomyelitis. J Immunol. 2014;192(9):4164–73.PubMedCrossRef
67.
Benedek G, Meza-Romero R, Jordan K, Keenlyside L, Offner H, Vandenbark AA. HLA-DRalpha1-mMOG-35-55 treatment of experimental autoimmune encephalomyelitis reduces CNS inflammation, enhances M2 macrophage frequency, and promotes neuroprotection. J Neuroinflamm. 2015;12:123.CrossRef
68.
Ji N, Kovalovsky A, Fingerle-Rowson G, Guentzel MN, Forsthuber TG. Macrophage migration inhibitory factor promotes resistance to glucocorticoid treatment in EAE. Neurol Neuroimmunol Neuroinflamm. 2015;2(5): e139.PubMedPubMedCentralCrossRef
69.
Denkinger CM, Denkinger M, Kort JJ, Metz C, Forsthuber TG. In vivo blockade of macrophage migration inhibitory factor ameliorates acute experimental autoimmune encephalomyelitis by impairing the homing of encephalitogenic T cells to the central nervous system. J Immunol. 2003;170(3):1274–82.PubMedCrossRef
70.
Kithcart AP, Cox GM, Sielecki T, Short A, Pruitt J, Papenfuss T, et al. A small-molecule inhibitor of macrophage migration inhibitory factor for the treatment of inflammatory disease. FASEB J. 2010;24(11):4459–66.PubMedPubMedCentralCrossRef
71.
Cho Y, Crichlow GV, Vermeire JJ, Leng L, Du X, Hodsdon ME, et al. Allosteric inhibition of macrophage migration inhibitory factor revealed by ibudilast. Proc Natl Acad Sci U S A. 2010;107(25):11313–8.PubMedPubMedCentralCrossRef
72.
Schwenkgrub J, Zaremba M, Mirowska-Guzel D, Kurkowska-Jastrzebska I. Ibudilast: a non-selective phosphodiesterase inhibitor in brain disorders. Postepy Hig Med Dosw (Online). 2017;71:137–48.PubMedCrossRef
73.
Oyama R, Yamamoto H, Titani K. Glutamine synthetase, hemoglobin alpha-chain, and macrophage migration inhibitory factor binding to amyloid beta-protein: their identification in rat brain by a novel affinity chromatography and in Alzheimer’s disease brain by immunoprecipitation. Biochim Biophys Acta. 2000;1479(1–2):91–102.PubMedCrossRef
74.
Lashuel HA, Aljabari B, Sigurdsson EM, Metz CN, Leng L, Callaway DJ, et al. Amyloid fibril formation by macrophage migration inhibitory factor. Biochem Biophys Res Commun. 2005;338(2):973–80.PubMedCrossRef
75.
Bryan KJ, Zhu X, Harris PL, Perry G, Castellani RJ, Smith MA, et al. Expression of CD74 is increased in neurofibrillary tangles in Alzheimer’s disease. Mol Neurodegener. 2008;3:13.PubMedPubMedCentralCrossRef
76.
Yoshiyama Y, Arai K, Oki T, Hattori T. Expression of invariant chain and pro-cathepsin L in Alzheimer’s brain. Neurosci Lett. 2000;290(2):125–8.PubMedCrossRef
77.
Bacher M, Deuster O, Aljabari B, Egensperger R, Neff F, Jessen F, et al. The role of macrophage migration inhibitory factor in Alzheimer’s disease. Mol Med. 2010;16(3–4):116–21.PubMedPubMedCentralCrossRef
78.
Carlred L, Michno W, Kaya I, Sjovall P, Syvanen S, Hanrieder J. Probing amyloid-beta pathology in transgenic Alzheimer’s disease (tgArcSwe) mice using MALDI imaging mass spectrometry. J Neurochem. 2016;138(3):469–78.PubMedCrossRef
79.
Li SQ, Yu Y, Han JZ, Wang D, Liu J, Qian F, et al. Deficiency of macrophage migration inhibitory factor attenuates tau hyperphosphorylation in mouse models of Alzheimer’s disease. J Neuroinflamm. 2015;12:177.CrossRef
80.
Liang CJ, Li JH, Zhang Z, Zhang JY, Liu SQ, Yang J. Suppression of MIF-induced neuronal apoptosis may underlie the therapeutic effects of effective components of Fufang Danshen in the treatment of Alzheimer’s disease. Acta Pharmacol Sin. 2018;39(9):1421–38.PubMedPubMedCentralCrossRef
81.
Al-Abed Y, VanPatten S. MIF as a disease target: ISO-1 as a proof-of-concept therapeutic. Future Med Chem. 2011;3(1):45–63.PubMedCrossRef
82.
Nasiri E, Sankowski R, Dietrich H, Oikonomidi A, Huerta PT, Popp J, et al. Key role of MIF-related neuroinflammation in neurodegeneration and cognitive impairment in Alzheimer’s disease. Mol Med. 2020;26(1):34.PubMedPubMedCentralCrossRef
83.
Vitek MP, Bhattacharya K, Glendening JM, Stopa E, Vlassara H, Bucala R, et al. Advanced glycation end products contribute to amyloidosis in Alzheimer disease. Proc Natl Acad Sci U S A. 1994;91(11):4766–70.PubMedPubMedCentralCrossRef
84.
Sato T, Shimogaito N, Wu X, Kikuchi S, Yamagishi S, Takeuchi M. Toxic advanced glycation end products (TAGE) theory in Alzheimer’s disease. Am J Alzheimers Dis Other Demen. 2006;21(3):197–208.PubMedCrossRef
85.
Yu M, Zang D, Xu Y, Meng J, Qian S. Protective effect of ISO-1 against advanced glycation end product aggravation of PC12 cell injury induced by Abeta1-40. Mol Med Rep. 2019;20(3):2135–42.PubMedPubMedCentral
86.
Kassaar O, Pereira Morais M, Xu S, Adam EL, Chamberlain RC, Jenkins B, et al. Macrophage migration inhibitory factor is subjected to glucose modification and oxidation in Alzheimer’s Disease. Sci Rep. 2017;7:42874.PubMedPubMedCentralCrossRef
87.
Popp J, Bacher M, Kolsch H, Noelker C, Deuster O, Dodel R, et al. Macrophage migration inhibitory factor in mild cognitive impairment and Alzheimer’s disease. J Psychiatr Res. 2009;43(8):749–53.PubMedCrossRef
88.
Oikonomidi A, Tautvydaite D, Gholamrezaee MM, Henry H, Bacher M, Popp J. Macrophage migration inhibitory factor is associated with biomarkers of Alzheimer’s disease pathology and predicts cognitive decline in mild cognitive impairment and mild dementia. J Alzheimers Dis. 2017;60(1):273–81.PubMedCrossRef
89.
Zhang S, Zhao J, Zhang Y, Zhang Y, Cai F, Wang L, et al. Upregulation of MIF as a defense mechanism and a biomarker of Alzheimer’s disease. Alzheimers Res Ther. 2019;11(1):54.PubMedPubMedCentralCrossRef
90.
Bae SH, Yoo MR, Kim YY, Hong IK, Kim MH, Lee SH, et al. Brain-derived neurotrophic factor mediates macrophage migration inhibitory factor to protect neurons against oxygen-glucose deprivation. Neural Regen Res. 2020;15(8):1483–9.PubMedPubMedCentralCrossRef
91.
Moon HY, Kim SH, Yang YR, Song P, Yu HS, Park HG, et al. Macrophage migration inhibitory factor mediates the antidepressant actions of voluntary exercise. Proc Natl Acad Sci U S A. 2012;109(32):13094–9.PubMedPubMedCentralCrossRef
92.
Wesseling P, Capper D. WHO 2016 Classification of gliomas. Neuropathol Appl Neurobiol. 2018;44(2):139–50.PubMedCrossRef
93.
Wenger A, Ferreyra Vega S, Kling T, Bontell TO, Jakola AS, Caren H. Intratumor DNA methylation heterogeneity in glioblastoma: implications for DNA methylation-based classification. Neuro Oncol. 2019;21(5):616–27.PubMedPubMedCentralCrossRef
94.
Melin BS, Barnholtz-Sloan JS, Wrensch MR, Johansen C, Il’yasova D, Kinnersley B, et al. Genome-wide association study of glioma subtypes identifies specific differences in genetic susceptibility to glioblastoma and non-glioblastoma tumors. Nat Genet. 2017;49(5):789–94.PubMedPubMedCentralCrossRef
95.
Nobre CC, de Araujo JM, Fernandes TA, Cobucci RN, Lanza DC, Andrade VS, et al. Macrophage migration inhibitory factor (MIF): biological activities and relation with cancer. Pathol Oncol Res. 2017;23(2):235–44.PubMedCrossRef
96.
Bach JP, Deuster O, Balzer-Geldsetzer M, Meyer B, Dodel R, Bacher M. The role of macrophage inhibitory factor in tumorigenesis and central nervous system tumors. Cancer. 2009;115(10):2031–40.PubMedCrossRef
97.
Bucala R, Donnelly SC. Macrophage migration inhibitory factor: a probable link between inflammation and cancer. Immunity. 2007;26(3):281–5.PubMedCrossRef
98.
Kindt N, Journe F, Laurent G, Saussez S. Involvement of macrophage migration inhibitory factor in cancer and novel therapeutic targets. Oncol Lett. 2016;12(4):2247–53.PubMedPubMedCentralCrossRef
99.
Simpson KD, Templeton DJ, Cross JV. Macrophage migration inhibitory factor promotes tumor growth and metastasis by inducing myeloid-derived suppressor cells in the tumor microenvironment. J Immunol. 2012;189(12):5533–40.PubMedCrossRef
100.
Apte RS, Sinha D, Mayhew E, Wistow GJ, Niederkorn JY. Cutting edge: role of macrophage migration inhibitory factor in inhibiting NK cell activity and preserving immune privilege. J Immunol. 1998;160(12):5693–6.PubMedCrossRef
101.
Yan X, Orentas RJ, Johnson BD. Tumor-derived macrophage migration inhibitory factor (MIF) inhibits T lymphocyte activation. Cytokine. 2006;33(4):188–98.PubMedPubMedCentralCrossRef
102.
Ghoochani A, Schwarz MA, Yakubov E, Engelhorn T, Doerfler A, Buchfelder M, et al. MIF-CD74 signaling impedes microglial M1 polarization and facilitates brain tumorigenesis. Oncogene. 2016;35(48):6246–61.PubMedCrossRef
103.
Alban TJ, Bayik D, Otvos B, Rabljenovic A, Leng L, Jia-Shiun L, et al. Glioblastoma myeloid-derived suppressor cell subsets express differential macrophage migration inhibitory factor receptor profiles that can be targeted to reduce immune suppression. Front Immunol. 2020;11:1191.PubMedPubMedCentralCrossRef
104.
Mittelbronn M, Platten M, Zeiner P, Dombrowski Y, Frank B, Zachskorn C, et al. Macrophage migration inhibitory factor (MIF) expression in human malignant gliomas contributes to immune escape and tumour progression. Acta Neuropathol. 2011;122(3):353–65.PubMedCrossRef
105.
Zeiner PS, Preusse C, Blank AE, Zachskorn C, Baumgarten P, Caspary L, et al. MIF receptor CD74 is restricted to microglia/macrophages, associated with a M1-polarized immune milieu and prolonged patient survival in gliomas. Brain Pathol. 2015;25(4):491–504.PubMedCrossRef
106.
Wang D, Luo L, Chen W, Chen LZ, Zeng WT, Li W, et al. Significance of the vascular endothelial growth factor and the macrophage migration inhibitory factor in the progression of hepatocellular carcinoma. Oncol Rep. 2014;31(3):1199–204.PubMedCrossRef
107.
Chang KP, Lin SJ, Liu SC, Yi JS, Chien KY, Chi LM, et al. Low-molecular-mass secretome profiling identifies HMGA2 and MIF as prognostic biomarkers for oral cavity squamous cell carcinoma. Sci Rep. 2015;5:11689.PubMedPubMedCentralCrossRef
108.
Vera PL, Meyer-Siegler KL. Association between macrophage migration inhibitory factor promoter region polymorphism (-173 G/C) and cancer: a meta-analysis. BMC Res Notes. 2011;4:395.PubMedPubMedCentralCrossRef
109.
De Souza MB, Curioni OA, Kanda JL, De Carvalho MB. Serum and salivary macrophage migration inhibitory factor in patients with oral squamous cell carcinoma. Oncol Lett. 2014;8(5):2267–75.PubMedCrossRef
110.
Bacher M, Schrader J, Thompson N, Kuschela K, Gemsa D, Waeber G, et al. Up-regulation of macrophage migration inhibitory factor gene and protein expression in glial tumor cells during hypoxic and hypoglycemic stress indicates a critical role for angiogenesis in glioblastoma multiforme. Am J Pathol. 2003;162(1):11–7.PubMedPubMedCentralCrossRef
111.
Wang XB, Tian XY, Li Y, Li B, Li Z. Elevated expression of macrophage migration inhibitory factor correlates with tumor recurrence and poor prognosis of patients with gliomas. J Neurooncol. 2012;106(1):43–51.PubMedCrossRef
112.
Baron N, Deuster O, Noelker C, Stuer C, Strik H, Schaller C, et al. Role of macrophage migration inhibitory factor in primary glioblastoma multiforme cells. J Neurosci Res. 2011;89(5):711–7.PubMedCrossRef
113.
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(4):895–903.PubMedCrossRef
114.
Guo X, Xu S, Gao X, Wang J, Xue H, Chen Z, et al. Macrophage migration inhibitory factor promotes vasculogenic mimicry formation induced by hypoxia via CXCR4/AKT/EMT pathway in human glioblastoma cells. Oncotarget. 2017;8(46):80358–72.PubMedPubMedCentralCrossRef
115.
Bacher M, Meinhardt A, Lan HY, Dhabhar FS, Mu W, Metz CN, et al. MIF expression in the rat brain: implications for neuronal function. Mol Med. 1998;4(4):217–30.PubMedPubMedCentralCrossRef
116.
117.
Gieryng A, Pszczolkowska D, Walentynowicz KA, Rajan WD, Kaminska B. Immune microenvironment of gliomas. Lab Invest. 2017;97(5):498–518.PubMedCrossRef
118.
Chen Z, Feng X, Herting CJ, Garcia VA, Nie K, Pong WW, et al. Cellular and molecular identity of tumor-associated macrophages in glioblastoma. Can Res. 2017;77(9):2266–78.CrossRef
119.
Otvos B, Silver DJ, Mulkearns-Hubert EE, Alvarado AG, Turaga SM, Sorensen MD, et al. Cancer stem cell-secreted macrophage migration inhibitory factor stimulates myeloid derived suppressor cell function and facilitates glioblastoma immune evasion. Stem Cells. 2016;34(8):2026–39.PubMedCrossRef
120.
Kumar R, de Mooij T, Peterson TE, Kaptzan T, Johnson AJ, Daniels DJ, et al. Modulating glioma-mediated myeloid-derived suppressor cell development with sulforaphane. PLoS ONE. 2017;12(6): e0179012.PubMedPubMedCentralCrossRef
121.
Alban TJ, Alvarado AG, Sorensen MD, Bayik D, Volovetz J, Serbinowski E, Mulkearns-Hubert EE, Sinyuk M, Hale JS, Onzi GR, McGraw M, Huang P, Grabowski MM, Wathen CA, Ahluwalia MS, Radivoyevitch T, Kornblum HI, Kristensen BW, Vogelbaum MA, Lathia JD. Global immune fingerprinting in glioblastoma patient peripheral blood reveals immune-suppression signatures associated with prognosis. JCI Insight. 2018;3(21):e122264. https://​doi.​org/​10.​1172/​jci.​insight.​122264.
122.
Maltby S, Khazaie K, McNagny KM. Mast cells in tumor growth: angiogenesis, tissue remodelling and immune-modulation. Biochim Biophys Acta. 2009;1796(1):19–26.PubMedPubMedCentral
123.
Polajeva J, Bergstrom T, Edqvist PH, Lundequist A, Sjosten A, Nilsson G, et al. Glioma-derived macrophage migration inhibitory factor (MIF) promotes mast cell recruitment in a STAT5-dependent manner. Mol Oncol. 2014;8(1):50–8.PubMedCrossRef
124.
125.
Wang Z, Xue Y, Wang P, Zhu J, Ma J. MiR-608 inhibits the migration and invasion of glioma stem cells by targeting macrophage migration inhibitory factor. Oncol Rep. 2016;35(5):2733–42.PubMedCrossRef
126.
Fukaya R, Ohta S, Yaguchi T, Matsuzaki Y, Sugihara E, Okano H, et al. MIF maintains the tumorigenic capacity of brain tumor-initiating cells by directly inhibiting p53. Cancer Res. 2016;76(9):2813–23.PubMedCrossRef
127.
Jankauskas SS, Wong DWL, Bucala R, Djudjaj S, Boor P. Evolving complexity of MIF signaling. Cell Signal. 2019;57:76–88.PubMedCrossRef
128.
Shi X, Leng L, Wang T, Wang W, Du X, Li J, et al. CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity. 2006;25(4):595–606.PubMedPubMedCentralCrossRef
129.
McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EW, Chang F, et al. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta. 2007;1773(8):1263–84.PubMedCrossRef
130.
131.
Lue H, Thiele M, Franz J, Dahl E, Speckgens S, Leng L, et al. Macrophage migration inhibitory factor (MIF) promotes cell survival by activation of the Akt pathway and role for CSN5/JAB1 in the control of autocrine MIF activity. Oncogene. 2007;26(35):5046–59.PubMedCrossRef
132.
Fingerle-Rowson G, Petrenko O, Metz CN, Forsthuber TG, Mitchell R, Huss R, et al. The p53-dependent effects of macrophage migration inhibitory factor revealed by gene targeting. Proc Natl Acad Sci U S A. 2003;100(16):9354–9.PubMedPubMedCentralCrossRef
133.
Tanese K, Hashimoto Y, Berkova Z, Wang Y, Samaniego F, Lee JE, et al. Cell surface CD74-MIF interactions drive melanoma survival in response to interferon-gamma. J Invest Dermatol. 2015;135(11):2775–84.PubMedPubMedCentralCrossRef
134.
Merk M, Zierow S, Leng L, Das R, Du X, Schulte W, et al. The D-dopachrome tautomerase (DDT) gene product is a cytokine and functional homolog of macrophage migration inhibitory factor (MIF). Proc Natl Acad Sci U S A. 2011;108(34):E577–85.PubMedPubMedCentralCrossRef
135.
Kobold S, Merk M, Hofer L, Peters P, Bucala R, Endres S. The macrophage migration inhibitory factor (MIF)-homologue D-dopachrome tautomerase is a therapeutic target in a murine melanoma model. Oncotarget. 2014;5(1):103–7.PubMedCrossRef
136.
Brock SE, Rendon BE, Yaddanapudi K, Mitchell RA. Negative regulation of AMP-activated protein kinase (AMPK) activity by macrophage migration inhibitory factor (MIF) family members in non-small cell lung carcinomas. J Biol Chem. 2012;287(45):37917–25.PubMedPubMedCentralCrossRef
137.
Coleman AM, Rendon BE, Zhao M, Qian MW, Bucala R, Xin D, et al. Cooperative regulation of non-small cell lung carcinoma angiogenic potential by macrophage migration inhibitory factor and its homolog, D-dopachrome tautomerase. J Immunol. 2008;181(4):2330–7.PubMedCrossRef
138.
Guo D, Guo J, Yao J, Jiang K, Hu J, Wang B, et al. D-dopachrome tautomerase is over-expressed in pancreatic ductal adenocarcinoma and acts cooperatively with macrophage migration inhibitory factor to promote cancer growth. Int J Cancer. 2016;139(9):2056–67.PubMedCrossRef
139.
Winner M, Meier J, Zierow S, Rendon BE, Crichlow GV, Riggs R, et al. A novel, macrophage migration inhibitory factor suicide substrate inhibits motility and growth of lung cancer cells. Cancer Res. 2008;68(18):7253–7.PubMedPubMedCentralCrossRef
140.
Lee SH, Kwon HJ, Park S, Kim CI, Ryu H, Kim SS, et al. Macrophage migration inhibitory factor (MIF) inhibitor 4-IPP downregulates stemness phenotype and mesenchymal trans-differentiation after irradiation in glioblastoma multiforme. PLoS ONE. 2021;16(9): e0257375.PubMedPubMedCentralCrossRef
141.
Pasupuleti V, Du W, Gupta Y, Yeh IJ, Montano M, Magi-Galuzzi C, et al. Dysregulated D-dopachrome tautomerase, a hypoxia-inducible factor-dependent gene, cooperates with macrophage migration inhibitory factor in renal tumorigenesis. J Biol Chem. 2014;289(6):3713–23.PubMedCrossRef
142.
Mangano K, Mazzon E, Basile MS, Di Marco R, Bramanti P, Mammana S, et al. Pathogenic role for macrophage migration inhibitory factor in glioblastoma and its targeting with specific inhibitors as novel tailored therapeutic approach. Oncotarget. 2018;9(25):17951–70.PubMedPubMedCentralCrossRef
143.
Karim R, Palazzo C, Evrard B, Piel G. Nanocarriers for the treatment of glioblastoma multiforme: current state-of-the-art. J Control Release. 2016;227:23–37.PubMedCrossRef
144.
145.
Schrader J, Deuster O, Rinn B, Schulz M, Kautz A, Dodel R, et al. Restoration of contact inhibition in human glioblastoma cell lines after MIF knockdown. BMC Cancer. 2009;9:464.PubMedPubMedCentralCrossRef
146.
Piette C, Deprez M, Roger T, Noel A, Foidart JM, Munaut C. 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. 2009;284(47):32483–92.PubMedPubMedCentralCrossRef
147.
Kitange GJ, Carlson BL, Schroeder MA, Decker PA, Morlan BW, Wu W, et al. Expression of CD74 in high grade gliomas: a potential role in temozolomide resistance. J Neurooncol. 2010;100(2):177–86.PubMedPubMedCentralCrossRef
148.
Ha W, Sevim-Nalkiran H, Zaman AM, Matsuda K, Khasraw M, Nowak AK, et al. Ibudilast sensitizes glioblastoma to temozolomide by targeting macrophage migration inhibitory factor (MIF). Sci Rep. 2019;9(1):2905.PubMedPubMedCentralCrossRef
149.
Berkova Z, Tao RH, Samaniego F. Milatuzumab—a promising new immunotherapeutic agent. Expert Opin Investig Drugs. 2010;19(1):141–9.PubMedCrossRef
150.
Gore Y, Starlets D, Maharshak N, Becker-Herman S, Kaneyuki U, Leng L, et al. Macrophage migration inhibitory factor induces B cell survival by activation of a CD74-CD44 receptor complex. J Biol Chem. 2008;283(5):2784–92.PubMedCrossRef
151.
Wallace DJ, Figueras F, Wegener WA, Goldenberg DM. Experience with milatuzumab, an anti-CD74 antibody against immunomodulatory macrophage migration inhibitory factor (MIF) receptor, for systemic lupus erythematosus (SLE). Ann Rheum Dis. 2021;80(7):954–5.PubMedCrossRef
152.
Mahalingam D, Patel MR, Sachdev JC, Hart LL, Halama N, Ramanathan RK, et al. Phase I study of imalumab (BAX69), a fully human recombinant antioxidized macrophage migration inhibitory factor antibody in advanced solid tumours. Br J Clin Pharmacol. 2020;86(9):1836–48.PubMedPubMedCentralCrossRef
153.
Pantouris G, Syed MA, Fan C, Rajasekaran D, Cho TY, Rosenberg EM Jr, et al. An analysis of MIF structural features that control functional activation of CD74. Chem Biol. 2015;22(9):1197–205.PubMedPubMedCentralCrossRef
154.
Fingerle-Rowson G, Kaleswarapu DR, Schlander C, Kabgani N, Brocks T, Reinart N, et al. A tautomerase-null macrophage migration-inhibitory factor (MIF) gene knock-in mouse model reveals that protein interactions and not enzymatic activity mediate MIF-dependent growth regulation. Mol Cell Biol. 2009;29(7):1922–32.PubMedPubMedCentralCrossRef
155.
Orita M, Yamamoto S, Katayama N, Fujita S. Macrophage migration inhibitory factor and the discovery of tautomerase inhibitors. Curr Pharm Des. 2002;8(14):1297–317.PubMedCrossRef
156.
Lubetsky JB, Dios A, Han J, Aljabari B, Ruzsicska B, Mitchell R, et al. The tautomerase active site of macrophage migration inhibitory factor is a potential target for discovery of novel anti-inflammatory agents. J Biol Chem. 2002;277(28):24976–82.PubMedCrossRef
157.
Cournia Z, Leng L, Gandavadi S, Du X, Bucala R, Jorgensen WL. Discovery of human macrophage migration inhibitory factor (MIF)-CD74 antagonists via virtual screening. J Med Chem. 2009;52(2):416–24.PubMedPubMedCentralCrossRef
158.
Hare AA, Leng L, Gandavadi S, Du X, Cournia Z, Bucala R, et al. Optimization of N-benzyl-benzoxazol-2-ones as receptor antagonists of macrophage migration inhibitory factor (MIF). Bioorg Med Chem Lett. 2010;20(19):5811–4.PubMedPubMedCentralCrossRef
159.
Leng L, Chen L, Fan J, Greven D, Arjona A, Du X, et al. A small-molecule macrophage migration inhibitory factor antagonist protects against glomerulonephritis in lupus-prone NZB/NZW F1 and MRL/lpr mice. J Immunol. 2011;186(1):527–38.PubMedCrossRef
160.
Nakamura A, Zeng F, Nakamura S, Reid KT, Gracey E, Lim M, et al. Macrophage migration inhibitory factor drives pathology in a mouse model of spondyloarthritis and is associated with human disease. Sci Transl Med. 2021;13(616):eabg1210.PubMedCrossRef
161.
Fox RJ, Coffey CS, Conwit R, Cudkowicz ME, Gleason T, Goodman A, et al. Phase 2 trial of ibudilast in progressive multiple sclerosis. N Engl J Med. 2018;379(9):846–55.PubMedPubMedCentralCrossRef
162.
Tilstam PV, Pantouris G, Corman M, Andreoli M, Mahboubi K, Davis G, et al. A selective small-molecule inhibitor of macrophage migration inhibitory factor-2 (MIF-2), a MIF cytokine superfamily member, inhibits MIF-2 biological activity. J Biol Chem. 2019;294(49):18522–31.PubMedPubMedCentralCrossRef
163.
Xiao Z, Osipyan A, Song S, Chen D, Schut RA, van Merkerk R, et al. Thieno[2,3-d]pyrimidine-2,4(1H,3H)-dione derivative inhibits d-dopachrome tautomerase activity and suppresses the proliferation of non-small cell lung cancer cells. J Med Chem. 2022;65(3):2059–77.PubMedPubMedCentralCrossRef
164.
Rajasekaran D, Zierow S, Syed M, Bucala R, Bhandari V, Lolis EJ. Targeting distinct tautomerase sites of D-DT and MIF with a single molecule for inhibition of neutrophil lung recruitment. FASEB J. 2014;28(11):4961–71.PubMedPubMedCentralCrossRef
165.
Meza-Romero R, Benedek G, Jordan K, Leng L, Pantouris G, Lolis E, et al. Modeling of both shared and distinct interactions between MIF and its homologue D-DT with their common receptor CD74. Cytokine. 2016;88:62–70.PubMedPubMedCentralCrossRef
166.
Burrows GG, Chang JW, Bachinger HP, Bourdette DN, Offner H, Vandenbark AA. Design, engineering and production of functional single-chain T cell receptor ligands. Protein Eng. 1999;12(9):771–8.PubMedCrossRef
167.
Burrows GG. Systemic immunomodulation of autoimmune disease using MHC-derived recombinant TCR ligands. Curr Drug Targets Inflamm Allergy. 2005;4(2):185–93.PubMedPubMedCentralCrossRef
168.
Offner H, Sinha S, Wang C, Burrows GG, Vandenbark AA. Recombinant T cell receptor ligands: immunomodulatory, neuroprotective and neuroregenerative effects suggest application as therapy for multiple sclerosis. Rev Neurosci. 2008;19(4–5):327–39.PubMedPubMedCentral
169.
Vandenbark AA, Meza-Romero R, Benedek G, Andrew S, Huan J, Chou YK, et al. A novel regulatory pathway for autoimmune disease: binding of partial MHC class II constructs to monocytes reduces CD74 expression and induces both specific and bystander T-cell tolerance. J Autoimmun. 2013;40:96–110.PubMedCrossRef
170.
Vandenbark AA, Rich C, Mooney J, Zamora A, Wang C, Huan J, et al. Recombinant TCR ligand induces tolerance to myelin oligodendrocyte glycoprotein 35–55 peptide and reverses clinical and histological signs of chronic experimental autoimmune encephalomyelitis in HLA-DR2 transgenic mice. J Immunol. 2003;171(1):127–33.PubMedCrossRef
171.
Yadav V, Bourdette DN, Bowen JD, Lynch SG, Mattson D, Preiningerova J, et al. Recombinant T-cell receptor ligand (RTL) for treatment of multiple sclerosis: a double-blind, placebo-controlled, phase 1, dose-escalation study. Autoimmune Dis. 2012;2012: 954739.PubMedPubMedCentral
172.
Offner H, Sinha S, Burrows GG, Ferro AJ, Vandenbark AA. RTL therapy for multiple sclerosis: a phase I clinical study. J Neuroimmunol. 2011;231(1–2):7–14.PubMedCrossRef
173.
Vandenbark AA, Meza-Romero R, Benedek G, Offner H. A novel neurotherapeutic for multiple sclerosis, ischemic injury, methamphetamine addiction, and traumatic brain injury. J Neuroinflamm. 2019;16(1):14.CrossRef
174.
Vandenbark AA, Meza-Romero R, Wiedrick J, Gerstner G, Headrick A, Kent G, et al. Brief report: enhanced DRalpha1-mMOG-35-55 treatment of severe EAE in MIF-1-deficient male mice. Cell Immunol. 2021;370: 104439.PubMedPubMedCentralCrossRef
175.
Vandenbark AA, Meza-Romero R, Wiedrick J, Gerstner G, Seifert H, Kent G, et al. “Near Cure” treatment of severe acute EAE in MIF-1-deficient female and male mice with a bifunctional MHCII-derived molecular construct. Cell Immunol. 2022;378: 104561.PubMedPubMedCentralCrossRef
176.
Meza-Romero R, Benedek G, Gerstner G, Kent G, Nguyen H, Offner H, et al. Increased CD74 binding and EAE treatment efficacy of a modified DRalpha1 molecular construct. Metab Brain Dis. 2019;34(1):153–64.PubMedCrossRef
Metadata
Title
MIF contribution to progressive brain diseases
Authors
Agata Matejuk
Gil Benedek
Richard Bucala
Szymon Matejuk
Halina Offner
Arthur A. Vandenbark
Publication date
01-12-2024
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2024
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-023-02993-6

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