
Macrophage migration inhibitory factor: Exploring physiological roles and comparing health benefits against oncogenic and autoimmune risks (Review)
- Authors:
- Gustavo Camacho Meza
- Guadalupe Avalos Navarro
- Ulises De La Cruz Mosso
- Ramiro Ramírez Patiño
- Jose Francisco Muñoz Valle
- Luis Alberto Bautista Herrera
-
Affiliations: Department of Pharmacobiology, University Center of Exact Sciences and Engineering, University of Guadalajara, Guadalajara, Jalisco 44430, Mexico, Department of Life Sciences, University Center of La Ciénega, University of Guadalajara, Ocotlán, Jalisco 47810, Mexico, Department of Molecular Biology and Genomics, University Center of Health Sciences, University of Guadalajara, Guadalajara, Jalisco 44340, Mexico - Published online on: July 18, 2025 https://doi.org/10.3892/ijmm.2025.5590
- Article Number: 149
-
Copyright: © Camacho Meza et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Bloom BR and Bennett B: Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science. 153:80–82. 1966. View Article : Google Scholar : PubMed/NCBI |
|
David JR: Delayed hypersensitivity in vitro: Its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc Natl Acad Sci USA. 56:72–77. 1966. View Article : Google Scholar : PubMed/NCBI |
|
Weiser WY, Temple PA, Witek-Giannotti JS, Remold HG, Clark SC and David JR: Molecular cloning of a cDNA encoding a human macrophage migration inhibitory factor. Proc Natl Acad Sci USA. 86:7522–7526. 1989. View Article : Google Scholar : PubMed/NCBI |
|
Bernhagen J, Mitchell RA, Calandra T, Voelter W, Cerami A and Bucala R: Purification, bioactivity, and secondary structure analysis of mouse and human macrophage migration inhibitory factor (MIF). Biochemistry. 33:14144–14155. 1994. View Article : Google Scholar : PubMed/NCBI |
|
Nishino T, Bernhagen J, Shiiki H, Calandra T, Dohi K and Bucala R: Localization of macrophage migration inhibitory factor (MIF) to secretory granules within the corticotrophic and thyrotrophic cells of the pituitary gland. Mol Med. 1:781–788. 1995. View Article : Google Scholar : PubMed/NCBI |
|
Sun HW, Bernhagentt J, Bucalat R and Lolis E: Crystal structure at 2.6-A resolution of human macrophage migration inhibitory factor. Proc Natl Acad Sci USA. 93:5191–5196. 1996. View Article : Google Scholar : PubMed/NCBI |
|
Bacher M, Metz CN, Calandra T, Mayer K, Chesney J, Lohoff M, Gemsa D, Donnelly T and Bucala R: An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc Natl Acad Sci USA. 93:7849–7854. 1996. View Article : Google Scholar : PubMed/NCBI |
|
Chesney J, Metz C, Bacher M, Peng T, Meinhardt A and Bucala R: An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Mol Med. 5:181–191. 1999. View Article : Google Scholar : PubMed/NCBI |
|
Huang XR, Chun Hui CW, Chen YX, Wong BC, Fung PC, Metz C, Cho CH, Hui WM, Bucala R, Lam SK and Lan HY: Macrophage migration inhibitory factor is an important mediator in the pathogenesis of gastric inflammation in rats. Gastroenterology. 121:619–630. 2001. View Article : Google Scholar : PubMed/NCBI |
|
Kleemann R, Kapurniotu A, Frank RW, Gessner A, Mischke R, Flieger O, Jüttner S, Brunner H and Bernhagen J: Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J Mol Biol. 280:85–102. 1998. View Article : Google Scholar : PubMed/NCBI |
|
Matsunaga J, Sinha D, Pannell L, Santist C, Solano F, Wistow GJ and Hearing VJ: Enzyme activity of macrophage migration inhibitory factor toward oxidized catecholamines. J Biol Chem. 274:3268–3271. 1999. View Article : Google Scholar : PubMed/NCBI |
|
Leech M, Metz C, Santos L, Peng T, Holdsworth SR, Bucala R and Morand EF: Involvement of macrophage migration inhibitory factor in the evolution of rat adjuvant arthritis. Arthritis Rheum. 41:910–917. 1998. View Article : Google Scholar : PubMed/NCBI |
|
Leech M, Metz C, Hall P, Hutchinson P, Gianis K, Smith M, Weedon H, Holdsworth SR, Bucala R and Morand EF: Macrophage migration inhibitory factor in rheumatoid arthritis: Evidence of proinflammatory function and regulation by glucocorticoids. Arthritis Rheum. 42:1601–1608. 1999. View Article : Google Scholar : PubMed/NCBI |
|
Petrovsky N, Socha L, Silva D, Grossman AB, Metz C and Bucala R: Macrophage migration inhibitory factor exhibits a pronounced circadian rhythm relevant to its role as a glucocorticoid counter-regulator. Immunol Cell Biol. 81:137–143. 2003. View Article : Google Scholar : PubMed/NCBI |
|
Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA and Bucala R: MIF signal transduction initiated by binding to CD74. J Exp Med. 197:1467–1476. 2003. View Article : Google Scholar : PubMed/NCBI |
|
Chen LC, Lei HY, Liu CC, Shiesh SC, Chen SH, Liu HS, Lin YS, Wang ST, Shyu HW and Yeh TM: Correlation of serum levels of macrophage migration inhibitory factor with disease severity and clinical outcome in dengue patients. Am J Trop Med Hyg. 74:142–147. 2006. View Article : Google Scholar : PubMed/NCBI |
|
Bernhagen J, Krohn R, Lue H, Gregory JL, Zernecke A, Koenen RR, Dewor M, Georgiev I, Schober A, Leng L, et al: MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med. 13:587–596. 2007. View Article : Google Scholar : PubMed/NCBI |
|
Chuang YC, Su WH, Lei HY, Lin YS, Liu HS, Chang CP and Yeh TM: Macrophage migration inhibitory factor induces autophagy via reactive oxygen species generation. PLoS One. 7:e376132012. View Article : Google Scholar : PubMed/NCBI |
|
Wang Y, Chen Y, Wang C, Yang M, Wang Y, Bao L, Wang JE, Kim B, Chan KY, Xu W, et al: MIF is a 3′ flap nuclease that facilitates DNA replication and promotes tumor growth. Nat Commun. 12:29542021. View Article : Google Scholar |
|
Michelet C: Evolutionary and functional analysis of macrophage migration inhibitory factors in eukaryotes. unpublished PhD thesis. COMUE Université Côte d'Azur; 2020, In French. |
|
Jankauskas SS, Wong DWL, Bucala R, Djudjaj S and Boor P: Evolving complexity of MIF signaling. Cell Signal. 57:76–88. 2019. View Article : Google Scholar : PubMed/NCBI |
|
Sumaiya K, Langford D, Natarajaseenivasan K and Shanmughapriya S: Macrophage migration inhibitory factor (MIF): A multifaceted cytokine regulated by genetic and physiological strategies. Pharmacol Ther. 233:1080242022. View Article : Google Scholar |
|
Merk M, Baugh J, Zierow S, Leng L, Pal U, Lee SJ, Ebert AD, Mizue Y, Trent JO, Mitchell R, et al: The Golgi-associated protein p115 mediates the secretion of macrophage migration inhibitory factor. J Immunol. 182:6896–6906. 2009. View Article : Google Scholar : PubMed/NCBI |
|
Cheng Q, McKeown SJ, Santos L, Santiago FS, Khachigian LM, Morand EF and Hickey MJ: Macrophage migration inhibitory factor increases leukocyte-endothelial interactions in human endothelial cells via promotion of expression of adhesion molecules. J Immunol. 185:1238–1247. 2010. View Article : Google Scholar : PubMed/NCBI |
|
He XX, Yang J, Ding YW, Liu W, Shen QY and Xia HHX: Increased epithelial and serum expression of macrophage migration inhibitory factor (MIF) in gastric cancer: Potential role of MIF in gastric carcinogenesis. Gut. 55:797–802. 2006. View Article : Google Scholar : PubMed/NCBI |
|
Hu CT, Guo LL, Feng N, Zhang L, Zhou N, Ma LL, Shen L, Tong GH, Yan QW, Zhu SJ, et al: MIF, secreted by human hepatic sinusoidal endothelial cells, promotes chemotaxis and outgrowth of colorectal cancer in liver prometastasis. Oncotarget. 6:22410–22423. 2015. View Article : Google Scholar : PubMed/NCBI |
|
Nishihira J, Koyama Y and Mizue Y: Identification of macrophage migration inhibitory factor (MIF) in human vascular endothelial cells and its induction by lipopolysaccharide. Cytokine. 10:199–205. 1998. View Article : Google Scholar : PubMed/NCBI |
|
Pellowe AS, Sauler M, Hou Y, Merola J, Liu R, Calderon B, Lauridsen HM, Harris MR, Leng L and Zhang Y: Endothelial cell-secreted MIF reduces pericyte contractility and enhances neutrophil extravasation. FASEB J. 33:2171–2186. 2019. View Article : Google Scholar : |
|
Farag AGA, Hammam MA, Habib MS, Elnaidany NF and Kamh ME: Macrophage migration inhibitory factor as an incriminating agent in vitiligo. An Bras Dermatol. 93:191–196. 2018. View Article : Google Scholar : PubMed/NCBI |
|
Waeber G, Calandra T, Roduit R, Haefliger JA, Bonny C, Thompson N, Thorens B, Temler E, Meinhardt A, Bacher M, et al: Insulin secretion is regulated by the glucose-dependent production of islet beta cell macrophage migration inhibitory factor. Proc Natl Acad Sci USA. 94:4782–4787. 1997. View Article : Google Scholar : PubMed/NCBI |
|
Guda MR, Rashid MA, Asuthkar S, Jalasutram A, Caniglia JL, Tsung AJ and Velpula KK: Pleiotropic role of macrophage migration inhibitory factor in cancer. Am J Cancer Res. 9:2760–2773. 2019. |
|
Kang I and Bucala R: The immunobiology of MIF: Function, genetics and prospects for precision medicine. Nat Rev Rheumatol. 15:427–437. 2019. View Article : Google Scholar : PubMed/NCBI |
|
Nobre CCG, de Araújo JMG, de Medeiros Fernandes TAA, Cobucci RN, Lanza DCF, Andrade VS and Fernandes JV: Macrophage migration inhibitory factor (MIF): Biological activities and relation with cancer. Pathol Oncol Res. 23:235–244. 2017. View Article : Google Scholar |
|
Osipyan A, Chen D and Dekker FJ: Epigenetic regulation in macrophage migration inhibitory factor (MIF)-mediated signaling in cancer and inflammation. Drug Discov Today. 26:1728–1734. 2021. View Article : Google Scholar : PubMed/NCBI |
|
Zhou Y, Chen H, Liu L, Yu X, Sukhova GK, Yang M, Zhang L, Kyttaris VC, Tsokos GC, Stillman IE, et al: CD74 deficiency mitigates systemic lupus erythematosus-like autoimmunity and pathological findings in mice. J Immunol. 198:2568–2577. 2017. View Article : Google Scholar : PubMed/NCBI |
|
Younan DNA, Agamia N, Elshafei A and Ebeid N: Serum level of macrophage migration inhibitory factor (MIF) in Egyptians with alopecia areata and its relation to the clinical severity of the disease. J Clin Lab Anal. 29:74–79. 2015. View Article : Google Scholar |
|
Llamas-Covarrubias MA, Valle Y, Navarro-Hernández RE, Guzmán-Guzmán IP, Ramírez-Dueñas MG, Rangel-Villalobos H, Estrada-Chávez C and Muñoz-Valle JF: Serum levels of macrophage migration inhibitory factor are associated with rheumatoid arthritis course. Rheumatol Int. 32:2307–2311. 2012. View Article : Google Scholar |
|
Mizue Y, Nishihira J, Miyazaki T, Fujiwara S, Chida M, Nakamura K, Kikuchi K and Mukai M: Quantitation of macrophage migration inhibitory factor (MIF) using the one-step sandwich enzyme immunosorbent assay: Elevated serum MIF concentrations in patients with autoimmune diseases and identification of MIF in erythrocytes. Int J Mol Med. 5:397–403. 2000.PubMed/NCBI |
|
Willeke P, Gaubitz M, Schotte H, Maaser C, Domschke W, Schlüter B and Becker H: Increased serum levels of macrophage migration inhibitory factor in patients with primary Sjögren's syndrome. Arthritis Res Ther. 9:R432007. View Article : Google Scholar |
|
Ren Y, Law S, Huang X, Lee PY, Bacher M, Srivastava G and Wong J: Macrophage migration inhibitory factor stimulates angiogenic factor expression and correlates with differentiation and lymph node status in patients with esophageal squamous cell carcinoma. Ann Surg. 242:55–63. 2005. View Article : Google Scholar : PubMed/NCBI |
|
Fersching DMI, Nagel D, Siegele B, Salat C, Heinemann V, Holdenrieder S and Stoetzer OJ: Apoptosis-related biomarkers sFAS, MIF, ICAM-1 and PAI-1 in serum of breast cancer patients undergoing neoadjuvant chemotherapy. Anticancer Res. 32:2047–2058. 2012.PubMed/NCBI |
|
Yamada G, Shijubo N, Takagi-Takahashi Y, Nishihira J, Mizue Y, Kikuchi K and Abe S: Elevated levels of serum macrophage migration inhibitory factor in patients with pulmonary tuberculosis. Clin Immunol. 104:123–127. 2002. View Article : Google Scholar : PubMed/NCBI |
|
Ganganna A, Subappa A and Bhandari P: Serum migration inhibitory factor levels in periodontal health and disease, its correlation with clinical parameters. Indian J Dent Res. 31:840–845. 2020. View Article : Google Scholar |
|
Emonts M, Sweep FCGJ, Grebenchtchikov N, Geurts-Moespot A, Knaup M, Chanson AL, Erard V, Renner P, Hermans PW, Hazelzet JA and Calandra T: Association between high levels of blood macrophage migration inhibitory factor, inappropriate adrenal response, and early death in patients with severe sepsis. Clin Infect Dis. 44:1321–1328. 2007. View Article : Google Scholar : PubMed/NCBI |
|
Honda K, Nishihira J, Nitta K, Kobayashi H, Uchida K, Kawashima A, Yumura W and Nihei H: Serum levels of macrophage migration inhibitory factor in various types of glomerulonephritis. Nephron. 86:91–92. 2000. View Article : Google Scholar : PubMed/NCBI |
|
Lee TJ, Chun JK, Yeon SI, Shin JS and Kim DS: Increased serum levels of macrophage migration inhibitory factor in patients with Kawasaki disease. Scand J Rheumatol. 36:222–225. 2007. View Article : Google Scholar : PubMed/NCBI |
|
Sugimoto H, Taniguchi M, Nakagawa A, Tanaka I, Suzuki M and Nishihira J: Crystal structure of human D-dopachrome tautomerase, a homologue of macrophage migration inhibitory factor, at 1.54 A resolution. Biochemistry. 38:3268–3279. 1999. View Article : Google Scholar : PubMed/NCBI |
|
Cooke G, Armstrong ME and Donnelly SC: Macrophage migration inhibitory factor (MIF), enzymatic activity and the inflammatory response. Biofactors. 35:165–168. 2009. View Article : Google Scholar : PubMed/NCBI |
|
Fernández G, Arráiz De Fernández C, Valero N, Andrés Martínez J and López J: Adiponectin, hepatic steatosis and the prevention of child obesity. Enferm Inv. 5:17–24. 2020.In Spanish. |
|
Farr L, Ghosh S and Moonah S: Role of MIF cytokine/CD74 receptor pathway in protecting against injury and promoting repair. Front Immunol. 11:12732020. View Article : Google Scholar : PubMed/NCBI |
|
Lue H, Thiele M, Franz J, Dahl E, Speckgens S, Leng L, Fingerle-Rowson G, Bucala R, Lüscher B and Bernhagen J: 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. 26:5046–5059. 2007. View Article : Google Scholar : PubMed/NCBI |
|
Matza D, Kerem A, Medvedovsky H, Lantner F and Shachar I: Invariant chain-induced B cell differentiation requires intramembrane proteolytic release of the cytosolic domain. Immunity. 17:549–560. 2002. View Article : Google Scholar : PubMed/NCBI |
|
Schneppenheim J, Dressel R, Hüttl S, Lüllmann-Rauch R, Engelke M, Dittmann K, Wienands J, Eskelinen EL, Hermans-Borgmeyer I, Fluhrer R, et al: The intramembrane protease SPPL2a promotes B cell development and controls endosomal traffic by cleavage of the invariant chain. J Exp Med. 210:41–58. 2013. View Article : Google Scholar : |
|
Bucala R and Shachar I: The integral role of CD74 in antigen presentation, MIF signal transduction, and B cell survival and homeostasis. Mini Rev Med Chem. 14:1132–1138. 2014. View Article : Google Scholar |
|
Lue H, Kapurniotu A, Fingerle-Rowson G, Roger T, Leng L, Thiele M, Calandra T, Bucala R and Bernhagen J: Rapid and transient activation of the ERK MAPK signalling pathway by macrophage migration inhibitory factor (MIF) and dependence on JAB1/CSN5 and Src kinase activity. Cell Signal. 18:688–703. 2006. View Article : Google Scholar |
|
Gaber T, Schellmann S, Erekul KB, Fangradt M, Tykwinska K, Hahne M, Maschmeyer P, Wagegg M, Stahn C, Kolar P, et al: Macrophage migration inhibitory factor counterregulates dexamethasone-mediated suppression of hypoxia-inducible factor-1 alpha function and differentially influences human CD4+ T cell proliferation under hypoxia. J Immunol. 186:764–774. 2011. View Article : Google Scholar |
|
Mun SH, Oh D and Lee SK: Macrophage migration inhibitory factor down-regulates the RANKL-RANK signaling pathway by activating Lyn tyrosine kinase in mouse models. Arthritis Rheumatol. 66:2482–2493. 2014. View Article : Google Scholar : PubMed/NCBI |
|
Guo Y, Pan W, Liu S, Shen Z, Xu Y and Hu L: ERK/MAPK signalling pathway and tumorigenesis (Review). Exp Ther Med. 19:1997–2007. 2020.PubMed/NCBI |
|
Bucala R and Bernhagen J: MIF Family Cytokines in Innate Immunity and Homeostasis. Springer; Cham: 2018 |
|
Zhang S, Zhao J, Zhang Y, Zhang Y, Cai F, Wang L and Song W: Upregulation of MIF as a defense mechanism and a biomarker of Alzheimer's disease. Alzheimers Res Ther. 11:542019. View Article : Google Scholar : PubMed/NCBI |
|
Heinrichs D, Berres ML, Coeuru M, Knauel M, Nellen A, Fischer P, Philippeit C, Bucala R, Trautwein C, Wasmuth HE and Bernhagen J: Protective role of macrophage migration inhibitory factor in nonalcoholic steatohepatitis. FASEB J. 28:5136–5147. 2014. View Article : Google Scholar : PubMed/NCBI |
|
Bencová S: Transcriptomic analysis of cutaneous inflammatory biomarkers in a mouse model of small fiber neuropathy. Univerzita Karlova, Farmaceutická fakulta v Hradci Králové; 2018 |
|
Miller EJ, Li J, Leng L, McDonald C, Atsumi T, Bucala R and Young LH: Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature. 451:578–582. 2008. View Article : Google Scholar : PubMed/NCBI |
|
Shachar I: An essential MIF-CD74 signaling axis in kidney tubular regeneration, with prospects for precision medicine and pharmacological augmentation. Am J Physiol Renal Physiol. 313:F1084–F1086. 2017. View Article : Google Scholar : PubMed/NCBI |
|
Stoppe C, Averdunk L, Goetzenich A, Soppert J, Marlier A, Kraemer S, Vieten J, Coburn M, Kowark A, Kim BS, et al: The protective role of macrophage migration inhibitory factor in acute kidney injury after cardiac surgery. Sci Transl Med. 10:eaan48862018. View Article : Google Scholar : PubMed/NCBI |
|
Sneath RJS and Mangham DC: The normal structure and function of CD44 and its role in neoplasia. Mol Pathol. 51:191–200. 1998. View Article : Google Scholar |
|
Weng X, Maxwell-Warburton S, Hasib A, Ma L and Kang L: The membrane receptor CD44: Novel insights into metabolism. Trends Endocrinol Metab. 33:318–332. 2022. View Article : Google Scholar : PubMed/NCBI |
|
Noe JT and Mitchell RA: MIF-dependent control of tumor immunity. Front Immunol. 11:6099482020. View Article : Google Scholar : PubMed/NCBI |
|
Calandra T and Roger T: Macrophage migration inhibitory factor: A regulator of innate immunity. Nat Rev Immunol. 3:791–800. 2003. View Article : Google Scholar : PubMed/NCBI |
|
Das R, Koo MS, Kim BH, Jacob ST, Subbian S, Yao J, Leng L, Levy R, Murchison C, Burman WJ, et al: Macrophage migration inhibitory factor (MIF) is a critical mediator of the innate immune response to Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 110:E2997–E3006. 2013. View Article : Google Scholar : PubMed/NCBI |
|
Ruiz-Rosado Jde D, Olguín JE, Juárez-Avelar I, Saavedra R, Terrazas LI, Robledo-Avila FH, Vazquez-Mendoza A, Fernández J, Satoskar AR, Partida-Sánchez S and Rodriguez-Sosa M: MIF promotes classical activation and conversion of inflammatory Ly6C(high) monocytes into TipDCs during murine toxoplasmosis. Mediators Inflamm. 2016:91017622016.PubMed/NCBI |
|
Koga K, Kenessey A, Powell SR, Sison CP, Miller EJ and Ojamaa K: Macrophage migration inhibitory factor provides cardioprotection during ischemia/reperfusion by reducing oxidative stress. Antioxid Redox Signal. 14:1191–1202. 2011. View Article : Google Scholar |
|
Luedike P, Hendgen-Cotta UB, Sobierajski J, Totzeck M, Reeh M, Dewor M, Lue H, Krisp C, Wolters D, Kelm M, et al: Cardioprotection through S-nitros(yl)ation of macrophage migration inhibitory factor. Circulation. 125:1880–1889. 2012. View Article : Google Scholar : PubMed/NCBI |
|
Rassaf T, Weber C and Bernhagen J: Macrophage migration inhibitory factor in myocardial ischaemia/reperfusion injury. Cardiovasc Res. 102:321–328. 2014. View Article : Google Scholar : PubMed/NCBI |
|
Cherepkova OA, Lyutova EM, Eronina TB and Gurvits BY: Chaperone-like activity of macrophage migration inhibitory factor. Int J Biochem Cell Biol. 38:43–55. 2006. View Article : Google Scholar |
|
Israelson A, Ditsworth D, Sun S, Song S, Liang J, Hruska-Plochan M, McAlonis-Downes M, Abu-Hamad S, Zoltsman G, Shani T, et al: Macrophage migration inhibitory factor as a chaperone inhibiting accumulation of misfolded SOD1. Neuron. 86:218–232. 2015. View Article : Google Scholar : PubMed/NCBI |
|
Leyton-Jaimes MF, Benaim C, Abu-Hamad S, Kahn J, Guetta A, Bucala R and Israelson A: Endogenous macrophage migration inhibitory factor reduces the accumulation and toxicity of misfolded SOD1 in a mouse model of ALS. Proc Natl Acad Sci USA. 113:10198–10203. 2016. View Article : Google Scholar : PubMed/NCBI |
|
Apte RS, Sinha D, Mayhew E, Wistow GJ and Niederkorn JY: Cutting edge: Role of macrophage migration inhibitory factor in inhibiting NK cell activity and preserving immune privilege. J Immunol. 160:5693–5696. 1998. View Article : Google Scholar : PubMed/NCBI |
|
Ito T, Ito N, Saatoff M, Hashizume H, Fukamizu H, Nickoloff BJ, Takigawa M and Paus R: Maintenance of hair follicle immune privilege is linked to prevention of NK cell attack. J Invest Dermatol. 128:1196–1206. 2008. View Article : Google Scholar |
|
Matsuda A, Tagawa Y, Matsuda H and Nishihira A: Expression of macrophage migration inhibitory factor in corneal wound healing in rats. Invest Ophthalmol Vis Sci. 38:1555–1562. 1997.PubMed/NCBI |
|
Nishio Y, Minami A, Kato H, Kaneda K and Nishihira J: Identification of macrophage migration inhibitory factor (MIF) in rat peripheral nerves: Its possible involvement in nerve regeneration. Biochim Biophys Acta. 1453:74–82. 1998. View Article : Google Scholar |
|
Shimizu T, Nishihira J, Mizue Y, Nakamura H, Abe R, Watanabe H, Ohkawara A and Shimizu H: High macrophage migration inhibitory factor (MIF) serum levels associated with extended psoriasis. J Invest Dermatol. 116:989–990. 2001. View Article : Google Scholar : PubMed/NCBI |
|
Benigni F, Atsumi T, Calandra T, Metz C, Echtenacher B, Peng T and Bucala R: The proinflammatory mediator macrophage migration inhibitory factor induces glucose catabolism in muscle. J Clin Invest. 106:1291–1300. 2000. View Article : Google Scholar : PubMed/NCBI |
|
Stojanovic I, Saksida T and Stosic-Grujicic S: Beta cell function: The role of macrophage migration inhibitory factor. Immunol Res. 52:81–88. 2012. View Article : Google Scholar : PubMed/NCBI |
|
Bozza FA, Gomes RN, Japiassú AM, Soares M, Castro-Faria-Neto HC, Bozza PT and Bozza MT: Macrophage migration inhibitory factor levels correlate with fatal outcome in sepsis. Shock. 22:309–313. 2004. View Article : Google Scholar : PubMed/NCBI |
|
Kim HR, Kim KW, Jung HG, Yoon KS, Oh HJ, Cho M La and Lee SH: Macrophage migration inhibitory factor enhances osteoclastogenesis through upregulation of RANKL expression from fibroblast-like synoviocytes in patients with rheumatoid arthritis. Arthritis Res Ther. 13:E432011. View Article : Google Scholar |
|
Sanchez-Zamora Y, Terrazas LI, Vilches-Flores A, Leal E, Juárez I, Whitacre C, Kithcart A, Pruitt J, Sielecki T, Satoskar AR and Rodriguez-Sosa M: Macrophage migration inhibitory factor is a therapeutic target in treatment of non-insulin-dependent diabetes mellitus. FASEB J. 24:2583–2590. 2010. View Article : Google Scholar : PubMed/NCBI |
|
Donnelly SC, Hasleit C, Reid PT, Grant IS, Wallace WA, Metz CN, Bruce LJ and Bucala R: Regulatory role for macrophage migration inhibitory factor in acute respiratory distress syndrome. Nat Med. 3:320–323. 1997. View Article : Google Scholar : PubMed/NCBI |
|
Benedek G, Meza-Romero R, Jordan K, Zhang Y, Nguyen H, Kent G, Li J, Siu E, Frazer J, Piecychna M, et al: MIF and D-DT are potential disease severity modifiers in male MS subjects. Proc Natl Acad Sci USA. 114:E8421–E8429. 2017. View Article : Google Scholar : PubMed/NCBI |
|
Tu Y, Guo R, Li J, Wang S, Leng L, Deng J, Bucala R and Lu L: MiRNA regulation of MIF in SLE and attenuation of murine lupus nephritis with miR-654. Front Immunol. 10:22292019. View Article : Google Scholar : PubMed/NCBI |
|
Bezdek S, Leng L, Busch H, Mousavi S, Rades D, Dahlke M, Zillikens D, Bucala R and Sadik CD: Macrophage migration inhibitory factor (MIF) drives murine psoriasiform dermatitis. Front Immunol. 9:22622018. View Article : Google Scholar : PubMed/NCBI |
|
Rajabi F, Amoli MM, Robati RM, Almasi-nasrabadi M and Jabalameli N: Macrophage migration inhibitory factor polymorphism (rs755622) in alopecia areata: A possible role in disease prevention. Arch Dermatol Res. 311:589–594. 2019. View Article : Google Scholar : PubMed/NCBI |
|
Chuang YC, Chen HR and Yeh TM: Pathogenic roles of macrophage migration inhibitory factor during dengue virus infection. Mediators Inflamm. 2015:5470942015. View Article : Google Scholar : PubMed/NCBI |
|
Mohla S: Tumor microenvironment. J Cell Biochem. 101:801–804. 2007. View Article : Google Scholar : PubMed/NCBI |
|
Wang Y and Dong X: MIF improves immune microenvironment of Lewis lung cancer brain metastases after radiotherapy via reducing M2 macrophages. J Clin Oncol. 40(16 Suppl): e210262022. View Article : Google Scholar |
|
Mantovani A, Allavena P, Sica A and Balkwill F: Cancer-related inflammation. Nature. 454:436–444. 2008. View Article : Google Scholar : PubMed/NCBI |
|
Balogh KN, Templeton DJ and Cross JV: Macrophage migration inhibitory factor protects cancer cells from immunogenic cell death and impairs anti-tumor immune responses. PLoS One. 13:e01977022018. View Article : Google Scholar : PubMed/NCBI |
|
Faucheux L, Grandclaudon M, Perrot-Dockès M, Sirven P, Berger F, Hamy AS, Fourchotte V, Vincent-Salomon A, Mechta-Grigoriou F, Reyal F, et al: A multivariate Th17 metagene for prognostic stratification in T cell non-inflamed triple negative breast cancer. Oncoimmunology. 8:e16241302019. View Article : Google Scholar : PubMed/NCBI |
|
Hanahan D: Hallmarks of cancer: New dimensions. Cancer Discov. 12:31–46. 2022. View Article : Google Scholar : PubMed/NCBI |
|
Hanahan D and Weinberg RA: Hallmarks of cancer: The next generation. Cell. 144:646–674. 2011. View Article : Google Scholar : PubMed/NCBI |
|
Hanahan D and Weinberg RA: The hallmarks of cancer. Cell. 100:57–70. 2000. View Article : Google Scholar : PubMed/NCBI |
|
Hashemi Goradel N, Najafi M, Salehi E, Farhood B and Mortezaee K: Cyclooxygenase-2 in cancer: A review. J Cell Physiol. 234:5683–5699. 2019. View Article : Google Scholar |
|
Jäger B, Klatt D, Plappert L, Golpon H, Lienenklaus S, Barbosa PD, Schambach A and Prasse A: CXCR4/MIF axis amplifies tumor growth and epithelial-mesenchymal interaction in non-small cell lung cancer. Cell Signal. 73:1096722020. View Article : Google Scholar : PubMed/NCBI |
|
Cotzomi-Ortega I, Nieto-Yañez O, Juárez-Avelar I, Rojas-Sanchez G, Montes-Alvarado JB, Reyes-Leyva J, Aguilar-Alonso P, Rodriguez-Sosa M and Maycotte P: Autophagy inhibition in breast cancer cells induces ROS-mediated MIF expression and M1 macrophage polarization. Cell Signal. 86:1100752021. View Article : Google Scholar : PubMed/NCBI |
|
Cheng B, Wang Q, Song Y, Liu Y, Liu Y, Yang S, Li D, Zhang Y and Zhu C: MIF inhibitor, ISO-1, attenuates human pancreatic cancer cell proliferation, migration and invasion in vitro, and suppresses xenograft tumour growth in vivo. Sci Rep. 10:67412020. View Article : Google Scholar : PubMed/NCBI |
|
Vaupel P and Mayer A: Hypoxia in tumors: Pathogenesis-related classification, characterization of hypoxia subtypes, and associated biological and clinical implications. Adv Exp Med Biol. 812:19–24. 2014. View Article : Google Scholar : PubMed/NCBI |
|
Avalos-Navarro G, Muñoz-Valle JF, Daneri-Navarro A, Quintero-Ramos A, Franco-Topete RA, Morán-Mendoza AJ, Oceguera-Villanueva A, Bautista-Herrera LA, Topete-Camacho A and Del Toro-Arreola A: Circulating soluble levels of MIF in women with breast cancer in the molecular subtypes: Relationship with Th17 cytokine profile. Clin Exp Med. 19:385–391. 2019. View Article : Google Scholar : PubMed/NCBI |
|
Klemke L, De Oliveira T, Witt D, Winkler N, Bohnenberger H, Bucala R, Conradi LC and Schulz-Heddergott R: Hsp90-stabilized MIF supports tumor progression via macrophage recruitment and angiogenesis in colorectal cancer. Cell Death Dis. 12:1552021. View Article : Google Scholar : PubMed/NCBI |
|
Cotzomi-Ortega I, Rosas-Cruz A, Ramírez-Ramírez D, Reyes-Leyva J, Rodriguez-Sosa M, Aguilar-Alonso P and Maycotte P: Autophagy inhibition induces the secretion of macrophage migration inhibitory factor (MIF) with autocrine and paracrine effects on the promotion of malignancy in breast cancer. Biology (Basel). 9:202020.PubMed/NCBI |
|
Rajendran G, Woolbright BL, Abbott E, Martin A, Dennis K and Taylor JA: Abstract 5150: MIF-2 in bladder cancer: Potential therapeutic target. Cancer Res. 80(16 Suppl): S51502020. View Article : Google Scholar |
|
Richard V, Kindt N and Saussez S: Macrophage migration inhibitory factor involvement in breast cancer (Review). Int J Oncol. 47:1627–1633. 2015. View Article : Google Scholar : PubMed/NCBI |
|
Schabath MB and Cote ML: Cancer progress and priorities: Lung cancer. Cancer Epidemiol Biomarkers Prev. 28:1563–1579. 2019. View Article : Google Scholar : PubMed/NCBI |
|
Guo Y, Hou J, Luo Y and Wang D: Functional disruption of macrophage migration inhibitory factor (MIF) suppresses proliferation of human H460 lung cancer cells by caspase-dependent apoptosis. Cancer Cell Int. 13:282013. View Article : Google Scholar : PubMed/NCBI |
|
Gámez-Pozo A, Sánchez-Navarro I, Calvo E, Agulló-Ortuño MT, López-Vacas R, Díaz E, Camafeita E, Nistal M, Madero R, Espinosa E, et al: PTRF/cavin-1 and MIF proteins are identified as non-small cell lung cancer biomarkers by label-free proteomics. PLoS One. 7:e337522012. View Article : Google Scholar : PubMed/NCBI |
|
Wang WM and Liu JC: Effect and molecular mechanism of mir-146a on proliferation of lung cancer cells by targeting and regulating MIF gene. Asian Pac J Trop Med. 9:806–811. 2016. View Article : Google Scholar : PubMed/NCBI |
|
Huang WC, Kuo KT, Wang CH, Yeh CT and Wang Y: Cisplatin resistant lung cancer cells promoted M2 polarization of tumor-associated macrophages via the Src/CD155/MIF functional pathway. J Exp Clin Cancer Res. 38:1802019. View Article : Google Scholar : PubMed/NCBI |
|
Mawhinney L, Armstrong ME, O'Reilly C, Bucala R, Leng L, Fingerle-Rowson G, Fayne D, Keane MP, Tynan A, Maher L, et al: Macrophage migration inhibitory factor (MIF) enzymatic activity and lung cancer. Mol Med. 20:729–735. 2015. View Article : Google Scholar : PubMed/NCBI |
|
Liu L, Wang J, Wang Y, Chen L, Peng L, Bin Y, Ding P, Zhang R, Tong F and Dong X: Blocking the MIF-CD74 axis augments radiotherapy efficacy for brain metastasis in NSCLC via synergistically promoting microglia M1 polarization. J Exp Clin Cancer Res. 43:1282024. View Article : Google Scholar : PubMed/NCBI |
|
Xiao Z, Song S, Chen D, van Merkerk R, van der Wouden PE, Cool RH, Quax WJ, Poelarends GJ, Melgert BN and Dekker FJ: Proteolysis targeting chimera (PROTAC) for macrophage migration inhibitory factor (MIF) has anti-proliferative activity in lung cancer cells. Angew Chem Int Ed Engl. 60:17514–17521. 2021. View Article : Google Scholar : PubMed/NCBI |
|
Gordon-Weeks AN, Lim SY, Yuzhalin AE, Jones K and Muschel R: Macrophage migration inhibitory factor: A key cytokine and therapeutic target in colon cancer. Cytokine Growth Factor Rev. 26:451–461. 2015. View Article : Google Scholar : PubMed/NCBI |
|
Shin HN, Moon HH and Ku JL: Stromal cell-derived factor-1α and macrophage migration-inhibitory factor induce metastatic behavior in CXCR4-expressing colon cancer cells. Int J Mol Med. 30:1537–1543. 2012. View Article : Google Scholar : PubMed/NCBI |
|
Lechien JR, Nassri A, Kindt N, Brown DN, Journe F and Saussez S: Role of macrophage migration inhibitory factor in head and neck cancer and novel therapeutic targets: A systematic review. Head Neck. 39:2573–2584. 2017. View Article : Google Scholar : PubMed/NCBI |
|
Grieb G, Merk M, Bernhagen J and Bucala R: Macrophage migration inhibitory factor (MIF): A promising biomarker. Drug News Perspect. 23:257–264. 2010. View Article : Google Scholar : PubMed/NCBI |
|
Zarrin AA, Bao K, Lupardus P and Vucic D: Kinase inhibition in autoimmunity and inflammation. Nat Rev Drug Discov. 20:39–63. 2021. View Article : Google Scholar |
|
Eaton WW, Rose NR, Kalaydjian A, Pedersen MG and Mortensen PB: Epidemiology of autoimmune diseases in Denmark. J Autoimmun. 29:1–9. 2007. View Article : Google Scholar : PubMed/NCBI |
|
Jacobson DL, Gange SJ, Rose NR and Graham NM: Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin Immunol Immunopathol. 84:223–243. 1997. View Article : Google Scholar : PubMed/NCBI |
|
Wang L, Wang FS and Gershwin ME: Human autoimmune diseases: A comprehensive update. J Intern Med. 278:369–395. 2015. View Article : Google Scholar : PubMed/NCBI |
|
Rosenblum MD, Remedios KA and Abbas AK: Mechanisms of human autoimmunity. J Clin Invest. 125:2228–2233. 2015. View Article : Google Scholar : PubMed/NCBI |
|
Günther S, Fagone P, Jalce G, Atanasov AG, Guignabert C and Nicoletti F: Role of MIF and D-DT in immune-inflammatory, autoimmune, and chronic respiratory diseases: From pathogenic factors to therapeutic targets. Drug Discov Today. 24:428–439. 2019. View Article : Google Scholar |
|
Brown EM, Kenny DJ and Xavier RJ: Gut microbiota regulation of T cells during inflammation and autoimmunity. Annu Rev Immunol. 37:599–624. 2019. View Article : Google Scholar : PubMed/NCBI |
|
Connelly KL, Kandane-Rathnayake R, Hoi A, Nikpour M and Morand EF: Association of MIF, but not type I interferon-induced chemokines, with increased disease activity in Asian patients with systemic lupus erythematosus. Sci Rep. 6:299092016. View Article : Google Scholar : PubMed/NCBI |
|
Feng X, Chen W, Xiao L, Gu F, Huang J, Tsao BP and Sun L: Artesunate inhibits type I interferon-induced production of macrophage migration inhibitory factor in patients with systemic lupus erythematosus. Lupus. 26:62–72. 2017. View Article : Google Scholar |
|
Fouda ME, El-shimi OS, Mahgoub MY, Abdelrahman SN and Abdelrahman AM: Evaluation of urinary and serum macrophage migration inhibition factor in a group of systemic lupus erythematosus Egyptian patients. Benha Med J. 39:164–178. 2022. |
|
Vincent FB, Slavin L, Hoi AY, Kitching AR, Mackay F, Harris J, Kandane-Rathnayake R and Morand EF: Analysis of urinary macrophage migration inhibitory factor in systemic lupus erythematosus. Lupus Sci Med. 5:e0002772018. View Article : Google Scholar : PubMed/NCBI |
|
Beltrán-Ramírez A, Muñoz-Valle JF, Gamez-Nava JI, Saldaña-Cruz AM, Gonzalez-Lopez L, Padilla-Ortega A, Arias-García FI, Sánchez-Zuno GA, Nava-Valdivia CA, Ponce-Guarneros JM, et al: Steroid resistance associated with high MIF and P-gp serum levels in SLE patients. Molecules. 27:67412022. View Article : Google Scholar : PubMed/NCBI |
|
Nim HT, Connelly K, Vincent FB, Petitjean F, Hoi A, Koelmeyer R, Boyd SE and Morand EF: Novel methods of incorporating time in longitudinal multivariate analysis reveals hidden associations with disease activity in systemic lupus erythematosus. Front Immunol. 10:16492019. View Article : Google Scholar : PubMed/NCBI |
|
De la Cruz-Mosso U, García-Iglesias T, Bucala R, Estrada-García I, González-López L, Cerpa-Cruz S, Parra-Rojas I, Gámez-Nava JI, Pérez-Guerrero EE and Muñoz-Valle JF: MIF promotes a differential Th1/Th2/Th17 inflammatory response in human primary cell cultures: Predominance of Th17 cytokine profile in PBMC from healthy subjects and increase of IL-6 and TNF-α in PBMC from active SLE patients. Cell Immunol. 324:42–49. 2018. View Article : Google Scholar : PubMed/NCBI |
|
Wallace DJ, Wegener WA, Horne H and Goldenberg DM: CT-01 Phase IB study of IMMU-115 (humanised ANTI-CD74 antibody) targeting antigen presenting cells in patients with systemic lupus erythematosus (SLE). Lupus Sci Med. 3:A37–A38. 2016. |
|
Bautista-Herrera LA, De la Cruz-Mosso U, Román-Fernández IV, Parra-Rojas I, Soñanez-Organis JG, Hernández-Bello J, Morales-Zambrano RA, Villanueva-Quintero GD and Muñoz-Valle JF: A potential inflammatory role of IL-31 in psoriatic arthritis: A correlation with Th17 cytokine profile. Int J Immunopathol Pharmacol. 34:20587384209071862020. View Article : Google Scholar : PubMed/NCBI |
|
Morales-Zambrano R, Bautista-Herrera LA, De La Cruz-Mosso U, Villanueva-Quintero GD, Padilla-Gutiérrez JR, Valle Y, Parra-Rojas I, Rangel-Villalobos H, Gutiérrez-Ureña SR and Muñoz-Valle JF: Macrophage migration inhibitory factor (MIF) promoter polymorphisms (-794 CATT5-8 and -173 G>C): association with MIF and TNFα in psoriatic arthritis. Int J Clin Exp Med. 7:2605–2614. 2014. |
|
Schneeberger EE, Citera G, Rodríguez Gil G, Granel A, Arturi A, Rosemffet GM, Maldonado Cocco JA, Berman A, Spindler A and Morales VH: Clinical and immunogenetic characterization in psoriatic arthritis patients. Clin Rheumatol. 34:1413–1418. 2015. View Article : Google Scholar |
|
Barnas JL and Ritchlin CT: Etiology and pathogenesis of psoriatic arthritis. Rheum Dis Clin North Am. 41:643–663. 2015. View Article : Google Scholar : PubMed/NCBI |
|
Veale DJ and Fearon U: The pathogenesis of psoriatic arthritis. Lancet. 391:2273–2284. 2018. View Article : Google Scholar : PubMed/NCBI |
|
Steinhoff M, Meinhardt A, Steinhoff A, Gemsa D, Bucala R and Bacher M: Evidence for a role of macrophage migration inhibitory factor in psoriatic skin disease. Br J Dermatol. 141:1061–1066. 1999. View Article : Google Scholar : PubMed/NCBI |
|
Chhabra S, Banerjee N, Narang T, Sood S, Bishnoi A, Goel S, Bansal F, Singh S, Priyanka K, Minz RW and Dogra S: Single-nucleotide polymorphism and haplotype analysis of macrophage migration inhibitory factor gene and its correlation with serum macrophage migration inhibitory factor levels in North Indian psoriatic patients with moderate disease severity: A cross-sectional study. Indian J Dermatol Venereol Leprol. 89:247–253. 2023. View Article : Google Scholar |
|
Donn RP, Plant D, Jury F, Richards HL, Worthington J, Ray DW and Griffiths CEM: Macrophage migration inhibitory factor gene polymorphism is associated with psoriasis. J Invest Dermatol. 123:484–487. 2004. View Article : Google Scholar : PubMed/NCBI |
|
Dobson R and Giovannoni G: Multiple sclerosis-a review. Eur J Neurol. 26:27–40. 2019. View Article : Google Scholar |
|
Cavalli E, Mazzon E, Basile MS, Mangano K, Di Marco R, Bramanti P, Nicoletti F, Fagone P and 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). 55:6672019. View Article : Google Scholar |
|
Wanleenuwat P and Iwanowski P: Role of B cells and antibodies in multiple sclerosis. Mult Scler Relat Disord. 36:1014162019. View Article : Google Scholar : PubMed/NCBI |
|
Guan D, Li Y, Cui Y, Zhao H, Dong N, Wang K, Ren D, Song T, Wang X, Jin S, et al: 5-HMF attenuates inflammation and demyelination in experimental autoimmune encephalomyelitis mice by inhibiting the MIF-CD74 interaction. Acta Biochim Biophys Sin (Shanghai). 55:1222–1233. 2023. View Article : Google Scholar : PubMed/NCBI |
|
Hjæresen S, Sejbaek T, Axelsson M, Mortensen SK, Vinsløv-Jensen H, Pihl-Jensen G, Novakova L, Pedersen CB, Halle B, Poulsen FR, et al: MIF in the cerebrospinal fluid is decreased during relapsing-remitting while increased in secondary progressive multiple sclerosis. J Neurol Sci. 439:1203202022. View Article : Google Scholar : PubMed/NCBI |
|
Rijvers L, Melief MJ, van der Vuurst de Vries RM, Stéphant M, van Langelaar J, Wierenga-Wolf AF, Hogervorst JM, Geurts-Moespot AJ, Sweep FCGJ, Hintzen RQ and van Luijn MM: The macrophage migration inhibitory factor pathway in human B cells is tightly controlled and dysregulated in multiple sclerosis. Eur J Immunol. 48:1861–1871. 2018. View Article : Google Scholar : PubMed/NCBI |
|
Castañeda-Moreno VA, De la Cruz-Mosso U, Torres-Carrillo N, Macías-Islas MA, Padilla-De la Torre O, Mireles-Ramírez MA, González-Pérez O, Ruiz-Sandoval JL, Huerta M, Trujillo X, et al: MIF functional polymorphisms (-794 CATT5-8 and -173 G>C) are associated with MIF serum levels, severity and progression in male multiple sclerosis from western Mexican population. J Neuroimmunol. 320:117–124. 2018. View Article : Google Scholar |
|
Vandenbark AA, Meza-Romero R, Benedek G and Offner H: A novel neurotherapeutic for multiple sclerosis, ischemic injury, methamphetamine addiction, and traumatic brain injury. J Neuroinflammation. 16:142019. View Article : Google Scholar : PubMed/NCBI |
|
Bloom J, Metz C, Nalawade S, Casabar J, Cheng KF, He M, Sherry B, Coleman T, Forsthuber T and Al-Abed Y: Identification of iguratimod as an inhibitor of macrophage migration inhibitory factor (MIF) with steroid-sparing potential. J Biol Chem. 291:26502–26514. 2016. View Article : Google Scholar : PubMed/NCBI |
|
Fox RJ, Coffey CS, Conwit R, Cudkowicz ME, Gleason T, Goodman A, Klawiter EC, Matsuda K, McGovern M, Naismith RT, et al: Phase 2 trial of ibudilast in progressive multiple sclerosis. N Engl J Med. 379:846–855. 2018. View Article : Google Scholar : PubMed/NCBI |
|
Pawlitzki M, Sweeney-Reed CM, Meuth SG, Reinhold D and Neumann J: CSF macrophage migration inhibitory factor levels did not predict steroid treatment response after optic neuritis in patients with multiple sclerosis. PLoS One. 13:e02077262018. View Article : Google Scholar : PubMed/NCBI |
|
Eldesouky F, Ibrahim AM and Sharaf SM: Macrophage migration inhibitory factor in alopecia areata and vitiligo: A case-controlled serological study. J Clin Aesthet Dermatol. 13:24–27. 2020. |
|
Sandoval DA and Plaza NE: Collapse of the immunoprivilege and emotional stress in alopecia areata. Rev Argent Dermatol. 101:41–50. 2020. |
|
Oh HA, Kwak J, Kim BJ, Jin HJ, Park WS, Choi SJ, Oh W and Um S: Migration inhibitory factor in conditioned medium from human umbilical cord blood-derived mesenchymal stromal cells stimulates hair growth. Cells. 9:13442020. View Article : Google Scholar : PubMed/NCBI |
|
Garcia-Orozco A, Martinez-Magaña IA, Riera-Leal A, Muñoz-Valle JF, Martinez-Guzman MA, Quiñones-Venegas R, Sánchez-Zuno GA and Fafutis-Morris M: Macrophage inhibitory factor (MIF) gene polymorphisms are associated with disease susceptibility and with circulating MIF levels in active non-segmental vitiligo in patients from western Mexico. Mol Genet Genomic Med. 8:e14162020. View Article : Google Scholar : PubMed/NCBI |
|
Ibrahim HM, Abd El-Aziz Nada EED, Abdel-Hamid Ali S, Hegazy EM and Hassan MH: Macrophage migration inhibitory factor in vitiligo: Pathogenesis and potential therapeutic aspects. Asian J Biochem Genet Mol Biol. 8:8–24. 2021. View Article : Google Scholar |
|
Solimani F, Meier K and Ghoreschi K: Emerging topical and systemic JAK inhibitors in dermatology. Front Immunol. 10:28472019. View Article : Google Scholar : PubMed/NCBI |
|
Chakraborty A, Thulasamma S, Kumar GS, Pallapolu P, Lahari K, Rafeeqi T, Husain G, Jabeen F, Javed G, Waheed MA and Kazmi MH: Expression levels of MIF, NLRP1 and FOXP3 genes along with biomarker levels in patients with active form of non-segmental generalized vitiligo: A study in South Indian population. Songklanakarin J Sci Technol. 44:353–360. 2022. |
|
Wang D, Min S, Lin X and Jiang G: Association among MIF, IFIH1, and IL6 gene polymorphisms and non-segmental vitiligo in a chinese han population. Clin Cosmet Investig Dermatol. 15:1597–1609. 2022. View Article : Google Scholar : PubMed/NCBI |
|
ElGhareeb MI, El Mokadem S, El Sayed B and Khalifa N: Soluble CD27 and MIF as possible serum biomarkers of vitiligo activity in Egyptian patients in Sharkia governorate. Dermatol Reports. 11:82652019. |
|
Bae SC and Lee YH: Associations between circulating macrophage migration inhibitory factor (MIF) levels and rheumatoid arthritis, and between MIF gene polymorphisms and disease susceptibility: A meta-analysis. Postgrad Med J. 94:109–115. 2018. View Article : Google Scholar |
|
Han Y, Wang J, Li S, Li Y, Zhang Y, Zhang R, Zhang Y, Fan H, Shi H, Pan J, et al: Isopsoralen ameliorates rheumatoid arthritis by targeting MIF. Arthritis Res Ther. 23:2432021. View Article : Google Scholar : PubMed/NCBI |
|
Taghadosi M, Adib M, Jamshidi A, Mahmoudi M and Farhadi E: The p53 status in rheumatoid arthritis with focus on fibroblast-like synoviocytes. Immunol Res. 69:225–238. 2021. View Article : Google Scholar : PubMed/NCBI |
|
Zhang Z, Zhang R, Li L, Zhu L, Gao S, Lu Q, Gu Y, Zhang Y, Yang H, Hou T, et al: Macrophage migration inhibitory factor (MIF) inhibitor, Z-590 suppresses cartilage destruction in adjuvant-induced arthritis via inhibition of macrophage inflammatory activation. Immunopharmacol Immunotoxicol. 40:149–157. 2018. View Article : Google Scholar : PubMed/NCBI |
|
Södergren A, Kar p K, Bengtsson C, Möller B, Rantapää-Dahlqvist S and Wållberg-Jonsson S: Biomarkers associated with cardiovascular disease in patients with early rheumatoid arthritis. PLoS One. 14:e02205312019. View Article : Google Scholar : PubMed/NCBI |
|
Santoscoy-Ascencio G, Baños-Hernández CJ, Navarro-Zarza JE, Hernández-Bello J, Bucala R, López-Quintero A, Valdés-Alvarado E, Parra-Rojas I, Illades-Aguiar B and Muñoz-Valle JF: Macrophage migration inhibitory factor promoter polymorphisms are associated with disease activity in rheumatoid arthritis patients from Southern Mexico. Mol Genet Genomic Med. 8:e10372020. View Article : Google Scholar : |
|
Hernández-Palma LA, García-Arellano S, Bucala R, Llamas-Covarrubias MA, De la Cruz-Mosso U, Oregon-Romero E, Cerpa-Cruz S, Parra-Rojas I, Plascencia-Hernández A and Muñoz-Valle JF: Functional MIF promoter haplotypes modulate Th17-related cytokine expression in peripheral blood mononuclear cells from control subjects and rheumatoid arthritis patients. Cytokine. 115:89–96. 2019. View Article : Google Scholar |
|
García-Arellano S, Hernández-Palma LA, Cerpa-Cruz S, Sánchez-Zuno GA, Herrera-Godina MG and Muñoz-Valle JF: The novel role of MIF in the secretion of IL-25, IL-31, and IL-33 from PBMC of patients with rheumatoid arthritis. Molecules. 26:49682021. View Article : Google Scholar : PubMed/NCBI |
|
Sogkas G, Klose K, Baerlecken N, Schweikhard E, Matthias T, Kniesch K, Schmidt RE and Witte T: CD74 is a T cell antigen in spondyloarthritis. Clin Exp Rheumatol. 38:195–202. 2020. View Article : Google Scholar |
|
Sánchez-Zuno GA, Bucala R, Hernández-Bello J, Román-Fernández IV, García-Chagollán M, Nicoletti F, Matuz-Flores MG, García-Arellano S, Esparza-Michel JA, Cerpa-Cruz S, et al: Canonical (CD74/CD44) and non-canonical (CXCR2, 4 and 7) MIF receptors are differentially expressed in rheumatoid arthritis patients evaluated by DAS28-ESR. J Clin Med. 11:1202021. View Article : Google Scholar |
|
Valdez CN, Sánchez-Zuno GA, Bucala R and Tran TT: Macrophage migration inhibitory factor (MIF) and D-dopachrome tautomerase (DDT): Pathways to tumorigenesis and therapeutic opportunities. Int J Mol Sci. 25:48492024. View Article : Google Scholar : PubMed/NCBI |
|
de Azevedo RA, Shoshan E, Whang S, Markel G, Jaiswal AR, Liu A, Curran MA, Travassos LR and Bar-Eli M: MIF inhibition as a strategy for overcoming resistance to immune checkpoint blockade therapy in melanoma. Oncoimmunology. 9:18469152020. View Article : Google Scholar : PubMed/NCBI |
|
Mora Barthelmess R, Stijlemans B and Van Ginderachter JA: Hallmarks of cancer affected by the MIF cytokine family. Cancers (Basel). 15:3952023. View Article : Google Scholar : PubMed/NCBI |
|
Valdez CN, Athziri Sánchez-Zuno G, Osmani L, Ibrahim W, Galan A, Bacchiocchi A, Halaban R, Kulkarni RP, Kang I, Bucala R and Tran T: Prognostic and therapeutic insights into MIF, DDT, and CD74 in melanoma. Oncotarget. 15:507–520. 2024. View Article : Google Scholar : PubMed/NCBI |
|
Sánchez-Zuno GA, Valdez CN, Osmani L, Kang I, Bucala R and Tran T: 571 Dual inhibition of MIF and DDT enhances the efficacy of anti-PD-1 therapy in murine melanoma. J Immunother Cancer. 12:A6512024. |
|
Bloom J, Pantouris G, He M, Aljabari B, Mishra L, Manjula R, Parkins A, Lolis EJ and Al-Abed Y: Iguratimod, an allosteric inhibitor of macrophage migration inhibitory factor (MIF), prevents mortality and oxidative stress in a murine model of acetaminophen overdose. Mol Med. 30:432024. View Article : Google Scholar : PubMed/NCBI |
|
Jiang H, Gao H, Wang Q, Wang M and Wu B: Molecular mechanisms and clinical application of iguratimod: A review. Biomed Pharmacother. 122:1097042020. View Article : Google Scholar : PubMed/NCBI |
|
Long Z, Zeng L, He Q, Yang K, Xiang W, Ren X, Deng Y and Chen H: Research progress on the clinical application and mechanism of iguratimod in the treatment of autoimmune diseases and rheumatic diseases. Front Immunol. 14:11506612023. View Article : Google Scholar : PubMed/NCBI |
|
Efferth T and Oesch F: The immunosuppressive activity of artemisinin-type drugs towards inflammatory and autoimmune diseases. Med Res Rev. 41:3023–3061. 2021. View Article : Google Scholar : PubMed/NCBI |
|
Ruwizhi N, Maseko RB and Aderibigbe BA: Recent advances in the therapeutic efficacy of artesunate. Pharmaceutics. 14:5042022. View Article : Google Scholar : PubMed/NCBI |
|
Guo S, Zhao Y, Yuan Y, Liao Y, Jiang X, Wang L, Lu W and Shi J: Progress in the development of macrophage migration inhibitory factor small-molecule inhibitors. Eur J Med Chem. 286:1172802025. View Article : Google Scholar : PubMed/NCBI |
|
Chen D, Zhao C, Zhang J, Knol CWJ, Osipyan A, Majerníková N, Chen T, Xiao Z, Adriana J and Griffith AJ: Small molecule MIF modulation enhances ferroptosis by impairing DNA repair mechanisms. Adv Sci (Weinh). 11:e24039632024. View Article : Google Scholar : PubMed/NCBI |
|
Li J, Leng L, Pantouris G, Manjula R, Piecychna M, Abriola L, Hu B, Lolis E, Armstrong ME, Donnelly SC and Bucala R: A small-molecule allele-selective transcriptional inhibitor of the MIF immune susceptibility locus. J Biol Chem. 300:1074432024. View Article : Google Scholar : PubMed/NCBI |
|
Sanchez-Zuno GA, Caulfield J, Leng L, Zhang L, Jilaveanu L, Kluger H, Bucala R and Tran T: 830 Inhibition of macrophage migration inhibitory factor (MIF) to overcome immune checkpoint resistance in melanoma. J Immunother Cancer. 11(Suppl 1): S9292023. |