Macrophage migration inhibitory factor modulates cytokine expression in the trophoblast cell line HTR-8/SVneo
Milica Jovanović Krivokuća A C * , Ivana Stefanoska A * , Aleksandra Vilotić A , Danica Ćujić A , Svetlana Vrzić Petronijević B and Ljiljana Vićovac AA Laboratory for Biology of Reproduction, Institute for the Application of Nuclear Energy (INEP), University of Belgrade, Banatska 31b, 11080 Belgrade, Serbia.
B Clinic of Obstetrics and Gynecology, Clinical Center of Serbia, Koste Todorovića 26, 11000 Belgrade, Serbia.
C Corresponding author. Email: milicaj@inep.co.rs
Reproduction, Fertility and Development 32(18) 1326-1337 https://doi.org/10.1071/RD20138
Submitted: 27 May 2020 Accepted: 26 October 2020 Published: 16 December 2020
Abstract
Extravillous trophoblasts are specific placental cells that invade the uterine stroma and spiral arteries modifying and adjusting them to pregnancy. Many pregnancy pathologies are associated with impairment of this process, including preeclampsia and intrauterine growth restriction, among others. Macrophage migration inhibitory factor (MIF) is a pleiotropic cytokine that is abundant at the fetomaternal interface. Previous results from our group showed that MIF participates in trophoblast invasion and modulates the expression of molecules known to mediate stromal and endovascular trophoblast invasion. In this study we investigated the possibility that MIF could act as a regulator of cytokines known to modulate trophoblast invasion using the normal extravillous trophoblast-derived cell line HTR-8/SVneo. Expression of trophoblast MIF was attenuated by MIF mRNA-specific small interfering RNAs. Cytokine expression was assessed at the mRNA and protein levels using real-time quantitative polymerase chain reaction and flow cytometry respectively. Knockdown of MIF led to a significant decrease in mRNA for IL-1β (IL1B) and IL-8 (CXCL8) and interleukin (IL)-8 protein. The addition of recombinant human MIF to cell culture medium increased IL-6 after 24 h treatment and IL-6 and IL-8 after 72 h treatment. Cell viability was not affected by MIF silencing or rhMIF treatment. The results of this study imply that at least some of the effects of MIF on trophoblast invasion could be mediated through autocrine or paracrine modulation of trophoblast cytokine production.
Keywords: cytokines, HTR-8/SVneo, macrophage migration inhibitory factor (MIF), trophoblast.
References
Ander, S. E., Diamond, M. S., and Coyne, C. B. (2019). Immune responses at the maternal–fetal interface. Sci. Immunol. 4, eaat6114.| Immune responses at the maternal–fetal interface.Crossref | GoogleScholarGoogle Scholar | 30635356PubMed |
Anton, L., Brown, A. G., Parry, S., and Elovitz, M. A. (2012). Lipopolysaccharide induces cytokine production and decreases extravillous trophoblast invasion through a mitogen-activated protein kinase-mediated pathway: possible mechanisms of first trimester placental dysfunction. Hum. Reprod. 27, 61–72.
| Lipopolysaccharide induces cytokine production and decreases extravillous trophoblast invasion through a mitogen-activated protein kinase-mediated pathway: possible mechanisms of first trimester placental dysfunction.Crossref | GoogleScholarGoogle Scholar | 22052387PubMed |
Bacher, M., Metz, C. N., Calandra, T., Mayer, K., Chesney, J., Lohoff, M., Gemsa, D., Donnelly, T., and Bucala, R. (1996). An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc. Natl Acad. Sci. USA 93, 7849–7854.
| An essential regulatory role for macrophage migration inhibitory factor in T-cell activation.Crossref | GoogleScholarGoogle Scholar | 8755565PubMed |
Bernhagen, J., Calandra, T., Mitchell, R. A., Martin, S. B., Tracey, K. J., Voelter, W., Manogue, K. R., Cerami, A., and Bucala, R. (1993). MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 365, 756–759.
| MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia.Crossref | GoogleScholarGoogle Scholar | 8413654PubMed |
Bernhagen, J., Krohn, R., Lue, H., Gregory, J. L., Zernecke, A., Koenen, R. R., Dewor, M., Georgiev, I., Schober, A., Leng, L., Kooistra, T., Fingerle-Rowson, G., Ghezzi, P., Kleemann, R., McColl, S. R., Bucala, R., Hickey, M. J., and Weber, C. (2007). MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat. Med. 13, 587–596.
| MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment.Crossref | GoogleScholarGoogle Scholar | 17435771PubMed |
Bevilacqua, E., Paulesu, L., Ferro, E. A., Ietta, F., Faria, M. R., Lorenzon, A. R., Costa, A. F., and Martucci, M. (2014). Review: putative roles for the macrophage migratory inhibitory factor at the maternal fetal interface. Placenta 35, S51–S56.
| Review: putative roles for the macrophage migratory inhibitory factor at the maternal fetal interface.Crossref | GoogleScholarGoogle Scholar | 24215782PubMed |
Bifulco, C., McDaniel, K., Leng, L., and Bucala, R. (2008). Tumor growth-promoting properties of macrophage migration inhibitory factor. Curr. Pharm. Des. 14, 3790–3801.
| Tumor growth-promoting properties of macrophage migration inhibitory factor.Crossref | GoogleScholarGoogle Scholar | 19128232PubMed |
Bozza, M., Satoskar, A. R., Lin, G., Lu, B., Humbles, A. A., Gerard, C., and David, J. R. (1999). Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J. Exp. Med. 189, 341–346.
| Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis.Crossref | GoogleScholarGoogle Scholar | 9892616PubMed |
Bucala, R., and Donnelly, S. C. (2007). Macrophage migration inhibitory factor: a probable link between inflammation and cancer. Immunity 26, 281–285.
| Macrophage migration inhibitory factor: a probable link between inflammation and cancer.Crossref | GoogleScholarGoogle Scholar | 17376392PubMed |
Bucala, R., and Lolis, E. (2005). Macrophage migration inhibitory factor: a critical component of autoimmune inflammatory diseases. Drug News Perspect. 18, 417–426.
| Macrophage migration inhibitory factor: a critical component of autoimmune inflammatory diseases.Crossref | GoogleScholarGoogle Scholar | 16362080PubMed |
Burger-Kentischer, A., Göbel, H., Kleemann, R., Zernecke, A., Bucala, R., Leng, L., Finkelmeier, D., Geiger, G., Schaefer, H. E., Schober, A., Weber, C., Brunner, H., Rütten, H., Ihling, C., and Bernhagen, J. (2006). Reduction of the aortic inflammatory response inspontaneous atherosclerosis by blockade of macrophage migration inhibitory factor (MIF). Atherosclerosis 184, 28–38.
| Reduction of the aortic inflammatory response inspontaneous atherosclerosis by blockade of macrophage migration inhibitory factor (MIF).Crossref | GoogleScholarGoogle Scholar | 15921687PubMed |
Calandra, T., and Bucala, R. (2017). Macrophage migration inhibitory factor (MIF): a glucocorticoid counter-regulator within the immune system. Crit. Rev. Immunol. 37, 359–370.
| Macrophage migration inhibitory factor (MIF): a glucocorticoid counter-regulator within the immune system.Crossref | GoogleScholarGoogle Scholar | 29773026PubMed |
Calandra, T., and Roger, T. (2003). Macrophage migration inhibitory factor: a regulator of innate immunity. Nat. Rev. Immunol. 3, 791–800.
| Macrophage migration inhibitory factor: a regulator of innate immunity.Crossref | GoogleScholarGoogle Scholar | 14502271PubMed |
Calandra, T., Bernhagen, J., Mitchell, R. A., and Bucala, R. (1994). The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J. Exp. Med. 179, 1895–1902.
| The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor.Crossref | GoogleScholarGoogle Scholar | 8195715PubMed |
Calandra, T., Bernhagen, J., Metz, C. N., Spiegel, L. A., Bacher, M., Donnelly, T., Cerami, A., and Bucala, R. (1995). MIF as a glucocorticoid-induced modulator of cytokine production. Nature 377, 68–71.
| MIF as a glucocorticoid-induced modulator of cytokine production.Crossref | GoogleScholarGoogle Scholar | 7659164PubMed |
Calandra, T., Echtenacher, B., Roy, D. L., Pugin, J., Metz, C. N., Hültner, L., Heumann, D., Männel, D., Bucala, R., and Glauser, M. P. (2000). Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat. Med. 6, 164–170.
| Protection from septic shock by neutralization of macrophage migration inhibitory factor.Crossref | GoogleScholarGoogle Scholar | 10655104PubMed |
Chagnon, F., Metz, C. N., Bucala, R., and Lesur, O. (2005). Endotoxin-induced myocardial dysfunction: effects of macrophage migration inhibitory factor neutralization. Circ. Res. 96, 1095–1102.
| Endotoxin-induced myocardial dysfunction: effects of macrophage migration inhibitory factor neutralization.Crossref | GoogleScholarGoogle Scholar | 15879312PubMed |
Cheng, Q., McKeown, S. J., Santos, L., Santiago, F. S., Khachigian, L. M., Morand, E. F., and Hickey, M. J. (2010). Macrophage migration inhibitory factor increases leukocyte–endothelial interactions in human endothelial cells via promotion of expression of adhesion molecules. J. Immunol. 185, 1238–1247.
| Macrophage migration inhibitory factor increases leukocyte–endothelial interactions in human endothelial cells via promotion of expression of adhesion molecules.Crossref | GoogleScholarGoogle Scholar | 20554956PubMed |
Cheon, S. K., Kim, H. P., Park, Y. L., Jang, J. E., Lim, Y., Song, S. H., Han, S. W., and Kim, T. Y. (2018). Macrophage migration inhibitory factor promotes resistance to MEK blockade in KRAS mutant colorectal cancer cells. Mol. Oncol. 12, 1398–1409.
| Macrophage migration inhibitory factor promotes resistance to MEK blockade in KRAS mutant colorectal cancer cells.Crossref | GoogleScholarGoogle Scholar | 29896883PubMed |
Cherepkova, O. A., Lyutova, E. M., Eronina, T. B., and Ya Gurvits, B. (2006). Chaperone-like activity of macrophage migration inhibitory factor. Int. J. Biochem. Cell Biol. 38, 43–55.
| Chaperone-like activity of macrophage migration inhibitory factor.Crossref | GoogleScholarGoogle Scholar | 16099194PubMed |
Chesney, J., Metz, C., Bacher, M., Peng, T., Meinhardt, A., and Bucala, R. (1999). An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Mol. Med. 5, 181–191.
| An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma.Crossref | GoogleScholarGoogle Scholar | 10404515PubMed |
Costa, A. F., Gomes, S. Z., Lorenzon-Ojea, A. R., Martucci, M., Faria, M. R., dos Santos Pinto, D., Oliveira, S. F., Ietta, F., Paulesu, L., and Bevilacqua, E. (2016). Macrophage migration inhibitory factor induces phosphorylation of Mdm2 mediated by phosphatidylinositol 3-kinase/Akt kinase: role of this pathway in decidual cell survival. Placenta 41, 27–38.
| Macrophage migration inhibitory factor induces phosphorylation of Mdm2 mediated by phosphatidylinositol 3-kinase/Akt kinase: role of this pathway in decidual cell survival.Crossref | GoogleScholarGoogle Scholar | 27208405PubMed |
Cox, G. M., Kithcart, A. P., Pitt, D., Guan, Z., Alexander, J., Williams, J. L., Shawler, T., Dagia, N. M., Popovich, P. G., Satoskar, A. R., and Whitacre, C. C. (2013). Macrophage migration inhibitory factor potentiates autoimmune-mediated neuroinflammation. J. Immunol. 191, 1043–1054.
| Macrophage migration inhibitory factor potentiates autoimmune-mediated neuroinflammation.Crossref | GoogleScholarGoogle Scholar | 23797673PubMed |
Das, R., Koo, M. S., Kim, B. H., Jacob, S. T., Subbian, S., Yao, J., Leng, L., Levy, R., Murchison, C., Burman, W. J., Moore, C. C., Scheld, W. M., David, J. R., Kaplan, G., MacMicking, J. D., and Bucala, R. (2013). 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.
| Macrophage migration inhibitory factor (MIF) is a critical mediator of the innate immune response to Mycobacterium tuberculosis.Crossref | GoogleScholarGoogle Scholar | 23882081PubMed |
Dickerhof, N., Schindler, L., Bernhagen, J., Kettle, A. J., and Hampton, M. B. (2015). Macrophage migration inhibitory factor (MIF) is rendered enzymatically inactive by myeloperoxidase-derived oxidants but retains its immunomodulatory function. Free Radic. Biol. Med. 89, 498–511.
| Macrophage migration inhibitory factor (MIF) is rendered enzymatically inactive by myeloperoxidase-derived oxidants but retains its immunomodulatory function.Crossref | GoogleScholarGoogle Scholar | 26453918PubMed |
Fitzgerald, J. S., Germeyer, A., Huppertz, B., Jeschke, U., Knöfler, M., Moser, G., Scholz, C., Sonderegger, S., Toth, B., and Markert, U. R. (2010). Governing the invasive trophoblast: current aspects on intra- and extracellular regulation. Am. J. Reprod. Immunol. 63, 492–505.
| Governing the invasive trophoblast: current aspects on intra- and extracellular regulation.Crossref | GoogleScholarGoogle Scholar | 20236263PubMed |
Ietta, F., Ferro, E. A. V., Bevilacqua, E., Benincasa, L., Maioli, E., and Paulesu, L. (2018). Role of the macrophage migration inhibitory factor (MIF) in the survival of first trimester human placenta under induced stress conditions. Sci. Rep. 8, 12150.
| Role of the macrophage migration inhibitory factor (MIF) in the survival of first trimester human placenta under induced stress conditions.Crossref | GoogleScholarGoogle Scholar | 30108299PubMed |
Jovanović Krivokuća, M., Stefanoska, I., Abu Rabi, T., Al-Abed, Y., Stošić-Grujičić, S., and Vićovac, Lj. (2015). Pharmacological inhibition of MIF interferes with trophoblast cell migration and invasiveness. Placenta 36, 150–159.
| Pharmacological inhibition of MIF interferes with trophoblast cell migration and invasiveness.Crossref | GoogleScholarGoogle Scholar | 25530499PubMed |
Jovanović-Krivokuća, M., Stefanoska, I., Rabi Abu, T., Vilotić, A., Petronijević, M., Vrzić-Petronijević, S., Radojčić, Lj., and Vićovac, Lj. (2016). MIF is among the proinflammatory cytokines increased by LPS in the human trophoblast line. Arch. Biol. Sci. 68, 715–722.
| MIF is among the proinflammatory cytokines increased by LPS in the human trophoblast line.Crossref | GoogleScholarGoogle Scholar |
Kaufmann, P., Black, S., and Huppertz, B. (2003). Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol. Reprod. 69, 1–7.
| Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia.Crossref | GoogleScholarGoogle Scholar | 12620937PubMed |
Khoufache, K., Bazin, S., Girard, K., Guillemette, J., Roy, M. C., Verreault, J. P., Al-Abed, Y., Foster, W., and Akoum, A. (2012). Macrophage migration inhibitory factor antagonist blocks the development of endometriosis in vivo. PLoS One 7, e37264.
| Macrophage migration inhibitory factor antagonist blocks the development of endometriosis in vivo.Crossref | GoogleScholarGoogle Scholar | 22649515PubMed |
Kleemann, R., Kapurniotu, A., Frank, R. W., Gessner, A., Mischke, R., Flieger, O., Jüttner, S., Brunner, H., and Bernhagen, J. (1998). Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J. Mol. Biol. 280, 85–102.
| Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase.Crossref | GoogleScholarGoogle Scholar | 9653033PubMed |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) method. Methods 25, 402–408.
| 11846609PubMed |
Lo, M. C., Yip, T. C., Ngan, K. C., Cheng, W. W., Law, C. K., Chan, P. S., Chan, K. C., Wong, C. K., Wong, R. N., Lo, K. W., Ng, W. T., Lee, W. M., Tsao, S. W., Kwong, L. W., Lung, M. L., and Mak, N. K. (2013). Role of MIF/CXCL8/CXCR2 signaling in the growth of nasopharyngeal carcinoma tumor spheres. Cancer Lett. 335, 81–92.
| Role of MIF/CXCL8/CXCR2 signaling in the growth of nasopharyngeal carcinoma tumor spheres.Crossref | GoogleScholarGoogle Scholar | 23403077PubMed |
Meyer-Siegler, K. L., Iczkowski, K. A., Leng, L., Bucala, R., and Vera, P. L. (2006). Inhibition of macrophage migration inhibitory factor or its receptor (CD74) attenuates growth and invasion of DU-145 prostate cancer cells. J. Immunol. 177, 8730–8739.
| Inhibition of macrophage migration inhibitory factor or its receptor (CD74) attenuates growth and invasion of DU-145 prostate cancer cells.Crossref | GoogleScholarGoogle Scholar | 17142775PubMed |
Milian, I. C. B., Silva, R. J., Manzan-Martins, C., Barbosa, B. F., Guirelli, P. M., Ribeiro, M., de Oliveira Gomes, A., Ietta, F., Mineo, J. R., Silva Franco, P., and Ferro, E. A. V. (2019). Increased Toxoplasma gondii intracellular proliferation in human extravillous trophoblast cells (HTR8/SVneo line) is sequentially triggered by MIF, ERK1/2, and COX-2. Front. Microbiol. 10, 852.
| Increased Toxoplasma gondii intracellular proliferation in human extravillous trophoblast cells (HTR8/SVneo line) is sequentially triggered by MIF, ERK1/2, and COX-2.Crossref | GoogleScholarGoogle Scholar |
Mirkov, I., Belij, S., Kataranovski, M., Zolotarevski, L., Glamoclija, J., Stojanovic, I., and Stosic-Grujicic, S. (2012). The relevance of the migration inhibitory factor (MIF) forperipheral tissue response in murine sublethal systemic Aspergillus fumigatus infection. Med. Mycol. 50, 476–487.
| The relevance of the migration inhibitory factor (MIF) forperipheral tissue response in murine sublethal systemic Aspergillus fumigatus infection.Crossref | GoogleScholarGoogle Scholar | 22217210PubMed |
Mor, G., Cardenas, I., Abrahams, V., and Guller, S. (2011). Inflammation and pregnancy: the role of the immune system at the implantation site. Ann. N. Y. Acad. Sci. 1221, 80–87.
| Inflammation and pregnancy: the role of the immune system at the implantation site.Crossref | GoogleScholarGoogle Scholar | 21401634PubMed |
Murakami, H., Akbar, S. M., Matsui, H., Horiike, N., and Onji, M. (2002). Macrophage migration inhibitory factor activates antigen-presenting dendritic cells and induces inflammatory cytokines in ulcerative colitis. Clin. Exp. Immunol. 128, 504–510.
| Macrophage migration inhibitory factor activates antigen-presenting dendritic cells and induces inflammatory cytokines in ulcerative colitis.Crossref | GoogleScholarGoogle Scholar | 12109441PubMed |
Nothnick, W. B., Falcone, T., Olson, M. R., Fazleabas, A. T., Tawfik, O. W., and Graham, A. (2018). Macrophage migration inhibitory factor receptor, CD74, is overexpressed in human and baboon (Papio anubis) endometriotic lesions and modulates endometriotic epithelial cell survival and interleukin 8 expression. Reprod. Sci. 25, 1557–1566.
| Macrophage migration inhibitory factor receptor, CD74, is overexpressed in human and baboon (Papio anubis) endometriotic lesions and modulates endometriotic epithelial cell survival and interleukin 8 expression.Crossref | GoogleScholarGoogle Scholar | 29592775PubMed |
Onodera, S., Nishihira, J., Koyama, Y., Majima, T., Aoki, Y., Ichiyama, H., Ishibashi, T., and Minami, A. (2004). Macrophage migration inhibitory factor up-regulates the expression of interleukin-8 messenger RNA in synovial fibroblasts of rheumatoid arthritis patients: common transcriptional regulatory mechanism between interleukin-8 and interleukin-1beta. Arthritis Rheum. 50, 1437–1447.
| Macrophage migration inhibitory factor up-regulates the expression of interleukin-8 messenger RNA in synovial fibroblasts of rheumatoid arthritis patients: common transcriptional regulatory mechanism between interleukin-8 and interleukin-1beta.Crossref | GoogleScholarGoogle Scholar | 15146413PubMed |
Powell, N. D., Papenfuss, T. L., McClain, M. A., Gienapp, I. E., Shawler, T. M., Satoskar, A. R., and Whitacre, C. C. (2005). Cutting edge: macrophage migration inhibitory factor is necessary for progression of experimental autoimmune encephalomyelitis. J. Immunol. 175, 5611–5614.
| Cutting edge: macrophage migration inhibitory factor is necessary for progression of experimental autoimmune encephalomyelitis.Crossref | GoogleScholarGoogle Scholar | 16237048PubMed |
Ren, Y., Chan, H. M., Li, Z., Lin, C., Nicholls, J., Chen, C. F., Lee, P. Y., Lui, V., Bacher, M., and Tam, P. K. (2004). Upregulation of macrophage migration inhibitory factor contributes to induced N-Myc expression by the activation of ERK signaling pathway and increased expression of interleukin-8 and VEGF in neuroblastoma. Oncogene 23, 4146–4154.
| Upregulation of macrophage migration inhibitory factor contributes to induced N-Myc expression by the activation of ERK signaling pathway and increased expression of interleukin-8 and VEGF in neuroblastoma.Crossref | GoogleScholarGoogle Scholar | 15064733PubMed |
Rendon, B. E., Willer, S. S., Zundel, W., and Mitchell, R. A. (2009). Mechanisms of macrophage migration inhibitory factor (MIF)-dependent tumor microenvironmental adaptation. Exp. Mol. Pathol. 86, 180–185.
| Mechanisms of macrophage migration inhibitory factor (MIF)-dependent tumor microenvironmental adaptation.Crossref | GoogleScholarGoogle Scholar | 19186177PubMed |
Rosengren, E., Bucala, R., Aman, P., Jacobsson, L., Odh, G., Metz, C. N., and Rorsman, H. (1996). The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyzes a tautomerization reaction. Mol. Med. 2, 143–149.
| The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyzes a tautomerization reaction.Crossref | GoogleScholarGoogle Scholar | 8900542PubMed |
Rosengren, E., Aman, P., Thelin, S., Hansson, C., Ahlfors, S., Björk, P., Jacobsson, L., and Rorsman, H. (1997). The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase. FEBS Lett. 417, 85–88.
| The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase.Crossref | GoogleScholarGoogle Scholar | 9395080PubMed |
Sakai, Y., Masamune, A., Satoh, A., Nishihira, J., Yamagiwa, T., and Shimosegawa, T. (2003). Macrophage migration inhibitory factor is a critical mediator of severe acute pancreatitis. Gastroenterology 124, 725–736.
| Macrophage migration inhibitory factor is a critical mediator of severe acute pancreatitis.Crossref | GoogleScholarGoogle Scholar | 12612911PubMed |
Sanchez-Zamora, Y., Terrazas, L. I., Vilches-Flores, A., Leal, E., Juárez, I., Whitacre, C., Kithcart, A., Pruitt, J., Sielecki, T., Satoskar, A. R., and Rodriguez-Sosa, M. (2010). Macrophage migration inhibitory factor is a therapeutic target in treatment of non-insulin-dependent diabetes mellitus. FASEB J. 24, 2583–2590.
| Macrophage migration inhibitory factor is a therapeutic target in treatment of non-insulin-dependent diabetes mellitus.Crossref | GoogleScholarGoogle Scholar | 20203087PubMed |
Santos, L. L., Lacey, D., Yang, Y., Leech, M., and Morand, E. F. (2004). Activation of synovial cell p38 MAP kinase by macrophage migration inhibitory factor. J. Rheumatol. 31, 1038–1043.
| 15170913PubMed |
Shi, X., Leng, L., Wang, T., Wang, W., Du, X., Li, J., McDonald, C., Chen, Z., Murphy, J. W., Lolis, E., Noble, P., Knudson, W., and Bucala, R. (2006). CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 25, 595–606.
| CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex.Crossref | GoogleScholarGoogle Scholar | 17045821PubMed |
Song, H., Zhu, Z., Zhou, Y., Du, N., Song, T., Liang, H., Chen, X., Wang, Y., Wang, Y., and Hu, Y. (2019). MIF/CD74 axis participates in inflammatory activation of Schwann cells following sciatic nerve injury. J. Mol. Histol. 50, 355–367.
| MIF/CD74 axis participates in inflammatory activation of Schwann cells following sciatic nerve injury.Crossref | GoogleScholarGoogle Scholar | 31197516PubMed |
Stojanović, I., Cvjetićanin, T., Lazaroski, S., Stosić-Grujicić, S., and Miljković, D. (2009). Macrophage migration inhibitory factor stimulates interleukin-17 expression and production in lymph node cells. Immunology 126, 74–83.
| Macrophage migration inhibitory factor stimulates interleukin-17 expression and production in lymph node cells.Crossref | GoogleScholarGoogle Scholar | 18624729PubMed |
Stosic-Grujicic, S., Stojanovic, I., and Nicoletti, F. (2009). MIF in autoimmunity and novel therapeutic approaches. Autoimmun. Rev. 8, 244–249.
| MIF in autoimmunity and novel therapeutic approaches.Crossref | GoogleScholarGoogle Scholar | 18721909PubMed |
Sun, H. W., Bernhagen, J., Bucala, R., and Lolis, E. (1996). Crystal structure at 2.6-A resolution of human macrophage migration inhibitory factor. Proc. Natl Acad. Sci. USA 93, 5191–5196.
| Crystal structure at 2.6-A resolution of human macrophage migration inhibitory factor.Crossref | GoogleScholarGoogle Scholar | 8643551PubMed |
Tanese, K., Hashimoto, Y., Berkova, Z., Wang, Y., Samanieg, F., Lee, J. E., Ekmekcioglu, S., and Grimm, E. A. (2015). Cell surface CD74-MIF interactions drive melanoma survival in response to interferon-γ. J. Invest. Dermatol. 135, 2775–2784.
| Cell surface CD74-MIF interactions drive melanoma survival in response to interferon-γ.Crossref | GoogleScholarGoogle Scholar | 26039541PubMed |
Tarnowski, M., Grymula, K., Liu, R., Tarnowska, J., Drukala, J., Ratajczak, J., Mitchell, R. A., Ratajczak, M. Z., and Kucia, M. (2010). Macrophage migration inhibitory factor is secreted by rhabdomyosarcoma cells, modulates tumor metastasis by binding to CXCR4 and CXCR7 receptors and inhibits recruitment of cancer-associated fibroblasts. Mol. Cancer Res. 8, 1328–1343.
| Macrophage migration inhibitory factor is secreted by rhabdomyosarcoma cells, modulates tumor metastasis by binding to CXCR4 and CXCR7 receptors and inhibits recruitment of cancer-associated fibroblasts.Crossref | GoogleScholarGoogle Scholar | 20861157PubMed |
Veillat, V., Carli, C., Metz, C. N., Al-Abed, Y., Naccache, P. H., and Akoum, A. (2010). Macrophage migration inhibitory factor elicits an angiogenic phenotype in human ectopic endometrial cells and triggers the production of major angiogenic factors via CD44, CD74, and MAPK signaling pathways. J. Clin. Endocrinol. Metab. 95, E403–E412.
| Macrophage migration inhibitory factor elicits an angiogenic phenotype in human ectopic endometrial cells and triggers the production of major angiogenic factors via CD44, CD74, and MAPK signaling pathways.Crossref | GoogleScholarGoogle Scholar | 20829186PubMed |
Vilotić, A., Jovanović Krivokuć, M., Stefanoska, I., Vrzić Petronijević, S., Petronijević, M., and Vićovac, Lj. (2019). Macrophage migration inhibitory factor is involved in endovascular trophoblast cell function in vitro. EXCLI J. 18, Doc1007.
| 31762725PubMed |
Wang, Y. Z., Tian, F. F., Liu, H., Zhang, W., Li, J., Xiao, B., and Zhou, W. B. (2013). Macrophage migration inhibitory factor is necessary for the Lipo-oligosaccharide-induced response by modulation of Toll-like receptor 4 in monocytes from GBS patients. J. Neuroimmunol. 257, 67–75.
| Macrophage migration inhibitory factor is necessary for the Lipo-oligosaccharide-induced response by modulation of Toll-like receptor 4 in monocytes from GBS patients.Crossref | GoogleScholarGoogle Scholar | 23411097PubMed |
Weber, C., Kraemer, S., Drechsler, M., Lue, H., Koenen, R. R., Kapurniotu, A., Zernecke, A., and Bernhagen, J. (2008). Structural determinants of MIF functions in CXCR2-mediated inflammatory and atherogenic leukocyte recruitment. Proc. Natl Acad. Sci. USA 105, 16278–16283.
| Structural determinants of MIF functions in CXCR2-mediated inflammatory and atherogenic leukocyte recruitment.Crossref | GoogleScholarGoogle Scholar | 18852457PubMed |
West, P. W., Parker, L. C., Ward, J. R., and Sabroe, I. (2008). Differential and cell-type specific regulation of responses to Toll-like receptor agonists by ISO-1. Immunology 125, 101–110.
| Differential and cell-type specific regulation of responses to Toll-like receptor agonists by ISO-1.Crossref | GoogleScholarGoogle Scholar | 18355244PubMed |
Xiong, C., Huang, B., Cun, Y., Aghdasi, B. G., and Zhou, Y. (2014). Migration inhibitory factor enhances inflammation via CD74 in cartilage end plates with Modic type 1 changes on MRI. Clin. Orthop. Relat. Res. 472, 1943–1954.
| Migration inhibitory factor enhances inflammation via CD74 in cartilage end plates with Modic type 1 changes on MRI.Crossref | GoogleScholarGoogle Scholar | 24569872PubMed |