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http://dx.doi.org/10.7314/APJCP.2012.13.5.1737

Macrophage Migration Inhibitory Factor: a Potential Marker for Cancer Diagnosis and Therapy  

Babu, Spoorthy N. (MS, IGNOU-I2IT Centre of Excellence for Advanced Education and Research)
Chetal, Gaurav (MS, IGNOU-I2IT Centre of Excellence for Advanced Education and Research)
Kumar, Sudhir (MS, IGNOU-I2IT Centre of Excellence for Advanced Education and Research)
Publication Information
Asian Pacific Journal of Cancer Prevention / v.13, no.5, 2012 , pp. 1737-1744 More about this Journal
Abstract
Macrophage migration inhibitory factor (MIF) is a pluripotent cytokine which plays roles in inflammation, immune responses and cancer development. It assists macrophages in carrying out functions like phagocytosis, adherence and motility. Of late, MIF is implicated in almost all stages of neoplasia and expression is a feature of most types of cancer. The presence of MIF in almost all tumors and all stages of cancer makes it an interesting candidate for cancer therapy. This review explores the roles of MIF in neoplasia.
Keywords
MIF; immune suppression; p53; hypoxia; neoplasia; metastasis;
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1 Liu Q, Yang H, Zhang SF (2010). Expression and significance of MIF and CD147 in non-small cell lung cancer. Sichuan Da Xue Xue Bao Yi Xue Ban, 41 85-90.
2 Lue H, Kapurniotu A, Fingerle-Rowson G, et al. (2006). 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.   DOI
3 Lue H, Thiele M, Franz J, et al (2007). 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, 5046-59.   DOI
4 Lyapina S, Cope G, Shevchenko A, et al (2001). Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science, 292, 1382-5.   DOI
5 Madani SY, Naderi N, Dissanayake O, Tan A, Seifalian AM (2011). A new era of cancer treatment: carbon nanotubes as drug delivery tools. Int J nanomedicine, 6, 2963-79.
6 Marhaba R, Zoller M (2004). CD44 in cancer progression: adhesion, migration and growth regulation. J Mol Histol, 35, 211-31.
7 Medema RH, Macurek L (2011). Checkpoint control and cancer. Oncogene.
8 Meyer-Siegler KL Iczkowski KA, Leng L, Bucala R, Vera PL (2006). Inhibition of macrophage migration inhibitory factor or its receptor (CD74) attenuates growth and invasion of DU-145 prostate cancer cells. J Immunol, 177, 8730-9.   DOI
9 Miller SC, Huang R, Sakamuru S, et al (2010). Identification of known drugs that act as inhibitors of NF-kappaB signaling and their mechanism of action. Biochem Pharmacol, 79, 1272-0.   DOI
10 Mitchell RA, Liao H, Chesney J, et al (2002). Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci U S A, 99, 345-50.   DOI
11 Mitchell RA, Metz CN, Peng T, Bucala R (1999). 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, 274, 18100-6.   DOI
12 Nakaya K, Nabata Y, Ichiyanagi T, An WW (2012). Stimulation of Dendritic Cell Maturation and Induction of Apoptosis in Leukemia Cells by a Heat-stable Extract from Azuki bean (Vigna angularis), a Promising Immunopotentiating Food and Dietary Supplement for Cancer Prevention. Asian Pac J Cancer Prev, 13, 607-11   DOI   ScienceOn
13 Nakayama KI, Nakayama K (2006). Ubiquitin ligases: cell-cycle control and cancer. Nat Rev Cancer, 6, 369-81.   DOI
14 Nemajerova A, Mena P, Fingerle-Rowson G, Moll UM, Petrenko O (2007). Impaired DNA damage checkpoint response in MIF-deficient mice. EMBO J, 26, 987-97.   DOI
15 Nemajerova A, Moll UM, Petrenko O, Fingerle-Rowson G (2007). Macrophage migration inhibitory factor coordinates DNA damage response with the proteasomal control of the cell cycle. Cell Cycle, 6, 1030-4.   DOI
16 Nguyen MT, Lue H, Kleemann R, et al (2003). The cytokine macrophage migration inhibitory factor reduces prooxidative stress-induced apoptosis. J Immunol, 170, 3337-47.   DOI
17 Nishihira J (2000). Macrophage migration inhibitory factor (MIF): its essential role in the immune system and cell growth. J Interferon Cytokine Res, 20, 751-62.   DOI
18 Oda S, Oda T, Nishi K, et al (2008). Macrophage migration inhibitory factor activates hypoxia-inducible factor in a p53-dependent manner. PLoS One, 3, 2215.   DOI
19 Nishihira J, Ishibashi T, Fukushima T, et al (2003). Macrophage migration inhibitory factor (MIF): Its potential role in tumor growth and tumor-associated angiogenesis. Ann N Y Acad Sci, 995, 171-2.   DOI
20 Nishihira J, Koyama Y, Mizue Y (1996). Identification of macrophage migration inhibitory factor in human leukemia HL-60 cells and its induction by lipopolysaccharide. Biochem Mol Biol Int, 40, 861-9.
21 Oloumi A, McPhee T and Dedhar S (2004). Regulation of E-cadherin expression and beta-catenin/Tcf transcriptional activity by the integrin-linked kinase. Biochim Biophys Acta, 1691, 1-15.   DOI   ScienceOn
22 Ong GL, Goldenberg DM, Hansen HJ and Mattes MJ (1999). Cell surface expression and metabolism of major histocompatibility complex class II invariant chain (CD74) by diverse cell lines. Immunology, 98, 296-2.   DOI
23 Pollard JW (2004). Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer, 4, 71-8.   DOI
24 Ren Y, Chan HM, Fan J, et al (2006). Inhibition of tumor growth and metastasis in vitro and in vivo by targeting macrophage migration inhibitory factor in human neuroblastoma. Oncogene, 25, 3501-8.   DOI
25 Ren Y, Chan HM, Li Z, et al (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, 4146-4.   DOI
26 Sen S and Hopwood V (2011). Molecular cytogenetic evidence for multistep tumorigenesis: implications for risk assessment and early detection. Cancer Biomark, 9, 113-32.   DOI
27 Ren Y, Law S, Huang X, et al (2005). 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, 55-3.   DOI
28 Rendon BE, Roger T, Teneng I, et al (2007). Regulation of human lung adenocarcinoma cell migration and invasion by macrophage migration inhibitory factor. J Biol Chem, 282, 29910-8.   DOI
29 Rosengren E, Bucala R, Aman P, et al (1996). The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyzes a tautomerization reaction. Mol Med, 2, 143-9.
30 Shimizu T, Abe R, Nakamura H, et al (1999). High expression of macrophage migration inhibitory factor in human melanoma cells and its role in tumor cell growth and angiogenesis. Biochem Biophys Res Commun, 264, 751-8.   DOI
31 Shimizu T, Nishihira J, Watanabe H, et al (2004). Macrophage migration inhibitory factor is induced by thrombin and factor Xa in endothelial cells. J Biol Chem, 279, 13729-7.   DOI
32 Shi X, Leng L, Wang T, et al (2006). CD44 is the signaling component of the macrophage migration inhibitory factor- CD74 receptor complex. Immunity, 25, 595-6.   DOI
33 Shkolnik T, Livni E, Reshef R, Lachter J, Eidelman S (1987). Comparison of two lymphokines (macrophage migration inhibition, leukocyte adherence inhibition factors) and carcinoembryonic antigen, in colorectal cancer and colonic premalignant lesions. Am J Gastroenterol, 82, 1275-8.
34 Stein R, Mattes MJ, Cardillo TM, et al (2007). CD74: a new candidate target for the immunotherapy of B-cell neoplasms. Clin Cancer Res, 13, 5556-3.   DOI
35 Spiller SE, Logsdon NJ, Deckard LA, Sontheimer H (2011). Inhibition of nuclear factor kappa-B signaling reduces growth in medulloblastoma in vivo. BMC Cancer, 11, 136.   DOI
36 Staller P, Peukert K, Kiermaier A, et al (2001). Repression of p15INK4b expression by Myc through association with Miz-1. Nat Cell Biol, 3, 392-9.   DOI   ScienceOn
37 Steegenga WT, van der Eb AJ, Jochemsen AG (1996). How phosphorylation regulates the activity of p53. J Mol Biol, 263, 103-3.   DOI
38 Strieter RM (2005). Masters of angiogenesis. Nat Med, 11, 925-7.   DOI
39 Sun B, Nishihira J, Yoshiki T, et al (2005). Macrophage migration inhibitory factor promotes tumor invasion and metastasis via the Rho-dependent pathway. Clin Cancer Res, 11, 1050-8.
40 Sun HW, Bernhagen J, Bucala R, Lolis E (1996). Crystal structure at 2.6-A resolution of human macrophage migration inhibitory factor. Proc Natl Acad Sci U S A, 93, 5191-6.   DOI
41 Sun HW, Swope M, Cinquina C, et al (1996). The subunit structure of human macrophage migration inhibitory factor: evidence for a trimer. Protein Eng, 9, 631-5.   DOI
42 Talos F, Mena P, Fingerle-Rowson G, Moll U, Petrenko O (2005). MIF loss impairs Myc-induced lymphomagenesis. Cell Death Differ, 12, 1319-8.   DOI
43 Tang WM, Gou X, Liu QX (2011). Expression of macrophage migration inhibition factor (MIF) in serum of patients with prostate cancer and its clinical significance. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi, 27, 97-8.
44 Vlach J, Hennecke S, Alevizopoulos K, Conti D, Amati B (1996). Growth arrest by the cyclin-dependent kinase inhibitor p27Kip1 is abrogated by c-Myc. EMBO J, 15, 6595-4.
45 Thiele M and Bernhagen J (2005). Link between macrophage migration inhibitory factor and cellular redox regulation. Antioxid Redox Signal, 7, 1234-48.   DOI
46 Tsvetkov LM, Yeh KH, Lee SJ, Sun H, Zhang H (1999). p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27. Curr Biol, 9, 661-4.   DOI   ScienceOn
47 Veillat V, Carli C, Metz CN, et al (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, E403-2.   DOI
48 Welcker M, Orian A, Jin J, et al (2004). The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylationdependent c-Myc protein degradation. Proc Natl Acad Sci U S A, 101, 9085-90.   DOI
49 Winner M, Koong AC, Rendon BE, Zundel W, Mitchell RA. (2007). Amplification of tumor hypoxic responses by macrophage migration inhibitory factor-dependent hypoxiainducible factor stabilization. Cancer Res, 67, 186-3.   DOI   ScienceOn
50 Winner M, Leng L, Zundel W, Mitchell RA (2007). Macrophage migration inhibitory factor manipulation and evaluation in tumoral hypoxic adaptation. Methods Enzymol, 435, 355-69.   DOI
51 Xu X, Wang B, Ye C, et al (2008). Overexpression of macrophage migration inhibitory factor induces angiogenesis in human breast cancer. Cancer Lett, 261, 147-7.   DOI
52 Bach JP, Rinn B, Meyer B, Dodel R, Bacher M (2008). Role of MIF in inflammation and tumorigenesis. Oncology, 75, 127-3.   DOI
53 Xue Y, Xu H, Rong L, et al (2010). The MIF -173G/C polymorphism and risk of childhood acute lymphoblastic leukemia in a Chinese population. Leuk Res, 34, 1282-6.   DOI
54 Yamasaki L, Pagano M (2004). Cell cycle, proteolysis and cancer. Curr Opin Cell Biol, 16, 623-8.   DOI
55 Zheng J, Yang X, Harrell JM, et al (2002). CAND1 binds to unneddylated CUL1 and regulates the formation of SCF ubiquitin E3 ligase complex. Mol Cell, 10, 1519-6.   DOI
56 Aalamian M, Pirtskhalaishvili G, Nunez A, et al (2001). Human prostate cancer regulates generation and maturation of monocyte-derived dendritic cells. Prostate, 46, 68-5.   DOI
57 Al-Abed Y, VanPatten S (2011). MIF as a disease target: ISO-1 as a proof-of-concept therapeutic. Future Med Chem, 3, 45-63.   DOI
58 Bacher M, Schrader J, Thompson N, et al (2003). 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, 162, 11-7.   DOI
59 Bando H, Matsumoto G, Bando M, et al (2002). Expression of macrophage migration inhibitory factor in human breast cancer: association with nodal spread. Jpn J Cancer Res, 93, 389-6.   DOI
60 Baugh JA, Chitnis S, Donnelly SC, et al (2002). A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis. Genes Immun, 3, 170-6.   DOI
61 Baugh JA, Gantier M, Li L, et al (2006). Dual regulation of macrophage migration inhibitory factor (MIF) expression in hypoxia by CREB and HIF-1. Biochem Biophys Res Commun, 347 , 895-3.   DOI
62 Bergers G, Benjamin LE (2003). Tumorigenesis and the angiogenic switch. Nat Rev Cancer, 3, 401-10.   DOI
63 Bernhagen J, Krohn R, Lue H, et al (2007). MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med, 13, 587-6.   DOI
64 Bornstein G, Ganoth D, Hershko A (2006). Regulation of neddylation and deneddylation of cullin1 in SCFSkp2 ubiquitin ligase by F-box protein and substrate. Proc Natl Acad Sci U S A, 103, 11515-0.   DOI
65 Bifulco C, McDaniel K, Leng L, Bucala R (2008). Tumor growth-promoting properties of macrophage migration inhibitory factor. Curr Pharm Des, 14, 3790-801.   DOI
66 Binsky I, Haran M, Starlets D, et al (2007). IL-8 secreted in a macrophage migration-inhibitory factor- and CD74- dependent manner regulates B cell chronic lymphocytic leukemia survival. Proc Natl Acad Sci U S A, 104, 13408-3.   DOI
67 Bondza PK, Metz CN, Akoum A (2008). Macrophage migration inhibitory factor up-regulates alpha(v)beta(3) integrin and vascular endothelial growth factor expression in endometrial adenocarcinoma cell line Ishikawa. J Reprod Immunol, 77, 142-1.   DOI
68 Bucala R, Donnelly SC (2007). Macrophage migration inhibitory factor: a probable link between inflammation and cancer. Immunity, 26, 281-5.   DOI
69 Budarf M, McDonald T, Sellinger B, et al (1997). Localization of the human gene for macrophage migration inhibitory factor (MIF) to chromosome 22q11.2. Genomics, 39, 235-6.   DOI
70 Calandra T, Bernhagen J, Metz CN, et al (1995). MIF as a glucocorticoid-induced modulator of cytokine production. Nature, 377, 68-1.   DOI   ScienceOn
71 Cardozo T, Pagano M (2004). The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol, 5, 739-51.   DOI
72 Cheng RJ, Deng WG, Niu CB, Li YY, Fu Y (2011). Expression of macrophage migration inhibitory factor and CD74 in cervical squamous cell carcinoma. Int J Gynecol Cancer, 21, 1004-2.   DOI
73 Conroy H, Mawhinney L and Donnelly SC (2010). Inflammation and cancer: macrophage migration inhibitory factor (MIF)- -the potential missing link. QJM, 103, 831-6.   DOI
74 Claassen GF, Hann SR (2000). A role for transcriptional repression of p21CIP1 by c-Myc in overcoming transforming growth factor beta -induced cell-cycle arrest. Proc Natl Acad Sci U S A, 97, 9498-3.   DOI   ScienceOn
75 Cohen S, Shoshana OY, Zelman-Toister E, et al (2012). The Cytokine Midkine and Its Receptor RPTPzeta Regulate B Cell Survival in a Pathway Induced by CD74. J Immunol, 188, 259-9.   DOI
76 Colombo MP, Mantovani A (2005). Targeting myelomonocytic cells to revert inflammation-dependent cancer promotion. Cancer Res, 65, 9113-6.   DOI
77 Dhingra S, Feng W, Brown RE, et al (2011). Clinicopathologic significance of putative stem cell markers, CD44 and nestin, in gastric adenocarcinoma. Int J Clin Exp Pathol, 4, 733-1.
78 El-Omar EM, Ng MT, Hold GL (2008). Polymorphisms in Tolllike receptor genes and risk of cancer. Oncogene, 27, 244-2.   DOI
79 Fingerle-Rowson G, Petrenko O (2007). MIF coordinates the cell cycle with DNA damage checkpoints. Lessons from knockout mouse models. Cell Div, 2, 22.   DOI
80 Gooding JM, Yap KL, Ikura M (2004). The cadherin-catenin complex as a focal point of cell adhesion and signalling: new insights from three-dimensional structures. Bioessays, 26, 497-11.   DOI
81 Guo YS, Dai YP, Li W, Liu LD (2011). Expression and significance of macrophage migration inhibitory factor in bladder urothelial cell carcinoma. Zhonghua Zhong Liu Za Zhi, 33, 28-1.
82 Hudson JD, Shoaibi MA, Maestro R, et al (1999). A proinflammatory cytokine inhibits p53 tumor suppressor activity. J Exp Med , 190, 1375-2.   DOI   ScienceOn
83 Hagemann T, Robinson SC, Thompson RG, et al (2007). Ovarian cancer cell-derived migration inhibitory factor enhances tumor growth, progression, and angiogenesis. Mol Cancer Ther, 6, 1993-2.   DOI
84 Hartwell LH, Kastan MB (1994). Cell cycle control and cancer. Science, 266, 1821-8.   DOI
85 Haupt Y, Maya R, Kazaz A, Oren M (1997). Mdm2 promotes the rapid degradation of p53. Nature, 387, 296-2   DOI
86 Hurlin PJ (2005). N-Myc functions in transcription and development. Birth Defects Res C Embryo Today, 75, 340-52.   DOI
87 Ichihara E, Kiura K, Tanimoto M (2011). Targeting angiogenesis in cancer therapy. Acta medica Okayama, 65, 353-2.
88 Jang BI, Li Y, Graham DY, Cen P (2011). The Role of CD44 in the Pathogenesis, Diagnosis, and Therapy of Gastric Cancer. Gut Liver, 5, 397-5.   DOI
89 Johnson JL, Pillai S, Pernazza D, et al (2011). Regulation of Matrix Metalloproteinase Genes by E2F transcription factors: Rb-Raf-1 interaction as a novel target for metastatic disease. Cancer Res.
90 Jung H, Seong HA and Ha H (2008). Critical role of cysteine residue 81 of macrophage migration inhibitory factor (MIF) in MIF-induced inhibition of p53 activity. J Biol Chem, 283, 20383-96.   DOI
91 Kleemann R, Hausser A, Geiger G, et al (2000). Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature, 408, 211-6.   DOI
92 Lane DP (1992). Cancer,p53, guardian of the genome. Nature, 358, 15-6.   DOI   ScienceOn
93 Kops GJ, Weaver BA, Cleveland DW (2005). On the road to cancer: aneuploidy and the mitotic checkpoint. Nat Rev Cancer, 5, 773-85.   DOI   ScienceOn
94 Krishnamachary B, Zagzag D, Nagasawa H, et al (2006). Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal cell carcinoma mediated by TCF3, ZFHX1A, and ZFHX1B. Cancer Res, 66 , 2725-1.   DOI
95 Krockenberger M, Dombrowski Y, Weidler C, et al (2008). Macrophage migration inhibitory factor contributes to the immune escape of ovarian cancer by down-regulating NKG2D. J Immunol, 180, 7338-48.   DOI
96 Lapidot T, Dar A and Kollet O (2005). How do stem cells find their way home? Blood, 106, 1901-10.   DOI
97 Lee EW, Oh W and Song J (2006). Jab1 as a mediator of nuclear export and cytoplasmic degradation of p53. Mol Cells, 22, 133-40.
98 Lee H, Rhee H, Kang HJ, et al (2008). Macrophage migration inhibitory factor may be used as an early diagnostic marker in colorectal carcinomas. Am J Clin Pathol, 129, 772-9.   DOI
99 Li Z, Lin SX, Liang YJ, Zong YS (2004). Effect of macrophage migration inhibitory factor (MIF) on expression of MMP- 2,MMP-9,and IL-8 in nasopharyngeal carcinoma cell strains. Ai Zheng, 23, 130-5.
100 Libra M, Scalisi A, Vella N, et al. (2009). Uterine cervical carcinoma: role of matrix metalloproteinases (review). Int J Oncol, 34, 897-3.
101 Liu L, Ji C, Chen J, et al (2008). A global genomic view of MIF knockdown-mediated cell cycle arrest. Cell Cycle, 7, 1678-92.   DOI