Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지
DOI QR코드

DOI QR Code

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)
  • Published : 2012.05.30
Download PDF
⟨ Previous Next ⟩

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

References

  1. 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. https://doi.org/10.1002/1097-0045(200101)46:1<68::AID-PROS1010>3.0.CO;2-2
  2. 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. https://doi.org/10.4155/fmc.10.281
  3. Bach JP, Rinn B, Meyer B, Dodel R, Bacher M (2008). Role of MIF in inflammation and tumorigenesis. Oncology, 75, 127-3. https://doi.org/10.1159/000155223
  4. 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. https://doi.org/10.1016/S0002-9440(10)63793-5
  5. 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. https://doi.org/10.1111/j.1349-7006.2002.tb01269.x
  6. 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. https://doi.org/10.1038/sj.gene.6363867
  7. 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. https://doi.org/10.1016/j.bbrc.2006.06.148
  8. Bergers G, Benjamin LE (2003). Tumorigenesis and the angiogenic switch. Nat Rev Cancer, 3, 401-10. https://doi.org/10.1038/nrc1093
  9. 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. https://doi.org/10.1038/nm1567
  10. Bifulco C, McDaniel K, Leng L, Bucala R (2008). Tumor growth-promoting properties of macrophage migration inhibitory factor. Curr Pharm Des, 14, 3790-801. https://doi.org/10.2174/138161208786898608
  11. 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. https://doi.org/10.1073/pnas.0701553104
  12. 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. https://doi.org/10.1016/j.jri.2007.07.004
  13. 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. https://doi.org/10.1073/pnas.0603921103
  14. Bucala R, Donnelly SC (2007). Macrophage migration inhibitory factor: a probable link between inflammation and cancer. Immunity, 26, 281-5. https://doi.org/10.1016/j.immuni.2007.03.005
  15. 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. https://doi.org/10.1006/geno.1996.4505
  16. Calandra T, Bernhagen J, Metz CN, et al (1995). MIF as a glucocorticoid-induced modulator of cytokine production. Nature, 377, 68-1. https://doi.org/10.1038/377068a0
  17. Cardozo T, Pagano M (2004). The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol, 5, 739-51. https://doi.org/10.1038/nrm1471
  18. 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. https://doi.org/10.1097/IGC.0b013e31821c45b7
  19. 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. https://doi.org/10.1073/pnas.150006697
  20. 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. https://doi.org/10.4049/jimmunol.1101468
  21. Colombo MP, Mantovani A (2005). Targeting myelomonocytic cells to revert inflammation-dependent cancer promotion. Cancer Res, 65, 9113-6. https://doi.org/10.1158/0008-5472.CAN-05-2714
  22. Conroy H, Mawhinney L and Donnelly SC (2010). Inflammation and cancer: macrophage migration inhibitory factor (MIF)- -the potential missing link. QJM, 103, 831-6. https://doi.org/10.1093/qjmed/hcq148
  23. 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.
  24. El-Omar EM, Ng MT, Hold GL (2008). Polymorphisms in Tolllike receptor genes and risk of cancer. Oncogene, 27, 244-2. https://doi.org/10.1038/sj.onc.1210912
  25. Fingerle-Rowson G, Petrenko O (2007). MIF coordinates the cell cycle with DNA damage checkpoints. Lessons from knockout mouse models. Cell Div, 2, 22. https://doi.org/10.1186/1747-1028-2-22
  26. 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. https://doi.org/10.1002/bies.20033
  27. 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.
  28. 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. https://doi.org/10.1158/1535-7163.MCT-07-0118
  29. Hartwell LH, Kastan MB (1994). Cell cycle control and cancer. Science, 266, 1821-8. https://doi.org/10.1126/science.7997877
  30. Haupt Y, Maya R, Kazaz A, Oren M (1997). Mdm2 promotes the rapid degradation of p53. Nature, 387, 296-2 https://doi.org/10.1038/387296a0
  31. Hudson JD, Shoaibi MA, Maestro R, et al (1999). A proinflammatory cytokine inhibits p53 tumor suppressor activity. J Exp Med , 190, 1375-2. https://doi.org/10.1084/jem.190.10.1375
  32. Hurlin PJ (2005). N-Myc functions in transcription and development. Birth Defects Res C Embryo Today, 75, 340-52. https://doi.org/10.1002/bdrc.20059
  33. Ichihara E, Kiura K, Tanimoto M (2011). Targeting angiogenesis in cancer therapy. Acta medica Okayama, 65, 353-2.
  34. 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. https://doi.org/10.5009/gnl.2011.5.4.397
  35. 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.
  36. 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. https://doi.org/10.1074/jbc.M800050200
  37. 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. https://doi.org/10.1038/35041591
  38. Kops GJ, Weaver BA, Cleveland DW (2005). On the road to cancer: aneuploidy and the mitotic checkpoint. Nat Rev Cancer, 5, 773-85. https://doi.org/10.1038/nrc1714
  39. 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. https://doi.org/10.1158/0008-5472.CAN-05-3719
  40. 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. https://doi.org/10.4049/jimmunol.180.11.7338
  41. Lane DP (1992). Cancer,p53, guardian of the genome. Nature, 358, 15-6. https://doi.org/10.1038/358015a0
  42. Lapidot T, Dar A and Kollet O (2005). How do stem cells find their way home? Blood, 106, 1901-10. https://doi.org/10.1182/blood-2005-04-1417
  43. 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.
  44. 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. https://doi.org/10.1309/GFCLLRH8A68XKMJN
  45. 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.
  46. Libra M, Scalisi A, Vella N, et al. (2009). Uterine cervical carcinoma: role of matrix metalloproteinases (review). Int J Oncol, 34, 897-3.
  47. 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. https://doi.org/10.4161/cc.7.11.6011
  48. 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.
  49. 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. https://doi.org/10.1016/j.cellsig.2005.06.013
  50. 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. https://doi.org/10.1038/sj.onc.1210318
  51. Lyapina S, Cope G, Shevchenko A, et al (2001). Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science, 292, 1382-5. https://doi.org/10.1126/science.1059780
  52. 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.
  53. Marhaba R, Zoller M (2004). CD44 in cancer progression: adhesion, migration and growth regulation. J Mol Histol, 35, 211-31.
  54. Medema RH, Macurek L (2011). Checkpoint control and cancer. Oncogene.
  55. 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. https://doi.org/10.4049/jimmunol.177.12.8730
  56. 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. https://doi.org/10.1016/j.bcp.2009.12.021
  57. 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. https://doi.org/10.1073/pnas.012511599
  58. 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. https://doi.org/10.1074/jbc.274.25.18100
  59. 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 https://doi.org/10.7314/APJCP.2012.13.2.607
  60. Nakayama KI, Nakayama K (2006). Ubiquitin ligases: cell-cycle control and cancer. Nat Rev Cancer, 6, 369-81. https://doi.org/10.1038/nrc1881
  61. 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. https://doi.org/10.1038/sj.emboj.7601564
  62. 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. https://doi.org/10.4161/cc.6.9.4163
  63. 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. https://doi.org/10.4049/jimmunol.170.6.3337
  64. 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. https://doi.org/10.1089/10799900050151012
  65. 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. https://doi.org/10.1111/j.1749-6632.2003.tb03220.x
  66. 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.
  67. 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. https://doi.org/10.1371/journal.pone.0002215
  68. 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. https://doi.org/10.1016/j.bbamcr.2003.12.002
  69. 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. https://doi.org/10.1046/j.1365-2567.1999.00868.x
  70. Pollard JW (2004). Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer, 4, 71-8. https://doi.org/10.1038/nrc1256
  71. 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. https://doi.org/10.1038/sj.onc.1209395
  72. 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. https://doi.org/10.1038/sj.onc.1207490
  73. 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. https://doi.org/10.1097/01.sla.0000168555.97710.bb
  74. 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. https://doi.org/10.1074/jbc.M704898200
  75. 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.
  76. Sen S and Hopwood V (2011). Molecular cytogenetic evidence for multistep tumorigenesis: implications for risk assessment and early detection. Cancer Biomark, 9, 113-32. https://doi.org/10.3233/CBM-2011-0171
  77. 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. https://doi.org/10.1006/bbrc.1999.1584
  78. 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. https://doi.org/10.1074/jbc.M400150200
  79. 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. https://doi.org/10.1016/j.immuni.2006.08.020
  80. 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.
  81. 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. https://doi.org/10.1186/1471-2407-11-136
  82. 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. https://doi.org/10.1038/35070076
  83. Steegenga WT, van der Eb AJ, Jochemsen AG (1996). How phosphorylation regulates the activity of p53. J Mol Biol, 263, 103-3. https://doi.org/10.1006/jmbi.1996.0560
  84. 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. https://doi.org/10.1158/1078-0432.CCR-07-1167
  85. Strieter RM (2005). Masters of angiogenesis. Nat Med, 11, 925-7. https://doi.org/10.1038/nm0905-925
  86. 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.
  87. 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. https://doi.org/10.1073/pnas.93.11.5191
  88. 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. https://doi.org/10.1093/protein/9.8.631
  89. Talos F, Mena P, Fingerle-Rowson G, Moll U, Petrenko O (2005). MIF loss impairs Myc-induced lymphomagenesis. Cell Death Differ, 12, 1319-8. https://doi.org/10.1038/sj.cdd.4401653
  90. 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.
  91. Thiele M and Bernhagen J (2005). Link between macrophage migration inhibitory factor and cellular redox regulation. Antioxid Redox Signal, 7, 1234-48. https://doi.org/10.1089/ars.2005.7.1234
  92. 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. https://doi.org/10.1016/S0960-9822(99)80290-5
  93. 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. https://doi.org/10.1210/jc.2010-0417
  94. 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.
  95. 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. https://doi.org/10.1073/pnas.0402770101
  96. 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. https://doi.org/10.1158/0008-5472.CAN-06-3292
  97. 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. https://doi.org/10.1016/S0076-6879(07)35018-0
  98. 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. https://doi.org/10.1016/j.canlet.2007.11.028
  99. 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. https://doi.org/10.1016/j.leukres.2010.03.030
  100. Yamasaki L, Pagano M (2004). Cell cycle, proteolysis and cancer. Curr Opin Cell Biol, 16, 623-8. https://doi.org/10.1016/j.ceb.2004.08.005
  101. 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. https://doi.org/10.1016/S1097-2765(02)00784-0

Cited by

  1. Prenatal Arsenic Exposure and Shifts in the Newborn Proteome: Interindividual Differences in Tumor Necrosis Factor (TNF)-Responsive Signaling vol.139, pp.2, 2014, https://doi.org/10.1093/toxsci/kfu053
  2. Are Neutrophil/Lymphocyte and Platelet/Lymphocyte Ratios Associated with Endometrial Precancerous and Cancerous Lesions in Patients with Abnormal Uterine Bleeding? vol.15, pp.4, 2014, https://doi.org/10.7314/APJCP.2014.15.4.1689
  3. The Role of MIF in Type 1 and Type 2 Diabetes Mellitus vol.2014, pp.2314-6753, 2014, https://doi.org/10.1155/2014/804519
  4. Serum levels of macrophage migration-inhibitory factor (MIF) have diagnostic, predictive and prognostic roles in epithelial ovarian cancer patients vol.35, pp.4, 2014, https://doi.org/10.1007/s13277-013-1438-z
  5. Contribution of Macrophage Migration Inhibitory Factor -173G/C Gene Polymorphism to the Risk of Cancer in Chinese Population vol.16, pp.11, 2015, https://doi.org/10.7314/APJCP.2015.16.11.4597
  6. Relations of Platelet Indices with Endometrial Hyperplasia and Endometrial Cancer vol.16, pp.12, 2015, https://doi.org/10.7314/APJCP.2015.16.12.4905
  7. Could the Platelet-to-Lymphocyte Ratio be a Novel Marker for Predicting Invasiveness of Cervical Pathologies? vol.16, pp.3, 2015, https://doi.org/10.7314/APJCP.2015.16.3.923
  8. Association between preoperative C-reactive protein level and colorectal cancer survival: a meta-analysis vol.26, pp.11, 2015, https://doi.org/10.1007/s10552-015-0663-8
  9. Pretreatment prognostic nutritional index is a significant predictor of prognosis in patients with cervical cancer treated with concurrent chemoradiotherapy vol.5, pp.5, 2016, https://doi.org/10.3892/mco.2016.1028
  10. Macrophage Migration Inhibitory Factor (MIF): Biological Activities and Relation with Cancer vol.23, pp.2, 2017, https://doi.org/10.1007/s12253-016-0138-6
  11. Single and combined use of red cell distribution width, mean platelet volume, and cancer antigen 125 for differential diagnosis of ovarian cancer and benign ovarian tumors vol.11, pp.1, 2018, https://doi.org/10.1186/s13048-018-0382-3
  12. Macrophage migration inhibitory factor as an incriminating agent in vitiligo vol.93, pp.2, 2018, https://doi.org/10.1590/abd1806-4841.20186068
  13. Optimization of Pyrazoles as Phenol Surrogates to Yield Potent Inhibitors of Macrophage Migration Inhibitory Factor vol.13, pp.11, 2018, https://doi.org/10.1002/cmdc.201800158
  14. Roles of macrophage migration inhibitory factor in Guillain-Barré syndrome and experimental autoimmune neuritis: beneficial or harmful? vol.22, pp.7, 2018, https://doi.org/10.1080/14728222.2018.1484109