Tumor growth-promoting properties of macrophage migration inhibitory factor

Current Pharmaceutical Design

Volumn 14, Issue 36, 2008, Pages 3790-3801

  Bifulco, Carlo ^a   McDaniel, Katy ^a   Leng, Lin ^a   Bucala, Richard ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; CD44; CD74; HIF 1; Macrophage migration inhibitory factor; P53; TAM; Tumor progression

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; CHEMOKINE RECEPTOR CXCR4; HYDROCORTISONE; HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MACROPHAGE MIGRATION INHIBITION FACTOR; MACROPHAGE MIGRATION INHIBITION FACTOR MONOCLONAL ANTIBODY; MITOGEN ACTIVATED PROTEIN KINASE 1; MONOCLONAL ANTIBODY; MYC PROTEIN; NONSTEROID ANTIINFLAMMATORY AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN E2; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN KINASE B; PROTEIN P53; TRANSCRIPTION FACTOR ETS; UNCLASSIFIED DRUG;

APOPTOSIS; B CELL LYMPHOMA; BLADDER CANCER; BREAST CARCINOMA; CANCER INVASION; CARCINOGENESIS; CELL HETEROGENEITY; CELL PROLIFERATION; CHROMOSOME 22Q; COLON CANCER; COLON POLYPOSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC ASSOCIATION; GENETIC TRANSFORMATION; HUMAN; LUNG CANCER; METASTASIS POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REDOX STRESS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR ASSOCIATED LEUKOCYTE; CELL DIVISION; CELL TRANSFORMATION; CHEMISTRY; CYTOLOGY; DISEASE COURSE; GENETICS; MACROPHAGE; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGY; PROTEIN CONFORMATION; VASCULARIZATION;

CELL DIVISION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; HUMANS; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MACROPHAGES; NEOPLASM INVASIVENESS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

EID: 61449209186     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161208786898608     Document Type: Review

References (193)

1. Kuper H, Adami HO, Trichopoulos D. Infections as a major preventable cause of human cancer. J Intern Med 2000; 248(3): 171-83.
2. Balkwill F, Mantovani A. Inflammation and cancer: Back to Virchow? Lancet 2001; 357(9255): 539-45.
3. Warzocha K, Ribeiro P, Bienvenu J, Roy P, Charlot C, Rigal D, et al. Genetic polymorphisms in the tumor necrosis factor locus influence non-Hodgkin's lymphoma outcome. Blood 1998; 91(10): 3574-81.
4. El-Omar EM, Carrington M, Chow WH, McColl KE, Bream JH, Young HA, et al. The role of interleukin-1 polymorphisms in the pathogenesis of gastric cancer. Nature 2001; 412(6842): 99.
5. El-Omar EM, Carrington M, Chow WH, McColl KE, Bream JH, Young HA, et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 2000; 404(6776): 398-402.
6. El-Omar EM, Ng MT, Hold GL. Polymorphisms in Toll-like receptor genes and risk of cancer. Oncogene 2008; 27(2): 244-52.
7. Xu XC. COX-2 inhibitors in cancer treatment and prevention, a recent development. Anticancer Drugs 2002; 13(2): 127-37.
8. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002; 420(6917): 860-7.
9. Karin M, Greten FR. NF-kappaB: Linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 2005; 5(10): 749-59.
10. Baugh JA, Bucala R. Macrophage migration inhibitory factor. Crit Care Med 2002; 30(1 Suppl): S27-35.
11. Bucala R. MIF rediscovered: Cytokine, pituitary hormone, and glucocorticoid-induced regulator of the immune response. FASEB J 1996; 10(14): 1607-13.
12. Bacher M, Metz CN, Calandra T, Mayer K, Chesney J, Lohoff M, et al. An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc Natl Acad Sci USA 1996; 93(15): 7849-54.
13. Bernhagen J, Mitchell RA, Calandra T, Voelter W, Cerami A, Bucala R. Purification, bioactivity, and secondary structure analysis of mouse and human macrophage migration inhibitory factor (MIF). Biochemistry 1994; 33(47): 14144-55.
14. Bucala R, Donnelly SC. Macrophage migration inhibitory factor: A probable link between inflammation and cancer. Immunity 2007; 26: 281-5.
15. Bernhagen J, Calandra T, Bucala R. The emerging role of MIF in septic shock and infection. Biotherapy 1994; 8(2): 123-7.
16. Eibl MM, Sitko C. MIF production of lymphocytes from patients with rheumatoid arthritis with antigen-antibody complexes. Ann Rheum Dis 1975; 34(2): 117-21.
17. Larson DF, Horak K. Macrophage migration inhibitory factor: Controller of systemic inflammation. Crit Care 2006; 10(2): 138.
18. Sorg C, Michels E, Malorny U, Neumann C. Migration inhibitory factors and macrophage differentiation. Springer Semin Immunopathol 1984; 7(4): 311-20.
19. Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, et al. MIF as a glucocorticoid-induced modulator of cytokine production. Nature 1995; 377(6544): 68-71.
20. Flaster H, Bernhagen J, Calandra T, Bucala R. The macrophage migration inhibitory factor-glucocorticoid dyad: Regulation of inflammation and immunity. Mol Endocrinol 2007; 21(6): 1267-80.
21. Bucala R. MIF, a previously unrecognized pituitary hormone and macrophage cytokine, is a pivotal mediator in endotoxic shock. Circ Shock 1994; 44(1): 35-9.
22. Bucala R, Donnelly SC. Macrophage migration inhibitory factor: A probable link between inflammation and cancer. Immunity 2007; 26(3): 281-5.
23. Cordon-Cardo C, Prives C. At the crossroads of inflammation and tumorigenesis. J Exp Med 1999; 190(10): 1367-70.
24. Budarf M, McDonald T, Sellinger B, Kozak C, Graham C, Wistow G. Localization of the human gene for macrophage migration inhibitory factor (MIF) to chromosome 22q11.2. Genomics 1997; 39(2): 235-6.
25. Baugh JA, Chitnis S, Donnelly SC, Monteiro J, Lin X, Plant BJ, et al. A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis. Genes Immun 2002; 3(3): 170-6.
26. Donn R, Alourfi Z, De Benedetti F, Meazza C, Zeggini E, Lunt M, et al. Mutation screening of the macrophage migration inhibitory factor gene: Positive association of a functional polymorphism of macrophage migration inhibitory factor with juvenile idiopathic arthritis. Arthritis Rheum 2002; 46(9): 2402-9.
27. De Benedetti F, Meazza C, Vivarelli M, Rossi F, Pistorio A, Lamb R, et al. Functional and prognostic relevance of the -173 polymorphism of the macrophage migration inhibitory factor gene in systemic-onset juvenile idiopathic arthritis. Arthritis Rheum 2003; 48(5): 1398-407.
28. Dambacher J, Staudinger T, Seiderer J, Sisic Z, Schnitzler F, Pfennig S, et al. Macrophage migration inhibitory factor (MIF) -173G/C promoter polymorphism influences upper gastrointestinal tract involvement and disease activity in patients with Crohn's disease. Inflamm Bowel Dis 2007; 13(1): 71-82.
29. Sanchez E, Gomez LM, Lopez-Nevot MA, Gonzalez-Gay MA, Sabio JM, Ortego-Centeno N, et al. Evidence of association of macrophage migration inhibitory factor gene polymorphisms with systemic lupus erythematosus. Genes Immun 2006; 7(5): 433-6.
30. Wu SP, Leng L, Feng Z, Liu N, Zhao H, McDonald C, et al. Macrophage migration inhibitory factor promoter polymorphisms and the clinical expression of scleroderma. Arthritis Rheum 2006; 54(11): 3661-9.
31. Shimizu T, Hizawa N, Honda A, Zhao Y, Abe R, Watanabe H, et al. Promoter region polymorphism of macrophage migration inhibitory factor is strong risk factor for young onset of extensive alopecia areata. Genes Immun 2005; 6(4): 285-9.
32. Yamaguchi E, Nishihira J, Shimizu T, Takahashi T, Kitashiro N, Hizawa N, et al. Macrophage migration inhibitory factor (MIF) in bronchial asthma. Clin Exp Allergy 2000; 30(9): 1244-9.
33. Meyer-Siegler KL, Vera PL, Iczkowski KA, Bifulco C, Lee A, Gregersen PK, et al. Macrophage migration inhibitory factor (MIF) gene polymorphisms are associated with increased prostate cancer incidence. Genes Immun 2007; 8(8): 646-52.
34. Arisawa T, Tahara T, Shibata T, Nagasaka M, Nakamura M, Kamiya Y, et al. Functional promoter polymorphisms of the macrophage migration inhibitory factor gene in gastric carcinogenesis. Oncol Rep 2008; 19(1): 223-8.
35. Sun HW, Bernhagen J, Bucala R, Lolis E. Crystal structure at 2.6-A resolution of human macrophage migration inhibitory factor. Proc Natl Acad Sci USA 1996; 93(11): 5191-6.
36. Taylor AB, Johnson WH, Jr., Czerwinski RM, Li HS, Hackert ML, Whitman CP. Crystal structure of macrophage migration inhibitory factor complexed with (E)-2-fluoro-p-hydroxycinnamate at 1.8 A resolution: implications for enzymatic catalysis and inhibition. Biochemistry 1999; 38(23): 7444-52.
37. Rosengren E, Bucala R, Aman P, Jacobsson L, Odh G, Metz CN, et al. The immunoregulatory mediator macrophage migration inhibitory factor MIF catalyzes a tautornerization reaction. Mol Med 1996; 2: 143-9.
38. Thiele M, Bernhagen J. Link between macrophage migration inhibitory factor and cellular redox regulation. Antioxid Redox Signal 2005; 7(9-10): 1234-48.
39. Nguyen MT, Lue H, Kleemann R, Thiele M, Tolle G, Finkelmeier D, et al. The cytokine macrophage migration inhibitory factor reduces pro-oxidative stress-induced apoptosis. J Immunol 2003; 170(6): 3337-47.
40. Senter RP, Al-Abed Y, Metz CN, Benigni F, Mitchell RA, Chesney J, et al. Inhibition of macrophage migration inhhibitory factor MIF tautomerase and biological activities by acetaminophen metabolites. Proc Natl Acad Sci USA 2002; 99: 144-9.
41. Dios A, Mitchell RA, Aljabari B, Lubetsky J, O'Connor K-A, Liac H, et al. Inhibition of MIF bioactivity by rational design of pharmacological inhibitors of MIF tautomerase activity. J Med Chem 2002; 45: 2410-6.
42. Bacher M, Meinhardt A, Lan HY, Mu W, Metz CN, Chesney JA, et al. Migration inhibitory factor expression in experimentally induced endotoxemia. Am J Pathol 1997; 150(1): 235-46.
43. Calandra T, Bernhagen J, Mitchell RA, Bucala R. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 1994; 179(6): 1895-902.
44. Kleemann R, Hausser A, Geiger G, Mischke R, Burger-Kentischer A, Flieger O, et al. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature 2000; 408(6809): 211-6.
45. Lue H, Thiele M, Franz J, Dahl E, Speckgens S, Leng L, et al. Macrophage migration inhibitory factor (MIF) promotes cell survival by activation of the Akt pathway and role for CSN5/JAB1 in the control of autocrine MIF activity. Oncogene 2007; 26(35): 5046-59.
46. Kobayashi S, Satomura K, Levsky JM, Sreenath T, Wistow GJ, Semba I, et al. Expression pattern of macrophage migration inhibitory factor during embryogenesis. Mech Dev 1999; 84(1-2): 153-6.
47. Bozza M, Satoskar AR, Lin G, Lu B, Humbles AA, Gerard C, et al. Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J Exp Med 1999; 189(2): 341-6.
48. Fingerle-Rowson G, Petrenko O, Metz CN, Forsthuber TG, Mitchell R, Huss RR, et al. The p53-dependent effects of macrophage migration inhibitory factor revealed by gene targeting. Proc Natl Acad Sci USA 2003; 100: 9354-9.
49. Ito K, Yoshiura Y, Ototake M, Nakanishi T. Macrophage migration inhibitory factor (MIF) is essential for development of zebrafish, Danio rerio. Dev Comp Immunol 2007.
50. Suzuki M, Takamura Y, Maeno M, Tochinai S, Iyaguchi D, Tanaka I, et al. Xenopus laevis macrophage migration inhibitory factor is essential for axis formation and neural development. J Biol Chem 2004; 279(20): 21406-14.
51. Shi X, Leng L, Wang T, Wang W, Du X, Li J, et al. CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 2006; 25(4): 595-606.
52. Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, et al. MIF signal transduction initiated by binding to CD74. J Exp Med 2003; 197(11): 1467-76.
53. Bernhagen J, Krohn R, Lue H, Gregory JL, Zernecke A, Koenen RR, et al. MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med 2007; 13(5): 587-96.
54. Ong GL, Goldenberg DM, Hansen HJ, Mattes MJ. Cell surface expression and metabolism of major histocompatibility complex class II invariant chain (CD74) by diverse cell lines. Immunology 1999; 98(2): 296-302.
55. Wraight CJ, van Endert P, Moller P, Lipp J, Ling NR, MacLennan IC, et al. Human major histocompatibility complex class II invariant chain is expressed on the cell surface. J Biol Chem 1990; 265(10): 5787-92.
56. Rubinfeld H, Seger R. The ERK cascade as a prototype of MAPK signaling pathways. Methods Mol Biol 2004; 250: 1-28.
57. Mitchell RA, Metz CN, Peng T, Bucala R. Sustained mitogen-activated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF). Regulatory role in cell proliferation and glucocorticoid action. J Biol Chem 1999; 274(25): 18100-6.
58. Swant JD, Rendon BE, Symons M, Mitchell RA. Rho GTPase-dependent signaling is required for macrophage migration inhibitory factor-mediated expression of cyclin D1. J Biol Chem 2005; 280(24): 23066-72.
59. Binsky I, Haran M, Starlets D, Gore Y, Lantner F, Harpaz N, et al. IL-8 secreted in a macrophage migration-inhibitory factor- and CD74-dependent manner regulates B cell chronic lymphocytic leukemia survival. Proc Natl Acad Sci USA 2007; 104(33): 13408-13.
60. Wei N, Deng XW. The COP9 signalosome. Annu Rev Cell Dev Biol 2003; 19: 261-86.
61. Chamovitz DA, Segal D. JAB1/CSN5 and the COP9 signalosome. A complex situation. EMBO Rep 2001; 2(2): 96-101.
62. Huang J, Yuan H, Lu C, Liu X, Cao X, Wan M. Jab1 mediates protein degradation of the Rad9-Rad1-Hus1 checkpoint complex. J Mol Biol 2007; 371(2): 514-27.
63. Zhang XC, Chen J, Su CH, Yang HY, Lee MH. Roles for CSN5 in control of p53/MDM2 activities. J Cell Biochem 2007; 103(4): 1219-30.
64. Lue H, Kapurniotu A, Fingerle-Rowson G, Roger T, Leng L, Thiele M, et al. 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 2006; 18(5): 688-703.
65. Liu X, Pan Z, Zhang L, Sun Q, Wan J, Tian C, et al. JAB1 accelerates mitochondrial apoptosis by interaction with proapoptotic BclGs. Cell Signal 2008; 20(1): 230-40.
66. Burger-Kentischer A, Finkelmeier D, Thiele M, Schmucker J, Geiger G, Tovar GE, et al. Binding of JAB1/CSN5 to MIF is mediated by the MPN domain but is independent of the JAMM motif. FEBS Lett 2005; 579(7): 1693-701.
67. Cope GA, Deshaies RJ. Targeted silencing of Jab1/Csn5 in human cells downregulates SCF activity through reduction of F-box protein levels. BMC Biochem 2006; 7: 1.
68. Nemajerova A, Mena P, Fingerle-Rowson G, Moll UM, Petrenko O. Impaired DNA damage checkpoint response in MIF-deficient mice. EMBO J 2007; 26(4): 987-97.
69. Kondo N, Ishii Y, Son A, Sakakura-Nishiyama J, Kwon YW, Tanito M, et al. Cysteine-dependent immune regulation by TRX and MIF/GIF family proteins. Immunol Lett 2004; 92(1-2): 143-7.
70. Nguyen MT, Beck J, Lue H, Funfzig H, Kleemann R, Koolwijk P, et al. A 16-residue peptide fragment of macrophage migration inhibitory factor, MIF-(50-65), exhibits redox activity and has MIF-like biological functions. J Biol Chem 2003; 278(36): 33654-71.
71. Biaglow JE, Miller RA. The thioredoxin reductase/thioredoxin system: novel redox targets for cancer therapy. Cancer Biol Ther 2005; 4(1): 6-13.
72. Bucala R, Donnelly SC. Macrophage migration inhibitory factor: A probable link between inflammation and cancer. Immunity 2007; 26: 281-5.
73. Bernhagen J. MIF redox activity. In: Bucala R Ed. MIF: A most interesting factor. Imperial College Press and World Scientific Publishing: London, UK 2007; pp. 65-94.
74. Gore Y, Starlets D, Maharshak N, Becker-Herman S, Kaneyuki U, Leng L, et al. Macrophage migration inhibitory factor (MIF) induces B cell survival by activation of a CD74/CD44 receptor complex. J Biol Chem 2007.
75. Ponta H, Sherman L, Herrlich PA. CD44: From adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 2003; 4(1): 33-45.
76. Marhaba R, Zoller M. CD44 in cancer progression: Adhesion, migration and growth regulation. J Mol Histol 2004; 35(3): 211-31.
77. Lim SD, Young AN, Paner GP, Amin MB. Prognostic role of CD44 cell adhesion molecule expression in primary and metastatic renal cell carcinoma: A clinicopathologic study of 125 cases. Virchows Arch 2008; 452(1): 49-55.
78. Lee LN, Kuo SH, Lee YC, Chang YL, Chang HC, Jan IS, et al. CD44 splicing pattern is associated with disease progression in pulmonary adenocarcinoma. J Formos Med Assoc 2005; 104(8): 541-8.
79. Nelson AD, Grandis JR. The role of CD44 in HNSCC. Cancer Biol Ther 2007; 6(1): 125-6.
80. Lee SM, Lee KE, Chang HJ, Choi MY, Cho MS, Min SK, et al. Prognostic Significance of CD44s Expression in Biliary Tract Cancers. Ann Surg Oncol 2008.
81. Hurt EM, Kawasaki BT, Klarmann GJ, Thomas SB, Farrar WL. CD44(+)CD24(-) prostate cells are early cancer progenitor/stem cells that provide a model for patients with poor prognosis. Br J Cancer 2008; 98(4): 756-65.
82. Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV, Varticovski L. Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res 2008; 10(1): R10.
83. Harper LJ, Piper K, Common J, Fortune F, Mackenzie IC. Stem cell patterns in cell lines derived from head and neck squamous cell carcinoma. J Oral Pathol Med 2007; 36(10): 594-603.
84. Fillmore C, Kuperwasser C. Human breast cancer stem cell markers CD44 and CD24: Enriching for cells with functional properties in mice or in man? Breast Cancer Res 2007; 9(3): 303.
85. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH, et al. CD44+/CD24-breast cancer cells exhibit enhanced invasive properties: An early step necessary for metastasis. Breast Cancer Res 2006; 8(5): R59.
86. Lapidot T, Dar A, Kollet O. How do stem cells find their way home? Blood 2005; 106(6): 1901-10.
87. Draffin JE, McFarlane S, Hill A, Johnston PG, Waugh DJ. CD44 potentiates the adherence of metastatic prostate and breast cancer cells to bone marrow endothelial cells. Cancer Res 2004; 64(16): 5702-11.
88. Pouysségur J, Dayan F, Mazure NM. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006; 441(7092): 437-43.
89. Liao D, Johnson RS. Hypoxia: A key regulator of angiogenesis in cancer. Cancer Metastasis Rev 2007; 26(2): 281-90.
90. Maxwell PH. The HIF pathway in cancer. Semin Cell Dev Biol 2005; 16(4-5): 523-30.
91. Koong AC, Denko NC, Hudson KM, Schindler C, Swiersz L, Koch C, et al. Candidate genes for the hypoxic tumor phenotype. Cancer Res 2000; 60(4): 883-7.
92. Bacher M, Schrader J, Thompson N, Kuschela K, Gemsa D, Waeber G, et al. Up-regulation of macrophage migration inhibitory factor gene and protein expression in glial tumor cells during hypoxic and hypoglycemic stress indicates a critical role for angiogenesis in glioblastoma multiforme. Am J Pathol 2003; 162(1): 11-7.
93. Baugh JA, Gantier M, Li L, Byrne A, Buckley A, Donnelly SC. Dual regulation of macrophage migration inhibitory factor (MIF) expression in hypoxia by CREB and HIF-1. Biochem Biophys Res Commun 2006; 347(4): 895-903.
94. Winner M, Koong AC, Rendon BE, Zundel W, Mitchell RA. Amplification of tumor hypoxic responses by macrophage migration inhibitory factor-dependent hypoxia-inducible factor stabilization. Cancer Res 2007; 67(1): 186-93.
95. Maity A, Koumenis C. HIF and MIF - a nifty way to delay senescence? Genes Dev 2006; 20(24): 3337-41.
96. Welford SM, Bedogni B, Gradin K, Poellinger L, Broome Powell M, Giaccia AJ. HIF1alpha delays premature senescence through the activation of MIF. Genes Dev 2006; 20(24): 3366-71.
97. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegue E, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer cell 2008; 13(3): 206-20.
98. Larsen M, Tazzyman S, Lund EL, Junker N, Lewis CE, Kristjansen PE, et al. Hypoxia-induced secretion of macrophage migration-inhibitory factor from MCF-7 breast cancer cells is regulated in a hypoxia-inducible factor-independent manner. Cancer Lett 2008.
99. Romer L, Klein C, Dehner A, Kessler H, Buchner J. p53 - a natural cancer killer: Structural insights and therapeutic concepts. Angew Chem Int Ed Engl 2006; 45(39): 6440-60.
100. Ryan KM, Phillips AC, Vousden KH. Regulation and function of the p53 tumor suppressor protein. Curr Opin Cell Biol 2001; 13(3): 332-7.
101. Hudson JD, Shoaibi MA, Maestro R, Carnero A, Hannon GJ, Beach DH. A proinflammatory cytokine inhibits p53 tumor suppressor activity. J Exp Med 1999; 190(10): 1375-82.
102. Mitchell RA, Liao H, Chesney J, Fingerle-Rowson G, Baugh J, David J, et al. Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: Regulatory role in the innate immune response. Proc Natl Acad Sci USA 2002; 99(1): 345-50.
103. Liao H, Bucala R, Mitchell RA. Adhesion-dependent signaling by macrophage migration inhibitory factor (MIF). J Biol Chem 2003; 278(1): 76-81.
104. Lee EW, Oh W, Song J. Jab1 as a mediator of nuclear export and cytoplasmic degradation of p53. Mol Cells 2006; 22(2): 133-40.
105. Petrenko O, Fingerle-Rowson G, Peng T, Mitchell RA, Metz CN. Macrophage migration inhibitory factor deficiency is associated with altered cell growth and reduced susceptibility to Ras-mediated transformation. J Biol Chem 2003; 278(13): 11078-85.
106. Fingerle-Rowson G, Petrenko O, Metz CN, Forsthuber TG, Mitchell R, Huss R, et al. The p53-dependent effects of macrophage migration inhibitory factor revealed by gene targeting. Proc Natl Acad Sci USA 2003; 100(16): 9354-9.
107. Talos F, Mena P, Fingerle-Rowson G, Moll U, Petrenko O. MIF loss impairs Myc-induced lymphomagenesis. Cell Death Differ 2005; 12(10): 1319-28.
108. Nemajerova A, Moll UM, Petrenko O, Fingerle-Rowson G. Macrophage migration inhibitory factor coordinates DNA damage response with the proteasomal control of the cell cycle. Cell Cycle 2007; 6(9): 1030-4.
109. Taylor JA, 3rd, Kuchel GA, Hegde P, Voznesensky OS, Claffey K, Tsimikas J, et al. Null mutation for macrophage migration inhibitory factor (MIF) is associated with less aggressive bladder cancer in mice. BMC Cancer 2007; 7: 135.
110. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003; 3(6): 401-10.
111. Folkman J. The role of angiogenesis in tumor growth. Semin Cancer Biol 1992; 3(2): 65-71.
112. Chesney J, Metz C, Bacher M, Peng T, Meinhardt A, Bucala R. An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Mol Med 1999; 5(3): 181-91.
113. Shimizu T, Abe R, Nakamura H, Ohkawara A, Suzuki M, Nishihira J. High expression of macrophage migration inhibitory factor in human melanoma cells and its role in tumor cell growth and angiogenesis. Biochem Biophys Res Commun 1999; 264(3): 751-8.
114. Nishihira J, Ishibashi T, Fukushima T, Sun B, Sato Y, Todo S. Macrophage migration inhibitory factor (MIF): Its potential role in tumor growth and tumor-associated angiogenesis. Ann N Y Acad Sci 2003; 995: 171-82.
115. Fukushima T, Nishihira J, Yoshiki T, Iwabuchi K, Iwabuchi C, Yamasaki Y, et al. Evidence of dual function of macrophage migration inhibitory factor relevant to tumor progression and regression. Int J Mol Med 2005; 16(1): 119-26.
116. Wilson JM, Coletta PL, Cuthbert RJ, Scott N, MacLennan K, Hawcroft G, et al. Macrophage migration inhibitory factor promotes intestinal tumorigenesis. Gastroenterology 2005; 129(5): 1485-503.
117. White ES, Flaherty KR, Carskadon S, Brant A, Iannettoni MD, Yee J, et al. Macrophage migration inhibitory factor and CXC chemokine expression in non-small cell lung cancer: Role in angiogenesis and prognosis. Clin Cancer Res 2003; 9(2): 853-60.
118. Ren Y, Tsui HT, Poon RT, Ng IO, Li Z, Chen Y, et al. Macrophage migration inhibitory factor: Roles in regulating tumor cell migration and expression of angiogenic factors in hepatocellular carcinoma. Int J Cancer 2003; 107(1): 22-9.
119. Xu X, Wang B, Ye C, Yao C, Lin Y, Huang X, et al. Overexpression of macrophage migration inhibitory factor induces angiogenesis in human breast cancer. Cancer Lett 2008; 261(2): 147-57.
120. Ren Y, Law S, Huang X, Lee PY, Bacher M, Srivastava G, et al. 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 2005; 242(1): 55-63.
121. Amin MA, Volpert OV, Woods JM, Kumar P, Harlow LA, Koch AE. Migration inhibitory factor mediates angiogenesis via mitogen-activated protein kinase and phosphatidylinositol kinase. Circ Res 2003; 93(4): 321-9.
122. Damico RL, Chesley A, Johnston L, Bind EP, Amaro E, Nijmeh J, et al. Macrophage Migration Inhibitory Factor Governs Endothelial Cell Sensitivity to LPS-Induced Apoptosis. Am J Respir Cell Mol Biol 2008.
123. Sun B, Nishihira J, Suzuki M, Fukushima N, Ishibashi T, Kondo M, et al. Induction of macrophage migration inhibitory factor by lysophosphatidic acid: Relevance to tumor growth and angiogenesis. Int J Mol Med 2003; 12(4): 633-41.
124. Shimizu T, Nishihira J, Watanabe H, Abe R, Honda A, Ishibashi T, et al. Macrophage migration inhibitory factor is induced by thrombin and factor Xa in endothelial cells. J Biol Chem 2004; 279(14): 13729-37.
125. Shun CT, Lin JT, Huang SP, Lin MT, Wu MS. Expression of macrophage migration inhibitory factor is associated with enhanced angiogenesis and advanced stage in gastric carcinomas. World J Gastroenterol 2005; 11(24): 3767-71.
126. Hira E, Ono T, Dhar DK, El-Assal ON, Hishikawa Y, Yamanoi A, et al. Overexpression of macrophage migration inhibitory factor induces angiogenesis and deteriorates prognosis after radical resection for hepatocellular carcinoma. Cancer 2005; 103(3): 588-98.
127. Meyer-Siegler KL, Iczkowski KA, Leng L, Bucala R, Vera PL. Inhibition of macrophage migration inhibitory factor or its receptor (CD74) attenuates growth and invasion of DU-145 prostate cancer cells. J Immunol 2006; 177(12): 8730-9.
128. Hardman MJ, Waite A, Zeef L, Burow M, Nakayama T, Ashcroft GS. Macrophage migration inhibitory factor: A central regulator of wound healing. Am J Pathol 2005; 167(6): 1561-74.
129. Ashcroft GS, Mills SJ, Lei K, Gibbons L, Jeong MJ, Taniguchi M, et al. Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J Clin Invest 2003; 111(9): 1309-18.
130. Shimizu T. Role of macrophage migration inhibitory factor (MIF) in the skin. J Dermatol Sci 2005; 37(2): 65-73.
131. Zhao Y, Shimizu T, Nishihira J, Koyama Y, Kushibiki T, Honda A, et al. Tissue regeneration using macrophage migration inhibitory factor-impregnated gelatin microbeads in cutaneous wounds. Am J Pathol 2005; 167(6): 1519-29.
132. Hagemann T, Wilson J, Kulbe H, Li NF, Leinster DA, Charles K, et al. Macrophages induce invasiveness of epithelial cancer cells via NF-kappa B and JNK. J Immunol 2005; 175(2): 1197-205.
133. Sun B, Nishihira J, Yoshiki T, Kondo M, Sato Y, Sasaki F, et al. Macrophage migration inhibitory factor promotes tumor invasion and metastasis via the Rho-dependent pathway. Clin Cancer Res 2005; 11(3): 1050-8.
134. Rendon BE, Roger T, Teneng I, Zhao M, Al-Abed Y, Calandra T, et al. Regulation of human lung adenocarcinoma cell migration and invasion by macrophage migration inhibitory factor. J Biol Chem 2007; 282(41): 29910-8.
135. Li Z, Ren Y, Wu QC, Lin SX, Liang YJ, Liang HZ. Macrophage migration inhibitory factor enhances neoplastic cell invasion by inducing the expression of matrix metalloproteinase 9 and interleukin-8 in nasopharyngeal carcinoma cell lines. Chin Med J 2004; 117(1): 107-14.
136. Li Z, Lin SX, Liang YJ, Zong YS. [Effect of macrophage migration inhibitory factor (MIF) on expression of MMP-2,MMP-9,and IL-8 in nasopharyngeal carcinoma cell strains]. Ai Zheng 2004; 23(2): 130-5.
137. Dirkx AE, Oude Egbrink MG, Wagstaff J, Griffioen AW. Monocyte/ macrophage infiltration in tumors: Modulators of angiogenesis. J Leukoc Biol 2006; 80(6): 1183-96.
138. Lewis C, Murdoch C. Macrophage responses to hypoxia: Implications for tumor progression and anti-cancer therapies. Am J Pathol 2005; 167(3): 627-35.
139. Colombo MP, Mantovani A. Targeting myelomonocytic cells to revert inflammation-dependent cancer promotion. Cancer Res 2005; 65(20): 9113-6.
140. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 2004; 4(1): 71-8.
141. Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M, et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 2004; 351(27): 2817-26.
142. Calandra T, Roger T. Macrophage migration inhibitory factor: A regulator of innate immunity. Nat Rev Immunol 2003; 3(10): 791-800.
143. Donnelly SC, Haslett C, Reid PT, Grant IS, Wallace WA, Metz CN, et al. Regulatory role for macrophage migration inhibitory factor in acute respiratory distress syndrome. Nat Med 1997; 3(3): 320-3.
144. Makita H, Nishimura M, Miyamoto K, Nakano T, Tanino Y, Hirokawa J, et al. Effect of anti-macrophage migration inhibitory factor antibody on lipopolysaccharide-induced pulmonary neutrophil accumulation. Am J Respir Crit Care Med 1998; 158(2): 573-9.
145. Hagemann T, Robinson SC, Thompson RG, Charles K, Kulbe H, Balkwill FR. Ovarian cancer cell-derived migration inhibitory factor enhances tumor growth, progression, and angiogenesis. Mol Cancer Ther 2007; 6(7): 1993-2002.
146. White ES, Strom SR, Wys NL, Arenberg DA. Non-small cell lung cancer cells induce monocytes to increase expression of angiogenic activity. J Immunol 2001; 166(12): 7549-55.
147. Daun JM, Cannon JG. Macrophage migration inhibitory factor antagonizes hydrocortisone-induced increases in cytosolic Ikappa-Balpha. Am J Physiol Regul Integr Comp Physiol 2000; 279(3): R1043-9.
148. Roger T, Froidevaux C, Martin C, Calandra T. Macrophage migration inhibitory factor (MIF) regulates host responses to endotoxin through modulation of Toll-like receptor 4 (TLR4). J Endotoxin Res 2003; 9(2): 119-23.
149. Ohkawara T, Takeda H, Miyashita K, Nishiwaki M, Nakayama T, Taniguchi M, et al. Regulation of Toll-like receptor 4 expression in mouse colon by macrophage migration inhibitory factor. Histochem Cell Biol 2006; 125(5): 575-82.
150. Chen R, Alvero AB, Silasi DA, Steffensen KD, Mor G. Cancers take their Toll - the function and regulation of Toll-like receptors in cancer cells. Oncogene 2008; 27(2): 225-33.
151. Lubetsky JB, Dios A, Han J, Aljabari B, Ruzsicska B, Mitchell R, et al. The tautomerase active site of macrophage migratioin inhibitory factor is a potential target for discovery of novel anti-inflammatory agents. J Biol Chem 2002; 277: 24976-82.
152. Xia HH, Zhang ST, Lam SK, Lin MC, Kung HF, Wong BC. Expression of macrophage migration inhibitory factor in esophageal squamous cell carcinoma and effects of bile acids and NSAIDs. Carcinogenesis 2005; 26(1): 11-5.
153. He XX, Yang J, Ding YW, Liu W, Shen QY, Xia HH. Increased epithelial and serum expression of macrophage migration inhibitory factor (MIF) in gastric cancer: Potential role of MIF in gastric carcinogenesis. Gut 2006; 55(6): 797-802.
154. Kettunen E, Anttila S, Seppanen JK, Karjalainen A, Edgren H, Lindstrom I, et al. Differentially expressed genes in nonsmall cell lung cancer: Expression profiling of cancer-related genes in squamous cell lung cancer. Cancer Genet Cytogenet 2004; 149(2): 98-106.
155. Kamimura A, Kamachi M, Nishihira J, Ogura S, Isobe H, Dosaka-Akita H, et al. Intracellular distribution of macrophage migration inhibitory factor predicts the prognosis of patients with adenocarcinoma of the lung. Cancer 2000; 89(2): 334-41.
156. Kayser K, Nwoye JO, Kosjerina Z, Goldmann T, Vollmer E, Kaltner H, et al. Atypical adenomatous hyperplasia of lung: Its incidence and analysis of clinical, glycohistochemical and structural features including newly defined growth regulators and vascularization. Lung Cancer 2003; 42(2): 171-82.
157. Legendre H, Decaestecker C, Nagy N, Hendlisz A, Schuring MP, Salmon I, et al. Prognostic values of galectin-3 and the macrophage migration inhibitory factor (MIF) in human colorectal cancers. Mod Pathol 2003; 16(5): 491-504.
158. Fei BY, Lv HX, Yang JM, Ye ZY. Association of MIF-173 gene polymorphism with inflammatory bowel disease in Chinese Han population. Cytokine 2008; 41(1): 44-7.
159. Nohara H, Okayama N, Inoue N, Koike Y, Fujimura K, Suehiro Y, et al. Association of the -173 G/C polymorphism of the macrophage migration inhibitory factor gene with ulcerative colitis. J Gastroenterol 2004; 39(3): 242-6.
160. Magi B, Bini L, Liberatori S, Marzocchi B, Raggiaschi R, Arcuri F, et al. Charge heterogeneity of macrophage migration inhibitory factor (MIF) in human liver and breast tissue. Electrophoresis 1998; 19(11): 2010-3.
161. Bini L, Magi B, Marzocchi B, Arcuri F, Tripodi S, Cintorino M, et al. Protein expression profiles in human breast ductal carcinoma and histologically normal tissue. Electrophoresis 1997; 18(15): 2832-41.
162. Bando H, Matsumoto G, Bando M, Muta M, Ogawa T, Funata N, et al. Expression of macrophage migration inhibitory factor in human breast cancer: Association with nodal spread. Jpn J Cancer Res 2002; 93(4): 389-96.
163. Xu X, Wang B, Ye C, Yao C, Lin Y, Huang X, et al. Overexpression of macrophage migration inhibitory factor induces angiogenesis in human breast cancer. Cancer Lett 2007 Dec 31.
164. Meyer-Siegler KL, Leifheit EC, Vera PL. Inhibition of macrophage migration inhibitory factor decreases proliferation and cytokine expression in bladder cancer cells. BMC Cancer 2004; 4: 34.
165. Meyer-Siegler KL, Iczkowski KA, Vera PL. Macrophage migration inhibitory factor is increased in the urine of patients with urinary tract infection: Macrophage migration inhibitory factor-protein complexes in human urine. J Urol 2006; 175(4): 1523-8.
166. Arcuri F, Ricci C, Ietta F, Cintorino M, Tripodi SA, Cetin I, et al. Macrophage migration inhibitory factor in the human endometrium: expression and localization during the menstrual cycle and early pregnancy. Biol Reprod 2001; 64(4): 1200-5.
167. Akoum A, Metz CN, Al-Akoum M, Kats R. Macrophage migration inhibitory factor expression in the intrauterine endometrium of women with
168. Bondza PK, Metz CN, Akoum A. 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 2007 Sep 11.
169. Wada S, Fujimoto S, Mizue Y, Nishihira J. Macrophage migration inhibitory factor in the human ovary: Presence in the follicular fluids and production by granulosa cells. Biochem Mol Biol Int 1997; 41(4): 805-14.
170. Matsuura T, Sugimura M, Iwaki T, Ohashi R, Kanayama N, Nishihira J. Anti-macrophage inhibitory factor antibody inhibits PMSGhCG-induced follicular growth and ovulation in mice. J Assist Reprod Genet 2002; 19(12): 591-5.
171. Agarwal R, Whang DH, Alvero AB, Visintin I, Lai Y, Segal EA, et al. Macrophage migration inhibitory factor expression in ovarian cancer. Am J Obstet Gynecol 2007; 196(4): 348 e1-5.
172. Meyer-Siegler K, Fattor RA, Hudson PB. Expression of macrophage migration inhibitory factor in the human prostate. Diagn Mol Pathol 1998; 7(1): 44-50.
173. Meyer-Siegler K, Hudson PB. Enhanced expression of macrophage migration inhibitory factor in prostatic adenocarcinoma metastases. Urology 1996; 48(3): 448-52.
174. Meyer-Siegler KL, Iczkowski KA, Vera PL. Further evidence for increased macrophage migration inhibitory factor expression in prostate cancer. BMC Cancer 2005; 5(1): 73.
175. del Vecchio MT, Tripodi SA, Arcuri F, Pergola L, Hako L, Vatti R, et al. Macrophage migration inhibitory factor in prostatic adenocarcinoma: Correlation with tumor grading and combination endocrine treatment-related changes. Prostate 2000; 45(1): 51-7.
176. Miracco C, De Nisi MC, Arcuri F, Cosci E, Pacenti L, Toscano M, et al. Macrophage migration inhibitory factor protein and mRNA expression in cutaneous melanocytic tumours. Int J Oncol 2006; 28(2): 345-52.
177. Gore Y, Starlets D, Maharshak N, Becker-Herman S, Kaneyuki U, Leng L, et al. Macrophage migration inhibitory factor induces B cell survival by activation of a CD74-CD44 receptor complex. J Biol Chem 2008; 283(5): 2784-92.
178. Sapoznikov A, Pewzner-Jung Y, Kalchenko V, Krauthgamer R, Shachar I, Jung S. Perivascular clusters of dendritic cells provide critical survival signals to B cells in bone marrow niches. Nat Immunol 2008; 9(4): 388-95.
179. Ma Y, Visser L, Roelofsen H, de Vries M, Diepstra A, van Imhoff G, et al. Proteomics analysis of Hodgkin lymphoma: Identification of new players involved in the cross-talk between HRS cells and infiltrating lymphocytes. Blood 2007 Dec 10.
180. Yasasever V, Camlica H, Duranyildiz D, Oguz H, Tas F, Dalay N. Macrophage migration inhibitory factor in cancer. Cancer Invest 2007; 25(8): 715-9.
181. Meyer-Siegler KL, Bellino MA, Tannenbaum M. Macrophage migration inhibitory factor evaluation compared with prostate specific antigen as a biomarker in patients with prostate carcinoma. Cancer 2002; 94(5): 1449-56.
182. Visintin I, Feng Z, Longton G, Ward DC, Alvero AB, Lai Y, et al. Diagnostic markers for early detection of ovarian cancer. Clin Cancer Res 2008; 14(4): 1065-72.
183. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100(1): 57-70.
184. Mitchell RA, Bucala R. Tumor growth-promoting properties of macrophage migration inhibitory factor (MIF). Semin Cancer Biol 2000; 10(5): 359-66.
185. Hoi AY, Iskander MN, Morand EF. Macrophage migration inhibitory factor: a therapeutic target across inflammatory diseases. Inflamm Allergy Drug Targets 2007; 6(3): 183-90.
186. Garai J, Molnar V, Eros D, Orfi L, Lorand T. MIF tautomerase inhibitor potency of alpha,beta-unsaturated cyclic ketones. Int Immunopharmacol 2007; 7(13): 1741-6.
187. Lolis E, Bucala R. Macrophage migratioin inhibitory factor. Expert Open Ther Target 2003; 7: 253-64.
188. Morand EF. New therapeutic target in inflammatory disease: Macrophage migration inhibitory factor. Intern Med J 2005; 35(7): 419-26.
189. Burton JD, Ely S, Reddy PK, Stein R, Gold DV, Cardillo TM, et al. CD74 is expressed by multiple myeloma and is a promising target for therapy. Clin Cancer Res 2004; 10(19): 6606-11.
190. Stein R, Qu Z, Cardillo TM, Chen S, Rosario A, Horak ID, et al. Antiproliferative activity of a humanized anti-CD74 monoclonal antibody, hLL1, on B-cell malignancies. Blood 2004; 104(12): 3705-11.
191. Michel RB, Andrews PM, Rosario AV, Goldenberg DM, Mattes MJ. 177Lu-antibody conjugates for single-cell kill of B-lymphoma cells in vitro and for therapy of micrometastases in vivo. Nucl Med Biol 2005; 32(3): 269-78.
192. Miles RR, Cairo MS, Satwani P, Zwick DL, Lones MA, Sposto R, et al. Immunophenotypic identification of possible therapeutic targets in paediatric non-Hodgkin lymphomas: A children's oncology group report. Br J Haematol 2007; 138(4): 506-12.
193. Stein R, Mattes MJ, Cardillo TM, Hansen HJ, Chang CH, Burton J, et al. CD74: A new candidate target for the immunotherapy of Bcell neoplasms. Clin Cancer Res 2007; 13(18 Pt 2): 5556s-63s.