Macrophage migration inhibitory factor induces epithelial to mesenchymal transition, enhances tumor aggressiveness and predicts clinical outcome in resected pancreatic ductal adenocarcinoma

International Journal of Cancer

Volumn 132, Issue 4, 2012, Pages 785-794

  Funamizu, Naotake ^a   Hu, Chaoxin ^b   Lacy, Curtis ^a   Schetter, Aaron ^a   Zhang, Geng ^a   He, Peijun ^a   Gaedcke, Jochen ^c   Ghadimi, Michael B ^c   Ried, Thomas ^a   Yfantis, Harris G ^d   Lee, Dong H ^d   Subleski, Jeffrey ^e   Chan, Tim ^e   Weiss, Jonathan M ^e   Back, Timothy C ^e   Yanaga, Katsuhiko ^f   Hanna, Nader ^g   Alexander, H Richard ^g   Maitra, Anirban ^b   Hussain, S Perwez ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d BALTIMORE VA MEDICAL CENTER   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^g UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

EMT; MIF; miR 200; pancreatic cancer

Indexed keywords

GEMCITABINE; MACROPHAGE MIGRATION INHIBITION FACTOR; MESSENGER RNA; MICRORNA 200B; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZEB1; TRANSCRIPTION FACTOR ZEB2; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; ANTINEOPLASTIC ANTIMETABOLITE; DEOXYCYTIDINE; MICRORNA; MIRN200 MICRORNA, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CANCER SURVIVAL; CHEMOSENSITIVITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; E CADHERIN GENE; EPITHELIAL MESENCHYMAL TRANSITION; GENE; GENE EXPRESSION REGULATION; GENE LOCATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE MIGRATION INHIBITION FACTOR GENE; MAJOR CLINICAL STUDY; METASTASIS; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PANCREAS ADENOCARCINOMA; PREDICTION; PRIORITY JOURNAL; PROTEIN FUNCTION; SURVIVAL RATE; TUMOR GROWTH; VIMENTIN GENE; ADULT; AGED; ANALOGS AND DERIVATIVES; ANIMAL; APOPTOSIS; CELL PROLIFERATION; DRUG EFFECTS; FEMALE; GENETICS; KAPLAN MEIER METHOD; MALE; METABOLISM; MIDDLE AGED; NUDE MOUSE; PANCREAS CARCINOMA; PANCREAS TUMOR; PATHOLOGY; PROGNOSIS; RNA INTERFERENCE; TUMOR CELL LINE; TUMOR INVASION; VERY ELDERLY; XENOGRAFT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; CELL PROLIFERATION; DEOXYCYTIDINE; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KAPLAN-MEIER ESTIMATE; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MALE; MICE, NUDE; MICRORNAS; MIDDLE AGED; NEOPLASM INVASIVENESS; PANCREATIC NEOPLASMS; PROGNOSIS; RNA INTERFERENCE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84871364500     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.27736     Document Type: Article

References (43)

1. Siegel R, Naishadham D, Jemal A,. Cancer statistics, 2012. CA Cancer J Clin 2012; 62: 10-29.
2. Hidalgo M,. Pancreatic cancer. N Engl J Med 2010; 362: 1605-17.
3. Vincent A, Herman J, Schulick R, et al. Pancreatic cancer. Lancet 2011; 378: 607-20.
4. Garcea G, Dennison AR, Steward WP, et al. Role of inflammation in pancreatic carcinogenesis and the implications for future therapy. Pancreatology 2005; 5: 514-29. (Pubitemid 41407282)
5. Lowenfels AB, Maisonneuve P, Cavallini G, et al. Pancreatitis and the risk of pancreatic cancer. International Pancreatitis Study Group. N Engl J Med 1993; 328: 1433-7. (Pubitemid 23143844)
6. Whitcomb DC, Applebaum S, Martin SP,. Hereditary pancreatitis and pancreatic carcinoma. Ann NY Acad Sci 1999; 880: 201-9. (Pubitemid 29349128)
7. Chu GC, Kimmelman AC, Hezel AF, et al. Stromal biology of pancreatic cancer. J Cell Biochem 2007; 101: 887-907. (Pubitemid 47040870)
8. Schetter AJ, Heegaard NH, Harris CC,. Inflammation and cancer: interweaving microRNA, free radical, cytokine and p53 pathways. Carcinogenesis 2010; 31: 37-49.
9. Hussain SP, Hofseth LJ, Harris CC,. Radical causes of cancer. Nat Rev Cancer 2003; 3: 276-85. (Pubitemid 37328863)
10. Rhim AD, Mirek ET, Aiello NM, et al. EMT and dissemination precede pancreatic tumor formation. Cell 2012; 148: 349-61.
11. Calandra T, Roger T,. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 2003; 3: 791-800. (Pubitemid 37328657)
12. He XX, Yang J, Ding YW, et al. Increased epithelial and serum expression of macrophage migration inhibitory factor (MIF) in gastric cancer: potential role of MIF in gastric carcinogenesis. Gut 2006; 55: 797-802. (Pubitemid 43764549)
13. Meyer-Siegler KL, Vera PL, Iczkowski KA, et al. Macrophage migration inhibitory factor (MIF) gene polymorphisms are associated with increased prostate cancer incidence. Genes Immun 2007; 8: 646-52. (Pubitemid 350238434)
14. Xu X, Wang B, Ye C, et al. Overexpression of macrophage migration inhibitory factor induces angiogenesis in human breast cancer. Cancer Lett 2008; 261: 147-57. (Pubitemid 351253721)
15. Kamimura A, Kamachi M, Nishihira J, et al. Intracellular distribution of macrophage migration inhibitory factor predicts the prognosis of patients with adenocarcinoma of the lung. Cancer 2000; 89: 334-41. (Pubitemid 30489881)
16. Denz A, Pilarsky C, Muth D, et al. Inhibition of MIF leads to cell cycle arrest and apoptosis in pancreatic cancer cells. J Surg Res 2010; 160: 29-34.
17. Winner M, Koong AC, Rendon BE, et al. Amplification of tumor hypoxic responses by macrophage migration inhibitory factor-dependent hypoxia-inducible factor stabilization. Cancer Res 2007; 67: 186-93. (Pubitemid 46142774)
18. Hudson JD, Shoaibi MA, Maestro R, et al. A proinflammatory cytokine inhibits p53 tumor suppressor activity. J Exp Med 1999; 190: 1375-82.
19. Glynn SA, Boersma BJ, Dorsey TH, et al. Increased NOS2 predicts poor survival in estrogen receptor-negative breast cancer patients. J Clin Invest 2010; 120: 3843-54.
20. Warner SL, Stephens BJ, Nwokenkwo S, et al. Validation of TPX2 as a potential therapeutic target in pancreatic cancer cells. Clin Cancer Res 2009; 15: 6519-28.
21. Feldmann G, Dhara S, Fendrich V, et al. Blockade of hedgehog signaling inhibits pancreatic cancer invasion and metastases: a new paradigm for combination therapy in solid cancers. Cancer Res 2007; 67: 2187-96. (Pubitemid 46424238)
22. Kalluri R, Weinberg RA,. The basics of epithelial-mesenchymal transition. J Clin Invest 2009; 119: 1420-8.
23. Thiery JP, Acloque H, Huang RY, et al. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-90.
24. Singh AB, Sharma A, Smith JJ, et al. Claudin-1 up-regulates the repressor ZEB-1 to inhibit E-cadherin expression in colon cancer cells. Gastroenterology 2011; 141: 2140-53.
25. Chua HL, Bhat-Nakshatri P, Clare SE, et al. NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene 2007; 26: 711-24. (Pubitemid 46204250)
26. Spaderna S, Schmalhofer O, Wahlbuhl M, et al. The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res 2008; 68: 537-44. (Pubitemid 351380082)
27. Burk U, Schubert J, Wellner U, et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 2008; 9: 582-9. (Pubitemid 351772923)
28. Bracken CP, Gregory PA, Kolesnikoff N, et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 2008; 68: 7846-54.
29. Feurino LW, Fisher WE, Bharadwaj U, et al. Current update of cytokines in pancreatic cancer: pathogenic mechanisms, clinical indication, and therapeutic values. Cancer Invest 2006; 24: 696-703. (Pubitemid 44841842)
30. Uomo I, Miraglia S, Pastorello M,. Inflammation and pancreatic ductal adenocarcinoma: a potential scenario for novel drug targets. JOP 2010; 11: 199-202.
31. Bucala R, Donnelly SC,. Macrophage migration inhibitory factor: a probable link between inflammation and cancer. Immunity 2007; 26: 281-5. (Pubitemid 46413914)
32. Yeh JJ,. Prognostic signature for pancreatic cancer: are we close? Future Oncol 2009; 5: 313-21.
33. Zhang G, Schetter A, He P, et al. DPEP1 inhibits tumor cell invasiveness, enhances chemosensitivity and predicts clinical outcome in pancreatic ductal adenocarcinoma. PLoS One 2012; 7: e31507.
34. Wang Z, Li Y, Ahmad A, et al. Pancreatic cancer: understanding and overcoming chemoresistance. Nat Rev Gastroenterol Hepatol 2011; 8: 27-33.
35. Singh A, Settleman J,. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010; 29: 4741-51.
36. Lopez-Novoa JM, Nieto MA,. Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO Mol Med 2009; 1: 303-14.
37. Keshamouni VG, Jagtap P, Michailidis G, et al. Temporal quantitative proteomics by iTRAQ 2D-LC-MS/MS and corresponding mRNA expression analysis identify post-transcriptional modulation of actin-cytoskeleton regulators during TGF-beta-Induced epithelial-mesenchymal transition. J Proteome Res 2009; 8: 35-47.
38. Li Y, VandenBoom TG, II, Kong D, et al. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res 2009; 69: 6704-12.
39. Du R, Sun W, Xia L, et al. Hypoxia-induced down-regulation of microRNA-34a promotes EMT by targeting the notch signaling pathway in tubular epithelial cells. PLoS One 2012; 7: e30771.
40. Liu YN, Yin JJ, Abou-Kheir W, et al. MiR-1 and miR-200 inhibit EMT via slug-dependent and tumorigenesis via slug-independent mechanisms. Oncogene 2012 Feb 27. doi: 10.1038/onc.2012.58. [Epub ahead of print].
41. Smith AL, Iwanaga R, Drasin DJ, et al. The miR-106b-25 cluster targets Smad7, activates TGF-beta signaling, and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer. Oncogene 2012 Jan 30. doi: 10.1038/onc.2012.11. [Epub ahead of print].
42. Wellner U, Schubert J, Burk UC, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 2009; 11: 1487-95.
43. Brabletz S, Brabletz T,. The ZEB/miR-200 feedback loop-A motor of cellular plasticity in development and cancer? EMBO Rep 2010; 11: 670-7.