MicroRNA-152-mediated dysregulation of hepatic transferrin receptor 1 in liver carcinogenesis

Oncotarget

Volumn 7, Issue 2, 2016, Pages 1276-1287

  Kindrat, Iryna ^a,c   Tryndyak, Volodymyr ^a   Conti, Aline de ^a   Shpyleva, Svitlana ^a   Mudalige, Thilak K ^b   Kobets, Tetyana ^a   Erstenyuk, Anna M ^c   Beland, Frederick A ^a   Pogribny, Igor P ^a  

^a NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^c IVANO FRANKIVSK NATIONAL MEDICAL UNIVERSITY   (Ukraine)

Author keywords

Dysregulation; Hepatocellular carcinoma; Iron metabolism; MicroRNA 152; Transferrin receptor 1

Indexed keywords

CD71 ANTIGEN; FERROPORTIN 1; IRON; MESSENGER RNA; MICRORNA; MICRORNA 152; UNCLASSIFIED DRUG; CARCINOGEN; LEUKOCYTE ANTIGEN; MIRN152 MICRORNA, HUMAN; N (2 FLUORENYL)ACETAMIDE; TFR1 PROTEIN, RAT; TRANSFERRIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL LEVEL; CONTROLLED STUDY; DNA METHYLATION; FPN1 GENE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LIVER CARCINOGENESIS; LIVER LEVEL; MALE; NONHUMAN; RAT; TFRC GENE; ANIMAL; CARCINOGENESIS; CHEMICALLY INDUCED; DRUG EFFECTS; EXPERIMENTAL LIVER NEOPLASM; GENETICS; HEP-G2 CELL LINE; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; TUMOR CELL LINE; WESTERN BLOTTING;

2-ACETYLAMINOFLUORENE; ANIMALS; ANTIGENS, CD; BLOTTING, WESTERN; CARCINOGENESIS; CARCINOGENS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICRORNAS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TRANSFERRIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84957667663     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6004     Document Type: Article

References (49)

1. Center MM, Jemal A. International trends in liver cancer incidence rates. Cancer Epidemiol. Biomarkers Prev. 2011; 20:2362-8.
2. Mittal S, El-Serag HB. Epidemiology of hepatocellular carcinoma: consider the population. J Clin Gastroenterol. 2013; 47:S2-S6.
3. American Association for Cancer Research. AACR Cancer Progress Report 2013. Clin Cancer Res. 2013; 19 (Supplement 1):S1-S98.
4. Torti SV, Torti FM. Iron and cancer: more ore to be mined. Nat Rev Cancer. 2013; 13:342-55.
5. Sorrentino P, D'Angelo S, Ferbo U, Micheli P, Bracigliano A, Vecchione R. Liver iron excess in patients with hepatocellular carcinoma developed on non-alcoholic steato-hepatitis. J Hepatol. 2009; 50:351-7.
6. Tirnitz-Parker JEE, Granfield A, Olynyk JK, Ramm GA. Iron and hepatic carcinogenesis. Crit Rev Oncog. 2013; 18:391-407.
7. Chen J, Chloupkova M. Abnormal iron uptake and liver cancer. Cancer Biol Ther. 2009; 8:1699-708.
8. Nahon P, Zucman-Rossi J. Single nucleotide polymorphisms and risk of hepatocellular carcinoma in cirrhosis. J Hepatol. 2012; 57:663-74.
9. Kessler SM, Laggai S, Kiemer AK, Barghash A, Helms V. Hepatic hepcidin expression is decreased in cirrhosis and HCC. J Hepatol. 2015; 62:977-9.
10. Viatte L, Vaulont S. Hepcidin, the iron watcher. Biochimie. 2009; 91:1223-8.
11. Martinelli ALC, Araujo Filho AB, Franco RF, Tavella MH, Ramalho LNZ, Zucoloto S, Rodrigues SS, Zago MA. Liver iron deposits in hepatitis B patients: association with severity of liver disease but not with hemochromatosis gene mutations. J Gastroenterol Hepatol. 2004; 19:1036-41.
12. Isom HC, McDevitt EI, Moon MS. Elevated hepatic iron: a confounding factor in chronic hepatitis C. Biochim Biophys Acta. 2009; 1790:650-62.
13. Kohgo Y, Ohtake T, Ikuta K, Suzuki Y, Torimoto Y, Kato J. Dysregulation of systemic iron metabolism in alcoholic liver diseases. J Gastroenterol Hepatol. 2008;Suppl 1:S78-81.
14. Nelson JE, Klintworth H, Kowdley KV. Iron metabolism in nonalcoholic fatty liver disease. Curr Gastroenterol Rep. 2012; 14:8-16.
15. Fargion S, Valenti L, Fracanzani AL. Beyond hereditary hemochromatosis: new insights into the relationship between iron overload and chronic liver diseases. Dig Liver Dis. 2011; 43:89-95.
16. Shpyleva SI, Muskhelishvili L, Tryndyak VP, Koturbash I, Tokar EJ, Waalkes MP, Beland FA, Pogribny IP. Chronic administration of 2-acetylaminofluorene alters the cellular iron metabolism in rat liver. Toxicol Sci. 2011; 123:433-40.
17. Bitsch A, Klohn P-C, Hadjiolov N, Bergmann O, Neumann H-G. New insights into carcinogenesis of the classical model arylamine 2-acetylaminofluorene. Cancer Lett. 1999; 143:223-7.
18. Solt D, Farber E. New principle for the analysis of chemical carcinogenesis. Nature. 1976; 263:701-3.
19. Petrelli A, Perra A, Cora D, Sulas P, Menegon S, Manca C, Migliore C, Kowalik MA, Ledda-Columbano GM, Giordano S, Columbano A. MicroRNA/gene profiling unveils early molecular changes and nuclear factor erythroid related factor 2 (NRF2) activation in a rat model recapitulating human hepatocellular carcinoma (HCC). Hepatology. 2014; 59:228-41.
20. Bagnyukova TV, Tryndyak VP, Montgomery B, Churchwell MI, Karpf AR, James SR, Muskhelishvili L, Beland FA, Pogribny IP. Genetic and epigenetic changes in rat preneoplastic liver tissue induced by 2-acetylaminofluorene. Carcinogenesis. 2008; 29:638-46.
21. Kuroiwa-Trzmielina J, de Conti A, Scolastici C, Pereira D, Horst MA, Purgatto E, Ong TP, Moreno FS. Chemoprevention of rat hepatocarcinogenesis with histone deacetylase inhibitors: efficacy of tributyrin, a butyric acid prodrug. Int J Cancer. 2009; 124:2520-7.
22. Riemer J, Hoepken HH, Czerwinska H, Robinson SR, Dringen R. Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal Biochem. 2004; 331:370-5.
23. Yokoo H, Kondo T, Fujii K, Yamada T, Todo S, Hirohashi S. Proteomic signature corresponding to alpha fetoprotein expression in liver cancer cells. Hepatology. 2004; 40:609-17.
24. Yamashita T, Budhu A, Forgues M, Wang XW. Activation of hepatic stem cell marker EpCAM by Wnt-β-catenin signaling in hepatocellular carcinoma. Cancer Res. 2007; 67:10831-9.
25. Jonsdottir K, Storkson R, Krog A, Bukholm IRK. Correlation between mRNA detected by microarrays and qRT-PCR and protein detected by immunohistochemistry of cyclins in tumour tissue from colonic adenocarcinomas. Open Pathol J. 2008; 2:96-101.
26. Ning B, Liu G, Liu Y, Su X, Anderson GJ, Zheng X, Chang Y, Guo M, Liu Y, Zhao Y, Nie G. 5-aza-2'-deoxycytidine activates iron uptake and heme biosynthesis by increasing c-Myc nuclear localization and binding to the E-boxes of transferrin receptor 1 (TfR1) and ferrochelatase (Fech) genes. J Biol Chem. 2011; 286:37196-206.
27. Graham RM, Chua ACG, Herbison CE, Olynyk JK, Trinder D. Liver iron transport. World J Gastroenterol. 2007; 13:4725-36.
28. Anderson CP, Shen L, Eisenstein RS, Leibold EA. Mammalian iron metabolism and its control by iron regulatory proteins. Biochim Biophys Acta. 2012; 1823:1468-83.
29. Herbison CE, Thorstensen K, Chua ACG, Graham RM, Leedman P, Olynyk JK, Trinder D. The role of transferrin receptor 1 and 2 in transferrin-bound iron uptake in human hepatoma cells. Am J Physiol Cell Physiol. 2009; 297:C1567-C75.
30. Pascale RM, De Miglio MR, Muroni MR, Simile MM, Daino L, Seddaiu MA, Pusceddu S, Gaspa L, Calvisi D, Manenti G, Feo F. Transferrin and transferrin receptor gene expression and iron uptake in hepatocellular carcinoma in the rat. Hepatology. 1998; 27:452-61.
31. Takahashi M, Shibutani M, Woo G-H, Inoue K, Fujimoto H, Igarashi K, Kanno J, Hirose M, Nishikawa A. Cellular distribution of molecules with altered expression specific to the tumor promotion process from the early stage in a rat two-stage hepatocarcinogenesis model. Carcinogernesis. 2008; 29:2218-26.
32. Mizukami S, Ichimura R, Kemmochi S, Taniai E, Shimamoto K, Ohishi T, Takahashi M, Mitsumori K, Shibutani M. Induction of GST-P-positive proliferative lesions facilitating lipid peroxidation with possible involvement of transferrin receptor up-regulation and cerruloplasmin down-regulation from the early stage of liver tumor promotion in rats. Arch Toxicol. 2010; 84:319-31.
33. Sakurai K, Sohda T, Ueda S, Tanaka T, Hirano G, Yokoyama K, Morihara D, Aanan A, Takeyama Y, Irie M, Iwata K, Syakado S, Noritomiz T, et al. Immunohistochemical demonstration of transferrin receptor 1 and 2 in human hepatocellular carcinoma tissue. Hepatogastroenterology. 2014; 61:426-30.
34. Rouault TA. The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat Chem Biol. 2006; 2:406-14.
35. Wang W, Deng Z, Hatcher H, Miller LD, Di X, Tesfay L, Sui G, D'Agostino RB Jr, Torti FM, Torti SV. IRP2 regulates breast tumor growth. Cancer Res. 2014; 74:497-507.
36. Huang H-L, Shaw N-S. Role of hypolipidemic drug clofibrate in altering iron regulatory proteins IRP2 and IEP2 activities and hepatic iron metabolism in rats fed a low-iron diet. Toxicol Appl Pharmacol. 2002; 180:118-28.
37. Maffettone C, Chen G, Drozdov I, Ouzounis C, Pantopoulos K. Tumorigenic properties of iron regulatory protein 2 (IRP2) mediated by its specific 73-amino acids insert. PLoS One. 2010; 5:e10163.
38. Chen G, Fillebeen C, Wang J, Pantopoulos K. Overexpression of iron regulatory protein 1 suppresses growth of tumor xenografts. Carcinogenesis. 2007; 28:785-91.
39. Du F, Qian Z-m, Gong Q, Zhu ZJ, Lu L, Ke Y. The iron regulatory hormone hepcidin inhibits expression of iron release as well as iron uptake proteins in J774 cells. J Nutr Biochem. 2012; 23:1694-1700.
40. Tseng H-H, Chang J-G, Hwang Y-H, Yeh K-T, Chen Y-L, Yu H-S. Expression of hepcidin and other iron-regulatory genes in human hepatocellular carcinoma and its clinical implications. J Cancer Res Clin Oncol. 2009; 135:1413-20.
41. Kerenyi MA, Grebien F, Gehart H, Schifrer M, Artaker M, Kovacic B, Beug H, Moriggl R, Müllner EW. Stat5 regulates cellular iron uptake of erythroid cells via IRP-2 and Tf R1. Blood. 2008; 112:3878-88.
42. O'Donnell KA, Yu D, Zeller KI, Kim J-w, Racke F, Thomas-Tikhonenko A, Dang CV. Activation of transferrin receptor 1 by c-Myc enhances cellular proliferation and tumorigenesis. Mol Cell Biol. 2006; 26:2373-86.
43. Schaar DG, Medina DJ, Moore DF, Strair RK, Ting Y. miR-320 targets transferrin receptor 1 (CD71) and inhibits cell proliferation. Exp Hematol. 2009; 37:245-55.
44. Yoshioka Y, Kosaka N, Ochiya T, Kato T. Micromanaging iron homeostasis: hypoxia-inducible micro-RNA-210 suppresses iron homeostasis-related proteins. J Biol Chem. 2012; 287:34110-9.
45. Yin K, Hacia JG, Zhong Z, Paine ML. Genome-wide analysis of miRNA and mRNA transcriptomes during amelogenesis. BMC Genomics. 2014; 15:998.
46. Huang J, Wang Y, Guo Y, Sun S. Down-regulated microRNA-152 induces aberrant DNA methylation in hepatitis B virus-related hepatocellular carcinoma by targeting DNA methyltransferase 1. Hepatology. 2010; 52:60-70.
47. Chen L, Yan H-X, Yang W, Hu L, Yu L-X, Liu Q, Li L, Huang D-D, Ding J, Shen F, Zhou W-P, Wu M-C, Wang H-Y. The role of microRNA expression pattern in human intrahepatic cholangiocarcinoma. J Hepatol. 2009; 50:358-69.
48. Ba Q, Hao M, Huang H, Hou J, Ge S, Zhang Z, Yin J, Chu R, Jiang H, Wang F, Chen K, Liu H, Wang H. Iron deprivation suppresses hepatocellular carcinoma growth in experimental studies. Clin Cancer Res. 2011; 17:7625-33.
49. Crépin R, Goenaga A-L, Jullienne B, Bougherara H, Legay C, Benihoud K, Marks JD, Poul M-A. Development of human single-chain antibodies to the transferrin receptor that effectively antagonize the growth of leukemias and lymphomas. Cancer Res. 2010; 70:5497-506.