Differences in the properties and mirna expression profiles between side populations from hepatic cancer cells and normal liver cells

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Liu, Wei hui ^a,b   Tao, Kai shan ^b   You, Nan ^b   Liu, Zheng cai ^b   Zhang, Hong tao ^b   Dou, Ke feng ^b  

^a CHENGDU MILITARY GENERAL HOSPITAL   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; ALPHA FETOPROTEIN; BIOLOGICAL MARKER; CD133 ANTIGEN; CYTOKINE 7; DIETHYLNITROSAMINE; EPITHELIAL CELL ADHESION MOLECULE; MICRORNA; SCATTER FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL ISOLATION; CELL SUBPOPULATION; CONTROLLED STUDY; DOWN REGULATION; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION PROFILING; IN VIVO STUDY; LIVER CELL; LIVER CELL CARCINOMA; MALE; NONHUMAN; QUANTITATIVE STUDY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; CELL CULTURE; CYTOLOGY; FISCHER 344 RAT; FLOW CYTOMETRY; GENETICS; LIVER TUMOR; METABOLISM; MOUSE; PHYSIOLOGY; TUMOR CELL CULTURE;

MUS MUSCULUS; RATTUS;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; FLOW CYTOMETRY; HEPATOCYTES; LIVER NEOPLASMS; MALE; MICE; MICRORNAS; RATS; RATS, INBRED F344; TUMOR CELLS, CULTURED;

EID: 79961035826     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023311     Document Type: Article

References (77)

1. Dalerba P, Cho RW, Clarke MF, (2007) Cancer stem cells: models and concepts. Annu Rev Med 58: 267-284.
2. Pardal R, Clarke MF, Morrison SJ, (2003) Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3: 895-902.
3. Wicha MS, Liu S, Dontu G, (2006) Cancer stem cells: an old idea-a paradigm shift. Cancer Res 66: 1883-1890; discussion 1895-1886.
4. Okuda K, Obata H, Nakajima Y, Ohtsuki T, Okazaki N, et al. (1984) Prognosis of primary hepatocellular carcinoma. Hepatology 4: 3S-6S.
5. Trichopoulos D, Day NE, Tzonou A, Hadziyannis S, Kaklamani E, et al. (1987) Delta agent and the etiology of hepatocellular carcinoma. Int J Cancer 39: 283-286.
6. Sasaki Y, Imaoka S, Masutani S, Ohashi I, Ishikawa O, et al. (1992) Influence of coexisting cirrhosis on long-term prognosis after surgery in patients with hepatocellular carcinoma. Surgery 112: 515-521.
7. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70.
8. Herr I, Groth A, Schemmer P, Buchler MW, (2007) Adult stem cells in progression and therapy of hepatocellular carcinoma. Int J Cancer 121: 1875-1882.
9. Chiba T, Zheng YW, Kita K, Yokosuka O, Saisho H, et al. (2007) Enhanced self-renewal capability in hepatic stem/progenitor cells drives cancer initiation. Gastroenterology 133: 937-950.
10. Nava S, Westgren M, Jaksch M, Tibell A, Broome U, et al. (2005) Characterization of cells in the developing human liver. Differentiation 73: 249-260.
11. Goodell MA, (2005) Stem cell identification and sorting using the Hoechst 33342 side population (SP). Curr Protoc Cytom Chapter 9: Unit9 18.
12. Johnnidis JB, Camargo FD, (2008) Isolation and functional characterization of side population stem cells. Methods Mol Biol 430: 183-193.
13. Uchida N, Fujisaki T, Eaves AC, Eaves CJ, (2001) Transplantable hematopoietic stem cells in human fetal liver have a CD34(+) side population (SP)phenotype. J Clin Invest 108: 1071-1077.
14. Hussain SZ, Strom SC, Kirby MR, Burns S, Langemeijer S, et al. (2005) Side population cells derived from adult human liver generate hepatocyte-like cells in vitro. Dig Dis Sci 50: 1755-1763.
15. Arends B, Vankelecom H, Vander Borght S, Roskams T, Penning LC, et al. (2009) The dog liver contains a "side population" of cells with hepatic progenitor-like characteristics. Stem Cells Dev 18: 343-350.
16. Forbes SJ, Alison MR, (2006) Side population (SP) cells: taking center stage in regeneration and liver cancer? Hepatology 44: 23-26.
17. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, et al. (2005) A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 353: 1793-1801.
18. Bottoni A, Zatelli MC, Ferracin M, Tagliati F, Piccin D, et al. (2007) Identification of differentially expressed microRNAs by microarray: a possible role for microRNA genes in pituitary adenomas. J Cell Physiol 210: 370-377.
19. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, et al. (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65: 7065-7070.
20. Peter ME, (2009) Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 8: 843-852.
21. Wang Y, Blelloch R, (2009) Cell cycle regulation by MicroRNAs in embryonic stem cells. Cancer Res 69: 4093-4096.
22. Wang Y, Russell I, Chen C, (2009) MicroRNA and stem cell regulation. Curr Opin Mol Ther 11: 292-298.
23. Gunaratne PH, (2009) Embryonic stem cell microRNAs: defining factors in induced pluripotent (iPS) and cancer (CSC) stem cells? Curr Stem Cell Res Ther 4: 168-177.
24. Riggi N, Suva ML, De Vito C, Provero P, Stehle JC, et al. (2010) EWS-FLI-1 modulates miRNA145 and SOX2 expression to initiate mesenchymal stem cell reprogramming toward Ewing sarcoma cancer stem cells. Genes Dev 24: 916-932.
25. Fiume L, Bolondi L, Busi C, Chieco P, Kratz F, et al. (2005) Doxorubicin coupled to lactosaminated albumin inhibits the growth of hepatocellular carcinomas induced in rats by diethylnitrosamine. J Hepatol 43: 645-652.
26. Pogribny IP, Tryndyak VP, Boyko A, Rodriguez-Juarez R, Beland FA, et al. (2007) Induction of microRNAome deregulation in rat liver by long-term tamoxifen exposure. Mutat Res 619: 30-37.
27. Hohne MW, Zieroth S, Veser U, Kahl GF, Schwarz LR, (1993) Carcinogen-induced diploid hepatocytes: sensitive target cells for transformation by mutated c-Ha-ras oncogene. Mol Carcinog 7: 180-189.
28. Oertel M, Menthena A, Chen YQ, Teisner B, Jensen CH, et al. (2008) Purification of fetal liver stem/progenitor cells containing all the repopulation potential for normal adult rat liver. Gastroenterology 134: 823-832.
29. Wong QW, Lung RW, Law PT, Lai PB, Chan KY, et al. (2008) MicroRNA-223 is commonly repressed in hepatocellular carcinoma and potentiates expression of Stathmin1. Gastroenterology 135: 257-269.
30. Beheshti B, Braude I, Marrano P, Thorner P, Zielenska M, et al. (2003) Chromosomal localization of DNA amplifications in neuroblastoma tumors using cDNA microarray comparative genomic hybridization. Neoplasia 5: 53-62.
31. Sui W, Dai Y, Huang Y, Lan H, Yan Q, et al. (2008) Microarray analysis of MicroRNA expression in acute rejection after renal transplantation. Transpl Immunol 19: 81-85.
32. Gregory PA, Bracken CP, Smith E, Bert AG, Wright JA, et al. (2011) An autocrine TGF-{beta}/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol Biol Cell.
33. Bendoraite A, Knouf EC, Garg KS, Parkin RK, Kroh EM, et al. (2010) Regulation of miR-200 family microRNAs and ZEB transcription factors in ovarian cancer: evidence supporting a mesothelial-to-epithelial transition. Gynecol Oncol 116: 117-125.
34. Alison MR, Lovell MJ, (2005) Liver cancer: the role of stem cells. Cell Prolif 38: 407-421.
35. Hadnagy A, Gaboury L, Beaulieu R, Balicki D, (2006) SP analysis may be used to identify cancer stem cell populations. Exp Cell Res 312: 3701-3710.
36. Meeson AP, Hawke TJ, Graham S, Jiang N, Elterman J, et al. (2004) Cellular and molecular regulation of skeletal muscle side population cells. Stem Cells 22: 1305-1320.
37. Oertel M, Menthena A, Dabeva MD, Shafritz DA, (2006) Cell competition leads to a high level of normal liver reconstitution by transplanted fetal liver stem/progenitor cells. Gastroenterology 130: 507-520; quiz 590.
38. Chiba T, Kita K, Zheng YW, Yokosuka O, Saisho H, et al. (2006) Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology 44: 240-251.
39. Zender L, Xue W, Cordon-Cardo C, Hannon GJ, Lucito R, et al. (2005) Generation and analysis of genetically defined liver carcinomas derived from bipotential liver progenitors. Cold Spring Harb Symp Quant Biol 70: 251-261.
40. Zhang B, Pan X, Cobb GP, Anderson TA, (2007) microRNAs as oncogenes and tumor suppressors. Dev Biol 302: 1-12.
41. Lee EJ, Gusev Y, Jiang J, Nuovo GJ, Lerner MR, et al. (2007) Expression profiling identifies microRNA signature in pancreatic cancer. Int J Cancer 120: 1046-1054.
42. Taylor DD, Gercel-Taylor C, (2008) MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 110: 13-21.
43. Chan JA, Krichevsky AM, Kosik KS, (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65: 6029-6033.
44. Si ML, Zhu S, Wu H, Lu Z, Wu F, et al. (2007) miR-21-mediated tumor growth. Oncogene 26: 2799-2803.
45. Roldo C, Missiaglia E, Hagan JP, Falconi M, Capelli P, et al. (2006) MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior. J Clin Oncol 24: 4677-4684.
46. Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, et al. (2007) MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133: 647-658.
47. Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, et al. (2007) MicroRNA signatures in human ovarian cancer. Cancer Res 67: 8699-8707.
48. Mirnezami AH, Pickard K, Zhang L, Primrose JN, Packham G, (2009) MicroRNAs: key players in carcinogenesis and novel therapeutic targets. Eur J Surg Oncol 35: 339-347.
49. Bandres E, Cubedo E, Agirre X, Malumbres R, Zarate R, et al. (2006) Identification by Real-time PCR of 13 mature microRNAs differentially expressed in colorectal cancer and non-tumoral tissues. Mol Cancer 5: 29.
50. Voorhoeve PM, Agami R, (2007) Classifying microRNAs in cancer: the good, the bad and the ugly. Biochim Biophys Acta 1775: 274-282.
51. Sengupta S, Nie J, Wagner RJ, Yang C, Stewart R, et al. (2009) MicroRNA 92b controls the G1/S checkpoint gene p57 in human embryonic stem cells. Stem Cells 27: 1524-1528.
52. Meng F, Henson R, Lang M, Wehbe H, Maheshwari S, et al. (2006) Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology 130: 2113-2129.
53. Ma L, Teruya-Feldstein J, Weinberg RA, (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682-688.
54. Zhu H, Wu H, Liu X, Evans BR, Medina DJ, et al. (2008) Role of MicroRNA miR-27a and miR-451 in the regulation of MDR1/P-glycoprotein expression in human cancer cells. Biochem Pharmacol 76: 582-588.
55. Ji J, Yamashita T, Budhu A, Forgues M, Jia HL, et al. (2009) Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells. Hepatology 50: 472-480.
56. Guo CJ, Pan Q, Li DG, Sun H, Liu BW, (2009) miR-15b and miR-16 are implicated in activation of the rat hepatic stellate cell: An essential role for apoptosis. J Hepatol 50: 766-778.
57. Cai KM, Bao XL, Kong XH, Jinag W, Mao MR, et al. (2010) Hsa-miR-34c suppresses growth and invasion of human laryngeal carcinoma cells via targeting c-Met. Int J Mol Med 25: 565-571.
58. Yang N, Kaur S, Volinia S, Greshock J, Lassus H, et al. (2008) MicroRNA microarray identifies Let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer. Cancer Res 68: 10307-10314.
59. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, et al. (2009) The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11: 1487-1495.
60. Rogler CE, (2009) MicroRNAs make inroads into liver development. Gastroenterology 136: 770-772.
61. DeSano JT, Xu L, (2009) MicroRNA regulation of cancer stem cells and therapeutic implications. AAPS J 11: 682-692.
62. Yui S, Nakamura T, Mizutani T, Nemoto Y, Okamoto R, et al. (2010) 849 A Long-Term, Mesenchyme-Free In Vitro Culture System of Colonic Epithelial Cells Retaining Stem Cell Compartment With Proliferation/Differentiation Properties. Gastroenterology 138: S-116.
63. Moriarty CH, Pursell B, Mercurio AM, (2010) miR-10b targets Tiam1: implications for Rac activation and carcinoma migration. J Biol Chem 285: 20541-20546.
64. Zheng L, Lv GC, Sheng J, Yang YD, (2010) Effect of miRNA-10b in regulating cellular steatosis level by targeting PPAR-alpha expression, a novel mechanism for the pathogenesis of NAFLD. J Gastroenterol Hepatol 25: 156-163.
65. Ali S, Ahmad A, Banerjee S, Padhye S, Dominiak K, et al. (2010) Gemcitabine sensitivity can be induced in pancreatic cancer cells through modulation of miR-200 and miR-21 expression by curcumin or its analogue CDF. Cancer Res 70: 3606-3617.
66. Shi L, Chen J, Yang J, Pan T, Zhang S, et al. (2010) MiR-21 protected human glioblastoma U87MG cells from chemotherapeutic drug temozolomide induced apoptosis by decreasing Bax:Bcl-2 ratio and caspase-3 activity. Brain Res In press.
67. Folini M, Gandellini P, Longoni N, Profumo V, Callari M, et al. (2010) miR-21: an oncomir on strike in prostate cancer. Mol Cancer 9: 12.
68. Cannell IG, Bushell M, (2010) Regulation of Myc by miR-34c: A mechanism to prevent genomic instability? Cell Cycle 9 In press.
69. Hagman Z, Larne O, Edsjo A, Bjartell A, Ehrnstrom RA, et al. (2010) miR-34c is down regulated in prostate cancer and exerts tumor suppressive functions. Int J Cancer In press.
70. Aqeilan RI, Calin GA, Croce CM, (2010) miR-15a and miR-16-1 in cancer: discovery, function and future perspectives. Cell Death Differ 17: 215-220.
71. Kaddar T, Rouault JP, Chien WW, Chebel A, Gadoux M, et al. (2009) Two new miR-16 targets: caprin-1 and HMGA1, proteins implicated in cell proliferation. Biol Cell 101: 511-524.
72. Bhattacharya R, Nicoloso M, Arvizo R, Wang E, Cortez A, et al. (2009) MiR-15a and MiR-16 control Bmi-1 expression in ovarian cancer. Cancer Res 69: 9090-9095.
73. Bandi N, Zbinden S, Gugger M, Arnold M, Kocher V, et al. (2009) miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non-small cell lung cancer. Cancer Res 69: 5553-5559.
74. O'Hara SP, Splinter PL, Gajdos GB, Trussoni CE, Fernandez-Zapico ME, et al. (2010) NFkappaB p50-CCAAT/enhancer-binding protein beta (C/EBPbeta)-mediated transcriptional repression of microRNA let-7i following microbial infection. J Biol Chem 285: 216-225.
75. Spaderna S, Brabletz T, Opitz OG, (2009) The miR-200 family: central player for gain and loss of the epithelial phenotype. Gastroenterology 136: 1835-1837.
76. Korpal M, Lee ES, Hu G, Kang Y, (2008) The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 283: 14910-14914.
77. Xia H, Ng SS, Jiang S, Cheung WK, Sze J, et al. (2010) miR-200a-mediated downregulation of ZEB2 and CTNNB1 differentially inhibits nasopharyngeal carcinoma cell growth, migration and invasion. Biochem Biophys Res Commun 391: 535-541.