MicroRNA-199a targets CD44 to suppress the tumorigenicity and multidrug resistance of ovarian cancer-initiating cells

FEBS Journal

Volumn 279, Issue 11, 2012, Pages 2047-2059

  Cheng, Weiwei ^a   Liu, Te ^a,b   Wan, Xiaoping ^a   Gao, Yongtao ^a   Wang, Hui ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

cancer initiating stem cells; drug resistance; microRNAs; ovarian cancer

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; CISPLATIN; DOXORUBICIN; HERMES ANTIGEN; LUCIFERASE; MESSENGER RNA; MICRORNA; MICRORNA 199A; PACLITAXEL; STEM CELL FACTOR RECEPTOR; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ABCG2 GENE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GENE THERAPY; CANCER STEM CELL; CARCINOGENICITY; CD44 GENE; CELL CYCLE; CELL MIGRATION; CELL PROLIFERATION; CLINICAL ARTICLE; COLONY FORMATION; DRUG SENSITIVITY; DRUG TARGETING; FEMALE; FLOW CYTOMETRY; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MARKER GENE; MOLECULAR CLONING; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; REPORTER GENE; TUMOR XENOGRAFT;

3' UNTRANSLATED REGIONS; ADULT; ANIMALS; ANTIGENS, CD44; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; CARCINOMA; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; FEMALE; GENES, REPORTER; HUMANS; LUCIFERASES; MICE; MICRORNAS; MIDDLE AGED; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; TUMOR MARKERS, BIOLOGICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84861193535     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08589.x     Document Type: Article

References (46)

1. Cannistra SA, (2004) Cancer of the ovary. N Engl J Med 351, 2519-2529.
2. Ozols RF, (2005) Treatment goals in ovarian cancer. Int J Gynecol Cancer 15 (Suppl 1), 3-11. (Pubitemid 40696471)
3. Thigpen JT, Aghajanian CA, Alberts DS, Campos SM, Gordon AN, Markman M, McMeekin DS, Monk BJ, &, Rose PG, (2005) Role of pegylated liposomal doxorubicin in ovarian cancer. Gynecol Oncol 96, 10-18. (Pubitemid 39612410)
4. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, &, Daidone MG, (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65, 5506-5511. (Pubitemid 40911148)
5. Reya T, Morrison SJ, Clarke MF, &, Weissman IL, (2001) Stem cells, cancer, and cancer stem cells. Nature 414, 105-111. (Pubitemid 33041634)
6. Marx J, (2003) Cancer research. Mutant stem cells may seed cancer. Science 301, 1308-1310. (Pubitemid 37075789)
7. Pardal R, Clarke MF, &, Morrison SJ, (2003) Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3, 895-902. (Pubitemid 37500174)
8. Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, Yan PS, Huang TH, &, Nephew KP, (2008) Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 68, 4311-4320.
9. Bonnet D, &, Dick JE, (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3, 730-737. (Pubitemid 27298715)
10. Mayol JF, Loeuillet C, Herodin F, &, Wion D, (2009) Characterisation of normal and cancer stem cells: one experimental paradigm for two kinds of stem cells. BioEssays 31, 993-1001.
11. Liu T, Xu F, Du X, Lai D, Zhao Y, Huang Q, Jiang L, Huang W, Cheng W, &, Liu Z, (2010) Establishment and characterization of multi-drug resistant, prostate carcinoma-initiating stem-like cells from human prostate cancer cell lines 22RV1. Mol Cell Biochem 340, 265-273.
12. Ma L, Lai D, Liu T, Cheng W, &, Guo L, (2010) Cancer stem-like cells can be isolated with drug selection in human ovarian cancer cell line SKOV3. Acta Biochim Biophys Sin (Shanghai) 42, 593-602.
13. Liu T, Cheng W, Lai D, Huang Y, &, Guo L, (2010) Characterization of primary ovarian cancer cells in different culture systems. Oncol Rep 23, 1277-1284.
14. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, &, Clarke MF, (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100, 3983-3988. (Pubitemid 36418143)
15. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, Hoey T, Gurney A, Huang EH, Simeone DM, et al. (2007) Phenotypic characterization of human -colorectal cancer stem cells. Proc Natl Acad Sci USA 104, 10158-10163. (Pubitemid 47175279)
16. O'Brien CA, Pollett A, Gallinger S, &, Dick JE, (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445, 106-110. (Pubitemid 46067310)
17. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, &, De Maria R, (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445, 111-115. (Pubitemid 46067311)
18. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, &, Dirks PB, (2004) Identification of human brain tumour initiating cells. Nature 432, 396-401. (Pubitemid 39551674)
19. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, &, Dick JE, (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367, 645-648. (Pubitemid 24067706)
20. Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, Gritti A, Piccinini A, Porro D, Santinami M, et al. (2007) Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 43, 935-946. (Pubitemid 46366698)
21. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, Conticello C, Ruco L, Peschle C, &, De Maria R, (2008) Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 15, 504-514. (Pubitemid 351267301)
22. Dou J, Pan M, Wen P, Li Y, Tang Q, Chu L, Zhao F, Jiang C, Hu W, Hu K, et al. (2007) Isolation and identification of cancer stem-like cells from murine melanoma cell lines. Cell Mol Immunol 4, 467-472.
23. Vrba L, Jensen TJ, Garbe JC, Heimark RL, Cress AE, Dickinson S, Stampfer MR, &, Futscher BW, (2010) Role for DNA methylation in the regulation of miR-200c and miR-141 expression in normal and cancer cells. PLoS One 5, e8697.
24. Lee RC, Feinbaum RL, &, Ambros V, (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843-854. (Pubitemid 24014542)
25. Carrington JC, &, Ambros V, (2003) Role of microRNAs in plant and animal development. Science 301, 336-338. (Pubitemid 36877060)
26. Guo X, Chen Y, Xu Z, Qian Y, &, Yu X, (2009) Prognostic significance of VEGF-C expression in correlation with COX-2, lymphatic microvessel density, and clinicopathologic characteristics in human non-small cell lung cancer. Acta Biochim Biophys Sin (Shanghai) 41, 217-222.
27. Jiang S, Zhang HW, Lu MH, He XH, Li Y, Gu H, Liu MF, &, Wang ED, (2010) MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res 70, 3119-3127.
28. Luzi E, Marini F, Sala SC, Tognarini I, Galli G, &, Brandi ML, (2008) Osteogenic differentiation of human adipose tissue-derived stem cells is modulated by the miR-26a targeting of the SMAD1 transcription factor. J Bone Miner Res 23, 287-295. (Pubitemid 351160043)
29. Eis PS, Tam W, Sun L, Chadburn A, Li Z, Gomez MF, Lund E, &, Dahlberg JE, (2005) Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc Natl Acad Sci USA 102, 3627-3632. (Pubitemid 40354662)
30. Zhang Y, Chao T, Li R, Liu W, Chen Y, Yan X, Gong Y, Yin B, Qiang B, Zhao J, et al. (2009) MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3a. J Mol Med 87, 43-51.
31. Sithanandam G, Fornwald LW, Fields J, &, Anderson LM, (2005) Inactivation of ErbB3 by siRNA promotes apoptosis and attenuates growth and invasiveness of human lung adenocarcinoma cell line A549. Oncogene 24, 1847-1859. (Pubitemid 40462787)
32. Huang S, He X, Ding J, Liang L, Zhao Y, Zhang Z, Yao X, Pan Z, Zhang P, Li J, et al. (2008) Upregulation of miR-23a∼27a∼24 decreases transforming growth factor-beta-induced tumor-suppressive activities in human hepatocellular carcinoma cells. Int J Cancer 123, 972-978. (Pubitemid 352032429)
33. Marhaba R, &, Zoller M, (2004) CD44 in cancer progression: adhesion, migration and growth regulation. J Mol Histol 35, 211-231. (Pubitemid 40585308)
34. Goodison S, Urquidi V, &, Tarin D, (1999) CD44 cell adhesion molecules. Mol Pathol 52, 189-196. (Pubitemid 29369203)
35. Blacking TM, Waterfall M, &, Argyle DJ, (2011) CD44 is associated with proliferation, rather than a specific cancer stem cell population, in cultured canine cancer cells. Vet Immunol Immunopathol 141, 46-57.
36. Hou NY, Yang K, Chen T, Chen XZ, Zhang B, Mo XM, &, Hu JK, (2011) CD133+ CD44+ subgroups may be human small intestinal stem cells. Mol Biol Rep 38, 997-1004.
37. Andersson E, Villabona L, Bergfeldt K, Carlson JW, Ferrone S, Kiessling R, Seliger B, &, Masucci GV, (2012) Correlation of HLA-A02* genotype and HLA class I antigen down-regulation with the prognosis of epithelial ovarian cancer. Cancer Immunol Immunother, doi:.
38. Rubatt JM, Darcy KM, Tian C, Muggia F, Dhir R, Armstrong DK, Bookman MA, Niedernhofer LJ, Deloia J, Birrer M, et al. (2012) Pre-treatment tumor expression of ERCC1 in women with advanced stage epithelial ovarian cancer is not predictive of clinical outcomes: a gynecologic oncology group study. Gynecol Oncol 125, 421-426.
39. Cheng W, Liu T, Jiang F, Liu C, Zhao X, Gao Y, Wang H, &, Liu Z, (2011) microRNA-155 regulates angiotensin II type 1 receptor expression in umbilical vein endothelial cells from severely pre-eclamptic pregnant women. Int J Mol Med 27, 393-399.
40. Zhang L, Liu T, Huang Y, &, Liu J, (2011) microRNA-182 inhibits the proliferation and invasion of human lung adenocarcinoma cells through its effect on human cortical actin-associated protein. Int J Mol Med 28, 381-388.
41. Henry JC, Park JK, Jiang J, Kim JH, Nagorney DM, Roberts LR, Banerjee S, &, Schmittgen TD, (2010) miR-199a-3p targets CD44 and reduces proliferation of CD44 positive hepatocellular carcinoma cell lines. Biochem Biophys Res Commun 403, 120-125.
42. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, et al. (2011) The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 17, 211-215.
43. He M, Xu Z, Ding T, Kuang DM, &, Zheng L, (2009) MicroRNA-155 regulates inflammatory cytokine production in tumor-associated macrophages via targeting C/EBPbeta. Cell Mol Immunol 6, 343-352.
44. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, et al. (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464, 1071-1076.
45. Jiang F, Liu T, He Y, Yan Q, Chen X, Wang H, &, Wan X, (2011) MiR-125b promotes proliferation and migration of type II endometrial carcinoma cells through targeting TP53INP1 tumor suppressor in vitro and in vivo. BMC Cancer 11, 425.
46. Carro MS, Lim WK, Alvarez MJ, Bollo RJ, Zhao X, Snyder EY, Sulman EP, Anne SL, Doetsch F, Colman H, et al. (2010) The transcriptional network for mesenchymal transformation of brain tumours. Nature 463, 318-325.