MicroRNA-145 Is Downregulated in Glial Tumors and Regulates Glioma Cell Migration by Targeting Connective Tissue Growth Factor

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Lee, Hae Kyung ^a   Bier, Ariel ^b   Cazacu, Simona ^a   Finniss, Susan ^a   Xiang, Cunli ^a   Twito, Hodaya ^b   Poisson, Laila M ^a   Mikkelsen, Tom ^a   Slavin, Shimon ^c   Jacoby, Elad ^d   Yalon, Michal ^d   Toren, Amos ^d   Rempel, Sandra A ^a   Brodie, Chaya ^a,b  

^a HENRY FORD HOSPITAL   (United States)

^b BAR ILAN UNIVERSITY   (Israel)

^c International Center for Cell Therapy and Cancer Immunotherapy CTCI   (Israel)

^d SHEBA MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; FOCAL ADHESION KINASE; MICRORNA 143; MICRORNA 145;

3' UNTRANSLATED REGION; ARTICLE; ASTROCYTE; CANCER INVASION; CANCER PROGNOSIS; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; GLIOMA; HUMAN; HUMAN TISSUE; NEURAL STEM CELL; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; ASTROCYTES; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CONNECTIVE TISSUE GROWTH FACTOR; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENES, REPORTER; GLIOBLASTOMA; HUMANS; LUCIFERASES; MICRORNAS; NEOPLASTIC STEM CELLS; NEURAL STEM CELLS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84873497493     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054652     Document Type: Article

References (72)

1. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, et al. (2007) Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 21: 2683-2710.
2. Noda SE, El-Jawahri A, Patel D, Lautenschlaeger T, Siedow M, (2009) Molecular advances of brain tumors in radiation oncology. Semin Radiat Oncol 19: 171-178.
3. Desjardins A, Rich JN, Quinn JA, Vredenburgh J, Gururangan S, et al. (2005) Chemotherapy and novel therapeutic approaches in malignant glioma. Front Biosci 10: 2645-2668.
4. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, et al. (2005) Malignant glioma: genetics and biology of a grave matter. Genes Dev 15: 1311-1333.
5. Emdad L, Dent P, Sarkar D, Fisher PB, (2012) Future approaches for the therapy of malignant glioma: targeting genes mediating invasion. Future Oncol 8: 343-346.
6. Giese A, Bjerkvig R, Berens ME, Westphal M, (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21: 1624-1636.
7. Lefranc F, Brotchi J, Kiss R, (2005) Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. J Clin Oncol 23: 2411-2422.
8. Bartel DP, (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
9. Carthew RW, (2006) Gene regulation by microRNAs. Curr Opin Genet Dev 16: 203-208.
10. Alvarez-Garcia I, Miska EA, (2005) MicroRNA functions in animal development and human disease. Development 132: 4653-4662.
11. Lawler S, Chiocca EA, (2009) Emerging functions of microRNAs in glioblastoma. J Neurooncol 92: 297-306.
12. Zhang B, Pan X, Cobb GP, Anderson TA, (2007) microRNAs as oncogenes and tumor suppressors. Dev Biol 302: 1-12.
13. Lovat F, Valeri N, Croce CM, (2011) MicroRNAs in the pathogenesis of cancer. Semin Oncol 38: 724-733.
14. Gaur AB, Holbeck SL, Colburn NH, Israel MA, (2011) Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro Oncol 13: 580-590.
15. Quintavalle C, Garofalo M, Zanca C, Romano G, Iaboni M, et al. (2012) miR-221/222 overexpession in human glioblastoma increases invasiveness by targeting the protein phosphate PTPμ. Oncogene 31: 858-868.
16. Fang L, Deng Z, Shatseva T, Yang J, Peng C, et al. (2011) MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-β8. Oncogene 30: 806-821.
17. Sasayama T, Nishihara M, Kondoh T, Hosoda K, Kohmura E, (2009) MicroRNA-10b is overexpressed in malignant glioma and associated with tumor invasive factors, uPAR and RhoC. Int J Cancer 125: 1407-1413.
18. Li Y, Guessous F, Zhang Y, Dipierro C, Kefas B, et al. (2009) MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 69: 7569-7576.
19. Kefas B, Comeau L, Erdle N, Montgomery E, Amos S, et al. (2010) Pyruvate kinase M2 is a target of the tumor-suppressive microRNA-326 and regulates the survival of glioma cells. Neuro Oncol 12: 1102-1112.
20. Sachdeva M, Zhu S, Wu F, Wu H, Walia V, et al. (2009) p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc Natl Acad Sci U S A 106: 3207-3212.
21. Li X, Luo F, Li Q, Xu M, Feng D, et al. (2011) Identification of new aberrantly expressed miRNAs in intestinal-type gastric cancer and its clinical significance. Oncol Rep 26: 1431-1439.
22. Liu X, Sempere LF, Galimberti F, Freemantle SJ, Black C, et al. (2009) Uncovering growth-suppressive MicroRNAs in lung cancer. Clin Cancer Res 15: 1177-1183.
23. Iorio MV, Ferracin M, Liu C-G, Veronese A, Spizzo R, et al. (2005) MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65: 7065-7070.
24. Zaman MS, Chen Y, Deng G, Shahryari V, Suh SO, et al. (2010) The functional significance of microRNA-145 in prostate cancer. Br J Cancer 103: 256-264.
25. La Rocca G, Badin M, Shi B, Xu S-Q, Deangelis T, et al. (2009) Mechanism of growth inhibition by MicroRNA 145: the role of the IGF-I receptor signaling pathway. J Cell Physiol 220: 485-491.
26. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS, (2009) MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137: 647-658.
27. Jia Y, Liu H, Zhuang Q, Xu S, Yang Z, et al. (2012) Tumorigenicity of cancer stem-like cells derived from hepatocarcinoma is regulated by microRNA-145. Oncol Rep 27: 1865-1872.
28. Lu Y, Chopp M, Zhang X, Katakowski M, Buller B, et al. (2012) MiR-145 reduces ADAM17 expression and inhibits in vitro migration and invasion of glioma cells. Oncol Rep 29: 67-72.
29. Sachdeva M, Mo Y-Y, (2010) miR-145-mediated suppression of cell growth, invasion and metastasis. Am J Transl Res 2: 170-180.
30. Kano M, Seki N, Kikkawa N, Fujimura L, Hoshino I, et al. (2010) miR-145, miR-133a and miR-133b: Tumor suppressive miRNAs target FSCN1 in esophageal squamous cell carcinoma. Int J Cancer 127: 2804-2814.
31. Kent OA, Chivukula RR, Mullendore M, Wentzel EA, Feldmann G, et al. (2010) Repression of the miR-143/145 cluster by oncogenic Ras initiates a tumor-promoting feed-forward pathway. Genes Dev 24: 2754-2759.
32. Suh SO, Chen Y, Zaman MS, Hirata H, Yamamura S, et al. (2011) MicroRNA-145 is regulated by DNA methylation and p53 gene mutation in prostate cancer. Carcinogenesis 32: 772-778.
33. Artym VV, Yamada KM, Mueller SC, (2009) ECM degradation assays for analyzing local cell invasion. Methods Mol Biol 522: 211-219.
34. Dhar A, Ray A, (2010) The CCN family proteins in carcinogenesis. Exp Oncol 32: 2-9.
35. Xie D, Yin D, Wang HJ, Liu GT, Elashoff R, et al. (2004) Levels of expression of CYR61 and CTGF are prognostic for tumor progression and survival of individuals with gliomas. Clin Cancer Res 10: 2072-2081.
36. Yin D, Chen W, O'Kelly J, Lu D, Ham M, et al. (2010) Connective tissue growth factor associated with oncogenic activities and drug resistance in glioblastoma multiforme. Int J Cancer 127: 2257-2267.
37. Bennewith KL, Huang X, Ham CM, Graves EE, Erler JT, et al. (2009) The role of tumor cell-derived connective tissue growth factor (CTGF/CCN2) in pancreatic tumor growth. Cancer Res 69: 775-784.
38. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, (2004) Identification of human brain tumour initiating cells. Nature 432: 396-401.
39. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, et al. (2004) Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64: 7011-7021.
40. Venere M, Fine HA, Dirks PB, Rich JN, (2011) Cancer stem cells in gliomas: identifying and understanding the apex cell in cancer's hierarchy. Glia 59: 1148-1154.
41. Schultz C, Lemke N, Ge S, Golembieski WA, Rempel SA, (2002) Secreted protein acidic and rich in cysteine promotes glioma invasion and delays tumor growth in vivo. Cancer Res 62: 6270-6277.
42. Liu D-P, Wang Y, Koeffler HP, Xie D, (2007) Ephrin-A1 is a negative regulator in glioma through down-regulation of EphA2 and FAK. Int J Oncol 30: 865-871.
43. Golembieski WA, Thomas SL, Schultz CR, Yunker CK, McClung HM, et al. (2008) HSP27 mediates SPARC-induced changes in glioma morphology, migration and invasion. Glia 56: 1061-1075.
44. Zhu L, Yan W, Rodriguez-Canales J, Rosenberg AM, Hu N, et al. (2011) MicroRNA analysis of microdissected normal squamous esophageal epithelium and tumor cells. Am J Cancer Res 1: 574-584.
45. Hamfjord J, Stangeland AM, Hughes T, Skrede ML, Tveit KM, et al. (2012) Differential expression of miRNAs in colorectal cancer: Comparison of paired tumor tissue and adjacent normal mucosa using high-throughput sequencing. PLoS One 7: e34150.
46. Lujambio A, Ropero S, Ballestar E, Fraga MF, Cerrato C, et al. (2007) Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res 67: 1424-1429.
47. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, et al. (2009) Modulation of microRNA processing by p53. Nature 460: 529-533.
48. Litofsky NS, Recht LD, (1997) The impact of p53 tumor suppressor gene on glioma biology. Neurosurg Focus 3: e4.
49. Sachdeva M, Liu Q, Cao J, Lu Z, Mo Y-Y (2012) Negative regulation of miR-145 by C/EBP-β through the Akt pathway in cancer cells. Nucleic Acids Res Epub ahead of print.
50. Zhu H, Dougherty U, Robinson V, Mustafi R, Pekow J, et al. (2011) EGFR signals downregulate tumor suppressors miR-143 and miR-145 in Western diet-promoted murine colon cancer: role of G1 regulators. Mol Cancer Res 9: 960-975.
51. Zhang J, Sun Q, Zhang Z, Ge S, Han ZG, et al. (2012) Loss of microRNA-143/145 disturbs cellular growth and apoptosis of human epithelial cancers by impairing the MDM2-p53 feedback loop. Oncogene Epub ahead of print.
52. Xu Q, Liu L-Z, Qian X, Chen Q, Jiang Y, et al. (2012) MiR-145 directly targets p70S6K1 in cancer cells to inhibit tumor growth and angiogenesis. Nucleic Acids Res 40: 761-774.
53. Sachdeva M, Mo Y-Y, (2010) MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1. Cancer Res 70: 378-387.
54. Gao P, Xing AY, Zhou GY, Zhang TG, Zhang JP, et al. (2012) The molecular mechanism of microRNA-145 to suppress invasion-metastasis cascade in gastric cancer. Oncogene Epub ahead of print.
55. Zhang J, Guo H, Qian G, Ge S, Ji H, et al. (2010) MiR-145, a new regulator of the DNA fragmentation factor-45 (DFF45)-mediated apoptotic network. Mol Cancer 9: 211.
56. Gregersen LH, Jacobsen AB, Frankel LB, Wen J, Krogh A, et al. (2010) MicroRNA-145 targets YES and STAT1 in colon cancer cells. PLoS One 5: e8836.
57. Perbal B, (2004) CCN proteins: multifunctional signalling regulators. Lancet 363: 62-64.
58. Abreu JG, Ketpura NI, Reversade B, De Robertis EM, (2002) Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat Cell Biol 4: 599-604.
59. Ernst A, Campos B, Meier J, Devens F, Liesenberg F, et al. (2010) De-repression of CTGF via the miR-17-92 cluster upon differentiation of human glioblastoma spheroid cultures. Oncogene 29: 3411-3422.
60. Sala-Torra O, Gundacker HM, Stirewalt DL, Ladne PA, Pogosova-Agadjanyan EL, et al. (2007) Connective tissue growth factor (CTGF) expression and outcome in adult patients with acute lymphoblastic leukemia. Blood 109: 3080-3083.
61. Deng Y-Z, Chen P-P, Wang Y, Yin D, Koeffler HP, et al. (2007) Connective tissue growth factor is overexpressed in esophageal squamous cell carcinoma and promotes tumorigenicity through beta-catenin-T-cell factor/Lef signaling. J Biol Chem 282: 36571-36581.
62. Kwon S, Munroe X, Crawley SC, Lee HY, Spong S, et al. (2007) Expression of connective tissue growth factor in pancreatic cancer cell lines. Int J Oncol 31: 693-703.
63. Yang F, Tuxhorn JA, Ressler SJ, McAlhany SJ, Dang TD, et al. (2005) Stromal expression of connective tissue growth factor promotes angiogenesis and prostate cancer tumorigenesis. Cancer Res 65: 8887-8895.
64. Pan L-H, Beppu T, Kurose A, Yamauchi K, Sugawara A, et al. (2002) Neoplastic cells and proliferating endothelial cells express connective tissue growth factor (CTGF) in glioblastoma. Neurol Res 24: 677-683.
65. Tan T-W, Lai C-H, Huang C-Y, Yang W-H, Chen H-T, et al. (2009) CTGF enhances migration and MMP-13 up-regulation via alphavbeta3 integrin, FAK, ERK, and NF-kappaB-dependent pathway in human chondrosarcoma cells. J Cell Biochem 107: 345-356.
66. Wang J-C, Lai S, Guo X, Zhang X, de Crombrugghe B, et al. (2010) Attenuation of fibrosis in vitro and in vivo with SPARC siRNA. Arthritis Res Ther 12: R60.
67. Edwards LA, Woolard K, Son MJ, Li A, Lee J, et al. (2011) Effect of brain- and tumor-derived connective tissue growth factor on glioma invasion. J Natl Cancer Inst 103: 1162-1178.
68. Lomonaco SL, Finniss S, Xiang C, DeCarvalho A, Umansky F, et al. (2009) The induction of autophagy by γ-radiation contributes to the radioresistance of glioma stem cells. Int J Cancer 125: 717-722.
69. deCarvalho AC, Nelson K, Lemke N, Lehman NL, Arbab AS, et al. (2010) Gliosarcoma stem cells undergo glial and dmesenchymal differentiation in vivo. Stem Cells 28: 181-190.
70. Ziv-Av A, Taller D, Attia M, Xiang C, Lee HK, et al. (2011) RTVP-1 expression is regulated by SRF downstream of protein kinase C and contributes to the effect of SRF on glioma cell migration. Cell Signal 23: 1936-1943.
71. Rosenzweig T, Ziv-Av A, Xiang C, Lu W, Cazacu S, et al. (2006) Related to testes-specific, vespid, and pathogenesis protein-1 (RTVP-1) is overexpressed in gliomas and regulates the growth, survival, and invasion of glioma cells. Cancer Res 66: 4139-4148.
72. Berdeaux RL, Diaz B, Kim L, Martin GS, (2004) Active Rho is localized to podosomes induced by oncogenic Src and is required for their assembly and function. J Cell Biol 166: 317-323.