Microrna mir-98 inhibits tumor angiogenesis and invasion by targeting activin receptor-like kinase-4 and matrix metalloproteinase-11

Oncotarget

Volumn 3, Issue 11, 2012, Pages 1370-1385

  Siragam, Vinayakumar ^a,d   Rutnam, Zina Jeyapalan ^a,d   Yang, Weining ^b   Fang, Ling ^a,d   Luo, Linlin ^b   Yang, Xiangling ^a,d   Li, Minhui ^a,d   Deng, Zhaoqun ^a,d   Qian, Jun ^c   Peng, Chun ^b   Yang, Burton B ^a,d  

^a Institute of Clinical Evaluative Sciences   (Canada)

^b YORK UNIVERSITY   (Canada)

^c AFFILIATED PEOPLE S HOSPITAL OF JIANGSU UNIVERSITY   (China)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Angiogenesis; Invasion; MicroRNA; MiR 98; Tumorigenesis

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 4; MICRORNA; MICRORNA 98; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; STROMELYSIN 3; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER CELL; CANCER INHIBITION; CANCER INVASION; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME REPRESSION; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION;

EID: 84872790880     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.717     Document Type: Article

References (50)

1. Hoodless PA and Wrana JL. Mechanism and function of signaling by the TGF beta superfamily. Curr Top Microbiol Immunol. 1998; 228:235-272.
2. Pepper MS. Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 1997; 8(1):21-43.
3. Graham H and Peng C. Activin receptor-like kinases: structure, function and clinical implications. Endocr Metab Immune Disord Drug Targets. 2006; 6(1):45-58.
4. Massague J and Chen YG. Controlling TGF-beta signaling. Genes Dev. 2000; 14(6):627-644.
5. Viticchie G, Lena AM, Latina A, Formosa A, Gregersen LH, Lund AH, Bernardini S, Mauriello A, Miano R, Spagnoli LG, Knight RA, Candi E and Melino G. MiR- 203 controls proliferation, migration and invasive potential of prostate cancer cell lines. Cell Cycle. 2011; 10(7):1121-1131.
6. Shatseva T, Lee DY, Deng Z and Yang BB. MicroRNA miR-199a-3p regulates cell proliferation and survival by targeting caveolin-2. J Cell Sci. 2011; 124(Pt 16):2826-2836.
7. Hidaka H, Seki N, Yoshino H, Yamasaki T, Yamada Y, Nohata N, Fuse M, Nakagawa M and Enokida H. Tumor suppressive microRNA-1285 regulates novel molecular targets: aberrant expression and functional significance in renal cell carcinoma. Oncotarget. 2012; 3(1):44-57.
8. Noonan EJ, Place RF, Basak S, Pookot D and Li LC. miR- 449a causes Rb-dependent cell cycle arrest and senescence in prostate cancer cells. Oncotarget. 2010; 1(5):349-358.
9. Lerner M, Lundgren J, Akhoondi S, Jahn A, Ng HF, Akbari Moqadam F, Oude Vrielink JA, Agami R, Den Boer ML, Grander D and Sangfelt O. MiRNA-27a controls FBW7/ hCDC4-dependent cyclin E degradation and cell cycle progression. Cell Cycle. 2011; 10(13):2172-2183.
10. Kahai S, Lee SC, Lee DY, Yang J, Li M, Wang CH, Jiang Z, Zhang Y, Peng C and Yang BB. MicroRNA miR-378 regulates nephronectin expression modulating osteoblast differentiation by targeting GalNT-7. PLoS One. 2009; 4(10):e7535.
11. Juan AH and Sartorelli V. MicroRNA-214 and polycomb group proteins: a regulatory circuit controlling differentiation and cell fate decisions. Cell Cycle. 2010; 9(8):1445-1446.
12. Luo L, Ye G, Nadeem L, Fu G, Yang BB, Honarparvar E, Dunk C, Lye S and Peng C. MicroRNA-378a-5p promotes trophoblast cell survival, migration and invasion by targeting Nodal. J Cell Sci. 2012; 125(Pt 13):3124-3132.
13. Hwang CI, Choi J, Zhou Z, Flesken-Nikitin A, Tarakhovsky A and Nikitin AY. MET-dependent cancer invasion may be preprogrammed by early alterations of p53-regulated feedforward loop and triggered by stromal cell-derived HGF. Cell Cycle. 2011; 10(22):3834-3840.
14. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A. 2006; 103(7):2257-2261.
15. Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T and Hammond SM. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes Dev. 2006; 20(16):2202-2207.
16. Nohata N, Hanazawa T, Enokida H and Seki N. microRNA- 1/133a and microRNA-206/133b clusters: dysregulation and functional roles in human cancers. Oncotarget. 2012; 3(1):9-21.
17. Valastyan S and Weinberg RA. miR-31: a crucial overseer of tumor metastasis and other emerging roles. Cell Cycle. 2010; 9(11):2124-2129.
18. Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S, Egan DA, Li A, Huang G, Klein-Szanto AJ, Gimotty PA, Katsaros D, Coukos G, Zhang L, Pure E and Agami R. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol. 2008; 10(2):202-210.
19. Rutnam ZJ and Yang BB. The involvement of microRNAs in malignant transformation. Histol Histopathol. 2012; 27(10):1263-1270.
20. Hua Z, Lv Q, Ye W, Wong CK, Cai G, Gu D, Ji Y, Zhao C, Wang J, Yang BB and Zhang Y. MiRNA-directed regulation of VEGF and other angiogenic factors under hypoxia. PLoS One. 2006; 1:e116.
21. Ye W, Lv Q, Wong CK, Hu S, Fu C, Hua Z, Cai G, Li G, Yang BB and Zhang Y. The effect of central loops in miRNA:MRE duplexes on the efficiency of miRNAmediated gene regulation. PLoS One. 2008; 3(3):e1719.
22. Jeyapalan Z, Deng Z, Shatseva T, Fang L, He C and Yang BB. Expression of CD44 3'-untranslated region regulates endogenous microRNA functions in tumorigenesis and angiogenesis. Nucleic Acids Res. 2011; 39(8):3026-3041.
23. Lee DY, Deng Z, Wang CH and Yang BB. MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression. Proc Natl Acad Sci U S A. 2007; 104(51):20350-20355.
24. Fang L, Deng Z, Shatseva T, Yang J, Peng C, Du WW, Yee AJ, Ang LC, He C, Shan SW and Yang BB. MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-beta8. Oncogene. 2011; 30(7):806-821.
25. Zou C, Xu Q, Mao F, Li D, Bian C, Liu LZ, Jiang Y, Chen X, Qi Y, Zhang X, Wang X, Sun Q, Kung HF, Lin MC, Dress A, Wardle F, et al. MiR-145 inhibits tumor angiogenesis and growth by N-RAS and VEGF. Cell Cycle. 2012; 11(11):2137-2145.
26. Smits M, Nilsson J, Mir SE, van der Stoop PM, Hulleman E, Niers JM, de Witt Hamer PC, Marquez VE, Cloos J, Krichevsky AM, Noske DP, Tannous BA and Wurdinger T. miR-101 is down-regulated in glioblastoma resulting in EZH2-induced proliferation, migration, and angiogenesis. Oncotarget. 2010; 1(8):710-720.
27. Wang Q, Huang Z, Xue H, Jin C, Ju XL, Han JD and Chen YG. MicroRNA miR-24 inhibits erythropoiesis by targeting activin type I receptor ALK4. Blood. 2008; 111(2):588-595.
28. Hebert C, Norris K, Scheper MA, Nikitakis N and Sauk JJ. High mobility group A2 is a target for miRNA-98 in head and neck squamous cell carcinoma. Mol Cancer. 2007; 6:5.
29. Hu G, Zhou R, Liu J, Gong AY, Eischeid AN, Dittman JW and Chen XM. MicroRNA-98 and let-7 confer cholangiocyte expression of cytokine-inducible Src homology 2-containing protein in response to microbial challenge. J Immunol. 2009; 183(3):1617-1624.
30. Du L, Schageman JJ, Subauste MC, Saber B, Hammond SM, Prudkin L, Wistuba, II, Ji L, Roth JA, Minna JD and Pertsemlidis A. miR-93, miR-98, and miR-197 regulate expression of tumor suppressor gene FUS1. Mol Cancer Res. 2009; 7(8):1234-1243.
31. Panda H, Chuang TD, Luo X and Chegini N. Endometrial miR-181a and miR-98 expression is altered during transition from normal into cancerous state and target PGR, PGRMC1, CYP19A1, DDX3X, and TIMP3. J Clin Endocrinol Metab. 2012; 97(7):E1316-1326.
32. Zhang S, Zhang C, Li Y, Wang P, Yue Z and Xie S. miR-98 regulates cisplatin-induced A549 cell death by inhibiting TP53 pathway. Biomed Pharmacother. 2011; 65(6):436-442.
33. Wendler A, Keller D, Albrecht C, Peluso JJ and Wehling M. Involvement of let-7/miR-98 microRNAs in the regulation of progesterone receptor membrane component 1 expression in ovarian cancer cells. Oncol Rep. 2011; 25(1):273-279.
34. Alajez NM, Shi W, Hui AB, Bruce J, Lenarduzzi M, Ito E, Yue S, O'Sullivan B and Liu FF. Enhancer of Zeste homolog 2 (EZH2) is overexpressed in recurrent nasopharyngeal carcinoma and is regulated by miR-26a, miR-101, and miR-98. Cell Death Dis. 2010; 1:e85.
35. Yan LX, Huang XF, Shao Q, Huang MY, Deng L, Wu QL, Zeng YX and Shao JY. MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. Rna. 2008; 14(11):2348-2360.
36. Peruzzi D, Mori F, Conforti A, Lazzaro D, De Rinaldis E, Ciliberto G, La Monica N and Aurisicchio L. MMP11: a novel target antigen for cancer immunotherapy. Clin Cancer Res. 2009; 15(12):4104-4113.
37. Najy AJ, Day KC and Day ML. ADAM15 supports prostate cancer metastasis by modulating tumor cell-endothelial cell interaction. Cancer Res. 2008; 68(4):1092-1099.
38. Egeblad M and Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2002; 2(3):161-174.
39. Xu G, Zhong Y, Munir S, Yang BB, Tsang BK and Peng C. Nodal induces apoptosis and inhibits proliferation in human epithelial ovarian cancer cells via activin receptorlike kinase 7. J Clin Endocrinol Metab. 2004; 89(11):5523-5534.
40. Xu G, Zhou H, Wang Q, Auersperg N and Peng C. Activin receptor-like kinase 7 induces apoptosis through upregulation of Bax and down-regulation of Xiap in normal and malignant ovarian epithelial cell lines. Mol Cancer Res. 2006; 4(4):235-246.
41. Hardy KM, Kirschmann DA, Seftor EA, Margaryan NV, Postovit LM, Strizzi L and Hendrix MJ. Regulation of the embryonic morphogen Nodal by Notch4 facilitates manifestation of the aggressive melanoma phenotype. Cancer Res. 2010; 70(24):10340-10350.
42. Strizzi L, Postovit LM, Margaryan NV, Seftor EA, Abbott DE, Seftor RE, Salomon DS and Hendrix MJ. Emerging roles of nodal and Cripto-1: from embryogenesis to breast cancer progression. Breast Dis. 2008; 29:91-103.
43. Zhong Y, Xu G, Ye G, Lee D, Modica-Amore J and Peng C. Nodal and activin receptor-like kinase 7 induce apoptosis in human breast cancer cell lines: Role of caspase 3. Int J Physiol Pathophysiol Pharmacol. 2009; 1(1):83-96.
44. Kelber JA, Shani G, Booker EC, Vale WW and Gray PC. Cripto is a noncompetitive activin antagonist that forms analogous signaling complexes with activin and nodal. J Biol Chem. 2008; 283(8):4490-4500.
45. de Castro NP, Rangel MC, Nagaoka T, Salomon DS and Bianco C. Cripto-1: an embryonic gene that promotes tumorigenesis. Future Oncol. 2010; 6(7):1127-1142.
46. Nadeem L, Munir S, Fu G, Dunk C, Baczyk D, Caniggia I, Lye S and Peng C. Nodal signals through activin receptorlike kinase 7 to inhibit trophoblast migration and invasion: implication in the pathogenesis of preeclampsia. Am J Pathol. 2011; 178(3):1177-1189.
47. LaPierre DP, Lee DY, Li SZ, Xie YZ, Zhong L, Sheng W, Deng Z and Yang BB. The ability of versican to simultaneously cause apoptotic resistance and sensitivity. Cancer Res. 2007; 67(10):4742-4750.
48. Wang CH, Lee DY, Deng Z, Jeyapalan Z, Lee SC, Kahai S, Lu WY, Zhang Y and Yang BB. MicroRNA miR-328 regulates zonation morphogenesis by targeting CD44 expression. PLoS One. 2008; 3(6):e2420.
49. Zheng PS, Wen J, Ang LC, Sheng W, Viloria-Petit A, Wang Y, Wu Y, Kerbel RS and Yang BB. Versican/PG-M G3 domain promotes tumor growth and angiogenesis. FASEB J. 2004; 18(6):754-756.
50. Lee DY, Shatseva T, Jeyapalan Z, Du WW, Deng Z and Yang BB. A 3'-untranslated region (3'UTR) induces organ adhesion by regulating miR-199a* functions. PLoS One. 2009; 4(2):e4527.