MicroRNA-34 suppresses breast cancer invasion and metastasis by directly targeting Fra-1

Oncogene

Volumn 32, Issue 36, 2013, Pages 4294-4303

  Yang, S ^a   Li, Y ^a   Gao, J ^a   Zhang, T ^a   Li, S ^a   Luo, A ^a   Chen, H ^a   Ding, F ^a   Wang, X ^a   Liu, Z ^a  

^a CANCER HOSPITAL   (China)

Author keywords

breast cancer; metastasis; miR 34a; miR 34c

Indexed keywords

MESSENGER RNA; MICRORNA 34A; MICRORNA 34C; TRANSCRIPTION FACTOR FRA 1; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; BREAST CANCER; CELL MIGRATION; CELL MOTILITY; DOWN REGULATION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; LYMPH NODE METASTASIS; METASTASIS; NONHUMAN; ONCOGENE; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR INVASION;

3' UNTRANSLATED REGIONS; ANIMALS; BASE PAIRING; BASE SEQUENCE; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPHATIC METASTASIS; MICE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PROTO-ONCOGENE PROTEINS C-FOS;

EID: 84883742665     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.432     Document Type: Article

References (68)

1. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 2011; 331: 1559-1564.
2. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 2003; 3: 453-458.
3. Steeg PS. Tumor metastasis: mechanistic insights and clinical challenges. Nat Med 2006; 12: 895-904.
4. Nicoloso MS, Spizzo R, Shimizu M, Rossi S, Calin GA. MicroRNAs-The micro steering wheel of tumour metastases. Nat Rev Cancer 2009; 9: 293-302.
5. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-233.
6. Valastyan S, Reinhardt F, Benaich N, Calogrias D, Szasz AM, Wang ZC et al. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 2009; 137: 1032-1046.
7. Tavazoie SF, Alarcon C, Oskarsson T, Padua D, Wang Q, Bos PD et al. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008; 451: 147-152.
8. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res 2008; 68: 7846-7854.
9. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 2008; 10: 593-601.
10. Lv XB, Jiao Y, Qing Y, Hu H, Cui X, Lin T et al. miR-124 suppresses multiple steps of breast cancer metastasis by targeting a cohort of pro-metastatic genes in vitro. Chin J Cancer 2011; 30: 821-830.
11. Wu ZS, Wu Q, Wang CQ, Wang XN, Huang J, Zhao JJ et al. miR-340 inhibition of breast cancer cell migration and invasion through targeting of oncoprotein c-Met. Cancer 2011; 117: 2842-2852.
12. Li Y, Zhang M, Chen H, Dong Z, Ganapathy V, Thangaraju M et al. Ratio of miR-196s to HOXC8 messenger RNA correlates with breast cancer cell migration and metastasis. Cancer Res 2010; 70: 7894-7904.
13. Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007; 449: 682-688.
14. Gee HE, Camps C, Buffa FM, Colella S, Sheldon H, Gleadle JM et al. MicroRNA-10b and breast cancer metastasis. Nature 2008; 455: E8-E9.
15. Stinson S, Lackner MR, Adai AT, Yu N, Kim HJ, O'Brien C et al. TRPS1 targeting by miR-221/222 promotes the epithelial-to-mesenchymal transition in breast cancer. Sci Signal 2011; 4: ra41.
16. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007; 26: 745-752.
17. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N et al. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 2007; 26: 731-743.
18. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE et al. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 2007; 17: 1298-1307.
19. Tazawa H, Tsuchiya N, Izumiya M, Nakagama H. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci USA 2007; 104: 15472-15477.
20. Sun F, Fu H, Liu Q, Tie Y, Zhu J, Xing R et al. Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett 2008; 582: 1564-1568.
21. Li N, Fu H, Tie Y, Hu Z, Kong W, Wu Y et al. miR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett 2009; 275: 44-53.
22. Kim NH, Kim HS, Li XY, Lee I, Choi HS, Kang SE et al. A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition. J Cell Biol 2011; 195: 417-433.
23. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y et al. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res 2008; 68: 4123-4132.
24. Guessous F, Zhang Y, Kofman A, Catania A, Li Y, Schiff D et al. microRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle 2010; 9: 1031-1036.
25. Welch C, Chen Y, Stallings RL. MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 2007; 26: 5017-5022.
26. Wei JS, Song YK, Durinck S, Chen QR, Cheuk AT, Tsang P et al. The MYCN oncogene is a direct target of miR-34a. Oncogene 2008; 27: 5204-5213.
27. Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L et al. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One 2009; 4: e6816.
28. Chim CS, Wong KY, Qi Y, Loong F, Lam WL, Wong LG et al. Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 2010; 31: 745-750.
29. Wiggins JF, Ruffino L, Kelnar K, Omotola M, Patrawala L, Brown D et al. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res 2010; 70: 5923-5930.
30. Cannell IG, Kong YW, Johnston SJ, Chen ML, Collins HM, Dobbyn HC et al. p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc Natl Acad Sci USA 2010; 107: 5375-5380.
31. Chen L, Mayer JA, Krisko TI, Speers CW, Wang T, Hilsenbeck SG et al. Inhibition of the p38 kinase suppresses the proliferation of human ER-negative breast cancer cells. Cancer Res 2009; 69: 8853-8861.
32. Christoffersen NR, Shalgi R, Frankel LB, Leucci E, Lees M, Klausen M et al. p53-independent upregulation of miR-34a during oncogene-induced senescence represses MYC. Cell Death Differ 2010; 17: 236-245.
33. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009; 37: 1-13.
34. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ 2010; 17: 193-199.
35. Kustikova O, Kramerov D, Grigorian M, Berezin V, Bock E, Lukanidin E et al. Fra-1 induces morphological transformation and increases in vitro invasiveness and motility of epithelioid adenocarcinoma cells. Mol Cell Biol 1998; 18: 7095-7105.
36. Ramos-Nino ME, Scapoli L, Martinelli M, Land S, Mossman BT. Microarray analysis and RNA silencing link fra-1 to cd44 and c-met expression in mesothelioma. Cancer Res 2003; 63: 3539-3545.
37. Debinski W, Gibo DM. Fos-related antigen 1 modulates malignant features of glioma cells. Mol Cancer Res 2005; 3: 237-249.
38. Tkach V, Tulchinsky E, Lukanidin E, Vinson C, Bock E, Berezin V. Role of the Fos family members, c-Fos, Fra-1 and Fra-2, in the regulation of cell motility. Oncogene 2003; 22: 5045-5054.
39. Usui A, Hoshino I, Akutsu Y, Sakata H, Nishimori T, Murakami K et al. The molecular role of Fra-1 and its prognostic significance in human esophageal squamous cell carcinoma. Cancer 2012; 118: 3387-3396.
40. Sayan AE, Stanford R, Vickery R, Grigorenko E, Diesch J, Kulbicki K et al. Fra-1 controls motility of bladder cancer cells via transcriptional upregulation of the receptor tyrosine kinase AXL. Oncogene 2011; 25: 8.
41. Zajchowski DA, Bartholdi MF, Gong Y, Webster L, Liu HL, Munishkin A et al. Identification of gene expression profiles that predict the aggressive behavior of breast cancer cells. Cancer Res 2001; 61: 5168-5178.
42. Belguise K, Kersual N, Galtier F, Chalbos D. FRA-1 expression level regulates proliferation and invasiveness of breast cancer cells. Oncogene 2005; 24: 1434-1444.
43. Luo YP, Zhou H, Krueger J, Kaplan C, Liao D, Markowitz D et al. The role of protooncogene Fra-1 in remodeling the tumor microenvironment in support of breast tumor cell invasion and progression. Oncogene 2010; 29: 662-673.
44. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S et al. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci USA 2004; 101: 2999-3004.
45. Osborne RJ, Hamshere MG. A genome-wide map showing common regions of loss of heterozygosity/allelic imbalance in breast cancer. Cancer Res 2000; 60: 3706-3712.
46. Bieche I, Khodja A, Lidereau R. Deletion mapping of chromosomal region 1p32-pter in primary breast cancer. Genes Chromosomes Cancer 1999; 24: 255-263.
47. Nagai H, Negrini M, Carter SL, Gillum DR, Rosenberg AL, Schwartz GF et al. Detection and cloning of a common region of loss of heterozygosity at chromosome 1p in breast cancer. Cancer Res 1995; 55: 1752-1757.
48. Ellsworth RE, Ellsworth DL, Lubert SM, Hooke J, Somiari RI, Shriver CD. Highthroughput loss of heterozygosity mapping in 26 commonly deleted regions in breast cancer. Cancer Epidemiol Biomarkers Prev 2003; 12: 915-919.
49. Ellsworth RE, Hooke JA, Love B, Kane JL, Patney HL, Ellsworth DL et al. Correlation of levels and patterns of genomic instability with histological grading of invasive breast tumors. Breast Cancer Res Treat 2008; 107: 259-265.
50. Winqvist R, Hampton GM, Mannermaa A, Blanco G, Alavaikko M, Kiviniemi H et al. Loss of heterozygosity for chromosome 11 in primary human breast tumors is associated with poor survival after metastasis. Cancer Res 1995; 55: 2660-2664.
51. Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, Blanco D et al. A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci USA 2008; 105: 13556-13561.
52. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Korner H et al. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 2008; 7: 2591-2600.
53. Yu F, Jiao Y, Zhu Y, Wang Y, Zhu J, Cui X et al. MiR-34c down-regulation via DNA methylation promotes self-renewal and epithelial-mesenchymal transition in breast tumor-initiating cells. J Biol Chem 2012; 287: 465-473.
54. Siemens H, Jackstadt R, Hunten S, Kaller M, Menssen A, Gotz U et al. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle 2011; 10: 4256-4271.
55. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H et al. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med 2011; 17: 211-215.
56. Choi YJ, Lin CP, Ho JJ, He X, Okada N, Bu P et al. miR-34 miRNAs provide a barrier for somatic cell reprogramming. Nat Cell Biol 2011; 13: 1353-1360.
57. Migliore C, Petrelli A, Ghiso E, Corso S, Capparuccia L, Eramo A et al. MicroRNAs impair MET-mediated invasive growth. Cancer Res 2008; 68: 10128-10136.
58. Hwang CI, Matoso A, Corney DC, Flesken-Nikitin A, Korner S, Wang W et al. Wildtype p53 controls cell motility and invasion by dual regulation of MET expression. Proc Natl Acad Sci USA 2011; 108: 14240-14245.
59. Mudduluru G, Ceppi P, Kumarswamy R, Scagliotti GV, Papotti M, Allgayer H. Regulation of Axl receptor tyrosine kinase expression by miR-34a and miR-199a/b in solid cancer. Oncogene 2011; 30: 2888-2899.
60. Mackiewicz M, Huppi K, Pitt JJ, Dorsey TH, Ambs S, Caplen NJ. Identification of the receptor tyrosine kinase AXL in breast cancer as a target for the human miR-34a microRNA. Breast Cancer Res Treat 2011; 130: 663-679.
61. Kim NH, Kim HS, Li XY, Lee I, Choi HS, Kang SE et al. A p53/miRNA-34 axis regulates Snail1-dependent cancer cell epithelial-mesenchymal transition. J Cell Biol 2011; 195: 417-433.
62. Wu J, Wu G, Lv L, Ren YF, Zhang XJ, Xue YF et al. MicroRNA-34a inhibits migration and invasion of colon cancer cells via targeting to Fra-1. Carcinogenesis 2012; 33: 519-528.
63. Serewko MM, Popa C, Dahler AL, Smith L, Strutton GM, Coman W et al. Alterations in gene expression and activity during squamous cell carcinoma development. Cancer Res 2002; 62: 3759-3765.
64. Chiappetta G, Tallini G, De Biasio MC, Pentimalli F, de Nigris F, Losito S et al. FRA-1 expression in hyperplastic and neoplastic thyroid diseases. Clin Cancer Res 2000; 6: 4300-4306.
65. Milde-Langosch K, Roder H, Andritzky B, Aslan B, Hemminger G, Brinkmann A et al. The role of the AP-1 transcription factors c-Fos, FosB, Fra-1 and Fra-2 in the invasion process of mammary carcinomas. Breast Cancer Res Treat 2004; 86: 139-152.
66. Bamberger AM, Methner C, Lisboa BW, Stadtler C, Schulte HM, Loning T et al. Expression pattern of the AP-1 family in breast cancer: association of fosB expression with a well-differentiated, receptor-positive tumor phenotype. Int J Cancer 1999; 84: 533-538.
67. Vial E, Marshall CJ. Elevated ERK-MAP kinase activity protects the FOS family member FRA-1 against proteasomal degradation in colon carcinoma cells. J Cell Sci 2003; 116(Pt 24): 4957-4963.
68. Tian Y, Luo A, Cai Y, Su Q, Ding F, Chen H et al. MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J Biol Chem 2010; 285: 7986-7994.