Dysregulation of the miR-34a-SIRT1 axis inhibits breast cancer stemness

Oncotarget

Volumn 6, Issue 12, 2015, Pages 10432-10444

  Ma, Wei ^a   Xiao, Gary Guishan ^b,c   Mao, Jun ^a   Lu, Ying ^a   Song, Bo ^a   Wang, Lihui ^a   Fan, Shujun ^a   Fan, Panhong ^a   Hou, Zhenhuan ^a   Li, Jiazhi ^a   Yu, Xiaotang ^a   Wang, Bo ^a   Wang, Huan ^a   Wang, Honghai ^a   Xu, Fei ^a   Li, Yan ^a   Liu, Qiang ^a   Li, Lianhong ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

^b DALIAN UNIVERSITY OF TECHNOLOGY   (China)

^c CREIGHTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

CD44+ CD24 BCSCs; miR 34 ; SIRT1; Stemness

Indexed keywords

ALDEHYDE DEHYDROGENASE ISOENZYME 1; BMI1 PROTEIN; MICRORNA 34A; SIRTUIN 1; TRANSCRIPTION FACTOR NANOG; MICRORNA; MIRN34 MICRORNA, HUMAN; SIRT1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER INHIBITION; CANCER STEM CELL; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MCF 7 CELL LINE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; STABLE EXPRESSION; TUMOR VOLUME; TUMOR XENOGRAFT; ANIMAL; BREAST NEOPLASMS; DRUG SCREENING; GENETIC TRANSFECTION; GENETICS; MCF-7 CELL LINE; METABOLISM; NUDE MOUSE; PATHOLOGY; RANDOMIZATION;

ANIMALS; BREAST NEOPLASMS; FEMALE; HUMANS; MCF-7 CELLS; MICE; MICE, NUDE; MICRORNAS; RANDOM ALLOCATION; RNA, SMALL INTERFERING; SIRTUIN 1; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84929600774     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3394     Document Type: Article

References (61)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61:69-90.
2. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, Wong H, Rosen J, Chang J. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst. 2008; 100:672-679.
3. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, Rimm DL, Wong H, Rodriguez A, Herschkowitz JI, Fan C, Zhang X, He X, Pavlick A, Gutierrez MC, Renshaw L, Larionov AA, Faratian D, Hilsenbeck SG, Perou CM, Lewis MT, Rosen JM, Chang JC. Residual breast cancers after conventional therapy display mesenchymal as well as tumor- initiating features. Proc Natl Acad Sci USA. 2009; 106:13820-13825.
4. Nguyen NP, Almeida FS, Chi A, Nguyen LM, Cohen D, Karlsson U, Vinh-Hung V. Molecular biology of breast cancer stem cells: potential clinical applications. Cancer Treat Rev. 2010; 36:485-491.
5. Jordan CT. Cancer stem cell biology: from leukemia to solid tumors. Curr Opin Cell Biol. 2004; 16:708-712.
6. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003; 100:3983-3988.
7. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009; 138:645-659.
8. Chan CH, Morrow JK, Li CF, Gao Y, Jin G, Moten A, Stagg LJ, Ladbury JE, Cai Z, Xu D, Logothetis CJ, Hung MC, Zhang S, Lin HK. Pharmacological inactivation of Skp2 SCF ubiquitin ligase restricts cancer stem cell traits and cancer progression. Cell. 2013; 154:556-568.
9. Sachlos E, Risueno RM, Laronde S, Shapovalova Z, Lee JH, Russell J, Malig M, McNicol JD, Fiebig-Comyn A, Graham M, Levadoux-Martin M, Lee JB, Giacomelli AO, Hassell JA, Fischer-Russell D, Trus MR, Foley R, Leber B, Xenocostas A, Brown ED, Collins TJ, Bhatia M. Identification of drugs including a dopamine receptor antagonist that selectively target cancer stem cells. Cell. 2012; 149:1284-1297.
10. Ginestier C, Liu S, Diebel ME, Korkaya H, Luo M, Brown M, Wicinski J, Cabaud O, Charafe-Jauffret E, Birnbaum D, Guan JL, Dontu G, Wicha MS. CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J Clin Invest. 2010; 120:485-497.
11. van Kouwenhove M, Kedde M, Agami R. MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat Rev Cancer. 2011; 11:644-656.
12. Zimmerman AL, Wu S. MicroRNAs, cancer and cancer stem cells. Cancer Lett. 2011; 300:10-19.
13. Ambros V. The functions of animal microRNAs. Nature. 2004; 431:350-355.
14. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136:215-233.
15. Zhang B, Pan X, Cobb GP, Anderson TA. microRNAs as oncogenes and tumor suppressors. Dev Biol. 2007; 302:1-12.
16. Le Quesne J, Caldas C. Micro-RNAs and breast cancer. Mol Oncol. 2010; 4:230-241.
17. Agostini M, knight RA. miR-34:from bench to bedside. Oncotarget. 2014; 5:872-881.
18. Eades G, Yao Y, Yang M, Zhang Y, Chumsri S, Zhou Q. miR-200a regulates SIRT1 expression and epithelial to mesenchymal transition (EMT)-like transformation in mammary epithelial cells. J Biol Chem. 2011; 286:25992-26002.
19. Guo X, Wu Y, Hartley RS. MicroRNA-125a represses cell growth by targeting HuR in breast cancer. RNA Biol. 2009; 6:575-583.
20. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, Diehn M, Liu H, Panula SP, Chiao E, Dirbas FM, Somlo G, Pera RA, Lao K, Clarke MF. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell. 2009; 138:592-603.
21. Li L, Xie X, Luo J, Liu M, Xi S, Guo J, Kong Y, Wu M, Gao J, Xie Z, Tang J, Wang X, Wei W, Yang M, Hung MC, Xie X. Targeted expression of miR-34a using the T-VISA system suppresses breast cancer cell growth and invasion. Mol Ther. 2012; 20:2326-2334.
22. Wu F, Zhu S, Ding Y, Beck WT, Mo YY. MicroRNAmediated regulation of Ubc9 expression in cancer cells. Clin Cancer Res. 2009; 15:1550-1557.
23. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ. 2010; 17:193-199.
24. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N, Bentwich Z, Oren M. Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell. 2007; 26:731-743.
25. Siemens H, Jackstadt R, Kaller M, Hermeking H. Repression of c-kit by p53 is mediated by miR-34 and is associated with reduced chemoresistance, migration and stemness. Oncotarget. 2013; 4:1399-1415.
26. Lodygin D, Tarasov V, Epanchintsev A, Berking C, Knyazeva T, Körner H, Knyazev P, Diebold J, Hermeking H. Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell cycle. 2008; 7:2591-2600.
27. Cole KA, Attiyeh EF, Mosse YP, Laquaglia MJ, Diskin SJ, Brodeur GM, Maris JM. A functional screen identifies miR-34a as a candidate neuroblastoma tumor suppressor gene. Mol Cancer Res. 2008; 6:735-742.
28. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D, Tang DG. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med. 2011; 17:211-215.
29. Li L, Yuan L, Luo J, Gao J, Guo J, Xie X. MiR-34a inhibits proliferation and migration of breast cancer through down-regulation of Bcl-2 and SIRT1. Clin Exp Med. 2013; 13:109-117.
30. Yamakuchi M, Ferlito M, Lowenstein CJ. miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci USA. 2008; 105:13421-13426.
31. Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L, Xiang D, Desano JT, Bommer GT, Fan D, Fearon ER, Lawrence TS, Xu L. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One. 2009; 4:e6816.
32. Nalls D, Tang SN, Rodova M, Srivastava RK, Shankar S. Targeting epigenetic regulation of miR-34a for treatment of pancreatic cancer by inhibition of pancreatic cancer stem cells. PLoS One. 2011; 6:e24099.
33. Liu T, Liu PY, Marshall GM. The critical role of the class III histone deacetylase SIRT1 in cancer. Cancer Res. 2009; 69:1702-1705.
34. Luo J, Nikolaev AY, Imai S, Chen D, Su F, Shiloh A, Guarente L, Gu W. Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell. 2001; 107:137-148.
35. Lee JT, Gu W. SIRT1: Regulator of p53 Deacetylation. Genes & Cancer. 2013; 4:112-117.
36. Calvanese V, Fraga MF. SirT1 brings stemness closer to cancer and aging. Aging. 2011; 3:162-167.
37. Calvanese V, Lara E, Suárez-Alvarez B, Abu Dawud R, Vázquez-Chantada M, Martínez-Chantar ML, Embade N, López-Nieva P, Horrillo A, Hmadcha A, Soria B, Piazzolla D, Herranz D, Serrano M, Mato JM, Andrews PW, López-Larrea C, Esteller M, Fraga MF. Sirtuin 1 regulation of developmental genes during differentiation of stem cells. Proc Natl Acad Sci USA. 2010; 107:13736-13741.
38. Ou X, Chae HD, Wang RH, Shelley WC, Cooper S, Taylor T, Kim YJ, Deng CX, Yoder MC, Broxmeyer HE. SIRT1 deficiency compromises mouse embryonic stem cell hematopoietic differentiation, and embryonic and adult hematopoiesis in the mouse. Blood. 2011; 117:440-450.
39. Han MK, Song EK, Guo Y, Ou X, Mantel C, Broxmeyer HE. SIRT1 regulates apoptosis and Nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization. Cell stem cell. 2008; 2:241-251.
40. Li L, Wang L, Li L, Wang Z, Ho Y, McDonald T, Holyoake TL, Chen W, Bhatia R. Activation of p53 by SIRT1 inhibition enhances elimination of CML leukemia stem cells in combination with imatinib. Cancer cell. 2012; 21:266-281.
41. Wang ZQ, Chen WY. Emerging roles of SIRT1 in cancer drug resistance. Genes & Cancer. 2013; 4:82-90.
42. Yamakuchi M, Lowenstein CJ. MiR-34, SIRT1 and p53: the feedback loop. Cell cycle. 2009; 8:712-715.
43. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, Schott A, Hayes D, Birnbaum D, Wicha MS, Dontu G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007; 1:555-567.
44. Lin T, Chao C, Saito S, Mazur SJ, Murphy ME, Appella E, Xu Y. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat Cell Biol. 2005; 7:165-171.
45. Mao J, Song B, Shi Y, Wang B, Fan S, Yu X, Tang Y, Li L. ShRNA targeting Notch1 sensitizes breast cancer stem cell to paclitaxel. Int J Biochem Cell Biol. 2013; 45:1064-1073.
46. Park EY, Chang E, Lee EJ, Lee HW, Kang HG, Chun KH, Woo Y, Kong H, Ko JY, Suzuki H, Song E, Park JH. Targeting of miR-34a-NOTCH1 axis reduced breast cancer stemness and chemoresistance. Cancer Res. 2014 Nov 3. pii: canres.1140.2014 [Epub ahead of print].
47. Schirmer U, Doberstein K, Rupp AK, Bretz NP, Wuttig D, Kiefel H, Breunig C, Fiegl H, Müller-Holzner E, Zeillinger R, Schuster E, Zeimet AG, Sültmann H, Altevogt P. Role of miR-34a as a suppressor of L1CAM in endometrial carcinoma. Oncotarget. 2014; 5:462-472.
48. 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.
49. Li N, Fu H, Tie Y, Hu Z, Kong W, Wu Y, Zheng X. miR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett. 2009; 275:44-53.
50. Gallardo E, Navarro A, Vinolas N, Marrades RM, Diaz T, Gel B, Quera A, Bandres E, Garcia-Foncillas J, Ramirez J, Monzo M. miR-34a as a prognostic marker of relapse in surgically resected non-small-cell lung cancer. Carcinogenesis. 2009; 30:1903-1909.
51. Peurala H, Greco D, Heikkinen T, Kaur S, Bartkova J, Jamshidi M, Aittomaki K, Heikkila P, Bartek J, Blomqvist C, Butzow R, Nevanlinna H. MiR-34a expression has an effect for lower risk of metastasis and associates with expression patterns predicting clinical outcome in breast cancer. PLoS One. 2011; 6:e26122.
52. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE, Zhai Y, Giordano TJ, Qin ZS, Moore BB, MacDougald OA, Cho KR, Fearon ER. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol. 2007; 17:1298-1307.
53. Guessous F, Zhang Y, Kofman A, Catania A, Li Y, Schiff D, Purow B, Abounader R. microRNA-34a is tumor suppressive in brain tumors and glioma stem cells. Cell Cycle. 2010; 9:1031-1036.
54. Liu TF and McCall CE. Deacetylation by SIRT1 reprograms inflammation and cancer. Genes & Cancer. 2013; 4:135-147.
55. Lin ZH, Fang DY. The roles of SIRT1 in cancer. Genes & Cancer. 2013; 4:97-104.
56. Raynes R, Brunquell J. Stress Inducibility of SIRT1 and Its Role in Cytoprotection and Cancer. Genes & Cancer. 2013; 4:172-182.
57. McBurney MW, Clark-Knowles KV, Caron AZ. SIRT1 is a Highly Networked Protein That Mediates the Adaptation to Chronic Physiological Stress. Genes & Cancer. 2013; 4:125-134.
58. Sung JY, Kim R, Kim JE, Lee J. Balance between SIRT1 and DBC1 expression is lost in breast cancer. Cancer Sci. 2010; 101:1738-1744.
59. Lee YL, Peng Q, Fong SW, Chen AC, Lee KF, Ng EH, Nagy A, Yeung WS. Sirtuin 1 facilitates generation of induced pluripotent stem cells from mouse embryonic fibroblasts through the miR-34a and p53 pathways. PLoS one. 2012; 7:e45633.
60. Saunders LR, Sharma AD, Tawney J, Nakagawa M, Okita K, Yamanaka S, Willenbring H, Verdin E. miRNAs regulate SIRT1 expression during mouse embryonic stem cell differentiation and in adultmouse tissues. Aging. 2010; 2:415-431.
61. Chang CJ, Hsu CC, Yung MC, Chen KY, Tzao C, Wu WF, Chou HY, Lee YY, Lu KH, Chiou SH, Ma HI. Enhanced radiosensitivity and radiation-induced apoptosis in glioma CD133-positive cells by knockdown of SirT1 expression. Biochem Biophys Res Commun. 2009; 380:236-242.