MicroRNA-34a is a potent tumor suppressor molecule in vivo in neuroblastoma

BMC Cancer

Volumn 11, Issue , 2011, Pages

  Tivnan, Amanda ^a,b   Tracey, Lorraine ^c   Buckley, Patrick G ^a,b   Alcock, Leah C ^a,b   Davidoff, Andrew M ^c,d   Stallings, Raymond L ^a,b  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b OUR LADY S CHILDREN S HOSPITAL   (Ireland)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B KINASE; JANUS KINASE; MICRORNA; MICRORNA 34A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; MIXED LINEAGE KINASE; MIXED LINEAGE KINASE 1; PHOSPHOPROTEIN; PROTEIN BCL 2; PROTEIN TYROSINE PHOSPHATASE; S6 KINASE; STAT PROTEIN; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F3; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; LUCIFERASE; MAP3K9 PROTEIN, HUMAN; MIRN34 MICRORNA, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIOLUMINESCENCE; CANCER CELL CULTURE; CELL CYCLE; CELL CYCLE ARREST; CELL GROWTH; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEUROBLASTOMA; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION; SIGNAL TRANSDUCTION; TUMOR VOLUME; ANIMAL; CELL PROLIFERATION; DRUG SCREENING; GENETICS; HUMAN; LUMINESCENCE; METABOLISM; MOUSE MUTANT; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; GENES, TUMOR SUPPRESSOR; HUMANS; LUCIFERASES; LUMINESCENT MEASUREMENTS; MAP KINASE KINASE KINASES; MICE; MICE, SCID; MICRORNAS; NEUROBLASTOMA; PHOSPHOPROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 78951477589     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-11-33     Document Type: Article

References (43)

1. Breving K, Esquela-Kerscher A. The complexities of microRNA regulation: mirandering around the rules. Int J Biochem Cell Biol 2009, 42(8):1316-1329. 10.1016/j.biocel.2009.09.016, 19800023.
2. Kim VN. Small RNAs: classification, biogenesis, and function. Mol Cells 2005, 19(1):1-15. 10.1016/j.molcel.2005.05.026, 15750334.
3. Garzon R, Calin GA, Croce CM. MicroRNAs in Cancer. Annu Rev Med 2009, 60:167-179. 10.1146/annurev.med.59.053006.104707, 19630570.
4. Brodeur GM. Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 2003, 3(3):203-216. 10.1038/nrc1014, 12612655.
5. Stallings RL, Foley NH, Bryan K, Buckley PG, Bray I. Therapeutic targeting of miRNAs in neuroblastoma. Expert Opin Ther Targets 2010, 14(9):951-962. 10.1517/14728222.2010.510136, 20658962.
6. Welch C, Chen Y, Stallings RL. MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 2007, 26(34):5017-5022. 10.1038/sj.onc.1210293, 17297439.
7. Stallings RL. Are chromosomal imbalances important in cancer?. Trends Genet 2007, 23(6):278-283. 10.1016/j.tig.2007.03.009, 17400327.
8. 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(5):735-742. 10.1158/1541-7786.MCR-07-2102, 18505919.
9. Wei JS, Song YK, Durinck S, Chen QR, Cheuk AT, Tsang P, Zhang Q, Thiele CJ, Slack A, Shohet J, et al. The MYCN oncogene is a direct target of miR-34a. Oncogene 2008, 27(39):5204-5213. 10.1038/onc.2008.154, 2562938, 18504438.
10. Chim CS, Wong KY, Qi Y, Loong F, Lam WL, Wong LG, Jin DY, Costello JF, Liang R. Epigenetic inactivation of the miR-34a in hematological malignancies. Carcinogenesis 31(4):745-750. 10.1093/carcin/bgq033, 20118199.
11. 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(1):44-53. 10.1016/j.canlet.2008.09.035, 19006648.
12. Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L, Xiang D, Desano JT, Bommer GT, Fan D, et al. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One 2009, 4(8):e6816. 10.1371/journal.pone.0006816, 2729376, 19714243.
13. 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(39):15472-15477. 10.1073/pnas.0707351104, 2000550, 17875987.
14. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE, Zhai Y, Giordano TJ, Qin ZS, Moore BB, et al. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 2007, 17(15):1298-1307. 10.1016/j.cub.2007.06.068, 17656095.
15. Luan S, Sun L, Huang F. MicroRNA-34a: a novel tumor suppressor in p53-mutant glioma cell line U251. Arch Med Res 2010, 41(2):67-74. 10.1016/j.arcmed.2010.02.007, 20470934.
16. Yamakuchi M, Ferlito M, Lowenstein CJ. miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci USA 2008, 105(36):13421-13426. 10.1073/pnas.0801613105, 2533205, 18755897.
17. Liu H, Brannon AR, Reddy AR, Alexe G, Seiler MW, Arreola A, Oza JH, Yao M, Juan D, Liou LS, et al. Identifying mRNA targets of microRNA dysregulated in cancer: with application to clear cell Renal Cell Carcinoma. BMC Syst Biol 2010, 4:51. 10.1186/1752-0509-4-51, 2876063, 20420713.
18. Pang RT, Leung CO, Ye TM, Liu W, Chiu PC, Lam KK, Lee KF, Yeung WS. MicroRNA-34a suppresses invasion through downregulation of Notch1 and Jagged1 in cervical carcinoma and choriocarcinoma cells. Carcinogenesis 2010, 31(6):1037-1044. 10.1093/carcin/bgq066, 20351093.
19. Sun F, Fu H, Liu Q, Tie Y, Zhu J, Xing R, Sun Z, Zheng X. Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett 2008, 582(10):1564-1568. 10.1016/j.febslet.2008.03.057, 18406353.
20. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, Feldmann G, Yamakuchi M, Ferlito M, Lowenstein CJ, et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 2007, 26(5):745-752. 10.1016/j.molcel.2007.05.010, 1939978, 17540599.
21. 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(5):731-743. 10.1016/j.molcel.2007.05.017, 17540598.
22. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A, Meister G, Hermeking H. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 2007, 6(13):1586-1593. 10.4161/cc.6.13.4436, 17554199.
23. Cai KM, Bao XL, Kong XH, Jinag W, Mao MR, Chu JS, Huang YJ, Zhao XJ. Hsa-miR-34c suppresses growth and invasion of human laryngeal carcinoma cells via targeting c-Met. Int J Mol Med 25(4):565-571.
24. Hagman Z, Larne O, Edsjo A, Bjartell A, Ehrnstrom RA, Ulmert D, Lilja H, Ceder Y. miR-34c is down regulated in prostate cancer and exerts tumor suppressive functions. Int J Cancer
25. Li Y, Guessous F, Zhang Y, Dipierro C, Kefas B, Johnson E, Marcinkiewicz L, Jiang J, Yang Y, Schmittgen TD, et al. MicroRNA-34a inhibits glioblastoma growth by targeting multiple oncogenes. Cancer Res 2009, 69(19):7569-7576. 10.1158/0008-5472.CAN-09-0529, 2756313, 19773441.
26. Wiggins JF, Ruffino L, Kelnar K, Omotola M, Patrawala L, Brown D, Bader AG. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res 2010, 70(14):5923-5930. 10.1158/0008-5472.CAN-10-0655, 20570894.
27. Chen Y, Zhu X, Zhang X, Liu B, Huang L. Nanoparticles Modified With Tumor-targeting scFv Deliver siRNA and miRNA for Cancer Therapy. Mol Ther 2010, 18(9):1650-1656. 10.1038/mt.2010.136, 20606648.
28. McKenzie PP, Guichard SM, Middlemas DS, Ashmun RA, Danks MK, Harris LC. Wild-type p53 can induce p21 and apoptosis in neuroblastoma cells but the DNA damage-induced G1 checkpoint function is attenuated. Clin Cancer Res 1999, 5(12):4199-4207.
29. Dickson PV, Hamner B, Ng CY, Hall MM, Zhou J, Hargrove PW, McCarville MB, Davidoff AM. In vivo bioluminescence imaging for early detection and monitoring of disease progression in a murine model of neuroblastoma. J Pediatr Surg 2007, 42(7):1172-1179. 10.1016/j.jpedsurg.2007.02.027, 17618876.
30. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 2007, 27(1):91-105. 10.1016/j.molcel.2007.06.017, 17612493.
31. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 2001, 22(2):153-183. 10.1210/er.22.2.153, 11294822.
32. Zhuang S, Schnellmann RG. A death-promoting role for extracellular signal-regulated kinase. J Pharmacol Exp Ther 2006, 319(3):991-997. 10.1124/jpet.106.107367, 16801453.
33. Subramaniam S, Unsicker K. ERK and cell death: ERK1/2 in neuronal death. FEBS J 2010, 277(1):22-29. 10.1111/j.1742-4658.2009.07367.x, 19843173.
34. Cheung EC, Slack RS. Emerging role for ERK as a key regulator of neuronal apoptosis. Sci STKE 2004, 2004(251):PE45. 10.1126/stke.2512004pe45, 15383672.
35. Kusaba T, Nakayama T, Yamazumi K, Yakata Y, Yoshizaki A, Inoue K, Nagayasu T, Sekine I. Activation of STAT3 is a marker of poor prognosis in human colorectal cancer. Oncol Rep 2006, 15(6):1445-1451.
36. Alvarez JV, Greulich H, Sellers WR, Meyerson M, Frank DA. Signal transducer and activator of transcription 3 is required for the oncogenic effects of non-small-cell lung cancer-associated mutations of the epidermal growth factor receptor. Cancer Res 2006, 66(6):3162-3168. 10.1158/0008-5472.CAN-05-3757, 16540667.
37. Chai H, Luo AZ, Weerasinghe P, Brown RE. Sorafenib downregulates ERK/Akt and STAT3 survival pathways and induces apoptosis in a human neuroblastoma cell line. Int J Clin Exp Pathol 2010, 3(4):408-415. 2872747, 20490331.
38. Gheeya JS, Chen QR, Benjamin CD, Cheuk AT, Tsang P, Chung JY, Metaferia BB, Badgett TC, Johansson P, Wei JS, et al. Screening a panel of drugs with diverse mechanisms of action yields potential therapeutic agents against neuroblastoma. Cancer Biol Ther 2009, 8(24):2386-2395. 10.4161/cbt.8.24.10184, 2829338, 19946221.
39. Greenberg AK, Basu S, Hu J, Yie TA, Tchou-Wong KM, Rom WN, Lee TC. Selective p38 activation in human non-small cell lung cancer. Am J Respir Cell Mol Biol 2002, 26(5):558-564.
40. Liu J, Lin A. Role of JNK activation in apoptosis: a double-edged sword. Cell Res 2005, 15(1):36-42. 10.1038/sj.cr.7290262, 15686625.
41. Bost F, McKay R, Bost M, Potapova O, Dean NM, Mercola D. The Jun kinase 2 isoform is preferentially required for epidermal growth factor-induced transformation of human A549 lung carcinoma cells. Mol Cell Biol 1999, 19(3):1938-1949. 83987, 10022881.
42. Potapova O, Anisimov SV, Gorospe M, Dougherty RH, Gaarde WA, Boheler KR, Holbrook NJ. Targets of c-Jun NH(2)-terminal kinase 2-mediated tumor growth regulation revealed by serial analysis of gene expression. Cancer Res 2002, 62(11):3257-3263.
43. Lee S, Das HK. Inhibition of basal activity of c-jun-NH2-terminal kinase (JNK) represses the expression of presenilin-1 by a p53-dependent mechanism. Brain Res 2008, 1207:19-31. 10.1016/j.brainres.2008.02.016, 18374905.