Regulation of miR106b cluster through the RB pathway: Mechanismand functional targets

Cell Cycle

Volumn 12, Issue 1, 2013, Pages 98-111

  Thangavel, Chellappagounder ^a   Boopathi, Ettickan ^d   Ertel, Adam ^b   Lim, Meng ^c   Addya, Sankar ^b   Fortina, Paolo ^b   Witkiewicz, Agnieszka K ^a   Knudsen, Erik S ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

CDK4 6 inhibitor; MCM7; Mir106b cluster; P21; PD 0332991; PTEN; Retinoblastoma protein (pRB); Transcriptional repression

Indexed keywords

6 ACETYL 8 CYCLOPENTYL 5 METHYL 2 [5 (1 PIPERAZINYL) 2 PYRIDINYLAMINO] 8H PYRIDO[2,3 D]PYRIMIDIN 7 ONE; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; MICRORNA; MICRORNA 106B; MINICHROMOSOME MAINTENANCE PROTEIN 7; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

EID: 84872321372     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.23029     Document Type: Article

References (51)

1. Knudsen ES, Knudsen KE. Tailoring to RB: tumour suppressor status and therapeutic response. Nat Rev Cancer 2008; 8:714-24; PMID:19143056; http://dx.doi.org/10.1038/nrc2401
2. Burkhart DL, Sage J. Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat Rev Cancer 2008; 8:671-82; PMID:18650841; http://dx.doi.org/10.1038/nrc2399
3. Goodrich DW. The retinoblastoma tumor-suppressor gene, the exception that proves the rule. Oncogene 2006; 25:5233-43; PMID:16936742; http://dx.doi.org/ 10.1038/sj.onc.1209616
4. Mittnacht S. Control of pRB phosphorylation. Curr Opin Genet Dev 1998; 8:21-7; PMID:9529601; http://dx.doi.org/10.1016/S0959-437X(98)80057-9
5. Wang JY, Knudsen ES, Welch PJ. The retinoblastoma tumor suppressor protein. Adv Cancer Res 1994; 64:25-85; PMID:7879661; http://dx.doi.org/10.1016/ S0065-230X(08)60834-9
6. Ishida S, Huang E, Zuzan H, Spang R, Leone G, West M, et al. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol Cell Biol 2001; 21:4684-99; PMID:11416145; http://dx.doi.org/10.1128/MCB.21.14.4684-4699.2001
7. Markey MP, Angus SP, Strobeck MW, Williams SL, Gunawardena RW, Aronow BJ, et al. Unbiased analysis of RB-mediated transcriptional repression identifies novel targets and distinctions from E2F action. Cancer Res 2002; 62:6587-97; PMID:12438254
8. Arima Y, Hayashi H, Sasaki M, Hosonaga M, Goto TM, Chiyoda T, et al. Induction of ZEB proteins by inactivation of RB protein is key determinant of mesenchymal phenotype of breast cancer. J Biol Chem 2012; 287:7896-906; PMID:22262832; http://dx.doi.org/10.1074/jbc.M111.313759
9. Ertel A, Dean JL, Rui H, Liu C, Witkiewicz AK, Knudsen KE, et al. RB pathway disruption in breast cancer: differential association with disease subtypes, disease-specific prognosis and therapeutic response. Cell Cycle 2010; 9:4153-63; PMID:20948315; http://dx.doi.org/10.4161/cc.9.20.13454
10. Herschkowitz JI, He X, Fan C, Perou CM. The functional loss of the retinoblastoma tumour suppressor is a common event in basal-like and luminal B breast carcinomas. Breast Cancer Res 2008; 10:R75; PMID:18782450; http://dx.doi.org/10.1186/bcr2142
11. Petrocca F, Visone R, Onelli MR, Shah MH, Nicoloso MS, de Martino I, et al. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 2008; 13:272-86; PMID:18328430; http://dx.doi.org/10.1016/j.ccr.2008.02.013
12. Bao J, Li D, Wang L, Wu J, Hu Y, Wang Z, et al. MicroRNA-449 and microRNA-34b/c function redundantly in murine testes by targeting E2F transcription factor-retinoblastoma protein (E2F-pRb) pathway. J Biol Chem 2012; 287:21686-98; PMID:22570483; http://dx.doi.org/10.1074/jbc.M111.328054
13. Benhamed M, Herbig U, Ye T, Dejean A, Bischof O. Senescence is an endogenous trigger for microRNA-directed transcriptional gene silencing in human cells. Nat Cell Biol 2012; 14:266-75; PMID:22366686; http://dx.doi.org/10.1038/ ncb2443
14. Ofir M, Hacohen D, Ginsberg D. MiR-15 and miR-16 are direct transcriptional targets of E2F1 that limit E2F-induced proliferation by targeting cyclin E. Mol Cancer Res 2011; 9:440-7; PMID:21454377; http://dx.doi.org/10.1158/1541-7786.MCR-10-0344
15. Khoshnaw SM, Green AR, Powe DG, Ellis IO. MicroRNA involvement in the pathogenesis and management of breast cancer. J Clin Pathol 2009; 62:422-8; PMID:19398594; http://dx.doi.org/10.1136/jcp.2008.060681
16. Smith AL, Iwanaga R, Drasin DJ, Micalizzi DS, Vartuli RL, Tan AC, et al. The miR-106b-25 cluster targets Smad7, activates TGF-β signaling, and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer. Oncogene 2012; In press; PMID:22286770; http://dx.doi.org/10.1038/onc.2012.11
17. Sempere LF, Christensen M, Silahtaroglu A, Bak M, Heath CV, Schwartz G, et al. Altered MicroRNA expression confined to specific epithelial cell subpopulations in breast cancer. Cancer Res 2007; 67:11612-20; PMID:18089790; http://dx.doi.org/10.1158/0008-5472.CAN-07-5019
18. Liu S, Patel SH, Ginestier C, Ibarra I, Martin-Trevino R, Bai S, et al. MicroRNA93 regulates proliferation and differentiation of normal and malignant breast stem cells. PLoS Genet 2012; 8:e1002751; PMID:22685420; http://dx.doi.org/10.1371/journal.pgen.1002751
19. Feng B, Dong TT, Wang LL, Zhou HM, Zhao HC, Dong F, et al. Colorectal cancer migration and invasion initiated by microRNA-106a. PLoS One 2012; 7:e43452; PMID:22912877; http://dx.doi.org/10.1371/journal.pone.0043452
20. Knudsen ES, Wang JY. Targeting the RB pathway in cancer therapy. Clin Cancer Res 2010; 16:1094-9; PMID:20145169; http://dx.doi.org/10.1158/1078-0432. CCR-09-0787
21. Toogood PL, Harvey PJ, Repine JT, Sheehan DJ, VanderWel SN, Zhou H, et al. Discovery of a potent and selective inhibitor of cyclin-dependent kinase 4/6. J Med Chem 2005; 48:2388-406; PMID:15801831; http://dx.doi.org/10.1021/ jm049354h
22. Dean JL, McClendon AK, Hickey TE, Butler LM, Tilley WD, Witkiewicz AK, et al. Therapeutic response to CDK4/6 inhibition in breast cancer defined by ex vivo analyses of human tumors. Cell Cycle 2012; 11:2756-61; PMID:22767154; http://dx.doi.org/10.4161/cc.21195
23. Nana-Sinkam SP, Fabbri M, Croce CM. MicroRNAs in cancer: personalizing diagnosis and therapy. Ann N Y Acad Sci 2010; 1210:25-33; PMID:20973796; http://dx.doi.org/10.1111/j.1749-6632.2010.05822.x
24. Ravi A, Gurtan AM, Kumar MS, Bhutkar A, Chin C, Lu V, et al. Proliferation and tumorigenesis of a murine sarcoma cell line in the absence of DICER1. Cancer Cell 2012; 21:848-55; PMID:22698408; http://dx.doi.org/10.1016/j. ccr.2012.04.037
25. Iorio MV, Croce CM. microRNA involvement in human cancer. Carcinogenesis 2012; 33:1126-33; PMID:22491715; http://dx.doi.org/10.1093/carcin/bgs140
26. Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, et al. Identification of the miR-106b-25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal 2010; 3:ra29; PMID:20388916; http://dx.doi.org/10.1126/scisignal. 2000594
27. Liu Y, Zhang Y, Wen J, Liu L, Zhai X, Liu J, et al. A genetic variant in the promoter region of miR-106b-25 cluster and risk of HBV infection and hepatocellular carcinoma. PLoS One 2012; 7:e32230; PMID:22393390; http://dx.doi.org/10.1371/journal.pone.0032230
28. Li Z, Yang CS, Nakashima K, Rana TM. Small RNA-mediated regulation of iPS cell generation. EMBO J 2011; 30:823-34; PMID:21285944; http://dx.doi.org/10. 1038/emboj.2011.2
29. Li Y, Tan W, Neo TW, Aung MO, Wasser S, Lim SG, et al. Role of the miR-106b-25 microRNA cluster in hepatocellular carcinoma. Cancer Sci 2009; 100:1234-42; PMID:19486339; http://dx.doi.org/10.1111/j.1349-7006.2009.01164.x
30. Chuang TD, Luo X, Panda H, Chegini N. miR-93/106b and their host gene, MCM7, are differentially expressed in leiomyomas and functionally target F3 and IL-8. Mol Endocrinol 2012; 26:1028-42; PMID:22556343; http://dx.doi.org/10.1210/ me.2012-1075
31. Markey MP, Bergseid J, Bosco EE, Stengel K, Xu H, Mayhew CN, et al. Loss of the retinoblastoma tumor suppressor: differential action on transcriptional programs related to cell cycle control and immune function. Oncogene 2007; 26:6307-18; PMID:17452985; http://dx.doi.org/10.1038/sj.onc.1210450
32. Li SS, Xue WC, Khoo US, Ngan HY, Chan KY, Tam IY, et al. Replicative MCM7 protein as a proliferation marker in endometrial carcinoma: a tissue microarray and clinicopathological analysis. Histopathology 2005; 46:307-13; PMID:15720416; http://dx.doi.org/10.1111/j.1365-2559.2005.02069.x
33. Ishimi Y. A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex. J Biol Chem 1997; 272:24508-13; PMID:9305914; http://dx.doi.org/10.1074/jbc.272.39.24508
34. Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, et al. Identification of the miR-106b-25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal 2010; 3:ra29; PMID:20388916; http://dx.doi.org/10.1126/scisignal. 2000594
35. Kan T, Sato F, Ito T, Matsumura N, David S, Cheng Y, et al. The miR-106b-25 polycistron, activated by genomic amplification, functions as an oncogene by suppressing p21 and Bim. Gastroenterology 2009; 136:1689-700; PMID:19422085; http://dx.doi.org/10.1053/j.gastro.2009.02.002
36. Smith AL, Iwanaga R, Drasin DJ, Micalizzi DS, Vartuli RL, Tan AC, et al. The miR-106b-25 cluster targets Smad7, activates TGF-β signaling, and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer. Oncogene 2012; In press; PMID:22286770; http://dx.doi.org/10.1038/onc.2012.11
37. Ivanovska I, Ball AS, Diaz RL, Magnus JF, Kibukawa M, Schelter JM, et al. MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell Biol 2008; 28:2167-74; PMID:18212054; http://dx.doi.org/ 10.1128/MCB.01977-07
38. Blenkiron C, Goldstein LD, Thorne NP, Spiteri I, Chin SF, Dunning MJ, et al. MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype. Genome Biol 2007; 8:R214; PMID:17922911; http://dx.doi.org/10. 1186/gb-2007-8-10-r214
39. Arima Y, Inoue Y, Shibata T, Hayashi H, Nagano O, Saya H, et al. Rb depletion results in deregulation of E-cadherin and induction of cellular phenotypic changes that are characteristic of the epithelial-to-mesenchymal transition. Cancer Res 2008; 68:5104-12; PMID:18593909; http://dx.doi.org/10. 1158/0008-5472.CAN-07-5680
40. Rizzi F, Belloni L, Crafa P, Lazzaretti M, Remondini D, Ferretti S, et al. A novel gene signature for molecular diagnosis of human prostate cancer by RT-qPCR. PLoS One 2008; 3:e3617; PMID:18974881; http://dx.doi.org/10.1371/ journal.pone.0003617
41. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 2010; 465:1033-8; PMID:20577206; http://dx.doi.org/10.1038/ nature09144
42. Dean JL, Thangavel C, McClendon AK, Reed CA, Knudsen ES. Therapeutic CDK4/6 inhibition in breast cancer: key mechanisms of response and failure. Oncogene 2010; 29:4018-32; PMID:20473330; http://dx.doi.org/10.1038/onc.2010.154
43. Dasgupta P, Sun J, Wang S, Fusaro G, Betts V, Padmanabhan J, et al. Disruption of the Rb - Raf-1 interaction inhibits tumor growth and angiogenesis. Mol Cell Biol 2004; 24:9527-41; PMID:15485920; http://dx.doi.org/10.1128/MCB. 24.21.9527-9541.2004
44. Suzuki S, Adachi A, Hiraiwa A, Ohashi M, Ishibashi M, Kiyono T. Cloning and characterization of human MCM7 promoter. Gene 1998; 216:85-91; PMID:9714754; http://dx.doi.org/10.1016/S0378-1119(98)00323-0
45. Thangavel C, Dean JL, Ertel A, Knudsen KE, Aldaz CM, Witkiewicz AK, et al. Therapeutically activating RB: reestablishing cell cycle control in endocrine therapy-resistant breast cancer. Endocr Relat Cancer 2011; 18:333-45; PMID:21367843; http://dx.doi.org/10.1530/ERC-10-0262
46. Kolachala VL, Wang L, Obertone TS, Prasad M, Yan Y, Dalmasso G, et al. Adenosine 2B receptor expression is post-transcriptionally regulated by microRNA. J Biol Chem 2010; 285:18184-90; PMID:20388705; http://dx.doi.org/10. 1074/jbc.M109.066555
47. Thangavel C, Boopathi E, Shapiro BH. Intrinsic sexually dimorphic expression of the principal human CYP3A4 correlated with suboptimal activation of GH/glucocorticoid-dependent transcriptional pathways in men. Endocrinology 2011; 152:4813-24; PMID:21952236; http://dx.doi.org/10.1210/en.2011-1274
48. Djuranovic S, Zinchenko MK, Hur JK, Nahvi A, Brunelle JL, Rogers EJ, et al. Allosteric regulation of Argonaute proteins by miRNAs. Nat Struct Mol Biol 2010; 17:144-50; PMID:20062058; http://dx.doi.org/10.1038/nsmb.1736
49. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011; 108:5003-8; PMID:21383194; http://dx.doi.org/10.1073/pnas.1019055108
50. Chiodelli P, Urbinati C, Mitola S, Tanghetti E, Rusnati M. Sialic acid associated with αvβ3 integrin mediates HIV-1 Tat protein interaction and endothelial cell proangiogenic activation. J Biol Chem 2012; 287:20456-66; PMID:22528484; http://dx.doi.org/10.1074/jbc.M111.337139
51. Witkiewicz AK, Rivadeneira DB, Ertel A, Kline J, Hyslop T, Schwartz GF, et al. Association of RB/p16-pathway perturbations with DCIS recurrence: dependence on tumor versus tissue microenvironment. Am J Pathol 2011; 179:1171-8; PMID:21756866; http://dx.doi.org/10.1016/j.ajpath.2011.05.043