Pumilio facilitates miRNA regulation of the E2F3 oncogene

Genes and Development

Volumn 26, Issue 4, 2012, Pages 356-368

  Miles, Wayne O ^a   Tschöp, Katrin ^a   Herr, Anabel ^a   Ji, Jun Yuan ^a   Dyson, Nicholas J ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

Cancer; E2f3; miRNA; Pumilio

Indexed keywords

MICRORNA; PROTEIN; PUMILIO; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F3; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; BLADDER CARCINOMA; CANCER CELL; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; ENZYME REPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; NONHUMAN; ONCOGENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; ANIMALS; CELL LINE, TUMOR; DROSOPHILA; DROSOPHILA PROTEINS; E2F TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HELA CELLS; HUMANS; MICRORNAS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 84857167551     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.182568.111     Document Type: Article

References (57)

1. Ambrus AM, Nicolay BN, Rasheva VI, Suckling RJ, Frolov MV. 2007. dE2F2-independent rescue of proliferation in cells lacking an activator dE2F1. Mol Cell Biol 27: 8561-8570.
2. Barker DD, Wang C, Moore J, Dickinson LK, Lehmann R. 1992. Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant Nanos. Genes Dev 6: 2312-2326.
3. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. 2006. Relief of microRNA-mediated trans-lational repression in human cells subjected to stress. Cell 125: 1111-1124.
4. Bild AH, Parker JS, Gustafson AM, Acharya CR, Hoadley KA, Anders C, Marcom PK, Carey LA, Potti A, Nevins JR, et al. 2009. An integration of complementary strategies for gene-expression analysis to reveal novel therapeutic opportunities for breast cancer. Breast Cancer Res 11: R55. doi: 10.1186/bcr2344.
5. Binne UK, Classon MK, Dick FA, Wei W, Rape M, Kaelin WG, Naar AM, Dyson NJ. 2007. Retinoblastoma protein and anaphase-promoting complex physically interact and func-tionally cooperate during cell-cycle exit. Nat Cell Biol 9: 225-232.
6. Chagnovich D, Lehmann R. 2001. Poly(A)-independent regulation of maternal hunchback translation in the Drosophila embryo. Proc Natl Acad Sci 98: 11359-11364.
7. Chen HZ, Tsai SY, Leone G. 2009. Emerging roles of E2Fs in cancer: An exit from cell cycle control. Nat Rev Cancer 9: 785-797.
8. Coller J, Parker R. 2005. General translational repression by activators of mRNA decapping. Cell 122: 875-886.
9. Cooper CS, Nicholson AG, Foster C, Dodson A, Edwards S, Fletcher A, Roe T, Clark J, Joshi A, Norman A, et al. 2006. Nuclear overexpression of the E2F3 transcription factor in human lung cancer. Lung Cancer 54: 155-162.
10. Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, Petcherski AG, Moulder G, Barstead R, Wickens M, Kimble J. 2002. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417: 660-663.
11. Dimova DK, Stevaux O, Frolov MV, Dyson NJ. 2003. Cell cycle-dependent and cell cycle-independent control of transcription by the Drosophila E2F/RB pathway. Genes Dev 17: 2308-2320.
12. Duronio RJ, O'Farrell PH. 1994. Developmental control of a G1-S transcriptional program in Drosophila. Development 120: 1503-1515.
13. Duronio RJ, O'Farrell PH, Xie JE, Brook A, Dyson N. 1995. The transcription factor E2F is required for S phase during Drosophila embryogenesis. Genes Dev 9: 1445-1455.
14. Dyrskjot L, Ostenfeld MS, Bramsen JB, Silahtaroglu AN, Lamy P, Ramanathan R, Fristrup N, Jensen JL, Andersen CL, Zieger K, et al. 2009. Genomic profiling of microRNAs in bladder cancer: miR-129 is associated with poor outcome and promotes cell death in vitro. Cancer Res 69: 4851-4860.
15. Feber A, Clark J, Goodwin G, Dodson AR, Smith PH, Fletcher A, Edwards S, Flohr P, Falconer A, Roe T, et al. 2004. Amplification and overexpression of E2F3 in human bladder cancer. Oncogene 23: 1627-1630.
16. Friedman RC, Farh KK, Burge CB, Bartel DP. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105.
17. Galgano A, Forrer M, Jaskiewicz L, Kanitz A, Zavolan M, Gerber AP. 2008. Comparative analysis of mRNA targets for human PUF-family proteins suggests extensive interaction with the miRNA regulatory system. PLoS ONE 3: e3164. doi: 10.1371/ journal.pone.0003164.
18. Gerber AP, Luschnig S, Krasnow MA, Brown PO, Herschlag D. 2006. Genome-wide identification of mRNAs associated with the translational regulator PUMILIO in Drosophila melanogaster. Proc Natl Acad Sci 103: 4487-4492.
19. Ginter-Matuszewska B, Spik A, Rembiszewska A, Koyias C, Kupryjanczyk J, Jaruzelska J. 2009. The SNARE-associated component SNAPIN binds PUMILIO2 and NANOS1 proteins in human male germ cells. Mol Hum Reprod 15: 173-179.
20. Goldstrohm AC, Seay DJ, Hook BA, Wickens M. 2007. PUF protein-mediated deadenylation is catalyzed by Ccr4p. J Biol Chem 282: 109-114.
21. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. 2007. MicroRNA targeting specificity in mammals: Determinants beyond seed pairing. Mol Cell 27: 91-105.
22. Gu S, Kay MA. 2010. How do miRNAs mediate translational repression? Silence 1: 11.
23. Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell 100: 57-70.
24. Hurst CD, Tomlinson DC, Williams SV, Platt FM, Knowles MA. 2008. Inactivation of the Rb pathway and overexpression of both isoforms of E2F3 are obligate events in bladder tumours with 6p22 amplification. Oncogene 27: 2716-2727.
25. Hutvagner G, Zamore PD. 2002. A microRNA in a multiple-turnover RNAi enzyme complex. Science 297: 2056-2060.
26. Iaquinta PJ, Lees JA. 2007. Life and death decisions by the E2F transcription factors. Curr Opin Cell Biol 19: 649-657.
27. Kedde M, Strasser MJ, Boldajipour B, Oude Vrielink JA, Slanchev K, le Sage C, Nagel R, Voorhoeve PM, van Duijse J, Orom UA, et al. 2007. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131: 1273-1286.
28. Kedde M, van Kouwenhove M, Zwart W, Oude Vrielink JA, Elkon R, Agami R. 2010. A Pumilio-induced RNA structure switch in p27-39 UTR controls miR-221 and miR-222 accessibility. Nat Cell Biol 12: 1014-1020.
29. Lammens T, Li J, Leone G, De Veylder L. 2009. Atypical E2Fs: New players in the E2F transcription factor family. Trends Cell Biol 19: 111-118.
30. Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
31. Lin H, Spradling AC. 1997. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124: 2463-2476.
32. Mayr C, Bartel DP. 2009. Widespread shortening of 39 UTRs by alternative cleavage and polyadenylation activates onco-genes in cancer cells. Cell 138: 673-684.
33. Meister G, Landthaler M, Peters L, Chen PY, Urlaub H, Luhrmann R, Tuschl T. 2005. Identification of novel Argo-naute-associated proteins. Curr Biol 15: 2149-2155.
34. Moore FL, Jaruzelska J, Fox MS, Urano J, Firpo MT, Turek PJ, Dorfman DM, Pera RA. 2003. Human Pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (deleted in azoospermia) and DAZ-like proteins. Proc Natl Acad Sci 100: 538-543.
35. Morris EJ, Ji JY, Yang F, Di Stefano L, Herr A, Moon NS, Kwon EJ, Haigis KM, Naar AM, Dyson NJ. 2008. E2F1 represses b-catenin transcription and is antagonized by both pRB and CDK8. Nature 455: 552-556.
36. Murata Y, Wharton RP. 1995. Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80: 747-756.
37. Nolde MJ, Saka N, Reinert KL, Slack FJ. 2007. The Caenorhab-ditis elegans pumilio homolog, puf-9, is required for the 39UTR-mediated repression of the let-7 microRNA target gene, hbl-1. Dev Biol 305: 551-563.
38. Oeggerli M, Tomovska S, Schraml P, Calvano-Forte D, Schafroth S, Simon R, Gasser T, Mihatsch MJ, Sauter G. 2004. E2F3 amplification and overexpression is associated with invasive tumor growth and rapid tumor cell proliferation in urinary bladder cancer. Oncogene 23: 5616-5623.
39. Olsson AY, Feber A, Edwards S, Te Poele R, Giddings I, Merson S, Cooper CS. 2007. Role of E2F3 expression in modulating cellular proliferation rate in human bladder and prostate cancer cells. Oncogene 26: 1028-1037.
40. Parks AL, Cook R, Belvin M, Dompe NA, Fawcett R, Huppert K, Tan LR, Winter CG, Bogart KP, Deal JE, et al. 2004. Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet 36: 288-292.
41. Pearlberg J, Degot S, Endege W, Park J, Davies J, Gelfand E, Sawyer J, Conery A, Doench J, Li W, et al. 2005. Screens using RNAi and cDNA expression as surrogates for genetics in mammalian tissue culture cells. Cold Spring Harb Symp Quant Biol 70: 449-459.
42. Quenault T, Lithgow T, Traven A. 2011. PUF proteins: Repression, activation and mRNA localization. Trends Cell Biol 21: 104-112.
43. Sandberg R, Neilson JR, Sarma A, Sharp PA, Burge CB. 2008. Proliferating cells express mRNAs with shortened 39 untranslated regions and fewer microRNA target sites. Science 320: 1643-1647.
44. Schwamborn JC, Berezikov E, Knoblich JA. 2009. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136: 913-925.
45. Schweers BA, Walters KJ, Stern M. 2002. The Drosophila melanogaster translational repressor pumilio regulates neu-ronal excitability. Genetics 161: 1177-1185.
46. Sherr CJ. 1995. Mammalian G1 cyclins and cell cycle progression. Proc Assoc Am Physicians 107: 181-186.
47. Shibutani ST, de la Cruz AF, Tran V, Turbyfill WJ, Reis T, Edgar BA, Duronio RJ. 2008. Intrinsic negative cell cycle regulation provided by PIP box- and Cul4Cdt2-mediated destruction of E2f1 during S phase. Dev Cell 15: 890-900.
48. Sonoda J, Wharton RP. 1999. Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev 13: 2704-2712.
49. Sonoda J, Wharton RP. 2001. Drosophila Brain tumor is a trans-lational repressor. Genes Dev 15: 762-773.
50. Spassov DS, Jurecic R. 2002. Cloning and comparative sequence analysis of PUM1 and PUM2 genes, human members of the Pumilio family of RNA-binding proteins. Gene 299: 195-204.
51. Spassov DS, Jurecic R. 2003. Mouse Pum1 and Pum2 genes, members of the Pumilio family of RNA-binding proteins, show differential expression in fetal and adult hematopoietic stem cells and progenitors. Blood Cells Mol Dis 30: 55-69.
52. Sylvestre Y, De Guire V, Querido E, Mukhopadhyay UK, Bourdeau V, Major F, Ferbeyre G, Chartrand P. 2007. An E2F/miR-20a autoregulatory feedback loop. J Biol Chem 282: 2135-2143.
53. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, Buchholz R, Demsky M, Fawcett R, Francis-Lang HL, et al. 2004. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36: 283-287.
54. Tordai A, Wang J, Andre F, Liedtke C, Yan K, Sotiriou C, Hortobagyi GN, Symmans WF, Pusztai L. 2008. Evaluation of biological pathways involved in chemotherapy response in breast cancer. Breast Cancer Res 10: R37. doi: 10.1186/ bcr2088.
55. Tschöp K, Conery AR, Settleman J, Harlow E, Dyson N. 2011. A kinase shRNA screen links LATS2 and the pRb tumor suppressor pathway. Genes Dev 25: 814-830.
56. Veltman JA, Fridlyand J, Pejavar S, Olshen AB, Korkola JE, DeVries S, Carroll P, Kuo WL, Pinkel D, Albertson D, et al. 2003. Array-based comparative genomic hybridization for genome-wide screening of DNA copy number in bladder tumors. Cancer Res 63: 2872-2880.
57. Vessey JP, Schoderboeck L, Gingl E, Luzi E, Riefler J, Di Leva F, Karra D, Thomas S, Kiebler MA, Macchi P. 2010. Mammalian Pumilio 2 regulates dendrite morphogenesis and synap-tic function. Proc Natl Acad Sci 107: 3222-3227.