PTBP1 induces ADAR1 p110 isoform expression through IRES-like dependent translation control and influences cell proliferation in gliomas

Cellular and Molecular Life Sciences

Volumn 72, Issue 22, 2015, Pages 4383-4397

  Yang, Bin ^a,c   Hu, Peishan ^a   Lin, Xihua ^a   Han, Wei ^a   Zhu, Liyuan ^a   Tan, Xiaochao ^a   Ye, Fei ^a   Wang, Guanzhou ^a   Wu, Fan ^a   Yin, Bin ^a   Bao, Zhaoshi ^b   Jiang, Tao ^b   Yuan, Jiangang ^a   Qiang, Boqin ^a   Peng, Xiaozhong ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c FUWAI HOSPITAL   (China)

Author keywords

ADAR1; Cell proliferation; Gliomas; IRES like; PTBP1

Indexed keywords

ADENOSINE DEAMINASE; ADENOSINE DEAMINASE THAT ACT ON RNA P110; ADENOSINE DEAMINASE THAT ACT ON RNA P150; MESSENGER RNA; POLYPYRIMIDINE TRACT BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ADAR1 PROTEIN, HUMAN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; INTERNAL RIBOSOME ENTRY SITE; ISOENZYME; PROTEIN BINDING; PTBP1 PROTEIN, HUMAN; RNA BINDING PROTEIN;

ARTICLE; ASTROCYTE; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; DRUG TARGETING; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; GLIOMA; GLIOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERNAL RIBOSOME ENTRY SITE; PROTEIN INDUCTION; RNA INTERFERENCE; TRANSLATION REGULATION; UPREGULATION; BINDING SITE; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ADENOSINE DEAMINASE; BASE SEQUENCE; BINDING SITES; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HEK293 CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; INTERNAL RIBOSOME ENTRY SITES; ISOENZYMES; MOLECULAR SEQUENCE DATA; POLYPYRIMIDINE TRACT-BINDING PROTEIN; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84945452740     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-015-1938-7     Document Type: Article

References (52)

1. Sonenberg N, Hinnebusch AG (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136:731-745
2. Schepens B, Tinton SA, Bruynooghe Y, Beyaert R, Cornelis S (2005) The polypyrimidine tract-binding protein stimulates HIF-1alpha IRES-mediated translation during hypoxia. Nucleic Acids Res 33:6884-6894
3. Bushell M, Stoneley M, Kong YW, Hamilton TL, Spriggs KA, Dobbyn HC et al (2006) Polypyrimidine tract binding protein regulates IRES-mediated gene expression during apoptosis. Mol Cell 23:401-412
4. Rubsamen D, Blees JS, Schulz K, Doring C, Hansmann ML, Heide H et al (2012) IRES-dependent translation of egr2 is induced under inflammatory conditions. RNA 18:1910-1920
5. Blau L, Knirsh R, Ben-Dror I, Oren S, Kuphal S, Hau P et al (2012) Aberrant expression of c-Jun in glioblastoma by internal ribosome entry site (IRES)-mediated translational activation. Proc Natl Acad Sci USA 109:E2875-E2884
6. Grover R, Ray PS, Das S (2008) Polypyrimidine tract binding protein regulates IRES-mediated translation of p53 isoforms. Cell Cycle 7:2189-2198
7. Evans JR, Mitchell SA, Spriggs KA, Ostrowski J, Bomsztyk K, Ostarek D et al (2003) Members of the poly (rC) binding protein family stimulate the activity of the c-myc internal ribosome entry segment in vitro and in vivo. Oncogene 22:8012-8020
8. Schepens B, Tinton SA, Bruynooghe Y, Parthoens E, Haegman M, Beyaert R et al (2007) A role for hnRNP C1/C2 and Unr in internal initiation of translation during mitosis. EMBO J 26:158-169
9. Kim U, Wang Y, Sanford T, Zeng Y, Nishikura K (1994) Molecular cloning of cDNA for double-stranded RNA adenosine deaminase, a candidate enzyme for nuclear RNA editing. Proc Natl Acad Sci USA 91:11457-11461
10. Gerber A, O'Connell MA, Keller W (1997) Two forms of human double-stranded RNA-specific editase 1 (hRED1) generated by the insertion of an Alu cassette. RNA 3:453-463
11. Melcher T, Maas S, Herb A, Sprengel R, Higuchi M, Seeburg PH (1996) RED2, a brain-specific member of the RNA-specific adenosine deaminase family. J Biol Chem 271:31795-31798
12. Chen CX, Cho DS, Wang Q, Lai F, Carter KC, Nishikura K (2000) A third member of the RNA-specific adenosine deaminase gene family, ADAR3, contains both single- and double-stranded RNA binding domains. RNA 6:755-767
13. Patterson JB, Samuel CE (1995) Expression and regulation by interferon of a double-stranded-RNA-specific adenosine deaminase from human cells: evidence for two forms of the deaminase. Mol Cell Biol 15:5376-5388
14. Desterro JM, Keegan LP, Lafarga M, Berciano MT, O'Connell M, Carmo-Fonseca M (2003) Dynamic association of RNA-editing enzymes with the nucleolus. J Cell Sci 116:1805-1818
15. Ma CH, Chong JH, Guo Y, Zeng HM, Liu SY, Xu LL et al (2011) Abnormal expression of ADAR1 isoforms in Chinese pediatric acute leukemias. Biochem Biophys Res Commun 406:245-251
16. Steinman RA, Yang Q, Gasparetto M, Robinson LJ, Liu X, Lenzner DE et al (2013) Deletion of the RNA-editing enzyme ADAR1 causes regression of established chronic myelogenous leukemia in mice. Int J Cancer 132:1741-1750
17. Jiang Q, Crews LA, Barrett CL, Chun HJ, Court AC, Isquith JM et al (2013) ADAR1 promotes malignant progenitor reprogramming in chronic myeloid leukemia. Proc Natl Acad Sci USA 110:1041-1046
18. Cenci C, Barzotti R, Galeano F, Corbelli S, Rota R, Massimi L et al (2008) Down-regulation of RNA editing in pediatric astrocytomas: ADAR2 editing activity inhibits cell migration and proliferation. J Biol Chem 283:7251-7260
19. Galeano F, Rossetti C, Tomaselli S, Cifaldi L, Lezzerini M, Pezzullo M et al (2013) ADAR2-editing activity inhibits glioblastoma growth through the modulation of the CDC14B/Skp2/p21/p27 axis. Oncogene 32:998-1009
20. Maas S, Patt S, Schrey M, Rich A (2001) Underediting of glutamate receptor GluR-B mRNA in malignant gliomas. Proc Natl Acad Sci USA 98:14687-14692
21. Jayan GC, Casey JL (2002) Inhibition of hepatitis delta virus RNA editing by short inhibitory RNA-mediated knockdown of ADAR1 but not ADAR2 expression. J Virol 76:12399-12404
22. Zhang Y, Chao T, Li R, Liu W, Chen Y, Yan X et al (2008) MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3a. J Mol Med 87:43-51
23. George CX, Samuel CE (1999) Human RNA-specific adenosine deaminase ADAR1 transcripts possess alternative exon 1 structures that initiate from different promoters, one constitutively active and the other interferon inducible. Proc Natl Acad Sci USA 96:4621-4626
24. George CX, Samuel CE (1999) Characterization of the 5′-flanking region of the human RNA-specific adenosine deaminase ADAR1 gene and identification of an interferon-inducible ADAR1 promoter. Gene 229:203-213
25. Kawakubo K, Samuel CE (2000) Human RNA-specific adenosine deaminase (ADAR1) gene specifies transcripts that initiate from a constitutively active alternative promoter. Gene 258:165-172
26. Lykke-Andersen S, Pinol-Roma S, Kjems J (2007) Alternative splicing of the ADAR1 transcript in a region that functions either as a 5′-UTR or an ORF. RNA 13:1732-1744
27. Lo HW, Zhu H, Cao X, Aldrich A, Ali-Osman F (2009) A novel splice variant of GLI1 that promotes glioblastoma cell migration and invasion. Cancer Res 69:6790-6798
28. Cancer Genome Atlas Research Network (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061-1068
29. Steinman RA, Wang Q (2011) ADAR1 isoform involvement in embryonic lethality. Proc Nat Acad Sci USA 108:E199 (author reply E200)
30. Cornelis S, Tinton SA, Schepens B, Bruynooghe Y, Beyaert R (2005) UNR translation can be driven by an IRES element that is negatively regulated by polypyrimidine tract binding protein. Nucleic Acids Res 33:3095-3108
31. Boutsma E, Noback S, van Lohuizen M (2008) The Polycomb protein and E3 ubiquitin ligase Ring1B harbors an IRES in its highly conserved 5′ UTR. PLoS ONE 3:e2322
32. Allam H, Ali N (2010) Initiation factor eIF2-independent mode of c-Src mRNA translation occurs via an internal ribosome entry site. J Biol Chem 285:5713-5725
33. Mitchell SA, Spriggs KA, Bushell M, Evans JR, Stoneley M, Le Quesne JP et al (2005) Identification of a motif that mediates polypyrimidine tract-binding protein-dependent internal ribosome entry. Genes Dev 19:1556-1571
34. Spriggs KA, Cobbold LC, Ridley SH, Coldwell M, Bottley A, Bushell M et al (2009) The human insulin receptor mRNA contains a functional internal ribosome entry segment. Nucleic Acids Res 37:5881-5893
35. Lin JY, Li ML, Huang PN, Chien KY, Horng JT, Shih SR (2008) Heterogeneous nuclear ribonuclear protein K interacts with the enterovirus 71 5′ untranslated region and participates in virus replication. J Gen Virol 89:2540-2549
36. Cheung HC, Hai T, Zhu W, Baggerly KA, Tsavachidis S, Krahe R et al (2009) Splicing factors PTBP1 and PTBP2 promote proliferation and migration of glioma cell lines. Brain J Neurol 132:2277-2288
37. Paz N, Levanon EY, Amariglio N, Heimberger AB, Ram Z, Constantini S et al (2007) Altered adenosine-to-inosine RNA editing in human cancer. Genome Res 17:1586-1595
38. Choudhury Y, Tay FC, Lam DH, Sandanaraj E, Tang C, Ang BT et al (2012) Attenuated adenosine-to-inosine editing of microRNA-376a promotes invasiveness of glioblastoma cells. J Clin Invest 122:4059-4076
39. Dominissini D, Amariglio N, Rechavi G (2012) Micro-editing mistake translates into a devastating brain tumor. J Clin Invest 122:3842-3845
40. Lospitao E, Perez-Ferreiro CM, Gosalbez A, Alonso MA, Correas I (2008) An internal ribosome entry site element directs the synthesis of the 80 kDa isoforms of protein 4.1R. BMC Biol 6:51
41. Thompson SR (2012) So you want to know if your message has an IRES? Wiley Interdiscip Rev RNA 3:697-705
42. Maas S, Kawahara Y, Tamburro KM, Nishikura K (2006) A-to-I RNA editing and human disease. RNA Biol 3:1-9
43. Nishikura K (2006) Editor meets silencer: crosstalk between RNA editing and RNA interference. Nat Rev Mol Cell Biol 7:919-931
44. Gallo A, Galardi S (2008) A-to-I RNA editing and cancer: from pathology to basic science. RNA Biol 5:135-139
45. Galeano F, Tomaselli S, Locatelli F, Gallo A (2012) A-to-I RNA editing: the "ADAR" side of human cancer. Semin Cell Dev Biol 23:244-250
46. Chen L, Li Y, Lin CH, Chan TH, Chow RK, Song Y et al (2013) Recoding RNA editing of AZIN1 predisposes to hepatocellular carcinoma. Nat Med 19:209-216
47. Qin YR, Qiao JJ, Chan TH, Zhu YH, Li FF, Liu H et al (2014) Adenosine-to-inosine RNA editing mediated by ADARs in esophageal squamous cell carcinoma. Cancer Res 74:840-851
48. Ota H, Sakurai M, Gupta R, Valente L, Wulff BE, Ariyoshi K et al (2013) ADAR1 forms a complex with Dicer to promote microRNA processing and RNA-induced gene silencing. Cell 153:575-589
49. Wang Q, Miyakoda M, Yang W, Khillan J, Stachura DL, Weiss MJ et al (2004) Stress-induced apoptosis associated with null mutation of ADAR1 RNA editing deaminase gene. J Biol Chem 279:4952-4961
50. Hartner JC, Walkley CR, Lu J, Orkin SH (2008) ADAR1 is essential for the maintenance of hematopoiesis and suppression of interferon signaling. Nat Immunol 10:109-115
51. XuFeng R, Boyer MJ, Shen H, Li Y, Yu H, Gao Y et al (2009) ADAR1 is required for hematopoietic progenitor cell survival via RNA editing. Proc Natl Acad Sci USA 106:17763-17768
52. Sebastiani P, Montano M, Puca A, Solovieff N, Kojima T, Wang MC et al (2009) RNA editing genes associated with extreme old age in humans and with lifespan in C. elegans. PLoS One 4:e8210