IRES-mediated translation of the carboxy-terminal domain of the horizontal cell specific connexin Cx55.5 in vivo and in vitro

BMC Molecular Biology

Volumn 9, Issue , 2008, Pages

  Ul Hussain, Mahboob ^a   Zoidl, Georg ^a   Klooster, Jan ^b   Kamermans, Maarten ^b,c   Dermietzel, Rolf ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 55.5; GAP JUNCTION PROTEIN; ISOPROTEIN; LUCIFERASE;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CODON; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTERNAL RIBOSOME ENTRY SITE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA HORIZONTAL NERVE CELL; RNA TRANSLATION; SIGNAL TRANSDUCTION; SYNAPSE; TRANSLATION INITIATION; ZEBRA FISH; ANIMAL; CELL STRAIN 3T3; CHEMISTRY; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; HELA CELL; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBOSOME; TUMOR CELL LINE; ULTRASTRUCTURE; WESTERN BLOTTING;

DANIO RERIO;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL NUCLEUS; CONNEXINS; HELA CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; LUCIFERASES; MICE; MICROSCOPY, IMMUNOELECTRON; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; PROMOTER REGIONS (GENETICS); PROTEIN BIOSYNTHESIS; PROTEIN ISOFORMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMES; TRANSCRIPTION, GENETIC; TRANSFECTION; ZEBRAFISH;

EID: 46049087514     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-9-52     Document Type: Article

References (49)

1. Huang RP Fan Y Hossain MZ Peng A Zeng ZL Boynton AL Reversion of the neoplastic phenotype of human glioblastoma cells by connexin 43 (cx43) Cancer Res 1998, 58:5089-5096 9823317
2. Olbina G Eckhart W Mutations in the second extra cellular region of connexin 43 prevent localization to the plasma membrane, but do not affect its ability to suppress cell growth Mol Cancer Res 2003, 1:690-700 12861055
3. Omori Y Yamasaki H Mutated connexin43 proteins inhibit rat glioma cell growth suppression mediated by wild-type connexin43 in a dominant-negative manner Int J Cancer 1998, 78:446-453 10.1002/ (SICI)1097-0215(19981109)78:4<446::AID-IJC10>3.0.CO;2-4 9797133
4. Cusato K Bosco A Rozental R Guimaraes CA Reese BE Linden R Spray DC Gap junctions mediate bystander cell death in developing retina J Neurosci 2003, 23:6413-6422 12878681
5. Zhang YW Kaneda M Morita I The gap junction-independent tumor-suppressing effect of connexin 43 J Biol Chem 2003, 278:44852-44856 10.1074/jbc.M305072200 12952975
6. Lin JH Yang J Liu S Takano T Wang X Gao Q Willecke K Nedergaard M Connexin mediates gap junction-independent resistance to cellular injury J Neurosci 2003, 23:430-441 12533603
7. Moorby C Patel M Dual functions for connexins: Cx43 regulates growth independently of gap junction formation Exp Cell Res 2001, 271:238-248 10.1006/excr.2001.5357 11716536
8. Qin H Shao Q Curtis H Galipeau J Belliveau DJ Wang T Alaoui-Jamali MA Laird DW Retroviral delivery of connexin genes to human breast tumor cells inhibits in vivo tumor growth by a mechanism that is independent of significant gap junctional intercellular communication J Biol Chem 2002, 277:29132-29138 10.1074/jbc.M200797200 12042301
9. Deisseroth K Bito H Tsien RW Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity Neuron 1996, 16:89-101 10.1016/S0896-6273(00)80026-4 8562094
10. Deisseroth K Mermelsteiny PG Xiaz H Tsienz RW Signaling from synapse to nucleus: The logic behind the mechanisms Currt Opin Neurobiol 2003, 13:354-365 10.1016/S0959-4388(03)00076-X
11. West AE Griffith EC Greenberg ME Regulation of transcription factors by neuronal activity Nat Rev Neurosci 2002, 3:921-931 10.1038/nrn987 12461549
12. Shields CR Klooster J Claassen Y Hussain MU Zoidl G Dermietzel R Kamermans M Retinal horizontal cell-specific promoter activity and protein expression of zebrafish connexin 52.6 and connexin 55.5 J Comp Neurol 2007, 501:765-779 10.1002/cne.21282 17299759
13. Montague PR Transforming sensory experience into structural change Proc Natl Acad Sci USA 1993, 90:6379-6380 46934 8393565 10.1073/ pnas.90.14.6379
14. Weiler R Wagner HJ Light-dependent change of cone-horizontal cell interactions in carp Brain Res 1984, 298:1-9 10.1016/ 0006-8993(84)91141-7 6326947
15. Weiler R Schultz K Pottek M Tieding S Janssen-Bienhold U Retinoic acid has light-adaptive effects on horizontal cells in the retina Proc Natl Acad Sci USA 1998, 95:7139-7144 22767 9618552 10.1073/pnas.95.12.7139
16. Söhl G Willecke K An update on connexin genes and their nomenclature in mouse and man Cell Commun Adhes 2003, 10:173-180 10.1080/ 714040423 14681012
17. Dermietzel R Kremer M Paputsoglu G Stang A Skerrett IM Gomes D Srinivas M Janssen-Bienhold U Weiler R Nicholson BJ Bruzzone R Spray DC Molecular and functional diversity of neural connexins in the retina J Neurosci 2000, 20:8331-8343 11069940
18. Zoidl G Bruzzone R Weickert S Kremer M Zoidl C Mitropoulou G Srinivas M Spray DC Dermietzel R Molecular cloning and functional expression of zfCx52.6: A novel connexin with hemichannel-forming properties expressed in horizontal cells of the zebrafish retina J Biol Chem 2004, 279:2913-2921 10.1074/jbc.M304850200 14583621
19. Milks LC Kumar NM Houghten R Unwin N Gilula NB Topology of the 32-kd liver gap junction protein determined by site-directed antibody localizations EMBO J 1988, 7:2967-2975 454678 2460334
20. Gellhaus A Dong X Propson S Maass K Klein-Hitpass L Kibschull M Traub O Willecke K Perbal B Lye SJ Winterhager E Connexin43 interacts with NOV: a possible mechanism for negative regulation of cell growth in choriocarcinoma cells J Biol Chem 2004, 279:36931-36942 10.1074/ jbc.M404073200 15181016
21. Fu CT Bechberger JF Ozog MA Perbal B Naus CC CCN3 (NOV) interacts with connexin43 in C6 glioma cells: Possible mechanism of connexin-mediated growth suppression J Biol Chem 2004, 279:36943-36950 10.1074/ jbc.M403952200 15213231
22. Dang X Doble BW Kardami E The carboxy-tail of connexin-43 localizes to the nucleus and inhibits cell growth Mol Cell Biochem 2003, 242:35-38 10.1023/A:1021152709313 12619863
23. Hussain MU Kremer M Zoidl G Dermietzel R Transcriptional and translational regulation of zebrafish connexin 55.5 (zf.Cx.55.5) and connexin 52.6 (zf.Cx52.6) Cell Commun Adhes 2003, 10:227-231 10.1080/ 714040432 14681021
24. Schiavi A Hudder A Werner R Connexin43 mRNA contains a functional internal ribosome entry site FEBS Lett 1999, 464:118-122 10.1016/ S0014-5793(99)01699-3 10618489
25. Hudder A Werner R Analysis of a Charcot-Marie-Tooth disease mutation reveals an essential internal ribosome entry site element in the connexin-32 gene J Biol Chem 2000, 275:34586-34591 10.1074/ jbc.M005199200 10931843
26. Lahlou H Fanjul M Pradayrol L Susini C Pyronnet S Restoration of functional gap junctions through internal ribosome entry site-dependent synthesis of endogenous connexins in density-inhibited cancer Mol Cell Biol 2005, 25:4034-4045 1087721 15870276 10.1128/MCB.25.10.4034-4045.2005
27. Meijer HA Dictus WJ Keuning ED Thomas AA Translational control of the xenopus laevis connexin-41 5′-untranslated region by three upstream open reading frames J Biol Chem 2000, 275:30787-30793 10.1074/ jbc.M005531200 10896676
28. Chubet RG Brizzard BL Vectors for expression and secretion of FLAG epitope-tagged proteins in mammalian cells Biotechniques 1996, 20:136-141 8770418
29. Deepak S Gek HC Kuo-Bin L Francis T Krishnan A pSLIP or: SVM based Protein Subcellular Localization Prediction using Multiple Physicochemical Properties BMC Bioinformatics 2005, 6:152 1182350 15963230 10.1186/1471-2105-6-152
30. Bhasin M Raghava GPS ESLpred: SVM Based Method for Subcellular Localization of Eukaryotic Proteins using Dipeptide Composition and PSI-BLAST Nucleic Acids Research 2004, 32:414-419 10.1093/nar/gkh350
31. Wang Z Weaver M Magnuson NS Cryptic promoter activity in the DNA sequence corresponding to the pim-1 5'-UTR Nucleic Acids Res 2005, 33:2248-2258 1083428 15843687 10.1093/nar/gki523
32. Pyronnet S Pradayrol L Sonenberg N Alternative splicing facilitates internal ribosome entry on the ornithine decarboxylase mRNA Cell Mol Life Sci 2005, 61:1267-1274 10.1007/s00018-005-5020-8
33. Yang Q Sarnow P Location of the internal ribosome entry site in the 5′ non-coding region of the immunoglobulin heavy-chain binding protein (BiP) mRNA: Evidence for specific RNA-protein interactions Nucleic Acids Res 1997, 25:2800-2807 146825 9207027 10.1093/nar/ 25.14.2800
34. Nanbru C Lafon I Audigier S Gensac MC Vagner S Huez G Prats AC Alternative translation of the proto-oncogene c-myc by an internal ribosome entry site J Biol Chem 1997, 272:32061-32066 10.1074/ jbc.272.51.32061 9405401
35. Huez I Creancier L Audigier S Gensac MC Prats AC Prats H Two independent internal ribosome entry sites are involved in translation initiation of vascular endothelial growth factor mRNA Mol Cell Biol 1998, 18:6178-6190 109205 9774635
36. Oumard A Hennecke M Hauser H Nourbakhsh M Translation of NRF mRNA is mediated by highly efficient internal ribosome entry Mol Cell Biol 2000, 20:2755-2759 85491 10733578 10.1128/MCB.20.8.2755-2759.2000
37. Shiroki K Ohsawa C Sugi N Wakiyama M Miura K Watanabe M Suzuki Y Sugano S Internal ribosome entry site-mediated translation of Smad5 in vivo: requirement for a nuclear event Nucleic Acids Res 2002, 30:2851-2861 117063 12087169 10.1093/nar/gkf408
38. Hellen CU Sarnow P Internal ribosome entry sites in eukaryotic mRNA molecules Genes Dev 2002, 15:1593-1612 10.1101/gad.891101
39. Cornelis S Bruynooghe Y Denecker G Van Huffel S Tinton S Beyaert R Identification and characterization of a novel cell cycle-regulated internal ribosome entry site Mol Cell 2000, 5:597-605 10.1016/ S1097-2765(00)80239-7 10882096
40. Maier D Nagel AC Preiss A Two isoforms of the Notch antagonist hairless are produced by differential translation initiation Proc Natl Acad Sci USA 2002, 99:15480-15485 137742 12422020 10.1073/pnas.242596699
41. Lauring AS Overbaugh J Evidence that an IRES within the Notch2 coding region can direct expression of a nuclear form of the protein Mol Cell 2000, 6:939-945 10.1016/S1097-2765(05)00084-5 11090631
42. Weiler R Schultz K Janssen-Bienhold U Retraction of spinule-type neurites from carp retinal horizontal cell dendrites during dark adaptation involves the activation of Ca2+/calmodulin-dependent protein kinase II Eur J Neurosci 1995, 7:1914-1919 10.1111/ j.1460-9568.1995.tb00713.x 8528466
43. Brandon C Lam DM The ultrastructure of rat rod synaptic terminals: Effects of dark-adaptation J Comp Neurol 1983, 217:167-175 10.1002/ cne.902170205 6886050
44. Wagner HJ Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas J Neurocytol 1980, 9:573-590 10.1007/BF01205026 7441304
45. Ma S Liu G Sun Y Xie J Relocalization of the polypyrimidine tract-binding protein during PKA-induced neurite growth Biochim Biophys Acta 2007, 1773:912-923 10.1016/j.bbamcr.2007.02.006 17400307
46. Marchler-Bauer A Anderson JB DeWeese-Scott C Fedorova ND Geer LY He S Hurwitz DI Jackson JD Jacobs AR Lanczycki CJ Liebert CA Liu C Madej T Marchler GH Mazumder R Nikolskaya AN Panchenko AR Rao BS Shoemaker BA Simonyan V Song JS Thiessen PA Vasudevan S Wang Y Yamashita RA Yin JJ Bryant SH CDD: A curated entrez database of conserved domain alignments Nucleic Acids Res 2003, 31:383-387 165534 12520028 10.1093/nar/gkg087
47. Billiard J Umayahara Y Wiren K Centrella M McCarthy TL Rotwein P Regulated nuclear-cytoplasmic localization of CCAAT/enhancer-binding protein delta in osteoblasts J Biol Chem 2001, 276:15354-15361 10.1074/ jbc.M009973200 11278589
48. Sheng T Chi S Zhang X Xie J Regulation of Gli1 localization by the cAMP/ protein kinase A signaling axis through a site near the nuclear localization signal J Biol Chem 2006, 281:9-12 10.1074/jbc.C500300200 16293631
49. Zoidl G Meier C Petrasch-Parwez E Zoidl C Habbes HW Kremer M Srinivas M Spray DC Dermietzel R Evidence for a role of the N-terminal domain in subcellular localization of the neuronal connexin36 (Cx36) J Neurosci Res 2002, 69:448-465 10.1002/jnr.10284 12210839