2′,3′-cyclic nucleotide 3′-phosphodiesterase: A novel RNA-binding protein that inhibits protein synthesis

Journal of Neuroscience Research

Volumn 87, Issue 5, 2009, Pages 1069-1079

  Gravel, Michel ^a   Robert, Francis ^a   Kottis, Vicky ^a   Gallouzi, Imed Eddine ^a   Pelletier, Jerry ^a,b   Braun, Peter E ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

CNP; RNA binding; Translation repression

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; MESSENGER RNA; POLYADENYLATED RNA; TUBULIN; CYTIDINE 3',5' PHOSPHATE PHOSPHODIESTERASE; PHOSPHODIESTERASE; PROTEIN SYNTHESIS INHIBITOR; RNA BINDING PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; IN VITRO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; OLIGODENDROGLIA; PRECIPITATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN SYNTHESIS INHIBITION; RAT; RNA ISOLATION; TRANSLATION REGULATION; ANIMAL; AUTORADIOGRAPHY; CELL STRAIN COS1; CERCOPITHECUS; CLASSIFICATION; COMBINATORIAL CHEMISTRY; GENETICS; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN SYNTHESIS; RABBIT; WESTERN BLOTTING;

ANIMALS; AUTORADIOGRAPHY; BLOTTING, WESTERN; CERCOPITHECUS AETHIOPS; COS CELLS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MICE; OLIGODENDROGLIA; PHOSPHORIC DIESTER HYDROLASES; PROTEIN BIOSYNTHESIS; PROTEIN SYNTHESIS INHIBITORS; RABBITS; RATS; RNA, MESSENGER; RNA-BINDING PROTEINS; SELEX APTAMER TECHNIQUE; TUBULIN;

EID: 65949118902     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21939     Document Type: Article

References (61)

1. Agrawal HC, Sprinkle TJ, Agrawal D. 1990a. 2′,3′-Cyclic nucleotide-3′-phosphodiesterase in the central nervous system is fatty-acylated by thioester linkage. J Biol Chem 265:11849-11853.
2. Agrawal HC, Sprinkle TJ, Agrawal D. 1990b. 2′,3′-Cyclic nucleotide-3′-phosphodiesterase in peripheral nerve myelin is phosphorylated by a phorbol ester-sensitive protein kinase. Biochem Biophys Res Commun 170:817-823.
3. Agrawal HC, Sprinkle TJ, Agrawal D. 1994. In vivo phosphorylation of 2′,3′-cyclic nucleotide 3′-phosphohydrolase (CNP): CNP in brain myelin is phosphorylated by forskolin- and phorbol ester-sensitive protein kinases. Neurochem Res 19:721-728.
4. Bader AG, Vogt PK. 2008. Phosphorylation by Akt disables the antioncogenic activity of YB-1. Oncogene 27:1179-1182.
5. Ballestero RP, Wilmot GR, Leski ML, Uhler MD, Agranoff BW. 1995. Isolation of cDNA clones encoding RICH: a protein induced during goldfish optic nerve regeneration with homology to mammalian 2′,3′-cyclic -nucleotide 3′-phosphodiesterases. Proc Natl Acad Sci U S A 92:8621-8625.
6. Ballestero RP, Wilmot GR, Agranoff BW, Uhler MD. 1997. gRICH68 and gRICH70 are 2′,3′-cyclic-nucleotide 3′-phosphodiesterases induced during goldfish optic nerve regeneration. J Biol Chem 272:11479-11486.
7. Ballestero RP, Dybowski JA, Levy G, Agranoff BW, Uhler MD. 1999. Cloning and characterization of zRICH, a 2′,3′-cyclic-nucleotide 3′-phosphodiesterase induced during zebrafish optic nerve regeneration. J Neurochem 72:1362-1371.
8. Bernier L, Alvarez F, Norgard EM, Raible DW, Mentaberry A, Schembri JG, Sabatini DD, Colman DR. 1987. Molecular cloning of a 2′,3′-cyclic nucleotide 3′-phosphodiesterase: mRNAs with different 5′ ends encode the same set of proteins in nervous and lymphoid tissues. J Neurosci 7:2703-2710.
9. Bifulco M, Laezza C, Stingo S, Wolff J. 2002. 2′,3′-Cyclic nucleotide 3′-phosphodiesterase: a membrane-bound, microtubule-associated protein and membrane anchor for tubulin. Proc Natl Acad Sci U S A 99:1807-1812.
10. Bostwick DG. 1992. Prostatic intraepithelial neoplasia (PIN): current concepts. J Cell Biochem Suppl 10-19.
11. Bouvet P, Matsumoto K, Wolffe AP. 1995. Sequence-specific RNA recognition by the Xenopus Y-box proteins. An essential role for the cold shock domain. J Biol Chem 270:28297-28303.
12. Braun PE, De Angelis D, Shtybel WW, Bernier L. 1991. Isoprenoid modification permits 2′,3′-cyclic nucleotide 3′-phosphodiesterase to bind to membranes. J Neurosci Res 30:540-544.
13. Braun PE, Lee J, Gravel M. 2004. 2′-3′-Cyclic nucleotide 3′-phosphodiesterase: structure, biology and function. In: Myelin biology and disorders, volume I; Lazzarini RA, editor. San Diego: Elsevier. p 499-522.
14. Buckanovich RJ, Darnell RB. 1997. The neuronal RNA binding protein Nova-1 recognizes specific RNA targets in vitro and in vivo. Mol Cell Biol 17:3194-3201.
15. Carson JH, Barbarese E. 2005. Systems analysis of RNA trafficking in neural cells. Biol Cell 97:51-62.
16. Culver GM, Consaul SA, Tycowski KT, Filipowicz W, Phizicky EM. 1994. tRNA splicing in yeast and wheat germ. A cyclic phosphodiesterase implicated in the metabolism of ADP-ribose 1′,2′-cyclic phosphate. J Biol Chem 269:24928-24934.
17. Darnell JC, Jensen KB, Jin P, Brown V, Warren ST, Darnell RB. 2001. Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107:489-499.
18. Davydova EK, Evdokimova VM, Ovchinnikov LP, Hershey JW. 1997. Overexpression in COS cells of p50, the major core protein associated with mRNA, results in translation inhibition. Nucleic Acids Res 25:2911-2916.
19. Drummond RJ, Dean G. 1980. Comparison of 2′,3′-cyclic nucleotide 3′-phosphodiesterase and the major component of Wolfgram protein W1. J Neurochem 35:1155-1165.
20. Ellington AD, Szostak JW. 1990. In vitro selection of RNA molecules that bind specific ligands. Nature 346:818-822.
21. Entelis NS, Kolesnikova OA, Martin RP, Tarassov IA. 2001. RNA delivery into mitochondria. Adv Drug Deliv Rev 49:199-215.
22. Evdokimova V, Ruzanov P, Imataka H, Raught B, Svitkin Y, Ovchinnikov LP, Sonenberg N. 2001. The major mRNA-associated protein YB-1 is a potent 5′ cap-dependent mRNA stabilizer. EMBO J 20:5491-5502.
23. Evdokimova V, Ovchinnikov LP, Sorensen PH. 2006a. Y-box binding protein 1: providing a new angle on translational regulation. Cell Cycle 5:1143-1147.
24. Evdokimova V, Ruzanov P, Anglesio MS, Sorokin AV, Ovchinnikov LP, Buckley J, Triche TJ, Sonenberg N, Sorensen PH. 2006b. Aktmediated YB-1 phosphorylation activates translation of silent mRNA species. Mol Cell Biol 26:277-292.
25. Gallouzi IE, Brennan CM, Stenberg MG, Swanson MS, Eversole A, Maizels N, Steitz JA. 2000. HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc Natl Acad Sci U S A 97:3073-3078.
26. Genschik P, Hall J, Filipowicz W. 1997. Cloning and characterization of the Arabidopsis cyclic phosphodiesterase which hydrolyzes ADP-ribose 1′,2′-cyclic phosphate and nucleoside 2′,3′-cyclic phosphates. J Biol Chem 272:13211-13219.
27. Gravel M, DeAngelis D, Braun PE. 1994. Molecular cloning and characterization of rat brain 2′,3′-cyclic nucleotide 3′-phosphodiesterase isoform 2. J Neurosci Res 38:243-247.
28. Heaton PA, Eckstein F. 1996. Diastereomeric specificity of 2′,3′-cyclic nucleotide 3′-phosphodiesterase. Nucleic Acids Res 24:850-853.
29. Hofmann A, Zdanov A, Genschik P, Ruvinov S, Filipowicz W, Wlodawer A. 2000. Structure and mechanism of activity of the cyclic phosphodiesterase of Appr>p, a product of the tRNA splicing reaction. EMBO J 19:6207-6217.
30. Hofmann A, Tarasov S, Grella M, Ruvinov S, Nasr F, Filipowicz W, Wlodawer A. 2002. Biophysical characterization of cyclic nucleotide phosphodiesterases. Biochem Biophys Res Commun 291:875-883.
31. Izumi H, Imamura T, Nagatani G, Ise T, Murakami T, Uramoto H, Torigoe T, Ishiguchi H, Yoshida Y, Nomoto M, Okamoto T, Uchiumi T, Kuwano M, Funa K, Kohno K. 2001. Y box-binding protein-1 binds preferentially to single-stranded nucleic acids and exhibits 3′→5′ exonuclease activity. Nucleic Acids Res 29:1200-1207.
32. Jansen RP. 1999. RNA-cytoskeleton associations. FASEB J 13:455-466. Kato M, Shirouzu M, Terada T, Yamaguchi H, Murayama K, Sakai H, Kuramitsu S, Yokoyama S. 2003. Crystal structure of the 2′-5′ RNA ligase from Thermus thermophilus HB8. J Mol Biol 329:903-911.
33. Kosturko LD, Maggipinto MJ, D'Sa C, Carson JH, Barbarese E. 2005. The microtubule-associated protein tumor overexpressed gene binds to the RNA trafficking protein heterogeneous nuclear ribonucleoprotein A2. Mol Biol Cell 16:1938-1947.
34. Kozlov G, Lee J, Elias D, Gravel M, Gutierrez P, Ekiel I, Braun PE, Gehring K. 2003. Structural evidence that brain cyclic nucleotide phosphodiesterase is a member of the 2H phosphodiesterase superfamily. J Biol Chem 278:46021-46028.
35. Kozlov G, Denisov AY, Pomerantseva E, Gravel M, Braun PE, Gehring K. 2007. Solution structure of the catalytic domain of RICH protein from goldfish. FEBS J 274:1600-1609.
36. Lee J, Gravel M, Gao E, O'Neill RC, Braun PE. 2001. Identification of essential residues in 2′,3′-cyclic nucleotide 3′-phosphodiesterase. Chemical modification and site-directed mutagenesis to investigate the role of cysteine and histidine residues in enzymatic activity. J Biol Chem 276:14804-14813.
37. Lee J, Gravel M, Zhang R, Thibault P, Braun PE. 2005. Process out-growth in oligodendrocytes is mediated by CNP, a novel microtubule assembly myelin protein. J Cell Biol 170:661-673.
38. Lee J, O'Neill RC, Park MW, Gravel M, Braun PE. 2006. Mitochondrial localization of CNP2 is regulated by phosphorylation of the N-terminal targeting signal by PKC: implications of a mitochondrial function for CNP2 in glial and non-glial cells. Mol Cell Neurosci 31:446-462.
39. Lin Q, Taylor SJ, Shalloway D. 1997. Specificity and determinants of Sam68 RNA binding. Implications for the biological function of K homology domains. J Biol Chem 272:27274-27280.
40. Mazumder R, Iyer LM, Vasudevan S, Aravind L. 2002. Detection of novel members, structure-function analysis and evolutionary classification of the 2H phosphoesterase superfamily. Nucleic Acids Res 30: 5229-5243.
41. Minich WB, Ovchinnikov LP. 1992. Role of cytoplasmic mRNP proteins in translation. Biochimie 74:477-483.
42. Minich WB, Maidebura IP, Ovchinnikov LP. 1993. Purification and characterization of the major 50-kDa repressor protein from cytoplasmic mRNP of rabbit reticulocytes. Eur J Biochem 212:633-638.
43. Novac O, Guenier AS, Pelletier J. 2004. Inhibitors of protein synthesis identified by a high throughput multiplexed translation screen. Nucleic Acids Res 32:902-915.
44. O'Neill RC, Braun PE. 2000. Selective synthesis of 2′,3′-cyclic nucleotide 3′-phosphodiesterase isoform 2 and identification of specifically phosphorylated serine residues. J Neurochem 74:540-546.
45. O'Neill RC, Minuk J, Cox ME, Braun PE, Gravel M. 1997. CNP2 mRNA directs synthesis of both CNP1 and CNP2 polypeptides. J Neurosci Res 50:248-257.
46. Pestova TV, Hellen CU. 2003. Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes Dev 17:181-186.
47. Phizicky EM, Schwartz RC, Abelson J. 1986. Saccharomyces cerevisiae tRNA ligase. Purification of the protein and isolation of the structural gene. J Biol Chem 261:2978-2986.
48. Pick L, Furneaux H, Hurwitz J. 1986. Purification of wheat germ RNA ligase. II. Mechanism of action of wheat germ RNA ligase. J Biol Chem 261:6694-6704.
49. Richter-Landsberg C, Heinrich M. 1996. OLN-93: a new permanent oligodendroglia cell line derived from primary rat brain glial cultures. J Neurosci Res 45:161-173.
50. Sambrook J, Russell DW. 2001. Molecular cloning. a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
51. Sawaya R, Schwer B, Shuman S. 2003. Genetic and biochemical analysis of the functional domains of yeast tRNA ligase. J Biol Chem 278: 43928-43938.
52. Scherer SS, Braun PE, Grinspan J, Collarini E, Wang DY, Kamholz J. 1994. Differential regulation of the 2′,3′-cyclic nucleotide 3′-phosphodiesterase gene during oligodendrocyte development. Neuron 12:1363-1375.
53. Schwer B, Aronova A, Ramirez A, Braun P, Shuman S. 2008. Mammalian 2′,3′ cyclic nucleotide phosphodiesterase (CNP) can function as a tRNA splicing enzyme in vivo. RNA 14:204-210.
54. Siomi H, Choi M, Siomi MC, Nussbaum RL, Dreyfuss G. 1994. Essential role for KH domains in RNA binding: impaired RNA binding by a mutation in the KH domain of FMR1 that causes fragile X syndrome. Cell 77:33-39.
55. Sprinkle TJ. 1989. 2′,3′-Cyclic nucleotide 3′-phosphodiesterase, an oligodendrocyte -Schwann cell and myelin-associated enzyme of the nervous system. Crit Rev Neurobiol 4:235-301.
56. Stingo S, Masullo M, Polverini E, Laezza C, Ruggiero I, Arcone R, Ruozi E, Dal Piaz F, Malfitano AM, D'Ursi AM, Bifulco M. 2007. The N-terminal domain of 2′,3′-cyclic nucleotide 3′-phosphodiesterase harbors a GTP/ATP binding site. Chem Biol Drug Des 70:502-510.
57. Swanson MS, Dreyfuss G. 1988. RNA binding specificity of hnRNP proteins: a subset bind to the 3′ end of introns. EMBO J 7:3519-3529.
58. Trapp BD, Bernier L, Andrews SB, Colman DR. 1988. Cellular and subcellular distribution of 2′, 3′-cyclic nucleotide 3′-phosphodiesterase and its mRNA in the rat nervous system. J Neurocehm 51:859-868.
59. Tsukada Y, Kurihara T. 1992. 2′,3′-cyclic nucleotide 3′-phosphodiesterase: molecular characterization and possible functional significance. In: Myelin: Biology and Chemistry; Martenson RE, editor. Boca Raton, FL: CRC Press. p 449-480.
60. Tuerk C, Gold L. 1990. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249:505-510.
61. Tyc K, Kellenberger C, Filipowicz W. 1987. Purification and characterization of wheat germ 2′,3′-cyclic nucleotide 3′-phosphodiesterase. J Biol Chem 262:12994-13000.