Polyadenylation site-specific differences in the activity of the neuronal βCstF-64 protein in PC-12 cells

Gene

Volumn 529, Issue 2, 2013, Pages 220-227

  Shankarling, Ganesh S ^a,b   MacDonald, Clinton C ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

adducin; Alternative polyadenylation; Alternative splicing; CstF 64; Neuronal gene expression

Indexed keywords

ADDUCIN; LUCIFERASE; MESSENGER RNA; NERVE GROWTH FACTOR;

ANIMAL CELL; ARTICLE; BRAIN; CELL DIFFERENTIATION; CELL STIMULATION; CONTROLLED STUDY; GENE; GENE EXPRESSION; MOUSE; NERVE CELL; NONHUMAN; PC12 CELL; PHENOTYPE; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPLEEN;

Β-ADDUCIN; ΒCSTF-64; 3′ RACE; 3′ RAPID AMPLIFICATION OF CDNA ENDS; ADD2; ALTERNATIVE POLYADENYLATION; ALTERNATIVE SPLICING; BRAIN-SPECIFIC SPLICE VARIANT OF CSTF-64; CLEAVAGE STIMULATION FACTOR; CLEAVAGE STIMULATION FACTOR, 64,000 M(R) SUBUNIT; CLEAVAGE STIMULATION FACTOR, 77,000 M(R) SUBUNIT; CSTF; CSTF-64; CSTF-77; CSTF2; CSTF2T; DMEM; DOWNSTREAM SEQUENCE ELEMENT; DSE; DULBECCO'S MINIMAL EAGLE MEDIA; HUMAN GENE ENCODING ΤCSTF-64; HUMAN GENE ENCODING CSTF-64; MOUSE GENE ENCODING Β-ADDUCIN; MOUSE OR RAT GENE ENCODING CSTF-64; N-CAM; NERVE GROWTH FACTOR; NESTED GENE-SPECIFIC PRIMER; NEURAL CELL ADHESION MOLECULE; NEUROFIBROMATOSIS TYPE 1; NEURONAL GENE EXPRESSION; NF1; NGF; NGSP; RELATIVE LUCIFERASE UNIT; REVERSE TRANSCRIPTASE-MEDIATED POLYMERASE CHAIN REACTION; RLU; RT-PCR; SLAP; STEM-LOOP LUCIFERASE ASSAY FOR POLYADENYLATION;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CLEAVAGE STIMULATION FACTOR; MICE; NERVE GROWTH FACTOR; NEURONS; PC12 CELLS; POLYADENYLATION; PROTEIN ISOFORMS; RATS; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 84883775020     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2013.08.007     Document Type: Article

References (48)

1. An J.J., Gharami K., Liao G.Y., Woo N.H., Lau A.G., et al. Distinct role of long 3' UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 2008, 134:175-187.
2. Anthony K., Gallo J.M. Aberrant RNA processing events in neurological disorders. Brain Res. 2010, 1338:67-77.
3. Barker P.A., Lomen-Hoerth C., Gensch E.M., Meakin S.O., Glass D.J., et al. Tissue-specific alternative splicing generates two isoforms of the trkA receptor. J. Biol. Chem. 1993, 268:15150-15157.
4. Chan S., Choi E.-A., Shi Y. Pre-mRNA 3'-end processing complex assembly and function. WIREs RNA 2010, 2:321-335.
5. Costessi L., Devescovi G., Baralle F.E., Muro A.F. Brain-specific promoter and polyadenylation sites of the beta-adducin pre-mRNA generate an unusually long 3'-UTR. Nucleic Acids Res. 2006, 34:243-253.
6. Costessi L., Porro F., Iaconcig A., Nedeljkovic M., Muro A.F. Characterization of the distal polyadenylation site of the ss-adducin (Add2) pre-mRNA. PLoS One 2013, 8:e58879.
7. Dass B., Tardif S., Park J.Y., Tian B., Weitlauf H.M., et al. Loss of polyadenylation protein τCstF-64 causes spermatogenic defects and male infertility. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:20374-20379.
8. de Sauvage F., Kruys V., Marinx O., Huez G., Octave J.N. Alternative polyadenylation of the amyloid protein precursor mRNA regulates translation. EMBO J. 1992, 11:3099-3103.
9. Di Giammartino D.C., Nishida K., Manley J.L. Mechanisms and consequences of alternative polyadenylation. Mol. Cell 2011, 43:853-866.
10. Flavell S.W., Kim T.K., Gray J.M., Harmin D.A., Hemberg M., et al. Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 2008, 60:1022-1038.
11. Fukumitsu H., Soumiya H., Furukawa S. Knockdown of pre-mRNA cleavage factor Im 25kDa promotes neurite outgrowth. Biochem. Biophys. Res. Commun. 2012, 425:848-853.
12. Ghosh T., Soni K., Scaria V., Halimani M., Bhattacharjee C., et al. MicroRNA-mediated up-regulation of an alternatively polyadenylated variant of the mouse cytoplasmic β-actin gene. Nucleic Acids Res. 2008, 36:6318-6332.
13. Greene L.A., Tischler A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. U. S. A. 1976, 73:2424-2428.
14. Hockert J.A., MacDonald C.C. The stem-loop luciferase assay for polyadenylation (SLAP) method for determining CstF-64-dependent polyadenylation activity. Polyadenylation: Methods and Protocols 2013, Humana Press. J. Rorbach, A. Bobrowicz (Eds.).
15. Hockert J.A., Yeh H.J., MacDonald C.C. The hinge domain of the cleavage stimulation factor protein CstF-64 is essential for CstF-77 interaction, nuclear localization, and polyadenylation. J. Biol. Chem. 2010, 285:695-704.
16. Hockert K.J., Martincic K., Mendis-Handagama S.M.L.C., Borghesi L.A., Milcarek C., et al. Spermatogenetic but not immunological defects in mice lacking the τCstF-64 polyadenylation protein. J. Reprod. Immunol. 2011, 89:26-37.
17. Hu X., Bi J., Loh H.H., Wei L.N. Regulation of mouse kappa opioid receptor gene expression by different 3'-untranslated regions and the effect of retinoic acid. Mol. Pharmacol. 2002, 62:881-887.
18. Huber Z., Monarez R.R., Dass B., MacDonald C.C. The mRNA encoding τCstF-64 is expressed ubiquitously in mouse tissues. Ann. N. Y. Acad. Sci. 2005, 1061:163-172.
19. Kyburz A., Friedlein A., Langen H., Keller W. Direct interactions between subunits of CPSF and the U2 snRNP contribute to the coupling of pre-mRNA 3' end processing and splicing. Mol. Cell 2006, 23:195-205.
20. Li Q., Lee J.A., Black D.L. Neuronal regulation of alternative pre-mRNA splicing. Nat. Rev. Neurosci. 2007, 8:819-831.
21. Li W., Yeh H.J., Shankarling G.S., Ji Z., Tian B., et al. The τCstF-64 polyadenylation protein controls genome expression in testis. PLoS One 2012, 7:e48373.
22. Licatalosi D.D., Mele A., Fak J.J., Ule J., Kayikci M., et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 2008, 456:464-469.
23. Lipscombe D. Neuronal proteins custom designed by alternative splicing. Curr. Opin. Neurobiol. 2005, 15:358-363.
24. Lutz C.S., Moreira A. Alternative mRNA polyadenylation in eukaryotes: an effective regulator of gene expression. WIREs RNA 2011, 2:23-31.
25. MacDonald C.C., McMahon K.W. Tissue-specific mechanisms of alternative polyadenylation: testis, brain and beyond. WIREs RNA 2010, 1:494-501.
26. Mandel C.R., Bai Y., Tong L. Protein factors in pre-mRNA 3'-end processing. Cell. Mol. Life Sci. 2008, 65:1099-1122.
27. Matsuoka Y., Li X., Bennett V. Adducin: structure, function and regulation. Cell. Mol. Life Sci. 2000, 57:884-895.
28. McMahon K.W., Hirsch B.A., MacDonald C.C. Differences in polyadenylation site choice between somatic and male germ cells. BMC Mol. Biol. 2006, 7:35.
29. Metheny L.J., Skuse G.R. NF1 mRNA isoform expression in PC12 cells: modulation by extrinsic factors. Exp. Cell Res. 1996, 228:44-49.
30. Millevoi S., Vagner S. Molecular mechanisms of eukaryotic pre-mRNA 3' end processing regulation. Nucleic Acids Res. 2010, 38:2757-2774.
31. Miura P., Shenker S., Andreu-Agullo C., Westholm J.O., Lai E.C. Widespread and extensive lengthening of 3' UTRs in the mammalian brain. Genome Res. 2013, 23:812-825.
32. Niwa M., MacDonald C.C., Berget S.M. Are vertebrate exons scanned during splice-site selection?. Nature 1992, 360:277-280.
33. Ozsolak F., Kapranov P., Foissac S., Kim S.W., Fishilevich E., et al. Comprehensive polyadenylation site maps in yeast and human reveal pervasive alternative polyadenylation. Cell 2010, 143:1018-1029.
34. Prentice H.M., Moore S.E., Dickson J.G., Doherty P., Walsh F.S. Nerve growth factor-induced changes in neural cell adhesion molecule (N-CAM) in PC12 cells. EMBO J. 1987, 6:1859-1863.
35. Proudfoot N.J. Ending the message: poly(A) signals then and now. Genes Dev. 2011, 25:1770-1782.
36. Ruepp M.D., Schweingruber C., Kleinschmidt N., Schümperli D. Interactions of CstF-64, CstF-77, and symplekin: implications on localisation and function. Mol. Biol. Cell 2011, 22:91-104.
37. Shankarling G.S., Coates P.W., Dass B., MacDonald C.C. A family of splice variants of CstF-64 expressed in vertebrate nervous systems. BMC Mol. Biol. 2009, 10:22.
38. Shi Y., Di Giammartino D.C., Taylor D., Sarkeshik A., Rice W.J., et al. Molecular architecture of the human pre-mRNA 3' processing complex. Mol. Cell 2009, 33:365-376.
39. Shin C., Manley J.L. Cell signalling and the control of pre-mRNA splicing. Nat. Rev. Mol. Cell Biol. 2004, 5:727-738.
40. Smith M.A., Fanger G.R., O'Connor L.T., Bridle P., Maue R.A. Selective regulation of agrin mRNA induction and alternative splicing in PC12 cells by Ras-dependent actions of nerve growth factor. J. Biol. Chem. 1997, 272:15675-15681.
41. Sun Y., Fu Y., Li Y., Xu A. Genome-wide alternative polyadenylation in animals: insights from high-throughput technologies. J. Mol. Cell Biol. 2012, 4:352-361.
42. r protein of the cleavage stimulation factor are expressed in mouse male germ cells. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:6763-6768.
43. Wallace A.M., Denison T., Attaya E.N., MacDonald C.C. Developmental differences in expression of two forms of the CstF-64 polyadenylation protein in rat and mouse. Biol. Reprod. 2004, 70:1080-1087.
44. Wang E.T., Sandberg R., Luo S., Khrebtukova I., Zhang L., et al. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456:470-476.
45. Wiesmann C., de Vos A.M. Nerve growth factor: structure and function. Cell. Mol. Life Sci. 2001, 58:748-759.
46. Yang X.C., Sabath I., Debski J., Kaus-Drobek M., Dadlez M., et al. A complex containing the CPSF73 endonuclease and other polyadenylation factors associates with U7 snRNP and is recruited to histone pre-mRNA for 3'-end processing. Mol. Cell. Biol. 2013, 33:28-37.
47. Zhang H., Lee J.Y., Tian B. Biased alternative polyadenylation in human tissues. Genome Biol. 2005, 6:R100.
48. Zhu H., Zhou H.L., Hasman R.A., Lou H. Hu proteins regulate polyadenylation by blocking sites containing U-rich sequences. J. Biol. Chem. 2007, 282:2203-2210.