Role of highly conserved pyrimidine-rich sequences in the 3′ untranslated region of the GAP-43 mRNA in mRNA stability and RNA-protein interactions

Molecular Brain Research

Volumn 36, Issue 2, 1996, Pages 240-250

  Kohn, Douglas T ^a   Tsai, Kao Chung ^a   Cansino, Victor V ^a   Neve, Rachael L ^b   Perrone Bizzozero, Nora I ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b MCLEAN HOSPITAL   (United States)

Author keywords

3 untranslated region; GAP 43; Gene expression; MRNA stability; RNA protein interaction; Sequence conservation

Indexed keywords

BETA GLOBIN; BRAIN PROTEIN; MESSENGER RNA; NEUROMODULIN; PYRIMIDINE; RNA BINDING PROTEIN;

ANIMAL CELL; ARTICLE; CHICKEN; CONTROLLED STUDY; DNA TRANSFECTION; HALF LIFE TIME; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; RAT; RNA DEGRADATION; RNA SEQUENCE; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION; TRANSGENE;

EID: 0029868063     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/0169-328X(95)00239-O     Document Type: Article

References (58)

1. Alberta, J.A., Rundell, K. and Stiles, C.D., Identification of an activity that interacts with the 3′-untranslated region of c-myc mRNA and the role of its target sequence in mediating rapid mRNA degradation, J. Biol. Chem., 269 (1994) 4532-4538.
2. Baizer, L., Alkan, S., Stocker, K. and Ciment, G., Chicken growth-associated protein (GAP-43): primary structure and regulated expression of mRNA during embryogenesis, Mol. Brain Res., 7 (1990) 61-68.
3. Basi, G.S., Jacobson, R.D., Virag, I., Schilling, J. and Skene, J.H.P., Primary structure and transcriptional regulation of GAP-43, a protein associated with nerve growth, Cell, 49 (1987) 785-791.
4. Belasco, J. and Brawerman, G., Control of messenger RNA stability, 1993, San Diego, CA: Academic Press.
5. Bell, L.R., Maine, E.M., Schnedl, P. and Cline, T.W., Sex-lethal, a Drosophila sex determination switch gene, exhibits sex-specific RNA splicing and sequence similarity to RNA binding proteins, Cell, 55 (1988) 1037-1046.
6. Benowitz, L.I. and Routtenberg, A., A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism and synaptic plasticity, Trends Neurosci., 10 (1987) 527-532.
7. Bohjanen, P.R., Petryniak, B., June, C.H., Thompson, C.B. and Lindsten, T., AU RNA-binding factors differ in their binding specificities and affinities, J. Biol. Chem., 267 (1992) 6302-6309.
8. Brewer, G., An A + U-rich element RNA binding factor regulates c-myc mRNA stability in vitro, Mol. Cell. Biol., 11 (1991) 3288-3295.
9. Burry, R.W. and Perrone-Bizzozero, N.I., Nerve growth factor stimulates GAP-43 expression in PC12 cell clones independently of neurite outgrowth, J. Neurosci. Res., 36 (1993) 241-251.
10. Chen, C.-Y. A., Chen, T.-M. and Shyu, A.-B., Interplay of two functionally and structurally distinct domains of the c-fos AU-rich element specifies its mRNA-destabilizing function, Mol. Cell. Biol., 14 (1994) 416-426.
11. Cleveland, D.W., Gene regulation through messenger RNA stability, Curr. Opin. Biol., 1 (1989) 1148-1153.
12. Costello, B., Meymandi, A. and Freeman, J.A., Factors influenceing GAP-43 gene expression in PC12 pheochromocytoma cells, J. Neurosci., 10 (1990) 1398-1406.
13. Czyzyk-Krzeska, M.F., Furnari, B.A., Lawson, E.E. and Milhorn, D.E., Hypoxia increases rate of transcription and stability of tyrosine hydroxylase mRNA in pheochromocytoma (PC12) cells, J. Biol Chem., 269 (1994) 760-764.
14. Decker, C.J. and Parker, R., Mechanisms of mRNA degradation in eukaryotes, Trends Biochem, Sci., 19 (1994) 336-340.
15. Dignam, J., Lebovitz, R.M. and Roeder, R.D., Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei, Nucleic Acids Res., 11 (1983) 1475-1489.
16. Duret, L., Dorkeld, F. and Gautier, C., Strong conservation of non-coding sequences during evolution: potential involvement in post-transcriptional regulation of gene expression, Nucleic Acids Res., 21 (1993) 2315-2322.
17. Eggen, B.J.L., Nielander, H.B., Rensen-De Leeuw, M.G.A., Schotman, P., Gispen, W.H. and Schrama, L.H., Identification of two promotor regions in the rat B-50/GAP-43 gene, Mol. Brain Res., 23 (1994) 221-234.
18. Federoff, H.J., Grabczyk, E. and Fishman, M.C., Dual regulation of GAP-43 gene expression by nerve growth factor and glucocorticoids, J. Biol. Chem., 263 (1988) 19290-19295.
19. Fennyhough, P., Mill, J.F., Roberts, J.L. and Ishii, D.N., Stabilization of tubulin mRNAs by insulin and insulin-like growth factor I during neurite formation, Mol. Brain Res., 6 (1989) 109-120.
20. Gorman, C., Padmanabhan, R. and Howard, B.H., High efficiency DNA-mediated transformation of primate cells, Science, 221 (1983) 551-553.
21. Grima, B., Lamouroux, A., Blanot, F., Biguet, N.F. and Mallet, F., Complete coding equence of rat tyrosine hydroxylase mRNA, Proc. Natl. Acad. Sci. USA, 82 (1985) 617-621.
22. Hadcock, J.R., Wang, H. and Malbon, C.C., Agonist-induced destabilization of the β-adrenergic receptor mRNA, J. Biol. Chem., 264 (1989) 19928-19933.
23. Ikenaka, K., Nakahira, K., Takayama, C., Wada, K., Hatanaka, H. and Mikoshiba, K., Nerve growth factor rapidly induces expression of the 68-kDa neurofilament gene by posttranscriptional modification in PC12h-R cells, J. Biol. Chem., 265 (1990) 19782-19785.
24. Kang, J., Lemaire, H.-G., Unterbeck, A., Salbaum, J.M., Masters, C.L., Grzeschik, K.H., Multhaup, G., Beyreuther, K. and Muller-Hill, B., The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor, Nature, 325 (1987) 733-736.
25. Kim, Y.-J. and Baker, B.S., The Drosophila gene rbp 9 encodes a protein that is a member of a conserved group of putative RNA binding proteins that are nervous system-specific in both flies and humans, J. Neurosci., 13 (1993) 1045-1056.
26. Klausner, R.D., Rouault, T.A. and Harford, J.B., Regulating the fate of mRNA: The control of cellular iron metabolism, Cell, 72 (1993) 19-28.
27. Kohn, D.T. and Perrone-Bizzozero, N.I., Brain proteins bind to the 3′UTR of the GAP-43 mRNA, J. Neurochem., 62 Suppl. (1993) S14.
28. Levine, T.D., Gao, F., King, P.H., Andrews, L.G. and Keene, J.D., Hel-N1: an autoimmune RNA-binding protein with specificity for 3′ uridylate-rich untranslated regions of growth factor mRNAs, Mol. Cell. Biol., 13 (1993) 3494-3504.
29. Liebold, H.A. and Munro, H.N., Cytoplasmic protein binds in vitro to a highly conserved sequence in the 5′ untranslated region of ferritin heavy- and light-subunit mRNAs, Proc. Natl. Acad. Sci. USA, 85 (1988) 2171-2175.
30. Malter, J.S., Identification of an AUUUA-specific messenger RNA binding protein, Science, 246 (1989) 664-666.
31. Müllner, E.W., Neupert, B. and Kühn, L.C., A specific mRNA binding factor regulates the iron-dependent stability of cytoplasmic transferrin receptor mRNA, Cell, 58 (1989) 373-382.
32. Nedivi, E., Basi, G.S., Akey, I.V. and Skene, J.H.P., A neural-specific GAP-43 core promoter located between unusual DNA elements that regulate its activity, J. Neurosci., 12 (1992) 691-704
33. Neve, R.N., Perrone-Bizzozero, N.I., Finklestein, S., Zwiers, H., Bird, E., Kurnit, D. and Benowitz, L.I., The neuronal growth-associated protein GAP-43 (B-50, F1): specificity, developmental regulation and regional expression of the human and rat genes, Mol. Brain Res., 2 (1987) 177-183.
34. Nielander, H.B., De Groen, P.C., Eggen, B.J.L., Schrama, L.H., Gispen, W.H. and Schotman, P., Structure of the human gene for the neural phosphoprotein B-50 (GAP-43) Mol. Brain Res., 19 (1993) 293-302.
35. Owen, D. and Kühn, L.C., Noncoding 3′ sequences of the transferrin receptor gene are required for mRNA regulation by iron, EMBO J., 6 (1987) 1287-1293.
36. Pandey, N.B. and Marzluff, W.F., The stem-loop structure at the 3′ end of histone mRNA is necessary and sufficient for regulation of histone mRNA stability, Mol. Cell. Biol., 7 (1987) 4557-4559.
37. Pandey, N.B., Sun, J.-H. and Marzuff, W.F., Different complexes are formed on the 3′ end of histone mRNA with nuclear and polyribosomal proteins, Nucleic Acids Res., 19 (1991) 5653-5659.
38. Perrone-Bizzozero, N.I., Tsai, K-C., Cansino, V.V., Romero, L. and Burry, R.W., Post-transcriptional control of GAP-43 mRNA in transfected cells, J. Neurochem., 62 Suppl. (1994) S14C.
39. Perrone-Bizzozero, N.I., Cansino, V.V. and Kohn, D.T., Post-transcriptional regulation of GAP-43 gene expression in PC12 cells through PKC-dependent stabilization of the mRNA, J. Cell Biol., 120 (1993) 1263-1270.
40. Perrone-Bizzozero, N.I., Neve, R.L., Irwin, N, Lewis, S., Fischer, I. and Benowitz, L.I., Post-transcriptional regulation of GAP-43 mRNA levels during neuronal differentiation and nerve regeneration, Mol. Cell Neurosci., 2 (1991) 402-409.
41. Rajagopalan, L.E. and Malter, J.S., Modulation of granulocyte-macrophage colony-stimulating factor mRNA stability in vitro by the adenosine-uridine binding factor, J. Biol. Chem., 269 (1994) 23882-23888.
42. Robinow, S., Campos, A., Yao, K. and White, K., The elav gene product of Drosophila, required in neurons, has three RNP consensus motifs, Science, 42 (1988) 1570-1572.
43. Ross, J. and Kobs, G., H4 Histone messenger RNA Decay in cell-free extracts initiates at or near the 3′ terminus and proceeds 3′ to 5′, J. Mol. Biol., 188 (1986) 579-583.
44. Sachs, A.B., Messenger RNA degradation in eukaryotes, Cell, 74 (1993) 413-421.
45. Savant-Bhonsale, S. and Cleveland, D. W., Evidence for instability of mRNAs containing AUUUA motifs mediated through translation-dependent assembly of a > 20S degradation complex, Genes Dev., 6 (1992) 1927-1939.
46. Shaw, G. and Kamen, R., Regulation of GM-CSF mRNA mediates selective mRNA degradation, Cell, 46 (1986) 659-667
47. Shyu, A.-B., Belasco, J.G. and Greenberg, M.E., Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay, Genes Dev., 5 (1989) 221-231.
48. Skene, J.H.P., Axonal growth-associated proteins, Annu. Rev. Neurosci., 12 (1989) 127-156.
49. Starr, R.G., Lu, B. and Federoff, H.J., Functional characterization of the rat GAP-43 promoter, Brain Res., 638 (1994) 211-220.
50. Szabo, A., Dalmau, J., Manley, G., Rosenfeld, M., Wong, E., Henson, J., Posner, J.B. and Furneaux, H.M., HuD, a paraneoplastic encephalomyelitis antigen, contains RNA-binding domains and is homologous to Elav and Sex-lethal, Cell, 67 (1991) 325-333.
51. Vakalopoulou, E., Schaack, J. and Shenk, T., A 32-kilodalton protein binds to AU-rich domains in the 3′ untranslated regions of rapidly degraded mRNAs, Mol. Cell Biol., 11 (1991) 3355-3364.
52. Vanselow, J., Grabczyk, E., Ping, J., Baetsher, M., Teng, S. and Fishman, M., GAP-43 transgenic mice: dispersed genomic sequences confer a GAP-43 like expression during development and regeneration, J.Neurosci., 14 (1994) 499-510.
53. Verhaagen, J., Koster, J.G., Schrama, L.H., Eggen, B.J.L., van der Neut, R., Gispen, W.H. and Destree, O.H.J., The rat B-50(GAP-43) promoter directs neural-preferred expression of a reporter gene in Xenopus laevis embryos, Neurosci. Res. Commun., 13 (1993) 83-90.
54. Wilson, T. and Treisman, R., Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3′ AU-rich sequences, Nature, 336 (1988) 396-399.
55. Wilusz, J. and Shenk, T., A 64 kd nuclear protein binds to RNA segments that include the AAUAAA polyadenylation motif, Cell, 52 (1988) 221-228.
56. You, Y., Chen, C.-Y. A. and Shyu, A.-B., U-rich sequnce-binding proteins (URBPs) interacting with a 20-nucleotide U-rich sequence in the 3′ untranslated region of c-fos mRNA may be involved in the first step of c-fos mRNA degradation, Mol. Cell. Biol., 12 (1992) 2931-2940.
57. Zaidi, S.H.E. and Malter, J.S., Amyloid precursor protein mRNA stability is controlled by a 29-base element in the 3′-untranslated region, J. Biol. Chem., 269 (1994) 24007-24013.
58. Zaidi, S.H.E., Denman, R. and Malter, J.S., Multiple proteins interact at a unique cis-element in the 3′-untranslated region of amyloid precursor protein mRNA, J. Biol. Chem., 269 (1994) 24000-24006.