NMDA induces post-transcriptional regulation of α2-guanylyl-cyclase-subunit expression in cerebellar granule cells

Journal of Cell Science

Volumn 119, Issue 8, 2006, Pages 1622-1631

  Jurado, Sandra ^a   Rodríguez Pascual, Fernando ^b   Sánchez Prieto, José ^a   Reimunde, Francisco M ^b   Lamas, Santiago ^b   Torres, Magdalena ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

AUF1; Cerebellar granule cells; mRNA decay; N methyl D aspartate; NO sensitive guanylyl cyclase

Indexed keywords

CALCIUM ION; CYCLIC GMP DEPENDENT PROTEIN KINASE; DACTINOMYCIN; GUANYLATE CYCLASE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; HUR PROTEIN; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CEREBELLUM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME SUBUNIT; FEMALE; GENE EXPRESSION; GENETIC CODE; GENETIC TRANSCRIPTION; GRANULE CELL; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA STABILITY; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CELL NUCLEUS; CELLS, CULTURED; CEREBELLUM; CYCLIC GMP; FEMALE; GUANYLATE CYCLASE; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN D; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; MALE; MOLECULAR SEQUENCE DATA; N-METHYLASPARTATE; NITRIC ACID; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; UP-REGULATION;

ANIMALIA;

EID: 33646704032     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02867     Document Type: Article

References (61)

1. Akamatsu, W., Okano, H. J., Osumi, N., Inoue, T., Nakamura, S., Sakakibara, S.-L., Miura, M., Matsuo, N., Darnell, R. B. and Okano, H. (1999). Mammalian ELAV-like neuronal RNA-binding proteins HuB and HuC promote neuronal development in both the central and the peripheral nervous system. Proc. Natl. Acad. Sci. USA 96, 9885-9890.
2. Altus, M. S., Pearson, D., Horiuchi, A. and Nagamine, Y. (1987). Inhibition of protein synthesis in LLC-PKl cells increases calcitonin-induced plasminogen-activator gene transcription and mRNA stability. Biochem. J. 242, 387-392.
3. Baader, S. L. and Schilling, K. (1996). Glutamate receptors mediate dynamic regulation of nitric oxide synthase expression in cerebellar granule cells. J. Neurosci. 16, 1440-1449.
4. Balazs, R., Jorgensen, O. S. and Hack, N. (1988). N-Methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neuroscience 27, 437-451.
5. Baptista, C. A., Hatten, M. E., Blazeski, R. and Mason, A. (1994). Cell-cell interactions influence survival and differentiation of purified Purkinje cells in vitro. Neuron 12, 243-260.
6. Bessho, Y., Nawa, H. and Nakanishi, S. (1994). Selective up-regulation of an NMDA receptor subunit mRNA in cultured cerebellar granule cells by K(+)-induced depolarization and NMDA treatment. Neuron 12, 87-95.
7. Bhattacharya, S., Giordano, T., Brewer, G. and Malter, J. S. (1999). Identification of AUF-1 ligands reveals vast diversity of early response gene mRNAs. Nucleic Acid Res. 27, 1464-1472.
8. Bredt, D. S. and Snyder, S. H. (1994). Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium. Neuron 13, 301-313.
9. Brenman, J. E., Chao, D. S., Gee, S. H., McGee, A. W., Craven, S. E., Santillano, D. R., Wu, Z., Huang, F., Xia, H., Peters, M. F. et al. (1996). Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alphal-syntrophin mediated by PDZ domains. Cell 84, 757-767.
10. Brewer, G. (1991). An A + U-rich element RNA-binding factor regulates c-myc mRNA stability in vitro. Mol. Cell. Biol. 11, 2460-2466.
11. Brewer, G. (1995). Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus. J. Neurosci. Res. 42, 674-683.
12. Broillet, M. C., Randin, O. and Chatton, J.-Y. (2001). Photoactivation and calcium sensitivity of the fluorescent NO indicator 4,5-diaminofluorescein (DAF-2): implications for cellular NO imaging. FEBS Lett. 491, 227-232.
13. Carballo, E., Lai, W. S. and Blackshear, P. J. (2000). Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability. Blood 95, 1891-1899.
14. Chan, S. H., Chang, K. F., Ou, C. C. and Chan, J. Y. (2004). Nitric oxide regulates c-fos expression in nucleus tractus solitarii induced by baroreceptor activation via cGMP-dependent protein kinase and cAMP response element-binding protein phosphorylation. Mol. Pharmacol. 65, 319-325.
15. Chen, C. Y. and Shyu, A.-B. (1995). AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20, 465-470.
16. Chen, Y., Zhuang, S., Cassenaer, S., Casteel, D. E., Gudi, T., Boss, G. R. and Pilz, R. B. (2003). Synergism between calcium and cyclic GMP in cyclic AMP response element-dependent transcriptional regulation requires cooperation between CREB and C/EBP-beta. Mol. Cell. Biol. 23, 4066-4082.
17. Ciani, E., Guidi, S., Bartesaghi, R. and Contestabile, A. (2002). Nitric oxide regulates cGMP-dependent CREB phosphorylation and Bcl-2 expression in cerebellar neurons: implication for a survival role of nitric oxide. J. Neurochem. 82, 1282-1289.
18. Contestabile, A. (2000). Roles of NMDA receptor activity and nitric oxide production in brain development. Brain Res. Brain Res. Rev. 32, 476-509.
19. Craven, S. E. and Bredt, D. S. (1998). PDZ proteins organize synaptic signalling pathways. Cell 93, 495-498.
20. Dawson, V. L., Dawson, T. M., Bartley, D. A., Uhl, G. R. and Snyder, S. H. (1993). Mechanism of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13, 2651-2661.
21. Ding, J.-D., Burette, A. and Weinberg, R. J. (2005). Expression of soluble guanylyl cyclase in rat cerebral cortex during postnatal development. J. Comp. Neural. 485, 255-265.
22. Fan, X. C. and Steitz, J. A. (1998). HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc. Natl. Acad. Sci. USA 95, 15293-15298.
23. Ferrero, R. and Torres, M. (2002). Prolonged exposure of chromaffin cells to nitric oxide down-regulates the activity of soluble guanylyl cyclase and corresponding mRNA and protein levels. BMC Biochem. 3, 26.
24. Ferrero, R., Rodríguez-Pascual, F., Miras-Portugal, M. T. and Torres, M. (2000). Nitric oxide-sensitive guanylyl cyclase activity inhibition through cyclic GMP-dependent dephosphorylation. J. Neurochem. 75, 2029-2039.
25. Fujiwara, M., Sengupta, P. and McIntire, S. L. (2002). Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36, 1091-1102.
26. Garthwaite, J. and Boulton, C. L. (1995). Nitric oxide signalling in the central nervous system. Annu. Rev. Physiol. 57, 683-706.
27. Garthwaite, J., Garthwaite, G. and Hajos, F. (1986). γ-Aminobutyric acid affects the developmental expression of neuron-associated proteins in cerebellar granule cell culture. J. Neurochem. 46, 1256-1262.
28. Gibb, B. J. and Garthwaite, J. (2001). Subunits of the nitric oxide receptor, soluble guanylyl cyclase, expressed in rat brain. Eur. J. Neurosci. 13, 539-544.
29. Gudi, T., Hong, G. K., Vaandrager, A. B., Lhomann, S. M. and Pilz, R. B. (1999). Nitric oxide and cGMP regulate gene expression in neuronal and glial cells by activating type II cGMP-dependent protein kinase. FASEB J. 13, 2143-2152.
30. Guhaniyogi, J. and Brewer, G. (2001). Regulation of mRNA stability in mammalian cells. Gene 265, 11-23.
31. Holscher, C. (1997). Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci. 20, 298-303.
32. Jurado, S., Sánchez-Prieto, J. and Torres, M. (2003). Differential expression of NO-sensitive guanylyl cyclase subunits during the development of rat cerebellar granule cells: regulation via N-methyl-D-aspartate receptors. J. Cell Sci. 116, 3165-3175.
33. Jurado, S., Sánchez-Prieto, J. and Torres, M. (2004). Elements of the nitric oxide/cGMP pathway expressed in cerebellar granule cells: biochemical and functional characterisation. Neurochem. Int. 45, 833-843.
34. Kleinschmidt, A., Bear, M. F. and Singer, W. (1987). Blockade of NMDA receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238, 355-358.
35. Klöss, S., Furneaux, H. and Mülsch, A. (2003). Post-transcriptional regulation of soluble guanylyl cyclase expression in rat aorta. J. Biol. Chem. 278, 2377-2383.
36. Klöss, S., Srivastava, R. and Mülsch, A. (2004). Down-regulation of soluble guanylyl cyclase expression by cyclic AMP is mediated by mRNA-stabilizing protein HuR. Mol. Pharmacol. 65, 1440-1451.
37. 2 subunit of soluble guanylyl cyclase. Biochim. Biophys. Acta 1494, 286-289.
38. Lal, A., Mazan-Mamezarz, K., Kawai, T., Yang, X., Martindale, J. L. and Gorospe, M. (2004). Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23, 3092-3102.
39. L'Etoile, N. D., Coburn, C. M., Eastham, J., Kistler, A., Gallegos, G. and Bargmann, C. L. (2002). The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans. Neuron 36, 1079-1089.
40. Ma, W. J., Cheng, S., Campbell, C., Wright, A. and Furneaux, H. (1996). Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J. Biol. Chem. 271, 8144-8151.
41. Meier, E. and Jorgensen, O. S. (1986). Gamma-aminobutyric acid affects the developmental expression of neuron-associated proteins in cerebellar granule cell culture. J. Neurochem. 45, 1256-1262.
42. Mergia, E., Russwurm, M., Zoidl, G. and Koesling, D. (2003). Major occurrence of the new αβ1 isoform of NO-sensitive guanylyl cyclase in brain. Cell. Signal. 15, 189-195.
43. Oliveira, C. C. and McCarthy, J. E. G. (1995). The relationship between eukaryotic translation and mRNA stability: a short upstream open reading frame strongly inhibits translational initiation and greatly accelerates mRNA degradation in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 270, 8936-8943.
44. Pearce, I. A., Cambray-Deakin, M. A. and Burgoyne, R. D. (1987). Glutamate acting on NMDA receptors stimulates neurite outgrowth from cerebellar granule cells. FEBS Lett. 233, 143-147.
45. Pendel, A., Tremmel, K. D., DeMaria, C. T., Blaxall, B. C., Minobe, W. A., Sherman, J. A., Bisognano, J. D.,Bristow, M. R., Brewer, G. and Port, J. D. (1996). Regulation of the mRNA-binding protein AUFl by activation of the β-adrenergic receptor signal transduction pathway. J. Biol. Chem. 271, 8493-8501.
46. Peng, S. S.-Y., Chen, C.-Y. A., Xu, N. and Shyu, A.-B. (1998). RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17, 3461-3470.
47. Pérez-Sala, D., Cernuda-Morollon, E., Díaz-Cazorla, M., Rodríguez-Pascual, F. and Lamas, S. (2001). Posttranscriptional regulation of human iNOS by the NO/cGMP pathway. Am. J. Physiol. Renal Physiol. 280, F466-F473.
48. Pilz, R. B. and Broderick, K. E. (2005). Role of cyclic GMP in gene regulation. Front. Biosci. 10, 1239-1268.
49. Polleux, F., Morrow, T. and Ghosh, A. (2000). Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404, 567-573.
50. Rodríguez-Pascual, F., Hausding, M., Ihrig-Biedert, I., Furneaux, H., Levy, A. P., Förstermann, U. and Kleinert, H. (2000). Complex contribution of the 3′- untranslated region to the expressional regulation of the human inducible nitric-oxide synthase gene. Involvement of the RNA-binding protein HuR. J. Biol. Chem. 275, 26040-26049.
51. Ross, J. (1995). mRNA stability in mammalian cells. Microbiol. Rev. 59, 423-450.
52. Russwurm, M., Wittaus, N. and Koesling, D. (2001). Guanylyl cyclase/ PSD-95 interaction targeting of the nitric oxide-sensitive α2β1 guanylyl cyclase to synaptic membranes. J. Biol. Chem. 276, 44647-44652.
53. Sachs, A.-B. (1993). Messenger RNA degradation in eukaryotes. Cell 74, 413-421.
54. Savant-Bhonsale, S. and Cleveland, D. W. (1992). Evidence for instability of mRNAs containing AUUUA motifs mediated through translation-dependent assembly of mRNAs >20S degradation complex. Genes Dev. 6, 1927-1939.
55. Schreiber, E., Matthias, P., Muller, M. M. and Schaffner, W. (1989). Rapid detection of octamer binding proteins with "mini-extracts", prepared from a small number of cells. Nucleic Acids Res. 17, 6418.
56. Sheng, M. and Pak, D. T. (2000). Ligand-gated ion channel interactions with cytoskeletal and signalling proteins. Annu. Rev. Physiol. 62, 755-778.
57. Smolenski, A., Schultess, J., Danielewski, O., Arguinzonis, M. I. G., Thalheimer, P., Kneitz, S., Walter, U. and Lohmann, S. M. (2004). Quantitative analysis of the cardiac fibroblast transcriptome-implications for NO/cGMP signaling. Genomics 83, 577-587.
58. Virgili, M., Facchinetti, F., Sparapani, M., Tregnago, M., Lucchi, R., Dall'Olio, R., Gandolfi, O. and Contestabile, A. (1998). Neuronal nitric oxide synthase is permanently decreased in the cerebellum of rats subjected to chronic neonatal blockade of N-methyl-D-aspartate receptors. Neurosci. Lett. 258, 1-4.
59. Wagenen, S. V. and Rehder, V. (2001). Regulation of neuronal growth cone filopodia by nitric oxide depends on soluble guanylyl cyclase. J. Neurobiol. 46, 206-219.
60. Wagner, B. J., De Maria, C. T., Sun, Y., Wilson, G. M. and Brewer, G. (1998). Structure and genomic organization of the human AUF1 gene: alternative pre-mRNA splicing generates four protein isoforms. Genomics 48, 195-202.
61. Xu, N., Chen, C. Y. and Shyu, A.-B. (1997). Modulation of the fate of cytoplasmic mRNA by AU-rich elements: key sequence features controlling mRNA deadenylation and decay. Mol. Cell. Biol. 17, 4611-4621.