Lovastatin effect in rat neuroblasts of the CNS: Inhibition of cap-dependent translation

Journal of Neurochemistry

Volumn 106, Issue 3, 2008, Pages 1078-1091

  Santa Catalina, Marta Olivera ^a   Garcia Marin, Luis Jesus ^b   Bragado, María Julia ^a  

^a Research Group of Intracellular Signalling and Technology of Reproduction   (Spain)

^b UNIVERSITY OF EXTREMADURA   (Spain)

Author keywords

eIF4G; Eukaryotic translation initiation factor 4E binding protein 1; Lovastatin; Neuroblasts; Translation

Indexed keywords

CASPASE; CASPASE 3; CYCLOHEXIMIDE; INITIATION FACTOR 4E BINDING PROTEIN 1; INITIATION FACTOR 4G; MAMMALIAN TARGET OF RAPAMYCIN; MEVINOLIN; PHOSPHATIDYLINOSITOL 3 KINASE; S6 KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; RAT;

ANIMALS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; DOSE-RESPONSE RELATIONSHIP, DRUG; LOVASTATIN; NEURONS; PROTEIN BIOSYNTHESIS; RATS; RNA CAP-BINDING PROTEINS;

EUKARYOTA; RATTUS;

EID: 48249135492     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05458.x     Document Type: Article

References (62)

1. Bradley C. A., Padovan J. C., Thompson T. L., Benoit C. A., Chait B. T. Rhoads R. E. (2002) Mass spectrometric analysis of the N terminus of translational initiation factor eIF4G-1 reveals novel isoforms. J. Biol. Chem. 277, 12559 12571.
2. Bragado M. J., Groblewski G. E. Williams J. A. (1998) Regulation of protein synthesis by cholecystokinin in rat pancreatic acini involves PHAS-I and the p70 S6 kinase pathway. Gastroenterology 115, 733 742.
3. Bushell M., McKendrick L., Janicke R. U., Clemens M. J. Morley S. J. (1999) Caspase-3 is necessary and sufficient for cleavage of protein synthesis eukaryotic initiation factor 4G during apoptosis. FEBS Lett. 451, 332 336.
4. Byrd M. P., Zamora M. Lloyd R. E. (2002) Generation of multiple isoforms of eukaryotic translation initiation factor 4GI by use of alternate translation initiation codons. Mol. Cell. Biol. 22, 4499 4511.
5. Casadio A., Martin K. C., Giustetto M., Zhu H., Chen M., Bartsch D., Bailey C. H. Kandel E. R. (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99, 221 237.
6. Cavender C. P., Turley S. D. Dietschy J. M. (1995) Sterol metabolism in fetal, newborn, and suckled lambs and their response to cholesterol after weaning. Am. J. Physiol. 269, E331 E340.
7. Cerezo-Guisado M. I., Garcia-Marin L. J., Lorenzo M. J. Bragado M. J. (2005) Lovastatin inhibits the growth and survival pathway of phosphoinositide 3-kinase/protein kinase B in immortalized rat brain neuroblasts. J. Neurochem. 94, 1277 1287.
8. Cerezo-Guisado M. I., Garcia-Roman N., Garcia-Marin L. J., varez-Barrientos A., Bragado M. J. Lorenzo M. J. (2007a) Lovastatin inhibits the extracellular-signal-regulated kinase pathway in immortalized rat brain neuroblasts. Biochem. J. 401, 175 183.
9. Cerezo-Guisado M. I., varez-Barrientos A., Argent R., Garcia-Marin L. J., Bragado M. J. Lorenzo M. J. (2007b) c-Jun N-terminal protein kinase signalling pathway mediates lovastatin-induced rat brain neuroblast apoptosis. Biochim. Biophys. Acta 1771, 164 176.
10. Clemens M. J., Bushell M., Jeffrey I. W., Pain V. M. Morley S. J. (2000) Translation initiation factor modifications and the regulation of protein synthesis in apoptotic cells. Cell Death Differ. 7, 603 615.
11. Constantinou C. Clemens M. J. (2007) Regulation of translation factors eIF4GI and 4E-BP1 during recovery of protein synthesis from inhibition by p53. Cell Death Differ. 14, 576 585.
12. Darzynkiewicz Z., Bruno S., Del Bino G., Gorczyca W., Hotz M. A., Lassota P. Traganos F. (1992) Features of apoptotic cells measured by flow cytometry. Cytometry 13, 795 808.
13. Duits N. Bos F. M. (1993) Depressive symptoms and cholesterol-lowering drugs. Lancet 341, 114.
14. Garcia-Roman N., Alvarez A. M., Toro M. J., Montes A. Lorenzo M. J. (2001) Lovastatin induces apoptosis of spontaneously immortalized rat brain neuroblasts: involvement of nonsterol isoprenoid biosynthesis inhibition. Mol. Cell. Neurosci. 17, 329 341.
15. Goelet P., Castellucci V. F., Schacher S. Kandel E. R. (1986) The long and the short of long-term memory - a molecular framework. Nature 322, 419 422.
16. Goldstein J. L. Brown M. S. (1990) Regulation of the mevalonate pathway. Nature 343, 425 430.
17. Gonzalez-Fernandez L., Cerezo-Guisado M. I., Langmesser S., Bragado M. J., Lorenzo M. J. Garcia-Marin L. J. (2006) Cleavage of focal adhesion proteins and PKCdelta during lovastatin-induced apoptosis in spontaneously immortalized rat brain neuroblasts. FEBS J. 273, 1 13.
18. Graves L. M., Bornfeldt K. E., Argast G. M., Krebs E. G., Kong X., Lin T. A., Lawrence J. C. Jr (1995) cAMP- and rapamycin-sensitive regulation of the association of eukaryotic initiation factor 4E and the translational regulator PHAS-I in aortic smooth muscle cells. Proc. Natl Acad. Sci. USA 92, 7222 7226.
19. Guijarro C., Blanco-Colio L. M., Ortego M., Alonso C., Ortiz A., Plaza J. J., Diaz C., Hernandez G. Egido J. (1998) 3-Hydroxy-3-methylglutaryl coenzyme a reductase and isoprenylation inhibitors induce apoptosis of vascular smooth muscle cells in culture. Circ. Res. 83, 490 500.
20. Holcik M., Sonenberg N. Korneluk R. G. (2000) Internal ribosome initiation of translation and the control of cell death. Trends Genet. 16, 469 473.
21. Hu C., Pang S., Kong X., Velleca M., Lawrence J. C. Jr (1994) Molecular cloning and tissue distribution of PHAS-I, an intracellular target for insulin and growth factors. Proc. Natl Acad. Sci. USA 91, 3730 3734.
22. Huber K., Kuehnel F., Wyatt S. Davies A. M. (2000) TrkB expression and early sensory neuron survival are independent of endogenous BDNF. J. Neurosci. Res. 59, 372 378.
23. Johnson-Anuna L. N., Eckert G. P., Keller J. H., Igbavboa U., Franke C., Fechner T., Schubert-Zsilavecz M., Karas M., Müller W. E. Word W. G. (2005) Chronic administration of statins alters multiple gene expression patterns in mouse cerebral cortex. J. Pharmacol. Exp. Ther. 312, 786 793.
24. Johnson-Anuna L. N., Eckert G. P., Franke C., Igbavboa U., Müller W. E. Word W. G. (2007) Simvastatin protects neurons from cytotoxicity by up-regulating Bcl-2 mRNA and protein. J. Neurochem. 101, 77 86.
25. Jones K. D., Couldwell W. T., Hinton D. R., Su Y., He S., Anker L. Law R. E. (1994) Lovastatin induces growth inhibition and apoptosis in human malignant glioma cells. Biochem. Biophys. Res. Commun. 205, 1681 1687.
26. Kang H. Schuman E. M. (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273, 1402 1406.
27. Kim J. S., Pirnia F., Choi Y. H. et al. (2000) Lovastatin induces apoptosis in a primitive neuroectodermal tumor cell line in association with RB down-regulation and loss of the G1 checkpoint. Oncogene 19, 6082 6090.
28. Kita T., Brown M. S. Goldstein J. (1980) Feedback regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase in livers of mice treated with mevinolin, a competitive inhibitor of the reductase. J. Clin. Invest. 6, 1094 1100.
29. Klann E. Dever T. E. (2004) Biochemical mechanisms for translational regulation in synaptic plasticity. Nat. Rev. Neurosci. 5, 931 942.
30. Kotti T. J., Ramirez D. M., Pfeiffer B. E., Huber K. M. Russell D. W. (2006) Brain cholesterol turnover required for geranylgeraniol production and learning in mice. Proc. Natl Acad. Sci. USA 103, 3869 3874.
31. Lin T. A., Kong X., Haystead T. A., Pause A., Belsham G., Sonenberg N. Lawrence J. C. Jr (1994) PHAS-J as a link between mitogen-activated protein kinase and translation initiation. Science 266, 653 656.
32. Macaulay R. J., Wang W., Dimitroulakos J., Becker L. E. Yeger H. (1999) Lovastatin-induced apoptosis of human medulloblastoma cell lines in vitro. J. Neurooncol. 42, 1 11.
33. Maltese W. A. Volpe J. J. (1979) Activation of 3-hydroxy-3- methylglutaryl-coenzyme A reductase in homogenates of developing rat brain. Biochem. J. 182, 367 370.
34. Marissen W. E. Lloyd R. E. (1998) Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol. Cell. Biol. 18, 7565 7574.
35. Marissen W. E., Gradi A., Sonenberg N. Lloyd R. E. (2000) Cleavage of eukaryotic translation initiation factor 4GII correlates with translation inhibition during apoptosis. Cell Death Differ. 7, 1234 1243.
36. Matthies H. Jr, Schulz S., Hollt V. Krug M. (1997) Inhibition by compactin demonstrates a requirement of isoprenoid metabolism for long-term potentiation in rat hippocampal slices. Neuroscience 79, 341 346.
37. Mauch D. H., Nagler K., Schumacher S., Goritz C., Muller E. C., Otto A. Pfrieger F. W. (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294, 1354 1357.
38. Mendez R. Richter J. D. (2001) Translational control by CPEB: a means to the end. Nat. Rev. Mol. Cell Biol. 2, 521 529.
39. Mendez R. Wells D. (2002) Location, location, location: translational control in development and neurobiology. Trends Cell Biol. 12, 407 409.
40. Michikawa M. Yanagisawa K. (1999) Inhibition of cholesterol production but not of nonsterol isoprenoid products induces neuronal cell death. J. Neurochem. 72, 2278 2285.
41. Montarolo P. G., Goelet P., Castellucci V. F., Morgan J., Kandel E. R. Schacher S. (1986) A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234, 1249 1254.
42. Morley S. J., Jeffrey I., Bushell M., Pain V. M. Clemens M. J. (2000) Differential requirements for caspase-B activity in the mechanism of phosphorylation of eIF2alpha, cleavage of eIF4GI and signalling events associated with inhibition of protein synthesis in apoptotic Jurkat T cells. FEBS Lett. 477, 229 236.
43. Morley S. J. Pain V. M. (2001) Proteasome inhibitors and immunosuppressive drugs promote the cleavage of eIF4GI and eIF4GII by caspase-8-independent mechanisms in Jurkat T cell lines. FEBS Lett. 503, 206 212.
44. Morley S. J., Coldwell M. J. Clemens M. J. (2005) Initiation factor modifications in the preapoptotic phase. Cell Death Differ. 12, 571 584.
45. Mosmann T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55 63.
46. Opitz J. M. de la Cruz F. (1994) Cholesterol metabolism in the RSH/Smith-Lemli-Opitz syndrome: summary of an NICHD conference. Am. J. Med. Genet. 50, 326 338.
47. Padayatty S. J., Marcelli M., Shao T. C. Cunningham G. R. (1997) Lovastatin-induced apoptosis in prostate stromal cells. J. Clin. Endocrinol. Metab. 82, 1434 1439.
48. Pause A., Belsham G. J., Gingras A. C., Donze O., Lin T. A., Lawrence J. C. Jr Sonenberg N. (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371, 762 767.
49. Perez-Sala D. Mollinedo F. (1994) Inhibition of isoprenoid biosynthesis induces apoptosis in human promyelocytic HL-60 cells. Biochem. Biophys. Res. Commun. 199, 1209 1215.
50. Pfeiffer B. E. Huber K. M. (2006) Current advances in local protein synthesis and synaptic plasticity. J. Neurosci. 26, 7147 7150.
51. Proud C. G. (2007) Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem. J. 403, 217 234.
52. Raiteri M., Arnaboldi L., McGeady P. et al. (1997) Pharmacological control of the mevalonate pathway: effect on arterial smooth muscle cell proliferation. J. Pharmacol. Exp. Ther. 281, 1144 1153.
53. Rochet J. C. (2006) Errors in translation cause selective neurodegeneration. ACS Chem. Biol. 1, 562 566.
54. Roux P. P., Shahbazian D., Vu H., Holz M. K., Cohen M. S., Taunton J., Sonenberg N. Blenis J. (2007) RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J. Biol. Chem. 282, 14056 14064.
55. Schulz J. G., Bosel J., Stoeckel M., Megow D., Dirnagl U. Endres M. (2004) HMG-CoA reductase inhibition causes neurite loss by interfering with geranylgeranyl pyrophosphate synthesis. J. Neurochem. 89, 24 32.
56. Spady D. K. Dietschy J. M. (1983) Sterol synthesis in vivo in 18 tissues of the squirrel monkey, guinea pig, rabbit, hamster, and rat. J. Lipid Res. 24, 303 315.
57. Sutton M. A. Schuman E. M. (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127, 49 58.
58. Tang S. J., Reis G., Kang H., Gingras A. C., Sonenberg N. Schuman E. M. (2002) A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc. Natl Acad. Sci. USA 99, 467 472.
59. Vgontzas A. N., Kales A., Bixler E. O., Manfredi R. L. Tyson K. L. (1991) Effects of lovastatin and pravastatin on sleep efficiency and sleep stages. Clin. Pharmacol. Ther. 50, 730 737.
60. Wolozin B. (2004) Cholesterol and the biology of Alzheimer's disease. Neuron 41, 7 10.
61. Zamora M., Marissen W. E. Lloyd R. E. (2002) Multiple eIF4GI-specific protease activities present in uninfected and poliovirus-infected cells. J. Virol. 76, 165 177.
62. Zheng J. Q., Kelly T. K., Chang B., Ryazantsev S., Rajasekaran A. K., Martin K. C. Twiss J. L. (2001) A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J. Neurosci. 21, 9291 9303.