Microtubules are required for NF-κB nuclear translocation in neuroblastoma IMR-32 cells: Modulation by zinc

Journal of Neurochemistry

Volumn 99, Issue 2, 2006, Pages 402-415

  Mackenzie, Gerardo G ^a,b   Keen, Carl L ^a   Oteiza, Patricia I ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Karyopherin ; Microtubules; Nervous system; NF B; Nuclear transport; Zinc deficiency

Indexed keywords

COLCHICINE; CYTOCHALASIN D; DYNEIN ADENOSINE TRIPHOSPHATASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KARYOPHERIN; PACLITAXEL; PROTEIN P50; TRANSCRIPTION FACTOR RELA; TUBULIN; VINBLASTINE; ZINC;

ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CELL TRANSPORT; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSKELETON; GENE CONTROL; GENE TRANSLOCATION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INHIBITION KINETICS; MICROTUBULE; MODULATION; MOLECULAR STABILITY; NERVE CELL; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN POLYMERIZATION; ZINC DEFICIENCY;

ACTINS; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANIMALS, NEWBORN; CELL LINE, TUMOR; CELL NUCLEUS; CELLS, CULTURED; HUMANS; MICROTUBULES; NEUROBLASTOMA; NEURONS; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; PRESYNAPTIC TERMINALS; PROTEIN BINDING; PROTEIN SYNTHESIS INHIBITORS; PROTEIN TRANSPORT; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION; TRANSCRIPTION FACTOR RELA; TUBULIN; TUBULIN MODULATORS; ZINC;

EID: 33749165927     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04005.x     Document Type: Article

References (57)

1. Albensi B. C. and Mattson M. P. (2000) Evidence for the involvement of TNF and NF-kappaB in hippocampal synaptic plasticity. Synapse 35, 151-159.
2. Baeuerle P. A. and Baltimore D. (1988) I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science 242, 540-546.
3. Ben-Ze'ev A. (1991) Animal cell shape changes and gene expression. Bioessays 13, 207-212.
4. Borodinsky L. N. and Fiszman M. L. (1998) Extracellular potassium concentration regulates proliferation of immature cerebellar granule cells. Brain Res. Dev Brain Res. 107, 43-48.
5. Bourgarel-Rey V., Vallee S., Rimet O., Champion S., Braguer D., Desobry A., Briand C. and Barra Y. (2001) Involvement of nuclear factor kappaB in c-Myc induction by tubulin polymerization inhibitors. Mol Pharmacol. 59, 1165-1170.
6. Chintala S. K., Sawaya R., Aggarwal B. B., Majumder S., Giri D. K., Kyritsis A. P., Gokaslan Z. L. and Rao J. S. (1998) Induction of matrix metalloproteinase-9 requires a polymerized actin cytoskeleton in human malignant glioma cells. J. Biol. Chem. 273, 13 545-13 551.
7. Cunningham M. D., Cleaveland J. and Nadler S. G. (2003) An intracellular targeted NLS peptide inhibitor of karyopherin alpha: NF-kappa B interactions. Biochem. Biophys. Res. Commun 300, 403-407.
8. Das K. C., Lewis-Molock Y. and White C. W. (1995) Thiol modulation of TNF alpha and IL-1 induced MnSOD gene expression and activation of NF-kappa B. Mol Cell Biochem. 148, 45-57.
9. Denis-Donini S., Caprini A., Frassoni C. and Grilli M. (2005) Members of the NF-kappaB family expressed in zones of active neurogenesis in the postnatal and adult mouse brain. Brain Res. Dev Brain Res. 154, 81-89.
10. Dennerll T. J., Joshi H. C., Steel V. L., Buxbaum R. E. and Heidemann S. R. (1988) Tension and compression in the cytoskeleton of PC-12 neurites. II: Quantitative measurements. J. Cell Biol. 107, 665-674.
11. Dignam J. D., Lebovitz. R. M. and Roeder R. G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucl Acids Res. 11, 1475-1489.
12. Erlejman A. G. and Oteiza P. I. (2002) The oxidant defense system in human neuroblastoma IMR-32 cells predifferentiation and postdifferentiation to neuronal phenotypes. Neurochem. Res. 27, 1499-1506.
13. Gallo V., Kingsbury A., Balazs R. and Jorgensen O. S. (1987) The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J. Neurosci. 7, 2203-2213.
14. Gisiger V. (1998) Regulation of gene expression by trans-synaptic activity: a role for the transcription factor NF-kappa B. J. Physiol. Paris 92, 163-166.
15. Gorlich D. and Laskey R. A. (1995) Roles of importin in nuclear protein import. Cold Spring Harb Symp Quant Biol. 60, 695-699.
16. Gorlich D. and Mattaj I. W. (1996) Nucleocytoplasmic transport. Science 271, 1513-1518.
17. Goslin K., Banker G. and Asmussen H. (1998) Rat Hippocampal Neurons in Low Density Cultures. MIT Press, Cambridge, MA.
18. Guerrini L., Blasi F. and Denis-Donini S. (1995) Synaptic activation of NF-kappa B by glutamate in cerebellar granule neurons in vitro. Proc. Natl Acad. Sci. U S A 92, 9077-9081.
19. Guzik B. W. and Goldstein L. S. (2004) Microtubule-dependent transport in neurons: steps towards an understanding of regulation, function and dysfunction. Curr. Opin. Cell Biol. 16, 443-450.
20. Hanz. S., Perlson E., Willis D, et al. (2003) Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40, 1095-1104.
21. Hwang S. and Ding A. (1995) Activation of NF-kappa B in murine macrophages by taxol. Cancer Biochem. Biophys. 14, 265-272.
22. Jans D. A., Xiao C. Y. and Lam M. H. (2000) Nuclear targeting signal recognition: a key control point in nuclear transport? Bioessays 22, 532-544.
23. Kaltschmidt C., Kaltschmidt B. and Baeuerle P. A. (1993) Brain synapses contain inducible forms of the transcription factor NF-kappa B. Mech Dev 43, 135-147.
24. Kaltschmidt C., Kaltschmidt B. and Baeuerle P. A. (1995) Stimulation of ionotropic glutamate receptors activates transcription factor NF-kappa B in primary neurons. Proc. Natl Acad. Sci. U S A 92, 9618-9622.
25. Karin M. (1999) How NF-kappaB is activated: the role of the IkappaB kinase (IKK) complex. Oncogene 18, 6867-6874.
26. Kovacs A. D., Chakraborty-Sett S., RamireZ. S. H., Sniderhan L. F., Williamson A. L. and Maggirwar S. B. (2004) Mechanism of NF-kappaB inactivation induced by survival signal withdrawal in cerebellar granule neurons. Eur J. Neurosci. 20, 345-352.
27. Lam M. H., Thomas R. J., Loveland K. L., Schilders S., Gu M., Martin T. J., Gillespie M. T. and Jans D. A. (2002) Nuclear transport of parathyroid hormone (PTH)-related protein is dependent on microtubules. Mol Endocrinol. 16, 390-401.
28. Lee H. H., Dadgostar H., Cheng Q., Shu J. and Cheng G. (1999) NFkappaB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc. Natl Acad. Sci. U S A 96, 9136-9141.
29. Lilienbaum A. and Israel A. (2003) From calcium to NF-kappa B signaling pathways in neurons. Mol Cell Biol. 23, 2680-2698.
30. Mackenzie G. G., Zago M. P., Erlejman A. G., Aimo L., Keen C. L. and Oteiza P. I. (2006) alpha-Lipoic acid and N-acetyl cysteine prevent zinc deficiency-induced activation of NF-kappaB and AP-1 transcription factors in human neuroblastoma IMR-32 cells. Free Radic Res. 40, 75-84.
31. Mackenzie G. G., Zago M. P., Keen C. L. and Oteiza P. I. (2002) Low intracellular zinc impairs the translocation of activated NF-kappa B to the nuclei in human neuroblastoma IMR-32 cells. J. Biol. Chem. 277, 34 610-34 617.
32. Marelli M., Dilworth D. J., Wozniak R. W. and Aitchison J. D. (2001) The dynamics of karyopherin-mediated nuclear transport. Biochem. Cell Biol. 79, 603-612.
33. Mattson M. P., Culmsee C., YuZ. and Camandola S. (2000) Roles of nuclear factor kappaB in neuronal survival and plasticity. J. Neurochem. 74, 443-456.
34. Mavlyutov T. A., Cai Y. and Ferreira P. A. (2002) Identification of RanBP2- and kinesin-mediated transport pathways with restricted neuronal and subcellular localization. Traffic 3, 630-640.
35. Meberg P. J., Kinney W. R., Valcourt E. G. and Routtenberg A. (1996) Gene expression of the transcription factor NF-kappa B in hippocampus: regulation by synaptic activity. Brain Res. Mol Brain Res. 38, 179-190.
36. Meffert M. K., Chang J. M., Wiltgen B. J., Fanselow M. S. and Baltimore D. (2003) NF-kappaB functions in synaptic signaling and behavior. Nat Neurosci.
37. Muller J. M., Rupec R. A. and Baeuerle P. A. (1997) Study of gene regulation by NF-kappa B and AP-1 in response to reactive oxygen intermediates. Methods 11, 301-312.
38. Neill D., Hughes D., Edwardson J. A., Rima B. K. and Allsop D. (1994) Human IMR-32 neuroblastoma cells as a model cell line in Alzheimer's disease research. J. Neurosci. Res. 39, 482-493.
39. O'Neill L. A. and Kaltschmidt C. (1997) NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci. 20, 252-258.
40. Osborn L., Kunkel S. and Nabel G. J. (1989) Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B. Proc. Natl Acad. Sci. U S A 86, 2336-2340.
41. Oteiza P. I., Clegg M. S., Zago M. P. and Keen C. L. (2000) Zinc deficiency induces oxidative stress and AP-1 activation in 3T3 cells. Free Radic Biol. Med. 28, 1091-1099.
42. Oteiza P. I., Cuellar S., Lonnerdal B., Hurley L. S. and Keen C. L. (1990) Influence of maternal dietary zinc intake on in vitro tubulin polymerization in fetal rat brain. Teratology 41, 97-104.
43. Oteiza P. I., Hurley L. S., Lonnerdal B. and Keen C. L. (1988) Marginal zinc deficiency affects maternal brain microtubule assembly in rats. J. Nutr 118, 735-738.
44. Oteiza P. I., Hurley L. S., Lonnerdal B. and Keen C. L. (1990) Effects of marginal zinc deficiency on microtubule polymerization in the developing rat brain. Biol. Trace Elem Res. 24, 13-23.
45. Pahl H. L. (1999) Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18, 6853-6866.
46. Piccioli P., Porcile C., Stanzione S., Bisaglia M., Bajetto A., Bonavia R., Florio T. and Schettini G. (2001) Inhibition of nuclear factor-kappaB activation induces apoptosis in cerebellar granule cells. J. Neurosci. Res. 66, 1064-1073.
47. Rosette C. and Karin M. (1995) Cytoskeletal control of gene expression: depolymerization of microtubules activates NF-kappa B. J. Cell Biol. 128, 1111-1119.
48. Routtenberg A. and Meberg P. M. (1998) A novel signaling system from the synapse to the nucleus. Trends Neurosci. 21, 106.
49. Sen R. and Baltimore D. (1986) Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell 46, 705-716.
50. Smith H. M. and Raikhel N. V. (1998) Nuclear localization signal receptor importin alpha associates with the cytoskeleton. Plant Cell 10, 1791-1799.
51. Taglialatela G., Kaufmann J. A., Trevino A. and Perez-Polo J. R. (1998) Central nervous system DNA fragmentation induced by the inhibition of nuclear factor kappa B. Neuroreport 9, 489-493.
52. Ten R. M., Paya C. V., Israel N., Le Bail O., Mattei M. G., Virelizier J. L., Kourilsky P. and Israel A. (1992) The characterization of the promoter of the gene encoding the p50 subunit of NF-kappa B indicates that it participates in its own regulation. EMBO J. 11, 195-203.
53. Vigorito E., Billadeu D. D., Savoy D., McAdam S., Doody G., Fort P. and Turner M. (2003) RhoG regulates gene expression and the actin cytoskeleton in lymphocytes. Oncogene 22, 330-342.
54. Wang Y., Chan S. L., Miele L., Yao P. J., Mackes J., Ingram D. K., Mattson M. P. and Furukawa K. (2004) Involvement of Notch signaling in hippocampal synaptic plasticity. Proc. Natl Acad. Sci. U S A 101, 9458-9462.
55. Wellmann H., Kaltschmidt B. and Kaltschmidt C. (2001) Retrograde transport of transcription factor NF-kappa B in living neurons. J. Biol. Chem. 276, 11 821-11 829.
56. West A. E., Griffith E. C. and Greenberg M. E. (2002) Regulation of transcription factors by neuronal activity. Nat Rev. Neurosci. 3, 921-931.
57. Yu Z., Zhou D., Bruce-Keller A. J., Kindy M. S. and Mattson M. P. (1999) Lack of the p50 subunit of nuclear factor-kappaB increases the vulnerability of hippocampal neurons to excitotoxic injury. J. Neurosci. 19, 8856-8865.