Cytoskeletal control of gene expression: depolymerization of microtubules activates NF-kappa B

This Article

	Full Text (PDF, 1844K)
	Alert me when this article is cited

Services

	Email this article
	Similar articles in this journal
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Rosette, C
	Articles by Karin, M
	Search for Related Content

PubMed

	Articles by Rosette, C
	Articles by Karin, M

Social Bookmarking

	What's this?

ARTICLES

Cytoskeletal control of gene expression: depolymerization of microtubules activates NF-kappa B

C Rosette and M Karin
Department of Pharmacology, School of Medicine, University of California at San Diego, La Jolla 92093-0636.

Cell shape changes exert specific effects on gene expression. It has been speculated that the cytoskeleton is responsible for converting changes in the cytoarchitecture to effects on gene transcription. However, the signal transduction pathways responsible for cytoskeletal- nuclear communication remained unknown. We now provide evidence that a variety of agents and conditions that depolymerize microtubules activate the sequence-specific transcription factor NF-kappa B and induce NF kappa B-dependent gene expression. These effects are caused by depolymerization of microtubule because they are blocked by the microtubule-stabilizing agent taxol. In nonstimulated cells, the majority of NF-kappa B resides in the cytosplasm as a complex with its inhibitor I kappa B. Upon cell stimulation, NF-kappa B translocates to the nucleus with concomitant degradation of I kappa B. We show that cold-induced depolymerization of microtubules also leads to I kappa B degradation and activation of NF-kappa B. However, the activated factor remains in the cytoplasm and translocates to the nucleus only upon warming to 37 degrees C, thus revealing two distinct steps in NF-kappa B activation. These findings establish a new role for NF-kappa B in sensing changes in the state of the cytoskeleton and converting them to changes in gene activity.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Vartanian, K. B., Berny, M. A., McCarty, O. J. T., Hanson, S. R., Hinds, M. T. (2010). Cytoskeletal structure regulates endothelial cell immunogenicity independent of fluid shear stress. Am. J. Physiol. Cell Physiol. 298: C333-C341 [Abstract] [Full Text]
Banerjee, A., Rose, R., Johnson, G. A., Burghardt, R. C., Ramaiah, S. K. (2009). The Influence of Estrogen on Hepatobiliary Osteopontin (SPP1) Expression in a Female Rodent Model of Alcoholic Steatohepatitis. Toxicol Pathol 37: 492-501 [Abstract] [Full Text]
Shrum, C. K., DeFrancisco, D., Meffert, M. K. (2009). Stimulated nuclear translocation of NF-{kappa}B and shuttling differentially depend on dynein and the dynactin complex. Proc. Natl. Acad. Sci. USA 106: 2647-2652 [Abstract] [Full Text]
Seng, S., Avraham, H. K., Jiang, S., Yang, S., Sekine, M., Kimelman, N., Li, H., Avraham, S. (2007). The Nuclear Matrix Protein, NRP/B, Enhances Nrf2-Mediated Oxidative Stress Responses in Breast Cancer Cells. Cancer Res. 67: 8596-8604 [Abstract] [Full Text]
Izzo, J. G., Malhotra, U., Wu, T.-T., Luthra, R., Correa, A. M., Swisher, S. G., Hofstetter, W., Chao, K.S. C., Hung, M.-C., Ajani, J. A. (2007). Clinical Biology of Esophageal Adenocarcinoma after Surgery Is Influenced by Nuclear Factor-{kappa}B Expression. Cancer Epidemiol. Biomarkers Prev. 16: 1200-1205 [Abstract] [Full Text]
Fazal, F., Minhajuddin, M., Bijli, K. M., McGrath, J. L., Rahman, A. (2007). Evidence for Actin Cytoskeleton-dependent and -independent Pathways for RelA/p65 Nuclear Translocation in Endothelial Cells. J. Biol. Chem. 282: 3940-3950 [Abstract] [Full Text]
Seng, S., Avraham, H. K., Jiang, S., Venkatesh, S., Avraham, S. (2006). KLHL1/MRP2 Mediates Neurite Outgrowth in a Glycogen Synthase Kinase 3{beta}-Dependent Manner. Mol. Cell. Biol. 26: 8371-8384 [Abstract] [Full Text]
Manavathi, B., Acconcia, F., Rayala, S. K., Kumar, R. (2006). An inherent role of microtubule network in the action of nuclear receptor. Proc. Natl. Acad. Sci. USA 103: 15981-15986 [Abstract] [Full Text]
Gastaldi, T., Bonvini, P., Sartori, F., Marrone, A., Iolascon, A., Rosolen, A. (2006). Plakoglobin is differentially expressed in alveolar and embryonal rhabdomyosarcoma and is regulated by DNA methylation and histone acetylation. Carcinogenesis 27: 1758-1767 [Abstract] [Full Text]
Chaqour, B., Yang, R., Sha, Q. (2006). Mechanical Stretch Modulates the Promoter Activity of the Profibrotic Factor CCN2 through Increased Actin Polymerization and NF-{kappa}B Activation. J. Biol. Chem. 281: 20608-20622 [Abstract] [Full Text]
Rached, E., Pfeiffer, E., Dekant, W., Mally, A. (2006). Ochratoxin A: Apoptosis and Aberrant Exit from Mitosis due to Perturbation of Microtubule Dynamics?. Toxicol Sci 92: 78-86 [Abstract] [Full Text]
Izzo, J. G., Malhotra, U., Wu, T.-T., Ensor, J., Luthra, R., Lee, J. H., Swisher, S. G., Liao, Z., Chao, K.S. C., Hittelman, W. N., Aggarwal, B. B., Ajani, J. A. (2006). Association of Activated Transcription Factor Nuclear Factor {kappa}B With Chemoradiation Resistance and Poor Outcome in Esophageal Carcinoma. JCO 24: 748-754 [Abstract] [Full Text]
Mizumoto, N., Gao, J., Matsushima, H., Ogawa, Y., Tanaka, H., Takashima, A. (2005). Discovery of novel immunostimulants by dendritic-cell-based functional screening. Blood 106: 3082-3089 [Abstract] [Full Text]
Huang, Y.-C. T., Li, Z., Brighton, L. E., Carson, J. L., Becker, S., Soukup, J. M. (2005). 3-Nitrotyrosine attenuates respiratory syncytial virus infection in human bronchial epithelial cell line. Am. J. Physiol. Lung Cell. Mol. Physiol. 288: L988-L996 [Abstract] [Full Text]
Ghisletti, S., Meda, C., Maggi, A., Vegeto, E. (2005). 17{beta}-Estradiol Inhibits Inflammatory Gene Expression by Controlling NF-{kappa}B Intracellular Localization. Mol. Cell. Biol. 25: 2957-2968 [Abstract] [Full Text]
Phung-Koskas, T., Pilon, A., Pous, C., Betzina, C., Sturm, M., Bourguet-Kondracki, M.-L., Durand, G., Drechou, A. (2005). STAT5B-mediated Growth Hormone Signaling Is Organized by Highly Dynamic Microtubules in Hepatic Cells. J. Biol. Chem. 280: 1123-1131 [Abstract] [Full Text]
Bonvini, P., Rosa, H. D., Vignes, N., Rosolen, A. (2004). Ubiquitination and Proteasomal Degradation of Nucleophosmin-Anaplastic Lymphoma Kinase Induced by 17-Allylamino-Demethoxygeldanamycin: Role of the Co-Chaperone Carboxyl Heat Shock Protein 70-Interacting Protein. Cancer Res. 64: 3256-3264 [Abstract] [Full Text]
Zoubiane, G. S., Valentijn, A., Lowe, E. T., Akhtar, N., Bagley, S., Gilmore, A. P., Streuli, C. H. (2004). A role for the cytoskeleton in prolactin-dependent mammary epithelial cell differentiation. J. Cell Sci. 117: 271-280 [Abstract] [Full Text]
Mistry, P., Deacon, K., Mistry, S., Blank, J., Patel, R. (2004). NF-{kappa}B Promotes Survival during Mitotic Cell Cycle Arrest. J. Biol. Chem. 279: 1482-1490 [Abstract] [Full Text]
Ott, C., Iwanciw, D., Graness, A., Giehl, K., Goppelt-Struebe, M. (2003). Modulation of the Expression of Connective Tissue Growth Factor by Alterations of the Cytoskeleton. J. Biol. Chem. 278: 44305-44311 [Abstract] [Full Text]
Jung, Y.-J., Isaacs, J. S., Lee, S., Trepel, J., Neckers, L. (2003). Microtubule Disruption Utilizes an NFkappa B-dependent Pathway to Stabilize HIF-1alpha Protein. J. Biol. Chem. 278: 7445-7452 [Abstract] [Full Text]
Mackenzie, G. G., Zago, M. P., Keen, C. L., 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: 34610-34617 [Abstract] [Full Text]
Algul, H., Tando, Y., Beil, M., Weber, C. K., Von Weyhern, C., Schneider, G., Adler, G., Schmid, R. M. (2002). Different modes of NF-kappa B/Rel activation in pancreatic lobules. Am. J. Physiol. Gastrointest. Liver Physiol. 283: G270-G281 [Abstract] [Full Text]
Michaelson, J. E., Ritzenthaler, J. D., Roman, J. (2002). Regulation of serum-induced fibronectin expression by protein kinases, cytoskeletal integrity, and CREB. Am. J. Physiol. Lung Cell. Mol. Physiol. 282: L291-L301 [Abstract] [Full Text]
Yasuda, S., Noguchi, T., Gohda, M., Arai, T., Tsutsui, N., Nakayama, Y., Matsuda, T., Nonogi, H. (2002). Local delivery of low-dose docetaxel, a novel microtubule polymerizing agent, reduces neointimal hyperplasia in a balloon-injured rabbit iliac artery model. Cardiovasc Res 53: 481-486 [Abstract] [Full Text]
Ye, R. D. (2001). Regulation of nuclear factor {kappa}B activation by G-protein-coupled receptors. J. Leukoc. Biol. 70: 839-848 [Abstract] [Full Text]
Inada, H., Izawa, I., Nishizawa, M., Fujita, E., Kiyono, T., Takahashi, T., Momoi, T., Inagaki, M. (2001). Keratin attenuates tumor necrosis factor-induced cytotoxicity through association with TRADD. JCB 155: 415-426 [Abstract] [Full Text]
Liao, C.-L., Lin, Y.-L., Wu, B.-C., Tsao, C.-H., Wang, M.-C., Liu, C.-I, Huang, Y.-L., Chen, J.-H., Wang, J.-P., Chen, L.-K. (2001). Salicylates Inhibit Flavivirus Replication Independently of Blocking Nuclear Factor Kappa B Activation. J. Virol. 75: 7828-7839 [Abstract] [Full Text]
Shmueli, O., Gdalyahu, A., Sorokina, K., Nevo, E., Avivi, A., Reiner, O. (2001). DCX in PC12 cells: CREB-mediated transcription and neurite outgrowth. Hum Mol Genet 10: 1061-1070 [Abstract] [Full Text]
Bourgarel-Rey, V., Vallee, S., Rimet, O., Champion, S., Braguer, D., Desobry, A., Briand, C., Barra, Y. (2001). Involvement of Nuclear Factor kappa B in c-Myc Induction by Tubulin Polymerization Inhibitors. Mol. Pharmacol. 59: 1165-1170 [Abstract] [Full Text]
Iacobelli, M., Wachsman, W., McGuire, K. L. (2000). Repression of IL-2 Promoter Activity by the Novel Basic Leucine Zipper p21SNFT Protein. J. Immunol. 165: 860-868 [Abstract] [Full Text]
Zhao, L., Gregoire, F., Sook Sul, H. (2000). Transient Induction of ENC-1, a Kelch-related Actin-binding Protein, Is Required for Adipocyte Differentiation. J. Biol. Chem. 275: 16845-16850 [Abstract] [Full Text]
Xia, Y., Makris, C., Su, B., Li, E., Yang, J., Nemerow, G. R., Karin, M. (2000). MEK kinase 1 is critically required for c-Jun N-terminal kinase activation by proinflammatory stimuli and growth factor-induced cell migration. Proc. Natl. Acad. Sci. USA 97: 5243-5248 [Abstract] [Full Text]
Harwood, F. G., Kasibhatla, S., Petak, I., Vernes, R., Green, D. R., Houghton, J. A. (2000). Regulation of FasL by NF-kappa B and AP-1 in Fas-dependent Thymineless Death of Human Colon Carcinoma Cells. J. Biol. Chem. 275: 10023-10029 [Abstract] [Full Text]
Guiet, C., Vito, P. (2000). Caspase Recruitment Domain (Card-Dependent) Cytoplasmic Filaments Mediate Bcl10-Induced Nf-{kappa}b Activation. JCB 148: 1131-1140 [Abstract] [Full Text]
Cook, J. R., Mody, M. K., Fini, M. E. (1999). Failure to Activate Transcription Factor NF-{kappa}B in Corneal Stromal Cells (Keratocytes). IOVS 40: 3122-3131 [Abstract] [Full Text]
Soltysik-Espanola, M., Rogers, R. A., Jiang, S., Kim, T.-A., Gaedigk, R., White, R. A., Avraham, H., Avraham, S. (1999). Characterization of Mayven, a Novel Actin-binding Protein Predominantly Expressed in Brain. Mol. Biol. Cell 10: 2361-2375 [Abstract] [Full Text]
Yujiri, T., Fanger, G. R., Garrington, T. P., Schlesinger, T. K., Gibson, S., Johnson, G. L. (1999). MEK Kinase 1�(MEKK1) Transduces c-Jun NH2-terminal Kinase Activation in Response to Changes in the Microtubule Cytoskeleton. J. Biol. Chem. 274: 12605-12610 [Abstract] [Full Text]
Oren, A., Herschkovitz, A., Ben-Dror, I., Holdengreber, V., Ben-Shaul, Y., Seger, R., Vardimon, L. (1999). The Cytoskeletal Network Controls c-Jun Expression and Glucocorticoid Receptor Transcriptional Activity in an Antagonistic and Cell-Type-Specific Manner. Mol. Cell. Biol. 19: 1742-1750 [Abstract] [Full Text]
Odde, D., Ma, L, Briggs, A., DeMarco, A, Kirschner, M. (1999). Microtubule bending and breaking in living fibroblast cells. J. Cell Sci. 112: 3283-3288 [Abstract]
Kasibhatla, S., Genestier, L., Green, D. R. (1999). Regulation of Fas-Ligand Expression during Activation-induced Cell Death in T Lymphocytes via Nuclear Factor kappa B. J. Biol. Chem. 274: 987-992 [Abstract] [Full Text]
Yang, Y, Relan, N., Przywara, D., Schuger, L (1999). Embryonic mesenchymal cells share the potential for smooth muscle differentiation: myogenesis is controlled by the cell's shape. Development 126: 3027-3033 [Abstract]
Norman, D. A.M., Yacoub, M. H., Barton, P. J.R. (1998). Nuclear factor NF-{kappa}B in myocardium: developmental expression of subunits and activation by interleukin-1{beta} in cardiac myocytes in vitro. Cardiovasc Res 39: 434-441 [Abstract] [Full Text]
JANMEY, P. A. (1998). The Cytoskeleton and Cell Signaling: Component Localization and Mechanical Coupling. Physiol. Rev. 78: 763-781 [Abstract] [Full Text]
Kessel, J. M., Hayflick, J., Weyrich, A. S., Hoffman, P. A., Gallatin, M., McIntyre, T. M., Prescott, S. M., Zimmerman, G. A. (1998). Coengagement of ICAM-3 and Fc Receptors Induces Chemokine Secretion and Spreading by Myeloid Leukocytes. J. Immunol. 160: 5579-5587 [Abstract] [Full Text]
Schmid-Alliana, A., Menou, L., Manie, S., Schmid-Antomarchi, H., Millet, M.-A., Giuriato, S., Ferrua, B., Rossi, B. (1998). Microtubule Integrity Regulates Src-like and Extracellular Signal-regulated Kinase Activities in Human Pro-monocytic Cells. IMPORTANCE FOR INTERLEUKIN-1 PRODUCTION. J. Biol. Chem. 273: 3394-3400 [Abstract] [Full Text]
Putnam, A., Cunningham, J., Dennis, R., Linderman, J., Mooney, D. (1998). Microtubule assembly is regulated by externally applied strain in cultured smooth muscle cells. J. Cell Sci. 111: 3379-3387 [Abstract]
Savkovic, S. D., Koutsouris, A., Hecht, G. (1997). Activation of NF-kappa B in intestinal epithelial cells by enteropathogenic Escherichia coli. Am. J. Physiol. Cell Physiol. 273: C1160-C1167 [Abstract] [Full Text]
Axel, D. I., Kunert, W., Goggelmann, C., Oberhoff, M., Herdeg, C., Kuttner, A., Wild, D. H., Brehm, B. R., Riessen, R., Koveker, G., Karsch, K. R. (1997). Paclitaxel Inhibits Arterial Smooth Muscle Cell Proliferation and Migration In Vitro and In Vivo Using Local Drug Delivery. Circulation 96: 636-645 [Abstract] [Full Text]
Das, K. C., White, C. W. (1997). Activation of NF-kappa B by Antineoplastic Agents. ROLE OF PROTEIN KINASE C. J. Biol. Chem. 272: 14914-14920 [Abstract] [Full Text]
Hernandez, M.-C., Andres-Barquin, P. J., Martinez, S., Bulfone, A., Rubenstein, J. L.R., Israel, M. A. (1997). ENC-1: A Novel Mammalian Kelch-Related Gene Specifically Expressed in the Nervous System Encodes an Actin-Binding Protein. J. Neurosci. 17: 3038-3051 [Abstract] [Full Text]
Canman, J., Bement, W. (1997). Microtubules suppress actomyosin-based cortical flow in Xenopus oocytes. J. Cell Sci. 110: 1907-1917 [Abstract]
Seveau, S, Lopez, S, Lesavre, P, Guichard, J, Cramer, E., Halbwachs-Mecarelli, L (1997). Leukosialin (CD43, sialophorin) redistribution in uropods of polarized neutrophils is induced by CD43 cross-linking by antibodies, by colchicine or by chemotactic peptides. J. Cell Sci. 110: 1465-1475 [Abstract]
Schmalz, D, Kalkbrenner, F, Hucho, F, Buchner, K (1996). Transport of protein kinase C alpha into the nucleus requires intact cytoskeleton while the transport of a protein containing a canonical nuclear localization signal does not. J. Cell Sci. 109: 2401-2406 [Abstract]