IKAP localizes to membrane ruffles with filamin A and regulates actin cytoskeleton organization and cell migration

Journal of Cell Science

Volumn 121, Issue 6, 2008, Pages 854-864

  Johansen, Lars Dan ^a   Naumanen, Tiina ^a   Knudsen, Astrid ^a   Westerlund, Nina ^b   Gromova, Irina ^c   Junttila, Melissa ^b   Nielsen, Christina ^a   Bøttzauw, Trine ^a   Tolkovsky, Aviva ^d   Westermarck, Jukka ^b,e   Coffey, Eleanor T ^b   Jäättelä, Marja ^a   Kallunki, Tuula ^a  

^a Institute of Biology   (Denmark)

^b UNIVERSITY OF TURKU   (Finland)

^c DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF TAMPERE   (Finland)

Author keywords

Beclin 1; ELP1; Familial dysautonomia; Neuronal migration; Paxillin

Indexed keywords

ACTIN; BECLIN 1; FILAMIN A; I KAPPA B KINASE; PAXILLIN;

AMINO ACID SEQUENCE; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL TYPE; CONTROLLED STUDY; CYTOSKELETON; CYTOSOL; DOWN REGULATION; DYSAUTONOMIA; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; NERVE CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; RNA INTERFERENCE; WILD TYPE;

ANIMALS; CARRIER PROTEINS; CELL ADHESION; CELL MOVEMENT; CELL SURFACE EXTENSIONS; CELLS, CULTURED; CEREBELLUM; CONTRACTILE PROTEINS; CYTOSOL; HUMANS; MICE; MICROFILAMENT PROTEINS; MUTATION; NEURONS; PAXILLIN; RATS; RNA INTERFERENCE; STRESS FIBERS; VINCULIN;

RATTUS;

EID: 42549137421     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.013722     Document Type: Article

References (39)

1. Abassi, Y. A., Rehn, M., Ekman, N., Alitalo, K. and Vuori, K. (2003). p130Cas Couples the tyrosine kinase Bmx/Etk with regulation of the actin cytoskeleton and cell migration. J. Biol. Chem. 278, 35636-35643.
2. Anderson, S. L., Coli, R., Daly, I. W., Kichula, E. A., Rork, M. J., Volpi, S. A., Ekstein, J. and Rubin, B. Y. (2001). Familial dysautonomia is caused by mutations of the IKAP gene. Am. J. Hum. Genet. 68, 753-758.
3. Axelrod, F. B. (2004). Familial dysautonomia. Muscle Nerve 29, 352-363.
4. Celis, J. E., Gromov, P., Cabezon, T., Moreira, J. M., Ambartsumian, N., Sandelin, K., Rank, F. and Gromova, I. (2004). Proteomic characterization of the interstitial fluid perfusing the breast tumor microenvironment: a novel resource for biomarker and therapeutic target discovery. Mol. Cell. Proteomics 3, 327-344.
5. Cheishvili, D., Maayan, C., Smith, Y., Ast, G. and Razin, A. (2007). IKAP/hELP1 deficiency in the cerebrum of familial dysautonomia patients results in down regulation of genes involved in oligodendrocyte differentiation and in myelination. Hum. Mol. Genet. 16, 2097-2104.
6. Close, P., Hawkes, N., Cornez, I., Creppe, C., Lambert, C. A., Rogister, B., Siebenlist, U., Merville, M. P., Slaugenhaupt, S. A., Bours, V. et al. (2006). Transcription impairment and cell migration defects in elongator-depleted cells: implication for familial dysautonomia. Mol. Cell 22, 521-531.
7. Coffey, E. T., Hongisto, V., Dickens, M., Davis, R. J. and Courtney, M. J. (2000). Dual roles for c-Jun N-terminal kinase in developmental and stress responses in cerebellar granule neurons. J. Neurosci. 20, 7602-7613.
8. Cohen, L., Henzel, W. J. and Baeuerle, P. A. (1998). IKAP is a scaffold protein of the IkappaB kinase complex. Nature 395, 292-296.
9. Collum, R. G., Brutsaert, S., Lee, G. and Schindler, C. (2000). A Stat3-interacting protein (StIP1) regulates cytokine signal transduction. Proc. Natl. Acad. Sci. USA 97, 10120-10125.
10. Cuajungco, M. P., Leyne, M., Mull, J., Gill, S. P., Lu, W., Zagzag, D., Axelrod, F. B., Maayan, C., Gusella, J. F. and Slaugenhaupt, S. A. (2003). Tissue-specific reduction in splicing efficiency of IKBKAP due to the major mutation associated with familial dysautonomia. Am. J. Hum. Genet. 72, 749-758.
11. Cunningham, C. C., Gorlin, J. B., Kwiatkowski, D. J., Hartwig, J. H., Janmey, P. A., Byers, H. R. and Stossel, T. P. (1992). Actin-binding protein requirement for cortical stability and efficient locomotion. Science 255, 325-327.
12. Dietrich, N., Thastrup, J., Holmberg, C., Gyrd-Hansen, M., Fehrenbacher, N., Lademann, U., Lerdrup, M., Herdegen, T., Jaattela, M. and Kallunki, T. (2004). JNK2 mediates TNF-induced cell death in mouse embryonic fibroblasts via regulation of both caspase and cathepsin protease pathways. Cell Death Differ. 11, 301-313.
13. Dujardin, D. L., Barnhart, L. E., Stehman, S. A., Gomes, E. R., Gundersen, G. G. and Vallee, R. B. (2003). A role for cytoplasmic dynein and LIS1 in directed cell movement. J. Cell Biol. 163, 1205-1211.
14. Esberg, A., Huang, B., Johansson, M. J. and Bystrom, A. S. (2006). Elevated levels of two tRNA species bypass the requirement for elongator complex in transcription and exocytosis. Mol. Cell 24, 139-148.
15. Fann, M. J. and Patterson, P. H. (1993). A novel approach to screen for cytokine effects on neuronal gene expression. J. Neurochem. 61, 1349-1355.
16. Fehrenbacher, N., Gyrd-Hansen, M., Poulsen, B., Felbor, U., Kallunki, T., Boes, M., Weber, E., Leist, M. and Jaattela, M. (2004). Sensitization to the lysosomal cell death pathway upon immortalization and transformation. Cancer Res. 64, 5301-5310.
17. Feng, Y. and Walsh, C. A. (2004). The many faces of filamin: a versatile molecular scaffold for cell motility and signalling. Nat. Cell Biol. 6, 1034-1038.
18. Fox, J. W., Lamperti, E. D., Eksioglu, Y. Z., Hong, S. E., Feng, Y., Graham, D. A., Scheffer, I. E., Dobyns, W. B., Hirsch, B. A., Radtke, R. A. et al. (1998). Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron 21, 1315-1325.
19. Friocourt, G., Kappeler, C., Saillour, Y., Fauchereau, F., Rodriguez, M. S., Bahi, N., Vinet, M. C., Chafey, P., Poirier, K., Taya, S. et al. (2005). Doublecortin interacts with the ubiquitin protease DFFRX, which associates with microtubules in neuronal processes. Mol. Cell. Neurosci. 28, 153-164.
20. Habecker, B. A., Asmus, S. A., Francis, N. and Landis, S. C. (1997). Target regulation of VIP expression in sympathetic neurons. Ann. N. Y. Acad. Sci. 814, 198-208.
21. Hatten, M. E. (1990). Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci. 13, 179-184.
22. Hawkes, N. A., Otero, G., Winkler, G. S., Marshall, N., Dahmus, M. E., Krappmann, D., Scheidereit, C., Thomas, C. L., Schiavo, G., Erdjument-Bromage, H. et al. (2002). Purification and characterization of the human elongator complex. J. Biol. Chem. 277, 3047-3052.
23. Hims, M. M., Shetty, R. J., Pickel, J., Mull, J., Leyne, M., Liu, L., Gusella, J. F. and Slaugenhaupt, S. A. (2007). A humanized IKBKAP transgenic mouse models a tissue-specific human splicing defect. Genomics 90, 389-396.
24. Holmberg, C., Katz, S., Lerdrup, M., Herdegen, T., Jaattela, M., Aronheim, A. and Kallunki, T. (2002). A novel specific role for I kappa B kinase complex-associated protein in cytosolic stress signaling. J. Biol. Chem. 277, 31918-31928.
25. Junttila, M. R., Saarinen, S., Schmidt, T., Kast, J. and Westermarck, J. (2005). Single-step Strep-tag purification for the isolation and identification of protein complexes from mammalian cells. Proteomics 5, 1199-1203.
26. Kiema, T., Lad, Y., Jiang, P., Oxley, C. L., Baldassarre, M., Wegener, K. L., Campbell, I. D., Ylänne, J. and Calderwood, D. A. (2006). The molecular basis of filamin binding to integrins and competition with talin. Mol. Cell 21, 337-347.
27. Krogan, J. N., Kim, M., Ahn, S. H., Zhong, G., Kobor, M. S., Cagney, G., Emili, A., Shilatifard, A., Buratowski, S. and Greenblatt, J. F. (2002). RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol. Cell. Biol. 22, 6979-6992.
28. Leonardi, A., Ellinger-Ziegelbauer, H., Franzoso, G., Brown, K. and Siebenlist, U. (2000). Physical and functional interaction of filamin (actin-binding protein-280) and tumor necrosis factor receptor-associated factor 2. J. Biol. Chem. 275, 271-278.
29. Otero, G., Fellows, J., Li, Y., de Bizemont, T., Dirac, A. M., Gustafsson, C. M., Erdjument-Bromage, H., Tempst, P. and Svejstrup, J. Q. (1999). Elongator, a multisubunit component of a novel RNA polymerase II holoenzyme for transcriptional elongation. Mol. Cell 3, 109-118.
30. Pokholok, D. K., Hannett, N. M. and Young, R. A. (2002). Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol. Cell 9, 799-809.
31. Popowicz, G. M., Schleicher, M., Noegel, A. A. and Holak, T. A. (2006). Filamins: promiscuous organizers of the cytoskeleton. Trends Biochem. Sci. 31, 411-419.
32. Rahl, P. B., Chen, C. Z. and Collins, R. N. (2005). Elp1p, the yeast homolog of the FD disease syndrome protein, negatively regulates exocytosis independently of transcriptional elongation. Mol. Cell 17, 841-853.
33. Rakic, P., Stensas, L. J., Sayre, E. and Sidman, R. L. (1974). Computer-aided three-dimensional reconstruction and quantitative analysis of cells from serial electron microscopic montages of foetal monkey brain. Nature 250, 31-34.
34. Sasaki, S., Shionoya, A., Ishida, M., Gambello, M. J., Yingling, J., Wynshaw-Boris, A. and Hirotsune, S. (2000). ALIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28, 681-696.
35. Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
36. Slaugenhaupt, S. A., Blumenfeld, A., Gill, S. P., Leyne, M., Mull, J., Cuajungco, M. P., Liebert, C. B., Chadwick, B., Idelson, M., Reznik, L. et al. (2001). Tissue-specific expression of a splicing mutation in the IKBKAP gene causes familial dysautonomia. Am. J. Hum. Genet. 68, 598-605.
37. Slaugenhaupt, S. A., Mull, J., Leyne, M., Cuajungco, M. P., Gill, S. P., Hims, M. M., Quintero, F., Axelrod, F. B. and Gusella, J. F. (2004). Rescue of a human mRNA splicing defect by the plant cytokinin kinetin. Hum. Mol. Genet. 13, 429-436.
38. Vadlamudi, R. K., Li, F., Adam, L., Nguyen, D., Ohta, Y., Stossel, T. P. and Kumar, R. (2002). Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat. Cell Biol. 4, 681-690.
39. Wyttenbach, A. and Tolkovsky, A. M. (2006). The BH3-only protein Puma is both necessary and sufficient for neuronal apoptosis induced by DNA damage in sympathetic neurons. J. Neurochem. 96, 1213-1226.