Glycogen synthase kinase-3 regulates cytoskeleton and translocation of Rac1 in long cellular extensions of human keratinocytes

Experimental Cell Research

Volumn 293, Issue 1, 2004, Pages 68-80

  Koivisto, Leeni ^a   Häkkinen, Lari ^a   Matsumoto, Kazue ^b   McCulloch, Christopher A ^c   Yamada, Kenneth M ^b   Larjava, Hannu ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Actin; Lamellipodia; Rho GTPases; Tubulin

Indexed keywords

2 (3 CHLORO 4 HYDROXYANILINO) 3 (2 NITROPHENYL)MALEIMIDE; ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; AMINOPHENOL DERIVATIVE; COLCHICINE; CORTACTIN; CYTOCHALASIN D; ENZYME INHIBITOR; FIBRONECTIN BINDING PROTEIN; FILAMIN; GLYCOGEN SYNTHASE KINASE 3; GUANOSINE TRIPHOSPHATASE; INTEGRIN; KERATIN; LITHIUM CHLORIDE; MALEIMIDE DERIVATIVE; NOCODAZOLE; NUCLEIC ACID SYNTHESIS INHIBITOR; PACLITAXEL; PHOSPHOLIPASE C; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN CDC42; RAC1 PROTEIN; RHO KINASE; STAUROSPORINE; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; BIOSYNTHESIS; CELL CULTURE; CHEMISTRY; CONTROLLED STUDY; CYTOSKELETON; DRUG EFFECT; EPIDERMIS CELL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; HUMAN CELL; KERATINOCYTE; LAMELLIPODIUM; METABOLISM; MICROTUBULE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOPODIUM;

EID: 0346059416     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.09.026     Document Type: Article

References (69)

1. Odland G., Ross R. Human wound repair: I. Epidermal regeneration. J. Cell Biol. 39:1968;135-151.
2. Larjava H., Haapasalmi K., Salo T., Wiebe C., Uitto V.-J. Keratinocyte integrins in wound healing and chronic inflammation of the human periodontium. Oral Dis. 2:1996;77-86.
3. Woodley D.T. Reepithelization. Clark R.A.F. The Molecular and Cellular Biology of Wound Repair. 1996;339-354 Plenum, New York.
4. Koivisto L., Alavian K., Häkkinen L., Pelech S., McCulloch C.A., Larjava H. Glycogen synthase kinase-3 regulates extended lamellipodia formation in human keratinocytes. J. Cell Sci. 116:2003;3749-3760.
5. Morley S.M., Lane E.B. The keratinocyte cytoskeleton. Leigh I., Lane B., Watt F. The Keratinocyte Handbook. 1994;293-321 Cambridge Univ. Press, Cambridge, UK.
6. Salas P.J. Insoluble gamma-tubulin-containing structures are anchored to the apical network of intermediate filaments in polarized CACO-2 epithelial cells. J. Cell Biol. 146:1999;645-658.
7. Small V.J., Rotter K., Kaverina I. Functional design in the actin cytoskeleton. Curr. Opin. Cell Biol. 11:1999;54-60.
8. Mikhailov A., Gundersen G.G. Relationship between microtubule dynamics and lamellipodium formation revealed by direct imaging of microtubules in cells treated with nocodazole and taxol. Cell Motil. Cytoskelet. 41:1998;325-340.
9. Waterman-Storer C.M., Salmon E. Positive feedback interactions between microtubule and actin dynamics during cell motility. Curr. Opin. Cell Biol. 11:1999;61-67.
10. Nobes C.D., Hall A. Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 23:1995;456-459.
11. Van Aelst L., D'Souza-Schorey C. Rho GTPases and signaling networks. Genes Dev. 11:1997;2295-2322.
12. Nobes C.D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 81:1995;53-62.
13. Sander E.E., ten Klooster J.P., van Delft S., van der Kammen R.A., Collard J.G. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147:1999;1009-1022.
14. Zondag G.C., Evers E.E., ten Klooster J.P., Janssen L., van der Kammen R.A., Collard J.G. Oncogenic Ras downregulates Rac activity, which leads to increased Rho activity and epithelial-mesenchymal transition. J. Cell Biol. 149:2000;775-782.
15. Yamaguchi Y., Katoh H., Yasui H., Mori K., Negishi M. RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. J. Biol. Chem. 276:2001;18977-18983.
16. Price L.S., Leng J., Schwartz M.A., Bokoch G.M. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol. Cell. 9:1998;1863-1871.
17. Waterman-Storer C.M., Worthylake R.A., Liu B.P., Burridge K., Salmon E.D. Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts. Nat. Cell Biol. 1:1999;45-50.
18. Burridge K., Chrzanowska-Wodnicka M. Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12:1996;463-518.
19. Mitchison T.J., Cramer L.P. Actin-based cell motility and cell locomotion. Cell. 84:1996;371-379.
20. Fenteany G., Janmey P.A., Stossel T.P. Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets. Curr. Biol. 10:2000;831-838.
21. Grinnell F. Wound repair, keratinocyte activation and integrin modulation. J. Cell Sci. 101:1992;1-5.
22. Hughes P.E., Pfaff M. Integrin affinity modulation. Trends Cell Biol. 8:1998;359-364.
23. Larjava H., Koivisto L., Häkkinen L. Keratinocyte interaction with fibronectin during wound healing. Heino J., Kähäri V.-M. Cell Invasion. 2002;42-64 Landes Biosciences, Georgetown, TX. www.Eurecah.com.
24. Larjava H., Salo T., Haapasalmi K., Kramer R.H., Heino J. Expression of integrins and basement membrane components by wound keratinocytes. J. Clin. Invest. 92:1993;1425-1435.
25. Haapasalmi K., Zhang K., Tonnesen M., Olerud J., Sheppard D., Salo T., Kramer R., Clark R.A., Uitto V.-J., Larjava H. Keratinocytes in human wounds express alpha v beta 6 integrin. J. Invest. Dermatol. 106:1996;42-48.
26. Koivisto L., Larjava K., Häkkinen L., Uitto V.-J., Heino J., Larjava H. Different integrins mediate cell spreading, haptotaxis and lateral migration of HaCaT keratinocytes on fibronectin. Cell Adhes. Commun. 7:1999;245-257.
27. Boukamp P., Petrusevska R.T., Breitkreut D., Hornung J., Markham A., Fusenig N.E. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte line. J. Cell Biol. 106:1988;761-771.
28. Damsky C.H., Fitzgerald M., Fisher S.J. Distribution patterns of extracellular matrix components and β1 integrin receptors are intricately modulated during differentiation of human cytotrophoblast to an invasive phenotype in vivo. J. Clin. Invest. 89:1992;210-222.
29. Akiyama S.K., Yamada S.S., Chen W.-T., Yamada K.M. Analysis of fibronectin receptor function with monoclonal antibodies: roles in cell adhesion, migration, matrix assembly, and cytoskeletal organization. J. Cell Biol. 109:1989;863-875.
30. Houghton A.N., Eisenger M., Albino A.P., Cairncross J.G., Old L.J. Surface antigens of melanocytes and melanomas. Markers of melanocyte differentiation and melanoma subsets. J. Exp. Med. 156:1982;1755-1766.
31. Larjava H., Peltonen J., Akiyama S.K., Yamada S.S., Gralnick H.R., Uitto J., Yamada K.M. Novel function for β1 integrins in keratinocyte cell-cell interactions. J. Cell Biol. 110:1990;803-815.
32. Teramoto H., Coso O.A., Miyata H., Igishi T., Miki T., Gutkind J.S. Signaling from the small GTP-binding proteins Rac1 and Cdc42 to the c-Jun N-terminal kinase/stress-activated protein kinase pathway. A role for mixed lineage kinase 3/protein-tyrosine kinase 1, a novel member of the mixed lineage kinase family. J. Biol. Chem. 271:1996;27225-27228.
33. Tran H., Pankov R., Tran S.D., Hampton B., Burgess W.H., Yamada K.M. Integrin clustering induces kinectin accumulation. J. Cell Sci. 115:2002;2031-2040.
34. Piperno G., LeDizet M., Chang X.J. Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J. Cell Biol. 104:1987;289-302.
35. Ryle C.M., Breitkreutz D., Stark H.J., Leigh I.M., Steinert P.M., Roop D., Fusenig N.E. Density-dependent modulation of synthesis of keratins 1 and 10 in the human keratinocyte line HACAT and in ras-transfected tumorigenic clones. Differentiation. 40:1989;42-54.
36. Fuchs E., Cleveland D.W. A structural scaffolding of intermediate filaments in health and disease. Science. 279:1998;514-519.
37. Coghlan M.P., Culbert A.A., Cross D.A., Corcoran S.L., Yates J.W., Pearce N.J., Rausch O.L., Murphy G.J., Carter P.S., Roxbee Cox L., Mills D., Brown M.J., Haigh D., Ward R.W., Smith D.G., Murray K.J., Reith A.D., Holder J.C. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem. Biol. 7:2000;793-803.
38. Feng J., Ito M., Kureishi Y., Ichikawa K., Amano M., Isaka N., Okawa K., Iwamatsu A., Kaibuchi K., Hartshorne D.J., Nakano T. Rho-associated kinase of chicken gizzard smooth muscle. J. Biol. Chem. 274:1999;3744-3752.
39. Zhang D., Wang Z., Jin N., Li L., Rhoades R.A., Yancey K.W., Swartz D.R. Microtubule disruption modulates the Rho-kinase pathway in vascular smooth muscle. J. Muscle Res. Cell Motil. 22:2001;193-200.
40. May R.C. The Arp2/3 complex: a central regulator of the actin cytoskeleton. Cell. Mol. Life Sci. 58:2001;1607-1626.
41. Stossel T.P., Condeelis J., Cooley L., Hartwig J.H., Noegel A., Schleicher M., Shapiro S.S. Filamins as integrators of cell mechanics and signalling. Nat. Rev,. Mol. Cell Biol. 2:2001;138-145.
42. Weed S.A., Parsons J.T. Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene. 20:2001;6418-6434.
43. Klein P.S., Melton D.A. A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. U. S. A. 93:1996;8455-8459.
44. Ridley A.J., Paterson H.F., Johnston C.L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 70:1992;401-410.
45. Best A., Ahmed S., Kozma R., Lim L. The Ras-related GTPase Rac1 binds tubulin. J. Biol. Chem. 271:1996;3756-3762.
46. Daub H., Gevaert K., Vandekerckhove J., Sobel A., Hall A. Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J. Biol. Chem. 276:2001;1677-1680.
47. Wittmann T., Bokoch G.M., Waterman-Storer C.M. Regulation of leading edge microtubule and actin dynamics downstream of Rac1. J. Cell Biol. 161:2003;845-851.
48. Larcher J.C., Boucher D., Lazereg S., Gros F., Denoulet P. Interaction of kinesin motor domains with alpha- and beta-tubulin subunits at a tau-independent binding site. Regulation by polyglutamylation. J. Biol. Chem. 271:1996;22117-22124.
49. Liao G., Gundersen G.G. Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J. Biol. Chem. 273:1998;9797-9803.
50. Morfini G., Szebenyi G., Elluru R., Ratner N., Brady S.T. Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J. 21:2002;, 281-293.
51. Mandelkow E.M., Drewes G., Biernat J., Gustke N., Van Lint J., Vandenheede J.R., Mandelkow E. Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett. 314:1992;315-321.
52. Gundersen G.G., Bulinski J.C. Selective stabilization of microtubules oriented toward the direction of cell migration. Proc. Natl. Acad. Sci U. S. A. 85:1988;5946-5950.
53. Gundersen G.G., Khawaja S., Bulinski J.C. Generation of a stable, posttranslationally modified microtubule array is an early event in myogenic differentiation. J. Cell Biol. 109:1989;2275-2288.
54. Baas P.W., Black M.M. Individual microtubules in the axon consist of domains that differ in both composition and stability. J. Cell Biol. 111:1990;495-509.
55. Rasouly D., Rahamim E., Ringel I., Ginzburg I., Muarakata C., Matsuda Y., Lazarovici P. Neurites induced by staurosporine in PC12 cells are resistant to colchicine and express high levels of tau proteins. Mol. Pharmacol. 45:1994;29-35.
56. Gurland G., Gundersen G.G. Protein phosphatase inhibitors induce the selective breakdown of stable microtubules in fibroblasts and epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 90:1993;8827-8831.
57. Liao H., Li Y., Brautigan D.L., Gundersen G.G. Protein phosphatase 1 is targeted to microtubules by the microtubule-associated protein Tau. J. Biol. Chem. 273:1998;21901-21908.
58. Ishihara H., Martin B.L., Brautigan D.L., Karaki H., Ozaki H., Kato Y., Fusetani N., Watabe S., Hashimoto K., Uemura D., Hartshorne J. Calyculin A and okadaic acid: inhibitors of protein phosphatase activity. Biochem. Biophys. Res. Commun. 159:1989;871-877.
59. Hemmings B.A., Resink T.J., Cohen P. Reconstitution of a Mg-ATP-dependent protein phosphatase and its activation through a phosphorylation mechanism. FEBS Lett. 150:1982;319-324.
60. Yang S.D., Chou C.K., Huang M., Song J.S., Chen H.C. Epidermal growth factor induces activation of protein kinase FA and ATP.Mg-dependent protein phosphatase in A431 cells. J. Biol. Chem. 264:1989;5407-5411.
61. Bennecib M., Gong C.X., Grundke-Iqbal I., Iqbal K. Role of protein phosphatase-2A and -1 in the regulation of GSK-3, cdk5 and cdc2 and the phosphorylation of tau in rat forebrain. FEBS Lett. 485:2000;87-93.
62. Svitkina T.M., Borisy G.G. Progress in protrusion: the tell-tale scar. Trends Biochem. Sci. 24:1999;432-436.
63. Mullins R.D. How WASP-family proteins and the Arp2/3 complex convert intracellular signals into cytoskeletal structures. Curr. Opin. Cell Biol. 12:2000;91-96.
64. Etienne-Manneville S., Hall A. Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature. 421:2003;753-756.
65. Hirose M., Ishizaki T., Watanabe N., Uehata M., Kranenburg O., Moolenaar W.H., Matsumura F., Maekawa M., Bito H., Narumiya S. Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141:1998;1625-1636.
66. Machesky L.M., Hall A. Role of actin polymerization and adhesion to extracellular matrix in Rac- and Rho-induced cytoskeletal reorganization. J. Cell Biol. 138:1997;913-926.
67. Clark E.A., King W.G., Brugge J.S., Symons M., Hynes R.O. Integrin-mediated signals regulated by members of the rho family of GTPases. J. Cell Biol. 142:1998;573-586.
68. Hall A. Rho GTPases and the actin cytoskeleton. Science. 279:1998;509-514.
69. del Pozo M.A., Price L.S., Alderson N.B., Ren X.D., Schwartz M.A. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19:2000;2008-2014.