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Cell Growth and Development

Hic-5-Reduced Cell Spreading on Fibronectin: Competitive Effects between Paxillin and Hic-5 through Interaction with Focal Adhesion Kinase

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Pages 5332-5345 | Received 05 Sep 2000, Accepted 16 May 2001, Published online: 28 Mar 2023

REFERENCES

  • Angers-Loustau, A., J.-F. Cote, A. Charest, D. Dowbenko, S. Spencer, L. A. Lasky, and M. L. Tremblay. 1999. Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts. J. Cell Biol. 144:1019–1031.
  • Avraham, S., R. London, Y. Fu, S. Ota, D. Hiregowdara, J. Li, S. Jiang, L. M. Pasztor, R. A. White, J. E. Groopman, and H. Avraham. 1995. Identification and characterization of a novel related adhesion focal tyrosine kinase (RAFTK) from megakaryocytes and brain. J. Biol. Chem. 270:27742–27751.
  • Bellis, S. L., J. T. Miller, and C. E. Turner. 1995. Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J. Biol. Chem. 270:17437–17441.
  • Birge, R. B., J. E. Fajardo, C. Reichman, S. E. Shoelson, Z. Songyang, L. C. Cantley, and H. Hanafusa. 1993. Identification and characterization of a high-affinity interaction between v-Crk and tyrosine-phosphorylated paxillin in CT10-transformed fibroblasts. Mol. Cell. Biol. 13:4648–4656.
  • Bockholt, S. M., and K. Burridge. 1993. Cell spreading on extracellular matrix proteins induces tyrosine phosphorylation of tensin. J. Biol. Chem. 268:14565–14567.
  • Brown, M. C., J. A. Perrotta, and C. E. Turner. 1996. Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding. J. Cell Biol. 135:1109–1123.
  • Brown, M. C., M. S. Curtis, and C. E. Turner. 1998. Paxillin LD motifs may define a new family of protein recognition domains. Nat. Struct. Biol. 5:677–678.
  • Burridge, K., K. Fath, T. Kelly, G. Nuckolls, and C. E. Turner. 1988. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4:487–525.
  • Burridge, K., C. E. Turner, and L. H. Romer. 1992. Tyrosine phosphorylation of paxillin and pp 125 FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119:898–903.
  • Clark, E. A., and J. S. Brugge. 1995. Integrins and signal transduction pathways: the road taken. Science 268:233–239.
  • Cote, J.-F., C. E. Turner, and M. L. Tremblay. 1999. Intact LIM 3 and LIM 4 domains of paxillin are required for the association to a novel polyproline region (Pro 2) of protein-tyrosine phosphatase-PEST. J. Biol. Chem. 274:20550–20560.
  • Courtneidge, S. A.. 1985. Activation of the pp60c-src kinase by middle T antigen binding or by dephosphorylation. EMBO J. 4:1471–1477.
  • Davis, R. J.. 1994. MAPKs: new JNK expands the group. Trends Biochem. Sci. 19:470–473.
  • Feller, S. M., B. Knudsen, and H. Hanafusa. 1995. Cellular proteins binding to the first Src homology 3 (SH3) domain of the proto-oncogene product c-Crk indicate Crk-specific signaling pathways. Oncogene 10:1465–1473.
  • Fujita, H., K. Kamiguchi, D. Cho, M. Shibanuma, C. Morimoto, and K. Tachibana. 1998. Interaction of Hic-5, a senescence-related protein, with focal adhesion kinase. J. Biol. Chem. 273:26516–26521.
  • Garton, A. J., and N. K. Tonks. 1999. Regulation of fibroblast motility by the protein tyrosine phosphatase PTP-PEST. J. Biol. Chem. 274:3811–3818.
  • Glenney, J. R. Jr., and L. Zokas. 1989. Novel tyrosine kinase substrates from Rous sarcoma virus-transformed cells are present in the membrane skeleton. J. Cell Biol. 108:2401–2408.
  • Gotoh, T., S. Hattori, S. Nakamura, H. Kitayama, M. Noda, Y. Takai, K. Kaibuchi, H. Matsui, O. Hatase, and H. Takahashi. 1995. Identification of Rap1 as a target for the Crk SH3 domain-binding guanine nucleotide-releasing factor C3G. Mol. Cell. Biol. 1995-15:6746–6753.
  • Guan, J. L., and D. Shalloway. 1992. Regulation of focal adhesion-associated protein tyrosine kinase by both cellular and oncogenic transformation. Nature 358:690–692.
  • Hall, A.. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509–514.
  • Hanks, S. K., and T. R. Polte. 1997. Signaling through focal adhesion kinase. Bioessays 19:137–145.
  • Hasegawa, H., E. Kiyokawa, S. Tanaka, K. Nagashima, N. Gotoh, M. Shibuya, T. Kurata, and M. Matsuda. 1996. DOCK180, a major CRK-binding protein, alters cell morphology upon translocation to the cell membrane. Mol. Cell. Biol. 16:1770–1776.
  • Hemler, M. E.. 1990. VLA proteins in the integrin family: structures, functions, and their role on leukocytes. Annu. Rev. Immunol. 8:365–400.
  • Hildebrand, J. D., M. D. Schaller, and J. T. Parsons. 1995. Paxillin, a tyrosine phosphorylated focal adhesion-associated protein binds to the carboxyl terminal domain of focal adhesion kinase. Mol. Biol. Cell 6:637–647.
  • Hirai, H., T. Suzuki, J. Fujisawa, J. Inoue, and M. Yoshida. 1994. Tax protein of human T-cell leukemia virus type I binds to the ankyrin motifs of inhibitory factor B and induces nuclear translocation of transcription factor NF-B proteins for transcriptional activation. Proc. Natl. Acad. Sci. USA 91:3584–3588.
  • Hynes, R. O.. 1992. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11–25.
  • Illic, D., Y. Furuta, S. Kanazawa, N. Tanaka, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, and T. Yamamoto. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539–544.
  • Ishino, K., J. Kaneyama, M. Shibanuma, and K. Nose. 2000. Specific decrease in the level of Hic-5, a focal adhesion protein, during immortalization of mouse embryonic fibroblasts, and its association with focal adhesion kinase. J. Cell. Biochem. 76:411–419.
  • Ishino, M., H. Aoto, H. Sasaski, R. Suzuki, and T. Sasaki. 2000. Phosphorylation of Hic-5 at tyrosine 60 by CAK β and Fyn. FEBS Lett. 474:179–183.
  • Juliano, R. L., and S. Haskill. 1993. Signal transduction from the extracellular matrix. J. Cell Biol. 120:577–585.
  • Kaplan, K. B., J. R. Swedlow, D. O. Morgan, and H. E. Varmus. 1995. c-Src enhances the spreading of src−/− fibroblasts on fibronectin by a kinase-independent mechanism. Genes Dev. 9:1505–1517.
  • Kitayama, H., Y. Sugimoto, T. Matsuzaki, Y. Ikawa, and M. Noda. 1989. A ras-related gene with transformation suppressor activity. Cell 56:77–84.
  • Kiyokawa, E., N. Mochizuki, T. Kurata, and M. Matsuda. 1997. Role of Crk oncogene product in physiologic signaling. Crit. Rev. Oncog. 8:329–342.
  • Kiyokawa, E., Y. Hashimoto, T. Kurata, H. Sugimura, and M. Matsuda. 1998. Evidence that DOCK180 up-regulates signals from the CrkII-p130C as complex. J. Biol. Chem. 273:24479–24484.
  • Kiyokawa, E., Y. Hashimoto, S. Kobayashi, H. Sugimura, T. Kurata, and M. Matsuda. 1998. Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev. 12:3331–3336.
  • Kizaka-Kondoh, S., M. Matsuda, and H. Okayama. 1996. CrkII signals from epidermal growth factor receptor to Ras. Proc. Natl. Acad. Sci. USA 93:12177–12182.
  • Kmiecik, T. E., and D. Shalloway. 1987. Activation and suppression of pp60c-src transforming ability by mutation of its primary sites of tyrosine phosphorylation. Cell 49:65–73.
  • Koch, C. A., D. Anderson, M. F. Moran, C. Ellis, and T. Pawson. 1991. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science 252:668–674.
  • Kozak, M.. 1987. At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J. Mol. Biol. 196:947–950.
  • Kozma, R., S. Ahmed, A. Best, and L. Lim. 1995. The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol. 15:1942–1952.
  • Lev, S., H. Moreno, R. Martinez, P. Canoll, E. Peles, J. M. Musacchio, G. D. Plowman, B. Rudy, and J. Schlessinger. 1995. Protein tyrosine kinase PYK2 involved in Ca2+-induced regulation of ion channel and MAP kinase functions. Nature 376:737–745.
  • Manser, E., H. Y. Huang, T. H. Loo, X. Q. Chen, J. M. Dong, T. Leung, and L. Lim. 1997. Expression of constitutively active alpha-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17:1129–1143.
  • Matsuda, M., S. Tanaka, S. Nagata, A. Kojima, T. Kurata, and M. Shibuya. Two species of human CRK cDNA encode proteins with distinct biological activities. Mol. Cell. Biol. 12:3482–3489.
  • Matsuda, M., Y. Hashimoto, K. Muroya, H. Hasegawa, T. Kurata, S. Tanaka, S. Nakamura, and S. Hattori. 1994. CRK protein binds to two guanine nucleotide-releasing proteins for the Ras family and modulates nerve growth factor-induced activation of Ras in PC12 cells. Mol. Cell. Biol. 14:5495–5500.
  • Matsuya, M., H. Sasaki, H. Aoto, T. Mitaka, K. Nagura, T. Ohba, M. Ishino, S. Takahashi, R. Suzuki, and T. Sasaki. 1998. Cell adhesion kinase beta forms a complex with a new member, Hic-5, of proteins localized at focal adhesions. J. Biol. Chem. 273:1003–1114.
  • Matsuyama, T., A. Yamada, J. Kay, K. M. Yamada, S. K. Akiyama, S. F. Schlossman, and C. Morimoto. 1989. Activation of CD4 cells by fibronectin and anti-CD3 antibody: a synergistic effect mediated by the VLA-5 fibronectin receptor complex. J. Exp. Med. 170:1133–1148.
  • Mayer, B. J., M. Hamaguchi, and H. Hanafusa. 1988. A novel viral oncogene with structural similarity to phospholipase C. Nature 332:272–275.
  • Mazaki, Y., S. Hashimoto, and H. Sabe. 1997. Monocyte cells and cancer cells express novel paxillin isoforms with different binding properties to focal adhesion proteins. J. Biol. Chem. 272:7437–7444.
  • Naviaux, R. K., E. Costanzi, M. Haas, and I. M. Verma. 1996. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70:5701–5705.
  • Nishiya, N., Y. Iwabuchi, M. Shibanuma, J.-F. Cote, M. L. Tremblay, and K. Nose. 1999. Hic-5, a paxillin homologue, binds to the protein-tyrosine phosphatase PEST (PTP-PEST) through its LIM 3 domain. J. Biol. Chem. 274:9847–9853.
  • Nobes, C. D., and A. Hall. 1995. Rho, Rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53–62.
  • Owen, J. D., P. J. Ruest, D. W. Fry, and S. K. Hanks. 1999. Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2. Mol. Cell. Biol. 19:4806–4818.
  • Petit, V., B. Boyer, D. Lentz, C. E. Turner, J. P. Thiery, and A. M. Valls. 2000. Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBT-II cells. J. Cell Biol. 148:957–970.
  • Polte, T. R., and S. K. Hanks. 1997. Complexes of focal adhesion kinase (FAK) and Crk-associated substrate (p 130cas) are elevated in cytoskeleton-associated fractions following adhesion and Src transformation. Requirements for Src kinase activity and FAK proline-rich motif. J. Biol. Chem. 272:5501–5509.
  • Price, L. S., J. Leng, M. A. Schwartz, and G. M. Bokoch. 1998. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol. Cell 9:1863–1871.
  • Richardson, A., and T. Parsons. 1996. A mechanism for regulation of the adhesion-associated protein tyrosine kinase pp 125FAK. Nature 380:538–540.
  • Richardson, A., R. K. Malik, J. D. Hildebrand, and J. T. Parsons. 1997. Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylation. Mol. Cell. Biol. 17:6906–6914.
  • Romer, L. H., N. McLean, C. E. Turner, and K. Burridge. 1994. Tyrosine kinase activity, cytoskeletal organization, and motility in human vascular endothelial cells. Mol. Biol. Cell 5:349–361.
  • Ruoslahti, E., and J. C. Reed. 1994. Anchorage dependence, integrins, and apoptosis. Cell 77:477–478.
  • Sakai, R., A. Iwamatsu, N. Hirano, S. Ogawa, T. Tanaka, H. Masno, Y. Yazaki, and H. Hirai. 1994. A novel signaling molecule, p130, forms stable complexes in vivo with v-Crk and v-Src in a tyrosine phosphorylation-dependent manner. EMBO J. 13:3748–3756.
  • Salgia, R., S. Avraham, E. Pisick, J. Li, S. Raja, E. A. Greenfield, M. Sattler, H. Avraham, and J. D. Griffin. 1996. The related adhesion focal tyrosine kinase forms a complex with paxillin in hematopoietic cells. J. Biol. Chem. 271:31222–31226.
  • Sander, E. E., J. P. ten Klooster, S. van Delft, R. A. van der Kammen, and J. G. Collard. 1999. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147:1009–1022.
  • Sasaki, H., K. Nagura, M. Ishino, H. Tobioka, K. Kotani, and T. Sasaki. 1995. Cloning and characterization of cell adhesion kinase, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily. J. Biol. Chem. 270:21206–21219.
  • Sanders, L. C., F. Matsumura, G. M. Bokoch, and P. de Lanerolle. 1999. Inhibition of myosin light chain kinase by p21-activated kinase. Science 283:2083–2085.
  • Schaller, M. D., C. A. Borgman, B. S. Cobb, R. R. Vines, A. B. Reynolds, and J. T. Parsons. 1992. pp125FAK, a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc. Natl. Acad. Sci. USA 89:5192–5196.
  • Schaller, M. D., and J. T. Parsons. 1995. pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15:2635–2645.
  • Schmeichel, K. L., and M. C. Beckerle. 1994. The LIM domain is a modular protein-binding interface. Cell 79:211–219.
  • Schwartz, M. A., M. D. Schaller, and M. H. Ginsberg. 1995. Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell Dev. Biol. 11:549–599.
  • Shibanuma, M., J. Mashimo, T. Kuroki, and K. Nose. Characterization of the TGF beta 1-inducible hic-5 gene that encodes a putative novel zinc finger protein and its possible involvement in cellular senescence. J. Biol. Chem. 17:26767–26774.
  • Shibanuma, M., E. Mochizuki, R. Maniwa, J. Mashimo, N. Nishiya, S. Imal, T. Takano, M. Oshimura, and K. Nose. 1997. Induction of senescence-like phenotypes by forced expression of hic-5, which encodes a novel LIM motif protein, in immortalized human fibroblasts. Mol. Cell. Biol. 17:1224–1235.
  • Shimizu, Y., G. A. van Seventer, K. J. Horgan, and S. Shaw. 1990. Costimulation of proliferative responses of resting CD4+ T cells by the interaction of VLA-4 and VLA-5 with fibronectin or VLA-6 with laminin. J. Immunol. 145:59–67.
  • Sieg, D. J., D. Ilic, K. C. Jones, C. H. Damsky, T. Hunter, and D. D. Schlaepfer. 1998. Pyk2 and Src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but Pyk2 does not fully function to enhance FAK-cell migration. EMBO J. 17:5933–5947.
  • Simon, M. A., D. D. Bowtell, G. S. Dodson, T. R. Laverty, and G. M. Rubin. 1991. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase M. Cell 67:701–716.
  • Tachibana, K., T. Sato, N. D'Avirro, and C. Morimoto. 1995. Direct association of pp125FAK with paxillin, the focal adhesion-targeting mechanism of pp125FAK. J. Exp. Med. 182:1089–1099.
  • Takayama, Y., S. Tanaka, K. Nagai, and M. Okada. 1999. Adenovirus-mediated overexpression of C-terminal Src kinase (Csk) in type I astrocytes interferes with cell spreading and attachment to fibronectin: correlation with tyrosine phosphorylations of paxillin and FAK. J. Biol. Chem. 274:2291–2297.
  • Tanaka, M., R. Gupta, and B. J. Mayer. 1995. Differential inhibition of signaling pathways by dominant-negative SH2/SH3 adapter proteins. Mol. Cell. Biol. 15:6829–6837.
  • Tanaka, S., T. Morishita, Y. Hashimoto, S. Hattori, S. Nakamura, M. Shibuya, K. Matuoka, T. Takenawa, T. Kurata, K. Nagashima, and M. Matsuda. 1994. C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins. Proc. Natl. Acad. Sci. USA 91:3443–3447.
  • Tanaka, S., T. Ouchi, and H. Hanafusa. 1997. Downstream of Crk adaptor signaling pathway: activation of Jun kinase by v-Crk through the guanine nucleotide exchange protein C3G. Proc. Natl. Acad. Sci. USA 94:2356–2361.
  • Thomas, J. W., M. A. Cooley, J. M. Broome, R. Salgia, J. D. Griffin, C. R. Lombardo, and M. D. Schaller. 1999. The role of focal adhesion kinase binding in the regulation of tyrosine phosphorylation of paxillin. J. Biol. Chem. 274:36684–36692.
  • Thomas, S. M., M. Hagel, and C. E. Turner. 1999. Characterization of a focal adhesion protein, Hic-5, that shares extensive homology with paxillin. J. Cell Sci. 112:181–190.
  • Turner, C. E., J. R. Glenney Jr., and K. Burridge. 1990. Paxillin: a new vinculin-binding protein present in focal adhesions. J. Cell Biol. 111:1059–1068.
  • Turner, C. E., and J. T. Miller. 1994. Primary sequence of paxillin contains putative SH2 and SH3 domain binding motifs and multiple LIM domains: identification of a vinculin and pp125Fak-binding region. J. Cell Sci. 107:1583–1591.
  • Turner, C. E.. 1998. Paxillin. Int. J. Biochem. Cell Biol. 30:955–959.
  • Turner, C. E., M. C. Brown, J. A. Perrotta, M. C. Riedy, S. N. Nikolopoulos, A. R. McDonald, S. Bagrodia, S. Thomas, and P. S. Leventhal. 1999. Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat, ARF-GAP protein: a role in cytoskeletal remodeling. J. Cell Biol. 145:851–863.
  • Vuori, K., and E. Ruoslahti. 1993. Activation of protein kinase C precedes alpha 5 beta 1 integrin-mediated cell spreading on fibronectin. J. Biol. Chem. 268:21459–21462.

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