Abstract
We investigated the focal adhesion proteins paxillin and Fak, and the cell-cell adhesion protein cadherin in developing zebrafish (Danio rerio) embryos. Cadherins are expressed in presomitic mesoderm where they delineate cells. The initiation of somite formation coincides with an increase in the phosphorylation of Fak, and the accumulation of Fak, phosphorylated Fak, paxillin, and fibronectin at nascent somite boundaries. In the notochord, cadherins are expressed on cells during intercalation, and phosphorylated Fak accumulates in circumferential rings where the notochord cells contact laminin in the perichordal sheath. Subsequently, changes in the orientations of collagen fibers in the sheath suggest that Fak-mediated adhesion allows longitudinal expansion of the notochord, but not lateral expansion, resulting in notochord elongation. Novel observations showed that focal adhesion kinase and paxillin concentrate at sites of cell-cell adhesion in the epithelial enveloping layer and may associate with actin cytoskeleton at epithelial junctions containing cadherins. Fak is phosphorylated at these epithelial junctions but is not phosphorylated on Tyr397, implicating a noncanonical mechanism of regulation. These data suggest that Fak and paxillin may function in the integration of cadherin-based and integrin-based cell adhesion during the morphogenesis of the early zebrafish embryo.
References
63
Referenced
107
-
Adams, D.S., Keller, R., and Ma, K. (1990). The mechanics of notochord elongation, straightening and stiffening in the embryo ofXenopus laevis.Development110, 115–130.
(
10.1242/dev.110.1.115
) -
Almeida, E.A.C., Ilic, D., Han, Q., Hauck, C.R., Jin, F., Kawakatsu, H., Schlaepfer, D.D., and Damsky, C.H. (2000). Matrix survival signaling: from fibronectin via focal adhesion kinase to c-Jun NH2-terminal kinase.J. Cell Biol.149, 741–754.
(
10.1083/jcb.149.3.741
) -
Avizienyte, E., Wyke, A.W., Jones, R.J., McLean, G.W., Westhoff, M.A., Brunton, V.G., and Frame, M.C. (2002). Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signaling.Nat. Cell Biol.4, 632–638.
(
10.1038/ncb829
) -
Babb, S.G., Barnett, J., Doedens, A.L., Cobb, N., Liu, Q., Sorkin, B.C., Yelick, P.C., Raymond, P.A., and Marrs, J.A. (2001). Zebrafish E-cadherin: expression during early embryogenesis and regulation during brain development.Dev. Dyn.22, 231–237.
(
10.1002/dvdy.1132
) -
Barrantes, I.B., Elia, A.J., Wunsch, K., De Angelis, M.H., Mak, T.W., Rossant, J., Conlon, R.A., Gossler, A., and de la Pompa, J.L. (1999). Interaction between notch signaling and lunatic fringe during somite boundary formation in the mouse.Curr. Biol.9, 470–480.
(
10.1016/S0960-9822(99)80212-7
) -
Betchaku, T., and Trinkaus, J.P. (1978). Contact relations, surface activity, and cortical microfilaments in marginal cells of the enveloping layer of the yolk syncytial and yolk cytoplasmic layers ofFundulusbefore and during epiboly.J. Exp. Zool.206, 381–426.
(
10.1002/jez.1402060310
) -
Bitzur, S., Kam, Z., and Geiger, B. (1994). Structure and distribution of N-cadherin in developing zebrafish embryos: morphogenetic effects of ectopic over-expression.Dev. Dyn.201, 121–136.
(
10.1002/aja.1002010204
) -
Brown, M.C., Curtis, M.S., and Turner, C.E. (1998). Paxillin LD motifs may define a new family of protein recognition domains.Nat. Struct. Biol.5, 677–678.
(
10.1038/1370
) 10.1091/mbc.02-02-0015
-
Cary, L.A., Klinghoffer, R.A., Sachsenmaier, C., and Cooper, J.A. (2002). SRC catalytic but not scaffolding function is needed for integrin-regulated tyrosine phosphorylation, cell migration, and cell spreading.Mol. Cell. Biol.22, 2427–2440.
(
10.1128/MCB.22.8.2427-2440.2002
) -
Chenn, A., Zhang, Y.A., Chang, B.T., and McConnell, S.K. (1998). Intrinsic polarity of mammalian neuroepithelial cells.Mol. Cell Neurosci.11, 183–193.
(
10.1006/mcne.1998.0680
) -
Conlon, R.A., Reaume, A.G., and Rossant, J. (1995). Notch1 is required for the coordinate segmentation of somites.Development121, 1533–1545.
(
10.1242/dev.121.5.1533
) - Cooper, M.S., and Kimmel, C.B. (1998).Morphogenetic cell behaviors and specification of cell fate during early teleost development, in Motion Analysis of Living Cells, ed. D.R. Soll and D. Wessels, New York: Wiley-Liss, 177–220.
-
Delarue, M., Saez, F.J., Boucaut, J.C., Thiery, J.P., and Broders, F. (1998). Medial cell mixing during axial morphogenesis of the amphibian embryo requires cadherin function.Dev. Dyn.213, 248–260.
(
10.1002/(SICI)1097-0177(199811)213:3<248::AID-AJA2>3.0.CO;2-F
) -
Duband, J.L., Dufour, S., Hatta, K., Takeichi, M., Edelman, G.M., and Thiery, J.P. (1987). Adhesion molecules during somitogenesis in the avian embryo.J. Cell Biol.104, 1361–174.
(
10.1083/jcb.104.5.1361
) - Furuta, Y., Ilic, D., Kanazawa, S., Takeda, N., Yamamoto, T., and Aizawa, S. (1995). Mesodermal defect in late phase of gastrulation by a targeted mutation of focal adhesion kinase, FAK.Oncogene11, 1989–1995.
-
Garcia-Alvarez, B., de Pereda, J.M., Calderwood, D.A., Ulmer, T.S., Critchley, D., Campbell, I.D., Ginsberg, M.H., and Liddington, R.C. (2003). Structural determinants of integrin recognition by talin.Mol. Cell.11, 49–58.
(
10.1016/S1097-2765(02)00823-7
) -
Georges-Labouesse, E.N., George, E.L., Rayburn, H., and Hynes, R.O. (1996). Mesodermal development in mouse embryos mutant for fibronectin.Dev. Dyn.207, 145–156.
(
10.1002/(SICI)1097-0177(199610)207:2<145::AID-AJA3>3.0.CO;2-H
) -
Ghanem, E. (1996). Immunohistochemical localization of type I and II collagens in the involuting chick notochords in vivo and in vitro.Cell Biol. Int.20, 681–685.
(
10.1006/cbir.1996.0090
) -
Gumbiner, B.M. (2000). Regulation of cadherin adhesive activity.J. Cell Biol.148, 399–403.
(
10.1083/jcb.148.3.399
) -
Hagel, M., George, E.L., Kim, A., Tamimi, R., Opitz, S.L., Turner, C.E., Imamoto, A., and Thomas, S.M. (2002). The adapter protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling.Mol. Cell. Biol.22, 901–915.
(
10.1128/MCB.22.3.901-915.2002
) -
Hanks, S.K., and Polte, T.R. (1997). Signaling through focal adhesion kinase.Bioessays19, 137–145.
(
10.1002/bies.950190208
) -
Henry, C.A., Hall, L.A., Hille, M.B., Solnica-Krezel, L., and Cooper, M.S. (2000). Somites in zebrafish doubly mutant forknypekandtrilobitefrom without internal mesenchymal cells or compaction.Curr. Biol.10, 1063–1066.
(
10.1016/S0960-9822(00)00677-1
) -
Henry, C.A., Crawford, B.D., Yan, Y.L., Postlethwait, J., Cooper, M.S., and Hille, M.B. (2001). Roles for zebrafish focal adhesion kinase in notochord and somite morphogenesis.Dev. Biol.240, 474–487.
(
10.1006/dbio.2001.0467
) -
Henry, C.A.et al. (2002). Two linked hairy/Enhancer of split-related Zebrafish genes, her1 and her7, function together to refine alternating somite boundaries.Development129, 3693–3704.
(
10.1242/dev.129.15.3693
) -
Hens, M.D., and DeSimone, D.W. (1995). Molecular analysis and developmental expression of the focal adhesion kinase pp125FAK inXenopus laevis.Dev. Biol.170, 274–288.
(
10.1006/dbio.1995.1214
) -
Holley, S.A., Jülich, D., Rauch, G.J., Geisler, R., and Nüsslein-Volhard, C. (2002). her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis.Development129, 1175–1183.
(
10.1242/dev.129.5.1175
) -
Jamora, C., and Fuchs, E. (2002). Intercellular adhesion, signalling and the cytoskeleton.Nat. Cell Biol.4, 101–108.
(
10.1038/ncb0402-e101
) -
Kane, D.A., Warga, R.M., and Kimmel, C.B. (1992). Mitotic domains in the early embryo of the zebrafish.Nature360, 735–737.
(
10.1038/360735a0
) -
Keller, R., Cooper, M.S., Danilchik, M., Tibbetts, P., and Wilson, P.A. (1989). Cell intercalation during notochord development inXenopus laevis.J. Exp. Zool.251, 134–154.
(
10.1002/jez.1402510204
) -
Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B., and Schilling, T.F. (1995). Stages of embryonic development of the zebrafish.Dev. Dyn.203, 253–310.
(
10.1002/aja.1002030302
) -
Krotoski, D., and Bronner-Fraser, M. (1990). Distribution of integrins and their ligands in the trunk ofXenopus laevisduring neural crest cell migration.J. Exp. Zool.253, 139–150.
(
10.1002/jez.1402530204
) -
Lee, C.H., and Gumbiner, B.M. (1995). Disruption of gastrulation movements inXenopusby a dominant-negative mutant for C-cadherin.Dev. Biol.171, 363–373.
(
10.1006/dbio.1995.1288
) -
Lele, Z., Folchert, A., Concha, M., Rauch, G.J., Geisler, R., Rosa, F., Wilson, S.W., Hammerschmidt, M., and Bally-Cuif, L. (2002). Parachute/N-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube.Development129, 3281–3294.
(
10.1242/dev.129.14.3281
) -
Lele, Z., and Krone, P.H. (1997). Expression of genes encoding the collagen-binding heat shock protein (Hsp47) and type II collage in developing zebrafish embryos.Mech. Dev.61, 89–98.
(
10.1016/S0925-4773(96)00626-0
) -
Levine, E., Lee, C.H., Kintner, C., and Gumbiner, B.M. (1994). Selective disruption of E-cadherin function in earlyXenopusembryos by a dominant negative mutant.Development120, 901–909.
(
10.1242/dev.120.4.901
) -
Liddington, R.C., Bankston, L.A., and de Pereda, J.M. (2003). Cell adhesion: a FERM grasp of membrane dynamics.Curr. Biol.13, R94–R95.
(
10.1016/S0960-9822(03)00035-6
) -
Linask, K.K., Ludwig, C., Han, M.D., Liu, X., Radice, G.L., and Knudsen, K.A. (1998). N-Cadherin/catenin-mediated morphoregulation of somite formation.Dev. Biol.202, 85–102.
(
10.1006/dbio.1998.9025
) -
McLean, G.W., Fincham, V.J., and Frame, M.C. (2000). v-Src induces tyrosine phosphorylation of focal adhesion kinase independently of tyrosine 397 and formation of a complex with Src.J. Biol. Chem.275, 23333–23339.
(
10.1074/jbc.M909322199
) -
Ogawa, M., Hiraoka, Y., Taniguchi, K., Sakai, Y., and Aiso, S. (2001). mRNA sequence of theXenopus laevispaxillin gene and its expression.Biochim. Biophys. Acta1519, 235–240.
(
10.1016/S0167-4781(01)00230-5
) -
Parsons, M.J., Pollard, S.M., Saúde, L., Feldman, B., Coutinho, P., Hirst, E.M.A., and Stemple, D.L. (2002). Zebrafish mutants identify an essential role for laminins in notochord formation.Development129, 3137–3146.
(
10.1242/dev.129.13.3137
) -
Polte, T.R., Naftilan, A.J., and Hanks, S.K. (1994). Focal adhesion kinase is abundant in developing blood vessels and elevation of its phosphotyrosine content in vascular smooth muscle cells is a rapid response to angiotensin II.J. Cell. Biochem.55, 106–119.
(
10.1002/jcb.240550113
) -
Radice, G.L., Rayburn, H., Matsunami, H., Knudsen, K.A., Takeichi, M., and Hynes, R.O. (1997). Developmental defects in mouse embryos lacking N-cadherin.Dev. Biol.181, 64–78.
(
10.1006/dbio.1996.8443
) -
Rongish, B.J., and Kinsey, W.H. (2000). Transient nuclear localization of Fyn kinase during development in zebrafish.Anat. Rec.260, 115–123.
(
10.1002/1097-0185(20001001)260:2<115::AID-AR10>3.0.CO;2-C
) -
Roy, S., Ruest, P.J., and Hanks, S.K. (2002). Fak regulates tyrosine phosphorylation of CAS, paxillin, and PYK2 in cells expressing v-Src, but is not a critical determinant of v-Src transformation.J. Cell. Biochem.84, 377–388.
(
10.1002/jcb.10025
) - Schlaepfer, D.D., and Hunter, T. (1998). Integrin signaling and tyrosine phosphorylation: just the FAKs?Trends Cell Biol.8, 151–157.
-
Schwartz, M.A. (2001). Integrin signaling revisited.Trends Cell Biol.11, 466–470.
(
10.1016/S0962-8924(01)02152-3
) -
Sugrue, S.P., and Zieske, J.D. (1997). ZO1 in corneal epithelium: association to the zonula occludens and adherens junctions.Exp. Eye Res.64, 11–20.
(
10.1006/exer.1996.0175
) -
Stemple, D.L. (1996). Mutations affecting development of the notochord in zebrafish.Development123, 117–128.
(
10.1242/dev.123.1.117
) - Tsai, W., and Kinsey, W.H. (2002). Role of c-Yes kinase during gastrulation of the zebrafish embryos.Mol. Biol. Cell13, 117a.
-
Tong, X., Salgia, R., Li, J.L., Griffin, J.D., and Howley, P.M. (1997). The bovine papillomavirus E6 protein binds to the LD motif repeats of paxillin and blocks its interaction with vinculin and the focal adhesion kinase.J. Biol. Chem.272, 33373–33376.
(
10.1074/jbc.272.52.33373
) -
Turner, C.E. (1991). Paxillin is a major phosphotyrosine-containing protein during embryonic development.J. Cell Biol.115, 201–207.
(
10.1083/jcb.115.1.201
) -
Turner, C.E. (2000a). Paxillin and focal adhesion signalling.Nat. Cell Biol.2, E231–E236.
(
10.1038/35046659
) -
Turner, C.E. (2000b). Paxillin interactions.J. Cell Sci.113, 4139–4140.
(
10.1242/jcs.113.23.4139
) -
West, K.A., Zhang, H., Brown, M.C., Nikolopoulos, S.N., Riedy, M.C., Horwitz, A.F., and Turner, C.E. (2001). The LD4 motif of paxillin regulates cell spreading and motility through an interaction with paxillin kinase linker (PKL).J. Cell Biol.154, 161–176.
(
10.1083/jcb.200101039
) - Westerfield, M. (1995). The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene, OR: University of Oregon Press.
-
Winklbauer, R., and Keller, R.E. (1996). Fibronectin, mesodermal migration and gastrulation.Dev. Biol.177, 413–426.
(
10.1006/dbio.1996.0174
) - Winklbauer, R., Nagel, M., Selchow, A., and Wacker, S. (1996). Mesoderm migration in theXenopus gastrula.Int. J. Dev. Biol.40, 305–311.
-
Wood, A., and Thorogood, P. (1994). Patterns of cell behaviour underlying somitogenesis and notochord formation in intact vertebrate embryos.Dev. Dyn.201, 151–167.
(
10.1002/aja.1002010206
) -
Yan, Y.L., Hatta, K., Riggleman, B., and Postlethwait, J.H. (1995). Expression of a type II collagen gene in the zebrafish embryonic axis.Dev. Dyn.203, 363–376.
(
10.1002/aja.1002030308
) -
Yang, J.T., Bader, B.L., Kreidberg, J.A., Ullman-Cullere, M., Trevithick, J.E., and Hynes, R.O. (1999). Overlapping and independent functions of fibronectin receptor integrins in early mesodermal development.Dev. Biol.215, 264–277.
(
10.1006/dbio.1999.9451
) -
Zalik, S.E., Lewandowski, E., Kam, Z., and Geiger, B. (1999). Cell adhesion and the actin cytoskeleton of the enveloping layer in the zebrafish embryo during epiboly.Biochem. Cell Biol.77, 527–542.
(
10.1139/o99-058
) -
Zhu, Y., McAlinden, A., and Sandell, L.J. (2001). Type IIA procollagen in development of the human intervertebral disc: regulated expression of the NH(2)-propeptide by enzymic processing reveals a unique developmental pathway.Dev. Dyn.220, 350–362.
(
10.1002/dvdy.1115
)
Dates
Type | When |
---|---|
Created | 22 years, 2 months ago (June 16, 2003, 8:35 p.m.) |
Deposited | 4 years, 2 months ago (June 7, 2021, 11:30 a.m.) |
Indexed | 2 months, 1 week ago (June 24, 2025, 12:46 p.m.) |
Issued | 22 years, 1 month ago (Aug. 1, 2003) |
Published | 22 years, 1 month ago (Aug. 1, 2003) |
Published Print | 22 years, 1 month ago (Aug. 1, 2003) |
@article{Crawford_2003, title={Activity and Distribution of Paxillin, Focal Adhesion Kinase, and Cadherin Indicate Cooperative Roles during Zebrafish Morphogenesis}, volume={14}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e02-08-0537}, DOI={10.1091/mbc.e02-08-0537}, number={8}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Crawford, Bryan D. and Henry, Clarissa A. and Clason, Todd A. and Becker, Amanda L. and Hille, Merrill B.}, year={2003}, month=aug, pages={3065–3081} }