The collagen receptor DDR1 regulates cell spreading and motility by associating with myosin IIA

Journal of Cell Science

Volumn 122, Issue 10, 2009, Pages 1637-1646

  Huang, Yun ^a   Arora, Pamela ^b   McCulloch, Christopher A ^b   Vogel, Wolfgang F ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Actin; Cell spreading; Discoidin domain receptor; Integrin; Migration; Non muscle myosin IIA

Indexed keywords

BETA1 INTEGRIN; BLEBBISTATIN; COLLAGEN; COLLAGEN RECEPTOR; DISCOIDIN DOMAIN RECEPTOR 1; MYOSIN IIA; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; COLLAGEN TYPE 1; DDR1 PROTEIN, HUMAN; DDR1 PROTEIN, MOUSE; FUSED HETEROCYCLIC RINGS; MOLECULAR MOTOR; MYH9 PROTEIN, HUMAN; MYH9 PROTEIN, MOUSE; MYOSIN HEAVY CHAIN; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MOTILITY; CELL SPREADING; CELL STRAIN 3T3; CONTROLLED STUDY; EMBRYO; IMMUNOPRECIPITATION; MOUSE; MUSCLE CONTRACTILITY; MUSCLE FORCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; STIMULUS RESPONSE; ANIMAL; CELL MOTION; CELL SHAPE; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; MICROFILAMENT; MOUSE MUTANT; MUTATION; PROTEIN BINDING; PROTEIN TRANSPORT; TIME; TUMOR CELL LINE;

ANIMALS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL SHAPE; COLLAGEN TYPE I; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; MICE; MICE, KNOCKOUT; MICROFILAMENTS; MOLECULAR MOTOR PROTEINS; MUTATION; MYOSIN HEAVY CHAINS; NIH 3T3 CELLS; NONMUSCLE MYOSIN TYPE IIA; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTOR PROTEIN-TYROSINE KINASES; TIME FACTORS; TRANSFECTION;

EID: 67649969512     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.046219     Document Type: Article

References (44)

1. Alves, F., Vogel, W., Mossie, K., Millauer, B., Hofler, H. and Ullrich, A. (1995). Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 10, 609-618.
2. Alves, F., Saupe, S., Ledwon, M., Schaub, F., Hiddemann, W. and Vogel, W. F. (2001). Identification of two novel, kinase-deficient variants of discoidin domain receptor 1, differential expression in human colon cancer cell lines. FASEB J. 15, 1321-1323.
3. Arora, P. D., Conti, M. A., Ravid, S., Sacks, D. B., Kapus, A., Adelstein, R. S., Bresnick, A. R. and McCulloch, C. A. (2008). Rap1 activation in collagen phagocytosis is dependent on non-muscle myosin II-A. Mol. Biol. Cell 19, 5032-5046.
4. Bolte, S. and Cordelieres, F. P. (2006). A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232.
5. Bresnick, A. R. (1999). Molecular mechanisms of nonmuscle myosin-II regulation. Curr. Opin. Cell Biol. 11, 26-33.
6. Conti, M. A., Even-Ram, S., Liu, C., Yamada, K. M. and Adelstein, R. S. (2004). Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J. Biol. Chem. 279, 41263-41266.
7. Curat, C. A. and Vogel, W. F. (2002). Discoidin domain receptor 1 controls growth and adhesion of mesangial cells. J. Am. Soc. Nephrol. 13, 2648-2656.
8. Dobereiner, H. G., Dubin-Thaler, B. J., Giannone, G. and Sheetz, M. P. (2005). Force sensing and generation in cell phases: analyses of complex functions. J. Appl. Physiol. 98, 1542-1546.
9. Even-Ram, S., Doyle, A. D., Conti, M. A., Matsumoto, K., Adelstein, R. S. and Yamada, K. M. (2007). Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nat. Cell Biol. 9, 299-309.
10. Faraci-Orf, E., McFadden, C. and Vogel, W. F. (2006). DDR1 signaling is essential to sustain Stat5 function during lactogenesis. J. Cell Biochem. 97, 109-121.
11. Geeves, M. A., Fedorov, R. and Manstein, D. J. (2005). Molecular mechanism of actomyosin-based motility. Cell Mol. Life Sci. 62, 1462-1477.
12. Giannone, G., Dubin-Thaler, B. J., Rossier, O., Cai, Y., Chaga, O., Jiang, G., Beaver, W., Dobereiner, H. G., Freund, Y., Borisy, G. et al. (2007). Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128, 561-575.
13. Hou, G., Vogel, W. and Bendeck, M. P. (2001). The discoidin domain receptor tyrosine kinase DDR1 in arterial wound repair. J. Clin. Invest. 107, 727-735.
14. Kamohara, H., Yamashiro, S., Galligan, C. and Yoshimura, T. (2001). Discoidin domain receptor 1 isoform-a (DDR1alpha) promotes migration of leukocytes in three-dimensional collagen lattices. FASEB J. 15, 2724-2726.
15. Kim, S. H., Lee, S., Suk, K., Bark, H., Jun, C. D., Kim, D. K., Choi, C. H. and Yoshimura, T. (2007). Discoidin domain receptor 1 mediates collagen-induced nitric oxide production in J774A.1 murine macrophages. Free Radic. Biol. Med. 42, 343-352.
16. Kolega, J. and Kumar, S. (1999). Regulatory light chain phosphorylation and the assembly of myosin II into the cytoskeleton of microcapillary endothelial cells. Cell Motil. Cytoskeleton 43, 255-268.
17. Koo, D. H., McFadden, C., Huang, Y., Abdulhussein, R., Friese-Hamim, M. and Vogel, W. F. (2006). Pinpointing phosphotyrosine-dependent interactions downstream of the collagen receptor DDR1. FEBS Lett. 580, 15-22.
18. Leitinger, B. and Hohenester, E. (2007). Mammalian collagen receptors. Matrix Biol. 26, 146-155.
19. Lenter, M., Uhlig, H., Hamann, A., Jeno, P., Imhof, B. and Vestweber, D. (1993). A monoclonal antibody against an activation epitope on mouse integrin chain beta 1 blocks adhesion of lymphocytes to the endothelial integrin alpha 6 beta 1. Proc. Natl. Acad. Sci. USA 90, 9051-9055.
20. Li, Z. H., Spektor, A., Varlamova, O. and Bresnick, A. R. (2003). Mts1 regulates the assembly of nonmuscle myosin-IIA. Biochemistry 42, 14258-14266.
21. Matsuyama, W., Wang, L., Farrar, W. L., Faure, M. and Yoshimura, T. (2004). Activation of discoidin domain receptor 1 isoform b with collagen up-regulates chemokine production in human macrophages: role of p38 mitogen-activated protein kinase and NF-kappa B. J. Immunol. 172, 2332-2340.
22. Mooney, D. J., Langer, R. and Ingber, D. E. (1995). Cytoskeletal filament assembly and the control of cell spreading and function by extracellular matrix. J. Cell Sci. 108, 2311-2320.
23. Nizak, C., Martin-Lluesma, S., Moutel, S., Roux, A., Kreis, T. E., Goud, B. and Perez, F. (2003). Recombinant antibodies against subcellular fractions used to track endogenous Golgi protein dynamics in vivo. Traffic 4, 739-753.
24. Ongusaha, P. P., Kim, J. I., Fang, L., Wong, T. W., Yancopoulos, G. D., Aaronson, S. A. and Lee, S. W. (2003). p53 induction and activation of DDR1 kinase counteract p53-mediated apoptosis and influence p53 regulation through a positive feedback loop. EMBO J. 22, 1289-1301.
25. Partridge, M. A. and Marcantonio, E. E. (2006). Initiation of attachment and generation of mature focal adhesions by integrin-containing filopodia in cell spreading. Mol. Biol. Cell 17, 4237-4248.
26. Pecci, A., Canobbio, I., Balduini, A., Stefanini, L., Cisterna, B., Marseglia, C., Noris, P., Savoia, A., Balduini, C. L. and Torti, M. (2005). Pathogenetic mechanisms of hematological abnormalities of patients with MYH9 mutations. Hum. Mol. Genet. 14, 3169-3178.
27. Richards, T. A. and Cavalier-Smith, T. (2005). Myosin domain evolution and the primary divergence of eukaryotes. Nature 436, 1113-1118.
28. Sakamoto, O., Suga, M., Suda, T. and Ando, M. (2001). Expression of discoidin domain receptor 1 tyrosine kinase on the human bronchial epithelium. Eur. Respir. J. 17, 969-974.
29. Sandquist, J. C., Swenson, K. I., Demali, K. A., Burridge, K. and Means, A. R. (2006). Rho kinase differentially regulates phosphorylation of nonmuscle myosin II isoforms A and B during cell rounding and migration. J. Biol. Chem. 281, 35873-35883.
30. Shrivastava, A., Radziejewski, C., Campbell, E., Kovac, L., McGlynn, M., Ryan, T. E., Davis, S., Goldfarb, M. P., Glass, D. J., Lemke, G. et al. (1997). An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol. Cell 1, 25-34.
31. Straight, A. F., Cheung, A., Limouze, J., Chen, I., Westwood, N. J., Sellers, J. R. and Mitchison, T. J. (2003). Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 299, 1743-1747.
32. Takubo, T., Wakui, S., Daigo, K., Kurokata, K., Ohashi, T., Katayama, K. and Hino, M. (2003). Expression of non-muscle type myosin heavy polypeptide 9 (MYH9) in mammalian cells. Eur. J. Histochem. 47, 345-352.
33. Vicente-Manzanares, M., Zareno, J., Whitmore, L., Choi, C. K. and Horwitz, A. F. (2007). Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J. Cell Biol. 176, 573-580.
34. Vogel, W. F. (2002). Ligand-induced shedding of discoidin domain receptor 1. FEBS Lett. 514, 175-180.
35. Vogel, W., Gish, G. D., Alves, F. and Pawson, T. (1997). The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell 1, 13-23.
36. Vogel, W., Brakebusch, C., Fassler, R., Alves, F., Ruggiero, F. and Pawson, T. (2000). Discoidin domain receptor 1 is activated independently of beta(1) integrin. J. Biol. Chem. 275, 5779-5784.
37. Vogel, W. F., Abdulhussein, R. and Ford, C. E. (2006). Sensing extracellular matrix: an update on discoidin domain receptor function. Cell. Signal. 18, 1108-1116.
38. Wakatsuki, T., Wysolmerski, R. B. and Elson, E. L. (2003). Mechanics of cell spreading: role of myosin II. J. Cell Sci. 116, 1617-1625.
39. Wang, C. Z., Hsu, Y. M. and Tang, M. J. (2005). Function of discoidin domain receptor I in HGF-induced branching tubulogenesis of MDCK cells in collagen gel. J. Cell Physiol. 203, 295-304.
40. Wang, C. Z., Su, H. W., Hsu, Y. C., Shen, M. R. and Tang, M. J. (2006). A discoidin domain receptor 1/SHP-2 signaling complex inhibits alpha2beta1-integrin-mediated signal transducers and activators of transcription 1/3 activation and cell migration. Mol. Biol. Cell 17, 2839-2852.
41. Yamaguchi, H. and Condeelis, J. (2007). Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim. Biophys. Acta 1773, 642-652.
42. Yeh, Y. C., Wang, C. Z. and Tang, M. J. (2009). Discoidin domain receptor 1 activation suppresses alpha2beta1 integrin-dependent cell spreading through inhibition of Cdc42 activity. J. Cell Physiol. 218, 146-156.
43. Yoshimura, T., Matsuyama, W. and Kamohara, H. (2005). Discoidin domain receptor 1, a new class of receptor regulating leukocyte-collagen interaction. Immunol. Res. 31, 219-230.
44. Zeng, W., Conibear, P. B., Dickens, J. L., Cowie, R. A., Wakelin, S., Malnasi-Csizmadia, A. and Bagshaw, C. R. (2004). Dynamics of actomyosin interactions in relation to the cross-bridge cycle. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359, 1843-1855.