LFA-1-induced T cell migration on ICAM-1 involves regulation of MLCK-mediated attachment and ROCK-dependent detachment

Journal of Cell Science

Volumn 116, Issue 15, 2003, Pages 3123-3133

  Smith, Andrew ^a   Bracke, Madelon ^a,b   Leitinger, Birgit ^a,c   Porter, Joanna C ^a,c   Hogg, Nancy ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

LFA 1; Migration; MLCK; Rho kinase; T lymphocyte

Indexed keywords

CALMODULIN; F ACTIN; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN LIGHT CHAIN KINASE; RHO KINASE;

CELL ADHESION; CELL COMPARTMENTALIZATION; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME REGULATION; HUMAN; LYMPHOCYTE MIGRATION; POLARIZATION; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MICROSCOPY, CONFOCAL; MICROSCOPY, VIDEO; MYOSIN-LIGHT-CHAIN KINASE; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 0041384357     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00606     Document Type: Review

References (48)

1. Alblas, J., Ulfman, L., Hordijk, P. and Koenderman, L. (2001). Activation of Rhoa and ROCK are essential for detachment of migrating leukocytes. Mol. Biol. Cell 12, 2137-2145.
2. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y. and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rho-associated kinase (Rho- kinase). J. Biol. Chem. 271, 20246-20249.
3. Berendt, A. R., McDowall, A., Craig, A. G., Bates, P. A., Sternberg, M. J., Marsh, K., Newbold, C. I. and Hogg, N. (1992). The binding site on ICAM-1 for Plasmodium falciparum-infected erythrocytes overlaps, but is distinct from, the LFA-1 binding site. Cell 68, 71-81.
4. Birukov, K. G., Schavocky, J. P., Shirinsky, V. P., Chibalina, M. V., van Eldik, L. J. and Watterson, D. M. (1998). Organization of the genetic locus for chicken myosin light chain kinase is complex: multiple proteins are encoded and exhibit differential expression and localization. J. Cell Biochem. 70, 402-413.
5. Blue, E. K., Goeckeler, Z. M., Jin, Y., Hou, L., Dixon, S. A., Herring, B. P., Wysolmerski, R. B. and Gallagher, P. J. (2002). 220- and 130-kDa MLCKs have distinct tissue distributions and intracellular localization patterns. Am. J. Physiol. Cell Physiol. 282, C451-C460.
6. Bresnick, A. R. (1999). Molecular mechanisms of nonmuscle myosin-II regulation. Curr Opin. Cell Biol. 11, 26-33.
7. Chew, T.-L., Wolf, W. A., Gallagher, P. J., Matsumura, E. and Chisholm, R. L. (2002). A flourescent resonant energy transfer-based biosensor reveals transient and regional myosin light chain kinase activation in lamella and cleavage furrows. J. Cell Biol. 156, 543-553.
8. Darzynkiewicz, Z., Bedner, E., Li, X., Gorczyca, W. and Melamed, M. R. (1999). Laser-scanning cytometry: a new instrumentation with many applications. Exp. Cell Res. 249, 1-12.
9. Davies, S. P., Reddy, H., Caivano, M. and Cohen, P. (2000). Specificity and mechanism of action of commonly used protein kinase inhibitors. Biochem. J. 351, 95-105.
10. Dransfield, I., Cabanas, C., Craig, A. and Hogg, N. (1992). Divalent cation regulation of the function of the leukocyte integrin LFA-1. J. Cell Biol. 116, 219-226.
11. 2+pendent myosin II activation is required for uropod retraction during neutrophil migration. J. Cell Sci. 113, 1287-1298.
12. Friedl, P. and Gunzer, M. (2001). Interaction of T cells with APCs: the serial encounter model. Trends Immunol. 22, 187-191.
13. Fukata, Y., Kimura, K., Oshiro, N., Saya, H., Matsuura, Y. and Kaibuchi, K. (1998). Association of the myosin-binding subunit of myosin phosphatase and moesin: dual regulation of moesin phosphorylation by Rho-associated kinase and myosin phosphatase. J. Cell Biol. 141, 409-418.
14. Fukata, Y., Oshiro, N., Kinoshita, N., Kawano, Y., Matsuoka, Y., Bennett, V., Matsuura, Y. and Kaibuchi, K. (1999). Phosphorylation of adducin by Rho-kinase plays a crucial role in cell motility. J. Cell Biol. 145, 347-361.
15. Horwitz, A. R. and Parsons, J. T. (1999). Cell migration-movin' on. Science 286, 1102-1103.
16. Ishizaki, T., Maekawa, M., Fujisawa, K., Okawa, K., Iwamatsu, A., Fujita, A., Watanabe, N., Saito, Y., Kakizuka, A., Morii, N. et al. (1996). The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy Kinase. EMBO J. 15, 1885-1893.
17. Kamm, K. E. and Stull, J. T. (2001). Dedicated myosin light chain kinases with diverse cellular functions. J. Biol. Chem. 276, 4527-4530.
18. Katoh, K., Kano, Y., Amano, M., Kaibuchi, K. and Fujiwara, K. (2001). Stress fiber organization regulated by MLCK and Rho-kinase in cultured human fibroblasts. Am. J. Physiol. Cell Physiol. 280, C1669-C1679.
19. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K. et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
20. Kishi, H., Mikawa, T., Seto, M., Sasaki, Y., Kanayasu-Toyoda, T., Yamaguchi, T., Imamura, M., Ito, M., Karaki, H., Bao, J. et al. (2000). Stable transfectants of smooth muscle cell line lacking the expression of myosin light chain kinase and their characterization with respect to the actomyosin system. J. Biol. Chem. 275, 1414-1420.
21. Kosako, H., Amano, M., Yanagida, M., Tanabe, K., Nishi, Y., Kaibuchi, K. and Inagaki, M. (1997). Phosphorylation of glial fibrillary acidic protein at the same sites by cleavage furrow kinase and Rho-associated kinase. J. Biol. Chem. 272, 10333-10336.
22. Kudryashov, D. S., Chibalina, M. V., Birukov, K. G., Lukas, T. J., Sellers, J. R., van Eldik, L. J., Watterson, D. M. and Shirinsky, V. P. (1999). Unique sequence of a high molecular weight myosin light chain kinase is involved in interaction with actin cytoskeleton. FEBS Lett. 463, 67-71.
23. Lazar, V. and Garcia, J. G. (1999). A single human myosin light chain kinase gene (MLCK; MYLK). Genomics 57, 256-267.
24. Lukas, T. J., Burgess, W. H., Prendergast, F. G., Lau, W. and Martin Watterson, D. (1986). Calmodulin binding domains: characterization of a phosphorylation and calmodulin binding site from myosin light chain kinase. Biochemistry 25, 1458-1464.
25. Miller, M. J., Wei, S. H., Cahalan, M. D. and Parker, I. (2003). Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy. Proc. Natl. Acad. Sci. USA 100, 2604-2609.
26. Niggli, V. (1999). Rho-kinase in human neutrophils: a role in signalling for myosin light chain phosphorylation and cell migration. FEBS Lett. 445, 69-72.
27. Poperechnaya, A., Varlamova, O., Lin, P. J., Stull, J. T. and Bresnick, A. R. (2000). Localization and activity of myosin light chain kinase isoforms during the cell cycle. J. Cell Biol. 151, 697-708.
28. Porter, J. C. and Hogg, N. (1997). Integrin cross talk: activation of lymphocyte function-associated antigen-1 on human T cells alters alpha4beta1- and alpha5beta1-mediated function. J. Cell Biol. 138, 1437-1447.
29. Porter, J. C., Bracke, M., Smith, A., Davies, D. and Hogg, N. (2002). Signaling through integrin LFA-1 leads to filamentous actin polymerization and remodeling, resulting in enhanced T cell adhesion. J. Immunol. 168, 6330-6335.
30. Ren, X. D., Kiosses, W. B. and Schwartz, M. A. (1999). Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18, 578-585.
31. Ridley, A. J. (2001). Rho family proteins: coordinating cell responses. Trends Cell Biol. 11, 471-477.
32. Saitoh, M., Ishikawa, T., Matsushima, S., Naka, M. and Hidaka, H. (1987). Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J. Biol. Chem. 262, 7796-7801.
33. Sanders, L. C., Matsumura, E., Bokoch, G. M. and de Lanerolle, P. (1999). Inhibition of myosin light chain kinase by p21-activated kinase. Science 283, 2083-2085.
34. Serrador, J. M., Nieto, M. and Sanchez-Madrid, F. (1999). Cytoskeletal rearrangement during migration and activation of T lymphocytes. Trends Cell Biol. 9, 228-233.
35. Smith, L., Parizi-Robinson, M., Zhu, M. S., Zhi, G., Fukui, R., Kamm, K. E. and Stull, J. T. (2002). Properties of long Myosin light chain kinase binding to f-actin in vitro and in vivo. J. Biol. Chem. 277, 35597-35604.
36. Smith, L., Su, X., Lin, P., Zhi, G. and Stull, J. T. (1999). Identification of a novel actin binding motif in smooth muscle myosin light chain kinase. J. Biol. Chem. 274, 29433-29438.
37. Stewart, M. and Hogg, N. (1996). Regulation of leukocyte integrin function: affinity vs. avidity. J. Cell Biochem. 61, 554-561.
38. Sumi, T., Matsumoto, K. and Nakamura, T. (2001). Specific activation of LIM kinase 2 via phosphorylation of threonine 505 by ROCK, a Rho-dependent protein kinase. J. Biol. Chem. 276, 670-676.
39. Tanaka, M., Ikebe, R., Matsuura, M. and Ikebe, M. (1995). Pseudosubstrate sequence may not be critical for autoinhibition of smooth muscle myosin light chain kinase. EMBO J. 14, 2839-2846.
40. Tominaga, T., Ishizaki, T., Narumiya, S. and Barber, D. L. (1998). p160ROCK mediates RhoA activation of Na-H exchange. EMBO J. 17, 4712-4722.
41. Totsukawa, G., Yamakita, Y., Yamashiro, S., Hartshorne, D. J., Sasaki, Y. and Matsumura, F. (2000). Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150, 797-806.
42. van Kooyk, Y. and Figdor, C. G. (2000). Avidity regulation of integrins: the driving force in leukocyte adhesion. Curr. Opin. Cell Biol. 12, 542-547.
43. Volkov, Y., Long, A., McGrath, S., Ni Eidhin, D. and Kelleher, D. (2001). Crucial importance of PKC-beta(I) in LFA-1-mediated locomotion of activated T cells. Nat. Immunol. 2, 508-514.
44. Walker, J. W., Gilbert, S. H., Drummond, R. M., Yamada, M., Sreekumar, R., Carraway, R. E., Ikebe, M. and Fay, F. S. (1998). Signaling pathways underlying eosinophil cell motility revealed by using caged peptides. Proc. Natl. Acad. Sci. USA 95, 1568-1573.
45. Worthylake, R. A. and Burridge, K. (2001). Leukocyte transendothelial migration: orchestrating the underlying molecular machinery. Curr. Opin. Cell Biol. 13, 569-577.
46. Worthylake, R. A., Lemoine, S., Watson, J. M. and Burridge, K. (2001). RhoA is required for monocyte tail retraction during transendothelial migration. J. Cell Biol. 154, 147-160.
47. Wulfing, C. and Davis, M. M. (1998). A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282, 2266-2269.
48. Ye, L. H., Kishi, H., Nakamura, A., Okagaki, T., Tanaka, T., Oiwa, K. and Kohama, K. (1999). Myosin light-chain kinase of smooth muscle stimulates myosin ATPase activity without phosphorylating myosin light chain. Proc. Natl. Acad. Sci. USA 96, 6666-6671.