CCL11 and GM-CSF differentially use the Rho GTPase pathway to regulate motility of human eosinophils in a three-dimensional microenvironment

Journal of Immunology

Volumn 180, Issue 12, 2008, Pages 8354-8360

  Muessel, Michelle J ^a   Scott, Karen S ^a   Friedl, Peter ^b   Bradding, Peter ^a   Wardlaw, Andrew J ^a,c  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c GLENFIELD HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAMBETA2 INTEGRIN; COMPLEMENT COMPONENT C5A; EOTAXIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTEGRIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; UNCLASSIFIED DRUG; BLOCKING ANTIBODY; CALCIUM; CCL11 PROTEIN, HUMAN; CD11B ANTIGEN; CHELATING AGENT; COLLAGEN TYPE 1; EDETIC ACID; ITGAM PROTEIN, HUMAN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA PROTEIN, HUMAN;

ARTICLE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; EOSINOPHIL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; COMPARATIVE STUDY; CYTOLOGY; DRUG ANTAGONISM; ENZYMOLOGY; GEL; IMMUNOLOGY; LEUKOCYTE MIGRATION INHIBITION TEST; METABOLISM; NEUTROPHIL CHEMOTAXIS; PHYSIOLOGY;

ANTIBODIES, BLOCKING; ANTIGENS, CD11B; CALCIUM; CELL MIGRATION INHIBITION; CHELATING AGENTS; CHEMOKINE CCL11; CHEMOTAXIS, LEUKOCYTE; COLLAGEN TYPE I; COMPLEMENT C5A; EDETIC ACID; EOSINOPHILS; GELS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 50949122360     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.12.8354     Document Type: Article

References (52)

1. Wardlaw, A. 1999. Molecular basis for selective eosinophil trafficking in asthma: a multistcp paradigm. J. Allergy Clin. Immunol. 104: 917-926.
2. Saetta, M., and G. Turato. 2001. Airway pathology in asthma. Eur. Respir. J. 18: 18S-23S.
3. Wills-Karp, M., and C. L. Karp. 2004. Eosinophils in asthma: remodeling a tangled tale. Science 305: 1726-1729.
4. Kay, A. B. 2005. The role of eosinophils in the pathogenesis of asthma. Trends Mol. Med. 11: 148-152.
5. Brightling, C. E., P. Bradding, F. A. Symon, S. T. Holgate, A. J. Wardlaw, and I. D. Pavord. 2002. Mast-cell infiltration of airway smooth muscle in asthma. N. Engl. J. Med. 346: 1699-1705.
6. Brightling, C., and I. D. Pavord. 2004. Location, location, location: microlocalization of inflammatory cells and airway dysfunction. Thorax 59: 734-735.
7. Fukala, M., M. Nakagawa, and K. Kaibuchi. 2003. Roles of Rho-family GTPases in cell polarisation and directional migration. Curr. Opin. Cell Biol. 15:590-597.
8. Raftopoulou, M., and A. Hall. 2004. Cell migration: Rho GTPases lead the way. Dev. Biol. 265: 23-32.
9. Niggli, V. 2003. Signaling to migration in neutrophils: importance of localized pathways. Int. J. Biochem. Cell. Biol. 35: 1619-1638.
10. Riento, K., and A. J. Ridley. 2003. Rocks: multifunctional kinases in cell behaviour. Nat. Rev. Mol. Cell Biol. 4: 446-456.
11. Sahai, E., and C. J. Marshall. 2003. Differing modes of tumor cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell. Biol. 5:711-719.
12. Nakayama, M., M. Amano, A. Katsumi, T. Kaneko, S. Kawabata, M. Takefuji, and K. Kaibuchi. 2005. Rho-kinase and myosin II activities are required for cell type and environment specific migration. Genes Cells 10: 107-117.
13. Niggli, V., M. Schmid, and A. Nievergelt. 2006. Differential roles of Rho-kinase and myosin light chain kinase in regulating shape, adhesion, and migration of HT1080 fibrosarcoma cells. Biochem. Biophys. Res. Commun. 343: 602-608.
14. Friedl, P., and E. B. Bröcker. 2000. The biology of cell locomotion within three-dimensional extracellular matrix. Cell. Mol. Life Sci. 57: 41-64.
15. Martins, G. G., and J. Kolega. 2006. Endothelial cell protrusion and migration in three-dimensional collagen matrices. Cell Motil. Cytoskeleton 63: 101-115.
16. Bousquet, J., P. K. Jeffery, W. W. Busse, M. Johnson, and A. M. Vignola. 2000. Asthma: from bronchoconstriction to airways inflammation and remodeling. Am. J. Respir. Crit. Care Med. 161: 1720-1745.
17. Bergeron, C., and L.-P. Boulet. 2006. Structural changes in airway diseases: characteristics, mechanisms, consequences, and pharmacologic modulation. Chest 129: 1068-1087.
18. Friedl, P., and E. Brocker. 2004. Reconstructing leukocyte migration in 3D extracellular matrix by time-lapse videomicroscopy and computer-assisted tracking. Methods Mol. Biol. 239: 77-90.
19. Lantero, S., G. Alessandri, D. Spallarossa, L. Scarso, and G. A. Rossi. 1998. LFA-1 expression by blood eosinophils is increased in atopic asthmatic children and is involved in eosinophil locomotion. Eur. Respir. J. 12: 1094-1098.
20. Ying, S., Q. Meng, K. Zeibecoglou, D. S. Robinson, A. Macfarlane, M. Humbert, and A. B. Kay. 1999. Eosinophil chcmotactic chemokines (eotaxin, eotaxin-2, RANTES, monocyte chemoattractant protein-3 (MCP-3), and MCP-4), and C-C chcmokine receptor 3 expression in bronchial biopsies from atopic and nonatopic (intrinsic) asthmatics. J. Immunol. 163: 6321-6329.
21. Teran, L. M. 2000. CCL chemokines and asthma. Immunol. Today 21: 235-242.
22. Alblas, J., L. Ulfman, P. Hordijk, and L. Koenderman. 2001. Activation of RhoA and ROCK are essential for detachment of migrating leukocytes. Mol. Biol. Cell 12: 2137-2145.
23. Hynes, R. 2002. Integrins: bidirectional, allosteric signaling molecules. Celt 110: 673-687.
24. Brundage, R., K. Fogarty, R. Tuft, and F. Fay. 1991. Calcium gradients underlying polarization and chemotaxis of eosinophils. Science 254: 703-706.
25. 2+. Am. J. Respir. Cell Mol. Biol. 28:713-721.
26. Ishizaki, T., M. Uehata, I. Tamechika, J. Keel, K. Nonomura, M. Maekawa, and S. Nammiya. 2000. Pharmacological properties of Y-27632, a specific inhibitor of Rho-associated kinases. Mol. Pharmacol. 57: 976-983.
27. Suki, B., S. Ito, D. Stamenovic, K. Lutchen, and E. Ingenito. 2005. Biomechanics of the luns parenchyma: critical roles of collagen and mechanical forces. J. Appl. Physiol. 98: 1892-1899.
28. 1 integrin-independent strategies for polarization, interaction with collagen fibers, and migration. Eur. J. Immunol. 28: 2331-2343.
29. Collins, P., S. Marleau, D. Griffiths-Johnson, P. Jose, and T. Williams. 1995. Cooperation between interleukin-5 and the chemokine eotaxin to induce eosinophil recruitment in vivo. J. Exp. Med. 182: 1169-1174.
30. Mould, A., K. Matthaei, I. Young, and P. Foster. 1997. Relationship between interleukin-5 and eotaxin in regulating blood and tissue eosinophilia in mice. J. Clin. Invest. 99: 1064-1071.
31. Zeibecoglou, K., S. Ying, Q. Meng, A. B. Kay, and D. S. Robinson. 2000. Expression of eotaxin in induced sputum of atopic and nonatopic asthmatics. Allergy 55: 1042-1048.
32. Pope, S., N. Zimmerman, K. Stringer, M. Karow, and M. Rothenberg. 2005. The eotaxin chemokines and CCR3 are fundamental regulators of allergen-induced pulmonary eosinophilia. J. Immunol. 175: 5341-5350.
33. Okada, S., II. Kita, T. George, G. Gleich, and K. Leiferman. 1996. Migration of eosinophils through basement membrane components in vitro: role of matrix metalloproteinase-9. Am. J. Respir. Cell Mol. Biol. 17: 519-528.
34. Wolf, K., R. Muller, S. Borgmann, E. Brocker, and P. Friedl. 2003. Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood 102: 3262-3269.
35. Sundqvist, K.-G., D. Hauzenberger, K. Hultenby, and S.-E. Bergstrom. 1993. T-lymphocyte infiltration of two- and three-dimensional collagen substrata by an adhesive mechanism. Exp. Cell Res. 206: 100-110.
36. Elenstrom-Magnusson, C., W. Chen, B. Clinchy, B. Obrink, and E. Severison. 1995. IL-4-induced B cell migration involves transient interactions between integrins and extracellular matrix components. Int. Immunol. 7: 567-573.
37. 1 integrins are critically involved in neutrophil locomotion in extrvascular tissue in vivo. J. Exp. Med. 187: 2091-2096.
38. Palecek, S., J. Loftus, M. Gisberg, D. Lauffenburger, and A. Horwitz. 1997. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385: 537-540.
39. Xu, J., F. Wang, A. van Keymeulen, P. Herzmark, A. Straight, K. Kelly, Y. Takuwa, N. Sugimoto, T. Mitchison, and H. Bourne. 2003. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114: 201-214.
40. Li. Z., X. Dong, Z. Wang, W. Liu, N. Deng, Y. Ding, L. Tang, T. Hla, R. Zeng, L. Li, and D. Wu. 2005. Regulation of PTEN by Rho small GTPases. Nat. Cell. Biol. 7: 399-404.
41. Adachi, T., R. Vita, S. Sannohe, S. Stafford, R. Alam, H. Kayaba, and J. Chihara. 2001. The functional role of Rho and Rho-associated coiled-coil forming protein kinase in eotaxin signaling in eosinophils. J. Immunol. 167: 4609-4615.
42. Kurokawa, K., and M. Matsuda. 2005. Localized RhoA activation as a requirement for the induction of membrane ruffling. Mol. Biol. Cell 16: 4294-4303.
43. Pertz, O., L. Hodgson, R. L. Klemke, and K. M. Hahn. 2006. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440: 1069-1072.
44. Worthylake, R., S. Lemoine, J. Watson, and K. Burridge. 2001. RhoA is required for monocyte tail retraction during transendothelial miaration. J. Cell Biol. 154: 147-160.
45. Sander, E., J. ten Klooster, F. van Delft, R. van der Kammen, and J. Collard. 1999. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147: 1009-1022.
46. Nimnual, A. S., L. J. Taylor, and D. Bar-Sagi. 2003. Redox-dependent down-regulation of Rho by Rac. Nat. Cell Biol. 5: 236-241.
47. Ward, Y., S. Yap, V. Ravichandran, F. Matsumura, M. Ito, B. Spinelli, and K. Kelly. 2002. The GTP binding proteins Gem and Rad are negative regulators of the Rho-Rho kinase pathway. J. Cell Biol. 157: 291-302.
48. Riento, K., R. Guasch, R. Garg, B. Jin, and A. J. Ridley. 2003. RhoE binds to ROCK I and inhibits downstream signaling. Mol. Cell. Biol. 23: 4219-4229.
49. Guasch, R., P. Scambler, G. Jones, and A. J. Ridley. 1998. RhoE regulates actin cytoskeleton organization and cell migration. Mol. Biol. Cell 18: 4761-4771.
50. Torka, R., F. Thuma, V. Herzog, and G. Kirfel. 2006. ROCK signaling mediates the adoption of different modes of migration and invasion in human mammary epithelial tumor cells. Exp. Cell Res. 312: 3857-3871.
51. Henry, P. J., T. S. Mann, and R. G. Goldie. 2005. A Rho kinase inhibitor, Y-27632 inhibits pulmonary eosinophilia, bronchoconstriction and airways hy-perresponsiveness in allergic mice. Pulm. Pharmacol. Ther. 18: 67-74.
52. Taki, F., H. Kume, T. Kobayashi, H. Ohta, H. Aratake, and K. Shimokata. 2007. Effects of Rho-kinase inactivation on eosinophilia and hyper-reactivity in murine airways by allergen challenges. Clin. Exp. Allergy 37: 599-607.