Essential role of integrin-linked kinase in regulation of phagocytosis in keratinocytes

FASEB Journal

Volumn 26, Issue 10, 2012, Pages 4218-4229

  Sayedyahossein, Samar ^a,b,c   Nini, Lylia ^a,b,c   Irvine, Timothy S ^a,b,c   Dagnino, Lina ^a,b,c  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

^c LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

Epidermis; ILK; Melanosome; Particle engulfment; Rac1

Indexed keywords

INTEGRIN; INTEGRIN LINKED KINASE; KERATINOCYTE GROWTH FACTOR RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 2; RAC1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; KERATINOCYTE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PSEUDOPODIUM;

ADENOVIRIDAE; ANIMALS; CELLS, CULTURED; IMMUNOBLOTTING; KERATINOCYTES; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; PHAGOCYTOSIS; PROTEIN-SERINE-THREONINE KINASES; PSEUDOPODIA; RAC1 GTP-BINDING PROTEIN; RECEPTOR, PAR-2;

MUS;

EID: 84868130011     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-207852     Document Type: Article

References (47)

1. Flannagan, R. S., Jaumouille, V., and Grinstein, S. (2012) The cell biology of phagocytosis. Annu. Rev. Pathol. 7, 61-98
2. Botelho, R. J., and Grinstein, S. (2011) Phagocytosis. Curr. Biol. 21, R533-R538
3. Fens, M. H., van Wijk, R., Andringa, G., van Rooijen, K. L., Dijstelbloem, H. M., Rasmussen, J. T., de Vooght, K. M., Schiffelers, R. M., Gaillard, C. A., and van Solinge, W. W. (2012) A role for activated endothelial cells in red blood cell clearance: implications for vasopathology. Haematologica 97, 500-508
4. Van Den Bossche, K., Naeyaert, J.-M., and Lambert, J. (2006) The quest for the mechanism of melanin transfer. Traffic 7, 769-778
5. Virador, V. M., Muller, J., Wu, X., Abdel-Malek, Z. A., Yu, Z. X., Ferrans, V. J., Kobayashi, N., Wakamatsu, K., Ito, S., Hammer, J. A., and Hearing, V. J. (2002) Influence of alpha-melanocytestimulating hormone and ultraviolet radiation on the transfer of melanosomes to keratinocytes. FASEB J. 16, 105-107
6. Sharlow, E. R., Paine, C. S., Babiarz, L., Eisinger, M., Shapiro, S., and Seiberg, M. (2000) The protease-activated receptor-2 upregulates keratinocyte phagocytosis. J. Cell Sci. 113, 3093-3101
7. Cardinali, G., Ceccarelli, S., Kovacs, D., Aspite, N., Lotti, L. V., Torrisi, M. R., and Picardo, M. (2005) Keratinocyte growth factor promotes melanosome transfer to keratinocytes. J. Invest. Dermatol. 125, 1190-1199
8. Byers, H. R., Dykstra, S. G., and Boissel, S. J. (2007) Requirement of dynactin p150(Glued) subunit for the functional integrity of the keratinocyte microparasol. J. Invest. Dermatol. 127, 1736-1744
9. Ho, E., and Dagnino, L. (2012) Epidermal growth factor induction of front-rear polarity and migration in keratinocytes is mediated by integrin-linked kinase and ELMO2. Mol. Biol. Cell 23, 492-502
10. Ho, E., Irvine, T., Vilk, G. J., Lajoie, G., Ravichandran, K. S., D'Souza, S. J., and Dagnino, L. (2009) Integrin-linked kinase interactions with ELMO2 modulate cell polarity. Mol. Biol. Cell 20, 3033-3043
11. Nakrieko, K. A., Welch, I., Dupuis, H., Bryce, D. M., Pajak, A., St-Arnaud, R. S., Dedhar, S., D'Souza, S. J. A., and Dagnino, L. (2008) Impaired hair follicle morphogenesis and polarized keratinocyte movement upon conditional inactivation of integrin-linked kinase in the epidermis. Mol. Biol. Cell 19, 1462-1473
12. Wickstrom, S. A., Lange, A., Montanez, E., and Fassler, R. (2010) The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase! EMBO J. 29, 281-291
13. Lorenz, K., Grashoff, C., Torka, R., Sakai, T., Langbein, L., Bloch, W., Aumalley, M., and Fassler, R. (2007) Integrin-linked kinase is required for epidermal and hair follicle morphogenesis. J. Cell Biol. 177, 501-513
14. Nakrieko, K. A., Rudkouskaya, A., Irvine, T. S., D'Souza S, J., and Dagnino, L. (2011) Targeted inactivation of integrin-linked kinase in hair follicle stem cells reveals an important modulatory role in skin repair after injury. Mol. Biol. Cell 22, 2532-2540
15. Liu, E., Sinha, S., Williams, C., Cyrille, M., Heller, E., Snapper, S. B., Georgopoulos, K., St-Arnaud, R., Force, T., Dedhar, S., and Gerszten, R. E. (2005) Targeted deletion of integrin-linked kinase reveals a role in T-cell chemotaxis and survival. Mol. Cell. Biol. 25, 11145-11155
16. Rooney, N., and Streuli, C. H. (2011) How integrins control mammary epithelial differentiation: a possible role for the ILK-PINCH-Parvin complex. FEBS Lett. 585, 1663-1672
17. Terpstra, L., Prud'homme, J., Arabian, A., Takeda, S., Karsenty, G., Dedhar, S., and St-Arnaud, R. (2003) Reduced chondrocyte proliferation and chondrodysplasia in mice lacking the integrinlinked kinase in chondrocytes. J. Cell Biol. 162, 139-148
18. Dassule, H. R., Lewis, P., Bei, M., Maas, R., and McMahon, A. P. (2000) Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127, 4775-4785
19. Raghavan, S., Bauer, C., Mundschan, G., Li, Q., and Fuchs, E. (2000) Conditional ablation of beta1 integrin in skin. Severe defects in epidermal proliferation, basement membrane formation, and hair follicle invagination. J. Cell. Biol. 150, 1149-1160
20. Glogauer, M., Marchal, C. C., Zhu, F., Worku, A., Clausen, B. E., Foerster, I., Marks, P., Downey, G. P., Dinauer, M., and Kwiatkowski, D. J. (2003) Rac1 deletion in mouse neutrophils has selective effects on neutrophil functions. J. Immunol. 170, 5652-5657
21. Dagnino, L., Ho, E., and Chang, W. Y. (2010) Expression and analysis of exogenous proteins in epidermal cells. Methods Mol. Biol. 585, 93-105
22. Vespa, A., D'Souza, S. J. A., and Dagnino, L. (2005) A novel role for integrin-linked kinase in epithelial sheet morphogenesis. Mol. Biol. Cell 16, 4084-4095
23. Ivanova, I. A., Vespa, A., and Dagnino, L. (2007) A novel mechanism of E2F1 regulation via nucleocytoplasmic shuttling: determinants of nuclear import and export. Cell Cycle 6, 2186-2195
24. Ivanova, I. A., and Dagnino, L. (2007) Activation of p38- and CRM1-dependent nuclear export promotes E2F1 degradation during keratinocyte differentiation. Oncogene 26, 1147-1154
25. Enomoto, A., Yoshihisa, Y., Yamakoshi, T., Ur Rehman, M., Norisugi, O., Hara, H., Matsunaga, K., Makino, T., Nishihira, J., and Shimizu, T. (2011) UV-B radiation induces macrophage migration inhibitory factor-mediated melanogenesis through activation of protease-activated receptor-2 and stem cell factor in keratinocytes. Am. J. Pathol. 178, 679-687
26. Swanson, J. A. (2008) Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 9, 639-649
27. Koivusalo, M., Welch, C., Hayashi, H., Scott, C. C., Kim, M., Alexander, T., Touret, N., Hahn, K. M., and Grinstein, S. (2010) Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J. Cell Biol. 188, 547-563
28. Cardinali, G., Bolasco, G., Aspite, N., Lucania, G., Lotti, L. V., Torrisi, M. R., and Picardo, M. (2008) Melanosome transfer promoted by keratinocyte growth factor in light and dark skin-derived keratinocytes. J. Invest. Dermatol. 128, 558-567
29. Yoshida, H., Kunisada, T., Kusakabe, M., Nishikawa, S., and Nishikawa, S. I. (1996) Distinct stages of melanocyte differentiation revealed by anlaysis of nonuniform pigmentation patterns. Development 122, 1207-1214
30. Judah, D., Rudkouskaya, A., Wilson, R., Carter, D. E., and Dagnino, L. (2012) Multiple roles of integrin-linked kinase in epidermal development, maturation and pigmentation revealed by molecular profiling. PLoS One 7, e36704
31. Flannagan, R. S., Harrison, R. E., Yip, C. M., Jaqaman, K., and Grinstein, S. (2010) Dynamic macrophage "probing" is required for the efficient capture of phagocytic targets. J. Cell Biol. 191, 1205-1218
32. Zeigler, M. E., Chi, Y., Schmidt, T., and Varani, J. (1999) Role of ERK and JNK pathways in regulating cell motility and matrix metalloproteinase 9 production in growth factor-stimulated human epidermal keratinocytes. J. Cell. Physiol. 180, 271-284
33. Costa, C., Germena, G., and Hirsch, E. (2010) Dissection of the interplay between class I PI3Ks and Rac signaling in phagocytic functions. Sci. World J. 10, 1826-1839
34. Tzircotis, G., Braga, V. M., and Caron, E. (2011) RhoG is required for both FcgammaR- and CR3-mediated phagocytosis. J. Cell Sci. 124, 2897-2902
35. Hannigan, G. E., Leung-Hagesteijn, C., Fitz-Gibbon, L., Coppolino, M. G., Radeva, G., Filmus, J., Bell, J. C., and Dedhar, S. (1996) Regulation of cell adhesion and anchorage-dependent cell growth by a new beta 1-integrin-linked protein kinase. Nature 379, 91-96
36. Wang, Q. Q., Li, H., Oliver, T., Glogauer, M., Guo, J., and He, Y. W. (2008) Integrin beta 1 regulates phagosome maturation in macrophages through Rac expression. J. Immunol. 180, 2419-2428
37. Raghavan, S., Vaezi, A., and Fuchs, E. (2003) A role for αβ1 integrins in focal adhesion function and polarized cytoskeletal dynamics. Dev. Cell. 5, 415-427
38. Sindrilaru, A., Peters, T., Schymeinsky, J., Oreshkova, T., Wang, H., Gompf, A., Mannella, F., Wlaschek, M., Sunderkotter, C., Rudolph, K. L., Walzog, B., Bustelo, X. R., Fischer, K. D., and Scharffetter-Kochanek, K. (2009) Wound healing defect of Vav3-/- mice due to impaired-2-integrin-dependent macrophage phagocytosis of apoptotic neutrophils. Blood 113, 5266-5276
39. Mao, Y., and Finnemann, S. C. (2012) Essential diurnal Rac1 activation during retinal phagocytosis requires αβ5 integrin but not tyrosine kinases focal adhesion kinase or Mer tyrosine kinase. Mol. Biol. Cell 23, 1104-1114
40. Rosenberger, G., Gal, A., and Kutsche, K. (2005) aPIX associates with calpain4, the small subunit of calpain, and has a dual role in integrin-mediated cell spreading. J. Biol. Chem. 280, 6879-6889
41. Boulter, E., Grall, D., Cagnol, S., and Van Obberghen-Schilling, E. (2006) Regulation of cell-matrix adhesion dynamics and Rac-1 by integrin linked kinase. FASEB J. 20, 1489-1491
42. Belleudi, F., Purpura, V., Scrofani, C., Persechino, F., Leone, L., and Torrisi, M. R. (2011) Expression and signaling of the tyrosine kinase FGFR2b/KGFR regulates phagocytosis and melanosome uptake in human keratinocytes. FASEB J. 25, 170-181
43. Botelho, R. J., Teruel, M., Dierckman, R., Anderson, R., Wells, A., York, J. D., Meyer, T., and Grinstein, S. (2000) Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151, 1353-1368
44. Guidetti, G. F., Bernardi, B., Consonni, A., Rizzo, P., Gruppi, C., Balduini, C., and Torti, M. (2009) Integrin α2β1 induces phosphorylation-dependent and phosphorylation-independent activation of phospholipase Cγ2 in platelets: role of Src kinase and Rac GTPase. J. Thromb. Haemost. 7, 1200-1206
45. Auriemma, C., Viscardi, M., Tafuri, S., Pavone, L. M., Capuano, F., Rinaldi, L., Della Morte, R., Iovane, G., and Staiano, N. (2010) Integrin receptors play a role in the internalin B-dependent entry of Listeria monocytogenes into host cells. Cell. Mol. Biol. Lett. 15, 496-506
46. Siemens, N., Patenge, N., Otto, J., Fiedler, T., and Kreikemeyer, B. (2011) Streptococcus pyogenes M49 plasminogen/plasmin binding facilitates keratinocyte invasion via integrin-integrin-linked kinase (ILK) pathways and protects from macrophage killing. J. Biol. Chem. 286, 21612-21622
47. Uliczka, F., Kornprobst, T., Eitel, J., Schneider, D., and Dersch, P. (2009) Cell invasion of Yersinia pseudotuberculosis by invasin and YadA requires protein kinase C, phospholipase C-γ1 and Akt kinase. Cell. Microbiol. 11, 1782-1801