Protein kinase D isoforms are dispensable for integrin-mediated lymphocyte adhesion and homing to lymphoid tissues

European Journal of Immunology

Volumn 42, Issue 5, 2012, Pages 1316-1326

  Matthews, Sharon A ^a   San Lek, Hwee ^a   Morrison, Vicky L ^a   Mackenzie, Matthew G ^a   Zarrouk, Marouan ^b   Cantrell, Doreen ^b   Fagerholm, Susanna C ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Adhesion; Integrin; Lymphocyte; PKC; Protein kinase D (PKD)

Indexed keywords

B LYMPHOCYTE RECEPTOR; BETA1 INTEGRIN; FIBRONECTIN; INTERCELLULAR ADHESION MOLECULE 1; ISOPROTEIN; LIGAND; PHORBOL ESTER; PROTEIN KINASE D; RAP1 PROTEIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL ADHESION; CELL ASSAY; CONCENTRATION RESPONSE; CONTROLLED STUDY; FLOW CYTOMETRY; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE HOMING; LYMPHOCYTE MIGRATION; LYMPHOID TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SHEAR FLOW; SHEAR STRESS; SIGNAL TRANSDUCTION; SPLEEN CELL;

ANIMALS; B-LYMPHOCYTES; CELL ADHESION; CELLS, CULTURED; GTPASE-ACTIVATING PROTEINS; INTEGRINS; ISOENZYMES; LYMPHOCYTES; LYMPHOID TISSUE; MICE; PHORBOL ESTERS; PROTEIN KINASES; RECEPTORS, ANTIGEN, B-CELL;

EID: 84860330197     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201142004     Document Type: Article

References (55)

1. Hogg, N., Patzak, I. and Willenbrock, F., The insider's guide to leukocyte integrin signalling and function. Nat. Rev. Immunol. 2011. 11: 416-426.
2. Gahmberg, C. G., Fagerholm, S. C., Nurmi, S. M., Chavakis, T., Marchesan, S. and Gronholm, M., Regulation of integrin activity and signalling. Biochim. Biophys. Acta 2009. 1790: 431-444.
3. Larjava, H., Plow, E. F. and Wu, C., Kindlins: essential regulators of integrin signalling and cell-matrix adhesion. EMBO Rep. 2008. 9: 1203-1208.
4. Andrew, D. P., Spellberg, J. P., Takimoto, H., Schmits, R., Mak, T. W. and Zukowski, M. M., Transendothelial migration and trafficking of leukocytes in LFA-1-deficient mice. Eur. J. Immunol. 1998. 28: 1959-1969.
5. Berlin-Rufenach, C., Otto, F., Mathies, M., Westermann, J., Owen, M. J., Hamann, A. and Hogg, N., Lymphocyte migration in lymphocyte function-associated antigen (LFA)-1-deficient mice. J. Exp. Med. 1999. 189: 1467-1478.
6. Lu, T. T. and Cyster, J. G., Integrin-mediated long-term B cell retention in the splenic marginal zone. Science 2002. 297: 409-412.
7. Lo, C. G., Lu, T. T. and Cyster, J. G., Integrin-dependence of lymphocyte entry into the splenic white pulp. J. Exp. Med. 2003. 197: 353-361.
8. Schmits, R., Kundig, T. M., Baker, D. M., Shumaker, G., Simard, J. J., Duncan, G. et al., LFA-1-deficient mice show normal CTL responses to virus but fail to reject immunogenic tumor. J. Exp. Med. 1996. 183: 1415-1426.
9. Scharffetter-Kochanek, K., Lu, H., Norman, K., van Nood, N., Munoz, F., Grabbe, S., McArthur, M. et al., Spontaneous skin ulceration and defective T cell function in CD18 null mice. J. Exp. Med. 1998. 188: 119-131.
10. Carrasco, Y. R. and Batista, F. D., B cell recognition of membrane-bound antigen: an exquisite way of sensing ligands. Curr. Opin. Immunol. 2006. 18: 286-291.
11. Carrasco, Y. R. and Batista, F. D., B-cell activation by membrane-bound antigens is facilitated by the interaction of VLA-4 with VCAM-1. Embo. J. 2006. 25: 889-899.
12. Carrasco, Y. R., Fleire, S. J., Cameron, T., Dustin, M. L. and Batista, F. D., LFA-1/ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity 2004. 20: 589-599.
13. Pabst, O., Peters, T., Czeloth, N., Bernhardt, G., Scharffetter-Kochanek, K. and Forster, R., Cutting edge: egress of newly generated plasma cells from peripheral lymph nodes depends on beta 2 integrin. J. Immunol. 2005. 174: 7492-7495.
14. Peters, T., Bloch, W., Wickenhauser, C., Tawadros, S., Oreshkova, T., Kess, D., Krieg, T. et al., Terminal B cell differentiation is skewed by deregulated interleukin-6 secretion in beta2 integrin-deficient mice. J. Leukoc. Biol. 2006. 80: 599-607.
15. Graf, B., Bushnell, T. and Miller, J., LFA-1-mediated T cell costimulation through increased localization of TCR/class II complexes to the central supramolecular activation cluster and exclusion of CD45 from the immunological synapse. J. Immunol. 2007. 179: 1616-1624.
16. Han, J., Lim, C. J., Watanabe, N., Soriani, A., Ratnikov, B., Calderwood, D. A., Puzon-McLaughlin, W. et al., Reconstructing and deconstructing agonist-induced activation of integrin alphaIIbbeta3. Curr. Biol. 2006. 16: 1796-1806.
17. Sebzda, E., Bracke, M., Tugal, T., Hogg, N. and Cantrell, D. A., Rap1A positively regulates T cells via integrin activation rather than inhibiting lymphocyte signaling. Nat. Immunol. 2002. 3: 251-258.
18. Ebisuno, Y., Katagiri, K., Katakai, T., Ueda, Y., Nemoto, T., Inada, H., Nabekura, J. et al., Rap1 controls lymphocyte adhesion cascade and interstitial migration within lymph nodes in RAPL-dependent and -independent manners. Blood 2010. 115: 804-814.
19. Manevich-Mendelson, E., Grabovsky, V., Feigelson, S. W., Cinamon, G., Gore, Y., Goverse, G., Monkley, S. J. et al., Talin1 is required for integrin-dependent B lymphocyte homing to lymph nodes and the bone marrow but not for follicular B-cell maturation in the spleen. Blood 2010. 116: 5907-5918.
20. McDowall, A., Svensson, L., Stanley, P., Patzak, I., Chakravarty, P., Howarth, K., Sabnis, H. et al., Two mutations in the KINDLIN3 gene of a new leukocyte adhesion deficiency III patient reveal distinct effects on leukocyte function in vitro. Blood 2010. 115: 4834-4842.
21. Svensson, L., Howarth, K., McDowall, A., Patzak, I., Evans, R., Ussar, S., Moser, M. et al., Leukocyte adhesion deficiency-III is caused by mutations in KINDLIN3 affecting integrin activation. Nat. Med. 2009. 15: 306-312.
22. Malinin, N. L., Zhang, L., Choi, J., Ciocea, A., Razorenova, O., Ma, Y. Q., Podrez, E. A. et al. A point mutation in KINDLIN3 ablates activation of three integrin subfamilies in humans. Nat. Med. 2009. 15: 313-318.
23. Moser, M., Bauer, M., Schmid, S., Ruppert, R., Schmidt, S., Sixt, M., Wang, H. V. et al., Kindlin-3 is required for beta2 integrin-mediated leukocyte adhesion to endothelial cells. Nat. Med. 2009. 15: 300-305.
24. Katagiri, K., Shimonaka, M. and Kinashi, T., Rap1-mediated lymphocyte function-associated antigen-1 activation by the T cell antigen receptor is dependent on phospholipase C-gamma1. J. Biol. Chem. 2004. 279: 11875-11881.
25. Ghandour, H., Cullere, X., Alvarez, A., Luscinskas, F. W. and Mayadas, T. N., Essential role for Rap1 GTPase and its guanine exchange factor CalDAG-GEFI in LFA-1 but not VLA-4 integrin mediated human T-cell adhesion. Blood 2007. 110: 3682-3690.
26. Letschka, T., Kollmann, V., Pfeifhofer-Obermair, C., Lutz-Nicoladoni, C., Obermair, G. J., Fresser, F., Leitges, M. et al., PKC-theta selectively controls the adhesion-stimulating molecule Rap1. Blood 2008. 112: 4617-4627.
27. Medeiros, R. B., Dickey, D. M., Chung, H., Quale, A. C., Nagarajan, L. R., Billadeau, D. D. and Shimizu, Y., Protein kinase D1 and the beta1 integrin cytoplasmic domain control beta1 integrin function via regulation of Rap1 activation. Immunity 2005. 23: 213-226.
28. Woods, A. J., White, D. P., Caswell, P. T. and Norman, J. C., PKD1/PKCmu promotes alpha v beta3 integrin recycling and delivery to nascent focal adhesions. Embo. J. 2004. 23: 2531-2543.
29. White, D. P., Caswell, P. T. and Norman, J. C., Alpha v beta3 and alpha5beta1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration. J. Cell Biol. 2007. 177: 515-525.
30. di Blasio, L., Droetto, S., Norman, J., Bussolino, F. and Primo, L., Protein kinase D1 regulates VEGF-A-induced alphavbeta3 integrin trafficking and endothelial cell migration. Traffic 2010. 11: 1107-1118.
31. Brenner, W., Beitz, S., Schneider, E., Benzing, F., Unger, R. E., Roos, F. C., Thuroff, J. W. et al., Adhesion of renal carcinoma cells to endothelial cells depends on PKCmu. BMC Cancer 2010. 10: 183.
32. Kim, M., Jang, H. R., Kim, J. H., Noh, S. M., Song, K. S., Cho, J. S., Jeong, H. Y. et al., Epigenetic inactivation of protein kinase D1 in gastric cancer and its role in gastric cancer cell migration and invasion. Carcinogenesis 2008. 29: 629-637.
33. Eiseler, T., Schmid, M. A., Topbas, F., Pfizenmaier, K. and Hausser, A., PKD is recruited to sites of actin remodelling at the leading edge and negatively regulates cell migration. FEBS Lett. 2007. 581: 4279-4287.
34. Simpson, K. J., Selfors, L. M., Bui, J., Reynolds, A., Leake, D., Khvorova, A. and Brugge, J. S., Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat. Cell Biol. 2008. 10: 1027-1038.
35. Eiseler, T., Doppler, H., Yan, I. K., Kitatani, K., Mizuno, K. and Storz, P., Protein kinase D1 regulates cofilin-mediated F-actin reorganization and cell motility through slingshot. Nat. Cell Biol. 2009. 11: 545-556.
36. Peterburs, P., Heering, J., Link, G., Pfizenmaier, K., Olayioye, M. A. and Hausser, A., Protein kinase D regulates cell migration by direct phosphorylation of the cofilin phosphatase slingshot 1 like. Cancer Res. 2009. 69: 5634-5638.
37. Matthews, S. A., Navarro, M. N., Sinclair, L. V., Emslie, E. A., Feijoo-Carnero, M. C. and Cantrell, D., Unique functions for protein kinase D1 and protein kinase D2 in mammalian cells. Biochem. J. 2010.
38. Chavakis, E., Choi, E. Y. and Chavakis, T., Novel aspects in the regulation of the leukocyte adhesion cascade. Thromb. Haemost. 2009. 102: 191-197.
39. Nagel, A. C., Schmid, J., Auer, J. S., Preiss, A. and Maier, D., Constitutively active protein kinase D acts as negative regulator of the Slingshot-phosphatase in Drosophila. Hereditas. 2010. 147: 237-242.
40. Eiseler, T., Hausser, A., De Kimpe, L., Van Lint, J. and Pfizenmaier, K., Protein kinase D controls actin polymerization and cell motility through phosphorylation of cortactin. J. Biol. Chem. 2010. 285: 18672-18683.
41. Matthews, S. A., Liu, P., Spitaler, M., Olson, E. N., McKinsey, T. A., Cantrell, D. A. and Scharenberg, A. M., Essential role for protein kinase D family kinases in the regulation of class II histone deacetylases in B lymphocytes. Mol. Cell Biol. 2006. 26: 1569-1577.
42. Patarroyo, M., Beatty, P. G., Fabre, J. W. and Gahmberg, C. G., Identification of a cell surface protein complex mediating phorbol ester-induced adhesion (binding) among human mononuclear leukocytes. Scand. J. Immunol. 1985. 22: 171-182.
43. Rothlein, R. and Springer, T. A., The requirement for lymphocyte function-associated antigen 1 in homotypic leukocyte adhesion stimulated by phorbol ester. J. Exp. Med. 1986. 163: 1132-1149.
44. Dang, L. H. and Rock, K. L., Stimulation of B lymphocytes through surface Ig receptors induces LFA-1 and ICAM-1-dependent adhesion. J. Immunol. 1991. 146: 3273-3279.
45. Monovich, L., Vega, R. B., Meredith, E., Miranda, K., Rao, C., Capparelli, M., Lemon, D. D. et al., A novel kinase inhibitor establishes a predominant role for protein kinase D as a cardiac class IIa histone deacetylase kinase. FEBS Lett. 2010. 584: 631-637.
46. Meredith, E. L., Beattie, K., Burgis, R., Capparelli, M., Chapo, J., Dipietro, L., Gamber, G. et al., Identification of potent and selective amidobipyridyl inhibitors of protein kinase D. J. Med. Chem. 2010. 53: 5422-5438.
47. Matthews, S. A., Rozengurt, E. and Cantrell, D., Characterization of serine 916 as an in vivo autophosphorylation site for protein kinase D/Protein kinase Cmu. J. Biol. Chem. 1999. 274: 26543-26549.
48. Matthews, S. A., Rozengurt, E. and Cantrell, D., Protein kinase D. A selective target for antigen receptors and a downstream target for protein kinase C in lymphocytes. J. Exp. Med. 2000. 191: 2075-2082.
49. Matthews, S. A., Dayalu, R., Thompson, L. J. and Scharenberg, A. M., Regulation of protein kinase Cnu by the B-cell antigen receptor. J. Biol. Chem. 2003. 278: 9086-9091.
50. Volkov, Y., Long, A., McGrath, S., Ni Eidhin, D. and Kelleher, D., Crucial importance of PKC-beta(I) in LFA-1-mediated locomotion of activated T cells. Nat. Immunol. 2001. 2: 508-514.
51. Leitges, M., Schmedt, C., Guinamard, R., Davoust, J., Schaal, S., Stabel, S. and Tarakhovsky, A., Immunodeficiency in protein kinase cbeta-deficient mice. Science 1996. 273: 788-791.
52. Patke, A., Mecklenbrauker, I., Erdjument-Bromage, H., Tempst, P. and Tarakhovsky, A., BAFF controls B cell metabolic fitness through a PKC beta- and Akt-dependent mechanism. J. Exp. Med. 2006. 203: 2551-2562.
53. Su, T. T., Guo, B., Kawakami, Y., Sommer, K., Chae, K., Humphries, L. A., Kato, R. M. et al., PKC-beta controls I kappa B kinase lipid raft recruitment and activation in response to BCR signaling. Nat. Immunol. 2002. 3: 780-786.
54. Konopatskaya, O., Matthews, S. A., Harper, M. T., Gilio, K., Cosemans, J. M., Williams, C. M., Navarro, M. N. et al., Protein kinase C mediates platelet secretion and thrombus formation through protein kinase D2. Blood 2011. 118: 416-424.
55. Fagerholm, S. C., Prescott, A., Cohen, P. and Gahmberg, C. G., An essential role for calmodulin in regulating human T cell aggregation. FEBS Lett. 2001. 491: 131-136.