Class I myosin Myo1e regulates TLR4-triggered macrophage spreading, chemokine release, and antigen presentation via MHC class II

European Journal of Immunology

Volumn 45, Issue 1, 2015, Pages 225-237

  Wenzel, Jens ^a   Ouderkirk, Jessica L ^b   Krendel, Mira ^b   Lang, Roland ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

Cytoskeleton; Macrophages; MHC class II; Myosin; Toll like receptors

Indexed keywords

ESCHERICHIA COLI LIPOPOLYSACCHARIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MOLECULAR MOTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; MYO1E PROTEIN; MYO1F PROTEIN; MYOSIN I; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; CCL2 PROTEIN, MOUSE; HLA ANTIGEN CLASS 2; LIPOPOLYSACCHARIDE; MYO1E PROTEIN, MOUSE; MYO1F PROTEIN, MOUSE; MYOSIN; TLR4 PROTEIN, MOUSE;

ACTIN FILAMENT; ADAPTIVE IMMUNITY; ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; BONE MARROW DERIVED DENDRITIC CELL; BONE MARROW DERIVED MACROPHAGE; CD4+ T LYMPHOCYTE; CELL SURFACE; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOCYTOSIS; IMMUNOSTIMULATION; INTRACELLULAR TRANSPORT; LYMPHOCYTE PROLIFERATION; MACROPHAGE MIGRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; CYTOSKELETON; DEFICIENCY; DENDRITIC CELL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGEN PRESENTATION; BONE MARROW CELLS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CHEMOKINE CCL2; CYTOSKELETON; DENDRITIC CELLS; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOSIN TYPE I; MYOSINS; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84920985809     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444698     Document Type: Article

References (41)

1. Fletcher, D. A. and Mullins, R. D., Cell mechanics and the cytoskeleton. Nature 2010. 463: 485-492.
2. Pollard, T. D. and Cooper, J. A., Actin, a central player in cell shape and movement. Science 2009. 326: 1208-1212.
3. Pollard, T. D. and Borisy, G. G., Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003. 112: 453-465.
4. Krendel, M. and Mooseker, M. S., Myosins: tails (and heads) of functional diversity. Physiology 2005. 20: 239-251.
5. Santos-Argumedo, L., Maravillas-Montero, J. L. and Lopez-Ortega, O., Class I myosins in B-cell physiology: functions in spreading, immune synapses, motility, and vesicular traffic. Immunol. Rev. 2013. 256: 190-202.
6. Maravillas-Montero, J. L., Gillespie, P. G., Patino-Lopez, G., Shaw, S. and Santos-Argumedo, L., Myosin 1c participates in B cell cytoskeleton rearrangements, is recruited to the immunologic synapse, and contributes to antigen presentation. J. Immunol. 2011. 187: 3053-3063.
7. Maravillas-Montero, J. L., Lopez-Ortega, O., Patino-Lopez, G. and Santos-Argumedo, L., Myosin 1g regulates cytoskeleton plasticity, cell migration, exocytosis, and endocytosis in B lymphocytes. Eur. J. Immunol. 2014. 44, 877-886.
8. Dart, A. E., Tollis, S., Bright, M. D., Frankel, G. and Endres, R. G., The motor protein myosin 1G functions in FcgammaR-mediated phagocytosis. J. Cell Sci. 2012. 125: 6020-6029.
9. Kim, S. V., Mehal, W. Z., Dong, X., Heinrich, V., Pypaert, M., Mellman, I., Dembo, M. et al., Modulation of cell adhesion and motility in the immune system by Myo1f. Science 2006. 314: 136-139.
10. Krendel, M., Osterweil, E. K. and Mooseker, M. S., Myosin 1E interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett. 2007. 581: 644-650.
11. Cheng, J., Grassart, A. and Drubin, D. G., Myosin 1E coordinates actin assembly and cargo trafficking during clathrin-mediated endocytosis. Mol. Biol. Cell 2012. 23: 2891-2904.
12. Mele, C., Iatropoulos, P., Donadelli, R., Calabria, A., Maranta, R., Cassis, P., Buelli, S. et al., MYO1E mutations and childhood familial focal segmental glomerulosclerosis. N. Engl. J. Med. 2011. 365: 295-306.
13. Chase, S. E., Encina, C. V., Stolzenburg, L. R., Tatum, A. H., Holzman, L. B. and Krendel, M., Podocyte-specific knockout of myosin 1e disrupts glomerular filtration. Am. J. Physiol. Renal. Physiol. 2012. 303: F1099-1106.
14. Krendel, M., Kim, S. V., Willinger, T., Wang, T., Kashgarian, M., Flavell, R. A. and Mooseker, M. S., Disruption of Myosin 1e promotes podocyte injury. J. Am. Soc. Nephrol. 2009. 20: 86-94.
15. Wenzel, J., Held, C., Palmisano, R., Teufel, S., David, J. P., Wittenberg, T. and Lang, R., Measurement of TLR-induced macrophage spreading by automated image analysis: differential role of Myd88 and MAPK in early and late responses. Front Physiol. 2011. 2: 71.
16. Blander, J. M. and Medzhitov, R., Regulation of phagosome maturation by signals from toll-like receptors. Science 2004. 304: 1014-1018.
17. Weintz, G., Olsen, J. V., Fruhauf, K., Niedzielska, M., Amit, I., Jantsch, J., Mages, J. et al., The phosphoproteome of toll-like receptor-activated macrophages. Mol. Syst. Biol. 2010. 6: 371.
18. Wiese, M., Castiglione, K., Hensel, M., Schleicher, U., Bogdan, C. and Jantsch, J., Small interfering RNA (siRNA) delivery into murine bone marrow-derived macrophages by electroporation. J. Immunol. Methods 2010. 353: 102-110.
19. Boczkowska, M., Rebowski, G., Petoukhov, M. V., Hayes, D. B., Svergun, D. I. and Dominguez, R., X-ray scattering study of activated Arp2/3 complex with bound actin-WCA. Structure 2008. 16: 695-704.
20. Dettenhofer, M., Zhou, F. and Leder, P., Formin 1-isoform IV deficient cells exhibit defects in cell spreading and focal adhesion formation. PLoS One 2008. 3: e2497.
21. Schonichen, A., Mannherz, H. G., Behrmann, E., Mazur, A. J., Kuhn, S., Silvan, U., Schoenenberger, C. A. et al., FHOD1 is a combined actin filament capping and bundling factor that selectively associates with actin arcs and stress fibers. J. Cell Sci. 2013. 126: 1891-1901.
22. Cai, L., Marshall, T. W., Uetrecht, A. C., Schafer, D. A. and Bear, J. E., Coronin 1B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell 2007. 128: 915-929.
23. Gandhi, M., Achard, V., Blanchoin, L. and Goode, B. L., Coronin switches roles in actin disassembly depending on the nucleotide state of actin. Mol. Cell 2009. 34: 364-374.
24. McConnell, R. E. and Tyska, M. J., Leveraging the membrane-cytoskeleton interface with myosin-1. Trends Cell Biol. 2010. 20: 418-426.
25. Jung, G. and Hammer, J. A., 3rd, The actin binding site in the tail domain of Dictyostelium myosin IC (myoC) resides within the glycine- and proline-rich sequence (tail homology region 2). FEBS Lett. 1994. 342: 197-202.
26. Rump, A., Scholz, T., Thiel, C., Hartmann, F. K., Uta, P., Hinrichs, M. H., Taft, M. H. et al., Myosin-1C associates with microtubules and stabilizes the mitotic spindle during cell division. J. Cell Sci. 2011. 124: 2521-2528.
27. Menegazzi, R., Busetto, S., Dri, P., Cramer, R. and Patriarca, P., Chloride ion efflux regulates adherence, spreading, and respiratory burst of neutrophils stimulated by tumor necrosis factor-alpha (TNF) on biologic surfaces. J. Cell Biol. 1996. 135: 511-522.
28. Schmidt, A., Caron, E. and Hall, A., Lipopolysaccharide-induced activation of beta2-integrin function in macrophages requires Irak kinase activity, p38 mitogen- activated protein kinase, and the Rap1 GTPase. Mol. Cell Biol. 2001. 21: 438-448.
29. Savina, A. and Amigorena, S., Phagocytosis and antigen presentation in dendritic cells. Immunol. Rev. 2007. 219: 143-156.
30. Rougerie, P., Miskolci, V. and Cox, D., Generation of membrane structures during phagocytosis and chemotaxis of macrophages: role and regulation of the actin cytoskeleton. Immunol. Rev. 2013. 256: 222-239.
31. Liu, S. L., May, J. R., Helgeson, L. A. and Nolen, B. J., Insertions within the actin core of actin-related protein 3 (Arp3) modulate branching nucleation by Arp2/3 complex. J. Biol. Chem. 2013. 288: 487-497.
32. Gupta, P., Gauthier, N. C., Cheng-Han, Y., Zuanning, Y., Pontes, B., Ohmstede, M., Martin, R. et al., Myosin 1E localizes to actin polymerization sites in lamellipodia, affecting actin dynamics and adhesion formation. Biol. Open 2013. 2: 1288-1299.
33. Cervero, P., Himmel, M., Kruger, M. and Linder, S., Proteomic analysis of podosome fractions from macrophages reveals similarities to spreading initiation centres. Eur. J. Cell Biol. 2012. 91: 908-922.
34. Schiller, H. B., Friedel, C. C., Boulegue, C. and Fassler, R., Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins. EMBO Rep. 2011. 12: 259-266.
35. Diakonova, M., Bokoch, G. and Swanson, J. A., Dynamics of cytoskeletal proteins during Fcgamma receptor-mediated phagocytosis in macrophages. Mol. Biol. Cell 2002. 13: 402-411.
36. Bi, J., Chase, S. E., Pellenz, C. D., Kurihara, H., Fanning, A. S. and Krendel, M., Myosin 1e is a component of the glomerular slit diaphragm complex that regulates actin reorganization during cell-cell contact formation in podocytes. Am. J. Physiol. Renal. Physiol. 2013. 305: F532-F544.
37. Schietroma, C., Yu, H. Y., Wagner, M. C., Umbach, J. A., Bement, W. M. and Gundersen, C. B., A role for myosin 1e in cortical granule exocytosis in Xenopus oocytes. J. Biol. Chem. 2007. 282: 29504-29513.
38. Vogel, D. Y., Heijnen, P. D., Breur, M., de Vries, H. E., Tool, A. T., Amor, S. and Dijkstra, C. D., Macrophages migrate in an activation-dependent manner to chemokines involved in neuroinflammation. J. Neuroinflammation 2014. 11: 23.
39. Paul, P., van den Hoorn, T., Jongsma, M. L., Bakker, M. J., Hengeveld, R., Janssen, L., Cresswell, P. et al., A Genome-wide multidimensional RNAi screen reveals pathways controlling MHC class II antigen presentation. Cell 2011. 145: 268-283.
40. Delamarre, L., Pack, M., Chang, H., Mellman, I. and Trombetta, E. S., Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005. 307: 1630-1634.
41. Savina, A., Jancic, C., Hugues, S., Guermonprez, P., Vargas, P., Moura, I. C., Lennon-Dumenil, A. M. et al., NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 2006. 126: 205-218.