Myosin 1g regulates cytoskeleton plasticity, cell migration, exocytosis, and endocytosis in B lymphocytes

European Journal of Immunology

Volumn 44, Issue 3, 2014, Pages 877-886

  Maravillas Montero, José L ^a   López Ortega, Orestes ^a   Patiño López, Genaro ^b,c   Santos Argumedo, Leopoldo ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b NATIONAL CANCER INSTITUTE   (United States)

^c HOSPITAL INFANTIL DE MÉXICO FEDERICO GÓMEZ   (Mexico)

Author keywords

B lymphocyte; Chemotaxis; Cytoskeleton; Exo endocytosis; Myosin

Indexed keywords

CHEMOKINE; MYOSIN 1G; MYOSIN I; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL ADHESION; CELL SPREADING; CHEMOTAXIS; CONTROLLED STUDY; CYTOSKELETON; ENDOCYTOSIS; EXOCYTOSIS; FEMALE; IN VITRO STUDY; LIPID RAFT; LYMPHOCYTE HOMING; LYMPHOCYTE MEMBRANE; LYMPHOCYTE MIGRATION; MEMBRANE STRUCTURE; MICROVILLUS; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM;

B LYMPHOCYTE; CHEMOTAXIS; CYTOSKELETON; EXO-ENDOCYTOSIS; MYOSIN;

ANIMALS; B-LYMPHOCYTES; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETON; ENDOCYTOSIS; EXOCYTOSIS; FEMALE; MICE; MICE, KNOCKOUT; MYOSINS; PROTEIN TRANSPORT;

EID: 84896055029     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343873     Document Type: Article

References (52)

1. Kim, S. V. and Flavell, R. A., Myosin I: from yeast to human. Cell Mol. Life Sci. 2008. 65: 2128-2137.
2. Berg, J. S., Powell, B. C. and Cheney, R. E., A millennial myosin census. Mol. Biol. Cell 2001. 12: 780-794.
3. Coluccio, L. M., Myosin I. Am. J. Physiol. 1997. 273: C347-C359.
4. Albanesi, J. P., Fujisaki, H., Hammer, J. A., 3rd, Korn, E. D., Jones, R. and Sheetz, M. P., Monomeric Acanthamoeba myosins I support movement in vitro. J. Biol. Chem. 1985. 260: 8649-8652.
5. Stafford, W. F., Walker, M. L., Trinick, J. A. and Coluccio, L. M., Mammalian class I myosin, Myo1b, is monomeric and cross-links actin filaments as determined by hydrodynamic studies and electron microscopy. Biophys. J. 2005. 88: 384-391.
6. Coluccio, L. M., Mooseker, M. S. and Foth, B. J., The Structural And Functional Diversity Of The Myosin Family Of Actin-Based Molecular Motors Myosins. Springer, the Netherlands, 2008, pp. 1-34.
7. Doberstein, S. K. and Pollard, T. D., Localization and specificity of the phospholipid and actin binding sites on the tail of Acanthamoeba myosin IC. J. Cell Biol. 1992. 117: 1241-1249.
8. Lee, W. L., Ostap, E. M., Zot, H. G. and Pollard, T. D., Organization and ligand binding properties of the tail of Acanthamoeba myosin-IA. Identification of an actin-binding site in the basic (tail homology-1) domain. J. Biol. Chem. 1999. 274: 35159-35171.
9. Heng, T. S. and Painter, M. W., The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 2008. 9: 1091-1094.
10. Wu, C., Orozco, C., Boyer, J., Leglise, M., Goodale, J., Batalov, S., Hodge, C. et al., BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 2009. 10: R130.
11. Maravillas-Montero, J. L. and Santos-Argumedo, L., The myosin family: unconventional roles of actin-dependent molecular motors in immune cells. J. Leukoc. Biol. 2012. 91: 35-46.
12. Olety, B., Walte, M., Honnert, U., Schillers, H. and Bahler, M., Myosin 1G (Myo1G) is a haematopoietic specific myosin that localises to the plasma membrane and regulates cell elasticity. FEBS Lett. 2010. 584: 493-499.
13. Patino-Lopez, G., Aravind, L., Dong, X., Kruhlak, M. J., Ostap, E. M. and Shaw, S., Myosin 1G is an abundant class I myosin in lymphocytes whose localization at the plasma membrane depends on its ancient divergent pleckstrin homology (PH) domain (Myo1PH). J. Biol. Chem. 2010. 285: 8675-8686.
14. 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.
15. Lafourcade, C., Sobo, K., Kieffer-Jaquinod, S., Garin, J. and van der Goot, F. G., Regulation of the V-ATPase along the endocytic pathway occurs through reversible subunit association and membrane localization. PLoS One 2008. 3: e2758.
16. Linkermann, A., Gelhaus, C., Lettau, M., Qian, J., Kabelitz, D. and Janssen, O., Identification of interaction partners for individual SH3 domains of Fas ligand associated members of the PCH protein family in T lymphocytes. Biochim. Biophys. Acta 2009. 1794: 168-176.
17. Perez-Hernandez, D., Gutierrez-Vazquez, C., Jorge, I., Lopez-Martin, S., Ursa, A., Sanchez-Madrid, F., Vazquez, J. et al., The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes. J. Biol. Chem. 2013. 288: 11649-11661.
18. 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.
19. Sumoza-Toledo, A., Gillespie, P. G., Romero-Ramirez, H., Ferreira-Ishikawa, H. C., Larson, R. E. and Santos-Argumedo, L., Differential localization of unconventional myosin I and nonmuscle myosin II during B cell spreading. Exp. Cell Res. 2006. 312: 3312-3322.
20. Soldati, T., Unconventional myosins, actin dynamics and endocytosis: a menage a trois? Traffic 2003. 4: 358-366.
21. Nebl, T., Pestonjamasp, K. N., Leszyk, J. D., Crowley, J. L., Oh, S. W. and Luna, E. J., Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J. Biol. Chem. 2002. 277: 43399-43409.
22. Saeki, K., Miura, Y., Aki, D., Kurosaki, T. and Yoshimura, A., The B cell-specific major raft protein, Raftlin, is necessary for the integrity of lipid raft and BCR signal transduction. EMBO J. 2003. 22: 3015-3026.
23. Houk, A. R., Jilkine, A., Mejean, C. O., Boltyanskiy, R., Dufresne, E. R., Angenent, S. B., Altschuler, S. J. et al., Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration. Cell 2012. 148: 175-188.
24. Liu, Y., Belkina, N. V., Park, C., Nambiar, R., Loughhead, S. M., Patino-Lopez, G., Ben-Aissa, K. et al., Constitutively active ezrin increases membrane tension, slows migration, and impedes endothelial transmigration of lymphocytes in vivo in mice. Blood 2012. 119: 445-453.
25. Bertram, A., Zhang, H., von Vietinghoff, S., de Pablo, C., Haller, H., Shushakova, N. and Ley, K., Protein kinase C-theta is required for murine neutrophil recruitment and adhesion strengthening under flow. J. Immunol. 2012. 188: 4043-4051.
26. Ng, T., Parsons, M., Hughes, W. E., Monypenny, J., Zicha, D., Gautreau, A., Arpin, M. et al., Ezrin is a downstream effector of trafficking PKC-integrin complexes involved in the control of cell motility. EMBO J. 2001. 20: 2723-2741.
27. Popi, A. F., Zamboni, D. S., Mortara, R. A. and Mariano, M., Microbicidal property of B1 cell derived mononuclear phagocyte. Immunobiology 2009. 214: 664-673.
28. Gao, J., Ma, X., Gu, W., Fu, M., An, J., Xing, Y., Gao, T. et al., Novel functions of murine B1 cells: active phagocytic and microbicidal abilities. Eur. J. Immunol. 2012. 42: 982-992.
29. Ray, A. and Dittel, B. N., Isolation of mouse peritoneal cavity cells. J. Vis. Exp. 2010. 35: e1488.
30. Keren, K., Pincus, Z., Allen, G. M., Barnhart, E. L., Marriott, G., Mogilner, A. and Theriot, J. A., Mechanism of shape determination in motile cells. Nature 2008. 453: 475-480.
31. Buckley, A. R., Prolactin, a lymphocyte growth and survival factor. Lupus 2001. 10: 684-690.
32. Díaz, L., Díaz-Muñoz, M., González, L., Lira-Albarrán, S., Larrea, F. and Méndez, I., Prolactin in the Immune System. In Nagy, G.M. and Toth, B.E. (Eds.), Prolactin. InTech, Croatia, 2013.
33. DiMattia, G. E., Gellersen, B., Bohnet, H. G. and Friesen, H. G., A human B-lymphoblastoid cell line produces prolactin. Endocrinology 1988. 122: 2508-2517.
34. Perez-Lopez, A., Rosales-Reyes, R., Alpuche-Aranda, C. M. and Ortiz-Navarrete, V., Salmonella downregulates Nod-like receptor family CARD domain containing protein 4 expression to promote its survival in B cells by preventing inflammasome activation and cell death. J. Immunol. 2013. 190: 1201-1209.
35. Hao, J. J., Wang, G., Pisitkun, T., Patino-Lopez, G., Nagashima, K., Knepper, M. A., Shen, R. F. et al., Enrichment of distinct microfilament-associated and GTP-binding-proteins in membrane/microvilli fractions from lymphoid cells. J. Proteome Res. 2008. 7: 2911-2927.
36. Greicius, G., Westerberg, L., Davey, E. J., Buentke, E., Scheynius, A., Thyberg, J. and Severinson, E., Microvilli structures on B lymphocytes: inducible functional domains? Int. Immunol. 2004. 16: 353-364.
37. Knorr, R., Karacsonyi, C. and Lindner, R., Endocytosis of MHC molecules by distinct membrane rafts. J. Cell Sci. 2009. 122: 1584-1594.
38. Petrie, R. J. and Deans, J. P., Colocalization of the B cell receptor and CD20 followed by activation-dependent dissociation in distinct lipid rafts. J. Immunol. 2002. 169: 2886-2891.
39. Greenberg, M. J. and Ostap, E. M., Regulation and control of myosin-I by the motor and light chain-binding domains. Trends Cell Biol. 2013. 23: 81-89.
40. 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.
41. Peterson, M. D., Novak, K. D., Reedy, M. C., Ruman, J. I. and Titus, M. A., Molecular genetic analysis of myoC, a Dictyostelium myosin I. J. Cell Sci. 1995. 108(Pt 3): 1093-1103.
42. Nambiar, R., McConnell, R. E. and Tyska, M. J., Control of cell membrane tension by myosin-I. Proc. Natl. Acad. Sci. USA 2009. 106: 11972-11977.
43. Raucher, D. and Sheetz, M. P., Cell spreading and lamellipodial extension rate is regulated by membrane tension. J. Cell Biol. 2000. 148: 127-136.
44. Pietuch, A. and Janshoff, A., Mechanics of spreading cells probed by atomic force microscopy. Open Biol. 2013. 3: 130084.
45. Delanoe-Ayari, H., Al Kurdi, R., Vallade, M., Gulino-Debrac, D. and Riveline, D., Membrane and acto-myosin tension promote clustering of adhesion proteins. Proc. Natl. Acad. Sci. USA 2004. 101: 2229-2234.
46. Simon, S. I., Hu, Y., Vestweber, D. and Smith, C. W., Neutrophil tethering on E-selectin activates beta 2 integrin binding to ICAM-1 through a mitogen-activated protein kinase signal transduction pathway. J. Immunol. 2000. 164: 4348-4358.
47. Xu, H., Manivannan, A., Crane, I., Dawson, R. and Liversidge, J., Critical but divergent roles for CD62L and CD44 in directing blood monocyte trafficking in vivo during inflammation. Blood 2008. 112: 1166-1174.
48. Raposo, G., Cordonnier, M. N., Tenza, D., Menichi, B., Durrbach, A., Louvard, D. and Coudrier, E., Association of myosin I alpha with endosomes and lysosomes in mammalian cells. Mol. Biol. Cell 1999. 10: 1477-1494.
49. Marion, S., Laurent, C. and Guillen, N., Signalization and cytoskeleton activity through myosin IB during the early steps of phagocytosis in Entamoeba histolytica: a proteomic approach. Cell Microbiol. 2005. 7: 1504-1518.
50. Keren, K., Cell motility: the integrating role of the plasma membrane. Eur. Biophys. J. 2011. 40: 1013-1027.
51. Marion, S., Wilhelm, C., Voigt, H., Bacri, J. C. and Guillen, N., Overexpression of myosin IB in living Entamoeba histolytica enhances cytoplasm viscosity and reduces phagocytosis. J. Cell Sci. 2004. 117: 3271-3279.
52. Nibbering, P. H., Broug-Holub, E., Bezemer, A. C., Jansen, R., van de Winkel, J. G. and Geertsma, M. F., Phagocytosis and intracellular killing of serum-opsonized Staphylococcus aureus by mouse fibroblasts expressing human Fcgamma receptor type IIa (CD32). Front Biosci. 1996. 1: a25-a33.