The architectural relationship of components controlling mast cell endocytosis

Journal of Cell Science

Volumn 126, Issue 21, 2013, Pages 4913-4925

  Cleyrat, Cédric ^a   Darehshouri, Anza ^a   Anderson, Karen L ^b   Page, Christopher ^b   Lidke, Diane S ^a   Volkmann, Niels ^b   Hanein, Dorit ^b   Wilson, Bridget S ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

Arf6; CIE; CME; Endocytosis; Eps15; Fc RI; Mast cell

Indexed keywords

ADAPTOR PROTEIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CLATHRIN; DYNAMIN; EPIDERMAL GROWTH FACTOR RECEPTOR PATHWAY SUBSTRATE 15; IMMUNOGLOBULIN E RECEPTOR; LIPID; TRANSFERRIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOCYTOSIS; IMMUNOELECTRON MICROSCOPY; MAST CELL; MAST CELL LEUKEMIA; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR AFFINITY;

ARF6; CIE; CME; ENDOCYTOSIS; EPS15; FCΕRI; MAST CELL;

ADP-RIBOSYLATION FACTORS; ANIMALS; CALCIUM-BINDING PROTEINS; CELL LINE, TUMOR; CELL MEMBRANE; CLATHRIN; DYNAMINS; ENDOCYTOSIS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAST CELLS; PROTEIN TRANSPORT; RATS;

EID: 84887569602     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.128876     Document Type: Article

References (62)

1. Andrews, N. L., Pfeiffer, J. R., Martinez, A. M., Haaland, D. M., Davis, R. W., Kawakami, T., Oliver, J. M., Wilson, B. S. and Lidke, D. S. (2009). Small, mobile FcepsilonRI receptor aggregates are signaling competent. Immunity 31, 469-479.
2. Benmerah, A., Lamaze, C., Bégue, B., Schmid, S. L., Dautry-Varsat, A. and Cerf-Bensussan, N. (1998). AP-2/Eps15 interaction is required for receptor-mediated endocytosis. J. Cell Biol. 140, 1055-1062.
3. Chadda, R., Howes, M. T., Plowman, S. J., Hancock, J. F., Parton, R. G. and Mayor, S. (2007). Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffic 8, 702-717.
4. Cupers, P., Jadhav, A. P. and Kirchhausen, T. (1998). Assembly of clathrin coats disrupts the association between Eps15 and AP-2 adaptors. J. Biol. Chem. 273, 1847-1850.
5. Damke, H., Baba, T., Warnock, D. E. and Schmid, S. L. (1994). Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934.
6. Daumke, O., Lundmark, R., Vallis, Y., Martens, S., Butler, P. J. and McMahon, H. T. (2007). Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449, 923-927.
7. Doherty, G. J. and McMahon, H. T. (2009). Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857-902.
8. Donaldson, J. G. (2003). Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J. Biol. Chem. 278, 41573-41576.
9. Donaldson, J. G. and Radhakrishna, H. (2001). Expression and properties of ADPribosylation factor (ARF6) in endocytic pathways. Methods Enzymol. 329, 247-256.
10. Dutta, D., Williamson, C. D., Cole, N. B. and Donaldson, J. G. (2012). Pitstop 2 is a potent inhibitor of clathrin-independent endocytosis. PLoS ONE 7, e45799.
11. Fattakhova, G., Masilamani, M., Borrego, F., Gilfillan, A. M., Metcalfe, D. D. and Coligan, J. E. (2006). The high-affinity immunoglobulin-E receptor (FcepsilonRI) is endocytosed by an AP-2/clathrin-independent, dynamin-dependent mechanism. Traffic 7, 673-685.
12. Glebov, O. O., Bright, N. A. and Nichols, B. J. (2006). Flotillin-1 defines a clathrinindependent endocytic pathway in mammalian cells. Nat. Cell Biol. 8, 46-54.
13. Goh, L. K., Huang, F., Kim, W., Gygi, S. and Sorkin, A. (2010). Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor. J. Cell Biol. 189, 871-883.
14. Hurley, J. H. and Wendland, B. (2002). Endocytosis: driving membranes around the bend. Cell 111, 143-146.
15. Kirkham, M., Fujita, A., Chadda, R., Nixon, S. J., Kurzchalia, T. V., Sharma, D. K., Pagano, R. E., Hancock, J. F., Mayor, S. and Parton, R. G. (2005). Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J. Cell Biol. 168, 465-476.
16. Kremer, J. R., Mastronarde, D. N. and McIntosh, J. R. (1996). Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76.
17. Lamaze, C., Dujeancourt, A., Baba, T., Lo, C. G., Benmerah, A. and Dautry-Varsat, A. (2001). Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell 7, 661-671.
18. Lemmon, S. K. and Traub, L. M. (2012). Getting in touch with the clathrin terminal domain. Traffic 13, 511-519.
19. Liu, F. T., Bohn, J. W., Ferry, E. L., Yamamoto, H., Molinaro, C. A., Sherman, L. A., Klinman, N. R. and Katz, D. H. (1980). Monoclonal dinitrophenyl-specific murine IgE antibody: preparation, isolation, and characterization. J. Immunol. 124, 2728-2737.
20. Liu, A. P., Aguet, F., Danuser, G. and Schmid, S. L. (2010). Local clustering of transferrin receptors promotes clathrin-coated pit initiation. J. Cell Biol. 191, 1381-1393.
21. Mao, S. Y., Varin-Blank, N., Edidin, M. and Metzger, H. (1991). Immobilization and internalization of mutated IgE receptors in transfected cells. J. Immunol. 146, 958-966.
22. Mao, S. Y., Pfeiffer, J. R., Oliver, J. M. and Metzger, H. (1993). Effects of subunit mutation on the localization to coated pits and internalization of cross-linked IgEreceptor complexes. J. Immunol. 151, 2760-2774.
23. Martínez-Martín, N., Fernández-Arenas, E., Cemerski, S., Delgado, P., Turner, M., Heuser, J., Irvine, D. J., Huang, B., Bustelo, X. R., Shaw, A. et al. (2011). T cell receptor internalization from the immunological synapse is mediated by TC21 and RhoG GTPase-dependent phagocytosis. Immunity 35, 208-222.
24. Mastronarde, D. N. (2005). Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36-51.
25. McMahon, H. T. and Boucrot, E. (2011). Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533.
26. Mellman, I. and Plutner, H. (1984). Internalization and degradation of macrophage Fc receptors bound to polyvalent immune complexes. J. Cell Biol. 98, 1170-1177.
27. Molfetta, R., Gasparrini, F., Peruzzi, G., Vian, L., Piccoli, M., Frati, L., Santoni, A. and Paolini, R. (2009). Lipid raft-dependent FcepsilonRI ubiquitination regulates receptor endocytosis through the action of ubiquitin binding adaptors. PLoS ONE 4, e5604.
28. Naslavsky, N., Weigert, R. and Donaldson, J. G. (2004). Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol. Biol. Cell 15, 3542-3552.
29. Nossal, R. and Zimmerberg, J. (2002). Endocytosis: curvature to the ENTH degree. Curr. Biol. 12, R770-R772.
30. Oliver, C., Fujimura, A., Silveirae Souza, A. M., Orlandini de Castro, R., Siraganian, R. P. and Jamur, M. C. (2007). Mast cell-specific gangliosides and FcepsilonRI follow the same endocytic pathway from lipid rafts in RBL-2H3 cells. J. Histochem. Cytochem. 55, 315-325.
31. Paolini, R. and Kinet, J. P. (1993). Cell surface control of the multiubiquitination and deubiquitination of high-affinity immunoglobulin E receptors. EMBO J. 12, 779-786.
32. Parachoniak, C. A. and Park, M. (2009). Distinct recruitment of Eps15 via Its coiledcoil domain is required for efficient down-regulation of the met receptor tyrosine kinase. J. Biol. Chem. 284, 8382-8394.
33. Pasqualato, S., Ménétrey, J., Franco, M. and Cherfils, J. (2001). The structural GDP/GTP cycle of human Arf6. EMBO Rep. 2, 234-238.
34. Peters, P. J., Hsu, V. W., Ooi, C. E., Finazzi, D., Teal, S. B., Oorschot, V., Donaldson, J. G. and Klausner, R. D. (1995). Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments. J. Cell Biol. 128, 1003-1017.
35. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C. and Ferrin, T. E. (2004). UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.
36. Polo, S. (2012). Signaling-mediated control of ubiquitin ligases in endocytosis. BMC Biol. 10, 25.
37. Radhakrishna, H. and Donaldson, J. G. (1997). ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139, 49-61.
38. Ramanan, V., Agrawal, N. J., Liu, J., Engles, S., Toy, R. and Radhakrishnan, R. (2011). Systems biology and physical biology of clathrin-mediated endocytosis. Integr. Biol. (Camb) 3, 803-815.
39. Sanan, D. A. and Anderson, R. G. (1991). Simultaneous visualization of LDL receptor distribution and clathrin lattices on membranes torn from the upper surface of cultured cells. J. Histochem. Cytochem. 39, 1017-1024.
40. Sauvonnet, N., Dujeancourt, A. and Dautry-Varsat, A. (2005). Cortactin and dynamin are required for the clathrin-independent endocytosis of gammac cytokine receptor. J. Cell Biol. 168, 155-163.
41. Schmid, S. L. and Frolov, V. A. (2011). Dynamin: functional design of a membrane fission catalyst. Annu. Rev. Cell Dev. Biol. 27, 79-105.
42. Sigismund, S., Woelk, T., Puri, C., Maspero, E., Tacchetti, C., Transidico, P., Di Fiore, P. P. and Polo, S. (2005). Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl. Acad. Sci. USA 102, 2760-2765.
43. Sorkin, A. and von Zastrow, M. (2009). Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-622.
44. Stoddart, A., Jackson, A. P. and Brodsky, F. M. (2005). Plasticity of B cell receptor internalization upon conditional depletion of clathrin. Mol. Biol. Cell 16, 2339-2348.
45. Sundborger, A., Soderblom, C., Vorontsova, O., Evergren, E., Hinshaw, J. E. and Shupliakov, O. (2011). An endophilin-dynamin complex promotes budding of clathrin-coated vesicles during synaptic vesicle recycling. J. Cell Sci. 124, 133-143.
46. Torgersen, M. L., Skretting, G., van Deurs, B. and Sandvig, K. (2001). Internalization of cholera toxin by different endocytic mechanisms. J. Cell Sci. 114, 3737-3747.
47. Traub, L. M. (2009). Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol. 10, 583-596.
48. Van Bergenen Henegouwen, P. M. (2009). Eps15: a multifunctional adaptor protein regulating intracellular trafficking. Cell Commun. Signal. 7, 24.
49. van der Heide, P., Xu, X. P., Marsh, B. J., Hanein, D. and Volkmann, N. (2007). Efficient automatic noise reduction of electron tomographic reconstructions based on iterative median filtering. J. Struct. Biol. 158, 196-204.
50. Volkmann, N. (2002). A novel three-dimensional variant of the watershed transform for segmentation of electron density maps. J. Struct. Biol. 138, 123-129.
51. Volkmann, N. (2004). An approach to automated particle picking from electron micrographs based on reduced representation templates. J. Struct. Biol. 145, 152-156.
52. Volkmann, N. and Hanein, D. (1999). Quantitative fitting of atomic models into observed densities derived by electron microscopy. J. Struct. Biol. 125, 176-184.
53. Von Kleist, L., Stahlschmidt, W., Bulut, H., Gromova, K., Puchkov, D., Robertson, M. J., MacGregor, K. A., Tomilin, N., Pechstein, A., Chau, N. et al. (2011). Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146, 471-484.
54. Whitaker, R. T. and Xue, X. (2001). Variable-conductance, level-set curvature for image denoising. Proc. Int. Conf. Image Proc. 3, 142-145.
55. Wilson, B. S., Pfeiffer, J. R. and Oliver, J. M. (2000). Observing FcepsilonRI signaling from the inside of the mast cell membrane. J. Cell Biol. 149, 1131-1142.
56. Wilson, B. S., Pfeiffer, J. R., Surviladze, Z., Gaudet, E. A. and Oliver, J. M. (2001). High resolution mapping of mast cell membranes reveals primary and secondary domains of Fc(epsilon)RI and LAT. J. Cell Biol. 154, 645-658.
57. Wilson, B. S., Pfeiffer, J. R. and Oliver, J. M. (2002). FcepsilonRI signaling observed from the inside of the mast cell membrane. Mol. Immunol. 38, 1259-1268.
58. Wilson, B. S., Steinberg, S. L., Liederman, K., Pfeiffer, J. R., Surviladze, Z., Zhang, J., Samelson, L. E., Yang, L. H., Kotula, P. G. and Oliver, J. M. (2004). Markers for detergent-resistant lipid rafts occupy distinct and dynamic domains in native membranes. Mol. Biol. Cell 15, 2580-2592.
59. Wilson, B. S., Pfeiffer, J. R., Raymond-Stintz, M. A., Lidke, D., Andrews, N., Zhang, J., Yin, W., Steinberg, S. and Oliver, J. M. (2007). Exploring membrane domains using native membrane sheets and transmission electron microscopy. Methods Mol. Biol. 398, 245-261.
60. Xue, M., Hsieh, G., Raymond-Stintz, M. A., Pfeiffer, J., Roberts, D., Steinberg, S. L., Oliver, J. M., Prossnitz, E. R., Lidke, D. S. and Wilson, B. S. (2007). Activated N-formyl peptide receptor and high-affinity IgE receptor occupy common domains for signaling and internalization. Mol. Biol. Cell 18, 1410-1420.
61. Zhang, J., Leiderman, K., Pfeiffer, J. R., Wilson, B. S., Oliver, J. M. and Steinberg, S. L. (2006). Characterizing the topography of membrane receptors and signaling molecules from spatial patterns obtained using nanometer-scale electron-dense probes and electron microscopy. Micron 37, 14-34.
62. Zwang, Y. and Yarden, Y. (2009). Systems biology of growth factor-induced receptor endocytosis. Traffic 10, 349-363.