Vfa1 binds to the N-terminal Microtubule-interacting and trafficking (MIT) domain of Vps4 and stimulates its ATPase activity

Journal of Biological Chemistry

Volumn 289, Issue 15, 2014, Pages 10378-10386

  Vild, Cody J ^a   Xu, Zhaohui ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTAL STRUCTURE;

ATP-ASE ACTIVITY; BINDING PROTEINS; BIOPHYSICAL STUDIES; GENETIC SCREENS; HIGH AFFINITY; MOLECULAR COMPLEXES; MULTIVESICULAR BODIES; OVER-EXPRESSION;

PROTEINS;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BINDING PROTEIN; ESCRT PROTEIN; UNCLASSIFIED DRUG; VFA1 PROTEIN; VPS4 PROTEIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; MICROTUBULE INTERACTING AND TRAFFICKING DOMAIN; MULTIVESICULAR BODY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION;

ATPASES; CRYSTAL STRUCTURE; ENDOSOMES; ESCRT; MEMBRANE TRAFFICKING; MVB; PROTEIN-PROTEIN INTERACTIONS; VFA1; VPS4;

ADENOSINE TRIPHOSPHATASES; CALORIMETRY; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; MICROTUBULES; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; ROSANILINE DYES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84898616566     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.532960     Document Type: Article

References (52)

1. Hanson, P. I., and Cashikar, A. (2012) Multivesicular body morphogenesis. Annu. Rev. Cell Dev. Biol. 28, 337-362
2. McCullough, J., Colf, L. A., and Sundquist, W. I. (2013) Membrane fission reactions of the mammalian ESCRT pathway. Annu. Rev. Biochem. 82, 663-692
3. Hurley, J. H., and Emr, S. D. (2006) The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35, 277-298
4. Henne, W. M., Buchkovich, N. J., and Emr, S. D. (2011) The ESCRT pathway. Dev. Cell 21, 77-91
5. Piper, R. C., and Katzmann, D. J. (2007) Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23, 519-547
6. Winter, V., and Hauser, M. T. (2006) Exploring the ESCRTing machinery in eukaryotes. Trends Plant Sci. 11, 115-123
7. Gruenberg, J., and Stenmark, H. (2004) The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5, 317-323
8. Hurley, J. H., and Hanson, P. I. (2010) Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat. Rev. Mol. Cell Biol. 11, 556-566
9. Hill, C. P., and Babst, M. (2012) Structure and function of the membrane deformation AAA ATPase Vps4. Biochim. Biophys. Acta 1823, 172-181
10. Carlton, J. G., and Martin-Serrano, J. (2007) Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-1912
11. Williams, R. L., and Urbé, S. (2007) The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368
12. Teis, D., Saksena, S., and Emr, S. D. (2008) Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Dev. Cell 15, 578-589
13. Bilodeau, P. S., Urbanowski, J. L., Winistorfer, S. C., and Piper, R. C. (2002) The Vps27p Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat. Cell Biol. 4, 534-539
14. Wollert, T., and Hurley, J. H. (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464, 864-869
15. Elia, N., Fabrikant, G., Kozlov, M. M., and Lippincott-Schwartz, J. (2012) Computational model of cytokinetic abscission driven by ESCRT-III polymerization and remodeling. Biophys. J. 102, 2309-2320
16. Rózycki, B., Boura, E., Hurley, J. H., and Hummer, G. (2012) Membraneelasticity model of Coatless vesicle budding induced by ESCRT complexes. PLoS Comput. Biol. 8, e1002736
17. Elia, N., Sougrat, R., Spurlin, T. A., Hurley, J. H., and Lippincott-Schwartz, J. (2011) Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc. Natl. Acad. Sci. U.S.A. 108, 4846-4851
18. Baumgärtel, V., Ivanchenko, S., Dupont, A., Sergeev, M., Wiseman, P. W., Kräusslich, H. G., Bräuchle, C.,Müller, B., and Lamb, D. C. (2011) Live-cell visualization of dynamics of HIV budding site interactions with an ESCRT component. Nat. Cell Biol. 13, 469-474
19. Lata, S., Roessle, M., Solomons, J., Jamin, M., Gottlinger, H. G., Svergun, D. I., and Weissenhorn, W. (2008) Structural basis for autoinhibition of ESCRT-III CHMP3. J. Mol. Biol. 378, 818-827
20. Nickerson, D. P., West, M., Henry, R., and Odorizzi, G. (2010) Regulators of Vps4 ATPase activity at endosomes differentially influence the size and rate of formation of intralumenal vesicles. Mol. Biol. Cell 21, 1023-1032
21. Wollert, T., Wunder, C., Lippincott-Schwartz, J., and Hurley, J. H. (2009) Membrane scission by the ESCRT-III complex. Nature 458, 172-177
22. Xiao, J., Xia, H., Yoshino-Koh, K., Zhou, J., and Xu, Z. (2007) Structural characterization of the ATPase reaction cycle of endosomal AAA protein Vps4. J. Mol. Biol. 374, 655-670
23. Gonciarz, M. D., Whitby, F. G., Eckert, D. M., Kieffer, C., Heroux, A., Sundquist, W. I., and Hill, C. P. (2008) Biochemical and structural studies of yeast Vps4 oligomerization. J. Mol. Biol. 384, 878-895
24. Landsberg, M. J., Vajjhala, P. R., Rothnagel, R., Munn, A. L., and Hankamer, B. (2009) Three-dimensional structure of AAA ATPase Vps4: advancing structural insights into the mechanisms of endosomal sorting and enveloped virus budding. Structure 17, 427-437
25. Monroe, N., Han, H., Gonciarz, M. D., Eckert, D. M., Karren, M. A., Whitby, F. G., Sundquist, W. I., and Hill, C. P. (2014) The oligomeric state of the active Vps4 AAA ATPase. J. Mol. Biol. 426, 510-525
26. Hurley, J. H., and Yang, D. (2008) MIT domainia. Dev. Cell 14, 6-8
27. Muzioł, T., Pineda-Molina, E., Ravelli, R. B., Zamborlini, A., Usami, Y., Göttlinger, H., and Weissenhorn, W. (2006) Structural basis for budding by the ESCRT-III factor CHMP3. Dev. Cell 10, 821-830
28. Shim, S., Kimpler, L. A., and Hanson, P. I. (2007) Structure/function analysis of four core ESCRT-III proteins reveals common regulatory role for extreme C-terminal domain. Traffic 8, 1068-1079
29. Rózycki, B., Kim, Y. C., and Hummer, G. (2011) SAXS ensemble refinement of ESCRT-III CHMP3 conformational transitions. Structure 19, 109-116
30. Stuchell-Brereton, M. D., Skalicky, J. J., Kieffer, C., Karren, M. A., Ghaffarian, S., and Sundquist, W. I. (2007) ESCRT-III recognition by VPS4 ATPases. Nature 449, 740-744
31. Obita, T., Saksena, S., Ghazi-Tabatabai, S., Gill, D. J., Perisic, O., Emr, S. D., and Williams, R. L. (2007) Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4. Nature 449, 735-739
32. Kieffer, C., Skalicky, J. J., Morita, E., De Domenico, I., Ward, D. M., Kaplan, J., and Sundquist, W. I. (2008) Two distinct modes of ESCRT-III recognition are required for VPS4 functions in lysosomal protein targeting and HIV-1 budding. Dev. Cell 15, 62-73
33. Yang, D., Rismanchi, N., Renvoisé, B., Lippincott-Schwartz, J., Blackstone, C., and Hurley, J. H. (2008) Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nat. Struct. Mol. Biol. 15, 1278-1286
34. Solomons, J., Sabin, C., Poudevigne, E., Usami, Y., Hulsik, D. L., Macheboeuf, P., Hartlieb, B., Göttlinger, H., and Weissenhorn, W. (2011) Structural basis for ESCRT-III CHMP3 recruitment of AMSH. Structure 19, 1149-1159
35. Yang, Z., Vild, C., Ju, J., Zhang, X., Liu, J., Shen, J., Zhao, B., Lan, W., Gong, F., Liu, M., Cao, C., and Xu, Z. (2012) Structural basis of molecular recognition between ESCRT-III-like protein Vps60 and AAA-ATPase regulator Vta1 in the multivesicular body pathway. J. Biol. Chem. 287, 43899-43908
36. Skalicky, J. J., Arii, J., Wenzel, D. M., Stubblefield, W. M., Katsuyama, A., Uter, N. T., Bajorek, M., Myszka, D. G., and Sundquist, W. I. (2012) Interactions of the human LIP5 regulatory protein with endosomal sorting complexes required for transport. J. Biol. Chem. 287, 43910-43926
37. Merrill, S. A., and Hanson, P. I. (2010) Activation of human VPS4A by ESCRT-III proteins reveals ability of substrates to relieve enzyme autoinhibition. J. Biol. Chem. 285, 35428-35438
38. Azmi, I., Davies, B., Dimaano, C., Payne, J., Eckert, D., Babst, M., and Katzmann, D. J. (2006) Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta 1. J. Cell Biol. 172, 705-717
39. Xiao, J., Xia, H., Zhou, J., Azmi, I. F., Davies, B. A., Katzmann, D. J., and Xu, Z. (2008) Structural basis of Vta1 function in the multivesicular body sorting pathway. Dev. Cell 14, 37-49
40. Arlt, H., Perz, A., and Ungermann, C. (2011) An overexpression screen in Saccharomyces cerevisiae identifies novel genes that affect endocytic protein trafficking. Traffic 12, 1592-1603
41. Chang, L., Bertelsen, E. B., Wisén, S., Larsen, E. M., Zuiderweg, E. R., and Gestwicki, J. E. (2008) High-throughput screen for small molecules that modulate the ATPase activity of the molecular chaperone DnaK. Anal. Biochem. 372, 167-176
42. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
43. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
44. Babst, M., Sato, T. K., Banta, L. M., and Emr, S. D. (1997) Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J. 16, 1820-1831
45. Bajorek, M., Morita, E., Skalicky, J. J., Morham, S. G., Babst, M., and Sundquist, W. I. (2009) Biochemical analyses of human IST1 and its function in cytokinesis. Mol. Biol. Cell 20, 1360-1373
46. Scott, A., Gaspar, J., Stuchell-Brereton, M. D., Alam, S. L., Skalicky, J. J., and Sundquist, W. I. (2005) Structure and ESCRT-III protein interactions of the MIT domain of human VPS4A. Proc. Natl. Acad. Sci. U.S.A. 102, 13813-13818
47. Azmi, I. F., Davies, B. A., Xiao, J., Babst, M., Xu, Z., and Katzmann, D. J. (2008) ESCRT-III family members stimulate Vps4 ATPase activity directly or via Vta1. Dev. Cell 14, 50-61
48. Shestakova, A., Hanono, A., Drosner, S., Curtiss, M., Davies, B. A., Katzmann, D. J., and Babst, M. (2010) Assembly of the AAA ATPase Vps4 on ESCRT-III. Mol. Biol. Cell 21, 1059-1071
49. Renvoisé, B., Parker, R. L., Yang, D., Bakowska, J. C., Hurley, J. H., and Blackstone, C. (2010) SPG20 protein spartin is recruited to midbodies by ESCRT-III protein Ist1 and participates in cytokinesis. Mol. Biol. Cell 21, 3293-3303
50. Giaever, G., Chu, A. M., Ni, L., Connelly, C., Riles, L., Véronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., André, B., Arkin, A. P., Astromoff, A., El-Bakkoury, M., Bangham, R., Benito, R., Brachat, S., Campanaro, S., Curtiss, M., Davis, K., Deutschbauer, A., Entian, K. D., Flaherty, P., Foury, F., Garfinkel, D. J., Gerstein, M., Gotte, D., Güldener, U., Hegemann, J. H., Hempel, S., Herman, Z., Jaramillo, D. F., Kelly, D. E., Kelly, S. L., Kotter, P., LaBonte, D., Lamb, D. C., Lan, N., Liang, H., Liao, H., Liu, L., Luo, C., Lussier, M., Mao, R., Menard, P., Ooi, S. L., Revuelta, J. L., Roberts, C. J., Rose, M., Ross-Macdonald, P., Scherens, B., Schimmack, G., Shafer, B., Shoemaker, D. D., Sookhai-Mahadeo, S., Storms, R. K., Strathern, J. N., Valle, G., Voet, M., Volckaert, G., Wang, C. Y., Ward, T. R., Wilhelmy, J., Winzeler, E. A., Yang, Y., Yen, G., Youngman, E., Yu, K., Bussey, H., Boeke, J. D., Snyder, M., Philippsen, P., Davis, R. W., and Johnston, M. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391
51. Rue, S. M., Mattei, S., Saksena, S., and Emr, S. D. (2008) Novel Ist1-Did2 complex functions at a late step in multivesicular body sorting. Mol. Biol. Cell 19, 475-484
52. Yu, H., Braun, P., Yildirim, M. A., Lemmens, I., Venkatesan, K., Sahalie, J., Hirozane-Kishikawa, T., Gebreab, F., Li, N., Simonis, N., Hao, T., Rual, J. F., Dricot, A., Vazquez, A., Murray, R. R., Simon, C., Tardivo, L., Tam, S., Svrzikapa, N., Fan, C., de Smet, A. S., Motyl, A., Hudson, M. E., Park, J., Xin, X., Cusick, M. E., Moore, T., Boone, C., Snyder, M., Roth, F. P., Barabási, A. L., Tavernier, J., Hill, D. E., and Vidal, M. (2008) High-quality binary protein interaction map of the yeast interactome network. Science 322, 104-110