Structural basis of molecular recognition between ESCRT-III-like protein Vps60 and AAA-ATPase regulator Vta1 in the multivesicular body pathway

Journal of Biological Chemistry

Volumn 287, Issue 52, 2012, Pages 43899-43908

  Yang, Zhongzheng ^a   Vild, Cody ^b   Ju, Jiaying ^a   Zhang, Xu ^c   Liu, Jianping ^a,d   Shen, Jie ^a   Zhao, Bin ^a   Lan, Wenxian ^a   Gong, Fuchun ^d   Liu, Maili ^c   Cao, Chunyang ^a   Xu, Zhaohui ^b  

^a SHANGHAI INSTITUTE OF ORGANIC CHEMISTRY   (China)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c Wuhan National Laboratory for Optoelectronics   (China)

^d CHANGSHA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONAL CHANGE; DOWN-REGULATION; MULTIVESICULAR BODIES; N-TERMINAL DOMAINS; NMR TECHNIQUES; STRUCTURAL BASIS;

BIOCHEMISTRY; BIOLOGY;

MOLECULAR RECOGNITION;

ADENOSINE TRIPHOSPHATASE; CELL PROTEIN; ENDOSOMAL SORTING COMPLEX REQUIRED FOR TRANSPORT III PROTEIN; ESCRT PROTEIN; UNCLASSIFIED DRUG; VPS60 PROTEIN; VTA1 PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; MULTIVESICULAR BODY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS;

ADENOSINE TRIPHOSPHATASES; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; MULTIPROTEIN COMPLEXES; MULTIVESICULAR BODIES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84871605394     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.390724     Document Type: Article

References (45)

1. Gruenberg, J., and Stenmark, H. (2004) The biogenesis of multivesicular endosomes. Nat. Rev. Mol. Cell Biol. 5, 317-323 (Pubitemid 38480612)
2. Morita, E., and Sundquist, W. I. (2004) Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20, 395-425 (Pubitemid 39488644)
3. Carlton, J. G., and Martin-Serrano, J. (2007) Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 316, 1908-1912 (Pubitemid 47025792)
4. Babst, M. (2005) A protein's final ESCRT. Traffic 6, 2-9
5. 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 (Pubitemid 43877379)
6. Piper, R. C., and Katzmann, D. J. (2007) Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23, 519-547
7. Winter, V., and Hauser, M. T. (2006) Exploring the ESCRTing machinery in eukaryotes. Trends Plant Sci. 11, 115-123 (Pubitemid 43376141)
8. Katzmann, D. J., Odorizzi, G., and Emr, S. D. (2002) Receptor down-regulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3, 8+93-905
9. Saksena, S., and Emr, S. D. (2009) ESCRTs and human disease. Biochem. Soc. Trans. 37, 167-172
10. Raiborg, C., and Stenmark, H. (2009) The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452
11. Bieniasz, P. D. (2009) The cell biology of HIV-1 virion genesis. Cell Host Microbe 5, 550-558
12. Fujii, K., Hurley, J. H., and Freed, E. O. (2007) Beyond Tsg101: the role of Alix in 'ESCRTing' HIV-1. Nat. Rev. Microbiol. 5, 912-916 (Pubitemid 350131179)
13. Williams, R. L., and Urbé, S. (2007) The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368 (Pubitemid 46643239)
14. Hurley, J. H. (2008) ESCRT complexes and the biogenesis of multivesicular bodies. Curr. Opin. Cell Biol. 20, 4-11
15. Babst, M., Wendland, B., Estepa, E. J., and Emr, S. D. (1998) The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J. 17, 2982-2993 (Pubitemid 28254371)
16. 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 (Pubitemid 350018775)
17. Yu, Z., Gonciarz, M. D., Sundquist, W. I., Hill, C. P., and Jensen, G. J. (2008) Cryo-EM structure of dodecameric Vps4p and its 2:1 complex with Vta1p. J. Mol. Biol. 377, 364-377
18. 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
19. 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 (Pubitemid 47552090)
20. 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 (Pubitemid 47552091)
21. 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 (Pubitemid 351895604)
22. Samson, R. Y., Obita, T., Freund, S. M., Williams, R. L., and Bell, S. D. (2008) A role for the ESCRT system in cell division in archaea. Science 322, 1710-1713
23. 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
24. 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
25. Babst, M., Davies, B. A., and Katzmann, D. J. (2011) Regulation of Vps4 during MVB sorting and cytokinesis. Traffic 12, 1298-1305
26. 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 Vta1. J. Cell Biol. 172, 705-717
27. 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
28. Dimaano, C., Jones, C. B., Hanono, A., Curtiss, M., and Babst, M. (2008) Ist1 regulates Vps4 localization and assembly. Mol. Biol. Cell 19, 465-474 (Pubitemid 351272136)
29. 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
30. Lottridge, J. M., Flannery, A. R., Vincelli, J. L., and Stevens, T. H. (2006) Vta1p and Vps46p regulate the membrane association and ATPase activity of Vps4p at the yeast multivesicular body. Proc. Natl. Acad. Sci. U.S.A. 103, 6202-6207
31. Scott, A., Chung, H. Y., Gonciarz-Swiatek, M., Hill, G. C., Whitby, F. G., Gaspar, J., Holton, J. M., Viswanathan, R., Ghaffarian, S., Hill, C. P., and Sundquist, W. I. (2005) Structural and mechanistic studies of VPS4 proteins. EMBO J. 24, 3658-3669 (Pubitemid 41509372)
32. Yang, D., and Hurley, J. H. (2010) Structural role of the Vps4-Vta1 interface in ESCRT-III recycling. Structure 18, 976-984
33. Bax, A., and Grzesiek, S. (1993) Methodological advances in protein NMR. Acc. Chem. Res. 26, 131-138
34. Clore, G. M., and Gronenborn, A. M. (1998) Determining the structures of large proteins and protein complexes by NMR. Trends Biotechnol. 16, 22-34 (Pubitemid 28064815)
35. 13C-labeled proteins via scalar couplings. J. Am. Chem. Soc. 115, 11054-11055
36. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
37. Goddard, T. D., and Kneller, D. G. (2001) SPARKY 3, University of California, San Francisco
38. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302 (Pubitemid 29143535)
39. Wang, C., Shen, J., Yang, Z., Chen, P., Zhao, B., Hu, W., Lan, W., Tong, X., Wu, H., Li, G., and Cao, C. (2011) Structural basis for site-specific reading of unmodified R2 of histone H3 tail by UHRF1 PHD finger. Cell Res. 21, 1379-1382
40. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (Pubitemid 126706801)
41. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph 14, 51-55 (Pubitemid 26152976)
42. 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 (Pubitemid 43779119)
43. 13C chemical-shift data. J. Biomol. NMR 4, 171-180
44. Shim, S., Merrill, S. A., and Hanson, P. I. (2008) Novel interactions of ESCRT-III with LIP5 and VPS4 and their implications for ESCRT-III disassembly. Mol. Biol. Cell 19, 2661-2672
45. Hurley, J. H., and Yang, D. (2008) MIT domainia. Dev. Cell 14, 6-8