Mechanism of recruitment and activation of the endosome-associated deubiquitinase AMSH

Biochemistry

Volumn 52, Issue 44, 2013, Pages 7818-7829

  Davies, Christopher W ^a   Paul, Lake N ^a   Das, Chittaranjan ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICAL ANALYSIS; CATALYTIC DOMAINS; CATALYTIC EFFICIENCIES; CATALYTIC MECHANISMS; DEUBIQUITINATING ENZYMES; SIGNALING RECEPTOR; SIMULTANEOUS BINDINGS; UBIQUITIN-INTERACTING MOTIFS;

CATALYSIS; CHAINS; ENZYME ACTIVITY; GENE ENCODING; MACHINERY; QUANTUM CHEMISTRY; SORTING;

CATALYST ACTIVITY;

AMSH PROTEIN; ESCRT PROTEIN; POLYUBIQUITIN; STAM PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; BIOCATALYSIS; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; THERMOSTABILITY;

CATALYTIC DOMAIN; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; ENDOSOMES; ENZYME ACTIVATION; HUMANS; KINETICS; MODELS, MOLECULAR; UBIQUITIN; UBIQUITIN THIOLESTERASE; UBIQUITIN-SPECIFIC PROTEASES;

EID: 84887695725     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401106b     Document Type: Article

References (47)

1. Maytal-Kivity, V., Reis, N., Hofmann, K., and Glickman, M. H. (2002) MPN+, a putative catalytic motif found in a subset of MPN domain proteins from eukaryotes and prokaryotes, is critical for Rpn11 function BMC Biochem. 3, 28
2. Komander, D. (2010) Mechanism, specificity and structure of the deubiquitinases Subcell. Biochem. 54, 69-87
3. Komander, D., Clague, M. J., and Urbe, S. (2009) Breaking the chains: Structure and function of the deubiquitinases Nat. Rev. Mol. Cell Biol. 10, 550-563
4. Wilkinson, K. D. (2009) DUBs at a glance J. Cell Sci. 122, 2325-2329
5. Nijman, S. M., Luna-Vargas, M. P., Velds, A., Brummelkamp, T. R., Dirac, A. M., Sixma, T. K., and Bernards, R. (2005) A genomic and functional inventory of deubiquitinating enzymes Cell 123, 773-786
6. Zhu, P., Zhou, W., Wang, J., Puc, J., Ohgi, K. A., Erdjument-Bromage, H., Tempst, P., Glass, C. K., and Rosenfeld, M. G. (2007) A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation Mol. Cell 27, 609-621
7. Sobhian, B., Shao, G., Lilli, D. R., Culhane, A. C., Moreau, L. A., Xia, B., Livingston, D. M., and Greenberg, R. A. (2007) RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites Science 316, 1198-1202
8. Avvakumov, G. V., Walker, J. R., Xue, S., Finerty, P. J., Jr., Mackenzie, F., Newman, E. M., and Dhe-Paganon, S. (2006) Amino-terminal dimerization, NRDP1-rhodanese interaction, and inhibited catalytic domain conformation of the ubiquitin-specific protease 8 (USP8) J. Biol. Chem. 281, 38061-38070
9. Clague, M. J. and Urbe, S. (2006) Endocytosis: The DUB version Trends Cell Biol. 16, 551-559
10. Wollert, T., Wunder, C., Lippincott-Schwartz, J., and Hurley, J. H. (2009) Membrane scission by the ESCRT-III complex Nature 458, 172-177
11. Saksena, S., Sun, J., Chu, T., and Emr, S. D. (2007) ESCRTing proteins in the endocytic pathway Trends Biochem. Sci. 32, 561-573
12. Roxrud, I., Stenmark, H., and Malerod, L. (2010) ESCRT & Co Biol. Cell 102, 293-318
13. McCullough, J., Row, P. E., Lorenzo, O., Doherty, M., Beynon, R., Clague, M. J., and Urbe, S. (2006) Activation of the endosome-associated ubiquitin isopeptidase AMSH by STAM, a component of the multivesicular body-sorting machinery Curr. Biol. 16, 160-165
14. Kim, M. S., Kim, J. A., Song, H. K., and Jeon, H. (2006) STAM-AMSH interaction facilitates the deubiquitination activity in the C-terminal AMSH Biochem. Biophys. Res. Commun. 351, 612-618
15. Solomons, J., Sabin, C., Poudevigne, E., Usami, Y., Hulsik, D. L., Macheboeuf, P., Hartlieb, B., Gottlinger, H., and Weissenhorn, W. (2011) Structural basis for ESCRT-III CHMP3 recruitment of AMSH Structure 19, 1149-1159
16. McDonell, L. M., Mirzaa, G. M., Alcantara, D., Schwartzentruber, J., Carter, M. T., Lee, L. J., Clericuzio, C. L., Graham, J. M., Jr., Morris-Rosendahl, D. J., Polster, T., Acsadi, G., Townshend, S., Williams, S., Halbert, A., Isidor, B., David, A., Smyser, C. D., Paciorkowski, A. R., Willing, M., Woulfe, J., Das, S., Beaulieu, C. L., Marcadier, J., Geraghty, M. T., Frey, B. J., Majewski, J., Bulman, D. E., Dobyns, W. B., O'Driscoll, M., and Boycott, K. M. (2013) Mutations in STAMBP, encoding a deubiquitinating enzyme, cause microcephaly-capillary malformation syndrome Nat. Genet. 45, 556-562
17. Carter, M. T. and Boycott, K. M. (2011) Microcephaly-capillary malformation syndrome: A story of rapid emergence of a new recognizable entity Am. J. Med. Genet., Part A 155A, 2078-2079
18. Mirzaa, G. M., Paciorkowski, A. R., Smyser, C. D., Willing, M. C., Lind, A. C., and Dobyns, W. B. (2011) The microcephaly-capillary malformation syndrome Am. J. Med. Genet., Part A 155A, 2080-2087
19. Isidor, B., Barbarot, S., Beneteau, C., Le Caignec, C., and David, A. (2011) Multiple capillary skin malformations, epilepsy, microcephaly, mental retardation, hypoplasia of the distal phalanges: Report of a new case and further delineation of a new syndrome Am. J. Med. Genet., Part A 155A, 1458-1460
20. Suzuki, S., Tamai, K., Watanabe, M., Kyuuma, M., Ono, M., Sugamura, K., and Tanaka, N. (2011) AMSH is required to degrade ubiquitinated proteins in the central nervous system Biochem. Biophys. Res. Commun. 408, 582-588
21. McCullough, J., Clague, M. J., and Urbe, S. (2004) AMSH is an endosome-associated ubiquitin isopeptidase J. Cell Biol. 166, 487-492
22. Sato, Y., Yoshikawa, A., Yamagata, A., Mimura, H., Yamashita, M., Ookata, K., Nureki, O., Iwai, K., Komada, M., and Fukai, S. (2008) Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains Nature 455, 358-362
23. Kikuchi, K., Ishii, N., Asao, H., and Sugamura, K. (2003) Identification of AMSH-LP containing a Jab1/MPN domain metalloenzyme motif Biochem. Biophys. Res. Commun. 306, 637-643
24. Agromayor, M. and Martin-Serrano, J. (2006) Interaction of AMSH with ESCRT-III and deubiquitination of endosomal cargo J. Biol. Chem. 281, 23083-23091
25. Davies, C. W., Paul, L. N., Kim, M. I., and Das, C. (2011) Structural and thermodynamic comparison of the catalytic domain of AMSH and AMSH-LP: Nearly identical fold but different stability J. Mol. Biol. 413, 416-429
26. Nakamura, M., Tanaka, N., Kitamura, N., and Komada, M. (2006) Clathrin anchors deubiquitinating enzymes, AMSH and AMSH-like protein, on early endosomes Genes Cells 11, 593-606
27. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) Analytical Ultracentrifugation in Biochemistry and Polymer Science, pp 90-125, Royal Society of Chemistry, Cambridge, U.K.
28. Brown, P. H. and Schuck, P. (2006) Macromolecular size-and-shape distributions by sedimentation velocity analytical ultracentrifugation Biophys. J. 90, 4651-4661
29. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling Biophys. J. 78, 1606-1619
30. Balbo, A., Minor, K. H., Velikovsky, C. A., Mariuzza, R. A., Peterson, C. B., and Schuck, P. (2005) Studying multiprotein complexes by multisignal sedimentation velocity analytical ultracentrifugation Proc. Natl. Acad. Sci. U.S.A. 102, 81-86
31. Dam, J. and Schuck, P. (2005) Sedimentation velocity analysis of heterogeneous protein-protein interactions: Sedimentation coefficient distributions c(s) and asymptotic boundary profiles from Gilbert-Jenkins theory Biophys. J. 89, 651-666
32. Dam, J., Velikovsky, C. A., Mariuzza, R. A., Urbanke, C., and Schuck, P. (2005) Sedimentation velocity analysis of heterogeneous protein-protein interactions: Lamm equation modeling and sedimentation coefficient distributions c(s) Biophys. J. 89, 619-634
33. Houtman, J. C., Brown, P. H., Bowden, B., Yamaguchi, H., Appella, E., Samelson, L. E., and Schuck, P. (2007) Studying multisite binary and ternary protein interactions by global analysis of isothermal titration calorimetry data in SEDPHAT: Application to adaptor protein complexes in cell signaling Protein Sci. 16, 30-42
34. Vistica, J., Dam, J., Balbo, A., Yikilmaz, E., Mariuzza, R. A., Rouault, T. A., and Schuck, P. (2004) Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition Anal. Biochem. 326, 234-256
35. Schuck, P. (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation Anal. Biochem. 320, 104-124
36. Keller, S., Vargas, C., Zhao, H., Piszczek, G., Brautigam, C. A., and Schuck, P. (2012) High-precision isothermal titration calorimetry with automated peak-shape analysis Anal. Chem. 84, 5066-5073
37. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 131, 266-280
38. Arnst, J. L., Davies, C. W., Raja, S. M., Das, C., and Natarajan, A. (2013) High-throughput compatible fluorescence resonance energy transfer-based assay to identify small molecule inhibitors of AMSH deubiquitinase activity Anal. Biochem. 440, 71-77
39. Fisher, R. D., Wang, B., Alam, S. L., Higginson, D. S., Robinson, H., Sundquist, W. I., and Hill, C. P. (2003) Structure and ubiquitin binding of the ubiquitin-interacting motif J. Biol. Chem. 278, 28976-28984
40. He, Y., Hicke, L., and Radhakrishnan, I. (2007) Structural basis for ubiquitin recognition by SH3 domains J. Mol. Biol. 373, 190-196
41. Stamenova, S. D., French, M. E., He, Y., Francis, S. A., Kramer, Z. B., and Hicke, L. (2007) Ubiquitin binds to and regulates a subset of SH3 domains Mol. Cell 25, 273-284
42. Lange, A., Ismail, M. B., Riviere, G., Hologne, M., Lacabanne, D., Guilliere, F., Lancelin, J. M., Krimm, I., and Walker, O. (2012) Competitive binding of UBPY and ubiquitin to the STAM2 SH3 domain revealed by NMR FEBS Lett. 586, 3379-3384
43. Mayers, J. R., Fyfe, I., Schuh, A. L., Chapman, E. R., Edwardson, J. M., and Audhya, A. (2011) ESCRT-0 assembles as a heterotetrameric complex on membranes and binds multiple ubiquitinylated cargoes simultaneously J. Biol. Chem. 286, 9636-9645
44. Wollert, T. and Hurley, J. H. (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes Nature 464, 864-869
45. Ren, X. and Hurley, J. H. (2010) VHS domains of ESCRT-0 cooperate in high-avidity binding to polyubiquitinated cargo EMBO J. 29, 1045-1054
46. Agromayor, M., Soler, N., Caballe, A., Kueck, T., Freund, S. M., Allen, M. D., Bycroft, M., Perisic, O., Ye, Y., McDonald, B., Scheel, H., Hofmann, K., Neil, S. J., Martin-Serrano, J., and Williams, R. L. (2012) The UBAP1 subunit of ESCRT-I interacts with ubiquitin via a SOUBA domain Structure 20, 414-428
47. Hurley, J. H. (2011) Nipped in the bud: How the AMSH MIT domain helps deubiquitinate lysosome-bound cargo Structure 19, 1033-1035