Recombinant expression, reconstitution and structure of human anaphase-promoting complex (APC/C)

Biochemical Journal

Volumn 449, Issue 2, 2013, Pages 365-371

  Zhang, Ziguo ^a   Yang, Jing ^a   Kong, Eric H ^a   Chao, William C H ^a   Morris, Edward P ^a   Da Fonseca, Paula C A ^a   Barford, David ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Anaphase promoting complex cyclosome (APC C); Cell cycle; Recombinant expression; Single particle electron microscopy; Three dimensional structure; Ubiquitination

Indexed keywords

ANAPHASE PROMOTING COMPLEX; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; CELL CYCLE PROGRESSION; CELL DENSITY; HUMAN; IN VITRO STUDY; MIXED INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN QUATERNARY STRUCTURE; SACCHAROMYCES CEREVISIAE; THREE DIMENSIONAL IMAGING; UBIQUITINATION;

ANIMALS; CELL CYCLE PROTEINS; CELL LINE; HUMANS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; VERTEBRATA;

EID: 84871404634     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121374     Document Type: Article

References (54)

1. Sali, A., Glaeser, R., Earnest, T. and Baumeister, W. (2003) From words to literature in structural proteomics. Nature 422, 216-225 (Pubitemid 36362759)
2. Gavin, A. C., Aloy, P., Grandi, P., Krause, R., Boesche, M., Marzioch, M., Rau, C., Jensen, L. J., Bastuck, S., Dumpelfeld, B. et al. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440, 631-636
3. Alberts, B. (1998) The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92, 291-294
4. Sharon, M. and Robinson, C. V. (2007) The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annu. Rev. Biochem. 76, 167-193
5. Pines, J. (2011) Cubism and the cell cycle: the many faces of the APC/C. Nat. Rev. Mol. Cell Biol. 12, 427-438
6. Thornton, B. R., Ng, T. M., Matyskiela, M. E., Carroll, C. W., Morgan, D. O. and Toczyski, D. P. (2006) An architectural map of the anaphase-promoting complex. Genes Dev. 20, 449-460 (Pubitemid 43244399)
7. Peters, J. M. (2006) The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 7, 644-656
8. Sullivan, M. and Morgan, D. O. (2007) Finishing mitosis, one step at a time. Nat. Rev. Mol. Cell Biol. 8, 894-903 (Pubitemid 47622563)
9. Barford, D. (2011) Structural insights into anaphase-promoting complex function and mechanism. Philos. Trans. R. Soc., B 366, 3605-3624
10. Glotzer, M., Murray, A. W. and Kirschner, M. W. (1991) Cyclin is degraded by the ubiquitin pathway. Nature 349, 132-138 (Pubitemid 21912025)
11. King, R. W., Glotzer, M. and Kirschner, M. W. (1996) Mutagenic analysis of the destruction signal of mitotic cyclins and structural characterization of ubiquitinated intermediates. Mol. Biol. Cell 7, 1343-1357 (Pubitemid 26304198)
12. Pfleger, C. M. and Kirschner, M. W. (2000) The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev. 14, 655-665 (Pubitemid 30176820)
13. Burton, J. L. and Solomon, M. J. (2001) D box and KEN box motifs in budding yeast Hsl1p are required for APC-mediated degradation and direct binding to Cdc20p and Cdh1p. Genes Dev. 15, 2381-2395 (Pubitemid 32899742)
14. Hilioti, Z., Chung, Y. S., Mochizuki, Y., Hardy, C. F. and Cohen-Fix, O. (2001) The anaphase inhibitor Pds1 binds to the APC/C-associated protein Cdc20 in a destruction box-dependent manner. Curr. Biol. 11, 1347-1352 (Pubitemid 32835875)
15. Kraft, C., Vodermaier, H. C., Maurer-Stroh, S., Eisenhaber, F. and Peters, J. M. (2005) The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol. Cell 18, 543-553 (Pubitemid 40726231)
16. Pfleger, C. M., Lee, E. and Kirschner, M. W. (2001) Substrate recognition by the Cdc20 and Cdh1 components of the anaphase-promoting complex. Genes Dev. 15, 2396-2407 (Pubitemid 32899743)
17. Schwab, M., Neutzner, M., Mocker, D. and Seufert, W. (2001) Yeast Hct1 recognizes the mitotic cyclin Clb2 and other substrates of the ubiquitin ligase APC. EMBO J. 20, 5165-5175 (Pubitemid 32910911)
18. Carroll, C. W. and Morgan, D. O. (2002) The Doc1 subunit is a processivity factor for the anaphase-promoting complex. Nat. Cell Biol. 4, 880-887 (Pubitemid 35331363)
19. Passmore, L. A., McCormack, E. A., Au, S. W., Paul, A., Willison, K. R., Harper, J. W. and Barford, D. (2003) Doc1 mediates the activity of the anaphase-promoting complex by contributing to substrate recognition. EMBO J. 22, 786-796 (Pubitemid 36227781)
20. Carroll, C. W., Enquist-Newman, M. and Morgan, D. O. (2005) The APC subunit Doc1 promotes recognition of the substrate destruction box. Curr. Biol. 15, 11-18 (Pubitemid 40084696)
21. da Fonseca, P. C., Kong, E. H., Zhang, Z., Schreiber, A., Williams, M. A., Morris, E. P. and Barford, D. (2011) Structures of APC/C(Cdh1) with substrates identify Cdh1 and Apc10 as the D-box co-receptor. Nature 470, 274-278
22. Hutchins, J. R., Toyoda, Y., Hegemann, B., Poser, I., Heriche, J. K., Sykora, M. M., Augsburg, M., Hudecz, O., Buschhorn, B. A., Bulkescher, J. et al. (2010) Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 328, 593-599
23. Kops, G. J., van der Voet, M., Manak, M. S., van Osch, M. H., Naini, S. M., Brear, A., McLeod, I. X., Hentschel, D. M., Yates, 3rd, J. R., van den Heuvel, S. and Shah, J. V. (2010) APC16 is a conserved subunit of the anaphase-promoting complex/cyclosome. J. Cell Sci. 123, 1623-1633
24. Schreiber, A., Stengel, F., Zhang, Z., Enchev, R. I., Kong, E. H., Morris, E. P., Robinson, C. V., da Fonseca, P. C. and Barford, D. (2011) Structural basis for the subunit assembly of the anaphase-promoting complex. Nature 470, 227-232
25. Berger, I., Fitzgerald, D. J. and Richmond, T. J. (2004) Baculovirus expression system for heterologous multiprotein complexes. Nat. Biotechnol. 22, 1583-1587 (Pubitemid 40039463)
26. Bieniossek, C., Richmond, T. J. and Berger, I. (2008) MultiBac: multigene baculovirus-based eukaryotic protein complex production. Curr. Protoc. Protein Sci. Chapter 5, Unit 5.20
27. Fitzgerald, D. J., Berger, P., Schaffitzel, C., Yamada, K., Richmond, T. J. and Berger, I. (2006) Protein complex expression by using multigene baculoviral vectors. Nat. Methods 3, 1021-1032 (Pubitemid 44782702)
28. Fitzgerald, D. J., Schaffitzel, C., Berger, P., Wellinger, R., Bieniossek, C., Richmond, T. J. and Berger, I. (2007) Multiprotein expression strategy for structural biology of eukaryotic complexes. Structure 15, 275-279 (Pubitemid 46366723)
29. Trowitzsch, S., Bieniossek, C., Nie, Y., Garzoni, F. and Berger, I. (2010) New baculovirus expression tools for recombinant protein complex production. J. Struct. Biol. 172, 45-54
30. Vijayachandran, L. S., Viola, C., Garzoni, F., Trowitzsch, S., Bieniossek, C., Chaillet, M., Schaffitzel, C., Busso, D., Romier, C., Poterszman, A. et al. (2011) Robots, pipelines, polyproteins: enabling multiprotein expression in prokaryotic and eukaryotic cells. J. Struct. Biol. 175, 198-208
31. Bieniossek, C., Imasaki, T., Takagi, Y. and Berger, I. (2012) MultiBac: expanding the research toolbox for multiprotein complexes. Trends Biochem. Sci. 37, 49-57
32. Yu, H., Peters, J. M., King, R. W., Page, A. M., Hieter, P. and Kirschner, M. W. (1998) Identification of a cullin homology region in a subunit of the anaphase-promoting complex. Science 279, 1219-1222 (Pubitemid 28164376)
33. Mansfeld, J., Collin, P., Collins, M. O., Choudhary, J. S. and Pines, J. (2011) APC15 drives the turnover of MCC-CDC20 to make the spindle assembly checkpoint responsive to kinetochore attachment. Nat. Cell Biol. 13, 1234-1243
34. Dube, P., Herzog, F., Gieffers, C., Sander, B., Riedel, D., Muller, S. A., Engel, A., Peters, J. M. and Stark, H. (2005) Localization of the coactivator Cdh1 and the cullin subunit Apc2 in a cryo-electron microscopy model of vertebrate APC/C. Mol. Cell 20, 867-879 (Pubitemid 41814876)
35. Herzog, F., Primorac, I., Dube, P., Lenart, P., Sander, B., Mechtler, K., Stark, H. and Peters, J. M. (2009) Structure of the anaphase-promoting complex/cyclosome interacting with a mitotic checkpoint complex. Science 323, 1477-1481
36. Bitinaite, J., Rubino, M., Varma, K. H., Schildkraut, I., Vaisvila, R. and Vaiskunaite, R. (2007) USER friendly DNA engineering and cloning method by uracil excision. Nucleic Acids Res. 35, 1992-2002 (Pubitemid 47061665)
37. Geu-Flores, F., Nour-Eldin, H. H., Nielsen, M. T. and Halkier, B. A. (2007) USER fusion: a rapid and efficient method for simultaneous fusion and cloning of multiple PCR products. Nucleic Acids Res. 35, e55
38. Nour-Eldin, H. H., Hansen, B. G., Norholm, M. H., Jensen, J. K. and Halkier, B. A. (2006) Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res. 34, e122
39. Passmore, L. A., Barford, D. and Harper, J. W. (2005) Purification and assay of the budding yeast anaphase-promoting complex. Methods Enzymol. 398, 195-219 (Pubitemid 41578885)
40. Ludtke, S. J., Baldwin, P. R. and Chiu, W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (Pubitemid 30013436)
41. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M. and Leith, A. (1996) SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199 (Pubitemid 26093143)
42. van Heel, M., Gowen, B., Matadeen, R., Orlova, E. V., Finn, R., Pape, T., Cohen, D., Stark, H., Schmidt, R., Schatz, M. and Patwardhan, A. (2000) Single-particle electron cryo-microscopy: towards atomic resolution. Q. Rev. Biophys. 33, 307-369 (Pubitemid 32151706)
43. da Fonseca, P. C., He, J. and Morris, E. P. (2012) Molecular model of the human 26S proteasome. Mol. Cell 46, 54-66
44. Enchev, R. I., Scott, D. C., da Fonseca, P. C., Schreiber, A., Monda, J. K., Schulman, B. A., Peter, M. and Morris, E. P. (2012) Structural basis for a reciprocal regulation between SCF and CSN. Cell Rep. 2, 616-627
45. Navaza, J., Lepault, J., Rey, F. A., Alvarez-Rua, C. and Borge, J. (2002) On the fitting of model electron densities into EM reconstructions: a reciprocal-space formulation. Acta Crystallogr. Sect. D Biol. Crystallogr. 58, 1820-1825 (Pubitemid 35169750)
46. Buschhorn, B. A., Petzold, G., Galova, M., Dube, P., Kraft, C., Herzog, F., Stark, H. and Peters, J. M. (2011) Substrate binding on the APC/C occurs between the coactivator Cdh1 and the processivity factor Doc1. Nat. Struct. Mol. Biol. 18, 6-13
47. Passmore, L. A., Booth, C. R., Venien-Bryan, C., Ludtke, S. J., Fioretto, C., Johnson, L. N., Chiu, W. and Barford, D. (2005) Structural analysis of the anaphase-promoting complex reveals multiple active sites and insights into polyubiquitylation. Mol. Cell 20, 855-866 (Pubitemid 41814875)
48. Ohi, M. D., Feoktistova, A., Ren, L., Yip, C., Cheng, Y., Chen, J. S., Yoon, H. J., Wall, J. S., Huang, Z., Penczek, P. A. et al. (2007) Structural organization of the anaphase-promoting complex bound to the mitotic activator Slp1. Mol. Cell 28, 871-885 (Pubitemid 350217056)
49. Han, D., Kim, K., Kim, Y., Kang, Y. and Lee, J. Y. (2009) Crystal structure of the N-terminal domain of anaphase-promoting complex subunit 7. J. Biol. Chem. 284, 15137-15146
50. Shakes, D. C., Allen, A. K., Albert, K. M. and Golden, A. (2011) emb-1 encodes the APC16 subunit of the Caenorhabditis elegans anaphase-promoting complex. Genetics 189, 549-560
51. Chao, W. C., Kulkarni, K., Zhang, Z., Kong, E. H. and Barford, D. (2012) Structure of the mitotic checkpoint complex. Nature 484, 208-213
52. Imasaki, T., Calero, G., Cai, G., Tsai, K. L., Yamada, K., Cardelli, F., Erdjument-Bromage, H., Tempst, P., Berger, I., Kornberg, G. L. et al. (2011) Architecture of the mediator head module. Nature 475, 240-243
53. Enchev, R. I., Schreiber, A., Beuron, F. and Morris, E. P. (2010) Structural insights into the COP9 signalosome and its common architecture with the 26S proteasome lid and eIF3. Structure 18, 518-527
54. Liu, Q., Greimann, J. C. and Lima, C. D. (2006) Reconstitution, activities, and structure of the eukaryotic RNA exosome. Cell 127, 1223-1237 (Pubitemid 44894519)