Molecular and cellular roles of PI31 (PSMF1) protein in regulation of proteasome function

Journal of Biological Chemistry

Volumn 289, Issue 25, 2014, Pages 17392-17405

  Li, Xiaohua ^a   Thompson, David ^a   Kumar, Brajesh ^a   DeMartino, George N ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERENCE SUPPRESSION;

26 S PROTEASOME; ADP-RIBOSYLATION; C-TERMINAL DOMAINS; HYDROPHOBIC AMINO ACIDS; MOLECULAR FEATURE; MULTIPLE REGIONS; RNA INTERFERENCE; STRUCTURAL RELATIONSHIP;

AMINO ACIDS;

PROTEASOME; PROTEIN PI31; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME REGULATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; STEADY STATE;

HBYX MOTIF; PI31; PROTEASE INHIBITOR; PROTEASOME; PROTEIN COMPLEX; PROTEIN DEGRADATION; UBIQUITIN-DEPENDENT PROTEASE;

AMINO ACID MOTIFS; ANIMALS; DROSOPHILA MELANOGASTER; HEK293 CELLS; HELA CELLS; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 84903475943     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.561183     Document Type: Article

References (54)

1. DeMartino, G. N., and Gillette, T. G. (2007) Proteasomes: machines for all reasons. Cell 129, 659-662 (Pubitemid 46802388)
2. Baumeister, W., Walz, J., Zühl, F., and Seemüller, E. (1998) The proteasome: paradigm of a self-compartmentalizing protease. Cell 92, 367-380 (Pubitemid 28093014)
3. Bochtler, M., Ditzel, L., Groll, M., Hartmann, C., and Huber, R. (1999) The proteasome. Annu. Rev. Biophys. Biomol. Struct. 28, 295-317 (Pubitemid 29319261)
4. Groll, M., Ditzel, L., Löwe, J., Stock, D., Bochtler, M., Bartunik, H. D., and Huber, R. (1997) Structure of the 20 S proteasome from yeast at 2.4 Å resolution. Nature 386, 463-471 (Pubitemid 27164066)
5. Murata, S., Sasaki, K., Kishimoto, T., Niwa, S., Hayashi, H., Takahama, Y., and Tanaka, K. (2007) Regulation of CD8+ T cell development by thymus-specific proteasomes. Science 316, 1349-1353 (Pubitemid 46871657)
6. Murata, S., Takahama, Y., and Tanaka, K. (2008) Thymoproteasome: probable role in generating positively selecting peptides. Curr. Opin. Immunol. 20, 192-196
7. Gaczynska, M., Rock, K. L., and Goldberg, A. L. (1993) γ-Interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes. Nature 365, 264-267 (Pubitemid 23282087)
8. Akiyama, K., Yokota, K., Kagawa, S., Shimbara, N., Tamura, T., Akioka, H., Nothwang, H. G., Noda, C., Tanaka, K., and Ichihara, A. (1994) cDNA cloning and interferon γ down-regulation of proteasomal subunits X and Y. Science 265, 1231-1234 (Pubitemid 24291981)
9. Gaczynska, M., Goldberg, A. L., Tanaka, K., Hendil, K. B., and Rock, K. L. (1996) Proteasome subunits X and Y alter peptidase activities in opposite ways to the interferon-γ-induced subunits LMP2 and LMP7. J. Biol. Chem. 271, 17275-17280 (Pubitemid 26244285)
10. Groll, M., Bajorek, M., Köhler, A., Moroder, L., Rubin, D. M., Huber, R., Glickman, M. H., and Finley, D.(2000) A gated channel into the proteasome core particle. Nat. Struct. Biol. 7, 1062-1067
11. Stadtmueller, B. M., and Hill, C. P. (2011) Proteasome activators. Mol. Cell 41, 8-19
12. Adams, G. M., Crotchett, B., Slaughter, C. A., DeMartino, G. N., and Gogol, E. P. (1998) Formation of proteasome-PA700 complexes directly correlates with activation of peptidase activity. Biochemistry 37, 12927-12932 (Pubitemid 28433526)
13. Gray, C. W., Slaughter, C. A., and DeMartino, G. N. (1994) PA28 activator protein forms regulatory caps on proteasome stacked rings. J. Mol. Biol. 236, 7-15 (Pubitemid 24148942)
14. Köhler, A., Cascio, P., Leggett, D. S., Woo, K. M., Goldberg, A. L., and Finley, D. (2001) The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release. Mol. Cell 7, 1143-1152 (Pubitemid 32607349)
15. Förster, A., Masters, E. I., Whitby, F. G., Robinson, H., and Hill, C. P. (2005) The 1.9 A structure of a proteasome-11S activator complex and implication for proteasome-PAN/PA700 interactions. Mol. Cell 18, 589-599 (Pubitemid 40726235)
16. Whitby, F. G., Masters, E. I., Kramer, L., Knowlton, J. R., Yao, Y., Wang, C. C., and Hill, C. P. (2000) Structural basis for the activation of 20 S proteasomes by 11S regulators. Nature 408, 115-120
17. Rechsteiner, M., and Hill, C. P. (2005) Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends Cell Biol. 15, 27-33 (Pubitemid 40094678)
18. Zhang, Z., Clawson, A., Realini, C., Jensen, C. C., Knowlton, J. R., Hill, C. P., and Rechsteiner, M. (1998) Identification of an activation region in the proteasome activator REGα. Proc. Natl. Acad. Sci. U.S.A. 95, 2807-2811 (Pubitemid 28135810)
19. Li, J., Gao, X., Joss, L., and Rechsteiner, M. (2000) The proteasome activator 11S REG or PA28: chimeras implicate carboxyl-terminal sequences in oligomerization and proteasome binding but not in the activation of specific proteasome catalytic subunits. J. Mol. Biol. 299, 641-654
20. Gillette, T. G., Kumar, B., Thompson, D., Slaughter, C. A., and DeMartino, G. N. (2008) Differential roles of the COOH termini of AAA subunits of PA700 (19 S regulator) in asymmetric assembly and activation of the 26 S proteasome. J. Biol. Chem. 283, 31813-31822
21. Sadre-Bazzaz, K., Whitby, F. G., Robinson, H., Formosa, T., and Hill, C. P. (2010) Structure of a Blm10 complex reveals common mechanisms for proteasome binding and gate opening. Mol. Cell 37, 728-735
22. Stadtmueller, B. M., Ferrell, K., Whitby, F. G., Heroux, A., Robinson, H., Myszka, D. G., and Hill, C. P. (2010) Structural models for interactions between the 20 S proteasome and its PAN/19S activators. J. Biol. Chem. 285, 13-17
23. Rabl, J., Smith, D. M., Yu, Y., Chang, S. C., Goldberg, A. L., and Cheng, Y. (2008) Mechanism of gate opening in the 20 S proteasome by the proteasomal ATPases. Mol. Cell 30, 360-368 (Pubitemid 351615314)
24. Smith, D. M., Chang, S. C., Park, S., Finley, D., Cheng, Y., and Goldberg, A. L. (2007) Docking of the proteasomal ATPases' carboxyl termini in the 20 S proteasome α ring opens the gate for substrate entry. Mol. Cell 27, 731-744 (Pubitemid 47333222)
25. Dange, T., Smith, D., Noy, T., Rommel, P. C., Jurzitza, L., Cordero, R. J., Legendre, A., Finley, D., Goldberg, A. L., and Schmidt, M. (2011) Blm10 protein promotes proteasomal substrate turnover by an active gating mechanism. J. Biol. Chem. 286, 42830-42839
26. Yu, Y., Smith, D. M., Kim, H. M., Rodriguez, V., Goldberg, A. L., and Cheng, Y. (2010) Interactions of PAN's C termini with archaeal 20 S proteasome and implications for the eukaryotic proteasome-ATPase interactions. EMBO J. 29, 692-702
27. Hirano, Y., Hendil, K. B., Yashiroda, H., Iemura, S., Nagane, R., Hioki, Y., Natsume, T., Tanaka, K., and Murata, S. (2005) A heterodimeric complex that promotes the assembly of mammalian 20 S proteasome. Nature 437, 1381-1385 (Pubitemid 41568686)
28. Kusmierczyk, A. R., Kunjappu, M. J., Funakoshi, M., and Hochstrasser, M. (2008) A multimeric assembly factor controls formation of alternative 20 S proteasomes. Nat. Struct. Mol. Biol. 15, 237-244 (Pubitemid 351654044)
29. Kusmierczyk, A. R., Kunjappu, M. J., Kim, R. Y., and Hochstrasser, M. (2011) A conserved 20 S proteasome assembly factor requires a C-terminal HbYX motif for proteasomal precursor binding. Nat. Struct. Mol. Biol. 18, 622-629
30. Sasaki, K., Hamazaki, J., Koike, M., Hirano, Y., Komatsu, M., Uchiyama, Y., Tanaka, K., and Murata, S. (2010) PAC1 gene knockout reveals an essential role of chaperone-mediated 20 S proteasome biogenesis and latent 20 S proteasomes in cellular homeostasis. Mol. Cell. Biol. 30, 3864-3874
31. Stadtmueller, B. M., Kish-Trier, E., Ferrell, K., Petersen, C. N., Robinson, H., Myszka, D. G., Eckert, D. M., Formosa, T., and Hill, C. P. (2012) Structure of a proteasome-Pba1-Pba2 complex: Implications for proteasome assembly, activation, and biological function. J. Biol. Chem. 287, 37371-37382
32. McCutchen-Maloney, S. L., Matsuda, K., Shimbara, N., Binns, D. D., Tanaka, K., Slaughter, C. A., and DeMartino, G. N.(2000) cDNA cloning, expression, and functional characterization of PI31, a proline-rich inhibitor of the proteasome. J. Biol. Chem. 275, 18557-18565 (Pubitemid 30414818)
33. Kirk, R., Laman, H., Knowles, P. P., Murray-Rust, J., Lomonosov, M., Meziane el K., and McDonald, N. Q. (2008) Structure of a conserved dimerization domain within the F-box protein Fbxo7 and the PI31 proteasome inhibitor. J. Biol. Chem. 283, 22325-22335
34. Ma, C.-P., Slaughter, C. A., and DeMartino, G. N. (1992) Purification and characterization of a protein inhibitor of the 20 S proteasome (macropain). Biochim. Biophys. Acta 1119, 303-311
35. Bader, M., Benjamin, S., Wapinski, O. L., Smith, D. M., Goldberg, A. L., and Steller, H. (2011) A conserved F box regulatory complex controls proteasome activity in Drosophila. Cell 145, 371-382
36. Kumar, B., Kim, Y. C., and DeMartino, G. N. (2010) The C terminus of Rpt3, an ATPase subunit of PA700 (19 S) regulatory complex, is essential for 26 S proteasome assembly but not for activation. J. Biol. Chem. 285, 39523-39535
37. DeMartino, G. N. (2005) Purification of PA700, the 19S regulatory complex of the 26 S proteasome. Methods Enzymol. 398, 295-306
38. Liu, C. W., Li, X., Thompson, D., Wooding, K., Chang, T. L., Tang, Z., Yu, H., Thomas, P. J, and DeMartino, G. N. (2006) ATP binding and ATP hydrolysis play distinct roles in the function of 26 S proteasome. Mol. Cell 24, 39-50 (Pubitemid 44466684)
39. McGuire, M. J., McCullough, M. L., Croall, D. E., and DeMartino, G. N. (1989) The high molecular weight multicatalytic proteinase, macropain, exists in a latent form in human erythrocytes. Biochim. Biophys. Acta 995, 181-186 (Pubitemid 19088375)
40. Thompson, D., Hakala, K., and DeMartino, G. N. (2009) Subcomplexes of PA700, the 19 S regulator of the 26 S proteasome, reveal relative roles of AAA subunits in 26 S proteasome assembly and activation and ATPase activity. J. Biol. Chem. 284, 24891-24903
41. Kim, Y. C., Li, X., Thompson, D., and DeMartino, G. N. (2013) ATPbinding by proteasomal ATPases regulates cellular assembly and substrate-induced functions of the 26 S proteasome. J. Biol. Chem. 288, 3334-3345
42. McGuire, M. J., and DeMartino, G. N. (1986) Purification and characterization of a high molecular weight protease (macropain) from human erythrocytes. Biochim. Biophys. Acta 873, 279-289 (Pubitemid 16027835)
43. Wójcik, C., Rowicka, M., Kudlicki, A., Nowis, D., McConnell, E., Kujawa, M., and DeMartino, G. N. (2006) Valosin-containing protein (p97) is a regulator of endoplasmic reticulum stress and of the degradation of N-end rule and ubiquitin-fusion degradation pathway substrates in mammalian cells. Mol. Biol. Cell 17, 4606-4618 (Pubitemid 44665732)
44. Kim, Y. C., and DeMartino, G. N. (2011) C termini of proteasomal ATPases play nonequivalent roles in cellular assembly of mammalian 26 S proteasome. J. Biol. Chem. 286, 26652-26666
45. Koulich, E., Li, X., and DeMartino, G. N. (2008) Relative Structural and functional roles of multiple deubiquitylating proteins associated with mammalian 26 S proteasome. Mol. Biol. Cell 19, 1072-1082 (Pubitemid 351481820)
46. DeMartino, G. N., Moomaw, C. R., Zagnitko, O. P., Proske, R. J., Ma, C.-P., Afendis, S. J., Swaffield, J. C., and Slaughter, C. A. (1994) PA700, an ATP-dependent activator of the 20 S proteasome, is an ATPase containing multiple members of a nucleotide-binding protein family. J. Biol. Chem. 269, 20878-20884 (Pubitemid 24266450)
47. Cho-Park, P. F., and Steller, H. (2013) Proteasome Regulation by ADPRibosylation. Cell 153, 614-627
48. Huang, S. M., Mishina, Y. M., Liu, S., Cheung, A., Stegmeier, F., Michaud, G. A., Charlat, O., Wiellette, E., Zhang, Y., Wiessner, S., Hild, M., Shi, X., Wilson, C. J., Mickanin, C., Myer, V., Fazal, A., Tomlinson, R., Serluca, F., Shao, W., Cheng, H., Shultz, M., Rau, C., Schirle, M., Schlegl, J., Ghidelli, S., Fawell, S., Lu, C., Curtis, D., Kirschner, M. W., Lengauer, C., Finan, P. M., Tallarico, J. A., Bouwmeester, T., Porter, J. A., Bauer, A., and Cong, F. (2009) Tankyrase inhibition stabilizes axin and antagonizes Wnt signaling. Nature 461, 614-620
49. Ma, C.-P., Slaughter, C. A., and DeMartino, G. N. (1992) Identification, purification, and characterization of a protein activator (PA28) of the 20 S proteasome. J. Biol. Chem. 267, 10515-10523
50. Chu-Ping, M., Vu, J. H., Proske, R. J., Slaughter, C. A., and DeMartino, G. N. (1994) Identification, purification, and characterization of a highmolecular weight, ATP-dependent activator (PA700) of the 20 S proteasome. J. Biol. Chem. 269, 3539-3547 (Pubitemid 24237678)
51. Guettler, S., LaRose, J., Petsalaki, E., Gish, G., Scotter, A., Pawson, T., Rottapel, R., and Sicheri, F. (2011) Structural basis and sequence rules for substrate recognition by Tankyrase explain the basis for cherubism disease. Cell 147, 1340-1354
52. Sbodio, J. I., and Chi, N. W. (2002) Identification of a tankyrase-binding motif shared by IRAP, TAB182, and human TRF1 but not mouse TRF1. NuMA contains this RXXPDG motif and is a novel tankyrase partner. J. Biol. Chem. 277, 31887-31892 (Pubitemid 34968996)
53. Djakovic, S. N., Marquez-Lona, E. M., Jakawich, S. K., Wright, R., Chu, C., Sutton, M. A., and Patrick, G. N. (2012) Phosphorylation of Rpt6 regulates synaptic strength in hippocampal neurons. J. Neurosci. 32, 5126-5131
54. Hamilton, A. M., Oh, W. C., Vega-Ramirez, H., Stein, I. S., Hell, J. W., Patrick, G. N., and Zito, K. (2012) Activity-dependent growth of new dendritic spines is regulated by the proteasome. Neuron. 74, 1023-1030