PAC1 gene knockout reveals an essential role of chaperone-mediated 20S proteasome biogenesis and latent 20S proteasomes in cellular homeostasis

Molecular and Cellular Biology

Volumn 30, Issue 15, 2010, Pages 3864-3874

  Sasaki, Katsuhiro ^a,b   Hamazaki, Jun ^b   Koike, Masato ^c   Hirano, Yuko ^a   Komatsu, Masaaki ^a   Uchiyama, Yasuo ^c   Tanaka, Keiji ^a   Murata, Shigeo ^b  

^a TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

20S PROTEASOME; BROXURIDINE; CHAPERONE; DUAL SPECIFICITY PHOSPHATASE 2; GENE PRODUCT; PROTEASOME; PROTEASOME INHIBITOR; UNCLASSIFIED DRUG; ATP DEPENDENT 26S PROTEASE; UBIQUITINATED PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOGENESIS; BRAIN DEVELOPMENT; CELL; CELL PROLIFERATION; CELL ULTRASTRUCTURE; DNA DAMAGE; ENZYME ACTIVATION; GENE INACTIVATION; GENE TARGETING; HISTOPATHOLOGY; HOMEOSTASIS; IMMUNOBLOTTING; LIVER CELL; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; REAL TIME POLYMERASE CHAIN REACTION; SENESCENCE; UBIQUITINATION; ANIMAL; CHEMISTRY; ENZYME ACTIVE SITE; GENETICS; MAMMAL; METABOLISM; MOUSE MUTANT; PHYSIOLOGICAL PROCESS; SACCHAROMYCES CEREVISIAE; TRANSGENIC MOUSE;

MAMMALIA; MUS;

ANIMALS; CATALYTIC DOMAIN; GENE KNOCKOUT TECHNIQUES; HOMEOSTASIS; MAMMALS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR CHAPERONES; PHYSIOLOGICAL PROCESSES; PROTEASOME ENDOPEPTIDASE COMPLEX; SACCHAROMYCES CEREVISIAE; UBIQUITINATED PROTEINS;

EID: 77955302229     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00216-10     Document Type: Article

References (80)

1. Abu-Bakar, A., V. Lamsa, S. Arpiainen, M. R. Moore, M. A. Lang, and J. Hakkola. 2007. Regulation of CYP2A5 gene by the transcription factor nuclear factor (erythroid-derived 2)-like 2. Drug Metab. Dispos 35:787-794. (Pubitemid 46641550)
2. Adams, J. 2004. The proteasome: a suitable antineoplastic target. Nat. Rev. Cancer. 4:349-360.
3. Andrew, W. 1962. An electron microscope study of age changes in the liver of the mouse. Am. J. Anat. 110:1-18.
4. Banning, A., S. Deubel, D. Kluth, Z. Zhou, and R. Brigelius-Flohe. 2005. The GI-GPx gene is a target for Nrf2. Mol. Cell. Biol. 25:4914-4923.
5. Baumeister, W., J. Walz, F. Zuhl, and E. Seemuller. 1998. The proteasome: paradigm of a self-compartmentalizing protease. Cell 92:367-380.
6. Beckman, K. B., and B. N. Ames. 1998. The free radical theory of aging matures. Physiol. Rev. 78:547-581.
7. Bieler, S., S. Meiners, V. Stangl, T. Pohl, and K. Stangl. 2009. Comprehensive proteomic and transcriptomic analysis reveals early induction of a protective anti-oxidative stress response by low-dose proteasome inhibition. Proteomics 9:3257-3267.
8. Breusing, N., and T. Grune. 2008. Regulation of proteasome-mediated protein degradation during oxidative stress and aging. Biol. Chem. 389:203-209.
9. Byrne, A., R. P. McLaren, P. Mason, L. Chai, M. R. Dufault, Y. Huang, B. Liang, J. D. Gans, M. Zhang, K. Carter, T. B. Gladysheva, B. A. Teicher, H. P. Biemann, M. Booker, M. A. Goldberg, K. W. Klinger, J. Lillie, S. L. Madden, and Y. Jiang. Knockdown of human deubiquitinase PSMD14 induces cell cycle arrest and senescence. Exp. Cell Res. 316:258-271.
10. Campisi, J., and F. d'Adda di Fagagna. 2007. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 8:729-740.
11. Cervantes-Laurean, D., M. J. Roberts, E. L. Jacobson, and M. K. Jacobson. 2005. Nuclear proteasome activation and degradation of carboxymethylated histones in human keratinocytes following glyoxal treatment. Free Radic Biol. Med. 38:786-795.
12. Chondrogianni, N., and E. S. Gonos. 2007. Overexpression of hUMP1/POMP proteasome accessory protein enhances proteasome-mediated antioxidant defence. Exp. Gerontol. 42:899-903.
13. Chondrogianni, N., F. L. Stratford, I. P. Trougakos, B. Friguet, A. J. Rivett, and E. S. Gonos. 2003. Central role of the proteasome in senescence and survival of human fibroblasts: induction of a senescence-like phenotype upon its inhibition and resistance to stress upon its activation. J. Biol. Chem. 278:28026-28037.
14. Chondrogianni, N., I. P. Trougakos, D. Kletsas, Q. M. Chen, and E. S. Gonos. 2008. Partial proteasome inhibition in human fibroblasts triggers accelerated M1 senescence or M2 crisis depending on p53 and Rb status. Aging Cell 7:717-732.
15. Chondrogianni, N., C. Tzavelas, A. J. Pemberton, I. P. Nezis, A. J. Rivett, and E. S. Gonos. 2005. Overexpression of proteasome beta5 assembled subunit increases the amount of proteasome and confers ameliorated response to oxidative stress and higher survival rates. J. Biol. Chem. 280: 11840-11850.
16. Collado, M., M. A. Blasco, and M. Serrano. 2007. Cellular senescence in cancer and aging. Cell 130:223-233.
17. Crone, S. A., A. Negro, A. Trumpp, M. Giovannini, and K. F. Lee. 2003. Colonic epithelial expression of ErbB2 is required for postnatal maintenance of the enteric nervous system. Neuron 37:29-40.
18. el-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
19. Essers, M. A., L. M. de Vries-Smits, N. Barker, P. E. Polderman, B. M. Burgering, and H. C. Korswagen. 2005. Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308:1181-1184.
20. Finkel, T., and N. J. Holbrook. 2000. Oxidants, oxidative stress and the biology of ageing. Nature 408:239-247.
21. Finley, D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78:477-513.
22. Fujita, T., T. Shirasawa, K. Uchida, and N. Maruyama. 1996. Gene regulation of senescence marker protein-30 (SMP30): coordinated up-regulation with tissue maturation and gradual down-regulation with aging. Mech. Ageing Dev. 87:219-229.
23. Funakoshi, M., R. J. Tomko, Jr., H. Kobayashi, and M. Hochstrasser. 2009. Multiple assembly chaperones govern biogenesis of the proteasome regulatory particle base. Cell 137:887-899.
24. Gillette, T. G., B. Kumar, D. Thompson, C. A. Slaughter, and G. N. DeMartino. 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.
25. Giorgio, M., M. Trinei, E. Migliaccio, and P. G. Pelicci. 2007. Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat. Rev. Mol. Cell Biol. 8:722-728.
26. Goldberg, A. L. 2003. Protein degradation and protection against misfolded or damaged proteins. Nature 426:895-899.
27. Graus-Porta, D., S. Blaess, M. Senften, A. Littlewood-Evans, C. Damsky, Z. Huang, P. Orban, R. Klein, J. C. Schittny, and U. Muller. 2001. Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31:367-379. (Pubitemid 32778557)
28. Guo, X., W. M. Keyes, C. Papazoglu, J. Zuber, W. Li, S. W. Lowe, H. Vogel, and A. A. Mills. 2009. TAp63 induces senescence and suppresses tumori-genesis in vivo. Nat. Cell Biol. 11:1451-1457.
29. Hamazaki, J., S. Iemura, T. Natsume, H. Yashiroda, K. Tanaka, and S. Murata. 2006. A novel proteasome interacting protein recruits the deubiquitinating enzyme UCH37 to 26S proteasomes. EMBO J. 25:4524-4536. (Pubitemid 44498126)
30. Hamazaki, J., K. Sasaki, H. Kawahara, S. Hisanaga, K. Tanaka, and S. Murata. 2007. Rpn10-mediated degradation of ubiquitinated proteins is essential for mouse development. Mol. Cell. Biol. 27:6629-6638.
31. Harris, S. L., and A. J. Levine. 2005. The p53 pathway: positive and negative feedback loops. Oncogene 24:2899-2908.
32. Hendil, K. B., R. Hartmann-Petersen, and K. Tanaka. 2002. 26 S proteasomes function as stable entities. J. Mol. Biol. 315:627-636.
33. Hirano, Y., H. Hayashi, S. Iemura, K. B. Hendil, S. Niwa, T. Kishimoto, M. Kasahara, T. Natsume, K. Tanaka, and S. Murata. 2006. Cooperation of multiple chaperones required for the assembly of mammalian 20S proteasomes. Mol. Cell 24:977-984. (Pubitemid 44960093)
34. Hirano, Y., K. B. Hendil, H. Yashiroda, S. Iemura, R. Nagane, Y. Hioki, T. Natsume, K. Tanaka, and S. Murata. 2005. A heterodimeric complex that promotes the assembly of mammalian 20S proteasomes. Nature 437:1381-1385. (Pubitemid 41568686)
35. Hirano, Y., T. Kaneko, K. Okamoto, M. Bai, H. Yashiroda, K. Furuyama, K. Kato, K. Tanaka, and S. Murata. 2008. Dissecting beta-ring assembly pathway of the mammalian 20S proteasome. EMBO J. 27:2204-2213.
36. Ishigami, A., Y. Kondo, R. Nanba, T. Ohsawa, S. Handa, S. Kubo, M. Akita, and N. Maruyama. 2004. SMP30 deficiency in mice causes an accumulation of neutral lipids and phospholipids in the liver and shortens the life span. Biochem. Biophys. Res. Commun. 315:575-580.
37. Jariel-Encontre, I., G. Bossis, and M. Piechaczyk. 2008. Ubiquitin-independent degradation of proteins by the proteasome. Biochim. Biophys. Acta 1786:153-177.
38. Jiang, Z., J. Hu, X. Li, Y. Jiang, W. Zhou, and D. Lu. 2006. Expression analyses of 27 DNA repair genes in astrocytoma by TaqMan low-density array. Neurosci. Lett. 409:112-117.
39. Jung, T., and T. Grune. 2008. The proteasome and its role in the degradation of oxidized proteins. IUBMB Life. 60:743-752.
40. Kaneko, T., J. Hamazaki, S. Iemura, K. Sasaki, K. Furuyama, T. Natsume, K. Tanaka, and S. Murata. 2009. Assembly pathway of the mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 137:914-925.
41. Kapeta, S., N. Chondrogianni, and E. S. Gonos. Nuclear erythroid factor 2-mediated proteasome activation delays senescence in human fibroblasts. J. Biol. Chem. 285:8171-8184.
42. Keyes, W. M., Y. Wu, H. Vogel, X. Guo, S. W. Lowe, and A. A. Mills. 2005. p63 deficiency activates a program of cellular senescence and leads to accelerated aging. Genes Dev. 19:1986-1999.
43. Kim, W. Y., and N. E. Sharpless. 2006. The regulation of INK4/ARF in cancer and aging. Cell 127:265-275.
44. Kleijnen, M. F., J. Roelofs, S. Park, N. A. Hathaway, M. Glickman, R. W. King, and D. Finley. 2007. Stability of the proteasome can be regulated allosterically through engagement of its proteolytic active sites. Nat. Struct. Mol. Biol. 14:1180-1188.
45. Komatsu, M., S. Waguri, T. Ueno, J. Iwata, S. Murata, I. Tanida, J. Ezaki, N. Mizushima, Y. Ohsumi, Y. Uchiyama, E. Kominami, K. Tanaka, and T. Chiba. 2005. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169:425-434. (Pubitemid 40686693)
46. Kops, G. J., T. B. Dansen, P. E. Polderman, I. Saarloos, K. W. Wirtz, P. J. Coffer, T. T. Huang, J. L. Bos, R. H. Medema, and B. M. Burgering. 2002. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419:316-321.
47. Kruse, J. P., and W. Gu. 2009. Modes of p53 regulation. Cell 137:609-622.
48. Kuk, J. L., T. J. Saunders, L. E. Davidson, and R. Ross. 2009. Age-related changes in total and regional fat distribution. Ageing Res. Rev. 8:339-348.
49. Le Tallec, B., M. B. Barrault, R. Courbeyrette, R. Guerois, M. C. Marsolier-Kergoat, and A. Peyroche. 2007. 20S proteasome assembly is orchestrated by two distinct pairs of chaperones in yeast and in mammals. Mol. Cell 27:660-674. (Pubitemid 47243701)
50. Liu, B., J. Wang, K. M. Chan, W. M. Tjia, W. Deng, X. Guan, J. D. Huang, K. M. Li, P. Y. Chau, D. J. Chen, D. Pei, A. M. Pendas, J. Cadinanos, C. Lopez-Otin, H. F. Tse, C. Hutchison, J. Chen, Y. Cao, K. S. Cheah, K. Tryggvason, and Z. Zhou. 2005. Genomic instability in laminopathy-based premature aging. Nat. Med. 11:780-785.
51. Matias, A. C., P. C. Ramos, and R. J. Dohmen. Chaperone-assisted assembly of the proteasome core particle. Biochem. Soc. Trans. 38:29-33.
52. McWalter, G. K., L. G. Higgins, L. I. McLellan, C. J. Henderson, L. Song, P. J. Thornalley, K. Itoh, M. Yamamoto, and J. D. Hayes. 2004. Transcription factor Nrf2 is essential for induction of NAD(P)H:quinone oxidoreductase 1, glutathione S-transferases, and glutamate cysteine ligase by broccoli seeds and isothiocyanates. J. Nutr. 134:3499S-3506S.
53. Meiners, S., D. Heyken, A. Weller, A. Ludwig, K. Stangl, P. M. Kloetzel, and E. Kruger. 2003. Inhibition of proteasome activity induces concerted expression of proteasome genes and de novo formation of mammalian proteasomes. J. Biol. Chem. 278:21517-21525.
54. Murata, S., H. Kawahara, S. Tohma, K. Yamamoto, M. Kasahara, Y. Nabeshima, K. Tanaka, and T. Chiba. 1999. Growth retardation in mice lacking the proteasome activator PA28gamma. J. Biol. Chem. 274:38211-38215.
55. Murata, S., H. Udono, N. Tanahashi, N. Hamada, K. Watanabe, K. Adachi, T. Yamano, K. Yui, N. Kobayashi, M. Kasahara, K. Tanaka, and T. Chiba. 2001. Immunoproteasome assembly and antigen presentation in mice lacking both PA28alpha and PA28beta. EMBO J. 20:5898-5907. (Pubitemid 33049265)
56. Murata, S., H. Yashiroda, and K. Tanaka. 2009. Molecular mechanisms of proteasome assembly. Nat. Rev. Mol. Cell Biol. 10:104-115.
57. Park, S., J. Roelofs, W. Kim, J. Robert, M. Schmidt, S. P. Gygi, and D. Finley. 2009. Hexameric assembly of the proteasomal ATPases is templated through their C termini. Nature 459:866-870.
58. Park, S., G. Tian, J. Roelofs, and D. Finley. Assembly manual for the proteasome regulatory particle: the first draft. Biochem. Soc. Trans. 38:6-13.
59. Patrick, G. N., P. Zhou, Y. T. Kwon, P. M. Howley, and L. H. Tsai. 1998. p35, the neuronal-specific activator of cyclin-dependent kinase 5 (Cdk5) is degraded by the ubiquitin-proteasome pathway. J. Biol. Chem. 273:24057-24064.
60. Périchon, R., J. M. Bourre, J. F. Kelly, and G. S. Roth. 1998. The role of peroxisomes in aging. Cell Mol. Life Sci. 54:641-652.
61. Postic, C., M. Shiota, K. D. Niswender, T. L. Jetton, Y. Chen, J. M. Moates, K. D. Shelton, J. Lindner, A. D. Cherrington, and M. A. Magnuson. 1999. Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J. Biol. Chem. 274:305-315.
62. Rabl, J., D. M. Smith, Y. Yu, S. C. Chang, A. L. Goldberg, and Y. Cheng. 2008. Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol. Cell 30:360-368. (Pubitemid 351615314)
63. Radhakrishnan, S. K., C. S. Lee, P. Young, A. Beskow, J. Y. Chan, and R. J. Deshaies. Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell 38:17-28.
64. Ramasamy, R., S. F. Yan, and A. M. Schmidt. 2006. Methylglyoxal comes of AGE. Cell 124:258-260.
65. Roelofs, J., S. Park, W. Haas, G. Tian, F. E. McAllister, Y. Huo, B. H. Lee, F. Zhang, Y. Shi, S. P. Gygi, and D. Finley. 2009. Chaperone-mediated pathway of proteasome regulatory particle assembly. Nature 459:861-865.
66. Saeki, Y., E. A. Toh, T. Kudo, H. Kawamura, and K. Tanaka. 2009. Multiple proteasome-interacting proteins assist the assembly of the yeast 19S regulatory particle. Cell 137:900-913.
67. Sakao, Y., T. Kawai, O. Takeuchi, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, K. Takeda, and S. Akira. 2000. Mouse proteasomal ATPases Psmc3 and Psmc4: genomic organization and gene targeting. Genomics 67:1-7. (Pubitemid 30471115)
68. Salceda, S., and J. Caro. 1997. Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 272:22642-22647.
69. Scaffidi, P., and T. Misteli. 2006. Lamin A-dependent nuclear defects in human aging. Science 312:1059-1063. (Pubitemid 43752916)
70. Schmidt, M., J. Hanna, S. Elsasser, and D. Finley. 2005. Proteasome-associated proteins: regulation of a proteolytic machine. Biol. Chem. 386:725-737.
71. Shibatani, T., E. J. Carlson, F. Larabee, A. L. McCormack, K. Fruh, and W. R. Skach. 2006. Global organization and function of mammalian cytosolic proteasome pools: implications for PA28 and 19S regulatory complexes. Mol. Biol. Cell 17:4962-4971.
72. Shibue, T., S. Suzuki, H. Okamoto, H. Yoshida, Y. Ohba, A. Takaoka, and T. Taniguchi. 2006. Differential contribution of Puma and Noxa in dual regulation of p53-mediated apoptotic pathways. EMBO J. 25:4952-4962. (Pubitemid 44607039)
73. Sillitoe, R. V., and A. L. Joyner. 2007. Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu. Rev. Cell Dev. Biol. 23:549-577.
74. Smith, D. M., S. C. Chang, S. Park, D. Finley, Y. Cheng, and A. L. Goldberg. 2007. Docking of the proteasomal ATPases' carboxyl termini in the 20S proteasome's alpha ring opens the gate for substrate entry. Mol. Cell 27: 731-744.
75. Sohal, R. S., and R. Weindruch. 1996. Oxidative stress, caloric restriction, and aging. Science 273:59-63. (Pubitemid 26255420)
76. Tanaka, K., and A. Ichihara. 1989. Half-life of proteasomes (multiprotease complexes) in rat liver. Biochem. Biophys. Res. Commun. 159:1309-1315.
77. Tonoki, A., E. Kuranaga, T. Tomioka, J. Hamazaki, S. Murata, K. Tanaka, and M. Miura. 2009. Genetic evidence linking age-dependent attenuation of the 26S proteasome with the aging process. Mol. Cell. Biol. 29:1095-1106.
78. Tronche, F., C. Kellendonk, O. Kretz, P. Gass, K. Anlag, P. C. Orban, R. Bock, R. Klein, and G. Schutz. 1999. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23:99-103.
79. Venugopal, R., and A. K. Jaiswal. 1996. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc. Natl. Acad. Sci. U. S. A. 93:14960-14965.
80. Villunger, A., E. M. Michalak, L. Coultas, F. Mullauer, G. Bock, M. J. Ausserlechner, J. M. Adams, and A. Strasser. 2003. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 302:1036-1038. (Pubitemid 37386194)