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01-12-2010 | NON-THEMATIC REVIEW

Feedback regulation of proteasome gene expression and its implications in cancer therapy

Author: Youming Xie

Published in: Cancer and Metastasis Reviews | Issue 4/2010

Abstract

Proteasomal protein degradation is one of the major regulatory mechanisms in the cell. Aberrant proteasome activity is directly related to the pathogenesis of many human diseases including cancers. How proteasome homeostasis is controlled is a fundamental question toward our understanding of proteasome dysregulation in cancer cells. The recent discovery of the Rpn4-proteasome negative feedback circuit provides mechanistic insight into the regulation of proteasome gene expression. This finding also has important implications in cancer therapy that uses small molecule inhibitors to target the proteasome.

Voges, D., Zwickl, P., & Baumeister, W. (1999). The 26S proteasome: A molecular machine designed for controlled proteolysis. Annual Review of Biochemistry, 68, 1015–1068.CrossRefPubMed

Finley, D. (2009). Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annual Review of Biochemistry, 78, 477–513.CrossRefPubMed

Glickman, M. H., & Ciechanover, A. (2002). The ubiquitin–proteasome proteolytic pathway: Destruction for the sake of construction. Physiological Reviews, 82, 373–428.PubMed

Pickart, C. M., & Cohen, R. E. (2004). Proteasomes and their kins: Proteases in the machine age. Nature Reviews. Molecular Cell Biology, 5, 177–187.CrossRefPubMed

Groll, M., Bochtler, M., Brandstetter, H., Clausen, T., & Huber, R. (2005). Molecular machines for protein degradation. Chembiochem, 6, 222–256.CrossRefPubMed

Nickell, S., Beck, F., Scheres, S. H., Korinek, A., Förster, F., Lasker, K., et al. (2009). Insights into the molecular architecture of the 26S proteasome. Proceedings of the National Academy of Sciences of the United States of America, 106, 11943–11947.CrossRefPubMed

Murata, S., Yashiroda, H., & Tanaka, K. (2009). Molecular mechanisms of proteasome assembly. Nature Reviews. Molecular Cell Biology, 10, 104–115.CrossRefPubMed

Marques, A. J., Palanimurugan, R., Matias, A. C., Ramos, P. C., & Dohmen, R. J. (2009). Catalytic mechanism and assembly of the proteasome. Chemical Reviews, 109, 1509–1536.CrossRefPubMed

Boes, B., Hengel, H., Ruppert, T., Multhaup, G., Koszinowski, U. H., & Kloetzel, P. M. (1994). Interferon stimulation modulates the proteolytic activity and cleavage site preference of 20S mouse proteasomes. The Journal of Experimental Medicine, 179, 901–909.CrossRefPubMed

10.

Gaczynska, M., Rock, K. L., Spies, T., & Goldberg, A. L. (1994). Peptidase activities of proteasomes are differentially regulated by the major histocompatibility complex-encoded genes for LMP2 and LMP7. Proceedings of the National Academy of Sciences of the United States of America, 91, 9213–9217.CrossRefPubMed

11.

Cardozo, C., & Kohanski, R. A. (1998). Altered properties of the branched chain amino acid-preferring activity contribute to increased cleavages after branched chain residues by the “immunoproteasome”. The Journal of Biological Chemistry, 273, 16764–16770.CrossRefPubMed

12.

Murata, S., Sasaki, K., Kishimoto, T., Niwa, S., Hayashi, H., Takahama, Y., et al. (2007). Regulation of CD8+ T cell development by thymus-specific proteasomes. Science, 316, 1349–1353.CrossRefPubMed

13.

Rabl, J., Smith, D. M., Yu, Y., Chang, S.-C., Goldberg, A. L., & Cheng, Y. (2008). Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Molecular Cell, 30, 360–368.CrossRefPubMed

14.

Smith, D. M., Chang, S. C., Park, S., Finley, D., Cheng, Y., & Goldberg, A. L. (2007). Docking of the proteasomal ATPases’ carboxyl termini in the 20S proteasome’s alpha ring opens the gate for substrate entry. Molecular Cell, 27, 731–744.CrossRefPubMed

15.

Tomko, R. J., Jr., Funakoshi, M., Schneider, K., Wang, J., & Hochstrasser, M. (2010). Heterohexameric ring arrangement of the eukaryotic proteasomal ATPases: Implications for proteasome structure and assembly. Molecular Cell, 38, 393–403.CrossRefPubMed

16.

Xie, Y., & Varshavsky, A. (2000). Physical association of ubiquitin ligases and the 26S proteasome. Proceedings of the National Academy of Sciences of the United States of America, 97, 2497–2502.CrossRefPubMed

17.

Xie, Y., & Varshavsky, A. (2002). UFD4 lacking the proteasome-binding region catalyses ubiquitination but is impaired in proteolysis. Nature Cell Biology, 4, 1003–1007.CrossRefPubMed

18.

Crosas, B., Hanna, J., Kirkpatrick, D.S., Zhang, D.P., Tone, Y., Hathaway, N.A., et al. (2006). Ubiquitin chains are remodeled at the proteasome by opposing ubiquitin ligase and deubiquitinating activities. Cell, 127, 1401–1413.CrossRefPubMed

19.

You, J., & Pickart, C. M. (2001). A HECT domain E3 enzyme assembles novel polyubiquitin chains. The Journal of Biological Chemistry, 276, 19871–19878.CrossRefPubMed

20.

Russell, S. J., Steger, K. A., & Johnston, S. A. (1999). Subcellular localization, stoichiometry, and protein levels of the 26S proteasome subunits in yeast. The Journal of Biological Chemistry, 274, 21943–21952.CrossRefPubMed

21.

Glickman, M. H., Rubin, D. M., Fried, V. A., & Finley, D. (1998). The regulatory particle of the Saccharomyces cerevisiae proteasome. Molecular and Cellular Biology, 18, 3149–3162.PubMed

22.

Mannhaupt, G., Schnall, R., Karpov, V., Vetter, I., & Feldmann, H. (1999). Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast. FEBS Letters, 450, 27–34.CrossRefPubMed

23.

Xie, Y., & Varshavsky, A. (2001). RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: A negative feedback circuit. Proceedings of the National Academy of Sciences of the United States of America, 98, 3056–3061.CrossRefPubMed

24.

Ju, D., Wang, L., Mao, X., & Xie, Y. (2004). Homeostatic regulation of the proteasome via an Rpn4-dependent feedback circuit. Biochemical and Biophysical Research Communications, 321, 51–57.CrossRefPubMed

25.

Wang, X., Xu, H., Ju, D., & Xie, Y. (2008). Disruption of Rpn4-induced proteasome expression in Saccharomyces cerevisiae reduces cell viability under stressed conditions. Genetics, 180, 1945–1953.CrossRefPubMed

26.

London, M., Keck, B. I., Ramos, P. C., & Dohmen, R. J. (2004). Regulatory mechanisms controlling biogenesis of ubiquitin and the proteasome. FEBS Letters, 567, 259–264.CrossRefPubMed

27.

Jelinsky, S. A., Estep, P., Church, G. M., & Samson, L. D. (2000). Regulatory networks revealed by transcriptional profiling of damaged Saccharomyces cerevisiae cells: Rpn4 links base excision repair with proteasomes. Molecular and Cellular Biology, 20, 8157–8167.CrossRefPubMed

28.

Gasch, A. P., Huang, M., Metzner, S., Botstein, D., Elledge, S. J., & Brown, P. O. (2001). Genomic expression response to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Molecular Biology of the Cell, 12, 2987–3003.PubMed

29.

Owsianik, G., Balzi, E., & Ghislain, M. (2002). Control of 26S proteasome expression by transcription factors regulating multidrug resistance in Saccharomyces cerevisiae. Molecular Microbiology, 43, 1295–1308.CrossRefPubMed

30.

Hahn, J.-S., Neef, D. W., & Thiele, D. J. (2006). A stress regulatory network for co-ordinated activation of proteasome expression mediated by yeast heat shock transcription factor. Molecular Microbiology, 60, 240–251.CrossRefPubMed

31.

Haugen, A. C., Kelley, R., Collins, J. B., Tucker, C. J., Deng, C., Afshari, C. A., et al. (2004). Integrating phenotypic and expression profiles to map arsenic-response networks. Genome Biology, 5, R95.CrossRefPubMed

32.

Guo, N., Yu, L., Meng, R., Fan, J., Wang, D., Sun, G., et al. (2008). Global gene expression profile of Saccharomyces cerevisiae induced by dictamnine. Yeast, 25, 631–641.CrossRefPubMed

33.

Salin, H., Fardeau, V., Piccini, E., Lelandais, G., Tanty, V., Lemoine, S., et al. (2008). Structure and properties of transcriptional networks driving selenite stress response in yeasts. BMC Genomics, 9, 333.CrossRefPubMed

34.

Mizukami-Murata, S., Iwahashi, H., Kimura, S., Nojima, K., Sakurai, Y., Saitou, T., et al. (2010). Genome-wide expression changes in Saccharomyces cerevisiae in response to high-LET ionizing radiation. Applied Biochemistry and Biotechnology, 162, 855–870.CrossRefPubMed

35.

Ng, D. T. W., Spear, E. D., & Walter, P. (2000). The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. The Journal of Cell Biology, 150, 77–88.CrossRefPubMed

36.

Cai, H., Kauffman, S., Naider, F., & Becker, J. M. (2006). Genomewide screen reveals a wide regulatory network for di/tripeptide utilization in Saccharomyces cerevisiae. Genetics, 172, 1459–1476.CrossRefPubMed

37.

Metzger, M. B., & Michaelis, S. (2009). Analysis of quality control substrates in distinct cellular compartments reveals a unique role for Rpn4p in tolerating misfolded membrane proteins. Molecular Biology of the Cell, 20, 1006–1019.CrossRefPubMed

38.

Hausmann, S., Zheng, S., Costanzo, M., Brost, R. L., Garcin, D., Boone, C., et al. (2008). Genetic and biochemical analysis of yeast and human cap trimethylguanosine synthase: Functional overlap of 2, 2, 7-trimethylguanosine caps, small nuclear ribonucleoprotein components, pre-mRNA splicing factors, and RNA decay pathways. The Journal of Biological Chemistry, 283, 31706–31718.CrossRefPubMed

39.

Teixeira, M. C., Dias, P. J., Simões, T., & Sá-Correia, I. (2008). Yeast adaptation to mancozeb involves the up-regulation of FLR1 under the coordinate control of Yap1, Rpn4, Pdr3, and Yrr1. Biochemical and Biophysical Research Communications, 367, 249–255.CrossRefPubMed

40.

Bosis, E., Salomon, D., Ohayon, O., Sivan, G., Bar-Nun, S., & Rabinovich, E. (2010). Ssz1 restores endoplasmic reticulum-associated protein degradation in cells expressing defective cdc48-ufd1-npl4 complex by upregulating cdc48. Genetics, 184, 695–706.CrossRefPubMed

41.

Wang, X., Xu, H., Ha, S.-W., Ju, D., & Xie, Y. (2010). Proteasomal degradation of Rpn4 in Saccharomyces cerevisiae is critical for cell viability under stressed conditions. Genetics, 184, 335–342.CrossRefPubMed

42.

Ju, D., Wang, X., Ha, S.-W., Fu, J., & Xie, Y. (2010). Inhibition of proteasomal degradation of Rpn4 impairs nonhomologous end-joining repair of DNA double-strand breaks. PLoS ONE, 5, e9877.CrossRefPubMed

43.

Mannhaupt, G., & Feldmann, H. (2007). Genomic evolution of the proteasome system among hemiascomycetous yeasts. Journal of Molecular Evolution, 65, 529–540.CrossRefPubMed

44.

Gasch, A. P., Moses, A. M., Chiang, D. Y., Fraser, H. B., Berardini, M., & Eisen, M. B. (2004). Conservation and evolution of cis-regulatory systems in Ascomycete fungi. PLoS Biology, 2, e398.CrossRefPubMed

45.

Meiners, S., Heyken, D., Weller, A., Ludwig, A., Stangl, K., Kloetzel, P.-M., et al. (2003). Inhibition of proteasome activity induces concerted expression of proteasome genes and de novo formation of Mammalian proteasomes. The Journal of Biological Chemistry, 278, 21517–21525.CrossRefPubMed

46.

Fleming, J. A., Lightcap, E. S., Sadis, S., Thoroddsen, V., Bulawa, C. E., & Blackman, R. K. (2002). Complementary whole-genome technologies reveal the cellular response to proteasome inhibition by PS-341. Proceedings of the National Academy of Sciences of the United States of America, 99, 1461–1466.CrossRefPubMed

47.

Lundgren, J., Masson, P., Realini, C. A., & Young, P. (2003). Use of RNA interference and complementation to study the function of the Drosophila and human 26S proteasome subunit S13. Molecular and Cellular Biology, 23, 5320–5330.CrossRefPubMed

48.

Wójcik, C., & DeMartino, G. N. (2002). RNA interference of valosin-containing protein (VCP/p97) reveals multiple cellular roles linked to ubiquitin/proteasome-dependent proteolysis. The Journal of Biological Chemistry, 277, 6188–6197.CrossRefPubMed

49.

Xu, H., Ju, D., Jarois, T., & Xie, Y. (2008). Diminished feedback regulation of proteasome expression and resistance to proteasome inhibitors in breast cancer cells. Breast Cancer Research and Treatment, 107, 267–274.CrossRefPubMed

50.

Sato, Y., Sakamoto, K., Sei, M., Ewis, A. A., & Nakahori, Y. (2009). Proteasome subunits are regulated and expressed in comparable concentrations as a functional cluster. Biochemical and Biophysical Research Communications, 378, 795–798.CrossRefPubMed

51.

Kraft, D. C., Deocaris, C. C., Wadhwa, R., & Rattan, S. I. S. (2006). Preincubation with the proteasome inhibitor MG-132 enhances proteasome activity via the Nrf2 transcription factor in aging human skin fibroblasts. Annals of the New York Academy of Sciences, 1067, 420–424.CrossRefPubMed

52.

Lee, C.-S., Tee, L. Y., Warmke, T., Vinjamoori, A., Cai, A., Fagan, A. M., et al. (2004). A proteasomal stress response: Pre-treatment with proteasome inhibitors increases proteasome activity and reduces neuronal vulnerability to oxidative injury. Journal of Neurochemistry, 91, 966–1006.

53.

Radhakrishnan, S. K., Lee, C. S., Young, P., Beskow, A., Chan, J. Y., & Deshaies, R. (2010). Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Molecular Cell, 38, 17–28.CrossRefPubMed

54.

Kwak, M. K., Wakabayashi, N., Greenlaw, J. L., Yamamoto, M., & Kensler, T. W. (2003). Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Molecular and Cellular Biology, 23, 8786–8794.CrossRefPubMed

55.

Kwak, M. K., & Kensler, T. W. (2006). Induction of 26S proteasome subunit PSMB5 by the bifunctional inducer 3-methycholanthrene through the Nrf2-ARE, but not the AhR/Arnt-XRE, pathway. Biochemical and Biophysical Research Communications, 345, 1350–1357.CrossRefPubMed

56.

Arlt, A., Bauer, I., Schafmayer, C., Tepel, J., Müerköster, S. S., Brosch, M., et al. (2009). Increased proteasome subunit protein expression and proteasome activity in colon cancer relate to an enhanced activation of nuclear factor E2-related factor 2 (Nrf2). Oncogene, 28, 3983–3996.CrossRefPubMed

57.

Kapeta, S., Chondrogianni, N., & Gonos, E. S. (2010). Nuclear erythroid factor 2 (Nrf2) mediated proteasome activation delays senescence in human fibroblasts. The Journal of Biological Chemistry, 285, 8171–8184.CrossRefPubMed

58.

Moi, P., Chan, K., Asunis, I., Cao, A., & Kan, Y. W. (1994). Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proceedings of the National Academy of Sciences of the United States of America, 91, 9926–9930.CrossRefPubMed

59.

Kensler, T. W., Wakabayashi, N., & Biswal, S. (2007). Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annual Review of Pharmacology and Toxicology, 47, 89–116.CrossRefPubMed

60.

Nguyen, T., Nioi, P., & Pickett, C. B. (2009). The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. The Journal of Biological Chemistry, 284, 13291–13295.CrossRefPubMed

61.

Orlowski, R. Z., & Kuhn, D. J. (2008). Proteasome inhibitors in cancer therapy: Lessons from the first decade. Clinical Cancer Research, 14, 1649–1657.CrossRefPubMed

62.

Schwartz, A. L., & Ciechanover, A. (1999). The ubiquitin-proteasome pathway and pathogenesis of human diseases. Annual Review of Medicine, 50, 57–74.CrossRefPubMed

63.

Kumatori, A., Tanaka, K., Inamura, N., Sone, S., Ogura, T., Matsumoto, T., et al. (1990). Abnormally high expression of proteasomes in human leukemic cells. Proceedings of the National Academy of Sciences of the United States of America, 87, 7071–7075.CrossRefPubMed

64.

Chen, L., & Madura, K. (2005). Increased proteasome activity, ubiquitin-conjugating enzymes, and eEF1A translation factor detected in breast cancer tissue. Cancer Research, 65, 5599–5606.CrossRefPubMed

65.

Bazzaro, M., Lee, M. K., Zoso, A., Stirling, W. L., Santillan, A., Shih, Ie M, et al. (2006). Ubiquitin-proteasome system stress sensitizes ovarian cancer to proteasome inhibitor-induced apoptosis. Cancer Research, 66, 3754–3763.CrossRefPubMed

66.

Pilarsky, C., Wenzig, M., Specht, T., Saeger, H. D., & Grützmann, R. (2004). Identification and validation of commonly overexpressed genes in solid tumors by comparison of microarray data. Neoplasia, 6, 744–750.CrossRefPubMed

67.

Milano, A., Iaffaioli, R. V., & Caponigro, F. (2007). The proteasome: A worthwhile target for the treatment of solid tumours? European Journal of Cancer, 43, 1125–1133.CrossRefPubMed

68.

Papandreou, C. N., Daliani, D. D., Nix, D., Yang, H., Madden, T., Wang, X., et al. (2004). Phase I trial of the proteasome inhibitor bortezomib in patients with advanced solid tumors with observations in androgen-independent prostate cancer. Journal of Clinical Oncology, 22, 2108–2121.CrossRefPubMed

69.

Schwartz, R., & Davidson, T. (2004). Pharmacology, pharmacokinetics, and practical applications of bortezomib. Oncology (Williston Park), 18(14 Suppl 11), 14–21.

70.

Chen, S., Blank, J. L., Peters, T., Liu, X. J., Rappoli, D. M., Pickard, M. D., et al. (2010). Genome-wide siRNA screen for modulators of cell death induced by proteasome inhibitor bortezomib. Cancer Research, 70, 4318–4326.CrossRefPubMed

71.

Pan, X., Ye, P., Yuan, D. S., Wang, X., Bader, J. S., & Boeke, J. D. (2006). A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell, 124, 1069–1081.CrossRefPubMed

72.

Tong, A. H., Lesage, G., Bader, G. D., Ding, H., Xu, H., Xin, X., et al. (2004). Global mapping of the yeast genetic interaction network. Science, 303, 808–813.CrossRefPubMed

73.

Ju, D., Wang, X., & Xie, Y. (2009). Dyclonine and alverine citrate enhance the cytotoxic effects of proteasome inhibitor MG132 on breast cancer cells. International Journal of Molecular Medicine, 23, 205–209.PubMed

74.

Lees, N. D., Skaggs, B., Kirsch, D. R., & Bard, M. (1995). Cloning of the late genes in the ergosterol biosynthetic pathway of Saccharomyces cerevisiae—a review. Lipids, 30, 221–226.CrossRefPubMed

75.

Bennati, A. M., Castelli, M., Fazia, M. A. D., Beccari, T., Caruso, D., Servillo, G., et al. (2006). Sterol dependent regulation of human TM7SF2 gene expression: Role of the encoded 3β-hydroxysterol Δ¹⁴-reductase in human cholesterol biosynthesis. Biochimica et Biophysica Acta, 1761, 677–685.PubMed

76.

Holmer, L., Pezhman, A., & Worman, H. J. (1998). The human lamin B receptor/sterol reductase multigene family. Genomics, 54, 469–476.CrossRefPubMed

77.

Giaever, G., Flaherty, P., Kumm, J., Proctor, M., Nislow, C., Jaramillo, D. F., et al. (2004). Chemogenomic profiling: Identifying the functional interactions of small molecules in yeast. Proceedings of the National Academy of Sciences of the United States of America, 101, 793–798.CrossRefPubMed

78.

Powell, S. R., Wang, P., Katzeff, H., Shringarpure, R., Teoh, C., Khaliulin, I., et al. (2005). Oxidized and ubiquitinated proteins may predict recovery of postischemic cardiac function: Essential role of the proteasome. Antioxidants Redox Signaling, 7, 538–546.CrossRefPubMed

79.

Zong, C., Gomes, A. V., Drews, O., Li, X., Young, G. W., Berhane, B., et al. (2006). Regulation of murine cardiac 20S proteasomes: Role of associating partners. Circulation Research, 99, 372–380.CrossRefPubMed

80.

Zhang, F., Su, K., Yang, X., Bowe, D. B., Paterson, A. J., & Kudlow, J. E. (2003). O-GlcNAc modification is an endogenous inhibitor of the proteasome. Cell, 115, 715–725.CrossRefPubMed

81.

Kimura, Y., Saeki, Y., Yokosawa, H., Polevoda, B., Sherman, F., & Hirano, H. (2003). N-Terminal modifications of the 19S regulatory particle subunits of the yeast proteasome. Archives of Biochemistry and Biophysics, 409, 341–348.CrossRefPubMed

Title: Feedback regulation of proteasome gene expression and its implications in cancer therapy
Author: Youming Xie
Publication date: 01-12-2010
Publisher: Springer US
Published in: Cancer and Metastasis Reviews / Issue 4/2010
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI: https://doi.org/10.1007/s10555-010-9255-y

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