Inhibition of proteasomal degradation of Rpn4 impairs nonhomologous end-joining repair of DNA double-strand breaks

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Ju, Donghong ^a   Wang, Xiaogang ^a   Ha, Seung Wook ^a   Fu, Jiejun ^a   Xie, Youming ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; PROTEASOME; PROTEIN MEC1; PROTEIN YKU70; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RPN4; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; RPN4 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA REPAIR; DNA STRAND BREAKAGE; DOWN REGULATION; ENZYME INHIBITION; GENE DELETION; GENE EXPRESSION; NONHUMAN; PROTEIN DEGRADATION; PROTEIN SECRETION; DOUBLE STRANDED DNA BREAK; DRUG ANTAGONISM; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, FUNGAL; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 77956320509     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009877     Document Type: Article

References (56)

1. Nelson MK, Kurihara T, Silver PA (1993) Extragenic suppressors of mutations in the cytoplasmic C terminus of SEC63 define five genes in Saccharomyces cerevisie. Genetics 134: 159-173.
2. Finley D, Tanaka K, Mann C, Feldmann H, Hochstrasser M, et al. (1998) Unified nomenclature for subunits of the Saccharomyces cerevisiae proteasome regulatory particle. Trends Biochem Sci 23: 244-245.
3. Johnson ES, Ma PC, Ota IM, Varshavsky A (1995) A proteolytic pathway that recognizes ubiquitin as a degradation signal. J Biol Chem 270: 17442-17456.
4. 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 Lett 450: 27-34.
5. Xie Y, Varshavsky A (2001) RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: A negative feedback circuit. Proc Natl Acad Sci USA 98: 3056-3061.
6. Ju D, Xie Y (2004) Proteasomal degradation of RPN4 via two distinct mechanisms: Ubiquitin-dependent and -independent. J Biol Chem 279: 23851-23854.
7. Ju D, Xie Y (2006) Identification of the preferential ubiquitination site and ubiquitin-dependent degradation signal of Rpn4. J Biol Chem 281: 10657-10662.
8. Ju D, Xu H, Wang X, Xie Y (2007) Ubiquitin-mediated degradation of Rpn4 is controlled by a phosphorylation-dependent ubiquitylation signal. Biochim Biophys Acta 1773: 1672-1680.
9. Wang L, Mao X, Ju D, Xie Y (2004) Rpn4 is a physiological substrate of the Ubr2 ubiquitin ligase. J Biol Chem 279: 55218-55223.
10. Ju D, Wang X, Xu H, Xie Y (2008) Genome-wide analysis identifies MYNDdomain protein Mub1 as an essential factor for Rpn4 ubiquitylation. Mol Cell Biol 28: 1404-1412.
11. Ju D, Wang L, Mao X, Xie Y (2004) Homeostatic regulation of the proteasome via an Rpn4-dependent feedback circuit. Biochem Biophys Res Commun 321: 51-57.
12. London M, Keck BI, Ramos PC, Dohmen RJ (2004) Regulatory mechanisms controlling biogenesis of ubiquitin and the proteasome. FEBS Lett 567: 259-264.
13. Lundgren J, Masson P, Realini CA, Young P (2003) Use of RNA interference and complementation to study the function of the Drosophila and human 26S proteasome subunit S13. Mol Cell Biol 23: 5320-5330.
14. Meiners S, Heyken D, Weller A, Ludwig A, Stangl K, et al. (2003) Inhibition of proteasome activity induces concerted expression of proteasome genes and de novo formation of Mammalian proteasomes. J Biol Chem 278: 21517-21525.
15. Wójcik C, DeMartino GN (2002) Analysis of Drosophila 26S proteasome using RNA interference. J Biol Chem 277: 6188-6197.
16. 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 Res Treat 107: 267-274.
17. Jelinsky SA, Estep P, Church GM, Samson LD (2000) Regulatory networks revealed by transcriptional profiling of damaged Saccharomyces cerevisiae cells: Rpn4 links base excision repair with proteasomes. Mol Cell Biol 20: 8157-8167.
18. Haugen AC, Kelley R, Collins JB, Tucker CJ, Deng C, et al. (2004) Integrating phenotypic and expression profiles to map arsenic-response networks. Genome Biol 5: R95.
19. Gasch AP, Huang M, Metzner S, Botstein D, Elledge SJ, et al. (2001) Genomic expression response to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol Biol Cell 12: 2987-3003.
20. Guo N, Yu L, Meng R, Fan J, Wang D, et al. (2008) Global gene expression profile of Saccharomyces cerevisiae induced by dictamnine. Yeast 25: 631-641.
21. Hausmann S, Zheng S, Costanzo M, Brost RL, Garcin D, 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. J Biol Chem 283: 31706-31718.
22. Salin H, Fardeau V, Piccini E, Lelandais G, Tanty V, et al. (2008) Structure and properties of transcriptional networks driving selenite stress response in yeasts. BMC Genomics 9: 333.
23. Teixeira MC, Dias PJ, 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. Biochem Biophys Res Commun 367: 249-255.
24. Hahn J-S, Neef DW, Thiele DJ (2006) A stress regulatory network for coordinated activation of proteasome expression mediated by yeast heat shock transcription factor. Mol Microbiol 60: 240-251.
25. Owsianik G, Balzi E, Ghislain M (2002) Control of 26S proteasome expression by transcription factors regulating multidrug resistance in Saccharomyces cerevisiae. Mol Microbiol 43: 1295-1308.
26. Hanna J, Meides A, Zhang DP, Finley D (2007) A ubiquitin stress response induces altered proteasome composition. Cell 129: 747-759.
27. 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.
28. 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.
29. Ju D, Xu H, Wang X, Xie Y (2010) The transcription activation domain of Rpn4 is separate from its degrons. Intl Biochem Cell Biol 42: 282-286.
30. Zhao X, Muller EG, Rothstein R (1998) A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol Cell 2: 329-340.
31. Sanchez Y, Desany BA, Jones WJ, Liu Q, Wang B, et al. (1996) Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271: 357-360.
32. Majka J, Burgers PM (2007) Clamping the Mec1/ATR checkpoint kinase into action. Cell Cycle 6: 1157-1160.
33. Rouse J, Jackson SP (2002) Interfaces between the detection, signaling, and repair of DNA damage. Science 297: 547-551.
34. Foss EJ (2001) Tof1p regulates DNA damage responses during S phase in Saccharomyces cerevisiae. Genetics 157: 567-577.
35. Hodgson B, Calzada A, Labib K (2007) Mrc1 and Tof1 regulate DNA replication forks in different ways during normal S phase. Mol Biol Cell 18: 3894-3902.
36. Katou Y, Kanoh Y, Bando M, Noguchi H, Tanaka H, et al. (2003) S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424: 1078-1083.
37. Morrow DM, Tagle DA, Shiloh Y, Collins FS, Hieter P (1995) TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1. Cell 82: 831-840.
38. Greenwell PW, Kronmal SL, Porter SE, Gassenhuber J, Obermaier B, et al. (1995) TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene. Cell 82: 823-829.
39. Pâques F, Leung W-Y, Haber JE (1998) Expansions and contractions in a tandem repeat induced by double-strand break repair. Mol Cell Biol 18: 2045-2054.
40. Daley JM, Palmbos PL, Wu D, Wilson TE (2005) Nonhomologous end joining in yeast. Annu Rev Genetics 39: 431-451.
41. Haber JE (1998) Mating-type gene switching in Saccharomyces cerevisiae. Annu Rev Genet 32: 561-599.
42. Krogan NJ, Lam MHY, Fillingham J, Keogh M-C, Gebbia M, et al. (2004) Proteasome involvement in the repair of DNA double-strand breaks. Mol Cell 16: 1027-1034.
43. Jessulat M, Alamgir M, Salsali H, Greenblat J, Xu J, et al. (2008) Interacting proteins Rtt109 and Vps75 affect the efficiency of non-homologous end-joining in Saccharomyces cerevisiae. Arch Biochem Biophys 469: 157-164.
44. Papamichos-Chronakis M, Krebs JE, Peterson CL (2006) Interplay between Ino80 and Swr1 chromatin remodeling enzymes regulates cell cycle checkpoint adaptation in response to DNA damage. Genes Dev 20: 2437-2449.
45. van Attikum H, Fritsch O, Gasser SM (2007) Distinct roles for SRW1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J 26: 4113-4125.
46. Shim EY, Ma J-L, Oum J-H, Yanez, Lee SE (2005) The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breakers. Mol Cell Biol 25: 3934-3944.
47. Wilson TE (2002) A genome-based screen for yeast mutants with an altered recombination/end-joining repair ratio. Genetics 162: 677-688.
48. Wu X, Wilson TE, Lieber MR (1999) A role for FEN-1 in nonhomologous DNA end joining: the order of strand annealing and nucleolytic processing events. Proc Natl Acad Sci USA 96: 1303-1308.
49. Chan C, Galli A, Schiestl RH (2008) Pol3 is involved in nonhomologous endjoining in Saccharomyces cerevisiae. DNA Repair 7: 1531-1541.
50. Fujimoro M, Tanaka K, Yokosawa H, Toh-e A (1998) Son1p is a component of the 26S proteasome of the yeast Saccharomyces cerevisiae, FEBS Lett 423: 149-154.
51. Schnerder J, Bajwa P, Johnson FC, Bhaumik SR, Shilatifard A (2006) Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J Biol Chem 281: 37270-37274.
52. Clikeman JA, Khalsa GJ, Barton SL, Nickoloff JA (2001) Homologous recombination repair of double-strand breaks in yeast in enhanced by MAT heterozygosity through yKu-dependent and-independent mechanism. Genetics 157: 579-589.
53. Zhang Y, Hefferin ML, Chen L, Shim EY, Tseng H-M, et al. (2007) Role of Dnl4-Lif1 in nonhomologous end-joining repair complex assembly and suppression of homologous recombination. Nat Struc Mol Biol 14: 639-646.
54. Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
55. Schmitt ME, Brown TA, Trumpower BL (1990) A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res 18: 3091-3092.
56. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.