Screening E3 Substrates Using a Live Phage Display Library

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Guo, Zhengguang ^a   Wang, Xiaorong ^a   Li, Huihua ^a   Gao, Youhe ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; PROTEIN DDX42; PROTEIN MDM2; PROTEIN RPL36A; PROTEIN TP53RK; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME SUBSTRATE; ESCHERICHIA COLI; EX VIVO STUDY; GENE AMPLIFICATION; HIGH THROUGHPUT SCREENING; IN VITRO STUDY; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGE DISPLAY; PLASMID; PROTEIN EXPRESSION; PROTEIN PURIFICATION; UBIQUITINATION;

CELL LINE; CELL SURFACE DISPLAY TECHNIQUES; HEK293 CELLS; HUMANS; PEPTIDE LIBRARY; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-MDM2; REPRODUCIBILITY OF RESULTS; SUBSTRATE SPECIFICITY; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84885032078     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076622     Document Type: Article

References (76)

1. Deshaies RJ, Joazeiro CA, (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78: 399-434. doi:10.1146/annurev.biochem.78.101807.093809. PubMed: 19489725.
2. Lu JY, Lin YY, Qian J, Tao SC, Zhu J, et al. (2008) Functional dissection of a HECT ubiquitin E3 ligase. Mol Cell Proteomics 7: 35-45. PubMed: 17951556.
3. Andrews PS, Schneider S, Yang E, Michaels M, Chen H, et al. (2010) Identification of substrates of SMURF1 ubiquitin ligase activity utilizing protein microarrays. Assay Drug Dev Technol 8: 471-487. doi:10.1089/adt.2009.0264. PubMed: 20804422.
4. Merbl Y, Kirschner MW, (2009) Large-scale detection of ubiquitination substrates using cell extracts and protein microarrays. Proc Natl Acad Sci U S A 106: 2543-2548. doi:10.1073/pnas.0812892106. PubMed: 19181856.
5. Gupta R, Kus B, Fladd C, Wasmuth J, Tonikian R, et al. (2007) Ubiquitination screen using protein microarrays for comprehensive identification of Rsp5 substrates in yeast. Mol Syst Biol 3: 116. PubMed: 17551511.
6. Persaud A, Alberts P, Amsen EM, Xiong X, Wasmuth J, et al. (2009) Comparison of substrate specificity of the ubiquitin ligases Nedd4 and Nedd4-2 using proteome arrays. Mol Syst Biol 5: 333. PubMed: 19953087.
7. Burande CF, Heuzé ML, Lamsoul I, Monsarrat B, Uttenweiler-Joseph S, et al. (2009) A label-free quantitative proteomics strategy to identify E3 ubiquitin ligase substrates targeted to proteasome degradation. Mol Cell Proteomics 8: 1719-1727. doi:10.1074/mcp.M800410-MCP200. PubMed: 19376791.
8. Hör S, Ziv T, Admon A, Lehner PJ, (2009) Stable isotope labeling by amino acids in cell culture and differential plasma membrane proteome quantitation identify new substrates for the MARCH9 transmembrane E3 ligase. Mol Cell Proteomics 8: 1959-1971. doi:10.1074/mcp.M900174-MCP200. PubMed: 19457934.
9. Bartee E, McCormack A, Früh K, (2006) Quantitative membrane proteomics reveals new cellular targets of viral immune modulators. PLOS Pathog 2: e107. doi:10.1371/journal.ppat.0020107. PubMed: 17238276.
10. Yen HC, Xu Q, Chou DM, Zhao Z, Elledge SJ, (2008) Global protein stability profiling in mammalian cells. Science 322: 918-923. doi:10.1126/science.1160489. PubMed: 18988847.
11. Yen HC, Elledge SJ, (2008) Identification of SCF ubiquitin ligase substrates by global protein stability profiling. Science 322: 923-929. doi:10.1126/science.1160462. PubMed: 18988848.
12. Smith GP, (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228: 1315-1317. doi:10.1126/science.4001944. PubMed: 4001944.
13. Benhar I, (2001) Biotechnological applications of phage and cell display. Biotechnol Adv 19: 1-33. doi:10.1016/S0734-9750(00)00054-9. PubMed: 14538090.
14. Matthews DJ, Wells JA, (1993) Substrate phage: selection of protease substrates by monovalent phage display. Science 260: 1113-1117. doi:10.1126/science.8493554. PubMed: 8493554.
15. Ding L, Coombs GS, Strandberg L, Navre M, Corey DR, et al. (1995) Origins of the specificity of tissue-type plasminogen activator. Proc Natl Acad Sci U S A 92: 7627-7631. doi:10.1073/pnas.92.17.7627. PubMed: 7644467.
16. Schmitz R, Baumann G, Gram H, (1996) Catalytic specificity of phosphotyrosine kinases Blk, Lyn, c-Src and Syk as assessed by phage display. J Mol Biol 260: 664-677. doi:10.1006/jmbi.1996.0429. PubMed: 8709147.
17. Dente L, Vetriani C, Zucconi A, Pelicci G, Lanfrancone L, et al. (1997) Modified phage peptide libraries as a tool to study specificity of phosphorylation and recognition of tyrosine containing peptides. J Mol Biol 269: 694-703. doi:10.1006/jmbi.1997.1073. PubMed: 9223634.
18. Sugimura Y, Hosono M, Wada F, Yoshimura T, Maki M, et al. (2006) Screening for the preferred substrate sequence of transglutaminase using a phage-displayed peptide library: identification of peptide substrates for TGASE 2 and Factor XIIIA. J Biol Chem 281: 17699-17706. doi:10.1074/jbc.M513538200. PubMed: 16636049.
19. Hitomi K, Kitamura M, Sugimura Y, (2009) Preferred substrate sequences for transglutaminase 2: screening using a phage-displayed peptide library. Amino Acids 36: 619-624. doi:10.1007/s00726-008-0126-6. PubMed: 18651094.
20. Cahilly-Snyder L, Yang-Feng T, Francke U, George DL, (1987) Molecular analysis and chromosomal mapping of amplified genes isolated from a transformed mouse 3T3 cell line. Somat Cell Mol Genet 13: 235-244. doi:10.1007/BF01535205. PubMed: 3474784.
21. Fakharzadeh SS, Trusko SP, George DL, (1991) Tumorigenic potential associated with enhanced expression of a gene that is amplified in a mouse tumor cell line. EMBO J 10: 1565-1569. PubMed: 2026149.
22. Momand J, Jung D, Wilczynski S, Niland J, (1998) The MDM2 gene amplification database. Nucleic Acids Res 26: 3453-3459. doi:10.1093/nar/26.15.3453. PubMed: 9671804.
23. Cordon-Cardo C, Latres E, Drobnjak M, Oliva MR, Pollack D, et al. (1994) Molecular abnormalities of mdm2 and p53 genes in adult soft tissue sarcomas. Cancer Res 54: 794-799. PubMed: 8306343.
24. Landers JE, Haines DS, Strauss JF 3rd, George DL, (1994) Enhanced translation: a novel mechanism of mdm2 oncogene overexpression identified in human tumor cells. Oncogene 9: 2745-2750. PubMed: 8058341.
25. Haupt Y, Maya R, Kazaz A, Oren M, (1997) Mdm2 promotes the rapid degradation of p53. Nature 387: 296-299. doi:10.1038/387296a0. PubMed: 9153395.
26. Kubbutat MH, Jones SN, Vousden KH, (1997) Regulation of p53 stability by Mdm2. Nature 387: 299-303. doi:10.1038/387299a0. PubMed: 9153396.
27. Jin Y, Lee H, Zeng SX, Dai MS, Lu H, (2003) MDM2 promotes p21waf1/cip1 proteasomal turnover independently of ubiquitylation. EMBO J 22: 6365-6377. doi:10.1093/emboj/cdg600. PubMed: 14633995.
28. Zhang Z, Wang H, Li M, Agrawal S, Chen X, et al. (2004) MDM2 is a negative regulator of p21WAF1/CIP1, independent of p53. J Biol Chem 279: 16000-16006. doi:10.1074/jbc.M312264200. PubMed: 14761977.
29. Xu H, Zhang Z, Li M, Zhang R, (2010) MDM2 promotes proteasomal degradation of p21Waf1 via a conformation change. J Biol Chem 285: 18407-18414. doi:10.1074/jbc.M109.059568. PubMed: 20308078.
30. Di Stefano V, Mattiussi M, Sacchi A, D'Orazi G, (2005) HIPK2 inhibits both MDM2 gene and protein by, respectively, p53-dependent and independent regulations. FEBS Lett 579: 5473-5480. doi:10.1016/j.febslet.2005.09.008. PubMed: 16212962.
31. Rinaldo C, Prodosmo A, Mancini F, Iacovelli S, Sacchi A, et al. (2007) MDM2-regulated degradation of HIPK2 prevents p53Ser46 phosphorylation and DNA damage-induced apoptosis. Mol Cell 25: 739-750. doi:10.1016/j.molcel.2007.02.008. PubMed: 17349959.
32. Uchida C, Miwa S, Kitagawa K, Hattori T, Isobe T, et al. (2005) Enhanced Mdm2 activity inhibits pRB function via ubiquitin-dependent degradation. EMBO J 24: 160-169. doi:10.1038/sj.emboj.7600486. PubMed: 15577944.
33. Sdek P, Ying H, Chang DL, Qiu W, Zheng H, et al. (2005) MDM2 promotes proteasome-dependent ubiquitin-independent degradation of retinoblastoma protein. Mol Cell 20: 699-708. doi:10.1016/j.molcel.2005.10.017. PubMed: 16337594.
34. Miwa S, Uchida C, Kitagawa K, Hattori T, Oda T, et al. (2006) Mdm2-mediated pRB downregulation is involved in carcinogenesis in a p53-independent manner. Biochem Biophys Res Commun 340: 54-61. doi:10.1016/j.bbrc.2005.11.148. PubMed: 16343421.
35. Yang JY, Zong CS, Xia W, Wei Y, Ali-Seyed M, et al. (2006) MDM2 promotes cell motility and invasiveness by regulating E-cadherin degradation. Mol Cell Biol 26: 7269-7282. doi:10.1128/MCB.00172-06. PubMed: 16980628.
36. Colledge M, Snyder EM, Crozier RA, Soderling JA, Jin Y, et al. (2003) Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron 40: 595-607. doi:10.1016/S0896-6273(03)00687-1. PubMed: 14642282.
37. Girnita L, Girnita A, Larsson O, (2003) Mdm2-dependent ubiquitination and degradation of the insulin-like growth factor 1 receptor. Proc Natl Acad Sci U S A 100: 8247-8252. doi:10.1073/pnas.1431613100. PubMed: 12821780.
38. Busso CS, Iwakuma T, Izumi T, (2009) Ubiquitination of mammalian AP endonuclease (APE1) regulated by the p53-MDM2 signaling pathway. Oncogene 28: 1616-1625. doi:10.1038/onc.2009.5. PubMed: 19219073.
39. Salcedo A, Mayor F Jr., Penela P, (2006) Mdm2 is involved in the ubiquitination and degradation of G-protein-coupled receptor kinase 2. EMBO J 25: 4752-4762. doi:10.1038/sj.emboj.7601351. PubMed: 17006543.
40. Usui I, Imamura T, Huang J, Satoh H, Shenoy SK, et al. (2004) beta-arrestin-1 competitively inhibits insulin-induced ubiquitination and degradation of insulin receptor substrate 1. Mol Cell Biol 24: 8929-8937. doi:10.1128/MCB.24.20.8929-8937.2004. PubMed: 15456867.
41. Wang P, Gao H, Ni Y, Wang B, Wu Y, et al. (2003) Beta-arrestin 2 functions as a G-protein-coupled receptor-activated regulator of oncoprotein Mdm2. J Biol Chem 278: 6363-6370. doi:10.1074/jbc.M210350200. PubMed: 12488444.
42. Sánchez-Molina S, Oliva JL, García-Vargas S, Valls E, Rojas JM, et al. (2006) The histone acetyltransferases CBP/p300 are degraded in NIH 3T3 cells by activation of Ras signalling pathway. Biochem J 398: 215-224. doi:10.1042/BJ20060052. PubMed: 16704373.
43. Miyake S, Sellers WR, Safran M, Li X, Zhao W, et al. (2000) Cells degrade a novel inhibitor of differentiation with E1A-like properties upon exiting the cell cycle. Mol Cell Biol 20: 8889-8902. doi:10.1128/MCB.20.23.8889-8902.2000. PubMed: 11073989.
44. Coutts AS, Boulahbel H, Graham A, La Thangue NB, (2007) Mdm2 targets the p53 transcription cofactor JMY for degradation. EMBO Rep 8: 84-90. doi:10.1038/sj.embor.7400855. PubMed: 17170761.
45. Jin Y, Zeng SX, Lee H, Lu H, (2004) MDM2 mediates p300/CREB-binding protein-associated factor ubiquitination and degradation. J Biol Chem 279: 20035-20043. doi:10.1074/jbc.M309916200. PubMed: 14769800.
46. Legube G, Linares LK, Lemercier C, Scheffner M, Khochbin S, et al. (2002) Tip60 is targeted to proteasome-mediated degradation by Mdm2 and accumulates after UV irradiation. EMBO J 21: 1704-1712. doi:10.1093/emboj/21.7.1704. PubMed: 11927554.
47. Pan Y, Chen J, (2003) MDM2 promotes ubiquitination and degradation of MDMX. Mol Cell Biol 23: 5113-5121. doi:10.1128/MCB.23.15.5113-5121.2003. PubMed: 12860999.
48. Kawai H, Wiederschain D, Kitao H, Stuart J, Tsai KK, et al. (2003) DNA damage-induced MDMX degradation is mediated by MDM2. J Biol Chem 278: 45946-45953. doi:10.1074/jbc.M308295200. PubMed: 12963717.
49. Wyszomierski SL, Yu D, (2005) A knotty turnabout?: Akt1 as a metastasis suppressor. Cancer Cell 8: 437-439. doi:10.1016/j.ccr.2005.11.006. PubMed: 16338656.
50. Foo RS, Chan LK, Kitsis RN, Bennett MR, (2007) Ubiquitination and degradation of the anti-apoptotic protein ARC by MDM2. J Biol Chem 282: 5529-5535. PubMed: 17142834.
51. Ofir-Rosenfeld Y, Boggs K, Michael D, Kastan MB, Oren M, (2008) Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26. Mol Cell 32: 180-189. doi:10.1016/j.molcel.2008.08.031. PubMed: 18951086.
52. Buschmann T, Fuchs SY, Lee CG, Pan ZQ, Ronai Z, (2000) SUMO-1 modification of Mdm2 prevents its self-ubiquitination and increases Mdm2 ability to ubiquitinate p53. Cell 101: 753-762. doi:10.1016/S0092-8674(00)80887-9. PubMed: 10892746.
53. Li L, Deng B, Xing G, Teng Y, Tian C, et al. (2007) PACT is a negative regulator of p53 and essential for cell growth and embryonic development. Proc Natl Acad Sci U S A 104: 7951-7956. doi:10.1073/pnas.0701916104. PubMed: 17470788.
54. Hwang YC, Lu TY, Huang DY, Kuo YS, Kao CF, et al. (2009) NOLC1, an enhancer of nasopharyngeal carcinoma progression, is essential for TP53 to regulate MDM2 expression. Am J Pathol 175: 342-354. doi:10.2353/ajpath.2009.080931. PubMed: 19541936.
55. Miyamoto-Sato E, Fujimori S, Ishizaka M, Hirai N, Masuoka K, et al. (2010) A comprehensive resource of interacting protein regions for refining human transcription factor networks. PLOS ONE 5: e9289. doi:10.1371/journal.pone.0009289. PubMed: 20195357.
56. Shadat NM, Koide N, Khuda II, Dagvadorj J, Tumurkhuu G, et al. (2010) Retinoblastoma protein-interacting zinc finger 1 (RIZ1) regulates the proliferation of monocytic leukemia cells via activation of p53. Cancer Invest 28: 806-812. doi:10.3109/07357907.2010.494323. PubMed: 20594067.
57. Buyse IM, Shao G, Huang S, (1995) The retinoblastoma protein binds to RIZ, a zinc-finger protein that shares an epitope with the adenovirus E1A protein. Proc Natl Acad Sci U S A 92: 4467-4471. doi:10.1073/pnas.92.10.4467. PubMed: 7538672.
58. Buyse IM, Huang S, (1997) In vitro analysis of the E1A-homologous sequences of RIZ. J Virol 71: 6200-6203. PubMed: 9223517.
59. Scherz-Shouval R, Weidberg H, Gonen C, Wilder S, Elazar Z, et al. (2010) p53-dependent regulation of autophagy protein LC3 supports cancer cell survival under prolonged starvation. Proc Natl Acad Sci U S A 107: 18511-18516. doi:10.1073/pnas.1006124107. PubMed: 20937856.
60. Ewing RM, Chu P, Elisma F, Li H, Taylor P, et al. (2007) Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol Syst Biol 3: 89. PubMed: 17353931.
61. Abe Y, Matsumoto S, Wei S, Nezu K, Miyoshi A, et al. (2001) Cloning and characterization of a p53-related protein kinase expressed in interleukin-2-activated cytotoxic T-cells, epithelial tumor cell lines, and the testes. J Biol Chem 276: 44003-44011. doi:10.1074/jbc.M105669200. PubMed: 11546806.
62. Hannan KM, Hannan RD, Smith SD, Jefferson LS, Lun M, et al. (2000) Rb and p130 regulate RNA polymerase I transcription: Rb disrupts the interaction between UBF and SL-1. Oncogene 19: 4988-4999. doi:10.1038/sj.onc.1203875. PubMed: 11042686.
63. Cavanaugh AH, Hempel WM, Taylor LJ, Rogalsky V, Todorov G, et al. (1995) Activity of RNA polymerase I transcription factor UBF blocked by Rb gene product. Nature 374: 177-180. doi:10.1038/374177a0. PubMed: 7877691.
64. Voit R, Schäfer K, Grummt I, (1997) Mechanism of repression of RNA polymerase I transcription by the retinoblastoma protein. Mol Cell Biol 17: 4230-4237. PubMed: 9234680.
65. Zhai W, Comai L, (2000) Repression of RNA polymerase I transcription by the tumor suppressor p53. Mol Cell Biol 20: 5930-5938. doi:10.1128/MCB.20.16.5930-5938.2000. PubMed: 10913176.
66. Crawford NP, Yang H, Mattaini KR, Hunter KW, (2009) The metastasis efficiency modifier ribosomal RNA processing 1 homolog B (RRP1B) is a chromatin-associated factor. J Biol Chem 284: 28660-28673. doi:10.1074/jbc.M109.023457. PubMed: 19710015.
67. Dupont J, Renou JP, Shani M, Hennighausen L, LeRoith D, (2002) PTEN overexpression suppresses proliferation and differentiation and enhances apoptosis of the mouse mammary epithelium. J Clin Invest 110: 815-825. doi:10.1172/JCI200213829. PubMed: 12235113.
68. Dai MS, Lu H, (2004) Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5. J Biol Chem 279: 44475-44482. doi:10.1074/jbc.M403722200. PubMed: 15308643.
69. Lohrum MA, Ludwig RL, Kubbutat MH, Hanlon M, Vousden KH, (2003) Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 3: 577-587. doi:10.1016/S1535-6108(03)00134-X. PubMed: 12842086.
70. Dai MS, Zeng SX, Jin Y, Sun XX, David L, et al. (2004) Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition. Mol Cell Biol 24: 7654-7668. doi:10.1128/MCB.24.17.7654-7668.2004. PubMed: 15314173.
71. Jin A, Itahana K, O'Keefe K, Zhang Y, (2004) Inhibition of HDM2 and activation of p53 by ribosomal protein L23. Mol Cell Biol 24: 7669-7680. doi:10.1128/MCB.24.17.7669-7680.2004. PubMed: 15314174.
72. Shin S, Janknecht R, (2007) Concerted activation of the Mdm2 promoter by p72 RNA helicase and the coactivators p300 and P/CAF. J Cell Biochem 101: 1252-1265. doi:10.1002/jcb.21250. PubMed: 17226766.
73. Shu XS, Geng H, Li L, Ying J, Ma C, et al. (2011) The epigenetic modifier PRDM5 functions as a tumor suppressor through modulating WNT/beta-catenin signaling and is frequently silenced in multiple tumors. PLOS ONE 6: e27346. doi:10.1371/journal.pone.0027346. PubMed: 22087297.
74. Hicke L, (2001) Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2: 195-201. doi:10.1038/35056583. PubMed: 11265249.
75. Hofmann K, (2009) Ubiquitin-binding domains and their role in the DNA damage response. DNA Repair (Amst) 8: 544-556. doi:10.1016/j.dnarep.2009.01.003. PubMed: 19213613.
76. Hochstrasser M, (2009) Origin and function of ubiquitin-like proteins. Nature 458: 422-429. doi:10.1038/nature07958. PubMed: 19325621.