Phosphoribosylation of Ubiquitin Promotes Serine Ubiquitination and Impairs Conventional Ubiquitination

Cell

Volumn 167, Issue 6, 2016, Pages 1636-1649.e13

  Bhogaraju, Sagar ^a   Kalayil, Sissy ^a   Liu, Yaobin ^a   Bonn, Florian ^a   Colby, Thomas ^b   Matic, Ivan ^b   Dikic, Ivan ^a,c  

^a GOETHE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

^c UNIVERSITY OF SPLIT   (Croatia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ARGININE; BACTERIAL PROTEIN; HYDROXYL GROUP; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHODIESTERASE; PROTEASOME; PROTEIN SDEA; RIBOSE; SERINE; TUMOR NECROSIS FACTOR; UBIQUITIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E1; UBIQUITIN PROTEIN LIGASE E2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; 8-OXODGTPASE; ADENOSINE TRIPHOSPHATE; DNA LIGASE; INORGANIC PYROPHOSPHATASE; MEMBRANE PROTEIN; PHOSPHATASE; PHOSPHORIBOSYLADENOSINE TRIPHOSPHATE; SDEA PROTEIN, LEGIONELLA PNEUMOPHILA;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CATALYSIS; CHEMICAL BOND; CHEMICAL MODIFICATION; CHEMICAL REACTION; CONJUGATION; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME DEGRADATION; ENZYME INACTIVATION; FEMALE; FUNGAL STRAIN; HUMAN; HUMAN CELL; LEGIONELLA PNEUMOPHILA; MITOPHAGY; NONHUMAN; PHOSPHORIBOSYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; UBIQUITINATION; ANALOGS AND DERIVATIVES; HELA CELL LINE; HOST PATHOGEN INTERACTION; LEGIONNAIRE DISEASE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATE; DNA REPAIR ENZYMES; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MEMBRANE PROTEINS; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORIC MONOESTER HYDROLASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PYROPHOSPHATASES; SACCHAROMYCES CEREVISIAE; SERINE; UBIQUITIN; UBIQUITINATION;

EID: 85001889664     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.11.019     Document Type: Article

References (64)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.-W., Kapral, G.J., Grosse-Kunstleve, R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 213–221.
2. Alva, V., Nam, S.-Z., Söding, J., Lupas, A.N., The MPI bioinformatics Toolkit as an integrative platform for advanced protein sequence and structure analysis. Nucleic Acids Res. 44:W1 (2016), W410–W415.
3. Bardill, J.P., Miller, J.L., Vogel, J.P., IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol. Microbiol. 56 (2005), 90–103.
4. Burch, T.J., Haas, A.L., Site-directed mutagenesis of ubiquitin. Differential roles for arginine in the interaction with ubiquitin-activating enzyme. Biochemistry 33 (1994), 7300–7308.
5. Ciehanover, A., Hod, Y., Hershko, A., A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes. Biochem. Biophys. Res. Commun. 81 (1978), 1100–1105.
6. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26 (2008), 1367–1372.
7. Cui, J., Yao, Q., Li, S., Ding, X., Lu, Q., Mao, H., Liu, L., Zheng, N., Chen, S., Shao, F., Glutamine deamidation and dysfunction of ubiquitin/NEDD8 induced by a bacterial effector family. Science 329 (2010), 1215–1218.
8. Daniels, C.M., Ong, S.-E., Leung, A.K.L., Phosphoproteomic approach to characterize protein mono- and poly(ADP-ribosyl)ation sites from cells. J. Proteome Res. 13 (2014), 3510–3522.
9. Daniels, C.M., Ong, S.-E., Leung, A.K.L., The promise of proteomics for the study of ADP-ribosylation. Mol. Cell 58 (2015), 911–924.
10. Daniels, C.M., Thirawatananond, P., Ong, S.-E., Gabelli, S.B., Leung, A.K.L., Nudix hydrolases degrade protein-conjugated ADP-ribose. Sci. Rep., 5, 2015, 18271.
11. Dantuma, N.P., Groothuis, T.A.M., Salomons, F.A., Neefjes, J., A dynamic ubiquitin equilibrium couples proteasomal activity to chromatin remodeling. J. Cell Biol. 173 (2006), 19–26.
12. Di Fiore, P.P., von Zastrow, M., Endocytosis, signaling, and beyond. Cold Spring Harb. Perspect. Biol., 6, 2014 a016865–a016865.
13. Duerksen-Hughes, P.J., Xu, X.X., Wilkinson, K.D., Structure and function of ubiquitin: evidence for differential interactions of arginine-74 with the activating enzyme and the proteases of ATP-dependent proteolysis. Biochemistry 26 (1987), 6980–6987.
14. Emsley, P., Cowtan, K., Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004), 2126–2132.
15. Ensminger, A.W., Isberg, R.R., E3 ubiquitin ligase activity and targeting of BAT3 by multiple Legionella pneumophila translocated substrates. Infect. Immun. 78 (2010), 3905–3919.
16. Finley, D., Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78 (2009), 477–513.
17. Geisler, S., Holmström, K.M., Skujat, D., Fiesel, F.C., Rothfuss, O.C., Kahle, P.J., Springer, W., PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12 (2010), 119–131.
18. Götze, M., Pettelkau, J., Schaks, S., Bosse, K., Ihling, C.H., Krauth, F., Fritzsche, R., Kühn, U., Sinz, A., StavroX-a software for analyzing crosslinked products in protein interaction studies. J. Am. Soc. Mass Spectrom. 23 (2012), 76–87.
19. Grabbe, C., Husnjak, K., Dikic, I., The spatial and temporal organization of ubiquitin networks. Nat. Rev. Mol. Cell Biol. 12 (2011), 295–307.
20. Havey, J.C., Roy, C.R., Toxicity and SidJ-mediated suppression of toxicity require distinct regions in the SidE family of Legionella pneumophila effectors. Infect. Immun. 83 (2015), 3506–3514.
21. Herhaus, L., Dikic, I., Expanding the ubiquitin code through post-translational modification. EMBO Rep. 16 (2015), 1071–1083.
22. Hershko, A., Ciechanover, A., Varshavsky, A., The ubiquitin system. Nat. Med. 6 (2000), 1073–1081.
23. Hicks, S.W., Galán, J.E., Exploitation of eukaryotic subcellular targeting mechanisms by bacterial effectors. Nat. Rev. Microbiol. 11 (2013), 316–326.
24. Hospenthal, M.K., Freund, S.M.V., Komander, D., Assembly, analysis and architecture of atypical ubiquitin chains. Nat. Struct. Mol. Biol. 20 (2013), 555–565.
25. Hsu, F., Luo, X., Qiu, J., Teng, Y.-B., Jin, J., Smolka, M.B., Luo, Z.-Q., Mao, Y., The Legionella effector SidC defines a unique family of ubiquitin ligases important for bacterial phagosomal remodeling. Proc. Natl. Acad. Sci. USA 111 (2014), 10538–10543.
26. Hubber, A., Roy, C.R., Modulation of host cell function by Legionella pneumophila type IV effectors. Annu. Rev. Cell Dev. Biol. 26 (2010), 261–283.
27. Husnjak, K., Dikic, I., Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 81 (2012), 291–322.
28. Jeong, K.C., Sexton, J.A., Vogel, J.P., Spatiotemporal regulation of a Legionella pneumophila T4SS substrate by the metaeffector SidJ. PLoS Pathog., 11, 2015, e1004695.
29. Kabsch, W., XDS. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 125–132.
30. Kazlauskaite, A., Kondapalli, C., Gourlay, R., Campbell, D.G., Ritorto, M.S., Hofmann, K., Alessi, D.R., Knebel, A., Trost, M., Muqit, M.M.K., Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem. J. 460 (2014), 127–139.
31. Kim, W., Kaelin, W.G. Jr., The von Hippel-Lindau tumor suppressor protein: new insights into oxygen sensing and cancer. Curr. Opin. Genet. Dev. 13 (2003), 55–60.
32. Kubori, T., Hyakutake, A., Nagai, H., Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol. Microbiol. 67 (2008), 1307–1319.
33. Lee, I., Schindelin, H., Structural insights into E1-catalyzed ubiquitin activation and transfer to conjugating enzymes. Cell 134 (2008), 268–278.
34. Leidecker, O., Bonfiglio, J.J., Colby, T., Zhang, Q., Atanassov, I., Zaja, R., Palazzo, L., Stockum, A., Ahel, I., Matic, I., Serine is a new target residue for endogenous ADP-ribosylation on histones. Nat. Chem. Biol., 2016, 10.1038/nchembio.2180 Published online October 10, 2016.
35. Llosa, M., Roy, C., Dehio, C., Bacterial type IV secretion systems in human disease. Mol. Microbiol. 73 (2009), 141–151.
36. Maculins, T., Fiskin, E., Bhogaraju, S., Dikic, I., Bacteria-host relationship: ubiquitin ligases as weapons of invasion. Cell Res. 26 (2016), 499–510.
37. Matic, I., Ahel, I., Hay, R.T., Reanalysis of phosphoproteomics data uncovers ADP-ribosylation sites. Nat. Methods 9 (2012), 771–772.
38. Narendra, D., Tanaka, A., Suen, D.-F., Youle, R.J., Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183 (2008), 795–803.
39. Newton, K., Dixit, V.M., Signaling in innate immunity and inflammation. Cold Spring Harb. Perspect. Biol., 4, 2012 a006049–a006049.
40. Ordureau, A., Sarraf, S.A., Duda, D.M., Heo, J.-M., Jedrychowski, M.P., Sviderskiy, V.O., Olszewski, J.L., Koerber, J.T., Xie, T., Beausoleil, S.A., et al. Quantitative proteomics reveal a feedforward mechanism for mitochondrial PARKIN translocation and ubiquitin chain synthesis. Mol. Cell 56 (2014), 360–375.
41. Palazzo, L., Thomas, B., Jemth, A.-S., Colby, T., Leidecker, O., Feijs, K.L.H., Zaja, R., Loseva, O., Puigvert, J.C., Matic, I., et al. Processing of protein ADP-ribosylation by Nudix hydrolases. Biochem. J. 468 (2015), 293–301.
42. Palazzo, L., Daniels, C.M., Nettleship, J.E., Rahman, N., McPherson, R.L., Ong, S.-E., Kato, K., Nureki, O., Leung, A.K.L., Ahel, I., ENPP1 processes protein ADP-ribosylation in vitro. FEBS J. 283 (2016), 3371–3388.
43. Price, C.T.D., Al-Quadan, T., Santic, M., Rosenshine, I., Abu Kwaik, Y., Host proteasomal degradation generates amino acids essential for intracellular bacterial growth. Science 334 (2011), 1553–1557.
44. Pu, Y., Zhao, Z., Li, Y., Zou, J., Ma, Q., Zhao, Y., Ke, Y., Zhu, Y., Chen, H., Baker, M.A.B., et al. Enhanced efflux activity facilitates drug tolerance in dormant bacterial cells. Mol. Cell 62 (2016), 284–294.
45. Qiu, J., Sheedlo, M.J., Yu, K., Tan, Y., Nakayasu, E.S., Das, C., Liu, X., Luo, Z.-Q., Ubiquitination independent of E1 and E2 enzymes by bacterial effectors. Nature 533 (2016), 120–124.
46. Ribet, D., Cossart, P., How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect. 17 (2015), 173–183.
47. Richter, B., Sliter, D.A., Herhaus, L., Stolz, A., Wang, C., Beli, P., Zaffagnini, G., Wild, P., Martens, S., Wagner, S.A., et al. Phosphorylation of OPTN by TBK1 enhances its binding to Ub chains and promotes selective autophagy of damaged mitochondria. Proc. Natl. Acad. Sci. USA 113 (2016), 4039–4044.
48. Rinaldo, S., Paiardini, A., Stelitano, V., Brunotti, P., Cervoni, L., Fernicola, S., Protano, C., Vitali, M., Cutruzzolà, F., Giardina, G., Structural basis of functional diversification of the HD-GYP domain revealed by the Pseudomonas aeruginosa PA4781 protein, which displays an unselective bimetallic binding site. J. Bacteriol. 197 (2015), 1525–1535.
49. Rogov, V., Dötsch, V., Johansen, T., Kirkin, V., Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol. Cell 53 (2014), 167–178.
50. Saha, A., Lewis, S., Kleiger, G., Kuhlman, B., Deshaies, R.J., Essential role for ubiquitin-ubiquitin-conjugating enzyme interaction in ubiquitin discharge from Cdc34 to substrate. Mol. Cell 42 (2011), 75–83.
51. Sansonetti, P.J., The bacterial weaponry: lessons from Shigella. Ann. N Y Acad. Sci. 1072 (2006), 307–312.
52. Sheedlo, M.J., Qiu, J., Tan, Y., Paul, L.N., Luo, Z.-Q., Das, C., Structural basis of substrate recognition by a bacterial deubiquitinase important for dynamics of phagosome ubiquitination. Proc. Natl. Acad. Sci. USA 112 (2015), 15090–15095.
53. Söding, J., Biegert, A., Lupas, A.N., The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33 (2005), W244–W248.
54. Storoni, L.C., McCoy, A.J., Read, R.J., Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60 (2004), 432–438.
55. Ulrich, H.D., Walden, H., Ubiquitin signalling in DNA replication and repair. Nat. Rev. Mol. Cell Biol. 11 (2010), 479–489.
56. Vittal, V., Stewart, M.D., Brzovic, P.S., Klevit, R.E., Regulating the regulators: recent revelations in the control of E3 ubiquitin ligases. J. Biol. Chem. 290 (2015), 21244–21251.
57. Vizcaíno, J.A., Csordas, A., Del-Toro, N., Dianes, J.A., Griss, J., Lavidas, I., Mayer, G., Perez-Riverol, Y., Reisinger, F., Ternent, T., et al. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res., 2016 Published online September 28, 2016. gkw880.
58. Wang, X., Herr, R.A., Hansen, T.H., Ubiquitination of substrates by esterification. Traffic 13 (2012), 19–24.
59. Wenger, C.D., Coon, J.J., A proteomics search algorithm specifically designed for high-resolution tandem mass spectra. J. Proteome Res. 12 (2013), 1377–1386.
60. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G.W., McCoy, A., et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. Sect. D Biol. Crystallogr. 67 (2011), 235–242.
61. Wiśniewski, J.R., Zougman, A., Nagaraj, N., Mann, M., Universal sample preparation method for proteome analysis. Nat. Methods 6 (2009), 359–362.
62. Wong, K., Kozlov, G., Zhang, Y., Gehring, K., Structure of the Legionella effector, lpg1496, suggests a role in nucleotide metabolism. J. Biol. Chem. 290 (2015), 24727–24737.
63. Xu, L., Luo, Z.-Q., Cell biology of infection by Legionella pneumophila. Microbes Infect. 15 (2013), 157–167.
64. Yau, R., Rape, M., The increasing complexity of the ubiquitin code. Nat. Cell Biol. 18 (2016), 579–586.