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Structural basis for the recognition and degradation of host TRIM proteins by Salmonella effector SopA.

Fiskin E, Bhogaraju S, Herhaus L, Kalayil S, Hahn M, Dikic I
Nat Commun 8 14004 (2017)
Cited: 33 times
EuropePMC logo PMID: 28084320

Abstract

The hallmark of Salmonella Typhimurium infection is an acute intestinal inflammatory response, which is mediated through the action of secreted bacterial effector proteins. The pro-inflammatory Salmonella effector SopA is a HECT-like E3 ligase, which was previously proposed to activate host RING ligases TRIM56 and TRIM65. Here we elucidate an inhibitory mechanism of TRIM56 and TRIM65 targeting by SopA. We present the crystal structure of SopA in complex with the RING domain of human TRIM56, revealing the atomic details of their interaction and the basis for SopA selectivity towards TRIM56 and TRIM65. Structure-guided biochemical analysis shows that SopA inhibits TRIM56 E3 ligase activity by occluding the E2-interacting surface of TRIM56. We further demonstrate that SopA ubiquitinates TRIM56 and TRIM65, resulting in their proteasomal degradation during infection. Our results provide the basis for how a bacterial HECT ligase blocks host RING ligases and exemplifies the multivalent power of bacterial effectors during infection.

Reviews - 5jw7 mentioned but not cited (1)

  1. Does it take two to tango? RING domain self-association and activity in TRIM E3 ubiquitin ligases. Fiorentini F, Esposito D, Rittinger K. Biochem Soc Trans 48 2615-2624 (2020)

Articles - 5jw7 mentioned but not cited (2)

  1. Structural basis for the recognition and degradation of host TRIM proteins by Salmonella effector SopA. Fiskin E, Bhogaraju S, Herhaus L, Kalayil S, Hahn M, Dikic I. Nat Commun 8 14004 (2017)
  2. A Ubiquitin-Binding Domain that Binds a Structural Fold Distinct from that of Ubiquitin. Lim M, Newman JA, Williams HL, Masino L, Aitkenhead H, Gravard AE, Gileadi O, Svejstrup JQ. Structure 27 1316-1325.e6 (2019)


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  1. Selective Autophagy and Xenophagy in Infection and Disease. Sharma V, Verma S, Seranova E, Sarkar S, Kumar D. Front Cell Dev Biol 6 147 (2018)
  2. Salmonella Pathogenicity Island 1 (SPI-1) and Its Complex Regulatory Network. Lou L, Zhang P, Piao R, Wang Y. Front Cell Infect Microbiol 9 270 (2019)
  3. Salmonella Typhimurium and inflammation: a pathogen-centric affair. Galán JE. Nat Rev Microbiol 19 716-725 (2021)
  4. Autophagy and Ubiquitination in Salmonella Infection and the Related Inflammatory Responses. Wang L, Yan J, Niu H, Huang R, Wu S. Front Cell Infect Microbiol 8 78 (2018)
  5. The ubiquitin ligation machinery in the defense against bacterial pathogens. Tripathi-Giesgen I, Behrends C, Alpi AF. EMBO Rep 22 e52864 (2021)
  6. Camouflage and interception: how pathogens evade detection by intracellular nucleic acid sensors. Unterholzner L, Almine JF. Immunology 156 217-227 (2019)
  7. Revisiting Bacterial Ubiquitin Ligase Effectors: Weapons for Host Exploitation. Pisano A, Albano F, Vecchio E, Renna M, Scala G, Quinto I, Fiume G. Int J Mol Sci 19 E3576 (2018)
  8. Insights from protein-protein interaction studies on bacterial pathogenesis. Gagarinova A, Phanse S, Cygler M, Babu M. Expert Rev Proteomics 14 779-797 (2017)
  9. Interesting Biochemistries in the Structure and Function of Bacterial Effectors. Mak H, Thurston TLM. Front Cell Infect Microbiol 11 608860 (2021)
  10. Modification of the host ubiquitome by bacterial enzymes. Berglund J, Gjondrekaj R, Verney E, Maupin-Furlow JA, Edelmann MJ. Microbiol Res 235 126429 (2020)
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  12. Current Understanding of the Structure and Function of Pentapeptide Repeat Proteins. Zhang R, Kennedy MA. Biomolecules 11 638 (2021)
  13. Keeping in Touch with Type-III Secretion System Effectors: Mass Spectrometry-Based Proteomics to Study Effector-Host Protein-Protein Interactions. Meyer M, Ryck J, Goormachtig S, Van Damme P. Int J Mol Sci 21 E6891 (2020)
  14. Contributions of Mass Spectrometry-Based Proteomics to Understanding Salmonella-Host Interactions. Zhang B, Liu B, Zhou Y, Zhang X, Zou Q, Liu X. Pathogens 9 E581 (2020)
  15. The Functions of TRIM56 in Antiviral Innate Immunity and Tumorigenesis. Fu L, Zhou X, Jiao Q, Chen X. Int J Mol Sci 24 5046 (2023)
  16. Speaking the host language: how Salmonella effector proteins manipulate the host. Pillay TD, Hettiarachchi SU, Gan J, Diaz-Del-Olmo I, Yu XJ, Muench JH, Thurston TLM, Pearson JS. Microbiology (Reading) 169 (2023)
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  1. TRIM14 Is a Key Regulator of the Type I IFN Response during Mycobacterium tuberculosis Infection. Hoffpauir CT, Bell SL, West KO, Jing T, Wagner AR, Torres-Odio S, Cox JS, West AP, Li P, Patrick KL, Watson RO. J Immunol 205 153-167 (2020)
  2. Bacterial OTU deubiquitinases regulate substrate ubiquitination upon Legionella infection. Shin D, Bhattacharya A, Cheng YL, Alonso MC, Mehdipour AR, van der Heden van Noort GJ, Ovaa H, Hummer G, Dikic I. Elife 9 e58277 (2020)
  3. TRIM21 Is Targeted for Chaperone-Mediated Autophagy during Salmonella Typhimurium Infection. Hos NJ, Fischer J, Hos D, Hejazi Z, Calabrese C, Ganesan R, Murthy AMV, Rybniker J, Kumar S, Krönke M, Robinson N. J Immunol 205 2456-2467 (2020)
  4. SIK2 orchestrates actin-dependent host response upon Salmonella infection. Hahn M, Covarrubias-Pinto A, Herhaus L, Satpathy S, Klann K, Boyle KB, Münch C, Rajalingam K, Randow F, Choudhary C, Dikic I. Proc Natl Acad Sci U S A 118 e2024144118 (2021)
  5. Toxoplasma gondii Type-I ROP18 Targeting Human E3 Ligase TRIM21 for Immune Escape. Yao L, Xu L, Zhou L, Wu S, Zou W, Chen M, Chen J, Peng H. Front Cell Dev Biol 9 685913 (2021)
  6. Mechanistic insights into the subversion of the linear ubiquitin chain assembly complex by the E3 ligase IpaH1.4 of Shigella flexneri. Liu J, Wang Y, Wang D, Wang Y, Xu X, Zhang Y, Li Y, Zhang M, Gong X, Tang Y, Shen L, Li M, Pan L. Proc Natl Acad Sci U S A 119 e2116776119 (2022)
  7. Structural insights into ubiquitin chain cleavage by Legionella ovarian tumor deubiquitinases. Kang S, Kim G, Choi M, Jeong M, van der Heden van Noort GJ, Roh SH, Shin D. Life Sci Alliance 6 e202201876 (2023)
  8. TRIM56 Reduces Radiosensitization of Human Glioblastoma by Regulating FOXM1-Mediated DNA Repair. Dong Y, Xiong Y, Zhou D, Yao M, Wang X, Bi W, Zhang J. Mol Neurobiol 59 5312-5325 (2022)
  9. The UAS thioredoxin-like domain of UBXN7 regulates E3 ubiquitin ligase activity of RNF111/Arkadia. Amhaz S, Boëda B, Chouchène M, Colasse S, Dingli F, Loew D, Henri J, Prunier C, Levy L. BMC Biol 21 73 (2023)
  10. Salmonella invasion of a cell is self-limiting due to effector-driven activation of N-WASP. Davidson A, Hume PJ, Greene NP, Koronakis V. iScience 26 106643 (2023)
  11. TRIM56 coiled-coil domain structure provides insights into its E3 ligase functions. Lou X, Ma B, Zhuang Y, Xiao X, Minze LJ, Xing J, Zhang Z, Li XC. Comput Struct Biotechnol J 21 2801-2808 (2023)


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