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The crystal structure Escherichia coli Spy.

Kwon E, Kim DY, Gross CA, Gross JD, Kim KK
Protein Sci 19 2252-9 (2010)
Cited: 29 times
EuropePMC logo PMID: 20799348

Abstract

Escherichia coli spheroplast protein y (EcSpy) is a small periplasmic protein that is homologous with CpxP, an inhibitor of the extracytoplasmic stress response. Stress conditions such as spheroplast formation induce the expression of Spy via the Cpx or the Bae two-component systems in E. coli, though the function of Spy is unknown. Here, we report the crystal structure of EcSpy, which reveals a long kinked hairpin-like structure of four α-helices that form an antiparallel dimer. The dimer contains a curved oval shape with a highly positively charged concave surface that may function as a ligand binding site. Sequence analysis reveals that Spy is highly conserved over the Enterobacteriaceae family. Notably, three conserved regions that contain identical residues and two LTxxQ motifs are placed at the horizontal end of the dimer structure, stabilizing the overall fold. CpxP also contains the conserved sequence motifs and has a predicted secondary structure similar to Spy, suggesting that Spy and CpxP likely share the same fold.

Reviews - 3oeo mentioned but not cited (2)

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Articles - 3oeo mentioned but not cited (6)

  1. The crystal structure Escherichia coli Spy. Kwon E, Kim DY, Gross CA, Gross JD, Kim KK. Protein Sci. 19 2252-2259 (2010)
  2. Structure of the periplasmic stress response protein CpxP. Thede GL, Arthur DC, Edwards RA, Buelow DR, Wong JL, Raivio TL, Glover JN. J. Bacteriol. 193 2149-2157 (2011)
  3. Visualizing chaperone-assisted protein folding. Horowitz S, Salmon L, Koldewey P, Ahlstrom LS, Martin R, Quan S, Afonine PV, van den Bedem H, Wang L, Xu Q, Trievel RC, Brooks CL, Bardwell JC. Nat. Struct. Mol. Biol. 23 691-697 (2016)
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  5. Eco-friendly synthesis, physicochemical studies, biological assay and molecular docking of steroidal oxime-ethers. Alam M, Lee DU. EXCLI J 14 394-407 (2015)
  6. Structural investigation on SPI-6-associated Salmonella typhimurium VirG-like stress protein that promotes pathogen survival in macrophages. Ray S, Pandey NK, Kushwaha GS, Das S, Ganguly AK, Vashi N, Kumar D, Suar M, Bhavesh NS. Protein Sci 31 835-849 (2022)


Reviews citing this publication (6)

  1. Just scratching the surface: an expanding view of the Cpx envelope stress response. Vogt SL, Raivio TL. FEMS Microbiol. Lett. 326 2-11 (2012)
  2. Folding mechanisms of periplasmic proteins. Goemans C, Denoncin K, Collet JF. Biochim. Biophys. Acta 1843 1517-1528 (2014)
  3. Engineering and Evolution of Molecular Chaperones and Protein Disaggregases with Enhanced Activity. Mack KL, Shorter J. Front Mol Biosci 3 8 (2016)
  4. Stress-Responsive Periplasmic Chaperones in Bacteria. Kim H, Wu K, Lee C. Front Mol Biosci 8 678697 (2021)
  5. Maintaining Integrity Under Stress: Envelope Stress Response Regulation of Pathogenesis in Gram-Negative Bacteria. Hews CL, Cho T, Rowley G, Raivio TL. Front Cell Infect Microbiol 9 313 (2019)
  6. Redefining Molecular Chaperones as Chaotropes. Macošek J, Mas G, Hiller S. Front Mol Biosci 8 683132 (2021)

Articles citing this publication (15)

  1. Reduction of cellular stress by TolC-dependent efflux pumps in Escherichia coli indicated by BaeSR and CpxARP activation of spy in efflux mutants. Rosner JL, Martin RG. J. Bacteriol. 195 1042-1050 (2013)
  2. Structural basis for two-component system inhibition and pilus sensing by the auxiliary CpxP protein. Zhou X, Keller R, Volkmer R, Krauss N, Scheerer P, Hunke S. J. Biol. Chem. 286 9805-9814 (2011)
  3. The Cpx stress response system potentiates the fitness and virulence of uropathogenic Escherichia coli. Debnath I, Norton JP, Barber AE, Ott EM, Dhakal BK, Kulesus RR, Mulvey MA. Infect. Immun. 81 1450-1459 (2013)
  4. The BaeSR regulon is involved in defense against zinc toxicity in E. coli. Wang D, Fierke CA. Metallomics 5 372-383 (2013)
  5. Super Spy variants implicate flexibility in chaperone action. Quan S, Wang L, Petrotchenko EV, Makepeace KA, Horowitz S, Yang J, Zhang Y, Borchers CH, Bardwell JC. Elife 3 e01584 (2014)
  6. ZraP is a periplasmic molecular chaperone and a repressor of the zinc-responsive two-component regulator ZraSR. Appia-Ayme C, Hall A, Patrick E, Rajadurai S, Clarke TA, Rowley G. Biochem. J. 442 85-93 (2012)
  7. Sublethal concentrations of carbapenems alter cell morphology and genomic expression of Klebsiella pneumoniae biofilms. Van Laar TA, Chen T, You T, Leung KP. Antimicrob. Agents Chemother. 59 1707-1717 (2015)
  8. A molecular mechanism of chaperone-client recognition. He L, Sharpe T, Mazur A, Hiller S. Sci Adv 2 e1601625 (2016)
  9. Genetic regulation of spy gene expression in Escherichia coli in the presence of protein unfolding agent ethanol. Srivastava SK, Lambadi PR, Ghosh T, Pathania R, Navani NK. Gene 548 142-148 (2014)
  10. Comparative genomics and transcriptomics analysis of experimentally evolved Escherichia coli MC1000 in complex environments. Puentes-Téllez PE, Kovács ÁT, Kuipers OP, van Elsas JD. Environ. Microbiol. 16 856-870 (2014)
  11. The crystal structure of the periplasmic domain of Vibrio parahaemolyticus CpxA. Kwon E, Kim DY, Ngo TD, Gross CA, Gross JD, Kim KK. Protein Sci. 21 1334-1343 (2012)
  12. The disinfection of impression materials by using microwave irradiation and hydrogen peroxide. Choi YR, Kim KN, Kim KM. J Prosthet Dent 112 981-987 (2014)
  13. Mechanistic insights into manganese oxidation of a soil-borne Mn(II)-oxidizing Escherichia coli strain by global proteomic and genetic analyses. Wang Z, Wang J, Liu J, Chen H, Li M, Li L. Sci Rep 7 1352 (2017)
  14. Common Patterns in Chaperone Interactions with a Native Client Protein. He L, Hiller S. Angew. Chem. Int. Ed. Engl. 57 5921-5924 (2018)
  15. Dynamic coupling of fast channel gating with slow ATP-turnover underpins protein transport through the Sec translocon. Crossley JA, Allen WJ, Watkins DW, Sabir T, Radford SE, Tuma R, Collinson I, Fessl T. EMBO J 43 1-13 (2024)


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