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Solution NMR structure of the NlpC/P60 domain of lipoprotein Spr from Escherichia coli: structural evidence for a novel cysteine peptidase catalytic triad.

Aramini JM, Rossi P, Huang YJ, Zhao L, Jiang M, Maglaqui M, Xiao R, Locke J, Nair R, Rost B, Acton TB, Inouye M, Montelione GT
Biochemistry 47 9715-7 (2008)
Cited: 55 times
EuropePMC logo PMID: 18715016

Abstract

Escherichia coli Spr is a membrane-anchored cell wall hydrolase. The solution NMR structure of the C-terminal NlpC/P60 domain of E. coli Spr described here reveals that the protein adopts a papain-like alpha+beta fold and identifies a substrate-binding cleft featuring several highly conserved residues. The active site features a novel Cys-His-His catalytic triad that appears to be a unique structural signature of this cysteine peptidase family. Moreover, the relative orientation of these catalytic residues is similar to that observed in the analogous Ser-His-His triad, a variant of the classic Ser-His-Asp charge relay system, suggesting the convergent evolution of a catalytic mechanism in quite distinct peptidase families.

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  1. Structure of a peptidoglycan amidase effector targeted to Gram-negative bacteria by the type VI secretion system. Chou S, Bui NK, Russell AB, Lexa KW, Gardiner TE, LeRoux M, Vollmer W, Mougous JD. Cell Rep 1 656-664 (2012)
  2. Structural basis of murein peptide specificity of a gamma-D-glutamyl-l-diamino acid endopeptidase. Xu Q, Sudek S, McMullan D, Miller MD, Geierstanger B, Jones DH, Krishna SS, Spraggon G, Bursalay B, Abdubek P, Acosta C, Ambing E, Astakhova T, Axelrod HL, Carlton D, Caruthers J, Chiu HJ, Clayton T, Deller MC, Duan L, Elias Y, Elsliger MA, Feuerhelm J, Grzechnik SK, Hale J, Han GW, Haugen J, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kozbial P, Kumar A, Marciano D, Morse AT, Nigoghossian E, Okach L, Oommachen S, Paulsen J, Reyes R, Rife CL, Trout CV, van den Bedem H, Weekes D, White A, Wolf G, Zubieta C, Hodgson KO, Wooley J, Deacon AM, Godzik A, Lesley SA, Wilson IA. Structure 17 303-313 (2009)
  3. Structural insights into the Pseudomonas aeruginosa type VI virulence effector Tse1 bacteriolysis and self-protection mechanisms. Ding J, Wang W, Feng H, Zhang Y, Wang DC. J. Biol. Chem. 287 26911-26920 (2012)
  4. Structural insights into the effector-immunity system Tse1/Tsi1 from Pseudomonas aeruginosa. Benz J, Sendlmeier C, Barends TR, Meinhart A. PLoS ONE 7 e40453 (2012)
  5. Structural elucidation of the Cys-His-Glu-Asn proteolytic relay in the secreted CHAP domain enzyme from the human pathogen Staphylococcus saprophyticus. Rossi P, Aramini JM, Xiao R, Chen CX, Nwosu C, Owens LA, Maglaqui M, Nair R, Fischer M, Acton TB, Honig B, Rost B, Montelione GT. Proteins 74 515-519 (2009)
  6. DisMeta: a meta server for construct design and optimization. Huang YJ, Acton TB, Montelione GT. Methods Mol. Biol. 1091 3-16 (2014)
  7. Crystal structure of an uncommon cellulosome-related protein module from Ruminococcus flavefaciens that resembles papain-like cysteine peptidases. Levy-Assaraf M, Voronov-Goldman M, Rozman Grinberg I, Weiserman G, Shimon LJ, Jindou S, Borovok I, White BA, Bayer EA, Lamed R, Frolow F. PLoS ONE 8 e56138 (2013)
  8. Solution structure of IseA, an inhibitor protein of DL-endopeptidases from Bacillus subtilis, reveals a novel fold with a characteristic inhibitory loop. Arai R, Fukui S, Kobayashi N, Sekiguchi J. J. Biol. Chem. 287 44736-44748 (2012)
  9. Novel Target Exploration from Hypothetical Proteins of Klebsiella pneumoniae MGH 78578 Reveals a Protein Involved in Host-Pathogen Interaction. Pranavathiyani G, Prava J, Rajeev AC, Pan A. Front Cell Infect Microbiol 10 109 (2020)
  10. Structural basis of adaptor-mediated protein degradation by the tail-specific PDZ-protease Prc. Su MY, Som N, Wu CY, Su SC, Kuo YT, Ke LC, Ho MR, Tzeng SR, Teng CH, Mengin-Lecreulx D, Reddy M, Chang CI. Nat Commun 8 1516 (2017)
  11. Identification and classification of papain-like cysteine proteinases. Ozhelvaci F, Steczkiewicz K. J Biol Chem 299 104801 (2023)
  12. Enterococcus faecium secreted antigen A generates muropeptides to enhance host immunity and limit bacterial pathogenesis. Kim B, Wang YC, Hespen CW, Espinosa J, Salje J, Rangan KJ, Oren DA, Kang JY, Pedicord VA, Hang HC. Elife 8 (2019)


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  1. Bacterial cell division regulation by Ser/Thr kinases: a structural perspective. Ruggiero A, De Simone P, Smaldone G, Squeglia F, Berisio R. Curr. Protein Pept. Sci. 13 756-766 (2012)
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  3. Peptidoglycan NlpC/P60 peptidases in bacterial physiology and host interactions. Griffin ME, Klupt S, Espinosa J, Hang HC. Cell Chem Biol 30 436-456 (2023)
  4. The Cell Wall Hydrolytic NlpC/P60 Endopeptidases in Mycobacterial Cytokinesis: A Structural Perspective. Squeglia F, Moreira M, Ruggiero A, Berisio R. Cells 8 (2019)

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  1. Three redundant murein endopeptidases catalyse an essential cleavage step in peptidoglycan synthesis of Escherichia coli K12. Singh SK, SaiSree L, Amrutha RN, Reddy M. Mol. Microbiol. 86 1036-1051 (2012)
  2. Structure and functional regulation of RipA, a mycobacterial enzyme essential for daughter cell separation. Ruggiero A, Marasco D, Squeglia F, Soldini S, Pedone E, Pedone C, Berisio R. Structure 18 1184-1190 (2010)
  3. Synthetic lethality of the lytE cwlO genotype in Bacillus subtilis is caused by lack of D,L-endopeptidase activity at the lateral cell wall. Hashimoto M, Ooiwa S, Sekiguchi J. J. Bacteriol. 194 796-803 (2012)
  4. Structure of the type VI effector-immunity complex (Tae4-Tai4) provides novel insights into the inhibition mechanism of the effector by its immunity protein. Zhang H, Zhang H, Gao ZQ, Wang WJ, Liu GF, Xu JH, Su XD, Dong YH. J. Biol. Chem. 288 5928-5939 (2013)
  5. Structural basis for the acyltransferase activity of lecithin:retinol acyltransferase-like proteins. Golczak M, Kiser PD, Sears AE, Lodowski DT, Blaner WS, Palczewski K. J. Biol. Chem. 287 23790-23807 (2012)
  6. Bacterial growth does require peptidoglycan hydrolases. Vollmer W. Mol. Microbiol. 86 1031-1035 (2012)
  7. Structure of the γ-D-glutamyl-L-diamino acid endopeptidase YkfC from Bacillus cereus in complex with L-Ala-γ-D-Glu: insights into substrate recognition by NlpC/P60 cysteine peptidases. Xu Q, Abdubek P, Astakhova T, Axelrod HL, Bakolitsa C, Cai X, Carlton D, Chen C, Chiu HJ, Chiu M, Clayton T, Das D, Deller MC, Duan L, Ellrott K, Farr CL, Feuerhelm J, Grant JC, Grzechnik A, Han GW, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kozbial P, Krishna SS, Kumar A, Lam WW, Marciano D, Miller MD, Morse AT, Nigoghossian E, Nopakun A, Okach L, Puckett C, Reyes R, Tien HJ, Trame CB, van den Bedem H, Weekes D, Wooten T, Yeh A, Hodgson KO, Wooley J, Elsliger MA, Deacon AM, Godzik A, Lesley SA, Wilson IA. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66 1354-1364 (2010)
  8. One for all or all for one: heterogeneous expression and host cell lysis are key to gene transfer agent activity in Rhodobacter capsulatus. Fogg PC, Westbye AB, Beatty JT. PLoS ONE 7 e43772 (2012)
  9. The phylogeny of Sodalis-like symbionts as reconstructed using surface-encoding loci. Snyder AK, McMillen CM, Wallenhorst P, Rio RV. FEMS Microbiol. Lett. 317 143-151 (2011)
  10. Structure/function relationships of adipose phospholipase A2 containing a cys-his-his catalytic triad. Pang XY, Cao J, Addington L, Lovell S, Battaile KP, Zhang N, Rao JL, Dennis EA, Moise AR. J. Biol. Chem. 287 35260-35274 (2012)
  11. NlpI-mediated modulation of outer membrane vesicle production through peptidoglycan dynamics in Escherichia coli. Schwechheimer C, Rodriguez DL, Kuehn MJ. Microbiologyopen 4 375-389 (2015)
  12. Crystal structure of the lytic CHAP(K) domain of the endolysin LysK from Staphylococcus aureus bacteriophage K. Sanz-Gaitero M, Keary R, Garcia-Doval C, Coffey A, van Raaij MJ. Virol. J. 11 133 (2014)
  13. Solution structure of the N-terminal catalytic domain of human H-REV107--a novel circular permutated NlpC/P60 domain. Ren X, Lin J, Jin C, Xia B. FEBS Lett. 584 4222-4226 (2010)
  14. Comparative genome analysis of Enterobacter cloacae. Liu WY, Wong CF, Chung KM, Jiang JW, Leung FC. PLoS ONE 8 e74487 (2013)
  15. Structural insights into the inhibition of type VI effector Tae3 by its immunity protein Tai3. Dong C, Zhang H, Gao ZQ, Wang WJ, She Z, Liu GF, Shen YQ, Su XD, Dong YH. Biochem. J. 454 59-68 (2013)
  16. Crystal structure of type VI effector Tse1 from Pseudomonas aeruginosa. Zhang H, Gao ZQ, Su XD, Dong YH. FEBS Lett. 586 3193-3199 (2012)
  17. Structures of a bifunctional cell wall hydrolase CwlT containing a novel bacterial lysozyme and an NlpC/P60 DL-endopeptidase. Xu Q, Chiu HJ, Farr CL, Jaroszewski L, Knuth MW, Miller MD, Lesley SA, Godzik A, Elsliger MA, Deacon AM, Wilson IA. J. Mol. Biol. 426 169-184 (2014)
  18. Structural analysis of papain-like NlpC/P60 superfamily enzymes with a circularly permuted topology reveals potential lipid binding sites. Xu Q, Rawlings ND, Chiu HJ, Jaroszewski L, Klock HE, Knuth MW, Miller MD, Elsliger MA, Deacon AM, Godzik A, Lesley SA, Wilson IA. PLoS ONE 6 e22013 (2011)
  19. Insights into Substrate Specificity of NlpC/P60 Cell Wall Hydrolases Containing Bacterial SH3 Domains. Xu Q, Mengin-Lecreulx D, Liu XW, Patin D, Farr CL, Grant JC, Chiu HJ, Jaroszewski L, Knuth MW, Godzik A, Lesley SA, Elsliger MA, Deacon AM, Wilson IA. MBio 6 e02327-14 (2015)
  20. Structural and functional studies of gpX of Escherichia coli phage P2 reveal a widespread role for LysM domains in the baseplates of contractile-tailed phages. Maxwell KL, Fatehi Hassanabad M, Chang T, Paul VD, Pirani N, Bona D, Edwards AM, Davidson AR. J. Bacteriol. 195 5461-5468 (2013)
  21. MAP1272c encodes an NlpC/P60 protein, an antigen detected in cattle with Johne's disease. Bannantine JP, Lingle CK, Stabel JR, Ramyar KX, Garcia BL, Raeber AJ, Schacher P, Kapur V, Geisbrecht BV. Clin. Vaccine Immunol. 19 1083-1092 (2012)
  22. RipD (Rv1566c) from Mycobacterium tuberculosis: adaptation of an NlpC/p60 domain to a non-catalytic peptidoglycan-binding function. Böth D, Steiner EM, Izumi A, Schneider G, Schnell R. Biochem. J. 457 33-41 (2014)
  23. Salinity-dependent impacts of ProQ, Prc, and Spr deficiencies on Escherichia coli cell structure. Kerr CH, Culham DE, Marom D, Wood JM. J. Bacteriol. 196 1286-1296 (2014)
  24. Mapping inhibitor binding modes on an active cysteine protease via nuclear magnetic resonance spectroscopy. Lee GM, Balouch E, Goetz DH, Lazic A, McKerrow JH, Craik CS. Biochemistry 51 10087-10098 (2012)
  25. NlpC/P60 domain-containing proteins of Mycobacterium avium subspecies paratuberculosis that differentially bind and hydrolyze peptidoglycan. Bannantine JP, Lingle CK, Adam PR, Ramyar KX, McWhorter WJ, Stabel JR, Picking WD, Geisbrecht BV. Protein Sci. 25 840-851 (2016)
  26. Transcriptomic analysis of human norovirus NS1-2 protein highlights a multifunctional role in murine monocytes. Lateef Z, Gimenez G, Baker ES, Ward VK. BMC Genomics 18 39 (2017)
  27. House dust mites possess a polymorphic, single domain putative peptidoglycan d,l endopeptidase belonging to the NlpC/P60 Superfamily. Tang VH, Stewart GA, Chang BJ. FEBS Open Bio 5 813-823 (2015)
  28. In Silico Characterization of a Hypothetical Protein from Shigella dysenteriae ATCC 12039 Reveals a Pathogenesis-Related Protein of the Type-VI Secretion System. Rabbi MF, Akter SA, Hasan MJ, Amin A. Bioinform Biol Insights 15 11779322211011140 (2021)
  29. Integration of host strain bioengineering and bioprocess development using ultra-scale down studies to select the optimum combination: an antibody fragment primary recovery case study. Aucamp JP, Davies R, Hallet D, Weiss A, Titchener-Hooker NJ. Biotechnol. Bioeng. 111 1971-1981 (2014)
  30. The 100-protein NMR spectra dataset: A resource for biomolecular NMR data analysis. Klukowski P, Damberger FF, Allain FH, Iwai H, Kadavath H, Ramelot TA, Montelione GT, Riek R, Güntert P. Sci Data 11 30 (2024)
  31. Enterococcus NlpC/p60 Peptidoglycan Hydrolase SagA Localizes to Sites of Cell Division and Requires Only a Catalytic Dyad for Protease Activity. Espinosa J, Lin TY, Estrella Y, Kim B, Molina H, Hang HC. Biochemistry 59 4470-4480 (2020)
  32. A Secreted NlpC/P60 Endopeptidase from Photobacterium damselae subsp. piscicida Cleaves the Peptidoglycan of Potentially Competing Bacteria. Lisboa J, Pereira C, Rifflet A, Ayala J, Terceti MS, Barca AV, Rodrigues I, Pereira PJB, Osorio CR, García-Del Portillo F, Gomperts Boneca I, do Vale A, Dos Santos NMS. mSphere 6 (2021)
  33. Chemical shift transfer: an effective strategy for protein NMR assignment with ARTINA. Wetton H, Klukowski P, Riek R, Güntert P. Front Mol Biosci 10 1244029 (2023)
  34. Cloning, expression, purification, crystallization and preliminary crystallographic analysis of the putative NlpC/P60 endopeptidase, TTHA0266, from Thermus thermophilus HB8. Wong JE, Blaise M. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 69 1291-1294 (2013)
  35. Development of a high yielding E. coli periplasmic expression system for the production of humanized Fab' fragments. Ellis M, Patel P, Edon M, Ramage W, Dickinson R, Humphreys DP. Biotechnol. Prog. 33 212-220 (2017)
  36. Muramyl Endopeptidase Spr Contributes to Intrinsic Vancomycin Resistance in Salmonella enterica Serovar Typhimurium. Vestö K, Huseby DL, Snygg I, Wang H, Hughes D, Rhen M. Front Microbiol 9 2941 (2018)
  37. P40 and P75 Are Singular Functional Muramidases Present in the Lactobacillus casei /paracasei/rhamnosus Taxon. Bäuerl C, Abitayeva G, Sosa-Carrillo S, Mencher-Beltrán A, Navarro-Lleó N, Coll-Marqués JM, Zúñiga-Cabrera M, Shaikhin S, Pérez-Martinez G. Front Microbiol 10 1420 (2019)
  38. Solution scattering study of the Bacillus subtilis PgdS enzyme involved in poly-γ-glutamic acids degradation. Zeng J, Jin Y, Liu Z. PLoS ONE 13 e0195355 (2018)
  39. The role of the bacterial protease Prc in the uropathogenesis of extraintestinal pathogenic Escherichia coli. Huang WC, Lin CY, Hashimoto M, Wu JJ, Wang MC, Lin WH, Chen CS, Teng CH. J. Biomed. Sci. 27 14 (2020)


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