Carbohydrate recognition and lysis by bacterial peptidoglycan hydrolases

Current Opinion in Structural Biology

Volumn 44, Issue , 2017, Pages 87-100

  Alcorlo, Martín ^a   Martínez Caballero, Siseth ^a   Molina, Rafael ^a   Hermoso, Juan A ^a  

^a INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; BACTERIAL ENZYME; CARBOHYDRATE; CARBOXYPEPTIDASE; GLUCOSAMINIDASE; GLYCOSYLTRANSFERASE; HYDROLASE; LYSOZYME; PEPTIDOGLYCAN; PROTEINASE; N ACETYLMURAMOYLALANINE AMIDASE; PROTEIN BINDING;

BACTERIAL CELL WALL; BACTERIOLYSIS; BACTERIUM; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN DATABASE; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW; ANIMAL; CARBOHYDRATE METABOLISM; CHEMISTRY; ENZYMOLOGY; HUMAN; METABOLISM;

ANIMALS; BACTERIA; CARBOHYDRATE METABOLISM; DATABASES, PROTEIN; HUMANS; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; PROTEIN BINDING;

EID: 85009914900     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2017.01.001     Document Type: Review

References (79)

1. 1 Dramsi, S., Magnet, S., Davison, S., Arthur, M., Covalent attachment of proteins to peptidoglycan. FEMS Microbiol Rev 32 (2008), 307–320.
2. 2 Vollmer, W., Blanot, D., de Pedro, M.A., Peptidoglycan structure and architecture. FEMS Microbiol Rev 32 (2008), 149–167.
3. 3 Cava, F., de Pedro, M.A., Peptidoglycan plasticity in bacteria: emerging variability of the murein sacculus and their associated biological functions. Curr Opin Microbiol 18 (2014), 46–53.
4. 4 Sharma, A.K., Kumar, S., Harish, K., Dhakan, D.B., Sharma, V.K., Prediction of peptidoglycan hydrolases—a new class of antibacterial proteins. BMC Genom, 17, 2016, 411.
5. 5 van Heijenoort, J., Peptidoglycan hydrolases of Escherichia coli. Microbiol Mol Biol Rev 75 (2011), 636–663.
6. 6 Wyckoff, T.J., Taylor, J.A., Salama, N.R., Beyond growth: novel functions for bacterial cell wall hydrolases. Trends Microbiol 20 (2012), 540–547.
7. 7 Lee, T.K., Huang, K.C., The role of hydrolases in bacterial cell-wall growth. Curr Opin Microbiol 16 (2013), 760–766.
8. 8 Domínguez-Gil, T., Molina, R., Alcorlo, M., Hermoso, J.A., Renew or die: the molecular mechanisms of peptidoglycan recycling and antibiotics resistance in Gram-negative pathogens. Drug Resist Updates 28 (2016), 91–104, 10.1016/j.drup.2016.07.002.
9. 9 Wolf, A.J., Reyes, C.N., Liang, W., Becker, C., Shimada, K., Wheeler, M.L., Cho, H.C., Popescu, N.I., Coggeshall, K.M., Arditi, M., et al. Hexokinase is an innate immune receptor for the detection of bacterial peptidoglycan. Cell 166 (2016), 624–636, 10.1016/j.cell.2016.05.076.
10. 10 Holtje, J.V., Mirelman, D., Sharon, N., Schwarz, U., Novel type of murein transglycosylase in Escherichia coli. J Bacteriol 124 (1975), 1067–1076.
11. 11 Lee, M., Hesek, D., Llarrull, L.I., Lastochkin, E., Pi, H., Boggess, B., Mobashery, S., Reactions of all Escherichia coli lytic transglycosylases with bacterial cell wall. J Am Chem Soc 135 (2013), 3311–3314.
12. 12 Votsch, W., Templin, M.F., Characterization of a beta-N-acetylglucosaminidase of Escherichia coli and elucidation of its role in muropeptide recycling and beta-lactamase induction. J Biol Chem 275 (2000), 39032–39038.
13. 13 Vocadlo, D.J., Mayer, C., He, S., Withers, S.G., Mechanism of action and identification of Asp242 as the catalytic nucleophile of Vibrio furnisii N-acetyl-beta-D-glucosaminidase using 2-acetamido-2-deoxy-5-fluoro-alpha-L-idopyranosyl fluoride. Biochemistry 39 (2000), 117–126.
14. 14 Stubbs, K.A., Balcewich, M., Mark, B.L., Vocadlo, D.J., Small molecule inhibitors of a glycoside hydrolase attenuate inducible AmpC-mediated beta-lactam resistance. J Biol Chem 282 (2007), 21382–21391.
15. 15 Cheng, Q., Li, H., Merdek, K., Park, J.T., Molecular characterization of the beta-N-acetylglucosaminidase of Escherichia coli and its role in cell wall recycling. J Bacteriol 182 (2000), 4836–4840.
16. 16 Yamaguchi, T., Blazquez, B., Hesek, D., Lee, M., Llarrull, L.I., Boggess, B., Oliver, A.G., Fisher, J.F., Mobashery, S., Inhibitors for bacterial cell-wall recycling. ACS Med Chem Lett 3 (2012), 238–242.
17. 17 Bai, X.H., Chen, H.J., Jiang, Y.L., Wen, Z., Huang, Y., Cheng, W., Li, Q., Qi, L., Zhang, J.R., Chen, Y., et al. Structure of pneumococcal peptidoglycan hydrolase LytB reveals insights into the bacterial cell wall remodeling and pathogenesis. J Biol Chem 289 (2014), 23403–23416.
18. 18 Rico-Lastres, P., Diez-Martínez, R., Iglesias-Bexiga, M., Bustamante, N., Aldridge, C., Hesek, D., Lee, M., Mobashery, S., Gray, J., Vollmer, W., et al. Substrate recognition and catalysis by LytB: a pneumococcal peptidoglycan hydrolase involved in virulence. Sci Rep, 5, 2015, 16198.
19. 19• Perez-Dorado, I., Gonzalez, A., Morales, M., Sanles, R., Striker, W., Vollmer, W., Mobashery, S., Garcia, J.L., Martínez-Ripoll, M., García, P., et al. Insights into pneumococcal fratricide from the crystal structures of the modular killing factor LytC. Nat Struct Mol Biol 17 (2010), 576–581 In this paper, the first structure of a pneumococcal autolysin named LytC was determined in complex with choline and a PG fragment revealing its substrate specificity recognition that justifies for itsin vivo features hydrolysing non-cross-linked PG chains. Therefore, this work affords an explanation for LytC activation during fratricide.
20. 20 Park, Y., Lim, J.A., Kong, M., Ryu, S., Rhee, S., Structure of bacteriophage SPN1S endolysin reveals an unusual two-module fold for the peptidoglycan lytic and binding activity. Mol Microbiol 92 (2014), 316–325.
21. 21 Tamai, E., Yoshida, H., Sekiya, H., Nariya, H., Miyata, S., Okabe, A., Kuwahara, T., Maki, J., Kamitori, S., X-ray structure of a novel endolysin encoded by episomal phage phiSM101 of Clostridium perfringens. Mol Microbiol 92 (2014), 326–337.
22. 22 Claverys, J.P., Havarstein, L.S., Cannibalism and fratricide: mechanisms and raisons d’être. Nat Rev Microbiol 5 (2007), 219–229.
23. 23 Scheurwater, E., Reid, C.W., Clarke, A.J., Lytic transglycosylases: bacterial space-making autolysins. Int J Biochem Cell Biol 40 (2008), 586–591.
24. 24 Cho, H., Uehara, T., Bernhardt, T.G., Beta-lactam antibiotics induce a lethal malfunctioning of the bacterial cell wall synthesis machinery. Cell 159 (2014), 1300–1311.
25. 25 Herlihey, F.A., Clarke, A.J., Controlling autolysis during flagella insertion in Gram-negative bacteria. Advances in Experimental Medicine and Biology, 2016, Springer, US, 1–16, 10.1007/5584_2016_52.
26. 26 Santin, Y.G., Cascales, E., Domestication of a housekeeping transglycosylase for assembly of a Type VI secretion system. EMBO Rep 18 (2016), 138–149, 10.15252/embr.201643206.
27. 27 Artola-Recolons, C., Carrasco-López, C., Llarrull, L.I., Kumarasiri, M., Lastochkin, E., Martinez de Ilarduya, I., Meindl, K., Uson, I., Mobashery, S., Hermoso, J.A., High-resolution crystal structure of MltE, an outer membrane-anchored endolytic peptidoglycan lytic transglycosylase from Escherichia coli. Biochemistry 50 (2011), 2384–2386.
28. 28 Fibriansah, G., Gliubich, F.I., Thunnissen, A.M., On the mechanism of peptidoglycan binding and cleavage by the endo-specific lytic transglycosylase MltE from Escherichia coli. Biochemistry 51 (2012), 9164–9177.
29. 29 Burkinshaw, B.J., Deng, W., Lameignere, E., Wasney, G.A., Zhu, H., Worrall, L.J., Finlay, B.B., Strynadka, N.C., Structural analysis of a specialized type III secretion system peptidoglycan-cleaving enzyme. J Biol Chem 290 (2015), 10406–10417.
30. 30 Herlihey, F.A., Osorio-Valeriano, M., Dreyfus, G., Clarke, A.J., Modulation of the lytic activity of the dedicated autolysin for flagellum formation SltF by flagellar rod proteins FlgB and FlgF. J Bacteriol 198 (2016), 1847–1856.
31. 31 Artola-Recolons, C., Lee, M., Bernardo-García, N., Blázquez, B., Hesek, D., Bartual, S.G., Mahasenan, K.V., Lastochkin, E., Pi, H., Boggess, B., et al. Structure and cell wall cleavage by modular lytic transglycosylase MltC of Escherichia coli. ACS Chem Biol 9 (2014), 2058–2066.
32. 32 Lee, M., Domínguez-Gil, T., Hesek, D., Mahasenan, K.V., Lastochkin, E., Hermoso, J.A., Mobashery, S., Turnover of bacterial cell wall by SltB3, a multidomain lytic transglycosylase of Pseudomonas aeruginosa. ACS Chem Biol 11 (2016), 1525–1531.
33. 33•• Domínguez-Gil, T., Lee, M., Acebrón-Ávalos, I., Mahasenan, K.V., Hesek, D., Dik, D.A., Byun, B., Lastochkin, E., Fisher, J.F., Mobashery, S., et al. Activation by allostery in cell-wall remodeling by a modular membrane-bound lytic transglycosylase from Pseudomonas aeruginosa. Structure 24 (2016), 1729–1741 This study shows for the first time an allosteric mechanism regulating the catalytic activity of a LT. The effector molecules are muropeptides that bind a module in MltF sharing homology with the substrate-binding proteins of ABC transporters.
34. 34 Cavallari, J.F., Lamers, R.P., Scheurwater, E.M., Matos, A.L., Burrows, L.L., Changes to its peptidoglycan-remodeling enzyme repertoire modulate beta-lactam resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 57 (2013), 3078–3084.
35. 35 Li, Y., Jin, K., Setlow, B., Setlow, P., Hao, B., Crystal structure of the catalytic domain of the Bacillus cereus SleB protein, important in cortex peptidoglycan degradation during spore germination. J Bacteriol 194 (2012), 4537–4545.
36. 36 Stapleton, M.R., Horsburgh, M.J., Hayhurst, E.J., Wright, L., Jonsson, I.M., Tarkowski, A., Kokai-Kun, J.F., Mond, J.J., Foster, S.J., Characterization of IsaA and SceD, two putative lytic transglycosylases of Staphylococcus aureus. J Bacteriol 189 (2007), 7316–7325.
37. 37 Squeglia, F., Romano, M., Ruggiero, A., Vitagliano, L., De Simone, A., Berisio, R., Carbohydrate recognition by RpfB from Mycobacterium tuberculosis unveiled by crystallographic and molecular dynamics analyses. Biophys J 104 (2013), 2530–2539.
38. 38 Mavrici, D., Prigozhin, D.M., Alber, T., Mycobacterium tuberculosis RpfE crystal structure reveals a positively charged catalytic cleft. Protein Sci 23 (2014), 481–487.
39. 39 Cohen-Gonsaud, M., Barthe, P., Bagneris, C., Henderson, B., Ward, J., Roumestand, C., Keep, N.H., The structure of a resuscitation-promoting factor domain from Mycobacterium tuberculosis shows homology to lysozymes. Nat Struct Mol Biol 12 (2005), 270–273.
40. 40 Nocadello, S., George Minasov, G., Shuvalova, L.S., Dubrovska, I., Sabini, E., Anderson, W.F., Crystal structures of the SpoIID lytic transglycosylases essential for bacterial sporulation. J Biol Chem 291 (2016), 14915–14926.
41. 41 Buttner, F.M., Renner-Schneck, M., Stehle, T., X-ray crystallography and its impact on understanding bacterial cell wall remodeling processes. Int J Med Microbiol 305 (2015), 209–216.
42. 42 Priyadarshini, R., de Pedro, M.A., Young, K.D., Role of peptidoglycan amidases in the development and morphology of the division septum in Escherichia coli. J Bacteriol 189 (2007), 5334–5347.
43. 43 Zoll, S., Patzold, B., Schlag, M., Gotz, F., Kalbacher, H., Stehle, T., Structural basis of cell wall cleavage by a staphylococcal autolysin. PLoS Pathog, 6, 2010, e1000807.
44. 44 Rivera, I., Molina, R., Lee, M., Mobashery, S., Hermoso, J.A., Orthologous and paralogous AmpD peptidoglycan amidases from Gram-negative bacteria. Microb Drug Resist 22 (2016), 470–476, 10.1089/mdr.2016.0083.
45. 45 Carrasco-López, C., Rojas-Altuve, A., Zhang, W., Hesek, D., Lee, M., Barbe, S., Andre, I., Ferrer, P., Silva-Martín, N., Castro, G.R., et al. Crystal structures of bacterial peptidoglycan amidase AmpD and an unprecedented activation mechanism. J Biol Chem 286 (2011), 31714–31722.
46. 46 Mellroth, P., Sandalova, T., Kikhney, A., Vilaplana, F., Hesek, D., Lee, M., Mobashery, S., Normark, S., Svergun, D., Henriques-Normark, B., et al. Structural and functional insights into peptidoglycan access for the lytic amidase LytA of Streptococcus pneumoniae. MBio 5 (2014), e01120–01113.
47. 47•• Buttner, F.M., Zoll, S., Nega, M., Gotz, F., Stehle, T., Structure-function analysis of Staphylococcus aureus amidase reveals the determinants of peptidoglycan recognition and cleavage. J Biol Chem 289 (2014), 11083–11094 This study shows relevant details for the interaction of PG with the important amidase AmiA ofS. aureus. It also provides important mechanistic details such as the water molecule that carries out the nucleophilic attack on the carbonyl carbon of the scissile bond.
48. 48•• Sandalova, T., Lee, M., Henriques-Normark, B., Hesek, D., Mobashery, S., Mellroth, P., Achour, A., The crystal structure of the major pneumococcal autolysin LytA in complex with a large peptidoglycan fragment reveals the pivotal role of glycans for lytic activity. Mol Microbiol 101 (2016), 954–967, 10.1111/mmi.13435 The pneumococcal amidase LytA is a key virulence factor being a potential target for developing new antibiotics. Throughout this paper, the 3-D structure of LytA:PG complex is dissected, providing a novel structural basis for ligand restriction and revealing for the first time an importance of the multivalent binding to PG saccharides.
49. 49 Kerff, F., Petrella, S., Mercier, F., Sauvage, E., Herman, R., Pennartz, A., Zervosen, A., Luxen, A., Frere, J.M., Joris, B., et al. Specific structural features of the N-acetylmuramoyl-L-alanine amidase AmiD from Escherichia coli and mechanistic implications for enzymes of this family. J Mol Biol 397 (2010), 249–259.
50. 50•• Martínez-Caballero, S., Lee, M., Artola-Recolons, C., Carrasco-López, C., Hesek, D., Spink, E., Lastochkin, E., Zhang, W., Hellman, L.M., Boggess, B., et al. Reaction products and the X-ray structure of AmpDh2, a virulence determinant of Pseudomonas aeruginosa. J Am Chem Soc 135 (2013), 10318–10321 See Ref. [51].
51. 51•• Lee, M., Artola-Recolons, C., Carrasco-López, C., Martínez-Caballero, S., Hesek, D., Spink, E., Lastochkin, E., Zhang, W., Hellman, L.M., Boggess, B., et al. Cell-wall remodeling by the zinc-protease AmpDh3 from Pseudomonas aeruginosa. J Am Chem Soc 135 (2013), 12604–12607 This study, together with Ref. [50], reports the nature of the reaction products of PG amidases AmpDh2 and AmpDh3 with the cell wall and shows that both enzymes interact with the cross-linked PG. A model is proposed for its activityin vivo during processive degradation of cell wall.
52. 52 Liepinsh, E., Genereux, C., Dehareng, D., Joris, B., NMR structure of Citrobacter freundii AmpD, comparison with bacteriophage T7 lysozyme and homology with PGRP domains. J Mol Biol 327 (2003), 833–842.
53. 53 Johnson, J.W., Fisher, J.F., Mobashery, S., Bacterial cell-wall recycling. Ann N Y Acad Sci 1277 (2013), 54–75.
54. 54 Courtin, P., Miranda, G., Guillot, A., Wessner, F., Mezange, C., Domakova, E., Kulakauskas, S., Chapot-Chartier, M.P., Peptidoglycan structure analysis of Lactococcus lactis reveals the presence of an L,D-carboxypeptidase involved in peptidoglycan maturation. J Bacteriol 188 (2006), 5293–5298.
55. 55 Barendt, S.M., Sham, L.T., Winkler, M.E., Characterization of mutants deficient in the L,D-carboxypeptidase (DacB) and WalRK (VicRK) regulon, involved in peptidoglycan maturation of Streptococcus pneumoniae serotype 2 strain D39. J Bacteriol 193 (2011), 2290–2300.
56. 56• Abdullah, M.R., Gutiérrez-Fernández, J., Pribyl, T., Gisch, N., Saleh, M., Rohde, M., Petruschka, L., Burchhardt, G., Schwudke, D., Hermoso, J.A., et al. Structure of the pneumococcal L,D-carboxypeptidase DacB and pathophysiological effects of disabled cell wall hydrolases DacA and DacB. Mol Microbiol 93 (2014), 1183–1206 This study shows together with Ref. [57], the molecular basis of the crucial role of the pneumococcal carboxypeptidases DacB for peptidoglycan architecture, bacterial shape and virulence.
57. 57• Hoyland, C.N., Aldridge, C., Cleverley, R.M., Duchene, M.C., Minasov, G., Onopriyenko, O., Sidiq, K., Stogios, P.J., Anderson, W.F., Daniel, R.A., et al. Structure of the LdcB LD-carboxypeptidase reveals the molecular basis of peptidoglycan recognition. Structure 22 (2014), 949–960 This study describes the residues essential for peptidoglycan recognition and the conformational changes that occur on ligand binding.
58. 58 Wu, Z., Wright, G.D., Walsh, C.T., Overexpression, purification, and characterization of VanX, a D-, D-dipeptidase which is essential for vancomycin resistance in Enterococcus faecium BM4147. Biochemistry 34 (1995), 2455–2463.
59. 59 Arthur, M., Depardieu, F., Snaith, H.A., Reynolds, P.E., Courvalin, P., Contribution of VanY D,D-carboxypeptidase to glycopeptide resistance in Enterococcus faecalis by hydrolysis of peptidoglycan precursors. Antimicrob Agents Chemother 38 (1994), 1899–1903.
60. 60• Meziane-Cherif, D., Stogios, P.J., Evdokimova, E., Savchenko, A., Courvalin, P., Structural basis for the evolution of vancomycin resistance D,D-peptidases. Proc Natl Acad Sci U S A 111 (2014), 5872–5877 Structural characterization de VanXY reveals the molecular basis of their specificity toward vancomycin-susceptible precursors and explains the dual function of VanXY.
61. 61 Kim, H.S., Im, H.N., An, D.R., Yoon, J.Y., Jang, J.Y., Mobashery, S., Hesek, D., Lee, M., Yoo, J., Cui, M., et al. The cell shape-determining Csd6 protein from Helicobacter pylori constitutes a new family of L,D-carboxypeptidase. J Biol Chem 290 (2015), 25103–25117.
62. 62•• Bartual, S.G., Straume, D., Stamsas, G.A., Muñoz, I.G., Alfonso, C., Martínez-Ripoll, M., Håvarstein, L.S., Hermoso, J.A., Structural basis of PcsB-mediated cell separation in Streptococcus pneumoniae. Nat Commun, 5, 2014, 3842 This is the first report in which the CHAP-containing protein PcsB is shown to have muralytic activity and the full-length protein structure presented is suggestive for a model explaining how the activity of the catalytic domain is regulated in the context of cellular division.
63. 63 Layec, S., Decaris, B., Leblond-Bourget, N., Characterization of proteins belonging to the CHAP-related superfamily within the Firmicutes. J Mol Microbiol Biotechnol 14 (2008), 31–40.
64. 64 Rigden, D.J., Jedrzejas, M.J., Galperin, M.Y., Amidase domains from bacterial and phage autolysins define a family of gamma-D,L-glutamate-specific amidohydrolases. Trends Biochem Sci 28 (2003), 230–234.
65. 65 Bateman, A., Rawlings, N.D., The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends Biochem Sci 28 (2003), 234–237.
66. 66 Anantharaman, V., Aravind, L., Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol, 4, 2003, R11.
67. 67 Gu, J., Feng, Y., Feng, X., Sun, C., Lei, L., Ding, W., Niu, F., Jiao, L., Yang, M., Li, Y., et al. Structural and biochemical characterization reveals LysGH15 as an unprecedented EF-hand-like calcium-binding phage lysin. PLoS Pathog, 10, 2014, e1004109.
68. 68 Rossi, P., Aramini, J.M., Xiao, R., Chen, C.X., Nwosu, C., Owens, L.A., Maglaqui, M., Nair, R., Fischer, M., Acton, T.B., et al. Structural elucidation of the Cys–His–Glu–Asn proteolytic relay in the secreted CHAP domain enzyme from the human pathogen Staphylococcus saprophyticus. Proteins 74 (2009), 515–519.
69. 69 Keary, R., Sanz-Gaitero, M., van Raaij, M.J., O'Mahony, J., Fenton, M., McAuliffe, O., Hill, C., Ross, R.P., Coffey, A., Characterization of a bacteriophage-derived murein peptidase for elimination of antibiotic-resistant Staphylococcus aureus. Curr Protein Pept Sci 17 (2016), 183–190.
70. 70 Xu, Q., Mengin-Lecreulx, D., Liu, X.W., Patin, D., Farr, C.L., Grant, J.C., Chiu, H.J., Jaroszewski, L., Knuth, M.W., Godzik, A., et al. Insights into substrate specificity of NlpC/P60 cell wall hydrolases containing bacterial SH3 domains. MBio 6 (2015), 02314–e02327.
71. 71 Xu, Q., Chiu, H.J., Farr, C.L., Jaroszewski, L., Knuth, M.W., Miller, M.D., Lesley, S.A., Godzik, A., Elsliger, M.A., Deacon, A.M., et al. Structures of a bifunctional cell wall hydrolase CwlT containing a novel bacterial lysozyme and an NlpC/P60 D,L-endopeptidase. J Mol Biol 426 (2014), 169–184.
72. 72 Mesnage, S., Dellarole, M., Baxter, N.J., Rouget, J.B., Dimitrov, J.D., Wang, N., Fujimoto, Y., Hounslow, A.M., Lacroix-Desmazes, S., Fukase, K., et al. Molecular basis for bacterial peptidoglycan recognition by LysM domains. Nat Commun, 5, 2014, 4269.
73. 73 Rocaboy, M., Herman, R., Sauvage, E., Remaut, H., Moonens, K., Terrak, M., Charlier, P., Kerff, F., The crystal structure of the cell division amidase AmiC reveals the fold of the AMIN domain, a new peptidoglycan binding domain. Mol Microbiol 90 (2013), 267–277.
74. 74 van Asselt, E.J., Thunnissen, A.M., Dijkstra, B.W., High resolution crystal structures of the Escherichia coli lytic transglycosylase Slt70 and its complex with a peptidoglycan fragment. J Mol Biol 291 (1999), 877–898.
75. 75 Galkin, V.E., Kolappan, S., Ng, D., Zong, Z., Li, J., Yu, X., Egelman, E.H., Craig, L., The structure of the CS1 pilus of enterotoxigenic Escherichia coli reveals structural polymorphism. J Bacteriol 195 (2013), 1360–1370.
76. 76 van Asselt, E.J., Kalk, K.H., Dijkstra, B.W., Crystallographic studies of the interactions of Escherichia coli lytic transglycosylase Slt35 with peptidoglycan. Biochemistry 39 (2000), 1924–1934.
77. 77 van Straaten, K.E., Barends, T.R., Dijkstra, B.W., Thunnissen, A.M., Structure of Escherichia coli lytic transglycosylase MltA with bound chitohexaose: implications for peptidoglycan binding and cleavage. J Biol Chem 282 (2007), 21197–21205.
78. 78 Lu, X., Shi, Y., Zhang, W., Zhang, Y., Qi, J., Gao, G.F., Structure and receptor-binding properties of an airborne transmissible avian influenza A virus hemagglutinin H5 (VN1203mut). Protein Cell 4 (2013), 502–511.
79. 79 Fokine, A., Miroshnikov, K.A., Shneider, M.M., Mesyanzhinov, V.V., Rossmann, M.G., Structure of the bacteriophage phi KZ lytic transglycosylase gp144. J Biol Chem 283 (2008), 7242–7250.