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Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Peptidoglycan Deacetylases in Bacterial Cell Wall Remodeling and Pathogenesis

Author(s): Antoni Planas*

Volume 29, Issue 7, 2022

Published on: 10 January, 2022

Page: [1293 - 1312] Pages: 20

DOI: 10.2174/0929867328666210915113723

Price: $65

Abstract

The bacterial cell wall peptidoglycan (PG) is a dynamic structure that is constantly synthesized, re-modeled and degraded during bacterial division and growth. Postsynthetic modifications modulate the action of endogenous autolysis during PG lysis and remodeling for growth and sporulation, but also they are a mechanism used by pathogenic bacteria to evade the host innate immune system. Modifications of the glycan backbone are limited to the C-2 amine and C-6 hydroxyl moieties of either GlcNAc or MurNAc residues. This paper reviews the functional roles and properties of peptidoglycan de-Nacetylases (distinct PG GlcNAc and MurNAc deacetylases) and recent progress through genetic studies and biochemical characterization to elucidate their mechanism of action, 3D structures, substrate specificities and biological functions. Since they are virulence factors in pathogenic bacteria, peptidoglycan deacetylases are potential targets for the design of novel antimicrobial agents.

Keywords: Peptidoglycan deacetylases, cell wall, pathogenesis, N-acetylglucosamine, N-acetylmuramic, specificity, x-ray structures, antimicrobial targets.

« Previous
[1]
Vollmer, W.; Blanot, D.; De Pedro, M.A. Peptidoglycan structure and architecture. In: FEMS Microbiology Reviews; Oxford Academic, 2008; pp. 149-167.
[http://dx.doi.org/10.1111/j.1574-6976.2007.00094.x]
[2]
Kashyap, D.R.; Wang, M.; Liu, L.H.; Boons, G.J.; Gupta, D.; Dziarski, R. Peptidoglycan recognition proteins kill bacteria by activating protein-sensing two-component systems. Nat. Med., 2011, 17(6), 676-683.
[http://dx.doi.org/10.1038/nm.2357] [PMID: 21602801]
[3]
Kashyap, D.R.; Kuzma, M.; Kowalczyk, D.A.; Gupta, D.; Dziarski, R. Bactericidal peptidoglycan recognition protein induces oxidative stress in Escherichia coli through a block in respiratory chain and increase in central carbon catabolism. Mol. Microbiol., 2017, 105(5), 755-776.
[http://dx.doi.org/10.1111/mmi.13733] [PMID: 28621879]
[4]
De Marzi, M.C.; Todone, M.; Ganem, M.B.; Wang, Q.; Mariuzza, R.A.; Fernández, M.M.; Malchiodi, E.L. Peptidoglycan recognition protein-peptidoglycan complexes increase monocyte/macrophage activation and enhance the inflammatory response. Immunology, 2015, 145(3), 429-442.
[http://dx.doi.org/10.1111/imm.12460] [PMID: 25752767]
[5]
Oliveira-Nascimento, L.; Massari, P.; Wetzler, L.M. The role of TLR2 in infection and immunity. Front. Immunol., 2012, 3, 79.
[http://dx.doi.org/10.3389/fimmu.2012.00079] [PMID: 22566960]
[6]
Wolf, A.J.; Underhill, D.M. Peptidoglycan recognition by the innate immune system. Nat. Rev. Immunol., 2018, 18(4), 243-254.
[http://dx.doi.org/10.1038/nri.2017.136] [PMID: 29292393]
[7]
Inohara, N.; Ogura, Y.; Fontalba, A.; Gutierrez, O.; Pons, F.; Crespo, J.; Fukase, K.; Inamura, S.; Kusumoto, S.; Hashimoto, M.; Foster, S.J.; Moran, A.P.; Fernandez-Luna, J.L.; Nuñez, G. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn’s disease. J. Biol. Chem., 2003, 278(8), 5509-5512.
[http://dx.doi.org/10.1074/jbc.C200673200] [PMID: 12514169]
[8]
Girardin, S.E.; Boneca, I.G.; Viala, J.; Chamaillard, M.; Labigne, A.; Thomas, G.; Philpott, D.J.; Sansonetti, P.J. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem., 2003, 278(11), 8869-8872.
[http://dx.doi.org/10.1074/jbc.C200651200] [PMID: 12527755]
[9]
Moreira, L.O.; Zamboni, D.S. NOD1 and NOD2 Signaling in Infection and Inflammation. Front. Immunol., 2012, 3, 328.
[http://dx.doi.org/10.3389/fimmu.2012.00328] [PMID: 23162548]
[10]
Caruso, R.; Warner, N.; Inohara, N.; Núñez, G. NOD1 and NOD2: signaling, host defense, and inflammatory disease. Immunity, 2014, 41(6), 898-908.
[http://dx.doi.org/10.1016/j.immuni.2014.12.010] [PMID: 25526305]
[11]
Pashenkov, M.V.; Murugina, N.E.; Budikhina, A.S.; Pinegin, B.V. Synergistic interactions between NOD receptors and TLRs: Mechanisms and clinical implications. J. Leukoc. Biol., 2019, 105(4), 669-680.
[http://dx.doi.org/10.1002/JLB.2RU0718-290R] [PMID: 30517768]
[12]
Root-Bernstein, R. Synergistic activation of toll-like and nod receptors by complementary antigens as facilitators of autoimmune disease: review, model and novel predictions. International Journal of Molecular Sciences; MDPI AG, 2020, pp. 1-34.
[http://dx.doi.org/10.3390/ijms21134645]
[13]
Moynihan, P.J.; Sychantha, D.; Clarke, A.J. Chemical biology of peptidoglycan acetylation and deacetylation. Bioorg. Chem., 2014, 54, 44-50.
[http://dx.doi.org/10.1016/j.bioorg.2014.03.010] [PMID: 24769153]
[14]
Yadav, A.K.; Espaillat, A.; Cava, F.; Yadav, A.K.; Espaillat, A. Bacterial strategies to preserve cell wall integrity against environmental threats. Front. Microbiol., 2018, 9, 2064.
[http://dx.doi.org/10.3389/fmicb.2018.02064] [PMID: 30233540]
[15]
Blake, C.C.F.; Koenig, D.F.; Mair, G.A.; North, A.C.T.; Phillips, D.C.; Sarma, V.R. Structure of hen egg-white lysozyme. a three-dimensional fourier synthesis at 2 Angstrom resolution. Nature, 1965, 206(4986), 757-761.
[http://dx.doi.org/10.1038/206757a0] [PMID: 5891407]
[16]
Clarke, A.J.; Dupont, C. O-acetylated peptidoglycan: its occurrence, pathobiological significance, and biosynthesis. Can. J. Microbiol., 1992, 38(2), 85-91.
[http://dx.doi.org/10.1139/m92-014] [PMID: 1521192]
[17]
Uehara, T.; Bernhardt, T.G. More than just lysins: peptidoglycan hydrolases tailor the cell wall. Current Opinion in Microbiology; NIH Public Access, 2011, pp. 698-703.
[http://dx.doi.org/10.1016/j.mib.2011.10.003]
[18]
Moynihan, P.J.; Clarke, A.J. O-acetylated peptidoglycan: controlling the activity of bacterial autoly-sins and lytic enzymes of innate immune systems. Int. J. Biochem. Cell Biol., Elsevier Ltd. 2011, 1655-1659.
[http://dx.doi.org/10.1016/j.biocel.2011.08.007]
[19]
Araki, Y.; Fukuoka, S.; Oba, S.; Ito, E. Enzymatic deacetylation of N-acetylglucosamine residues in peptidoglycan from Bacillus cereus cell walls. Biochem. Biophys. Res. Commun., 1971, 45(3), 751-758.
[http://dx.doi.org/10.1016/0006-291X(71)90481-5] [PMID: 4256847]
[20]
Araki, Y.; Oba, S.; Araki, S.; Ito, E. Enzymatic deacetylation of N-acetylglucosamine residues in cell wall peptidoglycan. J. Biochem., 1980, 88(2), 469-479.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a132994] [PMID: 6774970]
[21]
Mirelman, D.; Sharon, N. Isolation and characterization of two disaccharide-peptides from lysozyme digests of Micrococcus lysodeikticus cell walls. Biochem. Biophys. Res. Commun., 1966, 24(2), 237-243.
[http://dx.doi.org/10.1016/0006-291X(66)90726-1] [PMID: 5965232]
[22]
Warth, A.D.; Strominger, J.L. Structure of the peptidoglycan of bacterial spores: occurrence of the lactam of muramic acid. Proc. Natl. Acad. Sci. USA, 1969, 64(2), 528-535.
[http://dx.doi.org/10.1073/pnas.64.2.528] [PMID: 4982357]
[23]
Lombard, V.; Golaconda Ramulu, H.; Drula, E.; Coutinho, P.M.; Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res., 2014, 42(Database issue), D490-D495.
[http://dx.doi.org/10.1093/nar/gkt1178] [PMID: 24270786]
[24]
Pascual, S.; Planas, A. Carbohydrate de-N-acetylases acting on structural polysaccharides and glycoconjugates. Curr. Opin. Chem. Biol., 2021, 61, 9-18.
[http://dx.doi.org/10.1016/j.cbpa.2020.09.003] [PMID: 33075728]
[25]
John, M.; Röhrig, H.; Schmidt, J.; Wieneke, U.; Schell, J. Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc. Natl. Acad. Sci. USA, 1993, 90(2), 625-629.
[http://dx.doi.org/10.1073/pnas.90.2.625] [PMID: 8421697]
[26]
Blair, D.E.; Schüttelkopf, A.W.; MacRae, J.I.; van Aalten, D.M.F. Structure and metal-dependent mechanism of peptidoglycan deacetylase, a streptococcal virulence factor. Proc. Natl. Acad. Sci. USA, 2005, 102(43), 15429-15434.
[http://dx.doi.org/10.1073/pnas.0504339102] [PMID: 16221761]
[27]
Aragunde, H.; Biarnés, X.; Planas, A. Substrate recognition and specificity of chitin deacetylases and related family 4 carbohydrate esterases. Int. J. Mol. Sci., 2018, 19(2), 412.
[http://dx.doi.org/10.3390/ijms19020412] [PMID: 29385775]
[28]
Andrés, E.; Albesa-Jové, D.; Biarnés, X.; Moerschbacher, B.M.; Guerin, M.E.; Planas, A. Structural basis of chitin oligosaccharide deacetylation. Angew. Chem. Int. Ed. Engl., 2014, 53(27), 6882-6887.
[http://dx.doi.org/10.1002/anie.201400220] [PMID: 24810719]
[29]
Grifoll-Romero, L.; Pascual, S.; Aragunde, H.; Biarnés, X.; Planas, A. Chitin deacetylases: structures, specificities, and biotech applications. Polymers (Basel), 2018, 10(4), 352.
[http://dx.doi.org/10.3390/polym10040352] [PMID: 30966387]
[30]
Weiser, J.N. The pneumococcus: why a commensal misbehaves. J. Mol. Med. (Berl.), 2010, 88(2), 97-102.
[http://dx.doi.org/10.1007/s00109-009-0557-x] [PMID: 19898768]
[31]
Vollmer, W.; Tomasz, A. The pgdA gene encodes for a peptidoglycan N-acetylglucosamine deacetylase in Streptococcus pneumoniae. J. Biol. Chem., 2000, 275(27), 20496-20501.
[http://dx.doi.org/10.1074/jbc.M910189199] [PMID: 10781617]
[32]
Vollmer, W.; Tomasz, A.; Peptidoglycan, N. Peptidoglycan N-acetylglucosamine deacetylase, a putative virulence factor in Streptococcus pneumoniae. Infect. Immun., 2002, 70(12), 7176-7178.
[http://dx.doi.org/10.1128/IAI.70.12.7176-7178.2002] [PMID: 12438406]
[33]
Meyrand, M.; Boughammoura, A.; Courtin, P.; Mézange, C.; Guillot, A.; Chapot-Chartier, M.P. Peptidoglycan N-acetylglucosamine deacetylation decreases autolysis in Lactococcus lactis. Microbiology, 2007, 153(Pt 10), 3275-3285.
[http://dx.doi.org/10.1099/mic.0.2007/005835-0] [PMID: 17906127]
[34]
Cao, L.; Liang, D.; Hao, P.; Song, Q.; Xue, E.; Caiyin, Q.; Cheng, Z.; Qiao, J. The increase of O-acetylation and N-deacetylation in cell wall promotes acid resistance and nisin production through improving cell wall integrity in Lactococcus lactis. J. Ind. Microbiol. Biotechnol., 2018, 45(9), 813-825.
[http://dx.doi.org/10.1007/s10295-018-2052-2] [PMID: 29876686]
[35]
Dussurget, O.; Pizarro-Cerda, J.; Cossart, P. Molecular determinants of Listeria monocytogenes virulence. Annu. Rev. Microbiol., 2004, 58, 587-610.
[http://dx.doi.org/10.1146/annurev.micro.57.030502.090934] [PMID: 15487949]
[36]
Hamon, M.; Bierne, H.; Cossart, P. Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol., 2006, 4(6), 423-434.
[http://dx.doi.org/10.1038/nrmicro1413] [PMID: 16710323]
[37]
Boneca, I.G.; Dussurget, O.; Cabanes, D.; Nahori, M.A.; Sousa, S.; Lecuit, M.; Psylinakis, E.; Bouriotis, V.; Hugot, J.P.; Giovannini, M.; Coyle, A.; Bertin, J.; Namane, A.; Rousselle, J.C.; Cayet, N.; Prévost, M.C.; Balloy, V.; Chignard, M.; Philpott, D.J.; Cossart, P.; Girardin, S.E. A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc. Natl. Acad. Sci. USA, 2007, 104(3), 997-1002.
[http://dx.doi.org/10.1073/pnas.0609672104] [PMID: 17215377]
[38]
Rae, C.S.; Geissler, A.; Adamson, P.C.; Portnoy, D.A. Mutations of the Listeria monocytogenes peptidoglycan N-deacetylase and O-acetylase result in enhanced lysozyme sensitivity, bacteriolysis, and hyperinduction of innate immune pathways. Infect. Immun., 2011, 79(9), 3596-3606.
[http://dx.doi.org/10.1128/IAI.00077-11] [PMID: 21768286]
[39]
Popowska, M.; Kusio, M.; Szymañska, P.; Markiewicz, Z. Inactivation of the wall-associated de-N-acetylase (PgdA) of Listeria monocytogenes results in greater susceptibility of the cells to induced autolysis. J. Microbiol. Biotechnol., 2009, 19(9), 932-945.
[http://dx.doi.org/10.4014/jmb.0810.557] [PMID: 19809250]
[40]
Rismondo, J.; Wamp, S.; Aldridge, C.; Vollmer, W.; Halbedel, S. Stimulation of PgdA-dependent peptidoglycan N-deacetylation by GpsB-PBP A1 in Listeria monocytogenes. Mol. Microbiol., 2018, 107(4), 472-487.
[http://dx.doi.org/10.1111/mmi.13893] [PMID: 29215169]
[41]
Hébert, L.; Courtin, P.; Torelli, R.; Sanguinetti, M.; Chapot-Chartier, M.P.; Auffray, Y.; Benachour, A. Enterococcus faecalis constitutes an unusual bacterial model in lysozyme resistance. Infect. Immun., 2007, 75(11), 5390-5398.
[http://dx.doi.org/10.1128/IAI.00571-07] [PMID: 17785473]
[42]
Benachour, A.; Ladjouzi, R.; Le Jeune, A.; Hébert, L.; Thorpe, S.; Courtin, P.; Chapot-Chartier, M.P.; Prajsnar, T.K.; Foster, S.J.; Mesnage, S. The lysozyme-induced peptidoglycan N-acetylglucosamine deacetylase PgdA (EF1843) is required for Enterococcus faecalis virulence. J. Bacteriol., 2012, 194(22), 6066-6073.
[http://dx.doi.org/10.1128/JB.00981-12] [PMID: 22961856]
[43]
Fittipaldi, N.; Sekizaki, T.; Takamatsu, D.; de la Cruz Domínguez-Punaro, M.; Harel, J.; Bui, N.K.; Vollmer, W.; Gottschalk, M. Significant contribution of the pgdA gene to the virulence of Streptococcus suis. Mol. Microbiol., 2008, 70(5), 1120-1135.
[http://dx.doi.org/10.1111/j.1365-2958.2008.06463.x] [PMID: 18990186]
[44]
Wang, G.; Olczak, A.; Forsberg, L.S.; Maier, R.J. Oxidative stress-induced peptidoglycan deacetylase in Helicobacter pylori. J. Biol. Chem., 2009, 284(11), 6790-6800.
[http://dx.doi.org/10.1074/jbc.M808071200] [PMID: 19147492]
[45]
Wang, G.; Maier, S.E.; Lo, L.F.; Maier, G.; Dosi, S.; Maier, R.J. Peptidoglycan deacetylation in Helicobacter pylori contributes to bacterial survival by mitigating host immune responses. Infect. Immun., 2010, 78(11), 4660-4666.
[http://dx.doi.org/10.1128/IAI.00307-10] [PMID: 20805339]
[46]
Shaik, M.M.; Cendron, L.; Percudani, R.; Zanotti, G. The structure of Helicobacter pylori HP0310 reveals an atypical peptidoglycan deacetylase. PLoS One, 2011, 6(4), e19207.
[http://dx.doi.org/10.1371/journal.pone.0019207] [PMID: 21559431]
[47]
Suarez, G.; Romero-Gallo, J.; Piazuelo, M.B.; Wang, G.; Maier, R.J.; Forsberg, L.S.; Azadi, P.; Gomez, M.A.; Correa, P.; Peek, R.M. Jr. Modification of helicobacter pylori peptidoglycan enhances NOD1 activation and promotes cancer of the stomach. Cancer Res., 2015, 75(8), 1749-1759.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-2291] [PMID: 25732381]
[48]
Kaoukab-Raji, A.; Biskri, L.; Bernardini, M.L.; Allaoui, A. Characterization of SfPgdA, a Shigella flexneri peptidoglycan deacetylase required for bacterial persistence within polymorphonuclear neutrophils. Microbes Infect., 2012, 14(7-8), 619-627.
[http://dx.doi.org/10.1016/j.micinf.2012.01.009] [PMID: 22307019]
[49]
Yang, S.; Zhang, F.; Kang, J.; Zhang, W.; Deng, G.; Xin, Y.; Ma, Y. Mycobacterium tuberculosis Rv1096 protein: gene cloning, protein expression, and peptidoglycan deacetylase activity. BMC Microbiol., 2014, 14(1), 174.
[http://dx.doi.org/10.1186/1471-2180-14-174] [PMID: 24975018]
[50]
Lu, Q.; Zhang, W.; Fang, J.; Zheng, J.; Dong, C.; Xiong, S. Mycobacterium tuberculosis Rv1096, facilitates mycobacterial survival by modulating the NF-κB/MAPK pathway as peptidoglycan N-deacetylase. Mol. Immunol., 2020, 127(127), 47-55.
[http://dx.doi.org/10.1016/j.molimm.2020.08.005] [PMID: 32927163]
[51]
Ho, T.D.; Williams, K.B.; Chen, Y.; Helm, R.F.; Popham, D.L.; Ellermeier, C.D. Clostridium difficile extracytoplasmic function σ factor σV regulates lysozyme resistance and is necessary for pathogenesis in the hamster model of infection. Infect. Immun., 2014, 82(6), 2345-2355.
[http://dx.doi.org/10.1128/IAI.01483-13] [PMID: 24664503]
[52]
Coullon, H.; Rifflet, A.; Wheeler, R.; Janoir, C.; Boneca, I.G.; Candela, T. Peptidoglycan analysis reveals that synergistic deacetylase activity in vegetative clostridium difficile impacts the host response. J. Biol. Chem., 2020, 295(49), 16785-16796.
[http://dx.doi.org/10.1074/jbc.RA119.012442]
[53]
Kaus, G.M.; Snyder, L.F.; Müh, U.; Flores, M.J.; Popham, D.L.; Ellermeier, C.D. Lysozyme resistance in clostridioides difficile is dependent on two peptidoglycan deacetylases. J. Bacteriol., 2020, 202(22), e00421-20.
[http://dx.doi.org/10.1128/JB.00421-20] [PMID: 32868404]
[54]
Lambert, C.; Lerner, T.R.; Bui, N.K.; Somers, H.; Aizawa, S.; Liddell, S.; Clark, A.; Vollmer, W.; Lovering, A.L.; Sockett, R.E. Interrupting peptidoglycan deacetylation during Bdellovibrio predator-prey interaction prevents ultimate destruction of prey wall, liberating bacterial-ghosts. Sci. Rep., 2016, 6(1), 26010.
[http://dx.doi.org/10.1038/srep26010] [PMID: 27211869]
[55]
Deng, D.M.; Urch, J.E.; ten Cate, J.M.; Rao, V.A.; van Aalten, D.M.F.; Crielaard, W. Streptococcus mutans SMU.623c codes for a functional, metal-dependent polysaccharide deacetylase that modulates interactions with salivary agglutinin. J. Bacteriol., 2009, 191(1), 394-402.
[http://dx.doi.org/10.1128/JB.00838-08] [PMID: 18978064]
[56]
Milani, C.J.E.; Aziz, R.K.; Locke, J.B.; Dahesh, S.; Nizet, V.; Buchanan, J.T. The novel polysaccharide deacetylase homologue Pdi contributes to virulence of the aquatic pathogen Streptococcus iniae. Microbiology, 2010, 156(Pt 2), 543-554.
[http://dx.doi.org/10.1099/mic.0.028365-0] [PMID: 19762441]
[57]
Kao, P.H.N.; Kline, K.A. Dr. Jekyll and Mr. Hide: How Enterococcus faecalis subverts the host immune response to cause infection. J. Mol. Biol., 2019, 431(16), 2932-2945.
[http://dx.doi.org/10.1016/j.jmb.2019.05.030] [PMID: 31132360]
[58]
Goyette-Desjardins, G.; Auger, J.P.; Xu, J.; Segura, M.; Gottschalk, M. Streptococcus suis, an important pig pathogen and emerging zoonotic agent-an update on the worldwide distribution based on serotyping and sequence typing. Emerg. Microbes Infect., 2014, 3(6), e45.
[http://dx.doi.org/10.1038/emi.2014.45] [PMID: 26038745]
[59]
Kusters, J.G.; van Vliet, A.H.M.; Kuipers, E.J. Pathogenesis of Helicobacter pylori infection. Clin. Microbiol. Rev., 2006, 19(3), 449-490.
[http://dx.doi.org/10.1128/CMR.00054-05] [PMID: 16847081]
[60]
Austin, C.M.; Maier, R.J. Aconitase-mediated posttranscriptional regulation of Helicobacter pylori peptidoglycan deacetylase. J. Bacteriol., 2013, 195(23), 5316-5322.
[http://dx.doi.org/10.1128/JB.00720-13] [PMID: 24056106]
[61]
Nisa, I.; Qasim, M.; Yasin, N.; Ullah, R.; Ali, A. Shigella flexneri: an emerging pathogen. Folia Microbiologica; Springer, 2020, pp. 275-291.
[http://dx.doi.org/10.1007/s12223-020-00773-w]
[62]
Jennison, A.V.; Verma, N.K. Shigella flexneri Infection: pathogenesis and vaccine development. FEMS Microbiology Reviews; Elsevier, 2004, pp. 43-58.
[http://dx.doi.org/10.1016/j.femsre.2003.07.002]
[63]
Lin, Z.; Cai, X.; Chen, M.; Ye, L.; Wu, Y.; Wang, X.; Lv, Z.; Shang, Y.; Qu, D. Virulence and stress responses of Shigella flexneri regulated by PhoP/PhoQ. Front. Microbiol., 2018, 8(JAN), 2689.
[http://dx.doi.org/10.3389/fmicb.2017.02689] [PMID: 29379483]
[64]
Maitra, A.; Munshi, T.; Healy, J.; Martin, L.T.; Vollmer, W.; Keep, N.H.; Bhakta, S. Cell wall peptidoglycan in Mycobacterium tuberculosis: an achilles’ heel for the TB-causing pathogen. FEMS Microbiology Reviews; Oxford University Press, 2019, pp. 548-275.
[http://dx.doi.org/10.1093/femsre/fuz016]
[65]
Bartlett, J.G. Clostridium difficile infection. Infectious Disease Clinics of North America; Massachusetts Medical Society, 2017, pp. 489-495.
[http://dx.doi.org/10.1016/j.idc.2017.05.012]
[66]
Peltier, J.; Courtin, P.; El Meouche, I.; Lemée, L.; Chapot-Chartier, M.P.; Pons, J.L. Clostridium difficile has an original peptidoglycan structure with a high level of N-acetylglucosamine deacetylation and mainly 3-3 cross-links. J. Biol. Chem., 2011, 286(33), 29053-29062.
[http://dx.doi.org/10.1074/jbc.M111.259150] [PMID: 21685382]
[67]
Kirk, J.A.; Banerji, O.; Fagan, R.P. Characteristics of the Clostridium difficile cell envelope and its importance in therapeutics. Microb. Biotechnol., 2017, 10(1), 76-90.
[http://dx.doi.org/10.1111/1751-7915.12372] [PMID: 27311697]
[68]
Negus, D.; Moore, C.; Baker, M.; Raghunathan, D.; Tyson, J.; Sockett, R.E. Predator versus pathogen: how does predatory bdellovibrio bacteriovorus interface with the challenges of killing gram-negative pathogens in a host setting? Annu. Rev. Microbiol., 2017, 71(1), 441-457.
[http://dx.doi.org/10.1146/annurev-micro-090816-093618] [PMID: 28886689]
[69]
Sockett, R.E. Predatory lifestyle of bdellovibrio bacteriovorus. Annu. Rev. Microbiol., 2009, 63, 523-539.
[http://dx.doi.org/10.1146/annurev.micro.091208.073346]
[70]
Loesche, W.J. Role of Streptococcus Mutans in Human Dental Decay. Microbiological Reviews. American Society for Microbiology; ASM, 1986, pp. 353-380.
[http://dx.doi.org/10.1128/MMBR.50.4.353-380.1986]
[71]
Wang, Q.; Zhang, C.; Xu, L.; Chen, J.; Wang, X. Characterization of Streptococcus Iniae ghost vac-cine and its immunization in nile tilapia (Oreochromis niloticus). Aquac. Res., 2020, are.14990.
[http://dx.doi.org/ 10.1111/are.14990]
[72]
Agnew, W.; Barnes, A.C. Streptococcus iniae: an aquatic pathogen of global veterinary significance and a challenging candidate for reliable vaccination. Veterinary Microbiology; Elsevier, 2007, pp. 1-15.
[http://dx.doi.org/10.1016/j.vetmic.2007.03.002]
[73]
Ehling-Schulz, M.; Lereclus, D.; Koehler, T.M. The Bacillus Cereus Group. Bacillus species with pathogenic potential. Microbiol. Spectr., 2019, 7(3), 10.1128/microbiolspec. GPP3-0032-2018
[http://dx.doi.org/10.1128/microbiolspec.GPP3-0032-2018] [PMID: 31111815]
[74]
Żakowska, D.; Bartoszcze, M.; Niemcewicz, M.; Bielawska-Drózd, A.; Knap, J.; Cieślik, P.; Chomiczewski, K.; Kocik, J. Bacillus anthracis infections – new possibilities of treatment. Annals of Agricultural and Environmental Medicine; Institute of Rural Health, 2015, pp. 202-207.
[http://dx.doi.org/10.5604/12321966.1152065]
[75]
Balomenou, S.; Fouet, A.; Tzanodaskalaki, M.; Couture-Tosi, E.; Bouriotis, V.; Boneca, I.G. Distinct functions of polysaccharide deacetylases in cell shape, neutral polysaccharide synthesis and virulence of Bacillus anthracis. Mol. Microbiol., 2013, 87(4), 867-883.
[http://dx.doi.org/10.1111/mmi.12137] [PMID: 23336745]
[76]
Giastas, P.; Andreou, A.; Papakyriakou, A.; Koutsioulis, D.; Balomenou, S.; Tzartos, S.J.; Bouriotis, V.; Eliopoulos, E.E. Structures of the Peptidoglycan N-Acetylglucosamine Deacetylase Bc1974 and Its Complexes with Zinc Metalloenzyme Inhibitors. Biochemistry, 2018, 57(5), 753-763.
[http://dx.doi.org/10.1021/acs.biochem.7b00919] [PMID: 29257674]
[77]
Prejanò, M.; Romeo, I.; Sgrizzi, L.; Russo, N.; Marino, T. Why hydroxy-proline improves the catalytic power of the peptidoglycan N-deacetylase enzyme: insight from theory. Phys. Chem. Chem. Phys., 2019, 21(42), 23338-23345.
[http://dx.doi.org/10.1039/C9CP03804C] [PMID: 31617504]
[78]
Psylinakis, E.; Boneca, I.G.; Mavromatis, K.; Deli, A.; Hayhurst, E.; Foster, S.J.; Vårum, K.M.; Bouriotis, V. Peptidoglycan N-acetylglucosamine deacetylases from Bacillus cereus, highly conserved proteins in Bacillus anthracis. J. Biol. Chem., 2005, 280(35), 30856-30863.
[http://dx.doi.org/10.1074/jbc.M407426200] [PMID: 15961396]
[79]
Fadouloglou, V.E.; Balomenou, S.; Aivaliotis, M.; Kotsifaki, D.; Arnaouteli, S.; Tomatsidou, A.; Efstathiou, G.; Kountourakis, N.; Miliara, S.; Griniezaki, M.; Tsalafouta, A.; Pergantis, S.A.; Boneca, I.G.; Glykos, N.M.; Bouriotis, V.; Kokkinidis, M. Unusual α-Carbon Hydroxylation of Proline Promotes Active-Site Maturation. J. Am. Chem. Soc., 2017, 139(15), 5330-5337.
[http://dx.doi.org/10.1021/jacs.6b12209] [PMID: 28333455]
[80]
Fadouloglou, V.E.; Kapanidou, M.; Agiomirgianaki, A.; Arnaouteli, S.; Bouriotis, V.; Glykos, N.M.; Kokkinidis, M. Structure determination through homology modelling and torsion-angle simulated annealing: application to a polysaccharide deacetylase from Bacillus cereus. Acta Crystallogr. D Biol. Crystallogr., 2013, 69(Pt 2), 276-283.
[http://dx.doi.org/10.1107/S0907444912045829] [PMID: 23385463]
[81]
Arnaouteli, S.; Giastas, P.; Andreou, A.; Tzanodaskalaki, M.; Aldridge, C.; Tzartos, S.J.; Vollmer, W.; Eliopoulos, E.; Bouriotis, V. Two Putative Polysaccharide Deacetylases Are Required for Osmotic Stability and Cell Shape Maintenance in Bacillus anthracis. J. Biol. Chem., 2015, 290(21), 13465-13478.
[http://dx.doi.org/10.1074/jbc.M115.640029] [PMID: 25825488]
[82]
Andreou, A.; Giastas, P.; Arnaouteli, S.; Tzanodaskalaki, M.; Tzartos, S.J.; Bethanis, K.; Bouriotis, V.; Eliopoulos, E.E. The putative polysaccharide deacetylase Ba0331: cloning, expression, crystallization and structure determination. Acta Crystallogr. F Struct. Biol. Commun., 2019, 75(Pt 4), 312-320.
[http://dx.doi.org/10.1107/S2053230X19001766] [PMID: 30950833]
[83]
Soni, A.; Oey, I.; Silcock, P.; Ross, I.K.; Bremer, P.J. Effect of Pulsed Electric Field with Moderate Heat (80°C) on Inactivation, Thermal Resistance and Differential Gene Expression in B. cereus Spores. J. Food Process. Preserv., 2020, 44(7)
[http://dx.doi.org/10.1111/jfpp.14503]
[84]
Tomatsidou, A.; Koutsioulis, D.; Tzamarias, D.; Kokkinidis, M.; Vollmer, W.; Bouriotis, V. Role of the Putative Polysaccharide Deacetylase BA1836 from B. anthracis in Spore Development and Germination. Adv. Microbiol., 2019, 9, 679-702.
[http://dx.doi.org/10.4236/aim.2019.98042]
[85]
Andreou, A.; Giastas, P.; Christoforides, E.; Eliopoulos, E.E. Structural and Evolutionary Insights within the Polysaccharide Deacetylase Gene Family of Bacillus anthracis and Bacillus cereus. Genes (Basel), 2018, 9(8), 386.
[http://dx.doi.org/10.3390/genes9080386] [PMID: 30065210]
[86]
Strunk, R.J.; Piemonte, K.M.; Petersen, N.M.; Koutsioulis, D.; Bouriotis, V.; Perry, K.; Cole, K.E. Structure determination of BA0150, a putative polysaccharide deacetylase from Bacillus anthracis. Acta Crystallogr. F Struct. Biol. Commun., 2014, 70(Pt 2), 156-159.
[http://dx.doi.org/10.1107/S2053230X13034262] [PMID: 24637747]
[87]
Khanna, K.; Lopez-Garrido, J.; Pogliano, K. Shaping an Endospore: Architectural Transformations During Bacillus subtilis Sporulation. Annu. Rev. Microbiol., 2020, 74, 361-386.
[http://dx.doi.org/10.1146/annurev-micro-022520-074650] [PMID: 32660383]
[88]
Fukushima, T.; Yamamoto, H.; Atrih, A.; Foster, S.J.; Sekiguchi, J. A polysaccharide deacetylase gene (pdaA) is required for germination and for production of muramic δ-lactam residues in the spore cortex of Bacillus subtilis. J. Bacteriol., 2002, 184(21), 6007-6015.
[http://dx.doi.org/10.1128/JB.184.21.6007-6015.2002] [PMID: 12374835]
[89]
Gilmore, M.E.; Bandyopadhyay, D.; Dean, A.M.; Linnstaedt, S.D.; Popham, D.L. Production of muramic δ-lactam in Bacillus subtilis spore peptidoglycan. J. Bacteriol., 2004, 186(1), 80-89.
[http://dx.doi.org/10.1128/JB.186.1.80-89.2004] [PMID: 14679227]
[90]
Fukushima, T.; Kitajima, T.; Sekiguchi, J. A polysaccharide deacetylase homologue, PdaA, in Bacillus subtilis acts as an N-acetylmuramic acid deacetylase in vitro. J. Bacteriol., 2005, 187(4), 1287-1292.
[http://dx.doi.org/10.1128/JB.187.4.1287-1292.2005] [PMID: 15687192]
[91]
Blair, D.E.; van Aalten, D.M.F. Structures of Bacillus subtilis PdaA, a family 4 carbohydrate esterase, and a complex with N-acetyl-glucosamine. FEBS Lett., 2004, 570(1-3), 13-19.
[http://dx.doi.org/10.1016/j.febslet.2004.06.013] [PMID: 15251431]
[92]
Fukushima, T.; Tanabe, T.; Yamamoto, H.; Hosoya, S.; Sato, T.; Yoshikawa, H.; Sekiguchi, J. Characterization of a polysaccharide deacetylase gene homologue (pdaB) on sporulation of Bacillus subtilis. J. Biochem., 2004, 136(3), 283-291.
[http://dx.doi.org/10.1093/jb/mvh151] [PMID: 15598884]
[93]
Eminoğlu, A.; Ülker, S.; Sandallı, C. Cloning, Purification and Characterization of Acetyl Xylane Esterase from Anoxybacillus flavithermus DSM 2641(T) with Activity on Low Molecular-Weight Acetates. Protein J., 2015, 34(4), 237-242.
[http://dx.doi.org/10.1007/s10930-015-9618-x] [PMID: 26126589]
[94]
Kobayashi, K.; Sudiarta, I.P.; Kodama, T.; Fukushima, T.; Ara, K.; Ozaki, K.; Sekiguchi, J. Identification and characterization of a novel polysaccharide deacetylase C (PdaC) from Bacillus subtilis. J. Biol. Chem., 2012, 287(13), 9765-9776.
[http://dx.doi.org/10.1074/jbc.M111.329490] [PMID: 22277649]
[95]
Grifoll-Romero, L.; Sainz-Polo, M.A.; Albesa-Jové, D.; Guerin, M.E.; Biarnés, X.; Planas, A. Structure-function relationships underlying the dual N-acetylmuramic and N-acetylglucosamine specificities of the bacterial peptidoglycan deacetylase PdaC. J. Biol. Chem., 2019, 294(50), 19066-19080.
[http://dx.doi.org/10.1074/jbc.RA119.009510] [PMID: 31690626]
[96]
Hu, K.; Yang, H.; Liu, G.; Tan, H. Identification and characterization of a polysaccharide deacetylase gene from Bacillus thuringiensis. Can. J. Microbiol., 2006, 52(10), 935-941.
[http://dx.doi.org/10.1139/w06-045] [PMID: 17110961]
[97]
Taylor, E.J.; Gloster, T.M.; Turkenburg, J.P.; Vincent, F.; Brzozowski, A.M.; Dupont, C.; Shareck, F.; Centeno, M.S.J.; Prates, J.A.M.; Puchart, V.; Ferreira, L.M.A.; Fontes, C.M.G.A.; Biely, P.; Davies, G.J. Structure and activity of two metal ion-dependent acetylxylan esterases involved in plant cell wall degradation reveals a close similarity to peptidoglycan deacetylases. J. Biol. Chem., 2006, 281(16), 10968-10975.
[http://dx.doi.org/10.1074/jbc.M513066200] [PMID: 16431911]
[98]
Coullon, H.; Rifflet, A.; Wheeler, R.; Janoir, C.; Boneca, I.G.; Candela, T. N-Deacetylases required for muramic-δ-lactam production are involved in Clostridium difficile sporulation, germination, and heat resistance. J. Biol. Chem., 2018, 293(47), 18040-18054.
[http://dx.doi.org/10.1074/jbc.RA118.004273] [PMID: 30266804]
[99]
Szurmant, H.; Fukushima, T.; Hoch, J.A. The essential YycFG two-component system of Bacillus subtilis. Methods Enzymol., 2007, 422(06), 396-417.
[http://dx.doi.org/10.1016/S0076-6879(06)22020-2] [PMID: 17628151]
[100]
Cardona, S.T.; Choy, M.; Hogan, A.M. Essential Two-Component Systems Regulating Cell Envelope Functions: Opportunities for Novel Antibiotic Therapies. J. Membr. Biol., 2018, 251(1), 75-89.
[http://dx.doi.org/10.1007/s00232-017-9995-5] [PMID: 29098331]
[101]
Smits, W.K.; Lyras, D.; Lacy, D.B.; Wilcox, M.H.; Kuijper, E.J. Clostridium difficile infection. Nat. Rev. Dis. Primers, 2016, 2(1), 16020.
[http://dx.doi.org/10.1038/nrdp.2016.20] [PMID: 27158839]
[102]
Bartlett, J.G. Clostridium Difficile Infection. Infect. Dis. Clin. North Am., 2017, 31(3), 489-495.
[http://dx.doi.org/10.1016/j.idc.2017.05.012]
[103]
Bui, N.K.; Turk, S.; Buckenmaier, S.; Stevenson-Jones, F.; Zeuch, B.; Gobec, S.; Vollmer, W. Development of screening assays and discovery of initial inhibitors of pneumococcal peptidoglycan deacetylase PgdA. Biochem. Pharmacol., 2011, 82(1), 43-52.
[http://dx.doi.org/10.1016/j.bcp.2011.03.028] [PMID: 21501597]
[104]
Balomenou, S.; Koutsioulis, D.; Tomatsidou, A.; Tzanodaskalaki, M.; Petratos, K.; Bouriotis, V. Polysaccharide deacetylases serve as new targets for the design of inhibitors against Bacillus anthracis and Bacillus cereus. Bioorg. Med. Chem., 2018, 26(13), 3845-3851.
[http://dx.doi.org/10.1016/j.bmc.2018.06.045] [PMID: 29983281]
[105]
Melnyk, J.E.; Mohanan, V.; Schaefer, A.K.; Hou, C.W.; Grimes, C.L. Peptidoglycan Modifications Tune the Stability and Function of the Innate Immune Receptor Nod2. J. Am. Chem. Soc., 2015, 137(22), 6987-6990.
[http://dx.doi.org/10.1021/jacs.5b01607] [PMID: 26035228]
[106]
Wang, Y.; Lazor, K.M.; DeMeester, K.E.; Liang, H.; Heiss, T.K.; Grimes, C.L. Postsynthetic Modification of Bacterial Peptidoglycan Using Bioorthogonal N-Acetylcysteamine Analogs and Peptidoglycan O-Acetyltransferase B. J. Am. Chem. Soc., 2017, 139(39), 13596-13599.
[http://dx.doi.org/10.1021/jacs.7b06820] [PMID: 28898061]
[107]
DeMeester, K.E.; Liang, H.; Jensen, M.R.; Jones, Z.S.; D’Ambrosio, E.A.; Scinto, S.L.; Zhou, J.; Grimes, C.L. Synthesis of Functionalized N-Acetyl Muramic Acids To Probe Bacterial Cell Wall Recycling and Biosynthesis. J. Am. Chem. Soc., 2018, 140(30), 9458-9465.
[http://dx.doi.org/10.1021/jacs.8b03304] [PMID: 29986130]
[108]
Crump, G.M.; Zhou, J.; Mashayekh, S.; Grimes, C.L. Revisiting peptidoglycan sensing: interactions with host immunity and beyond. Chem. Commun., 2020, 56(87), 13313-13322.
[http://dx.doi.org/10.1039/D0CC02605K]

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