Listeria monocytogenes wall teichoic acid decoration in virulence and cell‐to‐cell spread

Spears, Patricia A.; Havell, Edward A.; Hamrick, Terri S.; Goforth, John B.; Levine, Alexandra L.; Abraham, S. Thomas; Heiss, Christian; Azadi, Parastoo; Orndorff, Paul E.

doi:10.1111/mmi.13353

Title: Listeria monocytogenes wall teichoic acid decoration in virulence and cell‐to‐cell spread

Journal Article · Thu Mar 10 00:00:00 EST 2016 · Molecular Microbiology

DOI:https://doi.org/10.1111/mmi.13353· OSTI ID:1400545

Spears, Patricia A. ^[1]; Havell, Edward A. ^[1]; Hamrick, Terri S. ^[2]; Goforth, John B. ^[2]; Levine, Alexandra L. ^[2]; Abraham, S. Thomas ^[3]; Heiss, Christian ^[4]; Azadi, Parastoo ^[4]; Orndorff, Paul E. ^[1]

Department of Population Health and Pathobiology, College of Veterinary Medicine North Carolina State University Raleigh NC 27606 USA
Department of Microbiology and Immunology, School of Osteopathic Medicine Campbell University Buies Creek NC 27506 USA
Department of Pharmaceutical Sciences, College of Pharmacy &, Health Sciences Campbell University Buies Creek NC 27506 USA
Complex Carbohydrate Research Center, The University of Georgia Athens GA 30602 USA

Summary Wall teichoic acid (WTA) comprises a class of glycopolymers covalently attached to the peptidoglycan of gram positive bacteria. In Listeria monocytogenes , mutations that prevent addition of certain WTA decorating sugars are attenuating. However, the steps required for decoration and the pathogenic process interrupted are not well described. We systematically examined the requirement for WTA galactosylation in a mouse oral‐virulent strain by first creating mutations in four genes whose products conferred resistance to a WTA‐binding bacteriophage. WTA biochemical and structural studies indicated that galactosylated WTA was directly required for bacteriophage adsorption and that mutant WTA lacked appreciable galactose in all except one mutant – which retained a level ca. 7% of the parent. All mutants were profoundly attenuated in orally infected mice and were impaired in cell‐to‐cell spread in vitro. Confocal microscopy of cytosolic mutants revealed that all expressed ActA on their cell surface and formed actin tails with a frequency similar to the parent. However, the mutant tails were significantly shorter – suggesting a defect in actin based motility. Roles for the gene products in WTA galactosylation are proposed. Identification and interruption of WTA decoration pathways may provide a general strategy to discover non‐antibiotic therapeutics for gram positive infections. © 2016 John Wiley & Sons Ltd

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: DE‐FG02‐93ER20097

OSTI ID:: 1400545

Journal Information:: Molecular Microbiology, Journal Name: Molecular Microbiology Vol. 101 Journal Issue: 5; ISSN 0950-382X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: FAO

Language:: English

Citation Metrics:

Cited by: 20 works

Citation information provided by
Web of Science

References (55)

A UDP glucosyltransferase from Bacillus subtilis successively transfers up to four glucose residues to 1,2‐diacylglycerol: expression of ypfP in Escherichia coli and structural analysis of its reaction products Jorasch, Petra; Wolter, Frank P.; Zähringer, Ulrich Molecular Microbiology, Vol. 29, Issue 2 https://doi.org/10.1046/j.1365-2958.1998.00930.x	journal	July 1998
Characterization of a novel linkage unit between ribitol teichoic acid and peptidoglycan in Listeria monocytogenes cell walls Kaya, Shunji; Araki, Yoshio; Ito, Eiji European Journal of Biochemistry, Vol. 146, Issue 3 https://doi.org/10.1111/j.1432-1033.1985.tb08682.x	journal	February 1985
Anti-biofilm agents: recent breakthrough against multi-drug resistant Staphylococcus aureus Chung, Pooi Y.; Toh, Yien S. Pathogens and Disease, Vol. 70, Issue 3 https://doi.org/10.1111/2049-632X.12141	journal	February 2014
The cell wall binding domain of Listeria bacteriophage endolysin PlyP35 recognizes terminal GlcNAc residues in cell wall teichoic acid: GlcNAc is the binding ligand for Listeria phage endolysin PlyP35 Eugster, Marcel R.; Haug, Martina C.; Huwiler, Simona G. Molecular Microbiology, Vol. 81, Issue 6 https://doi.org/10.1111/j.1365-2958.2011.07774.x	journal	August 2011
Functional analysis of the O antigen glucosylation gene cluster of Shigella flexneri bacteriophage SfX Guan, S.; Bastin, D. A.; Verma, N. K. Microbiology, Vol. 145, Issue 5 https://doi.org/10.1099/13500872-145-5-1263	journal	May 1999
Studies of the Genetics, Function, and Kinetic Mechanism of TagE, the Wall Teichoic Acid Glycosyltransferase in Bacillus subtilis 168 Allison, Sarah E.; D'Elia, Michael A.; Arar, Sharif Journal of Biological Chemistry, Vol. 286, Issue 27 https://doi.org/10.1074/jbc.M111.241265	journal	May 2011
Wall Teichoic Acid Glycosylation Governs Staphylococcus aureus Nasal Colonization Winstel, Volker; Kühner, Petra; Salomon, Ferdinand mBio, Vol. 6, Issue 4 https://doi.org/10.1128/mBio.00632-15	journal	June 2015
L-Rhamnosylation of Listeria monocytogenes Wall Teichoic Acids Promotes Resistance to Antimicrobial Peptides by Delaying Interaction with the Membrane Carvalho, Filipe; Atilano, Magda L.; Pombinho, Rita PLOS Pathogens, Vol. 11, Issue 5 https://doi.org/10.1371/journal.ppat.1004919	journal	May 2015
Optimization of Virulence Functions Through Glucosylation of Shigella LPS West, N. P. Science, Vol. 307, Issue 5713 https://doi.org/10.1126/science.1108472	journal	February 2005
Genes Required for Glycolipid Synthesis and Lipoteichoic Acid Anchoring in Staphylococcus aureus Grundling, A.; Schneewind, O. Journal of Bacteriology, Vol. 189, Issue 6 https://doi.org/10.1128/JB.01683-06	journal	January 2007
A Listeria monocytogenes Mutant Defective in Bacteriophage Attachment Is Attenuated in Orally Inoculated Mice and Impaired in Enterocyte Intracellular Growth Spears, P. A.; Suyemoto, M. M.; Palermo, A. M. Infection and Immunity, Vol. 76, Issue 9 https://doi.org/10.1128/IAI.00283-08	journal	June 2008
Glycosylation of Wall Teichoic Acid in Staphylococcus aureus by TarM Xia, Guoqing; Maier, Lisa; Sanchez-Carballo, Patricia Journal of Biological Chemistry, Vol. 285, Issue 18 https://doi.org/10.1074/jbc.M109.096172	journal	February 2010
Periodate oxidation of R36A pneumococci greatly enhances production of hybridomas secreting anti-protein antibodies Casal, Julio; Jado, Isabel; Fenoll, Asunción Microbial Pathogenesis, Vol. 24, Issue 2 https://doi.org/10.1006/mpat.1997.0175	journal	February 1998
New Aspects Regarding Evolution and Virulence of Listeria monocytogenes Revealed by Comparative Genomics and DNA Arrays Doumith, M.; Cazalet, C.; Simoes, N. Infection and Immunity, Vol. 72, Issue 2 https://doi.org/10.1128/IAI.72.2.1072-1083.2004	journal	January 2004
L isteria monocytogenes exopolysaccharide: origin, structure, biosynthetic machinery and c-di-GMP-dependent regulation Köseoğlu, Volkan K.; Heiss, Christian; Azadi, Parastoo Molecular Microbiology, Vol. 96, Issue 4 https://doi.org/10.1111/mmi.12966	journal	March 2015
Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species Nelson, K. E. Nucleic Acids Research, Vol. 32, Issue 8 https://doi.org/10.1093/nar/gkh562	journal	April 2004
In Vitro Properties of a Listeria monocytogenes Bacteriophage-Resistant Mutant Predict Its Efficacy as a Live Oral Vaccine Strain Spears, Patricia A.; Suyemoto, M. Mitsu; Hamrick, Terri S. Infection and Immunity, Vol. 79, Issue 12 https://doi.org/10.1128/IAI.05700-11	journal	September 2011
Lipoteichoic Acids, Phosphate-Containing Polymers in the Envelope of Gram-Positive Bacteria Schneewind, O.; Missiakas, D. Journal of Bacteriology, Vol. 196, Issue 6 https://doi.org/10.1128/JB.01155-13	journal	January 2014
Targeting virulence: a new paradigm for antimicrobial therapy Clatworthy, Anne E.; Pierson, Emily; Hung, Deborah T. Nature Chemical Biology, Vol. 3, Issue 9 https://doi.org/10.1038/nchembio.2007.24	journal	August 2007
Identification of critical residues of the serotype modifying O-acetyltransferase of Shigella flexneri Thanweer, Farzaana; Verma, Naresh K. BMC Biochemistry, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2091-13-13	journal	January 2012
‘Form variation’ of the O12 antigen is critical for persistence of Salmonella Typhimurium in the murine intestine Bogomolnaya, Lydia M.; Santiviago, Carlos A.; Yang, Hee-Jeong Molecular Microbiology, Vol. 70, Issue 5 https://doi.org/10.1111/j.1365-2958.2008.06461.x	journal	December 2008
Phage Receptors in Gram-positive Bacteria Archibald, A. R. Virus Receptors https://doi.org/10.1007/978-94-011-6918-9_2	book	January 1980
Teichoic Acid Glycosylation Mediated by gtcA Is Required for Phage Adsorption and Susceptibility of Listeria monocytogenes Serotype 4b Cheng, Y.; Promadej, N.; Kim, J. -W. Applied and Environmental Microbiology, Vol. 74, Issue 5 https://doi.org/10.1128/AEM.01773-07	journal	January 2008
Reticulum Cell Sarcoma: An Effector Cell in Antibody-Dependent Cell-Mediated Immunity Ralph, Peter; Prichard, John; Cohn, Melvin The Journal of Immunology, Vol. 114, Issue 2_Part_2 https://doi.org/10.4049/jimmunol.114.2_Part_2.898	journal	February 1975
Anti-virulence strategies to combat bacteria-mediated disease Rasko, David A.; Sperandio, Vanessa Nature Reviews Drug Discovery, Vol. 9, Issue 2 https://doi.org/10.1038/nrd3013	journal	January 2010
The Sweet Tooth of Bacteria: Common Themes in Bacterial Glycoconjugates Tytgat, H. L. P.; Lebeer, S. Microbiology and Molecular Biology Reviews, Vol. 78, Issue 3 https://doi.org/10.1128/MMBR.00007-14	journal	September 2014
Morphotypic Conversion in Listeria monocytogenes Biofilm Formation: Biological Significance of Rough Colony Isolates Monk, I. R.; Cook, G. M.; Monk, B. C. Applied and Environmental Microbiology, Vol. 70, Issue 11 https://doi.org/10.1128/AEM.70.11.6686-6694.2004	journal	November 2004
Identification of New Genes Involved in the Virulence of Listeria monocytogenes by Signature-Tagged Transposon Mutagenesis Autret, N.; Dubail, I.; Trieu-Cuot, P. Infection and Immunity, Vol. 69, Issue 4 https://doi.org/10.1128/IAI.69.4.2054-2065.2001	journal	April 2001
UTP: alpha-D-glucose-1-phosphate uridylyltransferase of Escherichia coli: isolation and DNA sequence of the galU gene and purification of the enzyme. Weissborn, A. C.; Liu, Q.; Rumley, M. K. Journal of Bacteriology, Vol. 176, Issue 9 https://doi.org/10.1128/jb.176.9.2611-2618.1994	journal	May 1994
The Role of L. monocytogenes Serotype 4b gtc A in Gastrointestinal Listeriosis in A/J Mice Faith, Nancy; Kathariou, Sophia; Cheng, Ying Foodborne Pathogens and Disease, Vol. 6, Issue 1 https://doi.org/10.1089/fpd.2008.0154	journal	February 2009
Examination of Listeria monocytogenes Intracellular Gene Expression by Using the Green Fluorescent Protein ofAequorea victoria Freitag, Nancy E.; Jacobs, Kathleen E. Infection and Immunity, Vol. 67, Issue 4 https://doi.org/10.1128/IAI.67.4.1844-1852.1999	journal	April 1999
Immortalization of mouse intestinal epithelial cells by the SV40-large T gene Vidal, Karine; Grosjean, Isabelle; Revillard, Jean-Pierre Journal of Immunological Methods, Vol. 166, Issue 1 https://doi.org/10.1016/0022-1759(93)90329-6	journal	November 1993
Bacteriophage predation promotes serovar diversification in L isteria monocytogenes : Bacteriophage influences Eugster, Marcel R.; Morax, Laurent S.; Hüls, Vanessa J. Molecular Microbiology, Vol. 97, Issue 1 https://doi.org/10.1111/mmi.13009	journal	April 2015
Polarized distribution of Listeria monocytogenes surface protein ActA at the site of directional actin assembly Kocks, C.; Hellio, R.; Gounon, P. Journal of Cell Science, Vol. 105, Issue 3 https://doi.org/10.1242/jcs.105.3.699	journal	July 1993
Listeria monocytogenes intragastric and intraperitoneal approximate 50% lethal doses for mice are comparable, but death occurs earlier by intragastric feeding. Pine, L.; Malcolm, G. B.; Plikaytis, B. D. Infection and Immunity, Vol. 58, Issue 9 https://doi.org/10.1128/iai.58.9.2940-2945.1990	journal	January 1990
Listeria monocytogenes, a food-borne pathogen. Farber, J. M.; Peterkin, P. I. Microbiological Reviews, Vol. 55, Issue 3 https://doi.org/10.1128/MMBR.55.3.476-511.1991	journal	January 1991
Biochemistry of the cell surface of Listeria strains: A locating general view Fiedler, F. Infection, Vol. 16, Issue S2 https://doi.org/10.1007/BF01639729	journal	March 1988
Characterization of Vibrio cholerae O1 El Tor galU and galE Mutants: Influence on Lipopolysaccharide Structure, Colonization, and Biofilm Formation Nesper, J.; Lauriano, C. M.; Klose, K. E. Infection and Immunity, Vol. 69, Issue 1 https://doi.org/10.1128/IAI.69.1.435-445.2001	journal	January 2001
Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri Allison, Gwen E.; Verma, Naresh K. Trends in Microbiology, Vol. 8, Issue 1, p. 17-23 https://doi.org/10.1016/S0966-842X(99)01646-7	journal	January 2000
The lmo1078 gene encoding a putative UDP-glucose pyrophosphorylase is involved in growth of Listeria monocytogenes at low temperature Chassaing, Danielle; Auvray, FrÃ©dÃ©ric FEMS Microbiology Letters, Vol. 275, Issue 1 https://doi.org/10.1111/j.1574-6968.2007.00840.x	journal	October 2007
Rapid Analysis of Listeria monocytogenes Cell Wall Teichoic Acid Carbohydrates by ESI-MS/MS Eugster, Marcel R.; Loessner, Martin J. PLoS ONE, Vol. 6, Issue 6 https://doi.org/10.1371/journal.pone.0021500	journal	June 2011
Adherence of a virulent strain of Listeria monocytogenes to the surface of a hepatocarcinoma cell line via lectin-substrate interaction Cowart, Richard E.; Lashmet, Jennifer; McIntosh, Margie E. Archives of Microbiology, Vol. 153, Issue 3 https://doi.org/10.1007/BF00249083	journal	February 1990
Structural Study on Teichoic Acids of Listeria monocytogenes Types 4a and 4d1 Fujii, Hideji; Kamisango, Kei-ichi; Nagaoka, Masato The Journal of Biochemistry, Vol. 97, Issue 3 https://doi.org/10.1093/oxfordjournals.jbchem.a135130	journal	March 1985
Structural Studies on Teichoic Acids in Cell Walls of Several Serotypes of Listeria monocytogenes1 Uchikawa, Keu-ichi; Sekiawa, Isao; Azuma, Ichiro The Journal of Biochemistry, Vol. 99, Issue 2 https://doi.org/10.1093/oxfordjournals.jbchem.a135486	journal	January 1986
Techniques Dykstra, Michael J.; Reuss, Laura E. Biological Electron Microscopy https://doi.org/10.1007/978-1-4419-9244-4_10	book	January 2003
Wall Teichoic Acids of Gram-Positive Bacteria Brown, Stephanie; Santa Maria, John P.; Walker, Suzanne Annual Review of Microbiology, Vol. 67, Issue 1 https://doi.org/10.1146/annurev-micro-092412-155620	journal	September 2013
Bacteriophage receptors on Listeria monocytogenes cells are the N-acetylglucosamine and rhamnose substituents of teichoic acids or the peptidoglycan itself Wendlinger, G.; Loessner, M. J.; Scherer, S. Microbiology, Vol. 142, Issue 4 https://doi.org/10.1099/00221287-142-4-985	journal	April 1996
Bacteriophage Receptors Lindberg, A. A. Annual Review of Microbiology, Vol. 27, Issue 1 https://doi.org/10.1146/annurev.mi.27.100173.001225	journal	October 1973
Cell Wall Teichoic Acid Glycosylation inListeria monocytogenes Serotype 4b Requires gtcA, a Novel, Serogroup-Specific Gene Promadej, N.; Fiedler, F.; Cossart, P. Journal of Bacteriology, Vol. 181, Issue 2 https://doi.org/10.1128/JB.181.2.418-425.1999	journal	January 1999
The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization Theriot, Julie A.; Mitchison, Timothy J.; Tilney, Lewis G. Nature, Vol. 357, Issue 6375 https://doi.org/10.1038/357257a0	journal	May 1992
Polyelectrolyte Nature of Bacterial Teichoic Acids Doyle, R. J.; McDannel, M. L.; Streips, U. N. Journal of Bacteriology, Vol. 118, Issue 2 https://doi.org/10.1128/jb.118.2.606-615.1974	journal	January 1974
Influence of Pregnancy on the Pathogenesis of Listeriosis in Mice Inoculated Intragastrically Hamrick, T. S.; Horton, J. R.; Spears, P. A. Infection and Immunity, Vol. 71, Issue 9 https://doi.org/10.1128/IAI.71.9.5202-5209.2003	journal	August 2003
Requirement of glucosylated teichoic acid for adsorption of phage in Bacillus subtilis 168. Young, F. E. Proceedings of the National Academy of Sciences, Vol. 58, Issue 6 https://doi.org/10.1073/pnas.58.6.2377	journal	December 1967
Phosphorus Assay in Column Chromatography Bartlett, Grant R. Journal of Biological Chemistry, Vol. 234, Issue 3 https://doi.org/10.1016/S0021-9258(18)70226-3	journal	March 1959
Methicillin resistance in Staphylococcus aureus requires glycosylated wall teichoic acids Brown, S.; Xia, G.; Luhachack, L. G. Proceedings of the National Academy of Sciences, Vol. 109, Issue 46 https://doi.org/10.1073/pnas.1209126109	journal	October 2012

Similar Records

Receptor binding proteins of Listeria monocytogenes bacteriophages A118 and P35 recognize serovar-specific teichoic acids

Journal Article · Sun Mar 15 00:00:00 EDT 2015 · Virology · OSTI ID:1400545

Bielmann, Regula; Habann, Matthias; Eugster, Marcel R.; +4 more

Structural insights into glutathione-mediated activation of the master regulator PrfA in Listeria monocytogenes

Journal Article · Tue Mar 07 00:00:00 EST 2017 · Protein & Cell · OSTI ID:1400545

Wang, Yong; Feng, Han; Zhu, Yalan; +1 more

Listeria monocytogenes virulence factors, including listeriolysin O, are secreted in biologically active extracellular vesicles

Journal Article · Tue Jan 01 00:00:00 EST 2019 · Journal of Biological Chemistry · OSTI ID:1400545

Coelho, Carolina; Brown, Lisa; Maryam, Maria; +13 more

Title: Listeria monocytogenes wall teichoic acid decoration in virulence and cell‐to‐cell spread

Citation Formats

References (55)

Similar Records

Related Subjects