L-Rhamnosylation of Wall Teichoic Acids Promotes Resistance to Antimicrobial Peptides by Delaying Interaction with the Membrane

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Listeria monocytogenes is a foodborne bacterial pathogen that preferentially infects immunocompromised hosts, eliciting a severe and often lethal disease. In humans, clinical manifestations range from asymptomatic intestinal carriage and gastroenteritis to harsher systemic states of the disease such as sepsis, meningitis or encephalitis, and fetal infections. The surface of L. monocytogenes is decorated with wall teichoic acids (WTAs), a class of carbohydrate-based polymers that contributes to cell surface-related events with implications in physiological processes, such as bacterial division or resistance to antimicrobial peptides (AMPs). The addition of other molecules to the backbone of WTAs modulates their chemical properties and consequently their functionality. In this context, we studied the role of WTA tailoring mechanisms in L. monocytogenes, whose WTAs are strictly decorated with monosaccharides. For the first time, we link WTA glycosylation with AMP resistance by showing that the decoration of L. monocytogenes WTAs with l-rhamnose confers resistance to host defense peptides. We suggest that this resistance is based on changes in the permeability of the cell wall that delay its crossing by AMPs and therefore promote the protection of the bacterial membrane integrity. Importantly, we also demonstrate the significance of this WTA modification in L. monocytogenes virulence.

Vyšlo v časopise: L-Rhamnosylation of Wall Teichoic Acids Promotes Resistance to Antimicrobial Peptides by Delaying Interaction with the Membrane. PLoS Pathog 11(5): e32767. doi:10.1371/journal.ppat.1004919
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004919

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1. Swaminathan B, Gerner-Smidt P. The epidemiology of human listeriosis. Microbes and Infection. 2007;9 : 1236–43. doi: 10.1016/j.micinf.2007.05.011 1906370.

2. Cossart P, Toledo-Arana A. Listeria monocytogenes, a unique model in infection biology: an overview. Microbes and infection / Institut Pasteur. 2008;10 : 1041–50. doi: 10.1016/j.micinf.2008.07.043 18775788.

3. Camejo A, Carvalho F, Reis O, Leitão E, Sousa S, Cabanes D. The arsenal of virulence factors deployed by Listeria monocytogenes to promote its cell infection cycle. Virulence. 2011;2 : 379–94. doi: 10.4161/viru.2.5.17703 21921683.

4. Carvalho F, Sousa S, Cabanes D. How Listeria monocytogenes organizes its surface for virulence. Frontiers in cellular and infection microbiology. 2014;4 : 48. doi: 10.3389/fcimb.2014.00048 24809022.

5. Fiedler F, Seger J, Schrettenbrunner A, Seeliger H. The biochemistry of murein and cell wall teichoic acids in the genus Listeria. Systematic and Applied Microbiology. 1984;5 : 360–76. doi: 10.1016/S0723-2020(84)80038-7

6. Fiedler F. Biochemistry of the cell surface of Listeria strains: a locating general view. Infection. 1988;16 Suppl 2:S92–7. 3417357.

7. Uchikawa K-i, Sekikawa I, Azuma I. Structural studies on lipoteichoic acids from four Listeria strains. Journal of bacteriology. 1986;168 : 115–22. 3093460.

8. Ruhland GJ, Fiedler F. Occurrence and biochemistry of lipoteichoic acids in the genus Listeria. Systematic and Applied Microbiology. 1987;9 : 40–6. doi: 10.1016/S0723-2020(87)80054-1

9. Weidenmaier C, Peschel A. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nature reviews Microbiology. 2008;6 : 276–87. doi: 10.1038/nrmicro1861 18327271.

10. Uchikawa K, Sekikawa I, Azuma I. Structural studies on teichoic acids in cell walls of several serotypes of Listeria monocytogenes. Journal of biochemistry. 1986;99 : 315–27. 3084460.

11. Marquis RE, Mayzel K, Carstensen EL. Cation exchange in cell walls of gram-positive bacteria. Canadian journal of microbiology. 1976;22 : 975–82. 822931.

12. Peschel A, Vuong C, Otto M, Götz F. The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrobial agents and chemotherapy. 2000;44 : 2845–7. doi: 10.1128/AAC.44.10.2845-2847.2000.Updated 10991869.

13. Schirner K, Marles-Wright J, Lewis RJ, Errington J. Distinct and essential morphogenic functions for wall -⁠ and lipo-teichoic acids in Bacillus subtilis. The EMBO journal. 2009;28 : 830–42. doi: 10.1038/emboj.2009.25 19229300.

14. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, Götz F. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. The Journal of Biological Chemistry. 1999;274 : 8405–10. doi: 10.1074/jbc.274.13.8405 10085071.

15. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, Gross M, et al. Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nature medicine. 2004;10 : 243–5. doi: 10.1038/nm991 14758355.

16. Weidenmaier C, Peschel A, Xiong Y-Q, Kristian Sa, Dietz K, Yeaman MR, et al. Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. The Journal of infectious diseases. 2005;191 : 1771–7. doi: 10.1086/429692 15838806.

17. Cederlund A, Gudmundsson GH, Agerberth B. Antimicrobial peptides important in innate immunity. The FEBS journal. 2011;278 : 3942–51. doi: 10.1111/j.1742-4658.2011.08302.x 21848912.

18. Peters BM, Shirtliff ME, Jabra-Rizk MA. Antimicrobial peptides: primeval molecules or future drugs? PLoS pathogens. 2010;6:e1001067. doi: 10.1371/journal.ppat.1001067 21060861.

19. Brogden Ka. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nature reviews Microbiology. 2005;3 : 238–50. doi: 10.1038/nrmicro1098 15703760.

20. Peschel A, Sahl H-G. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nature reviews Microbiology. 2006;4 : 529–36. doi: 10.1038/nrmicro1441 16778838.

21. Koprivnjak T, Peschel A. Bacterial resistance mechanisms against host defense peptides. Cellular and molecular life sciences: CMLS. 2011;68 : 2243–54. doi: 10.1007/s00018-011-0716-4 21560069.

22. Neuhaus FC, Baddiley J. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiology and molecular biology reviews: MMBR. 2003;67 : 686–723. doi: 10.1128/MMBR.67.4.686 14665680.

23. Koprivnjak T, Peschel A, Gelb MH, Liang NS, Weiss JP. Role of charge properties of bacterial envelope in bactericidal action of human group IIA phospholipase A2 against Staphylococcus aureus. The Journal of biological chemistry. 2002;277 : 47636–44. doi: 10.1074/jbc.M205104200 12359734.

24. Camejo A, Buchrieser C, Couvé E, Carvalho F, Reis O, Ferreira P, et al. In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathogens. 2009;5:e1000449. doi: 10.1371/journal.ppat.1000449 19478867.

25. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, Balestrino D, et al. The Listeria transcriptional landscape from saprophytism to virulence. Nature. 2009;459 : 950–6. doi: 10.1038/nature08080 19448609.

26. Doumith M, Cazalet C, Simoes N, Frangeul L, Jacquet C, Kunst F, et al. New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays. Infection and immunity. 2004;72 : 1072–83. doi: 10.1128/IAI.72.2.1072 14742555.

27. Li Q, Reeves PR. Genetic variation of dTDP-L-rhamnose pathway genes in Salmonella enterica. Microbiology. 2000;146 (Pt 9):2291–307. 10974117.

28. Macpherson DF, Manning PA, Morona R. Characterization of the dTDP-rhamnose biosynthetic genes encoded in the rfb locus of Shigella flexneri. Molecular microbiology. 1994;11 : 281–92. 8170390.

29. Li Q, Hobbs M, Reeves PR. The variation of dTDP-L-rhamnose pathway genes in Vibrio cholerae. Microbiology (Reading, England). 2003;149 : 2463–74. doi: 10.1099/mic.0.26382-0 12949172.

30. Aguirre-Ramírez M, Medina G, González-Valdez A, Grosso-Becerra V, Soberón-Chávez G. The Pseudomonas aeruginosa rmlBDAC operon, encoding dTDP-L-rhamnose biosynthetic enzymes, is regulated by the quorum-sensing transcriptional regulator RhlR and the alternative sigma factor σS. Microbiology (Reading, England). 2012;158 : 908–16. doi: 10.1099/mic.0.054726-0 22262098.

31. Li W, Xin Y, McNeil MR, Ma Y. rmlB and rmlC genes are essential for growth of mycobacteria. Biochemical and biophysical research communications. 2006;342 : 170–8. doi: 10.1016/j.bbrc.2006.01.130 16472764.

32. Tsukioka Y, Yamashita Y, Oho T, Nakano Y, Koga T. Biological function of the dTDP-rhamnose synthesis pathway in Streptococcus mutans. Journal of bacteriology. 1997;179 : 1126–34. 9023194.

33. Zayni S, Steiner K, Pföstl A, Hofinger A, Kosma P, Schäffer C, et al. The dTDP-4-dehydro-6-deoxyglucose reductase encoding fcd gene is part of the surface layer glycoprotein glycosylation gene cluster of Geobacillus tepidamans GS5-97T. Glycobiology. 2007;17 : 433–43. doi: 10.1093/glycob/cwl084 17202151.

34. Péant B, LaPointe G, Gilbert C, Atlan D, Ward P, Roy D. Comparative analysis of the exopolysaccharide biosynthesis gene clusters from four strains of Lactobacillus rhamnosus. Microbiology (Reading, England). 2005;151 : 1839–51. doi: 10.1099/mic.0.27852-0 15941992.

35. Giraud MF, Naismith JH. The rhamnose pathway. Current opinion in structural biology. 2000;10 : 687–96. 11114506.

36. Eugster MR, Loessner MJ. Wall teichoic acids restrict access of bacteriophage endolysin Ply118, Ply511, and PlyP40 cell wall binding domains to the Listeria monocytogenes peptidoglycan. Journal of bacteriology. 2012;194 : 6498–506. doi: 10.1128/JB.00808-12 23002226.

37. Atilano ML, Pereira PM, Yates J, Reed P, Veiga H, Pinho MG, et al. Teichoic acids are temporal and spatial regulators of peptidoglycan cross-linking in Staphylococcus aureus. Proceedings of the National Academy of Sciences of the United States of America. 2010;107 : 18991–6. doi: 10.1073/pnas.1004304107 20944066.

38. Freymond P-P, Lazarevic V, Soldo B, Karamata D. Poly(glucosyl-N-acetylgalactosamine 1-phosphate), a wall teichoic acid of Bacillus subtilis 168: its biosynthetic pathway and mode of attachment to peptidoglycan. Microbiology (Reading, England). 2006;152 : 1709–18. doi: 10.1099/mic.0.28814-0 16735734.

39. Breton C, Snajdrová L, Jeanneau C, Koca J, Imberty A. Structures and mechanisms of glycosyltransferases. Glycobiology. 2006;16 : 29R–37R. doi: 10.1093/glycob/cwj016 16037492.

40. Chassaing D, Auvray F. The lmo1078 gene encoding a putative UDP-glucose pyrophosphorylase is involved in growth of Listeria monocytogenes at low temperature. FEMS microbiology letters. 2007;275 : 31–7. doi: 10.1111/j.1574-6968.2007.00840.x 17666069.

41. Bera A, Biswas R, Herbert S, Kulauzovic E, Weidenmaier C, Peschel A, et al. Influence of wall teichoic acid on lysozyme resistance in Staphylococcus aureus. Journal of bacteriology. 2007;189 : 280–3. doi: 10.1128/JB.01221-06 17085565.

42. Boneca IG, Dussurget O, Cabanes D, Nahori M-A, Sousa S, Lecuit M, et al. A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proceedings of the National Academy of Sciences of the United States of America. 2007;104 : 997–1002. doi: 10.1073/pnas.0609672104 17215377.

43. Kovacs M, Halfmann A, Fedtke I, Heintz M, Peschel A, Vollmer W, et al. A Functional dlt Operon, Encoding Proteins Required for Incorporation of D-Alanine in Teichoic Acids in Gram-Positive Bacteria, Confers Resistance to Cationic Antimicrobial Peptides in Streptococcus pneumoniae. Journal of Bacteriology. 2006;188 : 5797–805. doi: 10.1128/JB.00336-06 16885447.

44. Kellner R, Jung G, Hörner T, Zähner H, Schnell N, Entian KD, et al. Gallidermin: a new lanthionine-containing polypeptide antibiotic. European journal of biochemistry / FEBS. 1988;177 : 53–9. 3181159.

45. Gallo RL, Kim KJ, Bernfield M, Kozak Ca, Zanetti M, Merluzzi L, et al. Identification of CRAMP, a cathelin-related antimicrobial peptide expressed in the embryonic and adult mouse. The Journal of biological chemistry. 1997;272 : 13088–93. 9148921.

46. Vandamme D, Landuyt B, Luyten W, Schoofs L. A comprehensive summary of LL-37, the factoctum human cathelicidin peptide. Cellular immunology. 2012;280 : 22–35. doi: 10.1016/j.cellimm.2012.11.009 23246832.

47. Abachin E, Poyart C, Pellegrini E, Milohanic E, Fiedler F, Berche P, et al. Formation of D-alanyl-lipoteichoic acid is required for adhesion and virulence of Listeria monocytogenes. Molecular microbiology. 2002;43 : 1–14. 11849532.

48. Shapiro HM. Membrane potential estimation by flow cytometry. Methods (San Diego, Calif). 2000;21 : 271–9. doi: 10.1006/meth.2000.1007 10873481.

49. Nizet V, Ohtake T, Lauth X, Trowbridge J, Rudisill J, Dorschner Ra, et al. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature. 2001;414 : 454–7. doi: 10.1038/35106587 11719807.

50. Frirdich E, Whitfield C. Lipopolysaccharide inner core oligosaccharide structure and outer membrane stability in human pathogens belonging to the Enterobacteriaceae. Journal of endotoxin research. 2005;11 : 133–44. doi: 10.1179/096805105X46592 15949142.

51. Chatterjee D. The mycobacterial cell wall: structure, biosynthesis and sites of drug action. Current opinion in chemical biology. 1997;1 : 579–88. 9667898.

52. Lairson LL, Henrissat B, Davies GJ, Withers SG. Glycosyltransferases: structures, functions, and mechanisms. Annual review of biochemistry. 2008;77 : 521–55. doi: 10.1146/annurev.biochem.76.061005.092322 18518825.

53. Brown S, Xia G, Luhachack LG, Campbell J, Meredith TC, Chen C, et al. Methicillin resistance in Staphylococcus aureus requires glycosylated wall teichoic acids. Proceedings of the National Academy of Sciences of the United States of America. 2012;109 : 18909–14. doi: 10.1073/pnas.1209126109 23027967.

54. Guilhelmelli F, Vilela N, Albuquerque P, Derengowski LDS, Silva-Pereira I, Kyaw CM. Antibiotic development challenges: the various mechanisms of action of antimicrobial peptides and of bacterial resistance. Frontiers in microbiology. 2013;4 : 353. doi: 10.3389/fmicb.2013.00353 24367355.

55. Nguyen LT, Haney EF, Vogel HJ. The expanding scope of antimicrobial peptide structures and their modes of action. Trends in biotechnology. 2011;29 : 464–72. doi: 10.1016/j.tibtech.2011.05.001 21680034.

56. Vadyvaloo V, Arous S, Gravesen A, Héchard Y, Chauhan-Haubrock R, Hastings JW, et al. Cell-surface alterations in class IIa bacteriocin-resistant Listeria monocytogenes strains. Microbiology (Reading, England). 2004;150 : 3025–33. doi: 10.1099/mic.0.27059-0 15347760.

57. Saar-Dover R, Bitler A, Nezer R, Shmuel-Galia L, Firon A, Shimoni E, et al. D-alanylation of lipoteichoic acids confers resistance to cationic peptides in group B streptococcus by increasing the cell wall density. PLoS pathogens. 2012;8:e1002891. doi: 10.1371/journal.ppat.1002891 22969424.

58. Faith N, Kathariou S, Cheng Y, Promadej N, Neudeck BL, Zhang Q, et al. The role of L. monocytogenes serotype 4b gtcA in gastrointestinal listeriosis in A/J mice. Foodborne pathogens and disease. 2009;6 : 39–48. doi: 10.1089/fpd.2008.0154 18991548.

59. Promadej N, Fiedler F, Cossart P, Dramsi S, Kathariou S. Cell wall teichoic acid glycosylation in Listeria monocytogenes serotype 4b requires gtcA, a novel, serogroup-specific gene. Journal of bacteriology. 1999;181 : 418–25. 9882654.

60. Eugster MR, Haug MC, Huwiler SG, Loessner MJ. The cell wall binding domain of Listeria bacteriophage endolysin PlyP35 recognizes terminal GlcNAc residues in cell wall teichoic acid. Molecular microbiology. 2011;81 : 1419–32. doi: 10.1111/j.1365-2958.2011.07774.x 21790805.

61. Autret N, Dubail I, Trieu-Cuot P, Berche P, Charbit A. Identification of new genes involved in the virulence of Listeria monocytogenes by signature-tagged transposon mutagenesis. Infection and immunity. 2001;69 : 2054–65. doi: 10.1128/IAI.69.4.2054-2065.2001 11254558.

62. Huang LC, Reins RY, Gallo RL, McDermott AM. Cathelicidin-deficient (Cnlp-/-) mice show increased susceptibility to Pseudomonas aeruginosa keratitis. Investigative ophthalmology & visual science. 2007;48 : 4498–508. doi: 10.1167/iovs.07-0274 17898271.

63. Chromek M, Arvidsson I, Karpman D. The antimicrobial peptide cathelicidin protects mice from Escherichia coli O157:H7-mediated disease. PloS one. 2012;7:e46476. doi: 10.1371/journal.pone.0046476 23077510.

64. Ménard S, Förster V, Lotz M, Gütle D, Duerr CU, Gallo RL, et al. Developmental switch of intestinal antimicrobial peptide expression. The Journal of experimental medicine. 2008;205 : 183–93. doi: 10.1084/jem.20071022 18180308.

65. Rosenberger CM, Gallo RL, Finlay BB. Interplay between antibacterial effectors: a macrophage antimicrobial peptide impairs intracellular Salmonella replication. Proceedings of the National Academy of Sciences of the United States of America. 2004;101 : 2422–7. 14983025.

66. Arnaud M, Chastanet A, Débarbouillé M. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Applied and environmental microbiology. 2004;70 : 6887–91. doi: 10.1128/AEM.70.11.6887-6891.2004 15528558.

67. Lauer P, Chow MYN, Loessner MJ, Portnoy DA, Calendar R. Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. Journal of bacteriology. 2002;184 : 4177–86. doi: 10.1128/JB.184.15.4177 12107135.

68. Milohanic E, Glaser P, Coppée J-Y, Frangeul L, Vega Y, Vázquez-Boland Ja, et al. Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Molecular microbiology. 2003;47 : 1613–25. 12622816.

69. Carvalho F, Pucciarelli MG, Portillo FG-d, Cabanes D, Cossart P. Extraction of cell wall-bound teichoic acids and surface proteins from Listeria monocytogenes. In: Delcour AH, editor. Methods in molecular biology (Clifton, NJ). Totowa, NJ: Humana Press; 2013. p. 289–308.

70. Filipe SR, Tomasz A, Ligoxygakis P. Requirements of peptidoglycan structure that allow detection by the Drosophila Toll pathway. EMBO reports. 2005;6 : 327–33. doi: 10.1038/sj.embor.7400371 15791270.

71. Hayashi K. A rapid determination of sodium dodecyl sulfate with methylene blue. Analytical biochemistry. 1975;67 : 503–6. 1163770.

72. Ornelas-Soares A, de Lencastre H, de Jonge BL, Tomasz A. Reduced methicillin resistance in a new Staphylococcus aureus transposon mutant that incorporates muramyl dipeptides into the cell wall peptidoglycan. The Journal of Biological Chemistry. 1994;269(44):27246–50. Epub 1994/11/04. 7961632.

73. Blanot S, Boumaila C, Berche P. Intracerebral activity of antibiotics against Listeria monocytogenes during experimental rhombencephalitis. The Journal of antimicrobial chemotherapy. 1999;44(4):565–8. Epub 1999/12/10. 10588323.

74. de Jonge BL, Chang YS, Gage D, Tomasz A. Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. The role of penicillin binding protein 2A. The Journal of biological chemistry. 1992;267 : 11248–54. 1597460.

75. Novo D, Perlmutter NG, Hunt RH, Shapiro HM. Accurate flow cytometric membrane potential measurement in bacteria using diethyloxacarbocyanine and a ratiometric technique. Cytometry. 1999;35 : 55–63. 10554181.

76. Cabanes D, Lecuit M, Cossart P. Animal models of Listeria infection. Current protocols in microbiology. 2008;Chapter 9:Unit9B.1. doi: 10.1002/9780471729259.mc09b01s10 18729060.

77. Simon R, Priefer U, Pühler A. A Broad Host Range Mobilization System for In Vivo Genetic Engineering: Transposon Mutagenesis in Gram Negative Bacteria. Bio/Technology. 1983;1 : 784–91. doi: 10.1038/nbt1183-784

78. Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, Baquero F, et al. Comparative genomics of Listeria species. Science (New York, NY). 2001;294 : 849–52. doi: 10.1126/science.1063447 11679669.

79. Murray EGD, Webb RA, Swann MBR. A disease of Rabbits characterised by a large mononuclear Leucocytosis, caused by a hitherto undescribed bacillus Bacterium monocytogenes. The Journal of Pathology and Bacteriology. 1926;29 : 407–39. doi: 10.1002/path.1700290409 188406400008.

80. Mandin P, Fsihi H, Dussurget O, Vergassola M, Milohanic E, Toledo-Arana A, et al. VirR, a response regulator critical for Listeria monocytogenes virulence. Molecular microbiology. 2005;57 : 1367–80. doi: 10.1111/j.1365-2958.2005.04776.x 16102006.