Bacterial autolysins trim cell surface peptidoglycan to prevent detection by the drosophila innate immune system

Magda Luciana Atilano, Pedro Matos Pereira, Filipa Vaz, Maria João Catalão, Patricia Reed, Maria Inês Ramos Grilo, Rita Gonçalves Sobral de Almeida, Petros Ligoxygakis, Mariana Gomes Pinho, Sérgio Joaquim Raposo Filipe

Research output: Contribution to journalArticle

24 Citations (Scopus)
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Abstract

Bacteria have to avoid recognition by the host immune system in order to establish a successful infection. Peptidoglycan, the principal constituent of virtually all bacterial surfaces, is a specific molecular signature recognized by dedicated host receptors, present in animals and plants, which trigger an immune response. Here we report that autolysins from Gram-positive pathogenic bacteria, enzymes capable of hydrolyzing peptidoglycan, have a major role in concealing this inflammatory molecule from Drosophila peptidoglycan recognition proteins (PGRPs). We show that autolysins trim the outermost peptidoglycan fragments and that in their absence bacterial virulence is impaired, as PGRPs can directly recognize leftover peptidoglycan extending beyond the external layers of bacterial proteins and polysaccharides. The activity of autolysins is not restricted to the producer cells but can also alter the surface of neighboring bacteria, facilitating the survival of the entire population in the infected host.

Original languageEnglish
Article numbere02277
JournaleLife
Volume2014
Issue number3
DOIs
Publication statusPublished - 1 Apr 2014

Fingerprint

N-Acetylmuramoyl-L-alanine Amidase
Peptidoglycan
Immune system
Drosophila
Immune System
Bacteria
Bacterial Polysaccharides
Bacterial Proteins
Gram-Positive Bacteria
Virulence
Animals
Molecules
Enzymes
Infection
Population
peptidoglycan recognition protein

Keywords

  • Animals
  • Drosophila
  • Gram-Positive Bacteria
  • Hydrolysis
  • Immunity, Innate
  • N-Acetylmuramoyl-L-alanine Amidase
  • Peptidoglycan
  • Virulence

Cite this

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title = "Bacterial autolysins trim cell surface peptidoglycan to prevent detection by the drosophila innate immune system",
abstract = "Bacteria have to avoid recognition by the host immune system in order to establish a successful infection. Peptidoglycan, the principal constituent of virtually all bacterial surfaces, is a specific molecular signature recognized by dedicated host receptors, present in animals and plants, which trigger an immune response. Here we report that autolysins from Gram-positive pathogenic bacteria, enzymes capable of hydrolyzing peptidoglycan, have a major role in concealing this inflammatory molecule from Drosophila peptidoglycan recognition proteins (PGRPs). We show that autolysins trim the outermost peptidoglycan fragments and that in their absence bacterial virulence is impaired, as PGRPs can directly recognize leftover peptidoglycan extending beyond the external layers of bacterial proteins and polysaccharides. The activity of autolysins is not restricted to the producer cells but can also alter the surface of neighboring bacteria, facilitating the survival of the entire population in the infected host.",
keywords = "Animals , Drosophila , Gram-Positive Bacteria , Hydrolysis , Immunity, Innate , N-Acetylmuramoyl-L-alanine Amidase , Peptidoglycan , Virulence",
author = "Atilano, {Magda Luciana} and Pereira, {Pedro Matos} and Filipa Vaz and Catal{\~a}o, {Maria Jo{\~a}o} and Patricia Reed and Grilo, {Maria In{\^e}s Ramos} and Almeida, {Rita Gon{\cc}alves Sobral de} and Petros Ligoxygakis and Pinho, {Mariana Gomes} and Filipe, {S{\'e}rgio Joaquim Raposo}",
note = "Fundacao para a Ciencia e Tecnologia PTDC/SAU-IMU/111806/2009 Sergio Raposo Filipe Wellcome Trust WT087680 Petros Ligoxygakis European Research Council ERC-2012-StG-310987 Mariana Gomes Pinho Fundacao para a Ciencia e Tecnologia PTDC/BIA-MIC/111817/2009 Sergio Raposo Filipe Fundacao para a Ciencia e Tecnologia PTDC/BIA-BCM/099152/2008 Mariana Gomes Pinho Fundacao para a Ciencia e Tecnologia PTDC/BIA-MIC/101375/2008 Rita Goncalves Sobral Fundacao para a Ciencia e Tecnologia PEst-OE/EQB/LA0004/2011 Mariana Gomes Pinho, Sergio Raposo Filipe Fundacao para a Ciencia e Tecnologia Fellowship SFRH/BD/28440/2006 Magda Luciana Atilano Fundacao para a Ciencia e Tecnologia Fellowship SFRH/BD/41119/2007 Pedro Matos Pereira Fundacao para a Ciencia e Tecnologia Fellowship SFRH/BD/78748/2011 Filipa Vaz Fundacao para a Ciencia e Tecnologia Fellowship SFRH/BD/77758/2011 Maria Joao Catalao Fundacao para a Ciencia e Tecnologia Fellowship SFRH/BD/23812/2005 Patricia Reed Fundacao para a Ciencia e Tecnologia Fellowship SFRH/BD/70162/2010 Ines Ramos Grilo The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.",
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Bacterial autolysins trim cell surface peptidoglycan to prevent detection by the drosophila innate immune system. / Atilano, Magda Luciana; Pereira, Pedro Matos; Vaz, Filipa; Catalão, Maria João; Reed, Patricia; Grilo, Maria Inês Ramos; Almeida, Rita Gonçalves Sobral de; Ligoxygakis, Petros; Pinho, Mariana Gomes; Filipe, Sérgio Joaquim Raposo.

In: eLife, Vol. 2014, No. 3, e02277, 01.04.2014.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Bacterial autolysins trim cell surface peptidoglycan to prevent detection by the drosophila innate immune system

AU - Atilano, Magda Luciana

AU - Pereira, Pedro Matos

AU - Vaz, Filipa

AU - Catalão, Maria João

AU - Reed, Patricia

AU - Grilo, Maria Inês Ramos

AU - Almeida, Rita Gonçalves Sobral de

AU - Ligoxygakis, Petros

AU - Pinho, Mariana Gomes

AU - Filipe, Sérgio Joaquim Raposo

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PY - 2014/4/1

Y1 - 2014/4/1

N2 - Bacteria have to avoid recognition by the host immune system in order to establish a successful infection. Peptidoglycan, the principal constituent of virtually all bacterial surfaces, is a specific molecular signature recognized by dedicated host receptors, present in animals and plants, which trigger an immune response. Here we report that autolysins from Gram-positive pathogenic bacteria, enzymes capable of hydrolyzing peptidoglycan, have a major role in concealing this inflammatory molecule from Drosophila peptidoglycan recognition proteins (PGRPs). We show that autolysins trim the outermost peptidoglycan fragments and that in their absence bacterial virulence is impaired, as PGRPs can directly recognize leftover peptidoglycan extending beyond the external layers of bacterial proteins and polysaccharides. The activity of autolysins is not restricted to the producer cells but can also alter the surface of neighboring bacteria, facilitating the survival of the entire population in the infected host.

AB - Bacteria have to avoid recognition by the host immune system in order to establish a successful infection. Peptidoglycan, the principal constituent of virtually all bacterial surfaces, is a specific molecular signature recognized by dedicated host receptors, present in animals and plants, which trigger an immune response. Here we report that autolysins from Gram-positive pathogenic bacteria, enzymes capable of hydrolyzing peptidoglycan, have a major role in concealing this inflammatory molecule from Drosophila peptidoglycan recognition proteins (PGRPs). We show that autolysins trim the outermost peptidoglycan fragments and that in their absence bacterial virulence is impaired, as PGRPs can directly recognize leftover peptidoglycan extending beyond the external layers of bacterial proteins and polysaccharides. The activity of autolysins is not restricted to the producer cells but can also alter the surface of neighboring bacteria, facilitating the survival of the entire population in the infected host.

KW - Animals

KW - Drosophila

KW - Gram-Positive Bacteria

KW - Hydrolysis

KW - Immunity, Innate

KW - N-Acetylmuramoyl-L-alanine Amidase

KW - Peptidoglycan

KW - Virulence

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U2 - 10.7554/eLife.02277

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M3 - Article

VL - 2014

JO - eLife

JF - eLife

SN - 2050-084X

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