Legionella pneumophila S1P-lyase targets host sphingolipid metabolism and restrains autophagy
Abstract
Autophagy is an essential component of innate immunity, enabling the detection and elimination of intracellular pathogens. Legionella pneumophila, an intracellular pathogen that can cause a severe pneumonia in humans, is able to modulate autophagy through the action of effector proteins that are translocated into the host cell by the pathogen’s Dot/Icm type IV secretion system. Many of these effectors share structural and sequence similarity with eukaryotic proteins. Indeed, phylogenetic analyses have indicated their acquisition by horizontal gene transfer from a eukaryotic host. Here we report that L. pneumophila translocates the effector protein sphingosine-1 phosphate lyase (LpSpl) to target the host sphingosine biosynthesis and to curtail autophagy. Our structural characterization of LpSpl and its comparison with human SPL reveals high structural conservation, thus supporting prior phylogenetic analysis. Here, we show that LpSpl possesses S1P lyase activity that was abrogated by mutation of the catalytic site residues. L. pneumophila triggers the reduction of several sphingolipids critical for macrophage function in an LpSpl-dependent and -independent manner. LpSpl activity alone was sufficient to prevent an increase in sphingosine levels in infected host cells and to inhibit autophagy during macrophage infection. LpSpl was required for efficient infection of A/J mice, highlighting an important virulence rolemore »
- Authors:
-
[3];
more »
- Inst. Pasteur, Paris (France); CNRS UMR 3525, Paris (France)
- Inst. Necker Enfants-Malades, Paris (France); Univ. Paris Descartes-Sorbonne Paris Cité, Paris (France)
- Centre de Recherches en Cancérologie de Toulouse (France); Inst. of Environmental Assessment and Water Research (IDAEA-CSIC), Barcelona (Spain)
- Univ. of Toronto, ON (Canada); Hospital for Sick Children, Toronto, ON (Canada)
- Monash Univ., Melbourne, VIC (Australia)
- Univ. of Toronto, ON (Canada)
- Univ. of Zurich (Switzerland)
- Univ. of Melbourne (Australia)
- Univ. of Melbourne at the Peter Doherty Inst. for Infection and Immunity, Melbourne, VIC (Australia)
- Centre de Recherches en Cancérologie de Toulouse (France)
- Monash Univ., Clayton, VIC (Australia)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); Swiss National Science Foundation (SNSF)
- OSTI Identifier:
- 1239413
- Grant/Contract Number:
- ANR-10-LABX-62-IBEID; ANR-13-IFEC-0003-02; GM074942; GM094585; AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 113; Journal Issue: 7; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Legionella pneumophila; sphingosine-1-phosphate lyase; autophagy; sphingolipids; virulence
Citation Formats
Rolando, Monica, Escoll, Pedro, Nora, Tamara, Botti, Joëlle, Boitez, Valérie, Bedia, Carmen, Daniels, Craig, Abraham, Gilu, Stogios, Peter J., Skarina, Tatiana, Christophe, Charlotte, Dervins-Ravault, Delphine, Cazalet, Christel, Hilbi, Hubert, Rupasinghe, Thusitha W. T., Tull, Dedreia, McConville, Malcolm J., Ong, Sze Ying, Hartland, Elizabeth L., Codogno, Patrice, Levade, Thierry, Naderer, Thomas, Savchenko, Alexei, and Buchrieser, Carmen. Legionella pneumophila S1P-lyase targets host sphingolipid metabolism and restrains autophagy. United States: N. p., 2016.
Web. doi:10.1073/pnas.1522067113.
Rolando, Monica, Escoll, Pedro, Nora, Tamara, Botti, Joëlle, Boitez, Valérie, Bedia, Carmen, Daniels, Craig, Abraham, Gilu, Stogios, Peter J., Skarina, Tatiana, Christophe, Charlotte, Dervins-Ravault, Delphine, Cazalet, Christel, Hilbi, Hubert, Rupasinghe, Thusitha W. T., Tull, Dedreia, McConville, Malcolm J., Ong, Sze Ying, Hartland, Elizabeth L., Codogno, Patrice, Levade, Thierry, Naderer, Thomas, Savchenko, Alexei, & Buchrieser, Carmen. Legionella pneumophila S1P-lyase targets host sphingolipid metabolism and restrains autophagy. United States. https://doi.org/10.1073/pnas.1522067113
Rolando, Monica, Escoll, Pedro, Nora, Tamara, Botti, Joëlle, Boitez, Valérie, Bedia, Carmen, Daniels, Craig, Abraham, Gilu, Stogios, Peter J., Skarina, Tatiana, Christophe, Charlotte, Dervins-Ravault, Delphine, Cazalet, Christel, Hilbi, Hubert, Rupasinghe, Thusitha W. T., Tull, Dedreia, McConville, Malcolm J., Ong, Sze Ying, Hartland, Elizabeth L., Codogno, Patrice, Levade, Thierry, Naderer, Thomas, Savchenko, Alexei, and Buchrieser, Carmen. Mon .
"Legionella pneumophila S1P-lyase targets host sphingolipid metabolism and restrains autophagy". United States. https://doi.org/10.1073/pnas.1522067113. https://www.osti.gov/servlets/purl/1239413.
@article{osti_1239413,
title = {Legionella pneumophila S1P-lyase targets host sphingolipid metabolism and restrains autophagy},
author = {Rolando, Monica and Escoll, Pedro and Nora, Tamara and Botti, Joëlle and Boitez, Valérie and Bedia, Carmen and Daniels, Craig and Abraham, Gilu and Stogios, Peter J. and Skarina, Tatiana and Christophe, Charlotte and Dervins-Ravault, Delphine and Cazalet, Christel and Hilbi, Hubert and Rupasinghe, Thusitha W. T. and Tull, Dedreia and McConville, Malcolm J. and Ong, Sze Ying and Hartland, Elizabeth L. and Codogno, Patrice and Levade, Thierry and Naderer, Thomas and Savchenko, Alexei and Buchrieser, Carmen},
abstractNote = {Autophagy is an essential component of innate immunity, enabling the detection and elimination of intracellular pathogens. Legionella pneumophila, an intracellular pathogen that can cause a severe pneumonia in humans, is able to modulate autophagy through the action of effector proteins that are translocated into the host cell by the pathogen’s Dot/Icm type IV secretion system. Many of these effectors share structural and sequence similarity with eukaryotic proteins. Indeed, phylogenetic analyses have indicated their acquisition by horizontal gene transfer from a eukaryotic host. Here we report that L. pneumophila translocates the effector protein sphingosine-1 phosphate lyase (LpSpl) to target the host sphingosine biosynthesis and to curtail autophagy. Our structural characterization of LpSpl and its comparison with human SPL reveals high structural conservation, thus supporting prior phylogenetic analysis. Here, we show that LpSpl possesses S1P lyase activity that was abrogated by mutation of the catalytic site residues. L. pneumophila triggers the reduction of several sphingolipids critical for macrophage function in an LpSpl-dependent and -independent manner. LpSpl activity alone was sufficient to prevent an increase in sphingosine levels in infected host cells and to inhibit autophagy during macrophage infection. LpSpl was required for efficient infection of A/J mice, highlighting an important virulence role for this effector. Thus, we have uncovered a previously unidentified mechanism used by intracellular pathogens to inhibit autophagy, namely the disruption of host sphingolipid biosynthesis.},
doi = {10.1073/pnas.1522067113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 7,
volume = 113,
place = {United States},
year = {Mon Feb 01 00:00:00 EST 2016},
month = {Mon Feb 01 00:00:00 EST 2016}
}
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