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Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod...
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| Zeitschriftentitel: | Infection and Immunity |
|---|---|
| Personen und Körperschaften: | , , , , |
| In: | Infection and Immunity, 77, 2009, 11, S. 4794-4805 |
| Format: | E-Article |
| Sprache: | Englisch |
| veröffentlicht: |
American Society for Microbiology
|
| Schlagwörter: |
| author_facet |
Fortier, Anne Doiron, Karine Saleh, Maya Grinstein, Sergio Gros, Philippe Fortier, Anne Doiron, Karine Saleh, Maya Grinstein, Sergio Gros, Philippe |
|---|---|
| author |
Fortier, Anne Doiron, Karine Saleh, Maya Grinstein, Sergio Gros, Philippe |
| spellingShingle |
Fortier, Anne Doiron, Karine Saleh, Maya Grinstein, Sergio Gros, Philippe Infection and Immunity Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 Infectious Diseases Immunology Microbiology Parasitology |
| author_sort |
fortier, anne |
| spelling |
Fortier, Anne Doiron, Karine Saleh, Maya Grinstein, Sergio Gros, Philippe 0019-9567 1098-5522 American Society for Microbiology Infectious Diseases Immunology Microbiology Parasitology http://dx.doi.org/10.1128/iai.01546-08 <jats:title>ABSTRACT</jats:title> <jats:p> The unique permissiveness of A/J mouse macrophages for replication of <jats:italic>Legionella pneumophila</jats:italic> is caused by a deficiency in the Nod-like receptor (NLR) protein and intracellular sensor for <jats:italic>L. pneumophila</jats:italic> flagellin ( <jats:italic>Naip5</jats:italic> ). The signaling pathways and proteins activated by Naip5 sensing in macrophages were investigated. Transcript profiling of macrophages from susceptible A/J mice and from resistant A/J mice harboring a transgenic wild-type copy of <jats:italic>Naip5</jats:italic> at 4 h following <jats:italic>L. pneumophila</jats:italic> infection suggested that two members of the Irf transcriptional regulator family, Irf1 and Irf8, are regulated in response to Naip5 sensing of <jats:italic>L. pneumophila</jats:italic> . We show that macrophages having defective alleles of either <jats:italic>Irf1</jats:italic> ( <jats:italic>Irf1</jats:italic> <jats:sup>−</jats:sup> <jats:sup>/</jats:sup> <jats:sup>−</jats:sup> ) or its heterodimerization partner gene <jats:italic>Irf8</jats:italic> ( <jats:italic> Irf8 <jats:sup>R294C</jats:sup> </jats:italic> ) become permissive for <jats:italic>L. pneumophila</jats:italic> replication, indicating that both the Irf1 and Irf8 proteins are essential for macrophage defense against <jats:italic>L. pneumophila</jats:italic> . Moreover, macrophages doubly heterozygous ( <jats:italic> Naip5 <jats:sup>AJ/WT</jats:sup> Irf8 <jats:sup>R294C/WT</jats:sup> </jats:italic> or <jats:italic>Nlrc4</jats:italic> <jats:sup>−/+</jats:sup> <jats:italic> Irf8 <jats:sup>R294C/WT</jats:sup> </jats:italic> ) for combined loss-of-function mutations in <jats:italic>Irf8</jats:italic> and in either <jats:italic>Naip5</jats:italic> or <jats:italic>Nlrc4</jats:italic> are highly susceptible to <jats:italic>L. pneumophila</jats:italic> , indicating that there is a strong genetic interaction between <jats:italic>Irf8</jats:italic> and the NLR protein family in the macrophage response to <jats:italic>L. pneumophila. Legionella</jats:italic> -containing phagosomes (LCPs) formed in permissive <jats:italic>Irf1</jats:italic> <jats:sup>−</jats:sup> <jats:sup>/</jats:sup> <jats:sup>−</jats:sup> or <jats:italic> Irf8 <jats:sup>R294C</jats:sup> </jats:italic> macrophages behave like LCPs formed in <jats:italic>Naip5</jats:italic> -insufficient and <jats:italic>Nlrc4</jats:italic> -deficient macrophages which fail to acidify. These results suggest that, in addition to <jats:italic>Naip5</jats:italic> and <jats:italic>Nlrc4</jats:italic> , <jats:italic>Irf1</jats:italic> and <jats:italic>Irf8</jats:italic> play a critical role in the early response of macrophages to infection with <jats:italic>L. pneumophila</jats:italic> , including antagonizing the ability of <jats:italic>L. pneumophila</jats:italic> to block phagosome acidification. They also suggest that flagellin sensing by the NLR proteins Naip5 and Nlrc4 may be coupled to Irf1-Irf8-mediated transcriptional activation of key effector genes essential for macrophage resistance to <jats:italic>L. pneumophila</jats:italic> infection. </jats:p> Restriction of <i>L</i> <i>egionella pneumophila</i> Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 Infection and Immunity |
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10.1128/iai.01546-08 |
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American Society for Microbiology, 2009 |
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American Society for Microbiology, 2009 |
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fortier2009restrictionoflegionellapneumophilareplicationinmacrophagesrequiresconcertedactionofthetranscriptionalregulatorsirf1andirf8andnodlikereceptorsnaip5andnlrc4 |
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American Society for Microbiology |
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Infection and Immunity |
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| title |
Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_unstemmed |
Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_full |
Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_fullStr |
Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_full_unstemmed |
Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_short |
Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_sort |
restriction of
<i>l</i>
<i>egionella pneumophila</i>
replication in macrophages requires concerted action of the transcriptional regulators irf1 and irf8 and nod-like receptors naip5 and nlrc4 |
| topic |
Infectious Diseases Immunology Microbiology Parasitology |
| url |
http://dx.doi.org/10.1128/iai.01546-08 |
| publishDate |
2009 |
| physical |
4794-4805 |
| description |
<jats:title>ABSTRACT</jats:title>
<jats:p>
The unique permissiveness of A/J mouse macrophages for replication of
<jats:italic>Legionella pneumophila</jats:italic>
is caused by a deficiency in the Nod-like receptor (NLR) protein and intracellular sensor for
<jats:italic>L. pneumophila</jats:italic>
flagellin (
<jats:italic>Naip5</jats:italic>
). The signaling pathways and proteins activated by Naip5 sensing in macrophages were investigated. Transcript profiling of macrophages from susceptible A/J mice and from resistant A/J mice harboring a transgenic wild-type copy of
<jats:italic>Naip5</jats:italic>
at 4 h following
<jats:italic>L. pneumophila</jats:italic>
infection suggested that two members of the Irf transcriptional regulator family, Irf1 and Irf8, are regulated in response to Naip5 sensing of
<jats:italic>L. pneumophila</jats:italic>
. We show that macrophages having defective alleles of either
<jats:italic>Irf1</jats:italic>
(
<jats:italic>Irf1</jats:italic>
<jats:sup>−</jats:sup>
<jats:sup>/</jats:sup>
<jats:sup>−</jats:sup>
) or its heterodimerization partner gene
<jats:italic>Irf8</jats:italic>
(
<jats:italic>
Irf8
<jats:sup>R294C</jats:sup>
</jats:italic>
) become permissive for
<jats:italic>L. pneumophila</jats:italic>
replication, indicating that both the Irf1 and Irf8 proteins are essential for macrophage defense against
<jats:italic>L. pneumophila</jats:italic>
. Moreover, macrophages doubly heterozygous (
<jats:italic>
Naip5
<jats:sup>AJ/WT</jats:sup>
Irf8
<jats:sup>R294C/WT</jats:sup>
</jats:italic>
or
<jats:italic>Nlrc4</jats:italic>
<jats:sup>−/+</jats:sup>
<jats:italic>
Irf8
<jats:sup>R294C/WT</jats:sup>
</jats:italic>
) for combined loss-of-function mutations in
<jats:italic>Irf8</jats:italic>
and in either
<jats:italic>Naip5</jats:italic>
or
<jats:italic>Nlrc4</jats:italic>
are highly susceptible to
<jats:italic>L. pneumophila</jats:italic>
, indicating that there is a strong genetic interaction between
<jats:italic>Irf8</jats:italic>
and the NLR protein family in the macrophage response to
<jats:italic>L. pneumophila. Legionella</jats:italic>
-containing phagosomes (LCPs) formed in permissive
<jats:italic>Irf1</jats:italic>
<jats:sup>−</jats:sup>
<jats:sup>/</jats:sup>
<jats:sup>−</jats:sup>
or
<jats:italic>
Irf8
<jats:sup>R294C</jats:sup>
</jats:italic>
macrophages behave like LCPs formed in
<jats:italic>Naip5</jats:italic>
-insufficient and
<jats:italic>Nlrc4</jats:italic>
-deficient macrophages which fail to acidify. These results suggest that, in addition to
<jats:italic>Naip5</jats:italic>
and
<jats:italic>Nlrc4</jats:italic>
,
<jats:italic>Irf1</jats:italic>
and
<jats:italic>Irf8</jats:italic>
play a critical role in the early response of macrophages to infection with
<jats:italic>L. pneumophila</jats:italic>
, including antagonizing the ability of
<jats:italic>L. pneumophila</jats:italic>
to block phagosome acidification. They also suggest that flagellin sensing by the NLR proteins Naip5 and Nlrc4 may be coupled to Irf1-Irf8-mediated transcriptional activation of key effector genes essential for macrophage resistance to
<jats:italic>L. pneumophila</jats:italic>
infection.
</jats:p> |
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| description | <jats:title>ABSTRACT</jats:title> <jats:p> The unique permissiveness of A/J mouse macrophages for replication of <jats:italic>Legionella pneumophila</jats:italic> is caused by a deficiency in the Nod-like receptor (NLR) protein and intracellular sensor for <jats:italic>L. pneumophila</jats:italic> flagellin ( <jats:italic>Naip5</jats:italic> ). The signaling pathways and proteins activated by Naip5 sensing in macrophages were investigated. Transcript profiling of macrophages from susceptible A/J mice and from resistant A/J mice harboring a transgenic wild-type copy of <jats:italic>Naip5</jats:italic> at 4 h following <jats:italic>L. pneumophila</jats:italic> infection suggested that two members of the Irf transcriptional regulator family, Irf1 and Irf8, are regulated in response to Naip5 sensing of <jats:italic>L. pneumophila</jats:italic> . We show that macrophages having defective alleles of either <jats:italic>Irf1</jats:italic> ( <jats:italic>Irf1</jats:italic> <jats:sup>−</jats:sup> <jats:sup>/</jats:sup> <jats:sup>−</jats:sup> ) or its heterodimerization partner gene <jats:italic>Irf8</jats:italic> ( <jats:italic> Irf8 <jats:sup>R294C</jats:sup> </jats:italic> ) become permissive for <jats:italic>L. pneumophila</jats:italic> replication, indicating that both the Irf1 and Irf8 proteins are essential for macrophage defense against <jats:italic>L. pneumophila</jats:italic> . Moreover, macrophages doubly heterozygous ( <jats:italic> Naip5 <jats:sup>AJ/WT</jats:sup> Irf8 <jats:sup>R294C/WT</jats:sup> </jats:italic> or <jats:italic>Nlrc4</jats:italic> <jats:sup>−/+</jats:sup> <jats:italic> Irf8 <jats:sup>R294C/WT</jats:sup> </jats:italic> ) for combined loss-of-function mutations in <jats:italic>Irf8</jats:italic> and in either <jats:italic>Naip5</jats:italic> or <jats:italic>Nlrc4</jats:italic> are highly susceptible to <jats:italic>L. pneumophila</jats:italic> , indicating that there is a strong genetic interaction between <jats:italic>Irf8</jats:italic> and the NLR protein family in the macrophage response to <jats:italic>L. pneumophila. Legionella</jats:italic> -containing phagosomes (LCPs) formed in permissive <jats:italic>Irf1</jats:italic> <jats:sup>−</jats:sup> <jats:sup>/</jats:sup> <jats:sup>−</jats:sup> or <jats:italic> Irf8 <jats:sup>R294C</jats:sup> </jats:italic> macrophages behave like LCPs formed in <jats:italic>Naip5</jats:italic> -insufficient and <jats:italic>Nlrc4</jats:italic> -deficient macrophages which fail to acidify. These results suggest that, in addition to <jats:italic>Naip5</jats:italic> and <jats:italic>Nlrc4</jats:italic> , <jats:italic>Irf1</jats:italic> and <jats:italic>Irf8</jats:italic> play a critical role in the early response of macrophages to infection with <jats:italic>L. pneumophila</jats:italic> , including antagonizing the ability of <jats:italic>L. pneumophila</jats:italic> to block phagosome acidification. They also suggest that flagellin sensing by the NLR proteins Naip5 and Nlrc4 may be coupled to Irf1-Irf8-mediated transcriptional activation of key effector genes essential for macrophage resistance to <jats:italic>L. pneumophila</jats:italic> infection. </jats:p> |
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| match_str | fortier2009restrictionoflegionellapneumophilareplicationinmacrophagesrequiresconcertedactionofthetranscriptionalregulatorsirf1andirf8andnodlikereceptorsnaip5andnlrc4 |
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| spelling | Fortier, Anne Doiron, Karine Saleh, Maya Grinstein, Sergio Gros, Philippe 0019-9567 1098-5522 American Society for Microbiology Infectious Diseases Immunology Microbiology Parasitology http://dx.doi.org/10.1128/iai.01546-08 <jats:title>ABSTRACT</jats:title> <jats:p> The unique permissiveness of A/J mouse macrophages for replication of <jats:italic>Legionella pneumophila</jats:italic> is caused by a deficiency in the Nod-like receptor (NLR) protein and intracellular sensor for <jats:italic>L. pneumophila</jats:italic> flagellin ( <jats:italic>Naip5</jats:italic> ). The signaling pathways and proteins activated by Naip5 sensing in macrophages were investigated. Transcript profiling of macrophages from susceptible A/J mice and from resistant A/J mice harboring a transgenic wild-type copy of <jats:italic>Naip5</jats:italic> at 4 h following <jats:italic>L. pneumophila</jats:italic> infection suggested that two members of the Irf transcriptional regulator family, Irf1 and Irf8, are regulated in response to Naip5 sensing of <jats:italic>L. pneumophila</jats:italic> . We show that macrophages having defective alleles of either <jats:italic>Irf1</jats:italic> ( <jats:italic>Irf1</jats:italic> <jats:sup>−</jats:sup> <jats:sup>/</jats:sup> <jats:sup>−</jats:sup> ) or its heterodimerization partner gene <jats:italic>Irf8</jats:italic> ( <jats:italic> Irf8 <jats:sup>R294C</jats:sup> </jats:italic> ) become permissive for <jats:italic>L. pneumophila</jats:italic> replication, indicating that both the Irf1 and Irf8 proteins are essential for macrophage defense against <jats:italic>L. pneumophila</jats:italic> . Moreover, macrophages doubly heterozygous ( <jats:italic> Naip5 <jats:sup>AJ/WT</jats:sup> Irf8 <jats:sup>R294C/WT</jats:sup> </jats:italic> or <jats:italic>Nlrc4</jats:italic> <jats:sup>−/+</jats:sup> <jats:italic> Irf8 <jats:sup>R294C/WT</jats:sup> </jats:italic> ) for combined loss-of-function mutations in <jats:italic>Irf8</jats:italic> and in either <jats:italic>Naip5</jats:italic> or <jats:italic>Nlrc4</jats:italic> are highly susceptible to <jats:italic>L. pneumophila</jats:italic> , indicating that there is a strong genetic interaction between <jats:italic>Irf8</jats:italic> and the NLR protein family in the macrophage response to <jats:italic>L. pneumophila. Legionella</jats:italic> -containing phagosomes (LCPs) formed in permissive <jats:italic>Irf1</jats:italic> <jats:sup>−</jats:sup> <jats:sup>/</jats:sup> <jats:sup>−</jats:sup> or <jats:italic> Irf8 <jats:sup>R294C</jats:sup> </jats:italic> macrophages behave like LCPs formed in <jats:italic>Naip5</jats:italic> -insufficient and <jats:italic>Nlrc4</jats:italic> -deficient macrophages which fail to acidify. These results suggest that, in addition to <jats:italic>Naip5</jats:italic> and <jats:italic>Nlrc4</jats:italic> , <jats:italic>Irf1</jats:italic> and <jats:italic>Irf8</jats:italic> play a critical role in the early response of macrophages to infection with <jats:italic>L. pneumophila</jats:italic> , including antagonizing the ability of <jats:italic>L. pneumophila</jats:italic> to block phagosome acidification. They also suggest that flagellin sensing by the NLR proteins Naip5 and Nlrc4 may be coupled to Irf1-Irf8-mediated transcriptional activation of key effector genes essential for macrophage resistance to <jats:italic>L. pneumophila</jats:italic> infection. </jats:p> Restriction of <i>L</i> <i>egionella pneumophila</i> Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 Infection and Immunity |
| spellingShingle | Fortier, Anne, Doiron, Karine, Saleh, Maya, Grinstein, Sergio, Gros, Philippe, Infection and Immunity, Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4, Infectious Diseases, Immunology, Microbiology, Parasitology |
| title | Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_full | Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_fullStr | Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_full_unstemmed | Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_short | Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| title_sort | restriction of <i>l</i> <i>egionella pneumophila</i> replication in macrophages requires concerted action of the transcriptional regulators irf1 and irf8 and nod-like receptors naip5 and nlrc4 |
| title_unstemmed | Restriction of L egionella pneumophila Replication in Macrophages Requires Concerted Action of the Transcriptional Regulators Irf1 and Irf8 and Nod-Like Receptors Naip5 and Nlrc4 |
| topic | Infectious Diseases, Immunology, Microbiology, Parasitology |
| url | http://dx.doi.org/10.1128/iai.01546-08 |