PittsburghV1, Main, Exploration, bibRecord, 000A07

Unexpected Role for IL-17 in Protective Immunity against Hypervirulent Mycobacterium tuberculosis HN878 Infection

Identifieur interne : 000A07 ( Main/Exploration ); précédent : 000A06; suivant : 000A08

Unexpected Role for IL-17 in Protective Immunity against Hypervirulent Mycobacterium tuberculosis HN878 Infection

Auteurs : Radha Gopal [États-Unis] ; Leticia Monin [États-Unis] ; Samantha Slight [États-Unis] ; Uzodinma Uche [États-Unis] ; Emmeline Blanchard [États-Unis] ; Beth A. Fallert Junecko [États-Unis] ; Rosalio Ramos-Payan [Mexique, États-Unis] ; Christina L. Stallings [États-Unis] ; Todd A. Reinhart [États-Unis] ; Jay K. Kolls [États-Unis] ; Deepak Kaushal [États-Unis] ; Uma Nagarajan [États-Unis] ; Javier Rangel-Moreno [États-Unis] ; Shabaana A. Khader [États-Unis]

Source :

PLoS Pathogens [ 1553-7366 ] ; 2014.

RBID : PMC:4022785

Descripteurs français

KwdFr :
- Animaux, Cellules cultivées, Cytoprotection (génétique), Cytoprotection (immunologie), Femelle, Immunité innée (génétique), Interleukine-1 bêta (physiologie), Interleukine-17 (génétique), Interleukine-17 (physiologie), Maladies transmissibles émergentes (génétique), Maladies transmissibles émergentes (immunologie), Mycobacterium tuberculosis (immunologie), Mycobacterium tuberculosis (pathogénicité), Mâle, Récepteur de type Toll-2 (physiologie), Récepteur à l'interleukine-1 de type I (génétique), Souris, Souris de lignée C57BL, Souris knockout, Tuberculose (génétique), Tuberculose (immunologie).
MESH :
- génétique : Cytoprotection, Immunité innée, Interleukine-17, Maladies transmissibles émergentes, Récepteur à l'interleukine-1 de type I, Tuberculose.
- immunologie : Cytoprotection, Maladies transmissibles émergentes, Mycobacterium tuberculosis, Tuberculose.
- pathogénicité : Mycobacterium tuberculosis.
- physiologie : Interleukine-1 bêta, Interleukine-17, Récepteur de type Toll-2.
- Animaux, Cellules cultivées, Femelle, Mâle, Souris, Souris de lignée C57BL, Souris knockout.

English descriptors

KwdEn :
- Animals, Cells, Cultured, Communicable Diseases, Emerging (genetics), Communicable Diseases, Emerging (immunology), Cytoprotection (genetics), Cytoprotection (immunology), Female, Immunity, Innate (genetics), Interleukin-17 (genetics), Interleukin-17 (physiology), Interleukin-1beta (physiology), Male, Mice, Mice, Inbred C57BL, Mice, Knockout, Mycobacterium tuberculosis (immunology), Mycobacterium tuberculosis (pathogenicity), Receptors, Interleukin-1 Type I (genetics), Toll-Like Receptor 2 (physiology), Tuberculosis (genetics), Tuberculosis (immunology).
MESH :
- chemical , genetics : Interleukin-17, Receptors, Interleukin-1 Type I.
- genetics : Communicable Diseases, Emerging, Cytoprotection, Immunity, Innate, Tuberculosis.
- immunology : Communicable Diseases, Emerging, Cytoprotection, Mycobacterium tuberculosis, Tuberculosis.
- pathogenicity : Mycobacterium tuberculosis.
- chemical , physiology : Interleukin-17, Interleukin-1beta, Toll-Like Receptor 2.
- Animals, Cells, Cultured, Female, Male, Mice, Mice, Inbred C57BL, Mice, Knockout.

Abstract

Mycobacterium tuberculosis (Mtb), the causative agent of tuberculosis (TB), infects one third of the world's population. Among these infections, clinical isolates belonging to the W-Beijing appear to be emerging, representing about 50% of Mtb isolates in East Asia, and about 13% of all Mtb isolates worldwide. In animal models, infection with W-Beijing strain, Mtb HN878, is considered “hypervirulent” as it results in increased mortality and causes exacerbated immunopathology in infected animals. We had previously shown the Interleukin (IL) -17 pathway is dispensable for primary immunity against infection with the lab adapted Mtb H37Rv strain. However, it is not known whether IL-17 has any role to play in protective immunity against infection with clinical Mtb isolates. We report here that lab adapted Mtb strains, such as H37Rv, or less virulent Mtb clinical isolates, such as Mtb CDC1551, do not require IL-17 for protective immunity against infection while infection with Mtb HN878 requires IL-17 for early protective immunity. Unexpectedly, Mtb HN878 induces robust production of IL-1β through a TLR-2-dependent mechanism, which supports potent IL-17 responses. We also show that the role for IL-17 in mediating protective immunity against Mtb HN878 is through IL-17 Receptor signaling in non-hematopoietic cells, mediating the induction of the chemokine, CXCL-13, which is required for localization of T cells within lung lymphoid follicles. Correct T cell localization within lymphoid follicles in the lung is required for maximal macrophage activation and Mtb control. Since IL-17 has a critical role in vaccine-induced immunity against TB, our results have far reaching implications for the design of vaccines and therapies to prevent and treat emerging Mtb strains. In addition, our data changes the existing paradigm that IL-17 is dispensable for primary immunity against Mtb infection, and instead suggests a differential role for IL-17 in early protective immunity against emerging Mtb strains.

Url:

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4022785

DOI: 10.1371/journal.ppat.1004099
PubMed: 24831696
PubMed Central: 4022785

Affiliations:

Le document en format XML

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 HN878 Infection</title>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Unexpected Role for IL-17 in Protective Immunity against Hypervirulent <italic>Mycobacterium tuberculosis</italic>
 HN878 Infection</title>
<author><name sortKey="Gopal, Radha" sort="Gopal, Radha" uniqKey="Gopal R" first="Radha" last="Gopal">Radha Gopal</name>
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<author><name sortKey="Slight, Samantha" sort="Slight, Samantha" uniqKey="Slight S" first="Samantha" last="Slight">Samantha Slight</name>
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<author><name sortKey="Uche, Uzodinma" sort="Uche, Uzodinma" uniqKey="Uche U" first="Uzodinma" last="Uche">Uzodinma Uche</name>
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<author><name sortKey="A Fallert Junecko, Beth" sort="A Fallert Junecko, Beth" uniqKey="A Fallert Junecko B" first="Beth" last="A. Fallert Junecko">Beth A. Fallert Junecko</name>
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<author><name sortKey="Ramos Payan, Rosalio" sort="Ramos Payan, Rosalio" uniqKey="Ramos Payan R" first="Rosalio" last="Ramos-Payan">Rosalio Ramos-Payan</name>
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</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Medicine, Division of Allergy, Immunology and Rheumatology, University of Rochester Medical Center, Rochester, New York</wicri:regionArea>
<placeName><region type="state">État de New York</region>
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<author><name sortKey="Stallings, Christina L" sort="Stallings, Christina L" uniqKey="Stallings C" first="Christina L." last="Stallings">Christina L. Stallings</name>
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<wicri:regionArea>Department of Molecular Microbiology, Washington University in St. Louis, St. Louis, Missouri</wicri:regionArea>
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<author><name sortKey="Kolls, Jay K" sort="Kolls, Jay K" uniqKey="Kolls J" first="Jay K." last="Kolls">Jay K. Kolls</name>
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</nlm:aff>
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<placeName><region type="state">Pennsylvanie</region>
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</author>
<author><name sortKey="Kaushal, Deepak" sort="Kaushal, Deepak" uniqKey="Kaushal D" first="Deepak" last="Kaushal">Deepak Kaushal</name>
<affiliation wicri:level="2"><nlm:aff id="aff7"><addr-line>Tulane National Primate Center, New Orleans, Louisiana, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Tulane National Primate Center, New Orleans, Louisiana</wicri:regionArea>
<placeName><region type="state">Louisiane</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Nagarajan, Uma" sort="Nagarajan, Uma" uniqKey="Nagarajan U" first="Uma" last="Nagarajan">Uma Nagarajan</name>
<affiliation wicri:level="2"><nlm:aff id="aff8"><addr-line>Department of Pediatrics, University of North Carolina, Chapel Hill, Chapel Hill, North Carolina, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Pediatrics, University of North Carolina, Chapel Hill, Chapel Hill, North Carolina</wicri:regionArea>
<placeName><region type="state">Caroline du Nord</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Rangel Moreno, Javier" sort="Rangel Moreno, Javier" uniqKey="Rangel Moreno J" first="Javier" last="Rangel-Moreno">Javier Rangel-Moreno</name>
<affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Medicine, Division of Allergy, Immunology and Rheumatology, University of Rochester Medical Center, Rochester, New York, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Medicine, Division of Allergy, Immunology and Rheumatology, University of Rochester Medical Center, Rochester, New York</wicri:regionArea>
<placeName><region type="state">État de New York</region>
</placeName>
</affiliation>
</author>
<author><name sortKey="Khader, Shabaana A" sort="Khader, Shabaana A" uniqKey="Khader S" first="Shabaana A." last="Khader">Shabaana A. Khader</name>
<affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Department of Pediatrics, Division of Infectious Diseases, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Pediatrics, Division of Infectious Diseases, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania</wicri:regionArea>
<placeName><region type="state">Pennsylvanie</region>
</placeName>
</affiliation>
<affiliation wicri:level="4"><nlm:aff id="aff5"><addr-line>Department of Molecular Microbiology, Washington University in St. Louis, St. Louis, Missouri, United States of America</addr-line>
</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Molecular Microbiology, Washington University in St. Louis, St. Louis, Missouri</wicri:regionArea>
<placeName><region type="state">Missouri (État)</region>
<settlement type="city">Saint-Louis (Missouri)</settlement>
</placeName>
<orgName type="university">Université Washington de Saint-Louis</orgName>
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</analytic>
<series><title level="j">PLoS Pathogens</title>
<idno type="ISSN">1553-7366</idno>
<idno type="eISSN">1553-7374</idno>
<imprint><date when="2014">2014</date>
</imprint>
</series>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term>
<term>Cells, Cultured</term>
<term>Communicable Diseases, Emerging (genetics)</term>
<term>Communicable Diseases, Emerging (immunology)</term>
<term>Cytoprotection (genetics)</term>
<term>Cytoprotection (immunology)</term>
<term>Female</term>
<term>Immunity, Innate (genetics)</term>
<term>Interleukin-17 (genetics)</term>
<term>Interleukin-17 (physiology)</term>
<term>Interleukin-1beta (physiology)</term>
<term>Male</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Mice, Knockout</term>
<term>Mycobacterium tuberculosis (immunology)</term>
<term>Mycobacterium tuberculosis (pathogenicity)</term>
<term>Receptors, Interleukin-1 Type I (genetics)</term>
<term>Toll-Like Receptor 2 (physiology)</term>
<term>Tuberculosis (genetics)</term>
<term>Tuberculosis (immunology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Animaux</term>
<term>Cellules cultivées</term>
<term>Cytoprotection (génétique)</term>
<term>Cytoprotection (immunologie)</term>
<term>Femelle</term>
<term>Immunité innée (génétique)</term>
<term>Interleukine-1 bêta (physiologie)</term>
<term>Interleukine-17 (génétique)</term>
<term>Interleukine-17 (physiologie)</term>
<term>Maladies transmissibles émergentes (génétique)</term>
<term>Maladies transmissibles émergentes (immunologie)</term>
<term>Mycobacterium tuberculosis (immunologie)</term>
<term>Mycobacterium tuberculosis (pathogénicité)</term>
<term>Mâle</term>
<term>Récepteur de type Toll-2 (physiologie)</term>
<term>Récepteur à l'interleukine-1 de type I (génétique)</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
<term>Souris knockout</term>
<term>Tuberculose (génétique)</term>
<term>Tuberculose (immunologie)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Interleukin-17</term>
<term>Receptors, Interleukin-1 Type I</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Communicable Diseases, Emerging</term>
<term>Cytoprotection</term>
<term>Immunity, Innate</term>
<term>Tuberculosis</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Cytoprotection</term>
<term>Immunité innée</term>
<term>Interleukine-17</term>
<term>Maladies transmissibles émergentes</term>
<term>Récepteur à l'interleukine-1 de type I</term>
<term>Tuberculose</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr"><term>Cytoprotection</term>
<term>Maladies transmissibles émergentes</term>
<term>Mycobacterium tuberculosis</term>
<term>Tuberculose</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Communicable Diseases, Emerging</term>
<term>Cytoprotection</term>
<term>Mycobacterium tuberculosis</term>
<term>Tuberculosis</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en"><term>Mycobacterium tuberculosis</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr"><term>Mycobacterium tuberculosis</term>
</keywords>
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<term>Interleukine-17</term>
<term>Récepteur de type Toll-2</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="physiology" xml:lang="en"><term>Interleukin-17</term>
<term>Interleukin-1beta</term>
<term>Toll-Like Receptor 2</term>
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<keywords scheme="MESH" xml:lang="en"><term>Animals</term>
<term>Cells, Cultured</term>
<term>Female</term>
<term>Male</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Mice, Knockout</term>
</keywords>
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<term>Cellules cultivées</term>
<term>Femelle</term>
<term>Mâle</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
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<front><div type="abstract" xml:lang="en"><p><italic>Mycobacterium tuberculosis (Mtb)</italic>
, the causative agent of tuberculosis (TB), infects one third of the world's population. Among these infections, clinical isolates belonging to the W-Beijing appear to be emerging, representing about 50% of <italic>Mtb</italic>
 isolates in East Asia, and about 13% of all <italic>Mtb</italic>
 isolates worldwide. In animal models, infection with W-Beijing strain, <italic>Mtb</italic>
 HN878, is considered “hypervirulent” as it results in increased mortality and causes exacerbated immunopathology in infected animals. We had previously shown the Interleukin (IL) -17 pathway is dispensable for primary immunity against infection with the lab adapted <italic>Mtb</italic>
 H37Rv strain. However, it is not known whether IL-17 has any role to play in protective immunity against infection with clinical <italic>Mtb</italic>
 isolates. We report here that lab adapted <italic>Mtb</italic>
 strains, such as H37Rv, or less virulent <italic>Mtb</italic>
 clinical isolates, such as <italic>Mtb</italic>
 CDC1551, do not require IL-17 for protective immunity against infection while infection with <italic>Mtb</italic>
 HN878 requires IL-17 for early protective immunity. Unexpectedly, <italic>Mtb</italic>
 HN878 induces robust production of IL-1β through a TLR-2-dependent mechanism, which supports potent IL-17 responses. We also show that the role for IL-17 in mediating protective immunity against <italic>Mtb</italic>
 HN878 is through IL-17 Receptor signaling in non-hematopoietic cells, mediating the induction of the chemokine, CXCL-13, which is required for localization of T cells within lung lymphoid follicles. Correct T cell localization within lymphoid follicles in the lung is required for maximal macrophage activation and <italic>Mtb</italic>
 control. Since IL-17 has a critical role in vaccine-induced immunity against TB, our results have far reaching implications for the design of vaccines and therapies to prevent and treat emerging <italic>Mtb</italic>
 strains. In addition, our data changes the existing paradigm that IL-17 is dispensable for primary immunity against <italic>Mtb</italic>
 infection, and instead suggests a differential role for IL-17 in early protective immunity against emerging <italic>Mtb</italic>
 strains.</p>
</div>
</front>
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   |type=    RBID
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   |texte=   Unexpected Role for IL-17 in Protective Immunity against Hypervirulent Mycobacterium tuberculosis HN878 Infection
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Unexpected Role for IL-17 in Protective Immunity against Hypervirulent Mycobacterium tuberculosis HN878 Infection

Unexpected Role for IL-17 in Protective Immunity against Hypervirulent Mycobacterium tuberculosis HN878 Infection

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