Cytosolic expression of SecA2 is a prerequisite for long-term protective immunity

Eric Muraille, Emilie Narni-mancinelli, Pierre Gounon, Delphine Bassand, Nicolas Glaichenhaus, Laurel L. Lenz, Gregoire Lauvau

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Induction of efficient adaptive T cell-mediated immunity against the intracellular bacterium Listeria monocytogenes requires its successful invasion of host cell cytosol. However, it is not clear whether its cytosolic escape and growth are sufficient to induce T cell-mediated clearance and protection upon secondary infection. To investigate this issue, we have searched for mutants that do not induce long-term protective immunity yet invade the cytosol of infected cells. We found that mice immunized with L. monocytogenes lacking the SecA2 ATPase, an auxiliary protein secretion system present in several Gram-positive pathogenic bacteria, mounted a robust cytolytic IFN-γ-secreting CD8+ T cell response but were not protected against a secondary challenge with wild-type (wt) bacteria. Furthermore, CD8+ T cells from mice immunized with secA2- bacteria failed to transfer protection when injected into recipient mice demonstrating that they were unable to confer protection. Also secA2- and wt L. monocytogenes spread to the same myeloid-derived cell types in vivo and SecA2 deficiency does not interfere with intracytosolic bacteria multiplication. Therefore, cytosol invasion is not sufficient for inducing secondary protective responses and induction of memory CD8+ T cells mediating long-term antibacterial protective immunity is dependent upon SecA2 expression inside the cytosol of host cells in vivo.

Original languageEnglish (US)
Pages (from-to)1445-1454
Number of pages10
JournalCellular Microbiology
Volume9
Issue number6
DOIs
StatePublished - Jun 2007
Externally publishedYes

Fingerprint

T-cells
Immunity
Bacteria
Cytosol
T-Lymphocytes
Listeria monocytogenes
Listeria
Gram-Positive Bacteria
Myeloid Cells
Coinfection
Cellular Immunity
Adenosine Triphosphatases
Data storage equipment
Growth

ASJC Scopus subject areas

  • Clinical Biochemistry
  • Microbiology

Cite this

Muraille, E., Narni-mancinelli, E., Gounon, P., Bassand, D., Glaichenhaus, N., Lenz, L. L., & Lauvau, G. (2007). Cytosolic expression of SecA2 is a prerequisite for long-term protective immunity. Cellular Microbiology, 9(6), 1445-1454. https://doi.org/10.1111/j.1462-5822.2007.00883.x

Cytosolic expression of SecA2 is a prerequisite for long-term protective immunity. / Muraille, Eric; Narni-mancinelli, Emilie; Gounon, Pierre; Bassand, Delphine; Glaichenhaus, Nicolas; Lenz, Laurel L.; Lauvau, Gregoire.

In: Cellular Microbiology, Vol. 9, No. 6, 06.2007, p. 1445-1454.

Research output: Contribution to journalArticle

Muraille, E, Narni-mancinelli, E, Gounon, P, Bassand, D, Glaichenhaus, N, Lenz, LL & Lauvau, G 2007, 'Cytosolic expression of SecA2 is a prerequisite for long-term protective immunity', Cellular Microbiology, vol. 9, no. 6, pp. 1445-1454. https://doi.org/10.1111/j.1462-5822.2007.00883.x
Muraille E, Narni-mancinelli E, Gounon P, Bassand D, Glaichenhaus N, Lenz LL et al. Cytosolic expression of SecA2 is a prerequisite for long-term protective immunity. Cellular Microbiology. 2007 Jun;9(6):1445-1454. https://doi.org/10.1111/j.1462-5822.2007.00883.x
Muraille, Eric ; Narni-mancinelli, Emilie ; Gounon, Pierre ; Bassand, Delphine ; Glaichenhaus, Nicolas ; Lenz, Laurel L. ; Lauvau, Gregoire. / Cytosolic expression of SecA2 is a prerequisite for long-term protective immunity. In: Cellular Microbiology. 2007 ; Vol. 9, No. 6. pp. 1445-1454.
@article{36029ba8e338422ba6ee38047b9d8287,
title = "Cytosolic expression of SecA2 is a prerequisite for long-term protective immunity",
abstract = "Induction of efficient adaptive T cell-mediated immunity against the intracellular bacterium Listeria monocytogenes requires its successful invasion of host cell cytosol. However, it is not clear whether its cytosolic escape and growth are sufficient to induce T cell-mediated clearance and protection upon secondary infection. To investigate this issue, we have searched for mutants that do not induce long-term protective immunity yet invade the cytosol of infected cells. We found that mice immunized with L. monocytogenes lacking the SecA2 ATPase, an auxiliary protein secretion system present in several Gram-positive pathogenic bacteria, mounted a robust cytolytic IFN-γ-secreting CD8+ T cell response but were not protected against a secondary challenge with wild-type (wt) bacteria. Furthermore, CD8+ T cells from mice immunized with secA2- bacteria failed to transfer protection when injected into recipient mice demonstrating that they were unable to confer protection. Also secA2- and wt L. monocytogenes spread to the same myeloid-derived cell types in vivo and SecA2 deficiency does not interfere with intracytosolic bacteria multiplication. Therefore, cytosol invasion is not sufficient for inducing secondary protective responses and induction of memory CD8+ T cells mediating long-term antibacterial protective immunity is dependent upon SecA2 expression inside the cytosol of host cells in vivo.",
author = "Eric Muraille and Emilie Narni-mancinelli and Pierre Gounon and Delphine Bassand and Nicolas Glaichenhaus and Lenz, {Laurel L.} and Gregoire Lauvau",
year = "2007",
month = "6",
doi = "10.1111/j.1462-5822.2007.00883.x",
language = "English (US)",
volume = "9",
pages = "1445--1454",
journal = "Cellular Microbiology",
issn = "1462-5814",
publisher = "Wiley-Blackwell",
number = "6",

}

TY - JOUR

T1 - Cytosolic expression of SecA2 is a prerequisite for long-term protective immunity

AU - Muraille, Eric

AU - Narni-mancinelli, Emilie

AU - Gounon, Pierre

AU - Bassand, Delphine

AU - Glaichenhaus, Nicolas

AU - Lenz, Laurel L.

AU - Lauvau, Gregoire

PY - 2007/6

Y1 - 2007/6

N2 - Induction of efficient adaptive T cell-mediated immunity against the intracellular bacterium Listeria monocytogenes requires its successful invasion of host cell cytosol. However, it is not clear whether its cytosolic escape and growth are sufficient to induce T cell-mediated clearance and protection upon secondary infection. To investigate this issue, we have searched for mutants that do not induce long-term protective immunity yet invade the cytosol of infected cells. We found that mice immunized with L. monocytogenes lacking the SecA2 ATPase, an auxiliary protein secretion system present in several Gram-positive pathogenic bacteria, mounted a robust cytolytic IFN-γ-secreting CD8+ T cell response but were not protected against a secondary challenge with wild-type (wt) bacteria. Furthermore, CD8+ T cells from mice immunized with secA2- bacteria failed to transfer protection when injected into recipient mice demonstrating that they were unable to confer protection. Also secA2- and wt L. monocytogenes spread to the same myeloid-derived cell types in vivo and SecA2 deficiency does not interfere with intracytosolic bacteria multiplication. Therefore, cytosol invasion is not sufficient for inducing secondary protective responses and induction of memory CD8+ T cells mediating long-term antibacterial protective immunity is dependent upon SecA2 expression inside the cytosol of host cells in vivo.

AB - Induction of efficient adaptive T cell-mediated immunity against the intracellular bacterium Listeria monocytogenes requires its successful invasion of host cell cytosol. However, it is not clear whether its cytosolic escape and growth are sufficient to induce T cell-mediated clearance and protection upon secondary infection. To investigate this issue, we have searched for mutants that do not induce long-term protective immunity yet invade the cytosol of infected cells. We found that mice immunized with L. monocytogenes lacking the SecA2 ATPase, an auxiliary protein secretion system present in several Gram-positive pathogenic bacteria, mounted a robust cytolytic IFN-γ-secreting CD8+ T cell response but were not protected against a secondary challenge with wild-type (wt) bacteria. Furthermore, CD8+ T cells from mice immunized with secA2- bacteria failed to transfer protection when injected into recipient mice demonstrating that they were unable to confer protection. Also secA2- and wt L. monocytogenes spread to the same myeloid-derived cell types in vivo and SecA2 deficiency does not interfere with intracytosolic bacteria multiplication. Therefore, cytosol invasion is not sufficient for inducing secondary protective responses and induction of memory CD8+ T cells mediating long-term antibacterial protective immunity is dependent upon SecA2 expression inside the cytosol of host cells in vivo.

UR - http://www.scopus.com/inward/record.url?scp=34248636516&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=34248636516&partnerID=8YFLogxK

U2 - 10.1111/j.1462-5822.2007.00883.x

DO - 10.1111/j.1462-5822.2007.00883.x

M3 - Article

C2 - 17244189

AN - SCOPUS:34248636516

VL - 9

SP - 1445

EP - 1454

JO - Cellular Microbiology

JF - Cellular Microbiology

SN - 1462-5814

IS - 6

ER -