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The Ly49E receptor inhibits the immune control of acute Trypanosoma cruzi infection

Jessica Filtjens, Nicolas Coltel, Sabrina Cencig, Sylvie Taveirne UGent, Els Van Ammel UGent, Aline Van Acker, Tessa Kerre UGent, Patrick Matthys, Tom Taghon UGent, Bart Vandekerckhove UGent, et al. (2016) FRONTIERS IN IMMUNOLOGY. 7.
abstract
The protozoan parasite Trypanosoma cruzi circulates in the blood upon infection and invades various cells. Parasites intensively multiply during the acute phase of infection and persist lifelong at low levels in tissues and blood during the chronic phase. Natural killer (NK) and NKT cells play an important role in the immune control of T. cruzi infection, mainly by releasing the cytokine IFN-gamma that activates the microbicidal action of macrophages and other cells and shapes a protective type 1 immune response. The mechanisms by which immune cells are regulated to produce IFN-gamma during T. cruzi infection are still incompletely understood. Here, we show that urokinase plasminogen activator (uPA) is induced early upon T. cruzi infection and remains elevated until day 20 post-infection. We previously demonstrated that the inhibitory receptor Ly49E, which is expressed, among others, on NK and NKT cells, is triggered by uPA. Therefore, we compared wild type (WT) to Ly49E knockout (KO) mice for their control of experimental T. cruzi infection. Our results show that young, i.e., 4- and 6-week-old, Ly49E KO mice control the infection better than WT mice, indicated by a lower parasite load and less cachexia. The beneficial effect of Ly49E depletion is more obvious in 4- week-old male than in female mice and weakens in 8-week-old mice. In young mice, the lower T. cruzi parasitemia in Ly49E KO mice is paralleled by higher IFN-gamma production compared to their WT controls. Our data indicate that Ly49E receptor expression inhibits the immune control of T. cruzi infection. This is the first demonstration that the inhibitory Ly49E receptor can interfere with the immune response to a pathogen in vivo.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
NATURAL-KILLER-CELLS, IFN-GAMMA PRODUCTION, NK CELLS, T-CELLS, PLASMINOGEN-ACTIVATOR, CHAGAS-DISEASE, EARLY-LIFE, DELTA-T, EXPRESSION, MICE, Ly49E receptor, natural killer cells, Trypanosoma cruzi, immune control, urokinase plasminogen activator, IFN-gamma
journal title
FRONTIERS IN IMMUNOLOGY
Front. Immunol.
volume
7
article number
472
pages
11 pages
Web of Science type
Article
Web of Science id
000387418500001
JCR category
IMMUNOLOGY
JCR impact factor
6.429 (2016)
JCR rank
21/150 (2016)
JCR quartile
1 (2016)
ISSN
1664-3224
DOI
10.3389/fimmu.2016.00472
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
8509449
handle
http://hdl.handle.net/1854/LU-8509449
date created
2017-02-14 14:36:08
date last changed
2017-09-01 08:03:52
@article{8509449,
  abstract     = {The protozoan parasite Trypanosoma cruzi circulates in the blood upon infection and invades various cells. Parasites intensively multiply during the acute phase of infection and persist lifelong at low levels in tissues and blood during the chronic phase. Natural killer (NK) and NKT cells play an important role in the immune control of T. cruzi infection, mainly by releasing the cytokine IFN-gamma that activates the microbicidal action of macrophages and other cells and shapes a protective type 1 immune response. The mechanisms by which immune cells are regulated to produce IFN-gamma during T. cruzi infection are still incompletely understood. Here, we show that urokinase plasminogen activator (uPA) is induced early upon T. cruzi infection and remains elevated until day 20 post-infection. We previously demonstrated that the inhibitory receptor Ly49E, which is expressed, among others, on NK and NKT cells, is triggered by uPA. Therefore, we compared wild type (WT) to Ly49E knockout (KO) mice for their control of experimental T. cruzi infection. Our results show that young, i.e., 4- and 6-week-old, Ly49E KO mice control the infection better than WT mice, indicated by a lower parasite load and less cachexia. The beneficial effect of Ly49E depletion is more obvious in 4- week-old male than in female mice and weakens in 8-week-old mice. In young mice, the lower T. cruzi parasitemia in Ly49E KO mice is paralleled by higher IFN-gamma production compared to their WT controls. Our data indicate that Ly49E receptor expression inhibits the immune control of T. cruzi infection. This is the first demonstration that the inhibitory Ly49E receptor can interfere with the immune response to a pathogen in vivo.},
  articleno    = {472},
  author       = {Filtjens, Jessica and Coltel, Nicolas and Cencig, Sabrina and Taveirne, Sylvie and Van Ammel, Els and Van Acker, Aline and Kerre, Tessa and Matthys, Patrick and Taghon, Tom and Vandekerckhove, Bart and Carlier, Yves and Truyens, Carine and Leclercq, Georges},
  issn         = {1664-3224},
  journal      = {FRONTIERS IN IMMUNOLOGY},
  keyword      = {NATURAL-KILLER-CELLS,IFN-GAMMA PRODUCTION,NK CELLS,T-CELLS,PLASMINOGEN-ACTIVATOR,CHAGAS-DISEASE,EARLY-LIFE,DELTA-T,EXPRESSION,MICE,Ly49E receptor,natural killer cells,Trypanosoma cruzi,immune control,urokinase plasminogen activator,IFN-gamma},
  language     = {eng},
  pages        = {11},
  title        = {The Ly49E receptor inhibits the immune control of acute Trypanosoma cruzi infection},
  url          = {http://dx.doi.org/10.3389/fimmu.2016.00472},
  volume       = {7},
  year         = {2016},
}

Chicago
Filtjens, Jessica, Nicolas Coltel, Sabrina Cencig, Sylvie Taveirne, Els Van Ammel, Aline Van Acker, Tessa Kerre, et al. 2016. “The Ly49E Receptor Inhibits the Immune Control of Acute Trypanosoma Cruzi Infection.” Frontiers in Immunology 7.
APA
Filtjens, J., Coltel, N., Cencig, S., Taveirne, S., Van Ammel, E., Van Acker, A., Kerre, T., et al. (2016). The Ly49E receptor inhibits the immune control of acute Trypanosoma cruzi infection. FRONTIERS IN IMMUNOLOGY, 7.
Vancouver
1.
Filtjens J, Coltel N, Cencig S, Taveirne S, Van Ammel E, Van Acker A, et al. The Ly49E receptor inhibits the immune control of acute Trypanosoma cruzi infection. FRONTIERS IN IMMUNOLOGY. 2016;7.
MLA
Filtjens, Jessica, Nicolas Coltel, Sabrina Cencig, et al. “The Ly49E Receptor Inhibits the Immune Control of Acute Trypanosoma Cruzi Infection.” FRONTIERS IN IMMUNOLOGY 7 (2016): n. pag. Print.