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Non-classical ProIL-1beta activation during mammary gland infection is pathogen-dependent but caspase-1 independent

Koen Breyne UGent, Steven Cool, Dieter Demon UGent, Kristel Demeyere UGent, Tom Vandenberghe UGent, Peter Vandenabeele UGent, Harald Carlsen, Wim Van Den Broeck UGent, Niek Sanders UGent and Evelyne Meyer UGent (2014) PLOS ONE. 9(8).
abstract
Infection of the mammary gland with live bacteria elicits a pathogen-specific host inflammatory response. To study these host-pathogen interactions wild type mice, NF-kappaB reporter mice as well as caspase-1 and IL-1beta knockout mice were intramammarily challenged with Escherichia coli (E. coli) and Staphylococcus aureus (S. aureus). The murine mastitis model allowed to compare the kinetics of the induced cytokine protein profiles and their underlying pathways. In vivo and ex vivo imaging showed that E. coli rapidly induced NF-kappaB inflammatory signaling concomitant with high mammary levels of TNF-alpha, IL-1 alpha and MCP-1 as determined by multiplex analysis. In contrast, an equal number of S. aureus bacteria induced a low NF-kappaB activity concomitant with high mammary levels of the classical IL-1beta fragment. These quantitative and qualitative differences in local inflammatory mediators resulted in an earlier neutrophil influx and in a more extensive alveolar damage post-infection with E. coli compared to S. aureus. Western blot analysis revealed that the inactive proIL-1beta precursor was processed into pathogen-specific IL-1beta fragmentation patterns as confirmed with IL-1beta knockout animals. Additionally, caspase-1 knockout animals allowed to investigate whether IL-1beta maturation depended on the conventional inflammasome pathway. The lack of caspase-1 did not prevent extensive proIL-1beta fragmentation by either of S. aureus or E. coli. These non-classical IL-1beta patterns were likely caused by different proteases and suggest a sentinel function of IL-1beta during mammary gland infection. Thus, a key signaling nodule can be defined in the differential host innate immune defense upon E. coli versus S. aureus mammary gland infection, which is independent of caspase-1.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
AUREUS-INDUCED MASTITIS, STAPHYLOCOCCUS-AUREUS, INNATE IMMUNE-RESPONSES, NF-KAPPA-B, ESCHERICHIA-COLI, EPITHELIAL-CELLS, MURINE MODEL, MATRIX METALLOPROTEINASES, ALVEOLAR MACROPHAGES, BOVINE NEUTROPHILS
journal title
PLOS ONE
PLoS One
volume
9
issue
8
article number
e105680
pages
12 pages
Web of Science type
Article
Web of Science id
000340880900042
JCR category
MULTIDISCIPLINARY SCIENCES
JCR impact factor
3.234 (2014)
JCR rank
9/57 (2014)
JCR quartile
1 (2014)
ISSN
1932-6203
DOI
10.1371/journal.pone.0105680
language
English
UGent publication?
yes
classification
A1
copyright statement
I have retained and own the full copyright for this publication
id
5785011
handle
http://hdl.handle.net/1854/LU-5785011
date created
2014-12-17 15:23:33
date last changed
2016-12-21 15:42:41
@article{5785011,
  abstract     = {Infection of the mammary gland with live bacteria elicits a pathogen-specific host inflammatory response. To study these host-pathogen interactions wild type mice, NF-kappaB reporter mice as well as caspase-1 and IL-1beta knockout mice were intramammarily challenged with Escherichia coli (E. coli) and Staphylococcus aureus (S. aureus). The murine mastitis model allowed to compare the kinetics of the induced cytokine protein profiles and their underlying pathways. In vivo and ex vivo imaging showed that E. coli rapidly induced NF-kappaB inflammatory signaling concomitant with high mammary levels of TNF-alpha, IL-1 alpha and MCP-1 as determined by multiplex analysis. In contrast, an equal number of S. aureus bacteria induced a low NF-kappaB activity concomitant with high mammary levels of the classical IL-1beta fragment. These quantitative and qualitative differences in local inflammatory mediators resulted in an earlier neutrophil influx and in a more extensive alveolar damage post-infection with E. coli compared to S. aureus. Western blot analysis revealed that the inactive proIL-1beta precursor was processed into pathogen-specific IL-1beta fragmentation patterns as confirmed with IL-1beta knockout animals. Additionally, caspase-1 knockout animals allowed to investigate whether IL-1beta maturation depended on the conventional inflammasome pathway. The lack of caspase-1 did not prevent extensive proIL-1beta fragmentation by either of S. aureus or E. coli. These non-classical IL-1beta patterns were likely caused by different proteases and suggest a sentinel function of IL-1beta during mammary gland infection. Thus, a key signaling nodule can be defined in the differential host innate immune defense upon E. coli versus S. aureus mammary gland infection, which is independent of caspase-1.},
  articleno    = {e105680},
  author       = {Breyne, Koen and Cool, Steven and Demon, Dieter and Demeyere, Kristel and Vandenberghe, Tom and Vandenabeele, Peter and Carlsen, Harald and Van Den Broeck, Wim and Sanders, Niek and Meyer, Evelyne},
  issn         = {1932-6203},
  journal      = {PLOS ONE},
  keyword      = {AUREUS-INDUCED MASTITIS,STAPHYLOCOCCUS-AUREUS,INNATE IMMUNE-RESPONSES,NF-KAPPA-B,ESCHERICHIA-COLI,EPITHELIAL-CELLS,MURINE MODEL,MATRIX METALLOPROTEINASES,ALVEOLAR MACROPHAGES,BOVINE NEUTROPHILS},
  language     = {eng},
  number       = {8},
  pages        = {12},
  title        = {Non-classical ProIL-1beta activation during mammary gland infection is pathogen-dependent but caspase-1 independent},
  url          = {http://dx.doi.org/10.1371/journal.pone.0105680},
  volume       = {9},
  year         = {2014},
}

Chicago
Breyne, Koen, Steven Cool, Dieter Demon, Kristel Demeyere, Tom Vandenberghe, Peter Vandenabeele, Harald Carlsen, Wim Van Den Broeck, Niek Sanders, and Evelyne Meyer. 2014. “Non-classical ProIL-1beta Activation During Mammary Gland Infection Is Pathogen-dependent but Caspase-1 Independent.” Plos One 9 (8).
APA
Breyne, K., Cool, S., Demon, D., Demeyere, K., Vandenberghe, T., Vandenabeele, P., Carlsen, H., et al. (2014). Non-classical ProIL-1beta activation during mammary gland infection is pathogen-dependent but caspase-1 independent. PLOS ONE, 9(8).
Vancouver
1.
Breyne K, Cool S, Demon D, Demeyere K, Vandenberghe T, Vandenabeele P, et al. Non-classical ProIL-1beta activation during mammary gland infection is pathogen-dependent but caspase-1 independent. PLOS ONE. 2014;9(8).
MLA
Breyne, Koen, Steven Cool, Dieter Demon, et al. “Non-classical ProIL-1beta Activation During Mammary Gland Infection Is Pathogen-dependent but Caspase-1 Independent.” PLOS ONE 9.8 (2014): n. pag. Print.