Revisiting Ehrlichia ruminantium Replication Cycle Using Proteomics: The Host and the Bacterium Perspectives

The Rickettsiales Ehrlichia ruminantium, the causal agent of the fatal tick-borne disease Heartwater, induces severe damage to the vascular endothelium in ruminants. Nevertheless, E. ruminantium-induced pathobiology remains largely unknown. Our work paves the way for understanding this phenomenon by...

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Bibliographic Details
Published in:Microorganisms (Basel) 2021-05, Vol.9 (6), p.1144
Main Authors: Marcelino, Isabel, Holzmuller, Philippe, Coelho, Ana, Mazzucchelli, Gabriel, Fernandez, Bernard, Vachiéry, Nathalie
Format: Article
Language:English
Subjects:
Albumins
Antibiotics
Aorta
Bacteria
bacterial life cycle
Biomarkers
Biotin
Coronary artery disease
Coronary vessels
Data analysis
differential protein expression
Ehrlichia ruminantium
Endothelial cells
Endothelium
Experiments
Heart diseases
Heartwater fever
host response
Immune response
Immune response (cell-mediated)
immunomodulation
Infections
Life Sciences
Parasitic diseases
Phosphatase
Proteins
Proteomics
Replication
Software
Tick-borne diseases
Two dimensional analysis
Virulence
Virulence factors
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Summary:The Rickettsiales Ehrlichia ruminantium, the causal agent of the fatal tick-borne disease Heartwater, induces severe damage to the vascular endothelium in ruminants. Nevertheless, E. ruminantium-induced pathobiology remains largely unknown. Our work paves the way for understanding this phenomenon by using quantitative proteomic analyses (2D-DIGE-MS/MS, 1DE-nanoLC-MS/MS and biotin-nanoUPLC-MS/MS) of host bovine aorta endothelial cells (BAE) during the in vitro bacterium intracellular replication cycle. We detect 265 bacterial proteins (including virulence factors), at all time-points of the E. ruminantium replication cycle, highlighting a dynamic bacterium–host interaction. We show that E. ruminantium infection modulates the expression of 433 host proteins: 98 being over-expressed, 161 under-expressed, 140 detected only in infected BAE cells and 34 exclusively detected in non-infected cells. Cystoscape integrated data analysis shows that these proteins lead to major changes in host cell immune responses, host cell metabolism and vesicle trafficking, with a clear involvement of inflammation-related proteins in this process. Our findings led to the first model of E. ruminantium infection in host cells in vitro, and we highlight potential biomarkers of E. ruminantium infection in endothelial cells (such as ROCK1, TMEM16K, Albumin and PTPN1), which may be important to further combat Heartwater, namely by developing non-antibiotic-based strategies.
ISSN:2076-2607
2076-2607
DOI:10.3390/microorganisms9061144