The intracellular bacterium Rickettsia rickettsii exerts an inhibitory effect on the apoptosis of tick cells
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Parasites & Vectors Open Access
RESEARCH
The intracellular bacterium Rickettsia rickettsii exerts an inhibitory effect on the apoptosis of tick cells Larissa Almeida Martins1,6, Giuseppe Palmisano1, Mauro Cortez1, Rebeca Kawahara1,7, José Mario de Freitas Balanco1, André Fujita2, Beatriz Iglesias Alonso1, Darci Moraes Barros‑Battesti3, Gloria Regina Cardoso Braz4, Lucas Tirloni5, Eliane Esteves1, Sirlei Daffre1 and Andréa Cristina Fogaça1*
Abstract Background: Rickettsia rickettsii is a tick-borne obligate intracellular bacterium that causes Rocky Mountain spotted fever, a life-threatening illness. To obtain an insight into the vector–pathogen interactions, we assessed the effects of infection with R. rickettsii on the proteome cells of the tick embryonic cell line BME26. Methods: The proteome of BME26 cells was determined by label-free high-performance liquid chromatography coupled with tandem mass spectrometry analysis. Also evaluated were the effects of infection on the activity of cas‑ pase-3, assessed by the hydrolysis of a synthetic fluorogenic substrate in enzymatic assays, and on the exposition of phosphatidyserine, evaluated by live-cell fluorescence microscopy after labeling with annexin-V. Finally, the effects of activation or inhibition of caspase-3 activity on the growth of R. rickettsii in BME26 cells was determined. Results: Tick proteins of different functional classes were modulated in a time-dependent manner by R. rickettsii infection. Regarding proteins involved in apoptosis, certain negative regulators were downregulated at the initial phase of the infection (6 h) but upregulated in the middle of the exponential phase of the bacterial growth (48 h). Microorganisms are known to be able to inhibit apoptosis of the host cell to ensure their survival and proliferation. We therefore evaluated the effects of infection on classic features of apoptotic cells and observed DNA fragmenta‑ tion exclusively in noninfected cells. Moreover, both caspase-3 activity and phosphatidylserine exposition were lower in infected than in noninfected cells. Importantly, while the activation of caspase-3 exerted a detrimental effect on rickettsial proliferation, its inhibition increased bacterial growth. Conclusions: Taken together, these results show that R. rickettsii modulates the proteome and exerts an inhibitory effect on apoptosis in tick cellsthat seems to be important to ensure cell colonization. Keywords: Apoptosis, Proteome, Rickettsiae, Tick Background Ticks are hematophagous arthropods that parasitize almost all classes of vertebrates throughout the world, resulting in the transmission of a vast list of pathogens *Correspondence: [email protected] 1 Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, SP, Brazil Full list of author information is available at the end of the article
that threaten both human and animal health [1–3]. Among tick-borne diseases, Rocky Mountain spotted fever, which is caused by the obligate intracellular bacterium Rickettsia rickettsi
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