Virulent Pseudomonas aeruginosa infection converts antimicrobial amyloids into cytotoxic prions
Pseudomonas aeruginosa infection elicits the production of cytotoxic amyloids from lung endothelium, yet molecular mechanisms of host‐pathogen interaction that underlie the amyloid production are not well understood. We examined the importance of type III secretion system (T3SS) effectors in the pro...
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Published in | The FASEB journal Vol. 34; no. 7; pp. 9156 - 9179 |
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Main Authors | , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
01.07.2020
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Abstract | Pseudomonas aeruginosa infection elicits the production of cytotoxic amyloids from lung endothelium, yet molecular mechanisms of host‐pathogen interaction that underlie the amyloid production are not well understood. We examined the importance of type III secretion system (T3SS) effectors in the production of cytotoxic amyloids. P aeruginosa possessing a functional T3SS and effectors induced the production and release of cytotoxic amyloids from lung endothelium, including beta amyloid, and tau. T3SS effector intoxication was sufficient to generate cytotoxic amyloid release, yet intoxication with exoenzyme Y (ExoY) alone or together with exoenzymes S and T (ExoS/T/Y) generated the most virulent amyloids. Infection with lab and clinical strains engendered cytotoxic amyloids that were capable of being propagated in endothelial cell culture and passed to naïve cells, indicative of a prion strain. Conversely, T3SS‐incompetent P aeruginosa infection produced non‐cytotoxic amyloids with antimicrobial properties. These findings provide evidence that (1) endothelial intoxication with ExoY is sufficient to elicit self‐propagating amyloid cytotoxins during infection, (2) pulmonary endothelium contributes to innate immunity by generating antimicrobial amyloids in response to bacterial infection, and (3) ExoY contributes to the virulence arsenal of P aeruginosa through the subversion of endothelial amyloid host‐defense to promote a lung endothelial‐derived cytotoxic proteinopathy. |
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AbstractList | Pseudomonas aeruginosa infection elicits the production of cytotoxic amyloids from lung endothelium, yet molecular mechanisms of host‐pathogen interaction that underlie the amyloid production are not well understood. We examined the importance of type III secretion system (T3SS) effectors in the production of cytotoxic amyloids. P aeruginosa possessing a functional T3SS and effectors induced the production and release of cytotoxic amyloids from lung endothelium, including beta amyloid, and tau. T3SS effector intoxication was sufficient to generate cytotoxic amyloid release, yet intoxication with exoenzyme Y (ExoY) alone or together with exoenzymes S and T (ExoS/T/Y) generated the most virulent amyloids. Infection with lab and clinical strains engendered cytotoxic amyloids that were capable of being propagated in endothelial cell culture and passed to naïve cells, indicative of a prion strain. Conversely, T3SS‐incompetent P aeruginosa infection produced non‐cytotoxic amyloids with antimicrobial properties. These findings provide evidence that (1) endothelial intoxication with ExoY is sufficient to elicit self‐propagating amyloid cytotoxins during infection, (2) pulmonary endothelium contributes to innate immunity by generating antimicrobial amyloids in response to bacterial infection, and (3) ExoY contributes to the virulence arsenal of P aeruginosa through the subversion of endothelial amyloid host‐defense to promote a lung endothelial‐derived cytotoxic proteinopathy. |
Author | Balczon, Ron Pittet, Jean‐Francois Simmons, Autumn Moser, Stephen A. Housley, Nicole Audia, Jonathon P. Stevens, Troy Frank, Dara W. Alexeyev, Mikhail Crawford, Michaela Madera, Kayla Francis, Christopher Michael Piechocki, Scott Wagener, Brant M. Gwin, Meredith Voth, Sarah |
Author_xml | – sequence: 1 givenname: Sarah orcidid: 0000-0003-3796-7154 surname: Voth fullname: Voth, Sarah organization: University of South Alabama – sequence: 2 givenname: Meredith surname: Gwin fullname: Gwin, Meredith organization: University of South Alabama – sequence: 3 givenname: Christopher Michael surname: Francis fullname: Francis, Christopher Michael organization: University of South Alabama – sequence: 4 givenname: Ron surname: Balczon fullname: Balczon, Ron organization: University of South Alabama – sequence: 5 givenname: Dara W. surname: Frank fullname: Frank, Dara W. organization: Medical College of Wisconsin – sequence: 6 givenname: Jean‐Francois surname: Pittet fullname: Pittet, Jean‐Francois organization: University of Alabama at Birmingham School of Medicine – sequence: 7 givenname: Brant M. surname: Wagener fullname: Wagener, Brant M. organization: University of Alabama at Birmingham School of Medicine – sequence: 8 givenname: Stephen A. surname: Moser fullname: Moser, Stephen A. organization: University of Alabama at Birmingham School of Medicine – sequence: 9 givenname: Mikhail surname: Alexeyev fullname: Alexeyev, Mikhail organization: University of South Alabama – sequence: 10 givenname: Nicole surname: Housley fullname: Housley, Nicole organization: University of South Alabama – sequence: 11 givenname: Jonathon P. surname: Audia fullname: Audia, Jonathon P. organization: University of South Alabama – sequence: 12 givenname: Scott surname: Piechocki fullname: Piechocki, Scott organization: University of South Alabama – sequence: 13 givenname: Kayla surname: Madera fullname: Madera, Kayla organization: University of South Alabama – sequence: 14 givenname: Autumn surname: Simmons fullname: Simmons, Autumn organization: University of South Alabama – sequence: 15 givenname: Michaela surname: Crawford fullname: Crawford, Michaela organization: University of South Alabama – sequence: 16 givenname: Troy surname: Stevens fullname: Stevens, Troy email: tstevens@southalabama.edu organization: University of South Alabama |
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Keywords | nosocomial pneumonia prion amyloid beta (Aβ) tau (τ) exoenzyme Y (ExoY) |
Language | English |
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Notes | Kayla Madera and Autumn Simmons contributed equally to this study. |
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SubjectTerms | Amyloid - chemistry amyloid beta (Aβ) Animals Anti-Bacterial Agents - pharmacology Bacterial Proteins - immunology Cytotoxins - pharmacology Endothelial Cells - drug effects Endothelial Cells - immunology Endothelial Cells - microbiology exoenzyme Y (ExoY) Female Host-Pathogen Interactions Humans Lung - drug effects Lung - immunology Lung - microbiology Male nosocomial pneumonia prion Prions - pharmacology Pseudomonas aeruginosa - isolation & purification Pseudomonas Infections - drug therapy Pseudomonas Infections - immunology Pseudomonas Infections - microbiology Rats Rats, Inbred F344 Rats, Sprague-Dawley tau (τ) Virulence - drug effects |
Title | Virulent Pseudomonas aeruginosa infection converts antimicrobial amyloids into cytotoxic prions |
URI | https://onlinelibrary.wiley.com/doi/abs/10.1096%2Ffj.202000051RRR https://www.ncbi.nlm.nih.gov/pubmed/32413239 |
Volume | 34 |
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