S. aureus drives itch and scratch-induced skin damage through a V8 protease-PAR1 axis

Itch is an unpleasant sensation that evokes a desire to scratch. The skin barrier is constantly exposed to microbes and their products. However, the role of microbes in itch generation is unknown. Here, we show that Staphylococcus aureus, a bacterial pathogen associated with itchy skin diseases, dir...

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Published in:	Cell Vol. 186; no. 24; p. 5375
Main Authors:	Deng, Liwen, Costa, Flavia, Blake, Kimbria J, Choi, Samantha, Chandrabalan, Arundhasa, Yousuf, Muhammad Saad, Shiers, Stephanie, Dubreuil, Daniel, Vega-Mendoza, Daniela, Rolland, Corinne, Deraison, Celine, Voisin, Tiphaine, Bagood, Michelle D, Wesemann, Lucia, Frey, Abigail M, Palumbo, Joseph S, Wainger, Brian J, Gallo, Richard L, Leyva-Castillo, Juan-Manuel, Vergnolle, Nathalie, Price, Theodore J, Ramachandran, Rithwik, Horswill, Alexander R, Chiu, Isaac M
Format:	Journal Article
Language:	English
Published:	United States 22.11.2023
Subjects:	Animals Humans Mice Peptide Hydrolases - metabolism Pruritus - microbiology Receptor, PAR-1 - metabolism Staphylococcal Infections - microbiology Staphylococcal Infections - pathology Staphylococcus aureus - enzymology Staphylococcus aureus - pathogenicity Staphylococcus aureus - physiology itch pruriceptor PAR1 proteinase-activated receptor V8 protease microbe Staphylococcus aureus
ISSN:	1097-4172, 1097-4172
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Abstract	Itch is an unpleasant sensation that evokes a desire to scratch. The skin barrier is constantly exposed to microbes and their products. However, the role of microbes in itch generation is unknown. Here, we show that Staphylococcus aureus, a bacterial pathogen associated with itchy skin diseases, directly activates pruriceptor sensory neurons to drive itch. Epicutaneous S. aureus exposure causes robust itch and scratch-induced damage. By testing multiple isogenic bacterial mutants for virulence factors, we identify the S. aureus serine protease V8 as a critical mediator in evoking spontaneous itch and alloknesis. V8 cleaves proteinase-activated receptor 1 (PAR1) on mouse and human sensory neurons. Targeting PAR1 through genetic deficiency, small interfering RNA (siRNA) knockdown, or pharmacological blockade decreases itch and skin damage caused by V8 and S. aureus exposure. Thus, we identify a mechanism of action for a pruritogenic bacterial factor and demonstrate the potential of inhibiting V8-PAR1 signaling to treat itch.
AbstractList	Itch is an unpleasant sensation that evokes a desire to scratch. The skin barrier is constantly exposed to microbes and their products. However, the role of microbes in itch generation is unknown. Here, we show that Staphylococcus aureus, a bacterial pathogen associated with itchy skin diseases, directly activates pruriceptor sensory neurons to drive itch. Epicutaneous S. aureus exposure causes robust itch and scratch-induced damage. By testing multiple isogenic bacterial mutants for virulence factors, we identify the S. aureus serine protease V8 as a critical mediator in evoking spontaneous itch and alloknesis. V8 cleaves proteinase-activated receptor 1 (PAR1) on mouse and human sensory neurons. Targeting PAR1 through genetic deficiency, small interfering RNA (siRNA) knockdown, or pharmacological blockade decreases itch and skin damage caused by V8 and S. aureus exposure. Thus, we identify a mechanism of action for a pruritogenic bacterial factor and demonstrate the potential of inhibiting V8-PAR1 signaling to treat itch.Itch is an unpleasant sensation that evokes a desire to scratch. The skin barrier is constantly exposed to microbes and their products. However, the role of microbes in itch generation is unknown. Here, we show that Staphylococcus aureus, a bacterial pathogen associated with itchy skin diseases, directly activates pruriceptor sensory neurons to drive itch. Epicutaneous S. aureus exposure causes robust itch and scratch-induced damage. By testing multiple isogenic bacterial mutants for virulence factors, we identify the S. aureus serine protease V8 as a critical mediator in evoking spontaneous itch and alloknesis. V8 cleaves proteinase-activated receptor 1 (PAR1) on mouse and human sensory neurons. Targeting PAR1 through genetic deficiency, small interfering RNA (siRNA) knockdown, or pharmacological blockade decreases itch and skin damage caused by V8 and S. aureus exposure. Thus, we identify a mechanism of action for a pruritogenic bacterial factor and demonstrate the potential of inhibiting V8-PAR1 signaling to treat itch. Itch is an unpleasant sensation that evokes a desire to scratch. The skin barrier is constantly exposed to microbes and their products. However, the role of microbes in itch generation is unknown. Here, we show that Staphylococcus aureus, a bacterial pathogen associated with itchy skin diseases, directly activates pruriceptor sensory neurons to drive itch. Epicutaneous S. aureus exposure causes robust itch and scratch-induced damage. By testing multiple isogenic bacterial mutants for virulence factors, we identify the S. aureus serine protease V8 as a critical mediator in evoking spontaneous itch and alloknesis. V8 cleaves proteinase-activated receptor 1 (PAR1) on mouse and human sensory neurons. Targeting PAR1 through genetic deficiency, small interfering RNA (siRNA) knockdown, or pharmacological blockade decreases itch and skin damage caused by V8 and S. aureus exposure. Thus, we identify a mechanism of action for a pruritogenic bacterial factor and demonstrate the potential of inhibiting V8-PAR1 signaling to treat itch.
Author	Deraison, Celine Palumbo, Joseph S Yousuf, Muhammad Saad Choi, Samantha Ramachandran, Rithwik Chiu, Isaac M Vergnolle, Nathalie Price, Theodore J Dubreuil, Daniel Leyva-Castillo, Juan-Manuel Costa, Flavia Frey, Abigail M Chandrabalan, Arundhasa Vega-Mendoza, Daniela Rolland, Corinne Blake, Kimbria J Horswill, Alexander R Deng, Liwen Bagood, Michelle D Wainger, Brian J Shiers, Stephanie Voisin, Tiphaine Wesemann, Lucia Gallo, Richard L
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SubjectTerms	Animals Humans Mice Peptide Hydrolases - metabolism Pruritus - microbiology Receptor, PAR-1 - metabolism Staphylococcal Infections - microbiology Staphylococcal Infections - pathology Staphylococcus aureus - enzymology Staphylococcus aureus - pathogenicity Staphylococcus aureus - physiology
Title	S. aureus drives itch and scratch-induced skin damage through a V8 protease-PAR1 axis
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