A Staphylococcus pro-apoptotic peptide induces acute exacerbation of pulmonary fibrosis

Corina N. D’alessandro-gabazza; Tetsu Kobayashi; Taro Yasuma; Masaaki Toda; Heejin Kim; Hajime Fujimoto; Osamu Hataji; Atsuro Takeshita; Kota Nishihama; Tomohito Okano; Yuko Okano; Yoichi Nishii; Atsushi Tomaru; Kentaro Fujiwara; Valeria Fridman D’alessandro; Ahmed M. Abdel-hamid; Yudong Ren; Gabriel V. Pereira; Christy L. Wright; Alvaro Hernandez; Christopher J. Fields; Peter M. Yau; Shujie Wang; Akira Mizoguchi; Masayuki Fukumura; Junpei Ohtsuka; Tetsuya Nosaka; Kensuke Kataoka; Yasuhiro Kondoh; Jing Wu; Hirokazu Kawagishi; Yutaka Yano; Roderick I. Mackie; Isaac Cann; Esteban C. Gabazza

doi:10.1038/s41467-020-15344-3

A Staphylococcus pro-apoptotic peptide induces acute exacerbation of pulmonary fibrosis

Corina N. D’alessandro-gabazza, Tetsu Kobayashi, Taro Yasuma, Masaaki Toda, Heejin Kim, Hajime Fujimoto, Osamu Hataji, Atsuro Takeshita, Kota Nishihama, Tomohito Okano, Yuko Okano, Yoichi Nishii, Atsushi Tomaru, Kentaro Fujiwara, Valeria Fridman D’alessandro, Ahmed M. Abdel-hamid, Yudong Ren, Gabriel V. Pereira, Christy L. Wright, Alvaro HernandezChristopher J. Fields, Peter M. Yau, Shujie Wang, Akira Mizoguchi, Masayuki Fukumura, Junpei Ohtsuka, Tetsuya Nosaka, Kensuke Kataoka, Yasuhiro Kondoh, Jing Wu, Hirokazu Kawagishi, Yutaka Yano, Roderick I. Mackie, Isaac Cann, Esteban C. Gabazza

Research output: Contribution to journal › Article › peer-review

Abstract

Idiopathic pulmonary fibrosis (IPF) is a chronic and fatal disease of unknown etiology; however, apoptosis of lung alveolar epithelial cells plays a role in disease progression. This intractable disease is associated with increased abundance of Staphylococcus and Streptococcus in the lungs, yet their roles in disease pathogenesis remain elusive. Here, we report that Staphylococcus nepalensis releases corisin, a peptide conserved in diverse staphylococci, to induce apoptosis of lung epithelial cells. The disease in mice exhibits acute exacerbation after intrapulmonary instillation of corisin or after lung infection with corisin-harboring S. nepalensis compared to untreated mice or mice infected with bacteria lacking corisin. Correspondingly, the lung corisin levels are significantly increased in human IPF patients with acute exacerbation compared to patients without disease exacerbation. Our results suggest that bacteria shedding corisin are involved in acute exacerbation of IPF, yielding insights to the molecular basis for the elevation of staphylococci in pulmonary fibrosis.

Original language	English (US)
Article number	1539
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-15344-3
State	Published - Dec 1 2020

Keywords

microbiome
translational research

ASJC Scopus subject areas

Physics and Astronomy(all)
Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)

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10.1038/s41467-020-15344-3License: CC BY

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D’alessandro-gabazza, C. N., Kobayashi, T., Yasuma, T., Toda, M., Kim, H., Fujimoto, H., Hataji, O., Takeshita, A., Nishihama, K., Okano, T., Okano, Y., Nishii, Y., Tomaru, A., Fujiwara, K., D’alessandro, V. F., Abdel-hamid, A. M., Ren, Y., Pereira, G. V., Wright, C. L., ... Gabazza, E. C. (2020). A Staphylococcus pro-apoptotic peptide induces acute exacerbation of pulmonary fibrosis. Nature Communications, 11(1), Article 1539. https://doi.org/10.1038/s41467-020-15344-3

D’alessandro-gabazza, CN, Kobayashi, T, Yasuma, T, Toda, M, Kim, H, Fujimoto, H, Hataji, O, Takeshita, A, Nishihama, K, Okano, T, Okano, Y, Nishii, Y, Tomaru, A, Fujiwara, K, D’alessandro, VF, Abdel-hamid, AM, Ren, Y, Pereira, GV, Wright, CL, Hernandez, A , Fields, CJ, Yau, PM, Wang, S, Mizoguchi, A, Fukumura, M, Ohtsuka, J, Nosaka, T, Kataoka, K, Kondoh, Y, Wu, J, Kawagishi, H, Yano, Y, Mackie, RI , Cann, I & Gabazza, EC 2020, 'A Staphylococcus pro-apoptotic peptide induces acute exacerbation of pulmonary fibrosis', Nature Communications, vol. 11, no. 1, 1539. https://doi.org/10.1038/s41467-020-15344-3

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title = "A Staphylococcus pro-apoptotic peptide induces acute exacerbation of pulmonary fibrosis",

abstract = "Idiopathic pulmonary fibrosis (IPF) is a chronic and fatal disease of unknown etiology; however, apoptosis of lung alveolar epithelial cells plays a role in disease progression. This intractable disease is associated with increased abundance of Staphylococcus and Streptococcus in the lungs, yet their roles in disease pathogenesis remain elusive. Here, we report that Staphylococcus nepalensis releases corisin, a peptide conserved in diverse staphylococci, to induce apoptosis of lung epithelial cells. The disease in mice exhibits acute exacerbation after intrapulmonary instillation of corisin or after lung infection with corisin-harboring S. nepalensis compared to untreated mice or mice infected with bacteria lacking corisin. Correspondingly, the lung corisin levels are significantly increased in human IPF patients with acute exacerbation compared to patients without disease exacerbation. Our results suggest that bacteria shedding corisin are involved in acute exacerbation of IPF, yielding insights to the molecular basis for the elevation of staphylococci in pulmonary fibrosis.",

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author = "D{\textquoteright}alessandro-gabazza, {Corina N.} and Tetsu Kobayashi and Taro Yasuma and Masaaki Toda and Heejin Kim and Hajime Fujimoto and Osamu Hataji and Atsuro Takeshita and Kota Nishihama and Tomohito Okano and Yuko Okano and Yoichi Nishii and Atsushi Tomaru and Kentaro Fujiwara and D{\textquoteright}alessandro, {Valeria Fridman} and Abdel-hamid, {Ahmed M.} and Yudong Ren and Pereira, {Gabriel V.} and Wright, {Christy L.} and Alvaro Hernandez and Fields, {Christopher J.} and Yau, {Peter M.} and Shujie Wang and Akira Mizoguchi and Masayuki Fukumura and Junpei Ohtsuka and Tetsuya Nosaka and Kensuke Kataoka and Yasuhiro Kondoh and Jing Wu and Hirokazu Kawagishi and Yutaka Yano and Mackie, {Roderick I.} and Isaac Cann and Gabazza, {Esteban C.}",

note = "Funding Information: This research was supported in part by the Ministry of Education, Culture, Sports, Science, and Technology of Japan (Kakenhi No 17K08442 and 18K08175), and in part by funding support for the Microbiome Metabolic Engineering Theme (Carl R. Woose Institute for Genomic Biology) and by the College of Agricultural, Consumer and Environmental Sciences Office of International Programs, University of Illinois at Urbana-Champaign. The funders had no role in study design, data analysis, decision to publish, or preparation of the manuscript. We would like to thank Lou Ann Miller (Frederick Seitz Material Research Lab, UIUC) and Miyuki Ieda (Mie University School of Medicine) for technical support.",

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AU - D’alessandro-gabazza, Corina N.

AU - Kobayashi, Tetsu

AU - Yasuma, Taro

AU - Toda, Masaaki

AU - Kim, Heejin

AU - Fujimoto, Hajime

AU - Hataji, Osamu

AU - Takeshita, Atsuro

AU - Nishihama, Kota

AU - Okano, Tomohito

AU - Okano, Yuko

AU - Nishii, Yoichi

AU - Tomaru, Atsushi

AU - Fujiwara, Kentaro

AU - D’alessandro, Valeria Fridman

AU - Abdel-hamid, Ahmed M.

AU - Ren, Yudong

AU - Pereira, Gabriel V.

AU - Wright, Christy L.

AU - Hernandez, Alvaro

AU - Fields, Christopher J.

AU - Yau, Peter M.

AU - Wang, Shujie

AU - Mizoguchi, Akira

AU - Fukumura, Masayuki

AU - Ohtsuka, Junpei

AU - Nosaka, Tetsuya

AU - Kataoka, Kensuke

AU - Kondoh, Yasuhiro

AU - Wu, Jing

AU - Kawagishi, Hirokazu

AU - Yano, Yutaka

AU - Mackie, Roderick I.

AU - Cann, Isaac

AU - Gabazza, Esteban C.

N1 - Funding Information: This research was supported in part by the Ministry of Education, Culture, Sports, Science, and Technology of Japan (Kakenhi No 17K08442 and 18K08175), and in part by funding support for the Microbiome Metabolic Engineering Theme (Carl R. Woose Institute for Genomic Biology) and by the College of Agricultural, Consumer and Environmental Sciences Office of International Programs, University of Illinois at Urbana-Champaign. The funders had no role in study design, data analysis, decision to publish, or preparation of the manuscript. We would like to thank Lou Ann Miller (Frederick Seitz Material Research Lab, UIUC) and Miyuki Ieda (Mie University School of Medicine) for technical support.

PY - 2020/12/1

Y1 - 2020/12/1

N2 - Idiopathic pulmonary fibrosis (IPF) is a chronic and fatal disease of unknown etiology; however, apoptosis of lung alveolar epithelial cells plays a role in disease progression. This intractable disease is associated with increased abundance of Staphylococcus and Streptococcus in the lungs, yet their roles in disease pathogenesis remain elusive. Here, we report that Staphylococcus nepalensis releases corisin, a peptide conserved in diverse staphylococci, to induce apoptosis of lung epithelial cells. The disease in mice exhibits acute exacerbation after intrapulmonary instillation of corisin or after lung infection with corisin-harboring S. nepalensis compared to untreated mice or mice infected with bacteria lacking corisin. Correspondingly, the lung corisin levels are significantly increased in human IPF patients with acute exacerbation compared to patients without disease exacerbation. Our results suggest that bacteria shedding corisin are involved in acute exacerbation of IPF, yielding insights to the molecular basis for the elevation of staphylococci in pulmonary fibrosis.

AB - Idiopathic pulmonary fibrosis (IPF) is a chronic and fatal disease of unknown etiology; however, apoptosis of lung alveolar epithelial cells plays a role in disease progression. This intractable disease is associated with increased abundance of Staphylococcus and Streptococcus in the lungs, yet their roles in disease pathogenesis remain elusive. Here, we report that Staphylococcus nepalensis releases corisin, a peptide conserved in diverse staphylococci, to induce apoptosis of lung epithelial cells. The disease in mice exhibits acute exacerbation after intrapulmonary instillation of corisin or after lung infection with corisin-harboring S. nepalensis compared to untreated mice or mice infected with bacteria lacking corisin. Correspondingly, the lung corisin levels are significantly increased in human IPF patients with acute exacerbation compared to patients without disease exacerbation. Our results suggest that bacteria shedding corisin are involved in acute exacerbation of IPF, yielding insights to the molecular basis for the elevation of staphylococci in pulmonary fibrosis.

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A Staphylococcus pro-apoptotic peptide induces acute exacerbation of pulmonary fibrosis

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