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Regulation of inflammation and protection against invasive pneumococcal infection by the long pentraxin PTX3

View ORCID ProfileRémi Porte, Rita Silva-Gomes, Charlotte Theroude, Raffaella Parente, Fatemeh Asgari, Marina Sironi, Fabio Pasqualini, Sonia Valentino, Rosanna Asselta, Camilla Recordati, Andrea Doni, Antonio Inforzato, Carlos Rodriguez-Gallego, Ignacio Obando, Elena Colino, Barbara Bottazzi, Alberto Mantovani
doi: https://doi.org/10.1101/2022.04.14.488329
Rémi Porte
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
2Department of Biomedical Sciences, Humanitas University Milan, Italy
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  • ORCID record for Rémi Porte
  • For correspondence: remi.porte@inserm.fr Barbara.Bottazzi@humanitasresearch.it Alberto.Mantovani@humanitasresearch.it
Rita Silva-Gomes
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
2Department of Biomedical Sciences, Humanitas University Milan, Italy
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Charlotte Theroude
3Infectious Diseases Service, Department of Medicine, Lausanne University Hospital and University of Lausanne, Epalinges, Switzerland
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Raffaella Parente
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
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Fatemeh Asgari
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
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Marina Sironi
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
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Fabio Pasqualini
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
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Sonia Valentino
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
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Rosanna Asselta
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
2Department of Biomedical Sciences, Humanitas University Milan, Italy
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Camilla Recordati
4Mouse and Animal Pathology Laboratory, Fondazione Filarete, Milan, Italy
5Department of Veterinary Medicine, University of Milan, Lodi, Italy
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Andrea Doni
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
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Antonio Inforzato
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
2Department of Biomedical Sciences, Humanitas University Milan, Italy
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Carlos Rodriguez-Gallego
6Department of Clinical Sciences, University Fernando Pessoa Canarias, Las Palmas de Gran Canaria, Spain
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Ignacio Obando
7Department of Pediatrics, Hospital Universitario Virgen del Rocío, Sevilla, Spain
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Elena Colino
8Department of Pediatrics, Complejo Hospitalario Universitario Insular_Materno Infantil, Las Palmas de Gran Canaria, Spain
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Barbara Bottazzi
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
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  • For correspondence: remi.porte@inserm.fr Barbara.Bottazzi@humanitasresearch.it Alberto.Mantovani@humanitasresearch.it
Alberto Mantovani
1IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy
2Department of Biomedical Sciences, Humanitas University Milan, Italy
9William Harvey Research Institute, Queen Mary University of London, Charterhouse Square, London EC1M 6BQ, UK
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  • For correspondence: remi.porte@inserm.fr Barbara.Bottazzi@humanitasresearch.it Alberto.Mantovani@humanitasresearch.it
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Abstract

Streptococcus pneumoniae is a major pathogen in children, elderly subjects and immunodeficient patients. PTX3 is a fluid phase pattern recognition molecule (PRM) involved in resistance to selected microbial agents and in regulation of inflammation. The present study was designed to assess the role of PTX3 in invasive pneumococcal infection. In a murine model of invasive pneumococcal infection, PTX3 was strongly induced in non-hematopoietic (particularly, endothelial) cells. The IL-1β/MyD88 axis played a major role in regulation of the Ptx3 gene expression. Ptx3-/- mice were more susceptible to invasive pneumococcal infection. Although high concentrations of PTX3 had opsonic activity in vitro, no evidence of PTX3-enhanced phagocytosis was obtained in vivo. In contrast, Ptx3-deficient mice showed enhanced recruitment of neutrophils and inflammation. Using P-selectin deficient mice, we found that protection against pneumococcus was dependent upon PTX3-mediated regulation of neutrophil inflammation. In humans, PTX3 genetic polymorphisms were associated with invasive pneumococcal infections. Thus, this fluid phase PRM plays an important role in tuning inflammation and resistance against invasive pneumococcal infection.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted April 15, 2022.
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Regulation of inflammation and protection against invasive pneumococcal infection by the long pentraxin PTX3
Rémi Porte, Rita Silva-Gomes, Charlotte Theroude, Raffaella Parente, Fatemeh Asgari, Marina Sironi, Fabio Pasqualini, Sonia Valentino, Rosanna Asselta, Camilla Recordati, Andrea Doni, Antonio Inforzato, Carlos Rodriguez-Gallego, Ignacio Obando, Elena Colino, Barbara Bottazzi, Alberto Mantovani
bioRxiv 2022.04.14.488329; doi: https://doi.org/10.1101/2022.04.14.488329
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Regulation of inflammation and protection against invasive pneumococcal infection by the long pentraxin PTX3
Rémi Porte, Rita Silva-Gomes, Charlotte Theroude, Raffaella Parente, Fatemeh Asgari, Marina Sironi, Fabio Pasqualini, Sonia Valentino, Rosanna Asselta, Camilla Recordati, Andrea Doni, Antonio Inforzato, Carlos Rodriguez-Gallego, Ignacio Obando, Elena Colino, Barbara Bottazzi, Alberto Mantovani
bioRxiv 2022.04.14.488329; doi: https://doi.org/10.1101/2022.04.14.488329

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