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Neutrophil infiltration in co-housed littermates plays a key role in nasal transmission of Streptococcus pneumoniae in an infant mouse model

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Abstract

Transmission plays an important role in establishing pneumococcal colonization. It comprises three key events: shedding to transmit, entering into a susceptible new host, and adhering to the mucosal surface. Shedding of pneumococci from the respiratory tract of a colonized host is a pivotal step in transmission. Using a co-housed littermate mouse model, we evaluated the importance of the susceptibility to colonization of Streptococcus pneumoniae TIGR4 strain shed from index pups to non-colonized naïve contact pups. Despite sufficient pneumococcal shedding from the colonized host, S. pneumoniae was not contagious between littermates. Neutrophils infiltrated the nasal mucosa of contact pups and contributed to susceptibility of pneumococcal colonization during the course of transmission. Rejection of pneumococcal colonization in the contact pups was associated with accumulation of neutrophils in the nasal mucosa. Inflammation, characterized by neutrophil infiltration, prevents newly entering pneumococci from adhering to the respiratory epithelium in contact mice, suggesting that it plays an important role in reducing the rate of transmission in the initial response of naïve susceptible hosts to pneumococcal acquisition. The initial response of contact mice may regulate neutrophil and/or macrophage infiltration and control the acquisition of existing pneumococci.

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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

The pathological specimen processing was supported by Professor Yasuteru Muragaki at the Department of Pathology, Wakayama Medical University. We acknowledge proofreading and editing by Benjamin Phillis at the Clinical Study Support Center, Wakayama Medical University.

Funding

This work was supported in part by national grants from the Japanese Ministry of Education, Culture, Sports, Science and Technology (principal investigator Kono M, grants 17K15690, 20K08825).

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Authors

Contributions

F.K., M.K., and M.H. made substantial contributions to the conception and the design of the work. F.K. made substantial contributions to the acquisition, analysis, and interpretation of data for the work. F.K., M.K., H.S., and M.H. drafted the work or revised it critically for important intellectual content. M.H. and H.S. finally approved of the version to be published and agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Muneki Hotomi.

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Ethics approval

This study was conducted according to the guidelines outlined by National Science Foundation Animal Welfare Requirements and the Public Health Service Policy on the Human Care and Use of Laboratory Animals. It was approved by the Wakayama Medical University Institutional Animal Care and Use Committee (approval number 827).

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The authors declare no competing interests.

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Kaneko, F., Kono, M., Sunose, H. et al. Neutrophil infiltration in co-housed littermates plays a key role in nasal transmission of Streptococcus pneumoniae in an infant mouse model. Folia Microbiol 67, 45–54 (2022). https://doi.org/10.1007/s12223-021-00901-0

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