Mutual exclusivity of hyaluronan and hyaluronidase in invasive group A Streptococcus

Article

Henningham, Anna, Yamaguchi, Masaya, Aziz, Ramy K., Kuipers, Kirsten, Buffalo, Cosmo Z., Dahesh, Samira, Choudhury, Biswa, Van Vleet, Jeremy, Yamaguchi, Yuka, Seymour, Lisa M., Ben Zakour, Nouri L., He, Lingjun, Smith, Helen V., Grimwood, Keith, Beatson, Scott A., Ghosh, Partho, Walker, Mark J., Nizet, Victor and Cole, Jason N.. 2014. "Mutual exclusivity of hyaluronan and hyaluronidase in invasive group A Streptococcus." Journal of Biological Chemistry. 289 (46), pp. 32303-32315. https://doi.org/10.1074/jbc.M114.602847
Article Title

Mutual exclusivity of hyaluronan and hyaluronidase in invasive group A Streptococcus

ERA Journal ID2230
Article CategoryArticle
AuthorsHenningham, Anna (Author), Yamaguchi, Masaya (Author), Aziz, Ramy K. (Author), Kuipers, Kirsten (Author), Buffalo, Cosmo Z. (Author), Dahesh, Samira (Author), Choudhury, Biswa (Author), Van Vleet, Jeremy (Author), Yamaguchi, Yuka (Author), Seymour, Lisa M. (Author), Ben Zakour, Nouri L. (Author), He, Lingjun (Author), Smith, Helen V. (Author), Grimwood, Keith (Author), Beatson, Scott A. (Author), Ghosh, Partho (Author), Walker, Mark J. (Author), Nizet, Victor (Author) and Cole, Jason N. (Author)
Journal TitleJournal of Biological Chemistry
Journal Citation289 (46), pp. 32303-32315
Number of Pages13
Year2014
Place of PublicationRockville, MD. United States
ISSN0021-9258
1083-351X
Digital Object Identifier (DOI)https://doi.org/10.1074/jbc.M114.602847
Web Address (URL)http://www.jbc.org/content/289/46/32303.full.pdf+html
Abstract

A recent analysis of group A Streptococcus (GAS) invasive infections in Australia has shown a predominance of M4 GAS, a serotype recently reported to lack the antiphagocytic hyaluronic acid (HA) capsule. Here, we use molecular genetics and bioinformatics techniques to characterize 17 clinical M4 isolates associated with invasive disease in children during this recent epidemiology. All M4 isolates lacked HA capsule, and whole genome sequence analysis of two isolates revealed the complete absence of the hasABC capsule biosynthesis operon. Conversely, M4 isolates possess a functional HA-degrading hyaluronate lyase (HylA) enzyme that is rendered nonfunctional in other GAS through a point mutation. Transformation with a plasmid expressing hasABC restored partial encapsulation in wild-type (WT) M4 GAS, and full encapsulation in an isogenic M4 mutant lacking HylA. However, partial encapsulation reduced binding to human complement regulatory protein C4BP, did not enhance survival in whole human blood, and did not increase virulence of WT M4 GAS in a mouse model of systemic infection. Bioinformatics analysis found no hasABC homologs in closely related species, suggesting that this operon was a recent acquisition. These data showcase a mutually exclusive interaction of HA capsule and active HylA among strains of this leading human pathogen.

Keywordsbacterial pathogenesis; group A Streptococcus; hyaluronan; hyaluronate; hyaluronate lyase; hyaluronic acid capsule; infectious disease; invasive disease; nonencapsulated; Streptococcus Pyogenes (S. Pyogenes)
ANZSRC Field of Research 2020320202. Clinical chemistry (incl. diagnostics)
320702. Medical infection agents (incl. prions)
310702. Infectious agents
Byline AffiliationsUniversity of Queensland
Osaka University, Japan
Cairo University, Egypt
Radboud University Medical Centre, Netherlands
University of California, United States
San Diego State University, United States
Department of Health, Queensland
Queensland Children's Medical Research Institute, Australia
Institution of OriginUniversity of Southern Queensland
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