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Research Paper

Galleria mellonella as an infection model for the multi-host pathogen Streptococcus agalactiae reflects hypervirulence of strains associated with human invasive disease

, , ORCID Icon, ORCID Icon &
Pages 600-609 | Received 23 Jan 2019, Accepted 07 Jun 2019, Published online: 24 Jun 2019

References

  • Barkema HW, Green MJ, Bradley AJ, et al. Invited review: the role of contagious disease in udder health. J Dairy Sci. 2009;92:4717–4729.
  • Robinson JA, Meyer FP. Streptococcal fish pathogen. J Bacteriol. 1966;92:512.
  • Kannika K, Pisuttharachai D, Srisapoome P, et al. Molecular serotyping, virulence gene profiling and pathogenicity of Streptococcus agalactiae isolated from tilapia farms in Thailand by multiplex PCR. J Appl Microbiol. 2017;122:1497–1507.
  • Soto E, Wang R, Wiles J, et al. Characterization of isolates of Streptococcus agalactiae from diseased farmed and wild marine fish from the U.S. Gulf Coast, Latin America, and Thailand. J Aquat Anim Health. 2015;27:123–134.
  • Verner‐Jeffreys DW, Wallis TJ, Cano Cejas I, et al. Streptococcus agalactiae Multilocus sequence type 261 is associated with mortalities in the emerging Ghanaian tilapia industry. J Fish Dis. 2017;41:175–179.
  • Liu G, Zhu J, Chen K, et al. Development of Streptococcus agalactiae vaccines for tilapia. Dis Aquat Organs. 2016;122:163–170.
  • Reid TM. Emergence of group B streptococci in obstetric and perinatal infections. Br Med J. 1975;2:533–535.
  • Madrid L, Seale AC, Kohli-Lynch M, et al. Infant group B Streptococcal disease incidence and serotypes worldwide: systematic review and meta-analyses. Clin Infect Dis. 2017;65:S160–S172.
  • Shabayek S, Spellerberg B. Group B streptococcal colonization, molecular characteristics, and epidemiology. Front Microbiol. 2018;9:1–14.
  • Skov Sørensen UB, Poulsen K, Ghezzo C, et al. Emergence and global dissemination of host-specific Streptococcus agalactiae clones. MBio. 2010;1:1–9.
  • Romain A-S, Cohen R, Plainvert C, et al. Clinical and laboratory features of group B Streptococcus meningitis in infants and newborns: study of 848 cases in France, 2001–2014. Clin Infect Dis. 2018;66:857–864.
  • No GG. Prevention of early-onset neonatal group B Streptococcal disease: green-top guideline no. 36. BJOG An Int J Obstet Gynaecol. 2017;124:e280–e305.
  • Phares CR, Lynfield R, Farley MM, et al. Epidemiology of invasive Group B streptococcal disease in the United States, 1999–2005. JAMA. 2008;299:2056–2065.
  • Chaiwarith R, Jullaket W, Bunchoo M, et al. Streptococcus agalactiae in adults at Chiang Mai University Hospital: a retrospective study. BMC Infect Dis. 2011;11:149.
  • Lambertsen L, Ekelund K, Skovsted IC, et al. Characterisation of invasive Group B streptococci from adults in Denmark 1999 to 2004. Eur J Clin Microbiol Infect Dis. 2010;29:1071–1077.
  • Kalimuddin S, Chen SL, Lim CT, et al. 2015 epidemic of severe Streptococcus agalactiae sequence type 283 infections in Singapore associated with the consumption of raw freshwater fish: a detailed analysis of clinical, epidemiological, and bacterial sequencing data. Clin Infect Dis. 2017;64:S145–S152.
  • Chau ML, Chen SL, Yap M, et al. Group B Streptococcus infections caused by improper sourcing and handling of fish for raw consumption, Singapore, 2015–2016. Emerg Infect Dis. 2017;23:2002.
  • Bisharat N, Crook DW, Leigh J, et al. Hyperinvasive neonatal group B Streptococcus has arisen from a bovine ancestor. J Clin Microbiol. 2004;42:2161–2167.
  • Delannoy CM, Crumlish M, Fontaine MC, et al. Human Streptococcus agalactiae strains in aquatic mammals and fish. BMC Microbiol. 2013;13:41.
  • Morach M, Stephan R, Schmitt S, et al. Population structure and virulence gene profiles of Streptococcus agalactiae collected from different hosts worldwide. Eur J Clin Microbiol Infect Dis. 2018;37:527–536.
  • Lyhs U, Kulkas L, Katholm J, et al. Streptococcus agalactiae Serotype IV in humans and cattle, Northern Europe1. Emerg Infect Dis. 2016;22:2097–2103.
  • Huang J, Li S, Li L, et al. Alarming regional differences in prevalence and antimicrobial susceptibility of Group B streptococci in pregnant women: a systematic review and meta-analysis. J Glob Antimicrob Resist. 2016;7:169–177.
  • Betriu C, Gomez M, Sanchez A, et al. Antibiotic resistance and penicillin tolerance in clinical isolates of group B streptococci. Antimicrob Agents Chemother. 2012;38:2183–2186.
  • Beall BW, Hensler ME, Van Sorge NM, et al. Point mutation in the group B Streptococcal pbp2x gene conferring decreased susceptibility to -lactam antibiotics. Antimicrob Agents Chemother. 2008;52:2915–2918.
  • Kimura K, Suzuki S, Wachino J-I, et al. First molecular characterization of group B streptococci with reduced penicillin susceptibility. Antimicrob Agents Chemother. 2008;52:2890–2897.
  • Hu Y, Kan Y, Zhang Z, et al. New mutations of penicillin-binding proteins in Streptococcus agalactiae isolates from cattle with decreased susceptibility to penicillin. Microb Drug Resist. 2018;24:1236–1241.
  • Barros RR, de Souza AF, Luiz FBO. Polyclonal spread of Streptococcus agalactiae resistant to clindamycin among pregnant women in Brazil. J Antimicrob Chemother. 2016;71:2054–2056.
  • Dogan B, Schukken YH, Santisteban C, et al. Distribution of serotypes and antimicrobial resistance genes among Streptococcus agalactiae isolates from bovine and human hosts. J Clin Microbiol. 2005;43:5899–5906.
  • Lopes E, Fernandes T,Machado MP, et al. Increasing macrolide resistance among Streptococcus agalactiae causing invasive disease in non-pregnant adults was driven by a single capsular-transformed lineage, Portugal, 2009 to 2015. Eurosurveillance. 2018;23:pii=1700473.
  • Guo Y, Deng X, Liang Y, et al. The draft genomes and investigation of serotype distribution, antimicrobial resistance of Group B Streptococcus strains isolated from urine in Suzhou, China. Ann Clin Microbiol Antimicrob. 2018;17:1–7.
  • Jensen N. Experimental bovine group B streptococcal mastitis induced by strains of human and bovine origin. Nord Vet Med. 1982;34:441–450.
  • Dzanibe S, Madhi SA. Systematic review of the clinical development of group B Streptococcus serotype-specific capsular polysaccharide-based vaccines. Expert Rev Vaccines. 2018;17:635–651.
  • Liu G, Yin J, Barkema HW, et al. Development of a single-dose recombinant CAMP factor entrapping poly(lactide-co-glycolide) microspheres-based vaccine against Streptococcus agalactiae. Vaccine. 2017;35:1246–1253.
  • Dzanibe S, Madhi SA. Systematic review of the clinical development of group B streptococcus serotype-specific capsular polysaccharide-based vaccines. Expert Rev Vaccines. 2018;1–17. DOI:10.1080/14760584.2018.1496021
  • Kim BJ, Hancock BM, Del Cid N, et al. Streptococcus agalactiae infection in zebrafish larvae. Microb Pathog. 2015;79:57–60.
  • Tazi A, Disson O, Bellais S, et al. The surface protein HvgA mediates group B Streptococcus hypervirulence and meningeal tropism in neonates. J Exp Med. 2010;207:2313–2322.
  • Noel GJ, Santos JI, Vitale JJ. Newborn sepsis following antepartum group B streptococcal maternal infection in rats. Pediatr Res. 1985;19:297–299.
  • Delannoy CMJ, Zadoks RN, Crumlish M, et al. Genomic comparison of virulent and non-virulent Streptococcus agalactiae in fish. J Fish Dis. 2016;39:13–29.
  • Jander G, Rahme LG, Ausubel FM. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol. 2000;182:3843–3845.
  • Fedhila S, Daou N, Lereclus D, et al. Identification of Bacillus cereus internalin and other candidate virulence genes specifically induced during oral infection in insects. Mol Microbiol. 2006;62:339–355.
  • Joyce SA, Gahan CGM. Molecular pathogenesis of Listeria monocytogenes in the alternative model host Galleria mellonella. Microbiology. 2010;156:3456–3468.
  • Mukherjee K, Altincicek B, Hain T, et al. Galleria mellonella as a model system for studyingListeria pathogenesis. Appl Environ Microbiol. 2010;76:310–317.
  • McMillan S, Verner-Jeffreys D, Weeks J, et al. Larva of the greater wax moth, Galleria mellonella, is a suitable alternative host for studying virulence of fish pathogenic Vibrio anguillarum. BMC Microbiol. 2015;15:127.
  • Nale JY, Chutia M, Carr P, et al. ‘Get in Early’; Biofilm and Wax Moth (Galleria mellonella) models reveal new insights into the therapeutic potential of Clostridium difficile bacteriophages. Front Microbiol. 2016;7.
  • Loh JMS, Adenwalla N, Wiles S, et al. Galleria mellonella larvae as an infection model for group A Streptococcus. Virulence. 2013;4:419–428.
  • Olsen RJ, Watkins ME, Cantu CC, et al. Virulence of serotype M3 Group A Streptococcus strains in wax worms (Galleria mellonella larvae). Virulence. 2011;2:111–119.
  • Evans BA, Rozen DE. A Streptococcus pneumoniae infection model in larvae of the wax moth Galleria mellonella. Eur J Clin Microbiol Infect Dis. 2012;31:2653–2660.
  • Velikova N, Kavanagh K, Wells JM. Evaluation of Galleria mellonella larvae for studying the virulence of Streptococcus suis. BMC Microbiol. 2016;16:291.
  • Tsai CJ-Y, Loh JMS, Proft T. Galleria mellonella infection models for the study of bacterial diseases and for antimicrobial drug testing. Virulence. 2016;7:214–229.
  • Desbois AP, Coote PJ. Utility of greater wax moth larva (Galleria mellonella) for evaluating the toxicity and efficacy of new antimicrobial agents. Adv Appl Microbiol. 2012;78:25–53.
  • Lange A, Beier S, Huson DH, et al. Genome Sequence of Galleria mellonella (Greater Wax Moth). Genome Announc. 2018;6:1–2.
  • Vogel H, Altincicek B, Glöckner G, et al. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics. 2011;12:308.
  • Mukherjee K, Vilcinskas A. Development and immunity-related microRNAs of the lepidopteran model host Galleria mellonella. BMC Genomics. 2014;15:1–12.
  • Browne N, Heelan M, Kavanagh K. An analysis of the structural and functional similarities of insect hemocytes and mammalian phagocytes. Virulence. 2013;4:597–603.
  • Renwick J, Reeves EP, Wientjes FB, et al. Translocation of proteins homologous to human neutrophil p47phox and p67phox to the cell membrane in activated hemocytes of Galleria mellonella. Dev Comp Immunol. 2007;31:347–359.
  • Bergin D, Reeves EP, Renwick J, et al. Superoxide production in Galleria mellonella hemocytes: identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun. 2005;73:4161–4170.
  • Tojo S, Naganuma F, Arakawa K, et al. Involvement of both granular cells and plasmatocytes in phagocytic reactions in the greater wax moth, Galleria mellonella. J Insect Physiol. 2000;46:1129–1135.
  • Desalermos A, Fuchs BB, Mylonakis E. Selecting an invertebrate model host for the study of fungal pathogenesis. PLoS Pathog. 2012;8:e1002451.
  • Pereira UP, Mian GF, Oliveira ICM, et al. Genotyping of Streptococcus agalactiae strains isolated from fish, human and cattle and their virulence potential in Nile tilapia. Vet Microbiol. 2009;140:186–192.
  • Richards VP, Lang P, Bitard PD, et al. Comparative genomics and the role of lateral gene transfer in the evolution of bovine adapted Streptococcus agalactiae. Infect. Genet. Evol. 2011;2011:1263–1275.
  • Richards VP, Choi SC, Bitar PDP, et al. Transcriptomic and genomic evidence for Streptococcus agalactiae adaptation to the bovine environment. BMC Genomics. 2013;14:1–15.
  • Yang Y, Luo M, Zhou H, et al. Role of two-component system response regulator bceR in the antimicrobial resistance, virulence, biofilm formation, and stress response of group B Streptococcus. Front Microbiol. 2019;10:1–15.
  • Luther MK, Arvanitis M, Mylonakis E, et al. Activity of daptomycin or linezolid in combination with rifampin or gentamicin against biofilm-forming Enterococcus faecalis or E. faecium in an in vitro pharmacodynamic model using simulated endocardial vegetations and an in vivo survival A. Antimicrob Agents Chemother. 2014;58:4612–4620.
  • Krezdorn J, Adams S, Coote PJ. A Galleria mellonella infection model reveals double and triple antibiotic combination therapies with enhanced efficacy versus a multidrug-resistant strain of Pseudomonas aeruginosa. J Med Microbiol. 2014;63:945–955.