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A molecular trigger for intercontinental epidemics of group A Streptococcus

Luchang Zhu, … , Frank R. DeLeo, James M. Musser

Luchang Zhu, … , Frank R. DeLeo, James M. Musser

Published August 10, 2015
Citation Information: J Clin Invest. 2015;125(9):3545-3559. https://doi.org/10.1172/JCI82478.

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Research Article Infectious disease

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Citations to this article (91)

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Epidemiology of Streptococcus pyogenes upper respiratory tract infections in Poland (2003-2017). Sitkiewicz I, Borek A, Gryko M, Karpińska A, Kozińska A, Obszańska K, Wilemska-Dziaduszycka J, Walory J, Bańska A, Belkiewicz K, Foryś M, Gołębiewska A, Hryniewicz W, Kadłubowski M, Kiedrowska M, Klarowicz A, Matynia B, Ronkiewicz P, Szczypa K, Waśko I, Wawszczak M, Wróbel-Pawelczyk I, Zieniuk B	Journal of Applied Genetics	2024
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A genome-scale metabolic model of a globally disseminated hyperinvasive M1 strain of Streptococcus pyogenes. Hirose Y, Zielinski DC, Poudel S, Rychel K, Baker JL, Toya Y, Yamaguchi M, Heinken A, Thiele I, Kawabata S, Palsson BO, Nizet V	mSystems	2024
Integrative genomic, virulence, and transcriptomic analysis of emergent Streptococcus dysgalactiae subspecies equisimilis (SDSE) emm type stG62647 isolates causing human infections. Eraso JM, Olsen RJ, Long SW, Gadd R, Boukthir S, Faili A, Kayal S, Musser JM	mBio	2024
Structural basis underlying the synergism of NADase and SLO during group A Streptococcus infection Tsai WJ, Lai YH, Shi YA, Hammel M, Duff AP, Whitten AE, Wilde KL, Wu CM, Knott R, Jeng US, Kang CY, Hsu CY, Wu JL, Tsai PJ, Chiang-Ni C, Wu JJ, Lin YS, Liu CC, Senda T, Wang S	Communications biology	2023
Pathogenesis, epidemiology and control of Group A Streptococcus infection Brouwer S, Rivera-Hernandez T, Curren BF, Harbison-Price N, De Oliveira DM, Jespersen MG, Davies MR, Walker MJ	Nature reviews. Microbiology	2023
Analysis of the Genomics and Mouse Virulence of an Emergent Clone of Streptococcus dysgalactiae Subspecies equisimilis. Beres SB, Olsen RJ, Long SW, Eraso JM, Boukthir S, Faili A, Kayal S, Musser JM	Microbiology spectrum	2023
Elucidation of independently modulated genes in Streptococcus pyogenes reveals carbon sources that control its expression of hemolytic toxins Hirose Y, Poudel S, Sastry AV, Rychel K, Lamoureux CR, Szubin R, Zielinski DC, Lim HG, Menon ND, Bergsten H, Uchiyama S, Hanada T, Kawabata S, Palsson BO, Nizet V	mSystems	2023
Interplay between human STING genotype and bacterial NADase activity regulates inter-individual disease variability. Movert E, Bolarin JS, Valfridsson C, Velarde J, Skrede S, Nekludov M, Hyldegaard O, Arnell P, Svensson M, Norrby-Teglund A, Cho KH, Elhaik E, Wessels MR, Råberg L, Carlsson F	Nature Communications	2023
Genomic epidemiology of Streptococcus dysgalactiae subsp. equisimilis strains causing invasive disease in Norway during 2018. Kaci A, Jonassen CM, Skrede S, Sivertsen A, Steinbakk M, Oppegaard O	Frontiers in microbiology	2023
Epidemiology and emm types among group A streptococcal pharyngitis in Finland: a prospective laboratory-based study. Virolainen M, Gröndahl-Yli-Hannuksela K, Rantakokko-Jalava K, Seiskari T, Lönnqvist E, Kolari T, Rissanen T, Hyyryläinen HL, Vuopio J	European journal of clinical microbiology & infectious diseases : official publication of the European Society of Clinical Microbiology	2023
Structure of the Streptococcus pyogenes NAD + Glycohydrolase Translocation Domain and Its Essential Role in Toxin Binding to Oropharyngeal Keratinocytes J Velarde, A Piai, I Lichtenstein, N Lynskey, J Chou, M Wessels, M Federle	Journal of bacteriology	2022
CovS inactivation reduces CovR promoter binding at diverse virulence factor encoding genes in group A Streptococcus N Horstmann, K Myers, C Tran, A Flores, S Shelburne, C Orihuela	PLoS pathogens	2022
An M protein coiled coil unfurls and exposes its hydrophobic core to capture LL-37 Kolesinski P, Wang KC, Hirose Y, Nizet V, Ghosh P	eLife	2022
Annotated Whole-Genome Multilocus Sequence Typing Schema for Scalable High-Resolution Typing of Streptococcus pyogenes Friães A, Mamede R, Ferreira M, Melo-Cristino J, Ramirez M	Journal of clinical microbiology	2022
Streptococcus pyogenes can support or inhibit growth of Haemophilus influenzae by supplying or restricting extracellular NAD+ Lee H, Edgar RJ, Lichtenstein IJ, Velarde JJ, Korotkova N, Wessels MR	PloS one	2022
Genome-Wide Transposon Mutagenesis Screens Identify Group A Streptococcus Genes Affecting Susceptibility to β-Lactam Antibiotics Zhu L, Eraso JM, Mangham RE, Ojeda Saavedra M, Olsen RJ, Beres SB, Musser JM	Journal of bacteriology	2022
Functional Insights into the High-Molecular-Mass Penicillin-Binding Proteins of Streptococcus agalactiae Revealed by Gene Deletion and Transposon Mutagenesis Analysis L Zhu, P Yerramilli, L Pruitt, A Mishra, RJ Olsen, SB Beres, AS Waller, JM Musser, MJ Federle	Journal of bacteriology	2021
Streptolysin O concentration and activity is central to in vivo phenotype and disease outcome in Group A Streptococcus infection J Clarke, M Baltazar, M Alsahag, S Panagiotou, M Pouget, WA Paxton, G Pollakis, D Everett, N French, A Kadioglu	Scientific Reports	2021
Population Genomics of emm4 Group A Streptococcus Reveals Progressive Replacement with a Hypervirulent Clone in North America S DebRoy, M Sanson, B Shah, S Regmi, LA Vega, C Odo, P Sahasrabhojane, A McGeer, GJ Tyrrell, N Fittipaldi, SA Shelburne, AR Flores, S Bordenstein	mSystems	2021
Streptococcus pyogenes TrxSR Two-Component System Regulates Biofilm Production in Acidic Environments M Isaka, A Okamoto, Y Miura, I Tatsuno, J Maeyama, T Hasegawa, NE Freitag	Infection and immunity	2021
Intracellular Group A Streptococcus Induces Golgi Fragmentation To Impair Host Defenses through Streptolysin O and NAD-Glycohydrolase T Nozawa, J Iibushi, H Toh, A Minowa-Nozawa, K Murase, C Aikawa, I Nakagawa, YF Chang	mBio	2021
Characterization of the Type I Restriction Modification System Broadly Conserved among Group A Streptococci S DebRoy, WC Shropshire, CN Tran, H Hao, M Gohel, J Galloway-Peña, B Hanson, AR Flores, SA Shelburne, PD Fey	mSphere	2021
Streptococcus pyogenes upregulates arginine catabolism to exert its pathogenesis on the skin surface Hirose Y, Yamaguchi M, Sumitomo T, Nakata M, Hanada T, Okuzaki D, Motooka D, Mori Y, Kawasaki H, Coady A, Uchiyama S, Hiraoka M, Zurich RH, Amagai M, Nizet V, Kawabata S	Cell Reports	2021
Streptococcus pyogenes Genes That Promote Pharyngitis in Primates Luchang Zhu, Randall Olsen, Stephen Beres, Matthew Ojeda Saavedra, Samantha L. Kubiak, Concepcion Cantu, Leslie A. Jenkins, Andrew S. Waller, Zhizeng Sun, Timothy Palzkill, Adeline Porter, Frank R. DeLeo, James Mallory Musser	JCI Insight	2020
Genome-Wide Screens Identify Group A Streptococcus Surface Proteins Promoting Female Genital Tract Colonization and Virulence L Zhu, RJ Olsen, SB Beres, MO Saavedra, SL Kubiak, CC Cantu, L Jenkins, P Yerramilli, L Pruitt, AR Charbonneau, AS Waller, JM Musser	The American Journal of Pathology	2020
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Genome-Wide Assessment of Streptococcus agalactiae Genes Required for Survival in Human Whole Blood and Plasma L Zhu, P Yerramilli, L Pruitt, MO Saavedra, CC Cantu, RJ Olsen, SB Beres, AS Waller, JM Musser, NE Freitag	Infection and immunity	2020
Genetic Basis Underlying the Hyperhemolytic Phenotype of Streptococcus agalactiae Strain CNCTC10/84 L Zhu, SB Beres, P Yerramilli, L Pruitt, CC Cantu, RJ Olsen, JM Musser, MJ Federle	Journal of bacteriology	2020
A Single Amino Acid Replacement in Penicillin Binding Protein 2X in Streptococcus pyogenes Significantly Increases Fitness upon Subtherapeutic Benzylpenicillin Treatment in a Mouse Model of Necrotizing Myositis RJ Olsen, L Zhu, JM Musser	The American Journal of Pathology	2020
Strain-Dependent Effect of Capsule on Transmission and Persistence in an Infant Mouse Model of Group A Streptococcus Infection LA Vega, MA Sanson, BJ Shah, AR Flores, NE Freitag	Infection and immunity	2020
Pathogenicity Characterization of Prevalent-Type Streptococcus dysgalactiae subsp. equisimilis Strains M Matsue, K Ogura, H Sugiyama, T Miyoshi-Akiyama, Y Takemori-Sakai, Y Iwata, T Wada, S Okamoto	Frontiers in microbiology	2020
Single Amino Acid Replacements in RocA Disrupt Protein-Protein Interactions To Alter the Molecular Pathogenesis of Group A Streptococcus PE Bernard, A Duarte, M Bogdanov, JM Musser, RJ Olsen, NE Freitag	Infection and immunity	2020
Nicotinamide Increases Intracellular NAD+ Content to Enhance Autophagy-Mediated Group A Streptococcal Clearance in Endothelial Cells CL Hsieh, SY Hsieh, HM Huang, SL Lu, H Omori, PX Zheng, YN Ho, YL Cheng, YS Lin, C Chiang-Ni, PJ Tsai, SY Wang, CC Liu, T Noda, JJ Wu	Frontiers in microbiology	2020
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Gene fitness landscape of group A streptococcus during necrotizing myositis Luchang Zhu, Randall Olsen, Stephen Beres, Jesus M Eraso, Matthew Ojeda Saavedra, Samantha Kubiak, Concepcion Cantu, Leslie Jenkins, Amelia RL Charbonneau, Andrew S Waller, James Mallory Musser	Journal of Clinical Investigation	2019
Integrated analysis of population genomics, transcriptomics and virulence provides novel insights into Streptococcus pyogenes pathogenesis P Kachroo, JM Eraso, SB Beres, RJ Olsen, L Zhu, W Nasser, PE Bernard, CC Cantu, MO Saavedra, MJ Arredondo, B Strope, H Do, M Kumaraswami, J Vuopio, K Gröndahl-Yli-Hannuksela, KG Kristinsson, M Gottfredsson, M Pesonen, J Pensar, ER Davenport, AG Clark, J Corander, DA Caugant, S Gaini, MD Magnussen, SL Kubiak, HA Nguyen, SW Long, AR Porter, FR DeLeo, JM Musser	Nature Genetics	2019
Conserved and specific features of Streptococcus pyogenes and Streptococcus agalactiae transcriptional landscapes I Rosinski-Chupin, E Sauvage, A Fouet, C Poyart, P Glaser	BMC Genomics	2019
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The Secreted Virulence Factor NADase of Group A Streptococcus Inhibits P2X7 Receptor-Mediated Release of IL-1β E Westerlund, C Valfridsson, DX Yi, JJ Persson	Frontiers in immunology	2019
Emergence of dominant toxigenic M1T1 Streptococcus pyogenes clone during increased scarlet fever activity in England: a population-based molecular epidemiological study NN Lynskey, E Jauneikaite, HK Li, X Zhi, CE Turner, M Mosavie, M Pearson, M Asai, L Lobkowicz, JY Chow, J Parkhill, T Lamagni, VJ Chalker, S Sriskandan	The Lancet Infectious Diseases	2019
Polymorphisms in Regulator of Cov Contribute to the Molecular Pathogenesis of Serotype M28 Group A Streptococcus PE Bernard, P Kachroo, JM Eraso, L Zhu, JE Madry, SE Linson, MO Saavedra, C Cantu, JM Musser, RJ Olsen	The American Journal of Pathology	2019
Changes in emm types and superantigen gene content of Streptococcus pyogenes causing invasive infections in Portugal A Friães, J Melo-Cristino, M Ramirez	Scientific Reports	2019
The Emergence of Successful Streptococcus pyogenes Lineages through Convergent Pathways of Capsule Loss and Recombination Directing High Toxin Expression CE Turner, MT Holden, B Blane, C Horner, SJ Peacock, S Sriskandan, P Keim	mBio	2019
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Canada-Wide Epidemic of emm74 Group A Streptococcus Invasive Disease S Teatero, A McGeer, GJ Tyrrell, L Hoang, H Smadi, MC Domingo, PN Levett, M Finkelstein, K Dewar, A Plevneshi, TB Athey, JB Gubbay, MR Mulvey, I Martin, W Demczuk, N Fittipaldi	Open Forum Infectious Diseases	2018
RocA has serotype-specific gene regulatory and pathogenesis activity in serotype M28 group A streptococcus PE Bernard, P Kachroo, L Zhu, SB Beres, JM Eraso, Z Kajani, SW Long, JM Musser, RJ Olsen	Infection and immunity	2018
In silico characterisation of the two-component system regulators of Streptococcus pyogenes SJ Buckley, P Timms, MR Davies, DJ McMillan, B Lei	PloS one	2018
Endopeptidase PepO Regulates the SpeB Cysteine Protease and Is Essential for the Virulence of Invasive M1T1 Streptococcus pyogenes S Brouwer, AJ Cork, CL Ong, TC Barnett, NP West, KS McIver, MJ Walker, O Schneewind	Journal of bacteriology	2018
NAD-Glycohydrolase Depletes Intracellular NAD+ and Inhibits Acidification of Autophagosomes to Enhance Multiplication of Group A Streptococcus in Endothelial Cells CL Hsieh, HM Huang, SY Hsieh, PX Zheng, YS Lin, C Chiang-Ni, PJ Tsai, SY Wang, CC Liu, JJ Wu	Frontiers in microbiology	2018
Variation, Indispensability, and Masking in the M protein P Ghosh	Trends in Microbiology	2018
Group A Streptococcus encounters with host macrophages JA Valderrama, V Nizet	Future Microbiology	2018
Using Machine Learning To Predict Antimicrobial MICs and Associated Genomic Features for Nontyphoidal Salmonella M Nguyen, SW Long, PF McDermott, RJ Olsen, R Olson, RL Stevens, GH Tyson, S Zhao, JJ Davis, DJ Diekema	Journal of clinical microbiology	2018
Molecular Epidemiology, Ecology, and Evolution of Group A Streptococci DE Bessen, PR Smeesters, BW Beall, VA Fischetti, RP Novick, JJ Ferretti, DA Portnoy, JI Rood	Microbiology spectrum	2018
Community outbreaks of group A Streptococcus revealed by genome sequencing CE Turner, L Bedford, NM Brown, K Judge, ME Török, J Parkhill, SJ Peacock	Scientific Reports	2017
Group A streptococcal M protein activates the NLRP3 inflammasome JA Valderrama, AM Riestra, NJ Gao, CN LaRock, N Gupta, SR Ali, HM Hoffman, P Ghosh, V Nizet	Nature Microbiology	2017
Rapid Emergence of a New Clone Impacts the Population at Risk and Increases the Incidence of Type emm89 Group A Streptococcus Invasive Disease S Teatero, BL Coleman, SB Beres, RJ Olsen, C Kandel, O Reynolds, TB Athey, JM Musser, A McGeer, N Fittipaldi	Open Forum Infectious Diseases	2017
Evolutionary Constraints Shaping Streptococcus pyogenes–Host Interactions RV Wilkening, MJ Federle	Trends in Microbiology	2017
Contribution of Secreted NADase and Streptolysin O to the Pathogenesis of Epidemic Serotype M1 Streptococcus pyogenes Infections L Zhu, RJ Olsen, JD Lee, AR Porter, FR DeLeo, JM Musser	The American Journal of Pathology	2017
Sequence analysis of pooled bacterial samples enables identification of strain variation in group A streptococcus RG Weldatsadik, J Wang, K Puhakainen, H Jiao, J Jalava, K Räisänen, N Datta, T Skoog, J Vuopio, TS Jokiranta, J Kere	Scientific Reports	2017
Necrotizing fasciitis: treatment concepts and clinical results M Leiblein, I Marzi, AL Sander, JH Barker, F Ebert, J Frank	European Journal of Trauma and Emergency Surgery	2017
Unravelling pathogenetic mechanisms of epidemic lineages O Oppegaard	Virulence	2017
A Red Blood Cell Membrane-Camouflaged Nanoparticle Counteracts Streptolysin O-Mediated Virulence Phenotypes of Invasive Group A Streptococcus T Escajadillo, J Olson, BT Luk, L Zhang, V Nizet	Frontiers in pharmacology	2017
Binding of NAD + -Glycohydrolase to Streptolysin O Stabilizes Both Toxins and Promotes Virulence of Group A Streptococcus JJ Velarde, M OSeaghdha, B Baddal, B Bastiat-Sempe, MR Wessels, GM Dunny	mBio	2017
Inhibition of Inflammasome-Dependent Interleukin 1β Production by Streptococcal NAD + -Glycohydrolase: Evidence for Extracellular Activity D Hancz, E Westerlund, B Bastiat-Sempe, O Sharma, C Valfridsson, L Meyer, JF Love, M OSeaghdha, MR Wessels, JJ Persson, VJ Torres	mBio	2017
Opacification Domain of Serum Opacity Factor Inhibits Beta-Hemolysis and Contributes to Virulence of Streptococcus pyogenes L Zhu, RJ Olsen, JM Musser, SE D'Orazio	mSphere	2017
Population and Whole Genome Sequence Based Characterization of Invasive Group A Streptococci Recovered in the United States during 2015 S Chochua, BJ Metcalf, Z Li, J Rivers, S Mathis, D Jackson, RE Gertz, V Srinivasan, R Lynfield, CV Beneden, L McGee, B Beall, JM Hughes	mBio	2017
Novel Genes Required for the Fitness of Streptococcus pyogenes in Human Saliva L Zhu, AR Charbonneau, AS Waller, RJ Olsen, SB Beres, JM Musser, SE D'Orazio	mSphere	2017
Genome sequence analysis of emm89 Streptococcus pyogenes strains causing infections in Scotland, 2010–2016 SB Beres, RJ Olsen, MO Saavedra, R Ure, A Reynolds, DS Lindsay, AJ Smith, JM Musser	Journal of Medical Microbiology	2017
Tissue tropisms in group A Streptococcus: what virulence factors distinguish pharyngitis from impetigo strains? DE Bessen	Current Opinion in Infectious Diseases	2016
Genomic Landscape of Intrahost Variation in Group A Streptococcus: Repeated and Abundant Mutational Inactivation of the fabT Gene Encoding a Regulator of Fatty Acid Synthesis JM Eraso, RJ Olsen, SB Beres, P Kachroo, AR Porter, W Nasser, PE Bernard, FR DeLeo, JM Musser, VB Young	Infection and immunity	2016
Transcriptome Remodeling Contributes to Epidemic Disease Caused by the Human Pathogen Streptococcus pyogenes SB Beres, P Kachroo, W Nasser, RJ Olsen, L Zhu, AR Flores, I la Riva, J Paez-Mayorga, FE Jimenez, C Cantu, J Vuopio, J Jalava, KG Kristinsson, M Gottfredsson, J Corander, N Fittipaldi, MC di Luca, D Petrelli, LA Vitali, A Raiford, L Jenkins, JM Musser	mBio	2016
Intergenic Variable-Number Tandem-Repeat Polymorphism Upstream of rocA Alters Toxin Production and Enhances Virulence in Streptococcus pyogenes L Zhu, RJ Olsen, N Horstmann, SA Shelburne, J Fan, Y Hu, JM Musser, A Camilli	Infection and immunity	2016
Regulatory gene mutation: a driving force behind group a Streptococcus strain- and serotype-specific variation: Regulator variation in GAS P Sarkar, P Sumby	Molecular Microbiology	2016
Genomic Characteristics Behind the Spread of Bacteremic Group A Streptococcus Type emm 89 in Finland, 2004–2014 F Latronico, W Nasser, K Puhakainen, J Ollgren, HL Hyyryläinen, SB Beres, O Lyytikäinen, J Jalava, JM Musser, J Vuopio	The Journal of Infectious Diseases	2016
The Majority of 9,729 Group A Streptococcus Strains Causing Disease Secrete SpeB Cysteine Protease: Pathogenesis Implications RJ Olsen, A Raghuram, C Cantu, M Harrell-Hartman, F Jimenez, S Lee, A Ngo, KA Rice, D Saddington, H Spillman, C Valson, AR Flores, SB Beres, SW Long, W Nasser, JM Musser	Infection and immunity	2015
Trading Capsule for Increased Cytotoxin Production: Contribution to Virulence of a Newly Emerged Clade of emm89 Streptococcus pyogenes L Zhu, RJ Olsen, W Nasser, IR la Morales, JM Musser	mBio	2015
Streptolysin O Rapidly Impairs Neutrophil Oxidative Burst and Antibacterial Responses to Group A Streptococcus S Uchiyama, S Döhrmann, AM Timmer, N Dixit, M Ghochani, T Bhandari, JC Timmer, K Sprague, J Bubeck-Wardenburg, SI Simon, V Nizet	Frontiers in immunology	2015
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Emergence of the Same Successful Clade among Distinct Populations of emm 89 Streptococcus pyogenes in Multiple Geographic Regions A Friães, MP Machado, C Pato, J Carriço, J Melo-Cristino, M Ramirez	mBio	2015
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