Estimating the Fitness Advantage Conferred by Permissive Neuraminidase Mutations in Recent Oseltamivir-Resistant A(H1N1)pdm09 Influenza Viruses
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{"title"=>"Estimating the Fitness Advantage Conferred by Permissive Neuraminidase Mutations in Recent Oseltamivir-Resistant A(H1N1)pdm09 Influenza Viruses", "type"=>"journal", "authors"=>[{"first_name"=>"Jeff", "last_name"=>"Butler", "scopus_author_id"=>"55633548700"}, {"first_name"=>"Kathryn A.", "last_name"=>"Hooper", "scopus_author_id"=>"55918548800"}, {"first_name"=>"Stephen", "last_name"=>"Petrie", "scopus_author_id"=>"55700278100"}, {"first_name"=>"Raphael", "last_name"=>"Lee", "scopus_author_id"=>"29067840500"}, {"first_name"=>"Sebastian", "last_name"=>"Maurer-Stroh", "scopus_author_id"=>"6602459149"}, {"first_name"=>"Lucia", "last_name"=>"Reh", "scopus_author_id"=>"55797830500"}, {"first_name"=>"Teagan", "last_name"=>"Guarnaccia", "scopus_author_id"=>"55698278800"}, {"first_name"=>"Chantal", "last_name"=>"Baas", "scopus_author_id"=>"8943994100"}, {"first_name"=>"Lumin", "last_name"=>"Xue", "scopus_author_id"=>"55262943600"}, {"first_name"=>"Sophie", "last_name"=>"Vitesnik", "scopus_author_id"=>"55586543400"}, {"first_name"=>"Sook Kwan", "last_name"=>"Leang", "scopus_author_id"=>"54949676400"}, {"first_name"=>"Jodie", "last_name"=>"McVernon", "scopus_author_id"=>"6701712603"}, {"first_name"=>"Anne", "last_name"=>"Kelso", "scopus_author_id"=>"24379314000"}, {"first_name"=>"Ian G.", "last_name"=>"Barr", "scopus_author_id"=>"7004651416"}, {"first_name"=>"James M.", "last_name"=>"McCaw", "scopus_author_id"=>"21735020500"}, {"first_name"=>"Jesse D.", "last_name"=>"Bloom", "scopus_author_id"=>"7201379306"}, {"first_name"=>"Aeron C.", "last_name"=>"Hurt", "scopus_author_id"=>"6603378203"}], "year"=>2014, "source"=>"PLoS Pathogens", "identifiers"=>{"pmid"=>"24699865", "sgr"=>"84901307271", "doi"=>"10.1371/journal.ppat.1004065", "scopus"=>"2-s2.0-84901307271", "pui"=>"373162956", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "issn"=>"15537374"}, "id"=>"f9fb33e6-fe06-3c7b-be8e-642d0226a822", "abstract"=>"Oseltamivir is relied upon worldwide as the drug of choice for the treatment of human influenza infection. Surveillance for oseltamivir resistance is routinely performed to ensure the ongoing efficacy of oseltamivir against circulating viruses. Since the emergence of the pandemic 2009 A(H1N1) influenza virus (A(H1N1)pdm09), the proportion of A(H1N1)pdm09 viruses that are oseltamivir resistant (OR) has generally been low. However, a cluster of OR A(H1N1)pdm09 viruses, encoding the neuraminidase (NA) H275Y oseltamivir resistance mutation, was detected in Australia in 2011 amongst community patients that had not been treated with oseltamivir. Here we combine a competitive mixtures ferret model of influenza infection with a mathematical model to assess the fitness, both within and between hosts, of recent OR A(H1N1)pdm09 viruses. In conjunction with data from in vitro analyses of NA expression and activity we demonstrate that contemporary A(H1N1)pdm09 viruses are now more capable of acquiring H275Y without compromising their fitness, than earlier A(H1N1)pdm09 viruses circulating in 2009. Furthermore, using reverse engineered viruses we demonstrate that a pair of permissive secondary NA mutations, V241I and N369K, confers robust fitness on recent H275Y A(H1N1)pdm09 viruses, which correlated with enhanced surface expression and enzymatic activity of the A(H1N1)pdm09 NA protein. These permissive mutations first emerged in 2010 and are now present in almost all circulating A(H1N1)pdm09 viruses. Our findings suggest that recent A(H1N1)pdm09 viruses are now more permissive to the acquisition of H275Y than earlier A(H1N1)pdm09 viruses, increasing the risk that OR A(H1N1)pdm09 will emerge and spread worldwide.", "link"=>"http://www.mendeley.com/research/estimating-fitness-advantage-conferred-permissive-neuraminidase-mutations-recent-oseltamivirresistan", "reader_count"=>58, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>3, "Student > Master"=>8, "Other"=>1, "Student > Bachelor"=>6, "Lecturer"=>2, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>3, "Student > Master"=>8, "Other"=>1, "Student > Bachelor"=>6, "Lecturer"=>2, "Professor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Biochemistry, Genetics and Molecular Biology"=>12, "Mathematics"=>3, "Agricultural and Biological Sciences"=>19, "Medicine and Dentistry"=>10, "Chemistry"=>1, "Social Sciences"=>1, "Computer Science"=>4, "Immunology and Microbiology"=>4}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>10}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>19}, "Computer Science"=>{"Computer Science"=>4}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>12}, "Mathematics"=>{"Mathematics"=>3}, "Unspecified"=>{"Unspecified"=>4}}, "reader_count_by_country"=>{"Japan"=>2, "Finland"=>1, "United Kingdom"=>1, "Australia"=>1}, "group_count"=>4}

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  • {"files"=>["https://ndownloader.figshare.com/files/1448373"], "description"=>"<p>Donor ferrets were infected with pure populations or virus mixtures of reverse genetics derived A/Perth/261/2009 oseltamivir resistant (rgPerth261 OR) and rgPerth261 V241I, N369K OR. Daily nasal washes from donor and 1st and 2nd recipient ferrets were assayed to measure the viral replication and transmission kinetics of each virus mixture/pure population and to assess the relative proportions of each virus within mixtures. (A) The infectious virus titre in each nasal wash was determined by titration on MDCK cells. (B) The relative proportions of virus encoding NA 241I, 369K (black bars) and NA 241V, 369N (white bars) in each nasal wash were determined by pyrosequencing. (A) Virus in donor ferrets (grey), 1st recipients (black lines solid squares), 2nd recipients (black lines, white triangles).</p>", "links"=>[], "tags"=>["Evolutionary biology", "Organismal evolution", "Microbial evolution", "Viral evolution", "microbiology", "Microbial control", "antimicrobials", "antivirals", "Virology", "co-infections", "Emerging viral diseases", "Viral persistence and latency", "Animal models of infection", "Microbial mutation", "Infectious diseases", "Emerging infectious diseases", "na", "v241i", "n369k", "earlier", "h275y"], "article_id"=>985886, "categories"=>["Biological Sciences"], "users"=>["Jeff Butler", "Kathryn A. Hooper", "Stephen Petrie", "Raphael Lee", "Sebastian Maurer-Stroh", "Lucia Reh", "Teagan Guarnaccia", "Chantal Baas", "Lumin Xue", "Sophie Vitesnik", "Sook-Kwan Leang", "Jodie McVernon", "Anne Kelso", "Ian G. Barr", "James M. McCaw", "Jesse D. Bloom", "Aeron C. Hurt"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004065.g004", "stats"=>{"downloads"=>0, "page_views"=>34, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Addition_of_NA_V241I_and_N369K_enhances_the_fitness_of_earlier_H275Y_A_H1N1_pdm09_viruses_/985886", "title"=>"Addition of NA V241I and N369K enhances the fitness of earlier H275Y A(H1N1)pdm09 viruses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-03 03:06:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1448370"], "description"=>"<p>Donor ferrets were infected with pure populations or virus mixtures of A/Newcastle/17/2011 oseltamivir resistant (New17 OR) and A/Newcastle/163/2011 oseltamivir sensitive (New163 OS). Daily nasal washes from donor and 1<sup>st</sup> and 2<sup>nd</sup> recipient ferrets were assayed to measure the viral replication and transmission kinetics of each virus mixture/pure population and to assess the relative proportions of each virus within mixtures. (A) The infectious virus titre in each nasal wash was determined by titration on MDCK cells. (B) The relative proportions of New17 OR virus encoding NA 275Y (black bars) and New163 OS virus encoding NA 275H (white bars) in each nasal wash were determined by pyrosequencing. (A) Virus in donor ferrets (grey), 1st recipient ferrets (black lines solid squares), 2nd recipient ferrets (black lines, white triangles).</p>", "links"=>[], "tags"=>["Evolutionary biology", "Organismal evolution", "Microbial evolution", "Viral evolution", "microbiology", "Microbial control", "antimicrobials", "antivirals", "Virology", "co-infections", "Emerging viral diseases", "Viral persistence and latency", "Animal models of infection", "Microbial mutation", "Infectious diseases", "Emerging infectious diseases", "h275y", "mutation", "hne2011"], "article_id"=>985882, "categories"=>["Biological Sciences"], "users"=>["Jeff Butler", "Kathryn A. Hooper", "Stephen Petrie", "Raphael Lee", "Sebastian Maurer-Stroh", "Lucia Reh", "Teagan Guarnaccia", "Chantal Baas", "Lumin Xue", "Sophie Vitesnik", "Sook-Kwan Leang", "Jodie McVernon", "Anne Kelso", "Ian G. Barr", "James M. McCaw", "Jesse D. Bloom", "Aeron C. Hurt"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004065.g001", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_H275Y_mutation_does_not_compromise_the_fitness_of_HNE2011_A_H1N1_pdm09_viruses_/985882", "title"=>"The H275Y mutation does not compromise the fitness of HNE2011 A(H1N1)pdm09 viruses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-03 03:06:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1448372"], "description"=>"<p>Donor ferrets were infected with pure populations or virus mixtures of reverse genetics derived New17 OR (rgNew17 OR) and rgNew17 I241V, K369N OR. Daily nasal washes from donor, and naive 1st and 2nd recipient ferrets were assayed to measure the viral replication and transmission kinetics of each virus mixture/pure population and to assess the relative proportions of each virus in mixtures. (A) The infectious virus titre in each nasal wash was determined by titration on MDCK cells. (B) The relative proportions of virus encoding NA 241I, 369K (black bars) and NA 241V, 369N (white bars) in each nasal wash were determined by pyrosequencing. (A) Virus in donor ferrets (grey), 1st recipient ferrets (black lines solid squares), 2nd recipient ferrets (black lines, white triangles).</p>", "links"=>[], "tags"=>["Evolutionary biology", "Organismal evolution", "Microbial evolution", "Viral evolution", "microbiology", "Microbial control", "antimicrobials", "antivirals", "Virology", "co-infections", "Emerging viral diseases", "Viral persistence and latency", "Animal models of infection", "Microbial mutation", "Infectious diseases", "Emerging infectious diseases", "na", "v241i", "n369k", "decreases", "h275y"], "article_id"=>985885, "categories"=>["Biological Sciences"], "users"=>["Jeff Butler", "Kathryn A. Hooper", "Stephen Petrie", "Raphael Lee", "Sebastian Maurer-Stroh", "Lucia Reh", "Teagan Guarnaccia", "Chantal Baas", "Lumin Xue", "Sophie Vitesnik", "Sook-Kwan Leang", "Jodie McVernon", "Anne Kelso", "Ian G. Barr", "James M. McCaw", "Jesse D. Bloom", "Aeron C. Hurt"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004065.g003", "stats"=>{"downloads"=>2, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Removal_of_NA_V241I_and_N369K_decreases_the_fitness_of_recent_H275Y_A_H1N1_pdm09_viruses_/985885", "title"=>"Removal of NA V241I and N369K decreases the fitness of recent H275Y A(H1N1)pdm09 viruses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-03 03:06:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1448371"], "description"=>"<p>Surface expressed NA protein and enzymatic activity was assessed 20-transfection of 293T cells with New17 OR (A), or A/California/7/2009 oseltamivir sensitive (Cal7 OS) (B), NA expression plasmids containing a C-terminal V5 epitope tag followed by an IRES-GFP, and encoding the amino acid mutations indicated. NA expression was assessed by flow cytometry after staining with a fluorescently conjugated anti-V5 antibody and gating on the GFP positive (transfected) cells. Enzyme activity was assessed by the <i>in vitro</i> NA inhibition assay. All results represent the mean and standard error of three replicate transfections and are normalised to the mean fluorescent intensity/NA activity of cells transfected with the New17 OR (A) or Cal7 OS (B) wild type NA plasmid. NA activity results for each group were compared to the relative NA activity of New17 OR, for groups shown in A, and Cal7 OS for groups shown in B, using a two-tailed <i>t</i> test. *  = <i>P</i>≤0.05, ** = <i>P</i>≤0.01, ns = <i>P</i>&gt;0.05.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Organismal evolution", "Microbial evolution", "Viral evolution", "microbiology", "Microbial control", "antimicrobials", "antivirals", "Virology", "co-infections", "Emerging viral diseases", "Viral persistence and latency", "Animal models of infection", "Microbial mutation", "Infectious diseases", "Emerging infectious diseases", "v241i", "n369k", "na"], "article_id"=>985884, "categories"=>["Biological Sciences"], "users"=>["Jeff Butler", "Kathryn A. Hooper", "Stephen Petrie", "Raphael Lee", "Sebastian Maurer-Stroh", "Lucia Reh", "Teagan Guarnaccia", "Chantal Baas", "Lumin Xue", "Sophie Vitesnik", "Sook-Kwan Leang", "Jodie McVernon", "Anne Kelso", "Ian G. Barr", "James M. McCaw", "Jesse D. Bloom", "Aeron C. Hurt"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004065.g002", "stats"=>{"downloads"=>0, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/NA_V241I_and_N369K_enhance_the_expression_and_activity_of_A_H1N1_pdm09_NA_proteins_/985884", "title"=>"NA V241I and N369K enhance the expression and activity of A(H1N1)pdm09 NA proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-03 03:06:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1448385", "https://ndownloader.figshare.com/files/1448396", "https://ndownloader.figshare.com/files/1448395", "https://ndownloader.figshare.com/files/1448394", "https://ndownloader.figshare.com/files/1448393", "https://ndownloader.figshare.com/files/1448392", "https://ndownloader.figshare.com/files/1448391", "https://ndownloader.figshare.com/files/1448390", "https://ndownloader.figshare.com/files/1448389", "https://ndownloader.figshare.com/files/1448388", "https://ndownloader.figshare.com/files/1448387", "https://ndownloader.figshare.com/files/1448386", "https://ndownloader.figshare.com/files/1448397"], "description"=>"<div><p>Oseltamivir is relied upon worldwide as the drug of choice for the treatment of human influenza infection. Surveillance for oseltamivir resistance is routinely performed to ensure the ongoing efficacy of oseltamivir against circulating viruses. Since the emergence of the pandemic 2009 A(H1N1) influenza virus (A(H1N1)pdm09), the proportion of A(H1N1)pdm09 viruses that are oseltamivir resistant (OR) has generally been low. However, a cluster of OR A(H1N1)pdm09 viruses, encoding the neuraminidase (NA) H275Y oseltamivir resistance mutation, was detected in Australia in 2011 amongst community patients that had not been treated with oseltamivir. Here we combine a competitive mixtures ferret model of influenza infection with a mathematical model to assess the fitness, both within and between hosts, of recent OR A(H1N1)pdm09 viruses. In conjunction with data from <i>in vitro</i> analyses of NA expression and activity we demonstrate that contemporary A(H1N1)pdm09 viruses are now more capable of acquiring H275Y without compromising their fitness, than earlier A(H1N1)pdm09 viruses circulating in 2009. Furthermore, using reverse engineered viruses we demonstrate that a pair of permissive secondary NA mutations, V241I and N369K, confers robust fitness on recent H275Y A(H1N1)pdm09 viruses, which correlated with enhanced surface expression and enzymatic activity of the A(H1N1)pdm09 NA protein. These permissive mutations first emerged in 2010 and are now present in almost all circulating A(H1N1)pdm09 viruses. Our findings suggest that recent A(H1N1)pdm09 viruses are now more permissive to the acquisition of H275Y than earlier A(H1N1)pdm09 viruses, increasing the risk that OR A(H1N1)pdm09 will emerge and spread worldwide.</p></div>", "links"=>[], "tags"=>["Evolutionary biology", "Organismal evolution", "Microbial evolution", "Viral evolution", "microbiology", "Microbial control", "antimicrobials", "antivirals", "Virology", "co-infections", "Emerging viral diseases", "Viral persistence and latency", "Animal models of infection", "Microbial mutation", "Infectious diseases", "Emerging infectious diseases", "conferred", "permissive", "neuraminidase", "mutations", "oseltamivir-resistant", "influenza"], "article_id"=>985889, "categories"=>["Biological Sciences"], "users"=>["Jeff Butler", "Kathryn A. Hooper", "Stephen Petrie", "Raphael Lee", "Sebastian Maurer-Stroh", "Lucia Reh", "Teagan Guarnaccia", "Chantal Baas", "Lumin Xue", "Sophie Vitesnik", "Sook-Kwan Leang", "Jodie McVernon", "Anne Kelso", "Ian G. Barr", "James M. McCaw", "Jesse D. Bloom", "Aeron C. Hurt"], "doi"=>[nil, nil, nil, nil, nil, nil, nil, nil, nil, nil, nil, nil, nil], "stats"=>{"downloads"=>19, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Estimating_the_Fitness_Advantage_Conferred_by_Permissive_Neuraminidase_Mutations_in_Recent_Oseltamivir_Resistant_A_H1N1_pdm09_Influenza_Viruses/985889", "title"=>"Estimating the Fitness Advantage Conferred by Permissive Neuraminidase Mutations in Recent Oseltamivir-Resistant A(H1N1)pdm09 Influenza Viruses", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-04-03 03:06:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/1448374"], "description"=>"<p>a, OS  =  Oseltamivir sensitive.</p><p>b, OR  =  Oseltamivir resistant due to the NA H275Y mutation.</p><p>c, Relative within-host fitness: values &gt;1 indicate advantage for virus B.</p><p>d, Relative transmission fitness: Values &gt;1 indicate advantage for virus B.</p><p>e, No significant difference is observed when the confidence intervals cross 1.</p>", "links"=>[], "tags"=>["Evolutionary biology", "Organismal evolution", "Microbial evolution", "Viral evolution", "microbiology", "Microbial control", "antimicrobials", "antivirals", "Virology", "co-infections", "Emerging viral diseases", "Viral persistence and latency", "Animal models of infection", "Microbial mutation", "Infectious diseases", "Emerging infectious diseases", "within-host", "pairs", "ferret"], "article_id"=>985887, "categories"=>["Biological Sciences"], "users"=>["Jeff Butler", "Kathryn A. Hooper", "Stephen Petrie", "Raphael Lee", "Sebastian Maurer-Stroh", "Lucia Reh", "Teagan Guarnaccia", "Chantal Baas", "Lumin Xue", "Sophie Vitesnik", "Sook-Kwan Leang", "Jodie McVernon", "Anne Kelso", "Ian G. Barr", "James M. McCaw", "Jesse D. Bloom", "Aeron C. Hurt"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004065.t001", "stats"=>{"downloads"=>3, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Relative_within_host_and_transmission_fitness_of_virus_pairs_used_in_ferret_experiments_/985887", "title"=>"Relative within-host and transmission fitness of virus pairs used in ferret experiments.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-04-03 03:06:21"}

PMC Usage Stats | Further Information

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Relative Metric

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