Multiple Reassortment Events in the Evolutionary History of H1N1 Influenza A Virus Since 1918

Nelson, Martha I.; Viboud, Cécile; Simonsen, Lone; Bennett, Ryan; Griesemer, Sara B.; George, Kirsten St.; Taylor, Jill; Spiro, David; Sengamalay, Naomi; Ghedin, Elodie; Taubenberger, Jeffery K.; Holmes, Edward C.

doi:10.1371/journal.ppat.1000012

Cited by 257 publications

(243 citation statements)

References 36 publications

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“…showed that reassortment occurs at rather low rates in viruses of the family Bunyaviridae (Henderson et al, 1995;Nemirov et al, 1999) or of other families (Fraile et al, 1997;Lin et al, 2004;Roossinck, 2002;Bonnet et al, 2005;Miranda et al, 2000;Iturriza-Gó mara et al, 2001;Watanabe et al, 2001;McDonald et al, 2009), which could be due to strong selection acting against reassortants (Brown et al, 2002;Fraile et al, 1997;Escriu et al, 2007). Some viral taxa seem however to show more extensive reassortment (Silander et al, 2005;Lindstrom et al, 2004;Nelson et al, 2008;Khiabanian et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Evolution and structure of Tomato spotted wilt virus populations: evidence of extensive reassortment and insights into emergence processes

Tentchev

Verdin

Marchal³

et al. 2010

Journal of General Virology

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Tomato spotted wilt virus (TSWV; genus Tospovirus, family Bunyaviridae) genetic diversity was evaluated by sequencing parts of the three RNA genome segments of 224 isolates, mostly from pepper and tomato crops in southern Europe. Eighty-three per cent of the isolates showed consistent clustering into three clades, corresponding to their geographical origin, Spain, France or the USA, for the three RNA segments. In contrast, the remaining 17 % of isolates did not belong to the same clade for the three RNA segments and were shown to be reassortants. Among them, eight different reassortment patterns were observed. Further phylogenetic analyses provided insights into the dynamic processes of the worldwide resurgence of TSWV that, since the 1980s, has followed the worldwide dispersal of the western flower thrips (Frankliniella occidentalis) tospovirus vector. For two clades composed essentially of Old World (OW) isolates, tree topology suggested a local re-emergence of indigenous TSWV populations following F. occidentalis introductions, while it could not be excluded that the ancestors of two other OW clades were introduced from North America contemporarily with F. occidentalis. Finally, estimation of the selection intensity that has affected the evolution of the NSs and nucleocapsid proteins encoded by RNA S of TSWV suggests that the former could be involved in the breakdown of resistance conferred by the Tsw gene in pepper.

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Section: Discussionmentioning

confidence: 99%

Evolution and structure of Tomato spotted wilt virus populations: evidence of extensive reassortment and insights into emergence processes

Tentchev

Verdin

Marchal³

et al. 2010

Journal of General Virology

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“…Genome segmentation complements the high mutation rate of IAV by facilitating reassortment, which can maximize positive intergenic epistasis (2)(3)(4)(5) and allow selective elimination of segments with deleterious mutations (6,7). Although reassortment is the most obvious and best-characterized benefit of segmentation, there are likely additional evolutionary advantages.…”

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confidence: 99%

Influenza A virus nucleoprotein selectively decreases neuraminidase gene-segment packaging while enhancing viral fitness and transmissibility

Brooke

Ince

Wei

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The influenza A virus (IAV) genome is divided into eight distinct RNA segments believed to be copackaged into virions with nearly perfect efficiency. Here, we describe a mutation in IAV nucleoprotein (NP) that enhances replication and transmission in guinea pigs while selectively reducing neuraminidase (NA) gene segment packaging into virions. We show that incomplete IAV particles lacking gene segments contribute to the propagation of the viral population through multiplicity reactivation under conditions of widespread coinfection, which we demonstrate commonly occurs in the upper respiratory tract of guinea pigs. NP also dramatically altered the functional balance of the viral glycoproteins on particles by selectively decreasing NA expression. Our findings reveal novel functions for NP in selective control of IAV gene packaging and balancing glycoprotein expression and suggest a role for incomplete gene packaging during host adaptation and transmission.influenza virus | genome segmentation | genome packaging | nucleoprotein | host adaptation S easonal influenza A virus (IAV) remains a major public health threat, causing tens of thousands of deaths each year in the United States alone (1). Morbidity and mortality rates can increase dramatically when a zoonotic strain adapts to circulate in humans, triggering a pandemic. The continuing toll exerted by IAV stems from its remarkable adaptability, which enables it to move between widely divergent host species and also evade herd immunity within each species. Defining the specific mechanisms that mediate IAV adaptation is essential to improving anti-IAV vaccines, therapeutics, and pandemic surveillance.The IAV genome consists of eight negative-sense RNA segments, each of which is required for productive infection. Genome segmentation complements the high mutation rate of IAV by facilitating reassortment, which can maximize positive intergenic epistasis (2-5) and allow selective elimination of segments with deleterious mutations (6, 7). Although reassortment is the most obvious and best-characterized benefit of segmentation, there are likely additional evolutionary advantages.Genome segmentation imposes the substantial constraint of maintaining a gene-packaging mechanism to produce fully infectious virions (8). For IAV, it is widely believed that a single copy of each segment is packaged into progeny virions with nearly perfect efficiency, resulting in an equimolar ratio of the segments at the population level (9-12). Confounding this model, we recently demonstrated that most IAV virions fail to express one or more gene products (13). This finding raises the possibility that in some circumstances incomplete influenza gene packaging is evolutionarily neutral and possibly even advantageous (14).The viral glycoproteins HA and neuraminidase (NA) are encoded by separate genome segments. HA attaches IAV to terminal sialic acid residues on the host cell surface, enabling viral entry. By hydrolyzing sialic acids, NA detaches budding virions and neutralizes HA-inhibiting glyco...

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“…9,10) Analysis of full genome sequences of representative in‰uenza A (H1N1) viruses from 17 countries andˆve continents that were sampled between 1918 and 2006 shows that all eight segments of the virus have had generally congruent patterns of evolution over time. 11) In‰uenza A (H1N1) abruptly disappeared from humans in 1957 and was replaced by a new reassortant virus called in‰uenza A (H2N2) strain contained three new segments from the avian source and maintained the otherˆve segments from the H1N1 strain of 1918 lineage. 12,14) After this pandemic subtype emerged, human in‰uenza A (H1N1) was not detected again until 1977.…”

Section: Emergence Of Influenza Viruses With Historical Perspectivesmentioning

confidence: 99%

Origins and Evolutionary Genomics of the Novel Swine-Origin Influenza A (H1N1) Virus in Humans —Past and Present Perspectives

Mamun

2011

YAKUGAKU ZASSHI

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Swine in‰uenza viruses cause annual epidemics and occasional pandemics claiming the lives of millions from the early history up to the present days. This virus has drawn on a bag of evolutionary tricks to survive in one or another form in both humans and pigs with novel gene constellations through the periodic importation or exportation of viral genes. A prime example is emergence of pandemic novel swine-origin in‰uenza A (H1N1) virus (S-OIV) in 2009 that have transmitted to and spread among humans, resulting in outbreaks internationally. The phylogenetic analysis of sequences of all genes of the S-OIV, showed that its genome contained six gene segments that were similar to ones previously found in triple-reassortant swine in‰uenza viruses circulating in pigs in North America. The genes encoding neuraminidase and M protein were most closely related to those in in‰uenza A viruses circulating in swine populations in Eurasia. This unique genetic combination of in‰uenza virus gene segments leading to the emergence of novel S-OIV that had not been seen before in the world. Here, it has been used evolutionary analysis to estimate the timescale of the origins and the early development of the S-OIV epidemic. This paper shows that it was derived from several viruses circulating in swine and makes a brie‰y review over the origins and evolutionary genomics of current S-OIV in humans with historical perspectives with a view to exhibition of evolutionary relationship between past and present origins of swine in‰uenza viruses.

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Multiple Reassortment Events in the Evolutionary History of H1N1 Influenza A Virus Since 1918

Cited by 257 publications

References 36 publications

Evolution and structure of Tomato spotted wilt virus populations: evidence of extensive reassortment and insights into emergence processes

Evolution and structure of Tomato spotted wilt virus populations: evidence of extensive reassortment and insights into emergence processes

Influenza A virus nucleoprotein selectively decreases neuraminidase gene-segment packaging while enhancing viral fitness and transmissibility

Origins and Evolutionary Genomics of the Novel Swine-Origin Influenza A (H1N1) Virus in Humans —Past and Present Perspectives

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