Productive infection of human skeletal muscle cells by pandemic and seasonal influenza A(H1N1) viruses.

Besides the classical respiratory and systemic symptoms, unusual complications of influenza A infection in humans involve the skeletal muscles. Numerous cases of acute myopathy and/or rhabdomyolysis have been reported, particularly following the outbreak of pandemic influenza A(H1N1) in 2009. The pa...

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Autores principales: Marion Desdouits, Sandie Munier, Marie-Christine Prevost, Patricia Jeannin, Gillian Butler-Browne, Simona Ozden, Antoine Gessain, Sylvie Van Der Werf, Nadia Naffakh, Pierre-Emmanuel Ceccaldi
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Publicado: Public Library of Science (PLoS) 2013
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spelling oai:doaj.org-article:2ab8858cdb53467ca9c15b91c67680f32021-11-18T08:48:16ZProductive infection of human skeletal muscle cells by pandemic and seasonal influenza A(H1N1) viruses.1932-620310.1371/journal.pone.0079628https://doaj.org/article/2ab8858cdb53467ca9c15b91c67680f32013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24223983/?tool=EBIhttps://doaj.org/toc/1932-6203Besides the classical respiratory and systemic symptoms, unusual complications of influenza A infection in humans involve the skeletal muscles. Numerous cases of acute myopathy and/or rhabdomyolysis have been reported, particularly following the outbreak of pandemic influenza A(H1N1) in 2009. The pathogenesis of these influenza-associated myopathies (IAM) remains unkown, although the direct infection of muscle cells is suspected. Here, we studied the susceptibility of cultured human primary muscle cells to a 2009 pandemic and a 2008 seasonal influenza A(H1N1) isolate. Using cells from different donors, we found that differentiated muscle cells (i. e. myotubes) were highly susceptible to infection by both influenza A(H1N1) isolates, whereas undifferentiated cells (i. e. myoblasts) were partially resistant. The receptors for influenza viruses, α2-6 and α2-3 linked sialic acids, were detected on the surface of myotubes and myoblasts. Time line of viral nucleoprotein (NP) expression and nuclear export showed that the first steps of the viral replication cycle could take place in muscle cells. Infected myotubes and myoblasts exhibited budding virions and nuclear inclusions as observed by transmission electron microscopy and correlative light and electron microscopy. Myotubes, but not myoblasts, yielded infectious virus progeny that could further infect naive muscle cells after proteolytic treatment. Infection led to a cytopathic effect with the lysis of muscle cells, as characterized by the release of lactate dehydrogenase. The secretion of proinflammatory cytokines by muscle cells was not affected following infection. Our results are compatible with the hypothesis of a direct muscle infection causing rhabdomyolysis in IAM patients.Marion DesdouitsSandie MunierMarie-Christine PrevostPatricia JeanninGillian Butler-BrowneSimona OzdenAntoine GessainSylvie Van Der WerfNadia NaffakhPierre-Emmanuel CeccaldiPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 11, p e79628 (2013)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Marion Desdouits
Sandie Munier
Marie-Christine Prevost
Patricia Jeannin
Gillian Butler-Browne
Simona Ozden
Antoine Gessain
Sylvie Van Der Werf
Nadia Naffakh
Pierre-Emmanuel Ceccaldi
Productive infection of human skeletal muscle cells by pandemic and seasonal influenza A(H1N1) viruses.
description Besides the classical respiratory and systemic symptoms, unusual complications of influenza A infection in humans involve the skeletal muscles. Numerous cases of acute myopathy and/or rhabdomyolysis have been reported, particularly following the outbreak of pandemic influenza A(H1N1) in 2009. The pathogenesis of these influenza-associated myopathies (IAM) remains unkown, although the direct infection of muscle cells is suspected. Here, we studied the susceptibility of cultured human primary muscle cells to a 2009 pandemic and a 2008 seasonal influenza A(H1N1) isolate. Using cells from different donors, we found that differentiated muscle cells (i. e. myotubes) were highly susceptible to infection by both influenza A(H1N1) isolates, whereas undifferentiated cells (i. e. myoblasts) were partially resistant. The receptors for influenza viruses, α2-6 and α2-3 linked sialic acids, were detected on the surface of myotubes and myoblasts. Time line of viral nucleoprotein (NP) expression and nuclear export showed that the first steps of the viral replication cycle could take place in muscle cells. Infected myotubes and myoblasts exhibited budding virions and nuclear inclusions as observed by transmission electron microscopy and correlative light and electron microscopy. Myotubes, but not myoblasts, yielded infectious virus progeny that could further infect naive muscle cells after proteolytic treatment. Infection led to a cytopathic effect with the lysis of muscle cells, as characterized by the release of lactate dehydrogenase. The secretion of proinflammatory cytokines by muscle cells was not affected following infection. Our results are compatible with the hypothesis of a direct muscle infection causing rhabdomyolysis in IAM patients.
format article
author Marion Desdouits
Sandie Munier
Marie-Christine Prevost
Patricia Jeannin
Gillian Butler-Browne
Simona Ozden
Antoine Gessain
Sylvie Van Der Werf
Nadia Naffakh
Pierre-Emmanuel Ceccaldi
author_facet Marion Desdouits
Sandie Munier
Marie-Christine Prevost
Patricia Jeannin
Gillian Butler-Browne
Simona Ozden
Antoine Gessain
Sylvie Van Der Werf
Nadia Naffakh
Pierre-Emmanuel Ceccaldi
author_sort Marion Desdouits
title Productive infection of human skeletal muscle cells by pandemic and seasonal influenza A(H1N1) viruses.
title_short Productive infection of human skeletal muscle cells by pandemic and seasonal influenza A(H1N1) viruses.
title_full Productive infection of human skeletal muscle cells by pandemic and seasonal influenza A(H1N1) viruses.
title_fullStr Productive infection of human skeletal muscle cells by pandemic and seasonal influenza A(H1N1) viruses.
title_full_unstemmed Productive infection of human skeletal muscle cells by pandemic and seasonal influenza A(H1N1) viruses.
title_sort productive infection of human skeletal muscle cells by pandemic and seasonal influenza a(h1n1) viruses.
publisher Public Library of Science (PLoS)
publishDate 2013
url https://doaj.org/article/2ab8858cdb53467ca9c15b91c67680f3
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