IRGM is a common target of RNA viruses that subvert the autophagy network.
Autophagy is a conserved degradative pathway used as a host defense mechanism against intracellular pathogens. However, several viruses can evade or subvert autophagy to insure their own replication. Nevertheless, the molecular details of viral interaction with autophagy remain largely unknown. We h...
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Public Library of Science (PLoS)
2011
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oai:doaj.org-article:f522e87acc8f40f39a32b6dfbd15fc1a2021-11-18T06:05:00ZIRGM is a common target of RNA viruses that subvert the autophagy network.1553-73661553-737410.1371/journal.ppat.1002422https://doaj.org/article/f522e87acc8f40f39a32b6dfbd15fc1a2011-12-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22174682/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Autophagy is a conserved degradative pathway used as a host defense mechanism against intracellular pathogens. However, several viruses can evade or subvert autophagy to insure their own replication. Nevertheless, the molecular details of viral interaction with autophagy remain largely unknown. We have determined the ability of 83 proteins of several families of RNA viruses (Paramyxoviridae, Flaviviridae, Orthomyxoviridae, Retroviridae and Togaviridae), to interact with 44 human autophagy-associated proteins using yeast two-hybrid and bioinformatic analysis. We found that the autophagy network is highly targeted by RNA viruses. Although central to autophagy, targeted proteins have also a high number of connections with proteins of other cellular functions. Interestingly, immunity-associated GTPase family M (IRGM), the most targeted protein, was found to interact with the autophagy-associated proteins ATG5, ATG10, MAP1CL3C and SH3GLB1. Strikingly, reduction of IRGM expression using small interfering RNA impairs both Measles virus (MeV), Hepatitis C virus (HCV) and human immunodeficiency virus-1 (HIV-1)-induced autophagy and viral particle production. Moreover we found that the expression of IRGM-interacting MeV-C, HCV-NS3 or HIV-NEF proteins per se is sufficient to induce autophagy, through an IRGM dependent pathway. Our work reveals an unexpected role of IRGM in virus-induced autophagy and suggests that several different families of RNA viruses may use common strategies to manipulate autophagy to improve viral infectivity.Isabel Pombo GrégoireClémence RichettaLaurène Meyniel-SchicklinSophie BorelFabrine PradezynskiOlivier DiazAlexandre DeloireOlga AzocarJoël BaguetMarc Le BretonPhilippe E MangeotVincent NavratilPierre-Emmanuel JoubertMonique FlacherPierre-Olivier VidalainPatrice AndréVincent LotteauMartine Biard-PiechaczykChantal Rabourdin-CombeMathias FaurePublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 7, Iss 12, p e1002422 (2011) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 |
| spellingShingle |
Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Isabel Pombo Grégoire Clémence Richetta Laurène Meyniel-Schicklin Sophie Borel Fabrine Pradezynski Olivier Diaz Alexandre Deloire Olga Azocar Joël Baguet Marc Le Breton Philippe E Mangeot Vincent Navratil Pierre-Emmanuel Joubert Monique Flacher Pierre-Olivier Vidalain Patrice André Vincent Lotteau Martine Biard-Piechaczyk Chantal Rabourdin-Combe Mathias Faure IRGM is a common target of RNA viruses that subvert the autophagy network. |
| description |
Autophagy is a conserved degradative pathway used as a host defense mechanism against intracellular pathogens. However, several viruses can evade or subvert autophagy to insure their own replication. Nevertheless, the molecular details of viral interaction with autophagy remain largely unknown. We have determined the ability of 83 proteins of several families of RNA viruses (Paramyxoviridae, Flaviviridae, Orthomyxoviridae, Retroviridae and Togaviridae), to interact with 44 human autophagy-associated proteins using yeast two-hybrid and bioinformatic analysis. We found that the autophagy network is highly targeted by RNA viruses. Although central to autophagy, targeted proteins have also a high number of connections with proteins of other cellular functions. Interestingly, immunity-associated GTPase family M (IRGM), the most targeted protein, was found to interact with the autophagy-associated proteins ATG5, ATG10, MAP1CL3C and SH3GLB1. Strikingly, reduction of IRGM expression using small interfering RNA impairs both Measles virus (MeV), Hepatitis C virus (HCV) and human immunodeficiency virus-1 (HIV-1)-induced autophagy and viral particle production. Moreover we found that the expression of IRGM-interacting MeV-C, HCV-NS3 or HIV-NEF proteins per se is sufficient to induce autophagy, through an IRGM dependent pathway. Our work reveals an unexpected role of IRGM in virus-induced autophagy and suggests that several different families of RNA viruses may use common strategies to manipulate autophagy to improve viral infectivity. |
| format |
article |
| author |
Isabel Pombo Grégoire Clémence Richetta Laurène Meyniel-Schicklin Sophie Borel Fabrine Pradezynski Olivier Diaz Alexandre Deloire Olga Azocar Joël Baguet Marc Le Breton Philippe E Mangeot Vincent Navratil Pierre-Emmanuel Joubert Monique Flacher Pierre-Olivier Vidalain Patrice André Vincent Lotteau Martine Biard-Piechaczyk Chantal Rabourdin-Combe Mathias Faure |
| author_facet |
Isabel Pombo Grégoire Clémence Richetta Laurène Meyniel-Schicklin Sophie Borel Fabrine Pradezynski Olivier Diaz Alexandre Deloire Olga Azocar Joël Baguet Marc Le Breton Philippe E Mangeot Vincent Navratil Pierre-Emmanuel Joubert Monique Flacher Pierre-Olivier Vidalain Patrice André Vincent Lotteau Martine Biard-Piechaczyk Chantal Rabourdin-Combe Mathias Faure |
| author_sort |
Isabel Pombo Grégoire |
| title |
IRGM is a common target of RNA viruses that subvert the autophagy network. |
| title_short |
IRGM is a common target of RNA viruses that subvert the autophagy network. |
| title_full |
IRGM is a common target of RNA viruses that subvert the autophagy network. |
| title_fullStr |
IRGM is a common target of RNA viruses that subvert the autophagy network. |
| title_full_unstemmed |
IRGM is a common target of RNA viruses that subvert the autophagy network. |
| title_sort |
irgm is a common target of rna viruses that subvert the autophagy network. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2011 |
| url |
https://doaj.org/article/f522e87acc8f40f39a32b6dfbd15fc1a |
| work_keys_str_mv |
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| _version_ |
1718424641818591232 |