Autophagy regulates UBC9 levels during viral-mediated tumorigenesis
UBC9, the sole E2-conjugating enzyme required for SUMOylation, is a key regulator of essential cellular functions and, as such, is frequently altered in cancers. Along these lines, we recently reported that its expression gradually increases during early stages of human papillomavirus (HPV)-mediated...
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| Published in: | PLoS pathogens Vol. 13; no. 3; p. e1006262 |
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| Main Authors: | , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
Public Library of Science
01.03.2017
Public Library of Science (PLoS) |
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| ISSN: | 1553-7374, 1553-7366, 1553-7374 |
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| Abstract | UBC9, the sole E2-conjugating enzyme required for SUMOylation, is a key regulator of essential cellular functions and, as such, is frequently altered in cancers. Along these lines, we recently reported that its expression gradually increases during early stages of human papillomavirus (HPV)-mediated cervical lesions transformation. However, a better understanding of how UBC9 is exploited by transforming viral oncoproteins is still needed. In the present study, we show that in human samples HPV drives UBC9 up-regulation also in very early steps of head and neck tumorigenesis, pointing to the important role for UBC9 in the HPV-mediated carcinogenic program. Moreover, using HPV-infected pre-cancerous tissues and primary human keratinocytes as the natural host of the virus, we investigate the pathological meaning and the cellular mechanisms responsible for UBC9 de-regulation in an oncoviral context. Our results show that UBC9 overexpression is promoted by transforming viral proteins to increase host cells' resistance to apoptosis. In addition, ultrastuctural, pharmacological and genetic approaches crucially unveil that UBC9 is physiologically targeted by autophagy in human cells. However, the presence of HPV E6/E7 oncoproteins negatively impacts the autophagic process through selective inhibition of autophagosome-lysosome fusion, finally leading to p53 dependent UBC9 accumulation during viral-induced cellular transformation. Therefore, our study elucidates how UBC9 is manipulated by HPV oncoproteins, details the physiological mechanism by which UBC9 is degraded in cells, and identifies how HPV E6/E7 impact on autophagy. These findings point to UBC9 and autophagy as novel hallmarks of HPV oncogenesis, and open innovative avenues towards the treatment of HPV-related malignancies. |
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| AbstractList | UBC9, the sole E2-conjugating enzyme required for SUMOylation, is a key regulator of essential cellular functions and, as such, is frequently altered in cancers. Along these lines, we recently reported that its expression gradually increases during early stages of human papillomavirus (HPV)-mediated cervical lesions transformation. However, a better understanding of how UBC9 is exploited by transforming viral oncoproteins is still needed. In the present study, we show that in human samples HPV drives UBC9 up-regulation also in very early steps of head and neck tumorigenesis, pointing to the important role for UBC9 in the HPV-mediated carcinogenic program. Moreover, using HPV-infected pre-cancerous tissues and primary human keratinocytes as the natural host of the virus, we investigate the pathological meaning and the cellular mechanisms responsible for UBC9 de-regulation in an oncoviral context. Our results show that UBC9 overexpression is promoted by transforming viral proteins to increase host cells’ resistance to apoptosis. In addition, ultrastuctural, pharmacological and genetic approaches crucially unveil that UBC9 is physiologically targeted by autophagy in human cells. However, the presence of HPV E6/E7 oncoproteins negatively impacts the autophagic process through selective inhibition of autophagosome-lysosome fusion, finally leading to p53 dependent UBC9 accumulation during viral-induced cellular transformation. Therefore, our study elucidates how UBC9 is manipulated by HPV oncoproteins, details the physiological mechanism by which UBC9 is degraded in cells, and identifies how HPV E6/E7 impact on autophagy. These findings point to UBC9 and autophagy as novel hallmarks of HPV oncogenesis, and open innovative avenues towards the treatment of HPV-related malignancies. High risk HPV is the primary cause of cervical cancer and in recent years a clear role for the virus in other anogenital malignancies, in head and neck and in nonmelanoma skin cancers is emerging. Cellular transformation is mediated by the viral oncoproteins E6 and E7 that have the ability to target several pathways. We recently demonstrated that UBC9, the key enzyme of the Small Ubiquitin-like Modifier (SUMO) pathway, is up-regulated during pre-cancerous and cancerous stages of cervical carcinogenesis. In this study, we elucidate the pathological impact and the cellular mechanisms responsible for UBC9 accumulation promoted by HPV in cervical and head and neck pre-cancerous tissues. Indeed, we show that UBC9 is physiologically degraded in cells by autophagy, and that the expression of HPV oncoproteins impairs autophagy finally leading to UBC9 accumulation and apoptosis resistance of infected cells. Our results therefore identify UBC9 and autophagy as important co-factors to prime early stages of HPV-mediated tumorigenesis, and pinpoint novel therapeutic strategies for treatment of carcinogenic HPV infections. UBC9, the sole E2-conjugating enzyme required for SUMOylation, is a key regulator of essential cellular functions and, as such, is frequently altered in cancers. Along these lines, we recently reported that its expression gradually increases during early stages of human papillomavirus (HPV)-mediated cervical lesions transformation. However, a better understanding of how UBC9 is exploited by transforming viral oncoproteins is still needed. In the present study, we show that in human samples HPV drives UBC9 up-regulation also in very early steps of head and neck tumorigenesis, pointing to the important role for UBC9 in the HPV-mediated carcinogenic program. Moreover, using HPV-infected pre-cancerous tissues and primary human keratinocytes as the natural host of the virus, we investigate the pathological meaning and the cellular mechanisms responsible for UBC9 de-regulation in an oncoviral context. Our results show that UBC9 overexpression is promoted by transforming viral proteins to increase host cells' resistance to apoptosis. In addition, ultrastuctural, pharmacological and genetic approaches crucially unveil that UBC9 is physiologically targeted by autophagy in human cells. However, the presence of HPV E6/E7 oncoproteins negatively impacts the autophagic process through selective inhibition of autophagosome-lysosome fusion, finally leading to p53 dependent UBC9 accumulation during viral-induced cellular transformation. Therefore, our study elucidates how UBC9 is manipulated by HPV oncoproteins, details the physiological mechanism by which UBC9 is degraded in cells, and identifies how HPV E6/E7 impact on autophagy. These findings point to UBC9 and autophagy as novel hallmarks of HPV oncogenesis, and open innovative avenues towards the treatment of HPV-related malignancies. UBC9, the sole E2-conjugating enzyme required for SUMOylation, is a key regulator of essential cellular functions and, as such, is frequently altered in cancers. Along these lines, we recently reported that its expression gradually increases during early stages of human papillomavirus (HPV)-mediated cervical lesions transformation. However, a better understanding of how UBC9 is exploited by transforming viral oncoproteins is still needed. In the present study, we show that in human samples HPV drives UBC9 up-regulation also in very early steps of head and neck tumorigenesis, pointing to the important role for UBC9 in the HPV-mediated carcinogenic program. Moreover, using HPV-infected pre-cancerous tissues and primary human keratinocytes as the natural host of the virus, we investigate the pathological meaning and the cellular mechanisms responsible for UBC9 de-regulation in an oncoviral context. Our results show that UBC9 overexpression is promoted by transforming viral proteins to increase host cells' resistance to apoptosis. In addition, ultrastuctural, pharmacological and genetic approaches crucially unveil that UBC9 is physiologically targeted by autophagy in human cells. However, the presence of HPV E6/E7 oncoproteins negatively impacts the autophagic process through selective inhibition of autophagosome-lysosome fusion, finally leading to p53 dependent UBC9 accumulation during viral-induced cellular transformation. Therefore, our study elucidates how UBC9 is manipulated by HPV oncoproteins, details the physiological mechanism by which UBC9 is degraded in cells, and identifies how HPV E6/E7 impact on autophagy. These findings point to UBC9 and autophagy as novel hallmarks of HPV oncogenesis, and open innovative avenues towards the treatment of HPV-related malignancies.UBC9, the sole E2-conjugating enzyme required for SUMOylation, is a key regulator of essential cellular functions and, as such, is frequently altered in cancers. Along these lines, we recently reported that its expression gradually increases during early stages of human papillomavirus (HPV)-mediated cervical lesions transformation. However, a better understanding of how UBC9 is exploited by transforming viral oncoproteins is still needed. In the present study, we show that in human samples HPV drives UBC9 up-regulation also in very early steps of head and neck tumorigenesis, pointing to the important role for UBC9 in the HPV-mediated carcinogenic program. Moreover, using HPV-infected pre-cancerous tissues and primary human keratinocytes as the natural host of the virus, we investigate the pathological meaning and the cellular mechanisms responsible for UBC9 de-regulation in an oncoviral context. Our results show that UBC9 overexpression is promoted by transforming viral proteins to increase host cells' resistance to apoptosis. In addition, ultrastuctural, pharmacological and genetic approaches crucially unveil that UBC9 is physiologically targeted by autophagy in human cells. However, the presence of HPV E6/E7 oncoproteins negatively impacts the autophagic process through selective inhibition of autophagosome-lysosome fusion, finally leading to p53 dependent UBC9 accumulation during viral-induced cellular transformation. Therefore, our study elucidates how UBC9 is manipulated by HPV oncoproteins, details the physiological mechanism by which UBC9 is degraded in cells, and identifies how HPV E6/E7 impact on autophagy. These findings point to UBC9 and autophagy as novel hallmarks of HPV oncogenesis, and open innovative avenues towards the treatment of HPV-related malignancies. |
| Audience | Academic |
| Author | Pawlita, Michael Chiocca, Susanna Tacchetti, Carlo Casadio, Chiara Tommasino, Massimo Raimondi, Andrea Mattoscio, Domenico Ansarin, Mohssen Galimberti, Viviana E. De Lorenzi, Francesca Chiesa, Fausto Tagliabue, Marta Maffini, Fausto Miccolo, Claudia Gheit, Tarik |
| AuthorAffiliation | 1 European Institute of Oncology, Department of Experimental Oncology, Milan, Italy 3 Experimental Imaging Center, IRCCS San Raffaele Scientific Institute, Milan, Italy 7 European Institute of Oncology Senology Division, Milan, Italy 5 Infections and Cancer Biology Group, International Agency for Research on Cancer, Lyon, France University of North Carolina at Chapel Hill, UNITED STATES 4 Department of Experimental Medicine, University of Genova, Genova, Italy 2 European Institute of Oncology, Department of Pathology, Milan, Italy 9 Division of Molecular Diagnostics of Oncogenic Infections, Research Program Infection, Inflammation and Cancer, German Cancer Research Center, Heidelberg, Germany 6 European Institute of Oncology, Division of Otolaryngology and Head and Neck Surgery, Milan, Italy 8 European Institute of Oncology, Plastic Surgery Department, Milan, Italy |
| AuthorAffiliation_xml | – name: 7 European Institute of Oncology Senology Division, Milan, Italy – name: 2 European Institute of Oncology, Department of Pathology, Milan, Italy – name: University of North Carolina at Chapel Hill, UNITED STATES – name: 1 European Institute of Oncology, Department of Experimental Oncology, Milan, Italy – name: 6 European Institute of Oncology, Division of Otolaryngology and Head and Neck Surgery, Milan, Italy – name: 5 Infections and Cancer Biology Group, International Agency for Research on Cancer, Lyon, France – name: 4 Department of Experimental Medicine, University of Genova, Genova, Italy – name: 3 Experimental Imaging Center, IRCCS San Raffaele Scientific Institute, Milan, Italy – name: 8 European Institute of Oncology, Plastic Surgery Department, Milan, Italy – name: 9 Division of Molecular Diagnostics of Oncogenic Infections, Research Program Infection, Inflammation and Cancer, German Cancer Research Center, Heidelberg, Germany |
| Author_xml | – sequence: 1 givenname: Domenico surname: Mattoscio fullname: Mattoscio, Domenico – sequence: 2 givenname: Chiara surname: Casadio fullname: Casadio, Chiara – sequence: 3 givenname: Claudia surname: Miccolo fullname: Miccolo, Claudia – sequence: 4 givenname: Fausto surname: Maffini fullname: Maffini, Fausto – sequence: 5 givenname: Andrea surname: Raimondi fullname: Raimondi, Andrea – sequence: 6 givenname: Carlo surname: Tacchetti fullname: Tacchetti, Carlo – sequence: 7 givenname: Tarik surname: Gheit fullname: Gheit, Tarik – sequence: 8 givenname: Marta surname: Tagliabue fullname: Tagliabue, Marta – sequence: 9 givenname: Viviana E. surname: Galimberti fullname: Galimberti, Viviana E. – sequence: 10 givenname: Francesca surname: De Lorenzi fullname: De Lorenzi, Francesca – sequence: 11 givenname: Michael orcidid: 0000-0002-4720-8306 surname: Pawlita fullname: Pawlita, Michael – sequence: 12 givenname: Fausto surname: Chiesa fullname: Chiesa, Fausto – sequence: 13 givenname: Mohssen surname: Ansarin fullname: Ansarin, Mohssen – sequence: 14 givenname: Massimo surname: Tommasino fullname: Tommasino, Massimo – sequence: 15 givenname: Susanna orcidid: 0000-0002-9721-0850 surname: Chiocca fullname: Chiocca, Susanna |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28253371$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2017 Public Library of Science 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Mattoscio D, Casadio C, Miccolo C, Maffini F, Raimondi A, Tacchetti C, et al. (2017) Autophagy regulates UBC9 levels during viral-mediated tumorigenesis. PLoS Pathog 13(3): e1006262. https://doi.org/10.1371/journal.ppat.1006262 2017 Mattoscio et al 2017 Mattoscio et al 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Mattoscio D, Casadio C, Miccolo C, Maffini F, Raimondi A, Tacchetti C, et al. (2017) Autophagy regulates UBC9 levels during viral-mediated tumorigenesis. PLoS Pathog 13(3): e1006262. https://doi.org/10.1371/journal.ppat.1006262 |
| Copyright_xml | – notice: COPYRIGHT 2017 Public Library of Science – notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Mattoscio D, Casadio C, Miccolo C, Maffini F, Raimondi A, Tacchetti C, et al. (2017) Autophagy regulates UBC9 levels during viral-mediated tumorigenesis. PLoS Pathog 13(3): e1006262. https://doi.org/10.1371/journal.ppat.1006262 – notice: 2017 Mattoscio et al 2017 Mattoscio et al – notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Mattoscio D, Casadio C, Miccolo C, Maffini F, Raimondi A, Tacchetti C, et al. (2017) Autophagy regulates UBC9 levels during viral-mediated tumorigenesis. PLoS Pathog 13(3): e1006262. https://doi.org/10.1371/journal.ppat.1006262 |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 MP received research funding from cooperation contracts from the DKFZ with Roche and Qiagen. He is inventor and receives royalties on a patent held by DKFZ in the field of molecular diagnostics for infectious disease. Conceptualization: DM SC.Formal analysis: DM SC.Funding acquisition: FC MP MTo SC.Investigation: DM CC CM FM AR CT TG MP SC.Methodology: DM SC.Project administration: SC.Resources: MTa VEG FDL FC MA SC.Supervision: SC.Validation: DM CM SC.Visualization: DM CC CM FM SC.Writing – original draft: DM SC.Writing – review & editing: DM MTo SC. |
| ORCID | 0000-0002-9721-0850 0000-0002-4720-8306 |
| OpenAccessLink | http://dx.doi.org/10.1371/journal.ppat.1006262 |
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| PublicationDate | 2017-03-01 |
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| SubjectTerms | Apoptosis Autophagy Autophagy (Cytology) Autophagy - physiology Biology and life sciences Brain cancer Carcinogens Care and treatment Cell cycle Cell death Cell Transformation, Neoplastic Cell Transformation, Viral - physiology Cellular proteins Cervical cancer Development and progression Enzymes Female Flow Cytometry Genetic aspects Genetic transformation Head Head & neck cancer Head and neck Health aspects Human papillomavirus Humans Immunoblotting Immunohistochemistry Infections Keratinocytes Lesions Medical research Medicine and Health Sciences Microscopy, Confocal Oncogene Proteins, Viral Oncology Otolaryngology p53 Protein Papillomaviridae - metabolism Papillomavirus infections Papillomavirus Infections - metabolism Papillomavirus Infections - pathology Pathology Phagocytosis Pharmacology Polymerase Chain Reaction Proteins Research and Analysis Methods Rodents SUMO protein Surgery Tissues Transduction, Genetic Transfection Transformation Tumorigenesis Ubiquitin-Conjugating Enzyme UBC9 Ubiquitin-Conjugating Enzymes - metabolism Viruses |
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| Title | Autophagy regulates UBC9 levels during viral-mediated tumorigenesis |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/28253371 https://www.proquest.com/docview/1900162863 https://www.proquest.com/docview/1874442598 https://pubmed.ncbi.nlm.nih.gov/PMC5349695 https://doaj.org/article/4db8a8c3ffdd42f3b3e247e424fd03ed http://dx.doi.org/10.1371/journal.ppat.1006262 |
| Volume | 13 |
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