Nonclassical autophagy activation pathways are essential for production of infectious Influenza A virus in vitro

Bell, Tisza S.; Velappan, Nileena; Gleasner, Cheryl D.; Xie, Gang; Starkenburg, Shawn R.; Waldo, Geoffrey; Banerjee, Shounak; Micheva‐Viteva, Sofiya N.

doi:10.1111/mmi.14865

Title: Nonclassical autophagy activation pathways are essential for production of infectious Influenza A virus in vitro

Journal Article · 05 January 2022 · Molecular Microbiology

DOI: https://doi.org/10.1111/mmi.14865 · OSTI ID:1841928

Bell, Tisza S. ^[1]; Velappan, Nileena ^[1]; Gleasner, Cheryl D. ^[1]; Xie, Gang ^[1];

^[1]; Waldo, Geoffrey ^[1]; Banerjee, Shounak ^[1];

^[1]

Los Alamos National Lab. (LANL), Los Alamos, NM (United States)

Autophagy is a critical mechanism deployed by eukaryotic cells in response to stress, including viral infection, to boost the innate antimicrobial responses. However, an increasing number of pathogens hijack the autophagic machinery to facilitate their own replication. Influenza A virus (IAV), responsible for several global pandemics, has an intricate dependence on autophagy for successful replication in mammalian cells. To elucidate key chokepoints in the host stress responses facilitating IAV replication, we constructed a meta-transcriptome of IAV and host gene expression dynamics during early (1–3 hpi), mid (4–6 hpi), and late (8–12 hpi) stages of the viral replication cycle at two multiplicities of infection (MOI): 1 and 5. We supplemented the global transcriptome study with phosphoproteomic analysis of stress-activated protein kinase (SAPK/JNK) signaling in lung carcinoma (predominantly used as an in vitro model of IAV replication) and normal human bronchial epithelial cells. We report significant differences in the activation profiles of autophagy regulating genes upon IAV infection at the two MOI as well as divergent dependence on ULK1 signaling within the normal and cancer cells. Regardless of the cell model, JNK-Thr187 signaling was crucial for the production of infectious viral particles.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program

Grant/Contract Number:: 89233218CNA000001

OSTI ID:: 1841928

Report Number(s):: LA-UR--20-30117

Journal Information:: Molecular Microbiology, Journal Name: Molecular Microbiology Journal Issue: 2 Vol. 117; ISSN 0950-382X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (80)

Influenza: Propagation, Quantification, and Storage Szretter, Kristy J.; Balish, Amanda L.; Katz, Jacqueline M. Current Protocols in Microbiology, Vol. 3, Issue 1 https://doi.org/10.1002/0471729256.mc15g01s3	journal	December 2006
Role of Hemagglutinin Cleavage for the Pathogenicity of Influenza Virus Steinhauer, David A. Virology, Vol. 258, Issue 1 https://doi.org/10.1006/viro.1999.9716	journal	May 1999
Control of apoptosis in influenza virus-infected cells by up-regulation of Akt and p53 signaling Zhirnov, Oleg P.; Klenk, Hans-Dieter Apoptosis, Vol. 12, Issue 8 https://doi.org/10.1007/s10495-007-0071-y	journal	April 2007
Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds Holsinger, Leslie J.; Alams, Robert Virology, Vol. 183, Issue 1 https://doi.org/10.1016/0042-6822(91)90115-R	journal	July 1991
Host cell proteases controlling virus pathogenicity Klenk, Hans-Dieter; Garten, Wolfgang Trends in Microbiology, Vol. 2, Issue 2 https://doi.org/10.1016/0966-842X(94)90123-6	journal	February 1994
TSC2 Integrates Wnt and Energy Signals via a Coordinated Phosphorylation by AMPK and GSK3 to Regulate Cell Growth Inoki, Ken; Ouyang, Hongjiao; Zhu, Tianqing Cell, Vol. 126, Issue 5 https://doi.org/10.1016/j.cell.2006.06.055	journal	September 2006
Methods in Mammalian Autophagy Research Mizushima, Noboru; Yoshimori, Tamotsu; Levine, Beth Cell, Vol. 140, Issue 3 https://doi.org/10.1016/j.cell.2010.01.028	journal	February 2010
mTOR Signaling in Growth Control and Disease Laplante, Mathieu; Sabatini, David M. Cell, Vol. 149, Issue 2 https://doi.org/10.1016/j.cell.2012.03.017	journal	April 2012
Biological Functions of Autophagy Genes: A Disease Perspective Levine, Beth; Kroemer, Guido Cell, Vol. 176, Issue 1-2 https://doi.org/10.1016/j.cell.2018.09.048	journal	January 2019
Matrix Protein 2 of Influenza A Virus Blocks Autophagosome Fusion with Lysosomes Gannagé, Monique; Dormann, Dorothee; Albrecht, Randy Cell Host & Microbe, Vol. 6, Issue 4 https://doi.org/10.1016/j.chom.2009.09.005	journal	October 2009
Selective Subversion of Autophagy Complexes Facilitates Completion of the Brucella Intracellular Cycle Starr, Tregei; Child, Robert; Wehrly, Tara D. Cell Host & Microbe, Vol. 11, Issue 1 https://doi.org/10.1016/j.chom.2011.12.002	journal	January 2012
A LC3-Interacting Motif in the Influenza A Virus M2 Protein Is Required to Subvert Autophagy and Maintain Virion Stability Beale, Rupert; Wise, Helen; Stuart, Amanda Cell Host & Microbe, Vol. 15, Issue 2 https://doi.org/10.1016/j.chom.2014.01.006	journal	February 2014
Rictor, a Novel Binding Partner of mTOR, Defines a Rapamycin-Insensitive and Raptor-Independent Pathway that Regulates the Cytoskeleton Current Biology, Vol. 14, Issue 14 https://doi.org/10.1016/j.cub.2004.06.054	journal	July 2004
A Potent and Selective ULK1 Inhibitor Suppresses Autophagy and Sensitizes Cancer Cells to Nutrient Stress Martin, Katie R.; Celano, Stephanie L.; Solitro, Abigail R. iScience, Vol. 8 https://doi.org/10.1016/j.isci.2018.09.012	journal	October 2018
Avian influenza A virus H5N1 causes autophagy-mediated cell death through suppression of mTOR signaling Ma, Jianhui; Sun, Qian; Mi, Ruifang Journal of Genetics and Genomics, Vol. 38, Issue 11 https://doi.org/10.1016/j.jgg.2011.10.002	journal	November 2011
JNK1-Mediated Phosphorylation of Bcl-2 Regulates Starvation-Induced Autophagy Wei, Yongjie; Pattingre, Sophie; Sinha, Sangita Molecular Cell, Vol. 30, Issue 6 https://doi.org/10.1016/j.molcel.2008.06.001	journal	June 2008
Small Molecule Inhibition of the Autophagy Kinase ULK1 and Identification of ULK1 Substrates Egan, Daniel F.; Chun, Matthew G. H.; Vamos, Mitchell Molecular Cell, Vol. 59, Issue 2 https://doi.org/10.1016/j.molcel.2015.05.031	journal	July 2015
Autophagy and MHC-restricted antigen presentation Valečka, Jan; Almeida, Catarina R.; Su, Bing Molecular Immunology, Vol. 99 https://doi.org/10.1016/j.molimm.2018.05.009	journal	July 2018
Autophagy as an emerging dimension to adaptive and innate immunity Hussey, Séamus; Travassos, Leonardo H.; Jones, Nicola L. Seminars in Immunology, Vol. 21, Issue 4 https://doi.org/10.1016/j.smim.2009.05.004	journal	August 2009
The Ras-ERK and PI3K-mTOR pathways: cross-talk and compensation Mendoza, Michelle C.; Er, E. Emrah; Blenis, John Trends in Biochemical Sciences, Vol. 36, Issue 6 https://doi.org/10.1016/j.tibs.2011.03.006	journal	June 2011
The origin and global emergence of adamantane resistant A/H3N2 influenza viruses Nelson, Martha I.; Simonsen, Lone; Viboud, Cécile Virology, Vol. 388, Issue 2 https://doi.org/10.1016/j.virol.2009.03.026	journal	June 2009
Role of c-Jun terminal kinase (JNK) activation in influenza A virus-induced autophagy and replication Zhang, Jingting; Ruan, Tao; Sheng, Tianyu Virology, Vol. 526 https://doi.org/10.1016/j.virol.2018.09.020	journal	January 2019
JNK2 is activated during ER stress and promotes cell survival Raciti, M.; Lotti, L. V.; Valia, S. Cell Death & Disease, Vol. 3, Issue 11 https://doi.org/10.1038/cddis.2012.167	journal	November 2012
Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1β production Saitoh, Tatsuya; Fujita, Naonobu; Jang, Myoung Ho Nature, Vol. 456, Issue 7219 https://doi.org/10.1038/nature07383	journal	October 2008
Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic Smith, Gavin J. D.; Vijaykrishna, Dhanasekaran; Bahl, Justin Nature, Vol. 459, Issue 7250 https://doi.org/10.1038/nature08182	journal	June 2009
Autophagy in immunity and inflammation Levine, Beth; Mizushima, Noboru; Virgin, Herbert W. Nature, Vol. 469, Issue 7330 https://doi.org/10.1038/nature09782	journal	January 2011
Identification of a candidate therapeutic autophagy-inducing peptide Shoji-Kawata, Sanae; Sumpter, Rhea; Leveno, Matthew Nature, Vol. 494, Issue 7436 https://doi.org/10.1038/nature11866	journal	January 2013
Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein Cabantous, Stéphanie; Terwilliger, Thomas C.; Waldo, Geoffrey S. Nature Biotechnology, Vol. 23, Issue 1 https://doi.org/10.1038/nbt1044	journal	January 2005
AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1 Kim, Joungmok; Kundu, Mondira; Viollet, Benoit Nature Cell Biology, Vol. 13, Issue 2 https://doi.org/10.1038/ncb2152	journal	January 2011
Autophagy in infection, inflammation and immunity Deretic, Vojo; Saitoh, Tatsuya; Akira, Shizuo Nature Reviews Immunology, Vol. 13, Issue 10 https://doi.org/10.1038/nri3532	journal	September 2013
Molecular mechanisms of mTOR-mediated translational control Ma, Xiaoju Max; Blenis, John Nature Reviews Molecular Cell Biology, Vol. 10, Issue 5 https://doi.org/10.1038/nrm2672	journal	April 2009
mTOR: from growth signal integration to cancer, diabetes and ageing Zoncu, Roberto; Efeyan, Alejo; Sabatini, David M. Nature Reviews Molecular Cell Biology, Vol. 12, Issue 1 https://doi.org/10.1038/nrm3025	journal	December 2010
Autophagy-activating strategies to promote innate defense against mycobacteria Kim, Yi Sak; Silwal, Prashanta; Kim, Soo Yeon Experimental & Molecular Medicine, Vol. 51, Issue 12 https://doi.org/10.1038/s12276-019-0290-7	journal	December 2019
Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype Kim, Daehwan; Paggi, Joseph M.; Park, Chanhee Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0201-4	journal	August 2019
A New Protein-Protein Interaction Sensor Based on Tripartite Split-GFP Association Cabantous, Stéphanie; Nguyen, Hau B.; Pedelacq, Jean-Denis Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep02854	journal	October 2013
Nutrient starvation elicits an acute autophagic response mediated by Ulk1 dephosphorylation and its subsequent dissociation from AMPK Shang, L.; Chen, S.; Du, F. Proceedings of the National Academy of Sciences, Vol. 108, Issue 12 https://doi.org/10.1073/pnas.1100844108	journal	March 2011
Twenty-five years of mTOR: Uncovering the link from nutrients to growth Sabatini, David M. Proceedings of the National Academy of Sciences, Vol. 114, Issue 45 https://doi.org/10.1073/pnas.1716173114	journal	October 2017
ERK1/2 Phosphorylate Raptor to Promote Ras-dependent Activation of mTOR Complex 1 (mTORC1) Carriere, Audrey; Romeo, Yves; Acosta-Jaquez, Hugo A. Journal of Biological Chemistry, Vol. 286, Issue 1 https://doi.org/10.1074/jbc.M110.159046	journal	January 2011
Autophagy Controls IL-1β Secretion by Targeting Pro-IL-1β for Degradation Harris, James; Hartman, Michelle; Roche, Caitrionna Journal of Biological Chemistry, Vol. 286, Issue 11 https://doi.org/10.1074/jbc.M110.202911	journal	March 2011
Hormonally Active Vitamin D3 (1α,25-Dihydroxycholecalciferol) Triggers Autophagy in Human Macrophages That Inhibits HIV-1 Infection Campbell, Grant R.; Spector, Stephen A. Journal of Biological Chemistry, Vol. 286, Issue 21 https://doi.org/10.1074/jbc.M110.206110	journal	May 2011
ULK1·ATG13·FIP200 Complex Mediates mTOR Signaling and Is Essential for Autophagy Ganley, Ian G.; Lam, Du H.; Wang, Junru Journal of Biological Chemistry, Vol. 284, Issue 18 https://doi.org/10.1074/jbc.M900573200	journal	March 2009
Differential use of autophagy by primary dendritic cells specialized in cross-presentation Mintern, Justine D.; Macri, Christophe; Chin, Wei Jin Autophagy, Vol. 11, Issue 6 https://doi.org/10.1080/15548627.2015.1045178	journal	May 2015
Autophagy gene ATG7 regulates ultraviolet radiation-induced inflammation and skin tumorigenesis Qiang, Lei; Sample, Ashley; Shea, Christopher R. Autophagy, Vol. 13, Issue 12 https://doi.org/10.1080/15548627.2017.1380757	journal	December 2017
Poliovirus induces autophagic signaling independent of the ULK1 complex Corona Velazquez, Angel; Corona, Abigail K.; Klein, Kathryn A. Autophagy, Vol. 14, Issue 7 https://doi.org/10.1080/15548627.2018.1458805	journal	July 2018
Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages Kyei, George B.; Dinkins, Christina; Davis, Alexander S. Journal of Cell Biology, Vol. 186, Issue 2 https://doi.org/10.1083/jcb.200903070	journal	July 2009
ULK-Atg13-FIP200 Complexes Mediate mTOR Signaling to the Autophagy Machinery Jung, Chang Hwa; Jun, Chang Bong; Ro, Seung-Hyun Molecular Biology of the Cell, Vol. 20, Issue 7 https://doi.org/10.1091/mbc.E08-12-1249	journal	April 2009
FAK Is Required for TGFβ-induced JNK Phosphorylation in Fibroblasts: Implications for Acquisition of a Matrix-remodeling Phenotype Liu, Shangxi; Shi-wen, Xu; Kennedy, Laura Molecular Biology of the Cell, Vol. 18, Issue 6 https://doi.org/10.1091/mbc.e06-12-1121	journal	June 2007
HTSeq--a Python framework to work with high-throughput sequencing data Anders, S.; Pyl, P. T.; Huber, W. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu638	journal	September 2014
The Genesis and Spread of Reassortment Human Influenza A/H3N2 Viruses Conferring Adamantane Resistance Simonsen, L.; Viboud, C.; Grenfell, B. T. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm103	journal	April 2007
Enabling the democratization of the genomics revolution with a fully integrated web-based bioinformatics platform Li, Po-E; Lo, Chien-Chi; Anderson, Joseph J. Nucleic Acids Research, Vol. 45, Issue 1 https://doi.org/10.1093/nar/gkw1027	journal	November 2016
A humanized anti-M2 scFv shows protective in vitro activity against influenza Gabbard, J.; Velappan, N.; Di Niro, R. Protein Engineering Design and Selection, Vol. 22, Issue 3 https://doi.org/10.1093/protein/gzn070	journal	October 2008
Inhibition of Autophagy Ameliorates Acute Lung Injury Caused by Avian Influenza A H5N1 Infection Sun, Yang; Li, Chenggang; Shu, Yuelong Science Signaling, Vol. 5, Issue 212 https://doi.org/10.1126/scisignal.2001931	journal	February 2012
Activation of c-jun N-Terminal Kinase upon Influenza A Virus (IAV) Infection Is Independent of Pathogen-Related Receptors but Dependent on Amino Acid Sequence Variations of IAV NS1 Nacken, W.; Anhlan, D.; Hrincius, E. R. Journal of Virology, Vol. 88, Issue 16 https://doi.org/10.1128/JVI.00424-14	journal	May 2014
SH3 Binding Motif 1 in Influenza A Virus NS1 Protein Is Essential for PI3K/Akt Signaling Pathway Activation Shin, Yeun-Kyung; Li, Yang; Liu, Qiang Journal of Virology, Vol. 81, Issue 23 https://doi.org/10.1128/JVI.01427-07	journal	December 2007
Autophagy Promotes Replication of Influenza A Virus In Vitro Wang, Ruifang; Zhu, Yinxing; Zhao, Jiachang Journal of Virology, Vol. 93, Issue 4 https://doi.org/10.1128/JVI.01984-18	journal	February 2019
Influenza A Virus NS1 Protein Activates the PI3K/Akt Pathway To Mediate Antiapoptotic Signaling Responses Ehrhardt, C.; Wolff, T.; Pleschka, S. Journal of Virology, Vol. 81, Issue 7 https://doi.org/10.1128/JVI.02082-06	journal	January 2007
Influenza A Virus Proteins NS1 and Hemagglutinin Along with M2 Are Involved in Stimulation of Autophagy in Infected Cells Zhirnov, O. P.; Klenk, H. D. Journal of Virology, Vol. 87, Issue 24 https://doi.org/10.1128/JVI.02148-13	journal	December 2013
Subversion of Cellular Autophagy Machinery by Hepatitis B Virus for Viral Envelopment Li, J.; Liu, Y.; Wang, Z. Journal of Virology, Vol. 85, Issue 13 https://doi.org/10.1128/JVI.02627-10	journal	April 2011
Protection against Fatal Sindbis Virus Encephalitis by Beclin, a Novel Bcl-2-Interacting Protein Liang, Xiao Huan; Kleeman, Linda K.; Jiang, Hui Hui Journal of Virology, Vol. 72, Issue 11 https://doi.org/10.1128/JVI.72.11.8586-8596.1998	journal	November 1998
Activation of cJUN N-Terminal Kinase by Herpes Simplex Virus Type 1 Enhances Viral Replication McLean, T. I.; Bachenheimer, S. L. Journal of Virology, Vol. 73, Issue 10 https://doi.org/10.1128/JVI.73.10.8415-8426.1999	journal	October 1999
Epstein-Barr Virus-Encoded Latent Membrane Protein 1 Activates the JNK Pathway through Its Extreme C Terminus via a Mechanism Involving TRADD and TRAF2 Eliopoulos, Aristides G.; Blake, Sarah M. S.; Floettmann, J. Eike Journal of Virology, Vol. 73, Issue 2 https://doi.org/10.1128/JVI.73.2.1023-1035.1999	journal	February 1999
Reovirus Infection Activates JNK and the JNK-Dependent Transcription Factor c-Jun Clarke, Penny; Meintzer, Suzanne M.; Widmann, Christian Journal of Virology, Vol. 75, Issue 23 https://doi.org/10.1128/JVI.75.23.11275-11283.2001	journal	December 2001
Cleavage of Influenza A Virus Hemagglutinin in Human Respiratory Epithelium Is Cell Associated and Sensitive to Exogenous Antiproteases Zhirnov, Oleg P.; Ikizler, Mine R.; Wright, Peter F. Journal of Virology, Vol. 76, Issue 17 https://doi.org/10.1128/JVI.76.17.8682-8689.2002	journal	September 2002
BCL-2 Is Phosphorylated and Inactivated by an ASK1/Jun N-Terminal Protein Kinase Pathway Normally Activated at G2/M Yamamoto, Kazuhito; Ichijo, Hidenori; Korsmeyer, Stanley J. Molecular and Cellular Biology, Vol. 19, Issue 12 https://doi.org/10.1128/MCB.19.12.8469	journal	December 1999
Autophagy and the Immune System Kuballa, Petric; Nolte, Whitney M.; Castoreno, Adam B. Annual Review of Immunology, Vol. 30, Issue 1 https://doi.org/10.1146/annurev-immunol-020711-074948	journal	April 2012
Weighing In on mTOR Complex 2 Signaling: The Expanding Role in Cell Metabolism Luo, Yongting; Xu, Wenyi; Li, Guannan Oxidative Medicine and Cellular Longevity, Vol. 2018 https://doi.org/10.1155/2018/7838647	journal	October 2018
Rapid evaluation and quality control of next generation sequencing data with FaQCs Lo, Chien-Chi; Chain, Patrick S. G. BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/s12859-014-0366-2	journal	November 2014
RETRACTED ARTICLE: Roles of the PI3K/AKT/mTOR signalling pathways in neurodegenerative diseases and tumours Xu, Fei; Na, Lixin; Li, Yanfei Cell & Bioscience, Vol. 10, Issue 1 https://doi.org/10.1186/s13578-020-00416-0	journal	April 2020
TFEB at a glance Napolitano, Gennaro; Ballabio, Andrea Journal of Cell Science https://doi.org/10.1242/jcs.146365	journal	January 2016
Influenza virus differentially activates mTORC1 and mTORC2 signaling to maximize late stage replication Kuss-Duerkop, Sharon K.; Wang, Juan; Mena, Ignacio PLOS Pathogens, Vol. 13, Issue 9 https://doi.org/10.1371/journal.ppat.1006635	journal	September 2017
Dysregulation of M segment gene expression contributes to influenza A virus host restriction Calderon, Brenda M.; Danzy, Shamika; Delima, Gabrielle K. PLOS Pathogens, Vol. 15, Issue 8 https://doi.org/10.1371/journal.ppat.1007892	journal	August 2019
West Nile virus capsid protein inhibits autophagy by AMP-activated protein kinase degradation in neurological disease development Kobayashi, Shintaro; Yoshii, Kentaro; Phongphaew, Wallaya PLOS Pathogens, Vol. 16, Issue 1 https://doi.org/10.1371/journal.ppat.1008238	journal	January 2020
Beyond clinical trials: Evolutionary and epidemiological considerations for development of a universal influenza vaccine Viboud, Cécile; Gostic, Katelyn; Nelson, Martha I. PLOS Pathogens, Vol. 16, Issue 9 https://doi.org/10.1371/journal.ppat.1008583	journal	September 2020
Autophagy and Its Interaction With Intracellular Bacterial Pathogens Siqueira, Mariana da Silva; Ribeiro, Renato de Moraes; Travassos, Leonardo H. Frontiers in Immunology, Vol. 9 https://doi.org/10.3389/fimmu.2018.00935	journal	May 2018
Host Receptors of Influenza Viruses and Coronaviruses—Molecular Mechanisms of Recognition Sriwilaijaroen, Nongluk; Suzuki, Yasuo Vaccines, Vol. 8, Issue 4 https://doi.org/10.3390/vaccines8040587	journal	October 2020
Autophagy is involved in influenza A virus replication Zhou, Zhi; Jiang, Xuejun; Liu, Di Autophagy, Vol. 5, Issue 3 https://doi.org/10.4161/auto.5.3.7406	journal	April 2009
ULK1 inhibits the kinase activity of mTORC1 and cell proliferation Jung, Chang Hwa; Seo, Minchul; Otto, Neil Michael Autophagy, Vol. 7, Issue 10 https://doi.org/10.4161/auto.7.10.16660	journal	October 2011
Autophagy stimulation by rapamycin suppresses lung inflammation and infection by Burkholderia cenocepacia in a model of cystic fibrosis Abdulrahman, Basant A.; Khweek, Arwa Abu; Akhter, Anwari Autophagy, Vol. 7, Issue 11 https://doi.org/10.4161/auto.7.11.17660	journal	November 2011
ULK1 inhibits mTORC1 signaling, promotes multisite Raptor phosphorylation and hinders substrate binding Dunlop, Elaine A.; Hunt, David K.; Acosta-Jaquez, Hugo A. Autophagy, Vol. 7, Issue 7 https://doi.org/10.4161/auto.7.7.15491	journal	July 2011
mTOR complex 2 signaling and functions Oh, Won Jun; Jacinto, Estela Cell Cycle, Vol. 10, Issue 14 https://doi.org/10.4161/cc.10.14.16586	journal	July 2011

Similar Records

Autophagic machinery activated by dengue virus enhances virus replication

Journal Article · 2008 · Virology · OSTI ID:21140977

Lee, Y -R; Lei, H -Y; Liu, M -T; +6 more

Single cell heterogeneity in influenza A virus gene expression shapes the innate antiviral response to infection

Journal Article · 2020 · PLoS Pathogens · OSTI ID:1762731

Sun, Jiayi; Vera, J. Cristobal; Drnevich, Jenny; +3 more

Autophagy sustains the replication of porcine reproductive and respiratory virus in host cells

Journal Article · 2012 · Virology · OSTI ID:22149286

Liu, Qinghao; Qin, Yixian; Zhou, Lei; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Influenza A virus
RNA-seq
ULK1 signaling
autophagy
infectious particles
mechanistic target of rapamycin complex 1 (mTORC1)
meta-transcriptome
stress-activated protein kinase (SAPK/JNK)

Title: Nonclassical autophagy activation pathways are essential for production of infectious Influenza A virus in vitro

Citation Formats

References (80)

Similar Records

Related Subjects