MTOR/p70S6K signaling distinguishes routine, maintenance-level autophagy from autophagic cell death during influenza A infection

Virology

Volumn 452-453, Issue , 2014, Pages 175-190

  Datan, Emmanuel ^a   Shirazian, Alireza ^a,e   Benjamin, Shawna ^a,e   Matassov, Demetrius ^a   Tinari, Antonella ^b   Malorni, Walter ^b,c   Lockshin, Richard A ^a   Garcia Sastre, Adolfo ^d   Zakeri, Zahra ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c San Raffaele Institute Sulmona   (Italy)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e Profectus Bio Sciences   (United States)

Author keywords

Apoptosis; Autophagy; Cell death; Influenza; MTORC1 2; P70S6K; Rapamycin; Torin1

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; P70S6 KINASE; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL DEATH; CELL STRESS; CELL SURVIVAL; CHICKEN; CONTROLLED STUDY; DOG; EMBRYO; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; INFLUENZA A; INFLUENZA VIRUS A; INTRACELLULAR SIGNALING; MOUSE; NECROPTOSIS; NONHUMAN; PRIORITY JOURNAL; VIRUS REPLICATION;

APOPTOSIS; AUTOPHAGY; CELL DEATH; INFLUENZA; MTORC1/2; P70S6K; RAPAMYCIN; TORIN1;

APOPTOSIS; AUTOPHAGY; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MULTIPROTEIN COMPLEXES; PHOSPHATIDYLINOSITOL 3-KINASES; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84893478933     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.01.008     Document Type: Article

References (64)

1. Abeliovich H., Dunn W.A., Kim J., Klionsky D.J. Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J. Cell Biol. 2000, 151:1025-1034.
2. Alexander A., Cai S.L., Kim J., Nanez A., Sahin M., MacLean K.H., Inoki K., Guan K.L., Shen J., Person M.D., Kusewitt D., Mills G.B., Kastan M.B., Walker C.L. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc. Natl. Acad. Sci. USA 2010, 107:4153-4158.
3. Avni D., Shama S., Loreni F., Meyuhas O. Vertebrate mRNAs with a 5'-terminal pyrimidine tract are candidates for translational repression in quiescent cells: characterization of the translational cis-regulatory element. Mol. Cell. Biol. 1994, 14:3822-3833.
4. Aweya J.J., Mak T.M., Lim S.G., Tan Y.J. The p7 protein of the hepatitis C virus induces cell death differently from the influenza A virus viroporin M2. Virus Res. 2013, 172:24-34.
5. Chang Y.Y., Juhasz G., Goraksha-Hicks P., Arsham A.M., Mallin D.R., Muller L.K., Neufeld T.P. Nutrient-dependent regulation of autophagy through the target of rapamycin pathway. Biochem. Soc. Trans. 2009, 37:232-236.
6. Chen W., Calvo P.A., Malide D., Gibbs J., Schubert U., Bacik I., Basta S., O'Neill R., Schickli J., Palese P., Henklein P., Bennink J.R., Yewdell J.W. A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med. 2001, 7:1306-1312.
7. Corradetti M., Guan K. Upstream of the mammalian target of rapamycin: do all roads pass through mTOR?. Oncogene 2006, 25:6347-6360.
8. Degterev A., Huang Z., Boyce M., Li Y., Jagtap P., Mizushima N., Cuny G.D., Mitchison T.J., Moskowitz M.A., Yuan J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 2005, 1:112-119.
9. Feldman M.E., Apsel B., Uotila A., Loewith R., Knight Z.A., Ruggero D., Shokat K.M. Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol. 2009, 7:e38.
10. Gannage M., Dormann D., Albrecht R., Dengjel J., Torossi T., Ramer P.C., Lee M., Strowig T., Arrey F., Conenello G., Pypaert M., Andersen J., Garcia-Sastre A., Munz C. Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 2009, 6:367-380.
11. Gill J.R., Sheng Z.M., Ely S.F., Guinee D.G., Beasley M.B., Suh J., Deshpande C., Mollura D.J., Morens D.M., Bray M., Travis W.D., Taubenberger J.K. Pulmonary pathologic findings of fatal 2009 pandemic influenza A/H1N1 viral infections. Arch. Pathol. Lab. Med. 2010, 134:235-243.
12. Hale B.G., Jackson D., Chen Y.H., Lamb R.A., Randall R.E. Influenza A virus NS1 protein binds p85beta and activates phosphatidylinositol-3-kinase signaling. Proc. Natl. Acad. Sci. USA 2006, 103:14194-14199.
13. Han J.W., Pearson R.B., Dennis P.B., Thomas G. Rapamycin, wortmannin, and the methylxanthine SQ20006 inactivate p70s6k by inducing dephosphorylation of the same subset of sites. J. Biol. Chem. 1995, 270:21396-21403.
14. Ilyinskii P.O., Gambaryan A.S., Meriin A.B., Gabai V., Kartashov A., Thoidis G., Shneider A.M. Inhibition of influenza M2-induced cell death alleviates its negative contribution to vaccination efficiency. PLoS One 2008, 3:e1417.
15. Ito T., Kobayashi Y., Morita T., Horimoto T., Kawaoka Y. Virulent influenza A viruses induce apoptosis in chickens. Virus Res. 2002, 84:27-35.
16. Jefferies H.B., Fumagalli S., Dennis P.B., Reinhard C., Pearson R.B., Thomas G. Rapamycin suppresses 5'TOP mRNA translation through inhibition of p70s6k. EMBO J. 1997, 16:3693-3704.
17. Jiang B.H., Liu L.Z. PI3K/PTEN signaling in tumorigenesis and angiogenesis. Biochim. Biophys. Acta (BBA) - Proteins Proteomics 2008, 1784:150-158.
18. Karasavvas N., Zakeri Z. Relationships of apoptotic signaling mediated by ceramide and TNF-alpha in U937 cells. Cell Death Differ. 1999, 6:115-123.
19. Kim K.W., Mutter R.W., Cao C., Albert J.M., Freeman M., Hallahan D.E., Lu B. Autophagy for cancer therapy through inhibition of pro-apoptotic proteins and mammalian target of rapamycin signaling. J. of Biol. Chem. 2006, 281:36883-36890.
20. Lawrence B.P., Brown W.J. Inhibition of protein synthesis separates autophagic sequestration from the delivery of lysosomal enzymes. J. Cell Sci. 1993, 105(Pt. 2):73--80..
21. Lazareno S., Popham A., Birdsall N.J. Muscarinic interactions of bisindolylmaleimide analogues. Eur. J. Pharmacol. 1998, 360:281-284.
22. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008, 132:27-42.
23. Levy S., Avni D., Hariharan N., Perry R.P., Meyuhas O. Oligopyrimidine tract at the 5' end of mammalian ribosomal protein mRNAs is required for their translational control. Proc. Natl. Acad. Sci. USA 1991, 88:3319-3323.
24. Lin L., Ye Y., Zakeri Z. p53, Apaf-1, caspase-3, and -9 are dispensable for Cdk5 activation during cell death. Cell Death Differ. 2006, 13:141-150.
25. Liu Q., Chang J.W., Wang J., Kang S.A., Thoreen C.C., Markhard A., Hur W., Zhang J., Sim T., Sabatini D.M., Gray N.S. Discovery of 1-(4-(4-propionylpiperazin-1-yl)-3-(trifluoromethyl)phenyl)-9-(quinolin-3-yl)benz o[h][1,6]naphthyridin-2(1H)-one as a highly potent, selective mammalian target of rapamycin (mTOR) inhibitor for the treatment of cancer. J. Med. Chem. 2010, 53:7146-7155.
26. Lockshin R.A., Zakeri Z. Caspase-independent cell deaths. Curr. Opin. Cell Biol. 2002, 14:727-733.
27. Marmy-Conus N., Hannan K.M., Pearson R.B. Ro 31-6045, the inactive analogue of the protein kinase C inhibitor Ro 31-8220, blocks in vivo activation of p70(s6k)/p85(s6k): implications for the analysis of S6K signalling. FEBS Lett. 2002, 519:135-140.
28. McLean J.E., Datan E., Matassov D., Zakeri Z.F. Lack of Bax prevents influenza A virus-induced apoptosis and causes diminished viral replication. J. Virol. 2009, 83:8233-8246.
29. McLean J.E., Wudzinska A., Datan E., Quaglino D., Zakeri Z. Flavivirus NS4A-induced autophagy protects cells against death and enhances virus replication. J. Biol. Chem. 2011, 286:22147.
30. Meyer L.R., Zweig A.S., Hinrichs A.S., Karolchik D., Kuhn R.M., Wong M., Sloan C.A., Rosenbloom K.R., Roe G., Rhead B., Raney B.J., Pohl A., Malladi V.S., Li C.H., Lee B.T., Learned K., Kirkup V., Hsu F., Heitner S., Harte R.A., Haeussler M., Guruvadoo L., Goldman M., Giardine B.M., Fujita P.A., Dreszer T.R., Diekhans M., Cline M.S., Clawson H., Barber G.P., Haussler D., Kent W.J. The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res. 2013, 41:D64-D69.
31. Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell 2010, 140:313-326.
32. Mohsin M.A., Morris S.J., Smith H., Sweet C. Correlation between levels of apoptosis, levels of infection and haemagglutinin receptor binding interaction of various subtypes of influenza virus: does the viral neuraminidase have a role in these associations. Virus Res. 2002, 85:123-131.
33. Mori I., Komatsu T., Takeuchi K., Nakakuki K., Sudo M., Kimura Y. In vivo induction of apoptosis by influenza virus. J. Gen. Virol. 1995, 76:2869.
34. Morris S.J., Price G.E., Barnett J.M., Hiscox S.A., Smith H., Sweet C. Role of neuraminidase in influenza virus-induced apoptosis. J. Gen. Virol. 1999, 80(Pt. 1):137-146.
35. Nencioni L., De Chiara G., Sgarbanti R., Amatore D., Aquilano K., Marcocci M.E., Serafino A., Torcia M., Cozzolino F., Ciriolo M.R., Garaci E., Palamara A.T. Bcl-2 expression and p38MAPK activity in cells infected with influenza A virus: impact on virally induced apoptosis and viral replication. J. Biol. Chem. 2009, 284:16004-16015.
36. Nicklin P., Bergman P., Zhang B., Triantafellow E., Wang H., Nyfeler B., Yang H., Hild M., Kung C., Wilson C., Myer V.E., MacKeigan J.P., Porter J.A., Wang Y.K., Cantley L.C., Finan P.M., Murphy L.O. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 2009, 136:521-534.
37. Olsen C.W., Kehren J.C., Dybdahl-Sissoko N.R., Hinshaw V.S. bcl-2 alters influenza virus yield, spread, and hemagglutinin glycosylation. J. Virol. 1996, 70:663-666.
38. Pastor M.D., Garcia-Yebenes I., Fradejas N., Perez-Ortiz J.M., Mora-Lee S., Tranque P., Moro M.A., Pende M., Calvo S. mTOR/S6 kinase pathway contributes to astrocyte survival during ischemia. J. Biol. Chem. 2009, 284:22067-22078.
39. Pattingre S., Espert L., Biard-Piechaczyk M., Codogno P. Regulation of macroautophagy by mTOR and Beclin 1 complexes. Biochimie 2008, 90:313-323.
40. Ravikumar B., Sarkar S., Davies J.E., Futter M., Garcia-Arencibia M., Green-Thompson Z.W., Jimenez-Sanchez M., Korolchuk V.I., Lichtenberg M., Luo S., Massey D.C., Menzies F.M., Moreau K., Narayanan U., Renna M., Siddiqi F.H., Underwood B.R., Winslow A.R., Rubinsztein D.C. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol. Rev. 2010, 90:1383-1435.
41. Scott R.C., Schuldiner O., Neufeld T.P. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 2004, 7:167-178.
42. Sekulic A., Hudson C.C., Homme J.L., Yin P., Otterness D.M., Karnitz L.M., Abraham R.T. A direct linkage between the phosphoinositide 3-kinase-AKT signaling pathway and the mammalian target of rapamycin in mitogen-stimulated and transformed cells. Cancer Res. 2000, 60:3504-3513.
43. Setalo G., Singh M., Nethrapalli I.S., Toran-Allerand C.D. Protein kinase C activity is necessary for estrogen-induced Erk phosphorylation in neocortical explants. Neurochem. Res. 2005, 30:779-790.
44. Suh Y., Afaq F., Khan N., Johnson J.J., Khusro F.H., Mukhtar H. Fisetin induces autophagic cell death through suppression of mTOR signaling pathway in prostate cancer cells. Carcinogenesis 2010, 31:1424-1433.
45. Tanida I., Minematsu-Ikeguchi N., Ueno T., Kominami E. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 2005, 1:84-91.
46. Taubenberger J.K., Morens D.M. The pathology of influenza virus infections. Annu. Rev. Pathol. 2008, 3:499-522.
47. Tripathi S., Batra J., Cao W., Sharma K., Patel J.R., Ranjan P., Kumar A., Katz J.M., Cox N.J., Lal R.B., Sambhara S., Lal S.K. Influenza A virus nucleoprotein induces apoptosis in human airway epithelial cells: implications of a novel interaction between nucleoprotein and host protein Clusterin. Cell Death Dis. 2013, 4:e562.
48. Tsujimoto Y., Shimizu S. Another way to die: autophagic programmed cell death. Cell Death Differ. 2005, 12(Suppl. 2):S1528-S1534.
49. Vanhaesebroeck B., Alessi D.R. The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 2000, 346(Pt. 3):561-576.
50. White E. Autophagic cell death unraveled: pharmacological inhibition of apoptosis and autophagy enables necrosis. Autophagy 2008, 4:399-401.
51. Widjaja I., de Vries E., Rottier P.J., de Haan C.A. Competition between influenza A virus genome segments. PLoS One 2012, 7:e47529.
52. Wong C.H., Iskandar K.B., Yadav S.K., Hirpara J.L., Loh T., Pervaiz S. Simultaneous induction of non-canonical autophagy and apoptosis in cancer cells by ROS-dependent ERK and JNK activation. PLoS One 2010, 5:e9996.
53. Wu Y.T., Tan H.L., Huang Q., Kim Y.S., Pan N., Ong W.Y., Liu Z.G., Ong C.N., Shen H.M. Autophagy plays a protective role during zVAD-induced necrotic cell death. Autophagy 2008, 4:457-466.
54. Wurzer W.J., Planz O., Ehrhardt C., Giner M., Silberzahn T., Pleschka S., Ludwig S. Caspase 3 activation is essential for efficient influenza virus propagation. EMBO J. 2003, 22:2717-2728.
55. Wurzer W.J., Ehrhardt C., Pleschka S., Berberich-Siebelt F., Wolff T., Walczak H., Planz O., Ludwig S. NF-kappaB-dependent induction of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and Fas/FasL is crucial for efficient influenza virus propagation. J. Biol. Chem. 2004, 279:30931-30937.
56. Yamashita R., Suzuki Y., Takeuchi N., Wakaguri H., Ueda T., Sugano S., Nakai K. Comprehensive detection of human terminal oligo-pyrimidine (TOP) genes and analysis of their characteristics. Nucleic Acids Res. 2008, 36:3707-3715.
57. Yang J.C., Chien C.T. A new approach for the prevention and treatment of Helicobacter pylori infection via upregulation of autophagy and downregulation of apoptosis. Autophagy 2009, 5:413-414.
58. Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell death Differ. 2005, 12(Suppl. 2):S1542-S1552.
59. Zakeri Z., Lockshin R.A., Criado-Rodriguez L.M., Martinez A.C. A generalized caspase inhibitor disrupts early mammalian development. Int. J. Dev. Biol. 2005, 49:43-47.
60. Zamarin D., Garcia-Sastre A., Xiao X., Wang R., Palese P. Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLoS Pathog. 2005, 1:e4.
61. Zhang C., Yang Y., Zhou X., Liu X., Song H., He Y., Huang P. Highly pathogenic avian influenza A virus H5N1 NS1 protein induces caspase-dependent apoptosis in human alveolar basal epithelial cells. Virol. J. 2010, 7:51.
62. Zhirnov O.P., Klenk H.D. Alterations in caspase cleavage motifs of NP and M2 proteins attenuate virulence of a highly pathogenic avian influenza virus. Virology 2009, 394:57-63.
63. Zhirnov O.P., Konakova T.E., Garten W., Klenk H. Caspase-dependent N-terminal cleavage of influenza virus nucleocapsid protein in infected cells. J. Virol. 1999, 73:10158-10163.
64. Zhou Z., Jiang X., Liu D., Fan Z., Hu X., Yan J., Wang M., Gao G.F. Autophagy is involved in influenza A virus replication. Autophagy 2009, 5:321-328.