Cytoplasmic STAT3 Represses Autophagy by Inhibiting PKR Activity

Molecular Cell

Volumn 48, Issue 5, 2012, Pages 667-680

  Shen, Shensi ^a,b,c   Niso Santano, Mireia ^a,b,c   Adjemian, Sandy ^a,b,c   Takehara, Tetsuo ^e   Malik, Shoaib Ahmad ^a,b,c   Minoux, Hervé ^f   Souquere, Sylvie ^b,d   Mariño, Guillermo ^a,b,c   Lachkar, Sylvie ^a,b,c   Senovilla, Laura ^a,b,c   Galluzzi, Lorenzo ^b,g   Kepp, Oliver ^a,b,c   Pierron, Gérard ^b,d   Maiuri, Maria Chiara ^a,b,c   Hikita, Hayato ^e   Kroemer, Romano ^f   Kroemer, Guido ^a,b,g,h,i  

^a Institut Gustave Roussy   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d CNRS   (France)

^e OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f SANOFI   (France)

^g UNIVERSITÉ PARIS DESCARTES   (France)

^h CENTRE DE RECHERCHE DES CORDELIERS   (France)

ⁱ HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

Author keywords

[No Author keywords available]

Indexed keywords

JSI 124; PALMITIC ACID; PROTEIN INHIBITOR; PROTEIN KINASE R; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

ANIMALS; AUTOPHAGY; CATALYTIC DOMAIN; CELL LINE, TUMOR; CYTOPLASM; EIF-2 KINASE; ENZYME ACTIVATION; EUKARYOTIC INITIATION FACTOR-2; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR DOCKING SIMULATION; PALMITIC ACID; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; STAT3 TRANSCRIPTION FACTOR; TIME FACTORS; TRANSFECTION;

EID: 84870901484     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.09.013     Document Type: Article

References (54)

1. Behrends C., Sowa M.E., Gygi S.P., Harper J.W. Network organization of the human autophagy system. Nature 2010, 466:68-76.
2. Blaskovich M.A., Sun J., Cantor A., Turkson J., Jove R., Sebti S.M. Discovery of JSI-124 (cucurbitacin I), a selective Janus kinase/signal transducer and activator of transcription 3 signaling pathway inhibitor with potent antitumor activity against human and murine cancer cells in mice. Cancer Res. 2003, 63:1270-1279.
3. Boengler K., Hilfiker-Kleiner D., Heusch G., Schulz R. Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res. Cardiol. 2010, 105:771-785.
4. Breitkreutz B.J., Stark C., Reguly T., Boucher L., Breitkreutz A., Livstone M., Oughtred R., Lackner D.H., Bähler J., Wood V., et al. The BioGRID Interaction Database: 2008 update. Nucleic Acids Res. 2008, 36(Database Issue):D637-D640.
5. Bromberg J.F., Wrzeszczynska M.H., Devgan G., Zhao Y., Pestell R.G., Albanese C., Darnell J.E. Stat3 as an oncogene. Cell 1999, 98:295-303.
6. Cadwell K., Liu J.Y., Brown S.L., Miyoshi H., Loh J., Lennerz J.K., Kishi C., Kc W., Carrero J.A., Hunt S., et al. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 2008, 456:259-263.
7. Cénit M.C., Alcina A., Márquez A., Mendoza J.L., Díaz-Rubio M., de las Heras V., Izquierdo G., Arroyo R., Fernández O., de la Concha E.G., et al. STAT3 locus in inflammatory bowel disease and multiple sclerosis susceptibility. Genes Immun. 2010, 11:264-268.
8. Comb W.C., Hutti J.E., Cogswell P., Cantley L.C., Baldwin A.S. p85α SH2 domain phosphorylation by IKK promotes feedback inhibition of PI3K and Akt in response to cellular starvation. Mol. Cell 2012, 45:719-730.
9. Comeau S.R., Gatchell D.W., Vajda S., Camacho C.J. ClusPro: a fully automated algorithm for protein-protein docking. Nucleic Acids Res. 2004, 32(Web Server Issue):W96-W99.
10. Cooney R., Baker J., Brain O., Danis B., Pichulik T., Allan P., Ferguson D.J., Campbell B.J., Jewell D., Simmons A. NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat. Med. 2010, 16:90-97.
11. Criollo A., Senovilla L., Authier H., Maiuri M.C., Morselli E., Vitale I., Kepp O., Tasdemir E., Galluzzi L., Shen S., et al. The IKK complex contributes to the induction of autophagy. EMBO J. 2010, 29:619-631.
12. Criollo A., Niso-Santano M., Malik S.A., Michaud M., Morselli E., Mariño G., Lachkar S., Arkhipenko A.V., Harper F., Pierron G., et al. Inhibition of autophagy by TAB2 and TAB3. EMBO J. 2011, 30:4908-4920.
13. Criollo A., Chereau F., Malik S.A., Niso-Santano M., Mariño G., Galluzzi L., Maiuri M.C., Baud V., Kroemer G. Autophagy is required for the activation of NFκB. Cell Cycle 2012, 11:194-199.
14. Danoy P., Pryce K., Hadler J., Bradbury L.A., Farrar C., Pointon J., Ward M., Weisman M., Reveille J.D., Wordsworth B.P., et al. Association of variants at 1q32 and STAT3 with ankylosing spondylitis suggests genetic overlap with Crohn's disease. PLoS Genet. 2010, 6:e1001195. Australo-Anglo-American Spondyloarthritis Consortium, Spondyloarthritis Research Consortium of CanadaSpondyloarthritis Research Consortium of Canada. 10.1371/journal.pgen.1001195.
15. Dar A.C., Dever T.E., Sicheri F. Higher-order substrate recognition of eIF2alpha by the RNA-dependent protein kinase PKR. Cell 2005, 122:887-900.
16. Gough D.J., Corlett A., Schlessinger K., Wegrzyn J., Larner A.C., Levy D.E. Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 2009, 324:1713-1716.
17. Green D.R., Galluzzi L., Kroemer G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 2011, 333:1109-1112.
18. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., Sadri N., Yun C., Popko B., Paules R., et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 2003, 11:619-633.
19. He C., Klionsky D.J. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 2009, 43:67-93.
20. Holland S.M., DeLeo F.R., Elloumi H.Z., Hsu A.P., Uzel G., Brodsky N., Freeman A.F., Demidowich A., Davis J., Turner M.L., et al. STAT3 mutations in the hyper-IgE syndrome. N. Engl. J. Med. 2007, 357:1608-1619.
21. Iwamaru A., Szymanski S., Iwado E., Aoki H., Yokoyama T., Fokt I., Hess K., Conrad C., Madden T., Sawaya R., et al. A novel inhibitor of the STAT3 pathway induces apoptosis in malignant glioma cells both in vitro and in vivo. Oncogene 2007, 26:2435-2444.
22. Kroemer G., Mariño G., Levine B. Autophagy and the integrated stress response. Mol. Cell 2010, 40:280-293.
23. Levine B., Mizushima N., Virgin H.W. Autophagy in immunity and inflammation. Nature 2011, 469:323-335.
24. Levy D.E., Darnell J.E. Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell Biol. 2002, 3:651-662.
25. Liu L., McBride K.M., Reich N.C. STAT3 nuclear import is independent of tyrosine phosphorylation and mediated by importin-alpha3. Proc. Natl. Acad. Sci. USA 2005, 102:8150-8155.
26. Livesey K.M., Kang R., Vernon P., Buchser W., Loughran P., Watkins S.C., Zhang L., Manfredi J.J., Zeh H.J., Li L., et al. p53/HMGB1 complexes regulate autophagy and apoptosis. Cancer Res. 2012, 72:1996-2005.
27. Ma J., Meng Y., Kwiatkowski D.J., Chen X., Peng H., Sun Q., Zha X., Wang F., Wang Y., Jing Y., et al. Mammalian target of rapamycin regulates murine and human cell differentiation through STAT3/p63/Jagged/Notch cascade. J. Clin. Invest. 2010, 120:103-114.
28. Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell 2010, 140:313-326.
29. Morselli E., Maiuri M.C., Markaki M., Megalou E., Pasparaki A., Palikaras K., Criollo A., Galluzzi L., Malik S.A., Vitale I., et al. Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis. 2010, 1:e10.
30. Morselli E., Galluzzi L., Kepp O., Mariño G., Michaud M., Vitale I., Maiuri M.C., Kroemer G. Oncosuppressive functions of autophagy. Antioxid. Redox Signal. 2011, 14:2251-2269.
31. Morselli E., Shen S., Ruckenstuhl C., Bauer M.A., Mariño G., Galluzzi L., Criollo A., Michaud M., Maiuri M.C., Chano T., et al. p53 inhibits autophagy by interacting with the human ortholog of yeast Atg17, RB1CC1/FIP200. Cell Cycle 2011, 10:2763-2769.
32. Nakamura T., Furuhashi M., Li P., Cao H., Tuncman G., Sonenberg N., Gorgun C.Z., Hotamisligil G.S. Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell 2010, 140:338-348.
33. Nie Y., Erion D.M., Yuan Z., Dietrich M., Shulman G.I., Horvath T.L., Gao Q. STAT3 inhibition of gluconeogenesis is downregulated by SirT1. Nat. Cell Biol. 2009, 11:492-500.
34. Orvedahl A., Alexander D., Tallóczy Z., Sun Q., Wei Y., Zhang W., Burns D., Leib D.A., Levine B. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 2007, 1:23-35.
35. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939.
36. Pilati C., Amessou M., Bihl M.P., Balabaud C., Nhieu J.T., Paradis V., Nault J.C., Izard T., Bioulac-Sage P., Couchy G., et al. Somatic mutations activating STAT3 in human inflammatory hepatocellular adenomas. J. Exp. Med. 2011, 208:1359-1366.
37. Qing G., Yan P., Xiao G. Hsp90 inhibition results in autophagy-mediated proteasome-independent degradation of IkappaB kinase (IKK). Cell Res. 2006, 16:895-901.
38. Ren Z., Mao X., Mertens C., Krishnaraj R., Qin J., Mandal P.K., Romanowski M.J., McMurray J.S., Chen X. Crystal structure of unphosphorylated STAT3 core fragment. Biochem. Biophys. Res. Commun. 2008, 374:1-5.
39. Rubinsztein D.C., Mariño G., Kroemer G. Autophagy and aging. Cell 2011, 146:682-695.
40. Sarbassov D.D., Ali S.M., Sabatini D.M. Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 2005, 17:596-603.
41. Schust J., Sperl B., Hollis A., Mayer T.U., Berg T. Stattic: a small-molecule inhibitor of STAT3 activation and dimerization. Chem. Biol. 2006, 13:1235-1242.
42. Shen S., Kepp O., Michaud M., Martins I., Minoux H., Métivier D., Maiuri M.C., Kroemer R.T., Kroemer G. Association and dissociation of autophagy, apoptosis and necrosis by systematic chemical study. Oncogene 2011, 30:4544-4556.
43. Tallóczy Z., Jiang W., Virgin H.W., Leib D.A., Scheuner D., Kaufman R.J., Eskelinen E.L., Levine B. Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl. Acad. Sci. USA 2002, 99:190-195.
44. Tallóczy Z., Virgin H.W., Levine B. PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy 2006, 2:24-29.
45. Tasdemir E., Maiuri M.C., Galluzzi L., Vitale I., Djavaheri-Mergny M., D'Amelio M., Criollo A., Morselli E., Zhu C., Harper F., et al. Regulation of autophagy by cytoplasmic p53. Nat. Cell Biol. 2008, 10:676-687.
46. Taylor S.S., Haste N.M., Ghosh G. PKR and eIF2alpha: integration of kinase dimerization, activation, and substrate docking. Cell 2005, 122:823-825.
47. Tourrière H., Chebli K., Zekri L., Courselaud B., Blanchard J.M., Bertrand E., Tazi J. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 2003, 160:823-831.
48. Traver M.K., Henry S.C., Cantillana V., Oliver T., Hunn J.P., Howard J.C., Beer S., Pfeffer K., Coers J., Taylor G.A. Immunity-related GTPase M (IRGM) proteins influence the localization of guanylate-binding protein 2 (GBP2) by modulating macroautophagy. J. Biol. Chem. 2011, 286:30471-30480.
49. Van Grol J., Subauste C., Andrade R.M., Fujinaga K., Nelson J., Subauste C.S. HIV-1 inhibits autophagy in bystander macrophage/monocytic cells through Src-Akt and STAT3. PLoS ONE 2010, 5:e11733. 10.1371/journal.pone.0011733.
50. Wegrzyn J., Potla R., Chwae Y.J., Sepuri N.B., Zhang Q., Koeck T., Derecka M., Szczepanek K., Szelag M., Gornicka A., et al. Function of mitochondrial Stat3 in cellular respiration. Science 2009, 323:793-797.
51. Weidberg H., Shvets E., Elazar Z. Biogenesis and cargo selectivity of autophagosomes. Annu. Rev. Biochem. 2011, 80:125-156.
52. Yang J., Chatterjee-Kishore M., Staugaitis S.M., Nguyen H., Schlessinger K., Levy D.E., Stark G.R. Novel roles of unphosphorylated STAT3 in oncogenesis and transcriptional regulation. Cancer Res. 2005, 65:939-947.
53. Yu H., Pardoll D., Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 2009, 9:798-809.
54. Yuan Z.L., Guan Y.J., Chatterjee D., Chin Y.E. Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 2005, 307:269-273.