TBK-1 Promotes Autophagy-Mediated Antimicrobial Defense by Controlling Autophagosome Maturation

Immunity

Volumn 37, Issue 2, 2012, Pages 223-234

  Pilli, Manohar ^a   Arko Mensah, John ^a   Ponpuak, Marisa ^a,b   Roberts, Esteban ^a   Master, Sharon ^a   Mandell, Michael A ^a   Dupont, Nicolas ^a   Ornatowski, Wojciech ^a   Jiang, Shanya ^a   Bradfute, Steven B ^a   Bruun, Jack Ansgar ^c   Hansen, Tom Egil ^c   Johansen, Terje ^c   Deretic, Vojo ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

^c UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR P62; ADAPTOR PROTEIN; INTERLEUKIN 1BETA; PHOSPHOTRANSFERASE; RAB PROTEIN; RAB8 PROTEIN; SERINE; TANK BINDING KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMICROBIAL ACTIVITY; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL MATURATION; CELL MIGRATION; CELL ORGANELLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INNATE IMMUNITY; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOPHAGY; GREEN FLUORESCENT PROTEINS; HEAT-SHOCK PROTEINS; HELA CELLS; HUMANS; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; MYCOBACTERIUM BOVIS; PHAGOSOMES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RAB GTP-BINDING PROTEINS; RNA, SMALL INTERFERING; SERINE; TUBERCULOSIS;

EID: 84865357562     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.04.015     Document Type: Article

References (50)

1. Alonso S., Pethe K., Russell D.G., Purdy G.E. Lysosomal killing of Mycobacterium mediated by ubiquitin-derived peptides is enhanced by autophagy. Proc. Natl. Acad. Sci. USA 2007, 104:6031-6036.
2. Bjørkøy G., Lamark T., Brech A., Outzen H., Perander M., Overvatn A., Stenmark H., Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 2005, 171:603-614.
3. Björkqvist M., Wild E.J., Thiele J., Silvestroni A., Andre R., Lahiri N., Raibon E., Lee R.V., Benn C.L., Soulet D., et al. A novel pathogenic pathway of immune activation detectable before clinical onset in Huntington's disease. J. Exp. Med. 2008, 205:1869-1877.
4. Clark K., Plater L., Peggie M., Cohen P. Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IkappaB kinase epsilon: a distinct upstream kinase mediates Ser-172 phosphorylation and activation. J. Biol. Chem. 2009, 284:14136-14146.
5. 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.
6. del Toro D., Alberch J., Lázaro-Diéguez F., Martín-Ibáñez R., Xifró X., Egea G., Canals J.M. Mutant huntingtin impairs post-Golgi trafficking to lysosomes by delocalizing optineurin/Rab8 complex from the Golgi apparatus. Mol. Biol. Cell 2009, 20:1478-1492.
7. Deretic V. Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors. Curr. Opin. Immunol. 2012, 24:21-31.
8. Deretic V. Autophagy: an emerging immunological paradigm. J. Immunol. 2012, 189:15-20.
9. Deretic V., Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 2009, 5:527-549.
10. Dupont N., Jiang S., Pilli M., Ornatowski W., Bhattacharya D., Deretic V. Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1β. EMBO J. 2011, 30:4701-4711.
11. Fremond C.M., Togbe D., Doz E., Rose S., Vasseur V., Maillet I., Jacobs M., Ryffel B., Quesniaux V.F. IL-1 receptor-mediated signal is an essential component of MyD88-dependent innate response to Mycobacterium tuberculosis infection. J. Immunol. 2007, 179:1178-1189.
12. Gutierrez M.G., Master S.S., Singh S.B., Taylor G.A., Colombo M.I., Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004, 119:753-766.
13. Hattula K., Peränen J. FIP-2, a coiled-coil protein, links Huntingtin to Rab8 and modulates cellular morphogenesis. Curr. Biol. 2000, 10:1603-1606.
14. Hirota Y., Tanaka Y. A small GTPase, human Rab32, is required for the formation of autophagic vacuoles under basal conditions. Cell Mol. Life Sci. 2009.
15. Hjerpe R., Aillet F., Lopitz-Otsoa F., Lang V., England P., Rodriguez M.S. Efficient protection and isolation of ubiquitylated proteins using tandem ubiquitin-binding entities. EMBO Rep. 2009, 10:1250-1258.
16. Itoh T., Kanno E., Uemura T., Waguri S., Fukuda M. OATL1, a novel autophagosome-resident Rab33B-GAP, regulates autophagosomal maturation. J. Cell Biol. 2011, 192:839-853.
17. Jäger S., Bucci C., Tanida I., Ueno T., Kominami E., Saftig P., Eskelinen E.L. Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 2004, 117:4837-4848.
18. Johansen T., Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011, 7:279-296.
19. Jounai N., Takeshita F., Kobiyama K., Sawano A., Miyawaki A., Xin K.Q., Ishii K.J., Kawai T., Akira S., Suzuki K., Okuda K. The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc. Natl. Acad. Sci. USA 2007, 104:14050-14055.
20. Kimura S., Noda T., Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007, 3:452-460.
21. Korolchuk V.I., Saiki S., Lichtenberg M., Siddiqi F.H., Roberts E.A., Imarisio S., Jahreiss L., Sarkar S., Futter M., Menzies F.M., et al. Lysosomal positioning coordinates cellular nutrient responses. Nat. Cell Biol. 2011, 13:453-460.
22. Lam K.K., Zheng X., Forestieri R., Balgi A.D., Nodwell M., Vollett S., Anderson H.J., Andersen R.J., Av-Gay Y., Roberge M. Nitazoxanide stimulates autophagy and inhibits mTORC1 signaling and intracellular proliferation of Mycobacterium tuberculosis. PLoS Pathog. 2012, 8:e1002691.
23. Lamark T., Perander M., Outzen H., Kristiansen K., Øvervatn A., Michaelsen E., Bjørkøy G., Johansen T. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J. Biol. Chem. 2003, 278:34568-34581.
24. Larsen K.B., Lamark T., Øvervatn A., Harneshaug I., Johansen T., Bjørkøy G. A reporter cell system to monitor autophagy based on p62/SQSTM1. Autophagy 2010, 6:784-793.
25. Levine B., Mizushima N., Virgin H.W. Autophagy in immunity and inflammation. Nature 2011, 469:323-335.
26. Liang C., Lee J.S., Inn K.S., Gack M.U., Li Q., Roberts E.A., Vergne I., Deretic V., Feng P., Akazawa C., Jung J.U. Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat. Cell Biol. 2008, 10:776-787.
27. Matsumoto G., Wada K., Okuno M., Kurosawa M., Nukina N. Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol. Cell 2011, 44:279-289.
28. Matsunaga K., Saitoh T., Tabata K., Omori H., Satoh T., Kurotori N., Maejima I., Shirahama-Noda K., Ichimura T., Isobe T., et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat. Cell Biol. 2009, 11:385-396.
29. Mayer-Barber K.D., Andrade B.B., Barber D.L., Hieny S., Feng C.G., Caspar P., Oland S., Gordon S., Sher A. Innate and adaptive interferons suppress IL-1α and IL-1β production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 2011, 35:1023-1034.
30. Mizushima N., Yoshimori T., Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 2011, 27:107-132.
31. Morton S., Hesson L., Peggie M., Cohen P. Enhanced binding of TBK1 by an optineurin mutant that causes a familial form of primary open angle glaucoma. FEBS Lett. 2008, 582:997-1002.
32. Nakagawa I., Amano A., Mizushima N., Yamamoto A., Yamaguchi H., Kamimoto T., Nara A., Funao J., Nakata M., Tsuda K., et al. Autophagy defends cells against invading group A Streptococcus. Science 2004, 306:1037-1040.
33. Nakahira K., Haspel J.A., Rathinam V.A., Lee S.J., Dolinay T., Lam H.C., Englert J.A., Rabinovitch M., Cernadas M., Kim H.P., et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 2011, 12:222-230.
34. Olkkonen V.M., Dupree P., Killisch I., Lütcke A., Zerial M., Simons K. Molecular cloning and subcellular localization of three GTP-binding proteins of the rab subfamily. J. Cell Sci. 1993, 106:1249-1261.
35. Ou Y.H., Torres M., Ram R., Formstecher E., Roland C., Cheng T., Brekken R., Wurz R., Tasker A., Polverino T., et al. TBK1 directly engages Akt/PKB survival signaling to support oncogenic transformation. Mol. Cell 2011, 41:458-470.
36. Pankiv S., Clausen T.H., Lamark T., Brech A., Bruun J.A., Outzen H., Øvervatn A., Bjørkøy G., Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 2007, 282:24131-24145.
37. Perkins N.D. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat. Rev. Mol. Cell Biol. 2007, 8:49-62.
38. Ponpuak M., Davis A.S., Roberts E.A., Delgado M.A., Dinkins C., Zhao Z., Virgin H.W., Kyei G.B., Johansen T., Vergne I., Deretic V. Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties. Immunity 2010, 32:329-341.
39. Radtke A.L., Delbridge L.M., Balachandran S., Barber G.N., O'Riordan M.X. TBK1 protects vacuolar integrity during intracellular bacterial infection. PLoS Pathog. 2007, 3:e29.
40. Ravikumar B., Imarisio S., Sarkar S., O'Kane C.J., Rubinsztein D.C. Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease. J. Cell Sci. 2008, 121:1649-1660.
41. Roberts E.A., Deretic V. Autophagic proteolysis of long-lived proteins in nonliver cells. Methods Mol. Biol. 2008, 445:111-117.
42. Saitoh T., Fujita N., Hayashi T., Takahara K., Satoh T., Lee H., Matsunaga K., Kageyama S., Omori H., Noda T., et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc. Natl. Acad. Sci. USA 2009, 106:20842-20846.
43. Sarkar S., Perlstein E.O., Imarisio S., Pineau S., Cordenier A., Maglathlin R.L., Webster J.A., Lewis T.A., O'Kane C.J., Schreiber S.L., Rubinsztein D.C. Small molecules enhance autophagy and reduce toxicity in Huntington's disease models. Nat. Chem. Biol. 2007, 3:331-338.
44. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68:850-858.
45. Söderberg O., Gullberg M., Jarvius M., Ridderstråle K., Leuchowius K.J., Jarvius J., Wester K., Hydbring P., Bahram F., Larsson L.G., Landegren U. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 2006, 3:995-1000.
46. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 2009, 10:513-525.
47. Thurston T.L., Ryzhakov G., Bloor S., von Muhlinen N., Randow F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 2009, 10:1215-1221.
48. Wild P., Farhan H., McEwan D.G., Wagner S., Rogov V.V., Brady N.R., Richter B., Korac J., Waidmann O., Choudhary C., et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011, 333:228-233.
49. Zhong Y., Wang Q.J., Li X., Yan Y., Backer J.M., Chait B.T., Heintz N., Yue Z. Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat. Cell Biol. 2009, 11:468-476.
50. Zhou R., Yazdi A.S., Menu P., Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225.