Secretory versus degradative autophagy: Unconventional secretion of inflammatory mediators

Journal of Innate Immunity

Volumn 5, Issue 5, 2013, Pages 471-479

  Jiang, Shanya ^a   Dupont, Nicolas ^a   Castillo, Eliseo F ^a   Deretic, Vojo ^a  

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

Author keywords

Alarmins; Autophagy; Calpain; Inflammasome

Indexed keywords

CASEIN KINASE II; COAT PROTEIN COMPLEX II; CYCLIN DEPENDENT KINASE 1; ESCRT PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; OPTINEURIN; PATTERN RECOGNITION RECEPTOR; POLO LIKE KINASE 1; REACTIVE OXYGEN METABOLITE; ACB1 PROTEIN; DGRASP PROTEIN; GRASP55 PROTEIN; GRASP65 PROTEIN; GRH1 PROTEIN; GRPA PROTEIN; PHOSPHATIDYLETHANOLAMINE; PROTEIN; PROTEIN KINASE; TBK 1 ENZYME; THYMOCYTE ANTIBODY; UNCLASSIFIED DRUG; AUTACOID; INTERLEUKIN 1;

AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CELL DEATH; CELL MEMBRANE; CYTOKINE RELEASE; CYTOSOL; DICTYOSTELIUM; DROSOPHILA; EUKARYOTIC CELL; EXOCYTOSIS; GOLGI COMPLEX; HUMAN; INNATE IMMUNITY; MACROPHAGE; MAMMAL CELL; MEMBRANE STRUCTURE; MITOCHONDRION; MITOSIS; NONHUMAN; OLIGOMERIZATION; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; QUALITY CONTROL; REVIEW; SECRETORY PATHWAY; STEADY STATE; CARBOXY TERMINAL SEQUENCE; CELL ORGANELLE; CONTROLLED STUDY; DEGRADATIVE AUTOPHAGY; SECRETORY AUTOPHAGY; YEAST; ANIMAL; CELL COMMUNICATION; COMPARATIVE STUDY; MAMMAL; METABOLISM; PHYSIOLOGY; PROTEIN DEGRADATION;

ANIMALS; AUTOPHAGY; CELL COMMUNICATION; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1; MAMMALS; PROTEOLYSIS; SECRETORY PATHWAY;

EID: 84880918899     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000346707     Document Type: Review

References (58)

1. Manjithaya R, Anjard C, Loomis WF, Subramani S: Unconventional secretion of Pichia pastoris Acb1 is dependent on GRASP protein, peroxisomal functions, and autophagosome formation. J Cell Biol 2010; 188: 537-546.
2. Bruns C, McCaffery JM, Curwin AJ, Duran JM, Malhotra V: Biogenesis of a novel compartment for autophagosome-mediated unconventional protein secretion. J Cell Biol 2011; 195: 979-992.
3. Duran JM, Anjard C, Stefan C, Loomis WF, Malhotra V: Unconventional secretion of Acb1 is mediated by autophagosomes. J Cell Biol 2010; 188: 527-536.
4. Dupont N, Jiang S, Pilli M, Ornatowski W, Bhattacharya D, Deretic V: Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1beta. EMBO J 2011; 30: 4701-4711.
5. Deretic V, Jiang S, Dupont N: Autophagy intersections with conventional and unconventional secretion in tissue development, remodeling and inflammation. Trends Cell Biol 2012; 22: 397-406.
6. Rabouille C, Malhotra V, Nickel W: Diversity of unconventional protein secretion. J Cell Sci 2012, in press.
7. Shorter J, Watson R, Giannakou ME, Clarke M, Warren G, Barr FA: GRASP55, a second mammalian GRASP protein involved in the stacking of Golgi cisternae in a cell-free system. EMBO J 1999; 18: 4949-4960. (Pubitemid 29443797)
8. Cabral M, Anjard C, Malhotra V, Loomis WF, Kuspa A: Unconventional secretion of AcbA in Dictyostelium discoideum through a vesicular intermediate. Eukaryot Cell 2010; 9: 1009-1017.
9. Kinseth MA, Anjard C, Fuller D, Guizzunti G, Loomis WF, Malhotra V: The Golgi-associated protein GRASP is required for unconventional protein secretion during development. Cell 2007; 130: 524-534. (Pubitemid 47198303)
10. Nickel W, Rabouille C: Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 2009; 10: 148-155.
11. Giuliani F, Grieve A, Rabouille C: Unconventional secretion: a stress on GRASP. Curr Opin Cell Biol 2011; 23: 498-504.
12. Mizushima N, Yoshimori T, Ohsumi Y: The role of Atg proteins in autophagosome formation. Ann Rev Cell Dev Biol 2011; 27: 107-132.
13. Rubinsztein DC, Codogno P, Levine B: Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 2012; 11: 709-730.
14. Mizushima N, Komatsu M: Autophagy: renovation of cells and tissues. Cell 2011; 147: 728-741.
15. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, Asara JM, Fitzpatrick J, Dillin A, Viollet B, Kundu M, Hansen M, Shaw RJ: Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 2011; 331: 456-461.
16. Criollo A, Niso-Santano M, Malik SA, Michaud M, Morselli E, Marino G, Lachkar S, Arkhipenko AV, Harper F, Pierron G, Rain JC, Ninomiya-Tsuji J, Fuentes JM, Lavandero S, Galluzzi L, Maiuri MC, Kroemer G: Inhibition of autophagy by TAB2 and TAB3. EMBO J 2011; 30: 4908-4920.
17. Nakatogawa H, Ichimura Y, Ohsumi Y: Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 2007; 130: 165-178. (Pubitemid 47031316)
18. Weidberg H, Shpilka T, Shvets E, Abada A, Shimron F, Elazar Z: LC3 and GATE-16 Ntermini mediate membrane fusion processes required for autophagosome biogenesis. Dev Cell 2011; 20: 444-454.
19. Nair U, Jotwani A, Geng J, Gammoh N, Richerson D, Yen WL, Griffith J, Nag S, Wang K, Moss T, Baba M, McNew JA, Jiang X, Reggiori F, Melia TJ, Klionsky DJ: SNARE proteins are required for macroautophagy. Cell 2011; 146: 290-302.
20. Narita M, Young AR, Arakawa S, Samarajiwa SA, Nakashima T, Yoshida S, Hong S, Berry LS, Reichelt S, Ferreira M, Tavare S, Inoki K, Shimizu S: Spatial coupling of mTOR and autophagy augments secretory phenotypes. Science 2011; 332: 966-970.
21. DeSelm CJ, Miller BC, Zou W, Beatty WL, van Meel E, Takahata Y, Klumperman J, Tooze SA, Teitelbaum SL, Virgin HW: Autophagy proteins regulate the secretory component of osteoclastic bone resorption. Dev Cell 2011; 21: 966-974.
22. Gee HY, Noh SH, Tang BL, Kim KH, Lee MG: Rescue of deltaF508-CFTR trafficking via a GRASP-dependent unconventional secretion pathway. Cell 2011; 146: 746-760.
23. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT: Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 2008; 182: 685-701.
24. Ishihara N, Hamasaki M, Yokota S, Suzuki K, Kamada Y, Kihara A, Yoshimori T, Noda T, Ohsumi Y: Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell 2001; 12: 3690-3702. (Pubitemid 33108497)
25. Zoppino FC, Militello RD, Slavin I, Alvarez C, Colombo MI: Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic 2010; 11: 1246-1261.
26. Winslow AR, Chen CW, Corrochano S, Acevedo-Arozena A, Gordon DE, Peden AA, Lichtenberg M, Menzies FM, Ravikumar B, Imarisio S, Brown S, O'Kane CJ, Rubinsztein DC: ?-Synuclein impairs macroautophagy: implications for Parkinson's disease. J Cell Biol 2010; 190: 1023-1037.
27. Deretic V: Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors. Curr Opin Immunol 2012; 24: 21-31.
28. Schotman H, Karhinen L, Rabouille C: dGRASP-mediated noncanonical integrin secretion is required for Drosophila epithelial remodeling. Dev Cell 2008; 14: 171-182. (Pubitemid 351189181)
29. Barr FA: Purification and functional interactions of GRASP55 with Rab2. Methods Enzymol 2005; 403: 391-401. (Pubitemid 43216925)
30. Truschel ST, Zhang M, Bachert C, Macbeth MR, Linstedt AD: Allosteric regulation of GRASP protein-dependent Golgi membrane tethering by mitotic phosphorylation. J Biol Chem 2012; 287: 19870-19875.
31. Jarvela T, Linstedt A: Golgi GRASPs: moonlighting membrane tethers. Cell Health Cytoskeleton 2012; 4: 37-47.
32. Pilli M, Arko-Mensah J, Ponpuak M, Roberts E, Master S, Mandell MA, Dupont N, Ornatowski W, Jiang S, Bradfute SB, Bruun JA, Hansen TE, Johansen T, Deretic V: TBK-1 promotes autophagy-mediated antimicrobial defense by controlling autophagosome maturation. Immunity 2012; 37: 223-234.
33. Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR, Richter B, Korac J, Waidmann O, Choudhary C, Dotsch V, Bumann D, Dikic I: Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011; 333: 228-233.
34. Bjorkoy 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. (Pubitemid 41668720)
35. 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.
36. Perkins ND: Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Molecular Cell Biol 2007; 8: 49-62. (Pubitemid 46012014)
37. Pfeffer SR: Unconventional secretion by autophagosome exocytosis. J Cell Biol 2010; 188: 451-452.
38. Saitoh T, Fujita N, Jang MH, Uematsu S, Yang BG, Satoh T, Omori H, Noda T, Yamamoto N, Komatsu M, Tanaka K, Kawai T, Tsujimura T, Takeuchi O, Yoshimori T, Akira S: Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 2008; 456: 264-268.
39. Zhou R, Yazdi AS, Menu P, Tschopp J: A role for mitochondria in NLRP3 inflammasome activation. Nature 2011; 469: 221-225.
40. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, Choi AM: Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12: 222-230.
41. Harris J, Hartman M, Roche C, Zeng SG, O'Shea A, Sharp FA, Lambe EM, Creagh EM, Golenbock DT, Tschopp J, Kornfeld H, Fitzgerald KA, Lavelle EC: Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J Biol Chem 2011; 286: 9587-9597.
42. Shi CS, Shenderov K, Huang NN, Kabat J, Abu-Asab M, Fitzgerald KA, Sher A, Kehrl JA: Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat Immunol 2012; 13: 255-263.
43. Rubartelli A, Cozzolino F, Talio M, Sitia R: A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J 1990; 9: 1503-1510.
44. Qu Y, Franchi L, Nunez G, Dubyak GR: Nonclassical IL-1 beta secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J Immunol 2007; 179: 1913-1925.
45. Dinarello CA: An IL-1 family member requires caspase-1 processing and signals through the ST2 receptor. Immunity 2005; 23: 461-462. (Pubitemid 41587885)
46. Rathinam VA, Vanaja SK, Fitzgerald KA: Regulation of inflammasome signaling. Nat Immunol 2012; 13: 333-332.
47. Peral de Castro C, Jones SA, Ni Cheallaigh C, Hearnden CA, Williams L, Winter J, Lavelle EC, Mills KH, Harris J: Autophagy regulates IL-23 secretion and innate T cell responses through effects on IL-1 secretion. J Immunol 2012; 189: 4144-4153.
48. Afonina IS, Tynan GA, Logue SE, Cullen SP, Bots M, Luthi AU, Reeves EP, McElvaney NG, Medema JP, Lavelle EC, Martin SJ: Granzyme B-dependent proteolysis acts as a switch to enhance the proinflammatory activity of IL-1alpha. Mol Cell 2011; 44: 265-278.
49. Yazdi AS, Guarda G, Riteau N, Drexler SK, Tardivel A, Couillin I, Tschopp J: Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1alpha and IL-1beta. Proc Natl Acad Sci USA 2010; 107: 19449-19454.
50. Castillo E, Dekonenko A, Arko-Mensah J, Mandell M, Dupont N, Jiang S, Delgado-Vargas M, Timmins G, Bhattacharya D, Yang H, Hutt J, Lyson C, Dobos K, Deretic V: Autophagy protects against active tuberculosis by suppressing bacterial burden and inflammation. Proc Natl Acad USA 2012, in press.
51. Chen CJ, Kono H, Golenbock D, Reed G, Akira S, Rock KL: Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat Med 2007; 13: 851-856. (Pubitemid 47038190)
52. Gross O, Yazdi AS, Thomas CJ, Masin M, Heinz LX, Guarda G, Quadroni M, Drexler SK, Tschopp J: Inflammasome activators induce interleukin-1alpha secretion via distinct pathways with differential requirement for the protease function of caspase-1. Immunity 2012; 36: 388-400.
53. Schott WH, Haskell BD, Tse HM, Milton MJ, Piganelli JD, Choisy-Rossi CM, Reifsnyder PC, Chervonsky AV, Leiter EH: Caspase-1 is not required for type 1 diabetes in the NOD mouse. Diabetes 2004; 53: 99-104. (Pubitemid 38044703)
54. Li Y, Arnold JM, Pampillo M, Babwah AV, Peng T: Taurine prevents cardiomyocyte death by inhibiting NADPH oxidase-mediated calpain activation. Free Radic Biol Med 2009; 46: 51-61.
55. Sharma AK, Rohrer B: Sustained elevation of intracellular cGMP causes oxidative stress triggering calpain-mediated apoptosis in photoreceptor degeneration. Curr Eye Res 2007; 32: 259-269. (Pubitemid 46439684)
56. Tal MC, Sasai M, Lee HK, Yordy B, Shadel GS, Iwasaki A: Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc Natl Acad Sci USA 2009; 106: 2770-2775.
57. Cadwell K, Liu JY, Brown SL, Miyoshi H, Loh J, Lennerz JK, Kishi C, Kc W, Carrero JA, Hunt S, Stone CD, Brunt EM, Xavier RJ, Sleckman BP, Li E, Mizushima N, Stappenbeck TS, Virgin HWT: A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 2008; 456: 259-263.
58. Cadwell K, Patel KK, Maloney NS, Liu TC, Ng AC, Storer CE, Head RD, Xavier R, Stappenbeck TS, Virgin HW: Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 2010; 141: 1135-1145.