Insulin-degrading enzyme secretion from astrocytes is mediated by an autophagy-based unconventional secretory pathway in Alzheimer disease

Autophagy

Volumn 12, Issue 5, 2016, Pages 784-800

  Son, Sung Min ^a   Cha, Moon Yong ^a   Choi, Heesun ^a   Kang, Seokjo ^a   Choi, Hyunjung ^a   Lee, Myung Shik ^b   Park, Sun Ah ^c   Mook Jung, Inhee ^a  

^a Seoul National University College of Medicine   (South Korea)

^b Sungkyunkwan University School of Medicine   (South Korea)

^c Soonchunhyang University   (South Korea)

Author keywords

Alzheimer disease; amyloid beta; autophagy; autophagy based unconventional secretion; insulin degrading enzyme

Indexed keywords

AMYLOID BETA PROTEIN; INSULINASE; PROTEASOME; INSULIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOPHAGY; BRAIN; CEREBROSPINAL FLUID; ENZYME ACTIVITY; ENZYME RELEASE; LYSOSOME; MOUSE; NONHUMAN; SECRETORY PATHWAY; ANIMAL; DISEASE MODEL; EXTRACELLULAR SPACE; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS);

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ASTROCYTES; AUTOPHAGY; BRAIN; DISEASE MODELS, ANIMAL; EXTRACELLULAR SPACE; HUMANS; INSULIN; MICE; SECRETORY PATHWAY;

EID: 84963623101     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2016.1159375     Document Type: Article

References (64)

1. D.M.Walsh, D.J.Selkoe. Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 2004; 44:181-93; PMID:15450169; http://dx.doi.org/10.1016/j.neuron.2004.09.010
2. D.J.Selkoe. Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat Cell Biol 2004; 6:1054-61; PMID:15516999; http://dx.doi.org/10.1038/ncb1104-1054
3. K.Vekrellis, Z.Ye, W.Q.Qiu, D.Walsh, D.Hartley, V.Chesneau, M.R.Rosner, D.J.Selkoe. Neurons regulate extracellular levels of amyloid beta-protein via proteolysis by insulin-degrading enzyme. J Neurosci 2000; 20:1657-65; PMID:10684867
4. V.B.Dorfman, L.Pasquini, M.Riudavets, J.J.Lopez-Costa, A.Villegas, J.C.Troncoso, F.Lopera, E.M.Castaño, L.Morelli. Differential cerebral deposition of IDE and NEP in sporadic and familial Alzheimer's disease. Neurobiol Aging 2010; 31:1743-57; PMID:19019493; http://dx.doi.org/10.1016/j.neurobiolaging.2008.09.016
5. W.C.Duckworth, R.G.Bennett, F.G.Hamel. Insulin degradation: progress and potential. Endocr Rev 1998; 19:608-24; PMID:9793760
6. W.Q.Qiu, Z.Ye, D.Kholodenko, P.Seubert, D.J.Selkoe. Degradation of amyloid beta-protein by a metalloprotease secreted by microglia and other neural and non-neural cells. J Biol Chem 1997; 272:6641-6; PMID:9045694; http://dx.doi.org/10.1074/jbc.272.10.6641
7. N.Mizushima, B.Levine, A.M.Cuervo, D.J.Klionsky. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538; http://dx.doi.org/10.1038/nature06639
8. N.Mizushima, B.Levine. Autophagy in mammalian development and differentiation. Nat Cell Biol 2010; 12:823-30; PMID:20811354; http://dx.doi.org/10.1038/ncb0910-823
9. V.Deretic, B.Levine. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 2009; 5:527-49; PMID:19527881; http://dx.doi.org/10.1016/j.chom.2009.05.016
10. D.J.Klionsky. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007; 8:931-7; PMID:17712358; http://dx.doi.org/10.1038/nrm2245
11. S.Subramani, V.Malhotra. Non-autophagic roles of autophagy-related proteins. EMBO Rep 2013; 14:143-51; PMID:23337627; http://dx.doi.org/10.1038/embor.2012.220
12. V.Deretic, S.Jiang, N.Dupont. Autophagy intersections with conventional and unconventional secretion in tissue development, remodeling and inflammation. Trends Cell Biol 2012; 22:397-406; PMID:22677446; http://dx.doi.org/10.1016/j.tcb.2012.04.008
13. N.Dupont, S.Jiang, M.Pilli, W.Ornatowski, D.Bhattacharya, V.Deretic. Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1beta. Embo J 2011; 30:4701-11; PMID:22068051; http://dx.doi.org/10.1038/emboj.2011.398
14. T.Torisu, K.Torisu, I.H.Lee, J.Liu, D.Malide, C.A.Combs, X.S.Wu, I.I.Rovira, M.M.Fergusson, R.Weigert, et al. Autophagy regulates endothelial cell processing, maturation and secretion of von Willebrand factor. Nat Med 2013; 19:1281-7; PMID:24056772; http://dx.doi.org/10.1038/nm.3288
15. I.Martins, Y.Wang, M.Michaud, Y.Ma, A.Q.Sukkurwala, S.Shen, O.Kepp, D.Métivier, L.Galluzzi, J.L.Perfettini, et al. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ 2014; 21:79-91; PMID:23852373; http://dx.doi.org/10.1038/cdd.2013.75
16. S.Jiang, N.Dupont, E.F.Castillo, V.Deretic. Secretory versus degradative autophagy: unconventional secretion of inflammatory mediators. J Innate Immun 2013; 5:471-9; PMID:23445716; http://dx.doi.org/10.1159/000346707
17. S.M.Son, E.S.Jung, H.J.Shin, J.Byun, I.Mook-Jung. Abeta-induced formation of autophagosomes is mediated by RAGE-CaMKKbeta-AMPK signaling. Neurobiol Aging 2012; 33:1006 e11-23; http://dx.doi.org/10.1016/j.neurobiolaging.2011.09.039
18. D.S.Yang, P.Stavrides, P.S.Mohan, S.Kaushik, A.Kumar, M.Ohno, S.D.Schmidt, D.Wesson, U.Bandyopadhyay, Y.Jiang, et al. Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 2011; 134:258-77; PMID:21186265; http://dx.doi.org/10.1093/brain/awq341
19. B.Boland, A.Kumar, S.Lee, F.M.Platt, J.Wegiel, W.H.Yu, R.A.Nixon. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J Neurosci 2008; 28:6926-37; PMID:18596167; http://dx.doi.org/10.1523/JNEUROSCI.0800-08.2008
20. H.Oakley, S.L.Cole, S.Logan, E.Maus, P.Shao, J.Craft, A.Guillozet-Bongaarts, M.Ohno, J.Disterhoft, L.Van Eldik, et al. Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J Neurosci 2006; 26:10129-40; PMID:17021169; http://dx.doi.org/10.1523/JNEUROSCI.1202-06.2006
21. S.M.Son, J.Byun, S.E.Roh, S.J.Kim, I.Mook-Jung. Reduced IRE1alpha mediates apoptotic cell death by disrupting calcium homeostasis via the InsP3 receptor. Cell Death Dis 2014; 5:e1188; PMID:24743743; http://dx.doi.org/10.1038/cddis.2014.129
22. P.Nilsson, K.Loganathan, M.Sekiguchi, Y.Matsuba, K.Hui, S.Tsubuki, M.Tanaka, N.Iwata, T.Saito, T.C.Saido. Abeta secretion and plaque formation depend on autophagy. Cell reports 2013; 5:61-9; PMID:24095740; http://dx.doi.org/10.1016/j.celrep.2013.08.042
23. J.Zhou, S.H.Tan, V.Nicolas, C.Bauvy, N.D.Yang, J.Zhang, Y.Xue, P.Codogno, H.M.Shen. Activation of lysosomal function in the course of autophagy via mTORC1 suppression and autophagosome-lysosome fusion. Cell Res 2013; 23:508-23; PMID:23337583; http://dx.doi.org/10.1038/cr.2013.11
24. J.H.Lee, W.H.Yu, A.Kumar, S.Lee, P.S.Mohan, C.M.Peterhoff, D.M.Wolfe, M.Martinez-Vicente, A.C.Massey, G.Sovak, et al. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 2010; 141:1146-58; PMID:20541250; http://dx.doi.org/10.1016/j.cell.2010.05.008
25. K.Glebov, S.Schutze, J.Walter. Functional relevance of a novel SlyX motif in non-conventional secretion of insulin-degrading enzyme. J Biol Chem 2011; 286:22711-5; PMID:21576244; http://dx.doi.org/10.1074/jbc.C110.217893
26. M.Zerial, H.McBride. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001; 2:107-17; PMID:11252952; http://dx.doi.org/10.1038/35052055
27. J.J.Bravo-Cordero, R.Marrero-Diaz, D.Megias, L.Genis, A.Garcia-Grande, M.A.Garcia, A.G.Arroyo, M.C.Montoya. MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. Embo J 2007; 26:1499-510; PMID:17332756; http://dx.doi.org/10.1038/sj.emboj.7601606
28. G.P.Hooff, W.G.Wood, W.E.Muller, G.P.Eckert. Isoprenoids, small GTPases and Alzheimer's disease. Biochimica et biophysica acta 2010; 1801:896-905; PMID:20382260; http://dx.doi.org/10.1016/j.bbalip.2010.03.014
29. A.Mohamed, L.Saavedra, A.Di Pardo, S.Sipione, E.Posse de Chaves. beta-amyloid inhibits protein prenylation and induces cholesterol sequestration by impairing SREBP-2 cleavage. J Neurosci 2012; 32:6490-500; PMID:22573671; http://dx.doi.org/10.1523/JNEUROSCI.0630-12.2012
30. J.M.Duran, C.Anjard, C.Stefan, W.F.Loomis, V.Malhotra. Unconventional secretion of Acb1 is mediated by autophagosomes. J Cell Biol 2010; 188:527-36; PMID:20156967; http://dx.doi.org/10.1083/jcb.200911154
31. R.Manjithaya, C.Anjard, W.F.Loomis, S.Subramani. Unconventional secretion of Pichia pastoris Acb1 is dependent on GRASP protein, peroxisomal functions, and autophagosome formation. J Cell Biol 2010; 188:537-46; PMID:20156962; http://dx.doi.org/10.1083/jcb.200911149
32. Y.M.Lim, H.Lim, K.Y.Hur, W.Quan, H.Y.Lee, H.Cheon, D.Ryu, S.H.Koo, H.L.Kim, J.Kim, et al. Systemic autophagy insufficiency compromises adaptation to metabolic stress and facilitates progression from obesity to diabetes. Nat Commun 2014; 5:4934; PMID:25255859; http://dx.doi.org/10.1038/ncomms5934
33. R.A.Nixon. The role of autophagy in neurodegenerative disease. Nat Med 2013; 19:983-97; PMID:23921753; http://dx.doi.org/10.1038/nm.3232
34. H.Harris, D.C.Rubinsztein. Control of autophagy as a therapy for neurodegenerative disease. Nat Rev Neurol 2012; 8:108-17; http://dx.doi.org/10.1038/nrneurol.2011.200
35. I.Y.Tamboli, E.Barth, L.Christian, M.Siepmann, S.Kumar, S.Singh, K.Tolksdorf, M.T.Heneka, D.Lütjohann, P.Wunderlich, et al. Statins promote the degradation of extracellular amyloid {beta}-peptide by microglia via stimulation of exosome-associated insulin-degrading enzyme (IDE) secretion. J Biol Chem 2010; 285:37405-14; PMID:20876579; http://dx.doi.org/10.1074/jbc.M110.149468
36. R.A.Nixon. Autophagy, amyloidogenesis and Alzheimer disease. J Cell Sci 2007; 120:4081-91; PMID:18032783; http://dx.doi.org/10.1242/jcs.019265
37. C.Settembre, A.Fraldi, D.L.Medina, A.Ballabio. Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol 2013; 14:283-96; PMID:23609508; http://dx.doi.org/10.1038/nrm3565
38. W.Nickel, C.Rabouille. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 2009; 10:148-55; PMID:19122676; http://dx.doi.org/10.1038/nrm2617
39. J.Merregaert, J.Van Langen, U.Hansen, P.Ponsaerts, A.El Ghalbzouri, E.Steenackers, X.Van Ostade, S.Sercu. Phospholipid scramblase 1 is secreted by a lipid raft-dependent pathway and interacts with the extracellular matrix protein 1 in the dermal epidermal junction zone of human skin. J Biol Chem 2010; 285:37823-37; PMID:20870722; http://dx.doi.org/10.1074/jbc.M110.136408
40. D.Ebrahimi-Fakhari, I.Cantuti-Castelvetri, Z.Fan, E.Rockenstein, E.Masliah, B.T.Hyman, P.J.McLean, V.K.Unni. Distinct roles in vivo for the ubiquitin-proteasome system and the autophagy-lysosomal pathway in the degradation of alpha-synuclein. J Neurosci 2011; 31:14508-20; PMID:21994367; http://dx.doi.org/10.1523/JNEUROSCI.1560-11.2011
41. C.Morck, L.Olsen, C.Kurth, A.Persson, N.J.Storm, E.Svensson, J.O.Jansson, M.Hellqvist, A.Enejder, N.J.Faergeman, et al. Statins inhibit protein lipidation and induce the unfolded protein response in the non-sterol producing nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A 2009; 106:18285-90; PMID:19826081; http://dx.doi.org/10.1073/pnas.0907117106
42. V.Deretic. Autophagy: an emerging immunological paradigm. J Immunol 2012; 189:15-20; http://dx.doi.org/10.4049/jimmunol.1102108
43. C.S.Shi, K.Shenderov, N.N.Huang, J.Kabat, M.Abu-Asab, K.A.Fitzgerald, A.Sher, J.H.Kehrl. Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat Immunol 2012; 13:255-63; PMID:22286270; http://dx.doi.org/10.1038/ni.2215
44. R.Jahn, T.Lang, T.C.Sudhof. Membrane fusion. Cell 2003; 112:519-33; PMID:12600315; http://dx.doi.org/10.1016/S0092-8674(03)00112-0
45. 2+-regulated exocytosis from cortical astrocytes. J Neurosci 2008; 28:7648-58; PMID:18650341; http://dx.doi.org/10.1523/JNEUROSCI.0744-08.2008
46. S.K.Rao, C.Huynh, V.Proux-Gillardeaux, T.Galli, N.W.Andrews. Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis. J Biol Chem 2004; 279:20471-9; PMID:14993220; http://dx.doi.org/10.1074/jbc.M400798200
47. C.Verderio, C.Cagnoli, M.Bergami, M.Francolini, U.Schenk, A.Colombo, L.Riganti, C.Frassoni, E.Zuccaro, L.Danglot, et al. TI-VAMP/VAMP7 is the SNARE of secretory lysosomes contributing to ATP secretion from astrocytes. Biol Cell 2012; 104:213-28; PMID:22188132; http://dx.doi.org/10.1111/boc.201100070
48. E.S.Jung, K.An, H.S.Hong, J.H.Kim, I.Mook-Jung. Astrocyte-originated ATP protects Abeta(1-42)-induced impairment of synaptic plasticity. J Neurosci 2012; 32:3081-7; PMID:22378880; http://dx.doi.org/10.1523/JNEUROSCI.6357-11.2012
49. I.Martins, Y.Wang, M.Michaud, Y.Ma, A.Q.Sukkurwala, S.Shen, O.Kepp, D.Métivier, L.Galluzzi, J.L.Perfettini, et al. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ 2014; 21:79-91; PMID:23852373; http://dx.doi.org/10.1038/cdd.2013.75
50. C.Eroglu, B.A.Barres. Regulation of synaptic connectivity by glia. Nature 2010; 468:223-31; PMID:21068831; http://dx.doi.org/10.1038/nature09612
51. P.B.Verghese, J.M.Castellano, K.Garai, Y.Wang, H.Jiang, A.Shah, G.Bu, C.Frieden, D.M.Holtzman. ApoE influences amyloid-beta (Abeta) clearance despite minimal apoE/Abeta association in physiological conditions. Proc Natl Acad Sci U S A 2013; 110:E1807-16; PMID:23620513; http://dx.doi.org/10.1073/pnas.1220484110
52. Q.Xiao, P.Yan, X.Ma, H.Liu, R.Perez, A.Zhu, E.Gonzales, J.M.Burchett, D.R.Schuler, J.R.Cirrito, et al. Enhancing astrocytic lysosome biogenesis facilitates Abeta clearance and attenuates amyloid plaque pathogenesis. J Neurosci 2014; 34:9607-20; PMID:25031402; http://dx.doi.org/10.1523/JNEUROSCI.3788-13.2014
53. K.Vekrellis, Z.Ye, W.Q.Qiu, D.Walsh, D.Hartley, V.Chesneau, M.R.Rosner, D.J.Selkoe. Neurons regulate extracellular levels of amyloid beta-protein via proteolysis by insulin-degrading enzyme. J Neurosci 2000; 20:1657-65; PMID:10684867
54. W.Gao, P.B.Eisenhauer, K.Conn, J.A.Lynch, J.M.Wells, M.D.Ullman, A.McKee, H.S.Thatte, R.E.Fine. Insulin degrading enzyme is expressed in the human cerebrovascular endothelium and in cultured human cerebrovascular endothelial cells. Neurosci Lett 2004; 371:6-11; PMID:15500957; http://dx.doi.org/10.1016/j.neulet.2004.07.034
55. E.Kilger, A.Buehler, H.Woelfing, S.Kumar, S.A.Kaeser, A.Nagarathinam, J.Walter, M.Jucker, J.Coomaraswamy. BRI2 protein regulates beta-amyloid degradation by increasing levels of secreted insulin-degrading enzyme (IDE). J Biol Chem 2011; 286:37446-57; PMID:21873424; http://dx.doi.org/10.1074/jbc.M111.288373
56. K.Blennow, H.Hampel, M.Weiner, H.Zetterberg. Cerebrospinal fluid and plasma biomarkers in Alzheimer disease. Nat Rev Neurol 2010; 6:131-44; PMID:20157306; http://dx.doi.org/10.1038/nrneurol.2010.4
57. A.J.Turner, L.Fisk, N.N.Nalivaeva. Targeting amyloid-degrading enzymes as therapeutic strategies in neurodegeneration. Ann N Y Acad Sci 2004; 1035:1-20; PMID:15681797; http://dx.doi.org/10.1196/annals.1332.001
58. K.G.Mawuenyega, W.Sigurdson, V.Ovod, L.Munsell, T.Kasten, J.C.Morris, K.E.Yarasheski, R.J.Bateman. Decreased clearance of CNS beta-amyloid in Alzheimer's disease. Science 2010; 330:1774; PMID:21148344; http://dx.doi.org/10.1126/science.1197623
59. L.Liu, K.Duff. A technique for serial collection of cerebrospinal fluid from the cisterna magna in mouse. J Vis Exp 2008; 10(21):pii: 960; PMID:19066529; http://dx.doi.org/10.3791/960
60. M.Moon, J.G.Choi, D.W.Nam, H.S.Hong, Y.J.Choi, M.S.Oh, I.Mook-Jung. Ghrelin ameliorates cognitive dysfunction and neurodegeneration in intrahippocampal amyloid-beta1-42 oligomer-injected mice. Journal of Alzheimer's disease: JAD 2011; 23:147-59; PMID:20930280
61. S.M.Son, H.Song, J.Byun, K.S.Park, H.C.Jang, Y.J.Park, I.Mook-Jung. Altered APP processing in insulin-resistant conditions is mediated by autophagosome accumulation via the inhibition of mammalian target of rapamycin pathway. Diabetes 2012; 61:3126-38; PMID:22829447; http://dx.doi.org/10.2337/db11-1735
62. L.Avrahami, D.Farfara, M.Shaham-Kol, R.Vassar, D.Frenkel, H.Eldar-Finkelman. Inhibition of glycogen synthase kinase-3 ameliorates beta-amyloid pathology and restores lysosomal acidification and mammalian target of rapamycin activity in the Alzheimer disease mouse model: in vivo and in vitro studies. J Biol Chem 2013; 288:1295-306; PMID:23155049; http://dx.doi.org/10.1074/jbc.M112.409250
63. K.Trajkovic, C.Hsu, S.Chiantia, L.Rajendran, D.Wenzel, F.Wieland, P.Schwille, B.Brügger, M.Simons. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008; 319:1244-7; PMID:18309083; http://dx.doi.org/10.1126/science.1153124
64. J.Byun, S.M.Son, M.Y.Cha, M.Shong, Y.J.Hwang, Y.Kim, H.Ryu, M.Moon, K.S.Kim, I.Mook-Jung. CR6-interacting factor 1 is a key regulator in Abeta-induced mitochondrial disruption and pathogenesis of Alzheimer's disease. Cell Death Differ 2015; 22(6):959-73. http://dx.doi.org/10.1038/cdd.2014.184