ESCRT-0 dysfunction compromises autophagic degradation of protein aggregates and facilitates ER stress-mediated neurodegeneration via apoptotic and necroptotic pathways

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Oshima, Ryuji ^a,b   Hasegawa, Takafumi ^a   Tamai, Keiichi ^b   Sugeno, Naoto ^a   Yoshida, Shun ^a   Kobayashi, Junpei ^a   Kikuchi, Akio ^a   Baba, Toru ^a   Futatsugi, Akira ^c   Sato, Ikuro ^b   Satoh, Kennichi ^b   Takeda, Atsushi ^d   Aoki, Masashi ^a   Tanaka, Nobuyuki ^b  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MIYAGI CANCER CENTER RESEARCH INSTITUTE   (Japan)

^c KOBE CITY COLLEGE OF NURSING   (Japan)

^d National Hospital Organization Sendai Nishitaga Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT PROTEIN; HEPATOCYTE GROWTH FACTOR-REGULATED TYROSINE KINASE SUBSTRATE; PHOSPHOPROTEIN; PROTEIN AGGREGATE; UBIQUITINATED PROTEIN;

ANIMAL; APOPTOSIS; AUTOPHAGY; CELL SURVIVAL; CYTOLOGY; ENDOPLASMIC RETICULUM STRESS; FOREBRAIN; GENE SILENCING; GENETICS; HIPPOCAMPUS; METABOLISM; MOUSE; NECROSIS; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELL SURVIVAL; ENDOPLASMIC RETICULUM STRESS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GENE SILENCING; HIPPOCAMPUS; MICE; NECROSIS; PHOSPHOPROTEINS; PROSENCEPHALON; PROTEIN AGGREGATES; SIGNAL TRANSDUCTION; UBIQUITINATED PROTEINS;

EID: 84964671180     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24997     Document Type: Article

References (54)

1. Reiss, C., Lesnik, T., Parvez, H., Parvez, S. & Ehrlich, R. Conformational toxicity and sporadic conformational diseases. Toxicology 153, 115-121 (2000).
2. Bourdenx, M. et al. Protein aggregation and neurodegeneration in prototypical neurodegenerative diseases: Examples of amyloidopathies, tauopathies and synucleinopathies. Prog Neurobiol. doi: 10.1016/j.pneurobio.2015.07.003 (2015).
3. Stefani, M. Generic cell dysfunction in neurodegenerative disorders: role of surfaces in early protein misfolding, aggregation, and aggregate cytotoxicity. Neuroscientist 13, 519-531, doi: 10.1177/1073858407303428 (2007).
4. Tanaka, N., Kyuuma, M. & Sugamura, K. Endosomal sorting complex required for transport proteins in cancer pathogenesis, vesicular transport, and non-endosomal functions. Cancer Sci 99, 1293-1303, doi: 10.1111/j.1349-7006.2008.00825.x (2008).
5. Bache, K. G., Brech, A., Mehlum, A. & Stenmark, H. Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J Cell Biol 162, 435-442, doi: 10.1083/jcb.200302131 (2003).
6. Fader, C. M. & Colombo, M. I. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ 16, 70-78, doi: 10.1038/cdd.2008.168 (2009).
7. Konno, M. et al. Suppression of dynamin GTPase decreases alpha-synuclein uptake by neuronal and oligodendroglial cells: a potent therapeutic target for synucleinopathy. Mol Neurodegener 7, 38, doi: 10.1186/1750-1326-7-38 (2012).
8. Miura, E. et al. VPS35 dysfunction impairs lysosomal degradation of alpha-synuclein and exacerbates neurotoxicity in a Drosophila model of Parkinson's disease. Neurobiol Dis 71c, 1-13, doi: 10.1016/j.nbd.2014.07.014 (2014).
9. Sugeno, N. et al. Lys-63-linked ubiquitination by E3 ubiquitin ligase Nedd4-1 facilitates endosomal sequestration of internalized alpha-synuclein. J Biol Chem 289, 18137-18151, doi: 10.1074/jbc.M113.529461 (2014).
10. Schreij, A. M., Fon, E. A. & McPherson, P. S. Endocytic membrane trafficking and neurodegenerative disease. Cell Mol Life Sci. doi: 10.1007/s00018-015-2105-x (2015).
11. Skibinski, G. et al. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat Genet 37, 806-808, doi: 10.1038/ng1609 (2005).
12. McDonell, L. M. et al. Mutations in STAMBP, encoding a deubiquitinating enzyme, cause microcephaly-capillary malformation syndrome. Nat Genet 45, 556-562, doi: 10.1038/ng.2602 (2013).
13. Hasegawa, T. et al. The AAA-ATPase VPS4 regulates extracellular secretion and lysosomal targeting of alpha-synuclein. PLos One 6, e29460, doi: 10.1371/journal.pone.0029460 (2011).
14. Yamazaki, Y. et al. Immunopositivity for ESCRT-III subunit CHMP2B in granulovacuolar degeneration of neurons in the Alzheimer's disease hippocampus. Neurosci Lett 477, 86-90, doi: 10.1016/j.neulet.2010.04.038 (2010).
15. Tanikawa, S. et al. Endosomal sorting related protein CHMP2B is localized in Lewy bodies and glial cytoplasmic inclusions in alphasynucleinopathy. Neurosci Lett 527, 16-21, doi: 10.1016/j.neulet.2012.08.035 (2012).
16. Edgar, J. R., Willen, K., Gouras, G. K. & Futter, C. E. ESCRTs regulate amyloid precursor protein sorting in multivesicular bodies and intracellular amyloid-beta accumulation. J Cell Sci 128, 2520-2528, doi: 10.1242/jcs.170233 (2015).
17. Morel, E. et al. Phosphatidylinositol-3-phosphate regulates sorting and processing of amyloid precursor protein through the endosomal system. Nat Commun 4, 2250, doi: 10.1038/ncomms3250 (2013).
18. Sekine, Y., Takeda, K. & Ichijo, H. The ASK1-MAP kinase signaling in ER stress and neurodegenerative diseases. Curr Mol Med 6, 87-97 (2006).
19. Zhang, R., Wang, R., Chen, Q. & Chang, H. Inhibition of autophagy using 3-methyladenine increases cisplatin-induced apoptosis by increasing endoplasmic reticulum stress in U251 human glioma cells. Mol Med Rep 12, 1727-1732, doi: 10.3892/mmr.2015.3588 (2015).
20. Xu, L., Liu, J. H., Zhang, J., Zhang, N. & Wang, Z. H. Blockade of autophagy aggravates endoplasmic reticulum stress and improves Paclitaxel cytotoxicity in human cervical cancer cells. Cancer Res Treat 47, 313-321, doi: 10.4143/crt.2013.222 (2015).
21. Liu, Z., Lv, Y., Zhao, N., Guan, G. & Wang, J. Protein kinase R-like ER kinase and its role in endoplasmic reticulum stress-decided cell fate. Cell Death Dis 6, e1822, doi: 10.1038/cddis.2015.183 (2015).
22. Senft, D. & Ronai, Z. A. UPR, autophagy, and mitochondria crosstalk underlies the ER stress response. Trends Biochem Sci 40, 141-148, doi: 10.1016/j.tibs.2015.01.002 (2015).
23. Feoktistova, M. & Leverkus, M. Programmed necrosis and necroptosis signalling. FEBS J 282, 19-31, doi: 10.1111/febs.13120 (2015).
24. Tamai, K. et al. Loss of hrs in the central nervous system causes accumulation of ubiquitinated proteins and neurodegeneration. Am J Pathol 173, 1806-1817, doi: 10.2353/ajpath.2008.080684 (2008).
25. Yamanaka, T. et al. Loss of aPKClambda in differentiated neurons disrupts the polarity complex but does not induce obvious neuronal loss or disorientation in mouse brains. PLos One 8, e84036, doi: 10.1371/journal.pone.0084036 (2013).
26. Tamai, K. et al. Role of Hrs in maturation of autophagosomes in mammalian cells. Biochem Biophys Res Commun 360, 721-727, doi: 10.1016/j.bbrc.2007.06.105 (2007).
27. Roudier, N., Lefebvre, C. & Legouis, R. CeVPS-27 is an endosomal protein required for the molting and the endocytic trafficking of the low-density lipoprotein receptor-related protein 1 in Caenorhabditis elegans. Traffic 6, 695-705, doi: 10.1111/j.1600-0854.2005.00309.x (2005).
28. Shirahama, K., Noda, T. & Ohsumi, Y. Mutational analysis of Csc1/Vps4p: involvement of endosome in regulation of autophagy in yeast. Cell Struct Funct 22, 501-509 (1997).
29. Ao, X., Zou, L. & Wu, Y. Regulation of autophagy by the Rab GTPase network. Cell Death Differ 21, 348-358, doi: 10.1038/ cdd.2013.187 (2014).
30. Jiang, P. et al. The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17. Mol Biol Cell 25, 1327-1337, doi: 10.1091/mbc.E13-08-0447 (2014).
31. Ganley, I. G. Autophagosome maturation and lysosomal fusion. Essays Biochem 55, 65-78, doi: 10.1042/bse0550065 (2013).
32. Shaid, S., Brandts, C. H., Serve, H. & Dikic, I. Ubiquitination and selective autophagy. Cell Death Differ 20, 21-30, doi: 10.1038/ cdd.2012.72 (2013).
33. Watanabe, Y. et al. p62/SQSTM1-dependent autophagy of Lewy body-like alpha-synuclein inclusions. PLos One 7, e52868, doi: 10.1371/journal.pone.0052868 (2012).
34. Tanji, K. et al. p62 Deficiency Enhances alpha-Synuclein Pathology in Mice. Brain Pathol 25, 552-564, doi: 10.1111/bpa.12214 (2015).
35. Filimonenko, M. et al. Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J Cell Biol 179, 485-500, doi: 10.1083/jcb.200702115 (2007).
36. Zatloukal, K. et al. p62 Is a common component of cytoplasmic inclusions in protein aggregation diseases. Am J Pathol 160, 255-263, doi: 10.1016/s0002-9440(10)64369-6 (2002).
37. Bernales, S., Schuck, S. & Walter, P. ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 3, 285-287 (2007).
38. Hasegawa, T. et al. Parkin protects against tyrosinase-mediated dopamine neurotoxicity by suppressing stress-activated protein kinase pathways. J Neurochem 105, 1700-1715 (2008).
39. Tournier, C. et al. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288, 870-874 (2000).
40. Yang, D. D. et al. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 389, 865-870, doi: 10.1038/39899 (1997).
41. Ofengeim, D. et al. Activation of necroptosis in multiple sclerosis. Cell reports 10, 1836-1849, doi: 10.1016/j.celrep.2015.02.051 (2015).
42. Degterev, A. et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 1, 112-119, doi: 10.1038/nchembio711 (2005).
43. Wu, J. R. et al. Necrostatin-1 protection of dopaminergic neurons. Neural Regen Res 10, 1120-1124, doi: 10.4103/1673-5374.160108 (2015).
44. Re, D. B. et al. Necroptosis drives motor neuron death in models of both sporadic and familial ALS. Neuron 81, 1001-1008, doi: 10.1016/j.neuron.2014.01.011 (2014).
45. Vandenabeele, P., Galluzzi, L., Vanden Berghe, T. & Kroemer, G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 11, 700-714, doi: 10.1038/nrm2970 (2010).
46. An, J. et al. ARC is a novel therapeutic approach against acetaminophen-induced hepatocellular necrosis. J Hepatol 58, 297-305, doi: 10.1016/j.jhep.2012.10.002 (2013).
47. Ramachandran, A. et al. Receptor interacting protein kinase 3 is a critical early mediator of acetaminophen-induced hepatocyte necrosis in mice. Hepatology 58, 2099-2108, doi: 10.1002/hep.26547 (2013).
48. Zhao, J. et al. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc Natl Acad Sci USA 109, 5322-5327, doi: 10.1073/pnas.1200012109 (2012).
49. Douglas, D. L. & Baines, C. P. PARP1-mediated necrosis is dependent on parallel JNK and Ca(2)(+ )/calpain pathways. J Cell Sci 127, 4134-4145, doi: 10.1242/jcs.128009 (2014).
50. Dillon, C. P. et al. Survival function of the FADD-CASPASE-8-cFLIP(L) complex. Cell Rep 1, 401-407, doi: 10.1016/j. celrep.2012.03.010 (2012).
51. Hasegawa, T. et al. Role of TPPP/p25 on alpha-synuclein-mediated oligodendroglial degeneration and the protective effect of SIRT2 inhibition in a cellular model of multiple system atrophy. Neurochem Int 57, 857-866 (2010).
52. Watanabe, S., Kaneko, K. & Yamanaka, K. Accelerated disease onset with stabilized familial amyotrophic lateral sclerosis (ALS)- linked mutant TDP-43 proteins. J Biol Chem 288, 3641-3654, doi: 10.1074/jbc.M112.433615 (2013).
53. Da Silva, J. S., Hasegawa, T., Miyagi, T., Dotti, C. G. & Abad-Rodriguez, J. Asymmetric membrane ganglioside sialidase activity specifies axonal fate. Nat Neurosci 8, 606-615, doi: 10.1038/nn1442 (2005).
54. Hasegawa, T. et al. Alpha-synuclein facilitates the toxicity of oxidized catechol metabolites: implications for selective neurodegeneration in Parkinson's disease. FEBS Lett 580, 2147-2152 (2006).