Syntaxin-17 delivers PINK1/parkin-dependent mitochondrial vesicles to the endolysosomal system

Journal of Cell Biology

Volumn 214, Issue 3, 2016, Pages 275-291

  McLelland, Gian Luca ^a   Lee, Sydney A ^a   McBride, Heidi M ^b   Fon, Edward A ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PARKIN; SNARE PROTEIN; SYNTAXIN; SYNTAXIN 17; UNCLASSIFIED DRUG; MULTIPROTEIN COMPLEX; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ARTICLE; CELL ULTRASTRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOSOME; LYSOSOME; MEMBRANE VESICLE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN TARGETING; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS CELL LINE; CYTOPLASM VESICLE; HUMAN; METABOLISM; MITOPHAGY; MOUSE; PHAGOSOME; PROTEIN TRANSPORT; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOPLASMIC VESICLES; ENDOSOMES; HUMANS; LYSOSOMES; MICE; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MULTIPROTEIN COMPLEXES; PHAGOSOMES; PROTEIN TRANSPORT; QA-SNARE PROTEINS; SNARE PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84980027958     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201603105     Document Type: Article

References (65)

1. Arasaki, K., H. Shimizu, H. Mogari, N. Nishida, N. Hirota, A. Furuno, Y. Kudo, M. Baba, N. Baba, J. Cheng, et al. 2015. A role for the ancient SNA RE syntaxin 17 in regulating mitochondrial division. Dev. Cell. 32:304-317. http ://dx.doi.org/10.1016/j.devcel.2014.12.011
2. Baker, R.W., P.D. Jeffrey, M. Zick, B.P. Phillips, W.T. Wickner, and F.M. Hughson. 2015. A direct role for the Sec1/Munc18-family protein Vps33 as a template for SNA RE assembly. Science. 349:1111-1114. http ://dx.doi.org/10.1126/science.aac7906
3. Balderhaar, H.J., and C. Ungermann. 2013. COR VET and HOPS tethering complexes-coordinators of endosome and lysosome fusion. J. Cell Sci. 126:1307-1316. http ://dx.doi.org/10.1242/jcs.107805
4. Braschi, E., V. Goyon, R. Zunino, A. Mohanty, L. Xu, and H.M. McBride. 2010. Vps35 mediates vesicle transport between the mitochondria and peroxisomes. Curr. Biol. 20:1310-1315. http ://dx.doi.org/10.1016/j.cub.2010.05.066
5. Byrnes, L.J., A. Singh, K. Szeto, N.M. Benvin, J.P. O'Donnell, W.R. Zipfel, and H. Sondermann. 2013. Structural basis for conformational switching and GTP loading of the large G protein atlastin. EMBO J. 32:369-384. http ://dx.doi.org/10.1038/emboj.2012.353
6. Cheng, X.T., B. Zhou, M.Y. Lin, Q. Cai, and Z.H. Sheng. 2015. Axonal autophagosomes recruit dynein for retrograde transport through fusion with late endosomes. J. Cell Biol. 209:377-386. http ://dx.doi.org/10.1083/jcb.201412046
7. Daumke, O., and G.J. Praefcke. 2011. Structural insights into membrane fusion at the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 108:2175-2176. http ://dx.doi.org/10.1073/pnas.1019194108
8. Deatherage, B.L., and B.T. Cookson. 2012. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect. Immun. 80:1948-1957. http ://dx.doi.org/10.1128/IAI.06014-11
9. Diao, J., R. Liu, Y. Rong, M. Zhao, J. Zhang, Y. Lai, Q. Zhou, L.M. Wilz, J. Li, S. Vivona, et al. 2015. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature. 520:563-566. http ://dx.doi.org/10.1038/nature14147
10. Durcan, T.M., M.Y. Tang, J.R. Pérusse, E.A. Dashti, M.A. Aguileta, G.L. McLelland, P. Gros, T.A. Shaler, D. Faubert, B. Coulombe, and E.A. Fon. 2014. USP8 regulates mitophagy by removing K6-linked ubiquitin conjugates from parkin. EMBO J. 33:2473-2491. http ://dx.doi.org/10.15252/embj.201489729
11. Fasshauer, D., R.B. Sutton, A.T. Brunger, and R. Jahn. 1998. Conserved structural features of the synaptic fusion complex: SNA RE proteins reclassified as Q-and R-SNA REs. Proc. Natl. Acad. Sci. USA. 95:15781-15786. http ://dx.doi.org/10.1073/pnas.95.26.15781
12. Fratti, R.A., K.M. Collins, C.M. Hickey, and W. Wickner. 2007. Stringent 3Q.1R composition of the SNA RE 0-layer can be bypassed for fusion by compensatory SNA RE mutation or by lipid bilayer modification. J. Biol. Chem. 282:14861-14867. http ://dx.doi.org/10.1074/jbc.M700971200
13. Frezza, C., S. Cipolat, and L. Scorrano. 2007. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat. Protoc. 2:287-295. http ://dx.doi.org/10.1038/nprot.2006.478
14. Gao, Y., S. Zorman, G. Gundersen, Z. Xi, L. Ma, G. Sirinakis, J.E. Rothman, and Y. Zhang. 2012. Single reconstituted neuronal SNA RE complexes zipper in three distinct stages. Science. 337:1340-1343. http ://dx.doi.org/10.1126/science.1224492
15. Gil, A., L.M. Gutiérrez, C. Carrasco-Serrano, M.T. Alonso, S. Viniegra, and M. Criado. 2002. Modifications in the C terminus of the synaptosomeassociated protein of 25 kDa (SNAP-25) and in the complementary region of synaptobrevin affect the final steps of exocytosis. J. Biol. Chem. 277:9904-9910. http ://dx.doi.org/10.1074/jbc.M110182200
16. Graham, M.E., P. Washbourne, M.C. Wilson, and R.D. Burgoyne. 2001. SNAP-25 with mutations in the zero layer supports normal membrane fusion kinetics. J. Cell Sci. 114:4397-4405.
17. Guo, B., Q. Liang, L. Li, Z. Hu, F. Wu, P. Zhang, Y. Ma, B. Zhao, A.L. Kovács, Z. Zhang, et al. 2014. O-GlcNAc-modification of SNAP-29 regulates autophagosome maturation. Nat. Cell Biol. 16:1215-1226. http ://dx.doi.org/10.1038/ncb3066
18. Hamasaki, M., N. Furuta, A. Matsuda, A. Nezu, A. Yamamoto, N. Fujita, H. Oomori, T. Noda, T. Haraguchi, Y. Hiraoka, et al. 2013. Autophagosomes form at ER-mitochondria contact sites. Nature. 495:389-393. http ://dx.doi.org/10.1038/nature11910
19. Hanson, P.I., R. Roth, H. Morisaki, R. Jahn, and J.E. Heuser. 1997. Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell. 90:523-535. http ://dx.doi.org/10.1016/S0092-8674(00)80512-7
20. Hu, J., Y. Shibata, P.P. Zhu, C. Voss, N. Rismanchi, W.A. Prinz, T.A. Rapoport, and C. Blackstone. 2009. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell. 138:549-561. http ://dx.doi.org/10.1016/j.cell.2009.05.025
21. Hung, V., P. Zou, H.W. Rhee, N.D. Udeshi, V. Cracan, T. Svinkina, S.A. Carr, V.K. Mootha, and A.Y. Ting. 2014. Proteomic mapping of the human mitochondrial intermembrane space in live cells via ratiometric APEX tagging. Mol. Cell. 55:332-341. http ://dx.doi.org/10.1016/j.molcel.2014.06.003
22. Itakura, E., C. Kishi-Itakura, and N. Mizushima. 2012. The hairpin-type tailanchored SNA RE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell. 151:1256-1269. http ://dx.doi.org/10.1016/j.cell.2012.11.001
23. Jiang, P., T. Nishimura, Y. Sakamaki, E. Itakura, T. Hatta, T. Natsume, and N. Mizushima. 2014. The HOPS complex mediates autophagosomelysosome fusion through interaction with syntaxin 17. Mol. Biol. Cell. 25:1327-1337. http ://dx.doi.org/10.1091/mbc.E13-08-0447
24. Kane, L.A., M. Lazarou, A.I. Fogel, Y. Li, K. Yamano, S.A. Sarraf, S. Banerjee, and R.J. Youle. 2014. PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell Biol. 205:143-153. http ://dx.doi.org/10.1083/jcb.201402104
25. Katz, L., and P. Brennwald. 2000. Testing the 3Q:1R "rule": mutational analysis of the ionic "zero" layer in the yeast exocytic SNA RE complex reveals no requirement for arginine. Mol. Biol. Cell. 11:3849-3858. http ://dx.doi.org/10.1091/mbc.11.11.3849
26. Kazlauskaite, A., C. Kondapalli, R. Gourlay, D.G. Campbell, M.S. Ritorto, K. Hofmann, D.R. Alessi, A. Knebel, M. Trost, and M.M. Muqit. 2014. Parkin is activated by PINK1-dependent phosphorylation of ubiquitin at Ser65. Biochem. J. 460:127-139. http ://dx.doi.org/10.1042/BJ20140334
27. Kishi-Itakura, C., I. Koyama-Honda, E. Itakura, and N. Mizushima. 2014. Ultrastructural analysis of autophagosome organization using mammalian autophagy-deficient cells. J. Cell Sci. 127:4089-4102. http ://dx.doi.org/10.1242/jcs.156034
28. Kitada, T., S. Asakawa, N. Hattori, H. Matsumine, Y. Yamamura, S. Minoshima, M. Yokochi, Y. Mizuno, and N. Shimizu. 1998. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 392:605-608. http ://dx.doi.org/10.1038/33416
29. Kloepper, T.H., C.N. Kienle, and D. Fasshauer. 2008. SNA REing the basis of multicellularity: consequences of protein family expansion during evolution. Mol. Biol. Evol. 25:2055-2068. http ://dx.doi.org/10.1093/molbev/msn151
30. Koumandou, V.L., B. Wickstead, M.L. Ginger, M. van der Giezen, J.B. Dacks, and M.C. Field. 2013. Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit. Rev. Biochem. Mol. Biol. 48:373-396. http ://dx.doi.org/10.3109/10409238.2013.821444
31. Koyano, F., K. Okatsu, H. Kosako, Y. Tamura, E. Go, M. Kimura, Y. Kimura, H. Tsuchiya, H. Yoshihara, T. Hirokawa, et al. 2014. Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature. 510:162-166. http ://dx.doi.org/10.1038/nature13392
32. Lauer, J.M., S. Dalal, K.E. Marz, M.L. Nonet, and P.I. Hanson. 2006. SNA RE complex zero layer residues are not critical for N-ethylmaleimidesensitive factor-mediated disassembly. J. Biol. Chem. 281:14823-14832. http ://dx.doi.org/10.1074/jbc.M512706200
33. Lawrence, G.W., and J.O. Dolly. 2002a. Ca2+-induced changes in SNA REs and synaptotagmin I correlate with triggered exocytosis from chromaffin cells: insights gleaned into the signal transduction using trypsin and botulinum toxins. J. Cell Sci. 115:2791-2800.
34. Lawrence, G.W., and J.O. Dolly. 2002b. Multiple forms of SNA RE complexes in exocytosis from chromaffin cells: effects of Ca(2+), MgATP and botulinum toxin type A. J. Cell Sci. 115:667-673.
35. Lee, S., C. Zhang, and X. Liu. 2015. Role of glucose metabolism and ATP in maintaining PINK1 levels during Parkin-mediated mitochondrial damage responses. J. Biol. Chem. 290:904-917. http ://dx.doi.org/10.1074/jbc.M114.606798
36. Li, F., D. Kümmel, J. Coleman, K.M. Reinisch, J.E. Rothman, and F. Pincet. 2014. A half-zippered SNA RE complex represents a functional intermediate in membrane fusion. J. Am. Chem. Soc. 136:3456-3464. http ://dx.doi.org/10.1021/ja410690m
37. Malik, B.R., V.K. Godena, and A.J. Whitworth. 2015. VPS35 pathogenic mutations confer no dominant toxicity but partial loss of function in Drosophila and genetically interact with parkin. Hum. Mol. Genet. 24:6106-6117. http ://dx.doi.org/10.1093/hmg/ddv322
38. McCoy, M.K., A. Kaganovich, I.N. Rudenko, J. Ding, and M.R. Cookson. 2014. Hexokinase activity is required for recruitment of parkin to depolarized mitochondria. Hum. Mol. Genet. 23:145-156. http ://dx.doi.org/10.1093/hmg/ddt407
39. McEwan, D.G., D. Popovic, A. Gubas, S. Terawaki, H. Suzuki, D. Stadel, F.P. Coxon, D. Miranda de Stegmann, S. Bhogaraju, K. Maddi, et al. 2015. PLE KHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GAB ARAP proteins. Mol. Cell. 57:39-54. http ://dx.doi.org/10.1016/j.molcel.2014.11.006
40. McLelland, G.L., V. Soubannier, C.X. Chen, H.M. McBride, and E.A. Fon. 2014. Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J. 33:282-295. http ://dx.doi.org/10.1002/embj.201385902
41. Mishra, P., and D.C. Chan. 2016. Metabolic regulation of mitochondrial dynamics. J. Cell Biol. 212:379-387. http ://dx.doi.org/10.1083/jcb.201511036
42. Neuspiel, M., A.C. Schauss, E. Braschi, R. Zunino, P. Rippstein, R.A. Rachubinski, M.A. Andrade-Navarro, and H.M. McBride. 2008. Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr. Biol. 18:102-108. http ://dx.doi.org/10.1016/j.cub.2007.12.038
43. Ossig, R., H.D. Schmitt, B. de Groot, D. Riedel, S. Keränen, H. Ronne, H. Grubmüller, and R. Jahn. 2000. Exocytosis requires asymmetry in the central layer of the SNA RE complex. EMBO J. 19:6000-6010. http ://dx.doi.org/10.1093/emboj/19.22.6000
44. Poirier, M.A., J.C. Hao, P.N. Malkus, C. Chan, M.F. Moore, D.S. King, and M.K. Bennett. 1998. Protease resistance of syntaxin.SNAP-25.VAMP complexes. Implications for assembly and structure. J. Biol. Chem. 273:11370-11377. http ://dx.doi.org/10.1074/jbc.273.18.11370
45. Rosenbloom, A.B., S.H. Lee, M. To, A. Lee, J.Y. Shin, and C. Bustamante. 2014. Optimized two-color super resolution imaging of Drp1 during mitochondrial fission with a slow-switching Dronpa variant. Proc. Natl. Acad. Sci. USA. 111:13093-13098. http ://dx.doi.org/10.1073/pnas.1320044111
46. Rothman, J.E. 2014. The principle of membrane fusion in the cell (Nobel lecture). Angew. Chem. Int. Ed. Engl. 53:12676-12694. http ://dx.doi.org/10.1002/anie.201402380
47. Ryan, B.J., S. Hoek, E.A. Fon, and R. Wade-Martins. 2015. Mitochondrial dysfunction and mitophagy in Parkinson's: from familial to sporadic disease. Trends Biochem. Sci. 40:200-210. http ://dx.doi.org/10.1016/j.tibs.2015.02.003
48. Scorrano, L. 2013. Keeping mitochondria in shape: a matter of life and death. Eur. J. Clin. Invest. 43:886-893. http ://dx.doi.org/10.1111/eci.12135
49. Sherer, N.M., M.J. Lehmann, L.F. Jimenez-Soto, A. Ingmundson, S.M. Horner, G. Cicchetti, P.G. Allen, M. Pypaert, J.M. Cunningham, and W. Mothes. 2003. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic. 4:785-801. http ://dx.doi.org/10.1034/j.1600-0854.2003.00135.x
50. Söllner, T., S.W. Whiteheart, M. Brunner, H. Erdjument-Bromage, S. Geromanos, P. Tempst, and J.E. Rothman. 1993. SNAP receptors implicated in vesicle targeting and fusion. Nature. 362:318-324. http ://dx.doi.org/10.1038/362318a0
51. Soubannier, V., G.L. McLelland, R. Zunino, E. Braschi, P. Rippstein, E.A. Fon, and H.M. McBride. 2012a. A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr. Biol. 22:135-141. http ://dx.doi.org/10.1016/j.cub.2011.11.057
52. Soubannier, V., P. Rippstein, B.A. Kaufman, E.A. Shoubridge, and H.M. McBride. 2012b. Reconstitution of mitochondria derived vesicle formation demonstrates selective enrichment of oxidized cargo. PLoS One. 7:e52830. http ://dx.doi.org/10.1371/journal.pone.0052830
53. Starai, V.J., C.M. Hickey, and W. Wickner. 2008. HOPS proofreads the trans-SNA RE complex for yeast vacuole fusion. Mol. Biol. Cell. 19:2500-2508. http ://dx.doi.org/10.1091/mbc.E08-01-0077
54. Sugiura, A., G.L. McLelland, E.A. Fon, and H.M. McBride. 2014. A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J. 33:2142-2156. http ://dx.doi.org/10.15252/embj.201488104
55. Sutton, R.B., D. Fasshauer, R. Jahn, and A.T. Brunger. 1998. Crystal structure of a SNA RE complex involved in synaptic exocytosis at 2.4 A resolution. Nature. 395:347-353. http ://dx.doi.org/10.1038/26412
56. Swaney, D.L., R.A. Rodríguez-Mias, and J. Villén. 2015. Phosphorylation of ubiquitin at Ser65 affects its polymerization, targets, and proteome-wide turnover. EMBO Rep. 16:1131-1144. http ://dx.doi.org/10.15252/embr.201540298
57. Takáts, S., P. Nagy, á. Varga, K. Pircs, M. Kárpáti, K. Varga, A.L. Kovács, K. Hegedus, and G. Juhász. 2013. Autophagosomal Syntaxin17-dependent lysosomal degradation maintains neuronal function in Drosophila. J. Cell Biol. 201:531-539. http ://dx.doi.org/10.1083/jcb.201211160
58. Takáts, S., K. Pircs, P. Nagy, á. Varga, M. Kárpáti, K. Hegedus, H. Kramer, A.L. Kovács, M. Sass, and G. Juhász. 2014. Interaction of the HOPS complex with Syntaxin 17 mediates autophagosome clearance in Drosophila. Mol. Biol. Cell. 25:1338-1354. http ://dx.doi.org/10.1091/mbc.E13-08-0449
59. Valente, E.M., P.M. Abou-Sleiman, V. Caputo, M.M. Muqit, K. Harvey, S. Gispert, Z. Ali, D. Del Turco, A.R. Bentivoglio, D.G. Healy, et al. 2004. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science. 304:1158-1160. http ://dx.doi.org/10.1126/science.1096284
60. Van Laar, V.S., B. Arnold, S.J. Cassady, C.T. Chu, E.A. Burton, and S.B. Berman. 2011. Bioenergetics of neurons inhibit the translocation response of Parkin following rapid mitochondrial depolarization. Hum. Mol. Genet. 20:927-940. http ://dx.doi.org/10.1093/hmg/ddq531
61. Vincow, E.S., G. Merrihew, R.E. Thomas, N.J. Shulman, R.P. Beyer, M.J. MacCoss, and L.J. Pallanck. 2013. The PINK1-Parkin pathway promotes both mitophagy and selective respiratory chain turnover in vivo. Proc. Natl. Acad. Sci. USA. 110:6400-6405. http ://dx.doi.org/10.1073/pnas.1221132110
62. Wang, W., X. Wang, H. Fujioka, C. Hoppel, A.L. Whone, M.A. Caldwell, P.J. Cullen, J. Liu, and X. Zhu. 2016. Parkinson's disease-associated mutant VPS35 causes mitochondrial dysfunction by recycling DLP1 complexes. Nat. Med. 22:54-63. http ://dx.doi.org/10.1038/nm.3983
63. Watanabe, Y., N. Katayama, K. Takeuchi, T. Togano, R. Itoh, M. Sato, M. Yamazaki, M. Abe, T. Sato, K. Oda, et al. 2013. Point mutation in syntaxin-1A causes abnormal vesicle recycling, behaviors, and short term plasticity. J. Biol. Chem. 288:34906-34919. http ://dx.doi.org/10.1074/jbc.M113.504050
64. Yamano, K., N. Matsuda, and K. Tanaka. 2016. The ubiquitin signal and autophagy: an orchestrated dance leading to mitochondrial degradation. EMBO Rep. 17:300-316. http ://dx.doi.org/10.15252/embr.201541486
65. Yoshii, S.R., and N. Mizushima. 2015. Autophagy machinery in the context of mammalian mitophagy. Biochim. Biophys. Acta. 1853(10, 10 Pt B):2797-2801. http ://dx.doi.org/10.1016/j.bbamcr.2015.01.013