Principles of membrane tethering and fusion in endosome and lysosome biogenesis

Current Opinion in Cell Biology

Volumn 29, Issue 1, 2014, Pages 61-66

  Kümmel, Daniel ^a   Ungermann, Christian ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ENDOSOMES; HUMANS; LYSOSOMES; MEMBRANE FUSION; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84900012487     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.04.007     Document Type: Review

References (58)

1. Huotari J., Helenius A. Endosome maturation. EMBO J 2011, 30:3481-3500.
2. Hurley J.H., Emr S.D. The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu Rev Biophys Biomol Struct 2006, 35:277-298.
3. Seaman M.N.J., Gautreau A., Billadeau D.D. Retromer-mediated endosomal protein sorting: all WASHed up!. Trends Cell Biol 2013, 10.1016/j.tcb.2013.04.010.
4. Weber T., Zemelman B., McNew J., Westermann B., Gmachl M., Parlati F., Sollner T., Rothman J. SNAREpins: minimal machinery for membrane fusion. Cell 1998, 92:759-772.
5. Sutton R., Fasshauer D., Jahn R., Brunger A. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4Å resolution. Nature 1998, 395:347-353.
6. Clary D., Griff I., Rothman J. SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast. Cell 1990, 61:709-721.
7. Block M., Glick B., Wilcox C., Wieland F., Rothman J. Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport. Proc Natl Acad Sci U S A 1988, 85:7852-7856.
8. Südhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
9. Barr F.A. Rab GTPases and membrane identity: causal or inconsequential?. J Cell Biol 2013, 202:191-199.
10. Zerial M., McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001, 2:107-117.
11. Pfeffer S. Transport-vesicle targeting: tethers before SNAREs. Nat Cell Biol 1999, 1:E17-E22.
12. Gillingham A., Munro S. Long coiled-coil proteins and membrane traffic. Biochim Biophys Acta 2003, 1641:71-85.
13. Yu I.-M., Hughson F.M. Tethering factors as organizers of intracellular vesicular traffic. Annu Rev Cell Dev Biol 2010, 26:137-156.
14. Jackson L.P., Kümmel D., Reinisch K.M., Owen D.J. Structures and mechanisms of vesicle coat components and multisubunit tethering complexes. Curr Opin Cell Biol 2012, 24:475-483.
15. Mima J., Hickey C.M., Xu H., Jun Y., Wickner W. Reconstituted membrane fusion requires regulatory lipids, SNAREs and synergistic SNARE chaperones. EMBO J 2008, 27:2031-2042.
16. Stroupe C., Hickey C.M., Mima J., Burfeind A.S., Wickner W. Minimal membrane docking requirements revealed by reconstitution of Rab GTPase-dependent membrane fusion from purified components. Proc Natl Acad Sci 2009, 106:17626-17633.
17. Ohya T., Miaczynska M., Coskun Ü., Lommer B., Runge A., Drechsel D., Kalaidzidis Y., Zerial M. Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes. Nature 2009, 459:1091-1097.
18. Bucci C., Parton R., Mather I., Stunnenberg H., Simons K., Hoflack B., Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 1992, 70:715-728.
19. Bethani I., Lang T., Geumann U., Sieber J.J., Jahn R., Rizzoli S.O. The specificity of SNARE pairing in biological membranes is mediated by both proof-reading and spatial segregation. EMBO J 2007, 26:3981-3992.
20. Mishra A., Eathiraj S., Corvera S., Lambright D.G. Structural basis for Rab GTPase recognition and endosome tethering by the C2H2 zinc finger of Early Endosomal Autoantigen 1 (EEA1). Proc Natl Acad Sci U S A 2010, 107:10866-10871.
21. Kutateladze T., Ogburn K., Watson W., de Beer T., Emr S., Burd C., Overduin M. Phosphatidylinositol 3-phosphate recognition by the FYVE domain. Mol Cell 1999, 3:805-811.
22. Lawe D., Patki V., Heller-Harrison R., Lambright D., Corvera S. The FYVE domain of early endosome antigen 1 is required for both phosphatidylinositol 3-phosphate and Rab5 binding. Critical role of this dual interaction for endosomal localization. J Biol Chem 2000, 275:3699-3705.
23. Dumas J., Merithew E., Sudharshan E., Rajamani D., Hayes S., Lawe D., Corvera S., Lambright D. Multivalent endosome targeting by homodimeric EEA1. Mol Cell 2001, 8:947-958.
24. Nielsen E., Christoforidis S., Uttenweiler-Joseph S., Miaczynska M., Dewitte F., Wilm M., Hoflack B., Zerial M. Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J Cell Biol 2000, 151:601-612.
25. Eathiraj S., Pan X., Ritacco C., Lambright D.G. Structural basis of family-wide Rab GTPase recognition by rabenosyn-5. Nature 2005, 436:415-419.
26. Morrison H.A., Dionne H., Rusten T.E., Brech A., Fisher W.W., Pfeiffer B.D., Celniker S.E., Stenmark H., Bilder D. Regulation of early endosomal entry by the Drosophila tumor suppressors Rabenosyn and Vps45. Mol Biol Cell 2008, 19:4167-4176.
27. Horiuchi H., Lippe R., McBride H., Rubino M., Woodman P., Stenmark H., Rybin V., Wilm M., Ashman K., Mann M., et al. A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 1997, 90:1149-1159.
28. Zhu G., Zhai P., Liu J., Terzyan S., Li G., Zhang X.C. Structural basis of Rab5-Rabaptin5 interaction in endocytosis. Nat Struct Mol Biol 2004, 11:975-983.
29. Lippé R., Miaczynska M., Rybin V., Runge A., Zerial M. Functional synergy between Rab5 effector rabaptin-5 and exchange factor rabex-5 when physically associated in a complex 2001, 12:2219-2228.
30. Delprato A., Lambright D.G. Structural basis for Rab GTPase activation by VPS9 domain exchange factors. Nat Struct Mol Biol 2007, 14:406-412.
31. Burd C.G., Emr S.D. Phosphatidylinositol(3)-phosphate signaling mediated by specific binding to RING FYVE domains. Mol Cell 1998, 2:157-162.
32. Peterson M.R., Burd C.G., Emr S.D. Vac1p coordinates Rab and phosphatidylinositol 3-kinase signaling in Vps45p-dependent vesicle docking/fusion at the endosome. Curr Biol 1999, 9:159-162.
33. Tall G., Hama H., DeWald D., Horazdovsky B. The phosphatidylinositol 3-phosphate binding protein Vac1p interacts with a Rab GTPase and a Sec1p homologue to facilitate vesicle-mediated vacuolar protein sorting. Mol Biol Cell 1999, 10:1873-1889.
34. Nickerson D.P., Brett C.L., Merz A.J. Vps-C complexes: gatekeepers of endolysosomal traffic. Curr Opin Cell Biol 2009, 21:543-551.
35. Solinger J.A., Spang A. Tethering complexes in the endocytic pathway: CORVET and HOPS. FEBS J 2013, 10.1111/febs.12151.
36. Balderhaar H.J.K., Ungermann C. CORVET and HOPS tethering complexes-coordinators of endosome and lysosome fusion. J Cell Sci 2013, 126:1307-1316.
37. Balderhaar H.J.K., Lachmann J., Yavavli E., Bröcker C., Lürick A., Ungermann C. The CORVET complex promotes tethering and fusion of Rab5/Vps21-positive membranes. Proc Natl Acad Sci 2013, 110:3823-3828.
38. Markgraf D.F., Ahnert F., Arlt H., Mari M., Peplowska K., Epp N., Griffith J., Reggiori F., Ungermann C. The CORVET subunit Vps8 cooperates with the Rab5 homolog Vps21 to induce clustering of late endosomal compartments. Mol Biol Cell 2009, 20:5276-5289.
39. Peplowska K., Markgraf D.F., Ostrowicz C.W., Bange G., Ungermann C. The CORVET tethering complex interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis. Dev Cell 2007, 12:739-750.
40. Plemel R.L., Lobingier B.T., Brett C.L., Angers C.G., Nickerson D.P., Paulsel A., Sprague D., Merz A.J. Subunit organization and Rab interactions of Vps-C protein complexes that control endolysosomal membrane traffic. Mol Biol Cell 2011, 22:1353-1363.
41. Ostrowicz C.W., Bröcker C., Ahnert F., Nordmann M., Lachmann J., Peplowska K., Perz A., Auffarth K., Engelbrecht-Vandré S., Ungermann C. Defined subunit arrangement and rab interactions are required for functionality of the HOPS tethering complex. Traffic 2010, 11:1334-1346.
42. Pawelec A., Arsić J., Kölling R. Mapping of Vps21 and HOPS binding sites in Vps8 and effect of binding site mutants on endocytic trafficking. Eukaryot Cell 2010, 9:602-610.
43. Seals D., Eitzen G., Margolis N., Wickner W., Price A. A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc Natl Acad Sci U S A 2000, 97:9402-9407.
44. Wurmser A.E., Sato T.K., Emr S.D. New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J Cell Biol 2000, 151:551-562.
45. Bröcker C., Kuhlee A., Gatsogiannis C., Kleine Balderhaar H.J., Hönscher C., Engelbrecht-Vandré S., Ungermann C., Raunser S. Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering complex. Proc Natl Acad Sci 2012, 109:1991-1996.
46. Cabrera M., Arlt H., Epp N., Lachmann J., Griffith J., Perz A., Reggiori F., Ungermann C. Functional separation of endosomal fusion factors and the class C core vacuole/endosome tethering (CORVET) complex in endosome biogenesis. J Biol Chem 2013, 288:5166-5175.
47. Zick M., Wickner W. The tethering complex HOPS catalyzes assembly of the soluble SNARE Vam7 into fusogenic trans-SNARE complexes. Mol Biol Cell 2013, 10.1091/mbc.E13-07-0419.
48. Rieder S.E., Emr S.D. A novel RING finger protein complex essential for a late step in protein transport to the yeast vacuole. Mol Biol Cell 1997, 8:2307-2327.
49. Price A., Wickner W., Ungermann C. Proteins needed for vesicle budding from the golgi complex are also required for the docking step of homotypic vacuole fusion. J Cell Biol 2000, 148:1223-1230.
50. Graham S.C., Wartosch L., Gray S.R., Scourfield E.J., Deane J.E., Luzio J.P., Owen D.J. Structural basis of Vps33A recruitment to the human HOPS complex by Vps16. Proc Natl Acad Sci 2013, 110:13345-13350.
51. Baker R.W., Jeffrey P.D., Hughson F.M. Crystal structures of the Sec1/Munc18 (SM) protein Vps33, alone and bound to the homotypic fusion and vacuolar protein sorting (HOPS) subunit Vps16*. PLoS ONE 2013, 8:e67409.
52. Jahn R., Scheller R. SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 2006, 7:631-643.
53. Nordmann M., Cabrera M., Perz A., Bröcker C., Ostrowicz C.W., Engelbrecht-Vandré S., Ungermann C. The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr Biol 2010, 20:1654-1659.
54. Gerondopoulos A., Langemeyer L., Liang J.-R., Linford A., Barr F.A. BLOC-3 mutated in Hermansky-Pudlak syndrome is a Rab32/38 guanine nucleotide exchange factor. Curr Biol 2012, 10.1016/j.cub.2012.09.020.
55. Hutagalung A.H., Novick P.J. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 2011, 91:119-149.
56. Geumann U., Barysch S.V., Hoopmann P., Jahn R., Rizzoli S.O. SNARE function is not involved in early endosome docking. Mol Biol Cell 2008, 19:5327-5337.
57. Hickey C.M., Wickner W. HOPS initiates vacuole docking by tethering membranes before trans-SNARE complex assembly. Mol Biol Cell 2010, 21:2297-2305.
58. Ma C., Su L., Seven A.B., Xu Y., Rizo J. Reconstitution of the vital functions of Munc18 and Munc13 in neurotransmitter release. Science 2013, 339:421-425.