Characterization of the mammalian CORVET and HOPS complexes and their modular restructuring for endosome specificity

Journal of Biological Chemistry

Volumn 290, Issue 51, 2015, Pages 30280-30290

  Van Der Kant, Rik ^a,c   Jonker, Caspar T H ^b   Wijdeven, Ruud H ^a   Bakker, Jeroen ^a   Janssen, Lennert ^a   Klumperman, Judith ^b   Neefjes, Jacques ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; PROTEINS; YEAST;

CORE INTERACTIONS; ENDOSOMAL SYSTEM; LATE ENDOSOMES; MOLECULAR SWITCHES; MULTISUBUNIT; NOVEL PROTEINS; RENAL DYSFUNCTION; SNARE PROTEINS;

MAMMALS;

CLASS C CORE VACUOLE ENDOSOME TETHERING COMPLEX; HOMOTYPIC FUSION AND VACUOLE PROTEIN SORTING COMPLEX; MEMBRANE PROTEIN; PROTEIN TGFBRAP1; PROTEIN VIPAS39; PROTEIN VPS11; PROTEIN VPS33B; RAB7 INTERACTING LYSOSOMAL PROTEIN; UNCLASSIFIED DRUG; MULTIPROTEIN COMPLEX; RILP PROTEIN, HUMAN; SIGNAL PEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TGFBRAP1 PROTEIN, HUMAN; VESICULAR TRANSPORT PROTEIN; VIPAS39 PROTEIN, HUMAN; VPS11 PROTEIN, HUMAN; VPS33B PROTEIN, HUMAN; VPS39 PROTEIN, HUMAN;

ARTHROGRYPOSIS; ARTICLE; CELL MIGRATION; CELL SPECIFICITY; CHOLESTASIS; CONTROLLED STUDY; ENDOSOME; HUMAN; HUMAN CELL; KIDNEY DYSFUNCTION; MOLECULAR INTERACTION; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS; AMINO ACID SUBSTITUTION; CELL LINE; GENETICS; KIDNEY FAILURE; METABOLISM; MISSENSE MUTATION; PATHOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SUBSTITUTION; ARTHROGRYPOSIS; CELL LINE; CHOLESTASIS; ENDOSOMES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MULTIPROTEIN COMPLEXES; MUTATION, MISSENSE; RENAL INSUFFICIENCY; VESICULAR TRANSPORT PROTEINS;

EID: 84950341301     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.688440     Document Type: Article

References (48)

1. Stenmark, H. (2009) Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513-525
2. Wickner, W. (2010) Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles. Annu. Rev. Cell Dev. Biol. 26, 115-136
3. Sato, T. K., Rehling, P., Peterson, M. R., and Emr, S. D. (2000) Class C Vps protein complex regulates vacuolar SNARE pairing and is required for vesicle docking/fusion. Mol. Cell 6, 661-671
4. Wurmser, A. E., Sato, T. K., and Emr, S. D. (2000) 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. 151, 551-562
5. Nakamura, N., Hirata, A., Ohsumi, Y., and Wada, Y. (1997) Vam2/Vps41p and Vam6/Vps39p are components of a protein complex on the vacuolar membranes and involved in the vacuolar assembly in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 272, 11344-11349
6. Plemel, R. L., Lobingier, B. T., Brett, C. L., Angers, C. G., Nickerson, D. P., Paulsel, A., Sprague, D., and Merz, A. J. (2011) Subunit organization and Rab interactions of Vps-C protein complexes that control endolysosomal membrane traffic. Mol. Biol. Cell 22, 1353-1363
7. Ostrowicz, C. W., Bröcker, C., Ahnert, F., Nordmann, M., Lachmann, J., Peplowska, K., Perz, A., Auffarth, K., Engelbrecht-Vandré, S., and Ungermann, C. (2010) Defined subunit arrangement and rab interactions are required for functionality of the HOPS tethering complex. Traffic 11, 1334-1346
8. Bröcker, C., Kuhlee, A., Gatsogiannis, C., Balderhaar, H. J., Hönscher, C., Engelbrecht-Vandré, S., Ungermann, C., and Raunser, S. (2012) Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering complex. Proc. Natl. Acad. Sci. U.S.A. 109, 1991-1996
9. Cabrera, M., Langemeyer, L., Mari, M., Rethmeier, R., Orban, I., Perz, A., Bröcker, C., Griffith, J., Klose, D., Steinhoff, H.-J., Reggiori, F., Engelbrecht-Vandré, S., and Ungermann, C. (2010) Phosphorylation of a membrane curvature-sensing motif switches function of the HOPS subunit Vps41 in membrane tethering. J. Cell Biol. 191, 845-859
10. Rink, J., Ghigo, E., Kalaidzidis, Y., and Zerial, M. (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749
11. Perini, E. D., Schaefer, R., Stöter, M., Kalaidzidis, Y., and Zerial, M. (2014) Mammalian CORVET is required for fusion and conversion of distinct early endosome subpopulations. Traffic 15, 1366-1389
12. Wartosch, L., Günesdogan, U., Graham, S. C., and Luzio, J. P. (2015) Recruitment of VPS33A to HOPS by VPS16 is required for lysosome fusion with endosomes and autophagosomes. Traffic 16, 727-742
13. Jiang, P., Nishimura, T., Sakamaki, Y., Itakura, E., Hatta, T., Natsume, T., and Mizushima, N. (2014) The HOPS complex mediates autophagosomelysosome fusion through interaction with syntaxin 17. Mol. Biol. Cell 25, 1327-1337
14. McEwan, D. G., Popovic, D., Gubas, A., Terawaki, S., Suzuki, H., Stadel, D., Coxon, F. P., Miranda de Stegmann, D., Bhogaraju, S., Maddi, K., Kirchof, A., Gatti, E., Helfrich, M. H., Wakatsuki, S., Behrends, C., Pierre, P., and Dikic, I. (2015)PLEKHM1regulates autophagosome-lysosome fusion throughHOPS complex and LC3/GABARAP proteins. Mol. Cell 57, 39-54
15. McEwan, D. G., Richter, B., Claudi, B., Wigge, C., Wild, P., Farhan, H., McGourty, K., Coxon, F. P., Franz-Wachtel, M., Perdu, B., Akutsu, M., Habermann, A., Kirchof, A., Helfrich, M. H., Odgren, P. R., Van Hul, W., Frangakis, A. S., Rajalingam, K., Macek, B., Holden, D. W., Bumann, D., and Dikic, I. (2015) PLEKHM1 regulates Salmonella-containing vacuole biogenesis and infection. Cell Host Microbe 17, 58-71
16. Zhu, G.-D., Salazar, G., Zlatic, S. A., Fiza, B., Doucette, M. M., Heilman, C. J., Levey, A. I., Faundez, V., and L'hernault, S. W. (2009) SPE-39 family proteins interact with the HOPS complex and function in lysosomal delivery. Mol. Biol. Cell 20, 1223-1240
17. Chirivino, D., Del Maestro, L., Formstecher, E.,Hupé, P., Raposo, G., Louvard, D., and Arpin, M. (2011) TheERMproteins interact with the HOPS complex to regulate the maturation of endosomes. Mol. Biol. Cell 22, 375-385
18. Liang, C., Lee, J.-S., Inn, K.-S., Gack, M. U., Li, Q., Roberts, E. A., Vergne, I., Deretic, V., Feng, P., Akazawa, C., and Jung, J. U. (2008) Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat. Cell Biol. 10, 776-787
19. Carette, J. E., Raaben, M., Wong, A. C., Herbert, A. S., Obernosterer, G., Mulherkar, N., Kuehne, A. I., Kranzusch, P. J., Griffin, A. M., Ruthel, G., Dal Cin, P., Dye, J. M., Whelan, S. P., Chandran, K., and Brummelkamp, T. R. (2011) Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477, 340-343
20. Garg, S., Sharma, M., Ung, C., Tuli, A., Barral, D. C., Hava, D. L., Veerapen, N., Besra, G. S., Hacohen, N., and Brenner, M. B. (2011) Lysosomal trafficking, antigen presentation, and microbial killing are controlled by the Arf-like GTPase Arl8b. Immunity 35, 182-193
21. Smith, H., Galmes, R., Gogolina, E., Straatman-Iwanowska, A., Reay, K., Banushi, B., Bruce, C. K., Cullinane, A. R., Romero, R., Chang, R., Ackermann, O., Baumann, C., Cangul, H., Cakmak Celik, F., Aygun, C., Coward, R., Dionisi-Vici, C., Sibbles, B., Inward, C., Kim, C. A., Klumperman, J., Knisely, A. S., Watson, S. P., and Gissen, P. (2012) Associations among genotype, clinical phenotype, and intracellular localization of trafficking proteins in ARC syndrome. Hum. Mutat. 33, 1656-1664
22. Cullinane, A. R., Straatman-Iwanowska, A., Zaucker, A., Wakabayashi, Y., Bruce, C. K., Luo, G., Rahman, F., Gürakan, F., Utine, E., Ozkan, T. B., Denecke, J., Vukovic, J., Di Rocco, M., Mandel, H., Cangul, H., Matthews, R. P., Thomas, S. G., Rappoport, J. Z., Arias, I. M., Wolburg, H., Knisely, A. S., Kelly, D. A.,Müller, F., Maher, E. R., and Gissen, P. (2010) Mutations in VIPAR cause an arthrogryposis, renal dysfunction, and cholestasis syndrome phenotype with defects in epithelial polarization. Nat. Genet. 42, 303-312
23. Gissen, P., Johnson, C. A., Morgan, N. V., Stapelbroek, J. M., Forshew, T., Cooper, W. N., McKiernan, P. J., Klomp, L. W., Morris, A. A., Wraith, J. E., McClean, P., Lynch, S. A., Thompson, R. J., Lo, B., Quarrell, O. W., Di Rocco, M., Trembath, R. C., Mandel, H., Wali, S., Karet, F. E., Knisely, A. S., Houwen, R. H., Kelly, D. A., and Maher, E. R. (2004) Mutations in VPS33B, encoding a regulator of SNARE-dependent membrane fusion, cause arthrogryposis- renal dysfunction-cholestasis (ARC) syndrome. Nat. Genet. 36, 400-404
24. Lo, B., Li, L., Gissen, P., Christensen, H., McKiernan, P. J., Ye, C., Abdelhaleem, M., Hayes, J. A., Williams, M. D., Chitayat, D., and Kahr, W. H. (2005) Requirement of VPS33B, a member of the Sec1/Munc18 protein family, in megakaryocyte and platelet α-granule biogenesis. Blood 106, 4159-4166
25. van Luijn, M. M., Kreft, K. L., Jongsma, M. L., Mes, S. W., Wierenga-Wolf, A. F., van Meurs, M., Melief, M.-J., der Kant, R. v., Janssen, L., Janssen, H., Tan, R., Priatel, J. J., Neefjes, J., Laman, J. D., and Hintzen, R. Q. (2015) Multiple sclerosis-associated CLEC16A controls HLA class II expression via late endosome biogenesis. Brain 138, 1531-1547
26. Tornieri, K., Zlatic, S. A., Mullin, A. P., Werner, E., Harrison, R., L'hernault, S. W., and Faundez, V. (2013) Vps33b pathogenic mutations preferentially affect VIPAS39/SPE-39-positive endosomes. Hum. Mol. Genet. 22, 5215-5228
27. Pols, M. S., van Meel, E., Oorschot, V., ten Brink, C., Fukuda, M., Swetha, M. G., Mayor, S., and Klumperman, J. (2013) hVps41 and VAMP7 function in direct TGN to late endosome transport of lysosomal membrane proteins. Nat. Commun. 4, 1361
28. Vennegoor, C., Calafat, J., Hageman, P., van Buitenen, F., Janssen, H., Kolk, A., and Rümke, P. (1985) Biochemical characterization and cellular localization of a formalin-resistant melanoma-associated antigen reacting with monoclonal antibody NKI/C-3. Int. J. Cancer 35, 287-295
29. Jordens, I., Fernandez-Borja, M., Marsman, M., Dusseljee, S., Janssen, L., Calafat, J., Janssen, H., Wubbolts, R., and Neefjes, J. (2001) The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 11, 1680-1685
30. van der Kant, R., Fish, A., Janssen, L., Janssen, H., Krom, S., Ho, N., Brummelkamp, T., Carette, J., Rocha, N., and Neefjes, J. (2013) Late endosomal transport and tethering are coupled processes controlled by RILP and the cholesterol sensor ORP1L. J. Cell Sci. 126, 3462-3474
31. Lin, X., Yang, T., Wang, S., Wang, Z., Yun, Y., Sun, L., Zhou, Y., Xu, X., Akazawa, C., Hong, W., and Wang, T. (2014) RILP interacts with HOPS complex via VPS41 subunit to regulate endocytic trafficking. Sci. Rep. 4, 7282
32. Gissen, P., Johnson, C. A., Gentle, D., Hurst, L. D., Doherty, A. J., O'Kane, C. J., Kelly, D. A., and Maher, E. R. (2005) Comparative evolutionary analysis of VPS33 homologues: genetic and functional insights. Hum. Mol. Genet. 14, 1261-1270
33. Bem, D., Smith, H., Banushi, B., Burden, J. J., White, I. J., Hanley, J., Jeremiah, N., Rieux-Laucat, F., Bettels, R., Ariceta, G., Mumford, A. D., Thomas, S. G., Watson, S. P., and Gissen, P. (2015) VPS33B regulates protein sorting into and maturation of α-granule progenitor organelles in mouse megakaryocytes. Blood 126, 133-143
34. Lachmann, J., Glaubke, E., Moore, P. S., and Ungermann, C. (2014) The Vps39-like TRAP1 is an effector of Rab5 and likely the missing Vps3 subunit of human CORVET. Cell. Logist. 4, e970840
35. Graham, S. C., Wartosch, L., Gray, S. R., Scourfield, E. J., Deane, J. E., Luzio, J. P., and Owen, D. J. (2013) Structural basis of Vps33A recruitment to the human HOPS complex by Vps16. Proc. Natl. Acad. Sci. U.S.A. 110, 13345-13350
36. Solinger, J. A., and Spang, A. (2014) Loss of the Sec1/Munc18-family proteins VPS-33.2 and VPS-33.1 bypasses a block in endosome maturation in Caenorhabditis elegans. Mol. Biol. Cell 25, 3909-3925
37. Akbar, M. A., Ray, S., and Krämer, H. (2009) The SM protein Car/Vps33A regulates SNARE-mediated trafficking to lysosomes and lysosome-related organelles. Mol. Biol. Cell 20, 1705-1714
38. Pulipparacharuvil, S., Akbar, M. A., Ray, S., Sevrioukov, E. A., Haberman, A. S., Rohrer, J., and Krämer, H. (2005) Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. J. Cell Sci. 118, 3663-3673
39. Suzuki, T., Oiso, N., Gautam, R., Novak, E. K., Panthier, J.-J., Suprabha, P. G., Vida, T., Swank, R. T., and Spritz, R. A. (2003) The mouse organellar biogenesis mutant buff results from a mutation in Vps33a, a homologue of yeast vps33 and Drosophila carnation. Proc. Natl. Acad. Sci. U.S.A. 100, 1146-1150
40. Lobingier, B. T., and Merz, A. J. (2012) Sec1/Munc18 protein Vps33 binds to SNARE domains and the quaternary SNARE complex. Mol. Biol. Cell 23, 4611-4622
41. Khatter, D., Raina, V. B., Dwivedi, D., Sindhwani, A., Bahl, S., and Sharma, M. (2015) The small GTPase Arl8b regulates assembly of the mammalian HOPS complex to lysosomes. J. Cell Sci. 128, 1746-1761
42. Schindler, C., Chen, Y., Pu, J., Guo, X., and Bonifacino, J. S. (2015) EARP is a multisubunit tethering complex involved in endocytic recycling. Nat. Cell Biol. 17, 639-650
43. Nordmann, M., Cabrera, M., Perz, A., Bröcker, C., Ostrowicz, C., Engelbrecht- Vandré, S., and Ungermann, C. (2010) The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr. Biol. 20, 1654-1659
44. Poteryaev, D., Datta, S., Ackema, K., Zerial, M., and Spang, A. (2010) Identification of the switch in early-to-late endosome transition. Cell 141, 497-508
45. Kinchen, J. M., and Ravichandran, K. S. (2010) Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature 464, 778-782
46. Felici, A., Wurthner, J. U., Parks, W. T., Giam, L. R.-Y., Reiss, M., Karpova, T. S., McNally, J. G., and Roberts, A. B. (2003) TLP, a novel modulator of TGF-β signaling, has opposite effects on Smad2- and Smad3-dependent signaling. EMBO J. 22, 4465-4477
47. Messler, S., Kropp, S., Episkopou, V., Felici, A., Würthner, J., Lemke, R., Jerabek-Willemsen, M., Willecke, R., Scheu, S., Pfeffer, K., and Wurthner, J. U. (2011) The TGF-β signaling modulators TRAP1/TGFBRAP1 and VPS39/Vam6/TLP are essential for early embryonic development. Immunobiology216, 343-350
48. Wurthner, J. U., Frank, D. B., Felici, A., Green, H. M., Cao, Z., Schneider, M. D., McNally, J. G., Lechleider, R. J., and Roberts, A. B. (2001) Transforming growth factor-β receptor-associated protein 1 is a Smad4 chaperone. J. Biol. Chem. 276, 19495-19502