Abstract
The endolysosomal system of eukaryotic cells has a key role in the homeostasis of the plasma membrane, in signaling and nutrient uptake, and is abused by viruses and pathogens for entry. Endocytosis of plasma membrane proteins results in vesicles, which fuse with the early endosome. If destined for lysosomal degradation, these proteins are packaged into intraluminal vesicles, converting an early endosome to a late endosome, which finally fuses with the lysosome. Each of these organelles has a unique membrane surface composition, which can form segmented membrane microcompartments by membrane contact sites or fission proteins. Furthermore, these organelles are in continuous exchange due to fission and fusion events. The underlying machinery, which maintains organelle identity along the pathway, is regulated by signaling processes. Here, we will focus on the Rab5 and Rab7 GTPases of early and late endosomes. As molecular switches, Rabs depend on activating guanine nucleotide exchange factors (GEFs). Over the last years, we characterized the Rab7 GEF, the Mon1-Ccz1 (MC1) complex, and key Rab7 effectors, the HOPS complex and retromer. Structural and functional analyses of these complexes lead to a molecular understanding of their function in the context of organelle biogenesis.
Funding source: Deutsche Forschungsgemeinschaft
Award Identifier / Grant number: SFB 944 - P11
Award Identifier / Grant number: SFB 944 - P17
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Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
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Research funding: This work was funded by DFG (SFB 944, project P11 to C.U., project P17 to D.K.).
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Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Angers, C.G. and Merz, A.J. (2009). HOPS interacts with Apl5 at the vacuole membrane and is required for consumption of AP-3 transport vesicles. Mol. Biol. Cell 20: 4563–4574, https://doi.org/10.1091/mbc.e09-04-0272.Suche in Google Scholar PubMed PubMed Central
Antón, Z., Betin, V.M.S., Simonetti, B., Traer, C.J., Attar, N., Cullen, P.J., and Lane, J.D. (2020). A heterodimeric SNX4–SNX7 SNX-BAR autophagy complex coordinates ATG9A trafficking for efficient autophagosome assembly. J. Cell Sci. 133: jcs246306.10.1101/2020.03.15.990713Suche in Google Scholar
Arlt, H., Reggiori, F., and Ungermann, C. (2015). Retromer and the dynamin Vps1 cooperate in the retrieval of transmembrane proteins from vacuoles. J. Cell Sci. 128: 645–655.10.1242/jcs.132720Suche in Google Scholar PubMed
Asensio, C.S., Sirkis, D.W., Maas, J.W., Egami, K., To, T.-L., Brodsky, F.M., Shu, X., Cheng, Y., and Edwards, R.H. (2013). Self-assembly of VPS41 promotes sorting required for biogenesis of the regulated secretory pathway. Dev. Cell 27: 425–437, https://doi.org/10.1016/j.devcel.2013.10.007.Suche in Google Scholar PubMed PubMed Central
Babst, M. (2020). Regulation of nutrient transporters by metabolic and environmental stresses. Curr. Opin. Cell Biol. 65: 35–41, https://doi.org/10.1016/j.ceb.2020.02.009.Suche in Google Scholar PubMed PubMed Central
Bagde, S.R. and Fromme, J.C. (2022). Structure of a TRAPPII-Rab11 activation intermediate reveals GTPase substrate selection mechanisms. Sci. Adv. 8: eabn7446, https://doi.org/10.1126/sciadv.abn7446.Suche in Google Scholar PubMed PubMed Central
Baker, R.W. and Hughson, F.M. (2016). Chaperoning SNARE assembly and disassembly. Nat. Rev. Mol. Cell Biol. 17: 465–479, https://doi.org/10.1038/nrm.2016.65.Suche in Google Scholar PubMed PubMed Central
Baker, R.W., Jeffrey, P.D., Zick, M., Phillips, B.P., Wickner, W.T., and Hughson, F.M. (2015). A direct role for the Sec1/Munc18-family protein Vps33 as a template for SNARE assembly. Science 349: 1111–1114, https://doi.org/10.1126/science.aac7906.Suche in Google Scholar PubMed PubMed Central
Balla, T. (2013). Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol. Rev. 93: 1019–1137, https://doi.org/10.1152/physrev.00028.2012.Suche in Google Scholar PubMed PubMed Central
Ballabio, A. and Bonifacino, J.S. (2019). Lysosomes as dynamic regulators of cell and organismal homeostasis. Nat. Rev. Mol. Cell Biol. 21: 101–118, https://doi.org/10.1038/s41580-019-0185-4.Suche in Google Scholar PubMed
Barbosa, A.D., Sembongi, H., Su, W.M., Abreu, S., Reggiori, F., Carman, G.M., and Siniossoglou, S. (2015). Lipid partitioning at the nuclear envelope controls membrane biogenesis. Mol. Biol. Cell 26: 3641–3657, https://doi.org/10.1091/mbc.e15-03-0173.Suche in Google Scholar
Barr, F.A. (2013). Rab GTPases and membrane identity: causal or inconsequential? J. Cell Biol. 202: 191–199, https://doi.org/10.1083/jcb.201306010.Suche in Google Scholar PubMed PubMed Central
Battaglioni, S., Benjamin, D., Wälchli, M., Maier, T., and Hall, M.N. (2022). mTOR substrate phosphorylation in growth control. Cell 185: 1814–1836, https://doi.org/10.1016/j.cell.2022.04.013.Suche in Google Scholar PubMed
Bean, B.D.M., Davey, M., Snider, J., Jessulat, M., Deineko, V., Tinney, M., Stagljar, I., Babu, M., and Conibear, E. (2015). Rab5-family guanine nucleotide exchange factors bind retromer and promote its recruitment to endosomes. Mol. Biol. Cell 26: 1119–1128, https://doi.org/10.1091/mbc.e14-08-1281.Suche in Google Scholar
Behrmann, H., Lürick, A., Kuhlee, A., Balderhaar, H.K., Bröcker, C., Kümmel, D., Engelbrecht-Vandré, S., Gohlke, U., Raunser, S., Heinemann, U., et al.. (2014). Structural identification of the Vps18 β-propeller reveals a critical role in the HOPS complex stability and function. J. Biol. Chem. 289: 33503–33512, https://doi.org/10.1074/jbc.m114.602714.Suche in Google Scholar
Bezeljak, U., Loya, H., Kaczmarek, B., Saunders, T.E., and Loose, M. (2020). Stochastic activation and bistability in a Rab GTPase regulatory network. Proc. Natl. Acad. Sci. USA 117: 6540–6549, https://doi.org/10.1073/pnas.1921027117.Suche in Google Scholar PubMed PubMed Central
Bisinski, D.D., Castro, I.G., Mari, M., Walter, S., Fröhlich, F., Schuldiner, M., and Montoro, A.G. (2022). Cvm1 is a component of multiple vacuolar contact sites required for sphingolipid homeostasis. J. Cell Biol. 221: e202103048, https://doi.org/10.1083/jcb.202103048.Suche in Google Scholar PubMed PubMed Central
Borchers, A.-C., Langemeyer, L., and Ungermann, C. (2021). Who’s in control? Principles of Rab GTPase activation in endolysosomal membrane trafficking and beyond. J. Cell Biol. 220: e202105120, https://doi.org/10.1083/jcb.202105120.Suche in Google Scholar PubMed PubMed Central
Bowman, S.L., Le, L., Zhu, Y., Harper, D.C., Sitaram, A., Theos, A.C., Sviderskaya, E.V., Bennett, D.C., Raposo-Benedetti, G., Owen, D.J., et al.. (2021). A BLOC-1–AP-3 super-complex sorts a cis-SNARE complex into endosome-derived tubular transport carriers. J. Cell Biol. 220: e202005173, https://doi.org/10.1083/jcb.202005173.Suche in Google Scholar PubMed PubMed Central
Bridges, D., Ma, J.-T., Park, S., Inoki, K., Weisman, L.S., and Saltiel, A.R. (2012). Phosphatidylinositol 3, 5-bisphosphate plays a role in the activation and subcellular localization of mechanistic target of rapamycin 1. Mol. Biol. Cell 23: 2955–2962, https://doi.org/10.1091/mbc.e11-12-1034.Suche in Google Scholar PubMed PubMed Central
Bröcker, C., Kuhlee, A., Gatsogiannis, C., Balderhaar, H.J.K., 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. USA 109: 1991–1996, https://doi.org/10.1073/pnas.1117797109.Suche in Google Scholar PubMed PubMed Central
Burd, C. and Cullen, P.J. (2014). Retromer: a master conductor of endosome sorting. CSH Persp. Biol. 6: a016774, https://doi.org/10.1101/cshperspect.a016774.Suche in Google Scholar PubMed PubMed Central
Cabrera, M., Langemeyer, L., Mari, M., Rethmeier, R., Orban, I., Perz, A., Bröcker, C., Griffith, J., Klose, D., Steinhoff, H.-J., et al.. (2010). Phosphorylation of a membrane curvature–sensing motif switches function of the HOPS subunit Vps41 in membrane tethering. J. Cell Biol. 191: 845–859, https://doi.org/10.1083/jcb.201004092.Suche in Google Scholar PubMed PubMed Central
Cabrera, M., Nordmann, M., Perz, A., Schmedt, D., Gerondopoulos, A., Barr, F., Piehler, J., Engelbrecht-Vandré, S., and Ungermann, C. (2014). The Mon1–Ccz1 GEF activates the Rab7 GTPase Ypt7 via a longin-fold–Rab interface and association with PI3P-positive membranes. J. Cell Sci. 127: 1043–1051.10.1242/jcs.140921Suche in Google Scholar PubMed PubMed Central
Casler, J.C. and Glick, B.S. (2020). A microscopy-based kinetic analysis of yeast vacuolar protein sorting. Elife 9: e56844, https://doi.org/10.7554/elife.56844.Suche in Google Scholar PubMed PubMed Central
Chen, Z., Malia, P.C., Hatakeyama, R., Nicastro, R., Hu, Z., Péli-Gulli, M.-P., Gao, J., Nishimura, T., Eskes, E., Stefan, C.J., et al.. (2021). TORC1 determines Fab1 lipid kinase function at signaling endosomes and vacuoles. Curr. Biol. 31: 297–309, https://doi.org/10.1016/j.cub.2020.10.026.e8.Suche in Google Scholar PubMed
Chi, R.J., Liu, J., West, M., Wang, J., Odorizzi, G., and Burd, C.G. (2014). Fission of SNX-BAR–coated endosomal retrograde transport carriers is promoted by the dynamin-related protein Vps1. J. Cell Biol. 204: 793–806, https://doi.org/10.1083/jcb.201309084.Suche in Google Scholar PubMed PubMed Central
Christoforidis, S., McBride, H., Burgoyne, R., and Zerial, M. (1999a). The Rab5 effector EEA1 is a core component of endosome docking. Nature 397: 621–625, https://doi.org/10.1038/17618.Suche in Google Scholar PubMed
Christoforidis, S., Miaczynska, M., Ashman, K., Wilm, M., Zhao, L., Yip, S.-C., Waterfield, M.D., Backer, J.M., and Zerial, M. (1999b). Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat. Cell Biol. 1: 249–252, https://doi.org/10.1038/12075.Suche in Google Scholar PubMed
Courtellemont, T., Leo, M.G.D., Gopaldass, N., and Mayer, A. (2022). CROP: a retromer-PROPPIN complex mediating membrane fission in the endo-lysosomal system. EMBO J. 41: e109646, https://doi.org/10.15252/embj.2021109646.Suche in Google Scholar PubMed PubMed Central
Cowles, C.R., Odorizzi, G., Payne, G.S., and Emr, S.D. (1997). The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91: 109–118, https://doi.org/10.1016/s0092-8674(01)80013-1.Suche in Google Scholar PubMed
Cui, Y., Zhao, Q., Gao, C., Ding, Y., Zeng, Y., Ueda, T., Nakano, A., and Jiang, L. (2014). Activation of the Rab7 GTPase by the MON1-CCZ1 complex is essential for PVC-to-vacuole trafficking and plant growth in Arabidopsis. Plant Cell 26: 2080–2097, https://doi.org/10.1105/tpc.114.123141.Suche in Google Scholar PubMed PubMed Central
Cullen, P.J. and Steinberg, F. (2018). To degrade or not to degrade: mechanisms and significance of endocytic recycling. Nat. Rev. Mol. Cell Biol. 19: 679–696, https://doi.org/10.1038/s41580-018-0053-7.Suche in Google Scholar PubMed
D’Agostino, M., Risselada, H.J., Lürick, A., Ungermann, C., and Mayer, A. (2017). A tethering complex drives the terminal stage of SNARE-dependent membrane fusion. Nature 551: 634–638, https://doi.org/10.1038/nature24469.Suche in Google Scholar PubMed
Daniele, T., Hurbain, I., Vago, R., Casari, G., Raposo, G., Tacchetti, C., and Schiaffino, M.V. (2014). Mitochondria and melanosomes establish physical contacts modulated by Mfn2 and involved in organelle biogenesis. Curr. Biol. 24: 393–403, https://doi.org/10.1016/j.cub.2014.01.007.Suche in Google Scholar PubMed
Dawaliby, R. and Mayer, A. (2010). Microautophagy of the nucleus coincides with a vacuolar diffusion barrier at nuclear-vacuolar junctions. Mol. Biol. Cell 21: 4173–4183, https://doi.org/10.1091/mbc.e09-09-0782.Suche in Google Scholar PubMed PubMed Central
Day, K.J., Casler, J.C., and Glick, B.S. (2018). Budding yeast has a minimal endomembrane system. Dev. Cell 44: 56–72, https://doi.org/10.1016/j.devcel.2017.12.014.e4.Suche in Google Scholar PubMed PubMed Central
Dehnen, L., Janz, M., Verma, J.K., Psathaki, O.E., Langemeyer, L., Fröhlich, F., Heinisch, J.J., Meyer, H., Ungermann, C., and Paululat, A. (2020). A trimeric metazoan Rab7 GEF complex is crucial for endocytosis and scavenger function. J. Cell Sci. 133: jcs247080.10.1242/jcs.247080Suche in Google Scholar PubMed
De Renzis, S., Sönnichsen, B., and Zerial, M. (2002). Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nat. Cell Biol. 4: 124–133, https://doi.org/10.1038/ncb744.Suche in Google Scholar PubMed
Doumane, M., Caillaud, M.-C., and Jaillais, Y. (2022). Experimental manipulation of phosphoinositide lipids: from cells to organisms. Trends Cell Biol. 32: 445–461, https://doi.org/10.1016/j.tcb.2022.01.009.Suche in Google Scholar PubMed
Dubouloz, F., Deloche, O., Wanke, V., Cameroni, E., and De Virgilio, C. (2005). The TOR and EGO protein complexes orchestrate microautophagy in yeast. Mol. Cell 19: 15–26, https://doi.org/10.1016/j.molcel.2005.05.020.Suche in Google Scholar PubMed
Eising, S., Esch, B., Wälte, M., Duarte, P.V., Walter, S., Ungermann, C., Bohnert, M., and Fröhlich, F. (2022). A lysosomal biogenesis map reveals the cargo spectrum of yeast vacuolar protein targeting pathways. J. Cell Biol. 221: e202107148, https://doi.org/10.1083/jcb.202107148.Suche in Google Scholar PubMed PubMed Central
Elbaz-Alon, Y., Eisenberg-Bord, M., Shinder, V., Stiller, S.B., Shimoni, E., Wiedemann, N., Geiger, T., and Schuldiner, M. (2015). Lam6 regulates the extent of contacts between organelles. Cell Rep. 12: 7–14, https://doi.org/10.1016/j.celrep.2015.06.022.Suche in Google Scholar PubMed PubMed Central
Elbaz-Alon, Y., Rosenfeld-Gur, E., Shinder, V., Futerman, A.H., Geiger, T., and Schuldiner, M. (2014). A dynamic interface between vacuoles and mitochondria in yeast. Dev. Cell 30: 95–102, https://doi.org/10.1016/j.devcel.2014.06.007.Suche in Google Scholar PubMed
Eltschinger, S. and Loewith, R. (2016). TOR complexes and the maintenance of cellular homeostasis. Trends Cell Biol. 26: 148–159, https://doi.org/10.1016/j.tcb.2015.10.003.Suche in Google Scholar PubMed
Fitzian, K., Brückner, A., Brohée, L., Zech, R., Antoni, C., Kiontke, S., Gasper, R., Matos, A.L.L., Beel, S., Wilhelm, S., et al.. (2021). TSC1 binding to lysosomal PIPs is required for TSC complex translocation and mTORC1 regulation. Mol. Cell 81: 2705–2721, https://doi.org/10.1016/j.molcel.2021.04.019.e8.Suche in Google Scholar PubMed
Franke, C., Repnik, U., Segeletz, S., Brouilly, N., Kalaidzidis, Y., Verbavatz, J., and Zerial, M. (2019). Correlative single-molecule localization microscopy and electron tomography reveals endosome nanoscale domains. Traffic 20: 601–617, https://doi.org/10.1111/tra.12671.Suche in Google Scholar PubMed PubMed Central
Füllbrunn, N., Li, Z., Jorde, L., Richter, C.P., Kurre, R., Langemeyer, L., Yu, C., Meyer, C., Enderlein, J., Ungermann, C., et al.. (2021). Nanoscopic anatomy of dynamic multi-protein complexes at membranes resolved by graphene-induced energy transfer. Elife 10: e62501, https://doi.org/10.7554/elife.62501.Suche in Google Scholar PubMed PubMed Central
Galindo, A., Planelles‐Herrero, V.J., Degliesposti, G., and Munro, S. (2021). Cryo‐EM structure of metazoan TRAPPIII, the multi‐subunit complex that activates the GTPase Rab1. EMBO J. 40: e107608, https://doi.org/10.15252/embj.2020107608.Suche in Google Scholar PubMed PubMed Central
Gan, N., Han, Y., Zeng, W., Wang, Y., Xue, J., and Jiang, Y. (2022). Structural mechanism of allosteric activation of TRPML1 by PI(3, 5)P2 and rapamycin. Proc. Natl. Acad. Sci. USA 119: e2120404119, https://doi.org/10.1073/pnas.2120404119.Suche in Google Scholar PubMed PubMed Central
Gao, J., Langemeyer, L., Kümmel, D., Reggiori, F., and Ungermann, C. (2018). Molecular mechanism to target the endosomal Mon1-Ccz1 GEF complex to the pre-autophagosomal structure. Elife 7: e31145, https://doi.org/10.7554/elife.31145.Suche in Google Scholar PubMed PubMed Central
Gao, J., Nicastro, R., Péli-Gulli, M.-P., Grziwa, S., Chen, Z., Kurre, R., Piehler, J., Virgilio, C.D., Fröhlich, F., and Ungermann, C. (2022). The HOPS tethering complex is required to maintain signaling endosome identity and TORC1 activity. J. Cell Biol. 221: e202109084, https://doi.org/10.1083/jcb.202109084.Suche in Google Scholar PubMed PubMed Central
Gerondopoulos, A., Langemeyer, L., Liang, J.-R., Linford, A., and Barr, F.A. (2012). BLOC-3 mutated in Hermansky-Pudlak syndrome is a Rab32/38 guanine nucleotide exchange factor. Curr. Biol. 22: 2135–2139, https://doi.org/10.1016/j.cub.2012.09.020.Suche in Google Scholar PubMed PubMed Central
Gerondopoulos, A., Strutt, H., Stevenson, N.L., Sobajima, T., Levine, T.P., Stephens, D.J., Strutt, D., and Barr, F.A. (2019). Planar cell polarity effector proteins inturned and fuzzy form a Rab23 GEF complex. Curr. Biol. 29: 3323–3330, https://doi.org/10.1016/j.cub.2019.07.090.e8.Suche in Google Scholar PubMed PubMed Central
Gomez-Navarro, N. and Miller, E.A. (2016). COP-coated vesicles. Curr. Biol. 26: R54–R57, https://doi.org/10.1016/j.cub.2015.12.017.Suche in Google Scholar PubMed
Goody, R.S., Müller, M.P., and Wu, Y.-W. (2017). Mechanisms of action of Rab proteins, key regulators of intracellular vesicular transport. Biol. Chem. 398: 565–575, https://doi.org/10.1515/hsz-2016-0274.Suche in Google Scholar PubMed
Graham, T.R. (2022). AP-3 shows off its flexibility for the cryo-EM camera. J. Biol. Chem. 298: 101491, https://doi.org/10.1016/j.jbc.2021.101491.Suche in Google Scholar PubMed PubMed Central
Gruenberg, J. (2019). Life in the lumen: the multivesicular endosome. Traffic 21: 76–93, https://doi.org/10.1111/tra.12715.Suche in Google Scholar PubMed PubMed Central
Harbour, M.E., Breusegem, S.Y.A., Antrobus, R., Freeman, C., Reid, E., and Seaman, M.N.J. (2010). The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J. Cell Sci. 123: 3703–3717, https://doi.org/10.1242/jcs.071472.Suche in Google Scholar PubMed PubMed Central
Hariri, H., Rogers, S., Ugrankar, R., Liu, Y.L., Feathers, J.R., and Henne, W.M. (2018). Lipid droplet biogenesis is spatially coordinated at ER-vacuole contacts under nutritional stress. EMBO Rep. 19: 57–72, https://doi.org/10.15252/embr.201744815.Suche in Google Scholar PubMed PubMed Central
Hatakeyama, R., Péli-Gulli, M.-P., Hu, Z., Jaquenoud, M., Osuna, G.M.G., Sardu, A., Dengjel, J., and Virgilio, C.D. (2019). Spatially distinct pools of TORC1 balance protein homeostasis. Mol. Cell 73: 325–338, https://doi.org/10.1016/j.molcel.2018.10.040.e8.Suche in Google Scholar PubMed
Hatakeyama, R. and Virgilio, C.D. (2019a). A spatially and functionally distinct pool of TORC1 defines signaling endosomes in yeast. Autophagy 15: 915–916, https://doi.org/10.1080/15548627.2019.1580107.Suche in Google Scholar PubMed PubMed Central
Hatakeyama, R. and Virgilio, C.D. (2019b). TORC1 specifically inhibits microautophagy through ESCRT-0. Curr. Genet. 65: 1243–1249, https://doi.org/10.1007/s00294-019-00982-y.Suche in Google Scholar PubMed PubMed Central
Hayes, M.J., Bryon, K., Satkurunathan, J., and Levine, T.P. (2011). Yeast homologues of three BLOC-1 subunits highlight KxDL proteins as conserved interactors of BLOC-Traffic 1. Traffic 12: 260–268, https://doi.org/10.1111/j.1600-0854.2010.01151.x.Suche in Google Scholar PubMed PubMed Central
Hegedűs, K., Takáts, S., Boda, A., Jipa, A., Nagy, P., Varga, K., Kovács, A.L., and Juhász, G. (2016). The Ccz1-Mon1-Rab7 module and Rab5 control distinct steps of autophagy. Mol. Biol. Cell 27: 3132–3142, https://doi.org/10.1091/mbc.e16-03-0205.Suche in Google Scholar PubMed PubMed Central
Heitman, J., Movva, N., and Hall, M. (1991). Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253: 905–909, https://doi.org/10.1126/science.1715094.Suche in Google Scholar PubMed
Herrmann, E., Langemeyer, L., Auffarth, K., Ungermann, C., and Kümmel, D. (2022). Targeting of the Mon1-Ccz1 Rab guanine nucleotide exchange factor to distinct organelles by a synergistic protein and lipid code. Biorxiv: 2022.08.14.503906.10.1101/2022.08.14.503906Suche in Google Scholar
Holthuis, J.C.M. and Ungermann, C. (2013). Cellular microcompartments constitute general suborganellar functional units in cells. Biol. Chem. 394: 151–161, https://doi.org/10.1515/hsz-2012-0265.Suche in Google Scholar PubMed
Hönscher, C., Mari, M., Auffarth, K., Bohnert, M., Griffith, J., Geerts, W., van der Laan, M., Cabrera, M., Reggiori, F., and Ungermann, C. (2014). Cellular metabolism regulates contact sites between vacuoles and mitochondria. Dev. Cell 30: 86–94, https://doi.org/10.1016/j.devcel.2014.06.006.Suche in Google Scholar PubMed
Hu, Z., Raucci, S., Jaquenoud, M., Hatakeyama, R., Stumpe, M., Rohr, R., Reggiori, F., Virgilio, C.D., and Dengjel, J. (2019). Multilayered control of protein turnover by TORC1 and Atg1. Cell Rep. 28: 3486–3496, https://doi.org/10.1016/j.celrep.2019.08.069.e6.Suche in Google Scholar PubMed
Huotari, J. and Helenius, A. (2011). Endosome maturation. EMBO J. 30: 3481–3500, https://doi.org/10.1038/emboj.2011.286.Suche in Google Scholar PubMed PubMed Central
Hutagalung, A.H. and Novick, P.J. (2011). Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91: 119–149, https://doi.org/10.1152/physrev.00059.2009.Suche in Google Scholar PubMed PubMed Central
Joiner, A.M., Phillips, B.P., Yugandhar, K., Sanford, E.J., Smolka, M.B., Yu, H., Miller, E.A., and Fromme, J.C. (2021). Structural basis of TRAPPIII-mediated Rab1 activation. EMBO J. 40: e107607.10.15252/embj.2020107607Suche in Google Scholar PubMed PubMed Central
Kinchen, J.M. and Ravichandran, K.S. (2010). Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature 464: 778–782, https://doi.org/10.1038/nature08853.Suche in Google Scholar PubMed PubMed Central
Kiontke, S., Langemeyer, L., Kuhlee, A., Schuback, S., Raunser, S., Ungermann, C., and Kümmel, D. (2017). Architecture and mechanism of the late endosomal Rab7-like Ypt7 guanine nucleotide exchange factor complex Mon1–Ccz1. Nat. Commun. 8: 14034, https://doi.org/10.1038/ncomms14034.Suche in Google Scholar PubMed PubMed Central
Klink, B.U., Herrmann, E., Antoni, C., Langemeyer, L., Kiontke, S., Gatsogiannis, C., Ungermann, C., Raunser, S., and Kümmel, D. (2022). Structure of the Mon1-Ccz1 complex reveals molecular basis of membrane binding for Rab7 activation. Proc. Natl. Acad. Sci. USA 119: e2121494119, https://doi.org/10.1073/pnas.2121494119.Suche in Google Scholar PubMed PubMed Central
Klionsky, D.J., Petroni, G., Amaravadi, R.K., Baehrecke, E.H., Ballabio, A., Boya, P., Pedro, J.M.B., Cadwell, K., Cecconi, F., Choi, A.M.K., et al.. (2021). Autophagy in major human diseases. EMBO J. 40: e108863, https://doi.org/10.15252/embj.2021108863.Suche in Google Scholar PubMed PubMed Central
Klumperman, J. and Raposo, G. (2014). The complex ultrastructure of the endolysosomal system. CSH Persp. Biol. 6: a016857, https://doi.org/10.1101/cshperspect.a016857.Suche in Google Scholar PubMed PubMed Central
Krick, R., Muehe, Y., Prick, T., Bremer, S., Schlotterhose, P., Eskelinen, E.-L., Millen, J., Goldfarb, D.S., and Thumm, M. (2008). Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol. Biol. Cell 19: 4492–4505, https://doi.org/10.1091/mbc.e08-04-0363.Suche in Google Scholar PubMed PubMed Central
Kucharczyk, R., Kierzek, A.M., Slonimski, P.P., and Rytka, J. (2001). The Ccz1 protein interacts with Ypt7 GTPase during fusion of multiple transport intermediates with the vacuole in S. cerevisiae. J. Cell Sci. 114: 3137–3145, https://doi.org/10.1242/jcs.114.17.3137.Suche in Google Scholar PubMed
Kumar, N., Leonzino, M., Hancock-Cerutti, W., Horenkamp, F.A., Li, P., Lees, J.A., Wheeler, H., Reinisch, K.M., and De Camilli, P. (2018). VPS13A and VPS13C are lipid transport proteins differentially localized at ER contact sites. J. Cell Biol. 28: 3625–3639.10.1083/jcb.201807019Suche in Google Scholar PubMed PubMed Central
Laage, R. and Ungermann, C. (2001). The N-terminal domain of the t-SNARE Vam3p coordinates priming and docking in yeast vacuole fusion. Mol. Biol. Cell 12: 3375–3385, https://doi.org/10.1091/mbc.12.11.3375.Suche in Google Scholar PubMed PubMed Central
Lachmann, J., Barr, F.A., and Ungermann, C. (2012). The Msb3/Gyp3 GAP controls the activity of the Rab GTPases Vps21 and Ypt7 at endosomes and vacuoles. Mol. Biol. Cell 23: 2516–2526, https://doi.org/10.1091/mbc.e11-12-1030.Suche in Google Scholar PubMed PubMed Central
Langemeyer, L., Borchers, A.-C., Herrmann, E., Füllbrunn, N., Han, Y., Perz, A., Auffarth, K., Kümmel, D., and Ungermann, C. (2020). A conserved and regulated mechanism drives endosomal Rab transition. Elife 9: e56090, https://doi.org/10.7554/elife.56090.Suche in Google Scholar PubMed PubMed Central
Langemeyer, L., Perz, A., Kümmel, D., and Ungermann, C. (2018). A guanine nucleotide exchange factor (GEF) limits Rab GTPase–driven membrane fusion. J. Biol. Chem. 293: 731–739, https://doi.org/10.1074/jbc.m117.812941.Suche in Google Scholar
Langemeyer, L. and Ungermann, C. (2015). BORC and BLOC-1: shared subunits in trafficking complexes. Dev. Cell 33: 121–122, https://doi.org/10.1016/j.devcel.2015.04.008.Suche in Google Scholar PubMed
Lawrence, G., Brown, C.C., Flood, B.A., Karunakaran, S., Cabrera, M., Nordmann, M., Ungermann, C., and Fratti, R.A. (2014). Dynamic association of the PI3P-interacting Mon1-Ccz1 GEF with vacuoles is controlled through its phosphorylation by the type 1 casein kinase Yck3. Mol. Biol. Cell 25: 1608–1619, https://doi.org/10.1091/mbc.e13-08-0460.Suche in Google Scholar PubMed PubMed Central
Lees, J.A., Li, P., Kumar, N., Weisman, L.S., and Reinisch, K.M. (2020). Insights into Lysosomal PI(3, 5)P2 Homeostasis from a structural-biochemical analysis of the PIKfyve lipid kinase complex. Mol. Cell 80: 736–743, https://doi.org/10.1016/j.molcel.2020.10.003.e4.Suche in Google Scholar PubMed PubMed Central
Leray, X., Hilton, J.K., Nwangwu, K., Becerril, A., Mikusevic, V., Fitzgerald, G., Amin, A., Weston, M.R., and Mindell, J.A. (2022). Tonic inhibition of the chloride/proton antiporter ClC-7 by PI(3, 5)P2 is crucial for lysosomal pH maintenance. Elife 11: e74136, https://doi.org/10.7554/elife.74136.Suche in Google Scholar PubMed PubMed Central
Li, Y., Li, B., Liu, L., Chen, H., Zhang, H., Zheng, X., and Zhang, Z. (2015). FgMon1, a guanine nucleotide exchange factor of FgRab7, is important for vacuole fusion, autophagy and plant infection in Fusarium graminearum. Sci. Rep. 5: 18101, https://doi.org/10.1038/srep18101.Suche in Google Scholar PubMed PubMed Central
Lippé, R., Miaczynska, M., Rybin, V., Runge, A., and Zerial, M. (2001). Functional synergy between Rab5 effector Rabaptin-5 and exchange factor Rabex-5 when physically associated in a complex. Mol. Biol. Cell 12: 2219–2228, https://doi.org/10.1091/mbc.12.7.2219.Suche in Google Scholar PubMed PubMed Central
Liu, G.Y. and Sabatini, D.M. (2020). mTOR at the nexus of nutrition, growth, ageing and disease. Nat. Rev. Mol. Cell Biol. 21: 183–203, https://doi.org/10.1038/s41580-019-0199-y.Suche in Google Scholar PubMed PubMed Central
Lürick, A., Gao, J., Kuhlee, A., Yavavli, E., Langemeyer, L., Perz, A., Raunser, S., and Ungermann, C. (2017). Multivalent Rab interactions determine tether-mediated membrane fusion. Mol. Biol. Cell 28: 322–332, https://doi.org/10.1091/mbc.e16-11-0764.Suche in Google Scholar
Lürick, A., Kuhlee, A., Bröcker, C., Kümmel, D., Raunser, S., and Ungermann, C. (2015). The Habc domain of the SNARE Vam3 interacts with the HOPS tethering complex to facilitate vacuole fusion. J. Biol. Chem. 290: 5405–5413, https://doi.org/10.1074/jbc.m114.631465.Suche in Google Scholar PubMed PubMed Central
Ma, M., Burd, C.G., and Chi, R.J. (2016). Distinct complexes of yeast Snx4 family SNX-BARs mediate retrograde trafficking of Snc1 and Atg27. Traffic 18: 134–144, https://doi.org/10.1111/tra.12462.Suche in Google Scholar PubMed PubMed Central
Ma, M., Kumar, S., Purushothaman, L., Babst, M., Ungermann, C., Chi, R.J., and Burd, C.G. (2018). Lipid trafficking by yeast Snx4 family SNX-BAR proteins promotes autophagy and vacuole membrane fusion. Mol. Biol. Cell 29: 2190–2200, https://doi.org/10.1091/mbc.e17-12-0743.Suche in Google Scholar PubMed PubMed Central
Marquardt, L., Taylor, M., Kramer, F., Schmitt, K., Braus, G.H., Valerius, O., and Thumm, M. (2022). Vacuole fragmentation depends on a novel Atg18-containing retromer-complex. Autophagy 15: 1–18, https://doi.org/10.1080/15548627.2022.2072656.Suche in Google Scholar PubMed PubMed Central
Martina, J.A., Moriyama, K., and Bonifacino, J.S. (2003). BLOC-3, a protein complex containing the Hermansky-Pudlak syndrome gene products HPS1 and HPS4. J. Biol. Chem. 278: 29376–29384, https://doi.org/10.1074/jbc.m301294200.Suche in Google Scholar PubMed
McNally, K.E. and Cullen, P.J. (2018). Endosomal retrieval of cargo: retromer is not alone. Trends Cell Biol. 28: 807–822, https://doi.org/10.1016/j.tcb.2018.06.005.Suche in Google Scholar PubMed
Mi, C., Zhang, L., Huang, G., Shao, G., Yang, F., You, X., Dong, M.-Q., Sun, S., and Sui, S.-F. (2022). Structural basis for assembly of TRAPPII complex and specific activation of GTPase Ypt31/32. Sci. Adv. 8: eabi5603, https://doi.org/10.1126/sciadv.abi5603.Suche in Google Scholar PubMed PubMed Central
Michaillat, L., Baars, T.L., and Mayer, A. (2012). Cell-free reconstitution of vacuole membrane fragmentation reveals regulation of vacuole size and number by TORC1. Mol. Biol. Cell 23: 881–895, https://doi.org/10.1091/mbc.e11-08-0703.Suche in Google Scholar
Montoro, A.G., Auffarth, K., Hönscher, C., Bohnert, M., Becker, T., Warscheid, B., Reggiori, F., van der Laan, M., Fröhlich, F., and Ungermann, C. (2018). Vps39 interacts with Tom40 to establish one of two functionally distinct vacuole-mitochondria contact sites. Dev. Cell 45: 621–636, https://doi.org/10.1016/j.devcel.2018.05.011.e7.Suche in Google Scholar PubMed
Montoro, A.G., Duarte, P.V., Auffarth, K., Walter, S., Fröhlich, F., and Ungermann, C. (2021). Subunit exchange among endolysosomal tethering complexes is linked to contact site formation at the vacuole. Mol. Biol. Cell 32: br14, https://doi.org/10.1091/mbc.e21-05-0227.Suche in Google Scholar PubMed PubMed Central
Murley, A., Yamada, J., Niles, B.J., Toulmay, A., Prinz, W.A., Powers, T., and Nunnari, J. (2017). Sterol transporters at membrane contact sites regulate TORC1 and TORC2 signaling. J. Cell Biol. 216: 2679–2689, https://doi.org/10.1083/jcb.201610032.Suche in Google Scholar PubMed PubMed Central
Murray, D.H., Jahnel, M., Lauer, J., Avellaneda, M.J., Brouilly, N., Cezanne, A., Morales-Navarrete, H., Perini, E.D., Ferguson, C., Lupas, A.N., et al.. (2016). An endosomal tether undergoes an entropic collapse to bring vesicles together. Nature 537: 107–111, https://doi.org/10.1038/nature19326.Suche in Google Scholar PubMed PubMed Central
Nicastro, R., Sardu, A., Panchaud, N., and Virgilio, C.D. (2017). The architecture of the Rag GTPase signaling network. Biomolecules 7: 48, https://doi.org/10.3390/biom7030048.Suche in Google Scholar PubMed PubMed Central
Nickerson, D.P., Russell, M.R.G., Lo, S.-Y., Chapin, H.C., Milnes, J.M., and Merz, A.J. (2012). Termination of isoform-selective Vps21/Rab5 signaling at endolysosomal organelles by Msb3/Gyp3. Traffic 13: 1411–1428, https://doi.org/10.1111/j.1600-0854.2012.01390.x.Suche in Google Scholar PubMed PubMed Central
Niwa, S., Tao, L., Lu, S.Y., Liew, G.M., Feng, W., Nachury, M.V., and Shen, K. (2017). BORC regulates the axonal transport of synaptic vesicle precursors by activating ARL-8. Curr. Biol. 27: 2569–2578, https://doi.org/10.1016/j.cub.2017.07.013.e4.Suche in Google Scholar PubMed PubMed Central
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, https://doi.org/10.1016/j.cub.2010.08.002.Suche in Google Scholar PubMed
Norris, A. and Grant, B.D. (2020). Endosomal microdomains: formation and function. Curr. Opin. Cell Biol. 65: 86–95, https://doi.org/10.1016/j.ceb.2020.02.018.Suche in Google Scholar PubMed PubMed Central
Ohya, T., Miaczynska, M., Coskun, Ü., Lommer, B., Runge, A., Drechsel, D., Kalaidzidis, Y., and Zerial, M. (2009). Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes. Nature 459: 1091–1097, https://doi.org/10.1038/nature08107.Suche in Google Scholar PubMed
Pan, X., Roberts, P., Chen, Y., Kvam, E., Shulga, N., Huang, K., Lemmon, S., and Goldfarb, D.S. (2000). Nucleus-vacuole junctions in Saccharomyces cerevisiae are formed through the direct interaction of Vac8p with Nvj1p. Mol. Biol. Cell 11: 2445–2457, https://doi.org/10.1091/mbc.11.7.2445.Suche in Google Scholar PubMed PubMed Central
Penengo, L., Mapelli, M., Murachelli, A.G., Confalonieri, S., Magri, L., Musacchio, A., Fiore, P.P.D., Polo, S., and Schneider, T.R. (2006). Crystal structure of the ubiquitin binding domains of Rabex-5 reveals two modes of interaction with ubiquitin. Cell 124: 1183–1195, https://doi.org/10.1016/j.cell.2006.02.020.Suche in Google Scholar PubMed
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, https://doi.org/10.1111/tra.12232.Suche in Google Scholar PubMed
Peter, A.T.J., Lachmann, J., Rana, M., Bunge, M., Cabrera, M., and Ungermann, C. (2013). The BLOC-1 complex promotes endosomal maturation by recruiting the Rab5 GTPase-activating protein Msb3. J. Cell Biol. 201: 97–111, https://doi.org/10.1083/jcb.201210038.Suche in Google Scholar PubMed PubMed Central
Phillips, M.J. and Voeltz, G.K. (2016). Structure and function of ER membrane contact sites with other organelles. Nat. Rev. Mol. Cell Biol. 17: 69–82, https://doi.org/10.1038/nrm.2015.8.Suche in Google Scholar PubMed PubMed Central
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, https://doi.org/10.1091/mbc.e10-03-0260.Suche in Google Scholar
Podinovskaia, M., Prescianotto-Baschong, C., Buser, D.P., and Spang, A. (2021). A novel live-cell imaging assay reveals regulation of endosome maturation. Elife 10: e70982, https://doi.org/10.7554/elife.70982.Suche in Google Scholar
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: 1361–12, https://doi.org/10.1038/ncomms2360.Suche in Google Scholar PubMed
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, https://doi.org/10.1016/j.cell.2010.03.011.Suche in Google Scholar PubMed
Prag, G., Misra, S., Jones, E.A., Ghirlando, R., Davies, B.A., Horazdovsky, B.F., and Hurley, J.H. (2003). Mechanism of ubiquitin recognition by the CUE domain of Vps9p. Cell 113: 609–620, https://doi.org/10.1016/s0092-8674(03)00364-7.Suche in Google Scholar PubMed
Pu, J., Keren-Kaplan, T., and Bonifacino, J.S. (2017). A Ragulator-BORC interaction controls lysosome positioning in response to amino acid availability. J. Cell Biol. 216: 4183–4197, https://doi.org/10.1083/jcb.201703094.Suche in Google Scholar PubMed PubMed Central
Pu, J., Schindler, C., Jia, R., Jarnik, M., Backlund, P., and Bonifacino, J.S. (2015). BORC, a multisubunit complex that regulates lysosome positioning. Dev. Cell 33: 176–188, https://doi.org/10.1016/j.devcel.2015.02.011.Suche in Google Scholar PubMed PubMed Central
Purushothaman, L.K., Arlt, H., Kuhlee, A., Raunser, S., and Ungermann, C. (2017). Retromer-driven membrane tubulation separates endosomal recycling from Rab7/Ypt7-dependent fusion. Mol. Biol. Cell 28: 783–791, https://doi.org/10.1091/mbc.e16-08-0582.Suche in Google Scholar PubMed PubMed Central
Purushothaman, L.K. and Ungermann, C. (2018). Cargo induces retromer-mediated membrane remodeling on membranes. Mol. Biol. Cell 29: 2709–2719, https://doi.org/10.1091/mbc.e18-06-0339.Suche in Google Scholar PubMed PubMed Central
Raiborg, C., Wenzel, E.M., and Stenmark, H. (2015). ER-endosome contact sites: molecular compositions and functions. EMBO J. 34: 1848–1858, https://doi.org/10.15252/embj.201591481.Suche in Google Scholar PubMed PubMed Central
Ramazanov, B.R., Tran, M.L., and von Blume, J. (2021). Sending out molecules from the TGN. Curr. Opin. Cell Biol. 71: 55–62, https://doi.org/10.1016/j.ceb.2021.02.005.Suche in Google Scholar PubMed PubMed Central
Rana, M., Lachmann, J., and Ungermann, C. (2015). Identification of a Rab GTPase-activating protein cascade that controls recycling of the Rab5 GTPase Vps21 from the vacuole. Mol. Biol. Cell 26: 2535–2549, https://doi.org/10.1091/mbc.e15-02-0062.Suche in Google Scholar PubMed PubMed Central
Rehling, P., Darsow, T., Katzmann, D.J., and Emr, S.D. (1999). Formation of AP-3 transport intermediates requires Vps41 function. Nat. Cell Biol. 1: 346–353, https://doi.org/10.1038/14037.Suche in Google Scholar PubMed
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, https://doi.org/10.1016/j.cell.2005.06.043.Suche in Google Scholar PubMed
Rizo, J. (2022). Molecular mechanisms underlying neurotransmitter release. Annu. Rev. Biophys. 51: 377–408, https://doi.org/10.1146/annurev-biophys-111821-104732.Suche in Google Scholar PubMed PubMed Central
Robinson, J.S., Klionsky, D.J., Banta, L.M., and Emr, S.D. (1988). Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol. Cell Biol. 8: 4936–4948, https://doi.org/10.1128/mcb.8.11.4936-4948.1988.Suche in Google Scholar PubMed PubMed Central
Rojas, R., van Vlijmen, T., Mardones, G.A., Prabhu, Y., Rojas, A.L., Mohammed, S., Heck, A.J.R., Raposo, G., van der Sluijs, P., and Bonifacino, J.S. (2008). Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 183: 513–526, https://doi.org/10.1083/jcb.200804048.Suche in Google Scholar PubMed PubMed Central
Rothman, J.H., Howald, I., and Stevens, T.H. (1989). Characterization of genes required for protein sorting and vacuolar function in the yeast Saccharomyces cerevisiae. EMBO J. 8: 2057–2065, https://doi.org/10.1002/j.1460-2075.1989.tb03614.x.Suche in Google Scholar PubMed PubMed Central
Rowland, A.A., Chitwood, P.J., Phillips, M.J., and Voeltz, G.K. (2014). ER contact sites define the position and timing of endosome fission. Cell 159: 1027–1041, https://doi.org/10.1016/j.cell.2014.10.023.Suche in Google Scholar PubMed PubMed Central
Saftig, P. and Puertollano, R. (2020). How lysosomes sense, integrate, and cope with stress. Trends Biochem. Sci. 46: 97–112, https://doi.org/10.1016/j.tibs.2020.09.004.Suche in Google Scholar PubMed PubMed Central
Sanger, A., Hirst, J., Davies, A.K., and Robinson, M.S. (2019). Adaptor protein complexes and disease at a glance. J. Cell Sci. 132: jcs222992, https://doi.org/10.1242/jcs.222992.Suche in Google Scholar PubMed
Sardana, R. and Emr, S.D. (2021). Membrane protein quality control mechanisms in the endo-lysosome system. Trends Cell Biol. 31: 269–283, https://doi.org/10.1016/j.tcb.2020.11.011.Suche in Google Scholar PubMed
Schoppe, J., Schubert, E., Apelbaum, A., Yavavli, E., Birkholz, O., Stephanowitz, H., Han, Y., Perz, A., Hofnagel, O., Liu, F., et al.. (2021). Flexible open conformation of the AP-3 complex explains its role in cargo recruitment at the Golgi. J. Biol. Chem. 297: 101334, https://doi.org/10.1016/j.jbc.2021.101334.Suche in Google Scholar PubMed PubMed Central
Schoppe, J., Mari, M., Yavavli, E., Auffarth, K., Cabrera, M., Walter, S., Fröhlich, F., and Ungermann, C. (2020). AP-3 vesicle uncoating occurs after HOPS-dependent vacuole tethering. EMBO J. 39: e105117, https://doi.org/10.15252/embj.2020105117.Suche in Google Scholar PubMed PubMed Central
Seaman, M.N.J. (2021). The retromer complex: from genesis to revelations. Trends Biochem. Sci. 46: 608–620, https://doi.org/10.1016/j.tibs.2020.12.009.Suche in Google Scholar PubMed
Shortill, S.P., Frier, M.S., and Conibear, E. (2022). You can go your own way: SNX-BAR coat complexes direct traffic at late endosomes. Curr. Opin. Cell Biol. 76: 102087, https://doi.org/10.1016/j.ceb.2022.102087.Suche in Google Scholar PubMed
Shvarev, D., Schoppe, J., König, C., Perz, A., Füllbrunn, N., Kiontke, S., Langemeyer, L., Januliene, D., Schnelle, K., Kümmel, D., et al.. (2022). Structure of the HOPS tethering complex, a lysosomal membrane fusion machinery. Elife 11: e80901, https://doi.org/10.7554/elife.80901.Suche in Google Scholar PubMed PubMed Central
Simonsen, A., Lippe, R., Christoforidis, S., Gaullier, J.M., Brech, A., Callaghan, J., Toh, B.H., Murphy, C., Zerial, M., and Stenmark, H. (1998). EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394: 494–498, https://doi.org/10.1038/28879.Suche in Google Scholar PubMed
Singh, M.K., Krüger, F., Beckmann, H., Brumm, S., Vermeer, J.E.M., Munnik, T., Mayer, U., Stierhof, Y.-D., Grefen, C., Schumacher, K., et al.. (2014). Protein delivery to vacuole requires SAND protein-dependent Rab GTPase conversion for MVB-vacuole fusion. Curr. Biol. 24: 1383–1389, https://doi.org/10.1016/j.cub.2014.05.005.Suche in Google Scholar PubMed
Skjeldal, F.M., Haugen, L.H., Mateus, D., Frei, D.M., Rødseth, A.V., Hu, X., and Bakke, O. (2021). De novo formation of early endosomes during Rab5 to Rab7 transition. J. Cell Sci. 134: 254185, https://doi.org/10.1242/jcs.254185.Suche in Google Scholar PubMed PubMed Central
Solís, A.G., Berryman, E., and Otegui, M.S. (2022). Plant endosomes as protein sorting hubs. FEBS Lett. 596: 2288–2304, https://doi.org/10.1002/1873-3468.14425.Suche in Google Scholar PubMed
Sönnichsen, B., Renzis, S.D., Nielsen, E., Rietdorf, J., and Zerial, M. (2000). Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149: 901–914, https://doi.org/10.1083/jcb.149.4.901.Suche in Google Scholar PubMed PubMed Central
Stenmark, H., Aasland, R., and Driscoll, P.C. (2002). The phosphatidylinositol 3-phosphate-binding FYVE finger. FEBS Lett. 513: 77–84, https://doi.org/10.1016/s0014-5793(01)03308-7.Suche in Google Scholar PubMed
Stepp, J., Huang, K., and Lemmon, S. (1997). The yeast adaptor protein complex, AP-3, is essential for the efficient delivery of alkaline phosphatase by the alternate pathway to the vacuole. J. Cell Biol. 139: 1761–1774, https://doi.org/10.1083/jcb.139.7.1761.Suche in Google Scholar PubMed PubMed Central
Striepen, J.F. and Voeltz, G.K. (2022). Coronin 1C restricts endosomal branched actin to organize ER contact and endosome fission. J. Cell Biol. 221: e202110089, https://doi.org/10.1083/jcb.202110089.Suche in Google Scholar PubMed PubMed Central
Suzuki, S.W., Oishi, A., Nikulin, N., Jorgensen, J.R., Baile, M.G., and Emr, S.D. (2021). A PX-BAR protein Mvp1/SNX8 and a dynamin-like GTPase Vps1 drive endosomal recycling. Elife 10: e69883, https://doi.org/10.7554/elife.69883.Suche in Google Scholar PubMed PubMed Central
Tall, G., Hama, H., DeWald, D., and Horazdovsky, B. (1999). 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 10: 1873–1889, https://doi.org/10.1091/mbc.10.6.1873.Suche in Google Scholar PubMed PubMed Central
Thomas, L.L. and Fromme, J.C. (2016). GTPase cross talk regulates TRAPPII activation of Rab11 homologues during vesicle biogenesis. J. Cell Biol. 215: 499–513, https://doi.org/10.1083/jcb.201608123.Suche in Google Scholar PubMed PubMed Central
Thomas, L.L., van der Vegt, S.A., and Fromme, J.C. (2019). A steric gating mechanism dictates the substrate specificity of a Rab-GEF. Dev. Cell 48: 100–114, https://doi.org/10.1016/j.devcel.2018.11.013.e9.Suche in Google Scholar PubMed PubMed Central
Tosal-Castano, S., Peselj, C., Kohler, V., Habernig, L., Berglund, L.L., Ebrahimi, M., Vögtle, F.-N., Höög, J., Andréasson, C., and Büttner, S. (2021). Snd3 controls nucleus-vacuole junctions in response to glucose signaling. Cell Rep. 34: 108637, https://doi.org/10.1016/j.celrep.2020.108637.Suche in Google Scholar PubMed
Toshima, J.Y., Nishinoaki, S., Sato, Y., Yamamoto, W., Furukawa, D., Siekhaus, D.E., Sawaguchi, A., and Toshima, J. (2014). Bifurcation of the endocytic pathway into Rab5-dependent and -independent transport to the vacuole. Nat. Commun. 5: 3498, https://doi.org/10.1038/ncomms4498.Suche in Google Scholar PubMed
Tremel, S., Ohashi, Y., Morado, D.R., Bertram, J., Perisic, O., Brandt, L.T.L., von Wrisberg, M.-K., Chen, Z.A., Maslen, S.L., Kovtun, O., et al.. (2021). Structural basis for VPS34 kinase activation by Rab1 and Rab5 on membranes. Nat. Commun. 12: 1564, https://doi.org/10.1038/s41467-021-21695-2.Suche in Google Scholar PubMed PubMed Central
Tsukada, M. and Ohsumi, Y. (1993). Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333: 169–174, https://doi.org/10.1016/0014-5793(93)80398-e.Suche in Google Scholar PubMed
Vaites, L.P., Paulo, J.A., Huttlin, E.L., and Harper, J.W. (2018). Systematic analysis of human cells lacking ATG8 proteins uncovers roles for GABARAPs and the CCZ1/MON1 regulator C18orf8/RMC1 in macroautophagic and selective autophagic flux. Mol. Cell Biol. 38: e00392–e00417, https://doi.org/10.1128/mcb.00392-17.Suche in Google Scholar PubMed PubMed Central
van der Beek, J., Jonker, C., van der Welle, R., Liv, N., and Klumperman, J. (2019). CORVET, CHEVI and HOPS – multisubunit tethers of the endo-lysosomal system in health and disease. J. Cell Sci. 132: jcs189134, https://doi.org/10.1242/jcs.189134.Suche in Google Scholar PubMed
van den Boomen, D.J., Sienkiewicz, A., Berlin, I., Jongsma, M.L.M., van Elsland, D.M., Luzio, J.P., Neefjes, J.J.C., and Lehner, P.J. (2020). A trimeric Rab7 GEF controls NPC1-dependent lysosomal cholesterol export. Nat. Commun. 11: 5559, https://doi.org/10.1038/s41467-020-19032-0.Suche in Google Scholar PubMed PubMed Central
Vietri, M., Radulovic, M., and Stenmark, H. (2020). The many functions of ESCRTs. Nat. Rev. Mol. Cell Biol. 21: 25–42, https://doi.org/10.1038/s41580-019-0177-4.Suche in Google Scholar PubMed
Wandinger-Ness, A. and Zerial, M. (2014). Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harbor Perspect. Biol. 6: a022616, https://doi.org/10.1101/cshperspect.a022616.Suche in Google Scholar PubMed PubMed Central
Wang, C.-W., Stromhaug, P.E., Kauffman, E.J., Weisman, L.S., and Klionsky, D.J. (2003). Yeast homotypic vacuole fusion requires the Ccz1-Mon1 complex during the tethering/docking stage. J. Cell Biol. 163: 973–985, https://doi.org/10.1083/jcb.200308071.Suche in Google Scholar PubMed PubMed Central
Wang, C.-W., Stromhaug, P.E., Shima, J., and Klionsky, D.J. (2002). The Ccz1-Mon1 protein complex is required for the late step of multiple vacuole delivery pathways. J. Biol. Chem. 277: 47917–47927, https://doi.org/10.1074/jbc.m208191200.Suche in Google Scholar PubMed PubMed Central
Wickner, W. and Rizo, J. (2017). A cascade of multiple proteins and lipids catalyzes membrane fusion. Mol. Biol. Cell 28: 707–711, https://doi.org/10.1091/mbc.e16-07-0517.Suche in Google Scholar PubMed PubMed Central
Wong, S., Hepowit, N.L., Port, S.A., Yau, R.G., Peng, Y., Azad, N., Habib, A., Harpaz, N., Schuldiner, M., Hughson, F.M., et al.. (2020). Cargo release from myosin V requires the convergence of parallel pathways that phosphorylate and ubiquitylate the cargo adaptor. Curr. Biol. 30: 4399–4412, https://doi.org/10.1016/j.cub.2020.08.062.e7.Suche in Google Scholar PubMed PubMed Central
Wong, Y.C., Kim, S., Peng, W., and Krainc, D. (2019). Regulation and function of mitochondria–lysosome membrane contact sites in cellular homeostasis. Trends Cell Biol. 29: 500–513, https://doi.org/10.1016/j.tcb.2019.02.004.Suche in Google Scholar PubMed PubMed Central
Wong, Y.C., Ysselstein, D., and Krainc, D. (2018). Mitochondria-lysosome contacts regulate mitochondrial fission via RAB7 GTP hydrolysis. Nature 554: 382–386, https://doi.org/10.1038/nature25486.Suche in Google Scholar PubMed PubMed Central
Wu, H., de Boer, R., Krikken, A.M., Akşit, A., Yuan, W., and van der Klei, I.J. (2019). Peroxisome development in yeast is associated with the formation of Pex3-dependent peroxisome-vacuole contact sites. Biochim. Biophys. Acta Mol. Cell Res. 1866: 349–359, https://doi.org/10.1016/j.bbamcr.2018.08.021.Suche in Google Scholar PubMed
Yan, B.-R., Li, T., Coyaud, E., Laurent, E.M.N., St-Germain, J., Zhou, Y., Kim, P.K., Raught, B., and Brumell, J.H. (2021). C5orf51 is a component of the MON1-CCZ1 complex and controls RAB7A localization and stability during mitophagy. Autophagy 18: 829–840, https://doi.org/10.1080/15548627.2021.1960116.Suche in Google Scholar PubMed PubMed Central
Yang, C. and Wang, X. (2021). Lysosome biogenesis: regulation and functions. J. Cell Biol. 220: e02001, https://doi.org/10.1083/jcb.202102001.Suche in Google Scholar PubMed PubMed Central
Yordanov, T.E., Hipolito, V.E.B., Liebscher, G., Vogel, G.F., Stasyk, T., Herrmann, C., Geley, S., Teis, D., Botelho, R.J., Hess, M.W., et al.. (2019). Biogenesis of lysosome-related organelles complex-1 (BORC) regulates late endosomal/lysosomal size through PIKfyve-dependent phosphatidylinositol-3, 5-bisphosphate. Traffic 20: 674–696.10.1111/tra.12679Suche in Google Scholar PubMed PubMed Central
Zech, R., Kiontke, S., Mueller, U., Oeckinghaus, A., and Kümmel, D. (2016). Structure of the tuberous sclerosis complex 2 (TSC2) N-terminus provides insight into complex assembly and tuberous sclerosis pathogenesis. J. Biol. Chem. 291: 20008–20020, https://doi.org/10.1074/jbc.m116.732446.Suche in Google Scholar
Zhang, Y. and Hughson, F.M. (2021). Chaperoning SNARE folding and assembly. Annu. Rev. Biochem. 90: 581–603, https://doi.org/10.1146/annurev-biochem-081820-103615.Suche in Google Scholar PubMed PubMed Central
Zhao, H., Khan, Z., and Westlake, C.J. (2022). Ciliogenesis membrane dynamics and organization. Semin. Cell Dev. Biol. 133: 20–31, https://doi.org/10.1016/j.semcdb.2022.03.021.Suche in Google Scholar PubMed PubMed Central
© 2022 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Highlight: Physiology and Dynamics of Cellular Microcompartments
- Highlight: on the past and the future of cellular microcompartments
- Nuclear redox processes in land plant development and stress adaptation
- The readily retrievable pool of synaptic vesicles
- Loss of respiratory complex I subunit NDUFB10 affects complex I assembly and supercomplex formation
- Modulation of self-organizing circuits at deforming membranes by intracellular and extracellular factors
- Computational resolution in single molecule localization – impact of noise level and emitter density
- Setting up a data management infrastructure for bioimaging
- Molecular insights into endolysosomal microcompartment formation and maintenance
- The role of lysosomes in lipid homeostasis
- Membrane damage and repair: a thin line between life and death
- Neuronal stress granules as dynamic microcompartments: current concepts and open questions
- Molecular determinants of protein half-life in chloroplasts with focus on the Clp protease system
- Neprilysin 4: an essential peptidase with multifaceted physiological relevance
- Determinants of synergistic cell-cell interactions in bacteria
- Drosophila collagens in specialised extracellular matrices
Artikel in diesem Heft
- Frontmatter
- Highlight: Physiology and Dynamics of Cellular Microcompartments
- Highlight: on the past and the future of cellular microcompartments
- Nuclear redox processes in land plant development and stress adaptation
- The readily retrievable pool of synaptic vesicles
- Loss of respiratory complex I subunit NDUFB10 affects complex I assembly and supercomplex formation
- Modulation of self-organizing circuits at deforming membranes by intracellular and extracellular factors
- Computational resolution in single molecule localization – impact of noise level and emitter density
- Setting up a data management infrastructure for bioimaging
- Molecular insights into endolysosomal microcompartment formation and maintenance
- The role of lysosomes in lipid homeostasis
- Membrane damage and repair: a thin line between life and death
- Neuronal stress granules as dynamic microcompartments: current concepts and open questions
- Molecular determinants of protein half-life in chloroplasts with focus on the Clp protease system
- Neprilysin 4: an essential peptidase with multifaceted physiological relevance
- Determinants of synergistic cell-cell interactions in bacteria
- Drosophila collagens in specialised extracellular matrices