Sorting of cargo in the tubular endosomal network.
Rab proteins
SNAREs
Sec1/Munc18 protein
adaptor proteins
endocytosis
membrane fission
membrane fusion
recycling endosomes
small GTPases
tether
tubular endosomal networks
vesicle transport
Journal
BioEssays : news and reviews in molecular, cellular and developmental biology
ISSN: 1521-1878
Titre abrégé: Bioessays
Pays: United States
ID NLM: 8510851
Informations de publication
Date de publication:
12 2022
12 2022
Historique:
revised:
28
09
2022
received:
11
08
2022
accepted:
29
09
2022
pubmed:
8
11
2022
medline:
29
11
2022
entrez:
7
11
2022
Statut:
ppublish
Résumé
Intercellular communication is an essential process in all multicellular organisms. During this process, molecules secreted by one cell will bind to a receptor on the cognate cell leading to the subsequent uptake of the receptor-ligand complex. Once inside, the cell then determines the fate of the receptor-ligand complex and any other proteins that were endocytosed together. Approximately 80% of endocytosed material is recycled back to the plasma membrane either directly or indirectly via the Golgi apparatus and the remaining 20% is delivered to the lysosome for degradation. Although most pathways have been identified, we still lack understanding on how specificity in sorting of recycling cargos into different pathways is achieved, and how the cell reaches high accuracy of these processes in the absence of clear sorting signals in the bulk of the client proteins. In this review, we will summarize our current understanding of the mechanism behind recycling cargo sorting and propose a model of differential affinities between cargo and cargo receptors/adaptors with regards to iterative sorting in endosomes.
Identifiants
pubmed: 36344475
doi: 10.1002/bies.202200158
doi:
Substances chimiques
Ligands
0
Proteins
0
Types de publication
Review
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2200158Informations de copyright
© 2022 Wiley Periodicals LLC.
Références
Spang, A. (2015). The road not taken: Less traveled roads from the TGN to the plasma membrane. Membranes (Basel), 5, 84-98.
Mayor, S., & Pagano, R. E. (2007). Pathways of clathrin-independent endocytosis. Nature Reviews Molecular Cell Biology, 8, 603-612.
Weinberg, J., & Drubin, D. G. (2012). Clathrin-mediated endocytosis in budding yeast. Trends in Cell Biology, 22, 1-13.
Mettlen, M., Chen, P. H., Srinivasan, S., Danuser, G., & Schmid, S. L. (2018). Regulation of clathrin-mediated endocytosis. Annual Review of Biochemistry, 87, 871-896.
van der Beek, J., de Heus, C., Liv, N., & Klumperman, J. (2022). Quantitative correlative microscopy reveals the ultrastructural distribution of endogenous endosomal proteins. Journal of Cell Biology, 221, e202106044.
Audhya, A., Desai, A., & Oegema, K. (2007). A role for rab5 in structuring the endoplasmic reticulum. Journal of Cell Biology, 178, 43-56.
Serio, G., Margaria, V., Jensen, S., Oldani, A., Bartek, J., Bussolino, F., & Lanzetti, L. (2011). Small GTPase rab5 participates in chromosome congression and regulates localization of the centromere-associated protein CENP-F to kinetochores. Proceedings of the National Academy of Sciences of the United States of America, 108, 17337-17342.
Borchers, A. C., Langemeyer, L., & Ungermann, C. (2021). Who's in control? Principles of rab GTPase activation in endolysosomal membrane trafficking and beyond. Journal of Cell Biology, 220, e202105120.
Guerra, F., & Bucci, C. (2016). Multiple roles of the small GTPase rab7. Cells, 5, 34.
Wilson, J. M., de Hoop, M., Zorzi, N., Toh, B. H., Dotti, C. G., & Parton, R. G. (2000). EEA1, a tethering protein of the early sorting endosome, shows a polarized distribution in hippocampal neurons, epithelial cells, and fibroblasts. Molecular Biology of the Cell, 11, 2657-2671.
Carlton, J., Bujny, M., Peter, B. J., Oorschot, V. M., Rutherford, A., Mellor, H., Klumperman, J., McMahon, H. T., & Cullen, P. J. (2004). Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides. Current Biology, 14, 1791-1800.
Shortill, S. P., Frier, M. S., & Conibear, E. (2022). You can go your own way: SNX-BAR coat complexes direct traffic at late endosomes. Current Opinion in Cell Biology, 76, 102087.
Poteryaev, D., Datta, S., Ackema, K., Zerial, M., & Spang, A. (2010). Identification of the switch in early-to-late endosome transition. Cell, 141, 497-508.
Podinovskaia, M., Prescianotto-Baschong, C., Buser, D. P., & Spang, A. (2021). A novel live-cell imaging assay reveals regulation of endosome maturation. Elife, 10, e70982.
Rahajeng, J., Giridharan, S. S., Cai, B., Naslavsky, N., & Caplan, S. (2010). Important relationships between rab and MICAL proteins in endocytic trafficking. World Journal of Biological Chemistry, 1, 254-264.
Murk, J. L., Posthuma, G., Koster, A. J., Geuze, H. J., Verkleij, A. J., Kleijmeer, M. J., & Humbel, B. M. (2003). Influence of aldehyde fixation on the morphology of endosomes and lysosomes: Quantitative analysis and electron tomography. Journal of Microscopy, 212, 81-90.
Franke, C., Repnik, U., Segeletz, S., Brouilly, N., Kalaidzidis, Y., Verbavatz, J. M., & Zerial, M. (2019). Correlative single-molecule localization microscopy and electron tomography reveals endosome nanoscale domains. Traffic (Copenhagen, Denmark), 20, 601-617.
Solinger, J. A., Rashid, H. O., Prescianotto-Baschong, C., & Spang, A. (2020). FERARI is required for Rab11-dependent endocytic recycling. Nature Cell Biology, 22, 213-224.
Solinger, J. A., Rashid, H. O., & Spang, A. (2022). FERARI and cargo adaptors coordinate cargo flow through sorting endosomes. Nature Communication, 13, 4620.
Klumperman, J., & Raposo, G. (2014). The complex ultrastructure of the endolysosomal system. Cold Spring Harbor Perspectives in Biology, 6, a016857.
Maxfield, F. R., & McGraw, T. E. (2004). Endocytic recycling. Nature Reviews Molecular Cell Biology, 5, 121-132.
Mihov, D., Raja, E., & Spiess, M. (2015). Chondroitin sulfate accelerates trans-Golgi-to-surface transport of proteoglycan amyloid precursor protein. Traffic (Copenhagen, Denmark), 16, 853-870.
Roux, A., Cuvelier, D., Nassoy, P., Prost, J., Bassereau, P., & Goud, B. (2005). Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO Journal, 24, 1537-1545.
Aimon, S., Callan-Jones, A., Berthaud, A., Pinot, M., Toombes, G. E., & Bassereau, P. (2014). Membrane shape modulates transmembrane protein distribution. Developmental Cell, 28, 212-218.
Chi, R. J., Harrison, M. S., & Burd, C. G. (2015). Biogenesis of endosome-derived transport carriers. Cellular and Molecular Life Sciences, 72, 3441-3455.
Cullen, P. J., & Steinberg, F. (2018). To degrade or not to degrade: Mechanisms and significance of endocytic recycling. Nature Reviews Molecular Cell Biology, 19, 679-696.
McNally, K. E., & Cullen, P. J. (2018). Endosomal retrieval of cargo: Retromer is not alone. Trends in Cell Biology, 28, 807-822.
Ritz, A. M., Trautwein, M., Grassinger, F., & Spang, A. (2014). The prion-like domain in the exomer-dependent cargo pin2 serves as a trans-Golgi retention motif. Cell Reports, 7, 249-260.
Xie, S., Bahl, K., Reinecke, J. B., Hammond, G. R., Naslavsky, N., & Caplan, S. (2016). The endocytic recycling compartment maintains cargo segregation acquired upon exit from the sorting endosome. Molecular Biology of the Cell, 27, 108-126.
Simonetti, B., Paul, B., Chaudhari, K., Weeratunga, S., Steinberg, F., Gorla, M., Heesom, K. J., Bashaw, G. J., Collins, B. M., & Cullen, P. J. (2019). Molecular identification of a BAR domain-containing coat complex for endosomal recycling of transmembrane proteins. Nature Cell Biology, 21, 1219-1233.
Pylypenko, O., Lundmark, R., Rasmuson, E., Carlsson, S. R., & Rak, A. (2007). The PX-BAR membrane-remodeling unit of sorting nexin 9. EMBO Journal, 26, 4788-4800.
van Weering, J. R., Sessions, R. B., Traer, C. J., Kloer, D. P., Bhatia, V. K., Stamou, D., Carlsson, S. R., Hurley, J. H., & Cullen, P. J. (2012). Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules. EMBO Journal, 31, 4466-4480.
Stoorvogel, W., Oorschot, V., & Geuze, H. J. (1996). A novel class of clathrin-coated vesicles budding from endosomes. Journal of Cell Biology, 132, 21-33.
Griffiths, G., Back, R., & Marsh, M. (1989). A quantitative analysis of the endocytic pathway in baby hamster kidney cells. Journal of Cell Biology, 109, 2703-2720.
Marsh, M., Griffiths, G., Dean, G. E., Mellman, I., & Helenius, A. (1986). Three-dimensional structure of endosomes in BHK-21 cells. Proceedings of the National Academy of Sciences of the United States of America, 83, 2899-2903.
Nilsson, T., Slusarewicz, P., Hoe, M. H., & Warren, G. (1993). Kin recognition. A model for the retention of golgi enzymes. FEBS Letters, 330, 1-4.
Mellman, I., & Yarden, Y. (2013). Endocytosis and cancer. Cold Spring Harbor Perspectives in Biology, 5, a016949.
Giridharan, S. S., Cai, B., Vitale, N., Naslavsky, N., & Caplan, S. (2013). Cooperation of MICAL-L1, syndapin2, and phosphatidic acid in tubular recycling endosome biogenesis. Molecular Biology of the Cell, 24, 1776-1790.
Farmer, T., Xie, S., Naslavsky, N., Stockli, J., James, D. E., & Caplan, S. (2021). Defining the protein and lipid constituents of tubular recycling endosomes. Journal of Biological Chemistry, 296, 100190.
Gleason, A. M., Nguyen, K. C., Hall, D. H., & Grant, B. D. (2016). Syndapin/SDPN-1 is required for endocytic recycling and endosomal actin association in the c. elegans intestine. Molecular Biology of the Cell, 27, 3746-3756.
Gomez-Navarro, N., & Miller, E. (2016). Protein sorting at the ER-Golgi interface. Journal of Cell Biology, 215, 769-778.
Sandmann, T., Herrmann, J. M., Dengjel, J., Schwarz, H., & Spang, A. (2003). Suppression of coatomer mutants by a new protein family with COPI and COPII binding motifs in saccharomyces cerevisiae. Molecular Biology of the Cell, 14, 3097-3113.
Michelsen, K., Schmid, V., Metz, J., Heusser, K., Liebel, U., Schwede, T., Spang, A., & Schwappach, B. (2007). Novel cargo-binding site in the beta and delta subunits of coatomer. Journal of Cell Biology, 179, 209-217.
Guo, Y., Sirkis, D. W., & Schekman, R. (2014). Protein sorting at the trans-Golgi network. Annual Review of Cell and Developmental Biology, 30, 169-206.
Ma, W., & Goldberg, J. (2013). Rules for the recognition of dilysine retrieval motifs by coatomer. EMBO Journal, 32, 926-937.
Wu, Z., Newstead, S., & Biggin, P. C. (2020). The KDEL trafficking receptor exploits pH to tune the strength of an unusual short hydrogen bond. Science Reports, 10, 16903.
Wilson, D. W., Lewis, M. J., & Pelham, H. R. (1993). pH-dependent binding of KDEL to its receptor in vitro. Journal of Biological Chemistry, 268, 7465-7468.
Eaton, B. E., Gold, L., & Zichi, D. A. (1995). Let's get specific: The relationship between specificity and affinity. Chemistry & Biology, 2, 633-638.
Landry, J. P., Ke, Y., Yu, G. L., & Zhu, X. D. (2015). Measuring affinity constants of 1450 monoclonal antibodies to peptide targets with a microarray-based label-free assay platform. Journal of Immunological Methods, 417, 86-96.
Montecinos-Franjola, F., Schuck, P., & Sackett, D. L. (2016). Tubulin dimer reversible dissociation: AFFINITY, KINETICS, AND DEMONSTRATION OF a STABLE MONOMER. Journal of Biological Chemistry, 291, 9281-9294.
Yong, X., Zhao, L., Deng, W., Sun, H.., Zhou, X., Mao, L., Hu, W., Shen, X., Sun, Q., Billadeau, D. D., Xue, Y., & Jia, D. (2020). Mechanism of cargo recognition by retromer-linked SNX-BAR proteins. Plos Biology, 18, e3000631.
Ghai, R., Mobli, M., Norwood, S. J., Bugarcic, A., Teasdale, R. D., King, G. F., & Collins, B. M. (2011). Phox homology band 4.1/ezrin/radixin/moesin-like proteins function as molecular scaffolds that interact with cargo receptors and ras GTPases. PNAS, 108, 7763-7768.
Ghai, R., Bugarcic, A., Liu, H., Norwood, S. J., Skeldal, S., Coulson, E. J., Li, S. S.-C., Teasdale, R. D., & Collins, B. M. (2013). Structural basis for endosomal trafficking of diverse transmembrane cargos by PX-FERM proteins. PNAS, 110, E643-E652.
McMillan, K. J., Banks, P. J., Hellel, F. L., Carmichael, R. E., Clairfeuille, T., Evans, A. J., Heesom, K. J., Lewis, P., Collins, B. M., Bashir, Z. I., Henley, J. M., Wilkinson, K. A., & Cullen, P. J. (2021). Sorting nexin-27 regulates AMPA receptor trafficking through the synaptic adhesion protein LRFN2. Elife 10.
McMillan, K. J., Gallon, M., Jellett, A. P., Clairfeuille, T., Tilley, F. C., McGough, I., Danson, C. M., Heesom, K. J., Wilkinson, K. A., Collins, B. M., & Cullen, P. J. (2016). Atypical parkinsonism-associated retromer mutant alters endosomal sorting of specific cargo proteins. Journal of Cell Biology, 214, 389-399.
Honing, S., Sosa, M., Hille-Rehfeld, A., & von Figura, K. (1997). The 46-kDa mannose 6-phosphate receptor contains multiple binding sites for clathrin adaptors. Journal of Biological Chemistry, 272, 19884-19890.
Negredo, P. N., Edgar, J. R., Wrobel, A. G., Zaccai, N. R., Antrobus, R., Owen, D. J., & Robinson, M. S. (2017). Contribution of the clathrin adaptor AP-1 subunit micro1 to acidic cluster protein sorting. Journal of Cell Biology, 216, 2927-2943.
Stephens, D. J., Crump, C. M., Clarke, A. R., & Banting, G. (1997). Serine 331 and tyrosine 333 are both involved in the interaction between the cytosolic domain of TGN38 and the mu2 subunit of the AP2 clathrin adaptor complex. Journal of Biological Chemistry, 272, 14104-14109.
Aguilar, R. C., Boehm, M., Gorshkova, I., Crouch, R. J., Tomita, K., Saito, T., Ohno, H., & Bonifacino, J. S. (2001). Signal-binding specificity of the mu4 subunit of the adaptor protein complex AP-4. Journal of Biological Chemistry, 276, 13145-13152.
Ross, B. H., Lin, Y., Corales, E. A., Burgos, P. V., & Mardones, G. A. (2014). Structural and functional characterization of cargo-binding sites on the mu4-subunit of adaptor protein complex 4. Plos One, 9, e88147.
Mayers, J. R., Fyfe, I., Schuh, A. L., Chapman, E. R., Edwardson, J. M., & Audhya, A. (2011). ESCRT-0 assembles as a heterotetrameric complex on membranes and binds multiple ubiquitinylated cargoes simultaneously. Journal of Biological Chemistry, 286, 9636-9645.
Aflatounian, M., Smith, H., Farahani, F., Naeem, A. T., Straatman-Iwanowska, A., Zoghi, S., Khatri, U., Tajdini, P., Fallahi, G. H., Gissen, P., & Rezaei, N. (2016). Novel VIPAS39 mutation in a syndromic patient with arthrogryposis, renal tubular dysfunction and intrahepatic cholestasis. Eur J Med Genet, 59, 237-239.
Ambrosio, A. L., & Di Pietro, S. M. (2019). Mechanism of platelet alpha-granule biogenesis: Study of cargo transport and the VPS33B-VPS16B complex in a model system. Blood Adv, 3, 2617-2626.
Hunter, M. R., Hesketh, G. G., Benedyk, T. H., Gingras, A. C., & Graham, S. C. (2018). Proteomic and biochemical comparison of the cellular interaction partners of human VPS33A and VPS33B. Journal of Molecular Biology, 430, 2153-2163.
Urban, D., Li, L., Christensen, H., Pluthero, F. G., Chen, S. Z., Puhacz, M., Garg, P. M., Lanka, K. K., Cummings, J. J., Kramer, H., Wasmuth, J. D., Parkinson, J., & Kahr, W. H. A. (2012). The VPS33B-binding protein VPS16B is required in megakaryocyte and platelet alpha-granule biogenesis. Blood, 120, 5032-5040.
Gengyo-Ando, K., Kuroyanagi, H., Kobayashi, T., & Murate, M. (2007). The SM protein VPS-45 is required for RAB-5-dependent endocytic transport in caenorhabditis elegans. Embo Reports, 8, 152-157.
Morrison, H. A., Dionne, H., Rusten, T. E., & Brech, A. (2008). Regulation of early endosomal entry by the drosophila tumor suppressors rabenosyn and vps45. Molecular Biology of the Cell, 19, 4167-4176.
Rahajeng, J., Caplan, S., & Naslavsky, N. (2010). Common and distinct roles for the binding partners rabenosyn-5 and vps45 in the regulation of endocytic trafficking in mammalian cells. Experimental Cell Research, 316, 859-874.
Scheidel, N., Kennedy, J., & Blacque, O. E (2018). Endosome maturation factors rabenosyn-5/vps45 and caveolin-1 regulate ciliary membrane and polycystin-2 homeostasis. Embo Journal 37.
Simon-Vecsei, Z., Soth, A., Lorincz, P., & Rubics, A. (2021). Identification of new interactions between endolysosomal tethering factors. Journal of Molecular Biology, 433, 166965.
de Renzis, S., Sonnichsen, B., & Zerial, M. (2002). Divalent rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nature Cell Biology, 4, 124-133.
Jones, T., Naslavsky, N., & Caplan, S. (2020). Eps15 homology domain protein 4 (EHD4) is required for eps15 homology domain protein 1 (EHD1)-mediated endosomal recruitment and fission. Plos One, 15, e0239657.
Kawasaki, A., Sakai, A., Nakanishi, H., & Hasegawa, J. (2022). PI4P/PS countertransport by ORP10 at ER-endosome membrane contact sites regulates endosome fission. Journal of Cell Biology 221.
Cai, B., Caplan, S., & Naslavsky, N. (2012). cPLA2alpha and EHD1 interact and regulate the vesiculation of cholesterol-rich, GPI-anchored, protein-containing endosomes. Molecular Biology of the Cell, 23, 1874-1888.
Dhawan, K., Naslavsky, N., & Caplan, S. (2022). Coronin2A links actin-based endosomal processes to the EHD1 fission machinery. Molecular Biology of the Cell,: mbcE21120624.
Bhattacharyya, S., Rainey, M. A., Arya, P., & Mohapatra, B. C (2016). Endocytic recycling protein EHD1 regulates primary cilia morphogenesis and SHH signaling during neural tube development. Science Reports, 6, 20727.
Woo, J. H., Park, S. J., Park, S. M., & Joe, E. H (2022). Interleukin-6 signaling requires EHD1-mediated alteration of membrane rafts. Febs Journal.
Bennett, V., & Lorenzo, D. N (2013). Spectrin- and ankyrin-based membrane domains and the evolution of vertebrates. Current Topics in Membranes, 72, 1-37.
Qu, F., Lorenzo, D. N., King, S. J., Brooks, R., Bear, J. E., & Bennett, V. (2016). Ankyrin-B is a PI3P effector that promotes polarized alpha5beta1-integrin recycling via recruiting RabGAP1L to early endosomes. Elife, 5, e20417.
Nelson, A. D., & Jenkins, P. M (2017). Axonal membranes and their domains: Assembly and function of the axon initial segment and node of ranvier. Front Cell Neurosci, 11, 136.
Stevens, S. R., & Rasband, M. N (2021). Ankyrins and neurological disease. Current Opinion in Neurobiology, 69, 51-57.
Qin, L., Nie, Y., Zhang, H., & Chen, L. (2020). Identification of new mutations in patients with hereditary spherocytosis by next-generation sequencing. Journal of Human Genetics, 65, 427-434.
Schonteich, E., Wilson, G. M., Burden, J., & Hopkins, C. R (2008). The rip11/rab11-fip5 and kinesin II complex regulates endocytic protein recycling. Journal of Cell Science, 121, 3824-3833.
Li, D., Mangan, A., Cicchini, L., & Margolis, B. (2014). FIP5 phosphorylation during mitosis regulates apical trafficking and lumenogenesis. Embo Reports, 15, 428-437.
Fan, X., Zhou, D., Zhao, B., & Sha, H. (2021). Rab11-FIP1 and rab11-fip5 regulate pIgR/pIgA transcytosis through TRIM21-Mediated polyubiquitination. International Journal of Molecular Sciences, 22, 10466.
Schwenk, R. W., Luiken, J. J., & Eckel, J. (2007). FIP2 and rip11 specify Rab11a-mediated cellular distribution of GLUT4 and FAT/CD36 in H9c2-hIR cells. Biochemical and Biophysical Research Communications, 363, 119-125.
Daumke, O., Lundmark, R., Vallis, Y., Martens, S., Butler, P. J., & McMahon, H. T. (2007). Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature, 449, 923-927.
Pant, S., Sharma, M., Patel, K., Caplan, S., Carr, C. M., & Grant, B. D. (2009). AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nature Cell Biology, 11, 1399-1410.
Deo, R., Kushwah, M. S., Kamerkar, S. C., Kadam, N. Y., Dar, S., Babu, K., Srivastava, A., & Pucadyil, T. J. (2018). ATP-dependent membrane remodeling links EHD1 functions to endocytic recycling. Nature Communication, 9, 5187.
Antonny, B., Burd, C., De Camilli, P., & Chen, E. (2016). Membrane fission by dynamin: What we know and what we need to know. Embo Journal, 35, 2270-2284.
Lawrence, C. M., Ray, S., Babyonyshev, M., & Galluser, R. (1999). Crystal structure of the ectodomain of human transferrin receptor. Science, 286, 779-782.
Gong, X., Qian, H., Cao, P., & Zhao, X. (2018). Structural basis for the recognition of sonic hedgehog by human patched1. Science, 361, eaas8935.
Taylor, M. J., Perrais, D., & Merrifield, C. J. (2011). A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biology, 9, e1000604.
Shnyrova, A. V., Bashkirov, P. V., Akimov, S. A., Pucadyil, T. J., Zimmerberg, J., Schmid, S. L., & Frolov, V. A. (2013). Geometric catalysis of membrane fission driven by flexible dynamin rings. Science, 339, 1433-1436.
Koseoglu, S., Peters, C. G., Fitch-Tewfik, J. L., Aisiku, O., Danglot, L., Galli, T., & Flaumenhaft, R. (2015). VAMP-7 links granule exocytosis to actin reorganization during platelet activation. Blood, 126, 651-660.
Kvainickas, A., Orgaz, A. J., Nagele, H., Diedrich, B., Heesom, K. J., Dengjel, J., Cullen, P. J., & Steinberg, F. (2017). Retromer- and WASH-dependent sorting of nutrient transporters requires a multivalent interaction network with ANKRD50. Journal of Cell Science, 130, 382-395.
Dunn, K. W., McGraw, T. E., & Maxfield, F. R. (1989). Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome. Journal of Cell Biology, 109, 3303-3314.
Rothman, J. E. (1981). The golgi apparatus: Two organelles in tandem. Science, 213, 1212-1219.
Glick, B. S., & Nakano, A. (2009). Membrane traffic within the golgi apparatus. Annual Review of Cell and Developmental Biology, 25, 113-132.
Peplowska, K., Markgraf, D. F., Ostrowicz, C. W., Bange, G., & Ungermann, C. (2007). The CORVET tethering complex interacts with the yeast rab5 homolog vps21 and is involved in endo-lysosomal biogenesis. Developmental Cell, 12, 739-750.
Solinger, J. A., & Spang, A. (2013). Tethering complexes in the endocytic pathway: CORVET and HOPS. FEBS Journal, 280, 2743-2757.
Kinchen, J. M., & Ravichandran, K. S. (2010). Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature, 464, 778-782.