Differences in the endosomal distributions of the two mannose 6- phosphate receptors

doi:10.1083/jcb.121.5.997

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Differences in the endosomal distributions of the two mannose 6- phosphate receptors

J Klumperman, A Hille, T Veenendaal, V Oorschot, W Stoorvogel, K von Figura and HJ Geuze
Department of Cell Biology, Utrecht University, The Netherlands.

Multiple immunolabeling of cryosections was performed to compare the subcellular distributions of the two mannose 6-phosphate receptors (MPRs) involved in the intracellular targeting of lysosomal enzymes: the cation-dependent (CD) and cation-independent (CI) MPR. In two cell types, the human hepatoma cell line HepG2 and BHK cells double transfected with cDNA's encoding for the human CD-MPR and CI-MPR, we found the two receptors at the same sites: the trans-Golgi reticulum (TGR), endosomes, electron-dense cytoplasmic vesicles, and the plasma membrane. In the TGR the two receptors colocalized and were concentrated to the same extent in the same HA I-adaptor positive coated buds and vesicles. Endosomes were identified by the presence of exogenous tracers. The two MPR codistributed to the same endosomes, but semiquantitative analysis showed a relative enrichment of the CI-MPR in endosomes containing many internal vesicles. Two endosomal subcompartments were discerned, the central vacuole and the associated tubules and vesicles (ATV). We found an enrichment of CD-MPR over CI- MPR in the ATV. Lateral segregation of the two receptors within the plane of membranes was also detected on isolated organelles. Double immunolabeling for the CD-MPR and the asialoglycoprotein receptor, which mainly recycles between endosomes and the plasma membrane, revealed that these two receptors were concentrated in different subpopulations of endosomal ATV. The small GTP-binding protein rab4, which has been shown to mediate recycling from endosomes to the plasma membrane, was localized at the cytosolic face of many endosomal ATV. Quantitative analysis of double-immunolabeled cells revealed only a limited codistribution of the MPRs and rab4 in ATV. These data suggest that the two MPRs exit the TGR via the same coated vesicles, but that upon arrival in the endosomes CD-MPR is more rapidly than CI-MPR, segregated into ATV which probably are destined to recycle MPRs to TGR.
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Storch, S., Pohl, S., Braulke, T. (2004). A Dileucine Motif and a Cluster of Acidic Amino Acids in the Second Cytoplasmic Domain of the Batten Disease-related CLN3 Protein Are Required for Efficient Lysosomal Targeting. J. Biol. Chem. 279: 53625-53634 [Abstract] [Full Text]
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Polishchuk, E. V., Di Pentima, A., Luini, A., Polishchuk, R. S. (2003). Mechanism of Constitutive Export from the Golgi: Bulk Flow via the Formation, Protrusion, and En Bloc Cleavage of large trans-Golgi Network Tubular Domains. Mol. Biol. Cell 14: 4470-4485 [Abstract] [Full Text]
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Ghosh, P., Kornfeld, S. (2003). AP-1 binding to sorting signals and release from clathrin-coated vesicles is regulated by phosphorylation. JCB 160: 699-708 [Abstract] [Full Text]
Hinners, I., Tooze, S. A. (2003). Changing directions: clathrin-mediated transport between the Golgi and endosomes. J. Cell Sci. 116: 763-771 [Abstract] [Full Text]
Doray, B., Ghosh, P., Griffith, J., Geuze, H. J., Kornfeld, S. (2002). Cooperation of GGAs and AP-1 in Packaging MPRs at the Trans-Golgi Network. Science 297: 1700-1703 [Abstract] [Full Text]
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Zhou, G., Roizman, B. (2002). Cation-Independent Mannose 6-Phosphate Receptor Blocks Apoptosis Induced by Herpes Simplex Virus 1 Mutants Lacking Glycoprotein D and Is Likely the Target of Antiapoptotic Activity of the Glycoprotein. J. Virol. 76: 6197-6204 [Abstract] [Full Text]
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Hirst, J., Lindsay, M. R., Robinson, M. S. (2001). Golgi-localized, gamma-Ear-containing, ADP-Ribosylation Factor-binding Proteins: Roles of the Different Domains and Comparison with AP-1 and Clathrin. Mol. Biol. Cell 12: 3573-3588 [Abstract] [Full Text]
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Ramm, G., Slot, J. W., James, D. E., Stoorvogel, W. (2000). Insulin Recruits GLUT4 from Specialized VAMP2-carrying Vesicles as well as from the Dynamic Endosomal/Trans-Golgi Network in Rat Adipocytes.. Mol. Biol. Cell 11: 4079-4091 [Abstract] [Full Text]
Sandholzer, U., von Figura, K., Pohlmann, R. (2000). Function and Properties of Chimeric MPR 46-MPR 300 Mannose 6-Phosphate Receptors. J. Biol. Chem. 275: 14132-14138 [Abstract] [Full Text]
Martin, S, Millar, C., Lyttle, C., Meerloo, T, Marsh, B., Gould, G., James, D. (2000). Effects of insulin on intracellular GLUT4 vesicles in adipocytes: evidence for a secretory mode of regulation. J. Cell Sci. 113: 3427-3438 [Abstract]
de Wit, H., Lichtenstein, Y., Geuze, H. J., Kelly, R. B., van der Sluijs, P., Klumperman, J. (1999). Synaptic Vesicles Form by Budding from Tubular Extensions of Sorting Endosomes in PC12 Cells. Mol. Biol. Cell 10: 4163-4176 [Abstract] [Full Text]
Advani, R. J., Yang, B., Prekeris, R., Lee, K. C., Klumperman, J., Scheller, R. H. (1999). Vamp-7 Mediates Vesicular Transport from Endosomes to Lysosomes. JCB 146: 765-776 [Abstract] [Full Text]
Steveson, T. C., Keutmann, H. T., Mains, R. E., Eipper, B. A. (1999). Phosphorylation of Cytosolic Domain Ser937 Affects Both Biosynthetic and Endocytic Trafficking of Peptidylglycine alpha -Amidating Monooxygenase. J. Biol. Chem. 274: 21128-21138 [Abstract] [Full Text]
Steegmaier, M., Klumperman, J., Foletti, D. L., Yoo, J.-S., Scheller, R. H. (1999). Vesicle-associated Membrane Protein 4�is Implicated in Trans-Golgi Network Vesicle Trafficking. Mol. Biol. Cell 10: 1957-1972 [Abstract] [Full Text]
Zhu, Y., Traub, L. M., Kornfeld, S. (1999). High-Affinity Binding Of The AP-1 Adaptor Complex to Trans-Golgi Network Membranes Devoid Of Mannose 6-Phosphate Receptors. Mol. Biol. Cell 10: 537-549 [Abstract] [Full Text]
Dittie, A., Klumperman, J, Tooze, S. (1999). Differential distribution of mannose-6-phosphate receptors and furin in immature secretory granules. J. Cell Sci. 112: 3955-3966 [Abstract]
Pauloin, A, Tooze, S., Michelutti, I, Delpal, S, Ollivier-Bousquet, M (1999). The majority of clathrin coated vesicles from lactating rabbit mammary gland arises from the secretory pathway. J. Cell Sci. 112: 4089-4100 [Abstract]
Breuer, P., Braulke, T. (1998). Stabilization of Mutant 46-kDa Mannose 6-Phosphate Receptors by Proteasomal Inhibitor Lactacystin. J. Biol. Chem. 273: 33254-33258 [Abstract] [Full Text]
Stang, E., Guerra, C. B., Amaya, M., Paterson, Y., Bakke, O., Mellins, E. D. (1998). DR/CLIP (Class II-Associated Invariant Chain Peptides) and DR/Peptide Complexes Colocalize in Prelysosomes in Human B Lymphoblastoid Cells. J. Immunol. 160: 4696-4707 [Abstract] [Full Text]
Klumperman, J., Kuliawat, R., Griffith, J. M., Geuze, H. J., Arvan, P. (1998). Mannose 6-Phosphate Receptors Are Sorted from Immature Secretory Granules via Adaptor Protein AP-1, Clathrin, and Syntaxin 6-positive Vesicles. JCB 141: 359-371 [Abstract] [Full Text]
Press, B., Feng, Y., Hoflack, B., Wandinger-Ness, A. (1998). Mutant Rab7 Causes the Accumulation of Cathepsin D and Cation-independent Mannose 6-Phosphate Receptor in an Early Endocytic Compartment. JCB 140: 1075-1089 [Abstract] [Full Text]
Laurent-Matha, V, Farnoud, M., Lucas, A, Rougeot, C, Garcia, M, Rochefort, H (1998). Endocytosis of pro-cathepsin D into breast cancer cells is mostly independent of mannose-6-phosphate receptors. J. Cell Sci. 111: 2539-2549 [Abstract]
Kleijmeer, M. J., Morkowski, S., Griffith, J. M., Rudensky, A. Y., Geuze, H. J. (1997). Major Histocompatibility Complex Class II Compartments in Human and Mouse B Lymphoblasts Represent Conventional Endocytic Compartments. JCB 139: 639-649 [Abstract] [Full Text]
Itin, C., Rancano, C., Nakajima, Y., Pfeffer, S. R. (1997). A Novel Assay Reveals a Role for Soluble N-Ethylmaleimide-sensitive Fusion Attachment Protein in Mannose 6-Phosphate Receptor Transport from Endosomes to the Trans Golgi Network. J. Biol. Chem. 272: 27737-27744 [Abstract] [Full Text]
Peraus, G. C., Masters, C. L., Beyreuther, K. (1997). Late Compartments of Amyloid Precursor Protein Transport in SY5Y Cells Are Involved in beta -Amyloid Secretion. J. Neurosci. 17: 7714-7724 [Abstract] [Full Text]
Shibata, H., Omata, W., Kojima, I. (1997). Insulin Stimulates Guanine Nucleotide Exchange on Rab4 via a Wortmannin-sensitive Signaling Pathway in Rat Adipocytes. J. Biol. Chem. 272: 14542-14546 [Abstract] [Full Text]
Palokangas, H, Mulari, M, Vaananen, H. (1997). Endocytic pathway from the basal plasma membrane to the ruffled border membrane in bone-resorbing osteoclasts. J. Cell Sci. 110: 1767-1780 [Abstract]
Boker, C, von Figura, K, Hille-Rehfeld, A (1997). The carboxy-terminal peptides of 46 kDa and 300 kDa mannose 6-phosphate receptors share partial sequence homology and contain information for sorting in the early endosomal pathway. J. Cell Sci. 110: 1023-1032 [Abstract]
Seaman, M. N.J., Sowerby, P. J., Robinson, M. S. (1996). Cytosolic and Membrane-associated Proteins Involved in the Recruitment of AP-1 Adaptors onto the Trans-Golgi Network. J. Biol. Chem. 271: 25446-25451 [Abstract] [Full Text]
Shibata, H., Omata, W., Suzuki, Y., Tanaka, S., Kojima, I. (1996). A Synthetic Peptide Corresponding to the Rab4 Hypervariable Carboxyl-terminal Domain Inhibits Insulin Action on Glucose Transport in Rat Adipocytes. J. Biol. Chem. 271: 9704-9709 [Abstract] [Full Text]
Pohlmann, R., Boeker, M. W. C., von Figura, K. (1995). The Two Mannose 6-Phosphate Receptors Transport Distinct Complements of Lysosomal Proteins. J. Biol. Chem. 270: 27311-27318 [Abstract] [Full Text]
Schmidt, B., Kiecke-Siemsen, C., Waheed, A., Braulke, T., Figura, K. v. (1995). Localization of the Insulin-like Growth Factor II Binding Site to Amino Acids 1508-1566 in Repeat 11 of the Mannose 6-Phosphate/Insulin-like Growth Factor II Receptor. J. Biol. Chem. 270: 14975-14982 [Abstract] [Full Text]
Griffiths, G, Pepperkok, R, Locker, J., Kreis, T. (1995). Immunocytochemical localization of beta-COP to the ER-Golgi boundary and the TGN. J. Cell Sci. 108: 2839-2856 [Abstract]
Rabouille, C, Hui, N, Hunte, F, Kieckbusch, R, Berger, E., Warren, G, Nilsson, T (1995). Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J. Cell Sci. 108: 1617-1627 [Abstract]
Conibear, E, Pearse, B. (1994). A chimera of the cytoplasmic tail of the mannose 6-phosphate/IGF-II receptor and lysozyme localizes to the TGN rather than prelysosomes where the bulk of the endogenous receptor is found. J. Cell Sci. 107: 923-932 [Abstract]
Schweizer, A., Stahl, P. D., Rohrer, J. (2000). A Di-aromatic Motif in the Cytosolic Tail of the Mannose Receptor Mediates Endosomal Sorting. J. Biol. Chem. 275: 29694-29700 [Abstract] [Full Text]
Barbero, P., Bittova, L., Pfeffer, S. R. (2002). Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. JCB 156: 511-518 [Abstract] [Full Text]
Sachse, M., Urbe, S., Oorschot, V., Strous, G. J., Klumperman, J. (2002). Bilayered Clathrin Coats on Endosomal Vacuoles Are Involved in Protein Sorting toward Lysosomes. Mol. Biol. Cell 13: 1313-1328 [Abstract] [Full Text]