Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis

doi:10.1083/jcb.115.1.151

Quantitative Colocalization Analysis Software

This Article

	Full Text (PDF, 1824K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Cameron, P. L.
	Articles by De Camilli, P.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Cameron, P. L.
	Articles by De Camilli, P.


Social Bookmarking

	What's this?

ARTICLES

Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis

PL Cameron, TC Sudhof, R Jahn and P De Camilli
Department of Cell Biology, Yale University School of Medicine, New Haven, Connecticut 06510.

We have reported previously that the synaptic vesicle (SV) protein synaptophysin, when expressed in fibroblastic CHO cells, accumulates in a population of recycling microvesicles. Based on preliminary immunofluorescence observations, we had suggested that synaptophysin is targeted to the preexisting population of microvesicles that recycle transferrin (Johnston, P. A., P. L. Cameron, H. Stukenbrok, R. Jahn, P. De Camilli, and T. C. Sudhof. 1989. EMBO (Eur. Mol. Biol. Organ.) J. 8:2863-2872). In contrast to our results, another group reported that expression of synaptophysin in cells which normally do not express SV proteins results in the generation of a novel population of microvesicles (Leube, R. E., B. Wiedenmann, and W. W. Franke. 1989. Cell. 59:433-446). We report here a series of morphological and biochemical studies conclusively demonstrating that synaptophysin and transferrin receptors are indeed colocalized on the same vesicles in transfected CHO cells. These observations prompted us to investigate whether an overlap between the distribution of the two proteins also occurs in endocrine cell lines that endogenously express synaptophysin and other SV proteins. We have found that endocrine cell lines contain two pools of membranes positive for synaptophysin and other SV proteins. One of the two pools also contains transferrin receptors and migrates faster during velocity centrifugation. The other pool is devoid of transferrin receptors and corresponds to vesicles with the same sedimentation characteristics as SVs. These findings suggest that in transfected CHO cells and in endocrine cell lines, synaptophysin follows the same endocytic pathway as transferrin receptors but that in endocrine cells, at some point along this pathway, synaptophysin is sorted away from the recycling receptors into a specialized vesicle population. Finally, using immunofluorescent analyses, we found an overlap between the distribution of synaptophysin and transferrin receptors in the dendrites of hippocampal neurons in primary cultures before synapse formation. Axons were enriched in synaptophysin immunoreactivity but did not contain detectable levels of transferrin receptor immunoreactivity. These results suggest that SVs may have evolved from, as well as coexist with, a constitutively recycling vesicular organelle found in all cells.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Bakirtzi, K., Belfort, G., Lopez-Coviella, I., Kuruppu, D., Cao, L., Abel, E. D., Brownell, A.-L., Kandror, K. V. (2009). Cerebellar Neurons Possess a Vesicular Compartment Structurally and Functionally Similar to Glut4-Storage Vesicles from Peripheral Insulin-Sensitive Tissues. J. Neurosci. 29: 5193-5201 [Abstract] [Full Text]
Maritzen, T., Keating, D. J., Neagoe, I., Zdebik, A. A., Jentsch, T. J. (2008). Role of the Vesicular Chloride Transporter ClC-3 in Neuroendocrine Tissue. J. Neurosci. 28: 10587-10598 [Abstract] [Full Text]
Liang, Y.-J., Wu, D.-F., Yang, L.-Q., Hollt, V., Koch, T. (2007). Interaction of the {micro}-Opioid Receptor with Synaptophysin Influences Receptor Trafficking and Signaling. Mol. Pharmacol. 71: 123-131 [Abstract] [Full Text]
Liu, T.-T., Kishimoto, T., Hatakeyama, H., Nemoto, T., Takahashi, N., Kasai, H. (2005). Exocytosis and endocytosis of small vesicles in PC12 cells studied with TEPIQ (two-photon extracellular polar-tracer imaging-based quantification) analysis. J. Physiol. 568: 917-929 [Abstract] [Full Text]
Salazar, G., Craige, B., Wainer, B. H., Guo, J., De Camilli, P., Faundez, V. (2005). Phosphatidylinositol-4-Kinase Type II {alpha} Is a Component of Adaptor Protein-3-derived Vesicles. Mol. Biol. Cell 16: 3692-3704 [Abstract] [Full Text]
Bundesen, L. (2004). Inaugural Article: Biography of Pietro De Camilli. Proc. Natl. Acad. Sci. USA 101: 8259-8261 [Full Text]
Pennuto, M., Bonanomi, D., Benfenati, F., Valtorta, F. (2003). Synaptophysin I Controls the Targeting of VAMP2/Synaptobrevin II to Synaptic Vesicles. Mol. Biol. Cell 14: 4909-4919 [Abstract] [Full Text]
Belfort, G. M., Kandror, K. V. (2003). Cellugyrin and Synaptogyrin Facilitate Targeting of Synaptophysin to a Ubiquitous Synaptic Vesicle-sized Compartment in PC12 Cells. J. Biol. Chem. 278: 47971-47978 [Abstract] [Full Text]
Spitzenberger, F., Pietropaolo, S., Verkade, P., Habermann, B., Lacas-Gervais, S., Mziaut, H., Pietropaolo, M., Solimena, M. (2003). Islet Cell Autoantigen of 69 kDa Is an Arfaptin-related Protein Associated with the Golgi Complex of Insulinoma INS-1 Cells. J. Biol. Chem. 278: 26166-26173 [Abstract] [Full Text]
Guo, J., Wenk, M. R., Pellegrini, L., Onofri, F., Benfenati, F., De Camilli, P. (2003). Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc. Natl. Acad. Sci. USA 100: 3995-4000 [Abstract] [Full Text]
Coco, S., Calegari, F., Pravettoni, E., Pozzi, D., Taverna, E., Rosa, P., Matteoli, M., Verderio, C. (2003). Storage and Release of ATP from Astrocytes in Culture. J. Biol. Chem. 278: 1354-1362 [Abstract] [Full Text]
Szaszi, K., Paulsen, A., Szabo, E. Z., Numata, M., Grinstein, S., Orlowski, J. (2002). Clathrin-mediated Endocytosis and Recycling of the Neuron-specific Na+/H+ Exchanger NHE5 Isoform. REGULATION BY PHOSPHATIDYLINOSITOL 3'-KINASE AND THE ACTIN CYTOSKELETON. J. Biol. Chem. 277: 42623-42632 [Abstract] [Full Text]
Koizumi, S., Rosa, P., Willars, G. B., Challiss, R. A. J., Taverna, E., Francolini, M., Bootman, M. D., Lipp, P., Inoue, K., Roder, J., Jeromin, A. (2002). Mechanisms Underlying the Neuronal Calcium Sensor-1-evoked Enhancement of Exocytosis in PC12 Cells. J. Biol. Chem. 277: 30315-30324 [Abstract] [Full Text]
Reinhardt, J., Kosch, M., Lerner, M., Bertram, H., Lemke, D., Oberleithner, H. (2002). Stimulation of protein kinase C pathway mediates endocytosis of human nongastric H+-K+-ATPase, ATP1AL1. Am. J. Physiol. Renal Physiol. 283: F335-F343 [Abstract] [Full Text]
Li, Y., Chin, L.-S., Levey, A. I., Li, L. (2002). Huntingtin-associated Protein 1 Interacts with Hepatocyte Growth Factor-regulated Tyrosine Kinase Substrate and Functions in Endosomal Trafficking. J. Biol. Chem. 277: 28212-28221 [Abstract] [Full Text]
Wheeler, T. C., Chin, L.-S., Li, Y., Roudabush, F. L., Li, L. (2002). Regulation of Synaptophysin Degradation by Mammalian Homologues of Seven in Absentia. J. Biol. Chem. 277: 10273-10282 [Abstract] [Full Text]
Patel, K. G., Liu, C., Cameron, P. L., Cameron, R. S. (2001). Myr 8, A Novel Unconventional Myosin Expressed during Brain Development Associates with the Protein Phosphatase Catalytic Subunits 1{alpha} and 1{gamma}1. J. Neurosci. 21: 7954-7968 [Abstract] [Full Text]
Berghs, S., Ferracci, F., Maksimova, E., Gleason, S., Leszczynski, N., Butler, M., De Camilli, P., Solimena, M. (2001). Autoimmunity to beta IV spectrin in paraneoplastic lower motor neuron syndrome. Proc. Natl. Acad. Sci. USA 98: 6945-6950 [Abstract] [Full Text]
Tam, B. M., Moritz, O. L., Hurd, L. B., Papermaster, D. S. (2000). Identification of an Outer Segment Targeting Signal in the Cooh Terminus of Rhodopsin Using Transgenic Xenopus laevis. JCB 151: 1369-1380 [Abstract] [Full Text]
ERICKSON, J. D., VAROQUI, H. (2000). Molecular analysis of vesicular amine transporter function and targeting to secretory organelles. FASEB J. 14: 2450-2458 [Abstract] [Full Text]
Berghs, S., Aggujaro, D., Dirkx, R. Jr., Maksimova, E., Stabach, P., Hermel, J.-M., Zhang, J.-P., Philbrick, W., Slepnev, V., Ort, T., Solimena, M. (2000). {beta}iv Spectrin, a New Spectrin Localized at Axon Initial Segments and Nodes of Ranvier in the Central and Peripheral Nervous System. JCB 151: 985-1002 [Abstract] [Full Text]
Roth, J. A., Horbinski, C., Feng, L., Dolan, K. G., Higgins, D., Garrick, M. D. (2000). Differential Localization of Divalent Metal Transporter 1 with and without Iron Response Element in Rat PC12 and Sympathetic Neuronal Cells. J. Neurosci. 20: 7595-7601 [Abstract] [Full Text]
Reinhardt, J., Grishin, A. V., Oberleithner, H., Caplan, M. J. (2000). Differential localization of human nongastric H+-K+-ATPase ATP1AL1 in polarized renal epithelial cells. Am. J. Physiol. Renal Physiol. 279: F417-F425 [Abstract] [Full Text]
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. Mol. Biol. Cell 11: 2657-2671 [Abstract] [Full Text]
Ochoa, G.-C., Slepnev, V. I., Neff, L., Ringstad, N., Takei, K., Daniell, L., Kim, W., Cao, H., McNiven, M., Baron, R., De Camilli, P. (2000). A Functional Link between Dynamin and the Actin Cytoskeleton at Podosomes. JCB 150: 377-390 [Abstract] [Full Text]
Krantz, D. E., Waites, C., Oorschot, V., Liu, Y., Wilson, R. I., Tan, P. K., Klumperman, J., Edwards, R. H. (2000). A Phosphorylation Site Regulates Sorting of the Vesicular Acetylcholine Transporter to Dense Core Vesicles. JCB 149: 379-396 [Abstract] [Full Text]
Dunbar, L. A., Aronson, P., Caplan, M. J. (2000). A Transmembrane Segment Determines the Steady-State Localization of an Ion-Transporting Adenosine Triphosphatase. JCB 148: 769-778 [Abstract] [Full Text]
Chin, L.-S., Nugent, R. D., Raynor, M. C., Vavalle, J. P., Li, L. (2000). SNIP, a Novel SNAP-25-interacting Protein Implicated in Regulated Exocytosis. J. Biol. Chem. 275: 1191-1200 [Abstract] [Full Text]
Kwong, J, Roundabush, F., Hutton Moore, P, Montague, M, Oldham, W, Li, Y, Chin, L., Li, L (2000). Hrs interacts with SNAP-25 and regulates Ca(2+)-dependent exocytosis. J. Cell Sci. 113: 2273-2284 [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]
Rosenthal, J. A., Chen, H., Slepnev, V. I., Pellegrini, L., Salcini, A. E., Di Fiore, P. P., De Camilli, P. (1999). The Epsins Define a Family of Proteins That Interact with Components of the Clathrin Coat and Contain a New Protein Module. J. Biol. Chem. 274: 33959-33965 [Abstract] [Full Text]
Blagoveshchenskaya, A. D., Hewitt, E. W., Cutler, D. F. (1999). Di-Leucine Signals Mediate Targeting of Tyrosinase and Synaptotagmin to Synaptic-like Microvesicles within PC12 Cells. Mol. Biol. Cell 10: 3979-3990 [Abstract] [Full Text]
Holroyd, C., Kistner, U., Annaert, W., Jahn, R. (1999). Fusion of Endosomes Involved in Synaptic Vesicle Recycling. Mol. Biol. Cell 10: 3035-3044 [Abstract] [Full Text]
Zuk, P. A., Elferink, L. A. (1999). Rab15 Mediates an Early Endocytic Event in Chinese Hamster Ovary Cells. J. Biol. Chem. 274: 22303-22312 [Abstract] [Full Text]
Calegari, F., Coco, S., Taverna, E., Bassetti, M., Verderio, C., Corradi, N., Matteoli, M., Rosa, P. (1999). A Regulated Secretory Pathway in Cultured Hippocampal Astrocytes. J. Biol. Chem. 274: 22539-22547 [Abstract] [Full Text]
Strasser, J. E., Arribas, M., Blagoveshchenskaya, A. D., Cutler, D. F. (1999). Secretagogue-triggered Transfer of Membrane Proteins from Neuroendocrine Secretory Granules to Synaptic-like Microvesicles. Mol. Biol. Cell 10: 2619-2630 [Abstract] [Full Text]
Vickery, R. G., von Zastrow, M. (1999). Distinct Dynamin-dependent and -independent Mechanisms Target Structurally Homologous Dopamine Receptors to Different Endocytic Membranes. JCB 144: 31-43 [Abstract] [Full Text]
Steegmaier, M., Yang, B., Yoo, J.-S., Huang, B., Shen, M., Yu, S., Luo, Y., Scheller, R. H. (1998). Three Novel Proteins of the Syntaxin/SNAP-25 Family. J. Biol. Chem. 273: 34171-34179 [Abstract] [Full Text]
Gibson, A., Futter, C.E., Maxwell, S., Allchin, E.H., Shipman, M., Kraehenbuhl, J.-P., Domingo, D., Odorizzi, G., Trowbridge, I.S., Hopkins, C.R. (1998). Sorting Mechanisms Regulating Membrane Protein Traffic in the Apical Transcytotic Pathway of Polarized MDCK Cells. JCB 143: 81-94 [Abstract] [Full Text]
Molloy, S. S., Thomas, L., Kamibayashi, C., Mumby, M. C., Thomas, G. (1998). Regulation of Endosome Sorting by a Specific PP2A Isoform. JCB 142: 1399-1411 [Abstract] [Full Text]
Cao, T. T., Mays, R. W., von Zastrow, M. (1998). Regulated Endocytosis of G-protein-coupled Receptors by a Biochemically and Functionally Distinct Subpopulation of Clathrin-coated Pits. J. Biol. Chem. 273: 24592-24602 [Abstract] [Full Text]
Lichtenstein, Y., Desnos, C., Faundez, V., Kelly, R. B., Clift-O'Grady, L. (1998). Vesiculation and sorting from PC12-derived endosomes in vitro. Proc. Natl. Acad. Sci. USA 95: 11223-11228 [Abstract] [Full Text]
Jarousse, N., Syan, S., Martinat, C., Brahic, M. (1998). The Neurovirulence of the DA and GDVII Strains of Theiler's Virus Correlates with Their Ability To Infect Cultured Neurons. J. Virol. 72: 7213-7220 [Abstract] [Full Text]
Varoqui, H., Erickson, J. D. (1998). The Cytoplasmic Tail of the Vesicular Acetylcholine Transporter Contains a Synaptic Vesicle Targeting Signal. J. Biol. Chem. 273: 9094-9098 [Abstract] [Full Text]
Weclewicz, K., Ekstrom, M., Kristensson, K., Garoff, H. (1998). Specific Interactions between Retrovirus Env and Gag Proteins in Rat Neurons. J. Virol. 72: 2832-2845 [Abstract] [Full Text]
Muth, T. R., Gottardi, C. J., Roush, D. L., Caplan, M. J. (1998). A basolateral sorting signal is encoded in the alpha -subunit of Na-K-ATPase. Am. J. Physiol. Cell Physiol. 274: C688-C696 [Abstract] [Full Text]
Nakata, T., Terada, S., Hirokawa, N. (1998). Visualization of the Dynamics of Synaptic Vesicle and Plasma Membrane Proteins in Living Axons. JCB 140: 659-674 [Abstract] [Full Text]
Mundigl, O., Ochoa, G.-C., David, C., Slepnev, V. I., Kabanov, A., De Camilli, P. (1998). Amphiphysin I Antisense Oligonucleotides Inhibit Neurite Outgrowth in Cultured Hippocampal Neurons. J. Neurosci. 18: 93-103 [Abstract] [Full Text]
Cameron, P. L., Ruffin, J. W., Bollag, R., Rasmussen, H., Cameron, R. S. (1997). Identification of Caveolin and Caveolin-Related Proteins in the Brain. J. Neurosci. 17: 9520-9535 [Abstract] [Full Text]
Hemar, A., Olivo, J.-C., Williamson, E., Saffrich, R., Dotti, C. G. (1997). Dendroaxonal Transcytosis of Transferrin in Cultured Hippocampal and Sympathetic Neurons. J. Neurosci. 17: 9026-9034 [Abstract] [Full Text]
Liu, Y., Edwards, R. H. (1997). Differential Localization of Vesicular Acetylcholine and Monoamine Transporters in PC12 Cells but Not CHO Cells. JCB 139: 907-916 [Abstract] [Full Text]
West, A. E., Neve, R. L., Buckley, K. M. (1997). Targeting of the Synaptic Vesicle Protein Synaptobrevin in the Axon of Cultured Hippocampal Neurons: Evidence for Two Distinct Sorting Steps. JCB 139: 917-927 [Abstract] [Full Text]
Grimes, M. L., Beattie, E., Mobley, W. C. (1997). A signaling organelle containing the nerve growth factor-activated receptor tyrosine kinase, TrkA. Proc. Natl. Acad. Sci. USA 94: 9909-9914 [Abstract] [Full Text]
West, A. E., Neve, R. L., Buckley, K. M. (1997). Identification of a Somatodendritic Targeting Signal in the Cytoplasmic Domain of the Transferrin Receptor. J. Neurosci. 17: 6038-6047 [Abstract] [Full Text]
Schmidt, A., Hannah, M. J., Huttner, W. B. (1997). Synaptic-like Microvesicles of Neuroendocrine Cells Originate from a Novel Compartment That Is Continuous with the Plasma Membrane and Devoid of Transferrin Receptor. JCB 137: 445-458 [Abstract] [Full Text]
Perego, C., Bulbarelli, A., Longhi, R., Caimi, M., Villa, A., Caplan, M. J., Pietrini, G. (1997). Sorting of Two Polytopic Proteins, the gamma -Aminobutyric Acid and Betaine Transporters, in Polarized Epithelial Cells. J. Biol. Chem. 272: 6584-6592 [Abstract] [Full Text]
Wilson, J. M., Colton, T. L. (1997). Targeting of an Intestinal Apical Endosomal Protein to Endosomes in Nonpolarized Cells. JCB 136: 319-330 [Abstract] [Full Text]
Marquez-Sterling, N. R., Lo, A. C.�Y., Sisodia, S. S., Koo, E. H. (1997). Trafficking of Cell-Surface beta -Amyloid Precursor Protein: Evidence that a Sorting Intermediate Participates in Synaptic Vesicle Recycling. J. Neurosci. 17: 140-151 [Abstract] [Full Text]
Bult, A., Zhao, F., Dirkx Jr., R., Sharma, E., Lukacsi, E., Solimena, M., Naegele, J. R., Lombroso, P. J. (1996). STEP61: A Member of a Family of Brain-Enriched PTPs Is Localized to the Endoplasmic Reticulum. J. Neurosci. 16: 7821-7831 [Abstract] [Full Text]
Ikin, A. F., Annaert, W. G., Takei, K., De Camilli, P., Jahn, R., Greengard, P., Buxbaum, J. D. (1996). Alzheimer Amyloid Protein Precursor Is Localized in Nerve Terminal Preparations to Rab5-containing Vesicular Organelles Distinct from Those Implicated in the Synaptic Vesicle Pathway. J. Biol. Chem. 271: 31783-31786 [Abstract] [Full Text]
Gillen, C. M., Brill, S., Payne, J. A., Forbush, B. III (1996). Molecular Cloning and Functional Expression of the K-Cl Cotransporter from Rabbit, Rat, and Human. A NEW MEMBER OF THE CATION-CHLORIDE COTRANSPORTER FAMILY. J. Biol. Chem. 271: 16237-16244 [Abstract] [Full Text]
Ahn, J., Mundigl, O., Muth, T. R., Rudnick, G., Caplan, M. J. (1996). Polarized Expression of GABA Transporters in Madin-Darby Canine Kidney Cells and Cultured Hippocampal Neurons. J. Biol. Chem. 271: 6917-6924 [Abstract] [Full Text]
Chang, S., Hemmings, H. C. Jr., Aderem, A. (1996). Stimulus-dependent Phosphorylation of MacMARCKS, a Protein Kinase C Substrate, in Nerve Termini and PC12 Cells. J. Biol. Chem. 271: 1174-1178 [Abstract] [Full Text]
Sofer, A, Schwarzmann, G, Futerman, A. (1996). The internalization of a short acyl chain analogue of ganglioside GM1 in polarized neurons. J. Cell Sci. 109: 2111-2119 [Abstract]
Yamazaki, T, Koo, E., Selkoe, D. (1996). Trafficking of cell-surface amyloid beta-protein precursor. II. Endocytosis, recycling and lysosomal targeting detected by immunolocalization. J. Cell Sci. 109: 999-1008 [Abstract]
Dirkx, R. Jr., Thomas, A., Li, L., Lernmark, �k., Sherwin, R. S., De Camilli, P., Solimena, M. (1995). Targeting of the 67-kDa Isoform of Glutamic Acid Decarboxylase to Intracellular Organelles Is Mediated by Its Interaction with the NH(2)-terminal Region of the 65-kDa Isoform of Glutamic Acid Decarboxylase. J. Biol. Chem. 270: 2241-2246 [Abstract] [Full Text]
Papini, E., Rossetto, O., Cutler, D. F. (1995). Vesicle-associated Membrane Protein (VAMP)/Synaptobrevin-2 Is Associated with Dense Core Secretory Granules in PC12 Neuroendocrine Cells. J. Biol. Chem. 270: 1332-1336 [Abstract] [Full Text]
Huttner, W.B., Ohashi, M., Kehlenbach, R.H., Barr, F.A., Bauerfeind, R., Braunling, O., Corbeil, D., Hannah, M., Pasolli, H.A., Schmidt, A., Schmidt, A.A., Thiele, C., Wang, Y., Kromer, A., Gerdes, H.-H. (1995). Biogenesis of Neurosecretory Vesicles. Cold Spring Harb Symp Quant Biol 60: 315-327 [Abstract]
Baurfend, R., David, C., Galli, T., McPherson, P.S., Takei, K., De Camilli, P. (1995). Molecular Mechanisms in Synaptic Vesicle Endocytosis. Cold Spring Harb Symp Quant Biol 60: 397-404 [Abstract]
Oyarce, A., Eipper, B. (1995). Identification of subcellular compartments containing peptidylglycine alpha-amidating monooxygenase in rat anterior pituitary. J. Cell Sci. 108: 287-297 [Abstract]
Simons, K., Dupree, P., Fiedler, K., Huber, L.A., Kobayashi, T., Kurzchalia, T., Olkkonen, V., Pimplikar, S., Parton, R., Dotti, C. (1992). Biogenesis of Cell-surface Polarity in Epithelial Cells and Neurons. Cold Spring Harb Symp Quant Biol 57: 611-619 [Abstract]
Grimme, S., Honing, S., von Figura, K., Schmidt, B. (2000). Endocytosis of Insulin-like Growth Factor II by a Mini-receptor Based on Repeat 11 of the Mannose 6-Phosphate/Insulin-like Growth Factor II Receptor. J. Biol. Chem. 275: 33697-33703 [Abstract] [Full Text]
Nemoto, Y., Wenk, M. R., Watanabe, M., Daniell, L., Murakami, T., Ringstad, N., Yamada, H., Takei, K., De Camilli, P. (2001). Identification and Characterization of a Synaptojanin 2 Splice Isoform Predominantly Expressed in Nerve Terminals. J. Biol. Chem. 276: 41133-41142 [Abstract] [Full Text]