Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 11 May 1990:
Vol. 248. no. 4956, pp. 742 - 745
DOI: 10.1126/science.2110383
Prev | Table of Contents | Next

Articles

Science, Vol 248, Issue 4956, 742-745
Copyright © 1990 by American Association for the Advancement of Science

articles

Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis

JE Casanova, PP Breitfeld, SA Ross, and KE Mostov

Department of Anatomy, University of California, San Francisco 94143.

The endosomal compartment of polarized epithelial cells is a major crossroads for membrane traffic. Proteins entering this compartment from the cell surface are sorted for transport to one of several destinations: recycling to the original cell surface, targeting to lysosomes for degradation, or transcytosis to the opposite surface. The polymeric immunoglobulin receptor (pIgR), which is normally transcytosed from the basolateral to the apical surface, was used as a model to dissect the signals that mediate this sorting event. When exogenous receptor was expressed in Madin-Darby Canine Kidney (MDCK) cells, it was shown that phosphorylation of pIgR at the serine residue at position 664 is required for efficient transcytosis. Replacement of this serine with alanine generated a receptor that is transcytosed only slowly, and appears to be recycled. Conversely, substitution with aspartic acid (which mimics the negative charge of the phosphate group) results in rapid transcytosis. It was concluded that phosphorylation is the signal that directs the pIgR from the endosome into the transcytotic pathway.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Remodeling Epithelial Cell Organization: Transitions Between Front-Rear and Apical-Basal Polarity.
W. J. Nelson (2009)
Cold Spring Harb Perspect Biol 1, a000513
   Abstract »    Full Text »    PDF »
Pathway selection to the axon depends on multiple targeting signals in NgCAM.
C. C. Yap, R. L. Nokes, D. Wisco, E. Anderson, H. Folsch, and B. Winckler (2008)
J. Cell Sci. 121, 1514-1525
   Abstract »    Full Text »    PDF »
A Teleost Polymeric Ig Receptor Exhibiting Two Ig-Like Domains Transports Tetrameric IgM into the Skin.
K. Hamuro, H. Suetake, N. R. Saha, K. Kikuchi, and Y. Suzuki (2007)
J. Immunol. 178, 5682-5689
   Abstract »    Full Text »    PDF »
Transition of Galactosyltransferase 1 from Trans-Golgi Cisterna to the Trans-Golgi Network Is Signal Mediated.
B. E. Schaub, B. Berger, E. G. Berger, and J. Rohrer (2006)
Mol. Biol. Cell 17, 5153-5162
   Abstract »    Full Text »    PDF »
GPI-anchored proteins are directly targeted to the apical surface in fully polarized MDCK cells.
S. Paladino, T. Pocard, M. A. Catino, and C. Zurzolo (2006)
J. Cell Biol. 172, 1023-1034
   Abstract »    Full Text »    PDF »
Transcytosis of NgCAM in epithelial cells reflects differential signal recognition on the endocytic and secretory pathways.
E. Anderson, S. Maday, J. Sfakianos, M. Hull, B. Winckler, D. Sheff, H. Folsch, and I. Mellman (2005)
J. Cell Biol. 170, 595-605
   Abstract »    Full Text »    PDF »
The Retinal Pigment Epithelium in Visual Function.
O. Strauss (2005)
Physiol Rev 85, 845-881
   Abstract »    Full Text »    PDF »
Phosphorylation influences the translation state of FMRP-associated polyribosomes.
S. Ceman, W. T. O'Donnell, M. Reed, S. Patton, J. Pohl, and S. T. Warren (2003)
Hum. Mol. Genet. 12, 3295-3305
   Abstract »    Full Text »    PDF »
Uncovering multiple axonal targeting pathways in hippocampal neurons.
D. Wisco, E. D. Anderson, M. C. Chang, C. Norden, T. Boiko, H. Folsch, and B. Winckler (2003)
J. Cell Biol. 162, 1317-1328
   Abstract »    Full Text »    PDF »
Multiple cytoplasmic signals direct the intracellular trafficking of chicken kidney AE1 anion exchangers in MDCK cells.
T. L. Adair-Kirk, F. C. Dorsey, and J. V. Cox (2003)
J. Cell Sci. 116, 655-663
   Abstract »    Full Text »    PDF »
Lung mucosal immunity: immunoglobulin-A revisited.
C. Pilette, Y. Ouadrhiri, V. Godding, J-P. Vaerman, and Y. Sibille (2001)
Eur. Respir. J. 18, 571-588
   Abstract »    Full Text »    PDF »
Effects of mutations in potential phosphorylation sites on transcytosis of FcRn.
K. McCarthy, M Lam, L Subramanian, R Shakya, Z Wu, E. Newton, and N. Simister (2001)
J. Cell Sci. 114, 1591-1598
   Abstract »    PDF »
The AP-3 Complex Required for Endosomal Synaptic Vesicle Biogenesis is Associated with a Casein Kinase Ialpha -Like Isoform.
V. V. Faundez and R. B. Kelly (2000)
Mol. Biol. Cell 11, 2591-2604
   Abstract »    Full Text »
Trafficking of Varicella-Zoster Virus Glycoprotein gI: T338-Dependent Retention in the trans-Golgi Network, Secretion, and Mannose 6-Phosphate-Inhibitable Uptake of the Ectodomain.
Z.-H. Wang, M. D. Gershon, O. Lungu, Z. Zhu, and A. A. Gershon (2000)
J. Virol. 74, 6600-6613
   Abstract »    Full Text »
Transcellular Transport of Leptin by the Short Leptin Receptor Isoform ObRa in Madin-Darby Canine Kidney Cells.
S. M. Hileman, J. Tornoe, J. S. Flier, and C. Bjorbak (2000)
Endocrinology 141, 1955-1961
   Abstract »    Full Text »    PDF »
Interactions between the Exocytic and Endocytic Pathways in Polarized Madin-Darby Canine Kidney Cells.
E. Orzech, S. Cohen, A. Weiss, and B. Aroeti (2000)
J. Biol. Chem. 275, 15207-15219
   Abstract »    Full Text »    PDF »
Aquaporin 2 is a vasopressin-independent, constitutive apical membrane protein in rat vas deferens.
A. L. Stevens, S. Breton, C. E. Gustafson, R. Bouley, R. D. Nelson, D. E. Kohan, and D. Brown (2000)
Am J Physiol Cell Physiol 278, C791-C802
   Abstract »    Full Text »    PDF »
Role of Megalin (gp330) in Transcytosis of Thyroglobulin by Thyroid Cells. A NOVEL FUNCTION IN THE CONTROL OF THYROID HORMONE RELEASE.
M. Marino, G. Zheng, L. Chiovato, A. Pinchera, D. Brown, D. Andrews, and R. T. McCluskey (2000)
J. Biol. Chem. 275, 7125-7137
   Abstract »    Full Text »    PDF »
Targeting of membrane transporters in renal epithelia: when cell biology meets physiology.
D. Brown (2000)
Am J Physiol Renal Physiol 278, F192-F201
   Abstract »    Full Text »    PDF »
Bidirectional transcytosis of IgG by the rat neonatal Fc receptor expressed in a rat kidney cell line: a system to study protein transport across epithelia.
K. McCarthy, Y Yoong, and N. Simister (2000)
J. Cell Sci. 113, 1277-1285
   Abstract »    PDF »
Endo180, an endocytic recycling glycoprotein related to the macrophage mannose receptor is expressed on fibroblasts, endothelial cells and macrophages and functions as a lectin receptor.
H Sheikh, H Yarwood, A Ashworth, and C. Isacke (2000)
J. Cell Sci. 113, 1021-1032
   Abstract »    PDF »
H(+)V-ATPase-dependent luminal acidification in the kidney collecting duct and the epididymis/vas deferens: vesicle recycling and transcytotic pathways.
D Brown and S Breton (2000)
J. Exp. Biol. 203, 137-145
   Abstract »
Two Stages of Increased IgA Transfer During Lactation in the Marsupial, Trichosurus vulpecula (Brushtail Possum).
F. M. Adamski and J. Demmer (1999)
J. Immunol. 162, 6009-6015
   Abstract »    Full Text »    PDF »
IL-4 and IFN-{gamma} Increase Steady State Levels of Polymeric Ig Receptor mRNA in Human Airway and Intestinal Epithelial Cells.
L. W. Ackermann, L. A. Wollenweber, and G. M. Denning (1999)
J. Immunol. 162, 5112-5118
   Abstract »    Full Text »    PDF »
Transduction of Basolateral-to-Apical Signals across Epithelial Cells: Ligand-stimulated Transcytosis of the Polymeric Immunoglobulin Receptor Requires Two Signals.
F. Luton and K. E. Mostov (1999)
Mol. Biol. Cell 10, 1409-1427
   Abstract »    Full Text »
The Receptor Recycling Pathway Contains Two Distinct Populations of Early Endosomes with Different Sorting Functions.
D. R. Sheff, E. A. Daro, M. Hull, and I. Mellman (1999)
J. Cell Biol. 145, 123-139
   Abstract »    Full Text »    PDF »
Nonvectorial Surface Transport, Endocytosis via a Di-leucine-based Motif, and Bidirectional Transcytosis of Chimera Encoding the Cytosolic Tail of Rat FcRn Expressed in Madin-Darby Canine Kidney Cells.
I. Stefaner, A. Praetor, and W. Hunziker (1999)
J. Biol. Chem. 274, 8998-9005
   Abstract »    Full Text »    PDF »
Interactions of the AP-1 Golgi Adaptor with the Polymeric Immunoglobulin Receptor and Their Possible Role in Mediating Brefeldin A-sensitive Basolateral Targeting from the trans-Golgi Network.
E. Orzech, K. Schlessinger, A. Weiss, C. T. Okamoto, and B. Aroeti (1999)
J. Biol. Chem. 274, 2201-2215
   Abstract »    Full Text »    PDF »
Putative O-Glycosylation Sites and a Membrane Anchor Are Necessary for Apical Delivery of the Human Neurotrophin Receptor in Caco-2 Cells.
L. Monlauzeur, L. Breuza, and A. Le Bivic (1998)
J. Biol. Chem. 273, 30263-30270
   Abstract »    Full Text »    PDF »
Efficient Trafficking of TGN38 from the Endosome to the trans-Golgi Network Requires a Free Hydroxyl Group at Position 331 in the Cytosolic Domain.
E. P. Roquemore and G. Banting (1998)
Mol. Biol. Cell 9, 2125-2144
   Abstract »    Full Text »
Role of Tyrosine Phosphorylation in Ligand-induced Regulation of Transcytosis of the Polymeric Ig Receptor.
F. Luton, M. H. Cardone, M. Zhang, and K. E. Mostov (1998)
Mol. Biol. Cell 9, 1787-1802
   Abstract »    Full Text »
The SNARE Machinery Is Involved in Apical Plasma Membrane Trafficking in MDCK Cells.
S. H. Low, S. J. Chapin, C. Wimmer, S. W. Whiteheart, L. G. Komuves, K. E. Mostov, and T. Weimbs (1998)
J. Cell Biol. 141, 1503-1513
   Abstract »    Full Text »    PDF »
Regulation of the polymeric immunoglobulin receptor by water intake and vasopressin in the rat kidney.
J. C. Rice, J. S. Spence, J. Megyesi, R. L. Safirstein, and R. M. Goldblum (1998)
Am J Physiol Renal Physiol 274, F966-F977
   Abstract »    Full Text »    PDF »
Opposite sorting and transcytosis of the polymeric immunoglobulin receptor in transfected endothelial and epithelial cells.
T Su and K. Stanley (1998)
J. Cell Sci. 111, 1197-1206
   Abstract »    PDF »
Divergent Signaling Capacities of the Long and Short Isoforms of the Leptin Receptor.
C. Bjorbak, S. Uotani, B. da Silva, and J. S. Flier (1997)
J. Biol. Chem. 272, 32686-32695
   Abstract »    Full Text »    PDF »
Cytoplasmic Domain of E-selectin Contains a Non-tyrosine Endocytosis Signal.
P. I. Chuang, B. A. Young, R. R. Thiagarajan, C. Cornejo, R. K. Winn, and J. M. Harlan (1997)
J. Biol. Chem. 272, 24813-24818
   Abstract »    Full Text »    PDF »
A New Function for the LDL Receptor: Transcytosis of LDL across the Blood-Brain Barrier.
B. Dehouck, L. Fenart, M.-P. Dehouck, A. Pierce, G. Torpier, and R. Cecchelli (1997)
J. Cell Biol. 138, 877-889
   Abstract »    Full Text »    PDF »
Systematic Mutational Analysis of the Cation-independent Mannose 6-Phosphate/Insulin-like Growth Factor II Receptor Cytoplasmic Domain. AN ACIDIC CLUSTER CONTAINING A KEY ASPARTATE IS IMPORTANT FOR FUNCTION IN LYSOSOMAL ENZYME SORTING.
H. J. Chen, J. Yuan, and P. Lobel (1997)
J. Biol. Chem. 272, 7003-7012
   Abstract »    Full Text »    PDF »
Hepatocyte Growth Factor Alters the Polarity of Madin-Darby Canine Kidney Cell Monolayers.
D. F. Balkovetz, A. L. Pollack, and K. E. Mostov (1997)
J. Biol. Chem. 272, 3471-3477
   Abstract »    Full Text »    PDF »
A Di-hydrophobic Leu-Val Motif Regulates the Basolateral Localization of CD44 in Polarized Madin-Darby Canine Kidney Epithelial Cells.
H. Sheikh and C. M. Isacke (1996)
J. Biol. Chem. 271, 12185-12190
   Abstract »    Full Text »    PDF »
Calmodulin Binds to the Basolateral Targeting Signal of the Polymeric Immunoglobulin Receptor.
S. J. Chapin, C. Enrich, B. Aroeti, R. J. Havel, and K. E. Mostov (1996)
J. Biol. Chem. 271, 1336-1342
   Abstract »    Full Text »    PDF »
Wortmannin, an Inhibitor of Phosphoinositide 3-Kinase, Inhibits Transcytosis in Polarized Epithelial Cells.
S. H. Hansen, A. Olsson, and J. E. Casanova (1995)
J. Biol. Chem. 270, 28425-28432
   Abstract »    Full Text »    PDF »
Transcytosis of Aminopeptidase N in Caco-2 Cells Is Mediated by a Non-cytoplasmic Signal.
L. K. Vogel, O. Norén, and H. Sjöström (1995)
J. Biol. Chem. 270, 22933-22938
   Abstract »    Full Text »    PDF »
Inhibition of Autophagy and Multiple Steps in Asialoglycoprotein Endocytosis by Inhibitors of Tyrosine Protein Kinases (Tyrphostins).
I. Holen, P. E. Str, P. B. Gordon, M. Fengsrud, T. O. Berg, and P. O. Seglen (1995)
J. Biol. Chem. 270, 12823-12831
   Abstract »    Full Text »    PDF »
Molecular Characterization of an Apical Early Endosomal Glycoprotein from Developing Rat Intestinal Epithelial Cells.
B. A. Speelman, K. Allen, T. L. Grounds, M. R. Neutra, T. Kirchhausen, and J. M. Wilson (1995)
J. Biol. Chem. 270, 1583-1588
   Abstract »    Full Text »    PDF »
Molecular Sorting of Membrane Proteins in Polarized and Nonpolarized Cells.
I. Mellman (1995)
Cold Spring Harb Symp Quant Biol 60, 745-752
   Abstract »    PDF »
Regulation of Protein Traffic in Polarized Epithelial Cells: The Polymeric Immunoglobulin Receptor Model.
K.E. Mostov, Y. Altschuler, S.J. Chapin, C. Enrich, S.-H. Low, F. Luton, J. Richman-Eisenstat, K.L. Singer, K. Tang, and T. Weimbs (1995)
Cold Spring Harb Symp Quant Biol 60, 775-781
   Abstract »    PDF »
Regulation of pathways within cultured epithelial cells for the transcytosis of a basal membrane-bound peroxidase-polylysine conjugate.
M. Taub and W. Shen (1993)
J. Cell Sci. 106, 1313-1321
   Abstract »    PDF »
Caveolin-1 Binding to Endoplasmic Reticulum Membranes and Entry into the Regulated Secretory Pathway Are Regulated by Serine Phosphorylation. PROTEIN SORTING AT THE LEVEL OF THE ENDOPLASMIC RETICULUM.
A. Schlegel, P. Arvan, and M. P. Lisanti (2001)
J. Biol. Chem. 276, 4398-4408
   Abstract »    Full Text »    PDF »
Signal Transduction by the CEACAM1 Tumor Suppressor. PHOSPHORYLATION OF SERINE 503 IS REQUIRED FOR GROWTH-INHIBITORY ACTIVITY.
V. T. Estrera, D.-T. Chen, W. Luo, D. C. Hixson, and S.-H. Lin (2001)
J. Biol. Chem. 276, 15547-15553
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)