Expression of macrophage-lymphocyte Fc receptors in Madin-Darby canine kidney cells: polarity and transcytosis differ for isoforms with or without coated pit localization domains

doi:10.1083/jcb.109.6.3291

This Article

	Full Text (PDF, 2665K)
	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 Hunziker, W.
	Articles by Mellman, I.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Hunziker, W.
	Articles by Mellman, I.


Social Bookmarking

	What's this?

ARTICLES

Expression of macrophage-lymphocyte Fc receptors in Madin-Darby canine kidney cells: polarity and transcytosis differ for isoforms with or without coated pit localization domains

W Hunziker and I Mellman
Department of Cell Biology, Yale University School of Medicine, New Haven, Connecticut 06510.

Many cells of the immune system and certain epithelia express receptors for the Fc domain of IgG (FcR). On mouse macrophages and lymphocytes, two distinct receptor isoforms have been identified, designated FcRII- B1 and FcRII-B2. The isoforms are identical except for an in-frame insertion of 47 amino acids in the cytoplasmic tail of FcRII-B1 that blocks its ability to be internalized by clathrin-coated pits. We have recently found that at least one IgG-transporting epithelium, namely placental syncytial trophoblasts, expresses transcripts encoding a receptor similar or identical to macrophage-lymphocyte FcRII. To determine whether FcRII of hematopoietic cells might also function as a transcytotic receptor if expressed in epithelial cells, FcRII-B1 and - B2 were transfected into Madin-Darby canine kidney (MDCK) cells and grown on permeable filter units. The two FcRII isoforms exhibited different patterns of polarized expression: FcRII-B1 was localized mainly to the apical plasma membrane domain, whereas FcRII-B2 was found predominantly on the basolateral surface. As expected for FcR in placenta, FcRII-B2 and to a lesser extent FcRII-B1 mediated transcellular transport of IgG-complexes from the apical to the basolateral plasma membrane. Neither receptor mediated transcytosis in the opposite direction, although FcRII-B2 also delivered ligand to lysosomes when internalized from either the basolateral or apical domains. Furthermore, FcRII-B2 was capable of transporting monovalent antireceptor antibody Fab fragments across the cell, suggesting that transcytosis was not dependent on receptor cross-linking. These findings suggest the possibility that FcRII can mediate transepithelial IgG transport when expressed in placental syncytial trophoblasts in addition to its "classical" endocytic and signaling activities when expressed in macrophages. Because FcRII-B1 and -B2 are expressed with distinct polarities, the results also suggest that interactions with clathrin-coated pits may play a role in generating the polarized distribution of at least some plasma membrane proteins in MDCK 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:

Desai, D. D., Harbers, S. O., Flores, M., Colonna, L., Downie, M. P., Bergtold, A., Jung, S., Clynes, R. (2007). Fc{gamma} Receptor IIB on Dendritic Cells Enforces Peripheral Tolerance by Inhibiting Effector T Cell Responses. J. Immunol. 178: 6217-6226 [Abstract] [Full Text]
Takizawa, T., Anderson, C. L., Robinson, J. M. (2005). A Novel Fc{gamma}R-Defined, IgG-Containing Organelle in Placental Endothelium. J. Immunol. 175: 2331-2339 [Abstract] [Full Text]
Newton, E. E., Wu, Z., Simister, N. E. (2005). Characterization of basolateral-targeting signals in the neonatal Fc receptor. J. Cell Sci. 118: 2461-2469 [Abstract] [Full Text]
van Lent, P., Nabbe, K. C., Boross, P., Blom, A. B., Roth, J., Holthuysen, A., Sloetjes, A., Verbeek, S., van den Berg, W. (2003). The Inhibitory Receptor Fc{gamma}RII Reduces Joint Inflammation and Destruction in Experimental Immune Complex-Mediated Arthritides Not Only by Inhibition of Fc{gamma}RI/III but Also by Efficient Clearance and Endocytosis of Immune Complexes. Am. J. Pathol. 163: 1839-1848 [Abstract] [Full Text]
ESTIENNE, V., DUTHOIT, C., REICHERT, M., PRAETOR, A., CARAYON, P., HUNZIKER, W., RUF, J. (2002). Androgen-dependent expression of Fc{gamma}RIIB2 by thyrocytes from patients with autoimmune Graves' disease: a possible molecular clue for sex dependence of autoimmune disease. FASEB J. 16: 1087-1092 [Abstract] [Full Text]
Lyden, T. W., Robinson, J. M., Tridandapani, S., Teillaud, J.-L., Garber, S. A., Osborne, J. M., Frey, J., Budde, P., Anderson, C. L. (2001). The Fc Receptor for IgG Expressed in the Villus Endothelium of Human Placenta Is Fc{{gamma}}RIIb2. J. Immunol. 166: 3882-3889 [Abstract] [Full Text]
Bender, F. C., Reymond, M. A., Bron, C., Quest, A. F. G. (2000). Caveolin-1 Levels Are Down-Regulated in Human Colon Tumors, and Ectopic Expression of Caveolin-1 in Colon Carcinoma Cell Lines Reduces Cell Tumorigenicity. Cancer Res. 60: 5870-5878 [Abstract] [Full Text]
McCarthy, K., Yoong, Y, Simister, N. (2000). 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. J. Cell Sci. 113: 1277-1285 [Abstract]
Simmen, T., Nobile, M., Bonifacino, J. S., Hunziker, W. (1999). Basolateral Sorting of Furin in MDCK Cells Requires a Phenylalanine-Isoleucine Motif Together with an Acidic Amino Acid Cluster. Mol. Cell. Biol. 19: 3136-3144 [Abstract] [Full Text]
Stefaner, I., Praetor, A., Hunziker, W. (1999). 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. J. Biol. Chem. 274: 8998-9005 [Abstract] [Full Text]
Praetor, A, Ellinger, I, Hunziker, W (1999). Intracellular traffic of the MHC class I-like IgG Fc receptor, FcRn, expressed in epithelial MDCK cells. J. Cell Sci. 112: 2291-2299 [Abstract]
Simmen, T, Schmidt, A, Hunziker, W, Beermann, F (1999). The tyrosinase tail mediates sorting to the lysosomal compartment in MDCK cells via a di-leucine and a tyrosine-based signal. J. Cell Sci. 112: 45-53 [Abstract]
Roush, D. L., Gottardi, C. J., Naim, H. Y., Roth, M. G., Caplan, M. J. (1998). Tyrosine-based Membrane Protein Sorting Signals Are Differentially Interpreted by Polarized Madin-Darby Canine Kidney and LLC-PK1 Epithelial Cells. J. Biol. Chem. 273: 26862-26869 [Abstract] [Full Text]
van IJzendoorn, S. C.D., Hoekstra, D. (1998). (Glyco)sphingolipids Are Sorted in Sub-Apical Compartments in HepG2 Cells: A Role for Non-Golgi-Related Intracellular Sites in the Polarized Distribution of (Glyco)sphingolipids. JCB 142: 683-696 [Abstract] [Full Text]
Hunziker, W., Peters, P. J. (1998). Rab17 Localizes to Recycling Endosomes and Regulates Receptor-mediated Transcytosis in Epithelial Cells. J. Biol. Chem. 273: 15734-15741 [Abstract] [Full Text]
Zacchi, P., Stenmark, H., Parton, R. G., Orioli, D., Lim, F., Giner, A., Mellman, I., Zerial, M., Murphy, C. (1998). Rab17 Regulates Membrane Trafficking through Apical Recycling Endosomes in Polarized Epithelial Cells. JCB 140: 1039-1053 [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]
Hartmann, T., Bergsdorf, C., Sandbrink, R., Tienari, P. J., Multhaup, G., Ida, N., Bieger, S., Dyrks, T., Weidemann, A., Masters, C. L., Beyreuther, K. (1996). Alzheimer's Disease beta A4 Protein Release and Amyloid Precursor Protein Sorting Are Regulated by Alternative Splicing. J. Biol. Chem. 271: 13208-13214 [Abstract] [Full Text]
Ellis, J. A., Luzio, J. P. (1995). Identification and Characterization of a Novel Protein (p137) Which Transcytoses Bidirectionally in Caco-2 Cells. J. Biol. Chem. 270: 20717-20723 [Abstract] [Full Text]
Mellman, I. (1995). Molecular Sorting of Membrane Proteins in Polarized and Nonpolarized Cells. Cold Spring Harb Symp Quant Biol 60: 745-752 [Abstract]
Casanova, J., Breitfeld, P., Ross, S., Mostov, K. (1990). Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis. Science 248: 742-745 [Abstract]