HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kitamura, T. Articles by Goldblum, R. M. Search for Related Content PubMed PubMed Citation Articles by Kitamura, T. Articles by Goldblum, R. M.

Human Intestinal Epithelial Cells Express a Novel Receptor for IgA¹

Tetsuro Kitamura^*, Roberto P. Garofalo^2,*, Atsushi Kamijo^*, Dianne K. Hammond^*, Janet A. Oka, Carlton R. Caflisch^*, Mohan Shenoy^*, Antonella Casola^*, Paul H. Weigel and Randall M. Goldblum^*

^* Department of Pediatrics, University of Texas Medical Branch, Galveston, TX 77555; and Department of Biochemistry, University of Oklahoma Health Science Center, Norman, OK 73190

	Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
Binding and transport of polymeric Igs (pIgA and IgM) across epithelia is mediated by the polymeric Ig receptor (pIgR), which is expressed on the basolateral surface of secretory epithelial cells. Although an Fc receptor for IgA (FcR) has been identified on myeloid cells and some cultured mesangial cells, the expression of an FcR on epithelial cells has not been described. In this study, binding of IgA to a human epithelial line, HT-29/19A, with features of differentiated colonic epithelial cells, was examined. Radiolabeled monomeric IgA (mIgA) showed a dose-dependent, saturable, and cation-independent binding to confluent monolayers of HT-29/19A cells. Excess of unlabeled mIgA, but not IgG or IgM, competed for the mIgA binding, indicating that the binding was IgA isotype-specific and was not mediated by the pIgR. The lack of competition by asialoorosomucoid and the lack of requirement for divalent cations excluded the possibility that IgA binding to HT-29/19A cells was due to the asialoglycoprotein receptor or ß-1,4-galactosyltransferase, previously described on HT-29 cells. Moreover, the FcR (CD89) protein and message were undetectable in HT-29/19A cells. FACS analysis of IgA binding demonstrated two discrete populations of HT-29/19 cells, which bound different amounts of mIgA. IgA binding to other colon carcinoma cell lines was also demonstrated by FACS analysis, suggesting that an IgA receptor, distinct from the pIgR, asialoglycoprotein receptor, galactosyltransferase, and CD89 is constitutively expressed on cultured human enterocytes. The function of this novel IgA receptor in mucosal immunity remains to be elucidated.

	Introduction

Top Abstract Introduction Materials and Methods Results Discussion References

 
Immunoglobulin A is the most prominent class of Ab in intestinal tissue and mucosal secretions. A better understanding of IgA-mediated mucosal immunity requires insights into the interaction between IgA and receptors present at mucosal surfaces (1, 2, 3, 4). In particular, the high concentrations of IgA on either side of the mucosal epithelium might have immunomodulatory effects on intestinal epithelial cells.

Receptors that bind human IgA have been demonstrated on numerous cell types and on some bacteria. The best characterized of these is the receptor for Fc fragments of IgA (FcR, CD89), which is expressed on myeloid cells including neutrophils (5, 6, 7), monocytes (8, 9, 10, 11), macrophages (12, 13, 14), and eosinophils (15). The asialoglycoprotein receptor (ASGPR)³ found on hepatocytes, some macrophages, and recently demonstrated on cultured intestinal epithelial cells (16, 17), and ß-1,4-galactosyltransferase expressed on plasma membranes (18) can also act as a cell-surface receptor for different forms of IgA. The polymeric Ig receptor (pIgR), expressed on secretory epithelium binds J chain-containing IgA polymers and IgM. Both B and T lymphocytes have been shown to bind IgA, but a receptor has not been fully characterized (19, 20). Expression of CD89 by cultured rat and human mesangial cells has been described (21). However, our recent studies suggest that another, as yet uncharacterized IgA receptor is constitutively expressed on mesangial cells (22). The function of this receptor may be related to its ability to initiate intracellular signals, leading to cellular activation.

HT-29, a well-characterized human cell line derived from a colonic adenocarcinoma, expresses pIgR on its surface (23). In the present study, we demonstrate that HT-29 clone 19A and other human colonic cell lines constitutively express a novel IgA receptor. The characteristics of this receptor are similar to those we have described on mesangial cells, but distinct from any IgA receptor previously described on epithelial or other cell types.

	Materials and Methods

Top Abstract Introduction Materials and Methods Results Discussion References

 
Intestinal epithelial cell lines

HT-29 clone 19A (HT-29/19A), a colonic adenocarcinoma cell line, was kindly provided by Dr. Andrew Morris (Baylor College of Medicine, Houston, TX). This clone was derived by sodium butyrate treatment of HT-29 cells and exhibits features of differentiated colonic epithelial cells, independent of the presence of glucose (24). The parent cell line HT-29 and the human colonic T84 and Caco 2 cells were obtained from American Type Culture Collection (Manassas, VA). Cells were cultured in DMEM, supplemented with 10% FCS, 2 mmol/L L-glutamine, 1 mmol/L sodium pyruvate, 50 µg/ml streptomycin, and 50 U/ml penicillin. T84 cells were grown in DMEM/F12 medium supplemented with 5% FCS. All cell lines were maintained at 37°C in 5% CO₂. All tissue culture reagents were purchased from Life Technologies (Gaithersburg, MD).

Ig preparations and reagents

Monomeric IgA1 (mIgA) was prepared in our laboratory as previously described (22). Briefly, IgA1 fraction was isolated from normal donors’ sera by Jacalin affinity chromatography. Serum was diluted with PBS (pH 7.1), filtered through a 0.2-µm filter (Corning Glass Works, Corning, NY), and chromatographed on columns of Jacalin immobilized on cross-linked 6% beaded agarose (Pierce, Rockford, IL). After washing the column with PBS, IgA1 was eluted with 0.2 M melibiose (Sigma, St. Louis, MO) in PBS and concentrated by ultrafiltration using 30,000 m.w. exclusion membranes (Centriprep 30; Amicon, Beverly, MA). The IgA1 was then fractionated into three peaks by HPLC molecular sieve chromatography, using a 1.5 x 30 cm Superdex HR 200 column (Pharmacia Biotech, Piscataway, NJ). The IgA1 fraction, found to be 98% pure by SDS-PAGE and densitometry of Coomassie-stained gels, was used for radiolabeling. Some mIgA was heat-aggregated (AIgA) by incubation for 150 min at 63°C, as previously described (21, 22). Human IgG, secretory IgA (S-IgA), BSA, and asialoorosomucoid were purchased from Sigma. Purified serum IgM and IgA was obtained from Pierce. mIgA2 was isolated from the later by removing all IgA1 by Jacalin affinity chromatography. Biotinylation of mIgA or AIgA was performed using EZ-Link NHS-Biotin (Pierce) according to the manufacturer’s instruction.

Binding of radiolabeled IgA1 to HT-29/19A cells

mIgA was radiolabeled with Na¹²⁵I (10–20 mCi/µg iodine) (Amersham, Arlington Heights, IL), as previously described (25). Confluent monolayers of HT-29/19A cells were washed once in PBS and incubated 30 min in DMEM without serum. The cells were then transferred to ice, washed twice with PBS, and incubated for 60 min with ¹²⁵I-labeled mIgA (¹²⁵I-mIgA) (2 µg/ml) in 0.2 ml of PBS (without divalent cations) alone or in the presence of various concentrations of nonradioactive mIgA, AIgA, S-IgA, IgG, IgM, or asiasoorosomucoid. The radioactive medium was removed and the cells were rapidly washed three times with HBSS. The cells were solubilized in 0.3 N NaOH (0.4 ml) and the lysates were transferred to gamma tubes and the radioactivity was quantified in a Packard 5002 gamma counter (Downers Grove, IL). The protein content of the lysates was measured by the Bradford’s method using BSA as the standard. Assays were performed in duplicate and the data were analyzed using the RADLIG and LIGAND programs (Biosoft, Ferguson, MO) (22).

Flow cytometric analysis

Single cell suspensions of epithelial cells obtained after trypsinization were cultured in petri dishes with constant rocking at 37°C in 5% CO₂ for 24 h to allow reexpression of receptors lost during the treatment with trypsin. The cell number and viability were determined by trypan blue dye exclusion. Approximately 1 x 10⁵ cells were incubated in PBS without divalent cations containing varying amounts of biotinylated mIgA or AIgA (1–10 µg) on ice for 1 h. After washing with PBS-BSA buffer (PBS containing 0.1% BSA and 0.05% NaN₃), cells were incubated with streptavidin-FITC (3 µg/ml) on ice for 1 h. The cells were then washed once quickly and fixed in 1% paraformaldehyde, and 10,000 cells per condition were analyzed for fluorescence by single-color flow cytometry on a FACScan (Becton Dickinson, San Jose, CA). In competition experiments, nonbiotinylated mIgA or AIgA were added for 1 h before addition of the biotinylated IgA. In other experiments, unlabeled mIgA1 were incubated with HT-29 cells as described above, followed by FITC-conjugated anti-IgA Ab (Sigma) and analyzed by single-color flow cytometry. To determine the expression of CD89, intestinal epithelial cells were incubated with a mAb to CD89 (My43) (kindly provided by Dr. Lee Shen, Dartmouth University), followed by FITC-labeled goat anti-mouse IgG (H+L) (Accurate Chemicals, Westbury, NY). PMA-stimulated U937 cells were employed as positive control in this experiment.

RT-PCR for FcR (CD89) mRNA

Total RNA was extracted from HT-29/19A and T84 intestinal cells and from U937 by the guanidium thiocyanate method with RNAzol B (Life Technologies) and RT-PCR for FcR was performed with Gene RNA PCR kit components (Perkin-Elmer Cetus, Branchburg, NJ), as previously described (22). First-strand cDNA was synthesized using murine leukemia virus reverse transcriptase and oligo(dT) at 42°C for 60 min. cDNA was amplified using the following primers based on the sequence data for U937 FcR cDNA (26): 5'-AAGCTTACCTGACCCAGCTGATG-3' (sense strand) and 5'-AAGCTTCTTAGTGAGCTTTTCTCTC-3' (antisense strand). The anticipated product contains 701 bases of the translated region and 96 bases of the untranslated 3' region of FcR cDNA, for a predicted size of 797 bp. PCR was performed in a DNA thermal cycler (Perkin-Elmer Cetus) programmed as follows: denaturation cycle at 94°C for 15 s, annealing at 58°C for 30 s, and extension at 72°C for 3 min, for a total of 35 cycles. PCR products were resolved alongside pUC18HaeIII DNA marker (Sigma) on a 2% agarose gel containing ethidium bromide, and visualized and photographed under UV light.

	Results

Top Abstract Introduction Materials and Methods Results Discussion References

 
Binding of ¹²⁵I-mIgA to HT-29/19A cells

Equilibrium binding studies were performed to determine whether mIgA binds to HT-29/19A and to characterize the binding. Fig. 1A shows the specific (inhibitable by a large excess of unlabeled IgA) binding of IgA. mIgA bound to HT-29/19A in a dose-dependent manner and was saturable at 800 nM of mIgA.

View larger version (12K): [in this window] [in a new window]   FIGURE 1. A, Equilibrium binding of 125I-mIgA to HT-29/19A cells. HT-29/19A cells were incubated for 60 min at 4°C with 125I-mIgA (2 µg/ml) alone or in the presence of increasing concentration of nonradiolabeled mIgA. Results are shown as specific binding (total binding - nonspecific binding). B, Specificity of 125I-mIgA binding to HT-29/19A cells. Up to 400 µg/ml of nonradiolabeled mIgA (200-fold molar excess over the radiolabeled-IgA) displayed maximal inhibition (50–60%) of labeled mIgA binding.

View larger version (15K): [in this window] [in a new window]   FIGURE 2. Scatchard plot. mIgA binds to HT-29/19A cells with a Kd of 6.7 x 10-8 M. Results are expressed as the mean of four experiments.

The isotype specificity of IgA binding was investigated by determining the pattern of inhibition obtained with various classes of Igs. Cells were incubated with human IgG (50–300 µg/ml) or IgM (50–300 µg/ml) before the addition of ¹²⁵I-mIgA. Neither IgG nor IgM blocked the mIgA binding (Fig. 3). These data suggest that the binding of IgA was Ig class specific and was not mediated by the pIgR, which binds polymeric forms of IgA and IgM.

View larger version (46K): [in this window] [in a new window]   FIGURE 3. Ig isotype specificity of 125I-mIgA binding to HT-29/19A cells. HT-29/19A cells were incubated with 125I-mIgA (2 µg/ml) alone (None), or in the presence of different concentrations of unlabeled human IgG, IgM, and mIgA. Results are presented as the percent of 125I-mIgA bound to the cells in the absence of inhibitors (100% binding). The results are from single experiments for the lowest concentrations of inhibitors. The mean ± SD from three to seven experiments are presented for the highest concentrations.

To determine the relative binding affinity of different molecular forms of IgA, HT-29/19A cells were first incubated with mIgA, S-IgA or AIgA. Next ¹²⁵I-mIgA was added. The results shown in Fig. 4 indicate that IgA binding is independent on the molecular size of the IgA, but that S-IgA does not bind to the HT-29/19A cells.

View larger version (50K): [in this window] [in a new window]   FIGURE 4. Binding of various molecular forms of IgA to HT-29/19A cells. Cells were incubated with 125I-mIgA (2 µg/ml) alone (None), or in the presence of different concentrations of unlabeled mIgA, AIgA, and S-IgA. Results are presented as the percent of 125I-mIgA bound to the cells in the absence of inhibitors (100% binding) or in the presence of unlabeled mIgA, AIgA, and S-IgA .

Because IgA can bind to the ASGPR (16), which was recently shown to be expressed on HT-29 cells (17), competition experiments were performed using asialoorosomucoid as a potential inhibitor of mIgA binding (28) (Fig. 5). The results indicate that the binding of mIgA to HT-29/19A cells was not mediated by an ASGPR.

View larger version (49K): [in this window] [in a new window]   FIGURE 5. mIgA does not bind the ASGPR on HT-29/19A cells. Cells were incubated with 125I-mIgA (2 µg/ml) alone (None) or in the presence of unlabeled mIgA (300 µg), or different concentrations of asialoorosomucoid (ASOR). Results are presented as the percent of 125I-mIgA bound to the cells in the absence of inhibitors (100% binding) (n = 1–7 experiments).

To confirm by an independent method the binding of mIgA to HT-29/19A cells and to evaluate the proportion of cells that bind mIgA, flow cytometry was performed using biotinylated mIgA as the probe. In these experiments, a dose-dependent binding of IgA to a subpopulation of the HT-29/19A cells (30% of total cells) was observed (Fig. 6). To demonstrate that this binding was specific, unlabeled mIgA was used to compete for binding of the biotinylated mIgA. In the presence of 100-fold molar excess of nonbiotinylated mIgA, we observed a reduction in fluorescence intensity to the levels seen for cells incubated without mIgA (i.e., stained only with avidin-FITC) (Fig. 7).

View larger version (23K): [in this window] [in a new window]   FIGURE 6. Dose-dependent binding of biotinylated-mIgA to a subset of HT-29/19A cells. Cells were incubated with different amounts of biotinylated-mIgA (1–10 µg) followed by streptavidin-FITC. The histogram shows overlays of logarithmic mean fluorescence frequency distribution of 10,000 cells. Cells incubated without IgA, followed by streptavidin-FITC, served as negative control (filled area). A representative experiment from five performed is shown.

View larger version (23K): [in this window] [in a new window]   FIGURE 7. Competition for biotinylated-mIgA binding to HT-29/19A cells by unconjugated IgA. Cells were incubated with 100-fold excess of nonbiotinylated mIgA for 90 min before adding biotinylated mIgA (2 µg/ml). The figure shows overlays of two histograms showing logarithmic fluorescence intensity of 10,000 cells each. A representative experiment from five performed is shown.

View larger version (18K): [in this window] [in a new window]   FIGURE 8. Binding of mIgA1 to HT-29 cells. Unlabeled, Jacalin-purified, mIgA1 (5 µg) were incubated with HT-29/19A cells followed by FITC-conjugated anti-IgA Ab. Cells incubated with FITC-conjugated anti-IgA Ab alone served as negative control. The figure is an overlay of two histograms showing the logarithmic fluorescence intensity of 10,000 cells each. A representative experiment from four performed is shown.

View larger version (23K): [in this window] [in a new window]   FIGURE 9. mIgA binding to intestinal cell lines. HT-29/19A, T84, and Caco 2 cells were incubated with biotinylated mIgA (10 µg) followed by streptavidin-FITC (open area). Cells incubated without IgA, followed by streptavidin-FITC served as negative control (filled area). The histogram shows overlays of logarithmic fluorescence intensity of 10,000 cells. A representative experiment from three performed is shown.

To exclude the possibility that mIgA binding to HT-29/19A cells was due to the expression of FcR1 (CD89), steady-state levels of mRNA for CD89 were analyzed by RT-PCR in HT-29, HT-29/19A, and T84 cells. U937 cells were used as positive control. As expected, PMA-stimulated U937 cells expressed CD89 mRNA (Fig. 10A). In contrast, HT-29, HT-29/19A, and T84 cells did not express mRNA for CD89. Expression of the housekeeping gene ß-actin demonstrated that the RNA from all the cells was intact and that relatively equal amounts of the RT-PCR mixtures were loaded on the gel. To confirm that long-lived FcR1 protein was not present on the surface of the epithelial cells, we used flow cytometry to examine the binding of My43, a monoclonal IgM Ab to FcR1, to HT-29/19A and U937 cells. Although a uniform staining was evident for U937 cells, no binding of My43 was detected on HT-29/19A cells (Fig. 10B). Thus, these data suggest that the binding of IgA1 to intestinal epithelial cells was not mediated by the FcR1.

View larger version (24K): [in this window] [in a new window]   FIGURE 10. Absence of CD89 expression in colon carcinoma cell lines. A, Expression of CD89 mRNA by HT-29, HT-29/19A, T84, and by the monocytic cell line U937 was determined by RT-PCR. U937 expresses CD89 mRNA, as previously shown. B, CD89 protein on HT-29/19A and U937 was examined by flow cytometry using the mAb My43. As for mRNA, only U937 expresses CD89 protein.

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

Experiments presented herein indicate that colonic epithelial cells also have receptors which specifically bind IgA. Again, the presence of secretory component (and/or J chain) on S-IgA seems to prevent their binding to this receptor. These characteristics appear to distinguish the epithelial receptor from all other IgA receptors described previously. Because our experiments were performed in PBS without divalent cations, the binding of mIgA to HT-29/19A cells observed in our study was not mediated by ß1-4 galactosyltransferase (18). We also performed additional experiments that excluded the possibility that the mIgA binding we observed in the colonic cell lines was due to the previously described FcR or the ASGPR. Further, the use of mIgA as the primary ligand and the lack of inhibition by IgM suggest that the pIgR, known to be present on HT-29/19A cells (23), is not responsible for the IgA binding we observed on colonic cells. Finally, the lack of binding of S-IgA distinguishes the receptor on HT-29/19A from that described on eosinophils, which only binds S-IgA and free secretory component (29, 30). The IgA receptors that have been described on B lymphocytes, T lymphocytes, and NK cells have not been fully characterized and thus cannot be distinguished from those we have described on mesangial and epithelial cells. A summary of the characteristics that differentiate the epithelial cell IgA receptors described here from those described previously is shown in the Table I.

Binding to some Ig receptors can result in internalization and transcellular transport of intact Igs, as in the case of the pIgR (33) and Fcn receptor of the neonatal rodent (34). The outcome of these processes is epithelial secretion or intestinal or transplacental uptake of Igs, respectively. Similarly, the ASGPR mediates internalization of glycoproteins, including Ig, but the major outcome is intracellular degradation of the ligand and recycling of the receptor to the cell surface (34). We have not explored in detail the possibility that the colonic epithelial or mesangial IgA receptor mediates such a process, but preliminary results suggest that neither cell specifically internalizes or degrades the IgA which binds to their cell surface receptors (results not shown).

Thus, we do not yet know either the structure or function of the IgA-specific receptor on intestinal epithelial cells, nor do we know the cell surface localization. However, based on the similarities between the mesangial cell and epithelial cell IgA receptors, we are currently investigating the effect of IgA on intracellular signaling pathways that are associated with the transcriptional activation of inflammatory genes in epithelial cells. The potential adaptive response of epithelial cells to such signals and the pathologic consequences of persistent activation may be important areas for future investigations.

	Acknowledgments

 
We thank Dr. Pearay L. Ogra for helpful discussions and suggestions.

	Footnotes

 
¹ This work was supported by Grants AI15939 (R.P.G.) and DK49340 (R.M.G.) from the National Institutes of Health. A.C. is the recipient of the 1998 European Society for Pediatric Infectious Disease Fellowship Award sponsored by Bristol-Myers Squibb.

² Address correspondence and reprint requests to Dr. Roberto P. Garofalo, Department of Pediatrics, University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555-0369.

³ Abbreviations used in this paper: ASGPR, asialoglycoprotein receptor; AIgA, heat-aggregated monomeric IgA; mIgA, monomeric IgA; pIgR, polymeric Ig receptor; S-IgA, secretory IgA; ¹²⁵I-mIgA, ¹²⁵I-labeled mIgA.

Received for publication April 21, 1999. Accepted for publication February 25, 2000.

	References

Top Abstract Introduction Materials and Methods Results Discussion References

 

1. Lamm, M. E.. 1976. Cellular aspects of immunoglobulin A. Adv. Immunol. 22:223.[Medline]
2. Underdown, B. J., J. M. Schiff. 1986. Immunoglobulin A: strategic defense initiative at the mucosal surface. Annu. Rev. Immunol. 4:389.[Medline]
3. Mestecky, J., J. R. McGhee. 1987. Immunoglobulin A (IgA): molecular and cellular interactions involved in IgA biosynthesis and immune response. Adv. Immunol. 40:153.[Medline]
4. Mostov, K., C. S Kaetzel. 1999. Immunoglobulin transport and the polymeric immunoglobulin receptor. P. L. Ogra, and J. Mestecky, and M. E. Lamm, and W. Strober, and J. Bienenstock, and J. R. McGhee, eds. Mucosal Immunology 181. Academic Press, San Diego, CA.
5. Albrechtsen, M., G. R. Yeaman, M. A. Kerr. 1988. Characterization of the IgA receptor from human polymorphonuclear leukocytes. Immunology 64:20.
6. Mazengera, R. L., M. A. Kerr. 1990. The specificity of the IgA receptor purified from human neutrophils. J. Biochem. 272:159.
7. Fanger, M. W., S. N. Goldstine, L. Shen. 1983. Cytofluorographic analysis of receptors for IgA on human polymorphonuclear cells and monocytes and the correlation of receptor expression with phagocytosis. Mol. Immunol. 20:1019.[Medline]
8. Chevailler, A., R. C. Monteiro, H. Kubagawa, M. D. Cooper. 1989. Immunofluorescence analysis of IgA binding by human mononuclear cells in blood and lymphoid tissue. J. Immunol. 142:2244.[Abstract]
9. Shen, L., R. Lasser, M. Fanger. 1989. My43, a monoclonal antibody that reacts with human myeloid cells inhibits IgA binding and triggers function. J. Immunol. 143:4117.[Abstract]
10. Monteiro, R. C., H. Kubagawa, M. D. Cooper. 1990. Cellular distribution, regulation and biological nature of an Fc receptor in humans. J. Exp. Med. 171:597.[Abstract/Free Full Text]
11. Maliszewski, C. R., C. J. March, M. A. Schoenborn, S. Gimpel, L. Shen. 1990. Expression cloning of a human Fc receptor for IgA. J. Exp. Med. 172:1665.[Abstract/Free Full Text]
12. Gauldie, J., C. Richards, L. Lamontagne. 1983. Fc receptors for IgA and other immunoglobulins on resident and activated alveolar macrophages. Mol. Immunol. 20:1029.[Medline]
13. Gorter, A., P. S. Hiemstra, E. A. M. van der Voort, L. A. van Es, M. R. Daha. 1988. Binding of human IgA to rat peritoneal macrophages. Immunology 64:207.[Medline]
14. Gorter, A., P. S. Hiemstra, N. Klar-Mohamad, L. A. van Es, M. R. Daha. 1988. Binding, internalization and degradation of soluble aggregates of human secretory IgA by resident rat peritoneal macrophages. Immunology 64:703.[Medline]
15. Monteiro, R. C., R. W. Hostoffer, M. D. Cooper, J. R. Bonner, G. L. Gartland, H. Kubagawa. 1993. Definition of immunoglobulin A receptors on eosinophils and their enhanced expression in allergic individuals. J. Clin. Invest. 92:1681.
16. Sancho, J., E. Gonzalez, J. Egido. 1986. The importance of the Fc receptors for IgA in the recognition of IgA by mouse liver cells: its comparison with carbohydrate and secretory component receptors. Immunology 57:37.[Medline]
17. Mu, J. Z., M. Gordon, J. S. Shao, D. H. Alpers. 1997. Apical expression of functional asialoglycoprotein receptor in the human intestinal cell line HT-29. Gastroenterology 113:1501.[Medline]
18. Tomana, M., J. Zikan., Z. Moldoveanu, J. Kulhavy, C. Bennett, J. Mestecky. 1993. Interactions of cell-surface galactosyltransferase with immunoglobulins. Mol. Immunol. 30:265.[Medline]
19. Millet, I., F. Briere, C. Vincent, F. Rousset, C. Andreoni, J. E. de Vries, J. P. Revillard. 1989. Spontaneous expression of low affinity Fc receptor for IgA (FcR) on human B cell lines. Clin. Exp. Immunol. 76:268.[Medline]
20. Rao, T. D., A. A. Naghazachi, A. V. Gonzalez, J. M. Phillips-Quagliata. 1992. A novel IgA receptor expressed on murine B cell lymphoma. J. Immunol. 149:143.[Abstract]
21. Gomez-Guerrero, C., E. Gonzalez, J. Egido. 1993. Evidence for a specific IgA receptor in rat and human mesangial cells. J. Immunol. 151:7172.[Abstract]
22. Diven, S. C., C. R. Caflisch, D. K. Hammond, P. H. Weigel, J. A. Okra, R. M. Goldblum. 1998. IgA induced activation of human mesangial cells: independent of FcR1 (CD89). Kidney Int. 54:837.[Medline]
23. Crago, S. S., R. Kulhavy, S. J. Prince, J. Mestecky. 1978. Secretory component on epithelial cells is a surface receptor for polymeric immunoglobulins. J. Exp. Med. 147:1832.[Abstract/Free Full Text]
24. Augeron, C., C. L. Laboisse. 1984. Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate. Cancer Res. 44:3961.[Abstract/Free Full Text]
25. Weigel, P. H., J. A. Oka. 1982. Endocytosis and degradation mediated by the asialoglycoprotein receptor in isolated rat hepatocytes. J. Biol. Chem. 257:1201.[Free Full Text]
26. Maliszewski, C. R., C. J. March, M. A. Schoenborn, S. Gimpel, L. Shen. 1990. Expression cloning of a human Fc receptor for IgA. J. Exp. Med. 172:1665.
27. Scatchard, G.. 1949. The attractions of proteins for small molecules and ions. Ann. NY Acad. Sci. 551:660.
28. Weigel, P. H., J. A. Oka. 1982. Endocytosis and degradation mediated by the asialoglycoprotein receptor in isolated rat hepatocytes. J. Biol. Chem. 257:1201.
29. Abu-Ghazaleh, R. I., T. Fujisawa, J. Mestecky, R. A. Kyle, G. J. Gleich. 1989. IgA-induced eosinophil degranulation. J. Immunol. 142:2393.[Abstract]
30. Lamkhioued, B., A. S. Gounni, V. Gruart, A. Pierce, A. Capron, M. Capron. 1995. Human eosinophils express a receptor for secretory component: role in secretory IgA-dependent activation. Eur. J. Immunol. 25:117.[Medline]
31. Raghavan, M., P. J. Bjorkman. 1996. Fc receptors and their interactions with immunoglobulins. Annu. Rev. Cell Dev. Biol. 12:181.[Medline]
32. Goldblum, R. M., L. A. Hanson, P. Brandtzaeg. 1996. The mucosal defense system. E. R. Stiehm, ed. Immunologic Disorders in Infants and Children 159. W. B. Saunders, Philadelphia.
33. Mostov, K. E., M. H. Cardone. 1992. regulation of protein traffic in polarized epithelial cells. BioEssays 17:129.
34. Story, C. M., J.E. Mikulska, N. E. Simister. 1994. A major histocompatibility complex class I-like Fc receptor cloned from human placenta: possible role in transfer of immunoglobulin G from mother to fetus. J. Exp. Med. 180:2377.[Abstract/Free Full Text]
35. Tomana, M., R. Kulhavy, J. Mestecky. 1988. Receptor mediated binding and uptake of immunoglobulin A by human liver. Gastroenterology 94:762.[Medline]

This article has been cited by other articles:

				B. J. Davids, J. E. D. Palm, M. P. Housley, J. R. Smith, Y. S. Andersen, M. G. Martin, B. A. Hendrickson, F.-E. Johansen, S. G. Svard, F. D. Gillin, et al. Polymeric Immunoglobulin Receptor in Intestinal Immune Defense against the Lumen-Dwelling Protozoan Parasite Giardia J. Immunol., November 1, 2006; 177(9): 6281 - 6290. [Abstract] [Full Text] [PDF]

				N. J. Mantis, M. C. Cheung, K. R. Chintalacharuvu, J. Rey, B. Corthesy, and M. R. Neutra Selective Adherence of IgA to Murine Peyer's Patch M Cells: Evidence for a Novel IgA Receptor J. Immunol., August 15, 2002; 169(4): 1844 - 1851. [Abstract] [Full Text] [PDF]

				I. C. Moura, M. N. Centelles, M. Arcos-Fajardo, D. M. Malheiros, J. F. Collawn, M. D. Cooper, and R. C. Monteiro Identification of the Transferrin Receptor as a Novel Immunoglobulin (Ig)a1 Receptor and Its Enhanced Expression on Mesangial Cells in Iga Nephropathy J. Exp. Med., August 20, 2001; 194(4): 417 - 426. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kitamura, T. Articles by Goldblum, R. M. Search for Related Content PubMed PubMed Citation Articles by Kitamura, T. Articles by Goldblum, R. M.