Ca2+-dependent calmodulin binding to FcRn affects immunoglobulin G transport in the transcytotic pathway

Molecular Biology of the Cell

Volumn 19, Issue 1, 2008, Pages 414-423

  Dickinson, Bonny L ^a,b   Claypool, Steven M ^c,d   D'Angelo, June A ^a,b   Aiken, Martha L ^a,b   Venu, Nanda ^d,e   Yen, Elizabeth H ^d,e   Wagner, Jessica S ^d,e,g   Borawski, Jason A ^d,e   Pierce, Amy T ^a,b   Hershberg, Robert ^f   Blumberg, Richard S ^c,g   Lencer, Wayne I ^d,e,g  

^a CHILDREN S HOSPITAL   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^g HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALMODULIN; FC RECEPTOR; IMMUNOGLOBULIN G; MUTANT PROTEIN; FC RECEPTOR, NEONATAL; HLA ANTIGEN CLASS 1;

ALPHA HELIX; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELL POLARITY; CELL SURFACE; CELL TRANSPORT; CONTROLLED STUDY; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN TRANSPORT; TRANSCYTOSIS; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMISTRY; CYTOLOGY; DOG; ENDOCYTOSIS; HALF LIFE TIME; HUMAN; INTESTINE; METABOLISM; MOLECULAR GENETICS; MOUSE; PROTEIN TERTIARY STRUCTURE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CALMODULIN; CELL LINE; CELL POLARITY; DOGS; ENDOCYTOSIS; HALF-LIFE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOGLOBULIN G; INTESTINES; LYSOSOMES; MICE; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, FC;

EID: 38749097778     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-07-0658     Document Type: Article

References (39)

1. Apodaca, G., Enrich, C., and Mostov, K. E. (1994). The calmodulin antagonist, W-13, alters transcytosis, recycling, and the morphology of the endocytic pathway in Madin-Darby canine kidney cells. J. Biol. Chem. 269, 19005-19013.
2. Bitonti, A. J. et al. (2004). Pulmonary delivery of an erythropoietin Fc fusion protein in non-human primates through an immunoglobulin transport pathway. Proc. Natl. Acad. Sci. USA 101, 9763-9768.
3. Borvak, J., Richardson, J., Medesan, C., Antohe, F., Radu, C., Simionescu, M., Ghetie, V., and Ward, E. S. (1998). Functional expression of the MHC class I-related receptor, FcRn, in endothelial cells of mice. Int. Immunol. 10, 1289-1298.
4. Burmeister, W. P., Gastinel, L. N., Simister, N. E., Blum, M. L., and Bjorkman, P. J. (1994). Crystal structure at 2.2 A resolution of the MHC-related neonatal Fc receptor. Nature 372, 336-343.
5. Chapin, S. J., Enrich, C., Aroeti, B., Havel, R. J., and Mostov, K. E. (1996). Calmodulin binds to the basolateral targeting signal of the polymeric immunoglobulin receptor. J. Biol. Chem. 271, 1336-1342.
6. Chin, D., and Means, A. R. (2000). Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10, 322-328.
7. Claypool, S. M., Dickinson, B. L., Wagner, J. S., Johansen, F.-E., Venu, N., Borawski, J. A., Lencer, W. I., and Blumberg, R. S. (2004). Bidirectional transepithelial IgG transport by a strongly polarized basolateral membrane Fc{gamma}-receptor. Mol. Biol. Cell 15, 1746-1759.
8. Claypool, S. M., Dickinson, B. L., Yoshida, M., Lencer, W. I., and Blumberg, R. S. (2002). Functional reconstitution of human FcRn in Madin-Darby canine kidney cells requires co-expressed human beta 2-microglobulin. J. Biol. Chem. 277, 28038-28050.
9. Colgan, S. P., Hershberg, R. M., Furuta, G. T., and Blumberg, R. S. (1999). Ligation of intestinal epithelial CD1d induces bioactive IL-10, critical role of the cytoplasmic tail in autocrine signaling. Proc. Natl. Acad. Sci. USA 96, 13938-13943.
10. Dickinson, B. L., Badizadegan, K., Wu, Z., Ahouse, J. C., Zhu, X., Simister, N. E., Blumberg, R. S., and Lencer, W. I. (1999). Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J. Clin. Investig. 104, 903-911.
11. Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., Evans, P. R., and McMahon, H. T. (2002). Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366.
12. Graff, J. M., Young, T. N., Johnson, J. D., and Blackshear, P. J. (1989). Phosphorylation-regulated calmodulin binding to a prominent cellular substrate for protein kinase C. J. Biol. Chem. 264, 21818-21823.
13. Grasso, J. A., Bruno, M., Yates, A. A., Wei, L. T., and Epstein, P. M. (1990). Calmodulin dependence of transferrin receptor recycling in rat reticulocytes. Biochem. J. 266, 261-272.
14. Hershberg, R. M., Framson, P. E., Cho, D. H., Lee, L. Y., Kovats, S., Beitz, J., Blum, J. S., and Nepom, G. T. (1997). Intestinal epithelial cells use two distinct pathways for HLA class II antigen processing. J. Clin. Invest. 100, 204-215.
15. Huber, A. H., Kelley, R. F., Gastinel, L. N., and Bjorkman, P. J. (1993). Crystallization and stoichiometry of binding of a complex between a rat intestinal Fc receptor and Fc. J. Mol. Biol. 230, 1077-1083.
16. Huber, L. A., Fialka, I., Paiha, K., Hunziker, W., Sacks, D. B., Bahler, M., Way, M., Gagescu, R., and Gruenberg, J. (2000). Both calmodulin and the unconventional myosin Myr4 regulate membrane trafficking along the recycling pathway of MDCK cells. Traffic 1, 494-503.
17. Hunt, R. C., and Marshall-Carlson, L. (1986). Internalization and recycling of transferrin and its receptor. Effect of trifluoperazine on recycling in human erythroleukemic cells. J. Biol. Chem. 261, 3681-3686.
18. Hunziker, W. (1994). The calmodulin antagonist W-7 affects transcytosis, lysosomal transport, and recycling but not endocytosis. J. Biol. Chem. 269, 29003-29009.
19. Kegel, K. B. et al. (2005). Huntingtin Associates with Acidic Phospholipids at the Plasma Membrane. J. Biol. Chem. 280, 36464-36473.
20. Lee, M. C., Orci, L., Hamamoto, S., Futai, E., Ravazzola, M., and Schekman, R. (2005). Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 122, 605-617.
21. McCarthy, K. M., Lam, M., Subramanian, L., Shakya, R., Wu, Z., Newton, E. E., and Simister, N. E. (2001). Effects of mutations in potential phosphorylation sites on transcytosis of FcRn. J. Cell Sci. 114, 1591-1598.
22. McIlroy, B. K., Walters, J. D., Blackshear, P. J., and Johnson, J. D. (1991). Phosphorylation-dependent binding of a synthetic MARCKS peptide to calmodulin. J. Biol. Chem. 266, 4959-4964.
23. McMahon, H. T., and Gallop, J. L. (2005). Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590-596.
24. Nakanishi, H., de los Santos, P., and Neiman, A. M. (2004). Positive and negative regulation of a SNARE protein by control of intracellular localization. Mol. Biol. Cell 15, 1802-1815.
25. Ober, R. J., Martinez, C., Vaccaro, C., Zhou, J., and Ward, E. S. (2004). Visualizing the site and dynamics of IgG salvage by the MHC class I-related receptor, FcRn. J. Immunol. 172, 2021-2029.
26. Raghavan, M., Gastinel, L. N., and Bjorkman, P. J. (1993). The class I major histocompatibility complex related Fc receptor shows pH-dependent stability differences correlating with immunoglobulin binding and release. Biochemistry 32, 8654-8660.
27. Rhoads, A., and Friedberg, F. (1997). Sequence motifs for calmodulin recognition. FASEB J. 11, 331-340.
28. Rodewald, R. (1976). pH-dependent binding of immunoglobulins to intestinal cells of the neonatal rat. J. Cell Biol. 71, 666-669.
29. Sainte-Marie, J., Lafont, V., Pecheur, E. I., Favero, J., Philippot, J. R., and Bienvenue, A. (1997). Transferrin receptor functions as a signal-transduction molecule for its own recycling via increases in the internal Ca2+ concentration. Eur. J. Biochem. 250, 689-697.
30. Spiekermann, G. M., Finn, P. W., Ward, E. S., Dumont, J., Dickinson, B. L., Blumberg, R. S., and Lencer, W. I. (2002). Receptor-mediated immunoglobulin G transport across mucosal barriers in adult life: functional expression of FcRn in the mammalian lung. J. Exp. Med. 196, 303-310.
31. Stefaner, I., Praetor, A., and 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.
32. Swierczynski, S. L., and Blackshear, P. J. (1996). Myristoylation- dependent and electrostatic interactions exert independent effects on the membrane association of the myristoylated alanine-rich protein kinase C substrate protein in intact cells. J. Biol. Chem. 271, 23424-23430.
33. Taniguchi, H., and Manenti, S. (1993). Interaction of myristoylated alanine-rich protein kinase C substrate (MARCKS) with membrane phospholipids. J. Biol. Chem. 268, 9960-9963.
34. Ward, E. S., Martinez, C., Vaccaro, C., Zhou, J., Tang, Q., and Ober, R. J. (2005). From sorting endosomes to exocytosis: association of Rab4 and Rab11 GTPases with the Fc receptor, FcRn, during recycling. Mol. Biol. Cell 16, 2028-2038.
35. Ward, E. S., Zhou, J., Ghetie, V., and Ober, R. J. (2003). Evidence to support the cellular mechanism involved in serum IgG homeostasis in humans. Int. Immunol. 15, 187-195.
36. Wu, Z., and Simister, N. E. (2001). Tryptophan- and dileucine-based endocytosis signals in the neonatal Fc receptor. J. Biol. Chem. 276, 5240-5247.
37. Yoshida, M., Claypool, S. M., Wagner, J. S., Mizoguchi, E., Mizoguchi, A., Roopenian, D. C., Lencer, W. I., and Blumberg, R. S. (2004). Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 20, 769-783.
38. Yoshida, M. et al. (2006). Neonatal Fc receptor for IgG regulates mucosal immune responses to luminal bacteria. J. Clin. Invest. 116, 2142-2151.
39. Zhao, Y., Kacskovics, I., Hao, Z., and Hammarstrom, L. (2003). Presence of the di-leucine motif in the cytoplasmic tail of the pig FcRn α chain. Vet. Immunol. Immunopathol. 96, 229-233.