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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Sorting and Function of the Human Folate Receptor Is Independent of the Caveolin Expression in Fisher Rat Thyroid Epithelial Cells

  • Kim, Chong-Ho (Department of Clinical Pathology, Wonkwang Health Science College) ;
  • Park, Young-Soon (Division of Biological Science, Wonkwang University) ;
  • Chung, Koong-Nah (Department of Clinical Pathology, Wonkwang Health Science College) ;
  • Elwood, Patrick C. (National Institutes of Health)
  • Published : 2002.07.31
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Abstract

Caveolae are small, flask-shaped, non-clathrin coated invaginations of the plasma membrane of many mammalian cells. Caveolae have a coat that includes caveolin. They have been implicated in numerous cellular processes, including potocytosis. Since the human folate receptor (hFR) and other glycosyl-phosphatidylinositol (GPI)-tailed proteins have been co-localized to caveolae, we studied the caveolin role in the hFR function by transfecting hFR and/or caveolin cDNA into Fischer rat thyroid epithelial (FRT) cells that normally do not express detectable levels of either protein. We isolated and characterized stable clones as follows: they express (1) high levels of caveolin alone, (2) hFR and caveolin, or (3) hFR alone. We discovered that hFR is correctly processed, sorted, and anchored by a GPI tail to the plasma membrane in FRT cells. No difference in the total folic acid binding or cell surface folic acid binding activity were found between the FRT cells that were transfected with hFR, or cells that were transfected with hFR and caveolin. The hFR that was expressed on the cell surface of clones that were transfected with hFR was also sensitive to phosphatidylinositol-specific phospholipase C (PI-PLC) release, and incorporated radiolabeled ethanolamine that supports the attachment of a GPI-tail on hFR. We conclude that the processing, sorting, and function of hFR is independent on the caveolin expression in FRT cells.

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References

  1. Anderson, R. G., Kamen, B. A., Rothberg, K. G. and Lacey, S. W. (1992) Potocytosis: sequestration and transport of small molecules by caveolae. Science 255, 410-411. https://doi.org/10.1126/science.1310359
  2. Antony, A. C. (1992) The biological chemistry of folate receptors. Blood 79, 2807-2820.
  3. Bae, J. S. and Lee, S. T. (2001) The human PTK6 interacts with a 23-kDa tyrosine-phophorylated protein and is localized in cytoplasm in breast in carcinoma T-47D cells. J. Biochem. Mol. Biol. 34, 33-38.
  4. Bagnoli, M., Tomassetti, A., Figini, M., Fiati, S., Dolo, V, Canevari, S. and Miotti, S. (2000) Downmodulation of caveolin-1 expression in human ovarian carcinoma is directly related to alpha-folate receptor over expression. Oncogene 19, 4754-4763. https://doi.org/10.1038/sj.onc.1203839
  5. Bist, A., Fielding, C. J. and Fielding, P. E. (2000) p53 regulates caveolin gene transcription, cell cholesterol, and growth by a novel mechanism. Biochemistry 39, 1966-1972. https://doi.org/10.1021/bi991721h
  6. Bridges, C. C., EI-Sherbeny, A., Roon, P., Ola, M. S., Kekuda, R, Ganapathy, V, Camero, R S., Cameron, P. L. and Smith, S. B. (2001) A comparision of caveolae and caveolin-1 to folate receptor alpha in retina and retinal pigment epithelium. Histochem. J. 33, 149-158. https://doi.org/10.1023/A:1017991925821
  7. Cain, T. J., Liu, Y., Takizawa, T. and Robinson, J. M. (1995) Solubilization of glycosylphosphat-idylinositol-anchored proteins in quiescent and stimulated neutrophils. Biochim. Biophys. Acta 1235, 69-78. https://doi.org/10.1016/0005-2736(94)00308-C
  8. Chung, K. N., Paik, T. H., Robert, S., Kim, C. H., Kirassova M., Weinstein, J. N., Trepel, J. B. and Elwood, P. C. (1994) Site-directed mutagenesis of tryptopan residues to conserved hydropholic residues inhibits the progressing of human KB cells folate receptor. Arch. Biochem. Biophy. 315, 407-414. https://doi.org/10.1006/abbi.1994.1518
  9. Chung, K. N., Roberts, S., Kim, C. H., Kirassova, M., Trepel, J. and Elwood, P. C. (1995) Rapid turnover and impaired cell-surface expression of the human folate receptor in mouse L ($tk^{-}$) fibroblasts, a cell line defective in glycosylphosphatidylinositol tail synthesis. Arch. Biochem. Biophys. 322, 228-234. https://doi.org/10.1006/abbi.1995.1456
  10. Chung, K. N., Saikawa, Y., Paik, T. H., Dixon, K. H., Mulligan, T. and Cowan, K. H. (1993) Stable transfectants of human MCF-7 breast cancer cells with increased levels of the human folate receptor exhibit an increased sensitivity to antifolates. J. Clin. Invest. 91, 1289-1294. https://doi.org/10.1172/JCI116327
  11. Elwood, P. C., Kane, M. A., Portillo, R. M. and Kolhouse, J. E (1986) The isolation, characterization and comparision of the membrane-associated and soluble folate-binding proteins from human KB cells. J. BioI. Chem. 261, 15416-15423.
  12. Elwood, P. C. (1989) Molecular cloning and characterization of human folate-binding protein cDNA from placenta and malignant tissue culture (KB) cells. J. BioI. Chem. 264, 14893-14901.
  13. Engelman, J. A., Zhang, X. L. and Lisanti, M. P. (1999) Sequence and detailed organization of the human caveolin-` and -2 genes located near the D7S522 locus (7q31.1). Methylation of a CpG island in the 5' promoter region of the caveolin-1 gene in human breast cancer cell lines. FEBS Left. 448, 221-230. https://doi.org/10.1016/S0014-5793(99)00365-8
  14. Fujimoto, T., Kogo, H., Nomura, R and Une, T. (2000) Isoforms of caveolin-1, and caveolar structure. J. Cell Sci. 113, 3509-3517.
  15. Galbiati, E, Yolonte, D., Minetti, C., Chu, J. B. and Lisanti, M. P. (1999) Phenotypic behavior of caveolin-3 mutations that cause autosomal dominant limb girdle muscular dystrophy (LGMD-1C). Retention of LGMD-1C caveolin-3 mutants within the Golgi complex. J. Biol. Chem. 274, 25632-25641. https://doi.org/10.1074/jbc.274.36.25632
  16. Glenney, J. Rand Soppet, D. (1992) Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in RSY-transformed fibroblasts. Proc. Natl. Acad. Sci. USA 89, 10517-10521. https://doi.org/10.1073/pnas.89.21.10517
  17. Henderson, G. B. (1990) Folate-binding proteins. Annu. Rev. Nutr. 10, 319-335. https://doi.org/10.1146/annurev.nu.10.070190.001535
  18. Kandror, K. V, Stephens, J. M. and Pilch, P. E (1995) Expression and compartmentalization of caveolin in adipose cells: coordinate regulation with and structural segregation from GLUT4. J. Cell. Biol. 129, 999-1006. https://doi.org/10.1083/jcb.129.4.999
  19. Kim, J. H ., Han, J. M., Lee, S., Kim, Y.. Lee, T. G., Park, J. B., Lee, S. D., Suh, P. G. and Ryu, S. H. (1999) Phospholipase D1 in caveolae: regulation by protein kinase Calpha and caveolin-1. Biochemistry 38. 3763-3769. https://doi.org/10.1021/bi982478+
  20. Lee, B. D ., Kim. Y., Han. J. M., Suh, P. G. and Ryu. S. H. (2001) Carbachol-induced Phosphorylation of Phospholipase D1 through Protein Kinase C is required for the Activation in COS-7 cells. J. Biochem. Mol. BioI. 34, 182-187.
  21. Matsue, H., Rothberg, K. G., Takashima, A.. Kamen, B. A., Anderson, R. G. and Lacey, S. W. (1992) Folate receptor allows cells to grow in low concentrations of 5-methyl tetrahydrofolate. Proc. Nati. Acad. Sci. USA 89, 6006-6009. https://doi.org/10.1073/pnas.89.13.6006
  22. Mayor. S. and Maxfield. E R (1995) Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol. BioI. Cell 6, 929-944. https://doi.org/10.1091/mbc.6.7.929
  23. Miotti, S., Bagnoli. M., Tomassetti, A., Colnaghi. M. I. and Canevari, S. (2000) Interaction of folate receptor with signaling molecules Iyn and G(alpha)(i-3) in detergent resistant complexes from the ovary carcinoma cell line IGROV1. J. Cell Sci. 2. 349-357.
  24. Oh, P. and Schnitzer. J. E. (2001) Segregation of heterotrimeric G proteins in cell surface microdomains. Gq binds caveolin to concentrate in caveolae, whereas Gi and Gs target lipid rafts by default. Mol. Biol. Cell 12, 685-698. https://doi.org/10.1091/mbc.12.3.685
  25. Park, W. Y., Cho, K. A.. Park. J. S., Kim, D. I. and Park, S. C. (2001) Attenuation of EGF signaling in senescent cells by caveolin. Ann. N. Y. Acad. Sci. 928, 79-84. https://doi.org/10.1111/j.1749-6632.2001.tb05638.x
  26. Rijnboutt, S., Jansen, G., Posthuma, G., Hynes, J. B., Schornagel, J. H. and Strous, G. J. (1996) Endocytosis of GPI-linked membrane folate receptor-alpha. J. Cell Biol. 132, 35-47. https://doi.org/10.1083/jcb.132.1.35
  27. Parton, R G. (1994) Ultrastructural localization of gangliosides: GM1 is concentrated in caveolae. J. Histochem. Cytochem. 42, 155-166. https://doi.org/10.1177/42.2.8288861
  28. Parton, R G., Joggerst, B. and Simons, K. (1994) Regulated internalization of caveolae. J. Cell Biol. 127, 1199-1215. https://doi.org/10.1083/jcb.127.5.1199
  29. Ryu, J. and Jung, C. Y. (2001) Compartmental analysis of the insulin-induced GLUT4 recruitment in adipocytes. J. Biochem. Mol. BioI. 34, 285-292.
  30. Sargiacomo, M., Sudol, M ., Tang, Z. L. and Lisanti, M. P. (1993) Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell BioI. 122, 789-807. https://doi.org/10.1083/jcb.122.4.789
  31. Scherer, P. E., Lisanti, M. P., Baldini, G., Sargiacomo, M., Corley-Mastick, C. and Lodish, H. F. (1994) Induction of caveolin during adipogenesis and association of GLUT4 with caveolin-rich vesicles. J. Cell Biol. 127, 1233-1243. https://doi.org/10.1083/jcb.127.5.1233
  32. Schnitzer,J. E., Oh, P., Jacobson, B. S. and Dvorak, A. M. (1995) Caveolae from luminal plasma lemma of rat lung endothelium: microdomains enriched in caveolin, Ca(2+)-ATPase, and inositol triphosphate receptor. Proc. Natl. AcM. Sci. USA 92, 1759-1763. https://doi.org/10.1073/pnas.92.5.1759
  33. Shu, L., Lee, l., Chang, Y, Holzman, L. B., Edwards, C. A., Shelden, E. and Shyman, J. A. (2000) Caveolar structure and protein sorting are maintained in NIH3T3 cells independent of glycosphingolipid depletion. Arch. Biochem. Biophys. 373, 83-90. https://doi.org/10.1006/abbi.1999.1553
  34. Smart, E. J., Foster, D. C., Ying, Y. S., Kamen, B. A. and Anderson, R. G. (1994) Protein kinase C activators inhibit receptor-mediated potocytosis by preventing internalization of caveolae. J. Cell Biol. 124, 307-313. https://doi.org/10.1083/jcb.124.3.307
  35. Song. J. H., Park, H. H., Park, H. J., Han, M. Y., Sung-Hoon Kim, S. Y and Lee, C. E. (2001) Role of STAT3 as a Molecular Adaptor in Cell Growth Signaling: Interaction with Ras and other STAT Proteins J. Biochem. Mol. Biol. 34, 484-488.
  36. Wu, M., Fan, J., Gunning, W. and Ratnam, M. (1997) Clustering of GPI-anchored folate receptor independent of both cross-linking and association with caveolin. J. Membr. Biol. 159, 137-147. https://doi.org/10.1007/s002329900277
  37. Yamada, E. (1955) The fine structure of the gall bladder epithelium of the mouse. J. Biophys. Biochem. Cytol. J, 441-458.

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