BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Sorting of the Human Folate Receptor in MDCK 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, P.C. (National Institutes of Health)
  • Published : 2004.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

The human folate receptor (hFR) is a glycosylphosphatidylinositol (GPI) linked plasma membrane protein that mediates delivery of folates into cells. We studied the sorting of the hFR using transfection of the hFR cDNA into MDCK cells. MDCK cells are polarized epithelial cells that preferentially sort GPI-linked proteins to their apical membrane. Unlike other GPI-tailed proteins, we found that in MDCK cells, hFR is functional on both the apical and basolateral surfaces. We verified that the same hFR cDNA that transfected into CHO cells produces the hFR protein that is GPI-linked. We also measured the hFR expression on the plasma membrane of type III paroxysmal nocturnal hemoglobinuria (PNH) human erythrocytes. PNH is a disease that is characterized by the inability of cells to express membrane proteins requiring a GPI anchor. Despite this defect, and different from other GPI-tailed proteins, we found similar levels of hFR in normal and type III PNH human erythrocytes. The results suggest the hypothesis that there may be multiple mechanisms for targeting hFR to the plasma membrane.

Keywords

References

  1. Antony, A. C., Bruno, E., Briddell, R. A., Brandt, J. E., Verma, R. S. and Hoffman, R. (1987) Effect of perturbation of specific folate receptors during in vitro erythropoiesis. J. Clin. Invest. 80, 1618-1623. https://doi.org/10.1172/JCI113249
  2. Brown, D. A. and Rose, J. K. (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544. https://doi.org/10.1016/0092-8674(92)90189-J
  3. Caplan, M. J., Anderson, H. C., Palade, G. E. and Jamieson, J. D. (1986) Intracellular sorting and polarized cell surface delivery of (Na+, K+) ATPase, an endogenous component of MDCK cell basolateral plasma membranes. Cell 46, 623-631. https://doi.org/10.1016/0092-8674(86)90888-3
  4. Chen, C. and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell Biol. 7, 2745-2752.
  5. Chow, F. L., Hall, S. E., Rosse, W.F. and Telen, M. J. (1986) Separation of the acetyl cholinesterase-deficient red cells in paroxysmal nocturnal hemoglobinuria. Blood 67, 893-897.
  6. Chung, K. N., Roberts, S., Kim, C. H., Kirassova, M., Trepel, J. and Elwood, P. C. (1995) Rapid turnover and impaired cellsurface 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
  7. 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
  8. Elwood, P. C. (1989) Molecular cloning and characterization of human folate-binding protein cDNA from placenta and malignant tissue culture (KB) cells. J. Biol. Chem. 264, 14893-14901.
  9. Elwood, P. C., Kane, M. A., Portillo, R. M. and Kolhouse, J. F. (1986) The isolation, characterization and comparison of the membrane-associated and soluble folate-binding proteins from human KB cells. J. Biol. Chem. 261, 15416-15423.
  10. Figini, M., Ferri, R., Mezzanzanica, D., Bagnoli, M., Luison, E., Miotti, S. and Canevari, S. (2003) Reversion of transformed phenotype in ovarian cancer cells by intracellular expression of anti folate receptor antibodies. Gene Ther. 10, 1018-1025. https://doi.org/10.1038/sj.gt.3301962
  11. Hwa, K. Y. (2001) Glycosyl phosphatidylinositol-linked glycoconjugates: structure, biosynthesis and function. Adv. Exp. Med. Biol. 491, 207-214. https://doi.org/10.1007/978-1-4615-1267-7_15
  12. Ju, S. K., Park, J. H., Na, S. Y., You, K. H., Kim, K. L. and Lee, M. K. (2001) Molecular cloning and recombinant expression of the long form of leptin receptor (Ob-Rb) cDNA as isolated from rat spleen . J. Biochem. Mol. Biol. 34, 156-165.
  13. Kane. M. A., Elwood, P. C., Portillo, R. M., Antony, A. C. and Kolhouse, J. F. (1986) The interrelationship of the soluble and membrane-associated folate-binding proteins in human KB cells. J. Biol. Chem. 261, 15625-15631.
  14. Kang, S. W., Cho, Y. W., Park, E. H., Shn, K. S. and Lim, C. J. (2001) Cloning and expression of alkaline phosphatase gene from Schizosaccharomyces pombe. J. Biochem. Mol. Biol. 34, 262-267.
  15. Kim, C. H., Park, Y. S., Chung, K. N. and Elwood, P. C. (2002) Sorting and function of the human folate receptor is independent of the caveolin expression in Fisher rat thyroid epithelial cells. J. Biochem. Mol. Biol. 35, 395-402. https://doi.org/10.5483/BMBRep.2002.35.4.395
  16. Kim, H. G., Lee, J. J., Park, E. H., Sa, J. H., Ahn, K. S. and Lim, C. J. (2001) Cloning and regulation of Schizosaccharomyces pombe gene encoding ribosomal protein L11. J. Biochem. Mol. Biol. 34, 379-384.
  17. Krauss, J. S. (2003) Laboratory diagnosis of paroxysmal nocturnal hemoglobinuria. Ann. Clin. Lab. Sci. 33, 401-406.
  18. Lacey, S. W., Sanders, J. M., Rothberg, K. G., Anderson, R. G. and Kamen, B. A. (1989) Complementary DNA for the folate binding protein correctly predicts anchoring to the membrane by glycosyl-phosphatidylinositol. J. Clin. Invest. 84, 715-720. https://doi.org/10.1172/JCI114220
  19. 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. Biol. 34, 182-187.
  20. Lisanti, M. P., Sargiacomo, M., Graeve, L., Saltiel, A. R. and Rodriguez-Boulan, E. (1988) Polarized apical distribution of glycosyl-phosphatidylinositol-anchored proteins in a renal epithelial cell line. Proc. Natl. Acad. Sci. USA 85, 9557-9561. https://doi.org/10.1073/pnas.85.24.9557
  21. Lu, S. Y., Qi, Y. P. and Gu, G. Q. (2002) Interaction of heliothis armigera nuclear polyhedrosis viral capsid protein with its host actin. J. Biochem. Mol. Biol. 35, 562-567. https://doi.org/10.5483/BMBRep.2002.35.6.562
  22. Luhrs, C. A. and Slomiany, B. L. (1989) A human membraneassociated folate binding protein is anchored by a glycosylphosphatidylinositol tail. J. Biol. Chem. 264, 21446-21449.
  23. Luhrs, C. A., Pitiranggon, P., da Costa, M., Rothenberg, S. P., Slomiany, B. L., Brink, L., Tous, G. I and Stein, S. (1987) Purified membrane and soluble folate binding proteins from cultured KB cells have similar amino acid compositions and molecular weights but differ in fatty acid acylation. Proc. Natl. Acad. Sci. USA 84, 6546-6549. https://doi.org/10.1073/pnas.84.18.6546
  24. Mahoney, J. F., Urakaze, M., Hall, S., DeGasperi, R., Chang, H. M., Sugiyama, E., Warren, C. D,, Borowitz, M., Nicholson-Weller, A. and Rosse, W. F. (1992) Defective glycosylphosphatidylinositol anchor synthesis in paroxysmal nocturnal hemoglobinuria granulocytes. Blood 79, 1400-1403.
  25. Nakagawa, Y., Okada, S., Hatano, M., Ebara, M., Saisho, H. and Tokuhisa, T. (2002) Downregulation of bcl-xL is relevant to UV-induced apoptosis in fibroblasts. J. Biochem. Mol. Biol. 35, 452-458. https://doi.org/10.5483/BMBRep.2002.35.5.452
  26. Ratnam, M., Hao, H., Zheng, X., Wang, H., Qi, H., Lee, R. and Pan, X. (2003) Receptor induction and targeted drug delivery: a new antileukaemia strategy. Expert Opin. Biol. Ther. 3, 563-574. https://doi.org/10.1517/14712598.3.4.563
  27. Rosse, W. F., Hoffman, S., Campbell, M., Borowitz, M., Moore, J. O. and Parker, C. J. (1991) The erythrocytes in paroxysmal nocturnal haemoglobinuria of intermediate sensitivity to complement lysis. Br. J. Haematol. 79, 99-107. https://doi.org/10.1111/j.1365-2141.1991.tb08014.x
  28. Sadasivan, E. and Rothenberg, S. P. (1989) The complete amino acid sequence of a human folate binding protein from KB cells determined from the cDNA. J. Biol. Chem. 264, 5806-5811.
  29. Schell, M. J., Maurice, M., Stieger, B. and Hubbard, A. L. (1992) 5'nucleotidase is sorted to the apical domain of hepatocytes via an indirect route. J. Cell Biol. 119, 1173-1182. https://doi.org/10.1083/jcb.119.5.1173
  30. Sinn, P. L., Hickey, M. A., Staber, P. D., Dylla, D. E., Jeffers, S. A., Davidson, B. L., Sanders, D. A. and McCray, P. B. (2003) Lentivirus vectors pseudotyped with filoviral envelope glycoproteins transduce airway epithelia from the apical surface independently of folate receptor alpha. J. Virol. 77, 5902-5910. https://doi.org/10.1128/JVI.77.10.5902-5910.2003
  31. Sloand, E. M., Fuhrer, M., Keyvanfar, K., Mainwaring, L., Maciejewski, J., Wang, Y., Johnson, S., Barrett, A. J. and Young, N. S. (2003) Cytogenetic abnormalities in paroxysmal nocturnal haemoglobinuria usually occur in haematopoietic cells that are glycosylphosphatidylinositol-anchored protein (GPI-AP) positive. Br. J. Haematol. 123, 173-176. https://doi.org/10.1046/j.1365-2141.2003.04562.x
  32. So, E. Y., Jang, J. H. and Lee, C. E. (2001) Cross-talk between STAT6 and Ras/MAPK pathway for the IL-4-mediated T cell survival. J. Biochem. Mol. Biol. 34, 578-583.
  33. Takeda, J., Miyata, T., Kawagoe, K., Iida, Y., Endo, Y., Fujita ,T., Takahashi, M., Kitani, T. and Kinoshita, T. (1993) Deficiency of the GPI anchor caused by a somatic mutation of the PIG-A gene in paroxysmal nocturnal hemoglobinuria. Cell 73, 703-711. https://doi.org/10.1016/0092-8674(93)90250-T
  34. Waxman, S. and Schreiber, C. (1980) Determination of folate by use of radioactive folate and binding proteins. Methods Enzymol. 66, 468-483. https://doi.org/10.1016/0076-6879(80)66490-8
  35. Wong, Y. W. and Low, M. G. (1992) Phospholipase resistance of the glycosyl-phosphatidylinositol membrane anchor on human alkaline phosphatase. Clin. Chem. 38, 2517-2525.