Endocytosis of GPI-linked membrane folate receptor-α

Journal of Cell Biology

Volumn 132, Issue 1-2, 1996, Pages 35-47

  Rijnboutt, Simon ^a   Jansen, Gerrit ^b   Posthuma, George ^a   Hynes, John B ^d   Schornagel, Jan H ^c   Strous, Ger J ^a,e  

^a UTRECHT UNIVERSITY   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLTETRAHYDROFOLIC ACID; GAMMA GLUTAMYL HYDROLASE; TRITON X 100;

AMINO ACID ANALYSIS; AMINO ACID SYNTHESIS; ANIMAL CELL; ANION EXCHANGE; ARTICLE; ENDOCYTOSIS; ENDOSOME; IMMUNOELECTRON MICROSCOPY; NONHUMAN; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; TRANSPORT KINETICS;

ANIMALIA;

EID: 0030046514     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.132.1.35     Document Type: Article

References (88)

1. Ahle, S., A. Mann, U. Eichelsbacher, and E. Ungewickell, 1988. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane EMBO (Eur. Mol Biol Organ) J. 7:919-930.
2. Alberti, S., S. Miotti, M. Fornaro, L. Mantovani, S. Walter, S. Canevari, S. Menard, and M. I. Colnaghi. 1990. The Ca-MOv18 molecule, a cell-surface marker of human ovarian carcinomas, is anchored to the cell membrane by phosphatidylinositol. Biochem. Biophys. Res Commun 171:1051-1055.
3. Anderson, R. G. W. 1993a. Plasmalemmal caveolae and GPI-anchored membrane proteins. Curr. Opin. Cell Biol. 5:647-652
4. Anderson, R. G. W. 1993b. Caveolae: where incoming and outgoing messengers meet Proc. Natl Acad. Sci. USA. 90:10909-10913.
5. Antony, A. C. 1992. The biological chemistry of folate receptors. Blood. 79: 2807-2820.
6. Antony, A C., M. A. Kane, R. M. Portillo, P. C. Elwood, and J. F. Kolhouse. 1985 Studies of the role of a particulate folate binding protein in the uptake of 5-methyltetrahydrofolate by cultured human KB cells. J. Biol Chem. 260 14911-14917.
7. Antony, A. C., R. A. Briddel, J E. Brandt, J. E. Straneva, R. S. Verma, M. E. Miller, L A. Kalasinski, and R. Hoffman. 1991. Megaloblastic hematopoiesis in vitro; interaction of anti-folate receptor antibodies with hematopoietic progenitor cells leads to a proliferative response independent of megaloblastic changes. J Clin. Invest 87:313-325.
8. Antony, A. C. E. Bruno, R A. Briddell, J. E. Brandt, R. S. Verma, and R. Hoffman. 1987. Effect of perturbation of specific folate receptors during in vitro erythropoiesis. J. Clin. Invest. 80:1618-1623.
9. Bamezai, A , V. S Goldmacher, and K. L. Rock. 1992. Internalization of glycosyl-phosphatidylinositol (GPI)-anchored lymphocyte proteins II. GPI-anchored and transmembrane molecules internalize through distinct pathways. Eur. J. Immunol. 22:15-21.
10. Bertino, J. R. 1993. Ode to methotrexate. J Clin. Oncol. 11:5-14.
11. Brigle, K. E., E. H. Westin, M. T Houghton, and I. D. Goldman. 1991. Characterization of two cDNAs encoding folate-binding proteins from L1210 murine leukemia cells. J Biol. Chem 266:17243-17249.
12. Brown, D. A., and J K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:533-544.
13. Campbell, I. G., T. A. Jones, W. D. Foulkes, and J. Trowsdale. 1991. Folate-binding protein is a marker for ovarian cancer. Cancer Res. 51:5329-5338.
14. Cerneus, D. P., E. Ueffing, G. Posthuma, G. J. Strous, and A. vanderEnde, 1993. Detergent-insolubility of alkaline phosphatase during biosynthetic transport and endocytosis: role of cholesterol. J. Biol. Chem 268.3150-3155
15. Chang, W J , Y S. Ying, K. G. Rothberg, N. M. Hooper, A. J. Turner, H. A. Gambliel, J. De Gunsburg, S. M Mumby, A. G. Gilman, and R. G. W. Anderson. 1994. Purification and characterization of smooth muscle cell caveolae. J. Cell Biol 126 127-138.
16. Cinek, T., and V. Horejsí. 1992. The nature of large noncovalent complexes containing glycosyl-phosphatidylinositol-anchored membrane glycoproteins and protein tyrosine kinases. J. Immunol. 149:2262-2270.
17. Dixon, K. H., B. C. Lanpher, J. Chiu, K. Kelley, and K. H. Cowan. 1994. A novel cDNA restores reduced folate carrier activity and methotrexate sensitivity to transport deficient cells. J Biol Chem. 269:17-20.
18. Draberova, L., and P. Draber. 1993. Thy-1 glycoprotein and src-like protein tyrosine kinase p53/56 lyn are associated in large detergent-resistant complexes in rat basophilic leukemia cells. Proc. Natl. Acad. Sci. USA. 90:3611-3615.
19. Dupree, P., R. G. Parton, G. Raposo, T. V. Kurzchalia, and K. Simons. 1993. Caveolae and sorting in the trans-Golgi network of epithelial cells. EMBO (Eur Mol. Biol. Organ.) J. 12:1597-1605.
20. Elwood P. C. 1989. Molecular cloning and characterization of the human folate-binding protein cDNA from placenta and malignant tissue culture (KB) cells. J. Biol. Chem. 264:14893-14901
21. Elwood, P. C., M. A. Kane, R. M. Portillo, and J. F. Kolhouse. 1986. The isolation, characterisation, and comparison of the membrane-associated and soluble folate-binding proteins from human KB Cells. J Biol. Chem. 261: 15416-15423.
22. Fiedler, K., T. Kobayashi, T. V. Kurzchalia, and K. Simons. 1993. Glycosphingolipid-enriched, detergent-insoluble complexes in protein sorting in epithelial cells. Biochemistry. 32:6365-6373.
23. Fra, A. M., E. Williamson, K. Simons, and R. G. Parton. 1994. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269:30745-30748.
24. Freisheim, J. H., E M. Price, and M. Ratnam 1989. Folate coenzyme and anti-folate transport proteins in normal and neoplastic cells. Adv. Enz. Regul. 29: 13-26.
25. Freisheim, J. H., M. Ratnam, T. P. McAlinden, K. M. R. Prasad, F E. Williams, G. R. Westerhof, J. H. Schornagel, and G. Jansen 1992. Molecular events in the membrane transport of methotrexate in human CCRF-CEM leukemia cell lines. Adv Enz. Regul. 32:17-31.
26. Fujimoto, T. 1993. Calcium pump of the plasma membrane is localized in caveolae. J Cell Biol. 120:1147-1157.
27. Fujimoto, T , S. Nakade, A. Miyawaki, K. Mikoshiba, and K. Ogawa. 1992. Localization of inositol 1,4,5,-triphosphate receptor-like protein in plasmalemmal caveolae. J. Cell Biol 119:1507-1513.
28. Garcia, M., C. Mirre, A. Quaroni, H. Reggio, and A. Lebivic 1993. GPI-anchored proteins associate to form microdomains during their intracellular transport in caco-2 cells. J. Cell Sci. 104:1281-1290.
29. Geuze, H. J., J. W. Slot, P. A. vanderLey, and R. C. T. Scheffer. 1981. Use of colloidal gold particles in double labeling immunoelectron microscopy on ultrathin frozen tissue sections. J. Cell Biol. 89:653-665.
30. Glenney, J. R. 1992. The sequence of human caveolin reveals identity with VIP21, a component of transport vesicles. FEBS Lett. 314:45-48.
31. Glenney, J. R., and D. Soppet. 1992. Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in RSV-transformed fibroblasts. Proc. Natl. Acad Sci. USA. 89: 10517-10521.
32. Henderson, G. A., J. M. Tsuji, and H. P. Kumar. 1986. Characterization of the individual transport routes that mediate the influx and efflux of methotrexate in CCRF-CEM human lymphoblastic cells Cancer Res. 46:1633-1638.
33. Henderson, G. B. 1990. Folate binding proteins. Ann. Rev. Nutr. 10:319-335.
34. Hjelle, J. T., E I Christensen, F. A. Carone, and J. Selhub. 1991. Cell fractionation and electron microscope studies of kidney folate-binding protein Amer. J. Physiol. 260:C338-C346
35. Jansen, G., I. Kathmann, B. C. Rademaker, B. J. M. Braakhuis, G. R. Westerhof, G. Rijksrn, and J. H. Schornagel 1989a. Expression of folate binding protein in L1210 cells grown in low folate medium. Cancer Res. 49:1959-1963.
36. Jansen, G., G R. Westerhof, I. Kathmann, B. C. Rademaker, G. Rijksen, and J. H. Schornagel. 1989b. Identification of a membrane-associated folate-binding protein in human leukemic CCRF-CEM cells with transport related methotrexate resistance. Cancer Res. 49:2455-2459.
37. Jansen, G., J. H Schornagel, G. R. Westerhof, G. Rijksen, D R. Newell, and A. L Jackman 1990a. Multiple membrane transport systems for the uptake of folate-based thymidylate synthase inhibitors. Cancer Res. 50:7544-7548.
38. Jansen, G , G. R. Westerhof, M. J. A. Jarmuszewski, I. Kathmann, G. Rijksen, and J. H. Schornagel. 1990b. Methotrexate transport in variant human CCRF-CEM leukemia cells with elevated levels of the reduced folate carrier. J. Biol. Chem. 265:18272-18277.
39. Kamen, B. A., M. T Wang, A. J. Streckfuss, X. Peryea, and R. G. W. Anderson. 1988. Delivery of folates to the cytoplasm of MA 104 cells is mediated by a surface membrane receptor that recycles. J. Biol. Chem. 263:13602-13609
40. Kamen, B. A., A K. Smith, and R G W Anderson 1991. The folate receptor works in tandem with a probenecid-sensitive carrier in MA104 cells in vitro. J. Clin. Invest. 87:1442-1449
41. Keller, G. A., M. W. Siegel, and I. W. Caras, 1992. Endocytosis of glycophospholipid-anchored and transmembrane forms of CD4 by different endocytic pathways. EMBO (Eur. Mol. Biol. Organ) J. 11:863-874
42. Kurzchalia, T. V., P. Dupree, R. G. Parton, R. Kellner, H. Virta, M. Lehnert, and K. Simons 1992. VIP-21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles. J Cell Biol. 118: 1003-1014
43. Lacey, S. W., J. M. Sanders, K G. Rothberg, R G. W. Anderson, and B. A. Kamen. 1989. Complementary DNA for the folate binding protein correctly predicts anchoring to the membrane by phosphatidylinositol. J. Clin Invest. 84:715-720
44. Lemansky, P., S. H. Fatemi, B. Gorican, S. Meyale, R. Rossero, and A. M. Tartakoff. 1990. Dynamics and longevity of the glycolipid-anchored membrane protein, thy-1. J. Cell Biol. 110:1525-1531.
45. Lisanti, M. P., I. W. Caras, T. Gilbert, D. Hanzel, and E. Rodriguez-Boulan 1990. Vectorial apical delivery and slow endocytosis of a glycolipid-anchored fusion protein in transfected MDCK cells. Proc. Natl. Acad. Sci. USA. 87: 7419-7423.
46. Lisanti, M. P., P. E. Schrer, J. Vidugiriene, Z. Tang, A. Hermanowski-Vosatka, Y. Hu, R. F. Cook, and M Sargiacomo 1994a. Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease J. Cell Biol. 126:111-126.
47. Lisanti, M P., P. E. Scherer, Z. Tang, and M. Sargiacomo. 1994b. Caveolae, caveolin and caveolin-rich membrane domains: a signalling hypothesis. Trends Cell Biol 4:231-235.
48. Low, M. G. 1989. The glycosyl-phosphatidylinositol anchor of membrane proteins. Biochim. Biophys. Acta. 988:427-454.
49. Luhrs, C. A. 1991. The role of glycosylation in the biosynthesis and acquisition of ligand-binding activity of the folate-binding protein in cultured KB cells. Blood. 77:1171-1180.
50. Luhrs, C. A., and B. L. Slomiany, 1989. A human membrane-associated folate binding protein is anchored by a glycosyl-phosphatidylinositol tail. J. Biol Chem. 264:21446-21449.
51. Luhrs, C. A., E Sadasivan, M. da Costa, and S. P. Rothenberg. 1986. The isolation and properties of multiple forms of folate binding protein in cultured KB cells. Arch. Biochem. Biophys. 250:94-105.
52. Matherly, L. H., S. C. Wong, S. M. Angeles, J. W. Taub, and G. K. Smith. 1994. Distribution of the reduced folate carrier (RFC) versus the high affinity membrane folate binding protein (mFBP) in human tumors and tissues. Proc. Am. Assoc. Cancer Res. 35:307.
53. Mayor, S., K. G. Rothberg, and F. R. Maxfield. 1994. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science (Wash. DC). 264:1948-1951.
54. McAlinden, T. P., J. B. Hynes, S. A. Patil, G. R. Westerhof, G. Jansen, J H. Schornagel, S. S. Kerwar, and J. H Freisheim. 1991. Synthesis and biological evaluation of a fluorescent analogue of folic acid. Biochemistry 30:5674-5681.
55. McGuire, J. J., P. Hsieh, J. K. Coward, and J. R. Bertino. 1980. Enzymatic synthesis of folylpolyglutomates. J. Biol. Chem 225:5776-5788.
56. McHugh, M., and Y. C. Cheng. 1979. Demonstration of a high affinity folate binder in human cell membranes and its characterization in cultured human KB cells. J. Biol. Chem. 254:11312-11318.
57. 2+ transport system associated with the plasma membrane of Dictyostelium Discoideum is activated by different chemoattractant receptors J. Cell Biol. 112:103-110.
58. Nykjær, A., C. M. Petersen, B. Moller, P. H. Jensen, S. K. Moestrup, T. L. Holtet, M. Etzerodt, H. C. Thogersen, M. Munch, P. A. Andreasen, et al. 1992. Purified α2-macroglobulin receptor/LDL receptor-related protein binds urokinase plasminogen activator inhibitor type-1 complex. Evidence that the α2-macroglobulin receptor mediates the cellular degradation of urokinase receptor bound complexes. J. Biol. Chem. 267:14543-14546.
59. Palade, G. E., and R. R. Bruns. 1968. Structural modulation of plasmalemmal vesicles. J Cell Biol. 37:633-649.
60. Price, E. M., and J. H. Freisheim. 1987. Photoaffinity analogues of methotrexate as folate antagonist binding probes. 2. Transport studies, photoaffinity labeling, and identification of the membrane carrier protein for methotrexate from murine L1210 cells. Biochemistry 26:4757-4763.
61. Price, E. M., L. Sams, K M. Harpring, R. J Kempton, and J. H. Freisheim. 1986. Photoaffinity analogues of methotrexate as probes for dihydrofolate reductase structure and function Biochem. Pharmacol. 35:4341-4343.
62. Ratnam, M., and J. H. Freisheim. 1990. Proteins involved in the transport of folates and antifolates by normal and neoplastic cells. In Folic Acid Metabolism in Health and Disease. M. F. Picciano, E. L. R. Stokstad, and J. F. Gregory, editors. Wiley-Liss, Inc. New York. 91-120.
63. Ratnam, M., H. Marquardt, J. L. Duhring, and J. H. Freisheim. 1989. Homologous membrane folate binding proteins in human placenta: cloning and sequence of a cDNA. Biochemistry. 28:8249-8254.
64. Rijnboutt, S., W Stoorvogel, H. J. Geuze, and G. J. Strous 1992 Identification of subcompartments involved in biosynthetic processing of cathepsin D. J Biol Chem. 267:5665-15672.
65. Ross, J. F., P. K. Chaudhuri, and M. Ratnam. 1994. Differential regulation of folate receptor isoforms in normal and malignant tissues in vivo and in established cell lines: physiologic and clinical implications. Cancer. 73:2432-2443
66. Rothberg, K. G., Y. S. Ying, J. F. Kolhouse, B. A. Kamen, and R. G. W. Anderson. 1990a. The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J. Cell Biol. 110: 637-649.
67. Rothberg, K. G., Y.-S. Ying, B. A. Kamen, and R. G. W. Anderson. 1990b. Cholesterol controls the clustering of the glycophospholipid-anchored membrane receptor for 5-methyltetrahydrofolate, J Cell Biol 111:2931-2938.
68. Rothberg, K. G., J. E Heuser, W. C. Donzell, Y. S. Ying, J. R. Glenney, and R. G. W. Anderson. 1992. Caveolin, a protein component of cavcolae membrane coats Cell. 68:673-682.
69. Sadasivan, E , and S. P. Rothenberg. 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.
70. Sandvig, K , and B. Van Deurs 1994. Endocytosis without clathrin. Trends Cell Biol. 4:275-277.
71. Sargiacomo, M., M. Sudol, Z. Tang, and M. P. Lisanti. 1993. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol 122:789-809
72. Severs, N J. 1988. Caveolae: static inpocketings of the plasma membrane, dynamic vesicles or plain artifact. J Cell Sci. 90:341-348.
73. Shen, F., J F. Ross, X. Wang, and M. Ratnam. 1994 Identification of a novel folate receptor, a truncated receptor and receptor type β in hematopoietic cells: cDNA cloning, expression, immunoreactivity and tissue distribution. Biochemistry 33:1209-1215.
74. Shenoy, S. A., J. Kwong, T. Fujita, M. W. Olszowy, A. S Shaw, and D. M. Lublin. 1992. Signal transduction through decay accelerating factor: interaction of glycosyl-phosphatidyl anchor and protein tyrosine kinases p56lck and p59fyn 1. J. Immunol. 149:3535-3541.
75. Shyng, S L., J E. Heuser, and D. A. Harris. 1994. A glycolipid-anchored prion protein is endocytosed via clathrin-coated pits. J. Cell Biol. 125:1239-1250.
76. Simons, K., and G. Van Meer. 1988. Lipid sorting in epithelial cells. Biochemistry. 27:6197-6202.
77. Sirotnak, F. M 1985. Obligate genetic expression in tumor cells of a fetal membrane property mediating "folate" transport, biological significance and implications for improved therapy of human cancer Cancer Res 45:3992-4000.
78. Stefanová, I. V. Horesjí, I. J. Ansotegui, W. Knapp, and H. Stockinger. 1991. GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science (Wash DC). 254:1016-1019.
79. Thomas, P M., and L. E Samuelson. 1992. The glycosylphosphatidylinositol anchored Thy-1 molecule interacts with the p60fyn protein tyrosine kinase in T cells. J. Biol. Chem. 267:12317-12322.
80. Van Deurs, B , P. K. Holm, K Sandvig, and S. H. Hansen. 1993. Are caveolae involved in clathrin-independent endocytosis? Trends Cell Biol 3:249-251
81. Watts, C., and M. Marsh. 1992 Endocytosis - what goes in and how. J. Cell Sci. 103:1-8
82. Weitman, S. D., R. H. Lark, L. R. Coney, D. W. Fort, V. Frasca, V. R. Zurawski, and B. A Kamen. 1992. Distribution of the folate receptor GP38 in normal and malignant cell lines and tissues. Cancer Res 52:3396-3401.
83. Westerhof, G. R., G Jansen, N. van Emmerik, I. Kathmann, G. Rijksen, A. L. Jackman, and J. H. Schornagel 1991. Membrane transport of natural and antifolate compounds in murine L1210 leukemia cells: role of carrier- and receptor-mediaied transport systems. Cancer Res 51:5507-5513.
84. Westerhof, G. R., J. H. Schornagel, I. Kathmann, P. Noordhuis, G. J. Peters, and G. Jansen. 1994. Membrane transport of folate antagonists in KB, IGROV-1 and MA-104 cells: evidence for separate carrier-mediated and receptor-mediated influx routes. Proc Am. Assoc Cancer Res 35:302-305.
85. Westerhof, G R., J. H. Schornagel, S. Rijnboutt, H. M Pinedo, and G. Jansen 1993. Identification of a reduced folate/methotrexate carrier in human KB-cells expressing high levels of membrane associated folate binding protein. In Chemistry and Biology of Pteridines and Folates. J. E. Ayling, M G. Nair, and C. M. Baugh, editors. Plenum Press. New York 771-774.
86. Williams, F. M. R., and W. F. Flintoff, 1995 Isolation of a human cDNA that complements a mutant hamster cell defective in methotrexate uptake. J. Biol Chem. 270:2987-2992.
87. Williams, F M. R , R. C. Murray, T. M. Underhill, and W. F. Flintoff. 1994. Isolation of a hamster cDNA clone encoding for a function involved in methotrexate uptake J. Biol. Chem 269:5810-5816.
88. Ying, Y. S., R G. W. Anderson, and K. G. Rothberg. 1992 Each caveola contains multiple glycosyl-phosphatidylinositol-anchored membrane proteins. Cold Spring Harbor Symp. Quant. Biol. 57:593-604.