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. 1995 Aug 1;130(3):537–551. doi: 10.1083/jcb.130.3.537

Selective reentry of recycling cell surface glycoproteins to the biosynthetic pathway in human hepatocarcinoma HepG2 cells

PMCID: PMC2120536  PMID: 7622556

Abstract

Return of cell surface glycoproteins to compartments of the secretory pathway has been examined in HepG2 cells comparing return to the trans- Golgi network (TGN), the trans/medial- and cis-Golgi. Transport to these sites was studied by example of the transferrin receptor (TfR) and the serine peptidase dipeptidylpeptidase IV (DPPIV) after labeling these proteins with the N-hydroxysulfosuccinimide ester of biotin on the cell surface. This experimental design allowed to distinguish between glycoproteins that return to these biosynthetic compartments from the cell surface and newly synthesized glycoproteins that pass these compartments during biosynthesis en route to the surface. Reentry to the TGN was measured in that surface glycoproteins were desialylated with neuraminidase and were monitored for resialylation during recycling. Return to the trans-Golgi was traced measuring the transfer of [3H]fucose residues to recycling surface proteins by fucosyltransferases. To study return to the cis-Golgi, surface proteins were metabolically labeled in the presence of the mannosidase I inhibitor deoxymannojirimycin (dMM). As a result surface proteins retained N-glycans of the oligomannosidic type. Return to the site of mannosidase I in the medial/cis-Golgi was measured monitoring conversion of these glycans to those of the complex type after washout of dMM. Our data demonstrate that DPPIV does return from the cell surface not only to the TGN, but also to the trans-Golgi thus linking the endocytic to the secretory pathway. In contrast, no reentry to sites of mannosidase I could be detected indicating that the early secretory pathway is not or is only at insignificant rates accessible to recycling DPPIV. In contrast to DPPIV, TfR was very efficiently sorted from endosomes to the cell surface and did not return to the TGN or to other biosynthetic compartments in detectable amounts, indicating that individual surface proteins are subject to different sorting mechanisms or sorting efficiencies during recycling.

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Selected References

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  1. Bauer C. H., Lukaschek R., Reutter W. G. Studies on the golgi apparatus. Cumulative inhibition of protein and glycoprotein secretion by D-galactosamine. Biochem J. 1974 Aug;142(2):221–230. doi: 10.1042/bj1420221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bischoff J., Kornfeld R. The effect of 1-deoxymannojirimycin on rat liver alpha-mannosidases. Biochem Biophys Res Commun. 1984 Nov 30;125(1):324–331. doi: 10.1016/s0006-291x(84)80371-x. [DOI] [PubMed] [Google Scholar]
  3. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  4. Braun M., Waheed A., von Figura K. Lysosomal acid phosphatase is transported to lysosomes via the cell surface. EMBO J. 1989 Dec 1;8(12):3633–3640. doi: 10.1002/j.1460-2075.1989.tb08537.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bretscher M. S. Endocytosis and recycling of the fibronectin receptor in CHO cells. EMBO J. 1989 May;8(5):1341–1348. doi: 10.1002/j.1460-2075.1989.tb03514.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Broquet P., Baubichon-Cortay H., George P., Louisot P. Glycoprotein sialyltransferases in eucaryotic cells. Int J Biochem. 1991;23(4):385–389. doi: 10.1016/0020-711x(91)90164-i. [DOI] [PubMed] [Google Scholar]
  7. Brändli A. W., Simons K. A restricted set of apical proteins recycle through the trans-Golgi network in MDCK cells. EMBO J. 1989 Nov;8(11):3207–3213. doi: 10.1002/j.1460-2075.1989.tb08479.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bucci C., Parton R. G., Mather I. H., Stunnenberg H., Simons K., Hoflack B., Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell. 1992 Sep 4;70(5):715–728. doi: 10.1016/0092-8674(92)90306-w. [DOI] [PubMed] [Google Scholar]
  9. Busch G., Hoder D., Reutter W., Tauber R. Selective isolation of individual cell surface proteins from tissue culture cells by a cleavable biotin label. Eur J Cell Biol. 1989 Dec;50(2):257–262. [PubMed] [Google Scholar]
  10. Ciechanover A., Schwartz A. L., Dautry-Varsat A., Lodish H. F. Kinetics of internalization and recycling of transferrin and the transferrin receptor in a human hepatoma cell line. Effect of lysosomotropic agents. J Biol Chem. 1983 Aug 25;258(16):9681–9689. [PubMed] [Google Scholar]
  11. Collawn J. F., Lai A., Domingo D., Fitch M., Hatton S., Trowbridge I. S. YTRF is the conserved internalization signal of the transferrin receptor, and a second YTRF signal at position 31-34 enhances endocytosis. J Biol Chem. 1993 Oct 15;268(29):21686–21692. [PubMed] [Google Scholar]
  12. DE DUVE C., PRESSMAN B. C., GIANETTO R., WATTIAUX R., APPELMANS F. Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem J. 1955 Aug;60(4):604–617. doi: 10.1042/bj0600604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Daniel P. F., Winchester B., Warren C. D. Mammalian alpha-mannosidases--multiple forms but a common purpose? Glycobiology. 1994 Oct;4(5):551–566. doi: 10.1093/glycob/4.5.551. [DOI] [PubMed] [Google Scholar]
  14. Dautry-Varsat A., Ciechanover A., Lodish H. F. pH and the recycling of transferrin during receptor-mediated endocytosis. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2258–2262. doi: 10.1073/pnas.80.8.2258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Duncan J. R., Kornfeld S. Intracellular movement of two mannose 6-phosphate receptors: return to the Golgi apparatus. J Cell Biol. 1988 Mar;106(3):617–628. doi: 10.1083/jcb.106.3.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dunn K. W., McGraw T. E., Maxfield F. R. Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome. J Cell Biol. 1989 Dec;109(6 Pt 2):3303–3314. doi: 10.1083/jcb.109.6.3303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Elbein A. D., Legler G., Tlusty A., McDowell W., Schwarz R. The effect of deoxymannojirimycin on the processing of the influenza viral glycoproteins. Arch Biochem Biophys. 1984 Dec;235(2):579–588. doi: 10.1016/0003-9861(84)90232-7. [DOI] [PubMed] [Google Scholar]
  18. Fishman J. B., Fine R. E. A trans Golgi-derived exocytic coated vesicle can contain both newly synthesized cholinesterase and internalized transferrin. Cell. 1987 Jan 16;48(1):157–164. doi: 10.1016/0092-8674(87)90366-7. [DOI] [PubMed] [Google Scholar]
  19. Fraker P. J., Speck J. C., Jr Protein and cell membrane iodinations with a sparingly soluble chloroamide, 1,3,4,6-tetrachloro-3a,6a-diphrenylglycoluril. Biochem Biophys Res Commun. 1978 Feb 28;80(4):849–857. doi: 10.1016/0006-291x(78)91322-0. [DOI] [PubMed] [Google Scholar]
  20. Fuhrmann U., Bause E., Legler G., Ploegh H. Novel mannosidase inhibitor blocking conversion of high mannose to complex oligosaccharides. Nature. 1984 Feb 23;307(5953):755–758. doi: 10.1038/307755a0. [DOI] [PubMed] [Google Scholar]
  21. Goda Y., Pfeffer S. R. Selective recycling of the mannose 6-phosphate/IGF-II receptor to the trans Golgi network in vitro. Cell. 1988 Oct 21;55(2):309–320. doi: 10.1016/0092-8674(88)90054-2. [DOI] [PubMed] [Google Scholar]
  22. Green S. A., Kelly R. B. Endocytic membrane traffic to the Golgi apparatus in a regulated secretory cell line. J Biol Chem. 1990 Dec 5;265(34):21269–21278. [PubMed] [Google Scholar]
  23. Green S. A., Kelly R. B. Low density lipoprotein receptor and cation-independent mannose 6-phosphate receptor are transported from the cell surface to the Golgi apparatus at equal rates in PC12 cells. J Cell Biol. 1992 Apr;117(1):47–55. doi: 10.1083/jcb.117.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hauri H. P., Sterchi E. E., Bienz D., Fransen J. A., Marxer A. Expression and intracellular transport of microvillus membrane hydrolases in human intestinal epithelial cells. J Cell Biol. 1985 Sep;101(3):838–851. doi: 10.1083/jcb.101.3.838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hedman K., Goldenthal K. L., Rutherford A. V., Pastan I., Willingham M. C. Comparison of the intracellular pathways of transferrin recycling and vesicular stomatitis virus membrane glycoprotein exocytosis by ultrastructural double-label cytochemistry. J Histochem Cytochem. 1987 Feb;35(2):233–243. doi: 10.1177/35.2.3025294. [DOI] [PubMed] [Google Scholar]
  26. Heukeshoven J., Dernick R. Improved silver staining procedure for fast staining in PhastSystem Development Unit. I. Staining of sodium dodecyl sulfate gels. Electrophoresis. 1988 Jan;9(1):28–32. doi: 10.1002/elps.1150090106. [DOI] [PubMed] [Google Scholar]
  27. Hirschberg C. B., Snider M. D. Topography of glycosylation in the rough endoplasmic reticulum and Golgi apparatus. Annu Rev Biochem. 1987;56:63–87. doi: 10.1146/annurev.bi.56.070187.000431. [DOI] [PubMed] [Google Scholar]
  28. Hortsch M. Preparation and analysis of membranes and membrane proteins from Drosophila. Methods Cell Biol. 1994;44:289–301. doi: 10.1016/s0091-679x(08)60920-6. [DOI] [PubMed] [Google Scholar]
  29. Huang K. M., Snider M. D. Glycoprotein recycling to the galactosyltransferase compartment of the Golgi complex. J Biol Chem. 1993 May 5;268(13):9302–9310. [PubMed] [Google Scholar]
  30. Jin M., Sahagian G. G., Jr, Snider M. D. Transport of surface mannose 6-phosphate receptor to the Golgi complex in cultured human cells. J Biol Chem. 1989 May 5;264(13):7675–7680. [PubMed] [Google Scholar]
  31. Karin M., Mintz B. Receptor-mediated endocytosis of transferrin in developmentally totipotent mouse teratocarcinoma stem cells. J Biol Chem. 1981 Apr 10;256(7):3245–3252. [PubMed] [Google Scholar]
  32. Klausner R. D., Van Renswoude J., Ashwell G., Kempf C., Schechter A. N., Dean A., Bridges K. R. Receptor-mediated endocytosis of transferrin in K562 cells. J Biol Chem. 1983 Apr 25;258(8):4715–4724. [PubMed] [Google Scholar]
  33. Knowles B. B., Howe C. C., Aden D. P. Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen. Science. 1980 Jul 25;209(4455):497–499. doi: 10.1126/science.6248960. [DOI] [PubMed] [Google Scholar]
  34. Kornfeld S., Mellman I. The biogenesis of lysosomes. Annu Rev Cell Biol. 1989;5:483–525. doi: 10.1146/annurev.cb.05.110189.002411. [DOI] [PubMed] [Google Scholar]
  35. Kreisel W., Hanski C., Tran-Thi T. A., Katz N., Decker K., Reutter W., Gerok W. Remodeling of a rat hepatocyte plasma membrane glycoprotein. De- and reglycosylation of dipeptidyl peptidase IV. J Biol Chem. 1988 Aug 25;263(24):11736–11742. [PubMed] [Google Scholar]
  36. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  37. Lippincott-Schwartz J., Yuan L., Tipper C., Amherdt M., Orci L., Klausner R. D. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell. 1991 Nov 1;67(3):601–616. doi: 10.1016/0092-8674(91)90534-6. [DOI] [PubMed] [Google Scholar]
  38. Loch N., Tauber R., Becker A., Hartel-Schenk S., Reutter W. Biosynthesis and metabolism of dipeptidylpeptidase IV in primary cultured rat hepatocytes and Morris hepatoma 7777 cells. Eur J Biochem. 1992 Nov 15;210(1):161–168. doi: 10.1111/j.1432-1033.1992.tb17404.x. [DOI] [PubMed] [Google Scholar]
  39. Lohmander L. S. Analysis by high-performance liquid chromatography of radioactively labeled carbohydrate components of proteoglycans. Anal Biochem. 1986 Apr;154(1):75–84. doi: 10.1016/0003-2697(86)90498-7. [DOI] [PubMed] [Google Scholar]
  40. Lombardi D., Soldati T., Riederer M. A., Goda Y., Zerial M., Pfeffer S. R. Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J. 1993 Feb;12(2):677–682. doi: 10.1002/j.1460-2075.1993.tb05701.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Markelonis G. J., Oh T. H., Park L. P., Cha C. Y., Sofia C. A., Kim J. W., Azari P. Synthesis of the transferrin receptor by cultures of embryonic chicken spinal neurons. J Cell Biol. 1985 Jan;100(1):8–17. doi: 10.1083/jcb.100.1.8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Matter K., Stieger B., Klumperman J., Ginsel L., Hauri H. P. Endocytosis, recycling, and lysosomal delivery of brush border hydrolases in cultured human intestinal epithelial cells (Caco-2). J Biol Chem. 1990 Feb 25;265(6):3503–3512. [PubMed] [Google Scholar]
  43. Michell R. H., Hawthorne J. N. The site of diphosphoinositide synthesis in rat liver. Biochem Biophys Res Commun. 1965 Nov 22;21(4):333–338. doi: 10.1016/0006-291x(65)90198-1. [DOI] [PubMed] [Google Scholar]
  44. Milla M. E., Clairmont C. A., Hirschberg C. B. Reconstitution into proteoliposomes and partial purification of the Golgi apparatus membrane UDP-galactose, UDP-xylose, and UDP-glucuronic acid transport activities. J Biol Chem. 1992 Jan 5;267(1):103–107. [PubMed] [Google Scholar]
  45. Neefjes J. J., Hengeveld T., Tol O., Ploegh H. L. Intracellular interactions of transferrin and its receptor during biosynthesis. J Cell Biol. 1990 Oct;111(4):1383–1392. doi: 10.1083/jcb.111.4.1383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Neefjes J. J., Verkerk J. M., Broxterman H. J., van der Marel G. A., van Boom J. H., Ploegh H. L. Recycling glycoproteins do not return to the cis-Golgi. J Cell Biol. 1988 Jul;107(1):79–87. doi: 10.1083/jcb.107.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Omary M. B., Trowbridge I. S. Biosynthesis of the human transferrin receptor in cultured cells. J Biol Chem. 1981 Dec 25;256(24):12888–12892. [PubMed] [Google Scholar]
  48. Orberger G., Geyer R., Stirm S., Tauber R. Structure of the N-linked oligosaccharides of the human transferrin receptor. Eur J Biochem. 1992 Apr 1;205(1):257–267. doi: 10.1111/j.1432-1033.1992.tb16776.x. [DOI] [PubMed] [Google Scholar]
  49. PENNINGTON R. J. Biochemistry of dystrophic muscle. Mitochondrial succinate-tetrazolium reductase and adenosine triphosphatase. Biochem J. 1961 Sep;80:649–654. doi: 10.1042/bj0800649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Paulson J. C., Colley K. J. Glycosyltransferases. Structure, localization, and control of cell type-specific glycosylation. J Biol Chem. 1989 Oct 25;264(30):17615–17618. [PubMed] [Google Scholar]
  51. Pfeiffer G., Geyer H., Geyer R., Kalsner I., Wendorf P. Separation of glycoprotein-N-glycans by high-pH anion-exchange chromatography. Biomed Chromatogr. 1990 Sep;4(5):193–199. doi: 10.1002/bmc.1130040505. [DOI] [PubMed] [Google Scholar]
  52. Prydz K., Brändli A. W., Bomsel M., Simons K. Surface distribution of the mannose 6-phosphate receptors in epithelial Madin-Darby canine kidney cells. J Biol Chem. 1990 Jul 25;265(21):12629–12635. [PubMed] [Google Scholar]
  53. Regoeczi E., Chindemi P. A., Debanne M. T., Charlwood P. A. Partial resialylation of human asialotransferrin type 3 in the rat. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2226–2230. doi: 10.1073/pnas.79.7.2226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Regoeczi E., Chindemi P. A., Debanne M. T. Partial resialylation of human asialotransferrin types 1 and 2 in the rat. Can J Biochem Cell Biol. 1984 Sep;62(9):853–858. doi: 10.1139/o84-109. [DOI] [PubMed] [Google Scholar]
  55. Regoeczi E., Koj A. Diacytosis of human asialotransferrin type 3 in the rat liver is due to the sequential engagement of two receptors. Exp Cell Res. 1985 Sep;160(1):1–8. doi: 10.1016/0014-4827(85)90230-7. [DOI] [PubMed] [Google Scholar]
  56. Reichner J. S., Whiteheart S. W., Hart G. W. Intracellular trafficking of cell surface sialoglycoconjugates. J Biol Chem. 1988 Nov 5;263(31):16316–16326. [PubMed] [Google Scholar]
  57. Roth J. Subcellular organization of glycosylation in mammalian cells. Biochim Biophys Acta. 1987 Oct 5;906(3):405–436. doi: 10.1016/0304-4157(87)90018-9. [DOI] [PubMed] [Google Scholar]
  58. Rothenberger S., Iacopetta B. J., Kühn L. C. Endocytosis of the transferrin receptor requires the cytoplasmic domain but not its phosphorylation site. Cell. 1987 May 8;49(3):423–431. doi: 10.1016/0092-8674(87)90295-9. [DOI] [PubMed] [Google Scholar]
  59. Rothman J. E., Orci L. Molecular dissection of the secretory pathway. Nature. 1992 Jan 30;355(6359):409–415. doi: 10.1038/355409a0. [DOI] [PubMed] [Google Scholar]
  60. Schneider C., Sutherland R., Newman R., Greaves M. Structural features of the cell surface receptor for transferrin that is recognized by the monoclonal antibody OKT9. J Biol Chem. 1982 Jul 25;257(14):8516–8522. [PubMed] [Google Scholar]
  61. Snider M. D., Rogers O. C. Intracellular movement of cell surface receptors after endocytosis: resialylation of asialo-transferrin receptor in human erythroleukemia cells. J Cell Biol. 1985 Mar;100(3):826–834. doi: 10.1083/jcb.100.3.826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Snider M. D., Rogers O. C. Membrane traffic in animal cells: cellular glycoproteins return to the site of Golgi mannosidase I. J Cell Biol. 1986 Jul;103(1):265–275. doi: 10.1083/jcb.103.1.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Stoorvogel W., Geuze H. J., Griffith J. M., Schwartz A. L., Strous G. J. Relations between the intracellular pathways of the receptors for transferrin, asialoglycoprotein, and mannose 6-phosphate in human hepatoma cells. J Cell Biol. 1989 Jun;108(6):2137–2148. doi: 10.1083/jcb.108.6.2137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Stoorvogel W., Geuze H. J., Griffith J. M., Strous G. J. The pathways of endocytosed transferrin and secretory protein are connected in the trans-Golgi reticulum. J Cell Biol. 1988 Jun;106(6):1821–1829. doi: 10.1083/jcb.106.6.1821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Sutherland R., Delia D., Schneider C., Newman R., Kemshead J., Greaves M. Ubiquitous cell-surface glycoprotein on tumor cells is proliferation-associated receptor for transferrin. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4515–4519. doi: 10.1073/pnas.78.7.4515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Tarentino A. L., Gómez C. M., Plummer T. H., Jr Deglycosylation of asparagine-linked glycans by peptide:N-glycosidase F. Biochemistry. 1985 Aug 13;24(17):4665–4671. doi: 10.1021/bi00338a028. [DOI] [PubMed] [Google Scholar]
  67. Tauber R., Park C. S., Becker A., Geyer R., Reutter W. Rapid intramolecular turnover of N-linked glycans in plasma membrane glycoproteins. Extension of intramolecular turnover to the core sugars in plasma membrane glycoproteins of hepatoma. Eur J Biochem. 1989 Dec 8;186(1-2):55–62. doi: 10.1111/j.1432-1033.1989.tb15177.x. [DOI] [PubMed] [Google Scholar]
  68. Tauber R., Park C. S., Reutter W. Intramolecular heterogeneity of degradation in plasma membrane glycoproteins: evidence for a general characteristic. Proc Natl Acad Sci U S A. 1983 Jul;80(13):4026–4029. doi: 10.1073/pnas.80.13.4026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Tauber R., Schenck I., Josić D., Gross V., Heinrich P. C., Gerok W., Reutter W. Different oligosaccharide processing of the membrane-integrated and the secretory form of gp 80 in rat liver. EMBO J. 1986 Sep;5(9):2109–2114. doi: 10.1002/j.1460-2075.1986.tb04473.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Trimble R. B., Maley F. Optimizing hydrolysis of N-linked high-mannose oligosaccharides by endo-beta-N-acetylglucosaminidase H. Anal Biochem. 1984 Sep;141(2):515–522. doi: 10.1016/0003-2697(84)90080-0. [DOI] [PubMed] [Google Scholar]
  71. Velasco A., Hendricks L., Moremen K. W., Tulsiani D. R., Touster O., Farquhar M. G. Cell type-dependent variations in the subcellular distribution of alpha-mannosidase I and II. J Cell Biol. 1993 Jul;122(1):39–51. doi: 10.1083/jcb.122.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Wood S. A., Park J. E., Brown W. J. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell. 1991 Nov 1;67(3):591–600. doi: 10.1016/0092-8674(91)90533-5. [DOI] [PubMed] [Google Scholar]
  73. Woods J. W., Doriaux M., Farquhar M. G. Transferrin receptors recycle to cis and middle as well as trans Golgi cisternae in Ig-secreting myeloma cells. J Cell Biol. 1986 Jul;103(1):277–286. doi: 10.1083/jcb.103.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Yamamoto K., Tsuji T., Irimura T., Osawa T. The structure of carbohydrate unit B of porcine thyroglobulin. Biochem J. 1981 Jun 1;195(3):701–713. doi: 10.1042/bj1950701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. van Deurs B., Sandvig K., Petersen O. W., Olsnes S., Simons K., Griffiths G. Estimation of the amount of internalized ricin that reaches the trans-Golgi network. J Cell Biol. 1988 Feb;106(2):253–267. doi: 10.1083/jcb.106.2.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. van den Bosch R. A., du Maine A. P., Geuze H. J., van der Ende A., Strous G. J. Recycling of 5'-nucleotidase in a rat hepatoma cell line. EMBO J. 1988 Nov;7(11):3345–3351. doi: 10.1002/j.1460-2075.1988.tb03206.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. van der Sluijs P., Hull M., Webster P., Mâle P., Goud B., Mellman I. The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell. 1992 Sep 4;70(5):729–740. doi: 10.1016/0092-8674(92)90307-x. [DOI] [PubMed] [Google Scholar]

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