Apical plasma membrane proteins and endolyn-78 travel through a subapical compartment in polarized WIF-B hepatocytes

Journal of Cell Biology

Volumn 141, Issue 1, 1998, Pages 115-133

  Ihrke, Gudrun ^a,c   Martin, Greg V ^a   Shanks, Michael R ^a   Schrader, Michael ^b   Schroer, Trina A ^b   Hubbard, Ann L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPEPTIDASE; ENDOLYN 78; IMMUNOGLOBULIN A; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE TRANSPORT; ENDOCYTOSIS; IMMUNOFLUORESCENCE TEST; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TARGETING;

5'-NUCLEOTIDASE; ANIMALS; ANTIBODIES; ANTIGENS, CD13; CELL MEMBRANE; CELL POLARITY; ENDOCYTOSIS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HYBRID CELLS; KINETICS; LIVER; LIVER NEOPLASMS, EXPERIMENTAL; LYSOSOMES; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; RATS; RECEPTORS, FC;

EID: 0032489801     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.1.115     Document Type: Article

References (96)

1. Anderson, R.G.W., M.S. Brown, U. Beisiegel, and J.L. Goldstein, 1982. Surface distribution and recycling of the low density lipoprotein receptor as visualized with antireceptor antibodies. J. Cell Biol. 93:523-531.
2. Apodaca, G., L.A. Katz, and K.E. Mostov. 1994. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125: 67-86.
3. Bacallao, R., C. Antony, C. Dotti, E. Karsenti, E.H. Stelzer, and K. Simons. 1989. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J. Cell Biol. 109:2817-2832.
4. Bailyes, E.M., M. Soos, P. Jackson, A.C. Newby, K. Siddle, and J.P. Luzio. 1984. The existence and properties of two dimers of rat liver ecto-5′-nucleotidase. Biochem. J. 221:369-377.
5. Barr, V.A., and A.L. Hubbard. 1993. Newly synthesized hepatocyte plasma membrane proteins are transported in transcytotic vesicles in the bile duct-ligated rat. Gastroenterology. 105:554-571.
6. Barr, V.A., L.J. Scott, and A.L. Hubbard. 1995. Immunoadsorption of hepatic vesicles carrying newly synthesized dipeptidyl peptidase IV and polymeric IgA receptor. J. Biol. Chem. 270:27834-27844.
7. Barroso, M., and E.S. Sztul. 1994. Basolateral to apical transcytosis in polarized cells is indirect and involves BFA and trimeric G protein-sensitive passage through the apical endosome. J. Cell Biol. 124:83-100.
8. Bartles, J.R., L.T. Braiterman, and A.L. Hubbard. 1985a. Endogenous and exogenous domain markers of the rat hepatocyte plasma membrane. J. Cell Biol. 100:1126-1138.
9. Bartles, J.R., L.T. Braiterman, and A.L. Hubbard. 1985b. Biochemical characterization of domain-specific glycoproteins of the rat hepatocyte plasma membrane. J. Biol. Chem. 260:12792-12802.
10. Bartles, J.R., H.M. Feracci, B. Stieger, and A.L. Hubbard. 1987. Biogenesis of the rat hepatocyte plasma membrane in vivo: comparison of the pathways taken by apical and basolateral proteins using subcellular fractionation. J. Cell Biol. 105:1241-1251.
11. Bomsel, M., K. Prydz, R.G. Parton, J. Gruenberg, and K. Simons. 1989. Endocytosis in filter-grown Madin-Darby canine kidney cells. J. Cell Biol. 109: 3243-3258.
12. Brändli, A.W., R.G. Parton, and K. Simons. 1990. Transcytosis in MDCK cells: identification of glycoproteins transported bidirectionally between both plasma membrane domains. J. Cell Biol. 111:2909-2921.
13. Burry, R.W. 1995. Pre-embedding Immunocytochemistry with Silver Enhanced Small Gold Particles. In Immunogold-Silver Staining: Principles, Methods, and Applications. M.A. Hayat, editor. CRC Press, Boca Raton, FL. 217-230.
14. Calhoun, B.C., and J.R. Goldenring. 1997. Two Rab proteins, vesicle-associated membrane protein 2 (VAMP-2) and secretory carrier membrane proteins (SCAMPs), are present on immunoisolated parietal cell tubulovesicles. Biochem. J. 325:559-564.
15. Cassio, D., C. Hamon-Benais, M. Guerin, and O. Lecoq. 1991. Hybrid cell lines constitute a potential reservoir of polarized cells: isolation and study of highly differentiated hepatoma-derived hybrid cells able to form functional bile canaliculi in vitro. J. Cell Biol. 115:1397-1408.
16. Coon, H.G., and M.C. Weiss. 1969. A quantitative comparison of formation of spontaneous and virus-produced viable hybrids. Proc. Natl. Acad. Sci. USA. 62:852-859.
17. Courtoy, P.J. 1993. Analytical subcellular fractionation of endosomal compartments in rat hepatocytes. Subcell. Biochem. 19:29-68.
18. Crawford, J.M. 1996. Role of vesicle-mediated transport pathways in hepatocellular bile secretion. Sem. Liver Disease. 16:169-189.
19. Crawford, J.M., G.M. Mockel, A.R. Crawford, S.J. Hagen, V.C. Hatch, S. Barnes, J.J. Godleski, and M.C. Carey. 1995. Imaging biliary lipid secretion in the rat-ultrastructural evidence for vesiculation of the hepatocyte canalicular membrane. J. Lipid Res. 36:2147-2163.
20. Croze, E., I.E. Ivanov, G. Kreibich, M. Adesnik, D.D. Sabatini, and M.G. Rosenfeld. 1989. Endolyn-78, a membrane glycoprotein present in morphologically diverse components of the endosomal and lysosomal compartments: implications for lysosome biogenesis. J. Cell Biol. 108:1597-1613.
21. Delgrossi, M.H., L. Breuza, C. Mirre, P. Chavrier, and A. LeBivic. 1997. Human syntaxin 3 is localized apically in human intestinal cells. J. Cell Sci. 110: 2207-2214.
22. Drubin, D.G., and W.J. Nelson. 1996. Origins of cell polarity. Cell. 84:335-344.
23. Dunn, W.J. 1990. Studies on the mechanisms of autophagy: maturation of the autophagic vacuole. J. Cell Biol. 110:1935-1945.
24. Fath, K.R., G.M. Trimbur, and D.R. Burgess. 1994. Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells. J. Cell Biol. 126:661-675.
25. Fujita, H., P.L. Tuma, C.M. Finnegan, L.L. Locco, and A.L. Hubbard. 1998. Endogenous syntaxins 2, 3 and 4 exhibit distinct but overlapping patterns of expression at the hepatocyte plasma membrane. Biochem. J. 329:527-538.
26. Furuno, K., T. Ishikawa, K. Akasaki, S. Yano, Y. Tanaka, Y. Yamaguchi, H. Tsuji, M. Himeno, and K. Kato. 1989. Morphological localization of a major lysosomal membrane glycoprotein in the endocytic membrane system. J. Biochem. (Tokyo). 106:708-716.
27. Gaisano, H.Y., M. Ghai, P.N. Malkus, L. Sheu, A. Bouquillon, M.K. Bennet. and W.S. Trimble. 1996. Distinct cellular locations of the syntaxin family of proteins in rat pancreatic acinar cells. Mol. Biol. Cell. 7:2019-2027.
28. Geuze, H.J., J.W. Slot, G.J. Strous, J. Peppard, K. von Figura, A. Hasilik, and A.L. Schwartz. 1984. Intracellular receptor sorting during endocytosis: comparative immunoelectron microscopy of multiple receptors in rat liver. Cell. 37:195-204.
29. Goldenring, J.R., J. Smith, H.D. Vaughan, P. Cameron, W. Hawkins, and J. Navarre. 1996. Rab11 is an apically located small GTP-binding protein in epithelial tissues. Am. J. Physiol. 33:0515-525.
30. 131I-labeled human growth hormone of high specific radioactivity. Biochem. J. (Tokyo). 89:114-123.
31. Grimaldi, K.A., J.C. Hutton, and K. Siddle. 1987. Production and characterization of monoclonal antibodies to insulin secretory granule membranes. Biochem. J. (Tokyo). 245:557-566.
32. Gruenberg, J., and F.R. Maxfield. 1995. Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7:552-563.
33. +(+)-ATPase in polarized epithelial cells. Science. 254:847-850.
34. Hayakawa, T., O.C. Ng, A. Ma, and J.L. Boyer. 1990. Taurocholate stimulates transcytotic vesicular pathways labeled by horseradish peroxidase in the isolated perfused rat liver (published erratum appears in Gastroenrerology 99: 905). Gastroenterology. 99:216-228.
35. Hemery, I., A.-M. Durand-Schneider, G. Feldmann, J.-P. Vaerman, and M. Maurice. 1996. The transcytotic pathway of an apical plasma membrane protein (B10) in hepatocytes is similar to that of IgA and occurs via a tubular pericentriolar compartment. J. Cell Sci. 109:1215-1227.
36. Hopkins, C.R., A. Gibson, M. Shipman, and K. Miller. 1990. Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum. Nature. 346:335-339.
37. Hoppe, C.A., T.P. Connolly, and A.L. Hubbard. 1985. Transcellular transport of polymeric IgA in the rat hepatocyte: biochemical and morphological characterization of the transport pathway. J. Cell Biol. 101:2113-2123.
38. Hubbard, A.L., and Z.A. Cohn. 1972. The enzymatic iodination of the red cell membrane. J. Cell Biol. 55:390-405.
39. Hubbard, A.L., J.R. Bartles, and L.T. Braiterman. 1985. Identification of rat hepatocyte plasma membrane proteins using monoclonal antibodies. J. Cell Biol. 100:1115-1125.
40. Hughson, E.J., and C.R. Hopkins. 1990. Endocytic pathways in polarized Caco-2 cells: identification of an endosomal compartment accessible from both apical and basolateral surfaces. J. Cell Biol. 110:337-348.
41. Hunziker, W., and H.W. Geuze. 1996. Intracellular trafficking of lysosmal membrane proteins. Bioessays. 18:379-389.
42. Ihrke, G., and A.L. Hubbard. 1995. Control of Vesicle Traffic in Hepatocytes. In Progress in Liver Diseases. J.L. Boyer and R.K. Ockner, editors. W.B. Saunders, Philadelphia, PA. 63-99.
43. Ihrke, G., E.B. Neufeld, T. Meads, M.R. Shanks, D. Cassio, M. Laurent, T.A. Schroer, R.E. Pagano, and A.L. Hubbard. 1993. WIF-B cells: an in vitro model for studies of hepatocyte polarity. J. Cell Biol. 123:1761-1775.
44. Kiess, W., J.F. Haskell, L. Lee, L.A. Greenstein, B.E. Miller, A.L. Aarons, M.M. Rechler, and S.P. Nissley. 1987. An antibody that blocks insulin-like growth factor (IGF) binding to the type II IGF receptor is neither an agonist nor an inhibitor of IGF-stimulated biologic responses in L6 myoblasts. J. Biol. Chem. 262:12745-12751.
45. Knight, A., E. Hughson, C.R. Hopkins, and D.F. Cutler. 1995. Membrane protein trafficking through the common apical endosome compartment of polarized Caco-2 cells. Mol. Biol. Cell. 6:597-610.
46. Ladinsky, M.S., and K.E. Howell. 1992. The trans-Golgi network can be dissected structurally and functionally from the cisternae of the Golgi complex by brefeldin A. Eur. J. Cell Biol. 59:92-105.
47. Leunissen, J.L.M., and J.R. De Mey. 1989. Preparation of Gold Probes. In Immuno-gold Labeling in Cell Biology. A.J. Verkleij and J.L.M. Leunissen, editors. CRC Press, Boca Raton, FL. 3-16.
48. Lewis, V., S.A. Green, M. Marsh, P. Vihko, A. Helenius, and I. Mellman. 1985. Glycoproteins of the lysosomal membrane. J. Cell Biol. 100:1839-1847.
49. Lippincott-Schwartz, J., and D.M. Fambrough. 1986. Lysosomal membrane dynamics: structure and interorganellar movement of a major lysosomal membrane glycoprotein. J. Cell Biol. 102:1593-1605.
50. Lisanti, M.P., and E. Rodriguez-Boulan. 1990. Glycophospholipid membrane anchoring provides clues to the mechanism of protein sorting in polarized epithelial cells. Trends Biochem. Sci. 15:113-118.
51. Low, S.-H., T. Chapin, L.G. Weimbs, M.K. Kömüves, M.K. Bennett, and K.E. Mostov. 1996. Differential localization of syntaxin isoforms in polarized Madin-Darby canine kidney cells. Mol. Biol. Cell. 7:2007-2018.
52. Marsh, E.W., P.L. Leopold, N.L. Jones, and F.R. Maxfield. 1995. Oligomerized transferrin receptors are selectively retained by a lumenal sorting signal in a long-lived endocytic recycling compartment. J. Cell Biol. 129:1509-1522.
53. Matter, K., and I. Mellman. 1994. Mechanisms of cell polarity: sorting and transport in epithelial cells. Curr. Opin. Cell Biol. 6:545-554.
54. Maurice, M., M.J. Schell, B. Lardeux, and A.L. Hubbard. 1994. Biosynthesis and intracellular transport of a bile canalicular plasma membrane protein: studies in vivo and in the perfused rat liver. Hepatology. 19:648-655.
55. Mays, R.W., K.A. Siemers, B.A. Fritz, A.W. Lowe, G. van Meer, and W.J. Nelson. 1995. Hierarchy of mechanisms involved in generating Na/K-ATPase polarity in MDCK epithelial cells. J. Cell Biol. 130:1105-1115.
56. Meads, T., and T.A. Schroer. 1995. Polarity and nucleation of microtubules in polarized epithelial cells. Cell Motil. Cytoskeleton. 32:273-288.
57. Mellman, I., and H. Plutner. 1984. Internalization and degradation of macrophage Fc receptors bound to polyvalent immune complexes. J. Cell Biol. 98: 1170-1177.
58. Mevel-Ninio, M., and M.C. Weiss. 1981. Immunofluorescence analysis of the time-course of extinction, reexpression, and activation of albumin production in rat hepatoma-mouse fibroblast heterokaryons and hybrids. J. Cell Biol. 90:339-350.
59. Milgram, S.L., E.Y. Chang, and R.E. Mains. 1996. Processing and routing of a membrane-anchored form of proneuropeptide Y. Mol. Endocrin. 10:837-846.
60. Mostov, K.E., and M.H. Cardone. 1995. Regulation of protein traffic in polarized epithelial cells. Bioessays. 17:129-138.
61. Musil, L.S., and J.U. Baenziger. 1988. Proteolytic processing of rat liver membrane secretory component. Cleavage activity is localized to bile canalicular membranes. J. Biol. Chem. 263:15799-15808.
62. Novick, P., and M. Zerial. 1997. The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol. 9:496-504.
63. Odorizzi, G., A. Pearse, D. Domingo, I.S. Trowbridge, and C.R. Hopkins. 1996. Apical and basolateral endosomes of MDCK cells are interconnected and contain a polarized sorting mechanism. J. Cell Biol. 135:139-152.
64. Parton, R.G., K. Prydz, M. Bomsel, K. Simons, and G. Griffiths. 1989. Meeting of the apical and basolateral endocytic pathways of the Madin-Darby canine kidney cell in late endosomes. J. Cell Biol. 109:3259-3272.
65. Porter, R.R. 1959. The hydrolysis of rabbit gamma-globulin and antibodies with crystalline papain. Biochem. J. (Tokyo). 73:119-225.
66. Quintart, J., P. Baudhuin, and P.J. Courtoy. 1989. Marker enzymes in rat liver vesicles involved in transcellular transport. Eur J. Biochem. 184:567-574.
67. Reaves, J.R., N.A. Bright, B.M. Mullock, and J.P. Luzio. 1996. The effect of wortmannin on the localisation of lysosomal type I integral membrane glycoproteins suggests a role for phosphoinositide 3-kinase activity in regulating membrane traffic late in the endocytic pathway. J. Cell Sci. 109:749-762.
68. Rizzolo, L.J., and H.C. Joshi. 1993. Apical orientation of the microtubule organizing center and associated g-tubulin during polarization of the retinal pigment epithelium in vivo. Dev. Biol. 157:147-156.
69. Rodriguez-Boulan, E., and S.K. Powell. 1992. Polarity of epithelial and neuronal cells. Annu. Rev. Cell Biol. 8:395-427.
70. Rodriguez-Boulan, E., and C. Zurzolo. 1993. Polarity signals in epithelial cells. J. Cell Sci. 17(Suppl.):9-12.
71. Roth, J., D. Taatjes, J. Lucocq, J. Weinstein, and J. Paulson. 1985. Demonstration of an extensive trans-tubular network continuous with the Golgi-apparatus stack that may function in glycosylation. Cell. 43:287-295.
72. Sandoval, I.V., and O. Bakke. 1994. Targeting of membrane proteins to endosomes and lysosomes. Trends Cell Biol. 4:292-297.
73. Schaerer, E., M.R. Neutra, and J.P. Kraehenbuhl. 1991. Molecular and cellular mechanisms involved in transepithelial transport. J. Membr. Biol. 123:93-103.
74. Schell, M.J., M. Maurice, B. Stieger, and A.L. Hubbard. 1992. 5′ nucleotidase is sorted to the apical domain of hepatocytes via an indirect route (published erratum appears in J. Cell Biol. 123:767). J. Cell Biol. 119:1173-1182.
75. Scott, L.J., and A.L. Hubbard. 1992. Dynamics of four rat liver plasma membrane proteins and polymeric IgA receptor. Rates of synthesis and selective loss into the bile (published erratum appears in J. Biol. Chem. 268:19160). J. Biol. Chem. 267:6099-6106.
76. Shanks, M.R., D. Cassio, O. Lecoq, and A.L. Hubbard. 1994. An improved polarized rat hepatoma hybrid cell line. Generation and comparison with its hepatoma relatives and hepatocytes in vivo. J. Cell Sci. 107:813-825.
77. Simons, K., and S.D. Fuller. 1985. Cell surface polarity in epithelia. Annu. Rev. Cell Biol. 1:243-288.
78. Simons, K., P. Dupree, K. Fiedler, L.A. Huber, T. Kobayashi, T. Kurzchalia, V. Olkkonen, S. Pimplikar, R. Parton, and C. Dotti. 1992. Biogenesis of Cell-Surface Polarity in Epithelial Cells and Neurons. In Cold Spring Harb. Symp. Quant. Biol. 57:611-618.
79. Slot, J.W., and H.J. Geuze. 1984. Gold Markers for Single and Double Immunolabeling of Ultrathin Cryosections. In Immunolabeling for Electronmicroscopy. J.M. Polak and I.M. Varndell, editors. Elsevier Science, New York. 129-142.
80. Slot, J.W., and H.J. Geuze. 1985. A new method for preparing gold probes for multiple labeling cytochemistry. Eur. J. Cell Biol. 38:87-93.
81. Tokuyasu, K.T. 1989. Use of poly(vinylpyrrolidone) and poly(vinyl alcohol) for cryoultramicrotomy. Histochem. J. 21:163-171.
82. van Deurs, B., S.H. Hansen, O.W. Petersen, E.L. Melby, and K. Sandvig. 1990. Endocytosis, intracellular transport and transcytosis of the toxic protein ricin by a polarized epithelium. Eur. J. Cell Biol. 51:96-109.
83. van Genderen, I., and G. van Meer. 1995. Differential targeting of glucosylceramide and galactosylceramide analogues after synthesis but not during transcytosis in Madin-Darby canine kidney cells. J. Cell Biol. 131:645-654.
84. van Ijzendoorn, S.C.D., M.M.P. Zegers, J.W. Kok, and D. Hoekstra. 1997. Segregation of glucosylceramide and sphingomyelin occurs in the apical to basoateral transcytotic route in HepG2 cells. J. Cell Biol. 137:347-357.
85. Verkatachalan, M.A., and H.D. Fahimi. 1969. The use of beef liver catalase as a protein tracer for electron microscopy. J. Cell Biol. 42:480-489.
86. Vogel, L.K., O. Noren, and H. Sjostrom. 1995. Transcytosis of aminopeptidase-N in Caco-2 cells is mediated by a non-cytoplasmic signal. J. Biol. Chem. 270: 22933-22938.
87. Vogel, L.K., M. Spiess, H. Sjostrom, and O. Noren. 1992. Evidence for an apical sorting signal on the ectodomain of human aminopeptidase N. J. Biol. Chem. 267: 7794-2797.
88. von Figura, K., V. Gieselmann, and A. Hasilik. 1984. Antibody to mannose 6-phosphate receptor induces receptor deficiency in human fibroblasts. EMBO (Eur. Mol. Biol. Organ.) J. 3:1281-1286.
89. Wall, D.A., G. Wilson, and A.L. Hubbard. 1980. The galactose-specific recognition system of mammalian liver: the route of ligand internalization in rat hepatocytes. Cell. 21:79-93.
90. Weimbs, T., S.H. Low, S.J. Chapin, and K.E. Mostov. 1997. Apical targeting in polarized epithelial cells: there's more afloat than rafts. Trends Cell Biol. 7:393-399.
91. Weissman, A.M., R.D. Klausner, R. Krishnamurty, and J.B. Harford. 1986. Exposure of K562 cells to anti-receptor monoclonal antibody OKT9 results in rapid redistribution and enhanced degradation of the transferrin receptor. J. Cell Biol. 102:951-958.
92. Weisz, O.A., C.E. Machamer, and A.L. Hubbard. 1992. Rat liver dipeptidylpeptidase IV contains competing apical and basolateral targeting information. J. Biol. Chem. 267:22282-22288.
93. Wollner, D.A., and W.J. Nelson. 1992. Establishing and maintaining epithehal cell polarity. Roles of protein sorting, delivery and retention. J. Cell Sci. 102: 185-190.
94. Yamashiro, D.J., B. Tycko, S.R. Fluss, and F.R. Maxfield. 1984. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell. 37:789-800.
95. Zaal, K.J., J.W. Kok, R. Sormunen, S. Eskelinen, and D. Hoekstra. 1994. Intracellular sites involved in the biogenesis of bile canaliculi in hepatic cells. Eur. J. Cell Biol. 63:10-19.
96. Zhu, D., and B.U. Pauli. 1991. Generation of monoclonal antibodies directed against organ-specific endothelial cell surface determinants. J. Histochem. Cytochem. 39:1137-1142.