Actin filaments and microtubules are involved in different membrane traffic pathways that transport sphingolipids to the apical surface of polarized HepG2 cells

Molecular Biology of the Cell

Volumn 9, Issue 7, 1998, Pages 1939-1949

  Zegers, Mirjam M P ^a,b   Zaal, Kristien J M ^a,c   Van IJzendoorn, Sven C D ^a   Klappe, Karin ^a   Hoekstra, Dick ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NOCODAZOLE; SPHINGOLIPID;

ACTIN FILAMENT; APICAL MEMBRANE; ARTICLE; CYTOSKELETON; HEPATOMA CELL; MEMBRANE TRANSPORT; MICROTUBULE; PRIORITY JOURNAL; TRANSCYTOSIS;

ARMORACIA RUSTICANA;

EID: 0031869224     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.7.1939     Document Type: Article

References (40)

1. Babia, T., Kok, J.W., and Hoekstra, D. (1994) The use of fluorescent lipid analogues to study endocytosis of glycosphingolipids. In: Receptor Research Methods, ed. B. Greenstein, London: Harwood Academic, 155-174.
2. Bligh, E.G., and Dyer, W.J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917.
3. Boyer, J.L., and Soroka, C.J. (1995). Vesicle targeting to the apical domain regulates bile excretory function in isolated rat hepatocyte couplets. Gastroenterology 109, 1600-1611.
4. Breitfeld, P.P., McKinnon, W.C., and Mostov, K.E. (1990). Effect of nocodazole on vesicular traffic to the apical and basolateral surfaces of polarized MDCK cells. J. Cell Biol. 111, 2365-2373.
5. Chazaud, B., Muriel, M.P., Bauvy, C., Codogno, P., Aubery, M., and Decastel, M. (1994). Requirement of either the NH4Cl-sensitive or the cytochalasin D-sensitive pathway for ricin toxicity depends upon the enterocyric state of differentiation of HT-29 cells. Eur. J. Cell Biol. 64, 15-28.
6. Costa de Beauregard, M.A., Pringault, E., Robine, S., and Louvard, D. (1995). Suppression of villin expression by antisense RNA impairs brush border assembly in polarized epithelial intestinal cells. EMBO J. 14, 409-421.
7. Deckert, M., Ticchioni, M., and Bernard, A. (1996). Endocytosis of GPI-anchored proteins in human lymphocytes: role of glycolipid-based domains, actin cytoskeleton, and protein kinases. J. Cell Biol. 133, 791-799.
8. Drubin, D.G., and Nelson, W.J. (1996). Origins of cell polarity. Cell, 84, 335-344.
9. Durrbach, A., Louvard, D., and Coudrier, E. (1996). Actin filaments facilitate two steps of endocytosis. J. Cell Sci. 109, 457-465.
10. Eilers, U., Klumperman, J., and Hauri, H.P. (1989). Nocodazole, a microtubule-active drug, interferes with apical protein delivery in cultured intestinal epithelial cells (Caco-2). J. Cell Biol. 108, 13-22.
11. Fath, K.R., and Burgess, D.R. (1993). Golgi-derived vesicles from developing epithelial cells bind actin filaments and possess myosin-I as a cytoplasmically oriented peripheral membrane protein. J. Cell Biol. 120, 117-127.
12. Fath, K.R., Trimbur, G.M., and Burgess, D.R. (1994). Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells. J. Cell Biol. 126, 661-675.
13. Gautam, A., Ng, O.C., and Boyer, J.L. (1987). Isolated rat hepatocyte couplets in short-term culture: structural characteristics and plasma membrane reorganization. Hepatology 7, 216-223.
14. Gilbert, T., Le Bivic, A., Quaroni, A., and Rodriguez Boulan, E. (1991). Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells. J. Cell Biol. 113, 275-288.
15. Gottlieb, I.A., Ivanov, I.E., Adesnik, M., and Sabatini, D.D. (1993). Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120, 695-710.
16. Harada, M. et al. (1995). Role of cytoskeleton and acidification of endocytic compartment in asialoglycoprotein metabolism in isolated rat hepatocyte couplets. Hepatology 21, 1413-1421.
17. Hunziker, W., Male, P., and Mellman, I. (1990). Differential microtubule requirements for transcytosis in MDCK cells. EMBO J. 9, 3515-3525.
18. Jackman, M.R., Shurety, W., Ellis, J.A., and Luzio, J.P. (1994). Inhibition of apical but not basolateral endocytosis of ricin and folate in Caco-2 cells by cytochalasin D. J. Cell Sci. 107, 2547-2556.
19. Kok, J.W., Babia, T., and Hoekstra, D. (1991). Sorting of sphingolipids in the endocytic pathway of HT29 cells. J. Cell Biol. 114, 231-239.
20. Kok, J.W., Hoekstra, K., Eskelinen, S., and Hoekstra, D. (1992). Recycling pathways of glucosylceramide in BHK cells: distinct involvement of early and late endosomes. J. Cell Sci. 103, 1139-1152.
21. Kubler, E., and Riezman, H. (1993). Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J. 12, 2855-2862.
22. Lipsky, N.G., and Pagano, R.E. (1985). Intracellular translocation of fluorescent sphingolipids in cultured fibroblasts: endogenously synthesized sphingomyelin and glucocerebrosidase analogues pass through the Golgi apparatus en route to the plasma membrane. J. Cell Biol. 100, 27-34.
23. Maples, C.J., Ruiz, W.G., and Apodaca, G. (1997). Both microtubules and actin filaments are required for efficient postendocytotic traffic of the polymeric immunoglobulin receptor in polarized Madin-Darby canine kidney cells. J. Biol. Chem. 272, 6741-6751.
24. Matter, K., Bucher, K., and Hauri, H.P. (1990). Microtubule perturbation retards both the direct and the indirect apical pathway but does not affect sorting of plasma membrane proteins in intestinal epithelial cells (Caco-2). EMBO J. 9, 3163-3170.
25. Mays, R.W., Beck, K.A., and Nelson, W.J. (1994). Organization and function of the cytoskeleton in polarized epithelial cells: a component of the protein sorting machinery. Curr. Opin. Cell Biol. 6, 16-24.
26. Muallem, S., Kwiatkowska, K., Xu, X., and Yin, H.L. (1995). Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J. Cell Biol. 128, 589-598.
27. Nolan, C.M. (1992). Receptor-mediated endocytosis and lysosomal transport. In: Protein Targeting. A Practical Approach, ed. A.I. Magee and T. Wileman, Oxford: Oxford University Press, 1-23.
28. Parczyk, K., Haase, W., and Kondor Koch, C. (1989). Microtubules are involved in the secretion of proteins at the apical cell surface of the polarized epithelial cell, Madin-Darby canine kidney, J. Biol. Chem. 264, 16837-16846.
29. Parton, R.G., Joggerst, B., and Simons, K. (1994). Regulated internalization of caveolae. J. Cell Biol. 127, 1199-1215.
30. Sakisaka, S., Ng, O.C., and Boyer, J.L. (1988). Tubulovesicular transcytotic pathway in isolated rat hepatocyte couplets in culture. Effect of colchicine and taurocholate. Gastroenterology 95, 793-804.
31. Salas, P.J.I., Misek, D.E., Vega-Salas, D.E., Gundersen, D., Cereijido, M., and Rodriguez-Boulan, E. (1986). Microtubules and actin filaments are not critically involved in the biogenesis of epithelial cell surface polarity. J. Cell Biol. 102, 1853-1867.
32. Sandvig, K., and van Deurs, B. (1990). Selective modulation of the endocytic uptake of ricin and fluid phase markers without alteration in transferrin endocytosis. J. Biol. Chem. 265, 6382-6388.
33. Schnitzer, J.E., Oh, P., Pinney, E., and Allard, J. (1994). Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J. Cell Biol. 127, 1217-1232.
34. Spector, I., Shochet, N.R., Kashman, Y., and Groweiss, A. (1983) Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219, 493-495.
35. van IJzendoorn, S.C.D., Zegers, M.M.P., Kok, J.W., and Hoekstra, D. (1997). Segregation of glucosylceramide and sphingomyelin occurs in the apical to basolateral transcytotic route in HepG2 cells. J. Cell Biol. 137, 347-357.
36. van Meer, G., and van't Hof, W. (1993). Epithelial sphingolipid sorting is insensitive to reorganization of the Golgi by nocodazole, but is abolished by monensin and by brefeldin A. J. Cell Sci. 104, 833-842.
37. van Zeijl, M.J., and Matlin, K.S. (1990) Microtubule perturbation inhibits intracellular transport of an apical membrane glycoprotein in a substrate-dependent manner in polarized Madin-Darby canine kidney epithelial cells. Cell Regul. 1, 921-936.
38. Zaal, K.J.M., Kok, J.W., Sormunen, R., Eskelinen, S., and Hoekstra, D. (1994). Intracellular sites involved in the biogenesis of bile canalshy; iculi in hepatic cells. Eur. J. Cell Biol. 63, 10-19.
39. Zegers, M.M.P., and Hoekstra, D. (1997). Sphingolipid transport to the apical plasma membrane domain in human hepatoma cells is controlled by PKC and PKA activity: a correlation with cell polarity in HepG2 cells. J. Cell Biol. 138, 307-321.
40. Zegers, M.M.P., Kok, J.W., and Hoeksrra, D. (1997) Use of photoactivatable sphingolipid analogs to monitor lipid transport in mammalian cells. Biochem. J. 328, 489-498.