Different transport routes for high density lipoprotein and its associated free sterol in polarized hepatic cells

Journal of Lipid Research

Volumn 45, Issue 3, 2004, Pages 427-437

  Wüstner, Daniel ^a,b   Mondal, Mousumi ^a   Huang, Amy ^a   Maxfield, Frederick R ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Bile; Dehydroergosterol; Fluorescence microscopy; Hepatocytes

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALEXA 488; APOLIPOPROTEIN; BLOCKING ANTIBODY; DEHYDROERGOSTEROL; ERGOSTEROL; HIGH DENSITY LIPOPROTEIN; METHYL BETA CYCLODEXTRIN; REAGENT; RECEPTOR ANTIBODY; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR BI; STEROL; UNCLASSIFIED DRUG;

APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; BILE; CELL POLARITY; CELL STRAIN HEPG2; CELL SURFACE; CHEMICAL LABELING; ENDOSOME; ENERGY METABOLISM; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INTERNALIZATION; INTRACELLULAR TRANSPORT; INTRAHEPATIC BILE DUCT; LIPID TRANSPORT; LIVER CELL; LYSOSOME; PRIORITY JOURNAL; RECYCLING;

ADENOSINE TRIPHOSPHATE; BIOLOGICAL TRANSPORT; CELL LINE, TUMOR; CELL POLARITY; ENDOCYTOSIS; ENDOSOMES; ERGOSTEROL; FLUORESCENCE; HEPATOCYTES; HUMANS; KINETICS; LIPOPROTEINS, HDL; LYSOSOMES; SPECTROMETRY, FLUORESCENCE; STEROLS;

EID: 12144286290     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M300440-JLR200     Document Type: Article

References (43)

1. Kuipers, F., R. P. J. Oude Elferink, H. Verkade, and A. K. Groen. 1997. Mechanisms and (patho) physiological significance of biliary cholesterol secretion. Subcell. Biochem. 28: 1053-1060.
2. Robins, S. J., and J. M. Fasulo. 1997. High density lipoproteins, but not other lipoproteins, provide a vehicle for sterol transport to bile. J. Clin. Invest. 99: 380-384.
3. Robins, S. J., and J. M. Fasulo. 1999. Delineation of a novel hepatic route for the selective transfer of unesterified sterols from high-density lipoproteins to bile: studies using the perfused rat liver. Hepatology. 29: 1541-1548.
4. Yu, L., J. Li-Hawkins, R. E. Hammer, K. E. Berge, J. D. Horton, J. C. Cohen, and H. H. Hobbs. 2002. Overexpression of ABCG5 and ABCG8 promotes biliary cholesterol secretion and reduces fractional absorption of dietary cholesterol. J. Clin. Invest. 110:671-680.
5. Graf, G. A., W. P. Li, R. D. Gerard, I. Gelissen, A. White, J. C. Cohen, and H. H. Hobbs. 2002. Coexpression of ATP-binding cassette proteins ABCG5 and ABCG8 permits their transport to the apical surface. J. Clin. Invest. 110: 659-669.
6. Jackle, S., F. Rinninger, T. Lorenzen, H. Greten, and E. Windler. 1993. Dissection of compartments in rat hepatocytes involved in the intracellular trafficking of high-density lipoprotein particles or their selectively internalized cholesteryl esters. Hepatology. 17: 455-465.
7. Kambouris, A. M., P. D. Roach, G. D. Calvert, and P. J. Nestel. 1990. Retroendocytosis of high density lipoproteins by the human hepatoma cell line, HepG2. Arteriosclerosis. 10: 582-590.
8. DeLamatre, J. G., T. G. Sarphie, R. C. Archibold, and C. A. Hornick. 1990. Metabolism of apoE-free high density lipoprotein in rat hepatoma cells: evidence for a retroendocytic pathway. J. Lipid Res. 31: 191-202.
9. Silver, D. L., N. Wang, and A. R. Tall. 2000. Defective HDL particle uptake in ob/ob hepatocytes causes decreased recycling, degradation, and selective lipid uptake. J. Clin. Invest. 105: 151-159.
10. Sormunen, R., S. Eskelinen, and V. P. Lehto. 1993. Bile canaliculus formation in cultured HepG2 cells. Lab. Invest. 68: 652-662.
11. Wüstner, D., A. Herrmann, M. Hao, and F. R. Maxfield. 2002. Rapid nonvesicular transport of sterol between the plasma membrane domains of polarized hepatic cells. J. Biol. Chem. 277: 30325-30336.
12. Wüstner, D., S. Mukherjee, F. R. Maxfield, P. Müller, and A. Herrmann. 2001. Vesicular and nonvesicular transport of phosphatidylcholine in polarized HepG2 cells. Traffic. 2: 277-296.
13. 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.
14. Silver, D. L., N. Wang, X. Xiao, and A. R. Tall. 2001. High density lipoprotein (HDL) particle uptake mediated by scavenger receptor class B type 1 results in selective sorting of HDL cholesterol from protein and polarized cholesterol secretion. J. Biol. Chem. 276:25287-25293.
15. Hao, M., S. X. Lin, O.J. Karylowski, D. Wüstner, T. E. McGraw, and F. R. Maxfield. 2002. Vesicular and non-vesicular sterol transport in living cells. The endocytic recycling compartment is a major sterol storage organelle. J. Biol. Chem. 277: 609-617.
16. Sheets, E. D., D. Holowka, and B. Baird. 1999. Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of FcepsilonRI and their association with detergent-resistant membranes. J. Cell Biol. 145: 877-887.
17. Loura, L. M., and M. Prieto. 1997. Dehydroergosterol structural organization in aqueous medium and in a model system of membranes. Biophys. J. 72: 2226-2236.
18. Mukherjee, S., X. Zha, I. Tabas, and F. R. Maxfield. 1998. Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys. J. 75: 1915-1925.
19. Ghosh, R. N., and F. R. Maxfield. 1995. Evidence for nonvectorial, retrograde transferrin trafficking in the early endosomes of HEp2 cells. J. Cell Biol. 128: 549-561.
20. Mukherjee, S., T. T. Soe, and F. R. Maxfield. 1999. Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J. Cell Biol. 144: 1271-1284.
21. Mayor, S., J. F. Presley, and F. R. Maxfield. 1993. Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. J. Cell Biol. 121: 1257-1269.
22. Mallet, W. G., and F. R. Maxfield. 1999. Chimeric forms of furin and TGN38 are transported from the plasma membrane to the trans-Golgi network via distinct endosomal pathways. J. Cell Biol. 146:345-359.
23. Kozarsky, K. F., M. H. Donahee, A. Rigotti, S. N. Iqbal, E. R. Edelman, and M. Krieger. 1997. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature. 387: 414-417.
24. Thuahnai, S. T., S. Lund-Katz, G. M. Anantharamaiah, D. L. Williams, and M. C. Phillips. 2003. A quantitative analysis of apolipoprotein binding to SR-BI: multiple binding sites for lipid-free and lipid-associated apolipoproteins. J. Lipid Res. 44: 1132-1142.
25. Mukherjee, S., R. N. Ghosh, and F. R. Maxfield. 1997. Endocytosis. Physiol. Rev. 77: 759-803.
26. Tycko, B., C. H. Keith, and F. R. Maxfield. 1983. Rapid acidification of endocytic vesicles containing asialoglycoprotein in cells of a human hepatoma line. J. Cell Biol. 97: 1762-1776.
27. Stoorvogel, W., H. J. Geuze, and G. J. Strous. 1987. Sorting of endocytosed transferrin and asialoglycoprotein occurs immediately after internalization in HepG2 cells. J. Cell Biol. 104: 1261-1268.
28. Garcia, A., R. Barbaras, X. Collet, A. Bogyo, H. Chap, and B. Perret. 1996. High-density lipoprotein 3 receptor-dependent endocytosis pathway in a human hepatoma cell line (HepG2). Biochemistry. 35: 13064-13071.
29. van Ijzendoorn, S. C., and D. Hoekstra. 1999. Polarized sphingolipid transport from the subapical compartment: evidence for distinct sphingolipid domains. Mol. Biol. Cell. 10: 3449-3461.
30. Maier, O., and D. Hoekstra. 2003. Trans-Golgi network and subapical compartment of HepG2 cells display different properties in sorting and exiting of sphingolipids. J. Biol. Chem. 278: 164-173.
31. Paresce, D. M., H. Chung, and F. R. Maxfield. 1997. Slow degradation of aggregates of the Alzheimer's disease amyloid beta-protein by microglial cells. J. Biol. Chem. 272: 29390-29397.
32. Ji, Y., N. Wang, R. Ramakrishnan, E. Sehayek, D. Huszar, J. L. Breslow, and A. R. Tall. 1999. Hepatic scavenger receptor BI promotes rapid clearance of high density lipoprotein free cholesterol and its transport into bile. J. Biol. Chem. 274: 33398-33402.
33. Rinninger, F., M. Brundert, S. Jackle, P. R. Galle, C. Busch, J. R. Izbicki, X. Rogiers, D. Henne-Bruns, B. Kremer, C. E. Broelsch, and H. Greeten. 1994. Selective uptake of high-density lipoprotein-associated cholesteryl esters by human hepatocytes in primary culture. Hepatology. 19: 1100-1114.
34. Martinez, L. O., V. Georgeaud, C. Rolland, X. Collet, F. Terce, B. Perret, and R. Barbaras. 2000. Characterization of two high-density lipoprotein binding sites on porcine hepatocyte plasma membranes: contribution of scavenger receptor class B type I (SR-BI) to the low-affinity component. Biochemistry. 39: 1076-1082.
35. Witt, W., I. Kolleck, H. Fechner, P. Sinha, and B. Rüstow. 2000. Regulation by vitamin E of the scavenger receptor BI in rat liver and HepG2 cells. J. Lipid Res. 41: 2009-2016.
36. Barbaras, R., X. Collet, H. Chap, and B. Perret. 1994. Specific binding of free apolipoprotein A-I to a high-affinity binding site on HepG2 cells: characterization of two high-density lipoprotein sites. Biochemistry. 33: 2335-2340.
37. Georgeaud, V., A. Garcia, D. Cachot, C. Rolland, F. Terce, H. Chap, X. Collet, B. Perret, and R. Barbaras. 2000. Identification of an ApoA-I ligand domain that interacts with high-affinity binding sites on HepG2 cells. Biochem. Biophys. Res. Commun. 267: 541-545.
38. Martinez, L. O., S. Jacquet, J-P. Esteve, C. Rolland, E. Cabezon, E. Champagne, T. Pineau, V. Georgeaud, J. E. Walker, F. Terce, X. Collet, B. Perret, and R. Barbaras. 2003. Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature. 421: 75-79.
39. Rogler, G., G. Herold, C. Fahr, M. Fahr, D. Rogler, F. M. Reimann, and E. F. Stange. 1992. High-density lipoprotein 3 retroendocytosis: a new lipoprotein pathway in the enterocyte (Caco-2). Gastroenterology. 103: 469-480.
40. 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 basolateral transcytotic route in HepG2 cells. J. Cell Biol. 137: 347-357.
41. Wittenburg, H., and M. C. Carey. 2002. Biliary cholesterol secretion by the twinned sterol half-transporters ABCG5 and ABCG8. J. Clin. Invest. 110: 605-609.
42. Hao, M., and F. R. Maxfield. 2000. Characterization of rapid membrane internalization and recycling. J. Biol. Chem. 275:15279-15286.
43. Sheff, D. R., E. A. Daro, M. Hull, and L. Mellman. 1999. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J. Cell Biol. 145: 123-139.