Apolipoprotein B-100 destined for lipoprotein assembly and intracellular degradation undergoes efficient translocation across the endoplasmic reticulum membrane

Journal of Lipid Research

Volumn 37, Issue 10, 1996, Pages 2202-2214

  Ingram, Michael F ^a   Shelness, Gregory S ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

ALLN; HepG2 cells; lipoprotein assembly; protein turnover; very low density lipoprotein

Indexed keywords

ALBUMIN; APOLIPOPROTEIN B100; HYBRID PROTEIN; PROTEINASE; PROTEINASE INHIBITOR;

ARTICLE; CELL STRAIN HEPG2; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; LIPOPROTEIN SYNTHESIS; MEMBRANE TRANSPORT; PRIORITY JOURNAL; PROTEIN DEGRADATION;

APOLIPOPROTEIN B-100; APOLIPOPROTEIN B-48; APOLIPOPROTEINS B; BIOLOGICAL TRANSPORT; CARCINOMA, HEPATOCELLULAR; ENDOPLASMIC RETICULUM; HUMANS; IMMUNOBLOTTING; INTRACELLULAR MEMBRANES; LEUPEPTINS; LIPOPROTEINS; LIVER; LIVER NEOPLASMS; PROTEASE INHIBITORS; TRYPSIN; TUMOR CELLS, CULTURED;

EID: 0029993847     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (59)

1. Alexander, C. A., R. L. Hamilton, and R. J. Havel. 1976. Subcellular localization of B apoprotein of plasma lipoproteins in rat liver. J. Cell Biol. 69: 241-263.
2. Rusiñol, A., H. Verkade, and J. E. Vance. 1993. Assembly of rat hepatic very low density lipoproteins in the endoplasmic reticulum. J. Biol. Chem. 268: 3555-3562.
3. Borén, J., L. Graham, M. Wettesten, J. Scott, A. White, and S-O. Olofsson. 1992. The assembly and secretion of apoB-100-containing lipoproteins in HepG2 cells. ApoB-100 is cotranslationally integrated into lipoproteins. J. Biol. Chem. 267: 9858-9867.
4. Borén, J., S. Rustaeus, and S-O. Olofsson. 1994. Studies on the assembly of apolipoprotein B-100- and B-48-containing very low density lipoproteins in McA-RH7777 cells. J. Biol. Chem. 269: 25879-25888.
5. Helenius, A., and K. Simons. 1971. Removal of lipids from human plasma low-density lipoprotein by detergents. Biochemistry. 10: 2542-2547.
6. Davis, R. A., R. N. Thrift, C. C. Wu, and K. E. Howell. 1990. Apolipoprotein B is both integrated into and translocated across the endoplasmic reticulum membrane. J. Biol. Chem. 265: 10005-10011.
7. Thrift, R. N., J. Drisko, S. Dueland, J. D. Trawick, and R. A. Davis. 1992. Translocation of apolipoprotein B across the endoplasmic reticulum is blocked in a nonhepatic cell line. Proc. Natl. Acad. Sci. USA. 89: 9161-9165.
8. Sakata, N., X. Wu, J. L. Dixon, and H. N. Ginsberg. 1993. Proteolysis and lipid-facilitated translocation are distinct but competitive processes that regulate secretion of apolipoprotein B in HepG2 cells. J. Biol. Chem. 268: 22967-22970.
9. Du, E. Z., J. Kurth, S-L. Wang, P. Humiston, and R. A. Davis. 1994. Proteolysis-coupled secretion of the N terminus of apolipoprotein B. Characterization of a transient, translocation arrested intermediate. J. Biol. Chem. 269: 24169-24176.
10. Dixon, J. L., T. Chattapadhyay, T. Huima, C. M. Redman, and D. Banerjee. 1992. Biosynthesis of lipoproteins: location of nascent apoA-I and apoB in the rough endoplasmic reticulum of chicken hepatocytes. J. Cell Biol. 117: 1161-1169.
11. Rusiñol, A. E., E. Y. W. Chan, and J. E. Vance. 1993. Movement of apolipoprotein B into the lumen of microsomes from hepatocytes is disrupted in membranes enriched in phosphatidylmonomethylethanolamine. J. Biol. Chem. 268: 25168-25175.
12. Furukawa, S., N. Sakata, H. N. Ginsberg, and J. L. Dixon. 1992. Studies of the sites of intracellular degradation of apolipoprotein B in HepG2 cells. J. Biol. Chem. 267: 22630-22638.
13. Verkade, H. J., D. G. Fast, A. E. Rusiñol, D. G. Scraba, and D. E. Vance. 1993. Impaired biosynthesis of phosphatidylcholine causes a decrease in the number of very low density lipoprotein particles in the Golgi but not in the endoplasmic reticulum of rat liver. J. Biol. Chem. 268: 24990-24996.
14. Borén, J., S. Rustaeus, M. Wettesten, M. Andersson, A. Wiklund, and S-O. Olofsson. 1993. Influence of triacylglycerol biosynthesis rate on the assembly of apoB-100-containing lipoproteins in HepG2 cells. Arterioscler. Thromb. 13: 1743-1754.
15. Wang, C. N., T. C. Hobman, and D. N. Brindley. 1995. Degradation of apolipoprotein B in cultured rat hepatocytes occurs in a post-endoplasmic reticulum compartment. J. Biol. Chem. 270: 24924-24931.
16. Bonnardel, J. A., and R. A. Davis. 1995. In HepG2 cells, translocation, not degradation, determines the fate of the de novo synthesized apolipoprotein B. J. Biol. Chem. 270: 28892-28896.
17. Wilkinson, J., J. A. Higgins, P. Groot, E. Gherardi, and D. Bowyer. 1993. Topography of apolipoprotein B in subcellular fractions of rabbit liver probed with a panel of monoclonal antibodies. J. Lipid Res. 34: 815-825.
18. Rusiñol, A. E., and J. E. Vance. 1995. Inhibition of secretion of truncated apolipoproteins B by monomethylethanolamine is independent of the length of the apolipoprotein. J. Biol. Chem. 270: 13318-13325.
19. Zhou, M. Y., X. J. Wu, L. S. Huang, and H. N. Ginsberg. 1995. Apoprotein B-100, an inefficiently translocated secretory protein, is bound to the cytosolic chaperone, heat shock protein 70. J. Biol. Chem. 270: 25220-25224.
20. Chuck, S. L., Z. Yao, B. D. Blackhart, B. J. McCarthy, and V. R. Lingappa. 1990. New variations on the translocation of proteins during early biogenesis of apolipoprotein B. Nature. 346: 382-385.
21. Chuck, S. L., and V. R. Lingappa. 1992. Pause transfer: a topogenic sequence in apolipoprotein B mediates stopping and restarting of translocation. Cell. 68: 9-21.
22. Chuck, S. L., and V. R. Lingappa. 1993. Analysis of a pause transfer sequence from apolipoprotein B. J. Biol. Chem. 268: 22794-22801.
23. Hegde, R. S., and V. R. Lingappa. 1996. Sequence-specific alterations of the ribosome-membrane junction exposes nascent secretory proteins to the cytosol. Cell. 85: 217-228.
24. Shelness, G. S., K. C. Morris-Rogers, and M. F. Ingram. 1994. Apolipoprotein B48-membrane interactions. Absence of transmembrane localization in nonhepatic cells. J. Biol. Chem. 269: 9310-9318.
25. Pease, R. J., J. M. Leiper, G. B. Harrison, and J. Scott. 1995. Studies on the translocation of the amino terminus of apolipoprotein B into the endoplasmic reticulum. J. Biol. Chem. 270: 7261-7271.
26. Shelness, G. S., and J. T. Thornburg. 1996. The role of intramolecular disulfide bond formation in the assembly and secretion of apolipoprotein B-100-containing lipoproteins. J. Lipid Res. 37: 408-419.
27. Dawson, P. A., S. L. Hofmann, D. R. van der Westhuyzen, T. C. Südhof, M. S. Brown, and J. L. Goldstein. 1988. Sterol-dependent repression of low density lipoprotein receptor promoter mediated by 16-base pair sequence adjacent to binding site for transcription factor Sp1. J. Biol. Chem. 263: 3372-3379.
28. Chamberlain, J. P. 1979. Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble fluor, sodium salicylate. Anal. Biochem. 98: 132-135.
29. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose paper: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76: 4350-4354.
30. Harlow, E., and D. Lane. 1988. Antibodies: a Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor. 490-492.
31. Hopp, T. P., K. S. Prickett, V. L. Price, R. T. Libby, C. J. March, D. P. Cerretti, D. L. Urdal, and P. J. Conlon. 1988. A short polypeptide marker sequence useful for recombinant protein identification and purification. BioTechnology. 6: 1204-1210.
32. Brizzard, B. L., R. G. Chubet, and D. L. Vizard. 1994. Immunoaffinity purification of FLAG epitope-tagged bacterial alkaline phosphatase using a novel monoclonal antibody and peptide elution. BioTechniques. 16: 730-734.
33. de Bruijn, M. H. L., and G. H. Fey. 1985. Human complement component C3: cDNA coding sequence and derived primary structure. Proc. Natl. Acad. Sci. USA. 82: 708-712.
34. Boström, K., M. Wettesten, J. Borén, G. Bondjers, O. Wiklund, and S-O. Olofsson. 1986. Pulse-chase studies of the synthesis and intracellular transport of apolipoprotein B-100 in HepG2 cells. J. Biol. Chem. 261: 13800-13806.
35. Blobel, G., and B. Dobberstein. 1975. Transfer of proteins across membranes: I. Presence of proteolytically processed and unprocessed nascent immunoglubulin light chains on membrane-bound ribosomes of murine myeloma. J. Cell Biol. 67: 835-851.
36. Blobel, G., and B. Dobberstein. 1975. Transfer of proteins across membranes: II. Reconstitution of functional rough microsomes from heterologous components. J. Cell Biol. 67: 852-862.
37. Walter, P., and G. Blobel. 1983. Preparation of microsomal membranes for cotranslational protein translocation. Methods Enzymol. 96: 84-93.
38. Wada, I., D. Rindress, P. H. Cameron, W-J. Ou, J. J. Doherty, II, D. Louvard, A. W. Bell, D. Dignard, D. Y. Thomas, and J. J. M. Bergeron. 1991. SSRα and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J. Biol. Chem. 266: 19599-19610.
39. 2+. J. Biol. Chem. 270: 18051-18059.
40. Shelness, G. S., L. Lin, and C. V. Nicchitta. 1993. Membrane topology and biogenesis of eukaryotic signal peptidase. J. Biol. Chem. 268: 5201-5208.
41. Crimaudo, C., M. Hortsch, H. Gausepohl, and D. I. Meyer. 1987. Human ribophorins I and II: the primary structure and membrane topology of two highly conserved rough endoplasmic reticulum-specific glycoproteins. EMBO J. 6: 75-82.
42. Kreibich, G., P. Debey, and D. Sabatini. 1973. Selective release of content from microsomal vesicles without membrane disassembly. I. Permeability changes induced by low detergent concentration. J. Cell Biol. 58: 436-462.
43. Price, N. C., and C. M. Johnson. 1989. Proteinases as probes of conformation of soluble proteins. In Proteolytic Enzymes: a Practical Approach. R. J. Beynon and J. S. Bond, editors. IRL Press at Oxford University Press, Oxford. 163-180.
44. Liebherz, H. G., T. Burke, J. E. Shackelford, J. E. Strickler, and K. J. Wilson. 1986. Specific proteolytic modification of creatine kinase isoenzymes. Implication of C-terminal involvement in enzymatic activity but not in subunitsubunit recognition. Biochem. J. 233: 51-56.
45. Ebeling, W., N. Hennrich, M. Klockow, H. Metz, H. D. Orth, and H. Lang. 1974. Proteinase K from Tritirachium album Limber. Eur. J. Biochem. 47: 91-97.
46. Hazuda, D. J., J. Strickler, P. Simon, and P. R. Young. 1991. Structure-function mapping of interleukin 1 precursors: cleavage leads to a conformational change in the mature protein. J. Biol. Chem. 266: 7081-7086.
47. Segrest, J. P., M. K. Jones, V. K. Mishra, G. M. Anantharamaiah, and D. W. Garber. 1994. ApoB-100 has a pentapartite structure composed of three amphipathic α-helical domains alternating with two amphipathic β-strand domains: detection by the computer program LOCATE. Arterioscler. Thromb. 14: 1674-1685.
48. Sallach, S. M., and K. Adeli. 1995. Intracellular degradation of apolipoprotein B generates an N-terminal 70 kDa fragment in the endoplasmic reticulum. Biochim. Biophys. Acta Mol. Cell Res. 1265: 29-32.
49. Adeli, K. 1994. Regulated intracellular degradation of apolipoprotein B in semipermeable HepG2 cells. J. Biol. Chem. 269: 9166-9175.
50. Du, E. Z., S-L. Wang, H. J. Kayden, R. Sokol, L. K. Curtiss, and R. A. Davis. 1996. Translocation of apolipoprotein B across the endoplasmic reticulum is blocked in abetalipoproteinemia. J. Lipid Res. 37: 1309-1315.
51. Morimoto, T., M. Arpin, and S. Gaetani. 1983. Use of proteases for the study of membrane insertion. Methods Enzymol. 96: 121-150.
52. Pratt, J. M. 1989. Proteases as topological probes for membrane proteins. In Proteolytic Enzymes: a Practical Approach. R. J. Beynon and J. S. Bond, editors. IRL Press at Oxford University Press, Oxford. 181-191.
53. Wong, L., and A. Torbati. 1994. Differentiation of intrahepatic membrane-bound and secretory apolipoprotein B by monoclonal antibodies: membrane-bound apolipoprotein B is more glycosylated. Biochemistry. 33: 1923-1929.
54. Pease, R. J., G. B. Harrison, and J. Scott. 1991. Cotranslocational insertion of apolipoprotein B into the inner leaflet of the endoplasmic reticulum. Nature. 353: 448-450.
55. Yang, C-y., Z-W. Gu, S-a. Weng, T. W. Kim, S-H. Chen, H. J. Pownall, P. M. Sharp, S-W. Liu, W-H. Li, A. M. Gotto, Jr., and L. Chan. 1989. Structure of apolipoprotein B-100 of human low density lipoprotein. Arteriosclerosis. 9: 96-108.
56. Hirschberg, D. B., and M. D. Snider. 1987. Topography of glycoyslation in the rough endoplasmic reticulum and Golgi apparatus. Annu. Rev. Biochem. 56: 63-87.
57. Leiper, J. M., G. B. Harrison, J. D. Bayliss, J. Scott, and R. J. Pease. 1996. Systematic expression of the complete coding sequence of apoB-100 does not reveal transmembrane determinants. J. Lipid Res. 37: 2215-2231.
58. Dixon, J. L., S. Furukawa, and H. N. Ginsberg. 1991. Oleate stimulates secretion of apolipoprotein B-containing lipoproteins from HepG2 cells by inhibiting early intracellular degradation of apolipoprotein B. J. Biol. Chem. 266: 5080-5086.
59. Hammond, C., and A. Helenius. 1995. Quality control in the secretory pathway. Curr. Opin. Cell Biol. 7: 523-529.