The ever-expanding role of degradation in the regulation of apolipoprotein B metabolism

Journal of Lipid Research

Volumn 50, Issue SUPPL., 2009, Pages

  Ginsberg, Henry N ^a   Fisher, Edward A ^b  

^a College of Physicians and Surgeons ^*  (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Lipids; Lipoproteins; Liver

Indexed keywords

APOLIPOPROTEIN B; FATTY ACID; INSULIN;

ENDOPLASMIC RETICULUM; HUMAN; METABOLISM; REVIEW; TRANSPORT AT THE CELLULAR LEVEL;

APOLIPOPROTEINS B; BIOLOGICAL TRANSPORT; ENDOPLASMIC RETICULUM; FATTY ACIDS; HUMANS; INSULIN;

EID: 66349135636     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.R800090-JLR200     Document Type: Review

References (47)

1. Williams, K. J., and I. Tabas. 2005. Lipoprotein retention-and clues for atheroma regression. Arterioscler. Thromb. Vasc. Biol. 25: 1536-1540. (Pubitemid 41098918)
2. Bostrom, K., M. Wettesten, J. Boren, 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. (Pubitemid 17196406)
3. Borchardt, R. A., and R. A. Davis. 1987. Intrahepatic assembly of very low density lipoproteins. Rate of transport out of the endoplasmic reticulum determines rate of secretion. J. Biol. Chem. 262: 16394-16402.
4. Fisher, E. A., and H. N. Ginsberg. 2002. Complexity in the secretory pathway: the assembly and secretion of apolipoprotein B-containing lipoproteins. J. Biol. Chem. 277: 17377-17380. (Pubitemid 34967535)
5. Adeli, K., C. Taghibiglou, S. C. Van Iderstine, and G. F. Lewis. 2001. Mechanisms of hepatic very low-density lipoprotein overproduction in insulin resistance. Trends Cardiovasc. Med. 11: 170-176. (Pubitemid 32946865)
6. Alder, N. N., and A. E. Johnson. 2004. Cotranslational membrane protein biogenesis at the endoplasmic reticulum. J. Biol. Chem. 279: 22787-22790. (Pubitemid 38685576)
7. Sturley, S. L., P. A. Talmud, R. Brasseur, M. R. Culbertson, S. E. Humphries, and A. D. Attie. 1994. Human apolipoprotein B signal sequence variants confer a secretion-defective phenotype when expressed in yeast. J. Biol. Chem. 269: 21670-21675.
8. Hegde, R. S., and V. R. Lingappa. 1996. Sequence-specific alteration of the ribosome-membrane junction exposes nascent secretory proteins to the cytosol. Cell. 85: 217-228.
9. Menetret, J. F., A. Neuhof, D. G. Morgan, K. Plath, M. Radermacher, T. A. Rapoport, and C. W. Akey. 2000. The structure of ribosome-channel complexes engaged in protein translocation. Mol. Cell. 6: 1219-1232.
10. Chuck, S. L., Z. Yao, B. D. Blackhart, B. J. McCarthy, and V. R. Lingappa. 1990. New variation on the translocation of proteins during early biogenesis of apolipoprotein B. Nature. 346: 382-385.
11. Yamaguchi, J., D. M. Conlon, J. J. Liang, E. A. Fisher, and H. N. Ginsberg. 2006. Translocation efficiency of apoliproptein B is determined by the presence of beta-sheet domains, not pause transfer sequences. J. Biol. Chem. 281: 27063-27071. (Pubitemid 44401735)
12. Hussain, M. M., J. Shi, and P. Dreizen. 2003. Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J. Lipid Res. 44: 22-32. (Pubitemid 36114766)
13. Pan, M., J. S. Liang, E. A. Fisher, and H. N. Ginsberg. 2000. Inhibition of translocation of nascent apolipoprotein B across the endoplasmic reticulum membrane is associated with selective inhibition of the synthesis of apolipoprotien B. J. Biol. Chem. 275: 27399-27405.
14. Mitchell, D. M., M. Zhou, R. Pariyarah, H. Wang, J. D. Aitchison, H. N. Ginsberg, and E. A. Fisher. 1998. Apoprotein B100 has a prolonged interaction with the translocon during which its lipidation and translocation change from dependence on the microsomal triglyceride transfer protein to independence. Proc. Natl. Acad. Sci. USA. 95: 14733-14738. (Pubitemid 29003699)
15. Dashti, N., M. Manchekar, Y. Liu, Z. Sun, and J. P. Segrest. 2007. Microsomal triglyceride transfer protein activity is not required for the initiation of apolipoprotein B-containing lipoprotein assembly in McA-RH7777 cells. J. Biol. Chem. 282: 28597-28608. (Pubitemid 47606040)
16. Wetterau, J. R., L. P. Aggerbeck, M. E. Bouma, C. Eisenberg, A. Munck, M. Hermier, J. Schmitz, G. Gay, D. J. Rader, and R. E. Gregg. 1992. Absence of microsomal triglyceride transfer protein in individuals with abetalipoproteinemia. Science. 258: 999-1001.
17. Benoist, F., and T. Grand-Perret. 1997. Co-translational degradation of apolipoprotein B100 by the proteasome is prevented by microsomal triglyceride transfer protein. Synchronized translation studies on HepG2 cells treated with an inhibitor of microsomal triglyceride transfer protein. J. Biol. Chem. 272: 20435-20442. (Pubitemid 27355596)
18. Dixon, J. L., S. Furukawa, and H. N. Ginsberg. 1991. Oleate stimulates secretion of apolipoprotein B-containing lipoproteins from Hep G2 cells by inhibiting early intracellular degradation of apolipoprotein B. J. Biol. Chem. 266: 5080-5086. (Pubitemid 21909463)
19. Brodsky, J. L. 2007. The protective and destructive roles played by molecular chaperones during ERAD (ER associated degradation). Biochem. J. 404: 353-363. (Pubitemid 46953909)
20. Zhou, M., E. A. Fisher, and H. N. Ginsberg. 1998. Regulated cotranslational ubiquitination of apoliprotein B100. A new paradigm for proteasomal degradation of a secretory protein. J. Biol. Chem. 273: 24649-24653. (Pubitemid 28454962)
21. Qiu, W., R. Kohen-Avramoglu, S. Mhapsekar, J. Tsai, R. C. Austin, and K. Adeli. 2005. Glucosamine-induced endoplasmic reticulum stress promotes ApoB100 degradation. Arterioscler. Thromb. Vasc. Biol. 25: 571-577.
22. Oyadomari, S., C. Yun, E. A. Fisher, N. Kreglinger, G. Kreibich, M. Oyadomari, H. P. Harding, A. G. Goodman, H. Harant, J. L. Garrison, et al. 2006. Cotranslocational degradation protects the stressed endoplasmic reticulum from protein overload. Cell. 126: 727-739. (Pubitemid 44233632)
23. Liang, J-S., T. Kim, S. Fang, A. M. Weissman, E. A. Fisher, and H. N. Ginsberg. 2003. Overexpression of the tumor autocrine motility factor receptor-gp78, a ubiquitin protein ligase (E3), results in increased ubiquitinylation and decreased secretion of apolipoprotein B100 in Hep G2 cells. J. Biol. Chem. 278: 23984-23988. (Pubitemid 36830228)
24. Nakatsukasa, K., G. Huyer, S. Michaelis, and J. L. Brodsky. 2008. Dissecting the ER-associated degradation of a misfolded polytopic membrane protein. Cell. 132: 101-112.
25. 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. 1265: 29-32.
26. Du, E. Z., S-L. Wang, H. J. Kayden, R. Sokol, L. K. Curtiss, and R. A. Davis. 1996. Translocation of apoplipoprotein B across the endoplasmic reticulum is blocked in abetalipoproteinemia. J. Lipid Res. 37: 1309-1315. (Pubitemid 26239085)
27. Kostova, Z., and D. H. Wolf. 2003. For whom the bell tolls: protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection. EMBO J. 22: 2309-2317. (Pubitemid 36604970)
28. Avramoglu, R. K., and K. Adeli. 2004. Hepatic regulation of apolipoprotein B. Rev. Endocr. Metab. Disord. 5: 293-301. (Pubitemid 39388747)
29. Liao, W., S. C. Yeung, and L. Chan. 1998. Proteasome-mediated degradation of apolipoprotein B targets both nascent peptides cotranslationally before translocation and full-length apolipoprotein B after translocation into the endoplasmic reticulum. J. Biol. Chem. 273: 27225-27230. (Pubitemid 28500433)
30. Huang, X. F., and G. S. Shelness. 1999. Efficient glycosylation site utilization by intracellular apolipoprotein B. Implications for proteasomal degradation. J. Lipid Res. 40: 2212-2222. (Pubitemid 30017523)
31. Schroder, M., and R. J. Kaufman. 2005. The mammalian unfolded protein response. Annu. Rev. Biochem. 74: 739-789. (Pubitemid 40995523)
32. Ota, T., C. Gayet, and H. N. Ginsberg. 2008. Selective inhibition of apolipoprotein B100 secretion by lipid-induced hepatic endoplasmic reticulum stress. J. Clin. Invest. 118: 316-332.
33. Dixon, J. L., and H. N. Ginsberg. 1993. Regulation of hepatic secretion of apolipoprotein B-containing lipoproteins: information obtained from cultured liver cells. J. Lipid Res. 34: 167-179. (Pubitemid 23067522)
34. Zhang, Y-L., A. Hernandez-Ono, C. Ko, K. Yasunaga, L-S. Huang, and H. N. Ginsberg. 2004. Regulation of hepatic apolipoprotein B-lipoprotein assembly and secretion by the availability of fatty acids 1: differential effects of delivering fatty acids via albumin or remnant-like emulsion particles. J. Biol. Chem. 279: 19362-19374. (Pubitemid 38623367)
35. Pan, M., A. I. Cederbaum, Y. L. Zhang, H. N. Ginsberg, J. Williams, and E. A. Fisher. 2004. Lipid peroxidation and oxidant stress regulate hepatic apolipoprotein B degradation and VLDL production. J Clin Invest. 113: 1277-1287. (Pubitemid 39069927)
36. Fisher, E. A., M. Pan, X. Chen, X. Wu, H. Wang, H. Jamil, J. D. Sparks, and K. J. Williams. 2001. The triple threat to nascent apolipoprotein B. Evidence for multiple, distinct degradative pathways. J. Biol. Chem. 276: 27855-27863.
37. Pan, M., V. Maitin, S. Parathath, U. Andreo, S. X. Lin, C. St Germain, Z. Yao, F. R. Maxfield, K. J. Williams, and E. A. Fisher. 2008. Presecretory oxidation, aggregation, and autophagosomal destruction of apolipoprotein-B: a pathway for late-stage quality control. Proc. Natl. Acad. Sci. USA. 105: 5862-5867. (Pubitemid 351758463)
38. Iwata, A., J. C. Christianson, M. Bucci, L. M. Ellerby, N. Nukina, L. S. Forno, and R. R. Kopito. 2005. Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. Proc. Natl. Acad. Sci. USA. 102: 13135-13140. (Pubitemid 41324991)
39. Bernales, S., K. L. McDonald, and P. Walter. 2006. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 4: e423.
40. Sparks, J. D., and C. E. Sparks. 1990. Insulin modulation of hepatic synthesis and secretion of apolipoprotein B by rat hepatocytes. J. Biol. Chem. 265: 8854-8862.
41. Phung, T. L., A. Roncone, K. L. Jensen, C. E. Sparks, and J. D. Sparks. 1997. Phosphoinositide 3-kinase activity is necessary for insulin-dependent inhibition of apolipoprotein B secretion by rat hepatocytes and localizes to the endoplasmic reticulum. J. Biol. Chem. 272: 30693-30702. (Pubitemid 27527502)
42. Tsai, J., W. Qiu, R. Kohen-Avramoglu, and K. Adeli. 2007. MEK-ERK inhibition corrects the defect in VLDL assembly in HepG2 cells: potential role of ERK in VLDL-ApoB100 particle assembly. Arterioscler. Thromb. Vasc. Biol. 27: 211-218. (Pubitemid 46360401)
43. Chirieac, D. V., H. L. Collins, J. Cianci, J. D. Sparks, and C. E. Sparks. 2004. Altered triglyceride-rich lipoprotein production in Zucker diabetic fatty rats. Am. J. Physiol. Endocrinol. Metab. 287: E42-E49. (Pubitemid 38856280)
44. Taghibiglou, C., A. Carpentier, S. C. Van Iderstine, B. Chen, D. Rudy, A. Aiton, G. F. Lewis, and K. Adeli. 2000. Mechanisms of hepatic very low density lipoprotein overproduction in insulin resistance. Evidence for enhanced lipoprotein assembly, reduced intracellular apoB degradation, and increased microsomal triglyceride transfer protein in a fructose-fed hamster model. J. Biol. Chem. 275: 8416-8425. (Pubitemid 30180185)
45. Avramoglu, R. K., H. Basciano, and K. Adeli. 2006. Lipid and lipoprotein dysregulation in insulin resistant states. Clin. Chim. Acta. 368: 1-19. (Pubitemid 43776015)
46. Biddinger, S. B., A. Hernandez-Ono, C. Rask-Madsen, J. T. Haas, J. O. Aleman, R. Suzuki, E. F. Scapa, C. Agarwal, M. C. Carey, G. Stephanopoulos, et al. 2008. Hepatic insulin resistance is sufficient to produce dyslipidemia and susceptibility to atherosclerosis. Cell Metab. 7: 95-96.
47. Sparks, J. D., and C. E. Sparks. 2008. Overindulgence and metabolic syndrome: is FoxO1 a missing link? J. Clin. Invest. 118: 2012-2015. (Pubitemid 351872319)