Apolipoprotein B100 biogenesis: A complex array of intracellular mechanisms regulating folding, stability, and lipoprotein assembly

Biochemistry and Cell Biology

Volumn 88, Issue 2, 2010, Pages 251-267

  Rutledge, Angela C ^a   Su, Qiaozhu ^a   Adeli, Khosrow ^a  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

ApoB; ER associated degradation; Lipoprotein assembly; Misfolding

Indexed keywords

DEGRADATION; SYNTHESIS (CHEMICAL);

AMPHIPATHIC; APOB; APOLIPOPROTEINS; AUTOPHAGY; DISULFIDE BOND FORMATION; DOMAIN STRUCTURE; HEPATOCYTES; INTRACELLULAR DEGRADATION; LIPID SPECIES; LIPID-BINDING PROTEINS; LIPIDATION; LIPOPROTEIN ASSEMBLY; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEINS; MISFOLDING; PROTEASOMAL DEGRADATION; UBIQUITINATION; VERY LOW DENSITY LIPOPROTEINS; VITELLOGENIN;

PROTEINS;

APOLIPOPROTEIN B100; CHAPERONE; LIPID BINDING PROTEIN; LIPOPROTEIN; MESSENGER RNA; VERY LOW DENSITY LIPOPROTEIN; VITELLOGENIN; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL;

AUTOPHAGY; BIOGENESIS; CONFERENCE PAPER; DISULFIDE BOND; ENDOPLASMIC RETICULUM; GLYCOSYLATION; LIVER CELL; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; OXIDATIVE STRESS; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; UBIQUITINATION; ANIMAL; BIOSYNTHESIS; CHEMISTRY; GENETICS; HUMAN; METABOLISM; RNA EDITING;

ANIMALS; APOLIPOPROTEIN B-100; CHOLESTEROL, VLDL; HUMANS; PROTEIN FOLDING; PROTEIN STABILITY; RNA EDITING;

EID: 77950622565     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O09-168     Document Type: Conference Paper

References (150)

1. Adeli, K. 1994. Regulated intracellular degradation of apolipoprotein B in semipermeable HepG2 cells. J. Biol. Chem. 269(12): 9166-9175. PMID:8132654.
2. Antes, T.J., Goodart, S.A., Chen, W., and Levy-Wilson, B. 2001. Human apolipoprotein B gene intestinal control region. Biochemistry, 40(23): 6720-6730. doi:10.1021/bi010073a. PMID:11389586.
3. Babin, P.J., Bogerd, J., Kooiman, F.P., Van Marrewijk, W.J., and Van der Horst, D.J. 1999. Apolipophorin II/I, apolipoprotein B, vitellogenin, and microsomal triglyceride transfer protein genes are derived from a common ancestor. J. Mol. Evol. 49(1): 150-160. doi:10.1007/PL00006528. PMID:10368443.
4. Baker, M.E. 1988. Is vitellogenin an ancestor of apolipoprotein B-100 of human low-density lipoprotein and human lipoprotein lipase? Biochem. J. 255(3): 1057-1060. PMID:3145737.
5. Bakillah, A., and Hussain, M.M. 2001. Binding of microsomal triglyceride transfer protein to lipids results in increased affinity for apolipoprotein B: evidence for stable microsomal MTP-lipid complexes. J. Biol. Chem. 276(33): 31466-31473. doi:10.1074/jbc.M100390200. PMID:11427523.
6. Barlowe, C. 2000. Traffic COPs of the early secretory pathway. Traffic, 1(5): 371-377. doi:10.1034/j.1600-0854.2000.010501.x. PMID:11208122.
7. Bernales, S., McDonald, K.L., and Walter, P. 2006. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 4(12): e423. doi:10.1371/journal.pbio.0040423. PMID:17132049.
8. Berriot-Varoqueaux, N., Aggerbeck, L.P., Samson-Bouma, M., and Wetterau, J.R. 2000. The role of the microsomal triglygeride transfer protein in abetalipoproteinemia. Annu. Rev. Nutr. 20(1): 663-697. doi:10.1146/annurev.nutr. 20.1.663.
9. Boerwinkle, E., and Chan, L. 1989. A three codon insertion/deletion polymorphism in the signal peptide region of the human apolipoprotein B (APOB) gene directly typed by the polymerase chain reaction. Nucleic Acids Res. 17(10): 4003 . doi:10.1093/nar/17.10.4003. PMID:2567503.
10. Borchardt, R.A., and Davis, R.A. 1987. Intrahepatic assembly of very low density lipoproteins. Rate of transport out of the endoplasmic reticulum determines rate of secretion. J. Biol. Chem. 262(34): 16394-16402. PMID:3680257.
11. Buhman, K.K., Accad, M., Novak, S., Choi, R.S., Wong, J.S., Hamilton, R.L., et al. 2000. Resistance to diet-induced hypercholesterolemia and gallstone formation in ACAT2-deficient mice. Nat. Med. 6(12): 1341-1347. doi:10.1038/82153. PMID:11100118.
12. Burch, W.L., and Herscovitz, H. 2000. Disulfide bonds are required for folding and secretion of apolipoprotein B regardless of its lipidation state. J. Biol. Chem. 275(21): 16267-16274. doi:10.1074/jbc.M000446200. PMID:10747912.
13. Carraway, M., Herscovitz, H., Zannis, V., and Small, D.M. 2000. Specificity of lipid incorporation is determined by sequences in the N-terminal 37 of apoB. Biochemistry, 39(32): 9737-9745. doi:10.1021/bi000791h. PMID:10933790.
14. Chandler, C.E., Wilder, D.E., Pettini, J.L., Savoy, Y.E., Petras, S.F., Chang, G., et al. 2003. CP-346086: an MTP inhibitor that lowers plasma cholesterol and triglycerides in experimental animals and in humans. J. Lipid Res. 44(10): 1887-1901. doi:10.1194/jlr.M300094-JLR200. PMID:12837854.
15. Chen, Y., Le Cahérec, F., and Chuck, S.L. 1998. Calnexin and other factors that alter translocation affect the rapid binding of ubiquitin to apoB in the Sec61 complex. J. Biol. Chem. 273(19): 11887-11894. doi:10.1074/jbc.273. 19.11887. PMID:9565615.
16. Christianson, J.C., Shaler, T.A., Tyler, R.E., and Kopito, R.R. 2008. OS-9 and GRP94 deliver mutant alpha1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat. Cell Biol. 10(3): 272-282. doi:10.1038/ncb1689. PMID:18264092.
17. Chuck, S.L., and Lingappa, V.R. 1993. Analysis of a pause transfer sequence from apolipoprotein B. J. Biol. Chem. 268(30): 22794-22801. PMID:8226789.
18. Cuchel, M., Bloedon, L.T., Szapary, P.O., Kolansky, D.M., Wolfe, M.L., Sarkis, A., et al. 2007. Inhibition of microsomal triglyceride transfer protein in familial hypercholesterolemia. N. Engl. J. Med. 356(2): 148-156. doi:10.1056/NEJMoa061189. PMID:17215532.
19. Dashti, N., Gandhi, M., Liu, X., Lin, X., and Segrest, J.P. 2002. The N-terminal 1000 residues of apolipoprotein B associate with microsomal triglyceride transfer protein to create a lipid transfer pocket required for lipoprotein assembly. Biochemistry, 41(22): 6978-6987. doi:10.1021/bi011757l. PMID:12033930.
20. Dashti, N., Manchekar, M., Liu, Y., Sun, Z., and Segrest, J.P. 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(39): 28597-28608. doi:10.1074/jbc.M700229200. PMID:17690102.
21. Davidson, N.O., and Shelness, G.S. 2000. APOLIPOPROTEIN B: mRNA editing, lipoprotein assembly, and presecretory degradation. Annu. Rev. Nutr. 20: 169-193.
22. Davis, R.A., McNeal, M.M., and Moses, R.L. 1982. Intrahepatic assembly of very low density lipoprotein. Competition by cholesterol esters for the hydrophobic core. J. Biol. Chem. 257(5): 2634-2640. PMID:7061440.
23. Day, D.A., and Tuite, M.F. 1998. Post-transcriptional gene regulatory mechanisms in eukaryotes: an overview. J. Endocrinol. 157(3): 361-371. doi:10.1677/joe.0.1570361. PMID:9691970.
24. De Lemos-Chiarandini, C., Ivessa, N.E., Black, V.H., Tsao, Y.S., Gumper, I., and Kreibich, G. 1992. A Golgi-related structure remains after the brefeldin A-induced formation of an ER-Golgi hybrid compartment. Eur. J. Cell Biol. 58(2): 187-201. PMID:1425761.
25. Du, E.Z., Kurth, J., Wang, S.L., Humiston, P., and Davis, R.A. 1994. Proteolysis-coupled secretion of the N terminus of apolipoprotein B. Characterization of a transient, translocation arrested intermediate. J. Biol. Chem. 269(39): 24169-24176. PMID:7523367.
26. Feldman, M., and van der Goot, F.G. 2009. Novel ubiquitin-dependent quality control in the endoplasmic reticulum. Trends Cell Biol. 19(8): 357-363. doi:10.1016/j.tcb.2009.05.005. PMID:19631546.
27. Finley, D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78: 477-513.
28. Fisher, E.A., Zhou, M., Mitchell, D.M., Wu, X., Omura, S., Wang, H., et al. 1997. The degradation of apolipoprotein B100 is mediated by the ubiquitin-proteasome pathway and involves heat shock protein 70. J. Biol. Chem. 272(33): 20427-20434. doi:10.1074/jbc.272.33.20427. PMID:9252351.
29. Fisher, E.A., Pan, M., Chen, X., Wu, X., Wang, H., Jamil, H., et al. 2001. The triple threat to nascent apolipoprotein B. Evidence for multiple, distinct degradative pathways. J. Biol. Chem. 276(30): 27855-27863. doi:10.1074/jbc.M008885200. PMID:11285257.
30. Fisher, E.A., Lapierre, L.R., Junkins, R.D., and McLeod, R.S. 2008. The AAA-ATPase p97 facilitates degradation of apolipoprotein B by the ubiquitin-proteasome pathway. J. Lipid Res. 49(10): 2149-2160. doi:10.1194/jlr.M800108-JLR200. PMID:18550891.
31. Fliegel, L., Burns, K., MacLennan, D.H., Reithmeier, R.A., and Michalak, M. 1989. Molecular cloning of the high affinity calcium-binding protein (calreticulin) of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 264(36): 21522-21528. PMID:2600080.
32. Gordon, D.A., Jamil, H., Sharp, D., Mullaney, D., Yao, Z., Gregg, R.E., and Wetterau, J. 1994. Secretion of apolipoprotein B-containing lipoproteins from HeLa cells is dependent on expression of the microsomal triglyceride transfer protein and is regulated by lipid availability. Proc. Natl. Acad. Sci. U.S.A. 91: 7628-7632.
33. Gusarova, V., Caplan, A.J., Brodsky, J.L., and Fisher, E.A. 2001. Apoprotein B degradation is promoted by the molecular chaperones hsp90 and hsp70. J. Biol. Chem. 276(27): 24891-24900. doi:10.1074/jbc.M100633200. PMID:11333259.
34. Gusarova, V., Brodsky, J.L., and Fisher, E.A. 2003. Apolipoprotein B100 exit from the endoplasmic reticulum (ER) is COPII-dependent, and its lipidation to very low density lipoprotein occurs post-ER. J. Biol. Chem. 278(48): 48051-48058. doi:10.1074/jbc.M306898200. PMID:12960170.
35. Helenius, A., and Aebi, M. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73: 1019-1049.
36. Herscovitz, H., Kritis, A., Talianidis, I., Zanni, E., Zannis, V., and Small, D.M. 1995. Murine mammary-derived cells secrete the N-terminal 41% of human apolipoprotein B on high density lipoprotein-sized lipoproteins containing a triacylglycerol-rich core. Proc. Natl. Acad. Sci. U.S.A. 92(3): 659-663. doi:10.1073/pnas.92.3.659. PMID:7846033.
37. Higuchi, K., Hospattankar, A.V., Law, S.W., Meglin, N., Cortright, J., and Brewer, H.B., Jr. 1988. Human apolipoprotein B (apoB) mRNA: identification of two distinct apoB mRNAs, an mRNA with the apoB-100 sequence and an apoB mRNA containing a premature in-frame translational stop codon, in both liver and intestine. Proc. Natl. Acad. Sci. U.S.A. 85(6): 1772-1776. doi:10.1073/pnas.85. 6.1772. PMID:2450346.
38. Hirano, K-I., Young, S.G., Farese, R.V., Jr., Ng, J., Sande, E., Warburton, C., et al. 1996. Targeted disruption of the mouse apobec- 1 gene abolishes apolipoprotein B mRNA editing and eliminates apolipoprotein B48. J. Biol. Chem. 271(17): 9887-9890. doi:10.1074/jbc.271.17.9887. PMID:8626621.
39. Hochstrasser, M. 1996. Ubiquitin-dependent protein degradation. Annu. Rev. Genet. 30: 405-30439.
40. Hosokawa, N., Wada, I., Hasegawa, K., Yorihuzi, T., Tremblay, L.O., Herscovics, A., and Nagata, K. 2001. A novel ER alphamannosidase-like protein accelerates ER-associated degradation. EMBO Rep. 2(5): 415-422. PMID:11375934.
41. Hosokawa, N., Wada, I., Nagasawa, K., Moriyama, T., Okawa, K., and Nagata, K. 2008. Human XTP3-B forms an endoplasmic reticulum quality control scaffold with the HRD1-SEL1L ubiquitin ligase complex and BiP. J. Biol. Chem. 283(30): 20914-20924. doi:10.1074/jbc.M709336200. PMID:18502753.
42. Hosokawa, N., Kamiya, Y., Kamiya, D., Kato, K., and Nagata, K. 2009. Human OS-9, a lectin required for glycoprotein endoplasmic reticulum-associated degradation, recognizes mannosetrimmed N-glycans. J. Biol. Chem. 284(25): 17061-17068. doi:10.1074/jbc.M809725200. PMID:19346256.
43. Huang, X.F., and Shelness, G.S. 1997. Identification of cysteine pairs within the amino-terminal 5% of apolipoprotein B essential for hepatic lipoprotein assembly and secretion. J. Biol. Chem. 272(50): 31872-31876. doi:10.1074/jbc.272.50.31872. PMID:9395534.
44. Hussain, M.M., Bakillah, A., and Jamil, H. 1997. Apolipoprotein B binding to microsomal triglyceride transfer protein decreases with increases in length and lipidation: implications in lipoprotein biosynthesis. Biochemistry, 36(42): 13060-13067. doi:10.1021/bi971395a. PMID:9335568.
45. Hussain, M.M., Bakillah, A., Nayak, N., and Shelness, G.S. 1998. Amino acids 430-570 in apolipoprotein B are critical for its binding to microsomal triglyceride transfer protein. J. Biol. Chem. 273(40): 25612-25615. doi:10.1074/jbc.273.40.25612. PMID:9748226.
46. Hwang, C., Sinskey, A.J., and Lodish, H.F. 1992. Oxidized redox state of glutathione in the endoplasmic reticulum. Science, 257(5076): 1496-1502. doi:10.1126/science.1523409. PMID:1523409.
47. Jacobs, R.L., Devlin, C., Tabas, I., and Vance, D.E. 2004. Targeted deletion of hepatic CTP:phosphocholine cytidylyltransferase alpha in mice decreases plasma high density and very low density lipoproteins. J. Biol. Chem. 279(45): 47402-47410. doi:10.1074/jbc.M404027200. PMID:15331603.
48. Jamil, H., Dickson, J.K., Jr., Chu, C.H., Lago, M.W., Rinehart, J.K., Biller, S.A., et al. 1995. Microsomal triglyceride transfer protein. Specificity of lipid binding and transport. J. Biol. Chem. 270(12): 6549-6554. PMID:7896791.
49. Jamil, H., Gordon, D.A., Eustice, D.C., Brooks, C.M., Dickson Jr., J.K., Chen, Y., et al. 1996. An inhibitor of the microsomal triglyceride transfer protein inhibits apoB secretion from HepG2 cells. Proc. Natl. Acad. Sci. U.S.A. 93:11991-11995.
50. Jiang, Z.G., Gantz, D., Bullitt, E., and McKnight, C.J. 2006. Defining lipid-interacting domains in the N-terminal region of apolipoprotein B. Biochemistry, 45(39): 11799-11808. doi:10.1021/bi060600w. PMID:17002280.
51. Johs, A., Hammel, M., Waldner, I., May, R.P., Laggner, P., and Prassl, R. 2006. Modular structure of solubilized human apolipoprotein B-100. Low resolution model revealed by small angle neutron scattering. J. Biol. Chem. 281(28): 19732-19739. doi:10.1074/jbc.M601688200. PMID:16704977.
52. Joy, T.R., and Hegele, R.A. 2008. Microsomal triglyceride transfer protein inhibition-friend or foe? Nat. Clin. Pract. Cardiovasc. Med. 5(8): 506-508. doi:10.1038/ncpcardio1251. PMID:18506153.
53. Joyce, C.W., Shelness, G.S., Davis, M.A., Lee, R.G., Skinner, K., Anderson, R.A., and Rudel, L.L. 2000. ACAT1 and ACAT2 membrane topology segregates a serine residue essential for activity to opposite sides of the endoplasmic reticulum membrane. Mol. Biol. Cell, 11(11): 3675-3687. PMID:11071899.
54. Kane, J.P. 1983. Apolipoprotein B: structural and metabolic heterogeneity. Annu. Rev. Physiol. 45: 637-45650.
55. Kane, J.P., Hardman, D.A., and Paulus, H.E. 1980. Heterogeneity of apolipoprotein B: isolation of a new species from human chylomicrons. Proc. Natl. Acad. Sci. U.S.A. 77(5): 2465-2469. doi:10.1073/pnas.77.5.2465. PMID:6930644.
56. Kennedy, E.P., and Weiss, S.B. 1956. The function of cytidine coenzymes in the biosynthesis of phospholipides. J. Biol. Chem. 222(1): 193-214. PMID:13366993.
57. Khan, B.V., Fungwe, T.V., Wilcox, H.G., and Heimberg, M. 1990. Cholesterol is required for the secretion of the very-low-density lipoprotein: in vivo studies. Biochim. Biophys. Acta, 1044(3): 297-304. PMID:2364096.
58. Kozak, M. 1991. Structural features in eukaryotic mRNAs that modulate the initiation of translation. J. Biol. Chem. 266(30): 19867-19870. PMID:1939050.
59. Kulinski, A., and Vance, J.E. 2007. Lipid homeostasis and lipoprotein secretion in Niemann-Pick C1-deficient hepatocytes. J. Biol. Chem. 282(3): 1627-1637. doi:10.1074/jbc.M610001200. PMID:17107950.
60. Kulinski, A., Rustaeus, S., and Vance, J.E. 2002. Microsomal triacylglycerol transfer protein is required for lumenal accretion of triacylglycerol not associated with ApoB, as well as for ApoB lipidation. J. Biol. Chem. 277(35): 31516-31525. doi:10.1074/jbc.M202015200. PMID:12072432.
61. Lee, A.H., Scapa, E.F., Cohen, D.E., and Glimcher, L.H. 2008. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science, 320(5882): 1492-1496. doi:10.1126/science.1158042. PMID:18556558.
62. Liang, J., Wu, X., Jiang, H., Zhou, M., Yang, H., Angkeow, P., et al. 1998. Translocation efficiency, susceptibility to proteasomal degradation, and lipid responsiveness of apolipoprotein B are determined by the presence of beta sheet domains. J. Biol. Chem. 273(52): 35216-35221. doi:10.1074/jbc.273.52. 35216. PMID:9857060.
63. Liang, S., Wu, X., Fisher, E.A., and Ginsberg, H.N. 2000. The amino-terminal domain of apolipoprotein B does not undergo retrograde translocation from the endoplasmic reticulum to the cytosol. Proteasomal degradation of nascent apolipoprotein B begins at the carboxyl terminus of the protein, while apolipoprotein B is still in its original translocon. J. Biol. Chem. 275(41): 32003-32010. doi:10.1074/jbc.M004646200. PMID:10922368.
64. Liang, J.S., Kim, T., Fang, S., Yamaguchi, J., Weissman, A.M., Fisher, E.A., and Ginsberg, H.N. 2003. Overexpression of the tumor autocrine motility factor receptor Gp78, a ubiquitin protein ligase, results in increased ubiquitinylation and decreased secretion of apolipoprotein B100 in HepG2 cells. J. Biol. Chem. 278(26): 23984-23988. doi:10.1074/jbc.M302683200. PMID:12670940.
65. Liao, W., and Chan, L. 2001. Tunicamycin induces ubiquitination and degradation of apolipoprotein B in HepG2 cells. Biochem. J. 353(Pt 3): 493-501. doi:10.1042/0264-6021:3530493. PMID:11171045.
66. Liao, W., Yeung, S.C., and Chan, L. 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(42): 27225-27230. doi:10.1074/jbc.273. 42.27225. PMID:9765244.
67. Lilley, B.N., and Ploegh, H.L. 2005. Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. U.S.A. 102(40): 14296-14301. doi:10.1073/pnas.0505014102. PMID:16186509.
68. Linnik, K.M., and Herscovitz, H. 1998. Multiple molecular chaperones interact with apolipoprotein B during its maturation. The network of endoplasmic reticulum-resident chaperones (ERp72, GRP94, calreticulin, and BiP) interacts with apolipoprotein b regardless of its lipidation state. J. Biol. Chem. 273(33): 21368-21373. doi:10.1074/jbc.273.33.21368. PMID:9694898.
69. Linton, M.F., Farese, R.V., Jr., and Young, S.G. 1993. Familial hypobetalipoproteinemia. J. Lipid Res. 34(4): 521-541. PMID:8496659.
70. Ludwig, E.H., Blackhart, B.D., Pierotti, V.R., Caiati, L., Fortier, C., Knott, T., et al. 1987. DNA sequence of the human apolipoprotein B gene. DNA, 6(4): 363-372. doi:10.1089/dna.1987.6.363. PMID:3652907.
71. Luz, J.M., and Lennarz, W.J. 1996. Protein disulfide isomerase: a multifunctional protein of the endoplasmic reticulum. EXS, 77: 97-117.
72. Macri, J., and Adeli, K. 1997. Conformational changes in apolipoprotein B modulate intracellular assembly and degradation of ApoB-containing lipoprotein particles in HepG2 cells. Arterioscler. Thromb. Vasc. Biol. 17(11): 2982-2994. PMID:9409285.
73. Manchekar, M., Richardson, P.E., Forte, T.M., Datta, G., Segrest, J.P., and Dashti, N. 2004. Apolipoprotein B-containing lipoprotein particle assembly: lipid capacity of the nascent lipoprotein particle. J. Biol. Chem. 279(38): 39757-39766. doi:10.1074/jbc.M406302200. PMID:15254032.
74. Mann, C.J., Anderson, T.A., Read, J., Chester, S.A., Harrison, G.B., Köchl, S., et al. 1999. The structure of vitellogenin provides a molecular model for the assembly and secretion of atherogenic lipoproteins. J. Mol. Biol. 285(1): 391-408. doi:10.1006/jmbi.1998.2298. PMID:9878414.
75. McLeod, R.S., Zhao, Y., Selby, S.L., Westerlund, J., and Yao, Z. 1994. Carboxyl-terminal truncation impairs lipid recruitment by apolipoprotein B100 but does not affect secretion of the truncated apolipoprotein B-containing lipoproteins. J. Biol. Chem. 269(4): 2852-2862. PMID:8300620.
76. McLeod, R.S., Wang, Y., Wang, S., Rusiñol, A., Links, P., and Yao, Z. 1996. Apolipoprotein B sequence requirements for hepatic very low density lipoprotein assembly. Evidence that hydrophobic sequences within apolipoprotein B48 mediate lipid recruitment. J. Biol. Chem. 271(31): 18445-18455. doi:10.1074/jbc.271.31.18445. PMID:8702489.
77. Michalak, M., Groenendyk, J., Szabo, E., Gold, L.I., and Opas, M. 2009. Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem. J. 417(3): 651-666. doi:10.1042/BJ20081847. PMID:19133842.
78. Mitchell, D.M., Zhou, M., Pariyarath, R., Wang, H., Aitchison, J.D., Ginsberg, H.N., and Fisher, E.A. 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. U.S.A. 95(25): 14733-14738. doi:10.1073/pnas.95.25.14733. PMID:9843958.
79. Molinari, M., Calanca, V., Galli, C., Lucca, P., and Paganetti, P. 2003. Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science, 299(5611): 1397-1400. doi:10.1126/science.1079474. PMID:12610306.
80. Noga, A.A., and Vance, D.E. 2003. A gender-specific role for phosphatidylethanolamine N-methyltransferase-derived phosphatidylcholine in the regulation of plasma high density and very low density lipoproteins in mice. J. Biol. Chem. 278(24): 21851-21859. doi:10.1074/jbc.M301982200. PMID:12668679.
81. Ohsaki, Y., Cheng, J., Fujita, A., Tokumoto, T., and Fujimoto, T. 2006. Cytoplasmic lipid droplets are sites of convergence of proteasomal and autophagic degradation of apolipoprotein B. Mol. Biol. Cell, 17(6): 2674-2683. doi:10.1091/mbc.E05-07-0659. PMID:16597703.
82. Ohsaki, Y., Cheng, J., Suzuki, M., Fujita, A., and Fujimoto, T. 2008. Lipid droplets are arrested in the ER membrane by tight binding of lipidated apolipoprotein B-100. J. Cell Sci. 121: 2415-2422. doi:10.1242/jcs.025452. PMID:18577578.
83. Pan, M., Liang, J., Fisher, E.A., and Ginsberg, H.N. 2000. Inhibition of translocation of nascent apolipoprotein B across the endoplasmic reticulum membrane is associated with selective inhibition of the synthesis of apolipoprotein B. J. Biol. Chem. 275(35): 27399-27405. PMID:10846173.
84. Pan, M., Liang Js, J.S., Fisher, E.A., and Ginsberg, H.N. 2002. The late addition of core lipids to nascent apolipoprotein B100, resulting in the assembly and secretion of triglyceride-rich lipoproteins, is independent of both microsomal triglyceride transfer protein activity and new triglyceride synthesis. J. Biol. Chem. 277(6): 4413-4421. doi:10.1074/jbc.M107460200. PMID:11704664.
85. Pan, M., Cederbaum, A.I., Zhang, Y.L., Ginsberg, H.N., Williams, K.J., and Fisher, E.A. 2004. Lipid peroxidation and oxidant stress regulate hepatic apolipoprotein B degradation and VLDL production. J. Clin. Invest. 113(9): 1277-1287. PMID:15124019.
86. Pan, M., Maitin, V., Parathath, S., Andreo, U., Lin, S.X., St Germain, C., et al. 2008. Presecretory oxidation, aggregation, and autophagic destruction of apoprotein-B: a pathway for late-stage quality control. Proc. Natl. Acad. Sci. U.S.A. 105(15): 5862-5867. doi:10.1073/pnas.0707460104. PMID:18391222.
87. Pariyarath, R., Wang, H., Aitchison, J.D., Ginsberg, H.N., Welch, W.J., Johnson, A.E., and Fisher, E.A. 2001. Co-translational interactions of apoprotein B with the ribosome and translocon during lipoprotein assembly or targeting to the proteasome. J. Biol. Chem. 276(1): 541-550. doi:10.1074/jbc.M007944200. PMID:11022045.
88. Park, S., Isaacson, R., Kim, H.T., Silver, P.A., and Wagner, G. 2005. Ufd1 exhibits the AAA-ATPase fold with two distinct ubiquitin interaction sites. Structure, 13(7): 995-1005. doi:10.1016/j.str.2005.04.013. PMID:16004872.
89. Pease, R.J., Leiper, J.M., Harrison, G.B., and Scott, J. 1995. Studies on the translocation of the amino terminus of apolipoprotein B into the endoplasmic reticulum. J. Biol. Chem. 270(13): 7261-7271. doi:10.1074/jbc.270. 13.7261. PMID:7706266.
90. Pollard, M.G., Travers, K.J., and Weissman, J.S. 1998. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell, 1(2): 171-182. doi:10.1016/S1097-2765(00) 80018-0. PMID:9659914.
91. Pontrelli, L., Sidiropoulos, K.G., and Adeli, K. 2004. Translational control of apolipoprotein B mRNA: regulation via cis elements in the 5' and 3' untranslated regions. Biochemistry, 43(21): 6734-6744. doi:10.1021/bi049887s. PMID:15157107.
92. Powell, L.M., Wallis, S.C., Pease, R.J., Edwards, Y.H., Knott, T.J., and Scott, J. 1987. A novel form of tissue-specific RNA processing produces apolipoprotein-B48 in intestine. Cell, 50(6): 831-840. doi:10.1016/0092-8674(87) 90510-1. PMID:3621347.
93. Qiu, W., Kohen-Avramoglu, R., Mhapsekar, S., Tsai, J., Austin, R.C., and Adeli, K. 2005. Glucosamine-induced endoplasmic reticulum stress promotes ApoB100 degradation: evidence for Grp78-mediated targeting to proteasomal degradation. Arterioscler. Thromb. Vasc. Biol. 25(3): 571-577. doi:10.1161/01.ATV.0000154142.61859.94. PMID:15618547.
94. Qiu, W., Avramoglu, R.K., Rutledge, A.C., Tsai, J., and Adeli, K. 2006. Mechanisms of glucosamine-induced suppression of the hepatic assembly and secretion of apolipoprotein B-100-containing lipoproteins. J. Lipid Res. 47(8): 1749-1761. doi:10.1194/jlr.M500363-JLR200. PMID:16672736.
95. Qiu, W., Su, Q., Rutledge, A.C., Zhang, J., and Adeli, K. 2009. Glucosamine-induced ER stress attenuates apolipoprotein B100 synthesis via PERK signaling. J. Lipid Res. 50: 1814-1823.
96. Raabe, M., Flynn, L.M., Zlot, C.H., Wong, J.S., Véniant, M.M., Hamilton, R.L., and Young, S.G. 1998. Knockout of the abetalipoproteinemia gene in mice: reduced lipoprotein secretion in heterozygotes and embryonic lethality in homozygotes. Proc. Natl. Acad. Sci. U.S.A. 95(15): 8686-8691. doi:10.1073/pnas.95.15.8686. PMID:9671739.
97. Rava, P., Ojakian, G.K., Shelness, G.S., and Hussain, M.M. 2006. Phospholipid transfer activity of microsomal triacylglycerol transfer protein is sufficient for the assembly and secretion of apolipoprotein B lipoproteins. J. Biol. Chem. 281(16): 11019-11027. doi:10.1074/jbc.M512823200. PMID:16478722.
98. Ron, D., and Walter, P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8(7): 519-529. doi:10.1038/nrm2199. PMID:17565364.
99. Ruddock, L.W., and Molinari, M. 2006. N-glycan processing in ER quality control. J. Cell Sci. 119: 4373-4380. doi:10.1242/jcs.03225. PMID:17074831.
100. Rustaeus, S., Lindberg, K., Borén, J., and Olofsson, S.O. 1995. Brefeldin A reversibly inhibits the assembly of apoB containing lipoproteins in McA-RH7777 cells. J. Biol. Chem. 270(48): 28879-28886. doi:10.1074/jbc.270.48. 28879. PMID:7499415.
101. Rutledge, A.C., Qiu, W., Zhang, R., Kohen-Avramoglu, R., Nemat-Gorgani, N., and Adeli, K. 2009. Mechanisms targeting apolipoprotein B100 to proteasomal degradation: evidence that degradation is initiated by BiP binding at the N terminus and the formation of a p97 complex at the C terminus. Arterioscler. Thromb. Vasc. Biol. 29(4): 579-585. doi:10.1161/ATVBAHA.108.181859. PMID:19164805.
102. Sahoo, D., Trischuk, T.C., Chan, T., Drover, V.A., Ho, S., Chimini, G., et al. 2004. ABCA1-dependent lipid efflux to apolipoprotein A-I mediates HDL particle formation and decreases VLDL secretion from murine hepatocytes. J. Lipid Res. 45(6): 1122-1131. doi:10.1194/jlr.M300529-JLR200. PMID:14993246.
103. Sallach, S.M., and Adeli, K. 1995. Intracellular degradation of apolipoprotein B generates an N-terminal 70 kDa fragment in the endoplasmic reticulum. Biochim. Biophys. Acta, 1265(1): 29-32. doi:10.1016/0167-4889(95) 00239-O. PMID:7857981.
104. Samaha, F.F., McKenney, J., Bloedon, L.T., Sasiela, W.J., and Rader, D.J. 2008. Inhibition of microsomal triglyceride transfer protein alone or with ezetimibe in patients with moderate hypercholesterolemia. Nat. Clin. Pract. Cardiovasc. Med. 5(8): 497-505. doi:10.1038/ncpcardio1250. PMID:18506154.
105. Schonfeld, G., Lin, X., and Yue, P. 2005. Familial hypobetalipoproteinemia: genetics and metabolism. Cell. Mol. Life Sci. 62(12): 1372-1378. doi:10.1007/s00018-005-4473-0. PMID:15818469.
106. Schroder, M., and Kaufman, R.J. 2005. The mammalian unfolded protein response. Annu. Rev. Biochem. 74: 739-789.
107. Schulze, A., Standera, S., Buerger, E., Kikkert, M., van Voorden, S., Wiertz, E., et al. 2005. The ubiquitin-domain protein HERP forms a complex with components of the endoplasmic reticulum associated degradation pathway. J. Mol. Biol. 354(5): 1021-1027. doi:10.1016/j.jmb.2005.10.020. PMID:16289116.
108. Scott, J. 1989a. Messenger RNA editing and modification. Curr. Opin. Cell Biol. 1(6): 1141-1147. doi:10.1016/S0955-0674(89)80064-X. PMID:2517580.
109. Scott, J. 1989b. The molecular and cell biology of apolipoprotein-B. Mol. Biol. Med. 6(1): 65-80. PMID:2666820.
110. Segrest, J.P., Garber, D.W., Brouillette, C.G., Harvey, S.C., and Anantharamaiah, G.M. 1994. The amphipathic alpha helix: a multifunctional structural motif in plasma apolipoproteins. Adv. Protein Chem. 45: 303-369.
111. Segrest, J.P., Jones, M.K., and Dashti, N. 1999. N-terminal domain of apolipoprotein B has structural homology to lipovitellin and microsomal triglyceride transfer protein: a "lipid pocket" model for self-assembly of apob-containing lipoprotein particles. J. Lipid Res. 40(8): 1401-1416. PMID:10428976.
112. Segrest, J.P., Jones, M.K., De Loof, H., and Dashti, N. 2001. Structure of apolipoprotein B-100 in low density lipoproteins. J. Lipid Res. 42(9): 1346-1367. PMID:11518754.
113. Sellers, J.A., Hou, L., Schoenberg, D.R., Batistuzzo de Medeiros, S.R., Wahli, W., and Shelness, G.S. 2005. Microsomal triglyceride transfer protein promotes the secretion of Xenopus laevis vitellogenin A1. J. Biol. Chem. 280(14): 13902-13905. doi:10.1074/jbc.M500769200. PMID:15701598.
114. Shelness, G.S., and Ledford, A.S. 2005. Evolution and mechanism of apolipoprotein B-containing lipoprotein assembly. Curr. Opin. Lipidol. 16(3): 325-332. doi:10.1097/01.mol.0000169353.12772.eb. PMID:15891394.
115. Shelness, G.S., and Thornburg, J.T. 1996. Role of intramolecular disulfide bond formation in the assembly and secretion of apolipoprotein B-100-containing lipoproteins. J. Lipid Res. 37(2): 408-419. PMID:9026538.
116. Shelness, G.S., Hou, L., Ledford, A.S., Parks, J.S., and Weinberg, R.B. 2003. Identification of the lipoprotein initiating domain of apolipoprotein B. J. Biol. Chem. 278(45): 44702-44707. doi:10.1074/jbc.M307562200. PMID:12941937.
117. Shoulders, C.C., Narcisi, T.M., Read, J., Chester, A., Brett, D.J., Scott, J., et al. 1994. The abetalipoproteinemia gene is a member of the vitellogenin family and encodes an alpha-helical domain. Nat. Struct. Biol. 1(5): 285-286. doi:10.1038/nsb0594-285. PMID:7664034.
118. Sidiropoulos, K.G., Pontrelli, L., and Adeli, K. 2005. Insulinmediated suppression of apolipoprotein B mRNA translation requires the 5' UTR and is characterized by decreased binding of an insulin-sensitive 110-kDa 5' UTR RNA-binding protein. Biochemistry, 44(37): 12572-12581. doi:10.1021/bi050368e. PMID:16156669.
119. Sidiropoulos, K.G., Meshkani, R., Avramoglu-Kohen, R., and Adeli, K. 2007. Insulin inhibition of apolipoprotein B mRNA translation is mediated via the PI-3 kinase/mTOR signaling cascade but does not involve internal ribosomal entry site (IRES) initiation. Arch. Biochem. Biophys. 465(2): 380-388. doi:10.1016/j.abb.2007.06.029. PMID:17698027.
120. Stillemark, P., Borén, J., Andersson, M., Larsson, T., Rustaeus, S., Karlsson, K.A., and Olofsson, S.O. 2000. The assembly and secretion of apolipoprotein B-48-containing very low density lipoproteins in McA-RH7777 cells. J. Biol. Chem. 275(14): 10506-10513. doi:10.1074/jbc.275.14.10506. PMID:10744742.
121. Su, Q., Tsai, J., Xu, E., Qiu, W., Bereczki, E., Santha, M., and Adeli, K. 2009. Apolipoprotein B100 acts as a molecular link between lipid-induced endoplasmic reticulum stress and hepatic insulin resistance. Hepatology, 50(1): 77-84. doi:10.1002/hep.22960. PMID:19434737.
122. Tamura, T., Cormier, J.H., and Hebert, D.N. 2008. Sweet bays of ERAD. Trends Biochem. Sci. 33(7): 298-300. doi:10.1016/j.tibs.2008.04.013. PMID:18538572.
123. Tatu, U., and Helenius, A. 1999. Interaction of newly synthesized apolipoprotein B with calnexin and calreticulin requires glucose trimming in the endoplasmic reticulum. Biosci. Rep. 19(3): 189-196. doi:10.1023/A: 1020225803282. PMID:10513896.
124. Thrower, J.S., Hoffman, L., Rechsteiner, M., and Pickart, C.M. 2000. Recognition of the polyubiquitin proteolytic signal. EMBO J. 19(1): 94-102. doi:10.1093/emboj/19.1.94. PMID:10619848.
125. Townley, A.K., Feng, Y., Schmidt, K., Carter, D.A., Porter, R., Verkade, P., and Stephens, D.J. 2008. Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J. Cell Sci. 121: 3025-3034. doi:10.1242/jcs.031070. PMID:18713835.
126. Tran, K., Borén, J., Macri, J., Wang, Y., McLeod, R., Avramoglu, R.K., et al. 1998. Functional analysis of disulfide linkages clustered within the amino terminus of human apolipoprotein B. J. Biol. Chem. 273(13): 7244-7251. doi:10.1074/jbc.273.13.7244. PMID:9516417.
127. Tran, K., Thorne-Tjomsland, G., DeLong, C.J., Cui, Z., Shan, J., Burton, L., et al. 2002. Intracellular assembly of very low density lipoproteins containing apolipoprotein B100 in rat hepatoma McA-RH7777 cells. J. Biol. Chem. 277(34): 31187-31200. doi:10.1074/jbc.M200249200. PMID:12065576.
128. Tsai, J., Qiu, W., Kohen-Avramoglu, R., and Adeli, K. 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(1): 211-218. doi:10.1161/01.ATV.0000249861.80471.96. PMID:17038630.
129. Vance, J.E., and Adeli, K. 2008. Assembly and secretion of triacylglycerol-rich lipoproteins. In Biochemistry of lipids, lipoproteins, and membranes.5th edition. Edited by D.E. Vance and J.E. Vance. Elsevier, Amsterdam, The Netherlands. pp. 507-531.
130. Vance, D.E., and Ridgway, N.D. 1988. The methylation of phosphatidylethanolamine. Prog. Lipid Res. 27(1): 61-79. doi:10.1016/0163- 7827(88)90005-7. PMID:3057511.
131. Vukmirica, J., Nishimaki-Mogami, T., Tran, K., Shan, J., McLeod, R.S., Yuan, J., and Yao, Z. 2002. The N-linked oligosaccharides at the amino terminus
132. Wahli, W., Dawid, I.B., Ryffel, G.U., and Weber, R. 1981. Vitellogenesis and the vitellogenin gene family. Science, 212(4492): 298-304. doi:10.1126/science.7209528. PMID:7209528.
133. Wang, S., McLeod, R.S., Gordon, D.A., and Yao, Z. 1996. The microsomal triglyceride transfer protein facilitates assembly and secretion of apolipoprotein B-containing lipoproteins and decreases cotranslational degradation of apolipoprotein B in transfected COS-7 cells. J. Biol. Chem. 271(24): 14124-14133. doi:10.1074/jbc.271.24.14124. PMID:8662886.
134. Wang, L., Fast, D.G., and Attie, A.D. 1997. The enzymatic and non-enzymatic roles of protein-disulfide isomerase in apolipoprotein B secretion. J. Biol. Chem. 272: 27644-27651.
135. Wang, L., Martin, D.D., Genter, E., Wang, J., McLeod, R.S., and Small, D.M. 2009. Surface study of apoB1694-1880, a sequence that can anchor apoB to lipoproteins and make it nonexchangeable. J. Lipid Res. 50(7): 1340-1352. doi:10.1194/jlr.M900040-JLR200. PMID:19251580.
136. Wedekind, J.E., Dance, G.S., Sowden, M.P., and Smith, H.C. 2003. Messenger RNA editing in mammals: new members of the APOBEC family seeking roles in the family business. Trends Genet. 19(4): 207-216. doi:10.1016/S0168- 9525(03)00054-4. PMID:12683974.
137. Wetterau, J.R., Aggerbeck, L.P., Laplaud, P.M., and McLean, L.R. 1991. Structural properties of the microsomal triglyceride-transfer protein complex. Biochemistry, 30: 4406-4412.
138. Whitfield, A.J., Barrett, P.H., van Bockxmeer, F.M., and Burnett, J.R. 2004. Lipid disorders and mutations in the APOB gene. Clin. Chem. 50(10): 1725-1732. doi:10.1373/clinchem.2004.038026. PMID:15308601.
139. Xu, P., Duong, D.M., Seyfried, N.T., Cheng, D., Xie, Y., Robert, J., et al. 2009. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell, 137(1): 133-145. doi:10.1016/j.cell.2009.01.041. PMID:19345192.
140. Yamaguchi, J., Conlon, D.M., Liang, J.J., Fisher, E.A., and Ginsberg, H.N. 2006. Translocation efficiency of apolipoprotein B is determined by the presence of beta-sheet domains, not pause transfer sequences. J. Biol. Chem. 281(37): 27063-27071. doi:10.1074/jbc.M606809200. PMID:16854991.
141. Yan, A.T., Yan, R.T., Tan, M., Hackam, D.G., Leblanc, K.L., Kertland, H., et al.; Vascular Protection (VP) and Guidelines Oriented Approach to Lipid Lowering (GOALL) Registries Investigators. 2006. Contemporary management of dyslipidemia in high-risk patients: targets still not met. Am. J. Med. 119(8): 676-683. doi:10.1016/j.amjmed.2005.11.015. PMID:16887414.
142. Yang, C.Y., Lee, F.S., Chan, L., Sparrow, D.A., Sparrow, J.T., and Gotto, A.M., Jr. 1986. Determination of the molecular mass of apolipoprotein B-100. A chemical approach. Biochem. J. 239(3): 777-780. PMID:3827828.
143. Yang, C.Y., Kim, T.W., Weng, S.A., Lee, B.R., Yang, M.L., and Gotto, A.M., Jr. 1990. Isolation and characterization of sulfhydryl and disulfide peptides of human apolipoprotein B-100. Proc. Natl. Acad. Sci. U.S.A. 87(14): 5523-5527. doi:10.1073/pnas.87.14.5523. PMID:2115173.
144. Ye, Y., Meyer, H.H., and Rapoport, T.A. 2003. Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J. Cell Biol. 162(1): 71-84. doi:10.1083/jcb.200302169. PMID:12847084.
145. Ye, Y., Shibata, Y., Kikkert, M., van Voorden, S., Wiertz, E., and Rapoport, T.A. 2005. Inaugural Article: Recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. U.S.A. 102(40): 14132-14138. doi:10.1073/pnas.0505006102. PMID:16186510.
146. Yeung, S.J., Chen, S.H., and Chan, L. 1996. Ubiquitin-proteasome pathway mediates intracellular degradation of apolipoprotein B. Biochemistry, 35(43): 13843-13848. doi:10.1021/bi9618777. PMID:8901527.
147. Zhang, J., and Herscovitz, H. 2003. Nascent lipidated apolipoprotein B is transported to the Golgi as an incompletely folded intermediate as probed by its assocation with network of endoplasmic reticulum molecular chaperones, GRP94, ERp72, BiP, calreticulin, and cyclophilin B. J. Biol. Chem. 278: 7459-7468.
148. Zhang, K., and Kaufman, R.J. 2008. From endoplasmic-reticulum stress to the inflammatory response. Nature, 454(7203): 455-462. doi:10.1038/nature07203. PMID:18650916.
149. Zhang, X., Shaw, A., Bates, P.A., Newman, R.H., Gowen, B., Orlova, E., et al. 2000. Structure of the AAA ATPase p97. Mol. Cell, 6(6): 1473-1484. doi:10.1016/S1097-2765(00)00143-X. PMID:11163219.
150. Zhou, M., Wu, X., Huang, L-S., and Ginsberg, H.N. 1995. Apoprotein B100, an inefficiently translocated secretory protein, is bound to the cytosolic chaperone, heat shock protein 70. J. Biol. Chem. 270(42): 25220-25224. doi:10.1074/jbc.270.42.25220. PMID:7559659.