Glucosamine-induced endoplasmic reticulum stress attenuates apolipoprotein B100 synthesis via PERK signaling

Journal of Lipid Research

Volumn 50, Issue 9, 2009, Pages 1814-1823

  Qiu, Wei ^a   Su, Qiaozhu ^a   Rutledge, Angela C ^a   Zhang, Jing ^a   Adeli, Khosrow ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Degradation; Glucose regulated protein 78; subunit of eukaryotic initiation factor 2

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; APOLIPOPROTEIN B; APOLIPOPROTEIN B100; APOLIPOPROTEIN B15; CELL ENZYME; DOUBLE STRANDED RNA; DOUBLE STRANDED RNA ACTIVATED PROTEIN KINASE LIKE ENDOPLASMIC RETICULUM KINASE; GLUCOSAMINE; INITIATION FACTOR 2ALPHA; MESSENGER RNA; MUTANT PROTEIN; PROTEASOME INHIBITOR; PROTEIN IRE1; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRAIN COS7; CELL STRESS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN SYNTHESIS; WILD TYPE;

EID: 70350365259     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800343-JLR200     Document Type: Article

References (36)

1. 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.
2. 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.
3. Fisher, E. A., M. Zhou, D. M. Mitchell, X. Wu, S. Omura, H. Wang, A. L. Goldberg, and H. N. Ginsberg. 1997. The degradation of apolipoprotein B100 is mediated by the ubiquitin-proteasome pathway and involves heat shock protein 70. J. Biol. Chem. 272: 20427-20434.
4. Adeli, K. 1994. Regulated intracellular degradation of apolipoprotein B in semipermeable HepG2 cells. J. Biol. Chem. 269: 9166-9175.
5. Cavallo, D., D. Rudy, A. Mohammadi, J. Macri, and K. Adeli. 1999. Studies on degradative mechanisms mediating post-translational fragmentation of apolipoprotein B and the generation of the 70-kDa fragment. J. Biol. Chem. 274: 23135-23143.
6. Qiu, W., R. Kohen-Avramoglu, F. Rashid-Kolvear, C. S. Au, T. M. Chong, G. F. Lewis, D. K. Trinh, R. C. Austin, R. Urade, and K. Adeli. 2004. Overexpression of the endoplasmic reticulum 60 protein ER-60 downregulates apoB100 secretion by inducing its intracellular degradation via a nonproteasomal pathway: evidence for an ER-60-mediated and pCMB-sensitive intracellular degradative pathway. Biochemistry. 43: 4819-4831.
7. 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.
8. Moberly, J. B., T. G. Cole, D. H. Alpers, and G. Schonfeld. 1990. Oleic acid stimulation of apolipoprotein B secretion from HepG2 and Caco-2 cells occurs post-transcriptionally. Biochim. Biophys. Acta. 1042: 70-80.
9. Sato, R., T. Imanaka, A. Takatsuki, and T. Takano. 1990. Degradation of newly synthesized apolipoprotein B-100 in a pre-Golgi compartment. J. Biol. Chem. 265: 11880-11884.
10. Cartwright, I. J., and J. A. Higgins. 1996. Intracellular degradation in the regulation of secretion of apolipoprotein B-100 by rabbit hepatocytes. Biochem. J. 314: 977-984.
11. Wang, H., X. Chen, and E. A. Fisher. 1993. N-3 fatty acids stimulate intracellular degradation of apoprotein B in rat hepatocytes. J. Clin. Invest. 91: 1380-1389.
12. Taghibiglou, C., D. Rudy, S. C. Van Iderstine, A. Aiton, D. Cavallo, R. Cheung, and K. Adeli. 2000. Intracellular mechanisms regulating apoB-containing lipoprotein assembly and secretion in primary hamster hepatocytes. J. Lipid Res. 41: 499-513.
13. Yeung, S. J., S. H. Chen, and L. Chan. 1996. Ubiquitin-proteasome pathway mediates intracellular degradation of apolipoprotein B. Biochemistry. 35: 13843-13848.
14. Zhou, M., E. A. Fisher, and H. N. Ginsberg. 1998. Regulated Cotranslational ubiquitination of apolipoprotein B100. A new paradigm for proteasomal degradation of a secretory protein. J. Biol. Chem. 273: 24649-24653.
15. 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.
16. Gordon, D. A., H. Jamil, R. E. Gregg, S. O. Olofsson, and J. Boren. 1996. Inhibition of the microsomal triglyceride transfer protein blocks the first step of apolipoprotein B lipoprotein assembly but not the addition of bulk core lipids in the second step. J. Biol. Chem. 271: 33047-33053.
17. Chen, Y., F. Le Caherec, and S. L. Chuck. 1998. Calnexin and other factors that alter translocation affect the rapid binding of ubiquitin to apoB in the Sec61 complex. J. Biol. Chem. 273: 11887-11894.
18. Zhang, J., and H. Herscovitz. 2003. Nascent lipidated apolipoprotein B is transported to the Golgi as an incompletely folded intermediate as probed by its association with network of endoplasmic reticulum molecular chaperones, GRP94, ERp72, BiP, calreticulin, and cyclophilin B. J. Biol. Chem. 278: 7459-7468.
19. Yoshida, H. 2007. ER stress and diseases. FEBS J. 274: 630-658.
20. 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.
21. Ota, T., C. Gayet, and H. N. Ginsberg. 2008. Inhibition of apolipoprotein B100 secretion by lipid-induced hepatic endoplasmic reticulum stress in rodents. J. Clin. Invest. 118: 316-332.
22. Qiu, W., R. Kohen-Avramoglu, S. Mhapsekar, J. Tsai, R. C. Austin, and K. Adeli. 2005. Glucosamine-induced endoplasmic reticulum stress promotes ApoB100 degradation: evidence for Grp78-mediated targeting to proteasomal degradation. Arterioscler. Thromb. Vasc. Biol. 25: 571-577.
23. Qiu, W., R. K. Avramoglu, A. C. Rutledge, J. Tsai, and K. Adeli. 2006. Mechanisms of glucosamine-induced suppression of the hepatic assembly and secretion of apolipoprotein B-100-containing lipoproteins. J. Lipid Res. 47: 1749-1761.
24. Qiu, W., R. K. Avramoglu, N. Dube, T. M. Chong, M. Naples, C. Au, K. G. Sidiropoulos, G. F. Lewis, J. S. Cohn, M. L. Tremblay, et al. 2004. Hepatic PTP-1B expression regulates the assembly and secretion of apolipoprotein B-containing lipoproteins: evidence from protein tyrosine phosphatase-1B overexpression, knockout, and RNAi studies. Diabetes. 53: 3057-3066.
25. Su, Q., S. Wang, H. Q. Gao, S. Kazemi, H. P. Harding, D. Ron, and A. E. Koromilas. 2008. Modulation of the eukaryotic initiation factor 2 alpha-subunit kinase PERK by tyrosine phosphorylation. J. Biol. Chem. 283: 469-475.
26. Qiu, W., C. Taghibiglou, R. K. Avramoglu, S. C. Van Iderstine, M. Naples, H. Ashrafpour, S. Mhapsekar, R. Sato, and K. Adeli. 2005. Oleate-mediated stimulation of microsomal triglyceride transfer protein (MTP) gene promoter: implications for hepatic MTP overexpression in insulin resistance. Biochemistry. 44: 3041-3049.
27. Cavallo, D., R. S. McLeod, D. Rudy, A. Aiton, Z. Yao, and K. Adeli. 1998. Intracellular translocation and stability of apolipoprotein B are inversely proportional to the length of the nascent polypeptide. J. Biol. Chem. 273: 33397-33405.
28. Vukmirica, J., T. Nishimaki-Mogami, K. Tran, J. Shan, R. S. McLeod, J. Yuan, and Z. Yao. 2002. The N-linked oligosaccharides at the amino terminus of human apoB are important for the assembly and secretion of VLDL. J. Lipid Res. 43: 1496-1507.
29. Hanson, S. R., E. K. Culyba, T-L. Hsu, C-H. Wong, J. W. Kelly, and E. T. Powers. 2009. The core trisaccharide of an N-linked glycoprotein intrinsically accelerates folding and enhances stability. Proc. Natl. Acad. Sci. USA. 106: 3131-3136.
30. Wernette-Hammond, M. E., S. J. Lauer, A. Corsini, D. Walker, J. M. Taylor, and S. C. Rall, Jr. 1989. Glycosylation of human apolipoprotein E. The carbohydrate attachment site is threonine 194. J. Biol. Chem. 264: 9094-9101.
31. Pan, M., J. 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 apolipoprotein B. J. Biol. Chem. 275: 27399-27405.
32. Liao, W., T. Y. Hui, S. G. Young, and R. A. Davis. 2003. Blocking microsomal triglyceride transfer protein interferes with apoB secretion without causing retention or stress in the ER. J. Lipid Res. 44: 978-985.
33. Haze, K., H. Yoshida, H. Yanagi, T. Yura, and K. Mori. 1999. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell. 10: 3787-3799.
34. Lee, A. H., N. N. Iwakoshi, and L. H. Glimcher. 2003. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23: 7448-7459.
35. Sriburi, R., S. Jackowski, K. Mori, and J. W. Brewer. 2004. XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167: 35-41.
36. Iwawaki, T., A. Hosoda, T. Okuda, Y. Kamigori, C. Nomura-Furuwatari, Y. Kimata, A. Tsuru, and K. Kohno. 2001. Translational control by the ER transmembrane kinase ribonuclease IRE1 under ER stress. Nat. Cell Biol. 3: 158-164.