Microsomal triglyceride transfer protein inhibition induces endoplasmic reticulum stress and increases gene transcription via Ire1α/cJun to enhance plasma ALT/AST

Journal of Biological Chemistry

Volumn 288, Issue 20, 2013, Pages 14372-14383

  Josekutty, Joby ^a   Iqbal, Jahangir ^a   Iwawaki, Takao ^b   Kohno, Kenji ^c   Hussain, M Mahmood ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

^b GUNMA UNIVERSITY   (Japan)

^c NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; CELL MEMBRANES; PROTEINS; TRANSCRIPTION; VEGETABLE OILS;

ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FREE CHOLESTEROLS; GENE TRANSCRIPTIONS; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEINS; PLASMA LIPID; PLASMA TRIGLYCERIDES; PROTEIN INHIBITION; TRIGLYCERIDE-RICH LIPOPROTEINS; UP-REGULATION;

CHOLESTEROL;

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GLUTATHIONE; LACTATE DEHYDROGENASE; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; PROTEIN C JUN; PROTEIN IRE1;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CELL FRACTIONATION; CELL ORGANELLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME INHIBITION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84877914445     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.459602     Document Type: Article

References (37)

1. Grundy, S. M., Cleeman, J. I., Merz, C. N., Brewer, H. B., Jr., Clark, L. T., Hunninghake, D. B., Pasternak, R. C., Smith, S. C., Jr., Stone, N. J., and Coordinating Committee of the National Cholesterol Education Program (2004) Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III Guidelines. J. Am. Coll. Cardiol. 44, 720-732
2. LaRosa, J. C., Grundy, S. M., Waters, D. D., Shear, C., Barter, P., Fruchart, J.-C., Gotto, A. M., Greten, H., Kastelein, J. J., Shepherd, J., Wenger, N. K., and Treating to New Targents (TNT) Investigators (2005) Intensive lipid lowering with atorvastatin in patients with stable coronary disease. N. Engl. J. Med. 352, 1425-1435 (Pubitemid 40471450)
3. Hussain, M. M., Rava, P., Walsh, M., Rana, M., and Iqbal, J. (2012) Multiple functions of microsomal triglyceride transfer protein. Nutr. Metab. 9, 14
4. Cuchel, M., Bloedon, L. T., Szapary, P. O., Kolansky, D. M., Wolfe, M. L., Sarkis, A., Millar, J. S., Ikewaki, K., Siegelman, E. S., Gregg, R. E., and Rader, D. J. (2007) Inhibition of microsomal triglyceride transfer protein in familial hypercholesterolemia. N. Engl. J. Med. 356, 148-156 (Pubitemid 46089675)
5. Liu, R., Pan, X., and Whitington, P. F. (2009) Increased hepatic expression is a major determinant of serum alanine aminotransferase elevation in mice with nonalcoholic steatohepatitis. Liver Int. 29, 337-343
6. Reichling, J. J., and Kaplan, M. M. (1988) Clinical use of serum enzymes in liver disease. Dig. Dis. Sci. 33, 1601-1614 (Pubitemid 19095465)
7. Pratt, D. S., and Kaplan, M. M. (2000) Evaluation of abnormal liver-enzyme results in asymptomatic patients. N. Engl. J. Med. 342, 1266-1271 (Pubitemid 30235957)
8. Iwawaki, T., Akai, R., Yamanaka, S., and Kohno, K. (2009) Function of IRE1- in the placenta is essential for placental development and embryonic viability. Proc. Natl. Acad. Sci. U.S.A. 106, 16657-16662
9. Nair, S., Xu, C., Shen, G., Hebbar, V., Gopalakrishnan, A., Hu, R., Jain, M. R., Liew, C., Chan, J. Y., and Kong, A.-N. (2007) Toxicogenomics of endoplasmic reticulum stress inducer tunicamycin in the small intestine and liver of Nrf2 knockout and C57BL/6J mice. Toxicol. Lett. 168, 21-39 (Pubitemid 44920408)
10. McKenney, J. M. (1988) Lovastatin. A new cholesterol-lowering agent. Clin. Pharm. 7, 21-36
11. Robl, J. A., Sulsky, R., Sun, C. Q., Simpkins, L. M., Wang, T., Dickson, J. K., Jr., Chen, Y., Magnin, D. R., Taunk, P., Slusarchyk, W. A., Biller, S. A., Lan, S. J., Connolly, F., Kunselman, L. K., Sabrah, T., Jamil, H., Gordon, D., Harrity, T. W., and Wetterau, J. R. (2001) A novel series of highly potent benzimidazole-based microsomal triglyceride transfer protein inhibitors. J. Med. Chem. 44, 851-856 (Pubitemid 32861609)
12. Kubota, N., Terauchi, Y., Kubota, T., Kumagai, H., Itoh, S., Satoh, H., Yano, W., Ogata, H., Tokuyama, K., Takamoto, I., Mineyama, T., Ishikawa, M., Moroi, M., Sugi, K., Yamauchi, T., Ueki, K., Tobe, K., Noda, T., Nagai, R., and Kadowaki, T. (2006) Pioglitazone ameliorates insulin resistance and diabetes by both adiponectin-dependent and -independent pathways. J. Biol. Chem. 281, 8748-8755 (Pubitemid 43847980)
13. Burstein, M., Scholnick, H. R., and Morfin, R. (1970) Rapid method for the isolation of lipoproteins from human serum by precipitation with polyanions. J. Lipid. Res. 11, 583-595
14. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Phys. 37, 911-917
15. Athar, H., Iqbal, J., Jiang, X. C., and Hussain, M. M. (2004) A simple, rapid, and sensitive fluorescence assay for microsomal triglyceride transfer protein. J. Lipid. Res. 45, 764-772 (Pubitemid 38405684)
16. Arduino, D. M., Esteves, A. R., Domingues, A. F., Pereira, C. M., Cardoso, S. M., and Oliveira, C. R. (2009) ER-mediated stress induces mitochondrial-dependent caspases activation in NT2 neuron-like cells. BMB. Rep. 42, 719-724
17. Liao, W., Hui, T. Y., Young, S. G., and Davis, R. A. (2003) Blocking microsomal triglyceride transfer protein interferes with apoB secretion without causing retention or stress in the ER. J. Lipid. Res. 44, 978-985 (Pubitemid 37279657)
18. Björkegren, J., Beigneux, A., Bergo, M. O., Maher, J. J., and Young, S. G. (2002) Blocking the secretion of hepatic very low density lipoproteins renders the liver more susceptible to toxin-induced injury. J. Biol. Chem. 277, 5476-5483 (Pubitemid 34968597)
19. 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, 497-505
20. Iqbal, J., Rudel, L. L., and Hussain, M. M. (2008) Microsomal triglyceride transfer protein enhances cellular cholesteryl esterification by relieving product inhibition. J. Biol. Chem. 283, 19967-19980
21. Marí, M., Caballero, F., Colell, A., Morales, A., Caballeria, J., Fernandez, A., Enrich, C., Fernandez-Checa, J. C., and García-Ruiz, C. (2006) Mitochondrial free cholesterol loading sensitizes to TNF- and Fas-mediated steatohepatitis. Cell. Metab. 4, 185-198
22. Tabas, I. (2002) Consequences of cellular cholesterol accumulation. Basic concepts and physiological implications. J. Clin. Invest. 110, 905-911
23. Vuppalanchi, R., and Chalasani, N. (2009) Nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Selected practical issues in their evaluation and management. Hepatology 49, 306-317
24. Walter, P., and Ron, D. (2011) The unfolded protein response. From stress pathway to homeostatic regulation. Science 334, 1081-1086
25. Crooke, R., Baker, B., and Wedel, M. (2008) in Antisense Drug Technology: Principles, Strategies, and Applications (Taylor & Francis Group, L., ed) pp. 614, CRC Press, Boca Raton, FL
26. Miyazaki, Miwa, S., Kodama, H., Yamada, H., Nagata, K., Toriumi, W., Kitamura, K., and Kume, E. (2007) Hepatic and intestinal changes in rats treated with T-0126, a microsomal triglyceride transfer protein (MTP) inhibitor. J. Toxicol. Sci. 32, 161-177
27. Chang, G., Ruggeri, R. B., and Harwood, H. J. (2002) Microsomal triglyceride transfer protein (MTP) inhibitors. Discovery of clinically active inhibitors using high-throughput screening and parallel synthesis paradigms. Curr. Opin. Drug Discov. Devel. 5, 562-570 (Pubitemid 36748986)
28. Chandler, C. E., Wilder, D. E., Pettini, J. L., Savoy, Y. E., Petras, S. F., Chang, G., Vincent, J., and Harwood, H. J. (2003) CP-346086. An MTP inhibitor that lowers plasma cholesterol and triglycerides in experimental animals and in humans. J. Lipid. Res. 44, 1887-1901 (Pubitemid 37356661)
29. Hong, R. W., Rounds, J. D., Helton, W. S., Robinson, M. K., and Wilmore, D. W. (1992) Glutamine preserves liver glutathione after lethal hepatic injury. Ann. Surg. 215, 114-119
30. Lee, A. H., and Glimcher, L. H. (2009) Intersection of the unfolded protein response and hepatic lipid metabolism. Cell. Mol. Life Sci. 66, 2835-2850
31. Wang, S., Chen, Z., Lam, V., Han, J., Hassler, J., Finck, B. N., Davidson, N. O., and Kaufman, R. J. (2012) IRE1α-XBP1s induces PDI expression to increase MTP activity for hepatic VLDL assembly and lipid homeostasis. Cell. Metab. 16, 473-486
32. Yu, X. X., Murray, S. F., Watts, L., Booten, S. L., Tokorcheck, J., Monia, B. P., and Bhanot, S. (2008) Reduction of JNK1 expression with antisense oligonucleotide improves adiposity in obese mice. Am. J. Physiol. Endocrinol. Metab. 295, E436-445
33. Whillier, S., Garcia, B., Chapman, B. E., Kuchel, P. W., and Raftos, J. E. (2011) Glutamine and α-ketoglutarate as glutamate sources for glutathione synthesis in human erythrocytes. FEBS J. 278, 3152-3163
34. Cheng, S., Rhee, E. P., Larson, M. G., Lewis, G. D., McCabe, E. L., Shen, D., Palma, M. J., Roberts, L. D., Dejam, A., Souza, A. L., Deik, A. A., Magnusson, M., Fox, C. S., O'Donnell, C. J., Vasan, R. S., Melander, O., Clish, C. B., Gerszten, R. E., and Wang, T. J. (2012) Metabolite profiling identifies pathways associated with metabolic risk in humans. Circulation 125, 2222-2231
35. Sookoian, S., and Pirola, C. J. (2012) Alanine and aspartate aminotransferase and glutamine-cycling pathway: their roles in pathogenesis of metabolic syndrome. World J. Gastroenterol. 18, 3775-3781
36. Leibowitz, A., Boyko, M., Shapira, Y., and Zlotnik, A. (2012) Blood glutamate scavenging. Insight into neuroprotection. Int. J. Mol. Sci. 13, 10041-10066
37. Pajor, A. M. (1999) Sodium-coupled transporters for Krebs cycle intermediates. Annu. Rev. Physiol. 61, 663-682