PPARα (peroxisome proliferator-activated receptor α) activation reduces hepatic CEACAM1 protein expression to regulate fatty acid oxidation during fasting-refeeding transition

Journal of Biological Chemistry

Volumn 291, Issue 15, 2016, Pages 8121-8129

  Ramakrishnan, Sadeesh K ^a   Khuder, Saja S ^a   Al Share, Qusai Y ^a   Russo, Lucia ^a   Abdallah, Simon L ^a   Patel, Payal R ^a   Heinrich, Garrett ^a   Muturi, Harrison T ^a   Mopidevi, Brahma R ^a   Oyarce, Ana Maria ^a   Shah, Yatrik M ^b   Sanchez, Edwin R ^a   Najjar, Sonia M ^a,c  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c OHIO UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION; CHEMICAL ACTIVATION; CYTOLOGY; ELECTROPHORESIS; INSULIN; MAMMALS; PHYSIOLOGY; PROTEINS; RATS;

CARCINOEMBRYONIC ANTIGEN; CHROMATIN IMMUNOPRECIPITATION ANALYSIS; FATTY ACID OXIDATION; FATTY ACID SYNTHASE; LUCIFERASE REPORTER ASSAYS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; PROTEIN EXPRESSIONS; WESTERN-BLOT ANALYSIS;

FATTY ACIDS;

CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; CD66 ANTIGENS; CELL ADHESION MOLECULE; FATTY ACID; INSULIN; LEUKOCYTE ANTIGEN; MESSENGER RNA;

5' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ARTICLE; CEACAM1 GENE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DIET RESTRICTION; DOWN REGULATION; ENZYME ACTIVATION; FATTY ACID OXIDATION; GENE DELETION; GENE EXPRESSION REGULATION; GLUCOSE HOMEOSTASIS; INSULIN CLEARANCE; INSULIN RELEASE; INSULIN SENSITIVITY; LUCIFERASE ASSAY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; GENETICS; LIVER; METABOLISM; OXIDATION REDUCTION REACTION; RAT;

ANIMALS; ANTIGENS, CD; CELL ADHESION MOLECULES; CELLS, CULTURED; FASTING; FATTY ACIDS; GENE DELETION; GENE EXPRESSION REGULATION; INSULIN; LIVER; MALE; MICE; MICE, INBRED C57BL; OXIDATION-REDUCTION; PPAR ALPHA; PROMOTER REGIONS, GENETIC; RATS; RNA, MESSENGER;

EID: 84964617557     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.714014     Document Type: Article

References (35)

1. Goodarzi, M. O., Cui, J., Chen, Y. D., Hsueh, W. A., Guo, X., and Rotter, J. I. (2011) Fasting insulin reflects heterogeneous physiological processes: role of insulin clearance. Am. J. Physiol. Endocrinol. Metab. 301, E402-E408
2. Ader, M., Stefanovski, D., Kim, S. P., Richey, J. M., Ionut, V., Catalano, K. J., Hucking, K., Ellmerer, M., Van Citters, G., Hsu, I. R., Chiu, J. D., Woolcott, O. O., Harrison, L. N., Zheng, D., Lottati, M., Kolka, C. M., Mooradian, V., Dittmann, J., Yae, S., Liu, H., Castro, A. V., Kabir, M., and Bergman, R. N. (2014) Hepatic insulin clearance is the primary determinant of insulin sensitivity in the normal dog. Obesity 22, 1238-1245
3. Najjar, S. M., Philippe, N., Suzuki, Y., Ignacio, G. A., Formisano, P., Accili, D., and Taylor, S. I. (1995) Insulin-stimulated phosphorylation of recombinant pp120/HA4, an endogenous substrate of the insulin receptor tyrosine kinase. Biochemistry 34, 9341-9349
4. Formisano, P., Najjar, S. M., Gross, C. N., Philippe, N., Oriente, F., Kern-Buell, C. L., Accili, D., and Gorden, P. (1995) Receptor-mediated internalization of insulin: potential role of pp120/HA4, a substrate of the insulin receptor kinase. J. Biol. Chem. 270, 24073-24077
5. Poy, M. N., Yang, Y., Rezaei, K., Fernström, M. A., Lee, A. D., Kido, Y., Erickson, S. K., and Najjar, S. M. (2002)CEACAM1regulates insulin clearance in liver. Nat. Genet. 30, 270-276
6. Najjar, S. M. (2002) Regulation of insulin action by CEACAM1. Trends. Endocrinol. Metab. 13, 240-245
7. Najjar, S. M., Boisclair, Y. R., Nabih, Z. T., Philippe, N., Imai, Y., Suzuki, Y., Suh, D. S., and Ooi, G. T. (1996) Cloning and characterization of a functional promoter of the rat pp120 gene, encoding a substrate of the insulin receptor tyrosine kinase. J. Biol. Chem. 271, 8809-8817
8. Ward, G. M., Walters, J. M., Aitken, P. M., Best, J. D., and Alford, F. P. (1990) Effects of prolonged pulsatile hyperinsulinemia in humans: enhancement of insulin sensitivity. Diabetes 39, 501-507
9. Wong, R. H., Chang, I., Hudak, C. S., Hyun, S., Kwan, H. Y., and Sul, H. S. (2009) A role of DNA-PK for the metabolic gene regulation in response to insulin. Cell 136, 1056-1072
10. Najjar, S. M., Yang, Y., Fernström, M. A., Lee, S. J., Deangelis, A. M., Rjaily, G. A., Al-Share, Q. Y., Dai, T., Miller, T. A., Ratnam, S., Ruch, R. J., Smith, S., Lin, S. H., Beauchemin, N., and Oyarce, A. M. (2005) Insulin acutely decreases hepatic fatty acid synthase activity. Cell Metab. 2, 43-53
11. Matveyenko, A. V., Liuwantara, D., Gurlo, T., Kirakossian, D., Dalla Man, C., Cobelli, C., White, M. F., Copps, K. D., Volpi, E., Fujita, S., and Butler, P. C. (2012) Pulsatile portal vein insulin delivery enhances hepatic insulin action and signaling. Diabetes 61, 2269-2279
12. Göttlicher, M., Widmark, E., Li, Q., and Gustafsson, J. A. (1992) Fatty acids activate a chimera of the clofibric acid-activated receptor and the glucocorticoid receptor. Proc. Natl. Acad. Sci. U.S.A. 89, 4653-4657
13. Kersten, S., Seydoux, J., Peters, J. M., Gonzalez, F. J., Desvergne, B., and Wahli, W. (1999) Peroxisome proliferator-activated receptor α mediates the adaptive response to fasting. J. Clin. Invest. 103, 1489-1498
14. Leone, T. C., Weinheimer, C. J., and Kelly, D. P. (1999) A critical role for the peroxisome proliferator-activated receptor α (PPARα) in the cellular fasting response: the PPARα-null mouse as a model of fatty acid oxidation disorders. Proc. Natl. Acad. Sci. U.S.A. 96, 7473-7478
15. Evans, R. M., Barish, G. D., and Wang, Y. X. (2004) PPARs and the complex journey to obesity. Nat. Med. 10, 355-361
16. Patsouris, D., Reddy, J. K., Müller, M., and Kersten, S. (2006) Peroxisome proliferator-activated receptor α mediates the effects of high-fat diet on hepatic gene expression. Endocrinology 147, 1508-1516
17. Sugden, M. C., Bulmer, K., Gibbons, G. F., Knight, B. L., and Holness, M. J. (2002) Peroxisome proliferator-activated receptor-α (PPARα) deficiency leads to dysregulation of hepatic lipid and carbohydrate metabolism by fatty acids and insulin. Biochem. J. 364, 361-368
18. Moir, A. M., and Zammit, V. A. (1993) Monitoring the partitioning of hepatic fatty acids in vivo: keeping track of control. Biochem. J. 289, 49-55
19. DeAngelis, A. M., Heinrich, G., Dai, T., Bowman, T. A., Patel, P. R., Lee, S. J., Hong, E. G., Jung, D. Y., Assmann, A., Kulkarni, R. N., Kim, J. K., and Najjar, S. M. (2008) Carcinoembryonic antigen-related cell adhesion molecule 1: a link between insulin and lipid metabolism. Diabetes 57, 2296-2303
20. Park, S. Y., Cho, Y. R., Kim, H. J., Hong, E. G., Higashimori, T., Lee, S. J., Goldberg, I. J., Shulman, G. I., Najjar, S. M., and Kim, J. K. (2006) Mechanism of glucose intolerance in mice with dominant negative mutation of CEACAM1. Am. J. Physiol. Endocrinol. Metab. 291, E517-E524
21. Al-Share, Q. Y., DeAngelis, A. M., Lester, S. G., Bowman, T. A., Ramakrishnan, S. K., Abdallah, S. L., Russo, L., Patel, P. R., Kaw, M. K., Raphael, C. K., Kim, A. J., Heinrich, G., Lee, A. D., Kim, J. K., Kulkarni, R. N., Philbrick, W. M., and Najjar, S. M. (2015) Forced hepatic overexpression of CEACAM1 curtails diet-induced insulin resistance. Diabetes 64, 2780-2790
22. Kim, J. B., Wright, H. M., Wright, M., and Spiegelman, B. M. (1998) ADD1/SREBP1 activates PPARα through the production of endogenous ligand. Proc. Natl. Acad. Sci. U.S.A. 95, 4333-4337
23. Kamiya, A., Inoue, Y., Kodama, T., and Gonzalez, F. J. (2004) Hepatocyte nuclear factors 1α and 4α control expression of proline oxidase in adult liver. FEBS Lett. 578, 63-68
24. Iritani, N. (1992) Nutritional and hormonal regulation of lipogenic-enzyme gene expression in rat liver. Eur. J. Biochem. 205, 433-442
25. Assifi, M. M., Suchankova, G., Constant, S., Prentki, M., Saha, A. K., and Ruderman, N. B. (2005) AMP-activated protein kinase and coordination of hepatic fatty acid metabolism of starved/carbohydrate-refed rats. Am. J. Physiol. Endocrinol. Metab. 289, E794-E800
26. Roden, M., and Shulman, G. I. (1999) Applications of NMR spectroscopy to study muscle glycogen metabolism in man. Annu. Rev. Med. 50, 277-290
27. Cariello, N. F., Romach, E. H., Colton, H. M., Ni, H., Yoon, L., Falls, J. G., Casey, W., Creech, D., Anderson, S. P., Benavides, G. R., Hoivik, D. J., Brown, R., and Miller, R. T. (2005) Gene expression profiling of the PPAR-α agonist ciprofibrate in the cynomolgus monkey liver. Toxicol. Sci. 88, 250-264
28. Gremlich, S., Nolan, C., Roduit, R., Burcelin, R., Peyot, M. L., Delghingaro-Augusto, V., Desvergne, B., Michalik, L., Prentki, M., and Wahli, W. (2005) Pancreatic islet adaptation to fasting is dependent on peroxisome proliferator-activated receptor α transcriptional up-regulation of fatty acid oxidation. Endocrinology 146, 375-382
29. Rubí, B., Antinozzi, P. A., Herrero, L., Ishihara, H., Asins, G., Serra, D., Wollheim, C. B., Maechler, P., and Hegardt, F. G. (2002) Adenovirusmediated overexpression of liver carnitine palmitoyltransferase I in INS1E cells: effects on cell metabolism and insulin secretion. Biochem. J. 364, 219-226
30. Kane, C. D., Stevens, K. A., Fischer, J. E., Haghpassand, M., Royer, L. J., Aldinger, C., Landschulz, K. T., Zagouras, P., Bagley, S. W., Hada, W., Dullea, R., Hayward, C. M., and Francone, O. L. (2009) Molecular charac-terization of novel and selective peroxisome proliferator-activated receptor α agonists with robust hypolipidemic activity in vivo. Mol. Pharmacol. 75, 296-306
31. Shah, Y. M., Morimura, K., Yang, Q., Tanabe, T., Takagi, M., and Gonzalez, F. J. (2007) Peroxisome proliferator-activated receptor α regulates a microRNA-mediated signaling cascade responsible for hepatocellular proliferation. Mol. Cell. Biol. 27, 4238-4247
32. Xu, E., Dubois, M. J., Leung, N., Charbonneau, A., Turbide, C., Avramoglu, R. K., DeMarte, L., Elchebly, M., Streichert, T., Lévy, E., Beauchemin, N., and Marette, A. (2009) Targeted disruption of carcinoembryonic antigenrelated cell adhesion molecule 1 promotes diet-induced hepatic steatosis and insulin resistance. Endocrinology 150, 3503-3512
33. Durgan, D. J., Smith, J. K., Hotze, M. A., Egbejimi, O., Cuthbert, K. D., Zaha, V. G., Dyck, J. R., Abel, E. D., and Young, M. E. (2006) Distinct transcriptional regulation of long-chain acyl-CoA synthetase isoforms and cytosolic thioesterase 1 in the rodent heart by fatty acids and insulin. Am. J. Physiol. Heart Circ. Physiol. 290, H2480-H2497
34. Hue, L., and Taegtmeyer, H. (2009) The Randle cycle revisited: a new head for an old hat. Am. J. Physiol. Endocrinol. Metab. 297, E578-E591
35. Xu, J., Xiao, G., Trujillo, C., Chang, V., Blanco, L., Joseph, S. B., Bassilian, S., Saad, M. F., Tontonoz, P., Lee, W. N., and Kurland, I. J. (2002) Peroxisome proliferator-activated receptor α (PPARα) influences substrate utilization for hepatic glucose production. J. Biol. Chem. 277, 50237-50244