Reversal of glucose intolerance in rat offspring exposed to ethanol before birth through reduction of nuclear skeletal muscle HDAC expression by the bile acid TUDCA

Physiological Reports

Volumn 2, Issue 12, 2014, Pages

  Yao, Xing Hai ^a   Nguyen, Khanh H ^a   Gregoire Nyomba B L ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Endoplasmic reticulum; Histone deacetylase; Insulin resistance; Prenatal alcohol exposure

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ALCOHOL; BILE ACID; GLUCOSE TRANSPORTER 4; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 7; HISTONE DEACETYLASE 9; HISTONE DEACETYLASE INHIBITOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; TAUROURSODEOXYCHOLIC ACID; X BOX BINDING PROTEIN 1;

ADULT; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; FEMALE; GASTROCNEMIUS MUSCLE; GENETIC TRANSFECTION; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; MTT ASSAY; NONHUMAN; PREGNANCY; PRENATAL DRUG EXPOSURE; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MYOBLAST; WESTERN BLOTTING;

EID: 85003571574     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12195     Document Type: Article

References (54)

1. Agudelo, M., N. Gandhi, Z. Saiyed, V. Pichili, S. Thangavel, P. Khatavkar, et al. 2011. Effects of alcohol on histone deacetylase 2 (HDAC2) and the neuroprotective role of trichostatin A (TSA). Alcohol. Clin. Exp. Res. 35:1550-1556.
2. Balasubramanyam, K., V. Swaminathan, A. Ranganathan, and T. K. Kundu. 2003. Small molecule modulators of histone acetyltransferase p300. J. Biol. Chem. 278:19134-19140.
3. Baumeister, P., S. Luo, W. C. Skarnes, G. Sui, E. Seto, Y. Shi, et al. 2005. Endoplasmic reticulum stress induction of the Grp78/BiP promoter: activating mechanisms mediated by YY1 and its interactive chromatin modifiers. Mol. Cell. Biol. 25:4529-4540.
4. Castells, S., E. Mark, F. Abaci, and E. Schwartz. 1981. Growth retardation in fetal alcohol syndrome. Unresponsiveness to growth-promoting hormones. Dev. Pharmacol. Ther. 3:232-241.
5. Chang, C. W., L. Lee, D. Yu, K. Dao, J. Bossuyt, and D. M. Bers. 2013. Acute beta-adrenergic activation triggers nuclear import of histone deacetylase 5 and delays G(q)-induced transcriptional activation. J. Biol. Chem. 288:192-204.
6. Chen, L., and B. L. Nyomba. 2003a. Effects of prenatal alcohol exposure on glucose tolerance in the rat offspring. Metabolism 52:454-462.
7. Chen, L., and B. L. Nyomba. 2003b. Glucose intolerance and resistin expression in rat offspring exposed to ethanol in utero: modulation by postnatal high-fat diet. Endocrinology 144:500-508.
8. Chen, L., X. H. Yao, and B. L. Nyomba. 2005. In vivo insulin signaling through PI3-kinase is impaired in skeletal muscle of adult rat offspring exposed to ethanol in utero. J. Appl. Physiol. 99:528-534.
9. Colell, A., O. Coll, C. Garcia-Ruiz, R. Paris, C. Tiribelli, N. Kaplowitz, et al. 2001. Tauroursodeoxycholic acid protects hepatocytes from ethanol-fed rats against tumor necrosis factor-induced cell death by replenishing mitochondrial glutathione. Hepatology 34:964-971.
10. Cortez, M. Y., C. E. Torgan, J. T. Brozinick Jr, and J. L. Ivy. 1991. Insulin resistance of obese Zucker rats exercise trained at two different intensities. Am. J. Physiol. 261: E613-E619.
11. D’Addario, C., S. Johansson, S. Candeletti, P. Romualdi, S. O. Ogren, L. Terenius, et al. 2011. Ethanol and acetaldehyde exposure induces specific epigenetic modifications in the prodynorphin gene promoter in a human neuroblastoma cell line. FASEB J. 25:1069-1075.
12. Dembele, K., X. H. Yao, L. Chen, and B. L. Nyomba. 2006. Intrauterine ethanol exposure results in hypothalamic oxidative stress and neuroendocrine alterations in adult rat offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291: R796-R802.
13. Elton, C. W., J. S. Pennington, S. A. Lynch, F. M. Carver, and S. N. Pennington. 2002. Insulin resistance in adult rat offspring associated with maternal dietary fat and alcohol consumption. J. Endocrinol. 173:63-71.
14. Guo, W., E. L. Crossey, L. Zhang, S. Zucca, O. L. George, C. F. Valenzuela, et al. 2011. Alcohol exposure decreases CREB binding protein expression and histone acetylation in the developing cerebellum. PLoS ONE 6:e19351.
15. Ha, C. H., J. Y. Kim, J. Zhao, W. Wang, B. S. Jhun, C. Wong, et al. 2010. PKA phosphorylates histone deacetylase 5 and prevents its nuclear export, leading to the inhibition of gene transcription and cardiomyocyte hypertrophy. Proc. Natl Acad. Sci. U.S.A. 107:15467-15472.
16. Hage Hassan, R., I. Hainault, J. T. Vilquin, C. Samama, F. Lasnier, P. Ferre, et al. 2012. Endoplasmic reticulum stress does not mediate palmitate-induced insulin resistance in mouse and human muscle cells. Diabetologia 55:204-214.
17. Harper, K. M., E. Tunc-Ozcan, E. N. Graf, and E. E. Redei. 2014. Intergenerational effects of prenatal ethanol on glucose tolerance and insulin response. Physiol. Genomics 46:159-168.
18. He, L., J. C. Marecki, G. Serrero, F. A. Simmen, M. J. Ronis, and T. M. Badger. 2007. Dose-dependent effects of alcohol on insulin signaling: partial explanation for biphasic alcohol impact on human health. Mol. Endocrinol. 21:2541-2550.
19. Hegedus, Z., A. Czibula, and E. Kiss-Toth. 2007. Tribbles: a family of kinase-like proteins with potent signalling regulatory function. Cell. Signal. 19:238-250.
20. Hong-Brown, L. Q., C. R. Brown, D. S. Huber, and C. H. Lang. 2006. Alcohol and indinavir adversely affect protein synthesis and phosphorylation of MAPK and mTOR signaling pathways in C2C12 myocytes. Alcohol. Clin. Exp. Res. 30:1297-1307.
21. Kadiyala, C. S., L. Zheng, Y. Du, E. Yohannes, H. Y. Kao, M. Miyagi, et al. 2012. Acetylation of retinal histones in diabetes increases inflammatory proteins: effects of minocycline and manipulation of histone acetyltransferase (HAT) and histone deacetylase (HDAC). J. Biol. Chem. 287:25869-25880.
22. Kahali, S., B. Sarcar, A. Prabhu, E. Seto, and P. Chinnaiyan. 2012. Class I histone deacetylases localize to the endoplasmic reticulum and modulate the unfolded protein response. FASEB J. 26:2437-2445.
23. Kaiser, C., and S. R. James. 2004. Acetylation of insulin receptor substrate-1 is permissive for tyrosine phosphorylation. BMC Biol. 2:23.
24. Kars, M., L. Yang, M. F. Gregor, B. S. Mohammed, T. A. Pietka, B. N. Finck, et al. 2010. Tauroursodeoxycholic Acid May Improve Liver and Muscle but Not Adipose Tissue Insulin Sensitivity in Obese Men and Women. Diabetes 59: 1899-1905.
25. Keshavarzian, A., S. Choudhary, E. W. Holmes, S. Yong, A. Banan, S. Jakate, et al. 2001. Preventing gut leakiness by oats supplementation ameliorates alcohol-induced liver damage in rats. J. Pharmacol. Exp. Ther. 299:442-448.
26. Lee, J. H., K. H. Nguyen, S. Mishra, and B. L. Nyomba. 2010. Prohibitin is expressed in pancreatic beta-cells and protects against oxidative and proapoptotic effects of ethanol. FEBS J. 277:488-500.
27. Lindblad, B., and R. Olsson. 1976. Unusually high levels of blood alcohol? J. Am. Med. Assoc. 236:1600-1602.
28. Liu, Y., and M. F. Schneider. 2013. Opposing HDAC4 nuclear fluxes due to phosphorylation by beta-adrenergic activated protein kinase A or by activity or Epac activated CaMKII in skeletal muscle fibres. J. Physiol. 591:3605-3623.
29. Liu, Y., E. O. Hernandez-Ochoa, W. R. Randall, and M. F. Schneider. 2012. NOX2-dependent ROS is required for HDAC5 nuclear efflux and contributes to HDAC4 nuclear efflux during intense repetitive activity of fast skeletal muscle fibers. Am. J. Physiol. Cell Physiol. 303:C334-C347.
30. McGee, S. L., and M. Hargreaves. 2010. Histone modifications and skeletal muscle metabolic gene expression. Clin. Exp. Pharmacol. Physiol. 37:392-396.
31. McKinsey, T. A., C. L. Zhang, and E. N. Olson. 2001. Identification of a signal-responsive nuclear export sequence in class II histone deacetylases. Mol. Cell. Biol. 21:6312-6321.
32. Miura, K., K. Taura, Y. Kodama, B. Schnabl, and D. A. Brenner. 2008. Hepatitis C virus-induced oxidative stress suppresses hepcidin expression through increased histone deacetylase activity. Hepatology 48:1420-1429.
33. Morton, G. J., M. E. Matsen, D. P. Bracy, T. H. Meek, H. T. Nguyen, D. Stefanovski, et al. 2013. FGF19 action in the brain induces insulin-independent glucose lowering. J. Clin. Invest. 123:4799-4808.
34. Narlikar, G. J., H. Y. Fan, and R. E. Kingston. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108:475-487.
35. Nguyen, K. H., J. H. Lee, and B. L. Nyomba. 2012. Ethanol causes endoplasmic reticulum stress and impairment of insulin secretion in pancreatic beta-cells. Alcohol 46:89-99.
36. Ojuka, E. O., V. Goyaram, and J. A. Smith. 2012. The role of CaMKII in regulating GLUT4 expression in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 303:E322-E331.
37. Okumura, K., M. Mendoza, R. M. Bachoo, R. A. DePinho, W. K. Cavenee, and F. B. Furnari. 2006. PCAF modulates PTEN activity. J. Biol. Chem. 281:26562-26568.
38. Pandey, S. C., R. Ugale, H. Zhang, L. Tang, and A. Prakash. 2008. Brain chromatin remodeling: a novel mechanism of alcoholism. J. Neurosci. 28:3729-3737.
39. Park, P. H., R. W. Lim, and S. D. Shukla. 2005. Involvement of histone acetyltransferase (HAT) in ethanol-induced acetylation of histone H3 in hepatocytes: potential mechanism for gene expression. Am. J. Physiol. Gastrointest. Liver Physiol. 289:G1124-G1136.
40. Raichur, S., S. H. Teh, K. Ohwaki, V. Gaur, Y. C. Long, M. Hargreaves, et al. 2012. Histone deacetylase 5 regulates glucose uptake and insulin action in muscle cells. J. Mol. Endocrinol. 49:203-211.
41. Raychaudhuri, N., S. Raychaudhuri, M. Thamotharan, and S. U. Devaskar. 2008. Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring. J. Biol. Chem. 283:13611-13626.
42. Takada, A., T. Miki, A. Kuno, H. Kouzu, D. Sunaga, T. Itoh, et al. 2012. Role of ER stress in ventricular contractile dysfunction in type 2 diabetes. PLoS ONE 7:e39893.
43. Takigawa-Imamura, H., T. Sekine, M. Murata, K. Takayama, K. Nakazawa, and J. Nakagawa. 2003. Stimulation of glucose uptake in muscle cells by prolonged treatment with scriptide, a histone deacetylase inhibitor. Biosci. Biotechnol. Biochem. 67:1499-1506.
44. Urso, T., J. S. Gavaler, and D. H. Van Thiel. 1981. Blood ethanol levels in sober alcohol users seen in an emergency room. Life Sci. 28:1053-1056.
45. Vandoorne, K., M. H. Vandsburger, K. Weisinger, V. Brumfeld, B. A. Hemmings, A. Harmelin, et al. 2013. Multimodal imaging reveals a role for Akt1 in fetal cardiac development. Physiol. Rep. 1:e00143.
46. Weems, J., and A. L. Olson. 2011. Class II histone deacetylases limit GLUT4 gene expression during adipocyte differentiation. J. Biol. Chem. 286:460-468.
47. Werts, R. L., S. C. Van Calcar, D. S. Wargowski, and S. M. Smith. 2014. Inappropriate feeding behaviors and dietary intakes in children with fetal alcohol spectrum disorder or probable prenatal alcohol exposure. Alcohol. Clin. Exp. Res. 38:871-878.
48. Yao, X. H., and B. L. Nyomba. 2007. Abnormal glucose homeostasis in adult female rat offspring after intrauterine ethanol exposure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292:R1926-R1933.
49. Yao, X. H., and B. L. Nyomba. 2008. Hepatic insulin resistance induced by prenatal alcohol exposure is associated with reduced PTEN and TRB3 acetylation in adult rat offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294:R1797-R1806.
50. Yao, X. H., H. K. Nguyen, and B. L. Nyomba. 2013. Prenatal ethanol exposure causes glucose intolerance with increased hepatic gluconeogenesis and histone deacetylases in adult rat offspring: reversal by tauroursodeoxycholic acid. PLoS ONE 8:e59680.
51. Zahradka, P., D. E. Larson, and B. H. Sells. 1989. RNA polymerase II-directed gene transcription by rat skeletal muscle nuclear extracts. Exp. Cell Res. 185:8-20.
52. Zhang, P., Q. Sun, C. Zhao, S. Ling, Q. Li, Y.-Z. Chang, et al. 2014. HDAC4 protects cells from ER stress induced apoptosis through interaction with ATF4. Cell. Signal. 26:556-563.
53. Zhong, L., J. Zhu, T. Lv, G. Chen, H. Sun, X. Yang, et al. 2010. Ethanol and its metabolites induce histone lysine 9 acetylation and an alteration of the expression of heart development-related genes in cardiac progenitor cells. Cardiovasc. Toxicol. 10:268-274.
54. Zhou, R., S. Wang, and X. Zhu. 2012. Prenatal ethanol exposure alters synaptic plasticity in the dorsolateral striatum of rat offspring via changing the reactivity of dopamine receptor. PLoS ONE 7:e42443.