Maternal protein restriction during pregnancy induces CCAAT/enhancer-binding protein (C/EBPβ) expression through the regulation of histone modification at its promoter region in female offspring rat skeletal muscle

Epigenetics

Volumn 6, Issue 2, 2011, Pages 161-170

  Zheng, Shasha ^a   Rollet, Michelle ^a   Pan, Yuan Xiang ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Developmental programming; Epigenetics; Pregnancy; Thrifty phenotype hypothesis

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; HISTONE H3; HISTONE H4; PHOSPHOENOLPYRUVATE CARBOXYKINASE (PYROPHOSPHATE); PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; ENERGY METABOLISM; EPIGENETICS; FEMALE; GENETIC REGULATION; HISTONE ACETYLATION; HISTONE MODIFICATION; MALE; MATERNAL NUTRITION; NONHUMAN; PREGNANCY; PROGENY; PROMOTER REGION; PROTEIN BINDING; PROTEIN DIET; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN RESTRICTION; RAT; SEX DIFFERENCE; SKELETAL MUSCLE; TRANSCRIPTION REGULATION;

RATTUS;

EID: 79951503905     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.6.2.13472     Document Type: Article

References (37)

1. Langley-Evans SC, Lilley C, McMullen S. Maternal protein restriction and fetal growth: lack of evidence of a role for homocysteine in fetal programming. Br J Nutr 2006; 96:578-86.
2. Gambling L, Dunford S, Wallace DI, Zuur G, Solanky N, Srai SK, et al. Iron deficiency during pregnancy affects postnatal blood pressure in the rat. J Physiol 2003; 552:603-10.
3. Khan IY, Taylor PD, Dekou V, Seed PT, Lakasing L, Graham D, et al. Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension 2003; 41:168-75.
4. Zimmerman JA, Malloy V, Krajcik R, Orentreich N. Nutritional control of aging. Exp Gerontol 2003; 38:47-52.
5. Zhu MJ, Ford SP, Means WJ, Hess BW, Nathanielsz PW, Du M. Maternal nutrient restriction affects properties of skeletal muscle in offspring. J Physiol 2006; 575:241-50.
6. Dahri S, Snoeck A, Reusens-Billen B, Remacle C, Hoet JJ. Islet function in offspring of mothers on low-protein diet during gestation. Diabetes 1991; 40:115-20.
7. Zambrano E, Bautista CJ, Deas M, Martinez-Samayoa PM, Gonzalez-Zamorano M, Ledesma H, et al. A low maternal protein diet during pregnancy and lactation has sex-and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol 2006; 571:221-30.
8. Lekstrom-Himes J, Xanthopoulos KG. Biological role of the CCAAT/enhancer-binding protein family of transcription factors. J Biol Chem 1998; 273:28545-8.
9. Ramji DP, Foka P. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem J 2002; 365:561-75.
10. Jain R, Police S, Phelps K, Pekala PH. Tumour necrosis factor-alpha regulates expression of the CCAATenhancer-binding proteins (C/EBPs) alpha and beta and determines the occupation of the C/EBP site in the promoter of the insulin-responsive glucose-transporter gene in 3T3-L1 adipocytes. Biochem J 1999; 338:737-43.
11. Tang QQ, Gronborg M, Huang H, Kim JW, Otto TC, Pandey A, et al. Sequential phosphorylation of CCAAT enhancer-binding protein beta by MAPK and glycogen synthase kinase 3beta is required for adipogenesis. Proc Natl Acad Sci USA 2005; 102:9766-71.
12. Paquin A, Barnabe-Heider F, Kageyama R, Miller FD. CCAAT/enhancer-binding protein phosphorylation biases cortical precursors to generate neurons rather than astrocytes in vivo. J Neurosci 2005; 25:10747-58.
13. Croniger CM, Millward C, Yang J, Kawai Y, Arinze IJ, Liu S, et al. Mice with a deletion in the gene for CCAAT/enhancer-binding protein beta have an attenuated response to cAMP and impaired carbohydrate metabolism. J Biol Chem 2001; 276:629-38.
14. Yang H, Mammen J, Wei W, Menconi M, Evenson A, Fareed M, et al. Expression and activity of C/EBPbeta and delta are upregulated by dexamethasone in skeletal muscle. J Cell Physiol 2005; 204:219-26.
15. Wang L, Shao J, Muhlenkamp P, Liu S, Klepcyk P, Ren J, et al. Increased insulin receptor substrate-1 and enhanced skeletal muscle insulin sensitivity in mice lacking CCAAT/enhancer-binding protein beta. J Biol Chem 2000; 275:14173-81.
16. Owen OE, Kalhan SC, Hanson RW. The key role of anaplerosis and cataplerosis for citric acid cycle function. J Biol Chem 2002; 277:30409-12.
17. Marten NW, Sladek FM, Straus DS. Effect of dietary protein restriction on liver transcription factors. Biochem J 1996; 317:361-70.
18. Siu F, Chen C, Zhong C, Kilberg MS. CCAAT/ enhancer-binding protein-beta is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J Biol Chem 2001; 276:48100-7.
19. Chen H, Pan YX, Dudenhausen EE, Kilberg MS. Amino acid deprivation induces the transcription rate of the human asparagine synthetase gene through a timed program of expression and promoter binding of nutrient-responsive basic region/leucine zipper transcription factors as well as localized histone acetylation. J Biol Chem 2004; 279:50829-39.
20. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 2005; 135:1382-6.
21. Sandoval J, Rodriguez JL, Tur G, Serviddio G, Pereda J, Boukaba A, et al. RNAPol-ChIP: a novel application of chromatin immunoprecipitation to the analysis of real-time gene transcription. Nucleic Acids Res 2004; 32:88.
22. Kilberg MS, Pan YX, Chen H, Leung-Pineda V. Nutritional control of gene expression: how mammalian cells respond to amino acid limitation. Annu Rev Nutr 2005; 25:59-85.
23. Kim J, Cantwell CA, Johnson PF, Pfarr CM, Williams SC. Transcriptional activity of CCAAT/enhancer-binding proteins is controlled by a conserved inhibitory domain that is a target for sumoylation. J Biol Chem 2002; 277:38037-44.
24. Descombes P, Schibler U. A liver-enriched transcriptional activator protein, LAP and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 1991; 67:569-79.
25. Marten NW, Burke EJ, Hayden JM, Straus DS. Effect of amino acid limitation on the expression of 19 genes in rat hepatoma cells. FASEB J 1994; 8:538-44.
26. Hilakivi-Clarke L, de AS. Fetal origins of breast cancer. Trends Endocrinol Metab 2006; 17:340-8.
27. Mantena SR, Kannan A, Cheon YP, Li Q, Johnson PF, Bagchi IC, et al. C/EBPbeta is a critical mediator of steroid hormone-regulated cell proliferation and differentiation in the uterine epithelium and stroma. Proc Natl Acad Sci USA 2006; 103:1870-5.
28. Musha Y, Itoh S, Hanson MA, Kinoshita K. Does estrogen affect the development of abnormal vascular function in offspring of rats fed a low-protein diet in pregnancy? Pediatr Res 2006; 59:784-9.
29. Du K, Ding J. Insulin regulates TRB3 and other stressresponsive gene expression through induction of C/ EBPbeta. Mol Endocrinol 2009; 23:475-85.
30. Chamson-Reig A, Thyssen SM, Arany E, Hill DJ. Altered pancreatic morphology in the offspring of pregnant rats given reduced dietary protein is time and gender specific. J Endocrinol 2006; 191:83-92.
31. Liu PC, Matsumura F. TCDD suppresses insulinresponsive glucose transporter (GLUT-4) gene expression through C/EBP nuclear transcription factors in 3T3-L1 adipocytes. J Biochem Mol Toxicol 2006; 20:79-87.
32. Galler JR, Tonkiss J. Prenatal protein malnutrition and maternal behavior in Sprague-Dawley rats. J Nutr 1991; 121:762-9.
33. Du M, Yan X, Tong JF, Zhao J, Zhu MJ. Maternal obesity, inflammation and fetal skeletal muscle development. Biol Reprod 2010; 82:4-12.
34. Du M, Yin J, Zhu MJ. Cellular signaling pathways regulating the initial stage of adipogenesis and marbling of skeletal muscle. Meat Sci 2010; 86:103-9.
35. Tipton KD. Gender differences in protein metabolism. Curr Opin Clin Nutr Metab Care 2001; 4:493-8.
36. Peiris HN, Ponnampalam AP, Mitchell MD, Green MP. Brief Communication: Sexual dimorphic expression of myostatin and follistatin like-3 in a rat transgenerational under-nutrition model. Nutr Metab 2010; 7:44.
37. Greco AV, Mingrone G, Giancaterini A, Manco M, Morroni M, Cinti S, et al. Insulin resistance in morbid obesity: reversal with intramyocellular fat depletion. Diabetes 2002; 51:144-51.