Advertisement

Carbohydrate-Responsive Histone Acetylation in Gene Body Regions

Carbohydrate-Inducible Histone Acetylation
  • Kazuki MochizukiEmail author
  • Natsuyo Hariya
  • Kazue Honma
  • Toshinao Goda
Reference work entry

Abstract

Epigenetic memory is manifested by DNA methylation and histone modification in the chromatin. In the present review, we introduce two types of epigenetic model. The first is the general model, involving a transcription initiation reaction that is regulated by transcription factors and histone acetylation in the promoter/enhancer region. The model is generally an ON-OFF mechanism via the promoter/enhancer region. The second novel model is the transcription elongation reaction, which is triggered by acetylated histone-BRD4-P-TEFb in the gene body region. This novel epigenetic model regulates the efficiency of mRNA synthesis, for example, from 100% to 160% or from 100% to 60%. Major nutrients, including carbohydrates and those that signal energy balance in the body, many of which are associated with development of metabolic diseases, regulate the novel epigenetic model. In addition, carbohydrate signals enhance histone H3K4 methylation, but not histone H3K9 methylation, in the gene bodies of carbohydrate-inducible genes. Taken together, major nutrients, including carbohydrates and those that control energy balance in the body, alter epigenetics in gene body regions.

Keywords

BRD4 Carbohydrate Epigenetics in gene body regions Epigenetics in promoter/enhancer regions Histone acetylation Histone H3K4 methylation Histone modifications Lifestyle related diseases P-TEFb Transcriptional elongation reaction Transcriptional initiation reaction 

Abbreviations

Atp6v0d2

ATPase H+ transporting V0 subunit d2

Bcmo1

β-carotene oxygenase

BRD4

Bromodomain containing 4

CDK

Cyclin dependent kinase

CDX

Caudal type homeobox

CHD

Chromodomain-helicase-DNA-binding protein

ChREBP

Carbohydrate-responsive element-binding protein

Clec4d

C-type lectin domain family 4, member D

CTD

C-terminal domain

Dak

Dihydroxyacetone kinase 2 homolog

Fas

Fatty acid synthase

Cyp8b1

Cytochrome P450, family 8, subfamily B, polypeptide 1

GCN5

General control of amino acid synthesis

Gip

Glucose-dependent insulinotropic polypeptide

Glut5

Glucose transporter

HAT

Histone acetyl-transferase

HNF1

Hepatocyte nuclear factor 1

K

Lysine

Mgam

Maltase-glucoamylase

Mmp12

Matrix metallopeptidase 12

Plin5

Perilipin 5

PolII

RNA polymerase II

PPAR

Peroxisome proliferator-activated receptor

P-TEFb

Positive transcription elongation factor b

RAR

Retinoic acid receptor

SAGA

Spt-Ada-Gcn5 acetyltransferase

SET

SET domain protein

Si

Sucrose-isomaltase

Sglt1

Sodium-glucose cotransporter

VDR

Vitamin D receptor

TFIIH

General transcription factor IIH

Thrsp

Thyroid hormone responsive protein

TR

Thyroid hormone receptor

Trem2

Triggering receptor expressed on myeloid cells 2

Notes

Acknowledgments

Our work cited in the present review was supported by Grants-in-Aid for Young Scientists (22680054), for Scientific Research (26282023) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), the Takeda Science Foundation, and the Uehara Memorial Foundation. We thank Dr. Ozato Keiko from the National Institute of Health for providing the opportunity to study BRD4.

References

  1. Bruce Alberts AJ, Lewis J, Morgan D, Raff M, Roberts K, Walter P (2015) Molecular biology of the cell, 6th edn. Paper ed. Garland Science, New YorkGoogle Scholar
  2. Fujimoto S, Goda T, Mochizuki K (2011) In vivo evidence of enhanced di-methylation of histone H3 K4 on upregulated genes in adipose tissue of diabetic db/db mice. Biochem Biophys Res Commun 404(1):223–227. Epub 2010/11/30CrossRefGoogle Scholar
  3. Girard J, Ferre P, Kervran A, Pegorier JP, Assan R (1977) Role of the insulin/glucagon ration in the change of hepatic metabolism during the development of the rat. In: Glucagon: its role in physiology and clinical medicine. Springer, New York, pp 563–581CrossRefGoogle Scholar
  4. Henning SJ (1978) Plasma concentrations of total and free corticosterone during development in the rat. Am J Phys 235(5):E451–E456. Epub 1978/11/01Google Scholar
  5. Hirose Y, Ohkuma Y (2007) Phosphorylation of the C-terminal domain of RNA polymerase II plays central roles in the integrated events of eucaryotic gene expression. J Biochem 141(5):601–608. Epub 2007/04/05CrossRefGoogle Scholar
  6. Houzelstein D, Bullock SL, Lynch DE, Grigorieva EF, Wilson VA, Beddington RS (2002) Growth and early postimplantation defects in mice deficient for the bromodomain-containing protein Brd4. Mol Cell Biol 22(11):3794–3802CrossRefGoogle Scholar
  7. Inamochi Y, Dey A, Nishiyama A, Kubota T, Ozato K, Goda T et al (2016) Transcription elongation factor Brd4-P-TEFb accelerates intestinal differentiation-associated SLC2A5 gene expression. Biochem Biophys Rep 7:150–156PubMedPubMedCentralGoogle Scholar
  8. Inoue S, Mochizuki K, Goda T (2011) Jejunal induction of SI and SGLT1 genes in rats by high-starch/low-fat diet is associated with histone acetylation and binding of GCN5 on the genes. J Nutr Sci Vitaminol 57(2):162–169. Epub 2011/06/24CrossRefGoogle Scholar
  9. Inoue S, Honma K, Mochizuki K, Goda T (2015) Induction of histone H3K4 methylation at the promoter, enhancer, and transcribed regions of the Si and Sglt1 genes in rat jejunum in response to a high-starch/low-fat diet. Nutrition 31(2):366–372. Epub 2015/01/17CrossRefGoogle Scholar
  10. Jang MK, Mochizuki K, Zhou M, Jeong HS, Brady JN, Ozato K (2005) The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol Cell 19(4):523–534. Epub 2005/08/20CrossRefGoogle Scholar
  11. Krasinski SD, Van Wering HM, Tannemaat MR, Grand RJ (2001) Differential activation of intestinal gene promoters: functional interactions between GATA-5 and HNF-1 alpha. Am J Physiol Gastrointest Liver Physiol 281(1):G69–G84. Epub 2001/06/16CrossRefGoogle Scholar
  12. Lochrin SE, Price DK, Figg WD (2014) BET bromodomain inhibitors – a novel epigenetic approach in castration-resistant prostate cancer. Cancer Biol Ther 15(12):1583–1585. Epub 2014/12/24CrossRefGoogle Scholar
  13. Mochizuki K, Nishiyama A, Jang MK, Dey A, Ghosh A, Tamura T et al (2008) The bromodomain protein Brd4 stimulates G1 gene transcription and promotes progression to S phase. J Biol Chem 283(14):9040–9048. Epub 2008/01/29CrossRefGoogle Scholar
  14. Mochizuki H, Mochizuki K, Suruga K, Igarashi M, Takase S, Goda T (2012) Induction of the BCMO1 gene during the suckling-weaning transition in rats is associated with histone H3 K4 methylation and subsequent coactivator binding and histone H3 acetylation to the gene. J Nutr Sci Vitaminol 58(5):319–326. Epub 2013/01/19CrossRefGoogle Scholar
  15. Morishita S, Mochizuki K, Goda T (2014) Bindings of ChREBP and SREBP1, and histone acetylation around the rat liver fatty acid synthase gene are associated with induction of the gene during the suckling-weaning transition. J Nutr Sci Vitaminol 60(2):94–100. Epub 2014/07/01CrossRefGoogle Scholar
  16. Ortega S, Malumbres M, Barbacid M (2002) Cyclin D-dependent kinases, INK4 inhibitors and cancer. Biochim Biophys Acta 1602(1):73–87. Epub 2002/04/19PubMedGoogle Scholar
  17. Pray-Grant MG, Daniel JA, Schieltz D, Yates JR 3rd, Grant PA (2005) Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 433(7024):434–438. Epub 2005/01/14CrossRefGoogle Scholar
  18. Sakurai N, Mochizuki K, Goda T (2009) Modifications of histone H3 at lysine 9 on the adiponectin gene in 3T3-L1 adipocytes. J Nutr Sci Vitaminol 55(2):131–138. Epub 2009/05/14CrossRefGoogle Scholar
  19. Shimada M, Mochizuki K, Goda T (2009) Dietary resistant starch reduces histone acetylation on the glucose-dependent insulinotropic polypeptide gene in the jejunum. Biosci Biotechnol Biochem 73(12):2754–2757. Epub 2009/12/08CrossRefGoogle Scholar
  20. Shimada M, Mochizuki K, Goda T (2011) Feeding rats dietary resistant starch reduces both the binding of ChREBP and the acetylation of histones on the Thrsp gene in the jejunum. J Agric Food Chem 59(4):1464–1469. Epub 2011/01/20CrossRefGoogle Scholar
  21. Shimada M, Mochizuki K, Goda T (2013) Methylation of histone H3 at lysine 4 and expression of the maltase-glucoamylase gene are reduced by dietary resistant starch. J Nutr Biochem 24(3):606–612. Epub 2012/07/24CrossRefGoogle Scholar
  22. Suzuki T, Douard V, Mochizuki K, Goda T, Ferraris RP (2011) Diet-induced epigenetic regulation in vivo of the intestinal fructose transporter Glut5 during development of rat small intestine. Biochem J 435(1):43–53. Epub 2011/01/13CrossRefGoogle Scholar
  23. Suzuki T, Muramatsu T, Morioka K, Goda T, Mochizuki K (2015) ChREBP binding and histone modifications modulate hepatic expression of the Fasn gene in a metabolic syndrome rat model. Nutrition 31(6):877–883. Epub 2015/05/03CrossRefGoogle Scholar
  24. Xu L, Glass CK, Rosenfeld MG (1999) Coactivator and corepressor complexes in nuclear receptor function. Curr Opin Genet Dev 9(2):140–147. Epub 1999/05/14CrossRefGoogle Scholar
  25. Yamada A, Honma K, Mochizuki K, Goda T (2016) BRD4 regulates fructose-inducible lipid accumulation-related genes in the mouse liver. Metabolism 65(10):1478–1488. Epub 2016/09/14CrossRefGoogle Scholar
  26. Yorita S, Mochizuki K, Goda T (2009) Induction of histone acetylation on the sucrase-isomaltase gene in the postnatal rat jejunum. Biosci Biotechnol Biochem 73(4):933–935. Epub 2009/04/09CrossRefGoogle Scholar
  27. Yoshinaga Y, Mochizuki K, Goda T (2012) Trimethylation of histone H3K4 is associated with the induction of fructose-inducible genes in rat jejunum. Biochem Biophys Res Commun 419(4):605–611. Epub 2012/03/01CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Kazuki Mochizuki
    • 1
    Email author
  • Natsuyo Hariya
    • 2
  • Kazue Honma
    • 3
    • 4
  • Toshinao Goda
    • 3
    • 4
  1. 1.Department of Local Produce and Food Sciences, Faculty of Life and Environmental SciencesUniversity of YamanashiKofuJapan
  2. 2.Department of Nutrition, Faculty of Health and NutritionYamanashi Gakuin UniversityKofuJapan
  3. 3.Graduate School of Nutritional and Environmental SciencesUniversity of ShizuokaShizuokaJapan
  4. 4.Department of Nutrition, School of Food and Nutritional SciencesThe University of ShizuokaShizuokaJapan

Personalised recommendations