ATP-citrate lyase is essential for high glucose-induced histone hyperacetylation and fibrogenic gene upregulation in mesangial cells

American Journal of Physiology - Renal Physiology

Volumn 313, Issue 2, 2017, Pages F423-F429

  Deb, Dilip K ^a   Chen, Yinyin ^a,b   Sun, Jian ^a,c   Wang, Youli ^a   Li, Yan Chun ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b HUNAN NORMAL UNIVERSITY   (China)

^c Central South University   (China)

Author keywords

ATP citrate lyase; Epigenetic regulation; Glomerulosclerosis; Histone acetylation; Hyperglycemia

Indexed keywords

ADENOSINE TRIPHOSPHATE CITRATE SYNTHASE; COLLAGEN TYPE 4; CONNECTIVE TISSUE GROWTH FACTOR; FIBRONECTIN; GLUCOSE; GREEN FLUORESCENT PROTEIN; HISTONE; HISTONE H3; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA3; ACETYL COENZYME A; CITRIC ACID; CTGF PROTEIN, MOUSE; TGFB1 PROTEIN, MOUSE; TGFB3 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FIBROGENESIS; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HISTONE ACETYLATION; MESANGIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; ACETYLATION; ANIMAL; DIABETIC NEPHROPATHY; DRUG EFFECTS; ENZYMOLOGY; FIBROSIS; GENETIC EPIGENESIS; GENETICS; METABOLISM; NUCLEOCYTOPLASMIC TRANSPORT; PATHOLOGY; PROTEIN PROCESSING; RNA INTERFERENCE; TIME FACTOR; TRANSFORMED CELL LINE;

ACETYL COENZYME A; ACETYLATION; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ATP CITRATE (PRO-S)-LYASE; CELL LINE, TRANSFORMED; CITRIC ACID; COLLAGEN TYPE IV; CONNECTIVE TISSUE GROWTH FACTOR; DIABETIC NEPHROPATHIES; EPIGENESIS, GENETIC; FIBRONECTINS; FIBROSIS; GLUCOSE; HISTONES; MESANGIAL CELLS; MICE; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA INTERFERENCE; TIME FACTORS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA3; UP-REGULATION;

EID: 85026828509     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00029.2017     Document Type: Article

References (41)

1. Bauer DE, Hatzivassiliou G, Zhao F, Andreadis C, Thompson CB. ATP citrate lyase is an important component of cell growth and transformation. Oncogene 24: 6314-6322, 2005. doi:10.1038/sj.onc.1208773.
2. Brasacchio D, Okabe J, Tikellis C, Balcerczyk A, George P, Baker EK, Calkin AC, Brownlee M, Cooper ME, El-Osta A. Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail. Diabetes 58: 1229-1236, 2009. doi:10.2337/db08-1666.
3. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820, 2001. doi:10.1038/414813a.
4. Chypre M, Zaidi N, Smans K. ATP-citrate lyase: a mini-review. Biochem Biophys Res Commun 422: 1-4, 2012. doi:10.1016/j.bbrc.2012. 04.144.
5. Clayton AL, Hazzalin CA, Mahadevan LC. Enhanced histone acetylation and transcription: a dynamic perspective. Mol Cell 23: 289-296, 2006. doi:10.1016/j.molcel.2006.06.017.
6. Cooper ME. Pathogenesis, prevention, and treatment of diabetic nephropathy. Lancet 352: 213-219, 1998. doi:10.1016/S0140-6736(98)01346-4.
7. D’Agord Schaan B, Lacchini S, Bertoluci MC, Irigoyen MC, Machado UF, Schmid H. Increased renal GLUT1 abundance and urinary TGF-β1 in streptozotocin-induced diabetic rats: implications for the development of nephropathy complicating diabetes. Horm Metab Res 33: 664-669, 2001. doi:10.1055/s-2001-18683.
8. Deb DK, Bao R, Li YC. Critical role of the cyclic AMP-protein kinase A pathway in hyperglycemia-induced epigenetic activation of fibrogenic program in the kidney. FASEB J. 31: 2065-2075, 2017. doi:10.1096/fj. 201601116R.
9. Eberharter A, Becker PB. Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep 3: 224-229, 2002. doi:10.1093/embo-reports/ kvf053.
10. El-Osta A, Brasacchio D, Yao D, Pocai A, Jones PL, Roeder RG, Cooper ME, Brownlee M. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 205: 2409-2417, 2008. doi:10.1084/jem. 20081188.
11. Gilbert SF, Migeon BR. D-valine as a selective agent for normal human and rodent epithelial cells in culture. Cell 5: 11-17, 1975. doi:10.1016/ 0092-8674(75)90086-0.
12. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77-88, 2007. doi:10.1016/j.cell.2007.05.042.
13. Gupta S, Clarkson MR, Duggan J, Brady HR. Connective tissue growth factor: potential role in glomerulosclerosis and tubulointerstitial fibrosis. Kidney Int 58: 1389-1399, 2000. doi:10.1046/j.1523-1755.2000.00301.x.
14. Hatzivassiliou G, Zhao F, Bauer DE, Andreadis C, Shaw AN, Dhanak D, Hingorani SR, Tuveson DA, Thompson CB. ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell 8: 311-321, 2005. doi:10.1016/j.ccr.2005.09.008.
15. Heilig C, Zaloga C, Lee M, Zhao X, Riser B, Brosius F, Cortes P. Immunogold localization of high-affinity glucose transporter isoforms in normal rat kidney. Lab Invest 73: 674-684, 1995.
16. Heilig CW, Liu Y, England RL, Freytag SO, Gilbert JD, Heilig KO, Zhu M, Concepcion LA, Brosius FC III. D-glucose stimulates mesangial cell GLUT1 expression and basal and IGF-I-sensitive glucose uptake in rat mesangial cells: implications for diabetic nephropathy. Diabetes 46: 1030-1039, 1997. doi:10.2337/diab.46.6.1030.
17. Kaelin WG Jr, McKnight SL. Influence of metabolism on epigenetics and disease. Cell 153: 56-69, 2013. doi:10.1016/j.cell.2013.03.004.
18. Karmodiya K, Krebs AR, Oulad-Abdelghani M, Kimura H, Tora L. H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genomics 13: 424, 2012. doi:10.1186/1471-2164-13-424.
19. Kato M, Natarajan R. Diabetic nephropathy—emerging epigenetic mechanisms. Nat Rev Nephrol 10: 517-530, 2014. doi:10.1038/nrneph. 2014.116.
20. Kouzarides T. Chromatin modifications and their function. Cell 128: 693-705, 2007. doi:10.1016/j.cell.2007.02.005.
21. Kurtz A, Jelkmann W, Sinowatz F, Bauer C. Renal mesangial cell cultures as a model for study of erythropoietin production. Proc Natl Acad Sci USA 80: 4008-4011, 1983. doi:10.1073/pnas.80.13.4008.
22. Lau OD, Kundu TK, Soccio RE, Ait-Si-Ali S, Khalil EM, Vassilev A, Wolffe AP, Nakatani Y, Roeder RG, Cole PA. HATs off: selective synthetic inhibitors of the histone acetyltransferases p300 and PCAF. Mol Cell 5: 589-595, 2000. doi:10.1016/S1097-2765(00)80452-9.
23. Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell 128: 707-719, 2007. doi:10.1016/j.cell.2007.01.015.
24. Li YC, Bolt MJG, Cao L-P, Sitrin MD. Effects of vitamin D receptor inactivation on the expression of calbindins and calcium metabolism. Am J Physiol Endocrinol Metab 281: E558-E564, 2001.
25. Marcus RG, England R, Nguyen K, Charron MJ, Briggs JP, Brosius FC III. Altered renal expression of the insulin-responsive glucose transporter GLUT4 in experimental diabetes mellitus. Am J Physiol Renal Physiol 267: F816-F824, 1994.
26. Murata H, Zhou L, Ochoa S, Hasan A, Badiavas E, Falanga V. TGF-β3 stimulates and regulates collagen synthesis through TGF-β1-dependent and independent mechanisms. J Invest Dermatol 108: 258-262, 1997. doi:10.1111/1523-1747.ep12286451.
27. Pierce MW, Palmer JL, Keutmann HT, Avruch J. ATP-citrate lyase. Structure of a tryptic peptide containing the phosphorylation site directed by glucagon and the cAMP-dependent protein kinase. J Biol Chem 256: 8867-8870, 1981.
28. Pirola L, Balcerczyk A, Okabe J, El-Osta A. Epigenetic phenomena linked to diabetic complications. Nat Rev Endocrinol 6: 665-675, 2010. doi:10.1038/nrendo.2010.188.
29. Reidy K, Kang HM, Hostetter T, Susztak K. Molecular mechanisms of diabetic kidney disease. J Clin Invest 124: 2333-2340, 2014. doi:10.1172/ JCI72271.
30. Rosner M, Schipany K, Hengstschläger M. Merging high-quality biochemical fractionation with a refined flow cytometry approach to monitor nucleocytoplasmic protein expression throughout the unperturbed mammalian cell cycle. Nat Protoc 8: 602-626, 2013. doi:10.1038/nprot.2013.011.
31. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3: 1101-1108, 2008. doi:10.1038/nprot. 2008.73.
32. Shahbazian MD, Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76: 75-100, 2007. doi:10.1146/annurev.biochem.76.052705.162114.
33. Sun G, Reddy MA, Yuan H, Lanting L, Kato M, Natarajan R. Epigenetic histone methylation modulates fibrotic gene expression. J Am Soc Nephrol 21: 2069-2080, 2010. doi:10.1681/ASN.2010060633.
34. Sutendra G, Kinnaird A, Dromparis P, Paulin R, Stenson TH, Haromy A, Hashimoto K, Zhang N, Flaim E, Michelakis ED. A nuclear pyruvate dehydrogenase complex is important for the generation of acetyl-CoA and histone acetylation. Cell 158: 84-97, 2014. doi:10.1016/j.cell.2014.04.046.
35. Wagner PD, Vu ND. Phosphorylation of ATP-citrate lyase by nucleoside diphosphate kinase. J Biol Chem 270: 21758-21764, 1995. doi:10.1074/ jbc.270.37.21758.
36. Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, Zhao K. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138: 1019-1031, 2009. doi:10.1016/j.cell. 2009.06.049.
37. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, Thompson CB. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324: 1076-1080, 2009. doi:10.1126/science.1164097.
38. Yang W, Xia Y, Hawke D, Li X, Liang J, Xing D, Aldape K, Hunter T, Alfred Yung WK, Lu Z. PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis. Cell 150: 685-696, 2012. doi:10.1016/j.cell.2012.07.018.
39. Yu L, Border WA, Huang Y, Noble NA. TGF-β isoforms in renal fibrogenesis. Kidney Int 64: 844-856, 2003. doi:10.1046/j.1523-1755. 2003.00162.x.
40. Ziyadeh FN. Mediators of diabetic renal disease: the case for TGF-β as the major mediator. J Am Soc Nephrol 15, Suppl 1: S55-S57, 2004. doi:10.1097/01.ASN.0000093460.24823.5B.
41. Ziyadeh FN, Sharma K, Ericksen M, Wolf G. Stimulation of collagen gene expression and protein synthesis in murine mesangial cells by high glucose is mediated by autocrine activation of transforming growth factor-β. J Clin Invest 93: 536-542, 1994. doi:10.1172/JCI117004.