SIRT1-metabolite binding histone macroH2A1.1 protects hepatocytes against lipid accumulation

Aging

Volumn 6, Issue 1, 2014, Pages 35-47

  Pazienza, Valerio ^a   Borghesan, Michela ^a   Mazza, Tommaso ^a   Sheedfar, Fareeba ^b   Panebianco, Concetta ^a   Williams, Roger ^c   Mazzoccoli, Gianluigi ^a   Andriulli, Angelo ^a   Nakanishi, Tomoko ^d   Vinciguerra, Manlio ^a,e,f  

^a CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c INSTITUTE OF HEPATOLOGY   (United Kingdom)

^d TOTTORI UNIVERSITY   (Japan)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f Euro Mediterranean Institute of Science and Technology   (Italy)

Author keywords

Gene expression; Hepatocyte; Histone macroH2A1; Lipids

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE ACETATE; FATTY ACID; GLUCOSE; HISTONE; MACROH2A HISTONE; SIRT1 PROTEIN, HUMAN; SIRT1 PROTEIN, MOUSE; SIRTUIN 1;

ANIMAL; ARTICLE; BIOSYNTHESIS; ENZYMOLOGY; FATTY LIVER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; GLYCOGEN LIVER LEVEL; HEPG2 CELL LINE; HUMAN; LIPID METABOLISM; LIVER CELL; METABOLISM; MOUSE; NONALCOHOLIC FATTY LIVER; PROTEIN BINDING;

ANIMALS; FATTY ACIDS; FATTY LIVER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; HEP G2 CELLS; HEPATOCYTES; HISTONES; HUMANS; LIPID METABOLISM; LIVER GLYCOGEN; MICE; O-ACETYL-ADP-RIBOSE; PROTEIN BINDING; SIRTUIN 1; TRANSFECTION;

EID: 84893472182     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100632     Document Type: Article

References (47)

1. Myers RP. Noninvasive diagnosis of nonalcoholic fatty liver disease. Ann Hepatol 2009; 8 Suppl 1:S25-33.
2. Lou-Bonafonte JM, Arnal C, Osada J. New genes involved in hepatic steatosis. Curr Opin Lidipol. 2011. 22:159-164.
3. Kantartzis K, Schick F, Haring HU, Stefan N. Environmental and genetic determinants of fatty liver in humans. Dig Dis. 2010. 28:169-178.
4. Sheedfar F, Biase SD, Koonen D, Vinciguerra M. Liver diseases and aging: friends or foes? Aging Cell. 2013. 12:950-954.
5. Podrini C, Borghesan M, Greco A, Pazienza V, Mazzoccoli G, Vinciguerra M. Redox homeostasis and epigenetics in nonalcoholic fatty liver disease (NAFLD). Curr Pharm Des. 2013. 19:2737-2746.
6. Boyd-Kirkup JD, Green CD, Wu G, Wang D, Han JD. Epigenomics and the regulation of aging. Epigenomics. 2013. 5:205-227.
7. Lopez MF, Tollervey J, Krastins B, Garces A, Sarracino D, Prakash A, Vogelsang M, Geesman G, Valderrama A, Jordan IK, Lunyak VV. Depletion of nuclear histone H2A variants is associated with chronic DNA damage signaling upon drugevoked senescence of human somatic cells. Aging. 2012, 4:823-842.
8. Goldberg A, Allis, CD, Bernstein, E. Epigenetics: a landscape takes shape. Cell. 2007. 128:635-638.
9. Doye nC, An, W, Angelov, D, Bondarenko, V, Mietton, F, Studitsky, VM, Hamiche, A, Roeder, RG, Bouvet, P, Dimitrov, S. Mechanism of polymerase II transcription repression by the histone variant macroH2A. Mol Cell Biol. 2006. 26:1156-1164.
10. Ladurner AG. Inactivating chromosomes: a macro domain that minimizes transcription. Mol Cell. 2003. 12:1-3.
11. Gamble M, Frizzell, KM, Yang, C, Krishnakumar, R, Kraus, WL. The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev. 2010, 24:21-32.
12. Changolkar LN, Costanzi C, Leu NA, Chen D, McLaughlin KJ, Pehrson JR. Developmental changes in histone macroH2A1-mediated gene regulation. Mol Cell Biol. 2007. 27:2758-2764.
13. Boulard M, Storck S, Cong R, Pinto R, Delage H, Bouvet P. Histone variant macroH2A1 deletion in mice causes femalespecific steatosis. Epigenetics & Chromatin. 2010; 3: 8.
14. Kustatscher G, Hothorn M, Pugieux C, Scheffzek K, Ladurner AG. Splicing regulates NAD metabolite binding to histone macroH2A. Nat Struct Mol Biol. 2005. 12:624-625.
15. Ladurner AG: Rheostat control of gene expression by metabolites. Mol Cell. 2006. 24:1-11.
16. Timinszky G, Till S, Hassa PO, Hothorn M, Kustatscher G, Nijmeijer B, Colombelli J, Altmeyer M, Stelzer EH, Scheffzek K, Hottiger MO, Ladurner AG. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat Struct Mol Biol. 2009. 16:923-929.
17. Rasmussen TP, Huang T, Mastrangelo MA, Loring J, Panning B, Jaenisch R. Messenger RNAs encoding mouse histone macroH2A1 isoforms are expressed at similar levels in male and female cells and result from alternative splicing. Nucleic Acid Research 1999. 27:3685-3689.
18. Novikov L, Park JW, Chen H, Klerman H, Jalloh AS, Gamble MJ. QKI-mediated alternative splicing of the histone variant MacroH2A1 regulates cancer cell proliferation. Mol Cell Biol. 2011. 31:4244-4255.
19. Sporn JC, Kustatscher G, Hothorn T, Collado M, Serrano M, Muley T, Schnabel P, Ladurner AG. Histone macroH2A isoforms predict the risk of lung cancer recurrence. Oncogene. 2009. 28:3423-3428.
20. Sporn JC, Jung B. Differential regulation and predictive potential of MacroH2A1 isoforms in colon cancer. Am J Pathol. 2012. 180:2516-2526.
21. Rappa F, Greco A, Podrini C, Cappello F, Foti M, Bourgoin L, Peyrou M, Marino A, Scibetta N, Williams R, Mazzoccoli G, Federici M, Pazienza V, Vinciguerra M. Immunopositivity for histone macroH2A1 isoforms marks steatosis-associated hepatocellular carcinoma. PLOS ONE. 2013. 8:e54458.
22. Kreiling JA, Tamamori-Adachi M, Sexton AN, Jeyapalan JC, Munoz-Najar U, Peterson AL, Manivannan J, Rogers ES, Pchelintsev NA, Adams PD, Sedivy JM. Age-associated increase in heterochromatic marks in murine and primate tissues. Aging Cell. 2011. 10:292-304.
23. Kapoor A, Goldberg MS, Cumberland LK, Ratnakumar K, Segura MF, Emanuel PO, Menendez S, Vardabasso C, Leroy G, Vidal CI, Polsky D, Osman I, Garcia BA, Hernando E, Bernstein E. The histone variant macroH2A suppresses melanoma progression through regulation of CDK8. Nature. 2010. 468:1105-1109.
24. Vinciguerra M, Carrozzino, F, Peyrou, M, Carlone, S, Montesano, R, Benelli, R, Foti, M. Unsaturated fatty acids promote hepatoma proliferation and progression through downregulation of the tumor suppressor PTEN. J Hepatol. 2009. 50:1132-1141.
25. Vinciguerra M, Sgroi A, Veyrat-Durebex C, Rubbia-Brandt L, Buhler LH, Foti M. Unsaturated fatty acids inhibit the expression of tumor suppressor phosphatase and tensin homolog (PTEN) via microRNA-21 up-regulation in hepatocytes. Hepatology. 2009. 49:1176-1184.
26. Vinciguerra M, Veyrat-Durebex C, Moukil MA, Rubbia-Brandt L, Rohner-Jeanrenaud F, Foti M. PTEN down-regulation by unsaturated fatty acids triggers hepatic steatosis via an NFkappaBp65/mTOR-dependent mechanism. Gastroenterology. 2008. 134:268-280.
27. Willhauck MJ, Sharif Samani BR, Klutz K, Cengic N, Wolf I, Mohr L, Geissler M, Senekowitsch-Schmidtke R, Göke B, Morris JC, Spitzweg C. Alpha-fetoprotein promoter-targeted sodium iodide symporter gene therapy of hepatocellular carcinoma. Gene Therapy. 2008. 15:214-223.
28. Brown MS, Goldstein JL. Selective versus total insulin resistance: a pathogenic paradox. Cell Metab. 2008. 7(2):95-96.
29. Kuhla A, Blei T, Jaster R, Vollmar B. Aging is associated with a shift of fatty metabolism toward lipogenesis. J Gerontol A Biol Sci Med Sci. 2011. 66:1192-1200.
30. Ferreri C, Kratzsch S, Brede O, Marciniak B, Chatgilialoglu C. Trans lipid formation induced by thiols in human monocytic leukemia cells. Free Rad Biol Med 2005. 38:1180-1187.
31. Pehrson JR, Fried VA. MacroH2A, a core histone containing a large nonhistone region. Science. 1992. 257:1398-1400.
32. Gaspar-Maia A, Qadeer ZA, Hasson D, Ratnakumar K, Leu NA, Leroy G, Liu S, Costanzi C, Valle-Garcia D, Schaniel C, Lemischka I, Garcia B, Pehrson JR, Bernstein E. MacroH2A histone variants act as a barrier upon reprogramming towards pluripotency. Nature Commun. 2013. 4: 1565.
33. Altmeyer M, Hottiger MO. Poly(ADP-ribose) polymerase 1 at the crossroad of metabolic stress and inflammation in aging. Aging. 2009. 1:458-469.
34. Guarente L: Franklin H. Epstein Lecture: Sirtuins, aging, and medicine. New Engl J Med. 2011. 364:2235-2244.
35. Dardenne E, Pierredon S, Driouch K, Gratadou L, Lacroix-Triki M, Espinoza MP, Zonta E, Germann S, Mortada H, Villemin JP, Dutertre M, Lidereau R, Vagner S, Auboeuf D. Splicing switch of an epigenetic regulator by RNA helicases promotes tumor-cell invasiveness. Nat Struct Mol Biol. 2012. 19:1139-1146.
36. Liu X, Strable MS, Ntambi JM: Stearoyl CoA desaturase 1. role in cellular inflammation and stress. Adv Nutr. 2011. 2:15-22.
37. Postic C, Girard J. Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. J Clin Invest. 2008. 118:829-838.
38. Herranz D, Munoz-Martin M, Canamero M, Mulero F, Martinez-Pastor B, Fernandez-Capetillo O, Serrano M. Sirt1 improves healthy ageing and protects from metabolic syndromeassociated cancer. Nature Commun. 2010, 1:3.
39. Bai P, Canto C. The role of PARP-1 and PARP-2 enzymes in metabolic regulation and disease. Cell Metab. 2012. 16:290-295.
40. Guarente L. Sirtuins, aging, and metabolism. Cold Spring Harb Symp Quant Biol. 2011. 76:81-90.
41. Chen D, Vollmar M, Rossi MN, Phillips C, Kraehenbuehl R, Slade D, Mehrotra PV, von Delft F, Crosthwaite SK, Gileadi O, Denu JM, Ahel I. Identification of macrodomain proteins as novel O-acetyl-ADP-ribose deacetylases. J Biol Chem. 2011. 286:13261-13271.
42. Tong L, Denu JM. Function and metabolism of sirtuin metabolite O-acetyl-ADP-ribose. Biochim Biophys Acta. 2010. 1804:1617-1625.
43. Kim JM, Heo K, Choi J, Kim K, An W. The histone variant MacroH2A regulates Ca(2+) influx through TRPC3 and TRPC6 channels. Oncogenesis. 2013. 2:e77.
44. Pasque V, Gillich A, Garrett N, Gurdon JB. Histone variant macroH2A confers resistance to nuclear reprogramming. EMBO J. 2011. 30:2373-2387.
45. Huang D, Cheung AT, Parsons JT, Bryer-Ash M. Focal adhesion kinase (FAK) regulates insulin-stimulated glycogen synthesis in hepatocytes. J Biol Chem. 2002. 277:18151-18160.
46. Deblon N, Bourgoin L, Veyrat-Durebex C, Peyrou M, Vinciguerra M, Caillon A, Maeder C, Fournier M, Montet X, Rohner-Jeanrenaud F, Foti, M. Chronic mTOR inhibition by rapamycin induces muscle insulin resistance despite weight loss in rats. Br J Pharmacol. 2012. 165:2325-2340.
47. Suzuki R, Shimodaira H: Pvclust. an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics. 2006. 22:1540-1542.