Deletion of PARP-2 induces hepatic cholesterol accumulation and decrease in HDL levels

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 4, 2014, Pages 594-602

  Szántó, Magdolna ^a,b   Brunyánszki, Attila ^a   Márton, Judit ^b   Vámosi, György ^b   Nagy, Lilla ^b   Fodor, Tamás ^b   Kiss, Borbála ^c   Virág, László ^a,b   Gergely, Pál ^b   Bai, Péter ^a,b  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

ABCA1; Cholesterol; HDL; Lipoprotein; PARP 2; SREBP1

Indexed keywords

ABC TRANSPORTER A1; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ANIMAL EXPERIMENT; ARTICLE; CARDIOVASCULAR DISEASE; CHOLESTEROL LIVER LEVEL; CONTROLLED STUDY; DEPLETION; ENZYME ACTIVATION; ENZYME INDUCTION; HOMEOSTASIS; HYPERCHOLESTEROLEMIA; LIPID LIVER LEVEL; LIPOPROTEIN BLOOD LEVEL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RISK FACTOR; STEADY STATE;

ABCA1; CHOLESTEROL; HDL; LIPOPROTEIN; PARP-2; SREBP1;

ANIMALS; CHOLESTEROL; HEP G2 CELLS; HUMANS; LIPOPROTEINS, HDL; LIVER; MALE; MICE; POLY(ADP-RIBOSE) POLYMERASES; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

EID: 84893489225     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.12.006     Document Type: Article

References (46)

1. Ame J.C., Rolli V., Schreiber V., Niedergang C., Apiou F., Decker P., Muller S., Hoger T., Menissier-de Murcia J., de Murcia G. PARP-2, A novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase. J. Biol. Chem. 1999, 274:17860-17868.
2. Schreiber V., Ame J.C., Dolle P., Schultz I., Rinaldi B., Fraulob V., Menissier-de Murcia J., de Murcia G. Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J. Biol. Chem. 2002, 277:23028-23036.
3. Haenni S.S., Hassa P.O., Altmeyer M., Fey M., Imhof R., Hottiger M.O. Identification of lysines 36 and 37 of PARP-2 as targets for acetylation and auto-ADP-ribosylation. Int. J. Biochem. Cell Biol. 2008, 40:2274-2283.
4. Szanto M., Brunyánszki A., Kiss B., Nagy L., Gergely P., Virag L., Bai P. Poly(ADP-ribose) polymerase-2: emerging transcriptional roles of a DNA repair protein. Cell. Mol. Life Sci. 2012, 69:4079-4092.
5. Bai P., Canto C., Brunyanszki A., Huber A., Szanto M., Cen Y., Yamamoto H., Houten S.M., Kiss B., Oudart H., Gergely P., Menissier-de Murcia J., Schreiber V., Sauve A.A., Auwerx J. PARP-2 regulates SIRT1 expression and whole-body energy expenditure. Cell Metab. 2011, 13:450-460.
6. Bai P., Houten S.M., Huber A., Schreiber V., Watanabe M., Kiss B., de Murcia G., Auwerx J., Menissier-de Murcia J. Poly(ADP-ribose) polymerase-2 controls adipocyte differentiation and adipose tissue function through the regulation of the activity of the retinoid X receptor/peroxisome proliferator-activated receptor-gamma heterodimer. J. Biol. Chem. 2007, 282:37738-37746.
7. Maeda Y., Hunter T.C., Loudy D.E., Dave V., Schreiber V., Whitsett J.A. PARP-2 interacts with TTF-1 and regulates expression of surfactant protein-B. J. Biol. Chem. 2006, 281:9600-9606.
8. Bai P., Canto C. The role of PARP-1 and PARP-2 enzymes in metabolic regulation and disease. Cell Metab. 2012, 16:290-295.
9. Erener S., Mirsaidi A., Hesse M., Tiaden A.N., Ellingsgaard H., Kostadinova R., Donath M.Y., Richards P.J., Hottiger M.O. ARTD1 deletion causes increased hepatic lipid accumulation in mice fed a high-fat diet and impairs adipocyte function and differentiation. Faseb J. 2012, 26:2631-2638.
10. Bai P., Canto C., Oudart H., Brunyanszki A., Cen Y., Thomas C., Yamamoto H., Huber A., Kiss B., Houtkooper R.H., Schoonjans K., Schreiber V., Sauve A.A., Menissier-de Murcia J., Auwerx J. PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab. 2011, 13:461-468.
11. Menissier-de Murcia J., Ricoul M., Tartier L., Niedergang C., Huber A., Dantzer F., Schreiber V., Ame J.C., Dierich A., LeMeur M., Sabatier L., Chambon P., de Murcia G. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J. 2003, 22:2255-2263.
12. Erdelyi K., Bai P., Kovacs I., Szabo E., Mocsar G., Kakuk A., Szabo C., Gergely P., Virag L. Dual role of poly(ADP-ribose) glycohydrolase in the regulation of cell death in oxidatively stressed A549 cells. Faseb J. 2009, 23:3553-3563.
13. Hasty A.H., Shimano H., Yahagi N., Amemiya-Kudo M., Perrey S., Yoshikawa T., Osuga J., Okazaki H., Tamura Y., Iizuka Y., Shionoiri F., Ohashi K., Harada K., Gotoda T., Nagai R., Ishibashi S., Yamada N. Sterol regulatory element-binding protein-1 is regulated by glucose at the transcriptional level. J. Biol. Chem. 2000, 275:31069-31077.
14. Szanto M., Rutkai I., Hegedus C., Czikora A., Rozsahegyi M., Kiss B., Virag L., Gergely P., Toth A., Bai P. Poly(ADP-ribose) polymerase-2 depletion reduces doxorubicin-induced damage through SIRT1 induction. Cardiovasc. Res. 2011, 92:430-438.
15. Geng B., Cai Y., Gao S., Lu J., Zhang L., Zou J., Liu M., Yu S., Ye J., Liu P. PARP-2 knockdown protects cardiomyocytes from hypertrophy via activation of SIRT1. Biochem. Biophys. Res. Commun. 2013, 430:944-950.
16. Yelamos J., Monreal Y., Saenz L., Aguado E., Schreiber V., Mota R., Fuente T., Minguela A., Parrilla P., de Murcia G., Almarza E., Aparicio P., Menissier-de Murcia J. PARP-2 deficiency affects the survival of CD4+CD8+ double-positive thymocytes. EMBO J. 2006, 25:4350-4360.
17. Liang Y.C., Hsu C.Y., Yao Y.L., Yang W.M. PARP-2 regulates cell cycle-related genes through histone deacetylation and methylation independently of poly(ADP-ribosyl)ation. Biochem. Biophys. Res. Commun. 2013, 431:58-64.
18. Cohausz O., Althaus F.R. Role of PARP-1 and PARP-2 in the expression of apoptosis-regulating genes in HeLa cells. Cell Biol. Toxicol. 2008, 25:379-391.
19. Brown M.S., Goldstein J.L. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997, 89:331-340.
20. Horton J.D., Shah N.A., Warrington J.A., Anderson N.N., Park S.W., Brown M.S., Goldstein J.L. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:12027-12032.
21. Wang X., Sato R., Brown M.S., Hua X., Goldstein J.L. SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell 1994, 77:53-62.
22. Hua X., Yokoyama C., Wu J., Briggs M.R., Brown M.S., Goldstein J.L., Wang X. SREBP-2, a second basic-helix-loop-helix-leucine zipper protein that stimulates transcription by binding to a sterol regulatory element. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:11603-11607.
23. Horton J.D., Shimomura I., Ikemoto S., Bashmakov Y., Hammer R.E. Overexpression of sterol regulatory element-binding protein-1a in mouse adipose tissue produces adipocyte hypertrophy, increased fatty acid secretion, and fatty liver. J. Biol. Chem. 2003, 278:36652-36660.
24. Moroni F., Formentini L., Gerace E., Camaioni E., Pellegrini-Giampietro D.E., Chiarugi A., Pellicciari R. Selective PARP-2 inhibitors increase apoptosis in hippocampal slices but protect cortical cells in models of post-ischaemic brain damage. Br. J. Pharmacol. 2009, 157:854-862.
25. Shieh W.M., Ame J.C., Wilson M.V., Wang Z.Q., Koh D.W., Jacobson M.K., Jacobson E.L. Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J. Biol. Chem. 1998, 273:30069-30072.
26. Bodzioch M., Orso E., Klucken J., Langmann T., Bottcher A., Diederich W., Drobnik W., Barlage S., Buchler C., Porsch-Ozcurumez M., Kaminski W.E., Hahmann H.W., Oette K., Rothe G., Aslanidis C., Lackner K.J., Schmitz G. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat. Genet. 1999, 22:347-351.
27. Brooks-Wilson A., Marcil M., Clee S.M., Zhang L.H., Roomp K., van Dam M., Yu L., Brewer C., Collins J.A., Molhuizen H.O., Loubser O., Ouelette B.F., Fichter K., Ashbourne-Excoffon K.J., Sensen C.W., Scherer S., Mott S., Denis M., Martindale D., Frohlich J., Morgan K., Koop B., Pimstone S., Kastelein J.J., Genest J., Hayden M.R. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet. 1999, 22:336-345.
28. Meder V.S., Boeglin M., de Murcia G., Schreiber V. PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli. J. Cell Sci. 2005, 118:211-222.
29. Farres J., Martin-Caballero J., Martinez C., Lozano J.J., Llacuna L., Ampurdanes C., Ruiz-Herguido C., Dantzer F., Schreiber V., Villunger A., Bigas A., Yelamos J. PARP-2 is required to maintain hematopoiesis following sublethal gamma-irradiation in mice. Blood 2013, 122:44-54.
30. Quenet D., Gasser V., Fouillen L., Cammas F., Sanglier-Cianferani S., Losson R., Dantzer F. The histone subcode: poly(ADP-ribose) polymerase-1 (Parp-1) and Parp-2 control cell differentiation by regulating the transcriptional intermediary factor TIF1beta and the heterochromatin protein HP1alpha. Faseb J. 2008, 22:3853-3865.
31. Wahlberg E., Karlberg T., Kouznetsova E., Markova N., Macchiarulo A., Thorsell A.G., Pol E., Frostell A., Ekblad T., Oncu D., Kull B., Robertson G.M., Pellicciari R., Schuler H., Weigelt J. Family-wide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat. Biotechnol. 2012, 30:283-288.
32. Kraus W.L. Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr. Opin. Cell Biol. 2008, 20:294-302.
33. Kraus W.L., Hottiger M.O. PARP-1 and gene regulation: progress and puzzles. Mol. Aspects Med. 2013, 34:1109-1123.
34. Liu X., Qiao A., Ke Y., Kong X., Liang J., Wang R., Ouyang X., Zuo J., Chang Y., Fang F. FoxO1 represses LXRalpha-mediated transcriptional activity of SREBP-1c promoter in HepG2 cells. FEBS Lett. 2010, 584:4330-4334.
35. Fernandez-Alvarez A., Tur G., Lopez-Rodas G., Casado M. Reciprocal regulation of the human sterol regulatory element binding protein (SREBP)-1a promoter by Sp1 and EGR-1 transcription factors. FEBS Lett. 2008, 582:177-184.
36. Field F.J., Watt K., Mathur S.N. Origins of intestinal ABCA1-mediated HDL-cholesterol. J. Lipid Res. 2008, 49:2605-2619.
37. Kolovou G.D., Mikhailidis D.P., Anagnostopoulou K.K., Daskalopoulou S.S., Cokkinos D.V. Tangier disease four decades of research: a reflection of the importance of HDL. Curr. Med. Chem. 2006, 13:771-782.
38. Kang M.H., Singaraja R., Hayden M.R. Adenosine-triphosphate-binding cassette transporter-1 trafficking and function. Trends Cardiovasc. Med. 2010, 20:41-49.
39. Soran H., Hama S., Yadav R., Durrington P.N. HDL functionality. Curr. Opin. Lipidol. 2012, 23:353-366.
40. Fisher E.A., Feig J.E., Hewing B., Hazen S.L., Smith J.D. High-density lipoprotein function, dysfunction, and reverse cholesterol transport. Arterioscler. Thromb. Vasc. Biol. 2012, 32:2813-2820.
41. Pacher P., Beckman J.S., Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007, 87:315-424.
42. Pacher P., Liaudet L., Bai P., Virag L., Mabley J.G., Hasko G., Szabo C. Activation of poly(ADP-ribose) polymerase contributes to development of doxorubicin-induced heart failure. J. Pharmacol. Exp. Ther. 2002, 300:862-867.
43. Hans C.P., Feng Y., Naura A.S., Zerfaoui M., Rezk B.M., Xia H., Kaye A.D., Matrougui K., Lazartigues E., Boulares A.H. Protective effects of PARP-1 knockout on dyslipidemia-induced autonomic and vascular dysfunction in ApoE mice: effects on eNOS and oxidative stress. PLoS One 2009, 4:e7430.
44. Hans C.P., Zerfaoui M., Naura A.S., Catling A., Boulares A.H. Differential effects of PARP inhibition on vascular cell survival and ACAT-1 expression favouring atherosclerotic plaque stability. Cardiovasc. Res. 2008, 78:429-439.
45. Benko R., Pacher P., Vaslin A., Kollai M., Szabo C. Restoration of the endothelial function in the aortic rings of apolipoprotein E deficient mice by pharmacological inhibition of the nuclear enzyme poly(ADP-ribose) polymerase. Life Sci. 2004, 75:1255-1261.
46. Xu S., Bai P., Little P.J., Liu P. Poly(ADP-ribose) polymerase 1 (PARP1) in atherosclerosis: from molecular mechanisms to therapeutic implications. Mol. Med. Rev. 2013, 10.1002/med.21300.