ARTD1-induced poly-ADP-ribose formation enhances PPARγ ligand binding and co-factor exchange

Nucleic Acids Research

Volumn 43, Issue 1, 2015, Pages 129-142

  Lehmann, Mareike ^a   Pirinen, Eija ^b,c   Mirsaidi, Ali ^a   Kunze, Friedrich A ^a   Richards, Peter J ^a   Auwerx, Johan ^b   Hottiger, Michael O ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b EPFL   (Switzerland)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); LIGAND; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, MOUSE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; POLY(ADENOSINE DIPHOSPHATE RIBOSE);

ADIPOGENESIS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; CELL LINE; CELL SIZE; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; GENETICS; LIPID DIET; MALE; METABOLISM; MOUSE; TRANSCRIPTION INITIATION; WEIGHT GAIN; WHITE ADIPOSE TISSUE;

ADIPOGENESIS; ADIPOSE TISSUE, WHITE; ANIMALS; CELL LINE; CELL SIZE; DIET, HIGH-FAT; DNA TOPOISOMERASES, TYPE II; LIGANDS; MALE; MICE; MICE, INBRED C57BL; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTORS; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; PPAR GAMMA; RESPONSE ELEMENTS; TRANSCRIPTIONAL ACTIVATION; WEIGHT GAIN;

EID: 84941124962     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1260     Document Type: Article

References (57)

1. Church, C., Horowitz, M., Rodeheffer, M. (2012) WAT is a functional adipocyte? Adipocyte, 1, 38-45.
2. Siersbaek, R., Nielsen, R., John, S., Sung, M.H., Baek, S., Loft, A., Hager, G.L., Mandrup, S. (2011) Extensive chromatin remodelling and establishment of transcription factor 'hotspots' during early adipogenesis. EMBO J., 30, 1459-1472.
3. Heikkinen, S., Auwerx, J., Argmann, C.A. (2007) PPARgamma in human and mouse physiology. Biochim. Biophys. Acta, 1771, 999-1013.
4. Tontonoz, P., Spiegelman, B.M. (2008) Fat and beyond: the diverse biology of PPAR-. Annu. Rev. Biochem., 77, 289-312.
5. Vidal-Puig, A., Jimenez-Linan, M., Lowell, B.B., Hamann, A., Hu, E., Spiegelman, B., Flier, J.S., Moller, D.E. (1996) Regulation of PPAR gamma gene expression by nutrition and obesity in rodents. J. Clin. Invest., 97, 2553-2561.
6. Fajas, L., Auboeuf, D., Raspe, E., Schoonjans, K., Lefebvre, A.M., Saladin, R., Najib, J., Laville, M., Fruchart, J.C., Deeb, S. et al. (1997) The organization, promoter analysis, and expression of the human PPARgamma gene. J. Biol. Chem., 272, 18779-18789.
7. Kliewer, S.A., Umesono, K., Mangelsdorf, D.J., Evans, R.M. (1992) Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature, 355, 446-449.
8. Escher, P., Braissant, O., Basu-Modak, S., Michalik, L., Wahli, W., Desvergne, B. (2001) Rat PPARs: quantitative analysis in adult rat tissues and regulation in fasting and refeeding. Endocrinology, 142, 4195-4202.
9. Chawla, A., Boisvert, W.A., Lee, C.H., Laffitte, B.A., Barak, Y., Joseph, S.B., Liao, D., Nagy, L., Edwards, P.A., Curtiss, L.K. et al. (2001) A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol. Cell, 7, 161-171.
10. Siersbaek, R., Nielsen, R., Mandrup, S. (2010) PPAR-in adipocyte differentiation and metabolism-novel insights from genome-wide studies. FEBS Lett., 584, 3242-3249.
11. Gampe, R.T. Jr., Montana, V.G., Lambert, M.H., Miller, A.B., Bledsoe, R.K., Milburn, M.V., Kliewer, S.A., Willson, T.M., Xu, H.E. (2000) Asymmetry in the PPAR-/RXR-crystal structure reveals the molecular basis of heterodimerization among nuclear receptors. Mol. Cell, 5, 545-555.
12. Kallenberger, B.C., Love, J.D., Chatterjee, V.K., Schwabe, J.W. (2003) A dynamic mechanism of nuclear receptor activation and its perturbation in a human disease. Nat. Struct. Biol., 10, 136-140.
13. Yu, C., Markan, K., Temple, K.A., Deplewski, D., Brady, M.J., Cohen, R.N. (2005) The nuclear receptor corepressors NCoR and SMRT decrease peroxisome proliferator-activated receptor gamma transcriptional activity and repress 3T3-L1 adipogenesis. J. Biol. Chem., 280, 13600-13605.
14. Tontonoz, P., Hu, E., Graves, R.A., Budavari, A.I., Spiegelman, B.M. (1994) mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev., 8, 1224-1234.
15. Lefterova, M.I., Zhang, Y., Steger, D.J., Schupp, M., Schug, J., Cristancho, A., Feng, D., Zhuo, D., Stoeckert, C.J. Jr., Liu, X.S. et al. (2008) PPAR-and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genome-wide scale. Genes Dev., 22, 2941-2952.
16. Saladin, R., Fajas, L., Dana, S., Halvorsen, Y.D., Auwerx, J., Briggs, M. (1999) Differential regulation of peroxisome proliferator activated receptor gamma1 (PPARgamma1) and PPARgamma2 messenger RNA expression in the early stages of adipogenesis. Cell Growth Differ., 10, 43-48.
17. Rosen, E.D., Hsu, C.H., Wang, X., Sakai, S., Freeman, M.W., Gonzalez, F.J., Spiegelman, B.M. (2002) C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev., 16, 22-26.
18. Hottiger, M.O., Hassa, P.O., Luscher, B., Schuler, H., Koch-Nolte, F. (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci., 35, 208-219.
19. Vyas, S., Matic, I., Uchima, L., Rood, J., Zaja, R., Hay, R.T., Ahel, I., Chang, P. (2014) Family-wide analysis of poly(ADP-ribose) polymerase activity. Nat. Commun., 5, 4426.
20. Hassa, P.O., Hottiger, M.O. (2008) The diverse biological roles of mammalian PARPs, a small but powerful family of poly-ADP-ribose polymerases. Front. Biosci., 13, 3046-3082.
21. Graziani, G., Szabo, C. (2005) Clinical perspectives of PARP inhibitors. Pharmacol. Res., 52, 109-118.
22. Underhill, C., Toulmonde, M., Bonnefoi, H. (2011) A review of PARP inhibitors: from bench to bedside. Ann. Oncol., 22, 268-279.
23. Wahlberg, E., Karlberg, T., Kouznetsova, E., Markova, N., Macchiarulo, A., Thorsell, A.G., Pol, E., Frostell, A., Ekblad, T., Oncu, D. et al. (2012) Family-wide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat. Biotechnol., 30, 283-288.
24. Erener, S., Hesse, M., Kostadinova, R., Hottiger, M.O. (2012) Poly(ADP-ribose)polymerase-1 (PARP1) controls adipogenic gene expression and adipocyte function. Mol. Endocrinol., 26, 79-86.
25. Erener, S., Mirsaidi, A., Hesse, M., Tiaden, A.N., Ellingsgaard, H., Kostadinova, R., Donath, M.Y., Richards, P.J., Hottiger, M.O. (2012) ARTD1 deletion causes increased hepatic lipid accumulation in mice fed a high-fat diet and impairs adipocyte function and differentiation. FASEB J., 26, 2631-2638.
26. Pirinen, E., Canto, C., Jo, Y.S., Morato, L., Zhang, H., Menzies, K.J., Williams, E.G., Mouchiroud, L., Moullan, N., Hagberg, C. et al. (2014) Pharmacological Inhibition of poly(ADP-ribose) polymerases improves fitness and mitochondrial function in skeletal muscle. Cell Metab., 19, 1034-1041.
27. Santoro, R., Li, J., Grummt, I. (2002) The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat. Genet., 32, 393-396.
28. Bai, P., Canto, C. (2012) The role of PARP-1 and PARP-2 enzymes in metabolic regulation and disease. Cell Metab., 16, 290-295.
29. Bai, P., Houten, S.M., Huber, A., Schreiber, V., Watanabe, M., Kiss, B., de Murcia, G., Auwerx, J., Menissier-de Murcia, J. (2007) Poly(ADP-ribose) polymerase-2 [corrected] controls adipocyte differentiation and adipose tissue function through the regulation of the activity of the retinoid X receptor/peroxisome proliferator-activated receptor-gamma [corrected] heterodimer. J. Biol. Chem., 282, 37738-37746.
30. Skurk, T., Alberti-Huber, C., Herder, C., Hauner, H. (2007) Relationship between adipocyte size and adipokine expression and secretion. J. Clin. Endocrinol. Metab., 92, 1023-1033.
31. Després, J.-P., Lemieux, I. (2006) Abdominal obesity and metabolic syndrome. Nature, 444, 881-887.
32. Ntambi, J.M., Young-Cheul, K. (2000) Adipocyte differentiation and gene expression. J. Nutr., 130, 3122S-3126S.
33. Picard, F., Kurtev, M., Chung, N., Topark-Ngarm, A., Senawong, T., Machado De Oliveira, R., Leid, M., McBurney, M.W., Guarente, L. (2004) Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature, 429, 771-776.
34. Shieh, W., Amé, J., Wilson, M., Wang, Z., Koh, D., Jacobson, M., Jacobson, E. (1998) Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J. Biol. Chem., 273, 30069-30072.
35. Tee, M.K., Rogatsky, I., Tzagarakis-Foster, C., Cvoro, A., An, J., Christy, R.J., Yamamoto, K.R., Leitman, D.C. (2004) Estradiol and selective estrogen receptor modulators differentially regulate target genes with estrogen receptors alpha and beta. Mol. Biol. Cell, 15, 1262-1272.
36. Gelman, L., Zhou, G., Fajas, L., Raspe, E., Fruchart, J.C., Auwerx, J. (1999) p300 interacts with the N-and C-terminal part of PPARgamma2 in a ligand-independent and-dependent manner, respectively. J. Biol. Chem., 274, 7681-7688.
37. Lee, J.W., Lee, Y.C., Na, S.Y., Jung, D.J., Lee, S.K. (2001) Transcriptional coregulators of the nuclear receptor superfamily: coactivators and corepressors. Cell. Mol. Life Sci., 58, 289-297.
38. Rosenfeld, M., Lunyak, V., Glass, C. (2006) Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev., 20, 1405-1428.
39. Rosen, E.D., Walkey, C.J., Puigserver, P., Spiegelman, B.M. (2000) Transcriptional regulation of adipogenesis. Genes Dev., 14, 1293-1307.
40. Ju, B.-G., Lunyak, V., Perissi, V., Garcia-Bassets, I., Rose, D., Glass, C., Rosenfeld, M. (2006) A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science, 312, 1798-1802.
41. Nitiss, J.L. (2009) DNA topoisomerase II and its growing repertoire of biological functions. Nat. Rev. Cancer, 9, 327-337.
42. Tzameli, I., Fang, H., Ollero, M., Shi, H., Hamm, J.K., Kievit, P., Hollenberg, A.N., Flier, J.S. (2004) Regulated production of a peroxisome proliferator-activated receptor-gamma ligand during an early phase of adipocyte differentiation in 3T3-L1 adipocytes. J. Biol. Chem., 279, 36093-36102.
43. Forman, B.M., Chen, J., Evans, R.M. (1997) Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc. Natl. Acad. Sci. U.S.A., 94, 4312-4317.
44. Keller, H., Dreyer, C., Medin, J., Mahfoudi, A., Ozato, K., Wahli, W. (1993) Fatty acids and retinoids control lipid metabolism through activation of peroxisome proliferator-activated receptor-retinoid X receptor heterodimers. Proc. Natl. Acad. Sci. U.S.A., 90, 2160-2164.
45. Kliewer, S.A., Sundseth, S.S., Jones, S.A., Brown, P.J., Wisely, G.B., Koble, C.S., Devchand, P., Wahli, W., Willson, T.M., Lenhard, J.M. et al. (1997) Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors alpha and gamma. Proc. Natl. Acad. Sci. U.S.A., 94, 4318-4323.
46. Krey, G., Braissant, O., L'Horset, F., Kalkhoven, E., Perroud, M., Parker, M.G., Wahli, W. (1997) Fatty acids, eicosanoids, and hypolipidemic agents identified as ligands of peroxisome proliferator-activated receptors by coactivator-dependent receptor ligand assay. Mol. Endocrinol., 11, 779-791.
47. Houseknecht, K.L., Cole, B.M., Steele, P.J. (2002) Peroxisome proliferator-activated receptor gamma (PPAR-) and its ligands: a review. Domest. Anim. Endocrinol., 22, 1-23.
48. Huang, D., Yang, C., Wang, Y., Liao, Y., Huang, K. (2009) PARP-1 suppresses adiponectin expression through poly(ADP-ribosyl)ation of PPAR gamma in cardiac fibroblasts. Cardiovasc. Res., 81, 98-107.
49. Bourguet, W., Germain, P., Gronemeyer, H. (2000) Nuclear receptor ligand-binding domains: three-dimensional structures, molecular interactions and pharmacological implications. Trends Pharmacol. Sci., 21, 381-388.
50. Li, P., Fan, W., Xu, J., Lu, M., Yamamoto, H., Auwerx, J., Sears, D.D., Talukdar, S., Oh, D., Chen, A. et al. (2011) Adipocyte NCoR knockout decreases PPARgamma phosphorylation and enhances PPARgamma activity and insulin sensitivity. Cell, 147, 815-826.
51. Hassa, P.O., Buerki, C., Lombardi, C., Imhof, R., Hottiger, M.O. (2003) Transcriptional coactivation of nuclear factor-B-dependent gene expression by p300 is regulated by poly(ADP)-ribose polymerase-1. J. Biol. Chem., 278, 45145-45153.
52. Tulin, A., Spradling, A. (2003) Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science, 299, 560-562.
53. Ju, B.-G., Solum, D., Song, E., Lee, K.-J., Rose, D., Glass, C., Rosenfeld, M. (2004) Activating the PARP-1 sensor component of the groucho/TLE1 corepressor complex mediates a CaMKinase IIdelta-dependent neurogenic gene activation pathway. Cell, 119, 815-829.
54. Ju, B.-G., Rosenfeld, M. (2006) A breaking strategy for topoisomerase IIbeta/PARP-1-dependent regulated transcription. Cell Cycle, 5, 2557-2560.
55. Straus, D.S., Glass, C.K. (2007) Anti-inflammatory actions of PPAR ligands: new insights on cellular and molecular mechanisms. Trends Immunol., 28, 551-558.
56. Li, P., Spann, N.J., Kaikkonen, M.U., Lu, M., Oh da, Y., Fox, J.N., Bandyopadhyay, G., Talukdar, S., Xu, J., Lagakos, W.S. et al. (2013) NCoR repression of LXRs restricts macrophage biosynthesis of insulin-sensitizing omega 3 fatty acids. Cell, 155, 200-214.
57. Rodriguez, A., Catalan, V., Gomez-Ambrosi, J., Fruhbeck, G. (2007) Visceral and subcutaneous adiposity: are both potential therapeutic targets for tackling the metabolic syndrome? Curr. Pharm. Des., 13, 2169-2175.