Transcriptional network analysis in muscle reveals AP-1 as a partner of PGC-1α in the regulation of the hypoxic gene program

Molecular and Cellular Biology

Volumn 34, Issue 16, 2014, Pages 2996-3012

  Baresic, Mario ^a   Salatino, Silvia ^a,b   Kupr, Barbara ^a   van Nimwegen, Erik ^a,b   Handschin, Christoph ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CELL NUCLEUS RECEPTOR; ESTROGEN RELATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; TRANSCRIPTION FACTOR AP 1;

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; ENDURANCE TRAINING; GENE EXPRESSION; GENE REGULATORY NETWORK; HYPOXIA; MALE; MOLECULAR MODEL; MOUSE; MUSCLE CELL; MUSCLE FUNCTION; MYOTUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SKELETAL MUSCLE; TRANSCRIPTION REGULATION; TREADMILL EXERCISE;

ANIMALS; BINDING SITES; CELL HYPOXIA; CELL LINE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; MICE; MUSCLE FIBERS, SKELETAL; PPAR GAMMA; PRINCIPAL COMPONENT ANALYSIS; RECEPTORS, ESTROGEN; RNA INTERFERENCE; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS;

EID: 84904479648     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01710-13     Document Type: Article

References (48)

1. Handschin C, Spiegelman BM. 2008. The role of exercise and PGC1alpha in inflammation and chronic disease. Nature 454:463-469. http://dx.doi.org/10.1038/nature07206.
2. Pedersen BK, Febbraio MA. 2012. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat. Rev. Endocrinol. 8:457-465. http://dx.doi.org/10.1038/nrendo.2012.49.
3. Handschin C. 2010. Regulation of skeletal muscle cell plasticity by the peroxisome proliferator-activated receptor gamma coactivator 1alpha. J. Recept. Signal Transduct. Res. 30:376-384. http://dx.doi.org/10.3109/10799891003641074.
4. Handschin C, Spiegelman BM. 2006. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 27:728-735. http://dx.doi.org/10.1210/er.2006-0037.
5. Finck BN, Kelly DP. 2006. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 116:615-622. http://dx.doi.org/10.1172/JCI27794.
6. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM. 2002. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418:797-801. http://dx.doi.org/10.1038/nature00904.
7. Handschin C, Chin S, Li P, Liu F, Maratos-Flier E, Lebrasseur NK, Yan Z, Spiegelman BM. 2007. Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1alpha muscle-specific knock-out animals. J. Biol. Chem. 282:30014-30021. http://dx.doi.org/10.1074/jbc. M704817200.
8. Handschin C, Choi CS, Chin S, Kim S, Kawamori D, Kurpad AJ, Neubauer N, Hu J, Mootha VK, Kim YB, Kulkarni RN, Shulman GI, Spiegelman BM. 2007. Abnormal glucose homeostasis in skeletal musclespecific PGC-1alpha knockout mice reveals skeletal muscle-pancreatic beta cell crosstalk. J. Clin. Invest. 117:3463-3474. http://dx.doi.org/10.1172/JCI31785.
9. Lonard DM, O'Malley BW. 2006. The expanding cosmos of nuclear receptor coactivators. Cell 125:411-414. http://dx.doi.org/10.1016/j.cell.2006.04.021.
10. Lonard DM, O'Malley BW. 2007. Nuclear receptor coregulators: judges, juries, and executioners of cellular regulation. Mol. Cell 27:691-700. http://dx.doi.org/10.1016/j.molcel.2007.08.012.
11. Spiegelman BM, Heinrich R. 2004. Biological control through regulated transcriptional coactivators. Cell 119:157-167. http://dx.doi.org/10.1016/j.cell.2004.09.037.
12. Puigserver P, Adelmant G, Wu Z, Fan M, Xu J, O'Malley B, Spiegelman BM. 1999. Activation of PPARgamma coactivator-1 through transcription factor docking. Science 286:1368-1371. http://dx.doi.org/10.1126/science.286.5443.1368.
13. Wallberg AE, Yamamura S, Malik S, Spiegelman BM, Roeder RG. 2003. Coordination of p300-mediated chromatin remodeling and TRAP/mediator function through coactivator PGC-1alpha. Mol. Cell 12:1137-1149. http://dx.doi.org/10.1016/S1097-2765(03)00391-5.
14. Li S, Liu C, Li N, Hao T, Han T, Hill DE, Vidal M, Lin JD. 2008. Genome-wide coactivation analysis of PGC-1alpha identifies BAF60a as a regulator of hepatic lipid metabolism. Cell Metab. 8:105-117. http://dx.doi.org/10.1016/j.cmet.2008.06.013.
15. Lin J, Handschin C, Spiegelman BM. 2005. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1:361-370. http://dx.doi.org/10.1016/j.cmet.2005.05.004.
16. Handschin C. 2009. The biology of PGC-1alpha and its therapeutic potential. Trends Pharmacol. Sci. 30:322-329. http://dx.doi.org/10.1016/j.tips.2009.03.006.
17. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. http://dx.doi.org/10.1186/gb-2009-10-3-r25.
18. Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302:205-217. http://dx.doi.org/10.1006/jmbi.2000.4042.
19. Perez-Schindler J, Summermatter S, Santos G, Zorzato F, Handschin C. 2013. The transcriptional coactivator PGC-1alpha is dispensable for chronic overload-induced skeletal muscle hypertrophy and metabolic remodeling. Proc. Natl. Acad. Sci. U. S. A. 110:20314-20319. http://dx.doi.org/10.1073/pnas.1312039110.
20. Arnold P, Erb I, Pachkov M, Molina N, van Nimwegen E. 2012. MotEvo: integrated Bayesian probabilistic methods for inferring regulatory sites and motifs on multiple alignments of DNA sequences. Bioinformatics 28:487-494. http://dx.doi.org/10.1093/bioinformatics/btr695.
21. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80. http://dx.doi.org/10.1186/gb-2004-5-10-r80.
22. R Development Core Team. 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
23. Al-Shahrour F, Diaz-Uriarte R, Dopazo J. 2004. FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 20:578-580. http://dx.doi.org/10.1093/bioinformatics/btg455.
24. Suzuki H, Forrest AR, van Nimwegen E, Daub CO, Balwierz PJ, Irvine KM, Lassmann T, Ravasi T, Hasegawa Y, de Hoon MJ, Katayama S, Schroder K, Carninci P, Tomaru Y, Kanamori-Katayama M, Kubosaki A, Akalin A, Ando Y, Arner E, Asada M, Asahara H, Bailey T, Bajic VB, Bauer D, Beckhouse AG, Bertin N, Bjorkegren J, Brombacher F, Bulger E, Chalk AM, Chiba J, Cloonan N, Dawe A, Dostie J, Engstrom PG, Essack M, Faulkner GJ, Fink JL, Fredman D, Fujimori K, Furuno M, Gojobori T, Gough J, Grimmond SM, Gustafsson M, Hashimoto M, Hashimoto T, Hatakeyama M, Heinzel S, Hide W, Hofmann O, Hornquist M, Huminiecki L, et al. 2009. The transcriptional network that controls growth arrest and differentiation in a human myeloid leukemia cell line. Nat. Genet. 41:553-562. http://dx.doi.org/10.1038/ng.375.
25. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, Weinstock GM, Wilson RK, Gibbs RA, Kent WJ, Miller W, Haussler D. 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15:1034-1050. http://dx.doi.org/10.1101/gr.3715005.
26. Siddharthan R, Siggia ED, van Nimwegen E. 2005. PhyloGibbs: a Gibbs sampling motif finder that incorporates phylogeny. PLoS Comput. Biol. 1:e67. http://dx.doi.org/10.1371/journal.pcbi.0010067.
27. Mahony S, Benos PV. 2007. STAMP: a web tool for exploring DNAbinding motif similarities. Nucleic Acids Res. 35:W253-W258. http://dx.doi.org/10.1093/nar/gkm272.
28. Summermatter S, Santos G, Perez-Schindler J, Handschin C. 2013. Skeletal muscle PGC-1alpha controls whole-body lactate homeostasis through estrogen-related receptor alpha-dependent activation of LDH B and repression of LDH A. Proc. Natl. Acad. Sci. U. S. A. 110:8738-8743. http://dx.doi.org/10.1073/pnas.1212976110.
29. Summermatter S, Shui G, Maag D, Santos G, Wenk MR, Handschin C. 2013. PGC-1alpha improves glucose homeostasis in skeletal muscle in an activity-dependent manner. Diabetes 62:85-95. http://dx.doi.org/10.2337/db12-0291.
30. Huss JM, Torra IP, Staels B, Giguere V, Kelly DP. 2004. Estrogenrelated receptor alpha directs peroxisome proliferator-activated receptor alpha signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell. Biol. 24:9079-9091. http://dx.doi.org/10.1128/MCB.24.20.9079-9091.2004.
31. Mootha VK, Handschin C, Arlow D, Xie X, St. Pierre J, Sihag S, Yang W, Altshuler D, Puigserver P, Patterson N, Willy PJ, Schulman IG, Heyman RA, Lander ES, Spiegelman BM. 2004. Erralpha and Gabpa/b specify PGC-1alpha-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. U. S. A. 101: 6570-6575. http://dx.doi.org/10.1073/pnas.0401401101.
32. Schreiber SN, Emter R, Hock MB, Knutti D, Cardenas J, Podvinec M, Oakeley EJ, Kralli A. 2004. The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)- induced mitochondrial biogenesis. Proc. Natl. Acad. Sci. U. S. A. 101: 6472-6477. http://dx.doi.org/10.1073/pnas.0308686101.
33. Eisele PS, Salatino S, Sobek J, Hottiger MO, Handschin C. 2013. The peroxisome proliferator-activated receptor gamma coactivator 1alpha/beta (PGC-1) coactivators repress the transcriptional activity of NFkappaB in skeletal muscle cells. J. Biol. Chem. 288:2246-2260. http://dx.doi.org/10.1074/jbc. M112.375253.
34. Mangelsdorf DJ, Evans RM. 1995. The RXR heterodimers and orphan receptors. Cell 83:841-850. http://dx.doi.org/10.1016/0092-8674(95)90200-7.
35. Hai T, Curran T. 1991. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc. Natl. Acad. Sci. U. S. A. 88:3720-3724. http://dx.doi.org/10.1073/pnas.88.9.3720.
36. Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM, Baek KH, Rosenzweig A, Spiegelman BM. 2008. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 451:1008-1012. http://dx.doi.org/10.1038/nature06613.
37. Ma Z, Swigut T, Valouev A, Rada-Iglesias A, Wysocka J. 2011. Sequence- specific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat. Struct. Mol. Biol. 18:120-127. http://dx.doi.org/10.1038/nsmb.2000.
38. Qian J, Chen S, Huang Y, Shi X, Liu C. 2013. PGC-1alpha regulates hepatic hepcidin expression and iron homeostasis in response to inflammation. Mol. Endocrinol. 27:683-692. http://dx.doi.org/10.1210/me.2012-1345.
39. Jang WG, Kim EJ, Park KG, Park YB, Choi HS, Kim HJ, Kim YD, Kim KS, Lee KU, Lee IK. 2007. Glucocorticoid receptor mediated repression of human insulin gene expression is regulated by PGC-1alpha. Biochem. Biophys. Res. Commun. 352:716-721. http://dx.doi.org/10.1016/j.bbrc.2006.11.074.
40. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, Spiegelman BM. 2006. PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc. Natl. Acad. Sci. U. S. A. 103:16260-16265. http://dx.doi.org/10.1073/pnas.0607795103.
41. Shaulian E, Karin M. 2002. AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4:E131-E136. http://dx.doi.org/10.1038/ncb0502-e131.
42. Curran T, Franza BR, Jr. 1988. Fos and Jun: the AP-1 connection. Cell 55:395-397. http://dx.doi.org/10.1016/0092-8674(88)90024-4.
43. Cam H, Easton JB, High A, Houghton PJ. 2010. mTORC1 signaling under hypoxic conditions is controlled by ATM-dependent phosphorylation of HIF-1alpha. Mol. Cell 40:509-520. http://dx.doi.org/10.1016/j.molcel.2010.10.030.
44. Majmundar AJ, Wong WJ, Simon MC. 2010. Hypoxia-inducible factors and the response to hypoxic stress. Mol. Cell 40:294-309. http://dx.doi.org/10.1016/j.molcel.2010.09.022.
45. Wagner PD. 2001. Skeletal muscle angiogenesis. A possible role for hypoxia. Adv. Exp. Med. Biol. 502:21-38. http://dx.doi.org/10.1007/978-1-4757-3401-0_4.
46. Pino E, Wang H, McDonald ME, Qiang L, Farmer SR. 2012. Roles for peroxisome proliferator-activated receptor gamma (PPARgamma) and PPARgamma coactivators 1alpha and 1beta in regulating response of white and brown adipocytes to hypoxia. J. Biol. Chem. 287:18351-18358. http://dx.doi.org/10.1074/jbc. M112.350918.
47. Zhao J, Li L, Pei Z, Li C, Wei H, Zhang B, Peng Y, Wang Y, Tao Y, Huang R. 2012. Peroxisome proliferator activated receptor (PPAR)- gamma co-activator 1-alpha and hypoxia induced factor-1alpha mediate neuro- and vascular protection by hypoxic preconditioning in vitro. Brain Res. 1447:1-8. http://dx.doi.org/10.1016/j.brainres.2012.01.059.
48. Charos AE, Reed BD, Raha D, Szekely AM, Weissman SM, Snyder M. 2012. A highly integrated and complex PPARGC1A transcription factor binding network in HepG2 cells. Genome Res. 22:1668-1679. http://dx.doi.org/10.1101/gr.127761.111.