Genome-wide analysis of chromatin states reveals distinct mechanisms of sex-dependent gene regulation in male and female mouse liver

Molecular and Cellular Biology

Volumn 33, Issue 18, 2013, Pages 3594-3610

  Sugathan, Aarathi ^a   Waxman, David J ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; PROTEIN BCL 6; STAT5 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOINFORMATICS; CELL DIFFERENTIATION; CHROMATIN; CONSTITUTIVE HETEROCHROMATIN; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; GENE CONTROL; GENE EXPRESSION; GENETIC ANALYSIS; HIDDEN MARKOV MODEL; HIGH THROUGHPUT SEQUENCING; HUMAN GENOME; LIVER DEVELOPMENT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SEX DIFFERENCE;

ANIMALS; CHROMATIN; DEOXYRIBONUCLEASE I; DNA-BINDING PROTEINS; ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; GENES, REGULATOR; GENOME-WIDE ASSOCIATION STUDY; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HEPATOCYTE NUCLEAR FACTOR 3-BETA; HISTONES; LIVER; MALE; METHYLATION; MICE; MULTIGENE FAMILY; SEX CHARACTERISTICS; STAT5 TRANSCRIPTION FACTOR; TRANSCRIPTION INITIATION SITE;

EID: 84883547823     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00280-13     Document Type: Article

References (80)

1. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, Ku M, Durham T, Kellis M, Bernstein BE. 2011. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473:43-49.
2. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39:311-318.
3. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B. 2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108-112.
4. Dong X, Greven MC, Kundaje A, Djebali S, Brown JB, Cheng C, Gingeras TR, Gerstein M, Guigo R, Birney E, Weng Z. 2012. Modeling gene expression using chromatin features in various cellular contexts. Genome Biol. 13:R53. doi:10.1186/gb-2012-13-9-r53.
5. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, Garg K, John S, Sandstrom R, Bates D, Boatman L, Canfield TK, Diegel M, Dunn D, Ebersol AK, Frum T, Giste E, Johnson AK, Johnson EM, Kutyavin T,Lajoie B, Lee BK, Lee K, London D, Lotakis D, Neph S, Neri F, Nguyen ED, Qu H, Reynolds AP, Roach V, Safi A, Sanchez ME, Sanyal A, Shafer A, Simon JM, Song L, Vong S, Weaver M, Yan Y, Zhang Z, Lenhard B, Tewari M, Dorschner MO, Hansen RS, Navas PA, Stamatoyannopoulos G, Iyer VR, Lieb JD, Sunyaev SR, Akey JM, Sabo PJ, Kaul R, Furey TS, Dekker J, Crawford GE, Stamatoyannopoulos JA. 2012. The accessible chromatin landscape of the human genome. Nature 489:75-82.
6. Natarajan A, Yardimci GG, Sheffield NC, Crawford GE, Ohler U. 2012. Predicting cell-type-specific gene expression from regions of open chromatin. Genome Res. 22:1711-1722.
7. Arvey A, Agius P, Noble WS, Leslie C. 2012. Sequence and chromatin determinants of cell-type-specific transcription factor binding. Genome Res. 22:1723-1734.
8. He HH, Meyer CA, Chen MW, Jordan VC, Brown M, Liu XS. 2012. Differential DNase I hypersensitivity reveals factor-dependent chromatin dynamics. Genome Res. 22:1015-1025.
9. Kundaje A, Kyriazopoulou-Panagiotopoulou S, Libbrecht M, Smith CL, Raha D, Winters EE, Johnson SM, Snyder M, Batzoglou S, Sidow A. 2012. Ubiquitous heterogeneity and asymmetry of the chromatin environment at regulatory elements. Genome Res. 22:1735-1747.
10. Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, Greven MC, Pierce BG, Dong X, Kundaje A, Cheng Y, Rando OJ, Birney E, Myers RM, Noble WS, Snyder M, Weng Z. 2012. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 22:1798-1812.
11. Zaret KS, Carroll JS. 2011. Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25:2227-2241.
12. Friedman JR, Kaestner KH. 2006. The Foxa family of transcription factors in development and metabolism. Cell. Mol. Life Sci. 63:2317-2328.
13. Hoffman BG, Robertson G, Zavaglia B, Beach M, Cullum R, Lee S, Soukhatcheva G, Li L, Wederell ED, Thiessen N, Bilenky M, Cezard T, Tam A, Kamoh B, Birol I, Dai D, Zhao Y, Hirst M, Verchere CB, Helgason CD, Marra MA, Jones SJ, Hoodless PA. 2010. Locus cooccupancy, nucleosome positioning, and H3K4me1 regulate the functionality of FOXA2-, HNF4A-, and PDX1-bound loci in islets and liver. Genome Res. 20:1037-1051.
14. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38:576-589.
15. Cheng C, Alexander R, Min R, Leng J, Yip KY, Rozowsky J, Yan KK, Dong X, Djebali S, Ruan Y, Davis CA, Carninci P, Lassman T, Gingeras TR, Guigo R, Birney E, Weng Z, Snyder M, Gerstein M. 2012. Understanding transcriptional regulation by integrative analysis of transcription factor binding data. Genome Res. 22:1658-1667.
16. Garber M, Yosef N, Goren A, Raychowdhury R, Thielke A, Guttman M, Robinson J, Minie B, Chevrier N, Itzhaki Z, Blecher-Gonen R, Bornstein C, Amann-Zalcenstein D, Weiner A, Friedrich D, Meldrim J, Ram O, Cheng C, Gnirke A, Fisher S, Friedman N, Wong B, Bernstein BE, Nusbaum C, Hacohen N, Regev A, Amit I. 2012. A high-throughput chromatin immunoprecipitation approach reveals principles of dynamic gene regulation in mammals. Mol. Cell 47:810-822.
17. Rinn JL, Snyder M. 2005. Sexual dimorphism in mammalian gene expression. Trends Genet. 21:298-305.
18. Wauthier V, Sugathan A, Meyer RD, Dombkowski AA, Waxman DJ. 2010. Intrinsic sex differences in the early growth hormone responsiveness of sex-specific genes in mouse liver. Mol. Endocrinol. 24:667-678.
19. Wauthier V, Waxman DJ. 2008. Sex-specific early growth hormone response genes in rat liver. Mol. Endocrinol. 22:1962-1974.
20. Zhang Y, Klein K, Sugathan A, Nassery N, Dombkowski A, Zanger UM, Waxman DJ. 2011. Transcriptional profiling of human liver identifies sex-biased genes associated with polygenic dyslipidemia and coronary artery disease. PLoS One 6:e23506. doi:10.1371/journal.pone.0023506.
21. Waxman DJ, Holloway MG. 2009. Sex differences in the expression of hepatic drug metabolizing enzymes. Mol. Pharmacol. 76:215-228.
22. Scandlyn MJ, Stuart EC, Rosengren RJ. 2008. Sex-specific differences in CYP450 isoforms in humans. Expert Opin. Drug Metab. Toxicol. 4:413-424.
23. Schwartz JB. 2007. The current state of knowledge on age, sex, and their interactions on clinical pharmacology. Clin. Pharmacol. Ther. 82:87-96.
24. Yokoyama Y, Nimura Y, Nagino M, Bland KI, Chaudry IH. 2005. Current understanding of gender dimorphism in hepatic pathophysiology. J. Surg. Res. 128:147-156.
25. Baik M, Yu JH, Hennighausen L. 2011. Growth hormone-STAT5 regulation of growth, hepatocellular carcinoma, and liver metabolism. Ann. N. Y. Acad. Sci. 1229:29-37.
26. Ruggieri A, Barbati C, Malorni W. 2010. Cellular and molecular mechanisms involved in hepatocellular carcinoma gender disparity. Int. J. Cancer 127:499-504.
27. Choi HK, Waxman DJ. 2000. Plasma growth hormone pulse activation of hepatic JAK-STAT5 signaling: developmental regulation and role in malespecific liver gene expression. Endocrinology 141:3245-3255.
28. Choi HK, Waxman DJ. 1999. Growth hormone, but not prolactin, maintains, low-level activation of STAT5a and STAT5b in female rat liver. Endocrinology 140:5126-5135.
29. Lanning NJ, Carter-Su C. 2006. Recent advances in growth hormone signaling. Rev. Endocr Metab. Disord. 7:225-235.
30. Zhang Y, Laz EV, Waxman DJ. 2012. Dynamic, sex-differential STAT5 and BCL6 binding to sex-biased, growth hormone-regulated genes in adult mouse liver. Mol. Cell. Biol. 32:880-896.
31. Clodfelter KH, Holloway MG, Hodor P, Park SH, Ray WJ, Waxman DJ. 2006. Sex-dependent liver gene expression is extensive and largely dependent upon signal transducer and activator of transcription 5b (STAT5b): STAT5b-dependent activation of male genes and repression of female genes revealed by microarray analysis. Mol. Endocrinol. 20:1333-1351.
32. Meyer RD, Laz EV, Su T, Waxman DJ. 2009. Male-specific hepatic Bcl6: growth hormone-induced block of transcription elongation in females and binding to target genes inversely coordinated with STAT5. Mol. Endocrinol. 23:1914-1926.
33. Laz EV, Holloway MG, Chen CS, Waxman DJ. 2007. Characterization of three growth hormone-responsive transcription factors preferentially expressed in adult female liver. Endocrinology 148:3327-3337.
34. Conforto TL, Zhang Y, Sherman J, Waxman DJ. 2012. Impact of CUX2 on the female mouse liver transcriptome: activation of female-biased genes and repression of male-biased genes. Mol. Cell. Biol. 32:4611-4627.
35. Holloway MG, Laz EV, Waxman DJ. 2006. Codependence of growth hormone-responsive, sexually dimorphic hepatic gene expression on signal transducer and activator of transcription 5b and hepatic nuclear factor 4α. Mol. Endocrinol. 20:647-660.
36. Holloway MG, Miles GD, Dombkowski AA, Waxman DJ. 2008. Liverspecific hepatocyte nuclear factor-4α deficiency: greater impact on gene expression in male than in female mouse liver. Mol. Endocrinol. 22:1274-1286.
37. Delesque-Touchard N, Park SH, Waxman DJ. 2000. Synergistic action of hepatocyte nuclear factors 3 and 6 on CYP2C12 gene expression and suppression by growth hormone-activated STAT5b. Proposed model for female specific expression of CYP2C12 in adult rat liver. J. Biol. Chem. 275:34173-34182.
38. Lahuna O, Fernandez L, Karlsson H, Maiter D, Lemaigre FP, Rousseau GG, Gustafsson J, Mode A. 1997. Expression of hepatocyte nuclear factor 6 in rat liver is sex-dependent and regulated by growth hormone. Proc. Natl. Acad. Sci. U. S. A. 94:12309-12313.
39. Ling G, Sugathan A, Mazor T, Fraenkel E, Waxman DJ. 2010. Unbiased, genome-wide in vivo mapping of transcriptional regulatory elements reveals sex differences in chromatin structure associated with sex-specific liver gene expression. Mol. Cell. Biol. 30:5531-5544.
40. Chia DJ, Rotwein P. 2010. Defining the epigenetic actions of growth hormone: acute chromatin changes accompany GH-activated gene transcription. Mol. Endocrinol. 24:2038-2049.
41. Chai X, Zeng S, Xie W. 2013. Nuclear receptors PXR and CAR: implications for drug metabolism regulation, pharmacogenomics and beyond. Expert Opin. Drug Metab. Toxicol. 9:253-266.
42. Kakizaki S, Yamazaki Y, Takizawa D, Negishi M. 2008. New insights on the xenobiotic-sensing nuclear receptors in liver diseases-CAR and PXR. Curr. Drug Metab. 9:614-621.
43. Hernandez JP, Mota LC, Baldwin WS. 2009. Activation of CAR and PXR by dietary, environmental and occupational chemicals alters drug metabolism, intermediary metabolism, and cell proliferation. Curr. Pharmacogenomics Person Med. 7:81-105.
44. Li Z, Tuteja G, Schug J, Kaestner KH. 2012. Foxa1 and Foxa2 are essential for sexual dimorphism in liver cancer. Cell 148:72-83.
45. 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. doi:10.1186/gb-2009-10-3-r25.
46. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-basedanalysis of ChIP-Seq (MACS). Genome Biol. 9:R137. doi:10.1186/gb-2008 -9-9-r137.
47. Zang C, Schones DE, Zeng C, Cui K, Zhao K, Peng W. 2009. A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25:1952-1958.
48. Audic S, Claverie JM. 1997. The significance of digital gene expression profiles. Genome Res. 7:986-995.
49. Shao Z, Zhang Y, Yuan GC, Orkin SH, Waxman DJ. 2012. MAnorm: a robust model for quantitative comparison of ChIP-Seq data sets. Genome Biol. 13:R16. doi:10.1186/gb-2012-13-3-r16.
50. Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, Krobitsch S, Lehrach H, Soldatov A. 2009. Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res. 37:e123. doi:10.1093/nar/gkp596.
51. Eisen MB, Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95:14863-14868.
52. Saldanha AJ. 2004. Java Treeview-extensible visualization of microarray data. Bioinformatics 20:3246-3248.
53. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140.
54. Tojima H, Kakizaki S, Yamazaki Y, Takizawa D, Horiguchi N, Sato K, Mori M. 2012. Ligand dependent hepatic gene expression profiles of nuclear receptors CAR and PXR. Toxicol. Lett. 212:288-297.
55. Tian J, Huang H, Hoffman B, Liebermann DA, Ledda-Columbano GM, Columbano A, Locker J. 2011. Gadd45β is an inducible coactivator of transcription that facilitates rapid liver growth in mice. J. Clin. Invest. 121:4491-4502.
56. Sanderson LM, Boekschoten MV, Desvergne B, Muller M, Kersten S. 2010. Transcriptional profiling reveals divergent roles of PPARβ/δ and PPAR/in regulation of gene expression in mouse liver. Physiol. Genomics 41:42-52.
57. Boverhof DR, Burgoon LD, Tashiro C, Chittim B, Harkema JR, Jump DB, Zacharewski TR. 2005. Temporal and dose-dependent hepatic gene expression patterns in mice provide new insights into TCDD-mediated hepatotoxicity. Toxicol. Sci. 85:1048-1063.
58. Huang da W, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44-57.
59. Huang da W, Sherman BT, Lempicki RA. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37:1-13.
60. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 102:15545-15550.
61. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, Boyer LA, Young RA, Jaenisch R. 2010. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. U. S. A. 107:21931-21936.
62. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823-837.
63. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553-560.
64. Bernstein BE, Humphrey EL, Erlich RL, Schneider R, Bouman P, Liu JS, Kouzarides T, Schreiber SL. 2002. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl. Acad. Sci. U. S. A. 99:8695-8700.
65. Bannister AJ, Schneider R, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T. 2005. Spatial distribution of di-and tri-methyl lysine 36 of histone H3 at active genes. J. Biol. Chem. 280:17732-17736.
66. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. 2011. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470:279-283.
67. Rosenfeld JA, Wang Z, Schones DE, Zhao K, DeSalle R, Zhang MQ. 2009. Determination of enriched histone modifications in non-genic portions of the human genome. BMC Genomics 10:143. doi:10.1186/1471 -2164-10-143.
68. Silva J, Mak W, Zvetkova I, Appanah R, Nesterova TB, Webster Z, Peters AH, Jenuwein T, Otte AP, Brockdorff N. 2003. Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes. Dev. Cell 4:481-495.
69. Boggs BA, Cheung P, Heard E, Spector DL, Chinault AC, Allis CD. 2002. Differentially methylated forms of histone H3 show unique association patterns with inactive human X chromosomes. Nat. Genet. 30:73-76.
70. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315-326.
71. Waxman DJ. 1999. P450 gene induction by structurally diverse xenochemicals: central role of nuclear receptors CAR, PXR, and PPAR. Arch. Biochem. Biophys. 369:11-23.
72. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, Carroll JS, Liu XS, Brown M. 2008. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132:958-970.
73. Cirillo LA, Lin FR, Cuesta I, Friedman D, Jarnik M, Zaret KS. 2002. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol. Cell 9:279-289.
74. Song L, Zhang Z, Grasfeder LL, Boyle AP, Giresi PG, Lee BK, Sheffield NC, Graf S, Huss M, Keefe D, Liu Z, London D, McDaniell RM, Shibata Y, Showers KA, Simon JM, Vales T, Wang T, Winter D, Clarke ND, Birney E, Iyer VR, Crawford GE, Lieb JD, Furey TS. 2011. Open chromatin defined by DNase I and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res. 21:1757-1767.
75. Gebert CA, Park SH, Waxman DJ. 1999. Down-regulation of liver JAK2-STAT5b signaling by the female plasma pattern of continuous growth hormone stimulation. Mol. Endocrinol. 13:213-227.
76. Gebert CA, Park SH, Waxman DJ. 1999. Termination of growth hormone pulse-induced STAT5b signaling. Mol. Endocrinol. 13:38-56.
77. Zaret K. 1999. Developmental competence of the gut endoderm: genetic potentiation by GATA and HNF3/fork head proteins. Dev. Biol. 209:1-10.
78. Kang K, Robinson GW, Hennighausen L. 2013. Comprehensive metaanalysis of Signal Transducers and Activators of Transcription (STAT) genomic binding patterns discerns cell-specific cis-regulatory modules. BMC Genomics 14:4. doi:10.1186/1471-2164-14-4.
79. Li Z, Schug J, Tuteja G, White P, Kaestner KH. 2011. The nucleosome map of the mammalian liver. Nat. Struct. Mol. Biol. 18:742-746.
80. Conforto TL, Waxman DJ. 2012. Sex-specific mouse liver gene expression: genome-wide analysis of developmental changes from pre-pubertal period to young adulthood. Biol. Sex Differ. 3:9. doi:10.1186/2042-6410 -3-9.