A genome-wide analysis of open chromatin in human epididymis epithelial cells reveals candidate regulatory elements for genes coordinating epididymal function

Biology of Reproduction

Volumn 89, Issue 4, 2013, Pages

  Bischof, Jared M ^a   Gillen, Austin E ^a   Song, Lingyun ^b   Gosalia, Nehal ^a   London, Darin ^b   Furey, Terrence S ^c   Crawford, Gregory E ^b   Harris, Ann ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b DUKE UNIVERSITY   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Epididymis epithelium; Male infertility; Sperm maturation; Transcriptional regulation

Indexed keywords

DEOXYRIBONUCLEASE I;

ARTICLE; CHROMATIN; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR GENE; EPIDIDYMIS; EPITHELIUM CELL; GENE; GENE EXPRESSION; GENOME ANALYSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; REGULATORY SEQUENCE;

EPIDIDYMIS EPITHELIUM; MALE INFERTILITY; SPERM MATURATION; TRANSCRIPTIONAL REGULATION;

CELLS, CULTURED; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME MAPPING; COMPUTATIONAL BIOLOGY; DNA, INTERGENIC; EPIDIDYMIS; EPITHELIAL CELLS; EXPERT SYSTEMS; FETUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME-WIDE ASSOCIATION STUDY; HUMANS; INFERTILITY, MALE; MALE; NUCLEOSOMES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC; SPERMATOGENESIS;

EID: 84899823633     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.110403     Document Type: Article

References (39)

1. Kirchhoff C. Gene expression in the epididymis. Int Rev Cytol 1999; 188: 133-202.
2. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, Kuehn MS, Taylor CM, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007; 447:799-816.
3. Boyle AP, Davis S, Shulha HP, Meltzer P, Margulies EH, Weng Z, Furey TS, Crawford GE. High-resolution mapping and characterization of open chromatin across the genome. Cell 2008; 132:311-322.
4. Harris A, Coleman L. Ductal epithelial cells cultured from human foetal epididymis and vas deferens: relevance to sterility in cystic fibrosis. J Cell Sci 1989; 92(pt 4):687-690.
5. Harris A, Chalkley G, Goodman S, Coleman L. Expression of the cystic fibrosis gene in human development. Development 1991; 113:305-310.
6. Ott CJ, Blackledge NP, Kerschner JL, Leir SH, Crawford GE, Cotton CU, Harris A. Intronic enhancers coordinate epithelial-specific looping of the active CFTR locus. Proc Natl Acad Sci U S A 2009; 106:19934-19939.
7. Song L, Zhang Z, Grasfeder LL, Boyle AP, Giresi PG, Lee BK, Sheffield NC, Graf S, Huss M, Keefe D, Liu Z, London D, et al. Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res 2011; 21:1757-1767.
8. Boyle AP, Guinney J, Crawford GE, Furey TS. F-Seq: a feature density estimator for high-throughput sequence tags. Bioinformatics 2008; 24: 2537-2538.
9. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4:44-57.
10. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009; 37:1-13.
11. Frith MC, Fu Y, Yu L, Chen JF, Hansen U, Weng Z. Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res 2004; 32:1372-1381.
12. Bryne JC, Valen E, Tang MH, Marstrand T, Winther O, da Piedade I, Krogh A, Lenhard B, Sandelin A. JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic Acids Res 2008; 36:D102-D106.
13. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, Barre-Dirrie A, Reuter I, Chekmenev D, Krull M, Hornischer K, Voss N, Stegmaier P, et al. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 2006; 34:D108-110.
14. Yigit E, Bischof JM, Zhang Z, Ott CJ, Kerschner JL, Leir SH, Buitrago-Delgado E, Zhang Q, Wang JP, Widom J, Harris A. Nucleosome mapping across the CFTR locus identifies novel regulatory factors. Nucleic Acids Res 2013; 41:2857-2868.
15. Dennis G. Jr., Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003; 4:P3.
16. Rajan N, Sung WK, Goodman DS. Localization of cellular retinol-binding protein mRNA in rat testis and epididymis and its stage-dependent expression during the cycle of the seminiferous epithelium. Biol Reprod 1990; 43:835-842.
17. Chinoy NJ, Rao MV, Kumar RA. Role of ascorbic acid in metabolism of rat testis and epididymis in relation to the onset of puberty. J Biosci 1984; 6:857-863.
18. Splinter E, Heath H, Kooren J, Palstra RJ, Klous P, Grosveld F, Galjart N, de Laat W. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev 2006; 20: 2349-2354.
19. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, Cobb BS, Yokomori K, et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 2008; 132:422-433.
20. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 2008; 451:796-801.
21. Lapinskas EJ, Palmer J, Ricardo S, Hertzog PJ, Hammacher A, Pritchard MA. A major site of expression of the ets transcription factor Elf5 is epithelia of exocrine glands. Histochem Cell Biol 2004; 122:521-526.
22. Kuschert S, Rowitch DH, Haenig B, McMahon AP, Kispert A. Characterization of Pax-2 regulatory sequences that direct transgene expression in the Wolffian duct and its derivatives. Dev Biol 2001; 229: 128-140.
23. O'Hara L, Welsh M, Saunders PT, Smith LB. Androgen receptor expression in the caput epididymal epithelium is essential for development of the initial segment and epididymal spermatozoa transit. Endocrinology 2011; 152:718-729.
24. De Santa Barbara P, Bonneaud N, Boizet B, Desclozeaux M, Moniot B, Sudbeck P, Scherer G, Poulat F, Berta P. Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol Cell Biol 1998; 18:6653-6665.
25. Zhang Z, Ott CJ, Lewandowska MA, Leir SH, Harris A. Molecular mechanisms controlling CFTR gene expression in the airway. J Cell Mol Med 2012; 16:1321-1330.
26. Kerschner JL, Harris A. Transcriptional networks driving enhancer function in the CFTR gene. Biochem J 2012; 446:203-212.
27. Blackledge NP, Ott CJ, Gillen AE, Harris A. An insulator element 30 to the CFTR gene binds CTCF and reveals an active chromatin hub in primary cells. Nucleic Acids Res 2009; 37:1086-1094.
28. Blackledge NP, Carter EJ, Evans JR, Lawson V, Rowntree RK, Harris A. CTCF mediates insulator function at the CFTR locus. Biochem J 2007; 408:267-275.
29. Zhang Z, Leir SH, Harris A. Immune mediators regulate CFTR expression through a bifunctional airway-selective enhancer. Mol Cell Biol 2013; 33: 2843-2853.
30. Bischof JM, Ott CJ, Leir SH, Gosalia N, Song L, London D, Furey TS, Cotton CU, Crawford GE, Harris A. A genome-wide analysis of open chromatin in human tracheal epithelial cells reveals novel candidate regulatory elements for lung function. Thorax 2012; 67:385-391.
31. Gerstein MB, Kundaje A, Hariharan M, Landt SG, Yan KK, Cheng C, Mu XJ, Khurana E, Rozowsky J, Alexander R, Min R, Alves P, et al. Architecture of the human regulatory network derived from ENCODE data. Nature 2012; 489:91-100.
32. Dehm SM, Tindall DJ. Alternatively spliced androgen receptor variants. EndocrRelat Cancer 2011; 18:R183-R196.
33. Gaulton KJ, Nammo T, Pasquali L, Simon JM, Giresi PG, Fogarty MP, Panhuis TM, Mieczkowski P, Secchi A, Bosco D, Berney T, Montanya E, et al. A map of open chromatin in human pancreatic islets. Nat Genet 2010; 42:255-259.
34. Coleman L, Harris A. Immortalization of male genital duct epithelium: an assay system for the cystic fibrosis gene. J Cell Sci 1991; 98(pt 1):85-89.
35. Chauvin TR, Griswold MD. Androgen-regulated genes in the murine epididymis. Biol Reprod 2004; 71:560-569.
36. Johnston DS, Jelinsky SA, Bang HJ, DiCandeloro P, Wilson E, Kopf GS, Turner TT. The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol Reprod 2005; 73: 404-413.
37. Jelinsky SA, Turner TT, Bang HJ, Finger JN, Solarz MK, Wilson E, Brown EL, Kopf GS, Johnston DS. The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides. Biol Reprod 2007; 76:561-570.
38. Bolton EC, So AY, Chaivorapol C, Haqq CM, Li H, Yamamoto KR. Celland gene-specific regulation of primary target genes by the androgen receptor. Genes Dev 2007; 21:2005-2017.
39. Kosova G, Scott NM, Niederberger C, Prins GS, Ober C. Genome-wide association study identifies candidate genes for male fertility traits in humans. Am J Hum Genet 2012; 90:950-961.