DNA demethylation-dependent AR recruitment and GATA factors drive Rhox5 homeobox gene transcription in the epididymis

Molecular Endocrinology

Volumn 26, Issue 4, 2012, Pages 538-549

  Bhardwaj, Anjana ^b   Song, Hye Won ^a,b   Beildeck, Marcy ^a   Kerkhofs, Stefanie ^c   Castoro, Ryan ^b   Shanker, Sreenath ^b   de Gendt, Karel ^a   Suzuki, Kichiya ^d   Claessens, Frank ^c   Issa, Jean Pierre ^b   Orgebin Crist, Marie Claire ^d   Wilkinson, Miles F ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; CYTOSINE; GUANINE; HOMEODOMAIN PROTEIN; PHOSPHATE; REPRODUCTIVE HOMEOBOX GENE ON X CHROMOSOME 5; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; DNA RESPONSIVE ELEMENT; EPIDIDYMIS; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; MALE; MALE FERTILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SPERMATOZOON MATURATION; SPERMATOZOON MOTILITY; X CHROMOSOME;

ANDROGENS; ANIMALS; CELL LINE; DNA METHYLATION; EPIDIDYMIS; GATA TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; HOMEODOMAIN PROTEINS; LUCIFERASES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGAN SPECIFICITY; RECEPTORS, ANDROGEN; RESPONSE ELEMENTS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 84859152323     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2011-1059     Document Type: Article

References (54)

1. Bedford JM, Calvin H, Cooper GW 1973 The maturation of spermatozoa in the human epididymis. J Reprod Fertil Suppl 18:199-213
2. Olson GE, Orgebin-Crist MC 1982 Sperm surface changes during epididymal maturation. Ann NY Acad Sci 383:372-392
3. Hinton BT, Palladino MA, Rudolph D, Lan ZJ, Labus JC 1996 The role of the epididymis in the protection of spermatozoa. Curr Top Dev Biol 33:61-102
4. Gerena RL, Eguchi N, Urade Y, Killian GJ 2000 Stage and regionspecific localization of lipocalin-type prostaglandin D synthase in the adult murine testis and epididymis. J Androl 21:848-854
5. Douglass J, Garrett SH, Garrett JE 1991 Differential patterns of regulated gene expression in the adult rat epididymis. AnnNYAcad Sci 637:384-398
6. Cornwall GA, Hann SR 1995 Specialized gene expression in the epididymis. J Androl 16:379-383
7. Kirchhoff C 1999 Gene expression in the epididymis. Int Rev Cytol 188:133-202
8. Ezer N, Robaire B 2003 Gene expression is differentially regulated in the epididymis after orchidectomy. Endocrinology 144:975-988
9. Johnston DS, Jelinsky SA, Bang HJ, DiCandeloro P, Wilson E, Kopf GS, Turner TT 2005 The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol Reprod 73:404-413
10. Sipilä P, Pujianto DA, Shariatmadari R, Nikkilä J, Lehtoranta M, Huhtaniemi IT, Poutanen M 2006 Differential endocrine regulation of genes enriched in initial segment and distal caput of the mouse epididymis as revealed by genome-wide expression profiling. Biol Reprod 75:240-251
11. Suzuki K, Yu X, Chaurand P, Araki Y, Lareyre JJ, Caprioli RM, Orgebin-Crist MC, Matusik RJ 2007 Epididymis-specific lipocalin promoters. Asian J Androl 9:515-521
12. Kohane AC, Piñeiro L, Blaquier JA 1983 Androgen-controlled synthesis of specific proteins in the rat epididymis. Endocrinology 112: 1590-1596
13. Hall JC, Killian GJ 1989 Two-dimensional gel electrophoretic analysis of rat sperm membrane interaction with cauda epididymal fluid. J Androl 10:64-76
14. Orgebin-Crist MC 1996 Androgens and epididymal function. In: Bhasin DGH, Spieler JM, Swerdloff RS, Wang C, eds. Pharmacology, biology, and clinical applications of androgens. New York: Wiley-Liss, Inc.; 27-38
15. Chauvin TR, Griswold MD 2004 Androgen-regulated genes in the murine epididymis. Biol Reprod 71:560-569
16. Yu X, Suzuki K, Wang Y, Gupta A, Jin R, Orgebin-Crist MC, Matusik R 2006 The role of forkhead box A2 to restrict androgenregulated gene expression of lipocalin 5 in the mouse epididymis. Mol Endocrinol 20:2418-2431
17. Lareyre JJ, Thomas TZ, Zheng WL, Kasper S, Ong DE, Orgebin-Crist MC, Matusik RJ 1999 A 5-kilobase pair promoter fragment of the murine epididymal retinoic acid-binding protein gene drives the tissue-specific, cell-specific, and androgen-regulated expression of a foreign gene in the epididymis of transgenic mice. J Biol Chem 274:8282-8290
18. Maclean 2nd JA, Chen MA, Wayne CM, Bruce SR, Rao M, Meistrich ML, Macleod C, Wilkinson MF 2005 Rhox: a new homeobox gene cluster. Cell 120:369-382
19. Maclean 2nd JA, Wilkinson MF 2005 Gene regulation in spermatogenesis. Curr Top Dev Biol 71:131-197
20. Jackson M, Watt AJ, Gautier P, Gilchrist D, Driehaus J, Graham GJ, Keebler J, Prugnolle F, Awadalla P, Forrester LM 2006 A murine specific expansion of the Rhox cluster involved in embryonic stem cell biology is under natural selection. BMC Genomics 7:212
21. MacLean 2nd JA, Lorenzetti D, Hu Z, Salerno WJ, Miller J, Wilkinson MF 2006 Rhox homeobox gene cluster: recent duplication of three family members. Genesis 44:122-129
22. Morris L, Gordon J, Blackburn CC 2006 Identification of a tandem duplicated array in the Rhox α locus on mouse chromosome X. Mamm Genome 17:178-187
23. Wang X, Zhang J 2006 Remarkable expansions of an X-linked reproductive homeobox gene cluster in rodent evolution. Genomics 88:34-43
24. MacLean 2nd JA, Wilkinson MF 2010 The Rhox genes. Reproduction 140:195-213
25. Rao MK, Wayne CM, Wilkinson MF 2002 Pem homeobox gene regulatory sequences that direct androgen-dependent developmentally regulated gene expression in different subregions of the epididymis. J Biol Chem 277:48771-48778
26. Lindsey JS, Wilkinson MF 1996 An androgen-regulated homeobox gene expressed in rat testis and epididymis. Biol Reprod 55:975-983
27. Cosentino MJ, Cockett AT 1986 Structure and function of the epididymis. Urol Res 14:229-240
28. Krutskikh A, De Gendt K, Sharp V, Verhoeven G, Poutanen M, Huhtaniemi I 2011 Targeted inactivation of the androgen receptor gene in murine proximal epididymis causes epithelial hypotrophy and obstructive azoospermia. Endocrinology 152:689-696
29. O'Hara L, Welsh M, Saunders PT, Smith LB 2011 Androgen receptor expression in the caput epididymal epithelium is essential for development of the initial segment and epididymal spermatozoa transit. Endocrinology 152:718-729
30. Ezer NRB, ed. 2002 Androgenic regulation of the structure and functions of the epididymis. New York: Kluwer Academic/Plenum Publishers
31. Walsh CP, Bestor TH 1999 Cytosine methylation and mammalian development. Genes Dev 13:26-34
32. Maiti S, Doskow J, Li S, Nhim RP, Lindsey JS, Wilkinson MF 1996 The Pem homeobox gene. Androgen-dependent and-independent promoters and tissue-specific alternativeRNAsplicing. J Biol Chem 271:17536-17546
33. Araki Y, Suzuki K, Matusik RJ, Obinata M, Orgebin-Crist MC 2002 Immortalized epididymal cell lines from transgenic mice overexpressing temperature-sensitive simian virus 40 large T-antigen gene. J Androl 23:854-869
34. Bhardwaj A, Rao MK, Kaur R, Buttigieg MR, Wilkinson MF 2008 GATA factors and androgen receptor collaborate to transcriptionally activate the Rhox5 homeobox gene in Sertoli cells. Mol Cell Biol 28:2138-2153
35. Barbulescu K, Geserick C, Schüttke I, Schleuning WD, Haendler B 2001 New androgen response elements in the murine pem promoter mediate selective transactivation. Mol Endocrinol 15:1803-1816
36. Schauwaers K, De Gendt K, Saunders PT, Atanassova N, Haelens A, Callewaert L, Moehren U, Swinnen JV, Verhoeven G, Verrijdt G, Claessens F 2007 Loss of androgen receptor binding to selective androgen response elements causes a reproductive phenotype in a knockin mouse model. Proc Natl Acad Sci USA 104:4961-4966
37. Viger RS, Guittot SM, Anttonen M, Wilson DB, Heikinheimo M 2008 Role of the GATA family of transcription factors in endocrine development, function, and disease. Mol Endocrinol 22:781-798
38. Ko LJ, Engel JD 1993 DNA-binding specificities of the GATA transcription factor family. Mol Cell Biol 13:4011-4022
39. Merika M, Orkin SH 1993 DNA-binding specificity of GATA family transcription factors. Mol Cell Biol 13:3999-4010
40. Jiang Y, Tarzami S, Burch JB, Evans T 1998 Common role for each of the cGATA-4/5/6 genes in the regulation of cardiac morphogenesis. Dev Genet 22:263-277
41. Ballestar E, Esteller M 2002 The impact of chromatin in human cancer: linking DNA methylation to gene silencing. Carcinogenesis 23:1103-1109
42. Weber M, Hellmann I, Stadler MB, Ramos L, Pääbo S, Rebhan M, Schübeler D 2007 Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39:457-466
43. Lindsey JS, Wilkinson MF 1996 Pem: a testosterone-and LH-regulated homeobox gene expressed in mouse Sertoli cells and epididymis. Dev Biol 179:471-484
44. Orgebin-Crist MC 1969 Studies on the function of the epididymis. Biol Reprod 1(Suppl 1):155-175
45. Robaire B, Hermo, L 1988 Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. New York: Raven Press
46. Rao MK, Wayne CM, Meistrich ML, Wilkinson MF 2003 Pem homeobox gene promoter sequences that direct transcription in a Sertoli cell-specific, stage-specific, and androgen-dependent manner in the testis in vivo. Mol Endocrinol 17:223-233
47. Hu Z, Dandekar D, O'Shaughnessy PJ, De Gendt K, Verhoeven G, Wilkinson MF 2010 Androgen-induced Rhox homeobox genes modulate the expression of AR-regulated genes. Mol Endocrinol 24:60-75
48. Benoit J 1926 Recherches anatomiques, cytologiques et histophysiologiques sur les voies excretices du testicle chez les mammifères. Archs Anat Histol Embryol 5:173-412
49. Hamzeh M, Robaire B 2010 Identification of early response genes and pathway activated by androgens in the initial segment and caput regions of the regressed rat epididymis. Endocrinology 151: 4504-4514
50. Costello JF, Vertino PM 2002 Methylation matters: a new spin on maspin. Nat Genet 31:123-124
51. Wayne CM, Sutton K, Wilkinson MF 2002 Expression of the pem homeobox gene in Sertoli cells increases the frequency of adjacent germ cells with deoxyribonucleic acid strand breaks. Endocrinology 143:4875-4885
52. Rasmussen R 2001 Rapid cycle real-time PCR, methods and applications. In: Meuer S, Wittwer C, Nakagawara K, eds. Quantification on the Light Cycler. Heidelberg: Springer Press; 21-34
53. Herman JG, Graff JR, Myöhänen S, Nelkin BD, Baylin SB 1996 Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 93:9821-9826
54. MacLean 2nd JA, Hayashi K, Turner T, Wilkinson MF 14 March 2012 The Rhox5 homeobox gene regulates the region-specific expression of its paralogs in the epididymis. Biol Reprod 10.1095/ biolreprod.112.099184