Sp1 Transcription Factor and GATA1 cis-Acting Elements Modulate Testis-Specific Expression of Mouse Cyclin A1

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Panigrahi, Sunil K ^a   Vasileva, Ana ^a   Wolgemuth, Debra J ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; PREGNANCY SPECIFIC BETA1 GLYCOPROTEIN; TRANSCRIPTION FACTOR GATA 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CCNA1 GENE; CELL DIFFERENTIATION; CELL LINEAGE; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE REPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; GERM CELL; HUMAN; HUMAN CELL; MALE; METHYLATION; MOUSE; NONHUMAN; PACHYTENE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELLS, CULTURED; CONSENSUS SEQUENCE; CPG ISLANDS; CYCLIN A1; GATA1 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; GERM CELLS; MALE; MICE; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; PROMOTER REGIONS, GENETIC; SP1 TRANSCRIPTION FACTOR; TESTIS;

EID: 84868112723     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047862     Document Type: Article

References (65)

1. Murray AW, (2004) Recycling the cell cycle: cyclins revisited. Cell 116: 221-234.
2. Sweeney C, Murphy M, Kubelka M, Ravnik SE, Hawkins CF, et al. (1996) A distinct cyclin A is expressed in germ cells in the mouse. Development 122: 53-64.
3. Pines J, Hunter T, (1990) Human cyclin A is adenovirus E1A-associated protein p60 and behaves differently from cyclin B. Nature. 346: 760-763.
4. Wang J, Chenivesse X, Henglein B, Brechot C, (1990) Hepatitis B virus integration in a cyclin A gene in a hepatocellular carcinoma. Nature 343: 555-557.
5. Ravnik SE, Wolgemuth DJ, (1996) The developmentally restricted pattern of expression in the male germ line of a murine cyclin A, cyclin A2, suggests roles in both mitotic and meiotic cell cycles. Dev Biol 173: 69-78.
6. Yang R, Morosetti R, Koeffler HP, (1997) Characterization of a second human cyclin A that is highly expressed in testis and in several leukemic cell lines. Cancer Res 57: 913-920.
7. Hochegger H, Takeda S, Hunt T, (2008) Cyclin-dependent kinases and cell-cycle transitions: does one fit all? Nat Rev Mol Cell Biol 9: 910-916.
8. Yam CH, Fung TK, Poon RY, (2002) Cyclin A in cell cycle control and cancer. Cell Mol Life Sci 59: 1317-1326.
9. Joshi AR, Jobanputra V, Lele KM, Wolgemuth DJ, (2009) Distinct properties of cyclin-dependent kinase complexes containing cyclin A1 and cyclin A2. Biochem Biophys Res Commun 378: 595-599.
10. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P, et al. (1998) Cyclin A1 is required for meiosis in the male mouse. Nat Genet 20: 377-380.
11. Ge RS, Hardy MP, (1997) Decreased cyclin A2 and increased cyclin G1 levels coincide with loss of proliferative capacity in rat Leydig cells during pubertal development. Endocrinology 138: 3719-3726.
12. Ravnik SE, Wolgemuth DJ, (1999) Regulation of meiosis during mammalian spermatogenesis: the A-type cyclins and their associated cyclin-dependent kinases are differentially expressed in the germ-cell lineage. Dev Biol 207: 408-418.
13. Nickerson HD, Joshi A, Wolgemuth DJ, (2007) Cyclin A1-deficient mice lack histone H3 serine 10 phosphorylation and exhibit altered aurora B dynamics in late prophase of male meiosis. Dev Biol 306: 725-735.
14. Murphy M, Stinnakre MG, Senamaud-Beaufort C, Winston NJ, Sweeney C, et al. (1997) Delayed early embryonic lethality following disruption of the murine cyclin A2 gene. Nat Genet 15: 83-86.
15. Kalaszczynska I, Geng Y, Iino T, Mizuno S, Choi Y, et al. (2009) Cyclin A is redundant in fibroblasts but essential in hematopoietic and embryonic stem cells. Cell 138: 352-365.
16. Lele KM, Wolgemuth DJ, (2004) Distinct regions of the mouse cyclin A1 gene, Ccna1, confer male germ-cell specific expression and enhancer function. Biol Reprod 71: 1340-1347.
17. Muller-Tidow C, Readhead C, Cohen AH, Asotra K, Idos G, et al. (2003) Successive increases in human cyclin A1 promoter activity during spermatogenesis in transgenic mice. Int J Mol Med 11: 311-315.
18. Tascou S, Nayernia K, Samani A, Schmidtke J, Vogel T, et al. (2000) Immortalization of murine male germ cells at a discrete stage of differentiation by a novel directed promoter-based selection strategy. Biol Reprod 63: 1555-1561.
19. Wolgemuth DJ, Gizang-Ginsberg E, Engelmyer E, Gavin BJ, Ponzetto C, (1985) Separation of mouse testis cells on a Celsep (TM) apparatus and their usefulness as a source of high molecular weight DNA or RNA. Gamete Res 12: 1-10.
20. Hajkova P, el-Maarri O, Engemann S, Oswald J, Olek A, et al. (2002) DNA-methylation analysis by the bisulfite-assisted genomic sequencing method. Methods Mol Biol 200: 143-154.
21. Kumaki Y, Oda M, Okano M, (2008) QUMA: quantification tool for methylation analysis. Nucleic Acids Res 36: W170-175.
22. Shang E, Nickerson HD, Wen D, Wang X, Wolgemuth DJ, (2007) The first bromodomain of Brdt, a testis-specific member of the BET sub-family of double-bromodomain-containing proteins, is essential for male germ cell differentiation. Development 134: 3507-3515.
23. Muir T, Sadler-Riggleman I, Skinner MK, (2005) Role of the basic helix-loop-helix transcription factor, scleraxis, in the regulation of Sertoli cell function and differentiation. Mol Endocrinol 19: 2164-2174.
24. Wood MA, Mukherjee P, Toocheck CA, Walker WH, (2011) Upstream stimulatory factor induces nr5a1 and shbg gene expression during the onset of rat sertoli cell differentiation. Biol Reprod 85: 965-976.
25. Choi SJ, Oba T, Callander NS, Jelinek DF, Roodman GD, (2003) AML-1A and AML-1B regulation of MIP-1alpha expression in multiple myeloma. Blood 101: 3778-3783.
26. Wu S, Hu YC, Liu H, Shi Y, (2009) Loss of YY1 impacts the heterochromatic state and meiotic double-strand breaks during mouse spermatogenesis. Mol Cell Biol 29: 6245-6256.
27. Black AR, Black JD, Azizkhan-Clifford J, (2001) Sp1 and kruppel-like factor family of transcription factors in cell growth regulation and cancer. J Cell Physiol 188: 143-160.
28. Wechsler J, Greene M, McDevitt MA, Anastasi J, Karp JE, et al. (2002) Acquired mutations in GATA1 in the megakaryoblastic leukemia of Down syndrome. Nat Genet 32: 148-152.
29. Wong EY, Lin J, Forget BG, Bodine DM, Gallagher PG, (2004) Sequences downstream of the erythroid promoter are required for high level expression of the human alpha-spectrin gene. J Biol Chem 279: 55024-55033.
30. Yu M, Riva L, Xie H, Schindler Y, Moran TB, et al. (2009) Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol Cell 36: 682-695.
31. Ketola I, Anttonen M, Vaskivuo T, Tapanainen JS, Toppari J, et al. (2002) Developmental expression and spermatogenic stage specificity of transcription factors GATA-1 and GATA-4 and their cofactors FOG-1 and FOG-2 in the mouse testis. Eur J Endocrinol 147: 397-406.
32. Qamar I, Park E, Gong EY, Lee HJ, Lee K, (2009) ARR19 (androgen receptor corepressor of 19 kDa), an antisteroidogenic factor, is regulated by GATA-1 in testicular Leydig cells. J Biol Chem 284: 18021-18032.
33. Ma W, Horvath GC, Kistler MK, Kistler WS, (2008) Expression patterns of SP1 and SP3 during mouse spermatogenesis: SP1 down-regulation correlates with two successive promoter changes and translationally compromised transcripts. Biol Reprod 79: 289-300.
34. Marban C, Suzanne S, Dequiedt F, de Walque S, Redel L, et al. (2007) Recruitment of chromatin-modifying enzymes by CTIP2 promotes HIV-1 transcriptional silencing. EMBO J 26: 412-423.
35. Horak CE, Mahajan MC, Luscombe NM, Gerstein M, Weissman SM, et al. (2002) GATA-1 binding sites mapped in the beta-globin locus by using mammalian chIp-chip analysis. Proc Natl Acad Sci U S A 99: 2924-2929.
36. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, et al. (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39: 457-466.
37. Pinheiro A, Faustino I, Silva MJ, Silva J, Sa R, et al. (2010) Human testis-specific PDHA2 gene: methylation status of a CpG island in the open reading frame correlates with transcriptional activity. Mol Genet Metab 99: 425-430.
38. Pohlers M, Truss M, Frede U, Scholz A, Strehle M, et al. (2005) A role for E2F6 in the restriction of male-germ-cell-specific gene expression. Curr Biol 15: 1051-1057.
39. Xie W, Han S, Khan M, DeJong J, (2002) Regulation of ALF gene expression in somatic and male germ line tissues involves partial and site-specific patterns of methylation. J Biol Chem 277: 17765-17774.
40. Pan B, Chao H, Chen B, Zhang L, Li L, et al. (2011) DNA methylation of germ cell-specific basic helix-loop-helix (HLH) transcription factors, Sohlh2 and Figl{alpha} during gametogenesis. Mol Hum Reprod.
41. Maatouk DM, Kellam LD, Mann MR, Lei H, Li E, et al. (2006) DNA methylation is a primary mechanism for silencing postmigratory primordial germ cell genes in both germ cell and somatic cell lineages. Development 133: 3411-3418.
42. Ordway JM, Bedell JA, Citek RW, Nunberg A, Garrido A, et al. (2006) Comprehensive DNA methylation profiling in a human cancer genome identifies novel epigenetic targets. Carcinogenesis 27: 2409-2423.
43. Kumar AP, Butler AP, (1997) Transcription factor Sp3 antagonizes activation of the ornithine decarboxylase promoter by Sp1. Nucleic Acids Res 25: 2012-2019.
44. Clare SE, Fantz DA, Kistler WS, Kistler MK, (1997) The testis-specific histone H1t gene is strongly repressed by a G/C-rich region just downstream of the TATA Box. J Biol Chem 272: 33028-33036.
45. Zakeri ZF, Wolgemuth DJ, Hunt CR, (1988) Identification and sequence analysis of a new member of the mouse HSP70 gene family and characterization of its unique cellular and developmental pattern of expression in the male germ line. Mol Cell Biol 8: 2925-2932.
46. Gebara MM, McCarrey JR, (1992) Protein-DNA interactions associated with the onset of testis-specific expression of the mammalian Pgk-2 gene. Mol Cell Biol 12: 1422-1431.
47. Iannello RC, Kola I, Dahl HH, (1993) Temporal and tissue-specific interactions involving novel transcription factors and the proximal promoter of the mouse Pdha-2 gene. J Biol Chem 268: 22581-22590.
48. Bonny C, Cooker LA, Goldberg E, (1998) Deoxyribonucleic acid-protein interactions and expression of the human testis-specific lactate dehydrogenase promoter: transcription factor Sp1 plays a major role. Biol Reprod 58: 754-759.
49. Esteller M, (2007) Epigenetic gene silencing in cancer: the DNA hypermethylome. Hum Mol Genet 16 Spec No 1: R50-59.
50. Reik W, Dean W, Walter J, (2001) Epigenetic reprogramming in mammalian development. Science 293: 1089-1093.
51. Hoivik EA, Aumo L, Aesoy R, Lillefosse H, Lewis AE, et al. (2008) Deoxyribonucleic acid methylation controls cell type-specific expression of steroidogenic factor 1. Endocrinology 149: 5599-5609.
52. Brower JV, Lim CH, Han C, Hankowski KE, Hamazaki T, et al. (2009) Differential CpG island methylation of murine adenine nucleotide translocase genes. Biochim Biophys Acta 1789: 198-203.
53. Wolfe SA, Grimes SR, (2003) Transcriptional repression of the testis-specific histone H1t gene mediated by an element upstream of the H1/AC box. Gene 308: 129-138.
54. Grabarek Z, Tan RY, Wang J, Tao T, Gergely J, (1990) Inhibition of mutant troponin C activity by an intra-domain disulphide bond. Nature 345: 132-135.
55. Deng HX, Klein CJ, Yan J, Shi Y, Wu Y, et al. (2010) Scapuloperoneal spinal muscular atrophy and CMT2C are allelic disorders caused by alterations in TRPV4. Nat Genet 42: 165-169.
56. Gao HB, Ge RS, Lakshmi V, Marandici A, Hardy MP, (1997) Hormonal regulation of oxidative and reductive activities of 11 beta-hydroxysteroid dehydrogenase in rat Leydig cells. Endocrinology 138: 156-161.
57. Liao C, Li SQ, Wang X, Muhlrad S, Bjartell A, et al. (2004) Elevated levels and distinct patterns of expression of A-type cyclins and their associated cyclin-dependent kinases in male germ cell tumors. Int J Cancer 108: 654-664.
58. Muller C, Yang R, Beck-von-Peccoz L, Idos G, Verbeek W, et al. (1999) Cloning of the cyclin A1 genomic structure and characterization of the promoter region. GC boxes are essential for cell cycle-regulated transcription of the cyclin A1 gene. J Biol Chem 274: 11220-11228.
59. Muller C, Readhead C, Diederichs S, Idos G, Yang R, et al. (2000) Methylation of the cyclin A1 promoter correlates with gene silencing in somatic cell lines, while tissue-specific expression of cyclin A1 is methylation independent. Mol Cell Biol 20: 3316-3329.
60. Yanatatsaneejit P, Mutirangura A, Kitkumthorn N, (2011) Human Papillomavirus's Physical State and Cyclin A1 Promoter Methylation in Cervical Cancer. Int J Gynecol Cancer 21: 902-906.
61. Kitkumthorn N, Yanatatsanajit P, Kiatpongsan S, Phokaew C, Triratanachat S, et al. (2006) Cyclin A1 promoter hypermethylation in human papillomavirus-associated cervical cancer. BMC Cancer 6: 55.
62. Suske G, (1999) The Sp-family of transcription factors. Gene 238: 291-300.
63. Bu Y, Gelman IH, (2007) v-Src-mediated down-regulation of SSeCKS metastasis suppressor gene promoter by the recruitment of HDAC1 into a USF1-Sp1-Sp3 complex. J Biol Chem 282: 26725-26739.
64. Lopez-Soto A, Folgueras AR, Seto E, Gonzalez S, (2009) HDAC3 represses the expression of NKG2D ligands ULBPs in epithelial tumour cells: potential implications for the immunosurveillance of cancer. Oncogene 28: 2370-2382.
65. Mottet D, Pirotte S, Lamour V, Hagedorn M, Javerzat S, et al. (2009) HDAC4 represses p21(WAF1/Cip1) expression in human cancer cells through a Sp1-dependent, p53-independent mechanism. Oncogene 28: 243-256.