YY1 acts as a transcriptional activator of Hoxa5 gene expression in mouse organogenesis

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Bérubé Simard, Félix Antoine ^a,b   Prudhomme, Christelle ^a,b   Jeannotte, Lucie ^a,b  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; TRANSCRIPTION FACTOR YY1; HOMEODOMAIN PROTEIN; HOXA5 PROTEIN, MOUSE; PHOSPHOPROTEIN; PROTEIN BINDING;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENHANCER REGION; GENE; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; HOXA4 GENE; HOXA5 GENE; IN VITRO STUDY; IN VIVO STUDY; MORPHOGENESIS; MOUSE; NONHUMAN; ORGANOGENESIS; PHENOTYPE; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE; ANIMAL; ANTIBODY SPECIFICITY; BINDING SITE; CHEMISTRY; DNA RESPONSIVE ELEMENT; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENE LOCUS; GENE ORDER; GENE TARGETING; GENETICS; LUNG; MESODERM; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROMOTER REGION; REGULATORY SEQUENCE;

ANIMALS; BASE SEQUENCE; BINDING SITES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE ORDER; GENE TARGETING; GENETIC LOCI; HOMEODOMAIN PROTEINS; LUNG; MESODERM; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; ORGANOGENESIS; PHENOTYPE; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; RESPONSE ELEMENTS; YY1 TRANSCRIPTION FACTOR;

EID: 84899079772     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093989     Document Type: Article

References (66)

1. Akam ME (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101: 1-22.
2. Pearson JC, Lemons D, McGinnis W (2005) Modulating Hox gene functions during animal body patterning. Nat Rev Genet 6: 893-904. (Pubitemid 41782157)
3. McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68: 283-302.
4. Wellik DM (2007) Hox patterning of the vertebrate axial skeleton. Dev Dyn 236: 2454-2463.
5. Jeannotte L, Lemieux M, Charron J, Poirier F, Robertson EJ (1993) Specification of axial identity in the mouse: role of the Hoxa-5 (Hox1.3) gene. Genes Dev 7: 2085-2096. (Pubitemid 23336136)
6. Aubin J, Lemieux M, Tremblay M, Bérard J, Jeannotte L (1997) Early postnatal lethality in Hoxa-5 mutant mice is attributable to respiratory tract defects. Dev Biol 192: 432-445. (Pubitemid 28066945)
7. Aubin J, Chailler P, Ménard D, Jeannotte L (1999) Loss of Hoxa5 gene function in mice perturbs intestinal maturation. Am J Physiol 277: C965-C973.
8. Aubin J, Déry U, Lemieux M, Chailler P, Jeannotte L (2002) Stomach regional specification requires Hoxa5-driven mesenchymal-epithelial signaling. Development 129: 4075-4087. (Pubitemid 35012493)
9. Meunier D, Aubin J, Jeannotte L (2003) Perturbed thyroid morphology and transient hypothyroidism symptoms in Hoxa5 mutant mice. Dev Dyn 227: 367-378. (Pubitemid 36828757)
10. Garin É, Lemieux M, Coulombe Y, Robinson GW, Jeannotte L (2006) Stromal Hoxa5 function controls the growth and differentiation of mammary alveolar epithelium. Dev Dyn 235: 1858-1871. (Pubitemid 43902344)
11. Gendronneau G, Boucherat O, Aubin J, Lemieux M, Jeannotte L (2012) The loss of Hoxa5 function causes estrous acyclicity and ovarian epithelila inclusion cysts. Endocrinology 153: 1484-1497.
12. Coulombe Y, Lemieux M, Moreau J, Aubin J, Joksimovic M, et al. (2010) Multiple promoters and alternative splicing: Hoxa5 transcriptional complexity in the mouse embryo. PLoS ONE 5(5): e10600. doi:10.1371/journal.pone.0010600.
13. Deschamps J, van Nes J (2005) Developmental regulation of the Hox genes during axial morphogenesis in the mouse. Development 132: 2931-2942. (Pubitemid 41086729)
14. Spitz F, Duboule D (2008) Global control regions and regulatory landscapes in vertebrate development and evolution. Adv Gent 61: 175-205.
15. Sharpe J, Nonchev S, Gould A, Whiting J, Krumlauf R (1998) Selectivity, sharing and competitive interactions in the regulation of Hoxb genes. EMBO J 17: 1788-1798. (Pubitemid 28119132)
16. Chambeyron S, Bickmore WA (2004) Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev 18: 1119-1130. (Pubitemid 38669033)
17. Parrish M, Nolte C, Krumlauf R (2009) Hox genes expression. In Squire L, editor. New Encyclopedia of Neuroscience. 4th ed, Academic Press. pp. 1221-1231.
18. Subramanian V, Meyer BI, Gruss P (1995) Disruption of the murine homeobox gene Cdx1 affects axial skeletal identities by altering the mesodermal expression domains of Hox genes. Cell 83: 641-653.
19. Charité J, de Graaff W, Consten D, Reijnen M J, Korving J, et al. (1998) Transducing positional information to the Hox genes: critical interaction of cdx gene products with position-sensitive regulatory elements. Development 125: 4349-4358. (Pubitemid 28564280)
20. Houle M, Prinos P, Iulianella A, Bouchard N, Lohnes D (2000) Retinoic acid regulation of Cdx1: an indirect mechanism for retinoids and vertebral specification. Mol Cell Biol 20: 6579-6586. (Pubitemid 30650242)
21. Pilon N, Oh K, Sylvestre JR, Savory JG, Lohnes D (2007) Wnt signaling is a key mediator of Cdx1 expression in vivo. Development 134: 2315-2323. (Pubitemid 47010020)
22. Dupé V, Davenne M, Brocard J, Dollé P, Mark M, et al. (1997) In vivo functional analysis of the Hoxa-1 39 retinoic acid response element (39RARE). Development 124: 399-410. (Pubitemid 27101674)
23. Oosterveen T, Niederreither K, Dollé P, Chambon P, Meijlink F, et al. (2003) Retinoids regulate the anterior expression boundaries of 5′ Hoxb genes in posterior hindbrain. EMBO J 22: 262-269. (Pubitemid 36119432)
24. Pöpperl H, Featherstone MS (1992) An autoregulatory element of the murine Hox-4.2 gene. EMBO J 11: 3673-3680.
25. Maconochie MK, Nonchev S, Studer M, Chan SK, Pöpperl H, et al. (1997) Cross-regulation in the mouse HoxB complex: the expression of Hoxb2 in rhombomere 4 is regulated by Hoxb1 . Genes Dev 15: 1885-1895. (Pubitemid 27315217)
26. Gilthorpe J, Vandromme M, Brend T, Gutman A, Summerbell D, et al. (2002) Spatially specific expression of Hoxb4 is dependent on the ubiquitous transcription factor NFY. Development 129: 3887-3899. (Pubitemid 34994018)
27. Meccia E, Bottero L, Felicetti F, Peschle C, Colombo MP, et al. (2003) HOXB7 expression is regulated by the transcription factors NF-Y, YY1, Sp1 and USF-1. Biochim Biophys Acta 1626: 1-9. (Pubitemid 36407450)
28. Kobrossy L, Rastegar M, Featherstone M (2006) Interplay between chromatin and trans-acting factors regulating the Hoxd4 promoter during neural differentiation. J Bio Chem 281: 25926-25939. (Pubitemid 44401798)
29. Woo CJ, Kharchenko PV, Daheron L, Park PJ, Kingston RE (2010) A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 140: 99-110.
30. Zakany J, Tuggle CK, Patel M, Nguyen-Huu MC (1988) Spatial regulation of homeobox gene fusions in the embryonic central nervous system of transgenic mice. Neuron 1: 679-691.
31. Larochelle C, Tremblay M, Bernier D, Aubin J, Jeannotte L (1999) Multiple cisacting regulatory regions are required for the restricted spatio-temporal Hoxa5 expression. Dev Dyn 214: 127-140. (Pubitemid 29070049)
32. Tabariès S, Lapointe J, Besch T, Carter M, Woollard J, et al. (2005) Cdx protein interaction with Hoxa5 regulatory sequences contributes to Hoxa5 regional expression along the axial skeleton. Mol Cell Biol 25: 1389-1401.
33. Moreau J, Jeannotte L (2002) Sequence analysis of Hoxa4-Hoxa5 intergenic region including shared regulatory elements. DNA Sequence 13: 203-209.
34. Herriges JC, Yi L, Hines EA, Harvey JF, Xu G, et al. (2012) Genome-scale study of transcription factor expression in the branching mouse lung. Dev Dyn 241: 1432-1453.
35. Boucherat O, Montaron S, Bérubé-Simard FA, Aubin J, Philippidou P, et al. (2013) Partial functional redundancy between Hoxa5 and Hoxb5 paralog genes during lung morphogenesis. Am J Physiol Lung Cell Mol Physiol 304: L817-L830.
36. Kothary R, Clapoff S, Darling,S, Perry MD, Moran LA, et al. (1989) Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 1989: 105: 707-714. (Pubitemid 19107069)
37. Hogan B, Beddington RS, Constantini F, Lacy E (1994) Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
38. Affar el B, Gay F, Shi Y, Liu H, Huarte M, et al. (2006) Essential dosage-dependent functions of the transcription factor yin yang 1 in late embryonic development and cell cycle progression. Mol Cell Biol 26: 3565-3581.
39. Yu K, Xu J, Liu Z, Sosic D, Shao J, et al. (2003) Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130: 3063-3074. (Pubitemid 36857252)
40. Jaffe L, Jeannotte L, Bikoff EK, Robertson EJ (1990) Analysis of beta 2-microglobulin gene expression in the developing mouse embryo and placenta. J Immunol 145: 3474-3482.
41. Boucherat O, Chakir J, Jeannotte L (2012) The loss of Hoxa5 function in mice promotes NOTCH-dependent goblet cell metaplasia in lung airways. Biology Open 1: 677-691.
42. Aparicio O, Geisberg JV, Sekinger E, Yang A, Moqtaderi Z, et al. (2005) Chromatin immunoprecipitation for determining the association of proteins with specific genomic sequences in vivo . Current Protocols in Molecular Biology 21.3.1-21.3.33.
43. Dony C, Gruss P (1987) Specific expression of the Hox1.3 homeo box gene in murine embryonic structures originating from or induced by the mesoderm. EMBO J 6: 2965-2975.
44. Packer AI, Crotty DA, Elwell VA, Wolgemuth DJ (1998) Expression of the murine Hoxa4 gene requires both autoregulation and a conserved retinoic acid response element. Development 125: 1991-1998. (Pubitemid 28297786)
45. Santini S, Boore JL, Meyer A (2003) Evolutionary conservation of regulatory elements in vertebrate Hox clusters. Genome Res 13: 1111-1122. (Pubitemid 36764191)
46. Khang K, Chung JH, Kim J (2009) Evolutionary Conserved Motif Finder (ECMFinder) for genome-wide identification of clustered YY1- and CTCF-binding sites. Nucl Acid Res 37: 2003-2013.
47. Donohoe M, Zhang X, McGinnis L, Biggers J, Li E, et al. (1999) Targeted disruption of mouse Yin Yang 1 transcription factor results in peri-implantation lethality. Mol Cell Biol 19: 7237-7244. (Pubitemid 29441903)
48. Marshall H, Morrison A, Studer M, Pöpperl H, Krumlauf R (1996) Retinoids and Hox genes. FASEB J 10: 969-978. (Pubitemid 26285972)
49. Nolte C, Amores A, Nagy Kovács E, Postlethwait J, Featherstone M (2003) The role of a retinoic acid response element in establishing the anterior neural expression border of Hoxd4 transgenes. Mech Dev 120: 325-335. (Pubitemid 36184628)
50. Pöpperl H, Featherstone MS (1993) Identification of a retinoic acid response element upstream of the murine Hox-4.2 gene. Mol Cell Biol 13: 257-265. (Pubitemid 23006903)
51. Mainguy G, In der Rieden PM, Berezikov E, Woltering JM, Plasterk RH, et al. (2003) A position-dependent organisation of retinoid response elements is conserved in the vertebrate Hox clusters. Trends Genet 19: 476-479. (Pubitemid 37101084)
52. Wang Z, Dollé P, Cardoso WV, Niederreither K (2006) Retinoic acid regulates morphogenesis and patterning of posterior foregut derivatives. Dev Biol 297: 433-445. (Pubitemid 44376638)
53. Chen H, Zhang H, Lee J, Liang X, Wu X, et al. (2007) HOXA5 acts directly dowstream of retinoic acid receptor b and contributes to retinoic acid-induced apoptosis and growth inhibition. Cancer Res 67: 8007-8013. (Pubitemid 47395134)
54. Thomas MJ, Seto E (1999) Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key? Gene 236: 197-208. (Pubitemid 29375109)
55. Ren G, Zhang G, Dong Z, Liu Z, Li L, et al. (2009) Recruitment of HDAC4 by transcription factor YY1 represses HOXB13 to affect cell growth in AR-negative prostate cancers. Int J Biochem Cell Biol 41: 1094-1101.
56. Kim SY, Paylor SW, Magnuson T, Schumacher A (2006) Juxtaposed Polycomb complexes co-regulate vertebral identity. Development 133: 4957-4968. (Pubitemid 46085061)
57. Rezai-Zadeh N, Zhang X, Namour F, Fejer G, Wen YD, et al. (2003) Targeted recruitment of a histone H4-specific methyltransferase by the transcription factor YY1. Genes Dev 17: 1019-1029. (Pubitemid 36459454)
58. Cai Y, Jin J, Yao T, Gottschalk AJ, Swanson SK, et al. (2007) YY1 functions with INO80 to activate transcription. Nat Struct Mol Biol 14: 872-874. (Pubitemid 47373827)
59. Wang CC, Tsai MF, Dai TH, Hong TM, Chan WK, et al. (2007) Synergistic activation of the tumor suppressor HLJ1 by the transcription factors YY1 and activator protein 1. Cancer Res 67: 4816-4826.
60. Yu H, Mashtalir N, Daou S, Hammond-Martel I, Ross J, et al. (2010) The ubiquitin carboxyl hydrolase BAP1 forms a ternary complex with YY1 and HCF-1 and is a critical regulator of gene expression. Mol Cell Biol 30: 5071-5085.
61. Bhalla SS, Robitaille L, Nemer M (2001) Cooperative activation by GATA-4 and YY1 of the cardiac B-type natriuretic peptide promoter. J Biol Chem 276: 11439-11445. (Pubitemid 38089339)
62. Trask MC, Tremblay KD, Mager J (2012) Yin-Yang 1 is required for epithelial-to-mesenchymal transition and regulation of Nodal signaling during mammalian gastrulation. Dev Biol 368: 273-282.
63. Li J, Song JS, Bell RJ, Tran TN, Haq R, et al. (2012) YY1 regulates melanocyte development and function by cooperating with MITF. PLoS Genet 8(5): e1002688.
64. Gregoire S, Karra R, Passer D, Deutsch MA, Krane M, et al. (2013) Essential and unexpected role of Yin Yang 1 to promote mesodermal cardiac differentiation. Circ Res 112: 900-910.
65. Rhee S, Guerrero-Zayas MI, Wallingford MC, Ortiz-Pineda P, Mager J, et al. (2013) Visceral endoderm expression of YY1 is required for VEGFA maintenance and yolk sac development. PLoS One 8(3): e58828. doi: 10.1371/journal.pone. 0058828.
66. Klug J, Beato M (1996) Binding of YY1 to a site overlapping a weak TATA box is essential for transcription from the uteroglobin promoter in endometrial cells. Mol Cell Biol 16: 6398-6407. (Pubitemid 26360998)