The ulnar-mammary syndrome gene, Tbx3, is a direct target of the retinoic acid signaling pathway, which regulates its expression during mouse limb development

Molecular Biology of the Cell

Volumn 23, Issue 12, 2012, Pages 2362-2372

  Ballim, Reyna Deeya ^a   Mendelsohn, Cathy ^b,c   Papaioannou, Virginia E ^c   Prince, Sharon ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOIC ACID; RETINOIC ACID RECEPTOR; T BOX TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ASSAY; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; FEMALE; GENE; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LIMB DEVELOPMENT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; SIGNAL TRANSDUCTION; TBX3 GENE; ULNAR MAMMARY SYNDROME;

ABNORMALITIES, MULTIPLE; ANIMALS; BLOTTING, WESTERN; BREAST DISEASES; CELL LINE, TUMOR; EMBRYO, MAMMALIAN; EXTREMITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEK293 CELLS; HUMANS; IN SITU HYBRIDIZATION; LUCIFERASES; MALE; MICE; MICE, INBRED ICR; MUTATION; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TRETINOIN; ULNA;

EID: 84862536481     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-09-0790     Document Type: Article

References (77)

1. Aagaard L, Amarzguioui M, Sun G, Santos LC, Ehsani A, Prydz H, Rossi JJ (2007). A facile lentiviral vector system for expression of doxycycline- inducible shRNAs: knockdown of the pre-miRNA processing enzyme Drosha. Mol Ther 15, 938-945. (Pubitemid 46621652)
2. Aström A, Pettersson U, Chambon P, Voorhees JJ (1994). Retinoic acid induction of human cellular retinoic acid-binding protein-II gene transcription is mediated by retinoic acid receptor-retinoid X receptor heterodimers bound to one far upstream retinoic acid-responsive element with 5-base pair spacing. J Biol Chem 269, 22334-22339.
3. Bakker ML, Boukens BJ, Mommersteeg MTM, Brons JF, Wakker V, Moorman AFM, Christoffels VM (2008). Transcription factor Tbx3 is required for the specification of the atrioventricular conduction system. Circ Res 102, 1340-1349.
4. Balmer JE, Blomhoff R (2002). Gene expression regulation by retinoic acid. J Lipid Res 43, 1773-1808. (Pubitemid 35315797)
5. Bamshad M et al. (1999). The spectrum of mutations in TBX3: genotype/phenotype relationship in ulnar-mammary syndrome. Am J Hum Genet 64, 1550-1562. (Pubitemid 30481507)
6. Bamshad M et al. (1997). Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome. Nat Genet 16, 311-315. (Pubitemid 27280219)
7. Bastien J, Rochette-Egly C (2004). Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 328, 1-16. (Pubitemid 38352876)
8. Behesti H, Holt JKL, Sowden JC (2006). The level of BMP4 signaling is critical for the regulation of distinct T-box gene expression domains and growth along the dorso-ventral axis of the optic cup. BMC Dev Biol 6, 62.
9. Brummelkamp TR, Kortlever RM, Lingbeek M, Trettel F, MacDonald ME, Lohuizen van M, Bernards R (2002). TBX-3, the gene mutated in ulnar-mammary syndrome, is a negative regulator of p19ARF and inhibits senescence. J Biol Chem 277, 6567-6572. (Pubitemid 34968456)
10. Carlson H, Ota S, Campbell CE, Hurlin PJ (2001). A dominant repression domain in Tbx3 mediates transcriptional repression and cell immortalization: relevance to mutations in Tbx3 that cause ulnar-mammary syndrome. Hum Mol Genet 10, 2403.
11. Chapman DL et al. (1996). Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev Dyn 206, 379-390. (Pubitemid 26260172)
12. Chen H, Zhang H, Lee J, Liang X, Wu X, Zhu T, Lo P-K, Zhang X, Sukumar S (2007). HOXA5 acts directly downstream of retinoic acid receptor beta and contributes to retinoic acid-induced apoptosis and growth inhibition. Cancer Res 67, 8007-8013. (Pubitemid 47395134)
13. Chia I, Grote D, Marcotte M, Batourina E, Mendelsohn C, Bouchard M (2011). Nephric duct insertion is a crucial step in urinary tract maturation that is regulated by a Gata3-Raldh2-Ret molecular network in mice. Development 138, 2089-2097.
14. Cooper KL, Hu JK-H, Berge ten D, Fernandez-Teran M, Ros MA, Tabin CJ (2011). Initiation of proximal-distal patterning in the vertebrate limb by signals and growth. Science 332, 1083-1086.
15. Davenport TG, Jerome-Majewska LA, Papaioannou VE (2003). Mammary gland, limb and yolk sac defects in mice lacking Tbx3, the gene mutated in human ulnar mammary syndrome. Development 130, 2263-2273. (Pubitemid 36656720)
16. Dhandapani L, Yue P, Ramalingam SS, Khuri FR, Sun S (2011). Retinoic acid enhances TRAIL-induced apoptosis in cancer cells by upregulating TRAIL receptor 1 expression. Cancer Res 71, 5245-5254.
17. Donato LJ, Suh JH, Noy N (2007). Suppression of mammary carcinoma cell growth by retinoic acid: the cell cycle control gene Btg2 is a direct target for retinoic acid receptor signaling. Cancer Res 67, 609-615. (Pubitemid 46192199)
18. Dupé V, Ghyselinck NB, Thomazy V, Nagy L, Davies PJ, Chambon P, Mark M (1999). Essential roles of retinoic acid signaling in interdigital apoptosis and control of BMP-7 expression in mouse autopods. Dev Biol 208, 30-43. (Pubitemid 29149445)
19. Fan W, Huang X, Chen C, Gray J, Huang T (2004). TBX3 and its isoform TBX3+2a are functionally distinctive in inhibition of senescence and are overexpressed in a subset of breast cancer cell lines. Cancer Res 64, 5132-5139. (Pubitemid 39006530)
20. Frasch M, Chen X, Lufkin T (1995). Evolutionary-conserved enhancers direct region-specific expression of the murine Hoxa-1 and Hoxa-2 loci in both mice and Drosophila. Development 121, 957-974.
21. Ghyselinck NB, Dupé V, Dierich A, Messaddeq N, Garnier JM, Rochette-Egly C, Chambon P, Mark M (1997). Role of the retinoic acid receptor beta (RARbeta) during mouse development. Int J Dev Biol 41, 425-447. (Pubitemid 27296912)
22. Gould A, Itasaki N, Krumlauf R (1998). Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron 21, 39-51. (Pubitemid 28355690)
23. Greulich F, Rudat C, Kispert A (2011). Mechanisms of T-box gene function in the developing heart. Cardiovasc Res 91, 212-222.
24. Han J et al. (2010). Tbx3 improves the germ-line competency of induced pluripotent stem cells. Nature 463, 1096-1100.
25. Hoogaars WM, Tessari A, Moorman AF, de Boer PA, Hagoort J, Soufan AT, Campione M, Christoffels VM (2004). The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart. Cardiovasc Res 62, 489-499. (Pubitemid 38648963)
26. Ito A, Asamoto M, Hokaiwado N, Takahashi S, Shirai T (2005). Tbx3 expression is related to apoptosis and cell proliferation in rat bladder both hyperplastic epithelial cells and carcinoma cells. Cancer Lett 219, 105-112. (Pubitemid 40203177)
27. Ivanova N, Dobrin R, Lu R, Kotenko I, Levorse J, DeCoste C, Schafer X, Lun Y, Lemischka IR (2006). Dissecting self-renewal in stem cells with RNA interference. Nature 442, 533-538. (Pubitemid 44167907)
28. Jerome-Majewska LA, Jenkins GP, Ernstoff E, Zindy F, Sherr CJ, Papaioannou VE (2005). Tbx3, the ulnar-mammary syndrome gene, and Tbx2 interact in mammary gland development through a p19Arf/p53-independent pathway. Dev Dyn 234, 922-933. (Pubitemid 41741164)
29. Lee KA, Green MR (1990). Small-scale preparation of extracts from radio-labeled cells efficient in pre-mRNA splicing. Methods Enzymol 181, 20-30. (Pubitemid 20219680)
30. Liberatore CM, Searcy-Schrick RD, Yutzey KE (2000). Ventricular expression of tbx5 inhibits normal heart chamber development. Dev Biol 223, 169-180. (Pubitemid 30439527)
31. Lingbeek ME, Jacobs JL, Lohuizen van M (2002). The T-box repressors TBX2 and TBX3 specifically regulate the tumor suppressor gene p14ARF via a variant T-site in the initiator. J Biol Chem 277, 26120-26127. (Pubitemid 34967096)
32. Lohnes D, Mark M, Mendelsohn C, Dolle P, Decimo D, Lemeur M, Dierich A, Gorry P, Chambon P (1995). Development roles of the retinoic acid receptors. J Steroid Biochem Mol Biol 53, 475-486.
33. Lohnes D, Mark M, Mendelsohn C, Dollé P, Dierich A, Gorry P, Gansmuller A, Chambon P (1994). Function of the retinoic acid receptors (RARs) during development (I). Craniofacial and skeletal abnormalities in RAR double mutants. Development 120, 2723-2748.
34. Lomnytska M, Dubrovska A, Hellman U, Volodko N, Souchelnytskyi S (2006). Increased expression of cSHMT, Tbx3 and utrophin in plasma of ovarian and breast cancer patients. Int J Cancer 118, 412-421. (Pubitemid 41779081)
35. Loudig O, Babichuk C, White J, Abu-Abed S, Mueller C, Petkovich M (2000). Cytochrome P450RAI(CYP26) promoter: a distinct composite retinoic acid response element underlies the complex regulation of retinoic acid metabolism. Mol Endocrinol 14, 1483-1497.
36. Lucas PC, O'Brien RM, Mitchell JA, Davis CM, Imai E, Forman BM, Samuels HH, Granner DK (1991). A retinoic acid response element is part of a pleiotropic domain in the phosphoenolpyruvate carboxykinase gene. Proc Natl Acad Sci USA 88, 2184-2188. (Pubitemid 21916379)
37. Lussier M, Canoun C, Ma C, Sank A, Shuler C (1993). Interdigital soft tissue separation induced by retinoic acid in mouse limbs cultured in vitro. Int J Dev Biol 37, 555-564. (Pubitemid 24063757)
38. Lyng H et al. (2006). Gene expressions and copy numbers associated with metastatic phenotypes of uterine cervical cancer. BMC Genomics 7, 268.
39. Mader S, Thiele K, Breuer B, Alonso A (1994). The promoter of the H1zero histone gene contains a DNA element bound by retinoic acid receptors. J Mol Biol 242, 37-44.
40. Mahlamäki EH, Barlund M, Tanner M, Gorunova L, Hoglund M, Karhu R, Kallioniemi A (2002). Frequent amplification of 8q24, 11q, 17q, and 20q-specific genes in pancreatic cancer. Genes Chromosomes Cancer 35, 353-358. (Pubitemid 35246993)
41. Mangelsdorf DJ et al. (1995). The nuclear receptor superfamily: the second decade. Cell 83, 835-839.
42. Martín M, Gallego-Llamas J, Ribes V, Kedinger M, Niederreither K, Chambon P, Dollé P, Gradwohl G (2005). Dorsal pancreas agenesis in retinoic acid-deficient Raldh2 mutant mice. Dev Biol 284, 399-411. (Pubitemid 41188144)
43. Mendelsohn C, Lohnes D, Décimo D, Lufkin T, LeMeur M, Chambon P, Mark M (1994). Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development 120, 2749-2771.
44. Mendelsohn C, Ruberte E, LeMeur M, Morriss-Kay G, Chambon P (1991). Developmental analysis of the retinoic acid-inducible RAR-beta 2 promoter in transgenic animals. Development 113, 723-734. (Pubitemid 21900312)
45. Mercader N, Leonardo E, Piedra ME, Martínez-A C, Ros MA, Torres M (2000). Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development 127, 3961-3970.
46. Mesbah K, Harrelson Z, Théveniau-Ruissy M, Papaioannou VE, Kelly RG (2008). Tbx3 is required for outflow tract development. Circ Res 103, 743-750.
47. Mic FA, Haselbeck RJ, Cuenca AE, Duester G (2002). Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development 129, 2271-2282. (Pubitemid 34874237)
48. Mowla S, Pinnock R, Leaner VD, Goding CR, Prince S (2011). PMA-induced up-regulation of TBX3 is mediated by AP-1 and contributes to breast cancer cell migration. Biochem J 433, 145-153.
49. Naiche LA, Papaioannou VE (2003). Loss of Tbx4 blocks hindlimb development and affects vascularization and fusion of the allantois. Development 130, 2681-2693. (Pubitemid 37069584)
50. Niederreither K, Fraulob V, Garnier J-M, Chambon P, Dollé P (2002a). Differential expression of retinoic acid-synthesizing (RALDH) enzymes during fetal development and organ differentiation in the mouse. Mech Dev 110, 165-171. (Pubitemid 34020635)
51. Niederreither K, Subbarayan V, Dollé P, Chambon P (1999). Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21, 444-448. (Pubitemid 29159586)
52. Niederreither K, Vermot J, Fraulob V, Chambon P, Dollé P (2002b). Retinaldehyde dehydrogenase 2 (RALDH2)-independent patterns of retinoic acid synthesis in the mouse embryo. Proc Natl Acad Sci USA 99, 16111-16116. (Pubitemid 35462757)
53. Niederreither K, Vermot J, Messaddeq N, Schuhbaur B, Chambon P, Dollé P (2001). Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development 128, 1019-1031. (Pubitemid 32401419)
54. Niwa H, Ogawa K, Shimosato D, Adachi K (2009). A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nat Lett 460, 118-122.
55. Ogura T, Evans RM (1995). A retinoic acid-triggered cascade of HOXB1 gene activation. Proc Natl Acad Sci USA 92, 387-391.
56. 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)
57. Peres J, Davis E, Mowla S, Bennett DC, Li JA, Wansleben S, Prince S (2010). The highly homologous T-box transcription factors, TBX2 and TBX3, have distinct roles in the oncogenic process. Genes Cancer 1, 272-282.
58. Prince S, Carreira S, Abrahams A, Goding CR (2004). Tbx2 directly represses the expression of the p21WAF1 cyclin-dependent kinase inhibitor. Cancer Res 64, 1669-1674. (Pubitemid 38428688)
59. Prince S, Wiggins T, Hulley PA, Kidson SH (2003). Stimulation of melanogenesis by tetradecanoylphorbol 13-acetate (TPA) in mouse melanocytes and neural crest cells. Pigment Cell Res 16, 26-34. (Pubitemid 36596691)
60. Renard C-A et al. (2007). Tbx3 is a downstream target of the Wnt/beta-catenin pathway and a critical mediator of beta-catenin survival functions in liver cancer. Cancer Res 67, 901-910.
61. Ribeiro I, Kawakami Y, Büscher D, Raya A, Rodríguez- León J, Morita M, Rodríguez Esteban C, Izpisúa Belmonte JC (2007). Tbx2 and Tbx3 regulate the dynamics of cell proliferation during heart remodeling. PloS One 2, e398.
62. Ribes V, Wang Z, Dollé P, Niederreither K (2006). Retinaldehyde dehydrogenase 2 (RALDH2)-mediated retinoic acid synthesis regulates early mouse embryonic forebrain development by controlling FGF and sonic hedgehog signaling. Development 133, 351-361. (Pubitemid 43210723)
63. Riddle RD, Johnson RL, Laufer E, Tabin C (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416. (Pubitemid 24021914)
64. Roberts C, Ivins SM, James CT, Scambler PJ (2005). Retinoic acid down-regulates Tbx1 expression in vivo and in vitro. Dev Dyn 232, 928-938. (Pubitemid 40463945)
65. Rodriguez M, Aladowicz E, Lanfrancone L, Goding CR (2008). Tbx3 represses E-cadherin expression and enhances melanoma invasiveness. Cancer Res 68, 7872-7881.
66. Roselló-Díez A, Ros MA, Torres M (2011). Diffusible signals, not autonomous mechanisms, determine the main proximodistal limb subdivision. Science 332, 1086-1088.
67. Rowley M, Grothey E, Couch FJ (2004). The role of Tbx2 and Tbx3 in mammary development and tumorigenesis. J Mammary Gland Biol Neoplasia 9, 109-118. (Pubitemid 39177497)
68. Sucov HM, Murakami KK, Evans RM (1990). Characterization of an autoregulated response element in the mouse retinoic acid receptor type beta gene. Proc Natl Acad Sci USA 87, 5392-5396.
69. Suzuki A, Sekiya S, Büscher D, Izpisúa Belmonte JC, Taniguchi H (2008). Tbx3 controls the fate of hepatic progenitor cells in liver development by suppressing p19ARF expression. Development 135, 1589-1595. (Pubitemid 351895488)
70. Suzuki T, Takeuchi J, Koshiba-Takeuchi K, Ogura T (2004). Tbx genes specify posterior digit identity through Shh and BMP signaling. Dev Cell 6, 43-53. (Pubitemid 38089204)
71. Tang X, Gudas LJ (2011). Retinoids, retinoic acid receptors, and cancer. Annu Rev Pathol 6, 345-364.
72. Tickle C, Alberts B, Wolpert L, Lee J (1982). Local application of retinoic acid to the limb bond mimics the action of the polarizing region. Nature 296, 564-566.
73. Tümpel S, Sanzezquerro J, Isaac A, Eblaghie M, Dobson J, Tickle C (2002). Regulation of Tbx3 expression by anteroposterior signalling in vertebrate limb development. Dev Biol 250, 251-262.
74. Wilkinson DG, Nieto MA (1993). Detection of messenger RNA by in situ hybridisation to tissue sections and whole mounts. Methods Enzymol 225, 361-373.
75. Yashiro K, Zhao X, Uehara M, Yamashita K, Nishijima M, Nishino J, Saijoh Y, Sakai Y, Hamada H (2004). Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev Cell 6, 411-422. (Pubitemid 38364572)
76. Zhao X, Brade T, Cunningham TJ, Duester G (2010). Retinoic acid controls expression of tissue remodeling genes Hmgn1 and Fgf18 at the digit-interdigit junction. Dev Dyn 239, 665-671.
77. Zhao X, Sirbu IO, Mic FA, Molotkova N, Molotkov A, Kumar S, Duester G (2009). Retinoic acid promotes limb induction through effects on body axis extension but is unnecessary for limb patterning. Curr Biol 19, 1050 1057.