Differential configurations involving binding of USF transcription factors and Twist1 regulate Alx3 promoter activity in mesenchymal and pancreatic cells

Biochemical Journal

Volumn 450, Issue 1, 2013, Pages 199-208

  García Sanz, Patricia ^a,b   Fernández Pérez, Antonio ^a   Vallejo, Mario ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO CAJAL   (Spain)

Author keywords

Aristaless; Basic helix loop helix protein; Homeodomain; Mesenchymal cell; Pancreatic islet cell; Transcription factor II I (TFII I)

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HOMEODOMAIN PROTEIN; HOMEODOMAIN PROTEIN ALX3; TRANSCRIPTION FACTOR TWIST1; UNCLASSIFIED DRUG; UPSTREAM STIMULATORY FACTOR; UPSTREAM STIMULATORY FACTOR 1; UPSTREAM STIMULATORY FACTOR 2;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL ISOLATION; CONTROLLED STUDY; E BOX ELEMENT; EMBRYO; FEMALE; FOREHEAD; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MESENCHYME CELL; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ANIMALS; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; EMBRYO, MAMMALIAN; FEMALE; GLUCAGON-SECRETING CELLS; HELA CELLS; HOMEODOMAIN PROTEINS; HUMANS; MESODERM; MICE; NIH 3T3 CELLS; NUCLEAR PROTEINS; PREGNANCY; PROMOTER REGIONS, GENETIC; TWIST TRANSCRIPTION FACTOR; UPSTREAM STIMULATORY FACTORS;

EID: 84873033118     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120962     Document Type: Article

References (56)

1. Meijlink, F., Beverdam, A., Brouwer, A., Oosterveen, T. C. and Ten Berge, D. (1999) Vertebrate aristaless-related genes. Int. J. Dev. Biol. 43, 651-663
2. Beverdam, A. and Meijlink, F. (2001) Expression patterns of group-I aristaless-related genes during craniofacial and limb development. Mech. Dev. 107, 163-167
3. Ten Berge, D., Brouwer, A., El Bahi, S., Guenet, J. L., Robert, B. and Meijlink, F. (1998) Mouse Alx3: an aristaless-like homeobox gene expressed during embryogenesis in ectomesenchyme and lateral plate mesoderm. Dev. Biol. 199, 11-25
4. Kuijper, S., Beverdam, A., Kroon, C., Brouwer, A., Candille, S., Barsh, G. and Meijlink, F. (2005) Genetics of shoulder girdle formation: roles of Tbx15 and aristaless-like genes. Development 132, 1601-1610
5. Qu, S., Tucker, S. C., Zhai, Q., de Crombrugghe, B. and Wisdom, R. (1999) Physical and genetic interactions between Alx4 and Cart1. Development 126, 359-369
6. McGonnell, I. M., Graham, A., Richardson, J., Fish, J. L., Depew, M. J., Dee, C. T., Holland, P. W. H. and Takahashi, T. (2011) Evolution of the Alx homeobox gene family: parallel retention and independent loss of the vertebrate Alx3 gene. Evol. Dev. 13, 343-351
7. Kayserili, H., Uz, E., Niessen, C., Vargel, I., Alanay, Y., Tuncbilek, G., Yigit, G., Uyguner, O., Candan, S., Okur, H. et al. (2009) ALX4 dysfunction disrupts craniofacial and epidermal development. Hum. Mol. Genet. 18, 4357-4366
8. Twigg, S. R. F., Versnel, S. L., Nurnberg, G., Lees, M. M., Bhat, M., Hammond, P., Hennekam, C. M., Hoogeboom, A. J. M., Hurst, J. A., Johnson, D. et al. (2009) Frontorhiny, a distinctive presentation of frontonasal dysplasia caused by recessive mutations in the ALX3 homeobox gene. Am. J. Hum. Genet. 84, 1-8
9. Uz, E., Alanay, Y., Aktas, D., Vargel, I., Gucer, S., Tuncbilek, G., von Eggeling, F., Yilmaz, E., Deren, O., Posorski, N. et al. (2010) Disruption of ALX1causes extreme microphtalmia and severe facial clefting: expanding the spectrum of autosomal-recessive ALX-related frontonasal dysplasia. Am. J. Hum. Genet. 86, 789-796
10. Zhao, Q., Behringer, R. R. and Crombrugghe (1996) Prenatal folic acid treatment suppresses acrania and meroanencephaly in mice mutant for the Cart1 homeobox gene. Nat. Genet. 13, 275-283
11. Qu, S., Niswender, K. D., Ji, Q., van der Meer, R., Keeney, D., Magnuson, M. A. and Wisdom, R. (1997) Polydactyly and ectopic ZPA formation in Alx-4 mutant mice. Development 124, 3999-4008
12. Qu, S., Tucker, S. C., Ehrlich, J. S., Levorse, J. M., Flaherty, L. A., Wisdom, R. and Vogt, T. F. (1998) Mutations in mouse Aristaless-like4 cause Strong's luxoid polydactyly. Development 125, 2711-2721
13. Takahashi, M., Tamura, K., Buscher, D., Masuya, H., Yonei-Tamura, S., Matsumoto, K., Naitoh-Matsuo, M., Takeuchi, J., Ogura, K., Shiroishi, T. et al. (1998) The role of Alx-4 in the establishment of anterior polarity during vertebrate limb development. Development 125, 4417-4425
14. Beverdam, A., Brouwer, A., Reijnen, M., Korving, J. and Meijlink, F. (2001) Severe nasal clefting and abnormal embryonic apoptosis in Alx3/Alx4 double mutant mice. Development 128, 3975-3986
15. Lakhwani, S., García-Sanz, P. and Vallejo, M. (2010) Alx3-deficient mice exhibit folic acid-resistant craniofacial midline and neural tube closure defects. Dev. Biol. 344, 869-880
16. Rudnick, A., Ling, T. Y., Odagiri, H., Rutter, W. and German, M. S. (1994) Pancreatic β-cells express a diverse set of homeobox genes. Proc. Natl. Acad. Sci. U.S.A. 91, 12203-12207
17. Mirasierra, M., Fernández-Pérez, A., Díaz-Prieto, N. and Vallejo, M. (2011) Alx3-deficient mice exhibit decreased insulin in beta cells, altered glucose homeostasis and increased apoptosis in pancreatic islets. Diabetologia 54, 403-414
18. Mirasierra, M. and Vallejo, M. (2006) The homeoprotein Alx3 expressed in pancreatic β-cells regulates insulin gene transcription by interacting with the basic helix-loop-helix protein E47. Mol. Endocrinol. 20, 2876-2889
19. McManus, M. F., Chen, L. C., Vallejo, I. and Vallejo, M. (1999) Astroglial differentiation of cortical precursor cells triggered by activation of the cAMP-dependent signaling pathway. J. Neurosci. 19, 9004-9015
20. Pérez-Villamil, B., Mirasierra, M. and Vallejo, M. (2004) The homeoprotein Alx3 contains discrete functional domains and exhibits cell-specific and selective monomeric binding and transactivation. J. Biol. Chem. 279, 38062-38071
21. Pérez-Moreno, M. A., Locascio, A., Rodrigo, I., Dhondt, G., Portillo, F., Nieto, M. A. and Cano, A. (2001) A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J. Biol. Chem. 276, 27424-27431
22. Coulson, J. M., Edgson, J. L., Marshall-Jones, Z. V., Mulgrew, R., Quinn, J. P. and Woll, P. J. (2003) Upstream stimulatory factor activates the vasopressin promoter via multiple motifs, including a non-canonical E-box. Biochem. J. 369, 549-561
23. Landa, I., Ruiz-Llorente, S., Montero-Conde, C., Inglada-P'erez, L., Schiavi, F., Leskelä, S., Pita, G., Milne, R., Maravall, J., Ramos, I. et al. (2009) The variant rs1867277 in FOXE1gene confers thyroid cancer susceptibility through the recruitment of USF1/USF2 transcription factors. PLoS Genet. 5, e1000637
24. Yang, J., Mani, S. A., Donaher, J. L., Ramaswamy, S., Itzykson, R. A., Come, C., Savagner, P., Gitelman, I., Richardson, A. and Weinberg, R. A. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 177, 927-939
25. Eckert, M. A., Lwin, T. M., Chang, A. T., Kim, J., Danis, E., Ohno-Machado, L. and Yang, J. (2011) Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 19, 372-386
26. Lee, Y. B., Bantounas, I., Lee, D. Y., Phylactou, L., Caldwell, M. A. and Uney, J. B. (2009) Twist-1 regulates the miR-199a/214 cluster during development. Nucleic Acids Res. 37, 123-128
27. Massari, M. E. and Murre, C. (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20, 429-440
28. Miyazaki, J., Araki, K., Yamato, E., Ikegami, H., Asano, T., Shibasaki, Y., Oka, Y. and Yamamura, K. (1990) Establishment of a pancreatic β cell line that retains glucose-inducible secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127, 126-132
29. Qian, J., Kaytor, E. N., Towle, H. C. and Olson, L. K. (1999) Upstream stimulatory factor regulates Pdx-1 gene expression in differentiated pancreatic β-cells. Biochem. J. 341, 315-322
30. Stoetzel, C., Weber, B., Bourgeois, P., Bolcato-Bellemin, A. L. and Perrin-Schmitt, F. (1995) Dorso-ventral and rostrocaudal sequential expression of M-twist in the postimplantation murine embryo. Mech. Dev. 51, 251-263
31. Connerney, J., Andreeva, V., Leshem, Y., Muentener, C., Mercado, M. A. and Spicer, D. B. (2006) Twist1 dimer selection regulates cranial suture patterning and fusion. Dev. Dyn. 235, 1345-1357
32. Roy, A. L., Meisterernst, M., Pognonec, P. and Roeder, R. G. (1991) Cooperative interaction of an initiator-binding transcription initiation factor and the helix-loop-helix activator USF. Nature 354, 245-248
33. Li, L. H., Nerlov, C., Prendergast, G., MacGregor, D. and Ziff, E. B. (1994) c-Myc represses transcription in vivoby a novel mechanism dependent on the initiator element and Myc box II. EMBO J. 13, 4070-4079
34. O'Rourke, M. P. and Tam, P. P. L. (2002) Twist functions in mouse development. Int. J. Dev. Biol. 46, 401-413
35. Chen, Z. F. and Behringer, R. R. (1995) twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes Dev. 9, 686-699
36. Soo, K., O'Rourke, M. P., Khoo, P. L., Steiner, K. A., Wong, N., Behringer, R. R. and Tam, P. P. L. (2002) Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo. Dev. Biol. 247, 251-270
37. Bildsoe, H., Loebel, D. A. F., Jones, V. J., Chen, Y. T., Behringer, R. R. and Tam, P. P. L. (2009) Requirement for Twist in frontonasal and skull vault development in the mouse embryo. Dev. Biol. 331, 176-188
38. Loebel, D. A. F., O'Rourke, M. P., Steiner, K. A., Banyer, J. and Tam, P. P. L. (2002) Isolation of differentially expressed genes from wild-type and Twist mutant mouse limb buds. Genesis 33, 103-113
39. O'Rourke, M. P., Soo, K., Behringer, R. R., Hui, C. C. and Tam, P. P. L. (2002) Twist plays an essential role in FGF and SHH signal transduction during mouse limb development. Dev. Biol. 248, 143-156
40. Howard, T. D., Paznekas, W. A., Green, E. D., Chiang, L. C., Ma, N., Ortiz De Luna, R. I., Delgado, C. G., Gonzalez-Ramos, M., Kline, A. D. and Jabs, E. W. (1997) Mutations in TWIST, a basic helix-loop-helix transcription factor, in Saethre-Chotzen syndrome. Nat. Genet. 15, 36-41
41. El Ghouzzi, V., Le Merrer, M., Perrin-Schmitt, F., Lajeunie, E., Benit, P., Renier, D., Bourgeois, P., Bolcato-Bellemin, A. L., Munnich, A. and Bonaventure, J. (1997) Mutations of the TWIST gene in the Saethre-Chotzen syndrome. Nat. Genet. 15, 42-46
42. Mavrogiannis, L. A., Antonopoulou, I., Baxová, A., Kutílek, S., Kim, C. A., Sugayama, S. M., Salamanca, A., Wall, S. A., Morriss-Kay, G. M. and Wilkie, A. O. (2001) Haploinsufficiency of the human homeobox gene ALX4 causes skull ossification defects. Nat. Genet. 27, 17-18
43. Connerney, J., Andreeva, V., Leshem, Y., Mercado, M. A., Dowell, K., Yang, X., Lindner, V., Friesel, R. E. and Spicer, D. B. (2008) Twist1 homodimers enhance FGF responsiveness of the cranial sutures and promote suture closure. Dev. Biol. 318, 323-334
44. Danciu, T. E. and Whitman, M. (2010) Oxidative stress drives disulfide bond formation between basic helix-loop-helix transcription factors. J. Cell. Biochem. 109, 417-424
45. Laursen, K. B., Mielke, E., Iannaccone, P. and Fuchtbauer, E. M. (2007) Mechanism of transcriptional activation by the proto-oncogene Twist1. J. Biol. Chem. 282, 34623-34633
46. Firulli, B. A., Krawchuk, D., Centonze, V. E., Vargesson, N., Virshup, D. M., Conway, S. J., Cserjesi, P., Laufer, E. and Firulli, A. B. (2005) Altered Twist1 and Hand2 dimerization is associated with Saethre-Chotzen syndrome and limb abnormalities. Nat. Genet. 37, 373-381
47. Villavicencio, E. H., Yoon, J. W., Frank, D. J., Fuchtbauer, E. M., Walterhouse, D. O. and Iannaccone, P. M. (2002) Cooperative E-box regulation of human GLI1 by TWIST and USF. Genesis 32, 247-258
48. Smale, S. T. (1997) Transcription initiation from TATA-less promoters within eukaryotic protein-coding genes. Biochem. Biophys. Acta 1351, 73-88
49. Breen, G. A. M. and Jordan, E. M. (2000) Upstream stimulatory factor 2 stimulates transcription through an initiator element in the mouse cytochrome c oxidase subunit Vb promoter. Biochem. Biophys. Acta 1517, 119-127
50. van Deursen, D., van Leeuwen, M., Vaulont, S., Jansen, H. and Verhoeven, A. J. M. (2009) Upstream stimulatory factors 1 and 2 activate the human hepatic lipase promoter via E-box dependent and independent mechanisms. Biochem. Biophys. Acta 1791, 229-237
51. Anantharaman, A., Lin, I. J., Barrow, J., Liang, S. Y., Masannat, J., Strouboulis, J., Huang, S. and Bungert, J. (2011) Role of helix-loop-helix proteins during differentiation of erythroid cells. Mol. Cell. Biol. 31, 1332-1343
52. Wang, S. M., Coljee, V. W., Pignolo, R. J., Rotenberg, M. O., Cristofalo, V. J. and Sierra, F. (1997) Cloning of the human Twist gene: its expression is retained in adult mesodermally-derived tissues. Gene 187, 83-92
53. Martin, C. C., Svitek, C. A., Oeser, J. K., Henderson, E., Stein, R. and O'Brien, R. M. (2003) Upstream stimulatory factor (USF) and neurogenic differentiation/β-cell E box transactivator 2 (NeuroD/BETA2) contribute to islet-specific glucose-6-phosphatase catalytic-subunit-related protein (IGRP) gene expression. Biochem. J. 371, 675-686
54. Boonsaen, T., Rojvirat, P., Surinya, K. H., Wallace, J. C. and Jitrapakdee, S. (2007) Transcriptional regulation of the distal promoter of the rat pyruvate carboxylase gene by hepatocyte nuclear factor 3β/Foxa2 and upstream stimulatory factors in insulinoma cells. Biochem. J. 405, 359-367
55. Bernardo, A. S., Hay, C. W. and Docherty, K. (2008) Pancreatic transcription factors and their role in the birth, life and survival of the pancreatic β cell. Mol. Cell. Endocrinol. 294, 1-9
56. Meex, S. J., van Vliet-Ostaptchouk, J. V., van der Kallen, C. J., van Greevenbroek, M. M., Schalkwijk, C. G., Feskens, E. J., Blaak, E. E., Wijmenga, C., Hokfer, M. H., Stehouwer, C. D. and de Bruin, T. W. (2008) Upstream transcription factor 1 (USF1) in risk of type 2 diabetes: association study in 2000 Dutch Caucasians. Mol. Genet. Metab. 94, 352-355