Artículo

Crocker, J.; Abe, N.; Rinaldi, L.; McGregor, A.P.; Frankel, N.; Wang, S.; Alsawadi, A.; Valenti, P.; Plaza, S.; Payre, F.; Mann, R.S.; Stern, D.L. "Low affinity binding site clusters confer HOX specificity and regulatory robustness" (2015) Cell. 160(1-2):191-203
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

In animals, Hox transcription factors define regional identity in distinct anatomical domains. How Hox genes encode this specificity is a paradox, because different Hox proteins bind with high affinity in vitro to similar DNA sequences. Here, we demonstrate that the Hox protein Ultrabithorax (Ubx) in complex with its cofactor Extradenticle (Exd) bound specifically to clusters of very low affinity sites in enhancers of the shavenbaby gene of Drosophila. These low affinity sites conferred specificity for Ubx binding in vivo, but multiple clustered sites were required for robust expression when embryos developed in variable environments. Although most individual Ubx binding sites are not evolutionarily conserved, the overall enhancer architecture - clusters of low affinity binding sites - is maintained and required for enhancer function. Natural selection therefore works at the level of the enhancer, requiring a particular density of low affinity Ubx sites to confer both specific and robust expression. © 2015 Elsevier Inc.

Registro:

Documento: Artículo
Título:Low affinity binding site clusters confer HOX specificity and regulatory robustness
Autor:Crocker, J.; Abe, N.; Rinaldi, L.; McGregor, A.P.; Frankel, N.; Wang, S.; Alsawadi, A.; Valenti, P.; Plaza, S.; Payre, F.; Mann, R.S.; Stern, D.L.
Filiación:Janelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, United States
Columbia University Medical Center, HHSC 1104, 701 West 168 th Street, New York, NY 10032, United States
Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, United Kingdom
Departamento de Ecología, Genética y Evolución, IEGEBA-CONICET, Universidad de Buenos Aires, Ciudad, Universitaria, Pabellón 21428, Argentina
New Jersey Neuroscience Institute, 65 James Street, Edison, NJ 08820, United States
Centre de Biologie du Développement, Université de Toulouse, UPS, Cedex 9, 31062, France
CNRS, UMR5547, Centre de Biologie du Développement, Toulouse, Cedex 9, 31062, France
Palabras clave:DNA fragment; Hox protein; DNA binding protein; Drosophila protein; extradenticle protein, Drosophila; homeodomain protein; ovo protein, Drosophila; protein binding; transcription factor; Ubx protein, Drosophila; animal cell; Article; binding affinity; binding site; chromatin immunoprecipitation; controlled study; DNA sequence; Drosophila melanogaster; Drosophila virilis; embryo; embryo cell; enhancer region; gel mobility shift assay; genetic conservation; genetic regulation; genetic variability; insect cell; natural selection; nonhuman; priority journal; reporter gene; trichome; wild type; animal; animal embryo; enhancer region; gene expression regulation; genetics; metabolism; molecular genetics; nucleotide sequence; sequence alignment; Animalia; Animals; Base Sequence; DNA-Binding Proteins; Drosophila melanogaster; Drosophila Proteins; Embryo, Nonmammalian; Enhancer Elements, Genetic; Gene Expression Regulation; Homeodomain Proteins; Molecular Sequence Data; Protein Binding; Sequence Alignment; Transcription Factors
Año:2015
Volumen:160
Número:1-2
Página de inicio:191
Página de fin:203
DOI: http://dx.doi.org/10.1016/j.cell.2014.11.041
Título revista:Cell
Título revista abreviado:Cell
ISSN:00928674
CODEN:CELLB
CAS:DNA-Binding Proteins; Drosophila Proteins; extradenticle protein, Drosophila; Homeodomain Proteins; ovo protein, Drosophila; Transcription Factors; Ubx protein, Drosophila
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00928674_v160_n1-2_p191_Crocker

Referencias:

  • Akam, M., Hox and HOM: Homologous gene clusters in insects and vertebrates (1989) Cell, 57, pp. 347-349
  • Arnone, M.I., Davidson, E.H., The hardwiring of development: Organization and function of genomic regulatory systems (1997) Development, 124, pp. 1851-1864
  • Belyi, V.A., Ak, P., Markert, E., Wang, H., Hu, W., Puzio-Kuter, A., Levine, A.J., The origins and evolution of the p53 family of genes (2010) Cold Spring Harb. Perspect. Biol., 2, p. a001198
  • Berger, M.F., Badis, G., Gehrke, A.R., Talukder, S., Philippakis, A.A., Peña-Castillo, L., Alleyne, T.M., Chan, E.T., Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences (2008) Cell, 133, pp. 1266-1276
  • Busser, B.W., Shokri, L., Jaeger, S.A., Gisselbrecht, S.S., Singhania, A., Berger, M.F., Zhou, B., Michelson, A.M., Molecular mechanism underlying the regulatory specificity of a Drosophila homeodomain protein that specifies myoblast identity (2012) Development, 139, pp. 1164-1174
  • Chan, S.-K.K., Jaffe, L., Capovilla, M., Botas, J., Mann, R.S., The DNA binding specificity of Ultrabithorax is modulated by cooperative interactions with extradenticle, another homeoprotein (1994) Cell, 78, pp. 603-615
  • Chang, C.P., Shen, W.F., Rozenfeld, S., Lawrence, H.J., Largman, C., Cleary, M.L., Pbx proteins display hexapeptide-dependent cooperative DNA binding with a subset of Hox proteins (1995) Genes Dev., 9, pp. 663-674
  • Chanut-Delalande, H., Fernandes, I., Roch, F., Payre, F., Plaza, S., Shavenbaby couples patterning to epidermal cell shape control (2006) PLoS Biol., 4, p. e290
  • Choo, S.W., White, R., Russell, S., Genome-wide analysis of the binding of the Hox protein Ultrabithorax and the Hox cofactor Homothorax in Drosophila (2011) PLoS ONE, 6, p. e14778
  • Coiffier, D., Charroux, B., Kerridge, S., Common functions of central and posterior Hox genes for the repression of head in the trunk of Drosophila (2008) Development, 135, pp. 291-300
  • Crocker, J., Stern, D.L., TALE-mediated modulation of transcriptional enhancers in vivo (2013) Nat. Methods, 10, pp. 762-767
  • Crocker, J., Tamori, Y., Erives, A., Evolution acts on enhancer organization to fine-tune gradient threshold readouts (2008) PLoS Biol., 6, p. e263
  • Delon, I., Chanut-Delalande, H., Payre, F., The Ovo/Shavenbaby transcription factor specifies actin remodelling during epidermal differentiation in Drosophila (2003) Mech. Dev., 120, pp. 747-758
  • Doniger, S.W., Fay, J.C., Frequent gain and loss of functional transcription factor binding sites (2007) PLoS Comput. Biol., 3, p. e99
  • Doniger, S.W., Huh, J., Fay, J.C., Identification of functional transcription factor binding sites using closely related Saccharomyces species (2005) Genome Res., 15, pp. 701-709
  • Driever, W., Nüsslein-Volhard, C., The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo (1989) Nature, 337, pp. 138-143
  • Driever, W., Thoma, G., Nüsslein-Volhard, C., Determination of spatial domains of zygotic gene expression in the Drosophila embryo by the affinity of binding sites for the bicoid morphogen (1989) Nature, 340, pp. 363-367
  • Dror, I., Zhou, T., Mandel-Gutfreund, Y., Rohs, R., Covariation between homeodomain transcription factors and the shape of their DNA binding sites (2014) Nucleic Acids Res., 42, pp. 430-441
  • Estella, C., McKay, D.J., Mann, R.S., Molecular integration of wingless, decapentaplegic, and autoregulatory inputs into Distalless during Drosophila leg development (2008) Dev. Cell, 14, pp. 86-96
  • Frankel, N., Davis, G.K., Vargas, D., Wang, S., Payre, F., Stern, D.L., Phenotypic robustness conferred by apparently redundant transcriptional enhancers (2010) Nature, 466, pp. 490-493
  • Frankel, N., Erezyilmaz, D.F., McGregor, A.P., Wang, S., Payre, F., Stern, D.L., Morphological evolution caused by many subtle-effect substitutions in regulatory DNA (2011) Nature, 474, pp. 598-603
  • Frankel, N., Wang, S., Stern, D.L., Conserved regulatory architecture underlies parallel genetic changes and convergent phenotypic evolution (2012) Proc. Natl. Acad. Sci. USA, 109, pp. 20975-20979
  • Gaudet, J., Mango, S.E., Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4 (2002) Science, 295, pp. 821-825
  • Giorgetti, L., Siggers, T., Tiana, G., Caprara, G., Notarbartolo, S., Corona, T., Pasparakis, M., Natoli, G., Noncooperative interactions between transcription factors and clustered DNA binding sites enable graded transcriptional responses to environmental inputs (2010) Mol. Cell, 37, pp. 418-428
  • Giorgianni, M.W., Mann, R.S., Establishment of medial fates along the proximodistal axis of the Drosophila leg through direct activation of dachshund by Distalless (2011) Dev. Cell, 20, pp. 455-468
  • González-Reyes, A., Morata, G., The developmental effect of overexpressing a Ubx product in Drosophila embryos is dependent on its interactions with other homeotic products (1990) Cell, 61, pp. 515-522
  • Gotea, V., Visel, A., Westlund, J.M., Nobrega, M.A., Pennacchio, L.A., Ovcharenko, I., Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers (2010) Genome Res., 20, pp. 565-577
  • Hasan, R., Leroy, C., Isnard, A.-D., Labarre, J., Boy-Marcotte, E., Toledano, M.B., The control of the yeast H2O2 response by the Msn2/4 transcription factors (2002) Mol. Microbiol., 45, pp. 233-241
  • He, X., Duque, T.S.P.C., Sinha, S., Evolutionary origins of transcription factor binding site clusters (2012) Mol. Biol. Evol., 29, pp. 1059-1070
  • Hersh, B.M., Carroll, S.B., Direct regulation of knot gene expression by Ultrabithorax and the evolution of cis-regulatory elements in Drosophila (2005) Development, 132, pp. 1567-1577
  • Jiang, J., Levine, M., Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen (1993) Cell, 72, pp. 741-752
  • Joshi, R., Passner, J.M., Rohs, R., Jain, R., Sosinsky, A., Crickmore, M.A., Jacob, V., Mann, R.S., Functional specificity of a Hox protein mediated by the recognition of minor groove structure (2007) Cell, 131, pp. 530-543
  • Jürgens, G., Wieschaus, E., Nüsselin-Volhard, C., Kluding, H., Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome (1984) Rouxs Arch. Dev. Biol., 193, pp. 283-295
  • Karch, F., Bender, W., Weiffenbach, B., AbdA expression in Drosophila embryos (1990) Genes Dev., 4, pp. 1573-1587
  • Kuroiwa, A., Kloter, U., Baumgartner, P., Gehring, W.J., Cloning of the homeotic Sex combs reduced gene in Drosophila and in situ localization of its transcripts (1985) EMBO J., 4 (13), pp. 3757-3764
  • Lebrecht, D., Foehr, M., Smith, E., Lopes, F.J.P., Vanario-Alonso, C.E., Reinitz, J., Burz, D.S., Hanes, S.D., Bicoid cooperative DNA binding is critical for embryonic patterning in Drosophila (2005) Proc. Natl. Acad. Sci. USA, 102, pp. 13176-13181
  • Lelli, K.M., Noro, B., Mann, R.S., Variable motif utilization in homeotic selector (Hox)-cofactor complex formation controls specificity (2011) Proc. Natl. Acad. Sci. USA, 108, pp. 21122-21127
  • Lewis, E.B., A gene complex controlling segmentation in Drosophila (1978) Nature, 276, pp. 565-570
  • Lifanov, A.P., Makeev, V.J., Nazina, A.G., Papatsenko, D.A., Homotypic regulatory clusters in Drosophila (2003) Genome Res., 13, pp. 579-588
  • Ludwig, M.Z., Patel, N.H., Kreitman, M., Functional analysis of eve stripe 2 enhancer evolution in Drosophila: Rules governing conservation and change (1998) Development, 125, pp. 949-958
  • Mann, R.S., Hogness, D.S., Functional dissection of Ultrabithorax proteins in D. Melanogaster (1990) Cell, 60, pp. 597-610
  • Mann, R.S., Lelli, K.M., Joshi, R., Hox specificity unique roles for cofactors and collaborators (2009) Curr. Top. Dev. Biol., 88, pp. 63-101
  • McGinnis, W., Krumlauf, R., Homeobox genes and axial patterning (1992) Cell, 68, pp. 283-302
  • McGregor, A.P., Orgogozo, V., Delon, I., Zanet, J., Srinivasan, D.G., Payre, F., Stern, D.L., Morphological evolution through multiple cis-regulatory mutations at a single gene (2007) Nature, 448, pp. 587-590
  • Moens, C.B., Selleri, L., Hox cofactors in vertebrate development (2006) Dev. Biol., 291, pp. 193-206
  • Noro, B., Culi, J., McKay, D.J., Zhang, W., Mann, R.S., Distinct functions of homeodomain-containing and homeodomain-less isoforms encoded by homothorax (2006) Genes Dev., 20, pp. 1636-1650
  • Noyes, M.B., Christensen, R.G., Wakabayashi, A., Stormo, G.D., Brodsky, M.H., Wolfe, S.A., Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites (2008) Cell, 133, pp. 1277-1289
  • Ochoa-Espinosa, A., Yucel, G., Kaplan, L., Pare, A., Pura, N., Oberstein, A., Papatsenko, D., Small, S., The role of binding site cluster strength in Bicoid-dependent patterning in Drosophila (2005) Proc. Natl. Acad. Sci. USA, 102, pp. 4960-4965
  • Pai, C.Y., Kuo, T.S., Jaw, T.J., Kurant, E., Chen, C.T., Bessarab, D.A., Salzberg, A., Sun, Y.H., The Homothorax homeoprotein activates the nuclear localization of another homeoprotein, extradenticle, and suppresses eye development in Drosophila (1998) Genes Dev., 12, pp. 435-446
  • Papatsenko, D.A., Makeev, V.J., Lifanov, A.P., Régnier, M., Nazina, A.G., Desplan, C., Extraction of functional binding sites from unique regulatory regions: The Drosophila early developmental enhancers (2002) Genome Res., 12, pp. 470-481
  • Payre, F., Vincent, A., Carreno, S., Ovo/svb integrates Wingless and der pathways to control epidermis differentiation (1999) Nature, 400, pp. 271-275
  • Peifer, M., Wieschaus, E., Mutations in the Drosophila gene extradenticle affect the way specific homeo domain proteins regulate segmental identity (1990) Genes Dev., 4, pp. 1209-1223
  • Peterson, K.A., Nishi, Y., Ma, W., Vedenko, A., Shokri, L., Zhang, X., McFarlane, M., Van Oudenaarden, A., Neural-specific Sox2 input and differential Gli-binding affinity provide context and positional information in Shh-directed neural patterning (2012) Genes Dev., 26, pp. 2802-2816
  • Powsner, L., The effects of temperature on the durations of the developmental stages of Drosophila melanogaster (1935) Physiol. Zool., 8, pp. 474-520
  • Ramos, A.I., Barolo, S., Low-affinity transcription factor binding sites shape morphogen responses and enhancer evolution (2013) Philos. Trans. R. Soc. Lond. B Biol. Sci., 368, p. 20130018
  • Rieckhof, G.E., Casares, F., Ryoo, H.D., Abu-Shaar, M., Mann, R.S., Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein (1997) Cell, 91, pp. 171-183
  • Rohs, R., West, S.M., Sosinsky, A., Liu, P., Mann, R.S., Honig, B., The role of DNA shape in protein-DNA recognition (2009) Nature, 461, pp. 1248-1253
  • Rowan, S., Siggers, T., Lachke, S.A., Yue, Y., Bulyk, M.L., Maas, R.L., Precise temporal control of the eye regulatory gene Pax6 via enhancer-binding site affinity (2010) Genes Dev., 24, pp. 980-985
  • Ryoo, H.D., Mann, R.S., The control of trunk Hox specificity and activity by Extradenticle (1999) Genes Dev., 13, pp. 1704-1716
  • Ryoo, H.D., Marty, T., Casares, F., Affolter, M., Mann, R.S., Regulation of Hox target genes by a DNA bound Homothorax/Hox/Extradenticle complex (1999) Development, 126, pp. 5137-5148
  • Sánchez-Herrero, E., Vernós, I., Marco, R., Morata, G., Genetic organization of Drosophila bithorax complex (1985) Nature, 313, pp. 108-113
  • Saramäki, A., Banwell, C.M., Campbell, M.J., Carlberg, C., Regulation of the human p21(waf1/cip1) gene promoter via multiple binding sites for p53 and the vitamin D3 receptor (2006) Nucleic Acids Res., 34, pp. 543-554
  • Scardigli, R., Bäumer, N., Gruss, P., Guillemot, F., Le Roux, I., Direct and concentration-dependent regulation of the proneural gene Neurogenin2 by Pax6 (2003) Development, 130, pp. 3269-3281
  • Segal, E., Raveh-Sadka, T., Schroeder, M., Unnerstall, U., Gaul, U., Predicting expression patterns from regulatory sequence in Drosophila segmentation (2008) Nature, 451, pp. 535-540
  • Silverman, N., Maniatis, T., NF-kappaB signaling pathways in mammalian and insect innate immunity (2001) Genes Dev., 15, pp. 2321-2342
  • Slattery, M., Riley, T., Liu, P., Abe, N., Gomez-Alcala, P., Dror, I., Zhou, T., Mann, R.S., Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins (2011) Cell, 147, pp. 1270-1282
  • Stanojevic, D., Small, S., Levine, M., Regulation of a segmentation stripe by overlapping activators and repressors in the Drosophila embryo (1991) Science, 254, pp. 1385-1387
  • Stewart-Ornstein, J., Nelson, C., Derisi, J., Weissman, J.S., El-Samad, H., Msn2 coordinates a stoichiometric gene expression program (2013) Curr. Biol., 23, pp. 2336-2345
  • Struhl, G., Genes controlling segmental specification in the Drosophila thorax (1982) Proc. Natl. Acad. Sci. USA, 79, pp. 7380-7384
  • Struhl, G., Struhl, K., Macdonald, P.M., The gradient morphogen bicoid is a concentration-dependent transcriptional activator (1989) Cell, 57, pp. 1259-1273
  • Swanson, C.I., Evans, N.C., Barolo, S., Structural rules and complex regulatory circuitry constrain expression of a Notch- and EGFR-regulated eye enhancer (2010) Dev. Cell, 18, pp. 359-370
  • Wakimoto, B.T., Kaufman, T.C., Analysis of larval segmentation in lethal genotypes associated with the antennapedia gene complex in Drosophila melanogaster (1981) Dev. Biol., 81, pp. 51-64

Citas:

---------- APA ----------
Crocker, J., Abe, N., Rinaldi, L., McGregor, A.P., Frankel, N., Wang, S., Alsawadi, A.,..., Stern, D.L. (2015) . Low affinity binding site clusters confer HOX specificity and regulatory robustness. Cell, 160(1-2), 191-203.
http://dx.doi.org/10.1016/j.cell.2014.11.041
---------- CHICAGO ----------
Crocker, J., Abe, N., Rinaldi, L., McGregor, A.P., Frankel, N., Wang, S., et al. "Low affinity binding site clusters confer HOX specificity and regulatory robustness" . Cell 160, no. 1-2 (2015) : 191-203.
http://dx.doi.org/10.1016/j.cell.2014.11.041
---------- MLA ----------
Crocker, J., Abe, N., Rinaldi, L., McGregor, A.P., Frankel, N., Wang, S., et al. "Low affinity binding site clusters confer HOX specificity and regulatory robustness" . Cell, vol. 160, no. 1-2, 2015, pp. 191-203.
http://dx.doi.org/10.1016/j.cell.2014.11.041
---------- VANCOUVER ----------
Crocker, J., Abe, N., Rinaldi, L., McGregor, A.P., Frankel, N., Wang, S., et al. Low affinity binding site clusters confer HOX specificity and regulatory robustness. Cell. 2015;160(1-2):191-203.
http://dx.doi.org/10.1016/j.cell.2014.11.041