Interaction of the BELL-like protein ATH1 with DNA: role of homeodomain residue 54 in specifying the different binding properties of BELL and KNOX proteins
-
Abstract
We have studied the interaction of the BELL-like Arabidopsis homeodomain protein ATH1 with DNA. Analysis of oligonucleotides selected by the ATH1 homeodomain from a random mixture suggests that ATH1 preferentially binds the sequence TGACAGGT. Single nucleotide replacements at positions 2 or 3 of this sequence abolish binding, while changes at position 4 are more tolerated. Changes outside this core differentially affect binding, depending on the position. Hydroxyl radical footprinting and missing nucleoside experiments showed that ATH1 interacts with a 7-bp region of the strand carrying the GAC core. On the other strand, protection was observed over a 7-bp region, comprising one additional nucleotide complementary to T in position 1. A comparative analysis of the binding preferences of the homeodomains of ATH1 and STM (a KNOX homeodomain protein) indicated that they bind similar sequences, but with differences in affinity and specificity. The decreased affinity displayed by the ATH1 homeodomain correlates with the presence of valine (instead of lysine as in STM) at position 54. This difference also explains the decreased and increased selectivities, respectively, at positions 4 and 5. Our results point to an essential role of residue 54 in determining the different binding properties of BELL and KNOX homeodomains.
References
Bellaoui, M., Pidkowich, M.S., Samach, A., Kushalappa, K., Kohalmi, S.E., Modrusan, Z., Crosby, W.L., and Haughn, G.W. (2001). The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals. Plant Cell13, 2455–2470.10.1105/tpc.010161Suche in Google Scholar
Bhatt, A.M., Etchells, J.P., Canales, C., Lagodienko, A., and Dickinson, H. (2004). VAAMANA-a BEL1-like homeodomain protein, interacts with KNOX proteins BP and STM and regulates inflorescence stem growth in Arabidopsis. Gene328, 103–111.10.1016/j.gene.2003.12.033Suche in Google Scholar
Blackwell, T.K. and Weintraub, H. (1990). Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science250, 1104–1110.10.1126/science.2174572Suche in Google Scholar
Bürglin, T.R. (1997). Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res.25, 4173–4180.10.1093/nar/25.21.4173Suche in Google Scholar
Chan, R.L., Gago, G.M., Palena, C.M., and Gonzalez, D.H. (1998). Homeoboxes in plant development. Biochim. Biophys. Acta1442, 1–19.10.1016/S0167-4781(98)00119-5Suche in Google Scholar
Chen, H., Rosin, F.M., Prat, S., and Hannapel, D.J. (2003). Interacting transcription factors from the TALE superclass regulate tuber formation. Plant Physiol.132, 1391–1404.10.1104/pp.103.022434Suche in Google Scholar
Chen, H., Banerjee, A.K., and Hannapel, D.J. (2004). The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J.38, 276–284.10.1111/j.1365-313X.2004.02048.xSuche in Google Scholar
Dixon, W.J., Hayes, J.J., Levin, J.R., Weidner, M.F., Dombroski, B.A., and Tullius, T.D. (1991). Hydroxyl radical footprinting. Methods Enzymol.208, 380–413.10.1016/0076-6879(91)08021-9Suche in Google Scholar
Gehring, W.J. (1987). Homeo boxes in the study of development. Science236, 1245–1252.10.1126/science.2884726Suche in Google Scholar PubMed
Gehring, W.J., Affolter, M., and Bürglin, T. (1994a). Homeodomain proteins. Annu. Rev. Biochem.63, 487–526.10.1146/annurev.bi.63.070194.002415Suche in Google Scholar PubMed
Gehring, W.J., Qian, Y.Q., Billeter, M., Furukubo-Tokunaga, K., Schier, A.F., Resendez-Perez, D., Affolter, M., Otting, G., and Wüthrich, K. (1994b). Homeodomain-DNA recognition. Cell78, 211–223.10.1016/0092-8674(94)90292-5Suche in Google Scholar
Krusell, L., Rasmussen, I., and Gausing, K. (1997). DNA binding sites recognised in vitro by a knotted class I homeodomain protein encoded by the hooded gene, k, in barley (Hordeum vulgare). FEBS Lett.408, 25–29.10.1016/S0014-5793(97)00382-7Suche in Google Scholar
LaRonde-LeBlanc, N.A. and Wolberger, C. (2003). Structure of HoxA9 and Pbx1 bound to DNA: Hox hexapeptide and DNA recognition anterior to posterior. Genes Dev.17, 2060–2072.10.1101/gad.1103303Suche in Google Scholar
Long, J.A., Moan, E.I., Medford, J.I., and Barton, M.K. (1996). A member of the knotted class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature378, 66–69.10.1038/379066a0Suche in Google Scholar
Müller, J., Wang, Y., Franzen, R., Santi, L., Salamini, F., and Rohde, W. (2001). In vitro interactions between barley TALE homeodomain proteins suggest a role for protein-protein associations in the regulation of Knox gene function. Plant J.27, 13–23.10.1046/j.1365-313x.2001.01064.xSuche in Google Scholar
Oliphant, A.R., Brandl, C.J., and Struhl, K. (1989). Defining the sequence specificity of DNA-binding proteins by selecting binding sites from random-sequence oligonucleotides: analysis of yeast GCN4 protein. Mol. Cell. Biol.9, 2944–2949.Suche in Google Scholar
Palena, C.M., Gonzalez, D.H., Guelman, S., and Chan, R.L. (1998). Expression of sunflower homeodomain containing proteins in Escherichia coli: purification and functional studies. Protein Expr. Purif.13, 97–103.10.1006/prep.1998.0875Suche in Google Scholar
Passner, J.M., Ryoo, H.D., Shen, L., Mann, R.S., and Aggarwal, A.K. (1999) Structure of a DNA-bound Ultrabithorax-Extradenticle homeodomain complex. Nature397, 714–719.10.1038/17833Suche in Google Scholar
Qian, Y.Q., Billeter, M., Otting, G., Müller, M., Gehring, W.J., and Wüthrich, K. (1989). The structure of the Antennapedia homeodomain determined by MNR spectroscopy in solution: comparison with prokaryotic repressors. Cell59, 573–580.10.1016/0092-8674(89)90040-8Suche in Google Scholar
Qian, Y.Q., Furukubo-Tokunaga, K., Müller, M., Resendez-Perez, D., Gehring, W.J., and Wüthrich, K. (1994). Nuclear magnetic resonance solution structure of the fushi tarazu homeodomain from Drosophila and comparison with the Antennapedia homeodomain. J. Mol. Biol.238, 333–345.10.1006/jmbi.1994.1296Suche in Google Scholar
Quaedvlieg, N., Dockx, J., Rook, F., Weisbeek, P., and Smeekens, S. (1995). The homeobox gene ATH1 of Arabidopsis is derepressed in the photomorphogenic mutants cop1 and det1. Plant Cell7, 117–129.Suche in Google Scholar
Reiser, L., Modrusan, Z., Margossian, L., Samach, A., Ohad, N., Haughn, G.W., and Fischer, R.L. (1995). The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell83, 735–742.10.1016/0092-8674(95)90186-8Suche in Google Scholar
Sedmak, J. and Grossberg, S. (1977). A rapid, sensitive, and versatile assay for protein using Coomassie brilliant blue G-250. Anal. Biochem.79, 544–552.10.1016/0003-2697(77)90428-6Suche in Google Scholar
Seki, M., Narusaka, M., Kamiya, A., Ishida, J., Satou, M., Sakurai, T., Nakajima, M., Enju, A., Akiyama, K., Oono, Y., et al. (2002). Functional annotation of a full-length Arabidopsis cDNA collection. Science296, 141–145.10.1126/science.1071006Suche in Google Scholar
Smith, H.M.S., Boschke, I., and Hake, S. (2002). Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity. Proc. Natl. Acad. Sci. USA99, 9579–9584.10.1073/pnas.092271599Suche in Google Scholar
Smith, D.B. and Johnson, K.S. (1988). Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene67, 31–40.10.1016/0378-1119(88)90005-4Suche in Google Scholar
Tioni, M.F., Viola, I.L., Chan, R.L., and Gonzalez, D.H. (2005). Site-directed mutagenesis and footprinting analysis of the interaction of the sunflower KNOX protein HAKN1 with DNA. FEBS J.272, 190–202.10.1111/j.1432-1033.2005.04402.xSuche in Google Scholar
Tsao, D.H.H., Gruschus, J.M., Wang, L., Nirenberg, M., and Ferretti, J.A. (1995). The three-dimensional solution structure of the NK-2 homeodomain from Drosophila. J. Mol. Biol.251, 297–307.10.1006/jmbi.1995.0435Suche in Google Scholar PubMed
Vollbrecht, E., Veit, B., Sinha, N., and Hake, S. (1991). The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature350, 241–243.10.1038/350241a0Suche in Google Scholar PubMed
©2006 by Walter de Gruyter Berlin New York
Artikel in diesem Heft
- Editor's Note
- Endothelial mediators and communication through vascular gap junctions
- Bradykinin and peripheral sensitization
- Renal gene expression profiling using kinin B1 and B2 receptor knockout mice reveals comparable modulation of functionally related genes
- Solvent-induced changes in photochemical activity and conformation of photosystem I particles by glycerol
- Interaction of the BELL-like protein ATH1 with DNA: role of homeodomain residue 54 in specifying the different binding properties of BELL and KNOX proteins
- Vitamin B1de novo synthesis in the human malaria parasite Plasmodium falciparum depends on external provision of 4-amino-5-hydroxymethyl-2-methylpyrimidine
- Ecto- and cytosolic 5′-nucleotidases in normal and AMP deaminase-deficient human skeletal muscle
- Dual signal transduction mediated by a single type of olfactory receptor expressed in a heterologous system
- Modulation of autocrine TNF-α-stimulated matrix metalloproteinase 9 (MMP-9) expression by mitogen-activated protein kinases in THP-1 monocytic cells
- The PAK1 autoregulatory domain is required for interaction with NIK in Helicobacter pylori-induced NF-κB activation
- Aflatoxin B1-induced toxicity in HepG2 cells inhibited by carotenoids: morphology, apoptosis and DNA damage
- Detection of prion particles in samples of BSE and scrapie by fluorescence correlation spectroscopy without proteinase K digestion
- A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: greater RNA than DNA oxidation in rat liver after doxorubicin administration
- NF-κB contributes to transcription of placenta growth factor and interacts with metal responsive transcription factor-1 in hypoxic human cells
Artikel in diesem Heft
- Editor's Note
- Endothelial mediators and communication through vascular gap junctions
- Bradykinin and peripheral sensitization
- Renal gene expression profiling using kinin B1 and B2 receptor knockout mice reveals comparable modulation of functionally related genes
- Solvent-induced changes in photochemical activity and conformation of photosystem I particles by glycerol
- Interaction of the BELL-like protein ATH1 with DNA: role of homeodomain residue 54 in specifying the different binding properties of BELL and KNOX proteins
- Vitamin B1de novo synthesis in the human malaria parasite Plasmodium falciparum depends on external provision of 4-amino-5-hydroxymethyl-2-methylpyrimidine
- Ecto- and cytosolic 5′-nucleotidases in normal and AMP deaminase-deficient human skeletal muscle
- Dual signal transduction mediated by a single type of olfactory receptor expressed in a heterologous system
- Modulation of autocrine TNF-α-stimulated matrix metalloproteinase 9 (MMP-9) expression by mitogen-activated protein kinases in THP-1 monocytic cells
- The PAK1 autoregulatory domain is required for interaction with NIK in Helicobacter pylori-induced NF-κB activation
- Aflatoxin B1-induced toxicity in HepG2 cells inhibited by carotenoids: morphology, apoptosis and DNA damage
- Detection of prion particles in samples of BSE and scrapie by fluorescence correlation spectroscopy without proteinase K digestion
- A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: greater RNA than DNA oxidation in rat liver after doxorubicin administration
- NF-κB contributes to transcription of placenta growth factor and interacts with metal responsive transcription factor-1 in hypoxic human cells
