Structural basis for sequence specific DNA binding and protein dimerization of HOXA13

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Zhang, Yonghong ^a   Larsen, Christine A ^b,c   Stadler, H Scott ^b,c   Ames, James B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c SHRINERS HOSPITAL FOR CHILDREN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANTENNAPEDIA PROTEIN; DIMER; DNA BINDING PROTEIN; ENGRAILED PROTEIN; HOMODIMER; HOXA13 DNA BINDING PROTEIN; LUCIFERASE; METHYL GROUP; MUTANT PROTEIN; PYRIMIDINE; THYMINE; TRANSCRIPTION FACTOR HOXA9; TRANSCRIPTION FACTOR HOXB1; TRANSCRIPTION FACTOR PDX 1; UNCLASSIFIED DRUG; DNA; HOMEOBOX PROTEIN HOXA13; HOMEODOMAIN PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; DISSOCIATION CONSTANT; DNA BINDING; DNA HELIX; DNA PROTEIN COMPLEX; DNA SEQUENCE; DNA TRANSCRIPTION; GENE MUTATION; HOX GENE; HOXA13 GENE; HYDROGEN BOND; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; MOLECULAR WEIGHT; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SITE DIRECTED MUTAGENESIS; WILD TYPE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; DIMERIZATION; DNA; HOMEODOMAIN PROTEINS; HYDROGEN BONDING; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MUTAGENESIS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 79960935110     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023069     Document Type: Article

References (55)

1. Krumlauf R, (1994) Hox genes in vertebrate development. Cell 78: 191-201.
2. Mortlock DP, Innis JW, (1997) Mutation of HOXA13 in hand-foot-genital syndrome. Nat Genet 15: 179-180.
3. Innis JW, Goodman FR, Bacchelli C, Williams TM, Mortlock DP, et al. (2002) A HOXA13 allele with a missense mutation in the homeobox and a dinucleotide deletion in the promoter underlies Guttmacher syndrome. Hum Mutat 19: 573-574.
4. Jorgensen EM, Ruman JI, Doherty L, Taylor HS, (2009) A novel mutation of HOXA13 in a family with hand-foot-genital syndrome and the role of polyalanine expansions in the spectrum of Müllerian fusion anomalies. Fertil Steril 94: 1235-1238.
5. Shaut C, Keene D, Sorensen L, Li D, Stadler H, (2008) HOXA13 Is essential for placental vascular patterning and labyrinth endothelial specification. PLoS Genet 4: e1000073.
6. Knosp WM, Scott V, Bachinger HP, Stadler HS, (2004) HOXA13 regulates the expression of bone morphogenetic proteins 2 and 7 to control distal limb morphogenesis. Development 131: 4581-4592.
7. Morgan E, Nguyen S, Scott V, Stadler H, (2003) Loss of Bmp7 and Fgf8 signaling in Hoxa13-mutant mice causes hypospadia. Development 130: 3095-3109.
8. Knosp WM, Saneyoshi C, Shou S, Bachinger HP, Stadler HS, (2007) Elucidation, quantitative refinement, and in vivo utilization of the HOXA13 DNA binding site. J Biol Chem 282: 6843-6853.
9. Piper DE, Batchelor AH, Chang CP, Cleary ML, Wolberger C, (1999) Structure of a HoxB1-Pbx1 Heterodimer Bound to DNA: Role of the Hexapeptide and a Fourth Homeodomain Helix in Complex Formation. Cell 96: 587-597.
10. Shanmugam K, Green N, Rambaldi I, Saragovi H, Featherstone M, (1999) PBX and MEIS as non-DNA-binding partners in trimeric complexes with HOX proteins. J Biol Chem 272: 19081-19087.
11. Shen W, Montgomery J, Rozenfeld S, Moskow J, Lawrence H, et al. (1997) AbdB-like Hox proteins stabilize DNA binding by the Meis1 homeodomain proteins. Mol Cell Biol 17: 6448-6458.
12. Shanmugam K, Featherstone M, Saragovi H, (1997) Residues flanking the HOX YPWM motif contribute to cooperative interactions with PBX. J Biol Chem 272: 19081-19087.
13. Shen W, Chang C, Rozenfeld S, Sauvageau G, Humphries R, et al. (1996) Hox homeodomain proteins exhibit selective complex stabilities with Pbx and DNA. Nucleic Acids Res 24: 898-906.
14. Zhang Y, Thornburg CK, Stadler HS, Ames JB, (2009) (1)H, (15)N, and (13)C chemical shift assignments of mouse HOXA13 DNA binding domain. Biomol NMR Assign 3: 199-201.
15. Longo A, Guanga GP, Rose RB, (2007) Structural basis for induced fit mechanisms in DNA recognition by the Pdx1 homeodomain. Biochemistry 46: 2948-2957.
16. Billeter M, Qian YQ, Otting G, Muller M, Gehring W, et al. (1993) Determination of the nuclear magnetic resonance solution structure of an Antennapedia homeodomain-DNA complex. J Mol Biol 234: 1084-1093.
17. Fraenkel E, Pabo CO, (1998) Comparison of X-ray and NMR structures for the Antennapedia homeodomain-DNA complex. Nat Struct Biol 5: 692-697.
18. Fraenkel E, Rould MA, Chambers KA, Pabo CO, (1998) Engrailed homeodomain-DNA complex at 2.2 A resolution: a detailed view of the interface and comparison with other engrailed structures. J Mol Biol 284: 351-361.
19. Kissinger CR, Liu BS, Martin-Blanco E, Kornberg TB, Pabo CO, (1990) Crystal structure of an engrailed homeodomain-DNA complex at 2.8 A resolution: a framework for understanding homeodomain-DNA interactions. Cell 63: 579-590.
20. LaRonde NA, Wolberger C, (2003) Structure of HoxA9 and Pbx1 bound to DNA: Hox hexapeptide and DNA recognition anterior to posterior. Genes Dev 17: 2060-2072.
21. Altieri AS, Hinton DP, Byrd RA, (1995) Association of biomolecular systems via pulsed field gradient NMR self-diffusion measurements. J Am Chem Soc 117: 7566-7567.
22. Shaut C, Saneyoshi C, Morgan E, Knosp W, Sexton D, et al. (2007) HOXA13 Directly Regulates EphA7 and EphA6 Expression in the Genital Tubercle Vascular Endothelia. Dev Dyn 236: 951-960.
23. Zhang Y, Thornburg CK, Stadler HS, Ames JB, (2010) Backbone chemical shift assignments of mouse HOXA13 DNA binding domain bound to duplex DNA. Biomol NMR Assign 4: 97-99.
24. Parker L, Mangwani J, Wakeling E, Singh D, (2011) Hallux valgus interphalangeus and a novel mutation in HOXA13. Part of thebroadening spectrum of Hand-Foot-Genital syndrome. Foot and Ankle Surgery 17: e28-e30.
25. Treisman J, Gonczy P, Vashishtha M, Harris E, Desplan C, (1989) A single amino acid can determine the DNA binding specificity of homeodomain proteins. Cell 59: 553-562.
26. Fromental-Ramain C, Warot X, Messadecq N, LeMeur M, Dolle P, et al. (1996) Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 122: 2997-3011.
27. Stadler H, Higgins K, Capecchi M, (2001) Loss of Eph-receptor expression correlates with loss of cell adhesion and chondrogenic capacity in Hoxa13 mutant limbs. Development 128: 4177-4188.
28. Weatherbee S, Halder G, Kim J, Hudson A, Carroll S, (1998) Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev 12: 1474-1482.
29. Szerlong H, Saha A, Cairns BR, (2003) The nuclear actin-related proteins Arp7 and Arp9: a dimeric module that cooperates with architectural proteins for chromatin remodeling. EMBO J 22: 3175-3187.
30. Innis JW, Mortlock DP, Chen Z, Ludwig M, Williams ME, et al. (2004) Polyalanine expansion in HOXA13: three new affected families and the molecular consequences in a mouse model. Hum Mol Genet 13: 2841-2851.
31. Utsch B, Becker K, Brock D, Lentze MJ, Bidlingmaier F, et al. (2002) A novel stable polyalanine [poly(A)] expansion in the HOXA13 gene associated with hand-foot-genital syndrome: proper function of poly(A)-harbouring transcription factors depends on a critical repeat length? Hum Genet 110: 488-494.
32. Jorgensen EM, Ruman JI, Doherty L, Taylor CW, (2010) A novel mutation of HOXA13 in a family with hand-foot-genital syndrome and the role of polyalanine expansions in the spectrum of Müllerian fusion anomalies. Fertil Steril 94: 1235-1238.
33. Utsch B, McCabe CD, Galbraith K, Gonzalez R, Born M, et al. (2007) Molecular characterization of HOXA13 polyalanine expansion proteins in hand-foot-genital syndrome. Am J Med Genet A 143: 3161-3168.
34. Albrecht AN, Kornak U, Boddrich A, Suring K, Robinson PN, et al. (2004) A molecular pathogenesis for transcription factor associated poly-alanine tract expansions. Hum Mol Genet 13: 2351-2359.
35. Williams T, Williams M, Innis J, (2005) Range of HOX/TALE superclass associations and protein domain requirements for HOXA13:MEIS interaction. Dev Biol 277: 457-471.
36. Williams T, Williams M, Heaton J, Gelehrter T, Innis J, (2005) Group 13 HOX proteins interact with the MH2 domain of R-Smads and modulate Smad transcriptional activation functions independent of HOX DNA-binding capability. Nucleic Acids Res 33: 4475-4484.
37. Sivashanmugam A, Murray V, Cui C, Zhang Y, Wang J, et al. (2009) Practical protocol for production of very high-yields of recombinant proteins using Eschericia coli. Protein Sci 18: 936-948.
38. Wyatt PJ, (1991) Combined differential light scattering with various liquid chromatography separation techniques. Biochem Soc Trans 19: 485.
39. Meyer M, Morganstern B, (2003) Characterization of gelatine and acid soluble collagen by size exclusion chromatography coupled with multi angle light scattering (SEC-MALS). Biomacromolecules 4: 1727-1732.
40. Neri D, Szyperski T, Otting G, Senn H, Wuthrich K, (1989) Stereospecific nuclear magnetic resonance assignments of the methyl groups of valine and leucine in the DNA-binding domain of the 434 repressor by biosynthetically directed fractional 13C labeling. Biochemistry 28: 7510-7516.
41. Lee W, Revington MJ, Arrowsmith C, Kay LE, (1994) A pulsed field gradient isotope-filtered 3D 13C HMQC-NOESY experiment for extracting intermolecular NOE contacts in molecular complexes. FEBS Lett 350: 87-90.
42. Delaglio F, Grzesiek S, Vuister GW, Zhu G, J P, et al. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
43. Ottinger M, Delaglio F, Bax A, (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J Magn Reson 131: 373-378.
44. Zweckstetter M, (2008) NMR: prediction of molecular alignment from structure using the PALES software. Nat Protoc 3: 679-690.
45. Farrow NA, Muhandiram R, Singer AU, Pascal SM, Kay CM, et al. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33: 5984-6003.
46. Freedberg DI, Ishima R, Jacob J, Wang YX, Torchia DA, (2002) Rapid structural fluctuations of the free HIV protease flaps in solution: relationship to crystal structures and comparison with predictions of dynamics calculations. Protein Sci 11: 221-232.
47. Clore GM, Gronenborn AM, (1997) NMR structures of proteins and protein complexes beyond 20,000 M(r). Nat Struct Biol 4: 849-853.
48. Nilges M, Gronenborn AM, Brunger AT, Clore GM, (1988) Determination of three-dimensional structures of proteins by simulated annealing with interproton distance restraints. Application to crambin, potato carboxypeptidase inhibitor and barley serine proteinase inhibitor 2. Protein Eng 2: 27-38.
49. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM, (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160: 65-73.
50. Bagby S, Harvey TS, Eagle SG, Inouye S, Ikura M, (1994) NMR-derived three-dimensional solution structure of protein S complexed with calcium. Structure 2: 107-122.
51. Dominguez C, Boelens R, Bonvin AM, (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125: 1731-1737.
52. van Dijk M, Bonvin AM, (2009) 3D-DART: a DNA structure modelling server. Nucleic Acids Res 37: W235-W239.
53. van Dijk M, van Dijk AD, Hsu V, Boelens R, Bovin AM, (2006) Information-driven protein-DNA docking using HADDOCK: it is a matter of flexibility. Nucleic Acids Res 34: 3317-3325.
54. Osawa M, Dace A, Tong KI, Valiveti A, Ikura M, et al. (2005) Mg2+ and Ca2+ differentially regulate DNA binding and dimerization of DREAM. J Biol Chem 280: 18008-18014.
55. Xu X, Xu W, Rayo J, Ishida Y, Leal WS, et al. (2010) NMR structure of navel orangeworm moth pheromone-binding protein (AtraPBP1): implications for pH-sensitive pheromone detection. Biochemistry 49: 1469-1476.