Roles for intrinsic disorder and fuzziness in generating context-specific function in ultrabithorax, a Hox transcription factor

Advances in Experimental Medicine and Biology

Volumn 725, Issue , 2012, Pages 86-105

  Bondos, Sarah E ^a   Hsiao, Hao Ching ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; HOX PROTEIN; INTINSICALLY DISORDERED PROTEIN; MESSENGER RNA; TRANSCRIPTION FACTOR; ULTRABITHORAX PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; UBX PROTEIN, DROSOPHILA;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; BONE DISEASE; CARBOXY TERMINAL SEQUENCE; GENE REPRESSION; GENETIC CONSERVATION; HUMAN; IN VITRO STUDY; INTRACELLULAR SIGNALING; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEFECT; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; STRUCTURE ANALYSIS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; CHEMISTRY; DROSOPHILA MELANOGASTER; METABOLISM; REVIEW;

ANIMALIA;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HOMEODOMAIN PROTEINS; TRANSCRIPTION FACTORS;

EID: 84859510055     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-0659-4_6     Document Type: Article

References (101)

1. KriwackiRW,HengstL,TennantLetal. Structuralstudiesofp21Wafl/Cipl/Sdil inthefreeandCdk2-bound state: conformational disordermediatesbinding diversity. Proc Natl AcadSci USA 1996; 93:11504-11509.
2. Tompa P, Szasz C, Buday L. Structural disorder throws new light on moonlighting. Trends Biochem Sci 2005; 30:484-489.
3. Romero PR, Zaidi S, Fang YY et al. Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proc Natl Acad Sci USA 2006; 103:8390-8395.
4. Vilasi S, Ragone R. Abundance of intrinsic disorder in SV-IV, a multifunctional androgen-dependent protein secreted from rat seminar vesicle. FEBS J 2008; 275:763-774.
5. Iakoucheva LM, Radivojac P, Brown CJ etal. The importance of intrinsic disorder for protein phosphorylation. Nucl Acids Res 2004; 32:1037-1049.
6. Lu X, Hamkalo B, Parseghian MH et al. Chromatin condensing functions of the linker histone C-terminal domain are mediated by specific amino acid composition and intrinsic protein disorder. Biochemistry 2009; 48:164-172.
7. Sandhu KS. Intrinsic disorder explains diverse nuclear roles of chromatin remodeling proteins. J Mol Recognit 2009; 22:1-8.
8. Galea CA, Wang Y, Sivakolundu SG et al. Regulation of cell division by intrinsically unstructured proteins: intrinsic flexibility, modularity and signaling conduits. Biochemistry 2008; 47:7598-7609.
9. Liu Y, Matthews KS, Bondos SE. Multiple intrinsically disordered sequences alter DNA binding by the homeodomain of the Drosophila Hox protein Ultrabithorax. J Biol Chem 2008; 283:20874-20887.
10. Liu Y, Matthews KS, Bondos SE. Internal regulatory interactions determine DNA binding specificity by a Hox transcription factor. J Mol Biol 2009; 390:760-774.
11. Phng LK, Gerhardt H.Angiogenesis: a team effort coordinated by Notch. Dev Cell 2009; 16:196-208.
12. Liu J, Perumal NB, Oldfield CJet al. Intrinsic disorder in transcription factors. Biochemistry 2006; 45:6873-6888.
13. Ward JJ, Sodhi JS, McGuffinLJet al. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 2004; 337:635-645.
14. Tompa P, Fuxreiter M. Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem Sci 2008; 33:2-8.
15. Halder G, Callaerts P, Gehring WJ. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 1995; 267:1788-1792.
16. Lo PCH, Frasch M. Establishing A-P polarity in the embryonic heart tube: a conserved function of Hox genes in Drosophila and vertebrates. Trends Cardiovasc Med 2003; 13:182-187.
17. Hughes CL, Kaufman TC.Hoxgenesandtheevolutionofthe arthropod body plan. EvolDev2002; 4:459-499.
18. Lewis EB. A gene complex controlling segmentation in Drosophila. Nature 1978; 276:565-570.
19. Gellon G, McGinnis W. Shaping animal body plans in development and evolution by modulation of Hox expression patterns. Bio Essays 1998; 20:116-125.
20. Pearson JC, Lemons D, McGinnis W. Modulating Hox gene functions during animal body patterning. Nature Rev Genet 2005; 6:893-904.
21. Bondos SE, Tan XX. Combinatorial transcription regulation: the interaction of transcription factors and cell signaling molecules with homeodomain proteins in Drosophila development. Crit Rev Euk Gene Express 2001; 11:145-171.
22. Mann RS, Lelli KM, Joshi R. Hox specificity: unique roles for cofactors and collaborators. Curr Topics Dev Biol 2009; 88:63-101.
23. Bienz M. Homeotic genes and positional signaling in the Drosophila viscera. Trends Genet 1994; 10:22-26.
24. Rivilin PK, Gong A, Schneiderman AM et al. The role ofUltrabithorax in the patterning ofadult thoracic muscles in Drosophila melanogaster. Dev Genes Evol 2001; 211:55-66.
25. Rogulja-Ortmann A, Renner S, Technau GM. Antagonistic roles for Ultrabithorax and Antennapedia in regulating segment-speciic apoptosis ofdifferentiated motoneurons in the Drosophila embryonic central nervous system. Development 2008; 135:3435-3445.
26. Graba Y, Aragnol D, Pradel J. Drosophila Hox complex downstream targets and the function ofhomeotic genes. BioEssays 1997; 19:379-388.
27. Capovilla M, Brandt M, Botas J. Direct regulation of decapentaplegic by Ultrabithorax and its role in Drosophila midgut morphogenesis. Cell 1994; 76:461-475.
28. de Navas LF, Garulet DL, Sanchez-Herrero E. The Ultrabithorax Hox gene of Drosophila controls haltere size by regulating the Dpp pathway. Development 2006; 133:4495-4506.
29. Weatherbee SD, Halder G, Kim J et al. Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev 1998; 12:1474-1482.
30. Bondos SE, Catanese DJ Jr, Tan XX et al. Hox transcription factor Ultrabithorax Ib physically and genetically interacts with Disconnected Interacting Protein 1, a double-stranded RNA-binding protein. J Biol Chem 2004; 279:26433-26444.
31. Bondos SE, Tan XX, Matthews KS.Physical and genetic interactions link Hox function with diverse transcription factors and cell signaling proteins. Mol Cell Proteomics 2006; 5:824-834.
32. Chan SK, Jaffe L, Capovilla M et al. The DNA binding speciicity of Ultrabithorax is modulated by cooperative interactions with Extradenticle, another homeoprotein. Cell 1994; 78:603-615.
33. Tan XX, Bondos S, Li L et al. Transcription activation by Ultrabithorax Ib requires a predicted a-helical region. Biochemistry 2002; 41:2774-2785.
34. Lopez AJ, Artero RD, Perez-Alonso M. Stage, tissue and cell specific distribution of alternative Ultrabithorax mRNAs and protein isoforms in the Drosophila embryo. Roux's Arch Dev Biol 1996; 205:450-459.
35. Mann RS, Hogness DS. Functional dissection of Ultrabithorax proteins in D. melanogaster. Cell 1990; 60:597-610.
36. Subramaniam V, Bomze HM, Lopez AJ. Functional differences between Ultrabithorax protein isoforms in Drosophila melanogaster: evidence from elimination, substitution and ectopic expression of speciic isoforms. Genetics 1994; 136:979-991.
37. Reed HC, Hoare T, Thomsen S. Alternative splicing modulates Ubx protein function in Drosophila melanogaster. Genetics 2010; 184:745-758.
38. Bomze HM, Lopez AJ. Evolutionary conservation of the structure and expression ofalternatively spliced Ultrabithorax isoforms from Drosophila. Genetics 1994; 136:965-977.
39. Merabet S, Hudry B, Saadaoui M et al. Classification of sequence signatures: a guide to Hox protein function. BioEssays 2009; 31:500-511.
40. Jones DT,Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Compt Appl Biosci 1992; 8:275-282.
41. White SH. Global statistics of protein sequences: implications for the origin, evolution and prediction of protein structure. Annu Rev Biophys Biomol Struct 1994; 23:407-439.
42. Tourasse NJ, Li WH. Selective constraints, amino acid composition and the rate of protein evolution. Mol Biol Evol 2000; 17:656-664.
43. Brooks DJ, Fresco JR. Increasedfrequency ofcysteine, tyrosine and phenylalanine since the lastuniversal ancestor. Mol Cell Proteomics 2002; 1:125-131.
44. Hubbard S, Benyon RJ. Proteolysis ofnative proteins as a structural probe. In: Benyon R, Bonds JS, eds. Proteolytic Enzymes, 2nd edition. Oxford: Oxford University Press, 2001:248-249.
45. López AJ,HognessDS. Immunochemical dissectionoftheUltrabithoraxhomeoproteinfamilyinDrosophila melanogaster. Proc Natl Acad Sci USA 1991; 88:9924-9928.
46. White RAH, Wilcox M. Protein products of the bithorax complex in Drosophila. Cell 1984; 39:163-171.
47. Hegedu″s T, Serohijos AWR, Dokholyan NV et al. Computational studies reveal phosphorylation-dependent changes in the unstructured R domain of CFTR. J Mol Biol 2008; 378:1052-1063.
48. Bondos SE, Bicknell A. Detection and prevention of protein aggregation before, during and after puriication. Anal Bioch 2003; 316:223-231.
49. Passner JM, Ryoo HD, Shen L et al. Structure ofa DNA-bound Ultrabithorax-Extradenticle homeodomain complex. Nature 1999; 397:714-719.
50. Bridges CB, Morgan TH. The third-chromosome group ofmutant characters ofDrosophila melanogaster. Publs Carnegie Instn 1923; 327:1-251.
51. Garber RL, Kuroiwa A, Gehring WJ. Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J 1983; 2:2027-2036.
52. Scott MP, Weiner AJ, Polisky BA et al. The molecular organization of the Antennapedia complex of Drosophila. Cell 1983; 35:763-776.
53. McGinnis W, Levine MS, Hafen E et al. A conserved DNA sequence in homeotic genes ofthe Drosophila antennapedia and bithorax complexes. Nature 1984; 308:428-433.
54. McGinnis W, Garber RL, Wirz J et al. A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell 1984; 37:403-408.
55. Hersh BM, Nelson CE, Stoll SJetal. The UBX-regulated network in the haltere imaginal disc of D. melanogaster. Dev Biol 2007; 302:717-727.
56. Carr A, Biggin MD. A comparison ofin vivo and in vitro DNA-binding speciicities suggests a new model for homeoprotein DNA binding in Drosophila embryos. EMBO J 1999; 18:1598-1608.
57. Mastick GS, McKay R, Oligino T et al. Identification of target genes regulated by homeotics proteins in Drosophila melanogaster through genetic selection of Ultrabithorax protein-binding sites in yeast. Genetics1995; 139:349-363.
58. Zhai Z, Stein MAS, Lohmann I.Expression of the apoptosis gene reaper in homeotic, segmentation and other mutants in Drosophila. Gene Expr Patterns 2009; 9:357-363.
59. Damante G, Pelizzari L,Esposito G et al. A molecular code dictates sequence-speciic DNA recognition by homeodomains. EMBO J 1996; 15:4992-5000.
60. Berger MF, Badis G, Gehrke AR. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 2008; 133:1266-1276.
61. Noyes MB, Christensen RG, Wakabayashi A et al. Analysis of homeodomain speciicities allows the family-wide prediction of preferred recognition sites. Cell 2008; 133:1277-1289.
62. Ekker SC, Young E, von Kessler DP et al. Optimal DNA sequence recognition by the Ultrabithorax homeodomain of Drosophila. EMBO J 1991; 10:1179-1186.
63. Ekker SC, Jackson DG, von Kessler DP et al. The degree of variation in DNA sequence recognition among four Drosophila homeotic proteins. EMBO J 1994; 13:3551-3560.
64. Frazee RW, Taylor JA, Tulius TD. Interchange ofDNA-binding modes in the deformed and Ultrabithorax homeodomain of Drosophila. EMBO J 2002; 10:1179-1186.
65. Gutmanas A, Billeter M. Specific DNA recognition by the Antp homeodomain: MD simulations of specific and nonspeciic complexes. Proteins 2004; 57:772-782.
66. Hoey T, Levine M. Divergent homeo box proteins recognize similar DNA seuqneces in Drosophila. Nature 1988; 332:858-861.
67. Kalionis B, O'Farrell PH. A universal target sequence is bound in vitro by diverse homeodomains. Mech Dev 1993; 43:57-70.
68. Gehring WJ, Qian YQ, Billeter M et al. Homeodomain-DNA recognition. Cell 1994; 78:211-223.
69. ClapierCR,CairnsBR.Thebiology ofchromatinremodelingcomplexes. AnnRevBiochem2009;78:273-304.
70. Gavis ER, Hogness DS. Phosphorylation, expression and function of the Ultrabithorax protein family in Drosophila melanogaster. Development 1991; 112:1077-1093.
71. Li L, von Kessler D, Beachy PA et al. pH-dependent enhancement ofDNA binding by the Ultrabithorax homeodomain. Biochemistry 1996; 35:9832-9839.
72. Tour E, Hittinger CT, McGinnis W. Evolutionarily conserved domains required for activation and repression functions of the Drosophila Hox protein Ultrabithorax. Development 2005; 132:5271-5281.
73. Chan SK, Pöpperl H, Krumlauf R et al. An Extradenticle-induced conformational change in a Hox protein overcomes an inhibitory function ofthe conserved hexapeptide motif. EMBO J 1996; 15:2476-2487.
74. Li X, Murre C, McGinnis W. Activity regulation of a Hox protein and a role for the homeodomain in inhibiting transcriptional activation. EMBO J 1999; 18:198-211.
75. Garza AS, Ahmad N, Kumar R. Role of intrinsically disordered protein regions/domains in transcriptional regulation. Life Sci 2009; 84:189-193.
76. Krasnow MA, Saffman EE, Kornfeld K et al. Transcriptional activation and repression by Ultrabithorax proteins in cultured Drosophila cells. Cell 1989; 57:1031-1043.
77. Galant R, Carroll SB. Evolution of a transcriptional repression domain in an insect Hox protein. Nature 2002; 415:910-913.
78. Ronshaugen M, McGinnis N, McGinnis W. Hox protein mutation and the macroevolution of the insect body plan. Nature 2002; 415:914-917.
79. Pinsonneault J, Florence B, Vaessin H et al. A model for Extradenticle-induced function as a switch that changes Hox proteins from repressors to activators. EMBO J 1997; 16:2032-2042.
80. Saleh M, Rammbaldi I, Yang XJ et al. Cell signaling switches Hox-Pbx complexes from repressors to activators of transcription. Mol Cell Biol 2000; 20:8623-8633.
81. Merabet S, Kambris Z, Capovilla M et al. The hexapeptide and linker regions of the AbdA Hox protein regulate its activating and repressive functions. Dev Cell 2003; 4:761-768.
82. Merabet S, Saadaoui M, Sambrani N et al. A unique Extradenticle recruitment mode in the Drosophila Hox protein Ultrabithorax. Proc Natl Acad Sci USA 2007; 104:16946-16951.
83. Mann RS, Chan SK. Extra speciicity from Extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet 1996; 12:258-262.
84. Mann RS, Affolter M. Hox proteins meet more partners. Curr Opin Genet Dev 1998; 8:423-429.
85. van Dijk MA, Murre C. Extradenticle raises the DNA binding specificity of homeotic selector gene products. Cell 1994; 78:617-624.
86. Heuber SD, Lohmann I. Shaping segments: Hox gene function in the genomic age. BioEssays 2008; 30:965-979.
87. Merabet S, Pradel J, Graba Y. Getting a molecular grasp on Hox contextual activity. Trends Genet 2005; 21:477-480.
88. Xu L. Regulation of Smad activities. Biochem Biophys Acta 2006; 1759:503-513.22.
89. Walsh CM, Carroll SB. Collaboration between Smads and a Hox protein in target gene repression. Development 2007; 134:3585-3592.
90. VerheyenEM,GottardiCJ.RegulationofWnt/betal- Cateninsignalingbyproteinkinases.DevDyn2010;239:34-44.
91. Johnson FB, Parker E, Krasnow MA. Extradenticle protein is a selective cofactor for the Drosophila homeotics: role of the homeodomain and YPWM amino acid motif in the interaction. Proc Natl Acad Sci USA 1995; 92:739-743.
92. Shanmugan K, Featherstone MS, Saragovi HU. Residues flanking the HOX YPWM motif contribute to cooperative interactions with PBX. J Biol Chem 1997; 272:19081-19087.
93. Asahara H, Dutta S, Kao HY et al. Pbx-Hox heterodimers recruit coactivator-corepressor complexes in an isoform-specific manner. Mol Cell Biol 1999; 19:8219-8225.
94. Haynes C, Oldfield CJ, Ji F et al. Intrinsic disorder is a common feature ofhub proteins from four eukaryotic interactomes. PLoS Comp Biol 2006; 8:890-901.
95. Hilser VJ, Thompson EB. Intrinsic disorder as a mechanism to optimize allosteric coupling in proteins. Proc Natl Acad Sci USA 2007; 104:8311-8315.
96. Dunker AK, Cortese MS, Romero P. Flexible nets: the roles of intrinsic disorder in protein interaction networks. FEBS J 2005; 272:5129-5148.
97. Hall J, Karplus PA, BarbarE. Multivalency inthe assembly of intrinsically disordered dyneinintermediate chain. J Biol Chem 2009; 48:33115-33121.
98. Beachy PA, Varkey J, Young KE etal. Cooperative binding of an Ultrabithorax homeodomain protein to nearby and distant DNA sites. Mol Cell Biol 1993; 13:6941-6956.
99. Gebelein B, Culi J, Ryoo HD et al. Specificity of Distalless repression and limb primordia development by Abdominal Hox proteins. Dev Cell 2002; 3:487-498.
100. Gebelein B, McKay DJ, Mann RS. Direct integration of Hox and segmentation gene inputs during Drosophila development. Nature 2004; 431:653-659.
101. Sun B, Hursh DA, Jackson D etal. Ultrabithorax protein is necessary but not suficient for full activation of decapentaplegic expression in the visceral mesoderm. EMBO J 1995; 14:520-535.