A Derived Allosteric Switch Underlies the Evolution of Conditional Cooperativity between HOXA11 and FOXO1

Cell Reports

Volumn 15, Issue 10, 2016, Pages 2097-2108

  Nnamani, Mauris C ^a   Ganguly, Soumya ^b   Erkenbrack, Eric M ^a   Lynch, Vincent J ^c   Mizoue, Laura S ^d   Tong, Yingchun ^a   Darling, Heather L ^b   Fuxreiter, Monika ^e   Meiler, Jens ^b   Wagner, Günter P ^a,f,g  

^a YALE UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d UNIVERSITY OF COLORADO   (United States)

^e UNIVERSITY OF DEBRECEN   (Hungary)

^f YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA PK KINASE; PHOSPHOTRANSFERASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR HOXA11; UNCLASSIFIED DRUG; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; DNA DEPENDENT PROTEIN KINASE; HOMEODOMAIN PROTEIN; HOXA11 PROTEIN, MOUSE; INTRINSICALLY DISORDERED PROTEIN; PROTEIN BINDING;

ALLOSTERIC SWITCH; ALLOSTERISM; ALPHA HELIX; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; INTERNAL REGULATORY DOMAIN; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REGULATORY MOTIF; TRANSACTIVATION DOMAIN; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; EVOLUTION; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MOLECULAR MODEL; PHOSPHORYLATION; PROTEIN SECONDARY STRUCTURE;

ALLOSTERIC REGULATION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BIOLOGICAL EVOLUTION; CREB-BINDING PROTEIN; DNA-ACTIVATED PROTEIN KINASE; FORKHEAD BOX PROTEIN O1; HELA CELLS; HOMEODOMAIN PROTEINS; HUMANS; INTRINSICALLY DISORDERED PROTEINS; MICE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN DOMAINS; PROTEIN STRUCTURE, SECONDARY; TRANSCRIPTIONAL ACTIVATION;

EID: 84969920170     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.04.088     Document Type: Article

References (66)

1. Baëza M., Viala S., Heim M., Dard A., Hudry B., Duffraisse M., Rogulja-Ortmann A., Brun C., Merabet S. Inhibitory activities of short linear motifs underlie Hox interactome specificity in vivo. eLife 2015, 4:4.
2. Bannister A.J., Oehler T., Wilhelm D., Angel P., Kouzarides T. Stimulation of c-Jun activity by CBP: c-Jun residues Ser63/73 are required for CBP induced stimulation in vivo and CBP binding in vitro. Oncogene 1995, 11:2509-2514.
3. Bartlett M.E., Whipple C.J. Protein change in plant evolution: tracing one thread connecting molecular and phenotypic diversity. Front. Plant Sci. 2013, 4:382.
4. Bei L., Lu Y., Bellis S.L., Zhou W., Horvath E., Eklund E.A. Identification of a HoxA10 activation domain necessary for transcription of the gene encoding beta3 integrin during myeloid differentiation. J. Biol. Chem. 2007, 282:16846-16859.
5. Brayer K.J., Lynch V.J., Wagner G.P. Evolution of a derived protein-protein interaction between HoxA11 and Foxo1a in mammals caused by changes in intramolecular regulation. Proc. Natl. Acad. Sci. USA 2011, 108:E414-E420.
6. Buchan D.W., Ward S.M., Lobley A.E., Nugent T.C., Bryson K., Jones D.T. Protein annotation and modelling servers at University College London. Nucleic Acids Res. 2010, 38:W563-W568.
7. Campbell K.M., Lumb K.J. Structurally distinct modes of recognition of the KIX domain of CBP by Jun and CREB. Biochemistry 2002, 41:13956-13964.
8. Carroll S.B. Evolution at two levels: on genes and form. PLoS Biol. 2005, 3:e245.
9. Carroll S.B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 2008, 134:25-36.
10. Chariot A., Gielen J., Merville M.-P., Bours V. The homeodomain-containing proteins: an update on their interacting partners. Biochem. Pharmacol. 1999, 58:1851-1857.
11. Cheatle Jarvela A.M., Hinman V.F. Evolution of transcription factor function as a mechanism for changing metazoan developmental gene regulatory networks. Evodevo 2015, 6:3.
12. Choe S.K., Lu P., Nakamura M., Lee J., Sagerström C.G. Meis cofactors control HDAC and CBP accessibility at Hox-regulated promoters during zebrafish embryogenesis. Dev. Cell 2009, 17:561-567.
13. Dai P., Akimaru H., Tanaka Y., Hou D.X., Yasukawa T., Kanei-Ishii C., Takahashi T., Ishii S. CBP as a transcriptional coactivator of c-Myb. Genes Dev. 1996, 10:528-540.
14. Das R., André I., Shen Y., Wu Y., Lemak A., Bansal S., Arrowsmith C.H., Szyperski T., Baker D. Simultaneous prediction of protein folding and docking at high resolution. Proc. Natl. Acad. Sci. USA 2009, 106:18978-18983.
15. Davidson E.H. The Regulatory Genome: Gene Regulatory Networks in Development and Evolution 2006, Academic Press.
16. Davis A.P., Witte D.P., Hsieh-Li H.M., Potter S.S., Capecchi M.R. Absence of radius and ulna in mice lacking hoxa-11 and hoxd-11. Nature 1995, 375:791-795.
17. Dyson H.J., Wright P.E. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 2005, 6:197-208.
18. Ernst P., Wang J., Huang M., Goodman R.H., Korsmeyer S.J. MLL and CREB bind cooperatively to the nuclear coactivator CREB-binding protein. Mol. Cell. Biol. 2001, 21:2249-2258.
19. Ferreon A.C., Ferreon J.C., Wright P.E., Deniz A.A. Modulation of allostery by protein intrinsic disorder. Nature 2013, 498:390-394.
20. Fleishman S.J., Leaver-Fay A., Corn J.E., Strauch E.M., Khare S.D., Koga N., Ashworth J., Murphy P., Richter F., Lemmon G., et al. RosettaScripts: a scripting language interface to the Rosetta macromolecular modeling suite. PLoS ONE 2011, 6:e20161.
21. Fuxreiter M., Simon I., Friedrich P., Tompa P. Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J. Mol. Biol. 2004, 338:1015-1026.
22. Galant R., Carroll S.B. Evolution of a transcriptional repression domain in an insect Hox protein. Nature 2002, 415:910-913.
23. Giordano A., Avantaggiati M.L. p300 and CBP: partners for life and death. J. Cell. Physiol. 1999, 181:218-230.
24. Goodman R.H., Smolik S. CBP/p300 in cell growth, transformation, and development. Genes Dev. 2000, 14:1553-1577.
25. Goto N.K., Zor T., Martinez-Yamout M., Dyson H.J., Wright P.E. Cooperativity in transcription factor binding to the coactivator CREB-binding protein (CBP). The mixed lineage leukemia protein (MLL) activation domain binds to an allosteric site on the KIX domain. J. Biol. Chem. 2002, 277:43168-43174.
26. Grenier J.K., Carroll S.B. Functional evolution of the Ultrabithorax protein. Proc. Natl. Acad. Sci. USA 2000, 97:704-709.
27. Grens A., Mason E., Marsh J.L., Bode H.R. Evolutionary conservation of a cell fate specification gene: the Hydra achaete-scute homolog has proneural activity in Drosophila. Development 1995, 121:4027-4035.
28. Halder G., Callaerts P., Gehring W.J. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 1995, 267:1788-1792.
29. Hsia C.C., McGinnis W. Evolution of transcription factor function. Curr. Opin. Genet. Dev. 2003, 13:199-206.
30. Hsieh-Li H.M., Witte D.P., Weinstein M., Branford W., Li H., Small K., Potter S.S. Hoxa 11 structure, extensive antisense transcription, and function in male and female fertility. Development 1995, 121:1373-1385.
31. Hu Z., Gallo S.M. Identification of interacting transcription factors regulating tissue gene expression in human. BMC Genomics 2010, 11:49.
32. Jensen M.R., Markwick P.R., Meier S., Griesinger C., Zweckstetter M., Grzesiek S., Bernadó P., Blackledge M. Quantitative determination of the conformational properties of partially folded and intrinsically disordered proteins using NMR dipolar couplings. Structure 2009, 17:1169-1185.
33. Jones D.T. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 1999, 292:195-202.
34. Kapusta A., Kronenberg Z., Lynch V.J., Zhuo X., Ramsay L., Bourque G., Yandell M., Feschotte C. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet. 2013, 9:e1003470.
35. Lamb R.S., Irish V.F. Functional divergence within the APETALA3/PISTILLATA floral homeotic gene lineages. Proc. Natl. Acad. Sci. USA 2003, 100:6558-6563.
36. Leman J.K., Mueller R., Karakas M., Woetzel N., Meiler J. Simultaneous prediction of protein secondary structure and transmembrane spans. Proteins 2013, 81:1127-1140.
37. Liu Y., Matthews K.S., Bondos S.E. Multiple intrinsically disordered sequences alter DNA binding by the homeodomain of the Drosophila hox protein ultrabithorax. J. Biol. Chem. 2008, 283:20874-20887.
38. Löhr U., Yussa M., Pick L. Drosophila fushi tarazu. a gene on the border of homeotic function. Curr. Biol. 2001, 11:1403-1412.
39. Lynch V.J., Tanzer A., Wang Y., Leung F.C., Gellersen B., Emera D., Wagner G.P. Adaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals. Proc. Natl. Acad. Sci. USA 2008, 105:14928-14933.
40. Lynch V.J., Brayer K., Gellersen B., Wagner G.P. HoxA-11 and FOXO1A cooperate to regulate decidual prolactin expression: towards inferring the core transcriptional regulators of decidual genes. PLoS ONE 2009, 4:e6845.
41. Lynch V.J., May G., Wagner G.P. Regulatory evolution through divergence of a phosphoswitch in the transcription factor CEBPB. Nature 2011, 480:383-386.
42. Lynch V.J., Nnamani M.C., Kapusta A., Brayer K., Plaza S.L., Mazur E.C., Emera D., Sheikh S.Z., Grützner F., Bauersachs S., et al. Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep. 2015, 10:551-561.
43. MacDonald N.S., Ibsen K.H., Urist M.R. Effect of Tetracycline on Retention of Calcium and Strontium in Rodents. Proc. Soc. Exp. Biol. Med. 1964, 115:1125-1128.
44. McGinnis N., Kuziora M.A., McGinnis W. Human Hox-4.2 and Drosophila deformed encode similar regulatory specificities in Drosophila embryos and larvae. Cell 1990, 63:969-976.
45. Merabet S., Kambris Z., Capovilla M., Bérenger H., Pradel J., Graba Y. The hexapeptide and linker regions of the AbdA Hox protein regulate its activating and repressive functions. Dev. Cell 2003, 4:761-768.
46. Mészáros B., Simon I., Dosztányi Z. Prediction of protein binding regions in disordered proteins. PLoS Comput. Biol. 2009, 5:e1000376.
47. Pearlman S.M., Serber Z., Ferrell J.E. A mechanism for the evolution of phosphorylation sites. Cell 2011, 147:934-946.
48. Prud'homme B., Gompel N., Carroll S.B. Emerging principles of regulatory evolution. Proc. Natl. Acad. Sci. USA 2007, 104(Suppl 1):8605-8612.
49. Ranganayakulu G., Elliott D.A., Harvey R.P., Olson E.N. Divergent roles for NK-2 class homeobox genes in cardiogenesis in flies and mice. Development 1998, 125:3037-3048.
50. Ronshaugen M., McGinnis N., McGinnis W. Hox protein mutation and macroevolution of the insect body plan. Nature 2002, 415:914-917.
51. Roth J.J., Breitenbach M., Wagner G.P. Repressor domain and nuclear localization signal of the murine Hoxa-11 protein are located in the homeodomain: no evidence for role of poly alanine stretches in transcriptional repression. J. Exp. Zoolog. B Mol. Dev. Evol. 2005, 304:468-475.
52. Schwab K., Hartman H.A., Liang H.C., Aronow B.J., Patterson L.T., Potter S.S. Comprehensive microarray analysis of Hoxa11/Hoxd11 mutant kidney development. Dev. Biol. 2006, 293:540-554.
53. Schwartz R.J., Olson E.N. Building the heart piece by piece: modularity of cis-elements regulating Nkx2-5 transcription. Development 1999, 126:4187-4192.
54. Simons K.T., Kooperberg C., Huang E., Baker D. Assembly of protein tertiary structures from fragments with similar local sequences using simulated annealing and Bayesian scoring functions. J. Mol. Biol. 1997, 268:209-225.
55. Sivanantharajah L., Percival-Smith A. Differential pleiotropy and HOX functional organization. Dev. Biol. 2015, 398:1-10.
56. Speleman F., Cauwelier B., Dastugue N., Cools J., Verhasselt B., Poppe B., Van Roy N., Vandesompele J., Graux C., Uyttebroeck A., et al. A new recurrent inversion, inv(7)(p15q34), leads to transcriptional activation of HOXA10 and HOXA11 in a subset of T-cell acute lymphoblastic leukemias. Leukemia 2005, 19:358-366.
57. Thorsness P.E., Koshland D.E. Inactivation of isocitrate dehydrogenase by phosphorylation is mediated by the negative charge of the phosphate. J. Biol. Chem. 1987, 262:10422-10425.
58. Tompa P. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett. 2005, 579:3346-3354.
59. Vo N., Goodman R.H. CREB-binding protein and p300 in transcriptional regulation. J. Biol. Chem. 2001, 276:13505-13508.
60. Vucetic S., Obradovic Z., Vacic V., Radivojac P., Peng K., Iakoucheva L.M., Cortese M.S., Lawson J.D., Brown C.J., Sikes J.G., et al. DisProt: a database of protein disorder. Bioinformatics 2005, 21:137-140.
61. Wagner G.P., Lynch V.J. The gene regulatory logic of transcription factor evolution. Trends Ecol. Evol. 2008, 23:377-385.
62. Wang F., Marshall C.B., Yamamoto K., Li G.Y., Gasmi-Seabrook G.M., Okada H., Mak T.W., Ikura M. Structures of KIX domain of CBP in complex with two FOXO3a transactivation domains reveal promiscuity and plasticity in coactivator recruitment. Proc. Natl. Acad. Sci. USA 2012, 109:6078-6083.
63. Wellik D.M., Capecchi M.R. Hox10 and Hox11 genes are required to globally pattern the mammalian skeleton. Science 2003, 301:363-367.
64. Wray G.A. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 2007, 8:206-216.
65. Yokouchi Y., Sakiyama J., Kuroiwa A. Coordinated expression of Abd-B subfamily genes of the HoxA cluster in the developing digestive tract of chick embryo. Dev. Biol. 1995, 169:76-89.
66. Zor T., Mayr B.M., Dyson H.J., Montminy M.R., Wright P.E. Roles of phosphorylation and helix propensity in the binding of the KIX domain of CREB-binding protein by constitutive (c-Myb) and inducible (CREB) activators. J. Biol. Chem. 2002, 277:42241-42248.