Hox proteins display a common and ancestral ability to diversify their interaction mode with the pbc class cofactors

PLoS Biology

Volumn 10, Issue 6, 2012, Pages

  Hudry, Bruno ^a   Remacle, Sophie ^b   Delfini, Marie Claire ^a   Rezsohazy, René ^b   Graba, Yacine ^a   Merabet, Samir ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; HEXAPEPTIDE; HOX PROTEIN; HOXA1 PROTEIN; HOXB6 PROTEIN; HOXB7 PROTEIN; HOXB8 PROTEIN; MEIS PROTEIN; PROTEIN PBC; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HOXA10; TRANSCRIPTION FACTOR HOXA9; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN COS7; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION PROFILING; GENE LOCUS; GENETIC CONSERVATION; IN VITRO STUDY; INTRACELLULAR SIGNALING; MOUSE; MUTATIONAL ANALYSIS; NEMATOSTELLA VECTENSIS; NONHUMAN; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SEA ANEMONE; ANIMAL; ANIMAL EMBRYO; CELL STRAIN COS1; CERCOPITHECUS; CHEMISTRY; CHICK EMBRYO; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PRENATAL DEVELOPMENT;

ACTINIARIA; NEMATOSTELLA VECTENSIS;

ANIMALS; CERCOPITHECUS AETHIOPS; CHICK EMBRYO; COS CELLS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICE;

EID: 84863702620     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001351     Document Type: Article

References (68)

1. McGinnis W, Krumlauf R, (1992) Homeobox genes and axial patterning. Cell 68: 283 302.
2. Hombria J. C, Lovegrove B, (2003) Beyond homeosis-HOX function in morphogenesis and organogenesis. Differentiation 71: 461 476.
3. Argiropoulos B, Humphries R. K, (2007) Hox genes in hematopoiesis and leukemogenesis. Oncogene 26: 6766 6776.
4. Awgulewitsch A, (2003) Hox in hair growth and development. Naturwissenschaften 90: 193 211.
5. Noyes M. B, Christensen R. G, Wakabayashi A, Stormo G. D, Brodsky M. H, (2008) Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133: 1277 1289.
6. Berger M. F, Badis G, Gehrke A. R, Talukder S, Philippakis A. A, (2008) Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133: 1266 1276.
7. Mukherjee K, Burglin T. R, (2007) Comprehensive analysis of animal TALE homeobox genes: new conserved motifs and cases of accelerated evolution. J Mol Evol 65: 137 153.
8. Mann R. S, Affolter M, (1998) Hox proteins meet more partners. Curr Opin Genet Dev 8: 423 429.
9. Mann R. S, Chan S-K, (1996) Extra specificity from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet 12: 258 262.
10. Mann R. S, Lelli K. M, Joshi R, (2009) Hox specificity unique roles for cofactors and collaborators. Curr Top Dev Biol 88: 63 101.
11. Moens C. B, Selleri L, (2006) Hox cofactors in vertebrate development. Dev Biol 291: 193 206.
12. Chang C. P, Brocchieri L, Shen W. F, Largman C, Cleary M. L, (1996) Pbx modulation of Hox homeodomain amino-terminal arms establishes different DNA-binding specificities across the Hox locus. Mol Cell Biol 16: 1734 1745.
13. Chan S. K, Ryoo H. D, Gould A, Krumlauf R, Mann R. S, (1997) Switching the in vivo specificity of a minimal Hox-responsive element. Development 124: 2007 2014.
14. Ebner A, Cabernard C, Affolter M, Merabet S, (2005) Recognition of distinct target sites by a unique Labial/Extradenticle/Homothorax complex. Development 132: 1591 1600.
15. Joshi R, Passner J. M, Rohs R, Jain R, Sosinsky A, (2007) Functional specificity of a Hox protein mediated by the recognition of minor groove structure. Cell 131: 530 543.
16. Slattery M, Riley T, Liu P, Abe N, Gomez-Alcala P, (2011) Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 147: 1270 1282.
17. Passner J. M, Ryoo H. D, Shen L, Mann R. S, Aggarwal A. K, (1999) Structure of a DNA-bound Ultrabithorax-Extradenticle homeodomain complex. Nature 397: 714 719.
18. Piper D. E, Batchelor A. H, Chang C. P, Cleary M. L, 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.
19. LaRonde-LeBlanc N. A, Wolberger C, (2003) Structure of HoxA9 and Pbx1 bound to DNA: Hox hexapeptide and DNA recognition anterior to posterior. Genes Dev 17: 2060 2072.
20. Knoepfler P. S, Kamps M. P, (1995) The pentapeptide motif of Hox proteins is required for cooperative DNA binding with Pbx1, physically contacts Pbx1, and enhances DNA binding by Pbx1. Mol Cell Biol 15: 5811 5819.
21. Neuteboom S. T, Peltenburg L. T, van Dijk M. A, Murre C, (1995) The hexapeptide LFPWMR in Hoxb-8 is required for cooperative DNA binding with Pbx1 and Pbx2 proteins. Proc Natl Acad Sci U S A 92: 9166 9170.
22. Phelan M. L, Rambaldi I, Featherstone M. S, (1995) Cooperative interactions between HOX and PBX proteins mediated by a conserved peptide motif. Mol Cell Biol 15: 3989 3997.
23. Lu Q, Knoepfler P. S, Scheele J, Wright D. D, Kamps M. P, (1995) Both Pbx1 and E2A-Pbx1 bind the DNA motif ATCAATCAA cooperatively with the products of multiple murine Hox genes, some of which are themselves oncogenes. Mol Cell Biol 15: 3786 3795.
24. Chang C-P, Shen W-F, Rozenfeld S, Lawrence H. J, Largman C, (1995) Pbx proteins display hexapeptide-dependent cooperative DNA binding with a subset of Hox proteins. Genes Dev 9: 663 674.
25. Shanmugam K, Featherstone M. S, Saragovi H. U, (1997) Residues flanking the HOX YPWM motif contribute to cooperative interactions with PBX. J Biol Chem 272: 19081 19087.
26. Li X, Murre C, McGinnis W, (1999) Activity regulation of a Hox protein and a role for the homeodomain in inhibiting transcriptional activation. Embo J 18: 198 211.
27. Chan S. K, Jaffe L, Capovilla M, Botas J, Mann R. S, (1994) The DNA binding specificity of Ultrabithorax is modulated by cooperative interactions with extradenticle, another homeoprotein. Cell 78: 603 615.
28. Merabet S, Saadaoui M, Sambrani N, Hudry B, Pradel J, (2007) A unique Extradenticle recruitment mode in the Drosophila Hox protein Ultrabithorax. Proc Natl Acad Sci U S A 104: 16946 16951.
29. Fischbach N. A, Rozenfeld S, Shen W, Fong S, Chrobak D, (2005) HOXB6 overexpression in murine bone marrow immortalizes a myelomonocytic precursor in vitro and causes hematopoietic stem cell expansion and acute myeloid leukemia in vivo. Blood 105: 1456 1466.
30. Knoepfler P. S, Sykes D. B, Pasillas M, Kamps M. P, (2001) HoxB8 requires its Pbx-interaction motif to block differentiation of primary myeloid progenitors and of most cell line models of myeloid differentiation. Oncogene 20: 5440 5448.
31. Calvo K. R, Knoepfler P. S, Sykes D. B, Pasillas M. P, Kamps M. P, (2001) Meis1a suppresses differentiation by G-CSF and promotes proliferation by SCF: potential mechanisms of cooperativity with Hoxa9 in myeloid leukemia. Proc Natl Acad Sci U S A 98: 13120 13125.
32. Medina-Martinez O, Ramirez-Solis R, (2003) In vivo mutagenesis of the Hoxb8 hexapeptide domain leads to dominant homeotic transformations that mimic the loss-of-function mutations in genes of the Hoxb cluster. Dev Biol 264: 77 90.
33. Chan S. K, Popperl H, Krumlauf R, Mann R. S, (1996) An extradenticle-induced conformational change in a HOX protein overcomes an inhibitory function of the conserved hexapeptide motif. EMBO J 15: 2476 2487.
34. Galant R, Walsh C. M, Carroll S. B, (2002) Hox repression of a target gene: extradenticle-independent, additive action through multiple monomer binding sites. Development 129: 3115 3126.
35. Merabet S, Kambris Z, Capovilla M, Berenger H, Pradel J, (2003) The hexapeptide and linker regions of the AbdA hox protein regulate its activating and repressive functions. Dev Cell 4: 761 768.
36. Kerppola T. K, (2008) Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annu Rev Biophys 37: 465 487.
37. Hudry B, Viala S, Graba Y, Merabet S, (2011) Visualization of protein interactions in living Drosophila embryos by the bimolecular fluorescence complementation assay. BMC Biol 9: 5.
38. Bischof J, Maeda R. K, Hediger M, Karch F, Basler K, (2007) An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci U S A 104: 3312 3317.
39. de Navas L, Foronda D, Suzanne M, Sanchez-Herrero E, (2006) A simple and efficient method to identify replacements of P-lacZ by P-Gal4 lines allows obtaining Gal4 insertions in the bithorax complex of Drosophila. Mech Dev 123: 860 867.
40. Jacobs Y, Schnabel C. A, Cleary M. L, (1999) Trimeric association of Hox and TALE homeodomain proteins mediates Hoxb2 hindbrain enhancer activity. Mol Cell Biol 19: 5134 5142.
41. Remacle S, Abbas L, De Backer O, Pacico N, Gavalas A, (2004) Loss of function but no gain of function caused by amino acid substitutions in the hexapeptide of Hoxa1 in vivo. Mol Cell Biol 24: 8567 8575.
42. Gaunt S. J, (2000) Evolutionary shifts of vertebrate structures and Hox expression up and down the axial series of segments: a consideration of possible mechanisms. Int J Dev Biol 44: 109 117.
43. Coy S, Caamano J. H, Carvajal J, Cleary M. L, Borycki A. G, (2011) A novel Gli3 enhancer controls the Gli3 spatiotemporal expression pattern through a TALE homeodomain protein binding site. Mol Cell Biol 31: 1432 1443.
44. Noro B, Lelli K, Sun L, Mann R. S, (2011) Competition for cofactor-dependent DNA binding underlies Hox phenotypic suppression. Genes Dev 25: 2327 2332.
45. Gebelein B, Culi J, Ryoo H. D, Zhang W, Mann R. S, (2002) Specificity of distalless repression and limb primordia development by abdominal hox proteins. Dev Cell 3: 487 498.
46. Kannan R, Berger C, Myneni S, Technau G. M, Shashidhara L. S, (2010) Abdominal-A mediated repression of Cyclin E expression during cell-fate specification in the Drosophila central nervous system. Mech Dev 127: 137 145.
47. Tumpel S, Cambronero F, Ferretti E, Blasi F, Wiedemann L. M, (2007) Expression of Hoxa2 in rhombomere 4 is regulated by a conserved cross-regulatory mechanism dependent upon Hoxb1. Dev Biol 302: 646 660.
48. Uhl J. D, Cook T. A, Gebelein B, (2010) Comparing anterior and posterior Hox complex formation reveals guidelines for predicting cis-regulatory elements. Dev Biol 343: 154 166.
49. Noro B, Culi J, McKay D. J, Zhang W, Mann R. S, (2006) Distinct functions of homeodomain-containing and homeodomain-less isoforms encoded by homothorax. Genes Dev 20: 1636 1650.
50. Gehring W. J, Affolter M, Bürglin T, (1994) Homeodomain proteins. Annu Rev Biochem 63: 487 526.
51. Ryan J. F, Mazza M. E, Pang K, Matus D. Q, Baxevanis A. D, (2007) Pre-bilaterian origins of the Hox cluster and the Hox code: evidence from the sea anemone, Nematostella vectensis. PLoS ONE 2: e153 doi:10.1371/journal.pone.0000153.
52. Kamm K, Schierwater B, Jakob W, Dellaporta S. L, Miller D. J, (2006) Axial patterning and diversification in the cnidaria predate the Hox system. Curr Biol 16: 920 926.
53. Chiori R, Jager M, Denker E, Wincker P, Da Silva C, (2009) Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (Cnidaria). PLoS ONE 4: e4231 doi:10.1371/journal.pone.0004231.
54. Thomas-Chollier M, Ledent V, Leyns L, Vervoort M, (2010) A non-tree-based comprehensive study of metazoan Hox and ParaHox genes prompts new insights into their origin and evolution. BMC Evol Biol 10: 73.
55. Balavoine G, de Rosa R, Adoutte A, (2002) Hox clusters and bilaterian phylogeny. Mol Phylogenet Evol 24: 366 373.
56. Merabet S, Litim-Mecheri I, Karlsson D, Dixit R, Saadaoui M, (2011) Insights into hox protein function from a large scale combinatorial analysis of protein domains. PLoS Genet 7: e1002302 doi:10.1371/journal.pgen.1002302.
57. Joshi R, Sun L, Mann R, (2010) Dissecting the functional specificities of two Hox proteins. Genes Dev 24: 1533 1545.
58. Li-Kroeger D, Witt L. M, Grimes H. L, Cook T. A, Gebelein B, (2008) Hox and senseless antagonism functions as a molecular switch to regulate EGF secretion in the Drosophila PNS. Dev Cell 15: 298 308.
59. Shen W. F, Montgomery J. C, Rozenfeld S, Moskow J. J, Lawrence H. J, (1997) AbdB-like Hox proteins stabilize DNA binding by the Meis1 homeodomain proteins. Mol Cell Biol 17: 6448 6458.
60. Williams T. M, Williams M. E, Innis J. W, (2005) Range of HOX/TALE superclass associations and protein domain requirements for HOXA13:MEIS interaction. Dev Biol 277: 457 471.
61. Meijsing S. H, Pufall M. A, So A. Y, Bates D. L, Chen L, (2009) DNA binding site sequence directs glucocorticoid receptor structure and activity. Science 324: 407 410.
62. Lelli K. M, Noro B, Mann R. S, (2011) Variable motif utilization in homeotic selector (Hox)-cofactor complex formation controls specificity. Proc Natl Acad Sci U S A 108: 21122 21127.
63. Li X, McGinnis W, (1999) Activity regulation of Hox proteins, a mechanism for altering functional specificity in development and evolution. Proc Natl Acad Sci U S A 96: 6802 6807.
64. Biggin M. D, McGinnis W, (1997) Regulation of segmentation and segmental identity by Drosophila homeoproteins: the role of DNA binding in functional activity and specificity. Development 124: 4425 4433.
65. Saadaoui M, Merabet S, Litim-Mecheri I, Arbeille E, Sambrani N, (2011) Selection of distinct Hox-Extradenticle interaction modes fine-tunes Hox protein activity. Proc Natl Acad Sci U S A.
66. Ryoo H. D, Mann R. S, (1999) The control of trunk Hox specificity and activity by Extradenticle. Genes Dev 13: 1704 1716.
67. Capovilla M, Kambris Z, Botas J, (2001) Direct regulation of the muscle-identity gene apterous by a Hox protein in the somatic mesoderm. Development 128: 1221 1230.
68. McCormick A, Core N, Kerridge S, Scott M. P, (1995) Homeotic response elements are tightly linked to tissue-specific elements in a transcriptional enhancer of the teashirt gene. Development 121: 2799 2812.