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Homeodomain Subtypes and Functional Diversity

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A Handbook of Transcription Factors

Part of the book series: Subcellular Biochemistry ((SCBI,volume 52))

Abstract

The homeodomain is a protein domain of about 60 amino acids that is encoded by homeobox genes. The homeodomain is a DNA binding domain, and hence homeodomain proteins are essentially transcription factors (TFs). They have been shown to play major roles in many developmental processes of animals, as well as fungi and plants. A primary function of homeodomain proteins is to regulate the expression of other genes in development and differentiation. Thousands of homeobox genes have been identified, and they can be grouped into many different classes. Often other conserved protein domains are found linked to a homeodomain. Several particular types of homeobox genes are organized into chromosomal clusters. The best-known cluster, the HOX cluster, is found in all bilaterian animals. Tetrapods contain four HOX clusters that arose through duplication in early vertebrate evolution. The genes in these clusters are called Hox genes. Lower chordates, insects and nematodes tend to have only one HOX cluster. Of particular interest is that many of the HOX cluster genes function in the process of pattern formation along the anterior-posterior body axis. Many other types of homeodomain proteins play roles in the determination of cell fates and cell differentiation. Homeobox genes thus perform key roles for all aspects of the development of an organism.

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References

  1. Carrasco AE, McGinnis W, Gehring WJ, De Robertis EM (1984) Cloning of an X. laevis gene expressed during early embryogenesis coding for a peptide region homologous to Drosophila homeotic genes. Cell 37:409–414

    Article  PubMed  CAS  Google Scholar 

  2. Laughon A, Scott MP (1984) Sequence of a Drosophila segmentation gene: protein structure homology with DNA-binding proteins. Nature 310:25–31

    Article  PubMed  CAS  Google Scholar 

  3. McGinnis W, Garber RL, Wirz J, Kuroiwa A, Gehring WJ (1984a) A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell 37:403–408

    Article  PubMed  CAS  Google Scholar 

  4. McGinnis W, Hart CP, Gehring WJ, Ruddle FH (1984b) Molecular cloning and chromosome mapping of a mouse DNA sequence homologous to homeotic genes of Drosophila. Cell 38:675–680

    Article  PubMed  CAS  Google Scholar 

  5. McGinnis W, Levine MS, Hafen E, Kuroiwa A, Gehring WJ (1984c) A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 308:428–433

    Article  PubMed  CAS  Google Scholar 

  6. Scott MP, Weiner AJ (1984) Structural relationships among genes that control development: Sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci in Drosophila. Proc Natl Acad Sci USA 81:4115–4119

    Article  PubMed  CAS  Google Scholar 

  7. Shepherd JCW, McGinnis W, Carrasco AE, De Robertis EM, Gehring WJ (1984) Fly and frog homoeo domains show homologies with yeast mating type regulatory proteins. Nature 310:70–71

    Article  PubMed  CAS  Google Scholar 

  8. Qian YQ, Billeter M, Otting G, Müller M, Gehring WJ, Wüthrich K (1989) The structure of the Antennapedia homeodomain determined by NMR spectroscopy in solution: comparison with prokaryotic repressors. Cell 59:573–580

    Article  PubMed  CAS  Google Scholar 

  9. Billeter M, Qian YQ, Otting G, Muller M, Gehring W, Wüthrich K (1993) Determination of the nuclear magnetic resonance solution structure of an Antennapedia homeodomain-DNA complex. J Mol Biol 234:1084–1093

    Article  PubMed  CAS  Google Scholar 

  10. Qian YQ, Furukubo-Tokunaga K, Resendez-Perez D, Müller M, Gehring WJ, 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

    Article  PubMed  CAS  Google Scholar 

  11. Kissinger CR, Liu B, Martin-Blanco E, Kornberg TB, Pabo CO (1990) Crystal structure of an engrailed homeodomain-DNA complex at 2.8 Å resolution: a framework for understanding homeodomain–DNA interactions. Cell 63:579–590

    Article  PubMed  CAS  Google Scholar 

  12. 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

    Article  PubMed  CAS  Google Scholar 

  13. Assa-Munt N, Mortishire-Smith RJ, Aurora R, Herr W, Wright PE (1993) The solution structure of the Oct-1 POU-specific domain reveals a striking similarity to the bacteriophage λ repressor DNA-binding domain. Cell 73:193–205

    Article  PubMed  CAS  Google Scholar 

  14. Dekker N, Cox M, Boelens R, Verrijzer CP, van der Vliet PC, Kaptein R (1993) Solution structure of the POU-specific DNA-binding domain of Oct-1. Nature 362:852–855

    Article  PubMed  CAS  Google Scholar 

  15. Ceska TA, Lamers M, Monaci P, Nicosia A, Cortese R, Suck D (1993) The X-ray structure of an atypical homeodomain present in the rat liver transcription factor LFB1/HNF1 and implications for DNA binding. EMBO J 12:1805–1810

    PubMed  CAS  Google Scholar 

  16. Chi YI, Frantz JD, Oh BC, Hansen L, Dhe-Paganon S, Shoelson SE (2002) Diabetes mutations delineate an atypical POU domain in HNF-1alpha. Mol Cell 10:1129–1137

    Article  PubMed  CAS  Google Scholar 

  17. Wolberger C, Vershon AK, Liu B, Johnson AD, Pabo CO (1991) Crystal structure of MATα2 Homeodomain-operator complex suggests a general model for homeodomain-DNA interactions. Cell 67:517–528

    Article  PubMed  CAS  Google Scholar 

  18. Hanes SD, Brent R (1989) DNA specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9. Cell 57:1275–1283

    Article  PubMed  CAS  Google Scholar 

  19. Bürglin TR (1994) A comprehensive classification of homeobox genes. In Guidebook to the Homeobox Genes, Duboule D, ed. (Oxford, Oxford University Press), pp. 25–71

    Google Scholar 

  20. Bürglin TR (2005) Homeodomain proteins. In Encyclopedia of Molecular Cell Biology and Molecular Medicine, Meyers RA, ed. (Weinheim, Wiley-VCH Verlag GmbH & Co.), pp. 179–222

    Google Scholar 

  21. Gehring WJ, Affolter M, Bürglin TR (1994) Homeodomain proteins. Annu Rev Biochem 63:487–526

    Article  PubMed  CAS  Google Scholar 

  22. Mukherjee K, Bürglin TR (2007) Comprehensive analysis of animal TALE homeobox genes: new conserved motifs and cases of accelerated evolution. J Mol Evol 65:137–153

    Article  PubMed  CAS  Google Scholar 

  23. Holland PW, Booth HA, Bruford EA (2007) Classification and nomenclature of all human homeobox genes. BMC Biol 5:47

    Article  PubMed  CAS  Google Scholar 

  24. Duboule D, Morata G (1994) Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet 10:358–364

    Article  PubMed  CAS  Google Scholar 

  25. Garcia-Fernàndez J, Holland PWH (1994) Archetypal organization of the amphioxus Hox gene cluster. Nature 370:563–566

    Article  PubMed  Google Scholar 

  26. Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, et al (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282:1711–1714

    Article  PubMed  CAS  Google Scholar 

  27. Crow KD, Stadler PF, Lynch VJ, Amemiya C, Wagner GP (2006) The “fish-specific” Hox cluster duplication is coincident with the origin of teleosts. Mol Biol Evol 23:121–136

    Article  PubMed  CAS  Google Scholar 

  28. Prohaska SJ, Stadler PF (2004) The duplication of the Hox gene clusters in teleost fishes. Theory Biosci 123:89–110

    Article  PubMed  CAS  Google Scholar 

  29. Pollard SL, Holland PWH (2000) Evidence for 14 homeobox gene clusters in human genome ancestry. Curr Biol 10:1059–1062

    Article  PubMed  CAS  Google Scholar 

  30. Aboobaker A, Blaxter M (2003a) Hox gene evolution in nematodes: novelty conserved. Curr Opin Genet Dev 13:593–598

    Article  PubMed  CAS  Google Scholar 

  31. Aboobaker AA, Blaxter ML (2003b) Hox gene loss during dynamic evolution of the nematode cluster. Curr Biol 13:37–40

    Article  PubMed  CAS  Google Scholar 

  32. Kmita M, Duboule D (2003) Organizing axes in time and space; 25 years of colinear tinkering. Science 301:331–333

    Article  PubMed  CAS  Google Scholar 

  33. Damen WGM, Tautz D (1998) A Hox class 3 orthologue from the spider Cupiennius salei is expressed in a Hox-gene-like fashion. Dev Genes Evol 208:586–590

    Article  PubMed  CAS  Google Scholar 

  34. Stauber M, Jäckle H, Schmidt-Ott U (1999) The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc Natl Acad Sci USA 96:3786–3789

    Article  PubMed  CAS  Google Scholar 

  35. Stauber M, Prell A, Schmidt-Ott U (2002) A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-Cyclorrhaphan flies. Proc Natl Acad Sci USA 99:274–279

    Article  PubMed  CAS  Google Scholar 

  36. Brown SJ, Hilgenfeld RB, Denell RE (1994) The beetle Tribolium castaneum has a fushi tarazu homolog expressed in stripes during segmentation. Proc Natl Acad Sci USA 91:12922–12926

    Article  PubMed  CAS  Google Scholar 

  37. Damen WG (2002) fushi tarazu: a Hox gene changes its role. Bioessays 24:992–995

    Article  PubMed  CAS  Google Scholar 

  38. Dawes R, Dawson I, Falciani F, Tear G, Akam M (1994) Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression. Development 120:1561–1572

    PubMed  CAS  Google Scholar 

  39. Zakany J, Duboule D (2007) The role of Hox genes during vertebrate limb development. Curr Opin Genet Dev 17:359–366

    Article  PubMed  CAS  Google Scholar 

  40. Brooke NM, Garcia-Fernàndez J, Holland PWH (1998) The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 392:920–922

    Article  PubMed  CAS  Google Scholar 

  41. Luke GN, Castro LF, McLay K, Bird C, Coulson A, Holland PW (2003) Dispersal of NK homeobox gene clusters in amphioxus and humans. Proc Natl Acad Sci U S A 100:5292–5295

    Article  PubMed  CAS  Google Scholar 

  42. Mulley JF, Chiu CH, Holland PW (2006) Breakup of a homeobox cluster after genome duplication in teleosts. Proc Natl Acad Sci USA 103:10369–10372

    Article  PubMed  CAS  Google Scholar 

  43. Garcia-Fernàndez J (2005) The genesis and evolution of homeobox gene clusters. Nat Rev Genet 6:881–892

    Article  PubMed  Google Scholar 

  44. Cande JD, Chopra VS, Levine M (2009) Evolving enhancer-promoter interactions within the tinman complex of the flour beetle, Tribolium castaneum. Development 136:3153–3160

    Article  PubMed  CAS  Google Scholar 

  45. Jagla K, Bellard M, Frasch M (2001) A cluster of Drosophila homeobox genes involved in mesoderm differentiation programs. Bioessays 23:125–133

    Article  PubMed  CAS  Google Scholar 

  46. Smith ST, Jaynes JB (1996) A conserved region of engrailed, shared among all en-, gsc-, Nk1-, Nk2- and msh-class homeoproteins, mediates active transcriptional repression in vivo. Development 122:3141–3150

    PubMed  CAS  Google Scholar 

  47. Xu W, Rould MA, Jun S, Desplan C, Pabo CO (1995) Crystal structure of a paired domain-DNA complex at 2.5 Å resolution reveals structural basis for Pax developmental mutations. Cell 80:639–650

    Article  PubMed  CAS  Google Scholar 

  48. Gruss P, Walther C (1992) Pax in development. Cell 69:719–722

    Article  PubMed  CAS  Google Scholar 

  49. Walther C, Guenet J-L, Simon D, Deutsch U, Jostes B, Goulding MD, Plachov D, Balling R, Gruss P (1991) Pax: a murine multigene family of paired box-containing genes. Genomics 11:424–434

    Article  PubMed  CAS  Google Scholar 

  50. Breitling R, Gerber JK (2000) Origin of the paired domain. Dev Genes Evol 210:644–650

    Article  PubMed  CAS  Google Scholar 

  51. Callaerts P, Halder G, Gehring WJ (1997) Pax-6 in development and evolution. Annu Rev Neurosci 20:483–532

    Article  PubMed  CAS  Google Scholar 

  52. Halder G, Callaerts P, Gehring WJ (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267:1788–1792

    Article  PubMed  CAS  Google Scholar 

  53. Quiring R, Walldorf U, Kloter U, Gehring WJ (1994) Homology of the eyeless gene of Drosophila to the Small eye gene in mice and Aniridia in humans. Science 265:785–789

    Article  PubMed  CAS  Google Scholar 

  54. Chow RL, Snow B, Novak J, Looser J, Freund C, Vidgen D, Ploder L, McInnes RR (2001) Vsx1, a rapidly evolving paired-like homeobox gene expressed in cone bipolar cells. Mech Dev 109:315–322

    Article  PubMed  CAS  Google Scholar 

  55. Liu ISC, Chen J, Ploder L, Vidgen D, van der Kooy D, Kalnins VI, McInnes RR (1994) Developmental expression of a novel murine homeobox gene (Chx10): evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron 13:377–393

    Article  PubMed  CAS  Google Scholar 

  56. Galliot B, de Vargas C, Miller D (1999) Evolution of homeobox genes: Q50 Paired-like genes founded the Paired class. Dev Genes Evol 209:186–197

    Article  PubMed  CAS  Google Scholar 

  57. Sun S, Ting CT, Wu CI (2004) The normal function of a speciation gene, Odysseus, and its hybrid sterility effect. Science 305:81–83

    Article  PubMed  CAS  Google Scholar 

  58. MacLean JA 2nd, Wilkinson MF (2010) The Rhox genes. Reproduction 140:195–213

    Article  PubMed  CAS  Google Scholar 

  59. Maclean JA 2nd, Chen MA, Wayne CM, Bruce SR, Rao M, Meistrich ML, Macleod C, Wilkinson MF (2005) Rhox: a new homeobox gene cluster. Cell 120:369–382

    Article  PubMed  CAS  Google Scholar 

  60. Herr W, Sturm RA, Clerc RG, Corcoran LM, Baltimore D, Sharp PA, Ingraham HA, Rosenfeld MG, Finney M, Ruvkun G, et al. (1988) The POU domain: a large conserved region in the mammalian pit-1, oct-1, oct-2, and Caenorhabditis elegans unc-86 gene products. Genes Dev 2:1513–1516

    Article  PubMed  CAS  Google Scholar 

  61. Jacobson EM, Li P, Leon-del-Rio A, Rosenfeld MG, Aggarwal AK (1997) Structure of Pit-1 POU domain bound to DNA as a dimer: unexpected arrangement and flexibility. Genes Dev 11:198–212

    Article  PubMed  CAS  Google Scholar 

  62. Klemm JD, Rould MA, Aurora R, Herr W, Pabo CO (1994) Crystal structure of the Oct-1 POU domain bound to an Octamer site: DNA recognition with tethered DNA-binding modules. Cell 77:21–32

    Article  PubMed  CAS  Google Scholar 

  63. Frain M, Swart G, Monaci P, Nicosia A, Stämpfli S, Frank R, Cortese R (1989) The liver-specific transcription factor LF-B1 contains a highly diverged homeobox DNA binding domain. Cell 59:145–157

    Article  PubMed  CAS  Google Scholar 

  64. Blochlinger K, Bodmer R, Jack J, Jan LY, Jan YN (1988) Primary structure and expression of a product from cut, a locus involved in specifying sensory organ identity in Drosophila. Nature 333:629–635

    Article  PubMed  CAS  Google Scholar 

  65. Iyaguchi D, Yao M, Watanabe N, Nishihira J, Tanaka I (2007) DNA recognition mechanism of the ONECUT homeodomain of transcription factor HNF-6. Structure 15:75–83

    Article  PubMed  CAS  Google Scholar 

  66. Yamaguchi H, Tateno M, Yamasaki K (2006) Solution structure and DNA-binding mode of the matrix attachment region-binding domain of the transcription factor SATB1 that regulates the T-cell maturation. J Biol Chem 281:5319–5327

    Article  PubMed  CAS  Google Scholar 

  67. Yamasaki K, Akiba T, Yamasaki T, Harata K (2007) Structural basis for recognition of the matrix attachment region of DNA by transcription factor SATB1. Nucleic Acids Res 35:5073–5084

    Article  PubMed  CAS  Google Scholar 

  68. Bürglin TR, Cassata G (2002) Loss and gain of domains during evolution of cut superclass homeobox genes. Int J Dev Biol 46:115–123

    PubMed  Google Scholar 

  69. Takatori N, Saiga H (2008) Evolution of CUT class homeobox genes: insights from the genome of the amphioxus, Branchiostoma floridae. Int J Dev Biol 52:969–977

    Article  PubMed  CAS  Google Scholar 

  70. Neufeld EJ, Skalnik DG, Lievens PM-J, Orkin SH (1992) Human CCAAT displacement protein is homologous to the Drosophila homeoprotein cut. Nature Genet 1:50–55

    Article  PubMed  CAS  Google Scholar 

  71. Gillingham AK, Pfeifer AC, Munro S (2002) CASP, the alternatively spliced product of the gene encoding the CCAAT-displacement protein transcription factor, is a Golgi membrane protein related to giantin. Mol Biol Cell 13:3761–3774

    Article  PubMed  CAS  Google Scholar 

  72. Dickinson LA, Dickinson CD, Kohwi-Shigematsu T (1997) An atypical homeodomain in SATB1 promotes specific recognition of the key structural element in a matrix attachment region. J Biol Chem 272:11463–11470

    Article  PubMed  CAS  Google Scholar 

  73. Morinaga T, Yasuda H, Hashimoto T, Higashio K, Tamaoki T (1991) A human alpha-fetoprotein enhancer-binding protein, ATBF1, contains four homeodomains and seventeen zinc fingers. Mol Cell Biol 11:6041–6049

    PubMed  CAS  Google Scholar 

  74. Freyd G, Kim S, Horvitz RH (1990) Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature 344:876–879

    Article  PubMed  CAS  Google Scholar 

  75. Srivastava M, Larroux C, Lu DR, Mohanty K, Chapman J, Degnan BM, Rokhsar DS (2010) Early evolution of the LIM homeobox gene family. BMC Biol 8:4

    Article  PubMed  CAS  Google Scholar 

  76. Schmeichel KL, Beckerle MC (1994) The LIM domain is a modular protein-binding interface. Cell 79:211–219

    Article  PubMed  CAS  Google Scholar 

  77. Agulnick AD, Taira M, Breen JJ, Tanaka T, Dawid IB, Westphal H (1996) Interactions of the LIM-domain-binding factor Ldb1 with LIM homeodomain proteins. Nature 384:270–272

    Article  PubMed  CAS  Google Scholar 

  78. Oliver G, Wehr R, Jenkins NA, Copeland NG, Cheyette BNR, Hartenstein V, Zipursky SL, Gruss P (1995) Homeobox genes and connective tissue patterning. Development 121:693–705

    PubMed  CAS  Google Scholar 

  79. Dozier C, Kagoshima H, Niklaus G, Cassata G, Bürglin TR (2001) The Caenorhabditis elegans Six/sine oculis class homeobox gene ceh-32 is required for head morphogenesis. Dev Biol 236:289–303

    Article  PubMed  CAS  Google Scholar 

  80. Chu-Lagraff Q, Wright DM, McNeil LK, Doe CQ (1991) The prospero gene encodes a divergent homeodomain protein that controls neuronal identity in Drosophila. Development Suppl. 2:79–85

    Google Scholar 

  81. Vaessin H, Grell E, Wolff E, Bier E, Jan LY, Jan YN (1991) prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell 67:941–953

    Article  PubMed  CAS  Google Scholar 

  82. Bürglin TR (1994) A Caenorhabditis elegans prospero homologue defines a novel domain. Trends Biochem Sci 19:70–71

    Article  PubMed  Google Scholar 

  83. Oliver G, Sosa-Pineda B, Geisendorf S, Spana EP, Doe CQ, Gruss P (1993) Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech Dev 44:3–16

    Article  PubMed  CAS  Google Scholar 

  84. Ryter JM, Doe CQ, Matthews BW (2002) Structure of the DNA binding region of prospero reveals a novel homeo-prospero domain. Structure (Camb) 10:1541–1549

    Article  CAS  Google Scholar 

  85. Bertolino E, Wildt S, Richards G, Clerc RG (1996) Expression of a novel murine homeobox gene in the developing cerebellar external granular layer during its proliferation. Dev Dyn 205:410–420

    Article  PubMed  CAS  Google Scholar 

  86. Bürglin TR (1997) Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucl Acids Res 25:4173–4180

    Article  PubMed  Google Scholar 

  87. Derelle R, Lopez P, Le Guyader H, Manuel M (2007) Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes. Evol Dev 9:212–219

    Article  PubMed  CAS  Google Scholar 

  88. Bürglin TR, Ruvkun G (1992) New motif in PBX genes. Nature Genet 1:319–320

    Article  PubMed  Google Scholar 

  89. Rauskolb C, Peifer M, Wieschaus E (1993) extradenticle, a regulator of homeotic gene activity, is a homolog of the homeobox-containing human proto-oncogene pbx1. Cell 74:1101–1112

    Article  PubMed  CAS  Google Scholar 

  90. Mann RS, Chan S-K (1996) Extra specificity from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet 12:258–262

    Article  PubMed  CAS  Google Scholar 

  91. Pai C-Y, Kuo T-S, Jaw TJ, Kurant E, Chen C-T, Bessarab DA, Salzberg A, Sun YH (1998) The Homothorax homeoprotein activates the nuclear localization of another homeoprotein, Extradenticle, and suppresses eye development in Drosophila. Genes Dev 12:435–446

    Article  PubMed  CAS  Google Scholar 

  92. Rieckhof GE, Casares F, Ryoo HD, Abu-Shaar M, Mann RS (1997) Nuclear translocation of Extradenticle requires homothorax, which encodes an Extradenticle-related Homeodomain protein. Cell 91:171–183

    Article  PubMed  CAS  Google Scholar 

  93. Jacobs Y, Schnabel CA, Cleary ML (1999) Trimeric association of Hox and TALE homeodomain proteins mediates Hoxb2 hindbrain enhancer activity. Mol Cell Biol 19:5134–5142

    PubMed  CAS  Google Scholar 

  94. Mann RS, Affolter M (1998) Hox proteins meet more partners. Curr Opin Genet Dev 8:423–429

    Article  PubMed  CAS  Google Scholar 

  95. Shen WF, Rozenfeld S, Kwong A, Kom ves LG, Lawrence HJ, Largman C (1999) HOXA9 forms triple complexes with PBX2 and MEIS1 in myeloid cells. Mol Cell Biol 19:3051–3061

    PubMed  CAS  Google Scholar 

  96. Gómez-Skarmeta J-L, Diez del Corral R, de la Calle-Mustienes E, Ferrés-Marcó D, Modolell J (1996) araucan and caupolican, two members of the novel Iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell 85:95–105

    Article  PubMed  Google Scholar 

  97. Kerner P, Ikmi A, Coen D, Vervoort M (2009) Evolutionary history of the iroquois/Irx genes in metazoans. BMC Evol Biol 9:74

    Article  PubMed  CAS  Google Scholar 

  98. Bertolino E, Reimund B, Wildt-Perinic D, Clerc RG (1995) A novel homeobox protein which recognizes a TGT core and functionally interferes with a retinoid-responsive motif. J Biol Chem 270:31178–31188

    Article  PubMed  CAS  Google Scholar 

  99. Kagoshima H, Cassata G, Bürglin TR (1999) A Caenorhabditis elegans homeobox gene expressed in the male tail, a link between pattern formation and sexual dimophism? Dev Genes Evol 209:59–62

    Article  PubMed  CAS  Google Scholar 

  100. Mizutani Y, Kihara A, Igarashi Y (2005) Mammalian Lass6 and its related family members regulate synthesis of specific ceramides. Biochem J 390:263–271

    Article  PubMed  CAS  Google Scholar 

  101. Pewzner-Jung Y, Ben-Dor S, Futerman AH (2006) When do Lasses (longevity assurance genes) become CerS (ceramide synthases)?: Insights into the regulation of ceramide synthesis. J Biol Chem 281:25001–25005

    Article  PubMed  CAS  Google Scholar 

  102. Astell CR, Ahlstrom-Jonasson L, Smith M, Tatchell K, Nasmyth KA, Hall BD (1981) The sequence of the DNAs coding for the mating-type loci of Saccharomyces cerevisiae. Cell 27:15–23

    Article  PubMed  CAS  Google Scholar 

  103. Kahmann R, Bölker M (1996) Self/nonself recognition in fungi: old mysteries and simple solutions. Cell 85:145–148

    Article  PubMed  CAS  Google Scholar 

  104. Bürglin TR (2003) The homeobox genes of Encephalitozoon cuniculi (Microsporidia) reveal a putative mating-type locus. Dev Genes Evol 213:50–52

    PubMed  Google Scholar 

  105. Mukherjee K, Brocchieri L, Bürglin TR (2009) A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol 26:2775–2794

    Article  PubMed  CAS  Google Scholar 

  106. Bürglin TR (1998) The PBC domain contains a MEINOX domain: Coevolution of Hox and TALE homeobox genes? Dev Genes Evol 208:113–116

    Article  PubMed  Google Scholar 

  107. Bellaoui M, Pidkowich MS, Samach A, Kushalappa K, Kohalmi SE, Modrusan Z, Crosby WL, Haughn GW (2001) The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals. Plant Cell 13:2455–2470

    Article  PubMed  CAS  Google Scholar 

  108. Chen H, Rosin FM, Prat S, Hannapel DJ (2003) Interacting transcription factors from the three-amino acid loop extension superclass regulate tuber formation. Plant Physiol 132:1391–1404

    Article  PubMed  CAS  Google Scholar 

  109. Muller J, Wang Y, Franzen R, Santi L, Salamini F, 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

    Article  PubMed  CAS  Google Scholar 

  110. Smith HMS, Boschke I, Hake S (2002) Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity. Proc Natl Acad Sci USA 99:9579–9584

    Article  PubMed  CAS  Google Scholar 

  111. Ryan JF, Burton PM, Mazza ME, Kwong GK, Mullikin JC, Finnerty JR (2006) The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes. Evidence from the starlet sea anemone, Nematostella vectensis. Genome Biol 7:R64

    Article  PubMed  CAS  Google Scholar 

  112. McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283–302

    Article  PubMed  CAS  Google Scholar 

  113. Reece-Hoyes JS, Deplancke B, Shingles J, Grove CA, Hope IA, Walhout AJ (2005) A compendium of Caenorhabditis elegans regulatory transcription factors: a resource for mapping transcription regulatory networks. Genome Biol 6:R110

    Article  PubMed  CAS  Google Scholar 

  114. Takatori N, Butts T, Candiani S, Pestarino M, Ferrier DE, Saiga H, Holland PW (2008) Comprehensive Survey and classification of homeobox genes in the genome of amphioxus, Branchiostoma floridae. Dev Genes Evol 218:579–590

    Article  PubMed  CAS  Google Scholar 

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Bürglin, T.R. (2011). Homeodomain Subtypes and Functional Diversity. In: Hughes, T. (eds) A Handbook of Transcription Factors. Subcellular Biochemistry, vol 52. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9069-0_5

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