Advertisement

Homeotic Gene Regulation: A Paradigm for Epigenetic Mechanisms Underlying Organismal Development

  • Navneet K. Matharu
  • Vasanthi Dasari
  • Rakesh K. MishraEmail author
Chapter
Part of the Subcellular Biochemistry book series (SCBI, volume 61)

Abstract

The organization of eukaryotic genome into chromatin within the nucleus eventually dictates the cell type specific expression pattern of genes. This higher order of chromatin organization is established during development and dynamically maintained throughout the life span. Developmental mechanisms are conserved in bilaterians and hence they have body plan in common, which is achieved by regulatory networks controlling cell type specific gene expression. Homeotic genes are conserved in metazoans and are crucial for animal development as they specify cell type identity along the anterior-posterior body axis. Hox genes are the best studied in the context of epigenetic regulation that has led to significant understanding of the organismal development. Epigenome specific regulation is brought about by conserved chromatin modulating factors like PcG/trxG proteins during development and differentiation. Here we discuss the conserved epigenetic mechanisms relevant to homeotic gene regulation in metazoans.

Keywords

Retinoic Acid Homeotic Gene Homeotic Transformation PRC2 Complex Polycomb Response Element 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, Rappsilber J, Issaeva I, Canaani E, Salcini AE, Helin K (2007) UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449:731–734PubMedCrossRefGoogle Scholar
  2. Bantignies F, Grimaud C, Lavrov S, Gabut M, Cavalli G (2003) Inheritance of Polycomb-dependent chromosomal interactions in Drosophila. Genes Dev 17:2406–2420PubMedCrossRefGoogle Scholar
  3. Bantignies F, Roure V, Comet I, Leblanc B, Schuettengruber B, Bonnet J, Tixier V, Mas A, Cavalli G (2011) Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 144:214–226PubMedCrossRefGoogle Scholar
  4. Beisel C, Paro R (2011) Silencing chromatin: comparing modes and mechanisms. Nat Rev Genet 12:123–135PubMedCrossRefGoogle Scholar
  5. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–1093PubMedCrossRefGoogle Scholar
  6. Bender W, Akam M, Karch F, Beachy PA, Peifer M, Spierer P, Lewis EB, Hogness DS (1983) Molecular genetics of the bithorax complex in Drosophila melanogaster. Science 221:23–29PubMedCrossRefGoogle Scholar
  7. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–326PubMedCrossRefGoogle Scholar
  8. Bhat KM, Farkas G, Karch F, Gyurkovics H, Gausz J, Schedl P (1996) The GAGA factor is required in the early Drosophila embryo not only for transcriptional regulation but also for nuclear division. Development 122:1113–1124PubMedGoogle Scholar
  9. Blobel GA, Kadauke S, Wang E, Lau AW, Zuber J, Chou MM, Vakoc CR (2009) A reconfigured pattern of MLL occupancy within mitotic chromatin promotes rapid transcriptional reactivation following mitotic exit. Mol Cell 36:970–983PubMedCrossRefGoogle Scholar
  10. Boulet AM, Lloyd A, Sakonju S (1991) Molecular definition of the morphogenetic and regulatory functions and the cis-regulatory elements of the Drosophila Abd-B homeotic gene. Development 111:393–405PubMedGoogle Scholar
  11. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, Vidal M, Gifford DK, Young RA, Jaenisch R (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441:349–353PubMedCrossRefGoogle Scholar
  12. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20:1123–1136PubMedCrossRefGoogle Scholar
  13. Buxton PG, Kostakopoulou K, Brickell P, Thorogood P, Ferretti P (1997) Expression of the transcription factor slug correlates with growth of the limb bud and is regulated by FGF-4 and retinoic acid. Int J Dev Biol 41:559–568PubMedGoogle Scholar
  14. Capelson M, Corces VG (2004) Boundary elements and nuclear organization. Biol Cell 96:617–629PubMedCrossRefGoogle Scholar
  15. Caretti G, Di Padova M, Micales B, Lyons GE, Sartorelli V (2004) The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev 18:2627–2638PubMedCrossRefGoogle Scholar
  16. Carroll SB (1995) Homeotic genes and the evolution of arthropods and chordates. Nature 376:479PubMedCrossRefGoogle Scholar
  17. Casanova M, Preissner T, Cerase A, Poot R, Yamada D, Li X, Appanah R, Bezstarosti K, Demmers J, Koseki H, Brockdorff N (2011) Polycomblike 2 facilitates the recruitment of PRC2 Polycomb group complexes to the inactive X chromosome and to target loci in embryonic stem cells. Development 138:1471–1482PubMedCrossRefGoogle Scholar
  18. Celniker SE, Keelan DJ, Lewis EB (1989) The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the Abdominal-B domain. Genes Dev 3:1424–1436PubMedCrossRefGoogle Scholar
  19. Celniker SE, Sharma S, Keelan DJ, Lewis EB (1990) The molecular genetics of the bithorax complex of Drosophila: cis-regulation in the Abdominal-B domain. EMBO J 9:4277–4286PubMedGoogle Scholar
  20. Chambeyron S, Bickmore WA (2004a) Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev 18:1119–1130PubMedCrossRefGoogle Scholar
  21. Chambeyron S, Bickmore WA (2004b) Does looping and clustering in the nucleus regulate gene expression? Curr Opin Cell Biol 16:256–262PubMedCrossRefGoogle Scholar
  22. Chambeyron S, Da Silva NR, Lawson KA, Bickmore WA (2005) Nuclear re-organisation of the Hoxb complex during mouse embryonic development. Development 132:2215–2223PubMedCrossRefGoogle Scholar
  23. Chan CS, Rastelli L, Pirrotta V (1994) A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J 13:2553–2564PubMedGoogle Scholar
  24. Chen SK, Tvrdik P, Peden E, Cho S, Wu S, Spangrude G, Capecchi MR (2010) Hematopoietic origin of pathological grooming in Hoxb8 mutant mice. Cell 141:775–785PubMedCrossRefGoogle Scholar
  25. Chevallier A, Kieny M, Mauger A (1978) Limb-somite relationship: effect of removal of somitic mesoderm on the wing musculature. J Embryol Exp Morphol 43:263–278PubMedGoogle Scholar
  26. Chopra VS, Hong JW, Levine M (2009) Regulation of Hox gene activity by transcriptional elongation in Drosophila. Curr Biol 19:688–693PubMedCrossRefGoogle Scholar
  27. Christen B, Bienz M (1994) Imaginal disc silencers from Ultrabithorax: evidence for Polycomb response elements. Mech Dev 48:255–266PubMedCrossRefGoogle Scholar
  28. Chung JH, Whiteley M, Felsenfeld G (1993) A 5′ element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell 74:505–514PubMedCrossRefGoogle Scholar
  29. Conlon RA (1995) Retinoic acid and pattern formation in vertebrates. Trends Genet 11:314–319PubMedCrossRefGoogle Scholar
  30. Dahanukar A, Wharton RP (1996) The Nanos gradient in Drosophila embryos is generated by translational regulation. Genes Dev 10:2610–2620PubMedCrossRefGoogle Scholar
  31. Dale L, Jones CM (1999) BMP signalling in early Xenopus development. Bioessays 21:751–760PubMedCrossRefGoogle Scholar
  32. Dekker EJ, Pannese M, Houtzager E, Boncinelli E, Durston A (1993) Colinearity in the Xenopus laevis Hox-2 complex. Mech Dev 40:3–12PubMedCrossRefGoogle Scholar
  33. Denis H, Lacroix JC (1993) The dichotomy between germ line and somatic line, and the origin of cell mortality. Trends Genet 9:7–11PubMedCrossRefGoogle Scholar
  34. Dickinson ME, McMahon AP (1992) The role of Wnt genes in vertebrate development. Curr Opin Genet Dev 2:562–566PubMedCrossRefGoogle Scholar
  35. Dorsett D (1999) Distant liaisons: long-range enhancer-promoter interactions in Drosophila. Curr Opin Genet Dev 9:505–514PubMedCrossRefGoogle Scholar
  36. Driever W, Nusslein-Volhard C (1988a) A gradient of bicoid protein in Drosophila embryos. Cell 54:83–93PubMedCrossRefGoogle Scholar
  37. Driever W, Nusslein-Volhard C (1988b) The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54:95–104PubMedCrossRefGoogle Scholar
  38. Duboule D (1994) Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Development Suppl:135–142Google Scholar
  39. Duboule D (2007) The rise and fall of Hox gene clusters. Development 134:2549–2560PubMedCrossRefGoogle Scholar
  40. Duncan I (1987) The bithorax complex. Annu Rev Genet 21:285–319PubMedCrossRefGoogle Scholar
  41. Ebralidse KK, Grachev SA, Mirzabekov AD (1988) A highly basic histone H4 domain bound to the sharply bent region of nucleosomal DNA. Nature 331:365–367PubMedCrossRefGoogle Scholar
  42. Endoh M, Endo TA, Endoh T, Fujimura Y, Ohara O, Toyoda T, Otte AP, Okano M, Brockdorff N, Vidal M, Koseki H (2008) Polycomb group proteins Ring1A/B are functionally linked to the core transcriptional regulatory circuitry to maintain ES cell identity. Development 135:1513–1524PubMedCrossRefGoogle Scholar
  43. Ferraiuolo MA, Rousseau M, Miyamoto C, Shenker S, Wang XQ, Nadler M, Blanchette M, Dostie J (2010) The three-dimensional architecture of Hox cluster silencing. Nucleic Acids Res 38:7472–7484PubMedCrossRefGoogle Scholar
  44. Flam F (1994) Hints of a language in junk DNA. Science 266:1320PubMedCrossRefGoogle Scholar
  45. Fromental-Ramain C, Warot X, Messadecq N, LeMeur M, Dolle P, Chambon P (1996) Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 122:2997–3011PubMedGoogle Scholar
  46. Gaszner M, Felsenfeld G (2006) Insulators: exploiting transcriptional and epigenetic mechanisms. Nat Rev Genet 7:703–713PubMedCrossRefGoogle Scholar
  47. Gaunt SJ (1994) Conservation in the Hox code during morphological evolution. Int J Dev Biol 38:549–552PubMedGoogle Scholar
  48. Gaunt SJ, Strachan L (1996) Temporal colinearity in expression of anterior Hox genes in developing chick embryos. Dev Dyn 207:270–280PubMedCrossRefGoogle Scholar
  49. Gause M, Morcillo P, Dorsett D (2001) Insulation of enhancer-promoter communication by a gypsy transposon insert in the Drosophila cut gene: cooperation between suppressor of hairy-wing and modifier of mdg4 proteins. Mol Cell Biol 21:4807–4817PubMedCrossRefGoogle Scholar
  50. Gehring WJ, Hiromi Y (1986) Homeotic genes and the homeobox. Annu Rev Genet 20:147–173PubMedCrossRefGoogle Scholar
  51. Gerard M, Zakany J, Duboule D (1997) Interspecies exchange of a Hoxd enhancer in vivo induces premature transcription and anterior shift of the sacrum. Dev Biol 190:32–40PubMedCrossRefGoogle Scholar
  52. Gerasimova TI, Corces VG (2001) Chromatin insulators and boundaries: effects on transcription and nuclear organization. Annu Rev Genet 35:193–208PubMedCrossRefGoogle Scholar
  53. Gillespie RF, Gudas LJ (2007) Retinoid regulated association of transcriptional co-regulators and the polycomb group protein SUZ12 with the retinoic acid response elements of Hoxa1, RARbeta(2), and Cyp26A1 in F9 embryonal carcinoma cells. J Mol Biol 372:298–316PubMedCrossRefGoogle Scholar
  54. Glass CK, Rosenfeld MG (2000) The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev 14:121–141PubMedGoogle Scholar
  55. Gohl D, Aoki T, Blanton J, Shanower G, Kappes G, Schedl P (2011) Mechanism of chromosomal boundary action: roadblock, sink, or loop? Genetics 187:731–748PubMedCrossRefGoogle Scholar
  56. Goodman F, Giovannucci-Uzielli ML, Hall C, Reardon W, Winter R, Scambler P (1998) Deletions in HOXD13 segregate with an identical, novel foot malformation in two unrelated families. Am J Hum Genet 63:992–1000PubMedCrossRefGoogle Scholar
  57. Gould A, Morrison A, Sproat G, White RA, Krumlauf R (1997) Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev 11:900–913PubMedCrossRefGoogle Scholar
  58. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77–88PubMedCrossRefGoogle Scholar
  59. Hanson RD, Hess JL, Yu BD, Ernst P, van Lohuizen M, Berns A, van der Lugt NM, Shashikant CS, Ruddle FH, Seto M, Korsmeyer SJ (1999) Mammalian Trithorax and polycomb-group homologues are antagonistic regulators of homeotic development. Proc Natl Acad Sci USA 96:14372–14377PubMedCrossRefGoogle Scholar
  60. Herault Y, Beckers J, Gerard M, Duboule D (1999) Hox gene expression in limbs: colinearity by opposite regulatory controls. Dev Biol 208:157–165PubMedCrossRefGoogle Scholar
  61. Hernandez RE, Putzke AP, Myers JP, Margaretha L, Moens CB (2007) Cyp26 enzymes generate the retinoic acid response pattern necessary for hindbrain development. Development 134:177–187PubMedCrossRefGoogle Scholar
  62. Hogan BL (1996) Bone morphogenetic proteins in development. Curr Opin Genet Dev 6:432–438PubMedCrossRefGoogle Scholar
  63. Holland PW, Holland LZ, Williams NA, Holland ND (1992) An amphioxus homeobox gene: sequence conservation, spatial expression during development and insights into vertebrate evolution. Development 116:653–661PubMedGoogle Scholar
  64. Holstege JC, de Graaff W, Hossaini M, Cano SC, Jaarsma D, van den Akker E, Deschamps J (2008) Loss of Hoxb8 alters spinal dorsal laminae and sensory responses in mice. Proc Natl Acad Sci U S A 105:6338–6343PubMedCrossRefGoogle Scholar
  65. Horton C, Maden M (1995) Endogenous distribution of retinoids during normal development and teratogenesis in the mouse embryo. Dev Dyn 202:312–323PubMedCrossRefGoogle Scholar
  66. Hsieh JJ, Cheng EH, Korsmeyer SJ (2003) Taspase1: a threonine aspartase required for cleavage of MLL and proper HOX gene expression. Cell 115:293–303PubMedCrossRefGoogle Scholar
  67. Hughes CM, Rozenblatt-Rosen O, Milne TA, Copeland TD, Levine SS, Lee JC, Hayes DN, Shanmugam KS, Bhattacharjee A, Biondi CA, Kay GF, Hayward NK, Hess JL, Meyerson M (2004) Menin associates with a trithorax family histone methyltransferase complex and with the hoxc8 locus. Mol Cell 13:587–597PubMedCrossRefGoogle Scholar
  68. Iimura T, Denans N, Pourquie O (2009) Establishment of Hox vertebral identities in the embryonic spine precursors. Curr Top Dev Biol 88:201–234PubMedCrossRefGoogle Scholar
  69. Iqbal H, Mishra R (2007) Chromatin domain boundaries: defining the functional domains in genome. Proc Indian Natl Sci Acad 73:239–253Google Scholar
  70. Jepsen K, Solum D, Zhou T, McEvilly RJ, Kim HJ, Glass CK, Hermanson O, Rosenfeld MG (2007) SMRT-mediated repression of an H3K27 demethylase in progression from neural stem cell to neuron. Nature 450:415–419PubMedCrossRefGoogle Scholar
  71. Joo HY, Zhai L, Yang C, Nie S, Erdjument-Bromage H, Tempst P, Chang C, Wang H (2007) Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature 449:1068–1072PubMedCrossRefGoogle Scholar
  72. Juan AH, Ruddle FH (2003) Enhancer timing of Hox gene expression: deletion of the endogenous Hoxc8 early enhancer. Development 130:4823–4834PubMedCrossRefGoogle Scholar
  73. Karch F, Weiffenbach B, Peifer M, Bender W, Duncan I, Celniker S, Crosby M, Lewis EB (1985) The abdominal region of the bithorax complex. Cell 43:81–96PubMedCrossRefGoogle Scholar
  74. Karch F, Galloni M, Sipos L, Gausz J, Gyurkovics H, Schedl P (1994) Mcp and Fab-7: molecular analysis of putative boundaries of cis-regulatory domains in the bithorax complex of Drosophila melanogaster. Nucleic Acids Res 22:3138–3146PubMedCrossRefGoogle Scholar
  75. Kashyap V, Gudas LJ, Brenet F, Funk P, Viale A, Scandura JM (2011) Epigenomic reorganization of the clustered Hox genes in embryonic stem cells induced by retinoic acid. J Biol Chem 286:3250–3260PubMedCrossRefGoogle Scholar
  76. Kastner P, Mark M, Chambon P (1995) Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell 83:859–869PubMedCrossRefGoogle Scholar
  77. Katsube K, Sakamoto K, Tamamura Y, Yamaguchi A (2009) Role of CCN, a vertebrate specific gene family, in development. Dev Growth Differ 51:55–67PubMedCrossRefGoogle Scholar
  78. Kennison JA (1995) The Polycomb and trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu Rev Genet 29:289–303PubMedCrossRefGoogle Scholar
  79. Kessel M, Gruss P (1991) Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67:89–104PubMedCrossRefGoogle Scholar
  80. Klebes A, Sustar A, Kechris K, Li H, Schubiger G, Kornberg TB (2005) Regulation of cellular plasticity in Drosophila imaginal disc cells by the Polycomb group, trithorax group and lama genes. Development 132:3753–3765PubMedCrossRefGoogle Scholar
  81. Kmita M, van Der Hoeven F, Zakany J, Krumlauf R, Duboule D (2000) Mechanisms of Hox gene colinearity: transposition of the anterior Hoxb1 gene into the posterior HoxD complex. Genes Dev 14:198–211PubMedGoogle Scholar
  82. Kmita M, Fraudeau N, Herault Y, Duboule D (2002a) Serial deletions and duplications suggest a mechanism for the collinearity of Hoxd genes in limbs. Nature 420:145–150PubMedCrossRefGoogle Scholar
  83. Kmita M, Tarchini B, Duboule D, Herault Y (2002b) Evolutionary conserved sequences are required for the insulation of the vertebrate Hoxd complex in neural cells. Development 129:5521–5528PubMedCrossRefGoogle Scholar
  84. Kondo T, Duboule D (1999) Breaking colinearity in the mouse HoxD complex. Cell 97:407–417PubMedCrossRefGoogle Scholar
  85. Kondo T, Dolle P, Zakany J, Duboule D (1996) Function of posterior HoxD genes in the morphogenesis of the anal sphincter. Development 122:2651–2659PubMedGoogle Scholar
  86. Kondo T, Zakany J, Duboule D (1998) Control of colinearity in AbdB genes of the mouse HoxD complex. Mol Cell 1:289–300PubMedCrossRefGoogle Scholar
  87. Krumlauf R (1992) Evolution of the vertebrate Hox homeobox genes. Bioessays 14:245–252PubMedCrossRefGoogle Scholar
  88. Krumlauf R (1994) Hox genes in vertebrate development. Cell 78:191–201PubMedCrossRefGoogle Scholar
  89. Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, Mikkelsen TS, Presser A, Nusbaum C, Xie X, Chi AS, Adli M, Kasif S, Ptaszek LM, Cowan CA, Lander ES, Koseki H, Bernstein BE (2008) Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4:e1000242PubMedCrossRefGoogle Scholar
  90. Kudoh T, Wilson SW, Dawid IB (2002) Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. Development 129:4335–4346PubMedGoogle Scholar
  91. Kuhn EJ, Geyer PK (2003) Genomic insulators: connecting properties to mechanism. Curr Opin Cell Biol 15:259–265PubMedCrossRefGoogle Scholar
  92. Lagarou A, Mohd-Sarip A, Moshkin YM, Chalkley GE, Bezstarosti K, Demmers JA, Verrijzer CP (2008) dKDM2 couples histone H2A ubiquitylation to histone H3 demethylation during Polycomb group silencing. Genes Dev 22:2799–2810PubMedCrossRefGoogle Scholar
  93. Lambert SF, Thomas JO (1986) Lysine-containing DNA-binding regions on the surface of the histone octamer in the nucleosome core particle. Eur J Biochem 160:191–201PubMedCrossRefGoogle Scholar
  94. Lan F, Bayliss PE, Rinn JL, Whetstine JR, Wang JK, Chen S, Iwase S, Alpatov R, Issaeva I, Canaani E, Roberts TM, Chang HY, Shi Y (2007) A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449:689–694PubMedCrossRefGoogle Scholar
  95. Landeira D, Sauer S, Poot R, Dvorkina M, Mazzarella L, Jorgensen HF, Pereira CF, Leleu M, Piccolo FM, Spivakov M, Brookes E, Pombo A, Fisher C, Skarnes WC, Snoek T, Bezstarosti K, Demmers J, Klose RJ, Casanova M, Tavares L, Brockdorff N, Merkenschlager M, Fisher AG (2010) Jarid2 is a PRC2 component in embryonic stem cells required for multi-lineage differentiation and recruitment of PRC1 and RNA Polymerase II to developmental regulators. Nat Cell Biol 12:618–624PubMedCrossRefGoogle Scholar
  96. Lanzuolo C, Roure V, Dekker J, Bantignies F, Orlando V (2007) Polycomb response elements mediate the formation of chromosome higher-order structures in the bithorax complex. Nat Cell Biol 9:1167–1174PubMedCrossRefGoogle Scholar
  97. Lee KK (1992) The regulative potential of the limb region in 11.5-day rat embryos following the amputation of the fore-limb bud. Anat Embryol (Berl) 186:67–74CrossRefGoogle Scholar
  98. Lee KK, Chan WY (1991) A study on the regenerative potential of partially excised mouse embryonic fore-limb bud. Anat Embryol (Berl) 184:153–157CrossRefGoogle Scholar
  99. Lee N, Maurange C, Ringrose L, Paro R (2005) Suppression of Polycomb group proteins by JNK signalling induces transdetermination in Drosophila imaginal discs. Nature 438:234–237PubMedCrossRefGoogle Scholar
  100. Lee MG, Villa R, Trojer P, Norman J, Yan KP, Reinberg D, Di Croce L, Shiekhattar R (2007) Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318:447–450PubMedCrossRefGoogle Scholar
  101. Leid M, Kastner P, Chambon P (1992) Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem Sci 17:427–433PubMedCrossRefGoogle Scholar
  102. Levine M, Hoey T (1988) Homeobox proteins as sequence-specific transcription factors. Cell 55:537–540PubMedCrossRefGoogle Scholar
  103. Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276:565–570PubMedCrossRefGoogle Scholar
  104. Li G, Margueron R, Ku M, Chambon P, Bernstein BE, Reinberg D (2010) Jarid2 and PRC2, partners in regulating gene expression. Genes Dev 24:368–380PubMedCrossRefGoogle Scholar
  105. Li HB, Muller M, Bahechar IA, Kyrchanova O, Ohno K, Georgiev P, Pirrotta V (2011) Insulators, not Polycomb response elements, are required for long-range interactions between Polycomb targets in Drosophila melanogaster. Mol Cell Biol 31:616–625PubMedCrossRefGoogle Scholar
  106. Lipshitz HD, Peattie DA, Hogness DS (1987) Novel transcripts from the Ultrabithorax domain of the bithorax complex. Genes Dev 1:307–322PubMedCrossRefGoogle Scholar
  107. Lutz B, Lu HC, Eichele G, Miller D, Kaufman TC (1996) Rescue of Drosophila labial null mutant by the chicken ortholog Hoxb-1 demonstrates that the function of Hox genes is phylogenetically conserved. Genes Dev 10:176–184PubMedCrossRefGoogle Scholar
  108. Maconochie M, Nonchev S, Morrison A, Krumlauf R (1996) Paralogous Hox genes: function and regulation. Annu Rev Genet 30:529–556PubMedCrossRefGoogle Scholar
  109. Maden M, Ong DE, Summerbell D, Chytil F (1988) Spatial distribution of cellular protein binding to retinoic acid in the chick limb bud. Nature 335:733–735PubMedCrossRefGoogle Scholar
  110. Maeda RK, Karch F (2006) The ABC of the BX-C: the bithorax complex explained. Development 133:1413PubMedCrossRefGoogle Scholar
  111. Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ 3rd, Voigt P, Martin SR, Taylor WR, De Marco V, Pirrotta V, Reinberg D, Gamblin SJ (2009) Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461:762–767PubMedCrossRefGoogle Scholar
  112. Mark M, Ghyselinck NB, Chambon P (2004) Retinoic acid signalling in the development of branchial arches. Curr Opin Genet Dev 14:591–598PubMedCrossRefGoogle Scholar
  113. Mark M, Ghyselinck NB, Chambon P (2006) Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu Rev Pharmacol Toxicol 46:451–480PubMedCrossRefGoogle Scholar
  114. Mark M, Ghyselinck NB, Chambon P (2009) Function of retinoic acid receptors during embryonic development. Nucl Recept Signal 7:e002PubMedGoogle Scholar
  115. Martin C, Cao R, Zhang Y (2006) Substrate preferences of the EZH2 histone methyltransferase complex. J Biol Chem 281:8365–8370PubMedCrossRefGoogle Scholar
  116. Matharu NK, Hussain T, Sankaranarayanan R, Mishra RK (2010) Vertebrate homologue of Drosophila GAGA factor. J Mol Biol 400:434–447PubMedCrossRefGoogle Scholar
  117. Maurange C, Lee N, Paro R (2006) Signaling meets chromatin during tissue regeneration in Drosophila. Curr Opin Genet Dev 16:485–489PubMedCrossRefGoogle Scholar
  118. McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283–302PubMedCrossRefGoogle Scholar
  119. Mihaly J, Hogga I, Barges S, Galloni M, Mishra RK, Hagstrom K, Muller M, Schedl P, Sipos L, Gausz J, Gyurkovics H, Karch F (1998) Chromatin domain boundaries in the Bithorax complex. Cell Mol Life Sci 54:60–70PubMedCrossRefGoogle Scholar
  120. Milinkovitch MC, Helaers R, Tzika AC (2010) Historical constraints on vertebrate genome evolution. Genome Biol Evol 2:13–18CrossRefGoogle Scholar
  121. Minsky N, Shema E, Field Y, Schuster M, Segal E, Oren M (2008) Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat Cell Biol 10:483–488PubMedCrossRefGoogle Scholar
  122. Mishra RK, Karch F (1999) Boundaries that demarcate structural and functional domains of chromatin. J Biosci 24:377–399CrossRefGoogle Scholar
  123. Mishra RK, Yamagishi T, Vasanthi D, Ohtsuka C, Kondo T (2007) Involvement of polycomb-group genes in establishing HoxD temporal colinearity. Genesis 45:570–576PubMedCrossRefGoogle Scholar
  124. Mohd-Sarip A, van der Knaap JA, Wyman C, Kanaar R, Schedl P, Verrijzer CP (2006) Architecture of a polycomb nucleoprotein complex. Mol Cell 24:91–100PubMedCrossRefGoogle Scholar
  125. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, Bibel M, Schubeler D (2008) Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30:755–766PubMedCrossRefGoogle Scholar
  126. Moon RT, Brown JD, Torres M (1997) WNTs modulate cell fate and behavior during vertebrate development. Trends Genet 13:157–162PubMedCrossRefGoogle Scholar
  127. Moon H, Filippova G, Loukinov D, Pugacheva E, Chen Q, Smith ST, Munhall A, Grewe B, Bartkuhn M, Arnold R, Burke LJ, Renkawitz-Pohl R, Ohlsson R, Zhou J, Renkawitz R, Lobanenkov V (2005) CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator. EMBO Rep 6:165–170PubMedCrossRefGoogle Scholar
  128. Morey C, Da Silva NR, Perry P, Bickmore WA (2007) Nuclear reorganisation and chromatin decondensation are conserved, but distinct, mechanisms linked to Hox gene activation. Development 134:909–919PubMedCrossRefGoogle Scholar
  129. Morey C, Da Silva NR, Kmita M, Duboule D, Bickmore WA (2008) Ectopic nuclear reorganisation driven by a Hoxb1 transgene transposed into Hoxd. J Cell Sci 121:571–577PubMedCrossRefGoogle Scholar
  130. Muragaki Y, Mundlos S, Upton J, Olsen BR (1996) Altered growth and branching patterns in synpolydactyly caused by mutations in HOXD13. Science 272:548–551PubMedCrossRefGoogle Scholar
  131. Ng HH, Robert F, Young RA, Struhl K (2003) Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11:709–719PubMedCrossRefGoogle Scholar
  132. Nusslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287:795–801PubMedCrossRefGoogle Scholar
  133. Ohtsuki S, Levine M (1998) GAGA mediates the enhancer blocking activity of the eve promoter in the Drosophila embryo. Genes Dev 12:3325–3330PubMedCrossRefGoogle Scholar
  134. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, Guigo R, Shiekhattar R (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143:46–58PubMedCrossRefGoogle Scholar
  135. Pasini D, Hansen KH, Christensen J, Agger K, Cloos PA, Helin K (2008) Coordinated regulation of transcriptional repression by the RBP2 H3K4 demethylase and polycomb-repressive complex 2. Genes Dev 22:1345–1355PubMedCrossRefGoogle Scholar
  136. Pasini D, Cloos PA, Walfridsson J, Olsson L, Bukowski JP, Johansen JV, Bak M, Tommerup N, Rappsilber J, Helin K (2010) JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464:306–310PubMedCrossRefGoogle Scholar
  137. Pathak RU, Rangaraj N, Kallappagoudar S, Mishra K, Mishra RK (2007) Boundary element-associated factor 32B connects chromatin domains to the nuclear matrix. Mol Cell Biol 27:4796–4806PubMedCrossRefGoogle Scholar
  138. Raab JR, Kamakaka RT (2010) Insulators and promoters: closer than we think. Nat Rev Genet 11:439–446PubMedCrossRefGoogle Scholar
  139. Ragoczy T, Bender MA, Telling A, Byron R, Groudine M (2006) The locus control region is required for association of the murine beta-globin locus with engaged transcription factories during erythroid maturation. Genes Dev 20:1447–1457PubMedCrossRefGoogle Scholar
  140. Richly H, Rocha-Viegas L, Ribeiro JD, Demajo S, Gundem G, Lopez-Bigas N, Nakagawa T, Rospert S, Ito T, Di Croce L (2010) Transcriptional activation of polycomb-repressed genes by ZRF1. Nature 468:1124–1128PubMedCrossRefGoogle Scholar
  141. Ringrose L, Paro R (2004) Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38:413–443PubMedCrossRefGoogle Scholar
  142. Ringrose L, Rehmsmeier M, Dura JM, Paro R (2003) Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster. Dev Cell 5:759–771PubMedCrossRefGoogle Scholar
  143. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129:1311–1323PubMedCrossRefGoogle Scholar
  144. Sarras MP Jr, Yan L, Leontovich A, Zhang JS (2002) Structure, expression, and developmental function of early divergent forms of metalloproteinases in hydra. Cell Res 12:163–176PubMedCrossRefGoogle Scholar
  145. Saunders A, Werner J, Andrulis ED, Nakayama T, Hirose S, Reinberg D, Lis JT (2003) Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 301:1094–1096PubMedCrossRefGoogle Scholar
  146. Savla U, Benes J, Zhang J, Jones RS (2008) Recruitment of Drosophila Polycomb-group proteins by Polycomblike, a component of a novel protein complex in larvae. Development 135:813–817PubMedCrossRefGoogle Scholar
  147. Scheuermann JC, de Ayala Alonso AG, Oktaba K, Ly-Hartig N, McGinty RK, Fraterman S, Wilm M, Muir TW, Muller J (2010) Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nature 465:243–247PubMedCrossRefGoogle Scholar
  148. Schier AF, Talbot WS (2005) Molecular genetics of axis formation in zebrafish. Annu Rev Genet 39:561–613PubMedCrossRefGoogle Scholar
  149. Schmitt S, Prestel M, Paro R (2005) Intergenic transcription through a polycomb group response element counteracts silencing. Genes Dev 19:697–708PubMedCrossRefGoogle Scholar
  150. Schoeftner S, Sengupta AK, Kubicek S, Mechtler K, Spahn L, Koseki H, Jenuwein T, Wutz A (2006) Recruitment of PRC1 function at the initiation of X inactivation independent of PRC2 and silencing. EMBO J 25:3110–3122PubMedCrossRefGoogle Scholar
  151. Schwartz YB, Kahn TG, Nix DA, Li XY, Bourgon R, Biggin M, Pirrotta V (2006) Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38:700–705PubMedCrossRefGoogle Scholar
  152. Scott MP, Tamkun JW, Hartzell GW 3rd (1989) The structure and function of the homeodomain. Biochim Biophys Acta 989:25–48PubMedGoogle Scholar
  153. Senthilkumar R, Mishra RK (2009) Novel motifs distinguish multiple homologues of Polycomb in vertebrates: expansion and diversification of the epigenetic toolkit. BMC Genomics 10:549PubMedCrossRefGoogle Scholar
  154. Sessa L, Breiling A, Lavorgna G, Silvestri L, Casari G, Orlando V (2007) Noncoding RNA synthesis and loss of Polycomb group repression accompanies the colinear activation of the human HOXA cluster. RNA 13:223–239PubMedCrossRefGoogle Scholar
  155. Sharpe J, Nonchev S, Gould A, Whiting J, Krumlauf R (1998) Selectivity, sharing and competitive interactions in the regulation of Hoxb genes. EMBO J 17:1788–1798PubMedCrossRefGoogle Scholar
  156. Shilatifard A (2006) Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75:243–269PubMedCrossRefGoogle Scholar
  157. Simon J, Chiang A, Bender W, Shimell MJ, O’Connor M (1993) Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev Biol 158:131–144PubMedCrossRefGoogle Scholar
  158. Sing A, Pannell D, Karaiskakis A, Sturgeon K, Djabali M, Ellis J, Lipshitz HD, Cordes SP (2009) A vertebrate Polycomb response element governs segmentation of the posterior hindbrain. Cell 138:885–897PubMedCrossRefGoogle Scholar
  159. Slack JM (1990) Growth factors as inducing agents in early Xenopus development. J Cell Sci 13(Suppl):119–130Google Scholar
  160. Soshnikova N, Duboule D (2009) Epigenetic temporal control of mouse Hox genes in vivo. Science 324:1320–1323PubMedCrossRefGoogle Scholar
  161. Stock JK, Giadrossi S, Casanova M, Brookes E, Vidal M, Koseki H, Brockdorff N, Fisher AG, Pombo A (2007) Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat Cell Biol 9:1428–1435PubMedCrossRefGoogle Scholar
  162. Stratford T, Horton C, Maden M (1996) Retinoic acid is required for the initiation of outgrowth in the chick limb bud. Curr Biol 6:1124–1133PubMedCrossRefGoogle Scholar
  163. Suganuma T, Workman JL (2008) Crosstalk among histone modifications. Cell 135:604–607PubMedCrossRefGoogle Scholar
  164. Sutherland H, Bickmore WA (2009) Transcription factories: gene expression in unions? Nat Rev Genet 10:457–466PubMedCrossRefGoogle Scholar
  165. Tian D, Sun S, Lee JT (2010) The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 143:390–403PubMedCrossRefGoogle Scholar
  166. Tillib S, Petruk S, Sedkov Y, Kuzin A, Fujioka M, Goto T, Mazo A (1999) Trithorax- and Polycomb-group response elements within an Ultrabithorax transcription maintenance unit consist of closely situated but separable sequences. Mol Cell Biol 19:5189–5202PubMedGoogle Scholar
  167. Tiwari VK, McGarvey KM, Licchesi JD, Ohm JE, Herman JG, Schubeler D, Baylin SB (2008) PcG proteins, DNA methylation, and gene repression by chromatin looping. PLoS Biol 6:2911–2927PubMedCrossRefGoogle Scholar
  168. Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W (2002) Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 10:1453–1465PubMedCrossRefGoogle Scholar
  169. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329:689–693PubMedCrossRefGoogle Scholar
  170. Valenzuela L, Kamakaka RT (2006) Chromatin insulators. Annu Rev Genet 40:107–138PubMedCrossRefGoogle Scholar
  171. van den Akker E, Fromental-Ramain C, de Graaff W, Le Mouellic H, Brulet P, Chambon P, Deschamps J (2001) Axial skeletal patterning in mice lacking all paralogous group 8 Hox genes. Development 128:1911–1921PubMedGoogle Scholar
  172. Vasanthi D, Mishra RK (2008) Epigenetic regulation of genes during development: a conserved theme from flies to mammals. J Genet Genomics 35:413–429PubMedCrossRefGoogle Scholar
  173. Vasanthi D, Anant M, Srivastava S, Mishra RK (2010) A functionally conserved boundary element from the mouse HoxD locus requires GAGA factor in Drosophila. Development 137:4239–4247PubMedCrossRefGoogle Scholar
  174. Vastenhouw NL, Zhang Y, Woods IG, Imam F, Regev A, Liu XS, Rinn J, Schier AF (2010) Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464:922–926PubMedCrossRefGoogle Scholar
  175. Vazquez J, Farkas G, Gaszner M, Udvardy A, Muller M, Hagstrom K, Gyurkovics H, Sipos L, Gausz J, Galloni M et al (1993) Genetic and molecular analysis of chromatin domains. Cold Spring Harb Symp Quant Biol 58:45–54PubMedCrossRefGoogle Scholar
  176. Wan Y, Chiang JH, Lin CH, Arens CE, Saleem RA, Smith JJ, Aitchison JD (2010) Histone chaperone Chz1p regulates H2B ubiquitination and subtelomeric anti-silencing. Nucleic Acids Res 38:1431–1440PubMedCrossRefGoogle Scholar
  177. Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS, Zhang Y (2004) Role of histone H2A ubiquitination in Polycomb silencing. Nature 431:873–878PubMedCrossRefGoogle Scholar
  178. Wellik DM, Capecchi MR (2003) Hox10 and Hox11 genes are required to globally pattern the mammalian skeleton. Science 301:363–367PubMedCrossRefGoogle Scholar
  179. West AG, Gaszner M, Felsenfeld G (2002) Insulators: many functions, many mechanisms. Genes Dev 16:271–288PubMedCrossRefGoogle Scholar
  180. Woo CJ, Kingston RE (2007) HOTAIR lifts noncoding RNAs to new levels. Cell 129:1257–1259PubMedCrossRefGoogle Scholar
  181. Woo CJ, Kharchenko PV, Daheron L, Park PJ, Kingston RE (2010) A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 140:99–110PubMedCrossRefGoogle Scholar
  182. Workman JL, Kingston RE (1998) Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem 67:545–579PubMedCrossRefGoogle Scholar
  183. Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329:444–448PubMedCrossRefGoogle Scholar
  184. Wysocka J, Milne TA, Allis CD (2005) Taking LSD 1 to a new high. Cell 122:654–658PubMedCrossRefGoogle Scholar
  185. Yamagishi T, Ozawa M, Ohtsuka C, Ohyama-Goto R, Kondo T (2007) Evx2-Hoxd13 intergenic region restricts enhancer association to Hoxd13 promoter. PLoS One 2:e175PubMedCrossRefGoogle Scholar
  186. Yamaguchi TP, Rossant J (1995) Fibroblast growth factors in mammalian development. Curr Opin Genet Dev 5:485–491PubMedCrossRefGoogle Scholar
  187. Zakany J, Gerard M, Favier B, Duboule D (1997) Deletion of a HoxD enhancer induces transcriptional heterochrony leading to transposition of the sacrum. EMBO J 16:4393–4402PubMedCrossRefGoogle Scholar
  188. Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, Song JJ, Kingston RE, Borowsky M, Lee JT (2010) Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell 40:939–953PubMedCrossRefGoogle Scholar
  189. Zhou W, Zhu P, Wang J, Pascual G, Ohgi KA, Lozach J, Glass CK, Rosenfeld MG (2008) Histone H2A monoubiquitination represses transcription by inhibiting RNA polymerase II transcriptional elongation. Mol Cell 29:69–80PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Navneet K. Matharu
    • 1
  • Vasanthi Dasari
    • 1
  • Rakesh K. Mishra
    • 1
    Email author
  1. 1.Centre for Cellular and Molecular BiologyCouncil of Scientific and Industrial Research (CSIR)HyderabadIndia

Personalised recommendations