Hox gene regulation and timing in embryogenesis

Seminars in Cell and Developmental Biology

Volumn 34, Issue , 2014, Pages 76-84

  Montavon, Thomas ^a   Soshnikova, Natalia ^b  

^a MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^b Institute of Molecular Biology gGmbH (IMB)   (Germany)

Author keywords

Collinearity; Enhancers; Gene clusters; Long range interactions; Polycomb

Indexed keywords

ANTERIOR POSTERIOR AXIS; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CHROMATIN STRUCTURE; EMBRYO DEVELOPMENT; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; GENETIC ORGANIZATION; GENOMICS; HOX GENE; NONHUMAN; PROMOTER REGION; REVIEW; TRANSCRIPTION INITIATION; UPREGULATION; ANIMAL; CHROMATIN; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MULTIGENE FAMILY;

CHROMATIN; HOMEODOMAIN PROTEIN;

ANIMALS; CHROMATIN; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; MULTIGENE FAMILY;

EID: 84914118887     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.06.005     Document Type: Review

References (117)

1. Alexander T., Nolte C., Krumlauf R. Hox genes and segmentation of the hindbrain and axial skeleton. Annu Rev Cell Dev Biol 2009, 25:431-456.
2. Gendron-Maguire M., Mallo M., Zhang M., Gridley T. Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell 1993, 75:1317-1331.
3. Kaufman T.C. Cytogenetic analysis of chromosome 3 in DROSOPHILA MELANOGASTER: isolation and characterization of four new alleles of the proboscipedia (pb) locus. Genetics 1978, 90:579-596.
4. Rijli F.M., Mark M., Lakkaraju S., Dierich A., Dolle P., Chambon P. A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell 1993, 75:1333-1349.
5. Denell R.E., Hummels K.R., Wakimoto B.T., Kaufman T.C. Developmental studies of lethality associated with the antennapedia gene complex in Drosophila melanogaster. Dev Biol 1981, 81:43-50.
6. Grammatopoulos G.A., Bell E., Toole L., Lumsden A., Tucker A.S. Homeotic transformation of branchial arch identity after Hoxa2 overexpression. Development 2000, 127:5355-5365.
7. Tschopp P., Duboule D. A regulatory 'landscape effect' over the HoxD cluster. Dev Biol 2011, 351:288-296.
8. van de Ven C., Bialecka M., Neijts R., Young T., Rowland J.E., Stringer E.J., et al. Concerted involvement of Cdx/Hox genes and Wnt signaling in morphogenesis of the caudal neural tube and cloacal derivatives from the posterior growth zone. Development 2011, 138:3451-3462.
9. Zakany J., Duboule D. The role of Hox genes during vertebrate limb development. Curr Opin Genet Dev 2007, 17:359-366.
10. Kondrashov N., Pusic A., Stumpf C.R., Shimizu K., Hsieh A.C., Xue S., et al. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 2011, 145:383-397.
11. Duboule D. The rise and fall of Hox gene clusters. Development 2007, 134:2549-2560.
12. Maeda R.K., Karch F. The bithorax complex of Drosophila an exceptional Hox cluster. Curr Top Dev Biol 2009, 88:1-33.
13. Mallo M., Alonso C.R. The regulation of Hox gene expression during animal development. Development 2013, 140:3951-3963.
14. Pascual-Anaya J., D'Aniello S., Kuratani S., Garcia-Fernandez J. Evolution of Hox gene clusters in deuterostomes. BMC Dev Biol 2013, 13:26.
15. Ohno S. Gene duplication and the uniqueness of vertebrate genomes circa 1970-1999. Semin Cell Dev Biol 1999, 10:517-522.
16. Gaunt S.J., Sharpe P.T., Duboule D. Spatially restricted domains of homeo-gene transcripts in mouse embryos: relation to a segmented body plan. Development (Suppl) 1988, 104:169-170.
17. Graham A., Papalopulu N., Krumlauf R. The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell 1989, 57:367-378.
18. Seo H.C., Edvardsen R.B., Maeland A.D., Bjordal M., Jensen M.F., Hansen A., et al. Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 2004, 431:67-71.
19. Izpisua Belmonte J.C., Falkenstein H., Dollé P., Renucci A., Duboule D. Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J 1991, 10:2279-2289.
20. Tschopp P., Tarchini B., Spitz F., Zakany J., Duboule D. Uncoupling time and space in the collinear regulation of Hox genes. PLoS Genet 2009, 5:e1000398.
21. Young T., Rowland J.E., van de Ven C., Bialecka M., Novoa A., Carapuco M., et al. Cdx and Hox genes differentially regulate posterior axial growth in mammalian embryos. Dev Cell 2009, 17:516-526.
22. Soshnikova N., Duboule D. Epigenetic temporal control of mouse Hox genes in vivo. Science 2009, 324:1320-1323.
23. Deschamps J., Wijgerde M. Two phases in the establishment of HOX expression domains. Dev Biol 1993, 156:473-480.
24. Gaunt S.J., Strachan L. Forward spreading in the establishment of a vertebrate Hox expression boundary: the expression domain separates into anterior and posterior zones, and the spread occurs across implanted glass barriers. Dev Dyn 1994, 199:229-240.
25. Deschamps J., van Nes J. Developmental regulation of the Hox genes during axial morphogenesis in the mouse. Development 2005, 132:2931-2942.
26. Dolle P., Izpisua-Belmonte J.C., Brown J.M., Tickle C., Duboule D. HOX-4 genes and the morphogenesis of mammalian genitalia. Genes Dev 1991, 5:1767-1777.
27. Kmita M., Fraudeau N., Herault Y., Duboule D. Serial deletions and duplications suggest a mechanism for the collinearity of Hoxd genes in limbs. Nature 2002, 420:145-150.
28. Montavon T., Le Garrec J.F., Kerszberg M., Duboule D. Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness. Genes Dev 2008, 22:346-359.
29. Montavon T., Soshnikova N., Mascrez B., Joye E., Thevenet L., Splinter E., et al. A regulatory archipelago controls Hox genes transcription in digits. Cell 2011, 147:1132-1145.
30. Dollé P., Izpisua Belmonte J.C., Falkenstein H., Renucci A., Duboule D. Coordinate expression of the murine Hox-5 complex homoeobox-containing genes during limb pattern formation. Nature 1989, 342:767-772.
31. Young T., Deschamps J. Hox, Cdx, and anteroposterior patterning in the mouse embryo. Curr Top Dev Biol 2009, 88:235-255.
32. Deschamps J., van den Akker E., Forlani S., De Graaff W., Oosterveen T., Roelen B., et al. Initiation, establishment and maintenance of Hox gene expression patterns in the mouse. Int J Dev Biol 1999, 43:635-650.
33. van der Hoeven F., Zakany J., Duboule D. Gene transpositions in the HoxD complex reveal a hierarchy of regulatory controls. Cell 1996, 85:1025-1035.
34. Schorderet P., Lonfat N., Darbellay F., Tschopp P., Gitto S., Soshnikova N., et al. A genetic approach to the recruitment of PRC2 at the HoxD locus. PLoS Genet 2013, 9:e1003951.
35. Rhinn M., Dolle P. Retinoic acid signalling during development. Development 2012, 139:843-858.
36. Gavalas A., Studer M., Lumsden A., Rijli F.M., Krumlauf R., Chambon P. Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 1998, 125:1123-1136.
37. Mazzoni E.O., Mahony S., Peljto M., Patel T., Thornton S.R., McCuine S., et al. Saltatory remodeling of Hox chromatin in response to rostrocaudal patterning signals. Nat Neurosci 2013, 16:1191-1198.
38. Nolte C., Jinks T., Wang X., Martinez Pastor M.T., Krumlauf R. Shadow enhancers flanking the HoxB cluster direct dynamic Hox expression in early heart and endoderm development. Dev Biol 2013, 383:158-173.
39. Packer A.I., Crotty D.A., Elwell V.A., Wolgemuth D.J. Expression of the murine Hoxa4 gene requires both autoregulation and a conserved retinoic acid response element. Development 1998, 125:1991-1998.
40. Oosterveen T., Niederreither K., Dolle P., Chambon P., Meijlink F., Deschamps J. Retinoids regulate the anterior expression boundaries of 5' Hoxb genes in posterior hindbrain. EMBO J 2003, 22:262-269.
41. van den Akker E., Forlani S., Chawengsaksophak K., de Graaff W., Beck F., Meyer B.I., et al. Cdx1 and Cdx2 have overlapping functions in anteroposterior patterning and posterior axis elongation. Development 2002, 129:2181-2193.
42. Bel-Vialar S., Itasaki N., Krumlauf R. Initiating Hox gene expression: in the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. Development 2002, 129:5103-5115.
43. Duboule D. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Dev Suppl 1994, 135-142.
44. Forlani S., Lawson K.A., Deschamps J. Acquisition of Hox codes during gastrulation and axial elongation in the mouse embryo. Development 2003, 130:3807-3819.
45. Iimura T., Pourquie O. Collinear activation of Hoxb genes during gastrulation is linked to mesoderm cell ingression. Nature 2006, 442:568-571.
46. Aulehla A., Wehrle C., Brand-Saberi B., Kemler R., Gossler A., Kanzler B., et al. Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev Cell 2003, 4:395-406.
47. Dubrulle J., McGrew M.J., Pourquie O. FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 2001, 106:219-232.
48. Moreno T.A., Kintner C. Regulation of segmental patterning by retinoic acid signaling during Xenopus somitogenesis. Dev Cell 2004, 6:205-218.
49. Zakany J., Kmita M., Alarcon P., de la Pompa J.L., Duboule D. Localized and transient transcription of Hox genes suggests a link between patterning and the segmentation clock. Cell 2001, 106:207-217.
50. Cordes R., Schuster-Gossler K., Serth K., Gossler A. Specification of vertebral identity is coupled to Notch signalling and the segmentation clock. Development 2004, 131:1221-1233.
51. Schuettengruber B., Cavalli G. Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 2009, 136:3531-3542.
52. Aloia L., Di Stefano B., Di Croce L. Polycomb complexes in stem cells and embryonic development. Development 2013, 140:2525-2534.
53. Boyer L.A., Plath K., Zeitlinger J., Brambrink T., Medeiros L.A., Lee T.I., et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006, 441:349-353.
54. Lee T.I., Jenner R.G., Boyer L.A., Guenther M.G., Levine S.S., Kumar R.M., et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006, 125:301-313.
55. Noordermeer D., Leleu M., Splinter E., Rougemont J., De Laat W., Duboule D. The dynamic architecture of Hox gene clusters. Science 2011, 334:222-225.
56. Simon J., Chiang A., Bender W. Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products. Development 1992, 114:493-505.
57. Cao R., Wang L., Wang H., Xia L., Erdjument-Bromage H., Tempst P., et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002, 298:1039-1043.
58. Endoh M., Endo T.A., Endoh T., Isono K., Sharif J., Ohara O., et al. Histone H2A mono-ubiquitination is a crucial step to mediate PRC1-dependent repression of developmental genes to maintain ES cell identity. PLoS Genet 2012, 8:e1002774.
59. de Napoles M., Mermoud J.E., Wakao R., Tang Y.A., Endoh M., Appanah R., et al. Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev Cell 2004, 7:663-676.
60. Stock J.K., Giadrossi S., Casanova M., Brookes E., Vidal M., Koseki H., et al. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat Cell Biol 2007, 9:1428-1435.
61. Wang H., Wang L., Erdjument-Bromage H., Vidal M., Tempst P., Jones R.S., et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004, 431:873-878.
62. Eskeland R., Leeb M., Grimes G.R., Kress C., Boyle S., Sproul D., et al. Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. Mol Cell 2010, 38:452-464.
63. Bernstein B.E., Humphrey E.L., Erlich R.L., Schneider R., Bouman P., Liu J.S., et al. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc Natl Acad Sci U S A 2002, 99:8695-8700.
64. Santos-Rosa H., Schneider R., Bannister A.J., Sherriff J., Bernstein B.E., Emre N.C., et al. Active genes are tri-methylated at K4 of histone H3. Nature 2002, 419:407-411.
65. Woo C.J., Kharchenko P.V., Daheron L., Park P.J., Kingston R.E. A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 2010, 140:99-110.
66. Ku M., Koche R.P., Rheinbay E., Mendenhall E.M., Endoh M., Mikkelsen T.S., et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 2008, 4:e1000242.
67. Lynch M.D., Smith A.J., De Gobbi M., Flenley M., Hughes J.R., Vernimmen D., et al. An interspecies analysis reveals a key role for unmethylated CpG dinucleotides in vertebrate Polycomb complex recruitment. EMBO J 2012, 31:317-329.
68. Mendenhall E.M., Koche R.P., Truong T., Zhou V.W., Issac B., Chi A.S., et al. GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet 2010, 6:e1001244.
69. Kim H., Kang K., Kim J. AEBP2 as a potential targeting protein for Polycomb Repression Complex PRC2. Nucleic Acids Res 2009, 37:2940-2950.
70. Peng J.C., Valouev A., Swigut T., Zhang J., Zhao Y., Sidow A., et al. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 2009, 139:1290-1302.
71. Shen X., Kim W., Fujiwara Y., Simon M.D., Liu Y., Mysliwiec M.R., et al. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 2009, 139:1303-1314.
72. Kanhere A., Viiri K., Araujo C.C., Rasaiyaah J., Bouwman R.D., Whyte W.A., et al. Short RNAs are transcribed from repressed polycomb target genes and interact with polycomb repressive complex-2. Mol Cell 2010, 38:675-688.
73. Rinn J.L., Kertesz M., Wang J.K., Squazzo S.L., Xu X., Brugmann S.A., et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129:1311-1323.
74. Zhao J., Sun B.K., Erwin J.A., Song J.J., Lee J.T. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 2008, 322:750-756.
75. Kaneko S., Bonasio R., Saldana-Meyer R., Yoshida T., Son J., Nishino K., et al. Interactions between JARID2 and noncoding RNAs regulate PRC2 recruitment to chromatin. Mol Cell 2014, 53:290-300.
76. Rinn J.L., Chang H.Y. Genome regulation by long noncoding RNAs. Annu Rev Biochem 2012, 81:145-166.
77. Tsai M.C., Manor O., Wan Y., Mosammaparast N., Wang J.K., Lan F., et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science 2010, 329:689-693.
78. Davidovich C., Zheng L., Goodrich K.J., Cech T.R. Promiscuous RNA binding by Polycomb repressive complex 2. Nat Struct Mol Biol 2013, 20:1250-1257.
79. Schorderet P., Duboule D. Structural and functional differences in the long non-coding RNA hotair in mouse and human. PLoS Genet 2011, 7:e1002071.
80. Li L., Liu B., Wapinski O.L., Tsai M.C., Qu K., Zhang J., et al. Targeted disruption of Hotair leads to homeotic transformation and gene derepression. Cell Rep 2013, 5:3-12.
81. Chambeyron S., Bickmore W.A. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev 2004, 18:1119-1130.
82. Chambeyron S., Da Silva N.R., Lawson K.A., Bickmore W.A. Nuclear re-organisation of the Hoxb complex during mouse embryonic development. Development 2005, 132:2215-2223.
83. de Laat W., Dekker J. 3C-based technologies to study the shape of the genome. Methods 2012, 58:189-191.
84. Ferraiuolo M.A., Rousseau M., Miyamoto C., Shenker S., Wang X.Q., Nadler M., et al. The three-dimensional architecture of Hox cluster silencing. Nucleic Acids Res 2010, 38:7472-7484.
85. Wang K.C., Yang Y.W., Liu B., Sanyal A., Corces-Zimmerman R., Chen Y., et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 2011, 472:120-124.
86. Fraser J., Rousseau M., Shenker S., Ferraiuolo M.A., Hayashizaki Y., Blanchette M., et al. Chromatin conformation signatures of cellular differentiation. Genome Biol 2009, 10:R37.
87. Andrey G., Montavon T., Mascrez B., Gonzalez F., Noordermeer D., Leleu M., et al. A switch between topological domains underlies HoxD genes collinearity in mouse limbs. Science 2013, 340:1234167.
88. Delpretti S., Montavon T., Leleu M., Joye E., Tzika A., Milinkovitch M., et al. Multiple enhancers regulate Hoxd genes and the Hotdog LncRNA during cecum budding. Cell Rep 2013, 5:137-150.
89. Noordermeer D., Leleu M., Schorderet P., Joye E., Chabaud F., Duboule D. Temporal dynamics and developmental memory of 3D chromatin architecture at Hox gene loci. eLife 2014, 10.7554/eLife.02557.
90. Grau D.J., Chapman B.A., Garlick J.D., Borowsky M., Francis N.J., Kingston R.E. Compaction of chromatin by diverse Polycomb group proteins requires localized regions of high charge. Genes Dev 2011, 25:2210-2221.
91. Bantignies F., Roure V., Comet I., Leblanc B., Schuettengruber B., Bonnet J., et al. Polycomb-dependent regulatory contacts between distant Hox loci in Drosophila. Cell 2011, 144:214-226.
92. 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.
93. Berlivet S., Paquette D., Dumouchel A., Langlais D., Dostie J., Kmita M. Clustering of tissue-specific sub-TADs accompanies the regulation of HoxA genes in developing limbs. PLoS Genet 2013, 9:e1004018.
94. Tarchini B., Duboule D. Control of Hoxd genes' collinearity during early limb development. Dev Cell 2006, 10:93-103.
95. Nelson C.E., Morgan B.A., Burke A.C., Laufer E., DiMambro E., Murtaugh L.C., et al. Analysis of Hox gene expression in the chick limb bud. Development 1996, 122:1449-1466.
96. Nora E.P., Lajoie B.R., Schulz E.G., Giorgetti L., Okamoto I., Servant N., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
97. Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
98. Haramis A.G., Brown J.M., Zeller R. The limb deformity mutation disrupts the SHH/FGF-4 feedback loop and regulation of 5' HoxD genes during limb pattern formation. Development 1995, 121:4237-4245.
99. Laufer E., Nelson C.E., Johnson R.L., Morgan B.A., Tabin C. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 1994, 79:993-1003.
100. Holland P.W. Evolution of homeobox genes. Wiley Interdiscip Rev Dev Biol 2013, 2:31-45.
101. Burke A.C., Nelson C.E., Morgan B.A., Tabin C. Hox genes and the evolution of vertebrate axial morphology. Development 1995, 121:333-346.
102. Gaunt S.J. Conservation in the Hox code during morphological evolution. Int J Dev Biol 1994, 38:549-552.
103. Gomez C., Ozbudak E.M., Wunderlich J., Baumann D., Lewis J., Pourquie O. Control of segment number in vertebrate embryos. Nature 2008, 454:335-339.
104. Di-Poi N., Montoya-Burgos J.I., Miller H., Pourquie O., Milinkovitch M.C., Duboule D. Changes in Hox genes' structure and function during the evolution of the squamate body plan. Nature 2010, 464:99-103.
105. Woltering J.M., Vonk F.J., Muller H., Bardine N., Tuduce I.L., de Bakker M.A., et al. Axial patterning in snakes and caecilians: evidence for an alternative interpretation of the Hox code. Dev Biol 2009, 332:82-89.
106. Voss S.R., Putta S., Walker J.A., Smith J.J., Maki N., Tsonis P.A. Salamander Hox clusters contain repetitive DNA and expanded non-coding regions: a typical Hox structure for non-mammalian tetrapod vertebrates?. Hum Genomics 2013, 7:9.
107. Di-Poi N., Montoya-Burgos J.I., Duboule D. Atypical relaxation of structural constraints in Hox gene clusters of the green anole lizard. Genome Res 2009, 19:602-610.
108. Karimi M.M., Goyal P., Maksakova I.A., Bilenky M., Leung D., Tang J.X., et al. DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 2011, 8:676-687.
109. Rebollo R., Karimi M.M., Bilenky M., Gagnier L., Miceli-Royer K., Zhang Y., et al. Retrotransposon-induced heterochromatin spreading in the mouse revealed by insertional polymorphisms. PLoS Genet 2011, 7:e1002301.
110. Sordino P., van der Hoeven F., Duboule D. Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 1995, 375:678-681.
111. Woltering J.M., Duboule D. The origin of digits: expression patterns versus regulatory mechanisms. Dev Cell 2010, 18:526-532.
112. Schneider I., Shubin N.H. The origin of the tetrapod limb: from expeditions to enhancers. Trends Genet 2013, 29:419-426.
113. Woltering J.M., Noordermeer D., Leleu M., Duboule D. Conservation and divergence of regulatory strategies at Hox Loci and the origin of tetrapod digits. PLoS Biol 2014, 12:e1001773.
114. Schneider I., Aneas I., Gehrke A.R., Dahn R.D., Nobrega M.A., Shubin N.H. Appendage expression driven by the Hoxd Global Control Region is an ancient gnathostome feature. Proc Natl Acad Sci U S A 2011, 108:12782-12786.
115. Amemiya C.T., Alfoldi J., Lee A.P., Fan S., Philippe H., Maccallum I., et al. The African coelacanth genome provides insights into tetrapod evolution. Nature 2013, 496:311-316.
116. Zakany J., Kmita M., Duboule D. A dual role for Hox genes in limb anterior-posterior asymmetry. Science 2004, 304:1669-1672.
117. Ahn Y., Mullan H.E., Krumlauf R. Long-range regulation by shared retinoic acid response elements modulates dynamic expression of posterior Hoxb genes in CNS development. Dev Biol 2014, 388:134-144.