Genomic Approaches to Understanding Hox Gene Function

Advances in Genetics

Volumn 76, Issue , 2011, Pages 55-91

  Choo, Siew Woh ^a,b   Russell, Steven ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

DNA; Drosophila; Genomics; Hox; Ultrabithorax

Indexed keywords

EID: 81455132498     PISSN: 00652660     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386481-9.00003-1     Document Type: Chapter

References (163)

1. Abbott M.K., Kaufman T.C. The relationship between the functional complexity and the molecular organization of the Antennapedia locus of Drosophila melanogaster. Genetics 1986, 114:919-942.
2. Aboobaker A., Blaxter M. Hox gene evolution in nematodes: Novelty conserved. Curr. Opin. Genet. Dev. 2003, 13:593-598.
3. Abzhanov A., Kaufman T.C. Homeotic genes and the arthropod head: Expression patterns of the labial, proboscipedia, and Deformed genes in crustaceans and insects. Proc. Natl. Acad. Sci. USA 1999, 96:10224-10229.
4. Akam M. Hox genes: From master genes to micromanagers. Curr. Biol. 1998, 8:R676-R678.
5. Aleksic J., Russell S. ChIPing away at the genome: The new frontier travel guide. Mol. Biosyst. 2009, 5:1421-1428.
6. Appel B., Sakonju S. Cell-type specific mechanisms of transcriptional repression by the homeotic gene products UBX and ABD-A in Drosophila embryos. EMBO J. 1993, 12:1099-1109.
7. Balazsi G., van Oudenaarden A., Collins J.J. Cellular decision making and biological noise: From microbes to mammals. Cell 2011, 144:910-925.
8. Bateson M.A.W. Materials for the Study of Variation Treated With Especial Regard to Discontinuity in the Origin of Species 1894, McMillan & Co, London.
9. Beachy P.A., Krasnow M.A., Gavis E.R., Hogness D.M. An Ultrabithorax protein binds near its own and Antennapedia P1 promoters. Cell 1988, 55:1069-1081.
10. Bender W., Akam M., Karch F., Beachy P.A., Peifer M., Spierer P., Lewis E.B., Hogness D.S. Molecular genetics of the bithorax complex in Drosophila melanogaster. Science 1983, 221:23-29.
11. Berman B.P., Nibu Y., Pfeiffer B.D., Tomancak P., Celniker S.E., Levine M., Rubin G.M., Eisen M.B. Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc. Natl. Acad. Sci. USA 2002, 99:757-762.
12. Bier E., Vaessin H., Shepherd S., Lee K., McCall K., Barbel S., Ackerman A., Carretto R., Uemura T., Grell E., et al. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 1989, 3:1273-1287.
13. Bridges C.B., Morgan T.H. The third-chromosome group of mutant characters of Drosophila melanogaster 1923, 327:1-251. Carnegie Institution of Washington, Washington, DC.
14. Capovilla M., Botas J. Functional dominance among Hox genes: Repression dominates activation in the regulation of Dpp. Development 1998, 125:4949-4957.
15. Capovilla M., Brandt M., Botas J. Direct regulation of decapentaplegic by Ultrabithorax and its role in Drosophila midgut morphogenesis. Cell 1994, 76:461-475.
16. Capovilla M., Kambris Z., Botas J. Direct regulation of the muscle-identity gene apterous by a Hox protein in the somatic mesoderm. Development 2001, 128:1221-1230.
17. Carroll S.B. Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom 2005, W.W. Norton & Co, New York.
18. Carroll S.B. Evo-devo and an expanding evolutionary synthesis: A genetic theory of morphological evolution. Cell 2008, 134:25-36.
19. Casares F., Calleja M., Sanchez-Herrero E. Functional similarity in appendage specification by the Ultrabithorax and abdominal-A Drosophila HOX genes. EMBO J. 1996, 15:3934-3942.
20. Catron K.M., Iler N., Abate C. Nucleotides flanking a conserved TAAT core dictate the DNA binding specificity of three murine homeodomain proteins. Mol. Cell. Biol. 1993, 13:2354-2365.
21. Chauvet S., Maurel-Zaffran C., Miassod R., Jullien N., Pradel J., Aragnol D. dlarp, a new candidate Hox target in Drosophila whose orthologue in mouse is expressed at sites of epithelium/mesenchymal interactions. Dev. Dyn. 2000, 218:401-413.
22. Choo S.W., White R., Russell S. Genome-wide analysis of the binding of the Hox protein Ultrabithorax and the Hox cofactor Homothorax in Drosophila. PLoS One 2011, 6:e14778.
23. Cobb J., Duboule D. Comparative analysis of genes downstream of the Hoxd cluster in developing digits and external genitalia. Development 2005, 132:3055-3067.
24. Costello J.C., Dalkilic M.M., Beason S.M., Gehlhausen J.R., Patwardhan R., Middha S., Eads B.D., Andrews J.R. Gene networks in Drosophila melanogaster: Integrating experimental data to predict gene function. Genome Biol. 2009, 10:R97.
25. Deutsch J.S. Segments and parasegments in arthropods: A functional perspective. Bioessays 2004, 26:1117-1125.
26. Duboule D. Guide to the Homeobox Genes 1994, Oxford University Press, Oxford.
27. Duboule D. Vertebrate hox gene regulation: Clustering and/or colinearity?. Curr. Opin. Genet. Dev. 1998, 8:514-518.
28. Duncan I. The bithorax complex. Annu. Rev. Genet. 1987, 21:285-319.
29. Ebner A., Cabernard C., Affolter M., Merabet S. Recognition of distinct target sites by a unique Labial/Extradenticle/Homothorax complex. Development 2005, 132:1591-1600.
30. Ekker S.C., Young K.E., Von Kessler D.P., Beachy P.A. Optimal DNA sequence recognition by the Ultrabithorax homeodomain of Drosophila. EMBO J. 1991, 10:1179-1186.
31. Erives A., Levine M. Coordinate enhancers share common organizational features in the Drosophila genome. Proc. Natl. Acad. Sci. USA 2004, 101:3851-3856.
32. Estrada B., Choe S.E., Gisselbrecht S.S., Michaud S., Raj L., Busser B.W., Halfon M.S., Church G.M., Michelson A.M. An integrated strategy for analyzing the unique developmental programs of different myoblast subtypes. PLoS Genet. 2006, 2:e16.
33. Euskirchen G.M., Rozowsky J.S., Wei C.L., Lee W.H., Zhang Z.D., Hartman S., Emanuelsson O., Stolc V., Weissman S., Gerstein M.B., et al. Mapping of transcription factor binding regions in mammalian cells by ChIP: Comparison of array- and sequencing-based technologies. Genome Res. 2007, 17:898-909.
34. Feinstein P.G., Kornfeld K., Hogness D.S., Mann R.S. Identification of homeotic target genes in Drosophila melanogaster including nervy, a proto-oncogene homologue. Genetics 1995, 140:573-586.
35. Ferrell C.M., Dorsam S.T., Ohta H., Humphries R.K., Derynck M.K., Haqq C., Largman C., Lawrence H.J. Activation of stem-cell specific genes by HOXA9 and HOXA10 homeodomain proteins in CD34+ human cord blood cells. Stem Cells 2005, 23:644-655.
36. Ferretti E., Marshall H., Popperl H., Maconochie M., Krumlauf R., Blasi F. Segmental expression of Hoxb2 in r4 requires two separate sites that integrate cooperative interactions between Prep1, Pbx and Hox proteins. Development 2000, 127:155-166.
37. Galant R., Walsh C.M., Carroll S.B. Hox repression of a target gene: Extradenticle-independent, additive action through multiple monomer binding sites. Development 2002, 129:3115-3126.
38. Garber R.L., Kuroiwa A., Gehring W.J. Genomic and cDNA clones of the homeotic locus Antennapedia in Drosophila. EMBO J. 1983, 2:2027-2036.
39. Garcia-Bellido A. Genetic control of wing disc development in Drosophila. Ciba Found. Symp. 1975, 29:161-182.
40. Garcia-Fernandez J. The genesis and evolution of homeobox gene clusters. Nat. Rev. Genet. 2005, 6:881-892.
41. Garcia-Fernandez J., Holland P.W. Archetypal organization of the amphioxus Hox gene cluster. Nature 1994, 370:563-566.
42. Gebelein B., Culi J., Ryoo H.D., Zhang W., Mann R.S. Specificity of Distalless repression and limb primordia development by abdominal Hox proteins. Dev. Cell 2002, 3:487-498.
43. Gebelein B., McKay D.J., Mann R.S. Direct integration of Hox and segmentation gene inputs during Drosophila development. Nature 2004, 431:653-659.
44. Gehring W.J., Hiromi Y. Homeotic genes and the homeobox. Annu. Rev. Genet. 1986, 20:147-173.
45. Gehring W.J., Kloter U., Suga H. Evolution of the Hox gene complex from an evolutionary ground state. Curr. Top. Dev. Biol. 2009, 88:35-61.
46. Gerstein M.B., Lu Z.J., Van Nostrand E.L., Cheng C., Arshinoff B.I., Liu T., Yip K.Y., Robilotto R., Rechtsteiner A., Ikegami K., et al. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 2010, 330:1775-1787.
47. Gould A.P., White R.A. Connectin, a target of homeotic gene control in Drosophila. Development 1992, 116:1163-1174.
48. Graba Y., Aragnol D., Laurenti P., Garzino V., Charmot D., Berenger H., Pradel J. Homeotic control in Drosophila; the scabrous gene is an in vivo target of Ultrabithorax proteins. EMBO J. 1992, 11:3375-3384.
49. Graba Y., Gieseler K., Aragnol D., Laurenti P., Mariol M.-C., Berenger H., Sagnier T., Pradel J. DWnt-4, a novel Drosophila Wnt gene acts downstream of homeotic complex genes in the visceral mesoderm. Development 1995, 121:209-218.
50. Graba Y., Aragnol D., Pradel J. Drosophila Hox complex downstream targets and the function of homeotic genes. Bioessays 1997, 19:379-388.
51. Grieder N.C., Marty T., Ryoo H.D., Mann R.S., Affolter M. Synergistic activation of a Drosophila enhancer by HOM/EXD and DPP signaling. EMBO J. 1997, 16:7402-7410.
52. Grienenberger A., Merabet S., Manak J., Iltis I., Fabre A., Berenger H., Scott M.P., Pradel J., Graba Y. Tgf-beta signaling acts on a Hox response element to confer specificity and diversity to Hox protein function. Development 2003, 130:5445-5455.
53. Grier D.G., Thompson A., Kwasniewska A., McGonigle G.J., Halliday H.L., Lappin T.R. The pathophysiology of HOX genes and their role in cancer. J. Pathol. 2005, 205:154-171.
54. Hakim O., Sung M.H., Hager G.L. 3D shortcuts to gene regulation. Curr. Opin. Cell Biol. 2010, 22:305-313.
55. Hedlund E., Karsten S.L., Kudo L., Geschwind D.H., Carpenter E.M. Identification of a Hoxd10-regulated transcriptional network and combinatorial interactions with Hoxa10 during spinal cord development. J. Neurosci. Res. 2004, 75:307-319.
56. Hersh B.M., Carroll S.B. Direct regulation of knot gene expression by Ultrabithorax and the evolution of cis-regulatory elements in Drosophila. Development 2005, 132:1567-1577.
57. Hersh B.M., Nelson C.E., Stoll S.J., Norton J.E., Albert T.J., Carroll S.B. The UBX-regulated network in the haltere imaginal disc of D. melanogaster. Dev. Biol. 2007, 302:717-727.
58. Heuer J.G., Li K., Kaufman T.C. The Drosophila homeotic target gene centrosomin (cnn) encodes a novel centrosomal protein with leucine zippers and maps to a genomic region required for midgut morphogenesis. Development 1995, 121:3861-3876.
59. Hinz U., Wolk A., Renkawitz-Pohl R. Ultrabithorax is a regulator of β3 tubulin expression in the Drosophila visceral mesoderm. Development 1992, 116:543-554.
60. Ho J.W., Bishop E., Karchenko P.V., Negre N., White K.P., Park P.J. ChIP-chip versus ChIP-seq: Lessons for experimental design and data analysis. BMC Genomics 2011, 12:134.
61. Hoegg S., Boore J.L., Kuehl J.V., Meyer A. Comparative phylogenomic analyses of teleost fish Hox gene clusters: Lessons from the cichlid fish Astatotilapia burtoni. BMC Genomics 2007, 8:317.
62. Hueber S.D., Lohmann I. Shaping segments: Hox gene function in the genomic age. Bioessays 2008, 30:965-979.
63. Hueber S.D., Bezdan D., Henz S.R., Blank M., Wu H., Lohmann I. Comparative analysis of Hox downstream genes in Drosophila. Development 2007, 134:381-392.
64. Jacobs Y., Schnabel C.A., Cleary M.L. Trimeric association of hox and TALE homeodomain proteins mediates Hoxb2 hindbrain enhancer activity. Mol. Cell. Biol. 1999, 19:5134-5142.
65. Johnson D.S., Mortazavi A., Myers R.M., Wold B. Genome-wide mapping of in vivo protein-DNA interactions. Science 2007, 316:1497-1502.
66. Joshi R., Sun L., Mann R. Dissecting the functional specificities of two Hox proteins. Genes Dev. 2010, 24:1533-1545.
67. Kaplan T., Li X.Y., Sabo P.J., Thomas S., Stamatoyannopoulos J.A., Biggin M.D., Eisen M.B. Quantitative models of the mechanisms that control genome-wide patterns of transcription factor binding during early Drosophila development. PLoS Genet. 2011, 7:e1001290.
68. Kaufman T.C., Lewis R., Wakimoto B. Cytogenetic analysis of chromosome 3 in Drosophila melanogaster: The homoeotic gene complex in polytene chromosome interval 84a-B. Genetics 1980, 94:115-133.
69. Kel A., Konovalova T., Waleev T., Cheremushkin E., Kel-Margoulis O., Wingender E. Composite module analyst: A fitness-based tool for identification of transcription factor binding site combinations. Bioinformatics 2006, 22:1190-1197.
70. Kwong C., Adryan B., Bell I., Meadows L., Russell S., Manak J.R., White R. Stability and dynamics of polycomb target sites in Drosophila development. PLoS Genet. 2008, 4:e1000178.
71. Lappin T.R., Grier D.G., Thompson A., Halliday H.L. HOX genes: Seductive science, mysterious mechanisms. Ulster Med. J. 2006, 75:23-31.
72. Lawrence P.A. The Making of a Fly: The Genetics of Animal Design 1992, Wiley-Blackwell, Oxford.
73. Le Gac S., van den Berg A. Single cells as experimentation units in lab-on-a-chip devices. Trends Biotechnol. 2010, 28:55-62.
74. Leemans R., Loop T., Egger B., He H., Kammermeier L., Hartmann B., Certa U., Reichert H., Hirth F. Identification of candidate downstream genes for the homeodomain transcription factor Labial in Drosophila through oligonucleotide-array transcript imaging. Genome Biol. 2001, 2.: RESEARCH0015.
75. Lei H., Wang H., Juan A.H., Ruddle F.H. The identification of Hoxc8 target genes. Proc. Natl. Acad. Sci. USA 2005, 102:2420-2424.
76. Lewis E.B. A gene complex controlling segmentation in Drosophila. Nature 1978, 276:565-570.
77. Lewis E.B. Homeosis: The first 100 years. Trends Genet. 1994, 10:341-343.
78. Li K., Kaufman T.C. The homeotic target gene centrosomin encodes an essential centrosomal component. Cell 1996, 85:585-596.
79. Li X.Y., MacArthur S., Bourgon R., Nix D., Pollard D.A., Iyer V.N., Hechmer A., Simirenko L., Stapleton M., Luengo Hendriks C.L., et al. Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol. 2008, 6:e27.
80. Li X.Y., Thomas S., Sabo P.J., Eisen M.B., Stamatoyannopoulos J.A., Biggin M.D. The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding. Genome Biol. 2011, 12:R34.
81. Lohmann I. Hox genes: Realising the importance of realisators. Curr. Biol. 2006, 16:R988-R989.
82. Lohmann I., McGinnis N., Bodmer M., McGinnis W. The Drosophila Hox gene deformed sculpts head morphology via direct regulation of the apoptosis activator reaper. Cell 2002, 110:457-466.
83. Lovegrove B., Simoes S., Rivas M.L., Sotillos S., Johnson K., Knust E., Jacinto A., Hombria J.C. Coordinated control of cell adhesion, polarity, and cytoskeleton underlies Hox-induced organogenesis in Drosophila. Curr. Biol. 2006, 16:2206-2216.
84. MacArthur S., Li X.Y., Li J., Brown J.B., Chu H.C., Zeng L., Grondona B.P., Hechmer A., Simirenko L., Keranen S.V., et al. Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions. Genome Biol. 2009, 10:R80.
85. MacQuarrie K.L., Fong A.P., Morse R.H., Tapscott S.J. Genome-wide transcription factor binding: Beyond direct target regulation. Trends Genet. 2011, 27:141-148.
86. Maeda R.K., Karch F. The ABC of the BX-C: The bithorax complex explained. Development 2006, 133:1413-1422.
87. Maeda R.K., Karch F. The Bithorax complex of Drosophila: An exceptional Hox cluster. Curr. Top. Dev. Biol. 2009, 88:1-33.
88. Mallo M., Wellik D.M., Deschamps J. Hox genes and regional patterning of the vertebrate body plan. Dev. Biol. 2010, 344:7-15.
89. Mann R.S. The specificity of homeotic gene function. Bioessays 1995, 17:855-893.
90. Mann R.S. Why are Hox genes clustered?. Bioessays 1997, 19:661-664.
91. Markstein M., Zinzen R., Markstein P., Yee K.P., Erives A., Stathopoulos A., Levine M. A regulatory code for neurogenic gene expression in the Drosophila embryo. Development 2004, 131:2387-2394.
92. Martinez-Ceballos E., Chambon P., Gudas L.J. Differences in gene expression between wild type and Hoxa1 knockout embryonic stem cells after retinoic acid treatment or leukemia inhibitory factor (LIF) removal. J. Biol. Chem. 2005, 280:16484-16498.
93. Mastick G.S., McKay R., Oligino T., Donovan K., Lopez A.J. Identification of target genes regulated by homeotic proteins in Drosophila melanogaster through genetic selection of Ultrabithorax protein-binding sites in yeast. Genetics 1995, 139:349-363.
94. Mattick J.S., Taft R.J., Faulkner G.J. A global view of genomic information-Moving beyond the gene and the master regulator. Trends Genet. 2009, 26:21-28.
95. McCabe C.D., Innis J.W. A genomic approach to the identification and characterization of HOXA13 functional binding elements. Nucleic Acids Res. 2005, 33:6782-6794.
96. McCormick A., Core N., Kerridge S., Scott M.P. Homeotic response elements are tightly linked to tissue-specific elements in a transcriptional enhancer of the teashirt gene. Development 1995, 121:2799-2812.
97. McGinnis W. A century of homeosis, a decade of homeoboxes. Genetics 1994, 137:607-611.
98. McGinnis W., Krumlauf R. Homeobox genes and axial patterning. Cell 1992, 68:283-302.
99. McGinnis W., Levine M.S., Hafen E., Kuroiwa A., Gehring W.J. A conserved DNA sequence in homoeotic genes of the Drosophila Antennapedia and bithorax complexes. Nature 1984, 308:428-433.
100. Merabet S., Saadaoui M., Sambrani N., Hudry B., Pradel J., Affolter M., Graba Y. A unique Extradenticle recruitment mode in the Drosophila Hox protein Ultrabithorax. Proc. Natl. Acad. Sci. USA 2007, 104:16946-16951.
101. Merabet S., Hudry B., Saadaoui M., Graba Y. Classification of sequence signatures: A guide to Hox protein function. Bioessays 2009, 31:500-511.
102. Miller D.F., Rogers B.T., Kalkbrenner A., Hamilton B., Holtzman S.L., Kaufman T. Cross-regulation of Hox genes in the Drosophila melanogaster embryo. Mech. Dev. 2001, 102:3-16.
103. Miller M.R., Robinson K.J., Cleary M.D., Doe C.Q. TU-tagging: Cell type-specific RNA isolation from intact complex tissues. Nat. Methods 2009, 6:439-441.
104. Mohit P., Makhijani K., Madhavi M.B., Bharathi V., Lal A., Sirdesai G., Reddy V.R., Ramesh P., Kannan R., Dhawan J., et al. Modulation of AP and DV signaling pathways by the homeotic gene Ultrabithorax during haltere development in Drosophila. Dev. Biol. 2006, 291:356-367.
105. Negre B., Ruiz A. HOM-C evolution in Drosophila: Is there a need for Hox gene clustering?. Trends Genet. 2007, 23:55-59.
106. Negre N., Brown C.D., Ma L., Bristow C.A., Miller S.W., Wagner U., Kheradpour P., Eaton M.L., Loriaux P., Sealfon R., et al. A cis-regulatory map of the Drosophila genome. Nature 2011, 471:527-531.
107. Niu W., Lu Z.J., Zhong M., Sarov M., Murray J.I., Brdlik C.M., Janette J., Chen C., Alves P., Preston E., et al. Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Res. 2010, 21:245-254.
108. Nojima H., Tougan T. Preparation of a high-quality cDNA library from a single-cell quantity of mRNA using chum-RNA. Methods Mol. Biol. 2011, 729:15-35.
109. Noyes M.B., Christensen R.G., Wakabayashi A., Stormo G.D., Brodsky M.H., Wolfe S.A. Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 2008, 133:1277-1289.
110. Oates A.C. What's all the noise about developmental stochasticity?. Development 2011, 138:601-607.
111. O'Kane C.J., Gehring W.J. Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl. Acad. Sci. USA 1987, 84:9123-9127.
112. Osborne C.S., Ewels P.A., Young A.N. Meet the neighbours: Tools to dissect nuclear structure and function. Brief. Funct. Genomics 2011, 10:11-17.
113. Pavlopoulos A., Akam M. Hox go omics: Insights from Drosophila into Hox gene targets. Genome Biol. 2007, 8:208.
114. Pavlopoulos A., Akam M. Hox gene Ultrabithorax regulates distinct sets of target genes at successive stages of Drosophila haltere morphogenesis. Proc. Natl. Acad. Sci. USA 2011, 108:2855-2860.
115. Pederson J.A., LaFollette J.W., Gross C., Veraksa A., McGinnis W., Mahaffey J.W. Regulation by homeoproteins: A comparison of deformed-responsive elements. Genetics 2000, 156:677-686.
116. Pellerin I., Schnabel C., Catron K.M., Abate C. Hox proteins have different affinities for a consensus DNA site that correlate with the positions of their genes on the hox cluster. Mol. Cell. Biol. 1994, 14:4532-4545.
117. Potter C.S., Pruett N.D., Kern M.J., Baybo M.A., Godwin A.R., Potter K.A., Peterson R.L., Sundberg J.P., Awgulewitsch A. The nude mutant gene Foxn1 is a HOXC13 regulatory target during hair follicle and nail differentiation. J. Invest. Dermatol. 2011, 131:828-837.
118. Pradel J., White R.A.H. From selectors to realizators. Int. J. Dev. Biol. 1998, 42:417-421.
119. Rajewsky N., Vergassola M., Gaul U., Siggia E.D. Computational detection of genomic cis-regulatory modules applied to body patterning in the early Drosophila embryo. BMC Bioinformatics 2002, 3:30.
120. Rees J.S., Lowe N., Armean I.M., Roote J., Johnson G., Drummond E., Spriggs H., Ryder E., Russell S., St Johnston D., Lilley K.S. In vivo analysis of proteomes and interactomes using parallel affinity capture (iPAC) coupled to mass spectrometry. Mol. Cell. Proteomics 2011, 10. M110.002386.
121. Robertson G., Hirst M., Bainbridge M., Bilenky M., Zhao Y., Zeng T., Euskirchen G., Bernier B., Varhol R., Delaney A., et al. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat. Methods 2007, 4:651-657.
122. Roch F., Akam M. Ultrabithorax and the control of cell morphology in Drosophila halteres. Development 2000, 127:97-107.
123. Rohrschneider M.R., Elsen G.E., Prince V.E. Zebrafish Hoxb1a regulates multiple downstream genes including prickle1b. Dev. Biol. 2007, 309:358-372.
124. Roy S., Ernst J., Kharchenko P.V., Kheradpour P., Negre N., Eaton M.L., Landolin J.M., Bristow C.A., Ma L., Lin M.F., et al. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 2010, 330:1787-1797.
125. Ryder E., Spriggs H., Drummond E., St Johnston D., Russell S. The Flannotator-A gene and protein expression annotation tool for Drosophila melanogaster. Bioinformatics 2009, 25:548-549.
126. Ryoo H.D., Mann R.S. The control of trunk Hox specificity and activity by Extradenticle. Genes Dev. 1999, 13:1704-1716.
127. Salsi V., Vigano M.A., Cocchiarella F., Mantovani R., Zappavigna V. Hoxd13 binds in vivo and regulates the expression of genes acting in key pathways for early limb and skeletal patterning. Dev. Biol. 2008, 317:497-507.
128. Schilling T.F., Knight R.D. Origins of anteroposterior patterning and Hox gene regulation during chordate evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2001, 356:1599-1613.
129. Schmid A., Kortmann H., Dittrich P.S., Blank L.M. Chemical and biological single cell analysis. Curr. Opin. Biotechnol. 2010, 21:12-20.
130. Schröder R., Beermann A., Wittkopp N., Lutz R. From development to biodiversity-Tribolium castaneum, an insect model organism for short germband development. Dev. Genes Evol. 2008, 218:116-126.
131. Schwab K., Hartman H.A., Liang H.C., Aronow B.J., Patterson L.T., Potter S.S. Comprehensive microarray analysis of Hoxa11/Hoxd11 mutant kidney development. Dev. Biol. 2006, 293:540-554.
132. Scott M.P. Vertebrate homeobox gene nomenclature. Cell 1992, 71:551-553.
133. Scott M.P., Weiner A.J. Structural relationships among genes that control development: Sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc. Natl. Acad. Sci. USA 1984, 81:4115-4119.
134. Scott M.P., Weiner A.J., Hazelrigg T.I., Polisky B.A., Pirrotta V., Scalenghe F., Kaufman T.C. The molecular organization of the Antennapedia locus of Drosophila. Cell 1983, 35:763-776.
135. Shen J., Wu H., Gudas L.J. Molecular cloning and analysis of a group of genes differentially expressed in cells which overexpress the Hoxa-1 homeobox gene. Exp. Cell Res. 2000, 259:274-283.
136. Singh N.P., Mishra R.K. A double-edged sword to force posterior dominance of Hox genes. Bioessays 2008, 30:1058-1061.
137. Slack J.M. Conrad Hal Waddington: The last Renaissance biologist?. Nat. Rev. Genet. 2002, 3:889-895.
138. Slattery M., Négre N., Ma L.M., White K.P., Mann R.S. Genome-wide tissue-specific occupancy of the Hox protein ultrabithorax and Hox cofactor Homothorax in Drosophila. PLoS One 2011, 6:e14686.
139. Stobe P., Stein M.A., Habring-Muller A., Bezdan D., Fuchs A.L., Hueber S.D., Wu H., Lohmann I. Multifactorial regulation of a hox target gene. PLoS Genet. 2009, 5:e1000412.
140. Strutt D.I., White R.A. Characterisation of T48, a target of homeotic gene regulation in Drosophila embryogenesis. Mech. Dev. 1994, 46:27-39.
141. Stuart J.J., Brown S.J., Beeman R.W., Denell R.E. A deficiency of the homeotic complex of the beetle Tribolium. Nature 1991, 350:72-74.
142. Stultz B.G., Jackson D.G., Mortin M.A., Yang X., Beachy P.A., Hursh D.A. Transcriptional activation by Extradenticle in the Drosophila visceral mesoderm. Dev. Biol. 2006, 290:482-494.
143. Su J., Teichmann S.A., Down T.A. Assessing computational methods of cis-regulatory module prediction. PLoS Comput. Biol. 2010, 6:e1001020.
144. Tang F., Lao K., Surani M.A. Development and applications of single-cell transcriptome analysis. Nat. Methods 2011, 8:S6-S11.
145. Tomoyasu Y., Wheeler S.R., Denell R.E. Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 2005, 433:643-647.
146. Tompa M., Li N., Bailey T.L., Church G.M., De Moor B., Eskin E., Favorov A.V., Frith M.C., Fu Y., Kent W.J., et al. Assessing computational tools for the discovery of transcription factor binding sites. Nat. Biotechnol. 2005, 23:137-144.
147. Tour E., Hittinger C.T., McGinnis W. Evolutionarily conserved domains required for activation and repression functions of the Drosophila Hox protein Ultrabithorax. Development 2005, 132:5271-5281.
148. Tumpel S., Wiedemann L.M., Krumlauf R. Hox genes and segmentation of the vertebrate hindbrain. Curr. Top. Dev. Biol. 2009, 88:103-137.
149. Vachon G., Cohen B., Pfeifle C., McGuffin M.E., Botas J., Cohen S.M. Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene Distal-less. Cell 1992, 71:437-450.
150. Valerius M.T., Patterson L.T., Witte D.P., Potter S.S. Microarray analysis of novel cell lines representing two stages of metanephric mesenchyme differentiation. Mech. Dev. 2002, 112:219-232.
151. van den Akker W.M., Durston A.J., Spaink H.P. Identification of hoxb1b downstream genes: hoxb1b as a regulatory factor controlling transcriptional networks and cell movement during zebrafish gastrulation. Int. J. Dev. Biol. 2010, 54:55-62.
152. Waddington C.H. The Strategy of the Genes 1957, Geo Allen & Unwin, London.
153. Walsh C.M., Carroll S.B. Collaboration between Smads and a Hox protein in target gene repression. Development 2007, 134:3585-3592.
154. Walter J., Dever C.A., Biggin M.D. Two homeodomain proteins bind with similar specificity to a wide range of DNA sites in Drosophila embryos. Genes Dev. 1994, 8:1678-1692.
155. Weatherbee S.D., Halder G., Kim J., Hudson A., Carroll S. Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev. 1998, 12:1474-1482.
156. Weatherbee S.D., Nijhout H.F., Grunert L.W., Halder G., Galant R., Selegue J., Carroll S. Ultrabithorax function in butterfly wings and the evolution of insect wing patterns. Curr. Biol. 1999, 9:109-115.
157. Wei C.L., Wu Q., Vega V.B., Chiu K.P., Ng P., Zhang T., Shahab A., Yong H.C., Fu Y., Weng Z., et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 2006, 124:207-219.
158. Wellik D.M. Hox genes and vertebrate axial pattern. Curr. Top. Dev. Biol. 2009, 88:257-278.
159. Williams T.M., Williams M.E., Kuick R., Misek D., McDonagh K., Hanash S., Innis J.W. Candidate downstream regulated genes of HOX group 13 transcription factors with and without monomeric DNA binding capability. Dev. Biol. 2005, 279:462-480.
160. Zakany J., Duboule D. The role of Hox genes during vertebrate limb development. Curr. Opin. Genet. Dev. 2007, 17:359-366.
161. Zeng C., Pinsonneault J., Gellon G., McGinnis N., McGinnis W. Deformed protein binding sites and cofactor binding sites are required for the function of a small segment-specific regulatory element in Drosophila embryos. EMBO J. 1994, 13:2362-2377.
162. Zhang X., Robertson G., Krzywinski M., Ning K., Droit A., Jones S., Gottardo R. PICS: Probabilistic inference for ChIP-seq. Biometrics 2011, 67:151-163.
163. Zhao Y., Potter S.S. Functional specificity of the Hoxa13 homeobox. Development 2001, 128:3197-3207.