Evolution of the HOXB6 intergenic region: Motif conservation at the lateral plate mesoderm (LPM) enhancer element
Amos Deinard
Department of Genetics, Yale University School of Medicine, New Haven, Connecticut 06520
Search for more papers by this authorRobert Dorit
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06511
Search for more papers by this authorCarmela Castiglione
Department of Genetics, Yale University School of Medicine, New Haven, Connecticut 06520
Search for more papers by this authorDiko Becker
Max-Planck-Institut fur Immunobiologie, Freiburg D-79108, Germany
Search for more papers by this authorFrank Ruddle
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06511
Search for more papers by this authorCorresponding Author
Kenneth Kidd
Department of Genetics, Yale University School of Medicine, New Haven, Connecticut 06520
Department of Genetics, Yale University School of Medicine, New Haven, CT 06520===Search for more papers by this authorAmos Deinard
Department of Genetics, Yale University School of Medicine, New Haven, Connecticut 06520
Search for more papers by this authorRobert Dorit
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06511
Search for more papers by this authorCarmela Castiglione
Department of Genetics, Yale University School of Medicine, New Haven, Connecticut 06520
Search for more papers by this authorDiko Becker
Max-Planck-Institut fur Immunobiologie, Freiburg D-79108, Germany
Search for more papers by this authorFrank Ruddle
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06511
Search for more papers by this authorCorresponding Author
Kenneth Kidd
Department of Genetics, Yale University School of Medicine, New Haven, Connecticut 06520
Department of Genetics, Yale University School of Medicine, New Haven, CT 06520===Search for more papers by this authorAbstract
This study reports the results of a comparative sequencing study in higher primates, focusing on the intergenic region located between HOXB6 and HOXB7. We have examined an 832 bp. region, encompassing a putative Lateral Plate Mesoderm (LPM) enhancer element in a variety of anthropoid apes. The interspecific comparisons reveal extensive substitutions occurring within this region, with a marked bias in favor of C→T transitions within the enhancer element. The pattern of these substitutions suggests that the LPM enhancer region is subject to specific sequence and compositional constraints that are only revealed through comparative sequencing. These constraints produce an enhancer signature, the CpG microisland, which may be useful in identifying additional regulatory elements located within the HOX complexes. J. Exp. Zool. (Mol. Dev. Evol.) 285:170–176, 1999. © 1999 Wiley-Liss, Inc.
LITERATURE CITED
- Akam M. 1998. Hox genes in arthropod development and evolution. Biol Bull 195: 373–374.Medline
- Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH. 1998. Zebrafish hox clusters and vertebrate genome evolution. Science 282: 1711–1714.Medline
- Bailey W, Kim J, Wagner G, Ruddle F. 1997. Phylogenetic reconstruction of vertebrate Hox cluster duplications. Mol Biol Evol 14: 843–853.Medline
- Becker D, Jiang Z, Knudler P, Deinard AS, Eid R, Kidd KK, Shashikant CS, Ruddle FH, Schughart K. 1996. A highly conserved regulatory element is involved in the early onset of Hoxb-6 gene expression. Dev Dynam 205: 73–81.Medline
10.1002/(SICI)1097-0177(199601)205:1<73::AID-AJA7>3.0.CO;2-2 CAS PubMed Web of Science® Google Scholar
- Blake RD, Hess ST, Nicholson Tuell J. 1992. The influence of nearest neighbors on the rate and pattern of spontaneous point mutations. J Mol Evol 34: 189–200.Medline
- Deinard AS, Kidd KK. 1995. Levels of DNA polymorphism in extant and extinct hominoids. In: S Brenner, editors. The origin and past of modern humans as viewed from DNA. NJ: World Scientific. p 149–170.
- Deinard AS, Kidd KK. 1999. Evolution of a HOXB6 intergenic region within the great apes and humans. J Hum Evol (in press)
- Deinard AS, Ruano G, Kidd KK. 1992. A dinucleotide repeat polymorphism at the HOX2B locus. Nucl Acids Res 20: 1171
- Delgado S, Gomez M, Bird A, Antequera F. 1998. Initiation of DNA replication at CpG islands in mammalian chromosomes. EMBO J 17: 2426–2435.Medline
- Duboule D. 1998. Vertebrate hox gene regulation: clustering and/or colinearity? Curr Opin Genet Dev 8: 514–518.Medline
- Eid R, Koseki H, Schughart K. 1993. Analysis of LacZ reporter genes in transgenic embryos suggests the presence of several cis-acting regulatory elements in the murine Hoxb-6 gene. Dev Dyn 196: 205–216.Medline
- Finnerty J, Martindale M. 1998. The evolution of the Hox cluster: insights from outgroups. Curr Opin Genet Dev 8: 681–687.Medline
- Gardiner Garden M, Frommer M. 1987. CpG islands in vertebrate genomes. J Mol Biol 196: 261–282.Medline
- Gaunt SJ. 1994. Conservation in the Hox code during morphological evolution. Int J Dev Biol 38: 549–552.Medline
- Gellon G, McGinnis W. 1998. Shaping animal body plans in development and evolution by modulation of Hox expression patterns. Bioessays 20: 116–125.Medline
10.1002/(SICI)1521-1878(199802)20:2<116::AID-BIES4>3.0.CO;2-R CAS PubMed Web of Science® Google Scholar
- Gould A, Morrison A, Sproat G, White RAH, Krumlauf R. 1997. Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev 11: 900–913.Medline
- Keegan LP, Haerry TE, Crotty DA, Packer AI, Wolgemuth DJ, Gehring WJ. 1997. A sequence conserved in vertebrate Hox gene introns functions as an enhancer regulated by posterior homeotic genes in Drosophila imaginal discs. Mech Dev 63: 145–157.Medline
- Larsen F, Gundersen G, Lopez R, Prydz H. 1992. CpG islands as gene markers in the human genome. Genomics 13: 1095–1107.Medline
- Maddison W, Maddison D. 1992. MacClade. Sunderland, MA: Sinauer Associates.
- McGinnis W. 1994. A century of homeosis, a decade of homeoboxes. Genetics 137: 607–611.Medline
- McGinnis W, Krumlauf R. 1992. Homeobox genes and axial patterning. Cell 24: 283–302.
- Murphy PD, Ferguson-Smith AC, Miki T, Feinberg AA, Ruddle FH, Kidd KK. 1987. A moderately frequent RFLP identified by both SacI and BanII with a probe from the HOX2 locus in man (17q11-17q22). Nucl Acids Res 15: 6311–6312.Medline
- Oxford Molecular Group (OMG). 1997. MacVector. Oxford, UK: Oxford Molecular Group.
- Ruano G, Gray MR, Miki T, Ferguson-Smith AC, Ruddle FHR, Kidd KK. 1990. Monomorphism among humans and sequence differences among higher primates for a sequence tagged site (STS) in homeo box cluster 2. Nucl Acids Res 18: 1314Medline
- Schorderet DF, Gartler SM. 1992. Analysis of CpG suppression in methylated and nonmethylated species. Proc Natl Acad Sci USA 89: 957–961.Medline
- Sharpe J, Nonchev S, Gould A, Whiting J, Krumlauf R. 1998. Selectivity, sharing and competitive interactions in the regulation of Hoxb genes. EMBO 17: 1788–1798.Medline
- Shen R, Chen Y, Huang L, Vitale E, Solursh M. 1994. Characterization of the human MSX-1 promoter and an enhancer responsible for retinoic acid induction. Cell Mol Biol Res 40: 297–312.Medline
- Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673–4680.Medline
