Home LiteratureArticle Details
PMID: 8790328 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S. Review

Modular cis-regulatory organization of developmentally expressed genes: two genes transcribed territorially in the sea urchin embryo, and additional examples.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 93 ·No. 18 ·1996-09-03 ·Pages 9322-8

Kirchhamer CV, Yuh CH, Davidson EH

Abstract

The cis-regulatory systems that control developmental expression of two sea urchin genes have been subjected to detailed functional analysis. Both systems are modular in organization: specific, separable fragments of the cis-regulatory DNA each containing multiple transcription factor target sites execute particular regulatory subfunctions when associated with reporter genes and introduced into the embryo. The studies summarized here were carried out on the CyIIIa gene, expressed in the embryonic aboral ectoderm and on the Endo16 gene, expressed in the embryonic vegetal plate, archenteron, and then midgut. The regulatory systems of both genes include modules that control particular aspects of temporal and spatial expression, and in both the territorial boundaries of expression depend on a combination of negative and positive functions. In both genes different regulatory modules control early and late embryonic expression. Modular cis-regulatory organization is widespread in developmentally regulated genes, and we present a tabular summary that includes many examples from mouse and Drosophila. We regard cis-regulatory modules as units of developmental transcription control, and also of evolution, in the assembly of transcription control systems.

MeSH Terms
Actins/genetics Animals Base Sequence Cell Adhesion Molecules/genetics DNA Gene Expression Regulation, Developmental Mice Molecular Sequence Data Proteins/genetics Restriction Mapping Sea Urchins/embryology,genetics Transcription, Genetic
Chemicals
Actins Cell Adhesion Molecules Proteins endo16 protein, sea urchin DNA
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Kirchhamer C V
Division of Biology, California Institute of Technology, Pasadena 91125, USA.
Yuh C H
Davidson E H
References (67)
67 references, click to expand
  1. Differential regulation of Ultrabithorax in two germ layers of Drosophila.
    Cell. 1988 May 20;53(4):567-76 PMID: 2897241
  2. An in vivo titration of regulatory factors required for expression of a fusion gene in transgenic sea urchin embryos.
    Proc Natl Acad Sci U S A. 1988 Oct;85(20):7607-11 PMID: 3174654
  3. Developmental appearance of factors that bind specifically to cis-regulatory sequences of a gene expressed in the sea urchin embryo.
    Genes Dev. 1988 Sep;2(9):1074-88 PMID: 3192074
  4. Spatial and temporal information processing in the sea urchin embryo: modular and intramodular organization of the CyIIIa gene cis-regulatory system.
    Development. 1996 Jan;122(1):333-48 PMID: 8565846
  5. SpRunt-1, a new member of the runt domain family of transcription factors, is a positive regulator of the aboral ectoderm-specific CyIIIA gene in sea urchin embryos.
    Dev Biol. 1996 Feb 25;174(1):43-54 PMID: 8626020
  6. Modular cis-regulatory organization of Endo16, a gut-specific gene of the sea urchin embryo.
    Development. 1996 Apr;122(4):1069-82 PMID: 8620834
  7. Sequences of the CyIIIa actin gene regulatory domain bound specifically by sea urchin embryo nuclear proteins.
    Mol Reprod Dev. 1990 Feb;25(2):110-22 PMID: 2310563
  8. Repetitive DNA sequences linked to the sea urchin spec genes contain transcriptional enhancer-like elements.
    Dev Biol. 1990 May;139(1):186-96 PMID: 2328835
  9. How embryos work: a comparative view of diverse modes of cell fate specification.
    Development. 1990 Mar;108(3):365-89 PMID: 2187672
  10. Position-specific activity of the Hox1.1 promoter in transgenic mice.
    Development. 1990 Mar;108(3):435-42 PMID: 1971214
  11. cis-acting control elements for Krüppel expression in the Drosophila embryo.
    EMBO J. 1990 Aug;9(8):2587-95 PMID: 2114978
  12. Competitive titration in living sea urchin embryos of regulatory factors required for expression of the CyIIIa actin gene.
    Development. 1990 Sep;110(1):31-40 PMID: 2081468
  13. Negative spatial regulation of the lineage specific CyIIIa actin gene in the sea urchin embryo.
    Development. 1990 Sep;110(1):41-50 PMID: 2081469
  14. Transcriptional control of Drosophila fushi tarazu zebra stripe expression.
    Genes Dev. 1989 Mar;3(3):384-98 PMID: 2498165
  15. Autoregulatory and gap gene response elements of the even-skipped promoter of Drosophila.
    EMBO J. 1989 Apr;8(4):1205-12 PMID: 2743979
  16. Endo16, a lineage-specific protein of the sea urchin embryo, is first expressed just prior to gastrulation.
    Dev Biol. 1989 Nov;136(1):264-72 PMID: 2680683
  17. Segregation of oral from aboral ectoderm precursors is completed at fifth cleavage in the embryogenesis of Strongylocentrotus purpuratus.
    Dev Biol. 1990 Jan;137(1):77-85 PMID: 2295368
  18. DNA regions that regulate the ovarian transcriptional specificity of Drosophila yolk protein genes.
    Genes Dev. 1989 Sep;3(9):1453-61 PMID: 2606354
  19. Lineage-specific gene expression and the regulative capacities of the sea urchin embryo: a proposed mechanism.
    Development. 1989 Mar;105(3):421-45 PMID: 2693035
  20. Spatial regulation of zerknüllt: a dorsal-ventral patterning gene in Drosophila.
    Genes Dev. 1989 Oct;3(10):1518-33 PMID: 2612903
  21. Expression of two actin genes during larval development in the sea urchin Strongylocentrotus purpuratus.
    Mol Reprod Dev. 1989;1(3):149-55 PMID: 2483321
  22. A positive cis-regulatory element with a bicoid target site lies within the sea urchin Spec2a enhancer.
    Dev Biol. 1993 May;157(1):119-32 PMID: 8097732
  23. Conservation of regulatory elements controlling hairy pair-rule stripe formation.
    Development. 1993 Feb;117(2):585-96 PMID: 8330529
  24. Identification of two regions from the Drosophila decapentaplegic gene required for embryonic midgut development and larval viability.
    Dev Biol. 1993 Sep;159(1):276-87 PMID: 8365566
  25. Proximal cis-acting elements cooperate to set Hoxb-7 (Hox-2.3) expression boundaries in transgenic mice.
    Development. 1993 May;118(1):71-82 PMID: 8104144
  26. Cross regulation of decapentaplegic and Ultrabithorax transcription in the embryonic visceral mesoderm of Drosophila.
    Development. 1993 Apr;117(4):1211-22 PMID: 8404526
  27. Whole mount in situ hybridization shows Endo 16 to be a marker for the vegetal plate territory in sea urchin embryos.
    Mech Dev. 1993 Aug;42(3):117-24 PMID: 8217840
  28. Highly identical cassettes of gene regulatory elements, genomically repetitive and present in RNA.
    Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10851-5 PMID: 8248181
  29. Structure and activity of regulatory elements involved in the activation of the Hoxd-11 gene during late gastrulation.
    EMBO J. 1993 Sep;12(9):3539-50 PMID: 7902810
  30. Direct regulation of decapentaplegic by Ultrabithorax and its role in Drosophila midgut morphogenesis.
    Cell. 1994 Feb 11;76(3):461-75 PMID: 7906203
  31. Neurogenic expression of snail is controlled by separable CNS and PNS promoter elements.
    Development. 1994 Jan;120(1):199-207 PMID: 8119127
  32. Transcriptional activation: a complex puzzle with few easy pieces.
    Cell. 1994 Apr 8;77(1):5-8 PMID: 8156597
  33. Embryonic expression patterns of the Drosophila decapentaplegic gene: separate regulatory elements control blastoderm expression and lateral ectodermal expression.
    Dev Dyn. 1994 Jan;199(1):28-44 PMID: 8167377
  34. A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1.
    Nature. 1994 Aug 18;370(6490):567-71 PMID: 7914354
  35. Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1.
    Science. 1994 Sep 16;265(5179):1728-32 PMID: 7916164
  36. Endo16, a large multidomain protein found on the surface and ECM of endodermal cells during sea urchin gastrulation, binds calcium.
    Dev Biol. 1994 Sep;165(1):73-85 PMID: 8088452
  37. Genomic regions regulating early embryonic expression of the Drosophila neurogenic gene Delta.
    Mech Dev. 1994 Jul;47(1):99-110 PMID: 7947325
  38. Short-range repression permits multiple enhancers to function autonomously within a complex promoter.
    Genes Dev. 1994 Aug 1;8(15):1829-38 PMID: 7958860
  39. The WD repeats of Tup1 interact with the homeo domain protein alpha 2.
    Genes Dev. 1994 Dec 1;8(23):2857-67 PMID: 7995523
  40. Complexity and organization of DNA-protein interactions in the 5'-regulatory region of an endoderm-specific marker gene in the sea urchin embryo.
    Mech Dev. 1994 Aug;47(2):165-86 PMID: 7811639
  41. A multimerizing transcription factor of sea urchin embryos capable of looping DNA.
    Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2989-93 PMID: 7708761
  42. SpZ12-1, a negative regulator required for spatial control of the territory-specific CyIIIa gene in the sea urchin embryo.
    Development. 1995 Apr;121(4):1111-22 PMID: 7743924
  43. Evolutionary-conserved enhancers direct region-specific expression of the murine Hoxa-1 and Hoxa-2 loci in both mice and Drosophila.
    Development. 1995 Apr;121(4):957-74 PMID: 7743939
  44. Spatial regulation of SpMTA metallothionein gene expression in sea urchin embryos by a regulatory cassette in intron 1.
    Mech Dev. 1995 Apr;50(2-3):131-7 PMID: 7619725
  45. Cis-regulatory control of the SM50 gene, an early marker of skeletogenic lineage specification in the sea urchin embryo.
    Development. 1995 Jul;121(7):1957-70 PMID: 7635044
  46. Cis-regulation of achaete and scute: shared enhancer-like elements drive their coexpression in proneural clusters of the imaginal discs.
    Genes Dev. 1995 Aug 1;9(15):1869-82 PMID: 7649474
  47. Regulation of the Hoxb-8 gene: synergism between multimerized cis-acting elements increases responsiveness to positional information.
    Dev Biol. 1995 Oct;171(2):294-305 PMID: 7556914
  48. Micromeres are required for normal vegetal plate specification in sea urchin embryos.
    Development. 1995 Oct;121(10):3215-22 PMID: 7588056
  49. Comparative analysis of chicken Hoxb-4 regulation in transgenic mice.
    Mech Dev. 1995 Sep;53(1):47-59 PMID: 8555111
  50. Specificity of CNS and PNS regulatory subelements comprising pan-neural enhancers of the deadpan and scratch genes is achieved by repression.
    Development. 1995 Nov;121(11):3549-60 PMID: 8582269
  51. The bx region enhancer, a distant cis-control element of the Drosophila Ubx gene and its regulation by hunchback and other segmentation genes.
    EMBO J. 1991 Jun;10(6):1415-25 PMID: 1902784
  52. Individual stripe regulatory elements in the Drosophila hairy promoter respond to maternal, gap, and pair-rule genes.
    Genes Dev. 1991 May;5(5):840-54 PMID: 1902805
  53. Synthetic oligonucleotides recreate Drosophila fushi tarazu zebra-stripe expression.
    Genes Dev. 1991 May;5(5):855-67 PMID: 1851122
  54. Decoding positional information: regulation of the pair-rule gene hairy.
    Development. 1990 Dec;110(4):1223-31 PMID: 2100260
  55. Cell type specification during sea urchin development.
    Trends Genet. 1991 Jul;7(7):212-8 PMID: 1887502
  56. Multiple spatially specific enhancers are required to reconstruct the pattern of Hox-2.6 gene expression.
    Genes Dev. 1991 Nov;5(11):2048-59 PMID: 1682218
  57. Spatial mechanisms of gene regulation in metazoan embryos.
    Development. 1991 Sep;113(1):1-26 PMID: 1684931
  58. Modulation of sea urchin actin mRNA prevalence during embryogenesis: nuclear synthesis and decay rate measurements of transcripts from five different genes.
    Dev Biol. 1992 Feb;149(2):415-31 PMID: 1730392
  59. Target sequences for hunchback in a control region conferring Ultrabithorax expression boundaries.
    Development. 1991 Dec;113(4):1171-9 PMID: 1687458
  60. The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo.
    Genes Dev. 1992 Sep;6(9):1728-39 PMID: 1325394
  61. A complete second gut induced by transplanted micromeres in the sea urchin embryo.
    Science. 1993 Feb 19;259(5098):1134-8 PMID: 8438164
  62. The interplay between multiple enhancer and silencer elements defines the pattern of decapentaplegic expression.
    Genes Dev. 1993 Apr;7(4):694-704 PMID: 8458580
  63. Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty.
    Q Rev Biol. 1971 Jun;46(2):111-38 PMID: 5160087
  64. Cell lineage-specific programs of expression of multiple actin genes during sea urchin embryogenesis.
    J Mol Biol. 1986 Mar 20;188(2):159-72 PMID: 3723594
  65. Ontogenic activation of a fusion gene introduced into sea urchin eggs.
    Proc Natl Acad Sci U S A. 1987 Jan;84(1):151-5 PMID: 3467346
  66. Correct cell-type-specific expression of a fusion gene injected into sea urchin eggs.
    Dev Biol. 1987 Jun;121(2):576-9 PMID: 3472980
  67. Lineage and fate of each blastomere of the eight-cell sea urchin embryo.
    Genes Dev. 1987 Mar;1(1):75-85 PMID: 2448185
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.93.18.9322
Published
1996-09-03
Pages
9322-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC38426
Subset
IM
Grants
NICHD NIH HHS · HD-05753 · United States
External Links
PubMed source DOI: 10.1073/pnas.93.18.9322 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2