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PMID: 1348688 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Structural complexity and evolutionary conservation of the Drosophila homeotic gene proboscipedia.

The EMBO journal ·Vol. 11 ·No. 4 ·1992-04-00 ·Pages 1437-49

Cribbs DL, Pultz MA, Johnson D, Mazzulla M, Kaufman TC

Abstract

Mutations of the homeotic gene proboscipedia (pb) of Drosophila cause striking transformations of the adult mouthparts, to legs or antennae. We report here an analysis of the gene structure of pb. Coding sequences across a 34 kb interval yield, by alternative splicing, four identified mRNA forms which differ immediately upstream of the homeobox. As a consequence, the homeodomain is expected to reside in four different contexts in the predicted protein isoforms. Mammalian homologs of pb, human HOX-2H and murine Hox-2.8, were identified based on the similarities of their homeodomains (95% identity) and several other conserved motifs. Examination of a collection of pb mutant alleles with antisera directed against the N-terminal region, the center or the C-terminal region of the protein showed that, surprisingly, several partial loss-of-function pb alleles appear to generate partially functional proteins truncated at their C-termini. This suggests that a significant portion of the protein contributes quantitatively to pb function, but is partially dispensable. Finally, evolutionary considerations suggest that pb may be one of several ancient genes which preceded the process yielding the modern homeotic gene complexes.

Related Genes
HOX-2H Hox-2.8 pb
MeSH Terms
Amino Acid Sequence Animals Base Sequence Biological Evolution DNA/genetics,isolation & purification Drosophila/genetics Exons Genes, Homeobox Humans Mice Molecular Sequence Data Oligodeoxyribonucleotides Phenotype Polymerase Chain Reaction/methods Protein Conformation RNA Splicing RNA, Messenger/genetics,metabolism Sequence Homology, Nucleic Acid
Chemicals
Oligodeoxyribonucleotides RNA, Messenger DNA
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Cribbs D L
Howard Hughes Medical Institute, Indiana University, Bloomington 47401.
Pultz M A
Johnson D
Mazzulla M
Kaufman T C
References (73)
73 references, click to expand
  1. The molecular basis for metameric pattern in the Drosophila embryo.
    Development. 1987 Sep;101(1):1-22 PMID: 2896587
  2. Evidence that the Abdominal-B r element function is conferred by a trans-regulatory homeoprotein.
    EMBO J. 1988 Oct;7(10):3223-31 PMID: 2903049
  3. opa: a novel family of transcribed repeats shared by the Notch locus and other developmentally regulated loci in D. melanogaster.
    Cell. 1985 Jan;40(1):55-62 PMID: 2981631
  4. Distribution of the Sex combs reduced gene products in Drosophila melanogaster.
    Genetics. 1987 Sep;117(1):51-60 PMID: 3117618
  5. DNA sequence comparison between two tissue-specific variants of the autonomous parvovirus, minute virus of mice.
    Nucleic Acids Res. 1985 May 24;13(10):3617-33 PMID: 3855242
  6. Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein.
    Cell. 1985 Nov;43(1):59-69 PMID: 3935318
  7. Transcription maps of polyoma virus-specific RNA: analysis by two-dimensional nuclease S1 gel mapping.
    Methods Enzymol. 1980;65(1):718-49 PMID: 6154876
  8. Sequencing end-labeled DNA with base-specific chemical cleavages.
    Methods Enzymol. 1980;65(1):499-560 PMID: 6246368
  9. Structural organization and sequence of the homeotic gene Antennapedia of Drosophila melanogaster.
    EMBO J. 1986 Apr;5(4):733-9 PMID: 10408949
  10. What determines the specificity of action of Drosophila homeodomain proteins?
    Cell. 1990 Nov 30;63(5):883-94 PMID: 1979524
  11. Human Hox-4.2 and Drosophila deformed encode similar regulatory specificities in Drosophila embryos and larvae.
    Cell. 1990 Nov 30;63(5):969-76 PMID: 1979526
  12. Alternative RNA products from the Ultrabithorax domain of the bithorax complex.
    EMBO J. 1988 Feb;7(2):435-45 PMID: 2452731
  13. Developmental distribution of RNA and protein products of the Drosophila alpha-tubulin gene family.
    Dev Biol. 1989 Mar;132(1):45-61 PMID: 2492961
  14. Distal-less encodes a homoeodomain protein required for limb development in Drosophila.
    Nature. 1989 Mar 30;338(6214):432-4 PMID: 2564639
  15. The homeotic gene Sex Combs Reduced of Drosophila: gene structure and embryonic expression.
    EMBO J. 1989 Jan;8(1):219-27 PMID: 2565809
  16. Hox and HOM: homologous gene clusters in insects and vertebrates.
    Cell. 1989 May 5;57(3):347-9 PMID: 2566382
  17. The murine and Drosophila homeobox gene complexes have common features of organization and expression.
    Cell. 1989 May 5;57(3):367-78 PMID: 2566383
  18. Transcriptional activation and repression by Ultrabithorax proteins in cultured Drosophila cells.
    Cell. 1989 Jun 16;57(6):1031-43 PMID: 2567632
  19. The structure and function of the homeodomain.
    Biochim Biophys Acta. 1989 Jul 28;989(1):25-48 PMID: 2568852
  20. A single amino acid can determine the DNA binding specificity of homeodomain proteins.
    Cell. 1989 Nov 3;59(3):553-62 PMID: 2572327
  21. Novel patterns of homeotic protein accumulation in the head of the Drosophila embryo.
    Development. 1989 Jan;105(1):167-74 PMID: 2572411
  22. The human HOX gene family.
    Nucleic Acids Res. 1989 Dec 25;17(24):10385-402 PMID: 2574852
  23. Distribution of the wingless gene product in Drosophila embryos: a protein involved in cell-cell communication.
    Cell. 1989 Nov 17;59(4):739-49 PMID: 2582493
  24. The proboscipedia locus of the Antennapedia complex: a molecular and genetic analysis.
    Genes Dev. 1988 Jul;2(7):901-20 PMID: 2850265
  25. Structure of transcripts from the homeotic Antennapedia gene of Drosophila melanogaster: two promoters control the major protein-coding region.
    Mol Cell Biol. 1986 Dec;6(12):4676-89 PMID: 2879223
  26. Divergent homeo box proteins recognize similar DNA sequences in Drosophila.
    Nature. 1988 Apr 28;332(6167):858-61 PMID: 2895896
  27. The molecular genetics of embryonic pattern formation in Drosophila.
    Nature. 1988 Sep 1;335(6185):25-34 PMID: 2901040
  28. Developmentally regulated alternative splicing of transcripts from the Drosophila homeotic gene Antennapedia can produce four different proteins.
    EMBO J. 1988 Oct;7(10):3211-22 PMID: 2903048
  29. Splicing of messenger RNA precursors.
    Annu Rev Biochem. 1986;55:1119-50 PMID: 2943217
  30. Assembly of the mitochondrial membrane system. CBP6, a yeast nuclear gene necessary for synthesis of cytochrome b.
    J Biol Chem. 1985 Feb 10;260(3):1513-20 PMID: 2981859
  31. How eukaryotic transcriptional activators work.
    Nature. 1988 Oct 20;335(6192):683-9 PMID: 3050531
  32. The bithorax complex.
    Annu Rev Genet. 1987;21:285-319 PMID: 3327467
  33. Segmental distribution of bithorax complex proteins during Drosophila development.
    Nature. 1985 Feb 14-20;313(6003):545-51 PMID: 3918274
  34. Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22.
    Cell. 1986 Feb 14;44(3):429-38 PMID: 3943132
  35. Synthesis of human insulin gene. VIII. Construction of expression vectors for fused proinsulin production in Escherichia coli.
    Gene. 1984 Jul-Aug;29(1-2):251-4 PMID: 6092228
  36. A simple and very efficient method for generating cDNA libraries.
    Gene. 1983 Nov;25(2-3):263-9 PMID: 6198242
  37. Kilo-sequencing: creation of an ordered nest of asymmetric deletions across a large target sequence carried on phage M13.
    Methods Enzymol. 1983;101:98-122 PMID: 6310345
  38. Genes controlling segmental specification in the Drosophila thorax.
    Proc Natl Acad Sci U S A. 1982 Dec;79(23):7380-4 PMID: 6961417
  39. A deficiency of the homeotic complex of the beetle Tribolium.
    Nature. 1991 Mar 7;350(6313):72-4 PMID: 11536480
  40. Proximal-distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development.
    EMBO J. 1989 Jul;8(7):2045-55 PMID: 16453891
  41. Cytogenetic Analysis of Chromosome 3 in DROSOPHILA MELANOGASTER: The Homoeotic Gene Complex in Polytene Chromosome Interval 84a-B.
    Genetics. 1980 Jan;94(1):115-33 PMID: 17248988
  42. Genetic Analysis of the Antennapedia Gene Complex (Ant-C) and Adjacent Chromosomal Regions of DROSOPHILA MELANOGASTER. II. Polytene Chromosome Segments 84A-84B1,2.
    Genetics. 1980 Jun;95(2):383-97 PMID: 17249042
  43. Cytogenetic Analysis of Chromosome 3 in DROSOPHILA MELANOGASTER: Isolation and Characterization of Four New Alleles of the Proboscipedia (pb) Locus.
    Genetics. 1978 Nov;90(3):579-96 PMID: 17248871
  44. Developmental and molecular analysis of Deformed; a homeotic gene controlling Drosophila head development.
    EMBO J. 1987 Mar;6(3):767-77 PMID: 16453752
  45. A gene complex controlling segmentation in Drosophila.
    Nature. 1978 Dec 7;276(5688):565-70 PMID: 103000
  46. Regionally restricted developmental defects resulting from targeted disruption of the mouse homeobox gene hox-1.5.
    Nature. 1991 Apr 11;350(6318):473-9 PMID: 1673020
  47. A cluster of Antennapedia-class homeobox genes in a nonsegmented animal.
    Science. 1991 Aug 2;253(5019):516-7 PMID: 1677487
  48. Rescue and regulation of proboscipedia: a homeotic gene of the Antennapedia Complex.
    Development. 1991 Sep;113(1):257-71 PMID: 1684932
  49. A functional and structural analysis of the Sex combs reduced locus of Drosophila melanogaster.
    Genetics. 1991 Oct;129(2):423-41 PMID: 1743486
  50. The specificities of Sex combs reduced and Antennapedia are defined by a distinct portion of each protein that includes the homeodomain.
    Cell. 1990 Sep 21;62(6):1087-103 PMID: 1976044
  51. Targets of homeotic gene control in Drosophila.
    Nature. 1990 Nov 22;348(6299):308-12 PMID: 1979146
  52. Mouse Hox-2.2 specifies thoracic segmental identity in Drosophila embryos and larvae.
    Cell. 1990 Nov 30;63(5):961-7 PMID: 1979525
  53. Functional dissection of Ultrabithorax proteins in D. melanogaster.
    Cell. 1990 Feb 23;60(4):597-610 PMID: 2105847
  54. Molecular structure and spatial expression of a homeobox gene from the labial region of the Antennapedia-complex.
    EMBO J. 1988 Aug;7(8):2569-78 PMID: 2461299
  55. Genetic analysis of the homeotic gene complex (HOM-C) in the beetle Tribolium castaneum.
    Dev Biol. 1989 May;133(1):196-209 PMID: 2565268
  56. Structure and expression of a family of Ultrabithorax mRNAs generated by alternative splicing and polyadenylation in Drosophila.
    Genes Dev. 1989 Feb;3(2):243-58 PMID: 2565858
  57. Isolation, structure, and expression of labial, a homeotic gene of the Antennapedia Complex involved in Drosophila head development.
    Genes Dev. 1989 Mar;3(3):399-414 PMID: 2566560
  58. Two steps in the evolution of Antennapedia-class vertebrate homeobox genes.
    Proc Natl Acad Sci U S A. 1989 Jul;86(14):5459-63 PMID: 2568634
  59. The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes.
    EMBO J. 1989 May;8(5):1497-505 PMID: 2569969
  60. Drosophila NK-homeobox genes.
    Proc Natl Acad Sci U S A. 1989 Oct;86(20):7716-20 PMID: 2573058
  61. The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the Abdominal-B domain.
    Genes Dev. 1989 Sep;3(9):1424-36 PMID: 2575066
  62. Multiple transcripts from the Antennapedia gene of Drosophila melanogaster.
    Mol Cell Biol. 1986 Dec;6(12):4667-75 PMID: 2879222
  63. Molecular characterization of the zerknüllt region of the Antennapedia gene complex in Drosophila.
    Genes Dev. 1987 Dec;1(10):1268-79 PMID: 2892759
  64. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  65. 3' non-coding region sequences in eukaryotic messenger RNA.
    Nature. 1976 Sep 16;263(5574):211-4 PMID: 822353
  66. Nematode homeobox cluster.
    Nature. 1991 Jun 27;351(6329):703 PMID: 1676487
  67. A mouse gene related to Distal-less shows a restricted expression in the developing forebrain.
    Nature. 1991 Jun 27;351(6329):748-51 PMID: 1676488
  68. Molecular cloning and expression of a novel homeobox gene AHox1 of the ascidian, Halocynthia roretzi.
    Development. 1991 Mar;111(3):821-8 PMID: 1679006
  69. Developmental and evolutionary implications of labial, Deformed and engrailed expression in the Drosophila head.
    Development. 1991 Sep;113(1):273-81 PMID: 1684933
  70. Cloning and analysis of three new homeobox genes from the nematode Caenorhabditis elegans.
    Nucleic Acids Res. 1990 Apr 25;18(8):2033-6 PMID: 1970877
  71. Molecular and genetic organization of the antennapedia gene complex of Drosophila melanogaster.
    Adv Genet. 1990;27:309-62 PMID: 1971986
  72. Crystal structure of an engrailed homeodomain-DNA complex at 2.8 A resolution: a framework for understanding homeodomain-DNA interactions.
    Cell. 1990 Nov 2;63(3):579-90 PMID: 1977522
  73. abdA expression in Drosophila embryos.
    Genes Dev. 1990 Sep;4(9):1573-87 PMID: 1979297
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1992-04-00
Pages
1437-49
Language
English
Region
England
NLM ID
8208664
PMCID
PMC556592
Subset
IM
Grants
NIGMS NIH HHS · GM07757 · United States
NIGMS NIH HHS · GM24299 · United States
Databases
GENBANK
X63633, X63634, X63635, X63636, X63637, X63638, X63639, X63640, X63728, X63729
External Links
PubMed source PMC Full Text View journal details
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