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PMID: 9724756 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The Drosophila LIM-only gene, dLMO, is mutated in Beadex alleles and might represent an evolutionarily conserved function in appendage development.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 95 ·No. 18 ·1998-09-01 ·Pages 10637-42

Zeng C, Justice NJ, Abdelilah S, Chan YM, Jan LY, Jan YN

Abstract

The process of wing patterning involves precise molecular mechanisms to establish an organizing center at the dorsal-ventral boundary, which functions to direct the development of the Drosophila wing. We report that misexpression of dLMO, a Drosophila LIM-only protein, in specific patterns in the developing wing imaginal disc, disrupts the dorsal-ventral (D-V) boundary and causes errors in wing patterning. When dLMO is misexpressed along the anterior-posterior boundary, extra wing outgrowth occurs, similar to the phenotype seen when mutant clones lacking Apterous, a LIM homeodomain protein known to be essential for normal D-V patterning of the wing, are made in the wing disc. When dLMO is misexpressed along the D-V boundary in third instar larvae, loss of the wing margin is observed. This phenotype is very similar to the phenotype of Beadex, a long-studied dominant mutation that we show disrupts the dLMO transcript in the 3' untranslated region. dLMO normally is expressed in the wing pouch of the third instar wing imaginal disc during patterning. A mammalian homolog of dLMO is expressed in the developing limb bud of the mouse. This indicates that LMO proteins might function in an evolutionarily conserved mechanism involved in patterning the appendages.

MeSH Terms
Alleles Animals Base Sequence Biological Evolution Blotting, Southern DNA Primers Drosophila/genetics Drosophila Proteins Extremities/growth & development Homeodomain Proteins/genetics Mice Mutation Wings, Animal/embryology
Chemicals
Bx protein, Drosophila DNA Primers Drosophila Proteins Homeodomain Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Zeng C
Howard Hughes Medical Institute, Department of Physiology and Department of Biochemistry, University of California at San Francisco, San Francisco, CA 94143-0725, USA.
Justice N J
Abdelilah S
Chan Y M
Jan L Y
Jan Y N
References (41)
41 references, click to expand
  1. Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing.
    Development. 1997 Feb;124(4):871-80 PMID: 9043068
  2. A single ancestral gene of the human LIM domain oncogene family LMO in Drosophila: characterization of the Drosophila Dlmo gene.
    Oncogene. 1995 Oct 5;11(7):1283-90 PMID: 7478548
  3. Serrate-mediated activation of Notch is specifically blocked by the product of the gene fringe in the dorsal compartment of the Drosophila wing imaginal disc.
    Development. 1997 Aug;124(15):2973-81 PMID: 9247339
  4. Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila.
    Cell. 1993 Nov 19;75(4):741-52 PMID: 8242746
  5. Nuclear LIM interactor, a rhombotin and LIM homeodomain interacting protein, is expressed early in neuronal development.
    Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11693-8 PMID: 8876198
  6. Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome.
    Nat Genet. 1998 May;19(1):51-5 PMID: 9590288
  7. The Beadex Locus in Drosophila Melanogaster: On the Nature of the Mutants Bx and Bx.
    Genetics. 1953 Jan;38(1):91-105 PMID: 17247425
  8. Functional analysis of the nuclear LIM domain interactor NLI.
    Mol Cell Biol. 1997 Oct;17(10):5688-98 PMID: 9315627
  9. Isolation and characterization of the Beadex locus of Drosophila melanogaster: a putative cis-acting negative regulatory element for the heldup-a gene.
    Mol Cell Biol. 1984 Jul;4(7):1343-53 PMID: 6095064
  10. Wingless signaling generates pattern through two distinct mechanisms.
    Development. 1997 Oct;124(19):3727-36 PMID: 9367428
  11. A cluster of chromosome 11p13 translocations found via distinct D-D and D-D-J rearrangements of the human T cell receptor delta chain gene.
    EMBO J. 1988 Jul;7(7):2011-7 PMID: 3416831
  12. The LIM domain: a new structural motif found in zinc-finger-like proteins.
    Trends Genet. 1994 Sep;10(9):315-20 PMID: 7974745
  13. Interactions of the LIM-domain-binding factor Ldb1 with LIM homeodomain proteins.
    Nature. 1996 Nov 21;384(6606):270-2 PMID: 8918878
  14. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes.
    Histochemistry. 1993 Dec;100(6):431-40 PMID: 7512949
  15. Tiggrin, a novel Drosophila extracellular matrix protein that functions as a ligand for Drosophila alpha PS2 beta PS integrins.
    Development. 1994 Jul;120(7):1747-58 PMID: 7924982
  16. Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos.
    Genes Dev. 1990 Aug;4(8):1322-31 PMID: 1977661
  17. The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes.
    Cell. 1994 Jan 14;76(1):77-87 PMID: 8287481
  18. The LIM-domain binding protein Ldb1 and its partner LMO2 act as negative regulators of erythroid differentiation.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13707-12 PMID: 9391090
  19. Specificity of single LIM motifs in targeting and LIM/LIM interactions in situ.
    Genes Dev. 1996 Feb 1;10(3):289-300 PMID: 8595880
  20. fringe, a Boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development.
    Cell. 1994 Nov 18;79(4):595-606 PMID: 7954826
  21. A modular misexpression screen in Drosophila detecting tissue-specific phenotypes.
    Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12418-22 PMID: 8901596
  22. Molecular models for vertebrate limb development.
    Cell. 1997 Sep 19;90(6):979-90 PMID: 9323126
  23. Genetic identification of dominant overproducing mutations: the Beadex gene.
    Mol Gen Genet. 1979 Mar 20;171(2):153-9 PMID: 108520
  24. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins.
    Cell. 1990 Apr 6;61(1):49-59 PMID: 2156629
  25. The LIM/double zinc-finger motif functions as a protein dimerization domain.
    Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10655-9 PMID: 7938009
  26. Chip, a widely expressed chromosomal protein required for segmentation and activity of a remote wing margin enhancer in Drosophila.
    Genes Dev. 1997 Oct 15;11(20):2729-40 PMID: 9334334
  27. DeLIMiting development.
    Bioessays. 1998 Jan;20(1):58-69 PMID: 9504048
  28. The cysteine-rich LIM domains inhibit DNA binding by the associated homeodomain in Isl-1.
    EMBO J. 1993 Nov;12(11):4243-50 PMID: 7901000
  29. Systematic gain-of-function genetics in Drosophila.
    Development. 1998 Mar;125(6):1049-57 PMID: 9463351
  30. Genetic control of wing disc development in Drosophila.
    Ciba Found Symp. 1975;0(29):161-82 PMID: 1039909
  31. Glued participates in distinct microtubule-based activities in Drosophila eye development.
    Development. 1997 Apr;124(8):1497-507 PMID: 9108366
  32. The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins.
    EMBO J. 1997 Jun 2;16(11):3145-57 PMID: 9214632
  33. Somitogenesis.
    Curr Top Dev Biol. 1998;38:225-87 PMID: 9399080
  34. The beadex locus in Drosophila melanogaster: genetic analysis of the mutant Bxr49k.
    Z Indukt Abstamm Vererbungsl. 1953;85(4):435-49 PMID: 13170354
  35. Extent and character of circadian gene expression in Drosophila melanogaster: identification of twenty oscillating mRNAs in the fly head.
    Curr Biol. 1995 Dec 1;5(12):1424-36 PMID: 8749395
  36. Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation.
    Genes Dev. 1996 Feb 15;10(4):421-34 PMID: 8600026
  37. A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins.
    Genes Dev. 1997 Jun 1;11(11):1370-80 PMID: 9192866
  38. Ectopic expression and function of the Antp and Scr homeotic genes: the N terminus of the homeodomain is critical to functional specificity.
    Development. 1993 Jun;118(2):339-52 PMID: 7900989
  39. apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins.
    Genes Dev. 1992 May;6(5):715-29 PMID: 1349545
  40. TTG-2, a new gene encoding a cysteine-rich protein with the LIM motif, is overexpressed in acute T-cell leukaemia with the t(11;14)(p13;q11).
    Oncogene. 1991 Oct;6(10):1887-93 PMID: 1923511
  41. Persistent expression of genes of the enhancer of split complex suppresses neural development in Drosophila.
    Neuron. 1996 Feb;16(2):275-86 PMID: 8789943
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.95.18.10637
Published
1998-09-01
Pages
10637-42
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC27947
Subset
IM
External Links
PubMed source DOI: 10.1073/pnas.95.18.10637 PMC Full Text View journal details
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