Home LiteratureArticle Details
PMID: 8794860 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Two muscle-specific LIM proteins in Drosophila.

The Journal of cell biology ·Vol. 134 ·No. 5 ·1996-09-00 ·Pages 1179-95

Stronach BE, Siegrist SE, Beckerle MC

Abstract

The LIM domain defines a zinc-binding motif found in a growing number of eukaryotic proteins that regulate cell growth and differentiation during development. Members of the cysteine-rich protein (CRP) family of LIM proteins have been implicated in muscle differentiation in vertebrates. Here we report the identification and characterization of cDNA clones encoding two members of the CRP family in Drosophila, referred to as muscle LIM proteins (Mlp). Mlp60A encodes a protein with a single LIM domain linked to a glycine-rich region. Mlp84B encodes a protein with five tandem LIM-glycine modules. In the embryo, Mlp gene expression is spatially restricted to somatic, visceral, and pharyngeal muscles. Within the somatic musculature, Mlp84B transcripts are enriched at the terminal ends of muscle fibers, whereas Mlp60A transcripts are found throughout the muscle fibers. The distributions of the Mlp60A and Mlp84B proteins mirror their respective mRNA localizations, with Mlp84B enrichment occurring at sites of muscle attachment. Northern blot analysis revealed that Mlp gene expression is developmentally regulated, showing a biphasic pattern over the course of the Drosophila life cycle. Peaks of expression occur late in embryogenesis and during metamorphosis, when the musculature is differentiating. Drosophila Mlp60A and Mlp84B, like vertebrate members of the CRP family, have the ability to associate with the actin cytoskeleton when expressed in rat fibroblast cells. The temporal expression and spatial distribution of muscle LIM proteins in Drosophila are consistent with a role for Mlps in myogenesis, late in the differentiation pathway.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Chromosome Mapping Cloning, Molecular Cytoskeleton/metabolism DNA, Complementary Drosophila Proteins Drosophila melanogaster/embryology,genetics,metabolism In Situ Hybridization LIM Domain Proteins Molecular Sequence Data Muscle Proteins/genetics,metabolism Muscles/embryology,metabolism Sequence Homology, Amino Acid
Chemicals
DNA, Complementary Drosophila Proteins LIM Domain Proteins Mlp60A protein, Drosophila Mlp84B protein, Drosophila Muscle Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Stronach B E
Department of Biology, University of Utah, Salt Lake City 84112, USA.
Siegrist S E
Beckerle M C
References (44)
44 references, click to expand
  1. mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans.
    Cell. 1988 Jul 1;54(1):5-16 PMID: 2898300
  2. The Drosophila PS2 antigen is an invertebrate integrin that, like the fibronectin receptor, becomes localized to muscle attachments.
    Cell. 1987 Dec 24;51(6):929-40 PMID: 2961459
  3. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback.
    Chromosoma. 1989 Aug;98(2):81-5 PMID: 2476281
  4. Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11.
    Nature. 1990 Apr 26;344(6269):876-9 PMID: 1970421
  5. crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia.
    Cell. 1990 Jun 1;61(5):787-99 PMID: 2344615
  6. Characterization of a human cDNA encoding a widely expressed and highly conserved cysteine-rich protein with an unusual zinc-finger motif.
    Nucleic Acids Res. 1990 Jul 11;18(13):3871-9 PMID: 2115670
  7. Expression of a MyoD family member prefigures muscle pattern in Drosophila embryos.
    Genes Dev. 1990 Dec;4(12A):2086-97 PMID: 2176634
  8. The embryonic development of larval muscles in Drosophila.
    Development. 1990 Nov;110(3):791-804 PMID: 2100994
  9. Eukaryotic start and stop translation sites.
    Nucleic Acids Res. 1991 Jun 25;19(12):3185-92 PMID: 1905801
  10. Human cysteine-rich protein. A member of the LIM/double-finger family displaying coordinate serum induction with c-myc.
    J Biol Chem. 1992 May 5;267(13):9176-84 PMID: 1374386
  11. Zyxin and cCRP: two interactive LIM domain proteins associated with the cytoskeleton.
    J Cell Biol. 1992 Dec;119(6):1573-87 PMID: 1469049
  12. Molecular genetic analysis of muscle development, structure, and function in Drosophila.
    Int Rev Cytol. 1993;143:63-152 PMID: 8449665
  13. Tissue-specific ecdysone responses: regulation of the Drosophila genes Eip28/29 and Eip40 during larval development.
    Development. 1992 Dec;116(4):865-76 PMID: 1295740
  14. The LIM motif defines a specific zinc-binding protein domain.
    Proc Natl Acad Sci U S A. 1993 May 15;90(10):4404-8 PMID: 8506279
  15. Suppression in transformed avian fibroblasts of a gene (crp) encoding a cysteine-rich protein containing LIM domains.
    Oncogene. 1993 Sep;8(9):2317-24 PMID: 8361751
  16. Common metal ion coordination in LIM domain proteins.
    Biochemistry. 1994 Jan 18;33(2):468-77 PMID: 8286377
  17. Biochemical and molecular characterization of the chicken cysteine-rich protein, a developmentally regulated LIM-domain protein that is associated with the actin cytoskeleton.
    J Cell Biol. 1994 Jan;124(1-2):117-27 PMID: 8294495
  18. The development of cellular junctions in the Drosophila embryo.
    Dev Biol. 1994 Feb;161(2):563-96 PMID: 8314002
  19. Mutational analysis of the metal sites in an LIM domain.
    J Biol Chem. 1994 Apr 15;269(15):11108-13 PMID: 8157637
  20. SH2/SH3 signaling proteins.
    Curr Opin Genet Dev. 1994 Feb;4(1):25-30 PMID: 8193536
  21. The oncogenic cysteine-rich LIM domain protein rbtn2 is essential for erythroid development.
    Cell. 1994 Jul 15;78(1):45-57 PMID: 8033210
  22. Conserved structures and diversity of functions of RNA-binding proteins.
    Science. 1994 Jul 29;265(5172):615-21 PMID: 8036511
  23. D-mef2: a Drosophila mesoderm-specific MADS box-containing gene with a biphasic expression profile during embryogenesis.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7520-4 PMID: 8052612
  24. LRG1 is expressed during sporulation in Saccharomyces cerevisiae and contains motifs similar to LIM and rho/racGAP domains.
    Nucleic Acids Res. 1994 Aug 11;22(15):3151-4 PMID: 8065929
  25. The LIM protein RBTN2 and the basic helix-loop-helix protein TAL1 are present in a complex in erythroid cells.
    Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8617-21 PMID: 8078932
  26. LIM domain recognition of a tyrosine-containing tight turn.
    J Biol Chem. 1994 Oct 7;269(40):25085-90 PMID: 7929196
  27. 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
  28. The LIM domain is a modular protein-binding interface.
    Cell. 1994 Oct 21;79(2):211-9 PMID: 7954790
  29. Muscle LIM protein, a novel essential regulator of myogenesis, promotes myogenic differentiation.
    Cell. 1994 Oct 21;79(2):221-31 PMID: 7954791
  30. The LIM domain: a new structural motif found in zinc-finger-like proteins.
    Trends Genet. 1994 Sep;10(9):315-20 PMID: 7974745
  31. Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila.
    Science. 1995 Feb 3;267(5198):688-93 PMID: 7839146
  32. SH2 and SH3 domains in signal transduction.
    Adv Cancer Res. 1994;64:87-110 PMID: 7533473
  33. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo.
    Nature. 1995 Mar 30;374(6521):464-7 PMID: 7700357
  34. Drosophila MEF2, a transcription factor that is essential for myogenesis.
    Genes Dev. 1995 Mar 15;9(6):730-41 PMID: 7729689
  35. Embryonic development of the larval body wall musculature of Drosophila melanogaster.
    Trends Genet. 1995 Apr;11(4):153-9 PMID: 7732594
  36. LIM domain proteins.
    C R Acad Sci III. 1995 Mar;318(3):295-306 PMID: 7788499
  37. The somatic-visceral subdivision of the embryonic mesoderm is initiated by dorsal gradient thresholds in Drosophila.
    Development. 1995 Jul;121(7):2107-16 PMID: 7635056
  38. Structure of the carboxy-terminal LIM domain from the cysteine rich protein CRP.
    Nat Struct Biol. 1994 Jun;1(6):388-98 PMID: 7664053
  39. The cysteine-rich protein family of highly related LIM domain proteins.
    J Biol Chem. 1995 Dec 1;270(48):28946-54 PMID: 7499425
  40. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  41. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  42. Are U4 small nuclear ribonucleoproteins involved in polyadenylation?
    Nature. 1984 May 10-16;309(5964):179-82 PMID: 6325940
  43. Identification of a new protein localized at sites of cell-substrate adhesion.
    J Cell Biol. 1986 Nov;103(5):1679-87 PMID: 3536951
  44. The function of PS integrins during Drosophila embryogenesis.
    Cell. 1989 Feb 10;56(3):401-8 PMID: 2492451
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1996-09-00
Pages
1179-95
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120973
Subset
IM
Grants
NIGMS NIH HHS · R01 GM050877 · United States
NIGMS NIH HHS · T32GM07464 · United States
NCI NIH HHS · CA42014 · United States
NIGMS NIH HHS · GM50877 · United States
Databases
GENBANK
X91244, X91245
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