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PMID: 10811919 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The ryanodine receptor is essential for larval development in Drosophila melanogaster.

Sullivan KM, Scott K, Zuker CS, Rubin GM

Abstract

We have investigated the role of the ryanodine receptor in Drosophila development by using pharmacological and genetic approaches. We identified a P element insertion in the Drosophila ryanodine receptor gene, Ryanodine receptor 44F (Ryr), and used it to generate the hypomorphic allele Ryr(16). An examination of hypodermal, visceral, and circulatory muscle showed that, in each case, muscle contraction was impaired in Ryr(16) larvae. Treatment with the drug ryanodine, a highly specific modulator of ryanodine receptor channel activity, also inhibited muscle function, and, at high levels, completely blocked hypodermal muscle contraction. These results suggest that the ryanodine receptor is required for proper muscle function and may be essential for excitation-contraction coupling in larval body wall muscles. Nonmuscle roles of Ryr were also investigated. Ryanodine-sensitive Ca(2+) stores had previously been implicated in phototransduction; to address this, we generated Ryr(16) mutant clones in the adult eye and performed whole-cell, patch-clamp recordings on dissociated ommatidia. Our results do not support a role for Ryr in normal light responses.

MeSH Terms
Alleles Animals Calcium Signaling/physiology DNA Transposable Elements Drosophila melanogaster/growth & development,metabolism Gastrointestinal Motility In Situ Hybridization, Fluorescence Larva Muscle Contraction Muscle Development Myocardial Contraction Patch-Clamp Techniques Polymerase Chain Reaction Ryanodine/pharmacology Ryanodine Receptor Calcium Release Channel/deficiency,drug effects,genetics,physiology
Chemicals
DNA Transposable Elements Ryanodine Receptor Calcium Release Channel Ryanodine
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sullivan K M
Howard Hughes Medical Institute and Department of Molecular and Cell Biology, University of California, Berkeley, CA 94702, USA. [email protected]
Scott K
Zuker C S
Rubin G M
References (28)
28 references, click to expand
  1. Cyclic ADP-ribose, the ryanodine receptor and Ca2+ release.
    Trends Pharmacol Sci. 1995 Nov;16(11):386-91 PMID: 8578608
  2. Pharmacological analysis of heartbeat in Drosophila.
    J Neurobiol. 1995 Nov;28(3):269-80 PMID: 8568510
  3. Spontaneous avoidance behavior in Drosophila null for calmodulin expression.
    Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2420-5 PMID: 8637889
  4. Ryanodine receptor Ca2+ release channels: does diversity in form equal diversity in function?
    Physiol Rev. 1996 Oct;76(4):1027-71 PMID: 8874493
  5. Calmodulin regulation of calcium stores in phototransduction of Drosophila.
    Science. 1997 Feb 21;275(5303):1119-21 PMID: 9027311
  6. InsP3 receptor is essential for growth and differentiation but not for vision in Drosophila.
    Neuron. 1997 Jun;18(6):881-7 PMID: 9208856
  7. Functional calcium release channel formed by the carboxyl-terminal portion of ryanodine receptor.
    Biophys J. 1997 Sep;73(3):1329-36 PMID: 9284301
  8. Requirement for the ryanodine receptor type 3 for efficient contraction in neonatal skeletal muscles.
    EMBO J. 1997 Dec 1;16(23):6956-63 PMID: 9384575
  9. Embryonic lethality and abnormal cardiac myocytes in mice lacking ryanodine receptor type 2.
    EMBO J. 1998 Jun 15;17(12):3309-16 PMID: 9628868
  10. Divergent roles for NK-2 class homeobox genes in cardiogenesis in flies and mice.
    Development. 1998 Aug;125(16):3037-48 PMID: 9671578
  11. Muscle-specific functions of ryanodine receptor channels in Caenorhabditis elegans.
    J Cell Sci. 1998 Oct;111 ( Pt 19):2885-95 PMID: 9730981
  12. Calcium--a life and death signal.
    Nature. 1998 Oct 15;395(6703):645-8 PMID: 9790183
  13. Targeted disruption of gene function in Drosophila by RNA interference (RNA-i): a role for nautilus in embryonic somatic muscle formation.
    Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1451-6 PMID: 9990044
  14. Cell-autonomous and non-autonomous growth-defective mutants of Drosophila melanogaster.
    Development. 1999 Jun;126(11):2365-75 PMID: 10225996
  15. Cloning and characterization of peter pan, a novel Drosophila gene required for larval growth.
    Mol Biol Cell. 1999 Jun;10(6):1733-44 PMID: 10359593
  16. Deletion of the ryanodine receptor type 3 (RyR3) impairs forms of synaptic plasticity and spatial learning.
    EMBO J. 1999 Oct 1;18(19):5264-73 PMID: 10508160
  17. Atypical intestinal striated muscle in Drosophila melanogaster.
    J Ultrastruct Res. 1967 Jun;18(5):695-702 PMID: 6027107
  18. Striated visceral muscle of drosophila melanogaster.
    J Morphol. 1971 Jul;134(3):315-34 PMID: 4999727
  19. Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum.
    J Biol Chem. 1986 May 15;261(14):6300-6 PMID: 2422165
  20. 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
  21. The ryanodine receptor-Ca2+ release channel complex of skeletal muscle sarcoplasmic reticulum. Evidence for a cooperatively coupled, negatively charged homotetramer.
    J Biol Chem. 1989 Oct 5;264(28):16776-85 PMID: 2550460
  22. A Drosophila mutant defective in extracellular calcium-dependent photoreceptor deactivation and rapid desensitization.
    Nature. 1991 Nov 21;354(6350):230-2 PMID: 1961249
  23. Drosophila homologs of two mammalian intracellular Ca(2+)-release channels: identification and expression patterns of the inositol 1,4,5-triphosphate and the ryanodine receptor genes.
    Development. 1992 Dec;116(4):967-75 PMID: 1338312
  24. Analysis of genetic mosaics in developing and adult Drosophila tissues.
    Development. 1993 Apr;117(4):1223-37 PMID: 8404527
  25. Isolation and characterization of a gene for a ryanodine receptor/calcium release channel in Drosophila melanogaster.
    FEBS Lett. 1994 Jan 3;337(1):81-7 PMID: 8276118
  26. Autosomal P[ovoD1] dominant female-sterile insertions in Drosophila and their use in generating germ-line chimeras.
    Development. 1993 Dec;119(4):1359-69 PMID: 8306893
  27. Excitation-contraction uncoupling and muscular degeneration in mice lacking functional skeletal muscle ryanodine-receptor gene.
    Nature. 1994 Jun 16;369(6481):556-9 PMID: 7515481
  28. Gene disruptions using P transposable elements: an integral component of the Drosophila genome project.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):10824-30 PMID: 7479892
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
Published
2000-05-23
Pages
5942-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC18538
Subset
IM
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