Advertisement
Journal Articles
Muscle-specific functions of ryanodine receptor channels in Caenorhabditis elegans
E.B. Maryon, B. Saari, P. Anderson
Journal of Cell Science 1998 111: 2885-2895;

Summary

Ryanodine receptor channels regulate contraction of striated muscle by gating the release of calcium ions from the sarcoplasmic reticulum. Ryanodine receptors are expressed in excitable and non-excitable cells of numerous species, including the nematode C. elegans. Unlike vertebrates, which have at least three ryanodine receptor genes, C. elegans has a single gene encoded by the unc-68 locus. We show that unc-68 is expressed in most muscle cells, and that the phenotypic defects exhibited by unc-68 null mutants result from the loss of unc-68 function in pharyngeal and body-wall muscle cells. The loss of unc-68 function in the isthmus and terminal bulb muscles of the pharynx causes a reduction in growth rate and brood size. unc-68 null mutants exhibit defective pharyngeal pumping (feeding) and have abnormal vacuoles in the terminal bulb of the pharynx. unc-68 is required in body-wall muscle cells for normal motility. We show that UNC-68 is localized in body-wall muscle cells to flattened vesicular sacs positioned between the apical plasma membrane and the myofilament lattice. In unc-68 mutants, the vesicles are enlarged and densely stained. The flattened vesicles in body-wall muscle cells thus represent the C. elegans sarcoplasmic reticulum. Morphological and behavioral phenotypes of unc-68 mutants suggest that intracellular calcium release is not essential for excitation-contraction coupling in C. elegans.

REFERENCES

    1. Albertson D. G. and
    2. Thomson J. N.
    (1997). The pharynx of Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci 275, 299–325
    OpenUrl
    1. Avery L.
    (1993). The genetics of feeding in Caenorhabditis elegans. Genetics 133, 897–917
    OpenUrlAbstract/FREE Full Text
    1. Bennett D. L.,
    2. Cheek T. R.,
    3. Berridge M. J.,
    4. De Smedt H.,
    5. Parys J. B.,
    6. Missiaen L. and
    7. Bootman M. D.
    (1996). Expression and function of ryanodine receptors in nonexcitable cells. J. Biol. Chem 271, 6356–6362
    OpenUrlAbstract/FREE Full Text
    1. Berridge M. J.
    (1993). Inositol trisphosphate and calcium signalling. Nature 361, 315–325
    OpenUrlCrossRefPubMedWeb of Science
    1. Brenner S.
    (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71–94
    OpenUrlAbstract/FREE Full Text
    1. Bhat M. B.,
    2. Zhao J.,
    3. Takeshima H. and
    4. Ma J.
    (1997). Functional calcium release channel formed by the carboxyl-terminal portion of the ryanodine receptor. Biophys. J 73, 1329–1336
    OpenUrlCrossRefPubMedWeb of Science
    1. Block B. A.,
    2. O'Brien J. and
    3. Franck J.
    (1996). The role of ryanodine receptor isoforms in the structure and function of the vertebrate triad. Soc. Gen. Physiologists Series 51, 47–65
    OpenUrlPubMed
    1. Buck E. D.,
    2. Nguyen H. T.,
    3. Pessah I. N. and
    4. Allen P. D.
    (1997). Dyspedic mouse skeletal muscle expresses major elements of the triadic junction but lacks detectable ryanodine receptor protein and function. J. Biol. Chem 272, 7360–7367
    OpenUrlAbstract/FREE Full Text
    1. Callaway C.,
    2. Seryshev A.,
    3. Wang J. P.,
    4. Slavik K. J.,
    5. Needleman D. H.,
    6. Cantu C.,
    7. Wu J.,
    8. Jayaraman T.,
    9. Marks A. R. and
    10. Hamilton S. L.
    (1994). Localization of the high and low affinity 3H-ryanodine binding sites on the skeletal muscle Ca2+release channel. J. Biol. Chem 280, 15876–15884
    OpenUrl
    1. Carl S. L.,
    2. Felix K.,
    3. Caswell A. H.,
    4. Brandt N. R.,
    5. Ball W. J.,
    6. Vaghy P. L.,
    7. Meissner G. and
    8. Ferguson D. G.
    (1995). Immunolocalization of sarcolemmal dihydropyridine receptor and sarcoplasmic reticular triadin and ryanodine receptor in rabbit ventricle and atrium. J. Cell Biol 129, 673–682
    OpenUrlAbstract/FREE Full Text
    1. Caterall W. A.
    (1991). Excitation-contraction coupling in vertebrae skeletal muscle: a tale of two calcium channels. Cell 64, 871–874
    OpenUrlCrossRefPubMedWeb of Science
    1. Chalfie M.,
    2. Tu Y.,
    3. Euskirchen G.,
    4. Ward W. W. and
    5. Prasher D. C.
    (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802–805
    OpenUrlAbstract/FREE Full Text
    1. Clandinin T. R.,
    2. DeMondena J. A. and
    3. Sternberg P. W.
    (1998). Inositol trisphosphate mediates a RAS-independent response to LET-23 receptor tyrosine kinase activation in C. elegans. Cell 92, 523–533
    OpenUrlCrossRefPubMedWeb of Science
    1. Coronado R.,
    2. Morrissette J.,
    3. Sukhareva M. and
    4. Vaughan D. M.
    (1994). Structure and function of ryanodine receptors. Am. J. Physiol 94, 1485–1504
    OpenUrl
    1. Fabiato A.
    (1983). Calcium-induced release of calcium from the cardiac sarcplasmic reticulum. Am. J. Physiol 245, 1–.
    OpenUrlPubMed
    1. Fire A.,
    2. Harrison S. W. and
    3. Dixon D.
    (1990). A modular set of LacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene 93, 189–198
    OpenUrlCrossRefPubMedWeb of Science
    1. Francis G. R. and
    2. Waterston R. H.
    (1985). Muscle organization in Caenorhabditis elegan: localization of proteins implicated in thin filament attachment and I-band organization. J. Cell Biol 101, 1532–1549
    OpenUrlAbstract/FREE Full Text
    1. Franzini-Armstrong C. and
    2. Protasi F.
    (1997). Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol. Rev. 77, 699–729
    OpenUrlAbstract/FREE Full Text
    1. Gainer H.
    (1968). The role of calcium in excitation-contraction coupling of lobster muscle. J. Gen. Physiol 52, 88–110
    OpenUrlAbstract/FREE Full Text
    1. Györke S. and
    2. Palade P.
    (1992). Calcium-induced calcium release in crayfish skeletal muscle. J. Physiol 457, 195–210
    OpenUrlPubMedWeb of Science
    1. Hagiwara S. and
    2. Byerly L.
    (1981). Calcium channel. Annu. Rev. Neurosci 4, 69–125
    OpenUrlCrossRefPubMedWeb of Science
    1. Ikemoto T.,
    2. Komazaki S.,
    3. Takeshima H.,
    4. Nishi M.,
    5. Noda T.,
    6. Iino M. and
    7. Endo H.
    (1997). Functional and morphological features from mutant mice lacking both type 1 and type 3 ryanodine receptors. J. Physiol 501, 305–312
    OpenUrlCrossRefPubMedWeb of Science
    1. Kim Y. K.,
    2. Valdivia H. H.,
    3. Maryon E. B.,
    4. Anderson P. and
    5. Coronado R.
    (1992). High molecular weight proteins in the nematode C. elegans bind3H-ryanodine and form a large conductance channel. Biophys. J 63, 1379–1384
    OpenUrlCrossRefPubMedWeb of Science
    1. Lee R. Y. N.,
    2. Lobel L.,
    3. Hnegartner M.,
    4. Horvitz H. R. and
    5. Avery L.
    (1997). Mutations in the Alpha-1 subunit of an L-type voltage activated calcium channel cause myotonia in Caenorhabditis elegans. EMBO J 16, 6066–6076
    OpenUrlAbstract
    1. Maryon E. B.,
    2. Coronado R. and
    3. Anderson P.
    (1996). unc-68 encodes a ryanodine receptor involved in regulating C. elegans body-wall muscle contraction. J. Cell Biol 134, 885–893
    OpenUrlAbstract/FREE Full Text
    1. Muir S. R. and
    2. Sanders D.
    (1996). Pharmacology of Ca2+release from red beet microsomes suggests the presence of ryanodine receptor homologs in higher plants. FEBS Lett 395, 39–42
    OpenUrlCrossRefPubMedWeb of Science
    1. Nelson M. T.,
    2. Cheng H.,
    3. Rupart M.,
    4. Santana L. F.,
    5. Bonev A. D.,
    6. Knot H. J. and
    7. Lederer W. J.
    (1995). Relaxation of arterial smooth muscle by calcium sparks. Science 270, 633–636
    OpenUrlAbstract/FREE Full Text
    1. Rios E.,
    2. Ma J. and
    3. Gonzalez A.
    (1991). The mechanical hypothesis of excitation-contraction (EC) coupling in skeletal muscle. J. Muscle Res. Cell Motil 12, 127–135
    OpenUrlCrossRefPubMedWeb of Science
    1. Sakube Y.,
    2. Ando H. and
    3. Kagawa H.
    (1997). An abnormal ketamine response in mutants defective in the ryanodine receptor gene ryr-1 (unc-68) of Caenorhabditis elegans. J. Mol. Biol 267, 849–864
    OpenUrlCrossRefPubMedWeb of Science
    1. Seok J. H.,
    2. Xu L.,
    3. Kramarcy N. R.,
    4. Sealock R. and
    5. Meissner G.
    (1992). The 30S lobster skeletal calcium release channel (ryanodine receptor) has functional properties distinct from the mammalian channel proteins. J. Biol. Chem 267, 15893–15901
    OpenUrlAbstract/FREE Full Text
    1. Sutko J. L. and
    2. Airey J. A.
    (1996). Ryanodine receptor Ca2+ release channels: does diversity in form equal diversity in function?. Physiol. Rev. 76, 1027–71
    OpenUrlAbstract/FREE Full Text
    1. Takeshima H.,
    2. Lino M.,
    3. Takekura H.,
    4. Nishi M.,
    5. Kuno J.,
    6. Minowa O.,
    7. Takano H. and
    8. Noda T.
    (1994). Excitation-contraction uncoupling and muscular degeneration in mice lacking functional skeletal muscle ryanodine-receptor gene. Nature 369, 556–559
    OpenUrlCrossRefPubMedWeb of Science
    1. Takeshima H.,
    2. Yamazawa T.,
    3. Ikemoto T.,
    4. Takekura H.,
    5. Nishi M.,
    6. Noda T. and
    7. Iino M.
    (1995). Ca(2+)-induced Ca2+ release in myocytes from dyspedic mice lacking the type-1 ryanodine receptor. EMBO J 14, 2999–3006
    OpenUrlPubMedWeb of Science
    1. Takeshima H.,
    2. Ikemoto T.,
    3. Nishi M.,
    4. Nishiyama N.,
    5. Shimuta M.,
    6. Sugutani Y.,
    7. Kuno J.,
    8. Saito I.,
    9. Saito H.,
    10. Endo M. and
    11. et al.
    (1996). Generation and characterization of mutant mice lacking ryanodine receptor type 3. J. Biol. Chem 271, 19649–19652
    OpenUrlAbstract/FREE Full Text
    1. Wagenknecht T. and
    2. Radermacher M.
    (1995). Three-dimensional architecture of the skeletal muscle ryanodine receptor. FEBS Lett 369, 43–46
    OpenUrlCrossRefPubMedWeb of Science
    1. Weisblat D. A.,
    2. Byerly L. and
    3. Russell R. L.
    (1976). Ionic mechanisms of electrical activity in somatic muscle of the nematode Ascaris lumbricoides. J. Comp. Physiol 111, 93–113
    OpenUrlCrossRef
    1. Williams B. D. and
    2. Waterston R. H.
    (1994). Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J. Cell Biol 124, 475–490
    OpenUrlAbstract/FREE Full Text
Back to top

 Download PDF

Email
Journal Articles
Muscle-specific functions of ryanodine receptor channels in Caenorhabditis elegans
E.B. Maryon, B. Saari, P. Anderson
Journal of Cell Science 1998 111: 2885-2895;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Introducing FocalPlane’s new Community Manager, Esperanza Agullo-Pascual

We are pleased to welcome Esperanza to the Journal of Cell Science team. The new Community Manager for FocalPlane, Esperanza is joining us from the Microscopy Core at Mount Sinai School of Medicine. Find out more about Esperanza in her introductory post over on FocalPlane.

New funding scheme supports sustainable events

As part of our Sustainable Conferencing Initiative, we are pleased to announce funding for organisers that seek to reduce the environmental footprint of their event. The next deadline to apply for a Scientific Meeting grant is 26 March 2021.

Read & Publish participation continues to grow

"Alongside pre-printing for early documentation of work, such mechanisms are particularly helpful for early-career researchers like me.”

Dr Chris MacDonald (University of York) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 150 institutions in 15 countries and four library consortia taking part – find out more and view our full list of participating institutions.

Cell scientist to watch: Romain Levayer

In an interview, Romain Levayer talks about starting his own lab, his love for preprints and his experience of balancing parenting with his research goals.

Live lactating mammary tissue

In a stunning video, Stewart et al. demonstrate warping of the alveolar unit due to basal cell-generated force as part of their recent work investigating roles for mechanically activated ion channels in lactation and involution.

Visit our YouTube channel to watch more videos from JCS, our sister journals and the Company.

JCS and COVID-19

For more information on measures Journal of Cell Science is taking to support the community during the COVID-19 pandemic, please see here.

If you have any questions or concerns, please do not hestiate to contact the Editorial Office.