In vivo single-molecule imaging identifies altered dynamics of calcium channels in dystrophin-mutant C. elegans

Nature Communications

Volumn 5, Issue , 2014, Pages

  Zhan, Hong ^a   Stanciauskas, Ramunas ^b   Stigloher, Christian ^c   Dizon, Kevin K ^b   Jospin, Maelle ^a   Bessereau, Jean Louis ^a   Pinaud, Fabien ^b  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; DYSTROPHIN; GREEN FLUORESCENT PROTEIN; VOLTAGE GATED CALCIUM CHANNEL; CAENORHABDITIS ELEGANS PROTEIN; CALCIUM; CALCIUM CHANNEL; HYBRID PROTEIN; MEMBRANE PROTEIN;

CALCIUM; CELL ORGANELLE; HOMEOSTASIS; MEMBRANE; MOLECULAR ANALYSIS; MUTATION; NEMATODE; PROTEIN; RESOLUTION; TECHNOLOGICAL CHANGE;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL MEMBRANE; CELL SURFACE; COMPLEMENTATION ACTIVATED LIGHT MICROSCOPY; CONTROLLED STUDY; DENSE BODY; EXTRACELLULAR MATRIX; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; IN VITRO STUDY; IN VIVO STUDY; LOCOMOTION; MICROSCOPY; MOLECULAR IMAGING; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE TONE; MUSCULAR DYSTROPHY; NEUROMUSCULAR SYNAPSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SARCOLEMMA; SINGLE MOLECULE FLUORESCENCE MICROSCOPY; ANIMAL; DIFFUSION; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; HOMEOSTASIS; METABOLISM; MUTATION;

ANIMALIA; CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM; CALCIUM CHANNELS; CELL MEMBRANE; DIFFUSION; DYSTROPHIN; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; HOMEOSTASIS; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MUTATION; RECOMBINANT FUSION PROTEINS; SARCOLEMMA;

EID: 84923306785     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5974     Document Type: Article

References (62)

1. Lord, S. J., Lee, H. L. & Moerner, W. E. Single-molecule spectroscopy and imaging of biomolecules in living cells. Anal. Chem. 82, 2192-2203 (2010).
2. Schaaf, M. J.M. et al. Single-molecule microscopy reveals membrane microdomain organization of cells in a living vertebrate. Biophys. J. 97, 1206-1214 (2009).
3. Shi, X. et al. Determination of dissociation constants in living zebrafish embryos with single wavelength fluorescence cross-correlation spectroscopy. Biophys. J. 97, 678-686 (2009).
4. Ries, J., Yu, S. R., Burkhardt, M., Brand, M. & Schwille, P. Modular scanning FCS quantifies receptor-ligand interactions in living multicellular organisms. Nat. Methods 6, 643-U631 (2009).
5. Petrasek, Z. et al. Characterization of Protein Dynamics in Asymmetric Cell Division by Scanning Fluorescence Correlation Spectroscopy. Biophys. J. 95, 5476-5486 (2008).
6. Robin, F. B., McFadden, W. M., Yao, B. & Munro, E. M. Single-molecule analysis of cell surface dynamics in Caenorhabditis elegans embryos. Nat. Methods 11, 677-682 (2014).
7. Tokunaga, M., Imamoto, N. & Sakata-Sogawa, K. Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat. Methods 5, 159-161 (2008).
8. Ritter, J. G., Veith, R., Veenendaal, A., Siebrasse, J. P. & Kubitscheck, U. Light sheet microscopy for single molecule tracking in living tissue. PLoS ONE 5, e11639 (2010).
9. Cella Zanacchi, F. et al. Live-cell 3D super-resolution imaging in thick biological samples. Nat. Methods 8, 1047-1049 (2011).
10. Stepanenko, O. V. et al. Modern fluorescent proteins: from chromophore formation to novel intracellular applications. Biotechniques 51, 313 (2011).
11. Yano, Y. & Matsuzaki, K. Tag-probe labeling methods for live-cell imaging of membrane proteins. Biochim. Biophys. Acta 1788, 2124-2131 (2009).
12. Pinaud, F. & Dahan, M. Targeting and imaging single biomolecules in living cells by complementation-activated light microscopy with split-fluorescent proteins. Proc. Natl Acad. Sci. USA 108, E201-E210 (2011).
13. Mathews, E. A. et al. Critical residues of the Caenorhabditis elegans unc-2 voltage-gated calcium channel that affect behavioral and physiological properties. J. Neurosci. 23, 6537-6545 (2003).
14. Gao, S. & Zhen, M. Action potentials drive body wall muscle contractions in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 108, 2557-2562 (2011).
15. Sancar, F. et al. The dystrophin-associated protein complex maintains muscle excitability by regulating Ca2+-dependent K+ (BK) channel localization. J. Biol. Chem. 286, 33501-33510 (2011).
16. Feinberg, E. H. et al. GFP reconstitution across synaptic partners (GRASP) defines cell contacts and Synapses in living nervous systems. Neuron 57, 353-363 (2008).
17. Schutz, G. J., Schindler, H. & Schmidt, T. Single-molecule microscopy on model membranes reveals anomalous diffusion. Biophys. J. 73, 1073-1080 (1997).
18. Simson, R. et al. Structural mosaicism on the submicron scale in the plasma membrane. Biophys. J. 74, 297-308 (1998).
19. Stuhmer, W. & Almers, W. Photobleaching through glass micropipettes: sodium channels without lateral mobility in the sarcolemma of frog skeletal muscle. Proc. Natl Acad. Sci. USA 79, 946-950 (1982).
20. Saheki, Y. & Bargmann, C. I. Presynaptic CaV2 calcium channel traffic requires CALF-1 and the alpha(2)delta subunit UNC-36. Nat. Neurosci. 12, 1257-1265 (2009).
21. Laine, V., Frokjaer-Jensen, C., Couchoux, H. & Jospin, M. The alpha 1 Subunit EGL-19, the alpha 2/delta subunit UNC-36, and the beta subunit CCB-1 underlie voltage-dependent calcium currents in Caenorhabditis elegans striated muscle. J. Biol. Chem. 286, 36180-36187 (2011).
22. Frokjaer-Jensen, C. et al. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 40, 1375-1383 (2008).
23. Davies, A. et al. The alpha2delta subunits of voltage-gated calcium channels form GPI-anchored proteins, a posttranslational modification essential for function. Proc. Natl Acad. Sci. USA 107, 1654-1659 (2010).
24. Altun, Z. F. & Hall, D. H. Muscle system, introduction, in WormAtlas (2009).
25. Street, S. F. Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J. Cell Physiol. 114, 346-364 (1983).
26. Ervasti, J. M. Costameres: the Achilles' heel of Herculean muscle. J. Biol. Chem. 278, 13591-13594 (2003).
27. Le Rumeur, E., Winder, S. J. & Hubert, J. F. Dystrophin: more than just the sum of its parts. Biochim. Biophys. Acta 1804, 1713-1722 (2010).
28. Lansman, J. B. & Franco, A. What does dystrophin do in normal muscle. Journal of Muscle Research and Cell Motility 12, 409-411 (1991).
29. Kumar, A., Khandelwal, N., Malya, R., Reid, M. B. & Boriek, A. M. Loss of dystrophin causes aberrant mechanotransduction in skeletal muscle fibers. FASEB J. 18, 102-113 (2004).
30. Zsnagy, I., Zhang, X., Kitani, K. & Nonomura, Y. The influence of dystrophin on lateral diffusion of proteins in sarcolemma of L-185 and C2 myoblasts and mature striated-muscle cells of rats and mice, as measured by FRAP technique. Biochim. Biophys. Res. Commun. 215, 67-74 (1995).
31. Sarkis, J. et al. Resisting sarcolemmal rupture: dystrophin repeats increase membrane-actin stiffness. FASEB J. 27, 359-367 (2013).
32. Dickinson, D. J., Ward, J. D., Reiner, D. J. & Goldstein, B. Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat. Methods 10, 1028 (2013).
33. Robert, V. J. & Bessereau, J. L. Genome engineering by transgene-instructed gene conversion in C. elegans. Methods Cell Biol. 106, 65-88 (2011).
34. Best, J. M. & Kamp, T. J. Different subcellular populations of L-type Ca2+ channels exhibit unique regulation and functional roles in cardiomyocytes. J. Mol. Cell. Cardiol. 52, 376-387 (2012).
35. Balijepalli, R. C., Foell, J. D., Hall, D. D., Hell, J. W. & Kamp, T. J. Localization of cardiac L-type Ca(2+) channels to a caveolar macromolecular signaling complex is required for beta(2)-adrenergic regulation. Proc. Natl Acad. Sci. USA 103, 7500-7505 (2006).
36. Suzuki, Y., Yamamura, H., Ohya, S. & Imaizumi, Y. Caveolin-1 facilitates the direct coupling between large conductance Ca2+-activated K+ (BKCa) and Cav1.2 Ca2+ channels and their clustering to regulate membrane excitability in vascular myocytes. J. Biol. Chem. 288, 36750-36761 (2013).
37. Tang, Z. et al. Identification, sequence, and expression of an invertebrate caveolin gene family from the nematode Caenorhabditis elegans. Implications for the molecular evolution of mammalian caveolin genes. J. Biol. Chem. 272, 2437-2445 (1997).
38. Kirkham, M. et al. Evolutionary analysis and molecular dissection of caveola biogenesis. J. Cell Sci. 121, 2075-2086 (2008).
39. Head, B. P. & Insel, P. A. Do caveolins regulate cells by actions outside of caveolae? Trends Cell Biol. 17, 51-57 (2007).
40. Lingwood, D. & Simons, K. Lipid Rafts as a membrane-organizing principle. Science 327, 46-50 (2010).
41. Rao, W., Isaac, R. E. & Keen, J. N. An analysis of the Caenorhabditis elegans lipid raft proteome using geLC-MS/MS. J. Proteomics 74, 242-253 (2011).
42. Davies, A. et al. The calcium channel alpha2delta-2 subunit partitions with CaV2.1 into lipid rafts in cerebellum: implications for localization and function. J. Neurosci. 26, 8748-8757 (2006).
43. Pinaud, F. et al. Dynamic partitioning of a glycosyl-phosphatidylinositolanchored protein in glycosphingolipid-rich microdomains imaged by single-quantum dot tracking. Traffic 10, 691-712 (2009).
44. Tadross, M. R., Tsien, R. W. & Yue, D. T. Ca2+ channel nanodomains boost local Ca2+ amplitude. Proc. Natl Acad. Sci. USA 110, 15794-15799 (2013).
45. Maryon, E. B., Saari, B. & Anderson, P. Muscle-specific functions of ryanodine receptor channels in Caenorhabditis elegans. J. Cell Sci. 111(Pt 19): 2885-2895 (1998).
46. Maryon, E. B., Coronado, R. & Anderson, P. unc-68 encodes a ryanodine receptor involved in regulating C. elegans body-wall muscle contraction. J. Cell biol. 134, 885-893 (1996).
47. Robertson, A. P., Clark, C. L. & Martin, R. J. Levamisole and ryanodine receptors. I: A contraction study in Ascaris suum. Mol. Biochem. Parasitol. 171, 1-7 (2010).
48. Berkefeld, H. et al. BKCa-Cav channel complexes mediate rapid and localized Ca2+-activated K+ signaling. Science 314, 615-620 (2006).
49. Kim, H. et al. The dystrophin complex controls bk channel localization and muscle activity in Caenorhabditis elegans. PLoS Genet. 5, e1000780 (2009).
50. Bessou, C., Giugia, J. B., Franks, C. J., Holden-Dye, L. & Segalat, L. Mutations in the Caenorhabditis elegans dystrophin-like gene dys-1 lead to hyperactivity and suggest a link with cholinergic transmission. Neurogenetics 2, 61-72 (1998).
51. Allard, B. Sarcolemmal ion channels in dystrophin-deficient skeletal muscle fibres. J. Muscle Res. Cell Motil. 27, 367-373 (2006).
52. Berchtold, M. W., Brinkmeier, H. & Muntener, M. Calcium ion in skeletal muscle: Its crucial role for muscle function, plasticity, and disease. Physiol. Rev. 80, 1215-1265 (2000).
53. Laine, V., Frokjaer-Jensen, C., Couchoux, H. & Jospin, M. The alpha1 subunit EGL-19, the alpha2/delta subunit UNC-36, and the beta subunit CCB-1 underlie voltage-dependent calcium currents in Caenorhabditis elegans striated muscle. J. Biol. Chem. 286, 36180-36187 (2011).
54. Gally, C. & Bessereau, J. L. GABA is dispensable for the formation of junctional GABA receptor clusters in Caenorhabditis elegans. J. Neurosci. 23, 2591-2599 (2003).
55. Francis, G. R. & Waterston, R. H. Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J. Cell Biol. 101, 1532-1549 (1985).
56. Gottschalk, A. & Schafer, W. R. Visualization of integral and peripheral cell surface proteins in live Caenorhabditis elegans. J. Neurosci.Methods 154, 68-79 (2006).
57. Kim, E., Sun, L., Gabel, C. V. & Fang-Yen, C. Long-term imaging of Caenorhabditis elegans using nanoparticle-mediated immobilization. PLoS ONE 8, e53419 (2013).
58. Serge, A., Bertaux, N., Rigneault, H. & Marguet, D. Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes. Nat. Methods 5, 687-694 (2008).
59. Thompson, R. E., Larson, D. R. & Webb, W. W. Precise nanometer localization analysis for individual fluorescent probes. Biophys. J. 82, 2775-2783 (2002).
60. Qian, H., Sheetz, M. P. & Elson, E. L. Single-particle tracking-analysis of diffusion and flow in 2-dimensional systems. Biophys. J. 60, 910-921 (1991).
61. Perry, G. L.W. SpPack: spatial point pattern analysis in Excel using Visual Basic for Applications (VBA). Environ. Model. Software 19, 559-569 (2004).
62. Moerman, D. G. & Williams, B. D. Sarcomere assembly in C. elegans muscle. WormBook : the online review of C. elegans biology 1-16 (2006).