Application of complementary luminescent and fluorescent imaging techniques to visualize nuclear and cytoplasmic Ca 2+ signalling during the in vivo differentiation of slow muscle cells in zebrafish embryos under normal and dystrophic conditions

Clinical and Experimental Pharmacology and Physiology

Volumn 39, Issue 1, 2012, Pages 78-86

  Webb, Sarah E ^a   Cheung, Chris C Y ^b   Chan, Ching Man ^a   Love, Donald R ^c   Miller, Andrew L ^a,d  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

Aequorin; Ca 2+ signalling; Dystrophin; Sapje mutant; Slow muscle cell; Zebrafish

Indexed keywords

AEQUORIN; CALCIUM ION; DEXTRAN; DYSTROPHIN; TRANSCRIPTION FACTOR SP1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM SIGNALING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DUCHENNE MUSCULAR DYSTROPHY; EMBRYO; FLUORESCENCE IMAGING; IN VIVO STUDY; LUMINESCENCE; MORPHOLOGY; MUSCLE DEVELOPMENT; MUTANT; MYOTOME; NONHUMAN; SARCOMERE; SLOW MUSCLE FIBER; TRANSGENIC ANIMAL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALCIUM SIGNALING; CELL NUCLEUS; CYTOPLASM; EMBRYONIC DEVELOPMENT; LUMINESCENT MEASUREMENTS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MORPHOLINOS; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE PROTEINS; MUSCULAR DYSTROPHIES; MUTATION; ORGAN SPECIFICITY; PROTEIN TRANSPORT; SARCOMERES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84855180012     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/j.1440-1681.2011.05582.x     Document Type: Article

References (62)

1. Flucher BE, Andrews SB. Characterization of spontaneous and action potential-induced calcium transients in developing myotubes in vitro. Cell Motil. Cytoskeleton 1993; 25: 143-57.
2. Ferrari MB, Rohrbough J, Spitzer NC. Spontaneous calcium transients regulate myofibrillogenesis in embryonic Xenopus myocytes. Dev. Biol. 1996; 178: 484-97.
3. Lorenzon P, Giovannelli A, Ragozzino D, Eusebi F, Ruzzier F. Spontaneous and repetitive calcium transients in C2C12 mouse myotubes during in vivo myogenesis. Eur. J. Neurosci. 1997; 9: 800-8.
4. Ferrari MB, Spitzer NC. Calcium signaling in the developing Xenopus myotome. Dev. Biol. 1999; 213: 269-82.
5. 2+ signaling pathway in skeletal muscle. J. Cell Sci. 2001; 114: 3673-83.
6. Li H, Cook JD, Terry M, Spitzer NG, Ferrari MB. Calcium transients regulate patterned actin assembly during myofibrillogenesis. Dev. Dyn. 2004; 229: 231-42.
7. Brennan C, Mangoli M, Dyer CEF, Ashworth R. Acetylcholine and calcium signaling regulates muscle fibre formation in the zebrafish embryo. J. Cell Sci. 2005; 118: 5181-90.
8. Campbell NR, Podugu SP, Ferrari MB. Spatiotemporal characterization of short versus long duration calcium transients in embryonic muscle and their role in myofibrillogenesis. Dev. Biol. 2006; 292: 253-64.
9. Fujita H, Nedachi T, Kanzaki M. Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes. Exp. Cell Res. 2007; 313: 1853-65.
10. Berchtold MW, Brinkmeier H, Müntener M. Calcium ion in skeletal muscle. Its crucial role for muscle function, plasticity, and disease. Physiol. Rev. 2000; 80: 1215-65.
11. Ferrari MB, Podugu S, Eskew JD. Assembling the myofibril: coordinating contractile cable construction with calcium. Cell Biochem. Biophys. 2006; 45: 317-37.
12. 2+/calmodulin-dependent transcriptional pathways: potential mediators of skeletal muscle growth and development. Biol. Rev. 2009; 84: 637-52.
13. 2+ signaling during embryonic skeletal muscle formation in vertebrates. Cold Spring Harb. Perspect Biol. 2010; doi:.
14. 2+ signals in muscle cells are involved in regulation of gene expression. Biol. Res. 2002; 35: 195-202.
15. 2+ signaling during the development of slow muscle cells in intact zebrafish embryos. Int. J. Dev. Biol. 2011; 55: 153-74.
16. Weinberg ES, Allende ML, Kelly CS et al. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development 1996; 122: 271-80.
17. Brennan C, Amacher SL, Currie PD. Aspects of organogenesis: somitogenesis. Results Probl. Cell Differ. 2002; 40: 271-97.
18. Ochi H, Westerfield M. Signaling networks that regulate muscle development: lessons from zebrafish. Dev. Growth Differ. 2007; 49: 1-11.
19. Blagden CS, Currie PD, Ingham PW, Hughes SM. Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. Genes Dev. 1997; 11: 2163-75.
20. Devoto SH, Melançon E, Eisen JS, Westerfield M. Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 1996; 122: 3371-780.
21. Barresi MJ, D'Angelo JA, Hernández LP, Devoto SH. Distinct mechanisms regulate slow-muscle development. Curr. Biol. 2001; 11: 1432-8.
22. Du SJ, Devoto SH, Westerfield M, Moon RT. Positive and negative regulation of muscle cell identity by members of the hedgehog and TGF-β gene families. J. Cell Biol. 1997; 139: 145-56.
23. Myers PZ, Eisen JS, Westerfield M. Development and axonal outgrowth of identified motoneurons in the zebrafish. J. Neurosci. 1986; 6: 2278-89.
24. Liu DW, Westerfield M. Clustering of muscle acetylcholine receptors requires motoneurons in live embryos, but not in cell culture. J. Neurosci. 1992; 12: 1859-66.
25. Saint-Amant L, Drapeau P. Time course of the development of motor behaviors in the zebrafish embryo. J. Neurobiol. 1998; 37: 622-32.
26. 2+ indicators, yellow Cameleon-Nano. Nat. Methods 2010; 7: 729-32.
27. Barresi MJ, Stickney HL, Devoto S. The zebrafish slow-muscle-omitted gene product is required for Hedgehog signal transduction and the development of slow muscle identity. Development 2000; 127: 2189-99.
28. Chen JK, Taipale J, Cooper MK, Beachy PA. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 2002; 16: 2743-8.
29. Claflin DR, Brooks SV. Direct observation of failing fibers in muscles of dystrophic mice provides mechanistic insight into muscular dystrophy. Am. J. Physiol. Cell Physiol. 2008; 294: C651-8.
30. Chambers SP, Anderson LV, Maguire GM, Dodd A, Love DR. Sarcoglycans of the zebrafish. Orthology and localization to the sarcolemma and myosepta of muscle. Biochem. Biophys. Res. Commun. 2003; 303: 488-95.
31. Bassett DI, Bryson-Richardson RJ, Daggett DF, Gautier P, Keenan DG, Currie PD. Dystrophin is required for the formation of stable muscle attachments in the zebrafish embryo. Development 2003; 130: 5851-60.
32. Guyon JR, Mosley AN, Zhou Y et al. The dystrophin associated protein complex in zebrafish. Hum. Mol. Genet. 2003; 12: 601-15.
33. Alderton JM, Steinhardt RA. Calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. J. Biol. Chem. 2000; 275: 9452-60.
34. + channels. Proc. Natl Acad. Sci. USA 2000; 97: 4950-5.
35. Robert V, Massimino ML, Tosello V, Cantini M, Sorrentino V, Pozzan T. Alteration in calcium handling at the subcellular level in mdx myotubes. J. Biol. Chem. 2001; 276: 4647-51.
36. Vandebrouck C, Martin D, Colson-Van Schoor M, Debaix H, Gailly P. Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J. Cell Biol. 2002; 158: 1089-96.
37. Basset O, Boittin F-X, Dorchies OM, Chatton J-Y, van Breemen C, Ruegg UT. Involvement of inositol 1, 4, 5-trisphosphate in nicotinic calcium responses in dystrophic myotubes assessed by near-plasma membrane calcium measurement. J. Biol. Chem. 2004; 179: 47092-100.
38. Basset O, Boittin F-X, Cognard C, Constantin B, Ruegg UT. Bcl-2 overexpression prevents calcium overload and subsequent apoptosis in dystrophic myotubes. Biochem. J. 2006; 395: 267-76.
39. 2+ entry into dystrophic skeletal muscle fibres. Biochem. Biophys. Res. Commun. 2010; 391: 401-6.
40. Cárdenas C, Juretić N, Bevilacqua JA et al. Abnormal distribution of inositol 1, 4, 5-trisphosphate receptors in human muscle can be related to altered calcium signals and gene expression in Duchenne dystrophy-derived cells. FASEB J. 2010; 24: 3210-21.
41. 2+ homeostasis during fatigue. Exp. Physiol. 2010; 95: 641-56.
42. Dodd A, Greenwood DR, Miller AL et al. Zebrafish: at the nexus of functional and chemical genetics. Biotechnol. Genet. Eng. Rev. 2006; 22: 77-99.
43. Westerfield M. The Zebrafish Book: a Guide for the Laboratory Use of Zebrafish (Brachydanio rerio). University of Oregon Press, Eugene. 1994.
44. Webb SE, Lee KW, Karplus E, Miller AL. Localized calcium transients accompany furrow positioning, propagation, and deepening during the early cleavage period of zebrafish embryos. Dev. Biol. 1997; 192: 78-92.
45. Cheung CY, Webb SE, Meng A, Miller AL. Transient expression of apoaequorin in zebrafish embryos. Extending the ability to image calcium transients during later stages of development. Int. J. Dev. Biol. 2006; 50: 561-9.
46. i with aequorin using a photon imaging detector. In: Nuccitelli R (ed.). Methods in Cell Biology, vol. 40. Academic Press, Orlando. 1994; 305-38.
47. 2+ dynamics: from subcellular microdomains to whole organisms. Methods Cell Biol. 2010; 99: 263-300.
48. Klar TA, Jakobs S, Dyba M, Egner A, Hell SW. Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc. Natl Acad. Sci. USA 2000; 97: 8206-10.
49. Créton R, Speksnijder JE, Jaffe LF. Patterns of free calcium in zebrafish embryos. J. Cell Sci. 1998; 111: 1613-22.
50. Webb SE, Miller AL. Calcium signaling during zebrafish embryonic development. Bioessays 2000; 22: 113-23.
51. Ashworth R, Bolsover SR. Spontaneous activity-independent intracellular calcium signals in the developing spinal cord of the zebrafish embryo. Dev. Brain Res. 2002; 139: 131-7.
52. 2+ signals in cultured skeletal muscle. Am. J. Physiol. Cell Physiol. 2000; 278: C998-1010.
53. Carrasco MA, Riveros N, Ríos J et al. Depolarization-induced slow calcium transients activate early genes in skeletal muscle cells. Am. J. Physiol. Cell Physiol. 2003; 284: C1438-47.
54. 2+ transients and modulate cAMP response element binding protein phosphorylation. J. Cell Sci. 2005; 118: 3131-40.
55. Blake DJ, Weir A, Newey SE, Davis KE. Function and genetics of dystropin and dystrophin-related proteins in muscle. Physiol. Rev. 2002; 82: 291-329.
56. 2+ signals in the formed somites during the early segmentation period in intact, normally developing zebrafish embryos. Dev. Growth Differ. 2009; 51: 617-37.
57. Guyon JR, Goswami J, Jun SJ et al. Genetic isolation and characterization of a splicing mutant of zebrafish dystrophin. Hum. Mol. Genet. 2009; 18: 202-11.
58. Chambers SP, Dodd A, Overall R et al. Dystrophin in adult zebrafish muscle. Biochem. Biophys. Res. Commun. 2001; 286: 478-83.
59. Berger J, Berker S, Hall TE, Lieschke GJ, Currie PD. Dystrophin-deficient zebrafish feature aspects of the duchenne muscular dystrophy pathology. Neuromusc. Disord. 2010; 20: 826-32.
60. Felsenfeld AL, Curry M, Kimmel CB. The fub-1 mutation blocks initial myofibril formation in zebrafish muscle pioneer cells. Dev. Biol. 1991; 148: 23-30.
61. Eisen JS, Myers PZ, Westerfield M. Pathway selection by growth cones of identified motoneurones in live zebra fish embryos. Nature 1986; 320: 269-71.
62. Henry CA, Amacher SL. Zebrafish slow muscle cell migration induces a wave of fast muscle morphogenesis. Dev. Cell 2004; 7: 917-23.