Inhibition of stored Ca2+ release disrupts convergence-related cell movements in the lateral intermediate mesoderm resulting in abnormal positioning and morphology of the pronephric anlagen in intact zebrafish embryos

Development Growth and Differentiation

Volumn 51, Issue 4, 2009, Pages 429-442

  Lam, Pui Ying ^a,c   Webb, Sarah E ^a   Leclerc, Catherine ^b   Moreau, Marc ^b   Miller, Andrew L ^a  

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

^b CNRS   (France)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Ca2+ signaling; Convergence; IP 3R; Pronephric anlagen; Zebrafish embryos

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 2,5 PYRROLIDINEDIONE; NIFEDIPINE; 1 (6 ((3 METHOXYESTRA 1,3,5(10) TRIEN 17 YL)AMINO)HEXYL) 1H PYRROLE 2,5 DIONE; 1-(6-((3-METHOXYESTRA-1,3,5(10)-TRIEN-17-YL)AMINO)HEXYL)-1H-PYRROLE-2,5-DIONE; 2 PYRROLIDONE DERIVATIVE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; DANTROLENE; ESTRANE DERIVATIVE; PAX2A PROTEIN, ZEBRAFISH; REPRESSOR PROTEIN; SIM1 PROTEIN, ZEBRAFISH; THAPSIGARGIN; TRANSCRIPTION FACTOR PAX2; ZEBRAFISH PROTEIN;

ARTICLE; CALCIUM TRANSPORT; CELL MOTION; CELL STRUCTURE; CONTROLLED STUDY; DRUG INHIBITION; EMBRYO; IN SITU HYBRIDIZATION; MESODERM; NONHUMAN; ZEBRA FISH; ANIMAL; CYTOLOGY; DRUG EFFECT; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT;

DANIO RERIO;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CELL MOVEMENT; DANTROLENE; ESTRENES; IN SITU HYBRIDIZATION; MESODERM; PAX2 TRANSCRIPTION FACTOR; PYRROLIDINONES; REPRESSOR PROTEINS; THAPSIGARGIN; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 65349175207     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2009.01106.x     Document Type: Article

References (67)

1. Amacher, S. L., Draper, B. W., Summers, B. R. Kimmel, C. B. 2002. The zebrafish T-box genes no tail and spadetail are required for development of trunk and tail mesoderm and medial floor plate. Development 129, 3311 3323.
2. Ashworth, R. 2004. Approaches to measuring calcium in zebrafish: focus on neuronal development. Cell Calcium 35, 393 402.
3. Bakkers, J., Kramer, C., Pothof, J., Quaedvlieg, N. E. M., Spaink, H. P. Hammerschmidt, M. 2004. Has2 is required upstream of Rac1 to govern dorsal migration of lateral cells during zebrafish gastrulation. Development 131, 525 537.
4. Biemar, F., Argenton, F., Schmidtke, R., Epperlein, S., Peers, B. Driever, W. 2001. Pancreas development in zebrafish: early dispersed appearance of endocrine hormone expressing cells and their convergence to form the definitive islet. Dev. Biol. 230, 189 203.
5. Bleasdale, J. E. Fisher, S. K. 1993. Use of U-73122 as an inhibitor of phospholipase C-dependent processes. Neuroprotocols 3, 125 133.
6. Borchers, A., Fonar, Y., Frank, D. Baker, J. C. 2006. XNF-ATc3 affects neural convergent extension. Development 133, 1745 1755.
7. Bradley, J. E., Anderson, U. A., Woolsey, S. M., Thornbury, K. D., McHale, N. G. Hollywood, M. A. 2004. Characterization of T-type calcium current and its contribution to electrical activity in rabbit urethra. Am. J. Physiol. Cell Physiol. 286, C1078 C1088.
8. Brennan, C., Mangoli, M., Dyer, C. E. Ashworth, R. 2005. Acetylcholine and calcium signalling regulates muscle fiber formation in the zebrafish embryo. J. Cell Sci. 118, 5181 5190.
9. Chow, E. S. H. Cheng, S. H. 2003. Cadmium affects muscle type development and axon growth in zebrafish embryonic somitogenesis. Toxicol. Sci. 73, 149 159.
10. Cooper, M. S. Kimmel, C. B. 1998. Morphogenetic cell behaviors and specification of cell fate during early teleost development. In : Motion Analysis of Living Cells (eds D. R. Soll D. Wessels pp. 177 220. Wiley-Liss, New York.
11. Créton, R., Speksnijder, J. E. Jaffe, L. F. 1998. Patterns of free calcium in zebrafish embryos. J. Cell Sci. 111, 1613 1622.
12. Drummond, I. A. 2000. The zebrafish pronephros: a genetic system for studies of kidney development. Pediatr. Nephrol. 14, 428 435.
13. Drummond, I. A. 2003. Making a zebrafish kidney: a tale of two tubules. Trends Cell Biol. 13, 357 365.
14. Drummond, I. A., Majumdar, A., Hentschel, H., Elger, M., Solnica-Krezel, L., Schier, A. F., Neuhauss, S. C. F., Stemple, D. L., Zwartkruis, F., Rangini, Z., Driever, W. Fishman, M. C. 1998. Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development 125, 4655 4667.
15. Du, S. J., Purcell, S. M., Christian, J. L., McGrew, L. L. Moon, R. T. 1995. Identification of distinct classes and functional domains of Wnts through expression of wild-type and chimeric protein in Xenopus embryos. Mol. Cell. Biol. 15, 2625 2634.
16. Eaton, J. L. Glasgow, E. 2006. The zebrafish bHLH PAS transcriptional regulator, single-minded 1 (sim1), is required for isotocin cell development. Dev. Dyn. 235, 2071 2082.
17. Ferrari, M. B. Spitzer, N. C. 1999. Calcium signaling in the developing Xenopus myotome. Dev. Biol. 213, 269 382.
18. Freisinger, C. M., Schneider, I., Westfall, T. A. Slusarski, D. C. 2008. Calcium dynamics integrated into signalling pathways that influence vertebrate axial patterning. Phil. Trans. R. Soc. 363, 1377 1385.
19. Gilland, E., Miller, A. L., Karplus, E., Baker, R. Webb, S. E. 1999. Imaging of multicellular large-scale rhythmic calcium waves during zebrafish gastrulation. Proc. Natl Acad. Sci. USA 96, 157 161.
20. Glickman, N. S., Kimmel, C. B., Jones, M. A. Adams, R. J. 2003. Shaping the zebrafish notochord. Development 130, 873 887.
21. Hayashi, T., Kagaya, A., Motohashi, N. Yamawaki, S. 1994. Possible mechanism of dantrolene stabilization of cultured neuroblastoma cell plasma membranes. J. Neurochem. 63, 1849 1854.
22. Horsfield, J., Ramachandran, A., Reuter, K., LaVallie, E., Collins-Racie, L., Crosier, K. Crosier, P. 2002. Cadherin-17 is required to maintain pronephric duct integrity during zebrafish development. Mech. Dev. 115, 15 26.
23. Jaffe, L. F. 1999. Organization of early development by calcium patterns. Bioessays 21, 657 667.
24. Kim, S. H., Yamamoto, A., Bouwmeester, T., Agius, E. Robertis, E. M. 1998. The role of paraxial protocadherin in selective adhesion and cell movements of the mesoderm during Xenopus gastrulation. Development 125, 4681 4690.
25. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. Schilling, T. F. 1995. Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253 310.
26. Krauss, S., Johansen, T., Korzh, V. Fjose, A. 1991. Expression of the zebrafish paired box gene pax[zf-b] during early neurogenesis. Development 113, 1193 1206.
27. 2+ signaling. Mech. Devel. 106, 61 76.
28. Kupperman, E., An, S., Osborne, N., Waldron, S. Stainier, D. Y. 2000. A sphingosine-1-phosphate receptor regulates cell migration during vertebrate heart development. Nature 406, 192 195.
29. Leclerc, C., Webb, S. E., Daguzan, C., Moreau, M. Miller, A. L. 2000. Imaging patterns of calcium transients during neural induction in Xenopus laevis embryos. J. Cell Sci. 113, 3519 3529.
30. Leclerc, C., Lee, M., Webb, S. E., Moreau, M. Miller, A. L. 2003. Calcium transients triggered by planar signals induce the expression of ZIC3 during neural induction in Xenopus. Dev. Biol. 261, 381 390.
31. 2+ levels is involved in pronephric tubule differentiation in the amphibian Xenopus laevis. Dev. Biol. 321, 357 367.
32. Lee, C. H. Gumbiner, B. M. 1995. Disruption of gastrulation movements in Xenopus by a dominant-negative mutant for C-cadherin. Dev. Biol. 171, 363 373.
33. Majumdar, A. Drummond, I. A. 2000. The zebrafish floating head mutant demonstrates podocytes play an important role in directing glomerular differentiation. Dev. Biol. 222, 147 157.
34. Majumdar, A., Lun, K., Brand, M. Drummond, I. A. 2000. Zebrafish no isthmus reveals a role for pax2.1 in tubule differentiation and patterning events in the pronephric primordia. Development 127, 2089 2098.
35. Matsui, T., Raya, A., Kawakami, Y., Callol-Massot, C., Capdevila, J., Rodríguez-Esteban, C. Izpisua Belmonte, J. C. 2005. Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev. 19, 164 175.
36. Moreau, M. Leclerc, C. 2004. The choice between epidermal and neural fate: a matter of calcium. Int. J. Dev. Biol. 48, 75 84.
37. 2+ mediates neural induction in the amphibian embryo. Proc. Natl Acad. Sci. USA 91, 12639 12643.
38. 2+ channels in the terminal mesenteric artery of guinea pig. Circ. Res. 85, 596 605.
39. Myers, D. C., Sepich, D. S. Solnica-Krezel, L. 2002. Convergence and extension in vertebrate gastrulae: cell movements according to or in search of identity? Trends Genet. 18, 447 455.
40. Nutt, S. L., Dingwell, K. S., Holt, C. E. Amaya, E. 2001. Xenopus Sprouty2 inhibits FGF-mediated gastrulation movements but does not affect mesoderm induction and patterning. Genes Dev. 15, 1152 1166.
41. Price, L. S., Langeslag, M., ten Klooster, J. P., Hordijk, P. L., Jalink, K. Collard, J. G. 2003. Calcium signaling regulates translocation and activation of Rac. J. Biol. Chem. 278, 39413 39421.
42. Raz, E. Reichman-Fried, M. 2006. Attraction rules: germ cell migration in zebrafish. Curr. Opin. Genet. Dev. 16, 355 359.
43. Saxén, L. Sariola, H. 1987. Early organogenesis of the kidney. Pediatr. Nephrol. 1, 385 392.
44. Schneider, I., Houston, D. W., Rebagliati, M. R. Slusarski, D. C. 2008. Calcium fluxes in dorsal forerunner cells antagonize β-catenin and alter left-right patterning. Development 135, 75 84.
45. Sepich, D. S., Myers, D. C., Short, R., Topczewski, J., Marlow, F. Solnica-Krezel, L. 2000. Role of the zebrafish trilobite locus in gastrulation movements of convergence and extension. Genesis 27, 159 173.
46. Serbedzija, G. N., Chen, J. N. Fishman, M. C. 1998. Regulation in the heart field of zebrafish. Development 125, 1095 1101.
47. Serluca, F. C. Fishman, M. C. 2001. Pre-pattern in the pronephric kidney field of zebrafish. Development 128, 2233 2241.
48. Sivak, J. M., Petersen, L. F. Amaya, E. 2005. FGF signal interpretation is directed by Sprouty and Spred proteins during mesoderm formation. Dev. Cell 8, 689 701.
49. Slusarski, D. C. Pelegri, F. 2007. Calcium signaling in vertebrate embryonic patterning and morphogenesis. Dev. Biol. 307, 1 13.
50. Slusarski, D. C., Corces, V. G. Moon, R. T. 1997. Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390, 410 413.
51. Stainier, D. Y. R. 2001. Zebrafish genetics and vertebrate heart formation. Nat. Rev. Genet. 2, 39 48.
52. Strieker, S. A. 1999. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev. Biol. 211, 157 176.
53. Thisse, C. Zon, L. I. 2002. Organogenesis - Heart and blood formation from the zebrafish point of view. Science 295, 457 462.
54. Torres, M. A., Yang-Snyder, J. A., Purcell, S. M., DeMarais, A. A., McGrew, L. L. Moon, R. T. 1996. Activities of the Wnt-1 class of secreted signaling factors are antagonized by the Wnt-5A class and by a dominant negative cadherin in early Xenopus development. J. Cell Biol. 133, 1123 1137.
55. Wallingford, J. B., Ewald, A. J., Harland, R. M. Fraser, S. E. 2001. Calcium signaling during convergent extension in Xenopus. Curr. Biol. 11, 652 661.
56. Warga, R. M. Kimmel, C. B. 1990. Cell movements during epiboly and gastrulation in zebrafish. Development 108, 569 580.
57. Webb, S. E. Miller, A. L. 2003. Calcium signalling during embryonic development. Nat. Rev. Mol. Cell Biol. 4, 539 551.
58. 2+ signaling and early embryonic patterning during the Blastula and Gastrula Periods of zebrafish and Xenopus development. Biochim. Biophys. Acta. 11, 1192 1208.
59. 2+ signaling during vertebrate somitogenesis. Acta Pharm. Sinica 27, 767 958.
60. Webb, S. E., Lee, K. W., Karplus, E. Miller, A. L. 1997. Localized calcium transients accompany furrow positioning, propagation, and deepening during the early cleavage period of zebrafish embryos. Dev Biol. 192, 78 92.
61. Webb, S. E., Moreau, M., Leclerc, C. Miller, A. L. 2005. Calcium transients and neural induction in vertebrates. Cell Calcium 37, 375 385.
62. Weidinger, G., Wolke, U., Köprunner, M., Thisse, C., Thisse, B. Raz, E. 2002. Regulation of zebrafish primordial germ cell migration by attraction towards an intermediate target. Development 129, 25 36.
63. Weinberg, E. S., Allende, M. L., Kelly, C. S., Abdelhamid, A., Murakami, T., Andermann, P., Doerre, O. G., Grunwald, D. J. Riggleman, B. 1996. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development 122, 271 280.
64. Westerfield, M. 1995. The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio Rerio), 3rd edn. University of Oregon Press, Eugene.
65. Whitaker, M. 2006. Calcium at fertilization and in early development. Physiol. Rev. 86, 25 88.
66. Whitaker, M. 2008. Calcium signaling in early embryos. Phil. Trans. R. Soc. 363, 1401 1418.
67. Yin, C., Kiskowski, M., Pouille, P. A., Farge, E. Solnica-Krezel, L. 2008. Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J. Cell Biol. 180, 221 232.