Calcium signaling in developing embryos: Focus on the regulation of cell shape changes and collective movements

Seminars in Cell and Developmental Biology

Volumn 23, Issue 3, 2012, Pages 298-307

  Markova, Olga ^a   Lenne, Pierre François ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Calcium signaling; Cell shape changes; Convergent extension; Cytoskeleton; Tissue morphogenesis

Indexed keywords

CALCIUM; MYOSIN ADENOSINE TRIPHOSPHATASE;

BLASTULA; CALCIUM SIGNALING; CELL MIGRATION; CELL MOTILITY; CELL SHAPE; CYTOSKELETON; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; GASTRULA; MORPHOGENESIS; NONHUMAN; ORYZIAS; REGULATORY MECHANISM; REVIEW; SOMITE; XENOPUS; ZEBRA FISH;

EID: 84860363791     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2012.03.006     Document Type: Review

References (75)

1. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003, 4:517-529.
2. Slusarski D.C., Pelegri F. Calcium signaling in vertebrate embryonic patterning and morphogenesis. Dev Biol 2007, 307:1-13.
3. Webb S.E., Miller A.L. Calcium signalling during embryonic development. Nat Rev Mol Cell Biol 2003, 4:539-551.
4. Wallingford J.B., Ewald A.J., Harland R.M., Fraser S.E. Calcium signaling during convergent extension in Xenopus. Curr Biol 2001, 11:652-661.
5. Freisinger C.M., Fisher R.A., Slusarski D.C. Regulator of g protein signaling 3 modulates wnt5b calcium dynamics and somite patterning. PLoS Genet 2010, 6:e1001020.
6. Créton R., Speksnijder J.E., Jaffe L.F. Patterns of free calcium in zebrafish embryos. J Cell Sci 1998, 111(Pt 12):1613-1622.
7. Shindo A., Hara Y., Yamamoto T.S., Ohkura M., Nakai J., Ueno N. Tissue-tissue interaction-triggered calcium elevation is required for cell polarization during Xenopus gastrulation. PLoS ONE 2010, 5:e8897.
8. 2+ signaling and early embryonic patterning during the blastula and gastrula periods of zebrafish and Xenopus development. Biochim Biophys Acta 2006, 1763:1192-1208.
9. Lecuit T., Lenne P.-F., Munro E. Force generation, transmission, and integration during cell and tissue morphogenesis. Ann Rev Cell Dev Biol 2011, 27:157-184.
10. Berridge M.J. Calcium microdomains: organization and function. Cell Calcium 2006, 40:405-412.
11. 2+ signalling. Nat Rev Neurosci 2007, 8:182-193.
12. Jaffe L.F. Fast calcium waves. Cell Calcium 2010, 48:102-113.
13. Jaffe L.F. Calcium waves. Philos Trans R Soc B Biol Sci 2008, 363:1311-1316.
14. Schwab A., Nechyporuk-Zloy V., Fabian A., Stock C. Cells move when ions and water flow. Pflugers Arch 2007, 453:421-432.
15. i and cell shape, polarity, and locomotion by InsP3, DAG, and protein kinase C in newt eosinophils. J Cell Biol 1994, 127:489-503.
16. Doyle A., Marganski W., Lee J. Calcium transients induce spatially coordinated increases in traction force during the movement of fish keratocytes. J Cell Sci 2004, 117:2203-2214.
17. Iwadate Y., Yumura S. Actin-based propulsive forces and myosin-II-based contractile forces in migrating dictyostelium cells. J Cell Sci 2008, 121:1314-1324.
18. Blaser H., Reichman-Fried M., Castanon I., Dumstrei K., Marlow F.L., Kawakami K., et al. Migration of zebrafish primordial germ cells: a role for myosin contraction and cytoplasmic flow. Dev Cell 2006, 11:613-627.
19. Athman R., Louvard D., Robine S. The epithelial cell cytoskeleton and intracellular trafficking. III. How is villin involved in the actin cytoskeleton dynamics in intestinal cells?. Am J Physiol Gastrointest Liver Physiol 2002, 283:G496-G502.
20. Ko K.S., Arora P.D., McCulloch C.A. Cadherins mediate intercellular mechanical signaling in fibroblasts by activation of stretch-sensitive calcium-permeable channels. J Biol Chem 2001, 276:35967-35977.
21. Moore T.M., Brough G.H., Babal P., Kelly J.J., Li M., Stevens T. Store-operated calcium entry promotes shape change in pulmonary endothelial cells expressing Trp1. Am J Physiol 1998, 275:L574-L582.
22. Fabian A., Fortmann T., Dieterich P., Riethmüller C., Schön P., Mally S., et al. TRPC1 channels regulate directionality of migrating cells. Pflugers Arch 2008, 457:475-484.
23. He L., Wang X., Tang H.L., Montell D.J. Tissue elongation requires oscillating contractions of a basal actomyosin network. Nat Cell Biol 2010, 12:1133-1142.
24. 2+ 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. Dev Growth Differ 2009, 51:429-442.
25. Cheng J.C., Miller A.L., Webb S.E. Organization and function of microfilaments during late epiboly in zebrafish embryos. Dev Dyn 2004, 231:313-323.
26. 2+ trafficking in the zebrafish blastula. Dev Cell 2011, 20:663-676.
27. Takano K., Obata S., Komazaki S., Masumoto M., Oinuma T., Ito Y., et al. Development of Ca2(+) signaling mechanisms and cell motility in presumptive ectodermal cells during amphibian gastrulation. Dev Growth Differ 2011, 53:37-47.
28. 2+ signals in the formed somites during the early segmentation period in intact, normally developing zebrafish embryos. Dev Growth Differ 2009, 51:617-637.
29. Chernoff E.A., Hilfer S.R. Calcium dependence and contraction in somite formation. Tissue Cell 1982, 14:435-449.
30. Lane M.C., Koehl M.A., Wilt F., Keller R. A role for regulated secretion of apical extracellular matrix during epithelial invagination in the sea urchin. Development 1993, 117:1049-1060.
31. Moran D., Rice R.W. Action of papaverine and ionophore A23187 on neurulation. Nature 1976, 261:497-499.
32. Creton R., Kreiling J.A., Jaffe L.F. Presence and roles of calcium gradients along the dorsal-ventral axis in Drosophila embryos. Dev Biol 2000, 217:375-385.
33. Leclerc C., Webb S.E., Daguzan C., Moreau M., Miller A.L. Imaging patterns of calcium transients during neural induction in Xenopus laevis embryos. J Cell Sci 2000, 113(Pt 19):3519-3529.
34. Stableford L.T. A study of calcium in the early development of the amphibian embryo. Dev Biol 1967, 16:303-314.
35. 2+ transients in initiating the apical-basolateral thinning of enveloping layer cells during the early blastula period of zebrafish development. Dev Growth Differ 2011, 53:679-696.
36. Brady R.C., Hilfer S.R. Optic cup formation: a calcium-regulated process. Proc Natl Acad Sci USA 1982, 79:5587-5591.
37. Reinhard E., Yokoe H., Niebling K.R., Allbritton N.L., Kuhn M.A., Meyer T. Localized calcium signals in early zebrafish development. Dev Biol 1995, 170:50-61.
38. 2+ signaling in the superficial epithelium following the mid-blastula transition in zebrafish embryos. Dev Biol 2009, 327:143-157.
39. Slusarski D.C., Corces V.G., Moon R.T. Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 1997, 390:410-413.
40. Holloway B.A., Gomez de la Torre Canny S., Ye Y., Slusarski D.C., Freisinger C.M., Dosch R., et al. A novel role for MAPKAPK2 in morphogenesis during zebrafish development. PLoS Genet 2009, 5:e1000413.
41. 2+ signaling by Wnt-5A. Dev Biol 1997, 182:114-120.
42. Lin S., Baye L.M., Westfall T.A., Slusarski D.C. Wnt5b-Ryk pathway provides directional signals to regulate gastrulation movement. J Cell Biol 2010, 190:263-278.
43. 2+ flux, PKC, and CamKII in vertebrate embryos. J Cell Biol 2003, 161:769-777.
44. Veeman M., Slusarski D., Kaykas A., Louie S., Moon R. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr Biol 2003, 13:680-685.
45. Webb S.E., Miller A.L. Imaging intercellular calcium waves during late epiboly in intact zebrafish embryos. Zygote 2003, 11:175-182.
46. Gilland E., Miller A.L., Karplus E., Baker R., Webb S.E. Imaging of multicellular large-scale rhythmic calcium waves during zebrafish gastrulation. Proc Natl Acad Sci USA 1999, 96:157-161.
47. Barber B., da Cruz M.J., DeLeon J., Fluck R.A., Hasenfeld M.P., Unis L.A. Pacemaker region in a rhythmically contracting embryonic epithelium, the enveloping layer of Oryzias latipes, a teleost. J Exp Zool 1987, 242:35-42.
48. Sguigna C., Fluck R., Barber B. Calcium dependence of rhythmic contractions of the Oryzias latipes blastoderm. Comp Biochem Physiol C Comp Pharmacol Toxicol 1988, 89:369-374.
49. Leclerc C., Lee M., Webb S.E., Moreau M., Miller A.L. Calcium transients triggered by planar signals induce the expression of ZIC3 gene during neural induction in Xenopus. Dev Biol 2003, 261:381-390.
50. Keller R. Mechanisms of elongation in embryogenesis. Development 2006, 133:2291-2302.
51. Kilian B., Mansukoski H., Barbosa F.C., Ulrich F., Tada M., Heisenberg C.P. The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mech Dev 2003, 120:467-476.
52. Westfall T.A., Hjertos B., Slusarski D.C. Requirement for intracellular calcium modulation in zebrafish dorsal-ventral patterning. Dev Biol 2003, 259:380-391.
53. Berchtold M.W., Brinkmeier H., Müntener M. Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev 2000, 80:1215-1265.
54. 2+ sensitization of smooth muscle contraction through myosin light chain phosphorylation. J Biol Chem 1991, 266:1708-1715.
55. Somlyo A.P., Somlyo A.V. Signal transduction and regulation in smooth muscle. Nature 1994, 372:231-236.
56. Forscher P. Calcium and polyphosphoinositide control of cytoskeletal dynamics. Trends Neurosci 1989, 12:468-474.
57. 2+ signalling. Acta Physiol (Oxf) 2009, 195:61-70.
58. Lim D., Lange K., Santella L. Activation of oocytes by latrunculin A. FASEB J 2002, 16:1050-1056.
59. Jaffe L.F. Stretch-activated calcium channels relay fast calcium waves propagated by calcium-induced calcium influx. Biol Cell 2007, 99:175-184.
60. 2+ signaling: a new view of an old problem. J Cell Physiol 1999, 180:19-34.
61. Tsuruwaka Y., Konishi T., Miyawaki A., Takagi M. Real-time monitoring of dynamic intracellular Ca(2+) movement during early embryogenesis through expression of yellow cameleon. Zebrafish 2007, 4:253-260.
62. Rauzi M., Lenne P.-F., Lecuit T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 2010, 468:1110-1114.
63. Martin A.C., Kaschube M., Wieschaus E.F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 2009, 457:495-499.
64. Solon J., Kaya-Copur A., Colombelli J., Brunner D. Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 2009, 137:1331-1342.
65. Schillers H., Wälte M., Urbanova K., Oberleithner H. Real-time monitoring of cell elasticity reveals oscillating myosin activity. Biophys J 2010, 99:3639-3646.
66. Gossler A., Hrabě de Angelis M. Somitogenesis. Curr Top Dev Biol 1998, 38:225-287.
67. Pourquié O. Vertebrate segmentation: from cyclic gene networks to scoliosis. Cell 2011, 145:650-663.
68. Oates A.C., Morelli L.G., Ares S. Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock. Development 2012, 139:625-639.
69. Ferrari M.B., Spitzer N.C. Calcium signaling in the developing Xenopus myotome. Dev Biol 1999, 213:269-282.
70. Martins G.G., Rifes P., Amândio R., Rodrigues G., Palmeirim I., Thorsteinsdóttir S. Dynamic 3D cell rearrangements guided by a fibronectin matrix underlie somitogenesis. PLoS ONE 2009, 4:e7429.
71. Li H., Cook J.D., Terry M., Spitzer N.C., Ferrari M.B. Calcium transients regulate patterned actin assembly during myofibrillogenesis. Dev Dyn 2004, 229:231-242.
72. Landsberg K.P., Farhadifar R., Ranft J., Umetsu D., Widmann T.J., Bittig T., et al. Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr Biol 2009, 19:1950-1955.
73. McKinney M.C., Kulesa P.M. In vivo calcium dynamics during neural crest cell migration and patterning using GCaMP3. Dev Biol 2011, Available at:. http://www.ncbi.nlm.nih.gov/pubmed/21864525.
74. Simon J.Z., Cooper M.S. Calcium oscillations and calcium waves coordinate rhythmic contractile activity within the stellate cell layer of medaka fish embryos. J Exp Zool 1995, 273(2):118-129.
75. Brennan C., Amacher S.L., Currie P.D. IV. Aspects of organogenesis: somitogenesis. Res Prob Cell Differ 2002, 40:271-297.