Regulator of G protein signaling 3 modulates Wnt5b calcium dynamics and somite patterning

PLoS Genetics

Volumn 6, Issue 7, 2010, Pages 1-11

  Freisinger, Christina M ^a   Fisher, Rory A ^b   Slusarski, Diane C ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; REGULATOR OF G PROTEIN SIGNALING 3; RGS PROTEIN; UNCLASSIFIED DRUG; WNT5B PROTEIN; CALCIUM; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; WNT PROTEIN; WNT5A PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

AMPLITUDE MODULATION; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FREQUENCY MODULATION; GENE CONTROL; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE INTERACTION; GENE SILENCING; IN VIVO STUDY; MOLECULAR DYNAMICS; MOLECULAR IMAGING; NONHUMAN; SIGNAL TRANSDUCTION; SOMITE; ZEBRA FISH; ANIMAL; CALCIUM SIGNALING; METABOLISM; MORPHOGENESIS; PHYSIOLOGY; PRENATAL DEVELOPMENT;

DANIO RERIO; VERTEBRATA;

ANIMALS; BODY PATTERNING; CALCIUM; CALCIUM SIGNALING; EMBRYONIC DEVELOPMENT; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GTPASE-ACTIVATING PROTEINS; HETEROTRIMERIC GTP-BINDING PROTEINS; MOLECULAR IMAGING; RGS PROTEINS; SIGNAL TRANSDUCTION; SOMITES; WNT PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 77957343157     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001020     Document Type: Article

References (73)

1. Cadigan KM, Nusse R (1997) Wnt signaling: a common theme in animal development. Genes Dev 11: 3286-305.
2. Kestler HA, Kuhl M (2008) From individual Wnt pathways towards a Wnt signalling network. Philos Trans R Soc Lond B Biol Sci 363: 1333-47.
3. Widelitz R (2005) Wnt signaling through canonical and non-canonical pathways: recent progress. Growth Factors 23: 111-6.
4. Willert K, Nusse R (1998) Beta-catenin: a key mediator of Wnt signaling. Curr Opin Genet Dev 8: 95-102.
5. Kohn AD, Moon RT (2005) Wnt and calcium signaling: beta-cateninindependent pathways. Cell Calcium 38: 439-46.
6. Cadigan KM, Liu YI (2006) Wnt signaling: complexity at the surface. J Cell Sci 119: 395-402.
7. Dale TC (1998) Signal transduction by the Wnt family of ligands. Biochem J 329(Pt 2): 209-23.
8. Kuhl M, Sheldahl LC, Park M, Miller JR, Moon RT (2000) The Wnt/Ca2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends Genet 16: 279-83.
9. Heisenberg CP, Solnica-Krezel L (2008) Back and forth between cell fate specification and movement during vertebrate gastrulation. Curr Opin Genet Dev 18: 311-6.
10. Sepich DS, Myers DC, Short R, Topczewski J, Marlow F, et al. (2000) Role of the zebrafish trilobite locus in gastrulation movements of convergence and extension. Genesis 27: 159-73.
11. Lin F, Chen S, Sepich DS, Panizzi JR, Clendenon SG, et al. (2009) Galpha12/13 regulate epiboly by inhibiting E-cadherin activity and modulating the actin cytoskeleton. J Cell Biol 184: 909-21.
12. Webb SE, Miller AL (2000) Calcium signalling during zebrafish embryonic development. Bioessays 22: 113-23.
13. Slusarski DC, Corces VG (2000) Calcium imaging in cell-cell signaling. Methods Mol Biol 135: 253-61.
14. Slusarski DC, Pelegri F (2007) Calcium signaling in vertebrate embryonic patterning and morphogenesis. Dev Biol 307: 1-13.
15. Slusarski DC, Yang-Snyder J, Busa WB, Moon RT (1997) Modulation of embryonic intracellular Ca2+ signaling by Wnt-5A. Dev Biol 182: 114-20.
16. Freisinger CM, Schneider I, Westfall TA, Slusarski DC (2008) Calcium dynamics integrated into signalling pathways that influence vertebrate axial patterning. Philos Trans R Soc Lond B Biol Sci 363: 1377-85.
17. Schneider I, Houston DW, Rebagliati MR, Slusarski DC (2008) Calcium fluxes in dorsal forerunner cells antagonize beta-catenin and alter left-right patterning. Development 135: 75-84.
18. Lyman Gingerich J, Westfall TA, Slusarski DC, Pelegri F (2005) hecate, a zebrafish maternal effect gene, affects dorsal organizer induction and intracellular calcium transient frequency. Dev Biol 286: 427-39.
19. Reinhard E, Yokoe H, Niebling KR, Allbritton NL, Kuhn MA, et al. (1995) Localized calcium signals in early zebrafish development. Dev Biol 170: 50-61.
20. Gilland E, Miller AL, Karplus E, Baker R, Webb SE (1999) Imaging of multicellular large-scale rhythmic calcium waves during zebrafish gastrulation. Proc Natl Acad Sci U S A 96: 157-61.
21. Webb SE, Miller AL (2003) Imaging intercellular calcium waves during late epiboly in intact zebrafish embryos. Zygote 11: 175-82.
22. Slusarski DC, Corces VG, Moon RT (1997) Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390: 410-3.
23. Westfall DJ (1997) Managed indemnity insurance-a clear choice for health plan sponsors. Empl Benefits J 22: 26-8.
24. Westfall TA, Brimeyer R, Twedt J, Gladon J, Olberding A, et al. (2003) Wnt-5/ pipetail functions in vertebrate axis formation as a negative regulator of Wnt/ beta-catenin activity. J Cell Biol 162: 889-98.
25. Holloway BA, Gomez de la Torre Canny S, Ye Y, Slusarski DC, Freisinger CM, et al. (2009) A novel role for MAPKAPK2 in morphogenesis during zebrafish development. PLoS Genet 5: e1000413. doi:10.1371/journal.pgen.1000413.
26. Westfall TA, Hjertos B, Slusarski DC (2003) Requirement for intracellular calcium modulation in zebrafish dorsal-ventral patterning. Dev Biol 259: 380-91.
27. Wodarz A, Nusse R (1998) Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 14: 59-88.
28. Malbon CC (2004) Frizzleds: new members of the superfamily of G-proteincoupled receptors. Front Biosci 9: 1048-58.
29. Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB (2003) The G-proteincoupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol 63: 1256-72.
30. Wang HY, Liu T, Malbon CC (2006) Structure-function analysis of Frizzleds. Cell Signal 18: 934-41.
31. Ahumada A, Slusarski DC, Liu X, Moon RT, Malbon CC, et al. (2002) Signaling of rat Frizzled-2 through phosphodiesterase and cyclic GMP. Science 298: 2006-10.
32. Katanaev VL, Ponzielli R, Semeriva M, Tomlinson A (2005) Trimeric G protein-dependent frizzled signaling in Drosophila. Cell 120: 111-22.
33. Gilman AG (1987) G proteins: transducers of receptor-generated signals. Annu Rev Biochem 56: 615-49.
34. Ross EM, Wilkie TM (2000) GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu Rev Biochem 69: 795-827.
35. Hollinger S, Hepler JR (2002) Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol Rev 54: 527-59.
36. De Vries L, Zheng B, Fischer T, Elenko E, Farquhar MG (2000) The regulator of G protein signaling family. Annu Rev Pharmacol Toxicol 40: 235-71.
37. Siderovski DP, Willard FS (2005) The GAPs, GEFs, and GDIs of heterotrimeric G-protein alpha subunits. Int J Biol Sci 1: 51-66.
38. Watson N, Linder ME, Druey KM, Kehrl JH, Blumer KJ (1996) RGS family members: GTPase-activating proteins for heterotrimeric G-protein alphasubunits. Nature 383: 172-5.
39. Hepler JR, Berman DM, Gilman AG, Kozasa T (1997) RGS4 and GAIP are GTPase-activating proteins for Gq alpha and block activation of phospholipase C beta by gamma-thio-GTP-Gq alpha. Proc Natl Acad Sci U S A 94: 428-32.
40. Kozasa T (1998) [Regulation of G protein-mediated signaling pathways by RGS proteins]. Seikagaku 70: 1418-22.
41. Kudoh T, Tsang M, Hukriede NA, Chen X, Dedekian M, et al. (2001) A gene expression screen in zebrafish embryogenesis. Genome Res 11: 1979-87.
42. Rauch GJ, Hammerschmidt M, Blader P, Schauerte HE, Strahle U, et al. (1997) Wnt5 is required for tail formation in the zebrafish embryo. Cold Spring Harb Symp Quant Biol 62: 227-34.
43. Freisinger CM, Houston DW, Slusarski DC (2008) Image analysis of calcium release dynamics. Methods Mol Biol 468: 145-56.
44. Chang DC, Meng C (1995) A Localized Elevation of Cytosolic Free Calcium is Associated with Cytokinesis in the Zebrafish Embryo. The Journal of Cell Biology 131: 1539-1545.
45. Lechleiter J, Gira S, Peralta E, Clapham D (1991) Spiral Calcium Wave Propagation and Annihilation in Xenopus laevis Oocytes. Science 252: 123-126.
46. Srinivasa SP, Watson N, Overton MC, Blumer KJ (1998) Mechanism of RGS4, a GTPase-activating protein for G protein alpha subunits. J Biol Chem 273: 1529-33.
47. Tesmer JJ, Berman DM, Gilman AG, Sprang SR (1997) Structure of RGS4 bound to AlF4-activated G(i alpha1): stabilization of the transition state for GTP hydrolysis. Cell 89: 251-61.
48. Natochin M, McEntaffer RL, Artemyev NO (1998) Mutational analysis of the Asn residue essential for RGS protein binding to G-proteins. J Biol Chem 273: 6731-5.
49. Morcos PA (2000) Gene switching: analyzing a broad range of mutations using steric block antisense oligonucleotides. Methods Enzymol 313: 174-89.
50. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
51. Creton R, Speksnijder JE, Jaffe LF (1998) Patterns of free calcium in zebrafish embryos. J Cell Sci 111(Pt 12): 1613-22.
52. Webb SE, Miller AL (2006) Ca2+ signaling during vertebrate somitogenesis. Acta Pharmacol Sin 27: 781-90.
53. Gao C, Chen YG. Dishevelled: The hub of Wnt signaling. Cell Signal 22: 717-27.
54. Angers S, Thorpe CJ, Biechele TL, Goldenberg SJ, Zheng N, et al. (2006) The KLHL12-Cullin-3 ubiquitin ligase negatively regulates the Wnt-beta-catenin pathway by targeting Dishevelled for degradation. Nat Cell Biol 8: 348-57.
55. Jung H, Kim HJ, Lee SK, Kim R, Kopachik W, et al. (2009) Negative feedback regulation of Wnt signaling by Gbetagamma-mediated reduction of Dishevelled. Exp Mol Med 41: 695-706.
56. Webb SE, Miller AL (2007) Ca2+ signalling and early embryonic patterning during zebrafish development. Clin Exp Pharmacol Physiol 34: 897-904.
57. Dohlman HG, Apaniesk D, Chen Y, Song J, Nusskern D (1995) Inhibition of Gprotein signaling by dominant gain-of-function mutations in Sst2p, a pheromone desensitization factor in Saccharomyces cerevisiae. Mol Cell Biol 15: 3635-43.
58. Koelle MR, Horvitz HR (1996) EGL-10 regulates G protein signaling in the C. elegans nervous system and shares a conserved domain with many mammalian proteins. Cell 84: 115-25.
59. Liu T, DeCostanzo AJ, Liu X, Wang H, Hallagan S, et al. (2001) G protein signaling from activated rat frizzled-1 to the beta-catenin-Lef-Tcf pathway. Science 292: 1718-22.
60. Liu X, Liu T, Slusarski DC, Yang-Snyder J, Malbon CC, et al. (1999) Activation of a frizzled-2/beta-adrenergic receptor chimera promotes Wnt signaling and differentiation of mouse F9 teratocarcinoma cells via Galphao and Galphat. Proc Natl Acad Sci U S A 96: 14383-8.
61. Feigin ME, Malbon CC (2007) RGS19 regulates Wnt-beta-catenin signaling through inactivation of Galpha(o). J Cell Sci 120: 3404-14.
62. Wu C, Zeng Q, Blumer KJ, Muslin AJ (2000) RGS proteins inhibit Xwnt-8 signaling in Xenopus embryonic development. Development 127: 2773-84.
63. Schulte G, Bryja V (2007) The Frizzled family of unconventional G-proteincoupled receptors. Trends Pharmacol Sci 28: 518-25.
64. Force T, Woulfe K, Koch WJ, Kerkela R (2007) Molecular scaffolds regulate bidirectional crosstalk between Wnt and classical seven-transmembrane-domain receptor signaling pathways. Sci STKE 2007: pe41.
65. Cirone P, Lin S, Griesbach HL, Zhang Y, Slusarski DC, et al. (2008) A role for planar cell polarity signaling in angiogenesis. Angiogenesis.
66. Parmalee NL, Kitajewski J (2008) Wnt signaling in angiogenesis. Curr Drug Targets 9: 558-64.
67. Zerlin M, Julius MA, Kitajewski J (2008) Wnt/Frizzled signaling in angiogenesis. Angiogenesis 11: 63-9.
68. Albig AR, Schiemann WP (2005) Identification and characterization of regulator of G protein signaling 4 (RGS4) as a novel inhibitor of tubulogenesis: RGS4 inhibits mitogen-activated protein kinases and vascular endothelial growth factor signaling. Mol Biol Cell 16: 609-25.
69. Westerfield M (1995) The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio) (Eugene, OR, M. Westerfield).
70. Thisse C, Thisse B, Schilling TF, Postlethwait JH (1993) Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119: 1203-15.
71. Long S, Rebagliati M (2002) Sensitive two-color whole-mount in situ hybridizations using digoxygenin- and dinitrophenol-labeled RNA probes. Biotechniques 32: 494, 496, 498 passim.
72. Chang DC, Meng C (1995) A localized elevation of cytosolic free calcium is associated with cytokinesis in the zebrafish embryo. J Cell Biol 131: 1539-45.
73. Lechleiter J, Girard S, Peralta E, Clapham D (1991) Spiral calcium wave propagation and annihilation in Xenopus laevis oocytes. Science 252: 123-6.