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PMID: 21963539 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Functional dissection of phosphorylation of Disheveled in Drosophila.

Developmental biology ·Vol. 360 ·No. 1 ·2011-12-01 ·Pages 132-42

Yanfeng WA, Berhane H, Mola M, Singh J, Jenny A, Mlodzik M

Abstract

Disheveled/Dsh proteins (Dvl in mammals) are core components of both Wnt/Wg-signaling pathways: canonical β-catenin signaling and Frizzled (Fz)-planar cell polarity (PCP) signaling. Although Dsh is a key cytoplasmic component of both Wnt/Fz-pathways, regulation of its signaling specificity is not well understood. Dsh is phosphorylated, but the functional significance of its phosphorylation remains unclear. We have systematically investigated the phosphorylation of Dsh by combining mass-spectrometry analyses, biochemical studies, and in vivo genetic methods in Drosophila. Our approaches identified multiple phospho-residues of Dsh in vivo. Our data define three novel and unexpected conclusions: (1) strikingly and in contrast to common assumptions, all conserved serines/threonines are non-essential for Dsh function in either pathway; (2) phosphorylation of conserved Tyrosine473 in the DEP domain is critical for PCP-signaling - Dsh(Y473F) behaves like a PCP-specific allele; and (3) defects associated with the PCP specific dsh(1) allele, Dsh(K417M), located within a putative Protein Kinase C consensus site, are likely due to a post-translational modification requirement of Lys417, rather than phosphorylation nearby. In summary, our combined data indicate that while many Ser/Thr and Tyr residues are indeed phosphorylated in vivo, strikingly most of these phosphorylation events are not critical for Dsh function with the exception of DshY473.

MeSH Terms
Adaptor Proteins, Signal Transducing/chemistry,genetics,metabolism Alleles Amino Acid Sequence Amino Acid Substitution Animals Animals, Genetically Modified Armadillo Domain Proteins/genetics,metabolism Binding Sites/genetics Cell Polarity Dishevelled Proteins Drosophila/genetics,growth & development,metabolism Drosophila Proteins/chemistry,genetics,metabolism Frizzled Receptors/genetics,metabolism Molecular Sequence Data Mutagenesis, Site-Directed Phosphoproteins/chemistry,genetics,metabolism Phosphorylation Signal Transduction Tandem Mass Spectrometry Transcription Factors/genetics,metabolism Wings, Animal/growth & development,metabolism Wnt Signaling Pathway
Chemicals
ARM protein, Drosophila Adaptor Proteins, Signal Transducing Armadillo Domain Proteins Dishevelled Proteins Drosophila Proteins Frizzled Receptors Phosphoproteins Transcription Factors dsh protein, Drosophila fz protein, Drosophila
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Yanfeng Wang A
Dept. of Developmental & Regenerative Biology, Mount Sinai School of Medicine, One Gustave L. Levy Place, New York, NY 10029, USA.
Berhane Hebist
Mola Marion
Singh Jaskirat
Jenny Andreas
Mlodzik Marek
References (50)
50 references, click to expand
  1. A mutational analysis of dishevelled in Drosophila defines novel domains in the dishevelled protein as well as novel suppressing alleles of axin.
    Genetics. 2002 Jun;161(2):747-62 PMID: 12072470
  2. Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling.
    Genes Dev. 2001 May 15;15(10):1182-7 PMID: 11358862
  3. The developmental biology of Dishevelled: an enigmatic protein governing cell fate and cell polarity.
    Development. 2005 Oct;132(20):4421-36 PMID: 16192308
  4. Wingless eliminates ommatidia from the edge of the developing eye through activation of apoptosis.
    Development. 2004 May;131(10):2409-18 PMID: 15128670
  5. PKC delta is essential for Dishevelled function in a noncanonical Wnt pathway that regulates Xenopus convergent extension movements.
    Genes Dev. 2003 Jul 1;17(13):1663-76 PMID: 12842914
  6. Dishevelled: at the crossroads of divergent intracellular signaling pathways.
    Mech Dev. 1999 May;83(1-2):27-37 PMID: 10507837
  7. Regulation of Lethal giant larvae by Dishevelled.
    Nature. 2005 Oct 27;437(7063):1376-80 PMID: 16251968
  8. Casein kinase 2 associates with and phosphorylates dishevelled.
    EMBO J. 1997 Jun 2;16(11):3089-96 PMID: 9214626
  9. Regulation of ciliary polarity by the APC/C.
    Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17799-804 PMID: 19805045
  10. A quest for the mechanism regulating global planar cell polarity of tissues.
    Trends Cell Biol. 2009 Jul;19(7):295-305 PMID: 19560358
  11. Planar signaling and morphogenesis in Drosophila.
    Dev Cell. 2002 May;2(5):525-35 PMID: 12015961
  12. frizzled and frizzled 2 play a partially redundant role in wingless signaling and have similar requirements to wingless in neurogenesis.
    Cell. 1998 Dec 23;95(7):1027-36 PMID: 9875856
  13. Wingless transduction by the Frizzled and Frizzled2 proteins of Drosophila.
    Development. 1999 Dec;126(23):5441-52 PMID: 10556068
  14. Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility.
    Nat Rev Genet. 2007 Feb;8(2):126-38 PMID: 17230199
  15. The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling.
    Dev Cell. 2008 Sep;15(3):462-469 PMID: 18804440
  16. Electrochemical cues regulate assembly of the Frizzled/Dishevelled complex at the plasma membrane during planar epithelial polarization.
    Nat Cell Biol. 2009 Mar;11(3):286-94 PMID: 19234454
  17. CKIepsilon/discs overgrown promotes both Wnt-Fz/beta-catenin and Fz/PCP signaling in Drosophila.
    Curr Biol. 2006 Jul 11;16(13):1337-43 PMID: 16824922
  18. Abelson family kinases regulate Frizzled planar cell polarity signaling via Dsh phosphorylation.
    Genes Dev. 2010 Oct 1;24(19):2157-68 PMID: 20837657
  19. Planar polarity in the Drosophila eye: a multifaceted view of signaling specificity and cross-talk.
    EMBO J. 1999 Dec 15;18(24):6873-9 PMID: 10601009
  20. Stability elements in the LRP6 cytoplasmic tail confer efficient signalling upon DIX-dependent polymerization.
    J Cell Sci. 2010 May 1;123(Pt 9):1588-99 PMID: 20388731
  21. Pathway specificity by the bifunctional receptor frizzled is determined by affinity for wingless.
    Mol Cell. 2000 Jul;6(1):117-26 PMID: 10949033
  22. Casein kinase Iepsilon modulates the signaling specificities of dishevelled.
    Mol Cell Biol. 2004 Mar;24(5):2000-11 PMID: 14966280
  23. Planar cell polarization: do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation?
    Trends Genet. 2002 Nov;18(11):564-71 PMID: 12414186
  24. Microscopic analysis of the adult Drosophila retina using semithin plastic sections.
    Methods Mol Biol. 2008;420:277-87 PMID: 18641954
  25. Wingless signaling in the Drosophila embryo: zygotic requirements and the role of the frizzled genes.
    Development. 1999 Feb;126(3):577-86 PMID: 9876186
  26. Shaping the vertebrate body plan by polarized embryonic cell movements.
    Science. 2002 Dec 6;298(5600):1950-4 PMID: 12471247
  27. Polarity determination in the Drosophila eye.
    Curr Opin Genet Dev. 1999 Aug;9(4):442-6 PMID: 10449350
  28. The Wnt signalling effector Dishevelled forms dynamic protein assemblies rather than stable associations with cytoplasmic vesicles.
    J Cell Sci. 2005 Nov 15;118(Pt 22):5269-77 PMID: 16263762
  29. Planar cell polarity: one or two pathways?
    Nat Rev Genet. 2007 Jul;8(7):555-63 PMID: 17563758
  30. Signaling specificity by Frizzled receptors in Drosophila.
    Science. 2000 Jun 9;288(5472):1825-8 PMID: 10846164
  31. Planar cell polarization: an emerging model points in the right direction.
    Annu Rev Cell Dev Biol. 2005;21:155-76 PMID: 16212491
  32. Distinct PAR-1 proteins function in different branches of Wnt signaling during vertebrate development.
    Dev Cell. 2005 Jun;8(6):829-41 PMID: 15935773
  33. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling.
    Cell. 1998 Jul 10;94(1):109-18 PMID: 9674432
  34. The Wnt signaling pathway in development and disease.
    Annu Rev Cell Dev Biol. 2004;20:781-810 PMID: 15473860
  35. Tissue/planar cell polarity in vertebrates: new insights and new questions.
    Development. 2007 Feb;134(4):647-58 PMID: 17259302
  36. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways.
    Genes Dev. 1998 Aug 15;12(16):2610-22 PMID: 9716412
  37. Transducing properties of Drosophila Frizzled proteins.
    Development. 2001 Dec;128(23):4829-35 PMID: 11731462
  38. Planar cell polarity signaling: from fly development to human disease.
    Annu Rev Genet. 2008;42:517-40 PMID: 18710302
  39. Wnt signaling and cancer.
    Genes Dev. 2000 Aug 1;14(15):1837-51 PMID: 10921899
  40. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling.
    Dev Cell. 2003 Sep;5(3):367-77 PMID: 12967557
  41. Subcellular localization of frizzled receptors, mediated by their cytoplasmic tails, regulates signaling pathway specificity.
    PLoS Biol. 2004 Jul;2(7):E158 PMID: 15252441
  42. RhoA effector mutants reveal distinct effector pathways for cytoskeletal reorganization, SRF activation and transformation.
    EMBO J. 1998 Mar 2;17(5):1350-61 PMID: 9482732
  43. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells.
    Nat Genet. 2008 Jul;40(7):871-9 PMID: 18552847
  44. Direct binding of the PDZ domain of Dishevelled to a conserved internal sequence in the C-terminal region of Frizzled.
    Mol Cell. 2003 Nov;12(5):1251-60 PMID: 14636582
  45. Frizzled and Dfrizzled-2 function as redundant receptors for Wingless during Drosophila embryonic development.
    Development. 1999 Sep;126(18):4175-86 PMID: 10457026
  46. Planar polarity is positively regulated by casein kinase Iepsilon in Drosophila.
    Curr Biol. 2006 Jul 11;16(13):1329-36 PMID: 16824921
  47. Structural basis of the recognition of the dishevelled DEP domain in the Wnt signaling pathway.
    Nat Struct Biol. 2000 Dec;7(12):1178-84 PMID: 11101902
  48. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation.
    Science. 2007 Jun 15;316(5831):1619-22 PMID: 17569865
  49. Initiation of Wnt signaling: control of Wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions.
    Development. 2008 Jan;135(2):367-75 PMID: 18077588
  50. Frizzled signalling and cell polarisation in Drosophila and vertebrates.
    Development. 2003 Oct;130(19):4501-13 PMID: 12925579
Article Info
Journal
Developmental biology
Abbr.
Dev Biol
ISSN
1095-564X
Published
2011-12-01
Epub
2011-00-22
Pages
132-42
Language
English
Region
United States
NLM ID
0372762
PMCID
PMC3221411
Subset
IM
Grants
NEI NIH HHS · EY13256 · United States
NEI NIH HHS · R01 EY013256 · United States
NIGMS NIH HHS · R01 GM088202 · United States
NEI NIH HHS · R01 EY013256-10 · United States
NIGMS NIH HHS · GM088202 · United States
NEI NIH HHS · R01 EY013256-11 · United States
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