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PMID: 19371734 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Suppressor of Fused inhibits mammalian Hedgehog signaling in the absence of cilia.

Developmental biology ·Vol. 330 ·No. 2 ·2009-06-15 ·Pages 452-60

Jia J, Kolterud A, Zeng H, Hoover A, Teglund S, Toftgård R, Liu A

Abstract

The Hedgehog (Hh) family of secreted proteins regulates mammalian development and cancer formation through Gli transcription factors, which exist in both activator and repressor forms. In vertebrates, the primary cilia play an essential role in Hh signal transduction and are required for both the activator and repressor activities of Gli proteins. In the current study, we demonstrate that mouse Suppressor of Fused (Sufu) interacts with Gli proteins and inhibits Gli activator activity in the absence of cilia. Removal of Sufu in both Smoothened (Smo) and Ift88 mutants, respectively, leads to full activation of Hh signaling, suggesting that Smo-mediated repression of Sufu, but not the inhibitory function of Sufu, requires cilia. Finally, we show that Sufu is important for proper activator/repressor ratio of Gli3 protein in mice, both in the presence and absence of cilia.

MeSH Terms
Animals Blotting, Western Cells, Cultured Cilia/metabolism Genes, Reporter Hedgehog Proteins/antagonists & inhibitors,metabolism Immunohistochemistry Immunoprecipitation Mice Mice, Mutant Strains Repressor Proteins/physiology Signal Transduction
Chemicals
Hedgehog Proteins Repressor Proteins Sufu protein, mouse
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Jia Jinping
Department of Biology, Eberly College of Science, The Pennsylvania State University, 201 Life Science Building, University Park, PA 16802, USA.
Kolterud Asa
Zeng Huiqing
Hoover Amber
Teglund Stephan
Toftgård Rune
Liu Aimin
References (35)
35 references, click to expand
  1. Smoothened mutants reveal redundant roles for Shh and Ihh signaling including regulation of L/R symmetry by the mouse node.
    Cell. 2001 Jul 27;106(2):781-92 PMID: 11517919
  2. Cilia and Hedgehog responsiveness in the mouse.
    Proc Natl Acad Sci U S A. 2005 Aug 9;102(32):11325-30 PMID: 16061793
  3. Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia.
    Mol Biol Cell. 2001 Mar;12(3):589-99 PMID: 11251073
  4. The Meckel-Gruber Syndrome proteins MKS1 and meckelin interact and are required for primary cilium formation.
    Hum Mol Genet. 2007 Jan 15;16(2):173-86 PMID: 17185389
  5. Characterization of the physical interaction of Gli proteins with SUFU proteins.
    J Biol Chem. 2003 Feb 14;278(7):5116-22 PMID: 12426310
  6. Hedgehog signalling in the mouse requires intraflagellar transport proteins.
    Nature. 2003 Nov 6;426(6962):83-7 PMID: 14603322
  7. Hedgehog stimulates maturation of Cubitus interruptus into a labile transcriptional activator.
    Nature. 1998 Dec 24-31;396(6713):749-53 PMID: 9874371
  8. An absolute requirement for Cubitus interruptus in Hedgehog signaling.
    Development. 2001 Mar;128(5):733-42 PMID: 11171398
  9. Vertebrate homologs of Drosophila suppressor of fused interact with the gli family of transcriptional regulators.
    Dev Biol. 1999 Aug 15;212(2):323-36 PMID: 10433824
  10. The negative regulator of Gli, Suppressor of fused (Sufu), interacts with SAP18, Galectin3 and other nuclear proteins.
    Biochem J. 2004 Mar 1;378(Pt 2):353-62 PMID: 14611647
  11. Intraflagellar transport, cilia, and mammalian Hedgehog signaling: analysis in mouse embryonic fibroblasts.
    Dev Dyn. 2008 Aug;237(8):2030-8 PMID: 18488998
  12. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3.
    Dev Cell. 2004 Jan;6(1):103-15 PMID: 14723851
  13. Altered neural cell fates and medulloblastoma in mouse patched mutants.
    Science. 1997 Aug 22;277(5329):1109-13 PMID: 9262482
  14. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb.
    Cell. 2000 Feb 18;100(4):423-34 PMID: 10693759
  15. Genetic elimination of Suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway.
    Dev Cell. 2006 Feb;10(2):187-97 PMID: 16459298
  16. Sonic hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation.
    Mol Cell Biol. 2006 May;26(9):3365-77 PMID: 16611981
  17. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling.
    Development. 1999 Sep;126(17):3915-24 PMID: 10433919
  18. Mammalian suppressor-of-fused modulates nuclear-cytoplasmic shuttling of Gli-1.
    Nat Cell Biol. 1999 Sep;1(5):312-9 PMID: 10559945
  19. Divergence of hedgehog signal transduction mechanism between Drosophila and mammals.
    Dev Cell. 2006 Feb;10(2):177-86 PMID: 16459297
  20. A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro.
    Development. 1997 Apr;124(7):1313-22 PMID: 9118802
  21. Characterization of the human suppressor of fused, a negative regulator of the zinc-finger transcription factor Gli.
    J Cell Sci. 1999 Dec;112 ( Pt 23):4437-48 PMID: 10564661
  22. Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function.
    PLoS Genet. 2005 Oct;1(4):e53 PMID: 16254602
  23. Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network.
    Development. 2008 Aug;135(15):2489-503 PMID: 18621990
  24. Suppressor of fused regulates Gli activity through a dual binding mechanism.
    Mol Cell Biol. 2004 Oct;24(19):8627-41 PMID: 15367681
  25. Patched1 regulates hedgehog signaling at the primary cilium.
    Science. 2007 Jul 20;317(5836):372-6 PMID: 17641202
  26. Vertebrate Smoothened functions at the primary cilium.
    Nature. 2005 Oct 13;437(7061):1018-21 PMID: 16136078
  27. Communicating with Hedgehogs.
    Nat Rev Mol Cell Biol. 2005 Apr;6(4):306-17 PMID: 15803137
  28. Direct interaction with Hoxd proteins reverses Gli3-repressor function to promote digit formation downstream of Shh.
    Development. 2004 May;131(10):2339-47 PMID: 15102708
  29. Suppressor of Fused represses Gli-mediated transcription by recruiting the SAP18-mSin3 corepressor complex.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5442-7 PMID: 11960000
  30. The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination.
    Development. 2000 Jun;127(11):2347-55 PMID: 10804177
  31. Mouse suppressor of fused is a negative regulator of sonic hedgehog signaling and alters the subcellular distribution of Gli1.
    Curr Biol. 1999 Oct 7;9(19):1119-22 PMID: 10531011
  32. C2cd3 is required for cilia formation and Hedgehog signaling in mouse.
    Development. 2008 Dec;135(24):4049-58 PMID: 19004860
  33. Mouse intraflagellar transport proteins regulate both the activator and repressor functions of Gli transcription factors.
    Development. 2005 Jul;132(13):3103-11 PMID: 15930098
  34. Characterization of Suppressor of fused, a complete suppressor of the fused segment polarity gene of Drosophila melanogaster.
    Genetics. 1992 Nov;132(3):725-36 PMID: 1468628
  35. Cardiac and CNS defects in a mouse with targeted disruption of suppressor of fused.
    Development. 2005 Oct;132(19):4407-17 PMID: 16155214
Article Info
Journal
Developmental biology
Abbr.
Dev Biol
ISSN
1095-564X
Published
2009-06-15
Epub
2009-00-14
Pages
452-60
Language
English
Region
United States
NLM ID
0372762
PMCID
PMC2687323
Subset
IM
Grants
NIAMS NIH HHS · AR47898 · United States
NCI NIH HHS · U01 CA105491 · United States
NIAMS NIH HHS · P01 AR047898-05 · United States
NIAMS NIH HHS · P01 AR047898 · United States
NCI NIH HHS · U01 CA105491-06 · United States
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