Home LiteratureArticle Details
PMID: 15591127 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The tricornered Ser/Thr protein kinase is regulated by phosphorylation and interacts with furry during Drosophila wing hair development.

Molecular biology of the cell ·Vol. 16 ·No. 2 ·2005-02-00 ·Pages 689-700

He Y, Fang X, Emoto K, Jan YN, Adler PN

Abstract

The Trc/Ndr/Sax1/Cbk1 family of ser/thr kinases plays a key role in the morphogenesis of polarized cell structures in flies, worms, and yeast. Tricornered (Trc), the Drosophila nuclear Dbf2-related (Ndr) serine/threonine protein kinase, is required for the normal morphogenesis of epidermal hairs, bristles, laterals, and dendrites. We obtained in vivo evidence that Trc function was regulated by phosphorylation and that mutations in key regulatory sites resulted in dominant negative alleles. We found that wild-type, but not mutant Trc, is found in growing hairs, and we failed to detect Trc in pupal wing nuclei, implying that in this developmental context Trc functions in the cytoplasm. The furry gene and its homologues in yeast and Caenorhabditis elegans have previously been implicated as being essential for the function of the Ndr kinase family. We found that Drosophila furry (Fry) also is found in growing hairs, that its subcellular localization is dependent on Trc function, and that it can be coimmunoprecipitated with Trc. Our data suggest a feedback mechanism involving Trc activity regulates the accumulation of Fry in developing hairs.

MeSH Terms
Animals Cells, Cultured Drosophila/cytology,enzymology,genetics,growth & development Drosophila Proteins/genetics,metabolism Gene Expression Regulation, Developmental Genes, Insect Hair/growth & development,metabolism Immunohistochemistry Microscopy, Confocal Models, Biological Mutation Nuclear Proteins/genetics,metabolism Phosphorylation Protein Serine-Threonine Kinases/genetics,metabolism Pupa Signal Transduction Transfection Wings, Animal/growth & development,metabolism
Chemicals
Drosophila Proteins Nuclear Proteins fry protein, Drosophila trc protein, Drosophila Protein Serine-Threonine Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
He Ying
Department of Biology, Center for Morphogenesis and Regenerative Medicine and Cancer Center, University of Virginia, Charlottesville, VA 22903, USA.
Fang Xiaolan
Emoto Kazuo
Jan Yuh-Nung
Adler Paul N
References (36)
36 references, click to expand
  1. The Cbk1p pathway is important for polarized cell growth and cell separation in Saccharomyces cerevisiae.
    Mol Cell Biol. 2001 Apr;21(7):2449-62 PMID: 11259593
  2. Ndr protein kinase is regulated by phosphorylation on two conserved sequence motifs.
    J Biol Chem. 1999 Nov 26;274(48):33847-50 PMID: 10567341
  3. Cellular mechanisms in the development of the Drosophila arista.
    Mech Dev. 2001 Jun;104(1-2):69-78 PMID: 11404081
  4. Protein kinase Cdc15 activates the Dbf2-Mob1 kinase complex.
    Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7325-30 PMID: 11404483
  5. The furry gene of Drosophila is important for maintaining the integrity of cellular extensions during morphogenesis.
    Development. 2001 Jul;128(14):2793-802 PMID: 11526084
  6. Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates.
    Cell. 2001 Dec 14;107(6):739-50 PMID: 11747810
  7. Control of actin reorganization by Slingshot, a family of phosphatases that dephosphorylate ADF/cofilin.
    Cell. 2002 Jan 25;108(2):233-46 PMID: 11832213
  8. Pag1p, a novel protein associated with protein kinase Cbk1p, is required for cell morphogenesis and proliferation in Saccharomyces cerevisiae.
    Mol Biol Cell. 2002 Feb;13(2):503-14 PMID: 11854408
  9. Rac function and regulation during Drosophila development.
    Nature. 2002 Mar 28;416(6879):438-42 PMID: 11919634
  10. Cbk1p, a protein similar to the human myotonic dystrophy kinase, is essential for normal morphogenesis in Saccharomyces cerevisiae.
    EMBO J. 2000 Sep 1;19(17):4524-32 PMID: 10970846
  11. Neuronal cell shape and neurite initiation are regulated by the Ndr kinase SAX-1, a member of the Orb6/COT-1/warts serine/threonine kinase family.
    Mol Biol Cell. 2000 Sep;11(9):3177-90 PMID: 10982409
  12. The tricornered gene, which is required for the integrity of epidermal cell extensions, encodes the Drosophila nuclear DBF2-related kinase.
    Genetics. 2000 Dec;156(4):1817-28 PMID: 11102376
  13. The Saccharomyces cerevisiae Mob2p-Cbk1p kinase complex promotes polarized growth and acts with the mitotic exit network to facilitate daughter cell-specific localization of Ace2p transcription factor.
    J Cell Biol. 2002 Sep 2;158(5):885-900 PMID: 12196508
  14. Fission yeast Mor2/Cps12, a protein similar to Drosophila Furry, is essential for cell morphogenesis and its mutation induces Wee1-dependent G(2) delay.
    EMBO J. 2002 Sep 16;21(18):4863-74 PMID: 12234926
  15. Mechanism of Ca2+-mediated regulation of NDR protein kinase through autophosphorylation and phosphorylation by an upstream kinase.
    J Biol Chem. 2003 Feb 28;278(9):6710-8 PMID: 12493777
  16. NDR family of AGC kinases--essential regulators of the cell cycle and morphogenesis.
    FEBS Lett. 2003 Jul 3;546(1):73-80 PMID: 12829239
  17. Ral-GTPases: approaching their 15 minutes of fame.
    Trends Cell Biol. 2003 Aug;13(8):419-25 PMID: 12888294
  18. RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis.
    Mol Biol Cell. 2003 Sep;14(9):3782-803 PMID: 12972564
  19. Structure of the Ca2+/S100B/NDR kinase peptide complex: insights into S100 target specificity and activation of the kinase.
    Biochemistry. 2003 Dec 16;42(49):14416-26 PMID: 14661952
  20. Regulation of NDR2 protein kinase by multi-site phosphorylation and the S100B calcium-binding protein.
    J Biol Chem. 2004 May 28;279(22):23806-12 PMID: 15037617
  21. Human Mob proteins regulate the NDR1 and NDR2 serine-threonine kinases.
    J Biol Chem. 2004 Jun 4;279(23):24444-51 PMID: 15067004
  22. Mechanism of activation of NDR (nuclear Dbf2-related) protein kinase by the hMOB1 protein.
    J Biol Chem. 2004 Aug 20;279(34):35228-35 PMID: 15197186
  23. Control of dendritic branching and tiling by the Tricornered-kinase/Furry signaling pathway in Drosophila sensory neurons.
    Cell. 2004 Oct 15;119(2):245-56 PMID: 15479641
  24. Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function.
    Genes Dev. 1993 Jan;7(1):29-41 PMID: 8422986
  25. Analysis of genetic mosaics in developing and adult Drosophila tissues.
    Development. 1993 Apr;117(4):1223-37 PMID: 8404527
  26. Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells.
    J Cell Biol. 1993 Oct;123(1):209-21 PMID: 8408199
  27. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.
    Development. 1993 Jun;118(2):401-15 PMID: 8223268
  28. Molecular cloning and characterization of a conserved nuclear serine(threonine) protein kinase.
    Proc Natl Acad Sci U S A. 1995 May 23;92(11):5022-6 PMID: 7761441
  29. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification.
    FASEB J. 1995 May;9(8):576-96 PMID: 7768349
  30. Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila.
    J Cell Biol. 1996 Dec;135(5):1277-89 PMID: 8947551
  31. The role of RhoA in tissue polarity and Frizzled signalling.
    Nature. 1997 May 15;387(6630):292-5 PMID: 9153394
  32. Distinct roles for the actin and microtubule cytoskeletons in the morphogenesis of epidermal hairs during wing development in Drosophila.
    Mech Dev. 1998 Jan;70(1-2):181-92 PMID: 9510034
  33. Fission yeast orb6, a ser/thr protein kinase related to mammalian rho kinase and myotonic dystrophy kinase, is required for maintenance of cell polarity and coordinates cell morphogenesis with the cell cycle.
    Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7526-31 PMID: 9636183
  34. Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila.
    Cell. 1999 Jun 25;97(7):853-63 PMID: 10399914
  35. The Drosophila Ral GTPase regulates developmental cell shape changes through the Jun NH(2)-terminal kinase pathway.
    J Cell Biol. 1999 Jul 26;146(2):361-72 PMID: 10427090
  36. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton.
    Cell. 2001 Apr 6;105(1):81-91 PMID: 11301004
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2005-02-00
Epub
2004-00-09
Pages
689-700
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC545904
Subset
IM
Grants
NIGMS NIH HHS · R01 GM053498 · United States
NINDS NIH HHS · R01 NS040929 · United States
NIGMS NIH HHS · GM-53498 · United States
NINDS NIH HHS · R01NS40929 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]