The tumor suppressor protein DLC1 is regulated by PKD-mediated GAP domain phosphorylation

Experimental Cell Research

Volumn 317, Issue 4, 2011, Pages 496-503

  Scholz, Rolf Peter ^a   Gustafsson, Johan O R ^b   Hoffmann, Peter ^b   Jaiswal, Mamta ^c   Ahmadian, Mohammed Reza ^c   Eisler, Stephan A ^a   Erlmann, Patrik ^a   Schmid, Simone ^a   Hausser, Angelika ^a   Olayioye, Monilola A ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Deleted in liver cancer 1 (DLC1); GTPase activating protein; Protein kinase D (PKD); Rho signaling; Serine phosphorylation; Tumor suppressor

Indexed keywords

ALANINE; DELETED IN LIVER CANCER 1 PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN KINASE D; SERINE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL FUNCTION; CELL STRAIN HEK293; CELL STRAIN MCF 7; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; IN VITRO STUDY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WILD TYPE;

EID: 78651415449     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.11.003     Document Type: Article

References (29)

1. Durkin M.E., Yuan B.Z., Zhou X., Zimonjic D.B., Lowy D.R., Thorgeirsson S.S., Popescu N.C. DLC-1:a Rho GTPase-activating protein and tumour suppressor. J. Cell. Mol. Med. 2007, 11:1185-1207.
2. Goodison S., Yuan J., Sloan D., Kim R., Li C., Popescu N.C., Urquidi V. The RhoGAP protein DLC-1 functions as a metastasis suppressor in breast cancer cells. Cancer Res. 2005, 65:6042-6053.
3. Xue W., Krasnitz A., Lucito R., Sordella R., Vanaelst L., Cordon-Cardo C., Singer S., Kuehnel F., Wigler M., Powers S., Zender L., Lowe S.W. DLC1 is a chromosome 8p tumor suppressor whose loss promotes hepatocellular carcinoma. Genes Dev. 2008, 22:1439-1444.
4. Healy K.D., Hodgson L., Kim T.Y., Shutes A., Maddileti S., Juliano R.L., Hahn K.M., Harden T.K., Bang Y.J., Der C.J. DLC-1 suppresses non-small cell lung cancer growth and invasion by RhoGAP-dependent and independent mechanisms. Mol. Carcinog. 2008, 47:326-337.
5. Jaffe A.B., Hall A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 2005, 21:247-269.
6. Wong C.M., Yam J.W., Ching Y.P., Yau T.O., Leung T.H., Jin D.Y., Ng I.O. Rho GTPase-activating protein deleted in liver cancer suppresses cell proliferation and invasion in hepatocellular carcinoma. Cancer Res. 2005, 65:8861-8868.
7. Holeiter G., Heering J., Erlmann P., Schmid S., Jahne R., Olayioye M.A. Deleted in liver cancer 1 controls cell migration through a Dia1-dependent signaling pathway. Cancer Res. 2008, 68:8743-8751.
8. Liao Y.C., Shih Y.P., Lo S.H. Mutations in the focal adhesion targeting region of deleted in liver cancer-1 attenuate their expression and function. Cancer Res. 2008, 68:7718-7722.
9. Hers I., Wherlock M., Homma Y., Yagisawa H., Tavare J.M. Identification of p122RhoGAP (deleted in liver cancer-1) Serine 322 as a substrate for protein kinase B and ribosomal S6 kinase in insulin-stimulated cells. J. Biol. Chem. 2006, 281:4762-4770.
10. Scholz R.P., Regner J., Theil A., Erlmann P., Holeiter G., Jahne R., Schmid S., Hausser A., Olayioye M.A. DLC1 interacts with 14-3-3 proteins to inhibit RhoGAP activity and block nucleocytoplasmic shuttling. J. Cell Sci. 2009, 122:92-102.
11. Hausser A., Link G., Bamberg L., Burzlaff A., Lutz S., Pfizenmaier K., Johannes F.J. Structural requirements for localization and activation of protein kinase C mu (PKC mu) at the Golgi compartment. J. Cell Biol. 2002, 156:65-74.
12. Olayioye M.A., Buchholz M., Schmid S., Schoffler P., Hoffmann P., Pomorski T. Phosphorylation of StarD10 on serine 284 by casein kinase II modulates its lipid transfer activity. J. Biol. Chem. 2007, 282:22492-22498.
13. Sykora C., Hoffmann R., Hoffmann P. Enrichment of multiphosphorylated peptides by immobilized metal affinity chromatography using Ga(III)- and Fe(III)-complexes. Protein Pept. Lett. 2007, 14:489-496.
14. Condina M.R., Guthridge M.A., McColl S.R., Hoffmann P. A sensitive magnetic bead method for the detection and identification of tyrosine phosphorylation in proteins by MALDI-TOF/TOF MS. Proteomics 2009, 9:3047-3057.
15. Eberth A., Lundmark R., Gremer L., Dvorsky R., Koessmeier K.T., McMahon H.T., Ahmadian M.R. A BAR domain-mediated autoinhibitory mechanism for RhoGAPs of the GRAF family. Biochem. J. 2009, 417:371-377.
16. Erlmann P., Schmid S., Horenkamp F.A., Geyer M., Pomorski T.G., Olayioye M.A. DLC1 activation requires lipid interaction through a polybasic region preceding the RhoGAP domain. Mol. Biol. Cell 2009, 20:4400-4411.
17. Cowell C.F., Yan I.K., Eiseler T., Leightner A.C., Doppler H., Storz P. Loss of cell-cell contacts induces NF-kappaB via RhoA-mediated activation of protein kinase D1. J. Cell. Biochem. 2009, 106:714-728.
18. Yuan J., Slice L.W., Rozengurt E. Activation of protein kinase D by signaling through Rho and the alpha subunit of the heterotrimeric G protein G13. J. Biol. Chem. 2001, 276:38619-38627.
19. Wong C.C., Wong C.M., Ko F.C., Chan L.K., Ching Y.P., Yam J.W., Ng I.O. Deleted in liver cancer 1 (DLC1) negatively regulates Rho/ROCK/MLC pathway in hepatocellular carcinoma. PLoS ONE 2008, 3:e2779.
20. Kim T.Y., Healy K.D., Der C.J., Sciaky N., Bang Y.J., Juliano R.L. Effects of structure of Rho GTPase-activating protein DLC-1 on cell morphology and migration. J. Biol. Chem. 2008, 283:32762-32770.
21. Minoshima Y., Kawashima T., Hirose K., Tonozuka Y., Kawajiri A., Bao Y.C., Deng X., Tatsuka M., Narumiya S., May W.S., Nosaka T., Semba K., Inoue T., Satoh T., Inagaki M., Kitamura T. Phosphorylation by aurora B converts MgcRacGAP to a RhoGAP during cytokinesis. Dev. Cell 2003, 4:549-560.
22. Liao Y.C., Si L., deVere White R.W., Lo S.H. The phosphotyrosine-independent interaction of DLC-1 and the SH2 domain of cten regulates focal adhesion localization and growth suppression activity of DLC-1. J. Cell Biol. 2007, 176:43-49.
23. Qian X., Li G., Asmussen H.K., Asnaghi L., Vass W.C., Braverman R., Yamada K.M., Popescu N.C., Papageorge A.G., Lowy D.R. Oncogenic inhibition by a deleted in liver cancer gene requires cooperation between tensin binding and Rho-specific GTPase-activating protein activities. Proc. Natl Acad. Sci. USA 2007, 104:9012-9017.
24. Yang X.Y., Guan M., Vigil D., Der C.J., Lowy D.R., Popescu N.C. p120Ras-GAP binds the DLC1 Rho-GAP tumor suppressor protein and inhibits its RhoA GTPase and growth-suppressing activities. Oncogene 2009, 28:1401-1409.
25. Wang Q.J. PKD at the crossroads of DAG and PKC signaling. Trends Pharmacol. Sci. 2006, 27:317-323.
26. Eiseler T., Hausser A., De Kimpe L., Van Lint J., Pfizenmaier K. Protein kinase D controls actin polymerization and cell motility through phosphorylation of cortactin. J. Biol. Chem. 2010, 285:18672-18683.
27. Peterburs P., Heering J., Link G., Pfizenmaier K., Olayioye M.A., Hausser A. Protein kinase D regulates cell migration by direct phosphorylation of the cofilin phosphatase slingshot 1 like. Cancer Res. 2009, 69:5634-5638.
28. Eiseler T., Doppler H., Yan I.K., Goodison S., Storz P. Protein kinase D1 regulates matrix metalloproteinase expression and inhibits breast cancer cell invasion. Breast Cancer Res. 2009, 11:R13.
29. Jaggi M., Rao P.S., Smith D.J., Wheelock M.J., Johnson K.R., Hemstreet G.P., Balaji K.C. E-cadherin phosphorylation by protein kinase D1/protein kinase C{mu} is associated with altered cellular aggregation and motility in prostate cancer. Cancer Res. 2005, 65:483-492.