Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Subscribe

Logo for

J. Cell Biol. 164 (7): 1009-1020

Copyright © 2004 by the Rockefeller University Press.

Article

YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3{zeta}

Christian Preisinger1, Benjamin Short1, Veerle De Corte2, Erik Bruyneel3, Alexander Haas1, Robert Kopajtich1, Jan Gettemans2, , and Francis A. Barr1

1 Max-Planck-Institute of Biochemistry, Martinsried, 82152 Germany
2 Department of Biochemistry and Molecular Biology, Faculty of Medicine and Health Sciences, Ghent University/Flanders Interuniversity Institute for Biotechnology (VIB09), B-9000 Ghent, Belgium
3 Laboratory of Experimental Cancerology, Department of Radiotherapy and Nuclear Medicine, Ghent University Hospital (1P7), B-9000 Ghent, Belgium

Address correspondence to Francis Barr, Max-Planck-Institute of Biochemistry, Am Klopferspitz 18, Martinsried, 82152 Germany. Tel.: 49-89-8578-3135. Fax: 49-89-8578-3102. email: barr{at}biochem.mpg.de

Abstract: The Golgi apparatus has long been suggested to be important for directing secretion to specific sites on the plasma membrane in response to extracellular signaling events. However, the mechanisms by which signaling events are coordinated with Golgi apparatus function remain poorly understood. Here, we identify a scaffolding function for the Golgi matrix protein GM130 that sheds light on how such signaling events may be regulated. We show that the mammalian Ste20 kinases YSK1 and MST4 target to the Golgi apparatus via the Golgi matrix protein GM130. In addition, GM130 binding activates these kinases by promoting autophosphorylation of a conserved threonine within the T-loop. Interference with YSK1 function perturbs perinuclear Golgi organization, cell migration, and invasion into type I collagen. A biochemical screen identifies 14-3-3{zeta} as a specific substrate for YSK1 that localizes to the Golgi apparatus, and potentially links YSK1 signaling at the Golgi apparatus with protein transport events, cell adhesion, and polarity complexes important for cell migration.

Key Words: Ste20 kinases; cell migration; polarity; collagen invasion; scaffold

C. Preisinger, B. Short, and V. De Corte contributed equally to this paper.

The online version of this article contains supplemental material.

Abbreviations used in this paper: MBP, myelin basic protein; MST, mammalian Ste20; siRNA, small interfering RNA; YSK1, yeast Sps1/Ste20-related kinase 1.

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
14-3-3{zeta} Protein Regulates Anterograde Transport of the Human {kappa}-Opioid Receptor (hKOPR).
J.-G. Li, C. Chen, P. Huang, Y. Wang, and L.-Y. Liu-Chen (2012)
J. Biol. Chem. 287, 37778-37792
   Abstract »    Full Text »    PDF »
STK25 Protein Mediates TrkA and CCM2 Protein-dependent Death in Pediatric Tumor Cells of Neural Origin.
B. Costa, M. J. Kean, V. Ast, J. D. R. Knight, A. Mett, Z. Levy, D. F. Ceccarelli, B. G. Badillo, R. Eils, R. Konig, et al. (2012)
J. Biol. Chem. 287, 29285-29289
   Abstract »    Full Text »    PDF »
GM130 gain-of-function induces cell pathology in a model of lysosomal storage disease.
E. Roy, J. Bruyere, P. Flamant, S. Bigou, J. Ausseil, S. Vitry, and J. M. Heard (2012)
Hum. Mol. Genet. 21, 1481-1495
   Abstract »    Full Text »    PDF »
Adaptor Protein Cerebral Cavernous Malformation 3 (CCM3) Mediates Phosphorylation of the Cytoskeletal Proteins Ezrin/Radixin/Moesin by Mammalian Ste20-4 to Protect Cells from Oxidative Stress.
M. Fidalgo, A. Guerrero, M. Fraile, C. Iglesias, C. M. Pombo, and J. Zalvide (2012)
J. Biol. Chem. 287, 11556-11565
   Abstract »    Full Text »    PDF »
Molecular Recognition of Leucine-Aspartate Repeat (LD) Motifs by the Focal Adhesion Targeting Homology Domain of Cerebral Cavernous Malformation 3 (CCM3).
X. Li, W. Ji, R. Zhang, E. Folta-Stogniew, W. Min, and T. J. Boggon (2011)
J. Biol. Chem. 286, 26138-26147
   Abstract »    Full Text »    PDF »
Structure-Function Analysis of Core STRIPAK Proteins: A SIGNALING COMPLEX IMPLICATED IN GOLGI POLARIZATION.
M. J. Kean, D. F. Ceccarelli, M. Goudreault, M. Sanches, S. Tate, B. Larsen, L. C. D. Gibson, W. B. Derry, I. C. Scott, L. Pelletier, et al. (2011)
J. Biol. Chem. 286, 25065-25075
   Abstract »    Full Text »    PDF »
Golgi Positioning.
S. Yadav and A. D. Linstedt (2011)
Cold Spring Harb Perspect Biol 3, a005322
   Abstract »    Full Text »    PDF »
Signalling to and from the secretory pathway.
H. Farhan and C. Rabouille (2011)
J. Cell Sci. 124, 171-180
   Abstract »    Full Text »    PDF »
The mitosis-to-interphase transition is coordinated by cross talk between the SIN and MOR pathways in Schizosaccharomyces pombe.
S. Ray, K. Kume, S. Gupta, W. Ge, M. Balasubramanian, D. Hirata, and D. McCollum (2010)
J. Cell Biol. 190, 793-805
   Abstract »    Full Text »    PDF »
MAPK signaling to the early secretory pathway revealed by kinase/phosphatase functional screening.
H. Farhan, M. W. Wendeler, S. Mitrovic, E. Fava, Y. Silberberg, R. Sharan, M. Zerial, and H.-P. Hauri (2010)
J. Cell Biol. 189, 997-1011
   Abstract »    Full Text »    PDF »
Regulation of O-glycosylation through Golgi-to-ER relocation of initiation enzymes.
D. J. Gill, J. Chia, J. Senewiratne, and F. Bard (2010)
J. Cell Biol. 189, 843-858
   Abstract »    Full Text »    PDF »
CCM3/PDCD10 stabilizes GCKIII proteins to promote Golgi assembly and cell orientation.
M. Fidalgo, M. Fraile, A. Pires, T. Force, C. Pombo, and J. Zalvide (2010)
J. Cell Sci. 123, 1274-1284
   Abstract »    Full Text »    PDF »
The Golgi and the centrosome: building a functional partnership.
C. Sutterlin and A. Colanzi (2010)
J. Cell Biol. 188, 621-628
   Abstract »    Full Text »    PDF »
Understanding protein phosphorylation on a systems level.
J. Lin, Z. Xie, H. Zhu, and J. Qian (2010)
Briefings in Functional Genomics
   Abstract »    Full Text »    PDF »
hnRNP A2 Regulates Alternative mRNA Splicing of TP53INP2 to Control Invasive Cell Migration.
K. Moran-Jones, J. Grindlay, M. Jones, R. Smith, and J. C. Norman (2009)
Cancer Res. 69, 9219-9227
   Abstract »    Full Text »    PDF »
Serine 58 of 14-3-3{zeta} Is a Molecular Switch Regulating ASK1 and Oxidant Stress-Induced Cell Death.
J. Zhou, Z. Shao, R. Kerkela, H. Ichijo, A. J. Muslin, C. Pombo, and T. Force (2009)
Mol. Cell. Biol. 29, 4167-4176
   Abstract »    Full Text »    PDF »
A Primary Role for Golgi Positioning in Directed Secretion, Cell Polarity, and Wound Healing.
S. Yadav, S. Puri, and A. D. Linstedt (2009)
Mol. Biol. Cell 20, 1728-1736
   Abstract »    Full Text »    PDF »
The mitotic spindle mediates inheritance of the Golgi ribbon structure.
J.-H. Wei and J. Seemann (2009)
J. Cell Biol. 184, 391-397
   Abstract »    Full Text »    PDF »
GM130-dependent Control of Cdc42 Activity at the Golgi Regulates Centrosome Organization.
A. Kodani, I. Kristensen, L. Huang, and C. Sutterlin (2009)
Mol. Biol. Cell 20, 1192-1200
   Abstract »    Full Text »    PDF »
A PP2A Phosphatase High Density Interaction Network Identifies a Novel Striatin-interacting Phosphatase and Kinase Complex Linked to the Cerebral Cavernous Malformation 3 (CCM3) Protein.
M. Goudreault, L. M. D'Ambrosio, M. J. Kean, M. J. Mullin, B. G. Larsen, A. Sanchez, S. Chaudhry, G. I. Chen, F. Sicheri, A. I. Nesvizhskii, et al. (2009)
Mol. Cell. Proteomics 8, 157-171
   Abstract »    Full Text »    PDF »
SOK1 Translocates from the Golgi to the Nucleus upon Chemical Anoxia and Induces Apoptotic Cell Death.
E. Nogueira, M. Fidalgo, A. Molnar, J. Kyriakis, T. Force, J. Zalvide, and C. M. Pombo (2008)
J. Biol. Chem. 283, 16248-16258
   Abstract »    Full Text »    PDF »
Coordination of Golgin Tethering and SNARE Assembly: GM130 BINDS SYNTAXIN 5 IN A p115-REGULATED MANNER.
A. Diao, L. Frost, Y. Morohashi, and M. Lowe (2008)
J. Biol. Chem. 283, 6957-6967
   Abstract »    Full Text »    PDF »
The Golgi Protein GM130 Regulates Centrosome Morphology and Function.
A. Kodani and C. Sutterlin (2008)
Mol. Biol. Cell 19, 745-753
   Abstract »    Full Text »    PDF »
The Ste20-like kinase SvkA of Dictyostelium discoideum is essential for late stages of cytokinesis.
M. Rohlfs, R. Arasada, P. Batsios, J. Janzen, and M. Schleicher (2007)
J. Cell Sci. 120, 4345-4354
   Abstract »    Full Text »    PDF »
Transcriptional Modulation of Genes Encoding Structural Characteristics of Differentiating Enterocytes During Development of a Polarized Epithelium In Vitro.
J. M. Halbleib, A. M. Saaf, P. O. Brown, and W. J. Nelson (2007)
Mol. Biol. Cell 18, 4261-4278
   Abstract »    Full Text »    PDF »
PDCD10 Interacts with Ste20-related Kinase MST4 to Promote Cell Growth and Transformation via Modulation of the ERK Pathway.
X. Ma, H. Zhao, J. Shan, F. Long, Y. Chen, Y. Chen, Y. Zhang, X. Han, and D. Ma (2007)
Mol. Biol. Cell 18, 1965-1978
   Abstract »    Full Text »    PDF »
The Biogenesis of the Golgi Ribbon: The Roles of Membrane Input from the ER and of GM130.
P. Marra, L. Salvatore, A. Mironov Jr, A. Di Campli, G. Di Tullio, A. Trucco, G. Beznoussenko, A. Mironov, and M. A. De Matteis (2007)
Mol. Biol. Cell 18, 1595-1608
   Abstract »    Full Text »    PDF »
Involvement of a Golgi-resident GPI-anchored Protein in Maintenance of the Golgi Structure.
X. Li, D. Kaloyanova, M. van Eijk, R. Eerland, G. van der Goot, V. Oorschot, J. Klumperman, F. Lottspeich, V. Starkuviene, F. T. Wieland, et al. (2007)
Mol. Biol. Cell 18, 1261-1271
   Abstract »    Full Text »    PDF »
Mitogen-activated Protein Kinase Kinase 1-dependent Golgi Unlinking Occurs in G2 Phase and Promotes the G2/M Cell Cycle Transition.
T. N. Feinstein and A. D. Linstedt (2007)
Mol. Biol. Cell 18, 594-604
   Abstract »    Full Text »    PDF »
Inhibition of Cell Migration by Autophosphorylated Mammalian Sterile 20-Like Kinase 3 (MST3) Involves Paxillin and Protein-tyrosine Phosphatase-PEST.
T.-J. Lu, W.-Y. Lai, C.-Y. F. Huang, W.-J. Hsieh, J.-S. Yu, Y.-J. Hsieh, W.-T. Chang, T.-H. Leu, W.-C. Chang, W.-J. Chuang, et al. (2006)
J. Biol. Chem. 281, 38405-38417
   Abstract »    Full Text »    PDF »
Role of tethering factors in secretory membrane traffic.
E. Sztul and V. Lupashin (2006)
Am J Physiol Cell Physiol 290, C11-C26
   Abstract »    Full Text »    PDF »
GMx33 Associates with the Trans-Golgi Matrix in a Dynamic Manner and Sorts within Tubules Exiting the Golgi.
C. M. Snyder, G. A. Mardones, M. S. Ladinsky, and K. E. Howell (2006)
Mol. Biol. Cell 17, 511-524
   Abstract »    Full Text »    PDF »
Regulation of NDR Protein Kinase by Hydrophobic Motif Phosphorylation Mediated by the Mammalian Ste20-Like Kinase MST3.
M. R. Stegert, A. Hergovich, R. Tamaskovic, S. J. Bichsel, and B. A. Hemmings (2005)
Mol. Cell. Biol. 25, 11019-11029
   Abstract »    Full Text »    PDF »
dGRASP Localization and Function in the Early Exocytic Pathway in Drosophila S2 Cells.
V. Kondylis, K. M. Spoorendonk, and C. Rabouille (2005)
Mol. Biol. Cell 16, 4061-4072
   Abstract »    Full Text »    PDF »
Convergence of Cell Cycle Regulation and Growth Factor Signals on GRASP65.
S.-i. Yoshimura, K. Yoshioka, F. A. Barr, M. Lowe, K. Nakayama, S. Ohkuma, and N. Nakamura (2005)
J. Biol. Chem. 280, 23048-23056
   Abstract »    Full Text »    PDF »
Golgi positioning: are we looking at the right MAP?.
F. A. Barr and J. Egerer (2005)
J. Cell Biol. 168, 993-998
   Abstract »    Full Text »    PDF »
Golgi polarization in a strong electric field.
J. Pu and M. Zhao (2005)
J. Cell Sci. 118, 1117-1128
   Abstract »    Full Text »    PDF »
mRNA Localization and ER-based Protein Sorting Mechanisms Dictate the Use of Transitional Endoplasmic Reticulum-Golgi Units Involved in Gurken Transport in Drosophila Oocytes.
B. Herpers and C. Rabouille (2004)
Mol. Biol. Cell 15, 5306-5317
   Abstract »    Full Text »    PDF »
The GTPase Arf1p and the ER to Golgi cargo receptor Erv14p cooperate to recruit the golgin Rud3p to the cis-Golgi.
A. K. Gillingham, A. H. Y. Tong, C. Boone, and S. Munro (2004)
J. Cell Biol. 167, 281-292
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882