The NDR Family Kinase NdrA of Dictyostelium Localizes to the Centrosome and Is Required for Efficient Phagocytosis

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Volumn 12, Issue 3, 2011, Pages 301-312

  Kastner, Peter M ^a,b   Schleicher, Michael ^a   Müller Taubenberger, Annette ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Centrosome; Dictyostelium discoideum; Mitosis; Mob1; Phagocytic cup

Indexed keywords

MEMBRANE PROTEIN; PROTEIN EMPC; PROTEIN NDRA; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; CENTROSOME; DICTYOSTELIUM DISCOIDEUM; GENE EXPRESSION PROFILING; HOMOLOGOUS RECOMBINATION; MITOSIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROPHASE; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

CELL CYCLE; CENTROSOME; DICTYOSTELIUM; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; PHAGOCYTOSIS; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTOZOAN PROTEINS;

EID: 79751472083     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2010.01147.x     Document Type: Article

References (53)

1. Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem 2009;78:857-902.
2. Ravanel K, de Chassey B, Cornillon S, Benghezal M, Zulianello L, Gebbie L, Letourneur F, Cosson P. Membrane sorting in the endocytic and phagocytic pathway of Dictyostelium discoideum. Eur J Cell Biol 2001;80:754-764.
3. Huynh KK, Kay JG, Stow JL, Grinstein S. Fusion, fission, and secretion during phagocytosis. Physiology (Bethesda) 2007;22:366-372.
4. Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, Gagnon E, Sadoul R, Rondeau C, Desjardins M. The phagosome proteome: insight into phagosome functions. J Cell Biol 2001;152:165-180.
5. Gotthardt D, Warnatz HJ, Henschel O, Bruckert F, Schleicher M, Soldati T. High-resolution dissection of phagosome maturation reveals distinct membrane trafficking phases. Mol Biol Cell 2002;13:3508-3520.
6. Gotthardt D, Blancheteau V, Bosserhoff A, Ruppert T, Delorenzi M, Soldati T. Proteomics fingerprinting of phagosome maturation and evidence for the role of a Galpha during uptake. Mol Cell Proteomics 2006;5:2228-2243.
7. Konzok A, Weber I, Simmeth E, Hacker U, Maniak M, Müller-Taubenberger A. DAip1, a Dictyostelium homologue of the yeast actin-interacting protein 1, is involved in endocytosis, cytokinesis, and motility. J Cell Biol 1999;146:453-464.
8. Janssen KP, Schleicher M. Dictyostelium discoideum: a genetic model system for the study of professional phagocytes. Profilin, phosphoinositides and the lmp gene family in Dictyostelium. Biochim Biophys Acta 2001;1525:228-233.
9. Maniak M, Rauchenberger R, Albrecht R, Murphy J, Gerisch G. Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein tag. Cell 1995;83:915-924.
10. Lindmo K, Stenmark H. Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Sci 2006;119:605-614.
11. Clarke M, Maddera L, Engel U, Gerisch G. Retrieval of the vacuolar H-ATPase from phagosomes revealed by live cell imaging. PLoS One 2010;5:e8585.
12. Fang J, Brzostowski JA, Ou S, Isik N, Nair V, Jin T. A vesicle surface tyrosine kinase regulates phagosome maturation. J Cell Biol 2007;178:411-423.
13. Pearce LR, Komander D, Alessi DR. The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 2010;11:9-22.
14. Hergovich A, Stegert MR, Schmitz D, Hemmings BA. NDR kinases regulate essential cell processes from yeast to humans. Nat Rev Mol Cell Biol 2006;7:253-264.
15. Tamaskovic R, Bichsel SJ, Hemmings BA. NDR family of AGC kinases-essential regulators of the cell cycle and morphogenesis. FEBS Lett 2003;546:73-80.
16. Goldberg JM, Manning G, Liu A, Fey P, Pilcher KE, Xu Y, Smith JL. The Dictyostelium kinome-analysis of the protein kinases from a simple model organism. PLoS Genet 2006;2:e38.
17. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 1988;16:10881-10890.
18. Hirabayashi S, Nakagawa K, Sumita K, Hidaka S, Kawai T, Ikeda M, Kawata A, Ohno K, Hata Y. Threonine 74 of MOB1 is a putative key phosphorylation site by MST2 to form the scaffold to activate nuclear Dbf2-related kinase 1. Oncogene 2008;27:4281-4292.
19. Faix J, Kreppel L, Shaulsky G, Schleicher M, Kimmel AR. A rapid and efficient method to generate multiple gene disruptions in Dictyostelium discoideum using a single selectable marker and the Cre-loxP system. Nucleic Acids Res 2004;32:e143.
20. Bretschneider T, Diez S, Anderson K, Heuser J, Clarke M, Müller-Taubenberger A, Köhler J, Gerisch G. Dynamic actin patterns and Arp2/3 assembly at the substrate-attached surface of motile cells. Curr Biol 2004;14:1-10.
21. Clarke M, Müller-Taubenberger A, Anderson KI, Engel U, Gerisch G. Mechanically induced actin-mediated rocketing of phagosomes. Mol Biol Cell 2006;17:4866-4875.
22. Hacker U, Albrecht R, Maniak M. Fluid-phase uptake by macropinocytosis in Dictyostelium. J Cell Sci 1997;110:105-112.
23. Gräf R, Daunderer C, Schliwa M. Dictyostelium DdCP224 is a microtubule-associated protein and a permanent centrosomal resident involved in centrosome duplication. J Cell Sci 2000;113: 1747-1758.
24. Hergovich A, Lamla S, Nigg EA, Hemmings BA. Centrosome-associated NDR kinase regulates centrosome duplication. Mol Cell 2007;25:625-634.
25. Stegert MR, Hergovich A, Tamaskovic R, Bichsel SJ, Hemmings BA. Regulation of NDR protein kinase by hydrophobic motif phosphorylation mediated by the mammalian Ste20-like kinase MST3. Mol Cell Biol 2005;25:11019-11029.
26. He Y, Emoto K, Fang X, Ren N, Tian X, Jan YN, Adler PN. Drosophila Mob family proteins interact with the related tricornered (Trc) and warts (Wts) kinases. Mol Biol Cell 2005;16:4139-4152.
27. Bichsel SJ, Tamaskovic R, Stegert MR, Hemmings BA. Mechanism of activation of NDR (nuclear Dbf2-related) protein kinase by the hMOB1 protein. J Biol Chem 2004;279:35228-35235.
28. Hou MC, Salek J, McCollum D. Mob1p interacts with the Sid2p kinase and is required for cytokinesis in fission yeast. Curr Biol 2000;10:619-622.
29. Hergovich A, Bichsel SJ, Hemmings BA. Human NDR kinases are rapidly activated by MOB proteins through recruitment to the plasma membrane and phosphorylation. Mol Cell Biol 2005;25:8259-8272.
30. Rot G, Parikh A, Curk T, Kuspa A, Shaulsky G, Zupan B. dictyExpress: a Dictyostelium discoideum gene expression database with an explorative data analysis web-based interface. BMC Bioinformatics 2009;10:265.
31. Eichinger L, Bähler M, Dietz M, Eckerskorn C, Schleicher M. Characterization and cloning of a Dictyostelium Ste20-like protein kinase that phosphorylates the actin-binding protein severin. J Biol Chem 1998;273:12952-12959.
32. Arasada R, Son H, Ramalingam N, Eichinger L, Schleicher M, Rohlfs M. Characterization of the Ste20-like kinase Krs1 of Dictyostelium discoideum. Eur J Cell Biol 2006;85:1059-1068.
33. Blum R, Feick P, Puype M, Vandekerckhove J, Klengel R, Nastainczyk W, Schulz I. Tmp21 and p24A, two type I proteins enriched in pancreatic microsomal membranes, are members of a protein family involved in vesicular trafficking. J Biol Chem 1996;271:17183-17189.
34. Charette SJ, Mercanti V, Letourneur F, Bennett N, Cosson P. A role for adaptor protein-3 complex in the organization of the endocytic pathway in Dictyostelium. Traffic 2006;7:1528-1538.
35. Lee WL, Mason D, Schreiber AD, Grinstein S. Quantitative analysis of membrane remodeling at the phagocytic cup. Mol Biol Cell 2007;18:2883-2892.
36. Swanson JA. Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 2008;9:639-649.
37. Czibener C, Sherer NM, Becker SM, Pypaert M, Hui E, Chapman ER, Mothes W, Andrews NW. Ca2+ and synaptotagmin VII-dependent delivery of lysosomal membrane to nascent phagosomes. J Cell Biol 2006;174:997-1007.
38. Bajno L, Peng XR, Schreiber AD, Moore HP, Trimble WS, Grinstein S. Focal exocytosis of VAMP3-containing vesicles at sites of phagosome formation. J Cell Biol 2000;149:697-706.
39. Gagnon E, Duclos S, Rondeau C, Chevet E, Cameron PH, Steele-Mortimer O, Paiement J, Bergeron JJ, Desjardins M. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 2002;110:119-131.
40. Strating JR, Martens GJ. The p24 family and selective transport processes at the ER-Golgi interface. Biol Cell 2009;101:495-509.
41. Jansen JM, Barry MF, Yoo CK, Weiss EL. Phosphoregulation of Cbk1 is critical for RAM network control of transcription and morphogenesis. J Cell Biol 2006;175:755-766.
42. Dohrmann PR, Voth WP, Stillman DJ. Role of negative regulation in promoter specificity of the homologous transcriptional activators Ace2p and Swi5p. Mol Cell Biol 1996;16:1746-1758.
43. Kurischko C, Kuravi VK, Wannissorn N, Nazarov PA, Husain M, Zhang C, Shokat KM, McCaffery JM, Luca FC. The yeast LATS/Ndr kinase Cbk1 regulates growth via Golgi-dependent glycosylation and secretion. Mol Biol Cell 2008;19:5559-5578.
44. Ziv C, Kra-Oz G, Gorovits R, Marz S, Seiler S, Yarden O. Cell elongation and branching are regulated by differential phosphorylation states of the nuclear Dbf2-related kinase COT1 in Neurospora crassa. Mol Microbiol 2009;74:974-989.
45. Jenne N, Rauchenberger R, Hacker U, Kast T, Maniak M. Targeted gene disruption reveals a role for vacuolin B in the late endocytic pathway and exocytosis. J Cell Sci 1998;111:61-70.
46. Rivero F, Maniak M. Quantitative and microscopic methods for studying the endocytic pathway. Methods Mol Biol 2006;346:423-438.
47. Gerisch G, Müller-Taubenberger A. GFP-fusion proteins as fluorescent reporters to study organelle and cytoskeleton dynamics in chemotaxis and phagocytosis. Methods Enzymol 2003;361:320-337.
48. Gräf R, Daunderer C, Schliwa M. Cell cycle-dependent localization of monoclonal antibodies raised against isolated Dictyostelium centrosomes. Biol Cell 1999;91:471-477.
49. Schulz I, Reinders Y, Sickmann A, Gräf R. An improved method for Dictyostelium centrosome isolation. Methods Mol Biol 2006;346:479-489.
50. Müller-Taubenberger A, Ishikawa-Ankerhold HC, Kastner PM, Burghardt E, Gerisch G. The STE group kinase SepA controls cleavage furrow formation in Dictyostelium. Cell Motil Cytoskeleton 2009;66:929-939.
51. Mondal S, Bakthavatsalam D, Steimle P, Gassen B, Rivero F, Noegel AA. Linking Ras to myosin function: RasGEF Q, a Dictyostelium exchange factor for RasB, affects myosin II functions. J Cell Biol 2008;181:747-760.
52. Sasaki AT, Firtel RA. Spatiotemporal regulation of Ras-GTPases during chemotaxis. Methods Mol Biol 2009;571:333-348.
53. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999;20:3551-3567.