Dictyostelium Sun1 is a dynamic membrane protein of both nuclear membranes and required for centrosomal association with clustered centromeres

European Journal of Cell Biology

Volumn 88, Issue 11, 2009, Pages 621-638

  Schulz, Irene ^a   Baumann, Otto ^a   Samereier, Matthias ^a   Zoglmeier, Christine ^a   Gräf, Ralph ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

Author keywords

Centrosome; Dictyostelium; Microtubules; Nuclear envelope; Sun family; Sun1

Indexed keywords

MEMBRANE PROTEIN; PROTEIN SUN1; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL NUCLEUS MEMBRANE; CENTROMERE; CENTROSOME; CONTROLLED STUDY; DICTYOSTELIUM; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; INTERPHASE; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; CELL CYCLE PROTEINS; CENTROMERE; DICTYOSTELIUM; GENOMIC INSTABILITY; MICROSCOPY, ELECTRON; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOSIS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PROTOZOAN PROTEINS;

DICTYOSTELIUM;

EID: 69949093384     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2009.06.003     Document Type: Article

References (45)

1. Barth C., Fraser D.J., and Fisher P.R. Co-insertional replication is responsible for tandem multimer formation during plasmid integration into the Dictyostelium genome. Plasmid 39 (1998) 141-153
2. Brito D.A., Strauss J., Magidson V., Tikhonenko I., Khodjakov A., and Koonce M.P. Pushing forces drive the comet-like motility of microtubule arrays in Dictyostelium. Mol. Biol. Cell 16 (2005) 3334-3340
3. Daunderer C., and Gräf R. Molecular analysis of the cytosolic Dictyostelium gamma-tubulin complex. Eur. J. Cell Biol. 81 (2002) 175-184
4. Daunderer C., Schliwa M., and Gräf R. Dictyostelium centrin-related protein (DdCrp), the most divergent member of the centrin family, possesses only two EF hands and dissociates from the centrosome during mitosis. Eur. J. Cell Biol. 80 (2001) 621-630
5. Doxsey S. Re-evaluating centrosome function. Nat. Rev. Mol. Cell Biol. 2 (2001) 688-698
6. Faix J., Kreppel L., Shaulsky G., Schleicher M., and Kimmel A.R. 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. 32 (2004) e143
7. Fukui Y., Yumura S., and Yumura T.K. Agar-overlay immunofluorescence: high resolution studies of cytoskeletal components and their changes during chemotaxis. Methods Cell Biol. 28 (1987) 347-356
8. Gräf R., Euteneuer U., Ueda M., and Schliwa M. Isolation of nucleation-competent centrosomes from Dictyostelium discoideum. Eur. J. Cell Biol. 76 (1998) 167-175
9. Gräf R., Daunderer C., and Schliwa M. Cell cycle-dependent localization of monoclonal antibodies raised against isolated Dictyostelium centrosomes. Biol. Cell 91 (1999) 471-477
10. Gräf R., Daunderer C., and Schliwa M. Dictyostelium DdCP224 is a microtubule-associated protein and a permanent centrosomal resident involved in centrosome duplication. J. Cell Sci. 113 (2000) 1747-1758
11. Gräf R., Euteneuer U., Ho T.H., and Rehberg M. Regulated expression of the centrosomal protein DdCP224 affects microtubule dynamics and reveals mechanisms for the control of supernumerary centrosome number. Mol. Biol. Cell 14 (2003) 4067-4074
12. Gräf R., Daunderer C., and Schulz I. Molecular and functional analysis of the Dictyostelium centrosome. Int. Rev. Cytol. 241 (2004) 155-202
13. Hestermann A., and Gräf R. The XMAP215-family protein DdCP224 is required for cortical interactions of microtubules. BMC Cell Biol. 5 (2004) 24
14. Jaspersen S.L., Martin A.E., Glazko G., Giddings Jr. T.H., Morgan G., Mushegian A., and Winey M. The Sad1-UNC-84 homology domain in Mps3 interacts with Mps2 to connect the spindle pole body with the nuclear envelope. J. Cell Biol. 174 (2006) 665-675
15. Kaller M., Euteneuer U., and Nellen W. Differential effects of heterochromatin protein 1 isoforms on mitotic chromosome distribution and growth in Dictyostelium discoideum. Eukaryot. Cell 5 (2006) 530-543
16. King M.C., Drivas T.G., and Blobel G. A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 134 (2008) 427-438
17. Kitanishi T., Shibaoka H., and Fukui Y. Disruption of microtubules and retardation of development of Dictyostelium with ethyl N-phenylcarbamate and thiabendazole. Protoplasma 120 (1984) 185-196
18. Koonce M.P., and Khodjakov A. Dynamic microtubules in Dictyostelium. J. Muscle Res. Cell Motil. 23 (2002) 613-619
19. Koonce M.P., Kohler J., Neujahr R., Schwartz J.M., Tikhonenko I., and Gerisch G. Dynein motor regulation stabilizes interphase microtubule arrays and determines centrosome position. EMBO J. 18 (1999) 6786-6792
20. Laube G., Roper J., Pitt J.C., Sewing S., Kistner U., Garner C.C., Pongs O., and Veh R.W. Ultrastructural localization of Shaker-related potassium channel subunits and synapse-associated protein 90 to septate-like junctions in rat cerebellar Pinceaux. Brain Res. Mol. Brain Res. 42 (1996) 51-61
21. Liu Q., Pante N., Misteli T., Elsagga M., Crisp M., Hodzic D., Burke B., and Roux K.J. Functional association of Sun1 with nuclear pore complexes. J. Cell Biol. 178 (2007) 785-798
22. Lu W., Gotzmann J., Sironi L., Jaeger V.M., Schneider M., Luke Y., Uhlen M., Szigyarto C.A., Brachner A., Ellenberg J., Foisner R., Noegel A.A., and Karakesisoglou I. Sun1 forms immobile macromolecular assemblies at the nuclear envelope. Biochim. Biophys. Acta 1783 (2008) 2415-2426
23. Malone C.J., Fixsen W.D., Horvitz H.R., and Han M. UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development 126 (1999) 3171-3181
24. Malone C.J., Misner L., Le Bot N., Tsai M.C., Campbell J.M., Ahringer J., and White J.G. The C. elegans hook protein, ZYG-12, mediates the essential attachement between the centrosome and nucleus. Cell 115 (2003) 825-836
25. Meyerzon M., Gao Z., Liu J., Wu J.C., Malone C.J., and Starr D.A. Centrosome attachment to the C. elegans male pronucleus is dependent on the surface area of the nuclear envelope. Dev. Biol. 327 (2009) 433-446
26. Miki F., Kurabayashi A., Tange Y., Okazaki K., Shimanuki M., and Niwa O. Two-hybrid search for proteins that interact with Sad1 and Kms1, two membrane-bound components of the spindle pole body in fission yeast. Mol. Genet. Genomics 270 (2004) 449-461
27. Nellen W., Datta S., Reymond C., Sivertsen A., Mann S., Crowley T., and Firtel R.A. Molecular biology in Dictyostelium: tools and applications. Methods Cell Biol 28 (1987) 67-100
28. Omura F., and Fukui Y. Dictyostelium MTOC: structure and linkage to the nucleus. Protoplasma 127 (1985) 212-221
29. Padmakumar V.C., Libotte T., Lu W., Zaim H., Abraham S., Noegel A.A., Gotzmann J., Foisner R., and Karakesisoglou I. The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J. Cell Sci. 118 (2005) 3419-3430
30. Patterson K., Molofsky A.B., Robinson C., Acosta S., Cater C., and Fischer J.A. The functions of Klarsicht and nuclear lamin in developmentally regulated nuclear migrations of photoreceptor cells in the Drosophila eye. Mol. Biol. Cell 15 (2004) 600-610
31. Rehberg M., Kleylein-Sohn J., Faix J., Ho T.H., Schulz I., and Gräf R. Dictyostelium LIS1 is a centrosomal protein required for microtubule/cell cortex interactions, nucleus/centrosome linkage, and actin dynamics. Mol. Biol. Cell 16 (2005) 2759-2771
32. Reinsch S., and Gönczy P. Mechanisms of nuclear positioning. J. Cell Sci. 111 (1998) 2283-2295
33. Schramm C., Elliott S., Shevchenko A., and Schiebel E. The Bbp1p-Mps2p complex connects the SPB to the nuclear envelope and is essential for SPB duplication. EMBO J. 19 (2000) 421-433
34. Schulz I., Reinders Y., Sickmann A., and Gräf R. An improved method for Dictyostelium centrosome isolation. Methods Mol. Biol. 346 (2006) 479-489
35. Schulz I., Erle A., Gräf R., Krüger A., Lohmeier H., Putzler S., Samereier M., and Weidenthaler S. Identification and cell cycle-dependent localization of nine novel, genuine centrosomal components in Dictyostelium discoideum. Cell Motil. Cytoskeleton (2009) 10.1002/cm.20384 (E-pub ahead of print)
36. Starr D.A. A nuclear-envelope bridge positions nuclei and moves chromosomes. J. Cell Sci. 122 (2009) 577-586
37. Tikhonenko I., Nag D.K., Robinson D.N., and Koonce M.P. Microtubule-nucleus interactions in Dictyostelium mediated by central motor kinesins. Eukaryot. Cell 8 (2009) 723-731
38. Tzur Y.B., Wilson K.L., and Gruenbaum Y. SUN-domain proteins: 'Velcro' that links the nucleoskeleton to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 7 (2006) 782-788
39. Ueda M., Gräf R., MacWilliams H.K., Schliwa M., and Euteneuer U. Centrosome positioning and directionality of cell movements. Proc. Natl. Acad. Sci. USA 94 (1997) 9674-9678
40. Ueda M., Schliwa M., and Euteneuer U. Unusual centrosome cycle in Dictyostelium: correlation of dynamic behavior and structural changes. Mol. Biol. Cell 10 (1999) 151-160
41. Wehland J., and Willingham M.C. A rat monoclonal antibody reacting specifically with the tyrosylated form of alpha-tubulin. II. Effects on cell movement, organization of microtubules, and intermediate filaments, and arrangement of Golgi elements. J. Cell Biol. 97 (1983) 1476-1490
42. Wetterauer B., Morandini P., Hribar I., MurgiaMorandini I., Hamker U., Singleton C., and MacWilliams H.K. Wild-type strains of Dictyostelium discoideum can be transformed using a novel selection cassette driven by the promoter of the ribosomal V18 gene. Plasmid 36 (1996) 169-181
43. Wilhelmsen K., Ketema M., Truong H., and Sonnenberg A. KASH-domain proteins in nuclear migration, anchorage and other processes. J. Cell Sci. 119 (2006) 5021-5029
44. Worman H.J., and Gundersen G.G. Here come the SUNs: a nucleocytoskeletal missing link. Trends Cell Biol. 16 (2006) 67-69
45. Xiong H., Rivero F., Euteneuer U., Mondal S., Mana-Capelli S., Larochelle D., Vogel A., Gassen B., and Noegel A.A. Dictyostelium Sun-1 connects the centrosome to chromatin and ensures genome stability. Traffic 9 (2008) 708-724