Nack kinesin is required for metaphase chromosome alignment and cytokinesis in the moss physcomitrella patens

Cell Structure and Function

Volumn 40, Issue 1, 2015, Pages 31-41

  Naito, Haruko ^a   Goshima, Gohta ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

Chromosome alignment; Kinesin 7; Phragmoplast expansion; Physcomitrella patens; Processive motility

Indexed keywords

KINESIN; NACK KINESIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ANAPHASE; ARTICLE; CELL CYCLE REGULATION; CELL EXPANSION; CELLS BY BODY ANATOMY; CHROMOSOME POSITIONING; CYTOKINESIS; ENZYME ACTIVITY; ENZYME LOCALIZATION; GENE SILENCING; IN VITRO STUDY; METAPHASE; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; PHENOTYPE; PHRAGMOPLAST; PHYSCOMITRELLA PATENS; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN DETERMINATION; PROTONEMAL CELL; RNA INTERFERENCE; SINGLE MOTOR MOTILITY ASSAY; TELOPHASE; TUBULIN POLYMERIZATION ASSAY; BRYOPSIDA; CYTOLOGY; DEFICIENCY; GENETICS; METABOLISM; MOVEMENT (PHYSIOLOGY); PLANT CHROMOSOME;

ARABIDOPSIS; BRYOPHYTA; NICOTIANA TABACUM; PHYSCOMITRELLA PATENS;

BRYOPSIDA; CHROMOSOMES, PLANT; CYTOKINESIS; KINESIN; METAPHASE; MICROTUBULES; MOVEMENT; PLANT PROTEINS; PROMETAPHASE; RNA INTERFERENCE; TELOPHASE;

EID: 84923034963     PISSN: 03867196     EISSN: 13473700     Source Type: Journal    
DOI: 10.1247/csf.14016     Document Type: Article

References (36)

1. Cove, D. 2005. The moss Physcomitrella patens. Annu. Rev. Genet., 39: 339-358.
2. Cove, D., Bezanilla, M., Harries, P., and Quatrano, R. 2006. Mosses as model systems for the study of metabolism and development. Annu. Rev. Plant Biol., 57: 497-520.
3. Cross, R.A. and McAinsh, A. 2014. Prime movers: The mechanochemistry of mitotic kinesins. Nat. Rev. Mol. Cell Biol., 15: 257-271.
4. Edelstein, A., Amodaj, N., Hoover, K., Vale, R., and Stuurman, N. 2010. Computer control of microscopes using microManager. Curr. Protoc. Mol. Biol., Chapter 14: Unit14 20.
5. Goshima, G., Kiyomitsu, T., Yoda, K., and Yanagida, M. 2003. Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J. Cell Biol., 160: 25-39.
6. Goshima, G. and Vale, R.D. 2003. The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J. Cell Biol., 162: 1003-1016.
7. Goshima, G. and Vale, R.D. 2005. Cell cycle-dependent dynamics and regulation of mitotic kinesins in Drosophila S2 cells. Mol. Biol. Cell, 16: 3896-3907.
8. Goshima, G., Wollman, R., Goodwin, N., Zhang, J.M., Scholey, J.M., Vale, R.D., and Stuurman, N. 2007. Genes required for mitotic spindle assembly in Drosophila S2 cells. Science, 316: 417-421.
9. Hildebrandt, E.R. and Hoyt, M.A. 2000. Mitotic motors in Saccharomyces cerevisiae. Biochim. Biophys. Acta, 1496: 99-116.
10. Hiwatashi, Y., Obara, M., Sato, Y., Fujita, T., Murata, T., and Hasebe, M.. 2008. Kinesins are indispensable for interdigitation of phragmoplast microtubules in the moss Physcomitrella patens. Plant Cell, 20: 30943106.
11. Ishikawa, M., Soyano, T., Nishihama, R., and Machida, Y. 2002. The NPK1 mitogen-activated protein kinase kinase kinase contains a functional nuclear localization signal at the binding site for the NACK1 kinesin-like protein. Plant J., 32: 789-798.
12. Jones, D.T., Taylor, W.R., and Thornton, J.M. 1992. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci., 8: 275-282.
13. Katoh, K., Misawa, K., Kuma, K., and Miyata, T. 2002. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res., 30: 3059-3066.
14. Katoh, K. and Standley, D.M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol., 30: 772-780.
15. Kosetsu, K., de Keijzer, J., Janson, M.E., and Goshima, G. 2013. MICROTUBULE-ASSOCIATED PROTEIN65 is essential for maintenance of phragmoplast bipolarity and formation of the cell plate in Phys- comitrella patens. Plant Cell, 25: 4479-4492.
16. Li, W., Moriwaki, T., Tani, T., Watanabe, T., Kaibuchi, K., and Goshima, G. 2012. Reconstitution of dynamic microtubules with Drosophila XMAP215, EB1, and Sentin. J. Cell Biol., 199: 849-862.
17. Maliga, Z., Junqueira, M., Toyoda, Y, Ettinger, A., Mora-Bermudez, F., Klemm, R.W., Vasilj, A., Guhr, E., Ibarlucea-Benitez, I., Poser, I., Bonifacio, E., Huttner, W.B., Shevchenko, A., and Hyman, A.A. 2013. A genomic toolkit to investigate kinesin and myosin motor function in cells. Nat. Cell Biol., 15: 325-334.
18. Miki, T., Naito, H., Nishina, M., and Goshima, G. 2014. Endogenous locali- zome identifies 43 mitotic kinesins in a plant cell. Proc. Natl. Acad. Sci. USA, 111: E1053-1061.
19. Miki, T., Nishina, M., and Goshima, G. 2015. RNAi screening identifies the armadillo repeat-containing kinesins responsible for microtubule- dependent nuclear positioning in Physcomitrella patens. Plant Cell Physiol., DOI: 10.1093/pcp/pcv002.
20. Nakaoka, Y., Miki, T., Fujioka, R., Uehara, R., Tomioka, A., Obuse, C., Kubo, M., Hiwatashi, Y., and Goshima, G. 2012. An inducible RNA interference system in Physcomitrella patens reveals a dominant role of aug- min in phragmoplast microtubule generation. Plant Cell, 24: 1478-1493.
21. Nishihama, R., Soyano, T., Ishikawa, M., Araki, S., Tanaka, H., Asada, T., Irie, K., Ito, M., Terada, M., Banno, H., Yamazaki, Y., and Machida, Y. Expansion of the cell plate in plant cytokinesis requires a kinesin- like protein/MAPKKK complex. Cell, 109: 87-99.
22. Oh, S.A., Bourdon, V., Das’Pal, M., Dickinson, H., and Twell, D. 2008. Arabidopsis kinesins HINKEL and TETRASPORE act redundantly to control cell plate expansion during cytokinesis in the male gametophyte. Mol. Plant, 1: 794-799.
23. Prigge, M.J. and Bezanilla, M. 2010. Evolutionary crossroads in developmental biology: Physcomitrella patens. Development, 137: 3535-3543.
24. Sasabe, M., Soyano, T., Takahashi, Y., Sonobe, S., Igarashi, H., Itoh, T.J., Hidaka, M., and Machida, Y. 2006. Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes Dev., 20: 1004-1014.
25. Sasabe, M., Boudolf, V., De Veylder, L., Inze, D., Genschik, P., and Machida, Y. 2011. Phosphorylation of a mitotic kinesin-like protein and a MAPKKK by cyclin-dependent kinases (CDKs) is involved in the transition to cytokinesis in plants. Proc. Natl. Acad. Sci. USA, 108: 1784417849.
26. Sasabe, M. and Machida, Y. 2012. Regulation of organization and function of microtubules by the mitogen-activated protein kinase cascade during plant cytokinesis. Cytoskeleton (Hoboken), 69: 913-918.
27. Shen, Z., Collatos, A.R., Bibeau, J.P., Furt, F., and Vidali, L. 2012. Phylogenetic analysis of the Kinesin superfamily from physcomitrella. Front. Plant Sci., 3: 230.
28. Soyano, T., Nishihama, R., Morikiyo, K., Ishikawa, M., and Machida, Y. NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK- mediated MAPK cascade and is required for plant cytokinesis. Genes Dev., 17: 1055-1067.
29. Strompen, G., El Kasmi, F., Richter, S., Lukowitz, W., Assaad, F.F., Jurgens, G., and Mayer, U. 2002. The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Curr Biol., 12: 153-158.
30. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol., 28: 2731-2739.
31. Tanaka, H., Ishikawa, M., Kitamura, S., Takahashi, Y., Soyano, T., Machida, C., and Machida, Y. 2004. The AtNACK1/HINKEL and STUD/TETRA- SPORE/AtNACK2 genes, which encode functionally redundant kinesins, are essential for cytokinesis in Arabidopsis. Genes Cells, 9: 1199-1211.
32. Tomishige, M. and Vale, R.D. 2000. Controlling kinesin by reversible disul- fide cross-linking. Identifying the motility-producing conformational change. J. Cell Biol., 151: 1081-1092.
33. Tytell, J.D. and Sorger, P.K. 2006. Analysis of kinesin motor function at budding yeast kinetochores. J. Cell Biol., 172: 861-874.
34. Vidali, L., Rounds, C.M., Hepler, P.K., and Bezanilla, M. 2009. Lifeact- mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. PLoS One, 4: 5744.
35. Woehlke, G., Ruby, A.K., Hart, C.L., Ly, B., Hom-Booher, N., and Vale, R.D. 1997. Microtubule interaction site of the kinesin motor. Cell, 90: 207-216
36. Yang, C.Y., Spielman, M., Coles, J.P, Li, Y., Ghelani, S., Bourdon, V., Brown, R.C., Lemmon, B.E., Scott, R.J., and Dickinson, H.G. 2003. TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J., 34: 229-240.