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Review

The functions of kinesin and kinesin-related proteins in eukaryotes

ORCID Icon & ORCID Icon
Pages 139-152 | Received 20 Jun 2019, Accepted 11 Aug 2020, Published online: 25 Aug 2020

References

  • Yu Y, Feng YM. The role of kinesin family proteins in tumorigenesis and progression. Cancer. 2010;116:5150–5160.
  • Gerdes JM, Davis EE, Katsanis N. The vertebrate primary cilium in development, homeostasis, and disease. Cell. 2009;137:32–45.
  • Salinas S, Bilsland LG, Schiavo G. Molecular landmarks along the axonal route: axonal transport in health and disease. Curr Opin Cell Biol. 2008;20:445–453.
  • Pegoraro AF, Janmey J, Weitz DA. Mechanical properties of the cytoskeleton and cells. Cold Spring Harb Perspect Biol. 2017;1:9.
  • Herrmann H, Aebi U. Intermediate filaments: structure and assembly. Cold Spring Harb Perspect Biol. 2016;8:a018242.
  • Barlan K, Gelfand VI. Microtubule-based transport and distribution, tethering, and organization of organelles. Cold Spring Harb Perspect Biol. 2017;1:9.
  • McIntosh JR. Mitosis. Cold Spring Harb Perspect Biol. 2016;8:a023218.
  • Viswanadha R, Sale WS, Porter ME. Ciliary motility: regulation of axonemal dynein motors. Cold Spring Harb. Perspect Biol. 2017;1:9.
  • Nick P. Microtubules, signalling and abiotic stress. Plant J. 2013;75:309–323.
  • Bisgrove SR. The roles of microtubules in tropisms. Plant Sci. 2008;175:747–755.
  • Guan Y, Guo J, Li H, et al. Signaling in pollen tube growth: crosstalk, feedback, and missing links. Mol Plant. 2013;6:1053–1064.
  • Klotz J, Nick P. A novel actin–microtubule cross-linking kinesin, NtKCH, functions in cell expansion and division. New Phytol. 2011;193:576–589.
  • Baskin TI. On the alignment of cellulose microfibrils by cortical microtubules: A review and a model. Protoplasma. 2001;215:150–171.
  • Chan J, Crowell E, Eder M, et al. The rotation of cellulose synthase trajectories is microtubule dependent and influences the texture of epidermal cell walls in Arabidopsis hypocotyls. J Cell Sci. 2010;123:3490–3495.
  • Fujita M, Himmelspach R, Hocart CH, et al. Cortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis. Plant J. 2011;66:915–928.
  • Godinho SA, Pellman D. Causes and consequences of centrosome abnormalities in cancer. Philos Trans R Soc Lond B Biol Sci. 2014;369:20130467.
  • Wittmann T, Hyman A, Desai A. The spindle: a dynamic assembly of microtubules and motors. Nat Cell Biol. 2001;3:28–34.
  • Hirokawa N, Pfister KK, Yorifuji H, et al. Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration. Cell. 1989;56:867–878.
  • Vale RD, Milligan RA. The way things move: looking under the hood of molecular motor proteins. Science. 2000;288:88–95.
  • Reddy ASN, Day IS. Kinesins in the Arabidopsis genome: A comparative analysis among eukaryotes. BMC Genomics. 2001;2:2.
  • Ali I, Yang WC. Why are ATP-driven microtubule minus-end directed motors critical to plants? An overview of plant multifunctional kinesins. Funct Plant Biol. 2020;47:524–536.
  • Miki H, Okada Y, Hirokawa N. Analysis of the kinesin superfamily: insights into structure and function. Trends Cell Biol. 2005;15:467–476.
  • Lawrence CJ, Dawe RK, Christie KR, et al. A standardized kinesin nomenclature. J Cell Biol. 2004;167:19–22.
  • Glotzer M. The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat Rev Mol Cell Biol. 2009;10:9–20.
  • Wordeman L. How kinesin motor proteins drive mitotic spindle function: lessons from molecular assays. Sem Cell Dev Biol. 2010;21:260–268.
  • Gicking AM, Swentowsky KW, Dawe RK, et al. Functional diversification of the kinesin-14 family in land plants. FEBS Lett. 2018;592:1918–1928.
  • Jonsson E, Yamada M, Vale RD, et al. Clustering of a kinesin-14 motor enables processive retrograde microtubule-based transport in plants. Nat Plants. 2015;1:15087.
  • Ambrose C, Cyr R. Mitotic spindle organization by the preprophase band. Mol Plant. 2008;1:950–960.
  • Asada T, Kuriyama R, Shibaoka H. TKRP125, a kinesin-related protein involved in the centrosome-independent organization of the cytokinetic apparatus in tobacco BY-2 cells. J Cell Sci. 1997;110:179–189.
  • Cai G, Cresti M. Microtubule motors and pollen tube growth: still an open question. Protoplasma. 2010;247:131–143.
  • Murata T, Toshio S, Sasabe M, et al. Mechanism of microtubule array expansion in the cytokinetic phragmoplast. Nat Commun. 2013;4:1967.
  • Miki T, Naito H, Nishina M, et al. Endogenous localizome identifies 43 mitotic kinesins in a plant cell. Proc Natl Acad Sci USA. 2014;111:1053–1061.
  • Liu B, Cyr RJ, Palevitz BA. A kinesin-like protein, KatAp, in the cells of Arabidopsis and other plants. Plant Cell. 1996;8:119–132.
  • Ambrose C, Li W, Marcus A, et al. A minus-end directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. Mol Biol Cell. 2005;16:1584–1592.
  • Vanstraelen M, Acosta JAT, De Veylder L, et al. A plant-specific subclass of C-terminal kinesins contains a conserved A-type cyclin-dependent kinase site implicated in folding and dimerization. Plant Physiol. 2004;135:1417–1429.
  • Xu T, Sun X, Jiang S, et al. Cotton GhKCH2, a plant-specific kinesin, is low-affinitive and nucleotide-independent as binding to microtubule. J Biochem Mol Biol. 2007;40:723–730.
  • Buschmann H, Dols J, Kopischke S, et al. Arabidopsis KCBP interacts with AIR9 but stays in the cortical division zone throughout mitosis via its MyTH4-FERM domain. J Cell Sci. 2015;128:2033–2046.
  • Yamada M, Tanaka-Takiguchi Y, Hayashi M, et al. Multiple kinesin-14 family members drive microtubule minus end–directed transport in plant cells. J Cell Biol. 2017;216:1705–1714.
  • Vos JW, Safadi F, Reddy ASN, et al. The kinesin-like calmodulin binding protein is differentially involved in cell division. Plant Cell. 2000;12:979–990.
  • Oh SA, Bourdon V, DasPal M, et al. Arabidopsis kinesins HINKEL and TETRASPORE act redundantly to control cell plate expansion during cytokinesis in the male gametophyte. Mol Plant. 2008;1:794–799.
  • Tanaka H, Ishikawa M, Kitamura S, et al. The AtNACK1/HINKEL and STUD/TETRASPORE/AtNACK2 genes, which encode functionally redundant kinesins, are essential for cytokinesis in Arabidopsis. Genes Cells. 2004;9:1199–1211.
  • Beck M, Komis G, Ziemann A, et al. Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol. 2011;189:1069–1083.
  • Nishihama R, Soyano T, Ishikawa M, et al. Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell. 2002;109:87–99.
  • Komis G, Illes P, Beck M, et al. Microtubules and mitogen-activated protein kinase signalling. Curr Opin Plant Biol. 2011;14:650–657.
  • Lee YR, Giang HM, Liu B. A novel plant kinesin-related protein specifically associates with the phragmoplast organelles. Plant Cell. 2001;13:2427–2439.
  • Barroso C, Chan J, Allan V, et al. Two kinesin-related proteins associated with the cold-stable cytoskeleton of carrot cells: characterization of a novel kinesin, DcKRP120-2. Plant J. 2000;24:859–868.
  • Bannigan A, Scheible WR, Lukowitz W, et al. A conserved role for kinesin-5 in plant mitosis. J Cell Sci. 2007;120:2819–2827.
  • Lee YR, Li Y, Liu B. Two Arabidopsis phragmoplast-associated kinesins play a critical role in cytokinesis during male gametogenesis. Plant Cell. 2007;19:2595–2605.
  • Pan R, Lee YR, Liu B. Localization of two homologous Arabidopsis kinesin related proteins in the phragmoplast. Planta. 2004;220:156–164.
  • Siller KH, Doe CQ. Spindle orientation during asymmetric cell division. Nat Cell Biol. 2009;11:365–374.
  • Garzon-Coral C, Fantana HA, Howard J. A force-generating machinery maintains the spindle at the cell center during mitosis. Science. 2016;352:1124–1127.
  • Kiyomitsu T, Cheeseman IM. Chromosome- and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nat Cell Biol. 2012;14:311–317.
  • Samora CP, Mogessie B, Conway L, et al. MAP4 and CLASP1 operate as a safety mechanism to maintain a stable spindle position in mitosis. Nat Cell Biol. 2011;13:1040–1050.
  • Rusan NM, Fagerstrom CJ, Yvon AM, et al. Cell cycle-dependent changes in microtubule dynamics in living cells expressing green fluorescent protein-alpha tubulin. Mol Biol Cell. 2001;12:971–980.
  • Ems-McClung SC, Walczak CE. Kinesin-13s in mitosis: key players in the spatial and temporal organization of spindle microtubules. Sem Cell Dev Biol. 2010;21:276–282.
  • Savoian MS, Glover DM. Drosophila Klp67A binds prophase kinetochores to subsequently regulate congression and spindle length. J Cell Sci. 2010;123:767–776.
  • Gupta ML, Carvalho JP, Roof DM, et al. Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle. Nat Cell Biol. 2006;8:913–923.
  • McHugh T, Gluszek AA, Welburn JPI. Microtubule end tethering of a processive kinesin-8 motor Kif18b is required for spindle positioning. J Cell Biol. 2018;217:2403–2416.
  • Zhu C, Dixit R. Functions of the Arabidopsis kinesin superfamily of microtubule-based motor proteins. Protoplasma. 2012;249:887–899.
  • Mazumdar M, Misteli T. Chromokinesins: multitalented players in mitosis. Trends Cell Biol. 2005;15:349–355.
  • Walczak CE, Heald R. Mechanisms of mitotic spindle assembly and function. Int Rev Cytol. 2008;265:111–158.
  • Gard DL, Kirschner MW. A microtubule-associated protein from Xenopus eggs that specifically promotes assembly at the plus-end. J Cell Biol. 1987;105:2203–2215.
  • Ohkura H, Adachi Y, Kinoshita N, et al. Cold-sensitive and caffeine-supersensitive mutants of the Schizosaccharomyces pombe dis genes implicated in sister chromatid separation during mitosis. Embo J. 1988;7:1465–1473.
  • Furuta K, Toyoshima YY. Minus-end directed motor Ncd exhibits processive movement that is enhanced by microtubule bundling in vitro. Curr Biol. 2008;18:152–157.
  • Lucas JR, Nadeau JA, Sack FD. Microtubule arrays and Arabidopsis stomatal development. J Exp Bot. 2006;57:71–79.
  • Wasteneys GO, Yang Z. New views on the plant cytoskeleton. Plant Physiol. 2004;136:3884–3891.
  • Zonia L, Tupy J, Staiger CJ. Unique actin and microtubule arrays co-ordinate the differentiation of microspores to mature pollen in Nicotiana tabacum. J Exp Bot. 1999;50:581–594.
  • Goto Y, Asada T. Excessive expression of the plant kinesin TBK5 converts cortical and perinuclear microtubules into a radial array emanating from a single focus. Plant Cell Physiol. 2007;48:753–761.
  • Mucha E, Hoefle C, Hückelhoven R, et al. RIP3 and AtKinesin-13A: A novel interaction linking Rho proteins of plants to microtubules. Eur J Cell Biol. 2010;89:906–916.
  • Mathur J, Chua NH. Microtubule stabilization leads to growth reorientation in Arabidopsis thaliana trichomes. Plant Cell. 2000;12:465–477.
  • Whittington AT, Vugrek OJ, Wei KG, et al. MOR1 is essential for organizing cortical microtubule in plants. Nature. 2001;411:610–613.
  • Bieling P, Telley IA, Surrey T. A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps. Cell. 2010;142:420–432.
  • Kurasawa Y, Earnshaw WC, Mochizuki Y, et al. Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation. Embo J. 2004;23:3237–3248.
  • Subramanian R, Ti SC, Tan L, et al. Marking and measuring single microtubules by PRC1 and kinesin-4. Cell. 2013;154:377–390.
  • Zhu C, Jiang W. Cell cycle-dependent translocation of PRC1 on the spindle by Kif4 is essential for midzone formation and cytokinesis. Proc Natl Acad Sci USA. 2005;102:343–348.
  • Bringmann H, Skiniotis G, Spilker A, et al. A kinesin-like motor inhibits microtubule dynamic instability. Science. 2004;303:1519–1522.
  • Mollinari C, Kleman JP, Jiang W, et al. PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J Cell Biol. 2002;157:1175–1186.
  • Bechstedt S, Brouhard GJ. Motors and MAPs collaborate to size up microtubules. Dev Cell. 2013;26:118–120.
  • Dawe RK, Lowry EG, Gent JI, et al. A kinesin-14 motor activates neocentromeres to promote meiotic drive in maize. Cell. 2018;173:839–850.
  • Chen C, Marcus A, Li W, et al. The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development. 2002;129:2401–2409.
  • McIntosh JR. Assessing the contributions of motor enzymes and microtubule dynamics to mitotic chromosome motions. Annu Rev Cell Dev Biol. 2017;33:1–22.
  • Vicente JJ, Wordeman L. Mitosis, microtubule dynamics and the evolution of kinesins. Exp Cell Res. 2015;334:61–69.
  • Gallagher KL, Sozzani R, Lee CM. Intercellular protein movement: deciphering the language of development. Annu Rev Cell Dev Biol. 2014;30:207–233.
  • Kurata T, Ishida T, Kawabata-Awai C, et al. Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development. 2005;132:5387–5398.
  • Pi L, Aichinger E, van der Graaff E, et al. Organizer-derived WOX5 signal maintains root Columella stem cells through chromatin-mediated repression of cdf4 expression. Dev Cell. 2015;33:576–588.
  • Raissig MT, Matos JL, Gil MXA, et al. Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata. Science. 2017;355:1215–1218.
  • Savage NS, Walker T, Wieckowski Y, et al. A mutual support mechanism through intercellular movement of CAPRICE and GLABRA3 can pattern the Arabidopsis root epidermis. PLoS Biol. 2008;6:e235.
  • Sessions A, Yanofsky MF, Weigel D. Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science. 2000;289:779–781.
  • Wu X, Dinneny JR, Crawford KM, et al. Modes of intercellular transcription factor movement in the Arabidopsis apex. Development. 2003;130:3735–3745.
  • Lucas WJ, Bouche-Pillon S, Jackson DP, et al. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science. 1995;270:1980–1983.
  • Yadav R, Perales M, Gruel J, et al. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 2011;25:2025–2030.
  • Schlereth A, Möller B, Liu W, et al. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature. 2010;464:913.
  • Oparka KJ. Getting the message across: how do plant cells exchange macromolecular complexes? Trends Plant Sci. 2004;9:33–41.
  • Spiegelman Z, Lee CM, Gallagher KL. KinG is a plant-specific kinesin that regulates both intra- and intercellular movement of short-root. Plant Physiol. 2018;176:392–405.
  • Helariutta Y, Fukaki H, Wysocka-Diller J, et al. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell. 2000;101:555–567.
  • Tsuboi H, Wada M. Chloroplasts can move in any direction to avoid strong light. J Plant Res. 2011;124:201–210.
  • Kadota A, Yamada N, Suetsugu N, et al. Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci USA. 2009;106:13106–13111.
  • Wada M. Chloroplast movement. Plant Sci. 2013;210:177–182.
  • Yamashita H, Sato Y, Kanegae T, et al. Chloroplast actin filaments organize meshwork on the photorelocated chloroplasts in the moss Physcomitrella patens. Planta. 2011;233:357–368.
  • Buchnik L, Abu-Abied M, Sadot E. Role of plant myosins in motile organelles: is a direct interaction required? J Integr Plant Biol. 2015;57:23–30.
  • Vidali L, Burkart GM, Augustine RC, et al. Myosin XI is essential for tip growth in Physcomitrella patens. Plant Cell. 2010;22:1868–1882.
  • Suetsugu N, Dolja VV, Wada M. Why have chloroplasts developed a unique motility system? Plant Signal Behav. 2010b;5:1190–1196.
  • Shen Z, Liu YC, Bibeau JP, et al. The kinesin-like proteins, KAC1/2, regulate actin dynamics underlying chloroplast light avoidance in Physcomitrella patens. J Integr Plant Biol. 2015;57:106–119.
  • Suetsugu N, Yamada N, Kagawa T, et al. Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2010a;107:8860–8865.
  • Suetsugu N, Sato Y, Tsuboi H, et al. The KAC family of kinesin-like proteins is essential for the association of chloroplasts with the plasma membrane in land plants. Plant Cell Physiol. 2012;53:1854–1865.
  • Corthesy-Theulaz I, Pauloin A, Pfeffer SR. Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J Cell Biol. 1992;118:1333–1345.
  • Wei L, Zhang W, Liu Z, et al. AtKinesin-13A is located on Golgi-associated vesicle and involved in vesicle formation/budding in Arabidopsis root-cap peripheral cells. BMC Plant Biol. 2009;9:138.
  • Lu L, Lee YR, Pan R, et al. An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis. Mol Biol Cell. 2005;16:811–823.
  • Varadi A, Johnson-Cadwell I, Cirulli L, et al. Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1. J Cell Sci. 2004;117:4389–4400.
  • Ni CZ, Wang HQ, Xu T, et al. AtKP1, a kinesin-like protein, mainly localizes to mitochondria in Arabidopsis thaliana. Cell Res. 2005;15:725–733.
  • Yang XY, Chen ZW, Xu T, et al. Arabidopsis kinesin KP1 specifically interacts with VDAC3, a mitochondrial protein, and regulates respiration during seed germination at low temperature. Plant Cell. 2011;23:1093–1106.
  • Romagnoli S, Cai G, Faleri C, et al. Microtubule- and actin filament-dependent motors are distributed on pollen tube mitochondria and contribute differently to their movement. Plant Cell Physiol. 2007;48:345–361.
  • Gundersen GG, Worman HJ. Nuclear positioning. Cell. 2013;152:1376–1389.
  • Bruusgaard JC, Liestøl K, Ekmark M, et al. Number and spatial distribution of nuclei in the muscle fibres of normal mice studied in vivo. J Physiol. 2003;551:467–478.
  • Cadot B, Gache V, Vasyutina E, et al. Nuclear movement during myotube formation is microtubule and dynein dependent and is regulated by Cdc42, Par6 and Par3. EMBO Rep. 2012;13:741–749.
  • Falcone S, Roman W, Hnia K, et al. N-WASP is required for Amphiphysin-2/BIN1-dependent nuclear positioning and triad organization in skeletal muscle and is involved in the pathophysiology of centronuclear myopathy. EMBO Mol Med. 2014;6:1455–1475.
  • Metzger T, Gache V, Xu M, et al. MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function. Nature. 2012;484:120.
  • Wilson MH, Holzbaur ELF. Nesprins anchor kinesin-1 motors to the nucleus to drive nuclear distribution in muscle cells. Development. 2015;142:218–228.
  • Jungbluth H, Wallgren-Pettersson C, Laporte J. Centronuclear (myotubular) myopathy. Orphanet J Rare Dis. 2008;3:26.
  • Gache V, Gomesa ER, Cadot B. Microtubule motors involved in nuclear movement during skeletal muscle differentiation. Mol Biol Cell. 2017;28:865–873.
  • Preuss ML, Kovar DR, Lee YR, et al. A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol. 2004;136:3945–3955.
  • Wang H, Liu R, Wang J, et al. The Arabidopsis kinesin gene AtKin-1 plays a role in the nuclear division process during megagametogenesis. Plant Cell Rep. 2014;33:819–828.
  • Frey N, Klotz J, Nick. P. A kinesin with calponin-homology domain is involved in premitotic nuclear migration. J Exp Bot. 2010;61:3423–3437.
  • Tsai JW, Lian WN, Kemal S, et al. Kinesin 3 and cytoplasmic dynein mediate inter-kinetic nuclear migration in neural stem cells. Nat Neurosci. 2010;13:1463–1471.
  • Miki T, Nishina M, Goshima G. RNAi screening identifies the armadillo repeat-containing kinesins responsible for microtubule-dependent nuclear positioning in Physcomitrella patens. Plant Cell Physiol. 2015;56:737–749.
  • Yamada M, Goshima G. The KCH kinesin drives nuclear transport and cytoskeletal coalescence to promote tip cell growth in Physcomitrella patens. Plant Cell. 2018;30:1496–1510.
  • Augustine RC. Nuclear positioning requires a tug-of-war between kinesin motors. Plant Cell. 2018;30:1383–1384.
  • McFarlane HE, Döring A, Persson S. The cell biology of cellulose synthesis. Annu Rev Plant Biol. 2014;65:69–94.
  • Gutierrez R, Lindeboom JJ, Paredez AR, et al. Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol. 2009;11:797.
  • Sampathkumar A, Gutierrez R, McFarlane HE, et al. Patterning and lifetime of plasma membrane–localized cellulose synthase is dependent on actin organization in Arabidopsis interphase cells. Plant Physiol. 2013;162:675–688.
  • Ledbetter M, Porter K. A “microtubule” in plant cell fine structure. J Cell Biol. 1963;19:239–250.
  • Lancelle SA, Callaham DA, Hepler PK. A method for rapid freeze fixation of plant cells. Protoplasma. 1986;131:153–165.
  • Oda Y. Emerging roles of cortical microtubule–membrane interactions. J Plant Res. 2018;131:5–14.
  • Zhang M, Zhang B, Qian Q, et al. Brittle Culm 12, a dual-targeting kinesin-4 protein, controls cell-cycle progression and wall properties in rice. Plant J. 2010;63:312–328.
  • Zhong R, Burk DH, Morrison WH, et al. A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell. 2002;14:3101–3117.
  • Ganguly A, DeMott L, Dixit R. The Arabidopsis kinesin-4, FRA1, requires a high level of processive motility to function correctly. J Cell Sci. 2017;130:1232–1238.
  • Kong Z, Ioki M, Braybrook S, et al. Kinesin-4 functions in vesicular transport on cortical microtubules and regulates cell wall mechanics during cell elongation in plants. Mol Plant. 2015;8:1011–1023.
  • Zhu C, Ganguly A, Baskin TI, et al. The Fragile Fiber1 kinesin contributes to cortical microtubule-mediated trafficking of cell wall components. Plant Physiol. 2015;167:780–792.
  • Tian J, Han L, Feng Z, et al. Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin. eLife. 2015;4:e09351.
  • Rolls MM, Jegla TJ. Neuronal polarity: an evolutionary perspective. J Exp Biol. 2015;218:572–580.
  • Stone MC, Roegiers F, Rolls MM. Microtubules have opposite orientation in axons and dendrites of Drosophila neurons. Mol Biol Cell. 2008;19:4122–4129.
  • Atherton J, Houdusse A, Moores C. Mapping out distribution routes for kinesin couriers. Biol Cell. 2013;105:465–487.
  • Bentley M, Banker G. The cellular mechanisms that maintain neuronal polarity. Nature Rev Neurosci. 2016;17:611.
  • Tas RP, Chazeau A, Cloin BM, et al. Differentiation between oppositely oriented microtubules controls polarized neuronal transport. Neuron. 2017;96:1264–1271.
  • Kelliher MT, Yue Y, Ng A, et al. Autoinhibition of kinesin-1 is essential to the dendrite-specific localization of Golgi outposts. J Cell Biol. 2018;217:2531–2547.
  • Kwon M, Godinho S, Chandhok N, et al. Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev. 2008;22:2189–2203.
  • Xiao YX, Shen HQ, She ZY, et al. C-terminal kinesin motor KIFC1 participates in facilitating proper cell division of human seminoma. Oncotarget. 2017;8:61373–61384.
  • Zhang C, Chen X, Chen X, et al. miR-135a acts as a tumor suppressor in gastric cancer in part by targeting KIFC1. Oncol Targets Ther. 2016;9:3555–3563.
  • Ogden A, Rida PC, Aneja R. Let’s huddle to prevent a muddle: centrosome declustering as an attractive anticancer strategy. Cell Death Differ. 2012;19:1255–1267.
  • Rath O, Kozielski F. Kinesins and cancer. Nat Rev Cancer. 2012;12:527–539.
  • Goshima G, Vale RD. The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J Cell Biol. 2003;162:1003–1016.
  • Stumpff J, Wagenbach M, Franck A, et al. Kif18A and chromokinesins confine centromere movements via microtubule growth suppression and spatial control of kinetochore tension. Dev Cell. 2012;22:1017–1029.
  • Wandke C, Barisic M, Sigl R, et al. Human chromokinesins promote chromosome congression and spindle microtubule dynamics during mitosis. J Cell Biol. 2012;198:847–863.
  • Ye AA, Verma V, Maresca TJ. NOD is a plus end–directed motor that binds EB1 via a new microtubule tip localization sequence. J Cell Biol. 2018;217:3007–3017.
  • Cane S, Ye AA, Luks-Morgan SJ, et al. Elevated polar ejection forces stabilize kinetochore-microtubule attachments. J Cell Biol. 2013;200:203–218.
  • Cochran JC, Sindelar CV, Mulko NK, et al. ATPase cycle of the nonmotile kinesin NOD allows microtubule end tracking and drives chromosome movement. Cell. 2009;136:110–122.
  • Cui W, Hawley RS. The HhH2/NDD domain of the Drosophila NOD chromokinesin-like protein is required for binding to chromosomes in the oocyte nucleus. Genetics. 2005;171:1823–1835.
  • Carpenter AT. A meiotic mutant defective in distributive disjunction in Drosophila melanogaster. Genetics. 1973;73:393–428.
  • Zhang P, Hawley RS. The genetic analysis of distributive segregation in Drosophila melanogaster. II. Further genetic analysis of the NOD locus. Genetics. 1990;125:115–127.
  • Yajima J, Edamatsu M, Watai‐Nishii J, et al. The human chromokinesin Kid is a plus end‐directed microtubule‐based motor. Embo J. 2003;22:1067–1074.
  • Tokai-Nishizumi N, Ohsugi M, Suzuki E, et al. The Chromokinesin Kid is required for maintenance of proper metaphase spindle size. Mol Biol Cell. 2005;16:5455–5463.
  • Antonio C, Ferby I, Wilhelm H, et al. Xkid, a chromokinesin required for chromosome alignment on the metaphase plate. Cell. 2000;102:425–435.
  • Takagi J, Itabashi T, Suzuki K, et al. Chromosome position at the spindle equator is regulated by chromokinesin and a bipolar microtubule array. Sci Rep. 2013;3:2808.
  • Corti B. Osservazioni microscopiche sulla Tremella: e sulla circolazione del fluido in una pianta acquajuola. Apresso G Rocchi. 1774;207:1729–1813.
  • Peremyslov VV, Prokhnevsky AI, Dolja VV. Class XI myosins are required for development, cell expansion, and F-actin organization in Arabidopsis. Plant Cell. 2010;22:1883–1897.
  • Ueda H, Yokota E, Kutsuna N, et al. Myosin-dependent endoplasmic reticulum motility and F-actin organization in plant cells. Proc Natl Acad Sci USA. 2010;107:6894–6899.
  • Shimmen T. The sliding theory of cytoplasmic streaming: fifty years of progress. J Plant Res. 2007;120:31–43.
  • Collings DA, Harper JDI, Marc J, et al. Life in the fast lane: actin-based motility of plant peroxisomes. Can J Bot. 2002;80:430–441.
  • Runions J, Brach T, Kuhner S, et al. Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J Exp Bot. 2006;57:43–50.
  • Palacios IM, St-Johnston D. Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte. Development. 2002;129:5473–5485.