Multiple Kinesin Motors Coordinate Cytoplasmic RNA Transport on a Subpopulation of Microtubules in Xenopus Oocytes

Timothy J. Messitt; James A. Gagnon; Jill A. Kreiling; Catherine A. Pratt; Young J. Yoon; Kimberly L. Mowry

doi:10.1016/j.devcel.2008.06.014

journal article Open Access Sep 01, 2008

Multiple Kinesin Motors Coordinate Cytoplasmic RNA Transport on a Subpopulation of Microtubules in Xenopus Oocytes

Timothy J. Messitt James A. Gagnon

Jill A. Kreiling

Catherine A. Pratt Young J. Yoon Kimberly L. Mowry

Developmental Cell Vol. 15 No. 3 pp. 426-436 · Elsevier BV

View at Publisher Save 10.1016/j.devcel.2008.06.014

Topics

No keywords indexed for this article. Browse by subject →

References

61

[1]

Alarcon "RNA anchoring in the vegetal cortex of the Xenopus oocyte" J. Cell Sci. (2001) 10.1242/jcs.114.9.1731

[2]

Aronov "Visualization of translated tau protein in the axons of neuronal P19 cells and characterization of tau RNP granules" J. Cell Sci. (2002) 10.1242/jcs.00058

[3]

Berliner "Failure of single-headed kinesin to track parallel to microtubule protofilaments" Nature (1995) 10.1038/373718a0

[4]

Kinesin II Mediates Vg1 mRNA Transport in Xenopus Oocytes

J. Nicholas Betley, Bianca Heinrich, Isabelle Vernos et al.

Current Biology 2004 10.1016/j.cub.2004.01.028

[5]

Birsoy "Vg1 is an essential signaling molecule in Xenopus development" Development (2006) 10.1242/dev.02144

[6]

Blangy "Rigor-type mutation in the kinesin-related protein HsEg5 changes its subcellular localization and induces microtubule bundling" Cell Motil. Cytoskeleton (1998) 10.1002/(sici)1097-0169(1998)40:2<174::aid-cm6>3.0.co;2-f

[7]

Brendza "A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein" Science (2000) 10.1126/science.289.5487.2120

[8]

Bullock "Translocation of mRNAs by molecular motors: Think complex?" Semin. Cell Dev. Biol. (2007) 10.1016/j.semcdb.2007.01.004

[9]

Bullock "Guidance of bidirectional motor complexes by mRNA cargoes through control of dynein number and activity" Curr. Biol. (2006) 10.1016/j.cub.2006.05.055

[10]

Carson "Translocation of myelin basic protein mRNA in oligodendrocytes requires microtubules and kinesin" Cell Motil. Cytoskeleton (1997) 10.1002/(sici)1097-0169(1997)38:4<318::aid-cm2>3.0.co;2-#

[11]

Cha "Kinesin I-dependent cortical exclusion restricts pole plasm to the oocyte posterior" Nat. Cell Biol. (2002) 10.1038/ncb832

[12]

Cole "Novel heterotrimeric kinesin-related proteins purified from sea urchin eggs" Nature (1993) 10.1038/366268a0

[13]

Condeelis "How and why does beta-actin mRNA target?" Biol. Cell (2005) 10.1042/bc20040063

[14]

Cote "A Xenopus protein related to hnRNP I has an essential role in cytoplasmic RNA localization" Mol. Cell (1999) 10.1016/s1097-2765(00)80345-7

[15]

Czaplinski "40LoVe interacts with Vg1RBP/Vera and hnRNP I in binding the Vg1-localization element" RNA (2006) 10.1261/rna.2820106

[16]

Dale "Secretion and mesoderm-inducing activity of the TGF-beta-related domain of Xenopus Vg1" EMBO J. (1993) 10.1002/j.1460-2075.1993.tb06136.x

[17]

De Marco "Analysis of heterodimer formation by Xklp3A/B, a newly cloned kinesin-II from Xenopus laevis" EMBO J. (2001) 10.1093/emboj/20.13.3370

[18]

Deshler "A highly conserved RNA-binding protein for cytoplasmic mRNA localization in vertebrates" Curr. Biol. (1998) 10.1016/s0960-9822(98)70200-3

[19]

Diefenbach "The C-terminal region of the stalk domain of ubiquitous human kinesin heavy chain contains the binding site for kinesin light chain" Biochemistry (1998) 10.1021/bi981163r

[20]

Du "Why cells move messages: The biological functions of mRNA localization" Semin. Cell Dev. Biol. (2007) 10.1016/j.semcdb.2007.01.010

[21]

Duncan "The cytoplasmic dynein and kinesin motors have interdependent roles in patterning the Drosophila oocyte" Curr. Biol. (2002) 10.1016/s0960-9822(02)01303-9

[22]

Gelfand "A dominant negative approach for functional studies of the kinesin II complex" (2001)

[23]

Glotzer "Cytoplasmic flows localize injected oskar RNA in Drosophila oocytes" Curr. Biol. (1997) 10.1016/s0960-9822(06)00156-4

[24]

Havin "RNA-binding protein conserved in both microtubule- and microfilament-based RNA localization" Genes Dev. (1998) 10.1101/gad.12.11.1593

[25]

Hirokawa "mRNA transport in dendrites: RNA granules, motors, and tracks" J. Neurosci. (2006) 10.1523/jneurosci.1821-06.2006

[26]

Houliston "The kinesin-related protein Eg5 associates with both interphase and spindle microtubules during Xenopus early development" Dev. Biol. (1994) 10.1006/dbio.1994.1187

[27]

Ingold "Inhibition of kinesin-driven microtubule motility by monoclonal antibodies to kinesin heavy chains" J. Cell Biol. (1988) 10.1083/jcb.107.6.2657

[28]

Januschke "Polar transport in the Drosophila oocyte requires Dynein and Kinesin I cooperation" Curr. Biol. (2002) 10.1016/s0960-9822(02)01302-7

[29]

Kanai "Kinesin transports RNA: Isolation and characterization of an RNA-transporting granule" Neuron (2004) 10.1016/j.neuron.2004.07.022

[30]

King "Putting RNAs in the right place at the right time: RNA localization in the frog oocyte" Biol. Cell (2005) 10.1042/bc20040067

[31]

Kloc "RNA localization mechanisms in oocytes" J. Cell Sci. (2005) 10.1242/jcs.01637

[32]

Nuclear RNP complex assembly initiates cytoplasmic RNA localization

Tracy L. Kress, Young J. Yoon, Kimberly L. Mowry

The Journal of cell biology 2004 10.1083/jcb.200309145

[33]

Lane "Microtubule-based endoplasmic reticulum motility in Xenopus laevis: Activation of membrane-associated kinesin during development" Mol. Biol. Cell (1999) 10.1091/mbc.10.6.1909

[34]

Lawrence "A standardized kinesin nomenclature" J. Cell Biol. (2004) 10.1083/jcb.200408113

[35]

Le Bot "Role of Xklp3, a subunit of the Xenopus kinesin II heterotrimeric complex, in membrane transport between the endoplasmic reticulum and the Golgi apparatus" J. Cell Biol. (1998) 10.1083/jcb.143.6.1559

[36]

Levi "Organelle transport along microtubules in Xenopus melanophores: evidence for cooperation between multiple motors" Biophys. J. (2006) 10.1529/biophysj.105.067843

[37]

Miki "Analysis of the kinesin superfamily: Insights into structure and function" Trends Cell Biol. (2005) 10.1016/j.tcb.2005.07.006

[38]

Mimori-Kiyosue "The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules" Curr. Biol. (2000) 10.1016/s0960-9822(00)00600-x

[39]

Minakhina "Axes formation and RNA localization" Curr. Opin. Genet. Dev. (2005) 10.1016/j.gde.2005.06.006

[40]

Mische "Direct observation of regulated ribonucleoprotein transport across the nurse cell/oocyte boundary" Mol. Biol. Cell (2007) 10.1091/mbc.e06-10-0959

[41]

Mowry "Complex formation between stage-specific oocyte factors and a Xenopus mRNA localization element" Proc. Natl. Acad. Sci. USA (1996) 10.1073/pnas.93.25.14608

[42]

Mowry "Vegetal messenger RNA localization directed by a 340-nt sequence element in Xenopus oocytes" Science (1992) 10.1126/science.1546297

[43]

Nakata "Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde lysosome membrane transport" J. Cell Biol. (1995) 10.1083/jcb.131.4.1039

[44]

Niethammer "Discrete states of a protein interaction network govern interphase and mitotic microtubule dynamics" PLoS Biol. (2007) 10.1371/journal.pbio.0050029

[45]

Ohashi "Identification of mRNA/protein (mRNP) complexes containing pur-alpha, mStaufen, fragile X protein, and myosin Va and their association with rough endoplasmic reticulum equipped with a kinesin motor" J. Cell Biol. (2002)

[46]

Palacios "How does an RNA find its way? Intracellular localisation of transcripts" Semin. Cell Dev. Biol. (2007) 10.1016/j.semcdb.2007.01.008

[47]

Palacios "Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte" Development (2002) 10.1242/dev.00119

[48]

Pfeiffer "Microtubules in Xenopus oocytes are oriented with their minus-ends towards the cortex" Cell Motil. Cytoskeleton (1999) 10.1002/(sici)1097-0169(199909)44:1<34::aid-cm3>3.0.co;2-6

[49]

St Johnston "Moving messages: The intracellular localization of mRNAs" Nat. Rev. Mol. Cell Biol. (2005) 10.1038/nrm1643

[50]

Stearns "Gamma-tubulin is a highly conserved component of the centrosome" Cell (1991) 10.1016/0092-8674(91)90390-k

Showing 50 of 61 references

Cited By

97

Kinesin-1 interacts with Bucky ball to form germ cells and is required to pattern the zebrafish body axis

Philip D. Campbell, Amanda E. Heim · 2015

Development

Metrics

97

Citations

61

References

Details

Published: Sep 01, 2008
Vol/Issue: 15(3)
Pages: 426-436
License: View

Authors

Department of Molecular Biology, Cell Biology and Biochemistry, Brown University, Providence, RI 02912, USA.

Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, RI 02912

K

Kimberly L. Mowry

Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, RI 02912

Funding

U.S. Public Health Service Award: GM071049

Cite This Article

Timothy J. Messitt, James A. Gagnon, Jill A. Kreiling, et al. (2008). Multiple Kinesin Motors Coordinate Cytoplasmic RNA Transport on a Subpopulation of Microtubules in Xenopus Oocytes. Developmental Cell, 15(3), 426-436. https://doi.org/10.1016/j.devcel.2008.06.014

Multiple Kinesin Motors Coordinate Cytoplasmic RNA Transport on a Subpopulation of Microtubules in Xenopus Oocytes

You May Also Like