Abstract
Nonmuscle myosin II isoforms A and B (hereafter, IIA and IIB) perform unique roles in cell migration, even though both isoforms share the same basic molecular functions. That IIA and IIB assume distinct subcellular distribution in migrating cells suggests that discrete spatiotemporal regulation of each isoform's activity may provide a basis for its unique migratory functions. Here, we make the surprising finding that swapping a small C-terminal portion of the tail between IIA and IIB inverts the distinct distribution of these isoforms in migrating cells. Moreover, swapping this region between isoforms also inverts their specific turnover properties, as assessed by fluorescence recovery after photobleaching and Triton solubility. These data, acquired through the use of chimeras of IIA and IIB, suggest that the C-terminal region of the myosin heavy chain supersedes the distinct motor properties of the two isoforms as the predominant factor directing isoform-specific distribution. Furthermore, our results reveal a correlation between isoform solubility and distribution, leading to the proposal that the C-terminal region regulates isoform distribution by tightly controlling the amount of each isoform that is soluble and therefore available for redistribution into new protrusions.
References
39
Referenced
87
10.1074/jbc.271.34.20246
/ J. Biol. Chem by Amano M. (1996)10.1074/jbc.M501573200
/ J. Biol. Chem by Bao J. (2005)10.1074/jbc.M306948200
/ J. Biol. Chem by Ben-Ya'acov A. (2003)10.1016/S0955-0674(99)80004-0
/ Curr. Opin. Cell Biol by Bresnick A. R. (1999)10.1083/jcb.133.6.1403
/ J. Cell Biol by Chrzanowska-Wodnicka M. (1996)10.1242/jcs.007112
/ J. Cell Sci by Conti M. A. (2008)10.1083/jcb.107.6.2631
/ J. Cell Biol by DeBiasio R. L. (1988)10.1021/bi0500776
/ Biochemistry by Dulyaninova N. G. (2005)10.1038/ncb1540
/ Nat. Cell Biol by Even-Ram S. (2007)10.1074/jbc.M309981200
/ J. Biol. Chem by Golomb E. (2004)10.1083/jcb.134.3.675
/ J. Cell Biol by Kelley C. A. (1996)10.1126/science.273.5272.245
/ Science by Kimura K. (1996)10.1242/jcs.111.15.2085
/ J. Cell Sci by Kolega J. (1998)10.1091/mbc.e03-04-0205
10.1016/j.bbrc.2004.06.045
/ Biochem. Biophys. Res. Commun by Kolega J. (2004)10.1091/mbc.e06-05-0431
10.1091/mbc.4.8.819
10.1074/jbc.M405319200
/ J. Biol. Chem by Kovacs M. (2004)10.1074/jbc.M305453200
/ J. Biol. Chem by Kovacs M. (2003)10.1016/S0092-8674(00)81280-5
/ Cell by Lauffenburger D. A. (1996)10.1158/0008-5472.CAN-05-3087
/ Cancer Res by Li Z. H. (2006)10.1007/s10974-004-6060-7
/ J. Muscle Res. Cell Motil by Limouze J. (2004)10.1073/pnas.84.14.4910
/ Proc. Natl. Acad. Sci. USA by Luby-Phelps K. (1987)10.1021/bi048807h
/ Biochemistry by Nakasawa T. (2005)10.1091/mbc.e05-07-0597
10.1371/journal.pone.0001496
/ PLoS ONE by Rosenberg M. (2008)10.1016/S0014-5793(01)03186-6
/ FEBS Lett by Saitoh T. (2001)10.1074/jbc.M605343200
/ J. Biol. Chem by Sandquist J. C. (2006)10.1091/mbc.e06-08-0706
10.1161/01.RES.69.2.530
/ Circ. Res by Simons M. (1991)10.1126/science.1081412
/ Science by Straight A. F. (2003)10.1242/jcs.114.16.3047
/ J. Cell Sci by Straussman R. (2001)10.1146/annurev.bi.61.070192.003445
/ Annu. Rev. Biochem by Tan J. L. (1992)10.1016/0955-0674(91)90172-U
/ Curr. Opin. Cell Biol by Trybus K. M. (1991)10.1083/jcb.200612043
/ J. Cell Biol by Vicente-Manzanares M. (2007)10.1074/jbc.M302510200
/ J. Biol. Chem by Wang F. (2003)10.1146/annurev.cb.03.110187.002115
/ Annu. Rev. Cell Biol by Warrick H. M. (1987)10.1091/mbc.11.10.3617
10.1074/jbc.M211584200
/ J. Biol. Chem by Worthylake R. A. (2003)
Dates
Type | When |
---|---|
Created | 16 years, 10 months ago (Oct. 8, 2008, 9:09 p.m.) |
Deposited | 3 years, 11 months ago (Sept. 18, 2021, 1:31 a.m.) |
Indexed | 3 months, 1 week ago (May 25, 2025, 9:02 a.m.) |
Issued | 16 years, 9 months ago (Dec. 1, 2008) |
Published | 16 years, 9 months ago (Dec. 1, 2008) |
Published Print | 16 years, 9 months ago (Dec. 1, 2008) |
@article{Sandquist_2008, title={The C-Terminal Tail Region of Nonmuscle Myosin II Directs Isoform-specific Distribution in Migrating Cells}, volume={19}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e08-05-0533}, DOI={10.1091/mbc.e08-05-0533}, number={12}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Sandquist, Joshua C. and Means, Anthony R.}, editor={Wang, Yu-Li}, year={2008}, month=dec, pages={5156–5167} }