A contractile and counterbalancing adhesion system controls the 3D shape of crawling cells

Journal of Cell Biology

Volumn 205, Issue 1, 2014, Pages 83-96

  Burnette, Dylan T ^a,h   Shao, Lin ^c   Ott, Carolyn ^a   Pasapera, Ana M ^b   Fischer, Robert S ^b   Baird, Michelle A ^d,e   Der Loughian, Christelle ^f   Delanoe Ayari, Helene ^f   Paszek, Matthew J ^g   Davidson, Michael W ^d,e   Betzig, Eric ^c   Lippincott Schwartz, Jennifer ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d FLORIDA STATE UNIVERSITY   (United States)

^e FLORIDA STATE UNIVERSITY   (United States)

^f UNIVERSITÉ DE LYON   (France)

^g Cornell University   (United States)

^h VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ALPHA ACTININ; BLEBBISTATIN; CONTRACTILE PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; MYOSIN IIA;

ACTIN FILAMENT; ARTICLE; CELL ADHESION; CELL MEMBRANE; CELL MOTILITY; CELL POPULATION; CELL SHAPE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; FIBROBLAST; FOCAL ADHESION; IMMUNOCYTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOMERE;

ACTIN CYTOSKELETON; ACTININ; ACTINS; ANIMALS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL SHAPE; CERCOPITHECUS AETHIOPS; COS CELLS; FOCAL ADHESIONS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; NONMUSCLE MYOSIN TYPE IIA; PRESSURE; TIME FACTORS; TRANSFECTION;

EID: 84901673131     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201311104     Document Type: Article

References (42)

1. Aman, A., and T. Piotrowski. 2010. Cell migration during morphogenesis. Dev. Biol. 341:20-33. http://dx.doi.org/10.1016/j.ydbio.2009.11.014
2. Burnette, D.T., L. Ji, A.W. Schaefer, N.A. Medeiros, G. Danuser, and P. Forscher. 2008. Myosin II activity facilitates microtubule bundling in the neuronal growth cone neck. Dev. Cell. 15:163-169. http://dx.doi.org/ 10.1016/j.devcel.2008.05.016
3. Burnette, D.T., S. Manley, P. Sengupta, R. Sougrat, M.W. Davidson, B. Kachar, and J. Lippincott-Schwartz. 2011. A role for actin arcs in the leadingedge advance of migrating cells. Nat. Cell Biol. 13:371-382. http://dx.doi.org/10.1038/ncb2205
4. Chua, J., R. Rikhy, and J. Lippincott-Schwartz. 2009. Dynamin 2 orchestrates the global actomyosin cytoskeleton for epithelial maintenance and apical constriction. Proc. Natl. Acad. Sci. USA. 106:20770-20775. http://dx.doi.org/10.1073/pnas.0909812106
5. Cramer, L.P., M. Siebert, and T.J. Mitchison. 1997. Identification of novel graded polarity actin filament bundles in locomoting heart fibroblasts: implications for the generation of motile force. J. Cell Biol. 136:1287-1305. http://dx.doi.org/10.1083/jcb.136.6.1287
6. Delanoë-Ayari, H., S. Iwaya, Y.T. Maeda, J. Inose, C. Rivière, M. Sano, and J.P. Rieu. 2008. Changes in the magnitude and distribution of forces at different Dictyostelium developmental stages. Cell Motil. Cytoskeleton. 65:314-331. http://dx.doi.org/10.1002/cm.20262
7. Döbereiner, H.G., B. Dubin-Thaler, G. Giannone, H.S. Xenias, and M.P. Sheetz. 2004. Dynamic phase transitions in cell spreading. Phys. Rev. Lett. 93:108105. http://dx.doi.org/10.1103/PhysRevLett.93.108105
8. DuFort, C.C., M.J. Paszek, and V.M. Weaver. 2011. Balancing forces: architectural control of mechanotransduction. Nat. Rev. Mol. Cell Biol. 12:308-319. http://dx.doi.org/10.1038/nrm3112
9. Elia, N., R. Sougrat, T.A. Spurlin, J.H. Hurley, and J. Lippincott-Schwartz. 2011. Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc. Natl. Acad. Sci. USA. 108:4846-4851. http://dx.doi.org/ 10.1073/pnas.1102714108
10. Even-Ram, S., A.D. Doyle, M.A. Conti, K. Matsumoto, R.S. Adelstein, and K.M. Yamada. 2007. Myosin IIA regulates cell motility and actomyosinmicrotubule crosstalk. Nat. Cell Biol. 9:299-309. http://dx.doi.org/10 .1038/ncb1540
11. Farge, E. 2011. Mechanotransduction in development. Curr. Top. Dev. Biol. 95:243-265. http://dx.doi.org/10.1016/B978-0-12-385065-2.00008-6
12. Fiolka, R., L. Shao, E.H. Rego, M.W. Davidson, and M.G. Gustafsson. 2012. Time-lapse two-color 3D imaging of live cells with doubled resolution using structured illumination. Proc. Natl. Acad. Sci. USA. 109:5311-5315. http://dx.doi.org/10.1073/pnas.1119262109
13. Gardel, M.L., B. Sabass, L. Ji, G. Danuser, U.S. Schwarz, and C.M. Waterman. 2008. Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed. J. Cell Biol. 183:999-1005. http://dx.doi.org/10 .1083/jcb.200810060
14. Gardel, M.L., I.C. Schneider, Y. Aratyn-Schaus, and C.M. Waterman. 2010. Mechanical integration of actin and adhesion dynamics in cell migration. Annu. Rev. Cell Dev. Biol. 26:315-333. http://dx.doi.org/10.1146/ annurev.cellbio.011209.122036
15. Gustafsson, M.G., L. Shao, P.M. Carlton, C.J. Wang, I.N. Golubovskaya, W.Z. Cande, D.A. Agard, and J.W. Sedat. 2008. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 94:4957-4970. http://dx.doi.org/10.1529/ biophysj.107.120345
16. Heath, J.P. 1981. Arcs: curved microfilament bundles beneath the dorsal surface of the leading lamellae of moving chick embryo fibroblasts. Cell Biol. Int. Rep. 5:975-980. http://dx.doi.org/10.1016/0309-1651(81) 90214-9
17. Heath, J.P., and B.F. Holifield. 1993. On the mechanisms of cortical actin flow and its role in cytoskeletal organisation of fibroblasts. Symp. Soc. Exp. Biol. 47:35-56.
18. Hotulainen, P., and P. Lappalainen. 2006. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J. Cell Biol. 173:383-394. http://dx.doi.org/10.1083/jcb.200511093
19. Hu, K., L. Ji, K.T. Applegate, G. Danuser, and C.M. Waterman-Storer. 2007. Differential transmission of actin motion within focal adhesions. Science. 315:111-115. http://dx.doi.org/10.1126/science.1135085
20. Keren, K., Z. Pincus, G.M. Allen, E.L. Barnhart, G. Marriott, A. Mogilner, and J.A. Theriot. 2008. Mechanism of shape determination in motile cells. Nature. 453:475-480. http://dx.doi.org/10.1038/nature06952
21. Legant, W.R., C.K. Choi, J.S. Miller, L. Shao, L. Gao, E. Betzig, and C.S. Chen. 2013. Multidimensional traction force microscopy reveals out-of-plane rotational moments about focal adhesions. Proc. Natl. Acad. Sci. USA. 110:881-886. http://dx.doi.org/10.1073/pnas.1207997110
22. Levin, M. 2012. Morphogenetic fields in embryogenesis, regeneration, and cancer: non-local control of complex patterning. Biosystems. 109:243-261. http://dx.doi.org/10.1016/j.biosystems.2012.04.005
23. Medeiros, N.A., D.T. Burnette, and P. Forscher. 2006. Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat. Cell Biol. 8:216-226. http://dx.doi.org/10.1038/ncb1367
24. Mogilner, A., and K. Keren. 2009. The shape of motile cells. Curr. Biol. 19:R762-R771. http://dx.doi.org/10.1016/j.cub.2009.06.053
25. Ponti, A., M. Machacek, S.L. Gupton, C.M. Waterman-Storer, and G. Danuser. 2004. Two distinct actin networks drive the protrusion of migrating cells. Science. 305:1782-1786. http://dx.doi.org/10.1126/science.1100533
26. Rambold, A.S., B. Kostelecky, N. Elia, and J. Lippincott-Schwartz. 2011. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl. Acad. Sci. USA. 108:10190-10195. http://dx.doi.org/10.1073/pnas.1107402108
27. Riahi, R., Y. Yang, D.D. Zhang, and P.K. Wong. 2012. Advances in woundhealing assays for probing collective cell migration. J. Lab. Autom. 17:59-65.
28. Sanger, J.W., S. Kang, C.C. Siebrands, N. Freeman, A. Du, J. Wang, A.L. Stout, and J.M. Sanger. 2005. How to build a myofibril. J. Muscle Res. Cell Motil. 26:343-354. http://dx.doi.org/10.1007/s10974-005-9016-7
29. Sanger, J.W., J. Wang, Y. Fan, J. White, and J.M. Sanger. 2010. Assembly and dynamics of myofibrils. J. Biomed. Biotechnol. 2010:858606. http://dx.doi.org/10.1155/2010/858606
30. Shao, L., P. Kner, E.H. Rego, and M.G. Gustafsson. 2011. Super-resolution 3D microscopy of live whole cells using structured illumination. Nat. Methods. 8:1044-1046. http://dx.doi.org/10.1038/nmeth.1734
31. Small, J.V., K. Rottner, I. Kaverina, and K.I. Anderson. 1998. Assembling an actin cytoskeleton for cell attachment and movement. Biochim. Biophys. Acta. 1404:271-281. http://dx.doi.org/10.1016/S0167-4889(98)00080-9
32. Straight, A.F., A. Cheung, J. Limouze, I. Chen, N.J. Westwood, J.R. Sellers, and T.J. Mitchison. 2003. Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science. 299:1743-1747. http://dx.doi.org/10.1126/science.1081412
33. Svitkina, T.M., A.B. Verkhovsky, K.M. McQuade, and G.G. Borisy. 1997. Analysis of the actin-myosin II system in fish epidermal keratocytes: mechanism of cell body translocation. J. Cell Biol. 139:397-415. http:// dx.doi.org/10.1083/jcb.139.2.397
34. Tojkander, S., G. Gateva, G. Schevzov, P. Hotulainen, P. Naumanen, C. Martin, P.W. Gunning, and P. Lappalainen. 2011. A molecular pathway for myosin II recruitment to stress fibers. Curr. Biol. 21:539-550. http://dx.doi.org/10.1016/j.cub.2011.03.007
35. Vallenius, T. 2013. Actin stress fibre subtypes in mesenchymal-migrating cells. Open Biol. 3:130001. http://dx.doi.org/10.1098/rsob.130001
36. Verkhovsky, A.B., T.M. Svitkina, and G.G. Borisy. 1995. Myosin II filament assemblies in the active lamella of fibroblasts: their morphogenesis and role in the formation of actin filament bundles. J. Cell Biol. 131:989-1002. http://dx.doi.org/10.1083/jcb.131.4.989
37. Vicente-Manzanares, M., X. Ma, R.S. Adelstein, and A.R. Horwitz. 2009. Nonmuscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10:778-790. http://dx.doi.org/10.1038/nrm2786
38. Wang, N., I.M. Tolić-Nørrelykke, J. Chen, S.M. Mijailovich, J.P. Butler, J.J. Fredberg, and D. Stamenović. 2002. Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am. J. Physiol. Cell Physiol. 282:C606-C616. http://dx.doi.org/10.1152/ajpcell.00269.2001
39. Watanabe, T., and Y. Takahashi. 2010. Tissue morphogenesis coupled with cell shape changes. Curr. Opin. Genet. Dev. 20:443-447. http://dx.doi.org/ 10.1016/j.gde.2010.05.004
40. Xu, K., H.P. Babcock, and X. Zhuang. 2012. Dual-objective STORM reveals three-dimensional filament organization in the actin cytoskeleton. Nat. Methods. 9:185-188. http://dx.doi.org/10.1038/nmeth.1841
41. Zhang, X.F., A.W. Schaefer, D.T. Burnette, V.T. Schoonderwoert, and P. Forscher. 2003. Rho-dependent contractile responses in the neuronal growth cone are independent of classical peripheral retrograde actin flow. Neuron. 40:931-944. http://dx.doi.org/10.1016/S0896-6273(03)00754-2
42. Zhang, H., C. Gally, and M. Labouesse. 2010. Tissue morphogenesis: how multiple cells cooperate to generate a tissue. Curr. Opin. Cell Biol. 22:575-582. http://dx.doi.org/10.1016/j.ceb.2010.08.011