Migrating fibroblasts reorient directionality: By a metastable, PI3K-dependent mechanism

Journal of Cell Biology

Volumn 197, Issue 1, 2012, Pages 105-114

  Welf, Erik S ^a   Ahmed, Shoeb ^a   Johnson, Heath E ^a   Melvin, Adam T ^a   Haugh, Jason M ^a  

^a North Carolina State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; RAC PROTEIN;

ARTICLE; CELL MIGRATION; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME LOCALIZATION; FIBROBLAST; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MESENCHYME CELL; MOLECULAR MECHANICS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; FIBROBLASTS; MICE; NIH 3T3 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; SIGNAL TRANSDUCTION;

EID: 84860295783     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201108152     Document Type: Article

References (56)

1. Abercrombie, M., J.E. Heaysman, and S.M. Pegrum. 1970. The locomotion of fibroblasts in culture. I. Movements of the leading edge. Exp. Cell Res. 59:393-398. http://dx.doi.org/10.1016/0014-4827(70)90646-4
2. Andrew, N., and R.H. Insall. 2007. Chemotaxis in shallow gradients is mediated independently of PtdIns 3-kinase by biased choices between random protrusions. Nat. Cell Biol. 9:193-200. http://dx.doi.org/10.1038/ncb1536
3. Arrieumerlou, C., and T. Meyer. 2005. A local coupling model and compass parameter for eukaryotic chemotaxis. Dev. Cell. 8:215-227. http://dx.doi.org/10.1016/j.devcel.2004.12.007
4. Bosgraaf, L., and P.J. Van Haastert. 2009a. Navigation of chemotactic cells by parallel signaling to pseudopod persistence and orientation. PLoS ONE. 4:e6842. http://dx.doi.org/10.1371/journal.pone.0006842
5. Bosgraaf, L., and P.J.M. Van Haastert. 2009b. The ordered extension of pseudopodia by amoeboid cells in the absence of external cues. PLoS ONE. 4:e5253. http://dx.doi.org/10.1371/journal.pone.0005253
6. Bosgraaf, L., I. Keizer-Gunnink, and P.J.M. Van Haastert. 2008. PI3-kinase signaling contributes to orientation in shallow gradients and enhances speed in steep chemoattractant gradients. J. Cell Sci. 121:3589-3597. http://dx.doi.org/10.1242/jcs.031781
7. Bosgraaf, L., P.J. van Haastert, and T. Bretschneider. 2009. Analysis of cell movement by simultaneous quantification of local membrane displacement and fluorescent intensities using Quimp2. Cell Motil. Cytoskeleton. 66:156-165. http://dx.doi.org/10.1002/cm.20338
8. Cirit, M., M. Krajcovic, C.K. Choi, E.S. Welf, A.F. Horwitz, and J.M. Haugh. 2010. Stochastic model of integrin-mediated signaling and adhesion dynamics at the leading edges of migrating cells. PLOS Comput. Biol. 6:e1000688. http://dx.doi.org/10.1371/journal.pcbi.1000688
9. Danuser, G. 2005. Coupling the dynamics of two actin networks-new views on the mechanics of cell protrusion. Biochem. Soc. Trans. 33:1250-1253. http://dx.doi.org/10.1042/BST20051250
10. Dhand, R., K. Hara, I. Hiles, B. Bax, I. Gout, G. Panayotou, M.J. Fry, K. Yonezawa, M. Kasuga, and M.D. Waterfield. 1994. PI 3-kinase: Structural and functional analysis of intersubunit interactions. EMBO J. 13:511-521.
11. Döbereiner, H.G., B.J. Dubin-Thaler, J.M. Hofman, H.S. Xenias, T.N. Sims, G. Giannone, M.L. Dustin, C.H. Wiggins, and M.P. Sheetz. 2006. Lateral membrane waves constitute a universal dynamic pattern of motile cells. Phys. Rev. Lett. 97:038102. http://dx.doi.org/10.1103/PhysRevLett.97.038102
12. Dunn, G.A., and A.F. Brown. 1987. A unified approach to analysing cell motility. J. Cell Sci. Suppl. 8:81-102.
13. Friedl, P., and K. Wolf. 2010. Plasticity of cell migration: A multiscale tuning model. J. Cell Biol. 188:11-19. http://dx.doi.org/10.1083/jcb.200909003
14. Gail, M.H., and C.W. Boone. 1970. The locomotion of mouse fibroblasts in tissue culture. Biophys. J. 10:980-993. http://dx.doi.org/10.1016/S0006-3495(70)86347-0
15. Giannone, G., B.J. Dubin-Thaler, H.-G. Döbereiner, N. Kieffer, A.R. Bresnick, and M.P. Sheetz. 2004. Periodic lamellipodial contractions correlate with rearward actin waves. Cell. 116:431-443. http://dx.doi.org/10.1016/S0092-8674(04)00058-3
16. Gupton, S.L., K.L. Anderson, T.P. Kole, R.S. Fischer, A. Ponti, S.E. Hitchcock-DeGregori, G. Danuser, V.M. Fowler, D. Wirtz, D. Hanein, and C.M. Waterman-Storer. 2005. Cell migration without a lamellipodium: Translation of actin dynamics into cell movement mediated by tropomyosin. J. Cell Biol. 168:619-631. http://dx.doi.org/10.1083/jcb.200406063
17. Hoeller, O., and R.R. Kay. 2007. Chemotaxis in the absence of PIP3 gradients. Curr. Biol. 17:813-817. http://dx.doi.org/10.1016/j.cub.2007.04.004
18. Laukaitis, C.M., D.J. Webb, K. Donais, and A.F. Horwitz. 2001. Differential dynamics of α5 integrin, paxillin, and α-actinin during formation and disassembly of adhesions in migrating cells. J. Cell Biol. 153:1427-1440. http://dx.doi.org/10.1083/jcb.153.7.1427
19. Lebensohn, A.M., and M.W. Kirschner. 2009. Activation of the WAVE complex by coincident signals controls actin assembly. Mol. Cell. 36:512-524. http://dx.doi.org/10.1016/j.molcel.2009.10.024
20. Lo, C.-M., D.B. Buxton, G.C.H. Chua, M. Dembo, R.S. Adelstein, and Y.-L. Wang. 2004. Nonmuscle myosin IIb is involved in the guidance of fibroblast migration. Mol. Biol. Cell. 15:982-989. http://dx.doi.org/10.1091/mbc.E03-06-0359
21. Loovers, H.M., M. Postma, I. Keizer-Gunnink, Y.E. Huang, P.N. Devreotes, and P.J. van Haastert. 2006. Distinct roles of PI(3,4,5)P3 during chemoattractant signaling in Dictyostelium: A quantitative in vivo analysis by inhibition of PI3-kinase. Mol. Biol. Cell. 17:1503-1513. http://dx.doi.org/10.1091/mbc.E05-09-0825
22. Machacek, M., and G. Danuser. 2006. Morphodynamic profiling of protrusion phenotypes. Biophys. J. 90:1439-1452. http://dx.doi.org/10.1529/biophysj.105.070383
23. Machacek, M., L. Hodgson, C. Welch, H. Elliott, O. Pertz, P. Nalbant, A. Abell, G.L. Johnson, K.M. Hahn, and G. Danuser. 2009. Coordination of Rho GTPase activities during cell protrusion. Nature. 461:99-103. http://dx.doi.org/10.1038/nature08242
24. Melvin, A.T., E.S. Welf, Y. Wang, D.J. Irvine, and J.M. Haugh. 2011. In chemotaxing fibroblasts, both high-fidelity and weakly biased cell movements track the localization of PI3K signaling. Biophys. J. 100:1893-1901. http://dx.doi.org/10.1016/j.bpj.2011.02.047
25. Merlot, S., and R.A. Firtel. 2003. Leading the way: Directional sensing through phosphatidylinositol 3-kinase and other signaling pathways. J. Cell Sci. 116:3471-3478. http://dx.doi.org/10.1242/jcs.00703
26. Millius, A., S.N. Dandekar, A.R. Houk, and O.D. Weiner. 2009. Neutrophils establish rapid and robust WAVE complex polarity in an actin-dependent fashion. Curr. Biol. 19:253-259. http://dx.doi.org/10.1016/j.cub.2008.12.044
27. Monypenny, J., D. Zicha, C. Higashida, F. Oceguera-Yanez, S. Narumiya, and N. Watanabe. 2009. Cdc42 and Rac family GTPases regulate mode and speed but not direction of primary fibroblast migration during plateletderived growth factor-dependent chemotaxis. Mol. Cell. Biol. 29:2730-2747. http://dx.doi.org/10.1128/MCB.01285-08
28. Oikawa, T., H. Yamaguchi, T. Itoh, M. Kato, T. Ijuin, D. Yamazaki, S. Suetsugu, and T. Takenawa. 2004. PtdIns(3,4,5)P3 binding is necessary for WAVE2-induced formation of lamellipodia. Nat. Cell Biol. 6:420-426. http://dx.doi.org/10.1038/ncb1125
29. Pankov, R., Y. Endo, S. Even-Ram, M. Araki, K. Clark, E. Cukierman, K. Matsumoto, and K.M. Yamada. 2005. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170:793-802. http://dx.doi.org/10.1083/jcb.200503152
30. Petrie, R.J., A.D. Doyle, and K.M. Yamada. 2009. Random versus directionally persistent cell migration. Nat. Rev. Mol. Cell Biol. 10:538-549. http://dx.doi.org/10.1038/nrm2729
31. 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
32. Postma, M., J. Roelofs, J. Goedhart, T.W.J. Gadella, A.J.W.G. Visser, and P.J.M. Van Haastert. 2003. Uniform cAMP stimulation of Dictyostelium cells induces localized patches of signal transduction and pseudopodia. Mol. Biol. Cell. 14:5019-5027. http://dx.doi.org/10.1091/mbc.E03-08-0566
33. Ridley, A.J., M.A. Schwartz, K. Burridge, R.A. Firtel, M.H. Ginsberg, G. Borisy, J.T. Parsons, and A.R. Horwitz. 2003. Cell migration: Integrating signals from front to back. Science. 302:1704-1709. http://dx.doi.org/10.1126/science.1092053
34. Riedl, J., A.H. Crevenna, K. Kessenbrock, J.H. Yu, D. Neukirchen, M. Bista, F. Bradke, D. Jenne, T.A. Holak, Z. Werb, et al. 2008. Lifeact: A versatile marker to visualize F-actin. Nat. Methods. 5:605-607. http://dx.doi.org/10.1038/nmeth.1220
35. Sabouri-Ghomi, M., Y. Wu, K. Hahn, and G. Danuser. 2008. Visualizing and quantifying adhesive signals. Curr. Opin. Cell Biol. 20:541-550. http://dx.doi.org/10.1016/j.ceb.2008.05.004
36. Sasaki, A.T., C. Janetopoulos, S. Lee, P.G. Charest, K. Takeda, L.W. Sundheimer, R. Meili, P.N. Devreotes, and R.A. Firtel. 2007. G protein-independent Ras/PI3K/F-actin circuit regulates basic cell motility. J. Cell Biol. 178: 185-191. http://dx.doi.org/10.1083/jcb.200611138
37. Schneider, I.C., and J.M. Haugh. 2004. Spatial analysis of 3' phosphoinositide signaling in living fibroblasts: II. Parameter estimates for individual cells from experiments. Biophys. J. 86:599-608. http://dx.doi.org/10.1016/S0006-3495(04)74138-7
38. Schneider, I.C., and J.M. Haugh. 2005. Quantitative elucidation of a distinct spatial gradient-sensing mechanism in fibroblasts. J. Cell Biol. 171:883-892. http://dx.doi.org/10.1083/jcb.200509028
39. Schneider, I.C., E.M. Parrish, and J.M. Haugh. 2005. Spatial analysis of 3' phosphoinositide signaling in living fibroblasts, III: Influence of cell morphology and morphological Polarity. Biophys. J. 89:1420-1430. http://dx.doi.org/10.1529/biophysj.105.061218
40. Sossey-Alaoui, K., X.R. Li, T.A. Ranalli, and J.K. Cowell. 2005. WAVE3-mediated cell migration and lamellipodia formation are regulated downstream of phosphatidylinositol 3-kinase. J. Biol. Chem. 280:21748-21755. http://dx.doi.org/10.1074/jbc.M500503200
41. Swaney, K.F., C.H. Huang, and P.N. Devreotes. 2010. Eukaryotic chemotaxis: A network of signaling pathways controls motility, directional sensing, and polarity. Annu Rev Biophys. 39:265-289. http://dx.doi.org/10.1146/annurev.biophys.093008.131228
42. Takeda, K., A.T. Sasaki, H.J. Ha, H.A. Seung, and R.A. Firtel. 2007. Role of phosphatidylinositol 3-kinases in chemotaxis in Dictyostelium. J. Biol. Chem. 282:11874-11884. http://dx.doi.org/10.1074/jbc.M610984200
43. Tsukada, Y., K. Aoki, T. Nakamura, Y. Sakumura, M. Matsuda, and S. Ishii. 2008. Quantification of local morphodynamics and local GTPase activity by edge evolution tracking. PLOS Comput. Biol. 4:e1000223. http:// dx.doi.org/10.1371/journal.pcbi.1000223
44. Uetrecht, A.C., and J.E. Bear. 2009. Golgi polarity does not correlate with speed or persistence of freely migrating fibroblasts. Eur. J. Cell Biol. 88:711-717. http://dx.doi.org/10.1016/j.ejcb.2009.08.001
45. Van Haastert, P.J. 2010. A stochastic model for chemotaxis based on the ordered extension of pseudopods. Biophys. J. 99:3345-3354. http://dx.doi.org/10.1016/j.bpj.2010.09.042
46. van Haastert, P.J., and M. Postma. 2007. Biased random walk by stochastic fluctuations of chemoattractant-receptor interactions at the lower limit of detection. Biophys. J. 93:1787-1796. http://dx.doi.org/10.1529/biophysj.107.104356
47. Van Haastert, P.J.M., and P.N. Devreotes. 2004. Chemotaxis: Signalling the way forward. Nat. Rev. Mol. Cell Biol. 5:626-634. http://dx.doi.org/10.1038/nrm1435
48. Vicente-Manzanares, M., J. Zareno, L. Whitmore, C.K. Choi, and A.F. Horwitz. 2007. Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J. Cell Biol. 176:573-580. http://dx.doi.org/10.1083/jcb.200612043
49. Vicente-Manzanares, M., C.K. Choi, and A.R. Horwitz. 2009. Integrins in cell migration-the actin connection. J. Cell Sci. 122:199-206. http://dx.doi.org/10.1242/jcs.018564
50. Ware, M.F., A. Wells, and D.A. Lauffenburger. 1998. Epidermal growth factor alters fibroblast migration speed and directional persistence reciprocally and in a matrix-dependent manner. J. Cell Sci. 111:2423-2432.
51. Weiger, M.C., C.-C. Wang, M. Krajcovic, A.T. Melvin, J.J. Rhoden, and J.M. Haugh. 2009. Spontaneous phosphoinositide 3-kinase signaling dynamics drive spreading and random migration of fibroblasts. J. Cell Sci. 122:313-323. http://dx.doi.org/10.1242/jcs.037564
52. Weiger, M.C., S. Ahmed, E.S. Welf, and J.M. Haugh. 2010. Directional persistence of cell migration coincides with stability of asymmetric intracellular signaling. Biophys. J. 98:67-75. http://dx.doi.org/10.1016/j.bpj.2009.09.051
53. Weiner, O.D., W.A. Marganski, L.F. Wu, S.J. Altschuler, and M.W. Kirschner. 2007. An actin-based wave generator organizes cell motility. PLoS Biol. 5:e221. http://dx.doi.org/10.1371/journal.pbio.0050221
54. Wu, Y.I., D. Frey, O.I. Lungu, A. Jaehrig, I. Schlichting, B. Kuhlman, and K.M. Hahn. 2009. A genetically encoded photoactivatable Rac controls the motility of living cells. Nature. 461:104-108. http://dx.doi.org/10.1038/nature08241
55. Xiong, Y., C.H. Huang, P.A. Iglesias, and P.N. Devreotes. 2010. Cells navigate with a local-excitation, global-inhibition-biased excitable network. Proc. Natl. Acad. Sci. USA. 107:17079-17086. http://dx.doi.org/10.1073/pnas.1011271107
56. Yoo, S.K., Q. Deng, P.J. Cavnar, Y.I. Wu, K.M. Hahn, and A. Huttenlocher. 2010. Differential regulation of protrusion and polarity by PI3K during neutrophil motility in live zebrafish. Dev. Cell. 18:226-236. http://dx.doi.org/10.1016/j.devcel.2009.11.015