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© The Rockefeller University Press, 0021-9525/1999//837 $5.00
The Journal of Cell Biology, Volume 145, Number 4, , 1999 837-849

p21-Activated Kinase 1 (Pak1) Regulates Cell Motility in Mammalian Fibroblasts

Fox Chase Cancer Center, Philadelphia, Pennsylvania 19111

The p21 (Cdc42/Rac) activated kinase Pak1 regulates cell morphology and polarity in most, if not all, eukaryotic cells. We and others have established that Pak's effects on these parameters are mediated by changes in the organization of cortical actin. Because cell motility requires polarized rearrangements of the actin/myosin cytoskeleton, we examined the role of Pak1 in regulating cell movement. We established clonal tetracycline-regulated NIH-3T3 cell lines that inducibly express either wild-type Pak1, a kinase-dead, or constitutively-active forms of this enzyme, and examined the morphology, F-actin organization, and motility of these cells. Expression of any of these forms of Pak1 induced dramatic changes in actin organization which were not inhibited by coexpression of a dominant-negative form of Rac1. Cells inducibly expressing wild-type or constitutively-active Pak1 had large, polarized lamellipodia at the leading edge, were more motile than their normal counterparts when plated on a fibronectin-coated surface, and displayed enhanced directional movement in response to an immobilized collagen gradient. In contrast, cells expressing a kinase-dead form of Pak1 projected multiple lamellipodia emerging from different parts of the cell simultaneously. These cells, though highly motile, displayed reduced persistence of movement when plated on a fibronectin-coated surface and had defects in directed motility toward immobilized collagen. Expression of constitutively activated Pak1 was accompanied by increased myosin light chain (MLC) phosphorylation, whereas expression of kinase-dead Pak1 had no effect on MLC. These results suggest that Pak1 affects the phosphorylation state of MLC, thus linking this kinase to a molecule that directly affects cell movement.

Key Words: p21-activated kinase • motility • GTPases • fibroblasts • phosphorylation

Abbreviations used in this paper: CS, calf serum; HA, hemagglutinin; LPA, lysophosphatidic acid; MAPK, mitogen-activated protein kinase; MLC, myosin light chain; Pak, p21-activated kinase; PBS, phosphate-buffered saline; PDGF, platelet-derived growth factor; PI3, phosphatidyl inositol 3; PIX, Pak-interacting exchange factor; SH3, src-homology 3; SAPK, stress-activated protein kinase.

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• Adam, L., Vadlamudi, R., Mandal, M., Chernoff, J., Kumar, R. (2000). Regulation of Microfilament Reorganization and Invasiveness of Breast Cancer Cells by Kinase Dead p21-activated Kinase-1. J. Biol. Chem. 275: 12041-12050 [Abstract] [Full Text]  
• Moore, T. M., Garg, R., Johnson, C., Coptcoat, M. J., Ridley, A. J., Morris, J. D. H. (2000). PSK, a Novel STE20-like Kinase Derived from Prostatic Carcinoma That Activates the c-Jun N-terminal Kinase Mitogen-activated Protein Kinase Pathway and Regulates Actin Cytoskeletal Organization. J. Biol. Chem. 275: 4311-4322 [Abstract] [Full Text]  
• Schürmann, A., Mooney, A. F., Sanders, L. C., Sells, M. A., Wang, H. G., Reed, J. C., Bokoch, G. M. (2000). p21-Activated Kinase 1 Phosphorylates the Death Agonist Bad and Protects Cells from Apoptosis. Mol. Cell. Biol. 20: 453-461 [Abstract] [Full Text]  
• Kishi, H., Mikawa, T., Seto, M., Sasaki, Y., Kanayasu-Toyoda, T., Yamaguchi, T., Imamura, M., Ito, M., Karaki, H., Bao, J., Nakamura, A., Ishikawa, R., Kohama, K. (2000). Stable Transfectants of Smooth Muscle Cell Line Lacking the Expression of Myosin Light Chain Kinase and Their Characterization with Respect to the Actomyosin System. J. Biol. Chem. 275: 1414-1420 [Abstract] [Full Text]  
• Mira, J.-P., Benard, V., Groffen, J., Sanders, L. C., Knaus, U. G. (2000). Endogenous, hyperactive Rac3 controls proliferation of breast cancer cells by a p21-activated kinase-dependent pathway. Proc. Natl. Acad. Sci. USA 97: 185-189 [Abstract] [Full Text]  
• Humbert, S, Dhavan, R, Tsai, L (2000). p39 activates cdk5 in neurons, and is associated with the actin cytoskeleton. J. Cell Sci. 113: 975-983 [Abstract]  
• Zeng, Q, Lagunoff, D, Masaracchia, R, Goeckeler, Z, Cote, G, Wysolmerski, R (2000). Endothelial cell retraction is induced by PAK2 monophosphorylation of myosin II. J. Cell Sci. 113: 471-482 [Abstract]  
• Sander, E. E., ten Klooster, J. P., van Delft, S., van der Kammen, R. A., Collard, J. G. (1999). Rac Downregulates Rho Activity: Reciprocal Balance between Both Gtpases Determines Cellular Morphology and Migratory Behavior. JCB 147: 1009-1022 [Abstract] [Full Text]  
• Kiosses, W. B., Daniels, R. H., Otey, C., Bokoch, G. M., Schwartz, M. A. (1999). A Role for P21-Activated Kinase in Endothelial Cell Migration. JCB 147: 831-844 [Abstract] [Full Text]  
• Joberty, G., Perlungher, R. R., Macara, I. G. (1999). The Borgs, a New Family of Cdc42 and TC10 GTPase-Interacting Proteins. Mol. Cell. Biol. 19: 6585-6597 [Abstract] [Full Text]  
• Fang, X., Burg, M. A., Barritt, D., Dahlin-Huppe, K., Nishiyama, A., Stallcup, W. B. (1999). Cytoskeletal Reorganization Induced by Engagement of the NG2 Proteoglycan Leads to Cell Spreading and Migration. Mol. Biol. Cell 10: 3373-3387 [Abstract] [Full Text]  
• Cheresh, D. A., Leng, J., Klemke, R. L. (1999). Regulation of Cell Contraction and Membrane Ruffling by Distinct Signals in Migratory Cells. JCB 146: 1107-1116 [Abstract] [Full Text]  

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