Pak1 and Pak2 mediate tumor cell invasion through distinct signaling mechanisms

Molecular and Cellular Biology

Volumn 28, Issue 12, 2008, Pages 4162-4172

  Coniglio, Salvatore J ^a,b   Zavarella, Salvatore ^b   Symons, Marc H ^a,b,c  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c NORTH SHORE UNIVERSITY HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COFILIN; MYOSIN LIGHT CHAIN; NEU DIFFERENTIATION FACTOR; P21 ACTIVATED KINASE 1; P21 ACTIVATED KINASE 2; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; BREAST CARCINOMA; CANCER INVASION; CELL INVASION; FOCAL ADHESION; HUMAN; HUMAN CELL; LAMELLIPODIUM; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; TUMOR CELL;

BREAST NEOPLASMS; CARCINOMA; CELL ADHESION; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEUREGULIN-1; P21-ACTIVATED KINASES; PHOSPHORYLATION; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 44949176114     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01532-07     Document Type: Article

References (61)

1. Adam, L., R. Vadlamudi, M. Mandal, J. Chernoff, and R. Kumar. 2000. Regulation of microfilament reorganization and invasiveness of breast cancer cells by kinase dead p21-activatcd kinase-1. J. Biol. Chem. 275:12041-12050.
2. Alberts, A. S., H. Qin, H. S. Carr, and J. A. Frost. 2005. PAK1 negatively regulates the activity of the Rho exchange factor NET1. J. Biol. Chem. 280:12152-12161.
3. Azim, A. C., K. L. Barkalow, and J. H. Hartwig. 2000. Determination of GTP loading on Rac and Cdc42 in platelets and fibroblasts. Methods Enzymol. 325:257-263.
4. Ballestrem, C., B. Hinz, B. A. Imhof, and B. Wehrle-Haller. 2001. Marching at the front and dragging behind: differential alphaVbeta3-integrin turnover regulates focal adhesion behavior. J. Cell Biol. 155:1319-1332.
5. Bamburg, J. R. 1999. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15:185-230.
6. Bokoch, G. M. 2003. Biology of the p21-activated kinases. Annu. Rev. Biochem. 72:743-781.
7. Bokoch, G. M., A. M. Reilly, R. H. Daniels, C. C. King, A. Olivera, S. Spiegel, and U. G. Knaus. 1998. A GTPase-independent mechanism of p21-activated kinase activation. Regulation by sphingosine and other biologically active lipids. J. Biol. Chem. 273:8137-8144.
8. Brown, M. C., K. A. West, and C. E. Turner. 2002. Paxillin-dependent paxillin kinase linker and p21-activatcd kinase localization to focal adhesions involves a multistep activation pathway. Mol. Biol. Cell 13:1550-1565.
9. Chan, A. Y., S. J. Coniglio, Y. Y. Chuang, D. Michaelson, U. G. Knaus, M. R. Philips, and M. Symons. 2005. Roles of the Rac1 and Rac3 GTPases in human tumor cell invasion. Oncogene 24:7821-7829.
10. Chew, T. L., R. A. Masaraeehia, Z. M. Goeckeler, and R. B. Wysolmerski. 1998. phosphorylation of non-muscle myosin II regulatory light chain by p21-activated kinase (gamma-PAK). J. Muscle Res. Cell Motil. 19:839-854.
11. Chrzanowska-Wodnicka, M., and K. Burridge. 1996. Rho-stimulated contractilitv drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133:1403-1415.
12. Dharmawardhane, S., L. C. Sanders, S. S. Martin, R. H. Daniels, and G. M. Bokoch. 1997. Localization of p21-activated kinase 1 (PAK1) to pinocytic vesicles and cortical actin structures in stimulated cells. J. Cell Biol. 138: 1265-1278.
13. Edwards, D. C., L. C. Sanders, G. M. Bokoch, and G. N. Gill. 1999. Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell Biol. 1:253-259.
14. Friedl, P. 2004. Prcspecification and plasticity: shifting mechanisms of cell migration. Curr. Opin. Cell Biol. 16:14-23.
15. Ghosh, M., X. Song, G. Mouneimne, M. Sidani, D. S. Lawrence, and J. S. Condeelis. 2004. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304:743-746.
16. Goeckeler, Z. M., R. A. Masaraeehia, Q. Zeng, T. L. Chew, P. Gallagher, and R. B. Wysolmerski. 2000. phosphorylation of myosin light chain kinase by p21-activatcd kinase PAK2. J. Biol. Chem. 275:18366- 18374.
17. Hofmann, C., M. Shepelev, and J. Chernoff. 2004. The genetics of Pak. J. Cell Sci. 117:4343-4354.
18. Huang, T. Y., C. DerMardirossian, and G. M. Bokoch. 2006. Cofilin phosphatases and regulation of actin dynamics. Curr. Opin. Cell Biol. 18:26-31.
19. Huang, Z., J. Ling, and J. A. Traugh. 2003. Localization of p21-activated protein kinase gamma-PAK/Pak2 in the endoplasmic reticulum is required for induction of cytostasis. J. Biol. Chem. 278:13101-13109.
20. Ichetovkin, I., W. Grant, and J. Condeelis. 2002. Cofilin produces newly polymerized actin filaments that are preferred for dendritic nucleation by the Arp2/3 complex. Curr. Biol. 12:79-84.
21. Kumar, R., A. E. Gururaj, and C. J. Barnes. 2006. p21-activated kinases in cancer. Nat. Rev. Cancer 6:459-471.
22. Lucanic, M., M. Kiley, N. Ashcroft, N. L'etoile, and H. J. Cheng. 2006. The Caenorhabditis elegans P21-activated kinases are differentially required for UNC-6/netrin-mediated commissural motor axon guidance. Development 133:4549-4559.
23. Manabe, R., M. Kovalenko, D. J. Webb, and A. R. Horwitz. 2002. GIT1 functions in a motile, multi-molecular signaling complex that regulates protrusive activity and cell migration. J. Cell Sci. 115:1497-1510.
24. Manser, E., H. Y. Huang, T. H. Loo, X. Q. Chen, J. M. Dong, T. Leung, and L. Lim. 1997. Expression of constitutively active α-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17:1129-1143.
25. Manser, E., T. H. Loo, C. G. Koh, Z. S. Zhao, X. Q. Chen, L. Tan, I. Tan, T. Leung, and L. Lim. 1998. PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell 1:183-192.
26. Marone, R., D. Hess, D. Dankort, W. J. Muller, N. E. Hynes, and A. Badaehe. 2004. Memo mediates ErbB2-driven cell motility. Nat. Cell Biol. 6:515-522.
27. Matsumura, F. 2005. Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 15:371-377.
28. Nagata-Ohashi, K., Y. Ohta, K. Goto, S. Chiba, R. Mori, M. Nishita, K. Ohashi, K. Kousaka, A. Iwamatsu, R. Niwa, T. Uemura, and K. Mizuno. 2004. A pathway of neuregulin-induced activation of cofilin-phosphatase Slingshot and cofilin in lamellipodia. J. Cell Biol. 165:465-471.
29. Nayal, A., D. J. Webb, C. M. Brown, E. M. Schaefer, M. Vicente-Manzanares, and A. R. Horwitz. 2006. Paxillin phosphorylation at Ser273 localizes a GIT1-PIX-PAK complex and regulates adhesion and protrusion dynamics. J. Cell Biol. 173:587-589.
30. Nimnual, A. S., L. J. Taylor, and D. Bar-Sagi. 2003. Redox-dependent downregulation of Rho by Rac. Nat. Cell Biol. 5:236-241.
31. Otto, I. M., T. Raabe, U. E. Rennefahrt, P. Bork, U. R. Rapp, and E. Kerkhoff. 2000. The p150-Spir protein provides a link between c-Jun N-terminal kinase function and actin reorganization. Curr. Biol. 10:345-348.
32. Ren, X. D., W. B. Kiosses, and M. A. Schwartz. 1999. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18:578-585.
33. Rennefahrt, U. E., S. W. Deacon, S. A. Parker, K. Devarajan, A. Beeser, J. Chernoff, S. Knapp, B. E. Turk, and J. R. Peterson. 2007. Specificity profiling of Pak kinases allows identification of novel phosphorylation sites. J. Biol. Chem. 282:15667-15678.
34. 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.
35. Riveline, D., E. Zamir, N. Q. Balaban, U. S. Schwarz, T. Ishizaki, S. Narumiya, Z. Kam, B. Geiger, and A. D. Bershadsky. 2001. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153:1175-1186.
36. Roig, J., and J. A. Traugh. 1999. p21-activated protein kinase gamma-PAK is activated by ionizing radiation and other DNA-damaging agents. Similarities and differences to alpha-PAK. J. Biol. Chem. 274:31119- 31122.
37. Rottner, K., A. Hall, and J. V. Small. 1999. Interplay between Rac and Rho in the control of substrate contact dynamics. Curr. Biol. 9:640-648.
38. Rudel, T., and G. M. Bokoch. 1997. Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276:1571-1574.
39. Sahai, E. 2005. Mechanisms of cancer cell invasion. Curr. Opin. Genet. Dev. 15:87-96.
40. Sahai, E., and C. J. Marshall. 2003. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5:711-719.
41. Salhia, B., F. Rutten, M. Nakada, C. Beaudry, M. Berens, A. Kwan, and J. T. Rutka. 2005. Inhibition of Rho-kinase affects astrocytoma morphology, motility, and invasion through activation of Rac1. Cancer Res. 65:8792-8800.
42. Sander, E. E., J. P. ten Klooster, S. van Delft, R. A. van der Kammen, and J. G. Collard. 1999. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147:1009-1022.
43. Sanders, L. C., F. Matsumura, G. M. Bokoch, and P. de Lanerolle. 1999. Inhibition of myosin light chain kinase by p21-activated kinase. Science 283:2083-2085.
44. Scheurlen, W., and J. Kuhl. 1998. Current diagnostic and therapeutic management of CNS metastasis in childhood primitive neuroectodermal tumors and ependymomas. J. Neurooncol. 38:181-185.
45. Sells, M. A., J. T. Boyd, and J. Chernoff. 1999. p21-activated kinase 1 (Pak1) regulates cell motility in mammalian fibroblasts. J. Cell Biol. 145:837-849.
46. Sells, M. A., A. Pfaff, and J. Chernoff. 2000. Temporal and spatial distribution of activated Pak1 in fibroblasts. J. Cell Biol. 151:1449-1458.
47. Shu, S., X. Liu, and E. D. Korn. 2005. Blebbistatin and blebbistatin-inactivatcd myosin II inhibit myosin II-independent processes in Dictyostelium. Proc. Natl. Acad. Sci. USA 102:1472-1477.
48. Stockton, R. A., E. Schaefer, and M. A. Schwartz. 2004. p21-activated kinase regulates endothelial permeability through modulation of contractility. J. Biol. Chem. 279:46621-46630.
49. Stofega, M. R., L. C. Sanders, E. M. Gardiner, and G. M. Bokoch. 2004. Constitutive p21-activatcd kinase (PAK) activation in breast cancer cells as a result of mislocalization of PAK to focal adhesions. Mol. Biol. Cell 15:2965-2977.
50. 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.
51. ten Klooster, J. P., Z. M. Jaffer, J. Chernoff, and P. L. Hordijk. 2006. Targeting and activation of Rac1 are mediated by the exchange factor beta-Pix. J. Cell Biol. 172:759-769.
52. Totsukawa, G., Y. Yamakita, S. Yamashiro, D. J. Hartshorne, Y. Sasaki, and F. Matsumura. 2000. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150:797-806.
53. Vadlamudi, R. K., L. Adam, R. A. Wang, M. Mandal, D. Nguyen, A. Sahin, J. Chernoff, M. C. Hung, and R. Kumar. 2000. Regulatable expression of p21-activated kinasc-1 promotes anchorage-independent growth and abnormal organization of mitotic spindles in human epithelial breast cancer cells. J. Biol. Chem. 275:36238-36244.
54. Vadlamudi, R. K., F. Li, L. Adam, D. Nguyen, Y. Ohta, T. P. Stossel, and R. Kumar. 2002. Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat. Cell Biol. 4:681-690.
55. Vadlamudi, R. K., F. Li, C. J. Barnes, R. Bagheri-Yarmand, and R. Kumar. 2004. p41-Arc subunit of human Arp2/3 complex is a p21-activated kinase-1-interacting substrate. EMBO Rep. 5:154-160.
56. Webb, B. A., S. Zhou, R. Eves, L. Shen, L. Jia, and A. S. Mak. 2006. phosphorylation of cortactin by p21-activated kinase. Arch. Biochem. Biophys. 456:183-193.
57. Wittmann, T., G. M. Bokoch, and C. M. Waterman-Storer. 2004. Regulation of microtubule destabilizing activity of Op18/stathmin downstream of Rac1. J. Biol. Chem. 279:6196-6203.
58. Wyckoff, J. B., S. E. Pinner, S. Gschmeissner, J. S. Condeelis, and E. Sahai. 2006. ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr. Biol. 16:1515-1523.
59. Yoneda, A., H. A. Multhaupt, and J. R. Couchman. 2005. The Rho kinases I and II regulate different aspects of myosin II activity. J. Cell Biol. 170:443-453.
60. Zeng, Q., D. Lagunoff, R. Masaraeehia, Z. Goeckeler, G. Cote, and R. Wysolmerski. 2000. Endothelial cell retraction is induced by PAK2 monophospliorylation of myosin II. J. Cell Sci. 113:471-482.
61. Zhao, Z. S., E. Manser, T. H. Loo, and L. Lim. 2000. Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol. Cell. Biol. 20:6354-6363.