Rac1-dependent lamellipodial motility in prostate cancer PC-3 cells revealed by optogenetic control of Rac1 activity

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Kato, Takuma ^a   Kawai, Katsuhisa ^a   Egami, Youhei ^a   Kakehi, Yoshiyuki ^a   Araki, Nobukazu ^a  

^a KAGAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PROTEIN WAVE2; RAC1 PROTEIN; UNCLASSIFIED DRUG; ENZYME INHIBITOR;

ARTICLE; CANCER CELL; CELL MOTILITY; CELL STRAIN; CELL STRAIN PC 3; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; LAMELLIPODIUM; LASER; OPTOGENETICS; PHOTOACTIVATION; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ANTAGONISTS AND INHIBITORS; MALE; METABOLISM; MOVEMENT (PHYSIOLOGY); PATHOLOGY; PROSTATE TUMOR; PROTEIN TRANSPORT; PSEUDOPODIUM; TUMOR CELL LINE;

CELL LINE, TUMOR; ENZYME INHIBITORS; HUMANS; MALE; MOVEMENT; OPTOGENETICS; PHOSPHATIDYLINOSITOL 3-KINASES; PROSTATIC NEOPLASMS; PROTEIN TRANSPORT; PSEUDOPODIA; RAC1 GTP-BINDING PROTEIN;

EID: 84901291313     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097749     Document Type: Article

References (34)

1. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, et al. (2003) Cell migration: Integrating signals from front to back. Science 302: 1704-1709. (Pubitemid 37505725)
2. Vicente-Manzanares M, Webb DJ, Horwitz AR (2005) Cell migration at a glance. J Cell Sci 118: 4917-4919. (Pubitemid 41672422)
3. Jaffe AB, Hall A (2005) Rho GTPases: Biochemistry and biology. Annu Rev Cell Dev Biol 21: 247-269. (Pubitemid 41740635)
4. Knight-Krajewski S, Welsh CF, Liu Y, Lyons LS, Faysal JM, et al. (2004) Deregulation of the Rho GTPase, Rac1, suppresses cyclin-dependent kinase inhibitor p21(CIP1) levels in androgen-independent human prostate cancer cells. Oncogene 23: 5513-5522. (Pubitemid 39044062)
5. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y (2004) Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci U S A 101: 7618-7623. (Pubitemid 38658078)
6. Spiering D, Hodgson L (2011) Dynamics of the Rho-family small GTPases in actin regulation and motility. Cell Adh Migr 5: 170-180.
7. Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I, et al. (2009) A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461: 104-108.
8. Wu YI, Wang X, He L, Montell D, Hahn KM (2011) Spatiotemporal control of small GTPases with light using the LOV domain. Methods Enzymol 497: 393-407.
9. Rikitake Y, Takai Y (2011) Directional cell migration regulation by small G proteins, nectin-like molecule-5, and afadin. Int Rev Cell Mol Biol 287: 97-143.
10. Costa C, Germena G, Hirsch E (2010) Dissection of the interplay between class I PI3Ks and Rac signaling in phagocytic functions. ScientificWorldJournal 10: 1826-1839.
11. Weiner OD, Neilsen PO, Prestwich GD, Kirschner MW, Cantley LC, et al. (2002) A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat Cell Biol 4: 509-513.
12. Inoue T, Meyer T (2008) Synthetic activation of endogenous PI3K and Rac identifies an AND-gate switch for cell polarization and migration. PLoS One 3: e3068.
13. Welf ES, Ahmed S, Johnson HE, Melvin AT, Haugh JM (2012) Migrating fibroblasts reorient directionality by a metastable, PI3K-dependent mechanism. J Cell Biol 197: 105-114.
14. Yoo SK, Deng Q, Cavnar PJ, Wu YI, Hahn KM, et al. (2010) Differential regulation of protrusion and polarity by PI3K during neutrophil motility in live zebrafish. Dev Cell 18: 226-236.
15. Fujii M, Kawai K, Egami Y, Araki N (2013) Dissecting the roles of Rac1 activation and deactivation in macropinocytosis using microscopic photomanipulation. Sci Rep 3: 2385.
16. Araki N, Ikeda Y, Kato T, Kawai K, Egami Y, et al. (2014) Development of an automated fluorescence microscopy system for photomanipulation of genetically encoded photoactivatable proteins (optogenetics) in live cells. Microscopy 63: doi: 10.1093/jmicro/dfu003.
17. Lebensohn AM, Kirschner MW (2009) Activation of the WAVE complex by coincident signals controls actin assembly. Mol Cell 36: 512-524.
18. Suetsugu S, Kurisu S, Oikawa T, Yamazaki D, Oda A, et al. (2006) Optimization of WAVE2 complex-induced actin polymerization by membrane-bound IRSp53, PIP(3), and Rac. J Cell Biol 173: 571-585. (Pubitemid 43765203)
19. Suetsugu S, Yamazaki D, Kurisu S, Takenawa T (2003) Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev Cell 5: 595-609. (Pubitemid 37243048)
20. Abercrombie M, Heaysman JE, Pegrum SM (1970) The locomotion of fibroblasts in culture. II. "RRuffling". Exp Cell Res 60: 437-444.
21. Claesson-Welsh L (1994) Signal transduction by the PDGF receptors. Prog Growth Factor Res 5: 37-54.
22. Araki N, Johnson MT, Swanson JA (1996) A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 135: 1249-1260. (Pubitemid 27014597)
23. Araki N, Egami Y, Watanabe Y, Hatae T (2007) Phosphoinositide metabolism during membrane ruffling and macropinosome formation in EGF-stimulated A431 cells. Exp Cell Res 313: 1496-1507. (Pubitemid 46507455)
24. Ridley AJ (2011) Life at the leading edge. Cell 145: 1012-1022.
25. Kurisu S, Takenawa T (2009) The WASP and WAVE family proteins. Genome Biol 10: 226.
26. Oda A, Eto K (2013) WASPs and WAVEs: From molecular function to physiology in hematopoietic cells. Semin Cell Dev Biol 24: 308-313.
27. Maekawa M, Terasaka S, Mochizuki Y, Kawai K, Ikeda Y, et al. (2014) Sequential breakdown of 3-phosphorylated phosphoinositides is essential for the completion of macropinocytosis. Proc Natl Acad Sci U S A 111: doi: 10.1073/pnas.1311029111.
28. Goc A, Abdalla M, Al-Azayzih A, Somanath PR (2012) Rac1 activation driven by 14-3-3zeta dimerization promotes prostate cancer cell-matrix interactions, motility and transendothelial migration. PLoS One 7: e40594.
29. Qin J, Xie Y, Wang B, Hoshino M, Wolff DW, et al. (2009) Upregulation of PIP3-dependent Rac exchanger 1 (P-Rex1) promotes prostate cancer metastasis. Oncogene 28: 1853-1863.
30. Lin KT, Gong J, Li CF, Jang TH, Chen WL, et al. (2012) Vav3-Rac1 signaling regulates prostate cancer metastasis with elevated Vav3 expression correlating with prostate cancer progression and posttreatment recurrence. Cancer Res 72: 3000-3009.
31. Kobayashi T, Inoue T, Shimizu Y, Terada N, Maeno A, et al. (2010) Activation of Rac1 is closely related to androgen-independent cell proliferation of prostate cancer cells both in vitro and in vivo. Mol Endocrinol 24: 722-734.
32. Frankenberry KA, Somasundar P, McFadden DW, Vona-Davis LC (2004) Leptin induces cell migration and the expression of growth factors in human prostate cancer cells. Am J Surg 188: 560-565. (Pubitemid 39491105)
33. Monet M, Gkika D, Lehen'kyi V, Pourtier A, Vanden Abeele F, et al. (2009) Lysophospholipids stimulate prostate cancer cell migration via TRPV2 channel activation. Biochim Biophys Acta 1793: 528-539.
34. Yu HM, Frank DE, Zhang J, You X, Carter WG, et al. (2004) Basal prostate epithelial cells stimulate the migration of prostate cancer cells. Mol Carcinog 41: 85-97. (Pubitemid 39336758)