Chimaerin Suppresses Rac1 Activation at the Apical Membrane to Maintain the Cyst Structure

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Yagi, Shunsuke ^a   Matsuda, Michiyuki ^a   Kiyokawa, Etsuko ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIN; RAC1 PROTEIN; SCATTER FACTOR;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASEMENT MEMBRANE; BIOACCUMULATION; CELL STRUCTURE; CONTROLLED STUDY; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION;

ANIMALS; CELL LINE; CHIMERIN 1; CHIMERIN PROTEINS; DOGS; HEPATOCYTE GROWTH FACTOR; MICROSCOPY, CONFOCAL; POLYMERASE CHAIN REACTION; RAC1 GTP-BINDING PROTEIN;

EID: 84871437716     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052258     Document Type: Article

References (38)

1. O'Brien LE, Zegers MM, Mostov KE, (2002) Opinion: Building epithelial architecture: insights from three-dimensional culture models. Nat Rev Mol Cell Biol 3: 531-537.
2. Yagi S, Matsuda M, Kiyokawa E, (2012) Suppression of Rac1 activity at the apical membrane of MDCK cells is essential for cyst structure maintenance. EMBO Rep 13: 237-243.
3. Kiyokawa E, Aoki K, Nakamura T, Matsuda M, (2010) Spatiotemporal regulation of small GTPases as revealed by probes based on the principle of Förster Resonance Energy Transfer (FRET): Implications for signaling and pharmacology. Annu Rev Pharmacol Toxicol 51: 337-358.
4. Rossman KL, Der CJ, Sondek J, (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 6: 167-180.
5. Vigil D, Cherfils J, Rossman KL, Der CJ, (2010) Ras superfamily GEFs and GAPs: validated and tractable targets for cancer therapy? Nat Rev Cancer 10: 842-857.
6. Tcherkezian J, Lamarche-Vane N, (2007) Current knowledge of the large RhoGAP family of proteins. Biol Cell 99: 67-86.
7. Schmidt A, Hall A, (2002) Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev 16: 1587-1609.
8. Rodriguez-Fraticelli AE, Vergarajauregui S, Eastburn DJ, Datta A, Alonso MA, et al. (2010) The Cdc42 GEF Intersectin 2 controls mitotic spindle orientation to form the lumen during epithelial morphogenesis. J Cell Biol 189: 725-738.
9. Qin Y, Meisen WH, Hao Y, Macara IG, (2010) Tuba, a Cdc42 GEF, is required for polarized spindle orientation during epithelial cyst formation. J Cell Biol 189: 661-669.
10. Itoh RE, Kurokawa K, Ohba Y, Yoshizaki H, Mochizuki N, et al. (2002) Activation of rac and cdc42 video imaged by fluorescent resonance energy transfer-based single-molecule probes in the membrane of living cells. Mol Cell Biol 22: 6582-6591.
11. Nishioka T, Aoki K, Hikake K, Yoshizaki H, Kiyokawa E, et al. (2008) Rapid Turnover Rate of Phosphoinositides at the Front of Migrating MDCK Cells. Mol Biol Cell 19: 4213-4223.
12. Aoki K, Nakamura T, Inoue T, Meyer T, Matsuda M, (2007) An essential role for the SHIP2-dependent negative feedback loop in neuritogenesis of nerve growth factor-stimulated PC12 cells. J Cell Biol 177: 817-827.
13. Montesano R, Matsumoto K, Nakamura T, Orci L, (1991) Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell 67: 901-908.
14. Yoshizaki H, Mochizuki N, Gotoh Y, Matsuda M, (2007) Akt-PDK1 Complex Mediates Epidermal Growth Factor-induced Membrane Protrusion through Ral Activation. Mol Biol Cell 18: 119-128.
15. Aoki K, Nakamura T, Fujikawa K, Matsuda M, (2005) Local Phosphatidylinositol 3,4,5-Trisphosphate Accumulation Recruits Vav2 and Vav3 to Activate Rac1/Cdc42 and Initiate Neurite Outgrowth in Nerve Growth Factor-stimulated PC12 Cells. Mol Biol Cell 16: 2207-2217.
16. Kumagai Y, Kamioka Y, Yagi S, Matsuda M, Kiyokawa E, (2011) A genetically encoded Forster resonance energy transfer biosensor for two-photon excitation microscopy. Anal Biochem 413: 192-199.
17. Martin-Belmonte F, Gassama A, Datta A, Yu W, Rescher U, Gerke V, et al. (2007) PTEN-Mediated Apical Segregation of Phosphoinositides Controls Epithelial Morphogenesis through Cdc42. Cell 128: 383-397.
18. Farmer P, Bonnefoi H, Anderle P, Cameron D, Wirapati P, et al. (2009) A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer. Nat Med 15: 68-74.
19. Hall C, Monfries C, Smith P, Lim HH, Kozma R, et al. (1990) Novel human brain cDNA encoding a 34,000 Mr protein n-chimaerin, related to both the regulatory domain of protein kinase C and BCR, the product of the breakpoint cluster region gene. J Mol Biol 211: 11-16.
20. Hall C, Michael GJ, Cann N, Ferrari G, Teo M, et al. (2001) alpha2-chimaerin, a Cdc42/Rac1 regulator, is selectively expressed in the rat embryonic nervous system and is involved in neuritogenesis in N1E-115 neuroblastoma cells. J Neurosci 21: 5191-5202.
21. Yang C, Kazanietz MG, (2007) Chimaerins: GAPs that bridge diacylglycerol signalling and the small G-protein Rac. Biochem J 403: 1-12.
22. Caloca MJ, Garcia-Bermejo ML, Blumberg PM, Lewin NE, Kremmer E, et al. (1999) beta2-chimaerin is a novel target for diacylglycerol: binding properties and changes in subcellular localization mediated by ligand binding to its C1 domain. Proc Natl Acad Sci U S A 96: 11854-11859.
23. Kogure T, Karasawa S, Araki T, Saito K, Kinjo M, et al. (2006) A fluorescent variant of a protein from the stony coral Montipora facilitates dual-color single-laser fluorescence cross-correlation spectroscopy. Nat Biotech 24: 577-581.
24. Hara S, Kiyokawa E, Iemura S, Natsume T, Wassmer T, et al. (2008) The DHR1 domain of DOCK180 binds to SNX5 and regulates cation-independent mannose 6-phosphate receptor transport. Mol Biol Cell 19: 3823-3835.
25. Sakurai A, Matsuda M, Kiyokawa E, (2012) Activated Ras protein accelerates cell cycle progression to perturb MDCK cystogenesis. J Biol Chem 287: 31703-31711.
26. Hall C, Sin WC, Teo M, Michael GJ, Smith P, et al. (1993) Alpha 2-chimerin, an SH2-containing GTPase-activating protein for the ras-related protein p21rac derived by alternate splicing of the human n-chimerin gene, is selectively expressed in brain regions and testes. Mol Cell Biol 13: 4986-4998.
27. Iwasato T, Katoh H, Nishimaru H, Ishikawa Y, Inoue H, et al. (2007) Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell 130: 742-753.
28. Leung T, How BE, Manser E, Lim L, (1993) Germ cell beta-chimaerin, a new GTPase-activating protein for p21rac, is specifically expressed during the acrosomal assembly stage in rat testis. J Biol Chem 268: 3813-3816.
29. Leung T, How BE, Manser E, Lim L, (1994) Cerebellar beta 2-chimaerin, a GTPase-activating protein for p21 ras-related rac is specifically expressed in granule cells and has a unique N-terminal SH2 domain. J Biol Chem 269: 12888-12892.
30. Riccomagno MM, Hurtado A, Wang H, Macopson JG, Griner EM, et al. (2012) The RacGAP β2-Chimaerin Selectively Mediates Axonal Pruning in the Hippocampus. Cell 149: 1594-1606.
31. Yang C, Liu Y, Leskow FC, Weaver VM, Kazanietz MG, (2005) Rac-GAP-dependent inhibition of breast cancer cell proliferation by β2-chimerin. J Biol Chem 280: 24363-24370.
32. Ohta Y, Hartwig JH, Stossel TP, (2006) FilGAP, a Rho- and ROCK-regulated GAP for Rac binds filamin A to control actin remodelling. Nat Cell Biol 8: 803-814.
33. Kozma R, Ahmed S, Best A, Lim L, (1996) The GTPase-activating protein n-chimaerin cooperates with Rac1 and Cdc42Hs to induce the formation of lamellipodia and filopodia. Mol Cell Biol 16: 5069-5080.
34. Caloca MJ, Wang H, Kazanietz MG, (2003) Characterization of the Rac-GAP (Rac-GTPase-activating protein) activity of beta2-chimaerin, a 'non-protein kinase C' phorbol ester receptor. Biochem J 375: 313-321.
35. Burbelo PD, Miyamoto S, Utani A, Brill S, Yamada KM, et al. (1995) p190-B, a New Member of the Rho GAP Family, and Rho Are Induced to Cluster after Integrin Cross-linking. J Biol Chem 270: 30919-30926.
36. Charrier C, Joshi K, Coutinho-Budd J, Kim JE, Lambert N, et al. (2012) Inhibition of SRGAP2 Function by Its Human-Specific Paralogs Induces Neoteny during Spine Maturation. Cell 149: 923-935.
37. Saras J, Franzen P, Aspenstrom P, Hellman U, Gonez LJ, et al. (1997) A Novel GTPase-activating Protein for Rho Interacts with a PDZ Domain of the Protein-tyrosine Phosphatase PTPL1. J Biol Chem 272: 24333-24338.
38. Wong K, Ren XR, Huang YZ, Xie Y, Liu G, et al. (2001) Signal Transduction in Neuronal Migration: Roles of GTPase Activating Proteins and the Small GTPase Cdc42 in the Slit-Robo Pathway. Cell 107: 209-221.