Asymmetric PTEN Distribution Regulated by Spatial Heterogeneity in Membrane-Binding State Transitions

PLoS Computational Biology

Volumn 9, Issue 1, 2013, Pages

  Matsuoka, Satomi ^a,b,c   Shibata, Tatsuo ^c,d   Ueda, Masahiro ^a,b,c  

^a RIKEN   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

STOCHASTIC MODELS; STOCHASTIC SYSTEMS;

BINDING STATE; LATERAL MOBILITY; MEMBRANE BINDING; MOLECULAR MECHANISM; MOTILE CELLS; SINGLE-MOLECULE TRACKING; SPATIAL HETEROGENEITY; STATE TRANSITIONS; STOCHASTIC STATE TRANSITIONS; TRACKING ANALYSIS;

MEMBRANES;

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ARTICLE; CELL POLARITY; DICTYOSTELIUM DISCOIDEUM; DIFFUSION COEFFICIENT; ENZYME LOCALIZATION; MATHEMATICAL MODEL; MEMBRANE BINDING; NONHUMAN; PROTEIN DEPLETION; QUANTITATIVE ANALYSIS;

EID: 84873507046     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002862     Document Type: Article

References (39)

1. Denhardt DT, (1996) Signal-transducing protein phosphorylation cascades mediated by Ras/Rho proteins in the mammalian cell: the potential for multiplex signaling. Biochem J 318(3): 729-47.
2. Vivanco I, Sawyers CL, (2002) The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2(7): 489-501.
3. Rhee SG, (2001) Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 70: 281-312.
4. Au-Yeung BB, Deindl S, Hsu LY, Palacios EH, Levin SE, et al. (2009) The structure, regulation, and function of ZAP-70. Immunol Rev 228(1): 41-57.
5. Shattil SJ, Kim C, Ginsberg MH, (2010) The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol 11(4): 288-300.
6. Swaney KF, Huang CH, Devreotes PN, (2010) Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu Rev Biophys 39: 265-89.
7. Sako Y, Minoghchi S, Yanagida T, (2000) Single-molecule imaging of EGFR signalling on the surface of living cells. Nat Cell Biol 2(3): 168-72.
8. Ueda M, Sako Y, Tanaka T, Devreotes P, Yanagida T, (2001) Single-molecule analysis of chemotactic signaling in Dictyostelium cells. Science 294(5543): 864-7.
9. Matsuoka S, Iijima M, Watanabe TM, Kuwayama H, Yanagida T, et al. (2006) Single-molecule analysis of chemoattractant-stimulated membrane recruitment of a PH-domain-containing protein. J Cell Sci 119: 1071-1079.
10. Hibino K, Shibata T, Yanagida T, Sako Y, (2011) Activation kinetics of RAF protein in the ternary complex of RAF, RAS-GTP, and kinase on the plasma membrane of living cells: single-molecule imaging analysis. J Biol Chem 286(42): 36460-8.
11. Qian H, Sheetz MP, Elson EL, (1991) Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys J 60(4): 910-21.
12. Kusumi A, Sako Y, Yamamoto M, (1993) Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys J 65(5): 2021-40.
13. Matsuoka S, Shibata T, Ueda M, (2009) Statistical analysis of lateral diffusion and multistate kinetics in single-molecule imaging. Biophys J 97(4): 1115-24.
14. Low-Nam ST, Lidke KA, Cutler PJ, Roovers RC, van Bergen en Henegouwen PM, et al. (2011) ErbB1 dimerization is promoted by domain co-confinement and stabilized by ligand binding. Nat Struct Mol Biol 18(11): 1244-9.
15. Sakmann B and Neher E. (1995). Single Channel Recording. New York: Plenum Press.
16. Miyanaga Y, Matsuoka S, Ueda M, (2009) Single-molecule imaging techniques to visualize chemotactic signaling events on the membrane of living Dictyostelium cells. Chemotaxis. (eds. D. Hereld and T. Jin) Methods in Molecular Biology 571: 417-435.
17. Sansal I, Sellers WR, (2004) The biology and clinical relevance of the PTEN tumor suppressor pathway. J Clin Oncol 22(14): 2954-63.
18. Parent CA, Blacklock BJ, Froehlich WM, Murphy DB, Devreotes PN, (1998) G protein signaling events are activated at the leading edge of chemotactic cells. Cell 95(1): 81-91.
19. Iijima M, Devreotes P, (2002) Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 109: 599-610.
20. Janetopoulos C, Ma L, Devreotes PN, Iglesias PA, (2004) Chemoattractant-induced phosphatidylinositol 3,4,5-trisphosphate accumulation is spatially amplified and adapts, independent of the actin cytoskeleton. Proc Natl Acad Sci U S A 101(24): 8951-6.
21. Postma M, Roelofs J, Goedhart J, Loovers HM, Visser AJ, Van Haastert PJ, (2004) Sensitization of Dictyostelium chemotaxis by phosphoinositide-3-kinase-mediated self-organizing signalling patches. J Cell Sci 117(14): 2925-35.
22. Arai Y, Shibata T, Matsuoka S, Sato MJ, Yanagida T, et al. (2010) Self-organization of the phosphatidylinositol lipids signaling system for random cell migration. Proc Natl Acad Sci U S A 107(27): 12399-12404.
23. Bosgraaf L, Van Haastert PJ, (2009) Navigation of chemotactic cells by parallel signaling to pseudopod persistence and orientation. PLoS One 4(8): e6842.
24. Gamba A, de Candia A, Di Talia S, Coniglio A, Bussolino F, et al. (2005) Diffusion-limited phase separation in eukaryotic chemotaxis. Proc Natl Acad Sci U S A 102(47): 16927-32.
25. Ma L, Janetopoulos C, Yang L, Devreotes PN, Iglesias PA, (2004) Two complementary, local excitation, global inhibition mechanisms acting in parallel can explain the chemoattractant-induced regulation of PI(3,4,5)P3 response in dictyostelium cells. Biophys J 87(6): 3764-74.
26. Krishnan J, Iglesias PA, A modelling framework describing the enzyme regulation of membrane lipids underlying gradient perception in Dictyostelium cells II: input-output analysis. J Theor Biol 235(4): 504-20.
27. Lee J, Yang H, Georgescu M, Cristofano A, Maehama T, et al. (1999) Crystal structure of the PTEN tumor suppressor: Implications for its phosphoinositide phosphatase activity and membrane association. Cell 99: 323-334.
28. Iijima M, Huang YE, Luo H, Vazquez F, Devreotes P, (2004) Novel mechanism of PTEN regulation by its phosphatidylinositol 4,5-bisphosphate binding motif is critical for chemotaxis. J Biol Chem 279: 16606-16613.
29. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A, (2002) Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 157(6): 1071-81.
30. Akaike H, (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19: 716-723.
31. Vazquez F, Matsuoka S, Sellers WR, Yanagida T, Ueda M, et al. (2006) Tumor suppressor PTEN acts through dynamic interaction with the plasma membrane. Proc Natl Acad Sci U S A 103: 3633-3638.
32. Redfern RE, Redfern D, Furgason ML, Munson M, Ross AH, et al. (2008) PTEN phosphatase selectively binds phosphoinositides and undergoes structural changes. Biochemistry 47(7): 2162-71.
33. Kamimura Y, Tang M, Devreotes P, (2009) Assays for chemotaxis and chemoattractant-stimulated TorC2 activation and PKB substrate phosphorylation in Dictyostelium. Methods Mol Biol 571: 255-70.
34. Miyanaga Y, Ueda M. (2010). Single-Molecule Kinetic Analysis of Stochastic Signal Transduction Mediated by G-protein Coupled Chemoattractant Receptors. In: Sako Y, Ueda M, editors. Cell Signaling Reactions: Single-Molecule Kinetic Analysis. Dordrecht Heidelberg London New York: Springer. pp. 33-57.
35. Saxton MJ, Jacobson K, (1997) Single-particle tracking: Applications to membrane dynamics. Annu Rev Biophys Biomol Struct 26: 373-99.
36. Xu X, Meckel T, Brzostowski JA, Yan J, Meier-Schellersheim M, et al. (2010) Coupling mechanism of a GPCR and a heterotrimeric G protein during chemoattractant gradient sensing in Dictyostelium. Sci Signal 3(141): ra71.
37. Shibata T, Nishikawa M, Matsuoka S, Ueda M, (2012) Modeling the self-organized phosphatidylinositol lipids signaling system in chemotactic cells based on quantitative image analysis. J Cell Sci doi:10.1242/jcs.108373.
38. Matsuoka S, Miyanaga Y, Yanagida T, Ueda M. (2008). Single molecule imaging of stochastic signaling events in living cells. In: Selvin PR, Ha T, editors. Single-Molecule Techniques: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press. pp. 239-258.
39. Fukui Y, Yumura S, Yumura TK, (1987) Agar-overlay immunofluorescence: high-resolution studies of cytoskeletal components and their changes during chemotaxis. Methods Cell Biol 28: 347-356.