Extracting Diffusive States of Rho GTPase in Live Cells: Towards In Vivo Biochemistry

PLoS Computational Biology

Volumn 11, Issue 10, 2015, Pages

  Koo, Peter K ^a   Weitzman, Matthew ^b   Sabanaygam, Chandran R ^b   van Golen, Kenneth L ^b   Mochrie, Simon G J ^a,b  

^a Yale University   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; LEARNING SYSTEMS; MAXIMUM PRINCIPLE; PROTEINS;

ACTIVATION STATE; BIOCHEMICAL INTERACTIONS; CLASSIFICATION METHODOLOGIES; DIFFUSIVE BEHAVIOR; EXPECTATION MAXIMIZATION; IN-VIVO; LIVE CELL; MACHINE-LEARNING; RHO GTPASES; SHORT TRAJECTORIES;

TRAJECTORIES;

RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOC GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOCHEMISTRY; CELL TRACKING; CELLS; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; COMPUTER MODEL; COMPUTER SIMULATION; CONTROLLED STUDY; DIFFUSION; ENZYME ACTIVATION; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; IN VIVO STUDY; LIVE CELL; MACHINE LEARNING; MICROSCOPY; PERTURBATION EXPECTATION MAXIMIZATION; PHOTO ACTIVATED LOCALIZATION MICROSCOPY; PROTEIN ANALYSIS; PROTEIN DIFFUSIVE STATE; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SINGLE CELL ANALYSIS; VALIDATION STUDY; BIOLOGICAL MODEL; CELL FRACTIONATION; CHEMICAL MODEL; CHEMISTRY; MOLECULAR IMAGING; PROCEDURES; STATISTICAL MODEL;

COMPUTER SIMULATION; DIFFUSION; MACHINE LEARNING; MODELS, BIOLOGICAL; MODELS, CHEMICAL; MODELS, STATISTICAL; MOLECULAR IMAGING; RHO GTP-BINDING PROTEINS; SUBCELLULAR FRACTIONS;

EID: 84946057629     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004297     Document Type: Article

References (66)

1. Burridge K, Wennerberg K, (2004) Rho and Rac take center stage. Cell 116: 167–179. doi: 10.1016/S0092-8674(04)00003-0 14744429
2. Hall A, Paterson HF, Adamson P, Ridley AJ, (1993) Cellular responses regulate by Rho-related small GTP-binding proteins. Philosophical Transactions of the Royal Society of London Series B:Biological Sciences 340: 267–271. doi: 10.1098/rstb.1993.0067 8103928
3. Jaffe AB, Hall A, (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21: 247–269. doi: 10.1146/annurev.cellbio.21.020604.150721 16212495
4. Ridley AJ, (2001) Rho GTPases and cell migration. Journal of Cell Science 114: 2713–2722. 11683406
5. Wheeler AP, Ridley AJ, (2004) Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Experimental Cell Research 301: 43–49. doi: 10.1016/j.yexcr.2004.08.012 15501444
6. Parri M, Chiarugi P, (2010) Rac and Rho GTPases in cancer cell motility control. Cell Communication and Signaling 8: 23. doi: 10.1186/1478-811X-8-23 20822528
7. Ho TG, Stultiens A, Dubail J, Lapière CM, Nusgens BV, et al. (2011) RhoGDIα-dependent balance between RhoA and RhoC is a key regulator of cancer cell tumorigenesis. Molecular Biology of the Cell 22: 3263–3275. doi: 10.1091/mbc.E11-01-0020
8. Simpson KJ, Dugan AS, Mercurio AM, (2004) Functional analysis of the contribution of RhoA and RhoC GTPases to invasive breast carcinoma. Cancer Research 64: 8694–8701. doi: 10.1158/0008-5472.CAN-04-2247 15574779
9. Bellovin DI, Simpson KJ, Danilov T, Maynard E, Rimm DL, et al. (2006) Reciprocal regulation of RhoA and RhoC characterizes the EMT and identifies RhoC as a prognostic marker of colon carcinoma. Oncogene 25: 6959–6967. doi: 10.1038/sj.onc.1209682 16715134
10. Kleer CG, Griffith KA, Sabel MS, Gallagher G, van Golen KL, et al. (2005) RhoC-GTPase is a novel tissue biomarker associated with biologically aggressive carcinomas of the breast. Breast Cancer Research and Treatment 93: 101–110. doi: 10.1007/s10549-005-4170-6 16187229
11. Lin M, DiVito MM, Merajver SD, Boyanapalli M, Van Golen KL, (2005) Regulation of pancreatic cancer cell migration and invasion by RhoC GTPase and caveolin-1. Molecular Cancer 4: 21. doi: 10.1186/1476-4598-4-21 15969750
12. Yao H, Dashner E, Van Golen C, Van Golen K, (2005) RhoC GTPase is required for PC-3 prostate cancer cell invasion but not motility. Oncogene 25: 2285–2296. doi: 10.1038/sj.onc.1209260
13. Ridley AJ, (2004) Rho proteins and cancer. Breast Cancer Research and Treatment 84: 13–19. doi: 10.1023/B:BREA.0000018423.47497.c6 14999150
14. Lipshtat A, Jayaraman G, He JC, Iyengar R, (2010) Design of versatile biochemical switches that respond to amplitude, duration, and spatial cues. Proceedings of the National Academy of Sciences 107: 1247–1252. doi: 10.1073/pnas.0908647107
15. Moon SY, Zheng Y, (2003) Rho GTPase-activating proteins in cell regulation. Trends in Cell Biology 13: 13–22. doi: 10.1016/S0962-8924(02)00004-1 12480336
16. Symons M, Settleman J, (2000) Rho family GTPases: more than simple switches. Trends in Cell Biology 10: 415–419. doi: 10.1016/S0962-8924(00)01832-8 10998597
17. Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF, et al. (2008) High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nature Methods 5: 155–157. doi: 10.1038/nmeth.1176 18193054
18. Patterson G, Davidson M, Manley S, Lippincott-Schwartz J, (2010) Superresolution imaging using single-molecule localization. Annual Review of Physical Chemistry 61: 345. doi: 10.1146/annurev.physchem.012809.103444 20055680
19. Savin T, Doyle PS, (2005) Static and dynamic errors in particle tracking microrheology. Biophysical Journal 88: 623–638. doi: 10.1529/biophysj.104.042457 15533928
20. Thompson RE, Larson DR, Webb WW, (2002) Precise nanometer localization analysis for individual fluorescent probes. Biophysical Journal 82: 2775–2783. doi: 10.1016/S0006-3495(02)75618-X 11964263
21. Mortensen KI, Churchman LS, Spudich JA, Flyvbjerg H, (2010) Optimized localization analysis for single-molecule tracking and super-resolution microscopy. Nature Methods 7: 377–381. doi: 10.1038/nmeth.1447 20364147
22. Ritchie K, Shan XY, Kondo J, Iwasawa K, Fujiwara T, et al. (2005) Detection of non-Brownian diffusion in the cell membrane in single molecule tracking. Biophysical Journal 88: 2266–2277. doi: 10.1529/biophysj.104.054106 15613635
23. Daumas F, Destainville N, Millot C, Lopez A, Dean D, et al. (2003) Confined diffusion without fences of a g-protein-coupled receptor as revealed by single particle tracking. Biophysical Journal 84: 356–366. doi: 10.1016/S0006-3495(03)74856-5 12524289
24. Dietrich C, Yang B, Fujiwara T, Kusumi A, Jacobson K, (2002) Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophysical Journal 82: 274–284. doi: 10.1016/S0006-3495(02)75393-9 11751315
25. Rossier O, Octeau V, Sibarita JB, Leduc C, Tessier B, et al. (2012) Integrins β1 and β3 exhibit distinct dynamic nanoscale organizations inside focal adhesions. Nature Cell Biology 14: 1057–1067. doi: 10.1038/ncb2620 23023225
26. Qian H, Sheetz MP, Elson EL, (1991) Single particle tracking analysis of diffusion and flow in two-dimensional systems. Biophysical Journal 60: 910–921. doi: 10.1016/S0006-3495(91)82125-7 1742458
27. Douglass AD, Vale RD, (2005) Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in t cells. Cell 121: 937–950. doi: 10.1016/j.cell.2005.04.009 15960980
28. 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. Biophysical Journal 65: 2021–2040. doi: 10.1016/S0006-3495(93)81253-0 8298032
29. Saxton MJ, Jacobson K, (1997) Single-particle tracking: applications to membrane dynamics. Annual Review of Biophysics and Biomolecular Structure 26: 373–399. doi: 10.1146/annurev.biophys.26.1.373 9241424
30. Deverall M, Gindl E, Sinner EK, Besir H, Ruehe J, et al. (2005) Membrane lateral mobility obstructed by polymer-tethered lipids studied at the single molecule level. Biophysical Journal 88: 1875–1886. doi: 10.1529/biophysj.104.050559 15613633
31. Gillespie DT, (1996) The mathematics of Brownian motion and Johnson noise. American Journal of Physics 64: 225. doi: 10.1119/1.18210
32. Persson F, Linden M, Unoson C, Elf J, (2013) Extracting intracellular diffusive states and transition rates from single-molecule tracking data. Nature Methods 10:265–269. doi: 10.1038/nmeth.2367 23396281
33. Itô K, (1974) Diffusion Processes. Wiley Online Library.
34. Berglund AJ, (2010) Statistics of camera-based single-particle tracking. Physical Review E 82: 011917. doi: 10.1103/PhysRevE.82.011917
35. Michalet X, Berglund AJ, (2012) Optimal diffusion coefficient estimation in single-particle tracking. Physical Review E 85: 061916. doi: 10.1103/PhysRevE.85.061916
36. Bishop CM, Nasrabadi NM, (2006) Pattern recognition and machine learning, volume 1. Springer New York.
37. Dempster AP, Laird NM, Rubin DB, (1977) Maximum likelihood from incomplete data via the EM algorithm. Journal of the Royal Statistical Society Series B (Methodological): 1–38.
38. Ueda N, Nakano R, (1998) Deterministic annealing em algorithm. Neural Networks 11: 271–282. doi: 10.1016/S0893-6080(97)00133-0 12662837
39. Murphy KP, (2012) Machine learning: a probabilistic perspective. The MIT Press.
40. Crocker JC, Grier DG, (1996) Methods of digital video microscopy for colloidal studies. Journal of Colloid and Interface Science 179: 298–310. doi: 10.1006/jcis.1996.0217
41. Das R, Cairo CW, Coombs D, (2009) A hidden Markov model for single particle tracks quantifies dynamic interactions between LFA-1 and the actin cytoskeleton. PLoS Computational Biology 5: e1000556. doi: 10.1371/journal.pcbi.1000556 19893741
42. Ott M, Shai Y, Haran G, (2013) Single-particle tracking reveals switching of the hiv fusion peptide between two diffusive modes in membranes. The Journal of Physical Chemistry B 117: 13308–13321. doi: 10.1021/jp4039418 23915358
43. Tait L, Soule HD, Russo J, (1990) Ultrastructural and immunocytochemical characterization of an immortalized human breast epithelial cell line, mcf-10. Cancer Research 50: 6087–6094. 1697506
44. Garrett MD, Self AJ, van Oers C, Hall A, (1989) Identification of distinct cytoplasmic targets for Ras/r-Ras and Rho regulatory proteins. Journal of Biological Chemistry 264: 10–13. 2491843
45. Ridley AJ, Hall A, (1992) The small GTP-binding protein Rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70: 389–399. doi: 10.1016/0092-8674(92)90163-7 1643657
46. Lin R, Cerione RA, Manor D, (1999) Specific contributions of the small GTPases Rho, Rac, and Cdc42 to DBL transformation. Journal of Biological Chemistry 274: 23633–23641. doi: 10.1074/jbc.274.33.23633 10438546
47. Miyazaki K, Yano T, Schmidt DJ, Tokui T, Shibata M, et al. (2002) Rho-dependent agonist-induced spatio-temporal change in myosin phosphorylation in smooth muscle cells. Journal of Biological Chemistry 277: 725–734. doi: 10.1074/jbc.M108568200 11673466
48. Feig LA, Cooper GM, (1988) Relationship among guanine nucleotide exchange, GTP hydrolysis, and transforming potential of mutated Ras proteins. Molecular and cellular biology 8: 2472–2478. doi: 10.1128/MCB.8.6.2472 3043178
49. Vestergaard CL, Blainey PC, Flyvbjerg H, (2014) Optimal estimation of diffusion coefficients from single-particle trajectories. Physical Review E 89: 022726. doi: 10.1103/PhysRevE.89.022726
50. Michaelson D, Silletti J, Murphy G, D’Eustachio P, Rush M, et al. (2001) Differential localization of Rho GTPases in live cells regulation by hypervariable regions and RhoGDI binding. The Journal of Cell Biology 152: 111–126. doi: 10.1083/jcb.152.1.111 11149925
51. van Hennik PB, ten Klooster JP, Halstead JR, Voermans C, Anthony EC, et al. (2003) The C-terminal domain of Rac1 contains two motifs that control targeting and signaling specificity. Journal of Biological Chemistry 278: 39166–39175. doi: 10.1074/jbc.M307001200 12874273
52. Dovas A, , Couchman Jx (2005) RhoGDI: multiple functions in the regulation of Rho family GTPase activities. Biochem J 390: 1–9. doi: 10.1042/BJ20050104 16083425
53. Lang P, Gesbert F, Delespine-Carmagnat M, Stancou R, Pouchelet M, et al. (1996) Protein kinase a phosphorylation of RhoA mediates the morphological and functional effects of cyclic amp in cytotoxic lymphocytes. The EMBO Journal 15: 510. 8599934
54. Burgers PP, Ma Y, Margarucci L, Mackey M, van der Heyden MA, et al. (2012) A small novel A-kinase anchoring protein (AKAP) that localizes specifically protein kinase A-regulatory subunit i (PKA-RI) to the plasma membrane. Journal of Biological Chemistry 287: 43789–43797. doi: 10.1074/jbc.M112.395970 23115245
55. Carragher NO, Frame MC, (2004) Focal adhesion and actin dynamics: a place where kinases and proteases meet to promote invasion. Trends in Cell Biology 14: 241–249. doi: 10.1016/j.tcb.2004.03.011 15130580
56. Hotchin NA, Hall A, (1995) The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular Rho/Rac GTPases. The Journal of Cell Biology 131: 1857–1865. doi: 10.1083/jcb.131.6.1857 8557752
57. Schwartz MA, Shattil SJ, (2000) Signaling networks linking integrins and Rho family GTPases. Trends in biochemical sciences 25: 388–391. doi: 10.1016/S0968-0004(00)01605-4 10916159
58. Van Golen KL, Wu ZF, Qiao XT, Bao LW, Merajver SD, (2000) RhoC GTPase, a novel transforming oncogene for human mammary epithelial cells that partially recapitulates the inflammatory breast cancer phenotype. Cancer Research 60: 5832–5838. 11059780
59. Liu M, Horowitz A, (2006) A PDZ-binding motif as a critical determinant of Rho guanine exchange factor function and cell phenotype. Molecular Biology of the Cell 17: 1880–1887. doi: 10.1091/mbc.E06-01-0002 16467373
60. García-Mata R, Burridge K, (2007) Catching a GEF by its tail. Trends in Cell Biology 17: 36–43. doi: 10.1016/j.tcb.2006.11.004 17126549
61. Medina F, Carter AM, Dada O, Gutowski S, Hadas J, et al. (2013) Activated RhoA is a positive feedback regulator of the LBC family of rho guanine nucleotide exchange factor proteins. Journal of Biological Chemistry 288: 11325–11333. doi: 10.1074/jbc.M113.450056 23493395
62. Kitzing TM, Sahadevan AS, Brandt DT, Knieling H, Hannemann S, et al. (2007) Positive feedback between Dia1, LARG, and RhoA regulates cell morphology and invasion. Genes & Development 21: 1478–1483. doi: 10.1101/gad.424807
63. Yang HW, Shin MG, Lee S, Kim JR, Park WS, et al. (2012) Cooperative activation of Pi3K by Ras and Rho family small GTPases. Molecular Cell 47: 281–290. doi: 10.1016/j.molcel.2012.05.007 22683270
64. Mammoto A, Huang S, Moore K, Oh P, Ingber DE, (2004) Role of RhoA, mDia, and ROCK in cell shape-dependent control of the Skp2-p27kip1 pathway and the G1/S transition. Journal of Biological Chemistry 279: 26323–26330. doi: 10.1074/jbc.M402725200 15096506
65. Khosravi-Far R, Solski PA, Clark GJ, Kinch MS, Der CJ, (1995) Activation of Rac1, RhoA, and mitogen-activated protein kinases is required for Ras transformation. Molecular and Cellular Biology 15: 6443–6453. 7565796
66. Pertz O, (2010) Spatio-temporal Rho GTPase signaling–where are we now? Journal of Cell Science 123: 1841–1850. doi: 10.1242/jcs.064345 20484664