A Hidden Markov Model for Single Particle Tracks Quantifies Dynamic Interactions between LFA-1 and the Actin Cytoskeleton

The extraction of hidden information from complex trajectories is a continuing problem in single-particle and single-molecule experiments. Particle trajectories are the result of multiple phenomena, and new methods for revealing changes in molecular processes are needed. We have developed a practical technique that is capable of identifying multiple states of diffusion within experimental trajectories. We model single particle tracks for a membrane-associated protein interacting with a homogeneously distributed binding partner and show that, with certain simplifying assumptions, particle trajectories can be regarded as the outcome of a two-state hidden Markov model. Using simulated trajectories, we demonstrate that this model can be used to identify the key biophysical parameters for such a system, namely the diffusion coefficients of the underlying states, and the rates of transition between them. We use a stochastic optimization scheme to compute maximum likelihood estimates of these parameters. We have applied this analysis to single-particle trajectories of the integrin receptor lymphocyte function-associated antigen-1 (LFA-1) on live T cells. Our analysis reveals that the diffusion of LFA-1 is indeed approximately two-state, and is characterized by large changes in cytoskeletal interactions upon cellular activation.

[1]  K. Jacobson,et al.  Single-particle tracking: applications to membrane dynamics. , 1997, Annual review of biophysics and biomolecular structure.

[2]  M. Saxton,et al.  Lateral diffusion in an archipelago. The effect of mobile obstacles. , 1987, Biophysical journal.

[3]  J. Käs,et al.  Apparent subdiffusion inherent to single particle tracking. , 2002, Biophysical journal.

[4]  J. Neefjes,et al.  From fixed to FRAP: measuring protein mobility and activity in living cells , 2001, Nature Cell Biology.

[5]  Tianquan Jin,et al.  Dynamitin Controls β2 Integrin Avidity by Modulating Cytoskeletal Constraint on Integrin Molecules* , 2002, The Journal of Biological Chemistry.

[6]  Michael Loran Dustin,et al.  Visualization of CD2 interaction with LFA-3 and determination of the two-dimensional dissociation constant for adhesion receptors in a contact area , 1996, The Journal of cell biology.

[7]  A Kusumi,et al.  Cell surface organization by the membrane skeleton. , 1996, Current opinion in cell biology.

[8]  A Kusumi,et al.  Compartmentalized structure of the plasma membrane for receptor movements as revealed by a nanometer-level motion analysis , 1994, The Journal of cell biology.

[9]  M K Cheezum,et al.  Quantitative comparison of algorithms for tracking single fluorescent particles. , 2001, Biophysical journal.

[10]  Biing-Hwang Juang,et al.  Fundamentals of speech recognition , 1993, Prentice Hall signal processing series.

[11]  R. Waugh,et al.  Membrane mobility of beta2 integrins and rolling associated adhesion molecules in resting neutrophils. , 2008, Biophysical journal.

[12]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[13]  D. Golan,et al.  Cytoskeletal regulation couples LFA-1 conformational changes to receptor lateral mobility and clustering. , 2006, Immunity.

[14]  C. le Grimellec,et al.  Single-molecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web , 2008, The Journal of cell biology.

[15]  Michael Loran Dustin,et al.  Mechanisms of Cellular Avidity Regulation in CD2-CD58-Mediated T Cell Adhesion. , 2006, ACS chemical biology.

[16]  Yoji Shimizu,et al.  T‐cell receptor signaling to integrins , 2007, Immunological reviews.

[17]  Ronald D. Vale,et al.  Single-Molecule Microscopy Reveals Plasma Membrane Microdomains Created by Protein-Protein Networks that Exclude or Trap Signaling Molecules in T Cells , 2005, Cell.

[18]  William H. Press,et al.  Numerical Recipes 3rd Edition: The Art of Scientific Computing , 2007 .

[19]  L. Baum,et al.  Statistical Inference for Probabilistic Functions of Finite State Markov Chains , 1966 .

[20]  Maxime Dahan,et al.  Transient directed motions of GABA(A) receptors in growth cones detected by a speed correlation index. , 2007, Biophysical journal.

[21]  Akihiro Kusumi,et al.  Relationship of lipid rafts to transient confinement zones detected by single particle tracking. , 2002, Biophysical journal.

[22]  David Brian Walton,et al.  Analysis of single-molecule kinesin assay data by hidden Markov model filtering , 2002 .

[23]  Anna Huttenlocher,et al.  Calpain-mediated proteolysis of talin regulates adhesion dynamics , 2004, Nature Cell Biology.

[24]  M. Saxton,et al.  Lateral diffusion in an archipelago. Single-particle diffusion. , 1993, Biophysical journal.

[25]  A. Kusumi,et al.  Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. , 1993, Biophysical journal.

[26]  D. Golan,et al.  Single-particle tracking and laser optical tweezers studies of the dynamics of individual protein molecules in membranes of intact human and mouse red cells. , 2001, Blood cells, molecules & diseases.

[27]  R. Simmons,et al.  Hidden-Markov methods for the analysis of single-molecule actomyosin displacement data: the variance-Hidden-Markov method. , 2001, Biophysical journal.

[28]  M. Saxton Single-particle tracking: the distribution of diffusion coefficients. , 1997, Biophysical journal.

[29]  N. Meilhac,et al.  Detection of confinement and jumps in single-molecule membrane trajectories. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[30]  B G de Grooth,et al.  3D single-particle tracking and optical trap measurements on adhesion proteins. , 1999, Cytometry.

[31]  D. Golan,et al.  T cell adhesion mechanisms revealed by receptor lateral mobility. , 2008, Biopolymers.

[32]  Anna Huttenlocher,et al.  Talin1 Regulates TCR-Mediated LFA-1 Function1 , 2006, The Journal of Immunology.

[33]  Alessandra Cambi,et al.  Organization of the integrin LFA-1 in nanoclusters regulates its activity. , 2006, Molecular biology of the cell.

[34]  J. Beausang,et al.  Diffusive hidden Markov model characterization of DNA looping dynamics in tethered particle experiments , 2007, Physical biology.

[35]  Fumio Takei,et al.  Activation of LFA-1 by ionomycin is independent of calpain-mediated talin cleavage. , 2007, Biochemical and biophysical research communications.

[36]  Nicolas Destainville,et al.  Confined diffusion without fences of a g-protein-coupled receptor as revealed by single particle tracking. , 2003, Biophysical journal.

[37]  Joerg Kallen,et al.  Statins selectively inhibit leukocyte function antigen-1 by binding to a novel regulatory integrin site , 2001, Nature Medicine.

[38]  S. Franco,et al.  Talin 1 Regulates TCR-Mediated LFA-1 Function 1 , 2006 .

[39]  K R Wilson,et al.  Lateral diffusion of membrane proteins in the presence of static and dynamic corrals: suggestions for appropriate observables. , 2000, Biophysical journal.

[40]  Lawrence R. Rabiner,et al.  A tutorial on hidden Markov models and selected applications in speech recognition , 1989, Proc. IEEE.

[41]  Sergio Grinstein,et al.  Fcγ-receptors Induce Mac-1 (CD11b/CD18) Mobilization and Accumulation in the Phagocytic Cup for Optimal Phagocytosis* , 2003, Journal of Biological Chemistry.

[42]  M. Saxton,et al.  Single-particle tracking: effects of corrals. , 1995, Biophysical journal.

[43]  E. Stelzer,et al.  Photobleaching GFP reveals protein dynamics inside live cells. , 1999, Trends in cell biology.

[44]  H. Qian,et al.  Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. , 1991, Biophysical journal.

[45]  Josef A. Käs,et al.  Measurement of diffusion in Langmuir monolayers by single-particle tracking , 2004 .

[46]  K. Jacobson,et al.  Detection of temporary lateral confinement of membrane proteins using single-particle tracking analysis. , 1995, Biophysical journal.

[47]  M. Saxton A biological interpretation of transient anomalous subdiffusion. II. Reaction kinetics. , 2008, Biophysical journal.

[48]  W. Webb,et al.  Precise nanometer localization analysis for individual fluorescent probes. , 2002, Biophysical journal.

[49]  J M Miller,et al.  Adhesion-activating phorbol ester increases the mobility of leukocyte integrin LFA-1 in cultured lymphocytes. , 1996, The Journal of clinical investigation.

[50]  Michael Loran Dustin,et al.  Analysis of two-dimensional dissociation constant of laterally mobile cell adhesion molecules. , 2007, Biophysical journal.