Emergent Systems Energy Laws for Predicting Myosin Ensemble Processivity

PLoS Computational Biology

Volumn 11, Issue 4, 2015, Pages

  Egan, Paul ^a   Moore, Jeffrey ^b   Schunn, Christian ^c   Cagan, Jonathan ^a   LeDuc, Philip ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b University of Massachusetts Lowell   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENERGY UTILIZATION; INDIUM COMPOUNDS; PROTEINS; STOCHASTIC SYSTEMS;

COMPONENT CONFIGURATIONS; COMPONENT SYSTEMS; ENERGY LAWS; EXPERIMENTAL EVIDENCE; IS-ENABLED; MECHANOCHEMICALS; PROCESSIVITY; STOCHASTIC COMPONENT; SYSTEM ENERGY; SYSTEM ENERGY CONSUMPTION;

FORECASTING;

ACTIN; MYOSIN; ISOPROTEIN;

ACTIN FILAMENT; ANALYTIC METHOD; ARTICLE; CHEMICAL STRUCTURE; CONTROLLED STUDY; EMERGENT SYSTEMS ENRGY LAWS; ENERGY CONSUMPTION; NONHUMAN; PREDICTION; PROBABILITY; PROTEIN PROTEIN INTERACTION; SIMULATION; STOCHASTIC MODEL; BIOLOGY; BIOMECHANICS; CHEMISTRY; COMPUTER SIMULATION; MARKOV CHAIN; METABOLISM; MOLECULAR MODEL; REPRODUCIBILITY;

BIOMECHANICAL PHENOMENA; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; MODELS, MOLECULAR; MYOSINS; PROTEIN ISOFORMS; REPRODUCIBILITY OF RESULTS; STOCHASTIC PROCESSES;

EID: 84929497887     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004177     Document Type: Article

References (40)

1. Albert-laszlo B, Albert R., (1999) Emergence of scaling in random networks. Science 285: 509–512.
2. Bhalla U, Iyengar R., (1999) Emergent properties of networks of biological signaling pathways. Science 283: 381–387. 9888852
3. van Oers RF, Merks RM (2013) Mechanical cell-substrate feedback explains pairwise and collective endothelial cell behavior in vitro. arXiv preprint arXiv:13083721.
4. Erickson RP, Jia Z, Gross SP, Clare CY, (2011) How molecular motors are arranged on a cargo is important for vesicular transport. PLoS computational biology 7: e1002032. doi: 10.1371/journal.pcbi.1002032 21573204
5. Campbell K, (2009) Interactions between connected half-sarcomeres produce emergent mechanical behavior in a mathematical model of muscle. PLoS Computational Biology 5.
6. Leibler SaDAH, (1993) Porters versus rowers: a unified stochastic model of motor proteins. The Journal of Cell Biology 121: 1357–1368. 8509455
7. Erdmann T, Schwarz U., (2012) Stochastic force generation by small ensembles of myosin II motors. Physical Review Letters 108: 188101. 22681120
8. Jülicher F, Ajdari A, Prost J, (1997) Modeling molecular motors. Reviews of Modern Physics 69: 1269.
9. LeDuc PR, Robert M, Bellin (2006) Nanoscale intracellular organization and functional architecture mediating cellular behavior. Annals of Biomedical Engineering 34: 102–113. 16456640
10. Resnicow DI, Deacon J. C., Warrick H. M., Spudich J. A., Leinwand L. A., (2010) Functional diversity among a family of human skeletal muscle myosin motors. PNAS 107: 1053–1058. doi: 10.1073/pnas.0913527107 20080549
11. Piazzesi G, et al. (2007) Skeletal muscle performance determined by modulation of number of myosin motors rather than motor force or stroke size. Cell 131: 784–795. 18022371
12. Van den Heuval M, Dekker C., (2007) Motor proteins at work for nanotechnology. Science 317: 333–336. 17641191
13. Scarabelli G, Grant B, (2014) Mapping the structural and dynamical features of kinesin motor domains. PLoS computational biology 9: e1003329. doi: 10.1371/journal.pcbi.1003329 24244137
14. Uyeda T, Abramson P., Spudich J., (1996) The neck region of the myosin motor domain acts as a lever arm to generate movement. PNAS 93: 4459–4464. 8633089
15. Egan P, Cagan J, Schunn C, LeDuc P, (2013) Design of complex biologically based nanoscale systems using multi-agent simulations and structure-behavior-function representations. Journal of Mechanical Design 135: 061005.
16. Moore JR, Leinwand L, Warshaw DM, (2012) Understanding cardiomyopathy phenotypes based on the functional impact of mutations in the myosin motor. Circulation Research 111: 375–385. doi: 10.1161/CIRCRESAHA.110.223842 22821910
17. Agarwal A, Hess H., (2010) Biomolecular motors at the intersection of nanotechnology and polymer science. Prog Polym Sci 25: 252–277.
18. Egan P, Cagan J, Schunn C, LeDuc P, (2015) Synergistic human-agent methods for deriving effective search strategies: The case of nanoscale design. Research in Engineering Design 26(2): 145–169.
19. Harada Y, Sakurada K, Aoki T, Thomas DD, Yanagida T, (1990) Mechanochemical coupling in actomyosin energy transduction studied by in vitro movement assay. Journal of Molecular Biology 216: 49–68. 2146398
20. Korten T, Mansson A., Diez S., (2010) Towards the application of cytoskeletal motor proteins in molecular detection and diagnostic devices. Current Opinion in Biotechnology 21: 477–488. doi: 10.1016/j.copbio.2010.05.001 20860918
21. Greenberg MJ, Kazmierczak K, Szczesna-Cordary D, Moore JR, (2010) Cardiomyopathy-linked myosin regulatory light chain mutations disrupt myosin strain-dependent biochemistry. Proceedings of the National Academy of Sciences 107: 17403–17408. doi: 10.1073/pnas.1009619107 20855589
22. Craig E, Linke H., (2009) Mechanochemical model for myosin V. PNAS 106: 18261–18266. doi: 10.1073/pnas.0908192106 19822760
23. Cooke R, White H., Pate E., (1994) A model of the release of myosin heads from actin in rapidly contracting muscle fibers. Biophysical Journal 66: 778–788. 8011910
24. Chin L, Yue P., Feng J. J., Seow C. Y., (2006) Mathematical simulation of muscle cross-bridge cycle and force-velocity relationship. Biophysical Journal 91: 3653–3663. 16935957
25. Ishijima A, Kojima H., Higuchi H., Harada Y., Funatsue T., Yanagida T., (1996) Multiple- and single-molecules analysis of the actomyosin motor by nanometer-piconewton manipulation with a microneedle: Unitary steps and forces. Biophysical Journal 70: 383–400. 8770215
26. Baker JE, Brosseau C., Joes P. B., Warshaw D. M., (2002) The biochemical kinetics underlying actin movement generated by one and many skeletal muscle myosin molecules. Biophysics Journal 82: 2134–2147. 11916869
27. Howard J, (2001) Mechanics of Motor Proteins and the Cytoskeleton Sunderland, MA: Sinauer Associates, Inc. 367 p. 11684429
28. Berger F, Keller C., Klumpp S., Lipowsky R., (2012) Distinct transport regimes for two elastically coupled molecular motors. Physical Review Letters 108: 208101. 23003191
29. Toyoshima Y, Kron S., Spudich J., (1990) The myosin step size: Measurement of the unit displacement per ATP hydrolyzed in an in vitro assay. PNAS 87: 7130–7134. 2144900
30. Sneddon M, Faeder J. R., Emonet T., (2011) Efficient modeling, simulation and coarse-graining of biological complexity with NFsim. Nature Methods 8: 177–185. doi: 10.1038/nmeth.1546 21186362
31. Hanna L, Cagan J., (2009) Evolutionary Multi-Agent Systems: An Adaptive and Dynamic Approach to Optimization. Journal of Mechanical Design 131: 011010-011011-011010-011018.
32. Redaelli A, Soncini M., Montevecchi F. M., (2001) Myosin cross-bridge mechanics: geometrical determinants for continuous sliding. Journal of Biomechanics 34: 1607–1617. 11716863
33. Weiss S, Rossi R., Pellegrino M., Bottinelli R., Geeves M. A., (2001) Differing ADP release rates from mosin heavy chain isoforms define the shortening velocity of skeletal muscle fibers. The Journal of Biological Chemistry 276: 45902–45908. 11590173
34. Harris DE, Work S. S., Wright R. K., Alpert N. R., Warshaw D. M., (1994) Smooth, cardiac and skeletal muscle myosin force and motion generation assessed by cross-bridge mechanical interactions in vitro. Journal of Muscle Research and Cell Motility 15: 11–19. 8182105
35. Ruff C, Fuch M., Brenner B., Manstein D. J., Meyhoefer E., (2001) Single-molecule tracking of myosins with genetically engineered amplifier domains. Nature Structural Biology 8: 226–229. 11224566
36. Hodges AR, Krementsova E. B., Trybus K. M., (2007) Engineering the processive run length of myosin V. The Journal of Biological Chemistry 282: 27192–27197. 17640878
37. Murphy CT, Spudich J. A., (1998) Dictyostelium myosin 25–50K loop substitutions specifically affect ADP release rates. Biochemistry 37: 6738–6744. 9578557
38. Ito K, Ikebe M., Kashiyama T., Mogami T., Kon T., Yamamoto K., (2007) Kinetic mechanism of the fastest motor protein, Chara myosin. Journal of Biological Chemistry 282: 19534–19545. 17488711
39. Uyeda T, Kron S, Spudich J, (1990) Myosin step size estimation from slow sliding movement of actin over low densities of heavy meromyosin. J Mol Biol 214: 699–710. 2143785
40. Alvarado J, Sheinman M, Sharma A, MacKintosh FC, Koenderink GH, (2013) Molecular motors robustly drive active gels to a critically connected state. Nature Physics 9: 591–597.