Why Muscle is an Efficient Shock Absorber
Publication Date
January 23, 2014
Journal
PLOS ONE
Authors
Michael A. Ferenczi, Sergey Y. Bershitsky, Natalia A. Koubassova, Galina V. Kopylova, et al
Volume
9
Issue
1
Pages
e85739
DOI
https://dx.plos.org/10.1371/journal.pone.0085739
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0085739
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/24465673
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3900422
Europe PMC
http://europepmc.org/abstract/MED/24465673
Web of Science
000330288000022
Scopus
84899810436
Mendeley
http://www.mendeley.com/research/muscle-efficient-shock-absorber
Events
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Mendeley | Further Information

{"title"=>"Why muscle is an efficient shock absorber", "type"=>"journal", "authors"=>[{"first_name"=>"Michael A.", "last_name"=>"Ferenczi", "scopus_author_id"=>"7004095466"}, {"first_name"=>"Sergey Y.", "last_name"=>"Bershitsky", "scopus_author_id"=>"6602382378"}, {"first_name"=>"Natalia A.", "last_name"=>"Koubassova", "scopus_author_id"=>"6603336307"}, {"first_name"=>"Galina V.", "last_name"=>"Kopylova", "scopus_author_id"=>"56402021500"}, {"first_name"=>"Manuel", "last_name"=>"Fernandez", "scopus_author_id"=>"57199901526"}, {"first_name"=>"Theyencheri", "last_name"=>"Narayanan", "scopus_author_id"=>"7005826466"}, {"first_name"=>"Andrey K.", "last_name"=>"Tsaturyan", "scopus_author_id"=>"6701901344"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"24465673", "doi"=>"10.1371/journal.pone.0085739", "sgr"=>"84899810436", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "scopus"=>"2-s2.0-84899810436", "issn"=>"19326203", "pui"=>"373023139"}, "id"=>"7ca6a794-fbe5-3daa-a82f-844ca9268419", "abstract"=>"Skeletal muscles power body movement by converting free energy of ATP hydrolysis into mechanical work. During the landing phase of running or jumping some activated skeletal muscles are subjected to stretch. Upon stretch they absorb body energy quickly and effectively thus protecting joints and bones from impact damage. This is achieved because during lengthening, skeletal muscle bears higher force and has higher instantaneous stiffness than during isometric contraction, and yet consumes very little ATP. We wish to understand how the actomyosin molecules change their structure and interaction to implement these physiologically useful mechanical and thermodynamical properties. We monitored changes in the low angle x-ray diffraction pattern of rabbit skeletal muscle fibers during ramp stretch compared to those during isometric contraction at physiological temperature using synchrotron radiation. The intensities of the off-meridional layer lines and fine interference structure of the meridional M3 myosin x-ray reflection were resolved. Mechanical and structural data show that upon stretch the fraction of actin-bound myosin heads is higher than during isometric contraction. On the other hand, the intensities of the actin layer lines are lower than during isometric contraction. Taken together, these results suggest that during stretch, a significant fraction of actin-bound heads is bound non-stereo-specifically, i.e. they are disordered azimuthally although stiff axially. As the strong or stereo-specific myosin binding to actin is necessary for actin activation of the myosin ATPase, this finding explains the low metabolic cost of energy absorption by muscle during the landing phase of locomotion.", "link"=>"http://www.mendeley.com/research/muscle-efficient-shock-absorber", "reader_count"=>25, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Student > Doctoral Student"=>3, "Researcher"=>3, "Student > Ph. D. Student"=>3, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Student > Doctoral Student"=>3, "Researcher"=>3, "Student > Ph. D. Student"=>3, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>4, "Unspecified"=>2, "Nursing and Health Professions"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>4, "Medicine and Dentistry"=>5, "Arts and Humanities"=>1, "Sports and Recreations"=>6, "Physics and Astronomy"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>4}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Sports and Recreations"=>{"Sports and Recreations"=>6}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>4}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>2}, "Arts and Humanities"=>{"Arts and Humanities"=>1}}, "reader_count_by_country"=>{"Austria"=>1, "Finland"=>1, "Nigeria"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1357697"], "description"=>"<p>Averaged records (from top to bottom): calculated temperature, motor position (in % of bundle length), tension and an example of the x-ray exposure framing (signal from a pin diode in a run of the experimental protocol). Noise on the pin diode signal, 30 ms from the beginning of the recording is caused by the high voltage heating pulse of the T-jump apparatus.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "muscle", "Muscle biochemistry", "Muscle functions", "Biochemistry", "enzymes", "Enzyme structure", "biophysics", "biomechanics", "Cell mechanics", "Cell motility", "Actin filaments", "Muscle components", "Cell physiology"], "article_id"=>909985, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Michael A. Ferenczi", "Sergey Y. Bershitsky", "Natalia A. Koubassova", "Galina V. Kopylova", "Manuel Fernandez", "Theyencheri Narayanan", "Andrey K. Tsaturyan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085739.g001", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimental_protocol_/909985", "title"=>"Experimental protocol.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-23 03:13:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/1357698"], "description"=>"<p><i>A</i>: records from top to bottom: tension, change in half-sarcomere length, ΔSL, calculated from the motor position for SL = 2.45 <b><i>μ</i></b>m; ΔSL measured by laser diffraction (more noisy traces). <i>B</i>: two fragments of the records shown in <i>A</i> on an expanded time scale to visualize changes in tension and sarcomere length during and after the step length changes applied during isometric contraction and ramp stretch. The length changes were used to measure fiber stiffness.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "muscle", "Muscle biochemistry", "Muscle functions", "Biochemistry", "enzymes", "Enzyme structure", "biophysics", "biomechanics", "Cell mechanics", "Cell motility", "Actin filaments", "Muscle components", "Cell physiology", "instantaneous", "stiffness"], "article_id"=>909986, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Michael A. Ferenczi", "Sergey Y. Bershitsky", "Natalia A. Koubassova", "Galina V. Kopylova", "Manuel Fernandez", "Theyencheri Narayanan", "Andrey K. Tsaturyan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085739.g002", "stats"=>{"downloads"=>2, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Change_in_instantaneous_stiffness_measured_in_a_control_experiment_with_a_single_muscle_fiber_/909986", "title"=>"Change in instantaneous stiffness measured in a control experiment with a single muscle fiber.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-23 03:13:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/1357700"], "description"=>"<p>The difference between the diffraction patterns recorded during the isometric and the stretching phases, collected from 9 runs of the protocol in 5 bundles of muscle fibers in the first experimental series. The isometric pattern was subtracted from the pattern collected during stretch that had been multiplied by a factor of 1.035–1.059 to correct for the stretch-induced decrease in the fiber volume exposed to the x-rays. White and black correspond to an increase and decrease in the intensity during stretch compared to isometric contraction, respectively. X-ray reflections of interest are marked.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "muscle", "Muscle biochemistry", "Muscle functions", "Biochemistry", "enzymes", "Enzyme structure", "biophysics", "biomechanics", "Cell mechanics", "Cell motility", "Actin filaments", "Muscle components", "Cell physiology", "x-ray"], "article_id"=>909988, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Michael A. Ferenczi", "Sergey Y. Bershitsky", "Natalia A. Koubassova", "Galina V. Kopylova", "Manuel Fernandez", "Theyencheri Narayanan", "Andrey K. Tsaturyan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085739.g003", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Low_angle_X_ray_diffraction_/909988", "title"=>"Low-angle X-ray diffraction.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-23 03:13:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/1357704"], "description"=>"<p>The intensities were integrated in the reciprocal radii regions of ±0.018 nm<sup>−1</sup> (meridian), 0.018–0.035 nm<sup>−1</sup> (10 row line), and 0.035–0.06 nm<sup>−1</sup> (11 row line) after correction for the change in specimen volume in the x-ray beam and mirroring four quadrants of the x-ray diffraction pattern. Background was subtracted as described <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085739#pone.0085739-Bershitsky2\" target=\"_blank\">[11]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085739#pone.0085739-Tsaturyan1\" target=\"_blank\">[14]</a>. The positions of some X-ray reflections of interest are marked.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "muscle", "Muscle biochemistry", "Muscle functions", "Biochemistry", "enzymes", "Enzyme structure", "biophysics", "biomechanics", "Cell mechanics", "Cell motility", "Actin filaments", "Muscle components", "Cell physiology", "profiles", "meridional", "off-meridional", "intensities", "isometric", "contraction", "ramp"], "article_id"=>909992, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Michael A. Ferenczi", "Sergey Y. Bershitsky", "Natalia A. Koubassova", "Galina V. Kopylova", "Manuel Fernandez", "Theyencheri Narayanan", "Andrey K. Tsaturyan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085739.g004", "stats"=>{"downloads"=>3, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Meridional_profiles_of_the_meridional_top_and_off_meridional_intensities_during_isometric_contraction_blue_lines_and_ramp_stretch_red_lines_in_the_1_st_series_of_experiments_/909992", "title"=>"Meridional profiles of the meridional (top) and off-meridional intensities during isometric contraction (blue lines) and ramp stretch (red lines) in the 1<sup>st</sup> series of experiments.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-23 03:13:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/1357705"], "description"=>"<p>The blue line corresponds to 40% of the total number of myosin heads bound to actin stereo-specifically by only one of the two heads of a myosin molecule. The black line corresponds to 60% of myosin heads stereo-specifically bound to actin: 20% of myosin molecules with one head only and the other 20% with both their heads. The purple and red lines correspond to non-stereo-specific attachment of the same 60% of heads with random uniform distribution of the azimuthal orientation angles within ranges of 60° or 80°, respectively. The vertical lines show the integration ranges for meridian (Mer), and the 10 and 11 row lines used for the experimental data shown in Fig. 3. Inset shows an actin filament (cyan, viewed along the filament axis) with a pair of stereo-specifically bound myosin heads (red heavy chains, magenta light chains). The same pair rotated by ±60° is shown in gray.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "muscle", "Muscle biochemistry", "Muscle functions", "Biochemistry", "enzymes", "Enzyme structure", "biophysics", "biomechanics", "Cell mechanics", "Cell motility", "Actin filaments", "Muscle components", "Cell physiology", "a1", "actin"], "article_id"=>909993, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Michael A. Ferenczi", "Sergey Y. Bershitsky", "Natalia A. Koubassova", "Galina V. Kopylova", "Manuel Fernandez", "Theyencheri Narayanan", "Andrey K. Tsaturyan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085739.g005", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Calculated_intensity_of_the_A1_actin_layer_line_/909993", "title"=>"Calculated intensity of the A1 actin layer line.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-23 03:13:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/1357706"], "description"=>"<p>The M3 profile during stretch scaled to equalize its low-angle peak with that measured during isometric contraction is shown by the dotted magenta line. Results of the modeling of the M3 meridional profile using the point diffractor model <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085739#pone.0085739-Linari2\" target=\"_blank\">[15]</a> with a half-bare zone length <i>b</i>, with the distance between crowns of myosin heads <i>d</i> and the total number of crowns <i>N</i> = 50 in each half of a thick filament: <i>b</i> = 74.75 nm and <i>d</i> = 14.564 nm that provide the best fit to the isometric data (blue dashed line) and <i>b</i> = 75.8 nm, <i>d</i> = 14.569 nm giving the best fit to the data obtained during stretch (red dashed line). The calculated profiles were then convoluted with a Gaussian point spread function with the standard deviation of 2.26 nm<sup>−1</sup>.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "muscle", "Muscle biochemistry", "Muscle functions", "Biochemistry", "enzymes", "Enzyme structure", "biophysics", "biomechanics", "Cell mechanics", "Cell motility", "Actin filaments", "Muscle components", "Cell physiology", "profiles", "isometric", "contraction", "experiments", "x-ray", "averaged", "halves", "patterns", "32", "runs"], "article_id"=>909994, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Michael A. Ferenczi", "Sergey Y. Bershitsky", "Natalia A. Koubassova", "Galina V. Kopylova", "Manuel Fernandez", "Theyencheri Narayanan", "Andrey K. Tsaturyan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085739.g006", "stats"=>{"downloads"=>3, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_M3_profiles_during_isometric_contraction_blue_continuous_line_and_stretch_red_continuous_line_in_the_second_series_of_experiments_with_a_long_x_ray_camera_averaged_over_two_halves_of_the_patterns_and_32_runs_of_the_protocol_in_three_fiber_bundles_/909994", "title"=>"M3 profiles during isometric contraction (blue continuous line) and stretch (red continuous line) in the second series of experiments with a long x-ray camera averaged over two halves of the patterns and 32 runs of the protocol in three fiber bundles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-23 03:13:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/1357707"], "description"=>"<p>During isometric contraction (state 1) only one (purple) head of a majority of myosin molecules is stereo-specifically bound to actin (cyan). Stretch unlocks the bound head to a non-stereo-specifically attached state and brings the distal part of the partner head to a position from which is can easily bind to a neighbor actin monomer (state 2). Then the second (red) head quickly binds actin also non-stereo-specifically (state 3). As both heads are bound non-stereo-specifically, the A1 intensity is low and stiffness is high. Further stretch leads to detachment of the purple head followed by its rapid rebinding to an actin 5.5 nm closer to the M-line of a sarcomere, thus producing a ‘head over head’ walking. The M-line of the sarcomere is on the left and the Z-disk is on the right.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "muscle", "Muscle biochemistry", "Muscle functions", "Biochemistry", "enzymes", "Enzyme structure", "biophysics", "biomechanics", "Cell mechanics", "Cell motility", "Actin filaments", "Muscle components", "Cell physiology", "myosin", "heads", "explains"], "article_id"=>909995, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Michael A. Ferenczi", "Sergey Y. Bershitsky", "Natalia A. Koubassova", "Galina V. Kopylova", "Manuel Fernandez", "Theyencheri Narayanan", "Andrey K. Tsaturyan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085739.g007", "stats"=>{"downloads"=>4, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_model_of_the_movement_of_myosin_heads_upon_muscle_stretch_that_explains_our_data_/909995", "title"=>"Schematic model of the movement of myosin heads upon muscle stretch that explains our data.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-23 03:13:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/1357708"], "description"=>"1<p>The off-meridional x-ray intensities of the M1 and A1 layer lines in the region of the 10 and 11 row lines (0.018–0.06 nm<sup>−1</sup>).</p>2<p>The meridional x-ray intensity of the M3 reflection integrated in the radial range of ±0.018 nm<sup>−1</sup> and meridional range of 0.066–0.072 nm<sup>−1</sup> in the experiments with short x-ray camera.</p>3<p>Average meridional spacing of the M3 reflection measured as the center of gravity of the intensity profile in the same meridional and radial range as <i>I</i><sub>M3</sub>. Summed data for all three experiments with long x-ray camera.</p>4<p>Average spacing of the M3 reflection calculated only for the data points where the intensity was above 5% of the peak value to avoid possible errors caused by background subtraction or the presence of non-myosin reflections; the same data set as for <i>S</i><sub>M3</sub>.</p>5<p>The ratio of the amplitudes of the high- and low-angle peaks in the fine structure of the M3 reflection. Statistics was obtained by analysing the M3 intensities in each half of the pattern in three experiments with long x-ray camera.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "muscle", "Muscle biochemistry", "Muscle functions", "Biochemistry", "enzymes", "Enzyme structure", "biophysics", "biomechanics", "Cell mechanics", "Cell motility", "Actin filaments", "Muscle components", "Cell physiology", "spacing", "x-ray", "reflections"], "article_id"=>909996, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Michael A. Ferenczi", "Sergey Y. Bershitsky", "Natalia A. Koubassova", "Galina V. Kopylova", "Manuel Fernandez", "Theyencheri Narayanan", "Andrey K. Tsaturyan"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085739.t001", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_the_intensity_and_spacing_of_some_x_ray_reflections_upon_stretch_/909996", "title"=>"Changes in the intensity and spacing of some x-ray reflections upon stretch.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-23 03:13:30"}

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Relative Metric

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