Oscillatory Behavior of Neutrophils under Opposing Chemoattractant Gradients Supports a Winner-Take-All Mechanism
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{"title"=>"Oscillatory behavior of neutrophils under opposing chemoattractant gradients supports a winner-take-all mechanism", "type"=>"journal", "authors"=>[{"first_name"=>"Matthew B.", "last_name"=>"Byrne", "scopus_author_id"=>"56389229800"}, {"first_name"=>"Yuki", "last_name"=>"Kimura", "scopus_author_id"=>"56389084700"}, {"first_name"=>"Ashish", "last_name"=>"Kapoor", "scopus_author_id"=>"35368543800"}, {"first_name"=>"Yuan", "last_name"=>"He", "scopus_author_id"=>"55542925900"}, {"first_name"=>"Kewin S.", "last_name"=>"Mattam", "scopus_author_id"=>"56389561000"}, {"first_name"=>"Katherine M.", "last_name"=>"Hasan", "scopus_author_id"=>"56389353900"}, {"first_name"=>"Luke N.", "last_name"=>"Olson", "scopus_author_id"=>"22235039300"}, {"first_name"=>"Fei", "last_name"=>"Wang", "scopus_author_id"=>"56388927200"}, {"first_name"=>"Paul J.A.", "last_name"=>"Kenis", "scopus_author_id"=>"6701733846"}, {"first_name"=>"Christopher V.", "last_name"=>"Rao", "scopus_author_id"=>"55362704500"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84903774661", "doi"=>"10.1371/journal.pone.0085726", "pui"=>"372852913", "pmid"=>"24465668", "scopus"=>"2-s2.0-84903774661", "issn"=>"19326203", "isbn"=>"1932-6203"}, "id"=>"3a4f846a-dede-3f6c-a50a-5d71a223299f", "abstract"=>"Neutrophils constitute the largest class of white blood cells and are the first responders in the innate immune response. They are able to sense and migrate up concentration gradients of chemoattractants in search of primary sites of infection and inflammation through a process known as chemotaxis. These chemoattractants include formylated peptides and various chemokines. While much is known about chemotaxis to individual chemoattractants, far less is known about chemotaxis towards many. Previous studies have shown that in opposing gradients of intermediate chemoattractants (interleukin-8 and leukotriene B4), neutrophils preferentially migrate toward the more distant source. In this work, we investigated neutrophil chemotaxis in opposing gradients of chemoattractants using a microfluidic platform. We found that primary neutrophils exhibit oscillatory motion in opposing gradients of intermediate chemoattractants. To understand this behavior, we constructed a mathematical model of neutrophil chemotaxis. Our results suggest that sensory adaptation alone cannot explain the observed oscillatory motion. Rather, our model suggests that neutrophils employ a winner-take-all mechanism that enables them to transiently lock onto sensed targets and continuously switch between the intermediate attractant sources as they are encountered. These findings uncover a previously unseen behavior of neutrophils in opposing gradients of chemoattractants that will further aid in our understanding of neutrophil chemotaxis and the innate immune response. In addition, we propose a winner-take-all mechanism allows the cells to avoid stagnation near local chemical maxima when migrating through a network of chemoattractant sources.", "link"=>"http://www.mendeley.com/research/oscillatory-behavior-neutrophils-under-opposing-chemoattractant-gradients-supports-winnertakeall-mec", "reader_count"=>40, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>5, "Researcher"=>13, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>3, "Student > Master"=>1, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>5, "Researcher"=>13, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>3, "Student > Master"=>1, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Engineering"=>2, "Biochemistry, Genetics and Molecular Biology"=>5, "Mathematics"=>1, "Agricultural and Biological Sciences"=>15, "Medicine and Dentistry"=>1, "Physics and Astronomy"=>5, "Immunology and Microbiology"=>6}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>5}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>6}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>15}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>5}}, "reader_count_by_country"=>{"Sweden"=>1, "United States"=>1, "Portugal"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

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  • {"files"=>["https://ndownloader.figshare.com/files/1353505"], "description"=>"<p>Representative cell trajectories indicating the migration behavior of cells in [A] isotropic conditions (50 nM LTB<sub>4</sub>), [B] single gradients (0–50 nM LTB<sub>4</sub>), and [C] dual opposing gradients of IL-8 (0–10 nM) and LTB<sub>4</sub> (0–15 nM).</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Immune physiology", "Immune cells", "developmental biology", "morphogenesis", "cell migration", "immunology", "immunity", "Innate immunity", "Molecular cell biology", "Cellular types", "Signal transduction", "systems biology", "Theoretical biology", "trajectories", "varying", "intermediate", "chemoattractant"], "article_id"=>905972, "categories"=>["Biological Sciences"], "users"=>["Matthew B. Byrne", "Yuki Kimura", "Ashish Kapoor", "Yuan He", "Kewin S. Mattam", "Katherine M. Hasan", "Luke N. Olson", "Fei Wang", "Paul J. A. Kenis", "Christopher V. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085726.g003", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sample_cell_trajectories_under_varying_intermediate_chemoattractant_conditions_/905972", "title"=>"Sample cell trajectories under varying intermediate chemoattractant conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:44:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1353500"], "description"=>"<p>[A] Chemotactic index in single attractant gradients. [B] Average linear velocities of the cells from the single attractant gradient experiments. In each experiment, 30 cells were tracked for 20 minutes.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Immune physiology", "Immune cells", "developmental biology", "morphogenesis", "cell migration", "immunology", "immunity", "Innate immunity", "Molecular cell biology", "Cellular types", "Signal transduction", "systems biology", "Theoretical biology", "attractant"], "article_id"=>905967, "categories"=>["Biological Sciences"], "users"=>["Matthew B. Byrne", "Yuki Kimura", "Ashish Kapoor", "Yuan He", "Kewin S. Mattam", "Katherine M. Hasan", "Luke N. Olson", "Fei Wang", "Paul J. A. Kenis", "Christopher V. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085726.g001", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chemotaxis_in_single_attractant_gradients_/905967", "title"=>"Chemotaxis in single attractant gradients.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:44:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1353510"], "description"=>"<p>[A] Cell trajectories along the channel width in our microfluidic experiments, under isotropic (25 nM IL-8), single linear gradient (0–25 nM IL-8), single hill-type gradient (0–25-0 nM IL-8), and dual opposing gradients of 150 nM LTB<sub>4</sub> and 100 nM IL-8, respectively. The hill-type gradient was established using a three-inlet device with a similar design to the “Y-shaped” device. Confirmation of the concentration profile is shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085726#pone.0085726.s006\" target=\"_blank\">Figure S6</a>. [B] Simulated cell positions along the channel width obtained from our feedback-based model, when applied to the corresponding chemoattractant conditions. The qualitative behaviors are similar. The parameter used for the simulation are: µm/s, M, M, and .</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Immune physiology", "Immune cells", "developmental biology", "morphogenesis", "cell migration", "immunology", "immunity", "Innate immunity", "Molecular cell biology", "Cellular types", "Signal transduction", "systems biology", "Theoretical biology", "neutrophil", "responses", "varying"], "article_id"=>905977, "categories"=>["Biological Sciences"], "users"=>["Matthew B. Byrne", "Yuki Kimura", "Ashish Kapoor", "Yuan He", "Kewin S. Mattam", "Katherine M. Hasan", "Luke N. Olson", "Fei Wang", "Paul J. A. Kenis", "Christopher V. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085726.g006", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_theoretical_and_experimental_neutrophil_responses_to_varying_conditions_/905977", "title"=>"Comparison of theoretical and experimental neutrophil responses to varying conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:44:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1353508"], "description"=>"<p>Oscillatory behavior results from the amplification of the response toward the distant chemokine source, while inhibition of the opposite signal results in the switch-like behavior. The variables and denote the positive feedback loops governing the switch behavior.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Immune physiology", "Immune cells", "developmental biology", "morphogenesis", "cell migration", "immunology", "immunity", "Innate immunity", "Molecular cell biology", "Cellular types", "Signal transduction", "systems biology", "Theoretical biology", "governing", "oscillatory"], "article_id"=>905975, "categories"=>["Biological Sciences"], "users"=>["Matthew B. Byrne", "Yuki Kimura", "Ashish Kapoor", "Yuan He", "Kewin S. Mattam", "Katherine M. Hasan", "Luke N. Olson", "Fei Wang", "Paul J. A. Kenis", "Christopher V. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085726.g005", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_of_proposed_mechanism_governing_oscillatory_motion_/905975", "title"=>"Schematic of proposed mechanism governing oscillatory motion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:44:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1353507"], "description"=>"<p>The cell trajectories were analyzed to count the number of times the channel centerline was crossed within each 80 minute experiment. Noise was attenuated using state estimation via a standard Kalman filter with process noise variance set to 10<sup>−4</sup> microns<sup>2</sup>. The first two columns on the left represent the single gradient controls for IL-8 and LTB<sub>4</sub> respectively. P-values relate to single gradient controls, where * represents statistical significance compared to isotropic conditions (p<0.05). Statistical significance was determined using a one-tailed Welch's t-test of unequal variance on the data.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Immune physiology", "Immune cells", "developmental biology", "morphogenesis", "cell migration", "immunology", "immunity", "Innate immunity", "Molecular cell biology", "Cellular types", "Signal transduction", "systems biology", "Theoretical biology", "zero"], "article_id"=>905974, "categories"=>["Biological Sciences"], "users"=>["Matthew B. Byrne", "Yuki Kimura", "Ashish Kapoor", "Yuan He", "Kewin S. Mattam", "Katherine M. Hasan", "Luke N. Olson", "Fei Wang", "Paul J. A. Kenis", "Christopher V. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085726.g004", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Oscillatory_behavior_based_on_zero_crossings_/905974", "title"=>"Oscillatory behavior based on zero crossings.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:44:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1353503"], "description"=>"<p>[A] Chemotactic index in a 0–25 nM fMLP gradient over uniform intermediate chemoattractant concentration. The fMLP gradient was fixed for all conditions, while the concentration of the uniform intermediate chemoattractant background was varied from 0 to 10 nM for both IL-8 and LTB<sub>4</sub>. 30 cells were tracked for 20 minutes for each experiment. [B] Chemotactic index in 0–25 nM IL-8 and 0–15 nM LTB<sub>4</sub> gradients over uniform concentration of fMLP. All conditions in the left figure consisted of a fixed 0–25 nM IL-8 gradient with a uniform concentration of fMLP, while all conditions on the right had a fixed 0–15 nM LTB<sub>4</sub> gradient with a uniform concentration of fMLP. 30 cells were tracked for each experiment. [C] Chemotactic indices for cells in intermediate chemoattractant gradients over uniform background concentration of alternate intermediate chemoattractant. All conditions in the left figure consisted of a fixed 0–15 nM IL-8 gradient over a varying uniform LTB<sub>4</sub> background, while all conditions in the right figure consisted of a fixed 0–25 nM LTB<sub>4</sub> gradient over a varying uniform IL-8 background.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Immune physiology", "Immune cells", "developmental biology", "morphogenesis", "cell migration", "immunology", "immunity", "Innate immunity", "Molecular cell biology", "Cellular types", "Signal transduction", "systems biology", "Theoretical biology", "gradients", "superimposed", "isotropic", "attractant"], "article_id"=>905970, "categories"=>["Biological Sciences"], "users"=>["Matthew B. Byrne", "Yuki Kimura", "Ashish Kapoor", "Yuan He", "Kewin S. Mattam", "Katherine M. Hasan", "Luke N. Olson", "Fei Wang", "Paul J. A. Kenis", "Christopher V. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085726.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chemotaxis_in_single_gradients_superimposed_over_isotropic_attractant_field_/905970", "title"=>"Chemotaxis in single gradients superimposed over isotropic attractant field.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:44:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1353516"], "description"=>"<p>Gray lines denote the trajectories of individual cells. Red and blue lines denote the contours for Gaussian concentration profiles for intermediate chemoattractant sources and the green lines denote the contours for an end-target chemoattractant source (positioned in the center of the plot). Note the cells migrate between intermediate sources of chemoattractants before converging on the final end target. The parameter values used in this simulation are: µm/s, M, , and . All chemoattractant sources were modeled as Gaussians: where µm<sup>2</sup> and denote the position of the source.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Immune physiology", "Immune cells", "developmental biology", "morphogenesis", "cell migration", "immunology", "immunity", "Innate immunity", "Molecular cell biology", "Cellular types", "Signal transduction", "systems biology", "Theoretical biology", "stepwise", "navigation", "chemoattractant"], "article_id"=>905983, "categories"=>["Biological Sciences"], "users"=>["Matthew B. Byrne", "Yuki Kimura", "Ashish Kapoor", "Yuan He", "Kewin S. Mattam", "Katherine M. Hasan", "Luke N. Olson", "Fei Wang", "Paul J. A. Kenis", "Christopher V. Rao"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0085726.g007", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Simulation_of_stepwise_navigation_through_multiple_chemoattractant_sources_/905983", "title"=>"Simulation of stepwise navigation through multiple chemoattractant sources.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-21 03:44:10"}

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Relative Metric

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