Defining the phenotype of neutrophils following reverse migration in zebrafish

Stimulation of neutrophil reverse migration presents an attractive, alternative therapeutic pathway to driving inflammation resolution. However, little is known about whether the activity of wound‐experienced neutrophils is altered and whether encouraging dispersal of such neutrophils back into the body may have undesirable consequences. This study used a zebrafish tail transection inflammation model, in combination with a photoconvertible neutrophil transgenic line, to allow internally controlled, simultaneous comparison of reverse‐migrated neutrophils with naïve neutrophils in the presence and absence of secondary insult. Detailed microscopy revealed that reverse‐migrated neutrophils exhibited an activated morphology but responded normally to secondary insult and are able to mount an effective antimicrobial response to Staphylococcus aureus. These results support a model in which reverse‐migrated neutrophils exhibit no long‐term behavioral alterations and encourage the notion of enhanced reverse migration as a viable target for pharmaceutical manipulation.

• Publication year

  2015

• Venue

  Journal of Leukocyte Biology

• Publication date

  2015-06-12

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1189/jlb.3MA0315-105RPMID 26071567PMCID 4661044
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• The Roles of Integrins in Function of Human Neutrophils after Their Migration through Endothelium into Interstitial Matrix

  2015cited by this paper
• Neutrophils in host defense: new insights from zebrafish

  2015cited by this paper
• Swimming Against the Tide: Drugs Drive Neutrophil Reverse Migration

  2014cited by this paper
• A Zebrafish Compound Screen Reveals Modulation of Neutrophil Reverse Migration as an Anti-Inflammatory Mechanism

  2014cited by this paper
• Real‐time imaging and genetic dissection of host–microbe interactions in zebrafish

  2014cited by this paper
• Redox and Src family kinase signaling control leukocyte wound attraction and neutrophil reverse migration

  2014cited by this paper
• The Role of Polymorphonuclear Leukocyte Trafficking in the Perpetuation of Inflammation During Inflammatory Bowel Disease

  2013cited by this paper
• Zebrafish tissue injury causes upregulation of interleukin-1 and caspase-dependent amplification of the inflammatory response

  2013cited by this paper
• Neutrophil function: from mechanisms to disease.

  2012cited by this paper
• Repelled from the wound, or randomly dispersed? Reverse migration behaviour of neutrophils characterized by dynamic modelling

  2012cited by this paper
• Drift-Diffusion Analysis of Neutrophil Migration during Inflammation Resolution in a Zebrafish Model

  2012cited by this paper
• A Method for the In Vivo Measurement of Zebrafish Tissue Neutrophil Lifespan

  2012influential reference
• Spatiotemporal photolabeling of neutrophil trafficking during inflammation in live zebrafish

  2011influential reference
• Neutrophil survival and c-kit(+)-progenitor proliferation in Staphylococcus aureus-infected skin wounds promote resolution.

  2011cited by this paper
• Activation of hypoxia-inducible factor-1α (Hif-1α) delays inflammation resolution by reducing neutrophil apoptosis and reverse migration in a zebrafish inflammation model.

  2011cited by this paper
• Phagosome dynamics during phagocytosis by neutrophils

  2011cited by this paper
• Junctional adhesion molecule-C (JAM-C) regulates polarized neutrophil transendothelial cell migration in vivo

  2011influential reference
• Neutrophil kinetics in health and disease

  2010cited by this paper
• Neutrophils in rheumatoid arthritis: More than simple final effectors.

  2010cited by this paper
• Fluorescent indicators for intracellular pH.

  2010cited by this paper
• Resolution of in flammation: state of the art, definitions and terms

  2006cited by this paper
• Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish

  2006cited by this paper
• Identification of a phenotypically and functionally distinct population of long‐lived neutrophils in a model of reverse endothelial migration

  2006cited by this paper
• A transgenic zebrafish model of neutrophilic inflammation.

  2006cited by this paper
• Neutrophils and immunity: challenges and opportunities

  2006cited by this paper
• Bacteremias: a leading cause of death.

  2005cited by this paper
• Resolution of inflammation: the beginning programs the end

  2005cited by this paper
• How neutrophils kill microbes.

  2005cited by this paper
• σB Modulates Virulence Determinant Expression and Stress Resistance: Characterization of a Functional rsbU Strain Derived from Staphylococcus aureus 8325-4

  2002cited by this paper
• Regulation of macrophage cytokine production by phagocytosis of apoptotic and post-apoptotic cells.

  1998cited by this paper
• The neutrophil in rheumatoid arthritis.

  1995cited by this paper
• Neutrophil priming: the cellular signals that say 'amber' but not 'green'.

  1995cited by this paper
• Neutrophil signal transduction and activation of the respiratory burst.

  1993cited by this paper
• Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products.

  1992cited by this paper
• Tissue destruction by neutrophils.

  1989cited by this paper
• Neutrophils and host defense.

  1988cited by this paper
• Neutrophils and host defense.

  1988cited by this paper
• Neutrophil leucocyte chemotaxis: a simplified assay for measuring polarizing responses to chemotactic factors.

  1985cited by this paper

• Vcam1 in endothelial and stromal cells regulates hematopoietic stem cell contact with the niche

  2025cites this paper
• Neutrophil Macrophage Crosstalk via Extracellular Vesicles Drives Reverse Migration in a Fully Human Model of Wound Healing

  2025cites this paper
• What can we learn about fish neutrophil and macrophage response to immune challenge from studies in zebrafish.

  2024cites this paper
• Neutrophils in cancer: from biology to therapy

  2024cites this paper
• Neutrophil immune profile guides spinal cord regeneration in zebrafish.

  2024cites this paper
• Fusobacterium nucleatum dissemination by neutrophils

  2023cites this paper
• Exploring the dynamic behavior of leukocytes with zebrafish.

  2023cites this paper
• Lemon-derived nanovesicles achieve antioxidant and anti-inflammatory effects activating the AhR/Nrf2 signaling pathway

  2023cites this paper
• Molecular Actors of Inflammation and Their Signaling Pathways: Mechanistic Insights from Zebrafish

  2023cites this paper
• Roscovitine Worsens Mycobacterium abscessus Infection by Reducing DUOX2-Mediated Neutrophil Response.

  2022cites this paper
• Neutrophil dynamics and inflammaging in acute ischemic stroke: A transcriptomic review

  2022cites this paper
• Neutrophil reverse migration

  2022cites this paper
• Human neutrophil kinetics: a call to revisit old evidence.

  2022cites this paper
• Wound Healing Insights from Flies and Fish.

  2022cites this paper
• Transgenic zebrafish larvae as a non-rodent alternative model to assess pro-inflammatory (neutrophil) responses to nanomaterials

  2022cites this paper
• Neutrophil Migratory Patterns: Implications for Cardiovascular Disease

  2022cites this paper
• Real‐time imaging of inflammation and its resolution: It’s apparent because it’s transparent *

  2022cites this paper
• Neutrophils in the Pathogenesis of Rheumatoid Arthritis and Systemic Lupus Erythematosus: Same Foe Different M.O.

  2021cites this paper
• Vascular endothelial growth factor-c regulates hematopoietic stem cell fate in the dorsal aorta.

  2021cites this paper
• Microfluidic devices for neutrophil migration studies

  2021cites this paper
• Neutrophils in acute inflammation: current concepts and translational implications

  2021cites this paper
• Development of Anti-fibrotic Therapy in Stricturing Crohn's Disease: Lessons from Randomized Trials in Other Fibrotic Diseases.

  2021cites this paper
• Neutrophil motion in numbers: How to analyse complex migration patterns.

  2021cites this paper
• Neutrophils in secondary lymphoid organs

  2021cites this paper
• Signal integration in forward and reverse neutrophil migration: Fundamentals and emerging mechanisms.

  2021cites this paper
• Persistent neutrophilic inflammation associated with chronic pulmonary infection causes progressive lung

  2021cites this paper
• Pioneer neutrophils release chromatin within in vivo swarms

  2021influential citation
• Zebrafish as a Tool for Studying Inflammation: A Systematic Review

  2021cites this paper
• Modeling Inflammation in Zebrafish for the Development of Anti-inflammatory Drugs

  2021cites this paper
• SLIT2/ROBO1-signaling inhibits macropinocytosis by opposing cortical cytoskeletal remodeling

  2020cites this paper
• Chemokine Receptors and Phagocyte Biology in Zebrafish

  2020influential citation
• Improvement Testing Strategy for Aligning Nanomaterial Safety Assessments and Oxidative Stress Responses

  2020cites this paper
• Hif‐1alpha stabilisation is protective against infection in zebrafish comorbid models

  2020cites this paper
• The Diverse Roles of Phagocytes During Bacterial and Fungal Infections and Sterile Inflammation: Lessons From Zebrafish

  2020cites this paper
• Live Imaging of Heart Injury in Larval Zebrafish Reveals a Multi-Stage Model of Neutrophil and Macrophage Migration

  2020cites this paper
• Correlations between oxidative stress and aligning nanoparticle safety assessments

  2020cites this paper
• Review of inflammation in fish and value of the zebrafish model.

  2020cites this paper
• Rheumatoid Arthritis Synovial Fluid Neutrophils Drive Inflammation Through Production of Chemokines, Reactive Oxygen Species, and Neutrophil Extracellular Traps

  2020cites this paper
• Edinburgh Research Explorer Live imaging of the immune response to heart injury in larval zebrafish reveals a multi-stage model of neutrophil and macrophage migration

  2020cites this paper
• Hif-1alpha stabilisation is protective against infection in a zebrafish model of comorbidity

  2019cites this paper
• Inhibition of ErbB kinase signalling promotes resolution of neutrophilic inflammation

  2019cites this paper
• Harmful neutrophil subsets in patients with ischemic stroke

  2019cites this paper
• Microfluidic arenas for war games between neutrophils and microbes.

  2019cites this paper
• Anti‐inflammatory effect of a novel synthetic compound 1‐((4‐fluorophenyl)thio)isoquinoline in RAW264.7 macrophages and a zebrafish model

  2019cites this paper
• Macrophages target Salmonella by Lc3-associated phagocytosis in a systemic infection model

  2019cites this paper
• Endogenous pioneer neutrophils release NETs during the swarming response in zebrafish

  2019cites this paper
• Neutrophil Diversity in Health and Disease

  2019cites this paper
• The CXCL12/CXCR4 Signaling Axis Retains Neutrophils at Inflammatory Sites in Zebrafish

  2019cites this paper
• Immunomodulation and cellular response to biomaterials: the overriding role of neutrophils in healing

  2019cites this paper
• Real-time functional analysis of Hv1 channel in neutrophils: a new approach from zebrafish model.

  2019cites this paper
• The CXCL12/CXCR4 signalling axis retains neutrophils at inflammatory sites in zebrafish

  2019cites this paper
• Prolonged neutrophil retention in the wound impairs zebrafish heart regeneration after cryoinjury.

  2019cites this paper
• Drosophila immune cells extravasate from vessels to wounds using Tre1 GPCR and Rho signaling

  2018cites this paper
• Adoption of in vitro systems and zebrafish embryos as alternative models for reducing rodent use in assessments of immunological and oxidative stress responses to nanomaterials

  2018cites this paper
• The Neutrophil Nucleus: An Important Influence on Neutrophil Migration and Function

  2018cites this paper
• The neutrophil: one cell on many missions or many cells with different agendas?

  2018cites this paper
• Parallels between vertebrate cardiac and cutaneous wound healing and regeneration

  2018cites this paper
• Cxcl8b and Cxcr2 Regulate Neutrophil Migration through Bloodstream in Zebrafish

  2017cites this paper
• The role of tetraspanins in neutrophil survival and phagocytosis

  2017cites this paper
• PGE2 production at sites of tissue injury promotes an anti-inflammatory neutrophil phenotype and determines the outcome of inflammation resolution in vivo

  2017cites this paper
• Measurement of bacterial capture and phagosome maturation of Kupffer cells by intravital microscopy.

  2017cites this paper
• Inflammation and metabolism in tissue repair and regeneration

  2017cites this paper
• Macrophages, but not neutrophils, are critical for proliferation of Burkholderia cenocepacia and ensuing host-damaging inflammation

  2017cites this paper
• Targeting Neutrophilic Inflammation Using Polymersome-Mediated Cellular Delivery

  2017cites this paper
• Myeloid Cells in Cutaneous Wound Repair

  2016cites this paper
• Editorial: Fish neutrophils meet proresolving eicosanoids

  2016cites this paper
• Neutrophil migration in infection and wound repair: going forward in reverse

  2016cites this paper
• Innate antiviral defense of zebrafish : from signalling to specialized cells

  2016cites this paper
• Défenses innées antivirales du poisson zèbre : de la signalisation aux cellules specialisées

  2016cites this paper
• Role of cyclin-dependent kinase 9 in the resolution of innate inflammation in a zebrafish tailfin injury model

  2016cites this paper
• Reverse Migration of Neutrophils: Where, When, How, and Why?

  2016cites this paper
• Role of reverse transendothelial migration of neutrophils in inflammation

  2016cites this paper
• Key mechanisms governing resolution of lung inflammation

  2016cites this paper
• Neutrophils in the Tumor Microenvironment.

  2016cites this paper
• Wound repair: a showcase for cell plasticity and migration.

  2016cites this paper
• Neutrophils and arthritis: Role in disease and pharmacological perspectives.

  2016cites this paper