Redox and Src Family Kinase Signaling Control Leukocyte Wound Attraction and Neutrophil Reverse Migration

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2014 Dec 10

PMID 25488917

Citations 74

Authors

Sebastien Tauzin

Taylor W Starnes

Francisco Barros Becker

Pui-Ying Lam

Anna Huttenlocher

Affiliations

Soon will be listed here.

Abstract

Tissue damage induces early recruitment of neutrophils through redox-regulated Src family kinase (SFK) signaling in neutrophils. Redox-SFK signaling in epithelium is also necessary for wound resolution and tissue regeneration. How neutrophil-mediated inflammation resolves remains unclear. In this paper, we studied the interactions between macrophages and neutrophils in response to tissue damage in zebrafish and found that macrophages contact neutrophils and induce resolution via neutrophil reverse migration. We found that redox-SFK signaling through p22phox and Yes-related kinase is necessary for macrophage wound attraction and the subsequent reverse migration of neutrophils. Importantly, macrophage-specific reconstitution of p22phox revealed that macrophage redox signaling is necessary for neutrophil reverse migration. Thus, redox-SFK signaling in adjacent tissues is essential for coordinated leukocyte wound attraction and repulsion through pathways that involve contact-mediated guidance.

Citing Articles

THP-1 Macrophages Limit Neutrophil Transendothelial Migration in a Model Infection.

Ignes-Romeu A, Weppner H, Kaur T, Singh M, Hind L Cell Mol Bioeng. 2024; 17(4):279-293.

PMID: 39372553 PMC: 11450111. DOI: 10.1007/s12195-024-00813-2.

IRG1/ACOD1 promotes neutrophil reverse migration and alleviates local inflammation.

Ji J, Zhong H, Li Y, Billiar T, Wilson M, Scott M J Leukoc Biol. 2024; 116(4):854-863.

PMID: 38713770 PMC: 11444257. DOI: 10.1093/jleuko/qiae110.

Loss of Myo19 increases metastasis by enhancing microenvironmental ROS gradient and chemotaxis.

Ren X, Shi P, Su J, Wei T, Li J, Hu Y EMBO Rep. 2024; 25(3):971-990.

PMID: 38279020 PMC: 10933354. DOI: 10.1038/s44319-023-00052-y.

Smart Responsive and Controlled-Release Hydrogels for Chronic Wound Treatment.

Jia X, Dou Z, Zhang Y, Li F, Xing B, Hu Z Pharmaceutics. 2023; 15(12).

PMID: 38140076 PMC: 10747460. DOI: 10.3390/pharmaceutics15122735.

Exploring the dynamic behavior of leukocytes with zebrafish.

Michael C, de Oliveira S Curr Opin Cell Biol. 2023; 85:102276.

PMID: 37956533 PMC: 10842401. DOI: 10.1016/j.ceb.2023.102276.

References

Li L, Yan B, Shi Y, Zhang W, Wen Z . Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration. J Biol Chem. 2012; 287(30):25353-60. PMC: 3408142. DOI: 10.1074/jbc.M112.349126. View

Chaubey S, Jones G, Shah A, Cave A, Wells C . Nox2 is required for macrophage chemotaxis towards CSF-1. PLoS One. 2013; 8(2):e54869. PMC: 3562318. DOI: 10.1371/journal.pone.0054869. View

Starnes T, Huttenlocher A . Neutrophil reverse migration becomes transparent with zebrafish. Adv Hematol. 2012; 2012:398640. PMC: 3401556. DOI: 10.1155/2012/398640. View

Baruzzi A, Caveggion E, Berton G . Regulation of phagocyte migration and recruitment by Src-family kinases. Cell Mol Life Sci. 2008; 65(14):2175-90. PMC: 11131848. DOI: 10.1007/s00018-008-8005-6. View

Woodfin A, Voisin M, Beyrau M, Colom B, Caille D, Diapouli F . The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat Immunol. 2011; 12(8):761-9. PMC: 3145149. DOI: 10.1038/ni.2062. View

Sindrilaru A, Scharffetter-Kochanek K . Disclosure of the Culprits: Macrophages-Versatile Regulators of Wound Healing. Adv Wound Care (New Rochelle). 2014; 2(7):357-368. PMC: 3842885. DOI: 10.1089/wound.2012.0407. View

Brune B, Dehne N, Grossmann N, Jung M, Namgaladze D, Schmid T . Redox control of inflammation in macrophages. Antioxid Redox Signal. 2013; 19(6):595-637. PMC: 3718318. DOI: 10.1089/ars.2012.4785. View

Abram C, Lowell C . The diverse functions of Src family kinases in macrophages. Front Biosci. 2008; 13:4426-50. PMC: 4457449. DOI: 10.2741/3015. View

Theveneau E, Steventon B, Scarpa E, Garcia S, Trepat X, Streit A . Chase-and-run between adjacent cell populations promotes directional collective migration. Nat Cell Biol. 2013; 15(7):763-72. PMC: 4910871. DOI: 10.1038/ncb2772. View

10.

Nathan C . Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol. 2006; 6(3):173-82. DOI: 10.1038/nri1785. View

11.

Byeon S, Yi Y, Oh J, Yoo B, Hong S, Cho J . The role of Src kinase in macrophage-mediated inflammatory responses. Mediators Inflamm. 2012; 2012:512926. PMC: 3504478. DOI: 10.1155/2012/512926. View

12.

Bratton D, Henson P . Neutrophil clearance: when the party is over, clean-up begins. Trends Immunol. 2011; 32(8):350-7. PMC: 3151332. DOI: 10.1016/j.it.2011.04.009. View

13.

Mathias J, Perrin B, Liu T, Kanki J, Look A, Huttenlocher A . Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J Leukoc Biol. 2006; 80(6):1281-8. DOI: 10.1189/jlb.0506346. View

14.

Silva M . When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J Leukoc Biol. 2010; 87(1):93-106. DOI: 10.1189/jlb.0809549. View

15.

Ortega-Gomez A, Perretti M, Soehnlein O . Resolution of inflammation: an integrated view. EMBO Mol Med. 2013; 5(5):661-74. PMC: 3662311. DOI: 10.1002/emmm.201202382. View

16.

Meng F, Lowell C . A beta 1 integrin signaling pathway involving Src-family kinases, Cbl and PI-3 kinase is required for macrophage spreading and migration. EMBO J. 1998; 17(15):4391-403. PMC: 1170772. DOI: 10.1093/emboj/17.15.4391. View

17.

Li L, Jin H, Xu J, Shi Y, Wen Z . Irf8 regulates macrophage versus neutrophil fate during zebrafish primitive myelopoiesis. Blood. 2010; 117(4):1359-69. DOI: 10.1182/blood-2010-06-290700. View

18.

ABERCROMBIE M . Contact inhibition: the phenomenon and its biological implications. Natl Cancer Inst Monogr. 1967; 26:249-77. View

19.

Zhu J, Brdicka T, Katsumoto T, Lin J, Weiss A . Structurally distinct phosphatases CD45 and CD148 both regulate B cell and macrophage immunoreceptor signaling. Immunity. 2008; 28(2):183-96. PMC: 2265106. DOI: 10.1016/j.immuni.2007.11.024. View

20.

Yoo S, Huttenlocher A . Spatiotemporal photolabeling of neutrophil trafficking during inflammation in live zebrafish. J Leukoc Biol. 2011; 89(5):661-7. PMC: 3079246. DOI: 10.1189/jlb.1010567. View