Defining the phenotype of neutrophils following reverse migration in zebrafish

Journal of Leukocyte Biology

Volumn 98, Issue 6, 2015, Pages 975-981

  Ellett, Felix ^a   Elks, Philip M ^a   Robertson, Anne L ^a   Ogryzko, Nikolay V ^a   Renshaw, Stephen A ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Chemotaxis; Granulocytes; Infection; Inflammation; Phagocytosis

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERICIDAL ACTIVITY; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; INFLAMMATION; LEUKOCYTE ACTIVATION; MICROSCOPY; MODEL; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL REVERSE MIGRATION; NONHUMAN; OXIDATIVE STRESS; PHAGOSOME; PHENOTYPE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; ZEBRA FISH; ANIMAL; CELL MOTION; GENETICS; IMMUNOLOGY; NEUTROPHIL; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL MOVEMENT; INFLAMMATION; NEUTROPHILS; STAPHYLOCOCCUS AUREUS; ZEBRAFISH;

EID: 84948969823     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3MA0315-105R     Document Type: Article

References (38)

1. Serhan, C. N., Brain, S. D., Buckley, C. D., Gilroy, D. W., Haslett, C., O’Neill, L. A., Perretti, M., Rossi, A. G., Wallace, J. L. (2007) Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21, 325–332.
2. Weiss, S. J. (1989) Tissue destruction by neutrophils. N. Engl. J. Med. 320, 365–376.
3. Brazil, J. C., Louis, N. A., Parkos, C. A. (2013) The role of polymorphonuclear leukocyte trafficking in the perpetuation of inflammation during inflammatory bowel disease. Inflamm. Bowel Dis. 19, 1556–1565.
4. Pillinger, M. H., Abramson, S. B. (1995) The neutrophil in rheumatoid arthritis. Rheum. Dis. Clin. North Am. 21, 691–714.
5. Cascão, R., Rosário, H. S., Souto-Carneiro, M. M., Fonseca, J. E. (2010) Neutrophils in rheumatoid arthritis: more than simple final effectors. Autoimmun. Rev. 9, 531–535.
6. Serhan, C. N., Savill, J. (2005) Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6, 1191–1197.
7. Buckley, C. D., Ross, E. A., McGettrick, H. M., Osborne, C. E., Haworth, O., Schmutz, C., Stone, P. C., Salmon, M., Matharu, N. M., Vohra, R. K., Nash, G. B., Rainger, G. E. (2006) Identification of a phenotypically and functionally distinct population of long-lived neutrophils in a model of reverse endothelial migration. J. Leukoc. Biol. 79, 303–311.
8. Elks, P. M., van Eeden, F. J., Dixon, G., Wang, X., Reyes-Aldasoro, C. C., Ingham, P. W., Whyte, M. K., Walmsley, S. R., Renshaw, S. A. (2011) Activation of hypoxia-inducible factor-1a (Hif-1a) delays inflammation resolution by reducing neutrophil apoptosis and reverse migration in a zebrafish inflammation model. Blood 118, 712–722.
9. Mathias, J. R., Perrin, B. J., Liu, T. X., Kanki, J., Look, A. T., Huttenlocher, A. (2006) Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J. Leukoc. Biol. 80, 1281–1288.
10. Woodfin, A., Voisin, M. B., Beyrau, M., Colom, B., Caille, D., Diapouli, F. M., Nash, G. B., Chavakis, T., Albelda, S. M., Rainger, G. E., Meda, P., Imhof, B. A., Nourshargh, S. (2011) The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat. Immunol. 12, 761–769.
11. Robertson, A.L., Holmes, G. R., Bojarczuk, A. N., Burgon, J., Loynes, C. A., Chimen, M., Sawtell, A. K., Hamza, B., Willson, J., Walmsley, S. R., Anderson, S. R., Coles, M. C., Farrow, S. N., Solari, R., Jones, S., Prince, L. R., Irimia, D., Rainger, G. E., Kadirkamanathan, V., Whyte, M. K., Renshaw, S. A. (2014) A zebrafish compound screen reveals modulation of neutrophil reverse migration as an anti-inflammatory mechanism. Sci. Transl. Med. 6, 225ra29.
12. Tauzin, S., Starnes, T. W., Becker, F. B., Lam, P. Y., Huttenlocher, A. (2014) Redox and Src family kinase signaling control leukocyte wound attraction and neutrophil reverse migration. J. Cell Biol. 207, 589–598.
13. Holmes, G. R., Anderson, S. R., Dixon, G., Robertson, A. L., Reyes- Aldasoro, C. C., Billings, S. A., Renshaw, S. A., Kadirkamanathan, V. (2012) Repelled from the wound, or randomly dispersed? Reverse migration behaviour of neutrophils characterized by dynamic modelling. J. R. Soc. Interface 9, 3229–3239.
14. Yoo, S. K., Huttenlocher, A. (2011) Spatiotemporal photolabeling of neutrophil trafficking during inflammation in live zebrafish. J. Leukoc. Biol. 89, 661–667.
15. Dixon, G., Elks, P. M., Loynes, C. A., Whyte, M. K., Renshaw, S. A. (2012) A method for the in vivo measurement of zebrafish tissue neutrophil lifespan. ISRN Hematol. 2012, 915868.
16. Westerfield, M. (2007) The Zebrafish Book, 5th Ed.; A Guide for the Laboratory Use of Zebrafish (Danio rerio), University of Oregon Press, Eugene, OR.
17. Holmes, G. R., Dixon, G., Anderson, S. R., Reyes-Aldasoro, C. C., Elks, P. M., Billings, S. A., Whyte, M. K., Kadirkamanathan, V., Renshaw, S. A. (2012) Drift-diffusion analysis of neutrophil migration during inflammation resolution in a zebrafish model. Adv. Hematol. 2012, 792163.
18. Horsburgh, M. J., Aish, J. L., White, I. J., Shaw, L., Lithgow, J. K., Foster, S. J. (2002) sigmaB Modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J. Bacteriol. 184, 5457–5467.
19. Renshaw, S. A., Loynes, C. A., Trushell, D. M., Elworthy, S., Ingham, P. W., Whyte, M. K. (2006) A transgenic zebrafish model of neutrophilic inflammation. Blood 108, 3976–3978.
20. Summers, C., Rankin, S. M., Condliffe, A. M., Singh, N., Peters, A. M., Chilvers, E. R. (2010) Neutrophil kinetics in health and disease. Trends Immunol. 31, 318–324.
21. Colotta, F., Re, F., Polentarutti, N., Sozzani, S., Mantovani, A. (1992) Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 80, 2012–2020.
22. Kim, M. H., Granick, J. L., Kwok, C., Walker, N. J., Borjesson, D. L., Curry, F. R., Miller, L. S., Simon, S. I. (2011) Neutrophil survival and c-kit (+)-progenitor proliferation in Staphylococcus aureus-infected skin wounds promote resolution. Blood 117, 3343–3352.
23. Hallett, M. B., Lloyds, D. (1995) Neutrophil priming: the cellular signals that say ‘amber’ but not ‘green’. Immunol. Today 16, 264–268.
24. Nathan, C. (2006) Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6, 173–182.
25. Haston, W. S., Shields, J. M. (1985) Neutrophil leucocyte chemotaxis: a simplified assay for measuring polarizing responses to chemotactic factors. J. Immunol. Methods 81, 229–237.
26. Thelen, M., Dewald, B., Baggiolini, M. (1993) Neutrophil signal transduction and activation of the respiratory burst. Physiol. Rev. 73, 797–821.
27. Amulic, B., Cazalet, C., Hayes, G. L., Metzler, K. D., Zychlinsky, A. (2012) Neutrophil function: from mechanisms to disease. Annu. Rev. Immunol. 30, 459–489.
28. Lehrer, R. I., Ganz, T., Selsted, M. E., Babior, B. M., Curnutte, J. T. (1988) Neutrophils and host defense. Ann. Intern. Med. 109, 127–142.
29. Segal, A. W. (2005) How neutrophils kill microbes. Annu. Rev. Immunol. 23, 197–223.
30. Bearman, G. M., Wenzel, R. P. (2005) Bacteremias: a leading cause of death. Arch. Med. Res. 36, 646–659.
31. Nordenfelt, P., Tapper, H. (2011) Phagosome dynamics during phagocytosis by neutrophils. J. Leukoc. Biol. 90, 271–284.
32. Han, J., Burgess, K. (2010) Fluorescent indicators for intracellular pH. Chem. Rev. 110, 2709–2728.
33. Fadok, V. A., McDonald, P. P., Bratton, D. L., Henson, P. M. (1998) Regulation of macrophage cytokine production by phagocytosis of apoptotic and post-apoptotic cells. Biochem. Soc. Trans. 26, 653–656.
34. Lucas, C. D., Hoodless, L. J., Rossi, A. G. (2014) Swimming against the tide: drugs drive neutrophil reverse migration. Sci. Transl. Med. 6, 225fs9.
35. Ogryzko, N. V., Hoggett, E. E., Solaymani-Kohal, S., Tazzyman, S., Chico, T. J., Renshaw, S. A., Wilson, H. L. (2014) Zebrafish tissue injury causes upregulation of interleukin-1 and caspase-dependent amplification of the inflammatory response. Dis. Model. Mech. 7, 259–264.
36. Meijer, A. H., van der Vaart, M., Spaink, H. P. (2014) Real-time imaging and genetic dissection of host-microbe interactions in zebrafish. Cell. Microbiol. 16, 39–49.
37. Harvie, E. A., Huttenlocher, A. (2015) Neutrophils in host defense: new insights from zebrafish. J. Leukoc. Biol. [Epub ahead of print] doi: 10.1189/jlb.4MR1114-524R.
38. Luo, D., McGettrick, H. M., Stone, P. C., Rainger, G. E., Nash, G. B. (2015) The roles of integrins in function of human neutrophils after their migration through endothelium into interstitial matrix. PLoS ONE 10, e0118593.