Lyn is a redox sensor that mediates leukocyte wound attraction in vivo

Nature

Volumn 480, Issue 7375, 2011, Pages 109-112

  Yoo, Sa Kan ^a   Starnes, Taylor W ^a   Deng, Qing ^a   Huttenlocher, Anna ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; HYDROGEN PEROXIDE; LYN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

CHEMOTAXIS; CYPRINID; ENZYME ACTIVITY; HYDROGEN PEROXIDE; IMMUNE RESPONSE; IMMUNITY; INHIBITION; INJURY; LARVA; REDOX CONDITIONS; TUMOR; WOUNDING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHOSPHORYLATION; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATION REDUCTION REACTION; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WOUND HEALING;

ANIMALS; CELLS, CULTURED; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; LARVA; NEUTROPHILS; OXIDATION-REDUCTION; SRC-FAMILY KINASES; WOUNDS AND INJURIES; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 82555168190     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10632     Document Type: Article

References (39)

1. Nathan, C. Neutrophils and immunity: challenges and opportunities. Nature Rev. Immunol. 6, 173-182 (2006). (Pubitemid 43290987)
2. Dvorak, H.F.Tumors: wounds thatdonot heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315, 1650-1659 (1986). (Pubitemid 17052899)
3. Klyubin, I. V., Kirpichnikova, K. M. & Gamaley, I. A. Hydrogen peroxide-induced chemotaxis of mouse peritoneal neutrophils. Eur. J. Cell Biol. 70, 347-351 (1996). (Pubitemid 26268238)
4. Feng, Y., Santoriello, C., Mione, M., Hurlstone, A. & Martin, P. Live imaging of innate immune cell sensing of transformed cells in zebrafish larvae: parallels between tumor initiation and wound inflammation. PLoS Biol. 8, e1000562 (2010).
5. Moreira, S., Stramer, B., Evans, I., Wood, W. & Martin, P. Prioritization of competing damage and developmental signals by migrating macrophages in the Drosophila embryo. Curr. Biol. 20, 464-470 (2010).
6. Niethammer, P., Grabher, C., Look, A. T. & Mitchison, T. J. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459, 996-999 (2009).
7. 2, a necessary evil for cell signaling. Science 312, 1882-1883 (2006). (Pubitemid 43993698)
8. Bienert, G. P., Schjoerring, J. K. & Jahn, T. P. Membrane transport of hydrogen peroxide. Biochim. Biophys. Acta 1758, 994-1003 (2006). (Pubitemid 44373854)
9. Paulsen, C. E. & Carroll, K. S. Orchestrating redox signaling networks through regulatory cysteine switches. ACS Chem. Biol. 5, 47-62 (2010).
10. Poole, L.B.&Nelson, K.J.Discoveringmechanismsofsignaling- mediatedcysteine oxidation. Curr. Opin. Chem. Biol. 12, 18-24 (2008).
11. Miller, E. W., Dickinson, B. C. & Chang, C. J. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc. Natl Acad. Sci. USA 107, 15681-15686 (2010).
12. Burgoyne, J. R. et al. Cysteine redox sensor in PKGIa enables oxidant-induced activation. Science 317, 1393-1397 (2007). (Pubitemid 47417480)
13. Giannoni, E., Buricchi, F., Raugei, G., Ramponi, G. & Chiarugi, P. Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol. Cell. Biol. 25, 6391-6403 (2005). (Pubitemid 41023216)
14. Guo, Z., Kozlov, S., Lavin, M. F., Person, M. D. & Paull, T. T. ATM activation by oxidative stress. Science 330, 517-521 (2010).
15. Kemble, D.J.&Sun, G.Direct and specific inactivationofprotein tyrosine kinases in the Src and FGFR familiesby reversible cysteine oxidation. Proc. Natl Acad. Sci. USA 106, 5070-5075 (2009).
16. Mathias, J. R. et al. Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J. Leukoc. Biol. 80, 1281-1288 (2006). (Pubitemid 44904967)
17. Tobin, D. M. et al. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 140, 717-730 (2010).
18. Yoo, S. K. et al. Differential regulation of protrusion and polarity by PI3K during neutrophil motility in live zebrafish. Dev. Cell 18, 226-236 (2010).
19. Yoo, S.K.&Huttenlocher, A. Spatiotemporal photolabelingofneutrophil trafficking during inflammation in live zebrafish. J. Leukoc. Biol. 89, 661-667 (2011).
20. Martin, G. S. The hunting of the Src. Nature Rev. Mol. Cell Biol. 2, 467-475 (2001).
21. Sicheri, F., Moarefi, I.& Kuriyan, J.Crystal structure ofthe Src family tyrosine kinase Hck. Nature 385, 602-609 (1997). (Pubitemid 27087567)
22. Xu, W., Harrison, S. C. & Eck, M. J. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385, 595-602 (1997). (Pubitemid 27087566)
23. Yeatman, T. J. A renaissance for SRC. Nature Rev. Cancer 4, 470-480 (2004). (Pubitemid 38745532)
24. Scapini, P., Pereira, S., Zhang, H. & Lowell, C. A. Multiple roles of Lyn kinase in myeloid cell signaling and function. Immunol. Rev. 228, 23-40 (2009).
25. Hibbs, M. L. et al. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 83, 301-311 (1995).
26. Nishizumi, H. et al. Impaired proliferation of peripheral B cells and indication of autoimmune disease in lyn-deficient mice. Immunity 3, 549-560 (1995).
27. Pereira, S. & Lowell, C. The Lyn tyrosine kinase negatively regulates neutrophil integrin signaling. J. Immunol. 171, 1319-1327 (2003). (Pubitemid 36900063)
28. Lee, Y. M. et al. NOX4 as an oxygen sensor to regulate TASK-1 activity. Cell. Signal. 18, 499-507 (2006).
29. Abe, J., Takahashi, M., Ishida, M., Lee, J.D.&Berk, B.C.c-Srcisrequired for oxidative stress-mediated activationof big mitogen-activated protein kinase 1. J. Biol. Chem. 272, 20389-20394 (1997). (Pubitemid 27355589)
30. lyn tyrosine kinases. J. Biol. Chem. 271, 23464-23471 (1996). (Pubitemid 26314797)
31. Mathias, J.R.etal. Characterizationofzebrafish larval inflammatory macrophages. Dev. Comp. Immunol. 33, 1212-1217 (2009).
32. Bennett, C. M. et al. Myelopoiesis in the zebrafish, Danio rerio. Blood 98, 643-651 (2001).
33. Thisse, C. & Thisse, B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nature Protocols 3, 59-69 (2008).
34. Urasaki, A., Morvan, G. & Kawakami, K. Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics 174, 639-649 (2006). (Pubitemid 44656456)
35. Belousov, V. V. et al. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nature Methods 3, 281-286 (2006).
36. Chan, K. T., Cortesio, C. L. & Huttenlocher, A. FAK alters invadopodia and focal adhesion composition and dynamicstoregulate breast cancer invasion.J.Cell Biol. 185, 357-370 (2009).
37. Wong, B. R. et al. TRANCE, a TNF family member, activates Akt/PKB through a signaling complex involving TRAF6 and c-Src. Mol. Cell 4, 1041-1049 (1999). (Pubitemid 30054909)
38. Yamanashi, Y. et al. Activation of Src-like protein-tyrosine kinase Lyn and its association with phosphatidylinositol 3-kinase upon B-cell antigen receptor-mediated signaling. Proc. Natl Acad. Sci. USA 89, 1118-1122 (1992).
39. Heit, B. & Kubes, P. Measuring chemotaxis and chemokinesis: the under-agarose cell migration assay. Sci. STKE 2003, pl5 (2003).