The Axl receptor tyrosine kinase is a discriminator of macrophage function in the inflamed lung

Mucosal Immunology

Volumn 8, Issue 5, 2015, Pages 1021-1030

  Fujimori, T ^a   Grabiec, A M ^a   Kaur, M ^a   Bell, T J ^a   Fujino, N ^b   Cook, P C ^a   Svedberg, F R ^a   Macdonald, A S ^a   Maciewicz, R A ^b   Singh, D ^a   Hussell, T ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b ASTRAZENECA R AND D   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AXL RECEPTOR TYROSINE KINASE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GROWTH ARREST SPECIFIC PROTEIN 6; INTERFERON; MERTK PROTEIN; PROTEIN TYROSINE KINASE; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; GROWTH ARREST-SPECIFIC PROTEIN 6; ONCOPROTEIN; PROTEIN S; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE FUNCTION; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UPREGULATION; ANIMAL; ANTIBODY SPECIFICITY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; MACROPHAGE; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PNEUMONIA;

ANIMALS; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG; MACROPHAGES; MICE; MICE, KNOCKOUT; ORGAN SPECIFICITY; ORTHOMYXOVIRIDAE INFECTIONS; PNEUMONIA; PROTEIN S; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 84939504757     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.129     Document Type: Article

References (49)

1. Lemke, G. Biology of the TAM receptors. Cold. Spring. Harb. Perspect. Biol. 5, a009076 (2013).
2. Lemke, G. & Rothlin, C.V. Immunobiology of the TAM receptors. Nat. Rev. Immunol. 8, 327-336 (2008).
3. Ravichandran, K.S. Beginnings of a good apoptotic meal: the find-me and eat-me signaling pathways. Immunity 35, 445-455 (2011).
4. Seitz, H.M., Camenisch, T.D., Lemke, G., Earp, H.S. & Matsushima, G.K. Macrophages and dendritic cells use different Axl/Mertk/Tyro3 receptors in clearance of apoptotic cells. J. Immunol. 178, 5635-5642 (2007).
5. Zagorska, A., Traves, P.G., Lew, E.D., Dransfield, I. & Lemke, G. Diversification of TAM receptor tyrosine kinase function. Nat. Immunol. 15, 920-928 (2014).
6. Alciato, F., Sainaghi, P.P., Sola, D., Castello, L. & Avanzi, G.C. TNF-alpha, IL-6, and IL-1 expression is inhibited by GAS6 in monocytes/macrophages. J. Leukoc. Biol. 87, 869-875 (2010).
7. Rothlin, C.V. & Lemke, G. TAM receptor signaling and autoimmune disease. Curr. Opin. Immunol. 22, 740-746 (2010).
8. Sharif, M.N. et al. Twistmediates suppression of inflammation by type I IFNs and Axl. J. Exp. Med. 203, 1891-1901 (2006).
9. Lu, Q. & Lemke, G. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 293, 306-311 (2001).
10. Camenisch, T.D., Koller, B.H., Earp, H.S. & Matsushima, G.K. A novel receptor tyrosine kinase, Mer, inhibits TNF-alpha production and lipopolysaccharide-induced endotoxic shock. J. Immunol. 162, 3498-3503 (1999).
11. Deng, T., Zhang, Y., Chen, Q., Yan, K. & Han,D. Toll-like receptor-mediated inhibition of Gas6 and ProS expression facilitates inflammatory cytokine production in mouse macrophages. Immunology 135, 40-50 (2012).
12. Binder, M.D. & Kilpatrick, T.J. TAM receptor signalling and demyelination. Neuro-Signals 17, 277-287 (2009).
13. Ekman, C., Linder, A., Akesson, P. & Dahlback, B. Plasma concentrations of Gas6 (growth arrest specific protein 6) and its soluble tyrosine kinase receptor sAxl in sepsis and systemic inflammatory response syndromes. Crit. Care 14, R158 (2010).
14. Guignant, C. et al. Increased MerTK expression in circulating innate immune cells of patients with septic shock. Intensive Care Med. 39, 1556-1564 (2013).
15. Hussell, T. & Bell, T.J. Alveolar macrophages: plasticity in a tissue-specific context. Nat. Rev. Immunol. 14, 81-93 (2014).
16. Verma, A., Warner, S.L., Vankayalapati, H., Bearss, D.J. & Sharma, S. Targeting Axl and Mer kinases in cancer. Mol. Cancer Ther. 10, 1763-1773 (2011).
17. Gautier, E.L. et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13, 1118-1128 (2012).
18. Guilliams, M. et al. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J. Exp. Med. 210, 1977-1992 (2013).
19. Schneider, C. et al. Alveolar macrophages are essential for protection from respiratory failure and associated morbidity following influenza virus infection. PLoS Pathog. 10, e1004053 (2014).
20. Snelgrove, R.J. et al. A critical function for CD200 in lung immune homeostasis and the severity of influenza infection. Nat. Immunol. 9, 1074-1083 (2008).
21. Didierlaurent, A. et al. Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J. Exp. Med. 205, 323-329 (2008).
22. Holdenrieder, S. & Stieber, P. Clinical use of circulating nucleosomes. Crit. Rev. Clin. Lab. Sci. 46, 1-24 (2009).
23. Avanzi, G.C. et al. GAS6, the ligand of Axl and Rse receptors, is expressed in hematopoietic tissue but lacks mitogenic activity. Exp. Hematol. 25, 1219-1226 (1997).
24. Manfioletti, G., Brancolini, C., Avanzi, G. & Schneider, C. The protein encoded by a growth arrest-specific gene (Gas6) is a new member of the vitamin-K-dependent proteins related to protein-S, a negative coregulator in the blood-coagulation cascade. Mol. Cell. Biol. 13, 4976-4985 (1993).
25. Nakano, T. et al. Vascular smooth muscle cell-derived, Gla-containing growth-potentiating factor for Ca-mobilizing growth factors. J. Biol. Chem. 270, 5702-5705 (1995).
26. Nagata, K. et al. Identification of the product of growth arrest-specific gene 6 as a common ligand for Axl, Sky, and Mer receptor tyrosine kinases. J. Biol. Chem. 271, 30022-30027 (1996).
27. Trapnell, B.C. & Whitsett, J.A. Gm-CSF regulates pulmonary surfactant homeostasis and alveolar macrophage-mediated innate host defense. Annu. Rev. Physiol. 64, 775-802 (2002).
28. Kitamura, T. et al. Idiopathic pulmonary alveolar proteinosis as an autoimmune disease with neutralizing antibody against granulocyte/ macrophage colony-stimulating factor. J. Exp. Med. 190, 875-880 (1999).
29. Huang, F.F. et al. GM-CSF in the lung protects against lethal influenza infection. Am. J. Respir. Crit. Care. Med. 184, 259-268 (2011).
30. Mercer, J. Viral apoptotic mimicry party: P.S. Bring your own Gas6. Cell Host Microbe 9, 255-257 (2011).
31. Morizono, K. et al. The soluble serum protein Gas6 bridges virion envelope phosphatidylserine to the TAMreceptor tyrosine kinase Axl to mediate viral entry. Cell Host Microbe 9, 286-298 (2011).
32. Jemielity, S. et al. TIM-family proteins promote infection of multiple enveloped viruses through virion-associated phosphatidylserine. PLoS Pathog. 9, e1003232 (2013).
33. Rothlin, C.V., Ghosh, S., Zuniga, E.I., Oldstone, M.B. & Lemke, G. TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 131, 1124-1136 (2007).
34. Bhattacharyya, S. et al. Enveloped viruses disable innate immune responses in dendritic cells by direct activation of TAM receptors. Cell Host Microbe 14, 136-147 (2013).
35. Rock, K.L., Lai, J.J. & Kono, H. Innate and adaptive immune responses to cell death. Immunol. Rev. 243, 191-205 (2011).
36. Poon, I.K., Lucas, C.D., Rossi, A.G. & Ravichandran, K.S. Apoptotic cell clearance: basic biology and therapeutic potential. Nat. Rev. Immunol. 14, 166-180 (2014).
37. Kono, H. & Rock, K.L. How dying cells alert the immune system to danger. Nat. Rev. Immunol. 8, 279-289 (2008).
38. Bonilla, W.V. et al. The alarmin interleukin-33 drives protective antiviral CD8() T cell responses. Science 335, 984-989 (2012).
39. Abrams, S.T. et al. Circulating histones are mediators of trauma-associated lung injury. Am. J. Respir. Crit. Care Med. 187, 160-169 (2013).
40. Shibata, T. et al. Axl receptor blockade ameliorates pulmonary pathology resulting from primary viral infection and viral exacerbation of asthma. J. Immunol. 192, 3569-3581 (2014).
41. Ye, X. et al. An anti-Axl monoclonal antibody attenuates xenograft tumor growth and enhances the effect of multiple anticancer therapies. Oncogene 29, 5254-5264 (2010).
42. Cohen, P.L. et al. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 196, 135-140 (2002).
43. Takagi, T. et al. Direct effects of protein S in ameliorating acute lung injury. J. Thromb. Haemost. 7, 2053-2063 (2009).
44. Holland, S.J. et al. R428, a selective small molecule inhibitor of Axl kinase, blocks tumor spread and prolongs survival in models of metastatic breast cancer. Cancer Res. 70, 1544-1554 (2010).
45. Lu, Q. et al. Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature 398, 723-728 (1999).
46. Wirtz, S., Neufert, C., Weigmann, B. & Neurath, M.F. Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2, 541-546 (2007).
47. van Elden, L.J., Nijhuis, M., Schipper, P., Schuurman, R. & van Loon, A.M. Simultaneous detection of influenza viruses A and B using real-time quantitative PCR. J. Clin. Microbiol. 39, 196-200 (2001).
48. Miksa, M., Komura, H., Wu, R., Shah, K.G. & Wang, P. A novel method to determine the engulfment of apoptotic cells by macrophages using pHrodo succinimidyl ester. J. Immunol. Methods 342, 71-77 (2009).
49. Kent, L.M., Fox, S.M., Farrow, S.N. & Singh, D. The effects of dexamethasone on cigarette smoke induced gene expression changes in COPD macrophages. Int. Immunopharmacol. 10, 57-64 (2010).