XLipidomic profiling of influenza infection identifies mediators that induce and resolve inflammation

Cell

Volumn 154, Issue 1, 2013, Pages 213-

  Tam, Vincent C ^a   Quehenberger, Oswald ^b,d   Oshansky, Christine M ^e   Suen, Rosa ^a   Armando, Aaron M ^c,d   Treuting, Piper M ^f   Thomas, Paul G ^e   Dennis, Edward A ^c,d   Aderem, Alan ^a  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d San Diego   (United States)

^e ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^f UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

13 HYDROXYOCTADECADIENOIC ACID; 9 HYDROXYOCTADECADIENOIC ACID; ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONATE 15 LIPOXYGENASE; ARACHIDONATE 5 LIPOXYGENASE; CYTOCHROME P450; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 1BETA; INTERLEUKIN 5; INTERLEUKIN 6; KERATINOCYTE DERIVED CHEMOKINE; LINOLEIC ACID; LINOLENIC ACID; LIPOXYGENASE; MACROPHAGE INFLAMMATORY PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL POPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; FEMALE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INFLAMMATION; INFLUENZA; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; LIPID ANALYSIS; LIPID PEROXIDATION; LIPIDOMICS; LIQUID CHROMATOGRAPHY; LUNG ALVEOLUS EPITHELIUM; LUNG LAVAGE; MASS SPECTROMETRY; MOUSE; NASOPHARYNX; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; VIRUS LOAD;

ANIMALIA;

EID: 84879935264     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.05.052     Document Type: Article

References (43)

1. Allan, W., Tabi, Z., Cleary, A., and Doherty, P.C. (1990). Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+ T cells. J. Immunol. 144, 3980-3986.
2. Altmann, R., Hausmann, M., Spöttl, T., Gruber, M., Bull, A.W., Menzel, K., Vogl, D., Herfarth, H., Schölmerich, J., Falk, W., and Rogler, G. (2007). 13-Oxo-ODE is an endogenous ligand for PPARgamma in human colonic epithelial cells. Biochem. Pharmacol. 74, 612-622.
3. Ariel, A., and Serhan, C.N. (2007). Resolvins and protectins in the termination program of acute inflammation. Trends Immunol. 28, 176-183.
4. Bannenberg, G.L., Chiang, N., Ariel, A., Arita, M., Tjonahen, E., Gotlinger, K.H., Hong, S., and Serhan, C.N. (2005). Molecular circuits of resolution: formation and actions of resolvins and protectins. J. Immunol. 174, 4345-4355.
5. Belvisi, M.G., and Mitchell, J.A. (2009). Targeting PPAR receptors in the airway for the treatment of inflammatory lung disease. Br. J. Pharmacol. 158, 994-1003.
6. Buczynski, M.W., Dumlao, D.S., and Dennis, E.A. (2009). Thematic Review Series: Proteomics. An integrated omics analysis of eicosanoid biology. J. Lipid Res. 50, 1015-1038.
7. Chiang, N., Fredman, G., Bäckhed, F., Oh, S.F., Vickery, T., Schmidt, B.A., and Serhan, C.N. (2012). Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 484, 524-528.
8. Dennis, E.A., Deems, R.A., Harkewicz, R., Quehenberger, O., Brown, H.A., Milne, S.B., Myers, D.S., Glass, C.K., Hardiman, G., Reichart, D., et al. (2010). A mouse macrophage lipidome. J. Biol. Chem. 285, 39976-39985.
9. Drake, D.R., Brogden, K.A., Dawson, D.V., and Wertz, P.W. (2008). Thematic review series: skin lipids. Antimicrobial lipids at the skin surface. J. Lipid Res. 49, 4-11.
10. Dumlao, D.S., Buczynski, M.W., Norris, P.C., Harkewicz, R., and Dennis, E.A. (2011). High-throughput lipidomic analysis of fatty acid derived eicosanoids and N-acylethanolamines. Biochim. Biophys. Acta 1811, 724-736.
11. Francis, T., and De Torregrosa, M.V. (1945). Combined infection of Mice with H. influenzae and influenza virus by the intranasal route. J. Infect. Dis. 76, 70-77.
12. Godson, C., Mitchell, S., Harvey, K., Petasis, N.A., Hogg, N., and Brady, H.R. (2000). Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J. Immunol. 164, 1663-1667.
13. Hattori, T., Obinata, H., Ogawa, A., Kishi, M., Tatei, K., Ishikawa, O., and Izumi, T. (2008). G2A plays proinflammatory roles in human keratinocytes under oxidative stress as a receptor for 9-hydroxyoctadecadienoic acid. J. Invest. Dermatol. 128, 1123-1133.
14. Ishizaki, T., Shigemori, K., Nakai, T., Miyabo, S., Ozawa, T., Chang, S.W., and Voelkel, N.F. (1995). Leukotoxin, 9, 10-epoxy-12-octadecenoate causes edematous lung injury via activation of vascular nitric oxide synthase. Am. J. Physiol. 269, L65-L70.
15. Ishizaki, T., Ozawa, T., and Voelkel, N.F. (1999). Leukotoxins and the lung. Pulm. Pharmacol. Ther. 12, 145-155.
16. Jagger, B.W., Wise, H.M., Kash, J.C., Walters, K.A., Wills, N.M., Xiao, Y.L., Dunfee, R.L., Schwartzman, L.M., Ozinsky, A., Bell, G.L., et al. (2012). An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337, 199-204.
17. Jankov, R.P., Luo, X., Demin, P., Aslam, R., Hannam, V., Tanswell, A.K., and Pace-Asciak, C.R. (2002). Hepoxilin analogs inhibit bleomycin-induced pulmonary fibrosis in the mouse. J. Pharmacol. Exp. Ther. 301, 435-440.
18. Ji, R.-R., Xu, Z.-Z., Strichartz, G., and Serhan, C.N. (2011). Emerging roles of resolvins in the resolution of inflammation and pain. Trends Neurosci. 34, 599-609.
19. Kash, J.C., Tumpey, T.M., Proll, S.C., Carter, V., Perwitasari, O., Thomas, M.J., Basler, C.F., Palese, P., Taubenberger, J.K., García- Sastre, A., et al. (2006). Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443, 578-581.
20. Kiss, L., Schütte, H., Mayer, K., Grimm, H., Padberg, W., Seeger, W., and Grimminger, F. (2000). Synthesis of arachidonic acid-derived lipoxygenase and cytochrome P450 products in the intact human lung vasculature. Am. J. Respir. Crit. Care Med. 161, 1917-1923.
21. Krönke, G., Katzenbeisser, J., Uderhardt, S., Zaiss, M.M., Scholtysek, C., Schabbauer, G., Zarbock, A., Koenders, M.I., Axmann, R., Zwerina, J., et al. (2009). 12/15-lipoxygenase counteracts inflammation and tissue damage in arthritis. J. Immunol. 183, 3383-3389.
22. Kühn, H., and O'Donnell, V.B. (2006). Inflammation and immune regulation by 12/15-lipoxygenases. Prog. Lipid Res. 45, 334-356.
23. Kühn, H., Walther, M., and Kuban, R.J. (2002). Mammalian arachidonate 15-lipoxygenases structure, function, and biological implications. Prostaglandins Other Lipid Mediat. 68-69, 263-290.
24. Levy, B.D., Kohli, P., Gotlinger, K., Haworth, O., Hong, S., Kazani, S., Israel, E., Haley, K.J., and Serhan, C.N. (2007). Protectin D1 is generated in asthma and dampens airway inflammation and hyperresponsiveness. J. Immunol. 178, 496-502.
25. Morgan, L.T., Thomas, C.P., Kühn, H., and O'Donnell, V.B. (2010). Thrombin-activated human platelets acutely generate oxidized docosahexaenoic-acid-containing phospholipids via 12-lipoxygenase. Biochem. J. 431, 141-148.
26. Morita, M., Kuba, K., Ichikawa, A., Nakayama, M., Katahira, J., Iwamoto, R., Watanebe, T., Sakabe, S., Daidoji, T., Nakamura, S., et al. (2013). The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza. Cell 153, 112-125.
27. Neumann, G., Noda, T., and Kawaoka, Y. (2009). Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459, 931-939.
28. Obinata, H., and Izumi, T. (2009). G2A as a receptor for oxidized free fatty acids. Prostaglandins Other Lipid Mediat. 89, 66-72.
29. O'Flaherty, J.T., Hu, Y., Wooten, R.E., Horita, D.A., Samuel, M.P., Thomas, M.J., Sun, H., and Edwards, I.J. (2012). 15-lipoxygenase metabolites of doco-sahexaenoic acid inhibit prostate cancer cell proliferation and survival. PLoS ONE 7, e45480.
30. Quehenberger, O., and Dennis, E.A. (2011). The human plasma lipidome. N. Engl. J. Med. 365, 1812-1823.
31. Quehenberger, O., Armando, A.M., Brown, A.H., Milne, S.B., Myers, D.S., Merrill, A.H., Bandyopadhyay, S., Jones, K.N., Kelly, S., Shaner, R.L., et al. (2010). Lipidomics reveals a remarkable diversity of lipids in human plasma. J. Lipid Res. 51, 3299-3305.
32. Ricote, M., Li, A.C., Willson, T.M., Kelly, C.J., and Glass, C.K. (1998). The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 391, 79-82.
33. Sato, M., Suemori, H., Hata, N., Asagiri, M., Ogasawara, K., Nakao, K., Nakaya, T., Katsuki, M., Noguchi, S., Tanaka, N., and Taniguchi, T. (2000). Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13, 539-548.
34. Serhan, C.N., Maddox, J.F., Petasis, N.A., Akritopoulou-Zanze, I., Papayianni, A., Brady, H.R., Colgan, S.P., and Madara, J.L. (1995). Designoflipoxin A4 stable analogs that block transmigration and adhesion of human neutrophils. Biochemistry 34, 14609-14615.
35. Serhan, C.N., Clish, C.B., Brannon, J., Colgan, S.P., Chiang, N., and Gronert, K. (2000). Novel functional sets of lipid-derived mediators with antiinflamma-tory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J. Exp. Med. 192, 1197-1204.
36. Serhan, C.N., Chiang, N., and Van Dyke, T.E. (2008). Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8, 349-361.
37. Sisemore, M.F., Zheng, J., Yang, J.C., Thompson, D.A., Plopper, C.G., Corto-passi, G.A., and Hammock, B.D. (2001). Cellular characterization of leukotoxin diol-induced mitochondrial dysfunction. Arch. Biochem. Biophys. 392, 32-37.
38. Spiteller, P., and Spiteller, G. (1997). 9-Hydroxy-10, 12-octadecadienoic acid (9-HODE) and 13-hydroxy-9, 11-octadecadienoic acid (13-HODE): excellent markers for lipid peroxidation. Chem. Phys. Lipids 89, 131-139.
39. Taubenberger, J.K., and Kash, J.C. (2010). Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7, 440-451.
40. Thomson, S.J., Askari, A., and Bishop-Bailey, D. (2012). Anti-inflammatory effects of epoxyeicosatrienoic acids. Int. J. Vasc. Med. 2012, 605101.
41. Tobin, D.M., Roca, F.J., Oh, S.F., McFarland, R., Vickery, T.W., Ray, J.P., Ko, D.C., Zou, Y., Bang, N.D., Chau, T.T.H., et al. (2012). Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections. Cell 148, 434-446.
42. Totani, Y., Saito, Y., Ishizaki, T., Sasaki, F., Ameshima, S., and Miyamori, I. (2000). Leukotoxin and its diol induce neutrophil chemotaxis through signal transduction different from that of fMLP. Eur. Respir. J. 15, 75-79.
43. Wray, J.A., Sugden, M.C., Zeldin, D.C., Greenwood, G.K., Samsuddin, S., Miller-Degraff, L., Bradbury, J.A., Holness, M.J., Warner, T.D., and Bishop-Bailey, D. (2009). The epoxygenases CYP2J2 activates the nuclear receptor PPARalpha in vitro and in vivo. PLoS ONE 4, e7421.