Identification of naturally occurring fatty acids of the myelin sheath that resolve neuroinflammation

Science Translational Medicine

Volumn 4, Issue 137, 2012, Pages

  Ho, Peggy P ^a   Kanter, Jennifer L ^a   Johnson, Amanda M ^a   Srinagesh, Hrishikesh K ^a   Chang, Eun Ju ^a,b   Purdy, Timothy M ^a,b   Van Haren, Keith ^a,b   Wikoff, William R ^c   Kind, Tobias ^c   Khademi, Mohsen ^d   Matloff, Laura Y ^a   Narayana, Sirisha ^a   Hur, Eun Mi ^a   Lindstrom, Tamsin M ^a,b   He, Zhigang ^e   Fiehn, Oliver ^c   Olsson, Tomas ^d   Han, Xianlin ^f   Han, May H ^a   Steinman, Lawrence ^a   Robinson, William H ^a,b   more..

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d KAROLINSKA INSTITUTE   (Sweden)

^e HARVARD MEDICAL SCHOOL   (United States)

^f BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 PALMITOYL 2 GLUTAROYL SN GLYCERO 3 PHOSPHOCHOLINE; 1 PALMITOYL 2 OLEOYL SN GLYCERO 3 [PHOSPHO SERINE]; AUTOANTIBODY; CENTRAL NERVOUS SYSTEM AGENTS; DIPALMITOYLPHOSPHATIDYLCHOLINE; FATTY ACID; PHOSPHATIDYLCHOLINE; PHOSPHOLIPID ANTIBODY; SATURATED FATTY ACID; SPHINGOMYELIN; UNCLASSIFIED DRUG; PHOSPHOLIPID;

ADULT; AGED; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DETECTION; ANTIGEN ANTIBODY REACTION; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DRUG DETERMINATION; DRUG EFFECT; DRUG STRUCTURE; FATTY ACID ANALYSIS; FEMALE; HUMAN; HUMAN TISSUE; LIPID STORAGE; LYMPHOCYTE PROLIFERATION; MALE; MASS SPECTROMETRY; MICROARRAY ANALYSIS; MOUSE; MULTIPLE SCLEROSIS; MYELIN SHEATH; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; ANIMAL; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM; NICK END LABELING; WESTERN BLOTTING;

ANIMALS; AUTOANTIBODIES; BLOTTING, WESTERN; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FATTY ACIDS; FEMALE; FLOW CYTOMETRY; IN SITU NICK-END LABELING; MICE; MULTIPLE SCLEROSIS; MYELIN SHEATH; PHOSPHOLIPIDS;

EID: 84862129146     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3003831     Document Type: Article

References (47)

1. C. P. Genain, B. Cannella, S. L. Hauser, C. S. Raine, Identification of autoantibodies associated with myelin damage in multiple sclerosis. Nat. Med. 5, 170 -175 (1999).
2. J. Goverman, Autoimmune T cell responses in the central nervous system. Nat. Rev. Immunol. 9, 393-407 (2009).
3. J. L. Kanter, S. Narayana, P. P. Ho, I. Catz, K. G. Warren, R. A. Sobel, L. Steinman, W. H. Robinson, Lipid microarrays identify key mediators of autoimmune brain inflammation. Nat. Med. 12, 138-143 (2006).
4. M. P. Pender, P. A. Csurhes, N. P.Wolfe, K. D. Hooper, M. F. Good, P. A. McCombe, J. M. Greer, Increased circulating T cell reactivity to GM3 and GQ1b gangliosides in primary progressive multiple sclerosis. J. Clin. Neurosci. 10, 63-66 (2003).
5. F. J. Quintana, M. F. Farez, V. Viglietta, A. H. Iglesias, Y. Merbl, G. Izquierdo, M. Lucas, A. S. Basso, S. J. Khoury, C. F. Lucchinetti, I. R. Cohen, H. L. Weiner, Antigen microarrays identify unique serum autoantibody signatures in clinical and pathologic subtypes of multiple sclerosis. Proc. Natl. Acad. Sci. U.S.A. 105, 18889-18894 (2008).
6. A. Shamshiev, A. Donda, I. Carena, L. Mori, L. Kappos, G. De Libero, Self glycolipids as T-cell autoantigens. Eur. J. Immunol. 29, 1667-1675 (1999).
7. L. M. Villar, M. C. Sádaba, E. Roldan, J. Masjuan, P. González-Porqué, N. Villarrubia, M. Espiño, J. A. García-Trujillo, A. Bootello, J. C. Alvarez-Cermeño, Intrathecal synthesis of oligoclonal IgM against myelin lipids predicts an aggressive disease course in MS. J. Clin. Invest. 115, 187-194 (2005).
8. J. Rosenbluth, R. Schiff, W. L. Liang, W. Dou, Antibody-mediated CNS demyelination II. Focal spinal cord lesions induced by implantation of an IgM antisulfatide-secreting hybridoma. J. Neurocytol. 32, 265-276 (2003).
9. V. G. Tusher, R. Tibshirani, G. Chu, Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U.S.A. 98, 5116-5121 (2001).
10. M. B. Eisen, P. T. Spellman, P. O. Brown, D. Botstein, Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95, 14863-14868 (1998).
11. J. Qin, R. Goswami, R. Balabanov, G. Dawson, Oxidized phosphatidylcholine is a marker for neuroinflammation in multiple sclerosis brain. J. Neurosci. Res. 85, 977 -984 (2007).
12. B. W. Agranoff, J. A. Benjamins, A. K. Hajra, Lipids, in Basic Neurochemistry: Molecular, Cellular and Medical Aspects, G. J. Siegel, B. W. Agranoff, R. W. Albers, S. K. Fisher, M. D. Fisher, Eds. (Lippincott-Raven, Philadelphia, 1999).
13. J. van Horssen, G. Schreibelt, J. Drexhage, T. Hazes, C. D. Dijkstra, P. van der Valk, H. E. de Vries, Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radic. Biol. Med. 45, 1729-1737 (2008).
14. M. H. Han, S. I. Hwang, D. B. Roy, D. H. Lundgren, J. V. Price, S. S. Ousman, G. H. Fernald, B. Gerlitz, W. H. Robinson, S. E. Baranzini, B. W. Grinnell, C. S. Raine, R. A. Sobel, D. K. Han, L. Steinman, Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets. Nature 451, 1076-1081 (2008).
15. J. J. Lafaille, K. Nagashima, M. Katsuki, S. Tonegawa, High incidence of spontaneous autoimmune encephalomyelitis in immunodeficient anti-myelin basic protein T cell receptor transgenic mice. Cell 78, 399-408 (1994).
16. J. Schulze-Luehrmann, S. Ghosh, Antigen-receptor signaling to nuclear factor kB. Immunity 25, 701-715 (2006).
17. M. A. Collart, P. Baeuerle, P. Vassalli, Regulation of tumor necrosis factor alpha transcription in macrophages: Involvement of four kB-like motifs and of constitutive and inducible forms of NF-kB. Mol. Cell. Biol. 10, 1498-1506 (1990).
18. T. A. Libermann, D. Baltimore, Activation of interleukin-6 gene expression through the NF-κB transcription factor. Mol. Cell. Biol. 10, 2327-2334 (1990).
19. A. Sica, L. Dorman, V. Viggiano, M. Cippitelli, P. Ghosh, N. Rice, H. A. Young, Interaction of NF-kB and NFAT with the interferon-γ promoter. J. Biol. Chem. 272, 30412-30420 (1997).
20. J. Dutta, Y. Fan, N. Gupta, G. Fan, C. Gélinas, Current insights into the regulation of programmed cell death by NF-κB. Oncogene 25, 6800-6816 (2006).
21. M. Hinz, D. Krappmann, A. Eichten, A. Heder, C. Scheidereit, M. Strauss, NF-κB function in growth control: Regulation of cyclin D1 expression and G0/G1-to-S-phase transition. Mol. Cell. Biol. 19, 2690-2698 (1999).
22. B. Greve, R. Weissert, N. Hamdi, E. Bettelli, R. A. Sobel, A. Coyle, V. K. Kuchroo, K. Rajewsky, M. Schmidt-Supprian, IkB kinase 2/β deficiency controls expansion of autoreactive T cells and suppresses experimental autoimmune encephalomyelitis. J. Immunol. 179, 179 -185 (2007).
23. R. Anjum, J. Blenis, The RSK family of kinases: Emerging roles in cellular signalling. Nat. Rev. Mol. Cell Biol. 9, 747-758 (2008).
24. M. W. Ludwinski, J. Sun, B. Hilliard, S. Gong, F. Xue, R. J. Carmody, J. Devirgiliis, Y. H. Chen, Critical roles of Bim in T cell activation and T cell -mediated autoimmune inflammation in mice. J. Clin. Invest. 119, 1706-1713 (2009).
25. F. Luciano, A. Jacquel, P. Colosetti, M. Herrant, S. Cagnol, G. Pages, P. Auberger, Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene 22, 6785-6793 (2003).
26. A. Essafi, S. Fernández de Mattos, Y. A. Hassen, I. Soeiro, G. J.Mufti, N. S. Thomas, R. H. Medema, E. W. Lam, Direct transcriptional regulation of Bim by FoxO3a mediates STI571-induced apoptosis in Bcr-Abl-expressing cells. Oncogene 24, 2317-2329 (2005).
27. M. C. Hu, D. F. Lee, W. Xia, L. S. Golfman, F. Ou-Yang, J. Y. Yang, Y. Zou, S. Bao, N. Hanada, H. Saso, R. Kobayashi, M. C. Hung, IkB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 117, 225-237 (2004).
28. A. Bonni, A. Brunet, A. E. West, S. R. Datta, M. A. Takasu, M. E. Greenberg, Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286, 1358-1362 (1999).
29. J. Zha, H. Harada, E. Yang, J. Jockel, S. J. Korsmeyer, Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-XL. Cell 87, 619-628 (1996).
30. O. Haworth, M. Cernadas, R. Yang, C. N. Serhan, B. D. Levy, Resolvin E1 regulates interleukin 23, interferon-g and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat. Immunol. 9, 873-879 (2008).
31. J. M. Schwab, N. Chiang, M. Arita, C. N. Serhan, Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447, 869-874 (2007).
32. G. O. Fruhwirth, A. Loidl, A. Hermetter, Oxidized phospholipids: From molecular properties to disease. Biochim. Biophys. Acta 1772, 718-736 (2007).
33. C. Lock, G. Hermans, R. Pedotti, A. Brendolan, E. Schadt, H. Garren, A. Langer-Gould, S. Strober, B. Cannella, J. Allard, P. Klonowski, A. Austin, N. Lad, N. Kaminski, S. J. Galli, J. R. Oksenberg, C. S. Raine, R. Heller, L. Steinman, Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8, 500 -508 (2002).
34. E. M. Hur, S. Youssef, M. E. Haws, S. Y. Zhang, R. A. Sobel, L. Steinman, Osteopontin-induced relapse and progression of autoimmune brain disease through enhanced survival of activated T cells. Nat. Immunol. 8, 74-83 (2007).
35. M. P. Pender, Treating autoimmune demyelination by augmenting lymphocyte apoptosis in the central nervous system. J. Neuroimmunol. 191, 26-38 (2007).
36. O. Bagasra, F. H. Michaels, Y. M. Zheng, L. E. Bobroski, S. V. Spitsin, Z. F. Fu, R. Tawadros, H. Koprowski, Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. Proc. Natl. Acad. Sci. U.S.A. 92, 12041-12045 (1995).
37. M. Barton, R. Minotti, E. Haas, Inflammation and atherosclerosis. Circ. Res. 101, 750-751 (2007).
38. J. A. Berliner, G. Subbanagounder, N. Leitinger, A. D. Watson, D. Vora, Evidence for a role of phospholipid oxidation products in atherogenesis. Trends Cardiovasc. Med. 11, 142-147 (2001).
39. V. N. Bochkov, D. Mechtcheriakova, M. Lucerna, J. Huber, R. Malli,W. F. Graier, E. Hofer, B. R. Binder, N. Leitinger, Oxidized phospholipids stimulate tissue factor expression in human endothelial cells via activation of ERK/EGR-1 and Ca++/NFAT. Blood 99, 199-206 (2002).
40. T. J. Cunningham, L. Yao, M. Oetinger, L. Cort, E. P. Blankenhorn, J. I. Greenstein, Secreted phospholipase A2 activity in experimental autoimmune encephalomyelitis and multiple sclerosis. J. Neuroinflammation 3, 26 (2006).
41. L. Klareskog, J. Ronnelid, K. Lundberg, L. Padyukov, L. Alfredsson, Immunity to citrullinated proteins in rheumatoid arthritis. Annu. Rev. Immunol. 26, 651-675 (2008).
42. H. Cheng, X. Jiang, X. Han, Alterations in lipid homeostasis of mouse dorsal root ganglia induced by apolipoprotein E deficiency: A shotgun lipidomics study. J. Neurochem. 101, 57-76 (2007).
43. X. Han, R. W. Gross, Shotgun lipidomics: Multidimensional MS analysis of cellular lipidomes. Expert Rev. Proteomics 2, 253-264 (2005).
44. X. Han, R. W. Gross, Shotgun lipidomics: Electrospray ionization mass spectrometric analysis and quantitation of cellular lipidomes directly from crude extracts of biological samples. Mass Spectrom. Rev. 24, 367-412 (2005).
45. X. Han, K. Yang, R. W. Gross, Microfluidics-based electrospray ionization enhances the intrasource separation of lipid classes and extends identification of individual molecular species through multi-dimensional mass spectrometry: Development of an automated high-throughput platform for shotgun lipidomics. Rapid Commun. Mass Spectrom. 22, 2115-2124 (2008).
46. A. K. Singh, M. T. Wilson, S. Hong, D. Olivares-Villagómez, C. Du, A. K. Stanic, S. Joyce, S. Sriram, Y. Koezuka, L. Van Kaer, Natural killer T cell activation protects mice against experimental autoimmune encephalomyelitis. J. Exp. Med. 194, 1801-1811 (2001).
47. I. Mattila, T. Seppänen-Laakso, T. Suortti, M. Oresic, Application of lipidomics and metabolomics to the study of adipose tissue. Methods Mol. Biol. 456, 123 -130 (2008).