Aspirin-triggered resolvin D1 prevents surgery-induced cognitive decline

FASEB Journal

Volumn 27, Issue 9, 2013, Pages 3564-3571

  Terrando, Niccolò ^a   Gómez Galán, Marta ^a   Yang, Ting ^a   Carlström, Mattias ^a   Gustavsson, Daniel ^a   Harding, Ralph E ^b   Lindskog, Maria ^a   Eriksson, Lars I ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Carl Vinson VA Medical Centre   (United States)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Astrocytes; Dementia; Inflammation; Long term potentiation; Resolution

Indexed keywords

ACETYLSALICYLIC ACID; INTERLEUKIN 6; LIPID; RESOLVIN D1; SUPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; COGNITIVE DEFECT; CONTROLLED STUDY; GLIA; HIPPOCAMPUS; INNATE IMMUNITY; MALE; MEMORY DISORDER; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PERITONEUM MACROPHAGE; POSTOPERATIVE COMPLICATION; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; TIBIA FRACTURE;

ASTROCYTES; DEMENTIA; INFLAMMATION; LONG-TERM POTENTIATION; RESOLUTION;

ANIMALS; ASPIRIN; BRAIN; COGNITION; DOCOSAHEXAENOIC ACIDS; ELECTROPHYSIOLOGY; IMMUNOHISTOCHEMISTRY; LOCOMOTION; LONG-TERM POTENTIATION; MACROPHAGES, PERITONEAL; MALE; MICE; POSTOPERATIVE COMPLICATIONS; SUPEROXIDES;

EID: 84883366706     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-230276     Document Type: Article

References (41)

1. Nathan, C. (2002) Points of control in inflammation. Nature 420, 846-852
2. Serhan, C. N., and Savill, J. (2005) Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6, 1191-1197
3. Serhan, C. N., Brain, S. D., Buckley, C. D., Gilroy, D. W., Haslett, C., O'Neill, L. A., Perretti, M., Rossi, A. G., and Wallace, J. L. (2007) Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21, 325-332
4. Schwab, J. M., Chiang, N., Arita, M., and Serhan, C. N. (2007) Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447, 869-874
5. Perry, V. H., Newman, T. A., and Cunningham, C. (2003) The impact of systemic infection on the progression of neurodegenerative disease. Nat. Rev. Neurosci. 4, 103-112
6. Fong, T. G., Tulebaev, S. R., and Inouye, S. K. (2009) Delirium in elderly adults: diagnosis, prevention and treatment. Nat. Rev. Neurol. 5, 210-220
7. Saczynski, J. S., Marcantonio, E. R., Quach, L., Fong, T. G., Gross, A., Inouye, S. K., and Jones, R. N. (2012) Cognitive trajectories after postoperative delirium. N. Engl. J. Med. 367, 30-39
8. Moller, J. T., Cluitmans, P., Rasmussen, L. S., Houx, P., Rasmussen, H., Canet, J., Rabbitt, P., Jolles, J., Larsen, K., Hanning, C. D., Langeron, O., Johnson, T., Lauven, P. M., Kristensen, P. A., Biedler, A., van Beem, H., Fraidakis, O., Silverstein, J. H., Beneken, J. E., and Gravenstein, J. S. (1998) Long-term postoperative cognitive dysfunction in the elderly ISPOCD1 study. ISPOCD investigators. International Study of Post-Operative Cognitive Dysfunction. Lancet 351, 857-861
9. Terrando, N., Brzezinski, M., Degos, V., Eriksson, L. I., Kramer, J. H., Leung, J. M., Miller, B. L., Seeley, W. W., Vacas, S., Weiner, M. W., Yaffe, K., Young, W. L., Xie, Z., and Maze, M. (2011) Perioperative cognitive decline in the aging population. Mayo Clin. Proc. 86, 885-893
10. Terrando, N., Monaco, C., Ma, D., Foxwell, B. M., Feldmann, M., and Maze, M. (2010) Tumor necrosis factor-alpha triggers a cytokine cascade yielding postoperative cognitive decline. Proc. Natl. Acad. Sci. U. S. A. 107, 20518-20522
11. Cibelli, M., Fidalgo, A. R., Terrando, N., Ma, D., Monaco, C., Feldmann, M., Takata, M., Lever, I. J., Nanchahal, J., Fanselow, M. S., and Maze, M. (2010) Role of interleukin-1β in postoperative cognitive dysfunction. Ann. Neurol. 68, 360-368
12. Terrando, N., Eriksson, L. I., Ryu, J. K., Yang, T., Monaco, C., Feldmann, M., Jonsson Fagerlund, M., Charo, I. F., Akassoglou, K., and Maze, M. (2011) Resolving postoperative neuroinflammation and cognitive decline. Ann. Neurol. 70, 986-995
13. Serhan, C. N., Hong, S., Gronert, K., Colgan, S. P., Devchand, P. R., Mirick, G., and Moussignac, R. L. (2002) Resolvins: a family of bioactive products of α-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J. Exp. Med. 196, 1025-1037
14. Sun, Y. P., Oh, S. F., Uddin, J., Yang, R., Gotlinger, K., Campbell, E., Colgan, S. P., Petasis, N. A., and Serhan, C. N. (2007) Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J. Biol. Chem. 282, 9323-9334
15. Serhan, C. N. (2010) Novel lipid mediators and resolution mechanisms in acute inflammation: to resolve or not? Am. J. Pathol. 177, 1576-1591
16. Carlstrom, M., Brown, R. D., Yang, T., Hezel, M., Larsson, E., Scheffer, P. G., Teerlink, T., Lundberg, J. O., and Persson, A. E. (2013) l-Arginine or tempol supplementation improves renal and cardiovascular function in rats with reduced renal mass and chronic high salt intake. Acta Physiol. (Oxf.) 207, 732-741
17. Qin, L., Liu, Y., Wang, T., Wei, S. J., Block, M. L., Wilson, B., Liu, B., and Hong, J. S. (2004) NADPH oxidase mediates lipopolysaccharide- induced neurotoxicity and proinflammatory gene expression in activated microglia. J. Biol. Chem. 279, 1415-1421
18. Hickey, W. F. (1991) Migration of hematogenous cells through the blood-brain barrier and the initiation of CNS inflammation. Brain Pathol. 1, 97-105
19. Ransohoff, R. M., and Brown, M. A. (2012) Innate immunity in the central nervous system. J. Clin. Invest. 122, 1164-1171
20. Kim, J. J., and Fanselow, M. S. (1992) Modality-specific retrograde amnesia of fear. Science 256, 675-677
21. Tang, J. X., Mardini, F., Janik, L. S., Garrity, S. T., Li, R. Q., Bachlani, G., Eckenhoff, R. G., and Eckenhoff, M. F. (2013) Modulation of murine Alzheimer pathogenesis and behavior by surgery. Ann. Surg. 257, 439-448.
22. Chen, J., Buchanan, J. B., Sparkman, N. L., Godbout, J. P., Freund, G. G., and Johnson, R. W. (2008) Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system. Brain Behav. Immun. 22, 301-311
23. Sofroniew, M. V. (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 32, 638-647
24. Ben Menachem-Zidon, O., Avital, A., Ben-Menahem, Y., Goshen, I., Kreisel, T., Shmueli, E. M., Segal, M., Ben Hur, T., and Yirmiya, R. (2011) Astrocytes support hippocampal-dependent memory and long-term potentiation via interleukin-1 signaling. Brain Behav. Immun. 25, 1008-1016
25. Gomez-Galan, M., De Bundel, D., Van Eeckhaut, A., Smolders, I., and Lindskog, M. (2013) Dysfunctional astrocytic regulation of glutamate transmission in a rat model of depression. Mol. Psychiatry 18, 582-594
26. Perea, G., Navarrete, M., and Araque, A. (2009) Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 32, 421-431
27. Halassa, M. M., and Haydon, P. G. (2010) Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 72, 335-355
28. Henneberger, C., Papouin, T., Oliet, S. H., and Rusakov, D. A. (2010) Long-term potentiation depends on release of d-serine from astrocytes. Nature 463, 232-236
29. 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
30. Serhan, C. N. (2007) Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu. Rev. Immunol. 25, 101-137
31. Barrientos, R. M., Hein, A. M., Frank, M. G., Watkins, L. R., and Maier, S. F. (2012) Intracisternal interleukin-1 receptor antagonist prevents postoperative cognitive decline and neuroinflammatory response in aged rats. J. Neurosci. 32, 14641-14648
32. Schneider, H., Pitossi, F., Balschun, D., Wagner, A., del Rey, A., and Besedovsky, H. O. (1998) A neuromodulatory role of interleukin-1β in the hippocampus. Proc. Natl. Acad. Sci. U. S. A. 95, 7778-7783
33. Zhang, M. J., and Spite, M. (2012) Resolvins: anti-inflammatory and proresolving mediators derived from α-3 polyunsaturated fatty acids. Annu. Rev. Nutr. 32, 203-227
34. Xu, Z. Z., Zhang, L., Liu, T., Park, J. Y., Berta, T., Yang, R., Serhan, C. N., and Ji, R. R. (2010) Resolvins RvE1 and RvD1 attenuate inflammatory pain via central and peripheral actions. Nat. Med. 16, 592-597
35. Chiang, N., Fredman, G., Backhed, 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
36. Psychogios, N., Hau, D. D., Peng, J., Guo, A. C., Mandal, R., Bouatra, S., Sinelnikov, I., Krishnamurthy, R., Eisner, R., Gautam, B., Young, N., Xia, J., Knox, C., Dong, E., Huang, P., Hollander, Z., Pedersen, T. L., Smith, S. R., Bamforth, F., Greiner, R., McManus, B., Newman, J. W., Goodfriend, T., and Wishart, D. S. (2011) The human serum metabolome. PLoS One 6, e16957
37. Mas, E., Croft, K. D., Zahra, P., Barden, A., and Mori, T. A. (2012) Resolvins D1, D2, and other mediators of self-limited resolution of inflammation in human blood following n-3 fatty acid supplementation. Clin. Chem. 58, 1476-1484
38. Liu, G., Fiala, M., Mizwicki, M. T., Sayre, J., Magpantay, L., Siani, A., Mahanian, M., Chattopadhyay, M., La Cava, A., and Wiedau-Pazos, M. (2012) Neuronal phagocytosis by inflammatory macrophages in ALS spinal cord: inhibition of inflammation by resolvin D1. Am. J. Neurodegener. Dis. 1, 60-74
39. Haworth, O., Cernadas, M., Yang, R., Serhan, C. N., and Levy, B. D. (2008) Resolvin E1 regulates interleukin 23, interferon- and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat. Immunol. 9, 873-879
40. Serhan, C. N., Dalli, J., Karamnov, S., Choi, A., Park, C. K., Xu, Z. Z., Ji, R. R., Zhu, M., and Petasis, N. A. (2012) Macrophage proresolving mediator maresin 1 stimulates tissue regeneration and controls pain. FASEB J. 26, 1755-1765
41. Norling, L. V., Spite, M., Yang, R., Flower, R. J., Perretti, M., and Serhan, C. N. (2011) Cutting edge: Humanized nano-proresolving medicines mimic inflammation-resolution and enhance wound healing. J. Immunol. 186, 5543-5547