Docosahexaenoic acid, but not eicosapentaenoic acid, reduces the early inflammatory response following compression spinal cord injury in the rat

Journal of Neurochemistry

Volumn 121, Issue 5, 2012, Pages 738-750

  Hall, Jodie C E ^a   Priestley, John V ^b   Perry, V Hugh ^c   Michael Titus, Adina T ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

docosahexaenoic acid; eicosapentaenoic acid; inflammation; neutrophil; spinal cord injury

Indexed keywords

C REACTIVE PROTEIN; CHEMOKINE; DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHEMOKINESIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; FEMALE; HISTOPATHOLOGY; IMMUNOREACTIVITY; INFLAMMATION; LAMINECTOMY; NEUROPROTECTION; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; RAT; SPINAL CORD COMPRESSION; SPINAL CORD INJURY; SPINAL CORD VENTRAL HORN;

RATTUS;

EID: 84860517355     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07726.x     Document Type: Article

References (89)

1. Bailes J., and, Mills J., (2010) Docosahexaenoic acid reduces traumatic axonal injury in a rodent head injury model. J. Neurotrauma 27, 1617-1624.
2. Bao F., Chen Y., Dekaban G., and, Weaver L., (2004) Early anti-inflammatory treatment reduces lipid peroxidation and protein nitration after spinal cord injury in rats. J. Neurochem. 88, 1335-1344. (Pubitemid 38366908)
3. Bao F., Dekaban G., and, Weaver L., (2005) Anti-CD11d antibody treatment reduces free radical formation and cell death in the injured spinal cord of rats. J. Neurochem. 94, 1361-1373. (Pubitemid 41232591)
4. Belayev L., Marcheselli V., Khoutorova L., Rodriguez de Turco E., Busto R., Ginsberg M., and, Bazan N., (2005) Docosahexaenoic acid complexed to albumin elicits high-grade ischemic neuroprotection. Stroke 36, 118-123. (Pubitemid 40054186)
5. Bousquet M., Saint-Pierre M., Julien C., Salem N.J., Cicchetti F., and, Calon F., (2008) Beneficial effects of dietary omega-3 polyunsaturated fatty acid on toxin-induced neuronal degeneration in an animal model of Parkinson's disease. FASEB J. 22, 1213-1225. (Pubitemid 351519975)
6. Burdge G., and, Calder P., (2005) Conversion of alpha-linolenic acid to longer-chain polyunsaturated fatty acids in human adults. Reprod. Nutr. Dev. 5, 581-597. (Pubitemid 41511883)
7. Calder P., (2003) N-3 polyunsaturated fatty acids and inflammation: from molecular biology to the clinic. Lipids 38, 343-352. (Pubitemid 36724290)
8. Calder P., (2010) The 2008 ESPEN Sir David Cuthbertson Lecture: Fatty acids and inflammation - from the membrane to the nucleus and from the laboratory bench to the clinic. Clin. Nutr. 29, 5-12.
9. Campbell S., Hughes P., Iredale J., Wilcockson D., Waters S., Docagne F., Perry V., and, Anthony D., (2003) CINC-1 is an acute-phase protein induced by focal brain injury causing leukocyte mobilization and liver injury. FASEB J. 17, 1168-1170.
10. Campbell S., Perry V., Pitossi F., Butchart A., Chertoff M., Waters S., Dempster R., and, Anthony D., (2005) Central nervous system injury triggers hepatic CC and CXC chemokine expression that is associated with leukocyte mobilization and recruitment to both the central nervous system and the liver. Am. J. Pathol. 166, 1487-1497. (Pubitemid 40586518)
11. Carlson S., Parrish M., Springer J., Doty K., and, Dossett L., (1998) Acute inflammatory response in spinal cord following impact injury. Exp. Neurol. 151, 77-88. (Pubitemid 28223857)
12. Cuzzocrea S., Bruscoli S., Mazzon E., Crisafulli C., Donato V., Di Paola R., Velardi E., Esposito E., Nocentini G., and, Riccardi C., (2008) Peroxisome proliferator-activated receptor-alpha contributes to the anti-inflammatory activity of glucocorticoids. Mol. Pharmacol. 73, 323-337. (Pubitemid 351181185)
13. Davis A., Campbell S., Wilainam P., and, Anthony D., (2005) Post-conditioning with lipopolysaccharide reduces the inflammatory infiltrate to the injured brain and spinal cord: a potential neuroprotective treatment. Eur. J. Neurosci. 22, 2441-2450. (Pubitemid 41758987)
14. De Caterina R., Cybulsky M. I., Clinton S. K., Gimbrone M. A. Jr, and, Libby P., (1994) The omega-3 fatty acid docosahexaenoate reduces cytokine-induced expression of proatherogenic and proinflammatory proteins in human endothelial cells. Arterioscler Thromb. 11, 1829-1836.
15. De Caterina R., and, Massaro M., (2005) Omega-3 fatty acids and the regulation of expression of endothelial pro-atherogenic and pro-inflammatory genes. J. Membr. Biol. 206, 103-116. (Pubitemid 43199144)
16. De Caterina R., Liao J. K., and, Libby P., (2000) Fatty acid modulation of endothelial activation. Am. J. Clin. Nutr. 71 (Suppl. 1), 213S-223S. (Pubitemid 30046119)
17. De Deckere E., (1999) Possible beneficial effect of fish and fish n-3 polyunsaturated fatty acids in breast and colorectal cancer. Eur. J. Cancer Prev. 8, 213-221.
18. De Smedt-Peyrusse V., Sargueil F., Moranis A., Harizi H., Mongrand S., and, Layé S., (2008) Docosahexaenoic acid prevents lipopolysaccharide- induced cytokine production in microglial cells by inhibiting lipopolysaccharide receptor presentation but not its membrane subdomain localization. J. Neurochem. 105, 296-307. (Pubitemid 351490003)
19. Demediuk P., Saunders R., Anderson D., Means E., and, Horrocks L., (1985a) Membrane lipid changes in laminectomized and traumatized cat spinal cord. Proc. Natl Acad Sci. USA 82, 7071-7075. (Pubitemid 16209694)
20. Demediuk P., Saunders R., Clendenon N., Means E., Anderson D., and, Horrocks L., (1985b) Changes in lipid metabolism in traumatized spinal cord. Prog. Brain Res. 63, 211-226.
21. Demediuk P., Daly M., and, Faden A., (1989) Changes in free fatty acids, phospholipids, and cholesterol following impact injury to the rat spinal cord. J. Neurosci. Res. 23, 95-106. (Pubitemid 19167328)
22. Ding G., Cheng L., Qin Q., Frontin S., and, Yang Q., (2006) PPARdelta modulates lipopolysaccharide-induced TNFalpha inflammation signaling in cultured cardiomyocytes. J. Mol. Cell. Cardiol. 40, 821-828. (Pubitemid 43817042)
23. Drew P., Storer P., Xu J., and, Chavis J., (2005) Hormone regulation of microglial cell activation: relevance to multiple sclerosis. Brain Res. Brain Res. Rev. 48, 322-327. (Pubitemid 40585762)
24. Dusart I., and, Schwab M., (1994) Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur. J. Neurosci. 6, 712-724. (Pubitemid 24143919)
25. Farooqui A., Horrocks L., and, Farooqui T., (2007) Modulation of inflammation in brain: a matter of fat. J. Neurochem. 101, 577-599. (Pubitemid 46633316)
26. Farzaneh-Far R., Harris W., Garg S., Na B., and, Whooley M., (2009) Inverse association of erythrocyte n-3 fatty acid levels with inflammatory biomarkers in patients with stable coronary artery disease: The Heart and Soul Study. Atherosclerosis 205, 538-43.
27. Fleming J., Bao F., Chen Y., Hamilton E., Relton J., and, Weaver L., (2008) Alpha4beta1 integrin blockade after spinal cord injury decreases damage and improves neurological function. Exp. Neurol. 214, 147-159.
28. Fleming J., Bao F., Chen Y., Hamilton E., Gonzalez-Lara L., Foster P., and, Weaver L., (2009) Timing and duration of anti-alpha4beta1 integrin treatment after spinal cord injury: effect on therapeutic efficacy. J. Neurosurg. Spine 11, 575-587.
29. Genovese T., Mazzon E., Rossi A., Di Paola R., Cannavo G., Muia C., Bramanti P., Sautebin L., and, Cuzzocrea S., (2005) Involvement of 5-lipoxygenase in spinal cord injury. J. Neuroimmunol. 166, 55-64. (Pubitemid 41074657)
30. Genovese T., Rossi A., Mazzon E., Di Paola R., Muia C., Caminiti R., Bramanti P., Sautebin L., and, Cuzzocre S., (2008) Effects of zileuton and montelukast in mouse experimental spinal cord injury. Br. J. Pharmacol. 153, 568-582. (Pubitemid 351199011)
31. Gibson A., Buchholz A., Martin Ginis K.,; SHAPE-SCI Research Group (2008) C-Reactive protein in adults with chronic spinal cord injury: increased chronic inflammation in tetraplegia vs paraplegia. Spinal Cord. 46, 616-21.
32. GorjÃo R., Verlengia R., Lima T. M., Soriano F. G., Boaventura M. F., Kanunfre C. C., et al. (2006) Effect of docosahexaenoic acid-rich fish oil supplementation on human leukocyte function. Clin. Nutr. 24, 923-938. (Pubitemid 44752719)
33. Gorjão R., Azevedo-Martins A. K., Rodrigues H. G., Abdulkader F., Arcisio-Miranda M., Procopio J., and, Curi R., (2009) Comparative effects of DHA and EPA on cell function. Pharmacol. Ther. 122, 56-64.
34. Gris D., Hamilton E., and, Weaver L., (2008) The systemic inflammatory response after spinal cord injury damages lungs and kidneys. Exp. Neurol. 211, 259-270.
35. Healy D., Wallace F., Miles E., Calder P., and, Newsholm P., (2000) Effect of low-to-moderate amounts of dietary fish oil on neutrophil lipid composition and function. Lipids 35, 763-768. (Pubitemid 30624541)
36. Heurteaux C., Guy N., Laigle C., et al. (2004) TREK-1, a K+ channel involved in neuroprotection and general anesthesia. EMBO J. 23, 2684-2695. (Pubitemid 38988239)
37. Hong S., Gronert K., Devchand P. R., Moussignac R. L., and, Serhan C,. (2003) Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. J. Biol. Chem. 278, 14677-14687. (Pubitemid 36799790)
38. Huang W., George K., Ibba V., Liu M., Averill S., Quartu M., Hamlyn P., and, Priestley J., (2007a) The characteristics of neuronal injury in a static compression model of spinal cord injury in adult rats. Eur. J. Neurosci. 25, 362-372.
39. Huang W., King V., Curran O., Dyall S., Ward R., Lal N., Priestley J., and, Michael-Titus A., (2007b) A combination of intravenous and dietary docosahexaenoic acid significantly improves outcome after spinal cord injury. Brain 130, 3004-3019. (Pubitemid 350033967)
40. Ito Y., Sugimoto Y., Tomioka M., Kai N., and, Tanaka M,. (2009) Does high dose methylprednisolone sodium succinate really improve neurological status in patient with acute cervical cord injury?: a prospective study about neurological recovery and early complications. Spine (Phila Pa 1976) 34, 2121-2124.
41. Kew S., Mesa M. D., Tricon S., Buckley R., Minihane A. M., and, Yaqoob P., (2004) Effects of oils rich in eicosapentaenoic and docosahexaenoic acids on immune cell composition and function in healthy humans. Am. J. Clin. Nutr. 79, 674-681. (Pubitemid 41103914)
42. Kigerl K. A., Gensel J. C., Ankeny D. P., Alexander J. K., Donnelly D. J., and, Popovich P. G., (2009) Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 43, 13435-13444.
43. King V., Huang W., Dyall S., Curran O., Priestley J., and, Michael-Titus A., (2006) Omega-3 fatty acids improve recovery, whereas omega-6 fatty acids worsen outcome, after spinal cord injury in the adult rat. J. Neurosci. 26, 4672-4680. (Pubitemid 44315368)
44. Klein-Platat C., Drai J., Oujaa M., Schlienger J.L., and, Simon C., (2005) Plasma fatty acid composition is associated with the metabolic syndrome and low-grade inflammation in overweight adolescents. Am. J. Clin. Nutr. 82, 1178-1184. (Pubitemid 43779715)
45. Lauritzen I., Blondeau N., Heurteaux C., Widmann C., Romey G., and, Lazdunski M., (2000) Polyunsaturated fatty acids are potent neuroprotectors. EMBO J. 19, 1784-1793. (Pubitemid 30204390)
46. Lee T., Hoover R., Williams J., Sperling R., Ravalese J.R., Spur B., Robinson D., Corey E., Lewis R., and, Austen K., (1985) Effect of dietary enrichment with eicosapentaenoic and docosahexaenoic acids on in vitro neutrophil and monocyte leukotriene generation and neutrophil function. N. Engl. J. Med. 312, 1217-1224. (Pubitemid 15009155)
47. Lee Y., Shih K., Bao P., Ghirnikar R., and, Eng L., (2000) Cytokine chemokine expression in contused rat spinal cord. Neurochem. Int. 36, 417-425. (Pubitemid 30101583)
48. Lim S., Huang W., Hall J., Ward R., Priestley J., and, Michael-Titus A., (2010) The acute administration of eicosapentaenoic acid is neuroprotective after spinal cord compression injury in rats. Prostaglandins Leukot. Essent. Fatty Acids 83, 193-201.
49. Lõpez-Vales R., Redensek A., Skinner T., Rathore K., Ghasemlou N., Wojewodka G., Desanctis J., Radzioch D., and, David S., (2010) Fenretinide promotes functional recovery and tissue protection after spinal cord contusion injury in mice. J. Neurosci. 30, 3220-3226.
50. Madsen T., Christensen J., Blom M., and, Schmidt E., (2003) The effect of dietary n-3 fatty acids on serum concentrations of C-reactive protein: a dose-response study. Br. J. Nutr. 89, 517-522. (Pubitemid 36582122)
51. Makhoul Z., Kristal A., Gulati R., et al. (2011) Associations of obesity with triglycerides and C-reactive protein are attenuated in adults with high red blood cell eicosapentaenoic and docosahexaenoic acids. Eur. J. Clin. Nutr. 65, 808-817.
52. Manns P., McCubbin J., and, Williams D,. (2005) Fitness, inflammation, and the metabolic syndrome in men with paraplegia. Arch. Phys. Med. Rehabil. 86, 1176-1181. (Pubitemid 40797772)
53. Marcheselli V., Hong S., Lukiw W., et al. (2003) Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression. J. Biol. Chem. 278, 43807-43817. (Pubitemid 37346009)
54. Matsumoto T., Tamaki T., Kawakami M., Yoshida M., Ando M., and, Yamada H,. (2001) Early complications of high-dose methylprednisolone sodium succinate treatment in the follow-up of acute cervical spinal cord injury. Spine (Phila Pa 1976) 26, 426-430. (Pubitemid 32184858)
55. Matzinger P., (1994) Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12, 991-1045. (Pubitemid 24140436)
56. Mey J,. (2006) New therapeutic target for CNS injury? The role of retinoic acid signaling after nerve lesions. J. Neurobiol. 66, 757-779. (Pubitemid 43939198)
57. Mills J., Bailes J., Sedney C., Hutchins H., and, Sears B., (2011) Omega-3 fatty acid supplementation and reduction of traumatic axonal injury in a rodent head injury model. J. Neurosurg. 114, 77-84.
58. Mukherjee P., Marcheselli V., Serhan C., and, Bazan N., (2004) Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc. Natl Acad. Sci. USA 101, 8491-8496. (Pubitemid 38736602)
59. Murphy E., Behrmann D., Bates C., and, Horrocks L., (1994) Lipid alterations following impact spinal cord injury in the rat. Mol. Chem. Neuropathol. 23, 13-26.
60. Park E., Park S., Joe E., and, Jou I., (2003) 15d-PGJ2 and rosiglitazone suppress Janus kinase-STAT inflammatory signaling through induction of suppressor of cytokine signaling 1 (SOCS1) and SOCS3 in glia. J. Biol. Chem. 278, 14747-14752. (Pubitemid 36799798)
61. Paterniti I., Esposito E., Mazzon E., Galuppo M., Di Paola R., Bramanti P., Kapoor A., Thiemermann C., and, Cuzzocrea S,. (2010) Evidence for the role of peroxisome proliferator-activated receptor-beta/delta in the development of spinal cord injury. J. Pharmacol. Exp. Ther. 2, 465-477.
62. Popovich P., Wei P., and, Stokes B., (1997) Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 377, 443-464. (Pubitemid 27016650)
63. Popovich P., Guan Z., Wei P., Huitinga I., van Rooijen N., and, Stokes B., (1999) Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp. Neurol. 158, 351-365. (Pubitemid 29382826)
64. Profyris C., Cheema S., Zang D., Azari M., Boyle K., and, Petratos S., (2004) Degenerative and regenerative mechanisms governing spinal cord injury. Neurobiol. Dis. 15, 415-436. (Pubitemid 38429958)
65. Raederstorff D., Pantze M., Bachmann H., and, Moser U., (1996) Anti-inflammatory properties of docosahexaenoic and eicosapentaenoic acids in phorbol-ester-induced mouse ear inflammation. Int. Arch. Allergy Immunol. 111, 284-290. (Pubitemid 26345387)
66. Rapoport S., Rao J., and, Igarashi M., (2007) Brain metabolism of nutritionally essential polyunsaturated fatty acids depends on both the diet and the liver. Prostaglandins Leukot. Essent. Fatty Acids 77, 251-261. (Pubitemid 350214520)
67. Schnell L., Fearn S., Klassen H., Schwab M., and, Perry V., (1999) Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur. J. Neurosci. 11, 3648-3658. (Pubitemid 29484261)
68. Serhan C., and, Savill J., (2005) Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6, 1191-1197. (Pubitemid 43045627)
69. Serhan C., Gotlinger K., Hong S., and, Arita M., (2004) Resolvins, docosatrienes, and neuroprotectins, novel omega-3-derived mediators, and their aspirin-triggered endogenous epimers: an overview of their protective roles in catabasis. Prostaglandins Other Lipid Mediat. 73, 155-172. (Pubitemid 38757795)
70. Serhan C., Gotlinger K., Hong S., Lu Y., Siegelman J., Baer T., Yang R., Colgan S., and, Petasis N., (2006) Anti-inflammatory actions of neuroprotectin D1/protectin D1 and its natural stereoisomers: assignments of dihydroxy-containing docosatrienes. J. Immunol. 176, 1848-1859. (Pubitemid 43134330)
71. Serhan C., Chiang N., and, Van Dyke T., (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8, 349-361. (Pubitemid 351595216)
72. Sierra S., Lara-Villoslada F., Comalada M., Olivares M., and, Xaus J., (2008) Dietary eicosapentaenoic acid and docosahexaenoic acid equally incorporate as decosahexaenoic acid but differ in inflammatory effects. Nutrition 24, 245-254. (Pubitemid 351179962)
73. Smith W., Garavito R., and, DeWitt D., (1996) Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J. Biol. Chem. 271, 33157-33160. (Pubitemid 27010118)
74. Sperling R., Benincaso A., Knoell C., Larkin J., Austen K., and, Robinson D., (1993) Dietary omega-3 polyunsaturated fatty acids inhibit phosphoinositide formation and chemotaxis in neutrophils. J. Clin. Invest. 91, 651-660. (Pubitemid 23064151)
75. Spite M., Norling L., Summers L., Yang R., Cooper D., Petasis N., Flower R., Perretti M., and, Serhan C., (2009) Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature 461, 1287-1291.
76. Streit W., Semple-Rowland S., Hurley S., Miller R., Popovich P., and, Stokes B., (1998) Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp. Neurol. 152, 74-87. (Pubitemid 28366968)
77. Taoka Y., Okajima K., Uchiba M., Murakami K., Kushimoto S., Johno M., Naruo M., Okabe H., and, Takatsuki K., (1997) Role of neutrophils in spinal cord injury in the rat. Neuroscience 79, 1177-1182. (Pubitemid 27293767)
78. Thompson D., Pepys M., and, Wood S., (1999) The physiological structure of human C-reactive protein and its complex with phosphocholine. Structure 7, 169-177. (Pubitemid 29159702)
79. Tomobe Y., Morizawa K., Tsuchida M., Hibino H., Nakano Y., and, Tanaka Y., (2000) Dietary docosahexaenoic acid suppresses inflammation and immunoresponses in contact hypersensitivity reaction in mice. Lipids 35, 61-69. (Pubitemid 30084631)
80. Verlengia R., Gorjão R., Kanunfre C. C., Bordin S., De Lima T. M., Martins E. F., Newsholme P., and, Curi R., (2004) Effects of EPA and DHA on proliferation, cytokine production, and gene expression in Raji cells. Lipid 39, 857-864. (Pubitemid 40030378)
81. Wang C., Olschowka J., and, Wrathall J., (1997) Increase of interleukin-1beta mRNA and protein in the spinal cord following experimental traumatic injury in the rat. Brain Res. 759, 190-196. (Pubitemid 27286694)
82. Wang C., Harris W., Chung M., Lichtenstein A., Balk E., Kupelnick B., Jordan H., and, Lau J., (2006) n-3 Fatty acids from fish or fish-oil supplements, but not alpha-linolenic acid, benefit cardiovascular disease outcomes in primary- and secondary-prevention studies: a systematic review. Am. J. Clin. Nutr. 84, 5-17. (Pubitemid 44699166)
83. Ward R., Huang W., Curran O., Priestley J., and, Michael-Titus A,. (2010) Docosahexaenoic acid prevents white matter damage following spinal cord injury. J. Neurotrauma. 10, 1769-1780.
84. Welch J., Ricote M., Akiyama T., Gonzalez F., and, Glass C., (2003) PPARgamma and PPARdelta negatively regulate specific subsets of lipopolysaccharide and IFN-gamma target genes in macrophages. Proc. Natl Acad. Sci. USA 100, 6712-6717. (Pubitemid 36666645)
85. Xu J., Hsu C. Y., Liu T. H., Hogan E. L., Perot E., and, Tai H., (1990) Leukotriene B4 release and polymorphonuclear cell infiltration in spinal cord injury. J. Neurochem. 55, 907-912.
86. Yakovlev A., and, Faden A., (1994) Sequential expression of c-fos protooncogene, TNF-alpha, and dynorphin genes in spinal cord following experimental traumatic injury. Mol. Chem. Neuropathol. 23, 179-190.
87. Yoshikawa T., Shimano H., Yahagi N., et al. (2002) Polyunsaturated fatty acids suppress sterol regulatory element-binding protein 1c promoter activity by inhibition of liver X receptor (LXR) binding to LXR response elements. J. Biol. Chem. 277, 1705-1711. (Pubitemid 34968740)
88. Zhang Q., Raoof M., Chen Y., Sumi Y., Sursal T., Junger W., Brohi K., Itagaki K., and, Hauser C., (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464, 104-107.
89. Zhou L., Vessby B., and, Nilsson A., (2002) Quantitative role of plasma free fatty acids in the supply of arachidonic acid to extrahepatic tissues in rats. J. Nutr. 132, 2626-2631. (Pubitemid 35013246)