Eicosanoid modulation by the short-chain fatty acid n-butyrate in human monocytes

Immunology

Volumn 139, Issue 3, 2013, Pages 395-405

  Kovarik, Johannes J ^a,b   Hölzl, Markus A ^c   Hofer, Johannes ^a   Waidhofer Söllner, Petra ^a   Sobanov, Yury ^d   Koeffel, René ^a   Saemann, Marcus D ^b   Mechtcheriakova, Diana ^d   Zlabinger, Gerhard J ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c CHILDREN'S CANCER RESEARCH INSTITUTE   (Austria)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Eicosanoids; Gene regulation; Monocytes; n butyrate

Indexed keywords

BUTYRIC ACID; ICOSANOID; LIPOPOLYSACCHARIDE; RNA; THROMBOXANE B2; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOMODULATION; MONOCYTE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; WESTERN BLOTTING;

BUTYRATES; CYCLOOXYGENASE 2; DINOPROSTONE; EICOSANOIDS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; LEUKOTRIENE B4; LIPOPOLYSACCHARIDES; MONOCYTES; REAL-TIME POLYMERASE CHAIN REACTION; THROMBOXANE B2; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; UP-REGULATION;

EID: 84879202714     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12089     Document Type: Article

References (66)

1. Gill N, Wlodarska M, Finlay BB. The future of mucosal immunology: studying an integrated system-wide organ. Nat Immunol 2010; 11:558-60.
2. Roediger WE. Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 1982; 83:424-9.
3. Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev 1990; 70:567-90.
4. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther 2008; 27:104-19.
5. Scheppach W, Weiler F. The butyrate story: old wine in new bottles? Curr Opin Clin Nutr Metab Care 2004; 7:563-7.
6. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 2001; 81:1031-64.
7. Crew TE, Elder DJ, Paraskeva C. A cyclooxygenase-2 (COX-2) selective non-steroidal anti-inflammatory drug enhances the growth inhibitory effect of butyrate in colorectal carcinoma cells expressing COX-2 protein: regulation of COX-2 by butyrate. Carcinogenesis 2000; 21:69-77.
8. Saemann MD, Böhmig GA, Österreicher CH et al. Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J 2000; 14:2380-2.
9. Saemann MD, Parolini O, Bohmig GA et al. Bacterial metabolite interference with maturation of human monocyte-derived dendritic cells. J Leukoc Biol 2002; 71:238-46.
10. Harizi H, Gualde N. The impact of eicosanoids on the crosstalk between innate and adaptive immunity: the key roles of dendritic cells. Tissue Antigens 2005; 65:507-14.
11. Wang D, Dubois RN. Eicosanoids and cancer. Nat Rev Cancer 2010; 10:181-93.
12. Harris SG, Padilla J, Koumas L, Ray D, Phipps RP. Prostaglandins as modulators of immunity. Trends Immunol 2002; 23:144-50.
13. Lee IY, Cho W, Kim J, Park CS, Choe J. Human follicular dendritic cells interact with T cells via expression and regulation of cyclooxygenases and prostaglandin E and I synthases. J Immunol 2008; 180:1390-7.
14. Mechtcheriakova D, Wlachos A, Sobanov J et al. Sphingosine 1-phosphate phosphatase 2 is induced during inflammatory responses. Cell Signal 2007; 19:748-60.
15. Saemann MD, Weichhart T, Zeyda M et al. Tamm-Horsfall glycoprotein links innate immune cell activation with adaptive immunity via a Toll-like receptor-4-dependent mechanism. J Clin Invest 2005; 115:468-75.
16. Adderley SR, Fitzgerald DJ. Oxidative damage of cardiomyocytes is limited by extracellular regulated kinases 1/2-mediated induction of cyclooxygenase-2. J Biol Chem 1999; 274:5038-46.
17. Monick MM, Powers LS, Barrett CW et al. Constitutive ERK MAPK activity regulates macrophage ATP production and mitochondrial integrity. J Immunol 2008; 180:7485-96.
18. Pouliot M, Gilbert C, Borgeat P et al. Expression and activity of prostaglandin endoperoxide synthase-2 in agonist-activated human neutrophils. FASEB J 1998; 12:1109-23.
19. Crofford LJ, Tan B, McCarthy CJ, Hla T. Involvement of nuclear factor κB in the regulation of cyclooxygenase-2 expression by interleukin-1 in rheumatoid synoviocytes. Arthritis Rheum 1997; 40:226-36.
20. Thomas B, Berenbaum F, Humbert L, Bian H, Bereziat G, Crofford L, Olivier JL. Critical role of C/EBPδ and C/EBPβ factors in the stimulation of the cyclooxygenase-2 gene transcription by interleukin-1β in articular chondrocytes. Eur J Biochem 2000; 267:6798-809.
21. Wadleigh DJ, Reddy ST, Kopp E, Ghosh S, Herschman HR. Transcriptional activation of the cyclooxygenase-2 gene in endotoxin-treated RAW 264.7 macrophages. J Biol Chem 2000; 275:6259-66.
22. Diakos C, Prieschl EE, Saemann M, Novotny V, Bohmig G, Csonga R, Baumruker T, Zlabinger GJ. Novel mode of interference with nuclear factor of activated T-cells regulation in T-cells by the bacterial metabolite n-butyrate. J Biol Chem 2002; 277:24243-51.
23. 2-terminal kinase activation and cytokine transcription in mast cells. Biochem Biophys Res Commun 2006; 349:863-8.
24. Millard AL, Mertes PM, Ittelet D, Villard F, Jeannesson P, Bernard J. Butyrate affects differentiation, maturation and function of human monocyte-derived dendritic cells and macrophages. Clin Exp Immunol 2002; 130:245-55.
25. Schwab M, Reynders V, Loitsch S, Steinhilber D, Stein J, Schroder O. Involvement of different nuclear hormone receptors in butyrate-mediated inhibition of inducible NF κB signalling. Mol Immunol 2007; 44:3625-32.
26. Alanko J, Riutta A, Vapaatalo H. Effects of catecholamines on eicosanoid synthesis with special reference to prostanoid/leukotriene ratio. Free Radic Biol Med 1992; 13:677-88.
27. Feuerstein G. Autonomic pharmacology of leukotrienes. J Auton Pharmacol 1985; 5:149-68.
28. Harizi H, Corcuff JB, Gualde N. Arachidonic-acid-derived eicosanoids: roles in biology and immunopathology. Trends Mol Med 2008; 14:461-9.
29. Daly K, Shirazi-Beechey SP. Microarray analysis of butyrate regulated genes in colonic epithelial cells. DNA Cell Biol 2006; 25:49-62.
30. Tong X, Yin L, Giardina C. Butyrate suppresses Cox-2 activation in colon cancer cells through HDAC inhibition. Biochem Biophys Res Commun 2004; 317:463-71.
31. Park GY, Joo M, Pedchenko T, Blackwell TS, Christman JW. Regulation of macrophage cyclooxygenase-2 gene expression by modifications of histone H3. Am J Physiol Lung Cell Mol Physiol 2004; 286:L956-62.
32. Iida T, Kawato T, Tanaka H et al. Sodium butyrate induces the production of cyclooxygenases and prostaglandin E in ROS 17/2.8 osteoblastic cells. Arch Oral Biol 2011; 56:678-86.
33. Narumiya S. Prostanoids and inflammation: a new concept arising from receptor knockout mice. J Mol Med (Berl) 2009; 87:1015-22.
34. Scher JU. Pillinger MH. J Investig Med: The anti-inflammatory effects of prostaglandins, 2009.
35. Kalinski P, Hilkens CM, Snijders A, Snijdewint FG, Kapsenberg ML. IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. J Immunol 1997; 159:28-35.
36. + dendritic cells: the levels of IL-12 are determined during the final dendritic cell maturation and are resistant to further modulation. J Immunol 1998; 161:2804-9.
37. Landi A, Babiuk LA, van Drunen Littel-van den Hurk S. Dendritic cells matured by a prostaglandin E2-containing cocktail can produce high levels of IL-12p70 and are more mature and Th1-biased than dendritic cells treated with TNF-α or LPS. Immunobiology 2011; 216:649-62.
38. Rieser C, Bock G, Klocker H, Bartsch G, Thurnher M. Prostaglandin E2 and tumor necrosis factor α cooperate to activate human dendritic cells: synergistic activation of interleukin 12 production. J Exp Med 1997; 186:1603-8.
39. Obermajer N, Muthuswamy R, Lesnock J, Edwards RP, Kalinski P. Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells towards stable myeloid-derived suppressor cells. Blood 2011; 118:5498-505.
40. Yang L, Yamagata N, Yadav R et al. Cancer-associated immunodeficiency and dendritic cell abnormalities mediated by the prostaglandin EP2 receptor. J Clin Investig 2003; 111:727-35.
41. 2: studies with prostaglandin receptor-deficient mice and prostaglandin E-receptor subtype-selective synthetic agonists. Biochem Pharmacol 2001; 61:1153-60.
42. Chinen T, Komai K, Muto G et al. Prostaglandin E2 and SOCS1 have a role in intestinal immune tolerance. Nat Commun 2011; 2:190.
43. 2 that regulate cellular immune responses in the mouse. J Clin Investig 2001; 108:1229-35.
44. Bryn T, Yaqub S, Mahic M, Henjum K, Aandahl EM, Tasken K. LPS-activated monocytes suppress T-cell immune responses and induce FOXP3+ T cells through a COX-2-PGE2-dependent mechanism. Int Immunol 2008; 20:235-45.
45. Wiemer AJ, Hegde S, Gumperz JE, Huttenlocher A. A live imaging cell motility screen identifies prostaglandin E2 as a T cell stop signal antagonist. J Immunol 2011; 187:3663-70.
46. Murn J, Alibert O, Wu N, Tendil S, Gidrol X. Prostaglandin E2 regulates B cell proliferation through a candidate tumor suppressor, Ptger4. J Exp Med 2008; 205:3091-103.
47. Garrone P, Galibert L, Rousset F, Fu SM, Banchereau J. Regulatory effects of prostaglandin E2 on the growth and differentiation of human B lymphocytes activated through their CD40 antigen. J Immunol 1994; 152:4282-90.
48. Brown DM, Warner GL, Ales-Martinez JE, Scott DW, Phipps RP. Prostaglandin E2 induces apoptosis in immature normal and malignant B lymphocytes. Clin Immunol Immunopathol 1992; 63:221-9.
49. Peters-Golden M, Henderson WR Jr. Leukotrienes. N Engl J Med 2007; 357:1841-54.
50. Samuelsson B, Dahlen SE, Lindgren JA, Rouzer CA, Serhan CN. Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. Science 1987; 237:1171-6.
51. Reims A, Redfors S, Sjovall H, Strandvik B. Cysteinyl leukotrienes are secretagogues in atrophic coeliac and in normal duodenal mucosa of children. Scand J Gastroenterol 2005; 40:160-8.
52. Shahbazian A, Heinemann A, Peskar BA, Holzer P. Differential peristaltic motor effects of prostanoid (DP, EP, IP, TP) and leukotriene receptor agonists in the guinea-pig isolated small intestine. Br J Pharmacol 2002; 137:1047-54.
53. Serhan CN, Chiang N, Van Dyke TE. Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 2008; 8:349-61.
54. Sharma JN, Mohammed LA. The role of leukotrienes in the pathophysiology of inflammatory disorders: is there a case for revisiting leukotrienes as therapeutic targets? Inflammopharmacology 2006; 14:10-6.
55. 4 activates MAPK through a Ras-independent but PKCε-dependent pathway in intestinal epithelial cells. J Cell Sci 2002; 115:1883-93.
56. Peters-Golden M, Canetti C, Mancuso P, Coffey MJ. Leukotrienes: underappreciated mediators of innate immune responses. J Immunol 2005; 174:589-94.
57. Bohmig GA, Csmarits B, Cerwenka A, Alaei P, Kovarik J, Zlabinger GJ. Induction of alloantigen-specific hyporesponsiveness in vitro by the short-chain fatty acid N-butyrate. Transplantation 1995; 59:1500-3.
58. Bohmig GA, Krieger PM, Saemann MD, Ullrich R, Karimi H, Wekerle T, Muhlbacher F, Zlabinger GJ. Stable prodrugs of n-butyric acid: suppression of T cell alloresponses in vitro and prolongation of heart allograft survival in a fully allogeneic rat strain combination. Transpl Immunol 1999; 7:221-7.
59. Bohmig GA, Krieger PM, Saemann MD, Wenhardt C, Pohanka E, Zlabinger GJ. n-Butyrate downregulates the stimulatory function of peripheral blood-derived antigen-presenting cells: a potential mechanism for modulating T-cell responses by short-chain fatty acids. Immunology 1997; 92:234-43.
60. Bohmig GA, Wekerle T, Saemann MD, Kovarik J, Zlabinger GJ. Induction of alloantigen-specific hyporesponsiveness in vitro by n-butyrate: antagonistic effect of cyclosporin A. Transpl Int 1996; 9(Suppl 1):S318-22.
61. Kovarik JJ, Tillinger W, Hofer J, Holzl MA, Heinzl H, Saemann MD, Zlabinger GJ. Impaired anti-inflammatory efficacy of n-butyrate in patients with IBD. Eur J Clin Invest 2011; 41:291-8.
62. Tanabe T, Tohnai N. Cyclooxygenase isozymes and their gene structures and expression. Prostaglandins Other Lipid Mediat 2002; 68-69:95-114.
63. Caivano M, Gorgoni B, Cohen P, Poli V. The induction of cyclooxygenase-2 mRNA in macrophages is biphasic and requires both CCAAT enhancer-binding protein beta (C/EBP β) and C/EBP δ transcription factors. J Biol Chem 2001; 276:48693-701.
64. Yin L, Laevsky G, Giardina C. Butyrate suppression of colonocyte NF-κB activation and cellular proteasome activity. J Biol Chem 2001; 276:44641-6.
65. Segain JP, Raingeard de la Bletiere D, Bourreille A et al. Butyrate inhibits inflammatory responses through NFκB inhibition: implications for Crohn's disease. Gut 2000; 47:397-403.
66. Usami M, Kishimoto K, Ohata A, Miyoshi M, Aoyama M, Fueda Y, Kotani J. Butyrate and trichostatin A attenuate nuclear factor κB activation and tumor necrosis factor α secretion and increase prostaglandin E2 secretion in human peripheral blood mononuclear cells. Nutr Res (New York, NY) 2008;28:321-8.