Natural indoles, indole-3-carbinol and 3,3'-diindolymethane, inhibit T cell activation by staphylococcal enterotoxin B through epigenetic regulation involving HDAC expression

Toxicology and Applied Pharmacology

Volumn 274, Issue 1, 2014, Pages 7-16

  Busbee, Philip B ^a   Nagarkatti, Mitzi ^a   Nagarkatti, Prakash S ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

3,3' Diindolylmethane; Epigenetic regulation; Histone deacetylase; Indole 3 carbinol; Inflammation; Staphylococcal enterotoxin B

Indexed keywords

3 [4 [3 (3 FLUOROPHENYL) 3 OXO 1 PROPENYL] 1 METHYL 1H PYRROL 2 YL]ACRYLOHYDROXAMIC ACID; 3 INDOLEMETHANOL; 3,3' DIINDOLYLMETHANE; CYTOKINE; DIMETHYL SULFOXIDE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1 INHIBITOR; HISTONE DEACETYLASE 2 INHIBITOR; HISTONE DEACETYLASE INHIBITOR; INDOLE DERIVATIVE; MOCETINOSTAT; STAPHYLOCOCCUS ENTEROTOXIN B; TRICHOSTATIN A; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRASSICACEAE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE STORM; DRUG INHIBITION; EPIGENETICS; FEMALE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MEDIATOR; MOUSE; NONHUMAN; PROTEIN FUNCTION; SPLEEN CELL; T LYMPHOCYTE ACTIVATION; VEGETABLE;

EID: 84889576330     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.10.022     Document Type: Article

References (60)

1. Aggarwal B.B., Ichikawa H. Molecular targets and anticancer potential of indole-3-carbinol and its derivaties. Cell Cycle 2005, 4(9):1201-1215.
2. Ahmad A., Sakr W.A., Rahman K.M. Anticancer properties of indole compounds: mechanism of apoptosis induction and role in chemotherapy. Curr. Drug Targets 2010, 11(6):652-666.
3. Allan R.S., Zueva E., Cammas F., Schreiber H.A., Masson V., Belz G.T., Roche D., Maison C., Quivy J.P., Almouzni G., Amigorena S. An epigenetic silencing pathway controlling T helper 2 cell lineage commitment. Nature 2012, 487(7406):249-253.
4. Assenmacher M., Löhning M., Scheffold A., Manz R.A., Schmitz J., Radbruch A. Sequential production of IL-2, IFN-gamma and IL-10 by individual staphylococcal enterotoxin B-activated T helper lymphocytes. Eur. J. Immunol. 1998, 28(5):1534-1543.
5. Auborn K.J., Fan S., Rosen E.M., Goodwin L., Chandraskaren A., Williams D.E., Chen D., Carter T.H. Indole-3-carbinol is a negative regulator of estrogen. J. Nutr. 2003, 133(7 Suppl.):2470S-2475S.
6. Baker M.D., Acharya K.R. Superantigens: structure-function relationships. Int. J. Med. Microbiol. 2004, 293:529-537.
7. Balasubramanian S., Verner E., Buggy J.J. Isoform-specific histone deacetylase inhibitors: the next step?. Cancer Lett. 2009, 280:211-221.
8. Benson J.M., Shepherd D.M. Dietary ligands of the aryl hydrocarbon receptor induce anti-inflammatory and immunoregulatory effects on murine dendritic cells. Toxicol. Sci. 2011, 124(2):327-338.
9. Boyce J.M., Havill N.L. Nosocomial antibiotic-associated diarrhea associated with enterotoxin-producing strains of methicillin-resistant staphylococcus aureus. Am. J. Gastroenterol. 2005, 100:1828-1834.
10. Busbee P.B., Rouse M., Nagarkatti M., Nagarkatti P.S. Use of natural AhR ligands as potential therapeutic modalities against inflammatory disorders. Nutr. Rev. 2013, 71(6):353-369.
11. Camacho I.A., Nagarkatti M., Nagarkatii P.S. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) induces Fas-dependent activation-induced cell death in superantigen-primed T cells. Arch. Toxicol. 2002, 76:570-580.
12. Chang H.P., Wang M.L., Hsu C.Y., Liu M.E., Chan M.H., Chen Y.H. Suppression of inflammation-associated factors by indole-3-carbinol in mice fed high-fat diets and in isolated, co-cultured macrophages and adipocytes. Int. J. Obes. (Lond.) 2011, 35(12):1530-1538.
13. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325(5942):834-840.
14. Coussens L.M., Werb Z. Inflammation and cancer. Nature 2002, 420(6917):860-867.
15. Darenberg J., Söderquist B., Normark B.H., Norrby-Teglund A. Differences in potency of intravenous polyspecific immunoglobulin G against streptococcal and staphylococcal superantigens: implications for therapy of toxic shock syndrome. Clin. Infect. Dis. 2004, 38(6):836-842.
16. Dinarello C.A., Fossati G., Mascagni P. Histone deacetylase inhibitors for treating a spectrum of diseases not related to cancer. Mol. Med. 2011, 17(5-6):333-352.
17. Dokmanovic M., Marks P.A. Prospects: histone deacetylase inhibitors. J. Cell. Biochem. 2005, 96:293-304.
18. Dong L., Xia S., Gao F., Zhang D., Chen J., Zhang J. 3,3'-Diindolylmethane attenuates experimental arthritis and osteoclastogenesis. Biochem. Pharmacol. 2010, 79(5):715-721.
19. Duong V., Bret C., Altucci L., Mai A., Duraffourd C., Loubersac J., Harmand P.O., Bonnet S., Valente S., Maudelonde T., Cavailles V., Boulle N. Specific activity of class II histone deacetylases in human breast cancer cells. Mol. Cancer Res. 2008, 6(12):1908-1919.
20. Fernández M.M., De Marzi M.C., Berguer P., Burzyn D., Langley R.J., Piazzon I., Mariuzza R.A., Malchiodi E.L. Binding of natural variants of staphylococcal superantigens SEG and SEI to TCR and MHC class II molecule. Mol. Immunol. 2006, 43(7):927-938.
21. Fields P.E., Kim S.T., Flavell R.A. Cutting edge: changes in histone acetylation at the IL-4 and IFN-gamma loci accompany Th1/Th2 differentiation. J. Immunol. 2002, 169(2):647-650.
22. Fournel M., Bonfils C., Hou Y., Yan P.T., Trachy-Bourget M.C., Kalita A., Liu J., Lu A.H., Zhou N.Z., Robert M.F., Gillespie J., Wang J.J., Ste-Croix H., Rahil J., Lefebvre S., Moradei O., Delorme D., Macleod A.R., Besterman J.M., Li Z. MGCD0103, a novel isotype-selective histone deacetylase inhibitor, has broad spectrum antitumor activity in vitro and in vivo. Mol. Cancer Ther. 2008, 7(4):759-768.
23. Fritzsche F.R., Weichert W., Röske A., Gekeler V., Beckers T., Stephan C., Jung K., Scholman K., Denkert C., Dietel M., Kristiansen G. Class I histone deacetylases 1, 2 and 3 are highly expressed in renal cell cancer. BMC Cancer 2008, 8:381.
24. Grabiec A.M., Korchynskyi O., Tak P.P., Reedquist K.A. Histone deacetylase inhibitors suppress rheumatoid arthritis fibroblast-like synoviocyte and macrophage IL-6 production by accelerating mRNA decay. Ann. Rheum. Dis. 2012, 71(3):424-431.
25. Haberland M., Montgomery R.L., Olson E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 2009, 10:32-42.
26. Han S.B., Lee J.K. Anti-inflammatory effect of trichostatin-A on murine bone marrow-derived macrophages. Arch. Pharm. Res. 2009, 32(4):613-624.
27. Heidemann S.M., Sandhu H., Kovacevic N., Phumeetham S., Solomon R. Detection of tumor necrosis factor-α and interleukin-6 in exhaled breath condensate of rats with pneumonia due to staphylococcal enterotoxin B. Exp. Lung Res. 2011, 37(9):563-567.
28. Henghold W.B. Other biologic toxin bioweapons: ricin, staphylococcal enterotoxin B, and trichothecene mycotoxins. Dermatol. Clin. 2004, 22:257-262.
29. Huang Z., Jiang Y., Yang Y., Shao J., Sun X., Chen J., Dong L., Zhang J. 3,3'-Diindolylmethane alleviates oxazolone-induced colitis through Th2/Th17 suppression and Treg induction. Mol. Immunol. 2013, 53(4):335-344.
30. Kim Y.H., Kwon H.S., Kim D.H., Shin E.K., Kang Y.H., Park J.H., Shin H.K., Kim J.K. 3,3'-Diindolylmethane attenuates colonic inflammation and tumorigenesis in mice. Inflamm. Bowel Dis. 2009, 15(8):1164-1173.
31. Kim E.J., Park H., Kim J., Park J.H. 3,3'-Diindolylmethane suppresses 12-O-tetradecanoylphorbol-13-acetate-induced inflammation and tumor promotion in mouse skin via the downregulation of inflammatory mediators. Mol. Carcinog. 2010, 49(7):672-683.
32. Krakauer T., Buckley M., Fisher D. Murine models of staphylococcal enterotoxin B-induced toxic shock. Mil. Med. 2010, 175(11):917-922.
33. Le Loir Y., Baron F., Gautier M. Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2003, 2(1):63-76.
34. Leoni F., Zaliani A., Bertolini G., Porro G., Pagani P., Pozzi P., Donà G., Fossati G., Sozzani S., Azam T., Bufler P., Fantuzzi G., Goncharov I., Kim S.H., Pomerantz B.J., Reznikov L.L., Siegmund B., Dinarello C.A., Mascagni P. The antitumor histone deacetylase inhibitor suberoylanilide hydroxamic acid exhibits antiinflammatory properties via suppression of cytokines. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(5):2995-3000.
35. Ler S.G., Lee F.K., Gopalakrishnakone P. Trends in detection of warfare agents. Detection methods for ricin, staphylococcal enterotoxin B, and T-2 toxin. J. Chromatogr. A 2006, 1133:1-12.
36. Lindsey W.B., Lowdell M.W., Marti G.E., Abbasi F., Zenger V., King K.M., Lamb L.S. CD69 expression as an index of T-cell function: assay standardization, validation and use in monitoring immune recovery. Cytotherapy 2007, 9(2):123-132.
37. Lührs H., Gerke T., Müller J.G., Melcher R., Schauber J., Boxberge F., Scheppach W., Menzel T. Butyrate inhibits NF-kappaB activation in lamina propria macrophages of patients with ulcerative colitis. Scand. J. Gastroenterol. 2002, 37(4):458-466.
38. Madsen J.M. Toxins as weapons of mass destruction. A comparison and contrast with biological-warfare and chemical-warfare agents. Clin. Lab. Med. 2001, 21(3):593-605.
39. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454(7203):436-444.
40. Marrack P., Blackman M., Kusnhir E., Kappler J. The toxicity of staphylococcal enterotoxin b in mice is mediated by T cells. J. Exp. Med. 1990, 171:455-464.
41. Marshall N.B., Kerkvliet N.I. Dioxin and immune regulation: emerging role of aryl hydrocarbon receptor in the generation of regulatory T cells. Ann. N. Y. Acad. Sci. 2010, 1183:25-37.
42. Mead P.S., Slutsker L., Dietz V., McCaig L.F., Bresee J.S., Shapiro C., Griffin P.M., Tauxe R.V. Food-related illness and death in the united states. Emerg. Infect. Dis. 1999, 5:607-625.
43. Mishra N., Reilly C.M., Brown D.R., Ruiz P., Gilkeson G.S. Histone deacetylase inhibitors modulate renal disease in the MRL-lpr/lpr mouse. J. Clin. Invest. 2003, 111(4):539-552.
44. Morris M.J., Monteggia L.M. Unique functional roles of class I and class II histone deacetylases in central nervous system development and function. Int. J. Dev. Neurosci. 2013, 31(6):370-381.
45. Mulvey L., Chandrasekaran A., Liu K., Lombardi S., Wang X.P., Auborn K.J., Goodwin L. Interplay of genes regulated by estrogen and diindolylmethane in breast cancer cell lines. Mol. Med. 2007, 13(1-2):69-78.
46. Nam H.J., Kang J.K., Kim S.K., Ahn K.J., Seok H., Park S.J., Chang J.S., Pothoulakis C., Lamont J.T., Kim H. Clostridium difficile toxin A decreases acetylation of tubulin, leading to microtubule depolymerization through activation of histone deacetylase 6, and this mediates acute inflammation. J. Biol. Chem. 2010, 285(43). (32888-32866).
47. Osada H., Tatematsu Y., Saito H., Yatabe Y., Mitsudomi T., Takahashi T. Reduced expression of class II histone deacetylase genes is associated with poor prognosis in lung cancer patients. Int. J. Cancer 2004, 112(1):26-32.
48. Pinchuk I.V., Beswick E.J., Reyes V.E. Staphylococcal enterotoxins. Toxins 2010, 2:2177-2197.
49. Reider S.A., Nagarkatti P., Nagarkatti M. CD1d-independent activation of invariant natural killer T cells by staphylococcal enterotoxin B through major histocompatibility complex class II/T cell receptor interaction results in acute lung injury. Infect. Immun. 2011, 79(8):3141-3148.
50. Rouse M., Singh N.P., Nagarkatti P.S., Nagarkatti M. Indoles mitigate the development of experimental autoimmune encephalomyelitis by induction of reciprocal differentiation of regulatory T cells and Th17 cells. Br. J. Pharmacol. 2013, 169(6):1305-1321.
51. Sarkar F.H., Li Y. Indole-3-carbinol and prostate cancer. J. Nutr. 2004, 134:3493S-3498S.
52. Schmitz F.J., MacKenzie C.R., Geisel R., Wagner S., Idel H., Verhoef J., Hadding U., Heinz H.P. Enterotoxin and toxic shock syndrome toxin-1 production of methicillin resistant and methicillin sensitive staphylococcus aureus Strains. Eur. J. Epidemiol. 1997, 13:699-708.
53. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
54. Urbich C., Rössig L., Kaluza D., Potente M., Boeckel J.N., Knau A., Diehl F., Geng J.G., Hofmann W.K., Zeiher A.M., Dimmeler S. HDAC5 is a repressor of angiogenesis and determines the angiogenic gene expression pattern of endothelial cells. Blood 2009, 113(22):5669-5679.
55. Usui T., Okada M., Mizuno W., Oda M., Ide N., Morita T., Hara Y., Yamawaki H. HDAC4 mediates development of hypertension via vascular inflammation in spontaneous hypertensive rats. Am. J. Physiol. Heart Circ. Physiol. 2012, 302(9):H1894-H1904.
56. Vanhaecke T., Papeleu P., Elaut G., Rogiers V. Trichostatin A-like hydroxamate histone deacetylase inhibitors as therapeutic agents: toxicological point of view. Curr. Med. Chem. 2004, 11(12):1629-1643.
57. Wang T.T., Milner M.J., Milner J.A., Kim Y.S. Estrogen receptor alpha as a target for indole-3-carbinol. J. Nutr. 2006, 17(10):659-664.
58. Weichert W., Röske A., Gekeler V., Beckers T., Stephan C., Jung K., Fritzsche F.R., Niesporek S., Denkert C., Dietel M., Kristiansen G. Histone deacetylases 1, 2 and 3 are highly expressed in prostate cancer and HDAC2 expression is associated with shorter PSA relapse time after radical prostatectomy. Br. J. Cancer 2008, 98(3):604-610.
59. Wood M.W., Breitschwerdt E.B., Gookin J.L. Autocrine effects of interleukin-6 mediate acute-phase proinflammatory and tissue-reparative transcriptional responses of canine bladder mucosa. Infect. Immun. 2011, 79(2):708-715.
60. Yongming L., Xia L., Bin G. Chemopreventative agent 3,3'-diindolylmethane selectively induces proteasomal degradation of class I histone deacetylases. Cancer Res. 2010, 70(2):646-654.