Isoflavones, Genistein and Daidzein, Regulate Mucosal Immune Response by Suppressing Dendritic Cell Function

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Wei, John ^a   Bhatt, Shiven ^a   Chang, Lisa M ^a   Sampson, Hugh A ^a   Masilamani, Madhan ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; BIOLOGICAL MARKER; CD83 ANTIGEN; CD86 ANTIGEN; DAIDZEIN; GAMMA INTERFERON; GENISTEIN; ISOFLAVONE DERIVATIVE; LIPOPOLYSACCHARIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL DEATH; CELL FUNCTION; CELL INTERACTION; CELL MATURATION; CELL SURFACE; CONTROLLED STUDY; CYTOTOXICITY; DEGRANULATION; DENDRITIC CELL; DIETARY INTAKE; EFFECTOR CELL; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; RESPIRATORY TRACT MUCOSA; SENSITIZATION; SOYBEAN; TH1 CELL; UPPER RESPIRATORY TRACT INFECTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIGENS, CD86; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; FEMALE; FLOW CYTOMETRY; GENISTEIN; HUMANS; IMMUNITY, MUCOSAL; INTERFERON-GAMMA; ISOFLAVONES; KILLER CELLS, NATURAL; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED BALB C; MONOCYTES; OVALBUMIN; PNEUMONIA; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84867739470     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047979     Document Type: Article

References (61)

1. Eisenbarth SC, Piggott DA, Huleatt JW, Visintin I, Herrick CA, et al. (2002) Lipopolysaccharide-enhanced, Toll-like Receptor 4 dependent T Helper Cell Type 2 Responses to Inhaled Antigen. The Journal of Experimental Medicine. 196: 1645-51.
2. Medzhitov R, (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1: 135-45.
3. Schnare M, Barton GM, Holt AC, Takeda K, Akira S, et al. (2001) Toll-like receptors control activation of adaptive immune responses. Nat Immunol 2: 947-950.
4. Brown J, Wang H, Hajishengallis GN, Martin M, (2011) TLR-signaling networks: an integration of adaptor molecules, kinases, and cross-talk. J Dent Res 90: 417-427.
5. Kawai T, Takeuchi O, Fujita T, Inoue J, Muhlradt PF, et al. (2001) Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J Immunol 167: 5887-5894.
6. Doyle S, Vaidya S, O'Connell R, Dadgostar H, Dempsey P, et al. (2002) IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17: 251-263.
7. Kaisho T, Takeuchi O, Kawai T, Hoshino K, Akira S, (2001) Endotoxin-Induced Maturation of MyD88-Deficient Dendritic Cells. The Journal of Immunology 166: 5688-5694.
8. Weighardt H, Jusek G, Mages J, Lang R, Hoebe K, et al. (2004) Identification of a TLR4- and TRIF-dependent activation program of dendritic cells. European Journal of Immunology 34: 558-564.
9. Shen H, Tesar BM, Walker WE, Goldstein DR, (2008) Dual signaling of MyD88 and TRIF is critical for maximal TLR4-induced dendritic cell maturation. J Immunol 181: 1849-1858.
10. Randolph DA, Carruthers CJL, Szabo SJ, Murphy KM, Chaplin DD, (1999) Modulation of Airway Inflammation by Passive Transfer of Allergen-Specific Th1 and Th2 Cells in a Mouse Model of Asthma. The Journal of Immunology 162: 2375-2383.
11. Dehzad N, Bopp T, Reuter S, Klein M, Martin H, et al. (2011) Regulatory T Cells More Effectively Suppress Th1-Induced Airway Inflammation Compared with Th2. The Journal of Immunology 186: 2238-2244.
12. Hansen G, Berry G, DeKruyff RH, Umetsu DT, (1999) Allergen-specific Th1 cells fail to counterbalance Th2 cell-induced airway hyperreactivity but cause severe airway inflammation. J Clin Invest 103: 175-183.
13. Dharajiya N, Vaidya S, Sinha M, Luxon B, Boldogh I, et al. (2009) Allergen Challenge Induces Ifng Dependent GTPases in the Lungs as Part of a Th1 Transcriptome Response in a Murine Model of Allergic Asthma. PLoS ONE 4: e8172.
14. Shannon J, Ernst P, Yamauchi Y, Olivenstein R, Lemiere C, et al. (2008) Differences in Airway Cytokine Profile in Severe Asthma Compared to Moderate Asthma*. Chest 133: 420-426.
15. Truyen E, Coteur L, Dilissen E, Overbergh L, Dupont LJ, et al. (2006) Evaluation of airway inflammation by quantitative Th1/Th2 cytokine mRNA measurement in sputum of asthma patients. Thorax 61: 202-208.
16. Sampath D, Castro M, Look DC, Holtzman MJ, (1999) Constitutive activation of an epithelial signal transducer and activator of transcription (STAT) pathway in asthma. J Clin Invest 103: 1353-1361.
17. Takaoka A, Tanaka Y, Tsuji T, Jinushi T, Hoshino A, et al. (2001) A Critical Role for Mouse CXC Chemokine(s) in Pulmonary Neutrophilia During Th Type 1-Dependent Airway Inflammation. The Journal of Immunology 167: 2349-2353.
18. Cui J, Pazdziorko S, Miyashiro JS, Thakker P, Pelker JW, et al. (2005) TH1-mediated airway hyperresponsiveness independent of neutrophilic inflammation. J Allergy Clin Immunol 115: 309-315.
19. Barnes S, (2010) The biochemistry, chemistry and physiology of the isoflavones in soybeans and their food products. Lymphat Res Biol 8: 89-98.
20. Beck V, Rohr U, Jungbauer A, (2005) Phytoestrogens derived from red clover: an alternative to estrogen replacement therapy? J Steroid Biochem Mol Biol 94: 499-518.
21. Kaufman PB, Duke JA, Brielmann H, Boik J, Hoyt JE, (1997) A comparative survey of leguminous plants as sources of the isoflavones, genistein and daidzein: implications for human nutrition and health. J Altern Complement Med 3: 7-12.
22. Masilamani M, Wei J, Sampson HA (2012) Regulation of the immune response by soybean isoflavones. Immunol Res.
23. Verdrengh M, Jonsson IM, Holmdahl R, Tarkowski A, (2003) Genistein as an anti-inflammatory agent. Inflamm Res 52: 341-346.
24. Yellayi S, Zakroczymski MA, Selvaraj V, Valli VE, V G, et al. (2003) The phytoestrogen genistein suppresses cell-mediated immunity in mice. J Endocrinol 176: 267-274.
25. Ogawara H, Akiyama T, Ishida J, Watanabe S, Suzuki K, (1986) A specific inhibitor for tyrosine protein kinase from Pseudomonas. J Antibiot (Tokyo) 39: 606-608.
26. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, et al. (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 262: 5592-5595.
27. Dijsselbloem N, Vanden Berghe W, De Naeyer A, Haegeman G, (2004) Soy isoflavone phyto-pharmaceuticals in interleukin-6 affections: Multi-purpose nutraceuticals at the crossroad of hormone replacement, anti-cancer and anti-inflammatory therapy. Biochem Pharmacol 68: 1171-1185.
28. Yamasaki M, Fujita S, Ishiyama E, Mukai A, Madhyastha H, et al. (2007) Soy-derived isoflavones inhibit the growth of adult T-cell leukemia cells in vitro and in vivo. Cancer Sci 98: 1740-1746.
29. Orgaard A, Jensen L, (2008) The Effects of Soy Isoflavones on Obesity. Exp Biol Med (Maywood) 233: 1066-1080.
30. Valsecchi AE, Franchi S, Panerai AE, Rossi A, Sacerdote P, et al. (2011) The soy isoflavone genistein reverses oxidative and inflammatory state, neuropathic pain, neurotrophic and vasculature deficits in diabetes mouse model. Eur J Pharmacol 650: 694-702.
31. Valles SL, Dolz-Gaiton P, Gambini J, Borras C, Lloret A, et al. (2010) Estradiol or genistein prevent Alzheimer's disease-associated inflammation correlating with an increase PPAR gamma expression in cultured astrocytes. Brain Res 1312: 138-144.
32. Beavers KM, Serra MC, Beavers DP, Cooke MB, Willoughby DS, (2010) Soy and the exercise-induced inflammatory response in postmenopausal women. Appl Physiol Nutr Metab 35: 261-269.
33. Miyake Y, Sasaki S, Ohya Y, Miyamoto S, Matsunaga I, et al. (2005) Soy, isoflavones, and prevalence of allergic rhinitis in Japanese women: The Osaka Maternal and Child Health Study. J Allergy Clin Immunol 115: 1176-1183.
34. Smith LJ, Holbrook JT, Wise R, Blumenthal M, Dozor AJ, et al. (2004) Dietary intake of soy genistein is associated with lung function in patients with asthma. J Asthma 41: 833-843.
35. Kalhan R, Smith LJ, Nlend MC, Nair A, Hixon JL, et al. (2008) A mechanism of benefit of soy genistein in asthma: inhibition of eosinophil p38-dependent leukotriene synthesis. Clin Exp Allergy 38: 103-112.
36. Bao ZS, Hong L, Guan Y, Dong XW, Zheng HS, et al. (2011) Inhibition of airway inflammation, hyperresponsiveness and remodeling by soy isoflavone in a murine model of allergic asthma. Int Immunopharmacol 11: 899-906.
37. Regal JF, Fraser DG, Weeks CE, Greenberg NA, (2000) Dietary phytoestrogens have anti-inflammatory activity in a guinea pig model of asthma. Proc Soc Exp Biol Med 223: 372-378.
38. Masilamani M, Wei J, Bhatt S, Paul M, Yakir S, et al. (2011) Soybean isoflavones regulate dendritic cell function and suppress allergic sensitization to peanut. J Allergy Clin Immunol 128: 1242-1250.e1241.
39. Steinman RM, (2007) Dendritic cells: Understanding immunogenicity. Eur J Immunol 37: S53-S60.
40. Setchell KD, Zimmer-Nechemias L, Cai J, Heubi JE, (1997) Exposure of infants to phyto-oestrogens from soy-based infant formula. Lancet 350: 23-27.
41. Marshall T, Shult P, Busse WW, (1988) Release of lysosomal enzyme beta-glucuronidase from isolated human eosinophils. J Allergy Clin Immunol 82: 550-555.
42. de Boer M, Roos D, (1986) Metabolic comparison between basophils and other leukocytes from human blood. J Immunol 136: 3447-3454.
43. Schwartz LB, Austen KF, (1980) Enzymes of the mast cell granule. J Invest Dermatol 74: 349-353.
44. Badger TM, Gilchrist JM, Pivik RT, Andres A, Shankar K, et al. (2009) The health implications of soy infant formula. Am J Clin Nutr 89: 1668S-1672S.
45. Merritt RJ, Jenks BH, (2004) Safety of Soy-Based Infant Formulas Containing Isoflavones: The Clinical Evidence. J Nutr 134: 1220S-1224.
46. Strom BL, Schinnar R, Ziegler EE, Barnhart KT, Sammel MD, et al. (2001) Exposure to soy-based formula in infancy and endocrinological and reproductive outcomes in young adulthood. JAMA 286: 807-814.
47. Neurath MF, Finotto S, Glimcher LH, (2002) The role of Th1/Th2 polarization in mucosal immunity. Nat Med 8: 567-573.
48. Batista FD, Harwood NE, (2009) The who, how and where of antigen presentation to B cells. Nat Rev Immunol 9: 15-27.
49. Ferlazzo G, Münz C (2009) Dendritic Cell Interactions with NK Cells from Different Tissues. J Clin Immunol.
50. Yum MK, Jung MY, Cho D, Kim TS, (2011) Suppression of dendritic cells' maturation and functions by daidzein, a phytoestrogen. Toxicol Appl Pharmacol 257: 174-181.
51. Zhang Y, Song TT, Cunnick JE, Murphy PA, Hendrich S, (1999) Daidzein and Genistein Glucuronides In Vitro Are Weakly Estrogenic and Activate Human Natural Killer Cells at Nutritionally Relevant Concentrations. J Nutr 129: 399-405.
52. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, et al. (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18: 767-811.
53. Bajenoff M, Breart B, Huang AY, Qi H, Cazareth J, et al. (2006) Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J Exp Med 203: 619-631.
54. Lanier LL, (2008) Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 9: 495-502.
55. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, et al. (2002) Reciprocal Activating Interaction between Natural Killer Cells and Dendritic Cells. J Exp Med 195: 327-333.
56. Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, et al. (2002) Human Dendritic Cells Activate Resting Natural Killer (NK) Cells and Are Recognized via the NKp30 Receptor by Activated NK Cells. J Exp Med 195: 343-351.
57. Moretta A, (2002) Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat Rev Immunol 2: 957-964.
58. Vitale M, Della Chiesa M, Carlomagno S, Pende D, Arico M, et al. (2005) NK-dependent DC maturation is mediated by TNFalpha and IFNgamma released upon engagement of the NKp30 triggering receptor. Blood 106: 566-571.
59. Pende D, Castriconi R, Romagnani P, Spaggiari GM, Marcenaro S, et al. (2006) Expression of the DNAM-1 ligands, Nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction. Blood 107: 2030-2036.
60. Spaggiari GM, Carosio R, Pende D, Marcenaro S, Rivera P, et al. (2001) NK cell-mediated lysis of autologous antigen-presenting cells is triggered by the engagement of the phosphatidylinositol 3-kinase upon ligation of the natural cytotoxicity receptors NKp30 and NKp46. Eur J Immunol 31: 1656-1665.
61. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, et al. (2004) Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 5: 1260-1265.