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Published in: BMC Complementary Medicine and Therapies 1/2019

Open Access 01-12-2019 | Cytokines | Research article

The mycelium of the Trametes versicolor (Turkey tail) mushroom and its fermented substrate each show potent and complementary immune activating properties in vitro

Authors: Kathleen F. Benson, Paul Stamets, Renee Davis, Regan Nally, Alex Taylor, Sonya Slater, Gitte S. Jensen

Published in: BMC Complementary Medicine and Therapies | Issue 1/2019

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Abstract

Background

The medicinal mushroom Trametes versicolor (Tv, Turkey Tail) is often prepared for consumption as a powder from the fungal mycelium and the fermented substrate on which it grew. The goal for this study was to evaluate the immune-modulating properties of the mycelium versus the fermented substrate, to document whether an important part of the immune-activating effects resides in the metabolically fermented substrate.

Methods

Tv mycelium was cultured on rice flour. The mycelium and the fermented substrate were mechanically separated, dried, and milled. The initial substrate served as a control. Aqueous fractions were extracted and passed through 0.22-μm filters. The remaining solids were passed through homogenization spin columns without filtration. The aqueous and solid fractions of the initial substrate (IS), the fermented substrate (FS), and the Trametes versicolor mycelium (TvM) were tested for immune-activating and modulating activities on human peripheral blood mononuclear cell cultures, to examine expression of the CD69 activation marker on lymphocytes versus monocytes, and on the T, NKT, and NK lymphocyte subsets. Culture supernatants were tested for cytokines using Luminex arrays.

Results

Both aqueous and solid fractions of TvM triggered robust induction of CD69 on lymphocytes and monocytes, whereas FS only triggered minor induction of CD69, and IS had no activating effect. The aqueous extract of TvM had stronger activating effects than the solid fraction. In contrast, the solid fraction of IS triggered a reduction in CD69, below levels on untreated cells.
Both aqueous and solid fractions of FS triggered large and dose-dependent increases in immune-activating pro-inflammatory cytokines (IL-2, IL-6), anti-inflammatory cytokines Interleukin-1 receptor antagonist (IL-1ra) and Interleukin-10 (IL-10), anti-viral cytokines interferon-gamma (IFN-γ) and Macrophage Inflammatory Protein-alpha (MIP-1α), as well as Granulocyte-Colony Stimulating Factor (G-CSF) and Interleukin-8 (IL-8). TvM triggered more modest cytokine increases. The aqueous extract of IS showed no effects, whereas the solid fraction showed modest effects on induction of cytokines and growth factors.

Conclusion

The results demonstrated that the immune-activating bioactivity of a mycelial-based medicinal mushroom preparation is a combination of the mycelium itself (including insoluble beta-glucans, and also water-soluble components), and the highly bioactive, metabolically fermented substrate, not present in the initial substrate.
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Literature
1.
go back to reference Aung SK: The Clinical Use of Mushrooms from a Traditional Chinese Medical Perspective. 2005, 7(3):375–376. Aung SK: The Clinical Use of Mushrooms from a Traditional Chinese Medical Perspective. 2005, 7(3):375–376.
2.
go back to reference Jin X, Ruiz Beguerie J, Sze DM-Y, Chan GCF. Ganoderma lucidum (Reishi mushroom) for cancer treatment. Cochrane Database Syst Rev. 2012;6:CD007731. Jin X, Ruiz Beguerie J, Sze DM-Y, Chan GCF. Ganoderma lucidum (Reishi mushroom) for cancer treatment. Cochrane Database Syst Rev. 2012;6:CD007731.
3.
go back to reference Yim M-H, Shin J-W, Son J-Y, Oh S-M, Han S-H, Cho J-H, Cho C-K, Yoo H-S, Lee Y-W, Son C-G. Soluble components of Hericium erinaceum induce NK cell activation via production of interleukin-12 in mice splenocytes. Acta Pharmacol Sin. 2007;28(6):901–7.PubMedCrossRef Yim M-H, Shin J-W, Son J-Y, Oh S-M, Han S-H, Cho J-H, Cho C-K, Yoo H-S, Lee Y-W, Son C-G. Soluble components of Hericium erinaceum induce NK cell activation via production of interleukin-12 in mice splenocytes. Acta Pharmacol Sin. 2007;28(6):901–7.PubMedCrossRef
4.
go back to reference Lu H, Yang Y, Gad E, Inatsuka C, Wenner CA, Disis ML, Standish LJ. TLR2 agonist PSK activates human NK cells and enhances the antitumor effect of HER2-targeted monoclonal antibody therapy. Clin Cancer Res. 2011;17(21):6742–53.PubMedCrossRefPubMedCentral Lu H, Yang Y, Gad E, Inatsuka C, Wenner CA, Disis ML, Standish LJ. TLR2 agonist PSK activates human NK cells and enhances the antitumor effect of HER2-targeted monoclonal antibody therapy. Clin Cancer Res. 2011;17(21):6742–53.PubMedCrossRefPubMedCentral
5.
go back to reference Wang G, Zhao J, Liu J, Huang Y, Zhong J-J, Tang W. Enhancement of IL-2 and IFN-gamma expression and NK cells activity involved in the anti-tumor effect of ganoderic acid me in vivo. Int Immunopharmacol. 2007;7(6):864–70.PubMedCrossRef Wang G, Zhao J, Liu J, Huang Y, Zhong J-J, Tang W. Enhancement of IL-2 and IFN-gamma expression and NK cells activity involved in the anti-tumor effect of ganoderic acid me in vivo. Int Immunopharmacol. 2007;7(6):864–70.PubMedCrossRef
6.
go back to reference Chien CM, Cheng JL, Chang WT, Tien MH, Tsao CM, Chang YH, Chang HY, Hsieh JF, Wong CH, Chen ST. Polysaccharides of Ganoderma lucidum alter cell immunophenotypic expression and enhance CD56+ NK-cell cytotoxicity in cord blood. Bioorg Med Chem. 2004;12(21):5603–9.PubMedCrossRef Chien CM, Cheng JL, Chang WT, Tien MH, Tsao CM, Chang YH, Chang HY, Hsieh JF, Wong CH, Chen ST. Polysaccharides of Ganoderma lucidum alter cell immunophenotypic expression and enhance CD56+ NK-cell cytotoxicity in cord blood. Bioorg Med Chem. 2004;12(21):5603–9.PubMedCrossRef
7.
go back to reference Yan ZF, Liu NX. Activation effects of polysaccharides of Flammulina velutipes mycorrhizae on the T lymphocyte immune function 2014, 285421. Yan ZF, Liu NX. Activation effects of polysaccharides of Flammulina velutipes mycorrhizae on the T lymphocyte immune function 2014, 285421.
8.
go back to reference Xu X, Li J, Hu Y. Polysaccharides from Inonotus obliquus sclerotia and cultured mycelia stimulate cytokine production of human peripheral blood mononuclear cells in vitro and their chemical characterization. Int Immunopharmacol. 2014;21(2):269–78.PubMedCrossRef Xu X, Li J, Hu Y. Polysaccharides from Inonotus obliquus sclerotia and cultured mycelia stimulate cytokine production of human peripheral blood mononuclear cells in vitro and their chemical characterization. Int Immunopharmacol. 2014;21(2):269–78.PubMedCrossRef
9.
go back to reference De Groote D, Zangerle PF, Gevaert Y, Fassotte MF, Beguin Y, Noizat-Pirenne F, . . . et al. Direct stimulation of cytokines (IL-1 beta, TNF-alpha, IL-6, IL-2, IFN-gamma and GM-CSF) in whole blood. I. Comparison with isolated PBMC stimulation. Cytokine, 1992, 4(3), 239–248.PubMedCrossRef De Groote D, Zangerle PF, Gevaert Y, Fassotte MF, Beguin Y, Noizat-Pirenne F, . . . et al. Direct stimulation of cytokines (IL-1 beta, TNF-alpha, IL-6, IL-2, IFN-gamma and GM-CSF) in whole blood. I. Comparison with isolated PBMC stimulation. Cytokine, 1992, 4(3), 239–248.PubMedCrossRef
10.
go back to reference Dai X, Stanilka JM, Rowe CA, Esteves EA, Nieves C, Spaiser SJ, et al. Consuming Lentinula edodes (shiitake) mushrooms daily improves human immunity: a randomized dietary intervention in healthy young adults. J Am Coll Nutr. 2015;34(6):478–87.PubMedCrossRef Dai X, Stanilka JM, Rowe CA, Esteves EA, Nieves C, Spaiser SJ, et al. Consuming Lentinula edodes (shiitake) mushrooms daily improves human immunity: a randomized dietary intervention in healthy young adults. J Am Coll Nutr. 2015;34(6):478–87.PubMedCrossRef
11.
go back to reference Wasser SP. Medicinal mushroom science: current perspectives, advances, evidences, and challenges. Biom J. 2014;37(6):345–56. Wasser SP. Medicinal mushroom science: current perspectives, advances, evidences, and challenges. Biom J. 2014;37(6):345–56.
12.
go back to reference Meng X, Liang H, Luo L. Antitumor polysaccharides from mushrooms: a review on the structural characteristics, antitumor mechanisms and immunomodulating activities. Carbohydr Res. 2016;424:30–41.PubMedCrossRef Meng X, Liang H, Luo L. Antitumor polysaccharides from mushrooms: a review on the structural characteristics, antitumor mechanisms and immunomodulating activities. Carbohydr Res. 2016;424:30–41.PubMedCrossRef
13.
go back to reference Kodama N, Komuta K, Sakai N, Nanba H. Effects of D-fraction, a polysaccharide from Grifola frondosa on tumor growth involve activation of NK cells. Biol Pharm Bull. 1647-1650;2002:25(12). Kodama N, Komuta K, Sakai N, Nanba H. Effects of D-fraction, a polysaccharide from Grifola frondosa on tumor growth involve activation of NK cells. Biol Pharm Bull. 1647-1650;2002:25(12).
14.
go back to reference Kino K, Yamashita A, Yamaoka K, Watanabe J, Tanaka S, Ko K, et al. Isolation and characterization of a new immunomodulatory protein, ling zhi-8 (LZ-8), from Ganoderma lucidium. J Biol Chem. 1989;264(1):472–8.PubMed Kino K, Yamashita A, Yamaoka K, Watanabe J, Tanaka S, Ko K, et al. Isolation and characterization of a new immunomodulatory protein, ling zhi-8 (LZ-8), from Ganoderma lucidium. J Biol Chem. 1989;264(1):472–8.PubMed
16.
go back to reference Akihisa T, Nakamura Y, Tagata M, Tokuda H, Yasukaw, K, Uchiyama E, Kimura Y. Anti-inflammatory and anti-tumor-promoting effects of triterpene acids and sterols from the fungus Ganoderma lucidum. 2007, Chem Biodivers, 4(2), 224–231. Akihisa T, Nakamura Y, Tagata M, Tokuda H, Yasukaw, K, Uchiyama E, Kimura Y. Anti-inflammatory and anti-tumor-promoting effects of triterpene acids and sterols from the fungus Ganoderma lucidum. 2007, Chem Biodivers, 4(2), 224–231.
17.
go back to reference Xue Z, Li J, Cheng A, Yu W, Zhang Z, Kou X, Zhou F. Structure identification of Triterpene from the mushroom Pleurotus eryngii with inhibitory effects against breast Cancer. Plant Foods Hum Nutr. 2015;70(3):291–6.PubMedCrossRef Xue Z, Li J, Cheng A, Yu W, Zhang Z, Kou X, Zhou F. Structure identification of Triterpene from the mushroom Pleurotus eryngii with inhibitory effects against breast Cancer. Plant Foods Hum Nutr. 2015;70(3):291–6.PubMedCrossRef
18.
go back to reference Durgo K, Koncar M, Komes D, Belscak-Cvitanovic A, Franekic J, Jakopovich I, et al. Cytotoxicity of blended versus single medicinal mushroom extracts on human cancer cell lines: contribution of polyphenol and polysaccharide content. Int J Med Mushrooms. 2013;15(5):435–48.PubMedCrossRef Durgo K, Koncar M, Komes D, Belscak-Cvitanovic A, Franekic J, Jakopovich I, et al. Cytotoxicity of blended versus single medicinal mushroom extracts on human cancer cell lines: contribution of polyphenol and polysaccharide content. Int J Med Mushrooms. 2013;15(5):435–48.PubMedCrossRef
19.
go back to reference Standish LJ, Wenner CA, Sweet ES, Bridge C, Nelson A, Martzen M, et al. Trametes versicolor mushroom immune therapy in breast cancer. J Soc Integr Oncol. 2008;6(3):122–8.PubMedPubMedCentral Standish LJ, Wenner CA, Sweet ES, Bridge C, Nelson A, Martzen M, et al. Trametes versicolor mushroom immune therapy in breast cancer. J Soc Integr Oncol. 2008;6(3):122–8.PubMedPubMedCentral
21.
go back to reference Torkelson CJ, Sweet E, Martzen MR, Sasagawa M, Wenner CA, Gay J, Putiri A, Standish LJ. Phase 1 clinical trial of Trametes versicolor in women with breast Cancer. ISRN Oncol. 2012;2012:251632.PubMedPubMedCentral Torkelson CJ, Sweet E, Martzen MR, Sasagawa M, Wenner CA, Gay J, Putiri A, Standish LJ. Phase 1 clinical trial of Trametes versicolor in women with breast Cancer. ISRN Oncol. 2012;2012:251632.PubMedPubMedCentral
22.
go back to reference Brown DC, Reet J. Single agent polysaccharopeptide delays metastases and improves survival in naturally occurring hemangiosarcoma. Evid Based Complement Alternat Med. 2012;384301. Brown DC, Reet J. Single agent polysaccharopeptide delays metastases and improves survival in naturally occurring hemangiosarcoma. Evid Based Complement Alternat Med. 2012;384301.
23.
go back to reference Rosendahl AH, Sun C, Wu D, Andersson R. Polysaccharide-K (PSK) increases p21(WAF/Cip1) and promotes apoptosis in pancreatic cancer cells. Pancreatology. 2012;12(6):467–74.PubMedCrossRef Rosendahl AH, Sun C, Wu D, Andersson R. Polysaccharide-K (PSK) increases p21(WAF/Cip1) and promotes apoptosis in pancreatic cancer cells. Pancreatology. 2012;12(6):467–74.PubMedCrossRef
24.
go back to reference Konagai A, Yoshimura K, Hazama S, Yamamoto N, Aoki K, Ueno T, et al. Correlation between NKG2DL expression and antitumor effect of protein-bound polysaccharide-K in tumor-bearing mouse models. Anticancer Res. 2017;37(8):4093–101.PubMed Konagai A, Yoshimura K, Hazama S, Yamamoto N, Aoki K, Ueno T, et al. Correlation between NKG2DL expression and antitumor effect of protein-bound polysaccharide-K in tumor-bearing mouse models. Anticancer Res. 2017;37(8):4093–101.PubMed
25.
go back to reference Fritz H, Kennedy DA, Ishii M, Fergusson D, Fernandes R, Cooley K, Seely D. Polysaccharide K and Coriolus versicolor extracts for lung cancer: a systematic review. Integr Cancer Ther. 2015;14(3):201–11.PubMedCrossRef Fritz H, Kennedy DA, Ishii M, Fergusson D, Fernandes R, Cooley K, Seely D. Polysaccharide K and Coriolus versicolor extracts for lung cancer: a systematic review. Integr Cancer Ther. 2015;14(3):201–11.PubMedCrossRef
26.
go back to reference Coy C, Standish LJ, Bender G, Lu H. Significant Correlation between TLR2 Agonist Activity and TNF-α Induction in J774. A1 Macrophage Cells by Different Medicinal Mushroom Products. Int J Med Mushrooms. 2015;17(8).PubMedCrossRef Coy C, Standish LJ, Bender G, Lu H. Significant Correlation between TLR2 Agonist Activity and TNF-α Induction in J774. A1 Macrophage Cells by Different Medicinal Mushroom Products. Int J Med Mushrooms. 2015;17(8).PubMedCrossRef
27.
go back to reference Hatakka A. Lignin-modifying enzymes from selected white-rot fungi: production and role from in lignin degradation. FEMS Microbiol Rev. 1994;13(2):125–35.CrossRef Hatakka A. Lignin-modifying enzymes from selected white-rot fungi: production and role from in lignin degradation. FEMS Microbiol Rev. 1994;13(2):125–35.CrossRef
28.
go back to reference Collins PJ, Dobson A. Regulation of laccase gene transcription in Trametes versicolor. Appl Environ Microbiol. 1997;63(9):3444–50.PubMedPubMedCentral Collins PJ, Dobson A. Regulation of laccase gene transcription in Trametes versicolor. Appl Environ Microbiol. 1997;63(9):3444–50.PubMedPubMedCentral
29.
go back to reference Bertrand T, Jolivalt C, Caminade E, Joly N, Mougin C, Briozzo P. Purification and preliminary crystallographic study of Trametes versicolor laccase in its native form. Acta Crystallogr D Biol Crystallogr. 2002;58(Pt 2):319–21.PubMedCrossRef Bertrand T, Jolivalt C, Caminade E, Joly N, Mougin C, Briozzo P. Purification and preliminary crystallographic study of Trametes versicolor laccase in its native form. Acta Crystallogr D Biol Crystallogr. 2002;58(Pt 2):319–21.PubMedCrossRef
30.
go back to reference Mayer AM, Staples RC. Laccase: new functions for an old enzyme. Phytochemistry. 2002;60(6):551–65.PubMedCrossRef Mayer AM, Staples RC. Laccase: new functions for an old enzyme. Phytochemistry. 2002;60(6):551–65.PubMedCrossRef
31.
go back to reference Chawachart N, Khanongnuch C, Watanabe T, Lumyong S. Rice bran as an efficient substrate for laccase production from thermotolerant basidiomycete Coriolus versicolor strain RC3. Fungal Divers. 2004;15:23–32. Chawachart N, Khanongnuch C, Watanabe T, Lumyong S. Rice bran as an efficient substrate for laccase production from thermotolerant basidiomycete Coriolus versicolor strain RC3. Fungal Divers. 2004;15:23–32.
32.
go back to reference Gloer JB. The chemistry of fungal antagonism and defense. Can J Bot. 1995;73(S1):1265–74.CrossRef Gloer JB. The chemistry of fungal antagonism and defense. Can J Bot. 1995;73(S1):1265–74.CrossRef
33.
go back to reference Elder AL. (1970). History of penicillin production. Chem. Eng. Prog. Symp. Series, no 100. New York: American Institute of Chemical Engineers; 1970. Elder AL. (1970). History of penicillin production. Chem. Eng. Prog. Symp. Series, no 100. New York: American Institute of Chemical Engineers; 1970.
34.
go back to reference Su C-H, Lai M-N, Lin C-C, Ng L-T. Comparative characterization of physicochemical properties and bioactivities of polysaccharides from selected medicinal mushrooms. Appl Microbiol Biotechnol. 2016;100(10):4385–93.PubMedCrossRef Su C-H, Lai M-N, Lin C-C, Ng L-T. Comparative characterization of physicochemical properties and bioactivities of polysaccharides from selected medicinal mushrooms. Appl Microbiol Biotechnol. 2016;100(10):4385–93.PubMedCrossRef
35.
go back to reference Lee JS, Min KM, Cho JY, Hong EK. Study of macrophage activation and structural characteristics of purified polysaccharides from the fruiting body of Hericium erinaceus. J Microbiol Biotechnol. 2009;19(9):951–9.PubMedCrossRef Lee JS, Min KM, Cho JY, Hong EK. Study of macrophage activation and structural characteristics of purified polysaccharides from the fruiting body of Hericium erinaceus. J Microbiol Biotechnol. 2009;19(9):951–9.PubMedCrossRef
36.
go back to reference Bak WC, Park JH, Park YA, Ka KH. Determination of Glucan contents in the fruiting bodies and mycelia of Lentinula edodes cultivars. Mycobiology. 2014;42(3):301–4.PubMedCrossRefPubMedCentral Bak WC, Park JH, Park YA, Ka KH. Determination of Glucan contents in the fruiting bodies and mycelia of Lentinula edodes cultivars. Mycobiology. 2014;42(3):301–4.PubMedCrossRefPubMedCentral
37.
38.
go back to reference Kasliwal RR, Bansal M, Gupta R, Shah S, Dani S, Oomman A, Pai V, Prasad GM, Singhvi S, Patel J, et al. ESSENS dyslipidemia: a placebo-controlled, randomized study of a nutritional supplement containing red yeast rice in subjects with newly diagnosed dyslipidemia. Nutrition. 2016;32(7–8):767–76.PubMedCrossRef Kasliwal RR, Bansal M, Gupta R, Shah S, Dani S, Oomman A, Pai V, Prasad GM, Singhvi S, Patel J, et al. ESSENS dyslipidemia: a placebo-controlled, randomized study of a nutritional supplement containing red yeast rice in subjects with newly diagnosed dyslipidemia. Nutrition. 2016;32(7–8):767–76.PubMedCrossRef
39.
go back to reference Jensen GS, Hart AN, Schauss AG. An antiinflammatory immunogen from yeast culture induces activation and alters chemokine receptor expression on human natural killer cells and B lymphocytes in vitro. Nutr Res. 2007;27:327–35.CrossRefPubMed Jensen GS, Hart AN, Schauss AG. An antiinflammatory immunogen from yeast culture induces activation and alters chemokine receptor expression on human natural killer cells and B lymphocytes in vitro. Nutr Res. 2007;27:327–35.CrossRefPubMed
40.
go back to reference Jensen GS, Carter SG, Reeves SG, Robinson LE, Benson KF. Anti-inflammatory properties of a dried fermentate in vitro and in vivo. J Med Food. 2015 Mar;18(3):378–84.PubMedCrossRefPubMedCentral Jensen GS, Carter SG, Reeves SG, Robinson LE, Benson KF. Anti-inflammatory properties of a dried fermentate in vitro and in vivo. J Med Food. 2015 Mar;18(3):378–84.PubMedCrossRefPubMedCentral
41.
go back to reference Jensen GS, Redman KA, Benson KF, Carter SG, Mitzner MA, Reeves S, Robinson L. Antioxidant bioavailability and rapid immune-modulating effects after consumption of a single acute dose of a high-metabolite yeast immunogen: results of a placebo-controlled double-blinded crossover pilot study. J Med Food. 2011 Sep;14(9):1002–10.PubMedCrossRefPubMedCentral Jensen GS, Redman KA, Benson KF, Carter SG, Mitzner MA, Reeves S, Robinson L. Antioxidant bioavailability and rapid immune-modulating effects after consumption of a single acute dose of a high-metabolite yeast immunogen: results of a placebo-controlled double-blinded crossover pilot study. J Med Food. 2011 Sep;14(9):1002–10.PubMedCrossRefPubMedCentral
42.
go back to reference Jensen GS, Patterson KM, Barnes J, Schauss AG, Beaman R, Reeves SG, Robinson LE. A double-blind placebo-controlled, randomized pilot study: consumption of a high-metabolite Immunogen from yeast culture has beneficial effects on erythrocyte health and mucosal immune protection in healthy subjects. The Open Nutrition Journal. 2008;2:68–75.CrossRef Jensen GS, Patterson KM, Barnes J, Schauss AG, Beaman R, Reeves SG, Robinson LE. A double-blind placebo-controlled, randomized pilot study: consumption of a high-metabolite Immunogen from yeast culture has beneficial effects on erythrocyte health and mucosal immune protection in healthy subjects. The Open Nutrition Journal. 2008;2:68–75.CrossRef
43.
go back to reference Moyad MA, Robinson LE, Zawada ET, Jr Kittelsrud JM. Chen DG. Reeves SG. Weaver SE. Effects of a modified yeast supplement on cold/flu symptoms. Urol Nurs. 2008 Feb;28(1):50–5.PubMed Moyad MA, Robinson LE, Zawada ET, Jr Kittelsrud JM. Chen DG. Reeves SG. Weaver SE. Effects of a modified yeast supplement on cold/flu symptoms. Urol Nurs. 2008 Feb;28(1):50–5.PubMed
44.
go back to reference Moyad MA, Robinson LE, Kittelsrud JM, Reeves SG, Weaver SE, Guzman AI, Bubak ME. Immunogenic yeast-based fermentation product reduces allergic rhinitis-induced nasal congestion: a randomized, double-blind, placebo-controlled trial. Adv Ther. 2009 Aug;26(8):795–804.PubMedCrossRef Moyad MA, Robinson LE, Kittelsrud JM, Reeves SG, Weaver SE, Guzman AI, Bubak ME. Immunogenic yeast-based fermentation product reduces allergic rhinitis-induced nasal congestion: a randomized, double-blind, placebo-controlled trial. Adv Ther. 2009 Aug;26(8):795–804.PubMedCrossRef
45.
go back to reference Possemiers S, Pinheiro I, Verhelst A, Van den Abbeele P, Maignien L, Laukens D, Reeves SG, Robinson LE, Raas T, Schneider YJ, Van de Wiele T, Marzorati M. A dried yeast fermentate selectively modulates both the luminal and mucosal gut microbiota and protects against inflammation, as studied in an integrated in vitro approach. J Agric Food Chem. 2013 Oct 2;61(39):9380–92.PubMedCrossRef Possemiers S, Pinheiro I, Verhelst A, Van den Abbeele P, Maignien L, Laukens D, Reeves SG, Robinson LE, Raas T, Schneider YJ, Van de Wiele T, Marzorati M. A dried yeast fermentate selectively modulates both the luminal and mucosal gut microbiota and protects against inflammation, as studied in an integrated in vitro approach. J Agric Food Chem. 2013 Oct 2;61(39):9380–92.PubMedCrossRef
46.
go back to reference Borrego F, Peña J, Solana R. Regulation of CD69 expression on human natural killer cells: differential involvement of protein kinase C and protein tyrosine kinases. Eur J Immunol. 1993 May;23(5):1039–43.PubMedCrossRef Borrego F, Peña J, Solana R. Regulation of CD69 expression on human natural killer cells: differential involvement of protein kinase C and protein tyrosine kinases. Eur J Immunol. 1993 May;23(5):1039–43.PubMedCrossRef
47.
go back to reference Moretta A, Poggi A, Pende D, Tripodi G, Orengo AM, Pella N, Augugliaro R, Bottino C, Ciccone E, Moretta L. CD69-mediated pathway of lymphocyte activation: anti-CD69 monoclonal antibodies trigger the cytolytic activity of different lymphoid effector cells with the exception of cytolytic T lymphocytes expressing T cell receptor alpha/beta. J Exp Med. 1991 Dec 1;174(6):1393–8.PubMedCrossRef Moretta A, Poggi A, Pende D, Tripodi G, Orengo AM, Pella N, Augugliaro R, Bottino C, Ciccone E, Moretta L. CD69-mediated pathway of lymphocyte activation: anti-CD69 monoclonal antibodies trigger the cytolytic activity of different lymphoid effector cells with the exception of cytolytic T lymphocytes expressing T cell receptor alpha/beta. J Exp Med. 1991 Dec 1;174(6):1393–8.PubMedCrossRef
48.
go back to reference Jensen GS, Hart AN. Immunomodulation by SanPharma fungal metabolic products. J Altern Complement Med. 2006 May;12(4):409–16.PubMedCrossRef Jensen GS, Hart AN. Immunomodulation by SanPharma fungal metabolic products. J Altern Complement Med. 2006 May;12(4):409–16.PubMedCrossRef
49.
go back to reference Hart AN, Zaske LA, Patterson KM, Drapeau C, Jensen GS. Natural killer cell activation and modulation of chemokine receptor profile in vitro by an extract from the cyanophyta Aphanizomenon flos-aquae. J Med Food. 2007 Sep;10(3):435–41.PubMedCrossRef Hart AN, Zaske LA, Patterson KM, Drapeau C, Jensen GS. Natural killer cell activation and modulation of chemokine receptor profile in vitro by an extract from the cyanophyta Aphanizomenon flos-aquae. J Med Food. 2007 Sep;10(3):435–41.PubMedCrossRef
50.
go back to reference Jensen GS, Patterson KM, Yoon I. Yeast culture has anti-inflammatory effects and specifically activates NK cells. Comp Immunol Microbiol Infect Dis. 2008 Nov;31(6):487–500.PubMedCrossRef Jensen GS, Patterson KM, Yoon I. Yeast culture has anti-inflammatory effects and specifically activates NK cells. Comp Immunol Microbiol Infect Dis. 2008 Nov;31(6):487–500.PubMedCrossRef
51.
go back to reference Benson KF, Carter SG, Patterson KM, Patel D, Jensen GS. A novel extract from bovine colostrum whey supports anti-bacterial and anti-viral innate immune functions in vitro and in vivo: I. Enhanced immune activity in vitro translates to improved microbial clearance in animal infection models. Prev Med. 2012 May;54 Suppl:S116–23.PubMedCrossRef Benson KF, Carter SG, Patterson KM, Patel D, Jensen GS. A novel extract from bovine colostrum whey supports anti-bacterial and anti-viral innate immune functions in vitro and in vivo: I. Enhanced immune activity in vitro translates to improved microbial clearance in animal infection models. Prev Med. 2012 May;54 Suppl:S116–23.PubMedCrossRef
52.
go back to reference Benson KF, Beaman JL, Ou B, Okubena A, Okubena O, Jensen GS. West African Sorghum bicolor leaf sheaths have anti-inflammatory and immune-modulating properties in vitro. J Med Food. 2013 Mar;16(3):230–8.PubMedCrossRefPubMedCentral Benson KF, Beaman JL, Ou B, Okubena A, Okubena O, Jensen GS. West African Sorghum bicolor leaf sheaths have anti-inflammatory and immune-modulating properties in vitro. J Med Food. 2013 Mar;16(3):230–8.PubMedCrossRefPubMedCentral
53.
go back to reference Benson KF, Newman RA, Jensen GS. Antioxidant, anti-inflammatory, anti-apoptotic, and skin regenerative properties of an Aloe vera-based extract of Nerium oleander leaves (nae-8(®)). Clin Cosmet Investig Dermatol. 2015;8:239–48.PubMedPubMedCentral Benson KF, Newman RA, Jensen GS. Antioxidant, anti-inflammatory, anti-apoptotic, and skin regenerative properties of an Aloe vera-based extract of Nerium oleander leaves (nae-8(®)). Clin Cosmet Investig Dermatol. 2015;8:239–48.PubMedPubMedCentral
54.
go back to reference Benson KF, Newman RA, Jensen GS. Water-soluble egg membrane enhances the immunoactivating properties of an Aloe vera-based extract of Nerium oleander leaves. Clin Cosmet Investig Dermatol. 2016;9:393–403.PubMedCrossRefPubMedCentral Benson KF, Newman RA, Jensen GS. Water-soluble egg membrane enhances the immunoactivating properties of an Aloe vera-based extract of Nerium oleander leaves. Clin Cosmet Investig Dermatol. 2016;9:393–403.PubMedCrossRefPubMedCentral
55.
go back to reference Jensen GS, Redman KA, Benson KF, Carter SG, Mitzner MA, Reeves S, Robinson L. Antioxidant bioavailability and rapid immune-modulating effects after consumption of a single acute dose of a high-metabolite yeast immunogen: results of a placebo-controlled double-blinded crossover pilot study. J Med Food. 2011 Sep;14(9):1002–10.PubMedCrossRefPubMedCentral Jensen GS, Redman KA, Benson KF, Carter SG, Mitzner MA, Reeves S, Robinson L. Antioxidant bioavailability and rapid immune-modulating effects after consumption of a single acute dose of a high-metabolite yeast immunogen: results of a placebo-controlled double-blinded crossover pilot study. J Med Food. 2011 Sep;14(9):1002–10.PubMedCrossRefPubMedCentral
56.
go back to reference Jensen GS, Patel D, Benson KF. A novel extract from bovine colostrum whey supports innate immune functions. II. Rapid changes in cellular immune function in humans. Prev Med. 2012 May;54 Suppl:S124–9.PubMedCrossRef Jensen GS, Patel D, Benson KF. A novel extract from bovine colostrum whey supports innate immune functions. II. Rapid changes in cellular immune function in humans. Prev Med. 2012 May;54 Suppl:S124–9.PubMedCrossRef
57.
go back to reference Dons'koi BV, Chernyshov VP, Osypchuk DV. Measurement of NK activity in whole blood by the CD69 up-regulation after co-incubation with K562, comparison with NK cytotoxicity assays and CD107a degranulation assay. J Immunol Methods. 2011;372(1–2):187–95.PubMedCrossRef Dons'koi BV, Chernyshov VP, Osypchuk DV. Measurement of NK activity in whole blood by the CD69 up-regulation after co-incubation with K562, comparison with NK cytotoxicity assays and CD107a degranulation assay. J Immunol Methods. 2011;372(1–2):187–95.PubMedCrossRef
58.
go back to reference Borrego F, Robertson MJ, Ritz J, Peña J, Solana R. CD69 is a stimulatory receptor for natural killer cell and its cytotoxic effect is blocked by CD94 inhibitory receptor. Immunology. 1999;97(1):159–65.PubMedCrossRefPubMedCentral Borrego F, Robertson MJ, Ritz J, Peña J, Solana R. CD69 is a stimulatory receptor for natural killer cell and its cytotoxic effect is blocked by CD94 inhibitory receptor. Immunology. 1999;97(1):159–65.PubMedCrossRefPubMedCentral
59.
go back to reference Clausen J, Vergeiner B, Enk M, Petzer AL, Gastl G, Gunsilius E. Functional significance of the activation-associated receptors CD25 and CD69 on human NK-cells and NK-like T-cells. Immunobiology. 2003;207(2):85–93.PubMedCrossRef Clausen J, Vergeiner B, Enk M, Petzer AL, Gastl G, Gunsilius E. Functional significance of the activation-associated receptors CD25 and CD69 on human NK-cells and NK-like T-cells. Immunobiology. 2003;207(2):85–93.PubMedCrossRef
60.
go back to reference Benlahrech A, Donaghy H, Rozis G, Goodier M, Klavinskis L, Gotch F, Patterson S. Human NK cell up-regulation of CD69, HLA-DR, interferon γ secretion and cytotoxic activity by Plasmacytoid dendritic cells is regulated through overlapping but different pathways. Sensors (Basel). 2009;9(1):386–403.CrossRef Benlahrech A, Donaghy H, Rozis G, Goodier M, Klavinskis L, Gotch F, Patterson S. Human NK cell up-regulation of CD69, HLA-DR, interferon γ secretion and cytotoxic activity by Plasmacytoid dendritic cells is regulated through overlapping but different pathways. Sensors (Basel). 2009;9(1):386–403.CrossRef
61.
go back to reference Batbayar S, Kim MJ, Kim HW. Medicinal mushroom Lingzhi or Reishi, Ganoderma lucidum (W.Curt.:Fr.) P. karst., beta-glucan induces toll-like receptors and fails to induce inflammatory cytokines in NF-kappaB inhibitor-treated macrophages. Int J Med Mushrooms. 2011;13(3):213–25.PubMedCrossRef Batbayar S, Kim MJ, Kim HW. Medicinal mushroom Lingzhi or Reishi, Ganoderma lucidum (W.Curt.:Fr.) P. karst., beta-glucan induces toll-like receptors and fails to induce inflammatory cytokines in NF-kappaB inhibitor-treated macrophages. Int J Med Mushrooms. 2011;13(3):213–25.PubMedCrossRef
62.
go back to reference Jo E-K, Heo D-J, Kim J-H, Lee Y-H, Ju Y-C, Lee S-C. The effects of subcritical water treatment on antioxidant activity of Golden oyster mushroom. Food Bioprocess Technol. 2013;6:2555–61.CrossRef Jo E-K, Heo D-J, Kim J-H, Lee Y-H, Ju Y-C, Lee S-C. The effects of subcritical water treatment on antioxidant activity of Golden oyster mushroom. Food Bioprocess Technol. 2013;6:2555–61.CrossRef
63.
go back to reference Seo H-K, Lee S-C. Antioxidant activity of subcritical water extracts from Chaga mushroom (Inonotus obliquus). Sep Sci Technol. 2009;45(2):198–203.CrossRef Seo H-K, Lee S-C. Antioxidant activity of subcritical water extracts from Chaga mushroom (Inonotus obliquus). Sep Sci Technol. 2009;45(2):198–203.CrossRef
Metadata
Title
The mycelium of the Trametes versicolor (Turkey tail) mushroom and its fermented substrate each show potent and complementary immune activating properties in vitro
Authors
Kathleen F. Benson
Paul Stamets
Renee Davis
Regan Nally
Alex Taylor
Sonya Slater
Gitte S. Jensen
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Cytokines
Published in
BMC Complementary Medicine and Therapies / Issue 1/2019
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-019-2681-7

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