Yeast-Derived β-Glucan in Cancer: Novel Uses of a Traditional Therapeutic

Anne Geller, Rejeena Shrestha, Jun Yan, Anne Geller, Rejeena Shrestha, Jun Yan

Abstract

An increased understanding of the complex mechanisms at play within the tumor microenvironment (TME) has emphasized the need for the development of strategies that target immune cells within the TME. Therapeutics that render the TME immune-reactive have a vast potential for establishing effective cancer interventions. One such intervention is β-glucan, a natural compound with immune-stimulatory and immunomodulatory potential that has long been considered an important anti-cancer therapeutic. β-glucan has the ability to modulate the TME both by bridging the innate and adaptive arms of the immune system and by modulating the phenotype of immune-suppressive cells to be immune-stimulatory. New roles for β-glucan in cancer therapy are also emerging through an evolving understanding that β-glucan is involved in a concept called trained immunity, where innate cells take on memory phenotypes. Additionally, the hollow structure of particulate β-glucan has recently been harnessed to utilize particulate β-glucan as a delivery vesicle. These new concepts, along with the emerging success of combinatorial approaches to cancer treatment involving β-glucan, suggest that β-glucan may play an essential role in future strategies to prevent and inhibit tumor growth. This review emphasizes the various characteristics of β-glucan, with an emphasis on fungal β-glucan, and highlights novel approaches of β-glucan in cancer therapy.

Keywords: adjuvant; cancer; combination therapy; immunotherapy; metabolic reprogramming; trained immunity; yeast-derived β-Glucan.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
The modulation of the immune cells in the tumor microenvironment by β-glucan. β-glucan binds to the Dectin-1 receptors expressed on cells of the myeloid lineage, and will then be phagocytosed. In 1a, β-glucan can be seen binding to Dectin-1 on an M-MDSC. Binding to the M-MDSC will cause the M-MDSC to switch from a suppressive phenotype, to a DC phenotype that can act as an APC. This dendritic cell (DC) will then activate CD4+ and CD8+ T-cells, where CD4+ T-cells will secrete pro-inflammatory cytokines, such as TNFα and IFN-γ, and CD8+ T-cells will secrete Granzyme B, perforins and IFN-γ. The secretion of these pro-inflammatory cytokines by CD4+ and CD8+ T-cells will lead to the destruction of tumor cells. Similar to 1a, in 1b, β-glucan induces the polarization of suppressive M2 macrophages into inflammatory M1 macrophages. M1 macrophages will then activate Th1 type T-cells, leading to damage to the tumor cells through the secretion of pro-inflammatory cytokines by CD4+ and CD8+ T-cells. Finally, in 1c, β-glucan will bind to the Dectin-1 receptor on polymorphonuclear (PMN)-MDSCs and cause apoptosis of the cell. As the cell undergoes apoptosis, it will produce ROS that will ultimately target the tumor cells, leading to tumor cell death. Overall, these mechanisms together convert a suppressive tumor microenvironment (TME), to an inflammatory TME that has a greater potential to induce killing of tumors.

References

    1. Robert V.A., Casadevall A. Vertebrate Endothermy Restricts Most Fungi as Potential Pathogens. J. Infect. Dis. 2009;200:1623–1626. doi: 10.1086/644642.
    1. Owocki K., Kremer B., Wrzosek B., Królikowska A., Kaźmierczak J. Fungal Ferromanganese Mineralisation in Cretaceous Dinosaur Bones from the Gobi Desert, Mongolia. PLoS ONE. 2016;11:e0146293. doi: 10.1371/journal.pone.0146293.
    1. Maheshwari G., Sowrirajan S., Joseph B. Extraction and Isolation of beta-Glucan from Grain Sources-A Review. J. Food Sci. 2017;82:1535–1545. doi: 10.1111/1750-3841.13765.
    1. Ruffing A.M., Castro-Melchor M., Hu W.S., Chen R.R. Genome sequence of the curdlan-producing Agrobacterium sp. strain ATCC 31749. J. Bacteriol. 2011;193:4294–4295. doi: 10.1128/JB.05302-11.
    1. Batbayar S., Lee D.H., Kim H.W. Immunomodulation of Fungal β-Glucan in Host Defense Signaling by Dectin-1. Biomol. Ther. 2012;20:433–445. doi: 10.4062/biomolther.2012.20.5.433.
    1. Vannucci L., Krizan J., Sima P., Stakheev D., Caja F., Rajsiglova L., Horak V., Saieh M. Immunostimulatory properties and antitumor activities of glucans (Review) Int. J. Oncol. 2013;43:357–364. doi: 10.3892/ijo.2013.1974.
    1. Pillemer L., Ecker E.E. Anticomplementary factor in fresh yeast. J. Biol. Chem. 1941;137:139–142.
    1. Riggi S.J., Di Luzio N.R. Identification of a reticuloendothelial stimulating agent in zymosan. Am. J. Physiol. 1961;200:297–300. doi: 10.1152/ajplegacy.1961.200.2.297.
    1. Synytsya A., Novák M. Structural diversity of fungal glucans. Carbohydr. Polym. 2013;92:792–809. doi: 10.1016/j.carbpol.2012.09.077.
    1. Chen J., Seviour R. Medicinal importance of fungal beta-(1->3), (1->6)-glucans. Mycol. Res. 2007;111:635–652. doi: 10.1016/j.mycres.2007.02.011.
    1. Dong Q., Yao J., Yang X., Fang J. Structural characterization of a water-soluble β-d-glucan from fruiting bodies of Agaricus blazei Murr. Carbohydr. Res. 2002;337:1417–1421. doi: 10.1016/S0008-6215(02)00166-0.
    1. Ge Q., Zhang A.Q., Sun P.L. Isolation, purification and structural characterization of a novel water-soluble glucan from the fruiting bodies of phellinus baumii pilát. J. Food Biochem. 2010;34:1205–1215. doi: 10.1111/j.1745-4514.2010.00359.x.
    1. Mandal S., Maity K.K., Bhunia S.K., Dey B., Patra S., Sikdar S.R., Islam S.S. Chemical analysis of new water-soluble (1→6)-, (1→4)-α, β-glucan and water-insoluble (1→3)-, (1→4)-β-glucan (Calocyban) from alkaline extract of an edible mushroom, Calocybe indica (Dudh Chattu) Carbohydr. Res. 2010;345:2657–2663. doi: 10.1016/j.carres.2010.10.005.
    1. Chakraborty I., Mondal S., Pramanik M., Rout D., Islam S.S. Structural investigation of a water-soluble glucan from an edible mushroom, Astraeus hygrometricus. Carbohydr. Res. 2004;339:2249–2254. doi: 10.1016/j.carres.2004.07.013.
    1. Lowman D.W., West L.J., Bearden D.W., Wempe M.F., Power T.D., Ensley H.E., Haynes K., Williams D.L., Kruppa M.D. New insights into the structure of (1->3,1->6)-beta-D-glucan side chains in the Candida glabrata cell wall. PLoS ONE. 2011;6:e27614. doi: 10.1371/journal.pone.0027614.
    1. Chan G.C.F., Chan W.K., Sze D.M.Y. The effects of beta-glucan on human immune and cancer cells. J. Hematol. Oncol. 2009;2:25. doi: 10.1186/1756-8722-2-25.
    1. Stier H., Ebbeskotte V., Gruenwald J. Immune-modulatory effects of dietary Yeast Beta-1,3/1,6-D-glucan. Nutr. J. 2014;13:38. doi: 10.1186/1475-2891-13-38.
    1. Rice P.J., Kelley J.L., Kogan G., Ensley H.E., Kalbfleisch J.H., Browder I.W., Williams D.L. Human monocyte scavenger receptors are pattern recognition receptors for (1->3)-beta-D-glucans. J. Leukoc. Biol. 2002;72:140–146.
    1. Zimmerman J.W., Lindermuth J., Fish P.A., Palace G.P., Stevenson T.T., DeMong D.E. A novel carbohydrate-glycosphingolipid interaction between a beta-(1-3)-glucan immunomodulator, PGG-glucan, and lactosylceramide of human leukocytes. J. Biol. Chem. 1998;273:22014–22020. doi: 10.1074/jbc.273.34.22014.
    1. Cain J.A., Newman S.L., Ross G.D. Role of complement receptor type three and serum opsonins in the neutrophil response to yeast. Complement. 1987;4:75–86. doi: 10.1159/000463011.
    1. Ariizumi K., Shen G.L., Shikano S., Xu S., Ritter R., Kumamoto T., Edelbaum D., Morita A., Bergstresser P.R., Takashima A. Identification of a novel, dendritic cell-associated molecule, dectin-1, by subtractive cDNA cloning. J. Biol. Chem. 2000;275:20157–20167. doi: 10.1074/jbc.M909512199.
    1. Taylor P.R., Brown G.D., Reid D.M., Willment J.A., Martinez-Pomares L., Gordon S., Wong S.Y. The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J. Immunol. 2002;169:3876–3882. doi: 10.4049/jimmunol.169.7.3876.
    1. Brown G.D. Dectin-1: A signalling non-TLR pattern-recognition receptor. Nat. Rev. Immunol. 2006;6:33–43. doi: 10.1038/nri1745.
    1. Reid D.M., Gow N.A., Brown G.D. Pattern recognition: Recent insights from Dectin-1. Curr. Opin. Immunol. 2009;21:30–37. doi: 10.1016/j.coi.2009.01.003.
    1. Brown G.D., Herre J., Williams D.L., Willment J.A., Marshall A.S., Gordon S. Dectin-1 mediates the biological effects of beta-glucans. J. Exp. Med. 2003;197:1119–1124. doi: 10.1084/jem.20021890.
    1. Herre J., Marshall A.S., Caron E., Edwards A.D., Williams D.L., Schweighoffer E., Tybulewicz V., Reise Sousa C., Gordon S., Brown G.D. Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood. 2004;104:4038–4045. doi: 10.1182/blood-2004-03-1140.
    1. Camilli G., Tabouret G., Quintin J. The Complexity of Fungal β-Glucan in Health and Disease: Effects on the Mononuclear Phagocyte System. Front. Immunol. 2018;9:673. doi: 10.3389/fimmu.2018.00673.
    1. O’Brien X.M., Heflin K.E., Lavigne L.M., Yu K., Kim M., Salomon A.R., Reichner J.S. Lectin Site Ligation of CR3 Induces Conformational Changes and Signaling. J. Biol. Chem. 2012;287:3337–3348. doi: 10.1074/jbc.M111.298307.
    1. Vetvicka V., Thornton B.P., Ross G.D. Soluble beta-glucan polysaccharide binding to the lectin site of neutrophil or natural killer cell complement receptor type 3 (CD11b/CD18) generates a primed state of the receptor capable of mediating cytotoxicity of iC3b-opsonized target cells. J. Clin. Invest. 1996;98:50–61. doi: 10.1172/JCI118777.
    1. Vetvicka V., Vetvickova J. 1, 3-Glucan: Silver Bullet or Hot Air? Open Glycosci. 2010;3:1–6.
    1. Sletmoen M., Stokke B.T. Higher order structure of (1,3)-beta-D-glucans and its influence on their biological activities and complexation abilities. Biopolymers. 2008;89:310–321. doi: 10.1002/bip.20920.
    1. Brown G.D., Gordon S. Fungal beta-glucans and mammalian immunity. Immunity. 2003;19:311–315. doi: 10.1016/S1074-7613(03)00233-4.
    1. Volman J.J., Ramakers J.D., Plat J. Dietary modulation of immune function by beta-glucans. Physiol. Behav. 2008;94:276–284. doi: 10.1016/j.physbeh.2007.11.045.
    1. Suzuki I., Hashimoto K., Ohno N., Tanaka H., Yadomae T. Immunomodulation by orally administered beta-glucan in mice. Int. J. Immunopharmacol. 1989;11:761–769. doi: 10.1016/0192-0561(89)90130-6.
    1. De Graaff P., Govers C., Wichers H.J., Debets R. Consumption of beta-glucans to spice up T cell treatment of tumors: A review. Expert Opin. Biol. Ther. 2018;18:1023–1040. doi: 10.1080/14712598.2018.1523392.
    1. Li B., Cai Y., Qi C., Hansen R., Ding C., Mitchell T.C., Yan J. Orally administered particulate beta-glucan modulates tumor-capturing dendritic cells and improves antitumor T-cell responses in cancer. Clin. Cancer Res. 2010;16:5153–5164. doi: 10.1158/1078-0432.CCR-10-0820.
    1. Xia Y., Ross G.D. Generation of recombinant fragments of CD11b expressing the functional beta-glucan-binding lectin site of CR3 (CD11b/CD18) J. Immunol. 1999;162:7285–7293.
    1. Hong F., Yan J., Baran J.T., Allendorf D.J., Hansen R.D., Ostroff G.R., Xing P.X., Cheung N.K., Ross G.D. Mechanism by which orally administered β-1, 3-glucans enhance the tumoricidal activity of antitumor monoclonal antibodies in murine tumor models. J. Immunol. 2004;173:797–806. doi: 10.4049/jimmunol.173.2.797.
    1. Mitroulis I., Ruppova K., Wang B., Chen L.S., Grzybek M., Grinenko T., Eugster A., Troullinaki M., Palladini A., Kourtzelis I., et al. Modulation of Myelopoiesis Progenitors Is an Integral Component of Trained Immunity. Cell. 2018;172:147–161. doi: 10.1016/j.cell.2017.11.034.
    1. Suzuki I., Tanaka H., Kinoshita A., Oikawa S., Osawa M., Yadomae T. Effect of orally administered beta-glucan on macrophage function in mice. Int. J. Immunopharmacol. 1990;12:675–684. doi: 10.1016/0192-0561(90)90105-V.
    1. Małaczewska J., Wojcik R., Jung L., Siwicki A. The effect of Biolex Beta-HP on the selected parameters of biochemical, specific and non-specific humoral and cellular immunity in rats. Bull. Vet. Inst. Pulawy. 2010;54:75–80.
    1. Leentjens J., Quintin J., Gerretsen J., Kox M., Pickkers P., Netea M.G. The Effects of Orally Administered Beta-Glucan on Innate Immune Responses in Humans, a Randomized Open-Label Intervention Pilot-Study. PLoS ONE. 2014;9:e108794. doi: 10.1371/journal.pone.0108794.
    1. Li B., Allendorf D.J., Hansen R., Marroquin J., Ding C., Cramer D.E., Yan J. Yeast β-Glucan Amplifies Phagocyte Killing of iC3b-Opsonized Tumor Cells via Complement Receptor 3-Syk-Phosphatidylinositol 3-Kinase Pathway. J. Immunol. 2006;177:1661–1669. doi: 10.4049/jimmunol.177.3.1661.
    1. Akramiene D., Kondrotas A., Didziapetriene J., Kevelaitis E. Effects of beta-glucans on the immune system. Medicina. 2007;43:597–606. doi: 10.3390/medicina43080076.
    1. Babineau T.J., Hackford A., Kenler A., Bistrian B., Forse R.A., Fairchild P.G., Heard S., Keroack M., Caushaj P., Benotti P. A phase II multicenter, double-blind, randomized, placebo-controlled study of three dosages of an immunomodulator (PGG-glucan) in high-risk surgical patients. Arch. Surg. 1994;129:1204–1210. doi: 10.1001/archsurg.1994.01420350102014.
    1. De Felippe Junior J., da Rocha e Silva Junior M., Maciel F.M., Soares Ade M., Mendes N.F. Infection prevention in patients with severe multiple trauma with the immunomodulator beta 1–3 polyglucose (glucan) Surg. Gynecol. Obstet. 1993;177:383–388.
    1. Babineau T.J., Marcello P., Swails W., Kenler A., Bistrian B., Forse R.A. Randomized phase I/II trial of a macrophage-specific immunomodulator (PGG-glucan) in high-risk surgical patients. Ann. Surg. 1994;220:601–609. doi: 10.1097/00000658-199411000-00002.
    1. Vetvicka V., Vetvickova J. A Comparison of Injected and Orally Administered β-glucans. J. Am. Nutraceutical Assoc. 2008;11:42–49.
    1. Zheng X., Fuling Z., Xu X., Zhang L. Uptake of intraperitoneally administrated triple helical β-glucan for antitumor in murine tumor models. J. Mater. Chem. B. 2017;5:9337–9345. doi: 10.1039/C7TB02649H.
    1. Zheng X., Lu F., Xu X., Zhang L. Extended chain conformation of β-glucan and its effect on antitumor activity. J. Mater. Chem. B. 2017;5:5623–5631. doi: 10.1039/C7TB01324H.
    1. Balkwill F.R., Capasso M., Hagemann T. The Tumor Microenvironment at a Glance. The Company of Biologists Ltd.; Cambridge, UK: 2012.
    1. Devaud C., John L.B., Westwood J.A., Darcy P.K., Kershaw M.H.J.O. Immune modulation of the tumor microenvironment for enhancing cancer immunotherapy. Oncoimmunology. 2013;2:e25961. doi: 10.4161/onci.25961.
    1. Whiteside T.J.O. The tumor microenvironment and its role in promoting tumor growth. Oncogene. 2008;27:5904. doi: 10.1038/onc.2008.271.
    1. Croci D.O., Fluck M.F.Z., Rico M.J., Matar P., Rabinovich G.A., Scharovsky O.G. Dynamic cross-talk between tumor and immune cells in orchestrating the immunosuppressive network at the tumor microenvironment. Cancer Immunol. Immunother. 2007;56:1687–1700. doi: 10.1007/s00262-007-0343-y.
    1. Wang X., Peralta S., Moraes C.T. Advances in Cancer Research. Volume 119. Elsevier; Amsterdam, The Netherlands: 2013. Mitochondrial alterations during carcinogenesis: A review of metabolic transformation and targets for anticancer treatments; pp. 127–160.
    1. Zhang M., Kim J.A., Huang A.Y. Optimizing Tumor Microenvironment for Cancer Immunotherapy: β-Glucan-Based Nanoparticles. Front. Immunol. 2018;9:341. doi: 10.3389/fimmu.2018.00341.
    1. Gantner B.N., Simmons R.M., Canavera S.J., Akira S., Underhill D.M. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 2003;197:1107–1117. doi: 10.1084/jem.20021787.
    1. Qi C., Cai Y., Gunn L., Ding C., Li B., Kloecker G., Qian K., Vasilakos J., Saijo S., Iwakura Y.J.B. Differential pathways regulating innate and adaptive antitumor immune responses by particulate and soluble yeast-derived β-glucans. Blood. 2011;117:6825–6836. doi: 10.1182/blood-2011-02-339812.
    1. Xia Y., Větvička V., Yan J., Hanikýřová M., Mayadas T., Ross G.D. The β-glucan-binding lectin site of mouse CR3 (CD11b/CD18) and its function in generating a primed state of the receptor that mediates cytotoxic activation in response to iC3b-opsonized target cells. J. Immunol. 1999;162:2281–2290.
    1. Wu T.C., Xu K., Banchereau R., Marches F., Chun I.Y., Martinek J., Anguiano E., Pedroza-Gonzalez A., Snipes G.J., O’Shaughnessy J. Reprogramming tumor-infiltrating dendritic cells for CD103+ CD8+ mucosal T-cell differentiation and breast cancer rejection. Cancer Immunol. Res. 2014;2:487–500. doi: 10.1158/2326-6066.CIR-13-0217.
    1. Osorio F., LeibundGut-Landmann S., Lochner M., Lahl K., Sparwasser T., Eberl G., Reis e Sousa C. DC activated via dectin-1 convert Treg into IL-17 producers. Eur. J. Immunol. 2008;38:3274–3281. doi: 10.1002/eji.200838950.
    1. Mantovani A.J.N. Cancer: Inflaming metastasis. Nature. 2009;457:36. doi: 10.1038/457036b.
    1. Campbell M.J., Tonlaar N.Y., Garwood E.R., Huo D., Moore D.H., Khramtsov A.I., Au A., Baehner F., Chen Y., Malaka D.O., et al. Proliferating macrophages associated with high grade, hormone receptor negative breast cancer and poor clinical outcome. Breast Cancer Res. Treat. 2011;128:703–711. doi: 10.1007/s10549-010-1154-y.
    1. Chung F.T., Lee K.Y., Wang C.W., Heh C.C., Chan Y.F., Chen H.W., Kuo C.H., Feng P.H., Lin T.Y., Wang C.H. Tumor-associated macrophages correlate with response to epidermal growth factor receptor-tyrosine kinase inhibitors in advanced non-small cell lung cancer. Int. J. Cancer. 2012;131:E227–E235. doi: 10.1002/ijc.27403.
    1. Liu M., Luo F., Ding C., Albeituni S., Hu X., Ma Y., Cai Y., McNally L., Sanders M.A., Jain D. Dectin-1 activation by a natural product β-glucan converts immunosuppressive macrophages into an M1-like phenotype. J. Immunol. 2015;195:5055–5065. doi: 10.4049/jimmunol.1501158.
    1. Albeituni S.H., Ding C., Liu M., Hu X., Luo F., Kloecker G., Bousamra M., Zhang H.G., Yan J. Yeast-derived particulate β-glucan treatment subverts the suppression of myeloid-derived suppressor cells (MDSC) by inducing polymorphonuclear MDSC apoptosis and monocytic MDSC differentiation to APC in cancer. J. Immunol. 2016;196:2167–2180. doi: 10.4049/jimmunol.1501853.
    1. Ali M.F., Driscoll C.B., Walters P.R., Limper A.H., Carmona E.M. β-glucan–activated human B lymphocytes participate in innate immune responses by releasing proinflammatory cytokines and stimulating neutrophil chemotaxis. J. Immunol. 2015;195:5318–5326. doi: 10.4049/jimmunol.1500559.
    1. Harnack U., Kellermann U., Pecher G. Yeast-derived beta-(1-3),(1-6)-D-glucan induces up-regulation of CD86 on dectin-1-positive human B-lymphoma cell lines. Anticancer Res. 2011;31:4195–4199.
    1. Warburg O. On the origin of cancer cells. Science. 1956;123:309–314. doi: 10.1126/science.123.3191.309.
    1. Biswas S.K., Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: Cancer as a paradigm. Nat. Immunol. 2010;11:889. doi: 10.1038/ni.1937.
    1. Puig-Kroger A., Sierra-Filardi E., Dominguez-Soto A., Samaniego R., Corcuera M.T., Gomez-Aguado F., Ratnam M., Sanchez-Mateos P., Corbi A.L. Folate receptor beta is expressed by tumor-associated macrophages and constitutes a marker for M2 anti-inflammatory/regulatory macrophages. Cancer Res. 2009;69:9395–9403. doi: 10.1158/0008-5472.CAN-09-2050.
    1. Recalcati S., Locati M., Marini A., Santambrogio P., Zaninotto F., De Pizzol M., Zammataro L., Girelli D., Cairo G. Differential regulation of iron homeostasis during human macrophage polarized activation. Eur. J. Immunol. 2010;40:824–835. doi: 10.1002/eji.200939889.
    1. Rodriguez-Prados J.C., Traves P.G., Cuenca J., Rico D., Aragones J., Martin-Sanz P., Cascante M., Bosca L. Substrate fate in activated macrophages: A comparison between innate, classic, and alternative activation. J. Immunol. 2010;185:605–614. doi: 10.4049/jimmunol.0901698.
    1. Jha A.K., Huang S.C.C., Sergushichev A., Lampropoulou V., Ivanova Y., Loginicheva E., Chmielewski K., Stewart K.M., Ashall J., Everts B., et al. Network Integration of Parallel Metabolic and Transcriptional Data Reveals Metabolic Modules that Regulate Macrophage Polarization. Immunity. 2015;42:419–430. doi: 10.1016/j.immuni.2015.02.005.
    1. Cheng S.C., Quintin J., Cramer R.A., Shepardson K.M., Saeed S., Kumar V., Giamarellos-Bourboulis E.J., Martens J.H., Rao N.A., Aghajanirefah A., et al. mTOR-and HIF-1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science. 2014;345:1250684. doi: 10.1126/science.1250684.
    1. Mourits V.P., Wijkmans J.C.H.M., Joosten L.A.B., Netea M.G. Trained immunity as a novel therapeutic strategy. Curr. Opin. Pharmacol. 2018;41:52–58. doi: 10.1016/j.coph.2018.04.007.
    1. Arts R.J.W., Moorlag S., Novakovic B., Li Y., Wang S.Y., Oosting M., Kumar V., Xavier R.J., Wijmenga C., Joosten L.A.B., et al. BCG Vaccination Protects against Experimental Viral Infection in Humans through the Induction of Cytokines Associated with Trained Immunity. Cell Host Microbe. 2018;23:89–100. doi: 10.1016/j.chom.2017.12.010.
    1. Van der Meer J.W.M., Joosten L.A.B., Riksen N., Netea M.G. Trained immunity: A smart way to enhance innate immune defence. Mol. Immunol. 2015;68:40–44. doi: 10.1016/j.molimm.2015.06.019.
    1. Netea M.G., Quintin J., van der Meer J.W. Trained Immunity: A Memory for Innate Host Defense. Cell Host Microbe. 2011;9:355–361. doi: 10.1016/j.chom.2011.04.006.
    1. Quintin J., Saeed S., Martens J.H.A., Giamarellos-Bourboulis E.J., Ifrim D.C., Logie C., Jacobs L., Jansen T., Kullberg B.J., Wijmenga C., et al. Candida albicans Infection Affords Protection against Reinfection via Functional Reprogramming of Monocytes. Cell Host Microbe. 2012;12:223–232. doi: 10.1016/j.chom.2012.06.006.
    1. Novakovic B., Habibi E., Wang S.Y., Arts R.J.W., Davar R., Megchelenbrink W., Kim B., Kuznetsova T., Kox M., Zwaag J., et al. β-Glucan Reverses the Epigenetic State of LPS-Induced Immunological Tolerance. Cell. 2016;167:1354–1368. doi: 10.1016/j.cell.2016.09.034.
    1. Bekkering S., Arts R.J.W., Novakovic B., Kourtzelis I., van der Heijden C., Li Y., Popa C.D., Ter Horst R., van Tuijl J., Netea-Maier R.T., et al. Metabolic Induction of Trained Immunity through the Mevalonate Pathway. Cell. 2018;172:135–146. doi: 10.1016/j.cell.2017.11.025.
    1. Buffen K., Oosting M., Quintin J., Ng A., Kleinnijenhuis J., Kumar V., van de Vosse E., Wijmenga C., van Crevel R., Oosterwijk E., et al. Autophagy Controls BCG-Induced Trained Immunity and the Response to Intravesical BCG Therapy for Bladder Cancer. PLoS Pathog. 2014;10:e1004485. doi: 10.1371/journal.ppat.1004485.
    1. Zhang Y., Morgan M.J., Chen K., Choksi S., Liu Z.G. Induction of autophagy is essential for monocyte-macrophage differentiation. Blood. 2012;119:2895–2905. doi: 10.1182/blood-2011-08-372383.
    1. Zhang Y., Choksi S., Liu Z. Chapter 12—Autophagy Is Required During Monocyte–Macrophage Differentiation. In: Hayat M.A., editor. Autophagy: Cancer, Other Pathologies, Inflammation, Immunity, Infection, and Aging. Academic Press; Amsterdam, The Netherlands: 2015. pp. 195–206.
    1. Germic N., Frangez Z., Yousefi S., Simon H.U. Regulation of the innate immune system by autophagy: Monocytes, macrophages, dendritic cells and antigen presentation. Cell Death Differ. 2019;26:715–727. doi: 10.1038/s41418-019-0297-6.
    1. Nardin A., Lefebvre M.L., Labroquere K., Faure O., Abastado J.P. Liposomal muramyl tripeptide phosphatidylethanolamine: Targeting and activating macrophages for adjuvant treatment of osteosarcoma. Curr. Cancer Drug Targets. 2006;6:123–133. doi: 10.2174/156800906776056473.
    1. Morales A., Eidinger D., Bruce A.W. Intracavitary Bacillus Calmette-Guerin in the treatment of superficial bladder tumors. J. Urol. 1976;116:180–183. doi: 10.1016/S0022-5347(17)58737-6.
    1. Luo Y., Knudson M.J. Mycobacterium bovis bacillus Calmette-Guerin-induced macrophage cytotoxicity against bladder cancer cells. Clin. Dev. Immunol. 2010;2010:357591. doi: 10.1155/2010/357591.
    1. Kawai K., Miyazaki J., Joraku A., Nishiyama H., Akaza H. Bacillus Calmette-Guerin (BCG) immunotherapy for bladder cancer: Current understanding and perspectives on engineered BCG vaccine. Cancer Sci. 2013;104:22–27. doi: 10.1111/cas.12075.
    1. Alexander M.P., Fiering S.N., Ostroff G.R., Cramer R.A., Mullins D.W. Beta-glucan-induced trained innate immunity mediates antitumor efficacy in the mouse lung. J. Immunol. 2016;196:1731–1742.
    1. Alexander M.P., Fiering S.N. Beta-glucan-induced inflammatory monocytes mediate antitumor efficacy in the murine lung. Cancer Immunol. Immunother. 2018;67:1731–1742. doi: 10.1007/s00262-018-2234-9.
    1. Netea M.G., Joosten L.A.B., van der Meer J.W.M. Hypothesis: Stimulation of trained immunity as adjunctive immunotherapy in cancer. J. Leukoc. Biol. 2017;102:1323–1332. doi: 10.1189/jlb.5RI0217-064RR.
    1. Sancho D., Reis e Sousa C. Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu. Rev. Immunol. 2012;30:491–529. doi: 10.1146/annurev-immunol-031210-101352.
    1. Greten F.R., Eckmann L., Greten T.F., Park J.M., Li Z.W., Egan L.J., Kagnoff M.F., Karin M.J.C. IKKβ links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell. 2004;118:285–296. doi: 10.1016/j.cell.2004.07.013.
    1. Maeda S., Kamata H., Luo J.L., Leffert H., Karin M.J.C. IKKβ couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell. 2005;121:977–990. doi: 10.1016/j.cell.2005.04.014.
    1. Connelly L., Barham W., Onishko H.M., Chen L., Sherrill T.P., Zabuawala T., Ostrowski M.C., Blackwell T.S., Yull F.E. NF-kappaB activation within macrophages leads to an anti-tumor phenotype in a mammary tumor lung metastasis model. Breast Cancer Res. 2011;13:R83. doi: 10.1186/bcr2935.
    1. Elder M.J., Webster S.J., Chee R., Williams D.L., Hill Gaston J.S., Goodall J.C. β-Glucan Size Controls Dectin-1-Mediated Immune Responses in Human Dendritic Cells by Regulating IL-1β Production. Front. Immunol. 2017;8:791. doi: 10.3389/fimmu.2017.00791.
    1. Gordon S. The macrophage: Past, present and future. Eur. J. Immunol. 2007;37(Suppl. 1):S9–S17. doi: 10.1002/eji.200737638.
    1. Zhang X., Edwards J.P., Mosser D.M. The expression of exogenous genes in macrophages: Obstacles and opportunities. Methods Mol. Biol. 2009;531:123–143. doi: 10.1007/978-1-59745-396-7_9.
    1. Basha G., Novobrantseva T.I., Rosin N., Tam Y.Y., Hafez I.M., Wong M.K., Sugo T., Ruda V.M., Qin J., Klebanov B., et al. Influence of cationic lipid composition on gene silencing properties of lipid nanoparticle formulations of siRNA in antigen-presenting cells. Mol. Ther. J. Am. Soc. Gene Ther. 2011;19:2186–2200. doi: 10.1038/mt.2011.190.
    1. Semple S.C., Akinc A., Chen J., Sandhu A.P., Mui B.L., Cho C.K., Sah D.W., Stebbing D., Crosley E.J., Yaworski E., et al. Rational design of cationic lipids for siRNA delivery. Nat. Biotechnol. 2010;28:172–176. doi: 10.1038/nbt.1602.
    1. Zhang M., Gao Y., Caja K., Zhao B., Kim J.A. Non-Viral Nanoparticle Delivers Small Interfering RNA to Macrophages In Vitro and In Vivo. PLoS ONE. 2015;10:e0118472. doi: 10.1371/journal.pone.0118472.
    1. Soto E.R., Caras A.C., Kut L.C., Castle M.K., Ostroff G.R. Glucan Particles for Macrophage Targeted Delivery of Nanoparticles. J. Drug Deliv. 2012;2012:13. doi: 10.1155/2012/143524.
    1. Bach J.P., Rinn B., Meyer B., Dodel R., Bacher M. Role of MIF in Inflammation and Tumorigenesis. Oncology. 2008;75:127–133. doi: 10.1159/000155223.
    1. Zhang M., Yan L., Kim J.A. Modulating mammary tumor growth, metastasis and immunosuppression by siRNA-induced MIF reduction in tumor microenvironment. Cancer Gene Ther. 2015;22:463–474. doi: 10.1038/cgt.2015.42.
    1. Aouadi M., Tesz G.J., Nicoloro S.M., Wang M., Chouinard M., Soto E., Ostroff G.R., Czech M.P. Orally delivered siRNA targeting macrophage Map4k4 suppresses systemic inflammation. Nature. 2009;458:1180. doi: 10.1038/nature07774.
    1. Tesz G.J., Aouadi M., Prot M., Nicoloro S.M., Boutet E., Amano S.U., Goller A., Wang M., Guo C.A., Salomon W.E., et al. Glucan particles for selective delivery of siRNA to phagocytic cells in mice. Biochem. J. 2011;436:351–362. doi: 10.1042/BJ20110352.
    1. Patel A.G., Kaufmann S.H. How does doxorubicin work? Elife. 2012;1:e00387. doi: 10.7554/eLife.00387.
    1. Hwang J., Lee K., Gilad A., Choi J. Synthesis of Beta-glucan Nanoparticles for the Delivery of Single Strand DNA. Biotechnol. Bioprocess Eng. 2018;23:144–149. doi: 10.1007/s12257-018-0003-4.
    1. Hollingsworth M.A., Swanson B.J. Mucins in cancer: Protection and control of the cell surface. Nat. Rev. Cancer. 2004;4:45–60. doi: 10.1038/nrc1251.
    1. Berner V.K., duPre S.A., Redelman D., Hunter K.W. Microparticulate β-glucan vaccine conjugates phagocytized by dendritic cells activate both naïve CD4 and CD8 T cells in vitro. Cell. Immunol. 2015;298:104–114. doi: 10.1016/j.cellimm.2015.10.007.
    1. Wang H., Yang B., Wang Y., Liu F., Fernandez-Tejada A., Dong S. beta-Glucan as an immune activator and a carrier in the construction of a synthetic MUC1 vaccine. Chem. Commun. 2018;55:253–256. doi: 10.1039/C8CC07691J.
    1. Jackson H.J., Rafiq S., Brentjens R.J. Driving CAR T-cells forward. Nat. Rev. Clin. Oncol. 2016;13:370. doi: 10.1038/nrclinonc.2016.36.
    1. Morales J.K., Kmieciak M., Graham L., Feldmesser M., Bear H.D., Manjili M.H. Adoptive transfer of HER2/neu-specific T cells expanded with alternating gamma chain cytokines mediate tumor regression when combined with the depletion of myeloid-derived suppressor cells. Cancer Immunol. Immunother. 2009;58:941. doi: 10.1007/s00262-008-0609-z.
    1. Ma C., Montalvo W., Yagita H., Allison J.P. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc. Natl. Acad. Sci. USA. 2010;107:4275–4280.
    1. Quail D.F., Joyce J.A. Microenvironmental regulation of tumor progression and metastasis. Nat. Med. 2013;19:1423. doi: 10.1038/nm.3394.
    1. Jin Y., Li P., Wang F. β-glucans as potential immunoadjuvants: A review on the adjuvanticity, structure-activity relationship and receptor recognition properties. Vaccine. 2018;36:5235–5244. doi: 10.1016/j.vaccine.2018.07.038.
    1. Hong F., Hansen R.D., Yan J., Allendorf D.J., Baran J.T., Ostroff G.R., Ross G.D. β-Glucan functions as an adjuvant for monoclonal antibody immunotherapy by recruiting tumoricidal granulocytes as killer cells. Cancer Res. 2003;63:9023–9031.
    1. Kushner B.H., Cheung I.Y., Modak S., Kramer K., Ragupathi G., Cheung N.K. Phase I trial of a bivalent gangliosides vaccine in combination with beta-glucan for high-risk neuroblastoma in second or later remission. Clin. Cancer Res. 2014;20:1375–1382. doi: 10.1158/1078-0432.CCR-13-1012.
    1. Modak S., Kushner B.H., Kramer K., Vickers A., Cheung I.Y., Cheung N.K.V. Anti-GD2 antibody 3F8 and barley-derived (1→3), (1→4)-β-D-glucan: A Phase I study in patients with chemoresistant neuroblastoma. Oncoimmunology. 2013;2:e23402. doi: 10.4161/onci.23402.
    1. Hirschowitz E.A., Mullins A., Prajapati D., Baeker T., Kloecker G., Foody T., Damron K., Love C., Yannelli J.R. Pilot study of 1650-G: A simplified cellular vaccine for lung cancer. J. Thorac. Oncol. 2011;6:169–173. doi: 10.1097/JTO.0b013e3181fb5c22.
    1. O’Day S., Borges V., Chmielowski B., Rao R., Abu-Khalaf M., Stopeck A., Lowe J., Mattson P., Breuer K., Gargano M., et al. Abstract P2-09-08: Imprime PGG, a novel innate immune modulator, combined with pembrolizumab in a phase 2 multicenter, open label study in chemotherapy-resistant metastatic triple negative breast cancer (TNBC) Cancer Res. 2019;79:P2–P9.
    1. Fraser K., Chan A., Fulton R., Leonardo S., Jonas A., Qiu X., Ottoson N., Kangas T., Gordon K., Graff J. Imprime PGG triggers PD-L1 expression on tumor and myeloid cells and prevents tumor establishment in combination with αPD-L1 treatment in vivo. Cancer Res. 2016;76 doi: 10.1158/1538-7445.
    1. Qiu X., Chan A.S., Jonas A.B., Kangas T., Ottoson N.R., Graff J.R., Bose N. Imprime PGG, a yeast β-glucan PAMP elicits a coordinated immune response in combination with anti-PD1 antibody. Am. Assoc. Immnol. 2016;196:16.
    1. Weitberg A.B. A phase I/II trial of beta-(1, 3)/(1, 6) D-glucan in the treatment of patients with advanced malignancies receiving chemotherapy. J. Exp. Clin. Cancer Res. 2008;27:40. doi: 10.1186/1756-9966-27-40.
    1. Segal N.H., Gada P., Senzer N., Gargano M.A., Patchen M.L., Saltz L.B. A phase II efficacy and safety, open-label, multicenter study of imprime PGG injection in combination with cetuximab in patients with stage IV KRAS-mutant colorectal cancer. Clin. Colorectal Cancer. 2016;15:222–227. doi: 10.1016/j.clcc.2016.02.013.
    1. Thomas M., Sadjadian P., Kollmeier J., Lowe J., Mattson P., Trout J.R., Gargano M., Patchen M.L., Walsh R., Beliveau M., et al. A randomized, open-label, multicenter, phase II study evaluating the efficacy and safety of BTH1677 (1,3-1,6 beta glucan; Imprime PGG) in combination with cetuximab and chemotherapy in patients with advanced non-small cell lung cancer. Investig. New Drugs. 2017;35:345–358. doi: 10.1007/s10637-017-0450-3.
    1. Jacobson C.A., Redd R., Reynolds C., Fields M., Armand P., Fisher D.C., Jacobsen E.D., LaCasce A.S., Bose N., Ottoson N., et al. A phase 2 clinical trial of rituximab and β-glucan pgg in relapsed/refractory indolent B-cell non-hodgkin lymphoma. Hematol. Oncol. 2019;37:521–523. doi: 10.1002/hon.207_2631.

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