C-Type Lectin Receptors-Triggered Antifungal Immunity May Synergize with and Optimize the Effects of Immunotherapy in Hepatocellular Carcinoma

References

• Llovet JM, Kelley RK, Villanueva A, et al. Hepatocellular carcinoma. Nat Rev Dis Primers. 2021;7(1):6. doi:10.1038/s41572-020-00240-3
   PubMed Web of Science ®Google Scholar
• Nault JC, Villanueva A. Biomarkers for hepatobiliary cancers. Hepatology. 2021;73(Suppl 1):115–127. doi:10.1002/hep.31175
   PubMed Web of Science ®Google Scholar
• Sonbol MB, Riaz IB, Naqvi SAA, et al. Systemic therapy and sequencing options in advanced hepatocellular carcinoma: a systematic review and network meta-analysis. JAMA Oncol. 2020;6(12):e204930. doi:10.1001/jamaoncol.2020.4930
   PubMed Web of Science ®Google Scholar
• Rizzo A, Nannini M, Novelli M, et al. Dose reduction and discontinuation of standard-dose regorafenib associated with adverse drug events in cancer patients: a systematic review and meta-analysis. Ther Adv Med Oncol. 2020;12:1758835920936932. doi:10.1177/1758835920936932
   Web of Science ®Google Scholar
• Donisi C, Puzzoni M, Ziranu P, et al. Immune checkpoint inhibitors in the treatment of HCC. Front Oncol. 2021;10:601240. doi:10.3389/fonc.2020.601240
   Web of Science ®Google Scholar
• Llovet JM, Castet F, Heikenwalder M, et al. Immunotherapies for hepatocellular carcinoma. Nat Rev Clin Oncol. 2022;19(3):151–172. doi:10.1038/s41571-021-00573-2
   PubMed Web of Science ®Google Scholar
• Rizzo A, Ricci AD, Gadaleta-Caldarola G, et al. First-line immune checkpoint inhibitor-based combinations in unresectable hepatocellular carcinoma: current management and future challenges. Expert Rev Gastroenterol Hepatol. 2021;15(11):1245–1251. doi:10.1080/17474124.2021.1973431
   PubMed Web of Science ®Google Scholar
• Rizzo A, Ricci AD, Di Federico A, et al. Predictive biomarkers for checkpoint inhibitor-based immunotherapy in hepatocellular carcinoma: where do we stand? Front Oncol. 2021;11:803133. doi:10.3389/fonc.2021.803133
   PubMed Web of Science ®Google Scholar
• Visschers RG, Luyer MD, Schaap FG, et al. The gut-liver axis. Curr Opin Clin Nutr Metab Care. 2013;16(5):576–581. doi:10.1097/MCO.0b013e32836410a4
   Web of Science ®Google Scholar
• Albillos A, de Gottardi A, Rescigno M. The gut-liver axis in liver disease: pathophysiological basis for therapy. J Hepatol. 2020;72(3):558–577. doi:10.1016/j.jhep.2019.10.003
   PubMed Web of Science ®Google Scholar
• Benson AK. The gut microbiome-an emerging complex trait. Nat Genet. 2016;48(11):1301–1302. doi:10.1038/ng.3707
   Web of Science ®Google Scholar
• Li J, Sung CYJ, Lee N, et al. Probiotics modulated gut microbiota suppresses hepatocellular carcinoma growth in mice. Proc Natl Acad Sci U S A. 2016;113(9):E1306–E1315. doi:10.1073/pnas.1518189113
   PubMed Web of Science ®Google Scholar
• Schwabe RF, Greten TF. Gut microbiome in HCC - mechanisms, diagnosis and therapy. J Hepatol. 2020;72(2):230–238. doi:10.1016/j.jhep.2019.08.016
   PubMed Web of Science ®Google Scholar
• Milosevic I, Vujovic A, Barac A, et al. Gut-liver axis, gut microbiota, and its modulation in the management of liver diseases: a review of the literature. Int J Mol Sci. 2019;20(2):395. doi:10.3390/ijms20020395
   PubMed Web of Science ®Google Scholar
• Hallen-Adams HE, Suhr MJ. Fungi in the healthy human gastrointestinal tract. Virulence. 2017;8(3):352–358. doi:10.1080/21505594.2016.1247140
   PubMed Web of Science ®Google Scholar
• Nash AK, Auchtung TA, Wong MC, et al. The gut mycobiome of the human microbiome project healthy cohort. Microbiome. 2017;5(1):153. doi:10.1186/s40168-017-0373-4
   PubMedGoogle Scholar
• Huffnagle GB, Noverr MC. The emerging world of the fungal microbiome. Trends Microbiol. 2013;21(7):334–341. doi:10.1016/j.tim.2013.04.002
   PubMed Web of Science ®Google Scholar
• Demir M, Lang S, Hartmann P, et al. The fecal mycobiome in non-alcoholic fatty liver disease. J Hepatol. 2022;76(4):788–799. doi:10.1016/j.jhep.2021.11.029
   PubMed Web of Science ®Google Scholar
• Brubaker SW, Bonham KS, Zanoni I, et al. Innate immune pattern recognition: a cell biological perspective. Annu Rev Immunol. 2015;33(1):257–290. doi:10.1146/annurev-immunol-032414-112240
   PubMedGoogle Scholar
• Casadevall A. Immunity to invasive fungal diseases. Annu Rev Immunol. 2022;40(1):121–141. doi:10.1146/annurev-immunol-101220-034306
   Google Scholar
• Wang T, Pan D, Zhou Z, et al. Dectin-3 deficiency promotes colitis development due to impaired antifungal innate immune responses in the gut. PLoS Pathog. 2016;12(6):e1005662. doi:10.1371/journal.ppat.1005662
   PubMed Web of Science ®Google Scholar
• Daley D, Mani VR, Mohan N, et al. Dectin 1 activation on macrophages by galectin 9 promotes pancreatic carcinoma and peritumoral immune tolerance. Nat Med. 2017;23(5):556–567. doi:10.1038/nm.4314
   PubMed Web of Science ®Google Scholar
• Zhao Y, Chu X, Chen J, et al. Dectin-1-activated dendritic cells trigger potent antitumour immunity through the induction of Th9 cells. Nat Commun. 2016;7(1):12368. doi:10.1038/ncomms12368
   Google Scholar
• Narunsky-Haziza L, Sepich-Poore GD, Livyatan I, et al. Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions. Cell. 2022;185(20):3789–3806 e17. doi:10.1016/j.cell.2022.09.005
   PubMed Web of Science ®Google Scholar
• Liu Z, Li Y, Li C, et al. Intestinal candida albicans promotes hepatocarcinogenesis by up-regulating NLRP6. Front Microbiol. 2022;13:812771. doi:10.3389/fmicb.2022.812771
   PubMed Web of Science ®Google Scholar
• Dohlman AB, Klug J, Mesko M, et al. A pan-cancer mycobiome analysis reveals fungal involvement in gastrointestinal and lung tumors. Cell. 2022;185(20):3807–3822 e12. doi:10.1016/j.cell.2022.09.015
   PubMed Web of Science ®Google Scholar
• Alam A, Levanduski E, Denz P, et al. Fungal mycobiome drives IL-33 secretion and type 2 immunity in pancreatic cancer. Cancer Cell. 2022;40(2):153–167 e11. doi:10.1016/j.ccell.2022.01.003
   PubMed Web of Science ®Google Scholar
• Shiao SL, Kershaw KM, Limon JJ, et al. Commensal bacteria and fungi differentially regulate tumor responses to radiation therapy. Cancer Cell. 2021;39(9):1202–1213 e6. doi:10.1016/j.ccell.2021.07.002
   PubMed Web of Science ®Google Scholar
• Wang T, Fan C, Yao A, et al. The adaptor protein CARD9 protects against colon cancer by restricting mycobiota-mediated expansion of myeloid-derived suppressor cells. Immunity. 2018;49(3):504–514 e4. doi:10.1016/j.immuni.2018.08.018
   PubMed Web of Science ®Google Scholar
• Tang J, Lin G, Langdon WY, et al. Regulation of C-type lectin receptor-mediated antifungal immunity. Front Immunol. 2018;9:123. doi:10.3389/fimmu.2018.00123
   PubMed Web of Science ®Google Scholar
• Zielinski CE, Mele F, Aschenbrenner D, et al. Pathogen-induced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature. 2012;484(7395):514–518. doi:10.1038/nature10957
   PubMed Web of Science ®Google Scholar
• Hashimoto H, Vertino PM, Cheng X. Molecular coupling of DNA methylation and histone methylation. Epigenomics. 2010;2(5):657–669. doi:10.2217/epi.10.44
   PubMed Web of Science ®Google Scholar
• Netea MG, Joosten LAB, van der Meer JWM, et al. Immune defence against Candida fungal infections. Nat Rev Immunol. 2015;15(10):630–642. doi:10.1038/nri3897
   PubMed Web of Science ®Google Scholar
• Li R, Zhu S. NLRP6 inflammasome. Mol Aspects Med. 2020;76:100859. doi:10.1016/j.mam.2020.100859
   PubMed Web of Science ®Google Scholar
• Gu C, Chen J, Dang X, et al. Hippo pathway core genes based prognostic signature and immune infiltration patterns in lung squamous cell carcinoma. Front Oncol. 2021;11:680918. doi:10.3389/fonc.2021.680918
   Google Scholar
• Leibundgut-Landmann S, Osorio F, Brown GD, et al. Stimulation of dendritic cells via the dectin-1/Syk pathway allows priming of cytotoxic T-cell responses. Blood. 2008;112(13):4971–4980. doi:10.1182/blood-2008-05-158469
   Web of Science ®Google Scholar
• Carter RW, Thompson C, Reid DM, et al. Induction of CD8+ T cell responses through targeting of antigen to Dectin-2. Cell Immunol. 2006;239(2):87–91. doi:10.1016/j.cellimm.2006.05.001
   Web of Science ®Google Scholar
• Preite NW, Feriotti C, Souza de lima D, et al. The syk-coupled C-type lectin receptors Dectin-2 and Dectin-3 are involved in paracoccidioides brasiliensis recognition by human plasmacytoid dendritic cells. Front Immunol. 2018;9:464. doi:10.3389/fimmu.2018.00464
   Web of Science ®Google Scholar
• Shiga M, Miyazaki J, Tanuma K, et al. The liposome of trehalose dimycolate extracted from M. bovis BCG induces antitumor immunity via the activation of dendritic cells and CD8+ T cells. Cancer Immunol Immunother. 2021;70(9):2529–2543. doi:10.1007/s00262-021-02870-2
   Web of Science ®Google Scholar
• Karnam A, Bonam SR, Rambabu N, et al. Wnt-beta-catenin signaling in human dendritic cells mediates regulatory T-cell responses to fungi via the PD-L1 pathway. mBio. 2021;12(6):e0282421. doi:10.1128/mBio.02824-21
   Web of Science ®Google Scholar
• Patel D, Gaikwad S, Challagundla N, et al. Spleen tyrosine kinase inhibition ameliorates airway inflammation through modulation of NLRP3 inflammosome and Th17/Treg axis. Int Immunopharmacol. 2018;54:375–384. doi:10.1016/j.intimp.2017.11.026
   PubMed Web of Science ®Google Scholar
• Chihara N, Madi A, Kondo T, et al. Induction and transcriptional regulation of the co-inhibitory gene module in T cells. Nature. 2018;558(7710):454–459. doi:10.1038/s41586-018-0206-z
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zheng J. Functions of immune checkpoint molecules beyond immune evasion. Adv Exp Med Biol. 2020;1248:201–226.
   PubMed Web of Science ®Google Scholar
• Dyck L, Mills KHG. Immune checkpoints and their inhibition in cancer and infectious diseases. Eur J Immunol. 2017;47(5):765–779. doi:10.1002/eji.201646875
   PubMed Web of Science ®Google Scholar
• Schreiber G, Walter MR. Cytokine-receptor interactions as drug targets. Curr Opin Chem Biol. 2010;14(4):511–519. doi:10.1016/j.cbpa.2010.06.165
   Web of Science ®Google Scholar
• Curdy N, Lanvin O, Laurent C, et al. Regulatory mechanisms of inhibitory immune checkpoint receptors expression. Trends Cell Biol. 2019;29(10):777–790. doi:10.1016/j.tcb.2019.07.002
   PubMed Web of Science ®Google Scholar
• Terawaki S, Chikuma S, Shibayama S, et al. IFN-alpha directly promotes programmed cell death-1 transcription and limits the duration of T cell-mediated immunity. J Immunol. 2011;186(5):2772–2779. doi:10.4049/jimmunol.1003208
   PubMed Web of Science ®Google Scholar
• Pedro ARV, Lima T, Fróis-Martins R, et al. Dectin-1-mediated production of pro-inflammatory cytokines induced by yeast beta-glucans in bovine monocytes. Front Immunol. 2021;12:689879. doi:10.3389/fimmu.2021.689879
   Web of Science ®Google Scholar
• Gringhuis SI, den Dunnen J, Litjens M, et al. Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappaB activation through Raf-1 and Syk. Nat Immunol. 2009;10(2):203–213. doi:10.1038/ni.1692
   PubMed Web of Science ®Google Scholar
• Sweeney CM, Lonergan R, Basdeo SA, et al. IL-27 mediates the response to IFN-beta therapy in multiple sclerosis patients by inhibiting Th17 cells. Brain Behav Immun. 2011;25(6):1170–1181. doi:10.1016/j.bbi.2011.03.007
   PubMed Web of Science ®Google Scholar
• Fisher J, Card G, Liang Y, et al. Orientia tsutsugamushi selectively stimulates the C-type lectin receptor mincle and type 1-skewed proinflammatory immune responses. PLoS Pathog. 2021;17(7):e1009782. doi:10.1371/journal.ppat.1009782
   Web of Science ®Google Scholar
• Palomino DC, Marti LC. Chemokines and immunity. Einstein. 2015;13(3):469–473. doi:10.1590/S1679-45082015RB3438
   PubMed Web of Science ®Google Scholar
• Xiu W, Luo J. CXCL9 secreted by tumor-associated dendritic cells up-regulates PD-L1 expression in bladder cancer cells by activating the CXCR3 signaling. BMC Immunol. 2021;22(1):3. doi:10.1186/s12865-020-00396-3
   Web of Science ®Google Scholar
• Guo Y, Kasahara S, Jhingran A, et al. During aspergillus infection, monocyte-derived DCs, neutrophils, and plasmacytoid DCs enhance innate immune defense through CXCR3-dependent crosstalk. Cell Host Microbe. 2020;28(1):104–116 e4. doi:10.1016/j.chom.2020.05.002
   PubMed Web of Science ®Google Scholar
• Nejman D, Livyatan I, Fuks G, et al. The human tumor microbiome is composed of tumor type-specific intracellular bacteria. Science. 2020;368(6494):973–980. doi:10.1126/science.aay9189
   PubMed Web of Science ®Google Scholar
• Riquelme E, Zhang Y, Zhang L, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell. 2019;178(4):795–806 e12. doi:10.1016/j.cell.2019.07.008
   PubMed Web of Science ®Google Scholar
• Kapitan M, Niemiec MJ, Steimle A, et al. Fungi as part of the microbiota and interactions with intestinal bacteria. Curr Top Microbiol Immunol. 2019;422:265–301. doi:10.1007/82_2018_117
   PubMed Web of Science ®Google Scholar
• Chiffoleau E. C-type lectin-like receptors as emerging orchestrators of sterile inflammation represent potential therapeutic targets. Front Immunol. 2018;9:227. doi:10.3389/fimmu.2018.00227
   PubMed Web of Science ®Google Scholar
• Kalia N, Singh J, Kaur M. The role of dectin-1 in health and disease. Immunobiology. 2021;226(2):152071. doi:10.1016/j.imbio.2021.152071
   Web of Science ®Google Scholar
• Nikolakopoulou C, Willment JA, Brown GD. C-type lectin receptors in antifungal immunity. Adv Exp Med Biol. 2020;1204:1–30.
   Web of Science ®Google Scholar
• Yan H, Kamiya T, Suabjakyong P, et al. Targeting C-type lectin receptors for cancer immunity. Front Immunol. 2015;6:408. doi:10.3389/fimmu.2015.00408
   PubMed Web of Science ®Google Scholar