Polyphenol Supplementation Enhances the Efficacy of PD-1/PD-L1 Inhibitors Against Cancer: A Meta-Analysis of Animal Studies

References

• Ostios-Garcia L, Villamayor J, Garcia-Lorenzo E, Vinal D, Feliu J. Understanding the immune response and the current landscape of immunotherapy in pancreatic cancer. World J Gastroenterol. 2021;27(40):6775–93. 10.3748/wjg.v27.i40.6775
   PubMed Web of Science ®Google Scholar
• Sun C, Mezzadra R, Schumacher TN. Regulation and function of the PD-L1 CHECKPOINT. Immunity. 2018;48(3):434–52. 10.1016/j.immuni.2018.03.014
   PubMed Web of Science ®Google Scholar
• Sasaki A, Kawazoe A, Eto T, Okunaka M, Mishima S, Sawada K, Nakamura Y, Kotani D, Kuboki Y, Taniguchi H, et al. Improved efficacy of taxanes and ramucirumab combination chemotherapy after exposure to anti-PD-1 therapy in advanced gastric cancer. ESMO Open. 2020;4(Suppl 2):e000775. 10.1136/esmoopen-2020-000775
   PubMed Web of Science ®Google Scholar
• Xiang Z, Li J, Zhang Z, Cen C, Chen W, Jiang B, Meng Y, Wang Y, Berglund B, Zhai G, et al. Comprehensive evaluation of anti-PD-1, anti-PD-L1, anti-CTLA-4 and their combined immunotherapy in clinical trials: a systematic review and meta-analysis. Front Pharmacol. 2022;13:883655. 10.3389/fphar.2022.883655
   PubMed Web of Science ®Google Scholar
• Yang L, Dong XZ, Xing XX, Cui XH, Li L, Zhang L. Efficacy and safety of anti-PD-1/anti-PD-L1 antibody therapy in treatment of advanced gastric cancer or gastroesophageal junction cancer: a meta-analysis. World J Gastrointest Oncol. 2020;12(11):1346–63. 10.4251/wjgo.v12.i11.1346
   PubMed Web of Science ®Google Scholar
• Chen S, Zhang Z, Zheng X, Tao H, Zhang S, Ma J, Liu Z, Wang J, Qian Y, Cui P, et al. Response efficacy of PD-1 and PD-L1 inhibitors in clinical trials: a systematic review and meta-analysis. Front Oncol. 2021;11:562315. 10.3389/fonc.2021.562315
   PubMedGoogle Scholar
• Rana P, Shrama A, Mandal CC. Molecular insights into phytochemicals-driven break function in tumor microenvironment. J Food Biochem. 2021;45(9):e13824. 10.1111/jfbc.13824
   PubMed Web of Science ®Google Scholar
• Yahfoufi N, Alsadi N, Jambi M, Matar C. The immunomodulatory and anti-inflammatory role of polyphenols. Nutrients. 2018;10(11):1618. 10.3390/nu10111618
   PubMed Web of Science ®Google Scholar
• Shakoor H, Feehan J, Apostolopoulos V, Platat C, Al Dhaheri AS, Ali HI, Ismail LC, Bosevski M, Stojanovska L. Immunomodulatory effects of dietary polyphenols. Nutrients. 2021;13(3):728. 10.3390/nu13030728
   PubMed Web of Science ®Google Scholar
• Mo D, Zhu H, Wang J, Hao H, Guo Y, Wang J, Han X, Zou L, Li Z, Yao H, et al. Icaritin inhibits PD-L1 expression by targeting protein IκB kinase α. Eur J Immunol. 2021;51(4):978–88. 10.1002/eji.202048905
   PubMed Web of Science ®Google Scholar
• Hao H, Zhang Q, Zhu H, Wen Y, Qiu D, Xiong J, Fu X, Wu Y, Meng K, Li J. Icaritin promotes tumor T-cell infiltration and induces antitumor immunity in mice. Eur J Immunol. 2019;49(12):2235–44. 10.1002/eji.201948225
   PubMed Web of Science ®Google Scholar
• Lasso P, Gomez-Cadena A, Urueña C, Donda A, Martinez-Usatorre A, Romero P, Barreto A, Fiorentino S. An immunomodulatory gallotanin-rich fraction from Caesalpinia spinosa enhances the therapeutic effect of anti-PD-L1 in melanoma. Front Immunol. 2020;11:584959. 10.3389/fimmu.2020.584959
   PubMed Web of Science ®Google Scholar
• Deng B, Yang B, Chen J, Wang S, Zhang W, Guo Y, Han Y, Li H, Dang Y, Yuan Y, et al. Gallic acid induces T-helper-1-like Treg cells and strengthens immune checkpoint blockade efficacy. J Immunother Cancer. 2022;10(7):e004037. 10.1136/jitc-2021-004037
   PubMed Web of Science ®Google Scholar
• Tang H, Liu Y, Wang C, Zheng H, Chen Y, Liu W, Chen X, Zhang J, Chen H, Yang Y, et al. Inhibition of COX-2 and EGFR by melafolone improves anti-PD-1 therapy through vascular normalization and PD-L1 Downregulation In Lung Cancer. J Pharmacol Exp Ther. 2019;368(3):401–13. 10.1124/jpet.118.254359
   PubMed Web of Science ®Google Scholar
• Sun D, Zou Y, Song L, Han S, Yang H, Chu D, Dai Y, Ma J, O'Driscoll CM, Yu Z, et al. A cyclodextrin-based nanoformulation achieves co-delivery of ginsenoside Rg3 and quercetin for chemo-immunotherapy in colorectal cancer. Acta Pharm Sin B. 2022;12(1):378–93. 10.1016/j.apsb.2021.06.005
   PubMed Web of Science ®Google Scholar
• Jia L, Gao Y, Zhou T, Zhao XL, Hu HY, Chen DW, Qiao MX. Enhanced response to PD-L1 silencing by modulation of TME via balancing glucose metabolism and robust co-delivery of siRNA/Resveratrol with dual-responsive polyplexes. Biomaterials. 2021;271:120711. 10.1016/j.biomaterials.2021.120711
   PubMed Web of Science ®Google Scholar
• Shao Y, Zhu W, Da J, Xu M, Wang Y, Zhou J, Wang Z. Bisdemethoxycurcumin in combination with α-PD-L1 antibody boosts immune response against bladder cancer. Onco Targets Ther. 2017;10:2675–83. 10.2147/OTT.S130653
   PubMed Web of Science ®Google Scholar
• Jiang ZB, Wang WJ, Xu C, Xie YJ, Wang XR, Zhang YZ, Huang JM, Huang M, Xie C, Liu P, et al. Luteolin and its derivative apigenin suppress the inducible PD-L1 expression to improve anti-tumor immunity in KRAS-mutant lung cancer. Cancer Lett. 2021;515:36–48. 10.1016/j.canlet.2021.05.019
   PubMed Web of Science ®Google Scholar
• Hooijmans CR, Rovers MM, de Vries RB, Leenaars M, Ritskes-Hoitinga M, Langendam MW. SYRCLE's risk of bias tool for animal studies. BMC Med Res Methodol. 2014;14(1):43. 10.1186/1471-2288-14-43
   PubMed Web of Science ®Google Scholar
• Wang L, Jiang G, Jing N, Liu X, Li Q, Liang W, Liu Z. Bilberry anthocyanin extracts enhance anti-PD-L1 efficiency by modulating gut microbiota. Food Funct. 2020;11(4):3180–90. 10.1039/d0fo00255k
   PubMed Web of Science ®Google Scholar
• Liu X, Wang L, Jing N, Jiang G, Liu Z. Biostimulating gut microbiome with bilberry anthocyanin combo to enhance anti-PD-L1 efficiency against murine colon cancer. Microorganisms. 2020;8(2):175. 10.3390/microorganisms8020175
   PubMed Web of Science ®Google Scholar
• Yang X, Lam W, Jiang Z, Guan F, Han X, Hu R, Cai W, Cheng W, Liu SH, Cheng P, et al. YIV-906 potentiated anti-PD1 action against hepatocellular carcinoma by enhancing adaptive and innate immunity in the tumor microenvironment. Sci Rep. 2021;11(1):13482. 10.1038/s41598-021-91623-3
   PubMed Web of Science ®Google Scholar
• Dent P, Booth L, Roberts JL, Poklepovic A, Hancock JF. (Curcumin + sildenafil) enhances the efficacy of 5FU and anti-PD1 therapies in vivo. J Cell Physiol. 2020;235(10):6862–74. 10.1002/jcp.29580
   PubMed Web of Science ®Google Scholar
• Hayakawa T, Yaguchi T, Kawakami Y. Enhanced anti-tumor effects of the PD-1 blockade combined with a highly absorptive form of curcumin targeting STAT3. Cancer Sci. 2020;111(12):4326–35. 10.1111/cas.14675
   PubMed Web of Science ®Google Scholar
• Guo L, Li H, Fan T, Ma Y, Wang L. Synergistic efficacy of curcumin and anti-programmed cell death-1 in hepatocellular carcinoma. Life Sci. 2021;279:119359. 10.1016/j.lfs.2021.119359
   PubMed Web of Science ®Google Scholar
• Gong F, Ma JC, Jia J, Li FZ, Wu JL, Wang S, Teng X, Cui ZK. Synergistic effect of the anti-PD-1 antibody with blood stable and reduction sensitive curcumin micelles on colon cancer. Drug Deliv. 2021;28(1):930–42. 10.1080/10717544.2021.1921077
   PubMed Web of Science ®Google Scholar
• Zhou Y, Zheng J, Li Y, Xu DP, Li S, Chen YM, Li HB. Natural polyphenols for prevention and treatment of cancer. Nutrients. 2016;8(8):515. 10.3390/nu8080515
   PubMed Web of Science ®Google Scholar
• Khodavandi A, Alizadeh F, Razis AFA. Association between dietary intake and risk of ovarian cancer: a systematic review and meta-analysis. Eur J Nutr. 2021;60(4):1707–36. 10.1007/s00394-020-02332-y
   PubMed Web of Science ®Google Scholar
• Chang H, Lei L, Zhou Y, Ye F, Zhao G. Dietary flavonoids and the risk of colorectal cancer: an updated meta-analysis of epidemiological studies. Nutrients. 2018;10(7):950. 10.3390/nu10070950
   PubMed Web of Science ®Google Scholar
• Russo GI, Campisi D, Di Mauro M, Regis F, Reale G, Marranzano M, Ragusa R, Solinas T, Madonia M, Cimino S, et al. Dietary consumption of phenolic acids and prostate cancer: A case-control study in Sicily, Southern Italy. Molecules. 2017;22(12):2159. 10.3390/molecules22122159
   PubMed Web of Science ®Google Scholar
• Bahrami A, Makiabadi E, Jalali S, Heidari Z, Assadi M, Rashidkhani B. Dietary intake of polyphenols and the risk of breast cancer: a case-control study. Clin Nutr Res. 2021;10(4):330–40. 10.7762/cnr.2021.10.4.330
   PubMedGoogle Scholar
• He Z, Wu S, Lin J, Booth A, Rankin GO, Martinez I, Chen YC. Polyphenols extracted from Chinese hickory (Carya cathayensis) promote apoptosis and inhibit proliferation through the p53-dependent intrinsic and HIF-1α-VEGF pathways in ovarian cancer cells. Appl Sci. 2020;10(23):8615. 10.3390/app10238615
   Google Scholar
• Huang Y, Zhu X, Zhu Y, Wang Z. Pinus koraiensis polyphenols: structural identification, in vitro antioxidant activity, immune function and inhibition of cancer cell proliferation. Food Funct. 2021;12(9):4176–98. 10.1039/D0FO03347B
   PubMedGoogle Scholar
• Kato K, Nagane M, Aihara N, Kamiie J, Miyanabe M, Hiraki S, Luo X, Nakanishi I, Shoji Y, Matsumoto KI, et al. Lipid-soluble polyphenols from sweet potato exert antitumor activity and enhance chemosensitivity in breast cancer. J Clin Biochem Nutr. 2021;68(3):193–200. 10.3164/jcbn.20-73
   PubMed Web of Science ®Google Scholar
• Herrero de la Parte B, Rodeño-Casado M, Iturrizaga Correcher S, Mar Medina C, García-Alonso I. Curcumin reduces colorectal cancer cell proliferation and migration and slows in vivo growth of liver metastases in rats. Biomedicines. 2021;9(9):1183. 10.3390/biomedicines9091183
   PubMed Web of Science ®Google Scholar
• Yang MD, Sun Y, Zhou WJ, Xie XZ, Zhou QM, Lu YY, Su SB. Resveratrol enhances inhibition effects of cisplatin on cell migration and invasion and tumor growth in breast cancer MDA-MB-231 cell models in vivo and in vitro. Molecules. 2021;26(8):2204. 10.3390/molecules26082204
   PubMed Web of Science ®Google Scholar
• Huang KY, Wang TH, Chen CC, Leu YL, Li HJ, Jhong CL, Chen CY. Growth suppression in lung cancer cells harboring EGFR-C797S mutation by quercetin. Biomolecules. 2021;11(9):1271. 10.3390/biom11091271
   PubMed Web of Science ®Google Scholar
• Mirza-Aghazadeh-Attari M, Ekrami EM, Aghdas SAM, Mihanfar A, Hallaj S, Yousefi B, Safa A, Majidinia M. Targeting PI3K/Akt/mTOR signaling pathway by polyphenols: implication for cancer therapy. Life Sci. 2020;255:117481. 10.1016/j.lfs.2020.117481
   PubMed Web of Science ®Google Scholar
• Villota H, Röthlisberger S, Pedroza-Díaz J. Modulation of the canonical Wnt signaling pathway by dietary polyphenols, an opportunity for colorectal cancer chemoprevention and treatment. Nutr Cancer. 2022;74(2):384–404. 10.1080/01635581.2021.1884730
   PubMed Web of Science ®Google Scholar
• Hu Z, Li M, Cao Y, Akan OD, Guo T, Luo F. Targeting AMPK signaling by dietary polyphenols in cancer prevention. Mol Nutr Food Res. 2022;66(2):e2100732.
   PubMed Web of Science ®Google Scholar
• Wang P, Hao X, Li X, Yan Y, Tian W, Xiao L, Wang Z, Dong J. Curcumin inhibits adverse psychological stress-induced proliferation and invasion of glioma cells via down-regulating the ERK/MAPK pathway. J Cell Mol Med. 2021;25(15):7190–203. 10.1111/jcmm.16749
   PubMed Web of Science ®Google Scholar
• Aziz MA, Sarwar MS, Akter T, Uddin MS, Xun S, Zhu Y, Islam MS, Hongjie Z. Polyphenolic molecules targeting STAT3 pathway for the treatment of cancer. Life Sci. 2021;268:118999. 10.1016/j.lfs.2020.118999
   PubMed Web of Science ®Google Scholar
• Hazafa A, Iqbal MO, Javaid U, Tareen MBK, Amna D, Ramzan A, Piracha S, Naeem M. Inhibitory effect of polyphenols (phenolic acids, lignans, and stilbenes) on cancer by regulating signal transduction pathways: a review. Clin Transl Oncol. 2022;24(3):432–45. 10.1007/s12094-021-02709-3
   PubMed Web of Science ®Google Scholar
• Wang JY, Jiang MW, Li MY, Zhang ZH, Xing Y, Ri M, Jin CH, Xu GH, Piao LX, Jin HL, et al. Formononetin represses cervical tumorigenesis by interfering with the activation of PD-L1 through MYC and STAT3 downregulation. J Nutr Biochem. 2022;100:108899. 10.1016/j.jnutbio.2021.108899
   PubMed Web of Science ®Google Scholar
• Rong W, Wan N, Zheng X, Shi G, Jiang C, Pan K, Gao M, Yin Z, Gao ZJ, Zhang J. Chrysin inhibits hepatocellular carcinoma progression through suppressing programmed death ligand 1 expression. Phytomedicine. 2022;95:153867. 10.1016/j.phymed.2021.153867
   PubMed Web of Science ®Google Scholar
• Liu X, Xing Y, Li M, Zhang Z, Wang J, Ri M, Jin C, Xu G, Piao L, Jin H, et al. Licochalcone A inhibits proliferation and promotes apoptosis of colon cancer cell by targeting programmed cell death-ligand 1 via the NF-κB and Ras/Raf/MEK pathways. J Ethnopharmacol. 2021;273:113989. 10.1016/j.jep.2021.113989
   PubMed Web of Science ®Google Scholar
• Kuo IY, Yang YE, Yang PS, Tsai YJ, Tzeng HT, Cheng HC, Kuo WT, Su WC, Chang CP, Wang YC. Converged Rab37/IL-6 trafficking and STAT3/PD-1 transcription axes elicit an immunosuppressive lung tumor microenvironment. Theranostics. 2021;11(14):7029–44. 10.7150/thno.60040
   PubMed Web of Science ®Google Scholar
• Li W, Kim TI, Kim JH, Chung HS. Immune checkpoint PD-1/PD-L1 CTLA-4/CD80 are blocked by Rhus verniciflua Stokes and its active compounds. Molecules. 2019;24(22):4062. 10.3390/molecules24224062
   PubMed Web of Science ®Google Scholar
• Jing L, Lin J, Yang Y, Tao L, Li Y, Liu Z, Zhao Q, Diao A. Quercetin inhibiting the PD-1/PD-L1 interaction for immune-enhancing cancer chemopreventive agent. Phytother Res. 2021;35(11):6441–51. 10.1002/ptr.7297
   PubMed Web of Science ®Google Scholar
• Gibson JT, Orlandella RM, Turbitt WJ, Behring M, Manne U, Sorge RE, Norian LA. Obesity-associated myeloid-derived suppressor cells promote apoptosis of tumor-infiltrating CD8 T cells and immunotherapy resistance in breast cancer. Front Immunol. 2020;11:590794. 10.3389/fimmu.2020.590794
   PubMed Web of Science ®Google Scholar
• Mao FY, Zhao YL, Lv YP, Teng YS, Kong H, Liu YG, Wu XL, Hao CJ, Chen W, Duan MB, et al. CD45+CD33lowCD11bdim myeloid-derived suppressor cells suppress CD8+ T cell activity via the IL-6/IL-8-arginase I axis in human gastric cancer. Cell Death Dis. 2018;9(7):763. 10.1038/s41419-018-0803-7
   PubMedGoogle Scholar
• Ribeiro EB, de Marchi PGF, Honorio-França AC, França EL, Soler MAG. Interferon-gamma carrying nanoemulsion with immunomodulatory and anti-tumor activities. J Biomed Mater Res A. 2020;108(2):234–45. 10.1002/jbm.a.36808
   PubMed Web of Science ®Google Scholar
• Ding G, Shen T, Yan C, Zhang M, Wu Z, Cao L. IFN-γ down-regulates the PD-1 expression and assist nivolumab in PD-1-blockade effect on CD8+ T-lymphocytes in pancreatic cancer. BMC Cancer. 2019;19(1):1053. 10.1186/s12885-019-6145-8
   PubMed Web of Science ®Google Scholar