Complexity of Tumor Microenvironment: Therapeutic Role of Curcumin and Its Metabolites

References

• Dagenais GR, Leong DP, Rangarajan S, Lanas F, Lopez-Jaramillo P, Gupta R, Diaz R, Avezum A, Oliveira GBF, Wielgosz A, et al. Variations in common diseases, hospital admissions, and deaths in middle-aged adults in 21 countries from five continents (PURE): a prospective cohort study. Lancet. 2020;395(10226):785–94. doi:10.1016/S0140-6736(19)32007-0
   PubMed Web of Science ®Google Scholar
• Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA 2021;71(3):209–49.
   Google Scholar
• Prasad S, Srivastava SK. Oxidative stress and cancer: chemopreventive and therapeutic role of triphala. Antioxidants. 2020;9(1):72. doi:10.3390/antiox9010072
   Web of Science ®Google Scholar
• Butler M, Prasad S, Srivastava SK. Targeting glioblastoma tumor microenvironment. Adv Exp Med Biol. 2020;1296:1–9.doi:10.1007/978-3-030-59038-3_1
   Google Scholar
• Jahanban-Esfahlan R, Seidi K, Monhemi H, Adli ADF, Minofar B, Zare P, Farajzadeh D, Farajnia S, Behzadi R, Abbasi MM, et al. RGD delivery of truncated coagulase to tumor vasculature affords local thrombotic activity to induce infarction of tumors in mice. Sci Rep. 2017;7(1):1–14. doi:10.1038/s41598-017-05326-9
   PubMed Web of Science ®Google Scholar
• Roma-Rodrigues C, Mendes R, Baptista PV, Fernandes AR. Targeting tumor microenvironment for cancer therapy. Int J Mol Sci. 2019;20(4):840. doi:10.3390/ijms20040840
   PubMed Web of Science ®Google Scholar
• Prasad S, DuBourdieu D, Srivastava A, Kumar P, Lall R. Metal–curcumin complexes in therapeutics: an approach to enhance pharmacological effects of curcumin. Int J Mol Sci. 2021;22(13):7094. doi:10.3390/ijms22137094
   PubMed Web of Science ®Google Scholar
• Prasad S, Aggarwal BB. Turmeric, the golden spice: from traditional medicine to modern medicine. In: Benzie IFF, Wachtel-Galor S, editors. Herbal medicine: biomolecular and clinical aspects. Chapter 13. 2nd ed. Boca Raton, FL: CRC Press/Taylor & Francis; 2021.
   Google Scholar
• Priyadarsini KI. The chemistry of curcumin: from extraction to therapeutic agent. Molecules. 2014;19(12):20091–112. doi:10.3390/molecules191220091
   PubMed Web of Science ®Google Scholar
• Gupta N, Verma K, Nalla S, Kulshreshtha A, Lall R, Prasad S. Free radicals as a double-edged sword: the cancer preventive and therapeutic roles of curcumin. Molecules. 2020;25(22):5390. doi:10.3390/molecules25225390
   PubMed Web of Science ®Google Scholar
• Saha P, Bose S, Srivastava AK, Chaudhary AA, Lall R, Prasad S. Jeopardy of COVID-19: rechecking the perks of phytotherapeutic interventions. Molecules. 2021;26(22):6783. doi:10.3390/molecules26226783
   PubMed Web of Science ®Google Scholar
• Kunnumakkara AB, Bordoloi D, Padmavathi G, Monisha J, Roy NK, Prasad S, Aggarwal BB. Curcumin, the golden nutraceutical: multitargeting for multiple chronic diseases. Br J Pharmacol. 2017;174(11):1325–48. doi:10.1111/bph.13621
   PubMed Web of Science ®Google Scholar
• Prasad S, Tyagi AK, Aggarwal BB. Recent developments in delivery, bioavailability, absorption and metabolism of curcumin: the golden pigment from golden spice. Cancer Res Treat. 2014;46(1):2–18. doi:10.4143/crt.2014.46.1.2
   PubMed Web of Science ®Google Scholar
• Aggarwal BB, Deb L, Prasad S. Curcumin differs from tetrahydrocurcumin for molecular targets, signaling pathways and cellular responses. Molecules. 2014;20(1):185–205. doi:10.3390/molecules20010185
   PubMed Web of Science ®Google Scholar
• Jabczyk M, Nowak J, Hudzik B, Zubelewicz-Szkodzińska B. Curcumin and its potential impact on microbiota. Nutrients. 2021;13(6):2004. doi:10.3390/nu13062004
   PubMed Web of Science ®Google Scholar
• Ireson CR, Jones DJ, Orr S, Coughtrie MW, Boocock DJ, Williams ML, Farmer PB, Steward WP, Gescher AJ. Metabolism of the cancer chemopreventive agent curcumin in human and rat intestine. Cancer Epidemiol Prev Biomarkers. 2002;11(1):105–11.
   PubMed Web of Science ®Google Scholar
• Wu Q, Li B, Li Z, Li J, Sun S, Sun S. Cancer-associated adipocytes: key players in breast cancer progression. J Hematol Oncol. 2019;12(1):1–15. doi:10.1186/s13045-019-0778-6
   PubMed Web of Science ®Google Scholar
• Pallegar NK, Christian SL. Adipocytes in the tumour microenvironment. Adv Exp Med Biol. 2020;1234:1–13.
   PubMed Web of Science ®Google Scholar
• Moraes JA, Encarnação C, Franco VA, Xavier Botelho LG, Rodrigues GP, Ramos-Andrade I, Barja-Fidalgo C, Renovato-Martins M. Adipose tissue-derived extracellular vesicles and the tumor microenvironment: revisiting the hallmarks of cancer. Cancers. 2021;13(13):3328. doi:10.3390/cancers13133328
   PubMed Web of Science ®Google Scholar
• Zewdu A, Casadei L, Pollock RE, Braggio D. Adipose tumor microenvironment. Adv Exp Med Biol. 2020;1226:73-86. doi: 10.1007/978-3-030-36214-0_6.
   Google Scholar
• Corrêa LH, Corrêa R, Farinasso CM, de Sant’Ana Dourado LP, Magalhães KG. Adipocytes and macrophages interplay in the orchestration of tumor microenvironment: new implications in cancer progression. Front Immunol. 2017;8:1129. doi:10.3389/fimmu.2017.01129
   PubMed Web of Science ®Google Scholar
• Wang S, Moustaid-Moussa N, Chen L, Mo H, Shastri A, Su R, Bapat P, Kwun I, Shen C-L. Novel insights of dietary polyphenols and obesity. J Nutr Biochem. 2014;25(1):1–18. doi:10.1016/j.jnutbio.2013.09.001
   PubMed Web of Science ®Google Scholar
• Bradford PG. Curcumin and obesity. Biofactors. 2013;39(1):78–87. doi:10.1002/biof.1074
   PubMed Web of Science ®Google Scholar
• Sakuma S, Sumida M, Endoh Y, Kurita A, Yamaguchi A, Watanabe T, Kohda T, Tsukiyama Y, Fujimoto Y. Curcumin inhibits adipogenesis induced by benzyl butyl phthalate in 3T3-L1 cells. Toxicol Appl Pharmacol. 2017;329:158–64. doi:10.1016/j.taap.2017.05.036
   PubMed Web of Science ®Google Scholar
• Xie X-y, Kong P-R, Wu J-f, Li Y, Li Y-x. Curcumin attenuates lipolysis stimulated by tumor necrosis factor-α or isoproterenol in 3T3-L1 adipocytes. Phytomedicine. 2012;20(1):3–8. doi:10.1016/j.phymed.2012.09.003
   PubMed Web of Science ®Google Scholar
• Shao-Ling W, Ying L, Ying W, Yan-Feng C, Li-Xin N, Song-Tao L, Chang-Hao S. Curcumin, a potential inhibitor of up-regulation of TNF-alpha and IL-6 induced by palmitate in 3T3-L1 adipocytes through NF-kappaB and JNK pathway. Biomed Environ Sci. 2009;22(1):32–9. doi:10.1016/S0895-3988(09)60019-2
   PubMed Web of Science ®Google Scholar
• Kim J-H, Park S-H, Nam S-W, Kwon H-J, Kim B-W, Kim W-J, Choi YH. Curcumin stimulates proliferation, stemness acting signals and migration of 3T3-L1 preadipocytes. Int J Mol Med. 2011;28(3):429–35.
   PubMed Web of Science ®Google Scholar
• Lee YK, Lee WS, Hwang JT, Kwon DY, Surh YJ, Park OJ. Curcumin exerts antidifferentiation effect through AMPKα-PPAR-γ in 3T3-L1 adipocytes and antiproliferatory effect through AMPKα-COX-2 in cancer cells. J Agric Food Chem. 2009;57(1):305–10. doi:10.1021/jf802737z
   PubMed Web of Science ®Google Scholar
• Alkasalias T, Moyano-Galceran L, Arsenian-Henriksson M, Lehti K. Fibroblasts in the tumor microenvironment: shield or spear? Int J Mol Sci. 2018;19(5):1532. doi:10.3390/ijms19051532
   PubMed Web of Science ®Google Scholar
• Wu F, Yang J, Liu J, Wang Y, Mu J, Zeng Q, Deng S, Zhou H. Signaling pathways in cancer-associated fibroblasts and targeted therapy for cancer. Sig Transduct Target Ther. 2021;6(1):1–35. doi:10.1038/s41392-021-00641-0
   PubMed Web of Science ®Google Scholar
• Mao X, Xu J, Wang W, Liang C, Hua J, Liu J, Zhang B, Meng Q, Yu X, Shi S. Crosstalk between cancer-associated fibroblasts and immune cells in the tumor microenvironment: new findings and future perspectives. Mol Cancer. 2021;20(1):1–30. doi:10.1186/s12943-021-01428-1
   PubMed Web of Science ®Google Scholar
• Winkler J, Abisoye-Ogunniyan A, Metcalf KJ, Werb Z. Concepts of extracellular matrix remodelling in tumour progression and metastasis. Nat Commun. 2020;11(1):1–19. doi:10.1038/s41467-020-18794-x
   PubMed Web of Science ®Google Scholar
• Taguchi A, Kawana K, Tomio K, Yamashita A, Isobe Y, Nagasaka K, Koga K, Inoue T, Nishida H, Kojima S, et al. Matrix metalloproteinase (MMP)-9 in cancer-associated fibroblasts (CAFs) is suppressed by omega-3 polyunsaturated fatty acids in vitro and in vivo. PLoS One. 2014;9(2):e89605. doi:10.1371/journal.pone.0089605
   PubMed Web of Science ®Google Scholar
• Monteran L, Erez N. The dark side of fibroblasts: cancer-associated fibroblasts as mediators of immunosuppression in the tumor microenvironment. Front Immunol. 2019;10) :1835. doi:10.3389/fimmu.2019.01835
   PubMed Web of Science ®Google Scholar
• Buhrmann C, Kraehe P, Lueders C, Shayan P, Goel A, Shakibaei M. Curcumin suppresses crosstalk between colon cancer stem cells and stromal fibroblasts in the tumor microenvironment: potential role of EMT. PLoS One. 2014;9(9):e107514. doi:10.1371/journal.pone.0107514
   PubMed Web of Science ®Google Scholar
• Yang J-y, Zhong X, Kim S-J, Kim D-H, Kim HS, Lee J-S, Yum H-W, Lee J, Na H-K, Surh Y-J. Comparative effects of curcumin and tetrahydrocurcumin on dextran sulfate sodium-induced colitis and inflammatory signaling in mice. J Cancer Prev. 2018;23(1):18–24. doi:10.15430/JCP.2018.23.1.18
   PubMed Web of Science ®Google Scholar
• Ba P, Xu M, Yu M, Li L, Duan X, Lv S, Fu G, Yang J, Yang P, Yang C, et al. Curcumin suppresses the proliferation and tumorigenicity of Cal27 by modulating cancer‐associated fibroblasts of TSCC. Oral Dis. 2020;26(7):1375–83. doi:10.1111/odi.13306
   PubMed Web of Science ®Google Scholar
• Dudás J, Fullár A, Romani A, Pritz C, Kovalszky I, Schartinger VH, Sprinzl GM, Riechelmann H. Curcumin targets fibroblast–tumor cell interactions in oral squamous cell carcinoma. Exp Cell Res. 2013;319(6):800–9. doi:10.1016/j.yexcr.2012.12.001
   PubMed Web of Science ®Google Scholar
• Du Y, Long Q, Zhang L, Shi Y, Liu X, Li X, Guan B, Tian Y, Wang X, Li L, et al. Curcumin inhibits cancer-associated fibroblast-driven prostate cancer invasion through MAOA/mTOR/HIF-1α signaling. Int J Oncol. 2015;47(6):2064–72. doi:10.3892/ijo.2015.3202
   PubMed Web of Science ®Google Scholar
• Zhang Y, Liu Y, Zou J, Yan L, Du W, Zhang Y, Sun H, Lu P, Geng S, Gu R, et al. Tetrahydrocurcumin induces mesenchymal-epithelial transition and suppresses angiogenesis by targeting HIF-1α and autophagy in human osteosarcoma. Oncotarget. 2017;8(53):91134–49. doi:10.18632/oncotarget.19845
   PubMedGoogle Scholar
• Hendrayani S-F, Al-Khalaf HH, Aboussekhra A. Curcumin triggers p16-dependent senescence in active breast cancer-associated fibroblasts and suppresses their paracrine procarcinogenic effects. Neoplasia. 2013;15(6):631–IN11. doi:10.1593/neo.13478
   PubMed Web of Science ®Google Scholar
• Yodkeeree S, Garbisa S, Limtrakul P. Tetrahydrocurcumin inhibits HT1080 cell migration and invasion via downregulation of MMPs and uPA 1. Acta Pharmacol Sin. 2008;29(7):853–60. doi:10.1111/j.1745-7254.2008.00792.x
   PubMed Web of Science ®Google Scholar
• Dhatchinamoorthy K, Colbert JD, Rock KL. Cancer immune evasion through loss of MHC class I antigen presentation. Front Immunol. 2021;12:636568. doi:10.3389/fimmu.2021.636568
   PubMed Web of Science ®Google Scholar
• Abel AM, Yang C, Thakar MS, Malarkannan S. Natural killer cells: development, maturation, and clinical utilization. Front Immunol. 2018;9:1869.
   PubMed Web of Science ®Google Scholar
• Xiao H, Guo Y, Li B, Li X, Wang Y, Han S, Cheng D, Shuai X. M2-like tumor-associated macrophage-targeted codelivery of STAT6 inhibitor and IKKβ siRNA induces M2-to-M1 repolarization for cancer immunotherapy with low immune side effects. ACS Cent Sci. 2020;6(7):1208–22. doi:10.1021/acscentsci.9b01235
   PubMed Web of Science ®Google Scholar
• Chanmee T, Ontong P, Konno K, Itano N. Tumor-associated macrophages as major players in the tumor microenvironment. Cancers (Basel). 2014;6(3):1670–90. doi:10.3390/cancers6031670
   PubMed Web of Science ®Google Scholar
• Sionov RV, Fridlender ZG, Granot Z. The multifaceted roles neutrophils play in the tumor microenvironment. Cancer Microenviron. 2015;8(3):125–58. doi:10.1007/s12307-014-0147-5
   PubMed Web of Science ®Google Scholar
• Li C, Jiang P, Wei S, Xu X, Wang J. Regulatory T cells in tumor microenvironment: new mechanisms, potential therapeutic strategies and future prospects. Mol Cancer. 2020;19(1)(1):23. doi:10.1186/s12943-020-01234-1
   PubMed Web of Science ®Google Scholar
• Li K, Shi H, Zhang B, Ou X, Ma Q, Chen Y, Shu P, Li D, Wang Y. Myeloid-derived suppressor cells as immunosuppressive regulators and therapeutic targets in cancer. Sig Transduct Target Ther. 2021;6(1):1–25. doi:10.1038/s41392-021-00670-9
   PubMed Web of Science ®Google Scholar
• Man S, Yao J, Lv P, Liu Y, Yang L, Ma L. Curcumin-enhanced antitumor effects of sorafenib via regulating the metabolism and tumor microenvironment. Food Funct. 2020;11(7):6422–32. doi:10.1039/c9fo01901d
   PubMed Web of Science ®Google Scholar
• Liao F, Liu L, Luo E, Hu J. Curcumin enhances anti-tumor immune response in tongue squamous cell carcinoma. Arch Oral Biol. 2018;92:32–7. doi:10.1016/j.archoralbio.2018.04.015
   PubMed Web of Science ®Google Scholar
• Kötting C, Hofmann L, Lotfi R, Engelhardt D, Laban S, Schuler PJ, Hoffmann TK, Brunner C, Theodoraki M-N. Immune-stimulatory effects of curcumin on the tumor microenvironment in head and neck squamous cell carcinoma. Cancers. 2021;13(6):1335. doi:10.3390/cancers13061335
   PubMed Web of Science ®Google Scholar
• Lee HH, Cho H. Improved anti-cancer effect of curcumin on breast cancer cells by increasing the activity of natural killer cells. J Microbiol Biotechnol. 2018;28(6):874–82. doi:10.4014/jmb.1801.01074
   PubMed Web of Science ®Google Scholar
• Chang Y-F, Chuang H-Y, Hsu C-H, Liu R-S, Gambhir SS, Hwang J-J. Immunomodulation of curcumin on adoptive therapy with T cell functional imaging in mice. Cancer Prev Res (Phila). 2012;5(3):444–52. doi:10.1158/1940-6207.CAPR-11-0308
   PubMed Web of Science ®Google Scholar
• Liu L, Lim MA, Jung S-N, Oh C, Won H-R, Jin YL, Piao Y, Kim HJ, Chang JW, Koo BS. The effect of Curcumin on multi-level immune checkpoint blockade and T cell dysfunction in head and neck cancer. Phytomedicine. 2021;92:153758. doi:10.1016/j.phymed.2021.153758
   PubMed Web of Science ®Google Scholar
• Lim S-O, Li C-W, Xia W, Cha J-H, Chan L-C, Wu Y, Chang S-S, Lin W-C, Hsu J-M, Hsu Y-H, et al. Deubiquitination and stabilization of PD-L1 by CSN5. Cancer Cell. 2016;30(6):925–39. doi:10.1016/j.ccell.2016.10.010
   PubMed Web of Science ®Google Scholar
• Lu Y, Miao L, Wang Y, Xu Z, Zhao Y, Shen Y, Xiang G, Huang L. Curcumin micelles remodel tumor microenvironment and enhance vaccine activity in an advanced melanoma model. Mol Therapy. 2016;24(2):364–74. doi:10.1038/mt.2015.165
   PubMed Web of Science ®Google Scholar
• MaruYama T, Kobayashi S, Shibata H, Chen W, Owada Y. Curcumin analog GO‐Y030 boosts the efficacy of anti‐PD‐1 cancer immunotherapy. Cancer Sci. 2021;112(12):4844–52. doi:10.1111/cas.15136
   PubMed Web of Science ®Google Scholar
• Shiri S, Alizadeh AM, Baradaran B, Farhanghi B, Shanehbandi D, Khodayari S, Khodayari H, Tavassoli A. Dendrosomal curcumin suppresses metastatic breast cancer in mice by changing m1/m2 macrophage balance in the tumor microenvironment. Asian Pac J Cancer Prev. 2015;16(9):3917–22. doi:10.7314/APJCP.2015.16.9.3917
   PubMedGoogle Scholar
• Zhang L-J, Huang R, Shen Y-W, Liu J, Wu Y, Jin J-M, Zhang H, Sun Y, Chen H-Z, Luan X. Enhanced anti-tumor efficacy by inhibiting HIF-1α to reprogram TAMs via core-satellite upconverting nanoparticles with curcumin mediated photodynamic therapy. Biomater Sci. 2021;9(19):6403–15. doi:10.1039/d1bm00675d
   PubMed Web of Science ®Google Scholar
• Wang M, Zhao J, Zhang L, Wei F, Lian Y, Wu Y, Gong Z, Zhang S, Zhou J, Cao K, et al. Role of tumor microenvironment in tumorigenesis. J Cancer. 2017;8(5):761–73. doi:10.7150/jca.17648
   PubMed Web of Science ®Google Scholar
• Malandrino A, Mak M, Kamm RD, Moeendarbary E. Complex mechanics of the heterogeneous extracellular matrix in cancer. Extreme Mech Lett. 2018;21:25–34. doi:10.1016/j.eml.2018.02.003
   PubMed Web of Science ®Google Scholar
• Brassart-Pasco S, Brézillon S, Brassart B, Ramont L, Oudart J-B, Monboisse JC. Tumor microenvironment: extracellular matrix alterations influence tumor progression. Front Oncol. 2020;10:397. doi:10.3389/fonc.2020.00397
   PubMed Web of Science ®Google Scholar
• Theocharis AD, Skandalis SS, Gialeli C, Karamanos NK. Extracellular matrix structure. Adv Drug Deliv Rev. 2016;97:4–27. doi:10.1016/j.addr.2015.11.001
   PubMed Web of Science ®Google Scholar
• Shakibaei M, Kraehe P, Popper B, Shayan P, Goel A, Buhrmann C. Curcumin potentiates antitumor activity of 5-fluorouracil in a 3D alginate tumor microenvironment of colorectal cancer. BMC Cancer. 2015;15(1):1–15. doi:10.1186/s12885-015-1291-0
   PubMed Web of Science ®Google Scholar
• Lin S-S, Lai K-C, Hsu S-C, Yang J-S, Kuo C-L, Lin J-P, Ma Y-S, Wu C-C, Chung J-G. Curcumin inhibits the migration and invasion of human A549 lung cancer cells through the inhibition of matrix metalloproteinase-2 and-9 and Vascular Endothelial Growth Factor (VEGF). Cancer Lett. 2009;285(2):127–33. doi:10.1016/j.canlet.2009.04.037
   PubMed Web of Science ®Google Scholar
• Hong J, Ahn K, Bae E, Jeon S, Choi H. The effects of curcumin on the invasiveness of prostate cancer in vitro and in vivo. Prostate Cancer Prostatic Dis. 2006;9(2):147–52. doi:10.1038/sj.pcan.4500856
   PubMed Web of Science ®Google Scholar
• Zong H, Wang F, Fan Q-x, Wang L-x. Curcumin inhibits metastatic progression of breast cancer cell through suppression of urokinase-type plasminogen activator by NF-kappa B signaling pathways. Mol Biol Rep. 2012;39(4):4803–8. doi:10.1007/s11033-011-1273-5
   PubMed Web of Science ®Google Scholar
• Chatterjee A, Mitra A, Ray S, Chattopadhyay N, Siddiqi M. Curcumin exhibits antimetastatic properties by modulating integrin receptors, collagenase activity, and expression of Nm23 and E-cadherin. J Env Path Tox Oncol. 2003;22(1):47–56. doi:10.1615/JEnvPathToxOncol.v22.i1.50
   Google Scholar
• Malik M, Mendoza M, Payson M, Catherino WH. Curcumin, a nutritional supplement with antineoplastic activity, enhances leiomyoma cell apoptosis and decreases fibronectin expression. Fertil Steril. 2009;91(5 Suppl):2177–84. doi:10.1016/j.fertnstert.2008.03.045
   PubMed Web of Science ®Google Scholar
• Li H, Wu H, Zhang H, Li Y, Li S, Hou Q, Wu S, Yang S-Y. Identification of curcumin-inhibited extracellular matrix receptors in non–small cell lung cancer A549 cells by RNA sequencing. Tumour Biol. 2017;39(6):1010428317705334. doi:10.1177/1010428317705334
   Google Scholar
• Im Kim H, Huang H, Cheepala S, Huang S, Chung J. Curcumin inhibition of integrin (α6β4)-dependent breast cancer cell motility and invasion. Cancer Prev Res (Phila). 2008;1(5):385–91. doi:10.1158/1940-6207.CAPR-08-0087
   PubMed Web of Science ®Google Scholar
• Ohashi Y, Tsuchiya Y, Koizumi K, Sakurai H, Saiki I. Prevention of intrahepatic metastasis by curcumin in an orthotopic implantation model. Oncology. 2003;65(3):250–8. doi:10.1159/000074478
   PubMed Web of Science ®Google Scholar
• Qi C, Wang D, Gong X, Zhou Q, Yue X, Li C, Li Z, Tian G, Zhang B, Wang Q, et al. Co-delivery of curcumin and capsaicin by dual-targeting liposomes for inhibition of aHSC-induced drug resistance and metastasis. ACS Appl Mater Interfaces. 2021;13(14):16019–35. doi:10.1021/acsami.0c23137
   PubMed Web of Science ®Google Scholar
• Dudley AC. Tumor endothelial cells. Cold Spring Harb Perspect Med. 2012;2(3):a006536. doi:10.1101/cshperspect.a006536
   PubMed Web of Science ®Google Scholar
• Hida K, Maishi N, Annan DA, Hida Y. Contribution of tumor endothelial cells in cancer progression. Int J Mol Sci. 2018;19(5):1272. doi:10.3390/ijms19051272
   PubMed Web of Science ®Google Scholar
• Chouaib S, Kieda C, Benlalam H, Noman MZ, Mami-Chouaib F, Ruegg C. Endothelial cells as key determinants of the tumor microenvironment: interaction with tumor cells, extracellular matrix and immune killer cells. Crit Rev Immunol. 2010;30(6):529–45. doi:10.1615/CritRevImmunol.v30.i6.30
   PubMed Web of Science ®Google Scholar
• Sobierajska K, Ciszewski WM, Sacewicz-Hofman I, Niewiarowska J. Endothelial cells in the tumor microenvironment. Adv Exp Med Biol. 2020;1234:71–86.
   PubMed Web of Science ®Google Scholar
• Jin G, Yang Y, Liu K, Zhao J, Chen X, Liu H, Bai R, Li X, Jiang Y, Zhang X, et al. Combination curcumin and (−)-epigallocatechin-3-gallate inhibits colorectal carcinoma microenvironment-induced angiogenesis by JAK/STAT3/IL-8 pathway. Oncogenesis. 2017;6(10):e384. doi:10.1038/oncsis.2017.84
   PubMed Web of Science ®Google Scholar
• Vyas D, Gupt S, Dixit V, Anita K, Kaur S. To study the effect of curcumin on the growth properties of circulating endothelial progenitor cells. In Vitro Cell Dev Biol Anim. 2015;51(5):488–94. doi:10.1007/s11626-014-9852-0
   PubMed Web of Science ®Google Scholar
• Matsuo M, Sakurai H, Koizumi K, Saiki I. Curcumin inhibits the formation of capillary-like tubes by rat lymphatic endothelial cells. Cancer Lett. 2007;251(2):288–95. doi:10.1016/j.canlet.2006.11.027
   PubMed Web of Science ®Google Scholar
• Wang W, Sukamtoh E, Xiao H, Zhang G. Curcumin inhibits lymphangiogenesis in vitro and in vivo. Mol Nutr Food Res. 2015;59(12):2345–54. doi:10.1002/mnfr.201500399
   PubMed Web of Science ®Google Scholar
• Yoysungnoen B, Bhattarakosol P, Patumraj S, Changtam C. Effects of tetrahydrocurcumin on hypoxia-inducible factor-1. Biomed Res Int. 2015;2015:391748. doi:10.1155/2015/391748
   PubMed Web of Science ®Google Scholar
• Liu B, Cui L-s, Zhou B, Zhang L-l, h. Liu Z, Zhang L. Monocarbonyl curcumin analog A2 potently inhibits angiogenesis by inducing ROS-dependent endothelial cell death. Acta Pharmacol Sin. 2019;40(11):1412–23. doi:10.1038/s41401-019-0224-x
   PubMed Web of Science ®Google Scholar
• Palange AL, Mascolo DD, Carallo C, Gnasso A, Decuzzi P. Lipid–polymer nanoparticles encapsulating curcumin for modulating the vascular deposition of breast cancer cells. Nanomedicine. 2014;10(5):e991–e1002. doi:10.1016/j.nano.2014.02.004
   PubMed Web of Science ®Google Scholar
• Koo H-J, Shin S, Choi JY, Lee K-H, Kim B-T, Choe YS. Introduction of methyl groups at C2 and C6 positions enhances the antiangiogenesis activity of curcumin. Sci Rep. 2015;5(1):14205–12. doi:10.1038/srep14205
   PubMed Web of Science ®Google Scholar