Startseite Potential anti-cancer activity of Moringa oleifera derived bio-active compounds targeting hypoxia-inducible factor-1 alpha in breast cancer
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Potential anti-cancer activity of Moringa oleifera derived bio-active compounds targeting hypoxia-inducible factor-1 alpha in breast cancer

  • Neha Masarkar , Suman Kumar Ray , Zirha Saleem und Sukhes Mukherjee EMAIL logo
Veröffentlicht/Copyright: 18. September 2023

Abstract

Breast cancer (BC) will become a highly detected malignancy in females worldwide in 2023, with over 2 million new cases. Studies have established the role of hypoxia-inducible factor-1α (HIF1α), a transcription factor that controls cellular response to hypoxic stress, and is essential for BC spread. HIF-1 is implicated in nearly every critical stage of the metastatic progression, including invasion, EMT, intravasation, extravasation, angiogenesis, and the formation of metastatic niches. HIF-1 overexpression has been associated with poor prognosis and increased mortality in BC patients. This is accomplished by controlling the expression of HIF-1 target genes involved in cell survival, angiogenesis, metabolism, and treatment resistance. Studies have indicated that inhibiting HIF-1 has an anti-cancer effect on its own and that inhibiting HIF-1-mediated signaling improves the efficacy of anti-cancer therapy. Approximately 74 % of recognized anti-cancer drugs are sourced from plant species. Studies on anti-cancer characteristics of phytochemicals derived from Moringa oleifera (MO), also known as the ‘Tree of Life’, have revealed a high therapeutic potential for BC. In this review, we have highlighted the various mechanisms through which bioactive compounds present in MO may modulate HIF and its regulatory genes/pathways, to prove their efficacy in treating and preventing BC.


Corresponding author: Dr. Sukhes Mukherjee, Additional Professor, Department of Biochemistry, All India Institute of Medical Sciences Bhopal, 3rd Floor, Medical College Building, Saket Nagar, Bhopal 462020, Madhya Pradesh, India, Phone: +91 9897800194, E-mail:
Neha Masarkar and Suman Kumar Ray contributed equally to this work.
  1. Ethical approval: Not applicable.

  2. Informed consent: Not applicable.

  3. Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.

  4. Competing interests: The authors state no conflict of interest.

  5. Research funding: Not applicable.

References

1. Ray, SK, Mukherjee, S. Hypoxia-inducible factors-based single nucleotide polymorphism in BC with more cancer susceptibility. Curr Mol Med 2023;23:285–8. https://doi.org/10.2174/1566524022666220513124853.Suche in Google Scholar PubMed

2. Al Tameemi, W, Dale, TP, Al-Jumaily, RMK, Forsyth, NR. Hypoxia-modified cancer cell metabolism. Front Cell Dev Biol 2019;7:4. https://doi.org/10.3389/fcell.2019.00004.Suche in Google Scholar PubMed PubMed Central

3. Soni, S, Padwad, YS. HIF-1 in cancer therapy: two-decade long story of a transcription factor. Acta Oncol 2017;56:503–15. https://doi.org/10.1080/0284186X.2017.1301680.Suche in Google Scholar PubMed

4. Rezvani, HR, Ali, N, Nissen, LJ, Harfouche, G, de Verneuil, H, Taïeb, A, et al.. HIF-1α in epidermis: oxygen sensing, cutaneous angiogenesis, cancer, and non-cancer disorders. J Invest Dermatol 2011;131:1793–805. https://doi.org/10.1038/jid.2011.141.Suche in Google Scholar PubMed

5. Xiong, Q, Liu, B, Ding, M, Zhou, J, Yang, C, Chen, Y. Hypoxia and cancer related pathology. Cancer Lett 2020;486:1–7. https://doi.org/10.1016/j.canlet.2020.05.002.Suche in Google Scholar PubMed

6. Schito, L, Semenza, GL. Hypoxia-inducible factors: master regulators of cancer progression. Trends Cancer 2016;2:758–70. https://doi.org/10.1016/j.trecan.2016.10.016.Suche in Google Scholar PubMed

7. Jun, JC, Rathore, A, Younas, H, Gilkes, D, Polotsky, VY. Hypoxia-inducible factors and cancer. Curr Sleep Med Rep 2017;3:1–10. https://doi.org/10.1007/s40675-017-0062-7.Suche in Google Scholar PubMed PubMed Central

8. Wicks, EE, Semenza, GL. Hypoxia-inducible factors: cancer progression and clinical translation. J Clin Invest 2022;132:e159839. https://doi.org/10.1172/JCI159839.Suche in Google Scholar PubMed PubMed Central

9. Infantino, V, Santarsiero, A, Convertini, P, Todisco, S, Iacobazzi, V. Cancer cell metabolism in hypoxia: role of HIF-1 as key regulator and therapeutic target. Int J Mol Sci 2021;22:5703. https://doi.org/10.3390/ijms22115703.Suche in Google Scholar PubMed PubMed Central

10. Jing, X, Yang, F, Shao, C, Wei, K, Xie, M, Shen, H, et al.. Role of hypoxia in cancer therapy by regulating the tumor microenvironment. Mol Cancer 2019;18:157. https://doi.org/10.1186/s12943-019-1089-9.Suche in Google Scholar PubMed PubMed Central

11. de Heer, EC, Jalving, M, Harris, AL. HIFs, angiogenesis, and metabolism: elusive enemies in BC. J Clin Invest 2020;130:5074–87. https://doi.org/10.1172/JCI137552.Suche in Google Scholar PubMed PubMed Central

12. You, L, Wu, W, Wang, X, Fang, L, Adam, V, Nepovimova, E, et al.. The role of hypoxia-inducible factor 1 in tumor immune evasion. Med Res Rev 2021;41:1622–43. https://doi.org/10.1002/med.21771.Suche in Google Scholar PubMed

13. Hashimoto, T, Shibasaki, F. Hypoxia-inducible factor as an angiogenic master switch. Front Pediatr 2015;3:33. https://doi.org/10.3389/fped.2015.00033.Suche in Google Scholar PubMed PubMed Central

14. Yong, L, Tang, S, Yu, H, Zhang, H, Zhang, Y, Wan, Y, et al.. The role of hypoxia-inducible factor-1 alpha in multidrug-resistant BC. Front Oncol 2022;12:964934. https://doi.org/10.3389/fonc.2022.964934.Suche in Google Scholar PubMed PubMed Central

15. Emran, TB, Shahriar, A, Mahmud, AR, Rahman, T, Abir, MH, Siddiquee, MF, et al.. Multidrug resistance in cancer: understanding molecular mechanisms, immunoprevention and therapeutic approaches. Front Oncol 2022;12:891652. https://doi.org/10.3389/fonc.2022.891652.Suche in Google Scholar PubMed PubMed Central

16. Talks, KL, Turley, H, Gatter, KC, Maxwell, PH, Pugh, CW, Ratcliffe, PJ, et al.. The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. Am J Pathol 2000;157:411–21. https://doi.org/10.1016/s0002-9440(10)64554-3.Suche in Google Scholar PubMed PubMed Central

17. Dengler, VL, Galbraith, M, Espinosa, JM. Transcriptional regulation by hypoxia inducible factors. Crit Rev Biochem Mol Biol 2014;49:1–15. https://doi.org/10.3109/10409238.2013.838205.Suche in Google Scholar PubMed PubMed Central

18. Yun, BD, Son, SW, Choi, SY, Kuh, HJ, Oh, TJ, Park, JK. Anti-cancer activity of phytochemicals targeting hypoxia-inducible factor-1 alpha. Int J Mol Sci 2021;22:9819. https://doi.org/10.3390/ijms22189819.Suche in Google Scholar PubMed PubMed Central

19. Hosseini, A, Ghorbani, A. Cancer therapy with phytochemicals: evidence from clinical studies. Avicenna J Phytomed 2015;5:84–97.Suche in Google Scholar

20. Abd Rani, NZ, Husain, K, Kumolosasi, E. Moringa genus: a review of phytochemistry and pharmacology. Front Pharmacol 2018;9:108. https://doi.org/10.3389/fphar.2018.00108.Suche in Google Scholar PubMed PubMed Central

21. Kashyap, P, Kumar, S, Riar, CS, Jindal, N, Baniwal, P, Guiné, RPF, et al.. Recent advances in drumstick (Moringa oleifera) leaves bioactive compounds: composition, health benefits, bioaccessibility, and dietary applications. Antioxidants 2022;11:402. https://doi.org/10.3390/antiox11020402.Suche in Google Scholar PubMed PubMed Central

22. Sung, H, Ferlay, J, Siegel, RL, Laversanne, M, Soerjomataram, I, Jemal, A, et al.. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;71:209–49. https://doi.org/10.3322/caac.21660.Suche in Google Scholar PubMed

23. Arnold, M, Morgan, E, Rumgay, H, Mafra, A, Singh, D, Laversanne, M, et al.. Current and future burden of BC: global statistics for 2020 and 2040. Breast 2022;66:15–23. https://doi.org/10.1016/j.breast.2022.08.010.Suche in Google Scholar PubMed PubMed Central

24. Zhang, Y, Zhang, H, Wang, M, Schmid, T, Xin, Z, Kozhuharova, L, et al.. Hypoxia in BC-scientific translation to therapeutic and diagnostic clinical applications. Front Oncol 2021;11:652266. https://doi.org/10.3389/fonc.2021.652266.Suche in Google Scholar PubMed PubMed Central

25. Mukherjee, S, Ray, SK. Targeting tumor hypoxia and hypoxia-inducible factors (HIFs) for the treatment of cancer- A story of transcription factors with novel approach in molecular medicine. Curr Mol Med 2022;22:285–6. https://doi.org/10.2174/156652402204220325161921.Suche in Google Scholar PubMed

26. Mandl, M, Depping, R. Hypoxia-inducible aryl hydrocarbon receptor nuclear translocator (ARNT) (HIF-1β): is it a rare exception? Mol Med 2014;20:215–20. https://doi.org/10.2119/molmed.2014.00032.Suche in Google Scholar PubMed PubMed Central

27. Haase, VH. The VHL tumor suppressor: master regulator of HIF. Curr Pharmaceut Des 2009;15:3895–903. https://doi.org/10.2174/138161209789649394.Suche in Google Scholar PubMed PubMed Central

28. Strowitzki, MJ, Cummins, EP, Taylor, CT. Protein hydroxylation by hypoxia-inducible factor (HIF) hydroxylases: unique or ubiquitous? Cells 2019;8:384. https://doi.org/10.3390/cells8050384.Suche in Google Scholar PubMed PubMed Central

29. Liu, ZJ, Semenza, GL, Zhang, HF. Hypoxia-inducible factor 1 and BC metastasis. J Zhejiang Univ Sci B 2015;16:32–43. https://doi.org/10.1631/jzus.B1400221.Suche in Google Scholar PubMed PubMed Central

30. Leone, A, Spada, A, Battezzati, A, Schiraldi, A, Aristil, J, Bertoli, S. Moringa oleifera seeds and oil: characteristics and uses for human health. Int J Mol Sci 2016;17:2141. https://doi.org/10.3390/ijms17122141.Suche in Google Scholar PubMed PubMed Central

31. Bhattacharya, A, Tiwari, P, Sahu, PK, Kumar, S. A review of the phytochemical and pharmacological characteristics of Moringa oleifera. J Pharm BioAllied Sci 2018;10:181–91. https://doi.org/10.4103/jpbs.jpbs_126_18.Suche in Google Scholar

32. Berkovich, L, Earon, G, Ron, I, Rimmon, A, Vexler, A, Lev-Ari, S. Moringa Oleifera aqueous leaf extract down-regulates nuclear factor-kappaB and increases cytotoxic effect of chemotherapy in pancreatic cancer cells. BMC Compl Alternative Med 2013;13:212. https://doi.org/10.1186/1472-6882-13-212.Suche in Google Scholar PubMed PubMed Central

33. Jung, IL. Soluble extract from Moringa oleifera leaves with a new anticancer activity. PLoS One 2014;9:e95492. https://doi.org/10.1371/journal.pone.0095492.Suche in Google Scholar PubMed PubMed Central

34. Al-Asmari, AK, Albalawi, SM, Athar, MT, Khan, AQ, Al-Shahrani, H, Islam, M. Moringa oleifera as an anti-cancer agent against breast and colorectal cancer cell lines. PLoS One 2015;10:e0135814. https://doi.org/10.1371/journal.pone.0135814.Suche in Google Scholar PubMed PubMed Central

35. Kou, X, Li, B, Olayanju, JB, Drake, JM, Chen, N. Nutraceutical or pharmacological potential of Moringa oleifera lam. Nutrients 2018;10:343. https://doi.org/10.3390/nu10030343.Suche in Google Scholar PubMed PubMed Central

36. AbdullRazis, AF, Ibrahim, MD, Kntayya, SB. Health benefits of Moringa oleifera. Asian Pac J Cancer Prev 2014;15:8571–6. https://doi.org/10.7314/apjcp.2014.15.20.8571.Suche in Google Scholar PubMed

37. Luo, S, Jiang, Y, Zheng, A, Zhao, Y, Wu, X, Li, M, et al.. Targeting hypoxia-inducible factors for BC therapy: a narrative review. Front Pharmacol 2022;13:1064661. https://doi.org/10.3389/fphar.2022.1064661.Suche in Google Scholar PubMed PubMed Central

38. Kozal, K, Krześlak, A. The role of hypoxia-inducible factor isoforms in BC and perspectives on their inhibition in therapy. Cancers 2022;14:4518. https://doi.org/10.3390/cancers14184518.Suche in Google Scholar PubMed PubMed Central

39. Nagle, DG, Zhou, YD. Natural product-based inhibitors of hypoxia-inducible factor-1 (HIF-1). Curr Drug Targets 2006;7:355–69. https://doi.org/10.2174/138945006776054979.Suche in Google Scholar PubMed PubMed Central

40. Manolescu, B, Oprea, E, Busu, C, Cercasov, C. Natural compounds and the hypoxia-inducible factor (HIF) signalling pathway. Biochimie 2009;91:1347–58. https://doi.org/10.1016/j.biochi.2009.08.005.Suche in Google Scholar PubMed

41. Masarkar, N, Mukherjee, S, Goel, S, Nema, R. Naturally derived formulations and prospects towards cancer. Health 2019;11:971–97. https://doi.org/10.4236/health.2019.117078.Suche in Google Scholar

42. Ekor, M. The growing use of herbal medicines: issues relating to adverse reactions and challenges in monitoring safety. Front Pharmacol 2014;4:177. https://doi.org/10.3389/fphar.2013.00177.Suche in Google Scholar PubMed PubMed Central

43. Harvey, AL. Natural products in drug discovery. Drug Discov Today 2008;13:894–901. https://doi.org/10.1016/j.drudis.2008.07.004.Suche in Google Scholar PubMed

44. Katiyar, C, Gupta, A, Kanjilal, S, Katiyar, S. Drug discovery from plant sources: an integrated approach. Ayu 2012;33:10–9. https://doi.org/10.4103/0974-8520.100295.Suche in Google Scholar PubMed PubMed Central

45. Khan, T, Ali, M, Khan, A, Nisar, P, Jan, SA, Afridi, S, et al.. Anticancer plants: a review of the active phytochemicals, applications in animal models, and regulatory aspects. Biomolecules 2019;10:47. https://doi.org/10.3390/biom10010047.Suche in Google Scholar PubMed PubMed Central

46. Israel, BB, Tilghman, SL, Parker-Lemieux, K, Payton-Stewart, F. Phytochemicals: current strategies for treating BC. Oncol Lett 2018;15:7471–8. https://doi.org/10.3892/ol.2018.8304.Suche in Google Scholar PubMed PubMed Central

47. Li, Y, Zhang, H, Merkher, Y, Chen, L, Liu, N, Leonov, S, et al.. Recent advances in therapeutic strategies for triple-negative BC. J Hematol Oncol 2022;15:121. https://doi.org/10.1186/s13045-022-01341-0.Suche in Google Scholar PubMed PubMed Central

48. Mansoori, B, Mohammadi, A, Davudian, S, Shirjang, S, Baradaran, B. The different mechanisms of cancer drug resistance: a brief review. Adv Pharmaceut Bull 2017;7:339–48. https://doi.org/10.15171/apb.2017.041.Suche in Google Scholar PubMed PubMed Central

49. Samanta, SK, Choudhury, P, Sarma, PP, Gogoi, B, Gogoi, N, Devi, R. Dietary phytochemicals/nutrients as promising protector of BC development: a comprehensive analysis. Pharmacol Rep 2022;74:583–601. https://doi.org/10.1007/s43440-022-00373-0.Suche in Google Scholar PubMed

50. Shoaib, M, Ahmed, SA. Role of natural herbs and phytochemicals to minimize tumor and economic burden in BC treatment. BC (Dove Med Press) 2016;8:241–2. https://doi.org/10.2147/BCTT.S125826.Suche in Google Scholar PubMed PubMed Central

51. Fernando, W, Rupasinghe, HP, Hoskin, DW. Regulation of hypoxia-inducible factor-1α and vascular endothelial growth factor signaling by plant flavonoids. Mini Rev Med Chem 2015;15:479–89. https://doi.org/10.2174/1389557515666150414152933.Suche in Google Scholar PubMed

52. Sohel, M, Aktar, S, Biswas, P, Amin, MA, Hossain, MA, Ahmed, N, et al.. Exploring the anti-cancer potential of dietary phytochemicals for the patients with BC: a comprehensive review. Cancer Med 2023;12:14556–83. https://doi.org/10.1002/cam4.5984.Suche in Google Scholar PubMed PubMed Central

53. Svolacchia, F, Brongo, S, Catalano, A, Ceccarini, A, Svolacchia, L, Santarsiere, A, et al.. Natural products for the prevention, treatment and progression of BC. Cancers 2023;15:2981. https://doi.org/10.3390/cancers15112981.Suche in Google Scholar PubMed PubMed Central

54. Fang, J, Zhou, Q, Liu, LZ, Xia, C, Hu, X, Shi, X, et al.. Apigenin inhibits tumor angiogenesis through decreasing hif-1alpha and vegf expression. Carcinogenesis 2007;28:858–64. https://doi.org/10.1093/carcin/bgl205.Suche in Google Scholar PubMed

55. Zhou, J, Callapina, M, Goodall, GJ, Brune, B. Functional integrity of nuclear factor kappa B, phosphatidylinositol 3’-kinase, and mitogen-activated protein kinase signaling allows tumor necrosis factor alpha-evoked bcl-2 expression to provoke internal ribosome entry site-dependent translation of hypoxia-inducible factor 1alpha. Cancer Res 2004;64:9041–8. https://doi.org/10.1158/0008-5472.can-04-1437.Suche in Google Scholar

56. Tong, X, Pelling, JC. Targeting the pi3k/akt/mtor axis by apigenin for cancer prevention. Anti Cancer Agents Med Chem 2013;13:971–8. https://doi.org/10.2174/18715206113139990119.Suche in Google Scholar PubMed PubMed Central

57. Fang, J, Zhou, Q, Liu, L-Z, Xia, C, Hu, X, Shi, X, et al.. Apigenin inhibits tumor angiogenesis through decreasing HIF-1a and VEGF expression. Carcinogenesis 2007;28:858–64. https://doi.org/10.1093/carcin/bgl205.Suche in Google Scholar

58. Mirzoeva, S, Kim, ND, Chiu, K, Franzen, CA, Bergan, RC, Pelling, JC. Inhibition of HIF-1 alpha and VEGF expression by the chemopreventive bioflavonoid apigenin is accompanied by Akt inhibition in human prostate carcinoma PC3-M cells. Mol Carcinog 2008;47:686–700. https://doi.org/10.1002/mc.20421.Suche in Google Scholar PubMed

59. Melstrom, LG, Salabat, MR, Ding, XZ, Milam, BM, Strouch, M, Pelling, JC, et al.. Apigenin inhibits the GLUT-1 glucose transporter and the phosphoinositide 3-kinase/Akt pathway in human pancreatic cancer cells. Pancreas 2008;37:426–31. https://doi.org/10.1097/MPA.0b013e3181735ccb.Suche in Google Scholar PubMed

60. Park, S, Kim, YS, Lee, HA, Lim, Y, Kim, Y. Mulberry leaf extract inhibits invasive potential and downregulates hypoxia-inducible factor-1α (HIF-1α) in SK-N-BE2C neuroblastoma cells. Biosci Biotechnol Biochem 2013;77:722–8. https://doi.org/10.1271/bbb.120763.Suche in Google Scholar PubMed

61. Singh-Gupta, V, Zhang, H, Banerjee, S, Kong, D, Raffoul, JJ, Sarkar, FH, et al.. Radiation-induced HIF-1alpha cell survival pathway is inhibited by soy isoflavones in prostate cancer cells. Int J Cancer 2009;124:1675–84. https://doi.org/10.1002/ijc.24015.Suche in Google Scholar PubMed PubMed Central

62. Zakaria, S, Nawaya, R, Abdel-Hamid, NM, Eldomany, RA, El-Shishtawy, MM. Targeting the HIF-1α/Cav-1 pathway with a chicory extract/daidzein combination plays a potential role in retarding hepatocellular carcinoma. Curr Cancer Drug Targets 2021;21:881–96. https://doi.org/10.2174/1568009621666210811121120.Suche in Google Scholar PubMed

63. Büchler, P, Reber, HA, Büchler, MW, Friess, H, Lavey, RS, Hines, OJ. Antiangiogenic activity of genistein in pancreatic carcinoma cells is mediated by the inhibition of hypoxia-inducible factor-1 and the down-regulation of VEGF gene expression. Cancer 2004;100:201–10. https://doi.org/10.1002/cncr.11873.Suche in Google Scholar PubMed

64. Zhang, QL, Li, P, Hong, L, Li, RZ, Wang, JQ, Cui, X. The protein tyrosine kinase inhibitor genistein suppresses hypoxia-induced atrial natriuretic peptide secretion mediated by the PI3K/Akt-HIF-1α pathway in isolated beating rat atria. Can J Physiol Pharmacol 2021;99:1184–90. https://doi.org/10.1139/cjpp-2020-0503.Suche in Google Scholar PubMed

65. Tuli, HS, Tuorkey, MJ, Thakral, F, Sak, K, Kumar, M, Sharma, AK, et al.. Molecular mechanisms of action of genistein in cancer: recent advances. Front Pharmacol 2019;10:1336. https://doi.org/10.3389/fphar.2019.01336.Suche in Google Scholar PubMed PubMed Central

66. Seo, S, Seo, K, Ki, SH, Shin, SM. Isorhamnetin inhibits reactive oxygen species-dependent hypoxia inducible factor (HIF)-1α accumulation. Biol Pharm Bull 2016;39:1830–8. https://doi.org/10.1248/bpb.b16-00414.Suche in Google Scholar PubMed

67. Mylonis, I, Lakka, A, Tsakalof, A, Simos, G. The dietary flavonoid kaempferol effectively inhibits HIF-1 activity and hepatoma cancer cell viability under hypoxic conditions. Biochem Biophys Res Commun 2010;398:74–8. https://doi.org/10.1016/j.bbrc.2010.06.038.Suche in Google Scholar PubMed

68. Luo, H, Rankin, GO, Liu, L, Daddysman, MK, Jiang, BH, Chen, YC. Kaempferol inhibits angiogenesis and VEGF expression through both HIF dependent and independent pathways in human ovarian cancer cells. Nutr Cancer 2009;61:554–63. https://doi.org/10.1080/01635580802666281.Suche in Google Scholar PubMed PubMed Central

69. Monti, E, Marras, E, Prini, P, Gariboldi, MB. Luteolin impairs hypoxia adaptation and progression in human breast and colon cancer cells. Eur J Pharmacol 2020;881:173210. https://doi.org/10.1016/j.ejphar.2020.173210.Suche in Google Scholar PubMed

70. Fang, B, Chen, X, Wu, M, Kong, H, Chu, G, Zhou, Z, et al.. Luteolin inhibits angiogenesis of the M2-like TAMs via the downregulation of hypoxia inducible factor-1α and the STAT3 signalling pathway under hypoxia. Mol Med Rep 2018;18:2914–22. https://doi.org/10.3892/mmr.2018.9250.Suche in Google Scholar PubMed

71. Samec, M, Liskova, A, Koklesova, L, Mersakova, S, Strnadel, J, Kajo, K, et al.. Flavonoids targeting HIF-1: implications on cancer metabolism. Cancers 2021;13:130. https://doi.org/10.3390/cancers13010130.Suche in Google Scholar PubMed PubMed Central

72. Huang, H, Chen, AY, Rojanasakul, Y, Ye, X, Rankin, GO, Chen, YC. Dietary compounds galangin and myricetin suppress ovarian cancer cell angiogenesis. J Funct Foods 2015;15:464–75. https://doi.org/10.1016/j.jff.2015.03.051.Suche in Google Scholar PubMed PubMed Central

73. Felice, MR, Maugeri, A, De Sarro, G, Navarra, M, Barreca, D. Molecular pathways involved in the anti-cancer activity of flavonols: a focus on myricetin and kaempferol. Int J Mol Sci 2022;23:4411. https://doi.org/10.3390/ijms23084411.Suche in Google Scholar PubMed PubMed Central

74. Wahyuningsih, SPA, Dewi, FRP, Hsan, ASY, Lim, V, Aun, L, Marviella, S, et al.. The regulation of hypoxia inducible factor (HIF)1α expression by quercetin: an in silico study. Acta Inf Med 2022;30:96–9. https://doi.org/10.5455/aim.2022.30.96-99.Suche in Google Scholar PubMed PubMed Central

75. Kim, HS, Wannatung, T, Lee, S, Yang, WK, Chung, SH, Lim, JS, et al.. Quercetin enhances hypoxia-mediated apoptosis via direct inhibition of AMPK activity in HCT116 colon cancer. Apoptosis 2012;17:938–49. https://doi.org/10.1007/s10495-012-0719-0.Suche in Google Scholar PubMed

76. Lee, DH, Lee, YJ. Quercetin suppresses hypoxia-induced accumulation of hypoxia-inducible factor-1alpha (HIF-1alpha) through inhibiting protein synthesis. J Cell Biochem 2008;105:546–53. https://doi.org/10.1002/jcb.21851.Suche in Google Scholar PubMed

77. Du, G, Lin, H, Wang, M, Zhang, S, Wu, X, Lu, L, et al.. Quercetin greatly improved therapeutic index of doxorubicin against 4T1 BC by its opposing effects on HIF-1α in tumor and normal cells. Cancer Chemother Pharmacol 2010;65:277–87. https://doi.org/10.1007/s00280-009-1032-7.Suche in Google Scholar PubMed

78. Lee, Y, Park, OK. Involvement of AMPK/mTOR/HIF-1α in anticancer control of quercetin in hypoxic MCF-7 cells. Food Sci Biotechnol 2011;20:371–5. https://doi.org/10.1007/s10068-011-0052-3.Suche in Google Scholar

79. Zheng, HL, Yang, J, Hou, Y, Sun, B, Zhang, Q, Mou, Y, et al.. Oligomer procyanidins (F2) isolated from grape seeds inhibits tumor angiogenesis and cell invasion by targeting HIF-1α in vitro. Int J Oncol 2015;46:708–20. https://doi.org/10.3892/ijo.2014.2744.Suche in Google Scholar PubMed

80. Zheng, HL, Wang, LH, Sun, BS, Li, Y, Yang, JY, Wu, CF. Oligomer procyanidins (F2) repress HIF-1α expression in human U87 glioma cells by inhibiting the EGFR/AKT/mTOR and MAPK/ERK1/2 signaling pathways in vitro and in vivo. Oncotarget 2017;8:85252–62. https://doi.org/10.18632/oncotarget.19654.Suche in Google Scholar PubMed PubMed Central

81. Gu, W, Yang, Y, Zhang, C, Zhang, Y, Chen, LJ, Shen, J, et al.. Caffeic acid attenuates the angiogenic function of hepatocellular carcinoma cells via reduction in JNK-1-mediated HIF-1α stabilization in hypoxia. RSC Adv 2016;6:82774–82. https://doi.org/10.1039/c6ra07703j.Suche in Google Scholar

82. Jung, JE, Kim, HS, Lee, CS, Park, DH, Kim, YN, Lee, MJ, et al.. Caffeic acid and its synthetic derivative CADPE suppress tumor angiogenesis by blocking STAT3-mediated VEGF expression in human renal carcinoma cells. Carcinogenesis 2007;28:1780–7. https://doi.org/10.1093/carcin/bgm130.Suche in Google Scholar PubMed

83. Park, JJ, Hwang, SJ, Park, JH, Lee, HJ. Chlorogenic acid inhibits hypoxia-induced angiogenesis via down-regulation of the HIF-1α/AKT pathway. Cell Oncol 2015;38:111–18. https://doi.org/10.1007/s13402-014-0216-2.Suche in Google Scholar PubMed

84. Lee, MS, Lee, SO, Kim, KR, Lee, HJ. Sphingosine kinase-1 involves the inhibitory action of HIF-1α by chlorogenic acid in hypoxic DU145 cells. Int J Mol Sci 2017;18:325. https://doi.org/10.3390/ijms18020325.Suche in Google Scholar PubMed PubMed Central

85. Siswanto, FM, Oguro, A, Imaoka, S. Chlorogenic acid modulates hypoxia response of Hep3B cells. Pers Med Universe 2017;6:12–6. https://doi.org/10.1016/j.pmu.2017.03.001.Suche in Google Scholar

86. Kowshik, J, Giri, H, Kishore, TK, Kesavan, R, Vankudavath, R, Reddy, G, et al.. Ellagic acid inhibits VEGF/VEGFR2, PI3K/Akt and MAPK signaling cascades in the hamster cheek pouch carcinogenesis model. Anti Cancer Agents Med Chem 2014;14:1249–60. https://doi.org/10.2174/1871520614666140723114217.Suche in Google Scholar PubMed

87. He, Z, Chen, AY, Rojanasakul, Y, Rankin, GO, Chen, YC. Gallic acid, a phenolic compound, exerts anti-angiogenic effects via the PTEN/AKT/HIF-1α/VEGF signaling pathway in ovarian cancer cells. Oncol Rep 2016;35:291–7. https://doi.org/10.3892/or.2015.4354.Suche in Google Scholar PubMed PubMed Central

88. Guimaraes, TA, Farias, LC, Fraga, CA, Feltenberger, JD, Melo, GA, Coletta, RD, et al.. Evaluation of the antineoplastic activity of gallic acid in oral squamous cell carcinoma under hypoxic conditions. Anti Cancer Drugs 2016;27:407–16. https://doi.org/10.1097/CAD.0000000000000342.Suche in Google Scholar PubMed

89. Rajakumar, T, Pugalendhi, P. Allyl isothiocyanate inhibits invasion and angiogenesis in BC via EGFR mediated JAK1/STAT3 signaling pathway. Amino Acids 2023. https://doi.org/10.1007/s00726-023-03285-2.Suche in Google Scholar PubMed

90. Boreddy, SR, Sahu, RP, Srivastava, SK. Benzyl isothiocyanate suppresses pancreatic tumor angiogenesis and invasion by inhibiting HIF-α/VEGF/Rho-GTPases: pivotal role of STAT-3. PLoS One 2011;6:e25799. https://doi.org/10.1371/journal.pone.0025799.Suche in Google Scholar PubMed PubMed Central

91. Liu, P, Atkinson, SJ, Akbareian, SE, Zhou, Z, Munsterberg, A, Robinson, SD, et al.. Sulforaphane exerts anti-angiogenesis effects against hepatocellular carcinoma through inhibition of STAT3/HIF-1α/VEGF signalling. Sci Rep 2017;7:12651. https://doi.org/10.1038/s41598-017-12855-w.Suche in Google Scholar PubMed PubMed Central

92. Kim, DH, Sung, B, Kang, YJ, Hwang, SY, Kim, MJ, Yoon, JH, et al.. Sulforaphane inhibits hypoxia-induced HIF-1α and VEGF expression and migration of human colon cancer cells. Int J Oncol 2015;47:2226–32. https://doi.org/10.3892/ijo.2015.3200.Suche in Google Scholar PubMed

93. Yao, H, Wang, H, Zhang, Z, Jiang, BH, Luo, J, Shi, X. Sulforaphane inhibited expression of hypoxia-inducible factor-1alpha in human tongue squamous cancer cells and prostate cancer cells. Int J Cancer 2008;123:1255–61. https://doi.org/10.1002/ijc.23647.Suche in Google Scholar PubMed

94. Jeon, YK, Yoo, DR, Jang, YH, Jang, SY, Nam, MJ. Sulforaphane induces apoptosis in human hepatic cancer cells through inhibition of 6-phosphofructo-2-kinase/fructose-2,6-biphosphatase4, mediated by hypoxia inducible factor-1-dependent pathway. Biochim Biophys Acta 2011;1814:1340–8. https://doi.org/10.1016/j.bbapap.2011.05.015.Suche in Google Scholar PubMed

95. Xia, Y, Kang, TW, Jung, YD, Zhang, C, Lian, S. Sulforaphane inhibits nonmuscle invasive bladder cancer cells proliferation through suppression of HIF-1α-Mediated glycolysis in hypoxia. J Agric Food Chem 2019;67:7844–54. https://doi.org/10.1021/acs.jafc.9b03027.Suche in Google Scholar PubMed

96. Kim, YS, Lee, HA, Lim, JY, Kim, Y, Jung, CH, Yoo, SH, et al.. β-Carotene inhibits neuroblastoma cell invasion and metastasis in vitro and in vivo by decreasing level of hypoxia-inducible factor-1α. J Nutr Biochem 2014;25:655–64. https://doi.org/10.1016/j.jnutbio.2014.02.006.Suche in Google Scholar PubMed

97. Li, Y, Zhang, Y, Liu, X, Wang, M, Wang, P, Yang, J, et al.. Lutein inhibits proliferation, invasion and migration of hypoxic BC cells via downregulation of HES1. Int J Oncol 2018;52:2119–29. https://doi.org/10.3892/ijo.2018.4332.Suche in Google Scholar PubMed

98. Park, EJ, Lee, YM, Oh, TI, Kim, BM, Lim, BO, Lim, JH. Vanillin suppresses cell motility by inhibiting STAT3-mediated HIF-1α mRNA expression in malignant melanoma cells. Int J Mol Sci 2017;18:532. https://doi.org/10.3390/ijms18030532.Suche in Google Scholar PubMed PubMed Central

Received: 2023-07-12
Accepted: 2023-08-13
Published Online: 2023-09-18

© 2023 Walter de Gruyter GmbH, Berlin/Boston

Artikel in diesem Heft

  1. Frontmatter
  2. Reviews
  3. Boldine: a narrative review of the bioactive compound with versatile biological and pharmacological potential
  4. Potential anti-cancer activity of Moringa oleifera derived bio-active compounds targeting hypoxia-inducible factor-1 alpha in breast cancer
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