337
Views
0
CrossRef citations to date
0
Altmetric
Review

Targeting HIF-1 for prostate cancer: a synthesis of preclinical evidence

&
Pages 715-731 | Received 21 May 2023, Accepted 10 Aug 2023, Published online: 24 Aug 2023

References

  • Wang GL, Jiang BH, Rue EA, et al. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci, USA. 1995;92:5510–5514. Available from https://pnas.org/doi/full/10.1073/pnas.92.12.5510.
  • Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem. 1995;270(3):1230–1237. doi: 10.1074/jbc.270.3.1230
  • Jiang B-H, Rue E, Wang GL, et al. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem. 1996;271(30):17771–17778. doi: 10.1074/jbc.271.30.17771
  • YANG C, ZHONG Z-F, WANG S-P, et al. HIF-1: structure, biology and natural modulators. Chin J Nat Med. 2021;19:521–527. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1875536421600511
  • Malkov MI, Lee CT, Taylor CT. Regulation of the hypoxia-inducible factor (HIF) by pro-inflammatory cytokines. Cells. 2021;10(9):2340. doi: 10.3390/cells10092340
  • Ratcliffe PJ. HIF-1 and HIF-2: working alone or together in hypoxia? J Clin Investig. 2007;117(4):862–865. doi: 10.1172/JCI31750
  • Hirota K, Semenza GL. Regulation of angiogenesis by hypoxia-inducible factor 1. Crit Rev Oncol Hematol. 2006;59(1):15–26. doi: 10.1016/j.critrevonc.2005.12.003
  • Taylor SE, Bagnall J, Mason D, et al. Differential sub-nuclear distribution of hypoxia-inducible factors (HIF)-1 and -2 alpha impacts on their stability and mobility. Open Biol. 2016;6(9):160195. doi: 10.1098/rsob.160195
  • Shi Y-H, Fang W-G. Hypoxia-inducible factor-1 in tumour angiogenesis. World J Gastroenterol. 2004;10(8):1082. doi: 10.3748/wjg.v10.i8.1082
  • Jin X, Dai L, Ma Y, et al. Implications of HIF-1α in the tumorigenesis and progression of pancreatic cancer. Cancer Cell Int. 2020;20(1):273. doi: 10.1186/s12935-020-01370-0
  • Masoud GN, Li W. HIF-1α pathway: role, regulation and intervention for cancer therapy. Acta Pharm Sin B. 2015;5(5):378–389. doi: 10.1016/j.apsb.2015.05.007
  • Iommarini L, Porcelli AM, Gasparre G, et al. Non-Canonical mechanisms regulating hypoxia-inducible factor 1 alpha in cancer. Front Oncol. 2017;7. doi: 10.3389/fonc.2017.00286.
  • Miao M, Wu M, Li Y, et al. Clinical potential of hypoxia inducible factors prolyl hydroxylase inhibitors in treating nonanemic diseases. Front Pharmacol [Internet]. 2022;13.
  • Wei J, Yang Y, Lu M, et al. Recent advances in the discovery of HIF-1α-p300/CBP inhibitors as anti-cancer agents. Mini-Rev Med Chem [Internet]. 2018;18. doi: 10.2174/1389557516666160630124938
  • Yang C, Wang W, Li G-D, et al. Anticancer osmium complex inhibitors of the HIF-1α and p300 protein-protein interaction. Sci Rep [Internet]. 2017;7(1):42860. doi: 10.1038/srep42860
  • Cohen M, Amir S, Golan M, et al. β-TrCP upregulates HIF-1 in prostate cancer cells. Prostate [Internet]. 2019;79(4):403–413. doi: 10.1002/pros.23746
  • Amir S, Golan M, Mabjeesh NJ. Targeted knockdown of SEPT9_v1 inhibits tumor growth and angiogenesis of human prostate cancer cells concomitant with disruption of hypoxia-inducible factor-1 pathway. Mol Cancer Res. 2010 [Internet];8(5):643–652. doi: 10.1158/1541-7786.MCR-09-0497
  • Golan M, Mabjeesh NJ. Imaging of hypoxia-inducible factor 1α and septin 9 interaction by bimolecular fluorescence complementation in live cancer cells. Oncotarget. 2017 [Internet];8(19):31830–31841. doi: 10.18632/oncotarget.16527
  • Paatero I, Jokilammi A, Heikkinen PT, et al. Interaction with ErbB4 promotes hypoxia-inducible factor-1α signaling. J Biol Chem [Internet]. 2012;287(13):9659–9671. doi: 10.1074/jbc.M111.299537
  • Takeda N, O’Dea EL, Doedens A, et al. Differential activation and antagonistic function of HIF-α isoforms in macrophages are essential for NO homeostasis. Genes Dev [Internet]. 2010;24(5):491–501. doi: 10.1101/gad.1881410
  • Kristan A, Debeljak N, Kunej T. Integration and visualization of regulatory elements and variations of the EPAS1 gene in human. Genes (Basel). 2021 [Internet];12(11):1793. doi: 10.3390/genes12111793
  • Zhdanov AV, Dmitriev RI, Golubeva AV, et al. Chronic hypoxia leads to a glycolytic phenotype and suppressed HIF-2 signaling in PC12 cells. Biochim Biophys Acta Gen Subj. 2013;1830:3553–3569. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0304416513000597
  • Toschi A, Lee E, Thompson S, et al. Phospholipase D-mTOR requirement for the Warburg effect in human cancer cells. Cancer Lett [Internet]. 2010;299(1):72–79. doi: 10.1016/j.canlet.2010.08.006
  • Compernolle V, Brusselmans K, Acker T, et al. Loss of HIF-2α and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med [Internet]. 2002;8(7):702–710. doi: 10.1038/nm721
  • Mohlin S, Hamidian A, von Stedingk K, et al. PI3K–mTORC2 but not PI3K–mTORC1 regulates transcription of HIF2A/EPAS1 and vascularization in neuroblastoma. Cancer Res [Internet]. 2015;75(21):4617–4628. doi: 10.1158/0008-5472.CAN-15-0708
  • Peng X, Gao H, Xu R, et al. Correction to: the interplay between HIF-1α and noncoding RNAs in cancer. J Exp Clin Cancer Res [Internet]. 2020;39(1):45. doi: 10.1186/s13046-020-01544-8
  • Na Y-R, Han K-C, Park H, et al. Menadione and ethacrynic acid inhibit the hypoxia-inducible factor (HIF) pathway by disrupting HIF-1α interaction with p300. Biochem Biophys Res Commun [Internet]. 2013;434(4):879–884. doi: 10.1016/j.bbrc.2013.04.044
  • Lv X, Li J, Zhang C, et al. The role of hypoxia-inducible factors in tumor angiogenesis and cell metabolism. Genes Dis [Internet]. 2017;4(1):19–24. doi: 10.1016/j.gendis.2016.11.003
  • Kierans SJ, Taylor CT. Regulation of glycolysis by the hypoxia‐inducible factor (HIF): implications for cellular physiology. J Physiol. 2021 [Internet];599(1):23–37. doi: 10.1113/JP280572
  • Ioannidou E, Moschetta M, Shah S, et al. Angiogenesis and anti-angiogenic treatment in prostate cancer: mechanisms of action and molecular targets. Int J Mol Sci [Internet]. 2021;22(18):9926. doi: 10.3390/ijms22189926
  • Haase VH. Hypoxia-inducible factors in the kidney. Am J Physiol Renal Physiol. 2006 [Internet];291(2):F271–F281. doi: 10.1152/ajprenal.00071.2006
  • Jelkmann W. Erythropoietin after a century of research: younger than ever. Eur J Haematol. 2007 [Internet];78(3):183–205. doi: 10.1111/j.1600-0609.2007.00818.x
  • Abdu A, Arogundade F, Adamu B, et al. Anaemia and its response to treatment with recombinant human erythropoietin in chronic kidney disease patients. West Afr J Med. 2010;28. Available from: http://www.ajol.info/index.php/wajm/article/view/55003
  • Semba H, Takeda N, Isagawa T, et al. HIF-1α-PDK1 axis-induced active glycolysis plays an essential role in macrophage migratory capacity. Nat Commun [Internet]. 2016;7(1):11635. doi: 10.1038/ncomms11635
  • Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell. 2012 [Internet];148(3):399–408. doi: 10.1016/j.cell.2012.01.021
  • Moslehi J, Rathmell WK. The 2019 nobel prize honors fundamental discoveries in hypoxia response. Journal Of Clinical Investigation. 2019;130(1):4–6. Available from: https://www.jci.org/articles/view/134813
  • Hirota K. Hypoxia-dependent signaling in perioperative and critical care medicine. J Anesth. 2021;35(5):741–756. doi: 10.1007/s00540-021-02940-w
  • Loenarz C. An oxygen sensation: progress in macromolecule hydroxylation triggered by the elucidation of cellular oxygen sensing. Angew Chem Int Ed. 2020;59:3776–3780. Available from: https://onlinelibrary.wiley.com/doi/10.1002/anie.201913263
  • Végran F, Boidot R, Michiels C, et al. Lactate Influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-κB/IL-8 pathway that drives tumor angiogenesis. Cancer Res [Internet]. 2011;71(7):2550–2560. doi: 10.1158/0008-5472.CAN-10-2828
  • Mullen AR, Wheaton WW, Jin ES, et al. Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature [Internet]. 2012;481(7381):385–388. doi: 10.1038/nature10642
  • Hu H, Takano N, Xiang L, et al. Hypoxia-inducible factors enhance glutamate signaling in cancer cells. Oncotarget [Internet]. 2014;5(19):8853–8868. doi: 10.18632/oncotarget.2593
  • Jun JC, Rathore A, Younas H, et al. Hypoxia-inducible factors and cancer. Curr Sleep Med Rep. 2017;3:1–10. Available from: http://link.springer.com/10.1007/s40675-017-0062-7
  • Colgan SP, Furuta GT, Taylor CT. Hypoxia and Innate immunity: keeping up with the HIFsters. Annu Rev Immunol. 2020 [Internet];38(1):341–363. doi: 10.1146/annurev-immunol-100819-121537
  • McGettrick AF, O’Neill LAJ. The role of HIF in immunity and inflammation. Cell Metab [Internet]. 2020;32(4):524–536. doi: 10.1016/j.cmet.2020.08.002
  • Hsu T-S, Lin Y-L, Wang Y-A, et al. HIF-2α is indispensable for regulatory T cell function. Nat Commun [Internet]. 2020;11(1):5005. doi: 10.1038/s41467-020-18731-y
  • Shi LZ, Wang R, Huang G, et al. HIF1α–dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and treg cells. J Exp Med [Internet]. 2011;208(7):1367–1376. doi: 10.1084/jem.20110278
  • Budda SA, Girton A, Henderson JG, et al. Transcription factor HIF-1α controls expression of the cytokine IL-22 in CD4 T cells. J Immunol [Internet]. 2016;197(7):2646–2652. doi: 10.4049/jimmunol.1600250
  • Taylor CT, Colgan SP. Regulation of immunity and inflammation by hypoxia in immunological niches. Nat Rev Immunol. 2017 [Internet];17(12):774–785. doi: 10.1038/nri.2017.103
  • Mingyuan X, Qianqian P, Shengquan X, et al. Hypoxia-inducible factor-1α activates transforming growth factor-β1/Smad signaling and increases collagen deposition in dermal fibroblasts. Oncotarget. 2018;9(3):3188–3197. doi: 10.18632/oncotarget.23225
  • Taylor CT, Kent BD, Crinion SJ, et al. Human adipocytes are highly sensitive to intermittent hypoxia induced NF-kappaB activity and subsequent inflammatory gene expression. Biochem Biophys Res Commun [Internet]. 2014;447(4):660–665. doi: 10.1016/j.bbrc.2014.04.062
  • Ando A, Hashimoto N, Sakamoto K, et al. Repressive role of stabilized hypoxia inducible factor 1α expression on transforming growth factor β‐induced extracellular matrix production in lung cancer cells. Cancer Sci [Internet]. 2019;110(6):1959–1973. doi: 10.1111/cas.14027
  • Zhong H, Chiles K, Feldser D, et al. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res . 2000 [cited 2000 Mar 15];60: 1541–1545. Available from http://www.ncbi.nlm.nih.gov/pubmed/10749120
  • Paul SAM, Simons JW, Mabjeesh NJ. HIF at the crossroads between ischemia and carcinogenesis. J Cell Physiol. 2004 [Internet];200(1):20–30. doi: 10.1002/jcp.10479
  • Hui AS, Bauer AL, Striet JB, et al. Calcium signaling stimulates translation of HIF‐α during hypoxia. FASEB J [Internet]. 2006;20(3):466–475. doi: 10.1096/fj.05-5086com
  • Manisterski M, Golan M, Amir S, et al. Hypoxia induces PTHrP gene transcription in human cancer cells through the HIF-2α. Cell Cycle [Internet]. 2010;9(18):3747–3753. doi: 10.4161/cc.9.18.12931
  • Liao J, Li X, Koh AJ, et al. Tumor expressed PTHrP facilitates prostate cancer-induced osteoblastic lesions. Int J Cancer [Internet]. 2008;123(10):2267–2278. doi: 10.1002/ijc.23602
  • Zhang Z, Karthaus WR, Lee YS, et al. Tumor microenvironment-derived NRG1 promotes antiandrogen resistance in prostate cancer. Cancer Cell [Internet]. 2020;38(2):279–296.e9. doi: 10.1016/j.ccell.2020.06.005
  • Hong S-S, Lee H, Kim K-W. HIF-1α: a Valid therapeutic target for tumor therapy. Cancer Res Treat. 2004 [Internet];36(6):343. doi: 10.4143/crt.2004.36.6.343
  • Kim LC, Simon MC. Hypoxia-inducible factors in cancer. Cancer Res. 2022;82:195–196. Available from: https://aacrjournals.org/cancerres/article/82/2/195/675484/Hypoxia-Inducible-Factors-in-CancerHypoxia
  • Patel SA, Simon MC. Biology of hypoxia-inducible factor-2α in development and disease. Cell Death Differ. 2008 [Internet];15(4):628–634. doi: 10.1038/cdd.2008.17
  • Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Sci (1979). 2009 [Internet];324(5930):1029–1033. doi: 10.1126/science.1160809
  • Li Y, Sun X-X, Qian DZ, et al. Molecular crosstalk between MYC and HIF in cancer. Front Cell Dev Biol [Internet]. 2020;8.
  • Aponte PM, Caicedo A. Stemness in cancer: Stem cells, cancer stem cells, and their microenvironment. Stem Cells Int [Internet]. 2017;2017:1–17. doi: 10.1155/2017/5619472
  • Yun Z, Lin Q. Hypoxia and regulation of cancer cell stemness. Adv Exp Med Biol. 2014;41–53. Available from: https://link.springer.com/10.1007/978-1-4614-5915-6_2
  • Shah S, Rachmat R, Enyioma S, et al. BRCA mutations in prostate cancer: assessment, implications and treatment considerations. Int J Mol Sci [Internet]. 2021;22(23):12628. doi: 10.3390/ijms222312628
  • Ni Raghallaigh H, Eeles R. Genetic predisposition to prostate cancer: an update. Fam Cancer. 2022 [Internet];21(1):101–114. doi: 10.1007/s10689-021-00227-3
  • Attard G, Murphy L, Clarke NW, et al. Abiraterone acetate and prednisolone with or without enzalutamide for high-risk non-metastatic prostate cancer: a meta-analysis of primary results from two randomised controlled phase 3 trials of the STAMPEDE platform protocol. Lancet [Internet]. 2022;399(10323):447–460. doi: 10.1016/S0140-6736(21)02437-5
  • Milosevic M, Warde P, Ménard C, et al. Tumor hypoxia predicts biochemical failure following radiotherapy for clinically localized prostate cancer. Clin Cancer Res [Internet]. 2012;18(7):2108–2114. doi: 10.1158/1078-0432.CCR-11-2711
  • Tran MGB, Bibby BAS, Yang L, et al. Independence of HIF1a and androgen signaling pathways in prostate cancer. BMC Cancer [Internet]. 2020;20(1):469. doi: 10.1186/s12885-020-06890-6
  • Ablain J, Liu S, Moriceau G, et al. SPRED1 deletion confers resistance to MAPK inhibition in melanoma. J Exp Med [Internet]. 2021;218(3). doi: 10.1084/jem.20201097
  • Kawazoe T, Taniguchi K. The sprouty/spred family as tumor suppressors: coming of age. Cancer Sci. 2019 [Internet];110(5):1525–1535. doi: 10.1111/cas.13999
  • Kachroo N, Valencia T, Warren AY, et al. Evidence for downregulation of the negative regulator SPRED2 in clinical prostate cancer. Br J Cancer [Internet]. 2013;108(3):597–601. doi: 10.1038/bjc.2012.507
  • Taylor BS, Schultz N, Hieronymus H, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell [Internet]. 2010;18(1):11–22. doi: 10.1016/j.ccr.2010.05.026
  • Jiang C-F, Shi Z-M, Li D-M, et al. Estrogen-induced miR-196a elevation promotes tumor growth and metastasis via targeting SPRED1 in breast cancer. Mol Cancer [Internet]. 2018;17(1):83. doi: 10.1186/s12943-018-0830-0
  • Seligson DB, Yu H, Tze S, et al. IGFBP-3 nuclear localization predicts human prostate cancer recurrence. Horm Cancer [Internet]. 2013;4(1):12–23. doi: 10.1007/s12672-012-0124-8
  • Mehta HH, Gao Q, Galet C, et al. IGFBP-3 is a metastasis suppression gene in prostate cancer. Cancer Res [Internet]. 2011;71(15):5154–5163. doi: 10.1158/0008-5472.CAN-10-4513
  • Miyata Y, Sakai H, Kanda S, et al. Expression of insulin-like growth factor binding protein-3 before and after neoadjuvant hormonal therapy in human prostate cancer tissues: correlation with histopathologic effects and biochemical recurrence. Urology [Internet]. 2004;63(6):1184–1190. doi: 10.1016/j.urology.2004.02.015
  • Igarashi K, Yui Y, Watanabe K, et al. Molecular evidence of IGFBP-3 dependent and independent VD3 action and its nonlinear response on IGFBP-3 induction in prostate cancer cells. BMC Cancer [Internet]. 2020;20(1):802. doi: 10.1186/s12885-020-07310-5
  • Ranasinghe WKB, Xiao L, Kovac S, et al. The role of hypoxia-inducible factor 1α in determining the properties of castrate-resistant prostate cancers. Agoulnik IU, editor. PLoS One. 2013;8:e54251. Available from: https://dx.plos.org/10.1371/journal.pone.0054251
  • Mei L, Nave K-A. Neuregulin-ERBB signaling in the nervous system and neuropsychiatric diseases. Neuron. 2014 [Internet];83(1):27–49. doi: 10.1016/j.neuron.2014.06.007
  • Xu Y, Li X, Liu X, et al. Neuregulin-1/ErbB signaling and chronic heart failure. Adv Pharmacol. 2010;31–51. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1054358910590021
  • Mitani T, Harada N, Nakano Y, et al. Coordinated action of hypoxia-inducible factor-1α and β-catenin in androgen receptor signaling. J Biol Chem [Internet]. 2012;287(40):33594–33606. doi: 10.1074/jbc.M112.388298
  • Yang M-H, Wu M-Z, Chiou S-H, et al. Direct regulation of TWIST by HIF-1α promotes metastasis. Nat Cell Biol [Internet]. 2008;10(3):295–305. doi: 10.1038/ncb1691
  • Zhang J, Zhang S, Gao S, et al. HIF-1α, TWIST-1 and ITGB-1, associated with tumor stiffness, as novel predictive markers for the pathological response to neoadjuvant chemotherapy in breast cancer. Cancer Manag Res. 2020;12:2209–2222. Available from: https://www.dovepress.com/hif-1alpha-twist-1-and-itgb-1-associated-with-tumor-stiffness-as-novel-peer-reviewed-article-CMAR
  • Chen P-C, Tai H-C, Lin T-H, et al. CCN3 promotes epithelial-mesenchymal transition in prostate cancer via FAK/Akt/HIF-1α-induced twist expression. Oncotarget [Internet]. 2017;8(43):74506–74518. doi: 10.18632/oncotarget.20171
  • Børretzen A, Gravdal K, Haukaas SA, et al. The epithelial–mesenchymal transition regulators twist, slug, and snail are associated with aggressive tumour features and poor outcome in prostate cancer patients. J Pathol Clin Res [Internet]. 2021;7(3):253–270. doi: 10.1002/cjp2.202
  • Abdelrahman AE, Arafa SA, Ahmed RA. Prognostic value of twist-1, e-cadherin and ezh2 in prostate cancer: an immunohistochemical study. Turk J Pathol 2017;33. doi: 10.5146/tjpath.2016.01392
  • Eisermann K, Fraizer G. The androgen receptor and VEGF: mechanisms of androgen-regulated angiogenesis in prostate cancer. Cancers (Basel). 2017 [Internet];9(12):32. doi: 10.3390/cancers9040032
  • Mabjeesh NJ, Willard MT, Frederickson CE, et al. Androgens stimulate hypoxia-inducible factor 1 activation via autocrine loop of tyrosine kinase receptor/phosphatidylinositol 3’-kinase/protein kinase B in prostate cancer cells. Clin Cancer Res. 2003 [cited 2003 Jul 1];9:2416–2425. Available from http://www.ncbi.nlm.nih.gov/pubmed/12855613
  • Eisermann K, Broderick CJ, Bazarov A, et al. Androgen up-regulates vascular endothelial growth factor expression in prostate cancer cells via an Sp1 binding site. Mol Cancer [Internet]. 2013;12(1):7. doi: 10.1186/1476-4598-12-7
  • Duque JLF, Loughlin KR, Adam RM, et al. Measurement of plasma levels of vascular endothelial growth factor in prostate cancer patients: relationship with clinical stage, Gleason score, prostate volume, and serum prostate-specific antigen. Clinics [Internet]. 2006 [cited 2006 Jan 23]];61(5):401–408. doi: 10.1590/S1807-59322006000500006
  • Caine GJ, Ryan P, Lip GYH, et al. Significant decrease in angiopoietin-1 and angiopoietin-2 after radical prostatectomy in prostate cancer patients. Cancer Lett [Internet]. 2007;251(2):296–301. doi: 10.1016/j.canlet.2006.11.026
  • Barata PC, Cooney M, Mendiratta P, et al. Phase I/II study evaluating the safety and clinical efficacy of temsirolimus and bevacizumab in patients with chemotherapy refractory metastatic castration-resistant prostate cancer. Invest New Drugs [Internet]. 2019;37(2):331–337. doi: 10.1007/s10637-018-0687-5
  • McKay RR, Zurita AJ, Werner L, et al. A randomized phase ii trial of short-course androgen deprivation therapy with or without bevacizumab for patients with recurrent prostate cancer after definitive local therapy. J Clin Oncol [Internet]. 2016;34(16):1913–1920. doi: 10.1200/JCO.2015.65.3154
  • Li H, Wang J, Jin Y, et al. Hypoxia upregulates the expression of lncRNA H19 in non-small cell lung cancer cells and induces drug resistance. Transl Cancer Res TCR [Internet]. 2022;11(8):2876–2886. doi: 10.21037/tcr-22-1812
  • Marengo B, Garbarino O, Speciale A, et al. MYC expression and metabolic redox changes in cancer cells: a synergy able to induce chemoresistance. Oxid Med Cell Longev [Internet]. 2019;2019:1–9. doi: 10.1155/2019/7346492
  • Icard P, Shulman S, Farhat D, et al. How the Warburg effect supports aggressiveness and drug resistance of cancer cells? Drug Resist Updat. 2018;38:1–11. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1368764618300219
  • Tan H. The association between hypoxia-inducible factor 1a, autophagy and cell stemness in tumor cells. AIP Conf Proc. 2021;020019. Available from: https://pubs.aip.org/aip/acp/article/731290
  • Sweeney CJ, Chen Y-H, Carducci M, et al. Chemohormonal therapy in metastatic hormone-sensitive prostate cancer. N Engl J Med [Internet]. 2015;373(8):737–746. doi: 10.1056/NEJMoa1503747
  • Belkahla S, Nahvi I, Biswas S, et al. Advances and development of prostate cancer, treatment, and strategies: a systemic review. Front Cell Dev Biol [Internet]. 2022;10.
  • Qian DZ, Rey S, Liu JO, et al. Retraction for Lee et al., Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells. Proc Natl Acad Sci. 2022;119. Available from: https://pnas.org/doi/full/10.1073/pnas.2213285119
  • Laber DA, Eatrides J, Jaglal MV, et al. A phase I/II study of docetaxel in combination with pegylated liposomal doxorubicin in metastatic castration-resistant prostate cancer. Med Oncol. 2020;37:95. Available from: https://link.springer.com/10.1007/s12032-020-01420-7
  • Soung N-K, Kim H-M, Asami Y, et al. Mechanism of the natural product moracin-O derived MO-460 and its targeting protein hnRNPA2B1 on HIF-1α inhibition. Exp Mol Med [Internet]. 2019;51(2):1–14. doi: 10.1038/s12276-018-0200-4
  • Kang T-S, Wang W, Zhong H-J, et al. An anti-prostate cancer benzofuran-conjugated iridium(III) complex as a dual inhibitor of STAT3 and NF-κB. Cancer Lett [Internet]. 2017;396:76–84. doi: 10.1016/j.canlet.2017.03.016
  • Bertozzi D, Marinello J, Manzo SG, et al. The natural inhibitor of DNA Topoisomerase i, camptothecin, modulates HIF-1α activity by changing miR expression patterns in human cancer cells. Mol Cancer Ther [Internet]. 2014;13(1):239–248. doi: 10.1158/1535-7163.MCT-13-0729
  • Gigliotti CL, Minelli R, Cavalli R, et al. In vitro and in vivo therapeutic evaluation of camptothecin-encapsulated β-cyclodextrin nanosponges in prostate cancer. J Biomed Nanotechnol. 2016;12:114–127. Available from: http://openurl.ingenta.com/content/xref?genre=article&issn=1550-7033&volume=12&issue=1&spage=114
  • Green AK, Corty RW, Wood WA, et al. Comparative effectiveness of mitoxantrone plus prednisone versus prednisone alone in metastatic castrate-resistant prostate cancer after docetaxel failure. Oncology [Internet]. 2015;20(5):516–522. doi: 10.1634/theoncologist.2014-0432
  • Kantoff PW, Halabi S, Conaway M, et al. Hydrocortisone with or without mitoxantrone in men with hormone-refractory prostate cancer: results of the cancer and leukemia group B 9182 study. J Clin Oncol [Internet]. 1999;17(8):2506–2506. doi: 10.1200/JCO.1999.17.8.2506
  • Dueck AC, Scher HI, Bennett AV, et al. Assessment of adverse events from the patient perspective in a phase 3 metastatic castration-resistant prostate cancer Clinical trial. JAMA Oncol. 2020;6:e193332. Available from: https://jamanetwork.com/journals/jamaoncology/fullarticle/2751871
  • Basch EM, Scholz MC, De Bono JS, et al. Final analysis of COMET-2: cabozantinib (Cabo) versus mitoxantrone/prednisone (MP) in metastatic castration-resistant prostate cancer (mCRPC) patients (pts) with moderate to severe pain who were previously treated with docetaxel (D) and abiraterone (A) and/or enzalutamide (E). J Clin Oncol. 2015;33:141–141. Available from: https://ascopubs.org/doi/10.1200/jco.2015.33.7_suppl.141
  • Karasneh RA, Murray LJ, Hughes CM, et al. Digoxin use after diagnosis of prostate cancer and survival: a population-based cohort study. Pharmacoepidemiol Drug Saf [Internet]. 2016;25(9):1099–1103. doi: 10.1002/pds.4018
  • Lin J, Hoffman-Censits JH, Duffy D, et al. A pilot phase II study of digoxin in patients with recurrent prostate cancer as evident by a rising PSA. J Clin Oncol [Internet]. 2013;31(15_suppl):5061–5061. doi: 10.1200/jco.2013.31.15_suppl.5061
  • Butt NA, Kumar A, Dhar S, et al. Targeting MTA 1/HIF ‐1 α signaling by pterostilbene in combination with histone deacetylase inhibitor attenuates prostate cancer progression. Cancer Med. 2017;6:2673–2685. Available from: https://onlinelibrary.wiley.com/doi/10.1002/cam4.1209
  • Reece KM, Richardson ED, Cook KM, et al. Epidithiodiketopiperazines (ETPs) exhibit in vitro antiangiogenic and in vivo antitumor activity by disrupting the HIF-1α/p300 complex in a preclinical model of prostate cancer. Mol Cancer [Internet]. 2014;13(1):91. doi: 10.1186/1476-4598-13-91
  • Kemp Bohan PM, Chick RC, O’Shea AE, et al. Phase I trial of encapsulated Rapamycin in patients with prostate cancer under active surveillance to prevent progression. Cancer Prev Res [Internet]. 2021;14(5):551–562. doi: 10.1158/1940-6207.CAPR-20-0383
  • Peng J, He Z, Yuan Y, et al. Docetaxel suppressed cell proliferation through Smad3/HIF-1α-mediated glycolysis in prostate cancer cells. Cell Commun Signaling [Internet]. 2022;20(1):194. doi: 10.1186/s12964-022-00950-z
  • Lage DE, Michaelson MD, Lee RJ, et al. Outcomes of older men receiving docetaxel for metastatic hormone-sensitive prostate cancer. Prostate Cancer Prostatic Dis [Internet]. 2021;24(4):1181–1188. doi: 10.1038/s41391-021-00389-2
  • Kyriakopoulos CE, Chen Y-H, Carducci MA, et al. Chemohormonal therapy in metastatic hormone-sensitive prostate cancer: long-term survival analysis of the randomized phase III E3805 CHAARTED trial. J Clin Oncol [Internet]. 2018;36(11):1080–1087. doi: 10.1200/JCO.2017.75.3657
  • Muldong M, Lee S, Mendoza T, et al. PD07-04 pre-clinical studies for advancing cirmtuzumab-based anti-ror1 therapies in metastatic prostate cancer. J Urol [Internet]. 2022;207(Supplement 5). doi: 10.1097/JU.0000000000002526.04
  • ZHENG R-P, WANG W, WEI C-D. Bortezomib inhibits cell proliferation in prostate cancer. Exp Ther Med. 2015 [Internet];10(3):1219–1223. doi: 10.3892/etm.2015.2617
  • Dreicer R, Petrylak D, Agus D, et al. Phase I/II study of Bortezomib plus docetaxel in patients with advanced androgen-independent prostate cancer. Clin Cancer Res [Internet]. 2007;13(4):1208–1215. doi: 10.1158/1078-0432.CCR-06-2046
  • Kuroda K, Liu H. The proteasome inhibitor, bortezomib, induces prostate cancer cell death by suppressing the expression of prostate-specific membrane antigen, as well as androgen receptor. Int J Oncol. 2019;54. Available from: http://www.spandidos-publications.com/10.3892/ijo.2019.4706
  • Zhang Y, Liu Q, Wei W, et al. Bortezomib potentiates antitumor activity of mitoxantrone through dampening Wnt/β-catenin signal pathway in prostate cancer cells. BMC Cancer [Internet]. 2021;21(1):1101. doi: 10.1186/s12885-021-08841-1
  • Lee Y-J, Song H, Yoon YJ, et al. Ethacrynic acid inhibits STAT3 activity through the modulation of SHP2 and PTP1B tyrosine phosphatases in DU145 prostate carcinoma cells. Biochem Pharmacol [Internet]. 2020;175:113920. doi: 10.1016/j.bcp.2020.113920
  • Martí JM, Garcia-Diaz A, Delgado-Bellido D, et al. Selective modulation by PARP-1 of HIF-1α-recruitment to chromatin during hypoxia is required for tumor adaptation to hypoxic conditions. Redox Biol [Internet]. 2021;41:101885. doi: 10.1016/j.redox.2021.101885
  • de Bono J, Mateo J, Fizazi K, et al. Olaparib for metastatic castration-resistant prostate cancer. N Engl J Med [Internet]. 2020;382(22):2091–2102. doi: 10.1056/NEJMoa1911440
  • Mateo J, Porta N, Bianchini D, et al. Olaparib in patients with metastatic castration-resistant prostate cancer with DNA repair gene aberrations (TOPARP-B): a multicentre, open-label, randomised, phase 2 trial. Lancet Oncol [Internet]. 2020;21(1):162–174. doi: 10.1016/S1470-2045(19)30684-9
  • Kageyama Y, Sugiyama H, Ayame H, et al. Suppression of VEGF transcription in renal cell carcinoma cells by pyrrole-imidazole hairpin polyamides targeting the hypoxia responsive element. Acta Oncol (Madr). 2006;45:317–324. Available from. doi: 10.1080/02841860500486648
  • Yang F, Nickols NG, Li BC, et al. Antitumor activity of a pyrrole-imidazole polyamide. Proc Natl Acad Sci, USA. 2013;110(5):1863–1868. Available from: https://pnas.org/doi/full/10.1073/pnas.1222035110
  • Kurmis AA, Yang F, Welch TR, et al. A pyrrole-imidazole polyamide is active against enzalutamide-resistant prostate cancer. Cancer Res [Internet]. 2017;77(9):2207–2212. doi: 10.1158/0008-5472.CAN-16-2503
  • Ganapathy M, Ghosh R, Jianping X, et al. Involvement of FLIP in 2-methoxyestradiol–Induced tumor regression in transgenic adenocarcinoma of mouse prostate model. Clin Cancer Res [Internet]. 2009;15(5):1601–1611. doi: 10.1158/1078-0432.CCR-08-1389
  • Ghosh R, Ganapathy M, Alworth WL, et al. Corrigendum to “combination of 2-methoxyestradiol (2-ME2) and eugenol for apoptosis induction synergistically in androgen independent prostate cancer cells” [J. Steroid Biochem. Mol. Biol. 113 (2009) 25–35]. J Steroid Biochem Mol Biol. 2021;(213):105962. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0960076021001552
  • Batth IS, Huang S-B, Villarreal M, et al. Evidence for 2-methoxyestradiol-mediated inhibition of receptor tyrosine kinase RON in the management of prostate cancer. Int J Mol Sci [Internet]. 2021;22(4):1852. doi: 10.3390/ijms22041852
  • Mabjeesh NJ, Escuin D, LaVallee TM, et al. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell [Internet]. 2003;3(4):363–375. doi: 10.1016/S1535-6108(03)00077-1
  • Ryu S, Lim W, Bazer FW, et al. Chrysin induces death of prostate cancer cells by inducing ROS and ER stress. J Cell Physiol [Internet]. 2017;232(12):3786–3797. doi: 10.1002/jcp.25861
  • Altabbal S, Athamnah K, Rahma A, et al. Propolis: A Detailed Insight of its anticancer molecular mechanisms. Pharmaceuticals [Internet]. 2023;16(3):450. doi: 10.3390/ph16030450
  • Pavese JM, Krishna SN, Bergan RC. Genistein inhibits human prostate cancer cell detachment, invasion, and metastasis. Am J Clin Nutr [Internet]. 2014;100:431S–436S. doi: 10.3945/ajcn.113.071290
  • Lakshman M, Xu L, Ananthanarayanan V, et al. Dietary genistein inhibits metastasis of human prostate cancer in mice. Cancer Res [Internet]. 2008;68(6):2024–2032. doi: 10.1158/0008-5472.CAN-07-1246
  • SZLISZKA E, ZYDOWICZ G, MIZGALA E, et al. Artepillin C (3,5-diprenyl-4-hydroxycinnamic acid) sensitizes LNCaP prostate cancer cells to TRAIL-induced apoptosis. Int J Oncol [Internet]. 2012;41(3):818–828. doi: 10.3892/ijo.2012.1527
  • Tseng J-C, Lin C-Y, Su L-C, et al. CAPE suppresses migration and invasion of prostate cancer cells via activation of non-canonical Wnt signaling. Oncotarget [Internet]. 2016;7(25):38010–38024. doi: 10.18632/oncotarget.9380
  • Nair HK, Rao KVK, Aalinkeel R, et al. Inhibition of prostate cancer cell colony formation by the flavonoid quercetin correlates with modulation of specific regulatory genes. Clin Vaccin Immunol [Internet]. 2004;11(1):63–69. doi: 10.1128/CDLI.11.1.63-69.2004
  • Puppo M, Battaglia F, Ottaviano C, et al. Topotecan inhibits vascular endothelial growth factor production and angiogenic activity induced by hypoxia in human neuroblastoma by targeting hypoxia-inducible factor-1α and -2α. Mol Cancer Ther [Internet]. 2008;7(7):1974–1984. doi: 10.1158/1535-7163.MCT-07-2059
  • Hörmann V, Kumi-Diaka J, Durity M, et al. Anticancer activities of genistein-topotecan combination in prostate cancer cells. J Cell Mol Med [Internet]. 2012;16(11):2631–2636. doi: 10.1111/j.1582-4934.2012.01576.x
  • Hu Y, Sun H, Owens RT, et al. Decorin suppresses prostate tumor growth through inhibition of epidermal growth factor and androgen receptor pathways. Neoplasia [Internet]. 2009;11(10):1042–1053. doi: 10.1593/neo.09760
  • Li H-X, Gao J-M, Liang J-Q, et al. Vitamin D 3 potentiates the growth inhibitory effects of metformin in DU145 human prostate cancer cells mediated by AMPK/mTOR signalling pathway. Clin Exp Pharmacol Physiol [Internet]. 2015;42(6):711–717. doi: 10.1111/1440-1681.12409
  • Thakur MK, Heilbrun LK, Sheng S, et al. A phase II trial of ganetespib, a heat shock protein 90 Hsp90) inhibitor, in patients with docetaxel-pretreated metastatic castrate-resistant prostate cancer (CRPC)-a prostate cancer clinical trials consortium (PCCTC) study. Invest New Drugs [Internet]. 2016;34(1):112–118. doi: 10.1007/s10637-015-0307-6
  • Ying W, Du Z, Sun L, et al. Ganetespib, a unique triazolone-containing hsp90 inhibitor, exhibits potent antitumor activity and a superior safety profile for cancer therapy. Mol Cancer Ther [Internet]. 2012;11(2):475–484. doi: 10.1158/1535-7163.MCT-11-0755
  • Sun H-L, Liu Y-N, Huang Y-T, et al. YC-1 inhibits HIF-1 expression in prostate cancer cells: contribution of Akt/NF-κB signaling to HIF-1α accumulation during hypoxia. Oncogene [Internet]. 2007;26(27):3941–3951. doi: 10.1038/sj.onc.1210169
  • Zhang J, Wu D, He Y, et al. Rapamycin inhibits AR signaling pathway in prostate cancer by interacting with the FK1 domain of FKBP51. Biochem Biophys Rep [Internet]. 2020;23:100778. doi: 10.1016/j.bbrep.2020.100778
  • Manohar SM, Padgaonkar AA, Jalota-Badhwar A, et al. A novel inhibitor of hypoxia-inducible factor-1α P3155 also modulates PI3K pathway and inhibits growth of prostate cancer cells. BMC Cancer [Internet]. 2011;11(1):338. doi: 10.1186/1471-2407-11-338

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.