AccScience Publishing / GPD / Volume 3 / Issue 2 / DOI: 10.36922/gpd.3431
REVIEW

Opportunities and challenges of integrating HIF-1 into clinical practice for cancer treatment

Maria Vasileiou1* Christina Tsianava2 Sotirios Charalampos Diamantoudis3 Teodora Mazneva4 Kleio Giortsiou3
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1 Department of Pharmacy, School of Health Sciences, National and Kapodistrian University of Athens, Athens, Greece
2 Department of Pharmacy, School of Health Sciences, University of Patras, Rion, Greece
3 School of Pharmacy, Faculty of Health Sciences, Aristotle University of Thessaloniki, Thessaloniki, Greece
4 Faculty of Pharmacy, Ss Cyril and Methodius University, Skopje, Republic of North Macedonia
Submitted: 16 April 2024 | Accepted: 18 June 2024 | Published: 28 June 2024
© 2024 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
Abstract

The Warburg effect is one of the most studied mechanisms involved in cancer progression. It refers to the increased glucose uptake by cancer cells through aerobic glycolysis, instead of the Krebs cycle that takes place under normal conditions, followed by lactic acid fermentation. This mechanism is regulated by hypoxia-inducible factor-1 (HIF-1), a transcription factor that regulates the expression of genes responsible for the synthesis of proteins involved in glucose metabolism. Overexpression of HIF-1 has been linked to the Warburg effect. While several HIF-1-targeted strategies have been investigated, the majority have proven to be unsuccessful, especially in cases of aggressive tumors with hypoxic tumor microenvironments. Current strategies expand beyond conventional chemotherapeutic agents and include chemodynamic therapy, radiation therapy, and immune checkpoint molecules. The aim of this literature review is to highlight the implication of HIF-1 in the Warburg effect and the limitations that render cancer treatment less effective.

Keywords
HIF-1
Warburg effect
Cancer metabolism
Hypoxia
Angiogenesis
Drug resistance
Funding
None.
Conflict of interest
The authors declare that they have no competing interests.
References
  1. Mattiuzzi C, Lippi G. Current cancer epidemiology. J Epidemiol Glob Health. 2019;9(4):217-222. doi: 10.2991/jegh.k.191008.001

 

  1. American Cancer Society. Cancer Facts and Figures. American Cancer Society; 2022. Available from: https:// www.cancer.org/research/cancer-facts-statistics/all-cancer-facts-figures/cancer-facts-figures-2022.html [Last accessed on 2024 Apr 10].

 

  1. Liberti MV, Locasale JW. The Warburg effect: How does it benefit cancer cells? Trends Biochem Sci. 2016;41(3):211-218. doi: 10.1016/j.tibs.2015.12.001

 

  1. Gaidai O, Yan P, Xing Y. Future world cancer death rate prediction. Sci Rep. 2023;13(1):303. doi: 10.1038/s41598-023-27547-x

 

  1. World Health Organization. “Cancer.” World Health Organization; 2022. Available from: https://www.who.int/ news-room/fact-sheets/detail/cancer [Last accessed on 2024 Apr 10].

 

  1. Icard P, Shulman S, Farhat D, Steyaert JM, Alifano M, Lincet H. How the Warburg effect supports aggressiveness and drug resistance of cancer cells? Drug Resist Updates. 2018;38:1-11. doi: 10.1016/j.drup.2018.03.001

 

  1. Wilde L, Roche M, Domingo-Vidal M, et al. Metabolic coupling and the reverse Warburg effect in cancer: Implications for novel biomarker and anticancer agent development. Semin Oncol. 2017;44(3):198-203. doi: 10.1053/j.seminoncol.2017.10.004

 

  1. Bhattacharya B, Mohd Omar MF, Soong R. The Warburg effect and drug resistance. Br J Pharmacol. 2016;173(6):970-979. doi: 10.1111/bph.13422

 

  1. Weidemann A, Johnson RS. Biology of HIF-1 α. Cell Death Different. 2008;15(4):621-627. doi: 10.1038/cdd.2008.12

 

  1. Smith TG, Robbins PA, Ratcliffe PJ. The human side of hypoxia-inducible factor. Br J Haematol. 2008;141(3):325-334. doi: 10.1111/j.1365-2141.2008.07029.x

 

  1. Yang SL, Wu C, Xiong ZF, Fang X. Progress on hypoxia-inducible factor-3: Its structure, gene regulation and biological function (Review). Mol Med Rep. 2015;12(2):2411-2416. doi: 10.3892/mmr.2015.3689

 

  1. Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell. 2012;148(3):399-408. doi: 10.1016%2Fj.cell.2012.01.021

 

  1. Dengler VL, Galbraith MD, Espinosa JM. Transcriptional regulation by hypoxia inducible factors. Crit Rev Biochem Mol Biol. 2013;49(1):1-15. doi: 10.3109/10409238.2013.838205

 

  1. Courtnay R, Ngo DC, Malik N, Ververis K, Tortorella SM, Karagiannis TC. Cancer metabolism and the Warburg effect: The role of HIF-1 and PI3K. Mol Biol Rep. 2015;42(4):841-851. doi: 10.1007/s11033-015-3858-x

 

  1. Nagao A, Kobayashi M, Koyasu S, Chow CCT, Harada H. HIF-1-dependent reprogramming of glucose metabolic pathway of cancer cells and its therapeutic significance. Int J Mol Sci. 2019;20(2):238. doi: 10.3390/ijms20020238

 

  1. Lu H, Li X, Luo Z, Liu J, Fan Z. Cetuximab reverses the Warburg effect by inhibiting HIF-1-regulated LDH-A. Mol Cancer Ther. 2013;12(10):2187-2199. doi: 10.1158/1535-7163.mct-12-1245

 

  1. Vaupel P, Multhoff G. Revisiting the Warburg effect: Historical dogma versus current understanding. J Physiol. 2021;599(6):1745-1757. doi: 10.1113/jp278810

 

  1. Gao JL, Chen Y. Natural compounds regulate glycolysis in hypoxic tumor microenvironment. Biomed Res Int. 2015;2015:354143. doi: 10.1155/2015/354143

 

  1. Ferraro E, Germanò M, Mollace R, Mollace V, Malara N. HIF-1, the Warburg effect, and macrophage/microglia polarization potential role in COVID-19 pathogenesis. Oxid Med Cell Longev. 2021;2021:8841911. doi: 10.1155/2021/8841911

 

  1. Balamurugan K. HIF-1 at the crossroads of hypoxia, inflammation, and cancer. Int J Cancer. 2015;138(5):1058-1066. doi: 10.1002/ijc.29519

 

  1. Semenza GL. Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology. Annu Rev Pathol. 2014;9(1):47-71. doi: 10.1146/annurev-pathol-012513-104720

 

  1. Keith B, Johnson RS, Simon MC. HIF1α and HIF2α: Sibling rivalry in hypoxic tumor growth and progression. Nat Rev Cancer. 2011;12(1):9-22. doi: 10.1038/nrc3183

 

  1. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE. 2005;306:re12. doi: 10.1126/stke.3062005re12

 

  1. Zhong H, De Marzo AM, Laughner E, et al. Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res. 1999;59(22):5830-5835.

 

  1. Scholz CC, Taylor CT. Targeting the HIF pathway in inflammation and immunity. Curr Opin Pharmacol. 2013;13(4):646-653. doi: 10.1016/j.coph.2013.04.009

 

  1. Cramer T, Yamanishi Y, Clausen BE, et al. HIF-1α is essential for myeloid cell-mediated inflammation. Cell. 2003;112(5):645-657. doi: 10.1016/S0092-8674(03)00154-5

 

  1. Shah YM, Ito S, Morimura K, et al. Hypoxia-inducible factor augments experimental colitis through an MIF-dependent inflammatory signaling cascade. Gastroenterology. 2008;134(7):2036-2048.e3. doi: 10.1053/j.gastro.2008.03.009

 

  1. Kim J, Tchernyshyov I, Semenza GL, Dang CV. HIF-1- mediated expression of pyruvate dehydrogenase kinase: A metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006,3(3):177-185. doi: 10.1016/j.cmet.2006.02.002

 

  1. Chan SY, Zhang YY, Hemann C, Mahoney CE, Zweier JL, Loscalzo J. MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron-sulfur cluster assembly proteins ISCU1/2. Cell Metab. 2009;10(4):273-284. doi: 10.1016/j.cmet.2009.08.015

 

  1. Zhang H, Gao P, Fukuda R, et al. HIF-1 Inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell. 2007;11(5):407-420. doi: 10.1016/j.ccr.2007.04.001

 

  1. Lu J, Tan M, Cai Q. The Warburg effect in tumor progression: Mitochondrial oxidative metabolism as an anti-metastasis mechanism. Cancer Lett. 2015;356(2):156-164. doi: 10.1016/j.canlet.2014.04.001

 

  1. Mimeault M, Batra SK. Hypoxia-inducing factors as master regulators of stemness properties and altered metabolism of cancer- and metastasis-initiating cells. J Cell Mol Med. 2013;17(1):30-54. doi: 10.1111/jcmm.12004

 

  1. Erler JT, Bennewith KL, Cox TR, et al. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell. 2009;15(1):35-44. doi: 10.1016/j.ccr.2008.11.012

 

  1. Wong CCL, Gilkes DM, Zhang H, et al. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc Natl Acad Sci. 2011;108(39):16369-16374. doi: 10.1073/pnas.1113483108

 

  1. Suva LJ, Griffin RJ, Makhoul I. Mechanisms of bone metastases of breast cancer. Endocr Relat Cancer. 2009;16(3):703-713. doi: 10.1677/erc-09-0012

 

  1. Nobuaki A, Kobayashi M, Horiuchi I, et al. Constitutive expression of hypoxia-inducible factor-1alpha renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation. Cancer Res. 2001;61(17):6548-6554.

 

  1. Kasuya K. Hypoxia-inducible factor-1α expression and gemcitabine chemotherapy for pancreatic cancer. Oncol Rep. 2011;26:1399-1406. doi: 10.3892/or.2011.1457

 

  1. Mamlouk S, Wielockx B. Hypoxia-inducible factors as key regulators of tumor inflammation. Int J Cancer. 2012;132(12):2721-2729. doi: 10.1002/ijc.27901

 

  1. Arantzazu A, Caro D, Vara A, Julián A, Vidal F, Landázuri MO. C-Jun and hypoxia-inducible factor 1 functionally cooperate in hypoxia-induced gene transcription. Mol Cell Biol. 2002;22(1):12-22. doi: 10.1128/mcb.22.1.12-22.2002

 

  1. Hoesel B, Schmid JA. The complexity of NF-ΚB signaling in inflammation and cancer. Mol Cancer. 2013;12(1):86. doi: 10.1186/1476-4598-12-86

 

  1. Lavecchia A, Di Giovanni C, Cerchia C. Novel inhibitors of signal transducer and activator of transcription 3 signaling pathway: An update on the recent patent literature. Expert Opin Ther Pat. 2014;24(4):383-400. doi: 10.1517/13543776.2014.877443

 

  1. Zong WX, Edelstein LC, Chen C, Bash J, Gelinas C. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappa B that blocks TNFalpha -induced apoptosis. Genes Dev. 1999;13(4):382-387. doi: 10.1101/gad.13.4.382

 

  1. Jung JE, Lee HG, Cho IH, et al. STAT3 is a potential modulator of HIF‐1‐mediated VEGF expression in human renal carcinoma cells. FASEB J. 2005;19(10):1296-1298. doi: 10.1096/fj.04-3099fje

 

  1. Pawlus MR, Wang L, Hu CJ. STAT3 and HIF1α cooperatively activate HIF1 target genes in MDA-MB-231 and RCC4 cells. Oncogene. 2013;33(13):1670-1679. doi: 10.1038/onc.2013.115

 

  1. Noman MZ, Buart S, Pelt JV, et al. The cooperative induction of hypoxia-inducible factor-1α and STAT3 during hypoxia induced an impairment of tumor susceptibility to CTL-mediated cell lysis. J Immunol. 2009;182(6):3510-3521. doi: 10.4049/jimmunol.0800854

 

  1. Tewari R, Choudhury SR, Ghosh S, Mehta VS, Sen E. Involvement of TNFα-induced TLR4-NF-ΚB and TLR4– HIF-1α feed-forward loops in the regulation of inflammatory responses in glioma. J Mol Med. 2011;90(1):67-80. doi: 10.1007/s00109-011-0807-6

 

  1. Zhang JJ. Expression and significance of TLR4 and HIF-1α in pancreatic ductal adenocarcinoma. World J Gastroenterol. 2010;16(23):2881. doi: 10.3748/wjg.v16.i23.2881

 

  1. Marin-Hernandez A, Gallardo-Perez J, Ralph S, Rodriguez- Enriquez S, Moreno-Sanchez R. HIF-1α modulates energy metabolism in cancer cells by inducing over-expression of specific glycolytic isoforms. Mini Rev Med Chem. 2009;9(9):1084-1101. doi: 10.2174/138955709788922610

 

  1. Wojtkowiak JW, Verduzco D, Schramm KJ, Gillies RJ. Drug resistance and cellular adaptation to tumor acidic PH microenvironment. Mol Pharm. 2011;8(6):2032-2038. doi: 10.1021/mp200292c

 

  1. Spivak-Kroizman TR, Hostetter G, Posner R, et al. Hypoxia triggers hedgehog-mediated tumor-stromal interactions in pancreatic cancer. Cancer Res. 2013;73(11):3235-3247. doi: 10.1158/0008-5472.can-11-1433

 

  1. Chafe SC, Lou Y, Sceneay J, et al. Carbonic anhydrase IX promotes myeloid-derived suppressor cell mobilization and establishment of a meta-static niche by stimulating G-CSF production. Cancer Res. 2015;75(6):996-1008. doi: 10.1158/0008-5472.can-14-3000

 

  1. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2014;15(3):178-196. doi: 10.1038/nrm3758

 

  1. Copple BL. Hypoxia stimulates hepatocyte epithelial to mesenchymal transition by hypoxia-inducible factor and transforming growth factor-β-dependent mechanisms. Liver Int. 2010;30(5):669-682. doi: 10.1111/j.1478-3231.2010.02205.x

 

  1. Jiang YG, Luo Y, He D, et al. Role of Wnt/β-catenin signaling pathway in epithelial-mesenchymal transition of human prostate cancer induced by hypoxia-inducible factor-1α. Int J Urol. 2007;14(11):1034-1039. doi: 10.1111/j.1442-2042.2007.01866.x

 

  1. Zhang Q, Bai X, Chen W, et al. Wnt/β-catenin signaling enhances hypoxia-induced epithelial-mesenchymal transition in hepatocellular carcinoma via crosstalk with hif-1α signaling. Carcinogenesis. 2013;34(5):962-973. doi: 10.1093/carcin/bgt027

 

  1. Bendris N, Arsic N, Lemmers B, Blanchard JM. Cyclin A2, Rho GTPases and EMT. Small GTPases. 2012;3(4):225-228. doi: 10.4161/sgtp.20791

 

  1. Hosseini K, Frenzel A, Fischer‐Friedrich E. EMT induces characteristic changes of Rho GTPases and downstream effectors with a mitosis-specific twist. Phys Biol. 2023;20(6):6001. doi: 10.1088/1478-3975/acf5bd

 

  1. Turcotte S. HIF-1alpha MRNA and protein upregulation involves Rho GTPase expression during hypoxia in renal cell carcinoma. J Cell Sci. 2003;116(11):2247-2260. doi: 10.1242/jcs.00427

 

  1. Weidemann A, Breyer J, Rehm M, et al. HIF-1α activation results in actin cytoskeleton reorganization and modulation of Rac-1 signaling in endothelial cells. Cell Commun Signal. 2013;11(1):80. doi: 10.1186/1478-811x-11-80

 

  1. Singh AK, Arya RK, Maheshwari S, et al. Tumor heterogeneity and cancer stem cell paradigm: Updates in concept, controversies and clinical relevance. Int J Cancer. 2014;136(9):1991-2000. doi: 10.1002/ijc.28804

 

  1. Lan L, Luo Y, Cui D, et al. Epithelial-mesenchymal transition triggers cancer stem cell generation in human thyroid cancer cells. Int J Oncol. 2013;43(1):113-120. doi: 10.3892/ijo.2013.1913

 

  1. Luo Y, Cui X, Zhao J, et al. Cells susceptible to epithelial-mesenchymal transition are enriched in stem-like side population cells from prostate cancer. Oncol Rep. 2013;31(2):874-884. doi: 10.3892/or.2013.2905

 

  1. Schwab LP, Peacock DL, Majumdar D, et al. Hypoxia-inducible factor 1α promotes primary tumor growth and tumor-initiating cell activity in breast cancer. Breast Cancer Res. 2012;14(1):R6. doi: 10.1186/bcr3087

 

  1. Zhu H, Wang D, Zhang L, et al. Upregulation of autophagy by hypoxia-inducible factor-1α promotes EMT and metastatic ability of CD133+ pancreatic cancer stem-like cells during intermittent hypoxia. Oncol Rep. 2014;32(3):935-942. doi: 10.3892/or.2014.3298

 

  1. Giannoni E, Parri M, Chiarugi P. EMT and oxidative stress: A bidirectional interplay affecting tumor malignancy. Antioxid Redox Signal. 2012;16(11):1248-1263. doi: 10.1089/ars.2011.4280

 

  1. Calvani M, Comito G, Giannoni E, Chiarugi P. Time-dependent stabilization of hypoxia inducible factor-1α by different intracellular sources of reactive oxygen species. PLoS One. 2012;7(10):e38388. doi: 10.1371/journal.pone.0038388

 

  1. Cho KH, Choi MJ, Jeong KJ, et al. A ROS/STAT3/HIF-1α signaling cascade mediates EGF-induced TWIST1 expression and prostate cancer cell invasion. Prostate. 2014;74(5):528-536. doi: 10.1002/pros.22776

 

  1. Seebacher NA, Richardson DR, Jansson PJ. Glucose modulation induces reactive oxygen species and increases P-glycoprotein-mediated multidrug resistance to chemotherapeutics. Br J Pharmacol. 2015;172(10):2557-2572. doi: 10.1111/bph.13079

 

  1. Yang Y, Lu H, Chen C, Lyu Y, Cole RN, Semenza GL. HIF-1 interacts with TRIM28 and DNA-PK to release paused RNA polymerase II and activate target gene transcription in response to hypoxia. Nat Commun. 2022;13(1):316. doi: 10.1038/s41467-021-27944-8

 

  1. Lyu Y, Yang Y, Talwar V, et al. Hypoxia-inducible factor 1 recruits FACT and RNF20/40 to mediate histone ubiquitination and transcriptional activation of target genes. Cell Rep. 2024;43(4):113972. doi: 10.1016/j.celrep.2024.113972

 

  1. Fleyshman D, Prendergast L, Safina A, et al. Level of fact defines the transcriptional landscape and aggressive phenotype of breast cancer cells. Oncotarget. 2017;8(13):20525-20542. doi: 10.18632/oncotarget.15656

 

  1. Hirota K, Semenza GL. Regulation of hypoxia-inducible factor 1 by prolyl and asparaginyl hydroxylases. Biochem Biophys Res Commun. 2005;338(1):610-616. doi: 10.1016/j.bbrc.2005.08.193

 

  1. Harada H. How can we overcome tumor hypoxia in radiation therapy? J Radiat Res. 2011;52(5):545-556. doi: 10.1269/jrr.11056

 

  1. Jiang BH, Agani F, Passaniti A, Semenza GL. V-SRC induces expression of hypoxia-inducible factor 1 (HIF-1) and transcription of genes encoding vascular endothelial growth factor and enolase 1: Involvement of HIF-1 in tumor progression. Cancer Res. 1997;57(23):5328-5335.

 

  1. Zhu B, Cao X, Zhang W, et al. MicroRNA‐31‐5p enhances the Warburg effect via targeting FIH. FASEB J. 2019;33(1):545-556. doi: 10.1096/fj.201800803r

 

  1. Li SJ, Liu HL, Tang SL, Li XJ, Wang XY. MicroRNA-150 regulates glycolysis by targeting von hippel-lindau in glioma cells. Am J Transl Res. 2017;9(3):1058-1066.

 

  1. Goto Y, Zeng L, Yeom CJ, et al. UCHL1 provides diagnostic and antimetastatic strategies due to its deubiquitinating effect on HIF-1α. Nat Commun. 2015;6(1):6153. doi: 10.1038/ncomms7153

 

  1. Zeng L, Morinibu A, Kobayashi M, et al. Aberrant IDH3α expression promotes malignant tumor growth by inducing HIF-1-mediated metabolic reprogramming and angiogenesis. Oncogene. 2014;34(36):4758-4766. doi: 10.1038/onc.2014.411

 

  1. Nakashima R, Goto Y, Koyasu S, et al. UCHL1-HIF-1 axis-mediated antioxidant property of cancer cells as a therapeutic target for radiosensitization. Sci Rep. 2017;7(1):6879. doi: 10.1038/s41598-017-06605-1

 

  1. Yeom CJ, Zeng L, Goto Y, et al. LY6E: A conductor of malignant tumor growth through modulation of the PTEN/ PI3K/Akt/HIF-1 axis. Oncotarget. 2016;7(40):65837-65848. doi: 10.18632/oncotarget.11670

 

  1. Koh MY, Powis G. HAF: The new player in oxygen-independent HIF-1α degradation. Cell Cycle. 2009;8(9):1359-1366. doi: 10.4161/cc.8.9.8303

 

  1. Guan Z, Ding C, Du Y, et al. HAF drives the switch of HIF-1α to HIF-2α by activating the NF-ΚB pathway, leading to malignant behavior of T24 bladder cancer cells. Int J Oncol. 2013;44(2):393-402. doi: 10.3892/ijo.2013.2210

 

  1. Koh MY, Lemos R, Liu X, Powis G. The hypoxia-associated factor switches cells from HIF-1 - to HIF-2 -dependent signaling promoting stem cell characteristics, aggressive tumor growth and invasion. Cancer Res. 2011;71(11):4015-4027. doi: 10.1158/0008-5472.can-10-4142

 

  1. Shurin MR, Umansky V. Cross-talk between HIF and PD-1/ PD-L1 pathways in carcinogenesis and therapy. J Clin Invest. 2022;132(9):e159473. doi: 10.1172/jci159473

 

  1. Samec M, Liskova A, Koklesova L, et al. Flavonoids targeting HIF-1: Implications on cancer metabolism. Cancers (Basel). 2021;13(1):130. doi: 10.3390/cancers13010130

 

  1. Onnis B, Rapisarda A, Melillo G. Development of HIF-1 inhibitors for cancer therapy. J Cell Mol Med. 2009;13(9a):2780-2786. doi: 10.1111/j.1582-4934.2009.00876.x

 

  1. Ziello JE, Jovin IS, Huang Y. Hypoxia-inducible factor (HIF)-1 regulatory pathway and its potential for therapeutic intervention in malignancy and ischemia. Yale J Biol Med. 2007;80(2):51-60.

 

  1. Afsar CU, Uysal P. HIF-1α levels in patients receiving chemoradiotherapy for locally advanced non-small cell lung carcinoma. Rev Assoc Méd Bras (1992). 2019;65(10):1295-1299. doi: 10.1590/1806-9282.65.10.1295

 

  1. Warfel NA, El-Deiry WS. HIF-1 signaling in drug resistance to chemotherapy. Curr Med Chem. 2014;21(26):3021-3028. doi: 10.2174/0929867321666140414101056

 

  1. Jin X, Gong L, Peng Y, Li L, Liu G. Enhancer-bound Nrf2 licenses HIF-1α transcription under hypoxia to promote cisplatin resistance in hepatocellular carcinoma cells. Aging (Albany NY). 2020;13(1):364. doi: 10.18632/aging.202137

 

  1. Zhang X, He C, Liu X, et al. One-pot synthesis of a microporous organosilica-coated cisplatin nanoplatform for HIF-1-targeted combination cancer therapy. Theranostics. 2020;10(7):2918-2929. doi: 10.7150/thno.41077

 

  1. Peng J, Zhang H, Yuan Y, et al. Docetaxel suppressed cell proliferation through Smad3/HIF-1α-mediated glycolysis in prostate cancer cells. Cell Commun Signal. 2022;20(1):194. doi: 10.1186/s12964-022-00950-z

 

  1. Oh ET, Kim CW, Kim SJ, Lee JS, Hong SS, Park HJ. Docetaxel induced-JNK2/PHD1 signaling pathway increases degradation of HIF-1α and causes cancer cell death under hypoxia. Sci Rep. 2016;6(1):27382. doi: 10.1038/srep27382

 

  1. Dingemans AMC, Groen HJM, Herder GJM, et al. Randomized phase II study comparing paclitaxel-carboplatin-bevacizumab with or without nitroglycerin patches in patients with stage IV nonsquamous nonsmall-cell lung cancer: NVALT12 (NCT01171170). Ann Oncol. 2015;26(11):2286-2293. doi: 10.1093/annonc/mdv370

 

  1. Yasuda H, Nakayama K, Watanabe M, et al. Nitroglycerin treatment may enhance chemosensitivity to docetaxel and carboplatin in patients with lung adenocarcinoma. Clin Cancer Res. 2006;12(22):6748-6757. doi: 10.1158/1078-0432.ccr-06-1124

 

  1. Arrieta O, Blake M, de la Mata-Moya MD, et al. Phase II study. Concurrent chemotherapy and radiotherapy with nitroglycerin in locally advanced non-small cell lung cancer. Radiother Oncol. 2014;111(2):311-315. doi: 10.1016/j.radonc.2014.01.021

 

  1. Li H, Sun X, Li J, et al. Hypoxia induces docetaxel resistance in triple-negative breast cancer via the HIF-1α/MiR-494/ survivin signaling pathway. Neoplasia. 2022;32:100821. doi: 10.1016/j.neo.2022.100821

 

  1. Doublier S, Belisario DC, Polimeni M, et al. HIF-1 activation induces doxorubicin resistance in MCF7 3-D spheroids via P-glycoprotein expression: A potential model of the chemo-resistance of invasive micropapillary carcinoma of the breast. BMC Cancer. 2012;12(1):4. doi: 10.1186/1471-2407-12-4

 

  1. Fourie C, du Plessis M, Mills J, Engelbrecht AM. The effect of HIF-1α inhibition in breast cancer cells prior to doxorubicin treatment under conditions of normoxia and hypoxia. Exp Cell Res. 2022;419(2):113334. doi: 10.1016/j.yexcr.2022.113334

 

  1. Yang Y, Chen DZ, Rey S, Liu JO, Semenza GL. Daily administration of low-dose daunorubicin or doxorubicin inhibits hypoxia-inducible factor 1 and tumor vascularization. bioRxiv. 2022:492526. doi: 10.1101/2022.06.15.492526

 

  1. Syukri A, Budu HM, Amir M, et al. Doxorubicin induced immune abnormalities and inflammatory responses via HMGB1, HIF1-α and VEGF pathway in progressive of cardiovascular damage. Ann Med Surg (Lond). 2022;76:103501. doi: 10.1016/j.amsu.2022.103501

 

  1. Xu L, Zhang Z, Ding Y, et al. Bifunctional liposomes reduce the chemotherapy resistance of doxorubicin induced by reactive oxygen species. Biomater Sci. 2019;7(11):4782-4789. doi: 10.1039/C9BM00590K

 

  1. Xiang L, Wang Y, Lan J, et al. HIF-1-dependent heme synthesis promotes gemcitabine resistance in human non-small cell lung cancers via enhanced ABCB6 expression. Cell Mol Life Sci. 2022;79(6):343. doi: 10.1007/s00018-022-04360-9

 

  1. Runglawan S, Yingpinyapat K, Suyanee T, et al. Potential role of HIF-1-responsive MicroRNA210/hif3 axis on gemcitabine resistance in cholangiocarcinoma cells. PLoS One. 2018;13(6):e0199827. doi: 10.1371/journal.pone.0199827

 

  1. Zhao T, Ren H, Jia L, et al. Inhibition of HIF-1α by PX-478 enhances the anti-tumor effect of gemcitabine by inducing immunogenic cell death in pancreatic ductal adenocarcinoma. Oncotarget. 2014;6(4):2250-2262. doi: 10.18632/oncotarget.2948

 

  1. Wouters A, Pauwels B, Burrows N, et al. The radiosensitising effect of gemcitabine and its main metabolite DFdU under low oxygen conditions is in vitro not dependent on functional HIF-1 protein. BMC Cancer. 2014;14(1):594. doi: 10.1186/1471-2407-14-594

 

  1. Kang G, Hu M, Ren H, et al. VHH212 nanobody targeting the hypoxia-inducible factor 1α suppresses angiogenesis and potentiates gemcitabine therapy in pancreatic cancer in vivo. Cancer Biol Med. 2021;18(3):772-787. doi: 10.20892/j.issn.2095-3941.2020.0568

 

  1. Wang X, Zhong X, Liu Z, Cheng L. Recent progress of chemodynamic therapy-induced combination cancer therapy. Nano Today. 2020;35:100946. doi: 10.1016/j.nantod.2020.100946

 

  1. Zhang X, He C, He X, et al. HIF-1 inhibitor-based one-stone-two-birds strategy for enhanced cancer chemodynamic-immunotherapy. J Controll Rel. 2023;356:649-662. doi: 10.1016/j.jconrel.2023.03.026

 

  1. He C, Zhang X, Chen C, et al. A solid lipid coated calcium peroxide nanocarrier enables combined cancer chemo/ chemodynamic therapy with O2/H2O2 self-sufficiency. Acta Biomater. 2021;122:354-364. doi: 10.1016/j.actbio.2020.12.036

 

  1. Huang R, Zhou PK. HIF-1 signaling: A key orchestrator of cancer radioresistance. Radiat Med Protect. 2020;1(1):7-14. doi: 10.1016/j.radmp.2020.01.006

 

  1. Multhoff G, Radons J, Vaupel P. Critical role of aberrant angiogenesis in the development of tumor hypoxia and associated radioresistance. Cancers (Basel). 2014;6(2):813-828. doi: 10.3390/cancers6020813

 

  1. Boulefour W, Rowinski E, Louati S, et al. A review of the role of hypoxia in radioresistance in cancer therapy. Med Sci Monit. 2021;27:e934116. doi: 10.12659/MSM.934116

 

  1. Calvo-Asensio I, Dillon ET, Lowndes NF, Ceredig R. The transcription factor Hif-1 enhances the radio-resistance of mouse MSCs. Front Physiol. 2018;9:439. doi: 10.3389/fphys.2018.00439

 

  1. Wiechec E, Matic N, Ali A, Roberg K. Hypoxia induces radioresistance, epithelialmesenchymal transition, cancer stem celllike phenotype and changes in genes possessing multiple biological functions in head and neck squamous cell carcinoma. Oncol Rep. 2022;47(3):58. doi: 10.3892/or.2022.8269

 

  1. Hennessey D, Martin LM, Atzberger A, Lynch TH, Hollywood D, Marignol L. Exposure to hypoxia following irradiation increases radioresistance in prostate cancer cells. Urol Oncol. 2013;31(7):1106-1116. doi: 10.1016/j.urolonc.2011.10.008

 

  1. Kabakov AE, Yakimova AO. Hypoxia-induced cancer cell responses driving radioresistance of hypoxic tumors: Approaches to targeting and radiosensitizing. Cancers (Basel). 2021;13(5):1102. doi: 10.3390/cancers13051102

 

  1. Domènech M, Hernández A, Plaja A, Martínez-Balibrea E, Balañà C. Hypoxia: The cornerstone of glioblastoma. Int J Mol Sci. 2021;22(22):12608. doi: 10.3390/ijms222212608

 

  1. Feng H, Wang J, Chen W, et al. Hypoxia-induced autophagy as an additional mechanism in human osteosarcoma radioresistance. J Bone Oncol. 2016;5(2):67-73. doi: 10.1016/j.jbo.2016.03.001

 

  1. Guo D, Jin J, Liu J, Wang Y, Li D, He Y. Baicalein inhibits the progression and promotes radiosensitivity of esophageal squamous cell carcinoma by targeting HIF-1A. Drug Design Devel Ther. 2022;16:2423-2436. doi: 10.2147/dddt.s370114

 

  1. Zeng X, Wan L, Wang Y, Xue J, Yang H, Zhu Y. Effect of low dose of berberine on the radioresistance of cervical cancer cells via a PI3K/HIF-1 pathway under nutrient-deprived conditions. Int J Radiat Biol. 2020;96(8):1060-1067. doi: 10.1080/09553002.2020.1770358

 

  1. Habashy KJ, Mansour R, Moussalem C, Sawaya R, Massaad MJ. Challenges in glioblastoma immunotherapy: Mechanisms of resistance and therapeutic approaches to overcome them. Br J Cancer. 2022;127(6):976-987. doi: 10.1038/s41416-022-01864-w

 

  1. Lequeux A, Noman MZ, Xiao M, et al. Targeting HIF-1 alpha transcriptional activity drives cytotoxic immune effector cells into melanoma and improves combination immunotherapy. Oncogene. 2021;40(28):4725-4735. doi: 10.1038/s41388-021-01846-x

 

  1. Halpin-Veszeleiova K, Hatfield SM. Oxygenation and A2AR blockade to eliminate hypoxia/HIF-1α- adenosinergic immunosuppressive axis and improve cancer immunotherapy. Curr Opin Pharmacol. 2020;53:84-90. doi: 10.1016/j.coph.2020.07.005

 

  1. Nakamura K, Smyth MJ. Targeting cancer‐related inflammation in the era of immunotherapy. Immunol Cell Biol. 2017;95(4):325-332. doi: 10.1038/icb.2016.126

 

  1. You L, Wu W, Wang X, et al. The role of hypoxia‐inducible factor 1 in tumor immune evasion. Med Res Rev. 2020;41(3):1622-1643. doi: 10.1002/med.21771

 

  1. Lin Q, Wang X, Hu Y. The opportunities and challenges in immunotherapy: Insights from the regulation of PD-L1 in cancer cells. Cancer Lett. 2023;569:216318. doi: 10.1016/j.canlet.2023.216318

 

  1. Bailey CM, Liu Y, Liu M, et al. Targeting HIF-1α abrogates PD-L1-mediated immune evasion in tumor microenvironment but promotes tolerance in normal tissues. J Clin Invest. 2022;132(9):e150846. doi: 10.1172/JCI150846

 

  1. Garziera M, Scarabel L, Toffoli G. Hypoxic modulation of HLA-G expression through the metabolic sensor HIF-1 in human cancer cells. J Immunol Res. 2017;2017:4587520. doi: 10.1155/2017/4587520

 

  1. Noman MZ, Hasmim M, Lequeux A, et al. Improving cancer immunotherapy by targeting the hypoxic tumor microenvironment: New opportunities and challenges. Cells. 2019;8(9):1083. doi: 10.3390/cells8091083

 

  1. Wang B, Zhao Q, Zhang Y, et al. Targeting hypoxia in the tumor microenvironment: A potential strategy to improve cancer immunotherapy. J Exp Clin Cancer Res. 2021;40:24. doi: 10.1186/s13046-020-01820-7

 

  1. Food and Drug Administration. FDA Approves First Oral Treatment for Anemia Caused by Chronic Kidney Disease for Adults on Dialysis. Available from: https://www.fda.gov/ news-events/press-announcements/fda-approves-first-oral-treatment-anemia-caused-chronic-kidney-disease-adults-dialysis [Last accessed on 2024 Apr 10].

 

  1. Ishii T, Tanaka T, Nangaku M. Profile of daprodustat in the treatment of renal anemia due to chronic kidney disease. Ther Clin Risk Manag. 2021;17:155-163. doi: 10.2147/tcrm.s293879

 

  1. Dhillon S. Daprodustat: First approval. Drugs. 2020;80(14):1491-1497. doi: 10.1007/s40265-020-01384-y

 

  1. Food and Drug Administration. FDA Approves Belzutifan for Cancers Associated with von Hippel-Lindau Disease. Available from: https://www.fda.gov/drugs/resources-information-approved-drugs/fda-approves-belzutifan-cancers-associated-von-hippel-lindau-disease [Last accessed on 2024 Apr 10].

 

  1. Deeks ED. Belzutifan: First approval. Drugs. 2021;81:1921-1927. doi: 10.1007/s40265-021-01606-x

 

  1. Mortezaee K, Majidpoor J, Kharazinejad E. The impact of hypoxia on tumor-mediated bypassing anti-PD-(L)1 therapy. Biomed Pharmacother. 2023;162:114646. doi: 10.1016/j.biopha.2023.114646

 

  1. Anang V, Singh A, Kottarath SK, Verma C. Receptors of immune cells mediates recognition for tumors. Prog Mol Biol Transl Sci. 2023;194:219-267. doi: 10.1016/bs.pmbts.2022.09.009

 

  1. Kumar V, Patel S, Tcyganov E, Gabrilovich DI. The nature of myeloid-derived suppressor cells in the tumor microenvironment. Trends Immunol. 2016;37(3):208-220. doi: 10.1016/j.it.2016.01.004

 

  1. Benoit A, Vogin G, Duhem C, Berchem G, Janji B. Lighting up the fire in the microenvironment of cold tumors: A major challenge to improve cancer immunotherapy. Cells. 2023;12(13):1787. doi: 10.3390/cells12131787
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