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Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Review Article

Hypoxia A Typical Target in Human Lung Cancer Therapy

Author(s): Asmat Ullah*, Somia Shehzadi, Najeeb Ullah, Touseef Nawaz, Haroon Iqbal and Tariq Aziz*

Volume 25, Issue 5, 2024

Published on: 29 November, 2023

Page: [376 - 385] Pages: 10

DOI: 10.2174/0113892037252820231114045234

Price: $65

Abstract

Lung cancer (LC) is the leading cause of cancer-related death globally. Comprehensive knowledge of the cellular and molecular etiology of LC is perilous for the development of active treatment approaches. Hypoxia in cancer is linked with malignancy, and its phenotype is implicated in the hypoxic reaction, which is being studied as a prospective cancer treatment target. The hypervascularization of the tumor is the main feature of human LC, and hypoxia is a major stimulator of neo-angiogenesis. It was seen that low oxygen levels in human LC are a critical aspect of this lethal illness. However, as there is a considerable body of literature espousing the presumed functional relevance of hypoxia in LC, the direct measurement of oxygen concentration in Human LC is yet to be determined. This narrative review aims to show the importance and as a future target for novel research studies that can lead to the perception of LC therapy in hypoxic malignancies.

Graphical Abstract

[1]
Riaz, S.P.; Lüchtenborg, M.; Coupland, V.H.; Spicer, J.; Peake, M.D.; Møller, H. Trends in incidence of small cell lung cancer and all lung cancer. Lung Cancer, 2012, 75(3), 280-284.
[http://dx.doi.org/10.1016/j.lungcan.2011.08.004] [PMID: 21893364]
[2]
Toschi, L.; Cappuzzo, F.; Jänne, P.A. Evolution and future perspectives in the treatment of locally advanced non-small cell lung cancer. Ann. Oncol., 2007, 18(Suppl. 9), ix150-ix155.
[http://dx.doi.org/10.1093/annonc/mdm311] [PMID: 17631569]
[3]
Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 Countries. CA Cancer J. Clin., 2021, 71(3), 209-249.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[4]
Thun, M.; Peto, R.; Boreham, J.; Lopez, A.D. Stages of the cigarette epidemic on entering its second century. Tob. Control, 2012, 21(2), 96-101.
[http://dx.doi.org/10.1136/tobaccocontrol-2011-050294] [PMID: 22345230]
[5]
Sampsonas, F. State of the art molecular pharmacology, pathogenesis and epigenetics of 3 major cancers: Lung cancer, ovarian cancer, and gliomas. Curr. Mol. Pharmacol., 2021, 14(6), 1003.
[http://dx.doi.org/10.2174/187446721406211220154432] [PMID: 35018882]
[6]
Lung Cancer Incidence and Mortality with Extended Follow-up in the National Lung Screening Trial. J. Thorac. Oncol., 2019, 14(10), 1732-1742.
[http://dx.doi.org/10.1016/j.jtho.2019.05.044] [PMID: 31260833]
[7]
Pastorino, U.; Silva, M.; Sestini, S.; Sabia, F.; Boeri, M.; Cantarutti, A.; Sverzellati, N.; Sozzi, G.; Corrao, G.; Marchianò, A. Prolonged lung cancer screening reduced 10-year mortality in the MILD trial: New confirmation of lung cancer screening efficacy. Ann. Oncol., 2019, 30(7), 1162-1169.
[http://dx.doi.org/10.1093/annonc/mdz117] [PMID: 30937431]
[8]
Novikova, S.E.; Kurbatov, L.K.; Zavialova, M.G.; Zgoda, V.G.; Archakov, A.I. Omics technologies in diagnostics of lung adenocarcinoma. Biomed. Khim., 2017, 63(3), 181-210.
[http://dx.doi.org/10.18097/PBMC20176303181] [PMID: 28781253]
[9]
Reck, M.; Mok, T.S.K.; Nishio, M.; Jotte, R.M.; Cappuzzo, F.; Orlandi, F.; Stroyakovskiy, D.; Nogami, N.; Rodríguez-Abreu, D.; Moro-Sibilot, D.; Thomas, C.A.; Barlesi, F.; Finley, G.; Lee, A.; Coleman, S.; Deng, Y.; Kowanetz, M.; Shankar, G.; Lin, W.; Socinski, M.A.; Reck, M.; Mok, T.S.K.; Nishio, M.; Jotte, R.M.; Cappuzzo, F.; Orlandi, F.; Stroyakovskiy, D.; Nogami, N.; Rodríguez-Abreu, D.; Moro-Sibilot, D.; Thomas, C.A.; Barlesi, F.; Finley, G.; Lee, A.; Coleman, S.; Deng, Y.; Kowanetz, M.; Shankar, G.; Lin, W.; Socinski, M.A. Atezolizumab plus bevacizumab and chemotherapy in non-small-cell lung cancer (IMpower150): Key subgroup analyses of patients with EGFR mutations or baseline liver metastases in a randomised, open-label phase 3 trial. Lancet Respir. Med., 2019, 7(5), 387-401.
[http://dx.doi.org/10.1016/S2213-2600(19)30084-0] [PMID: 30922878]
[10]
Carvalho, S.; Troost, E.G.C.; Bons, J.; Menheere, P.; Lambin, P.; Oberije, C. Prognostic value of blood-biomarkers related to hypoxia, inflammation, immune response and tumour load in non-small cell lung cancer – A survival model with external validation. Radiother. Oncol., 2016, 119(3), 487-494.
[http://dx.doi.org/10.1016/j.radonc.2016.04.024] [PMID: 27139126]
[11]
Wang, Y.; Yang, J.; Liu, H.; Bi, J.R.; Liu, Y.; Chen, Y.Y.; Cao, J.Y.; Lu, Y.J. The association between osteopontin and survival in non-small-cell lung cancer patients: a meta-analysis of 13 cohorts. OncoTargets Ther., 2015, 8, 3513-3521.
[PMID: 26648743]
[12]
Ullah, A.; Leong, S.W.; Wang, J.; Wu, Q.; Ghauri, M.A.; Sarwar, A.; Su, Q.; Zhang, Y. Cephalomannine inhibits hypoxia-induced cellular function via the suppression of APEX1/HIF-1α interaction in lung cancer. Cell Death Dis., 2021, 12(5), 490.
[http://dx.doi.org/10.1038/s41419-021-03771-z] [PMID: 33990544]
[13]
İlie, M.; Mazure, N.M.; Hofman, V.; Ammadi, R.E.; Ortholan, C.; Bonnetaud, C.; Havet, K.; Venissac, N.; Mograbi, B.; Mouroux, J.; Pouysségur, J.; Hofman, P. High levels of carbonic anhydrase IX in tumour tissue and plasma are biomarkers of poor prognostic in patients with non-small cell lung cancer. Br. J. Cancer, 2010, 102(11), 1627-1635.
[http://dx.doi.org/10.1038/sj.bjc.6605690] [PMID: 20461082]
[14]
Lim, A.M.; Rischin, D.; Fisher, R.; Cao, H.; Kwok, K.; Truong, D.; McArthur, G.A.; Young, R.J.; Giaccia, A.; Peters, L.; Le, Q.T. Prognostic significance of plasma osteopontin in patients with locoregionally advanced head and neck squamous cell carcinoma treated on TROG 02.02 phase III trial. Clin. Cancer Res., 2012, 18(1), 301-307.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-2295] [PMID: 22096023]
[15]
Overgaard, J.; Eriksen, J.G.; Nordsmark, M.; Alsner, J.; Horsman, M.R. Plasma osteopontin, hypoxia, and response to the hypoxia sensitiser nimorazole in radiotherapy of head and neck cancer: results from the DAHANCA 5 randomised double-blind placebo- controlled trial. Lancet Oncol., 2005, 6(10), 757-764.
[http://dx.doi.org/10.1016/S1470-2045(05)70292-8] [PMID: 16198981]
[16]
Kulshreshtha, R.; Ferracin, M.; Wojcik, S.E.; Garzon, R.; Alder, H.; Agosto-Perez, F.J.; Davuluri, R.; Liu, C.G.; Croce, C.M.; Negrini, M.; Calin, G.A.; Ivan, M. A microRNA signature of hypoxia. Mol. Cell. Biol., 2007, 27(5), 1859-1867.
[http://dx.doi.org/10.1128/MCB.01395-06] [PMID: 17194750]
[17]
Grosso, S.; Doyen, J.; Parks, S.K.; Bertero, T.; Paye, A.; Cardinaud, B.; Gounon, P.; Lacas-Gervais, S.; Noël, A.; Pouysségur, J.; Barbry, P.; Mazure, N.M.; Mari, B. MiR-210 promotes a hypoxic phenotype and increases radioresistance in human lung cancer cell lines. Cell Death Dis., 2013, 4(3), e544.
[http://dx.doi.org/10.1038/cddis.2013.71] [PMID: 23492775]
[18]
Eilertsen, M.; Andersen, S.; Al-Saad, S.; Richardsen, E.; Stenvold, H.; Hald, S.M.; Al-Shibli, K.; Donnem, T.; Busund, L.T.; Bremnes, R.M. Positive prognostic impact of miR-210 in non-small cell lung cancer. Lung Cancer, 2014, 83(2), 272-278.
[http://dx.doi.org/10.1016/j.lungcan.2013.11.005] [PMID: 24305009]
[19]
Osugi, J.; Kimura, Y.; Owada, Y.; Inoue, T.; Watanabe, Y.; Yamaura, T.; Fukuhara, M.; Muto, S.; Okabe, N.; Matsumura, Y.; Hasegawa, T.; Yonechi, A.; Hoshino, M.; Higuchi, M.; Shio, Y.; Suzuki, H.; Gotoh, M. Prognostic impact of hypoxia-inducible miRNA-210 in patients with lung adenocarcinoma. J. Oncol., 2015, 2015, 1-8.
[http://dx.doi.org/10.1155/2015/316745] [PMID: 25733977]
[20]
Li, Z.H.; Zhang, H.; Yang, Z.G.; Wen, G.Q.; Cui, Y.B.; Shao, G.G. Prognostic significance of serum microRNA-210 levels in nonsmall-cell lung cancer. J. Int. Med. Res., 2013, 41(5), 1437-1444.
[http://dx.doi.org/10.1177/0300060513497560] [PMID: 24065453]
[21]
Ono, S.; Lam, S.; Nagahara, M.; Hoon, D. Circulating microRNA biomarkers as liquid biopsy for cancer patients: Pros and cons of current assays. J. Clin. Med., 2015, 4(10), 1890-1907.
[http://dx.doi.org/10.3390/jcm4101890] [PMID: 26512704]
[22]
Bao, Y.; Deng, L.; Su, D.; Xiao, J.; Ge, D.; Geng, Y.; Jing, H. Identification of crucial microRNAs and genes in hypoxia-induced human lung adenocarcinoma cells. Onco. Targets Ther., 2016, 9, 4605-4616.
[http://dx.doi.org/10.2147/OTT.S103430] [PMID: 27524914]
[23]
Vaupel, P.; Flood, A.B.; Swartz, H.M. Oxygenation status of malignant tumors vs. Normal tissues: Critical evaluation and updated data source based on direct measurements with po2 microsensors. Appl. Magn. Reson., 2021, 52(10), 1451-1479.
[http://dx.doi.org/10.1007/s00723-021-01383-6]
[24]
Höckel, M.; Vaupel, P. Tumor hypoxia: Definitions and current clinical, biologic, and molecular aspects. J. Natl. Cancer Inst., 2001, 93(4), 266-276.
[http://dx.doi.org/10.1093/jnci/93.4.266] [PMID: 11181773]
[25]
D’Alonzo, R.A.; Gill, S.; Rowshanfarzad, P.; Keam, S.; MacKinnon, K.M.; Cook, A.M.; Ebert, M.A. In vivo noninvasive preclinical tumor hypoxia imaging methods: A review. Int. J. Radiat. Biol., 2021, 97(5), 593-631.
[http://dx.doi.org/10.1080/09553002.2021.1900943] [PMID: 33703994]
[26]
Vaupel, P.; Schlenger, K.; Knoop, C.; Höckel, M. Oxygenation of human tumors: Evaluation of tissue oxygen distribution in breast cancers by computerized O2 tension measurements. Cancer Res., 1991, 51(12), 3316-3322.
[PMID: 2040005]
[27]
Su, Q.; Wang, J.; Fan, M.; Ghauri, M.A.; Ullah, A.; Wang, B.; Dai, B.; Zhan, Y.; Zhang, D.; Zhang, Y. Sanguinarine disrupts the colocalization and interaction of HIF-1α with tyrosine and serine phosphorylated-STAT3 in breast cancer. J. Cell. Mol. Med., 2020, 24(6), 3756-3761.
[http://dx.doi.org/10.1111/jcmm.15056] [PMID: 32065498]
[28]
Ziółkowska-Suchanek, I. Mimicking tumor hypoxia in non-small cell lung cancer employing three-dimensional in vitro models. Cells, 2021, 10(1), 141.
[http://dx.doi.org/10.3390/cells10010141] [PMID: 33445709]
[29]
Vaupel, P.; Höckel, M.; Mayer, A. Detection and characterization of tumor hypoxia using pO2 histography. Antioxid. Redox Signal., 2007, 9(8), 1221-1236.
[http://dx.doi.org/10.1089/ars.2007.1628] [PMID: 17536958]
[30]
Emami Nejad, A.; Najafgholian, S.; Rostami, A.; Sistani, A.; Shojaeifar, S.; Esparvarinha, M.; Nedaeinia, R.; Haghjooy Javanmard, S.; Taherian, M.; Ahmadlou, M.; Salehi, R.; Sadeghi, B.; Manian, M. The role of hypoxia in the tumor microenvironment and development of cancer stem cell: A novel approach to developing treatment. Cancer Cell Int., 2021, 21(1), 62.
[http://dx.doi.org/10.1186/s12935-020-01719-5] [PMID: 33472628]
[31]
De Mello, R.A.; Luis, M.; Araújo, A.; Reis, R.M.; Hespanhol, V. The role of angiogenesis in non-small cell lung cancer tumor behavior. In: Biochemical Basis and Therapeutic Implications of Angiogenesis; Mehta, J.L.; Mathur, P.; Dhalla, N.S., Eds.; Springer International Publishing: Cham, 2017; pp. 217-239.
[http://dx.doi.org/10.1007/978-3-319-61115-0_10]
[32]
Powers, K.A.; Dhamoon, A.S. Physiology, pulmonary ventilation and perfusion. In: StatPearls; StatPearls Publishing Copyright © 2022, StatPearls Publishing LLC.,: Treasure Island (FL), 2022.
[33]
Jiang, G.M.; Zhao, J.W.; Chen, Y.X.; Tian, F. Blood supply of pulmonary metastases and its clinical significance. Chin. J. Cancer, 2006, 25(7), 885-887.
[PMID: 16831283]
[34]
Jamil, A.; Kasi, A. Lung Metastasis. In: StatPearls; StatPearls Publishing Copyright © 2022, StatPearls Publishing LLC: Treasure Island (FL), 2022.
[35]
Bobba, R.K.; Holly, J.S.; Loy, T.; Perry, M.C. Scar carcinoma of the lung: A historical perspective. Clin. Lung Cancer, 2011, 12(3), 148-154.
[http://dx.doi.org/10.1016/j.cllc.2011.03.011] [PMID: 21663856]
[36]
Ortiz-Prado, E.; Dunn, J.F.; Vasconez, J.; Castillo, D.; Viscor, G. Partial pressure of oxygen in the human body: A general review. Am. J. Blood Res., 2019, 9(1), 1-14.
[PMID: 30899601]
[37]
Semenza, G.L. The hypoxic tumor microenvironment: A driving force for breast cancer progression. Biochim. Biophys. Acta Mol. Cell Res., 2016, 1863(3), 382-391.
[http://dx.doi.org/10.1016/j.bbamcr.2015.05.036] [PMID: 26079100]
[38]
Harris, A.L. Hypoxia-a key regulatory factor in tumour growth. Nat. Rev. Cancer, 2002, 2(1), 38-47.
[http://dx.doi.org/10.1038/nrc704] [PMID: 11902584]
[39]
Ancel, J.; Perotin, J.M.; Dewolf, M.; Launois, C.; Mulette, P.; Nawrocki-Raby, B.; Dalstein, V.; Gilles, C.; Deslée, G.; Polette, M.; Dormoy, V. Hypoxia in lung cancer management: A translational approach. Cancers, 2021, 13(14), 3421.
[http://dx.doi.org/10.3390/cancers13143421] [PMID: 34298636]
[40]
Satija, S.; Kaur, H.; Tambuwala, M.M.; Sharma, P.; Vyas, M.; Khurana, N.; Sharma, N.; Bakshi, H.A.; Charbe, N.B.; Zacconi, F.C.; Aljabali, A.A.; Nammi, S.; Dureja, H.; Singh, T.G.; Gupta, G.; Dhanjal, D.S.; Dua, K.; Chellappan, D.K.; Mehta, M. Hypoxia-inducible factor (HIF): Fuel for cancer progression. Curr. Mol. Pharmacol., 2021, 14(3), 321-332.
[http://dx.doi.org/10.2174/1874467214666210120154929] [PMID: 33494692]
[41]
Wang, G.L.; Jiang, B.H.; Rue, E.A.; Semenza, G.L. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA, 1995, 92(12), 5510-5514.
[http://dx.doi.org/10.1073/pnas.92.12.5510] [PMID: 7539918]
[42]
Baqlouq, L.; Zihlif, M.; Hammad, H.; Thaib, T.M.A. Determining the relative gene expression level of hypoxia related genes in different cancer cell lines. Curr. Mol. Pharmacol., 2020, 14(1), 52-59.
[http://dx.doi.org/10.2174/1874467213666200521081653] [PMID: 32436837]
[43]
Mayer, A.; Höckel, M.; Wree, A.; Vaupel, P. Microregional expression of glucose transporter-1 and oxygenation status: Lack of correlation in locally advanced cervical cancers. Clin. Cancer Res., 2005, 11(7), 2768-2773.
[http://dx.doi.org/10.1158/1078-0432.CCR-04-2344] [PMID: 15814659]
[44]
Su, Q.; Fan, M.; Wang, J.; Ullah, A.; Ghauri, M.A.; Dai, B.; Zhan, Y.; Zhang, D.; Zhang, Y. Sanguinarine inhibits epithelial–mesenchymal transition via targeting HIF-1α/TGF-β feed-forward loop in hepatocellular carcinoma. Cell Death Dis., 2019, 10(12), 939.
[http://dx.doi.org/10.1038/s41419-019-2173-1] [PMID: 31819036]
[45]
Mayer, A.; Wree, A.; Höckel, M.; Leo, C.; Pilch, H.; Vaupel, P. Lack of correlation between expression of HIF-1alpha protein and oxygenation status in identical tissue areas of squamous cell carcinomas of the uterine cervix. Cancer Res., 2004, 64(16), 5876-5881.
[http://dx.doi.org/10.1158/0008-5472.CAN-03-3566] [PMID: 15313932]
[46]
Mayer, A.; Höckel, M.; Wree, A.; Leo, C.; Horn, L.C.; Vaupel, P. Lack of hypoxic response in uterine leiomyomas despite severe tissue hypoxia. Cancer Res., 2008, 68(12), 4719-4726.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-6339] [PMID: 18559518]
[47]
Ren, W.; Mi, D.; Yang, K.; Cao, N.; Tian, J.; Li, Z.; Ma, B. The expression of hypoxia-inducible factor-1α and its clinical significance in lung cancer: A systematic review and meta-analysis. Swiss Med. Wkly., 2013, 143, w13855.
[http://dx.doi.org/10.4414/smw.2013.13855] [PMID: 24018850]
[48]
Wilson, W.R.; Hay, M.P. Targeting hypoxia in cancer therapy. Nat. Rev. Cancer, 2011, 11(6), 393-410.
[http://dx.doi.org/10.1038/nrc3064] [PMID: 21606941]
[49]
Wardman, P. Chemical radiosensitizers for use in radiotherapy. In: Clinical oncology (Royal College of Radiologists); (Great Britain), 2007; 19, pp. (6)497-417.
[http://dx.doi.org/10.1016/j.clon.2007.03.010]
[50]
Peters, L.; Rischin, D. Elusive goal of targeting tumor hypoxia for therapeutic gain. J. Clin. Oncol., 2012, 30(15), 1741-1743.
[http://dx.doi.org/10.1200/JCO.2011.40.8294] [PMID: 22508811]
[51]
Li, L.; Hu, M.; Zhu, H.; Zhao, W.; Yang, G.; Yu, J. Comparison of 18F-Fluoroerythronitroimidazole and 18F-fluorodeoxyglucose positron emission tomography and prognostic value in locally advanced non-small-cell lung cancer. Clin. Lung Cancer, 2010, 11(5), 335-340.
[http://dx.doi.org/10.3816/CLC.2010.n.042] [PMID: 20837459]
[52]
Trinkaus, M.E.; Blum, R.; Rischin, D.; Callahan, J.; Bressel, M.; Segard, T.; Roselt, P.; Eu, P.; Binns, D.; MacManus, M.P.; Ball, D.; Hicks, R.J. Imaging of hypoxia with 18 F-FAZA PET in patients with locally advanced non-small cell lung cancer treated with definitive chemoradiotherapy. J. Med. Imaging Radiat. Oncol., 2013, 57(4), 475-481.
[http://dx.doi.org/10.1111/1754-9485.12086] [PMID: 23870348]
[53]
van Elmpt, W.; Zegers, C.M.L.; Reymen, B.; Even, A.J.G.; Dingemans, A.M.C.; Oellers, M.; Wildberger, J.E.; Mottaghy, F.M.; Das, M.; Troost, E.G.C.; Lambin, P. Multiparametric imaging of patient and tumour heterogeneity in non-small-cell lung cancer: quantification of tumour hypoxia, metabolism and perfusion. Eur. J. Nucl. Med. Mol. Imaging, 2016, 43(2), 240-248.
[http://dx.doi.org/10.1007/s00259-015-3169-4] [PMID: 26338178]
[54]
Tirpe, A.A.; Gulei, D.; Ciortea, S.M.; Crivii, C.; Berindan-Neagoe, I. Hypoxia: Overview on hypoxia-mediated mechanisms with a focus on the role of HIF genes. Int. J. Mol. Sci., 2019, 20(24), 6140.
[http://dx.doi.org/10.3390/ijms20246140] [PMID: 31817513]
[55]
Duan, C. Hypoxia-inducible factor 3 biology: Complexities and emerging themes. Am. J. Physiol. Cell Physiol., 2016, 310(4), C260-C269.
[http://dx.doi.org/10.1152/ajpcell.00315.2015] [PMID: 26561641]
[56]
Liao, C.; Zhang, Q. Understanding the oxygen-sensing pathway and its therapeutic implications in diseases. Am. J. Pathol., 2020, 190(8), 1584-1595.
[http://dx.doi.org/10.1016/j.ajpath.2020.04.003] [PMID: 32339495]
[57]
Joshi, S.; Singh, A.R.; Durden, D.L. MDM2 regulates hypoxic hypoxia-inducible factor 1α stability in an E3 ligase, proteasome, and PTEN-phosphatidylinositol 3-kinase-AKT-dependent manner. J. Biol. Chem., 2014, 289(33), 22785-22797.
[http://dx.doi.org/10.1074/jbc.M114.587493] [PMID: 24982421]
[58]
Pore, N.; Jiang, Z.; Shu, H.K.; Bernhard, E.; Kao, G.D.; Maity, A. Akt1 activation can augment hypoxia-inducible factor-1alpha expression by increasing protein translation through a mammalian target of rapamycin-independent pathway. Mol. Cancer Res., 2006, 4(7), 471-479.
[http://dx.doi.org/10.1158/1541-7786.MCR-05-0234] [PMID: 16849522]
[59]
Cao, Y.; Eble, J.M.; Moon, E.; Yuan, H.; Weitzel, D.H.; Landon, C.D.; Yu-Chih Nien, C.; Hanna, G.; Rich, J.N.; Provenzale, J.M.; Dewhirst, M.W. Tumor cells upregulate normoxic HIF-1α in response to doxorubicin. Cancer Res., 2013, 73(20), 6230-6242.
[http://dx.doi.org/10.1158/0008-5472.CAN-12-1345] [PMID: 23959856]
[60]
Moniz, S.; Bandarra, D.; Biddlestone, J.; Campbell, K.J.; Komander, D.; Bremm, A.; Rocha, S. Cezanne regulates E2F1-dependent HIF2α expression. J. Cell Sci., 2015, 128(16), 3082-3093.
[PMID: 26148512]
[61]
Son, S.W.; Yun, B.D.; Song, M.G.; Lee, J.K.; Choi, S.Y.; Kuh, H.J.; Park, J.K. The hypoxia–long noncoding rna interaction in solid cancers. Int. J. Mol. Sci., 2021, 22(14), 7261.
[http://dx.doi.org/10.3390/ijms22147261] [PMID: 34298879]
[62]
Poon, E.; Harris, A.L.; Ashcroft, M. Targeting the hypoxia-inducible factor (HIF) pathway in cancer. Expert Rev. Mol. Med., 2009, 11, e26.
[http://dx.doi.org/10.1017/S1462399409001173] [PMID: 19709449]
[63]
Bertout, J.A.; Majmundar, A.J.; Gordan, J.D.; Lam, J.C.; Ditsworth, D.; Keith, B.; Brown, E.J.; Nathanson, K.L.; Simon, M.C. HIF2α inhibition promotes p53 pathway activity, tumor cell death, and radiation responses. Proc. Natl. Acad. Sci. USA, 2009, 106(34), 14391-14396.
[http://dx.doi.org/10.1073/pnas.0907357106] [PMID: 19706526]
[64]
Nardinocchi, L.; Puca, R.; D’Orazi, G. HIF-1α antagonizes p53- mediated apoptosis by triggering HIPK2 degradation. Aging (Albany NY), 2011, 3(1), 33-43.
[http://dx.doi.org/10.18632/aging.100254] [PMID: 21248371]
[65]
Wang, X.; Dong, J.; Jia, L.; Zhao, T.; Lang, M.; Li, Z.; Lan, C.; Li, X.; Hao, J.; Wang, H.; Qin, T.; Huang, C.; Yang, S.; Yu, M.; Ren, H. HIF-2-dependent expression of stem cell factor promotes metastasis in hepatocellular carcinoma. Cancer Lett., 2017, 393, 113-124.
[http://dx.doi.org/10.1016/j.canlet.2017.01.032] [PMID: 28153790]
[66]
Zhang, L.; Huang, G.; Li, X.; Zhang, Y.; Jiang, Y.; Shen, J.; Liu, J.; Wang, Q.; Zhu, J.; Feng, X.; Dong, J.; Qian, C. Hypoxia induces epithelial-mesenchymal transition via activation of SNAI1 by hypoxia-inducible factor -1α in hepatocellular carcinoma. BMC Cancer, 2013, 13(1), 108.
[http://dx.doi.org/10.1186/1471-2407-13-108] [PMID: 23496980]
[67]
Choueiri, T.K.; Kaelin, W.G., Jr Targeting the HIF2–VEGF axis in renal cell carcinoma. Nat. Med., 2020, 26(10), 1519-1530.
[http://dx.doi.org/10.1038/s41591-020-1093-z] [PMID: 33020645]
[68]
Ravi, R.; Mookerjee, B.; Bhujwalla, Z.M.; Sutter, C.H.; Artemov, D.; Zeng, Q.; Dillehay, L.E.; Madan, A.; Semenza, G.L.; Bedi, A. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1α. Genes Dev., 2000, 14(1), 34-44.
[http://dx.doi.org/10.1101/gad.14.1.34] [PMID: 10640274]
[69]
Meijer, T.W.H.; Kaanders, J.H.A.M.; Span, P.N.; Bussink, J. Targeting hypoxia, HIF-1, and tumor glucose metabolism to improve radiotherapy efficacy. Clin. Cancer Res., 2012, 18(20), 5585-5594.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-0858] [PMID: 23071360]
[70]
Samanta, D.; Gilkes, D.M.; Chaturvedi, P.; Xiang, L.; Semenza, G.L. Hypoxia-inducible factors are required for chemotherapy resistance of breast cancer stem cells. Proc. Natl. Acad. Sci. USA, 2014, 111(50), E5429-E5438.
[http://dx.doi.org/10.1073/pnas.1421438111] [PMID: 25453096]
[71]
Noman, M.Z.; Desantis, G.; Janji, B.; Hasmim, M.; Karray, S.; Dessen, P.; Bronte, V.; Chouaib, S. PD-L1 is a novel direct target of HIF-1α, and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J. Exp. Med., 2014, 211(5), 781-790.
[http://dx.doi.org/10.1084/jem.20131916] [PMID: 24778419]
[72]
Imtiyaz, H.Z.; Williams, E.P.; Hickey, M.M.; Patel, S.A.; Durham, A.C.; Yuan, L.J.; Hammond, R.; Gimotty, P.A.; Keith, B.; Simon, M.C. Hypoxia-inducible factor 2α regulates macrophage function in mouse models of acute and tumor inflammation. J. Clin. Invest., 2010, 120(8), 2699-2714.
[http://dx.doi.org/10.1172/JCI39506] [PMID: 20644254]
[73]
Talks, K.L.; Turley, H.; Gatter, K.C.; Maxwell, P.H.; Pugh, C.W.; Ratcliffe, P.J.; Harris, A.L. 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(2), 411-421.
[http://dx.doi.org/10.1016/S0002-9440(10)64554-3] [PMID: 10934146]
[74]
Liu, Y.M.; Ying, S.P.; Huang, Y.R.; Pan, Y.; Chen, W.J.; Ni, L.Q.; Xu, J.Y.; Shen, Q.Y.; Liang, Y. Expression of HIF-1α and HIF-2α correlates to biological and clinical significance in papillary thyroid carcinoma. World J. Surg. Oncol., 2015, 14(1), 30.
[http://dx.doi.org/10.1186/s12957-016-0785-9] [PMID: 26846782]
[75]
Zhang, L.; Chen, Q.; Hu, J.; Chen, Y.; Liu, C.; Xu, C. Expression of HIF-2α and VEGF in cervical squamous cell carcinoma and its clinical significance. BioMed Res. Int., 2016, 2016, 5631935.
[PMID: 27413748]
[76]
Moreno Roig, E.; Groot, A.; Yaromina, A.; Hendrickx, T.; Barbeau, L.; Giuranno, L.; Dams, G.; Ient, J.; Olivo Pimentel, V.; van Gisbergen, M.; Dubois, L.; Vooijs, M. HIF-1α and HIF-2α differently regulate the radiation sensitivity of NSCLC cells. Cells, 2019, 8(1), 45.
[http://dx.doi.org/10.3390/cells8010045] [PMID: 30642030]
[77]
Isono, T.; Chano, T.; Yoshida, T.; Kageyama, S.; Kawauchi, A.; Suzaki, M.; Yuasa, T. Hydroxyl-HIF2-alpha is potential therapeutic target for renal cell carcinomas. Am. J. Cancer Res., 2016, 6(10), 2263-2276.
[PMID: 27822416]
[78]
Downes, NL; Laham-Karam, N; Kaikkonen, MU; Ylä-Herttuala, S. Differential but Complementary HIF1α and HIF2α transcriptional regulation. J. Am. Soc. Gene. Ther., 2018, 26(7), 1735-1745.
[http://dx.doi.org/10.1016/j.ymthe.2018.05.004]
[79]
Loboda, A.; Jozkowicz, A.; Dulak, J. HIF-1 and HIF-2 transcription factors — Similar but not identical. Mol. Cells, 2010, 29(5), 435-442.
[http://dx.doi.org/10.1007/s10059-010-0067-2] [PMID: 20396958]
[80]
Hoefflin, R.; Harlander, S.; Schäfer, S.; Metzger, P.; Kuo, F.; Schönenberger, D.; Adlesic, M.; Peighambari, A.; Seidel, P.; Chen, C.; Consenza-Contreras, M.; Jud, A.; Lahrmann, B.; Grabe, N.; Heide, D.; Uhl, F.M.; Chan, T.A.; Duyster, J.; Zeiser, R.; Schell, C.; Heikenwalder, M.; Schilling, O.; Hakimi, A.A.; Boerries, M.; Frew, I.J. HIF-1α and HIF-2α differently regulate tumour development and inflammation of clear cell renal cell carcinoma in mice. Nat. Commun., 2020, 11(1), 4111.
[http://dx.doi.org/10.1038/s41467-020-17873-3] [PMID: 32807776]
[81]
Bertout, J.A.; Patel, S.A.; Simon, M.C. The impact of O2 availability on human cancer. Nat. Rev. Cancer, 2008, 8(12), 967-975.
[http://dx.doi.org/10.1038/nrc2540] [PMID: 18987634]
[82]
Brustugun, O.T. Hypoxia as a cause of treatment failure in non-small cell carcinoma of the lung. Semin. Radiat. Oncol., 2015, 25(2), 87-92.
[http://dx.doi.org/10.1016/j.semradonc.2014.11.006] [PMID: 25771412]
[83]
Dewhirst, M.W.; Birer, S.R. Oxygen-enhanced MRI is a major advance in tumor hypoxia imaging. Cancer Res., 2016, 76(4), 769-772.
[http://dx.doi.org/10.1158/0008-5472.CAN-15-2818] [PMID: 26837768]
[84]
Sharma, R.A.; Plummer, R.; Stock, J.K.; Greenhalgh, T.A.; Ataman, O.; Kelly, S.; Clay, R.; Adams, R.A.; Baird, R.D.; Billingham, L.; Brown, S.R.; Buckland, S.; Bulbeck, H.; Chalmers, A.J.; Clack, G.; Cranston, A.N.; Damstrup, L.; Ferraldeschi, R.; Forster, M.D.; Golec, J.; Hagan, R.M.; Hall, E.; Hanauske, A.R.; Harrington, K.J.; Haswell, T.; Hawkins, M.A.; Illidge, T.; Jones, H.; Kennedy, A.S.; McDonald, F.; Melcher, T.; O’Connor, J.P.B.; Pollard, J.R.; Saunders, M.P.; Sebag-Montefiore, D.; Smitt, M.; Staffurth, J.; Stratford, I.J.; Wedge, S.R. Clinical development of new drug–radiotherapy combinations. Nat. Rev. Clin. Oncol., 2016, 13(10), 627-642.
[http://dx.doi.org/10.1038/nrclinonc.2016.79] [PMID: 27245279]
[85]
Salem, A.; Asselin, M.C.; Reymen, B.; Jackson, A.; Lambin, P.; West, C.M.L.; O’Connor, J.P.B.; Faivre-Finn, C. Targeting hypoxia to improve non–small cell lung cancer outcome. J. Natl. Cancer Inst., 2018, 110(1), 14-30.
[http://dx.doi.org/10.1093/jnci/djx160] [PMID: 28922791]
[86]
Son, S.W.; Lee, H.Y.; Moeng, S.; Kuh, H.J.; Choi, S.Y.; Park, J.K. Participation of MicroRNAs in the treatment of cancer with phytochemicals. Molecules, 2020, 25(20), 4701.
[http://dx.doi.org/10.3390/molecules25204701] [PMID: 33066509]
[87]
Montané, X.; Kowalczyk, O.; Reig-Vano, B.; Bajek, A.; Roszkowski, K.; Tomczyk, R.; Pawliszak, W.; Giamberini, M.; Mocek-Płóciniak, A.; Tylkowski, B. Current perspectives of the applications of polyphenols and flavonoids in cancer therapy. Molecules, 2020, 25(15), 3342.
[http://dx.doi.org/10.3390/molecules25153342] [PMID: 32717865]
[88]
Mitra, T.; Bhattacharya, R. Phytochemicals modulate cancer aggressiveness: A review depicting the anticancer efficacy of dietary polyphenols and their combinations. J. Cell. Physiol., 2020, 235(11), 7696-7708.
[http://dx.doi.org/10.1002/jcp.29703] [PMID: 32324275]
[89]
Wheelock, C.E.; Goss, V.M.; Balgoma, D.; Nicholas, B.; Brandsma, J.; Skipp, P.J.; Snowden, S.; Burg, D.; D’Amico, A.; Horvath, I.; Chaiboonchoe, A.; Ahmed, H.; Ballereau, S.; Rossios, C.; Chung, K.F.; Montuschi, P.; Fowler, S.J.; Adcock, I.M.; Postle, A.D.; Dahlén, S.E.; Rowe, A.; Sterk, P.J.; Auffray, C.; Djukanović, R. Application of ’omics technologies to biomarker discovery in inflammatory lung diseases. Eur. Respir. J., 2013, 42(3), 802-825.
[http://dx.doi.org/10.1183/09031936.00078812] [PMID: 23397306]
[90]
Rong, Z.H.U.; Lingyun, D.A.I.; Jinxing, L.I.U.; Ying, G.U.O. Diagnostic classification of lung cancer using deep transfer learning technology and multi-omics data. Chin. J. Electron., 2021, 30(5), 843-852.
[http://dx.doi.org/10.1049/cje.2021.06.006]
[91]
Altorki, N.K.; Markowitz, G.J.; Gao, D.; Port, J.L.; Saxena, A.; Stiles, B.; McGraw, T.; Mittal, V. The lung microenvironment: An important regulator of tumour growth and metastasis. Nat. Rev. Cancer, 2019, 19(1), 9-31.
[http://dx.doi.org/10.1038/s41568-018-0081-9] [PMID: 30532012]
[92]
Schito, L.; Semenza, G.L. Hypoxia-inducible factors: Master regulators of cancer progression. Trends Cancer, 2016, 2(12), 758-770.
[http://dx.doi.org/10.1016/j.trecan.2016.10.016] [PMID: 28741521]
[93]
Iommarini, L.; Porcelli, A.M.; Gasparre, G.; Kurelac, I. Non-canonical mechanisms regulating hypoxia-inducible factor 1 alpha in cancer. Front. Oncol., 2017, 7, 286.
[http://dx.doi.org/10.3389/fonc.2017.00286] [PMID: 29230384]
[94]
LaGory, E.L.; Giaccia, A.J. The ever-expanding role of HIF in tumour and stromal biology. Nat. Cell Biol., 2016, 18(4), 356-365.
[http://dx.doi.org/10.1038/ncb3330] [PMID: 27027486]
[95]
Walsh, J.C.; Lebedev, A.; Aten, E.; Madsen, K.; Marciano, L.; Kolb, H.C. The clinical importance of assessing tumor hypoxia: relationship of tumor hypoxia to prognosis and therapeutic opportunities. Antioxid. Redox Signal., 2014, 21(10), 1516-1554.
[http://dx.doi.org/10.1089/ars.2013.5378] [PMID: 24512032]
[96]
Robinson, M.F.; Dupuis, N.P.; Kusumoto, T.; Liu, F.; Menon, K.; Teicher, B.A. Increased tumor oxygenation and radiation sensitivity in two rat tumors by a hemoglobin-based, oxygen-carrying preparation. Artif. Cells Blood Substit. Immobil. Biotechnol., 1995, 23(3), 431-438.
[http://dx.doi.org/10.3109/10731199509117959] [PMID: 7493064]
[97]
Sun, C.J.; Li, C.; Lv, H.B.; Zhao, C.; Yu, J.M.; Wang, G.H.; Luo, Y.X.; Li, Y.; Xiao, M.; Yin, J.; Lang, J.Y. Comparing CT perfusion with oxygen partial pressure in a rabbit VX2 soft-tissue tumor model. J. Radiat. Res. (Tokyo), 2014, 55(1), 183-190.
[http://dx.doi.org/10.1093/jrr/rrt092] [PMID: 24078878]
[98]
Doss, M.; Zhang, J.J.; Bélanger, M.J.; Stubbs, J.B.; Hostetler, E.D.; Alpaugh, K.; Kolb, H.C.; Yu, J.Q. Biodistribution and radiation dosimetry of the hypoxia marker 18F–HX4 in monkeys and humans determined by using whole-body PET/CT. Nucl. Med. Commun., 2010, 31(12), 1016-1024.
[http://dx.doi.org/10.1097/MNM.0b013e3283407950] [PMID: 20948452]
[99]
Logothetis, N.K. The underpinnings of the BOLD functional magnetic resonance imaging signal. J. Neurosci., 2003, 23(10), 3963-3971.
[http://dx.doi.org/10.1523/JNEUROSCI.23-10-03963.2003] [PMID: 12764080]
[100]
Daponte, A.; Ioannou, M.; Mylonis, I.; Simos, G.; Minas, M.; Messinis, I.E.; Koukoulis, G. Prognostic significance of Hypoxia-Inducible Factor 1 alpha(HIF-1alpha) expression in serous ovarian cancer: An immunohistochemical study. BMC Cancer, 2008, 8(1), 335.
[http://dx.doi.org/10.1186/1471-2407-8-335] [PMID: 19014607]
[101]
Nordsmark, M.; Loncaster, J.; Aquino-Parsons, C.; Chou, S.C.; Gebski, V.; West, C.; Lindegaard, J.C.; Havsteen, H.; Davidson, S.E.; Hunter, R.; Raleigh, J.A.; Overgaard, J. The prognostic value of pimonidazole and tumour pO2 in human cervix carcinomas after radiation therapy: A prospective international multi-center study. Radiother. Oncol., 2006, 80(2), 123-131.
[http://dx.doi.org/10.1016/j.radonc.2006.07.010] [PMID: 16890316]
[102]
Dunwoodie, S.L. The role of hypoxia in development of the Mammalian embryo. Dev. Cell, 2009, 17(6), 755-773.
[http://dx.doi.org/10.1016/j.devcel.2009.11.008] [PMID: 20059947]
[103]
DiGiacomo, J.W.; Gilkes, D.M. Tumor hypoxia as an enhancer of inflammation-mediated metastasis: Emerging therapeutic strategies. Target. Oncol., 2018, 13(2), 157-173.
[http://dx.doi.org/10.1007/s11523-018-0555-4] [PMID: 29423593]
[104]
DiGiacomo, J.W.; Gilkes, D.M. Therapeutic strategies to block the hypoxic response. Adv. Exp. Med. Biol., 2019, 1136, 141-157.
[http://dx.doi.org/10.1007/978-3-030-12734-3_10] [PMID: 31201722]

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