HIFs, angiogenesis, and metabolism: Elusive enemies in breast cancer
Open accessAbstract
Hypoxia-inducible factors (HIFs) and the HIF-dependent cancer hallmarks angiogenesis and metabolic rewiring are well-established drivers of breast cancer aggressiveness, therapy resistance, and poor prognosis. Targeting of HIF and its downstream targets in angiogenesis and metabolism has been unsuccessful so far in the breast cancer clinical setting, with major unresolved challenges residing in target selection, development of robust biomarkers for response prediction, and understanding and harnessing of escape mechanisms. This Review discusses the pathophysiological role of HIFs, angiogenesis, and metabolism in breast cancer and the challenges of targeting these features in patients with breast cancer. Rational therapeutic combinations, especially with immunotherapy and endocrine therapy, seem most promising in the clinical exploitation of the intricate interplay of HIFs, angiogenesis, and metabolism in breast cancer cells and the tumor microenvironment.
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HIFs play critical roles in cancer progression by activating transcription of genes encoding proteins involved in angiogenesis, glucose metabolism, invasion/metastasis, stem cell specification, protumoral inflammatory responses, and tumor immune evasion.
“Hypoxia-inducible factors (HIFs) play critical roles in cancer progression by activating the transcription of a large battery of genes encoding proteins that play key roles in angiogenesis, glucose metabolism, invasion/metastasis, stem cell specification, protumoral inflammatory responses, and tumor immune evasion (18, 23–27).”
From HIF inhibitor 32-134D eradicates murine hepatocellular carcinoma in combination with anti-PD1 therapy (2022) · cites this paper as [23]
Tumors can induce angiogenesis from nearby blood vessels, triggered by hypoxia-induced HIF signaling and VEGF secretion by cancer cells in a growing tumor.
“In addition, there is crosstalk between (primary) tumors and blood vessels: tumors can induce angiogenesis from nearby blood vessels, which is triggered by hypoxia-induced hypoxia-inducible factor (HIF) signaling and vascular endothelial growth factor (VEGF) secretion by cancer cells in a growing tumor [48,49].”
From Cancer-on-chip models for metastasis: importance of the tumor microenvironment (2024) · cites this paper as [48]
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4 retracted
Samanta, D., Gilkes, D. M., Chaturvedi, P., Xiang, L., & Semenza, G. L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421438111 · Cited by 460 · see citing works
RetractedZhang, H., Wong, C. C. L., Wei, H., Gilkes, D. M., Korangath, P., Chaturvedi, P., Schito, L., Chen, J., Krishnamachary, B., Winnard, P. T., et al. (2012) · Oncogene · doi:10.1038/onc.2011.365 · Cited by 326 · see citing works
RetractedSamanta, D., Park, Y., Andrabi, S. A., Shelton, L. M., Gilkes, D. M., & Semenza, G. L. (2016) · Cancer Research · doi:10.1158/0008-5472.can-16-0530 · Cited by 238 · see citing works
RetractedMboge, M. Y., Chen, Z., Khokhar, D., Wolff, A., Ai, L., Heldermon, C. D., Bozdağ, M., Carta, F., Supuran, C. T., Brown, K. D., et al. (2019) · Biochemical Journal · doi:10.1042/bcj20190177 · Cited by 36 · see citing works
RetractedPD-1 and PD-L1 Immune Checkpoint Blockade to Treat Breast Cancer
Hartkopf, A. D., Taran, F., Wallwiener, M., Walter, C. B., Krämer, B., Grischke, E., & Brucker, S. Y. (2016) · Breast Care · doi:10.1159/000453569 · Cited by 30,989 · see citing works
Nishimura, R., Osako, T., Nishiyama, Y., Tashima, R., Nakano, M., Fujisue, M., Toyozumi, Y., & Arima, N. (2013) · Oncology · doi:10.1159/000353099 · Cited by 13,239 · see citing works
Comprehensive molecular portraits of human breast tumours
The Cancer Genome Atlas Network (2012) · Nature · doi:10.1038/nature11412 · Cited by 12,129 · see citing works
Biomarkers and surrogate endpoints: Preferred definitions and conceptual framework
Biomarkers Definitions Working Group (2001) · Clinical Pharmacology & Therapeutics · doi:10.1067/mcp.2001.113989 · Cited by 6,771 · see citing works
Wang, G. L., Jiang, B. H., Rue, E. A., & Semenza, G. L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.12.5510 · Cited by 6,212 · see citing works
Molecular mechanisms and clinical applications of angiogenesis
Carmeliet, P., & Jain, R. K. (2011) · Nature · doi:10.1038/nature10144 · Cited by 5,467 · see citing works
Targeting Hypoxia-Inducible Factors for the Treatment of Anemia in Chronic Kidney Disease Patients
Locatelli, F., Fishbane, S. N., Block, G. A., & Macdougall, I. C. (2017) · American Journal of Nephrology · doi:10.1159/000455166 · Cited by 4,834 · see citing works
Kim, J.-W., Tchernyshyov, I., Semenza, G. L., & Dang, C. V. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.02.002 · Cited by 3,905 · see citing works
Otto Warburg's contributions to current concepts of cancer metabolism
Koppenol, W. H., Bounds, P. L., & Dang, C. V. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3038 · Cited by 3,427 · see citing works
Breast cancer statistics, 2019
Desantis, C. E., Ma, J., Gaudet, M. M., Newman, L. A., Miller, K. D., Sauer, A. G., Jemal, A., & Siegel, R. L. (2019) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21583 · Cited by 3,126 · see citing works
From Krebs to clinic: glutamine metabolism to cancer therapy
Altman, B. J., Stine, Z. E., & Dang, C. V. (2016) · Nature Reviews Cancer · doi:10.1038/nrc.2016.71 · Cited by 2,119 · see citing works
The multifaceted roles of fatty acid synthesis in cancer
Röhrig, F., & Schulze, A. (2016) · Nature Reviews Cancer · doi:10.1038/nrc.2016.89 · Cited by 1,651 · see citing works
HIF-1 mediates metabolic responses to intratumoral hypoxia and oncogenic mutations
Semenza, G. L. (2013) · Journal of Clinical Investigation · doi:10.1172/jci67230 · Cited by 1,335 · see citing works
Hypoxia-inducible expression of tumor-associated carbonic anhydrases.
Wykoff, C. C., Beasley, N. J. P., Watson, P. H., Turner, K., Pastorek, J., Sibtain, A., Wilson, G. D., Turley, H., Talks, K., Maxwell, P. H., et al. (2000) · PubMed · Cited by 1,258 · see citing works
Self-citationLaughner, E., Taghavi, P., Chiles, K., Mahon, P. C., & Semenza, G. L. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.12.3995-4004.2001 · Cited by 1,256 · cited 1× · see citing works
“increase HIF levels through increased PI3K/Akt/mTOR signaling (14, 15).”
BackgroundVaupel, P. W., Schlenger, K., Knoop, C., & Höckel, M. (1991) · PubMed · Cited by 952 · see citing works
Advances in Hypoxia-Inducible Factor Biology
Choudhry, H., & Harris, A. L. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.10.005 · Cited by 873 · see citing works
Self-citationMutual regulation of tumour vessel normalization and immunostimulatory reprogramming
Tian, L., Goldstein, A., Wang, H., Ching Lo, H., Sun Kim, I., Welte, T., Sheng, K., Dobrolecki, L. E., Zhang, X., Putluri, N., et al. (2017) · Nature · doi:10.1038/nature21724 · Cited by 841 · see citing works
Antiangiogenic therapy in oncology: current status and future directions
Jayson, G. C., Kerbel, R. S., Ellis, L. M., & Harris, A. L. (2016) · The Lancet · doi:10.1016/s0140-6736(15)01088-0 · Cited by 829 · see citing works
Self-citationCombined antiangiogenic and anti–PD-L1 therapy stimulates tumor immunity through HEV formation
Allen, E., Jabouille, A., Rivera, L. B., Lodewijckx, I., Missiaen, R., Steri, V., Feyen, K., Tawney, J., Hanahan, D., Michael, I. P., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aak9679 · Cited by 820 · see citing works
XBP1 promotes triple-negative breast cancer by controlling the HIF1α pathway
Chen, X., Iliopoulos, D., Zhang, Q. H., Tang, Q., Greenblatt, M. B., Hatziapostolou, M., Lim, E., Tam, W. L., Ni, M., Chen, Y., et al. (2014) · Nature · doi:10.1038/nature13119 · Cited by 817 · see citing works
Chen, F., Chen, J., Yang, L., Liu, J., Zhang, X., Zhang, Y., Tu, Q., Yin, D., Lin, D., Wong, P., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0299-0 · Cited by 712 · see citing works
Therapeutic targeting of hypoxia and hypoxia-inducible factors in cancer
Wigerup, C., Påhlman, S., & Bexell, D. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.04.009 · Cited by 687 · see citing works
Monocarboxylate transporters in cancer
Payen, V. L., Mina, E., Hée, V. F. V., Porporato, P. E., & Sonveaux, P. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.07.006 · Cited by 665 · see citing works
Improving immunotherapy outcomes with anti-angiogenic treatments and vice versa
Khan, K. A., & Kerbel, R. S. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2018.9 · Cited by 661 · see citing works
Lee, K., Giltnane, J. M., Balko, J. M., Schwarz, L. J., Zotano, Á. G., Hutchinson, K. E., Nixon, M. J., Estrada, M. V., Sanchez, V. M., Sanders, M. E., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.09.009 · Cited by 652 · see citing works
Molecular mechanisms linking exercise to cancer prevention and treatment
Hojman, P., Gehl, J., Christensen, J. F., & Pedersen, B. K. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2017.09.015 · Cited by 600 · see citing works
Consensus guidelines for the use and interpretation of angiogenesis assays
Nowak-Sliwinska, P. M., Alitalo, K. K., Allen, E., Anisimov, A., Aplin, A. C., Auerbach, R., Augustin, H. G., Bates, D. O., B, J. R. V. B., Bender, R. H. F., et al. (2018) · Angiogenesis · doi:10.1007/s10456-018-9613-x · Cited by 600 · see citing works
Self-citationLevels of Hypoxia-Inducible Factor-1 During Breast Carcinogenesis
Bos, R., Zhong, H., Hanrahan, C. F., Mommers, E. C. M., Semenza, G. L., Pinedo, H. M., Abeloff, M. D., Simons, J. W., van Diest, P. J., & van der Wall, E. (2001) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/93.4.309 · Cited by 593 · see citing works
GDF15 mediates the effects of metformin on body weight and energy balance
Coll, A. P., Chen, M., Taskar, P., Rimmington, D., Patel, S., Tadross, J. A., Cimino, I., Yang, M., Welsh, P., Virtue, S., et al. (2020) · Nature · doi:10.1038/s41586-019-1911-y · Cited by 584 · see citing works
Schmittnaegel, M., Rigamonti, N., Kadioglu, E., Cassará, A., Wyser Rmili, C., Kiialainen, A., Kienast, Y., Mueller, H.-J., Ooi, C.-H., Laoui, D., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aak9670 · Cited by 582 · see citing works
The Regulation and Function of Lactate Dehydrogenase A: Therapeutic Potential in Brain Tumor
Valvona, C. J., Fillmore, H. L., Nunn, P. B., & Pilkington, G. J. (2015) · Brain Pathology · doi:10.1111/bpa.12299 · Cited by 570 · see citing works
The hypoxic tumor microenvironment: A driving force for breast cancer progression
Semenza, G. L. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.05.036 · Cited by 535 · see citing works
Normalizing Function of Tumor Vessels: Progress, Opportunities, and Challenges
Martin, J. D., Seano, G., & Jain, R. K. (2019) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020518-114700 · Cited by 530 · see citing works
An HIF-1α/VEGF-A Axis in Cytotoxic T Cells Regulates Tumor Progression
Palazon, A., Tyrakis, P. A., Macias, D., Veliça, P., Rundqvist, H., Fitzpatrick, S., Vojnovic, N., Phan, A. T., Loman, N., Hedenfalk, I., et al. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.10.003 · Cited by 521 · see citing works
Fasting and cancer: molecular mechanisms and clinical application
Nencioni, A., Caffa, I., Cortellino, S., & Longo, V. D. (2018) · Nature Reviews Cancer · doi:10.1038/s41568-018-0061-0 · Cited by 518 · see citing works
Pastorek, J., Pastoreková, S., Callebaut, I., Mornon, J., Zelnı́k, V., Opavský, R., Zaťovičová, M., Liao, S., Portetelle, D., & Stanbridge, E. J. (1994) · PubMed · Cited by 509 · see citing works
Bos, R., van der Groep, P., Greijer, A. E., Shvarts, A., Meijer, S., Pinedo, H. M., Semenza, G. L., van Diest, P. J., & van der Wall, E. (2003) · Cancer · doi:10.1002/cncr.11246 · Cited by 500 · see citing works
Schulte, M. L., Fu, A., Zhao, P., Li, J., Geng, L., Smith, S. T., Kondo, J., Coffey, R. J., Johnson, M. O., Rathmell, J. C., et al. (2018) · Nature Medicine · doi:10.1038/nm.4464 · Cited by 494 · see citing works
Wang, T., Gilkes, D. M., Takano, N., Xiang, L., Luo, W., Bishop, C. J., Chaturvedi, P., Green, J. J., & Semenza, G. L. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1410041111 · Cited by 493 · see citing works
Interplay between Circadian Clock and Cancer: New Frontiers for Cancer Treatment
Sulli, G., Lam, M. T. Y., & Panda, S. (2019) · Trends in cancer · doi:10.1016/j.trecan.2019.07.002 · Cited by 484 · see citing works
Microvessel Density as a Prognostic Factor in Women with Breast Cancer
Uzzan, B., Nicolas, P., Cucherat, M., & Perret, G. Y. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-1957 · Cited by 470 · see citing works
Vessel co-option mediates resistance to anti-angiogenic therapy in liver metastases
Frentzas, S., Simoneau, È., Bridgeman, V. L., Vermeulen, P., Foo, S., Kostaras, E., Nathan, M. R., Wotherspoon, A. C., Gao, Z., Shi, Y., et al. (2016) · Nature Medicine · doi:10.1038/nm.4197 · Cited by 456 · see citing works
Serine Catabolism Regulates Mitochondrial Redox Control during Hypoxia
Ye, J., Fan, J., Venneti, S., Wan, Y.-W., Pawel, B. R., Zhang, J., Finley, L. W. S., Lu, C., Lindsten, T., Cross, J. R., et al. (2014) · Cancer Discovery · doi:10.1158/2159-8290.cd-14-0250 · Cited by 452 · see citing works
Yoo, H. C., Park, S. J., Nam, M., Kang, J., Kim, K., Yeo, J. H., Kim, J.-K., Heo, Y., Lee, H. S., Lee, M. Y., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2019.11.020 · Cited by 449 · see citing works
Chia, S., Wykoff, C. C., Watson, P. H., Han, C., Leek, R., Pastorek, J., Gatter, K. C., Ratcliffe, P. J., & Harris, A. L. (2001) · Journal of Clinical Oncology · doi:10.1200/jco.2001.19.16.3660 · Cited by 434 · see citing works
Self-citationWalsh, J. C., Lebedev, A. Y., Aten, E., Madsen, K. S., Marciano, L., & Kolb, H. C. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5378 · Cited by 419 · see citing works
Benjamin, D., Robay, D., Hindupur, S. K., Pohlmann, J., Colombi, M., El‐Shemerly, M., Maira, S.-M., Moroni, C., Lane, H. A., & Hall, M. N. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.043 · Cited by 414 · see citing works
Dietary modifications for enhanced cancer therapy
Kanarek, N., Petrova, B., & Sabatini, D. M. (2020) · Nature · doi:10.1038/s41586-020-2124-0 · Cited by 414 · see citing works
Aberrant FGFR signaling mediates resistance to CDK4/6 inhibitors in ER+ breast cancer
Formisano, L., Lu, Y., Servetto, A., Hanker, A. B., Jansen, V. M., Bauer, J. A., Sudhan, D. R., Zotano, Á. G., Croessmann, S., Guo, Y. P., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09068-2 · Cited by 409 · see citing works
Oxygen-regulated transferrin expression is mediated by hypoxia-inducible factor-1
Rolfs, A., Kvietikova, I., Gassmann, M., & Wenger, R. H. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.32.20055 · Cited by 401 · see citing works
(2002) · PubMed · Cited by 385 · see citing works
Semenza, G. L. (2016) · The EMBO Journal · doi:10.15252/embj.201695204 · Cited by 369 · see citing works
Gebhart, G., Lamberts, L. E., Wimana, Z., Garcia, C. A., Emonts, P., Ameye, L., Stroobants, S. G., Huizing, M. T., Aftimos, P., Tol, J., et al. (2015) · Annals of Oncology · doi:10.1093/annonc/mdv577 · Cited by 354 · see citing works
Metabolism of [U‐ <sup>13</sup> C]glucose in human brain tumors <i>in vivo</i>
Maher, E. A., Marin‐Valencia, I., Bachoo, R. M., Mashimo, T., Raisanen, J., Hatanpaa, K. J., Jindal, A., Jeffrey, F. M., Choi, C., Madden, C., et al. (2012) · NMR in Biomedicine · doi:10.1002/nbm.2794 · Cited by 341 · see citing works
ERGO: A pilot study of ketogenic diet in recurrent glioblastoma
Rieger, J., Bähr, O., Maurer, G. D., Hattingen, E., Franz, K., Brucker, D. P., Walenta, S., Kämmerer, U., Coy, J. F., Weller, M., et al. (2014) · International Journal of Oncology · doi:10.3892/ijo.2014.2382 · Cited by 283 · see citing works
Collagen prolyl 4-hydroxylase 1 is essential for HIF-1α stabilization and TNBC chemoresistance
Xiong, G., Stewart, R. L., Chen, J., Gao, T., Scott, T. L., Samayoa, L. M., O’Connor, K. L., Lane, A. N., & Xu, R. (2018) · Nature Communications · doi:10.1038/s41467-018-06893-9 · Cited by 277 · see citing works
Fate-mapping post-hypoxic tumor cells reveals a ROS-resistant phenotype that promotes metastasis
Godet, I., Shin, Y. J., Ju, J. A., Ye, I. C., Wang, G., & Gilkes, D. M. (2019) · Nature Communications · doi:10.1038/s41467-019-12412-1 · Cited by 274 · see citing works
Lu, H., Samanta, D., Xiang, L., Zhang, H., Hu, H., Chen, I., Bullen, J. W., & Semenza, G. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1513433112 · Cited by 270 · see citing works
A guide to 13C metabolic flux analysis for the cancer biologist
Antoniewicz, M. R. (2018) · Experimental & Molecular Medicine · doi:10.1038/s12276-018-0060-y · Cited by 264 · see citing works
de Groot, S., Vreeswijk, M. P. G., Welters, M. J. P., Gravesteijn, G., Boei, J. J. W. A., Jochems, A., Houtsma, D., Putter, H., van der Hoeven, J. J. M., Nortier, J. W. R., et al. (2015) · BMC Cancer · doi:10.1186/s12885-015-1663-5 · Cited by 257 · see citing works
Characterization of hypoxia-associated molecular features to aid hypoxia-targeted therapy
Ye, Y., Hu, Q., Chen, H., Liang, K., Yuan, Y., Xiang, Y., Ruan, H., Zhang, Z., Song, A., Zhang, H., et al. (2019) · Nature Metabolism · doi:10.1038/s42255-019-0045-8 · Cited by 251 · see citing works
Generali, D., Berruti, A., Brizzi, M. P., Campo, L., Bonardi, S., Wigfield, S., Bersiga, A., Allevi, G., Milani, M., Aguggini, S., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-2690 · Cited by 250 · see citing works
Self-citationWykoff, C. C., Beasley, N. J. P., Watson, P. H., Campo, L., Chia, S., English, R. E., Pastorek, J., Sly, W. S., Ratcliffe, P. J., & Harris, A. L. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64048-5 · Cited by 249 · see citing works
Self-citationSullivan, M. R., Mattaini, K. R., Dennstedt, E. A., Nguyen, A. A., Sivanand, S., Reilly, M. F., Meeth, K. M., Muir, A., Darnell, A. M., Bosenberg, M., et al. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.02.015 · Cited by 242 · see citing works
ASCT2/SLC1A5 controls glutamine uptake and tumour growth in triple-negative basal-like breast cancer
van Geldermalsen, M., Wang, Q., Nagarajah, R., Marshall, A., Thoeng, A., Gao, D., Ritchie, W., Feng, Y., Bailey, C. G., Deng, N., et al. (2015) · Oncogene · doi:10.1038/onc.2015.381 · Cited by 235 · see citing works
Jeon, Y. J., Khelifa, S., Ratnikov, B. I., Scott, D. A., Feng, Y., Parisi, F., Ruller, C. M., Lau, E. K., Kim, H., Brill, L. M., et al. (2015) · Cancer Cell · doi:10.1016/j.ccell.2015.02.006 · Cited by 229 · see citing works
Paracrine Induction of HIF by Glutamate in Breast Cancer: EglN1 Senses Cysteine
Briggs, K. J., Koivunen, P., Cao, S., Backus, K. M., Olenchock, B. A., Patel, H., Zhang, Q. H., Signoretti, S., Gerfen, G. J., Richardson, A. L., et al. (2016) · Cell · doi:10.1016/j.cell.2016.05.042 · Cited by 228 · see citing works
MCT1 Modulates Cancer Cell Pyruvate Export and Growth of Tumors that Co-express MCT1 and MCT4
Hong, C. S., Graham, N. A., Gu, W., Camacho, C. E., Mah, V. H., Maresh, E. L., Alavi, M., Bagryanova, L., Krotee, P., Gardner, B. K., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.057 · Cited by 223 · see citing works
Incio, J., Ligibel, J. A., McManus, D. T., Suboj, P., Jung, K., Kawaguchi, K., Pinter, M., Babykutty, S., Chin, S. M., Vardam, T. D., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aag0945 · Cited by 222 · see citing works
Stessels, F., den Eynden, G. V., der Auwera, I. V., Salgado, R., den Heuvel, E. V., Harris, A. L., Jackson, D. G., Colpaert, C., Marck, E. A. V., Dirix, L. Y., et al. (2004) · British Journal of Cancer · doi:10.1038/sj.bjc.6601727 · Cited by 215 · see citing works
Self-citationHIF2α Acts as an mTORC1 Activator through the Amino Acid Carrier SLC7A5
Elorza, A., Soro-Arnáiz, I., Meléndez‐Rodríguez, F., Rodríguez-Vaello, V., Marsboom, G., de Cárcer, G., Acosta‐Iborra, B., Albacete-Albacete, L., Ordóñez, Á., Serrano‐Oviedo, L., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.09.017 · Cited by 206 · see citing works
Hypoxic Radioresistance: Can ROS Be the Key to Overcome It?
Wang, H., Jiang, H., Gucht, M. V. D., & Ridder, M. D. (2019) · Cancers · doi:10.3390/cancers11010112 · Cited by 206 · see citing works
Barrios, C. H., Liu, M.-C., Lee, S. C., Vanlemmens, L., Ferrero, J.-., Tabei, T., Pivot, X. B., Iwata, H., Aogi, K., Lugo-Quintana, R., et al. (2010) · Breast Cancer Research and Treatment · doi:10.1007/s10549-010-0788-0 · Cited by 199 · see citing works
Advances in Targeting Src in the Treatment of Breast Cancer and Other Solid Malignancies
Mayer, E. L., & Krop, I. E. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-1834 · Cited by 197 · see citing works
Inherent DNA‐binding specificities of the HIF‐1α and HIF‐2α transcription factors in chromatin
Smythies, J. A., Sun, M., Masson, N., Salama, R., Simpson, P. D., Murray, E., Neumann, V., Cockman, M. E., Choudhry, H., Ratcliffe, P. J., et al. (2019) · The EMBO Reports · doi:10.15252/embr.201846401 · Cited by 195 · see citing works
Mihály, Z., Kormos, M., Lánczky, A., Dank, M., Budczies, J., Szász, M. A., & Győrffy, B. (2013) · Breast Cancer Research and Treatment · doi:10.1007/s10549-013-2622-y · Cited by 190 · see citing works
Brooks, D. L. P., Schwab, L. P., Krutilina, R. I., Parke, D. N., Sethuraman, A., Hoogewijs, D., Schörg, A., Gotwald, L., Fan, M., Wenger, R. H., et al. (2016) · Molecular Cancer · doi:10.1186/s12943-016-0510-x · Cited by 190 · see citing works
Metabolic adaptation of cancer and immune cells mediated by hypoxia-inducible factors
Samanta, D., & Semenza, G. L. (2018) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2018.07.002 · Cited by 190 · see citing works
Sutendra, G., Dromparis, P., Kinnaird, A. S., Stenson, T. H., Haromy, A., Parker, J. M. R., McMurtry, M. S., & Michelakis, E. D. (2012) · Oncogene · doi:10.1038/onc.2012.198 · Cited by 185 · see citing works
Niu, Y.-L., Bao, L., Chen, Y., Wang, C., Luo, M., Zhang, B., Zhou, M., Wang, J. E., Fang, Y. V., Kumar, A., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-1532 · Cited by 177 · see citing works
ZMYND8 acetylation mediates HIF-dependent breast cancer progression and metastasis
Chen, Y., Zhang, B., Bao, L., Jin, L., Yang, M., Peng, Y., Kumar, A., Wang, J. E., Wang, C., Zou, X., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci95089 · Cited by 176 · see citing works
Wang, B.-Y., Zhang, J., Wang, J.-L., Sun, S., Wang, Z., Wang, L.-P., Zhang, Q.-L., Lv, F.-F., Cao, E.-Y., Shao, Z.-M., et al. (2015) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-015-0194-x · Cited by 174 · see citing works
The prognostic value of GLUT1 in cancers: a systematic review and meta-analysis
Yu, M., Yongzhi, H., Chen, S., Luo, X., Lin, Y., Zhou, Y., Jin, H., Hou, B., Deng, Y., Tu, L., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.17445 · Cited by 167 · see citing works
Lampa, M., Arlt, H., He, T., Ospina, B., Reeves, J., Zhang, B., Murtie, J. C., Deng, G., Barberis, C., Hoffmann, D., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0185092 · Cited by 166 · see citing works
Chafe, S. C., McDonald, P. C., Saberi, S., Nemirovsky, O., Venkateswaran, G., Burugu, S., Gao, D., Delaidelli, A., Kyle, A. H., Baker, J. H. E., et al. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0657 · Cited by 166 · see citing works
Cohen, C. W., Fontaine, K. R., Arend, R. C., Alvarez, R. D., Leath, C. A., Huh, W. K., Bevis, K. S., Kim, K. H., Straughn, J. M., & Gower, B. A. (2018) · Journal of Nutrition · doi:10.1093/jn/nxy119 · Cited by 164 · see citing works
Fu, X., Pereira, R., Angelis, C. D., Veeraraghavan, J., Nanda, S., Qin, L., Cataldo, M. L., Sethunath, V., Mehravaran, S., Gutiérrez, C., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1911584116 · Cited by 163 · see citing works
Gebhart, G., Cenzano, C. G., Holmes, E. M., Robles, J., Garcia, C. A., Cortés, M., de Azambuja, E., Fauria, K., Dooren, V. V., Aktan, G., et al. (2013) · Journal of Nuclear Medicine · doi:10.2967/jnumed.112.119271 · Cited by 162 · see citing works
Garcia, S., Dalès, J.-P., Charafe‐Jauffret, E., Carpentier-Meunier, S., Andrac, L., Jacquemier, J. D., Andonian, C., Lavaut, M., Allasia, C., Bonnier, P., et al. (2007) · Human Pathology · doi:10.1016/j.humpath.2006.11.015 · Cited by 156 · see citing works
Prognostic Significance of Carbonic Anhydrase IX Expression in Cancer Patients: A Meta-Analysis
van Kuijk, S. J. A., Yaromina, A., Houben, R. M. A., Niemans, R., Lambin, P., & Dubois, L. J. (2016) · Frontiers in Oncology · doi:10.3389/fonc.2016.00069 · Cited by 154 · see citing works
Liang, H., Xiao, J., Zhou, Z., Wu, J., Ge, F., Li, Z., Zhang, H., Sun, J., Li, F., Liu, R., et al. (2018) · Oncogene · doi:10.1038/s41388-017-0089-8 · Cited by 154 · see citing works
Low-Dose Anti-Angiogenic Therapy Sensitizes Breast Cancer to PD-1 Blockade
Li, Q., Wang, Y., Jia, W., Deng, H., Li, G., Deng, W., Chen, J., Kim, B. Y. S., Jiang, W., Liu, Q., et al. (2019) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-19-2179 · Cited by 154 · see citing works
Rai, G., Brimacombe, K. R., Mott, B. T., Urban, D. J., Hu, X., Yang, S., Lee, T. D., Cheff, D. M., Kouznetsova, J., Benavides, G. A., et al. (2017) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.7b00941 · Cited by 153 · see citing works
Coudert, B. P., Pierga, J., Mouret‐Reynier, M., et al. (2014) · The Lancet Oncology · doi:10.1016/s1470-2045(14)70475-9 · Cited by 149 · see citing works
Beloueche‐Babari, M., Galobart, T. C., Delgado‐Goñi, T., Wantuch, S., Parkes, H. G., Tandy, D., Harker, J. A., & Leach, M. O. (2020) · British Journal of Cancer · doi:10.1038/s41416-019-0717-x · Cited by 148 · see citing works
Yang, J., AlTahan, A. M., Jones, D. T., Buffa, F. M., Bridges, E., Interiano, R. B., Qu, C., Vogt, N., Li, J., Baban, D. F., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1422015112 · Cited by 139 · see citing works
Self-citationWang, J.-C., Li, G.-Y., Wang, B., Han, S.-X., Sun, X., Jiang, Y.-N., Shen, Y.-W., Zhou, C., Feng, J., Lu, S.-Y., et al. (2019) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-019-1211-2 · Cited by 138 · see citing works
Chu, Q. S.-C., Sangha, R. S., Spratlin, J. L., Vos, L. J., Mackey, J. R., McEwan, A. J. B., Venner, P. M., & Michelakis, E. D. (2015) · Investigational New Drugs · doi:10.1007/s10637-015-0221-y · Cited by 137 · see citing works
Helczynska, K., Larsson, A.-M., Holmquist Mengelbier, L., Bridges, E., Fredlund, E., Borgquist, S., Landberg, G., Påhlman, S., & Jirström, K. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-1135 · Cited by 136 · see citing works
Ansari, R. E., Craze, M. L., Miligy, I. M., Diez, M., Nolan, C. C., Ellis, I. O., Rakha, E. A., & Green, A. R. (2018) · Breast Cancer Research · doi:10.1186/s13058-018-0946-6 · Cited by 136 · see citing works
Tromberg, B. J., Zhang, Z., Leproux, A., O’Sullivan, T. D., Cerussi, A. E., Carpenter, P. M., Mehta, R. S., Roblyer, D. M., Yang, W. T., Paulsen, K. D., et al. (2016) · Cancer Research · doi:10.1158/0008-5472.can-16-0346 · Cited by 132 · see citing works
Lord, S., Cheng, W., Liu, D., Gaude, E., Haider, S. A., Metcalf, T., Patel, N., Teoh, E., Gleeson, F. V., Bradley, K. M., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.08.021 · Cited by 132 · see citing works
Self-citationCao, J., Liu, X., Yang, Y., et al. (2020) · Angiogenesis · doi:10.1007/s10456-020-09707-z · Cited by 132 · see citing works
Hypoxia-induced switch in SNAT2/SLC38A2 regulation generates endocrine resistance in breast cancer
Morotti, M., Bridges, E., Valli, A., Choudhry, H., Sheldon, H., Wigfield, S., Gray, N., Zois, C. E., Grimm, F., Jones, D., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1818521116 · Cited by 131 · see citing works
Self-citationJamali, S., Klier, M., Ames, S., Barros, L. F., McKENNA, R. V., Deitmer, J. W., & Becker, H. M. (2015) · Scientific Reports · doi:10.1038/srep13605 · Cited by 129 · see citing works
Miles, D. W., Cameron, D., Bondarenko, I., Manzyuk, L., Alcedo, J. C., Lopez, R. I., Im, S., Canon, J.-L. R., Shparyk, Y. V., Yardley, D. A., et al. (2016) · European Journal of Cancer · doi:10.1016/j.ejca.2016.09.024 · Cited by 126 · see citing works
Reduced Expression of Hypoxia-Inducible Factor-1α in Perinecrotic Regions of Solid Tumors
Sobhanifar, S., Aquino‐Parsons, C., Stanbridge, E. J., & Olive, P. L. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4480 · Cited by 124 · see citing works
Obesity-associated inflammation promotes angiogenesis and breast cancer via angiopoietin-like 4
Kolb, R. H., Kluz, P., Tan, Z. W., Borcherding, N. C., Bormann, N. L., Vishwakarma, A., Balcziak, L. K., Zhu, P., Davies, B. S. J., Gourronc, F. A., et al. (2018) · Oncogene · doi:10.1038/s41388-018-0592-6 · Cited by 123 · see citing works
Higashimura, Y., Nakajima, Y., Yamaji, R., et al. (2011) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2011.02.011 · Cited by 122 · see citing works
Phase II and Biomarker Study of Cabozantinib in Metastatic Triple-Negative Breast Cancer Patients
Tolaney, S. M., Ziehr, D. R., Guo, H., Ng, M. R., Barry, W. T., Higgins, M. J., Isakoff, S. J., Brock, J. E., Ivanova, E. V., Paweletz, C. P., et al. (2016) · The Oncologist · doi:10.1634/theoncologist.2016-0229 · Cited by 118 · see citing works
LDH-A regulates the tumor microenvironment via HIF-signaling and modulates the immune response
Serganova, I. S., Cohen, I., Vemuri, K., Shindo, M., Maeda, M., Mane, M. M., Moroz, E., Khanin, R., Satagopan, J. M., Koutcher, J. A., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0203965 · Cited by 118 · see citing works
Bartlett, J. M. S., Thomas, J. S. J., Ross, D. T., Seitz, R. S., Ring, B. Z., Beck, R. A., Pedersen, H. C., Munro, A. F., Kunkler, I. H., Campbell, F., et al. (2010) · Breast Cancer Research · doi:10.1186/bcr2604 · Cited by 117 · see citing works
Generali, D., Buffa, F. M., Berruti, A., Brizzi, M. P., Campo, L., Bonardi, S., Bersiga, A., Allevi, G., Milani, M., Aguggini, S., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2007.13.7083 · Cited by 116 · see citing works
Self-citationCheng, J., Li, L., Xu, J., Sun, Y., Zhang, Y., Wang, X., Pan, L., Shao, Z., Zhang, Y., & Liu, G. (2013) · Journal of Nuclear Medicine · doi:10.2967/jnumed.112.111963 · Cited by 107 · see citing works
Ueda, S., Saeki, T., Osaki, A., Yamane, T., & Kuji, I. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-0874 · Cited by 104 · see citing works
Szutowicz, A., Kwiatkowski, J., & Angielski, S. (1979) · British Journal of Cancer · doi:10.1038/bjc.1979.120 · Cited by 103 · see citing works
NDRG1 regulates neutral lipid metabolism in breast cancer cells
Sevinsky, C. J., Khan, F., Kokabee, L., Darehshouri, A., Maddipati, K. R., & Conklin, D. S. (2018) · Breast Cancer Research · doi:10.1186/s13058-018-0980-4 · Cited by 103 · see citing works
Liver-Type Glutaminase GLS2 Is a Druggable Metabolic Node in Luminal-Subtype Breast Cancer
Lukey, M. J., Cluntun, A. A., Katt, W. P., Lin, M.-C. J., Druso, J. E., Ramachandran, S., Erickson, J. W., Le, H. H., Wang, Z.-E., Blank, B., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.08.076 · Cited by 103 · see citing works
Bröer, A., Gauthier-Coles, G., Rahimi, F., van Geldermalsen, M., Dorsch, D., Wegener, A. A., Holst, J., & Bröer, S. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006378 · Cited by 101 · see citing works
Bane, A. L., Whelan, T. J., Pond, G. R., Parpia, S., Gohla, G., Fyles, A., Pignol, J., Pritchard, K. I., Chambers, S., & Levine, M. N. (2014) · Annals of Oncology · doi:10.1093/annonc/mdu090 · Cited by 100 · see citing works
Yang, J., Staples, O. D., Thomas, L. W., Briston, T., Robson, M. P., Poon, E., Simões, M. L., El‐Emir, E., Buffa, F. M., Ahmed, A., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58780 · Cited by 95 · see citing works
Self-citationMolecular Portrait of Hypoxia in Breast Cancer: A Prognostic Signature and Novel HIF-Regulated Genes
Ye, I. C., Fertig, E. J., DiGiacomo, J. W., Considine, M., Godet, I., & Gilkes, D. M. (2018) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-18-0345 · Cited by 95 · see citing works
Prognostic role of glycolysis for cancer outcome: evidence from 86 studies
Yu, M., Chen, S., Hong, W., Gu, Y., Huang, B., Lin, Y., Zhou, Y., Jin, H., Deng, Y., Tu, L., et al. (2019) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-019-02847-w · Cited by 93 · see citing works
Tafreshi, N. K., Bui, M. M., Bishop, K., Lloyd, M. C., Enkemann, S. A., Lopez, A. S., Abrahams, D. F., Carter, B. W., Vágner, J., Grobmyer, S. R., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-0238 · Cited by 91 · see citing works
Choi, J., Jung, W.-H., & Koo, J. S. (2012) · Pathobiology · doi:10.1159/000339513 · Cited by 89 · see citing works
The SIAH2-NRF1 axis spatially regulates tumor microenvironment remodeling for tumor progression
Ma, B., Cheng, H., Mu, C., Geng, G., Zhao, T., Luo, Q., Ma, K., Chang, R., Liu, Q., Gao, R., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08618-y · Cited by 89 · see citing works
Pan-genomic binding of hypoxia-inducible transcription factors
Schödel, J., Mole, D. R., & Ratcliffe, P. J. (2013) · Biological Chemistry · doi:10.1515/hsz-2012-0351 · Cited by 86 · see citing works
Tian, F., Shen, G., Deng, Y., et al. (2017) · European Radiology · doi:10.1007/s00330-017-4831-y · Cited by 85 · see citing works
Chen, Z., Wang, Y.-Z., Warden, C., & Chen, S. (2015) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2015.02.004 · Cited by 81 · see citing works
c- erb B-2 Related Aggressiveness in Breast Cancer Is Hypoxia Inducible Factor-1α Dependent
Giatromanolaki, A. N., Koukourakis, M. I., Simopoulos, C., Polychronidis, A., Gatter, K. C., Harris, A. L., & Sivridis, E. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-1068 · Cited by 81 · see citing works
Self-citationSamuel, S., Varghese, E., Kubatka, P., Triggle, C., & Büsselberg, D. (2019) · Biomolecules · doi:10.3390/biom9120846 · Cited by 81 · see citing works
Prognostic significance of c-Met in breast cancer: a meta-analysis of 6010 cases
Yan, S., Jiao, X., Zou, H., & Li, K. (2015) · Diagnostic Pathology · doi:10.1186/s13000-015-0296-y · Cited by 80 · see citing works
Grandjean, G. V., de Jong, P. R., James, B. P., Koh, M. Y., Lemos, R., Kingston, J., Aleshin, A. E., Bankston, L. A., Miller, C. P., Cho, E. J., et al. (2016) · Cancer Research · doi:10.1158/0008-5472.can-16-0401 · Cited by 79 · see citing works
Rodrigues, L. M., Uribe‐Lewis, S., Madhu, B., Honess, D. J., Stubbs, M., & Griffiths, J. R. (2017) · Cancer & Metabolism · doi:10.1186/s40170-017-0166-z · Cited by 78 · see citing works
Fako, V. E., Wu, X., Pflug, B. R., et al. (2014) · Journal of Medicinal Chemistry · doi:10.1021/jm501543u · Cited by 76 · see citing works
Ketogenic diets in medical oncology: a systematic review with focus on clinical outcomes
Klement, R. J., Brehm, N., & Sweeney, R. A. (2020) · Medical Oncology · doi:10.1007/s12032-020-1337-2 · Cited by 76 · see citing works
EglN2 associates with the NRF1‐PGC1α complex and controls mitochondrial function in breast cancer
Zhang, J., Wang, C., Chen, X., Takada, M., Fan, C., Zheng, X., Wen, H., Liu, Y., Wang, C., Pestell, R. G., et al. (2015) · The EMBO Journal · doi:10.15252/embj.201591437 · Cited by 74 · see citing works
HER2 regulates HIF-2α and drives an increased hypoxic response in breast cancer
Jarman, E. J., Ward, C., Turnbull, A., Martínez-Pérez, C., Meehan, J., Xintaropoulou, C., Sims, A. H., & Langdon, S. P. (2019) · Breast Cancer Research · doi:10.1186/s13058-019-1097-0 · Cited by 73 · see citing works
Targeting tumor-associated acidity in cancer immunotherapy
Lacroix, R., Rozeman, E. A., Kreutz, M. P., Renner, K., & Blank, C. U. (2018) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-018-2195-z · Cited by 71 · see citing works
(2019) · Advances in Cancer Research · doi:10.1016/bs.acr.2018.11.001 · Cited by 71 · see citing works
Jögi, A., Ehinger, A., Hartman, L. W., & Alkner, S. (2019) · PLoS ONE · doi:10.1371/journal.pone.0226150 · Cited by 70 · see citing works
Glutamine Metabolism Drives Growth in Advanced Hormone Receptor Positive Breast Cancer
Demas, D. M., Demo, S. D., Fallah, Y., Clarke, R. C., Nephew, K. P., Althouse, S. K., Sandusky, G. E., He, W., & Shajahan‐Haq, A. N. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00686 · Cited by 66 · see citing works
Hypoxia-reprogrammed tricarboxylic acid cycle promotes the growth of human breast tumorigenic cells
Tang, K., Yu, Y., Zhu, L., Xu, P., Chen, J., Ma, J., Zhang, H., Fang, H., Sun, W., Zhou, L., et al. (2019) · Oncogene · doi:10.1038/s41388-019-0932-1 · Cited by 66 · see citing works
Nieto, Y. L., Woods, J., Nawaz, F., Baron, A. D., Jones, R. B., Shpall, E. J., & Nawaz, S. (2007) · British Journal of Cancer · doi:10.1038/sj.bjc.6603875 · Cited by 63 · see citing works
van Geldermalsen, M., Quek, L., Turner, N. A., Freidman, N., Pang, A., Guan, Y. F., Krycer, J. R., Ryan, R. M., Wang, Q., & Holst, J. (2018) · BMC Cancer · doi:10.1186/s12885-018-4599-8 · Cited by 62 · see citing works
Hlouschek, J., Ritter, V., Wirsdörfer, F., Klein, D., Jendrossek, V., & Matschke, J. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.09.002 · Cited by 62 · see citing works
Ames, S., Pastoreková, S., & Becker, H. M. (2018) · Oncotarget · doi:10.18632/oncotarget.25371 · Cited by 61 · see citing works
Hypoxic pathobiology of breast cancer metastasis
Schito, L., & Rey, S. (2017) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2017.05.004 · Cited by 60 · see citing works
Altemus, M., Goo, L., Little, A. C., Yates, J. A., Cheriyan, H., Wu, Z.-F., & Merajver, S. D. (2019) · PLoS ONE · doi:10.1371/journal.pone.0220973 · Cited by 59 · see citing works
CAIX forms a transport metabolon with monocarboxylate transporters in human breast cancer cells
Ames, S., Andring, J. T., McKENNA, R. V., & Becker, H. M. (2019) · Oncogene · doi:10.1038/s41388-019-1098-6 · Cited by 58 · see citing works
den Eynden, G. G. V., der Auwera, I. V., Laere, S. V., Colpaert, C., Turley, H., Harris, A. L., van Dam, P. A., Dirix, L. Y., Vermeulen, P., & Marck, E. A. V. (2005) · British Journal of Cancer · doi:10.1038/sj.bjc.6602828 · Cited by 56 · see citing works
Self-citationThe Linkage between Breast Cancer, Hypoxia, and Adipose Tissue
Rausch, L. K., Netzer, N. C., Hoegel, J. J., & Pramsohler, S. (2017) · Frontiers in Oncology · doi:10.3389/fonc.2017.00211 · Cited by 56 · see citing works
Dieras, V. C., Wildiers, H. P. M. W., Jassem, J., et al. (2015) · The Breast · doi:10.1016/j.breast.2014.11.003 · Cited by 50 · see citing works
Reguera-Nuñez, E., Xu, P., Chow, A., Man, S., Hilberg, F., & Kerbel, R. S. (2019) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-018-0999-5 · Cited by 50 · see citing works
Quintela-Fandiño, M., Morales, S. M., Cortés-Salgado, A., Manso, L., Apala, J. V., Muñoz, M., Cudós, A. G., Fortuny, J. S., Gión, M., López‐Alonso, A., et al. (2019) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-19-2023 · Cited by 49 · see citing works
Metformin-induced caveolin-1 expression promotes T-DM1 drug efficacy in breast cancer cells
Chung, Y., Chang, C.-M., Wei, W., Chang, T.-W., Chang, K., & Chao, W. (2018) · Scientific Reports · doi:10.1038/s41598-018-22250-8 · Cited by 48 · see citing works
Wu, F. T. H., Xu, P., Chow, A., Man, S., Krüger, J., Khan, K. A., Paez-Ribes, M., Pham, E., & Kerbel, R. S. (2019) · British Journal of Cancer · doi:10.1038/s41416-018-0297-1 · Cited by 47 · see citing works
GOUSSIA, A. C., Simou, N., Zagouri, F., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0200302 · Cited by 46 · see citing works
Bello, E., Taraboletti, G., Colella, G., Zucchetti, M., Forestieri, D., Licandro, S. A., Berndt, A., Richter, P., D’Incalci, M., Cavalletti, E., et al. (2012) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-12-0275-t · Cited by 45 · see citing works
A network analysis to identify mediators of germline-driven differences in breast cancer prognosis
Escala-Garcia, M., Abraham, J., Andrulis, I. L., Anton‐Culver, H., Arndt, V., Ashworth, A., Auer, P. L., Auvinen, P., Beckmann, M. W., Beesley, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-019-14100-6 · Cited by 42 · see citing works
Tagg, S., Foster, P., Leese, M. P., et al. (2008) · British Journal of Cancer · doi:10.1038/sj.bjc.6604752 · Cited by 41 · see citing works
DNA Methylation Signatures Predicting Bevacizumab Efficacy in Metastatic Breast Cancer
Gampenrieder, S. P., Rinnerthaler, G., Hackl, H., Pulverer, W., Weinhaeusel, A., Ilic, S., Hufnagl, C., Hauser‐Kronberger, C., Egle, A., Risch, A., et al. (2018) · Theranostics · doi:10.7150/thno.23544 · Cited by 41 · see citing works
Na+,HCO3− cotransporter NBCn1 accelerates breast carcinogenesis
Boedtkjer, E. (2019) · Cancer and Metastasis Reviews · doi:10.1007/s10555-019-09784-7 · Cited by 41 · see citing works
Mehta, S., Hughes, N. P., Li, S., Jubb, A. M., Adams, R. F., Lord, S., Koumakis, L., van Stiphout, R. G. P. M., Padhani, A. R., Makris, A., et al. (2016) · EBioMedicine · doi:10.1016/j.ebiom.2016.07.017 · Cited by 39 · see citing works
Self-citationGolfmann, K., Meder, L., Koker, M., Volz, C., Borchmann, S., Tharun, L., Dietlein, F., Malchers, F., Florin, A., Büttner, R., et al. (2018) · Oncogene · doi:10.1038/s41388-018-0380-3 · Cited by 39 · see citing works
Targeting of two aspects of metabolism in breast cancer treatment
Gang, B. P., Dilda, P. J., Hogg, P. J., & Blackburn, A. C. (2014) · Cancer Biology & Therapy · doi:10.4161/15384047.2014.955992 · Cited by 38 · see citing works
Nie, C., Lv, H., Bie, L., Hou, H., & Chen, X. (2018) · Medicine · doi:10.1097/md.0000000000013551 · Cited by 38 · see citing works
Godbole, M. S., Togar, T., Patel, K., Dharavath, B., Yadav, N., Janjuha, S., Gardi, N., Tiwary, K., Terwadkar, P., Desai, S., et al. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.002894 · Cited by 37 · see citing works
Leone, J. P., Duda, D. G., Hu, J., Barry, W. T., Trippa, L., Gerstner, E. R., Jain, R. K., Tan, S., Lawler, E., Winer, E. P., et al. (2019) · Breast Cancer Research and Treatment · doi:10.1007/s10549-019-05445-z · Cited by 37 · see citing works
Mahdi, A., Darvishi, B., Majidzadeh‐A, K., Salehi, M., & Farahmand, L. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27414 · Cited by 35 · see citing works
HIF-1α Overexpression in Ductal Carcinoma In Situ of the Breast in BRCA1 and BRCA2 Mutation Carriers
van der Groep, P., van Diest, P. J., Smolders, Y. H. C. M., Ausems, M. G. E. M., van der Luijt, R. B., Menko, F. H., Bart, J., de Vries, E. G. E., & van der Wall, E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056055 · Cited by 34 · see citing works
Humbert, O., Lasserre, M., Bertaut, A., Fumoleau, P., Coutant, C., Brunotte, F., & Cochet, A. (2018) · Journal of Nuclear Medicine · doi:10.2967/jnumed.117.203075 · Cited by 33 · see citing works
Asano, A., Ueda, S., Kuji, I., et al. (2018) · Breast Cancer Research · doi:10.1186/s13058-018-0970-6 · Cited by 33 · see citing works
Chandran, V. I., Månsson, A., Barbachowska, M., Cerezo-Magaña, M., Nodin, B., Joshi, B., Koppada, N., Saad, O. M., Gluz, O., Isaksson, K., et al. (2020) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-19-0856 · Cited by 32 · see citing works
Quintela-Fandiño, M., Apala, J. V., Malón, D., Mouron, S. A., Hornedo, J., González‐Cortijo, L., Colomer, R., & Guerra, J. A. (2019) · Breast Cancer Research · doi:10.1186/s13058-019-1152-x · Cited by 30 · see citing works
Wang, F., Li, S., Zhao, Y., et al. (2016) · The Breast · doi:10.1016/j.breast.2016.04.016 · Cited by 29 · see citing works
Phase II randomised discontinuation trial of brivanib in patients with advanced solid tumours
Jones, R. L., Ratain, M. J., O'Dwyer, P. J., Siu, L. L., Jassem, J., Médioni, J., deJonge, M. J. A., Rudin, C. M., Sawyer, M. B., Khayat, D., et al. (2019) · European Journal of Cancer · doi:10.1016/j.ejca.2019.07.024 · Cited by 29 · see citing works
In vitro downregulated hypoxia transcriptome is associated with poor prognosis in breast cancer
Abu‐Jamous, B., Buffa, F. M., Harris, A. L., & Nandi, A. K. (2017) · Molecular Cancer · doi:10.1186/s12943-017-0673-0 · Cited by 28 · see citing works
Self-citationBRCA1-IRIS promotes human tumor progression through PTEN blockade and HIF-1α activation
Li, A. G., Murphy, E. C., Culhane, A. C., Powell, E., Wang, H., Bronson, R. T., Von, T., Giobbie‐Hurder, A., Gelman, R. S., Briggs, K. J., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1807112115 · Cited by 28 · see citing works
Causes and Consequences of A Glutamine Induced Normoxic HIF1 Activity for the Tumor Metabolism
Kappler, M., Pabst, U., Weinholdt, C., Taubert, H. W., Rot, S., Kaune, T., Kotrba, J., Porsch, M., Güttler, A., Bache, M., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20194742 · Cited by 28 · see citing works
Han, S., Huang, T., Hou, F., Yao, L., Wang, X., & Wu, X. (2019) · Therapeutic Advances in Medical Oncology · doi:10.1177/1758835919875851 · Cited by 28 · see citing works
Naranjo, I. D. (2019) · Journal of Breast Cancer · doi:10.4048/jbc.2019.22.e26 · Cited by 27 · see citing works
Fuady, J. H., Gutsche, K., Santambrogio, S., Varga, Z., Hoogewijs, D., & Wenger, R. H. (2016) · Oncotarget · doi:10.18632/oncotarget.8866 · Cited by 26 · see citing works
Metabolic consequences of HIF silencing in a triple negative human breast cancer xenograft
Bharti, S. K., Mironchik, Y., Wildes, F. B., Penet, M., Goggins, E. S., Krishnamachary, B., & Bhujwalla, Z. M. (2018) · Oncotarget · doi:10.18632/oncotarget.24569 · Cited by 26 · see citing works
Adams, A. L. L., van Brussel, A. S. A., Vermeulen, J. F., Mali, W. P. T. M., van der Wall, E., van Diest, P. J., & Elias, S. G. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-538 · Cited by 24 · see citing works
Ho, D., Huang, J. Y., Chapman, J. W., et al. (2017) · Breast Cancer Research and Treatment · doi:10.1007/s10549-017-4273-x · Cited by 23 · see citing works
Thomas, L. W., Stephen, J. M., Esposito, C., et al. (2019) · Cancer & Metabolism · doi:10.1186/s40170-019-0194-y · Cited by 23 · see citing works
Koukourakis, M. I., Giatromanolaki, A. N., Bottini, A., Cappelletti, M., Zanotti, L., Allevi, G., Strina, C., Ardine, M., Milani, M., Brugnoli, G., et al. (2014) · British Journal of Cancer · doi:10.1038/bjc.2014.196 · Cited by 19 · see citing works
Self-citationAlves, W. E. F. M., Bonatelli, M., Dufloth, R. M., Kerr, L. M., Carrara, G. F. A., Costa, R. F. A., Scapulatempo‐Neto, C., Tiezzi, D. G., Vieira, R. A. D. C., & Pinheiro, C. M. (2019) · BMC Cancer · doi:10.1186/s12885-019-6353-2 · Cited by 19 · see citing works
Msaki, A., Pastò, A., Curtarello, M., Arigoni, M., Barutello, G., Calogero, R., Macagno, M., Cavallo, F., Amadori, A., & Indraccolo, S. (2016) · Oncotarget · doi:10.18632/oncotarget.8859 · Cited by 18 · see citing works
Zhang, Z., Luo, G., Tang, H., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165725 · Cited by 18 · see citing works
Pivovarova, A. I., & MacGregor, G. G. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.12.048 · Cited by 17 · see citing works
Luo, D., Liu, H., Lin, D., Lian, K., & Ren, H. (2018) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-18-0881 · Cited by 17 · see citing works
Karn, T., Meißner, T., Weber, K. E., et al. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-19-1954 · Cited by 16 · see citing works
Liu, Y. H., Xue, L. B., Yang, Y. F., et al. (2018) · Medicine · doi:10.1097/md.0000000000012683 · Cited by 13 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [5]5. Harris AL. Clinical strategies to inhibit tumor vas- cularization. In: Ribatti D, Pezzella F, eds. Tumor Vascularization. Elsevier Science; 2020:147-175.
- [19]19. Giatromanolaki A, et al. c-erbB-2 related aggres- siveness in breast cancer is hypoxia inducible factor-1alpha dependent. Clin Cancer Res. 2004;10(23):7972-7977.
Cited by
Sorted by citations
HIF-1-Independent Mechanisms Regulating Metabolic Adaptation in Hypoxic Cancer Cells
Lee, S.-H., Golinska, M., & Griffiths, J. R. (2021) · Cells · doi:10.3390/cells10092371 · Cited by 169 · see citing works
Salman, S., Meyers, D. J., Wicks, E. E., Lee, S. N., Datan, E., Thomas, A. M., Anders, N. M., Hwang, Y., Lyu, Y., Yang, Y., et al. (2022) · Journal of Clinical Investigation · doi:10.1172/jci156774 · Cited by 111 · see citing works
Cancer-on-chip models for metastasis: importance of the tumor microenvironment
Jouybar, M., de Winde, C. M., Wolf, K., Friedl, P., Mebius, R. E., & den Toonder, J. M. J. (2024) · Trends in Biotechnology · doi:10.1016/j.tibtech.2023.10.001 · Cited by 66 · see citing works
McCubrey, J. A., Yang, L. V., Abrams, S. L., Steelman, L. S., Follo, M. Y., Cocco, L., Ratti, S., Martelli, A. M., Augello, G., & Cervello, M. (2022) · Cells · doi:10.3390/cells11142155 · Cited by 49 · see citing works
Li, P., Dong, Z., Jiang, Q., Yu, C., Liu, Y., Yuan, R., Qiu, Y., Meng, T., Hu, F., & Yuan, H. (2026) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.114406 · Cited by 6 · see citing works
- Authors
- de Heer, E. C., Jalving, M., & Harris, A. L.
- Affiliations
- University Medical Center Groningen (NL)
- University of Oxford (GB)
- Corresponding author
- Harris, Adrian L.
- Venue
- Journal of Clinical Investigation
- Published
- 2020-10-01
- Volume
- 130
- Issue
- 10
- Pages
- 5074-5087
- ISSN
- 0021-9738 (ISSN-L)
- 1558-8238
- PMC
- PMC7524491
- OpenAlex
- W3082891477
- Cited by
- 372
- References
- 202
- Citations by year
- 2026: 32 · 2025: 69 · 2024: 83 · 2023: 94 · 2022: 71 · 2021: 22
- FWCI
- 4.79
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- other-oa
- Locations
- Journal of Clinical Investigation (publishedVersion, other-oa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Funders
- Breast Cancer Research Foundation
- Cancer Research UK (A18974, 18974)
- University of Oxford
- KWF Kankerbestrijding (Young Investigator Grant 10913/2017-1, 10913/2017-1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- hypoxia-inducible factor, breast cancer, angiogenesis, cancer metabolism, metabolic reprogramming, treatment resistance, tumor microenvironment, combination immunotherapy, endocrine therapy, biomarkers, HIF-targeted therapy
- MeSH terms
- Animals, Hypoxia, Breast Neoplasms, Female, Humans, Models, Biological, Neovascularization, Pathologic, Prognosis, Biomarkers, Tumor, Signal Transduction, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins, Hypoxia-Inducible Factor 1, alpha Subunit, Tumor Microenvironment
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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