Angiogenesis and Metabolism: Entwined for Therapy Resistance
Abstract
Angiogenesis and metabolism are entwined processes that permit tumor growth and progression. Blood vessel supply is necessary for tumor survival not only by providing oxygen and nutrients for anabolism but also by removing waste products from cellular metabolism. On the other hand, blocking angiogenesis with antiangiogenic therapies shows clinical benefits in treating several tumor types. Nevertheless, resistance to therapy emerges over time. In this review we discuss a novel mechanism of adaptive resistance involving metabolic adaptation of tumor cells, and we also provide examples of tumor adaptation to therapy, which may represent a new mechanism of resistance in several types of cancer. Thus, targeting this metabolic tumor adaptation could be a way to avoid resistance in cancer patients.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Metabolic adaptation can be observed when tumor cells survive the consequences of anti-angiogenetic or anti-HIF1α treatments.
“Metabolic adaptation can be observed in case tumor cells survive the consequences of anti-angiogenetic or anti-HIF1α treatments.”
From Hypoxia Signaling in Cancer: From Basics to Clinical Practice (2021) · cites this paper as [95]
Cites
1 retracted
Csibi, A., Lee, G., Yoon, S.-O., Tong, H., Ilter, D., Elia, I., Fendt, S., Roberts, T. M., & Blenis, J. (2014) · Current Biology · doi:10.1016/j.cub.2014.08.007 · Cited by 253 · see citing works
RetractedHallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
Hanahan, D., & Weinberg, R. A. (2000) · Cell · doi:10.1016/s0092-8674(00)81683-9 · Cited by 29,219 · see citing works
Tumor angiogenesis: therapeutic implications
Sherwood, L. M., Parris, E. E., & Folkman, J. (1971) · New England Journal of Medicine · doi:10.1056/nejm197111182852108 · Cited by 10,187 · see citing works
The emerging hallmarks of cancer metabolism
Pavlova, N. N., & Thompson, C. B. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2015.12.006 · Cited by 5,926 · see citing works
Modes of resistance to anti-angiogenic therapy
Bergers, G., & Hanahan, D. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2442 · Cited by 2,953 · cited 1× · see citing works
“Antiangiogenic drugs used in the clinic extend survival in the order of months in some 203 cancer settings while failing to induce survival benefit in others, in part because of intrinsic 204 refractoriness or evasive escape[39].”
BackgroundCancer cell metabolism: warburg and beyond
Hsu, P. P., & Sabatini, D. M. (2008) · Cell · doi:10.1016/j.cell.2008.08.021 · Cited by 2,452 · see citing works
Angiogenesis: an organizing principle for drug discovery?
Folkman, J. (2007) · Nature Reviews Drug Discovery · doi:10.1038/nrd2115 · Cited by 2,248 · see citing works
Shibuya, M. (2011) · Genes & Cancer · doi:10.1177/1947601911423031 · Cited by 1,778 · see citing works
Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance
Boehm, T., Folkman, J., Browder, T., & O'Reilly, M. S. (1997) · Nature · doi:10.1038/37126 · Cited by 1,683 · see citing works
Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice
Sonveaux, P., Végran, F., Schroeder, T., Wergin, M., Verrax, J., Rabbani, Z. N., Saedeleer, C. J. D., Kennedy, K. M., Diepart, C., Jordan, B. F., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci36843 · Cited by 1,633 · see citing works
Normalization of the Vasculature for Treatment of Cancer and Other Diseases
Goel, S., Duda, D. G., Xu, L., Munn, L. L., Boucher, Y., Fukumura, D., & Jain, R. K. (2011) · Physiological Reviews · doi:10.1152/physrev.00038.2010 · Cited by 1,605 · see citing works
Nishida, N., Yano, H., Nishida, T., Kamura, T., & Kojiro, M. (2006) · Vascular Health and Risk Management · doi:10.2147/vhrm.2006.2.3.213 · Cited by 1,467 · see citing works
Hypoxia-Induced Angiogenesis: Good and Evil
Krock, B. L., Skuli, N., & Simon, M. C. (2011) · Genes & Cancer · doi:10.1177/1947601911423654 · Cited by 1,179 · see citing works
Hypoxia and Metabolic Adaptation of Cancer Cells
Eales, K. L., Hollinshead, K. E. R., & Tennant, D. A. (2016) · Oncogenesis · doi:10.1038/oncsis.2015.50 · Cited by 724 · cited 1× · see citing works
“But more importantly, they are 41 highly entwined processes that share common molecules and signaling 42 pathways[4].”
BackgroundGlutaminolysis Activates Rag-mTORC1 Signaling
Durán, R. V., Oppliger, W., Robitaille, A. M., Heiserich, L., Skendaj, R., Gottlieb, E., & Hall, M. N. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.05.043 · Cited by 723 · see citing works
Disrupting proton dynamics and energy metabolism for cancer therapy
Parks, S. K., Chiche, J., & Pouysségur, J. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3579 · Cited by 613 · see citing works
Why are tumour blood vessels abnormal and why is it important to know?
Nagy, J. A., Chang, S.-H., Dvorak, A. M., & Dvorak, H. F. (2009) · British Journal of Cancer · doi:10.1038/sj.bjc.6604929 · Cited by 611 · see citing works
Nucleoside analogues and nucleobases in cancer treatment
Galmarini, C. M., Mackey, J. R., & Dumontet, C. (2002) · The Lancet Oncology · doi:10.1016/s1470-2045(02)00788-x · Cited by 608 · see citing works
Resistance to targeted therapy in renal-cell carcinoma
Rini, B. I., & Atkins, M. B. (2009) · The Lancet Oncology · doi:10.1016/s1470-2045(09)70240-2 · Cited by 569 · see citing works
Benita, Y., Kikuchi, H., Smith, A. D., Zhang, M. Q., Chung, D. C., & Xavier, R. J. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp425 · Cited by 469 · see citing works
Use of ?-asparaginase in childhood ALL
Müller, H.-J. (1998) · Critical Reviews in Oncology/Hematology · doi:10.1016/s1040-8428(98)00015-8 · Cited by 458 · see citing works
Molecular aspects of cancer cell resistance to chemotherapy
Rebucci, M., & Michiels, C. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.02.017 · Cited by 409 · see citing works
The pentose phosphate pathway: An antioxidant defense and a crossroad in tumor cell fate
Riganti, C., Gazzano, E., Polimeni, M., Aldieri, E., & Ghigo, D. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.05.006 · Cited by 408 · see citing works
Sun, R. C., & Denko, N. C. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2013.11.022 · Cited by 344 · see citing works
Oxygen-independent Regulation of HIF-1: Novel Involvement of PI3K/ AKT/mTOR Pathway in Cancer
Agani, F. H., & Jiang, B. (2013) · Current Cancer Drug Targets · doi:10.2174/1568009611313030003 · Cited by 265 · see citing works
Alfarouk, K. O., Verduzco, D., Rauch, C., Muddathir, A. K., Bashir, A. H. H., Elhassan, G. O., Ibrahim, M. E., Orozco, J. D. P., Cardone, R. A., Reshkin, S. J., et al. (2014) · Oncoscience · doi:10.18632/oncoscience.109 · Cited by 245 · see citing works
Hypoxia and energetic tumour metabolism
Brahimi-Horn, M. C., Bellot, G. L., & Pouysségur, J. (2010) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2010.10.006 · Cited by 228 · see citing works
Allen, E., Miéville, P., Warren, C. M., Saghafinia, S., Li, L., Peng, M.-W., & Hanahan, D. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.029 · Cited by 221 · see citing works
Targeting Metabolic Symbiosis to Overcome Resistance to Anti-angiogenic Therapy
Pisarsky, L., Bill, R., Fagiani, E., Dimeloe, S., Goosen, R., Hagmann, J., Hess, C., & Christofori, G. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.028 · Cited by 199 · see citing works
Walling, J. (2006) · Investigational New Drugs · doi:10.1007/s10637-005-4541-1 · Cited by 182 · see citing works
Kaluz, Š., Kaluzová, M., & Stanbridge, E. J. (2008) · Clinica Chimica Acta · doi:10.1016/j.cca.2008.05.002 · Cited by 171 · see citing works
The role of acidity in solid tumour growth and invasion
B, K. S. A., Gavaghan, D. J., Gatenby, R. A., & Maini, P. K. (2005) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2005.02.001 · Cited by 157 · see citing works
Recent Advances in Anti-Angiogenic Therapy of Cancer
Samant, R. S., & Shevde, L. A. (2011) · Oncotarget · doi:10.18632/oncotarget.234 · Cited by 130 · see citing works
Phase 1 trial of everolimus plus sunitinib in patients with metastatic renal cell carcinoma
Molina, A. M., Feldman, D. R., Voss, M. H., Ginsberg, M. S., Baum, M. S., Brocks, D. R., Fischer, P., Trinos, M. J., Patil, S., & Motzer, R. J. (2011) · Cancer · doi:10.1002/cncr.26429 · Cited by 127 · see citing works
Motzer, R. J., Hutson, T. E., Ren, M., Dutcus, C. E., & Larkin, J. (2015) · The Lancet Oncology · doi:10.1016/s1470-2045(15)00543-4 · Cited by 124 · see citing works
The pharmacology of cancer resistance.
O'Connor, R. A. (2007) · PubMed · Cited by 121 · see citing works
Regulation of mTORC1 Signaling by pH
Balgi, A. D., Diering, G. H., Donohue, E., Lam, K., Fonseca, B. D., Zimmerman, C., Numata, M., & Roberge, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021549 · Cited by 118 · see citing works
Jiménez-Valerio, G., Martínez‐Lozano, M., Bassani, N., Vidal, A., Ochoa-de-Olza, M., Suárez, C., del Muro, X. G., Carles, J., Viñals, F., Graupera, M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.015 · Cited by 118 · see citing works
Organ-Specific Cancer Metabolism and Its Potential for Therapy
Elia, I., Schmieder, R., Christen, S., & Fendt, S. (2015) · Handbook of experimental pharmacology · doi:10.1007/164_2015_10 · Cited by 111 · see citing works
Endothelial cell metabolism: parallels and divergences with cancer cell metabolism
Verdegem, D., Moens, S., Stapor, P. C., & Carmeliet, P. (2014) · Cancer & Metabolism · doi:10.1186/2049-3002-2-19 · Cited by 110 · see citing works
Antiangiogenic Therapies: Going beyond Their Limits
Moserle, L., Jiménez-Valerio, G., & Casanovas, O. (2013) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0199 · Cited by 102 · see citing works
Kerbel, R. S. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.09.016 · Cited by 58 · see citing works
Phase II trial of second-line everolimus in patients with metastatic renal cell carcinoma (RECORD-4)
Motzer, R. J., Alyasova, A. V., Ye, D., Karpenko, A., Li, H., Alekseev, B. Y., Xie, L., Kurteva, G. P., Kowalyszyn, R. D., Karyakin, O. B., et al. (2015) · Annals of Oncology · doi:10.1093/annonc/mdv612 · Cited by 44 · see citing works
Antiangiogenic Resistance: Novel Angiogenesis Axes Uncovered by Antiangiogenic Therapies Research
Jiménez-Valerio, G., & Casanovas, O. (2016) · Current Drug Targets · doi:10.2174/1389450117666160301101425 · Cited by 13 · see citing works
Resistance to anti-angiogenic agents: a brief review of mechanisms and consequences.
Edelman, M. J., & Mao, L. (2013) · Europe PMC (PubMed Central) · doi:10.3978/j.issn.2218-6751.2013.01.02 · Cited by 9 · see citing works
Combination therapy in kidney cancer: the next revolution?
Buti, S., & Bersanelli, M. (2015) · The Lancet Oncology · doi:10.1016/s1470-2045(15)00325-3 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Cuproptosis: A novel therapeutic target for overcoming cancer drug resistance
Wang, Y., Chen, Y., Zhang, J., Yang, Y., Fleishman, J. S., Wang, Y., Wang, J., Chen, J., Li, Y., & Wang, H. (2023) · Drug Resistance Updates · doi:10.1016/j.drup.2023.101018 · Cited by 265 · see citing works
Zhou, Y., Chen, X., Cao, J., & Gao, H. (2020) · Journal of Materials Chemistry B · doi:10.1039/d0tb00649a · Cited by 213 · see citing works
New insights into antiangiogenic therapy resistance in cancer: Mechanisms and therapeutic aspects
Huang, M., Lin, Y., Wang, C., Deng, L., Chen, M., Assaraf, Y. G., Chen, Z., Ye, W., & Zhang, D. (2022) · Drug Resistance Updates · doi:10.1016/j.drup.2022.100849 · Cited by 176 · see citing works
Where Metabolism Meets Senescence: Focus on Endothelial Cells
Sabbatinelli, J., Prattichizzo, F., Olivieri, F., Procopio, A. D., Rippo, M. R., & Giuliani, A. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01523 · Cited by 168 · see citing works
Metabolic Fitness and Plasticity in Cancer Progression
McGuirk, S., Audet-Delage, Y., & St‐Pierre, J. (2020) · Trends in cancer · doi:10.1016/j.trecan.2019.11.009 · Cited by 133 · see citing works
Ciccone, V., Terzuoli, E., Donnini, S., Giachetti, A., Morbidelli, L., & Ziche, M. (2018) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-018-0975-0 · Cited by 132 · see citing works
Oxidative stress-induced angiogenesis
Huang, Y., & Nan, G. (2019) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2019.02.019 · Cited by 121 · see citing works
Hypoxia Signaling in Cancer: From Basics to Clinical Practice
Sebestyén, A., Kopper, L., Dankó, T., & Tímár, J. (2021) · Pathology and Oncology Research · doi:10.3389/pore.2021.1609802 · Cited by 110 · see citing works
Starvation and antimetabolic therapy promote cytokine release and recruitment of immune cells
Püschel, F., Favaro, F., Redondo-Pedraza, J., Lucendo, E., Iurlaro, R., Marchetti, S., Majem, B., Eldering, E., Nadal, E., Ricci, J., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1913707117 · Cited by 99 · see citing works
Resistance to Anti-angiogenic Therapies: A Mechanism Depending on the Time of Exposure to the Drugs
Montemagno, C., & Pagès, G. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00584 · Cited by 93 · see citing works
Ocaña, M. C., Martı́nez-Poveda, B., Quesada, A. R., & Medina, M. Á. (2018) · Medicinal Research Reviews · doi:10.1002/med.21511 · Cited by 91 · see citing works
Badraoui, R., Rebaï, T., Elkahoui, S., Alreshidi, M. M., Veettil, V. N., Noumi, E., Al-Motair, K. A., Aouadi, K., Kadri, A., Feo, V. D., et al. (2020) · Antioxidants · doi:10.3390/antiox9101003 · Cited by 63 · see citing works
RAD51 is a potential marker for prognosis and regulates cell proliferation in pancreatic cancer
Zhang, X., Ma, N., Yao, W., Li, S., & Ren, Z. (2019) · Cancer Cell International · doi:10.1186/s12935-019-1077-6 · Cited by 63 · see citing works
Antioxidants stimulate BACH1-dependent tumor angiogenesis
Wang, T., Dong, Y., Huang, Z., Zhang, G., Zhao, Y. H., Yao, H., Hu, J., Tüksammel, E., Cai, H., Liang, N., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci169671 · Cited by 57 · see citing works
Du, Y., Zhang, J., Gong, L., Feng, Z.-Y., Wang, D., Pan, Y., Sun, L., Wen, J., Chen, G., Liang, J., et al. (2021) · Cancer Letters · doi:10.1016/j.canlet.2021.11.031 · Cited by 55 · see citing works
Wang, C., Huang, M., Lin, Y., Zhang, Y., Pan, J., Jiang, C., Cheng, M.-J., Li, S., He, W., Li, Z., et al. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00883-y · Cited by 52 · see citing works
Glycosylation as new pharmacological strategies for diseases associated with excessive angiogenesis
Bousseau, S., Vergori, L., Soleti, R., Lenaers, G., Martínez, M. C., & Andriantsitohaina, R. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.06.003 · Cited by 51 · see citing works
Ye, W.-L., Huang, L., Yang, X., Wan, S., Gan, W.-J., Yang, Y., He, X., Liu, F., Guo, X., Liu, Y.-X., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2406936121 · Cited by 49 · see citing works
Succinate at the Crossroad of Metabolism and Angiogenesis: Roles of SDH, HIF1α and SUCNR1
Atallah, R., Olschewski, A., & Heinemann, Á. (2022) · Biomedicines · doi:10.3390/biomedicines10123089 · Cited by 43 · see citing works
RBM45 reprograms lipid metabolism promoting hepatocellular carcinoma via Rictor and ACSL1/ACSL4
Wang, C., Chen, Z., Yi, Y., Ding, Y., Xu, F., Kang, H., Lin, K., Shu, X., Zhong, Z., Zhang, Z., et al. (2024) · Oncogene · doi:10.1038/s41388-023-02902-4 · Cited by 42 · see citing works
Li, Z., Ning, F., Wang, C., Yu, H., Ma, Q., & Sun, Y. (2021) · Nanoscale · doi:10.1039/d1nr03387e · Cited by 39 · see citing works
The role of angiogenesis in melanoma: Clinical treatments and future expectations
Wu, Z., Bian, Y., Chu, T., Wang, Y., Man, S., Song, Y., & Wang, Z. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.1028647 · Cited by 32 · see citing works
Kong, J., Yao, C., Ding, X., Dong, S., Wu, S., Sun, W., & Zheng, L. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.01080 · Cited by 31 · see citing works
Zhu, T., Xie, P., Gao, Y., Huang, M., Li, X., Zhang, W., Zhou, H., & Liu, Z. (2018) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12803 · Cited by 30 · see citing works
Xu, Y., Zhang, X., Zhou, A., Cheng, C., Chen, K., Zhou, X., Zhang, G., Ding, L., Wu, X., Ge, H., et al. (2022) · Advanced Materials · doi:10.1002/adma.202207384 · Cited by 25 · see citing works
Ferreira, R. C., Batista, T. M., Duarte, S. S., Silva, D. K. F., Lisboa, T. M. H., Cavalcanti, R. F. P., Leite, F. C., Mangueira, V. M., de Sousa, T. K. G., de Abrantes, R. A., et al. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110247 · Cited by 24 · see citing works
Wang, X., Wang, S., Mu, H.-X., Xu, K.-Y., Wang, X., Shi, J.-T., Cui, Q.-H., Zhang, L., & Chen, S. (2022) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2022.114821 · Cited by 24 · see citing works
In vitro angiogenesis inhibition with selective compounds targeting the key glycolytic enzyme PFKFB3
Abdali, A., Baci, D., Damiani, I., Belloni, F., Dominicis, C. D., Gelmi, M. L., Corsini, A., & Bellosta, S. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105592 · Cited by 23 · see citing works
lncRNA SYTL5-OT4 promotes vessel co-option by inhibiting the autophagic degradation of ASCT2
Wen, Q., Huang, M., Xie, J., Liu, R., Miao, Q., Huang, J., Zhang, J., Lyu, W.-Y., Qi, M., Wu, C., et al. (2023) · Drug Resistance Updates · doi:10.1016/j.drup.2023.100975 · Cited by 21 · see citing works
Neovascularization directed by CAVIN1/CCBE1/VEGFC confers TMZ-resistance in glioblastoma
Wang, M., Xia, D., Xu, D., Yin, Y., Xu, F., Zhang, B., Li, K., Yang, Z., & Zou, J. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216593 · Cited by 21 · see citing works
Armani, G., Pozzi, E., Pagani, A., Porta, C., Rizzo, M., Cicognini, D., Rovati, B., Moccia, F. D., Pedrazzoli, P., & Ferraris, E. (2021) · Microvascular Research · doi:10.1016/j.mvr.2021.104189 · Cited by 21 · see citing works
Biomechanical forces and force-triggered drug delivery in tumor neovascularization
Wendong, Y., Jiali, J., Fan, Q., Yayun, W., Xie, X., Zheng, S., & Huang, W. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.116117 · Cited by 19 · see citing works
Ornell, K. J., Mistretta, K. S., Newman, E. A., Ralston, C. Q., & Coburn, J. M. (2019) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.9b01267 · Cited by 18 · see citing works
Zhang, F., Wang, B., Zhang, W., Xu, Y., Zhang, C., & Xue, X. (2024) · Current Cancer Drug Targets · doi:10.2174/0115680096265896231226062212 · Cited by 16 · see citing works
Heat‐Shock protein A12A is a novel PCNA‐binding protein and promotes hepatocellular carcinoma growth
Cheng, H., Cao, X., Min, X., Zhang, X., Kong, Q., Mao, Q., Li, R., Xue, B., Fang, L., Liu, L., et al. (2020) · FEBS Journal · doi:10.1111/febs.15276 · Cited by 16 · see citing works
Role and mechanisms of exercise therapy in enhancing drug treatment for glioma: a review
Guanghui, W., Chen, Y., Chen, C., Liu, J., Wu, Q., Zhang, Y., Chen, R., Xiao, J., Su, Y., Shi, H., et al. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1576283 · Cited by 15 · see citing works
NSD1 promotes esophageal cancer tumorigenesis via HIF1α signaling
He, F., Xiao, H., Cai, Y., & Zhang, N. (2022) · Cell Biology and Toxicology · doi:10.1007/s10565-022-09786-2 · Cited by 14 · see citing works
Bosch‐Barrera, J., Verdura, S., Ruffinelli, J. C., Carcereny, E., Sais, È., Cuyàs, E., Palmero, R., López‐Bonet, E., Hernández, A., Oliveras, G., et al. (2021) · Cancers · doi:10.3390/cancers13164168 · Cited by 14 · see citing works
Li, G., He, Y., Liu, H., Liu, D., Chen, L., Luo, Y., Chen, L., Qi, L., Wang, Y., Wang, Y., et al. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-04953-z · Cited by 13 · see citing works
Ruzzo, A., Graziano, F., Bagaloni, I., Bartolomeo, M. D., Prisciandaro, M., Aprile, G., Ongaro, E., Vincenzi, B., Perrone, G., Santini, D., et al. (2020) · Gastric Cancer · doi:10.1007/s10120-020-01078-0 · Cited by 13 · see citing works
Iqbal, M. A., Siddiqui, S., Smith, K., Singh, P. K., Kumar, B., Chouaı̈b, S., & Chandrasekaran, S. (2023) · iScience · doi:10.1016/j.isci.2023.108059 · Cited by 12 · see citing works
Chen, Q., Yu, W.-Y., Zhang, H., Zhang, S., Fang, J., Wu, F., Ying, H., & Yu, C.-H. (2020) · BioMed Research International · doi:10.1155/2020/8954513 · Cited by 11 · see citing works
Gao, S., Wang, Y., Xu, Y., & Liu, S. (2023) · Journal of Personalized Medicine · doi:10.3390/jpm13030513 · Cited by 10 · see citing works
Liu, J., Huang, H., Zhang, X., Shen, Y., Jiang, D., Hu, S., Li, S., Yan, Z., Hu, W., Luo, J., et al. (2025) · Research · doi:10.34133/research.0698 · Cited by 10 · see citing works
Buckley, A. M., Dunne, M. R., Morrissey, M. E., Kennedy, S. A., Nolan, A. A., Davern, M., Foley, E. K., Clarke, N. E., Lysaght, J., Ravi, N., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-68777-7 · Cited by 10 · see citing works
Chen, R., Yang, X., Li, L., Zhao, H., Huang, G., & Liu, J. (2024) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-024-07029-6 · Cited by 9 · see citing works
Zhang, H., Gan, L., Duan, X., Tuo, B., Zhang, H., Liu, S., Lian, Y., Liu, E., & Sun, Z. (2025) · Journal of Gastroenterology · doi:10.1007/s00535-025-02273-5 · Cited by 8 · see citing works
Klid, S., Algaba‐Chueca, F., Maymó‐Masip, E., Ballesteros, M., Inglés, M., Guarque, A., Vilanova, N., Prats, A., Kulovic‐Sissawo, A., Weiß, E., et al. (2025) · The Journal of Physiology · doi:10.1113/jp288010 · Cited by 7 · see citing works
The role and mechanisms of the HIF-1 signaling pathway in LC-COPD
Zheng, Y., & Qian, J. (2025) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-025-06373-w · Cited by 6 · see citing works
Cuproptosis in inflammation and cancer: molecular mechanisms and therapeutic targets
Liu, J., Huang, H., Luo, P., Shen, Y., Hu, S., Zhang, X., Yu, Q., Liu, Y., Huang, L., Luo, J., et al. (2026) · Molecular Cancer · doi:10.1186/s12943-026-02644-3 · Cited by 5 · see citing works
Zeng, T., Wang, Q., Li, L., Tan, X., He, J., Liu, Y., Wang, X., He, R., Ding, G., Zeng, X., et al. (2026) · Drug Resistance Updates · doi:10.1016/j.drup.2026.101413 · Cited by 5 · see citing works
Li, W., Peng, J., He, J., Liao, L., Kang, D., Zhang, W., Wang, W., Wang, R., Wang, S., Liao, Y., et al. (2026) · Cancer Research · doi:10.1158/0008-5472.can-25-3520 · Cited by 4 · see citing works
Vascular disruption agent and phototherapeutic assembled nanoparticles for enhanced tumor inhibition
Pan, T., Tang, Y., Pang, E.-N., Zhao, S., Yao, C., Wang, B., Song, X., & Lan, M. (2023) · Chemical Communications · doi:10.1039/d3cc02647g · Cited by 4 · see citing works
Reciprocal Dynamics of Metabolism and mRNA Translation in Tumor Angiogenesis
Lidonnici, J., & Oberkersch, R. E. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252011284 · Cited by 4 · see citing works
Rai, Y., Singh, S. P., Pandey, S., Sah, D. K., Sah, R. K., Roy, B. G., Dwarakanath, B. S. R., & Bhatt, A. N. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1063531 · Cited by 4 · see citing works
Ornell, K. J., Mistretta, K. S., Ralston, C. Q., & Coburn, J. M. (2020) · Biomaterials Science · doi:10.1039/d0bm01153c · Cited by 3 · see citing works
Marcone, S., Spadavecchia, J., Khan, M., Vella, G., O’Connell, F., Pendino, M., Menon, M. S., Donohoe, C. L., Ravi, N., Reynolds, J. V., et al. (2024) · Cancers · doi:10.3390/cancers16234007 · Cited by 2 · see citing works
A primer on metabolic contributions in tumor angiogenic microenvironment
Ocaña, M. C., Bernal, M., Quesada, A. R., & Medina, M. Á. (2025) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2025.189417 · Cited by 2 · see citing works
Cuproptosis: An Emerging Cell Death Modality for Antitumor Therapy
Han, Y., Zhu, G., Jin, Y., & Li, C. (2025) · ACS Materials Letters · doi:10.1021/acsmaterialslett.5c00711 · Cited by 2 · see citing works
FMO2 Promotes Angiogenesis via Regulation of N‐Acetylornithine
Wang, J., Xu, Y., Wu, X., Li, M., Xiao, C., Fu, Z., Chen, Y., Li, Q., Ruan, Y.-E., Zhao, J., et al. (2025) · Advanced Science · doi:10.1002/advs.202506618 · Cited by 2 · see citing works
Han, X., Peng, Z., Cao, K., & Liang, G. (2026) · APOPTOSIS · doi:10.1007/s10495-026-02352-9 · Cited by 2 · see citing works
Endothelial metabolic reprogramming influences tumor immune microenvironment
Chen, M., & Chen, Z.-G. (2026) · World Journal of Clinical Oncology · doi:10.5306/wjco.v17.i3.113326 · Cited by 1 · see citing works
Renal coenzyme A (CoA) production from VB5 fuels stem cell proliferation and tumor growth
Miao, T., Liu, Y., Qadiri, M., Dasseux, A., Asara, J. M., Hu, Y., Sun, X., Pliego-Alcántara, L. D. C., Dibble, C. C., & Perrimon, N. (2026) · Nature Communications · doi:10.1038/s41467-026-71716-1 · Cited by 1 · see citing works
Wang, X. R., Wang, S., Mu, H.-X., Xu, K., Wang, X. T., Shi, J. T., Cui, Q.-H., Zhang, L. W., & Chen, S. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4163279 · Cited by 1 · see citing works
Yu, F., & Tan, Y. (2024) · Research Square · doi:10.21203/rs.3.rs-3996638/v1
Wang, J., Jia, J., Liu, J., Yao, X., & Yuan, Z. (2024) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2024.12488
Xi, Q., Lin, X., Xie, Y., Cheng, F., Hu, B., Zhang, F., Sun, F., Han, B., Lai, Y., Wang, Y., et al. (2025) · Chemical Engineering Journal · doi:10.1016/j.cej.2025.170761
- Authors
- Jiménez-Valerio, G., & Casanovas, O.
- Affiliations
- Institut d'Investigació Biomédica de Bellvitge (ES)
- Corresponding author
- Casanovas, Oriol
- ORCID
- Casanovas, Oriol
- Venue
- Trends in cancer
- Publisher
- Elsevier BV
- Published
- 2017-01
- Volume
- 3
- Issue
- 1
- Pages
- 10-18
- ISSN
- 2405-8025 (ISSN-L)
- 2405-8033
- OpenAlex
- W2562133517
- Cited by
- 68
- References
- 47
- Citations by year
- 2026: 6 · 2025: 9 · 2024: 8 · 2023: 9 · 2022: 9 · 2021: 6 · 2020: 12 · 2019: 5 · 2018: 4
- FWCI
- 0.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Trends in cancer (publishedVersion)
- PubMed (publishedVersion)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, public-domain)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- angiogenesis, cancer metabolism, adaptive resistance, anti-angiogenic therapy, metabolic adaptation, tumor growth, tumor vascularization, cancer therapy resistance
- MeSH terms
- Animals, Hypoxia, Humans, Neoplasms, Neovascularization, Pathologic, Drug Resistance, Neoplasm, Angiogenesis Inhibitors
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review