A Role for p53 in the Adaptation to Glutamine Starvation through the Expression of SLC1A3
Open accessAbstract
Numerous mechanisms to support cells under conditions of transient nutrient starvation have been described. Several functions of the tumor-suppressor protein p53 can contribute to the adaptation of cells to metabolic stress and help cancer cell survival under nutrient-limiting conditions. We show here that p53 promotes the expression of SLC1A3, an aspartate/glutamate transporter that allows the utilization of aspartate to support cells in the absence of extracellular glutamine. Under glutamine deprivation, SLC1A3 expression maintains electron transport chain and tricarboxylic acid cycle activity, promoting de novo glutamate, glutamine, and nucleotide synthesis to rescue cell viability. Tumor cells with high levels of SLC1A3 expression are resistant to glutamine starvation, and SLC1A3 depletion retards the growth of these cells in vitro and in vivo, suggesting a therapeutic potential for SLC1A3 inhibition.
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SLC1A3, as a crucial effector of p53, supports cell survival and growth in the absence of glutamine.
“Recently, SLC1A3, as a crucial effector of p53, has been shown to support cell survival and growth in the absence of glutamine149.”
From Glutamine reliance in cell metabolism (2020) · cites this paper as [149]
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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Multiplex Genome Engineering Using CRISPR/Cas Systems
Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., et al. (2013) · Science · doi:10.1126/science.1231143 · Cited by 15,339 · see citing works
Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., & Salzberg, S. L. (2013) · Genome Biology · doi:10.1186/gb-2013-14-4-r36 · Cited by 12,668 · see citing works
Trapnell, C., Roberts, A., Goff, L. A., Pertea, G. M., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., & Pachter, L. S. (2012) · Nature Protocols · doi:10.1038/nprot.2012.016 · Cited by 11,930 · see citing works
Glutamate neurotoxicity and diseases of the nervous system
Choi, D. W. (1988) · Neuron · doi:10.1016/0896-6273(88)90162-6 · Cited by 8,152 · see citing works
Improved vectors and genome-wide libraries for CRISPR screening
Sanjana, N. E., Shalem, O., & Zhang, F. (2014) · Nature Methods · doi:10.1038/nmeth.3047 · Cited by 5,239 · see citing works
Blinded by the Light: The Growing Complexity of p53
Vousden, K. H., & Prives, C. (2009) · Cell · doi:10.1016/j.cell.2009.04.037 · Cited by 3,163 · see citing works
Self-citationA role for Wnt signalling in self-renewal of haematopoietic stem cells
Reya, T., Duncan, A. W., Ailles, L., Domen, J., Scherer, D. C., Willert, K., Hintz, L., Nusse, R., & Weissman, I. L. (2003) · Nature · doi:10.1038/nature01593 · Cited by 2,159 · 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
Morgenstern, J. P., & Land, H. (1990) · Nucleic Acids Research · doi:10.1093/nar/18.12.3587 · Cited by 2,099 · see citing works
Wise, D. R., DeBerardinis, R. J., Mancuso, A., Sayed, N., Zhang, X.-Y., Pfeiffer, H. K., Nissim, I., Daikhin, E., Yudkoff, M., McMahon, S. B., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810199105 · Cited by 2,001 · see citing works
Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway
Son, J., Lyssiotis, C. A., Ying, H., Wang, X., Hua, S., Ligorio, M., Perera, R. M., Ferrone, C. R., Mullarky, E., Shyh-Chang, N., et al. (2013) · Nature · doi:10.1038/nature12040 · Cited by 1,990 · see citing works
Rare Structural Variants Disrupt Multiple Genes in Neurodevelopmental Pathways in Schizophrenia
Walsh, T., McClellan, J. M., McCarthy, S. E., Addington, A. M., Pierce, S. B., Cooper, G. M., Nord, A. S., Kusenda, M., Malhotra, D., Bhandari, A., et al. (2008) · Science · doi:10.1126/science.1155174 · Cited by 1,800 · see citing works
Epilepsy and Exacerbation of Brain Injury in Mice Lacking the Glutamate Transporter GLT-1
Tanaka, K., Watase, K., Manabe, T., Yamada, K., Watanabe, M., Takahashi, K., Iwama, H., Nishikawa, T., Ichihara, N., Kikuchi, T., et al. (1997) · Science · doi:10.1126/science.276.5319.1699 · Cited by 1,755 · see citing works
p53 Regulates Mitochondrial Respiration
Matoba, S., Kang, J.-G., Patino, W. D., Wragg, A., Boehm, M., Gavrilova, O., Hurley, P. J., Bunz, F., & Hwang, P. M. (2006) · Science · doi:10.1126/science.1126863 · Cited by 1,650 · see citing works
Birsoy, K., Wang, T., Chen, W. W., Freinkman, E., Abu-Remaileh, M., & Sabatini, D. M. (2015) · Cell · doi:10.1016/j.cell.2015.07.016 · Cited by 1,388 · see citing works
Supporting aspartate biosynthesis is an essential function of respiration in proliferating cells
Sullivan, L. B., Gui, D. Y., Hosios, A. M., Bush, L. N., Freinkman, E., & Vander Heiden, M. G. (2015) · Cell · doi:10.1016/j.cell.2015.07.017 · Cited by 1,173 · see citing works
P53 in survival, death and metabolic health: a lifeguard with a licence to kill.
Kruiswijk, F., Labuschagne, C. F., & Vousden, K. H. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm4007 · Cited by 1,080 · see citing works
Self-citationAntitumor activity of the glutaminase inhibitor CB-839 in triple-negative breast cancer
Gross, M. I., Demo, S. D., Dennison, J. B., Chen, L., Chernov-Rogan, T., Goyal, B., Janes, J. R., Laidig, G. J., Lewis, E. R., Li, J., et al. (2014) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-13-0870 · Cited by 1,068 · see citing works
Serine starvation induces stress and p53-dependent metabolic remodelling in cancer cells
Maddocks, O. D. K., Berkers, C. R., Mason, S. M., Zheng, L., Blyth, K., Gottlieb, E., & Vousden, K. H. (2013) · Nature · doi:10.1038/nature11743 · Cited by 1,007 · see citing works
Self-citationFunctional comparisons of three glutamate transporter subtypes cloned from human motor cortex
Arriza, J. L., Fairman, W. A., Wadiche, J. I., Murdoch, G., Kavanaugh, M. P., & Amara, S. G. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-09-05559.1994 · Cited by 998 · see citing works
Regulation of mammalian nucleotide metabolism and biosynthesis
Lane, A. N., & Fan, T. W.-M. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv047 · Cited by 959 · see citing works
Kamphorst, J. J., Nofal, M., Commisso, C., Hackett, S. R., Lu, W., Grabocka, E., Vander Heiden, M. G., Miller, G., Drebin, J. A., Bar-Sagi, D., et al. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-2211 · Cited by 893 · see citing works
Fisher, S., Barry, A. J., Abreu, J., Minie, B., Nolan, J., Delorey, T. M., Young, G., Fennell, T. J., Allen, A., Ambrogio, L., et al. (2011) · Genome biology · doi:10.1186/gb-2011-12-1-r1 · Cited by 683 · see citing works
Serine, but not glycine, supports one-carbon metabolism and proliferation of cancer cells
Labuschagne, C. F., van den Broek, N. J. F., Mackay, G. M., Vousden, K. H., & Maddocks, O. D. K. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.04.045 · Cited by 576 · see citing works
Self-citationTardito, S., Oudin, A., Ahmed, S. U., Fack, F., Keunen, O., Zheng, L., Miletic, H., Sakariassen, P. Ø., Weinstock, A., Wagner, A., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3272 · Cited by 557 · see citing works
Self-citationMetabolic recycling of ammonia via glutamate dehydrogenase supports breast cancer biomass
Spinelli, J. B., Yoon, H., Ringel, A. E., Jeanfavre, S., Clish, C. B., & Haigis, M. C. (2017) · Science · doi:10.1126/science.aam9305 · Cited by 468 · cited 1× · see citing works
“Cells can produce glutamate directly from a-KG and ammonia (Spinelli et al., 2017) or from a-KG plus other amino acids such as alanine, serine, or aspartate.”
BackgroundAsparagine Plays a Critical Role in Regulating Cellular Adaptation to Glutamine Depletion
Zhang, J., Fan, J., Venneti, S., Cross, J. R., Takagi, T., Bhinder, B., Djaballah, H., Kanai, M., Cheng, E. H., Judkins, A. R., et al. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.08.018 · Cited by 439 · see citing works
Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice
Watase, K., Hashimoto, K., Kano, M., Yamada, K., Watanabe, M., Inoue, Y., Okuyama, S., Sakagawa, T., Ogawa, S., Kawashima, N., et al. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00108.x · Cited by 408 · see citing works
McConnell, B. B., Starborg, M., Brookes, S., & Peters, G. (1998) · Current Biology · doi:10.1016/s0960-9822(98)70137-x · Cited by 314 · see citing works
Cytosolic Aspartate Availability Determines Cell Survival When Glutamine Is Limiting
Alkan, H. F., Walter, K. E., Luengo, A., Madreiter‐Sokolowski, C. T., Stryeck, S., Lau, A. N., Zoughbi, W. A., Lewis, C. A., Thomas, C. J., Höefler, G., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.07.021 · Cited by 205 · see citing works
TIGAR Is Required for Efficient Intestinal Regeneration and Tumorigenesis
Cheung, E. C., Athineos, D., Lee, P., Ridgway, R. A., Lambie, W., Nixon, C., Strathdee, D., Blyth, K., Sansom, O. J., & Vousden, K. H. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.05.001 · Cited by 191 · see citing works
Self-citationVan Nguyen, T., Lee, J. E., Sweredoski, M. J., Yang, S.-J., Jeon, S.-J., Harrison, J. S., Yim, J.-H., Lee, S. G., Handa, H., Kuhlman, B., et al. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.032 · Cited by 177 · cited 1× · see citing works
“GS catalyzes the condensation of glutamate and ammonia into glutamine, and wild-type p53 cells showed a strong stabilization of GS in response to glutamine starvation (Figure S1B), as previously reported (Nguyen et al., 2016).”
ResultKarlsson, R.-M., Tanaka, K., Saksida, L. M., Bussey, T. J., Heilig, M., & Holmes, A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.215 · Cited by 165 · see citing works
The B55α Subunit of PP2A Drives a p53-Dependent Metabolic Adaptation to Glutamine Deprivation
Reid, M. A., Wang, W.-I., Rosales, K. R., Welliver, M. X., Pan, M., & Kong, M. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.02.008 · Cited by 154 · see citing works
Episodic Ataxia Associated With EAAT1 Mutation C186S Affecting Glutamate Reuptake
de Vries, B., Mamsa, H., Stam, A. H., Wan, J., Bakker, S. L. M., Vanmolkot, K. R. J., Haan, J., Terwindt, G. M., Boon, E. M. J., Howard, B. D., et al. (2009) · Archives of Neurology · doi:10.1001/archneurol.2008.535 · Cited by 145 · see citing works
Erichsen, M. N., Huynh, T. H. V., Abrahamsen, B., Bastlund, J. F., Bundgaard, C., Monrad, O., Bekker-Jensen, A., Nielsen, C. W., Frydenvang, K., Jensen, A. A., et al. (2010) · Journal of Medicinal Chemistry · doi:10.1021/jm1009154 · Cited by 121 · see citing works
AGC1/2, the mitochondrial aspartate-glutamate carriers
Amoêdo, N. D., Punzi, G., Obre, É., Lacombe, D., Grassi, A., Pierri, C. L., & Rossignol, R. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2016.04.011 · Cited by 120 · see citing works
Functional interplay between MDM2, p63/p73 and mutant p53
Stindt, M., Muller, P. A. J., Ludwig, R., Kehrloesser, S., Dötsch, V., & Vousden, K. H. (2014) · Oncogene · doi:10.1038/onc.2014.359 · Cited by 109 · see citing works
Self-citationByun, J., Choi, Y., Kim, J. H., Jeong, J. Y., Jeon, H., Kim, M. K., Hwang, I., Lee, S.-Y., Lee, Y. M., Lee, I., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.06.066 · Cited by 84 · see citing works
Tran, T. Q., Lowman, X. H., Reid, M. A., Mendez‐Dorantes, C., Pan, M., Yang, Y., & Kong, M. (2016) · Oncogene · doi:10.1038/onc.2016.360 · Cited by 77 · see citing works
Argininosuccinate synthase 1 is an intrinsic Akt repressor transactivated by p53
Miyamoto, T., Lo, P. H. Y., Saichi, N., Ueda, K., Hirata, M., Tanikawa, C., & Matsuda, K. (2017) · Science Advances · doi:10.1126/sciadv.1603204 · Cited by 59 · see citing works
Ralphe, J. C. (2004) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2004.04.008 · Cited by 57 · see citing works
Šerý, O., Sultana, N., Kashem, M. A., Pow, D. V., & Balcar, V. J. (2015) · Neurochemical Research · doi:10.1007/s11064-015-1605-2 · Cited by 53 · see citing works
Glutamate transporter Slc1a3 mediates inter‐niche stem cell activation during skin growth
Reichenbach, B., Classon, J., Aida, T., Tanaka, K., Genander, M., & Göritz, C. (2018) · The EMBO Journal · doi:10.15252/embj.201798280 · Cited by 43 · see citing works
Cetinbas, N. M., Sudderth, J., Harris, R. C., Cebeci, A., Negri, G. L., Yilmaz, Ö. H., DeBerardinis, R. J., & Sorensen, P. H. B. (2016) · Scientific Reports · doi:10.1038/srep32606 · Cited by 42 · see citing works
Stoffel, W., Körner, R., Wachtmann, D., & Keller, B. U. (2004) · Molecular Brain Research · doi:10.1016/j.molbrainres.2004.06.026 · Cited by 39 · see citing works
iRFP is a sensitive marker for cell number and tumor growth in high-throughput systems
Hock, A. K., Lee, P., Maddocks, O. D. K., Mason, S. M., Blyth, K., & Vousden, K. H. (2013) · Cell Cycle · doi:10.4161/cc.26985 · Cited by 36 · see citing works
Self-citationRalphe, J. C., Bedell, K. A., Segar, J. L., & SCHOLZ, T. D. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00991.2004 · Cited by 32 · see citing works
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Yoo, H. C., Yu, Y. C., Sung, Y., & Han, J. M. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-00504-8 · Cited by 1,021 · see citing works
Distinct Regulation of Th17 and Th1 Cell Differentiation by Glutaminase-Dependent Metabolism
Johnson, M. O., Wolf, M. M., Madden, M. Z., Andrejeva, G., Sugiura, A., Contreras, D. C., Maseda, D., Liberti, M. V., Paz, K. G., Kishton, R. J., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.001 · Cited by 702 · see citing works
Amino acid metabolism in health and disease
Ling, Z., Jiang, Y.-F., Ru, J.-N., Lu, J.-H., Ding, B., & Wu, J. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01569-3 · Cited by 574 · see citing works
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Jin, J., Byun, J., Choi, Y., & Park, K. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-00971-9 · Cited by 574 · see citing works
Understanding the complexity of p53 in a new era of tumor suppression
Liu, Y., Su, Z., Tavana, O., & Gu, W. J. (2024) · Cancer Cell · doi:10.1016/j.ccell.2024.04.009 · Cited by 519 · see citing works
New aspects of amino acid metabolism in cancer
Vettore, L. A., Westbrook, R. L., & Tennant, D. A. (2019) · British Journal of Cancer · doi:10.1038/s41416-019-0620-5 · Cited by 503 · 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
Energy metabolism in health and diseases
Liu, H., Wang, S., Wang, J., Guo, X., Song, Y., Fu, K., Gao, Z., Liu, D., He, W., & Yang, L. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02141-x · Cited by 438 · see citing works
Lacroix, M., Riscal, R., Arena, G., Linares, L. K., & Cam, L. L. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.10.002 · Cited by 367 · see citing works
Metabolic communication in the tumour–immune microenvironment
Kao, K., Vilbois, S., Tsai, C., & Ho, P. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-01002-x · Cited by 354 · see citing works
p53, cancer and the immune response
Blagih, J., Buck, M. D., & Vousden, K. H. (2020) · Journal of Cell Science · doi:10.1242/jcs.237453 · Cited by 333 · see citing works
Self-citationp53 and Tumor Suppression: It Takes a Network
Boutelle, A. M., & Attardi, L. D. (2021) · Trends in Cell Biology · doi:10.1016/j.tcb.2020.12.011 · Cited by 322 · see citing works
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Chen, X., Ling, H., Hao, Q., & Zhou, X. Y. (2023) · Cell Death and Differentiation · doi:10.1038/s41418-023-01125-0 · Cited by 280 · see citing works
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Liu, Y., & Gu, W. J. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.03.010 · Cited by 260 · see citing works
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Chen, J., Cui, L., Lu, S., & Xu, S. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06435-w · Cited by 268 · see citing works
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Ritterhoff, J., Young, S., Villet, O. M., Shao, D., Neto, F. C., Bettcher, L., Hsu, Y. A., Kolwicz, S. C., Raftery, D., & Tian, R. (2019) · Circulation Research · doi:10.1161/circresaha.119.315483 · Cited by 229 · see citing works
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Alkan, H. F., Walter, K. E., Luengo, A., Madreiter‐Sokolowski, C. T., Stryeck, S., Lau, A. N., Zoughbi, W. A., Lewis, C. A., Thomas, C. J., Höefler, G., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.07.021 · Cited by 205 · see citing works
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Humpton, T. J., Alagesan, B., DeNicola, G. M., Lu, D., Yordanov, G. N., Leonhardt, C. S., Yao, M. A., Alagesan, P., Zaatari, M. N., Park, Y., et al. (2019) · Cancer Discovery · doi:10.1158/2159-8290.cd-18-1409 · Cited by 198 · see citing works
Self-citationBott, A. J., Shen, J., Tonelli, C., Zhan, L., Sivaram, N., Jiang, Y.-P., Yu, X., Bhatt, V., Chiles, E., Zhong, H., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.09.056 · Cited by 185 · see citing works
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Recouvreux, M. V., Moldenhauer, M. R., Galenkamp, K. M. O., Jung, M., James, B., Zhang, Y., Lowy, A., Bagchi, A., & Commisso, C. (2020) · Journal of Experimental Medicine · doi:10.1084/jem.20200388 · Cited by 181 · see citing works
Adapt and conquer: Metabolic flexibility in cancer growth, invasion and evasion
Kreuzaler, P. A., Panina, Y., Segal, J., & Yuneva, M. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.08.021 · Cited by 151 · see citing works
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Boukalová, Š., Hubáčková, S., Milošević, M., Ezrova, Z., Neužil, J., & Rohlena, J. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2020.165759 · Cited by 165 · see citing works
Exploring the multiple roles of guardian of the genome: P53
Feroz, W., & Sheikh, A. M. A. (2020) · Egyptian Journal of Medical Human Genetics · doi:10.1186/s43042-020-00089-x · Cited by 161 · see citing works
Wei, F., Wang, D., Wei, J., Tang, N., Tang, L. M., Xiong, F., Guo, C. J., Zhou, M., Li, X., Li, G., et al. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03581-0 · Cited by 128 · see citing works
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Vaghari‐Tabari, M., Ferns, G. A., Qujeq, D., Andevari, A. N., Sabahi, Z., & Moein, S. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.30276 · Cited by 117 · see citing works
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Lee, P., Malik, D. M., Perkons, N. R., Huangyang, P., Khare, S., Rhoades, S. D., Gong, Y.-Y., Burrows, M., Finan, J. M., Nissim, I., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14374-1 · Cited by 101 · see citing works
Gabra, M. B. I., Yang, Y., Li, H., Senapati, P., Hanse, E. A., Lowman, X. H., Tran, T. Q., Zhang, L., Doan, L. T., Xu, X., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17181-w · Cited by 99 · see citing works
Pi, M., Kuang, H., Yue, C., Yang, Q., Wu, A., Li, Y., Assaraf, Y. G., Yang, D., & Wu, S. (2022) · Drug Resistance Updates · doi:10.1016/j.drup.2022.100822 · Cited by 98 · see citing works
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Natarajan, S. K., & Venneti, S. (2019) · Cancers · doi:10.3390/cancers11111628 · Cited by 96 · see citing works
Defining a metabolic landscape of tumours: genome meets metabolism
Nanda, C. S., Venkateswaran, S. V., Patani, N., & Yuneva, M. O. (2019) · British Journal of Cancer · doi:10.1038/s41416-019-0663-7 · Cited by 94 · see citing works
Glutamine addiction in tumor cell: oncogene regulation and clinical treatment
Li, X., Peng, X., Li, Y., Wei, S., He, G., Liu, J., Li, X., Yang, S., Dai, L., Lin, W., et al. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-023-01449-x · Cited by 99 · see citing works
Yuan, M., Tu, B., Li, H., Pang, H., Zhang, N., Fan, M., Bai, J., Wang, W., Shu, Z., DuFort, C. C., et al. (2022) · Nature Cancer · doi:10.1038/s43018-022-00426-6 · Cited by 96 · see citing works
Wang, R., Cao, L., Thorne, R. F., Zhang, X. D., Li, J., Shao, F., Zhang, L., & Wu, M. (2021) · Science Advances · doi:10.1126/sciadv.abe5708 · Cited by 93 · see citing works
Kaymak, I., Maier, C. R., Schmitz, W., Campbell, A. D., Dankworth, B., Ade, C. P., Walz, S., Paauwe, M., Kalogirou, C., Marouf, H., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-19-0650 · Cited by 88 · see citing works
Advancing Cancer Treatment by Targeting Glutamine Metabolism—A Roadmap
Halama, A., & Suhre, K. (2022) · Cancers · doi:10.3390/cancers14030553 · Cited by 92 · see citing works
Li, J., Ye, Y., Liu, Z., Zhang, G., Dai, H., Li, J., Zhou, B., Li, Y., Zhao, Q., Huang, J., et al. (2022) · Nature Cancer · doi:10.1038/s43018-022-00354-5 · Cited by 87 · see citing works
Targeting extracellular nutrient dependencies of cancer cells
García‐Bermúdez, J., Williams, R. T., Guarecuco, R., & Birsoy, K. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.11.011 · Cited by 87 · see citing works
Li, M., Thorne, R. F., Shi, R., Zhang, X. D., Li, J., Li, J., Zhang, Q., Wu, M., & Liu, L. (2021) · Advanced Science · doi:10.1002/advs.202003732 · Cited by 81 · see citing works
Zhou, Q., Lin, W., Wang, C., Sun, F., Ju, S., Chen, Q., Wang, Y., Chen, Y., Li, H., Wang, L., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30559-2 · Cited by 80 · see citing works
Sestrins at the Interface of ROS Control and Autophagy Regulation in Health and Disease
Cordani, M., Sánchez‐Álvarez, M., Strippoli, R., Bazhin, A. V., & Donadelli, M. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/1283075 · Cited by 75 · see citing works
Liao, Q., Deng, J., Tong, J., Gan, Y., Hong, W., Dong, H., Cao, M., Chen, X., Chen, Y., Xie, B., et al. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.11.013 · Cited by 79 · see citing works
Xu, R., Yang, J., Ren, B., Wang, H., Yang, G., Chen, Y., You, L., & Zhao, Y. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.572722 · Cited by 70 · see citing works
Yokoyama, Y., Estok, T. M., & Wild, R. (2022) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-22-0282 · Cited by 74 · see citing works
SLC1A3 contributes to L‐asparaginase resistance in solid tumors
Sun, J., Nagel, R., Zaal, E. A., Ugalde, A. P., Han, R., Proost, N., Song, J., Pataskar, A., Burylo, A. M., Fu, H., et al. (2019) · The EMBO Journal · doi:10.15252/embj.2019102147 · Cited by 69 · see citing works
Deregulated transcription factors in cancer cell metabolisms and reprogramming
Kant, R., Manne, R., Anas, M., Penugurti, V., Chen, T., Pan, B., Hsu, C.-C., & Lin, H. (2022) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2022.10.001 · Cited by 72 · see citing works
Regulation of Ferroptosis by Amino Acid Metabolism in Cancer
Yang, J., Dai, X., Xu, H., Tang, Q., & Bi, F. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.64982 · Cited by 69 · see citing works
Determinants of nutrient limitation in cancer
Sullivan, M. R., & Heiden, M. G. V. (2019) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2019.1611733 · Cited by 65 · see citing works
Freidman, N., Chen, I., Wu, Q., Briot, C., Holst, J., Font, J. S., Vandenberg, R. J., & Ryan, R. M. (2020) · Neurochemical Research · doi:10.1007/s11064-019-02934-x · Cited by 67 · see citing works
RETRACTED: SLC1A3 promotes gastric cancer progression via the PI3K/AKT signalling pathway
Xu, L., Chen, J., Jia, L., Chen, X., Moumin, F. A., & Cai, J. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.16060 · Cited by 64 · see citing works
Retractedp53‐mediated adaptation to serine starvation is retained by a common tumour‐derived mutant
Humpton, T. J., Hock, A. K., Maddocks, O. D. K., & Vousden, K. H. (2018) · Cancer & Metabolism · doi:10.1186/s40170-018-0191-6 · Cited by 58 · see citing works
Self-citationThe p53 Pathway and Metabolism: The Tree That Hides the Forest
Lahalle, A., Lacroix, M., Blasio, C. D., Cissé, M. Y., Linares, L. K., & Cam, L. L. (2021) · Cancers · doi:10.3390/cancers13010133 · Cited by 61 · see citing works
Wu, S., Guo, B., Zhang, L., Zhu, X., Zhao, P., Deng, J., Zheng, J., Li, F., Wang, Y., Zhang, S., et al. (2022) · Oncogene · doi:10.1038/s41388-022-02229-6 · Cited by 60 · see citing works
Context is everything: extrinsic signalling and gain-of-function p53 mutants
Amelio, I., & Melino, G. (2020) · Cell Death Discovery · doi:10.1038/s41420-020-0251-x · Cited by 59 · see citing works
A PROTAC‐Based Cuproptosis Sensitizer in Lung Cancer Therapy
Wang, Y., Yao, X., Lu, Y., Ruan, J., Yang, Z., Wang, C., Yang, N., Gao, Y., & Shi, S. (2025) · Advanced Materials · doi:10.1002/adma.202501435 · Cited by 56 · see citing works
Mutant p53 in cell-cell interactionsPreprint
Pilley, S. E., Rodríguez, T. A., & Vousden, K. H. (2021) · Genes & Development · doi:10.1101/gad.347542.120 · Cited by 54 · see citing works
Self-citationSupply and demand: Cellular nutrient uptake and exchange in cancer
Papalazarou, V., & Maddocks, O. D. K. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.08.026 · Cited by 52 · see citing works
He, W., Hu, Y., Chen, D., Li, Y., Ye, D., Zhao, Q., Li, L., Shi, X., Lu, L., Yin, Z., et al. (2022) · Clinical and Translational Medicine · doi:10.1002/ctm2.800 · Cited by 53 · see citing works
Sestrins as a Therapeutic Bridge between ROS and Autophagy in Cancer
Sánchez-Álvarez, M., Strippoli, R., Donadelli, M., Bazhin, A., & Cordani, M. (2019) · Cancers · doi:10.3390/cancers11101415 · Cited by 49 · see citing works
Glutamine Metabolism in Cancer Stem Cells: A Complex Liaison in the Tumor Microenvironment
Pacifico, F., Leonardi, A., & Crescenzi, E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032337 · Cited by 52 · see citing works
Transporters at the Interface between Cytosolic and Mitochondrial Amino Acid Metabolism
Hewton, K. G., Johal, A. S., & Parker, S. J. (2021) · Metabolites · doi:10.3390/metabo11020112 · Cited by 49 · see citing works
The emerging relationship between metabolism and DNA repair
Cucchi, D., Gibson, A., & Martin, S. A. (2021) · Cell Cycle · doi:10.1080/15384101.2021.1912889 · Cited by 48 · see citing works
Contribution of adipocytes in the tumor microenvironment to breast cancer metabolism
Lyu, X., Zhang, Q., Fares, H. M., Wang, Y., Han, Y., & Sun, L. (2022) · Cancer Letters · doi:10.1016/j.canlet.2022.215616 · Cited by 48 · see citing works
Helenius, I. T., Madala, H. R., & Yeh, J.-R. J. (2021) · Biomolecules · doi:10.3390/biom11111666 · Cited by 43 · see citing works
A CRISPRi/a screening platform to study cellular nutrient transport in diverse microenvironments
Chidley, C., Darnell, A. M., Gaudio, B. L., Lien, E. C., Barbeau, A. M., Heiden, M. G. V., & Sorger, P. K. (2024) · Nature Cell Biology · doi:10.1038/s41556-024-01402-1 · Cited by 45 · see citing works
Lactic acidosis induces resistance to the pan-Akt inhibitor uprosertib in colon cancer cells
Barnes, E., Xu, Y., Benito, A., Herendi, L., Siskos, A., Aboagye, E. O., Nijhuis, A. M., & Keun, H. C. (2020) · British Journal of Cancer · doi:10.1038/s41416-020-0777-y · Cited by 47 · see citing works
Emerging Roles of the Tumor Suppressor p53 in Metabolism
Yu, L., Wu, M. Y., Zhu, G., & Xu, Y. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.762742 · Cited by 46 · see citing works
Selective advantage of epigenetically disrupted cancer cells via phenotypic inertia
Loukas, I., Simeoni, F., Milan, M., Inglese, P., Patel, H., Goldstone, R. J., East, P., Strohbuecker, S., Mitter, R., Talsania, B., et al. (2022) · Cancer Cell · doi:10.1016/j.ccell.2022.10.002 · Cited by 46 · see citing works
Nutrient transporters: connecting cancer metabolism to therapeutic opportunities
Nwosu, Z. C., Song, M. G., di Magliano, M. P., Lyssiotis, C. A., & Kim, S. E. (2023) · Oncogene · doi:10.1038/s41388-023-02593-x · Cited by 47 · see citing works
Zheng, L., Liu, C., & Yu, K. (2023) · Journal of Hematology & Oncology · doi:10.1186/s13045-023-01522-5 · Cited by 45 · see citing works
Restall, I. J., Cseh, O., Richards, L. M., Pugh, T. J., Luchman, H. A., & Weiss, S. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-3923 · Cited by 42 · see citing works
The crisscross between p53 and metabolism in cancer
Mao, Y., & Jiang, P. (2023) · Acta Biochimica et Biophysica Sinica · doi:10.3724/abbs.2023109 · Cited by 43 · see citing works
Harnessing the Co-vulnerabilities of Amino Acid-Restricted Cancers
Pathria, G., & Ronai, Z. A. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2020.12.009 · Cited by 42 · see citing works
Linder, S. J., Bernasocchi, T., Martínez-Pastor, B., Sullivan, K. D., Galbraith, M. D., Lewis, C. A., Ferrer, C. M., Boon, R., da Silveira, G. G., Cho, H. M., et al. (2023) · Nature Metabolism · doi:10.1038/s42255-023-00919-3 · Cited by 40 · see citing works
Fan, Y., Xue, H., Li, Z., Huo, M., Gao, H., & Guan, X. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2024.1345522 · Cited by 40 · see citing works
Humpton, T. J., Hall, H., Kiourtis, C., Nixon, C., Clark, W. A., Hedley, A., Shaw, R., Bird, T. G., Blyth, K., & Vousden, K. H. (2021) · Cell Death and Differentiation · doi:10.1038/s41418-021-00871-3 · Cited by 40 · see citing works
Self-citationSun, H.-W., Wu, W., Chen, H., Xu, Y.-T., Yang, Y., Chen, J., Yu, X.-J., Wang, Z., Shuang, Z., & Zheng, L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.616367 · Cited by 40 · see citing works
Malic enzyme 2 maintains protein stability of mutant p53 through 2-hydroxyglutarate
Zhao, M., Yao, P., Mao, Y., Wu, J., Wang, W., Geng, C., Cheng, J., Du, W., & Jiang, P. (2022) · Nature Metabolism · doi:10.1038/s42255-022-00532-w · Cited by 40 · see citing works
Hsu, D. J., Gao, J., Yamaguchi, N., Pinzaru, A. M., Wu, Q., Nandan, M. O., Liberti, M. V., Heissel, S., Alwaseem, H., Tavazoie, S., et al. (2023) · Science Advances · doi:10.1126/sciadv.ade9120 · Cited by 39 · see citing works
Ingaramo, M., Sánchez, J. A., Perrimon, N., & Dekanty, A. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108321 · Cited by 39 · see citing works
Metabolic regulation by p53: Implications for cancer therapy
Koo, K. Y., Moon, K., He, S., & Lee, M.-S. (2025) · Molecules and Cells · doi:10.1016/j.mocell.2025.100198 · Cited by 40 · see citing works
Tackling cuproptosis: from metabolic rewiring to therapeutic exploitation in cancer
Hao, Q., Gan, Y., & Zhou, X. (2026) · Cellular and Molecular Immunology · doi:10.1038/s41423-026-01387-x · Cited by 40 · see citing works
Han, Y., Pu, Y., Liu, X., Liu, Z., Chen, Y., Tang, L., Zhou, J., Song, Q., & Ji, Q. (2024) · Cancer Letters · doi:10.1016/j.canlet.2024.217186 · Cited by 36 · see citing works
Hashimoto, N., Nagano, H., & Tanaka, T. (2019) · Endocrine Journal · doi:10.1507/endocrj.ej18-0565 · Cited by 35 · see citing works
Cell Intrinsic and Systemic Metabolism in Tumor Immunity and Immunotherapy
Coleman, M. F., Cozzo, A. J., Pfeil, A. J., Etigunta, S. K., & Hursting, S. D. (2020) · Cancers · doi:10.3390/cancers12040852 · Cited by 37 · see citing works
Glutamine promotes escape from therapy-induced senescence in tumor cells
Pacifico, F., Badolati, N., Mellone, S., Stornaiuolo, M., Leonardi, A., & Crescenzi, E. (2021) · Aging · doi:10.18632/aging.203495 · Cited by 36 · see citing works
Non-Coding RNAs as Key Regulators of Glutaminolysis in Cancer
Ortiz-Pedraza, Y., Muñoz-Bello, J. O., Olmedo‐Nieva, L., Contreras‐Paredes, A., Martínez-Ramírez, I., Langley, E., & Lizano, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082872 · Cited by 34 · see citing works
Take Advantage of Glutamine Anaplerosis, the Kernel of the Metabolic Rewiring in Malignant Gliomas
Martins, F., Gonçalves, L. G., Pojo, M., & Serpa, J. (2020) · Biomolecules · doi:10.3390/biom10101370 · Cited by 35 · see citing works
The role of autophagy in colorectal cancer: Impact on pathogenesis and implications in therapy
Mahgoub, E., Taneera, J., Sulaiman, N. D., & Saber-Ayad, M. M. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.959348 · Cited by 34 · see citing works
Kong, Y., Wu, M., Wan, X., Sun, M., Zhang, Y., Wu, Z., Li, C., Liang, X., Gao, L., Ma, C., et al. (2023) · Redox Biology · doi:10.1016/j.redox.2023.102732 · Cited by 35 · see citing works
Immunosurveillance encounters cancer metabolism
Chuang, Y., Tzeng, S., Ho, P., & Tsai, C. (2024) · EMBO Reports · doi:10.1038/s44319-023-00038-w · Cited by 34 · see citing works
Cellular metabolism in pancreatic cancer as a tool for prognosis and treatment (Review)
Zuzčák, M., & Trnka, J. (2022) · International Journal of Oncology · doi:10.3892/ijo.2022.5383 · Cited by 33 · see citing works
Chen, C., Ye, L., Yi, J., Liu, T., & Li, Z. (2023) · Breast Cancer Research and Treatment · doi:10.1007/s10549-023-07032-9 · Cited by 30 · see citing works
Lemberg, K. M., Zhao, L., Wu, Y., Veeravalli, V., Alt, J., Aguilar, J. M. H., Dash, R. P., Lam, J., Tenora, L., Rodriguez, C., et al. (2019) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-19-0319 · Cited by 30 · see citing works
Li, G., Zhou, X., Jiang, W., Wu, P., Liu, Y., Jiang, J., Kuang, S., Tang, L. Y., Shi, H.-Q., & Feng, L. (2020) · Aquaculture Research · doi:10.1111/are.14777 · Cited by 30 · see citing works
Fan, H., Wang, K., Zhao, X., Song, B., Yao, T., Liu, T., Gao, G., Lu, W., & Liu, C. (2024) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2024.1335122 · Cited by 31 · see citing works
SLC1A3 facilitates Newcastle disease virus replication by regulating glutamine catabolism
Liu, P.-R., Tang, N., Meng, C., Yin, Y.-C., Qiu, X., Tan, L., Sun, Y.-J., Song, C.-P., Liu, W., Liao, Y., et al. (2022) · Virulence · doi:10.1080/21505594.2022.2112821 · Cited by 25 · see citing works
PRMT1 promotes Warburg effect by regulating the PKM2/PKM1 ratio in non-small cell lung cancer
Lu, P., Zhao, Y., Tan, J., Hou, J., Jin, X., Liu, D., Huang, B., & Lü, J. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06898-x · Cited by 28 · see citing works
Wang, C., Wang, Z., Liu, W., & Ai, Z. (2019) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2019.02.023 · Cited by 28 · see citing works
- Authors
- Tajan, M., Hock, A. K., Blagih, J., Robertson, N. A., Labuschagne, C. F., Kruiswijk, F., Humpton, T. J., Adams, P. D., & Vousden, K. H.
- Affiliations
- The Francis Crick Institute (GB)
- Cancer Research UK Scotland Institute (GB)
- University of Glasgow (GB)
- Sanford Burnham Prebys Medical Discovery Institute (US)
- Corresponding author
- Vousden, Karen H.
- ORCID
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2018-11
- Volume
- 28
- Issue
- 5
- Pages
- 721-736.e6
- ISSN
- 1550-4131 (ISSN-L)
- PMC
- PMC6224545
- OpenAlex
- W2885597648
- Cited by
- 230
- References
- 49
- Citations by year
- 2026: 19 · 2025: 21 · 2024: 31 · 2023: 29 · 2022: 40 · 2021: 26 · 2020: 35 · 2019: 24 · 2018: 4
- FWCI
- 6.73
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell Metabolism (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- Wellcome Trust
- Cancer Research UK (C10652/A16566, C596/A10419, C596/A26855, WO/2017/144877)
- Medical Research Council
- Francis Crick Institute
- Astex Pharmaceuticals
- European Research Council (322842-METABOp53)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- p53, GLAST, glutamine starvation, glutamate synthesis, nucleotide synthesis, electron transport chain, TCA cycle, metabolic stress, tumor cell survival, cancer therapy
- MeSH terms
- Adaptation, Physiological, Animals, Cell Survival, Citric Acid Cycle, Female, Glutamine, Humans, Mice, Inbred BALB C, Neoplasms, Starvation, Tumor Suppressor Protein p53, Excitatory Amino Acid Transporter 1, Cell Line, Tumor
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