{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,27]],"date-time":"2026-10-27T08:29:58Z","timestamp":1793089798213,"version":"4.5.0"},"reference-count":57,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2022,1,23]],"date-time":"2022-01-23T00:00:00Z","timestamp":1642896000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002661","name":"Fund for Scientific Research","doi-asserted-by":"publisher","award":["Research Director, Research Associate and Televie grants"],"award-info":[{"award-number":["Research Director, Research Associate and Televie grants"]}],"id":[{"id":"10.13039\/501100002661","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002661","name":"Fund for Scientific Research","doi-asserted-by":"publisher","award":["FNRS T.0030.21-P"],"award-info":[{"award-number":["FNRS T.0030.21-P"]}],"id":[{"id":"10.13039\/501100002661","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002661","name":"Fund for Scientific Research","doi-asserted-by":"publisher","award":["EOS : program no. 30770923"],"award-info":[{"award-number":["EOS : program no. 30770923"]}],"id":[{"id":"10.13039\/501100002661","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Patronage from the 'Pharmacies Servais'","award":["Study of the links between obesity and breast cancer"],"award-info":[{"award-number":["Study of the links between obesity and breast cancer"]}]},{"name":"Actions de Recherches concert\u00e9es-Communaut\u00e9 Fran\u00e7aise de Belgique","award":["ARC19\/24-096"],"award-info":[{"award-number":["ARC19\/24-096"]}]},{"name":"Walloon Excellence in Lifesciences and Biotechnology","award":["WELBIO-CR-2019C-02R"],"award-info":[{"award-number":["WELBIO-CR-2019C-02R"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cancers"],"abstract":"<jats:p>Obesity is characterized by an excessive fat mass accumulation associated with multiple disorders, including impaired glucose homeostasis, altered adipokine levels, and hyperlipidemia. Despite clear associations between tumor progression and obesity, the effects of these disorders on tumor metabolism remain largely unknown. Thus, we studied the metabolic differences between tumors of obese and lean mice in murine models of triple-negative breast cancer (E0771 and PY8819). For this purpose, a real-time hyperpolarized 1-13C-pyruvate-to-lactate conversion was studied before and after glucose administration in fasting mice. This work was completed by U-13C glucose tracing experiments using nuclear magnetic resonance (NMR) spectroscopy, as well as mass spectrometry (MS). Ex vivo analyses included immunostainings of major lipid, glucose, and monocarboxylic acids transporters. On the one hand, we discovered that tumors of obese mice yield higher lactate\/pyruvate ratios after glucose administration. On the other hand, we found that the same tumors produce higher levels of lactate and alanine from glucose than tumors from lean mice, while no differences on the expression of key transporters associated with glycolysis (i.e., GLUT1, MCT1, MCT4) have been observed. In conclusion, our data suggests that breast tumor metabolism is regulated by the host\u2019s physiological status, such as obesity and diabetes.<\/jats:p>","DOI":"10.3390\/cancers14030562","type":"journal-article","created":{"date-parts":[[2022,1,23]],"date-time":"2022-01-23T20:32:52Z","timestamp":1642969972000},"page":"562","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Tumor Metabolism Is Affected by Obesity in Preclinical Models of Triple-Negative Breast Cancer"],"prefix":"10.3390","volume":"14","author":[{"given":"Caner","family":"Yelek","sequence":"first","affiliation":[{"name":"Biomedical Magnetic Resonance Research Group, Louvain Drug Research Institute, Universit\u00e9 Catholique de Louvain, UCLouvain, B-1200 Brussels, Belgium"},{"name":"Metabolism and Nutrition Research Group, Louvain Drug Research Institute, Walloon Excellence in Life Sciences and BIOtechnology (WELBIO), Universit\u00e9 Catholique de Louvain, UCLouvain, B-1200 Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9426-8600","authenticated-orcid":false,"given":"Lionel","family":"Mignion","sequence":"additional","affiliation":[{"name":"Biomedical Magnetic Resonance Research Group, Louvain Drug Research Institute, Universit\u00e9 Catholique de Louvain, UCLouvain, B-1200 Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4784-3510","authenticated-orcid":false,"given":"Adrien","family":"Paquot","sequence":"additional","affiliation":[{"name":"Bioanalysis and Pharmacology of Bioactive Lipids Research Group, Louvain Drug Research Institute, Universit\u00e9 Catholique de Louvain, UCLouvain, B-1200 Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0694-1947","authenticated-orcid":false,"given":"Caroline","family":"Bouzin","sequence":"additional","affiliation":[{"name":"IREC Imaging Platform, Institut de Recherche Exp\u00e9rimentale et Clinique, Universit\u00e9 Catholique de Louvain, UCLouvain, B-1200 Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8795-9131","authenticated-orcid":false,"given":"Cyril","family":"Corbet","sequence":"additional","affiliation":[{"name":"Pole of Pharmacology and Therapeutics, Institut de Recherche Exp\u00e9rimentale et Clinique, Universit\u00e9 Catholique de Louvain, UCLouvain, B-1200 Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1600-9259","authenticated-orcid":false,"given":"Giulio G.","family":"Muccioli","sequence":"additional","affiliation":[{"name":"Bioanalysis and Pharmacology of Bioactive Lipids Research Group, Louvain Drug Research Institute, Universit\u00e9 Catholique de Louvain, UCLouvain, B-1200 Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2040-2448","authenticated-orcid":false,"given":"Patrice D.","family":"Cani","sequence":"additional","affiliation":[{"name":"Metabolism and Nutrition Research Group, Louvain Drug Research Institute, Walloon Excellence in Life Sciences and BIOtechnology (WELBIO), Universit\u00e9 Catholique de Louvain, UCLouvain, B-1200 Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B\u00e9n\u00e9dicte F.","family":"Jordan","sequence":"additional","affiliation":[{"name":"Biomedical Magnetic Resonance Research Group, Louvain Drug Research Institute, Universit\u00e9 Catholique de Louvain, UCLouvain, B-1200 Brussels, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,1,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"209","DOI":"10.3322\/caac.21660","article-title":"Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries","volume":"71","author":"Sung","year":"2021","journal-title":"CA Cancer J. Clin."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1038\/s41572-019-0111-2","article-title":"Breast cancer","volume":"5","author":"Harbeck","year":"2019","journal-title":"Nat. Rev. Dis. Primers"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"378","DOI":"10.3322\/caac.21405","article-title":"Obesity and adverse breast cancer risk and outcome: Mechanistic insights and strategies for intervention","volume":"67","author":"Friedman","year":"2017","journal-title":"CA Cancer J. Clin."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.breast.2019.07.003","article-title":"BMI is an independent prognostic factor for late outcome in patients diagnosed with early breast cancer: A landmark survival analysis","volume":"47","author":"Vernaci","year":"2019","journal-title":"Breast"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1056\/NEJM196304042681404","article-title":"Plasma free fatty acid concentrations in obesity","volume":"268","author":"Opie","year":"1963","journal-title":"N. Engl. J. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1111\/j.0954-6820.1969.tb07347.x","article-title":"Plasma free fatty acid turnover rate in obesity","volume":"185","author":"Bjorntorp","year":"1969","journal-title":"Acta Med. Scand."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1168","DOI":"10.1172\/JCI113997","article-title":"Influence of body fat distribution on free fatty acid metabolism in obesity","volume":"83","author":"Jensen","year":"1989","journal-title":"J. Clin. Investig."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1097\/MED.0b013e3283444b09","article-title":"Obesity, insulin resistance and free fatty acids","volume":"18","author":"Boden","year":"2011","journal-title":"Curr. Opin. Endocrinol. Diabetes Obes."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1097\/MCO.0000000000000381","article-title":"Emerging roles of lipid metabolism in cancer progression","volume":"20","author":"Corbet","year":"2017","journal-title":"Curr. Opin. Clin. Nutr. Metab. Care"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1533","DOI":"10.1016\/j.bbalip.2013.02.010","article-title":"Adipose tissue and adipocytes support tumorigenesis and metastasis","volume":"1831","author":"Nieman","year":"2013","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1038\/nrendo.2014.94","article-title":"Obesity and cancer--mechanisms underlying tumour progression and recurrence","volume":"10","author":"Park","year":"2014","journal-title":"Nat. Rev. Endocrinol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2455","DOI":"10.1158\/0008-5472.CAN-10-3323","article-title":"Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion","volume":"71","author":"Dirat","year":"2011","journal-title":"Cancer Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s40170-016-0163-7","article-title":"Adipocyte lipolysis links obesity to breast cancer growth: Adipocyte-derived fatty acids drive breast cancer cell proliferation and migration","volume":"5","author":"Balaban","year":"2017","journal-title":"Cancer Metab."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e87489","DOI":"10.1172\/jci.insight.87489","article-title":"Mammary adipocytes stimulate breast cancer invasion through metabolic remodeling of tumor cells","volume":"2","author":"Wang","year":"2017","journal-title":"JCI Insight"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1186\/s12964-018-0221-6","article-title":"Utilization of adipocyte-derived lipids and enhanced intracellular trafficking of fatty acids contribute to breast cancer progression","volume":"16","author":"Yang","year":"2018","journal-title":"Cell Commun. Signal."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1038\/s41580-018-0093-z","article-title":"Adipogenesis and metabolic health","volume":"20","author":"Ghaben","year":"2019","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1017\/S0007114508971282","article-title":"Hypoxia in adipose tissue: A basis for the dysregulation of tissue function in obesity?","volume":"100","author":"Trayhurn","year":"2008","journal-title":"Br. J. Nutr."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1999","DOI":"10.15252\/embj.201696206","article-title":"Adipose tissue: Between the extremes","volume":"36","author":"Vegiopoulos","year":"2017","journal-title":"EMBO J."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1038\/nature05482","article-title":"Mechanisms linking obesity to insulin resistance and type 2 diabetes","volume":"444","author":"Kahn","year":"2006","journal-title":"Nature"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"194","DOI":"10.3109\/03014460.2010.507221","article-title":"A cross-sectional analysis of the associations between adult height, BMI and serum concentrations of IGF-I and IGFBP-1 -2 and -3 in the European Prospective Investigation into Cancer and Nutrition (EPIC)","volume":"38","author":"Crowe","year":"2011","journal-title":"Ann. Hum. Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1038\/s41574-021-00487-0","article-title":"Metabolic pathways in obesity-related breast cancer","volume":"17","author":"Brown","year":"2021","journal-title":"Nat. Rev. Endocrinol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"14195","DOI":"10.1111\/jcmm.16034","article-title":"Acetate: Friend or foe against breast tumour growth in the context of obesity?","volume":"24","author":"Yelek","year":"2020","journal-title":"J. Cell. Mol. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"10233","DOI":"10.1111\/jcmm.15639","article-title":"Obesity and triple-negative-breast-cancer: Is apelin a new key target?","volume":"24","author":"Gourgue","year":"2020","journal-title":"J. Cell. Mol. Med."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"6279","DOI":"10.21873\/anticanres.11223","article-title":"High-fat Diet Enhances Mammary Tumorigenesis and Pulmonary Metastasis and Alters Inflammatory and Angiogenic Profiles in MMTV-PyMT Mice","volume":"36","author":"Sundaram","year":"2016","journal-title":"Anticancer Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"28572","DOI":"10.18632\/oncotarget.25574","article-title":"2\u2019-deoxy-2\u2019-[18F] fluoro-D-glucose positron emission tomography, diffusion-weighted magnetic resonance imaging, and choline spectroscopy to predict the activity of cetuximab in tumor xenografts derived from patients with squamous cell carcinoma of the head and neck","volume":"9","author":"Mignion","year":"2018","journal-title":"Oncotarget"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1934","DOI":"10.1111\/jcmm.14890","article-title":"Metabolic imaging using hyperpolarized (13) C-pyruvate to assess sensitivity to the B-Raf inhibitor vemurafenib in melanoma cells and xenografts","volume":"24","author":"Acciardo","year":"2020","journal-title":"J. Cell. Mol. Med."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1016\/j.molmet.2014.09.006","article-title":"Defective insulin secretory response to intravenous glucose in C57Bl\/6J compared to C57Bl\/6N mice","volume":"3","author":"Fergusson","year":"2014","journal-title":"Mol. Metab."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"986906","DOI":"10.1155\/2013\/986906","article-title":"Methods and models for metabolic assessment in mice","volume":"2013","author":"Pacini","year":"2013","journal-title":"J. Diabetes Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1038\/s41596-018-0102-x","article-title":"Ex vivo and in vivo stable isotope labelling of central carbon metabolism and related pathways with analysis by LC-MS\/MS","volume":"14","author":"Yuan","year":"2019","journal-title":"Nat. Protoc."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2692","DOI":"10.1038\/nprot.2007.376","article-title":"Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts","volume":"2","author":"Beckonert","year":"2007","journal-title":"Nat. Protoc."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.canlet.2019.12.003","article-title":"Acidosis-induced metabolic reprogramming in tumor cells enhances the anti-proliferative activity of the PDK inhibitor dichloroacetate","volume":"470","author":"Schoonjans","year":"2020","journal-title":"Cancer Lett."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Le Roy, T., Moens de Hase, E., Van Hul, M., Paquot, A., Pelicaen, R., Regnier, M., Depommier, C., Druart, C., Everard, A., and Maiter, D. (2021). Dysosmobacter welbionis is a newly isolated human commensal bacterium preventing diet-induced obesity and metabolic disorders in mice. Gut.","DOI":"10.1136\/gutjnl-2020-323778"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1016\/S0140-6736(05)67402-8","article-title":"The metabolic syndrome\u2014A new worldwide definition","volume":"366","author":"Alberti","year":"2005","journal-title":"Lancet"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"13007","DOI":"10.1038\/ncomms13007","article-title":"Obesity-associated NLRC4 inflammasome activation drives breast cancer progression","volume":"7","author":"Kolb","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"11270","DOI":"10.1073\/pnas.0601319103","article-title":"Real-time metabolic imaging","volume":"103","author":"Golman","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"10855","DOI":"10.1158\/0008-5472.CAN-06-2564","article-title":"Metabolic imaging by hyperpolarized 13C magnetic resonance imaging for in vivo tumor diagnosis","volume":"66","author":"Golman","year":"2006","journal-title":"Cancer Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1369\/jhc.4A6514.2005","article-title":"Immunohistochemical expression of endothelial markers CD31, CD34, von Willebrand factor, and Fli-1 in normal human tissues","volume":"54","author":"Pusztaszeri","year":"2006","journal-title":"J. Histochem. Cytochem."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2979","DOI":"10.1002\/1097-0142(19931115)72:10<2979::AID-CNCR2820721020>3.0.CO;2-X","article-title":"Overexpression of Glut-1 glucose transporter in human breast cancer. An immunohistochemical study","volume":"72","author":"Brown","year":"1993","journal-title":"Cancer"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.molmet.2019.07.006","article-title":"Monocarboxylate transporters in cancer","volume":"33","author":"Payen","year":"2020","journal-title":"Mol. Metab."},{"key":"ref_40","first-page":"8924","article-title":"Carbonic anhydrase 9 as an endogenous marker for hypoxic cells in cervical cancer","volume":"61","author":"Olive","year":"2001","journal-title":"Cancer Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"4893","DOI":"10.7150\/thno.36037","article-title":"CD36 tango in cancer: Signaling pathways and functions","volume":"9","author":"Wang","year":"2019","journal-title":"Theranostics"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Schlaepfer, I.R., and Joshi, M. (2020). CPT1A-mediated Fat Oxidation, Mechanisms, and Therapeutic Potential. Endocrinology, 161.","DOI":"10.1210\/endocr\/bqz046"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1038\/nm.4236","article-title":"A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice","volume":"23","author":"Plovier","year":"2017","journal-title":"Nat. Med."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1701","DOI":"10.1016\/j.cmet.2021.05.016","article-title":"Peroxidation of n-3 and n-6 polyunsaturated fatty acids in the acidic tumor environment leads to ferroptosis-mediated anticancer effects","volume":"33","author":"Dierge","year":"2021","journal-title":"Cell Metab."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neo.2018.09.006","article-title":"Hyperpolarized (13)C MRI: Path to Clinical Translation in Oncology","volume":"21","author":"Kurhanewicz","year":"2019","journal-title":"Neoplasia"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"22378","DOI":"10.1073\/pnas.2003537117","article-title":"Hyperpolarized [1-(13)C]pyruvate-to-[1-(13)C]lactate conversion is rate-limited by monocarboxylate transporter-1 in the plasma membrane","volume":"117","author":"Rao","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1038\/s41568-019-0216-7","article-title":"The PI3K-AKT network at the interface of oncogenic signalling and cancer metabolism","volume":"20","author":"Hoxhaj","year":"2020","journal-title":"Nat. Rev. Cancer"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3892","DOI":"10.1158\/0008-5472.CAN-03-2904","article-title":"Akt stimulates aerobic glycolysis in cancer cells","volume":"64","author":"Elstrom","year":"2004","journal-title":"Cancer Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"23798","DOI":"10.1074\/jbc.M113.482026","article-title":"Akt phosphorylates HK-II at Thr-473 and increases mitochondrial HK-II association to protect cardiomyocytes","volume":"288","author":"Roberts","year":"2013","journal-title":"J. Biol. Chem."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"17269","DOI":"10.1074\/jbc.272.28.17269","article-title":"Phosphorylation and activation of heart 6-phosphofructo-2-kinase by protein kinase B and other protein kinases of the insulin signaling cascades","volume":"272","author":"Deprez","year":"1997","journal-title":"J. Biol. Chem."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Manerba, M., Di Ianni, L., Govoni, M., Comparone, A., and Di Stefano, G. (2018). The activation of lactate dehydrogenase induced by mTOR drives neoplastic change in breast epithelial cells. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0202588"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1437","DOI":"10.1091\/mbc.e06-07-0593","article-title":"Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase\/Akt regulation of Glut1 activity and trafficking","volume":"18","author":"Wieman","year":"2007","journal-title":"Mol. Biol. Cell"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1186\/s13058-018-1029-4","article-title":"Obesity promotes the expansion of metastasis-initiating cells in breast cancer","volume":"20","author":"Bousquenaud","year":"2018","journal-title":"Breast Cancer Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2092","DOI":"10.1073\/pnas.1913841117","article-title":"Imaging breast cancer using hyperpolarized carbon-13 MRI","volume":"117","author":"Gallagher","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1016\/j.cmet.2016.01.007","article-title":"Environment Impacts the Metabolic Dependencies of Ras-Driven Non-Small Cell Lung Cancer","volume":"23","author":"Davidson","year":"2016","journal-title":"Cell Metab"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1016\/j.cell.2015.12.034","article-title":"Metabolic Heterogeneity in Human Lung Tumors","volume":"164","author":"Hensley","year":"2016","journal-title":"Cell"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1016\/j.semcdb.2019.05.016","article-title":"Reconciling environment-mediated metabolic heterogeneity with the oncogene-driven cancer paradigm in precision oncology","volume":"98","author":"Corbet","year":"2020","journal-title":"Semin. Cell Dev. Biol."}],"container-title":["Cancers"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6694\/14\/3\/562\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:06:07Z","timestamp":1760133967000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6694\/14\/3\/562"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,23]]},"references-count":57,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2022,2]]}},"alternative-id":["cancers14030562"],"URL":"https:\/\/doi.org\/10.3390\/cancers14030562","relation":{},"ISSN":["2072-6694"],"issn-type":[{"value":"2072-6694","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,23]]}}}