The DOI matches its Crossref record; 59 of the 61 references it cites were found in a registry or an index.
Combination therapy with BPTES nanoparticles and metformin targets the metabolic heterogeneity of pancreatic cancer
Open accessAbstract
Significance: There are no effective therapies currently available for advanced pancreatic cancer. We show that there are two populations of cancer cells within a pancreatic tumor that require targeting by different metabolic inhibitors for effective tumor control. Rapidly dividing cells use glutamine, and can be effectively killed by administration of a nanoparticle containing an inhibitor of glutamine metabolism. Hypoxic cells, which are slowly dividing cells, metabolize glucose and can be targeted by metformin, a drug used for the treatment of diabetes. Clinical trials are needed to determine whether combination therapy, with drugs that effectively block the metabolism of glutamine and glucose, improves the survival of patients with pancreatic cancer.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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?
In the citing paper
“pancreatic tumor-initiating cells have been found to preferentially utilize mitochondrial metabolism, as compared to glycolytic metabolism preferred by bulk tumor cells244.”
From Pancreatic cancer: Advances and challenges (2023) · cites this paper as [244]
Citations
Cites
Rahib, L., Smith, B. D., Aizenberg, R., Rosenzweig, A. B., Fleshman, J. M., & Matrisian, L. M. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-0155 · Cited by 7,094
Core Signaling Pathways in Human Pancreatic Cancers Revealed by Global Genomic Analyses
Jones, S., Zhang, X., Parsons, D. W., Lin, J. C.-H., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Kamiyama, H., Jimeno, A., et al. (2008) · Science · doi:10.1126/science.1164368 · Cited by 3,969
HMDB: the Human Metabolome Database
Wishart, D. S., Tzur, D., Knox, C., Eisner, R., Guo, A. C., Young, N., Cheng, D., Jewell, K., Arndt, D., Sawhney, S., et al. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkl923 · Cited by 3,219
From genomics to chemical genomics: new developments in KEGG
Kanehisa, M. I. (2005) · Nucleic Acids Research · doi:10.1093/nar/gkj102 · Cited by 3,126
OWEN, M. R., DORAN, E., & HALESTRAP, A. P. (2000) · Biochemical Journal · doi:10.1042/bj3480607 · Cited by 2,157
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
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
Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression
Le, A., Cooper, C. R., Gouw, A. M., Dinavahi, R., Maitra, A., Deck, L. M., Royer, R. E., Jagt, D. L. V., Semenza, G. L., & Dang, C. V. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914433107 · Cited by 1,528
Self-citationEl-Mir, M.-Y., Nogueira, V., Fontaine, E., Avéret, N., Rigoulet, M., & Leverve, X. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.1.223 · Cited by 1,399
Reactome: a knowledgebase of biological pathways
Joshi-Tope, G. (2004) · Nucleic Acids Research · doi:10.1093/nar/gki072 · Cited by 1,291
Cited by
Sorted by citations
Items 101–200 of 238
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
Zhang, L., Zhai, B.-Z., Wu, Y., & Wang, Y. (2023) · Drug Delivery · doi:10.1080/10717544.2022.2144541 · Cited by 39
“Elgogary et al. reported the bis-2-(5-phenylacetamido-1, 2, 4-thiadiazol-2-yl) ethyl sulfide (BPTES), a selective and insoluble glutaminase enzyme inhibitor, encapsulated in PLGA-PEG NPs for combinational therapy of pancreatic cancer (Elgogary et al., 2016).”
MethodTargeting glutaminase-mediated glutamine dependence in papillary thyroid cancer
Yu, Y. W., Yu, X., Fan, C., Wang, H., Wang, R., Feng, C., & Guan, H. (2018) · Journal of Molecular Medicine · doi:10.1007/s00109-018-1659-0 · Cited by 38
Polymer nanoparticle-assisted chemotherapy of pancreatic cancer
Su, T., Yang, B., Gao, T., Liu, T., & Li, J. (2020) · Therapeutic Advances in Medical Oncology · doi:10.1177/1758835920915978 · Cited by 38
Chemistry of Advanced Nanomedicines in Cancer Cell Metabolism Regulation
Yang, B., & Shi, J. (2020) · Advanced Science · doi:10.1002/advs.202001388 · Cited by 36
The Heterogeneity of Lipid Metabolism in Cancer
Park, J. K., Coffey, N. J., Limoges, A., & Le, A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65768-0_3 · Cited by 38
Self-citationTargets (Metabolic Mediators) of Therapeutic Importance in Pancreatic Ductal Adenocarcinoma
Rai, V., & Agrawal, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228502 · Cited by 36
Phenformin Enhances the Efficacy of ERK Inhibition in NF1-Mutant Melanoma
Trousil, S., Chen, S., Chan, M., Shaw, F. M., Yao, Z., Ran, Y., Tiwari, S., Merghoub, T., Manstein, D., Rosen, N. X., et al. (2017) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2017.01.013 · Cited by 37
“The notion that different metabolic programs co-exist in tumors has been recently suggested in a pancreatic ductal adenocarcinoma mouse models (Viale et al. 2014; Elgogary et al. 2016) and lung cancer patients (Hensley et al. 2016).”
BackgroundAmino Acid Oncometabolism and Immunomodulation of the Tumor Microenvironment in Lung Cancer
Fahrmann, J. F., Vykoukal, J. V., & Ostrin, E. J. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00276 · Cited by 35
“Several lines of evidence have demonstrated utility of glutaminase inhibitors as anticancer agents in a variety of cancer types including breast cancer (46, 61), lung cancer (62), pancreatic cancer (63), melanoma (64), and hematological malignancies (65).”
BackgroundZhu, X., Kong, Q., Niu, X., Chen, L., & Ge, C. (2020) · International Journal of Nanomedicine · doi:10.2147/ijn.s253599 · Cited by 36
Cai, L., Jin, X., Zhang, J., Li, L., & Zhao, J. (2020) · Aging · doi:10.18632/aging.103777 · Cited by 36
Nrf2 Activation Sensitizes K-Ras Mutant Pancreatic Cancer Cells to Glutaminase Inhibition
Hamada, S., Matsumoto, R., Tanaka, Y., Taguchi, K., Yamamoto, M. P., & Masamune, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041870 · Cited by 36
TCA cycle-derived oncometabolites in cancer and the immune microenvironment
Sarkar, S., Chang, C.-I., Jean, J., & Wu, M. (2025) · Journal of Biomedical Science · doi:10.1186/s12929-025-01186-y · Cited by 39
“BPTES, an early GLS allosteric inhibitor, showed anti-tumor activity in preclinical models but faced challenges due to poor pharmacokinetics [178].”
Targeting Metabolic Cross Talk between Cancer Cells and Cancer-Associated Fibroblasts
Jung, J. G., & Le, A. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-77736-8_12 · Cited by 38
Self-citationDesigning the Next Generation of Vaccines: Relevance for Future Pandemics
Domínguez‐Andrés, J., van Crevel, R., Divangahi, M., & Netea, M. G. (2020) · mBio · doi:10.1128/mbio.02616-20 · Cited by 37
“polyamine metabolism, both used in clinical trials with human subjects (68, 69), could be”
MethodThe Intratumoral Heterogeneity of Cancer Metabolism
Nabi, K., & Le, A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65768-0_11 · Cited by 37
Self-citationGlutaminase inhibition as potential cancer therapeutics: current status and future applications
Cyriac, R., & Lee, K. (2023) · Journal of Enzyme Inhibition and Medicinal Chemistry · doi:10.1080/14756366.2023.2290911 · Cited by 38
Different Tumor Microenvironments Lead to Different Metabolic Phenotypes
Antonio, M. J., & Le, A. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-77736-8_9 · Cited by 37
Self-citationNon-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
Lin, P., Lu, Y., Zheng, J., Lin, Y., Zhao, X., & Cui, L. (2024) · Journal of Nanobiotechnology · doi:10.1186/s12951-024-02585-3 · Cited by 35
“Several compounds inhibiting mitochondrial metabolic enzymes, including eto-moxir and BPTES, have demonstrated promising in vitro results [183, 184].”
BackgroundKitayama, K., Yashiro, M., Morisaki, T., Miki, Y., Okuno, T., Kinoshita, H., Fukuoka, T., Kasashima, H., Masuda, G., Hasegawa, T., et al. (2017) · Cancer Science · doi:10.1111/cas.13421 · Cited by 32
Nanotechnology improves delivery efficiency and bioavailability of tea polyphenols
Yin, C., Cheng, L., Zhang, X., & Wu, Z. (2020) · Journal of Food Biochemistry · doi:10.1111/jfbc.13380 · Cited by 32
Cardoso, H. J., Figueira, M. I., Vaz, C. V., Carvalho, T. M. A., Brás, L. A., Madureira, P. A., Oliveira, P. J., Sardão, V. A., & Socorro, S. (2021) · Cellular Oncology · doi:10.1007/s13402-020-00575-9 · Cited by 34
Zhang, J., Wei, L., Ma, X., Wang, J., Liang, S., Chen, K., Wu, M., Niu, L., & Zhang, Y. (2023) · Acta Biomaterialia · doi:10.1016/j.actbio.2023.05.040 · Cited by 30
Sheikh, T. N., Patwardhan, P. P., Cremers, S., & Schwartz, G. K. (2017) · Oncotarget · doi:10.18632/oncotarget.21573 · Cited by 30
“Though previous studies have evaluated efficacy of glutaminase inhibitors in cancers such as triple negative breast cancer [28], acute myeloid leukemia [35] and pancreatic cancer [36], glutamine dependency in NF1 associated malignancies has not been studied before.”
ResultUltrasound-Activated Cascade Effect for Synergistic Orthotopic Pancreatic Cancer Therapy
Cheng, D., Zhang, X., Chen, Y., Chen, H., Qiao, Z., & Wang, H. (2020) · iScience · doi:10.1016/j.isci.2020.101144 · Cited by 30
The Heterogeneity of Breast Cancer Metabolism
Tan, J., & Le, A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65768-0_6 · Cited by 36
Self-citationGlutaminase inhibitors: a patent review
Wu, C., Chen, L., Jin, S., & Li, H. (2018) · Expert Opinion on Therapeutic Patents · doi:10.1080/13543776.2018.1530759 · Cited by 29
“nanoparticles and delivered safely and effectively for treatment of glutamine addicted cancers like pancreatic cancer [100].”
BackgroundTea polyphenols-loaded nanocarriers: preparation technology and biological function
Zhang, W., Liu, Y., Zhang, X., Wu, Z., & Weng, P. (2022) · Biotechnology Letters · doi:10.1007/s10529-022-03234-1 · Cited by 29
Self-citationDifferent Tumor Microenvironments Lead to Different Metabolic Phenotypes
Antonio, M. J., Zhang, C., & Le, A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65768-0_10 · Cited by 32
Self-citationAlkhathami, A. G., Sahib, A. S., Fayi, M. S. A., Fadhil, A. A., Jawad, M. A., Shafik, S. A., Sultan, S. J., Almulla, A. F., & Shen, M. (2023) · Environmental Research · doi:10.1016/j.envres.2023.116007 · Cited by 28
Zare, I., Kiadeh, S. Z. H., Varol, A., Varol, T. Ö., Varol, M., Sezen, S., Zarepour, A., Mostafavi, E., Nasab, S. Z., Rahi, A., et al. (2024) · Journal of Controlled Release · doi:10.1016/j.jconrel.2024.05.032 · Cited by 28
Shining a light on metabolic vulnerabilities in non-small cell lung cancer
Dowling, C. M., Zhang, H., Chonghaile, T. N., & Wong, K.-K. (2021) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2020.188462 · Cited by 26
Cancer cells employ lipid droplets to survive toxic stress
Kostecka, L. G., Mendez, S. A., Li, M., Khare, P., Zhang, C., Le, A., Amend, S. R., & Pienta, K. J. (2024) · The Prostate · doi:10.1002/pros.24680 · Cited by 26
Self-citationZhao, Y., Wang, Y., Miao, Z., Liu, Y., & Yang, Q. (2023) · Molecular Biology Reports · doi:10.1007/s11033-023-08495-1 · Cited by 26
Self-citationDecoding mitochondria's role in immunity and cancer therapy
Zhang, Y., YAN, H. H., Wei, Y., & Wei, X. (2024) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2024.189107 · Cited by 30
Giesen, B., Nickel, A., Barthel, J., Kahlert, U. D., & Janiak, C. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13020295 · Cited by 25
Nidadavolu, L. S., Stern, D., Lin, R., Wang, Y., Li, Y., Wu, Y., Marin, S., Antonio, M. J., Yenokyan, G., Boronina, T. N., et al. (2021) · Wound Repair and Regeneration · doi:10.1111/wrr.12974 · Cited by 25
Self-citationTargeting Metabolic Cross Talk Between Cancer Cells and Cancer-Associated Fibroblasts
Jung, J. G., & Le, A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65768-0_15 · Cited by 24
Self-citationGlutaminases as a Novel Target for SDHB-Associated Pheochromocytomas/Paragangliomas
Sarkadi, B., Meszaros, K., Krencz, I., Canu, L., Krokker, L., Zakarias, S., Barna, G., Sebestyen, A., Papay, J., Hujber, Z., et al. (2020) · Cancers · doi:10.3390/cancers12030599 · Cited by 23
Nguyen, T. T., Katt, W. P., & Cerione, R. A. (2022) · Future Drug Discovery · doi:10.4155/fdd-2022-0011 · Cited by 23
“Moreover, improvement in the delivery strategy for BPTES, such as encapsulation of the compound in dense poly(ethylene glycol) nanoparticles, also showed enhanced drug exposure and lower liver toxicity in mice bearing orthotopic pancreatic tumors [66,67].”
BackgroundCooper, A. J. L., Dorai, T., Pinto, J. T., & Denton, T. T. (2023) · Biology · doi:10.3390/biology12081131 · Cited by 23
Zhang, J., Chen, M., Yang, Y., Liu, Z., Guo, W., Xiang, P., Zeng, Z., Wang, D., & Xiong, W. (2024) · Journal of Cellular Physiology · doi:10.1002/jcp.31349 · Cited by 23
“…as potential anticancer drugs across various cancer types, including breast cancer, (DeLaBarre et al., 2011; Gross et al., 2014) lung cancer, (Galan ‐ Cobo et al., 2019) pancreatic cancer, (Elgogary et al., 2016) melanoma, (Shah et al., 2019) and hematologic malignancies (Gregory et al., 2019).”
Anzmann, A. F., Carney, O. S., Pado, A. M., Busa, V. F., Vaz, F. M., Kreimer, S. D., Devine, L. R., Cole, R. N., Le, A., Kirsch, B. J., et al. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101005 · Cited by 21
Self-citationAutophagy in cancer: The cornerstone during glutamine deprivation
Fares, H. M., Lyu, X., Xu, X., Dong, R., Ding, M., Mi, S., Wang, Y., Li, X., Yuan, S., & Sun, L. (2021) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2021.174723 · Cited by 22
Effects of metabolic cancer therapy on tumor microenvironment
Hyroššová, P., Milošević, M., Škoda, J., Vachtenheim, J., Jr., Rohlena, J., & Rohlenová, K. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1046630 · Cited by 23
Tousian, B., & Khosravi, A. (2023) · Results in Chemistry · doi:10.1016/j.rechem.2023.101146 · Cited by 21
Dietary approaches for exploiting metabolic vulnerabilities in cancer
Menyhárt, O., & Győrffy, B. (2023) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2023.189062 · Cited by 23
Wu, C., Zheng, M., Gao, S., Luan, S., Cheng, L., Wang, L., Li, J., Chen, L., & Li, H. (2017) · Oncotarget · doi:10.18632/oncotarget.23058 · Cited by 21
“It has been determined that growing cancer cells were strongly dependent on energy sources such as glucose and glutamine [26].”
BackgroundDesign of Nanoparticles in Cancer Therapy Based on Tumor Microenvironment Properties
Firouzabadi, B. M., Gigliobianco, M. R., Joseph, J. M., Censi, R., & Martino, P. D. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14122708 · Cited by 21
“[118] P8, A6L, A32, P198, E3, P215, P10, JD13D patient-derived PDAC cell lines, and patient-derived pancreatic tumors BPTES is a glutaminase inhibitor, and the nanoparticle system demonstrated a significant effect on pancreatic cancer models in combination with metformin therapy Metabolic changes in TME PLGA-PEG nanop…”
BackgroundEnhancement of targeted therapy in combination with metformin on human breast cancer cell lines
Mahmoudi, G., Ehteshaminia, Y., Kokhaei, P., Jalali, S. F., Jadidi‐Niaragh, F., Pagheh, A. S., Enderami, S. E., Abediankenari, S., & Hassannia, H. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-023-01446-0 · Cited by 20
“Furthermore, studies focusing on combination therapy have demonstrated the reinforcing effects of Met combination therapy in pancreatic, lung, and breast cancers [16–18].”
BackgroundLiu, X., Wang, L., Jiang, W., Lu, W., Yang, J., & Yang, W. (2018) · Journal of Cancer · doi:10.7150/jca.24331 · Cited by 19
“Based on their distinct metabolic wiring, alterations in energy metabolism and increased dependency on glycolysis or glutaminolysis, we predicted that Glu-dependent and GLN-addicted cell lines would show differential sensitivity to inhibitors targeting aerobic glycolysis (3-BrPA) [22] and glutaminolysis [bis-2-(5-phen…”
BackgroundTherapeutic Targeting of Glutaminolysis as a Novel Strategy to Combat Cancer Stem Cells
Kao, T., Chuang, Y.-C., Lee, H., Kuo, C., & Shen, Y. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232315296 · Cited by 19
Roy, S. K., Đukić, T., Bhandary, B., Tu, K. J., Molitoris, J. K., Ko, Y. H., & Shukla, H. D. (2022) · PubMed Central · Cited by 18
Genetic Ablation of LAT1 Inhibits Growth of Liver Cancer Cells and Downregulates mTORC1 Signaling
Kim, S.-Y., Ong, Q., Liao, Y., Ding, Z., Tan, A. Q. L., Lim, L. T. R., Tan, H. M., Lim, S. L., Lee, Q. Y., & Han, W. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24119171 · Cited by 18
The Intricate Metabolism of Pancreatic Cancers
Camelo, F., & Le, A. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-77736-8_5 · Cited by 19
Self-citationDual role of N-acetyl-aspartyl-glutamate metabolism in cancer monitor and therapy
Asaka, R., & Le, A. (2019) · Molecular & Cellular Oncology · doi:10.1080/23723556.2019.1627273 · Cited by 18
Self-citationAlvina, F. B., Gouw, A. M., & Le, A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65768-0_12 · Cited by 17
Self-citationAlshememry, A. K., Alsaleh, N. B., Alkhudair, N. A., Alzhrani, R. M., & Alshamsan, A. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.933457 · Cited by 17
“Integrating RNAi with NPs can therefore be extremely effective at treating PC (Hiss et al., 2007; Gurunathan et al., 2018).”
MethodInfluentialLiu, D., Wang, Y., Li, X., Wang, Y., Zhang, Z., Wang, Z., & Zhang, X. (2023) · Amino Acids · doi:10.1007/s00726-023-03316-y · Cited by 17
“Combination therapy using BPTES NPs and metformin has been designed and targeted in mouse models transplanted with patient-derived pancreatic tumor cells to obtain cytotoxic activity against hypoxic non-cyclic cells as well (Elgogary et al. 2016).”
MethodGlutamine addiction and therapeutic strategies in pancreatic cancer
Ren, L., Mao, T., Meng, P., Zhang, L., Wei, H., & Tian, Z. (2023) · World Journal of Gastrointestinal Oncology · doi:10.4251/wjgo.v15.i11.1852 · Cited by 16
“Metformin was chosen for application with BPTES nanoparticles based on this finding, and the reduction in pancreatic tumors was significantly more significant than treatment alone[83].”
Recent Advances in Nanoparticle-Mediated Diagnosis and the Treatment of Pancreatic Cancer
Nedelcu, A., Mocan, T., Grapa, C. M., & MOCAN, L. C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158060 · Cited by 14
Fang, J., Chen, Z., Song, J., Li, J., Han, Y., Hou, W., Wang, W., & Ruan, B. H. (2021) · RSC Chemical Biology · doi:10.1039/d1cb00089f · Cited by 14
Regulation of metabolism in pancreatic ductal adenocarcinoma via nanotechnology-enabled strategies
Wang, Z., Wu, B., Nie, G., Wei, J., & Li, Y. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216138 · Cited by 15
Oyama, K., Iwagami, Y., Kobayashi, S., Sasaki, K., Yamada, D., Tomimaru, Y., Noda, T., Asaoka, T., Takahashi, H., Tanemura, M., et al. (2023) · International Journal of Cancer · doi:10.1002/ijc.34725 · Cited by 16
“37 Therefore, using a low concentration of a GLS1 inhibitor, which does not affect other organs, may eliminate iSnCa cells emerging due to insufficient therapeutic intensity or drug resistance from gemcitabine administration in PDAC.”
BackgroundChen, X., Li, L., Deng, Y., Liao, J., Meng, H., Liang, L., Hu, J., Xie, D., & Liang, G. (2025) · Immunology Letters · doi:10.1016/j.imlet.2025.106974 · Cited by 14
The Intricate Metabolism of Pancreatic Cancers
Camelo, F. S., & Le, A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65768-0_5 · Cited by 15
Self-citationHuang, Y., Chen, Y., Zhou, S., Xie, L., Liang, K., Xu, J., Zhang, Q., Chen, H., Wang, D., Song, Q., et al. (2023) · ACS Nano · doi:10.1021/acsnano.3c04069 · Cited by 13
Fu, Z., Du, H., Meng, S., Yao, M., Zhao, P., Li, X., Zheng, X., Zhang, Y., Yang, H., Cai, K., et al. (2022) · Materials Today Bio · doi:10.1016/j.mtbio.2022.100449 · Cited by 13
“However, its antitumor therapeutic effect was actually limited by the compensatory glycolysis metabolism [11,12].”
BackgroundBiochemical hallmarks-targeting antineoplastic nanotherapeutics
Han, J. G., Dong, H., Zhu, T., Wei, Q., Wang, Y., Wang, Y., Lv, Y. B., Mu, H., Huang, S., Zeng, K., et al. (2024) · Bioactive Materials · doi:10.1016/j.bioactmat.2024.05.042 · Cited by 14
“To overcome these obstacles, Elgogary et al. encapsulated BPTES into biodegradable nanoparticles comprising PLGA and PEG to form BPTES-NP [288].”
BackgroundGulla, A., Andriusaityte, U., Zdanys, G., Babonaite, E., Strupas, K., & Kelly, H. M. (2022) · Medicina · doi:10.3390/medicina58040467 · Cited by 12
Deciphering the landscape of allosteric glutaminase 1 inhibitors as anticancer agents
Vagaggini, C., D’Ursi, P., Poggialini, F., Fossa, P., Francesconi, V., Trombetti, G., Orro, A., Dreassi, E., Schenone, S., Tonelli, M., et al. (2025) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2025.108523 · Cited by 12
Mansoori, A. A., Baig, B., Harati, R., Alhamidi, R. S., Hamza, A. A., Al‐Salam, S., Le, A., Zhang, C., Khare, P., Hamoudi, R., et al. (2026) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-026-05573-6 · Cited by 10
“Metabolites were extracted from all tissue samples simultaneously using a previously established protocol (Elgogary et al. 2016; Nguyen et al. 2019; Udupa et al. 2019)).”
Self-citationMetabolic Intersection of Cancer and Cardiovascular Diseases: Opportunities for Cancer Therapy
Hoang, G., Nguyen, K. T., & Le, A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65768-0_18 · Cited by 10
Self-citationT-cell Metabolism as a Target to Control Autoreactive T Cells in β-Cell Autoimmunity
Bordignon, C., Canu, A., Dyczko, A., Leone, S., & Monti, P. (2017) · Current Diabetes Reports · doi:10.1007/s11892-017-0848-5 · Cited by 10
Long non‑coding RNAs: Key regulators involved in metabolic reprogramming in cancer (Review)
Liu, C., Li, H. R., Chu, F., Zhou, X., Xie, R., Wei, Q., Yang, S., Li, T., Liang, S., & Lü, M. (2021) · Oncology Reports · doi:10.3892/or.2021.8005 · Cited by 10
Integrative insights into the role of CAV1 in ketogenic diet and ferroptosis in pancreatic cancer
Liang, X., Tian, R.-F., Li, T., Wang, H., Qin, Y., Qian, M., Fan, J., Wang, D., Cui, H., & Jiang, J. (2025) · Cell Death Discovery · doi:10.1038/s41420-025-02421-z · Cited by 9
“Therapeutic approaches targeting metabolic heterogeneity have sparked increasing interest [6, 7], and the metabolic environment within pancreatic cancer is dysregulated [8].”
Metabolic plasticity in pancreatic ductal adenocarcinoma progression and response to treatment
Ma, J., Bhardwaj, V., Lobie, P. E., & Pandey, V. (2026) · Molecular Cancer · doi:10.1186/s12943-026-02620-x · Cited by 10
“When combined with the glycolytic inhibitor metformin, this dual-metabolic targeting approach significantly suppresses tumor growth in patient-derived orthotopic PDAC xenograft models by simultaneously inhibiting GLS in cycling cells and glycolysis in the surviving, hypoxic cell population [378].”
Diabetes and Cancer: The Epidemiological and Metabolic Associations
Zhang, C., & Le, A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65768-0_16 · Cited by 9
Self-citationSaeui, C. T., Shah, S. R., Fernández-Gil, B. I., Zhang, C., Agatemor, C., Dammen‐Brower, K., Mathew, M. P., Buettner, M. J., Gowda, P. C., Khare, P., et al. (2023) · ACS Chemical Biology · doi:10.1021/acschembio.2c00784 · Cited by 8
Self-citationZhang, Y., Kumata, K., Xie, L., Kurihara, Y., Ogawa, M., Kokufuta, T., Nengaki, N., & Zhang, M. (2023) · Pharmaceuticals · doi:10.3390/ph16070963 · Cited by 8
Bridging the Metabolic Parallels Between Neurological Diseases and Cancer
Guo, S., Gu, Y., Qu, J., & Le, A. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-65768-0_17 · Cited by 8
Self-citationCheng, Q., Chen, Y., Zou, D., Li, Q., Shi, X., Qin, Q., Liu, M., Wang, L., & Wang, Z. (2024) · Advanced Science · doi:10.1002/advs.202409329 · Cited by 8
Zhang, B., Fan, R., Hai, Y., Chen, Y., Lu, X., Wang, W., Dou, J., Yan, J., Su, C., Chen, Y., et al. (2025) · Advanced Science · doi:10.1002/advs.202513986 · Cited by 7
Targeting cancer metabolism through synthetic lethality-based combinatorial treatment strategies
Bajpai, R., & Shanmugam, M. (2018) · Current Opinion in Oncology · doi:10.1097/cco.0000000000000467 · Cited by 8
Thermosensitive hydrogel loaded with nanozyme and BPTES for enhanced tumor catalytic therapy
Lv, X., Liu, Z., Qi, P., & Chen, K. (2025) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2025.114600 · Cited by 6
Glutaminase 1 inhibitors: Therapeutic potential, mechanisms of action, and clinical perspectives
Wang, H., Li, X., Hu, H., & Gao, Z. (2025) · Biochemical Pharmacology · doi:10.1016/j.bcp.2025.117275 · Cited by 10
Hoang, G., Zhang, C., Attarwala, N., Jung, J. G., Cooper, A. J. L., & Le, A. (2021) · Analytical Biochemistry · doi:10.1016/j.ab.2021.114206 · Cited by 6
Self-citationRapid quantification of glutaminase 2 (GLS2)-related metabolites by HILIC-MS/MS
Chen, G., Chao, H., Liao, H., Tsai, I., & Kuo, C. (2017) · Analytical Biochemistry · doi:10.1016/j.ab.2017.10.002 · Cited by 6
Kar, N. P., Lin, J., Rad, A. H., Li, W., Aboushanab, A. R., Li, Y., & Sun, J. (2025) · Smart Materials in Medicine · doi:10.1016/j.smaim.2025.09.003 · Cited by 6
“Elgogary et al. developed PLGA nanoparticles loaded with the GLS1 inhibitor BPTES to disrupt glutamine metabolism in PDAC, modestly slowing tumor growth [120].”
Self-Assembled Micellar Glutaminase Allosteric Inhibitor for Effective Therapeutic Intervention
Fang, J., Chen, Z., Li, J., Li, D., Wang, W., & Ruan, B. H. (2022) · International Journal of Nanomedicine · doi:10.2147/ijn.s346596 · Cited by 5
“Polymeric nanoparticles have been designed for BPTES and verified to show improvement in solubility, cellular uptake and tumor damage.(13)”
Mapping the current research landscape of metformin in cancer based on bibliometric analysis
Wang, Y., He, S., Li, Z., Jiang, N., & Sun, G. (2025) · Discover Oncology · doi:10.1007/s12672-025-03327-z · Cited by 4
“A recent study demonstrated that nanoparticle-encapsulated BPTES improved pharmacokinetics, efficacy, and safety, selectively targeting proliferating pancreatic cancer cells [77].”
Recent advances in nanotechnology for metabolic cancer therapy
Hou, G., Lu, Y., Chen, Y., Lei, H., & Cheng, L. (2025) · Coordination Chemistry Reviews · doi:10.1016/j.ccr.2025.216889 · Cited by 4
Yang, X., Lai, Q., Yang, X., Xie, B., Zhang, B., Zhang, X., & Wei, Y. (2021) · Materials Chemistry Frontiers · doi:10.1039/d1qm01277k · Cited by 4
Diseases & Disorders | Therapies Targeting Glutamine Addiction in Cancer
Attarwala, N., Zhang, C., & Le, A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819460-7.00079-7 · Cited by 4
Self-citationBionic nanomedicines for microwave-triggered cuproptosis to enhance cancer immunotherapy
Suo, M., Wang, Z., Zhang, S., Tang, W., Liang, D., Chen, X. S., & Ning, S. (2025) · Nanoscale Horizons · doi:10.1039/d5nh00425j · Cited by 3
Metabolic Recycling Enhances Proliferation in MYC‐Transformed Lymphoma B Cells
Zhang, C., Hoang, G., Attarwala, N., Cooper, A. J. L., Asaka, R., & Le, A. (2022) · Advanced Biology · doi:10.1002/adbi.202200233 · Cited by 3
Self-citationNanoparticle-based formulation for drug repurposing in cancer treatment
Cheng, B., & Xu, P. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819668-7.00013-0 · Cited by 3
Engineering glutamine-regulating nanomedicines for efficient tumor therapy
Hou, G., Lu, S., Chen, Y., Lei, H., Yi, B., & Cheng, L. (2025) · Materials Today · doi:10.1016/j.mattod.2025.09.019 · Cited by 2
Ammonia in cancer: dual roles and therapeutic strategies
Wei, J., Chen, Y., Li, Q., Huang, F., Zhang, C., Hou, B., & Huang, S. (2025) · Cancer Cell International · doi:10.1186/s12935-025-04065-6 · Cited by 2
Metadata
- Authors
- Elgogary, A., Xu, Q., Poore, B., Alt, J., Zimmermann, S. C., Zhao, L., Fu, J., Chen, B., Xia, S., Liu, Y., Neisser, M., Nguyen, C., Lee, R., Park, J. K., Reyes, J., Hartung, T., Rojas, C., Rais, R., Tsukamoto, T., Semenza, G. L., Hanes, J., Slusher, B. S., & Le, A.
- Affiliations
- Johns Hopkins University (US)
- Department of Environmental Health Sciences, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205;
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2016-08-24
- Volume
- 113
- Issue
- 36
- Pages
- E5328-36
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC5018752
- OpenAlex
- W2515129893
- Cited by
- 234
- References
- 61
- Citations by year
- 2026: 16 · 2025: 20 · 2024: 17 · 2023: 25 · 2022: 24 · 2021: 38 · 2020: 32 · 2019: 19 · 2018: 21 · 2017: 21 · 2016: 1
- FWCI
- 8.61
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Cancer Institute (R01-CA193895, R21-CA169757)
- HHS | NIH | National Institute on Drug Abuse (R03-DA032470)
- HHS | NIH | National Institute of Mental Health (P30-MH075673)
- HHS | NIH | National Center for Advancing Translational Sciences (UL1-TR001079)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
- Keywords
- BPTES, glutaminase inhibition, glutamine metabolism, pancreatic cancer, nanoparticles, drug encapsulation, metformin, combination therapy, tumor metabolic heterogeneity, tumor hypoxia, glycolysis, glycogen synthesis, CB-839, pharmacokinetics, cancer metabolism
- MeSH terms
- Animals, Antineoplastic Combined Chemotherapy Protocols, Glutaminase, Glutamine, Humans, Metformin, Pancreatic Neoplasms, Sulfides, Thiadiazoles, Proto-Oncogene Proteins p21(ras), Xenograft Model Antitumor Assays, Benzeneacetamides, Cell Line, Tumor, Mice, Nanoparticles
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
