Imaging of glucose metabolism by 13C-MRI distinguishes pancreatic cancer subtypes in mice
Open accessAbstract
Metabolic differences among and within tumors can be an important determinant in cancer treatment outcome. However, methods for determining these differences non-invasively in vivo is lacking. Using pancreatic ductal adenocarcinoma as a model, we demonstrate that tumor xenografts with a similar genetic background can be distinguished by their differing rates of the metabolism of 13C labeled glucose tracers, which can be imaged without hyperpolarization by using newly developed techniques for noise suppression. Using this method, cancer subtypes that appeared to have similar metabolic profiles based on steady state metabolic measurement can be distinguished from each other. The metabolic maps from 13C-glucose imaging localized lactate production and overall glucose metabolism to different regions of some tumors. Such tumor heterogeneity would not be not detectable in FDG-PET.
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Differential metabolism of tumor regions can be observed through imaging techniques, including spatial heterogeneity of glycolysis.
“The differential metabolism of these regions can be readily observed through imaging techniques236,237, including spatial heterogeneity of glycolysis.”
From Pancreatic cancer: Advances and challenges (2023) · cites this paper as [236]
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A Simple Sequentially Rejective Multiple Test Procedure
(1979) · Scandinavian Journal of Statistics · doi:10.2307/4615733 · Cited by 21,526 · see citing works
Spencer, P. M., Cameron, J. L., & Lin, L. (2000) · Cited by 7,202 · see citing works
The emerging hallmarks of cancer metabolism
Pavlova, N. N., & Thompson, C. B. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2015.12.006 · Cited by 5,926 · see citing works
HMDB 4.0: the human metabolome database for 2018
Wishart, D. S., Feunang, Y. D., Marcu, A., Guo, A. C., Liang, K., Vázquez-Fresno, R., Sajed, T., Johnson, D., Li, C., Karu, N., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gkx1089 · Cited by 3,438 · see citing works
Metabolic Reprogramming: A Cancer Hallmark Even Warburg Did Not Anticipate
Ward, P. S., & Thompson, C. B. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.02.014 · Cited by 3,233 · see citing works
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 · see citing works
Hidalgo, M. (2010) · New England Journal of Medicine · doi:10.1056/nejmra0901557 · Cited by 2,570 · see citing works
Understanding the Intersections between Metabolism and Cancer Biology
Heiden, M. G. V., & DeBerardinis, R. J. (2017) · Cell · doi:10.1016/j.cell.2016.12.039 · Cited by 2,316 · see citing works
RARE imaging: A fast imaging method for clinical MR
Hennig, J., Nauerth, A., & Friedburg, H. (1986) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910030602 · Cited by 2,088 · see citing works
Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism
Ying, H., Kimmelman, A. C., Lyssiotis, C. A., Hua, S., Chu, G. C., Fletcher-Sananikone, E., Locasale, J. W., Son, J., Zhang, H., Coloff, J. L., et al. (2012) · Cell · doi:10.1016/j.cell.2012.01.058 · Cited by 2,043 · see citing works
Glucose feeds the TCA cycle via circulating lactate
Hui, S., Ghergurovich, J. M., Morscher, R. J., Jang, C., Teng, X., Lu, W., Esparza, L. A., Reya, T., Zhan, L., Yanxiang Guo, J., et al. (2017) · Nature · doi:10.1038/nature24057 · Cited by 1,721 · see citing works
Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice
Sonveaux, P., Végran, F., Schroeder, T., Wergin, M., Verrax, J., Rabbani, Z. N., Saedeleer, C. J. D., Kennedy, K. M., Diepart, C., Jordan, B. F., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci36843 · Cited by 1,635 · see citing works
On the Best Rank-1 and Rank-( R 1 , R 2 ,. . ., R N ) Approximation of Higher-Order Tensors
Lathauwer, L. D., Moor, B. D., & Vandewalle, J. P. L. (2000) · SIAM Journal on Matrix Analysis and Applications · doi:10.1137/s0895479898346995 · Cited by 1,622 · see citing works
Pancreatic cancers require autophagy for tumor growth
Yang, S., Wang, X., Contino, G., Liesa, M., Sahin, E., Ying, H., Bause, A., Li, Y., Stommel, J. M., Dell'Antonio, G., et al. (2011) · Genes & Development · doi:10.1101/gad.2016111 · Cited by 1,498 · see citing works
Eilers, P. H. C. (2003) · Analytical Chemistry · doi:10.1021/ac034173t · Cited by 1,347 · see citing works
Lactate Metabolism in Human Lung Tumors
Faubert, B., Li, K. Y., Cai, L., Hensley, C. T., Kim, J., Zacharias, L. G., Yang, C., Do, Q. N., Doucette, S., Burguete, D., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.019 · Cited by 1,343 · see citing works
Andersson, C. A., & Bro, R. (2000) · Chemometrics and Intelligent Laboratory Systems · doi:10.1016/s0169-7439(00)00071-x · Cited by 1,235 · see citing works
Metabolic heterogeneity in human lung tumors
Hensley, C. T., Faubert, B., Yuan, Q., Lev-Cohain, N., Jin, E., Kim, J., Jiang, L., Ko, B., Skelton, R., Loudat, L., et al. (2016) · Cell · doi:10.1016/j.cell.2015.12.034 · Cited by 1,138 · see citing works
Pancreatic stellate cells support tumour metabolism through autophagic alanine secretion
Sousa, C. M., Biancur, D. E., Wang, X., Halbrook, C. J., Sherman, M. H., Zhang, L., Kremer, D., Hwang, R. F., Witkiewicz, A. K., Ying, H., et al. (2016) · Nature · doi:10.1038/nature19084 · Cited by 1,122 · see citing works
Regulation of pyruvate metabolism and human disease
Gray, L. R., Tompkins, S. C., & Taylor, E. B. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1539-2 · Cited by 951 · see citing works
Phenotype and Genotype of Pancreatic Cancer Cell Lines
Deer, E. L., González-Hernández, J., Coursen, J. D., Shea, J. E., Ngatia, J., Scaife, C. L., Firpo, M. A., & Mulvihill, S. J. (2010) · Pancreas · doi:10.1097/mpa.0b013e3181c15963 · Cited by 936 · 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
Automatic, localized in Vivo adjustment of all first‐and second‐order shim coils
Gruetter, R. (1993) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910290613 · Cited by 875 · see citing works
KRAS: feeding pancreatic cancer proliferation
Bryant, K. L., Mancias, J. D., Kimmelman, A. C., & Der, C. J. (2014) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2013.12.004 · Cited by 675 · see citing works
Pancreatic tumors show high levels of hypoxia
Koong, A. C., Mehta, V. K., Le, Q., Fisher, G. A., Terris, D. J., Brown, J. M., Bastidas, A. J., & Vierra, M. A. (2000) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/s0360-3016(00)00803-8 · Cited by 653 · see citing works
Pancreatic Ductal Adenocarcinoma: Current and Evolving Therapies
Adamska, A., Domenichini, A., & Falasca, M. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18071338 · Cited by 601 · see citing works
Pancreatic cancer: from state-of-the-art treatments to promising novel therapies
Garrido‐Laguna, I., & Hidalgo, M. M. (2015) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2015.53 · Cited by 565 · see citing works
Involvement of endothelial PECAM-1/CD31 in angiogenesis.
DeLisser, H. M., Christofidou‐Solomidou, M., Strieter, R. M., Burdick, M. D., Robinson, C., Wexler, R. S., Kerr, J. S., Garlanda, C., Merwin, J. R., Madri, J. A., et al. (1997) · Europe PMC (PubMed Central) · Cited by 564 · see citing works
Svensson, R. U., Parker, S. J., Eichner, L. J., Kolar, M. J., Wallace, M., Brun, S. N., Lombardo, P. S., Van Nostrand, J. L., Hutchins, A., Vera, L., et al. (2016) · Nature Medicine · doi:10.1038/nm.4181 · Cited by 536 · see citing works
Guillaumond, F., Leca, J., Olivares, O., Lavaut, M.-N., Vidal, N., Berthezène, P., Dusetti, N. J., Loncle, C., Calvo, E., Turrini, O., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219555110 · Cited by 413 · see citing works
Daemen, A., Peterson, D., Sahu, N., McCord, R., Du, X., Liu, B., Kowanetz, K., Hong, R., Moffat, J., Gao, M., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501605112 · Cited by 398 · see citing works
Generation of orthotopic and heterotopic human pancreatic cancer xenografts in immunodeficient mice
Kim, M. P., Evans, D. B., Wang, H., Abbruzzese, J. L., Fleming, J. B., & Gallick, G. E. (2009) · Nature Protocols · doi:10.1038/nprot.2009.171 · Cited by 383 · see citing works
Diversion of aspartate in ASS1-deficient tumours fosters de novo pyrimidine synthesis
Rabinovich, S., Adler, L., Yizhak, K., Sarver, A., Silberman, A., Agron, S., Stettner, N., Sun, Q., Brandis, A., Helbling, D., et al. (2015) · Nature · doi:10.1038/nature15529 · Cited by 382 · see citing works
Deuterium metabolic imaging (DMI) for MRI-based 3D mapping of metabolism in vivo
Feyter, H. M. D., Behar, K. L., Corbin, Z. A., Fulbright, R. K., Brown, P. B., McIntyre, S., Nixon, T. W., Rothman, D. L., & de Graaf, R. A. (2018) · Science Advances · doi:10.1126/sciadv.aat7314 · Cited by 378 · see citing works
New developments in pairwise multiple comparisons: Some powerful and practicable procedures.
Seaman, M. A., Levin, J. R., & Serlin, R. C. (1991) · Psychological Bulletin · doi:10.1037/0033-2909.110.3.577 · Cited by 326 · see citing works
Compensatory metabolic networks in pancreatic cancers upon perturbation of glutamine metabolism
Biancur, D. E., Paulo, J. A., Małachowska, B., Quiles Del Rey, M., Sousa, C. M., Wang, X., Sohn, A. S. W., Chu, G. C., Gygi, S. P., Harper, J. W., et al. (2017) · Nature Communications · doi:10.1038/ncomms15965 · Cited by 315 · see citing works
The Proto-oncometabolite Fumarate Binds Glutathione to Amplify ROS-Dependent Signaling
Sullivan, L. B., Martinez-Garcia, E., Nguyen, H., Mullen, A. R., Dufour, E., Sudarshan, S., Licht, J. D., Deberardinis, R. J., & Chandel, N. S. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.05.003 · Cited by 304 · see citing works
Magnetic resonance imaging of tumor glycolysis using hyperpolarized 13C-labeled glucose
Rodrigues, T. B., Serrão, E. M., Kennedy, B. W. C., Hu, D., Kettunen, M. I., & Brindle, K. M. (2013) · Nature Medicine · doi:10.1038/nm.3416 · Cited by 274 · see citing works
The Impact of Peroxisomes on Cellular Aging and Death
Manivannan, S., Scheckhuber, C. Q., Marten Veenhuis, A., & van der Klei, I. J. (2012) · Frontiers in Oncology · doi:10.3389/fonc.2012.00050 · Cited by 273 · see citing works
Badar‐Goffer, R. S., Bachelard, H. S., & Morris, P. G. (1990) · Biochemical Journal · doi:10.1042/bj2660133 · Cited by 258 · see citing works
van Beek, J. D. (2007) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2007.03.017 · Cited by 231 · see citing works
Saunier, E. F., Benelli, C., & Bortoli, S. (2015) · International Journal of Cancer · doi:10.1002/ijc.29564 · Cited by 217 · see citing works
Applications of NMR spectroscopy to systems biochemistry
Fan, T. W. ‐., & Lane, A. N. (2016) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2016.01.005 · Cited by 209 · see citing works
Self-citationTargeting amino acid metabolism in cancer growth and anti-tumor immune response
Ananieva, E. A. (2015) · World Journal of Biological Chemistry · doi:10.4331/wjbc.v6.i4.281 · Cited by 198 · see citing works
Anderson, M., Marayati, R., Moffitt, R. A., & Yeh, J. J. (2016) · Oncotarget · doi:10.18632/oncotarget.9760 · Cited by 191 · see citing works
The emerging role of fumarate as an oncometabolite
Yang, M., Soga, T., Pollard, P. J., & Adam, J. (2012) · Frontiers in Oncology · doi:10.3389/fonc.2012.00085 · Cited by 189 · see citing works
Kinetic modeling of hyperpolarized 13C1-pyruvate metabolism in normal rats and TRAMP mice
Zierhut, M. L., Yen, Y., Chen, A. P., Bok, R., Albers, M. J., Zhang, V. Y., Tropp, J., Park, I., Vigneron, D. B., Kurhanewicz, J. V., et al. (2009) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2009.10.003 · Cited by 166 · see citing works
Self-citationHill, D. K., Orton, M. R., Mariotti, E., Boult, J. K. R., Panek, R., Jafar, M. M., Parkes, H. G., Jamin, Y., Miniotis, M. F., Al-Saffar, N. M. S., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071996 · Cited by 165 · see citing works
Broadband Decoupling in High-Resolution Nuclear Magnetic Resonance Spectroscopy
Levitt, M. H., Freeman, R., & Frenkiel, T. A. (1983) · Advances in magnetic and optical resonance · doi:10.1016/b978-0-12-025511-5.50008-6 · Cited by 154 · see citing works
Rai, G., Brimacombe, K. R., Mott, B. T., Urban, D. J., Hu, X., Yang, S., Lee, T. D., Cheff, D. M., Kouznetsova, J., Benavides, G. A., et al. (2017) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.7b00941 · Cited by 153 · see citing works
A new general-purpose fully automatic baseline-correction procedure for 1D and 2D NMR data
Cobas, J. C., Bernstein, M. A., Martín‐Pastor, M., & Tahoces, P. G. (2006) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2006.07.013 · Cited by 147 · see citing works
Stromal cues regulate the pancreatic cancer epigenome and metabolome
Sherman, M. H., Yu, R. T., Tseng, T. W., Sousa, C. M., Liu, S., Truitt, M. L., He, N., Ding, N., Liddle, C., Atkins, A. R., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1620164114 · Cited by 147 · see citing works
Metabolism addiction in pancreatic cancer
Blum, R., & Kloog, Y. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.38 · Cited by 134 · see citing works
An efficient algorithm for automatic phase correction of NMR spectra based on entropy minimization
Chen, L., Weng, Z., Goh, L. Y., & Garland, M. (2002) · Journal of Magnetic Resonance · doi:10.1016/s1090-7807(02)00069-1 · Cited by 127 · see citing works
Mirnezami, R., Spagou, K., Vorkas, P. A., Lewis, M. R., Kinross, J. K., Want, E. J., Shion, H., Goldin, R. D., Darzi, A. W., Takáts, Z., et al. (2013) · Molecular Oncology · doi:10.1016/j.molonc.2013.08.010 · Cited by 125 · see citing works
Supercycles for broadband heteronuclear decoupling
Levitt, M. H., Freeman, R., & Frenkiel, T. A. (1982) · Journal of Magnetic Resonance (1969) · doi:10.1016/0022-2364(82)90042-7 · Cited by 117 · see citing works
Liu, Q., Sun, J. D., Wang, J., Ahluwalia, D., Baker, A. F., Cranmer, L. D., Ferraro, D., Wang, Y., Duan, J.-X., Ammons, W. S., et al. (2012) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-012-1852-8 · Cited by 113 · see citing works
A comparison of quantitative methods for clinical imaging with hyperpolarized 13C‐pyruvate
Daniels, C. J., McLean, M. A., Schulte, R. F., Robb, F. J. L., Gill, A. B., McGlashan, N., Graves, M. J., Schwaiger, M., Lomas, D. J., Brindle, K. M., et al. (2016) · NMR in Biomedicine · doi:10.1002/nbm.3468 · Cited by 108 · see citing works
Tumor Heterogeneity in Pancreatic Adenocarcinoma
Cros, J. F., Raffenne, J., Couvelard, A., & Poté, N. (2017) · Pathobiology · doi:10.1159/000477773 · Cited by 102 · see citing works
Fast and precise automatic baseline correction of one- and two-dimensional nmr spectra
Dietrich, W., Rüdel, C. H., & Neumann, M. (1991) · Journal of Magnetic Resonance (1969) · doi:10.1016/0022-2364(91)90402-f · Cited by 99 · see citing works
Personalised medicine for cancer: from drug development into clinical practice
Jain, K. K. (2005) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.6.9.1463 · Cited by 85 · see citing works
3D Mass Spectrometry Imaging Reveals a Very Heterogeneous Drug Distribution in Tumors
Giordano, S., Morosi, L., Veglianese, P., Licandro, S. A., Frapolli, R., Zucchetti, M., Cappelletti, G., Falciola, L., Pifferi, V., Visentin, S., et al. (2016) · Scientific Reports · doi:10.1038/srep37027 · Cited by 82 · see citing works
Improved linear prediction of damped NMR signals using modified “forward-backward” linear prediction
Zhu, G., & Bax, A. (1992) · Journal of Magnetic Resonance (1969) · doi:10.1016/0022-2364(92)90379-l · Cited by 77 · see citing works
Dynamic Imaging of Glucose and Lactate Metabolism by 13C-MRS without Hyperpolarization
Brender, J., Kishimoto, S., Merkle, H., Reed, G. D., Hurd, R. E., Chen, A. P., Ardenkjær‐Larsen, J. H., Munasinghe, J., Saito, K., Seki, T., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-38981-1 · Cited by 75 · see citing works
Self-citationLane, A. N., & Fan, T. W. ‐. (2007) · Metabolomics · doi:10.1007/s11306-006-0047-x · Cited by 73 · see citing works
Self-citationIn vivo magnetic resonance imaging of glucose – initial experience
Allouche‐Arnon, H., Wade, T., Friesen‐Waldner, L. J., Miller, V. N., Gomori, J. M., Katz‐Brull, R., & McKenzie, C. A. (2012) · Contrast Media & Molecular Imaging · doi:10.1002/cmmi.1497 · Cited by 57 · see citing works
The use of dynamic nuclear polarization (13)C-pyruvate MRS in cancer.
Gutte, H., Hansen, A. E., Johannesen, H. H., Clemmensen, A., Ardenkjær‐Larsen, J. H., Nielsen, C. H., & Kjær, A. (2015) · Europe PMC (PubMed Central) · Cited by 53 · see citing works
Chiang, B., Wang, K., Ethier, C. R., & Prausnitz, M. R. (2017) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.16-20679 · Cited by 53 · see citing works
Matsumoto, S., Kishimoto, S., Saito, K., Takakusagi, Y., Munasinghe, J., Devasahayam, N., Hart, C. P., Gillies, R. J., Mitchell, J. B., & Krishna, M. C. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-0491 · Cited by 48 · see citing works
Self-citationMatsumoto, S., Saito, K., Takakusagi, Y., Matsuo, M., Munasinghe, J., Morris, H. D., Lizak, M. J., Merkle, H., Yasukawa, K., Devasahayam, N., et al. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5725 · Cited by 47 · see citing works
Self-citationTimm, K. N., Hartl, J., Keller, M. A., Hu, D., Kettunen, M. I., Rodrigues, T. B., Ralser, M., & Brindle, K. M. (2014) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25561 · Cited by 41 · see citing works
Liu, Q., Stewart, J., Wang, H., Rashid, A., Zhao, J., Katz, M. H. G., Lee, J. E., Fleming, J. B., Maitra, A., Wolff, R. A., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0171985 · Cited by 34 · see citing works
Wang, A. S., Lodi, A., Rivera, L. B., Izquierdo-García, J. L., Firpo, M. A., Mulvihill, S. J., Tempero, M. A., Bergers, G., & Ronen, S. M. (2014) · NMR in Biomedicine · doi:10.1002/nbm.3198 · Cited by 32 · see citing works
Bailey, K. M., Cornnell, H. H., Ibrahim‐Hashim, A., Wojtkowiak, J. W., Hart, C. P., Zhang, X., Leos, R. A., Martinez, G. V., Baker, A. F., & Gillies, R. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113586 · Cited by 30 · see citing works
Detection of necrosis in human tumour xenografts by proton magnetic resonance imaging
Jakobsen, I., Kaalhus, O., Lyng, H., & Rofstad, E. (1995) · British Journal of Cancer · doi:10.1038/bjc.1995.93 · Cited by 30 · see citing works
Mathews, E. H., Stander, A., Joubert, A. M., & Liebenberg, L. (2013) · Nutrition · doi:10.1016/j.nut.2013.07.024 · Cited by 28 · see citing works
Zhang, X., Wojtkowiak, J. W., Martinez, G. V., Cornnell, H. H., Hart, C. P., Baker, A. F., & Gillies, R. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0155289 · Cited by 25 · see citing works
Crooks, D. R., Fan, T. W. ‐., & Linehan, W. M. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9027-6_1 · Cited by 22 · see citing works
Self-citationKinetic modeling in pre-clinical positron emission tomography
Kuntner, C. (2014) · Zeitschrift für Medizinische Physik · doi:10.1016/j.zemedi.2014.02.003 · Cited by 17 · see citing works
Harada, M., Kubo, H., Abe, T., Maezawa, H., & Otsuka, H. (2010) · Japanese Journal of Radiology · doi:10.1007/s11604-009-0390-8 · Cited by 17 · see citing works
Assignment Strategies for Nuclear Magnetic Resonances in Metabolomic Research
Fan, T. W. ‐., & Lane, A. N. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9780511996634.028 · Cited by 9 · see citing works
Self-citationLiu, Y., Zhang, Y., Mao, X., Qi, Q., Zhu, M., Zhang, C., Pan, X., & Ling, Y. (2017) · Biomedical Reports · doi:10.3892/br.2017.1008 · Cited by 5 · see citing works
Approaching Pancreatic Cancer Phenotypes via Metabolomics
McGranaghan, P., Rennefahrt, U. E. E., Kamlage, B., Reszka, R. C., Schatz, P., Bethan, B., Mayerle, J. V., & Lerch, M. M. (2016) · Springer eBooks · doi:10.1007/978-1-4939-6631-8_61-1 · Cited by 2 · see citing works
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Pancreatic cancer: Advances and challenges
Halbrook, C. J., Lyssiotis, C. A., Pasca di Magliano, M., & Maitra, A. (2023) · Cell · doi:10.1016/j.cell.2023.02.014 · Cited by 1,321 · see citing works
Halbrook, C. J., Thurston, G., Boyer, S., Anaraki, C., Jiménez, J. A., McCarthy, A., Steele, N. G., Kerk, S. A., Hong, H. S., Lin, L., et al. (2022) · Nature Cancer · doi:10.1038/s43018-022-00463-1 · Cited by 80 · see citing works
Casingal, C. R., Kikkawa, T., Inada, H., Sasaki, Y., & Osumi, N. (2020) · Molecular Brain · doi:10.1186/s13041-020-00706-1 · Cited by 69 · see citing works
Region-level epimutation rates in Arabidopsis thaliana
Denkena, J., Johannes, F. M., & Colomé‐Tatché, M. (2021) · Heredity · doi:10.1038/s41437-021-00441-w · Cited by 65 · see citing works
Goldblum, R. R., McClellan, M., White, K., Gonzalez, S. J., Thompson, B. R., Vang, H. X., Cohen, H., Higgins, L., Markowski, T. W., Yang, T.-Y., et al. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.07.004 · Cited by 64 · see citing works
Théry, M., & Blanchoin, L. (2020) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.10.012 · Cited by 49 · see citing works
Object-Displacement-Sensitive Visual Neurons Drive Freezing in Drosophila
Tanaka, R., & Clark, D. A. (2020) · Current Biology · doi:10.1016/j.cub.2020.04.068 · Cited by 44 · see citing works
Metabolic imaging with deuterium labeled substrates
Low, J. C. M., Wright, A. J., Hesse, F., Cao, J., & Brindle, K. M. (2023) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2023.02.002 · Cited by 45 · see citing works
Jackson, H. O., Taunt, H. N., Mordaka, P. M., Smith, A. G., & Purton, S. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2021.708370 · Cited by 37 · see citing works
Magnetic resonance spectroscopy for the study of cns malignancies
Ruiz‐Rodado, V., Brender, J., Cherukuri, M. K., Gilbert, M. R., & Larion, M. (2020) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2020.11.001 · Cited by 37 · see citing works
Self-citationChen, H., Autry, A. W., Brender, J., Kishimoto, S., Krishna, M. C., Vareth, M., Bok, R., Reed, G. D., Carvajal, L. E., Gordon, J. W., et al. (2020) · Magnetic Resonance in Medicine · doi:10.1002/mrm.28328 · Cited by 34 · see citing works
Self-citationDeuterium MRSI characterizations of glucose metabolism in orthotopic pancreatic cancer mouse models
Marković, S., Roussel, T., Agemy, L., Sasson, K., Preise, D., Scherz, A. J., & Frydman, L. (2021) · NMR in Biomedicine · doi:10.1002/nbm.4569 · Cited by 30 · see citing works
Protective roles for myeloid cells in neuroinflammation
Owens, T., Benmamar‐Badel, A., Włodarczyk, A., Marczynska, J., Mørch, M. T., Dubik, M., Arengoth, D. S., Asgari, N., Webster, G., & Khorooshi, R. (2020) · Scandinavian Journal of Immunology · doi:10.1111/sji.12963 · Cited by 28 · see citing works
Gkiouli, M., Biechl, P., Eisenreich, W., & Otto, A. M. (2019) · Cells · doi:10.3390/cells8101113 · Cited by 24 · see citing works
Huang, J., Lai, J. H. C., Han, X., Chen, Z., Xiao, P., Liu, Y., Chen, L., Xu, J., & Chan, K. W. Y. (2021) · NMR in Biomedicine · doi:10.1002/nbm.4640 · Cited by 23 · see citing works
Real-Time insight into in vivo redox status utilizing hyperpolarized [1-13C] N-acetyl cysteine
Yamamoto, K., Opina, A. C. L., Sail, D., Blackman, B. N., Saito, K., Brender, J., Malinowski, R. M., Seki, T., Oshima, N., Crooks, D. R., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-90921-0 · Cited by 19 · see citing works
Self-citationQuantum Cognitive Triad: Semantic Geometry of Context Representation
Суров, И. А. (2020) · Foundations of Science · doi:10.1007/s10699-020-09712-x · Cited by 18 · see citing works
AbuSalim, J. E., Yamamoto, K., Miura, N., Blackman, B. N., Brender, J., Mushti, C., Seki, T., Camphausen, K. A., Swenson, R. E., Krishna, M. C., et al. (2021) · ACS Chemical Biology · doi:10.1021/acschembio.1c00561 · Cited by 18 · see citing works
Self-citationThe potential role of miRNA therapies in spinal muscle atrophy
Gandhi, G., Abdullah, S., Foead, A. I., & Yeo, W. W. Y. (2021) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2021.117485 · Cited by 17 · see citing works
Fan, T. W. ‐., Higashi, R. M., Chernayavskaya, Y., & Lane, A. N. (2020) · Metabolites · doi:10.3390/metabo10060249 · Cited by 16 · see citing works
Self-citationSpatiotemporal expression of IgLON family members in the developing mouse nervous system
Fearnley, S., Raja, R., & Cloutier, J. (2021) · Scientific Reports · doi:10.1038/s41598-021-97768-5 · Cited by 14 · see citing works
Najera, S. S., Ricketts, C. J., Schmidt, L. S., Medina, J. I., Saito, K., Ileva, L. V., Brender, J., James, A. E., Peer, C. J., Gouker, B. A., et al. (2024) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-24-0225 · Cited by 14 · see citing works
Self-citationMuñoz-Nava, L. M., Alvarez, H. A., Flores-Flores, M., Chara, O., & Nahmad, M. (2020) · Developmental Biology · doi:10.1016/j.ydbio.2020.03.009 · Cited by 13 · see citing works
Nannan, L., Gsell, W., Belderbos, S., Gallet, C., Wouters, J., Brassart‐Pasco, S., Himmelreich, U., & Brassart, B. (2023) · British Journal of Cancer · doi:10.1038/s41416-023-02242-w · Cited by 12 · see citing works
Overview and progress of X-nuclei magnetic resonance imaging in biomedical studies
Wang, G., Yang, H., Li, J., Wen, J., Zhong, K., & Tian, C. (2023) · Magnetic Resonance Letters · doi:10.1016/j.mrl.2023.05.002 · Cited by 9 · see citing works
Pravdivtsev, A. N., Sönnichsen, F. D., & Hövener, J. (2020) · PLoS ONE · doi:10.1371/journal.pone.0239982 · Cited by 9 · see citing works
Sun, P., Wu, Z., Lin, L., Hu, G., Zhang, X., & Wang, J. (2022) · NMR in Biomedicine · doi:10.1002/nbm.4845 · Cited by 8 · see citing works
Coherent polarization transfer in chemically exchanging systems
Pravdivtsev, A. N., & Hövener, J. (2020) · Physical Chemistry Chemical Physics · doi:10.1039/c9cp06873b · Cited by 7 · see citing works
Hyperpolarized 13C tracers: Technical advancements and perspectives for clinical applications
Fiedorowicz, M., Wieteska, M., Rylewicz, K., Kossowski, B., Piątkowska-Janko, E., Czarnecka, A. M., Toczyłowska, B., & Bogorodzki, P. (2021) · Journal of Applied Biomedicine · doi:10.1016/j.bbe.2021.03.010 · Cited by 7 · see citing works
Challenges of Spatially Resolved Metabolism in Cancer Research
Lane, A. N., Higashi, R. M., & Fan, T. W. ‐. (2024) · Metabolites · doi:10.3390/metabo14070383 · Cited by 7 · see citing works
Self-citationMetabolic and imaging phenotypes associated with RB1 and TP53 loss in prostate cancer
Ahmad, F., White, M. E., Yamamoto, K., Crooks, D. R., Agarwal, S., Yang, Y., Capaldo, B. J., Raj, S., Alilin, A. N., Ton, A., et al. (2025) · Neoplasia · doi:10.1016/j.neo.2025.101235 · Cited by 6 · see citing works
Self-citationSynthetic genomics for curing genetic diseases
Grazioli, S., & Petris, G. (2021) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2021.02.002 · Cited by 5 · see citing works
Molecular Imaging: Unveiling Metabolic Abnormalities in Pancreatic Cancer
Wang, H., Gui, Y., & Lv, K. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26115242 · Cited by 3 · see citing works
Single‐Cell Metabolic Imaging Reveals Glycogen‐Driven Adaptations in Endothelial Cells
Chadha, R. S., Yang, B. K., Yuan, D., Kapelczak, E. D., Kocheril, P. A., Tapia, A., Mahajan, S., Colazo, A., Malhi, N. K., Ambarian, J. A., et al. (2025) · Advanced Science · doi:10.1002/advs.202508517 · Cited by 3 · see citing works
Isocitrate Dehydrogenase Mutations in Cancer: From Bench to Bedside Applications
Fang, Y., Wang, X., Luo, K., Dakal, T. C., Bai, H., Xu, C., & Zhang, G. (2026) · MedComm · doi:10.1002/mco2.70732 · Cited by 4 · see citing works
Sawami, K., Naganuma, T., Yabe, H., Taki, T., Stewart, N. J., Uchio, Y., Takeda, N., Hatae, N., Hashimoto, T., Hirata, H., et al. (2024) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2024.3365195 · Cited by 3 · see citing works
Self-citationAssmann, J. C., Brender, J., Farthing, D. E., Saito, K., Kishimoto, S., Warrick, K. A., Maglakelidze, N., Crooks, D. R., Merkle, H., Gress, R. E., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/809327 · Cited by 3 · see citing works
Self-citationTomiyama, H., Yamasaki, M., Isagawa, T., Takeda, N., Hashimoto, T., Hirata, H., & Matsumoto, S. (2025) · Discover Nano · doi:10.1186/s11671-025-04304-9 · Cited by 2 · see citing works
Self-citationEditorial for “Hyperpolarized 13C Metabolic MRI of Patients with Pancreatic Ductal Adenocarcinoma”
Robb, F. J. L., & Chen, A. (2023) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.29163
Self-citationGenetically Encoded Glucosensor for Multiplexed 129Xe NMR
He, J., Rudman, N. A., Nisita, G., & Dmochowski, I. J. (2026) · ACS Sensors · doi:10.1021/acssensors.6c02887
- Authors
- Kishimoto, S., Brender, J. R., Crooks, D. R., Matsumoto, S., Seki, T., Oshima, N., Merkle, H., Lin, P., Reed, G., Chen, A. P., Ardenkjaer-Larsen, J. H., Munasinghe, J., Saito, K., Yamamoto, K., Choyke, P. L., Mitchell, J., Lane, A. N., Fan, T. W., Linehan, W. M., & Krishna, M. C.
- Affiliations
- National Institutes of Health (US)
- Hokkaido University (JP)
- University of Kentucky (US)
- GE HealthCare, Chicago, United States
- Corresponding author
- Brender, Jeffrey R
- Krishna, Murali C
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2019-08-13
- Volume
- 8
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC6706239
- OpenAlex
- W2968441812
- Cited by
- 41
- References
- 85
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 4 · 2023: 5 · 2022: 2 · 2021: 11 · 2020: 11 · 2019: 2
- FWCI
- 2.60
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- UKnowledge (University of Kentucky) (submittedVersion, public-domain)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion, other-oa)
- Kyoto University Research Information Repository (Kyoto University) (submittedVersion)
- Funders
- National Cancer Institute (1ZIASC006321-39, Intramural Research Program)
- Shared Resource(s) of the University of Kentucky Markey Cancer Center (P30CA177558)
- Topics
- Physical Sciences › Chemistry › Spectroscopy › Advanced NMR Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Keywords
- pancreatic ductal adenocarcinoma, 13C MRI, glucose metabolism, tumor heterogeneity, tumor subtypes, lactic acid production, noise reduction, tumor xenografts, metabolic imaging
- MeSH terms
- Adenocarcinoma, Animals, Carbon Isotopes, Disease Models, Animal, Glucose, Magnetic Resonance Imaging, Pancreatic Neoplasms, Carcinoma, Pancreatic Ductal, Mice
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