HR-MAS NMR Based Quantitative Metabolomics in Breast Cancer
Abstract
1. Introduction
2. Preanalytical Factors and Measurement Conditions
3. NMR Techniques Employed in Tissue Analysis
3.1. Water Suppression
3.2. Pulse Sequences for 1D-NMR
3.3. Pulse Sequences for 2D-NMR
4. Metabolites Identified with HR-MAS NMR in Breast Tumour Tissue
5. Metabolite Quantification with HR-MAS NMR
6. Significant Associations with Clinical Factors
7. Summary
Funding
Acknowledgments
Conflicts of Interest
References
- Perou, C.M.; Sørlie, T.; Eisen, M.B.; van de Rijn, M.; Jeffrey, S.S.; Rees, C.A.; Pollack, J.R.; Ross, D.T.; Johnsen, H.; Akslen, L.A.; et al. Molecular portraits of human breast tumours. Nature 2000, 406, 747–752. [Google Scholar] [CrossRef] [PubMed]
- Sørlie, T.; Perou, C.M.; Tibshirani, R.; Aas, T.; Geisler, S.; Johnsen, H.; Hastie, T.; Eisen, M.B.; van de Rijn, M.; Jeffrey, S.S.; et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. USA 2001, 98, 10869–10874. [Google Scholar] [CrossRef]
- Parker, J.S.; Mullins, M.; Cheang, M.C.U.; Leung, S.; Voduc, D.; Vickery, T.; Davies, S.; Fauron, C.; He, X.; Hu, Z.; et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 2009, 27, 1160–1167. [Google Scholar] [CrossRef] [PubMed]
- Paik, S.; Shak, S.; Tang, G.; Kim, C.; Baker, J.; Cronin, M.; Baehner, F.L.; Walker, M.G.; Watson, D.; Park, T.; et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. New Engl. J. Med. 2004, 351, 2817–2826. [Google Scholar] [CrossRef] [PubMed]
- Filipits, M.; Rudas, M.; Jakesz, R.; Dubsky, P.; Fitzal, F.; Singer, C.F.; Dietze, O.; Greil, R.; Jelen, A.; Sevelda, P.; et al. A new molecular predictor of distant recurrence in ER-positive, HER2-negative breast cancer adds independent information to conventional clinical risk factors. Clin. Cancer Res. An. Off. J. Am. Assoc. Cancer Res. 2011, 17, 6012–6020. [Google Scholar] [CrossRef] [PubMed]
- Sparano, J.A. Prognostic gene expression assays in breast cancer: Are two better than one? NPJ Breast Cancer 2018, 4, 11. [Google Scholar] [CrossRef] [PubMed]
- Wishart, D.S. Emerging applications of metabolomics in drug discovery and precision medicine. Nat. Rev. Drug Discov. 2016, 15, 473–484. [Google Scholar] [CrossRef]
- Nagana Gowda, G.A.; Raftery, D. Can NMR solve some significant challenges in metabolomics? J. Magn. Reson. (San Diego Calif 1997) 2015, 260, 144–160. [Google Scholar] [CrossRef] [PubMed]
- Maniara, G.; Rajamoorthi, K.; Rajan, S.; Stockton, G.W. Method performance and validation for quantitative analysis by (1)h and (31)p NMR spectroscopy. Applications to analytical standards and agricultural chemicals. Anal. Chem. 1998, 70, 4921–4928. [Google Scholar] [CrossRef]
- Mountford, C.; Ramadan, S.; Stanwell, P.; Malycha, P. Proton MRS of the breast in the clinical setting. NMR Biomed. 2009, 22, 54–64. [Google Scholar] [CrossRef] [PubMed]
- Beckonert, O.; Coen, M.; Keun, H.C.; Wang, Y.; Ebbels, T.M.D.; Holmes, E.; Lindon, J.C.; Nicholson, J.K. High-resolution magic-angle-spinning NMR spectroscopy for metabolic profiling of intact tissues. Nat. Protoc. 2010, 5, 1019–1032. [Google Scholar] [CrossRef] [PubMed]
- Martin, R.W.; Jachmann, R.C.; Sakellariou, D.; Nielsen, U.G.; Pines, A. High-resolution nuclear magnetic resonance spectroscopy of biological tissues using projected magic angle spinning. Magn. Reson. Med. 2005, 54, 253–257. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.-H.; Enloe, B.M.; Xiao, Y.; Cory, D.G.; Singer, S. Isotropic susceptibility shift under MAS: The origin of the split water resonances in 1H MAS NMR spectra of cell suspensions. Magn. Reson. Med. 2003, 50, 515–521. [Google Scholar] [CrossRef] [PubMed]
- Andrew, E.R.; Bradbury, A.; Eades, R.G. Removal of Dipolar Broadening of Nuclear Magnetic Resonance Spectra of Solids by Specimen Rotation. Nature 1959, 183, 1802–1803. [Google Scholar] [CrossRef]
- Lowe, I.J. Free Induction Decays of Rotating Solids. Phys. Rev. Lett. 1959, 2, 285–287. [Google Scholar] [CrossRef]
- Keifer, P.A.; Baltusis, L.; Rice, D.M.; Tymiak, A.A.; Shoolery, J.N. A Comparison of NMR Spectra Obtained for Solid-Phase-Synthesis Resins Using Conventional High-Resolution, Magic-Angle-Spinning, and High-Resolution Magic-Angle-Spinning Probes. J. Magn. Reson. Ser. A 1996, 119, 65–75. [Google Scholar] [CrossRef]
- Millis, K.K.; Maas, W.E.; Cory, D.G.; Singer, S. Gradient, high-resolution, magic-angle spinning nuclear magnetic resonance spectroscopy of human adipocyte tissue. Magn. Reson. Med. 1997, 38, 399–403. [Google Scholar] [CrossRef]
- Millis, K.; Weybright, P.; Campbell, N.; Fletcher, J.A.; Fletcher, C.D.; Cory, D.G.; Singer, S. Classification of human liposarcoma and lipoma using ex vivo proton NMR spectroscopy. Magn. Reson. Med. 1999, 41, 257–267. [Google Scholar] [CrossRef]
- Cheng, L.L.; Ma, M.J.; Becerra, L.; Ptak, T.; Tracey, I.; Lackner, A.; Gonzalez, R.G. Quantitative neuropathology by high resolution magic angle spinning proton magnetic resonance spectroscopy. Proc. Natl. Acad. Sci. 1997, 94, 6408–6413. [Google Scholar] [CrossRef]
- Cheng, L.L.; Lean, C.L.; Bogdanova, A.; Wright, S.C.; Ackerman, J.L.; Brady, T.J.; Garrido, L. Enhanced resolution of proton NMR spectra of malignant lymph nodes using magic-angle spinning. Magn. Reson. Med. 1996, 36, 653–658. [Google Scholar] [CrossRef]
- Doty, F.D.; Entzminger, G.; Yang, Y.A. Magnetism in high-resolution NMR probe design. I: General methods. Concepts Magn. Reson. 1998, 10, 133–156. [Google Scholar] [CrossRef]
- Doty, F.D.; Entzminger, G.; Yang, Y.A. Magnetism in high-resolution NMR probe design. II: HR MAS. Concepts Magn. Reson. 1998, 10, 239–260. [Google Scholar] [CrossRef]
- Tosi, R.; Tugnoli, V. Nuclear Magnetic Resonance Spectroscopy in the Study of Neoplastic Tissue; Nova Science: New York, NY, USA, 2005. [Google Scholar]
- Sitter, B.; Sonnewald, U.; Spraul, M.; Fjösne, H.E.; Gribbestad, I.S. High-resolution magic angle spinning MRS of breast cancer tissue. NMR Biomed. 2002, 15, 327–337. [Google Scholar] [CrossRef] [PubMed]
- Esteve, V.; Martínez-Granados, B.; Martínez-Bisbal, M.C. Pitfalls to be considered on the metabolomic analysis of biological samples by HR-MAS. Front. Chem. 2014, 2, 33. [Google Scholar] [CrossRef]
- Righi, V.; Schenetti, L.; Maiorana, A.; Libertini, E.; Bettelli, S.; Bonetti, L.R.; Mucci, A. Assessment of freezing effects and diagnostic potential of BioBank healthy and neoplastic breast tissues through HR-MAS NMR spectroscopy. Metabol. Off. J. Metabol. Soc. 2015, 11, 487–498. [Google Scholar] [CrossRef]
- Haukaas, T.H.; Moestue, S.A.; Vettukattil, R.; Sitter, B.; Lamichhane, S.; Segura, R.; Giskeødegård, G.F.; Bathen, T.F. Impact of Freezing Delay Time on Tissue Samples for Metabolomic Studies. Front. Oncol. 2016, 6, 17. [Google Scholar] [CrossRef] [PubMed]
- Opstad, K.S.; Bell, B.A.; Griffiths, J.R.; Howe, F.A. An investigation of human brain tumour lipids by high-resolution magic angle spinning 1H MRS and histological analysis. NMR Biomed. 2008, 21, 677–685. [Google Scholar] [CrossRef] [PubMed]
- Middleton, D.A.; Bradley, D.P.; Connor, S.C.; Mullins, P.G.; Reid, D.G. The effect of sample freezing on proton magic-angle spinning NMR spectra of biological tissue. Magn. Reson. Med. 1998, 40, 166–169. [Google Scholar] [CrossRef]
- Waters, N.J.; Garrod, S.; Farrant, R.D.; Haselden, J.N.; Connor, S.C.; Connelly, J.; Lindon, J.C.; Holmes, E.; Nicholson, J.K. High-resolution magic angle spinning (1)H NMR spectroscopy of intact liver and kidney: Optimization of sample preparation procedures and biochemical stability of tissue during spectral acquisition. Anal. Biochem. 2000, 282, 16–23. [Google Scholar] [CrossRef]
- Shabihkhani, M.; Lucey, G.M.; Wei, B.; Mareninov, S.; Lou, J.J.; Vinters, H.V.; Singer, E.J.; Cloughesy, T.F.; Yong, W.H. The procurement, storage, and quality assurance of frozen blood and tissue biospecimens in pathology, biorepository, and biobank settings. Clin. Biochem. 2014, 47, 258–266. [Google Scholar] [CrossRef]
- Jordan, K.W.; He, W.; Halpern, E.F.; Wu, C.-L.; Cheng, L.L. Evaluation of Tissue Metabolites with High Resolution Magic Angle Spinning MR Spectroscopy Human Prostate Samples after Three-Year Storage at −80 °C. BiomarkInsights 2017, 2, 117727190700200. [Google Scholar] [CrossRef]
- Giskeødegård, G.F.; Cao, M.D.; Bathen, T.F. High-resolution magic-angle-spinning NMR spectroscopy of intact tissue. Methods Mol. Biol. (Clifton, NJ) 2015, 1277, 37–50. [Google Scholar] [CrossRef]
- Bertilsson, H.; Angelsen, A.; Viset, T.; Skogseth, H.; Tessem, M.-B.; Halgunset, J. A new method to provide a fresh frozen prostate slice suitable for gene expression study and MR spectroscopy. Prostate 2011, 71, 461–469. [Google Scholar] [CrossRef] [PubMed]
- Gogiashvili, M.; Horsch, S.; Marchan, R.; Gianmoena, K.; Cadenas, C.; Tanner, B.; Naumann, S.; Ersova, D.; Lippek, F.; Rahnenführer, J.; et al. Impact of intratumoral heterogeneity of breast cancer tissue on quantitative metabolomics using high-resolution magic angle spinning 1 H NMR spectroscopy. NMR Biomed. 2018, 31. [Google Scholar] [CrossRef] [PubMed]
- Gogiashvili, M.; Edlund, K.; Gianmoena, K.; Marchan, R.; Brik, A.; Andersson, J.T.; Lambert, J.; Madjar, K.; Hellwig, B.; Rahnenführer, J.; et al. Metabolic profiling of ob/ob mouse fatty liver using HR-MAS 1H-NMR combined with gene expression analysis reveals alterations in betaine metabolism and the transsulfuration pathway. Anal. Bioanal. Chem. 2017, 409, 1591–1606. [Google Scholar] [CrossRef] [PubMed]
- Cao, M.D.; Giskeødegård, G.F.; Bathen, T.F.; Sitter, B.; Bofin, A.; Lønning, P.E.; Lundgren, S.; Gribbestad, I.S. Prognostic value of metabolic response in breast cancer patients receiving neoadjuvant chemotherapy. BMC Cancer 2012, 12, 39. [Google Scholar] [CrossRef]
- Cao, M.D.; Sitter, B.; Bathen, T.F.; Bofin, A.; Lønning, P.E.; Lundgren, S.; Gribbestad, I.S. Predicting long-term survival and treatment response in breast cancer patients receiving neoadjuvant chemotherapy by MR metabolic profiling. NMR Biomed. 2012, 25, 369–378. [Google Scholar] [CrossRef] [PubMed]
- Sitter, B.; Bathen, T.F.; Singstad, T.E.; Fjøsne, H.E.; Lundgren, S.; Halgunset, J.; Gribbestad, I.S. Quantification of metabolites in breast cancer patients with different clinical prognosis using HR MAS MR spectroscopy. NMR Biomed. 2010, 23, 424–431. [Google Scholar] [CrossRef]
- Moestue, S.A.; Borgan, E.; Huuse, E.M.; Lindholm, E.M.; Sitter, B.; Børresen-Dale, A.-L.; Engebraaten, O.; Maelandsmo, G.M.; Gribbestad, I.S. Distinct choline metabolic profiles are associated with differences in gene expression for basal-like and luminal-like breast cancer xenograft models. BMC Cancer 2010, 10, 433. [Google Scholar] [CrossRef] [PubMed]
- Sitter, B.; Lundgren, S.; Bathen, T.F.; Halgunset, J.; Fjosne, H.E.; Gribbestad, I.S. Comparison of HR MAS MR spectroscopic profiles of breast cancer tissue with clinical parameters. NMR Biomed. 2006, 19, 30–40. [Google Scholar] [CrossRef]
- Grinde, M.T.; Skrbo, N.; Moestue, S.A.; Rødland, E.A.; Borgan, E.; Kristian, A.; Sitter, B.; Bathen, T.F.; Børresen-Dale, A.-L.; Mælandsmo, G.M.; et al. Interplay of choline metabolites and genes in patient-derived breast cancer xenografts. Breast Cancer Res. BCR 2014, 16, R5. [Google Scholar] [CrossRef] [PubMed]
- Euceda, L.R.; Haukaas, T.H.; Giskeødegård, G.F.; Vettukattil, R.; Engel, J.; Silwal-Pandit, L.; Lundgren, S.; Borgen, E.; Garred, Ø.; Postma, G.; et al. Evaluation of metabolomic changes during neoadjuvant chemotherapy combined with bevacizumab in breast cancer using MR spectroscopy. Metabol. Off. J. Metabol. Soc. 2017, 13, 80. [Google Scholar] [CrossRef]
- Euceda, L.R.; Hill, D.K.; Stokke, E.; Hatem, R.; El Botty, R.; Bièche, I.; Marangoni, E.; Bathen, T.F.; Moestue, S.A. Metabolic Response to Everolimus in Patient-Derived Triple-Negative Breast Cancer Xenografts. J. Proteome Res. 2017, 16, 1868–1879. [Google Scholar] [CrossRef] [PubMed]
- Haukaas, T.H.; Euceda, L.R.; Giskeødegård, G.F.; Lamichhane, S.; Krohn, M.; Jernström, S.; Aure, M.R.; Lingjærde, O.C.; Schlichting, E.; Garred, Ø.; et al. Metabolic clusters of breast cancer in relation to gene- and protein expression subtypes. Cancer Metabol. 2016, 4, 12. [Google Scholar] [CrossRef] [PubMed]
- Bathen, T.F.; Jensen, L.R.; Sitter, B.; Fjösne, H.E.; Halgunset, J.; Axelson, D.E.; Gribbestad, I.S.; Lundgren, S. MR-determined metabolic phenotype of breast cancer in prediction of lymphatic spread, grade, and hormone status. Breast Cancer Res. Treat. 2007, 104, 181–189. [Google Scholar] [CrossRef] [PubMed]
- Choi, J.S.; Baek, H.-M.; Kim, S.; Kim, M.J.; Youk, J.H.; Moon, H.J.; Kim, E.-K.; Han, K.H.; Kim, D.-H.; Kim, S.I.; et al. HR-MAS MR spectroscopy of breast cancer tissue obtained with core needle biopsy: Correlation with prognostic factors. PLoS ONE 2012, 7, e51712. [Google Scholar] [CrossRef] [PubMed]
- Choi, J.S.; Baek, H.-M.; Kim, S.; Kim, M.J.; Youk, J.H.; Moon, H.J.; Kim, E.-K.; Nam, Y.K. Magnetic resonance metabolic profiling of breast cancer tissue obtained with core needle biopsy for predicting pathologic response to neoadjuvant chemotherapy. PLoS ONE 2013, 8, e83866. [Google Scholar] [CrossRef] [PubMed]
- Cheng, L.L.; Chang, I.W.; Smith, B.L.; Gonzalez, R.G. Evaluating human breast ductal carcinomas with high-resolution magic-angle spinning proton magnetic resonance spectroscopy. J. Magn. Reson. (San Diego Calif 1997) 1998, 135, 194–202. [Google Scholar] [CrossRef]
- Park, V.Y.; Yoon, D.; Koo, J.S.; Kim, E.-K.; Kim, S.I.; Choi, J.S.; Park, S.; Park, H.S.; Kim, S.; Kim, M.J. Intratumoral Agreement of High-Resolution Magic Angle Spinning Magnetic Resonance Spectroscopic Profiles in the Metabolic Characterization of Breast Cancer. Medicine 2016, 95, e3398. [Google Scholar] [CrossRef]
- Li, M.; Song, Y.; Cho, N.; Chang, J.M.; Koo, H.R.; Yi, A.; Kim, H.; Park, S.; Moon, W.K. An HR-MAS MR metabolomics study on breast tissues obtained with core needle biopsy. PLoS ONE 2011, 6, e25563. [Google Scholar] [CrossRef]
- Taylor, J.L.; Wu, C.-L.; Cory, D.; Gonzalez, R.G.; Bielecki, A.; Cheng, L.L. High-resolution magic angle spinning proton NMR analysis of human prostate tissue with slow spinning rates. Magn. Reson. Med. 2003, 50, 627–632. [Google Scholar] [CrossRef] [PubMed]
- Weybright, P.; Millis, K.; Campbell, N.; Cory, D.G.; Singer, S. Gradient, high-resolution, magic angle spinning1H nuclear magnetic resonance spectroscopy of intact cells. Magn. Reson. Med. 1998, 39, 337–345. [Google Scholar] [CrossRef] [PubMed]
- Aime, S.; Bruno, E.; Cabella, C.; Colombatto, S.; Digilio, G.; Mainero, V. HR-MAS of cells: A “cellular water shift” due to water-protein interactions? Magn. Reson. Med. 2005, 54, 1547–1552. [Google Scholar] [CrossRef] [PubMed]
- André, M.; Dumez, J.-N.; Rezig, L.; Shintu, L.; Piotto, M.; Caldarelli, S. Complete protocol for slow-spinning high-resolution magic-angle spinning NMR analysis of fragile tissues. Anal. Chem. 2014, 86, 10749–10754. [Google Scholar] [CrossRef]
- Chae, E.Y.; Shin, H.J.; Kim, S.; Baek, H.-M.; Yoon, D.; Kim, S.; Shim, Y.E.; Kim, H.H.; Cha, J.H.; Choi, W.J.; et al. The Role of High-Resolution Magic Angle Spinning 1H Nuclear Magnetic Resonance Spectroscopy for Predicting the Invasive Component in Patients with Ductal Carcinoma In Situ Diagnosed on Preoperative Biopsy. PLoS ONE 2016, 11, e0161038. [Google Scholar] [CrossRef] [PubMed]
- Renault, M.; Shintu, L.; Piotto, M.; Caldarelli, S. Slow-spinning low-sideband HR-MAS NMR spectroscopy: Delicate analysis of biological samples. Sci. Rep. 2013, 3, 3349. [Google Scholar] [CrossRef] [PubMed]
- Hoult, D.I. Solvent peak saturation with single phase and quadrature fourier transformation. J. Magn. Reson. (1969) 1976, 21, 337–347. [Google Scholar] [CrossRef]
- Tzika, A.A.; Cheng, L.L.; Goumnerova, L.; Madsen, J.R.; Zurakowski, D.; Astrakas, L.G.; Zarifi, M.K.; Scott, R.M.; Anthony, D.C.; Gonzalez, R.G.; et al. Biochemical characterization of pediatric brain tumors by using in vivo and ex vivo magnetic resonance spectroscopy. J. Neurosurg. 2002, 96, 1023–1031. [Google Scholar] [CrossRef]
- Cheng, L.L.; Chang, I.W.; Louis, D.N.; Gonzalez, R.G. Correlation of high-resolution magic angle spinning proton magnetic resonance spectroscopy with histopathology of intact human brain tumor specimens. Cancer Res. 1998, 58, 1825–1832. [Google Scholar]
- Barton, S.J.; Howe, F.A.; Tomlins, A.M.; Cudlip, S.A.; Nicholson, J.K.; Anthony Bell, B.; Griffiths, J.R. Comparison of in vivo1H MRS of human brain tumours with1H HR-MAS spectroscopy of intact biopsy samples in vitro. MAGMA 1999, 8, 121–128. [Google Scholar] [CrossRef]
- Ludwig, C.; Viant, M.R. Two-dimensional J-resolved NMR spectroscopy: Review of a key methodology in the metabolomics toolbox. Phytochem. Anal. PCA 2010, 21, 22–32. [Google Scholar] [CrossRef]
- Palmer, A.G.; Cavanagh, J.; Wright, P.E.; Rance, M. Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy. J. Magn. Reson. (1969) 1991, 93, 151–170. [Google Scholar] [CrossRef]
- Morris, G.A.; Freeman, R. Enhancement of nuclear magnetic resonance signals by polarization transfer. J. Am. Chem. Soc. 1979, 101, 760–762. [Google Scholar] [CrossRef]
- Ravikumar, M.; Bothner-By, A.A. A two-dimensional NMR experiment for the correlation of spin-locked and free-precession frequencies. J. Am. Chem. Soc. 1993, 115, 7537–7538. [Google Scholar] [CrossRef]
- Kupce, E.; Keifer, P.A.; Delepierre, M. Adiabatic TOCSY MAS in liquids. J. Magn. Reson. (San Diego Calif 1997) 2001, 148, 115–120. [Google Scholar] [CrossRef]
- Wieruszeski, J.M.; Montagne, G.; Chessari, G.; Rousselot-Pailley, P.; Lippens, G. Rotor synchronization of radiofrequency and gradient pulses in high-resolution magic angle spinning NMR. J. Magn. Reson. (San Diego Calif 1997) 2001, 152, 95–102. [Google Scholar] [CrossRef]
- Yoon, H.; Yoon, D.; Yun, M.; Choi, J.S.; Park, V.Y.; Kim, E.-K.; Jeong, J.; Koo, J.S.; Yoon, J.H.; Moon, H.J.; et al. Metabolomics of Breast Cancer Using High-Resolution Magic Angle Spinning Magnetic Resonance Spectroscopy: Correlations with 18F-FDG Positron Emission Tomography-Computed Tomography, Dynamic Contrast-Enhanced and Diffusion-Weighted Imaging MRI. PLoS ONE 2016, 11, e0159949. [Google Scholar] [CrossRef]
- Antzutkin, O.N.; Shekar, S.C.; Levitt, M.H. Two-Dimensional Sideband Separation in Magic-Angle-Spinning NMR. J. Magn. Reson. Ser. A 1995, 115, 7–19. [Google Scholar] [CrossRef]
- Hu, J.Z.; Wang, W.; Liu, F.; Solum, M.S.; Alderman, D.W.; Pugmire, R.J.; Grant, D.M. Magic-Angle-Turning Experiments for Measuring Chemical-Shift-Tensor Principal Values in Powdered Solids. J. Magn. Reson. Ser. A 1995, 113, 210–222. [Google Scholar] [CrossRef]
- Aguilar, J.A.; Nilsson, M.; Bodenhausen, G.; Morris, G.A. Spin echo NMR spectra without J modulation. Chem. Commun. (Camb. Engl.) 2012, 48, 811–813. [Google Scholar] [CrossRef] [PubMed]
- Esmaeili, M.; Bathen, T.F.; Engebråten, O.; Mælandsmo, G.M.; Gribbestad, I.S.; Moestue, S.A. Quantitative (31)P HR-MAS MR spectroscopy for detection of response to PI3K/mTOR inhibition in breast cancer xenografts. Magn. Reson. Med. 2014, 71, 1973–1981. [Google Scholar] [CrossRef]
- Swanson, M.G.; Zektzer, A.S.; Tabatabai, Z.L.; Simko, J.; Jarso, S.; Keshari, K.R.; Schmitt, L.; Carroll, P.R.; Shinohara, K.; Vigneron, D.B.; et al. Quantitative analysis of prostate metabolites using 1H HR-MAS spectroscopy. Magn. Reson. Med. 2006, 55, 1257–1264. [Google Scholar] [CrossRef] [PubMed]
- Martínez-Bisbal, M.C.; Monleon, D.; Assemat, O.; Piotto, M.; Piquer, J.; Llácer, J.L.; Celda, B. Determination of metabolite concentrations in human brain tumour biopsy samples using HR-MAS and ERETIC measurements. NMR Biomed. 2009, 22, 199–206. [Google Scholar] [CrossRef] [PubMed]
- Kriat, M.; Confort-Gouny, S.; Vion-Dury, J.; Sciaky, M.; Viout, P.; Cozzone, P.J. Quantitation of metabolites in human blood serum by proton magnetic resonance spectroscopy. A comparative study of the use of formate and TSP as concentration standards. NMR Biomed. 1992, 5, 179–184. [Google Scholar] [CrossRef] [PubMed]
- Albers, M.J.; Butler, T.N.; Rahwa, I.; Bao, N.; Keshari, K.R.; Swanson, M.G.; Kurhanewicz, J. Evaluation of the ERETIC method as an improved quantitative reference for 1H HR-MAS spectroscopy of prostate tissue. Magn. Reson. Med. 2009, 61, 525–532. [Google Scholar] [CrossRef] [PubMed]
- Kostidis, S.; Addie, R.D.; Morreau, H.; Mayboroda, O.A.; Giera, M. Quantitative NMR analysis of intra- and extracellular metabolism of mammalian cells: A tutorial. Anal. Chim. Acta 2017, 980, 1–24. [Google Scholar] [CrossRef] [PubMed]
- Nowick, J.S.; Khakshoor, O.; Hashemzadeh, M.; Brower, J.O. DSA: A new internal standard for NMR studies in aqueous solution. Org. Lett. 2003, 5, 3511–3513. [Google Scholar] [CrossRef] [PubMed]
- Alum, M.F.; Shaw, P.A.; Sweatman, B.C.; Ubhi, B.K.; Haselden, J.N.; Connor, S.C. 4,4-Dimethyl-4-silapentane-1-ammonium trifluoroacetate (DSA), a promising universal internal standard for NMR-based metabolic profiling studies of biofluids, including blood plasma and serum. Metabol. Off. J. Metabol. Soc. 2008, 4, 122–127. [Google Scholar] [CrossRef]
- Barker, P.B.; Soher, B.J.; Blackband, S.J.; Chatham, J.C.; Mathews, V.P.; Bryan, R.N. Quantitation of proton NMR spectra of the human brain using tissue water as an internal concentration reference. NMR Biomed. 1993, 6, 89–94. [Google Scholar] [CrossRef] [PubMed]
- Barantin, L.; Le Pape, A.; Akoka, S. A new method for absolute quantitation MRS metabolites. Magn. Reson. Med. 1997, 38, 179–182. [Google Scholar] [CrossRef]
- Akoka, S.; Barantin, L.; Trierweiler, M. Concentration Measurement by Proton NMR Using the ERETIC Method. Anal. Chem. 1999, 71, 2554–2557. [Google Scholar] [CrossRef] [PubMed]
- Wider, G.; Dreier, L. Measuring protein concentrations by NMR spectroscopy. J. Am. Chem. Soc. 2006, 128, 2571–2576. [Google Scholar] [CrossRef] [PubMed]
- Borgan, E.; Sitter, B.; Lingjærde, O.C.; Johnsen, H.; Lundgren, S.; Bathen, T.F.; Sørlie, T.; Børresen-Dale, A.-L.; Gribbestad, I.S. Merging transcriptomics and metabolomics—Advances in breast cancer profiling. BMC Cancer 2010, 10, 628. [Google Scholar] [CrossRef] [PubMed]
- Giskeødegård, G.F.; Lundgren, S.; Sitter, B.; Fjøsne, H.E.; Postma, G.; Buydens, L.M.C.; Gribbestad, I.S.; Bathen, T.F. Lactate and glycine-potential MR biomarkers of prognosis in estrogen receptor-positive breast cancers. NMR Biomed. 2012, 25, 1271–1279. [Google Scholar] [CrossRef] [PubMed]
- He, Q.H.; Shungu, D.C.; Vanzijl, P.C.M.; Bhujwalla, Z.M.; Glickson, J.D. Single-Scan in Vivo Lactate Editing with Complete Lipid and Water Suppression by Selective Multiple-Quantum-Coherence Transfer (Sel-MQC) with Application to Tumors. J. Magn. Reson. Ser. B 1995, 106, 203–211. [Google Scholar] [CrossRef]
- Holbach, M.; Lambert, J.; Suter, D. Optimized multiple-quantum filter for robust selective excitation of metabolite signals. J. Magn. Reson. (San Diego Calif 1997) 2014, 243, 8–16. [Google Scholar] [CrossRef]
- Holbach, M.; Lambert, J.; Johst, S.; Ladd, M.E.; Suter, D. Optimized selective lactate excitation with a refocused multiple-quantum filter. J. Magn. Reson. (San Diego Calif 1997) 2015, 255, 34–38. [Google Scholar] [CrossRef]
- Maximov, I.I.; Tosner, Z.; Nielsen, N.C. Optimal control design of NMR and dynamic nuclear polarization experiments using monotonically convergent algorithms. J. Chem. Phys. 2008, 128, 184505. [Google Scholar] [CrossRef]
- Ye, T.; Zheng, C.; Zhang, S.; Gowda, G.A.N.; Vitek, O.; Raftery, D. “Add to subtract”: A simple method to remove complex background signals from the 1H nuclear magnetic resonance spectra of mixtures. Anal. Chem. 2012, 84, 994–1002. [Google Scholar] [CrossRef]
- Provencher, S.W. Estimation of metabolite concentrations from localizedin vivo proton NMR spectra. Magn. Reson. Med. 1993, 30, 672–679. [Google Scholar] [CrossRef]
- Provencher, S.W. Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed. 2001, 14, 260–264. [Google Scholar] [CrossRef] [PubMed]
- Bathen, T.F.; Geurts, B.; Sitter, B.; Fjøsne, H.E.; Lundgren, S.; Buydens, L.M.; Gribbestad, I.S.; Postma, G.; Giskeødegård, G.F. Feasibility of MR metabolomics for immediate analysis of resection margins during breast cancer surgery. PLoS ONE 2013, 8, e61578. [Google Scholar] [CrossRef] [PubMed]
- Martelotto, L.G.; Ng, C.K.Y.; Piscuoglio, S.; Weigelt, B.; Reis-Filho, J.S. Breast cancer intra-tumor heterogeneity. Breast Cancer Res. BCR 2014, 16, 210. [Google Scholar] [CrossRef] [PubMed]
- Ng, C.K.Y.; Pemberton, H.N.; Reis-Filho, J.S. Breast cancer intratumor genetic heterogeneity: Causes and implications. Expert Rev. Anticancer Ther. 2012, 12, 1021–1032. [Google Scholar] [CrossRef] [PubMed]
- Cao, M.D.; Lamichhane, S.; Lundgren, S.; Bofin, A.; Fjøsne, H.; Giskeødegård, G.F.; Bathen, T.F. Metabolic characterization of triple negative breast cancer. BMC Cancer 2014, 14, 941. [Google Scholar] [CrossRef] [PubMed]
- Curigliano, G.; Burstein, H.J.; P Winer, E.; Gnant, M.; Dubsky, P.; Loibl, S.; Colleoni, M.; Regan, M.M.; Piccart-Gebhart, M.; Senn, H.-J.; et al. De-escalating and escalating treatments for early-stage breast cancer: The St. Gallen International Expert Consensus Conference on the Primary Therapy of Early Breast Cancer 2017. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2017, 28, 1700–1712. [Google Scholar] [CrossRef] [PubMed]
- Giskeødegård, G.F.; Grinde, M.T.; Sitter, B.; Axelson, D.E.; Lundgren, S.; Fjøsne, H.E.; Dahl, S.; Gribbestad, I.S.; Bathen, T.F. Multivariate modeling and prediction of breast cancer prognostic factors using MR metabolomics. J. Proteome Res. 2010, 9, 972–979. [Google Scholar] [CrossRef]
- Cortazar, P.; Zhang, L.; Untch, M.; Mehta, K.; Costantino, J.P.; Wolmark, N.; Bonnefoi, H.; Cameron, D.; Gianni, L.; Valagussa, P.; et al. Pathological complete response and long-term clinical benefit in breast cancer: The CTNeoBC pooled analysis. Lancet 2014, 384, 164–172. [Google Scholar] [CrossRef]
- Bingol, K. Recent Advances in Targeted and Untargeted Metabolomics by NMR and MS/NMR Methods. High.-Throughput 2018, 7. [Google Scholar] [CrossRef]
Gogiashvili et al. 2018 # (A) | Tayyari et al. 2018 # | Euceda et al. 2017a # | Euceda et al. 2017b $ | Park et al. 2016 # (B) | Yoon 2016 # (B) | Haukaas 2016a $ | Haukaas 2016b # | Chae 2016 # (B) | Cao et al. 2014 # | Grinde et al. 2014 $ (C) | Choi et al. 2013 # (B) | Borgan et al. 2013 $ (A) | Bathen et al. 2013 # | Giskeødegård et al. 2012 # | Cao et al. 2012b # | Cao et al. 2012a # (A) | Choi et al. 2012 # (B) | Li et al. 2011 # | Sitter et al. 2010 # (A) | Moestue et al. 2010 # $ (A) | Borgan et al. 2010 # | Giskeødegård et al. 2010 # | Bathen et al. 2007 # | Sitter et al. 2006 # (B) | Sitter et al. 2002 # | Cheng et al. 1998 # | |
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3-Hydroxybutyrate | Q | ||||||||||||||||||||||||||
Acetate | Q | Q | Q | R | I | R | I | ||||||||||||||||||||
Adipate | Q | ||||||||||||||||||||||||||
Alanine | Q | R | R | R | Q | Q | R | R | Q | R | Q | R | I | I | Q | I | I | I | I | I | |||||||
Arginine | R | Q | Q | I | |||||||||||||||||||||||
Ascorbate | Q | R | R | R | R | R | I | I | |||||||||||||||||||
Asparagine | Q | Q | I | I | |||||||||||||||||||||||
Aspartate | Q | Q | Q | I | I | I | I | ||||||||||||||||||||
ATP | R | ||||||||||||||||||||||||||
Betaine | Q | Q | Q | I | |||||||||||||||||||||||
Choline | Q | R | R | R | Q | Q | R | R | Q | R | Q | Q | Q | R | I | R | Q | Q | I | Q | Q | I | I | I | Q | I | I |
Creatine | Q | R | R | R | Q | Q | R | R | Q | R | I | Q | Q | R | I | I | I | Q | I | Q | Q | I | I | I | Q | I | I |
Ethanol | Q | ||||||||||||||||||||||||||
Ethanolamine | Q | Q | |||||||||||||||||||||||||
Formate | I | ||||||||||||||||||||||||||
Fumarate | Q | Q | |||||||||||||||||||||||||
Glucose | Q | R | R | R | Q | Q | R | R | I | I | R | I | R | I | Q | I | I | Q | I | ||||||||
Glutamate | Q | R | R | R | Q | Q | R | R | I | R | I | I | R | I | I | I | I | I | |||||||||
Glutamine | Q | R | R | R | Q | Q | R | R | I | R | I | R | I | I | I | ||||||||||||
Glutathione | Q | R | R | R | R | R | |||||||||||||||||||||
Glycerol | Q | Q | I | ||||||||||||||||||||||||
Glycine | Q | R | R | R | Q | Q | R | R | Q | R | I | Q | Q | R | R | R | Q | Q | I | Q | Q | I | I | I | Q | I | I |
GPC | Q | R | R | Q | Q | R | R | Q | I | Q | Q | Q | R | I | R | Q | Q | Q | Q | I | I | I | Q | I | |||
Histidine | Q | Q | I | ||||||||||||||||||||||||
Inosine | Q | I | |||||||||||||||||||||||||
Isoleucine | Q | Q | Q | I | I | I | I | ||||||||||||||||||||
Lactate | Q | R | R | R | Q | Q | R | R | I | R | I | I | Q | R | R | R | I | I | I | Q | I | I | I | I | I | I | |
Leucine | Q | R | Q | Q | I | I | I | I | |||||||||||||||||||
Lysine | Q | R | Q | Q | I | I | I | I | |||||||||||||||||||
Methionine | Q | R | Q | Q | |||||||||||||||||||||||
myo-Inositol | Q | R | R | R | Q | Q | R | R | Q | I | I | Q | R | Q | I | Q | I | I | Q | I | |||||||
O-Phosphocholine | Q | R | R | R | Q | Q | R | R | Q | R | Q | Q | Q | R | I | R | Q | Q | I | Q | Q | I | I | I | Q | I | I |
O-Phosphoethanolamine | Q | Q | Q | I | I | I | I | ||||||||||||||||||||
Phenylalanine | Q | R | Q | Q | I | I | |||||||||||||||||||||
Proline | Q | Q | Q | ||||||||||||||||||||||||
scyllo-Inositol | Q | R | R | I | R | Q | I | I | I | ||||||||||||||||||
Serine | Q | Q | Q | I | |||||||||||||||||||||||
Succinate | Q | R | R | R | R | Q | R | I | Q | I | |||||||||||||||||
Taurine | Q | R | R | R | Q | Q | R | R | Q | I | I | Q | Q | R | I | R | Q | Q | I | Q | Q | I | I | I | Q | I | I |
Threonine | Q | R | Q | Q | |||||||||||||||||||||||
Tyrosine | Q | R | R | R | Q | Q | R | R | I | I | |||||||||||||||||
Uracil | Q | Q | I | ||||||||||||||||||||||||
Uridine | R | ||||||||||||||||||||||||||
Valine | Q | R | Q | Q | I | I | I | I | I |
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Share and Cite
Gogiashvili, M.; Nowacki, J.; Hergenröder, R.; Hengstler, J.G.; Lambert, J.; Edlund, K. HR-MAS NMR Based Quantitative Metabolomics in Breast Cancer. Metabolites 2019, 9, 19. https://doi.org/10.3390/metabo9020019
Gogiashvili M, Nowacki J, Hergenröder R, Hengstler JG, Lambert J, Edlund K. HR-MAS NMR Based Quantitative Metabolomics in Breast Cancer. Metabolites. 2019; 9(2):19. https://doi.org/10.3390/metabo9020019
Chicago/Turabian StyleGogiashvili, Mikheil, Jessica Nowacki, Roland Hergenröder, Jan G. Hengstler, Jörg Lambert, and Karolina Edlund. 2019. "HR-MAS NMR Based Quantitative Metabolomics in Breast Cancer" Metabolites 9, no. 2: 19. https://doi.org/10.3390/metabo9020019
APA StyleGogiashvili, M., Nowacki, J., Hergenröder, R., Hengstler, J. G., Lambert, J., & Edlund, K. (2019). HR-MAS NMR Based Quantitative Metabolomics in Breast Cancer. Metabolites, 9(2), 19. https://doi.org/10.3390/metabo9020019