In vivo absolute quantification of hepatic γ-ATP concentration in mice using


Journal

NMR in biomedicine
ISSN: 1099-1492
Titre abrégé: NMR Biomed
Pays: England
ID NLM: 8915233

Informations de publication

Date de publication:
02 2021
Historique:
received: 03 04 2020
revised: 14 09 2020
accepted: 15 09 2020
pubmed: 8 10 2020
medline: 19 11 2021
entrez: 7 10 2020
Statut: ppublish

Résumé

Measurement of ATP concentrations and synthesis in humans indicated abnormal hepatic energy metabolism in obesity, non-alcoholic fatty liver disease (NAFLD) and Type 2 diabetes. Further mechanistic studies on energy metabolism require the detailed phenotyping of specific mouse models. Thus, this study aimed to establish and evaluate a robust and fast single voxel

Identifiants

pubmed: 33025629
doi: 10.1002/nbm.4422
doi:

Substances chimiques

Recombinant Proteins 0
Sterol Regulatory Element Binding Protein 1 0
Phosphorus 27YLU75U4W
Adenosine Triphosphate 8L70Q75FXE

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e4422

Informations de copyright

© 2020 The Authors. NMR in Biomedicine published by John Wiley & Sons Ltd.

Références

Koliaki C, Roden M. Alterations of mitochondrial function and insulin sensitivity in human obesity and diabetes mellitus. Annu Rev Nutr. 2016;36(1):337-367. https://doi.org/10.1038/s41586-019-1797-8
Roden M, Shulman GI. The integrative biology of type 2 diabetes. Nature. 2019;576(7785):51-60. https://doi.org/10.1038/s41586-019-1797-8
Szendroedi J, Phielix E, Roden M. The role of mitochondria in insulin resistance and type 2 diabetes mellitus. Nat Rev Endocrinol. 2012;8(2):92-103. https://doi.org/10.1038/nrendo.2011.138
Koliaki C, Szendroedi J, Kaul K, et al. Adaptation of hepatic mitochondrial function in humans with non-alcoholic fatty liver is lost in steatohepatitis. Cell Metab. 2015;21(5):739-746. https://doi.org/10.1016/j.cmet.2015.04.004
Meyerhoff DJ, Karczmar GS, Matson GB, Boska MD, Weiner MW. Non-invasive quantitation of human liver metabolites using image-guided 31P magnetic resonance spectroscopy. NMR Biomed. 1990;3(1):17-22.
Li CW, Negendank WG, Murphy-Boesch J, Padavic-Shaller K, Brown TR. Molar quantitation of hepatic metabolites in vivo in proton-decoupled, nuclear overhauser effect enhanced 31P NMR spectra localized by three-dimensional chemical shift imaging. NMR Biomed. 1996;9(4):141-155. https://doi.org/10.1002/(SICI)1099-1492(199606)9:4<141::AID-NBM403>3.0.CO;2-P
Laufs A, Livingstone R, Nowotny B, et al. Quantitative liver 31P magnetic resonance spectroscopy at 3T on a clinical scanner. Magn Reson Med. 2014;71(5):1670-1675. https://doi.org/10.1002/mrm.24835
Szendroedi J, Chmelik M, Schmid AI, et al. Abnormal hepatic energy homeostasis in type 2 diabetes. Hepatology. 2009;50(4):1079-1086. https://doi.org/10.1002/hep.23093
Chmelík M, Schmid AI, Gruber S, et al. Three-dimensional high-resolution magnetic resonance spectroscopic imaging for absolute quantification of 31P metabolites in human liver. Magn Reson Med. 2008;60(4):796-802. https://doi.org/10.1002/mrm.21762
Valkovic L, Chmelik M, Krššák M. In-vivo 31P-MRS of skeletal muscle and liver: a way for non-invasive assessment of their metabolism. Anal Biochem. 2017;529:193-215. https://doi.org/10.1016/j.ab.2017.01.018
Pfleger L, Gajdošík M, Wolf P, et al. Absolute quantification of phosphor-containing metabolites in the liver using 31P MRSI and hepatic lipid volume correction at 7T suggests no dependence on body mass index or age. J Magn Reson Imaging. 2019;49(2):597-607. https://doi.org/10.1002/jmri.26225
Fritsch M, Koliaki C, Livingstone R, et al. Time course of postprandial hepatic phosphorus metabolites in lean, obese, and type 2 diabetes patients. Am J Clin Nutr. 2015;102(5):1051-1058. https://doi.org/10.3945/ajcn.115.107599
Bawden SJ, Stephenson MC, Ciampi E, et al. Investigating the effects of an oral fructose challenge on hepatic ATP reserves in healthy volunteers: a 31P MRS study. Clin Nutr. 2015;35(3):645-649. https://doi.org/10.1016/j.clnu.2015.04.001
Hernández EÁ, Kahl S, Seelig A, et al. Acute dietary fat intake initiates alterations in energy metabolism and insulin resistance. J Clin Invest. 2017;127(2):695-708. https://doi.org/10.1172/JCI89444
Schmid AI, Szendroedi J, Chmelik M, Krššák M, Moser E, Roden M. Liver ATP synthesis is lower and relates to insulin sensitivity in patients with type 2 diabetes. Diabetes Care. 2011;34(2):448-453. https://doi.org/10.2337/dc10-1076
Gancheva S, Bierwagen A, Kaul K, et al. Variants in genes controlling oxidative metabolism contribute to lower hepatic ATP independent of liver fat content in type 1 diabetes. Diabetes. 2016;65(7):1849-1857.
Cui MH, Jayalakshmi K, Liu L, Guha C, Branch CA. In vivo 1H MRS and 31P MRSI of the response to cyclocreatine in transgenic mouse liver expressing creatine kinase. NMR Biomed. 2015;28(12):1634-1644. https://doi.org/10.1002/nbm.3391
Brauer M, Ling M. In vivo 31P NMR studies of alterations in liver metabolism in chronic ethanol-treated rats. Magn Reson Med. 1991;20(1):100-112.
Corbin IR, Buist R, Peeling J, Zhang M, Uhanova J, Minuk GY. Hepatic 31P MRS in rat models of chronic liver disease: assessing the extent and progression of disease. Gut. 2003;52(7):1046-1053. https://doi.org/10.1136/gut.52.7.1046
Zakian KL, D'Angelica M, Matei C, et al. A quantitative assessment of liver metabolites during jaundice using three dimensional phosphorus chemical shift imaging. Magn Reson Imaging. 2000;18(2):181-187. https://doi.org/10.1016/S0730-725X(99)00119-8
Jelenik T, Kaul K, Séquaris G, et al. Mechanisms of insulin resistance in primary and secondary nonalcoholic fatty liver. Diabetes. 2017;66(8):2241-2253. https://doi.org/10.2337/db16-1147
Pouymayou B, Buehler T, Kreis R, Boesch C. Test-retest analysis of multiple 31P magnetization exchange pathways using asymmetric adiabatic inversion. Magn Reson Med. 2017;78(1):33-39. https://doi.org/10.1002/mrm.26337
Shimomura I, Hammer RE, Richardson JA, et al. Insulin resistance and diabetes mellitus in transgenic mice expressing nuclear SREBP-1c in adipose tissue: model for congenital generalized lipodystrophy. Genes Dev. 1998;12(20):3182-3194. https://doi.org/10.1101/gad.12.20.3182
Gülden E, Ihira M, Ohashi A, et al. Toll-like receptor 4 deficiency accelerates the development of insulin-deficient diabetes in non-obese diabetic mice. PLoS ONE. 2013;8(9):e75385. https://doi.org/10.1371/journal.pone.0075385
Jelenik T, Séquaris G, Kaul K, et al. Tissue-specific differences in the development of insulin resistance in a mouse model for type 1 diabetes. Diabetes. 2014;63(11):3856-3867.
Haase A, Frahm J, Matthaei D, Hanicke W, Merboldt K. FLASH imaging. Rapid NMR imaging using low flip-angle pulses. J Magn Reson. 1986;67(2):258-266.
Pauly J, Nishimura D, Macovski A, Le Roux P. Parameter relations for the Shinnar-Le Roux selective excitation pulse design algorithm. IEEE Trans Med Imaging. 1991;10(1):53-65. https://doi.org/10.1109/42.75611
Shinnar M, Leigh JS. The application of spinors to pulse synthesis and analysis. Magn Reson Med. 1989;12(1):93-98.
Shinnar M, Bolinger L, Leigh JS. The synthesis of soft pulses with a specified frequency-response. Magn Reson Med. 1989;12(1):88-92.
Shinnar M, Bolinger L, Leigh JS. The use of finite impulse-response filters in pulse design. Magn Reson Imaging. 1989;12:81-87.
Shinnar M, Eleff S, Subramanian H, Leigh JS. The synthesis of pulse sequences yielding arbitrary magnetization vectors. Magn Reson Med. 1989;12(1):74-80.
Hennig J, Ott D, Adam T, Friedburg H. Measurement of CSF flow using an interferrographic MR technique based on the RARE-fast imaging sequence. Magn Reson Imaging. 1990;8(5):543-556.
Burger C, Buchli R, Mckinnon G, Meier D, Boesiger P. The impact of the ISIS experiment order on spatial contamination. Magn Reson Med. 1992;26(2):218-230. https://doi.org/10.1002/mrm.1910260204
Bottomley P. Selective volume method for performing localized NMR spectroscopy. US patent 4480228A. Oct. 30,1984.
Frahm J, Bruhn H, Gyngell ML, Merboldt KD, Hanicke W, Sauter R. Localized high-resolution proton NMR spectroscopy using stimulated echoes: initial applications to human brain in vivo. Magn Reson Med. 1989;9(1):79-93.
Longo R, Pollesello P, Ricci C, et al. Proton MR spectroscopy in quantitative in vivo determination of fat content in human liver steatosis. J Magn Reson Imaging. 1995;5(3):281-285. https://doi.org/10.1002/jmri.1880050311
Hamilton G, Yokoo T, Bydder M, et al. In vivo characterization of the liver fat 1H MR spectrum. NMR Biomed. 2011;24(7):784-790. https://doi.org/10.1002/nbm.1622
Stefan D, Di Cesare F, Andrasescu A, et al. Quantitation of magnetic resonance spectroscopy signals: the jMRUI software package. Meas Sci Technol. 2009;20(10):104035. https://doi.org/10.1088/0957-0233/20/10/104035
Naressi A, Couturier C, Castang I, De Beer R, Graveron-Demilly D. Java-based graphical user interface for MRUI, a software package for quantitation of in vivo/medical magnetic resonance spectroscopy signals. Comput Biol Med. 2001;31(4):269-286. https://doi.org/10.1016/S0010-4825(01)00006-3
Naressi A, Couturier C, Devos JM, et al. Java-based graphical user interface for the MRUI quantitation package. Magn Reson Mater Phys Biol Med. 2001;12:141-152. https://doi.org/10.1007/BF02668096
van den Boogaart A, Van Hecke P, Van Huffel S, Graveron-Demilly D, van Ormondt D, de Beer R. MRUI: a graphical user interface for accurate routine MRS data analysis. Proceedings of the European Society of Magnetic Resonance in Medicine and Biology 13th Annual Meeting. Prague, Czech Republic; 1997:318.
van den Boogaart A. MRUI MANUAL V. 96.3. In: A User's Guide to the Magnetic Resonance User Interface Software Package. Delft: Delft Technical University Press; 1997.
Vanhamme L, van den Boogaart A, Van Huffel S. Improved Method for Accurate and Efficient Quantification of MRS Data with Use of Prior Knowledge. J Magn. Reson. 1997;43(129):35-43. https://doi.org/10.1006/jmre.1997.1244
Ordidge RJ, Bowley RM, McHale G. A general approach to selection of multiple cubic volume elements using the ISIS technique. Magn Reson Med. 1988;8(3):323-331.
Schmid AI, Chmelik M, Szendroedi J, et al. Quantitative ATP synthesis in human liver measured by localized 31P spectroscopy using the magnetization transfer experiment. NMR Biomed. 2008;21(5):437-443. https://doi.org/10.1002/nbm
Evelhoch JL, Ewy CS, Siegfried BA, Ackerman JJH, Rice DW, Briggs RW. 31P Spin-lattice relaxation times and resonance linewidths of rat tissue in vivo: dependence upon the static magnetic field strength. Magn Reson Med. 1985;2(4):410-417. https://doi.org/10.1002/mrm.1910020409
Chmelik M, Považan M, Krššák M, et al. In vivo 31P magnetic resonance spectroscopy of the human liver at 7 T: an initial experience. NMR Biomed. 2014;27(4):478-485. https://doi.org/10.1002/nbm.3084
Purvis LAB, Clarke WT, Valkovič L, et al. Phosphodiester content measured in human liver by in vivo 31P MR spectroscopy at 7 tesla. Magn Reson Med. 2017;78(6):2095-2105. https://doi.org/10.1002/mrm.26635
Malloy CR, Cunningham CC, Radda GK. The metabolic state of the rat liver in vivo measured by 31P-NMR spectroscopy. Biochim Biophys Acta. 1986;885(1):1-11.
Jensen JE, Drost DJ, Menon RS, Williamson PC. In vivo brain 31P-MRS: Measuring mhe phospholipid resonances at 4 Tesla from small voxels. NMR Biomed. 2002;15(5):338-347. https://doi.org/10.1002/nbm.776
Ramamonjisoa N, Ratiney H, Mutel E, et al. In vivo hepatic lipid quantification using MRS at 7 Tesla in a mouse model of glycogen storage disease type 1a. J Lipid Res. 2013;54(7):2010-2022. https://doi.org/10.1194/jlr.D033399
Ye Q, Danzer CF, Fuchs A, Wolfrum C, Rudin M. Hepatic lipid composition differs between ob/ob and ob/+ control mice as determined by using in vivo localized proton magnetic resonance spectroscopy. Magn Reson Mater Phys Biol Med. 2012;25(5):381-389. https://doi.org/10.1007/s10334-012-0310-2
Tang H, Miller C, Kennan R, Wu EX, Williams DS, Liu H. In vivo lipid quantitation in mouse liver using the gradient reversal water-fat imaging method. Proc Int Soc Magn Reson Med. 2007;15(727).
Soares AF, Lei H, Gruetter R. Characterization of hepatic fatty acids in mice with reduced liver fat by ultra-short echo time 1H-MRS at 14.1 T in vivo. NMR Biomed. 2015;28(8):1009-1020. https://doi.org/10.1002/nbm.3345
Strobel K, Van Den Hoff J, Pietzsch J. Localized proton magnetic resonance spectroscopy of lipids in adipose tissue at high spatial resolution in mice in vivo. J Lipid Res. 2008;49(2):473-480. https://doi.org/10.1194/jlr.D700024-JLR200
Lu M, Zhu XH, Zhang Y, Chen W. Intracellular redox state revealed by in vivo 31P MRS measurement of NAD+ and NADH contents in brains. Magn Reson Med. 2014;71(6):1959-1972. https://doi.org/10.1002/mrm.24859
Brosnan MJ, Chen L, Wheeler CE, Van Dyke TA, Koretsky AP. Phosphocreatine protects ATP from a fructose load in transgenic mouse liver expressing creatine kinase. Am J Physiol. 1991;260(6):1191-1200.
Lawry TJ, Karczmar GS, Weiner MW, Matson GB. Computer simulation of MRS localization techniques: an analysis of ISIS. Magn Reson Med. 1989;9(3):299-314. https://doi.org/10.1002/mrm.1910090302
Bakermans AJ, Abdurrachim D, van Nierop BJ, et al. In vivo mouse myocardial 31P MRS using three-dimensional image-selected in vivo spectroscopy (3D ISIS): technical considerations and biochemical validations. NMR Biomed. 2015;28(10):1218-1227. https://doi.org/10.1002/nbm.3371
Ljungberg M, Starck G, Vikhoff-Baaz B, Alpsten M, Ekholm S, Forssell-Aronsson E. Extended ISIS sequences insensitive to T1 smearing. Magn Reson Med. 2000;44(4):546-555. https://doi.org/10.1002/1522-2594(200010)44:4<546::AID-MRM8>3.0.CO;2-7
Bogner W, Chmelik M, Andronesi OC, Sorensen AG, Trattnig S, Gruber S. In vivo 31P spectroscopy by fully adiabatic extended image selected in vivo spectroscopy: a comparison between 3 T and 7 T. Magn Reson Med. 2011;66(4):923-930. https://doi.org/10.1002/mrm.22897
Buchli R, Meier D, Martin E, Boesiger P. Assessment of absolute metabolite concentrations in human tissue by 31P MRS in vivo. Part II: Muscle, liver, kidney. Magn Reson Med. 1994;32(4):453-458. https://doi.org/10.1002/mrm.1910320405
Sohlenius-Sternbeck A-K. Determination of the hepatocellularity number for human, dog, rabbit, rat and mouse livers from protein concentration measurements. Toxicol In Vitro. 2006;20(8):1582-1586. https://doi.org/10.1016/j.tiv.2006.06.003

Auteurs

Maik Rothe (M)

Institute for Clinical Diabetology, German Diabetes Center at Heinrich Heine University, Leibniz Institute for Diabetes Research, Düsseldorf, Germany.
German Center for Diabetes Research, München-Neuherberg, Germany.

Corinna Wessel (C)

Institute for Clinical Diabetology, German Diabetes Center at Heinrich Heine University, Leibniz Institute for Diabetes Research, Düsseldorf, Germany.
German Center for Diabetes Research, München-Neuherberg, Germany.

Sandra Cames (S)

Institute for Clinical Diabetology, German Diabetes Center at Heinrich Heine University, Leibniz Institute for Diabetes Research, Düsseldorf, Germany.
German Center for Diabetes Research, München-Neuherberg, Germany.

Julia Szendroedi (J)

Institute for Clinical Diabetology, German Diabetes Center at Heinrich Heine University, Leibniz Institute for Diabetes Research, Düsseldorf, Germany.
German Center for Diabetes Research, München-Neuherberg, Germany.
Division of Endocrinology and Diabetology, Medical Faculty, Heinrich Heine University, Düsseldorf, Germany.

Volker Burkart (V)

Institute for Clinical Diabetology, German Diabetes Center at Heinrich Heine University, Leibniz Institute for Diabetes Research, Düsseldorf, Germany.
German Center for Diabetes Research, München-Neuherberg, Germany.

Jong-Hee Hwang (JH)

Institute for Clinical Diabetology, German Diabetes Center at Heinrich Heine University, Leibniz Institute for Diabetes Research, Düsseldorf, Germany.
German Center for Diabetes Research, München-Neuherberg, Germany.

Michael Roden (M)

Institute for Clinical Diabetology, German Diabetes Center at Heinrich Heine University, Leibniz Institute for Diabetes Research, Düsseldorf, Germany.
German Center for Diabetes Research, München-Neuherberg, Germany.
Division of Endocrinology and Diabetology, Medical Faculty, Heinrich Heine University, Düsseldorf, Germany.

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