Detection of myocardial medium-chain fatty acid oxidation and tricarboxylic acid cycle activity with hyperpolarized [1-
13C-MRS
beta-oxidation
cardiac
dissolution dynamic nuclear polarization
hyperpolarization
medium-chain triglyceride
serum albumin
Journal
NMR in biomedicine
ISSN: 1099-1492
Titre abrégé: NMR Biomed
Pays: England
ID NLM: 8915233
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
08
10
2019
revised:
22
11
2019
accepted:
27
11
2019
pubmed:
7
1
2020
medline:
8
1
2021
entrez:
7
1
2020
Statut:
ppublish
Résumé
Under normal conditions, the heart mainly relies on fatty acid oxidation to meet its energy needs. Changes in myocardial fuel preference are noted in the diseased and failing heart. The magnetic resonance signal enhancement provided by spin hyperpolarization allows the metabolism of substrates labeled with carbon-13 to be followed in real time in vivo. Although the low water solubility of long-chain fatty acids abrogates their hyperpolarization by dissolution dynamic nuclear polarization, medium-chain fatty acids have sufficient solubility to be efficiently polarized and dissolved. In this study, we investigated the applicability of hyperpolarized [1-
Substances chimiques
Blood Glucose
0
Caprylates
0
Carbon Isotopes
0
Lactic Acid
33X04XA5AT
Carbon-13
FDJ0A8596D
octanoic acid
OBL58JN025
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e4243Informations de copyright
© 2020 John Wiley & Sons, Ltd.
Références
Stanley WC, Recchia FA, Lopaschuk GD. Myocardial substrate metabolism in the normal and failing heart. Physiol Rev. 2005;85:1093-1129.
Ventura-Clapier R, Garnier A, Veksler V. Energy metabolism in heart failure. J Physiol. 2004;555:1-13.
King LM, Opie LH. Glucose and glycogen utilisation in myocardial ischemia-changes in metabolism and consequences for the myocyte. Mol Cell Biochem. 1998;180:3-26.
Lopaschuk GD, Ussher JR, Folmes CDL, Jaswal JS, Stanley WC. Myocardial fatty acid metabolism in health and disease. Physiol Rev. 2010;90:207-258.
Parang P, Singh B, Arora R. Metabolic modulators for chronic cardiac ischemia. J Cardiovasc Pharmacol Ther. 2005;10:217-223.
Marten B, Pfeuffer M, Schrezenmeir J. Medium-chain triglycerides. Int Dairy J. 2006;16:1374-1382.
Eaton S, Bartlett K, Pourfarzam M. Mammalian mitochondrial beta-oxidation. Biochem J. 1996;320:345-357.
Nagao K, Yanagita T. Medium-chain fatty acids: functional lipids for the prevention and treatment of the metabolic syndrome. Pharmacol Res. 2010;61:208-212.
Gavva SR, Wiethoff AJ, Zhao P, Malloy CR, Sherry AD. A 13C isotopomer NMR method for monitoring incomplete beta-oxidation of fatty acids in intact tissue. Biochem J. 1994;303:847-853.
Walton ME, Ebert D, Haller RG. Octanoate oxidation measured by 13C-NMR spectroscopy in rat skeletal muscle, heart, and liver. J Appl Physiol. 2003;95:1908-1916.
McGarry JD, Foster DW. The regulation of ketogenesis from octanoic acid. The role of the tricarboxylic acid cycle and fatty acid synthesis. J Biol Chem. 1971;246:1149-1159.
Golman K, Zandt RIT, Thaning M. Real-time metabolic imaging. P Natl Acad Sci USA. 2006;103:11270-11275.
Comment A, Merritt ME. Hyperpolarized magnetic resonance as a sensitive detector of metabolic function. Biochemistry. 2014;53:7333-7357.
Jensen PR, Peitersen T, Karlsson M, et al. Tissue-specific short chain fatty acid metabolism and slow metabolic recovery after ischemia from hyperpolarized NMR in vivo. J Biol Chem. 2009;284:36077-36082.
Koellisch U, Gringeri CV, Rancan G, et al. Metabolic imaging of hyperpolarized [1-13 C]acetate and [1-13 C]acetylcarnitine - investigation of the influence of dobutamine induced stress. Magn Reson Med. 2014;74:1011-1018.
Bastiaansen JAM, Cheng T, Lei H, Gruetter R, Comment A. Direct noninvasive estimation of myocardial tricarboxylic acid cycle flux in vivo using hyperpolarized C-13 magnetic resonance. J Mol Cell Cardiol. 2015;87:129-137.
Flori A, Liserani M, Frijia F, et al. Real-time cardiac metabolism assessed with hyperpolarized [1-13C]acetate in a large-animal model. Contrast Media Mol Imaging. 2015;10:194-202.
Koellisch U, Laustsen C, Nørlinger TS, et al. Investigation of metabolic changes in STZ-induced diabetic rats with hyperpolarized [1-13C]acetate. Physiol Rep. 2015;3:e12474.
Ball DR, Rowlands B, Dodd MS, et al. Hyperpolarized butyrate: a metabolic probe of short chain fatty acid metabolism in the heart. Magn Reson Med. 2014;71:1663-1669.
Bastiaansen JAM, Merritt ME, Comment A. Measuring changes in substrate utilization in the myocardium in response to fasting using hyperpolarized [1-13C]butyrate and [1-13C]pyruvate. Sci Rep. 2016;6:25573.
Bastiaansen JAM, Yoshihara HAI, Capozzi A, et al. Probing cardiac metabolism by hyperpolarized 13C MR using an exclusively endogenous substrate mixture and photo-induced nonpersistent radicals. Magn Reson Med. 2018;79:2451-2459.
Flori A, Giovannetti G, Santarelli MF, et al. Biomolecular imaging of 13C-butyrate with dissolution-DNP: polarization enhancement and formulation for in vivo studies. Spectrochim Acta A. 2018;199:153-160.
Abdurrachim D, Teo XQ, Woo CC, et al. Cardiac metabolic modulation upon low-carbohydrate low-protein ketogenic diet in diabetic rats studied in vivo using hyperpolarized 13 C pyruvate, butyrate, and acetoacetate probes [published online ahead of print December 11, 2018]. Diabetes Obes Metab. doi, https://doi.org/10.1111/dom.13608
Kenyon MA, Hamilton JA. 13C NMR studies of the binding of medium-chain fatty acids to human serum albumin. J Lipid Res. 1994;35:458-467.
Lerche MH, Meier S, Jensen PR, et al. Study of molecular interactions with 13C DNP-NMR. J Magn Reson. 2010;203:52-56.
Cheng T, Capozzi A, Takado Y, Balzan R, Comment A. Over 35% liquid-state 13C polarization obtained via dissolution dynamic nuclear polarization at 7 T and 1 K using ubiquitous nitroxyl radicals. Phys Chem Chem Phys. 2013;15:20819-20822.
Cheng T, Mishkovsky M, Bastiaansen JAM, et al. Automated transfer and injection of hyperpolarized molecules with polarization measurement prior to in vivo NMR. NMR Biomed. 2013;26:1582-1588.
Comment A, van den Brandt B, Uffmann K, et al. Design and performance of a DNP prepolarizer coupled to a rodent MRI scanner. Concept Magn Reson B. 2007;31:255-269.
Yoshihara HAI, Can E, Karlsson M, Lerche MH, Schwitter J, Comment A. High-field dissolution dynamic nuclear polarization of [1-13C]pyruvic acid. Phys Chem Chem Phys. 2016;18:12409-12413.
Gruetter R, Tkác I. Field mapping without reference scan using asymmetric echo-planar techniques. Magn Reson Med. 2000;43:319-323.
Marutyan KR, Bretthorst GL. The Bayesian analysis software developed at Washington University. AIP Conf Proc. 2009;1193:368-381.
Wishart DS, Feunang YD, Marcu A, et al. HMDB 4.0: the human metabolome database for 2018. Nucleic Acids Res. 2018;46:D608-D617.
Schroeder MA, Atherton HJ, Ball DR, et al. Real-time assessment of Krebs cycle metabolism using hyperpolarized 13C magnetic resonance spectroscopy. FASEB J. 2009;23:2529-2538.
Josan S, Hurd R, Park JM, et al. Dynamic metabolic imaging of hyperpolarized [2-13C]pyruvate using spiral chemical shift imaging with alternating spectral band excitation. Magn Reson Med. 2014;71:2051-2058.
Miller JJ, Ball DR, Lau AZ, Tyler DJ. Hyperpolarized ketone body metabolism in the rat heart. NMR Biomed. 2018;60:e3912.
Abdurrachim D, Woo CC, Teo XQ, Chan WX, Radda GK, Lee PTH. A new hyperpolarized 13C ketone body probe reveals an increase in acetoacetate utilization in the diabetic rat heart. Sci Rep. 2019;9:5532.
Abdurrachim D, Teo XQ, Woo CC, et al. Empagliflozin reduces myocardial ketone utilization while preserving glucose utilization in diabetic hypertensive heart disease: a hyperpolarized 13C magnetic resonance spectroscopy study. Diabetes Obes Metab. 2018;59:8.
Chen W, Sharma G, Jiang W, et al. Metabolism of hyperpolarized 13 C-acetoacetate to β-hydroxybutyrate detects real-time mitochondrial redox state and dysfunction in heart tissue. NMR Biomed. 2019;32:e4091.
Rinaldo P, Matern D, Bennett MJ. Fatty acid oxidation disorders. Annu Rev Physiol. 2002;64:477-502.
Kobayashi A, Jiang LL, Hashimoto T. Two mitochondrial 3-hydroxyacyl-CoA dehydrogenases in bovine liver. J Biochem. 1996;119:775-782.
Miyazawa S, Osumi T, Hashimoto T. The presence of a new 3-oxoacyl-CoA thiolase in rat liver peroxisomes. Eur J Biochem. 1980;103:589-596.
Schroeder MA, Atherton HJ, Dodd MS, et al. The cycling of acetyl-coenzyme a through acetylcarnitine buffers cardiac substrate supply: a hyperpolarized 13C magnetic resonance study. Circ Cardiovasc Imaging. 2012;5:201-209.
Labarthe F, Gélinas R, Rosiers DC. Medium-chain fatty acids as metabolic therapy in cardiac disease. Cardiovasc Drugs Ther. 2008;22:97-106.
Pearson DJ, Tubbs PK. Carnitine and derivatives in rat tissues. Biochem J. 1967;105:953-963.
Ekwall P. Solutions of alkali soaps and water in fatty acids XI. Correlation between the acid sodium octanoate in the most water-rich part of the L2-phase and the acid soaps in two adjacent phases. Colloid Polym Sci. 1988;266:729-733.
Hargreaves WR, Deamer DW. Liposomes from ionic, single-chain amphiphiles. Biochemistry. 1978;17:3759-3768.
Karlsson M, Jensen PR, Duus JØ, Meier S, Lerche MH. Development of dissolution DNP-MR substrates for metabolic research. Appl Magn Reson. 2012;43:223-236.
Wycoff CC, Cann JE. Experimental pulmonary air embolism in dogs. Calif Med. 1966;105:361-367.
Drakenberg T, Lindman B. 13C NMR of micellar solutions. J Colloid Interface Sci. 1973;44:184-186.
Allerhand A, Doddrell D. Segmental motion in liquid 1-decanol. Application of natural-abundance carbon-13 partially relaxed Fourier transform nuclear magnetic resonance. J Am Chem Soc. 1971;93:1558-1559.
Hamilton JA, Cistola DP, Morrisett JD, Sparrow JT, Small DM. Interactions of myristic acid with bovine serum albumin: a 13C NMR study. P Natl Acad Sci USA. 1984;81:3718-3722.