Noninvasive identification and assessment of functional brown adipose tissue in rodents using hyperpolarized 13C imaging

International Journal of Obesity

Volumn 38, Issue 1, 2014, Pages 126-131

  Lau, A Z ^a,b   Chen, A P ^c   Gu, Y ^a   Ladouceur Wodzak, M ^a   Nayak, K S ^d   Cunningham, C H ^a,b  

^a SUNNYBROOK RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c GE HEALTHCARE   (Canada)

^d University of Southern California   (United States)

Author keywords

brown adipose tissue; hyperpolarized 13C imaging; magnetic resonance; metabolism; pyruvate

Indexed keywords

BICARBONATE C 13; EOSIN; HEMATOXYLIN; LACTIC ACID C 13; NORADRENALIN; PYRUVIC ACID C 13; RADIOPHARMACEUTICAL AGENT; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; FEASIBILITY STUDY; HISTOLOGY; HYPERPOLARIZATION; MALE; NON INVASIVE PROCEDURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; RAT; RODENT MODEL; TISSUE DISTRIBUTION; TISSUE METABOLISM;

RATTUS; RODENTIA;

ADIPOSE TISSUE, BROWN; ANIMALS; CARBON ISOTOPES; ENERGY METABOLISM; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NOREPINEPHRINE; PYRUVIC ACID; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCIBILITY OF RESULTS;

EID: 84891825869     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2013.58     Document Type: Article

References (41)

1. Celi FS. Brown adipose tissue-when it pays to be inefficient. N Engl J Med 2009; 360: 1553-1556.
2. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T et al. Functional brown adipose tissue in healthy adults. N Engl J Med 2009; 360: 1518-1525.
3. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JMAFL, Kemerink GJ, Bouvy ND et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med 2009; 360: 1500-1508.
4. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med 2009; 360: 1509-1517.
5. Hu HH, Smith Jr DL, Nayak KS, Goran MI, Nagy TR. Identification of brown adipose tissue in mice with fat-water IDEAL-MRI. J Magn Reson Imaging 2010; 31: 1195-1202.
6. Hu HH, Tovar JP, Pavlova Z, Smith ML, Gilsanz V. Unequivocal identification of brown adipose tissue in a human infant. J Magn Reson Imaging 2012; 35: 938-942.
7. Baron DM, Clerte M, Brouckaert P, Raher MJ, Flynn AW, Zhang H et al. In vivo noninvasive characterization of brown adipose tissue blood flow by contrast ultrasound in mice. Circ Cardiovasc Imaging 2012; 5: 652-659.
8. Khanna A, Branca RT. Detecting brown adipose tissue activity with BOLD MRI in mice. J Magn Reson Imaging 2012; 68: 1285-1290.
9. Lubura M, Hesse D, Neumann N, Scherneck S, Wiedmer P, Schurmann A. Noninvasive quantification of white and brown adipose tissues and liver fat content by computed tomography in mice. PLOS One 2012; 7: e37026.
10. Symonds ME, Henderson K, Elvidge L, Bosman C, Sharkey D, Perkins AC et al. Thermal imaging to assess age-related changes of skin temperature within the supraclavicular region co-locating with brown adipose tissue in healthy children. J Pediatr 2012; 161: 892-898.
11. Ardenkjaer-Larsen JH, Fridlund B, Gram A, Hansson G, Hansson L, Lerche MH et al. Increase in signal-to-noise ratio of410,000 times in liquid-state NMR. Proc Natl Acad Sci USA 2003; 100: 10158-10163.
12. Golman K, RIt Zandt, Lerche M, Pehrson R, Ardenkjaer-Larsen JH. Metabolic imaging by hyperpolarized 13C magnetic resonance imaging for in vivo tumor diagnosis. Cancer Res 2006; 66: 10855-10860.
13. Day SE, Kettunen MI, Gallagher FA, Hu D-E, Lerche M, Wolber J et al. Detecting tumor response to treatment using hyperpolarized 13C magnetic resonance imaging and spectroscopy. Nat Med 2007; 13: 1382-1387.
14. Schroeder MA, Cochlin LE, Heather LC, Clarke K, Radda GK, Tyler DJ. In vivo assessment of pyruvate dehydrogenase flux in the heart using hyperpolarized carbon-13 magnetic resonance. Proc Natl Acad Sci USA 2008; 105: 12051-12056.
15. Schroeder MA, Atherton HJ, Ball DR, Cole MA, Heather LC, Griffin JL et al. Real-time assessment of Krebs cycle metabolism using hyperpolarized 13C magnetic resonance spectroscopy. FASEB J 2009; 23: 2529-2538.
16. Golman K, Petersson JS, Magnusson P, Johansson E, Akeson P, Chai C-M et al. Cardiac metabolism measured noninvasively by hyperpolarized 13C MRI. Magn Reson Med 2008; 59: 1005-1013.
17. Merritt ME, Harrison C, Storey C, Jeffrey FM, Sherry AD, Malloy CR. Hyperpolarized 13C allows a direct measure of flux through a single enzyme-catalyzed step by NMR. Proc Natl Acad Sci USA 2007; 104: 19773-19777.
18. Merritt ME, Harrison C, Storey C, Sherry AD, Malloy CR. Inhibition of carbohydrate oxidation during the first minute of reperfusion after brief ischemia: NMR detection of hyperpolarized 13CO2 and H13CO3. Magn Reson Med 2008; 60: 1029-1036.
19. Lau AZ, Chen AP, Ghugre NR, Ramanan V, Lam WW, Connelly KA et al. Rapid multislice imaging of hyperpolarized (13)C pyruvate and bicarbonate in the heart. Magn Reson Med 2010; 64: 1323-1331.
20. Lau AZ, Chen AP, Barry J, Graham JJ, Dominguez-Viqueira W, Ghugre NR et al. Reproducibility study for free-breathing measurements of pyruvate metabolism using hyperpolarized (13) C in the heart. Magn Reson Med 2013; 69: 1063-1071.
21. Merritt ME, Harrison C, Sherry AD, Malloy CR, Burgess SC. Flux through hepatic pyruvate carboxylase and phosphoenolpyruvate carboxykinase detected by hyperpolarized 13C magnetic resonance. Proc Natl Acad Sci USA 2011; 108: 19084-19089.
22. Lee P, Leong W, Tan T, Lim M, Han W, Radda GK. In vivo hyperpolarized carbon-13 magnetic resonance spectroscopy reveals increased pyruvate carboxylase flux in an insulin resistant mouse model. Hepatology 2012; 57: 515-524.
23. Nelson SJ, Kurhanewicz J, Vigneron DB, Larson PEZ, Harzstark A, Ferrone M et al. Proof of Concept Clinical Trial of Hyperpolarized C-13 Pyruvate in Patients with Prostate Cancer. International Society for Magnetic Resonance in Medicine (ISMRM): Melbourne, Australia, 2012 (abstract 274).
24. Ardenkjaer-Larsen JH, Leach AM, Clarke N, Urbahn J, Anderson D, Skloss TW. Dynamic nuclear polarization polarizer for sterile use intent. NMR Biomed 2011; 24: 927-932.
25. Lau AZ, Chen AP, Cunningham CH. Integrated Bloch-Siegert B(1) mapping and multislice imaging of hyperpolarized (13) C pyruvate and bicarbonate in the heart. Magn Reson Med 2011; 67: 62-71.
26. Lau AZ, Chen AP, Hurd RE, Cunningham CH. Spectral-spatial excitation for rapid imaging of DNP compounds. NMR Biomed 2011; 24: 988-996.
27. Ma SW, Foster DO. Uptake of glucose and release of fatty acids and glycerol by rat brown adipose tissue in vivo. Can J Physiol Pharmacol 1986; 64: 609-614.
28. Menichetti L, Frijia F, Flori A, Wiesinger F, Lionetti V, Giovannetti G et al. Assessment of real-time myocardial uptake and enzymatic conversion of hyperpolarized [1-(13) C]pyruvate in pigs using slice selective magnetic resonance spectroscopy. Contrast Media Mol Imaging 2012; 7: 85-94.
29. Lopez-Soriano FJ, Alemany M. In vitro alanine utilization by rat interscapular brown adipose tissue. Biochim Biophys Acta 1990; 1036: 6-10.
30. Cannon B, Nedergaard J. The physiological role of pyruvate carboxylation in hamster brown adipose tissue. Eur J Biochem 1979; 94: 419-426.
31. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004; 84: 277-359.
32. Whittle AJ, Lopez M, Vidal-Puig A. Using brown adipose tissue to treat obesity-the central issue. Trends Mol Med 2011; 17: 405-411.
33. Carter EA, Bonab AA, Hamrahi V, Pitman J, Winter D, Macintosh LJ et al. Effects of burn injury, cold stress and cutaneous wound injury on the morphology and energy metabolism of murine brown adipose tissue (BAT) in vivo. Life Sci 2011; 89: 78-85.
34. Ouellet V, Labbé SM, Blondin DP, Phoenix S, Gué rin B, Haman F et al. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest 2012; 122: 545-552.
35. Rothwell NJ, Stock MJ. A role for brown adipose tissue in diet-induced thermogenesis. Nature 1979; 281: 31-35.
36. Rothwell NJ, Stock MJ. Effect of chronic food restriction on energy balance, thermogenic capacity, and brown-adipose-tissue activity in the rat. Bioscience Rep 1982; 2: 543-549.
37. Williams G, Kolodny GM. Method for decreasing uptake of 18F-FDG by hypermetabolic brown adipose tissue on PET. AJR Am J Roentgenol 2008; 190: 1406-1409.
38. Zierhut ML, Yen Y-F, Chen AP, Bok R, Albers MJ, Zhang V et al. Kinetic modeling of hyperpolarized (13)C(1)-pyruvate metabolism in normal rats and TRAMP mice. J Magn Reson 2009; 202: 85-92.
39. Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K et al. Brown adipose tissue activity controls triglyceride clearance. Nat Med 2011; 17: 200-205.
40. Ball DR, Dodd MS, Atherton HJ, Schroeder MA, Carr C, Radda GK et al. Hyperpolarized butyrate: a novel substrate for the assessment of cardiac fatty acid metabolism. 19th Proceedings of the ISMRM. International Society for Magnetic Resonance in Medicine (ISMRM): Montreal, Canada, 2011 (abstract 658).
41. Colombo Serra S, Karlsson M, Giovenzana GB, Cavallotti C, Tedoldi F, Aime S. Hyperpolarized (13) C-labelled anhydrides as DNP precursors of metabolic MRI agents. Contrast Media Mol Imaging 2012; 7: 469-477.