In vivo noninvasive characterization of brown adipose tissue blood flow by contrast ultrasound in mice

Circulation: Cardiovascular Imaging

Volumn 5, Issue 5, 2012, Pages 652-659

  Baron, David M ^a   Clerte, Maeva ^b   Brouckaert, Peter ^a,c   Raher, Michael J ^a   Flynn, Aidan W ^b   Zhang, Haihua ^b   Carter, Edward A ^b   Picard, Michael H ^b   Bloch, Kenneth D ^a   Buys, Emmanuel S ^a   Scherrer Crosbie, Marielle ^b  

^a Anesthesia Center for Critical Care Research   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

Brown adipose tissue; Contrast ultrasound; Imaging; Nitric oxide synthase; Uncoupling protein

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; MICROSPHERE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; NORADRENALIN; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3;

ADIPOSE TISSUE BLOOD FLOW; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CONTRAST ECHOGRAPHY; CONTRAST ENHANCEMENT; ECHOGRAPHY; FEASIBILITY STUDY; GENOTYPE; HEART OUTPUT; IN VIVO STUDY; KIDNEY BLOOD FLOW; MALE; MICROBUBBLE; MOUSE; MUSCLE BLOOD FLOW; NONHUMAN; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE;

ADIPOSE TISSUE, BROWN; ANIMALS; BLOOD FLOW VELOCITY; CARDIAC OUTPUT; CONTRAST MEDIA; ENZYME INHIBITORS; FEASIBILITY STUDIES; FLUORESCENT DYES; FLUOROCARBONS; GENE EXPRESSION REGULATION; HEMODYNAMICS; INFUSIONS, INTRAVENOUS; ION CHANNELS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROBUBBLES; MITOCHONDRIAL PROTEINS; NITRIC OXIDE SYNTHASE TYPE III; NOREPINEPHRINE; REAL-TIME POLYMERASE CHAIN REACTION; REGIONAL BLOOD FLOW; RNA, MESSENGER; TIME FACTORS;

EID: 84867173476     PISSN: 19419651     EISSN: 19420080     Source Type: Journal    
DOI: 10.1161/CIRCIMAGING.112.975607     Document Type: Article

References (40)

1. Tseng YH, Cypess AM, Kahn CR. Cellular bioenergetics as a target for obesity therapy. Nat Rev Drug Discov. 2010;9:465-482.
2. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84:277-359. (Pubitemid 38054374)
3. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJ. 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, Kuo FC, Palmer EL, Tseng YH, Doria A, Kolodny GM, Kahn CR. Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009;360:1509-1517.
5. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerbäck S, Nuutila P. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360:1518-1525.
6. Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, Iwanaga T, Miyagawa M, Kameya T, Nakada K, Kawai Y, Tsujisaki M. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes. 2009;58:1526-1531.
7. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab. 2007;293:E444-E452. (Pubitemid 47205086)
8. Lever JD, Nnodim JO, Symons D. Arteriovenous anastomoses in interscapular brown adipose tissue in the rat. J Anat. 1985;143:207-210. (Pubitemid 16177346)
9. Foster DO, Frydman ML. Nonshivering thermogenesis in the rat. II. Measurements of blood flow with microspheres point to brown adipose tissue as the dominant site of the calorigenesis induced by noradrenaline. Can J Physiol Pharmacol. 1978;56:110-122.
10. Foster DO, Frydman ML. Tissue distribution of cold-induced thermogenesis in conscious warm- or cold-acclimated rats reevaluated from changes in tissue blood flow: the dominant role of brown adipose tissue in the replacement of shivering by nonshivering thermogenesis. Can J Physiol Pharmacol. 1979;57:257-270. (Pubitemid 9155091)
11. Nagashima T, Ohinata H, Kuroshima A. Involvement of nitric oxide in noradrenaline-induced increase in blood flow through brown adipose tissue. Life Sci. 1994;54:17-25.
12. Ma SW, Foster DO. Brown adipose tissue, liver, and diet-induced thermogenesis in cafeteria diet-fed rats. Can J Physiol Pharmacol. 1989;67:376-381. (Pubitemid 19141129)
13. Rothwell NJ, Stock MJ. Influence of noradrenaline on blood flow to brown adipose tissue in rats exhibiting diet-induced thermogenesis. Pflugers Arch. 1981;389:237-242. (Pubitemid 11150174)
14. Enerbäck S, Jacobsson A, Simpson EM, Guerra C, Yamashita H, Harper ME, Kozak LP. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature. 1997;387:90-94. (Pubitemid 27202655)
15. Matthias A, Jacobsson A, Cannon B, Nedergaard J. The bioenergetics of brown fat mitochondria from UCP1-ablated mice. Ucp1 is not involved in fatty acid-induced de-energization ("uncoupling"). J Biol Chem. 1999;274:28150-28160.
16. Al Zubair K, Bexis S, Docherty JR. Relaxations to beta-adrenoceptor subtype selective agonists in wild-type and NOS-3-KO mouse mesenteric arteries. Eur J Pharmacol. 2008;587:216-223.
17. Rebich S, Devine JO, Armstead WM. Role of nitric oxide and cAMP in beta-adrenoceptor-induced pial artery vasodilation. Am J Physiol. 1995;268(3 Pt 2):H1071-H1076.
18. Akimoto Y, Horinouchi T, Shibano M, Matsushita M, Yamashita Y, Okamoto T, Yamaki F, Tanaka Y, Koike K. Nitric oxide (NO) primarily accounts for endothelium-dependent component of beta-adrenoceptor-activated smooth muscle relaxation of mouse aorta in response to isoprenaline. J Smooth Muscle Res. 2002;38:87-99. (Pubitemid 36205760)
19. Brawley L, Shaw AM, MacDonald A. Role of endothelium/nitric oxide in atypical beta-adrenoceptor-mediated relaxation in rat isolated aorta. Eur J Pharmacol. 2000;398:285-296. (Pubitemid 30333356)
20. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, Sciorati C, Bracale R, Valerio A, Francolini M, Moncada S, Carruba MO. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science. 2003;299:896-899. (Pubitemid 36182449)
21. Kikuchi-Utsumi K, Gao B, Ohinata H, Hashimoto M, Yamamoto N, Kuroshima A. Enhanced gene expression of endothelial nitric oxide synthase in brown adipose tissue during cold exposure. Am J Physiol Regul Integr Comp Physiol. 2002;282:R623-R626. (Pubitemid 34664615)
22. Capettini LS, Cortes SF, Lemos VS. Relative contribution of eNOS and nNOS to endothelium-dependent vasodilation in the mouse aorta. Eur J Pharmacol. 2010;643:260-266.
23. Raher MJ, Thibault H, Poh KK, Liu R, Halpern EF, Derumeaux G, Ichinose F, Zapol WM, Bloch KD, Picard MH, Scherrer-Crosbie M. In vivo characterization of murine myocardial perfusion with myocardial contrast echocardiography: validation and application in nitric oxide synthase 3 deficient mice. Circulation. 2007;116:1250-1257. (Pubitemid 47517536)
24. Wei K, Jayaweera AR, Firoozan S, Linka A, Skyba DM, Kaul S. Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation. 1998;97:473-483. (Pubitemid 28090220)
25. Vogel R, Indermühle A, Reinhardt J, Meier P, Siegrist PT, Namdar M, Kaufmann PA, Seiler C. The quantification of absolute myocardial perfusion in humans by contrast echocardiography: algorithm and validation. J Am Coll Cardiol. 2005;45:754-762. (Pubitemid 40278975)
26. Sjøberg KA, Rattigan S, Hiscock N, Richter EA, Kiens B. A new method to study changes in microvascular blood volume in muscle and adipose tissue: real-time imaging in humans and rat. Am J Physiol Heart Circ Physiol. 2011;301:H450-H458.
27. Ohlson KB, Lindahl SG, Cannon B, Nedergaard J. Thermogenesis inhibition in brown adipocytes is a specific property of volatile anesthetics. Anesthesiology. 2003;98:437-448. (Pubitemid 36592813)
28. DosSantos RA, Alfadda A, Eto K, Kadowaki T, Silva JE. Evidence for a compensated thermogenic defect in transgenic mice lacking the mitochondrial glycerol-3-phosphate dehydrogenase gene. Endocrinology. 2003;144:5469-5479. (Pubitemid 37476076)
29. Rauch JC, Hayward JS. Topography and vascularization of brown fat in a small nonhibernator (deer mouse, Peromyscus maniculatus). Can J Zool. 1969;47:1301-1314.
30. Mattson DL, Meister CJ. Renal cortical and medullary blood flow responses to L-NAME and ANG II in wild-type, nNOS null mutant, and eNOS null mutant mice. Am J Physiol Regul Integr Comp Physiol. 2005;289:R991-R997. (Pubitemid 41397046)
31. Tournoux F, Petersen B, Thibault H, Zou L, Raher MJ, Kurtz B, Halpern EF, Chaput M, Chao W, Picard MH, Scherrer-Crosbie M. Validation of noninvasive measurements of cardiac output in mice using echocardiography. J Am Soc Echocardiogr. 2011;24:465-470.
32. Van Oosterhout MF, Willigers HM, Reneman RS, Prinzen FW. Fluorescent microspheres to measure organ perfusion: validation of a simplified sample processing technique. Am J Physiol. 1995;269(2 Pt 2):H725-H733.
33. Heim T, Hull D. The blood flow and oxygen consumption of brown adipose tissue in the new-born rabbit. J Physiol (Lond). 1966;186:42-55.
34. Carter EA, Bonab AA, Hamrahi V, Pitman J, Winter D, Macintosh LJ, Cyr EM, Paul K, Yerxa J, Jung W, Tompkins RG, Fischman AJ. 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.
35. Carter EA, Bonab AA, Paul K, Yerxa J, Tompkins RG, Fischman AJ. Association of heat production with 18F-FDG accumulation in murine brown adipose tissue after stress. J Nucl Med. 2011;52:1616-1620.
36. Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T, Scheinin M, Taittonen M, Niemi T, Enerbäck S, Virtanen KA. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 2011;14:272-279.
37. Matthias A, Ohlson KB, Fredriksson JM, Jacobsson A, Nedergaard J, Cannon B. Thermogenic responses in brown fat cells are fully UCP1- dependent. UCP2 or UCP3 do not substitute for UCP1 in adrenergically or fatty scid-induced thermogenesis. J Biol Chem. 2000;275:25073-25081.
38. Fredriksson JM, Nikami H, Nedergaard J. Cold-induced expression of the VEGF gene in brown adipose tissue is independent of thermogenic oxygen consumption. FEBS Lett. 2005;579:5680-5684. (Pubitemid 41455648)
39. Xue Y, Petrovic N, Cao R, Larsson O, Lim S, Chen S, Feldmann HM, Liang Z, Zhu Z, Nedergaard J, Cannon B, Cao Y. Hypoxia-independent angiogenesis in adipose tissues during cold acclimation. Cell Metab. 2009;9:99-109.
40. Maling HM, Highman B. Exaggerated ventricular arrhythmias and myocardial fatty changes after large doses of norepinephrine and epinephrine in unanesthetized dogs. Am J Physiol. 1958;194:590-596.