Bioenergetic profiles diverge during macrophage polarization: Implications for the interpretation of 18F-FDG PET imaging of atherosclerosis

Journal of Nuclear Medicine

Volumn 54, Issue 9, 2013, Pages 1661-1667

  Tavakoli, Sina ^a   Zamora, Debora ^a,b   Ullevig, Sarah ^a   Asmis, Reto ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b TRINITY UNIVERSITY   (United States)

Author keywords

Glucose uptake; Macrophage polarization; Oxidative phosphorylation; PET

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; DEOXYGLUCOSE; FLUORODEOXYGLUCOSE F 18; GAMMA INTERFERON; GLUCOSE; GLUCOSE TRANSPORTER 1; HEXOKINASE 1; HEXOKINASE 2; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; DIAGNOSTIC AGENT; RADIOPHARMACEUTICAL AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ATHEROSCLEROSIS; BIOENERGY; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DISEASE COURSE; GENE DOSAGE; GENE EXPRESSION ASSAY; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; INTRACELLULAR TRANSPORT; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PERITONEUM MACROPHAGE; POLARIZATION; POLYMERASE CHAIN REACTION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RESPIRATORY CHAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; 18F-FDG; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL POLARITY; ENERGY METABOLISM; IMMUNOLOGY; MACROPHAGE; MACROPHAGE POLARIZATION; METHODOLOGY; PATHOLOGY; PET; SCINTISCANNING;

18F-FDG; GLUCOSE UPTAKE; MACROPHAGE POLARIZATION; OXIDATIVE PHOSPHORYLATION; PET;

ANIMALS; ATHEROSCLEROSIS; CELL POLARITY; CELLS, CULTURED; ENERGY METABOLISM; FLUORODEOXYGLUCOSE F18; MACROPHAGES; MICE; MICE, INBRED C57BL; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS;

EID: 84887357874     PISSN: 01615505     EISSN: None     Source Type: Journal    
DOI: 10.2967/jnumed.112.119099     Document Type: Article

References (40)

1. Tavakoli S, Sadeghi MM. Imaging of vascular biology in the heart. Curr Cardiovasc Imaging Rep. 2009;2:40-49.
2. Tavakoli S, Asmis R. Reactive oxygen species and thiol redox signaling in the macrophage biology of atherosclerosis. Antioxid Redox Signal. 2012;17:1785-1795.
3. Rabbani R, Topol EJ. Strategies to achieve coronary arterial plaque stabilization. Cardiovasc Res. 1999;41:402-417.
4. Myers KS, Rudd JH, Hailman EP, et al. Correlation between arterial FDG uptake and biomarkers in peripheral artery disease. JACC Cardiovasc Imaging. 2012;5:38-45.
5. Figueroa AL, Subramanian SS, Cury RC, et al. Distribution of inflammation within carotid atherosclerotic plaques with high-risk morphological features: a comparison between positron emission tomography activity, plaque morphology, and histopathology. Circ Cardiovasc Imaging. 2012;5:69-77.
6. Fayad ZA, Mani V, Woodward M, et al. Safety and efficacy of dalcetrapib on atherosclerotic disease using novel non-invasive multimodality imaging (dal- PLAQUE): a randomised clinical trial. Lancet. 2011;378:1547-1559.
7. Choi YS, Youn HJ, Chung WB, et al. Uptake of F-18 FDG and ultrasound analysis of carotid plaque. J Nucl Cardiol. 2011;18:267-272.
8. Wu YW, Kao HL, Huang CL, et al. The effects of 3-month atorvastatin therapy on arterial inflammation, calcification, abdominal adipose tissue and circulating biomarkers. Eur J Nucl Med Mol Imaging. 2012;39:399-407.
9. Laurberg JM, Olsen AK, Hansen SB, et al. Imaging of vulnerable atherosclerotic plaques with FDG-microPET: no FDG accumulation. Atherosclerosis. 2007; 192:275-282.
10. Rosenbaum D, Millon A, Fayad ZA. Molecular imaging in atherosclerosis: FDG PET. Curr Atheroscler Rep. 2012;14:429-437.
11. Gautier EL, Huby T, Witztum JL, et al. Macrophage apoptosis exerts divergent effects on atherogenesis as a function of lesion stage. Circulation. 2009;119:1795-1804.
12. Tabas I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol. 2010;10:36-46.
13. Folco EJ, Sheikine Y, Rocha VZ, et al. Hypoxia but not inflammation augments glucose uptake in human macrophages: implications for imaging atherosclerosis with 18fluorine-labeled 2-deoxy-D-glucose positron emission tomography. J Am Coll Cardiol. 2011;58:603-614.
14. Qiao M, Zhao Q, Lee CF, et al. Thiol oxidative stress induced by metabolic disorders amplifies macrophage chemotactic responses and accelerates atherogenesis and kidney injury in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2009;29:1779-1786.
15. Nicholls DG, Darley-Usmar VM, Wu M, Jensen PB, Rogers GW, Ferrick DA. Bioenergetic profile experiment using C2C12 myoblast cells. J Vis Exp. 2010;46:2511.
16. Guo W, Jiang L, Bhasin S, Khan SM, Swerdlow RH. DNA extraction procedures meaningfully influence qPCR-based mtDNA copy number determination. Mitochondrion. 2009;9:261-265.
17. Pena OM, Pistolic J, Raj D, Fjell CD, Hancock RE. Endotoxin tolerance represents a distinctive state of alternative polarization (M2) in human mononuclear cells. J Immunol. 2011;186:7243-7254.
18. Porta C, Rimoldi M, Raes G, et al. Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc Natl Acad Sci USA. 2009;106:14978-14983.
19. Aloj L, Caraco C, Jagoda E, Eckelman WC, Neumann RD. Glut-1 and hexokinase expression: relationship with 2-fluoro-2-deoxy-D-glucose uptake in A431 and T47D cells in culture. Cancer Res. 1999;59:4709-4714.
20. Través PG, de Atauri P, Marin S, et al. Relevance of the MEK/ERK signaling pathway in the metabolism of activated macrophages: a metabolomic approach. J Immunol. 2012;188:1402-1410.
21. Kelly DP, Scarpulla RC. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 2004;18:357-368.
22. Murdoch C, Muthana M, Lewis CE. Hypoxia regulates macrophage functions in inflammation. J Immunol. 2005;175:6257-6263.
23. Parathath S, Mick SL, Feig JE, et al. Hypoxia is present in murine atherosclerotic plaques and has multiple adverse effects on macrophage lipid metabolism. Circ Res. 2011;109:1141-1152.
24. Vink A, Schoneveld AH, Lamers D, et al. HIF-1 alpha expression is associated with an atheromatous inflammatory plaque phenotype and upregulated in activated macrophages. Atherosclerosis. 2007;195:e69-e75.
25. Cramer T, Yamanishi Y, Clausen BE, et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell. 2003;112:645-657.
26. Rogers IS, Nasir K, Figueroa AL, et al. Feasibility of FDG imaging of the coronary arteries: comparison between acute coronary syndrome and stable angina. JACC Cardiovasc Imaging. 2010;3:388-397.
27. Rudd JH, Myers KS, Bansilal S, et al. 18Fluorodeoxyglucose positron emission tomography imaging of atherosclerotic plaque inflammation is highly reproducible: implications for atherosclerosis therapy trials. J Am Coll Cardiol. 2007;50:892-896.
28. Rominger A, Saam T, Wolpers S, et al. 18F-FDG PET/CT identifies patients at risk for future vascular events in an otherwise asymptomatic cohort with neoplastic disease. J Nucl Med. 2009;50:1611-1620.
29. Rudd JH, Myers KS, Bansilal S, et al. Atherosclerosis inflammation imaging with 18F-FDG PET: carotid, iliac, and femoral uptake reproducibility, quantification methods, and recommendations. J Nucl Med. 2008;49:871-878.
30. Tawakol A, Migrino RQ, Bashian GG, et al. In vivo 18F-fluorodeoxyglucose positron emission tomography imaging provides a noninvasive measure of carotid plaque inflammation in patients. J Am Coll Cardiol. 2006;48:1818-1824.
31. Rudd JH, Warburton EA, Fryer TD, et al. Imaging atherosclerotic plaque inflammation with [18F]-fluorodeoxyglucose positron emission tomography. Circulation. 2002;105:2708-2711.
32. Marnane M, Merwick A, Sheehan OC, et al. Carotid plaque inflammation on 18Ffluorodeoxyglucose positron emission tomography predicts early stroke recurrence. Ann Neurol. 2012;71:709-718.
33. Waldo SW, Li Y, Buono C, et al. Heterogeneity of human macrophages in culture and in atherosclerotic plaques. Am J Pathol. 2008;172:1112-1126.
34. Khallou-Laschet J, Varthaman A, Fornasa G, et al. Macrophage plasticity in experimental atherosclerosis. PLoS ONE. 2010;5:e8852.
35. Parathath S, Grauer L, Huang LS, et al. Diabetes adversely affects macrophages during atherosclerotic plaque regression in mice. Diabetes. 2011;60:1759-1769.
36. Tawakol A, Rudd J, Fayad Z, Bosca L. Classical but not innate activation augments 2-deoxy-D-glucose uptake in macrophages: implications for atherosclerosis imaging [abstract]. J Nucl Med. 2012;53(suppl):464.
37. Vats D, Mukundan L, Odegaard JI, et al. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 2006;4:13-24.
38. Tavakoli S, Razavian M, Zhang J, et al. Matrix metalloproteinase activation predicts amelioration of remodeling after dietary modification in injured arteries. Arterioscler Thromb Vasc Biol. 2011;31:102-109.
39. Stoll LL, Denning GM, Weintraub NL. Potential role of endotoxin as a proinflammatory mediator of atherosclerosis. Arterioscler Thromb Vasc Biol. 2004; 24:2227-2236.
40. van der Windt GJ, Everts B, Chang CH, et al. Mitochondrial respiratory capacity is a critical regulator of CD81 T cell memory development. Immunity. 2012;36:68-78.