862
Views
14
CrossRef citations to date
0
Altmetric
Review Article

Diabetic vascular disease and the potential role of macrophage glucose metabolism

&
Pages 555-563 | Received 13 Dec 2010, Accepted 19 Apr 2011, Published online: 10 Sep 2012

References

  • Lehto S, Rönnemaa T, Pyörälä K, Laakso M. Poor glycemic control predicts coronary heart disease events in patients with type 1 diabetes without nephropathy. Arterioscler Thromb Vasc Biol. 1999;19:1014–9.
  • Nathan DM, Cleary PA, Backlund JY, Genuth SM, Lachin JM, Orchard TJ, . Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med. 2005;353:2643–53.
  • Eeg-Olofsson K, Cederholm J, Nilsson PM, Zethelius B, Svensson A-M, Gudbjörnsdóttir S, . Glycemic control and cardiovascular disease in 7,454 patients with type 1 diabetes. An observational study from the Swedish National Diabetes Register (NDR). Diabetes Care. 2010;33:1640–6.
  • Effect of intensive diabetes management on macrovascular events and risk factors in the Diabetes Control and Complications Trial (DCCT). Am J Cardiol. 1995;75:894–903.
  • Orchard TJ, Olson JC, Erbey JR, Williams K, Forrest KY, Smithline Kinder L, . Insulin resistance-related factors, but not glycemia, predict coronary artery disease in type 1 diabetes: 10-year follow-up data from the Pittsburgh Epidemiology of Diabetes Complications Study. Diabetes Care. 2003;26:1374–9.
  • Prince CT, Becker DJ, Costacou T, Miller RG, Orchard TJ. Changes in glycaemic control and risk of coronary artery disease in type 1 diabetes mellitus: findings from the Pittsburgh Epidemiology of Diabetes Complications Study (EDC). Diabetologia. 2007;50:2280–8.
  • Soranzo N, Sanna S, Wheeler E, Gieger C, Radke D, Dupuis J, . Common variants at 10 genomic loci influence hemoglobin A1C levels via glycemic and nonglycemic pathways. Diabetes. 2010;59:3229–39.
  • Holman RR, Paul SK, Bethel MA, Matthews DR, Neil HA. 10-year follow-up of intensive glucose control in type 2 diabetes. N Engl J Med. 2008;359:1577–89.
  • Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet. 1998; 352:837–53.
  • Gerstein HC, Miller ME, Byington RP, Goff DC Jr, Bigger JT, Buse JB, . Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med. 2008;358:2545–59.
  • ADVANCE Collaborative Group; Patel A, MacMahon S, Chalmers J, Neal B, Billot L, Woodward M, . Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med. 2008;358:2560–72.
  • Zoungas S, Patel A, Chalmers J, de Galan BE, Li Q, Billot L, . Severe hypoglycemia and risks of vascular events and death. N Engl J Med. 2010;363:1410–8.
  • Kannel WB, McGee DL. Diabetes and glucose tolerance as risk factors for cardiovascular disease: the Framingham study. Diabetes Care. 1979;2:120–6.
  • Renard CB, Kramer F, Johansson F, Lamharzi N, Tannock LR, von Herrath MG, . Diabetes and diabetes-associated lipid abnormalities have distinct effects on initiation and progression of atherosclerotic lesions. J Clin Invest. 2004;114: 659–68.
  • Vikramadithyan RK, Hu Y, Noh HL, Liang CP, Hallam K, Tall AR, . Human aldose reductase expression accelerates diabetic atherosclerosis in transgenic mice. J Clin Invest. 2005;115:2434–43.
  • Johansson F, Kramer F, Barnhart S, Kanter JE, Vaisar T, Merrill RD, . Type 1 diabetes promotes disruption of advanced atherosclerotic lesions in LDL receptor-deficient mice. Proc Natl Acad Sci USA. 2008;105:2082–7.
  • El-Osta A, Brasacchio D, Yao D, Pocai A, Jones PL, Roeder RG, . Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med. 2008;205:2409–17.
  • Duff GL, Payne TP. The effect of alloxan diabetes on experimental cholesterol atherosclerosis in the rabbit. III. The mechanism of the inhibition of experimental cholesterol atherosclerosis in alloxan-diabetic rabbits. J Exp Med. 1950; 92:299–317.
  • Gerrity RG, Natarajan R, Nadler JL, Kimsey T. Diabetes-induced accelerated atherosclerosis in swine. Diabetes. 2001; 50:1654–65.
  • Kanter JE, Johansson F, LeBoeuf RC, Bornfeldt KE. Do glucose and lipids exert independent effects on atherosclerotic lesion initiation or progression to advanced plaques? Circ Res. 2007;100:769–81.
  • Park L, Raman KG, Lee KJ, Lu Y, Ferran LJ Jr, Chow WS, . Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat Med. 1998;4:1025–31.
  • Reaven P, Merat S, Casanada F, Sutphin M, Palinski W. Effect of streptozotocin-induced hyperglycemia on lipid profiles, formation of advanced glycation endproducts in lesions, and extent of atherosclerosis in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol. 1997;17:2250–6.
  • Dixon JL, Shen S, Vuchetich JP, Wysocka E, Sun GY, Sturek M. Increased atherosclerosis in diabetic dyslipidemic swine: protection by atorvastatin involves decreased VLDL triglycerides but minimal effects on the lipoprotein profile. J Lipid Res. 2002;43:1618–29.
  • Adhikari N, Basi DL, Carlson M, Mariash A, Hong Z, Lehman U, . Increase in GLUT1 in smooth muscle alters vascular contractility and increases inflammation in response to vascular injury. Arterioscler Thromb Vasc Biol. 2011;31:86–94.
  • Soro-Paavonen A, Watson AM, Li J, Paavonen K, Koitka A, Calkin AC, . Receptor for advanced glycation end products (RAGE) deficiency attenuates the development of atherosclerosis in diabetes. Diabetes. 2008;57:2461–9.
  • Harja E, Bu DX, Hudson BI, Chang JS, Shen X, Hallam K, . Vascular and inflammatory stresses mediate atherosclerosis via RAGE and its ligands in apoE-/- mice. J Clin Invest. 2008;118:183–94.
  • Preusch MR, Morris-Rosenfeld S, Bierhaus A, Albrecht C, Erwin Blessing E, Andrassy M, . Deletion of bone marrow derived receptor for advanced glycation end-products (RAGE) does not attenuate plaque formation but inhibits plaque progression in a mouse model of advanced atherosclerosis. Circulation. 2009;120:S1137–8, Abstract 5672.
  • Booth G, Stalker TJ, Lefer AM, Scalia R. Elevated ambient glucose induces acute inflammatory events in the microvasculature: effects of insulin. Am J Physiol Endocrinol Metab. 2001;280:E848–56.
  • Azcutia V, Abu-Taha M, Romacho T, Vázquez-Bella M, Matesanz N, Luscinskas FW, . Inflammation determines the pro-adhesive properties of high extracellular d-glucose in human endothelial cells in vitro and rat microvessels in vivo. PLoS One. 2010;5:e10091.
  • Gerrity RG, Naito HK, Richardson M, Schwartz CJ. Dietary induced atherogenesis in swine. Morphology of the intima in prelesion stages. Am J Pathol. 1979;95:775–92.
  • Zhu SN, Chen M, Jongstra-Bilen J, Cybulsky MI. GM-CSF regulates intimal cell proliferation in nascent atherosclerotic lesions. J Exp Med. 2009;206:2141–9.
  • Hansch A, Stiehl P, Geiler G. [Quantification of macrophages and granulocytes at the joint cartilage-pannus junction in rheumatoid arthritis]. Z Rheumatol. 1996;55: 401–9.
  • Hunt TK, Knighton DR, Thakral KK, Goodson WH 3rd, Andrews WS. Studies on inflammation and wound healing: angiogenesis and collagen synthesis stimulated in vivo by resident and activated wound macrophages. Surgery. 1984;96:48–54.
  • Lewis JS, Lee JA, Underwood JC, Harris AL, Lewis CE. Macrophage responses to hypoxia: relevance to disease mechanisms. J Leukoc Biol. 1999;66:889–900.
  • Krawczyk CM, Holowka T, Sun J, Blagih J, Amiel E, DeBerardinis RJ, . Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood. 2010;115:4742–9.
  • Newsholme P, Newsholme EA. Rates of utilization of glucose, glutamine and oleate and formation of end-products by mouse peritoneal macrophages in culture. Biochem J. 1989;261:211–8.
  • Newsholme P, Gordon S, Newsholme EA. Rates of utilization and fates of glucose, glutamine, pyruvate, fatty acids and ketone bodies by mouse macrophages. Biochem J. 1987;242: 631–6.
  • Roiniotis J, Dinh H, Masendycz P, Turner A, Elsegood CL, Scholz GM, . Hypoxia prolongs monocyte/macrophage survival and enhanced glycolysis is associated with their maturation under aerobic conditions. J Immunol. 2009;182: 7974–81.
  • Ross R. Atherosclerosis—an inflammatory disease. N Engl J Med. 1999;340:115–26.
  • Weber C, Zernecke A, Libby P. The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat Rev Immunol. 2008;8:802–15.
  • Björnheden T, Levin M, Evaldsson M, Wiklund O. Evidence of hypoxic areas within the arterial wall in vivo. Arterioscler Thromb Vasc Biol. 1999;19:870–6.
  • Leppänen O, Björnheden T, Evaldsson M, Borén J, Wiklund O, Levin M. ATP depletion in macrophages in the core of advanced rabbit atherosclerotic plaques in vivo. Atherosclerosis. 2006;188:323–30.
  • Hiari N, Rudd JH. FDG PET imaging and cardiovascular inflammation. Curr Cardiol Rep. 2011;13:43–8.
  • Chen W, Bural GG, Torigian DA, Rader DJ, Alavi A. Emerging role of FDG-PET/CT in assessing atherosclerosis in large arteries. Eur J Nucl Med Mol Imaging. 2009;36: 144–51.
  • Kim TN, Kim S, Yang SJ, Yoo HJ, Seo JA, Kim SG, . Vascular inflammation in patients with impaired glucose tolerance and type 2 diabetes: analysis with 18F-fluorodeoxyglucose positron emission tomography. Circ Cardiovasc Imaging. 2010;3:142–8.
  • Thorens B, Mueckler M. Glucose transporters in the 21st Century. Am J Physiol Endocrinol Metab. 2010;298:E141–5.
  • Malide D, Davies-Hill TM, Levine M, Simpson IA. Distinct localization of GLUT-1, -3, and -5 in human monocyte-derived macrophages: effects of cell activation. Am J Physiol. 1998;274:E516–26.
  • Fu Y, Maianu L, Melbert BR, Garvey WT. Facilitative glucose transporter gene expression in human lymphocytes, monocytes, and macrophages: a role for GLUT isoforms 1, 3, and 5 in the immune response and foam cell formation. Blood Cells Mol Dis. 2004;32:182–90.
  • Chang M, Hamilton JA, Scholz GM, Masendycz P, Macaulay SL, Elsegood CL. Phosphatidylinostitol-3 kinase and phospholipase C enhance CSF-1-dependent macrophage survival by controlling glucose uptake. Cell Signal. 2009;21: 1361–9.
  • Okar DA, Manzano A, Navarro-Sabatè A, Riera L, Bartrons R, Lange AJ. PFK-2/FBPase-2: maker and breaker of the essential biofactor fructose-2,6-bisphosphate. Trends Biochem Sci. 2001;26:30–5.
  • Rider MH, Bertrand L, Vertommen D, Michels PA, Rousseau GG, Hue L. 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis. Biochem J. 2004;381:561–79.
  • Newsholme P, Curi R, Gordon S, Newsholme EA. Metabolism of glucose, glutamine, long-chain fatty acids and ketone bodies by murine macrophages. Biochem J. 1986; 239:121–5.
  • Aragonés J, Fraisl P, Baes M, Carmeliet P. Oxygen sensors at the crossroad of metabolism. Cell Metab. 2009;9:11–22.
  • Denko NC. Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer. 2008;8:705–13.
  • Cramer T, Yamanishi Y, Clausen BE, Förster I, Pawlinski R, Mackman N, . HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell. 2003;112:645–57.
  • Chan DA, Sutphin PD, Yen SE, Giaccia AJ. Coordinate regulation of the oxygen-dependent degradation domains of hypoxia-inducible factor 1α. Mol Cell Biol. 2005;25: 6415–26.
  • Berra E, Benizri E, Ginouvès A, Volmat V, Roux D, Pouysségur J. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1α in normoxia. EMBO J. 2003;22:4082–90.
  • Dann CE 3rd, Bruick RK, Deisenhofer J. Structure of factor-inhibiting hypoxia-inducible factor 1: an asparaginyl hydroxylase involved in the hypoxic response pathway. Proc Natl Acad Sci U S A. 2002;99:15351–6.
  • Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 2002;16:1466–71.
  • Sakamoto T, Seiki M. Mint3 enhances the activity of hypoxia-inducible factor-1 (HIF-1) in macrophages by suppressing the activity of factor inhibiting HIF-1. J Biol Chem. 2009;284:30350–9.
  • Sakamoto T, Seiki M. A membrane protease regulates energy production in macrophages by activating hypoxia-inducible factor-1 via a non-proteolytic mechanism. J Biol Chem. 2010; 285:29951–64.
  • Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;5:953–64.
  • Mantovani A, Sica A, Locati M. Macrophage polarization comes of age. Immunity. 2005;23:344–6.
  • Vats D, Mukundan L, Odegaard JI, Zhang L, Smith KL, Morel CR, . Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 2006;4:13–24.
  • Rodríguez-Prados JC, Través PG, Cuenca J, Rico D, Aragonés J, Martín-Sanz P, . Substrate fate in activated macrophages: a comparison between innate, classic, and alternative activation. J Immunol. 2010;185:605–14.
  • Fukuzumi M, Shinomiya H, Shimizu Y, Ohishi K, Utsumi S. Endotoxin-induced enhancement of glucose influx into murine peritoneal macrophages via GLUT1. Infect Immun. 1996;64:108–12.
  • Obach M, Navarro-Sabaté À, Caro J, Kong X, Duran J, Gómez M, . 6-Phosphofructo-2-kinase (pfkfb3) gene promoter contains hypoxia-inducible factor-1 binding sites necessary for transactivation in response to hypoxia. J Biol Chem. 2004;279:53562–70.
  • Bartrons R, Caro J. Hypoxia, glucose metabolism and the Warburg's effect. J Bioenerg Biomembr. 2007;39:223–9.
  • Minchenko A, Leshchinsky I, Opentanova I, Sang N, Srinivas V, Armstead V, . Hypoxia-inducible factor-1-mediated expression of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3 (PFKFB3) gene. Its possible role in the Warburg effect. J Biol Chem. 2002;277:6183–7.
  • Spolarics Z. Endotoxin stimulates gene expression of ROS-eliminating pathways in rat hepatic endothelial and Kupffer cells. Am J Physiol. 1996;270:G660–6.
  • Huo Y, Guo X, Li H, Wang H, Zhang W, Wang Y, . Disruption of inducible 6-phosphofructo-2-kinase ameliorates diet-induced adiposity but exacerbates systemic insulin resistance and adipose tissue inflammatory response. J Biol Chem. 2010;285:3713–21.
  • Ham M, Lee J-W, Choi AH, Masuzaki H, Kim JB. Increase of glucose-6-phosphate dehydrogenase in macrophage is associated with enhanced inflammatory responses in obesity. FASEB J. 2008;22:615.
  • Sanna F, Bonatesta RR, Frongia B, Uda S, Banni S, Melis MP, . Production of inflammatory molecules in peripheral blood mononuclear cells from severely glucose-6-phosphate dehydrogenase-deficient subjects. J Vasc Res. 2007;44:253–63.
  • Matsui R, Xu S, Maitland KA, Mastroianni R, Leopold JA, Handy DE, . Glucose-6-phosphate dehydrogenase deficiency decreases vascular superoxide and atherosclerotic lesions in apolipoprotein E(-/-) mice. Arterioscler Thromb Vasc Biol. 2006;26:910–6.
  • Ramana KV, Fadl AA, Tammali R, Reddy ABM, Chopra AK, Srivastava SK. Aldose reductase mediates the lipopolysaccharide-induced release of inflammatory mediators in RAW264.7 murine macrophages. J Biol Chem. 2006;281: 33019–29.
  • Gleissner CA, Sanders JM, Nadler J, Ley K. Upregulation of aldose reductase during foam cell formation as possible link among diabetes, hyperlipidemia, and atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28: 1137–43.
  • Woo HG, Jung YS, Baik EJ, Moon CH, Lee SH. The enhancement of endotoxin-induced nitric oxide production by elevation of glucose concentration in macrophage. Korean J Physiol Pharmacol. 1999;3:447–54.
  • Devaraj S, Glaser N, Griffen S, Wang-Polagruto J, Miguelino E, Jialal I. Increased monocytic activity and biomarkers of inflammation in patients with type 1 diabetes. Diabetes. 2006; 55:774–9.
  • Bradshaw EM, Raddassi K, Elyaman W, Orban T, Gottlieb PA, Kent SC, . Monocytes from patients with type 1 diabetes spontaneously secrete proinflammatory cytokines inducing Th17 cells. J Immunol. 2009;183:4432–9.
  • Wen Y, Gu J, Li SL, Reddy MA, Natarajan R, Nadler JL. Elevated glucose and diabetes promote interleukin-12 cytokine gene expression in mouse macrophages. Endocrinology. 2006;147:2518–25.
  • Padmos RC, Schloot NC, Beyan H, Ruwhof C, Staal FJ, de Ridder D, . Distinct monocyte gene-expression profiles in autoimmune diabetes. Diabetes. 2008;57: 2768–73.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.