Endothelium as a gatekeeper of fatty acid transport

Trends in Endocrinology and Metabolism

Volumn 25, Issue 2, 2014, Pages 99-106

  Mehrotra, Devi ^a   Wu, Jingxia ^a   Papangeli, Irinna ^a   Chun, Hyung J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apelin; Endothelium; Fatty acid transport; PPAR ; VEGF B

Indexed keywords

APELIN; FATTY ACID; INSULIN; INSULIN SENSITIZING AGENT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; VASCULOTROPIN B;

CELL FUNCTION; DIABETES MELLITUS; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM; FATTY ACID TRANSPORT; HUMAN; METABOLIC SYNDROME X; NONHUMAN; OBESITY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

APELIN; ENDOTHELIUM; FATTY ACID TRANSPORT; PPAR-Γ; VEGF-B;

ADIPOSE TISSUE, WHITE; ANIMALS; BIOLOGICAL TRANSPORT; DIABETES MELLITUS; ENDOTHELIUM; FATTY ACIDS; HUMANS; INSULIN RESISTANCE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; OBESITY; PPAR GAMMA; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR B;

EID: 84892982580     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2013.11.001     Document Type: Review

References (98)

1. Florey L. The endothelial cell. Br. Med. J. 1966, 2:487-490.
2. Hsieh P.C., et al. Endothelial-cardiomyocyte interactions in cardiac development and repair. Annu. Rev. Physiol. 2006, 68:51-66.
3. Van der Vusse G.J., et al. Transport of long-chain fatty acids across the muscular endothelium. Adv. Exp. Med. Biol. 1998, 441:181-191.
4. Roden M., et al. Mechanism of free fatty acid-induced insulin resistance in humans. J. Clin. Invest. 1996, 97:2859-2865.
5. Samuel V.T., et al. Lipid-induced insulin resistance: unravelling the mechanism. Lancet 2010, 375:2267-2277.
6. Malik V.S., et al. Global obesity: trends, risk factors and policy implications. Nat. Rev. Endocrinol. 2013, 9:13-27.
7. Yudkin J.S., et al. Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the linkα. Atherosclerosis 2000, 148:209-214.
8. Ridker P.M., et al. Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation 2000, 101:1767-1772.
9. Ridker P.M., et al. Elevation of tumor necrosis factor-alpha and increased risk of recurrent coronary events after myocardial infarction. Circulation 2000, 101:2149-2153.
10. Huang P.L. eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrinol. Metab. 2009, 20:295-302.
11. Cai H., Harrison D.G. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ. Res. 2000, 87:840-844.
12. Olsson A.K., et al. VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 2006, 7:359-371.
13. Stuttfeld E., Ballmer-Hofer K. Structure and function of VEGF receptors. IUBMB Life 2009, 61:915-922.
14. Bry M., et al. Vascular endothelial growth factor-B acts as a coronary growth factor in transgenic rats without inducing angiogenesis, vascular leak, or inflammation. Circulation 2010, 122:1725-1733.
15. Zhang F., et al. VEGF-B is dispensable for blood vessel growth but critical for their survival, and VEGF-B targeting inhibits pathological angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:6152-6157.
16. Albrecht I., et al. Suppressive effects of vascular endothelial growth factor-B on tumor growth in a mouse model of pancreatic neuroendocrine tumorigenesis. PLoS ONE 2010, 5:e14109.
17. Karpanen T., et al. Overexpression of vascular endothelial growth factor-B in mouse heart alters cardiac lipid metabolism and induces myocardial hypertrophy. Circ. Res. 2008, 103:1018-1026.
18. Hagberg C.E., et al. Vascular endothelial growth factor B controls endothelial fatty acid uptake. Nature 2010, 464:917-921.
19. Hirsch D., et al. A family of fatty acid transporters conserved from mycobacterium to man. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:8625-8629.
20. Schaffer J.E., Lodish H.F. Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 1994, 79:427-436.
21. Kazantzis M., Stahl A. Fatty acid transport proteins, implications in physiology and disease. Biochim. Biophys. Acta 2012, 1821:852-857.
22. Hajri T., et al. Defective fatty acid uptake modulates insulin responsiveness and metabolic responses to diet in CD36-null mice. J. Clin. Invest. 2002, 109:1381-1389.
23. Calvo D., et al. Human CD36 is a high affinity receptor for the native lipoproteins HDL, LDL, and VLDL. J. Lipid Res. 1998, 39:777-788.
24. Hiratsuka S., et al. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:9349-9354.
25. Acevedo L.M., et al. Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeability factor. Blood 2008, 111:2674-2680.
26. Hagberg C.E., et al. Targeting VEGF-B as a novel treatment for insulin resistance and type 2 diabetes. Nature 2012, 490:426-430.
27. Genuth S.M., et al. Insulin resistance in genetically obese, hyperglycemic mice. Endocrinology 1971, 88:1230-1238.
28. Poesen K., et al. Novel role for vascular endothelial growth factor (VEGF) receptor-1 and its ligand VEGF-B in motor neuron degeneration. J. Neurosci. 2008, 28:10451-10459.
29. Li Y., et al. VEGF-B inhibits apoptosis via VEGFR-1-mediated suppression of the expression of BH3-only protein genes in mice and rats. J. Clin. Invest. 2008, 118:913-923.
30. Evans R.M., et al. PPARs and the complex journey to obesity. Nat. Med. 2004, 10:355-361.
31. Forman B.M., et al. 15-Deoxy-delta 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR gamma. Cell 1995, 83:803-812.
32. Forman B.M., et al. Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:4312-4317.
33. Forman B.M., et al. The peroxisome proliferator-activated receptors: ligands and activators. Ann. N. Y. Acad. Sci. 1996, 804:266-275.
34. Chandra V., et al. Structure of the intact PPAR-gamma-RXR-nuclear receptor complex on DNA. Nature 2008, 456:350-356.
35. Chawla A., et al. Nuclear receptors and lipid physiology: opening the X-files. Science 2001, 294:1866-1870.
36. Yki-Järvinen H. Thiazolidinediones. N. Engl. J. Med. 2004, 351:1106-1118.
37. Nissen S.E., Wolski K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N. Engl. J. Med. 2007, 356:2457-2471.
38. Lincoff A.M., et al. Pioglitazone and risk of cardiovascular events in patients with type 2 diabetes mellitus: a meta-analysis of randomized trials. JAMA 2007, 298:1180-1188.
39. Azoulay L., et al. The use of pioglitazone and the risk of bladder cancer in people with type 2 diabetes: nested case-control study. BMJ 2012, 344:e3645.
40. Neumann A., et al. Pioglitazone and risk of bladder cancer among diabetic patients in France: a population-based cohort study. Diabetologia 2012, 55:1953-1962.
41. Tontonoz P., Spiegelman B.M. Fat and beyond: the diverse biology of PPARgamma. Annu. Rev. Biochem. 2008, 77:289-312.
42. He W., et al. Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:15712-15717.
43. Lu M., et al. Brain PPAR-gamma promotes obesity and is required for the insulin-sensitizing effect of thiazolidinediones. Nat. Med. 2011, 17:618-622.
44. Ryan K.K., et al. A role for central nervous system PPAR-gamma in the regulation of energy balance. Nat. Med. 2011, 17:623-626.
45. Hevener A.L., et al. Muscle-specific Pparg deletion causes insulin resistance. Nat. Med. 2003, 9:1491-1497.
46. Norris A.W., et al. Muscle-specific PPARgamma-deficient mice develop increased adiposity and insulin resistance but respond to thiazolidinediones. J. Clin. Invest. 2003, 112:608-618.
47. Gavrilova O., et al. Liver peroxisome proliferator-activated receptor gamma contributes to hepatic steatosis, triglyceride clearance, and regulation of body fat mass. J. Biol. Chem. 2003, 278:34268-34276.
48. Goto K., et al. Peroxisome proliferator-activated receptor-gamma in capillary endothelia promotes fatty acid uptake by heart during long-term fasting. J. Am. Heart Assoc. 2013, 2:e004861.
49. Kanda T., et al. PPARgamma in the endothelium regulates metabolic responses to high-fat diet in mice. J. Clin. Invest. 2009, 119:110-124.
50. Marx N., et al. Peroxisome proliferator-activated receptor-gamma activators inhibit IFN-gamma-induced expression of the T cell-active CXC chemokines IP-10, Mig, and I-TAC in human endothelial cells. J. Immunol. 2000, 164:6503-6508.
51. Pasceri V., et al. Modulation of vascular inflammation in vitro and in vivo by peroxisome proliferator-activated receptor-gamma activators. Circulation 2000, 101:235-238.
52. Jackson S.M., et al. Peroxisome proliferator-activated receptor activators target human endothelial cells to inhibit leukocyte-endothelial cell interaction. Arterioscler. Thromb. Vasc. Biol. 1999, 19:2094-2104.
53. Furuhashi M., Hotamisligil G.S. Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat. Rev. Drug Discov. 2008, 7:489-503.
54. Antohe F., et al. Heart microvessels and aortic endothelial cells express the 15kDa heart-type fatty acid-binding proteins. Eur. J. Cell Biol. 1998, 76:102-109.
55. Elmasri H., et al. Fatty acid binding protein 4 is a target of VEGF and a regulator of cell proliferation in endothelial cells. FASEB J. 2009, 23:3865-3873.
56. Masouye I., et al. Endothelial cells of the human microvasculature express epidermal fatty acid-binding protein. Circ. Res. 1997, 81:297-303.
57. Febbraio M., et al. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J. Clin. Invest. 2001, 108:785-791.
58. Chu L.Y., et al. Thrombospondin-1 modulates VEGF signaling via CD36 by recruiting SHP-1 to VEGFR2 complex in microvascular endothelial cells. Blood 2013, 122:1822-1832.
59. Dawson D.W., et al. CD36 mediates the In vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol. 1997, 138:707-717.
60. Ibrahimi A., et al. Expression of the CD36 homolog (FAT) in fibroblast cells: effects on fatty acid transport. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:2646-2651.
61. Nickerson J.G., et al. Greater transport efficiencies of the membrane fatty acid transporters FAT/CD36 and FATP4 compared with FABPpm and FATP1 and differential effects on fatty acid esterification and oxidation in rat skeletal muscle. J. Biol. Chem. 2009, 284:16522-16530.
62. Coburn C.T., et al. Defective uptake and utilization of long chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J. Biol. Chem. 2000, 275:32523-32529.
63. Geloen A., et al. CD36 inhibitors reduce postprandial hypertriglyceridemia and protect against diabetic dyslipidemia and atherosclerosis. PLoS ONE 2012, 7:e37633.
64. Furuhashi M., et al. Treatment of diabetes and atherosclerosis by inhibiting fatty-acid-binding protein aP2. Nature 2007, 447:959-965.
65. Barnes G., et al. Translational promise of the apelin--APJ system. Heart 2010, 96:1011-1016.
66. Sheikh A.Y., et al. In vivo genetic profiling and cellular localization of apelin reveals a hypoxia-sensitive, endothelial-centered pathway activated in ischemic heart failure. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:88-98.
67. Boucher J., et al. Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology 2005, 146:1764-1771.
68. Daviaud D., et al. TNFalpha up-regulates apelin expression in human and mouse adipose tissue. FASEB J. 2006, 20:1528-1530.
69. Saint-Geniez M., et al. The msr/apj gene encoding the apelin receptor is an early and specific marker of the venous phenotype in the retinal vasculature. Gene Expr. Patterns 2003, 3:467-472.
70. Dray C., et al. Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab. 2008, 8:437-445.
71. Yue P., et al. Apelin is necessary for the maintenance of insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 2010, 298:59-67.
72. Yue P., et al. Apelin decreases lipolysis via G(q), G(i), and AMPK-dependent mechanisms. Endocrinology 2011, 152:59-68.
73. Attane C., et al. Apelin treatment increases complete fatty acid oxidation, mitochondrial oxidative capacity, and biogenesis in muscle of insulin-resistant mice. Diabetes 2012, 61:310-320.
74. Chun H.J., et al. Apelin signaling antagonizes Ang II effects in mouse models of atherosclerosis. J. Clin. Invest. 2008, 118:3343-3354.
75. Kidoya H., et al. Apelin induces enlarged and nonleaky blood vessels for functional recovery from ischemia. Blood 2010, 115:3166-3174.
76. McLean D.L., et al. Apelin/APJ signaling is a critical regulator of statin effects in vascular endothelial cells - brief report. Arterioscler. Thromb. Vasc. Biol. 2012, 32:2640-2643.
77. Sawane M., et al. Apelin inhibits diet-induced obesity by enhancing lymphatic and blood vessel integrity. Diabetes 2013, 62:1970-1980.
78. Sawane M., et al. Apelin attenuates UVB-induced edema and inflammation by promoting vessel function. Am. J. Pathol. 2011, 179:2691-2697.
79. Kim J., et al. An endothelial apelin-FGF link mediated by miR-424 and miR-503 is disrupted in pulmonary arterial hypertension. Nat. Med. 2013, 19:74-82.
80. Chandra S.M., et al. Disruption of the apelin-APJ system worsens hypoxia-induced pulmonary hypertension. Arterioscler. Thromb. Vasc. Biol. 2011, 31:814-820.
81. Kang Y., et al. Apelin-APJ signaling is a critical regulator of endothelial MEF2 activation in cardiovascular development. Circ. Res. 2013, 113:22-31.
82. Alastalo T.P., et al. Disruption of PPARgamma/beta-catenin-mediated regulation of apelin impairs BMP-induced mouse and human pulmonary arterial EC survival. J. Clin. Invest. 2011, 121:3735-3746.
83. Davies B.S., et al. GPIHBP1 is responsible for the entry of lipoprotein lipase into capillaries. Cell Metab. 2010, 12:42-52.
84. Davies B.S., et al. Assessing mechanisms of GPIHBP1 and lipoprotein lipase movement across endothelial cells. J. Lipid Res. 2012, 53:2690-2697.
85. Young S.G., Zechner R. Biochemistry and pathophysiology of intravascular and intracellular lipolysis. Genes Dev. 2013, 27:459-484.
86. Beigneux A.P., et al. Glycosylphosphatidylinositol-anchored high-density lipoprotein-binding protein 1 plays a critical role in the lipolytic processing of chylomicrons. Cell Metab. 2007, 5:279-291.
87. Wang J., Hegele R.A. Homozygous missense mutation (G56R) in glycosylphosphatidylinositol-anchored high-density lipoprotein-binding protein 1 (GPI-HBP1) in two siblings with fasting chylomicronemia (MIM 144650). Lipids Health Dis. 2007, 6:23.
88. Franssen R., et al. Chylomicronemia with low postheparin lipoprotein lipase levels in the setting of GPIHBP1 defects. Circ. Cardiovasc. Genet. 2010, 3:169-178.
89. Olivecrona G., et al. Mutation of conserved cysteines in the Ly6 domain of GPIHBP1 in familial chylomicronemia. J. Lipid Res. 2010, 51:1535-1545.
90. Beigneux A.P., et al. Chylomicronemia with a mutant GPIHBP1 (Q115P) that cannot bind lipoprotein lipase. Arterioscler. Thromb. Vasc. Biol. 2009, 29:956-962.
91. Charriere S., et al. GPIHBP1 C89F neomutation and hydrophobic C-terminal domain G175R mutation in two pedigrees with severe hyperchylomicronemia. J. Clin. Endocrinol. Metab. 2011, 96:1675-1679.
92. Voss C.V., et al. Mutations in lipoprotein lipase that block binding to the endothelial cell transporter GPIHBP1. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:7980-7984.
93. Olivecrona G., Beisiegel U. Lipid binding of apolipoprotein CII is required for stimulation of lipoprotein lipase activity against apolipoprotein CII-deficient chylomicrons. Arterioscler. Thromb. Vasc. Biol. 1997, 17:1545-1549.
94. Sukonina V., et al. Angiopoietin-like protein 4 converts lipoprotein lipase to inactive monomers and modulates lipase activity in adipose tissue. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:17450-17455.
95. Schoonjans K., et al. PPARalpha and PPARgamma activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene. EMBO J. 1996, 15:5336-5348.
96. Davies B.S., et al. The expression of GPIHBP1, an endothelial cell binding site for lipoprotein lipase and chylomicrons, is induced by peroxisome proliferator-activated receptor-gamma. Mol. Endocrinol. 2008, 22:2496-2504.
97. Jun J.C., et al. Acute hypoxia induces hypertriglyceridemia by decreasing plasma triglyceride clearance in mice. Am. J. Physiol. Endocrinol. Metab. 2012, 303:377-388.
98. Mead J.R., et al. Lipoprotein lipase: structure, function, regulation, and role in disease. J. Mol. Med. 2002, 80:753-769.