Meox2/Tcf15 heterodimers program the heart capillary endothelium for cardiac fatty acid uptake

Circulation

Volumn 131, Issue 9, 2015, Pages 815-826

  Coppiello, Giulia ^a   Collantes, Maria ^c   Sirerol Piquer, María Salomé ^d   Vandenwijngaert, Sara ^b   Schoors, Sandra ^b   Swinnen, Melissa ^b   Vandersmissen, Ine ^a   Herijgers, Paul ^b   Topal, Baki ^e   Van Loon, Johannes ^e   Goffin, Jan ^e   Prósper, Felipe ^c   Carmeliet, Peter ^b   García Verdugo, Jose Manuel ^d   Janssens, Stefan ^b   Peñuelas, Iván ^c   Aranguren, Xabier L ^a,c   Luttun, Aernout ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY CLINIC OF NAVARRA   (Spain)

^d UNIVERSITY OF VALENCIA   (Spain)

^e UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

Endothelium; Fatty acids; Heart; Metabolism; Transcription factors

Indexed keywords

APOLIPOPROTEIN B; CD36 ANTIGEN; CHYLOMICRON; FATTY ACID TRANSPORTER; GLUCOSE TRANSPORTER 1; HETERODIMER; LIPOPROTEIN LIPASE; MESENCHYME HOMEOBOX 2 PROTEIN; PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 15; UNCLASSIFIED DRUG; VASCULOTROPIN B; VERY LOW DENSITY LIPOPROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; FATTY ACID; FATTY ACID BINDING PROTEIN; GLUCOSE; HOMEODOMAIN PROTEIN; LPL PROTEIN, HUMAN; MEOX2 PROTEIN, MOUSE; SMALL INTERFERING RNA; TCF15 PROTEIN, MOUSE; TRANSCRIPTOME;

ADIPOSE TISSUE; ALLELE; ANIMAL CELL; ARTICLE; BRAIN; CAPILLARY DENSITY; COMPLEX FORMATION; ECHOCARDIOGRAPHY; ENDOTHELIUM; ENERGY YIELD; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SPACE; FATTY ACID TRANSPORT; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENETIC CODE; GENETIC SIGNATURE; HEART; HEART MUSCLE CAPILLARY; HEART MUSCLE CONTRACTILITY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LIPID STORAGE; LIPOLYSIS; LIVER; MICROARRAY ANALYSIS; MOLECULAR GENETICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; WHITE ADIPOSE TISSUE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CARDIAC OUTPUT, LOW; CELL CULTURE; CHEMISTRY; COMPARATIVE STUDY; CORONARY BLOOD VESSEL; CYTOLOGY; DEFICIENCY; ENDOTHELIUM CELL; GENETICS; HEART MUSCLE; HETEROZYGOTE; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS; TISSUE MICROARRAY; VASCULARIZATION;

ADIPOSE TISSUE; ANIMALS; ANTIGENS, CD36; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARDIAC OUTPUT, LOW; CELLS, CULTURED; CORONARY VESSELS; ENDOTHELIAL CELLS; FATTY ACID-BINDING PROTEINS; FATTY ACIDS; GLUCOSE; HETEROZYGOTE; HOMEODOMAIN PROTEINS; HUMANS; LIPOPROTEIN LIPASE; LIPOPROTEINS, VLDL; MICE; MICE, INBRED C57BL; MYOCARDIUM; PROTEIN INTERACTION MAPPING; RNA, SMALL INTERFERING; TISSUE ARRAY ANALYSIS; TRANSCRIPTOME;

EID: 84928766072     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.114.013721     Document Type: Article

References (39)

1. Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res. 2007;100:158-173. doi: 10.1161/01.RES.0000255691.76142.4a.
2. Géraud C, Schledzewski K, Demory A, Klein D, Kaus M, Peyre F, Sticht C, Evdokimov K, Lu S, Schmieder A, Goerdt S. Liver sinusoidal endothelium: a microenvironment-dependent differentiation program in rat including the novel junctional protein liver endothelial differentiation-associated protein-1. Hepatology. 2010;52:313-326. doi: 10.1002/hep.23618.
3. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010;37:13-25. doi: 10.1016/j.nbd.2009.07.030.
4. Brutsaert DL, Fransen P, Andries LJ, De Keulenaer GW, Sys SU. Cardiac endothelium and myocardial function. Cardiovasc Res. 1998;38:281-290.
5. Kuruvilla L, Kartha CC. Molecular mechanisms in endothelial regulation of cardiac function. Mol Cell Biochem. 2003;253:113-123.
6. Neubauer S. The failing heart-an engine out of fuel. N Engl J Med. 2007;356:1140-1151. doi: 10.1056/NEJMra063052.
7. Stanley WC, Recchia FA, Lopaschuk GD. Myocardial substrate metabolism in the normal and failing heart. Physiol Rev. 2005;85:1093-1129. doi: 10.1152/physrev.00006.2004.
8. Krishnan J, Suter M, Windak R, Krebs T, Felley A, Montessuit C, Tokarska-Schlattner M, Aasum E, Bogdanova A, Perriard E, Perriard JC, Larsen T, Pedrazzini T, Krek W. Activation of a HIF1alpha-PPARgamma axis underlies the integration of glycolytic and lipid anabolic pathways in pathologic cardiac hypertrophy. Cell Metab. 2009;9:512-524. doi: 10.1016/j.cmet.2009.05.005.
9. Battiprolu PK, Hojayev B, Jiang N, Wang ZV, Luo X, Iglewski M, Shelton JM, Gerard RD, Rothermel BA, Gillette TG, Lavandero S, Hill JA. Metabolic stress-induced activation of FoxO1 triggers diabetic cardiomyopathy in mice. J Clin Invest. 2012;122:1109-1118. doi: 10.1172/JCI60329.
10. Altin SE, Schulze PC. Metabolism of the right ventricle and the response to hypertrophy and failure. Prog Cardiovasc Dis. 2012;55:229-233. doi: 10.1016/j.pcad.2012.07.010.
11. Abel ED, O'Shea KM, Ramasamy R. Insulin resistance: metabolic mechanisms and consequences in the heart. Arterioscler Thromb Vasc Biol. 2012;32:2068-2076. doi: 10.1161/ATVBAHA.111.241984.
12. Rider OJ, Cox P, Tyler D, Clarke K, Neubauer S. Myocardial substrate metabolism in obesity. Int J Obes (Lond). 2013;37:972-979. doi: 10.1038/ijo.2012.170.
13. Glatz JF, Luiken JJ, Bonen A. Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol Rev. 2010;90:367-417. doi: 10.1152/physrev.00003.2009.
14. Hagberg C, Mehlem A, Falkevall A, Muhl L, Eriksson U. Endothelial fatty acid transport: role of vascular endothelial growth factor B. Physiology (Bethesda). 2013;28:125-134. doi: 10.1152/physiol.00042.2012.
15. Irie H, Krukenkamp IB, Brinkmann JF, Gaudette GR, Saltman AE, Jou W, Glatz JF, Abumrad NA, Ibrahimi A. Myocardial recovery from ischemia is impaired in CD36-null mice and restored by myocyte CD36 expression or medium-chain fatty acids. Proc Natl Acad Sci U S A. 2003;100:6819-6824. doi: 10.1073/pnas.1132094100.
16. van der Vusse GJ, van Bilsen M, Glatz JF. Cardiac fatty acid uptake and transport in health and disease. Cardiovasc Res. 2000;45:279-293.
17. Binas B, Danneberg H, McWhir J, Mullins L, Clark AJ. Requirement for the heart-type fatty acid binding protein in cardiac fatty acid utilization. FASEB J. 1999;13:805-812.
18. Steinbusch LK, Luiken JJ, Vlasblom R, Chabowski A, Hoebers NT, Coumans WA, Vroegrijk IO, Voshol PJ, Ouwens DM, Glatz JF, Diamant M. Absence of fatty acid transporter CD36 protects against Western-type diet-related cardiac dysfunction following pressure overload in mice. Am J Physiol Endocrinol Metab. 2011;301:E618-E627. doi: 10.1152/ajpendo.00106.2011.
19. Watanabe K, Ohta Y, Toba K, Ogawa Y, Hanawa H, Hirokawa Y, Kodama M, Tanabe N, Hirono S, Ohkura Y, Nakamura Y, Kato K, Aizawa Y, Fuse I, Miyajima S, Kusano Y, Nagamoto T, Hasegawa G, Naito M. Myocardial CD36 expression and fatty acid accumulation in patients with type I and II CD36 deficiency. Ann Nucl Med. 1998;12:261-266.
20. Heather LC, Cole MA, Lygate CA, Evans RD, Stuckey DJ, Murray AJ, Neubauer S, Clarke K. Fatty acid transporter levels and palmitate oxidation rate correlate with ejection fraction in the infarcted rat heart. Cardiovasc Res. 2006;72:430-437. doi: 10.1016/j.cardiores.2006.08.020.
21. Hagberg CE, Falkevall A, Wang X, Larsson E, Huusko J, Nilsson I, van Meeteren LA, Samen E, Lu L, Vanwildemeersch M, Klar J, Genove G, Pietras K, Stone-Elander S, Claesson-Welsh L, Ylä-Herttuala S, Lindahl P, Eriksson U. Vascular endothelial growth factor B controls endothelial fatty acid uptake. Nature. 2010;464:917-921. doi: 10.1038/nature08945.
22. Hagberg CE, Mehlem A, Falkevall A, Muhl L, Fam BC, Ortsäter H, Scotney P, Nyqvist D, Samén E, Lu L, Stone-Elander S, Proietto J, Andrikopoulos S, Sjöholm A, Nash A, Eriksson U. Targeting VEGF-B as a novel treatment for insulin resistance and type 2 diabetes. Nature. 2012;490:426-430. doi: 10.1038/nature11464.
23. Kanda T, Brown JD, Orasanu G, Vogel S, Gonzalez FJ, Sartoretto J, Michel T, Plutzky J. PPARgamma in the endothelium regulates metabolic responses to high-fat diet in mice. J Clin Invest. 2009;119:110-124. doi: 10.1172/JCI36233.
24. Burgess R, Rawls A, Brown D, Bradley A, Olson EN. Requirement of the paraxis gene for somite formation and musculoskeletal patterning. Nature. 1996;384:570-573. doi: 10.1038/384570a0.
25. Mankoo BS, Collins NS, Ashby P, Grigorieva E, Pevny LH, Candia A, Wright CV, Rigby PW, Pachnis V. Mox2 is a component of the genetic hierarchy controlling limb muscle development. Nature. 1999;400:69-73. doi: 10.1038/21892.
26. Burgess R, Cserjesi P, Ligon KL, Olson EN. Paraxis: a basic helix-loop-helix protein expressed in paraxial mesoderm and developing somites. Dev Biol. 1995;168:296-306. doi: 10.1006/dbio.1995.1081.
27. Gorski DH, Leal AJ. Inhibition of endothelial cell activation by the homeobox gene Gax. J Surg Res. 2003;111:91-99.
28. Wu Z, Guo H, Chow N, Sallstrom J, Bell RD, Deane R, Brooks AI, Kanagala S, Rubio A, Sagare A, Liu D, Li F, Armstrong D, Gasiewicz T, Zidovetzki R, Song X, Hofman F, Zlokovic BV. Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nat Med. 2005;11:959-965. doi: 10.1038/nm1287.
29. Quertermous EE, Hidai H, Blanar MA, Quertermous T. Cloning and characterization of a basic helix-loop-helix protein expressed in early mesoderm and the developing somites. Proc Natl Acad Sci U S A. 1994;91:7066-7070.
30. Aranguren XL, Beerens M, Coppiello G, Wiese C, Vandersmissen I, Nigro AL, Verfaillie CM, Gessler M, Luttun A. COUP-TFII orchestrates venous and lymphatic endothelial identity by homo- or heterodimerisation with PROX1. J Cell Sci.2013;126:1164-1175.
31. Calabria AR, Shusta EV. A genomic comparison of in vivo and in vitro brain microvascular endothelial cells. J Cereb Blood Flow Metab. 2008;28:135-148. doi: 10.1038/sj.jcbfm.9600518.
32. Aranguren XL, Agirre X, Beerens M, Coppiello G, Uriz M, Vandersmissen I, Benkheil M, Panadero J, Aguado N, Pascual-Montano A, Segura V, Prósper F, Luttun A. Unraveling a novel transcription factor code determining the human arterial-specific endothelial cell signature. Blood. 2013;122:3982-3992. doi: 10.1182/blood-2013-02-483255.
33. Iso T, Maeda K, Hanaoka H, Suga T, Goto K, Syamsunarno MR, Hishiki T, Nagahata Y, Matsui H, Arai M, Yamaguchi A, Abumrad NA, Sano M, Suematsu M, Endo K, Hotamisligil GS, Kurabayashi M. Capillary endothelial fatty acid binding proteins 4 and 5 play a critical role in fatty acid uptake in heart and skeletal muscle. Arterioscler Thromb Vasc Biol. 2013;33:2549-2557. doi: 10.1161/ATVBAHA.113.301588.
34. Davies BS, Beigneux AP, Fong LG, Young SG. New wrinkles in lipoprotein lipase biology. Curr Opin Lipidol. 2012;23:35-42. doi: 10.1097/MOL.0b013e32834d0b33.
35. Bharadwaj KG, Hiyama Y, Hu Y, Huggins LA, Ramakrishnan R, Abumrad NA, Shulman GI, Blaner WS, Goldberg IJ. Chylomicron- and VLDL-derived lipids enter the heart through different pathways: in vivo evidence for receptor- and non-receptor-mediated fatty acid uptake. J Biol Chem. 2010;285:37976-37986. doi: 10.1074/jbc.M110.174458.
36. Augustus AS, Buchanan J, Park TS, Hirata K, Noh HL, Sun J, Homma S, D'armiento J, Abel ED, Goldberg IJ. Loss of lipoprotein lipase-derived fatty acids leads to increased cardiac glucose metabolism and heart dysfunction. J Biol Chem. 2006;281:8716-8723. doi: 10.1074/jbc.M509890200.
37. van Bilsen M, van Nieuwenhoven FA, van der Vusse GJ. Metabolic remodelling of the failing heart: beneficial or detrimental? Cardiovasc Res. 2009;81:420-428. doi: 10.1093/cvr/cvn282.
38. Koskivirta I, Kassiri Z, Rahkonen O, Kiviranta R, Oudit GY, McKee TD, Kytö V, Saraste A, Jokinen E, Liu PP, Vuorio E, Khokha R. Mice with tissue inhibitor of metalloproteinases 4 (Timp4) deletion succumb to induced myocardial infarction but not to cardiac pressure overload. J Biol Chem. 2010;285:24487-24493. doi: 10.1074/jbc.M110.136820.
39. Kern CB, Wessels A, McGarity J, Dixon LJ, Alston E, Argraves WS, Geeting D, Nelson CM, Menick DR, Apte SS. Reduced versican cleavage due to Adamts9 haploinsufficiency is associated with cardiac and aortic anomalies. Matrix Biol. 2010;29:304-316. doi: 10.1016/j.matbio.2010.01.005.