Adipose vascular endothelial growth factor regulates metabolic homeostasis through angiogenesis

Cell Metabolism

Volumn 17, Issue 1, 2013, Pages 61-72

  Sung, Hoon Ki ^a   Doh, Kyung Oh ^b   Son, Joe Eun ^a   Park, Jin Gyoon ^a   Bae, Yunui ^b   Choi, Soojeong ^a   Nelson, Seana Mary Lunney ^a,d   Cowling, Rebecca ^a   Nagy, Kristina ^a   Michael, Iacovos P ^a   Koh, Gou Young ^c   Adamson, S Lee ^a,d   Pawson, Tony ^a,d   Nagy, Andras ^a,d  

^a MOUNT SINAI HOSPITAL   (Canada)

^b Yeungnam University College of Medicine   (South Korea)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; VASCULOTROPIN;

ADIPOSE TISSUE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DENSITY; CELL METABOLISM; CONTROLLED STUDY; GENE DELETION; GENE INDUCTION; GENE OVEREXPRESSION; HOMEOSTASIS; HYPOXEMIA; INBORN ERROR OF METABOLISM; INFLAMMATION; LIPID DIET; LIPID METABOLISM; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ADIPOKINES; ADIPOSE TISSUE; ANIMALS; APOPTOSIS; DIET, HIGH-FAT; DOXYCYCLINE; GLUCOSE INTOLERANCE; INFLAMMATION; INSULIN RESISTANCE; MACROPHAGES; MICE; MICE, TRANSGENIC; MODELS, ANIMAL; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MUS;

EID: 84872158534     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2012.12.010     Document Type: Article

References (66)

1. A.L. Akeson, J.M. Greenberg, J.E. Cameron, F.Y. Thompson, S.K. Brooks, D. Wiginton, and J.A. Whitsett Temporal and spatial regulation of VEGF-A controls vascular patterning in the embryonic lung Dev. Biol. 264 2003 443 455 (Pubitemid 37490980)
2. F. Baffert, T. Le, B. Sennino, G. Thurston, C.J. Kuo, D. Hu-Lowe, and D.M. McDonald Cellular changes in normal blood capillaries undergoing regression after inhibition of VEGF signaling Am. J. Physiol. Heart Circ. Physiol. 290 2006 H547 H559
3. S. Basaria, M. Braga, and W.T. Moore Doxycycline-induced hypoglycemia in a nondiabetic young man South. Med. J. 95 2002 1353 1354 (Pubitemid 36109353)
4. G. Belteki, J. Haigh, N. Kabacs, K. Haigh, K. Sison, F. Costantini, J. Whitsett, S.E. Quaggin, and A. Nagy Conditional and inducible transgene expression in mice through the combinatorial use of Cre-mediated recombination and tetracycline induction Nucleic Acids Res. 33 2005 e51 10.1093/nar/gni051 (Pubitemid 41418409)
5. E. Bråkenhielm, R. Cao, B. Gao, B. Angelin, B. Cannon, P. Parini, and Y. Cao Angiogenesis inhibitor, TNP-470, prevents diet-induced and genetic obesity in mice Circ. Res. 94 2004 1579 1588 (Pubitemid 38856965)
6. Y. Cao Angiogenesis modulates adipogenesis and obesity J. Clin. Invest. 117 2007 2362 2368 (Pubitemid 47494333)
7. Y. Cao Adipose tissue angiogenesis as a therapeutic target for obesity and metabolic diseases Nat. Rev. Drug Discov. 9 2010 107 115
8. P. Carmeliet Angiogenesis in health and disease Nat. Med. 9 2003 653 660 (Pubitemid 36749213)
9. P. Carmeliet, B.W. Wong, and K. De Bock Treating diabetes by blocking a vascular growth factor Cell Metab. 16 2012 553 555
10. J.T. Chi, Z. Wang, D.S. Nuyten, E.H. Rodriguez, M.E. Schaner, A. Salim, Y. Wang, G.B. Kristensen, A. Helland, and A.L. Børresen-Dale Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers PLoS Med. 3 2006 e47 10.1371/journal.pmed.0030047
11. C.H. Cho, Y.J. Koh, J. Han, H.K. Sung, H. Jong Lee, T. Morisada, R.A. Schwendener, R.A. Brekken, G. Kang, and Y. Oike Angiogenic role of LYVE-1-positive macrophages in adipose tissue Circ. Res. 100 2007 e47 e57
12. V. Christiaens, and H.R. Lijnen Angiogenesis and development of adipose tissue Mol. Cell. Endocrinol. 318 2010 2 9
13. S. Cinti, G. Mitchell, G. Barbatelli, I. Murano, E. Ceresi, E. Faloia, S. Wang, M. Fortier, A.S. Greenberg, and M.S. Obin Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans J. Lipid Res. 46 2005 2347 2355 (Pubitemid 41532523)
14. I. Elias, S. Franckhauser, T. Ferré, L. Vilà, S. Tafuro, S. Muñoz, C. Roca, D. Ramos, A. Pujol, and E. Riu Adipose tissue overexpression of vascular endothelial growth factor protects against diet-induced obesity and insulin resistance Diabetes 61 2012 1801 1813
15. M. Ema, S. Takahashi, and J. Rossant Deletion of the selection cassette, but not cis-acting elements, in targeted Flk1-lacZ allele reveals Flk1 expression in multipotent mesodermal progenitors Blood 107 2006 111 117 (Pubitemid 43053531)
16. J. Folkman Angiogenesis in cancer, vascular, rheumatoid and other disease Nat. Med. 1 1995 27 31
17. G.H. Fong, J. Rossant, M. Gertsenstein, and M.L. Breitman Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium Nature 376 1995 66 70
18. Y. Fu, N. Luo, and M.F. Lopes-Virella Oxidized LDL induces the expression of ALBP/aP2 mRNA and protein in human THP-1 macrophages J. Lipid Res. 41 2000 2017 2023 (Pubitemid 32038997)
19. M. Furuhashi, R. Fucho, C.Z. Görgün, G. Tuncman, H. Cao, and G.S. Hotamisligil Adipocyte/macrophage fatty acid-binding proteins contribute to metabolic deterioration through actions in both macrophages and adipocytes in mice J. Clin. Invest. 118 2008 2640 2650 (Pubitemid 351949791)
20. I.C. Gaemers, J.M. Stallen, C. Kunne, C. Wallner, J. van Werven, A. Nederveen, and W.H. Lamers Lipotoxicity and steatohepatitis in an overfed mouse model for non-alcoholic fatty liver disease Biochim. Biophys. Acta 1812 2011 447 458
21. V.P. Garbitelli Tetracycline reduces the need for insulin N. Y. State J. Med. 87 1987 576 (Pubitemid 18008988)
22. H.P. Gerber, K.J. Hillan, A.M. Ryan, J. Kowalski, G.A. Keller, L. Rangell, B.D. Wright, F. Radtke, M. Aguet, and N. Ferrara VEGF is required for growth and survival in neonatal mice Development 126 1999 1149 1159 (Pubitemid 29182112)
23. G.H. Goossens, A. Bizzarri, N. Venteclef, Y. Essers, J.P. Cleutjens, E. Konings, J.W. Jocken, M. Cajlakovic, V. Ribitsch, K. Clément, and E.E. Blaak Increased adipose tissue oxygen tension in obese compared with lean men is accompanied by insulin resistance, impaired adipose tissue capillarization, and inflammation Circulation 124 2011 67 76
24. M.F. Gregor, and G.S. Hotamisligil Thematic review series: Adipocyte Biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease J. Lipid Res. 48 2007 1905 1914 (Pubitemid 47360610)
25. C.E. Hagberg, A. Falkevall, X. Wang, E. Larsson, J. Huusko, I. Nilsson, L.A. van Meeteren, E. Samen, L. Lu, and M. Vanwildemeersch Vascular endothelial growth factor B controls endothelial fatty acid uptake Nature 464 2010 917 921
26. C.E. Hagberg, A. Mehlem, A. Falkevall, L. Muhl, B.C. Fam, H. Ortsäter, P. Scotney, D. Nyqvist, E. Samén, and L. Lu Targeting VEGF-B as a novel treatment for insulin resistance and type 2 diabetes Nature 490 2012 426 430
27. N. Halberg, T. Khan, M.E. Trujillo, I. Wernstedt-Asterholm, A.D. Attie, S. Sherwani, Z.V. Wang, S. Landskroner-Eiger, S. Dineen, and U.J. Magalang Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue Mol. Cell. Biol. 29 2009 4467 4483
28. G.J. Hausman, and R.L. Richardson Adipose tissue angiogenesis J. Anim. Sci. 82 2004 925 934 (Pubitemid 38572359)
29. W. He, Y. Barak, A. Hevener, P. Olson, D. Liao, J. Le, M. Nelson, E. Ong, J.M. Olefsky, and R.M. Evans Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle Proc. Natl. Acad. Sci. USA 100 2003 15712 15717 (Pubitemid 38021055)
30. N. Hosogai, A. Fukuhara, K. Oshima, Y. Miyata, S. Tanaka, K. Segawa, S. Furukawa, Y. Tochino, R. Komuro, M. Matsuda, and I. Shimomura Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation Diabetes 56 2007 901 911 (Pubitemid 46525054)
31. G.S. Hotamisligil Inflammation and metabolic disorders Nature 444 2006 860 867 (Pubitemid 46024993)
32. N. Houstis, E.D. Rosen, and E.S. Lander Reactive oxygen species have a causal role in multiple forms of insulin resistance Nature 440 2006 944 948
33. T. Kamba, B.Y. Tam, H. Hashizume, A. Haskell, B. Sennino, M.R. Mancuso, S.M. Norberg, S.M. O'Brien, R.B. Davis, and L.C. Gowen VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature Am. J. Physiol. Heart Circ. Physiol. 290 2006 H560 H576
34. R.S. Kerbel Tumor angiogenesis N. Engl. J. Med. 358 2008 2039 2049 (Pubitemid 351656458)
35. J.Y. Kim, E. van de Wall, M. Laplante, A. Azzara, M.E. Trujillo, S.M. Hofmann, T. Schraw, J.L. Durand, H. Li, and G. Li Obesity-associated improvements in metabolic profile through expansion of adipose tissue J. Clin. Invest. 117 2007 2621 2637 (Pubitemid 47494363)
36. H.R. Lijnen Angiogenesis and obesity Cardiovasc. Res. 78 2008 286 293 (Pubitemid 351556088)
37. H.R. Lijnen, V. Christiaens, I. Scroyen, G. Voros, M. Tjwa, P. Carmeliet, and D. Collen Impaired adipose tissue development in mice with inactivation of placental growth factor function Diabetes 55 2006 2698 2704 (Pubitemid 44923667)
38. X. Liu, L. Hao, S. Zhang, Y. Ji, Y. Zhang, X. Lu, B. Shi, H. Pei, Y. Wang, and D. Chen Genetic repression of mouse VEGF expression regulates coagulation cascade IUBMB Life 62 2010 819 824
39. X. Lu, Y. Ji, L. Zhang, Y. Zhang, S. Zhang, Y. An, P. Liu, and Y. Zheng Resistance to obesity by repression of VEGF gene expression through induction of brown-like adipocyte differentiation Endocrinology 153 2012 3123 3132
40. L. Makowski, J.B. Boord, K. Maeda, V.R. Babaev, K.T. Uysal, M.A. Morgan, R.A. Parker, J. Suttles, S. Fazio, G.S. Hotamisligil, and M.F. Linton Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis Nat. Med. 7 2001 699 705 (Pubitemid 32588026)
41. G.J. Mick, X. Wang, and K. McCormick White adipocyte vascular endothelial growth factor: regulation by insulin Endocrinology 143 2002 948 953 (Pubitemid 34164042)
42. S. Miyazawa-Hoshimoto, K. Takahashi, H. Bujo, N. Hashimoto, and Y. Saito Elevated serum vascular endothelial growth factor is associated with visceral fat accumulation in human obese subjects Diabetologia 46 2003 1483 1488 (Pubitemid 37518569)
43. S. Miyazawa-Hoshimoto, K. Takahashi, H. Bujo, N. Hashimoto, K. Yagui, and Y. Saito Roles of degree of fat deposition and its localization on VEGF expression in adipocytes Am. J. Physiol. Endocrinol. Metab. 288 2005 E1128 E1136
44. M. Odeh, and A. Oliven Doxycycline-induced hypoglycemia J. Clin. Pharmacol. 40 2000 1173 1174
45. C.R. Ozawa, A. Banfi, N.L. Glazer, G. Thurston, M.L. Springer, P.E. Kraft, D.M. McDonald, and H.M. Blau Microenvironmental VEGF concentration, not total dose, determines a threshold between normal and aberrant angiogenesis J. Clin. Invest. 113 2004 516 527 (Pubitemid 38542501)
46. U. Ozcan, Q. Cao, E. Yilmaz, A.H. Lee, N.N. Iwakoshi, E. Ozdelen, G. Tuncman, C. Görgün, L.H. Glimcher, and G.S. Hotamisligil Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 2004 457 461 (Pubitemid 39372439)
47. M. Pasarica, O.R. Sereda, L.M. Redman, D.C. Albarado, D.T. Hymel, L.E. Roan, J.C. Rood, D.H. Burk, and S.R. Smith Reduced adipose tissue oxygenation in human obesity: evidence for rarefaction, macrophage chemotaxis, and inflammation without an angiogenic response Diabetes 58 2009 718 725
48. M. Pasarica, J. Rood, E. Ravussin, J.M. Schwarz, S.R. Smith, and L.M. Redman Reduced oxygenation in human obese adipose tissue is associated with impaired insulin suppression of lipolysis J. Clin. Endocrinol. Metab. 95 2010 4052 4055
49. M.A. Rupnick, D. Panigrahy, C.Y. Zhang, S.M. Dallabrida, B.B. Lowell, R. Langer, and M.J. Folkman Adipose tissue mass can be regulated through the vasculature Proc. Natl. Acad. Sci. USA 99 2002 10730 10735
50. D.B. Savage Mouse models of inherited lipodystrophy Dis. Model. Mech. 2 2009 554 562
51. K.R. Segal, J. Albu, A. Chun, A. Edano, B. Legaspi, and F.X. Pi-Sunyer Independent effects of obesity and insulin resistance on postprandial thermogenesis in men J. Clin. Invest. 89 1992 824 833
52. K.J. Strissel, Z. Stancheva, H. Miyoshi, J.W. Perfield 2nd, J. DeFuria, Z. Jick, A.S. Greenberg, and M.S. Obin Adipocyte death, adipose tissue remodeling, and obesity complications Diabetes 56 2007 2910 2918 (Pubitemid 350223625)
53. K. Sun, I. Wernstedt Asterholm, C.M. Kusminski, A.C. Bueno, Z.V. Wang, J.W. Pollard, R.A. Brekken, and P.E. Scherer Dichotomous effects of VEGF-A on adipose tissue dysfunction Proc. Natl. Acad. Sci. USA 109 2012 5874 5879
54. P. Trayhurn, B. Wang, and I.S. Wood Hypoxia in adipose tissue: a basis for the dysregulation of tissue function in obesity? Br. J. Nutr. 100 2008 227 235
55. S. Virtue, and A. Vidal-Puig Adipose tissue expandability, lipotoxicity and the Metabolic Syndrome - an allostatic perspective Biochim. Biophys. Acta 1801 2010 338 349
56. H. Waki, and P. Tontonoz Endocrine functions of adipose tissue Annu. Rev. Pathol. 2 2007 31 56 (Pubitemid 46448059)
57. S.P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R.L. Leibel, and A.W. Ferrante Jr. Obesity is associated with macrophage accumulation in adipose tissue J. Clin. Invest. 112 2003 1796 1808 (Pubitemid 38063703)
58. K.E. Wellen, and G.S. Hotamisligil Inflammation, stress, and diabetes J. Clin. Invest. 115 2005 1111 1119 (Pubitemid 40629025)
59. WHO (2010). 10 facts on obesity. WHO website, http://www.who.int/ features/factfiles/obesity/en/.
60. I.S. Wood, F.P. de Heredia, B. Wang, and P. Trayhurn Cellular hypoxia and adipose tissue dysfunction in obesity Proc. Nutr. Soc. 68 2009 370 377
61. H. Xu, G.T. Barnes, Q. Yang, G. Tan, D. Yang, C.J. Chou, J. Sole, A. Nichols, J.S. Ross, L.A. Tartaglia, and H. Chen Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance J. Clin. Invest. 112 2003 1821 1830 (Pubitemid 38063705)
62. D. Yach, D. Stuckler, and K.D. Brownell Epidemiologic and economic consequences of the global epidemics of obesity and diabetes Nat. Med. 12 2006 62 66 (Pubitemid 43050076)
63. T. Yamauchi, J. Kamon, H. Waki, Y. Terauchi, N. Kubota, K. Hara, Y. Mori, T. Ide, K. Murakami, and N. Tsuboyama-Kasaoka The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity Nat. Med. 7 2001 941 946 (Pubitemid 32756432)
64. T. Yamauchi, J. Kamon, Y. Minokoshi, Y. Ito, H. Waki, S. Uchida, S. Yamashita, M. Noda, S. Kita, and K. Ueki Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase Nat. Med. 8 2002 1288 1295 (Pubitemid 35373562)
65. J. Yin, Z. Gao, Q. He, D. Zhou, Z. Guo, and J. Ye Role of hypoxia in obesity-induced disorders of glucose and lipid metabolism in adipose tissue Am. J. Physiol. Endocrinol. Metab. 296 2009 E333 E342
66. Q.X. Zhang, C.J. Magovern, C.A. Mack, K.T. Budenbender, W. Ko, and T.K. Rosengart Vascular endothelial growth factor is the major angiogenic factor in omentum: mechanism of the omentum-mediated angiogenesis J. Surg. Res. 67 1997 147 154 (Pubitemid 27188010)