Increased angiogenesis protects against adipose hypoxia and fibrosis in metabolic disease-resistant 11β-hydroxysteroid dehydrogenase type 1 (HSD1)-deficient mice

Journal of Biological Chemistry

Volumn 287, Issue 6, 2012, Pages 4188-4197

  Michailidou, Zoi ^a   Turban, Sophie ^b   Miller, Eileen ^b   Zou, Xiantong ^b   Schrader, Joerg ^a   Ratcliffe, Peter J ^c   Hadoke, Patrick W F ^b   Walker, Brian R ^b   Iredale, John P ^a   Morton, Nicholas M ^b   Seckl, Jonathan R ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOSE TISSUE; ANGIOGENESIS; ANGIOGENIC FACTOR; DIET-INDUCED OBESITY; FIBROGENESIS; HYDROXYSTEROID DEHYDROGENASE; HYPOXIA-INDUCIBLE FACTORS; INDUCIBLE EXPRESSION; INSULIN RESISTANCE; METABOLIC DISEASE; PEROXISOME PROLIFERATORS; SIGNALING PATHWAYS; SMOOTH MUSCLE ACTINS; WEIGHT GAIN;

CYTOLOGY; DEHYDROGENATION; MAMMALS; METABOLISM; PROTEINS; TISSUE;

NUTRITION;

11BETA HYDROXYSTEROID DEHYDROGENASE 1; ALPHA SMOOTH MUSCLE ACTIN; ANGIOPOIETIN; ANGIOPOIETIN LIKE PROTEIN 4; APELIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ADIPOCYTE; ADIPOSE TISSUE; ADULT ANIMAL; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET; ENZYME DEFICIENCY; FIBROGENESIS; FIBROSIS; HYPOXEMIA; MALE; METABOLIC DISORDER; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; VASCULARIZATION; WEIGHT GAIN;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; ACTINS; ADIPOSE TISSUE; ANGIOPOIETINS; ANIMALS; ANOXIA; FIBROSIS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INSULIN RESISTANCE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; OBESITY; PPAR GAMMA; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WEIGHT GAIN;

MUS;

EID: 84856728017     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.259325     Document Type: Article

References (38)

1. Hosogai, N., Fukuhara, A., Oshima, K., Miyata, Y., Tanaka, S., Segawa, K., Furukawa, S., Tochino, Y., Komuro, R., Matsuda, M., and Shimomura, I. (2007) Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 56, 901-911 (Pubitemid 46525054)
2. Rausch, M. E. Weisberg, S., Vardhana, P., and Tortoriello, D. V. (2008) Obesity in C57BL/6J mice is characterized by adipose tissue hypoxia and cytotoxic T-cell infiltration. Int. J. Obes. (Lon.) 32, 451-463 (Pubitemid 351414814)
3. Yin, J., Gao, Z., He, Q., Zhou, D., Guo, Z., and Ye, J. (2009) Role of hypoxia in obesity-induced disorders of glucose and lipid metabolism in adipose tissue. Am. J. Physiol. Endocrinol. Metab. 296, E333-E342
4. Pasarica, M., Sereda, O. R., Redman, L. M., Albarado, D. C., Hymel, D. T., Roan, L. E., Rood, J. C., Burk, D. H., and Smith, S. R. (2009) Reduced adipose tissue oxygenation in human obesity: evidence for rarefaction, macrophage chemotaxis, and inflammation without an angiogenic response. Diabetes 58, 718-725
5. Yun, Z., Maecker, H. L., Johnson, R. S., and Giaccia, A. J. (2002) Inhibition of PPARγ2 gene expression by the HIF-1-regulated gene DEC1/Stra13: a mechanism for regulation of adipogenesis by hypoxia. Dev. Cell 2, 331-341 (Pubitemid 34266118)
6. Shimba, S., Wada, T., Hara, S., Tezuka, M. (2004) EPAS1 promotes adipose differentiation in 3T3-L1 cells. J. Biol. Chem. 279, 40946-40953 (Pubitemid 39287694)
7. Halberg, N., Khan, T., Trujillo, M. E., Wernstedt-Asterholm, I., Attie, A. D., Sherwani, S., Wang, Z. V., Landskroner-Eiger, S., Dineen, S., Magalang, U. J., Brekken, R. A., and Scherer, P. E. (2009) Hypoxia-inducible factor 1α induces fibrosis and insulin resistance in white adipose tissue. Molecular and cellular biology 29, 4467-4483
8. Rask, E., Olsson, T., Söderberg, S., Andrew, R., Livingstone, D. E., Johnson, O., Walker, B. R. (2001) Tissue-specific dysregulation of cortisol metabolism in human obesity. J. Clin. Endocrinol. Metab. 86, 1418-1421 (Pubitemid 32323037)
9. Michailidou, Z., Jensen, M. D., Dumesic, D. A., Chapman, K. E., Seckl, J. R., Walker, B. R., and Morton, N. M (2007) Omental 11β-hydroxysteroid dehydrogenase 1 correlates with fat cell size independently of obesity. Obesity 15, 1155-1163 (Pubitemid 46932470)
10. Masuzaki, H., Paterson, J., Shinyama, H., Morton, N. M., Mullins, J. J., Seckl, J. R., and Flier, J. S. (2001) A transgenic model of visceral obesity and the metabolic syndrome. Science 294, 2166-2170 (Pubitemid 33150673)
11. Kotelevtsev, Y., Holmes, M. C., Burchell, A., Houston, P. M., Schmoll, D., Jamieson, P., Best, R., Brown, R., Edwards, C. R., Seckl, J. R., and Mullins, J. J. (1997) 11β-hydroxysteroid dehydrogenase type 1 knockout mice show attenuated glucocorticoid-inducible responses and resist hyperglycemia on obesity or stress. Proc. Natl. Acad. Sci. U.S.A. 94, 14924-14929 (Pubitemid 28041476)
12. Morton, N. M., Paterson, J. M., Masuzaki, H., Holmes, M. C., Staels, B., Fievet, C., Walker, B. R., Flier, J. S., Mullins, J. J., and Seckl, J. R. (2004) Novel adipose tissue-mediated resistance to diet-induced visceral obesity in 11β-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes 53, 931-938 (Pubitemid 38436604)
13. Wamil, M., Battle, J. H., Turban, S., Kipari, T., Seguret, D., de Sousa Peixoto, R., Nelson, Y. B., Nowakowska, D., Ferenbach, D., Ramage, L., Chapman, K. E., Hughes, J., Dunbar, D. R., Seckl, J. R., Morton, N. M. (2011) Novel fat depot-specific mechanisms underlie resistance to visceral obesity and inflammation in 11β-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes 60, 1158-1167
14. Small, G. R., Hadoke, P. W., Sharif, I., Dover, A. R., Armour, D., Kenyon, C. J., Gray, G. A., Walker, B. R. (2005) Preventing local regeneration of glucocorticoids by 11β-hydroxysteroid dehydrogenase type 1 enhances angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 102, 12165-12170 (Pubitemid 41291146)
15. McSweeney, S. J., Hadoke, P. W., Kozak, A. M, Small, G. R., Khaled, H., Walker, B. R., Gray, G. A. (2010) Improved heart function follows enhanced inflammatory cell recruitment and angiogenesis in 11βHSD1-deficient mice post-MI. Cardiovasc Res. 88, 159-167
16. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R., and Ratcliffe, P. J. (1999) The tumor suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275 (Pubitemid 29246458)
17. Epstein, A. C., Gleadle, J. M., McNeill, L. A., Hewitson, K. S., O'Rourke, J., Mole, D. R., Mukherji, M., Metzen, E., Wilson, M. I., Dhanda, A., Tian, Y. M., Masson, N., Hamilton, D. L., Jaakkola, P., Barstead, R., Hodgkin, J., Maxwell, P. H., Pugh, C. W., Schofield, C. J., and Ratcliffe, P. J. (2001) Caenorhabditis elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43-54 (Pubitemid 32972036)
18. Ivan, M., Kondo, K., Yang, H., Kim, W., Valiando, J., Ohh, M., Salic, A., Asara, J. M., Lane, W. S., and Kaelin, W. G., Jr. (2001) HIFα targeted for VHL-mediated destruction by proline hydroxylation: implications for O2sensing. Science 292, 464-468 (Pubitemid 32335941)
19. Copple, B. L., Bai, S., Moon, J. O. (2010) Hypoxia-inducible factor-dependent production of profibrotic mediators by hypoxic Kupffer cells. Hepatol. Res. 40, 530-539
20. Iredale, J. P. (2007) Models of liver fibrosis: exploring the dynamic nature of inflammation and repair in a solid organ. J. Clin. invest. 117, 539-548
21. Eickelberg, O. (2001) Endless healing: TGF-β, SMADs, and fibrosis. FEBS Lett. 506, 11-14
22. Keophiphath, M., Achard, V., Henegar, C., Rouault, C., Clément, K., and Lacasa, D. (2009) Macrophage-secreted factors promote a profibrotic phenotype in human preadipocytes. Mol. Endocrinol. 23, 11-24
23. Friedman, S. L. (2010) Evolving challenges in hepatic fibrosis. Nat. Rev. Gastroenterol. Hepatol. 7, 425-436
24. Stockmann, C., Kerdiles, Y., Nomaksteinsky, M., Weidemann, A., Takeda, N., Doedens, A., Torres-Collado, A. X., Iruela-Arispe, L., Nizet, V., and Johnson, R. S. (2010) Loss of myeloid cell-derived vascular endothelial growth factor accelerates fibrosis. Proc. Natl. Acad. Sci. U.S.A. 107, 4329-4334
25. Gealekman, O., Burkart, A., Chouinard, M., Nicoloro, S. M., Straubhaar, J., and Corvera, S. (2008) Enhanced angiogenesis in obesity and in response to PPARγ activators through adipocyte VEGF and ANGPTL4 production. Am. J. Physiol. Endocrinol. Metab. 295, E1056-E1064
26. Arany, Z., Foo, S. Y., Ma, Y., Ruas, J. L., Bommi-Reddy, A., Girnun, G., Cooper, M., Laznik, D., Chinsomboon, J., Rangwala, S. M., Baek, K. H., Rosenzweig, A., and Spiegelman, B. M. (2008) HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1α. Nature 451, 1008-1012 (Pubitemid 351301733)
27. Ndubuizu, O. I., Tsipis, C. P., Li, A., LaManna, J. C. (2010) Hypoxia-inducible factor-1 (HIF-1)-independent microvascular angiogenesis in the aged rat brain. Brain Res. 1366, 101-109
28. Nauck, M., Karakiulakis, G., Perruchoud, A. P., Papakonstantinou, E., Roth, M. (1998) Corticosteroids inhibit the expression of the vascular endothelial growth factor gene in human vascular smooth muscle cells. Eur. J. Pharmacol. 341, 309-315 (Pubitemid 28131129)
29. Leonard, M. O., Godson, C., Brady, H. R., Taylor, C. T. (2005) Potentiation of glucocorticoid activity in hypoxia through induction of the glucocorticoid receptor. J. Immunol. 174, 2250-2257 (Pubitemid 40223972)
30. De Sousa Peixoto, R. A., Turban, S., Battle, J. H., Chapman, K. E., Seckl, J. R., Morton, N. M. (2008) Preadipocyte 11β-hydroxysteroid dehydrogenase type 1 is a keto-reductase and contributes to diet-induced visceral obesity in vivo. Endocrinology 149, 1861-1868 (Pubitemid 351468317)
31. Villaret, A., Galitzky, J., Decaunes, P., Estève, D., Marques, M. A., Sengenès, C., Chiotasso, P., Tchkonia, T., Lafontan, M., Kirkland, J. L., Bouloumié, A. (2010) Adipose tissue endothelial cells from obese human subjects: differences among depots in angiogenic, metabolic, and inflammatory gene expression and cellular senescence. Diabetes 59, 2755-2763
32. Ye, J., Gao, Z., Yin, J., and He, Q. (2007) Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am. J. Physiol. Endocrinol. Metab. 293, E1118-E1128 (Pubitemid 47535846)
33. Kodama, T., Shimizu, N., Yoshikawa, N., Makino, Y., Ouchida, R., Okamoto, K., Hisada, T., Nakamura, H., Morimoto, C., and Tanaka, H. (2003) Role of the glucocorticoid receptor for regulation of hypoxia-dependent gene expression. J. Biol. Chem. 278, 33384-33391 (Pubitemid 37055791)
34. Haddad, J. J., Land, S. C. (2001) A non-hypoxic, ROS-sensitive pathway mediates TNF-α-dependent regulation of HIF-1α. FEBS Lett. 505, 269-274 (Pubitemid 32896679)
35. Jung, Y. J., Isaacs, J. S., Lee, S., Trepel, J., Neckers, L. (2003) IL-1β-mediated up-regulation of HIF-1α via an NFκB/COX-2 pathway identifies HIF-1 as a critical link between inflammation and oncogenesis. FASEB J. 17, 2115-2117
36. Feldser, D., Agani, F., Iyer, N. V., Pak, B., Ferreira, G., and Semenza, G. L (1999) Reciprocal positive regulation of hypoxia-inducible factor 1α and insulin-like growth factor 2. Cancer Res. 59, 3915-3918 (Pubitemid 29393552)
37. Treins, C., Giorgetti-Peraldi, S., Murdaca, J., Semenza, G. L., Van Obberghen, E. (2002) Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J. Biol. Chem. 277, 27975-27981 (Pubitemid 34966746)
38. He, Q., Gao, Z., Yin, J., Zhang, J., Yun, Z., Ye, J. (2011) Regulation of HIF-1α activity in adipose tissue by obesity-associated factors: adipogenesis, insulin, and hypoxia. Am. J. Physiol. Endocrinol. Metab. 300, E877-885