Control of adipose tissue expandability in response to high fat diet by the insulin-like growth factor-binding protein-4

Journal of Biological Chemistry

Volumn 289, Issue 26, 2014, Pages 18327-18338

  Gealekman, Olga ^a   Gurav, Kunal ^a   Chouinard, My ^a   Straubhaar, Juerg ^a   Thompson, Michael ^a   Malkani, Samir ^a   Hartigan, Celia ^a   Corvera, Silvia ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; ENDOTHELIAL CELLS; EXPANSION; GENES; INSULIN; MAMMALS; NUTRITION; PROTEINS; TISSUE;

ADIPOSE TISSUE; CDNA MICROARRAYS; EXPANDABILITY; HIGH-FAT DIET; IMMUNOSTAINING; PROLIFERATIVE CELLS; ROSIGLITAZONE; SUBCUTANEOUS ADIPOSE TISSUES;

TISSUE ENGINEERING;

INSULIN; ROSIGLITAZONE; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; THYMOSIN BETA10;

ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE 1 RECEPTOR 1 GENE; ADIPOCYTE; ADIPOSE TISSUE; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASPARTATE BETA HYDROXYLASE GENE; CAPILLARY DENSITY; CONTROLLED STUDY; DNA MICROARRAY; ENDOTHELIUM CELL; FATTY ACID DESATURASE 3 GENE; GENE; HUMAN; HUMAN TISSUE; INSULIN LIKE GROWTH FACTOR BINDING PROTEIN 4 GENE; LIPID DIET; MALE; MOUSE; MTOR BINDING PROTEIN GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHATASE 1B GENE; RAS LIKE FAMILY 12 GENE; SUBCUTANEOUS FAT; THYMOSIN BETA10 GENE; TISSUE GROWTH;

ADIPOCYTE; ANGIOGENESIS; ENDOTHELIAL CELL; INSULIN; INSULIN-LIKE GROWTH FACTOR (IGF); OBESITY; VASCULAR BIOLOGY;

ADIPOSE TISSUE; ANIMALS; CELL PROLIFERATION; DIET, HIGH-FAT; DIETARY FATS; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 4; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; MICE, INBRED C57BL; OBESITY; SIGNAL TRANSDUCTION;

EID: 84903530217     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.545798     Document Type: Article

References (51)

1. Arner, E., Westermark, P. O., Spalding, K. L., Britton, T., Rydén, M., Frisén, J., Bernard, S., and Arner, P. (2010) Adipocyte turnover: relevance to human adipose tissue morphology. Diabetes 59, 105-109
2. Tchoukalova, Y. D., Votruba, S. B., Tchkonia, T., Giorgadze, N., Kirkland, J. L., and Jensen, M. D. (2010) Regional differences in cellular mechanisms of adipose tissue gain with overfeeding. Proc. Natl. Acad. Sci. U. S. A. 107, 18226-18231
3. Bouloumie, A., Lolmede, K., Sengenes, C., Galitzky, J., and Lafontan, M. (2002) Angiogenesis in adipose tissue. Ann. Endocrinol. 63, 91-95
4. Christiaens, V., and Lijnen, H. R. (2010) Angiogenesis and development of adipose tissue. Mol. Cell. Endocrinol. 318, 2-9
5. Hausman, G. J., and Richardson, R. L. (2004) Adipose tissue angiogenesis. J. Anim. Sci. 82, 925-934
6. Han, J., Lee, J. E., Jin, J., Lim, J. S., Oh, N., Kim, K., Chang, S. I., Shibuya, M., Kim, H., and Koh, G. Y. (2011) The spatiotemporal development of adipose tissue. Development 138, 5027-5037
7. Nishimura, S., Manabe, I., Nagasaki, M., Hosoya, Y., Yamashita, H., Fujita, H., Ohsugi, M., Tobe, K., Kadowaki, T., Nagai, R., and Sugiura, S. (2007) Adipogenesis in obesity requires close interplay between differentiating adipocytes, stromal cells, and blood vessels. Diabetes 56, 1517-1526
8. Spencer, M., Unal, R., Zhu, B., Rasouli, N., McGehee, R. E., Jr., Peterson, C. A., and Kern, P. A. (2011) Adipose tissue extracellular matrix and vascular abnormalities in obesity and insulin resistance. J. Clin. Endocrinol. Metab. 96, E1990-E1998
9. Gealekman, O., Guseva, N., Hartigan, C., Apotheker, S., Gorgoglione, M., Gurav, K., Tran, K. V., Straubhaar, J., Nicoloro, S., Czech, M. P., Thompson, M., Perugini, R. A., and Corvera, S. (2011) Depot-specific differences and insufficient subcutaneous adipose tissue angiogenesis in human obesity. Circulation 123, 186-194
10. Pasarica, M., Rood, J., Ravussin, E., Schwarz, J. M., Smith, S. R., and Redman, L. M. (2010) Reduced oxygenation in human obese adipose tissue is associated with impaired insulin suppression of lipolysis. J. Clin. Endocrinol. Metab. 95, 4052-4055
11. Mazzatti, D., Lim, F. L., O'Hara, A., Wood, I. S., and Trayhurn, P. (2012) A microarray analysis of the hypoxia-induced modulation of gene expression in human adipocytes. Arch. Physiol. Biochem. 118, 112-120
12. Sun, K., Wernstedt Asterholm, I., Kusminski, C. M., Bueno, A. C., Wang, Z. V., Pollard, J. W., Brekken, R. A., and Scherer, P. E. (2012) Dichotomous effects of VEGF-A on adipose tissue dysfunction. Proc. Natl. Acad. Sci. U. S. A. 109, 5874-5879
13. Elias, I., Franckhauser, S., Ferré, T., Vilà, L., Tafuro, S., Muñoz, S., Roca, C., Ramos, D., Pujol, A., Riu, E., Ruberte, J., and Bosch, F. (2012) Adipose tissue overexpression of vascular endothelial growth factor protects against diet-induced obesity and insulin resistance. Diabetes 61, 1801-1813
14. Goossens, G. H., Bizzarri, A., Venteclef, N., Essers, Y., Cleutjens, J. P., Konings, E., Jocken, J. W., Cajlakovic, M., Ribitsch, V., Clément, K., and Blaak, E. E. (2011) Increased adipose tissue oxygen tension in obese compared with lean men is accompanied by insulin resistance, impaired adipose tissue capillarization, and inflammation. Circulation 124, 67-76
15. 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. Mol. Cell. Biol. 29, 4467-4483
16. Wellen, K. E., and Hotamisligil, G. S. (2003) Obesity-induced inflammatory changes in adipose tissue. J. Clin. Invest. 112, 1785-1788
17. Xu, H., Barnes, G. T., Yang, Q., Tan, G., Yang, D., Chou, C. J., Sole, J., Nichols, A., Ross, J. S., Tartaglia, L. A., and Chen, H. (2003) Chronic inflammation in fat plays a crucial role in the development of obesityrelated insulin resistance. J. Clin. Invest. 112, 1821-1830
18. Osborn, O., and Olefsky, J. M. (2012) The cellular and signaling networks linking the immune system and metabolism in disease. Nat. Med. 18, 363-374
19. Condeelis, J., and Pollard, J. W. (2006) Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124, 263-266
20. Cho, C. H., Koh, Y. J., Han, J., Sung, H. K., Jong Lee, H., Morisada, T., Schwendener, R. A., Brekken, R. A., Kang, G., Oike, Y., Choi, T. S., Suda, T., Yoo, O. J., and Koh, G. Y. (2007) Angiogenic role of LYVE-1-positive macrophages in adipose tissue. Circ. Res. 100, e47-57
21. Tang, W., Zeve, D., Suh, J. M., Bosnakovski, D., Kyba, M., Hammer, R. E., Tallquist, M. D., and Graff, J. M. (2008) White fat progenitor cells reside in the adipose vasculature. Science 322, 583-586
22. Tran, K. V., Gealekman, O., Frontini, A., Zingaretti, M. C., Morroni, M., Giordano, A., Smorlesi, A., Perugini, J., De Matteis, R., Sbarbati, A., Corvera, S., and Cinti, S. (2012) The vascular endothelium of the adipose tissue gives rise to both white and brown fat cells. Cell Metab. 15, 222-229
23. Tang, W., Zeve, D., Seo, J., Jo, A. Y., and Graff, J. M. (2011) Thiazolidinediones regulate adipose lineage dynamics. Cell Metab. 14, 116-122
24. Rojas-Rodriguez, R., Gealekman, O., Kruse, M. E., Rosenthal, B., Rao, K., Min, S., Bellve, K. D., Lifshitz, L. M., and Corvera, S. (2014) Adipose tissue angiogenesis assay. Methods Enzymol. 537, 75-91
25. Smyth, G. K. (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3
26. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B 57, 289-300
27. Jo, J., Guo, J., Liu, T., Mullen, S., Hall, K. D., Cushman, S. W., and Periwal, V. (2010) Hypertrophy-driven adipocyte death overwhelms recruitment under prolonged weight gain. Biophys. J. 99, 3535-3544
28. Alkhouri, N., Gornicka, A., Berk, M. P., Thapaliya, S., Dixon, L. J., Kashyap, S., Schauer, P. R., and Feldstein, A. E. (2010) Adipocyte apoptosis, a link between obesity, insulin resistance, and hepatic steatosis. J. Biol. Chem. 285, 3428-3438
29. Murano, I., Barbatelli, G., Parisani, V., Latini, C., Muzzonigro, G., Castellucci, M., and Cinti, S. (2008) Dead adipocytes, detected as crown-like structures, are prevalent in visceral fat depots of genetically obese mice. J. Lipid Res. 49, 1562-1568
30. Prieur, X., Mok, C. Y., Velagapudi, V. R., Núñez, V., Fuentes, L., Montaner, D., Ishikawa, K., Camacho, A., Barbarroja, N., O'Rahilly, S., Sethi, J. K., Dopazo, J., Orešic., M., Ricote, M., and Vidal-Puig, A. (2011) Differential lipid partitioning between adipocytes and tissue macrophages modulates macrophage lipotoxicity and M2/M1 polarization in obese mice. Diabetes 60, 797-809
31. Winzell, M. S., and Ahrén, B. (2004) The high-fat diet fed mouse. Diabetes 53, S215-S219
32. Maddox, D. E., Shibata, S., and Goldstein, I. J. (1982) Stimulated macrophages express a new glycoprotein receptor reactive with Griffonia simplicifolia I-B4 isolectin. Proc. Natl. Acad. Sci. U. S. A. 79, 166-170
33. Dalmas, E., Clément, K., and Guerre-Millo, M. (2011) Defining macrophage phenotype and function in adipose tissue. Trends Immunol. 32, 307-314
34. 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
35. 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. 32, 451-463
36. Ryan, A. J., Napoletano, S., Fitzpatrick, P. A., Currid, C. A., O'Sullivan, N. C., and Harmey, J. H. (2009) Expression of a protease-resistant insulinlike growth factor-binding protein-4 inhibits tumour growth in a murine model of breast cancer. Br. J. Cancer 101, 278-286
37. Jehle, P. M., Jehle, D. R., Mohan, S., and Böhm, B. O. (1998) Serum levels of insulin-like growth factor system components and relationship to bone metabolism in type 1 and type 2 diabetes mellitus patients. J. Endocrinol. 159, 297-306
38. Zhang, X., Lam, K. S., Ye, H., Chung, S. K., Zhou, M., Wang, Y., and Xu, A. (2010) Adipose tissue-specific inhibition of hypoxia-inducible factor 1α induces obesity and glucose intolerance by impeding energy expenditure in mice. J. Biol. Chem. 285, 32869-32877
39. Leibovich, S. J., Polverini, P. J., Shepard, H. M., Wiseman, D. M., Shively, V., and Nuseir, N. (1987) Macrophage-induced angiogenesis is mediated by tumour necrosis factor-α. Nature 329, 630-632
40. Clemmons, D. R. (2012) Metabolic actions of insulin-like growth factor-I in normal physiology and diabetes. Endocrinol. Metab. Clin. North Am. 41, 425-443
41. Scheiwiller, E., Guler, H. P., Merryweather, J., Scandella, C., Maerki, W., Zapf, J., and Froesch, E. R. (1986) Growth restoration of insulin-deficient diabetic rats by recombinant human insulin-like growth factor I. Nature 323, 169-171
42. Russell-Jones, D. L., Rattray, M., Wilson, V. J., Jones, R. H., Sönksen, P. H., and Thomas, C. R. (1992) Intraperitoneal insulin is more potent than subcutaneous insulin at restoring hepatic insulin-like growth factor-I mRNA levels in the diabetic rat: a functional role for the portal vascular link. J. Mol. Endocrinol. 9, 257-263
43. Alarid, E. T., Schlechter, N. L., Russell, S. M., and Nicoll, C. S. (1992) Evidence suggesting that insulin-like growth factor-I is necessary for the trophic effects of insulin on cartilage growth in vivo. Endocrinology 130, 2305-2309
44. Phillips, L. S., Goldstein, S., and Pao, C. I. (1991) Nutrition and somatomedin. XXVI. Molecular regulation of IGF-I by insulin in cultured rat hepatocytes. Diabetes 40, 1525-1530
45. Gousseva, N., Kugathasan, K., Chesterman, C. N., and Khachigian, L. M. (2001) Early growth response factor-1 mediates insulin-inducible vascular endothelial cell proliferation and regrowth after injury. J. Cell. Biochem. 81, 523-534
46. Lassance, L., Miedl, H., Absenger, M., Diaz-Perez, F., Lang, U., Desoye, G., and Hiden, U. (2013) Hyperinsulinemia stimulates angiogenesis of human fetoplacental endothelial cells: a possible role of insulin in placental hypervascularization in diabetes mellitus. J. Clin. Endocrinol. Metab. 98, E1438-E1447
47. Qiao, J. G., Wu, L., Lei, D. X., and Wang, L. (2005) Insulin promotes sinusoidal endothelial cell proliferation mediated by upregulation of vascular endothelial growth factor in regenerating rat liver after partial hepatectomy. World J. Gastroenterol. 11, 5978-5983
48. Carnesecchi, S., Carpentier, J. L., Foti, M., and Szanto, I. (2006) Insulininduced vascular endothelial growth factor expression is mediated by the NADPH oxidase NOX3. Exp. Cell Res. 312, 3413-3424
49. Tchoukalova, Y. D., Nathanielsz, P. W., Conover, C. A., Smith, S. R., and Ravussin, E. (2009) Regional variation in adipogenesis and IGF regulatory proteins in the fetal baboon. Biochem. Biophys. Res. Commun. 380, 679-683
50. Owen, C., Czopek, A., Agouni, A., Grant, L., Judson, R., Lees, E. K., Mcilroy, G. D., Göransson, O., Welch, A., Bence, K. K., Kahn, B. B., Neel, B. G., Mody, N., and Delibegovič, M. (2012) Adipocyte-specific protein tyrosine phosphatase 1B deletion increases lipogenesis, adipocyte cell size and is a minor regulator of glucose homeostasis. PLoS One 7, e32700
51. Kim, F., Pham, M., Maloney, E., Rizzo, N. O., Morton, G. J., Wisse, B. E., Kirk, E. A., Chait, A., and Schwartz, M. W. (2008) Vascular inflammation, insulin resistance, and reduced nitric oxide production precede the onset of peripheral insulin resistance. Arterioscler. Thromb. Vasc. Biol. 28, 1982-1988