Bone morphogenetic protein-7 (BMP-7) augments insulin sensitivity in mice with type II diabetes mellitus by potentiating PI3K/AKT pathway

BioFactors

Volumn 43, Issue 2, 2017, Pages 195-209

  Chattopadhyay, Tandrika ^a,c   Singh, Rajiv Ranjan ^a   Gupta, Sarika ^a   Surolia, Avadhesha ^a,b  

^a NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

^b INDIAN INSTITUTE OF SCIENCE   (India)

^c TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

adipose tissue; bone morphogenetic protein; diabetes; glucose homeostasis; insulin

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; GLUCOSE; INSULIN; OSTEOGENIC PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; BMP4 PROTEIN, MOUSE; GLUCOSE TRANSPORTER 4; ONCOPROTEIN; PROTEIN SERINE THREONINE KINASE; PYRUVATE DEHYDROGENASE (ACETYL-TRANSFERRING) KINASE; SLC2A4 PROTEIN, MOUSE;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY FAT; CELL MEMBRANE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORT; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; METABOLIC PARAMETERS; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; BLOOD; GENETICS; HUMAN; METABOLISM; NONOBESE DIABETIC MOUSE; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 7; DIABETES MELLITUS, TYPE 2; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; HUMANS; INSULIN; INSULIN RESISTANCE; MICE; MICE, INBRED NOD; ONCOGENE PROTEIN V-AKT; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 85012071197     PISSN: 09516433     EISSN: 18728081     Source Type: Journal    
DOI: 10.1002/biof.1334     Document Type: Article

References (45)

1. Kahn, B. B., and Flier, J. S. (2000) Obesity and insulin resistance. J. Clin. Invest. 4, 473–481.
2. Odegaard, J. I., and Chawla, A. (2013) Pleiotropic actions of insulin resistance and inflammation in metabolic homeostasis. Science 339, 172–177.
3. Stumvoll, M., Goldstein, B. J., and van Haeften, T. W. (2005) Type 2 diabetes: principles of pathogenesis and therapy. Lancet 365, 1333–1346.
4. Kahn, C. R. (1994) Banting Lecture. Insulin action, diabetogenes, and the cause of type II diabetes. Diabetes 43, 1066–1084.
5. Zimmet, P., Alberti, K. G., and Shaw, J. (2001) Global and societal implications of the diabetes epidemic. Nature 414, 782–787.
6. Kim, J. K., Kim, Y. J., Fillmore, J. J., Chen, Y., Moore, I., et al. (2001) Prevention of fat-induced insulin resistance by salicylate. J. Clin. Invest. 108, 437–446.
7. Samuel, V. T., Petersen, K. F., and Shulman, G. I. (2010) Lipid-induced insulin resistance: unraveling the mechanism. Lancet 375, 2267–2277.
8. Gesta, S., Tseng, Y. H., and Kahn, C. R. (2007) Developmental origin of fat: tracking obesity to its source. Cell 131, 242–256.
9. Odegaard, J. I., Ganeshan, K., and Chawla, A. (2013) Adipose tissue macrophages: amicus adipem? Cell Metab. 18, 767–768.
10. Hotamisligil, G. S., Shargill, N. S., and Spiegelman, B. M. (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259, 87–91.
11. Olefsky, J. M., and Glass, C. K. (2010) Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 72, 219–246.
12. Shi, Y., and Massague, J. (2003) Mechanisms of TGF-beta signalling from cell membrane to the nucleus. Cell 113, 685–700.
13. Chen, D., Zhao, M., and Mundy, G. R. (2004) Bone morphogenetic proteins. Growth Factors 22, 233–241.
14. Hogan, B. L. (1996) Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580–1594.
15. Massague, J., and Chen, Y. G. (2000) Controlling TGF-beta signalling. Genes Dev. 14, 627–644.
16. Miyazono, K., Kamiya, Y., and Morikawa, M. (2010) Bone morphogenetic protein receptors and signal transduction. J. Biochem. 147, 35–51.
17. Schulz, T. J., and Tseng, Y. H. (2009) Emerging role of bone morphogenetic proteins in adipogenesis and energy metabolism. Cytokine Growth Factor Rev. 20, 523–531.
18. Martínez, V. G., Hernández-López, C., Valencia, J., Hidalgo, L., Entrena, A., et al. (2011) The canonical BMP signalling pathway is involved in human monocyte-derived dendritic cell maturation. Immunol. Cell Biol. 89, 610–618.
19. Bowers, R. R., and Lane, M. D. (2007) A role for bone morphogenetic protein-4 in adipocyte development. Cell Cycle 15, 385–389.
20. Hua, H., Zhang, Y. Q., Dabernat, S., Kritzik, M., Dietz, D., et al. (2006) BMP4 regulates pancreatic progenitor cell expansion through ID2. J. Biol. Chem. 281, 13574–13580.
21. Tseng, Y. H., Kokkotou, E., Schulz, T. J., Huang, T. L., Winnay, J. N., et al. (2008) New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454, 1000–1004.
22. Urbina, P., and Singla, D. K. (2014) BMP-7 attenuates adverse cardiac remodeling mediated through M2 macrophages in prediabetic cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol. 307, H762–H772.
23. Klein, D., Álvarez-Cubela, S., Lanzoni, G., Vargas, N., Prabakar, K. R., et al. (2015) The authors showed that BMP-7 induces pancreatic exocrine-to-endocrine tissue conversion in human adult tissue. Diabetes 64, 4123–4134.
24. Lowell, B. B., and Spiegelman, B. M. (2000) Towards a molecular understanding of adaptive thermogenesis. Nature 404, 652–660.
25. Zhang, H., Schulz, T. J., Espinoza, D. O., Huang, T. L., Emanuelli, B., et al. (2010) Cross talk between insulin and bone morphogenetic protein signalling systems in brown adipogenesis. Mol. Cell Biol. 17, 4224–4233.
26. White, M. F., and Kahn, C. R. (1994) The insulin signalling system. J. Biol. Chem. 269, 1–4.
27. Jessen, N., Pold, R., Buhl, E. S., Jensen, L. S., Schmitz, O., et al. (2003) Effects of AICAR and exercise on insulin-stimulated glucose uptake, signalling, and GLUT-4 content in rat muscles. J. Appl. Physiol. 94, 1373–1379.
28. Zhang, W., Patil, S., Chauhan, B., Guo, S., Powell, D. R., et al. (2006) FoxO1 regulates multiple metabolic pathways in the liver: effects on gluconeogenic, glycolytic, and lipogenic gene expression. J. Biol. Chem. 14, 281–296.
29. Schmitz-Peiffer, C., Browne, C. L., Oakes, N. D., Watkinson, A., Chisholm, D. J., et al. (1997) Alterations in the expression and cellular localization of protein kinase C isozymes epsilon and theta are associated with insulin resistance in skeletal muscle of the high-fat-fed rat. Diabetes 46, 169–178.
30. Li, Y., Soos, T. J., Li, X., Wu, J., Degennaro, M., et al. (2004) Protein kinase C θ inhibits insulin signalling by phosphorylating IRS1 at Ser-1101. J. Biol. Chem. 279, 45304–45307.
31. DeFea, K., and Roth, R. A. (1997) Protein kinase C modulation of insulin receptor substrate-1 tyrosine phosphorylation requires serine 612. Biochemistry 36, 12939–12947.
32. Zick, Y. (2005) Ser/Thr phosphorylation of IRS proteins: a molecular basis for insulin resistance. Sci. STKE 268, pe4.
33. Schulz, T. J., Huang, P., Huang, T. L., Xue, R., McDougall, L. E., et al. (2013) Brown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat. Nature 49, 379–383.
34. Schwartz, M. W., and Kahn, S. E. (1999) Insulin resistance and obesity. Nature 402, 860–861.
35. Thomson, M. J., Williams, M. G., and Frost, S. C. (1997) Development of insulin resistance in 3T3-L1 adipocytes. J. Biol. Chem. 272, 7759–7764.
36. Lee, J. O., Lee, S. K., Kim, J. H., et al. (2012) Metformin regulates glucose transporter 4 (GLUT4) translocation through AMP-activated protein kinase (AMPK)-mediated Cbl/CAP signaling in 3T3-L1 preadipocyte cells. J. Biol. Chem. 287, 441219-9.
37. Abel, E. D., Peroni, O., Kim, J. K., et al. (2001) Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature 409, 729–733.
38. Lumeng, C. N., Deyoung, S. M., and Saltiel, A. R. (2007) Macrophages block insulin action in adipocytes by altering expression of signalling and glucose transport proteins. Am. J. Physiol. Endocrinol. Metab. 292, E166–E174.
39. Maeno, Y., Li, Q., Park, K., et al. (2012) Inhibition of insulin signalling in endothelial cells by protein kinase C-induced phosphorylation of p85 subunit of phosphatidylinositol 3-kinase (PI3K). J. Biol. Chem. 287, 4518–4530.
40. Kubota, T., Kubota, N., Kumagai, H., et al. (2011) Impaired insulin signalling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. Cell Metab. 13, 294–307.
41. Cai, D., Yuan, M., Frantz, D. F., et al. (2005) Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat. Med. 11, 183–190.
42. Goulley, J., Dahl, U., Baeza, N., Mishina, Y., and Edlund, H. (2007) BMP4-BMPR1A signaling in b cells is required for and augments glucose-stimulated insulin secretion. Cell Metab. 5, 207–219.
43. Boon, M. R., van den Berg, S. A., Wang, Y., van den Bossche, J., Karkampouna, S., et al. (2013) BMP7 activates brown adipose tissue and reduces diet-induced obesity only at subthermoneutrality. PLoS One 8, e74083.
44. Stein, S. A., Lamos, E. M., and Davis, S. N. (2012) A review of the efficacy and safety of oral antidiabetic drugs. Expert Opin. Drug Saf. 12, 153–75.
45. Lu, M., Sarruf, D. A., Talukdar, S., et al. (2011) Brain PPAR-γ promotes obesity and is required for the insulin-sensitizing effect of thiazolidinediones. Nat. Med. 17, 618–622.