FA1 induces pro-inflammatory and anti-adipogenic pathways/markers in human myotubes established from lean, obese, and type 2 diabetic subjects but not insulin resistance

Frontiers in Endocrinology

Volumn 4, Issue APR, 2013, Pages

  Abdallah, Basem M ^a   Beck Nielsen, Henning ^a   Gaster, Michael ^a  

^a ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Dlk1; FA1; Human myotubes; Insulin resistance; Obesity; Pref 1; Skeletal muscle; Type 2 diabetes

Indexed keywords

ADIPOCYTE PROTEIN 2; CD36 ANTIGEN; FETAL ANTIGEN; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; UNCLASSIFIED DRUG;

ADIPOGENESIS; ADULT; ARTICLE; CELL DIFFERENTIATION; CLINICAL ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOGEN SYNTHESIS; HUMAN; HUMAN CELL; INSULIN RESISTANCE; LIPID METABOLISM; LIPID TRANSPORT; MYOTUBE; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; OXIDATION; REAL TIME POLYMERASE CHAIN REACTION;

EID: 84884182859     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2013.00045     Document Type: Article

References (44)

1. Abdallah, B. M., Bay-Jensen, A. C., Srinivasan, B., Tabassi, N. C., Garnero, P., Delaisse, J. M., et al. (2011a). Estrogen inhibits Dlk1/FA1 production: a potential mechanism for estrogen effects on bone turnover. J. Bone Miner. Res. 26, 2548-2551.
2. Abdallah, B. M., Ditzel, N., Mahmood, A., Isa, A., Traustadottir, G. A., Schilling, A. F., et al. (2011b). DLK1 is a novel regulator of bone mass that mediates estrogen deficiency-induced bone loss in mice. J. Bone Miner. Res. 26, 1457-1471.
3. Abdallah, B. M., Boissy, P., Tan, Q., Dahlgaard, J., Traustadottir, G. A., Kupisiewicz, K., et al. (2007a). dlk1/FA1 regulates the function of human bone marrow mesenchymal stem cells by modulating gene expression of pro-inflammatory cytokines and immune response-related factors. J. Biol. Chem. 282, 7339-7351.
4. Abdallah, B. M., Ding, M., Jensen, C. H., Ditzel, N., Flyvbjerg, A., Jensen, T. G., et al. (2007b). Dlk1/FA1 is a novel endocrine regulator of bone and fat mass and its serum level is modulated by growth hormone. Endocrinology 148, 3111-3121.
5. Abdallah, B. M., Jensen, C. H., Gutierrez, G., Leslie, R. G., Jensen, T. G., and Kassem, M. (2004). Regulation of human skeletal stem cells differentiation by Dlk1/Pref-1. J. Bone Miner. Res. 19, 841-852.
6. Bachmann, E., Krogh, T. N., Hojrup, P., Skjodt, K., and Teisner, B. (1996). Mouse fetal antigen 1 (mFA1), the circulating gene product of mdlk, pref-1 and SCP-1: isolation, characterization and biology. J. Reprod. Fertil. 107, 279-285.
7. Bastard, J. P., Maachi, M., Lagathu, C., Kim, M. J., Caron, M., Vidal, H., et al. (2006). Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur. Cytokine Netw. 17, 4-12.
8. Berends, M. J., Hordijk, R., Scheffer, H., Oosterwijk, J. C., Halley, D. J., and Sorgedrager, N. (1999). Two cases of maternal uniparental disomy 14 with a phenotype overlapping with the Prader-Willi phenotype. Am. J. Med. Genet. 84, 76-79.
9. Cai, D., Yuan, M., Frantz, D. F., Melendez, P. A., Hansen, L., Lee, J., et al. (2005). Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB. Nat. Med. 11, 183-190.
10. Chacon, M. R., Miranda, M., Jensen, C. H., Fernandez-Real, J. M., Vilarrasa, N., Gutierrez, C., et al. (2008). Human serum levels of fetal antigen 1 (FA1/Dlk1) increase with obesity, are negatively associated with insulin sensitivity and modulate inflammation in vitro. Int. J. Obes. (Lond.) 32, 1122-1129.
11. Crameri, R. M., Langberg, H., Magnusson, P., Jensen, C. H., Schroder, H. D., Olesen, J. L., et al. (2004). Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J. Physiol. (Lond.) 558, 333-340.
12. Fleming, R. J. (1998). Structural conservation of Notch receptors and ligands. Semin. Cell Dev. Biol. 9, 599-607.
13. Floridon, C., Jensen, C. H., Thorsen, P., Nielsen, O., Sunde, L., Westergaard, J. G., et al. (2000). Does fetal antigen 1 (FA1) identify cells with regenerative, endocrine and neuroendocrine potentials? A study of FA1 in embryonic, fetal, and placental tissue and in maternal circulation 7. Differentiation 66, 49-59.
14. Frederiksen, C. M., Hojlund, K., Hansen, L., Oakeley, E. J., Hemmings, B., Abdallah, B. M., et al. (2008). Transcriptional profiling of myotubes from patients with type 2 diabetes: no evidence for a primary defect in oxidative phosphorylation genes. Diabetologia. 51, 2068-2077.
15. Freking, B. A., Murphy, S. K., Wylie, A. A., Rhodes, S. J., Keele, J. W., Leymaster, K. A., et al. (2002). Identification of the single base change causing the callipyge muscle hypertrophy phenotype, the only known example of polar overdominance in mammals. Genome Res. 12, 1496-1506.
16. Gaster, M. (2009a). Reduced lipid oxidation in myotubes established from obese and type 2 diabetic subjects. Biochem. Biophys. Res. Commun. 382, 766-770.
17. Gaster, M. (2009b). The dynamic of lipid oxidation in human myotubes. Biochim. Biophys. Acta 1791, 17-24.
18. Gaster, M., and Beck-Nielsen, H. (2004). The reduced insulin-mediated glucose oxidation in skeletal muscle from type 2 diabetic subjects may be of genetic origin-evidence from cultured myotubes. Biochim. Biophys. Acta 1690, 85-91.
19. Gaster, M., and Beck-Nielsen, H. (2006). Triacylglycerol accumulation is not primarily affected in myotubes established from type 2 diabetic subjects. Biochim. Biophys. Acta 1761, 100-110.
20. Gaster, M., Beck-Nielsen, H., and Schroder, H. D. (2001a). Proliferation conditions for human satellite cells. The fractional content of satellite cells. APMIS 109, 726-734.
21. Gaster, M., Kristensen, S. R., Beck-Nielsen, H., and Schroder, H. D. (2001b). A cellular model system of differentiated human myotubes. APMIS 109, 735-744.
22. Gaster, M., Schroder, H. D., Handberg, A., and Beck-Nielsen, H. (2001c). The basal kinetic parameters of glycogen synthase in human myotube cultures are not affected by chronic high insulin exposure. Biochim. Biophys. Acta 1537, 211-221.
23. Gaster, M., Petersen, I., Hojlund, K., Poulsen, P., and Beck-Nielsen, H. (2002). The diabetic phenotype is conserved in myotubes established from diabetic subjects: evidence for primary defects in glucose transport and glycogen synthase activity 4. Diabetes 51, 921-927.
24. Gaster, M., Rustan, A. C., Aas, V., and Beck-Nielsen, H. (2004). Reduced lipid oxidation in skeletal muscle from type 2 diabetic subjects may be of genetic origin: evidence from cultured myotubes. Diabetes 53, 542-548.
25. Harken, J. C., Drivsholm, L., Laursen, I., and Teisner, B. (1999). Elevated serum levels of fetal antigen 1,a member of the epidermal growth factor superfamily, in patients with small cell lung cancer. Tumour Biol. 20, 256-262.
26. Jensen, C. H., Jauho, E. I., Santoni-Rugiu, E., Holmskov, U., Teisner, B., Tygstrup, N., et al. (2004). Transit-amplifying ductular (oval) cells and their hepatocytic progeny are characterized by a novel and distinctive expression of delta-like protein/preadipocyte factor 1/fetal antigen 1. Am. J. Pathol. 164, 1347-1359.
27. Jensen, C. H., Krogh, T. N., Hojrup, P., Clausen, P. P., Skjodt, K., Larsson, L. I., et al. (1994). Protein structure of fetal antigen 1 (FA1). A novel circulating human epidermal-growth-factor-like protein expressed in neuroendocrine tumors and its relation to the gene products of dlk and pG2. Eur. J. Biochem. 225, 83-92.
28. Jensen, C. H., Krogh, T. N., Stoving, R. K., Holmskov, U., and Teisner, B. (1997). Fetal antigen 1 (FA1), a circulating member of the epidermal growth factor (EGF) superfamily: ELISA development, physiology and metabolism in relation to renal function. Clin. Chim. Acta 268, 1-20.
29. Jensen, C. H., Schroder, H. D., Teisner, B., Laursen, I., Brandrup, F., and Rasmussen, H. B. (1999). Fetal antigen 1, a member of the epidermal growth factor superfamily, in neurofibromas and serum from patients with neurofibromatosis type 1. Br. J. Dermatol. 140, 1054-1059.
30. Jensen, C. H., Teisner, B., Hojrup, P., Rasmussen, H. B., Madsen, O. D., Nielsen, B., et al. (1993). Studies on the isolation, structural analysis and tissue localization of fetal antigen 1 and its relation to a human adrenal-specific cDNA, pG2. Hum. Reprod. 8, 635-641.
31. Kalupahana, N. S., Moustaid-Moussa, N., and Claycombe, K. J. (2012). Immunity as a link between obesity and insulin resistance. Mol. Aspects Med. 33, 26-34.
32. Kim, K. S., Kim, J. J., Dekkers, J. C., and Rothschild, M. F. (2004). Polar overdominant inheritance of a DLK1 polymorphism is associated with growth and fatness in pigs. Mamm. Genome 15, 552-559.
33. Laborda, J. (2000). The role of the epidermal growth factor-like protein dlk in cell differentiation 3. Histol. Histopathol. 15, 119-129.
34. Laborda, J., Sausville, E. A., Hoffman, T., and Notario, V. (1993). dlk, a putative mammalian homeotic gene differentially expressed in small cell lung carcinoma and neuroendocrine tumor cell line. J. Biol. Chem. 268, 3817-3820.
35. Lee, K., Villena, J. A., Moon, Y. S., Kim, K. H., Lee, S., Kang, C., et al. (2003). Inhibition of adipogenesis and development of glucose intolerance by soluble preadipocyte factor-1 (Pref-1). J. Clin. Invest. 111, 453-461.
36. Moon, Y. S., Smas, C. M., Lee, K., Villena, J. A., Kim, K. H., Yun, E. J., et al. (2002). Mice lacking paternally expressed Pref-1/Dlk1 display growth retardation and accelerated adiposity. Mol. Cell. Biol. 22, 5585-5592.
37. Ortenblad, N., Mogensen, M., Petersen, I., Hojlund, K., Levin, K., Sahlin, K., et al. (2005). Reduced insulin-mediated citrate synthase activity in cultured skeletal muscle cells from patients with type 2 diabetes: evidence for an intrinsic oxidative enzyme defect. Biochim. Biophys. Acta 1741, 206-214.
38. Plomgaard, P., Bouzakri, K., Krogh-Madsen, R., Mittendorfer, B., Zierath, J. R., and Pedersen, B. K. (2005). Tumor necrosis factor-alpha induces skeletal muscle insulin resistance in healthy human subjects via inhibition of Akt substrate 160 phosphorylation. Diabetes 54, 2939-2945.
39. Sakajiri, S., O'Kelly, J., Yin, D., Miller, C. W., Hofmann, W. K., Oshimi, K., et al. (2005). Dlk1 in normal and abnormal hematopoiesis. Leukemia 19, 1404-1410.
40. Samulewicz, S. J., Seitz, A., Clark, L., and Heber-Katz, E. (2002). Expression of preadipocyte factor-1(Pref-1), a delta-like protein, in healing mouse ears. Wound Repair Regen. 10, 215-221.
41. Smas, C. M., and Sul, H. S. (1993). Pref-1, a protein containing EGF-like repeats, inhibits adipocyte differentiation. Cell 73, 725-734.
42. Villena, J. A., Choi, C. S., Wang, Y., Kim, S., Hwang, Y. J., Kim, Y. B., et al. (2008). Resistance to high-fat diet-induced obesity but exacerbated insulin resistance in mice overexpressing preadipocyte factor-1 (Pref-1): a new model of partial lipodystrophy. Diabetes 57, 3258-3266.
43. Wang, Y., and Sul, H. S. (2006). Ectodomain shedding of preadipocyte factor 1 (Pref-1) by tumor necrosis factor alpha converting enzyme (TACE) and inhibition of adipocyte differentiation. Mol. Cell. Biol. 26, 5421-5435.
44. Yevtodiyenko, A., and Schmidt, J. V. (2006). Dlk1 expression marks developing endothelium and sites of branching morphogenesis in the mouse embryo and placenta. Dev. Dyn. 235, 1115-1123