DLK1/PREF1 regulates nutrient metabolism and protects from steatosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 45, 2014, Pages 16088-16093

  Charalambous, Marika ^a,b   Da Rocha, Simao Teixeira ^a,c   Radford, Elizabeth Jane ^a   Medina Gomez, Gema ^a,d   Curran, Scott ^a,e   Pinnock, Scarlett B ^a   Ferrón, Sacri R ^a,f   Vidal Puig, Antonio ^a   Ferguson Smith, Anne C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c INSTITUT CURIE   (France)

^d UNIVERSIDAD REY JUAN CARLOS   (Spain)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Adipose tissue; Delta like homologue 1; Genomic imprinting; Growth hormone; Hepatosteatosis

Indexed keywords

GROWTH HORMONE; SOMATOMEDIN C; DLK1 PROTEIN, MOUSE; INSULIN-LIKE GROWTH FACTOR-1, MOUSE; SIGNAL PEPTIDE;

ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DELTA LIKE HOMOLOG 1 GENE; ENERGY EXPENDITURE; FATTY LIVER; GENE; GENE CONTROL; GENE FUNCTION; GENE OVEREXPRESSION; GLUCOSE TOLERANCE; HORMONE RELEASE; INSULIN SENSITIVITY; LIPID DIET; LIPID OXIDATION; LIPID STORAGE; LIPOGENESIS; LIVER PROTECTION; METABOLIC STRESS; MOUSE; NONHUMAN; SPATIOTEMPORAL ANALYSIS; STEATOSIS; TISSUE EXPANSION; TRANSGENE; WHITE ADIPOSE TISSUE; ANIMAL; EMBRYO DEVELOPMENT; FEMALE; GENETICS; LIPID METABOLISM; METABOLISM; PATHOLOGY; PREGNANCY; TRANSGENIC MOUSE;

ANIMALS; EMBRYONIC DEVELOPMENT; FATTY LIVER; FEMALE; INSULIN-LIKE GROWTH FACTOR I; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPID METABOLISM; MICE; MICE, TRANSGENIC; PREGNANCY;

EID: 84909619346     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1406119111     Document Type: Article

References (48)

1. Postic C, Girard J (2008) The role of the lipogenic pathway in the development of hepatic steatosis. Diabetes Metab 34(6 Pt 2):643-648.
2. Møller N, Jørgensen JO (2009) Effects of growth hormone on glucose, lipid, and protein metabolism in human subjects. Endocr Rev 30(2):152-177.
3. Fan Y, et al. (2009) Liver-specific deletion of the growth hormone receptor reveals essential role of growth hormone signaling in hepatic lipid metabolism. J Biol Chem 284(30):19937-19944.
4. Barclay JL, et al. (2011) GH-dependent STAT5 signaling plays an important role in hepatic lipid metabolism. Endocrinology 152(1):181-192.
5. Sos BC, et al. (2011) Abrogation of growth hormone secretion rescues fatty liver in mice with hepatocyte-specific deletion of JAK2. J Clin Invest 121(4):1412-1423, and erratum (2011) 121:3360.
6. Wang Z, Masternak MM, Al-Regaiey KA, Bartke A (2007) Adipocytokines and the regulation of lipid metabolism in growth hormone transgenic and calorie-restricted mice. Endocrinology 148(6):2845-2853.
7. Takada S, et al. (2000) Delta-like and gtl2 are reciprocally expressed, differentially methylated linked imprinted genes on mouse chromosome 12. Curr Biol 10(18):1135-1138.
8. Schmidt JV, Matteson PG, Jones BK, Guan XJ, Tilghman SM (2000) The Dlk1 and Gtl2 genes are linked and reciprocally imprinted. Genes Dev 14(16):1997-2002.
9. Laborda J, Sausville EA, Hoffman T, 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(6):3817-3820.
10. Jensen CH, 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(4):635-641.
11. Smas CM, Sul HS (1993) Pref-1, a protein containing EGF-like repeats, inhibits adipocyte differentiation. Cell 73(4):725-734.
12. Smas CM, Chen L, Sul HS (1997) Cleavage of membrane-associated pref-1 generates a soluble inhibitor of adipocyte differentiation. Mol Cell Biol 17(2):977-988.
13. Lee K, et al. (2003) Inhibition of adipogenesis and development of glucose intolerance by soluble preadipocyte factor-1(Pref-1). J Clin Invest 111(4):453-461.
14. Villena JA, 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(12):3258-3266.
15. Garcés C, Ruiz-Hidalgo MJ, Bonvini E, Goldstein J, Laborda J (1999) Adipocyte differentiation is modulated by secreted delta-like (dlk) variants and requires the expression of membrane-associated dlk. Differentiation 64(2):103-114.
16. Ferrón SR, et al. (2011) Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature 475(7356):381-385.
17. Mortensen SB, et al. (2012) Membrane-tethered delta-like 1 homolog (DLK1) restricts adipose tissue size by inhibiting preadipocyte proliferation. Diabetes 61(11):2814-2822.
18. da Rocha ST, et al. (2009) Gene dosage effects of the imprinted delta-like homologue 1 (dlk1/pref1) in development: Implications for the evolution of imprinting. PLoS Genet 5(2):e1000392.
19. da Rocha ST, et al. (2007) Restricted co-expression of Dlk1 and the reciprocally imprinted non-coding RNA, Gtl2: Implications for cis-acting control. Dev Biol 306(2):810-823.
20. Bachmann E, Krogh TN, Højrup P, Skjø dt K, 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(2):279-285.
21. Charalambous M, et al. (2012) Imprinted gene dosage is critical for the transition to independent life. Cell Metab 15(2):209-221.
22. Vijayakumar A, et al. (2012) Skeletal muscle growth hormone receptor signaling regulates basal, but not fasting-induced, lipid oxidation. PLoS ONE 7(9):e44777.
23. Halder SK, et al. (1998) Cloning of a membrane-spanning protein with epidermal growth factor-like repeat motifs from adrenal glomerulosa cells. Endocrinology 139(7):3316-3328.
24. Larsen JB, et al. (1996) Fetal antigen 1 and growth hormone in pituitary somatotroph cells. Lancet 347(8995):191.
25. Jensen CH, et al. (2001) Neurons in the monoaminergic nuclei of the rat and human central nervous system express FA1/dlk. Neuroreport 12(18):3959-3963.
26. Andersen DC, Jensen L, Schrø der HD, Jensen CH (2009) "The preadipocyte factor" DLK1 marks adult mouse adipose tissue residing vascular cells that lack in vitro adipogenic differentiation potential. FEBS Lett 583(17):2947-2953.
27. Andersen DC, etal. (2009) Characterization of DLK1 +cells emerging during skeletal muscle remodeling in response to myositis, myopathies, and acute injury. Stem Cells 27(4):898-908.
28. Floridon C, 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. Differentiation 66(1):49-59.
29. Medina-Gomez G, et al. (2007) PPAR gamma 2 prevents lipotoxicity by controlling adipose tissue expandability and peripheral lipid metabolism. PLoS Genet 3(4):e64.
30. Kakuma T, et al. (2000) Leptin, troglitazone, and the expression of sterol regulatory element binding proteins in liver and pancreatic islets. Proc Natl Acad Sci USA 97(15):8536-8541.
31. Yahagi N, et al. (2002) Absence of sterol regulatory element-binding protein-1(SREBP-1) ameliorates fatty livers but not obesity or insulin resistance in Lep (ob)/Lep (ob) mice. J Biol Chem 277(22):19353-19357.
32. Jeong JY, Jeoung NH, Park KG, Lee IK (2012) Transcriptional regulation of pyruvate dehydrogenase kinase. Diabetes Metab J 36(5):328-335.
33. Jing K, et al. (2009) Expression regulation and function of Pref-1 during adipogenesis of human mesenchymal stem cells (MSCs). Biochim Biophys Acta 1791(8):816-826.
34. Yamashita S, Melmed S (1987) Insulinlike growth factor I regulation of growth hormone gene transcription in primary rat pituitary cells. J Clin Invest 79(2):449-452.
35. Romero CJ, et al. (2010) Targeted deletion of somatotroph insulin-like growth factor-I signaling in a cell-specific knockout mouse model. Mol Endocrinol 24(5):1077-1089.
36. Romero CJ, et al. (2012) Insulin-like growth factor 1 mediates negative feedback to somatotroph GH expression via POU1F1/CREB binding protein interactions. Mol Cell Biol 32(21):4258-4269.
37. Castillo AI, Aranda A (1997) Differential regulation of pituitary-specific gene expression by insulin-like growth factor 1 in rat pituitary GH4C1 and GH3 cells. Endocrinology 138(12):5442-5451.
38. Puertas-Avendaño RA, et al. (2011) Role of the non-canonical notch ligand deltalike protein 1 in hormone-producing cells of the adult male mouse pituitary. J Neuroendocrinol 23(9):849-859.
39. Appelbe OK, Yevtodiyenko A, Muniz-Talavera H, Schmidt JV (2013) Conditional deletions refine the embryonic requirement for Dlk1. Mech Dev 130(2-3):143-159.
40. Cheung LY, Rizzoti K, Lovell-Badge R, LeTissier PR (2013) Pituitary phenotypes of mice lacking the notch signalling ligand delta-like 1 homologue. JNeuroendocrinol 25(4):391-401.
41. Ansell PJ, et al. (2007) Regulation of growth hormone expression by Delta-like protein 1(Dlk1). Mol Cell Endocrinol 271(1-2):55-63.
42. Carlsson C, et al. (1997) Growth hormone and prolactin stimulate the expression of rat preadipocyte factor-1/delta-like protein in pancreatic islets: Molecular cloning and expression pattern during development and growth of the endocrine pancreas. Endocrinology 138(9):3940-3948.
43. Wolfrum C, et al. (2003) Role of Foxa-2 in adipocyte metabolism and differentiation. J Clin Invest 112(3):345-356.
44. Abdallah BM, et al. (2007) Dlk1/FA1 is a novel endocrine regulator of bone and fat mass and its serum level is modulated by growth hormone. Endocrinology 148(7):3111-3121.
45. List EO, et al. (2011) Endocrine parameters and phenotypes of the growth hormone receptor gene disrupted (GHR-/-) mouse. Endocr Rev 32(3):356-386.
46. List EO, et al. (2013) The role of GH in adipose tissue: Lessons from adipose-specific GH receptor gene-disrupted mice. Mol Endocrinol 27(3):524-535.
47. Herrera E, Amusquivar E (2000) Lipid metabolism in the fetus and the newborn. Diabetes Metab Res Rev 16(3):202-210.
48. Medina-Gomez G, et al. (2005) The link between nutritional status and insulin sensitivity is dependent on the adipocyte-specific peroxisome proliferator-activated receptor-gamma2 isoform. Diabetes 54(6):1706-1716.