Induction of STEAP4 correlates with 1,25-dihydroxyvitamin D3 stimulation of adipogenesis in mesenchymal progenitor cells derived from human adipose tissue

Journal of Cellular Physiology

Volumn 228, Issue 10, 2013, Pages 2024-2036

  Narvaez, C J ^a   Simmons, K M ^a   Brunton, J ^b   Salinero, A ^a   Chittur, S V ^a   Welsh, J E ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITRIOL; FATTY ACID BINDING PROTEIN 4; FATTY ACID SYNTHASE; OXIDOREDUCTASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STEAP4 ENZYME; UNCLASSIFIED DRUG;

ADIPOGENESIS; ADULT; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION; GENOME ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; INSULIN RESISTANCE; MESENCHYMAL STROMA CELL; METABOLIC SYNDROME X; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL;

ADIPOGENESIS; ADIPOSE TISSUE; ADULT; ANIMALS; BODY WEIGHT; CELL DIFFERENTIATION; CELLS, CULTURED; FATTY ACID SYNTHETASE COMPLEX, TYPE I; FATTY ACID-BINDING PROTEINS; FEMALE; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; MEMBRANE PROTEINS; MESENCHYMAL STROMAL CELLS; MICE; MICE, KNOCKOUT; MIDDLE AGED; OXIDOREDUCTASES; PPAR GAMMA; STEM CELLS; VITAMIN D;

MUS;

EID: 84879527555     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24371     Document Type: Article

References (49)

1. Atmani H, Chappard D, Basle MF. 2003. Proliferation and differentiation of osteoblasts and adipocytes in rat bone marrow stromal cell cultures: Effects of dexamethasone and calcitriol. J Cell Biochem 89:364-372.
2. Ba K, Yang X, Wu L, Wei X, Fu N, Fu Y, Cai X, Yao Y, Ge Y, Lin Y. 2012. Jagged-1-mediated activation of notch signalling induces adipogenesis of adipose-derived stem cells. Cell Prolif 45:538-544.
3. Bellows CG, Wang YH, Heersche JN, Aubin JE. 1994. 1, 25-dihydroxyvitamin D3 stimulates adipocyte differentiation in cultures of fetal rat calvaria cells: Comparison with the effects of dexamethasone. Endocrinology 134:2221-2229.
4. Blumberg JM, Tzameli I, Astapova I, Lam FS, Flier JS, Hollenberg AN. 2006. Complex role of the vitamin D receptor and its ligand in adipogenesis in 3T3-L1 cells. J Biol Chem 281:11205-11213.
5. Chen X, Zhu C, Ji C, Zhao Y, Zhang C, Chen F, Gao C, Zhu J, Qian L, Guo X. 2010. STEAP4, a gene associated with insulin sensitivity, is regulated by several adipokines in human adipocytes. Int J Mol Med 25:361-367.
6. Cheng S, Massaro JM, Fox CS, Larson MG, Keyes MJ, McCabe EL, Robins SJ, O'Donnell CJ, Hoffmann U, Jacques PF, Booth SL, Vasan RS, Wolf M, Wang TJ. 2010. Adiposity, cardiometabolic risk, and vitamin D status: The Framingham Heart Study. Diabetes 59:242-248.
7. Ching S, Kashinkunti S, Niehaus MD, Zinser GM. 2011. Mammary adipocytes bioactivate 25-hydroxyvitamin D(3) and signal via vitamin D(3) receptor, modulating mammary epithelial cell growth. J Cell Biochem 112:3393-3405.
8. Cianferotti L, Demay MB. 2007. VDR-mediated inhibition of DKK1 and SFRP2 suppresses adipogenic differentiation of murine bone marrow stromal cells. J Cell Biochem 101:80-88.
9. Counter CM, Hahn WC, Wei W, Caddle SD, Beijersbergen RL, Lansdorp PM, Sedivy JM, Weinberg RA. 1998. Dissociation among in vitro telomerase activity, telomere maintenance, and cellular immortalization. Proc Natl Acad Sci USA 95:14723-14728.
10. Cubillos-Rojas M, Amair-Pinedo F, Tato I, Bartrons R, Ventura F, Rosa JL. 2010. Simultaneous electrophoretic analysis of proteins of very high and low molecular mass using Tris-acetate polyacrylamide gels. Electrophoresis 31:1318-1321.
11. Dace A, Martin-el Yazidi C, Bonne J, Planells R, Torresani J. 1997. Calcitriol is a positive effector of adipose differentiation in the OB 17 cell line: Relationship with the adipogenic action of triiodothyronine. Biochem Biophys Res Commun 232:771-776.
12. Elbein SC, Kern PA, Rasouli N, Yao-Borengasser A, Sharma NK, Das SK. 2011. Global gene expression profiles of subcutaneous adipose and muscle from glucose-tolerant, insulin-sensitive, and insulin-resistant individuals matched for BMI. Diabetes 60:1019-1029.
13. Forsythe LK, Livingstone MB, Barnes MS, Horigan G, McSorley EM, Bonham MP, Magee PJ, Hill TR, Lucey AJ, Cashman KD, Kiely M, Strain JJ, Wallace JM. 2012. Effect of adiposity on vitamin D status and the 25-hydroxycholecalciferol response to supplementation in healthy young and older Irish adults. Br J Nutr 107:126-134.
14. Fu M, Sun T, Bookout AL, Downes M, Yu RT, Evans RM, Mangelsdorf DJ. 2005. A Nuclear Receptor Atlas: 3T3-L1 adipogenesis. Mol Endocrinol (Baltimore, Md) 19:2437-2450.
15. Gao D, Trayhurn P, Bing C. 2013. 1, 25-Dihydroxyvitamin D(3) inhibits the cytokine-induced secretion of MCP-1 and reduces monocyte recruitment by human preadipocytes. Int J Obesity 37:357-365.
16. Gimm T, Wiese M, Teschemacher B, Deggerich A, Schodel J, Knaup KX, Hackenbeck T, Hellerbrand C, Amann K, Wiesener MS, Honing S, Eckardt KU, Warnecke C. 2010. Hypoxia-inducible protein 2 is a novel lipid droplet protein and a specific target gene of hypoxia-inducible factor-1. FASEB 24:4443-4458.
17. Gomes IM, Maia CJ, Santos CR. 2012. STEAP proteins: From structure to applications in cancer therapy. Mol Cancer Res 10:573-587.
18. Grunewald TG, Bach H, Cossarizza A, Matsumoto I. 2012. The STEAP protein family: Versatile oxidoreductases and targets for cancer immunotherapy with overlapping and distinct cellular functions. Biol Cell 104:641-657.
19. Guo YY, Li NF, Zhou L, Yao XG, Wang HM, Zhang JH, Luo WL. 2011. A common variation within the STEAP4 gene exons is associated with obesity in Uygur general population. Chin Med J 124:2096-2100.
20. Heaney RP, Horst RL, Cullen DM, Armas LA. 2009. Vitamin D3 distribution and status in the body. J Am Coll Nutr 28:252-256.
21. Imai T, Jiang M, Chambon P, Metzger D. 2001. Impaired adipogenesis and lipolysis in the mouse upon selective ablation of the retinoid X receptor alpha mediated by a tamoxifen-inducible chimeric Cre recombinase (Cre-ERT2) in adipocytes. Proc Natl Acad Sci USA 98:224-228.
22. Klotz B, Mentrup B, Regensburger M, Zeck S, Schneidereit J, Schupp N, Linden C, Merz C, Ebert R, Jakob F. 2012. 1, 25-dihydroxyvitamin D3 treatment delays cellular aging in human mesenchymal stem cells while maintaining their multipotent capacity. PloS ONE 7:e29959.
23. Kong J, Li YC. 2006. Molecular mechanism of 1, 25-dihydroxyvitamin D3 inhibition of adipogenesis in 3T3-L1 cells. Am J Physiol Endocrinol Metab 290:E916-E924.
24. Le TT, Cheng JX. 2009. Single-cell profiling reveals the origin of phenotypic variability in adipogenesis. PloS ONE 4:e5189.
25. Lee H, Bae S, Yoon Y. 2012. Anti-adipogenic effects of 1, 25-dihydroxyvitamin D3 are mediated by the maintenance of the wingless-type MMTV integration site/beta-catenin pathway. Int J Mol Med 30:1219-1224.
26. Li J, Byrne ME, Chang E, Jiang Y, Donkin SS, Buhman KK, Burgess JR, Teegarden D. 2008. 1alpha, 25-Dihydroxyvitamin D hydroxylase in adipocytes. J Steroid Biochem Mol Biol 112:122-126.
27. Lindstad T, Jin Y, Wang L, Qu S, Saatcioglu F. 2010. STAMPs at the crossroads of cancer and nutrition. Nutr Cancer 62:891-895.
28. Lira FS, Rosa JC, Cunha CA, Ribeiro EB, do Nascimento CO, Oyama LM, Mota JF. 2011. Supplementing alpha-tocopherol (vitamin E) and vitamin D3 in high fat diet decrease IL-6 production in murine epididymal adipose tissue and 3T3-L1 adipocytes following LPS stimulation. Lipids Health Dis 10:37.
29. Mahajan A, Stahl CH. 2009. Dihydroxy-cholecalciferol stimulates adipocytic differentiation of porcine mesenchymal stem cells. J Nutr Biochem 20:512-520.
30. Marcotorchino J, Gouranton E, Romier B, Tourniaire F, Astier J, Malezet C, Amiot MJ, Landrier JF. 2012. Vitamin D reduces the inflammatory response and restores glucose uptake in adipocytes. Mol Nutr Food Res 56:1771-1782.
31. Moreno-Navarrete JM, Ortega F, Serrano M, Perez-Perez R, Sabater M, Ricart W, Tinahones F, Peral B, Fernandez-Real JM. 2011. Decreased STAMP2 expression in association with visceral adipose tissue dysfunction. J Clin Endocrinol Metab 96:E1816-E1825.
32. Mostafa NZ, Fitzsimmons R, Major PW, Adesida A, Jomha N, Jiang H, Uludag H. 2012. Osteogenic differentiation of human mesenchymal stem cells cultured with dexamethasone, vitamin D3, basic fibroblast growth factor, and bone morphogenetic protein-2. Connect Tissue Res 53:117-131.
33. Narvaez CJ, Matthews D, Broun E, Chan M, Welsh J. 2009. Lean phenotype and resistance to diet-induced obesity in vitamin D receptor knockout mice correlates with induction of uncoupling protein-1 in white adipose tissue. Endocrinology 150:651-661.
34. Nimitphong H, Holick MF, Fried SK, Lee MJ. 2012. 25-hydroxyvitamin d(3) and 1, 25-dihydroxyvitamin d(3) promote the differentiation of human subcutaneous preadipocytes. PloS ONE 7:e52171.
35. Panda DK, Miao D, Bolivar I, Li J, Huo R, Hendy GN, Goltzman D. 2004. Inactivation of the 25-hydroxyvitamin D 1alpha-hydroxylase and vitamin D receptor demonstrates independent and interdependent effects of calcium and vitamin D on skeletal and mineral homeostasis. J Biol Chem 279:16754-16766.
36. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, Prockop DJ. 2004. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103:1662-1668.
37. Qin DN, Kou CZ, Ni YH, Zhang CM, Zhu JG, Zhu C, Wang YP, Zhu GZ, Shi C, Ji CB, Guo XR. 2010. Monoclonal antibody to the six-transmembrane epithelial antigen of prostate 4 promotes apoptosis and inhibits proliferation and glucose uptake in human adipocytes. Int J Mol Med 26:803-811.
38. Rice T, Chagnon YC, Perusse L, Borecki IB, Ukkola O, Rankinen T, Gagnon J, Leon AS, Skinner JS, Wilmore JH, Bouchard C, Rao DC. 2002. A genomewide linkage scan for abdominal subcutaneous and visceral fat in black and white families: The HERITAGE Family Study. Diabetes 51:848-855.
39. Roth SM, Schrager MA, Metter EJ, Riechman SE, Fleg JL, Hurley BF, Ferrell RE. 2002. IGF2 genotype and obesity in men and women across the adult age span. Int J Obesity Relat Metab Disorders 26:585-587.
40. Ukkola O, Sun G, Bouchard C. 2001. Insulin-like growth factor 2 (IGF2) and IGF-binding protein 1 (IGFBP1) gene variants are associated with overfeeding-induced metabolic changes. Diabetologia 44:2231-2236.
41. Voros G, Sandy JD, Collen D, Lijnen HR. 2006. Expression of aggrecan(ases) during murine preadipocyte differentiation and adipose tissue development. Biochim Biophys acta 1760:1837-1844.
42. Weber K, Erben RG. 2012. Differences in triglyceride and cholesterol metabolism and resistance to obesity in male and female vitamin D receptor knockout mice. J Anim Physiol Anim Nutr. DOI: 10.1111/j-1439-0396.2012.01308.x
43. Welsh J, Zinser LN, Mianecki-Morton L, Martin J, Waltz SE, James H, Zinser GM. 2011. Age-related changes in the epithelial and stromal compartments of the mammary gland in normocalcemic mice lacking the vitamin D3 receptor. PloS ONE 6:e16479.
44. Wong KE, Kong J, Zhang W, Szeto FL, Ye H, Deb DK, Brady MJ, Li YC. 2011. Targeted expression of human vitamin D receptor in adipocytes decreases energy expenditure and induces obesity in mice. J Biol Chem 286:33804-33810.
45. Wong KE, Szeto FL, Zhang W, Ye H, Kong J, Zhang Z, Sun XJ, Li YC. 2009. Involvement of the vitamin D receptor in energy metabolism: Regulation of uncoupling proteins. Am J Physiol Endocrinol Metab 296:E820-E828.
46. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X. 1997. Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science (New York, NY) 275:1129-1132.
47. Zhang CM, Chi X, Wang B, Zhang M, Ni YH, Chen RH, Li XN, Guo XR. 2008. Downregulation of STEAP4, a highly-expressed TNF-alpha-inducible gene in adipose tissue, is associated with obesity in humans. Acta Pharmacol Sin 29:587-592.
48. Zhang S, Chan M, Aubin JE. 2006. Pleiotropic effects of the steroid hormone 1, 25-dihydroxyvitamin D3 on the recruitment of mesenchymal lineage progenitors in fetal rat calvaria cell populations. J Mol Endocrinol 36:425-433.
49. Zhu F, Sweetwyne MT, Hankenson KD. 2013. Pkcdelta is required for jagged-1 induction of hMSC osteogenic differentiation. Stem cells (Dayton, Ohio). doi: 10.1002/stem.1353