Optimizing adipogenic transdifferentiation of bovine mesenchymal stem cells: a prominent role of ascorbic acid in FABP4 induction

References

• Roeder I, Lorenz R. Asymmetry of stem cell fate and the potential impact of the niche. Stem Cell Rev. 2006;2:171–180.
   PubMedGoogle Scholar
• Cignarelli A, Perrini S, Nigro P, et al. Long-acting insulin analog detemir displays reduced effects on adipocyte differentiation of human subcutaneous and visceral adipose stem cells. Nutr Metab Cardiovasc Dis. 2016;26:333–344.
   PubMed Web of Science ®Google Scholar
• Priya N, Sarcar S, Majumdar AS, et al. Explant culture: a simple, reproducible, efficient and economic technique for isolation of mesenchymal stromal cells from human adipose tissue and lipoaspirate. J Tissue Eng Regen Med. 2014;8:706–716.
   PubMed Web of Science ®Google Scholar
• Albrecht E, Kuzinski J, Komolka K, et al. Localization and abundance of early markers of fat cell differentiation in the skeletal muscle of cattle during growth—Are DLK1-positive cells the origin of marbling flecks? Meat Sci. 2015;100:237–245.
   PubMed Web of Science ®Google Scholar
• Baglioni S, Cantini G, Poli G, et al. Functional differences in visceral and subcutaneous fat pads originate from differences in the adipose stem cell. PLoS One. 2012;7:e36569.
   PubMed Web of Science ®Google Scholar
• Jeong JY, Park MN, Cho ES, et al. Epigallocatechin-3-gallate-induced free-radical production upon adipogenic differentiation in bovine bone-marrow mesenchymal stem cells. Cell Tissue Res. 2015;362:87–96.
   PubMed Web of Science ®Google Scholar
• Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell. 2002;13:4279–4295.
   PubMed Web of Science ®Google Scholar
• Sampaio RV, Chiaratti MR, Santos DCN, et al. Generation of bovine (Bos indicus) and buffalo (Bubalus bubalis) adipose tissue derived stem cells: isolation, characterization, and multipotentiality. Genet Mol Res. 2015;14:53–62.
   PubMed Web of Science ®Google Scholar
• Barry FP, Boynton RE, Haynesworth S, et al. The monoclonal antibody SH-2, raised against human mesenchymal stem cells, recognizes an epitope on endoglin (CD105). Biochem Biophys Res Commun. 1999;265:134–139.
   PubMed Web of Science ®Google Scholar
• Barry F, Boynton R, Murphy M, et al. The SH-3 and SH-4 antibodies recognize distinct epitopes on CD73 from human mesenchymal stem cells. Biochem Biophys Res Commun. 2001;289:519–524.
   PubMed Web of Science ®Google Scholar
• Ong WK, Tan CS, Chan KL, et al. Identification of specific cell-surface markers of adipose-derived stem cells from subcutaneous and visceral fat depots. Stem Cell Reports. 2014;2:171–179.
   PubMed Web of Science ®Google Scholar
• Eckle T, Füllbier L, Wehrmann M, et al. Identification of ectonucleotidases CD39 and CD73 in innate protection during acute lung injury. J Immunol. 2007;178:8127–8137.
   PubMed Web of Science ®Google Scholar
• Haeryfar SM, Hoskin DW. Thy-1: more than a mouse pan-T cell marker. J Immunol. 2004;173:3581–3588.
   PubMed Web of Science ®Google Scholar
• Farahani RM, Xaymardan M. Platelet-derived growth factor receptor alpha as a marker of mesenchymal stem cells in development and stem cell biology. Stem Cells Int. 2015;2015:362753.
   PubMed Web of Science ®Google Scholar
• Vieira NM, Brandalise V, Zucconi E, et al. Isolation, characterization, and differentiation potential of canine adipose-derived stem cells. Cell Transplant. 2010;19:279–289.
   PubMed Web of Science ®Google Scholar
• Chamberlain G, Fox J, Ashton B, et al. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007;25:2739–2749.
   PubMed Web of Science ®Google Scholar
• Weiser B, Sommer F, Neubauer M, et al. Ascorbic acid enhances adipogenesis of bone marrow-derived mesenchymal stromal cells. Cells Tissues Organs. 2009;189:373–381.
   PubMed Web of Science ®Google Scholar
• Grant AC, Ortiz-Colon G, Doumit ME, et al. Optimization of in vitro conditions for bovine subcutaneous and intramuscular preadipocyte differentiation. J Anim Sci. 2008;86:73–82.
   PubMed Web of Science ®Google Scholar
• Vernon RG. Lipid metabolism in the adipose tissue of ruminant animals. Prog Lipid Res. 1980;19:23–106.
   PubMedGoogle Scholar
• Sandhu MA, Jurek S, Trappe S, et al. Influence of bovine serum lipids and fetal bovine serum on the expression of cell surface markers in cultured bovine preadipocytes. Cells Tissues Organs. 2017;204:13–24.
   PubMed Web of Science ®Google Scholar
• Greenspan P, Mayer EP, Fowler SD. Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol. 1985;100:965–973.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25:402–408.
   PubMed Web of Science ®Google Scholar
• Riedel J, Badewien‐Rentzsch B, Kohn B, et al. Characterization of key genes of the renin–angiotensin system in mature feline adipocytes and during in vitro adipogenesis. J Anim Physiol Anim Nutr. 2016;100:1139–1148.
   PubMed Web of Science ®Google Scholar
• Petersen RK, Madsen L, Pedersen LM, et al. Cyclic AMP (cAMP)-mediated stimulation of adipocyte differentiation requires the synergistic action of Epac-and cAMP-dependent protein kinase-dependent processes. Mol Cell Biol. 2008;28:3804–3816.
   PubMed Web of Science ®Google Scholar
• Costa‐Almeida R, Berdecka D, Rodrigues MT, et al. Tendon explant cultures to study the communication between adipose stem cells and native tendon niche. J Cell Biochem. 2018;119:3653–3662.
   PubMed Web of Science ®Google Scholar
• Miyata Y, Otsuki M, Kita S, et al. Identification of mouse mesenteric and subcutaneous in vitro adipogenic cells. Sci Rep. 2016;6:21041.
   PubMed Web of Science ®Google Scholar
• Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–147.
   PubMed Web of Science ®Google Scholar
• Fernyhough ME, Okine E, Hausman G, et al. PPARγ and GLUT-4 expression as developmental regulators/markers for preadipocyte differentiation into an adipocyte. Dom Anim Endocrinol. 2007;33:367–378.
   PubMed Web of Science ®Google Scholar
• Spiegelman BM. PPAR-gamma: adipogenic regulator and thiazolidinedione receptor. Diabetes. 1998;47:507–514.
   PubMed Web of Science ®Google Scholar
• Wu Z, Bucher NL, Farmer SR. Induction of peroxisome proliferator-activated receptor gamma during the conversion of 3T3 fibroblasts into adipocytes is mediated by C/EBPbeta, C/ EBPdelta,and glucocorticoids. Mol Cell Biol. 1996;16:4128–4136.
   PubMed Web of Science ®Google Scholar
• Caprio M, Feve B, Claës A, et al. Pivotal role of the mineralocorticoid receptor in corticosteroid-induced adipogenesis. Faseb J. 2007;21:2185–2194.
   PubMed Web of Science ®Google Scholar
• Beloor J, Kang HK, Moon YS. Serum lipids can convert bovine myogenic satellite cells to adipocytes. Asian-Australas J Anim Sci. 2010;23:1519–1526.
   Web of Science ®Google Scholar
• Gaebel R, Furlani D, Sorg H, et al. Cell origin of human mesenchymal stem cells determines a different healing performance in cardiac regeneration. PLoS One. 2011;6:e15652.
   PubMed Web of Science ®Google Scholar
• Jones E, English A, Churchman SM, et al. Large‐scale extraction and characterization of CD271+ multipotential stromal cells from trabecular bone in health and osteoarthritis: implications for bone regeneration strategies based on uncultured or minimally cultured multipotential stromal cells. Arthritis Rheum. 2010;62:1944–1954.
   PubMedGoogle Scholar
• Dominici MLBK, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–317.
   PubMed Web of Science ®Google Scholar
• Boxall SA, Jones E. Markers for characterization of bone marrow multi-potential stromal cells. Stem Cells Int. 2012;2012 :975871.
   PubMed Web of Science ®Google Scholar
• Mark P, Kleinsorge M, Gaebel R, et al. Human mesenchymal stem cells display reduced expression of CD105 after culture in serum-free medium. Stem Cells Int. 2013;2013:698076.
   PubMed Web of Science ®Google Scholar
• Woeller CF, O’loughlin CW, Pollock SJ, et al. Thy1 (CD90) controls adipogenesis by regulating activity of the Src family kinase, Fyn. Faseb J. 2014;29:920–931.
   PubMed Web of Science ®Google Scholar
• Moraes DA, Sibov TT, Pavon LF, et al. A reduction in CD90 (THY-1) expression results in increased differentiation of mesenchymal stromal cells. Stem Cell Res Ther. 2016;7:97.
   PubMed Web of Science ®Google Scholar
• Cuaranta-Monroy I, Simandi Z, Kolostyak Z, et al. Highly efficient differentiation of embryonic stem cells into adipocytes by ascorbic acid. Stem Cell Res. 2014;13:88–97.
   PubMed Web of Science ®Google Scholar
• Furuhashi M, Hotamisligil GS. Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat Rev Drug Discov. 2008;7:489.
   PubMed Web of Science ®Google Scholar
• Tontonoz P, Spiegelman BM. Fat and beyond: the diverse biology of PPARγ. Annu Rev Biochem. 2008;77:289–312.
   PubMed Web of Science ®Google Scholar
• Garin-Shkolnik T, Rudich A, Hotamisligil GS, et al. FABP4 attenuates PPARγ and adipogenesis and is inversely correlated with PPARγ in adipose tissues. Diabetes. 2014;63:900–911.
   PubMed Web of Science ®Google Scholar
• Ono M, Aratani Y, Kitagawa I, et al. Ascorbic acid phosphate stimulates type IV collagen synthesis and accelerates adipose conversion of 3T3-L1 cells. Exp Cell Res. 1990;187:309–314.
   PubMed Web of Science ®Google Scholar
• Lee OH, Seo DH, Park CS, et al. Puerarin enhances adipocyte differentiation, adiponectin expression, and antioxidant response in 3T3‐L1 cells. Biofactors. 2010;36:459–467.
   PubMed Web of Science ®Google Scholar
• Steen KA, Xu H, Bernlohr DA. FABP4/aP2 regulates macrophage redox signaling and inflammasome activation via control of UCP2. Mol Cell Biol. 2017;37:e00282–16.
   PubMed Web of Science ®Google Scholar
• Smas CM, Chen L, Sul HS. Cleavage of membrane-associated pref-1 generates a soluble inhibitor of adipocyte differentiation. Mol Cell Biol. 1997;17:977–988.
   PubMed Web of Science ®Google Scholar
• Hudak CS, Sul HS. Pref-1, a gatekeeper of adipogenesis. Front Endocrinol. 2013;4:79.
   PubMedGoogle Scholar
• Abel ED, Peroni O, Kim JK, et al. Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature. 2001;409: 729–433.
   PubMed Web of Science ®Google Scholar