Abstract
Adipose tissue contains a stroma that can be easily isolated. Thus, human adipose tissue presents an source of multipotent stromal cells. In order to determine the implication of hematopoietic markers in adipocyte biology, we have defined part of the phenotype of the human adipose tissue-derived stromal cells, and compared this to fully differentiated adipocytes. Flow cytometry demonstrates that the protein expression phenotype of both cell types are similar and includes the expression of CD10, CD13, CD34, CD36, CD55, CD59 and CD65. No significant difference between subcutaneous and omental adipose tissue could be demonstrated concerning the expression of these markers. However, the expression of CD34, CD36 and CD65 is cell-dependent. While the expression of CD36 and CD65 doubled between stromal cells and mature adipocytes, the expression of CD34 decreased, despite this protein being present on the mature adipocyte. As CD34 is described as a stem cell marker and it being unlikely to be expressed on differentiated cells, this result was confirmed by immunostaining and western blot. The clear function of this protein on the adipocyte membrane remains to be determined. The characterization of new proteins on mature adipocytes could have broad implications for the comprehension of the biology of this tissue.
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Aust L, Devlin B, Foster SJ, Halvorsen YD, Hicok K, du Laney T, Sen A, Willingmyre GD, Gimble JM (2004) Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 6:7–14
Baumhueter S, Dybdal N, Kyle C, Lasky LA (1994) Global vascular expression of murine CD34, a sialomucin-like endothelial ligand for L-selectin. Blood 84:2554–2565
Berenson RJ, Bensinger WI, Hill RS, Andrews RG, Garcia-Lopez J, Kalamasz DF, Still BJ, Spitzer G, Buckner CD, Bernstein ID et al (1991) Engraftment after infusion of CD34+ marrow cells in patients with breast cancer or neuroblastoma. Blood 77:1717–1722
Bornstein SR, Abu-Asab M, Glasow A, Path G, Hauner H, Tsokos M, Chrousos GP, Scherbaum WA (2000) Immunohistochemical and ultrastructural localization of leptin and leptin receptor in human white adipose tissue and differentiating human adipose cells in primary culture. Diabetes 49:532–538
Bouloumie A, Sengenes C, Portolan G, Galitzky J, Lafontan M (2001) Adipocyte produces matrix metalloproteinases 2 and 9: involvement in adipose differentiation. Diabetes 50:2080–2086
Delia D, Lampugnani MG, Resnati M, Dejana E, Aiello A, Fontanella E, Soligo D, Pierotti MA, Greaves MF (1993) CD34 expression is regulated reciprocally with adhesion molecules in vascular endothelial cells in vitro. Blood 81:1001–1008
Drew E, Merkens H, Chelliah S, Doyonnas R, McNagny KM (2002) CD34 is a specific marker of mature murine mast cells. Exp Hematol 30:1211
Fain JN, Kanu A, Bahouth SW, Cowan GS, Lloyd Hiler M (2003) Inhibition of leptin release by atrial natriuretic peptide (ANP) in human adipocytes. Biochem Pharmacol 65:1883–1888
Fain JN, Madan AK, Hiler ML, Cheema P, Bahouth SW (2004) Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 145:2273–2282
Febbraio M, Abumrad NA, Hajjar DP, Sharma K, Cheng W, Pearce SF, Silverstein RL (1999) A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J Biol Chem 274:19055–19062
Fina L, Molgaard HV, Robertson D, Bradley NJ, Monaghan P, Delia D, Sutherland DR, Baker MA, Greaves MF (1990) Expression of the CD34 gene in vascular endothelial cells. Blood 75:2417–2426
Fried SK, Russell CD, Grauso NL, Brolin RE (1993) Lipoprotein lipase regulation by insulin and glucocorticoid in subcutaneous and omental adipose tissues of obese women and men. J Clin Invest 92:2191–2198
Frleta D, Noelle RJ, Wade WF (2003) CD40-mediated up-regulation of Toll-like receptor 4-MD2 complex on the surface of murine dendritic cells. J Leukoc Biol 74:1064–1073
Gronthos S, Franklin DM, Leddy HA, Robey PG, Storms RW, Gimble JM (2001) Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 189:54–63
Gupta SK, Lysko PG, Pillarisetti K, Ohlstein E, Stadel JM (1998) Chemokine receptors in human endothelial cells. Functional expression of CXCR4 and its transcriptional regulation by inflammatory cytokines. J Biol Chem 273:4282–4287
van Harmelen V, Dicker A, Ryden M, Hauner H, Lonnqvist F, Naslund E, Arner P (2002) Increased lipolysis and decreased leptin production by human omental as compared with subcutaneous preadipocytes. Diabetes 51:2029–2036
Hazan U, Romero IA, Cancello R, Valente S, Perrin V, Mariot V, Dumonceaux J, Gerhardt CC, Strosberg AD, Couraud PO, Pietri-Rouxel F (2002) Human adipose cells express CD4, CXCR4, and CCR5 [corrected] receptors: a new target cell type for the immunodeficiency virus-1? Faseb J 16:1254–1256
Healy L, May G, Gale K, Grosveld F, Greaves M, Enver T (1995) The stem cell antigen CD34 functions as a regulator of hemopoietic cell adhesion. Proc Natl Acad Sci USA 92:12240–12244
Heine H, El-Samalouti VT, Notzel C, Pfeiffer A, Lentschat A, Kusumoto S, Schmitz G, Hamann L, Ulmer AJ (2003) CD55/decay accelerating factor is part of the lipopolysaccharide-induced receptor complex. Eur J Immunol 33:1399–1408
Katz FE, Tindle R, Sutherland DR, Greaves MF (1985) Identification of a membrane glycoprotein associated with haemopoietic progenitor cells. Leuk Res 9:191–198
Kuniyasu A, Hayashi S, Nakayama H (2002) Adipocytes recognize and degrade oxidized low density lipoprotein through CD36. Biochem Biophys Res Commun 295:319–323
Kuniyasu A, Ohgami N, Hayashi S, Miyazaki A, Horiuchi S, Nakayama H (2003) CD36-mediated endocytic uptake of advanced glycation end products (AGE) in mouse 3T3-L1 and human subcutaneous adipocytes. FEBS Lett 537:85–90
Liang CP, Han S, Okamoto H, Carnemolla R, Tabas I, Accili D, Tall AR (2004) Increased CD36 protein as a response to defective insulin signaling in macrophages. J Clin Invest 113:764–773
Lihn AS, Bruun JM, He G, Pedersen SB, Jensen PF, Richelsen B (2004) Lower expression of adiponectin mRNA in visceral adipose tissue in lean and obese subjects. Mol Cell Endocrinol 219:9–15
Lundgren M, Buren J, Ruge T, Myrnas T, Eriksson JW (2004) Glucocorticoids down-regulate glucose uptake capacity and insulin-signaling proteins in omental but not subcutaneous human adipocytes. J Clin Endocrinol Metab 89:2989–2997
Lynn WA, Liu Y, Golenbock DT (1993) Neither CD14 nor serum is absolutely necessary for activation of mononuclear phagocytes by bacterial lipopolysaccharide. Infect Immun 61:4452–4461
Majdic O, Stockl J, Pickl WF, Bohuslav J, Strobl H, Scheinecker C, Stockinger H, Knapp W (1994) Signaling and induction of enhanced cytoadhesiveness via the hematopoietic progenitor cell surface molecule CD34. Blood 83:1226–1234
Marin P, Lonn L, Andersson B, Oden B, Olbe L, Bengtsson BA, Bjorntorp P (1996) Assimilation of triglycerides in subcutaneous and intraabdominal adipose tissues in vivo in men: effects of testosterone. J Clin Endocrinol Metab 81:1018–1022
Martin ML, Jensen MD (1991) Effects of body fat distribution on regional lipolysis in obesity. J Clin Invest 88:609–613
Miyaoka K, Kuwasako T, Hirano K, Nozaki S, Yamashita S, Matsuzawa Y (2001) CD36 deficiency associated with insulin resistance. Lancet 357:686–687
Montague CT, Prins JB, Sanders L, Digby JE, O’Rahilly S (1997) Depot- and sex-specific differences in human leptin mRNA expression: implications for the control of regional fat distribution. Diabetes 46:342–347
Montague CT, Prins JB, Sanders L, Zhang J, Sewter CP, Digby J, Byrne CD, O’Rahilly S (1998) Depot-related gene expression in human subcutaneous and omental adipocytes. Diabetes 47:1384–1391
Motoshima H, Wu X, Sinha MK, Hardy VE, Rosato EL, Barbot DJ, Rosato FE, Goldstein BJ (2002) Differential regulation of adiponectin secretion from cultured human omental and subcutaneous adipocytes: effects of insulin and rosiglitazone. J Clin Endocrinol Metab 87:5662–5667
Noguchi M, Sato N, Sugimori H, Mori K, Oshimi K (2001) A minor E-selectin ligand, CD65, is critical for extravascular infiltration of acute myeloid leukemia cells. Leuk Res 25:847–853
Planat-Benard V, Silvestre JS, Cousin B, Andre M, Nibbelink M, Tamarat R, Clergue M, Manneville C, Saillan-Barreau C, Duriez M, Tedgui A, Levy B, Penicaud L, Casteilla L (2004) Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 109:656–663
Rebuffe-Scrive M, Bronnegard M, Nilsson A, Eldh J, Gustafsson JA, Bjorntorp P (1990) Steroid hormone receptors in human adipose tissues. J Clin Endocrinol Metab 71:1215–1219
Sewter CP, Digby JE, Blows F, Prins J, O’Rahilly S (1999) Regulation of tumour necrosis factor-alpha release from human adipose tissue in vitro. J Endocrinol 163:33–38
Sfeir Z, Ibrahimi A, Amri E, Grimaldi P, Abumrad N (1999) CD36 antisense expression in 3T3-F442A preadipocytes. Mol Cell Biochem 192:3–8
Shahparaki A, Grunder L, Sorisky A (2002) Comparison of human abdominal subcutaneous versus omental preadipocyte differentiation in primary culture. Metabolism 51:1211–1215
Shubinsky G, Schlesinger M (1997) The CD38 lymphocyte differentiation marker: new insight into its ectoenzymatic activity and its role as a signal transducer. Immunity 7:315–324
Stanton LA, van de Venter M, Litthauer D, Oelofsen W (1997) Effect of lipoproteins on the differentiation of 3T3-L1 and human preadipocytes in cell culture. Comp Biochem Physiol B Biochem Mol Biol 116:65–73
Su GL, Dorko K, Strom SC, Nussler AK, Wang SC (1999) CD14 expression and production by human hepatocytes. J Hepatol 31:435–442
Teboul L, Febbraio M, Gaillard D, Amri EZ, Silverstein R, Grimaldi PA (2001) Structural and functional characterization of the mouse fatty acid translocase promoter: activation during adipose differentiation. Biochem J 360:305–312
Tedder TF, Streuli M, Schlossman SF, Saito H (1988) Isolation and structure of a cDNA encoding the B1 (CD20) cell-surface antigen of human B lymphocytes. Proc Natl Acad Sci USA 85:208–212
Tiraby C, Tavernier G, Lefort C, Larrouy D, Bouillaud F, Ricquier D, Langin D (2003) Acquirement of brown fat cell features by human white adipocytes. J Biol Chem 278:33370–33376
Young HE, Steele TA, Bray RA, Detmer K, Blake LW, Lucas PW, Black AC Jr (1999) Human pluripotent and progenitor cells display cell surface cluster differentiation markers CD10, CD13, CD56, and MHC class-I. Proc Soc Exp Biol Med 221:63–71
Zhao SP, Zhang DQ (2004) Atorvastatin enhances cellular uptake of oxidized LDL in adipocytes from hypercholesterolemic rabbits. Clin Chim Acta 339:189–194
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Festy, F., Hoareau, L., Bes-Houtmann, S. et al. Surface protein expression between human adipose tissue-derived stromal cells and mature adipocytes. Histochem Cell Biol 124, 113–121 (2005). https://doi.org/10.1007/s00418-005-0014-z
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DOI: https://doi.org/10.1007/s00418-005-0014-z