Skip to main content

Advertisement

Log in

Surface protein expression between human adipose tissue-derived stromal cells and mature adipocytes

  • Original paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Katz FE, Tindle R, Sutherland DR, Greaves MF (1985) Identification of a membrane glycoprotein associated with haemopoietic progenitor cells. Leuk Res 9:191–198

    Article  PubMed  CAS  Google Scholar 

  • Kuniyasu A, Hayashi S, Nakayama H (2002) Adipocytes recognize and degrade oxidized low density lipoprotein through CD36. Biochem Biophys Res Commun 295:319–323

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Martin ML, Jensen MD (1991) Effects of body fat distribution on regional lipolysis in obesity. J Clin Invest 88:609–613

    PubMed  CAS  Google Scholar 

  • Miyaoka K, Kuwasako T, Hirano K, Nozaki S, Yamashita S, Matsuzawa Y (2001) CD36 deficiency associated with insulin resistance. Lancet 357:686–687

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sfeir Z, Ibrahimi A, Amri E, Grimaldi P, Abumrad N (1999) CD36 antisense expression in 3T3-F442A preadipocytes. Mol Cell Biochem 192:3–8

    Article  PubMed  CAS  Google Scholar 

  • Shahparaki A, Grunder L, Sorisky A (2002) Comparison of human abdominal subcutaneous versus omental preadipocyte differentiation in primary culture. Metabolism 51:1211–1215

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Su GL, Dorko K, Strom SC, Nussler AK, Wang SC (1999) CD14 expression and production by human hepatocytes. J Hepatol 31:435–442

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhao SP, Zhang DQ (2004) Atorvastatin enhances cellular uptake of oxidized LDL in adipocytes from hypercholesterolemic rabbits. Clin Chim Acta 339:189–194

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Régis Roche.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-005-0014-z

Keywords

Navigation