4,451
Views
22
CrossRef citations to date
0
Altmetric
Research Paper

Flow cytometric single cell analysis reveals heterogeneity between adipose depots

, , &
Pages 112-123 | Received 07 Apr 2017, Accepted 10 Apr 2017, Published online: 28 Apr 2017

References

  • Berry DC, Stenesen D, Zeve D, Graff JM. The developmental origins of adipose tissue. Development 2013; 140(19):3939–49; PMID:24046315; https://doi.org/10.1242/dev.080549</bib>
  • Ahmadian M, E Duncan R, Jaworski K, Sarkadi-Nagy E, Sul HS. Triacylglycerol metabolism in adipose tissue. Future Lipidol 2007; 2(2):229–37; PMID:19194515; https://doi.org/10.2217/17460875.2.2.229
  • Harms M, Seale P. Brown and beige fat: development, function and therapeutic potential. Nat Med 2013; 19(10):1252–63; PMID:24100998; https://doi.org/10.1038/nm.3361
  • Gesta S, Tseng Y-H, Kahn CR. Developmental origin of fat: Tracking obesity to its source. Cell 2007; 131(2):242–56; PMID:17956727; https://doi.org/10.1016/j.cell.2007.10.004
  • Lee MJ, Wu Y, Fried SK. Adipose tissue heterogeneity: Implication of depot differences in adipose tissue for obesity complications. Mol Aspects Med 2013; 34(1):1–11; PMID:23068073; https://doi.org/10.1016/j.mam.2012.10.001
  • Chau YY, Hastie N. Wt1, the mesothelium and the origins and heterogeneity of visceral fat progenitors. Adipocyte 2014; 4(3):217–21; https://doi.org/10.4161/21623945.2014.985009
  • Shungin D, Winkler TW, Croteau-Chonka DC, Ferreira T, Locke AE, Mägi R, Strawbridge J, Pers TH, Fischer K, Justice AE, et al. New genetic loci link adipose and insulin biology to body fat distribution. Nature 2015; 518(7538):187–96; PMID:25673412; https://doi.org/10.1038/nature14132
  • Sackmann-Sala L, Berryman DE, Munn RD, Lubbers ER, Kopchick JJ. Heterogeneity among white adipose tissue depots in male C57BL/6J mice. Obesity 2011; 20(1):101–11; PMID:21779095; https://doi.org/10.1038/oby.2011.235
  • Huang ZH, Espiritu DJ, Uy A, Holterman AX, Vitello J, Mazzone T. Adipose tissue depot-specific differences in adipocyte apolipoprotein E expression. Metabolism 2011; 60(12):1692–701; PMID:21664633; https://doi.org/10.1016/j.metabol.2011.04.012
  • White UA, Tchoukalova YD. Sex dimorphism and depot differences in adipose tissue function. Biochim Biophys Acta 2014; 1842(3):377–92; PMID:23684841; https://doi.org/10.1016/j.bbadis.2013.05.006
  • Jeffery E, Church CD, Holtrup B, Colman L, Rodeheffer MS. Rapid depot-specific activation of adipocyte precursor cells at the onset of obesity. Nat Cell Biol 2015; 17(4):376–85; PMID:25730471; https://doi.org/10.1038/ncb3122
  • Brake DK, Smith CW. Flow cytometry on the stromal-vascular fraction of white adipose tissue. Methods Mol Biol 2008; 456:221–29; PMID:18516564
  • Majka SM, Miller HL, Sullivan T, Erickson PF, Kong R, Weiser-Evans M, Nemenoff R, Moldovan R, Morandi RSA, Davis JA, et al. Adipose lineage specification of bone marrow-derived myeloid cells. Adipocyte 2014; 1(4):215–29; https://doi.org/10.4161/adip.21496
  • Majka SM, Fox KE, Psilas JC, Helm KM, Childs CR, Acosta AS, Janssen RC, Friedman JE, Woessner BT, Shade TR, et al. De novo generation of white adipocytes from the myeloid lineage via mesenchymal intermediates is age, adipose depot, and gender specific. Proc Natl Acad Sci U S A 2010; 107(22):14781–86; PMID:20679227; https://doi.org/10.1073/pnas.1003512107
  • Crossno JT, Majka SM, Grazia T, Gill RG, Klemm DJ. Rosiglitazone promotes development of a novel adipocyte population from bone marrow–derived circulating progenitor cells. J Clin Invest 2006; 116(12):3220–28; PMID:17143331; https://doi.org/10.1172/JCI28510
  • Gavin KM, Gutman JA, Kohrt WM, Wei Q, Shea KL, Miller HL, Sullivan TM, Erickson PD, Helm KM, Acosta AS, et al. De novo generation of adipocytes from circulating progenitor cells in mouse and human adipose tissue. FASEB J 2016; 30(3):1096–1108; PMID:26581599
  • Majka SM, Miller HL, Helm KM, Acosta AS, Childs CR, Kong R, Klemm DJ. Analysis and isolation of Adipocytes by flow cytometry. Methods Enzymol 2014; 537:281–96; PMID:24480352
  • Durandt C, van Vollenstee FA, Dessels C, Kallmeyer K, de Villiers D, Murdoch C, et al. Novel flow cytometric approach for the detection of adipocyte sub-populations during adipogenesis. J Lipid Red 2016; 57:729–42
  • Carswell KA, Lee M-J, Fried SK. Culture of isolated human adipocytes and isolated adipose tissue. Methods Mol Biol 2012; 806:203–214; PMID:22057454
  • Schaedlich K, Knelangen JM, Navarrete Santos A, Fischer B, Navarrete Santos A. A simple method to sort ESC-derived adipocytes. Cytometry 2010; 77A(10):990–5
  • Bjørndal B, Burri L, Staalesen V, Skorve J, Berge RK. Different Adipose Depots: Their role in the development of metabolic syndrome and mitochondrial response to Hypolipidemic Agents. J Obes 2011; 2011(1):1–15
  • Varlamov O, Somwar R, Cornea A, Kievit P, Grove KL, Roberts CT, Jr. Single-cell analysis of insulin-regulated fatty acid uptake in adipocytes. Am J Physiol Endocrinol Metab 2010; 299(3):E486–E496; PMID:20570821
  • Cawthorn WP, Scheller EL, MacDougald OA. Adipose tissue stem cells meet preadipocyte commitment: going back to the future. J Lipid Res 2012; 53(2):227–46; PMID:22140268
  • Qiao L, Zou C, Shao P, Schaack J, Johnson PF, Shao J. Transcriptional regulation of fatty acid translocase/CD36 expression by CCAAT/enhancer-binding protein alpha. J Biol Chem 2008; 283(14):8788–95; PMID:18263877
  • Liu Q, Wang M, Hu Y, Xing H, Chen X, Zhang Y, Zhu P. Significance of CD71 expression by flow cytometry in diagnosis of acute leukemia. Leuk Lymphoma 2015; 55(4):892–8
  • Adachi Y, Hino T, Ohsawa M, Ueki K, Murao T, Li M, Cui Y, Okigaki M, Ito M, Ikehara S. A case of CD10-negative angioimmunoblastic T cell lymphoma with leukemic change and increased plasma cells mimicking plasma cell leukemia: A case report. Oncol Lett 2015; 10:1555–60; PMID:26622708
  • Rawstron AC, Fazi C, Agathangelidis A, Villamor N, Letestu R, Nomdedeu J, Palacio C, Stehlikova O, Kreuzer KA, Liptrot S, et al. A complementary role of Multiparameter flow cytometry and high-throughput sequencing for minimal residual disease detection in chronic lymphocyte leukemia: an European Research Initiative on CLL study. Leukemia 2015; 30:1–27; PMID:26108693
  • Weir EG, Borowitz MJ. Flow cytometry in the diagnosis of acute leukemia. Semin Hematol 2001; 38(2):124–38; PMID:11309694
  • Xiao L, Yang X, Lin Y, Li S, Jiang J, Qian S, Tang Q, He R, Li X. Large adipocytes function as antigen-presenting cells to activate CD4(+) T cells via upregulating MHCII in obesity. Int J Obes (Lond) 2016; 40(1):112–20; PMID:26248660
  • Yoshida M, Stadler J, Bertholdt G, Gerisch G. Wheat germ agglutinin binds to the contact site A glycoprotein of Dictyostelium discoideum and inhibits EDTA-stable cell adhesion. EMBO J 2984; 3(11):2663–70
  • Smith JL. The staining of fat by Nile-blue sulphate. J Pathol Bacteriol 1911; 15:53–5; https://doi.org/10.1002/path.1700150107
  • Greenspan P, Mayer EP, Fowler SD. Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 1985; 100(3):965–73; PMID:3972906; https://doi.org/10.1083/jcb.100.3.965
  • Gocze PM, Freeman DA. Factors underlying the variability of lipid droplet fluorescence in MA-10 Leydig tumor cells. Cytometry 1994; 17(2):151–8; PMID:7835165; https://doi.org/10.1002/cyto.990170207
  • Chau YY, Bandiera R, Serrels A, Martínez-Estrada OM, Qing W, Lee M, Slight J, Thornburn A, Berry R, McHaffie S, et al. Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source. Nat Cell Biol 2014; 16(4):367–75; PMID:24609269; https://doi.org/10.1038/ncb2922
  • Poot M, Zhang YZ, Krämer JA, Wells KS, Jones LJ, Hanzel DK, Lugade AG, Singer VL, Haugland RP. Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J Histochem Cytochem 1996; 44(12):1363–72; PMID:8985128; https://doi.org/10.1177/44.12.8985128
  • Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerbäck S, et al. Functional Brown Adipose Tissue in Healthy Adults. N Engl J Med 2009; 360(15):1518–25; PMID:19357407; https://doi.org/10.1056/NEJMoa0808949
  • Sacks HS, Fain JN, Bahouth SW, Ojha S, Frontini A, Budge H, Cinti S, Symonds ME. Adult epicardial fat exhibits beige features. J Clin Endocrinol Metab 2013; 98(9):E1448–55; PMID:23824424; https://doi.org/10.1210/jc.2013-1265
  • Xu S, Jay A, Brunaldi K, Huang N, Hamilton JA. CD36 enhances fatty acid uptake by increasing the rate of intracellular Esterification but not transport across the plasma membrane. Biochemistry 2013; 52(41):7254–61; PMID:24090054; https://doi.org/10.1021/bi400914c
  • Putri M, Syamsunarno MRAA, Iso T, Yamaguchi A, Hanaoka H, Sunaga H, Koitabashi N, Matsui H, Yamazaki C, Kameo S, et al. CD36 is indispensible for thermogenesis under conditions of fasting and cold stress. Biochem Biophys Res Commun 2015; 457(4):520–5; PMID:25596128; https://doi.org/10.1016/j.bbrc.2014.12.124
  • Cherian S, Lopaschuk GD, Carvalho E. Cellular cross-talk between epicardial adipose tissue and myocardium in relation to the pathogenesis of cardiovascular disease. AJP: Endocrinol Metab 2012; 303(8):E937–49
  • Glatz JFC, Angin Y, Steinbusch LKM, Schwenk RW, Luiken JJFP. CD36 as a target to prevent cardiac lipotoxicity and insulin resistance. Prostaglandins Leukot essent Fatty Acids 2013; 88(1):71–7; PMID:22580174; https://doi.org/10.1016/j.plefa.2012.04.009
  • Fuente-Martín E, Argente-Arizón P, Ros P, Argente J, Chowen JA. Sex differences in adipose tissue. Adipocyte 2014; 2(3):128–34; https://doi.org/10.4161/adip.24075
  • Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med 2009; 360(15):1509–17; PMID:19357406; https://doi.org/10.1056/NEJMoa0810780
  • Ogunyemi D, Xu J, Mahesan AM, Rad S, Kim E, Yano J, Alexander C, Rotter JI, Chen Y-DI. Differentially expressed genes in adipocytokine signaling pathway of adipose tissue in pregnancy. J Diabetes Mellitus 2013; 03(2):86–95; https://doi.org/10.4236/jdm.2013.32013
  • Millican PE, Vernon RG, Pain VM. Protein-Metabolism in the mouse during pregnancy and lactation. Biochem J 1987; 248(1):251–7; PMID:3435442; https://doi.org/10.1042/bj2480251
  • Jones HN, Woollett LA, Barbour N, Prasad PD, Powell TL, Jansson T. High-fat diet before and during pregnancy causes marked up-regulation of placental nutrient transport and fetal overgrowth in C57/BL6 mice. FASEB J 2008; 23(1):271–8; PMID:18827021; https://doi.org/10.1096/fj.08-116889
  • Hajri T, Hall AM, Jensen DR, Pietka TA, Drover VA, Tao H, Eckel R, Abumrad NA. CD36-facilitated fatty acid uptake inhibits leptin production and signaling in adipose tissue. Diabetes 2007; 56(7):1872–80; PMID:17440173; https://doi.org/10.2337/db06-1699
  • Boyle KE, Hwang H, Janssen RC, DeVente JM, Barbour LA, Hernandez TL, Mandarino LJ, Friedman JE. Gestational diabetes is characterized by reduced mitochondrial protein expression and altered calcium signaling proteins in skeletal muscle. PLoS One 2014; 9(9):e106872; PMID:25216282; https://doi.org/10.1371/journal.pone.0106872
  • Nar G, Inci S, Aksan G, Unal OK, Nar R, Soylu K. The relationship between epicardial fat thickness and gestational diabetes mellitus. Diabetol Metab Syndr 2014; 6(1):120; PMID:25400702; https://doi.org/10.1186/1758-5996-6-120
  • Friedman JE. Obesity and Gestational Diabetes Mellitus pathways for programming in mouse, monkey, and man—Where do we go next? The 2014 Norbert Freinkel award lecture. Diabetes Care 2015; 38(8):1402–11; PMID:26207051; https://doi.org/10.2337/dc15-0628

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.