Analysis of In Vitro Insulin-Resistance Models and Their Physiological Relevance to InVivo Diet-Induced Adipose Insulin Resistance

Cell Reports

Volumn 5, Issue 1, 2013, Pages 259-270

  Lo, KinyuiAlice ^a,b   Labadorf, Adam ^a   Kennedy, Norman J ^d   Han, MyoungSook ^d   Yap, YoonSing ^a   Matthews, Bryan ^a   Xin, Xiaofeng ^a   Sun, Lei ^b   Davis, Roger J ^d   Lodish, Harvey F ^a,b,c   Fraenkel, Ernest ^a,e  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; DEOXYRIBONUCLEASE I; DEXAMETHASONE; INSULIN; TUMOR NECROSIS FACTOR ALPHA;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRAIN 3T3; CONTROLLED STUDY; DIET; DIET INDUCED OBESITY; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; INSULIN RESISTANCE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PRIORITY JOURNAL; RNA SEQUENCE; TRANSCRIPTION REGULATION; WHITE ADIPOSE TISSUE;

MUS;

ADIPOSE TISSUE; ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; INSULIN RESISTANCE; MICE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84885859572     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.08.039     Document Type: Article

References (46)

1. Andrews R.C., Walker B.R. Glucocorticoids and insulin resistance: old hormones, new targets. Clin. Sci. 1999, 96:513-523.
2. Birney E., Stamatoyannopoulos J.A., Dutta A., Guigó R., Gingeras T.R., Margulies E.H., Weng Z., Snyder M., Dermitzakis E.T., Thurman R.E., et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447:799-816. ENCODE Project Consortium, NISC Comparative Sequencing ProgramNISC Comparative Sequencing Program, Baylor College of Medicine Human Genome Sequencing CenterBaylor College of Medicine Human Genome Sequencing Center, Washington University Genome Sequencing CenterWashington University Genome Sequencing Center, Broad InstituteBroad Institute, Children's Hospital Oakland Research InstituteChildren's Hospital Oakland Research Institute.
3. Eguchi J., Yan Q.W., Schones D.E., Kamal M., Hsu C.H., Zhang M.Q., Crawford G.E., Rosen E.D. Interferon regulatory factors are transcriptional regulators of adipogenesis. Cell Metab. 2008, 7:86-94.
4. Elbein S.C., Kern P.A., Rasouli N., Yao-Borengasser A., Sharma N.K., Das S.K. Global gene expression profiles of subcutaneous adipose and muscle from glucose-tolerant, insulin-sensitive, and insulin-resistant individuals matched for BMI. Diabetes 2011, 60:1019-1029.
5. Fitzgibbons T.P., Kogan S., Aouadi M., Hendricks G.M., Straubhaar J., Czech M.P. Similarity of mouse perivascular and brown adipose tissues and their resistance to diet-induced inflammation. Am. J. Physiol. Heart Circ. Physiol. 2011, 301:H1425-H1437.
6. Forner F., Kumar C., Luber C.A., Fromme T., Klingenspor M., Mann M. Proteome differences between brown and white fat mitochondria reveal specialized metabolic functions. Cell Metab. 2009, 10:324-335.
7. Fujisaka S., Usui I., Kanatani Y., Ikutani M., Takasaki I., Tsuneyama K., Tabuchi Y., Bukhari A., Yamazaki Y., Suzuki H., et al. Telmisartan improves insulin resistance and modulates adipose tissue macrophage polarization in high-fat-fed mice. Endocrinology 2011, 152:1789-1799.
8. Green H., Meuth M. An established pre-adipose cell line and its differentiation in culture. Cell 1974, 3:127-133.
9. Hesselberth J.R., Chen X., Zhang Z., Sabo P.J., Sandstrom R., Reynolds A.P., Thurman R.E., Neph S., Kuehn M.S., Noble W.S., et al. Global mapping of protein-DNA interactions invivo by digital genomic footprinting. Nat. Methods 2009, 6:283-289.
10. Hosogai N., Fukuhara A., Oshima K., Miyata Y., Tanaka S., Segawa K., Furukawa S., Tochino Y., Komuro R., Matsuda M., Shimomura I. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 2007, 56:901-911.
11. Hotamisligil G.S., Shargill N.S., Spiegelman B.M. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993, 259:87-91.
12. Jager J., Grémeaux T., Cormont M., Le Marchand-Brustel Y., Tanti J.F. Interleukin-1β-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology 2007, 148:241-251.
13. Jiao P., Chen Q., Shah S., Du J., Tao B., Tzameli I., Yan W., Xu H. Obesity-related upregulation of monocyte chemotactic factors in adipocytes: involvement of nuclear factor-kappaB and c-Jun NH2-terminal kinase pathways. Diabetes 2009, 58:104-115.
14. Knutson V.P., Balba Y. 3T3-L1 adipocytes as a cell culture model of insulin resistance. InVitro Cell. Dev. Biol. Anim. 1997, 33:77-81.
15. Ling G., Sugathan A., Mazor T., Fraenkel E., Waxman D.J. Unbiased, genome-wide invivo mapping of transcriptional regulatory elements reveals sex differences in chromatin structure associated with sex-specific liver gene expression. Mol. Cell. Biol. 2010, 30:5531-5544.
16. MacIsaac K.D., Lo K.A., Gordon W., Motola S., Mazor T., Fraenkel E. A quantitative model of transcriptional regulation reveals the influence of binding location on expression. PLoS Comput. Biol. 2010, 6:e1000773.
17. Masuzaki H., Paterson J., Shinyama H., Morton N.M., Mullins J.J., Seckl J.R., Flier J.S. A transgenic model of visceral obesity and the metabolic syndrome. Science 2001, 294:2166-2170.
18. Mikkelsen T.S., Xu Z., Zhang X., Wang L., Gimble J.M., Lander E.S., Rosen E.D. Comparative epigenomic analysis of murine and human adipogenesis. Cell 2010, 143:156-169.
19. Millward C.A., Heaney J.D., Sinasac D.S., Chu E.C., Bederman I.R., Gilge D.A., Previs S.F., Croniger C.M. Mice with a deletion in the gene for CCAAT/enhancer-binding protein beta are protected against diet-induced obesity. Diabetes 2007, 56:161-167.
20. Nelson B.A., Robinson K.A., Buse M.G. High glucose and glucosamine induce insulin resistance via different mechanisms in 3T3-L1 adipocytes. Diabetes 2000, 49:981-991.
21. Newgard C.B., An J., Bain J.R., Muehlbauer M.J., Stevens R.D., Lien L.F., Haqq A.M., Shah S.H., Arlotto M., Slentz C.A., et al. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 2009, 9:311-326.
22. Nguyen M.T.A., Satoh H., Favelyukis S., Babendure J.L., Imamura T., Sbodio J.I., Zalevsky J., Dahiyat B.I., Chi N.W., Olefsky J.M. JNK and tumor necrosis factor-α mediate free fatty acid-induced insulin resistance in 3T3-L1 adipocytes. J.Biol. Chem. 2005, 280:35361-35371.
23. Pietiläinen K.H., Naukkarinen J., Rissanen A., Saharinen J., Ellonen P., Keränen H., Suomalainen A., Götz A., Suortti T., Yki-Järvinen H., et al. Global transcript profiles of fat in monozygotic twins discordant for BMI: pathways behind acquired obesity. PLoS Med. 2008, 5:e51.
24. Powers D.E., Milman J.R., Bonner-Weir S., Rappel M.J., Colton C.K. Accurate control of oxygen level in cells during culture on silicone rubber membranes with application of stem cell differentiation. Biotechnol. Prog. 2010, 26:805-818.
25. Qi L., Saberi M., Zmuda E., Wang Y., Altarejos J., Zhang X., Dentin R., Hedrick S., Bandyopadhyay G., Hai T., et al. Adipocyte CREB promotes insulin resistance in obesity. Cell Metab. 2009, 9:277-286.
26. Reaven G.M. The insulin resistance syndrome: definition and dietary approaches to treatment. Annu. Rev. Nutr. 2005, 25:391-406.
27. Regazzetti C., Peraldi P., Grémeaux T., Najem-Lendom R., Ben-Sahra I., Cormont M., Bost F., Le Marchand-Brustel Y., Tanti J.F., Giorgetti-Peraldi S. Hypoxia decreases insulin signaling pathways in adipocytes. Diabetes 2009, 58:95-103.
28. Rotter V., Nagaev I., Smith U. Interleukin-6 (IL-6) induces insulin resistance in 3T3-L1 adipocytes and is, like IL-8 and tumor necrosis factor-α, overexpressed in human fat cells from insulin-resistant subjects. J.Biol. Chem. 2003, 278:45777-45784.
29. Ruan H., Hacohen N., Golub T.R., Van Parijs L., Lodish H.F. Tumor necrosis factor-α suppresses adipocyte-specific genes and activates expression of preadipocyte genes in 3T3-L1 adipocytes: nuclear factor-kappaB activation by TNF-α is obligatory. Diabetes 2002, 51:1319-1336.
30. Sakoda H., Ogihara T., Anai M., Funaki M., Inukai K., Katagiri H., Fukushima Y., Onishi Y., Ono H., Fujishiro M., et al. Dexamethasone-induced insulin resistance in 3T3-L1 adipocytes is due to inhibition of glucose transport rather than insulin signal transduction. Diabetes 2000, 49:1700-1708.
31. Schroeder-Gloeckler J.M., Rahman S.M., Janssen R.C., Qiao L., Shao J., Roper M., Fischer S.J., Lowe E., Orlicky D.J., McManaman J.L., et al. CCAAT/enhancer-binding protein beta deletion reduces adiposity, hepatic steatosis, and diabetes in Lepr(db/db) mice. J.Biol. Chem. 2007, 282:15717-15729.
32. Schupp M., Cristancho A.G., Lefterova M.I., Hanniman E.A., Briggs E.R., Steger D.J., Qatanani M., Curtin J.C., Schug J., Ochsner S.A., et al. Re-expression of GATA2 cooperates with peroxisome proliferator-activated receptor-γ depletion to revert the adipocyte phenotype. J.Biol. Chem. 2009, 284:9458-9464.
33. Shanik M.H., Xu Y., Skrha J., Dankner R., Zick Y., Roth J. Insulin resistance and hyperinsulinemia: is hyperinsulinemia the cart or the horse?. Diabetes Care 2008, 31(Suppl 2):S262-S268.
34. Siersbæk R., Nielsen R., John S., Sung M.H., Baek S., Loft A., Hager G.L., Mandrup S. Extensive chromatin remodelling and establishment of transcription factor 'hotspots' during early adipogenesis. EMBO J. 2011, 30:1459-1472.
35. Smith T.R., Elmendorf J.S., David T.S., Turinsky J. Growth hormone-induced insulin resistance: role of the insulin receptor, IRS-1, GLUT-1, and GLUT-4. Am. J. Physiol. 1997, 272:E1071-E1079.
36. Steger D.J., Grant G.R., Schupp M., Tomaru T., Lefterova M.I., Schug J., Manduchi E., Stoeckert C.J., Lazar M.A. Propagation of adipogenic signals through an epigenomic transition state. Genes Dev. 2010, 24:1035-1044.
37. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
38. Sun L., Goff L.A., Trapnell C., Alexander R., Lo K.A., Hacisuleyman E., Sauvageau M., Tazon-Vega B., Kelley D.R., Hendrickson D.G., et al. Long noncoding RNAs regulate adipogenesis. Proc. Natl. Acad. Sci. USA 2013, 110:3387-3392.
39. Thomson M.J., Williams M.G., Frost S.C. Development of insulin resistance in 3T3-L1 adipocytes. J.Biol. Chem. 1997, 272:7759-7764.
40. Trapnell C., Williams B.A., Pertea G., Mortazavi A., Kwan G., van Baren M.J., Salzberg S.L., Wold B.J., Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010, 28:511-515.
41. Van Epps-Fung M., Williford J., Wells A., Hardy R.W. Fatty acid-induced insulin resistance in adipocytes. Endocrinology 1997, 138:4338-4345.
42. Wang M. The role of glucocorticoid action in the pathophysiology of the Metabolic Syndrome. Nutr. Metab. (Lond) 2005, 2:3.
43. Wang T.J., Larson M.G., Vasan R.S., Cheng S., Rhee E.P., McCabe E., Lewis G.D., Fox C.S., Jacques P.F., Fernandez C., et al. Metabolite profiles and the risk of developing diabetes. Nat. Med. 2011, 17:448-453.
44. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. J.Clin. Invest. 2003, 112:1796-1808.
45. Ye J., Gao Z., Yin J., He Q. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E1118-E1128.
46. Zhang Y., Liu T., Meyer C.A., Eeckhoute J., Johnson D.S., Bernstein B.E., Nusbaum C., Myers R.M., Brown M., Li W., Liu X.S. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008, 9:R137.