Beta-mecaptoethanol suppresses inflammation and induces adipogenic differentiation in 3T3-F442A murine preadipocytes

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Guo, Wen ^a   Li, Yahui ^a   Liang, Wentao ^a   Wong, Siu ^a   Apovian, Caroline ^a   Kirkland, James L ^b   Corkey, Barbara E ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; FAT DROPLET; I KAPPA B; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; LUCIFERASE; MERCAPTOETHANOL; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA;

ADIPOGENESIS; ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; AP2 GENE; ARTICLE; BIOACCUMULATION; CELL DIFFERENTIATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE; GENE EXPRESSION REGULATION; GLUT4 GENE; MARKER GENE; MICROPHOTOGRAPHY; MOUSE; NONHUMAN; PROADIPOCYTE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; SCD 1 GENE; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

3T3-L1 CELLS; ADIPOCYTES; ADIPOGENESIS; ANIMALS; CCAAT-ENHANCER-BINDING PROTEINS; CYTOKINES; ENZYME ACTIVATION; FREE RADICAL SCAVENGERS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; LIPID METABOLISM; MERCAPTOETHANOL; MICE; NF-KAPPA B; PPAR GAMMA; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TUMOR NECROSIS FACTOR-ALPHA;

MURINAE;

EID: 84864262961     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040958     Document Type: Article

References (79)

1. van Tienen FH, van der Kallen CJ, Lindsey PJ, Wanders RJ, van Greevenbroek MM, et al. (2011) Preadipocytes of type 2 diabetes subjects display an intrinsic gene expression profile of decreased differentiation capacity. Int J Obes (Lond) 35: 1154-1164.
2. Lijnen HR, Christiaens V, Scroyen L, (2011) Growth arrest-specific protein 6 receptor antagonism impairs adipocyte differentiation and adipose tissue development in mice. J Pharmacol Exp Ther 337: 457-464.
3. O'Connell J, Lynch L, Hogan A, Cawood TJ, O'Shea D, (2011) Preadipocyte factor-1 is associated with metabolic profile in severe obesity. J Clin Endocrinol Metab 96: E680-684.
4. Park HT, Lee ES, Cheon YP, Lee DR, Yang KS, et al. (2011) The relationship between fat depot-specific preadipocyte differentiation and metabolic syndrome in obese women. Clin Endocrinol (Oxf) 76: 59-66.
5. Moon MK, Cho BJ, Lee YJ, Choi SH, Lim S, et al. (2012) The effects of chronic exercise on the inflammatory cytokines interleukin-6 and tumor necrosis factor-alpha are different with age. Appl Physiol Nutr Metab: May 4 [Epub ahead of print].
6. Beyer I, Mets T, Bautmans I, (2011) Chronic low-grade inflammation and age-related sarcopenia. Curr Opin Clin Nutr Metab Care 15: 12-22.
7. Kalupahana NS, Moustaid-Moussa N, Claycombe KJ, (2011) Immunity as a link between obesity and insulin resistance. Mol Aspects Med 33: 26-34.
8. Kaur S, Zilmer K, Kairane C, Kals M, Zilmer M, (2008) Clear differences in adiponectin level and glutathione redox status revealed in obese and normal-weight patients with psoriasis. Br J Dermatol 159: 1364-1367.
9. Hotamisligil GS, Shargill NS, Spiegelman BM, (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259: 87-91.
10. Lee OH, Seo DH, Park CS, Kim YC, (2010) Puerarin enhances adipocyte differentiation, adiponectin expression, and antioxidant response in 3T3-L1 cells. Biofactors 36: 459-467.
11. Imhoff BR, Hansen JM, (2010) Extracellular redox environments regulate adipocyte differentiation. Differentiation 80: 31-39.
12. Imhoff BR, Hansen JM, (2011) Differential redox potential profiles during adipogenesis and osteogenesis. Cell Mol Biol Lett 16: 149-161.
13. Vigilanza P, Aquilano K, Baldelli S, Rotilio G, Ciriolo MR, (2011) Modulation of intracellular glutathione affects adipogenesis in 3T3-L1 cells. J Cell Physiol 226: 2016-2024.
14. Kobayashi H, Matsuda M, Fukuhara A, Komuro R, Shimomura I, (2009) Dysregulated glutathione metabolism links to impaired insulin action in adipocytes. Am J Physiol Endocrinol Metab 296: E1326-1334.
15. Click RE, (2010) Obesity, longevity, quality of life: alteration by dietary 2-mercaptoethanol. Virulence 1: 509-515.
16. Click RE, (2010) Longevity of SLE-prone mice increased by dietary 2-mercaptoethanol via a mechanism imprinted within the first 28 days of life. Virulence 1: 516-522.
17. Kirkland JL, Tchkonia T, Pirtskhalava T, Han J, Karagiannides I, (2002) Adipogenesis and aging: does aging make fat go MAD? Exp Gerontol 37: 757-767.
18. Green H, Kehinde O, (1976) Spontaneous heritable changes leading to increased adipose conversion in 3T3 cells. Cell 7: 105-113.
19. Diaz-Velasquez CE, Castro-Munozledo F, Kuri-Harcuch W, (2008) Staurosporine rapidly commits 3T3-F442A cells to the formation of adipocytes by activation of GSK-3beta and mobilization of calcium. J Cell Biochem 105: 147-157.
20. Moghe SS, Juma S, Imrhan V, Vijayagopal P, (2012) Effect of Blueberry Polyphenols on 3T3-F442A Preadipocyte Differentiation. J Med Food 15: 448-452.
21. Green H, Kehinde O, (1979) Formation of normally differentiated subcutaneous fat pads by an established preadipose cell line. J Cell Physiol 101: 169-171.
22. Mandrup S, Loftus TM, MacDougald OA, Kuhajda FP, Lane MD, (1997) Obese gene expression at in vivo levels by fat pads derived from s.c. implanted 3T3-F442A preadipocytes. Proc Natl Acad Sci U S A 94: 4300-4305.
23. MacDougald OA, Lane MD, (1995) Adipocyte differentiation. When precursors are also regulators. Curr Biol 5: 618-621.
24. Rosen ED, Spiegelman BM, (2000) Molecular regulation of adipogenesis. Annu Rev Cell Dev Biol 16: 145-171.
25. Koutnikova H, Auwerx J, (2001) Regulation of adipocyte differentiation. Ann Med 33: 556-561.
26. Fink T, Zachar V, (2011) Adipogenic differentiation of human mesenchymal stem cells. Methods Mol Biol 698: 243-251.
27. Spangenburg EE, Pratt SJ, Wohlers LM, Lovering RM, (2011) Use of BODIPY (493/503) to visualize intramuscular lipid droplets in skeletal muscle. J Biomed Biotechnol 2011: 598358.
28. Siersbaek R, Nielsen R, Mandrup S, (2010) PPARgamma in adipocyte differentiation and metabolism-novel insights from genome-wide studies. FEBS Lett 584: 3242-3249.
29. Cristancho AG, Lazar MA, (2011) Forming functional fat: a growing understanding of adipocyte differentiation. Nat Rev Mol Cell Biol 12: 722-734.
30. Elbrecht A, Chen Y, Adams A, Berger J, Griffin P, et al. (1999) L-764406 is a partial agonist of human peroxisome proliferator-activated receptor gamma. The role of Cys313 in ligand binding. J Biol Chem 274: 7913-7922.
31. Simone RE, Russo M, Catalano A, Monego G, Froehlich K, et al. (2011) Lycopene inhibits NF-kB-mediated IL-8 expression and changes redox and PPARgamma signalling in cigarette smoke-stimulated macrophages. PLoS One 6: e19652.
32. Blanquicett C, Kang BY, Ritzenthaler JD, Jones DP, Hart CM, (2010) Oxidative stress modulates PPAR gamma in vascular endothelial cells. Free Radic Biol Med 48: 1618-1625.
33. Tontonoz P, Hu E, Graves RA, Budavari AI, Spiegelman BM, (1994) mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev 8: 1224-1234.
34. Lee JH, Kim KA, Kwon KB, Kim EK, Lee YR, et al. (2007) Diallyl disulfide accelerates adipogenesis in 3T3-L1 cells. Int J Mol Med 20: 59-64.
35. Chiarugi P, Fiaschi T, (2009) Adiponectin in health and diseases: from metabolic syndrome to tissue regeneration. Expert Opin Ther Targets 14: 193-206.
36. MacDougald OA, Lane MD, (1995) Transcriptional regulation of gene expression during adipocyte differentiation. Annu Rev Biochem 64: 345-373.
37. Sundar IK, Caito S, Yao H, Rahman I, (2010) Oxidative stress, thiol redox signaling methods in epigenetics. Methods Enzymol 474: 213-244.
38. Bird SD, Legge M, Walker RJ, (2011) Thiols stabilize cobblestone morphology of cultured mesothelial cells. Cell Biol Int 35: 857-867.
39. Zembron-Lacny A, Slowinska-Lisowska M, Ziemba A, (2010) Integration of the thiol redox status with cytokine response to physical training in professional basketball players. Physiol Res 59: 239-245.
40. Gustafson B, Gogg S, Hedjazifar S, Jenndahl L, Hammarstedt A, et al. (2009) Inflammation and impaired adipogenesis in hypertrophic obesity in man. Am J Physiol Endocrinol Metab 297: E999-E1003.
41. Prins JB, O'Rahilly S, (1997) Regulation of adipose cell number in man. Clin Sci (Lond) 92: 3-11.
42. Finck BN, Kelley KW, Dantzer R, Johnson RW, (1998) In vivo and in vitro evidence for the involvement of tumor necrosis factor-alpha in the induction of leptin by lipopolysaccharide. Endocrinology 139: 2278-2283.
43. Finck BN, Johnson RW, (2000) Tumor necrosis factor (TNF)-alpha induces leptin production through the p55 TNF receptor. Am J Physiol Regul Integr Comp Physiol 278: R537-543.
44. Brodsky M, Halpert G, Albeck M, Sredni B, (2010) The anti-inflammatory effects of the tellurium redox modulating compound, AS101, are associated with regulation of NFkappaB signaling pathway and nitric oxide induction in macrophages. J Inflamm (Lond) 7: 3.
45. Fukuyama R, Ng KP, Cicek M, Kelleher C, Niculaita R, et al. (2007) Role of IKK and oscillatory NFkappaB kinetics in MMP-9 gene expression and chemoresistance to 5-fluorouracil in RKO colorectal cancer cells. Mol Carcinog 46: 402-413.
46. Cheong R, Hoffmann A, Levchenko A, (2008) Understanding NF-kappaB signaling via mathematical modeling. Mol Syst Biol 4: 192.
47. Singh S, Khar A, (2006) Biological effects of curcumin and its role in cancer chemoprevention and therapy. Anticancer Agents Med Chem 6: 259-270.
48. Kamata H, Hirata H, (1999) Redox regulation of cellular signalling. Cell Signal 11: 1-14.
49. Rahman I, Marwick J, Kirkham P, (2004) Redox modulation of chromatin remodeling: impact on histone acetylation and deacetylation, NF-kappaB and pro-inflammatory gene expression. Biochem Pharmacol 68: 1255-1267.
50. Berg AH, Lin Y, Lisanti MP, Scherer PE, (2004) Adipocyte differentiation induces dynamic changes in NF-kappaB expression and activity. Am J Physiol Endocrinol Metab 287: E1178-1188.
51. Chung SW, Kang BY, Kim SH, Pak YK, Cho D, et al. (2000) Oxidized low density lipoprotein inhibits interleukin-12 production in lipopolysaccharide-activated mouse macrophages via direct interactions between peroxisome proliferator-activated receptor-gamma and nuclear factor-kappa B. J Biol Chem 275: 32681-32687.
52. Ricote M, Huang J, Fajas L, Li A, Welch J, et al. (1998) Expression of the peroxisome proliferator-activated receptor gamma (PPARgamma) in human atherosclerosis and regulation in macrophages by colony stimulating factors and oxidized low density lipoprotein. Proc Natl Acad Sci U S A 95: 7614-7619.
53. Jiang C, Ting AT, Seed B, (1998) PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 391: 82-86.
54. Coskun H, Summerfield TL, Kniss DA, Friedman A, (2010) Mathematical modeling of preadipocyte fate determination. J Theor Biol 265: 87-94.
55. Cho S, Urata Y, Iida T, Goto S, Yamaguchi M, et al. (1998) Glutathione downregulates the phosphorylation of I kappa B: autoloop regulation of the NF-kappa B-mediated expression of NF-kappa B subunits by TNF-alpha in mouse vascular endothelial cells. Biochem Biophys Res Commun 253: 104-108.
56. Kil IS, Kim SY, Park JW, (2008) Glutathionylation regulates IkappaB. Biochem Biophys Res Commun 373: 169-173.
57. Lin YC, Huang GD, Hsieh CW, Wung BS, (2012) The glutathionylation of p65 modulates NF-kappaB activity in 15-Deoxy-Delta(12,14)-prostaglandin J(2)-treated endothelial cells. Free Radic Biol Med. 52: 1844-53.
58. Qanungo S, Starke DW, Pai HV, Mieyal JJ, Nieminen AL, (2007) Glutathione supplementation potentiates hypoxic apoptosis by S-glutathionylation of p65-NFkappaB. J Biol Chem 282: 18427-18436.
59. Vallespi MG, Colas M, Garay H, Reyes O, Arana MJ, (2004) Differential regulation of Th1/Th2 in relevant tissues for sepsis pathogenesis with a Limulus anti-LPS factor-derived peptide increases survival in Gram-positive sepsis. Int Immunopharmacol 4: 1343-1351.
60. Higa A, Chevet E, (2012) Redox signaling loops in the unfolded protein response. Cell Signal 24: 1548-1555.
61. Basseri S, Lhotak S, Sharma AM, Austin RC, (2009) The chemical chaperone 4-phenylbutyrate inhibits adipogenesis by modulating the unfolded protein response. J Lipid Res 50: 2486-2501.
62. Gummersbach C, Hemmrich K, Kroncke KD, Suschek CV, Fehsel K, et al. (2009) New aspects of adipogenesis: radicals and oxidative stress. Differentiation 77: 115-120.
63. Relic B, Zeddou M, Desoroux A, Beguin Y, de Seny D, et al. (2009) Genistein induces adipogenesis but inhibits leptin induction in human synovial fibroblasts. Lab Invest 89: 811-822.
64. Samuni Y, Cook JA, Choudhuri R, Degraff W, Sowers AL, et al. (2010) Inhibition of adipogenesis by Tempol in 3T3-L1 cells. Free Radic Biol Med 49: 667-673.
65. Imhoff BR, Hansen JM, (2010) Extracellular redox environments regulate adipocyte differentiation. Differentiation 80: 31-39.
66. Cho KJ, Moon HE, Moini H, Packer L, Yoon DY, et al. (2003) Alpha-lipoic acid inhibits adipocyte differentiation by regulating pro-adipogenic transcription factors via mitogen-activated protein kinase pathways. J Biol Chem 278: 34823-34833.
67. Lechpammer S, Epperly MW, Zhou S, Nie S, Glowacki J, et al. (2005) Adipocyte differentiation in Sod2(-/-) and Sod2(+/+) murine bone marrow stromal cells is associated with low antioxidant pools. Exp Hematol 33: 1201-1208.
68. Lee H, Lee YJ, Choi H, Ko EH, Kim JW, (2009) Reactive oxygen species facilitate adipocyte differentiation by accelerating mitotic clonal expansion. J Biol Chem 284: 10601-10609.
69. Zhou QG, Peng X, Hu LL, Xie D, Zhou M, et al. (2010) Advanced oxidation protein products inhibit differentiation and activate inflammation in 3T3-L1 preadipocytes. J Cell Physiol 225: 42-51.
70. Abe D, Saito T, Kubo Y, Nakamura Y, Sekiya K, (2010) A fraction of unripe kiwi fruit extract regulates adipocyte differentiation and function in 3T3-L1 cells. Biofactors 36: 52-59.
71. Abeydeera LR, Wang WH, Cantley TC, Prather RS, Day BN, (1998) Presence of beta-mercaptoethanol can increase the glutathione content of pig oocytes matured in vitro and the rate of blastocyst development after in vitro fertilization. Theriogenology 50: 747-756.
72. Bridgeman MM, Marsden M, Selby C, Morrison D, MacNee W, (1994) Effect of N-acetyl cysteine on the concentrations of thiols in plasma, bronchoalveolar lavage fluid, and lung tissue. Thorax 49: 670-675.
73. Briggs DB, Jones CM, Mashalidis EH, Nunez M, Hausrath AC, et al. (2009) Disulfide-dependent self-assembly of adiponectin octadecamers from trimers and presence of stable octadecameric adiponectin lacking disulfide bonds in vitro. Biochemistry 48: 12345-12357.
74. Antonopoulos AS, Lee R, Margaritis M, Antoniades C, (2011) Adiponectin as a regulator of vascular redox state: therapeutic implications. Recent Pat Cardiovasc Drug Discov 6: 78-88.
75. Vincent HK, Bourguignon CM, Weltman AL, Vincent KR, Barrett E, et al. (2009) Effects of antioxidant supplementation on insulin sensitivity, endothelial adhesion molecules, and oxidative stress in normal-weight and overweight young adults. Metabolism 58: 254-262.
76. Sun K, Kusminski CM, Scherer PE, (2011) Adipose tissue remodeling and obesity. J Clin Invest 121: 2094-2101.
77. Tchkonia T, Morbeck DE, Von Zglinicki T, Van Deursen J, Lustgarten J, et al. (2010) Fat tissue, aging, and cellular senescence. Aging Cell 9: 667-684.
78. Heidrick ML, Hendricks LC, Cook DE, (1984) Effect of dietary 2-mercaptoethanol on the life span, immune system, tumor incidence and lipid peroxidation damage in spleen lymphocytes of aging BC3F1 mice. Mech Ageing Dev 27: 341-358.
79. Fisette PL, Ram S, Andersen JM, Guo W, Ingalls RR, (2003) The Lip lipoprotein from Neisseria gonorrhoeae stimulates cytokine release and NF-kappaB activation in epithelial cells in a Toll-like receptor 2-dependent manner. J Biol Chem 278: 46252-46260.