Monoterpene limonene induces brown fat-like phenotype in 3T3-L1 white adipocytes

Life Sciences

Volumn 153, Issue , 2016, Pages 198-206

  Lone, Jameel ^a   Yun, Jong Won ^a  

^a Daegu University   (South Korea)

Author keywords

3T3 L1 adipocytes; Anti obesity; Fat browning; Limonene; UCP1

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ACONITATE HYDRATASE; CARNITINE PALMITOYLTRANSFERASE I; CCAAT ENHANCER BINDING PROTEIN BETA; CYTOCHROME C; CYTOCHROME C OXIDASE; HORMONE SENSITIVE LIPASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LIMONENE; MITOGEN ACTIVATED PROTEIN KINASE; PERILIPIN; PROTEIN SERINE THREONINE KINASE INHIBITOR; TERPENE; UNCOUPLING PROTEIN 1; CYCLOHEXENE DERIVATIVE;

3T3 CELL LINE; ARTICLE; BROWN ADIPOCYTE; BROWN FAT LIKE PHENOTYPE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; LIPID METABOLISM; LIPOLYSIS; MITOCHONDRIAL BIOGENESIS; PHENOTYPE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WHITE ADIPOCYTE; ADIPOCYTE; ANIMAL; BROWN ADIPOSE TISSUE; CYTOLOGY; DRUG EFFECTS; MOUSE; WHITE ADIPOSE TISSUE;

3T3-L1 CELLS; ADIPOCYTES; ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANIMALS; CELL DIFFERENTIATION; CYCLOHEXENES; MICE; PHENOTYPE; TERPENES;

EID: 84971602444     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2016.04.010     Document Type: Article

References (62)

1. Y.H. Tseng, A.M. Cypess, and C.R. Kahn Cellular bioenergetics as a target for obesity therapy Nat. Rev. Drug Discov. 9 2010 465 482
2. S. Cinti Adipocyte differentiation and transdifferentiation: plasticity of the adipose organ J. Endocrinol. Investig. 25 2002 823 835
3. M. Harms, and P. Seale Brown and beige fat: development, function and therapeutic potential Nat. Med. 19 2013 1252 1263
4. K.A. Virtanen, M.E. Lidell, J. Orava, M. Heglind, and et al. Functional brown adipose tissue in healthy adults N. Engl. J. Med. 360 2009 1518 1525
5. M. Rosenwald, A. Perdikari, T. Rulicke, and C. Wolfrum Bi-directional interconversion of brite and white adipocytes Nat. Cell Biol. 15 2013 659 667
6. D. Ricquier Uncoupling protein 1 of brown adipocytes, the only uncoupler: a historicalperspective Front. Endocrinol. 2 2011 85 10.3389/fendo. 2011.00085
7. P. Seale, B. Bjork, W. Yang, S. Kajimura, S. Chin, S. Kuang, and et al. PRDM16 controls a brown fat/skeletal muscle switch Nature 7207 2008 961 967
8. J. Sanchez-Gurmaches, C.M. Hung, C.A. Sparks, Y. Tang, H. Li, and D.A. Guertin PTEN loss in the Myf5 lineage redistributes body fat and reveals subsets of white adipocytes that arise from Myf5 precursors Cell Metab. 3 2012 348 362
9. H. Asano, Y. Kanamori, S. Higurashi, T. Nara, K. Kato, T. Matsui, and M. Funaba Induction of beige-like adipocytes in 3T3-L1 cells J Vet Med Sci. 76 2014 57 64
10. M. Giralt, and F. Villarroya White, brown, beige/brite: different adipose cells for different functions? Endocrinology 154 2013 2992 3000
11. G. Fruhbeck, S. Becerril, N. Sáinz, P. Garrastachu, and M.J. García-Velloso BAT a new target for human obesity? Trends Pharmacol. Sci. 30 2009 387 396
12. M.J. Barbera, A. Schluter, N. Pedraza, R. Iglesias, F. Villarroya, and M. Giralt Peroxisome proliferator-activated receptor alpha activates transcription of the brown fat uncoupling protein-1 gene, a link between regulation of the thermogenic and lipid oxidation pathway in the brown fat cell J. Biol. Chem. 276 2001 1486 1493
13. A. Cederberg, L.M. Gronning, B. Ahrén, K. Taskén, P. Carlsson, and S. Enerbäck FOXC2 is a winged helix gene that counteracts obesity, hypertriglyceridemia, and diet-induced insulin resistance Cell 106 2001 563 573
14. H.M. Feldmann, V. Golozoubova, B. Cannon, and J. Nedergaard UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality Cell Metab. 9 2009 203 209
15. M.L. Bonet, P. Oliver, and A. Palou Pharmacological and nutritional agents promoting browning of white adipose tissue Biochim. Biophys. Acta 1831 2013 969 985
16. J. Merlin, B.A. Evans, N. Dehvari, M. Sato, T. Bengtsson, and D.S. Hutchinson Could burning fat start with a brite spark?, pharmacological and nutritional ways to promote thermogenesis Mol. Nutr. Food Res. 60 2015 18 42
17. S. Wang, X. Wang, Z. Ye, C. Xu, M. Zhang, B. Ruan, M. Wei, Y. Jiang, Y. Zhang, L. Wang, X. Lei, and Z. Lu Curcumin promotes browning of white adipose tissue in a norepinephrine-dependent way Biochem. Biophys. Res. Commun. 466 2015 247 253
18. J. Lone, J.H. Choi, S.W. Kim, and J.W. Yun Curcumin induces brown fat-like phenotype in 3T3-L1 and primary white adipocytes J Nutr Biochem. 27 2016 193 202
19. Z. Zhang, H. Zhang, B. Li, X. Meng, J. Wang, Y. Zhang, and et al. Berberine activates thermogenesis in white and brown adipose tissue Nat Commun. 25 2014 10.1038/ncomms 6493
20. R.K. Baboota, D.P. Singh, S.M. Sarma, J. Kaur, and et al. Capsaicin induces "brite" phenotype in differentiating 3 T3-L1 preadipocytes PLoS One 9 2014 e103093
21. J. Sun d-Limonene: safety and clinical applications Altern. Med. Rev. 12 2007 259 264
22. P.L. Crowell, and M.N. Gould Chemoprevention and therapy of cancer by d-limonene Crit. Rev. Oncog. 5 1994 1 22
23. D. Roberto, P. Micucci, T. Sebastian, F. Graciela, and C. Anesini Antioxidant activity of limonene on normal murine lymphocytes: relation to H2O2 modulation and cell proliferation Basic Clin Pharmacol Toxicol. 106 2010 38 44
24. C.E. Elson, T.H. Maltzman, J.L. Boston, M.A. Tanner, and M.N. Gould Anti-carcinogenic activity of d-limonene during the initiation and promotion/progression stages of DMBA-induced rat mammary carcinogenesis Carcinogenesis 9 1988 331 332
25. B. Chueca, R. Pagan, and D. García-Gonzalo Differential mechanism of Escherichia coli inactivation by (+)-limonene as a function of cell physiological state and drug's concentration PLoS One 9 2014 e94072
26. G.S. Kim, H.J. Park, J.H. Woo, M.K. Kim, P.O. Koh, W. Min, Y.G. Ko, C.H. Kim, C.K. Won, and J.H. Cho Citrus aurantium flavonoids inhibit adipogenesis through the Akt signaling pathway in 3T3-L1 cells BMC Complement Altern Med. 3 2012 12 31
27. C.M. Lappas, and N.T. Lappas d-Limonene modulates T lymphocyte activity and viability Cell. Immunol. 279 2012 30 41
28. S.S. Jia, G.P. Xi, M. Zhang, Y.B. Chen, B. Lei, X.S. Dong, and Y.M. Yang Induction of apoptosis by d-limonene is mediated by inactivation of Akt in LS174T human colon cancer cells Oncol. Rep. 29 2013 349 354
29. S. Kapoor d-Limonene: an emerging antineoplastic agent Hum Exp Toxicol. 32 2013 10.1177/0960327113489053
30. P.A. d'Alessio, R. Ostan, J.F. Bisson, J.D. Schulzke, M.V. Ursini, and M.C. Bene Oral administration of d-limonene controls inflammation in rat colitis and displays anti-inflammatory properties as diet supplementation in humans Life Sci. 92 2013 1151 1156
31. S. Cho, Y. Choi, S. Park, and T. Park Carvacrol prevents diet-induced obesity by modulating gene expressions involved in adipogenesis and inflammation in mice fed with high-fat diet J. Nutr. Biochem. 2 2012 192 201
32. P.L. Crowell, and M.N. Gould Chemoprevention and therapy of cancer by d-limonene Crit. Rev. Oncog. 5 1994 1 22
33. N.W. Baddar, T.A. Aburjai, M.O. Taha, and A.M. Disi Thujone corrects cholesterol and triglyceride profiles in diabetic rat model Nat. Prod. Res. 25 2011 1180 1184
34. L. Jing, Y. Zhang, S. Fan, M. Gu, Y. Guan, X. Lu, C. Huang, and Z. Zhou Preventive and ameliorating effects of citrus d-limonene on dyslipidemia and hyperglycemia in mice with high-fat diet-induced obesity Eur. J. Pharmacol. 715 2013 46 55
35. R. Murali, A. Karthikeyan, and R. Saravanan Protective effects of d-limonene on lipid peroxidation and antioxidant enzymes in streptozotocin-induced diabetic rats Basic. Clin Pharmacol Toxicol. 112 2013 175 181
36. J. Victor Antony Santiago, J. Jayachitra, M. Shenbagam, and N. Nalini Dietary d-limonene alleviates insulin resistance and oxidative stress-induced liver injury in high-fat diet and l-NAME-treated rats Eur J Nutr. 51 2012 57 68
37. L.Z. Sharp, K. Shinoda, H. Ohno, D.W. Scheel, E. Tomoda, L. Ruiz, and et al. Human BAT possesses molecular signatures that resemble beige/brite cells PLoS One 7 2012 e49452
38. C. Tiraby, G. Tavernier, C. Lefort, D. Larrouy, F. Bouillaud, D. Ricquier, and et al. Acquirement of brown fat cell features by human white adipocytes J. Biol. Chem. 278 2003 33370 33376
39. P. Seale, H.M. Conroe, J. Estall, S. Kajimura, A. Frontini, J. Ishibashi, and et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice J. Clin. Invest. 121 2011 96 105
40. M. Rosell, M. Kaforou, A. Frontini, A. Okolo, Y.W. Chan, and et al. Brown and white adipose tissues: intrinsic differences in gene expression and response to cold exposure in mice Am. J. Physiol. Endocrinol. Metab. 306 2014 E945 E964
41. P.J. Fernandez-Marcos, and J. Auwerx Regulation of PGC-1alpha, a nodal regulator of mitochondrial biogenesis Am. J. Clin. Nutr. 93 2011 884S 890S
42. J.A. Villena, M.C. Carmona, M. Rodriguez de la Concepcion, M. Rossmeisl, O. Vinas, and et al. Mitochondrial biogenesis in brown adipose tissue is associated with differential expression of transcription regulatory factors Cell Mol. Life Sci. 59 2002 1934 1944
43. K.L. Townsend, D. An, M.D. Lynes, T.L. Huang, H. Zhang, L.J. Goodyear, and et al. Increased mitochondrial activity in BMP7-treated brown adipocytes, due to increased CPT1- and CD36-mediated fattyacid uptake Antioxid. Redox Signal. 19 2013 243 257
44. P. Seale, S. Kajimura, W. Yang, S. Chin, L.M. Rohas, M. Uldry, G. Tavernier, D. Langin, and B.M. Spiegelman Transcriptional control of brown fat determination by PRDM16 Cell Metab. 7 2007 38 54
45. R.H. Lu, H. Ji, Z.G. Chang, S.S. Su, and G.S. Yang Mitochondrial development and the influence of its dysfunction during rat adipocyte differentiation Mol. Biol. Rep. 37 2010 2173 2182
46. E. Duplus, and C. Forest Is there a single mechanism for fatty acid regulation of gene transcription? Biochem. Pharmacol. 64 2002 893 901
47. J.W. Park, K.H. Jung, J.H. Lee, C.H. Quach, S.H. Moon, Y.S. Cho, and K.H. Lee 18F-FDG PET/CT monitoring of β3 agonist-stimulated brown adipocyte recruitment in white adipose tissue J. Nucl. Med. 56 2015 153 158
48. A. Lass, R. Zimmermann, M. Oberer, and R. Zechner Lipolysis - a highly regulated multi-enzyme complex mediates the catabolism of cellular fat stores Prog. Lipid Res. 50 2011 14 27
49. D. Langin, A. Dicker, G. Tavernier, J. Hoffstedt, A. Mairal, M. Rydén, E. Arner, A. Sicard, C.M. Jenkins, N. Viguerie, V. van Harmelen, R.W. Gross, C. Holm, and P. Arner Adipocyte lipases and defect of lipolysis in human obesity Diabetes 54 2005 3190 3197
50. E.P. Mottillo, A.E. Bloch, T. Leff, and J.G. Granneman Lipolytic products activate peroxisome proliferator-activated receptor (PPAR) α and δ in brown adipocytes to match fatty acid oxidation with supply J. Biol. Chem. 287 2012 25038 25048
51. E.P. Mottillo, X.J. Shen, and J.G. Granneman Role of hormone-sensitive lipase in beta- adrenergic remodeling of white adipose tissue Am. J. Physiol. Endocrinol. Metab. 293 2007 1188 1197
52. W.J. Shen, S. Patel, H. Miyoshi, A.S. Greenberg, and F.B. Kraemer Functional interaction of hormone-sensitive lipase and perilipin in lipolysis J. Lipid Res. 50 2009 2306 2313
53. T. Sawada, H. Miyoshi, K. Shimada, A. Suzuki, Y. Okamatsu-Ogura, J.W. Kondo, S. Nagai, C. Shimizu, N. Yoshioka, A.S. Greenberg, K. Kimura, and T. Koike Perilipin overexpression in white adipose tissue induces a brown fat-like phenotype PLoS One 5 2010 e14006
54. L.A. Harris, J.R. Skinner, T.M. Shew, T.A. Pietka, N.A. Abumrad, and N.E. Wolins Perilipin 5-driven lipid droplet accumulation in skeletal muscle stimulates the expression of Fibroblast Growth Factor 21 Diabetes 64 2015 2757 2768
55. D. Grahame Hardie AMP-activated protein kinase: a key regulator of energy balance with many roles in human disease J Intern Med. 276 2014 543 559
56. K.H. Kim Regulation of mammalian acetyl-coenzyme a carboxylase Annu. Rev. Nutr. 17 1997 77 99
57. G.L. Russo, M. Russo, and P. Ungaro AMP-activated protein kinase: a target for old drugs against diabetes and cancer Biochem. Pharmacol. 86 2013 339 350
58. S. Collins β-Adrenoceptor signaling networks in adipocytes for recruiting stored fat and energy expenditure Front Endocrinol. 2 2012 102 10.3389/fendo.2011.00102
59. D. Grujic, V.S. Susulic, M.E. Harper, J. Himms-Hagen, B.A. Cunningham, B.E. Corkey, and B.B. Lowell Beta3-adrenergic receptors on white and brown adipocytes mediate beta3-selective agonist-induced effects on energy expenditure, insulin secretion, and food intake. A study using transgenic and gene knockout mice J Biol Chem. 272 1997 17686 17693
60. J. Klein, M. Fasshauer, M. Benito, and C.R. Kahn Insulin and the beta3-adrenoceptor differentially regulate uncoupling protein-1 expression Mol. Endocrinol. 14 2000 764 773
61. M. Jimenez, G. Barbatelli, R. Allevi, S. Cinti, J. Seydoux, J.P. Giacobino, P. Muzzin, and F. Preitner Beta 3-adrenoceptor knockout in C57BL/6J mice depresses the occurrence of brown adipocytes in white fat Eur. J. Biochem. 270 2003 699 705
62. Y. Zhang, R. Li, Y. Meng, S. Li, W. Donelan, Y. Zhao, L. Qi, M. Zhang, X. Wang, T. Cui, L.J. Yang, and D. Tang Irisin stimulates browning of white adipocytes through mitogen-activated protein kinase p38 MAP kinase and ERK MAP kinase signaling Diabetes 63 2014 514 525