Modification of curcumin with polyethylene glycol enhances the delivery of curcumin in preadipocytes and its antiadipogenic property

Journal of Agricultural and Food Chemistry

Volumn 59, Issue 3, 2011, Pages 1012-1019

  Kim, Choon Young ^a   Bordenave, Nicolas ^a   Ferruzzi, Mario G ^a   Safavy, Ahmad ^b   Kim, Kee Hong ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

3T3 L1; Adipogenesis; Bioavailability; Curcumin; Polyethylene glycol; Solubility

Indexed keywords

3T3-L1; ADIPOCYTE DIFFERENTIATION; ADIPOCYTES; ADIPOGENESIS; ANTI-PROLIFERATIVE; BIOAVAILABILITY; CELL TOXICITY; CELLULAR UPTAKE; CURCUMIN; CYTOTOXIC EFFECTS; HUMAN CANCER CELLS; PEG-TREATMENT; PEGYLATION; PREADIPOCYTES; TOXIC EFFECT; WATER SOLUBILITIES;

BIOCHEMISTRY; CELL CULTURE; POLYETHYLENE OXIDES; POLYETHYLENES; SOLUBILITY; THERMOPLASTICS; TOXICITY;

POLYETHYLENE GLYCOLS;

CURCUMIN; MACROGOL DERIVATIVE; WATER;

ADIPOCYTE; ADIPOGENESIS; ANIMAL; ARTICLE; CELL STRAIN 3T3; CHEMISTRY; DRUG EFFECT; METABOLISM; MOUSE; SOLUBILITY;

3T3-L1 CELLS; ADIPOCYTES; ADIPOGENESIS; ANIMALS; CURCUMIN; MICE; POLYETHYLENE GLYCOLS; SOLUBILITY; WATER;

EID: 79851473420     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf103873k     Document Type: Article

References (61)

1. Dandona, P.; Aljada, A.; Bandyopadhyay, A. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol. 2004, 25(1), 4-7. (Pubitemid 38032801)
2. Kahn, S. E.; Hull, R. L.; Utzschneider, K. M. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006, 444(7121), 840-846. (Pubitemid 46024990)
3. Bruce, K. D.; Hanson, M. A. The developmental origins, mechanisms, and implications of metabolic syndrome. J. Nutr. 2010, 140(3), 648-652.
4. Spiegelman, B. M.; Flier, J. S. Adipogenesis and obesity: rounding out the big picture. Cell 1996, 87(3), 377-389. (Pubitemid 26374313)
5. Ntambi, J. M.; Young-Cheul, K. Adipocyte differentiation and gene expression. J. Nutr. 2000, 130(12), 3122S-3126S. (Pubitemid 32005353)
6. Sul, H. S.; Smas, C. M.; Wang, D.; Chen, L. Regulation of fat synthesis and adipose differentiation. Prog. Nucleic Acid Res. Mol. Biol. 1998, 60, 317-345.
7. Ross, S. E.; Hemati, N.; Longo, K. A.; Bennett, C. N.; Lucas, P. C.; Erickson, R. L.; MacDougald, O. A. Inhibition of adipogenesis by Wnt signaling. Science 2000, 289(5481), 950-953. (Pubitemid 30659947)
8. Lee, M. S.; Kim, C. T.; Kim, Y. Green tea (-)-epigallocatechin-3-gallate reduces body weight with regulation of multiple genes expression in adipose tissue of diet-induced obese mice. Ann. Nutr. Metab. 2009, 54(2), 151-157.
9. Moon, H. S.; Chung, C. S.; Lee, H. G.; Kim, T. G.; Choi, Y. J.; Cho, C. S. Inhibitory effect of (-)-epigallocatechin-3-gallate on lipid accumulation of 3T3-L1 cells. Obesity (Silver Spring) 2007, 15(11), 2571-2582.
10. Wolfram, S.; Wang, Y.; Thielecke, F. Anti-obesity effects of green tea: from bedside to bench. Mol. Nutr. Food Res. 2006, 50(2), 176-187. (Pubitemid 43325659)
11. Baur, J. A.; Pearson, K. J.; Price, N. L.; Jamieson, H. A.; Lerin, C.; Kalra, A.; Prabhu, V. V.; Allard, J. S.; Lopez-Lluch, G.; Lewis, K.; Pistell, P. J.; Poosala, S.; Becker, K. G.; Boss, O.; Gwinn, D.; Wang, M.; Ramaswamy, S.; Fishbein, K. W.; Spencer, R. G.; Lakatta, E. G.; Le Couteur, D.; Shaw, R. J.; Navas, P.; Puigserver, P.; Ingram, D. K; de Cabo, R.; Sinclair, D. A. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006, 444(7117), 337-342. (Pubitemid 44764104)
12. Macarulla, M. T.; Alberdi, G.; Gomez, S.; Tueros, I.; Bald, C.; Rodriguez, V. M.; Martinez, J. A.; Portillo, M. P. Effects of different doses of resveratrol on body fat and serum parameters in rats fed a hypercaloric diet. J. Physiol. Biochem. 2009, 65(4), 369-376.
13. Kennedy, A.; Overman, A.; Lapoint, K.; Hopkins, R.; West, T.; Chuang, C C.; Martinez, K.; Bell, D.; McIntosh, M. Conjugated linoleic acid-mediated inflammation and insulin resistance in human adipocytes are attenuated by resveratrol. J. Lipid Res. 2009, 50(2), 225-232.
14. Hsu, C. L.; Yen, G. C. Effects of capsaicin on induction of apoptosis and inhibition of adipogenesis in 3T3-L1 cells. J. Agric. Food Chem. 2007, 55(5), 1730-1736.
15. Kang, J. H.; Goto, T.; Han, I. S.; Kawada, T.; Kim, Y. M.; Yu, R. Dietary capsaicin reduces obesity-induced insulin resistance and hepatic steatosis in obese mice fed a high-fat diet. Obesity (Silver Spring) 2010, 18(4), 780-787.
16. Kang, J. H.; Kim, C. S.; Han, I. S.; Kawada, T.; Yu, R. Capsaicin, a spicy component of hot peppers, modulates adipokine gene expression and protein release from obese-mouse adipose tissues and isolated adipocytes, and suppresses the inflammatory responses of adipose tissue macrophages. FEBS Lett. 2007, 581(23), 4389-4396. (Pubitemid 47368195)
17. Yang, C. S.; Sang, S.; Lambert, J. D.; Lee, M. J. Bioavailability issues in studying the health effects of plant polyphenolic compounds. Mol. Nutr. Food Res. 2008, 52 (Suppl. 1), S139-S151.
18. Huang, Q.; Yu, H.; Ru, Q. Bioavailability and delivery of nutraceuticals using nanotechnology. J. Food Sci. 2010, 75(1), R50-R57.
19. Aggarwal, B. B.; Sundaram, C.; Malani, N.; Ichikawa, H. Curcumin: the Indian solid gold. Adv. Exp. Med. Biol. 2007, 595, 1-75.
20. Ravindran, J.; Prasad, S.; Aggarwal, B. B. Curcumin and cancer cells: how many ways can curry kill tumor cells selectively? AAPS J. 2009, 11(3), 495-510.
21. Sharma, R. A.; Euden, S. A.; Platton, S. L.; Cooke, D. N.; Shafayat, A.; Hewitt, H. R.; Marczylo, T. H.; Morgan, B.; Hemingway, D.; Plummer, S. M.; Pirmohamed, M.; Gescher, A. J.; Steward, W. P. Phase I clinical trial of oral curcumin: biomarkers of systemic activity and compliance. Clin. Cancer Res. 2004, 10(20), 6847-6854. (Pubitemid 39383033)
22. Steward, W. P.; Gescher, A. J. Curcumin in cancer management: recent results of analogue design and clinical studies and desirable future research. Mol. Nutr. Food Res. 2008, 52(9), 1005-1009.
23. Villegas, I.; Sanchez-Fidalgo, S.; Alarcon de la Lastra, C. New mechanisms and therapeutic potential of curcumin for colorectal cancer. Mol. Nutr. Food Res. 2008, 52(9), 1040-1061.
24. Jutooru, I.; Chadalapaka, G.; Lei, P.; Safe, S. Inhibition of NFκB and pancreatic cancer cell and tumor growth by curcumin is dependent on specificity protein down-regulation. J. Biol. Chem. 2010, 285(33), 25332-25344.
25. Montopoli, M.; Ragazzi, E.; Froldi, G.; Caparrotta, L. Cell-cycle inhibition and apoptosis induced by curcumin and cisplatin or oxaliplatin in human ovarian carcinoma cells. Cell Prolif. 2009, 42(2), 195-206.
26. Jagetia, G C.; Aggarwal, B. B. "Spicing up" of the immune system by curcumin. J. Clin. Immunol. 2007, 27(1), 19-35.
27. Weisberg, S. P.; Leibel, R.; Tortoriello, D. V. Dietary curcumin significantly improves obesity-associated inflammation and diabetes in mouse models of diabesity. Endocrinology 2008, 149(7), 3549-3558. (Pubitemid 351919581)
28. Asai, A.; Miyazawa, T. Dietary curcuminoids prevent high-fat dietinduced lipid accumulation in rat liver and epididymal adipose tissue. J. Nutr. 2001, 131(11), 2932-2935. (Pubitemid 33063126)
29. Seo, K. I.; Choi, M. S.; Jung, U. J.; Kim, H. J.; Yeo, J.; Jeon, S. M.; Lee, M. K. Effect of curcumin supplementation on blood glucose, plasma insulin, and glucose homeostasis related enzyme activities in diabetic db/db mice. Mol. Nutr. Food Res. 2008, 52(9), 995-1004.
30. Jang, E. M.; Choi, M. S.; Jung, U. J.; Kim, M. J.; Kim, H. J.; Jeon, S. M.; Shin, S. K.; Seong, C N.; Lee, M. K. Beneficial effects of curcumin on hyperlipidemia and insulin resistance in high-fat-fed hamsters. Metabolism 2008, 57(11), 1576-1583.
31. Ejaz, A.; Wu, D.; Kwan, P.; Meydani, M. Curcumin inhibits adipogenesis in 3T3-L1 adipocytes and angiogenesis and obesity in C57/BL mice. J. Nutr. 2009, 139(5), 919-925.
32. Ahn, J.; Lee, H.; Kim, S.; Ha, T. Curcumin-induced suppression of adipogenic differentiation is accompanied by activation of Wnt/β-catenin signaling. Am. J. Physiol. Cell Physiol. 2010, 298(6), C1510-C1516.
33. Kim, C Y.; Le, T. T.; Chen, C.; Cheng, J. X.; Kim, K. H. Curcumin inhibits adipocyte differentiation through modulation of mitotic clonal expansion. J. Nutr. Biochem. 2010, DOI: 10.1016/j.jnutbio. 2010.08.003.
34. Aggarwal, B. B.; Kumar, A.; Bharti, A. C. Anticancer potential of curcumin: preclinical and clinical studies. Anticancer Res. 2003, 23 (1A), 363-398. (Pubitemid 36361976)
35. Yen, F. L.; Wu, T. H.; Tzeng, C W.; Lin, L. T.; Lin, C. C. Curcumin nanoparticles improve the physicochemical properties of curcumin and effectively enhance its antioxidant and antihepatoma activities. J. Agric. Food Chem. 2010, 58(12), 7376-7382.
36. Mach, C. M.; Chen, J. H.; Mosley, S. A.; Kurzrock, R.; Smith, J. A. Evaluation of liposomal curcumin cytochrome p450 metabolism. Anticancer Res. 2010, 30(3), 811-814.
37. Takahashi, M.; Uechi, S.; Takara, K.; Asikin, Y.; Wada, K. Evaluation of an oral carrier system in rats: bioavailability and antioxidant properties of liposome-encapsulated curcumin. J. Agric. Food Chem. 2009, 57(19), 9141-9146.
38. Wang, F.; Wu, X.; Wang, F.; Liu, S.; Jia, Z.; Yang, J. The sensitive fluorimetric method for the determination of curcumin using the enhancement of mixed micelle. J. Fluorescence 2006, 16(1), 53-59.
39. Chin, S. F.; Iyer, K. S.; Saunders, M.; St. Pierre, T. G.; Buckley, C.; Paskevicius, M.; Raston, C. L. Encapsulation and sustained release of curcumin using superparamagnetic silica reservoirs. Chemistry 2009, 15(23), 5661-5665.
40. Suresh, D.; Srinivasan, K. Tissue distribution and elimination of capsaicin, piperine and curcumin following oral intake in rats. Indian J. Med. Res. 2010, 131, 682-691.
41. Dosio, F.; Arpicco, S.; Brusa, P.; Stella, B.; Cattel, L. Poly (ethylene glycol)-human serum albumin-paclitaxel conjugates: preparation, characterization and pharmacokinetics. J. Controlled Release 2001, 76 (1-2), 107-117. (Pubitemid 32786889)
42. Guerra-Tschuschke, I.; Martin, I.; Gonzalez, M. T. Polyethylene glycol-induced internalization of bacteria into fungal protoplasts: electron microscopic study and optimization of experimental conditions. Appl. Environ. Microbiol. 1991, 57(5), 1516-1522.
43. Sugiyama, A.; Sato, A.; Takeuchi, T. PEGylated lactoferrin enhanced its hepatoprotective effects on acute liver injury induced by carbon tetrachloride in rats. Food Chem. Toxicol. 2009, 47(7), 1453-1458.
44. Biasutto, L.; Marotta, E.; Mattarei, A.; Beltramello, S.; Caliceti, P.; Salmaso, S.; Bernkop-Schnurch, A.; Garbisa, S.; Zoratti, M.; Paradisi, C. Absorption and metabolism of resveratrol carboxyesters and methanesulfonate by explanted rat intestinal segments. Cell Physiol. Biochem. 2009, 24 (5-6), 557-566.
45. Liu, X.; Yu, B.; Wang, N.; Zhang, B.; Du, F.; He, C.; Ye, Z. A validated stability-indicating HPLC method for the determination of PEGylated puerarin in aqueous solutions. J, Chromatogr., B: Anal. Technol. Biomed. Life Sci. 2010, 878(23), 2061-2066.
46. Safavy, A.; Raisch, K. P.; Mantena, S.; Sanford, L. L.; Sham, S. W.; Krishna, N. R.; Bonner, J. A. Design and development of watersoluble curcumin conjugates as potential anticancer agents. J. Med. Chem. 2007, 50(24), 6284-6288.
47. Kunwar, A.; Barik, A.; Mishra, B.; Rathinasamy, K.; Pandey, R.; Priyadarsini, K. I. Quantitative cellular uptake, localization and cytotoxicity of curcumin in normal and tumor cells. Biochim. Biophys. Acta 2008, 1780(4), 673-679.
48. Anand, P.; Nair, H. B.; Sung, B.; Kunnumakkara, A. B.; Yadav, V. R.; Tekmal, R. R.; Aggarwal, B. B. Design of curcumin-loaded PLGA nanoparticles formulation with enhanced cellular uptake, and increased bioactivity in vitro and superior bioavailability in vivo. Biochem. Pharmacol. 2009, 79(3), 330-338.
49. Ryu, M. J.; Cho, M.; Song, J. Y.; Yun, Y. S.; Choi, I. W.; Kim, D. E.; Park, B. S.; Oh, S. Natural derivatives of curcumin attenuate the Wnt/β-catenin pathway through down-regulation of the transcriptional coactivator p300. Biochem. Biophys. Res. Commun. 2008, 377(4), 1304-1308.
50. Zhang, J.; Jinnai, S.; Ikeda, R.; Wada, M.; Hayashida, S.; Nakashima, K. A simple HPLC-fluorescence method for quantitation of curcuminoids and its application to turmeric products. Anal. Sci. 2009, 25(3), 385-388.
51. Schiborr, C.; Eckert, G P.; Rimbach, G.; Frank, J. A validated method for the quantification of curcumin in plasma and brain tissue by fast narrow-bore high-performance liquid chromatography with fluorescence detection. Anal. Bioanal. Chem. 2010, 397(5), 1917-1925.
52. Wang, Y. J.; Pan, M. H.; Cheng, A. L.; Lin, L. I.; Ho, Y. S.; Hsieh, C. Y.; Lin, J. K. Stability of curcumin in buffer solutions and characterization of its degradation products. J. Pharm. Biomed. Anal. 1997, 15(12), 1867-1876.
53. Oetari, S.; Sudibyo, M.; Commandeur, J. N.; Samhoedi, R.; Vermeulen, N. P. Effects of curcumin on cytochrome P450 and glutathione S-transferase activities in rat liver. Biochem. Pharmacol. 1996, 51(1), 39-45. (Pubitemid 26020677)
54. Garcea, G.; Jones, D. J.; Singh, R.; Dennison, A. R.; Farmer, P. B.; Sharma, R. A.; Steward, W. P.; Gescher, A. J.; Berry, D. P. Detection of curcumin and its metabolites in hepatic tissue and portal blood of patients following oral administration. Br. J. Cancer 2004, 90(5), 1011-1015. (Pubitemid 38499692)
55. Hoehle, S. I.; Pfeiffer, E.; Solyom, A. M.; Metzler, M. Metabolism of curcuminoids in tissue slices and subcellular fractions from rat liver. J. Agric. Food Chem. 2006, 54(3), 756-764. (Pubitemid 43274111)
56. Remaut, K.; Lucas, B.; Raemdonck, K.; Braeckmans, K.; Demeester, J.; De Smedt, S. C. Protection of oligonucleotides against enzymatic degradation by pegylated and nonpegylated branched polyethyleneimine. Biomacromolecules 2007, 8(4), 1333-1340. (Pubitemid 46672715)
57. Zhang, G.; Han, B.; Lin, X.; Wu, X.; Yan, H. Modification of antimicrobial peptide with low molar mass poly (ethylene glycol). J. Biochem. 2008, 144(6), 781-788.
58. Choudhuri, T.; Pal, S.; Das, T.; Sa, G. Curcumin selectively induces apoptosis in deregulated cyclin D1-expressed cells at G2 phase of cell cycle in a p53-dependent manner. J. Biol. Chem. 2005, 280(20), 20059-20068. (Pubitemid 41379535)
59. Fishburn, C. S. The pharmacology of PEGylation: balancing PD with PK to generate novel therapeutics. J. Pharm. Sci. 2008, 97(10), 4167-4183.
60. Gursahani, H.; Riggs-Sauthier, J.; Pfeiffer, J.; Lechuga-Ballesteros, D.; Fishburn, C. S. Absorption of polyethylene glycol (PEG) polymers: the effect of PEG size on permeability. J. Pharm. Sci. 2009, 98(8), 2847-2856.
61. Asada, H.; Douen, T.; Mizokoshi, Y.; Fujita, T.; Murakami, M.; Yamamoto, A.; Muranishi, S. Stability of acyl derivatives of insulin in the small intestine: relative importance of insulin association characteristics in aqueous solution. Pharm. Res. 1994, 11(8), 1115-1120. (Pubitemid 24259850)