Inhibition of adipogenesis and induction of apoptosis and lipolysis by stem bromelain in 3T3-L1 adipocytes

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Dave, Sandeep ^a   Kaur, Naval Jit ^a   Nanduri, Ravikanth ^a   Dkhar, H Kitdorlang ^a   Kumar, Ashwani ^a   Gupta, Pawan ^a  

^a INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADIPONECTIN; BROMELAIN; CCAAT ENHANCER BINDING PROTEIN ALPHA; CCAAT ENHANCER BINDING PROTEIN BETA; CD36 ANTIGEN; FATTY ACID BINDING PROTEIN 2; FATTY ACID SYNTHASE; HORMONE SENSITIVE LIPASE; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; LIPOPROTEIN LIPASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MESSENGER RNA; PERILIPIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHODIESTERASE III; PROTEIN KINASE B; RETINOIC ACID; STEM BROMELAIN; TUBERIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VITAMIN D; ANTILIPEMIC AGENT; CCAAT ENHANCER BINDING PROTEIN; CCAAT ENHANCER BINDING PROTEIN DELTA; CEBPA PROTEIN, MOUSE; CEBPB PROTEIN, MOUSE; CEBPD PROTEIN, MOUSE;

ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DIET SUPPLEMENTATION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; IN VITRO STUDY; LIPOLYSIS; METABOLIC INHIBITION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN SECRETION; UPREGULATION; ANIMAL; CELL STRAIN 3T3; DRUG EFFECT; EVALUATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ATRA;

3T3-L1 CELLS; ADIPOCYTES; ADIPOGENESIS; ANIMALS; APOPTOSIS; BROMELAINS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; CCAAT-ENHANCER-BINDING PROTEINS; CELL DIFFERENTIATION; DOWN-REGULATION; GENE EXPRESSION REGULATION; HYPOLIPIDEMIC AGENTS; LIPOLYSIS; MICE; PPAR GAMMA; UP-REGULATION;

EID: 84856158975     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030831     Document Type: Article

References (70)

1. Spiegelman BM, Flier JS, (1996) Adipogenesis and obesity: rounding out the big picture. Cell 87: 377-389.
2. Spiegelman BM, Flier JS, (2001) Obesity and the regulation of energy balance. Cell 104: 531-543.
3. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, et al. (2001) The hormone resistin links obesity to diabetes. Nature 409: 307-312.
4. Kopelman PG, (2000) Obesity as a medical problem. Nature 404: 635-643.
5. Green H, Kehinde O, (1975) An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell 5: 19-27.
6. Hirsch J, Han PW, (1969) Cellularity of rat adipose tissue: effects of growth, starvation, and obesity. J Lipid Res 10: 77-82.
7. Roncari DA, Lau DC, Kindler S, (1981) Exaggerated replication in culture of adipocyte precursors from massively obese persons. Metabolism 30: 425-427.
8. Tang QQ, Lane MD, (1999) Activation and centromeric localization of CCAAT/enhancer-binding proteins during the mitotic clonal expansion of adipocyte differentiation. Genes Dev 13: 2231-2241.
9. Altiok S, Xu M, Spiegelman BM, (1997) PPARgamma induces cell cycle withdrawal: inhibition of E2F/DP DNA-binding activity via down-regulation of PP2A. Genes Dev 11: 1987-1998.
10. Wang H, Iakova P, Wilde M, Welm A, Goode T, et al. (2001) C/EBPalpha arrests cell proliferation through direct inhibition of Cdk2 and Cdk4. Mol Cell 8: 817-828.
11. Farmer SR, (2006) Transcriptional control of adipocyte formation. Cell Metab 4: 263-273.
12. Zhang HH, Huang J, Duvel K, Boback B, Wu S, et al. (2009) Insulin stimulates adipogenesis through the Akt-TSC2-mTORC1 pathway. PLoS One 4: e6189.
13. Alkhouri N, Gornicka A, Berk MP, Thapaliya S, Dixon LJ, et al. (2010) Adipocyte apoptosis, a link between obesity, insulin resistance, and hepatic steatosis. J Biol Chem 285: 3428-3438.
14. De Smet PA, (2002) Herbal remedies. N Engl J Med 347: 2046-2056.
15. Feldmann M, (2008) Many cytokines are very useful therapeutic targets in disease. J Clin Invest 118: 3533-3536.
16. Rodrigo R, Guichard C, Charles R, (2007) Clinical pharmacology and therapeutic use of antioxidant vitamins. Fundam Clin Pharmacol 21: 111-127.
17. Lee J, Jung E, Kim S, Huh S, Kim Y, et al. (2009) Isorhamnetin represses adipogenesis in 3T3-L1 cells. Obesity (Silver Spring) 17: 226-232.
18. Moon HS, Chung CS, Lee HG, Kim TG, Choi YJ, et al. (2007) Inhibitory effect of (-)-epigallocatechin-3-gallate on lipid accumulation of 3T3-L1 cells. Obesity (Silver Spring) 15: 2571-2582.
19. Ka SO, Kim KA, Kwon KB, Park JW, Park BH, (2009) Silibinin attenuates adipogenesis in 3T3-L1 preadipocytes through a potential upregulation of the insig pathway. Int J Mol Med 23: 633-637.
20. Berry DC, Noy N, (2009) All-trans-retinoic acid represses obesity and insulin resistance by activating both peroxisome proliferation-activated receptor beta/delta and retinoic acid receptor. Mol Cell Biol 29: 3286-3296.
21. Kong J, Li YC, (2006) Molecular mechanism of 1,25-dihydroxyvitamin D3 inhibition of adipogenesis in 3T3-L1 cells. Am J Physiol Endocrinol Metab 290: E916-924.
22. Vanhoof G, Cooreman W, (1997) Bromelain. In: Lauwers A, Scharpé S, editors. Pharmaceutical Enzymes New York Marcel Dekker Inc pp. 131-154.
23. Yuan G, Wahlqvist ML, He G, Yang M, Li D, (2006) Natural products and anti-inflammatory activity. Asia Pac J Clin Nutr 15: 143-152.
24. Maurer HR, (2001) Bromelain: biochemistry, pharmacology and medical use. Cell Mol Life Sci 58: 1234-1245.
25. Mynott TL, Ladhams A, Scarmato P, Engwerda CR, (1999) Bromelain, from pineapple stems, proteolytically blocks activation of extracellular regulated kinase-2 in T cells. J Immunol 163: 2568-2575.
26. Barnwell SG, (1998) Medical application of bromelain. In: patent US, editors. United Kingdom Cortecs Limited United Kingdom pp. 1-6.
27. Hale LP, Haynes BF, (1992) Bromelain treatment of human T cells removes CD44, CD45RA, E2/MIC2, CD6, CD7, CD8, and Leu 8/LAM1 surface molecules and markedly enhances CD2-mediated T cell activation. J Immunol 149: 3809-3816.
28. Dave S, Dkhar HK, Singh MP, Gupta G, Chandra V, et al. (2010) Hexafluoroisopropanol-induced helix-sheet transition of stem bromelain: correlation to function. Int J Biochem Cell Biol 42: 938-947.
29. Kalra N, Bhui K, Roy P, Srivastava S, George J, et al. (2008) Regulation of p53, nuclear factor kappaB and cyclooxygenase-2 expression by bromelain through targeting mitogen-activated protein kinase pathway in mouse skin. Toxicol Appl Pharmacol 226: 30-37.
30. Grabovac V, Bernkop-Schnurch A, (2006) Improvement of the intestinal membrane permeability of low molecular weight heparin by complexation with stem bromelain. Int J Pharm 326: 153-159.
31. Seifert J, Ganser R, Brendel W, (1979) [Absorption of a proteolytic enzyme originating from plants out of the gastro-intestinal tract into blood and lymph of rats (author's transl)]. Z Gastroenterol 17: 1-8.
32. White RR, Crawley FE, Vellini M, Rovati LA, (1988) Bioavailability of 125I bromelain after oral administration to rats. Biopharm Drug Dispos 9: 397-403.
33. Castell JV, Friedrich G, Kuhn CS, Poppe GE, (1997) Intestinal absorption of undegraded proteins in men: presence of bromelain in plasma after oral intake. Am J Physiol 273: G139-146.
34. Fujisaki S, Fujisaki T, Yoshida J, Fujisaki Y, (1984) Preventive and treating agent for blood lipids abnormality and/or arteriosclerosis. In: patent US, editors. Tokyo, Japan Japan: Kaken Pharmaceutical Co., Ltd. pp. 1-4.
35. Maurer R, Eckert K, Grabowska E, Eschmann K, (2004) US6803038: Use of bromelaine proteases for inhibiting blood coagulation. United States of America Ursapharm Arzneimittel GmbH Germany pp. 1-6.
36. Mynott TL, (1998) US5824305: Method of treating diseases mediated by cyclic nucleotide pathways with purified stem bromelain protease. In: Patent U, editors. United States of America Cortecs (UK) Limited United Kingdom pp. 1-16.
37. Suryawan A, Hu CY, (1993) Effect of serum on differentiation of porcine adipose stromal-vascular cells in primary culture. Comp Biochem Physiol Comp Physiol 105: 485-492.
38. Ioannou YA, Chen FW, (1996) Quantitation of DNA fragmentation in apoptosis. Nucleic Acids Res 24: 992-993.
39. Xie S, Lee YF, Kim E, Chen LM, Ni J, et al. (2009) TR4 nuclear receptor functions as a fatty acid sensor to modulate CD36 expression and foam cell formation. Proc Natl Acad Sci U S A 106: 13353-13358.
40. Tontonoz P, Nagy L, Alvarez JG, Thomazy VA, Evans RM, (1998) PPARgamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93: 241-252.
41. Gupta P, Park SW, Farooqui M, Wei LN, (2007) Orphan nuclear receptor TR2, a mediator of preadipocyte proliferation, is differentially regulated by RA through exchange of coactivator PCAF with corepressor RIP140 on a platform molecule GRIP1. Nucleic Acids Res 35: 2269-2282.
42. Gupta P, Khan RH, Saleemuddin M, (2003) Induction of 'molten globule' like state in acid-denatured state of unmodified preparation of stem bromelain: implications of disulfides in protein folding. Int J Biol Macromol 33: 167-174.
43. Gupta P, Khan RH, Saleemuddin M, (2003) Binding of antibromelain monomeric Fab' improves the stability of stem bromelain against inactivation. Biochim Biophys Acta 1646: 131-135.
44. Tang QQ, Otto TC, Lane MD, (2003) Mitotic clonal expansion: a synchronous process required for adipogenesis. Proc Natl Acad Sci U S A 100: 44-49.
45. Manning BD, Cantley LC, (2007) AKT/PKB signaling: navigating downstream. Cell 129: 1261-1274.
46. Alessi MC, Lijnen HR, Bastelica D, Juhan-Vague I, (2003) Adipose tissue and atherothrombosis. Pathophysiol Haemost Thromb 33: 290-297.
47. Tang QQ, Otto TC, Lane MD, (2003) CCAAT/enhancer-binding protein beta is required for mitotic clonal expansion during adipogenesis. Proc Natl Acad Sci U S A 100: 850-855.
48. Wan X, Kong J, Li YC, (2001) Protein kinase C is involved in the regulation of hairless mRNA expression during mouse keratinocyte differentiation. Biochem Biophys Res Commun 284: 99-105.
49. Yanagiya T, Tanabe A, Hotta K, (2007) Gap-junctional communication is required for mitotic clonal expansion during adipogenesis. Obesity (Silver Spring) 15: 572-582.
50. Hassan M, El Yazidi C, Landrier JF, Lairon D, Margotat A, et al. (2007) Phloretin enhances adipocyte differentiation and adiponectin expression in 3T3-L1 cells. Biochem Biophys Res Commun 361: 208-213.
51. Kawaji A, Ohnaka Y, Osada S, Nishizuka M, Imagawa M, (2010) Gelsolin, an actin regulatory protein, is required for differentiation of mouse 3T3-L1 cells into adipocytes. Biol Pharm Bull 33: 773-779.
52. Bhui K, Tyagi S, Srivastava AK, Singh M, Roy P, et al. (2011) Bromelain inhibits nuclear factor kappa-B translocation, driving human epidermoid carcinoma A431 and melanoma A375 cells through G(2)/M arrest to apoptosis. Mol Carcinog.
53. Ozes ON, Mayo LD, Gustin JA, Pfeffer SR, Pfeffer LM, et al. (1999) NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401: 82-85.
54. Barth H, Guseo A, Klein R, (2005) In vitro study on the immunological effect of bromelain and trypsin on mononuclear cells from humans. Eur J Med Res 10: 325-331.
55. Engwerda CR, Andrew D, Murphy M, Mynott TL, (2001) Bromelain activates murine macrophages and natural killer cells in vitro. Cell Immunol 210: 5-10.
56. Prins JB, O'Rahilly S, (1997) Regulation of adipose cell number in man. Clin Sci (Lond) 92: 3-11.
57. Schultz DR, Harrington WJ Jr, (2003) Apoptosis: programmed cell death at a molecular level. Semin Arthritis Rheum 32: 345-369.
58. Tamai M, Shimada T, Hiramatsu N, Hayakawa K, Okamura M, et al. Selective deletion of adipocytes, but not preadipocytes, by TNF-alpha through C/EBP- and PPARgamma-mediated suppression of NF-kappaB. Lab Invest 90: 1385-1395.
59. Xing H, Northrop JP, Grove JR, Kilpatrick KE, Su JL, et al. (1997) TNF alpha-mediated inhibition and reversal of adipocyte differentiation is accompanied by suppressed expression of PPARgamma without effects on Pref-1 expression. Endocrinology 138: 2776-2783.
60. Ryden M, Arvidsson E, Blomqvist L, Perbeck L, Dicker A, et al. (2004) Targets for TNF-alpha-induced lipolysis in human adipocytes. Biochem Biophys Res Commun 318: 168-175.
61. Prins JB, Niesler CU, Winterford CM, Bright NA, Siddle K, et al. (1997) Tumor necrosis factor-alpha induces apoptosis of human adipose cells. Diabetes 46: 1939-1944.
62. Arimura N, Horiba T, Imagawa M, Shimizu M, Sato R, (2004) The peroxisome proliferator-activated receptor gamma regulates expression of the perilipin gene in adipocytes. J Biol Chem 279: 10070-10076.
63. Souza SC, de Vargas LM, Yamamoto MT, Lien P, Franciosa MD, et al. (1998) Overexpression of perilipin A and B blocks the ability of tumor necrosis factor alpha to increase lipolysis in 3T3-L1 adipocytes. J Biol Chem 273: 24665-24669.
64. Rahn Landstrom T, Mei J, Karlsson M, Manganiello V, Degerman E, (2000) Down-regulation of cyclic-nucleotide phosphodiesterase 3B in 3T3-L1 adipocytes induced by tumour necrosis factor alpha and cAMP. Biochem J 346 Pt 2: 337-343.
65. Gasic S, Tian B, Green A, (1999) Tumor necrosis factor alpha stimulates lipolysis in adipocytes by decreasing Gi protein concentrations. J Biol Chem 274: 6770-6775.
66. Xue JC, Schwarz EJ, Chawla A, Lazar MA, (1996) Distinct stages in adipogenesis revealed by retinoid inhibition of differentiation after induction of PPARgamma. Mol Cell Biol 16: 1567-1575.
67. Villarroya F, Giralt M, Iglesias R, (1999) Retinoids and adipose tissues: metabolism, cell differentiation and gene expression. Int J Obes Relat Metab Disord 23: 1-6.
68. Padwal RS, Majumdar SR, (2007) Drug treatments for obesity: orlistat, sibutramine, and rimonabant. Lancet 369: 71-77.
69. Chapman MJ, (2003) Fibrates in 2003: therapeutic action in atherogenic dyslipidaemia and future perspectives. Atherosclerosis 171: 1-13.
70. Bray GA, (2001) Drug treatment of obesity. Rev Endocr Metab Disord 2: 403-418.