Lycopene attenuates LPS-induced TNF-α secretion in macrophages and inflammatory markers in adipocytes exposed to macrophage-conditioned media

Molecular Nutrition and Food Research

Volumn 56, Issue 5, 2012, Pages 725-732

  Marcotorchino, Julie ^a,b   Romier, Beatrice ^a,b   Gouranton, Erwan ^a,b   Riollet, Celine ^a,b   Gleize, Beatrice ^a,b   Malezet Desmoulins, Christiane ^a,b   Landrier, Jean François ^a,b  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Adipocyte; Cytokines; Inflammation; Lycopene; Macrophage

Indexed keywords

BIOLOGICAL MARKER; CAROTENOID; CHEMOKINE; CYTOKINE; LIPOPOLYSACCHARIDE; LYCOPENE; NONSTEROID ANTIINFLAMMATORY AGENT; TUMOR NECROSIS FACTOR ALPHA;

ADIPOCYTE; ANIMAL; ARTICLE; CELL CULTURE; CELL MOTION; CELL STRAIN 3T3; CULTURE MEDIUM; DRUG EFFECT; GENETICS; INFLAMMATION; MACROPHAGE; METABOLISM; MOUSE; SECRETION (PROCESS); SIGNAL TRANSDUCTION;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BIOLOGICAL MARKERS; CAROTENOIDS; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINES; CULTURE MEDIA, CONDITIONED; CYTOKINES; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MICE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84861692997     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201100623     Document Type: Article

References (45)

1. Rao, A. V., Ray, M. R., Rao, L. G., Lycopene. Adv. Food Nutr. Res. 2006, 51, 99-164.
2. Krinsky, N. I., Johnson, E. J., Carotenoid actions and their relation to health and disease. Mol. Aspects Med. 2005, 26, 459-516.
3. Joo, Y. E., Karrasch, T., Muhlbauer, M., Allard, B., et al., Tomato lycopene extract prevents lipopolysaccharide-induced NF-kappaB signaling but worsens dextran sulfate sodium-induced colitis in NF-kappaBEGFP mice. PLoS One 2009, 4, e4562.
4. Bignotto, L., Rocha, J., Sepodes, B., Eduardo-Figueira, M., et al., Anti-inflammatory effect of lycopene on carrageenan-induced paw oedema and hepatic ischaemia-reperfusion in the rat. Br. J. Nutr. 2009, 102, 126-133.
5. Hung, C. F., Huang, T. F., Chen, B. H., Shieh, J. M., et al., Lycopene inhibits TNF-alpha-induced endothelial ICAM-1 expression and monocyte-endothelial adhesion. Eur. J. Pharmacol. 2008, 586, 275-282.
6. Feng, D., Ling, W. H., Duan, R. D., Lycopene suppresses LPS-induced NO and IL-6 production by inhibiting the activation of ERK, p38MAPK, and NF-kappaB in macrophages. Inflamm. Res. 2010, 59, 115-121.
7. Gouranton, E., Thabuis, C., Riollet, C., Malezet-Desmoulins, C., et al., Lycopene inhibits proinflammatory cytokine and chemokine expression in adipose tissue. J. Nutr. Biochem. 2011, 22, 642-648.
8. Palozza, P., Parrone, N., Catalano, A., Simone, R., Tomato lycopene and inflammatory cascade: basic interactions and clinical implications. Curr. Med. Chem. 2010, 17, 2547-2563.
9. Simone, R. E., Russo, M., Catalano, A., Monego, G., et al., Lycopene inhibits NF-kB-mediated IL-8 expression and changes Redox and PPARgamma signaling in cigarette smoke-stimulated macrophages. PLoS One 2011, 6, e19652.
10. Chung, H. Y., Ferreira, A. L., Epstein, S., Paiva, S. A., et al., Site-specific concentrations of carotenoids in adipose tissue: relations with dietary and serum carotenoid concentrations in healthy adults. Am. J. Clin. Nutr. 2009, 90, 533-539.
11. Moussa, M., Gouranton, E., Gleize, B., Yazidi, C. E., et al., CD36 is involved in lycopene and lutein uptake by adipocytes and adipose tissue cultures. Mol. Nutr. Food Res. 2011, 55, 578-584.
12. Gouranton, E., Yazidi, C. E., Cardinault, N., Amiot, M. J., et al., Purified low-density lipoprotein and bovine serum albumin efficiency to internalise lycopene into adipocytes. Food Chem. Toxicol. 2008, 46, 3832-3836.
13. Tourniaire, F., Gouranton, E., von Lintig, J., Keijer, J., et al., Beta-carotene conversion products and their effects on adipose tissue. Genes. Nutr. 2009, 4, 179-187.
14. Lobo, G. P., Amengual, J., Li, H. N., Golczak, M., et al., Beta, beta-carotene decreases peroxisome proliferator receptor gamma activity and reduces lipid storage capacity of adipocytes in a beta, beta-carotene oxygenase 1-dependent manner. J. Biol. Chem. 2010, 285, 27891-27899.
15. Amengual, J., Gouranton, E., van Helden, Y. G., Hessel, S., et al., Beta-carotene reduces body adiposity of mice via BCMO1. PLoS One 2011, 6, e20644.
16. Sluijs, I., Beulens, J. W., Grobbee, D. E., van der Schouw, Y. T., Dietary carotenoid intake is associated with lower prevalence of metabolic syndrome in middle-aged and elderly men. J. Nutr. 2009, 139, 987-992.
17. Gouranton, E., Aydin, G., Reynault, E., Malezet, C., et al., Apo-10́-lycopenoic acid is an active metabolite of lycopene in adipose tissue. H. Biochim. Biophys. Act. 2011, 1811, 1105-1114.
18. Gregor, M. F., Hotamisligil, G. S., Inflammatory mechanisms in obesity. Annu. Rev. Immunol. 2011, 29, 415-445.
19. Hotamisligil, G. S., Inflammation and metabolic disorders. Nature. 2006, 444, 860-867.
20. Bourlier, V., Bouloumie, A., Role of macrophage tissue infiltration in obesity and insulin resistance. Diabetes Metab. 2009, 35, 251-260.
21. Olefsky, J. M., Glass, C. K., Macrophages, inflammation, and insulin resistance. Annu. Rev. Physiol. 2010, 72, 219-246.
22. Suganami, T., Nishida, J., Ogawa, Y., A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor alpha. Arterioscler. Thromb. Vasc. Biol. 2005, 25, 2062-2068.
23. Landrier, J. F., Gouranton, E., El Yazidi, C., Malezet, C., et al., Adiponectin expression is induced by vitamin E via a peroxisome proliferator-activated receptor gamma-dependent mechanism. Endocrinology. 2009, 150, 5318-5325.
24. Landrier, J. F., Gouranton, E., Reboul, E., et al., Vitamin E decreases endogenous cholesterol synthesis and apo-AI-mediated cholesterol secretion in Caco-2 cells. J. Nutr. Biochem. 2010, 21, 1207-1213.
25. Landrier, J. F., Malezet-Desmoulins, C., Reboul, E., Lorec, M. A., et al., Comparison of different vehicles to study the effect of tocopherols on gene expression in intestinal cells. Free Radic. Res. 2008, 42, 523-530.
26. Romier, B., Van De Walle, J., During, A., Larondelle, Y., et al., Modulation of signalling nuclear factor-kappaB activation pathway by polyphenols in human intestinal Caco-2 cells. Br. J. Nutr. 2008, 100, 542-551.
27. Hassan, M., El Yazidi, C., Landrier, J. F., Lairon, D., et al., Phloretin enhances adipocyte differentiation and adiponectin expression in 3T3-L1 cells. Biochem. Biophys. Res. Commun. 2007, 361, 208-213.
28. Cani, P. D., Amar, J., Iglesias, M. A., Poggi, M., et al., Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007, 56, 1761-1772.
29. Cani, P. D., Bibiloni, R., Knauf, C., Waget, A., et al., Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008, 57, 1470-1481.
30. Allen, C. M., Schwartz, S. J., Craft, N. E., Giovannucci, E. L., et al., Changes in plasma and oral mucosal lycopene isomer concentrations in healthy adults consuming standard servings of processed tomato products. Nutr. Cancer 2003, 47, 48-56.
31. Fain, J. N., Madan, A. K., Hiler, M. L., Cheema, P., et al., Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 2004, 145, 2273-2282.
32. 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-alpha, overexpressed in human fat cells from insulin-resistant subjects. J. Biol. Chem. 2003, 278, 45777-45784.
33. Jager, J., Gremeaux, T., Cormont, M., Le Marchand-Brustel, Y., et al., Interleukin-1beta-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology 2007, 148, 241-251.
34. Ishizuka, K., Usui, I., Kanatani, Y., Bukhari, A., et al., Chronic tumor necrosis factor-alpha treatment causes insulin resistance via insulin receptor substrate-1 serine phosphorylation and suppressor of cytokine signaling-3 induction in 3T3-L1 adipocytes. Endocrinology 2007, 148, 2994-3003.
35. Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., et al., Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112, 1796-1808.
36. Xu, H., Barnes, G. T., Yang, Q., Tan, G., et al., Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 2003, 112, 1821-1830.
37. Rafi, M. M., Yadav, P. N., Reyes, M., Lycopene inhibits LPS-induced proinflammatory mediator inducible nitric oxide synthase in mouse macrophage cells. J. Food. Sci. 2007, 72, S069-S074.
38. Lara-Castro, C., Fu, Y., Chung, B. H., Garvey, W. T., Adiponectin and the metabolic syndrome: mechanisms mediating risk for metabolic and cardiovascular disease. Curr. Opin. Lipidol. 2007, 18, 263-270.
39. Filippin-Monteiro, F. B., de Oliveira, E. M., Sandri, S., Knebel, F. H., et al., Serum amyloid A is a growth factor for 3T3-L1 adipocytes, inhibits differentiation and promotes insulin resistance. Int. J. Obes. (Lond). 2011. doi:10.1038/ijo.2011.193. [Epub ahead of print].
40. Keophiphath, M., Rouault, C., Divoux, A., Clement, K., et al., CCL5 promotes macrophage recruitment and survival in human adipose tissue. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 39-45.
41. Yamashita, A., Soga, Y., Iwamoto, Y., Asano, T., et al., DNA microarray analyses of genes expressed differentially in 3T3-L1 adipocytes co-cultured with murine macrophage cell line RAW 264.7 in the presence of the toll-like receptor 4 ligand bacterial endotoxin. Int. J. Obes. 2008, 32, 1725-1729.
42. McCall, K. D., Holliday, D., Dickerson, E., Wallace, B., et al., Phenylmethimazole blocks palmitate-mediated induction of inflammatory cytokine pathways in 3T3L1 adipocytes and RAW 264.7 macrophages. J. Endocrinol. 2010, 207, 343-353.
43. Maffei, M., Funicello, M., Vottari, T., Gamucci, O., et al., The obesity and inflammatory marker haptoglobin attracts monocytes via interaction with chemokine (C-C motif) receptor 2 (CCR2). BMC Biol. 2009, 7, 87.
44. Maquoi, E., Munaut, C., Colige, A., Collen, D., et al., Modulation of adipose tissue expression of murine matrix metalloproteinases and their tissue inhibitors with obesity. Diabetes 2002, 51, 1093-1101.
45. O'Hara A, Lim, F. L., Mazzatti, D. J., Trayhurn, P., Microarray analysis identifies matrix metalloproteinases (MMPs) as key genes whose expression is up-regulated in human adipocytes by macrophage-conditioned medium. Pflugers Arch. 2009, 458, 1103-1114.