[en] We revisited the action of a carotenoid, the lycopene, on the expression of proinflammatory genes, reactive oxygen species (ROS) production, and metalloprotease (MMP9) activity. THP1 and Caco2 cell lines were used as in vitro models for the two main cell types found in intestine tissue, that is, monocytes and epithelial cells. Proinflammatory condition was induced using either phorbol ester acetate (PMA), lipopolysaccharide (LPS) or tumor necrosis factor (TNF). In THP1 cells, short term pretreatment (2 h) with a low concentration (2 muM) of lycopene reinforce proinflammatory gene expression. The extent of the effect of lycopene is dependent on the proinflammtory stimulus (PMA, LPS or TNF) used. Lycopene enhanced MMP9 secretion via a c-AMP-dependent process, and reduced ROS production at higher concentrations than 2 muM. Cell culture media, conditioned by PMA-treated monocytes and then transferred on CaCo-2 epithelial cells, induced a proinflammatory state in these cells. The extent of this inflammatory effect was reduced when cells has been pretreated (12 h) with lycopene. At low concentration (2 muM or less), lycopene appeared to promote an inflammatory state not correlated with ROS modulation. At higher concentration (5 muM-20 muM), an anti-inflammatory effect takes place as a decrease of ROS production was detected. So, both concentration and time have to be considered in order to define the exact issue of the effect of carotenoids present in meals.
Disciplines :
Endocrinology, metabolism & nutrition
Author, co-author :
Njock, Makon-Sébastien ; Laboratoire de Génie Génétique, Faculté de Pharmacie, Aix-Marseille Université, 27 boulevard Jean Moulin, 13385 Marseille, France ; Advanced Diagnostics, Toronto General Research Institute, University Health Network, 101 College Street, TMDT, Rm. 3-301, Toronto, ON, Canada M5G 1L7
Fouchier, Francis; Laboratoire de Génie Génétique, Faculté de Pharmacie, Aix-Marseille Université, 27 boulevard Jean Moulin, 13385 Marseille, France
Seree, Eric; Laboratoire de Génie Génétique, INRA 1260, Faculté de Pharmacie, 27 boulevard Jean Moulin, 13385 Marseille Cedex 5, France
Villard Pierre, Henry; IMBE-UMR CNRS 7263/IRD 237, Mutagenèse Environnementale, Faculté de Pharmacie, Aix-Marseille Université, 27 boulevard Jean Moulin, 13385 Marseille, France
Landrier Jean, Francois; INRA, UMR1260/1062 INSERM/AMU, Nutrition, Obésité et Risque Thrombotique, 27 boulevard Jean Moulin, 13385 Marseille, France
Pechere, Laurent; Laboratoires YVERY, 134 rue Edmond Rostand, 13008 Marseille, France
Barra, Yves; Laboratoire de Génie Génétique, Faculté de Pharmacie, Aix-Marseille Université, 27 boulevard Jean Moulin, 13385 Marseille, France
Champion, Serge; IMBE-UMR CNRS 7263/IRD 237, Mutagenèse Environnementale, Faculté de Pharmacie, Aix-Marseille Université, 27 boulevard Jean Moulin, 13385 Marseille, France
Language :
English
Title :
Lycopene modulates THP1 and Caco2 cells inflammatory state through transcriptional and nontranscriptional processes.
Gerster, H., Anticarcinogenic effect of common carotenoids (1993) International Journal for Vitamin and Nutrition Research, 63 (2), pp. 93-121. , 2-s2.0-0027346190
Van Poppel, G., Goldbohm, R.A., Epidemiologic evidence for β -carotene and cancer prevention (1995) The American Journal of Clinical Nutrition, 62 (6 SUPPL.), pp. 1393S-1402S. , 2-s2.0-0028863736
Heinonen, O.P., Albanes, D., The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers (1994) New England Journal of Medicine, 330 (15), pp. 1029-1035. , DOI 10.1056/NEJM199404143301501
Canene-Adams, K., Campbell, J.K., Zaripheh, S., Jeffery, E.H., Erdman Jr., J.W., The tomato as a functional food (2005) Journal of Nutrition, 135 (5), pp. 1226-1230
Levy, J., Bosin, E., Feldman, B., Giat, Y., Miinster, A., Danilenko, M., Sharoni, Y., Lycopene is a more potent inhibitor of human cancer cell proliferation than either α -carotene or β -carotene (1995) Nutrition and Cancer, 24 (3), pp. 257-266. , 2-s2.0-0028863013
Bhuvaneswari, V., Nagini, S., Lycopene: A review of its potential as an anticancer agent (2005) Current Medicinal Chemistry - Anti-Cancer Agents, 5 (6), pp. 627-635
Chalabi, N., Le Corre, L., Maurizis, J.-C., Bignon, Y.-J., Bernard-Gallon, D.J., The effects of lycopene on the proliferation of human breast cells and BRCA1 and BRCA2 gene expression (2004) European Journal of Cancer, 40 (11), pp. 1768-1775. , DOI 10.1016/j.ejca.2004.03.028, PII S0959804904003429
Chalabi, N., Delort, L., Satih, S., Dechelotte, P., Bignon, Y.-J., Bernard-Gallon, D.J., Immunohistochemical expression of RARα, RARβ, and Cx43 in breast tumor cell lines after treatment with lycopene and correlation with RT-QPCR (2007) Journal of Histochemistry and Cytochemistry, 55 (9), pp. 877-883. , DOI 10.1369/jhc.7A7185.2007
Chalabi, N., Delort, L., Le Corre, L., Satih, S., Bignon, Y.J., Bernard-Gallon, D., Gene signature of breast cancer cell lines treated with lycopene (2006) Pharmacogenomics, 7 (5), pp. 663-672. , http://www.futuremedicine.com/doi/full/10.2217/14622416.7.5.663, DOI 10.2217/14622416.7.5.663
Cousins, R.J., Nutritional regulation of gene expression (1999) American Journal of Medicine, 106 (1), pp. 20S-23S. , PII S0002934399003428
Hesketh, J.E., Vasconcelos, M.H., Bermano, G., Regulatory signals in messenger RNA: Determinants of nutrient-gene interaction and metabolic compartmentation (1998) British Journal of Nutrition, 80 (4), pp. 307-321
Salati, L.M., Szeszel-Fedorowicz, W., Tao, H., Gibson, M.A., Amir-Ahmady, B., Stabile, L.P., Hodge, D.L., Nutritional regulation of mRNA processing (2004) Journal of Nutrition, 134 (9), pp. 2437S-2443S
Stahl, W., Nicolai, S., Briviba, K., Hanusch, M., Broszeit, G., Peters, M., Martin, H.-D., Sies, H., Biological activities of natural and synthetic carotenoids: Induction of gap junctional communication and singlet oxygen quenching (1997) Carcinogenesis, 18 (1), pp. 89-92. , DOI 10.1093/carcin/18.1.89
Zhang, L.-X., Cooney, R.V., Bertram, J.S., Carotenoids up-regulate connexin43 gene expression independent of their provitamin A or antioxidant properties (1992) Cancer Research, 52 (20), pp. 5707-5712. , 2-s2.0-0026675706
Zhang, L.-X., Cooney, R.V., Bertram, J.S., Carotenoids enhance gap junctional communication and inhibit lipid peroxidation in C3H/10T1/2 cells: Relationship to their cancer chemopreventive action (1991) Carcinogenesis, 12 (11), pp. 2109-2114. , 2-s2.0-0025955567
Bertram, J.S., Pung, A., Churley, M., Kappock, T.J.I.V., Wilkins, L.R., Cooney, R.V., Diverse carotenoids protect against chemically induced neoplastic transformation (1991) Carcinogenesis, 12 (4), pp. 671-678. , 2-s2.0-0025753537
Nahum, A., Hirsch, K., Danilenko, M., Watts, C.K.W., Prall, O.W.J., Levy, J., Sharoni, Y., Lycopene inhibition of cell cycle progression in breast and endometrial cancer cells is associated with reduction in cyclin D levels and retention of p27Kip1 in the cyclin E-cdk2 complexes (2001) Oncogene, 20 (26), pp. 3428-3436. , DOI 10.1038/sj.onc.1204452
Gouranton, E., Aydemir, G., Reynaud, E., Marcotorchino, J., Malezet, C., Caris-Veyrat, C., Blomhoff, R., Rühl, R., Apo-10′ -lycopenoic acid impacts adipose tissue biology via the retinoic acid receptors (2011) Biochimica et Biophysica Acta, 1811 (12), pp. 1105-1114. , 2-s2.0-80155161346 10.1016/j.bbalip.2011.09.002
Gouranton, E., Thabuis, C., Riollet, C., Malezet-Desmoulins, C., El Yazidi, C., Amiot, M.J., Borel, P., Landrier, J.F., Lycopene inhibits proinflammatory cytokine and chemokine expression in adipose tissue (2011) Journal of Nutritional Biochemistry, 22 (7), pp. 642-648. , 2-s2.0-79958791073 10.1016/j.jnutbio.2010.04.016
Marcotorchino, J., Romier, B., Gouranton, E., Lycopene attenuates LPS-induced TNF-alpha secretion in macrophages and inflammatory markers in adipocytes exposed to macrophage-conditioned media (2012) Molecular Nutrition & Food Research, 56 (5), pp. 725-732. , 10.1002/mnfr.201100623
Huang, C.-S., Fan, Y.-E., Lin, C.-Y., Hu, M.-L., Lycopene inhibits matrix metalloproteinase-9 expression and down-regulates the binding activity of nuclear factor-kappa B and stimulatory protein-1 (2007) Journal of Nutritional Biochemistry, 18 (7), pp. 449-456. , DOI 10.1016/j.jnutbio.2006.08.007, PII S0955286306001914
Cellier, C., Cervoni, J.-P., Patey, N., Barbier, J.-P., Brousse, N., Adhesion molecules and inflammatory bowel disease (1997) Gastroenterologie Clinique et Biologique, 21 (11), pp. 832-842
Gan, X., Wong, B., Wright, S.D., Cai, T.-Q., Production of matrix metalloproteinase-9 in CaCO-2 cells in response to inflammatory stimuli (2001) Journal of Interferon and Cytokine Research, 21 (2), pp. 93-98. , DOI 10.1089/107999001750069953
Scott, K.A., Arnott, C.H., Robinson, S.C., Moore, R.J., Thompson, R.G., Marshall, J.F., Balkwill, F.R., TNF-α regulates epithelial expression of MMP-9 and integrin αvβ6 during tumour promotion. A role for TNF-α in keratinocyte migration? (2004) Oncogene, 23 (41), pp. 6954-6966. , DOI 10.1038/sj.onc.1207915
Kelly, D., Campbell, J.I., King, T.P., Grant, G., Jansson, E.A., Coutts, A.G.P., Pettersson, S., Conway, S., Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shutting of PPAR-γ and ReIA (2004) Nature Immunology, 5 (1), pp. 104-112. , DOI 10.1038/ni1018
Aneja, R., Odoms, K., Dunsmore, K., Shanley, T.P., Wong, H.R., Extracellular heat shock protein-70 induces endotoxin tolerance in THP-1 cells (2006) Journal of Immunology, 177 (10), pp. 7184-7192
Joo, Y.-E., Karrasch, T., Mühlbauer, M., Allard, B., Narula, A., Herfarth, H.H., Jobin, C., Tomato lycopene extract prevents lipopolysaccharide-induced NF- B signaling but worsens dextran sulfate sodium-induced colitis in NF- BEGFP mice (2009) PLoS ONE, 4 (2). , 2-s2.0-62349131372 10.1371/journal.pone.0004562 e4562
Reifen, R., Nur, T., Matas, Z., Halpern, Z., Lycopene supplementation attenuates the inflammatory status of colitis in a rat model (2001) International Journal for Vitamin and Nutrition Research, 71 (6), pp. 347-351
Kaulmann, A., Serchi, T., Renaut, J., Hoffmann, L., Bohn, T., Carotenoid exposure of Caco-2 intestinal epithelial cells did not affect selected inflammatory markers but altered their proteomic response (2012) British Journal of Nutrition, 108 (6), pp. 963-973. , 10.1017/S0007114511006349
Auweter, H., Haberkorn, H., Heckmann, W., Horn, D., Luddecke, E., Rieger, J., Weiss, H., Supramolecular structure of precipitated nanosize β-carotene particles (1999) Angewandte Chemie - International Edition, 38 (15), pp. 2188-2191. , DOI 10.1002/(SICI)1521-3773(19990802) 38:15<2188::AID-ANIE2188>3.0. CO
2-#
Gum, R., Wang, H., Lengyel, E., Juarez, J., Boyd, D., Regulation of 92 kDa type IV collagenase expression by the jun aminoterminal kinase- and the extracellular signal-regulated kinase-dependent signaling cascades (1997) Oncogene, 14 (12), pp. 1481-1493
Sato, H., Seiki, M., Regulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells (1993) Oncogene, 8 (2), pp. 395-405
Vallee, S., Fouchier, F., Bremond, P., Briand, C., Marvaldi, J., Champion, S., Insulin-like growth factor-1 downregulates nuclear factor κB activation and upregulates interleukin-8 gene expression induced by tumor necrosis factor α (2003) Biochemical and Biophysical Research Communications, 305 (4), pp. 831-839. , DOI 10.1016/S0006-291X(03)00866-0
Vallee, S., Laforest, S., Fouchier, F., Montero, M.P., Penel, C., Champion, S., Cytokine-induced upregulation of NF-κB, IL-8, and ICAM-1 is dependent on colonic cell polarity: Implication for PKCδ (2004) Experimental Cell Research, 297 (1), pp. 165-185. , DOI 10.1016/j.yexcr.2004.03.007, PII S0014482704001144
Fouchier, F., Penel, C., Pierre Montero, M., Bremond, P., Champion, S., Integrin αvβ6 mediates HT29-D4 cell adhesion to MMP-processed fibrinogen in the presence of Mn2+ (2007) European Journal of Cell Biology, 86 (3), pp. 143-160. , DOI 10.1016/j.ejcb.2006.12.002, PII S0171933506001919
Kimura, A., Israel, A., Le Bail, O., Kourilsky, P., Detailed analysis of the mouse H-2Kb promoter: Enhancer-like sequences and their role in the regulation of class I gene expression (1986) Cell, 44 (2), pp. 261-272
Schmittgen, T.D., Livak, K.J., Analyzing real-time PCR data by the comparative CT method (2008) Nature Protocols, 3 (6), pp. 1101-1108. , DOI 10.1038/nprot.2008.73, PII NPROT.2008.73
Cooney, R.V., Bertram, J.S., Hankin, J.H., Kolonel, L.N., Miyake, A., Billings, K., Bourne, W., Relationship between dietary, serum, and tissue levels of carotenoids (1991) Cancer Letters, 61 (1), pp. 81-87. , 2-s2.0-0026343507 10.1016/0304-3835(91)90080-2
Allen, C.M., Schwartz, S.J., Craft, N.E., Giovannucci, E.L., De Groff, V.L., Clinton, S.K., Changes in Plasma and Oral Mucosal Lycopene Isomer Concentrations in Healthy Adults Consuming Standard Servings of Processed Tomato Products (2003) Nutrition and Cancer, 47 (1), pp. 48-56
Schnaeker, E.-M., Ossig, R., Ludwig, T., Dreier, R., Oberleithner, H., Wilhelmi, M., Schneider, S.W., Microtubule-dependent matrix metalloproteinase-2/matrix metalloproteinase-9 exocytosis: Prerequisite in human melanoma cell invasion (2004) Cancer Research, 64 (24), pp. 8924-8931. , DOI 10.1158/0008-5472.CAN-04-0324
Pearson, G.T., Singh, J., Petersen, O.H., Adrenergic nervous control of cAMP-mediated amylase secretion in the rat pancreas (1984) American Journal of Physiology - Gastrointestinal and Liver Physiology, 9 (5), pp. G563-G573
Wang, X., Klein, R.D., Prostaglandin E2 induces vascular endothelial growth factor secretion in prostate cancer cells through EP2 receptor-mediated cAMP pathway (2007) Molecular Carcinogenesis, 46 (11), pp. 912-923. , DOI 10.1002/mc.20320
Mcquaid, T.S., Saleh, M.C., Joseph, J.W., Gyulkhandanyan, A., Manning-Fox, J.E., MacLellan, J.D., Wheeler, M.B., Chan, C.B., CAMP-mediated signaling normalizes glocuse-stimulated insulin secretion in uncoupling protein-2 overexpressing β-cells (2006) Journal of Endocrinology, 190 (3), pp. 669-680. , DOI 10.1677/joe.1.06723
Ozaki, N., Shibasaki, T., Kashima, Y., Miki, T., Takahashi, K., Ueno, H., Sunaga, Y., Seino, S., CAMP-GEFII is a direct target of cAMP in regulated exocytosis (2000) Nature Cell Biology, 2 (11), pp. 805-811. , 2-s2.0-0033769693 10.1038/35041046
Stork, P.J.S., Schmitt, J.M., Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation (2002) Trends in Cell Biology, 12 (6), pp. 258-266. , DOI 10.1016/S0962-8924(02)02294-8, PII S0962892402022948
Hazuka, M.B., Edwards-Prasad, J., Newman, F., Kinzie, J.J., Prasad, K.N., β -carotene induces morphological differentiation and decreases adenylate cyclase activity in melanoma cells in culture (1990) Journal of the American College of Nutrition, 9 (2), pp. 143-149. , 2-s2.0-0025542987
Al-Wadei, H.A.N., Majidi, M., Tsao, M.-S., Schuller, H.M., Low concentrations of beta-carotene stimulate the proliferation of human pancreatic duct epithelial cells in a PKA-dependent manner (2007) Cancer Genomics and Proteomics, 4 (1), pp. 35-42
Krakstad, C., Christensen, A.E., Doskeland, S.O., CAMP protects neutrophils against TNF-α-induced apoptosis by activation of cAMP-dependent protein kinase, independently of exchange protein directly activated by cAMP (Epac) (2004) Journal of Leukocyte Biology, 76 (3), pp. 641-647. , DOI 10.1189/jlb.0104005
Hur, E.-M., Kim, K.-T., G protein-coupled receptor signalling and cross-talk: Achieving rapidity and specificity (2002) Cellular Signalling, 14 (5), pp. 397-405. , DOI 10.1016/S0898-6568(01)00258-3, PII S0898656801002583
Palozza, P., Sestito, R., Picci, N., Lanza, P., Monego, G., Ranelletti, F.O., The sensitivity to β -carotene growth-inhibitory and proapoptotic effects is regulated by caveolin-1 expression in human colon and prostate cancer cells (2008) Carcinogenesis, 29 (11), pp. 2153-2161. , 2-s2.0-56049115353 10.1093/carcin/bgn018
Llaverias, G., Vazquez-Carrera, M., Sanchez, R.M., Noe, V., Ciudad, C.J., Laguna, J.C., Alegret, M., Rosiglitazone upregulates caveolin-1 expression in THP-1 cells through a PPAR-dependent mechanism (2004) Journal of Lipid Research, 45 (11), pp. 2015-2024. , DOI 10.1194/jlr.M400049-JLR200
