Protective effect of strawberry extract against inflammatory stress induced in human dermal fibroblasts

Molecules

Volumn 22, Issue 1, 2017, Pages

  Gasparrini, Massimiliano ^a   Forbes Hernandez, Tamara Y ^a,b   Giampieri, Francesca ^a   Afrin, Sadia ^a   Mezzetti, Bruno ^a   Quiles, Josè L ^c   Bompadre, Stefano ^a   Battino, Maurizio ^a,d  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b Area de Nutrición y Salud Universidad Internacional Iberoamericana UNINI   (Mexico)

^c UNIVERSITY OF GRANADA   (Spain)

^d Parque Científico y Tecnológico de Cantabria   (Spain)

Author keywords

Inflammation; LPS; Oxidative stress; Prevention; Strawberry

Indexed keywords

ANTIINFLAMMATORY AGENT; BACTERIAL POLYSACCHARIDE; LIPOPOLYSACCHARIDE; PLANT EXTRACT;

CELL LINE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DNA DAMAGE; DRUG EFFECTS; ESCHERICHIA COLI; FIBROBLAST; FRAGARIA; HUMAN; METABOLISM; OXIDATIVE STRESS;

ANTI-INFLAMMATORY AGENTS; CELL LINE; CELL SURVIVAL; DNA DAMAGE; ESCHERICHIA COLI; FIBROBLASTS; FRAGARIA; HUMANS; LIPOPOLYSACCHARIDES; OXIDATIVE STRESS; PLANT EXTRACTS; POLYSACCHARIDES, BACTERIAL;

EID: 85011706099     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules22010164     Document Type: Article

References (56)

1. Joseph, S.V.; Edirisinghe, I.; Burton-Freeman, B.M. Berries: Anti-inflammatory Effects in Humans. J. Agric. Food Chem. 2014, 62, 3886-3903. [CrossRef] [PubMed]
2. Trachootham, D.; Lu, W.; Ogasawara, M.A.; Nilsa, R.D.; Huang, P. Redox regulation of cell survival. Antioxid. Redox Signal. 2008,10,1343-1374. [CrossRef] [PubMed]
3. Ray, P.D.; Huang, B.W.; Tsuji, Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal. 2012, 24, 981-990. [CrossRef] [PubMed]
4. Elliott, C.G.; Forbes, T.L.; Leask, A.; Hamilton, D.W. Inflammatory microenvironment and tumor necrosis factor alpha as modulators of periostin and CCN2 expression in human non-healing skin wounds and dermal fibroblasts. Matrix Biol. 2015, 43, 71-84. [CrossRef] [PubMed]
5. Landen, N.X.; Li, D.; Stahle, M. Transition from inflammation to proliferation: A critical step during wound healing. Cell. Mol. Life Sci. 2016, 73, 3861-3885. [CrossRef] [PubMed]
6. Alvarez-Suarez, J.M.; Giampieri, F.; Cordero, M.; Gasparrini, M.; Forbes-Hernandez, T.Y.; Mazzoni, L.; Afrin, S.; Beltran-Ayala, P.; Gonzalez-Paramas, A.M.; Santos-Buelga, C.; et al. Activation of AMPK/Nrf2 signalling by Manuka honey protects human dermal fibroblasts against oxidative damage by improving antioxidant response and mitochondrial function promoting wound healing. J. Funct. Foods 2016, 25, 38-49. [CrossRef]
7. Afrin, S.; Giampieri, F.; Gasparrini, M.; Forbes-Hernandez, T.Y.; Varela-Lopez, A.; Quiles, J.L.; Mezzetti, B.; Battino, M. Chemopreventive and Therapeutic Effects of Edible Berries: A Focus on Colon Cancer Prevention and Treatment. Molecules 2016,21,169. [CrossRef] [PubMed]
8. Davies, K.J. Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life 2000, 50, 279-289. [CrossRef] [PubMed]
9. Kohen, R.; Nyska, A. Oxidation of biological systems: Oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol. Pathol. 2002, 30, 620-650. [CrossRef] [PubMed]
10. Forbes-Hernandez, T.Y.; Giampieri, F.; Gasparrini, M.; Mazzoni, L.; Quiles, J.L.; Alvarez-Suarez, J.M.; Battino, M. The effects of bioactive compounds from plant foods on mitochondrial function: A focus on apoptotic mechanisms. Food Chem. Toxicol. 2014, 68,154-182. [CrossRef] [PubMed]
11. Giampieri, F.; Alvarez-Suarez, J.M.; Battino, M. Strawberry and human health: Effects beyond antioxidant activity. J. Agric. Food Chem. 2014, 62, 3867-3876. [CrossRef] [PubMed]
12. McCarty, M.F.; DiNicolantonio, J.J.; O'Keefe, J.H. Capsaicin may have important potential for promoting vascular and metabolic health. Open Heart 2015, 2, e000262. [CrossRef] [PubMed]
13. Giampieri, F.; Tulipani, S.; Alvarez-Suarez, J.M.; Quiles, J.L.; Mezzetti, B.; Battino, M. The strawberry: Composition, nutritional quality, and impact on human health. Nutrition 2012,28,9-19. [CrossRef] [PubMed]
14. Giampieri, F.; Alvarez-Suarez, J.M.; Mazzoni, L.; Romandini, S.; Bompadre, S.; Diamanti, J.; Capocasa, F.; Mezzetti, B.; Quiles, J.L.; Ferreiro, M.S.; et al. The potential impact of strawberry on human health. Nat. Prod. Res. 2013, 27, 448-455. [CrossRef] [PubMed]
15. Lee, J.; Kim, S.; Namgung, H.; Jo, Y.H.; Bao, C.; Choi, H.K.; Auh, J.H.; Lee, H.J. Ellagic acid identified through metabolomic analysis is an active metabolite in strawberry ('Seolhyang') regulating lipopolysaccharide-induced inflammation. J. Agric. Food Chem. 2014, 62, 3954-3962. [CrossRef] [PubMed]
16. Alarcon, M.; Fuentes, E.; Olate, N.; Navarrete, S.; Carrasco, G.; Palomo, I. Strawberry extract presents antiplatelet activity by inhibition of inflammatory mediator of atherosclerosis (sP-selectin, sCD40L, RANTES, and IL-113) and thrombus formation. Platelets 2015,26, 224-229. [CrossRef] [PubMed]
17. Amatori, S.; Mazzoni, L.; Alvarez-Suarez, J.M.; Giampieri, F.; Gasparrini, M.; Forbes-Hernandez, T.Y.; Afrin, S.; Errico Provenzano, A.; Persico, G.; Mezzetti, B.; et al. Polyphenol-rich strawberry extract (PRSE) shows in vitro and in vivo biological activity against invasive breast cancer cells. Sci. Rep. 2016, 6, 30917. [CrossRef] [PubMed]
18. Mayer, H.; Tharanathan, R.N.; Weckesser, J. Analysis of Lipopolysaccharides of Gram-Negative Bacteria. Methods Microbiol. 1985,118,157-207.
19. Giampieri, F.; Forbes-Hernandez, T.Y.; Gasparrini, M.; Alvarez-Suarez, J.M.; Afrin, S.; Bompadre, S.; Quiles, J.L.; Mezzetti, B.; Battino, M. Strawberry as a health promoter: An evidence based review. Food Funct. 2015, 6, 1386-1398. [CrossRef] [PubMed]
20. Malpass, G.E.; Arimilli, S.; Prasad, G.L.; Howlett, A.C. Complete artificial saliva alters expression of proinflammatory cytokines in human dermal fibroblasts. Toxicol. Sci. 2013,134,18-25. [CrossRef] [PubMed]
21. Awang, M.A.; Firdaus, M.A.; Busra, M.B.; Chowdhury, S.R.; Fadilah, N.R.; Wan Hamirul, W.K.; Reusmaazran, M.Y.; Aminuddin, M.Y.; Ruszymah, B.H. Cytotoxic evaluation of biomechanically improved crosslinked ovine collagen on human dermal fibroblasts. Biomed. Mater. Eng. 2014, 24,1715-1724. [PubMed]
22. Tardif, F.; Ross, G.; Rouabhia, M. Gingival and dermal fibroblasts produce interleukin-1 beta converting enzyme and interleukin-1 beta but not interleukin-18 even after stimulation with lipopolysaccharide. J. Cell. Physiol. 2004, 198, 125-132. [CrossRef] [PubMed]
23. Wheater, M.A.; Falvo, J.; Ruiz, F.; Byars, M. Chlorhexidine, ethanol, lipopolysaccharide and nicotine do not enhance the cytotoxicity of a calcium hydroxide pulp capping material. Int. Endod. J. 2012, 45, 989-995. [CrossRef] [PubMed]
24. Tulipani, S.; Mezzetti, B.; Battino, M. Impact of strawberries on human health: Insight into marginally discussed bioactive compounds for the Mediterranean diet. Public Health Nutr. 2009, 12, 1656-1662. [CrossRef] [PubMed]
25. Buendia, B.; Gil, M.I.; Tudela, J.A.; Gady, A.L.; Medina, J.J.; Soria, C.; Lopez, J.M.; Tomas-Barberan, F.A. HPLC-MS analysis of proanthocyanidin oligomers and other phenolics in 15 strawberry cultivars. J. Agric. Food Chem. 2010, 58, 3916-3926. [CrossRef] [PubMed]
26. Giampieri, F.; Alvarez-Suarez, J.M.; Tulipani, S.; Gonzales-Paramas, A.M.; Santos-Buelga, C.; Bompadre, S.; Quiles, J.L.; Mezzetti, B.; Battino, M. Photoprotective potential of strawberry (Fragaria x ananassa) extract against UV-A irradiation damage on human fibroblasts. J. Agric. Food Chem. 2012, 60, 2322-2327. [CrossRef] [PubMed]
27. Giampieri, F.; Alvarez-Suarez, J.M.; Mazzoni, L.; Forbes-Hernandez, T.Y.; Gasparrini, M.; Gonzalez-Paramas, A.M.; Santos-Buelga, C.; Quiles, J.L.; Bompadre, S.; Mezzetti, B.; et al. An anthocyanin-rich strawberry extract protects against oxidative stress damage and improves mitochondrial functionality in human dermal fibroblasts exposed to an oxidizing agent. Food Funct. 2014, 5,1939-1948. [CrossRef] [PubMed]
28. Ariza, M.T.; Martinez-Ferri, E.; Dominguez, P.; Medina, J.J.; Miranda, L.; Soria, C. Effects of harvest time on functional compounds and fruit antioxidant capacity in ten strawberry cultivars. J. Berry Res. 2015,5, 71-80. [CrossRef]
29. Giampieri, F.; Alvarez-Suarez, J.M.; Mazzoni, L.; Forbes-Hernandez, T.Y.; Gasparrini, M.; Gonzalez-Paramas, A.M.; Santos-Buelga, C.; Quiles, J.L.; Bompadre, S.; Mezzetti, B.; et al. Polyphenol-rich strawberry extract protects human dermal fibroblasts against hydrogen peroxide oxidative damage and improves mitochondrial functionality. Molecules 2014,19, 7798-7816. [CrossRef] [PubMed]
30. Schieber, M.; Chandel, N.S. ROS function in redox signaling and oxidative stress. Curr. Biol. 2014, 24, R453-R462. [CrossRef] [PubMed]
31. Park, G.J.; Kim, Y.S.; Kang, K.L.; Bae, S.J.; Baek, H.S.; Auh, Q.S.; Chun, Y.H.; Park, B.H.; Kim, E.C. Effects of sirtuin 1 activation on nicotine and lipopolysaccharide-induced cytotoxicity and inflammatory cytokine production in human gingival fibroblasts. J. Periodontal Res. 2013, 48, 483-492. [CrossRef] [PubMed]
32. Mo, C.; Wang, L.; Zhang, J.; Numazawa, S.; Tang, H.; Tang, X.; Han, X.; Li, J.; Yang, M.; Wang, Z.; et al. The crosstalk between Nrf2 and AMPK signal pathways is important for the anti-inflammatory effect of berberine in LPS-stimulated macrophages and endotoxin-shocked mice. Antioxid. Redox Signal. 2014, 20, 574-588. [CrossRef] [PubMed]
33. Choi, E.Y.; Kim, H.J.; Han, J.S. Anti-inflammatory effects of calcium citrate in RAW 264.7 cells via suppression of NF-kB activation. Environ. Toxicol. Pharmacol. 2015, 39, 27-34. [CrossRef] [PubMed]
34. Zong, Y.; Sun, L.; Liu, B.; Deng, Y.S.; Zhan, D.; Chen, Y.L.; He, Y.; Liu, J.; Zhang, Z.J.; Sun, J.; et al. Resveratrol inhibits LPS-induced MAPKs activation via activation of the phosphatidylinositol 3-kinase pathway in murine RAW 264.7 macrophage cells. PLoS ONE 2012, 7, e44107. [CrossRef] [PubMed]
35. Espanol, A.J.; Goren, N.; Ribeiro, M.L.; Sales, M.E. Nitric oxide synthase 1 and cyclooxygenase-2 enzymes are targets of muscarinic activation in normal and inflamed NIH3T3 cells. Inflamm. Res. 2010, 59, 227-238. [CrossRef] [PubMed]
36. DeLeve, L.D.; Kaplowitz, N. Importance and regulation of hepatic glutathione. Semin. Liver Dis. 1990,10, 251-266. [CrossRef] [PubMed]
37. Ciolino, H.P.; Levine, R.L. Modification of proteins in endothelial cell death during oxidative stress. Free Radic. Biol. Med. 1997, 22, 1277-1282. [CrossRef]
38. Babujanarthanam, R.; Kavitha, P.; Mahadeva Rao, U.S.; Pandian, M.R. Quercitrin a bioflavonoid improves the antioxidant status in streptozotocin: Induced diabetic rat tissues. Mol. Cell. Biochem. 2011, 358,121-129. [CrossRef] [PubMed]
39. Hacker, H.; Redecke, V.; Blagoev, B.; Kratchmarova, I.; Hsu, L.C.; Wang, G.G.; Kamps, M.P.; Raz, E.; Wagner, H.; Hacker, G.; et al. Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 2006, 439, 204-207. [CrossRef] [PubMed]
40. Slinkard, K.; Singleton, V.L. Total Phenol analysis: Automation and comparison with manual methods. Am. J. Enol. Viticult. 1977, 28, 49-55.
41. Dewanto, V.; Wu, X.; Adom, K.K.; Liu, R.H. Thermal processing enhances the nutritional values of tomatoes by increasing the total antioxidant activity. J. Agric. Food Chem. 2002, 50, 3010-3014. [CrossRef] [PubMed]
42. Jastrebova, J.; Witthoft, C.; Grahn, A.; Svensson, U.; Jagerstad, M. HPLC determination of folates in raw and processed beetroots. Food Chem. 2003, 80, 579-588. [CrossRef]
43. Patring, J.D.; Jastrebova, J.A.; Hjortmo, S.B.; Andlid, T.A.; Jagerstad, I.M. Development of a simplified method for the determination of folates in baker's yeast by HPLC with ultraviolet and fluorescence detection. J. Agric. Food Chem. 2005, 53, 2406-2411. [CrossRef] [PubMed]
44. Giusti, M.; Wrolstad, R.E. Characterization and Measurement of Anthocyanins by UV-Visible Spectroscopy. Curr. Protoc. Food Anal. Chem. 2001. [CrossRef]
45. Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 1999,26,1231-1237. [CrossRef]
46. Benzie, I.F.F.; Strain, J.J. Ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: The FRAP assay. Anal. Biochem. 1996, 239, 70-76. [CrossRef] [PubMed]
47. Prymont-Przyminska, A.; Zwolinska, A.; Sarniak, A.; Wlodarczyk, A.; Krol, M.; Nowak, M.; de Graft-Johnson, J.; Padula, G.; Bialasiewicz, P.; Markowski, J.; et al. Consumption of strawberries on a daily basis increases the non-urate 2,2-diphenyl-1-picryl-hydrazyl (DPPH) radical scavenging activity of fasting plasma in healthy subjects. J. Clin. Biochem. Nutr. 2014, 55, 48-55. [CrossRef] [PubMed]
48. Gasparrini, M.; Forbes-Hernandez, T.Y.; Afrin, S.; Alvarez-Suarez, J.M.; Gonzalez-Paramas, A.M.; Santos-Buelga, C.; Bompadre, S.; Quiles, J.L.; Mezzetti, B.; Giampieri, F. A Pilot Study of the Photoprotective Effects of Strawberry-Based Cosmetic Formulations on Human Dermal Fibroblasts. Int. J. Mol. Sci. 2015,16, 17870-17884. [CrossRef] [PubMed]
49. Moongkarndi, P.; Kosem, N.; Kaslungka, S.; Luanratana, O.; Pongpan, N.; Neungton, N. Antiproliferation, antioxidation and induction of apoptosis by Garcinia mangostana (mangosteen) on SKBR3 human breast cancer cell line. J. Ethnopharmacol. 2004, 90,161-166. [CrossRef] [PubMed]
50. Lyu, S.Y.; Park, W.B. Photoprotective Potential of Anthocyanins Isolated from Acanthopanax divaricatus Var. albeofructus Fruits against UV Irradiation in Human Dermal Fibroblast Cells. Biomol. Ther. 2012, 20, 201-206. [CrossRef] [PubMed]
51. Wang, R.; Ghahary, A.; Shen, Y.J.; Scott, P.G.; Tredget, E.E. Human dermal fibroblasts produce nitric oxide and express both constitutive and inducible nitric oxide synthase isoforms. J. Investig. Dermatol. 1996,106, 419-427. [CrossRef] [PubMed]
52. Doktorovova, S.; Santos, D.L.; Costa, I.; Andreani, T.; Souto, E.B.; Silva, A.M. Cationic solid lipid nanoparticles interfere with the activity of antioxidant enzymes in hepatocellular carcinoma cells. Int. J. Pharm. 2014, 471, 18-27. [CrossRef] [PubMed]
53. Levine, R.L.; Garland, D.; Oliver, C.N.; Amici, A.; Climent, I.; Lenz, A.G.; Ahn, B.W.; Shaltiel, S.; Stadtman, E.R. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990,186, 464-478. [PubMed]
54. Griffith, O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 1980,106, 207-212. [CrossRef]
55. Ohkawa, H.; Ohishi, N.; Yagi, K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95, 351-358. [CrossRef]
56. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254. [CrossRef]