Strawberry consumption improves aging-associated impairments, mitochondrial biogenesis and functionality through the AMP-activated protein kinase signaling cascade

Food Chemistry

Volumn 234, Issue , 2017, Pages 464-471

  Giampieri, Francesca ^a   Alvarez Suarez, Josè M ^a,b   Cordero, Mario D ^c   Gasparrini, Massimiliano ^a   Forbes Hernandez, Tamara Y ^a,d   Afrin, Sadia ^a   Santos Buelga, Celestino ^e   González Paramás, Ana M ^e   Astolfi, Paola ^a   Rubini, Corrado ^a   Zizzi, Antonio ^a   Tulipani, Sara ^f,g   Quiles, Josè L ^h   Mezzetti, Bruno ^a   Battino, Maurizio ^a,i  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSIDAD DE LAS AMÉRICAS   (Ecuador)

^c UNIVERSITY OF SEVILLE   (Spain)

^d Universidad Internacional Iberoamericana   (Mexico)

^e UNIVERSITY OF SALAMANCA   (Spain)

^f UNIVERSITY OF BARCELONA   (Spain)

^g Malaga Hospital Complex Virgen de la Victoria   (Spain)

^h UNIVERSITY OF GRANADA   (Spain)

ⁱ Parque Científico y Tecnológico de Cantabria   (Spain)

Author keywords

Aging; AMPK activation; Mitochondrial functionality; Oxidative stress; Strawberry polyphenols

Indexed keywords

AGING OF MATERIALS; ANTIOXIDANTS; BIOMARKERS; BIOSYNTHESIS; ENZYMES; FRUITS; GENE EXPRESSION; OXIDATIVE STRESS; PROTEINS;

AMP-ACTIVATED PROTEIN KINASE; ANTIOXIDANT DEFENCE; ANTIOXIDANT ENZYME ACTIVITY; BENEFICIAL EFFECTS; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL FUNCTIONALITY; POLYPHENOLS;

ENZYME ACTIVITY;

ADENOSINE TRIPHOSPHATE; CATALASE; CITRATE SYNTHASE; CITRININ; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; ROTENONE; SIRTUIN 1; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOMASS; BODY WEIGHT; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; FOOD INTAKE; FUNCTIONAL FOOD; HEP-G2 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPID PEROXIDATION; LIVER HOMOGENATE; LIVER MITOCHONDRION; MALE; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STRAWBERRY; ANIMAL; FRAGARIA; METABOLISM; MITOCHONDRION; ORGANELLE BIOGENESIS;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIOXIDANTS; FRAGARIA; HUMANS; MITOCHONDRIA; ORGANELLE BIOGENESIS; RATS;

EID: 85019059122     PISSN: 03088146     EISSN: 18737072     Source Type: Journal    
DOI: 10.1016/j.foodchem.2017.05.017     Document Type: Article

References (39)

1. Alvarez-Suarez, J.M., Giampieri, F., Tulipani, S., Casoli, T., Di Stefano, G., González-Paramás, A.M., et al. One-month strawberry-rich anthocyanin supplementation ameliorates cardiovascular risk, oxidative stress markers and platelet activation in humans. Journal of Nutritional Biochemistry 25:3 (2014), 289–294.
2. Amatori, S., Mazzoni, L., Alvarez-Suarez, J.M., Giampieri, F., Gasparrini, M., Forbes-Hernandez, T.Y., et al. Polyphenol-rich strawberry extract (PRSE) shows in vitro and in vivo biological activity against invasive breast cancer cells. Scientific Reports, 6, 2016, 30917.
3. Basu, A., Betts, N.M., Nguyen, A., Newman, E.D., Fu, D., Lyons, T.J., Freeze-dried strawberries lower serum cholesterol and lipid peroxidation in adults with abdominal adiposity and elevated serum lipids. Journal of Nutrition 144 (2014), 830–837.
4. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 (1976), 248–254.
5. Bullon, P., Cordero, M.D., Quiles, J.L., Morillo, J.M., del Carmen Ramirez-Tortosa, M., Battino, M., Mitochondrial dysfunction promoted by Porphyromonas gingivalis lipopolysaccharide as a possible link between cardiovascular disease and periodontitis. Free Radical Biology and Medicine 50 (2011), 1336–1343.
6. Colombo, S.L., Moncada, S., AMPKalpha1 regulates the antioxidant status of vascular endothelial cells. Biochemical Journal 421 (2009), 163–169.
7. Cordero, M.D., Alcocer-Gómez, E., de Miguel, M., Culic, O., Carrión, A.M., Alvarez-Suarez, J.M., Bullón, P., Can coenzyme q10 improve clinical and molecular parameters in fibromyalgia?. Antioxidant and Redox Signaling 19 (2013), 1356–1361.
8. Forbes-Hernandez, T.Y., Gasparrini, M., Afrin, S., Bompadre, S., Mezzetti, B., Quiles, J.L., et al. The healthy effects of strawberry polyphenols: Which strategy behind antioxidant capacity?. Critical Review in Food Science and Nutrition 56 (2016), S46–59.
9. Gasparrini, M., Forbes-Hernandez, T.Y., Giampieri, F., Afrin, S., AlvarezSuarez, J.M., Mazzoni, L., et al. Anti-inflammatory effect of strawberry extract against LPS-induced stress in RAW 264.7 macrophages. Food and Chemical Toxicology, 2017, 10.1016/j.fct.2017.01.018.
10. Gasparrini, M., Giampieri, F., Alvarez-Suarez, J.M., Mazzoni, L., Forbes-Hernandez, T.Y., Quiles, J.L., et al. AMPK as a new attractive therapeutic target for disease prevention: The role of dietary compounds. Current Drug Targets 16 (2015), 1–25.
11. Gesing, A., Masternak, M.M., Wang, F., Joseph, A.M., Leeuwenburgh, C., Westbrook, R., et al. Expression of key regulators of mitochondrial biogenesis in growth hormone receptor knockout (GHRKO) mice is enhanced but is not further improved by other potential life-extending interventions. The Journals of Gerontology: Series A, Biological sciences and medical sciences 66A (2011), 1062–1076.
12. Giampieri, F., Alvarez-Suarez, J.M., Battino, M., Strawberry and human health: Effects beyond antioxidant activity. Journal of Agricultural and Food Chemistry 62 (2014), 3867–3876.
13. Giampieri, F., Alvarez-Suarez, J.M., Gasparrini, M., Forbes-Hernandez, T.Y., Afrin, S., Bompadre, S., et al. Strawberry consumption alleviates doxorubicin-induced toxicity by suppressing oxidative stress. Food and Chemical Toxicology 94 (2016), 128–137.
14. Giampieri, F., Alvarez-Suarez, J.M., Gasparrini, M., Forbes-Hernandez, T.Y., Afrin, A., Rubini, C., Zizzi, A., Battino, M., Data on body weight and liver functionality in aged rats fed an enriched strawberry diet. Data In Brief, 2017 [Submitted for publication].
15. 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 28 (2012), 9–19.
16. Hardie, D.G., Ross, F.A., Hawley, S.A., AMPK: A nutrient and energy sensor that maintains energy homeostasis. Nature Reviews Molecular Cell Biology 13 (2012), 251–262.
17. Harman, D., Aging: A theory based on free radical and radiation chemistry. Journal of Gerontology 11 (1956), 298–300.
18. Hsieh, Y.C., Yang, S., Choudhry, M.A., Yu, H.P., Rue, L.W., Bland, K.I., Chaudry, I.H., PGC-1 upregulation via estrogen receptors: A common mechanism of salutary effects of estrogen and flutamide on heart function after trauma hemorrhage. American Journal of Physiology-Heart and Circulatory Physiology 289 (2005), H2665–H2672.
19. Lee, Y.K., Lee, W.S., Kim, G.S., Park, O.J., Anthocyanins are novel AMPKα1 stimulators that suppress tumor growth by inhibiting mTOR phosphorylation. Oncology Reports 24 (2010), 1471–1477.
20. López-Lluch, G., Irusta, P.M., Navas, P., de Cabo, R., Mitochondrial biogenesis and healthy aging. Experimental Gerontology 43 (2008), 813–819.
21. Malin, D.H., Lee, D.R., Goyarzu, P., Chang, Y.H., Ennis, L.J., Beckett, E., et al. Short-term blueberry-enriched diet prevents and reverses object recognition memory loss in aging rats. Nutrition 27 (2011), 338–342.
22. 10. Free Radical Biology and Medicine 50 (2011), 1053–1064.
23. Panov, A., Dikalov, S., Shalbuyeva, N., Taylor, G., Sherer, T., Greenamyre, J.T., Rotenone model of Parkinson's disease: Multiple brain mitochondria dysfunctions after short-term systemic rotenone intoxication. The Journal of Biological Chemistry 280 (2005), 42026–42035.
24. Park, E., Edirisinghe, I., Wei, H., Vijayakumar, L.P., Banaszewski, K., Cappozzo, J.C., et al. A dose-response evaluation of freeze-dried strawberries independent of fiber content on metabolic indices in abdominally obese individuals with insulin resistance in a randomized, single-blinded, diet-controlled crossover trial. Molecular Nutrition & Food Research 60 (2016), 1099–1109.
25. Park, S.Y., Lee, Y.K., Lee, W.S., Park, O.J., Kim, Y.M., The involvement of AMPK/GSK3-beta signals in the control of metastasis and proliferation in hepato-carcinoma cells treated with anthocyanins extracted from Korea wild berry Meoru. BMC Complementary and Alternative Medicine, 14, 2014, 109.
26. Pedersen, P.L., Greeawalt, J.W., Reynafarje, B., Hullihen, J., Decker, G.L., Soper, J.W., et al. Preparation and characterization of mitochondria and submitochondrial particles of rat liver and liver-derived tissues. Methods in Cell Biology 20 (1978), 411–481.
27. Poulose, S.M., Bielinski, D.F., Carey, A., Schauss, A.G., Shukitt-Hale, B., Modulation of oxidative stress, inflammation, autophagy and expression of Nrf2 in hippocampus and frontal cortex of rats fed with açaí-enriched diets. Nutritional Neuroscience, 2016, 10.1080/1028415X.2015.1125654.
28. Reznick, R.M., Zong, H., Li, J., Morino, K., Moore, I.K., Yu, H.J., et al. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metababolism 5 (2007), 151–156.
29. Richardson, T.E., Yu, A.E., Wen, Y., Yang, S.H., Simpkins, J.W., Estrogen prevents oxidative damage to the mitochondria in Friedreich's ataxia skin fibroblasts. PLoS One, 7, 2012, e34600.
30. Salminen, A., Kaarniranta, K., AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Research Reviews 11 (2012), 230–241.
31. Shang-U, Kim., Frederick, A.V., Reactivities of superoxide and hydroperoxyl radicals with disubstituted cyclic nitrones: A DFT Study. The Journal of Physical Chemistry A 116 (2012), 886–898.
32. Shi, L., Liu, B., Zhang, Y., Xue, Z., Liu, Y., Chen, Y., Exercise training reverses unparallel downregulation of MaxiK channel α- and β1-subunit to enhance vascular function in aging mesenteric arteries. The Journals of Gerontology: Series A, Biological sciences and medical sciences 69 (2014), 1462–1473.
33. Shukitt-Hale, B., Bielinski, D.F., Lau, F.C., Willis, L.M., Carey, A.N., Joseph, J.A., The beneficial effects of berries on cognition, motor behaviour and neuronal function in ageing. British Journal of Nutrition 114 (2015), 1542–1549.
34. Steinberg, G.R., Kemp, B.E., AMPK in health and disease. Physiological Reviews 89 (2009), 1025–1078.
35. Takikawa, M., Inoue, S., Horio, F., Tsuda, T., Dietary anthocyanin-rich bilberry extract ameliorates hyperglycemia and insulin sensitivity via activation of AMP-activated protein kinase in diabetic mice. Journal of Nutrition 140 (2010), 527–533.
36. Tulipani, S., Armeni, T., Giampieri, F., Alvarez-Suarez, J.M., Gonzalez-Paramás, A.M., Santos-Buelga, C., et al. Strawberry intake increases blood fluid, erythrocyte and mononuclear cell defenses against oxidative challenge. Food Chemistry 1 (2014), 87–93.
37. Turrens, J.F., Mitochondrial formation of reactive oxygen species. The Journal of Physiology 552 (2003), 335–344.
38. Watanabe, T., Owada, S., Kobayashi, H.P., Kawakami, H., Nagaoka, S., Murakami, E., et al. Protective effects of MnM2Py4P and Mn-salen against small bowel ischemia/reperfusion injury in rats using an in vivo and an ex vivo electron paramagnetic resonance technique with a spin probe. Transplantation Proceeding 39 (2007), 3002–3006.
39. Zhang, Y., Wang, X., Wang, Y., Liu, Y., Xia, M., Supplementation of cyanidin-3-O-β-glucoside promotes endothelial repair and prevents enhanced atherogenesis in diabetic apolipoprotein E-deficient mice. Journal of Nutrition 143 (2013), 1248–1253.