Grain and bean lysates improve function of endothelial progenitor cells from human peripheral blood: Involvement of the endogenous antioxidant defenses

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Lucchesi, Daniela ^a   Russo, Rossella ^b   Gabriele, Morena ^b   Longo, Vincenzo ^b   Del Prato, Stefano ^a   Penno, Giuseppe ^a   Pucci, Laura ^b  

^a UNIVERSITY OF PISA   (Italy)

^b Institute of Agricultural Biology and Biotechnology   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; FIBRONECTIN; GLUTATHIONE PEROXIDASE 1; HEME OXYGENASE 1; HYDROGEN PEROXIDE; LADY JOY; LISOSAN G; MANGANESE SUPEROXIDE DISMUTASE; NUCLEAR FACTOR ERYTHROID DERIVED 2 LIKE 2; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; GLUTATHIONE PEROXIDASE; NFE2L2 PROTEIN, HUMAN; PLANT EXTRACT; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2;

ADHERENT CELL; ANTIOXIDANT ACTIVITY; ARTICLE; BEAN; CELL ADHESION; CELL FUNCTION; CELL ISOLATION; CELL PROTECTION; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; ENZYME ACTIVATION; GENE EXPRESSION; GRAIN; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MONONUCLEAR CELL; NORMAL HUMAN; OXIDATIVE STRESS; SENESCENCE; CELL CULTURE; CELL SURVIVAL; CEREAL; CHEMISTRY; DRUG EFFECTS; FABACEAE; GENETICS; METABOLISM;

ANTIOXIDANTS; CELL SURVIVAL; CELLS, CULTURED; CEREALS; ENDOTHELIAL PROGENITOR CELLS; FABACEAE; GLUTATHIONE PEROXIDASE; HUMANS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PLANT EXTRACTS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 84908052883     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109298     Document Type: Article

References (72)

1. Badimon L, Vilahur G, Padro T (2010) Nutraceuticals and atherosclerosis: human trials. Cardiovasc Ther 28: 202-215.
2. Diplock AT, Aggott PJ, Ashwell M, Bornet F, Fern EB, et al. (1999) Scientific Concepts of Functional Foods in Europe Consensus Document. Br J Nutr 81: S1-S27.
3. Angeloni C, Pirola L, Vauzour D, Maraldi T (2012) Dietary polyphenols and their effects on cell biochemistry and pathophysiology. Oxid Med Cell Longev ID 883901; doi:10.1155/2012/585901.
4. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, et al. (1997) Isolation of putative endothelial progenitor cells for angiogenesis. Science 275: 964-967.
5. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, et al. (1999) Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85: 221-228.
6. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, et al. (2001) Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89: E1-E7.
7. Shantsila E, Watson T, Lip GY (2007) Endothelial progenitor cells in cardiovascular disorders. J Am Coll Cardiol 20: 741-752
8. Fadini GP, Losordo D, Dimmeler S (2012) Critical re-evaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 110: 624-637.
9. Fadini GP (2014) reappraisal of the role of circulating (progenitor) cells in the pathobiology of diabetic complications. Diabetologia 57: 4-15.
10. Yoder MC (2012) Human Endothelial Progenitor Cells. Cold Spring Harb Perspect Med 2012; 2: a006692.
11. Basile DP, Yoder MC (2014) Circulating and tissue resident endothelial progenitor cells. J Cell Physiol 229: 10-16.
12. Wang XB, Zhu L, Huang J, Yin YG, Kong XQ, et al. (2011) Resveratrolinduced augmentation of telomerase activity delays senescence of endothelial progenitor cells. Chin Med J 124: 4310-4315.
13. Dong XX, Hui ZJ, Xiang WX, Rong ZF, Jian S, et al. (2007) Ginkgo biloba extract reduces endothelial progenitor-cell senescence through augmentation of telomerase activity. J Cardiovasc Pharmacol 49: 111-115.
14. Van Oostrom O, de Kleijn DP, Fledderus JO, Pescatori M, Stubbs A, et al. (2009) Folic acid supplementation normalizes the endothelial progenitor cell transcriptome of patients with type 1 diabetes: a case-control pilot study. Cardiovasc Diabetol 8: 47.
15. Chan YH, Lam TH, Lau KK, Yiu KH, Siu CW, et al. (2011) Dietary intake of phytoestrogen is associated with increased circulating endothelial progenitor cells in patients with cardiovascular disease. Eur J Cardiovasc Prev Rehabil 18: 360-368.
16. Wong CY, Yiu KH, Li SW, Lee S, Tam S, et al. (2010) Fish-oil supplement has neutral effects on vascular and metabolic function but improves renal function in patients with Type 2 diabetes mellitus. Diabet Med 27: 54-60.
17. Flight I, Clifton P (2006) Cereal grains and legumes in the prevention of coronary heart disease and stroke: a review of the literature. Eur J Clin Nutr 60: 1145-1159.
18. Harris KA, Kris-Etherton PM (2010) Effects of whole grains on coronary heart disease risk. Curr Atheroscler Rep 12: 368-376.
19. Okarter N, Liu RH (2010) Health benefits of whole grain phytochemicals. Crit Rev Food Sci Nutr 50: 193-208.
20. de Munter JS, Hu FB, Spiegelman D, Franz M, van Dam RM (2007) Whole grain, bran, and germ intake and risk of type 2 diabetes: a prospective cohort study and systematic review. PLoS Med 4: e261.
21. Eilat-Adar S, Goldbourt U (2010) Nutritional recommendations for preventing coronary heart disease in women: evidence concerning whole foods and supplements. Nutr Metab Cardiovasc Dis 20: 459-466.
22. Jonnalagadda SS, Harnack L, Liu RH, McKeown N, Seal C, et al. (2011) Putting the whole grain puzzle together: health benefits associated with whole grains-summary of American Society for Nutrition 2010 Satellite Symposium. J Nutr 141: 1011S-1022S.
23. Fraga CG, Galleano M, Verstraeten SV, Oteiza PI (2010) Basic biochemical mechanisms behind the health benefits of polyphenols. Mol Aspects Med 31: 435-445.
24. Longo V, Chirulli V, Gervasi PG, Nencioni S, Pellegrini M (2007) Lisosan G, a powder of grain, does not interfere with the drug metabolizing enzymes and has a protective role on carbon tetrachloride- induced hepatotoxicity. Biotechnol Lett 29: 1155-1159.
25. Longo V, Gervasi PG, Lubrano V (2011) Cisplatin induced toxicity in rat tissues: the protective effect of lisosan G. Food Chem Toxicol 49: 233-237.
26. Banwell JG, Howard R, Cooper D, Costerton JW (1985) Intestinal microbial flora after feeding phytohemagglutinin lectins (Phaseolus vulgaris) to rats. Appl Environ Microbiol 50: 68-80.
27. Obiro WC, Zhang T, Jiang B (2008) The nutraceutical role of the Phaseolus vulgaris alpha-amylase inhibitor. Br J Nutr 100: 1-12.
28. Preuss HG (2009) Bean amylase inhibitor and other carbohydrate absorption blockers: effects on diabesity and general health. J Am Coll Nutr 28: 266-276.
29. Beutler TM, Gallagher EP, Wang C, Stahl DL, Hayes JD, et al. (1995) Induction of phase I and phase II drug metabolizing enzyme mRNA, protein and activity by BHA, ethoxyquin and oltipraz. Toxicol Appl Pharmacol 135: 45-57.
30. Hayes JD, Pulford JD (1995) The glutathione S-transferase supergene family: Regulation of GST and the contribution of the isozymes to cancer chemoprevention and drug resistance. Crit Rev Biochem Mol Biol 30: 445-600.
31. Rushmore TH, Morton MR, Pickett CB (1991) The antioxidant responsive element. J Biol Chem 266: 11632-11639.
32. Friling RS, Bensimon S, Daniel V (1990) Xenobiotic-inducible expression of murine glutathione S-transferase Ya subunit gene is controlled by an electrophile-responsive element. Proc Natl Acad Sci USA 87: 6258-6262.
33. Moi P, Chan K, Asunis I, Cao A, Kan YW (1994) Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc Natl Acad Sci USA 91: 9926-9930.
34. Itoh K, Ishii T, Wakabayashi N, Yamamoto M (1999) Regulatory mechanisms of cellular response to oxidative stress. Free Radic Res 31: 319-324.
35. Gwarzo MY (2009) Nrf2 transcription factor gene regulates basal transcription of mitochondrial superoxide dismutase enzyme in mouse brain. Afr J Biotechnol 8: 5169-5172.
36. Cao Z, Li Y (2004) Potent induction of cellular antioxidants and phase 2 enzymes by resveratrol in cardiomyocytes: protection against oxidative and electrophilic injury. Eur J Pharmacol 489: 39-48.
37. Felice F, Lucchesi D, di Stefano R, Barsotti MC, Storti E, et al. (2010) Oxidative stress in response to high glucose levels in endothelial cells and in endothelial progenitor cells: evidence for differential glutathione peroxidase-1 expression. Microvasc Res 80: 332-338.
38. Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of folinciocalteu reagent. Methods Enzymol 299: 152-178.
39. Everette JD, Bryant QM, Green AM, Abbey YA, Wangila GW, et al. (2010) Thorough study of reactivity of various compound classes towards the Folin- Ciocalteau Reagent. J Agric Food Chem 58: 8139-8144.
40. Lee KW, Kim YJ, Kim DO, Lee HJ, Lee CY (2003) Major phenolics in apple and their contribution to the total antioxidant capacity. J Agric Food Chem 51: 6516-20.
41. Huang D, Ou B, Hampsch-Woodill M, Flanagan JA, Prior RL (2002) Highthroughput assay of oxygen radical absorbance capacity (ORAC) using a nultichannel liquid handling system coupled with a microplate fluorescence reader in 96-well format. J Agric Food Chem 50: 4437-4444.
42. Urbich C, Dimmeler S (2004) Endothelial progenitor cells: characterization and role in vascular biology. Circulation Research 95: 343-353.
43. Lin CP, Lin FY, Huang PH, Chen YL, Chen WC, et al. (2013) Endothelial progenitor cell dysfunction in cardiovascular diseases: role of reactive oxygen species and inflammation. Biomed Res Int 2013: 845037.
44. Albiero M, Menegazzo L, Avogaro A, Fadini GP (2010) Pharmacologic targeting of endothelial progenitor cells. Cardiovasc Hematol Disord Drug Targets 10: 16-32.
45. Desouza CV (2013) Does drug therapy reverse endothelial progenitor cell dysfunction in diabetes? J Diabetes Complications 27: 519-25.
46. Heart Protection Study Collaborative Group (2002) MRC/BHF Heart Protection Study of antioxidant vitamin supplementation in 20,536 high-risk individuals: a randomised placebo-controlled trial. Lancet. 2002 Jul 6; 360(9326): 23-33.
47. ORIGIN Trial Investigators, Bosch J, Gerstein HC, Dagenais GR, Díaz R, et al. (2012) n-3 fatty acids and cardiovascular outcomes in patients with dysglycemia. N Engl J Med 367: 309-318.
48. Madonna R, De Caterina R (2011) Cellular and molecular mechanisms of vascular injury in diabetes part II: cellular mechanisms and therapeutic targets. Vascul Pharmacol 54: 75-79.
49. Zhu J, Wang X, Shang Y, Xie X, Zhang F, et al. (2008) Puerarin reduces endothelial progenitor cells senescence through augmentation of telomerase activity. Vasc Pharmacol 49: 106-110.
50. Hamed S, Alshiek J, Aharon A, Brenner B, Roguin A (2010) Red wine consumption improves in vitro migration of endothelial progenitor cells in young, healthy individuals. Am J Clin Nutr 92: 161-169.
51. Xu MG, Wang JM, Chen L, Wang Y, Yang Z, et al. (2009) Berberine-induced upregulation of circulating endothelial progenitor cells is related to nitric oxide production in healthy subjects. Cardiology 112: 279-286.
52. Li YJ, Duan CL, Liu JX, Xu YG (2010) Pro-angiogenic actions of Salvianolic acids on in vitro cultured endothelial progenitor cells and chick embryo chorioallantoic membrane model. J Ethnopharmacol 131: 562-566.
53. He W, Wu WK, Wu YL, Yang XH, Lin QX, et al. (2011) Ginsenoside-Rg1 mediates microenvironment-dependent endothelial differentiation of human mesenchymal stem cells in vitro. J Asian Nat Prod Res 13: 1-11.
54. Turgeon J, Dussault S, Maingrette F, Groleau J, Haddad P, et al. (2013) Fish oilenriched diet protects against ischemia by improving angiogenesis, endothelial progenitor cell function and postnatal neovascularization. Atherosclerosis. Aug; 229(2): 295-303.
55. Tang Y, Vater C, Jacobi A, Liebers C, Zou X, et al. (2014) Salidroside exerts angiogenic and cytoprotective effects towards human bone marrow derived endothelial progenitor cells via Akt/mTOR/p70S6 K and MAPK signaling pathways. Br J Pharmacol Jan 29. doi:10.1111/bph.12611.
56. Urbich C, Dernbach E, Zeiher AM, Dimmeler S (2002) Double-edged role of statins in angiogenesis signaling. Circ Res 90: 737-744.
57. Pasciu V, Posadiono AM, Cossu A, Sanna B, Tadolini B, et al. (2010) Akt downregulation by flavin oxidase-induced ROS generation mediates dosedependent endothelial cell damage elicited by natural antioxidants. Toxicol Sci 114: 101-112.
58. Marin C, Yubero-Serrano EM, Lopez-Miranda J, Perez-Jimenez F (2013) Endothelial aging associated with oxidative stress can be modulated by a healthy Mediterranean diet. Int J Mol Sci 14: 8869-8889.
59. Alfadda AA, Sallam RM (2012) Reactive oxygen species in health and disease. J Biomed Biotechnol 2012: ID 936486, doi:10.1155/2012/936486.
60. He T, Peterson TE, Holmuhamedov EL, Terzic A, Caplice NM, et al. (2004) Human endothelial progenitor cells tolerate oxidative stress due to intrinsically high expression of manganese superoxide dismutase. Arterioscler Thromb Vasc Biol 24: 2021-2027.
61. Dernbach E, Urbich C, Brandes RP, Hofmann WK, Zeiher AM, et al. (2004) Antioxidative stress associated genes in circulating progenitor cells: evidence for enhanced resistance against oxidative stress. Blood 104: 3591-3597.
62. Wang XB, Huang J, Zou JG, Su EB, Shan QJ, et al. (2007) Effects of resveratrol on number and activity of endothelial progenitor cells from human peripheral blood. Clin Exp Phramacol Physiol 34: 1109-1115.
63. Lubrano V, Baldi S, Napoli D, Longo V (2012) Beneficial effect of Lisosan G on cultured human microvascular endothelial cells exposed to oxidised low density lipoprotein. Indian J Med Res 136: 82-88.
64. Tang Y, Huang B, Sun L, Peng X, Chen X, et al. (2011) Ginkgolide B promotes proliferation and functional activities of bone marrow-derived endothelial progenitor cells: involvement of Akt/eNOS and MAPK/P38 signaling pathways. European Cells and Materials 21: 459-469.
65. Zhao M, Wang XX, Wan WH (2014) Effects of the ginkgo biloba extract on the superoxide dismutase activity and apoptosis of endothelial progenitor cells from diabetic peripheral blood. Genet Mol Res 13: 220-227.
66. Lee SH, Kim JY, Yoo SY, Kwon SM (2013) Cytoprotective effect of dieckol on human endothelial progenitor cells (hEPCs) from oxidative stress-induced apoptosis. Free Radic Res 47: 526-534.
67. 2- induced injury: involvement of antioxidation and Akt/ eNOS signaling pathways. Eur J Pharmacol 707: 87-94.
68. Chen XL, Dodd G, Thomas S, Zhang X, Wasserman MA, et al. (2006) Activation of Nrf2/ARE pathway protects endothelial cells from oxidant injury and inhibits inflammatory gene expression. Am J Physiol Heart Circ Physiol 290: H1862-H1870.
69. Saragih H, Zilian E, Jaimes Y, Paine A, Figueiredo C, et al. (2014) PECAM-1- dependent heme oxygenase-1 regulation via an Nrf2-mediated pathway in endothelial cells. Thromb Haemost Feb 6; 111(6). [Epub ahead of print].
70. Huang XS, Chen HP, Yu HH, Yan YF, Liao ZP, et al. (2014) Nrf2-dependent upregulation of antioxidative enzymes: a novel pathway for hypoxic precondi-tioning- mediated delayed cardioprotection. Mol Cell Biochem 385: 33-41.
71. Zhang T, Wang F, Xu HX, Yi L, Qin Y, et al. (2013) Activation of nuclear factor erythroid 2-related factor 2 and PPAR C plays a role in the genisteinmediated attenuation of oxidative stress-induced endothelial cell injury. Br J Nutr 109: 223-235.
72. Parkonzo A, Czerwinska ME, Kiss AK, Naruszewicz M (2013) Oleuropein and oleacein may restore biological functions of endothelial progenitor cells impaired by angiotensin II via activation of Nrf2/heme oxygenase-1 pathway. Phytomedicine 20: 1088-1094.