Nanomolar caffeic acid decreases glucose uptake and the effects of high glucose in endothelial cells

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Natarelli, Lucia ^a,d   Ranaldi, Giulia ^a   Leoni, Guido ^b   Roselli, Marianna ^a   Guantario, Barbara ^a   Comitato, Raffaella ^a   Ambra, Roberto ^a   Cimino, Francesco ^c   Speciale, Antonio ^c   Virgili, Fabio ^a   Canali, Raffaella ^a  

^a National Institute for Research in Food and Nutrition   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF MESSINA   (Italy)

^d LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CAFFEIC ACID; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; GLUCOSE; GLUCOSE TRANSPORTER 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; PROTEIN BCL 2; SYNAPTOTAGMIN I; CAFFEIC ACID DERIVATIVE; SLC2A1 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GENE EXPRESSION; GLUCOSE TRANSPORT; GLUT 1 GENE; HUMAN; HUMAN CELL; METABOLIC STRESS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; CELL LINE; DRUG EFFECTS; GENETICS; METABOLISM; PERMEABILITY; UMBILICAL VEIN ENDOTHELIAL CELL;

APOPTOSIS; CAFFEIC ACIDS; CELL LINE; ENDOTHELIAL CELLS; GLUCOSE; GLUCOSE TRANSPORTER TYPE 1; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; NF-KAPPA B; PERMEABILITY; RNA, MESSENGER;

EID: 84952684646     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142421     Document Type: Article

References (54)

1. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001;414(6865):813-20. Epub 2001/12/14. PMID: 11742414
2. de Jongh RT, Serne EH, Jzerman RG, de Vries G, Stehouwer CD. Impaired microvascular function in obesity: implications for obesity-associated microangiopathy, hypertension, and insulin resistance. Circulation. 2004;109(21):2529-35. PMID: 15136505
3. Nobe K, Miyatake M, Sone T, Honda K. High-glucose-altered endothelial cell function involves both disruption of cell-to-cell connection and enhancement of force development. J Pharmacol Exp Ther. 2006;318(2):530-9. Epub 2006/05/16. PMID: 16699065
4. Hempel A, Maasch C, Heintze U, Lindschau C, Dietz R, Luft FC, et al. High glucose concentrations increase endothelial cell permeability via activation of protein kinase C alpha. Circulation research. 1997;81(3):363-71. Epub 1997/09/01. PMID: 9285638
5. Baumgartner-Parzer SM, Wagner L, Pettermann M, Grillari J, Gessl A, WaldhauslW. High-glucose-triggered apoptosis in cultured endothelial cells. Diabetes. 1995;44(11):1323-7. Epub 1995/11/01. PMID: 7589831
6. Frustaci A, Kajstura J, Chimenti C, Jakoniuk I, Leri A, Maseri A, et al. Myocardial cell death in human diabetes. Circulation research. 2000;87(12):1123-32. Epub 2000/01/11. PMID: 11110769
7. Miele C, Paturzo F, Teperino R, Sakane F, Fiory F, Oriente F, et al. Glucose regulates diacylglycerol intracellular levels and protein kinase C activity by modulating diacylglycerol kinase subcellular localization. The Journal of biological chemistry. 2007;282(44):31835-43. Epub 2007/08/07. PMID: 17675299
8. Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation. 2006;114(6):597-605. Epub 2006/08/09. PMID: 16894049
9. Kishimoto Y, Tani M, Kondo K. Pleiotropic preventive effects of dietary polyphenols in cardiovascular diseases. Eur J Clin Nutr. 2013;67(5):532-5. Epub 2013/02/14. doi:10.1038/ejcn. 2013.29 PMID: 23403879
10. Vauzour D, Rodriguez-Mateos A, Corona G, Oruna-Concha MJ, Spencer JP. Polyphenols and human health: prevention of disease and mechanisms of action. Nutrients. 2010;2(11):1106-31. Epub 2010/11/01. doi:10.3390/nu2111106 PMID: 22254000
11. Tunnicliffe JM, Shearer J. Coffee, glucose homeostasis, and insulin resistance: physiological mechanisms and mediators. Appl Physiol Nutr Metab. 2008;33(6):1290-300. Epub 2008/12/18. doi:10.1139/H08-123 PMID: 19088791
12. van Dam RM, Hu FB. Coffee consumption and risk of type 2 diabetes: a systematic review. Jama. 2005;294(1):97-104. Epub 2005/07/07. PMID: 15998896
13. Yochum L, Kushi LH, Meyer K, Folsom AR. Dietary flavonoid intake and risk of cardiovascular disease in postmenopausal women. Am J Epidemiol. 1999;149(10):943-9. Epub 1999/05/26. PMID: 10342803
14. Nardini M, Cirillo E, Natella F, Scaccini C. Absorption of phenolic acids in humans after coffee consumption. J Agric Food Chem. 2002;50(20):5735-41. Epub 2002/09/19. PMID: 12236707
15. Edgell CJ, McDonald CC, Graham JB. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proceedings of the National Academy of Sciences of the United States of America. 1983;80(12):3734-7. Epub 1983/06/01. PMID: 6407019
16. Tobin NP, Henehan GT, Murphy RP, Atherton JC, Guinan AF, Kerrigan SW, et al. Helicobacter pyloriinduced inhibition of vascular endothelial cell functions: a role for VacA-dependent nitric oxide reduction. American journal of physiology Heart and circulatory physiology. 2008;295(4):H1403-13. Epub 2008/07/29. doi:10.1152/ajpheart.00240.2008 PMID: 18660451
17. Ranaldi G, Ferruzza S, Canali R, Leoni G, Zalewski PD, Sambuy Y, et al. Intracellular zinc is required for intestinal cell survival signals triggered by the inflammatory cytokine TNFalpha. The Journal of nutritional biochemistry. 2013;24(6):967-76. Epub 2012/09/13. doi:10.1016/j.jnutbio.2012.06.020 PMID: 22967671
18. Lee H, Yeh F, Wu C. The effect of elevated extracellular glucose on adherens junction proteins in cultured rat heart endothelial cells. Life sciences. 2004;74(17):2085-96. PMID: 14969714
19. Cerami EG, Gross BE, Demir E, Rodchenkov I, Babur O, Anwar N, et al. Pathway Commons, a web resource for biological pathway data. Nucleic acids research. 2011;39(Database issue):D685-90. Epub 2010/11/13. doi:10.1093/nar/gkq1039 PMID: 21071392
20. Ruvolo PP, Deng X, May WS. Phosphorylation of Bcl-2 and regulation of apoptosis. Leukemia. 2001;15(4):515-22. Epub 2001/05/23. PMID: 11368354
21. Nourbakhsh M, Hauser H. Constitutive silencing of IFN-beta promoter is mediated by NRF (NF-kappaB-repressing factor), a nuclear inhibitor of NF-kappaB. The EMBO journal. 1999;18(22):6415-25. PMID: 10562553
22. Hindley A, Kolch W. Extracellular signal regulated kinase (ERK)/mitogen activated protein kinase (MAPK)-independent functions of Raf kinases. J Cell Sci. 2002;115(Pt 8):1575-81. PMID: 11950876
23. Chen ZJ. Ubiquitin signalling in the NF-kappaB pathway. Nature cell biology. 2005;7(8):758-65. Epub 2005/08/02. PMID: 16056267
24. Wegener E, Krappmann D. CARD-Bcl10-Malt1 signalosomes: missing link to NF-kappaB. Sci STKE. 2007;384:pe21.
25. Munshi N, Fernandis AZ, Cherla RP, Park IW, Ganju RK. Lipopolysaccharide-induced apoptosis of endothelial cells and its inhibition by vascular endothelial growth factor. J Immunol. 2002;168(11):5860-6. Epub 2002/05/23. PMID: 12023390
26. Bhupathiraju SN, Pan A, Malik VS, Manson JE, Willett WC, van Dam RM, et al. Caffeinated and caffeine-free beverages and risk of type 2 diabetes. The American journal of clinical nutrition. 2013;97(1):155-66. Epub 2012/11/16. doi:10.3945/ajcn. 112.048603 PMID: 23151535
27. van Dam RM, Pasman WJ, Verhoef P. Effects of coffee consumption on fasting blood glucose and insulin concentrations: randomized controlled trials in healthy volunteers. Diabetes care. 2004;27(12):2990-2. Epub 2004/11/25. PMID: 15562223
28. Natella F, Scaccini C. Role of coffee in modulation of diabetes risk. Nutr Rev. 2012;70(4):207-17. Epub 2012/03/31. PMID: 22458694
29. Kang NJ, Lee KW, Shin BJ, Jung SK, Hwang MK, Bode AM, et al. Caffeic acid, a phenolic phytochemical in coffee, directly inhibits Fyn kinase activity and UVB-induced COX-2 expression. Carcinogenesis. 2009;30(2):321-30. Epub 2008/12/17. doi:10.1093/carcin/bgn282 PMID: 19073879
30. Vacaresse N, Vieira O, Robbesyn F, Jurgens G, Salvayre R, Negre-Salvayre A. Phenolic antioxidants trolox and caffeic acid modulate the oxidized LDL-induced EGF-receptor activation. Br J Pharmacol. 2001;132(8):1777-88. Epub 2001/04/20. PMID: 11309250
31. Bauer J, Margolis M, Schreiner C, Edgell CJ, Azizkhan J, Lazarowski E, et al. In vitro model of angiogenesis using a human endothelium-derived permanent cell line: contributions of induced gene expression, G-proteins, and integrins. J Cell Physiol 1992;153(3):437-9. PMID: 1280276
32. Busik JV, Olson LK, Grant MB, Henry DN. Glucose-induced activation of glucose uptake in cells from the inner and outer blood-retinal barrier. Invest Ophthalmol Vis Sci. 2002;43(7):2356-63. Epub 2002/07/02. PMID: 12091438
33. Alpert E, Gruzman A, Totary H, Kaiser N, Reich R, Sasson S. A natural protective mechanism against hyperglycaemia in vascular endothelial and smooth-muscle cells: role of glucose and 12-hydroxyeicosatetraenoic acid. Biochem J. 2002;362(Pt 2):413-22. Epub 2002/02/21. PMID: 11853550
34. Alpert E, Gruzman A, Riahi Y, Blejter R, Aharoni P, Weisinger G, et al. Delayed autoregulation of glucose transport in vascular endothelial cells. Diabetologia. 2005;48(4):752-5. Epub 2005/03/02. PMID: 15739115
35. Cohen G, Riahi Y, Alpert E, Gruzman A, Sasson S. The roles of hyperglycaemia and oxidative stress in the rise and collapse of the natural protective mechanism against vascular endothelial cell dysfunction in diabetes. Arch Physiol Biochem. 2007;113(4-5):259-67. Epub 2007/12/26. PMID: 18158647
36. Huang DW, Shen SC, Wu JS. Effects of caffeic acid and cinnamic acid on glucose uptake in insulinresistant mouse hepatocytes. J Agric Food Chem. 2009;57(17):7687-92. Epub 2009/08/19. doi:10. 1021/jf901376x PMID: 19685889
37. Welsch CA, Lachance PA, Wasserman BP. Dietary phenolic compounds: inhibition of Na+-dependent D-glucose uptake in rat intestinal brush border membrane vesicles. The Journal of nutrition. 1989;119(11):1698-704. Epub 1989/11/01. PMID: 2600675
38. Riahi Y, Sin-Malia Y, Cohen G, Alpert E, Gruzman A, Eckel J, et al. The natural protective mechanism against hyperglycemia in vascular endothelial cells: roles of the lipid peroxidation product 4-hydroxydodecadienal and peroxisome proliferator-activated receptor delta. Diabetes. 2010;59(4):808-18. Epub 2010/01/29. doi:10.2337/db09-1207 PMID: 20107107
39. Kaiser N, Sasson S, Feener EP, Boukobza-Vardi N, Higashi S, Moller DE, et al. Differential regulation of glucose transport and transporters by glucose in vascular endothelial and smooth muscle cells. Diabetes. 1993;42(1):80-9. Epub 1993/01/01. PMID: 7678404
40. Duffy A, Liew A, O'Sullivan J, Avalos G, Samali A, O'Brien T. Distinct effects of high-glucose conditions on endothelial cells of macrovascular and microvascular origins. Endothelium: journal of endothelial cell research. 2006;13(1):9-16. Epub 2006/08/04.
41. Nakagami H, Morishita R, Yamamoto K, Yoshimura SI, Taniyama Y, Aoki M, et al. Phosphorylation of p38 mitogen-activated protein kinase downstream of bax-caspase-3 pathway leads to cell death induced by high D-glucose in human endothelial cells. Diabetes. 2001;50(6):1472-81. Epub 2001/05/26. PMID: 11375350
42. Salameh A, Zinn M, Dhein S. High D-glucose induces alterations of endothelial cell structure in a cellculture model. Journal of cardiovascular pharmacology. 1997;30(2):182-90. Epub 1997/08/01. PMID: 9269945
43. Davidson SM, Yellon DM. Does hyperglycemia reduce proliferation or increase apoptosis? American journal of physiology Heart and circulatory physiology. 2006;291(3):H1486; author reply H7. Epub 2006/04/18. PMID: 16617134
44. Sheu ML, Ho FM, Yang RS, Chao KF, Lin WW, Lin-Shiau SY, et al. High glucose induces human endothelial cell apoptosis through a phosphoinositide 3-kinase-regulated cyclooxygenase-2 pathway. Arterioscler Thromb Vasc Biol. 2005;25(3):539-45. Epub 2005/01/18. PMID: 15653566
45. McIlwain DR, Berger T, Mak TW. Caspase functions in cell death and disease. Cold Spring Harbor perspectives in biology. 2013;5(4):a008656. Epub 2013/04/03. doi:10.1101/cshperspect.a008656 PMID: 23545416
46. Swanton E, Savory P, Cosulich S, Clarke P, Woodman P. Bcl-2 regulates a caspase-3/caspase-2 apoptotic cascade in cytosolic extracts. Oncogene. 1999;18(10):1781-7. Epub 1999/03/23. PMID: 10086332
47. Sprick MR, Walczak H. The interplay between the Bcl-2 family and death receptor-mediated apoptosis. Biochim Biophys Acta 2004;1644(2-3):125-32. PMID: 14996497
48. Chang WC, Hsieh CH, Hsiao MW, Lin WC, Hung YC, Ye JC. Caffeic acid induces apoptosis in human cervical cancer cells through the mitochondrial pathway. Taiwan J Obstet Gynecol. 2010;49(4):419-24. Epub 2011/01/05. doi:10.1016/S1028-4559 (10) 60092-7 PMID: 21199742
49. Ho FM, Lin WW, Chen BC, Chao CM, Yang CR, Lin LY, et al. High glucose-induced apoptosis in human vascular endothelial cells is mediated through NF-kappaB and c-Jun. NH2-terminal kinase pathway and prevented by PI3K/Akt/eNOS pathway. Cell Signal. 2006;18(3):391-9. Epub 2005/06/23. PMID: 15970429
50. Salaun B, Romero P, Lebecque S. Toll-like receptors' two-edged sword: when immunity meets apoptosis. Eur J Immunol 2007;37(12):3311-8. PMID: 18034428
51. Aliprantis AO, Yang RB, Weiss DS, Godowski P, Zychlinsky A. The apoptotic signaling pathway activated by Toll-like receptor-2. The EMBO journal. 2000;19(13):3325-36. Epub 2000/07/06. PMID: 10880445
52. Sun R, Zhang Y, Lv Q, Liu B, Jin M, Zhang W, et al. Toll-like receptor 3 (TLR3) induces apoptosis via death receptors and mitochondria by up-regulating the transactivating p63 isoform alpha (TAP63alpha). The Journal of biological chemistry. 2011;286(18):15918-28. Epub 2011/03/04. doi:10.1074/jbc. M110.178798 PMID: 21367858
53. Handa P, Tupper JC, Jordan KC, Harlan JM. FLIP (Flice-like inhibitory protein) suppresses cytoplasmic double-stranded-RNA-induced apoptosis and NF-kappaB and IRF3-mediated signaling. Cell communication and signaling: CCS. 2011;9:16. Epub 2011/06/04.
54. Kaiser WJ, Kaufman JL, Offermann MK. IFN-alpha sensitizes human umbilical vein endothelial cells to apoptosis induced by double-stranded RNA. J Immunol. 2004;172(3):1699-710. Epub 2004/01/22. PMID: 14734752