Premature senescence of endothelial cells upon chronic exposure to TNFα can be prevented by N-acetyl cysteine and plumericin

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Khan, Shafaat Y ^a,b   Awad, Ezzat M ^a   Oszwald, Andre ^a   Mayr, Manuel ^c   Yin, Xiaoke ^c   Waltenberger, Birgit ^d   Stuppner, Hermann ^d   Lipovac, Markus ^e   Uhrin, Pavel ^a   Breuss, Johannes M ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF SARGODHA   (Pakistan)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF INNSBRUCK   (Austria)

^e Karl Landsteiner Institute for Cell based Therapy in Gynecology   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; REACTIVE OXYGEN METABOLITE; SCAVENGER; TUMOR NECROSIS FACTOR;

CELL AGING; CELL CYCLE CHECKPOINT; CELL PROLIFERATION; CHEMICALLY INDUCED; DRUG EFFECT; ENDOTHELIUM CELL; HUMAN; INFLAMMATION; METABOLISM; PHENOTYPE; SIGNAL TRANSDUCTION;

ACETYLCYSTEINE; CELL CYCLE CHECKPOINTS; CELL PROLIFERATION; CELLULAR SENESCENCE; ENDOTHELIAL CELLS; FREE RADICAL SCAVENGERS; HUMANS; INFLAMMATION; NF-KAPPA B; PHENOTYPE; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85008313698     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep39501     Document Type: Article

References (69)

1. National Center for Health, S. In Health, United States, 2010: With Special Feature on Death and Dying (National Center for Health Statistics (US) (2011).
2. Galley, H. F. & Webster, N. R. Physiology of the endothelium. Br J Anaesth 93, 105-113, doi: 10.1093/bja/aeh163 (2004).
3. Rodier, F. & Campisi, J. Four faces of cellular senescence. The Journal of cell biology 192, 547-556, doi: 10.1083/jcb.201009094 (2011).
4. Minamino, T. et al. Endothelial cell senescence in human atherosclerosis: role of telomere in endothelial dysfunction. Circulation 105, 1541-1544 (2002).
5. Hayashi, T. & Iguchi, A. Possibility of the regression of atherosclerosis through the prevention of endothelial senescence by the regulation of nitric oxide and free radical scavengers. Geriatrics & gerontology international 10, 115-130, doi: 10.1111/j.1447-0594.2009.00581.x (2010).
6. Donato, A. J., Morgan, R. G., Walker, A. E. & Lesniewski, L. A. Cellular and molecular biology of aging endothelial cells. J Mol Cell Cardiol 89, 122-135, doi: 10.1016/j.yjmcc.2015.01.021 (2015).
7. Maier, J. A., Statuto, M. & Ragnotti, G. Senescence stimulates U937-endothelial cell interactions. Experimental cell research 208, 270-274, doi: 10.1006/excr.1993.1246 (1993).
8. Nakajima, M. et al. Aging decreases the production of PGI2 in rat aortic endothelial cells. Experimental gerontology 32, 685-693 (1997).
9. Di Leonardo, A., Linke, S. P., Clarkin, K. & Wahl, G. M. DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes & development 8, 2540-2551 (1994).
10. Valenzuela, M. T. et al. A comparison of p53 and p16 expression in human tumor cells treated with hyperthermia or ionizing radiation. International journal of cancer. Journal international du cancer 72, 307-312 (1997).
11. Counter, C. M. et al. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. The EMBO journal 11, 1921-1929 (1992).
12. Chung, H. Y., Kim, H. J., Kim, K. W., Choi, J. S. & Yu, B. P. Molecular inflammation hypothesis of aging based on the anti-aging mechanism of calorie restriction. Microscopy research and technique 59, 264-272, doi: 10.1002/jemt.10203 (2002).
13. Vasto, S. et al. Inflammatory networks in ageing, age-related diseases and longevity. Mechanisms of ageing and development 128, 83-91, doi: 10.1016/j.mad.2006.11.015 (2007).
14. Rogers, S. C., Zhang, X., Azhar, G., Luo, S. & Wei, J. Y. Exposure to high or low glucose levels accelerates the appearance of markers of endothelial cell senescence and induces dysregulation of nitric oxide synthase. The journals of gerontology. Series A, Biological sciences and medical sciences 68, 1469-1481, doi: 10.1093/gerona/glt033 (2013).
15. Matsui-Hirai, H. et al. Dose-dependent modulatory effects of insulin on glucose-induced endothelial senescence in vitro and in vivo: a relationship between telomeres and nitric oxide. The Journal of pharmacology and experimental therapeutics 337, 591-599, doi: 10.1124/jpet.110.177584 (2011).
16. Dumont, P., Balbeur, L., Remacle, J. & Toussaint, O. Appearance of biomarkers of in vitro ageing after successive stimulation of WI-38 fibroblasts with IL-1alpha and TNF-alpha: senescence associated beta-galactosidase activity and morphotype transition. Journal of anatomy 197 Pt 4, 529-537 (2000).
17. Kojima, H., Kunimoto, H., Inoue, T. & Nakajima, K. The STAT3-IGFBP5 axis is critical for IL-6/gp130-induced premature senescence in human fibroblasts. Cell cycle (Georgetown, Tex.) 11, 730-739, doi: 10.4161/cc.11.4.19172 (2012).
18. Sharpless, N. E. & Sherr, C. J. Forging a signature of in vivo senescence. Nat Rev Cancer 15, 397-408, doi: 10.1038/nrc3960 (2015).
19. Chen, J. et al. Contribution of p16INK4a and p21CIP1 pathways to induction of premature senescence of human endothelial cells: permissive role of p53. American journal of physiology. Heart and circulatory physiology 290, H1575-1586, doi: 10.1152/ ajpheart.00364.2005 (2006).
20. Beausejour, C. M. et al. Reversal of human cellular senescence: roles of the p53 and p16 pathways. The EMBO journal 22, 4212-4222, doi: 10.1093/emboj/cdg417 (2003).
21. Rodier, F. et al. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nature cell biology 11, 973-979, doi: 10.1038/ncb1909 (2009).
22. Rodier, F. et al. DNA-SCARS: distinct nuclear structures that sustain damage-induced senescence growth arrest and inflammatory cytokine secretion. Journal of cell science 124, 68-81, doi: 10.1242/jcs.071340 (2011).
23. Salminen, A., Kauppinen, A. & Kaarniranta, K. Emerging role of NF-kappaB signaling in the induction of senescence-associated secretory phenotype (SASP). Cellular signalling 24, 835-845, doi: 10.1016/j.cellsig.2011.12.006 (2012).
24. Tilstra, J. S. et al. NF-kappaB inhibition delays DNA damage-induced senescence and aging in mice. The Journal of clinical investigation 122, 2601-2612, doi: 10.1172/JCI45785 (2012).
25. Coppe, J. P. et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS biology 6, 2853-2868, doi: 10.1371/journal.pbio.0060301 (2008).
26. Hubackova, S., Krejcikova, K., Bartek, J. & Hodny, Z. IL1-and TGFbeta-Nox4 signaling, oxidative stress and DNA damage response are shared features of replicative, oncogene-induced, and drug-induced paracrine 'bystander senescence'. Aging 4, 932-951 (2012).
27. Prattichizzo, F. et al. Anti-TNF-alpha treatment modulates SASP and SASP-related microRNAs in endothelial cells and in circulating angiogenic cells. Oncotarget 7, 11945-11958, doi: 10.18632/oncotarget.7858 (2016).
28. Bruunsgaard, H., Skinhoj, P., Pedersen, A. N., Schroll, M. & Pedersen, B. K. Ageing, tumour necrosis factor-alpha (TNF-alpha) and atherosclerosis. Clinical and experimental immunology 121, 255-260 (2000).
29. Csiszar, A., Ungvari, Z., Koller, A., Edwards, J. G. & Kaley, G. Proinflammatory phenotype of coronary arteries promotes endothelial apoptosis in aging. Physiological genomics 17, 21-30, doi: 10.1152/physiolgenomics.00136.2003 (2004).
30. Kristiansen, O. P. & Mandrup-Poulsen, T. Interleukin-6 and diabetes: the good, the bad, or the indifferent? Diabetes 54 Suppl 2, S114-124 (2005).
31. Kim, J. J., Lee, S. B., Park, J. K. & Yoo, Y. D. TNF-alpha-induced ROS production triggering apoptosis is directly linked to Romo1 and Bcl-X(L). Cell death and differentiation 17, 1420-1434, doi: 10.1038/cdd.2010.19 (2010).
32. Pober, J. S. & Sessa, W. C. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 7, 803-815, doi: 10.1038/ nri2171 (2007).
33. Mbalaviele, G. et al. A novel, highly selective, tight binding IkappaB kinase-2 (IKK-2) inhibitor: a tool to correlate IKK-2 activity to the fate and functions of the components of the nuclear factor-kappaB pathway in arthritis-relevant cells and animal models. The Journal of pharmacology and experimental therapeutics 329, 14-25, doi: 10.1124/jpet.108.143800 (2009).
34. Fakhrudin, N. et al. Identification of plumericin as a potent new inhibitor of the NF-kappaB pathway with anti-inflammatory activity in vitro and in vivo. British journal of pharmacology 171, 1676-1686, doi: 10.1111/bph.12558 (2014).
35. Zafarullah, M., Li, W. Q., Sylvester, J. & Ahmad, M. Molecular mechanisms of N-acetylcysteine actions. Cell Mol Life Sci 60, 6-20 (2003).
36. Sun, S. Y. N-acetylcysteine, reactive oxygen species and beyond. Cancer biology & therapy 9, 109-110 (2010).
37. Hampel, B. et al. Increased expression of extracellular proteins as a hallmark of human endothelial cell in vitro senescence. Experimental gerontology 41, 474-481, doi: 10.1016/j.exger.2006.03.001 (2006).
38. Yanaka, M. et al. Increased monocytic adhesion by senescence in human umbilical vein endothelial cells. Bioscience, biotechnology, and biochemistry 75, 1098-1103 (2011).
39. Rombouts, C. et al. Transcriptomic profiling suggests a role for IGFBP5 in premature senescence of endothelial cells after chronic low dose rate irradiation. Int J Radiat Biol 90, 560-574, doi: 10.3109/09553002.2014.905724 (2014).
40. Wu, Z. et al. Role of p38 mitogen-activated protein kinase in vascular endothelial aging: interaction with Arginase-II and S6K1 signaling pathway. Aging 7, 70-81 (2015).
41. Balwani, S., Nandi, D., Jaisankar, P. & Ghosh, B. 2-Methyl-pyran-4-one-3-O-beta-D-glucopyranoside isolated from leaves of Punica granatum inhibits the TNFalpha-induced cell adhesion molecules expression by blocking nuclear transcription factor-kappaB (NF-kappaB). Biochimie 93, 921-930, doi: 10.1016/j.biochi.2011.01.010 (2011).
42. Passos, J. F., Miwa, S. & von Zglinicki, T. Measuring reactive oxygen species in senescent cells. Methods Mol Biol 965, 253-263, doi: 10.1007/978-1-62703-239-1-17 (2013).
43. Davalli, P., Mitic, T., Caporali, A., Lauriola, A. & D'Arca, D. ROS, Cell Senescence, and Novel Molecular Mechanisms in Aging and Age-Related Diseases. Oxidative medicine and cellular longevity 2016, 3565127, doi: 10.1155/2016/3565127 (2016).
44. Awad, E. M. et al. Cold induces reactive oxygen species production and activation of the NF-kappa B response in endothelial cells and inflammation in vivo. Journal of thrombosis and haemostasis: JTH 11, 1716-1726, doi: 10.1111/jth.12357 (2013).
45. Ellis, J. A., Mayer, S. J. & Jones, O. T. The effect of the NADPH oxidase inhibitor diphenyleneiodonium on aerobic and anaerobic microbicidal activities of human neutrophils. The Biochemical journal 251, 887-891 (1988).
46. Beyne-Rauzy, O. et al. Tumor necrosis factor alpha induces senescence and chromosomal instability in human leukemic cells. Oncogene 23, 7507-7516, doi: 10.1038/sj.onc.1208024 (2004).
47. Zhang, Y. et al. Premature senescence of highly proliferative endothelial progenitor cells is induced by tumor necrosis factor-alpha via the p38 mitogen-activated protein kinase pathway. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 23, 1358-1365, doi: 10.1096/fj.08-110296 (2009).
48. Shimada, Y., Ito, H., Kaji, K. & Fukuda, M. Tumor necrosis factor reduces lifespan of human endothelial cells in vitro. Mechanisms of ageing and development 55, 245-254 (1990).
49. Yamagata, K., Suzuki, S. & Tagami, M. Docosahexaenoic acid prevented tumor necrosis factor alpha-induced endothelial dysfunction and senescence. Prostaglandins Leukot Essent Fatty Acids 104, 11-18, doi: 10.1016/j.plefa.2015.10.006 (2016).
50. Maciel-Baron, L. A. et al. Senescence associated secretory phenotype profile from primary lung mice fibroblasts depends on the senescence induction stimuli. Age (Dordrecht, Netherlands) 38, 26, doi: 10.1007/s11357-016-9886-1 (2016).
51. Coppe, J. P., Desprez, P. Y., Krtolica, A. & Campisi, J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 5, 99-118, doi: 10.1146/annurev-pathol-121808-102144 (2010).
52. Kortlever, R. M., Higgins, P. J. & Bernards, R. Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence. Nature cell biology 8, 877-884, doi: 10.1038/ncb1448 (2006).
53. Medina, R. J. et al. Ex vivo expansion of human outgrowth endothelial cells leads to IL-8-mediated replicative senescence and impaired vasoreparative function. Stem cells (Dayton, Ohio) 31, 1657-1668, doi: 10.1002/stem.1414 (2013).
54. Chen, X. et al. Role of Reactive Oxygen Species in Tumor Necrosis Factor-alpha Induced Endothelial Dysfunction. Current hypertension reviews 4, 245-255 (2008).
55. Zinovkin, R. A. et al. Role of mitochondrial reactive oxygen species in age-related inflammatory activation of endothelium. Aging 6, 661-674 (2014).
56. Yan, S. et al. Clematichinenoside inhibits VCAM-1 and ICAM-1 expression in TNF-alpha-treated endothelial cells via NADPH oxidase-dependent IkappaB kinase/NF-kappaB pathway. Free radical biology & medicine 78, 190-201, doi: 10.1016/j. freeradbiomed.2014.11.004 (2015).
57. Li, J. M., Fan, L. M., Christie, M. R. & Shah, A. M. Acute tumor necrosis factor alpha signaling via NADPH oxidase in microvascular endothelial cells: role of p47phox phosphorylation and binding to TRAF4. Mol Cell Biol 25, 2320-2330, doi: 10.1128/ MCB.25.6.2320-2330.2005 (2005).
58. Corda, S., Laplace, C., Vicaut, E. & Duranteau, J. Rapid reactive oxygen species production by mitochondria in endothelial cells exposed to tumor necrosis factor-alpha is mediated by ceramide. Am J Respir Cell Mol Biol 24, 762-768, doi: 10.1165/ ajrcmb.24.6.4228 (2001).
59. Sen, C. K. & Packer, L. Antioxidant and redox regulation of gene transcription. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 10, 709-720 (1996).
60. Morgan, M. J. & Liu, Z. G. Crosstalk of reactive oxygen species and NF-kappaB signaling. Cell research 21, 103-115, doi: 10.1038/ cr.2010.178 (2011).
61. Li, Y. & Trush, M. A. Diphenyleneiodonium, an NAD(P)H oxidase inhibitor, also potently inhibits mitochondrial reactive oxygen species production. Biochemical and biophysical research communications 253, 295-299, doi: 10.1006/bbrc.1998.9729 (1998).
62. Ladner, K. J., Caligiuri, M. A. & Guttridge, D. C. Tumor necrosis factor-regulated biphasic activation of NF-kappa B is required for cytokine-induced loss of skeletal muscle gene products. The Journal of biological chemistry 278, 2294-2303, doi: 10.1074/jbc. M207129200 (2003).
63. Heiss, E. H. et al. Plumericin inhibits proliferation of vascular smooth muscle cells by blocking STAT3 signaling via S-glutathionylation. Sci Rep 6, 20771, doi: 10.1038/srep20771 (2016).
64. Chen, K. H., Reece, L. M. & Leary, J. F. Mitochondrial glutathione modulates TNF-alpha-induced endothelial cell dysfunction. Free radical biology & medicine 27, 100-109 (1999).
65. Friedrichs, B., Muller, C. & Brigelius-Flohe, R. Inhibition of tumor necrosis factor-alpha-and interleukin-1-induced endothelial E-selectin expression by thiol-modifying agents. Arteriosclerosis, thrombosis, and vascular biology 18, 1829-1837 (1998).
66. Waltenberger, B., Rollinger, J. M., Griesser, U. J., Stuppner, H. & Gelbrich, T. Plumeridoid C from the Amazonian traditional medicinal plant Himatanthus sucuuba. Acta crystallographica. Section C, Crystal structure communications 67, o409-412, doi: 10.1107/s0108270111035761 (2011).
67. Crampton, S. P., Davis, J. & Hughes, C. C. Isolation of human umbilical vein endothelial cells (HUVEC). Journal of visualized experiments: JoVE, 183, doi: 10.3791/183 (2007).
68. Richard, L., Velasco, P. & Detmar, M. A simple immunomagnetic protocol for the selective isolation and long-term culture of human dermal microvascular endothelial cells. Experimental cell research 240, 1-6, doi: 10.1006/excr.1998.3936 (1998).
69. Mechtcheriakova, D., Wlachos, A., Holzmuller, H., Binder, B. R. & Hofer, E. Vascular endothelial cell growth factor-induced tissue factor expression in endothelial cells is mediated by EGR-1. Blood 93, 3811-3823 (1999).