Zinc regulates Nox1 expression through a NF-κB and mitochondrial ROS dependent mechanism to induce senescence of vascular smooth muscle cells

Free Radical Biology and Medicine

Volumn 108, Issue , 2017, Pages 225-235

  Salazar, G ^a   Huang, J ^a   Feresin, R G ^b   Zhao, Y ^a   Griendling, K K ^c  

^a FLORIDA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mitochondria; NF B; Nox1; ROS; Senescence; VSMCs; Zinc; ZnT10; ZnT3

Indexed keywords

ACETYLCYSTEINE; ANGIOTENSIN II; BETA GALACTOSIDASE; CATALASE; COBALT; COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; DACTINOMYCIN; HISTONE H2AX; HISTONE H2AX GAMMA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IRON; MANGANESE; MANGANESE SUPEROXIDE DISMUTASE; PROTEIN P21; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG; ZINC; CARRIER PROTEIN; ETHYLENEDIAMINE DERIVATIVE; MEMBRANE PROTEIN; N,N,N',N'-TETRAKIS(2-PYRIDYLMETHYL)ETHYLENEDIAMINE; SLC30A3 PROTEIN, MOUSE; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; EMBRYO; ENDOSOME; ENZYME ACTIVITY; HEK293 CELL LINE; HISTONE PHOSPHORYLATION; LYSOSOME; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PC12 CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENESCENCE; TELOMERE LENGTH; UPREGULATION; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; C57BL MOUSE; CELL AGING; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; SMOOTH MUSCLE CELL; SPRAGUE DAWLEY RAT; THORACIC AORTA;

ANGIOTENSIN II; ANIMALS; AORTA, THORACIC; CARRIER PROTEINS; CELLS, CULTURED; CELLULAR SENESCENCE; DACTINOMYCIN; ETHYLENEDIAMINES; GENE EXPRESSION REGULATION; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MYOCYTES, SMOOTH MUSCLE; NADPH OXIDASE 1; NADPH OXIDASE 4; NF-KAPPA B; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; ZINC;

EID: 85016779291     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2017.03.032     Document Type: Article

References (52)

1. [1] Candore, G., Caruso, C., Colonna-Romano, G., Inflammation, genetic background and longevity. Biogerontology 11:5 (2010), 565–573.
2. [2] Tchkonia, T., et al. Cellular senescence and the senescent secretory phenotype: therapeutic opportunities. J. Clin. Investig. 123:3 (2013), 966–972.
3. [3] Kunieda, T., et al. Angiotensin II induces premature senescence of vascular smooth muscle cells and accelerates the development of atherosclerosis via a p21-dependent pathway. Circulation 114:9 (2006), 953–960.
4. [4] Patrushev, N., Seidel-Rogol, B., Salazar, G., Angiotensin II requires zinc and downregulation of the zinc transporters ZnT3 and ZnT10 to induce senescence of vascular smooth muscle cells. PLoS One, 7(3), 2012, e33211.
5. [5] Feresin, R.G., et al. Blackberry, raspberry and black raspberry polyphenol extracts attenuate angiotensin II-induced senescence in vascular smooth muscle cells. Food Funct. 7:10 (2016), 4175–4187.
6. [6] Cabrera, Á., Zinc, aging, and immunosenescence: an overview. Pathobiol. Aging Age Relat. Dis., 5, 2015, 25592.
7. [7] Prasad, A.S., et al. Zinc supplementation decreases incidence of infections in the elderly: effect of zinc on generation of cytokines and oxidative stress. Am. J. Clin. Nutr. 85:3 (2007), 837–844.
8. [8] Wong, C.P., Magnusson, K.R., Ho, E., Increased inflammatory response in aged mice is associated with age-related zinc deficiency and zinc transporter dysregulation. J. Nutr. Biochem. 24:1 (2013), 353–359.
9. [9] Reiterer, G., et al. Zinc deficiency increases plasma lipids and atherosclerotic markers in LDL-receptor-deficient mice. J. Nutr. 135:9 (2005), 2114–2118.
10. [10] Wessels, I., et al. Zinc deficiency induces production of the proinflammatory cytokines IL-1β and TNFα in promyeloid cells via epigenetic and redox-dependent mechanisms. J. Nutr. Biochem. 24:1 (2013), 289–297.
11. [11] Wong, C.P., Rinaldi, N.A., Ho, E., Zinc deficiency enhanced inflammatory response by increasing immune cell activation and inducing IL6 promoter demethylation. Mol. Nutr. Food Res. 59:5 (2015), 991–999.
12. [12] Ranasinghe, P., et al. Effects of zinc supplementation on serum lipids: a systematic review and meta-analysis. Nutr. Metab., 12, 2015, 26.
13. [13] Kumar, J., et al. Zinc levels modulate lifespan through multiple longevity pathways in Caenorhabditis elegans. PLoS One, 11(4), 2016, e0153513.
14. [14] Kambe, T., et al. The physiological, biochemical, and molecular roles of zinc transporters in zinc homeostasis and metabolism. Physiol. Rev. 95:3 (2015), 749–784.
15. [15] Sladek, R., et al. A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445:7130 (2007), 881–885.
16. [16] Wenzlau, J.M., et al. The cation efflux transporter ZnT8 (Slc30A8) is a major autoantigen in human type 1 diabetes. Proc. Natl. Acad. Sci. USA 104:43 (2007), 17040–17045.
17. [17] Lee, J.Y., et al. Contribution by synaptic zinc to the gender-disparate plaque formation in human Swedish mutant APP transgenic mice. Proc. Natl. Acad. Sci. USA 99:11 (2002), 7705–7710.
18. [18] Smidt, K., et al. SLC30A3 responds to glucose- and zinc variations in beta-cells and is critical for insulin production and in vivo glucose-metabolism during beta-cell stress. PLoS One, 4(5), 2009, e5684.
19. [19] Sindreu, C., Palmiter, R.D., Storm, D.R., Zinc transporter ZnT-3 regulates presynaptic Erk1/2 signaling and hippocampus-dependent memory. Proc. Natl. Acad. Sci. USA 108:8 (2011), 3366–3370.
20. [20] Zhao, Y., et al. Differential targeting of SLC30A10/ZnT10 heterodimers to endolysosomal compartments modulates EGF-induced MEK/ERK1/2 activity. Traffic 17:3 (2016), 267–288.
21. [21] Saito, T., et al. Deficiencies of hippocampal Zn and ZnT3 accelerate brain aging of Rat. Biochem. Biophys. Res. Commun. 279:2 (2000), 505–511.
22. [22] Hilenski, L.L., et al. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 24:4 (2004), 677–683.
23. [23] Dineley, K.E., et al. Zinc causes loss of membrane potential and elevates reactive oxygen species in rat brain mitochondria. Mitochondrion 5:1 (2005), 55–65.
24. [24] Bao, B., et al. Zinc up-regulates NF-kappaB activation via phosphorylation of IkappaB in HUT-78 (Th0) cells. FEBS Lett. 581:23 (2007), 4507–4511.
25. [25] Prasad, A.S., et al. Zinc activates NF-kappaB in HUT-78 cells. J. Lab. Clin. Med. 138:4 (2001), 250–256.
26. [26] Kim, Y.M., et al. Zn2+-induced NF-kappaB-dependent transcriptional activity involves site-specific p65/RelA phosphorylation. Cell Signal. 19:3 (2007), 538–546.
27. [27] Griendling, K.K., et al. Characterization of phosphatidylinositol-specific phospholipase C from cultured vascular smooth muscle cells. J. Biol. Chem. 266:23 (1991), 15498–15504.
28. [28] San Martin, A., et al. Nox1-based NADPH oxidase-derived superoxide is required for VSMC activation by advanced glycation end-products. Free Radic. Biol. Med. 42:11 (2007), 1671–1679.
29. [29] Dikalov, S.I., et al. Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated superoxide and hydrogen peroxide production. Free Radic. Biol. Med. 45:9 (2008), 1340–1351.
30. [30] Xiong, S., et al. Peroxisome proliferator-activated receptor gamma coactivator-1alpha is a central negative regulator of vascular senescence. Arterioscler. Thromb. Vasc. Biol. 33:5 (2013), 988–998.
31. [31] Dikalova, A., et al. Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 112:17 (2005), 2668–2676.
32. [32] Herbert, K.E., et al. Angiotensin II-mediated oxidative DNA damage accelerates cellular senescence in cultured human vascular smooth muscle cells via telomere-dependent and independent pathways. Circ. Res. 102:2 (2008), 201–208.
33. [33] Rogakou, E.P., et al. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273:10 (1998), 5858–5868.
34. [34] Herbig, U., et al. Cellular senescence in aging primates. Science, 311(5765), 2006, 1257.
35. [35] Manea, A., et al. Transcriptional regulation of NADPH oxidase isoforms, Nox1 and Nox4, by nuclear factor-kappaB in human aortic smooth muscle cells. Biochem. Biophys. Res. Commun. 396:4 (2010), 901–907.
36. [36] Manea, A., et al. AP-1-dependent transcriptional regulation of NADPH oxidase in human aortic smooth muscle cells: role of p22phox subunit. Arterioscler. Thromb. Vasc. Biol. 28:5 (2008), 878–885.
37. [37] Lee, S.J., et al. 4-Hydroxynonenal enhances MMP-2 production in vascular smooth muscle cells via mitochondrial ROS-mediated activation of the Akt/NF-kappaB signaling pathways. Free Radic. Biol. Med. 45:10 (2008), 1487–1492.
38. [38] Prasad, A.S., Zinc is an antioxidant and anti-inflammatory agent: its role in human health. Front. Nutr., 1, 2014, 14.
39. [39] McCord, M.C., Aizenman, E., The role of intracellular zinc release in aging, oxidative stress, and Alzheimer's disease. Front. Aging Neurosci., 6, 2014, 77.
40. [40] Leyva-Illades, D., et al. SLC30A10 is a cell surface-localized manganese efflux transporter, and parkinsonism-causing mutations block its intracellular trafficking and efflux activity. J. Neurosci. 34:42 (2014), 14079–14095.
41. [41] Chen, P., et al. SLC30A10: a novel manganese transporter. Worm, 4(3), 2015, e1042648.
42. [42] Sensi, S.L., Yin, H.Z., Weiss, J.H., AMPA/kainate receptor-triggered Zn2+ entry into cortical neurons induces mitochondrial Zn2+ uptake and persistent mitochondrial dysfunction. Eur. J. Neurosci. 12:10 (2000), 3813–3818.
43. [43] Doughan, A.K., Harrison, D.G., Dikalov, S.I., Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ. Res. 102:4 (2008), 488–496.
44. [44] Chaplin, N.L., et al. Arterial smooth muscle mitochondria amplify hydrogen peroxide microdomains functionally coupled to L-type calcium channels. Circ. Res. 117:12 (2015), 1013–1023.
45. [45] Wosniak, J., et al. Cross-talk between mitochondria and NADPH oxidase: effects of mild mitochondrial dysfunction on angiotensin II-mediated increase in Nox isoform expression and activity in vascular smooth muscle cells. Antioxid. Redox Signal. 11:6 (2009), 1265–1278.
46. [46] Chung, H.Y., et al. The molecular inflammatory process in aging. Antioxid. Redox Signal. 8:3–4 (2006), 572–581.
47. [47] Napetschnig, J., Wu, H., Molecular basis of NF-κB signaling. Annu. Rev. Biophys. 42 (2013), 443–468.
48. [48] O'Leary, D.P., et al. TLR-4 signalling accelerates colon cancer cell adhesion via NF-κB mediated transcriptional up-regulation of Nox-1. PLoS One, 7(10), 2012, e44176.
49. [49] Buss, H., et al. Constitutive and interleukin-1-inducible phosphorylation of p65 NF-{kappa}B at serine 536 is mediated by multiple protein kinases including I{kappa}B kinase (IKK)-{alpha}, IKK{beta}, IKK{epsilon}, TRAF family member-associated (TANK)-binding kinase 1 (TBK1), and an unknown kinase and couples p65 to TATA-binding protein-associated factor II31-mediated interleukin-8 transcription. J. Biol. Chem. 279:53 (2004), 55633–55643.
50. [50] Saccani, S., et al. Degradation of promoter-bound p65/RelA is essential for the prompt termination of the nuclear factor kappaB response. J. Exp. Med. 200:1 (2004), 107–113.
51. [51] Shen, J., et al. Disruption of SM22 promotes inflammation after artery injury via nuclear factor kappaB activation. Circ. Res. 106:8 (2010), 1351–1362.
52. [52] Oh, H., et al. Phosphorylation of serine282 in NADPH oxidase activator 1 by Erk desensitizes EGF-induced ROS generation. Biochem. Biophys. Res. Commun. 394:3 (2010), 691–696.