Low concentrations of uncouplers of oxidative phosphorylation prevent inflammatory activation of endothelial cells by tumor necrosis factor

Biochemistry (Moscow)

Volumn 80, Issue 5, 2015, Pages 610-619

  Romaschenko, V P ^a   Zinovkin, R A ^a   Galkin, I I ^a   Zakharova, V V ^a   Panteleeva, A A ^a   Tokarchuk, A V ^a   Lyamzaev, K G ^a   Pletjushkina, O Yu ^a   Chernyak, B V ^a   Popova, E N ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

adhesion molecules; endothelium; inflammation; mitochondria; penetrating cations of SkQ family; uncoupling of oxidative phosphorylation

Indexed keywords

ANTIOXIDANT; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; I KAPPA B; ICAM1 PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; TNF PROTEIN, HUMAN; TUMOR NECROSIS FACTOR; UNCOUPLING PROTEIN; VASCULAR CELL ADHESION MOLECULE 1;

BIOSYNTHESIS; CELL ADHESION; CELL LINE; DOSE RESPONSE; DRUG EFFECTS; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; HUMAN; INFLAMMATION; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; NEUTROPHIL; PATHOLOGY;

ANTIOXIDANTS; CELL ADHESION; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; E-SELECTIN; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; I-KAPPA B PROTEINS; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; MEMBRANE POTENTIAL, MITOCHONDRIAL; NEUTROPHILS; NF-KAPPA B; TUMOR NECROSIS FACTOR-ALPHA; UNCOUPLING AGENTS; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84928993305     PISSN: 00062979     EISSN: 16083040     Source Type: Journal    
DOI: 10.1134/S0006297915050144     Document Type: Article

References (42)

1. Bruunsgaard, H., Skinhoj, P., Pedersen, A. N., Schroll, M., and Pedersen, B. K. (2000) Ageing, tumor necrosis factor-α (TNF-α) and atherosclerosis, Clin. Exp. Immunol., 121, 255-260.
2. Chung, H. Y., Sung, B., Jung, K. J., Zou, Y., and Yu, B. P. (2006) The molecular inflammatory process in aging, Antioxid. Redox Signal., 8, 572-581.
3. Csiszar, A., Ungvari, Z., Koller, A., Edwards, J. G., and Kaley, G. (2003) Aging-induced proinflammatory shift in cytokine expression profile in coronary arteries, FASEB J., 17, 1183-1185.
4. Dandona, P., Aljada, A., and Bandyopadhyay, A. (2004) Inflammation: the link between insulin resistance, obesity and diabetes, Trends Immunol., 25, 4-7.
5. Springer, T. A. (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm, Cell, 76, 301-314.
6. Roebuck, K. A., and Finnegan, A. (1999) Regulation of intercellular adhesion molecule-1 (CD54) gene expression, J. Leukoc. Biol., 66, 876-888.
7. Park, J., Choi, H., Min, J. S., Park, S. J., Kim, J. H., Park, H. J., Kim, B., Chae, J. I., Yim, M., and Lee, D. S. (2013) Mitochondrial dynamics modulate the expression of proinflammatory mediators in microglial cells, J. Neurochem., 127, 221-232.
8. West, A. P., Shadel, G. S., and Ghosh, S. (2011) Mitochondria in innate immune responses, Nature Rev. Immunol., 11, 389-402.
9. Davidson, S. M., and Duchen, M. R. (2007) Endothelial mitochondria: contributing to vascular function and disease, Circ. Res., 100, 1128-1141.
10. Culic, O., Gruwel, M. L., and Schrader, J. (1997) Energy turnover of vascular endothelial cells, Am. J. Physiol., 273, 205-213.
11. Addabbo, F., Ratliff, B., Park, H. C., Kuo, M. C., Ungvari, Z., Csiszar, A., Krasnikov, B., Sodhi, K., Zhang, F., Nasjletti, A., and Goligorsky, M. S. (2009) The Krebs cycle and mitochondrial mass are early victims of endothelial dysfunction: proteomic approach, Am. J. Pathol., 174, 34-43.
12. Madamanchi, N. R., and Runge, M. S. (2007) Mitochondrial dysfunction in atherosclerosis, Circ. Res., 100, 460-473.
13. Schulz, E., Dopheide, J., Schuhmacher, S., Thomas, S. R., Chen, K., Daiber, A., Wenzel, P., Munzel, T., and Keaney, J. F., Jr. (2008) Suppression of the JNK pathway by induction of a metabolic stress response prevents vascular injury and dysfunction, Circulation, 118, 1347-1357.
14. Wrzosek, A., Lukasiak, A., Gwozdz, P., Malinska, D., Kozlovski, V. I., Szewczyk, A., Chlopicki, S., and Dolowy, K. (2009) Large-conductance K+ channel opener CGS7184 as a regulator of endothelial cell function, Eur. J. Pharmacol., 602, 105-111.
15. 2+ regulation, Cell Calcium, 35, 509-521.
16. Joo, H. K., Lee, Y. R., Lim, S. Y., Lee, E. J., Choi, S., Cho, E. J., Park, M. S., Ryoo, S., Park, J. B., and Jeon, B. H. (2012) Peripheral benzodiazepine receptor regulates vascular endothelial activations via suppression of the voltagedependent anion channel-1, FEBS Lett., 586, 1349-1355.
17. Feletou, M., and Vanhoutte, P. M. (2006) Endothelial dysfunction: a multifaceted disorder (The Wiggers Award Lecture), Am. J. Physiol. Heart Circ. Physiol., 291, 985-1002.
18. Galkin, I. I., Pletjushkina, O. Yu., Zinovkin, R. A., Zakharova, V. V., Biryukov, I. S., Chernyak, B. V., and Popova, E. N. (2014) Mitochondria-targeted antioxidants prevent the tumor necrosis factor induced apoptosis of endothelial cells, Biochemistry (Moscow), 79, 124-130.
19. Rahman, A., Kefer, J., Bando, M., Niles, W. D., and Malik, A. B. (1998) E-selectin expression in human endothelial cells by TNF-α-induced oxidant generation and NF-κB activation, Am. J. Physiol., 275, L533-544.
20. Deshpande, S. S., Angkeow, P., Huang, J., Ozaki, M., and Irani, K. (2000) Rac1 inhibits TNF-α-induced endothelial cell apoptosis: dual regulation by reactive oxygen species, FASEB J., 14, 1705-1714.
21. Zinovkin, R. A., Romaschenko, V. P., Galkin, I. I., Zakharova, V. V., Pletjushkina, O. Y., Chernyak, B. V., and Popova, E. N. (2014) Role of mitochondrial reactive oxygen species in age-related inflammatory activation of endothelium, Aging (Albany N. Y.), 6, 671-674.
22. Brigelius-Flohe, R., and Flohe, L. (2011) Basic principles and emerging concepts in the redox control of transcription factors, Antioxid. Redox Signal., 15, 2335-2381.
23. Korshunov, S. S., Skulachev, V. P., and Starkov, A. A. (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria, FEBS Lett., 416, 15-18.
24. Severin, F. F., Severina, I. I., Antonenko, Y. N., Rokitskaya, T. I., Cherepanov, D. A., Mokhova, E. N., Vyssokikh, M. Y., Pustovidko, A. V., Markova, O. V., Yaguzhinsky, L. S., Korshunova, G. A., Sumbatyan, N. V., Skulachev, M. V., and Skulachev, V. P. (2010) Penetrating cation/fatty acid anion pair as a mitochondria-targeted protonophore, Proc. Natl. Acad. Sci. USA, 107, 663-668.
25. Skulachev, V. P., Antonenko, Y. N., Cherepanov, D. A., Chernyak, B. V., Izyumov, D. S., Khailova, L. S., Klishin, S. S., Korshunova, G. A., Lyamzaev, K. G., Pletjushkina, O. Y., Roginsky, V. A., Rokitskaya, T. I., Severin, F. F., Severina, I. I., Simonyan, R. A., Skulachev, M. V., Sumbatyan, N. V., Sukhanova, E. I., Tashlitsky, V. N., Trendeleva, T. A., Vyssokikh, M. Y., and Zvyagilskaya, R. A. (2010) Prevention of cardiolipin oxidation and fatty acid cycling as two antioxidant mechanisms of cationic derivatives of plastoquinone (SkQs), Biochim. Biophys. Acta, 1797, 878-889.
26. Duval, C., Negre-Salvayre, A., Dogilo, A., Salvayre, R., Penicaud, L., and Casteilla, L. (2002) Increased reactive oxygen species production with antisense oligonucleotides directed against uncoupling protein 2 in murine endothelial cells, Biochem. Cell Biol., 80, 757-764.
27. Fink, B. D., Reszka, K. J., Herlein, J. A., Mathahs, M. M., and Sivitz, W. I. (2005) Respiratory uncoupling by UCP1 and UCP2 and superoxide generation in endothelial cell mitochondria, Am. J. Physiol. Endocrinol. Metab., 288, 71-79.
28. Lee, K. U., Lee, I. K., Han, J., Song, D. K., Kim, Y. M., Song, H. S., Kim, H. S., Lee, W. J., Koh, E. H., Song, K. H., Han, S. M., Kim, M. S., Park, I. S., and Park, J. Y. (2005) Effects of recombinant adenovirus-mediated uncoupling protein 2 overexpression on endothelial function and apoptosis, Circ. Res., 96, 1200-1207.
29. Park, J. Y., Park, K. G., Kim, H. J., Kang, H. G., Ahn, J. D., Kim, H. S., Kim, Y. M., Son, S. M., Kim, I. J., Kim, Y. K., Kim, C. D., Lee, K. U., and Lee, I. K. (2005) The effects of the overexpression of recombinant uncoupling protein 2 on proliferation, migration and plasminogen activator inhibitor 1 expression in human vascular smooth muscle cells, Diabetologia, 48, 1022-1028.
30. 2 production promotes endothelial NF-κB activation in aged rat arteries, Am. J. Physiol. Heart Circ. Physiol., 293, 37-47.
31. Barbour, J. A., and Turner, N. (2014) Mitochondrial stress signaling promotes cellular adaptations, Int. J. Cell Biol., 2014, 156020.
32. Tilstra, J. S., Clauson, C. L., Niedernhofer, L. J., and Robbins, P. D. (2011) NF-κB in aging and disease, Aging Dis., 2, 449-465.
33. Popova, E. N., Pletjushkina, O. Y., Dugina, V. B., Domnina, L. V., Ivanova, O. Y., Izyumov, D. S., Skulachev, V. P., and Chernyak, B. V. (2010) Scavenging of reactive oxygen species in mitochondria induces myofibroblast differentiation, Antioxid. Redox Signal., 13, 1297-1307.
34. Izyumov, D. S., Domnina, L. V., Nepryakhina, O. K., Avetisyan, A. V., Golyshev, S. A., Ivanova, O. Yu., Korotetskaya, M. V., Lyamzayev, K. G., Pletjushkina, O. Yu., Popova, E. N., and Chernyak, B. V. (2010) Mitochondria as sources of reactive oxygen species during oxidative stress. The study with novel mitochondria-targeted antioxidants on the basis of "Skulachev ions", Biochemistry (Moscow), 75, 123-129.
35. Agapova, L. S., Chernyak, B. V., Domnina, L. V., Dugina, V. B., Efimenko, A. Yu., Fetisova, E. K., Ivanova, O. Yu., Kalinina, N. I., Lichinitser, M. R., Lukashev, A. N., Khromova, N. V., Kopnin, B. P., Korotetskaya, M. V., Pletjushkina, O. Yu., Popova, E. N., Shagieva, G. S., Skulachev, M. V., Stepanova, E. V., Titova, E. V., Tkachuk, V. A., Vasilyev, Yu. M., and Skulachev, V. P. (2008) Mitochondriatargeted plastoquinone derivative as a tool interrupting the aging program. 3. SkQ1 suppresses tumor development from p53-deficient cells, Biochemistry (Moscow), 73, 1300-1316.
36. Caldeira da Silva, C. C., Cerqueira, F. M., Barbosa, L. F., Medeiros, M. H., and Kowaltowski, A. J. (2008) Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity, Aging Cell, 7, 552-560.
37. Cerqueira, F. M., Laurindo, F. R., and Kowaltowski, A. J. (2011) Mild mitochondrial uncoupling and calorie restriction increase fasting eNOS, akt and mitochondrial biogenesis, PLoS One, 6, e18433.
38. Lyamzaev, K. G., Izyumov, D. S., Avetisyan, A. V., Yang, F., Pletjushkina, O. Y., and Chernyak, B. V. (2004) Inhibition of mitochondrial bioenergetics: the effects on structure of mitochondria in the cell and on apoptosis, Acta Biochim. Pol., 51, 553-562.
39. Pletjushkina, O. Y., Lyamzaev, K. G., Popova, E. N., Nepryakhina, O. K., Ivanova, O. Y., Domnina, L. V., Chernyak, B. V., and Skulachev, V. P. (2006) Effect of oxidative stress on dynamics of mitochondrial reticulum, Biochim. Biophys. Acta, 1757, 518-524.
40. Bradley, J. R. (2008) TNF-mediated inflammatory disease, J. Pathol., 214, 149-160.
41. Hirata, Y., Nagata, D., Suzuki, E., Nishimatsu, H., Suzuki, J.-I., and Nagai, R. (2010) Diagnosis and treatment of endothelial dysfunction in cardiovascular disease, Int. Heart J., 51, 1-6.
42. Plotnikov, E. Yu., Silachev, D. N., Jankauskas, S. S., Rokitskaya, T. I., Chuprykina, A. A., Pevzner, I. B., Zorova, L. D., Isaev, N. K., Antonenko, Yu. N., Skulachev, V. P., and Zorov, D. B. (2012) Partial uncoupling of respiration and phosphorylation as one of the pathways of implementation of the nephro- and neuroprotective effects of penetrating cations of the SkQ family, Biochemistry (Moscow), 77, 1029-1037.