Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 6408278, 10 pages
https://doi.org/10.1155/2017/6408278
Research Article

Mitochondria-Targeted Antioxidant SkQ1 Improves Dermal Wound Healing in Genetically Diabetic Mice

1Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory 1-12, Moscow 119234, Russia
2Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Leninskie Gory 1-40, Moscow 119992, Russia
3Institute of Mitoengineering, Lomonosov Moscow State University, Leninskie Gory 1-73, Moscow 119992, Russia

Correspondence should be addressed to Ekaterina N. Popova; ur.liam@hc_avopop_k

Received 21 February 2017; Accepted 20 April 2017; Published 6 July 2017

Academic Editor: Maik Hüttemann

Copyright © 2017 Ilya A. Demyanenko et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Gary Sibbald and K. Y. Woo, “The biology of chronic foot ulcers in persons with diabetes,” Diabetes/Metabolism Research and Reviews, vol. 24, pp. S25–S30, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Monnier, E. Mas, C. Ginet et al., “Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes,” Journal of the American Medical Association, vol. 295, pp. 1681–1687, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. M. J. Callaghan, D. J. Ceradini, and G. C. Gurtner, “Hyperglycemia-induced reactive oxygen species and impaired endothelial progenitor cell function,” Antioxidants & Redox Signaling, vol. 7, pp. 1476–1482, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. F. Folli, D. Corradi, P. Fanti et al., “The role of oxidative stress in the pathogenesis of type 2 diabetes mellitus micro- and macrovascular complications: avenues for a mechanistic-based therapeutic approach,” Current Diabetes Reviews, vol. 7, pp. 313–324, 2011. View at Publisher · View at Google Scholar
  5. M. Brownlee, “The pathobiology of diabetic complications,” Diabetes, vol. 54, pp. 1615–1625, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Giacco and M. Brownlee, “Oxidative stress and diabetic complications,” Circulation Research, vol. 107, pp. 1058–1070, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. K. Sharma, “Mitochondrial hormesis and diabetic complications,” Diabetes, vol. 64, pp. 663–672, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Houstis, E. D. Rosen, and E. S. Lander, “Reactive oxygen species have a causal role in multiple forms of insulin resistance,” Nature, vol. 440, pp. 944–948, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. M. V. Skulachev, Y. N. Antonenko, V. N. Anisimov et al., “Mitochondrial-targeted plastoquinone derivatives. Effect on senescence and acute age-related pathologies,” Current Drug Targets, vol. 12, pp. 800–826, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Paglialunga, B. Van Bree, M. Bosma et al., “Targeting of mitochondrial reactive oxygen species production does not avert lipid-induced insulin resistance in muscle tissue from mice,” Diabetologia, vol. 55, pp. 2759–2768, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. S. S. Jain, S. Paglialunga, C. Vigna et al., “High-fat diet–induced mitochondrial biogenesis is regulated by mitochondrial-derived reactive oxygen species activation of CaMKII,” Diabetes, vol. 63, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. I. A. Demyanenko, E. N. Popova, V. V. Zakharova et al., “Mitochondria-targeted antioxidant SkQ1 improves impaired dermal wound healing in old mice,” Aging (Albany NY), vol. 7, pp. 475–485, 2015. View at Publisher · View at Google Scholar
  13. M. Mihara and M. Uchiyama, “Determination of malonaldehyde precursor in tissues by thiobarbituric acid test,” Analytical Biochemistry, vol. 86, pp. 271–278, 1978. View at Google Scholar
  14. R. A. Underwood, N. S. Gibran, L. A. Muffley, M. L. Usui, and J. E. Olerud, “Color subtractive–computer-assisted image analysis for quantification of cutaneous nerves in a diabetic mouse model,” The Journal of Histochemistry and Cytochemistry, vol. 49, pp. 1285–1291, 2001. View at Publisher · View at Google Scholar
  15. J. Michaels, S. S. Churgin, K. M. Blechman et al., “db/db mice exhibit severe wound-healing impairments compared with other murine diabetic strains in a silicone-splinted excisional wound model,” Wound Repair and Regeneration, vol. 15, pp. 665–670, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. V. I. Tkalčević, S. Čužić, M. J. Parnham, I. Pašalić, and K. Brajša, “Differential evaluation of excisional non-occluded wound healing in db/db mice,” Toxicologic Pathology, vol. 37, pp. 183–192, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. E. N. Popova, O. Y. Pletjushkina, V. B. Dugina et al., “Scavenging of reactive oxygen species in mitochondria induces myofibroblast differentiation,” Antioxidants & Redox Signaling, vol. 13, pp. 1297–1307, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. I. A. Demianenko, T. V. Vasilieva, L. V. Domnina et al., “Novel mitochondria-targeted antioxidants, “Skulachev-ion” derivatives, accelerate dermal wound healing in animals,” Biochemistry (Mosc), vol. 75, pp. 274–280, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Feillet-Coudray, G. Fouret, R. Ebabe Elle et al., “The mitochondrial-targeted antioxidant MitoQ ameliorates metabolic syndrome features in obesogenic diet-fed rats better than apocynin or allopurinol,” Free Radical Research, vol. 48, pp. 1232–1246, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. S. A. Eming, T. Krieg, and J. M. Davidson, “Inflammation in wound repair: molecular and cellular mechanisms,” The Journal of Investigative Dermatology, vol. 127, pp. 514–525, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. J. V. Dovi, L.-K. He, and L. A. DiPietro, “Accelerated wound closure in neutrophil-depleted mice,” Journal of Leukocyte Biology, vol. 73, pp. 448–455, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Mahadev, A. Zilbering, L. Zhu, and B. J. Goldstein, “Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1B in vivo and enhances the early insulin action cascade,” The Journal of Biological Chemistry, vol. 276, pp. 21938–21942, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Biosciences, “Epigenetic modifications regulate gene expression, Pathways Mag. 2008,” March 2017, http://www.sabiosciences.com/pathwaymagazine/pathways8/epigenetic-modifications-regulate-gene-expression.php. View at Google Scholar
  24. J. P. Gray and E. Heart, “Usurping the mitochondrial supremacy: extramitochondrial sources of reactive oxygen intermediates and their role in beta cell metabolism and insulin secretion,” Toxicology Mechanisms and Methods, vol. 20, pp. 167–174, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Leloup, C. Tourrel-Cuzin, C. Magnan et al., “Mitochondrial reactive oxygen species are obligatory signals for glucose-induced insulin secretion,” Diabetes, vol. 58, pp. 673–681, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. R. P. Robertson, “Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes,” The Journal of Biological Chemistry, vol. 279, pp. 42351–42354, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. R. A. Zinovkin, V. P. Romaschenko, I. I. Galkin et al., “Role of mitochondrial reactive oxygen species in age-related inflammatory activation of endothelium,” Aging (Albany NY), vol. 6, pp. 661–674, 2014. View at Publisher · View at Google Scholar
  28. I. I. Galkin, O. Y. Pletjushkina, R. A. Zinovkin et al., “Mitochondria-targeted antioxidants prevent TNFα-induced endothelial cell damage,” Biochemistry (Moscow), vol. 79, pp. 124–130, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Maruyama, J. Asai, M. Ii, T. Thorne, D. W. Losordo, and P. A. D’Amore, “Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing,” The American Journal of Pathology, vol. 170, pp. 1178–1191, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Khanna, S. Biswas, Y. Shang et al., “Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice,” PloS One, vol. 5, article e9539, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. R. E. Mirza, M. M. Fang, E. M. Weinheimer-Haus, W. J. Ennis, and T. J. Koh, “Sustained inflammasome activity in macrophages impairs wound healing in type 2 diabetic humans and mice,” Diabetes, vol. 63, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Zhou, A. S. Yazdi, P. Menu, and J. Tschopp, “A role for mitochondria in NLRP3 inflammasome activation,” Nature, vol. 469, pp. 221–225, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Dashdorj, K. Jyothi, S. Lim et al., “Mitochondria-targeted antioxidant MitoQ ameliorates experimental mouse colitis by suppressing NLRP3 inflammasome-mediated inflammatory cytokines,” BMC Medicine, vol. 11, p. 178, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. M. L. Lamers, M. E. S. Almeida, M. Vicente-Manzanares, A. F. Horwitz, and M. F. Santos, “High glucose-mediated oxidative stress impairs cell migration,” PloS One, vol. 6, article e22865, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. C. H. Lee, B. Shah, E. K. Moioli, and J. J. Mao, “CTGF directs fibroblast differentiation from human mesenchymal stem/stromal cells and defines connective tissue healing in a rodent injury model,” The Journal of Clinical Investigation, vol. 120, pp. 3340–3349, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. F. Ferraro, S. Lymperi, S. Méndez-Ferrer et al., “Diabetes impairs hematopoietic stem cell mobilization by altering niche function,” Science Translational Medicine, vol. 3, no. 104, article 104ra101, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Albiero, N. Poncina, M. Tjwa et al., “Diabetes causes bone marrow autonomic neuropathy and impairs stem cell mobilization via dysregulated p66Shc and Sirt1,” Diabetes, vol. 63, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. E. R. Galimov, B. V. Chernyak, A. S. Sidorenko, A. V. Tereshkova, and P. M. Chumakov, “Prooxidant properties of p66shc are mediated by mitochondria in human cells,” PloS One, vol. 9, article e86521, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. I. N. Shipounova, D. A. Svinareva, T. V. Petrova et al., “Reactive oxygen species produced in mitochondria are involved in age-dependent changes of hematopoietic and mesenchymal progenitor cells in mice. A study with the novel mitochondria-targeted antioxidant SkQ1,” Mechanisms of Ageing and Development, vol. 131, pp. 415–421, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. M. S. Bitar and Z. N. Labbad, “Transforming growth factor-β and insulin-like growth factor-I in relation to diabetes-induced impairment of wound healing,” The Journal of Surgical Research, vol. 61, pp. 113–119, 1996. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Gong, W. Shi, S. Yi, H. Chen, J. Groffen, and N. Heisterkamp, “TGFβ signaling plays a critical role in promoting alternative macrophage activation,” BMC Immunology, vol. 13, p. 31, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. E. J. Marrotte, D. D. Chen, J. S. Hakim, and A. F. Chen, “Manganese superoxide dismutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice,” The Journal of Clinical Investigation, vol. 120, pp. 4207–4219, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. V. P. Skulachev, V. N. Anisimov, Y. N. Antonenko et al., “An attempt to prevent senescence: a mitochondrial approach,” Biochimica et Biophysica Acta - Bioenergetics, vol. 1787, pp. 437–461, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. V. N. Anisimov, M. V. Egorov, M. S. Krasilshchikova et al., “Effects of the mitochondria-targeted antioxidant SkQ1 on lifespan of rodents,” Aging (Albany NY), vol. 3, pp. 1110–1119, 2011. View at Publisher · View at Google Scholar