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Oxidative Medicine and Cellular Longevity
Volume 2015, Article ID 351698, 14 pages
http://dx.doi.org/10.1155/2015/351698
Research Article

L-Lactate Protects Skin Fibroblasts against Aging-Associated Mitochondrial Dysfunction via Mitohormesis

1Institute of Physiology, Czech Academy of Sciences, Vídeňská 1083, 142 20 Prague, Czech Republic
2Department of Biochemistry and Microbiology, Institute of Chemical Technology Prague, Technická 5, 166 28 Prague, Czech Republic

Received 11 March 2015; Revised 25 May 2015; Accepted 27 May 2015

Academic Editor: Liang-Jun Yan

Copyright © 2015 Jaroslav Zelenka 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. U. S. National Institute of Aging and World Health Organization, Global Health and Aging, World Health Organization, Geneva, Switzerland, 2011.
  2. D. Harman, “The biologic clock: the mitochondria?” Journal of the American Geriatrics Society, vol. 20, no. 4, pp. 145–147, 1972. View at Publisher · View at Google Scholar · View at Scopus
  3. G. Barja, “Updating the mitochondrial free radical theory of aging: an integrated view, key aspects, and confounding concepts,” Antioxidants & Redox Signaling, vol. 19, no. 12, pp. 1420–1445, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Ristow, “Unraveling the truth about antioxidants: mitohormesis explains ROS-induced health benefits,” Nature Medicine, vol. 20, no. 7, pp. 709–711, 2014. View at Publisher · View at Google Scholar
  5. H. Kawagishi and T. Finkel, “Unraveling the truth about antioxidants: ROS and disease: finding the right balance,” Nature Medicine, vol. 20, no. 7, pp. 711–713, 2014. View at Publisher · View at Google Scholar
  6. L. J. Yan, “Positive oxidative stress in aging and aging-related disease tolerance,” Redox Biology, vol. 2, no. 1, pp. 165–169, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Yun and T. Finkel, “Mitohormesis,” Cell Metabolism, vol. 19, no. 5, pp. 757–766, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Ristow and K. Schmeisser, “Mitohormesis: promoting health and lifespan by increased levels of reactive oxygen species (ROS),” Dose-Response, vol. 12, no. 2, pp. 288–341, 2014. View at Publisher · View at Google Scholar
  9. A. B. Hwang, E. A. Ryu, M. Artan et al., “Feedback regulation via AMPK and HIF-1 mediates ROS-dependent longevity in Caenorhabditis elegans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 42, pp. E4458–E4467, 2014. View at Publisher · View at Google Scholar
  10. D. Wang, D. Malo, and S. Hekimi, “Elevated mitochondrial reactive oxygen species generation affects the immune response via hypoxia-inducible factor-1alpha in long-lived Mclk1 +/– mouse mutants,” Journal of Immunology, vol. 184, no. 2, pp. 582–590, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Ristow, K. Zarse, A. Oberbach et al., “Antioxidants prevent health-promoting effects of physical exercise in humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 21, pp. 8665–8670, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Liu, J. Wu, J. Zhu et al., “Lactate inhibits lipolysis in fat cells through activation of an orphan G-protein-coupled receptor, GPR81,” The Journal of Biological Chemistry, vol. 284, no. 5, pp. 2811–2822, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. C. L. Roland, T. Arumugam, D. Deng et al., “Cell surface lactate receptor GPR81 is crucial for cancer cell survival,” Cancer Research, vol. 74, no. 18, pp. 5301–5310, 2014. View at Publisher · View at Google Scholar
  14. R. Hoque, A. Farooq, A. Ghani, F. Gorelick, and W. Z. Mehal, “Lactate reduces liver and pancreatic injury in toll-like receptor- and inflammasome-mediated inflammation via gpr81-mediated suppression of innate immunity,” Gastroenterology, vol. 146, no. 7, pp. 1763–1774, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. F. Tang, S. Lane, A. Korsak et al., “Lactate-mediated glia-neuronal signalling in the mammalian brain,” Nature Communications, vol. 5, article 3284, 2014. View at Publisher · View at Google Scholar
  16. K. H. Lauritzen, C. Morland, M. Puchades et al., “Lactate receptor sites link neurotransmission, neurovascular coupling, and brain energy metabolism,” Cerebral Cortex, vol. 24, no. 10, pp. 2784–2795, 2014. View at Publisher · View at Google Scholar
  17. T. Hashimoto, R. Hussien, S. Oommen, K. Gohil, and G. A. Brooks, “Lactate sensitive transcription factor network in L6 cells: activation of MCT1 and mitochondrial biogenesis,” The FASEB Journal, vol. 21, no. 10, pp. 2602–2612, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Gambini, M. C. Gomez-Cabrera, C. Borras et al., “Free [NADH]/[NAD+] regulates sirtuin expression,” Archives of Biochemistry and Biophysics, vol. 512, no. 1, pp. 24–29, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Lezi, J. Lu, J. E. Selfridge, J. M. Burns, and R. H. Swerdlow, “Lactate administration reproduces specific brain and liver exercise-related changes,” Journal of Neurochemistry, vol. 127, no. 1, pp. 91–100, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Coco, S. Caggia, G. Musumeci et al., “Sodium L-lactate differently affects brain-derived neurothrophic factor, inducible nitric oxide synthase, and heat shock protein 70 kDa production in human astrocytes and SH-SY5Y cultures,” Journal of Neuroscience Research, vol. 91, no. 2, pp. 313–320, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Schiffer, S. Schulte, B. Sperlich, S. Achtzehn, H. Fricke, and H. K. Strüder, “Lactate infusion at rest increases BDNF blood concentration in humans,” Neuroscience Letters, vol. 488, no. 3, pp. 234–237, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. P. Sonveaux, T. Copetti, C. J. De Saedeleer et al., “Targeting the lactate transporter MCT1 in endothelial cells inhibits lactate-induced HIF-1 activation and tumor angiogenesis,” PLoS ONE, vol. 7, no. 3, Article ID e33418, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. D. J. Samuvel, K. P. Sundararaj, A. Nareika, M. F. Lopes-Virella, and Y. Huang, “Lactate boosts TLR4 signaling and NF-kappaB pathway-mediated gene transcription in macrophages via monocarboxylate transporters and MD-2 up-regulation,” Journal of Immunology, vol. 182, no. 4, pp. 2476–2484, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. V. S. LeBleu, J. T. O’Connell, K. N. G. Herrera et al., “PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis,” Nature Cell Biology, vol. 16, no. 10, pp. 992–1003, 2014. View at Publisher · View at Google Scholar
  25. F. Debacq-Chainiaux, J. D. Erusalimsky, J. Campisi, and O. Toussaint, “Protocols to detect senescence-associated beta-galactosidase (SA-βgal) activity, a biomarker of senescent cells in culture and in vivo,” Nature Protocols, vol. 4, no. 12, pp. 1798–1806, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Koníčková, K. Vaňková, J. Vaníková et al., “Anti-cancer effects of blue-green alga Spirulina platensis, a natural source of bilirubin-like tetrapyrrolic compounds,” Annals of Hepatology, vol. 13, no. 2, pp. 273–283, 2014. View at Google Scholar · View at Scopus
  27. W. Guo, L. Jiang, S. Bhasin, S. M. Khan, and R. H. Swerdlow, “DNA extraction procedures meaningfully influence qPCR-based mtDNA copy number determination,” Mitochondrion, vol. 9, no. 4, pp. 261–265, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. L. Alán, T. Špaček, J. Zelenka et al., “Assessment of mitochondrial DNA as an indicator of islet quality: an example in Goto Kakizaki rats,” Transplantation Proceedings, vol. 43, no. 9, pp. 3281–3284, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. T. V. Votyakova and I. J. Reynolds, “ΔΨm-Dependent and -independent production of reactive oxygen species by rat brain mitochondria,” Journal of Neurochemistry, vol. 79, no. 2, pp. 266–277, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. C.-A. W. Emhoff, L. A. Messonnier, M. A. Horning, J. A. Fattor, T. J. Carlson, and G. A. Brooks, “Direct and indirect lactate oxidation in trained and untrained men,” Journal of Applied Physiology, vol. 115, no. 6, pp. 829–838, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. J. M. S. Lemons, X.-J. Feng, B. D. Bennett et al., “Quiescent fibroblasts exhibit high metabolic activity,” PLoS Biology, vol. 8, no. 10, Article ID e1000514, 2010. View at Publisher · View at Google Scholar
  32. M. Adeva, M. González-Lucán, M. Seco, and C. Donapetry, “Enzymes involved in l-lactate metabolism in humans,” Mitochondrion, vol. 13, no. 6, pp. 615–629, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Mullen, Z. Hu, X. Shi et al., “Oxidation of alpha-ketoglutarate is required for reductive carboxylation in cancer cells with mitochondrial defects,” Cell Reports, vol. 7, no. 5, pp. 1679–1690, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. L. de Bari, D. Valenti, A. Atlante, and S. Passarella, “l-Lactate generates hydrogen peroxide in purified rat liver mitochondria due to the putative l-lactate oxidase localized in the intermembrane space,” FEBS Letters, vol. 584, no. 11, pp. 2285–2290, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. E. Owusu-Ansah, W. Song, and N. Perrimon, “Muscle mitohormesis promotes longevity via systemic repression of insulin signaling,” Cell, vol. 155, no. 3, pp. 699–712, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Jäer, C. Handschin, J. St-Pierre, and B. M. Spiegelman, “AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 29, pp. 12017–12022, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. T. Wenz, S. G. Rossi, R. L. Rotundo, B. M. Spiegelman, and C. T. Moraes, “Increased muscle PGC-1α expression protects from sarcopenia and metabolic disease during aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 48, pp. 20405–20410, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Handschin and B. M. Spiegelman, “The role of exercise and PGC1α in inflammation and chronic disease,” Nature, vol. 454, no. 7203, pp. 463–469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Lagouge and N. G. Larsson, “The role of mitochondrial DNA mutations and free radicals in disease and ageing,” Journal of Internal Medicine, vol. 273, no. 6, pp. 529–543, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Ikeda, S. Sciarretta, N. Nagarajan et al., “New insights into the role of mitochondrial dynamics and autophagy during oxidative stress and aging in the heart,” Oxidative Medicine and Cellular Longevity, vol. 2014, Article ID 210934, 13 pages, 2014. View at Publisher · View at Google Scholar
  41. E. Barbieri, D. Agostini, E. Polidori et al., “The pleiotropic effect of physical exercise on mitochondrial dynamics in aging skeletal muscle,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 917085, 15 pages, 2015. View at Publisher · View at Google Scholar
  42. S. I. S. Rattan, “Targeting the age-related occurrence, removal, and accumulation of molecular damage by hormesis,” Annals of the New York Academy of Sciences, vol. 1197, pp. 28–32, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Zoncu, A. Efeyan, and D. M. Sabatini, “mTOR: from growth signal integration to cancer, diabetes and ageing,” Nature Reviews Molecular Cell Biology, vol. 12, no. 1, pp. 21–35, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. D. D. Sarbassov and D. M. Sabatini, “Redox regulation of the nutrient-sensitive raptor-mTOR pathway and complex,” The Journal of Biological Chemistry, vol. 280, no. 47, pp. 39505–39509, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Campisi, “Aging, cellular senescence, and cancer,” Annual Review of Physiology, vol. 75, pp. 685–705, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. J. J. Wu, C. Quijano, E. Chen et al., “Mitochondrial dysfunction and oxidative stress mediate the physiological impairment induced by the disruption of autophagy,” Aging, vol. 1, no. 4, pp. 425–437, 2009. View at Google Scholar · View at Scopus
  47. D. J. Klionsky, F. C. Abdalla, H. Abeliovich et al., “Guidelines for the use and interpretation of assays for monitoring autophagy,” Autophagy, vol. 8, no. 4, pp. 445–544, 2012. View at Google Scholar