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Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 7410257, 14 pages
http://dx.doi.org/10.1155/2016/7410257
Research Article

CD38 Deficiency Protects the Heart from Ischemia/Reperfusion Injury through Activating SIRT1/FOXOs-Mediated Antioxidative Stress Pathway

1Institute of Translational Medicine, Nanchang University, Nanchang 330031, China
2National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
3Department of Basic Medical Science, Shock/Trauma Research Center, School of Medicine, University of Missouri-Kansas City, Kansas City, MO 64108, USA

Received 7 April 2016; Revised 25 May 2016; Accepted 14 June 2016

Academic Editor: Massimo Collino

Copyright © 2016 Xiao-Hui Guan 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. A. Frank, M. Bonney, S. Bonney, L. Weitzel, M. Koeppen, and T. Eckle, “Myocardial ischemia reperfusion injury: from basic science to clinical bedside,” Seminars in Cardiothoracic and Vascular Anesthesia, vol. 16, no. 3, pp. 123–132, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Raedschelders, D. M. Ansley, and D. D. Y. Chen, “The cellular and molecular origin of reactive oxygen species generation during myocardial ischemia and reperfusion,” Pharmacology and Therapeutics, vol. 133, no. 2, pp. 230–255, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Sanada, I. Komuro, and M. Kitakaze, “Pathophysiology of myocardial reperfusion injury: preconditioning, postconditioning, and translational aspects of protective measures,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 301, no. 5, pp. H1723–H1741, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. X. Zhu, L. Zuo, A. J. Cardounel, J. L. Zweier, and G. He, “Characterization of in vivo tissue redox status, oxygenation, and formation of reactive oxygen species in postischemic myocardium,” Antioxidants and Redox Signaling, vol. 9, no. 4, pp. 447–455, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. Y. Maejima, J. Kuroda, S. Matsushima, T. Ago, and J. Sadoshima, “Regulation of myocardial growth and death by NADPH oxidase,” Journal of Molecular and Cellular Cardiology, vol. 50, no. 3, pp. 408–416, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. D. J. Hausenloy and D. M. Yellon, “Myocardial ischemia-reperfusion injury: a neglected therapeutic target,” The Journal of Clinical Investigation, vol. 123, no. 1, pp. 92–100, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. E. L. Reinherz, P. C. Kung, G. Goldstein, R. H. Levey, and S. F. Schlossman, “Discrete stages of human intrathymic differentiation: analysis of normal thymocytes and leukemic lymphoblasts of T-cell lineage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 3 I, pp. 1588–1592, 1980. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Aksoy, T. A. White, M. Thompson, and E. N. Chini, “Regulation of intracellular levels of NAD: a novel role for CD38,” Biochemical and Biophysical Research Communications, vol. 345, no. 4, pp. 1386–1392, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. D. G. Jackson and J. I. Bell, “Isolation of a cDNA encoding the human CD38 (T10) molecule, a cell surface glycoprotein with an unusual discontinuous pattern of expression during lymphocyte differentiation,” The Journal of Immunology, vol. 144, no. 7, pp. 2811–2815, 1990. View at Google Scholar · View at Scopus
  10. M. Howard, J. C. Grimaldi, J. F. Bazan et al., “Formation and hydrolysis of cyclic ADP-ribose catalyzed by lymphocyte antigen CD38,” Science, vol. 262, no. 5136, pp. 1056–1059, 1993. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Aarhus, R. M. Graeff, D. M. Dickey, T. F. Walseth, and C. L. Hon, “ADP-ribosyl cyclase and CD38 catalyze the synthesis of a calcium-mobilizing metabolite from NADP,” The Journal of Biological Chemistry, vol. 270, no. 51, pp. 30327–30333, 1995. View at Publisher · View at Google Scholar · View at Scopus
  12. H. C. Lee, R. Aarhus, and T. F. Walseth, “Calcium mobilization by dual receptors during fertilization of sea urchin eggs,” Science, vol. 261, no. 5119, pp. 352–355, 1993. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Galione, A. McDougall, W. B. Busa, N. Willmott, I. Gillot, and M. Whitaker, “Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs,” Science, vol. 261, no. 5119, pp. 348–352, 1993. View at Publisher · View at Google Scholar · View at Scopus
  14. A. H. Guse, C. P. da Silva, I. Berg et al., “Regulation of calcium signalling in T lymphocytes by the second messenger cyclic ADP-ribose,” Nature, vol. 398, no. 6722, pp. 70–73, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Gasser, S. Bruhn, and A. H. Guse, “Second messenger function of nicotinic acid adenine dinucleotide phosphate revealed by an improved enzymatic cycling assay,” The Journal of Biological Chemistry, vol. 281, no. 25, pp. 16906–16913, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Partida-Sánchez, D. A. Cockayne, S. Monard et al., “Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo,” Nature Medicine, vol. 7, no. 11, pp. 1209–1216, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Takasawa, K. Nata, H. Yonekura, and H. Okamoto, “Cyclic ADP-ribose in insulin secretion from pancreatic β cells,” Science, vol. 259, no. 5093, pp. 370–373, 1993. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Gally, J. M. Hartney, W. J. Janssen, and A.-L. Perraud, “CD38 plays a dual role in allergen-induced airway hyperresponsiveness,” American Journal of Respiratory Cell and Molecular Biology, vol. 40, no. 4, pp. 433–442, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. E. N. Chini, “CD38 as a regulator of cellular NAD: a novel potential pharmacological target for metabolic conditions,” Current Pharmaceutical Design, vol. 15, no. 1, pp. 57–63, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. P. Aksoy, C. Escande, T. A. White et al., “Regulation of SIRT 1 mediated NAD dependent deacetylation: a novel role for the multifunctional enzyme CD38,” Biochemical and Biophysical Research Communications, vol. 349, no. 1, pp. 353–359, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Matsushima and J. Sadoshima, “The role of sirtuins in cardiac disease,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 309, no. 9, pp. H1375–H1389, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Sengupta, J. D. Molkentin, J.-H. Paik, R. A. DePinho, and K. E. Yutzey, “FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress,” The Journal of Biological Chemistry, vol. 286, no. 9, pp. 7468–7478, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Daitoku, M. Hatta, H. Matsuzaki et al., “Silent information regulator 2 potentiates Foxo 1-mediated transcription through its deacetylase activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 27, pp. 10042–10047, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. I. Kitamura, T. Kitamura, J.-P. Kruse et al., “FoxO1 protects against pancreatic β cell failure through NeuroD and MafA induction,” Cell Metabolism, vol. 2, no. 3, pp. 153–163, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. G. S. Young, E. Choleris, F. E. Lund, and J. B. Kirkland, “Decreased cADPR and increased NAD+ in the Cd38−/− mouse,” Biochemical and Biophysical Research Communications, vol. 346, no. 1, pp. 188–192, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Ge, W. Jiang, L. Gan et al., “Mouse embryonic fibroblasts from CD38 knockout mice are resistant to oxidative stresses through inhibition of reactive oxygen species production and Ca2+ overload,” Biochemical and Biophysical Research Communications, vol. 399, no. 2, pp. 167–172, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. G. J. P. L. Kops, N. D. de Ruiter, A. M. M. De Vries-Smits, D. R. Powell, J. L. Bos, and B. M. T. Burgering, “Direct control of the Forkhead transcription factor AFX by protein kinase B,” Nature, vol. 398, no. 6728, pp. 630–634, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Meier, D. R. Alessi, P. Cron, M. Andjelković, and B. A. Hemmings, “Mitogenic activation, phosphorylation, and nuclear translocation of protein kinase Bβ,” The Journal of Biological Chemistry, vol. 272, no. 48, pp. 30491–30497, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. R. B. Jennings, H. M. Sommers, G. A. Smyth, H. A. Flack, and H. Linn, “Myocardial necrosis induced by temporary occlusion of a coronary artery in the dog,” Archives of Pathology, vol. 70, pp. 68–78, 1960. View at Google Scholar
  30. M. T. P. Barbosa, S. M. Soares, C. M. Novak et al., “The enzyme CD38 (a NAD glycohydrolase, EC 3.2.2.5) is necessary for the development of diet-induced obesity,” The FASEB Journal, vol. 21, no. 13, pp. 3629–3639, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. Y.-Q. Wang, Q. Cao, F. Wang et al., “SIRT1 protects against oxidative stress-induced endothelial progenitor cells apoptosis by inhibiting FOXO3a via FOXO3a ubiquitination and degradation,” Journal of Cellular Physiology, vol. 230, no. 9, pp. 2098–2107, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. S. M. Ronnebaum and C. Patterson, “The FoxO family in cardiac function and dysfunction,” Annual Review of Physiology, vol. 72, pp. 81–94, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. J. B. Pillai, A. Isbatan, S.-I. Imai, and M. P. Gupta, “Poly(ADP-ribose) polymerase-1-dependent cardiac myocyte cell death during heart failure is mediated by NAD+ depletion and reduced Sir2α deacetylase activity,” The Journal of Biological Chemistry, vol. 280, no. 52, pp. 43121–43130, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Halmosi, Z. Berente, E. Osz, K. Toth, P. Literati-Nagy, and B. Sumegi, “Effect of poly(ADP-ribose) polymerase inhibitors on the ischemia-reperfusion-induced oxidative cell damage and mitochondrial metabolism in langendorff heart perfusion system,” Molecular Pharmacology, vol. 59, no. 6, pp. 1497–1505, 2001. View at Google Scholar · View at Scopus
  35. A. A. Pieper, T. Walles, G. Wei et al., “Myocardial postischemic injury is reduced by polyADPripose polymerase-1 gene disruption,” Molecular Medicine, vol. 6, no. 4, pp. 271–282, 2000. View at Google Scholar · View at Scopus
  36. L. Liaudet, F. G. Soriano, É. Szabó et al., “Protection against hemorrhagic shock in mice genetically deficient in poly(ADP-ribose)polymerase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 18, pp. 10203–10208, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. C.-P. Hsu, S. Oka, D. Shao, N. Hariharan, and J. Sadoshima, “Nicotinamide phosphoribosyltransferase regulates cell survival through NAD+ synthesis in cardiac myocytes,” Circulation Research, vol. 105, no. 5, pp. 481–491, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Kalogeris, Y. Bao, and R. J. Korthuis, “Mitochondrial reactive oxygen species: a double edged sword in ischemia/reperfusion vs preconditioning,” Redox Biology, vol. 2, no. 1, pp. 702–714, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. D. M. Yellon and D. J. Hausenloy, “Myocardial reperfusion injury,” The New England Journal of Medicine, vol. 357, no. 11, pp. 1074–1135, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Lassègue, A. San Martín, and K. K. Griendling, “Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system,” Circulation Research, vol. 110, no. 10, pp. 1364–1390, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Takahashi, Y. Kagaya, I. Kato et al., “Deficit of CD38/cyclic ADP-ribose is differentially compensated in hearts by gender,” Biochemical and Biophysical Research Communications, vol. 312, no. 2, pp. 434–440, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Gan, W. Jiang, Y.-F. Xiao et al., “Disruption of CD38 gene enhances cardiac functions by elevating serum testosterone in the male null mice,” Life Sciences, vol. 89, no. 13-14, pp. 491–497, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. D. A. Cockayne, T. Muchamuel, J. C. Grimaldi et al., “Mice deficient for the ecto-nicotinamide adenine dinucleotide glycohydrolase CD38 exhibit altered humoral immune responses,” Blood, vol. 92, no. 4, pp. 1324–1333, 1998. View at Google Scholar · View at Scopus