Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2017, Article ID 4985323, 13 pages
https://doi.org/10.1155/2017/4985323
Research Article

Overexpression of Heme Oxygenase-1 in Mesenchymal Stem Cells Augments Their Protection on Retinal Cells In Vitro and Attenuates Retinal Ischemia/Reperfusion Injury In Vivo against Oxidative Stress

1Department of Ophthalmology, Jinan Military General Hospital, No. 25 Shifan Road, Tianqiao District, Jinan 250031, China
2Department of Ophthalmology, The 88th Hospital of Chinese People’s Liberation Army, No. 6 Hushan East Road, Tai’an 271000, China
3Department of Ophthalmology, 401 Hospital of Chinese People’s Liberation Army, No. 22 Minjiang Road, Qingdao 266071, China
4Department of Ophthalmology, Chinese People’s Liberation Army General Hospital, No. 28 Fuxing Road, Haidian District, Beijing 100853, China
5Department of Cardre Ward, The 316th Hospital of Chinese People’s Liberation Army, No. A2 Niangniangfu, Xiangshan Road, Haidian District, Beijing 100093, China
6Department of Ophthalmology & Visual Science, University of Louisville, 301 E. Muhammad Ali Blvd., Louisville, KY 40202, USA

Correspondence should be addressed to Hua Jiang; moc.621@801auhgnaiJ

Received 6 September 2016; Revised 26 November 2016; Accepted 21 December 2016; Published 1 February 2017

Academic Editor: Salvatore Scacco

Copyright © 2017 Li Li 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. N. N. Osborne, R. J. Casson, J. P. M. Wood, G. Chidlow, M. Graham, and J. Melena, “Retinal ischemia: mechanisms of damage and potential therapeutic strategies,” Progress in Retinal and Eye Research, vol. 23, no. 1, pp. 91–147, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. M. E. Szabo, D. Haines, E. Garay et al., “Antioxidant properties of calcium dobesilate in ischemic/reperfused diabetic rat retina,” European Journal of Pharmacology, vol. 428, no. 2, pp. 277–286, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. J. Kusari, E. Padillo, S. X. Zhou et al., “Effect of brimonidine on retinal and choroidal neovascularization in a mouse model of retinopathy of prematurity and laser-treated rats,” Investigative Ophthalmology and Visual Science, vol. 52, no. 8, pp. 5424–5431, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Yokota, S. P. Narayanan, W. Zhang et al., “Neuroprotection from retinal ischemia/reperfusion injury by NOX2 NADPH oxidase deletion,” Investigative Ophthalmology and Visual Science, vol. 52, no. 11, pp. 8123–8131, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. Y. Wei, J. Gong, T. Yoshida et al., “Nrf2 has a protective role against neuronal and capillary degeneration in retinal ischemia-reperfusion injury,” Free Radical Biology and Medicine, vol. 51, no. 1, pp. 216–224, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. I. Laskowski, J. Pratschke, M. J. Wilhelm, M. Gasser, and N. L. Tilney, “Molecular and cellular events associated with ischemia/reperfusion injury,” Annals of Transplantation, vol. 5, no. 4, pp. 29–35, 2000. View at Google Scholar · View at Scopus
  7. S. M. Hong and Y. S. Yang, “A potential role of crystallin in the vitreous bodies of rats after ischemia-reperfusion injury,” Korean Journal of Ophthalmology, vol. 26, no. 4, pp. 248–254, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. Z. Zhang, X. Qin, X. Zhao et al., “Valproic acid regulates antioxidant enzymes and prevents ischemia/reperfusion injury in the rat retina,” Current Eye Research, vol. 37, no. 5, pp. 429–437, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Pan, M. He, R. Liu, N. C. Brecha, A. C. H. Yu, and M. Pu, “Sulforaphane protects rodent retinas against ischemia-reperfusion injury through the activation of the Nrf2/HO-1 antioxidant pathway,” PLoS ONE, vol. 9, no. 12, Article ID e114186, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Kamihata, H. Matsubara, T. Nishiue et al., “Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines,” Circulation, vol. 104, no. 9, pp. 1046–1052, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Kinnaird, E. Stabile, M. S. Burnett, and S. E. Epstein, “Bone marrow–derived cells for enhancing collateral development: mechanisms, animal data, and initial clinical experiences,” Circulation Research, vol. 95, no. 4, pp. 354–363, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. X. Wang, C. Liu, S. Li et al., “Hypoxia precondition promotes adipose-derived mesenchymal stem cells based repair of diabetic erectile dysfunction via augmenting angiogenesis and neuroprotection,” PLoS ONE, vol. 10, no. 3, Article ID e0118951, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Dominici, K. Le Blanc, I. Mueller et al., “Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement,” Cytotherapy, vol. 8, no. 4, pp. 315–317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. F. Arslan, R. C. Lai, M. B. Smeets et al., “Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury,” Stem Cell Research, vol. 10, no. 3, pp. 301–312, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Zhou, H. Xu, W. Xu et al., “Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro,” Stem Cell Research and Therapy, vol. 4, no. 2, article 34, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Jiang, B. N. Jahagirdar, R. L. Reinhardt et al., “Pluripotency of mesenchymal stem cells derived from adult marrow,” Nature, vol. 418, no. 6893, pp. 41–49, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Kroon, L. A. Martinson, K. Kadoya et al., “Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo,” Nature Biotechnology, vol. 26, no. 4, pp. 443–452, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. D. Cia, J. Vergnaud-Gauduchon, N. Jacquemot, and M. Doly, “Epigallocatechin gallate (EGCG) prevents H2O2-induced oxidative stress in primary rat retinal pigment epithelial cells,” Current Eye Research, vol. 39, no. 9, pp. 944–952, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. Á. F. Castilho, C. A. Aveleira, E. C. Leal et al., “Heme oxygenase-1 protects retinal endothelial cells against high glucose- and oxidative/nitrosative stress-induced toxicity,” PLOS ONE, vol. 7, no. 8, Article ID e42428, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Pittenger and A. Vinik, “Nerve growth factor and diabetic neuropathy,” Experimental Diabesity Research, vol. 4, no. 4, pp. 271–285, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. N. Li, X. R. Li, and J. Q. Yuan, “Effects of bone-marrow mesenchymal stem cells transplanted into vitreous cavity of rat injured by ischemia/reperfusion,” Graefe's Archive for Clinical and Experimental Ophthalmology, vol. 247, no. 4, pp. 503–514, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. M. P. Soares, S. Brouard, R. N. Smith, and F. H. Bach, “Heme oxygenase-1, a protective gene that prevents the rejection of transplanted organs,” Immunological Reviews, vol. 184, pp. 275–285, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Cruse and M. D. Maines, “Evidence suggesting that the two forms of heme oxygenase are products of different genes,” Journal of Biological Chemistry, vol. 263, no. 7, pp. 3348–3353, 1988. View at Google Scholar · View at Scopus
  25. W. K. Mccoubrey Jr., T. J. Huang, and M. D. Maines, “Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3,” European Journal of Biochemistry, vol. 247, no. 2, pp. 725–732, 1997. View at Publisher · View at Google Scholar · View at Scopus
  26. K. D. Poss and S. Tonegawa, “Reduced stress defense in heme oxygenase 1-deficient cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 20, pp. 10925–10930, 1997. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Exner, E. Minar, O. Wagner, and M. Schillinger, “The role of heme oxygenase-1 promoter polymorphisms in human disease,” Free Radical Biology and Medicine, vol. 37, no. 8, pp. 1097–1104, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Foresti, H. Goatly, C. J. Green, and R. Motterlini, “Role of heme oxygenase-1 in hypoxia-reoxygenation: requirement of substrate heme to promote cardioprotection,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 281, no. 5, pp. H1976–H1984, 2001. View at Google Scholar · View at Scopus
  29. S. Hayashi, R. Takamiya, T. Yamaguchi et al., “Induction of heme oxygenase-1 suppresses venular leukocyte adhesion elicited by oxidative stress: role of bilirubin generated by the enzyme,” Circulation Research, vol. 85, no. 8, pp. 663–671, 1999. View at Publisher · View at Google Scholar · View at Scopus
  30. L. E. Otterbein, F. H. Bach, J. Alam et al., “Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway,” Nature Medicine, vol. 6, no. 4, pp. 422–428, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. S.-J. Mo, Q. Zhong, Y.-F. Zhou, D. B. Deng, and X.-Q. Zhang, “Bone marrow-derived mesenchymal stem cells prevent the apoptosis of neuron-like PC12 cells via erythropoietin expression,” Neuroscience Letters, vol. 522, no. 2, pp. 92–97, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. I.-M. Fang, C.-M. Yang, C.-H. Yang, S.-H. Chiou, and M.-S. Chen, “Transplantation of induced pluripotent stem cells without C-Myc attenuates retinal ischemia and reperfusion injury in rats,” Experimental Eye Research, vol. 113, pp. 49–59, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. I.-M. Fang, C.-M. Yang, and C.-H. Yang, “Chitosan oligosaccharides prevented retinal ischemia and reperfusion injury via reduced oxidative stress and inflammation in rats,” Experimental Eye Research, vol. 130, pp. 38–50, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. M. E. Szabo, M. T. Droy-Lefaix, M. Doly, C. Carre, and P. Braquet, “Ischemia and reperfusion-induced histologic changes in the rat retina. Demonstration of a free radical-mediated mechanism,” Investigative Ophthalmology and Visual Science, vol. 32, no. 5, pp. 1471–1478, 1991. View at Google Scholar · View at Scopus
  35. D. Xu, D. Liu, B. Wang et al., “In Situ OH Generation from O2 and H2O2 plays a critical role in plasma-induced cell death,” PLOS ONE, vol. 10, no. 6, Article ID e0128205, 2015. View at Publisher · View at Google Scholar
  36. H. Sies, “Role of metabolic H2O2 generation: redox signaling and oxidative stress,” Journal of Biological Chemistry, vol. 289, no. 13, pp. 8735–8741, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. T. Ma, T. Chen, P. Li et al., “Heme oxygenase-1 (HO-1) protects human lens epithelial cells (SRA01/04) against hydrogen peroxide (H2O2)-induced oxidative stress and apoptosis,” Experimental Eye Research, vol. 146, pp. 318–329, 2016. View at Publisher · View at Google Scholar · View at Scopus
  38. I. Tochitsky, A. Polosukhina, V. E. Degtyar et al., “Restoring visual function to blind mice with a photoswitch that exploits electrophysiological remodeling of retinal ganglion cells,” Neuron, vol. 81, no. 4, pp. 800–813, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. A. J. Hill, I. Zwart, H. H. Tam et al., “Human umbilical cord blood-derived mesenchymal stem cells do not differentiate into neural cell types or integrate into the retina after intravitreal grafting in neonatal rats,” Stem Cells and Development, vol. 18, no. 3, pp. 399–409, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. A.-J. Carr, A. A. Vugler, S. T. Hikita et al., “Protective effects of human iPS-derived retinal pigment epithelium cell transplantation in the retinal dystrophic rat,” PLOS ONE, vol. 4, no. 12, Article ID e8152, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Panieri, V. Gogvadze, E. Norberg, R. Venkatesh, S. Orrenius, and B. Zhivotovsky, “Reactive oxygen species generated in different compartments induce cell death, survival, or senescence,” Free Radical Biology and Medicine, vol. 57, pp. 176–187, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. B. M. Marte and J. Downward, “PKB/Akt: connecting phosphoinositide 3-kinase to cell survival and beyond,” Trends in Biochemical Sciences, vol. 22, no. 9, pp. 355–358, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Sun, Y. Jin, L. Dong, R. Sumi, R. Jahan, and Z. Li, “The neuroprotective effects of coccomyxa gloeobotrydiformis on the ischemic stroke in a rat model,” International Journal of Biological Sciences, vol. 9, no. 8, pp. 811–817, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. Q. Zhang, W.-D. Huang, X.-Y. Lv, and Y.-M. Yang, “Ghrelin protects H9c2 cells from hydrogen peroxide-induced apoptosis through NF-κB and mitochondria-mediated signaling,” European Journal of Pharmacology, vol. 654, no. 2, pp. 142–149, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Han, P. Tan, Z. Li et al., “Fuzi attenuates diabetic neuropathy in rats and protects schwann cells from apoptosis induced by high glucose,” PLOS ONE, vol. 9, no. 1, Article ID e86539, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. S. M. Pereira, D. Moss, S. R. Williams, P. Murray, and A. Taylor, “Overexpression of the MRI reporter genes ferritin and transferrin receptor affect iron homeostasis and produce limited contrast in mesenchymal stem cells,” International Journal of Molecular Sciences, vol. 16, no. 7, pp. 15481–15496, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. V. Ionta, W. Liang, E. H. Kim et al., “SHOX2 overexpression favors differentiation of embryonic stem cells into cardiac pacemaker cells, improving biological pacing ability,” Stem Cell Reports, vol. 4, no. 1, pp. 129–142, 2015. View at Publisher · View at Google Scholar · View at Scopus