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Journal of Transplantation
Volume 2012 (2012), Article ID 740653, 10 pages
http://dx.doi.org/10.1155/2012/740653
Research Article

Gene Transfer of Heme Oxygenase-1 Using an Adeno-Associated Virus Serotype 6 Vector Prolongs Cardiac Allograft Survival

1Department of Anesthesiology Critical Care Medicine, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA
2Department of Cardiothoracic Surgery, Children's Hospital Los Angeles, Los Angeles, CA 90027, USA
3Department of Pathology and Human Anatomy, Loma Linda University School of Medicine, Alumni Hall Room 326, 11021 Campus Street, Loma Linda, CA 92350, USA

Received 18 May 2012; Revised 7 September 2012; Accepted 7 September 2012

Academic Editor: Simon Robson

Copyright © 2012 Jacqueline M. Evans 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. M. Velez and M. R. Johnson, “Management of allosensitized cardiac transplant candidates,” Transplantation Reviews, vol. 23, no. 4, pp. 235–247, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. I. Kaczmarek, M. A. Deutsch, T. Kauke et al., “Donor-specific HLA alloantibodies: long-term impact on cardiac allograft vasculopathy and mortality after heart transplant,” Experimental and Clinical Transplantation, vol. 6, no. 3, pp. 229–235, 2008. View at Scopus
  3. C. Larosa, B. H. Jorge, and K. E. C. Meyers, “Outcomes in pediatric solid-organ transplantation,” Pediatric Transplantation, vol. 15, no. 2, pp. 128–141, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. M. N. Scherer, B. Banas, K. Mantouvalou et al., “Current concepts and perspectives of immunosuppression in organ transplantation,” Langenbeck's Archives of Surgery, vol. 392, no. 5, pp. 511–523, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. J. D. Vega, J. Moore, S. Murray, J. M. Chen, M. R. Johnson, and D. B. Dyke, “Heart transplantation in the United States, 1998–2007,” American Journal of Transplantation, vol. 9, no. 4, pp. 932–941, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Schrem, H. Barg-Hock, C. P. Strassburg, A. Schwarz, and J. Klempnauer, “Aftercare for patients with transplanted organs,” Deutsches Arzteblatt, vol. 106, no. 9, pp. 148–156, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Vassalli, S. Fleury, J. Li, J. J. Goy, L. Kappenberger, and L. K. Von Segesser, “Gene transfer of cytoprotective and immunomodulatory molecules for prevention of cardiac allograft rejection,” European Journal of Cardio-thoracic Surgery, vol. 24, no. 5, pp. 794–806, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. B. K. Brar, A. Stephanou, M. J. D. Wagstaff et al., “Heat shock proteins delivered with a virus vector can protect cardiac cells against apoptosis as well as against thermal or hypoxic stress,” Journal of Molecular and Cellular Cardiology, vol. 31, no. 1, pp. 135–146, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Fu, D. Chen, X. Mao, N. Zhang, Y. Ding, and J. S. Bromberg, “Feline immunodeficiency virus-mediated viral interleukin-10 gene transfer prolongs non-vascularized cardiac allograft survival,” American Journal of Transplantation, vol. 3, no. 5, pp. 552–561, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Furukawa, K. Oshima, T. Tung, G. Cui, H. Laks, and L. Sen, “Liposome-mediated combinatorial cytokine gene therapy induces localized synergistic immunosuppression and promotes long-term survival of cardiac allografts,” Journal of Immunology, vol. 174, no. 11, pp. 6983–6992, 2005. View at Scopus
  11. R. Brauner, M. Nonoyama, H. Laks et al., “Intracoronary adenovirus-mediated transfer of immunosuppressive cytokine genes prolongs allograft survival,” Journal of Thoracic and Cardiovascular Surgery, vol. 114, no. 6, pp. 923–933, 1997. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Katori, R. Buelow, B. Ke et al., “Heme oxygenase-1 overexpression protects rat hearts from cold ischemia/reperfusion injury via an antiapoptotic pathway,” Transplantation, vol. 73, no. 2, pp. 287–292, 2002. View at Scopus
  13. Y. Akamatsu, M. Haga, S. Tyagi et al., “Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury,” The FASEB Journal, vol. 18, no. 6, pp. 771–772, 2004. View at Scopus
  14. L. G. Melo, R. Agrawal, L. Zhang et al., “Gene therapy strategy for long-term myocardial protection using adeno-associated virus-mediated delivery of heme oxygenase gene,” Circulation, vol. 105, no. 5, pp. 602–607, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. S. R. Vulapalli, Z. Chen, B. H. L. Chua, T. Wang, and C. S. Liang, “Cardioselective overexpression of HO-1 prevents I/R-induced cardiac dysfunction and apoptosis,” American Journal of Physiology, vol. 283, no. 2, pp. H688–H694, 2002. View at Scopus
  16. S. F. Yet, R. Tian, M. D. Layne et al., “Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice,” Circulation Research, vol. 89, no. 2, pp. 168–173, 2001. View at Scopus
  17. J. Ma, C. K. Lau, A. Obed et al., “A cell penetrating heme oxygenase protein protects heart graft against ischemia/reperfusion injury,” Gene Therapy, vol. 16, no. 3, pp. 320–328, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Katori, R. W. Busuttil, and J. W. Kupiec-Weglinski, “Heme oxygenase-1 system in organ transplantation,” Transplantation, vol. 74, no. 7, pp. 905–912, 2002. View at Scopus
  19. S. G. Tullius, M. Nieminen-Kelhä, R. Buelow et al., “Inhibition of ischemia/reperfusion injury and chronic graft deterioration by a single-donor treatment with cobalt-protoporphyrin for the induction of heme oxygenase-1,” Transplantation, vol. 74, no. 5, pp. 591–598, 2002. View at Scopus
  20. M. P. Soares, Y. Lin, J. Anrather et al., “Expression of heme oxygenase-1 can determine cardiac xenograft survival,” Nature Medicine, vol. 4, no. 9, pp. 1073–1077, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. W. W. Hancock, R. Buelow, M. H. Sayegh, and L. A. Turka, “Antibody-induced transplant arteriosclerosis is prevented by graft expression of anti-oxidant and anti-apoptotic genes,” Nature Medicine, vol. 4, no. 12, pp. 1392–1396, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Yamashita, R. Öllinger, J. McDaid et al., “Heme oxygenase-1 is essential for and promotes tolerance to transplanted organs,” FASEB Journal, vol. 20, no. 6, pp. 776–778, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. J. A. Araujo, L. Meng, A. D. Tward et al., “Systemic rather than local heme oxygenase-1 overexpression improves cardiac allograft outcomes in a new transgenic mouse,” Journal of Immunology, vol. 171, no. 3, pp. 1572–1580, 2003. View at Scopus
  24. L. A. Debruyne, J. C. Magee, R. Buelow, and J. S. Bromberg, “Gene transfer of immunomodulatory peptides correlates with heme oxygenase-1 induction and enhanced allograft survival,” Transplantation, vol. 69, no. 1, pp. 120–128, 2000. View at Scopus
  25. D. A. Tulis, W. Durante, K. J. Peyton, A. J. Evans, and A. I. Schafer, “Heme oxygenase-1 attenuates vascular remodeling following balloon injury in rat carotid arteries,” Atherosclerosis, vol. 155, no. 1, pp. 113–122, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. H. J. Duckers, M. Boehm, A. L. True et al., “Heme oxygenase-1 protects against vascular constriction and proliferation,” Nature Medicine, vol. 7, no. 6, pp. 693–698, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. L. E. Otterbein, B. S. Zuckerbraun, M. Haga et al., “Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury,” Nature Medicine, vol. 9, no. 2, pp. 183–190, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. W. Durante, “Heme oxygenase-1 in growth control and its clinical application to vascular disease,” Journal of Cellular Physiology, vol. 195, no. 3, pp. 373–382, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Chauveau, D. Bouchet, J. C. Roussel et al., “Gene transfer of heme oxygenase-1 and carbon monoxide delivery inhibit chronic rejection,” American Journal of Transplantation, vol. 2, no. 7, pp. 581–592, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Bouchet, C. Chauveau, J. C. Roussel et al., “Inhibition of graft arteriosclerosis development in rat aortas following heme oxygenase-1 gene transfer,” Transplant Immunology, vol. 9, no. 2–4, pp. 235–238, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Braudeau, D. Bouchet, L. Tesson et al., “Induction of long-term cardiac allograft survival by heme oxygenase-1 gene transfer,” Gene Therapy, vol. 11, no. 8, pp. 701–710, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. Yang, Q. Li, H. C. J. Ertl, and J. M. Wilson, “Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses,” Journal of Virology, vol. 69, no. 4, pp. 2004–2015, 1995. View at Scopus
  33. P. E. Monahan and R. J. Samulski, “Adeno-associated virus vectors for gene therapy: more pros than cons?” Molecular Medicine Today, vol. 6, no. 11, pp. 433–440, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Mueller and T. R. Flotte, “Clinical gene therapy using recombinant adeno-associated virus vectors,” Gene Therapy, vol. 15, no. 11, pp. 858–863, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Daya and K. I. Berns, “Gene therapy using adeno-associated virus vectors,” Clinical Microbiology Reviews, vol. 21, no. 4, pp. 583–593, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. D. G. Miller, L. M. Petek, and D. W. Russell, “Adeno-associated virus vectors integrate at chromosome breakage sites,” Nature Genetics, vol. 36, no. 7, pp. 767–773, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. Q. Li, Y. Guo, Q. Ou et al., “Gene transfer as a strategy to achieve permanent cardioprotection II: rAAV-mediated gene therapy with heme oxygenase-1 limits infarct size 1 year later without adverse functional consequences,” Basic Research in Cardiology, vol. 106, no. 6, pp. 1367–1377, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. A. S. Pachori, L. G. Melo, L. Zhang, S. D. Solomon, and V. J. Dzau, “Chronic recurrent myocardial ischemic injury is significantly attenuated by pre-emptive adeno-associated virus heme oxygenase-1 gene delivery,” Journal of the American College of Cardiology, vol. 47, no. 3, pp. 635–643, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. X. Liu, A. S. Pachori, C. A. Ward et al., “Heme oxygenase-1 (HO-1) inhibits postmyocardial infarct remodeling and restores ventricular function,” FASEB Journal, vol. 20, no. 2, pp. 207–216, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Burdorf, N. Schuhmann, J. Postrach et al., “AAV-mediated gene transfer to cardiac cells in a heterotopic rat heart transplantation model,” Transplantation Proceedings, vol. 39, no. 2, pp. 567–568, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. B. Asfour, H. A. Baba, H. H. Scheld, R. H. Hruban, D. Hammel, and B. J. Byrne, “Uniform long-term gene expression using adeno-associated virus (AAV) by ex vivo recirculation in rat-cardiac isografts,” Thoracic and Cardiovascular Surgeon, vol. 50, no. 6, pp. 347–350, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. Z. Chen, L. Lu, J. Li, X. Xiao, J. J. Fung, and S. Qian, “Prolonged survival of heart allografts transduced with AAV-CTLA41g,” Microsurgery, vol. 23, no. 5, pp. 489–493, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Doenecke, E. Frank, M. N. Scherer, H. J. Schlitt, and E. K. Geissler, “Prolongation of heart allograft survival after long-term expression of soluble MHC class I antigens and vIL-10 in the liver by AAV-plasmid-mediated gene transfer,” Langenbeck's Archives of Surgery, vol. 393, no. 3, pp. 343–348, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. J. M. Schirmer, N. Miyagi, V. P. Rao et al., “Recombinant adeno-associated virus vector for gene transfer to the transplanted rat heart,” Transplant International, vol. 20, no. 6, pp. 550–557, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Y. Tsui, X. Wu, C. K. Lau et al., “Prevention of chronic deterioration of heart allograft by recombinant adeno-associated virus-mediated heme oxygenase-1 gene transfer,” Circulation, vol. 107, no. 20, pp. 2623–2629, 2003. View at Scopus
  46. P. Gregorevic, M. J. Blankinship, J. M. Allen et al., “Systemic delivery of genes to striated muscles using adeno-associated viral vectors,” Nature Medicine, vol. 10, no. 8, pp. 828–834, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. S. J. McNally, J. A. Ross, O. James Garden, and S. J. Wigmore, “Optimization of the paired enzyme assay for heme oxygenase activity,” Analytical Biochemistry, vol. 332, no. 2, pp. 398–400, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. R. J. Corry, H. J. Winn, and P. S. Russell, “Primarily vascularized allografts of hearts in mice. The role of H 2D, H 2K, and non H 2 antigens in rejection,” Transplantation, vol. 16, no. 4, pp. 343–350, 1973. View at Scopus
  49. K. Sato, J. Balla, L. Otterbein et al., “Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants,” Journal of Immunology, vol. 166, no. 6, pp. 4185–4194, 2001. View at Scopus
  50. R. de Waal Malefyt, J. Haanen, H. Spits et al., “Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression,” Journal of Experimental Medicine, vol. 174, no. 4, pp. 915–924, 1991. View at Scopus
  51. J. C. Magee, L. A. DeBruyne, R. Buelow, and J. S. Bromberg, “Gene transfer of immunosuppressive peptides B2702 and RDP1257 prolongs allograft survival: evidence suggesting a role for heme oxygenase-I,” Transplantation Proceedings, vol. 31, no. 1-2, p. 1194, 1999. View at Publisher · View at Google Scholar · View at Scopus
  52. B. Ke, X. D. Shen, Y. Zhai et al., “Heme oxygenase 1 mediates the immunomodulatory and antiapoptotic effects of interleukin 13 gene therapy in vivo and in vitro,” Human Gene Therapy, vol. 13, no. 15, pp. 1845–1857, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Guillot, P. Mathieu, H. Coathalem et al., “Tolerance to cardiac allografts via local and systemic mechanisms after adenovirus-mediated CTLA4Ig expression,” Journal of Immunology, vol. 164, no. 10, pp. 5258–5268, 2000. View at Scopus
  54. J. Lee, H. Laks, D. C. Drinkwater et al., “Cardiac gene transfer by intracoronary infusion of adenovirus vector- mediated reporter gene in the transplanted mouse heart,” Journal of Thoracic and Cardiovascular Surgery, vol. 111, no. 1, pp. 246–252, 1996. View at Publisher · View at Google Scholar · View at Scopus
  55. A. H. Schulick, G. Vassalli, P. F. Dunn et al., “Established immunity precludes adenovirus-mediated gene transfer in rat carotid arteries: potential for immunosuppression and vector engineering to overcome barriers of immunity,” Journal of Clinical Investigation, vol. 99, no. 2, pp. 209–219, 1997. View at Scopus
  56. C. Zincarelli, S. Soltys, G. Rengo, W. J. Koch, and J. E. Rabinowitz, “Comparative cardiac gene delivery of adeno-associated virus serotypes 1–9 reveals that AAV6 mediates the most efficient transduction in mouse heart,” Clinical and Translational Science, vol. 3, no. 3, pp. 81–89, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. L. T. Bish, K. Morine, M. M. Sleeper et al., “Adeno-associated virus (AAV) serotype 9 provides global cardiac gene transfer superior to AAV1, AAV6, AAV7, and AAV8 in the mouse and rat,” Human Gene Therapy, vol. 19, no. 12, pp. 1359–1368, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. B. Afzali, G. Lombardi, R. I. Lechler, and G. M. Lord, “The role of T helper 17 (Th17) and regulatory T cells (Treg) in human organ transplantation and autoimmune disease,” Clinical and Experimental Immunology, vol. 148, no. 1, pp. 32–46, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Yamaguchi, K. Fujio, H. Shoda et al., “IL-17B and IL-17C are associated with TNF-α production and contribute to the exacerbation of inflammatory arthritis,” Journal of Immunology, vol. 179, no. 10, pp. 7128–7136, 2007. View at Scopus
  60. S. Itoh, N. Kimura, R. C. Axtell, et al., “Interleukin-17 accelerates allograft rejection by suppressing regulatory T cell expansion,” Circulation, vol. 124, no. 11, supplement, pp. S187–S196, 2011.
  61. A. Awasthi, G. Murugaiyan, and V. K. Kuchroo, “Interplay between effector Th17 and regulatory T cells,” Journal of Clinical Immunology, vol. 28, no. 6, pp. 660–670, 2008. View at Publisher · View at Google Scholar · View at Scopus