Current status of pig lung xenotransplantation

International Journal of Surgery

Volumn 23, Issue , 2015, Pages 247-254

  Kubicki, Natalia ^a   Laird, Christopher ^a   Burdorf, Lars ^a   Pierson, Richard N ^a,b   Azimzadeh, Agnes M ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b Division of Cardiac Surgery   (United States)

Author keywords

Genetically engineered pig; Immune modulation; Immune response; Lung xenotransplantation; Thromboregulation

Indexed keywords

TISSUE FACTOR PATHWAY INHIBITOR; VON WILLEBRAND FACTOR; ANTIBODY;

ADAPTIVE IMMUNITY; BLOOD CLOTTING DISORDER; GENE INACTIVATION; GENE TRANSFER; GRAFT RECIPIENT; GRAFT REJECTION; HUMAN; LUNG TRANSPLANTATION; LUNG XENOTRANSPLANTATION; NONHUMAN; PIG; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; THROMBOSIS; XENOTRANSPLANTATION; ADVERSE EFFECTS; ANIMAL; BABOON; GENETICS; IMMUNOLOGY; LUNG INJURY; PERFUSION; PROCEDURES; TRANSGENIC ANIMAL; XENOGRAFT;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIBODIES; HUMANS; LUNG INJURY; LUNG TRANSPLANTATION; PAPIO; PERFUSION; REPERFUSION INJURY; SWINE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84951573561     PISSN: 17439191     EISSN: 17439159     Source Type: Journal    
DOI: 10.1016/j.ijsu.2015.08.019     Document Type: Review

References (48)

1. Yusen R.D., Edwards L.B., Kucheryavaya A.Y., Benden C., Dipchand A.I., Dobbels F., et al. The registry of the international society for heart and lung transplantation: thirty-first adult lung and Heart-Lung transplant Report-2014; focus theme: retransplantation. J. Hear. Lung Transplant. 2014, 33:1009-1024.
2. den Hengst W.A., Gielis J.F., Lin J.Y., Van Schil P.E., De Windt L.J., Moens A.L. Lung ischemia-reperfusion injury: a molecular and clinical view on a complex pathophysiological process. Am. J. Physiol. Heart Circ. Physiol. 2010, 299:H1283-H1299.
3. Ranieri V.M., Suter P.M., De Tullio R., Dayer J.M., Brienza A., Bruno F., et al. Effect of mechanical ventilation. J. Am. Med. Assoc. 1999, 281:54-61.
4. Pierson R.N., Dorling A., Ayares D., Rees M.A., Seebach J.D., Fishman J.A., et al. Current status of xenotransplantation and prospects for clinical application. Xenotransplantation 2009, 16:263-280.
5. Pierson R.N. Antibody-mediated xenograft injury: mechanisms and protective strategies. Transpl. Immunol. 2009, 21:65-69.
6. Nguyen B.N.H., Azimzadeh A.M., Schroeder C., Buddensick T., Zhang T., Laaris A., et al. Absence of Gal epitope prolongs survival of swine lungs in an ex vivo model of hyperacute rejection. Xenotransplantation 2011, 18:94-107.
7. Nguyen B.N.H., Azimzadeh A.M., Zhang T., Wu G., Shuurman H.J., Sachs D.H., et al. Life-supporting function of genetically modified swine lungs in baboons. J. Thorac. Cardiovasc. Surg. 2007, 133:1354-1363.
8. Cooper D.K., Keogh a M., Brink J., Corris P.A., Klepetko W., Pierson R.N., et al. Report of the xenotransplantation advisory committee of the international society for heart and lung transplantation: the present status of xenotransplantation and its potential role in the treatment of end-stage cardiac and pulmonary diseases. J. Hear. Lung Transplant. 2000, 19:1125-1165.
9. Burdorf L., Azimzadeh A.M., Pierson R.N. Xenogeneic lung transplantation models., in: Methods. Mol. Biol. 2012, 169-189.
10. Sanchez P.G., Bittle G.J., Burdorf L., Pierson R.N., Griffith B.P. State of Art: clinical ex vivo lung perfusion: rationale, current status, and future directions. J. Hear. Lung Transplant. 2012, 31:339-348.
11. Harris D.G., Benipal P.K., Cheng X., Burdorf L., Azimzadeh A.M., Pierson R.N. Four-dimensional characterization of thrombosis in a live-cell, shear-flow assay: development and application to xenotransplantation. PLoS One 2015, 10:e0123015.
12. Burdorf L., Zhang T., Rybak, Elena, et al. Combined GPIb and GPIIb/IIIa blockade prevents sequestration of platelets in a pig-to-human lung perfusion model. Xenotransplantation 2011, 18:287.
13. Mohiuddin M.M., Singh K.A., Corcoran P.C., Hoyt R.F., Thomas M.L., Lewis B.G.T., et al. One-year heterotopic cardiac xenograft survival in a pig to baboon model. Am. J. Transplant. 2014, 14:488-489.
14. Iwase H., Liu H., Wijkstrom M., Zhou H., Singh J., Hara H., Ezzelarab M., Long C., Klein E., Wagner R., Phelps C., Ayares D., Shapiro R., Humar A., Cooper D.K. Pig kidney graft survival in a baboon for 136 days: longest life-supporting organ graft survival to date. Xenotransplantation 2015 Jun 29, 10.1111/xen.12174.
15. Vial C.M., Ostlie D.J., Bhatti F.N.K., Cozzi E., Goddard M., Pino Chavez G., et al. Life supporting function for over one month of a transgenic porcine heart in a baboon. J. Hear. Lung Transplant. 2000, 19:224-229.
16. Burdorf L., Rybak E., Zhang T., Harris D., Dahi S., Kubicki N., et al. Extended life-supporting xenogeneic lung function with multi-Transgeneic donor pigs and targeted drug treatments. Am. J. Transplant. 2015, 15:S3. Abstract number: 1617.
17. Galili U., Shohet S.B., Kobrin E., Stults C.L., Macher B.a Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells. J. Biol. Chem. 1988, 263:17755-17762.
18. Phelps C.J., Koike C., Vaught T.D., Boone J., Wells K.D., Chen H., et al. Production of α1,3-galactosyltransferase-deficient pigs. Science 2011, 299:411-414. (80).
19. Schroeder C., Allan J.S., Nguyen B.N., Wu G., Zhang T., Azimzadeh M.A., et al. Hyperacute rejection is attenuated in GalT knockout swine lungs perfused ex vivo with human blood. Transplant. Proc. 2005, 37:512-513.
20. Gonzalez-Stawinski G.V., Daggett C.W., Lau C.L., Karoor S., Love S.D., Logan J.S., et al. Non-anti-Galα1-3Gal antibody, mechanisms are sufficient to cause hyperacute lung dysfunction in pulmonary xenotransplantation. J. Am. Coll. Surg. 2002, 194:765-773.
21. Chen G., Qian H., Starzl T., Sun H., Garcia B., Wise Y., et al. Acute rejection is associated with antibodies to non-Gal antigens in baboons using Gal-knockout pig kidneys. Nat. Med. 2005, 11:1295-1298.
22. Zhu A., Hurst R. Anti-N-glycolylneuraminic acid antibodies identified in healthy human serum. Xenotransplantation 2002, 9:376-381.
23. Lutz A.J., Li P., Estrada J.L., Sidner R.a, Chihara R.K., Downey S.M., et al. Double knockout pigs deficient in N-glycolylneuraminic acid and Galactose[U+202F]??-1,3-Galactose reduce the humoral barrier to xenotransplantation. Xenotransplantation 2013, 20:27-35.
24. Byrne G.W., Stalboerger P.G., Davila E., Heppelmann C.J., Gazi M.H., Mcgregor H.C.J., et al. Proteomic identification of non-Gal antibody targets after pig-to-primate cardiac xenotransplantation. Xenotransplantation 2008, 15:268-276.
25. Byrne G.W., Stalboerger P.G., Du Z., Davis T.R. C.G. a McGregor, identification of new carbohydrate and membrane protein antigens in cardiac xenotransplantation. Transplantation 2011, 91:287-292.
26. Diamond L.E., Quinn C.M., Martin M.J., Lawson J., Platt J.L., Logan J.S. A human CD46 transgenic pig model system for the study of discordant xenotransplantation. Transplantation 2001, 71:132-142.
27. Miyagawa S., Yamamoto A., Matsunami K., Wang D., Takama Y., Ueno T., et al. Complement regulation in the GalT KO era. Xenotransplantation 2010, 17:11-25.
28. Harris D.G., Quinn K.J., French B.M., Schwartz E., Kang E., Dahi S., et al. Meta-analysis of the independent and cumulative effects of multiple genetic modifications on pig lung xenograft performance during ex vivo perfusion with human blood. Xenotransplantation 2014, 17:102-111.
29. Collins B.J., Blum M.G., Parker R.E., Chang a.C., Blair K.S., Zorn G.L., et al. Thromboxane mediates pulmonary hypertension and lung inflammation during hyperacute lung rejection. J. Appl. Physiol. 2001, 90:2257-2268.
30. Chitko-McKown C.G., Chapes S.K., Brown R.E., Phillips R.M., McKown R.D., Blecha F. Porcine alveolar and pulmonary intravascular macrophages: comparison of immune functions. J. Leukoc. Biol. 1991, 50:364-372.
31. Cantu E., Gaca J.G., Palestrant D., Baig K., Lukes D.J., Gibson S.E., et al. Depletion of pulmonary intravascular macrophages prevents hyperacute pulmonary xenograft dysfunction. Transplantation 2006, 81:1157-1164.
32. Ide K., Wang H., Tahara H., Liu J., Wang X., Asahara T., et al. Role for CD47-SIRPalpha signaling in xenograft rejection by macrophages. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:5062-5066.
33. Khalfoun B., Barrat D., Watier H., Machet M.C., Arbeille-Brassart B., Riess J.G., et al. Development of an ex vivo model of pig kidney perfused with human lymphocytes. Analysis of xenogeneic cellular reactions. Surgery 2000, 128:447-457.
34. Rieben R., Seebach J.D. Xenograft rejection: IgG 1, complement and NK cells team up to activate and destroy the endothelium. Trends Immunol. 2005, 26:2-5.
35. Phelps C.J., Ball S.F., Vaught T.D., Vance A.M., Mendicino M., Monahan J.a., et al. Production and characterization of transgenic pigs expressing porcine CTLA4-Ig. Xenotransplantation 2009, 16:477-485.
36. Cooper D.K.C., Ekser B., Burlak C., Ezzelarab M., Paris L., Tector a.J., et al. Clinical lung xenotransplantation - what donor genetic modifications may be necessary?. Xenotransplantation 2012, 19:144-158.
37. Cowan P.J., Robson S.C., d'Apice A.J.F. Controlling coagulation dysregulation in xenotransplantation. Curr. Opin. Organ Transplant. 2011, 16:214-221.
38. Gaca J.G., Lesher A., Aksoy O., Ruggeri Z.M., Parker W., Davis R.D. The role of the porcine von Willebrand factor: baboon platelet interactions in pulmonary xenotransplantation. Transplantation 2002, 74:1596-1603.
39. Kim Y.T., Lee H.J., Lee S.W., Kim J.Y., Wi H.C., Park S.J., et al. Pre-treatment of porcine pulmonary xenograft with desmopressin: a novel strategy to attenuate platelet activation and systemic intravascular coagulation in an ex-vivo model of swine-to-human pulmonary xenotransplantation. Xenotransplantation 2008, 15:27-35.
40. Burdorf L., Zhang T., Rybak, Elena, et al. Blocking GP1b-vWF interaction by anti-GP1b fab reduces activation and sequestration of platelets in a xenogeneic pig lung perfusion model. J. Hear. Lung Transplant. 2011, 30:S103.
41. Chen D., Riesbeck K., McVey J., Al E. Regulated inhibition of coagulation by porcine endothelial cells expressing P-selectin-tagged hirudin and tissue factor pathway inhibitor fusion proteins. Transplantation 1999, 68:832-839.
42. Ghanekar A., Mendicino M., Liu H., He W., Liu M., Zhong R., et al. Endothelial induction of fgl2 contributes to thrombosis during acute vascular xenograft rejection. J. Immunol. 2004, 172:5693-5701.
43. Roussel J.C., Moran C.J., Salvaris E.J., Nandurkar H.H., D'Apice a.J.F., Cowan P.J. Pig thrombomodulin binds human thrombin but is a poor cofactor for activation of human protein C and TAFI. Am. J. Transplant. 2008, 8:1101-1112.
44. Petersen B., Ramackers W., Tiede A., Lucas-Hahn A., Herrmann D., Barg-Kues B., et al. Pigs transgenic for human thrombomodulin have elevated production of activated protein C. Xenotransplantation 2009, 16:486-495.
45. Peterson B., Ramackers W., Tiede A., Al E. Pigs transgenic for human thrombomodulin have elevated production of activated protein C. Xenotransplantation 2009, 16:486-495.
46. Harris D., Benipal P., Gao Z., Al E. Activated protein C decreases thrombosis on porcine endothelium transgenic for human endothelial protein C receptor-A novel mechanism to decrease porcine xenograft injury. J. Surg. Res. 2014, 186:579.
47. Crikis S., Lu B., Murray-Segal L.M., Selan C., Robson S.C., D'Apice a.J.F., et al. Transgenic overexpression of CD39 protects against renal ischemia-reperfusion and transplant vascular injury. Am. J. Transplant. 2010, 10:2586-2595.
48. Higginbotham L., Mathews D., Breeden C.A., Song M., Farris A.B., Larsen C.P., Ford M.L., Lutz A.J., Tector M., Newell K.A., Tector A.J., Adams A.B. Pre-transplant antibody screening and anti-CD154 costimulation blockade promote long-term xenograft survival in a pig-to-primate kidney transplant model. Xenotransplantation 2015 May, 22(3):221-230.