Abstract
Successes associated with cardiac transplantation in newborn infants, especially ABO-incompatible transplantation, may offer lessons pertinent for the transplantation of organs and tissues from animals into man, that is, xenotransplantation. For example, the scarcity of hearts of suitable size and condition for transplantation in newborn infants with severe cardiac failure, which motivated the use of ABO-incompatible hearts, also motivates consideration of using hearts from animals in lieu of hearts from humans, i.e., xenotransplantation, for this purpose. Clearly, xenotransplantation could address this problem, but the various biological barriers to xenotransplantation, especially the immune barrier, may preclude application of this approach. Because several components of the immune barrier to xenotransplantation are modeled by ABO-incompatible allografts, insights drawn from the successful transplantation of ABO-incompatible hearts in newborn infants might be pertinent to the application of xenotransplantation in infants or, indeed, in all human recipients. Here, we review those insights and discuss the potential relevance for xenotransplantation.
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Abbreviations
- Gal:
-
Galactose-α1,3-galactose
- HLA:
-
Human leukocyte antigen
References
Platt JL, West LJ, Chinnock RE, Cascalho M. Toward a solution for cardiac failure in the newborn. Xenotransplantation. 2018;25:e12479.
West LJ, Pollock-Barziv SM, Dipchand AI, et al. ABO-incompatible heart transplantation in infants. N Engl J Med. 2001;344:793–800.
Hammer C, Chaussy CH, Brendel W. Preformed natural antibodies in animals and man: outlook on xenotransplantation. Eur Surg Res. 1973;5:162166.
Hammer C. Isohemagglutinins and preformed natural antibodies in xenogeneic organ transplantation. Transplant Proc. 1987;19:4443–7.
Platt JL, Vercellotti GM, Dalmasso AP, et al. Transplantation of discordant xenografts: a review of progress. Immunol Today. 1990;11:450–6.
Parker W, Saadi S, Lin SS, Holzknecht ZE, Bustos M, Platt JL. Transplantation of discordant xenografts: a challenge revisited. Immunol Today. 1996;17:373–8.
Cascalho M, Platt JL. The immunological barrier to xenotransplantation. Immunity. 2001;14:437–46.
Hume DM, Merrill JP, Miller BF, Thorn GW. Experiences with renal homotransplantation in the human: report of nine cases. J Clin Investig. 1955;34:327–82.
Starzl TE, Marchioro TL, Holmes JH, et al. Renal homografts in patients with major donor-recipient blood group incompatibilities. Surgery. 1964;55:195–209.
Gleason RE, Murray JE. Report from kidney transplant registry: analysis of variables in the function of human kidney transplants. Transplantation. 1967;5:343–59.
Wilbrandt R, Tung KSK, Deodhar SD, Nakamoto S, Kolff WJ. ABO blood group incompatibility in human renal homotransplantation. Am J Clin Pathol. 1969;51:15–23.
Moore FD, Burch GE, Harken DE, Swan HJ, Murray JE, Lillihei CW. Cardiac and other organ transplantation. In the setting of transplant science as a national effort. JAMA. 1968;206:2489–500.
Rapaport FT, Dausset J. Activity of the ABO antigen system as a determinant of histocompatibility in human transplantation. Transplant Proc. 1987;19:4487–91.
Alexandre GP, De Bruyere M, Squifflet JP, Moriau M, Latinne D, Pirson Y. Human ABO-incompatible living donor renal homografts. Neth J Med. 1985;28:231–4.
Alexandre GPJ, Squifflet JP, De Bruyere M, et al. Present experiences in a series of 26 ABO-incompatible living donor renal allografts. Transplant Proc. 1987;19:4538–42.
Breimer ME, Brynger H, Le Pendu J, et al. Blood group ABO-incompatible kidney transplantation biochemical and immunochemical studies of blood group A glycolipid antigens in human kidney and characterization of the antibody response (antigen specificity and antibody class) in O recipients receiving A2 grafts. Transplant Proc. 1987;19:226–30.
Paul LC, van Es LA, de la Reviere GB, Eernisse G, de Graeff J. Blood group B antigen on renal endothelium as the target for rejection in an ABO-incompatible recipient. Transplantation. 1978;26:268–71.
Chopek MW, Simmons RL, Platt JL. ABO-incompatible renal transplantation: initial immunopathologic evaluation. Transplant Proc. 1987;19:4553–7.
Bannett AD, McAlack RF, Morris M, Chopek M, Platt JL. ABO incompatible renal transplantation: a qualitative analysis of native endothelial tissue ABO antigens after transplant. Transplant Proc. 1989;21:783–5.
Koch CA, Khalpey ZI, Platt JL. Accommodation: preventing injury in transplantation and disease. J Immunol. 2004;172:5143–8.
Garcia de Mattos Barbosa M, Cascalho M, Platt JL. Accommodation in ABO-incompatible organ transplants. Xenotransplantation. 2018;25:e12418.
Platt JL, Fischel RJ, Matas AJ, Reif SA, Bolman RM, Bach FH. Immunopathology of hyperacute xenograft rejection in a swine-to-primate model. Transplantation. 1991;52:214–20.
Platt JL. Xenotransplantation: immunological hurdles and prospects for future success. J Nephrol. 1993;6:182–92.
Lin SS, Weidner BC, Byrne GW, et al. The role of antibodies in acute vascular rejection of pig-to-baboon cardiac transplants. J Clin Investig. 1998;101:1745–56.
Opelz G, Morath C, Susal C, Tran TH, Zeier M, Dohler B. Three-year outcomes following 1420 ABO-incompatible living-donor kidney transplants performed after ABO antibody reduction: results from 101 centers. Transplantation. 2015;99:400–4.
Montgomery JR, Berger JC, Warren DS, James NT, Montgomery RA, Segev DL. Outcomes of ABO-incompatible kidney transplantation in the United States. Transplantation. 2012;93:603–9.
Tanabe K, Ishida H, Inui M, et al. ABO-incompatible kidney transplantation: long-term outcomes. Clin Transpl. 2013:307–12.
Bustos M, Platt JL. The pathology of cardiac xenografts. J Card Surg. 2001;16:357–62.
Chinnakotla S, Verghese P, Chavers B, et al. Outcomes and risk factors for graft loss: lessons learned from 1,056 pediatric kidney transplants at the University of Minnesota. J Am Coll Surg. 2017;224:473–86.
McCurry KR, Kooyman DL, Alvarado CG, et al. Human complement regulatory proteins protect swine-to-primate cardiac xenografts from humoral injury. Nat Med. 1995;1:423–7.
Pierson RN, Winn HJ, Russell PS, Auchincloss H. Xenogeneic skin graft rejection is especially dependent on CD4+ T cells. J Exp Med. 1989;170:991–6.
Lawson JH, Platt JL. Molecular barriers to xenotransplantation. Transplantation. 1996;62:303–10.
Hammer C. Physiological obstacles after xenotransplantation. Ann N Y Acad Sci. 1998;862:19–27.
Platt JL, Cascalho M, Piedrahita JA. Xenotransplantation: progress along paths uncertain from models to application. ILAR J. 2018;59:286–308.
Bergenfeldt H, Andersson B, Bucin D, et al. Outcomes after ABO-incompatible heart transplantation in adults: a registry study. J Heart Lung Transplant. 2015;34:892–8.
Urschel S, West LJ. ABO-incompatible heart transplantation. Curr Opin Pediatr. 2016;28:613–9.
Dipchand AI, Pollock-Barziv SM, Manlhiot C, West LJ, Vandervliet M, McCrindle BW. Equivalent outcomes for pediatric heart transplantation recipients: ABO-blood group incompatible versus ABO-compatible. Am J Transplant. 2009;10:389–97.
Henderson HT, Canter CE, Mahle WT, et al. ABO-incompatible heart transplantation: analysis of the Pediatric Heart Transplant Study (PHTS) database. J Heart Lung Transplant. 2012;31:173–9.
Parker W, Bruno D, Platt JL. Xenoreactive natural antibodies in the world of natural antibodies: typical or unique? Transpl Immunol. 1995;3:181–91.
Parker W, Lundberg-Swanson K, et al. Isohemagglutinins and xenoreactive antibodies are members of a distinct family of natural antibodies. Hum Immunol. 1996;45:94–104.
Chinnock RE, Bailey LL. Heart transplantation for congenital heart disease in the first year of life. Curr Cardiol Rev. 2011;7:72–84.
Copeland H, Razzouk A, Chinnock R, Deming D, Hasaniya N, Bailey L. Pediatric recipient survival beyond 15 post-heart transplant years: a single-center experience. Ann Thorac Surg. 2014;98:2145–50; discussion 50–51.
John M, Bailey LL. Neonatal heart transplantation. Ann Cardiothorac Surg. 2018;7:118–25.
Dipchand AI. Current state of pediatric cardiac transplantation. Ann Cardiothorac Surg. 2018;7:31–55.
Urschel S, Meyer SR, Larsen IM, et al. Absence of donor-specific anti-HLA antibodies after ABO-incompatible heart transplantation in infancy - altered immunity or age? Am J Transplant. 2010;10:149–56.
Kobayashi D, Du W, L'Ecuyer TJ. Predictors of cardiac allograft vasculopathy in pediatric heart transplant recipients. Pediatr Transplant. 2013;17:436–40.
Chen CY, Warner P, Albers EL, et al. Donor-specific anti-HLA antibody production following pediatric ABO-incompatible heart transplantation. Pediatr Transplant. 2019;23:e13332.
Fan X, Ang A, Pollock-BarZiv SM, et al. Donor-specific B-cell tolerance after ABO-incompatible infant heart transplantation. Nat Med. 2004;10:1227–33.
Cooper DKC, Hara H, Iwase H, Banks CA, Cleveland DC. An approach to induction of tolerance to pig cardiac xenografts in neonates. Xenotransplantation. 2018;25(6):e12454.
Lombardi G, Sidhu S, Daly M, Batchelor JR, Makgoba W, Lechler RI. Are primary alloresponses truly primary? Int Immunol. 1990;2:9–13.
Saadi S, Holzknecht RA, Patte CP, Stern DM, Platt JL. Complement-mediated regulation of tissue factor activity in endothelium. J Exp Med. 1995;182:1807–14.
Saadi S, Platt JL. Transient perturbation of endothelial integrity induced by natural antibodies and complement. J Exp Med. 1995;181:21–31.
Malyguine AM, Saadi S, Platt JL, Dawson JR. Human natural killer cells induce morphologic changes in porcine endothelial cell monolayers. Transplantation. 1996;61:161–4.
Malyguine AM, Saadi S, Holzknecht RA, et al. Induction of procoagulant function in porcine endothelial cells by human NK cells. J Immunol. 1997;159:4659–64.
Bustos M, Coffman TM, Saadi S, Platt JL. Modulation of eicosanoid metabolism in endothelial cells in a xenograft model: role of cyclooxygenase-2. J Clin Investig. 1997;100:1150–8.
Nagayasu T, Saadi S, Holzknecht RA, Patte CA, Plummer TB, Platt JL. Expression of tissue factor mRNA in cardiac xenografts: clues to the pathogenesis of acute vascular rejection. Transplantation. 2000;69:475–82.
Bustos M, Saadi S, Platt JL. Platelet-mediated activation of endothelial cells: implications for the pathogenesis of transplant rejection. Transplantation. 2001;72:509–15.
Parker W, Lin SS, Platt JL. Antigen expression in xenotransplantation: how low must it go? Transplantation. 2001;71:313–9.
Saadi S, Wrenshall LE, Platt JL. Regional manifestations and control of the immune system. FASEB J. 2002;16:849–56.
Williams JM, Holzknecht ZE, Plummer TB, Lin SS, Brunn GJ, Platt JL. Acute vascular rejection and accommodation: divergent outcomes of the humoral response to organ transplantation. Transplantation. 2004;78:1471–8.
Bach FH, Ferran C, Hechenleitner P, et al. Accommodation of vascularized xenografts: expression of “protective genes” by donor endothelial cells in a host Th2 cytokine environment. Nat Med. 1997;3:196–204.
Parker W, Holzknecht ZE, Song A, et al. Fate of antigen in xenotransplantation: implications for acute vascular rejection and accommodation. Am J Pathol. 1998;152:829–39.
Altman B. Tissue transplantation: circulating antibody in the homotransplantation of kidney and skin. Ann R Coll Surg Engl. 1963;33:79–104.
Milgrom F, Litvak BI, Kano K, Witebsky E. Humoral antibodies in renal homograft. JAMA. 1966;198:226–30.
Platt JL, Cascalho M. Donor specific antibodies after transplantation. Pediatr Transplant. 2011;15:686–90.
Cascalho MI, Chen BJ, Kain M, Platt JL. The paradoxical functions of B cells and antibodies in transplantation. J Immunol. 2013;190:875–9.
Lynch RJ, Silva IA, Chen BJ, Punch JD, Cascalho M, Platt JL. Cryptic B cell response to renal transplantation. Am J Transplant. 2013;13:1713–23.
Ali SR, Hippenmeyer S, Saadat LV, Luo L, Weissman IL, Ardehali R. Existing cardiomyocytes generate cardiomyocytes at a low rate after birth in mice. Proc Natl Acad Sci U S A. 2014;111:8850–5.
van Berlo JH, Molkentin JD. An emerging consensus on cardiac regeneration. Nat Med. 2014;20:1386–93.
Zhang Y, Mignone J, MacLellan WR. Cardiac regeneration and stem cells. Physiol Rev. 2015;95:1189–204.
Sereti KI, Nguyen NB, Kamran P, et al. Analysis of cardiomyocyte clonal expansion during mouse heart development and injury. Nat Commun. 2018;9:754.
Zhou X, Merchak K, Lee W, Grande JP, Cascalho M, Platt JL. Cell fusion connects oncogenesis with tumor evolution. Am J Pathol. 2015;185:2049–460.
Dolle ME, Snyder WK, Gossen JA, Lohman PH, Vijg J. Distinct spectra of somatic mutations accumulated with age in mouse heart and small intestine. Proc Natl Acad Sci U S A. 2000;97:8403–8.
Ogle BM, Butters KB, Plummer TB, et al. Spontaneous fusion of cells between species yields transdifferentiation and retroviral in vivo. FASEB J. 2004;18:548–50.
Ogle BM, Cascalho M, Platt JL. Biological implications of cell fusion. Nat Rev Mol Cell Biol. 2005;6:567–75.
Bailey LL, Gundry SR. Survival following orthotopic cardiac xenotransplantation between juvenile baboon recipients and concordant and discordant donor species: foundation for clinical trials. World J Surg. 1997;21:943–50.
Platt JL, Nath KA. Heme oxygenase: protective gene or Trojan horse. Nat Med. 1998;4:1364–5.
Platt JL, Cascalho M. IgM in the kidney: a multiple personality disorder. Kidney Int. 2015;88:439–41.
Platt JL, Kaufman CL, Garcia de Mattos Barbosa M, Cascalho M. Accommodation and related conditions in vascularized composite allografts. Curr Opin Organ Transplant. 2017;22:470–6.
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Supported by grants from the National Institutes of Health (AI123262, AI122369, OD023138)
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Platt, J.L., Cascalho, M. (2020). Lessons from ABO-Incompatible Cardiac Allotransplantation in the Newborn. In: Cooper, D.K.C., Byrne, G. (eds) Clinical Xenotransplantation. Springer, Cham. https://doi.org/10.1007/978-3-030-49127-7_12
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