Immunologic benefit of maternal donors in pediatric living donor liver transplantation.
Treg
living donor liver transplantation
maternal living donor allograft
maternal-fetal microchimerism
pediatric liver transplantation
spontaneous operational tolerance
Journal
Pediatric transplantation
ISSN: 1399-3046
Titre abrégé: Pediatr Transplant
Pays: Denmark
ID NLM: 9802574
Informations de publication
Date de publication:
11 2019
11 2019
Historique:
received:
30
04
2019
revised:
18
06
2019
accepted:
08
07
2019
pubmed:
14
8
2019
medline:
26
8
2020
entrez:
13
8
2019
Statut:
ppublish
Résumé
Long-term follow-up has suggested that pediatric LDLT may have superior outcomes compared to deceased donor recipients. In this review, we describe the subset of LDLT recipients with maternal donors that have lower reported rates of rejection and improved allograft survival. Pediatric LDLT recipients, particularly those with a primary diagnosis of biliary atresia who receive grafts from their mothers, have been reported to have lower rates of acute cellular rejection post-transplant and graft failure. Maternal-fetal microchimerism and the persistence of regulatory T cells may be related to improved outcomes observed in recipients with maternal donors. Further, recent studies have shown that up to 60% of pediatric LDLT recipients can undergo intentional withdrawal of immunosuppression and achieve long-term operational tolerance. The impact of graft type on operational tolerance has not been thoroughly investigated; however, investigation of tolerant pediatric LDLT patients with maternal donors may provide key insights into the mechanisms of immune tolerance. While excellent outcomes can be achieved in pediatric LDLT, there is still a measurable decrease in graft and patient survival over time post-transplant. Recipients of maternal donor liver transplants are a subset of patients who may be advantaged toward improved outcomes by means of immune tolerance.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13560Subventions
Organisme : NIAID NIH HHS
ID : R01 AI145813
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL144790
Pays : United States
Informations de copyright
© 2019 Wiley Periodicals, Inc.
Références
Kim WR, Lake JR, Smith JM, et al. OPTN/SRTR 2015 annual data report: liver. Am J Transplant. 2017;17:174-251.
Kasahara M, Sakamoto S, Fukuda A. Pediatric living-donor liver transplantation. Semin Pediatr Surg. 2017;26(4):224-232.
Mogul D, Chow E, Luo X, et al. Racial and ethnic variations in donor type among pediatric liver transplant recipients. Hepatology. 2015;62:1056-1064.
Ueda M, Oike F, Ogura Y, et al. Long-term outcomes of 600 living donor liver transplants for pediatric patients at a single center. Liver Transplant. 2006;12(9):1326-1336.
Bonanno AP, Saad WA, Ribeiro M. Pediatric liver transplantation: comparison between results from deceased and living related transplantation. Transplant Proc. 2008;40(3):720-721.
Hong JC, Yersiz H, Farmer DG, et al. Longterm outcomes for whole and segmental liver grafts in adult and pediatric liver transplant recipients: a 10-year comparative analysis of 2,988 cases. J Am Coll Surg. 2009;208(5 PG-682-689; discusion 689-691):682-689; discusion 689. Available from: NS -.
Laurence JM, Sapisochin G, DeAngelis M, et al. Biliary complications in pediatric liver transplantation: Incidence and management over a decade. Liver Transpl. 2015;21(8 PG-1082-1090):1082-1090. Available from: NS.
Olthoff KM, Smith AR, Abecassis M, et al. Defining long-term outcomes with living donor liver transplantation in North America. Ann Surg. 2015;262(3):465-475.
Yankol Y, Fernandez LA, Kanmaz T, et al. Results of pediatric living donor compared to deceased donor liver transplantation in the PELD/MELD era: experience from two centers on two different continents. Pediatr Transplant. 2016;20(1):72-82.
Mogul DB, Luo X, Bowring MG, et al. Fifteen-year trends in pediatric liver transplants: split, whole deceased, and living donor grafts. J Pediatr. 2018;196:148-153.e2.
Kehar M, Parekh RS, Stunguris J, et al. Superior outcomes and reduced wait times in pediatric recipients of living donor liver transplantation. Transplant Direct. 2019;5(3):e430.
Chung P, Chan SC, Mok V, Tam P, Lo CM. Recipient body size does not matter in pediatric liver transplantation. J Pediatr Surg. 2014;49(12):1734-1737.
Eboli L, Tannuri AC, Gibelli N, Silva T, Braga P, Tannuri U. Comparison of the results of living donor liver transplantation due to acute liver failure and biliary atresia in a quaternary center. Transplant Proc. 2017;49(4):832-835.
Haberal M, Sevmis S, Karakayali H, et al. Pediatric liver transplant: results of a single center. Exp Clin Transplant. 2008;6(1):7-13.
Laurence JM, Sapisochin G, DeAngelis M, et al. Biliary complications in pediatric liver transplantation: Incidence and management over a decade. Liver Transpl. 2015;21(8):1082-1090.
De Jonge J, Kurian S, Shaked A, et al. Unique early gene expression patterns in human adult-to-adult living donor liver grafts compared to deceased donor grafts. Am J Transplant. 2009;9:758-772.
Sanada Y, Kawano Y, Miki A, et al. Maternal grafts protect daughter recipients from acute cellular rejection after pediatric living donor liver transplantation for biliary atresia. Transpl Int. 2014;27(4):383-390.
Przybyszewski EM, Verna EC, Lobritto SJ, et al. Clinical and immunologic advantage of living donor liver transplantation in children. Transplantation. 2018;102(6):953-960.
Yi NJ, Park MS, Song EY, et al. Pretransplantation fetal-maternal microchimerism in pediatric liver transplantation from mother. World J Gastroenterol. 2017;23(45):8017-8026.
Gurevich M, Guy-Viterbo V, Janssen M, et al. Living donor liver transplantation in children surgical and immunological results in 250 recipients at université catholique de louvain. Ann Surg. 2015;262(6):1141-1149.
Nijagal A, Fleck S, Hills NK, et al. Decreased risk of graft failure with maternal liver transplantation in patients with biliary atresia. Am J Transplant. 2012;12(2):409-419.
Lim WH, McDonald SP, Coates PT, Chapman JR, Russ GR, Wong G. Maternal compared with paternal donor kidneys are associated with poorer graft outcomes after kidney transplantation. Kidney Int. 2016;89:659-665.
Brenner BM, Milford EL. Nephron underdosing: a programmed cause of chronic renal allograft failure. Am J Kidney Dis. 1993;21(5):66-72.
Kolonko A, Chudek J, Wiecek A. Nephron underdosing as a risk factor for impaired early kidney graft function and increased graft loss during the long-term follow-up period. Transplant Proc. 2013;45(4):1639-1643.
Smits J, Claas F, van Houwelingen HC, Persijn GG. Do noninherited maternal antigens (NIMA) enhance renal graft survival? Transpl Int. 1998;11(2):82-88.
Burlingham WJ, Grailer AP, Heisey DM, et al. The effect of tolerance to noninherited maternal HLA antigens on the survival of renal transplants from sibling donors. N Engl J Med. 1998;339(23):1657-1664.
Levitsky J, Goldberg D, Smith AR, et al. Acute rejection increases risk of graft failure and death in recent liver transplant recipients. Clin Gastroenterol Hepatol. 2017;15(4):584-593.e2.
Maloney S, Smith A, Furst DE, et al. Microchimerism of maternal origin persists into adult life. J Clin Invest. 1999;104(1):41-47.
Rosenblum MD, Way SS, Abbas AK. Regulatory T cell memory. Nat Rev Immunol. 2016;16(2):90-101.
Li Y, Zhao X, Cheng D, et al. The presence of Foxp3 expressing T cells within grafts of tolerant human liver transplant recipients. Transplantation. 2008;86(12):1837-1843.
Taubert R, Danger R, Londoño MC, et al. Hepatic infiltrates in operational tolerant patients after liver transplantation show enrichment of regulatory T cells before proinflammatory genes are downregulated. Am J Transplant. 2016;16(4):1285-1293.
Miyao T, Floess S, Setoguchi R, et al. Plasticity of Foxp3(+) T cells reflects promiscuous Foxp3 expression in conventional T cells but not reprogramming of regulatory T cells. Immunity. 2012;36(2):262-275.
Tran DQ, Ramsey H, Shevach EM. Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor- dependent but does not confer a regulatory phenotype. Blood. 2007;110(8):2983-2990.
Andrassy J, Kusaka S, Jankowska-Gan E, et al. Tolerance to noninherited maternal MHC antigens in mice. J Immunol. 2003;171(10):5554-5561.
Mold JE, Michaelsson J, Burt TD, et al. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science. 2008;322(5907):1562-1565.
Dutta P, Molitor-Dart M, Bobadilla JL, et al. Microchimerism is strongly correlated with tolerance to noninherited maternal antigens in mice. Blood. 2009;114(17):3578-3587.
Zhou L, Yoshimura Y, Huang YY, et al. Two independent pathways of maternal cell transmission to offspring: through placenta during pregnancy and by breast-feeding after birth. Immunology. 2000;101(4):570-580.
Campbell DA, Lorber MI, Sweeton JC, Turcotte JG, Niederhuber JE, Beer AE. Breast feeding and maternal-donor renal allografts. Possibly the original donor-specific transfusion. Transplantation. 1984;37(4):340-344.
Hayashida M, Nishimoto Y, Matsuura T, et al. The evidence of maternal microchimerism in biliary atresia using fluorescent in situ hybridization. J Pediatr Surg. 2007;42(12):2097-2101.
Kinder JM, Stelzer IA, Arck PC, Way SS. Immunological implications of pregnancy-induced microchimerism. Nat Rev Immunol. 2017;17(8):483-494.
Malvey EN, Jenkins MK, Mueller DL. Peripheral immune tolerance blocks clonal expansion but fails to prevent the differentiation of Th1 cells. J Immunol. 1998;161(5):2168-2177.
Dutta P, Burlingham WJ. Microchimerism: tolerance vs. sensitization. Curr Opin Organ Transplant. 2011;16(4):359-365.
Nelson JL, Furst DE, Maloney S, et al. Microchimerism and HLA-compatible relationships of pregnancy in scleroderma. Lancet (London, England). 1998;351(9102):559-562.
Kekow M, Barleben M, Drynda S, Jakubiczka S, Kekow J, Brune T. Long-term persistence and effects of fetal microchimerisms on disease onset and status in a cohort of women with rheumatoid arthritis and systemic lupus erythematosus. BMC Musculoskelet Disord. 2013;18(14):325.
Kinder JM, Jiang TT, Ertelt JM, et al. Cross-generational reproductive fitness enforced by microchimeric maternal cells. Cell. 2015;162(3):505-515.
Mold JE, Venkatasubrahmanyam S, Burt TD, et al. Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans. Science. 2010;330(6011):1695-1699.
Kinder JM, Jiang TT, Ertelt JM, et al. Tolerance to noninherited maternal antigens, reproductive microchimerism and regulatory T cell memory: 60 years after ‘Evidence for actively acquired tolerance to Rh antigens’. Chimerism. 2015;6(1-2):8-20.
Suskind DL, Rosenthal P, Heyman MB, et al. Maternal microchimerism in the livers of patients with biliary atresia. BMC Gastroenterol. 2004;4:1-7.
Kobayashi H, Tamatani T, Tamura T, et al. Maternal microchimerism in biliary atresia. J Pediatr Surg. 2007;42(6):987-991.
Muraji T, Hosaka N, Irie N, et al. Maternal microchimerism in underlying pathogenesis of biliary atresia: quantification and phenotypes of maternal cells in the liver. Pediatrics. 2008;121(3):517-521.
Muraji T. Maternal microchimerism in biliary atresia: are maternal cells effector cells, targets, or just bystanders? Chimerism. 2014;5(1):1-5.
Muraji T, Hosaka N, Irie N, et al. Maternal microchimerism in underlying pathogenesis of biliary atresia: quantification and phenotypes of maternal cells in the liver. Pediatrics. 2008;121(3):517-521.
Tzakis AG, Reyes J, Zeevi A, et al. Early tolerance in pediatric liver allograft recipients. J Pediatr Surg. 1994;29(6):754-756.
Hurwitz M, Desai DM, Cox KL, Berquist WE, Esquivel CO, Millan MT. Complete immunosuppressive withdrawal as a uniform approach to post-transplant lymphoproliferative disease in pediatric liver transplantation. Pediatr Transplant. 2004;8(3):267-272.
Lee JH, Lee SK, Lee HJ, et al. Withdrawal of immunosuppression in pediatric liver transplant recipients in Korea. Yonsei Med J. 2009;50(6 PG-784-788):784-788.
Koshiba T, Li Y, Takemura M, et al. Clinical, immunological, and pathological aspects of operational tolerance after pediatric living-donor liver transplantation. Transpl Immunol. 2007;17(2):94-97.
Feng S, Ekong UD, Lobritto SJ, et al. Complete immunosuppression withdrawal and subsequent allograft function among pediatric recipients of parental living donor liver transplants. JAMA. 2012;307(3):283-293.
Feng S, Demetris AJ, Spain KM, et al. Five-year histological and serological follow-up of operationally tolerant pediatric liver transplant recipients enrolled in WISP-R. Hepatology. 2017;65(2):647-660.
Immunosuppression Withdrawal for Stable Pediatric Liver Transplant Recipients (iWITH) [Internet]. https://clinicaltrials.gov/ct2/show/NCT01638559. Accessed January 20, 2019.
Li Y, Koshiba T, Yoshizawa A, et al. Analyses of peripheral blood mononuclear cells in operational tolerance after pediatric living donor liver transplantation. Am J Transplant. 2004;4(12):2118-2125.
Nagaeva O, Jonsson L, Mincheva-Nilsson L. Dominant IL-10 and TGF-beta mRNA expression in gammadeltaT cells of human early pregnancy decidua suggests immunoregulatory potential. Am J Reprod Immunol. 2002;48(1):9-17.
Martínez-Llordella M, Puig-Pey I, Orlando G, et al. Multiparameter immune profiling of operational tolerance in liver transplantation. Am J Transplant. 2007;7(2):309-319.
Carding SR, Egan PJ. γδ T cells: functional plasticity and heterogeneity. Nat Rev Immunol. 2002;2(5):336-345.
Zhao X, Li Y, Ohe H, et al. Intragraft Vδ1 γδ T cells with a unique T-Cell receptor are closely associated with pediatric semiallogeneic liver transplant tolerance. Transplantation. 2013;95(1):192-202.
Polgar B, Barakonyi A, Xynos I, Szekeres-Bartho J. The role of gamma/delta T cell receptor positive cells in pregnancy. Am J Reprod Immunol. 1999;41(4):239-244.
Barakonyi A, Polgar B, Szekeres-Bartho J. The role of gamma/delta T-cell receptor-positive cells in pregnancy: part II. Am J Reprod Immunol. 1999;42(2):83-87.
Schulz-Juergensen S, Marischen L, Wesch D, et al. Markers of operational immune tolerance after pediatric liver transplantation in patients under immunosuppression. Pediatr Transplant. 2013;17(4):348-354.
Kaneku H, O’Leary JG, Banuelos N, et al. De novo donor-specific HLA antibodies decrease patient and graft survival in liver transplant recipients. Am J Transplant. 2013;13(6):1541-1548.
Grabhorn E, Binder T, Obrecht D, et al. Long-term clinical relevance of de novo donor-specific antibodies after pediatric liver transplantation. Transplantation. 2015;99(9):1876-1881.
Lau AH, Vitalone MJ, Haas K, et al. Mass cytometry reveals a distinct immunoprofile of operational tolerance in pediatric liver transplantation. Pediatr Transplant. 2016;20(8):1072-1080.
Morris H, DeWolf S, Robins H, et al. Tracking donor-reactive T cells: Evidence for clonal deletion in tolerant kidney transplant patients. Sci Transl Med. 2015;7(272):272ra10-272ra10.
Zemmour D, Zilionis R, Kiner E, Klein AM, Mathis D, Benoist C. Single-cell gene expression reveals a landscape of regulatory T cell phenotypes shaped by the TCR article. Nat Immunol. 2018;19(3):291-301.
Bradley A, Hashimoto T, Ono M. Elucidating T cell activation-dependent mechanisms for bifurcation of regulatory and effector T cell differentiation by multidimensional and single-cell analysis. Front Immunol. 2018;9:1444.