Concise review: Immunologic lessons from solid organ transplantation for stem cell-based therapies

Stem Cells Translational Medicine

Volumn 2, Issue 2, 2013, Pages 136-142

  Loewendorf, Andrea ^a,b   Csete, Marie ^c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AABB   (United States)

^d University of California   (United States)

Author keywords

Endothelial cell; Immunogenicity; Immunosuppression; NK cells; Stem cell transplantation; Stem cells; T cell; Transplantation

Indexed keywords

B7 ANTIGEN; CD28 ANTIGEN; CD8 ANTIGEN; CD86 ANTIGEN; CD94 ANTIGEN; IMMUNOGLOBULIN G3; IMMUNOLOGIC FACTOR; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 1ALPHA; INTERLEUKIN 4; NATURAL KILLER CELL RECEPTOR NKG2A; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; CELL PROLIFERATION; CLINICAL TRIAL (TOPIC); ENDOTHELIUM CELL; GRAFT REJECTION; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; ISCHEMIA; LIVER GRAFT; LYMPHOID ORGAN; MAJOR HISTOCOMPATIBILITY COMPLEX; NATURAL KILLER CELL; NONHUMAN; ORGAN TRANSPLANTATION; REGULATORY T LYMPHOCYTE; REPERFUSION INJURY; REVIEW; STEM CELL TRANSPLANTATION;

EID: 84876509737     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2012-0125     Document Type: Review

References (108)

1. English K, Wood KJ. Immunogenicity of embryonic stem cell-derived progenitors after transplantation. Curr Opin Organ Transplant 2011;16:90-95.
2. Tang C, Drukker M. Potential barriers to therapeutics utilizing pluripotent cell derivatives: Intrinsic immunogenicity of in vitro maintained and matured populations. Semin Immunopathol 2011;33:563-572.
3. Franquesa M, Hoogduijn MJ, Baan CC. The impact of mesenchymal stem cell therapy in transplant rejection and tolerance. Curr Opin Organ Transplant 2012;17:355-361.
4. Yang XF. Immunology of stem cells and cancer stem cells. Cell Mol Immunol 2007;4: 161-171.
5. Charron D, Suberbielle-Boissel C, Al-Daccak R. Immunogenicity and allogenicity: A challenge of stem cell therapy. J Cardiovasc Transl Res 2009;2:130-138.
6. Karabekian Z, Posnack NG, Sarvazyan N. Immunological barriers to stem-cell based cardiac repair. Stem Cell Rev 2011;7:315-325.
7. Israeli M, Klein T, Brandhorst G et al. Confronting the challenge: Individualized immune monitoring after organ transplantation using the cellular immune function assay. Clin Chim Acta 2012;413:1374-1378.
8. Sawitzki B, Schlickeiser S, Reinke P et al. Monitoring tolerance and rejection in organ transplant recipients. Biomarkers 2011; 16(suppl 1):S42-S50.
9. Llacuna L, Mari M, Lluis JM et al. Reactive oxygen species mediate liver injury through parenchymal nuclear factor-kappaB inactivation in prolonged ischemia/reperfusion. Am J Pathol 2009;174:1776-1785.
10. Hanschen M, Zahler S, Krombach F et al. Reciprocal activation between CD4 T cells and Kupffer cells during hepatic ischemia-reperfusion. Transplantation 2008;86:710-718.
11. Caldwell CC, Tschoep J, Lentsch AB. Lymphocyte function during hepatic ischemia/reperfusion injury. J Leukoc Biol 2007;82:457-464.
12. Zhai Y, Busuttil RW, Kupiec-Weglinski JW. Liver ischemia and reperfusion injury: New insights into mechanisms of innate-adaptive immune-mediated tissue inflammation. Am J Transplant 2011;11:1563-1569.
13. Shen X, Wang Y, Gao F et al. CD4 T cells promote tissue inflammation via CD40 signaling without de novo activation in a murine model of liver ischemia/reperfusion injury. Hepatology 2009;50:1537-1546.
14. Abu-Amara M, Yang SY, Tapuria N et al. Liver ischemia/reperfusion injury: Processes in inflammatory networks-a review. Liver Transpl 2010;16:1016-1032.
15. Zhang X, Majlessi L, Deriaud E et al. Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 2009;31:761-771.
16. Ellett JD, Atkinson C, Evans ZP et al. Murine Kupffer cells are protective in total hepatic ischemia/reperfusion injury with bowel congestion through IL-10. J Immunol 2010;184: 5849-5858.
17. Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010;10:170-181.
18. Coulson MT, Jablonski P, Howden BO et al. Beyond operational tolerance: Effect of ischemic injury on development of chronic damage in renal grafts. Transplantation 2005; 80:353-361.
19. Preynat-Seauve O, de Rham C, Tirefort D et al. Neural progenitors derived from human embryonic stem cells are targeted by allogeneic T and natural killer cells. J Cell Mol Med 2009;13:3556-3569.
20. Cerwenka A, Lanier LL. NKG2D ligands: Unconventional MHC class I-like molecules exploited by viruses and cancer. Tissue Antigens 2003;61:335-343.
21. Yokoyama WM, Plougastel BF. Immune functions encoded by the natural killer gene complex. Nat Rev Immunol 2003;3:304-316.
22. Bottino C, Castriconi R, Moretta L et al. Cellular ligands of activating NK receptors. Trends Immunol 2005;26:221-226.
23. Moretta L, Locatelli F, Pende D et al. Killer Ig-like receptor-mediated control of natural killer cell alloreactivity in haploidentical hematopoietic stem cell transplantation. Blood 2011;117:764-771.
24. Farag SS, Caligiuri MA. Human natural killer cell development and biology. Blood Rev 2006;20:123-137.
25. van der Touw W, Bromberg JS. Natural killer cells and the immune response in solid organ transplantation. Am J Transplant 2010; 10:1354-1358.
26. Kärre K, Ljunggren HG, Piontek G et al. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 1986;319:675-678.
27. Ruggeri L, Aversa F, Martelli MF et al. Allogeneic hematopoietic transplantation and natural killer cell recognition of missing self. Immunol Rev 2006;214:202-218.
28. Lin G, Xie Y, Ouyang Q et al. HLA-matching potential of an established human embryonic stem cell bank in China. Cell Stem Cell 2009;5:461-465.
29. Taylor CJ, Bolton EM, Pocock S et al. Banking on human embryonic stem cells: Estimating the number of donor cell lines needed for HLA matching. Lancet 2005;366:2019-2025.
30. Taylor CJ, Peacock S, Chaudhry AN et al. Generating an iPSC bank for HLA-matched tissue transplantation based on known donor and recipient HLA types. Cell Stem Cell 2012; 11:147-152.
31. Walzer T, Dalod M, Robbins SH et al. Natural-killer cells and dendritic cells: "L'union fait la force." Blood 2005;106:2252-2258.
32. Andrews DM, Andoniou CE, Scalzo AA et al. Cross-talk between dendritic cells and natural killer cells in viral infection. Mol Immunol 2005;42:547-555.
33. Zingoni A, Sornasse T, Cocks BG et al. NK cell regulation of T cell-mediated responses. Mol Immunol 2005;42:451-454.
34. Alter G, Altfeld M. Mutiny or scrutiny: NK cell modulation of DC function in HIV-1 infection. Trends Immunol 2011;32:219-224.
35. Frenzel LP, Abdullah Z, Kriegeskorte AK et al. Role of natural-killer group 2 member D ligands and intercellular adhesion molecule 1 in natural killer cell-mediated lysis of murine embryonic stem cells and embryonic stem cell-derived cardiomyocytes. STEM CELLS 2009; 27:307-316.
36. Stern M, Elsasser H, Honger G et al. The number of activating KIR genes inversely correlates with the rate of CMV infection/reactivation in kidney transplant recipients. Am J Transplant 2008;8:1312-1317.
37. Wilkinson GW, Tomasec P, Stanton RJ et al. Modulation of natural killer cells by human cytomegalovirus. J Clin Virol 2008;41:206-212.
38. McSharry BP, Burgert HG, Owen DP et al. Adenovirus E3/19K promotes evasion of NK cell recognition by intracellular sequestration of the NKG2D ligands major histocompatibility complex class I chain-related proteins A and B. J Virol 2008;82:4585-4594.
39. Jensen H, Andresen L, Nielsen J et al. Vesicular stomatitis virus infection promotes immune evasion by preventing NKG2D-ligand surface expression. PLoS One 2011;6:e23023.
40. Kitchens WH, Uehara S, Chase CM et al. The changing role of natural killer cells in solid organ rejection and tolerance. Transplantation 2006;81:811-817.
41. Ahern AT, Artruc SB, DellaPelle P et al. Hyperacute rejection of HLA-AB-identical renal allografts associated with B lymphocyte and endothelial reactive antibodies. Transplantation 1982;33:103-106.
42. Amico P, Honger G, Bielmann D et al. Incidence and prediction of early antibody-mediated rejection due to non-human leukocyte antigen-antibodies. Transplantation 2008;85: 1557-1563.
43. Grafft CA, Cornell LD, Gloor JM et al. Antibody-mediated rejection following transplantation from an HLA-identical sibling. Nephrol Dial Transplant 2010;25:307-310.
44. Zhang Q, Reed EF. Non-MHC antigenic targets of the humoral immune response in transplantation. Curr Opin Immunol 2010;22: 682-688.
45. Ford WL, Atkins RC. The proportion of lymphocytes capable of recognizing strong transplantation antigens in vivo. Adv Exp Med Biol 1973;29:255-262.
46. Ford WL, Simmonds SJ, Atkins RC. Early cellular events in a systematic graft-vs.-host reaction. II. Autoradiographic estimates of the frequency of donor lymphocytes which respond to each Ag-B-determined antigenic complex. J Exp Med 1975;141:681-696.
47. Matzinger P, Bevan MJ. Hypothesis: Why do so many lymphocytes respond to major his-tocompatibility antigens? Cell Immunol 1977; 29:1-5.
48. Spencer CT, Gilchuk P, Dragovic SM et al. Minor histocompatibility antigens: Presentation principles, recognition logic and the potential for a healing hand. Curr Opin Organ Transplant 2010;15:512-525.
49. Dierselhuis M, Goulmy E. The relevance of minor histocompatibility antigens in solid organ transplantation. Curr Opin Organ Transplant 2009;14:419-425.
50. Dragun D, Hegner B. Non-HLA antibodies post-transplantation: Clinical relevance and treatmet in solid organ transplantation. Contrib Nephrol 2009;162:129-139.
51. D'Orsogna LJ, Roelen DL, Doxiadis II et al. TCR cross-reactivity and allorecognition: New insights into the immunogenetics of allorecognition. Immunogenetics 2012;64:77-85.
52. Koehn B, Gangappa S, Miller JD et al. Patients, pathogens, and protective immunity: The relevance of virus-induced alloreactivity in transplantation. J Immunol 2006;176:2691-2696.
53. Selin LK, Brehm MA, Naumov YN et al. Memory of mice and men: CD8 T-cell cross-reactivity and heterologous immunity. Immunol Rev 2006;211:164-181.
54. Obst R, Netuschil N, Klopfer K et al. The role of peptides in T cell alloreactivity is determined by self-major histocompatibility complex molecules. J Exp Med 2000;191:805-812.
55. Garcia KC, Tallquist MD, Pease LR et al. Alphabeta T cell receptor interactions with syngeneic and allogeneic ligands: Affinity measurements and crystallization. Proc Natl Acad Sci USA 1997;94:13838-13843.
56. Schneck J, Maloy WL, Coligan JE et al. Inhibition of an allospecific T cell hybridoma by soluble class I proteins and peptides: Estimation of the affinity of a T cell receptor for MHC. Cell 1989;56:47-55.
57. Sykulev Y, Brunmark A, Tsomides TJ et al. High-affinity reactions between antigen-specific-T-cell receptors and peptides associated with allogeneic and syngeneic major histocompatibility complex class I proteins. Proc Natl Acad Sci USA 1994;91:11487-11491.
58. Boisgérault F, Liu Y, Anosova N et al. Differential roles of direct and indirect allorecognition pathways in the rejection of skin and corneal transplants. Transplantation 2009;87: 16-23.
59. Brennan TV, Jaigirdar A, Hoang V et al. Preferential priming of alloreactive T cells with indirect reactivity. Am J Transplant 2009;9: 709-718.
60. Alonso Arias R, Lopex-Vazquez A, Lopez-Larrea C. Immunology and the challenge of transplantation. Adv Exp Med Biol 2012;741: 27-43.
61. Afzali B, Lombardi G, Lechler RI. Pathways of major histocompatibility complex allorecognition. Curr Opin Organ Transplant 2008;13:438-444.
62. Game DS, Lechler RI. Pathways of allorecognition: Implications for transplantation tolerance. Transpl Immunol 2002;10:101-108.
63. Epperson DE, Pober JS. Antigen-presenting function of human endothelial cells: Direct activation of resting CD8 T cells. J Immunol 1994;153:5402-5412.
64. Kreisel D, Krupnick AS, Gelman AE et al. Non-hematopoietic allograft cells directly activate CD8 T cells and trigger acute rejection: An alternative mechanism of allorecognition. Nat Med 2002;8:233-239.
65. Taflin C, Charron D, Glotz D et al. Regulation of the CD4()Tcellallo-immuneresponse by endothelial cells. Hum Immunol 2012;73: 1269-1274.
66. Taflin C, Charron D, Glotz D et al. Immunological function of the endothelial cell within the setting of organ transplantation. Immunol Lett 2011;139:1-6.
67. Rodig N, Ryan T, Allen JA et al. Endothelial expression of PD-L1 and PD-L2 down-regulates CD8 T cell activation and cytolysis. Eur J Immunol 2003;33:3117-3126.
68. Mazanet MM, Hughes CC. B7-H1 is expressed by human endothelial cells and suppresses T cell cytokine synthesis. J Immunol 2002;169:3581-3588.
69. Vos IH, Briscoe DM. Endothelial injury: Cause and effect of alloimmune inflammation. Transpl Infect Dis 2002;4:152-159.
70. Naemi FM, Ali S, Kirby JA. Antibody-mediated allograft rejection: The emerging role of endothelial cell signaling and transcription factors. Transpl Immunol 2011;25:96-103.
71. Ochando JC, Homma C, Yang Y et al. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat Immunol 2006;7:652-662.
72. Lakkis FG, Arakelov A, Konieczny BT et al. Immunologic 'ignorance' of vascularized organ transplants in the absence of secondary lymphoid tissue. Nat Med 2000;6:686-688.
73. Obhrai JS, Oberbarnscheidt M, Zhang N et al. Langerhans cells are not required for efficient skin graft rejection. J Invest Dermatol 2008;128:1950-1955.
74. Sumpter TL, Lunz JG 3rd, Demetris AJ et al. Molecular regulation of hepatic dendritic cell function and its relation to liver transplant outcome. Transplantation 2009;88:S40-S44.
75. Baddoura FK, Nasr IW, Wrobel B et al. Lymphoid neogenesis in murine cardiac allografts undergoing chronic rejection. Am J Transplant 2005;5:510-518.
76. Thaunat O, Nicoletti A. Lymphoid neogenesis in chronic rejection. Curr Opin Organ Transplant 2008;13:16-19.
77. Motallebzadeh R, Bolton EM, Pettigrew GL. Lymphoid tissue formation in allografts: Innocent until proven guilty. Transplantation 2008;85:309-311.
78. Wojciechowski D, Vincenti F. Challenges and opportunities in targeting the costimulation pathway in solid organ transplantation. Semin Immunol 2011;23:157-164.
79. Croft M. The role of TNF superfamily members in T-cell function and diseases. Nat Rev Immunol 2009;9:271-284.
80. Bour-Jordan H, Esensten JH, Martinez-Llordella M et al. Intrinsic and extrinsic control of peripheral T-cell tolerance by costimulatory molecules of the CD28/B7 family. Immunol Rev 2011;241:180-205.
81. Jenkins MK, Schwartz RH. Antigen presentation by chemically modified splenocytes induces antigen-specific T cell unresponsiveness in vitro and in vivo. J Exp Med 1987;165: 302-319.
82. Newell KA, He G, Guo Z et al. Cutting edge: Blockade of the CD28/B7 costimulatory pathway inhibits intestinal allograft rejection mediated by CD4 but not CD8 T cells. J Immunol 1999;163:2358-2362.
83. Farber DL. Biochemical signaling pathways for memory T cells. Semin Immunol 2009; 21:84-91.
84. Hakim FT, Gress RE. Immunosenescence: Deficits in adaptive immunity in the elderly. Tissue Antigens 2007;70:179-189.
85. Goronzy JJ, Weyand CM. Immune aging and autoimmunity. Cell Mol Life Sci 2012;69: 1615-1623.
86. Alegre M, Fallarino F, Zhou P et al. Transplantation and the CD28/CTLA/B7 pathway. Transplant Proc 2001;33:209-211.
87. Lo DJ, Weaver TA, Stempora L et al. Selective targeting of human alloresponsive CD8 effector memory T cells based on CD2 expression. Am J Transplant 2011;11:22-33.
88. Taylor DK, Neujahr D, Turka LA. Heterologous immunity and homeostatic proliferation as barriers to tolerance. Curr Opin Immunol 2004;16:558-564.
89. Williams KM, Hakim FT, Gress RE. T cell immune reconstitution following lymphodepletion. Semin Immunol 2007;19:318-330.
90. Tchao NK, Turka LA. Lymphodepletion and homeostatic proliferation: Implications for transplantation. Am J Transplant 2012;12: 1079-1090.
91. Wu Z, Bensinger SJ, Zhang J et al. Homeostatic proliferation is a barrier to transplantation tolerance. Nat Med 2004;10:87-92.
92. Smith JD, Banner NR, Hamour IM et al. De novo donor HLA-specific antibodies after heart transplantation are an independent predictor of poor patient survival. Am J Transplant 2011;11:312-319.
93. Berry G. Antibody-mediated rejection of the cardiac allograft: Where do we stand in 2012? Curr Opin Organ Transplant 2012;17: 303-308.
94. Lee PC, Zhu L, Terasaki PI et al. HLA-specific antibodies developed in the first year posttransplant are predictive of chronic rejection and renal graft loss. Transplantation 2009; 88:568-574.
95. Herzenberg AM, Gill JS, Djurdjev O, Magil AB. C4d deposition in acute rejection: An independent long-term prognostic factor. J Am Soc Nephrol 2002;13:234-241.
96. Loupy A, Hill GS, Jordan SC. The impact of donor-specific anti-HLA antibodies on late kidney allograft failure. Nat Rev Nephrol 2012;8: 348-357.
97. Hidalgo LG, Campbell PM, Sis B et al. De novo donor-specific antibody at the time of kidney transplant biopsy associates with microvascular pathology and late graft failure. Am J Transplant 2009;9:2532-2541.
98. Bolton EM, Bradley JA, Pettigrew GJ. Indirect allorecognition: Not simple but effective. Transplantation 2008;85:667-669.
99. Thaunat O, Patey N, Gautreau C et al. B cell survival in intragraft tertiary lymphoid organs after rituximab therapy. Transplantation 2008;85:1648-1653.
100. Pons JA, Revilla-Nuin B, Baroja-Mazo A et al. FoxP3 in peripheral blood is associated with operational tolerance in liver transplant patients during immunosuppressive with-drawal. Transplantation 2008;86:1370-1378.
101. 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;4:2116-2125.
102. Martínez-Llordella M, Puig-Pey I, Orlando G et al. Multiparameter immune profiling of operational tolerance in liver transplantation. Am J Transplant 2007;7:309-319.
103. Brouard S, Mansfield E, Braud C et al. Identification of a peripheral blood transcriptional biomarker panel associated with operational renal allograft tolerance. Proc Natl Acad Sci USA 2007;104:15448-15453.
104. Louis S, Braudeau C, Giral M et al. Contrasting CD25hiCD4 T cells/FOXP3 patterns in chronic rejection and operational drug-free tolerance. Transplantation 2006;81:398-407.
105. Wood KJ, Bushell A, Hester J. Regulatory immune cells in transplantation. Nat Rev Immunol 2012;12:417-430.
106. Newell KA, Phippard D, Turka LA. Regulatory cells and cell signatures in clinical transplantation tolerance. Curr Opin Immunol 2011; 23:655-659.
107. Hippen KL, Riley JL, June CH et al. Clinical perspectives for regulatory T cells in transplantation tolerance. Semin Immunol 2011;23: 462-468.
108. Tang Q, Bluestone JA, Kang SM. CD4(+)Foxp3(+) regulatory T cell therapy in transplantation. J Mol Cell Biol 2012;4:11-21.