Non-inherited maternal antigens, pregnancy, and allotolerance

Biomedical Journal

Volumn 38, Issue 1, 2015, Pages 39-51

  Bracamonte Baran, William ^a,b   Burlingham, William ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSIDAD CENTRAL DE VENEZUELA   (Venezuela)

Author keywords

microchimerism; non inherited maternal antigens; tolerance; Tregs

Indexed keywords

ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 35; NON INHERITED MATERNAL ANTIGEN; NON INHERTITED PATERNAL ANTIGEN; PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

CELL TRANSPORT; DECIDUA; GENE EXPRESSION; HUMAN; IMMUNE SYSTEM; IMMUNOLOGICAL TOLERANCE; MICROCHIMERISM; MOLECULAR RECOGNITION; MOTHER; NONHUMAN; PERIPHERAL LYMPHOCYTE; PREGNANCY; PROGENY; REGULATORY T LYMPHOCYTE; REVIEW; TROPHOBLAST; ANIMAL; CHIMERA; CYTOLOGY; EMBRYOLOGY; ENVIRONMENTAL EXPOSURE; FEMALE; IMMUNOLOGY;

ANIMALS; ANTIGENS; CHIMERISM; FEMALE; HUMANS; IMMUNE TOLERANCE; MATERNAL EXPOSURE; PREGNANCY; T-LYMPHOCYTES, REGULATORY;

EID: 84923364237     PISSN: 23194170     EISSN: None     Source Type: Journal    
DOI: 10.4103/2319-4170.143498     Document Type: Review

References (82)

1. Burt TD. Fetal regulatory T cells and peripheral immune tolerance in utero: Implications for development and disease. Am J Reprod Immunol 2013;69:346-58
2. Burlingham WJ, Benichou G. Bidirectional alloreactivity: A proposed microchimerism-based solution to the NIMA paradox. Chimerism 2012;3:29-36
3. Van Rood JJ, Class F. Both self and non-inherited maternal HLA antigens influence the immune response. Immunol Today 2000;21:269-73
4. Abbas A, Lichtman A, Pillai S. Cellular and molecular immunology. 6th ed. Philadelphia: Saunders-Elsevier; 2010
5. Araki M, Hirayama M, Azuma E, Kumamoto T, Iwamoto S, Toyoda H, et al. Prediction of reactivity to noninherited maternal antigen in MHC-mismatched, minor histocompatibility antigen-matched stem cell transplantation in a mouse model. J Immunol 2010;185:7739-45
6. Hirayama M, Azuma E, Komada Y. Tolerogenic effect of non-inherited maternal antigens in hematopoietic stem cell transplantation. Front Immunol 2012;3:135
7. Van Rood JJ, Scaradavou A, Stevens CE. Indirect evidence that maternal microchimerism in cord blood mediates a graft-versus-leukemia effect in cord blood transplantation. Proc Natl Acad Sci USA 2012;109:2509-14
8. Dutta P, Burlingham WJ. Microchimerism: Tolerance vs. sensitization. Curr Opin Organ Transplant 2011;16:359-65
9. Dutta P, Burlingham WJ. Correlation between post transplant maternal microchimerism and tolerance across MHC barriers in mice. Chimerism 2011;2:78-83
10. Revillard JP. Immunological aspects of interactions between mother and foetus. Bull Cancer 1979;66115-25
11. Dutta P, Burlingham W. Tolerance to non-inherited maternal antigens in mice and humans. Curr Opin Organ Transplant 2009;14:439-47
12. Claas FH, Gijbels Y, Van Der Velden-de Muck J, Van Rood JJ. Induction of B cell unresponsiveness to noninherited maternal HLA antigens during fetal life. Science 1988;241:1815-7
13. Dausset J, Brecy H. Identical nature of leucocyte antigens detectable in monozygotic twins by means of immune iso-leuco-Agglutinins. Nature 1957;180:1430
14. Yin L, Scott-Browne J, Kappler JW, Gapin L, Marrack P. T cells and their eons-old obsession with MHC. Immunol Rev 2012;250:49-60
15. Morris G, Ni P, Allen P. Alloreactivity is limited by the endogenous peptide repertoire. Proc Natl Acad Sci USA 2011;108:3695-700
16. DOrsogna LJ, Nguyen TH, Claas FH, Witt C, Mifsud NA. Endogenous-peptide-dependent alloreactivity: New scientific insights and clinical implications. Tissue Antigens 2013;81:399-407
17. Hornick P, Lechler R. Direct and indirect pathways of alloantigen recognition: Relevance to acute and chronic allograft rejection. Nephrol Dial Transplant 1997;12:1806-10
18. Benichou G. Direct and indirect antigen recognition: The pathways to allograft immune rejection. Front Biosci 1999;4:D476-80
19. Brennan TV, Hoang V, Garrod KR, Liu FC, Hayden T, Kim J, et al. A new T-cell receptor transgenic model of the CD4+direct pathway: Level of priming determines acute versus chronic rejection. Transplantation 2008;85:247-55
20. Wilkes D, Burlingham W, editors. Immunobiology of Organ Transplantation. 1st ed. Springer; 2004
21. Afzali B, Lombardi G, Lechler R. Pathways of major histocompatibility complex allorecognition. Curr Opin Organ Transplant 2008;13:438-44
22. Herrera OB, Golshayan D, Tibbott R, Ochoa F, James MJ, Marelli-Berq FM, et al. A novel pathway of alloantigen presentation by dendritic cells. J Immunol 2004;173:4828-37
23. Smyth LA, Herrera OB, Golshayan D, Lombardi G, Lechler RI. A novel pathway of antigen presentation by dendritic and endothelial cells: Implications for allorecognition in infectious diseases. Transplantation 2006;82 (1 Suppl):S15-8
24. Morelli AE. Dendritic cells of myeloid lineage: The masterminds behind acute allograft rejection. Curr Opin Organ Transplant 2014;19:20-7
25. Bracamonte-Baran, Zhou Y, Brennan T, Burlingham W. Is semi-direct pathway the missing link between microchimerism and tolerance?. Abstract #587, to be presented at World Transplant Congress 2014
26. Mold JE, Michaelson J, Burt TD, Muench MO, Beckerman KP, Busch MP, et al. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 2008;322:1562-5
27. Leveque L, Hodgson S, Peyton S, Koyama M, MacDonald KP, Khosrotehrani K. Selective organ specific inflammation in offspring harbouring microchimerism from strongly allreactive mothers. J Autoimmun 2014;50:51-8
28. Arck PC, Hecher K. Fetomaternal immune cross-talk and its consequences for maternal and offspring's health. Nat Med 2013;19:548-56
29. Van Halteren AG, Jankowska-Gan E, Joosten A, Blokland E, Pool J, Brand A, et al. Naturally acquired tolerance and sensitization to minor histocompatibility antigens in healthy family members. Blood 2009;114:2263-72
30. Dierselhuis MP, Jankowska-Gan E, Blokland E, Pool J, Burlingham WJ, Van Halteren AG, et al. HY Immune tolerance is common in women without male offspring. PLoS One 2014;9:e91274
31. Starzl TE, Demetris AJ, Trucco M, Ramos H, Zeevi A, Rudert WA, et al. Systemic chimerism in human female recipients of male livers. Lancet 1992;340:876-7
32. Moffett A, Loke C. Immunology of placentation in eutherian mammals. Nat Rev Immunol 2006;6:584-94
33. IFPA Meeting 2010 Workshop Repor I. Placenta 2011:32(Suppl 2):S81-9
34. Elliot MG, Crespi BJ. Placental invasiveness mediates the evolution of hybrid inviability in mammals. Am Nat 2006;168:114-20
35. Owen RD. Immunogenetic consequences of vascular anastomoses between bovine twins. Science 1945;102:400-1
36. Burlingham WJ. Chimerism, Tolerance and Twins. Obstet Gynecol 2010;116 Suppl 2:475-6
37. Dutta P, Dart M, Roenneburg DA, Torrealba JR, Burlingham WJ. Pretransplant immune-regulation predicts allograft tolerance. Am J Transplant 2011;11:1296-301
38. Dutta P, Burlingham WJ. Stem cell microchimerism and tolerance to non-inherited maternal antigens. Chimerism 2010;1:2-10
39. Campbell DA Jr, 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;37:340-4
40. Molitor-Dart M, Andrassy J, Haynes L, Burlingham W. Tolerance induction or sensitization in mice exposed to noninherited maternal antigens (NIMA). Am J Transplant 2008;8:2307-15
41. Mazzini E, Massimiliano L, Penna G, Rescigno M. Oral tolerance can be established via Gap junction transfer of fed antigens from C3CR1+macrophages to CD103+dendritic cells. Immunity 2014;40:248-61
42. Burlingham WJ, Grailer AP, Fechner JH Jr, Kusaka S, Trucco M, Kocova M, et al. Microchimerism linked to cytotoxic T lymphocyte functional unresponsiveness (clonal anergy) in a tolerant renal transplant recipient. Transplantation 1995;59:1147-55
43. Andrassy J, Kusaka S, Jankowska-Gan E, Torrealba JR, Haynes LD, Marthaler BR, et al. Tolerance to noninherited maternal MHC antigens in mice. J Immunol 2003;171:5554-61
44. Dutta P, Molitor-Dart M, Bobadilla JL, Roenneburg DA, Yan Z, Torrealba JR, et al. Microchimerism is strongly correlated with tolerance to noninherited maternal antigens in mice. Blood 2009;114:3578-87
45. Burlingham WJ, Grailer AP, Heisy DM, Class FH, Norman D, Mohanakumar T, 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;339:1657-64
46. Van Rood JJ, Loberiza FR Jr, Zhang MJ, Oudshoorn M, Claas F, Cairo MS, et al. Effect of tolerance to noninherited maternal antigens on the occurrence of graft-versus-host disease after bone marrow transplantation from a parent or a HLA-haploidentical sibling. Blood 2002;99:1572-7
47. Stern M, Ruggeri L, Mancusi A, Bernardo ME, Angelis C, Bucher C, et al. Survival after T cell-depleted haploidentical stem cell transplantation is improved using mother as donor. Blood 2008;112:2990-5
48. Owen RD, Wood HR, Foord AG, Sturgeon P, Baldwin LG. Evidence for actively acquired tolerance to Rh antigens. Proc Natl Acad Sci USA 1954;40:420-4
49. Claas FH, Gijbels Y, Van Der Velden-de Muck J, Van Rood JJ. Induction of B cell unresponsiveness to noninherited maternal HLA antigens during fetal life. Science 1988;241:1815-7
50. Zhang L, Van Rood JJ, Claas FH. The T-cell repertoire is not dictated by self antigens alone. Res Immunol 1991;142:441-5
51. Moretta A, Locatelli F, Mingrat G, Rondini G, Montagna D, Comoli P, et al. Characterisation of CTL directed towards non-inherited maternal alloantigens in human cord blood. Bone Marrow Transplant 1999;24:1161-6
52. Akiyama Y, Caucheteux SM, Vernochet C, Iwamoto Y, Tanaka K, Kanellopoulos-Langevin C, et al. Transplantation tolerance to a single noninherited MHC class I maternal alloantigen studied in a TCR-transgenic mouse model. J Immunol 2011;186:1442-9
53. Hadley GA, Phelan D, Duffy BF, Mohanakumar T. Lack of T-cell tolerance of noninherited maternal HLA antigens in normal humans. Hum Immunol 1990;28:373-81
54. Roelen DL, Van Bree FP, Van Beelen E, Van Rood JJ, Claas FH. No evidence of influence of the noninherited maternal HLA antigens on the alloreactive T cell repertoire in healthy individuals. Transplantation 1995;59:1728-33
55. Jankowska-Gan E, Sheka A, Sollinger HW, Pirsch JD, Hofmann RM, Haynes LD, et al. Pretransplant immune regulation predicts allograft outcome: Bidirectional regulation correlates with excellent renal transplant function in living-related donor-recipient pairs. Transplantation 2012;93:283-90
56. Al-Adra DP, Anderson CC. Mixed chimerism and split tolerance: Mechanisms and clinical correlations. Chimerism 2011;2:89-101
57. Zhang L, Miller RG. The correlation of prolonged survival of maternal skin grafts with the presence of naturally transferred maternal T cells. Transplantation 1993;56:918-21
58. Molitor-Dart ML, Andrassy J, Haynes LD, Burlingham WJ. Tolerance induction or sensitization in mice exposed to non-inherited maternal antigens (NIMA). Am J Transplant 2008;8:2307-15
59. Abbas AK, Benoist C, Bluestone JA, Campbell DJ, Ghosh S, Hori S, et al. Regulatory T cells: Recommendations to simplifly nomenclature. Nat Immunol 2013;14:307-8
60. Molitor-Dart ML, Andrassy J, Kwun J, Kayaoqlu HA, Roennburg DA, Haynes LD, et al. Developmental exposure to noninherited maternal antigens induces CD4+T regulatory cells: Relevance to mechanism of heart allograft tolerance. J Immunol 2007;179:6749-61
61. Burlingham W, Jankowska-Gan E, Kempton S, Kaufman D, Haynes L. Doeminant role of IL-35 in naturally acquired immune regulation in Rhesus macaque and human families. Abstract to be presented at World Transplant Congress 2014
62. Xu L, Kitani A, Fuss I, Strober W. Cutting edge: Regulatory R cells induce CD4+CD25-FoxP3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J Immunol 2007;178:6725-9
63. Sewell H. HLA and disease. Non-inherited maternal HLA antigens. Lancet 1993;341:211
64. Ten Wolde S, Breedveld FC, De Vries RR, DAmaro J, Rubestein P, Schreuder GM, et al. Influence of non-inherited maternal HLA antigens on ocurrence of rheumatoid arthritis. Lancet 1993;341:200-2
65. Guthrie KA, Tishkevich NR, Lee Nelson JL. Non inherited maternal HLA antigens in susceptibility to familial rheumatoid arthritis. Ann Rheum Dis 2009;68:107-9
66. Feitsma AL, Van Der Helm-van Mil AH, Huizinga TW, De Vries RR, Toes RE. Protection against rheumatoid arthritis and nurture. Ann Rheum Dis 2008;67 Suppl 3:iii61-3
67. Nijagal A, Fleck S, MacKenzie TC. Maternal microchimerism in patients with biliary atresia. Implications for allograft tolerance. Chimerism 2012;3:37-9
68. Nijagal A, Fleck S, Hills NK, Feng S, Tang Q, Kang SM, et al. Decreased risk of graft failure with maternal liver transplantation in patients with biliary atresia. Am J Transplant 2012;12:409-19
69. Samstein RM, Josefowicz SZ, Arvey A, Treuting PM, Rudensky AY. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 2012;150:29-38
70. Rowe JH, Ertelt JM, Xin L, Way SS. Pregnancy imprints regulatory memory that sustains anergy to fetal antigen. Nature 2012;490:102-6
71. Santner-Nanan B, Peek MJ, Khanam R, Richarts L, Zhu E, Fazekas De St Groth B, et al. Systemic increase in the ratio between Foxp3+and IL-17 producing CD4+T cells in healthy pregnancy but not in preeclampsia. J Immunol 2009;183:7023-30
72. Dutta P, Dart ML, Schumacher SM, Burlingham WJ. Fetal microchimerism persists at high levels in c-kit+stem cells in sensitized mothers. Chimerism 2010;1:51-5
73. Mold JE, Venkatasubrahmanyam S, Burt TD, Michaelsson J, Rivera JM, Galkina SA, et al. Fetal and adult hematopoietic stem cells give rise to distinct T cell leineages in humans. Science 2010;330:1695-9
74. Mold JE, McCune JM. At the crossroads between tolerance and aggression. Revisiting the layered immune system hypothesis. Chimerism 2011;2:35-41
75. Dierselhuis MP, Blokland EC, Pool J, Schrama E, Scherjon SA, Goulmy E. Transmaternal cell flow leads to antigen-experienced cord blood. Blood 2012;120:505-10
76. Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL, et al. Endometrial exosomes/microvesicles in the uterine microenviroment: A new paradigm for embryo-endometrial cross talk at implantation. PLoS One 2013;8:e58502
77. Raposo G, Stoorvogel W. Extracellular vesicles: Exosomes, microvesicles and friends. J Cell Biol 2013;200:373-83
78. De Candia P, Torri A, Pagani M, Abrignani S. Serum microRNAs as biomarkers of human lymphocyte activation in health and disease. Front Immunol 2014;5:43
79. Montecalvo A, Larregina AT, Morelli AE. Methods of analysis of dendritic cell-derived exosomes-shuttle microRNA and its horizontal propagation between dendritic cells. Methods Mol Biol 2013;1024:19-40
80. Breman E, Van Miert PP, Van Der Steen DM, Heemskerk MH, Doxiadis II, Roelen D, et al. HLA monomers as a tool to monitor indirect allorecognition. Transplantation 2014;97:1119-27
81. Kusaka S, Grailer AP, Fechner JH Jr, Jankowska-Gan E, Oberley T, Sollinger HW, et al. Clonotype analysis of human alloreactive T cells: A novel approach to studying peripheral tolerance in a transplant patient. J Immunol 2000;164:2240-7
82. Burlingham WJ, Jankowska-Gan E, VanBuskirk A, Orosz CG, Lee JH, Kusaka S. Loss of tolerance to a maternal kidney transplant is selective for HLA class II: Evidence from trans-vivo DTH and alloantibody analysis. Hum Immunol 2000;61:1396-402