Tolerogenic effect of non-inherited maternal antigens in hematopoietic stem cell transplantation

Frontiers in Immunology

Volumn 3, Issue MAY, 2012, Pages

  Hirayama, Masahiro ^a   Azuma, Eiichi ^a   Komada, Yoshihiro ^a  

^a MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Acute GVHD; Hematopoietic stem cell transplantation; NIMA; Tolerance

Indexed keywords

EID: 84874203838     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00135     Document Type: Article

References (51)

1. Akatsuka, Y., Nishida, T., Kondo, E., Miyazaki, M., Taji, H., Iida, H., Tsu-jimura, K., Yazaki, M., Naoe, T., Mor-ishima, Y., Kodera, Y., Kuzushima, K., and Takahashi, T. (2003).Identification of a polymorphicgene, BCL2A1, encoding two novel hematopoietic lineage-specific minor histo compatibility antigens. J. Exp.Med. 197, 1489-1500.
2. Andrassy, J., Kusaka, S., Jankowska-Gan, E., Torrealba, J.R., Haynes, L.D., Marthaler, B.R., Tam, R.C., Illigens, B.M., Anosova, N., Benichou, G., and Burlingham, W.J.(2003).Toler-ancetononinheritedmaternalMHC antigens inmice. J. Immunol. 171, 5554-5561.
3. Aoyama, K., Koyama, M., Matsuoka, K., Hashimoto, D., Ichinohe, T., Harada, M., Akashi, K., Tanimoto, M.,and Teshima, T.(2009).Improvedout-comeofallogeneicbonemarrow transplantationduetobreastfeeding-inducedtolerancetomaternalanti-gens. Blood 113, 1829-1833.
4. Araki, M., Hirayama, M., Azuma, E., Kumamoto, T., Iwamoto, S., Toyoda, H., Ito, M., Amano, K.,and Komada, Y.(2010).Predictionofreactivity to noninherited maternal antigen in MHC-mismatched, minor histocompatibility antigen-matched stemcell transplantation in a mouse model. J. Immunol. 185, 7739-7745. Beatty, P.G., Anasetti, C., Hansen, J.
5. A., Longton, G.M., Sanders, J.E., Martin, P.J., Mickelson, E.M., Choo, S. Y., Petersdorf, E.W., Pepe, M.S., Appelbaum, F.R., Bearman, S.I., Buckner, C.D., Clift, R.A., Petersen, F.B., Singer, J., Stewart, P.S., Storb, R. F., Sullivan, K.M., Tesler, M. C., Witherspoon, R.P.,and Thomas, E.D.(1993). Marrow transplantation from unrelated donors for treatment of hematologic malignancies:effect of mismatching for one HLA locus. Blood 81, 249-253.
6. Bemelman, F., Honey, K., Adams, E., Cobbold, S.,and Waldmann, H. (1998). Bone marrow transplantation induces either clonaldeletionor infectious tolerancedependingonthe dose. J. Immunol. 160, 2645-2648.
7. Billingham, R.E., Brent, L.,and Medawar, P.B.(1953).Actively acquired tolerance of foreign cells. Nature 172, 603-606.
8. Bonilla, W. V., Geuking, M. B., Aichele, P., Ludewig, B., Hengartner, H., and Zinkernagel, R. M. (2006). Microchimerism maintains deletion of the donor cell-specific CD8+ T cell repertoire. J. Clin. Invest. 116, 156-162.
9. Burlingham, W. J., Grailer, A. P., Heisey, D. M., Claas, F. H., Norman, D., Mohanakumar, T., Brennan, D. C., de Fijter, H., van Gelder, T., Pirsch, J. D., Sollinger, H. W., and Bean, M. A. (1998). The effect of tolerance to noninherited maternal HLA antigens on the survival of renal transplants from sibling donors. N. Engl. J. Med. 339, 1657-1664.
10. Choi, E. Y., Christianson, G. J., Yoshimura, Y., Jung, N., Sproule, T. J., Malarkannan, S., Joyce, S., and Roopenian, D. C. (2002). Realtime T-cell profiling identifies H60 as a major minor histocompatibility antigen in murine graft-versus-host disease. Blood 100, 4259-4265.
11. Choi, E.Y., Yoshimura, Y., Christianson, G. J., Sproule, T. J., Malarkannan, S., Shastri, N., Joyce, S., and Roopenian, D. C. (2001). Quantitative analysis of the immune response to mouse non-MHC transplantation antigens in vivo: the H60 histocompatibility antigen dominates over all others. J. Immunol. 166,4370-4379.
12. Claas, F. H., Gijbels, Y., van der Veldende Munck, J., and van Rood, J. J. (1988). Induction of B cell unresponsiveness to noninherited maternal HLA antigens during fetal life. Science 241,1815-1817.
13. de Rijke, B., van Horssen-Zoetbrood, A., Beekman, J. M., Otterud, B., Maas, F., Woestenenk, R., Kester, M., Leppert, M., Schattenberg, A. V., de Witte, T., van de Wielvan Kemenade, E., and Dolstra, H. (2005). A frameshift polymorphism inP2X5elicitsanallogeneiccytotoxic T lymphocyte response associated with remission of chronic myeloid leukemia. J. Clin. Invest. 115, 35063516.
14. Eden, P. A., Christianson, G. J., Fontaine, P., Wettstein, P. J., Perreault, C., and Roopenian, D. C. (1999). Biochemical and immunogenetic analysis of an immunodominant peptide (B6dom1) encoded by the classical H7 minor histocompatibility locus. J. Immunol. 162, 45024510.
15. Falkenburg, J. H., van Luxemburg-Heijs, S. A., Lim, F. T., Kanhai, H. H., and Willemze, R. (1996). Umbilical cord blood contains normal frequencies of cytotoxic T-lymphocyte precursors (ctlp) and helper T-lymphocyte precursors against noninherited maternal antigens and noninherited paternal antigens. Ann. Hematol. 72, 260-264.
16. Gonnella, P. A., Kodali, D., and Weiner, H. L. (2003). Induction of low dose oral tolerance in monocyte chemoattractant protein-1and CCR2-deficient mice. J. Immunol. 170,2316-2322.
17. Hirayama, M., and Azuma, E. (2011). Major and minor histocompatibility antigens to NIMA: prediction of a tolerogenic NIMA effect. Chimerism 2,23-24.
18. Ichinohe, T., Maruya, E., and Saji, H. (2002). Long-term feto-maternal microchimerism: natures hidden clueforalternativedonorhematopoieticcelltransplantationInt.J.Hematol. 76,229-237.
19. Ichinohe, T., Uchiyama, T., Shimazaki, C., Matsuo, K., Tamaki, S., Hino, M., Watanabe, A., Hamaguchi, M., Adachi, S., Gondo, H., Uoshima, N., Yoshihara, T., Hatanaka, K., Fujii, H., Kawa, K., Kawanishi, K., Oka, K., Kimura, H., Itoh, M., Inukai, T., Maruya, E., Saji, H., Kodera, Y., (2004) and Japanese Collaborative Study Group for NIMA-Complementary Haploidentical Stem Cell Transplantation Feasibility of HLA-haploidentical hematopoietic stem cell transplantation between noninherited maternal antigen (NIMA)-mismatched family members linked with long-term fetomaternal microchimerism. Blood 104,3821-3828.
20. Kanda, J., Ichinohe, T., Shimazaki, C., Hamaguchi, M., Watanabe, A., Ishida, H., Yoshihara, T., Morimoto, A., Uoshima, N., Adachi, S., Inukai, T., Sawada, A., Oka, K., Itoh, M., Hino, M., Maruya, E., Saji, H., Uchiyama, T., and Kodera, Y. (2009). Long-term survival after HLA-haploidentical SCT fromnoninheritedmaternalantigenmismatchedfamilydonors:impactof chronic GVHD. Bone Marrow Transplant. 44,327-329.
21. Kircher, B., Niederwieser, D., Gächter, A., Lätzer, K., Eibl, G., Gastl, G., and Nachbaur, D. (2004). No predictive value of cytotoxic or helper T-cell precursor frequencies for outcome when analyzed from the graft after stem cell transplantation. Ann. Hematol. 83, 566-572.
22. Ko, S., Deiwick, A., Jäger, M. D., Dinkel, A., Rohde, F., Fischer, R., Tsui, T. Y., Rittmann, K. L., Wonigeit, K., and Schlitt, H. J. (1999). The functional relevanceofpassengerleukocytesand microchimerism for heart allograft acceptance in the rat. Nat. Med. 5, 1292-1297.
23. Kodera, Y., Nishida, T., Ichinohe, T., andSaji, H.(2005).Humanleukocyte antigenhaploidenticalhematopoietic stem cell transplantation: indications and tentative outcomes in Japan. Semin. Hematol. 42,112-118.
24. Levitsky, J., Miller, J., Leventhal, J., Huang, X., Flaa, C., Wang, E., Tambur, A., Burt, R. K., Gallon, L., and Mathew, J. M. (2009). The human "Treg MLR": immune monitoring for FOXP3+ T regulatory cell generation. Transplantation 88, 1303-1311.
25. Lo, Y. M., Lo, E. S., Watson, N., Noakes, L., Sargent, I. L., Thilaganathan, B., and Wainscoat, J. S. (1996). Twoway cell traffic between mother and fetus: biologic and clinical implications. Blood 88,4390-4395.
26. Malarkannan, S., Horng, T., Eden, P., Gonzalez, F., Shih, P., Brouwenstijn, N., Klinge, H., Christianson, G., Roopenian, D., and Shastri, N. (2000). Differences that matter: major cytotoxic T cell-stimulating minor histocompatibility antigens. Immunity 13, 333-344.
27. Maloney, S., Smith, A., Furst, D. E., Myerson, D., Rupert, K., Evans, P. C., and Nelson, J. L. (1999). Microchimerism of maternal origin persists into adult life. J. Clin. Invest. 104,41-47.
28. Mendoza, L. M., Paz, P., Zuberi, A., Christianson, G., Roopenian, D., and Shastri, N. (1997). Minors held by majors:the H13 minor his to compatibility locus defined as a peptide/MHC class I complex. Immunity 7, 461-472.
29. Mold, J. E., Michaëlsson, J., Burt, T. D., Muench, M. O., Beckerman, K. P., Busch, M. P., Lee, T. H., Nixon, D. F., and McCune, J. M. (2008). Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322, 1562-1565.
30. Molitor, M. L., Haynes, L. D., Jankowska-Gan, E., Mulder, A., and Burlingham, W. J. (2004). HLA class I noninherited maternal antigens in cord blood and breast milk. Hum. Immunol. 65, 231-239.
31. Molitor-Dart, M. L., Andrassy, J., Haynes, L. D., and Burlingham, W. J. (2008). Tolerance induction or sensitizationinmiceexposedtononinherited maternal antigens (NIMA). Am. J. Transplant. 8,2307-2315.
32. Moretta, A., Locatelli, F., Mingrat, G., Rondini, G., Montagna, D., Comoli, P., Gandossini, S., Montini, E., Labirio, M., and Maccario, R. (1999). Characterisation of CTL directed towards non-inherited maternal alloantigens in human cord blood. Bone Marrow Transplant. 24, 1161-1166.
33. Nelson, J.L.(2003). Microchimerismin human health and disease. Autoimmunity 36,5-9.
34. Okumura, H., Yamaguchi, M., Kotani, T., Sugimori, N., Sugimori, C., Ozaki, J., Kondo, Y., Yamazaki, H., Chuhjo, T., Takami, A., Ueda, M., Ohtake, S., and Nakao, S. (2007). Graft rejection and hyperacute graftversus-host disease in stem cell transplantation from non-inherited maternal-antigen-complementary HLA-mismatched siblings. Eur. J. Haematol. 78,157-160.
35. Owen, R. D., Wood, H. R., Foord, A. G., Sturgeon, P., and Baldwin, L. G. (1954). Evidence for actively acquired tolerance to Rh antigens. Proc. Natl. Acad. Sci. U.S.A. 40,420-424.
36. Petersdorf, E. W., Longton, G. M., Anasetti, C., Martin, P. J., Mickelson, E. M., Smith, A. G., and Hansen, J. A. (1995). The significance of HLADRB1 matching on clinical outcome after HLA-A, B, DR identical unrelated donor marrow transplantation. Blood 86,1606-1613.
37. Roopenian, D., Choi, E. Y., and Brown, A. (2002). The immunogenomics of minor his to compatibility antigens. Immunol. Rev. 190,86-94.
38. Sanderson, C. J., and Frost, P. (1974). The induction of tumour immunity in mice using glutaraldehyde-treated tumor cells. Nature 248,690-691.
39. Sellami, M. H., Kaabi, H., Bibi, A., Sahli, C., Bani, M., Ben Ahmed, A., Massoud, T., and Hmida, S. (2011). Minor histocompatibility antigens in Tunisians: could platelet endothelial cell adhesion molecule 1 marker be one of them Tissue Antigens 77, 68-73.
40. Stern, M., Passweg, J. R., Locasciulli, A., Socié, G., Schrezenmeier, H., Békássy, A. N., Fuehrer, M., Hows, J., Korthof, E. T., McCann, S., Tichelli, A., Zoumbos, N. C., Marsh, J. C., Bacigalupo, A., Gratwohl, A., (2006) and for the Aplastic Anemia Working Party of the European Group for Blood and Marrow Transplantation Influence of donor/recipient sex matching on outcome of allogeneic hematopoietic stem cell transplantation for aplastic anemia. Transplantation 82, 218-226.
41. Suskind, D. L., Rosenthal, P., Heyman, M. B., Kong, D., Magrane, G., Baxter-Lowe, L. A., and Muench, M. O. (2004). Maternal microchimerism in the livers of patients with biliary atresia. BMC Gastroenterol. 4, 14. doi: 10.1186/1471-230X-4-14
42. Tsafrir, A., Brautbar, C., Nagler, A., Elchalal, U., Miller, K., and Bishara, A. (2000). Alloreactivity of umbilical cord blood mononuclear cells: specific hyporesponse to noninherited maternal antigens. Hum. Immunol. 61,548-554.
43. + Tregs by TCR gene transfer favors transplantation tolerance in mice. J. Clin. Invest. 118, 3619-3628.
44. Van Bergen, C. A., Rutten, C. E., Van Der Meijden, E. D., Van Luxemburg-Heijs, S.A., Lurvink, E.G., HouwingDuistermaat, J. J., Kester, M. G., Mulder, A., Willemze, R., Falkenburg, J.H.,and Griffioen, M.(2010). Highthroughput characterization of 10 new minor histocompatibility antigens by whole genome association scanning. Cancer Res. 70, 90739083.
45. van Halteren, A. G., Jankowska-Gan, E., Joosten, A., Blokland, E., Pool, J., Brand, A., Burlingham, W. J., and Goulmy, E. (2009). Naturally acquired tolerance and sensitization to minor histocompatibility antigens in healthy family members. Blood 114,2263-2272.
46. van Rood, J. J., and Claas, F. (2000). Bothself andnon-inheritedmaternal HLA antigens influence the immune response. Immunol. Today 21, 269-273.
47. van Rood, J. J., Loberiza, F. R. Jr., Zhang, M. J., Oudshoorn, M., Claas, F., Cairo, M. S., Champlin, R. E., Gale, R. P., Ringdén, O., Hows, J. M., and Horowitz, M. H. (2002). Effect of tolerance to noninherited maternal antigens on the occurrence of graft-versus-host disease after bone marrow transplantation from a parent or an HLA-haploidentical sibling. Blood 99,1572-1577.
48. Verdijk, R. M., Kloosterman, A., Pool, J., van de Keur, M., Naipal, A. M., van Halteren, A. G., Brand, A., Mutis, T., and Goulmy, E. (2004). Pregnancy induces minor histocompatibility antigen-specific cytotoxic T cells: implications for stem cell transplantation and immunotherapy. Blood 103, 1961-1964.
49. Verhasselt, V., Milcent, V., Cazareth, J., Kanda, A., Fleury, S., Dombrowicz, D., Glaichenhaus, N., and Julia, V. (2008). Breast milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma. Nat. Med. 14,170-175.
50. Vernochet, C., Caucheteux, S. M., Gendron, M. C., Wantyghem, J., and Kanellopoulos-Langevin, C. (2005). Affinity-dependent alterations of mouse B cell development by noninherited maternal antigen. Biol. Reprod. 72, 460-469.
51. Yang, J., Jaramillo, A., Liu, W., Olack, B., Yoshimura, Y., Joyce, S., Kaleem, Z., and Mohanakumar, T. (2003). Chronic rejection of murine cardiac allografts discordant at the H13 minor histocompatibility antigen correlates with the generation of the H13-specific CD8+ cytotoxic T cells. Transplantation 76, 84-91.