Advertisement

Chimerism pp 153-179 | Cite as

Autoimmune Disease

  • Nathalie Lambert
Chapter

Abstract

The first “autoimmune disease” for which fetal chimeric cells had been implicated in its pathogenesis, about a century ago, is preeclampsia. Indeed pregnancy complications could accentuate feto-maternal trafficking at an immunologically immature stage and leave long-term sequelae in the mother. In 1998, postdelivery fetal microchimerism (FMc) was found to be more prevalent in women with scleroderma (SSc) compared to matched controls. One hypothesis might be that microchimeric fetal T cells are activated and induce a graft-versus-host reaction manifesting as SSc. In the current chapter, we detail the arguments for a role of fetal cells as immune effector cells and explain the way chimeric cells may interact together in a particular Human Leukocyte Antigen (HLA) context. We also show this mechanism has some limitations and review the different factors that may have contributed to discredit this hypothesis. Moreover, studies in SSc and other autoimmune diseases have described fetal but also maternal Mc, in tissues, which raises the question of a restorative function within these tissues by different natural immigrants from diverse origin. The answer is probably not simple as multiple “grafts” across generations may all play a role.

Keywords

Microchimerism Autoimmune diseases Preeclampsia Scleroderma Systemic lupus erythematosus Rheumatoid arthritis Tissue repair 

References

  1. 1.
    Nelson JL. Maternal-fetal immunology and autoimmune disease: is some autoimmune disease auto-alloimmune or allo-autoimmune? Arthritis Rheum. 1996;39(2):191–4.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Nelson JL, Furst DE, Maloney S, Gooley T, Evans PC, Smith A, et al. Microchimerism and HLA-compatible relationships of pregnancy in scleroderma. Lancet. 1998;351(9102):559–62.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Lambert N, Nelson JL. Microchimerism in autoimmune disease: more questions than answers? Autoimmun Rev. 2003;2(3):133–9.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Xia Y, Kellems RE. Is preeclampsia an autoimmune disease? Clin Immunol. 2009;133(1):1–12.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Lapaire O, Holzgreve W, Oosterwijk JC, Brinkhaus R, Bianchi DW. Georg Schmorl on trophoblasts in the maternal circulation. Placenta. 2007;28(1):1–5.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Vlkova B, Turna J, Celec P. Fetal DNA in maternal plasma in preeclamptic pregnancies. Hypertens Pregnancy. 2015;34(1):36–49.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Lo YM, Leung TN, Tein MS, Sargent IL, Zhang J, Lau TK, et al. Quantitative abnormalities of fetal DNA in maternal serum in preeclampsia. Clin Chem. 1999;45(2):184–8.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Fisher SJ. Why is placentation abnormal in preeclampsia? Am J Obstet Gynecol. 2015;213(4 Suppl):S115–22.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Gammill HS, Aydelotte TM, Guthrie KA, Nkwopara EC, Nelson JL. Cellular fetal microchimerism in preeclampsia. Hypertension. 2013;62(6):1062–7.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Khosrotehrani K, Johnson KL, Lau J, Dupuy A, Cha DH, Bianchi DW. The influence of fetal loss on the presence of fetal cell microchimerism: a systematic review. Arthritis Rheum. 2003;48(11):3237–41.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Ooki I, Takakuwa K, Akashi M, Nonaka T, Yokoo T, Tanaka K. Studies on the compatibility of HLA-class II alleles in patient couples with severe pre-eclampsia using PCR-RFLP methods. Am J Reprod Immunol. 2008;60(1):75–84.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    van Wyk L, van der Marel J, Schuerwegh AJ, Schouffoer AA, Voskuyl AE, Huizinga TW, et al. Increased incidence of pregnancy complications in women who later develop scleroderma: a case control study. Arthritis Res Ther. 2011;13(6):R183.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Silman AJ, Black C. Increased incidence of spontaneous abortion and infertility in women with scleroderma before disease onset: a controlled study. Ann Rheum Dis. 1988;47(6):441–4.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Pisa FE, Bovenzi M, Romeo L, Tonello A, Biasi D, Bambara LM, et al. Reproductive factors and the risk of scleroderma: an Italian case-control study. Arthritis Rheum. 2002;46(2):451–6.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Furst DE, Clements PJ, Graze P, Gale R, Roberts N. A syndrome resembling progressive systemic sclerosis after bone marrow transplantation. A model for scleroderma? Arthritis Rheum. 1979;22(8):904–10.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Artlett CM, Welsh KI, Black CM, Jimenez SA. Fetal-maternal HLA compatibility confers susceptibility to systemic sclerosis. Immunogenetics. 1997;47(1):17–22.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Mullinax F. Chimerism in scleroderma. Lancet. 1998;351(9119):1886; author reply 7.CrossRefGoogle Scholar
  18. 18.
    Murata H, Nakauchi H, Sumida T. Microchimerism in Japanese women patients with systemic sclerosis. Lancet. 1999;354(9174):220.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Gannage M, Amoura Z, Lantz O, Piette JC, Caillat-Zucman S. Feto-maternal microchimerism in connective tissue diseases. Eur J Immunol. 2002;32(12):3405–13.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Selva-O’Callaghan A, Mijares-Boeckh-Behrens T, Prades EB, Solans-Laque R, Simeon-Aznar CP, Fonollosa-Pla V, et al. Lack of evidence of fetal microchimerism in female Spanish patients with systemic sclerosis. Lupus. 2003;12(1):15–20.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Abengozar MA, de Frutos S, Ferreiro S, Soriano J, Perez-Martinez M, Olmeda D, et al. Blocking ephrinB2 with highly specific antibodies inhibits angiogenesis, lymphangiogenesis, and tumor growth. Blood. 2012;119(19):4565–76.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Ohtsuka T, Miyamoto Y, Yamakage A, Yamazaki S. Quantitative analysis of microchimerism in systemic sclerosis skin tissue. Arch Dermatol Res. 2001;293(8):387–91.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Artlett CM, Cox LA, Ramos RC, Dennis TN, Fortunato RA, Hummers LK, et al. Increased microchimeric CD4+ T lymphocytes in peripheral blood from women with systemic sclerosis. Clin Immunol. 2002;103(3 Pt 1):303–8.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Lambert NC, Lo YM, Erickson TD, Tylee TS, Guthrie KA, Furst DE, et al. Male microchimerism in healthy women and women with scleroderma: cells or circulating DNA? A quantitative answer. Blood. 2002;100(8):2845–51.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Sahin A, Ozkan T, Turkcapar N, Kucuksahin O, Koksoy EB, Ozturk G, et al. Peripheral blood mononuclear cell microchimerism in Turkish female patients with systemic sclerosis. Mod Rheumatol. 2014;24(1):97–105.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Lambert NC. [Microchimerism in scleroderma: ten years later]. Rev Med Interne. 2010;31(7):523–9.Google Scholar
  27. 27.
    de Bellefon LM, Heiman P, Kanaan SB, Azzouz DF, Rak JM, Martin M, et al. Cells from a vanished twin as a source of microchimerism 40 years later. Chimerism. 2010;1(2):56–60.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Nakagome Y, Nagafuchi S, Nakahori Y. Prenatal sex determination. Lancet. 1990;335(8684):291.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Nakagome Y, Nagafuchi S, Seki S, Nakahori Y, Tamura T, Yamada M, et al. A repeating unit of the DYZ1 family on the human Y chromosome consists of segments with partial male-specificity. Cytogenet Cell Genet. 1991;56(2):74–7.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    De Moor G, De Bock G, Noens L, De Bie S. A new case of human chimerism detected after pregnancy: 46,XY karyotype in the lymphocytes of a woman. Acta Clin Belg. 1988;43(3):231–5.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Artlett CM, Smith JB, Jimenez SA. Identification of fetal DNA and cells in skin lesions from women with systemic sclerosis. N Engl J Med. 1998;338(17):1186–91.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Evans PC, Lambert N, Maloney S, Furst DE, Moore JM, Nelson JL. Long-term fetal microchimerism in peripheral blood mononuclear cell subsets in healthy women and women with scleroderma. Blood. 1999;93(6):2033–7.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Lambert NC, Evans PC, Hashizumi TL, Maloney S, Gooley T, Furst DE, et al. Cutting edge: persistent fetal microchimerism in T lymphocytes is associated with HLA-DQA1*0501: implications in autoimmunity. J Immunol. 2000;164(11):5545–8.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Miyashita Y, Ono M, Ueki H, Kurasawa K. Y chromosome microchimerism in rheumatic autoimmune disease. Ann Rheum Dis. 2000;59(8):655–6.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Artlett CM, Cox LA, Jimenez SA. Detection of cellular microchimerism of male or female origin in systemic sclerosis patients by polymerase chain reaction analysis of HLA-Cw antigens. Arthritis Rheum. 2000;43(5):1062–7.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Murata H, Sumida T. Quantitative analysis of fetal microchimerism in Japanese women patients with systemic sclerosis. Mod Rheumatol. 2001;11(3):259–60.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Johnson KL, Nelson JL, Furst DE, McSweeney PA, Roberts DJ, Zhen DK, et al. Fetal cell microchimerism in tissue from multiple sites in women with systemic sclerosis. Arthritis Rheum. 2001;44(8):1848–54.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Scaletti C, Vultaggio A, Bonifacio S, Emmi L, Torricelli F, Maggi E, et al. Th2-oriented profile of male offspring T cells present in women with systemic sclerosis and reactive with maternal major histocompatibility complex antigens. Arthritis Rheum. 2002;46(2):445–50.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Aractingi S, Sibilia J, Meignin V, Launay D, Hachulla E, Le Danff C, et al. Presence of microchimerism in labial salivary glands in systemic sclerosis but not in Sjogren’s syndrome. Arthritis Rheum. 2002;46(4):1039–43.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Burastero SE, Galbiati S, Vassallo A, Sabbadini MG, Bellone M, Marchionni L, et al. Cellular microchimerism as a lifelong physiologic status in parous women: an immunologic basis for its amplification in patients with systemic sclerosis. Arthritis Rheum. 2003;48(4):1109–16.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Artlett CM, O’Hanlon TP, Lopez AM, Song YW, Miller FW, Rider LG. HLA-DQA1 is not an apparent risk factor for microchimerism in patients with various autoimmune diseases and in healthy individuals. Arthritis Rheum. 2003;48(9):2567–72.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Sawaya HH, Jimenez SA, Artlett CM. Quantification of fetal microchimeric cells in clinically affected and unaffected skin of patients with systemic sclerosis. Rheumatology. 2004;43(8):965–8.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Lambert NC, Pang JM, Yan Z, Erickson TD, Stevens AM, Furst DE, et al. Male microchimerism in women with systemic sclerosis and healthy women who have never given birth to a son. Ann Rheum Dis. 2005;64(6):845–8.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Rak JM, Pagni PP, Tiev K, Allanore Y, Farge D, Harle JR, et al. Male microchimerism and HLA compatibility in French women with sclerodema: a different profile in limited and diffuse subset. Rheumatology. 2009;48(4):363–6.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Azzouz DF, Rak JM, Fajardy I, Allanore Y, Tiev KP, Farge-Bancel D, et al. Comparing HLA shared epitopes in French Caucasian patients with scleroderma. PLoS One. 2012;7(5):e36870.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Rak JM, Maestroni L, Balandraud N, Guis S, Boudinet H, Guzian MC, et al. Transfer of the shared epitope through microchimerism in women with rheumatoid arthritis. Arthritis Rheum. 2009;60(1):73–80.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Landy HJ, Keith LG. The vanishing twin: a review. Hum Reprod Update. 1998;4(2):177–83.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Jiang TT, Chaturvedi V, Ertelt JM, Kinder JM, Clark DR, Valent AM, et al. Regulatory T cells: new keys for further unlocking the enigma of fetal tolerance and pregnancy complications. J Immunol. 2014;192(11):4949–56.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Yan Z, Lambert NC, Guthrie KA, Porter AJ, Loubiere LS, Madeleine MM, et al. Male microchimerism in women without sons: quantitative assessment and correlation with pregnancy history. Am J Med. 2005;118(8):899–906.PubMedCrossRefGoogle Scholar
  50. 50.
    De Wit D, Van Mechelen M, Zanin C, Doutrelepont JM, Velu T, Gerard C, et al. Preferential activation of Th2 cells in chronic graft-versus-host reaction. J Immunol. 1993;150(2):361–6.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Lepez T, Vandewoestyne M, Deforce D. Fetal microchimeric cells in autoimmune thyroid diseases: harmful, beneficial or innocent for the thyroid gland? Chimerism. 2013;4(4):111–8.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Nelson JL. The otherness of self: microchimerism in health and disease. Trends Immunol. 2012;33(8):421–7.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Fialkow PJ, Gilchrist C, Allison AC. Autoimmunity in chronic graft-versus-host disease. Clin Exp Immunol. 1973;13(4):479–86.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Invernizzi P, Selmi C, Gershwin ME. Update on primary biliary cirrhosis. Dig Liver Dis. 2010;42(6):401–8.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Corpechot C, Barbu V, Chazouilleres O, Poupon R. Fetal microchimerism in primary biliary cirrhosis. J Hepatol. 2000;33(5):696–700.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Invernizzi P, De Andreis C, Sirchia SM, Battezzati PM, Zuin M, Rossella F, et al. Blood fetal microchimerism in primary biliary cirrhosis. Clin Exp Immunol. 2000;122(3):418–22.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Schoniger-Hekele M, Muller C, Ackermann J, Drach J, Wrba F, Penner E, et al. Lack of evidence for involvement of fetal microchimerism in pathogenesis of primary biliary cirrhosis. Dig Dis Sci. 2002;47(9):1909–14.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Selva O’Callaghan A, Balada Prades E, Castells Fuste L, Vargas Blasco V, Solans Laque R, Vilardell Tarres M. [Fetal microchimerism in patients with primary biliary cirrhosis]. Med Clin (Barc). 2002;119(20):770–2.Google Scholar
  59. 59.
    Tanaka A, Lindor K, Gish R, Batts K, Shiratori Y, Omata M, et al. Fetal microchimerism alone does not contribute to the induction of primary biliary cirrhosis. Hepatology. 1999;30(4):833–8.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, et al. Bone marrow as a potential source of hepatic oval cells. Science. 1999;284(5417):1168–70.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Theise ND, Badve S, Saxena R, Henegariu O, Sell S, Crawford JM, et al. Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology. 2000;31(1):235–40.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Khosrotehrani K, Reyes RR, Johnson KL, Freeman RB, Salomon RN, Peter I, et al. Fetal cells participate over time in the response to specific types of murine maternal hepatic injury. Hum Reprod. 2007;22(3):654–61.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Stevens AM, McDonnell WM, Mullarkey ME, Pang JM, Leisenring W, Nelson JL. Liver biopsies from human females contain male hepatocytes in the absence of transplantation. Lab Investig. 2004;84(12):1603–9.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Fanning PA, Jonsson JR, Clouston AD, Edwards-Smith C, Balderson GA, Macdonald GA, et al. Detection of male DNA in the liver of female patients with primary biliary cirrhosis. J Hepatol. 2000;33(5):690–5.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Sumida T, Azuma N, Moriyama M, Takahashi H, Asashima H, Honda F, Abe S, Ono Y, Hirota T, Hirata S, Tanaka Y, Shimizu T, Nakamura H, Kawakami A, Sano H, Ogawa Y, Tsubota K, Ryo K, Saito I, Tanaka A, Nakamura S, Takamura E, Tanaka M, Suzuki K, Takeuchi T, Yamakawa N, Mimori T, Ohta A, Nishiyama S, Yoshihara T, Suzuki Y, Kawano M, Tomiita M, Tsuboi H. Clinical practice guideline for Sjögren’s syndrome 2017. Mod Rheumatol. 2018:1–26. https://doi.org/10.1080/14397595.2018.1438093.
  66. 66.
    Abbud Filho M, Pavarino-Bertelli EC, Alvarenga MP, Fernandes IM, Toledo RA, Tajara EH, et al. Systemic lupus erythematosus and microchimerism in autoimmunity. Transplant Proc. 2002;34(7):2951–2.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    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;14:325.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    da Silva Florim GM, Caldas HC, Pavarino EC, Bertollo EM, Fernandes IM, Abbud-Filho M. Variables associated to fetal microchimerism in systemic lupus erythematosus patients. Clin Rheumatol. 2016;35(1):107–11.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Mosca M, Curcio M, Lapi S, Valentini G, D’Angelo S, Rizzo G, et al. Correlations of Y chromosome microchimerism with disease activity in patients with SLE: analysis of preliminary data. Ann Rheum Dis. 2003;62(7):651–4.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Kremer Hovinga IC, Koopmans M, Baelde HJ, de Heer E, Bruijn JA, Bajema IM. Tissue chimerism in systemic lupus erythematosus is related to injury. Ann Rheum Dis. 2007;66(12):1568–73.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Kremer Hovinga IC, Koopmans M, Baelde HJ, van der Wal AM, Sijpkens YW, de Heer E, et al. Chimerism occurs twice as often in lupus nephritis as in normal kidneys. Arthritis Rheum. 2006;54(9):2944–50.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Desai RG, Creger WP. Maternofetal passage of leukocytes and platelets in man. Blood. 1963;21:665–73.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Pollack MS, Kapoor N, Sorell M, Kim SJ, Christiansen FT, Silver DM, et al. DR-positive maternal engrafted T cells in a severe combined immunodeficiency patient without graft-versus-host disease. Transplantation. 1980;30(5):331–4.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Maloney S, Smith A, Furst DE, Myerson D, Rupert K, Evans PC, et al. Microchimerism of maternal origin persists into adult life. J Clin Invest. 1999;104(1):41–7.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Lambert NC, Erickson TD, Yan Z, Pang JM, Guthrie KA, Furst DE, et al. Quantification of maternal microchimerism by HLA-specific real-time polymerase chain reaction—studies of healthy women and women with scleroderma. Arthritis Rheum. 2004;50(3):906–14.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Loubiere LS, Lambert NC, Flinn LJ, Erickson TD, Yan Z, Guthrie KA, et al. Maternal microchimerism in healthy adults in lymphocytes, monocyte/macrophages and NK cells. Lab Investig. 2006;86(11):1185–92.PubMedPubMedCentralGoogle Scholar
  77. 77.
    Stevens AM. Maternal microchimerism in health and disease. Best Pract Res Clin Obstet Gynaecol. 2016;31:121–30.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Stevens AM, Hermes HM, Rutledge JC, Buyon JP, Nelson JL. Myocardial-tissue-specific phenotype of maternal microchimerism in neonatal lupus congenital heart block. Lancet. 2003;362(9396):1617–23.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Artlett CM, Ramos R, Jiminez SA, Patterson K, Miller FW, Rider LG. Chimeric cells of maternal origin in juvenile idiopathic inflammatory myopathies. Childhood Myositis Heterogeneity Collaborative Group. Lancet. 2000;356(9248):2155–6.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Reed AM, Picornell YJ, Harwood A, Kredich DW. Chimerism in children with juvenile dermatomyositis. Lancet. 2000;356(9248):2156–7.PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Artlett CM, Sassi-Gaha S, Ramos RC, Miller FW, Rider LG. Chimeric cells of maternal origin do not appear to be pathogenic in the juvenile idiopathic inflammatory myopathies or muscular dystrophy. Arthritis Res Ther. 2015;17:238.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Suskind DL, Rosenthal P, Heyman MB, Kong D, Magrane G, Baxter-Lowe LA, et al. Maternal microchimerism in the livers of patients with biliary atresia. BMC Gastroenterol. 2004;4:14.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Kobayashi H, Tamatani T, Tamura T, Kusafuka J, Yamataka A, Lane GJ, et al. Maternal microchimerism in biliary atresia. J Pediatr Surg. 2007;42(6):987–91. Discussion 91.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Lakshminarayanan B, Davenport M. Biliary atresia: a comprehensive review. J Autoimmun. 2016;73:1–9.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Muraji T, Hosaka N, Irie N, Yoshida M, Imai Y, Tanaka K, et al. Maternal microchimerism in underlying pathogenesis of biliary atresia: quantification and phenotypes of maternal cells in the liver. Pediatrics. 2008;121(3):517–21.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    Muraji T. Maternal microchimerism in biliary atresia: are maternal cells effector cells, targets, or just bystanders? Chimerism. 2014;5(1):1–5.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Irie N, Muraji T, Hosaka N, Takada Y, Sakamoto S, Tanaka K. Maternal HLA class I compatibility in patients with biliary atresia. J Pediatr Gastroenterol Nutr. 2009;49(4):488–92.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    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(2):409–19.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Nelson JL, Gillespie KM, Lambert NC, Stevens AM, Loubiere LS, Rutledge JC, et al. Maternal microchimerism in peripheral blood in type 1 diabetes and pancreatic islet beta cell microchimerism. Proc Natl Acad Sci U S A. 2007;104(5):1637–42.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Moles JP, Tuaillon E, Kankasa C, Bedin AS, Nagot N, Marchant A, et al. Breastfeeding-related maternal microchimerism. Nat Rev Immunol. 2017;17(11):729–1.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Ebers GC, Sadovnick AD, Dyment DA, Yee IM, Willer CJ, Risch N. Parent-of-origin effect in multiple sclerosis: observations in half-siblings. Lancet. 2004;363(9423):1773–4.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Ramagopalan SV, Herrera BM, Bell JT, Dyment DA, Deluca GC, Lincoln MR, et al. Parental transmission of HLA-DRB1*15 in multiple sclerosis. Hum Genet. 2008;122(6):661–3.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Willer CJ, Herrera BM, Morrison KM, Sadovnick AD, Ebers GC, Canadian Collaborative Study on Genetic Susceptibility to Multiple Sclerosis. Association between microchimerism and multiple sclerosis in Canadian twins. J Neuroimmunol. 2006;179(1-2):145–51.PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Kanold AM, Svenungsson E, Gunnarsson I, Gotherstrom C, Padyukov L, Papadogiannakis N, et al. A research study of the association between maternal microchimerism and systemic lupus erythematosus in adults: a comparison between patients and healthy controls based on single-nucleotide polymorphism using quantitative real-time PCR. PLoS One. 2013;8(9):e74534.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Bianchi DW, Zickwolf GK, Weil GJ, Sylvester S, DeMaria MA. Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proc Natl Acad Sci U S A. 1996;93(2):705–8.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Guetta E, Gordon D, Simchen MJ, Goldman B, Barkai G. Hematopoietic progenitor cells as targets for non-invasive prenatal diagnosis: detection of fetal CD34+ cells and assessment of post-delivery persistence in the maternal circulation. Blood Cells Mol Dis. 2003;30(1):13–21.PubMedCrossRefPubMedCentralGoogle Scholar
  97. 97.
    O’Donoghue K, Chan J, de la Fuente J, Kennea N, Sandison A, Anderson JR, et al. Microchimerism in female bone marrow and bone decades after fetal mesenchymal stem-cell trafficking in pregnancy. Lancet. 2004;364(9429):179–82.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Kara RJ, Bolli P, Karakikes I, Matsunaga I, Tripodi J, Tanweer O, et al. Fetal cells traffic to injured maternal myocardium and undergo cardiac differentiation. Circ Res. 2012;110(1):82–93.PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Nassar D, Droitcourt C, Mathieu-d’Argent E, Kim MJ, Khosrotehrani K, Aractingi S. Fetal progenitor cells naturally transferred through pregnancy participate in inflammation and angiogenesis during wound healing. FASEB J. 2012;26(1):149–57.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    Bonney EA, Matzinger P. The maternal immune system’s interaction with circulating fetal cells. J Immunol. 1997;158(1):40–7.PubMedPubMedCentralGoogle Scholar
  101. 101.
    Kaplan J, Land S. Influence of maternal-fetal histocompatibility and MHC zygosity on maternal microchimerism. J Immunol. 2005;174(11):7123–8.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Gregersen PK, Silver J, Winchester RJ. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 1987;30(11):1205–13.PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    Roudier J. Association of MHC and rheumatoid arthritis. Association of RA with HLA-DR4: the role of repertoire selection. Arthritis Res. 2000;2(3):217–20.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    van der Horst-Bruinsma IE, Hazes JM, Schreuder GM, Radstake TR, Barrera P, van de Putte LB, et al. Influence of non-inherited maternal HLA-DR antigens on susceptibility to rheumatoid arthritis. Ann Rheum Dis. 1998;57(11):672–5.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Silman AJ, Hay EM, Worthington J, Thomson W, Pepper L, Davidson J, et al. Lack of influence of non-inherited maternal HLA-DR alleles on susceptibility to rheumatoid arthritis. Ann Rheum Dis. 1995;54(4):311–3.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    MacGregor A, Ollier W, Thomson W, Jawaheer D, Silman A. HLA-DRB1*0401/0404 genotype and rheumatoid arthritis: increased association in men, young age at onset, and disease severity. J Rheumatol. 1995;22(6):1032–6.PubMedPubMedCentralGoogle Scholar
  107. 107.
    Yan Z, Aydelotte T, Gadi V, Guthrie KA, Nelson JL. Acquisition of the rheumatoid arthritis HLA shared epitope through microchimerism. Arthritis Rheum. 2011;63:640.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Chan WFN, Atkins CJ, Naysmith D, van der Westhuizen N, Woo J, Nelson JL. Microchimerism in the rheumatoïd nodules of patients with rheumatoid arthritis. Arthritis Rheum. 2012;64(2):380–8.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Hromadnikova I, Zlacka D, Hien Nguyen TT, Sedlackova L, Zejskova L, Sosna A. Fetal cells of mesenchymal origin in cultures derived from synovial tissue and skin of patients with rheumatoid arthritis. Joint Bone Spine. 2008;75(5):563–6.PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Cruz GI, Shao X, Quach H, Ho KA, Sterba K, Noble JA, et al. Increased risk of rheumatoid arthritis among mothers with children who carry DRB1 risk-associated alleles. Ann Rheum Dis. 2017;76(8):1405–10.PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    Nelson JL, Lambert NC. Rheumatoid arthritis: forward and reverse inheritance—the yin and the yang. Nat Rev Rheumatol. 2017;13(7):396–7.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Wrenshall LE, Stevens ET, Smith DR, Miller JD. Maternal microchimerism leads to the presence of interleukin-2 in interleukin-2 knock out mice: implications for the role of interleukin-2 in thymic function. Cell Immunol. 2007;245(2):80–90.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Arvola M, Gustafsson E, Svensson L, Jansson L, Holmdahl R, Heyman B, et al. Immunoglobulin-secreting cells of maternal origin can be detected in B cell-deficient mice. Biol Reprod. 2000;63(6):1817–24.PubMedCrossRefPubMedCentralGoogle Scholar
  114. 114.
    Gregg R, Smith CM, Clark FJ, Dunnion D, Khan N, Chakraverty R, et al. The number of human peripheral blood CD4+ CD25high regulatory T cells increases with age. Clin Exp Immunol. 2005;140(3):540–6.PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Kubista M, Dreyer-Lamm J, Stahlberg A. The secrets of the cell. Mol Asp Med. 2018;59:1–4.CrossRefGoogle Scholar
  116. 116.
    Stahlberg A, El-Heliebi A, Sedlmayr P, Kroneis T. Unravelling the biological secrets of microchimerism by single-cell analysis. Brief Funct Genomics. 2017:1–10. https://doi.org/10.1093/bfgp/elx027.
  117. 117.
    Kinder JM, Stelzer IA, Arck PC, Way SS. Immunological implications of pregnancy-induced microchimerism. Nat Rev Immunol. 2017;17(8):483–94.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Aix Marseille Univeristy, INSERM UMRs 1097, Arthrites Autoimmunes AAMarseilleFrance

Personalised recommendations