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Stem Cell Reviews and Reports

, Volume 14, Issue 5, pp 632–641 | Cite as

Incognito: Are Microchimeric Fetal Stem Cells that Cross Placental Barrier Real Emissaries of Peace?

  • Cosmin Andrei Cismaru
  • Laura Pop
  • Ioana Berindan-Neagoe
Article
  • 148 Downloads

Abstract

Chimerism occurs naturaly throughout gestation and can also occur as a consequence of transfusion and transplantation therapy. It consists of the acquisition and long-term persistence of a genetically distinct population of allogenic cells inside another organism. Previous reports have suggested that feto-maternal microchimerism could exert a beneficial effect on the treatment of hematological and solid tumors in patients treated by PBSCT. In this review we report the mechanism of transplacental fetal stem cell trafficking during pregnancy and the effect of their long-term persistence on autoimmunity, GVHD, PBSCT, cancer and stem cell treatment.

Keywords

Chimerism Rechimerism Transplantation Allograft Autograft PBSC GVHD GVT NIMA Exosomes Pluripotent stem cells VSELs 

Notes

Compliance with Ethical Standards

Conflict of Interests

All authors have read and approved this version of the article, and due care has been taken to ensure the integrity of the work. No part of this article has been published or submitted elsewhere. No financial conflict of interest exists in the submission of this manuscript.

References

  1. 1.
    Chan, W. F., Gurnot, C., Montine, T. J., Sonnen, J. A., Guthrie, K. A., & Nelson, J. L. (2012). Male microchimerism in the human female brain. PLoS One, 7(9), e45592.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Georgiades, P., Ferguson-Smith, A. C., & Burton, G. J. (2002). Comparative developmental anatomy of the murine and human definitive placentae. Placenta, 23(1), 3–19.CrossRefPubMedGoogle Scholar
  3. 3.
    Bainbridge, D. R. (2000). Evolution of mammalian pregnancy in the presence of the maternal immune system. Reviews of Reproduction, 5(2), 67–74 Review.CrossRefPubMedGoogle Scholar
  4. 4.
    Thomas, M. R., Williamson, R., Craft, I., & Rodeck, C. H. (1994). The time of appearance, and quantitation, of fetal DNA in the maternal circulation. Annals of the New York Academy of Sciences, 731, 217–225.CrossRefPubMedGoogle Scholar
  5. 5.
    Ariga, H., Ohto, H., Busch, M. P., Imamura, S., Watson, R., Reed, W., et al. (2001). Kinetics of fetal cellular and cell-free DNA in the maternal circulation during and after pregnancy: implications for noninvasive prenatal diagnosis. Transfusion, 41(12), 1524–1530.CrossRefPubMedGoogle Scholar
  6. 6.
    Bianchi, D. W., & Hanson, J. (2006). Sharpening the tools: a summary of a National Institutes of Health workshop on new technologies for detection of fetal cells in maternal blood for early prenatal diagnosis. The Journal of Maternal-Fetal & Neonatal Medicine, 19(4), 199–207.CrossRefGoogle Scholar
  7. 7.
    Tafuri, A., Alferink, J., Möller, P., Hämmerling, G. J., & Arnold, B. (1995). T cell awareness of paternal alloantigens during pregnancy. Science, 270(5236), 630–633.CrossRefPubMedGoogle Scholar
  8. 8.
    Thellin, O., Coumans, B., Zorzi, W., Igout, A., & Heinen, E. (2000). Tolerance to the foeto-placental ‘graft’: ten ways to support a child for nine months. Current Opinion in Immunology, 12(6), 731–737 Review.CrossRefPubMedGoogle Scholar
  9. 9.
    Housseau, F., Rouas-Freiss, N., Benifla, J. L., Marcillac, I., Roy, M., Troalen, F., et al. (1995). Reaction of peripheral-blood lymphocytes to the human chorionic gonadotropin beta sub-unit in patients with productive tumors. International Journal of Cancer, 63(5), 633–638.CrossRefPubMedGoogle Scholar
  10. 10.
    Guleria, I., Khosroshahi, A., Ansari, M. J., Habicht, A., Azuma, M., Yagita, H., et al. (2005). A critical role for the programmed death ligand 1 in fetomaternal tolerance. The Journal of Experimental Medicine, 202(2), 231–237.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Sánchez-Fueyo, A., Sandner, S., Habicht, A., Mariat, C., Kenny, J., Degauque, N., et al. (2006). Specificity of CD4 + CD25+ regulatory T cell function in alloimmunity. Journal of Immunology, 176(1), 329–334.CrossRefGoogle Scholar
  12. 12.
    Mellor, A. L., & Munn, D. H. (2001). Extinguishing maternal immune responses during pregnancy: implications for immunosuppression. Seminars in Immunology, 13(4), 213–218 Review.CrossRefPubMedGoogle Scholar
  13. 13.
    Xu, C., Mao, D., Holers, V. M., Palanca, B., Cheng, A. M., & Molina, H. (2000). A critical role for murine complement regulator crry in fetomaternal tolerance. Science, 287(5452), 498–501.CrossRefPubMedGoogle Scholar
  14. 14.
    Aluvihare, V. R., Kallikourdis, M., & Betz, A. G. (2004). Regulatory T cells mediate maternal tolerance to the fetus. Nature Immunology, 5(3), 266–271.CrossRefPubMedGoogle Scholar
  15. 15.
    Darrasse-Jèze, G., Klatzmann, D., Charlotte, F., Salomon, B. L., & Cohen, J. L. (2006). CD4 + CD25+ regulatory/suppressor T cells prevent allogeneic fetus rejection in mice. Immunology Letters, 102(1), 106–109 Erratum in: Immunol Lett. Feb 15;102(2):241.CrossRefPubMedGoogle Scholar
  16. 16.
    Lucia Mincheva-Nilsson, Vladimir Baranov. (2012). Placenta-Derived Exosomes and Their Role in the Immune Protection of the Fetus. Recent Advances in Research on the Human Placenta. Chapter. March pg.243–260.  https://doi.org/10.5772/32445. Available online at www.researchgate.net/publication/221927564_Placenta-Derived_Exosomes_and_Their_Role_in_the_Immune_Protection_of_the_Fetus
  17. 17.
    Tan, X. W., Liao, H., Sun, L., Okabe, M., Xiao, Z. C., & Dawe, G. S. (2005). Fetal microchimerism in the maternal mouse brain: a novel population of fetal progenitor or stem cells able to cross the blood-brain barrier? Stem Cells, 23(10), 1443–1452.CrossRefPubMedGoogle Scholar
  18. 18.
    Maloney, S., Smith, A., Furst, D. E., Myerson, D., Rupert, K., Evans, P. C., & Nelson, J. L. (1999). Microchimerism of maternal origin persists into adult life. The Journal of Clinical Investigation, 104, 41–47.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Lo, Y. M., Lo, E. S., Watson, N., Noakes, L., Sargent, I. L., Thilaganathan, B., & Wainscoat, J. S. (1996). Twoway cell traffic between mother and fetus: biologic and clinical implications. Blood, 88, 4390–4395.PubMedGoogle Scholar
  20. 20.
    Stevens, A. M., Hermes, H. M., Rutledge, J. C., Buyon, J. P., & Nelson, J. L. (2003). Myocardial-tissue-specific phenotype of maternal microchimerism in neonatal lupus congenital heart block. Lancet, 362, 1617–1623.CrossRefPubMedGoogle Scholar
  21. 21.
    Reed, A. M., Picornell, Y. J., Harwood, A., & Kredich, D. W. (2000). Chimerism in children with juvenile dermatomyositis. Lancet, 356, 2156–2157.CrossRefPubMedGoogle Scholar
  22. 22.
    Bianchi, D. W., Klinger, K. W., Vadnais, T. J., Demaria, M. A., Shuber, A. P., Skoletsky, J., et al. (1996). Development of a model system to compare cell separation methods for the isolation of fetal cells from maternal blood. Prenatal Diagnosis, 16(4), 289–298.CrossRefPubMedGoogle Scholar
  23. 23.
    Evans, P. C., Lambert, N., Maloney, S., Furst, D. E., Moore, J. M., & Nelson, J. L. (1999). Long-term fetal microchimerism in peripheral blood mononuclear cell subsets in healthy women and women with scleroderma. Blood, 93(6), 2033–2037.PubMedGoogle Scholar
  24. 24.
    Khosrotehrani, K., Leduc, M., Bachy, V., Nguyen Huu, S., Oster, M., Abbas, A., et al. (2008). Pregnancy allows the transfer and differentiation of fetal lymphoid progenitors into functional T and B cells in mothers. Journal of Immunology, 180(2), 889–897 Erratum in: J Immunol. Mar 1;180(5):3613.CrossRefGoogle Scholar
  25. 25.
    Fujiki, Y., Johnson, K. L., Peter, I., Tighiouart, H., & Bianchi, D. W. (2009). Fetal cells in the pregnant mouse are diverse and express a variety of progenitor and differentiated cell markers. Biology of Reproduction, 81(1), 26–32.  https://doi.org/10.1095/biolreprod.108.074468.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Bayes-Genis, A., Bellosillo, B., de la Calle, O., Salido, M., Roura, S., Ristol, F. S., et al. (2005). Identification of male cardiomyocytes of extracardiac origin in the hearts of women with male progeny: male fetal cell microchimerism of the heart. The Journal of Heart and Lung Transplantation, 24(12), 2179–2183.CrossRefPubMedGoogle Scholar
  27. 27.
    Wang, X. R., Chen, S. H., Liu, H. Z., Xiong, J. W., & Ling, X. Z. (2004). The experimental study of guinea pig cytomegalovirus infection in the kidney of the pup of guinea pig. Chinese Journal of Obstetrics and Gynecology, 39(02), 91–93.Google Scholar
  28. 28.
    Guettier, C., Sebagh, M., Buard, J., Feneux, D., Ortin-Serrano, M., Gigou, M., et al. (2005). Male cell microchimerism in normal and diseased female livers from fetal life to adulthood. Hepatology, 42(1), 35–43.CrossRefPubMedGoogle Scholar
  29. 29.
    Parant, O., Dubernard, G., Challier, J. C., Oster, M., Uzan, S., Aractingi, S., et al. (2009). CD34+ cells in maternal placental blood are mainly fetal in origin and express endothelial markers. Laboratory Investigation, 89(8), 915–923.CrossRefPubMedGoogle Scholar
  30. 30.
    Srivatsa, B., Srivatsa, S., Johnson, K. L., Samura, O., Lee, S. L., & Bianchi, D. W. (2001). Microchimerism of presumed fetal origin in thyroid specimens from women: a case-control study. Lancet, 358(9298), 2034–2038.CrossRefPubMedGoogle Scholar
  31. 31.
    O’Donoghue, K., Choolani, M., Chan, J., de la Fuente, J., Kumar, S., Campagnoli, C., et al. (2003). Identification of fetal mesenchymal stem cells in maternal blood: implications for non-invasive prenatal diagnosis. Molecular Human Reproduction, 9(8), 497–502.CrossRefPubMedGoogle Scholar
  32. 32.
    Bianchi, D. W., Zickwolf, G. K., Weil, G. J., Sylvester, S., & DeMaria, M. A. (1996). Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proceedings of the National Academy of Sciences of the United States of America, 93(2), 705–708.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Sunami, R., Komuro, M., Tagaya, H., & Hirata, S. (2010). Migration of microchimeric fetal cells into maternal circulation before placenta formation. Chimerism, 1(2), 66–68.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Johnson, K. L., Samura, O., Nelson, J. L., McDonnell, M. d. W. M., & Bianchi, D. W. (2002). Significant fetal cell microchimerism in a nontransfused woman with hepatitis C: Evidence of long-term survival and expansion. Hepatology, 36(5), 1295–1297.CrossRefPubMedGoogle Scholar
  35. 35.
    Magued, M., Hamdi, H., Welsh, J., Levicar, N., Marley, S., Nicholls, J., et al. (2008). High frequency of fetal cells within a primitive stem cell population in maternal blood. Human Reproduction, 23(4), 928–933.CrossRefGoogle Scholar
  36. 36.
    Ratajczak, M., Machalinski, B., Wojakowski, W., Ratajczak, J., & Kucia, M. (2007). A hypothesis for an embryonic origin of pluripotent Oct-4 + stem cells in adult bone marrow and other tissues. Leukemia, 21, 860–867.CrossRefPubMedGoogle Scholar
  37. 37.
    Ratajczak, M. Z., Suszynska, M., Pedziwiatr, D., Mierzejewska, K., & Greco, N. J. (2012). Umbilical cord blood-derived very small embryonic like stem cells (VSELs) as a source of pluripotent stem cells for regenerative medicine. Pediatric Endocrinology Reviews, 9(3), 639–643.PubMedGoogle Scholar
  38. 38.
    Artlett, C. M., Bruce Smith, J., & Jimenez, S. A. (1998). Identification of Fetal DNA and Cells in Skin Lesions from Women with Systemic Sclerosis. New England Journal of Medicine, 338(17), 1186–1191.CrossRefPubMedGoogle Scholar
  39. 39.
    Johnson, K. L., Nelson, J. L., Furst, D. E., McSweeney, P. A., Roberts, D. J., Zhen, D. K., & Bianchi, D. W. (2001). Fetal cell microchimerism in tissue from multiple sites in women with systemic sclerosis. Arthritis and Rheumatism, 44(8), 1848–1854.CrossRefPubMedGoogle Scholar
  40. 40.
    Ohtsuka, T., Miyamoto, Y., Yamakage, A., & Yamazaki, S. (2001). Quantitative analysis of microchimerism in systemic sclerosis skin tissue. Archives of Dermatological Research, 293(8), 387–391.CrossRefPubMedGoogle Scholar
  41. 41.
    Lambert, N. C., Lo, Y. M., Erickson, T. D., Tylee, T. S., Guthrie, K. A., Furst, D. E., & Nelson, J. L. (2002). Male microchimerism in healthy women and women with scleroderma: cells or circulating DNA? A quantitative answer. Blood, 100(8), 2845–2851.CrossRefPubMedGoogle Scholar
  42. 42.
    Ichikawa, N., Kotake, S., Hakoda, M., & Kamatani, N. (2001). Microchimerism in Japanese patients with systemic sclerosis. Arthritis and Rheumatism, 44(5), 1226–1228.CrossRefPubMedGoogle Scholar
  43. 43.
    Klintschar, M., Schwaiger, P., Mannweiler, S., Regauer, S., & Kleiber, M. (2001). Evidence of fetal microchimerism in Hashimoto's thyroiditis. The Journal of Clinical Endocrinology and Metabolism, 86(6), 2494–2498.PubMedGoogle Scholar
  44. 44.
    Ando, T., Imaizumi, M., Graves, P. N., Unger, P., & Davies, T. F. (2002). Intrathyroidal fetal microchimerism in Graves' disease. The Journal of Clinical Endocrinology and Metabolism, 87(7), 3315–3320.PubMedGoogle Scholar
  45. 45.
    Fanning, P. A., Jonsson, J. R., Clouston, A. D., Edwards-Smith, C., Balderson, G. A., Macdonald, G. A., Crawford, D. H., Kerlin, P., Powell, L. W., & Powell, E. E. (2000). Detection of male DNA in the liver of female patients with primary biliary cirrhosis. Journal of Hepatology, 33(5), 690–695.CrossRefPubMedGoogle Scholar
  46. 46.
    Selva O'Callaghan, A., Balada Prades, E., Castells Fusté, L., Vargas Blasco, V., Solans Laque, R., & Vilardell, T. M. (2002). Fetal microchimerism in patients with primary biliary cirrhosis. Medicina Clínica (Barcelona), 119(20), 770–772.CrossRefGoogle Scholar
  47. 47.
    Hovinga, I. C. L. K., Koopmans, M., Baelde, H. J., van der Wal, A. M., Sijpkens, Y. W. J., de Heer, E., Bruijn, J. A., & Bajema, I. M. (2006). Chimerism occurs twice as often in lupus nephritis as in normal kidneys. Arthritis and Rheumatism, 54(9), 2944–2950.CrossRefGoogle Scholar
  48. 48.
    Florim, G. M. S., Caldas, H. C., de Melo, J. C. R., Baptista, M. A. S. F., Fernandes, I. M. M., Savoldi-Barbosa, M., Goldman, G. H., & Abbud-Filho, M. (2015). Fetal microchimerism in kidney biopsies of lupus nephritis patients may be associated with a beneficial effect. Arthritis Research & Therapy, 17(1).Google Scholar
  49. 49.
    Lee Nelson, J., Hughes, K. A., Smith, A. G., Nisperos, B. B., Branchaud, A. M., & Hansen, J. A. (1993). Maternal-Fetal Disparity in HLA Class II Alloantigens and the Pregnancy-Induced Amelioration of Rheumatoid Arthritis. New England Journal of Medicine, 329(7), 466–471.CrossRefGoogle Scholar
  50. 50.
    Gammill, H. S., & Nelson, J. L. (2010). Naturally acquired microchimerism. The International Journal of Developmental Biology, 54(2–3), 531–543.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Khosrotehrani, K., Mery, L., Aractingi, S., Bianchi, D. W., & Johnson, K. L. (2005). Absence of fetal cell microchimerism in cutaneous lesions of lupus erythematosus. Annals of the Rheumatic Diseases, 64(1), 159–160.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Pidala, J., Kim, J., Anasetti, C., Nishihori, T., Betts, B., Field, T., et al. (2011). The global severity of chronic graft-versus-host disease, determined by National Institutes of Health consensus criteria, is associated with overall survival and non-relapse mortality. Haematologica, 96(11), 1678–1684.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Beatty, P. G., Clift, R. A., Mickelson, E. M., Nisperos, B. B., Flournoy, N., Martin, P. J., et al. (1985). Marrow transplantation from related donors other than HLA-identical siblings. The New England Journal of Medicine, 313(13), 765–771.CrossRefPubMedGoogle Scholar
  54. 54.
    Ochiai, N., Inaba, T., Maruya, E., Saji, H., Nakagawa, M., & Shimazaki, C. Feto-maternal microchimaerism does not indicate the existence of feto-maternal immunological tolerance in human leucocyte antigen haploidentical haematopoietic stem cell transplantation from mother to offspring. British Journal of Haematology, 122(5), 869–870.Google Scholar
  55. 55.
    Yoshihara, T., Morimoto, A., Inukai, T., Kuroda, H., Ishida, H., Sugita, K., et al. Non-T-cell-depleted HLA haploidentical stem cell transplantation based on feto-maternal microchimerism in pediatric patients with advanced malignancies. Bone Marrow Transplantation, 34(4), 373–375.Google Scholar
  56. 56.
    Yabe, H., Inoue, H., Matsumoto, M., Hamanoue, S., Hiroi, A., Koike, T., et al. (2004). Unmanipulated HLA-haploidentical bone marrow transplantation for the treatment of fatal, nonmalignant diseases in children and adolescents. International Journal of Hematology, 80(1), 78–82.CrossRefPubMedGoogle Scholar
  57. 57.
    Shimazaki, C., Ochiai, N., Uchida, R., Okano, A., Fuchida, S., Ashihara, E., et al. (2002). Non-T-cell-depleted HLA haploidentical stem cell transplantation in advanced hematologic malignancies based on the feto-maternal michrochimerism. Blood, 101(8), 3334–3336.CrossRefPubMedGoogle Scholar
  58. 58.
    van Rood, J. J., Roelen, D. L., & Claas, F. H. (2005). The effect of noninherited maternal antigens in allogeneic transplantation. Seminars in Hematology, 42(2), 104–111.CrossRefPubMedGoogle Scholar
  59. 59.
    Satoh, M., Miyamura, K., Yamada, M., Ishidoya, S., Childs, R. W., & Arai, Y. (2004). Haploidentical, non-myeloablative stem-cell transplantation for advanced renal-cell carcinoma. The Lancet Oncology, 5(2), 125–126.CrossRefPubMedGoogle Scholar
  60. 60.
    Tsutsumi, Y., Tanaka, J., Miura, T., Saitoh, S., Yamada, M., Yamato, H., et al. (2004). Successful non-T-cell-depleted nonmyeloablative hematopoietic stem cell transplantation (NST) from an HLA-haploidentical 2-loci-mismatched sibling in a heavily transfused patient with severe aplastic anemia based on the fetomaternal microchimerism. Bone Marrow Transplantation, 34(3), 267–269.CrossRefPubMedGoogle Scholar
  61. 61.
    Manilay, J. O., Pearson, D. A., Sergio, J. J., Swenson, K. G., & Sykes, M. (1998). Intrathymic deletion of alloreactive T cells in mixed bone marrow chimeras prepared with a nonmyeloablative conditioning regimen. Transplantation, 66(1), 96–102.CrossRefPubMedGoogle Scholar
  62. 62.
    Kawai, T., Cosimi, A. B., Colvin, R. B., Powelson, J., Eason, J., Koz lowski, T., et al. (1995). Mixed allogeneic chimerism and renal allograft tolerance in cynomologous monkeys. Transplantation, 59, 256–262.CrossRefPubMedGoogle Scholar
  63. 63.
    Durham, M. M., Bingaman, A. W., Adams, A. B., Ha, J., Waitze, S. Y., Pearson, T. C., et al. (2000). Cutting edge: administration of anti-CD40 ligand and donor bone marrow leads to hemopoietic chimerism and donor-specific tolerance without cytoreductive conditioning. Journal of Immunology, 165, 1–4.CrossRefGoogle Scholar
  64. 64.
    Teshima, T., Matsuoka, K., & IchinoheT. (2006). Impact of fetal-maternal tolerance in hematopoietic stem cell transplantation. Archivum Immunologiae et Therapiae Experimentalis, 54, 165–172.Google Scholar
  65. 65.
    Yu, J., Ren, X., Cao, S., Li, H., & Hao, X. (2008). Beneficial effects of fetal-maternal microchimerism on the activated haplo-identical peripheral blood stem cell treatment for cancer. Cytotherapy, 10(4), 331–339.CrossRefPubMedGoogle Scholar
  66. 66.
    Masahiro, H., Eiichi, A., Tsuyoshi, I., Yoshitaka, K., & Yoshihiro, K. (2013). A feasibility study on the prediction of acute graft-vs.-host disease before hematopoietic stem cell transplantation based on fetomaternal tolerance. Chimerism, 4(3), 84–86 July/August/September; © 2013 Landes Bioscience.CrossRefGoogle Scholar
  67. 67.
    Starzl, T. E., Demetris, A. J., Murase, N., Ildstad, S., Ricordi, C., & Trucco, M. (1992). Cell migration, chimerism and graft acceptance. Lancet, 339, 1579–1582.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Gadi, V. K., & Nelson, J. L. (2007). Fetal microchimerism in women with breast cancer. Cancer Research, 67(19), 9035–9038.CrossRefPubMedGoogle Scholar
  69. 69.
    Gadi, V. K., Malone, K. E., Guthrie, K. A., Porter, P. L., & Nelson, J. L. (2008). Case-control study of fetal microchimerism and breast cancer. PLoS One, 3(3), e1706.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Gilmore, G. L., Haq, B., Shadduck, R. K., Jasthy, S. L., & Lister, J. (2008). Fetal-maternal microchimerism in normal parous females and parous female cancer patients. Experimental Hematology, 36(9), 1073–1077.CrossRefPubMedGoogle Scholar
  71. 71.
    Cirello, V., Recalcati, M. P., Muzza, M., Rossi, S., Perrino, M., Vicentini, L., et al. (2008). Fetal cell microchimerism in papillary thyroid cancer: a possible role in tumor damage and tissue repair. Cancer Research, 15, 8482–8488.CrossRefGoogle Scholar
  72. 72.
    Dhimolea, E., Denes, V., Lakk, M., Al-Bazzaz, S., Aziz-Zaman, S., Pilichowska, M., et al. (2013). High male chimerism in the female breast shows quantitative links with cancer. International Journal of Cancer, 133, 835–842.CrossRefPubMedGoogle Scholar
  73. 73.
    Nguyen Huu, S., Oster, M., & Avril, M. F. (2009). Fetal microchimeric cells participate in tumour angiogenesis in melanomas occurring during pregnancy. The American Journal of Pathology, 174(2), 630–637.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Lee, E. S. M., Bou-Gharios, G., Seppanen, E., Khosrotehrani, K., & Fisk, N. M. (2010). Fetal stem cell microchimerism: natural-born healers or killers? Molecular Human Reproduction, 16(11), 869–878.CrossRefPubMedGoogle Scholar
  75. 75.
    O’Donoghue, K., & Fisk, N. M. (2004). Fetal stem cells. Best Practice & Research Clinical Obstetrics & Gynaecology, 18(6), 853–875.CrossRefGoogle Scholar
  76. 76.
    Ying, H., Jinpu, Y., Shui, C., Hui, L., Baozhu, R., Xiumei, A., et al. (2010). Fetal–Maternal Microchimerism Enhances the Survival Effect of Interleukin-2-Activated Haploidentical Peripheral Blood Stem Cell Treatment in Patients with Advanced Solid Cancer. Cancer Biotherapy and Radiopharmaceuticals, 25(6, Mary Ann Liebert, Inc.).  https://doi.org/10.1089/cbr.2010.0770.
  77. 77.
    Obama K, Utsunomiya A, Takatsuka Y, Takemoto Y. (2004) Reduced-intensity non-T-cell depleted HLA-haploidentical stem cell transplantation for older patients based on the concept of feto-maternal tolerance. Bone Marrow Transplant.Google Scholar
  78. 78.
    Farina, A., Sekizawa, A., Sugito, Y., Iwasaki, M., Jimbo, M., Saito, H., Okai, T. F., et al. (2004). DNA in maternal plasma as a screening variable for preeclampsia. A preliminary nonparametric analysis of detection rate in low-risk nonsymptomatic patients. Prenatal Diagnosis, 24, 83–86.CrossRefPubMedGoogle Scholar
  79. 79.
    Jakobsen, T. R., Clausen, F. B., Rode, L., Dziegiel, M. H., & Tabor, A. (2012). High levels of fetal DNA are associated with increased risk of spontaneous preterm delivery. Prenatal Diagnosis, 32, 840–845.PubMedGoogle Scholar
  80. 80.
    Rava RP, Srinivasan A, Sehnert AJ, Bianchi DW. (2013). Circulating fetal cell-free DNA fractions differ in autosomal aneuploidies and monosomy X. Clinical Chemistry Google Scholar
  81. 81.
    Majhail, S., Farnia, S., Carpenter, P., Champlin, R., Crawford, S., Marks, D., et al. (2015). Indications for Autologous and Allogeneic Hematopoietic Cell Transplantation: Guidelines from the American Society for Blood and Marrow Transplantation. Biology of Blood and Marrow Transplantation, xxx–xx7.Google Scholar

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Authors and Affiliations

  1. 1.Research Center for Functional Genomics, Biomedicine and Translational Medicine“Iuliu Hatieganu” University of Medicine and PharmacyCluj-NapocaRomania

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