The fetal allograft revisited: Does the study of an ancient invertebrate species shed light on the role of natural killer cells at the maternal-fetal interface?

Clinical and Developmental Immunology

Volumn 2008, Issue , 2008, Pages

  Lightner, Amy ^a   Schust, Danny J ^b   Chen, Yi Bin A ^c   Barrier, Breton F ^b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of Missouri   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOGRAFT; BOTRYLLUS SCHLOSSERI; CARDIOVASCULAR SYSTEM; CELL TYPE; CHIMERA; FETOMATERNAL TRANSFUSION; HUMAN; IMMUNE RESPONSE; INVERTEBRATE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR EVOLUTION; NATURAL KILLER CELL; NONHUMAN; PARASITISM; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TROPHOBLAST; UTERUS; ALLOTRANSPLANTATION; ANIMAL; CLASSIFICATION; FEMALE; FETUS; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; PREGNANCY; UROCHORDATA;

HLA ANTIGEN CLASS 1;

ANIMALS; CHIMERISM; FEMALE; FETUS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; MATERNAL-FETAL EXCHANGE; PREGNANCY; TRANSPLANTATION, HOMOLOGOUS; UROCHORDATA; UTERUS;

EID: 47349100390     PISSN: 17402522     EISSN: 17402530     Source Type: Journal    
DOI: 10.1155/2008/631920     Document Type: Review

References (85)

1. Medawar P. B., Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates Society for Experimental Biology, Evolution Symposium 1953 7 New York, NY, USA Academic Press 320 328
2. Sargent I. L., Maternal and fetal immune responses during pregnancy Experimental and Clinical Immunogenetics 1993 10 2 85 102
3. Tafuri A., Alferink J., Moller P., Hammerling G. J., Arnold B., T cell awareness of paternal alloantigens during pregnancy Science 1995 270 5236 630 633
4. Shao L., Jacobs A. R., Johnson V. V., Mayer L., Activation of CD8+ regulatory T cells by human placental trophoblasts The Journal of Immunology 2005 174 12 7539 7547
5. Adinolfi M., The maternal-fetal interaction: some controversies and solutions Experimental and Clinical Immunogenetics 1993 10 2 103 117
6. Damber M. G., von Schoultz B., Stigbrand T., The immunological paradox of pregnancy Acta Obstetricia et Gynecologica Scandinavica. Supplement 1977 66 39 47
7. Rast J. P., Anderson M. K., Strong S. J., Luer C., Litman R. T., Litman G. W., α, β, γ, and δ T cell antigen receptor genes arose early in vertebrate phylogeny Immunity 1997 6 1 1 11
8. Rinkevich B., The colonial urochordate Botryllus schlosseri: from stem cells and natural tissue transplantation to issues in evolutionary ecology BioEssays 2002 24 8 730 740
9. Rinkevich B., Yankelevich I., Environmental split between germ cell parasitism and somatic cell synergism in chimeras of a colonial urochordate Journal of Experimental Biology 2004 207 20 3531 3536
10. Ballarin L., Dall'Oro M., Bertotto D., Libertini A., Francescon A., Barbaro A., Haematological parameters in Umbrina cirrosa (Teleostei, Sciaenidae): a comparison between diploid and triploid specimens Comparative Biochemistry and Physiology Part A 2004 138 1 45 51
11. Saito Y., Watanabe H., Colony specificity in the compound ascidian, Botryllus schlosseri Proceedings of the Japan Academy. Series B 1982 58 4 105 108
12. Cima F., Sabbadin A., Ballarin L., Cellular aspects of allorecognition in the compound ascidian Botryllus schlosseri Developmental & Comparative Immunology 2004 28 9 881 889
13. Weissman I. L., Saito Y., Rinkevich B., Allorecognition histocompatibility in a protochordate species: is the relationship to MHC somatic or structural? Immunological Reviews 1990 113 227 241
14. Rinkevich B., Primitive immune systems: are your ways my ways? Immunological Reviews 2004 198 1 25 35
15. Saito Y., Hirose E., Watanabe H., Allorecognition in compound ascidians International Journal of Developmental Biology 1994 38 2 237 247
16. Oka H., Watanabe H., Problems of colony specificity in compound ascidians The Bulletin of the Marine Biological Station of Asamushi 1960 10 153 155
17. Sabbadin A., Coloniality in ascidians and its adaptive value, with special reference to Botryllus schlosseri Animal Biology 1994 3 157 163
18. Grosberg R. K., Quinn J. F., The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate Nature 1986 322 6078 456 459
19. Rinkevich B., Weissman I. L., Incidents of rejection and indifference in Fu/HC incompatible protochordate colonies Journal of Experimental Zoology 1992 263 1 105 111
20. Cima F., Ballarin L., Gasparini F., Burighel P., External amebocytes guard the pharynx entry in a tunicate (Ascidiacea) Developmental & Comparative Immunology 2006 30 5 463 472
21. Ballarin L., Cima F., Cytochemical properties of Botryllus schlosseri haemocytes: indications for morpho-functional characterisation European Journal of Histochemistry 2005 49 3 255 264
22. Ballarin L., Cima F., Sabbadin A., Histoenzymatic staining and characterization of the colonial ascidian Botryllus schlosseri hemocites Bollettino di Zoologia 1993 60 1 19 24
23. Ballarin L., Franchini A., Ottaviani E., Sabbadin A., Morula cells as the major immunomodulatory hemocytes in ascidians: evidences from the colonial species Botryllus schlosseri Biological Bulletin 2001 201 1 59 64
24. Cima F., Sabbadin A., Ballarin L., Cellular aspects of allorecognition in the compound ascidian Botryllus schlosseri Developmental & Comparative Immunology 2004 28 9 881 889
25. Peddie C. M., Smith V. J., 'Lymphocyte-like' cells in ascidians precursors for vertebrate lymphocytes? Fish & Shellfish Immunology 1995 5 8 613 629
26. Marchalonis J. J., Schluter S. F., On the relevance of invertebrate recognition and defence mechanisms to the emergence of the immune response of vertebrates Scandinavian Journal of Immunology 1990 32 1 13 20
27. Danska J. S., McIntyre B. W., McDevitt H. O., Weissman I. L., Structural similarity between a primitive chordate membrane heterodimer and lymphocyte antigen receptors International Immunology 1990 2 9 795 802
28. Sabbadin A., Zaniolo G., Sexual differentiation and germ transfer in the colonial ascidian Botryllus schlosseri Journal of Experimental Zoology 1979 207 289 304
29. Stoner D. S., Weissman I. L., Somatic and germ cell parasitism in a colonial ascidian: possible role for a highly polymorphic allorecognition system Proceedings of the National Academy of Sciences of the United States of America 1996 93 26 15254 15259
30. Magor B. G., De Tomaso A., Rinkevich B., Weissman I. L., Allorecognition in colonial tunicates: protection against predatory cell lineages? Immunological Reviews 1999 167 1 69 79
31. Stoner D. S., Rinkevich B., Weissman I. L., Heritable germ and somatic cell lineage competitions in chimeric colonial protochordates Proceedings of the National Academy of Sciences of the United States of America 1999 96 16 9148 9153
32. Delsuc F., Brinkmann H., Chourrout D., Philippe H., Tunicates and not cephalochordates are the closest living relatives of vertebrates Nature 2006 439 7079 965 968
33. Cadavid L. F., Powell A. E., Nicotra M. L., Moreno M., Buss L. W., An invertebrate histocompatibility complex Genetics 2004 167 1 357 365
34. Mokady O., Buss L. W., Transmission genetics of allorecognition in Hydractinia symbiolongicarpus (Cnidaria: Hydrozoa) Genetics 1996 143 2 823 827
35. Powell A. E., Nicotra M. L., Moreno M. A., Lakkis F. G., Dellaporta S. L., Buss L. W., Differential effect of allorecognition loci on phenotype in Hydractinia symbiolongicarpus (Cnidaria: Hydrozoa) Genetics 2007 177 4 2101 2107
36. Benirschke K., Kaufman P., Pathology of the Human Placenta 1990 New York, NY, USA Springer
37. Rinkevich B., Immunology of human implantation: from the invertebrates' point of view Human Reproduction 1998 13 2 455 459
38. Raulet D. H., Development and tolerance of natural killer cells Current Opinion in Immunology 1999 11 2 129 134
39. Loke Y. W., King A., Immunology of human implantation: an evolutionary perspective Human Reproduction 1996 11 2 283 286
40. King A., Burrows T., Loke Y. W., Human uterine natural killer cells Natural Immunity 1996 15 1 41 52
41. Lanier L. L., NK cell receptors Annual Review of Immunology 1998 16 359 393
42. Bryceson Y. T., March M. E., Ljunggren H.-G., Long E. O., Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion Blood 2006 107 1 159 166
43. Moretta L., Mingari M. C., Bottino C., Pende D., Biassoni R., Moretta A., Cellular and molecular basis of natural killer and natural killer-like activity Immunology Letters 2003 88 2 89 93
44. Bulmer J. N., Morrison L., Longfellow M., Ritson A., Pace D., Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies Human Reproduction 1991 6 6 791 798
45. Ritson A., Bulmer J. N., Endometrial granulocytes in human decidua react with a natural-killer (NK) cell marker, NKH1 Immunology 1987 62 2 329 331
46. Dosiou C., Giudice L. C., Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives Endocrine Reviews 2005 26 1 44 62
47. Hiby S. E., King A., Sharkey A. M., Loke Y. W., Human uterine NK cells have a similar repertoire of killer inhibitory and activatory receptors to those found in blood, as demonstrated by RT-PCR and sequencing Molecular Immunology 1997 34 5 419 430
48. Scaife P. J., Searle R. F., Bulmer J. N., Robson S. C., Innes B. A., Searle R. F., Effector activity of decidual CD8+ lymphocytes in early human pregnancy Biology of Reproduction 2006 75 4 562 567
49. Whitelaw P. F., Croy B. A., Granulated lymphocytes of pregnancy Placenta 1996 17 8 533 543
50. Trundley A., Moffett A., Human uterine leukocytes and pregnancy Tissue Antigens 2004 63 1 1 12
51. Faulk W. P., Temple A., Distribution of β 2 microglobulin and HLA in chorionic villi of human placentae Nature 1976 262 5571 799 802
52. Lala P. K., Kearns M., Colavincenzo V., Cells of the fetomaternal interface: their role in the maintenance of viviparous pregnancy American Journal of Anatomy 1984 170 3 501 517
53. Furman M. H., Ploegh H. L., Schust D. J., Can viruses help us to understand and classify the MHC class I molecules at the maternal-fetal interface? Human Immunology 2000 61 11 1169 1176
54. Kovats S., Main E. K., Librach C., Stubblebine M., Fisher S. J., DeMars R., A class I antigen, HLA-G, expressed in human trophoblasts Science 1990 248 4952 220 223
55. Loke Y. W., King A., Immunology of human placental implantation: clinical implications of our current understanding Molecular Medicine Today 1997 3 4 153 159
56. Huddleston H., Schust D. J., Immune interactions at the maternal-fetal interface: a focus on antigen presentation American Journal of Reproductive Immunology 2004 51 4 283 289
57. Cohen G. B., Gandhi R. T., Davis D. M., The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells Immunity 1999 10 6 661 671
58. Tortorella D., Gewurz B. E., Furman M. H., Schust D. J., Ploegh H. L., Viral subversion of the immune system Annual Review of Immunology 2000 18 861 926
59. Biassoni R., Cantoni C., Marras D., Human natural killer cell receptors: insights into their molecular function and structure Journal of Cellular and Molecular Medicine 2003 7 4 376 387
60. King A., Allan D. S. J., Bowen M., HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells European Journal of Immunology 2000 30 6 1623 1631
61. Mandelboim O., Reyburn H. T., Sheu E. G., The binding site of NK receptors on HLA-C molecules Immunity 1997 6 3 341 350
62. Clements C. S., Kjer-Nielsen L., Kostenko L., Crystal structure of HLA-G: a nonclassical MHC class I molecule expressed at the fetal-maternal interface Proceedings of the National Academy of Sciences of the United States of America 2005 102 9 3360 3365
63. Rajagopalan S., Long E. O., A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells Journal of Experimental Medicine 1999 189 7 1093 1100
64. Rouas-Freiss N., Gonçalves R. M.-B., Menier C., Dausset J., Carosella E. D., Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis Proceedings of the National Academy of Sciences of the United States of America 1997 94 21 11520 11525
65. Yokoyama W. M., The mother-child union: the case of missing-self and protection of the fetus Proceedings of the National Academy of Sciences of the United States of America 1997 94 12 5998 6000
66. Le Bouteiller P., Pizzato N., Barakonyi A., Solier C., HLA-G, pre-eclampsia, immunity and vascular events Journal of Reproductive Immunology 2003 59 2 219 234
67. Goldman-Wohl D. S., Ariel I., Greenfield C., Lack of human leukocyte antigen-G expression in extravillous trophoblasts is associated with pre-eclampsia Molecular Human Reproduction 2000 6 1 88 95
68. Jokhi P. P., King A., Loke Y. W., Production of granulocyte-macrophage colony-stimulatmg factor by human trophoblast cells and by decidual large granular lymphocytes Human Reproduction 1994 9 9 1660 1669
69. Jokhi P. P., King A., Loke Y. W., Cytokine production and cytokine receptor expression by cells of the human first trimester placental-uterine interface Cytokine 1997 9 2 126 137
70. Rieger L., Hofmeister V., Probe C., Th1- and Th2-like cytokine production by first trimester decidual large granular lymphocytes is influenced by HLA-G and HLA-E Molecular Human Reproduction 2002 8 3 255 261
71. Li X. F., Charnock-Jones D. S., Zhang E., Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells The Journal of Clinical Endocrinology & Metabolism 2001 86 4 1823 1834
72. Guimond M.-J., Luross J. A., Wang B., Terhorst C., Danial S., Croy B. A., Absence of natural killer cells during murine pregnancy is associated with reproductive compromise in TgE26 mice Biology of Reproduction 1997 56 1 169 179
73. Guimond M.-J., Wang B., Croy B. A., Immune competence involving the natural killer cell lineage promotes placental growth Placenta 1999 20 5-6 441 450
74. Ashkar A. A., Di Santo J. P., Croy B. A., Interferon γ contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy Journal of Experimental Medicine 2000 192 2 259 269
75. Dunk C., Shams M., Nijjar S., Angiopoietin-1 and angiopoietin-2 activate trophoblast Tie-2 to promote growth and migration during placental development American Journal of Pathology 2000 156 6 2185 2199
76. Bauer S., Pollheimer J., Hartmann J., Husslein P., Aplin J. D., Knöfler M., Tumor necrosis factor- α inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures The Journal of Clinical Endocrinology & Metabolism 2004 89 2 812 822
77. Otun H. A., Lash G. E., Bulmer J. N., Searle R. F., Robson S. C., Inhibition of first trimester human extravillous trophoblast invasion by TNF- α and IFN- γ Placenta 2003 24 A67
78. Graham C. H., Connelly I., MacDougall J. R., Kerbel R. S., Stetler-Stevenson W. G., Lala P. K., Resistance of malignant trophoblast cells to both the anti-proliferative and anti-invasive effects of transforming growth factor- β Experimental Cell Research 1994 214 1 93 99
79. Lash G. E., Otun H. A., Innes B. A., Bulmer J. N., Searle R. F., Robson S. C., Inhibition of trophoblast cell invasion by TGFB1, 2, and 3 is associated with a decrease in active proteases Biology of Reproduction 2005 73 2 374 381
80. Menin A., del Favero M., Cima F., Ballarin L., Release of phagocytosis-stimulating factor(s) by morula cells in a colonial ascidian Marine Biology 2005 148 2 225 230
81. Ballarin L., Menin A., Franchi N., Bertoloni G., Cima F., Morula cells and non-self recognition in the compound ascidian Botryllus schlosseri Invertebrate Survival Journal 2005 2 1 1 5
82. De Tomaso A. W., Weissman I. L., Initial characterization of a protochordate histocompatibility locus Immunogenetics 2003 55 7 480 490
83. Boyson J. E., Iwanaga K. K., Golos T. G., Watkins D. I., Identification of a novel MHC class I gene, Mamu-AG, expressed in the placenta of a primate with an inactivated G locus The Journal of Immunology 1997 159 7 3311 3321
84. Bainbridge D. R., Evolution of mammalian pregnancy in the presence of the maternal immune system Reviews of Reproduction 2000 5 2 67 74
85. Lawlor D. A., Warren E., Taylor P., Parham P., Gorilla class I major histocompatibility complex alleles: comparison to human and chimpanzee class I Journal of Experimental Medicine 1991 174 6 1491 1509