How does variability of immune system genes affect placentation?

Placenta

Volumn 32, Issue 8, 2011, Pages 539-545

  Colucci, F ^a,b,c   Boulenouar, S ^a,b,c   Kieckbusch, J ^a,b,c   Moffett, A ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b NIHR Cambridge Biomedical Research Centre   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Killer cell immunoglobulin like receptors (KIR); Ly49 receptors; Major histocompatibility complex (MHC); Pregnancy; Trophoblast; Uterine Natural Killer (uNK) cells

Indexed keywords

CD94 ANTIGEN; HLA C ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; NATURAL KILLER CELL LECTIN LIKE RECEPTOR; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A; NATURAL KILLER CELL RECEPTOR;

DNA POLYMORPHISM; GENE CLUSTER; GENETIC VARIABILITY; HUMAN; IMMUNE SYSTEM; IMMUNOGENETICS; INTRAUTERINE GROWTH RETARDATION; LYMPHOCYTE FUNCTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOTHER FETUS RELATIONSHIP; NATURAL KILLER CELL; NONHUMAN; PLACENTA DEVELOPMENT; PREECLAMPSIA; PRIORITY JOURNAL; REPRODUCTION; REVIEW; RISK ASSESSMENT; SPONTANEOUS ABORTION; TROPHOBLAST;

EID: 79960601633     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2011.05.001     Document Type: Article

References (70)

1. A. Moffett, and C. Loke Immunology of placentation in eutherian mammals Nat Rev Immunol 6 2006 584 594 (Pubitemid 44134091)
2. F. Colucci, M.A. Caligiuri, and J.P. Di Santo What does it take to make a natural killer? Nat Rev Immunol 3 2003 413 425 (Pubitemid 37323201)
3. A. Moffett-King Natural killer cells and pregnancy Nat Rev Immunol 2 2002 656 663 (Pubitemid 37328723)
4. L.A. Koopman, H.D. Kopcow, B. Rybalov, J.L. Boyson, J.S. Orange, and F. Schatz Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential J Exp Med 198 2003 1201 1212 (Pubitemid 37323385)
5. G.E. Lash, B. Schiessl, M. Kirkley, B.A. Innes, A. Cooper, and R.F. Searle Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy J Leukoc Biol 80 2006 572 580 (Pubitemid 44835791)
6. J. Hanna, D. Goldman-Wohl, Y. Hamani, I. Avraham, C. Greenfield, and S. Natanson-Yaron Decidual NK cells regulate key developmental processes at the human fetal-maternal interface Nat Med 12 2006 1065 1074 (Pubitemid 44353388)
7. A.A. Ashkar, J.P. Di Santo, and B.A. Croy Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy J Exp Med 192 2000 259 270
8. R. Pijnenborg, L. Vercruysse, and M. Hanssens The uterine spiral arteries in human pregnancy: facts and controversies Placenta 27 2006 939 958 (Pubitemid 44204033)
9. S.E. Hiby, A. King, A.M. Sharkey, and Y.W. Loke 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 Mol Immunol 34 1997 419 430 (Pubitemid 27368338)
10. S. Verma, A. King, and Y.W. Loke Expression of killer cell inhibitory receptors on human uterine natural killer cells Eur J Immunol 27 1997 979 983 (Pubitemid 27153669)
11. A.M. Sharkey, L. Gardner, S. Hiby, L. Farrell, R. Apps, and L. Masters Killer Ig-like receptor expression in uterine NK cells is biased toward recognition of HLA-C and alters with gestational age J Immunol 181 2008 39 46
12. R. Apps, S.P. Murphy, R. Fernando, L. Gardner, T. Ahad, and A. Moffett Human leucocyte antigen (HLA) expression of primary trophoblast cells and placental cell lines, determined using single antigen beads to characterize allotype specificities of anti-HLA antibodies Immunology 127 2009 26 39
13. R.D. Emes, L. Goodstadt, E.E. Winter, and C.P. Ponting Comparison of the genomes of human and mouse lays the foundation of genome zoology Hum Mol Genet 12 2003 701 709 (Pubitemid 36416957)
14. J. Kelley, and J. Trowsdale Features of MHC and NK gene clusters Transpl Immunol 14 2005 129 134 (Pubitemid 40848517)
15. S.E. Hiby, L. Regan, W. Lo, L. Farrell, M. Carrington, and A. Moffett Association of maternal killer-cell immunoglobulin-like receptors and parental HLA-C genotypes with recurrent miscarriage Hum Reprod 23 2008 972 976
16. P. Parham, and L.A. Guethlein Pregnancy immunogenetics: NK cell education in the womb? J Clin Invest 120 2010 3801 3804
17. S.E. Hiby, J.J. Walker, K.M. O'Shaughnessy, C.W. Redman, M. Carrington, and J. Trowsdale Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success J Exp Med 200 2004 957 965 (Pubitemid 39431121)
18. S.E. Hiby, R. Apps, A.M. Sharkey, L.E. Farrell, L. Gardner, and A. Mulder Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2 J Clin Invest 120 2010 4102 4110
19. E.A. Steegers, P. von Dadelszen, J.J. Duvekot, and R. Pijnenborg Pre-eclampsia Lancet 376 2010 631 644
20. T.Y. Khong, F. De Wolf, W.B. Robertson, and I. Brosens Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants Br J Obstet Gynaecol 93 1986 1049 1059 (Pubitemid 16004866)
21. Y.M. Kim, E. Bujold, T. Chaiworapongsa, R. Gomez, B.H. Yoon, and H.T. Thaler Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes Am J Obstet Gynecol 189 2003 1063 1069 (Pubitemid 37373899)
22. E. Jauniaux, and G.J. Burton Pathophysiology of histological changes in early pregnancy loss Placenta 26 2005 114 123 (Pubitemid 40246999)
23. T.Y. Khong, H.S. Liddell, and W.B. Robertson Defective haemochorial placentation as a cause of miscarriage: a preliminary study Br J Obstet Gynaecol 94 1987 649 655 (Pubitemid 17093781)
24. J.N. Bulmer, L. Morrison, M. Longfellow, A. Ritson, and D. Pace Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies Hum Reprod 6 1991 791 798
25. P. Vacca, C. Cantoni, M. Vitale, C. Prato, F. Canegallo, and D. Fenoglio Crosstalk between decidual NK and CD14+ myelomonocytic cells results in induction of Tregs and immunosuppression Proc Natl Acad Sci U S A 107 2010 11918 11923
26. J. Hempstock, T. Cindrova-Davies, E. Jauniaux, and G.J. Burton Endometrial glands as a source of nutrients, growth factors and cytokines during the first trimester of human pregnancy: a morphological and immunohistochemical study Reprod Biol Endocrinol 2 2004 58
27. A.A. Ashkar, G.P. Black, Q. Wei, H. He, L. Liang, and J.R. Head Assessment of requirements for IL-15 and IFN regulatory factors in uterine NK cell differentiation and function during pregnancy J Immunol 171 2003 2937 2944 (Pubitemid 37093515)
28. E.M. Barber, and J.W. Pollard The uterine NK cell population requires IL-15 but these cells are not required for pregnancy nor the resolution of a Listeria monocytogenes infection J Immunol 171 2003 37 46 (Pubitemid 36745271)
29. P. Georgiades, A.C. Ferguson-Smith, and G.J. Burton Comparative developmental anatomy of the murine and human definitive placentae Placenta 23 2002 3 19 (Pubitemid 41110436)
30. J.C. Cross, D. Baczyk, N. Dobric, M. Hemberger, M. Hughes, and D.G. Simmons Genes, development and evolution of the placenta Placenta 24 2003 123 130 (Pubitemid 37184707)
31. Z. Madeja, H. Yadi, R. Apps, S. Boulenouar, S.J. Roper, and L. Gardner Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth Proc Natl Acad Sci U S A 2011
32. H. Yadi, S. Burke, Z. Madeja, M. Hemberger, A. Moffett, and F. Colucci Unique receptor repertoire in mouse uterine NK cells J Immunol 181 2008 6140 6147
33. T.V. Mallidi, L.E. Craig, S.R. Schloemann, and J.K. Riley Murine endometrial and decidual NK1.1+ natural killer cells display a B220+CD11c+ cell surface phenotype Biol Reprod 81 2009 310 318
34. J. Zhang, Z. Chen, G.N. Smith, and B.A. Croy Natural killer cell-triggered vascular transformation: maternal care before birth? Cell Mol Immunol 8 2010 1 11
35. E.N. Sanchez-Rodriguez, S. Nava-Salazar, C.A. Mendoza-Rodriguez, C. Moran, J.F. Romero-Arauz, and E. Ortega Persistence of decidual NK cells and KIR genotypes in healthy pregnant and preeclamptic women: a case-control study in the third trimester of gestation Reprod Biol Endocrinol 9 2011 8
36. C. Wang, T. Tanaka, H. Nakamura, N. Umesaki, K. Hirai, and O. Ishiko Granulated metrial gland cells in the murine uterus: localization, kinetics, and the functional role in angiogenesis during pregnancy Microsc Res Tech 60 2003 420 429 (Pubitemid 36184296)
37. R. Barten, M. Torkar, A. Haude, J. Trowsdale, and M.J. Wilson Divergent and convergent evolution of NK-cell receptors Trends Immunol 22 2001 52 57 (Pubitemid 32675282)
38. J.R. Carlyle, A. Mesci, J.H. Fine, P. Chen, S. Belanger, and L.H. Tai Evolution of the Ly49 and Nkrp1 recognition systems Semin Immunol 20 2008 321 330
39. S. Johansson, M. Salmon-Divon, M.H. Johansson, Y. Pickman, P. Brodin, and K. Karre Probing natural killer cell education by Ly49 receptor expression analysis and computational modelling in single MHC class I mice PLoS One 4 2009 e6046
40. Ensembl. Mus Musculus: Chromosome 7: 1-1. http://www.ensembl.org/Mus- musculus/Location/Chromosome?r=7. 15.02.2011.
41. Ensembl. Mus Musculus: Chromosome 6: 1-1. http://www.ensembl.org/Mus- musculus/Location/Chromosome?r=6. 15.02.2011.
42. Ensembl. Homo Sapiens: Chromosome 19: 1-1. http://www.ensembl.org/Homo- sapiens/Location/Chromosome?r=19. 15.03.2011.
43. Ensembl. Homo Sapiens: Chromosome 12: 1-1. http://www.ensembl.org/Homo- sapiens/Location/Chromosome?r=12. 15.03.2011.
44. F. Colucci, J.P. Di Santo, and P.J. Leibson Natural killer cell activation in mice and men: different triggers for similar weapons? Nat Immunol 3 2002 807 813
45. P. Parham MHC class I molecules and KIRs in human history, health and survival Nat Rev Immunol 5 2005 201 214 (Pubitemid 40364822)
46. L. Abi-Rached, A.K. Moesta, R. Rajalingam, L.A. Guethlein, and P. Parham Human-specific evolution and adaptation led to major qualitative differences in the variable receptors of human and chimpanzee natural killer cells PLoS Genet 6 2010 e1001192
47. V. Pascal, M.J. Stulberg, and S.K. Anderson Regulation of class I major histocompatibility complex receptor expression in natural killer cells: one promoter is not enough! Immunol Rev 214 2006 9 21 (Pubitemid 44707898)
48. J.A. Yoder, and G.W. Litman The phylogenetic origins of natural killer receptors and recognition: relationships, possibilities, and realities Immunogenetics 63 2011 123 141
49. T. Sasazuki, T. Juji, Y. Morishima, N. Kinukawa, H. Kashiwabara, and H. Inoko Effect of matching of class I HLA alleles on clinical outcome after transplantation of hematopoietic stem cells from an unrelated donor. Japan Marrow Donor Program N Engl J Med 339 1998 1177 1185 (Pubitemid 28482126)
50. C. Ohlen, G. Kling, P. Hoglund, M. Hansson, G. Scangos, and C. Bieberich Prevention of allogeneic bone marrow graft rejection by H-2 transgene in donor mice Science 246 1989 666 668 (Pubitemid 19283359)
51. Y.Y. Yu, V. Kumar, and M. Bennett Murine natural killer cells and marrow graft rejection Annu Rev Immunol 10 1992 189 213
52. J. Trowsdale, and A. Moffett NK receptor interactions with MHC class I molecules in pregnancy Semin Immunol 20 2008 317 320
53. H. El Costa, A. Casemayou, M. Aguerre-Girr, M. Rabot, A. Berrebi, and O. Parant Critical and differential roles of NKp46- and NKp30-activating receptors expressed by uterine NK cells in early pregnancy J Immunol 181 2008 3009 3017
54. R. Apps, L. Gardner, and A. Moffett A critical look at HLA-G Trends Immunol 29 2008 313 321
55. L.L. Lanier Evolutionary struggles between NK cells and viruses Nat Rev Immunol 8 2008 259 268 (Pubitemid 351432802)
56. P. Parham The genetic and evolutionary balances in human NK cell receptor diversity Semin Immunol 20 2008 311 316
57. P. Brodin, K. Karre, and P. Hoglund NK cell education: not an on-off switch but a tunable rheostat Trends Immunol 30 2009 143 149
58. A.K. Moesta, P.J. Norman, M. Yawata, N. Yawata, M. Gleimer, and P. Parham Synergistic polymorphism at two positions distal to the ligand-binding site makes KIR2DL2 a stronger receptor for HLA-C than KIR2DL3 J Immunol 180 2008 3969 3979
59. T. Graef, A.K. Moesta, P.J. Norman, L. Abi-Rached, L. Vago, and A.M. Older Aguilar KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A11 while diminishing avidity for HLA-C J Exp Med 206 2009 2557 2572
60. G.V. Quinnan, and J.E. Manischewitz The role of natural killer cells and antibody-dependent cell-mediated cytotoxicity during murine cytomegalovirus infection J Exp Med 150 1979 1549 1554 (Pubitemid 10168604)
61. H.G. Ljunggren, and K. Karre Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism J Exp Med 162 1985 1745 1759 (Pubitemid 16149673)
62. M.J. Bilinski, J.G. Thorne, M.J. Oh, S. Leonard, C. Murrant, and C. Tayade Uterine NK cells in murine pregnancy Reprod Biomed Online 16 2008 218 226 (Pubitemid 351291968)
63. D.J. Barker, J.G. Eriksson, T. Forsen, and C. Osmond Fetal origins of adult disease: strength of effects and biological basis Int J Epidemiol 31 2002 1235 1239 (Pubitemid 36204489)
64. J.C. Sun, S. Lopez-Verges, C.C. Kim, J.L. Derisi, and L.L. Lanier NK cells and immune "memory J Immunol 186 2011 1891 1897
65. R. Skjaerven, A.J. Wilcox, and R.T. Lie The interval between pregnancies and the risk of preeclampsia New Engl J Med 346 2002 33 38 (Pubitemid 34438917)
66. S.I. Khakoo, C.L. Thio, M.P. Martin, C.R. Brooks, X. Gao, and J. Astemborski HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection Science 305 2004 872 874 (Pubitemid 39038423)
67. S. Knapp, U. Warshow, D. Hegazy, L. Brackenbury, I.N. Guha, and A. Fowell Consistent beneficial effects of killer cell immunoglobulin-like receptor 2DL3 and group 1 human leukocyte antigen-C following exposure to hepatitis C virus Hepatology 51 2010 1168 1175
68. J. Rolff, and M.T. Siva-Jothy Invertebrate ecological immunology Science 301 2003 472 475 (Pubitemid 36900296)
69. K. Gendzekhadze, P.J. Norman, L. Abi-Rached, T. Graef, A.K. Moesta, and Z. Layrisse Co-evolution of KIR2DL3 with HLA-C in a human population retaining minimal essential diversity of KIR and HLA class I ligands Proc Natl Acad Sci U S A 106 2009 18692 18697
70. A.L. Graham, A.D. Hayward, K.A. Watt, J.G. Pilkington, J.M. Pemberton, and D.H. Nussey Fitness correlates of heritable variation in antibody responsiveness in a wild mammal Science 330 2010 662 665