Natural killer cells and pregnancy (original) (raw)

• Beer, A. E. & Billingham, R. E. The Immunobiology of Mammalian Reproduction (Prentice–Hall, New Jersey, USA, 1976).
  Google Scholar
• Loke, Y. W. & King, A. Human Implantation: Cell Biology and Immunology (Cambridge University Press, Cambridge, UK, 1995).
  Google Scholar
• King, A., Burrows, T., Verma, S., Hiby, S. & Loke, Y. W. Human uterine lymphocytes. Hum. Reprod. Update 4, 480–485 (1998).References 2 and 3 provide detailed background information on the cellular relationships that occur during placentation.
  CAS PubMed Google Scholar
• Trowsdale, J. Genetic and functional relationships between MHC and NK receptor genes. Immunity 15, 363–374 (2001).A concise and comprehensive review of MHC and NK-cell receptor genes.
  CAS PubMed Google Scholar
• Pijnenborg, R., Bland, J. M., Robertson, W. B. & Brosens, I. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 4, 397–414 (1983).
  CAS PubMed Google Scholar
• Pijnenborg, R. Trophoblast invasion. Reprod. Med. Rev. 3, 53–73 (1994).A detailed review of how placental cells invade maternal arteries.
  Google Scholar
• Brosens, I. A. Morphological changes in the utero-placental bed in pregnancy hypertension. Clin. Obstet. Gynaecol. 4, 573–593 (1977).
  CAS PubMed Google Scholar
• Khong, T. Y., De Wolf, F., Robertson, W. B. & Brosens, I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br. J. Obstet. Gynaecol. 93, 1049–1059 (1986).
  CAS PubMed Google Scholar
• King, A. Uterine leukocytes and decidualization. Hum. Reprod. Update 6, 28–36 (2000).
  CAS PubMed Google Scholar
• Gubbay, O., Critchley, H. O. D., King, A., Bowen, J. M. & Jabbour, H. N. Prolactin induces ERK phosphorylation in epithelial and CD56+ natural killer cells of the human endometrium. J. Clin. Endocrinol. Metab. 87, 2329–2335 (2002).
  CAS PubMed Google Scholar
• Dunn, C. L., Critchley, H. O. D. & Kelly, R. W. IL-15 regulation in human endometrial stromal cells. J. Clin. Endocrinol. Metab. 87, 1898–1901 (2002).
  CAS PubMed Google Scholar
• Spornitz, U. M. The functional morphology of the human endometrium and decidua. Adv. Anat. Embryol. Cell Biol. 124, 1–99 (1992).
  CAS PubMed Google Scholar
• Li, X. F. et al. Angiogenic growth factor mRNAs in uterine natural killer cells. J. Clin. Endocrinol. Metab. 86, 1823–1834 (2001).
  CAS PubMed Google Scholar
• Wheeler, J. E., Gersell, D. J. & Kraus, F. T. in Blaustein's Pathology of the Female Genital Tract (ed. Kurman, R. J.) 630–633 & 1111–1113 (Springer, New York, 2002).
  Google Scholar
• Ellis, S. A., Palmer, M. S. & McMichael, A. J. Human trophoblast and the choriocarcinoma cell line BeWo express a truncated HLA class I molecule. J. Immunol. 144, 731–735 (1990).
  CAS PubMed Google Scholar
• Kovats, S. et al. A class I antigen, HLA-G, expressed in human trophoblasts. Science 248, 220–223 (1990).
  CAS PubMed Google Scholar
• King, A., Boocock, C., Sharkey, A., Gardner, L. & Loke, Y. W. Evidence for the expression of HLA-C class I mRNA and protein by human first trimester trophoblast. J. Immunol. 156, 2068–2076 (1996).
  CAS PubMed Google Scholar
• King, A. et al. Surface expression of HLA-C antigen by human extravillous trophoblast. Placenta 21, 376–387 (2000).
  CAS PubMed Google Scholar
• Taruscio, D. & Mantovani, A. Human endogenous retroviral sequences: possible roles in reproductive physiopathology. Biol. Reprod. 59, 713–724 (1998).
  CAS PubMed Google Scholar
• Harris, J. R. Placental endogenous retrovirus (ERV): structural, functional and evolutionary significance. BioEssays 20, 307–316 (1998).
  CAS PubMed Google Scholar
• Loke, Y. W. in Immunology of Pregnancy and its Disorders (ed. Stern, C.) 61–89 (Kluwer Academic Publishers, Dordrecht, The Netherlands, 1988).
  Google Scholar
• Brummer, J. et al. Interaction of the cell adhesion molecule CEACAM1 with integrin-β3. Am. J. Pathol. 159, 537–546 (2001).
  CAS PubMed PubMed Central Google Scholar
• Braud, V. M. et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391, 795–799 (1998).
  CAS PubMed Google Scholar
• Lee, N. et al. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl Acad. Sci. USA 95, 5199–5204 (1998).
  CAS PubMed PubMed Central Google Scholar
• Boyington, J. C., Brooks, A. G. & Sun, P. D. Structure of killer cell immunoglobulin-like receptors and their recognition of the class I MHC molecules. Immunol. Rev. 181, 52–65 (2001).
  Google Scholar
• Long, E. O. et al. Inhibition of natural killer cell activation signals by killer cell immunoglobulin-like receptors (CD158). Immunol. Rev. 181, 223–233 (2001).
  CAS PubMed Google Scholar
• Vilches, C. & Parham, P. KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu. Rev. Immunol. 20, 217–251 (2002).A comprehensive review of KIR genes.
  CAS PubMed Google Scholar
• King, A. et al. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur. J. Immunol. 30, 1623–1631 (2000).
  CAS PubMed Google Scholar
• Haedicke, W. et al. Expression of CD94/NKG2A and killer immunoglobulin-like receptors in NK cells and a subset of extranodal cytotoxic T-cell lymphomas. Blood 95, 3628–3630 (2000).
  CAS PubMed Google Scholar
• Llano, M. et al. HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur. J. Immunol. 28, 2854–2863 (1998).
  CAS PubMed Google Scholar
• Vales-Gomez, M., Reburn, H. T., Erskine, R. A., Lopez-Botet, M. & Strominger, J. L. Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/NKG2-C to HLA-E. EMBO J. 18, 4250–4260 (1999).
  CAS PubMed PubMed Central Google Scholar
• McMaster, M. et al. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J. Immunol. 154, 3771–3778 (1995).
  CAS PubMed Google Scholar
• Loke, Y. W. et al. Evaluation of trophoblast HLA-G antigen with a specific monoclonal antibody. Tissue Antigens 50, 135–146 (1997).
  CAS PubMed Google Scholar
• Suarez, M. B. et al. A new HLA-G allele (HLA-G*0105N) and its distribution in the Spanish population. Immunogenetics 45, 464–465 (1997).
  CAS PubMed Google Scholar
• Arnaiz-Villena, A. et al. The evolution of the MHC-G gene does not support a functional role for the complete protein. Immunol. Rev. 183, 65–75 (2001).
  CAS PubMed Google Scholar
• Uhrberg, M. et al. Human diversity in killer cell inhibitory genes. Immunity 7, 753–763 (1997).
  CAS PubMed Google Scholar
• Rajalingam, R., Gardiner, C. M., Canavez, F., Vilches, C. & Parham, P. Identification of seventeen novel KIR variants: fourteen of them from non-Caucasian donors. Tissue Antigens 57, 22–31 (2001).
  CAS PubMed Google Scholar
• Wilson, M. et al. Plasticity in the organisation and sequences of human KIT/ILKT families. Proc. Natl Acad. Sci. USA 97, 4778–4783 (2000).
  CAS PubMed PubMed Central Google Scholar
• Rajalingam, R. et al. Short KIR haplotypes in pygmy chimpanzee (bonobo) resemble the conserved framework of diverse human KIR haplotypes. J. Exp. Med. 193, 135–146 (2001).
  CAS PubMed PubMed Central Google Scholar
• Khakoo, S. I. et al. Rapid evolution of NK-cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12, 687–698 (2000).
  CAS PubMed Google Scholar
• Hiby, S. E., King, A., Sharkey, A. M. & Loke, Y. W. Human uterine 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, 419–430 (1997).
  CAS PubMed Google Scholar
• Verma, S., King, A. & Loke, Y. W. Expression of killer-cell inhibitory receptors (KIR) on human uterine NK cells. Eur. J. Immunol. 27, 979–983 (1997).
  CAS PubMed Google Scholar
• Valiante, N. M. et al. Functionally and structurally distinct NK-cell receptor repertoires in the peripheral blood of two human donors. Immunity 7, 739–751 (1997).
  CAS PubMed Google Scholar
• Jacobs, R. et al. CD56bright cells differ in their KIR repertoire and cytotoxic features from CD56dim NK cells. Eur. J. Immunol. 31, 3121–3126 (2001).
  CAS PubMed Google Scholar
• Lanier, L. L. Natural killer cells fertile with receptors for HLA-G? Proc. Natl Acad. Sci. USA 96, 5343–5345 (1999).
  CAS PubMed PubMed Central Google Scholar
• Rajagopalan, S. & Long, E. O. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J. Exp. Med. 189, 1093–1100 (1999).
  CAS PubMed PubMed Central Google Scholar
• Ponte, M. et al. Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, and HLA-G1-specific receptor. Proc. Natl Acad. Sci. USA 96, 5674–5679 (1999).
  CAS PubMed PubMed Central Google Scholar
• Rajagopalan, S., Fu, J. & Long, E. O. Induction of IFN-γ production but not cytotoxicity by the killer-cell Ig-like receptor KIR2DL4 (CD158d) in resting NK cells. J. Immunol. 167, 1877–1881 (2001).References 46–48 describe the expression and function of KIR2DL4.
  CAS PubMed Google Scholar
• Allan, D. S. J. et al. Tetrameric complexes of human histocompatibility leukocyte antigen (HLA-G) bind to peripheral-blood myelomonocytic cells. J. Exp. Med. 189, 1–7 (1999).
  Google Scholar
• Navarro, F. et al. NK-cell receptors respectively recognize HLA-G1 and HLA-E molecules co-expressed on target cells. Eur. J. Immunol. 29, 277–283 (1999).
  CAS PubMed Google Scholar
• Chang, C. C. et al. Tolerization of dendritic cells by Ts cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nature Immunol. 3, 237–243 (2002).
  CAS Google Scholar
• McMaster, M. et al. HLA-G isoforms produced by placental cytotrophoblasts and found in amniotic fluid are due to unusual glycosylation. J. Immunol. 160, 5922–5928.
• King, A. & Loke, Y. W. On the nature and function of human uterine granular lymphocytes. Immunol. Today 12, 432–435 (1991).
  CAS PubMed Google Scholar
• Avril, T. et al. Trophoblast cell line resistance to NK lysis mainly involves an HLA class-I-independent mechanism. J. Immunol. 162, 5902–5909 (1999).
  CAS PubMed Google Scholar
• Norwitz, E. R., Schust, D. J. & Fisher, S. J. Implantation and the survival of early pregnancy. N. Engl. J. Med. 345, 1400–1408 (2001).
  CAS PubMed Google Scholar
• Cooper, M. A., Fehniger, T. A. & Caligiuri, M. A. The biology of human natural killer-cell subsets. Trends Immunol. 22, 633–640 (2001).
  CAS PubMed Google Scholar
• King, A., Thomas, L. & Bischoff, P. Cell-culture models of trophoblast. II. Trophoblast cell lines — a workshop report. Trophoblast Res. 14, S113–S119 (2000).
  Google Scholar
• Sharkey, A. M. et al. Localization of leukemia inhibitory factor and its receptor in human placenta throughout pregnancy. Biol. Reprod. 60, 355–364 (1999).
  CAS PubMed Google Scholar
• Steven, D. H. Comparative Placentation, Essays in Structure and Function (Academic Press, London, 1975).
  Google Scholar
• Liu, C.-C. & Young, J. D.-E. Uterine natural killer cells in the pregnant uterus. Adv. Immunol. 79, 297–329 (2001).
  CAS PubMed Google Scholar
• Rossant, J. & Cross, J. C. Placental development: lessons from mouse mutants. Nature Rev. Genet. 2, 538–548 (2001).
  CAS PubMed Google Scholar
• Georgiades, P., Ferguson-Smith, A. C. & Burton, G. J. Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23, 3–19 (2002).
  CAS PubMed Google Scholar
• Chantakru, S. et al. Contributions from self-renewal and trafficking to the uterine NK-cell population of early pregnancy. J. Immunol. 168, 22–28 (2002).This article describes homing experiments of uterine NK cells in mice.
  CAS PubMed Google Scholar
• Kruse, A., Martens, N., Fernekorn, U., Hallmann, R. & Butcher, E. C. Alterations in the expression of homing-associated molecules at the maternal/fetal interface during the course of pregnancy. Biol. Reprod. 66, 333–345 (2002).
  CAS PubMed Google Scholar
• Burrows, T. D., King, A. & Loke, Y. W. Expression of adhesion molecules by endovascular trophoblast and decidual endothelial cells: implications for vascular invasion during implantation. Placenta 15, 21–33 (1994).
  CAS PubMed Google Scholar
• Burrows, T. D., King, A. & Loke, Y. W. Expression of adhesion molecules by human decidual large granular lymphocytes. Cell. Immunol. 147, 81–94 (1993).
  CAS PubMed Google Scholar
• Guimond, M.-J., Wang, B. & Croy, B. A. Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficit in natural killer cell-deficient tgɛ mice. J. Exp. Med. 187, 217–223 (1998).
  CAS PubMed PubMed Central Google Scholar
• Greenwood, J. D. et al. Ultrastructural studies of implantation sites from mice deficient in uterine natural killer cells. Placenta 21, 693–702 (2000).
  CAS PubMed Google Scholar
• Ashkar, A. A. & Croy, B. A. Functions of uterine natural killer cells are mediated by interferon-γ production during murine pregnancy. Semin. Immunol. 13, 235–241 (2001).This study describes changes in mice that are deficient in uterine NK cells.
  CAS PubMed Google Scholar
• Boyson, J. E., Iwanaga, K. K., Golos, R. G. & Watkins, D. I. Identification of the rhesus monkey HLA-G ortholog. Mamu-G is a pseudogene. J. Immunol. 157, 5428–5437 (1996).
  CAS PubMed Google Scholar
• Adams, E. J. & Parham, P. Species-specific evolution of MHC class I genes in the higher primates. Immunol. Rev. 183, 41–64 (2001).
  CAS PubMed Google Scholar
• Cooper, M. A. et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56bright subset. Blood 97, 3146–3151 (2001).
  CAS PubMed Google Scholar
• Gieselhart, A. et al. Comparative analysis of the phenotypes of decidual and peripheral blood large granular lymphocytes and T cells during early human pregnancy. Am. J. Reprod. Immunol. 33, 315–322 (1995).
  Google Scholar
• Schalhammer, L., Walcher, W., Wintersteiger, R., Dohr, G. & Sedlmayr, P. Phenotypic comparison of natural killer cells from peripheral blood and early pregnancy decidua. Early Pregnancy 3, 15–22 (1997).
  Google Scholar