The role of the maternal immune system in the regulation of human birthweight

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1663, 2015, Pages

  Moffett, Ashley ^a   Hiby, Susan E ^a   Sharkey, Andrew M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Birthweight; Fetal growth restriction; Immunology; Natural killer cells; Placental development; Pre eclampsia

Indexed keywords

ALLELE; BLOOD; BODY MASS; FUNCTIONAL ROLE; GENOTYPE; HUMAN EVOLUTION; IMMUNE SYSTEM; MATERNAL HEALTH; MEMBRANE; POLYMORPHISM; SURVIVAL;

HLA C ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KIR2DS1 PROTEIN, HUMAN;

BIRTH WEIGHT; CYTOLOGY; FEMALE; FETOMATERNAL TRANSFUSION; FETUS DEVELOPMENT; GENETIC SELECTION; GENOTYPE; HUMAN; IMMUNOLOGY; METABOLISM; NATURAL KILLER CELL; PHYSIOLOGY; PLACENTA; PREGNANCY; REPRODUCTION; TROPHOBLAST; UTERUS; VASCULARIZATION;

BIRTH WEIGHT; FEMALE; FETAL DEVELOPMENT; GENOTYPE; HLA-C ANTIGENS; HUMANS; KILLER CELLS, NATURAL; MATERNAL-FETAL EXCHANGE; PLACENTA; PLACENTATION; PREGNANCY; RECEPTORS, KIR; SELECTION, GENETIC; TROPHOBLASTS; UTERUS;

EID: 84922295428     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0071     Document Type: Review

References (54)

1. Karn MN, Penrose LS. 1951 Birth weight and gestation time in relation to maternal age, parity and infant survival. Ann. Eugen. 16, 147-164. (doi:10.1111/j.1469-1809.1951.tb02469.x)
2. Cavalli-Sforza LL, Bodmer WF. 1971 The genetics of human populations, pp. 612-613. San Francisco, CA: W. H. Freeman and Company.
3. Hiby SE, Apps R, Chazara O, Farrell LE, Magnus P, Trogstad L, Gjessing HK, Carrington M, Moffett A. 2014 Maternal KIR in combination with paternal HLA-C2 regulate human birth weight. J. Immunol. 192, 5069-5073. (doi:10.4049/jimmunol.1400577)
4. Burton GJ, Woods AW, Jauniaux E, Kingdom JC. 2009 Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 30, 473-482. (doi:10.1016/j.placenta.2009.02.009)
5. Moffett-King A. 2002 Natural killer cells and pregnancy. Nat. Rev. Immunol. 2, 656-663. (doi:10.1038/nri886)
6. Brosens I, Pijnenborg R, Vercruysse L, Romero R. 2011 The ‘Great Obstetrical Syndromes’ are associated with disorders of deep placentation. Am. J. Obstet. Gynecol. 204, 3193-3201. (doi:10.1016/j.ajog.2010.08.009)
7. Wittman AB, Wall LL. 2007 The evolutionary origins of obstructed labor: bipedalism, encephalization, and the human obstetric dilemma. Obstet. Gynecol. Surv. 62, 739-748. (doi:10.1097/01.ogx.0000286584.04310.5c)
8. Schwartz N, Quant HS, Sammel MD, Parry S. 2014 Macrosomia has its roots in early placental development. Placenta 35, 684-690. (doi:10.1016/j.placenta.2014.06.373)
9. Weaver TD, Hublin JJ. 2009 Neandertal birth canal shape and the evolution of human childbirth. Proc. Natl Acad. Sci. USA 106, 8151-8156. (doi:10.1073/pnas.0812554106)
10. Abitbol MM. 1996 Birth and human evolution: anatomical and obstetrical mechanics in primates, pp. 8-18. Westport, CT: Bergin & Garvey.
11. Carter AM, Pijnenborg R. 2011 Evolution of invasive placentation with special reference to non-human primates. Best Pract. Res. Clin. Obstet. Gynaecol. 25, 249-257. (doi:10.1016/j.bpobgyn.2010.10.010)
12. Parham P, Moffett A. 2013 Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat. Rev. Immunol. 13, 133-144. (doi:10.1038/nri3370)
13. Coqueugniot H, Hublin JJ. 2012 Age-related changes of digital endocranial volume during human ontogeny: results from an osteological reference collection. Am. J. Phys. Anthropol. 147, 312-318. (doi:10.1002/ajpa.21655)
14. Hannon T, Innes BA, Lash GE, Bulmer JN, Robson SC. 2012 Effects of local decidua on trophoblast invasion and spiral artery remodeling in focal placenta creta-an immunohistochemical study. Placenta 33, 998-1004. (doi:10.1016/j.placenta.2012.09.004)
15. Colucci F, Boulenouar S, Kieckbusch J, Moffett A. 2011 How does variability of immune system genes affect placentation? Placenta 32, 539-545. (doi:10.1016/j.placenta.2011.05.001)
16. Moffett A, Colucci F. 2014 Uterine NK cells: active regulators at the maternal-fetal interface. J. Clin. Invest. 124, 1872-1879. (doi:10.1172/JCI68107)
17. Abalos E, Cuesta C, Carroli G, Qureshi Z, Widmer M, Vogel JP, Souza JP. 2014 Pre-eclampsia, eclampsia and adverse maternal and perinatal outcomes: a secondary analysis of the World Health Organization Multicountry Survey on Maternal and Newborn Health. BJOG 121(1), 14-24. (doi:10.1111/1471-0528.12629)
18. Li DK, Wi S. 2000 Changing paternity and the risk of preeclampsia/eclampsia in the subsequent pregnancy. Am. J. Epidemiol. 151, 57-62. (doi:10.1093/oxfordjournals.aje.a010122)
19. Esplin MS, Fausett MB, Fraser A, Kerber R, Mineau G, Carrillo J, Varner MW. 2001 Paternal and maternal components of the predisposition to preeclampsia. N. Engl. J. Med. 344, 867-872. (doi:10.1056/NEJM200103223441201)
20. Magnus P, Gjessing HK, Skrondal A, Skjaerven R. 2001 Paternal contribution to birth weight. J. Epidemiol. Community Health 55, 873-877. (doi:10.1136/jech.55.12.873)
21. Rice F, Thapar A. 2010 Estimating the relative contributions of maternal genetic, paternal genetic and intrauterine factors to offspring birth weight and head circumference. Early Hum. Dev. 86, 425-432. (doi:10.1016/j.earlhumdev.2010.05.021)
22. Billingham RE, Brent L, Medawar PB. 1953 Actively acquired tolerance of foreign cells. Nature 172, 603-606. (doi:10.1038/172603a0)
23. van Kampen CA, Versteeg Voort Maarschalk MF, Langerak-Langerak J, Roelen DL, Claas FH. 2002 Kinetics of the pregnancy-induced humoral and cellular immune response against the paternal HLA class I antigens of the child. Hum. Immunol. 63, 452-458. (doi:10.1016/S0198-8859(02)00396-8)
24. Lissauer D, Piper K, Goodyear O, Kilby MD, Moss PA. 2012 Fetal-specific CD8þ cytotoxic T cell responses develop during normal human pregnancy and exhibit broad functional capacity. J. Immunol. 189, 1072-1080. (doi:10.4049/jimmunol.1200544)
25. Apps R, Murphy SP, Fernando R, Gardner L, Ahad T, Moffett A. 2009 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, 26-39. (doi:10.1111/j.1365-2567.2008.03019.x)
26. Tilburgs T, Scherjon SA, van der Mast BJ, Haasnoot GW, Versteeg Voort-Maarschalk M, Roelen DL, van Rood JJ, Claas FH. 2009 Fetal-maternal HLA-C mismatch is associated with decidual T cell activation and induction of functional T regulatory cells. J. Reprod. Immunol. 82, 148-157. (doi:10.1016/j.jri.2009.05.003)
27. Littman DR, Rudensky AY. 2010 Th17 and regulatory T cells in mediating and restraining inflammation. Cell 140, 845-858. (doi:10.1016/j.cell.2010.02.021)
28. Tafuri A, Alferink J, Moller P, Hammerling GJ, Arnold B. 1995 T cell awareness of paternal alloantigens during pregnancy. Science 270, 630-633. (doi:10.1126/science.270.5236.630)
29. Erlebacher A, Vencato D, Price KA, Zhang D, Glimcher LH. 2007 Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus. J. Clin. Invest. 117, 1399-1411. (doi:10.1172/JCI28214)
30. Madeja Z, Yadi H, Apps R, Boulenouar S, Roper SJ, Gardner L, Moffett A, Colucci F, Hemberger M. 2011 Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc. Natl Acad. Sci. USA 108, 4012-4017. (doi:10.1073/pnas.1005342108)
31. Aluvihare VR, Kallikourdis M, Betz AG. 2004 Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 5, 266-271. (doi:10.1038/ni1037)
32. Nancy P, Erlebacher A. 2014 T cell behavior at the maternal-fetal interface. Int. J. Dev. Biol. 58, 189-198. (doi:10.1387/ijdb.140054ae)
33. Koopman LA et al. 2003 Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med. 198, 1201-1212. (doi:10.1084/jem.20030305)
34. Hanna J et al. 2006 Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat. Med. 12, 1065-1074. (doi:10.1038/nm1452)
35. Hiby SE et al. 2010 Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Invest. 120, 4102-4110. (doi:10.1172/JCI43998)
36. Parham P. 2005 MHC class I molecules and KIRs in human history, health and survival. Nat. Rev. Immunol. 5, 201-214. (doi:10.1038/nri1570)
37. Hiby SE, Walker JJ, O’Shaughnessy KM, Redman CW, Carrington M, Trowsdale J, Moffett A. 2004 Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 200, 957-965. (doi:10.1084/jem.20041214)
38. Hiby SE, Regan L, Lo W, Farrell L, Carrington M, Moffett A. 2008 Association of maternal killer-cell immunoglobulin-like receptors and parental HLA-C genotypes with recurrent miscarriage. Hum. Reprod. 23, 972-976. (doi:10.1093/humrep/den011)
39. Hilton HG et al. 2012 Mutation at positively selected positions in the binding site for HLA-C shows that KIR2DL1 is a more refined but less adaptable NK cell receptor than KIR2DL3. J. Immunol. 189, 1418-1430. (doi:10.4049/jimmunol.1100431)
40. King A et al. 2000 HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur. J. Immunol. 30, 1623-1631. (doi:10.1002/1521-4141(200006)30:6,1623::AID-IMMU1623.3.0.CO;2-M)
41. Kopcow HD, Allan DS, Chen X, Rybalov B, Andzelm MM, Ge B, Strominger JL. 2005 Human decidual NK cells form immature activating synapses and are not cytotoxic. Proc. Natl Acad. Sci. USA 102, 15563-15568. (doi:10.1073/pnas.0507835102)
42. Xiong S et al. 2013 Maternal uterine NK cell-activating receptor KIR2DS1 enhances placentation. J. Clin. Invest. 123, 4264-4272. (doi:10.1172/JCI68991)
43. Kieckbusch J, Gaynor LM, Moffett A, Colucci F. 2014 MHC-dependent inhibition of uterine NK cells impedes fetal growth and decidual vascular remodelling. Nat. Commun. 5, 3359. (doi:10.1038/ncomms4359)
44. Pijnenborg R, Vercruysse L, Brosens I. 2011 Deep placentation. Best Pract. Res. Clin. Obstet. Gynaecol. 25, 273-285. (doi:10.1016/j.bpobgyn.2010.10.009)
45. Bari R, Bell T, Leung WH, Vong QP, Chan WK, Das Gupta N, Holladay M, Rooney B, Leung W. 2009 Significant functional heterogeneity among KIR2DL1 alleles and a pivotal role of arginine 245. Blood 114, 5182-5190. (doi:10.1182/blood-2009-07-231977)
46. Gendzekhadze K, Norman PJ, Abi-Rached L, Graef T, Moesta AK, Layrisse Z, Parham P. 2009 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. USA 106, 18692-18697. (doi:10.1073/pnas.0906051106)
47. Single RM, Martin MP, Gao X, Meyer D, Yeager M, Kidd JR, Kidd KK, Carrington M. 2007 Global diversity and evidence for coevolution of KIR and HLA. Nat. Genet. 39, 1114-1119. (doi:10.1038/ng2077)
48. Khan KS, Wojdyla D, Say L, Gulmezoglu AM, Van Look PF. 2006 WHO analysis of causes of maternal death: a systematic review. Lancet 367, 1066-1074. (doi:10.1016/S0140-6736(06)68397-9)
49. World Health Organization. 2010 World Health maternal mortality: 1990 to 2008. Geneva, Switzerland: WHO.
50. Nakimuli A, Chazara O, Byamugisha J, Elliott AM, Kaleebu P, Mirembe F, Moffett A. 2014 Pregnancy, parturition and preeclampsia in women of African ancestry. Am. J. Obstet. Gynecol. 210, 510-520.e1. (doi:10.1016/j.ajog.2013.10.879)
51. Nakimuli A et al. 2013 Killer cell immunoglobulinlike receptor (KIR) genes and their HLA-C ligands in a Ugandan population. Immunogenetics 65, 765-775. (doi:10.1007/s00251-013-0724-7)
52. Khakoo SI et al. 2004 HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305, 872-874. (doi:10.1126/science.1097670)
53. Handa VL, Lockhart ME, Fielding JR, Bradley CS, Brubaker L, Cundiff GW, Ye W, Richter HE, Pelvic Floor Disorders Network. 2008 Racial differences in pelvic anatomy by magnetic resonance imaging. Obstet. Gynecol. 111, 914-920. (doi:10.1097/AOG.0b013e318169ce03)
54. Patel RR, Steer P, Doyle P, Little MP, Elliott P. 2004 Does gestation vary by ethnic group? A Londonbased study of over 122 000 pregnancies with spontaneous onset of labour. Int. J. Epidemiol. 33, 107-113. (doi:10.1093/ije/dyg238)