Natural Killer Cells Promote Fetal Development through the Secretion of Growth-Promoting Factors

Immunity

Volumn 47, Issue 6, 2017, Pages 1100-1113.e6

  Fu, Binqing ^a,b   Zhou, Yonggang ^a,b   Ni, Xiang ^a,b   Tong, Xianhong ^c   Xu, Xiuxiu ^a,b   Dong, Zhongjun ^d   Sun, Rui ^a,b   Tian, Zhigang ^a,b   Wei, Haiming ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c ANHUI PROVINCIAL HOSPITAL   (China)

^d Tsinghua University   (China)

Author keywords

aged pregnancy; decidual NK cells; fetal development; fetal growth restriction; growth promoting factors; maternal fetal interface; tissue resident NK

Indexed keywords

ALPHA1 INTEGRIN; CD56 ANTIGEN; GROWTH PROMOTOR; HLA G ANTIGEN; PLEIOTROPHIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NFIL3; UNCLASSIFIED DRUG; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CARRIER PROTEIN; CYTOKINE; EOMES PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTOR SUBFAMILY B MEMBER 1; LILRB1 PROTEIN, HUMAN; NFIL3 PROTEIN, HUMAN; OGN PROTEIN, HUMAN; SIGNAL PEPTIDE; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; FETUS DEVELOPMENT; FETUS WASTAGE; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOCYTE SUBPOPULATION; MICROENVIRONMENT; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; ADULT; ANIMAL; C57BL MOUSE; CYTOLOGY; DECIDUA; FETUS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INTRAUTERINE GROWTH RETARDATION; PATHOLOGY; PREGNANCY; RECURRENT ABORTION; SECRETION (PROCESS); SIGNAL TRANSDUCTION; TRANSPLANTATION; TUMOR MICROENVIRONMENT;

ABORTION, HABITUAL; ADOPTIVE TRANSFER; ADULT; ANIMALS; ANTIGENS, CD; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CARRIER PROTEINS; CELLULAR MICROENVIRONMENT; CYTOKINES; DECIDUA; FEMALE; FETAL DEVELOPMENT; FETAL GROWTH RETARDATION; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HLA-G ANTIGENS; HUMANS; INTEGRIN ALPHA1; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KILLER CELLS, NATURAL; LEUKOCYTE IMMUNOGLOBULIN-LIKE RECEPTOR B1; MICE; MICE, INBRED C57BL; PREGNANCY; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS;

EID: 85038239143     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2017.11.018     Document Type: Article

References (64)

1. Ahokas, R., and McKinney, E. (2008). Development and physiology of the placenta and membranes. https://doi.org/10.3843/GLOWM.10101.
2. Arck, P.C., Hecher, K., Fetomaternal immune cross-talk and its consequences for maternal and offspring's health. Nat. Med. 19 (2013), 548–556.
3. Barber, E.M., Pollard, J.W., 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.
4. Boulenouar, S., Doisne, J.M., Sferruzzi-Perri, A., Gaynor, L.M., Kieckbusch, J., Balmas, E., Yung, H.W., Javadzadeh, S., Volmer, L., Hawkes, D.A., et al. The residual innate lymphoid cells in NFIL3-deficient mice support suboptimal maternal adaptations to pregnancy. Front. Immunol., 7, 2016, 43.
5. Camous, X., Pera, A., Solana, R., Larbi, A., NK cells in healthy aging and age-associated diseases. J. Biomed. Biotechnol., 2012, 2012, 195956.
6. Cheng, M., Chen, Y.Y., Xiao, W.H., Sun, R., Tian, Z.G., NK cell-based immunotherapy for malignant diseases. Cell Mol. Immunol. 10 (2013), 230–252.
7. Choi, S.T., Kim, J.H., Kang, E.J., Lee, S.W., Park, M.C., Park, Y.B., Lee, S.K., Osteopontin might be involved in bone remodelling rather than in inflammation in ankylosing spondylitis. Rheumatology (Oxford) 47 (2008), 1775–1779.
8. Colucci, F., Kieckbusch, J., Maternal uterine natural killer cells nurture fetal growth: in medio stat virtus. Trends Mol. Med. 21 (2015), 60–67.
9. Cong, L., Zhang, F., Genome engineering using CRISPR-Cas9 system. Methods Mol. Biol. 1239 (2015), 197–217.
10. Cortez, V.S., Cervantes-Barragan, L., Robinette, M.L., Bando, J.K., Wang, Y.M., Geiger, T.L., Gilfillan, S., Fuchs, A., Vivier, E., Sun, J.C., et al. Transforming Growth Factor-beta signaling guides the differentiation of innate lymphoid cells in salivary glands. Immunity 44 (2016), 1127–1139.
11. Cortez, V.S., Fuchs, A., Cella, M., Gilfillan, S., Colonna, M., Cutting edge: Salivary gland NK cells develop independently of Nfil3 in steady-state. J. Immunol. 192 (2014), 4487–4491.
12. Doisne, J.M., Balmas, E., Boulenouar, S., Gaynor, L.M., Kieckbusch, J., Gardner, L., Hawkes, D.A., Barbara, C.F., Sharkey, A.M., Brady, H.J., et al. Composition, development, and function of uterine innate lymphoid cells. J. Immunol. 195 (2015), 3937–3945.
13. Dreyfus, J., Brunet-de Carvalho, N., Duprez, D., Raulais, D., Vigny, M., HB-GAM/pleiotrophin: localization of mRNA and protein in the chicken developing leg. Int. J. Dev. Biol. 42 (1998), 189–198.
14. Eberl, G., Di Santo, J.P., Vivier, E., The brave new world of innate lymphoid cells. Nat. Immunol. 16 (2015), 1–5.
15. El Costa, H., Tabiasco, J., Berrebi, A., Parant, O., Aguerre-Girr, M., Piccinni, M.P., Le Bouteiller, P., Effector functions of human decidual NK cells in healthy early pregnancy are dependent on the specific engagement of natural cytotoxicity receptors. J. Reprod. Immunol. 82 (2009), 142–147.
16. Fu, B., Li, X., Sun, R., Tong, X., Ling, B., Tian, Z., Wei, H., Natural killer cells promote immune tolerance by regulating inflammatory TH17 cells at the human maternal-fetal interface. Proc. Natl. Acad. Sci. USA 110 (2013), E231–E240.
17. Fu, B., Tian, Z., Wei, H., Subsets of human natural killer cells and their regulatory effects. Immunology 141 (2014), 483–489.
18. Fu, B.Q., Tian, Z.G., Wei, H.M., TH17 cells in human recurrent pregnancy loss and pre-eclampsia. Cell Mol. Immunol. 11 (2014), 564–570.
19. Fu, B., Wang, F., Sun, R., Ling, B., Tian, Z., Wei, H., CD11b and CD27 reflect distinct population and functional specialization in human natural killer cells. Immunology 133 (2011), 350–359.
20. Gasteiger, G., Rudensky, A.Y., Interactions between innate and adaptive lymphocytes. Nat. Rev. Immunol. 14 (2014), 631–639.
21. Gordon, S.M., Chaix, J., Rupp, L.J., Wu, J., Madera, S., Sun, J.C., Lindsten, T., Reiner, S.L., The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 36 (2012), 55–67.
22. Hanna, J., Goldman-Wohl, D., Hamani, Y., Avraham, I., Greenfield, C., Natanson-Yaron, S., Prus, D., Cohen-Daniel, L., Arnon, T.I., Manaster, I., et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat. Med. 12 (2006), 1065–1074.
23. Hiby, S.E., Apps, R., Chazara, O., Farrell, L.E., Magnus, P., Trogstad, L., Gjessing, H.K., Carrington, M., Moffett, A., Maternal KIR in combination with paternal HLA-C2 regulate human birth weight. J. Immunol. 192 (2014), 5069–5073.
24. Hiby, S.E., Apps, R., Sharkey, A.M., Farrell, L.E., Gardner, L., Mulder, A., Claas, F.H., Walker, J.J., Redman, C.W., Morgan, L., et al. Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Invest. 120 (2010), 4102–4110.
25. Hunt, J.S., Petroff, M.G., McIntire, R.H., Ober, C., HLA-G and immune tolerance in pregnancy. FASEB J. 19 (2005), 681–693.
26. Jabrane-Ferrat, N., Siewiera, J., The up side of decidual natural killer cells: new developments in immunology of pregnancy. Immunology 141 (2014), 490–497.
27. Jolly, M., Sebire, N., Harris, J., Robinson, S., Regan, L., The risks associated with pregnancy in women aged 35 years or older. Hum. Reprod. 15 (2000), 2433–2437.
28. Jurisicova, A., Casper, R.F., MacLusky, N.J., Mills, G.B., Librach, C.L., HLA-G expression during preimplantation human embryo development. Proc. Natl. Acad. Sci. USA 93 (1996), 161–165.
29. Kalkunte, S.S., Mselle, T.F., Norris, W.E., Wira, C.R., Sentman, C.L., Sharma, S., Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface. J. Immunol. 182 (2009), 4085–4092.
30. Kieckbusch, J., Gaynor, L.M., Moffett, A., Colucci, F., MHC-dependent inhibition of uterine NK cells impedes fetal growth and decidual vascular remodelling. Nat. Commun., 5, 2014, 3359.
31. Klose, C.S., Flach, M., Mohle, L., Rogell, L., Hoyler, T., Ebert, K., Fabiunke, C., Pfeifer, D., Sexl, V., Fonseca-Pereira, D., et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157 (2014), 340–356.
32. Koopman, L.A., Kopcow, H.D., Rybalov, B., Boyson, J.E., Orange, J.S., Schatz, F., Masch, R., Lockwood, C.J., Schachter, A.D., Park, P.J., Strominger, J.L., Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med. 198 (2003), 1201–1212.
33. Lash, G.E., Schiessl, B., Kirkley, M., Innes, B.A., Cooper, A., Searle, R.F., Robson, S.C., Bulmer, J.N., Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy. J. Leukoc. Biol. 80 (2006), 572–580.
34. LeMaoult, J., Zafaranloo, K., Le Danff, C., Carosella, E.D., HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cells. Faseb. J. 19 (2005), 662–664.
35. Male, V., Sharkey, A., Masters, L., Kennedy, P.R., Farrell, L.E., Moffett, A., The effect of pregnancy on the uterine NK cell KIR repertoire. Eur. J. Immunol. 41 (2011), 3017–3027.
36. Mansell, T., Novakovic, B., Meyer, B., Rzehak, P., Vuillermin, P., Ponsonby, A.L., Collier, F., Burgner, D., Saffery, R., Ryan, J., The effects of maternal anxiety during pregnancy on IGF2/H19 methylation in cord blood. Transl. Psychiatry, 6, 2016, e765.
37. Michaud, M., Balardy, L., Moulis, G., Gaudin, C., Peyrot, C., Vellas, B., Cesari, M., Nourhashemi, F., Proinflammatory cytokines, aging, and age-related diseases. J. Am. Med. Dir. Assoc. 14 (2013), 877–882.
38. Nagashima, T., Li, Q., Clementi, C., Lydon, J.P., DeMayo, F.J., Matzuk, M.M., BMPR2 is required for postimplantation uterine function and pregnancy maintenance. J. Clin. Invest. 123 (2013), 2539–2550.
39. Niu, Y., Shen, B., Cui, Y., Chen, Y., Wang, J., Wang, L., Kang, Y., Zhao, X., Si, W., Li, W., et al. Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156 (2014), 836–843.
40. Otto, F., Thornell, A.P., Crompton, T., Denzel, A., Gilmour, K.C., Rosewell, I.R., Stamp, G.W., Beddington, R.S., Mundlos, S., Olsen, B.R., et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89 (1997), 765–771.
41. Parham, P., Moffett, A., Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat. Rev. Immunol. 13 (2013), 133–144.
42. Peng, H., Sun, R., Liver-resident NK cells and their potential functions. Cell Mol. Immunol. 14 (2017), 890–894.
43. Peng, H., Jiang, X., Chen, Y., Sojka, D.K., Wei, H., Gao, X., Sun, R., Yokoyama, W.M., Tian, Z., Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Invest. 123 (2013), 1444–1456.
44. Perez-Pinera, P., Berenson, J.R., Deuel, T.F., Pleiotrophin, a multifunctional angiogenic factor: mechanisms and pathways in normal and pathological angiogenesis. Curr. Opin. Hematol. 15 (2008), 210–214.
45. Rajagopalan, S., HLA-G-mediated NK cell senescence promotes vascular remodeling: implications for reproduction. Cell Mol. Immunol. 11 (2014), 460–466.
46. Rajagopalan, S., Long, E.O., Cellular senescence induced by CD158d reprograms natural killer cells to promote vascular remodeling. Proc. Natl. Acad. Sci. USA 109 (2012), 20596–20601.
47. Rauvala, H., An 18-kd heparin-binding protein of developing brain that is distinct from fibroblast growth factors. EMBO J. 8 (1989), 2933–2941.
48. Rouas-Freiss, N., Gonçalves, R.M., 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. Proc. Natl. Acad. Sci. USA 94 (1997), 11520–11525.
49. Roy, A.K., Oh, T., Rivera, O., Mubiru, J., Song, C.S., Chatterjee, B., Impacts of transcriptional regulation on aging and senescence. Ageing Res. Rev. 1 (2002), 367–380.
50. Sanders, S.K., Giblin, P.A., Kavathas, P., Cell-cell adhesion mediated by Cd8 and human histocompatibility leukocyte antigen-G, a nonclassical major histocompatibility complex class-1 molecule on cytotrophoblasts. J. Exp. Med. 174 (1991), 737–740.
51. Sarwar, R., Petretto, E., Grieve, I.C., Lu, H., Kumaran, M.K., Muckett, P.J., Mangion, J., Schroen, B., Benson, M., Punjabi, P.P., et al. Integrated genomics approaches identify osteoglycin as a regulator of left ventricular mass. Heart, 95, 2009 A4.
52. Schulkey, C.E., Regmi, S.D., Magnan, R.A., Danzo, M.T., Luther, H., Hutchinson, A.K., Panzer, A.A., Grady, M.M., Wilson, D.B., Jay, P.Y., The maternal-age-associated risk of congenital heart disease is modifiable. Nature 520 (2015), 230–233.
53. Seillet, C., Huntington, N.D., Gangatirkar, P., Axelsson, E., Minnich, M., Brady, H.J.M., Busslinger, M., Smyth, M.J., Belz, G.T., Carotta, S., Differential requirement for Nfil3 during NK cell development. J. Immunol. 192 (2014), 2667–2676.
54. Singh, M., Dalal, S., Singh, K., Osteopontin: At the cross-roads of myocyte survival and myocardial function. Life Sci. 118 (2014), 1–6.
55. Sojka, D.K., Plougastel-Douglas, B., Yang, L., Pak-Wittel, M.A., Artyomov, M.N., Ivanova, Y., Zhong, C., Chase, J.M., Rothman, P.B., Yu, J., et al. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife, 3, 2014, e01659.
56. Sun, L.L., Wang, A.M., Haines, C.J., Han, Y., Yao, Y.Q., Down-regulation of HLA-G attenuates cleavage rate in human triploid embryos. J. Reprod. Infertil. 12 (2011), 215–220.
57. Tilburgs, T., Evans, J.H., Crespo, A.C., Strominger, J.L., The HLA-G cycle provides for both NK tolerance and immunity at the maternal-fetal interface. Proc. Natl. Acad. Sci. USA 112 (2015), 13312–13317.
58. Vacca, P., Mingari, M.C., Moretta, L., Natural killer cells in human pregnancy. J. Reprod. Immunol. 97 (2013), 14–19.
59. Wang, H., Yang, H., Shivalila, C.S., Dawlaty, M.M., Cheng, A.W., Zhang, F., Jaenisch, R., One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153 (2013), 910–918.
60. Williamson, R.E., Darrow, K.N., Giersch, A.B.S., Resendes, B.L., Huang, M., Conrad, G.W., Chen, Z.Y., Liberman, M.C., Morton, C.C., Tasheva, E.S., Expression studies of osteoglycin/mimecan (OGN) in the cochlea and auditory phenotype of Ogn-deficient mice. Hear. Res. 237 (2008), 57–65.
61. Woods, L., Perez-Garcia, V., Kieckbusch, J., Wang, X., DeMayo, F., Colucci, F., Hemberger, M., Decidualisation and placentation defects are a major cause of age-related reproductive decline. Nat. Commun., 8, 2017, 352.
62. Xiong, S., Sharkey, A.M., Kennedy, P.R., Gardner, L., Farrell, L.E., Chazara, O., Bauer, J., Hiby, S.E., Colucci, F., Moffett, A., Maternal uterine NK cell-activating receptor KIR2DS1 enhances placentation. J. Clin. Invest. 123 (2013), 4264–4272.
63. Zhang, J., Chen, Z., Smith, G.N., Croy, B.A., Natural killer cell-triggered vascular transformation: maternal care before birth?. Cell Mol. Immunol. 8 (2011), 1–11.
64. Zhang, J.H., Dunk, C.E., Kwan, M., Jones, R.L., Harris, L.K., Keating, S., Lye, S.J., Human dNK cell function is differentially regulated by extrinsic cellular engagement and intrinsic activating receptors in first and second trimester pregnancy. Cell Mol. Immunol. 14 (2017), 203–213.