Features of Human Decidual NK Cells in Healthy Pregnancy and During Viral Infection

Nabila Jabrane-Ferrat, Nabila Jabrane-Ferrat

Abstract

The hallmark of human early pregnancy is the accumulation of a unique population of Natural Killer (dNK) cells at the main maternal-fetal interface, the decidua basalis. dNK cells play a crucial role in successful placentation probably by orchestrating the invasion of trophoblast cells deep into the decidua basalis and remodeling of the maternal spiral arteries. Recent advances in the field emphasize the importance of the local microenvironment in shaping both the phenotype and the effector functions of these innate lymphoid cells. Despite slow progress in the field, ex vivo studies revealed that dNK cells sense and destroy infected cells in order to protect the fetus from invading pathogens. In this review, we will discuss key features of dNK cells during healthy pregnancy as well as their functional adaptations in limiting pathogen dissemination to the growing conceptus. The challenge is to better understand the plasticity of dNK cells in the maternal-fetal interface. Such insights would enable greater understanding of the pathogenesis in congenital infections and pregnancy disorders.

Keywords: congenital infection; cytokines; decidual natural killer; pregnancy; receptor.

Figures

Figure 1
Figure 1
Schematic representation of the maternal-fetal interface. Floating chorionic villi are bathed in maternal blood within the intervillous space. A multinucleated syncytiotrophoblast (STB) outer cell layer covering the chorionic villi. STB layer serves for transport of nutrient and barrier function. A layer of cytotrophoblast cells (CTBs), underlines the STB. CTBs differentiate into extravillous trophoblast (EVTs) and invade the maternal decidua. Through the release of soluble factors (cytokines, chemokines, and proangiogenic factors), maternal decidual NK (dNK) cells participate actively in the attraction of invasive EVTs and remodeling of the spiral arteries. Invasive EVTs are also in contact with decidual macrophages (dM) and T cells. Fetal blood vessel (BV), mesenchymal stem cells (MSC), Hofbauer cells (fetal macrophage).
Figure 2
Figure 2
Role of the microenvironment in shaping NK cell phenotype and functions: cNK cells expressing activating isoforms of the NKp30 and NKp44 receptors (NKp30a, NKp44b) which endows them with cytotoxic function, can be converted into dNK like cells. Exposure to a combination of TGF-β, IL-15 and IL-18) drives the isoform expression profile toward regulatory profile (NKp30c, NKp44a,c), a hallmark of dNK cells. This conversion is associated with the switch from cytotoxic to “helper-like” or tolerogenic effector functions associated with major changes in the secretome. How micro-environmental changes during pregnancy disorders or congenital infection might influence the dNK cell plasticity and effector functions is still an open question.

References

    1. Billingham RE, Brent L, Medawar PB. Actively acquired tolerance of foreign cells. Nature. (1953) 172:603–6. 10.1038/172603a0
    1. Jabrane-Ferrat N, Siewiera J. The up side of decidual natural killer cells: new developments in immunology of pregnancy. Immunology. (2014) 141:490–7. 10.1111/imm.12218
    1. Siewiera J, Gouilly J, Hocine HR, Cartron G, Levy C, Al-Daccak R, et al. . Natural cytotoxicity receptor splice variants orchestrate the distinct functions of human natural killer cell subtypes. Nat Commun. (2015) 6:10183. 10.1038/ncomms10183
    1. Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, Schatz F, et al. . Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med. (2003) 198:1201–12. 10.1084/jem.20030305
    1. Ivarsson MA, Loh L, Marquardt N, Kekäläinen E, Berglin L, Björkström NK, et al. . Differentiation and functional regulation of human fetal NK cells. J Clin Invest. (2013) 123:3889–901. 10.1172/JCI68989
    1. Mold JE, Michaëlsson J, Burt TD, Muench MO, Beckerman KP, Busch MP, et al. . Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science. (2008) 322:1562–5. 10.1126/science.1164511
    1. McGovern N, Shin A, Low G, Low D, Duan K, Yao LJ, et al. . Human fetal dendritic cells promote prenatal T-cell immune suppression through arginase-2. Nature. (2017) 546:662–6. 10.1038/nature22795
    1. Hamilton WJ, Boyd JD. Development of the human placenta in the first three months of gestation. J Anat. (1960) 94:297–328.
    1. Brosens I, Dixon HG. The anatomy of the maternal side of the placenta. J Obstet Gynaecol Br Commonw. (1966) 73:357–363. 10.1111/j.1471-0528.1966.tb05175.x
    1. Boyd JD, Hamilton WJ. Development and structure of the human placenta from the end of the 3rd month of gestation. J Obstet Gynaecol Br Commonw. (1967) 74:161–226. 10.1111/j.1471-0528.1967.tb14864.x
    1. Enders AC. Cytology of human early implantation. Res Reprod. (1976) 8:1–2.
    1. Enders AC, King BF. Early stages of trophoblastic invasion of the maternal vascular system during implantation in the macaque and baboon. Am J Anat. (1991) 192:329–46. 10.1002/aja.1001920403
    1. Hönig A, Rieger L, Kapp M, Sütterlin M, Dietl J, Kämmerer U. Indoleamine 2,3-dioxygenase (IDO) expression in invasive extravillous trophoblast supports role of the enzyme for materno-fetal tolerance. J Reprod Immunol. (2004) 61:79–86. 10.1016/j.jri.2003.11.002
    1. King A, Burrows TD, Hiby SE, Bowen JM, Joseph S, Verma S, et al. . Surface expression of HLA-C antigen by human extravillous trophoblast. Placenta. (2000) 21:376–87. 10.1053/plac.1999.0496
    1. Kovats S, Main EK, Librach C, Stubblebine M, Fisher SJ, DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science. (1990) 248:220–3. 10.1126/science.2326636
    1. Chumbley G, King A, Robertson K, Holmes N, Loke YW. Resistance of HLA-G and HLA-A2 transfectants to lysis by decidual NK cells. Cell Immunol. (1994) 155:312–22. 10.1006/cimm.1994.1125
    1. King A, Allan DS, Bowen M, Powis SJ, Joseph S, Verma S, et al. . HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur J Immunol. (2000) 30:1623–31. 10.1002/1521-4141(200006)30:6<1623::AID-IMMU1623>;2-M
    1. Llano M, Lee N, Navarro F, García P, Albar JP, Geraghty DE, 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. (1998) 28:2854–63. 10.1002/(SICI)1521-4141(199809)28:09<2854::AID-IMMU2854>;2-W
    1. Caumartin J, Favier B, Daouya M, Guillard C, Moreau P, Carosella ED, et al. . Trogocytosis-based generation of suppressive NK cells. EMBO J. (2007) 26:1423–33. 10.1038/sj.emboj.7601570
    1. Tilburgs T, Evans JH, Crespo ÂC, Strominger JL. The HLA-G cycle provides for both NK tolerance and immunity at the maternal-fetal interface. Proc Natl Acad Sci USA. (2015) 112:13312–7. 10.1073/pnas.1517724112
    1. Pijnenborg R, Bland JM, Robertson WB, Brosens I. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta. (1983) 4:397–413. 10.1016/S0143-4004(83)80043-5
    1. Robertson WB, Brosens I, Dixon G. Uteroplacental vascular pathology. Eur J Obstet Gynecol Reprod Biol. (1975) 5:47–65. 10.1016/0028-2243(75)90130-6
    1. Hustin J, Schaaps JP. Echographic [corrected] and anatomic studies of the maternotrophoblastic border during the first trimester of pregnancy. Am J Obstet Gynecol. (1987) 157:162–8. 10.1016/S0002-9378(87)80371-X
    1. Soothill PW, Nicolaides KH, Rodeck CH, Campbell S. Effect of gestational age on fetal and intervillous blood gas and acid-base values in human pregnancy. Fetal Ther. (1986) 1:168–75. 10.1159/000262264
    1. Watson AL, Skepper JN, Jauniaux E, Burton GJ. Susceptibility of human placental syncytiotrophoblastic mitochondria to oxygen-mediated damage in relation to gestational age. J Clin Endocrinol Metab. (1998) 83:1697–705. 10.1210/jc.83.5.1697
    1. Jauniaux E, Bersinger NA, Gulbis B, Meuris S. The contribution of maternal serum markers in the early prenatal diagnosis of molar pregnancies. Hum Reprod. (1999) 14:842–6. 10.1093/humrep/14.3.842
    1. Maltepe E, Fisher SJ. Placenta: the forgotten organ. Annu Rev Cell Dev Biol. (2015) 31:523–52. 10.1146/annurev-cellbio-100814-125620
    1. Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta. (2006) 27:939–58. 10.1016/j.placenta.2005.12.006
    1. Red-Horse K, Rivera J, Schanz A, Zhou Y, Winn V, Kapidzic M, et al. . Cytotrophoblast induction of arterial apoptosis and lymphangiogenesis in an in vivo model of human placentation. J Clin Invest. (2006) 116:2643–52. 10.1172/JCI27306
    1. Brosens I, Pijnenborg R, Vercruysse L, Romero R. The “Great Obstetrical Syndromes” are associated with disorders of deep placentation. Am J Obstet Gynecol. (2011) 204:193–201. 10.1016/j.ajog.2010.08.009
    1. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. (2008) 9:503–10. 10.1038/ni1582
    1. Cerwenka A, Lanier LL. Natural killer cell memory in infection, inflammation and cancer. Nat Rev Immunol. (2016) 16:112–23. 10.1038/nri.2015.9
    1. Waggoner SN, Cornberg M, Selin LK, Welsh RM. Natural killer cells act as rheostats modulating antiviral T cells. Nature. (2011) 481:394–8. 10.1038/nature10624
    1. Lopez-Verges S, Milush JM, Schwartz BS, Pando MJ, Jarjoura J, York VA, et al. Expansion of a unique CD57(+)NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci USA. (2011) 108:14725–32. 10.1073/pnas.1110900108
    1. Björkström NK, Ljunggren HG, Michaëlsson J. Emerging insights into natural killer cells in human peripheral tissues. Nat Rev Immunol. (2016) 16:310–20. 10.1038/nri.2016.34
    1. Aw Yeang HX, Piersma SJ, Lin Y, Yang L, Malkova ON, Miner C, et al. . Cutting edge: human CD49e- NK cells are tissue resident in the liver. J Immunol. (2017) 198:1417–22. 10.4049/jimmunol.1601818
    1. King A, Loke YW. On the nature and function of human uterine granular lymphocytes. Immunol Today. (1991) 12:432–5. 10.1016/0167-5699(91)90014-K
    1. Siewiera J, El Costa H, Tabiasco J, Berrebi A, Cartron G, Le Bouteiller P, et al. . Human cytomegalovirus infection elicits new decidual natural killer cell effector functions. PLoS Pathog. (2013) 9:e1003257. 10.1371/journal.ppat.1003257
    1. Ramathal CY, Bagchi IC, Taylor RN, Bagchi MK. Endometrial decidualization: of mice and men. Semin Reprod Med. (2010) 28:17–26. 10.1055/s-0029-1242989
    1. Burton GJ, Watson AL, Hempstock J, Skepper JN, Jauniaux E. Uterine glands provide histiotrophic nutrition for the human fetus during the first trimester of pregnancy. J Clin Endocrinol Metab. (2002) 87:2954–9. 10.1210/jcem.87.6.8563
    1. Hempstock J, Cindrova-Davies T, Jauniaux E, Burton GJ. 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. (2004) 2:58. 10.1186/1477-7827-2-58
    1. Moffett-King A. Natural killer cells and pregnancy. Nat Rev Immunol. (2002) 2:656–63. 10.1038/nri886
    1. Montaldo E, Vacca P, Chiossone L, Croxatto D, Loiacono F, Martini S, et al. . Unique eomes(+) NK cell subsets are present in uterus and decidua during early pregnancy. Front Immunol. (2015) 6:646. 10.3389/fimmu.2015.00646
    1. Bulmer JN, Longfellow M, Ritson A. Leukocytes and resident blood cells in endometrium. Ann N Y Acad Sci. (1991) 622:57–68. 10.1111/j.1749-6632.1991.tb37850.x
    1. Gardner L, Moffett A. Dendritic cells in the human decidua. Biol Reprod. (2003) 69:1438–46. 10.1095/biolreprod.103.017574
    1. Heikkinen J, Möttönen M, Alanen A, Lassila O. Phenotypic characterization of regulatory T cells in the human decidua. Clin Exp Immunol. (2004) 136:373–8. 10.1111/j.1365-2249.2004.02441.x
    1. Doisne JM, Balmas E, Boulenouar S, Gaynor LM, Kieckbusch J, Gardner L, et al. . Composition, development, and function of uterine innate lymphoid cells. J Immunol. (2015) 195:3937–45. 10.4049/jimmunol.1500689
    1. Vacca P, Montaldo E, Croxatto D, Loiacono F, Canegallo F, Venturini PL, et al. . Identification of diverse innate lymphoid cells in human decidua. Mucosal Immunol. (2015) 8:254–64. 10.1038/mi.2014.63
    1. Gibbs A, Leeansyah E, Introini A, Paquin-Proulx D, Hasselrot K, Andersson E, et al. . MAIT cells reside in the female genital mucosa and are biased towards IL-17 and IL-22 production in response to bacterial stimulation. Mucosal Immunol. (2017) 10:35–45. 10.1038/mi.2016.30
    1. King A, Hiby SE, Verma S, Burrows T, Gardner L, Loke YW. Uterine NK cells and trophoblast HLA class I molecules. Am J Reprod Immunol. (1997) 37:459–62. 10.1111/j.1600-0897.1997.tb00260.x
    1. Moffett A, Colucci F. Uterine NK cells: active regulators at the maternal-fetal interface. J Clin Invest. (2014) 124:1872–9. 10.1172/JCI68107
    1. El Costa H, Casemayou A, Aguerre-Girr M, Rabot M, Berrebi A, Parant O, et al. . Critical and differential roles of NKp46- and NKp30-activating receptors expressed by uterine NK cells in early pregnancy. J Immunol. (2008) 181:3009–17. 10.4049/jimmunol.181.5.3009
    1. Lockwood CJ, Huang SJ, Chen CP, Huang Y, Xu J, Faramarzi S, et al. . Decidual cell regulation of natural killer cell-recruiting chemokines: implications for the pathogenesis and prediction of preeclampsia. Am J Pathol. (2013) 183:841–56. 10.1016/j.ajpath.2013.05.029
    1. Vacca P, Pietra G, Falco M, Romeo E, Bottino C, Bellora F, et al. . Analysis of natural killer cells isolated from human decidua: evidence that 2B4 (CD244) functions as an inhibitory receptor and blocks NK-cell function. Blood. (2006) 108:4078–85. 10.1182/blood-2006-04-017343
    1. Male V, Sharkey A, Masters L, Kennedy PR, Farrell LE, Moffett A. The effect of pregnancy on the uterine NK cell KIR repertoire. Eur J Immunol. (2011) 41:3017–27. 10.1002/eji.201141445
    1. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, et al. . Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med. (2006) 12:1065–74. 10.1038/nm1452
    1. Vento-Tormo R, Efremova M, Botting RA, Turco MY, Vento-Tormo M, Meyer KB, et al. . Single-cell reconstruction of the early maternal-fetal interface in humans. Nature. (2018) 563:347–53. 10.1038/s41586-018-0698-6
    1. Zhao H, Bo C, Kang Y, Li H. What else can CD39 tell us? Front Immunol. (2017) 8:727. 10.3389/fimmu.2017.00727
    1. Vacca P, Moretta L, Moretta A, Mingari MC. Origin, phenotype and function of human natural killer cells in pregnancy. Trends Immunol. (2011) 32:517–23. 10.1016/j.it.2011.06.013
    1. Vacca P, Vitale C, Montaldo E, Conte R, Cantoni C, Fulcheri E, et al. . CD34+ hematopoietic precursors are present in human decidua and differentiate into natural killer cells upon interaction with stromal cells. Proc Natl Acad Sci USA. (2011) 108:2402–7. 10.1073/pnas.1016257108
    1. Male V, Hughes T, McClory S, Colucci F, Caligiuri MA, Moffett A. Immature NK cells, capable of producing IL-22, are present in human uterine mucosa. J Immunol. (2010) 185:3913–8. 10.4049/jimmunol.1001637
    1. Hanna J, Wald O, Goldman-Wohl D, Prus D, Markel G, Gazit R, et al. . CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells. Blood. (2003) 102:1569–77. 10.1182/blood-2003-02-0517
    1. Kunkel EJ, Butcher EC. Chemokines and the tissue-specific migration of lymphocytes. Immunity. (2002) 16:1–4. 10.1016/S1074-7613(01)00261-8
    1. Santoni A, Carlino C, Stabile H, Gismondi A. Mechanisms underlying recruitment and accumulation of decidual NK cells in uterus during pregnancy. Am J Reprod Immunol. (2008) 59:417–24. 10.1111/j.1600-0897.2008.00598.x
    1. Allan DS, Rybalov B, Awong G, Zúñiga-Pflücker JC, Kopcow HD, Carlyle JR, et al. . TGF-β affects development and differentiation of human natural killer cell subsets. Eur J Immunol. (2010) 40:2289–95. 10.1002/eji.200939910
    1. Cerdeira AS, Rajakumar A, Royle CM, Lo A, Husain Z, Thadhani RI, et al. . Conversion of peripheral blood NK cells to a decidual NK-like phenotype by a cocktail of defined factors. J Immunol. (2013) 190:3939–48. 10.4049/jimmunol.1202582
    1. Keskin DB, Allan DS, Rybalov B, Andzelm MM, Stern JN, Kopcow HD, et al. . TGFβ promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells. Proc Natl Acad Sci USA. (2007) 104:3378–83. 10.1073/pnas.0611098104
    1. Jokhi PP, King A, Loke YW. Cytokine production and cytokine receptor expression by cells of the human first trimester placental-uterine interface. Cytokine. (1997) 9:126–37. 10.1006/cyto.1996.0146
    1. Dunn CL, Critchley HO, Kelly RW. IL-15 regulation in human endometrial stromal cells. J Clin Endocrinol Metab. (2002) 87:1898–901. 10.1210/jcem.87.4.8539
    1. Wang F, Zhu H, Li B, Liu M, Liu D, Deng M, et al. . Effects of human chorionic gonadotropin, estradiol, and progesterone on interleukin-18 expression in human decidual tissues. Gynecol Endocrinol. (2017) 33:265–9. 10.1080/09513590.2016.1212829
    1. Kopcow HD, Allan DS, Chen X, Rybalov B, Andzelm MM, Ge B, et al. Human decidual NK cells form immature activating synapses and are not cytotoxic. Proc Natl Acad Sci USA. (2005) 102:15563–8. 10.1073/pnas.0507835102
    1. Moffett A, Shreeve N. First do no harm: uterine natural killer (NK) cells in assisted reproduction. Hum Reprod. (2015) 30:1519–25. 10.1093/humrep/dev098
    1. Jones RL, Stoikos C, Findlay JK, Salamonsen LA. TGF-β superfamily expression and actions in the endometrium and placenta. Reproduction. (2006) 132:217–32. 10.1530/rep.1.01076
    1. Lockwood CJ, Basar M, Kayisli UA, Guzeloglu-Kayisli O, Murk W, Wang J, et al. . Interferon-gamma protects first-trimester decidual cells against aberrant matrix metalloproteinases 1, 3, and 9 expression in preeclampsia. Am J Pathol. (2014) 184:2549–59. 10.1016/j.ajpath.2014.05.025
    1. Otun HA, Lash GE, Innes BA, Bulmer JN, Naruse K, Hannon T, et al. . Effect of tumour necrosis factor-alpha in combination with interferon-gamma on first trimester extravillous trophoblast invasion. J Reprod Immunol. (2011) 88:1–11. 10.1016/j.jri.2010.10.003
    1. Prossler J, Chen Q, Chamley L, James JL. The relationship between TGFβ, low oxygen and the outgrowth of extravillous trophoblasts from anchoring villi during the first trimester of pregnancy. Cytokine. (2014) 68:9–15. 10.1016/j.cyto.2014.03.001
    1. Parham P, Guethlein LA. Pregnancy immunogenetics: NK cell education in the womb? J Clin Invest. (2010) 120:3801–4. 10.1172/JCI44559
    1. Tilburgs T, Crespo ÂC, van der Zwan A, Rybalov B, Raj T, Stranger B, et al. . Human HLA-G+ extravillous trophoblasts: immune-activating cells that interact with decidual leukocytes. Proc Natl Acad Sci USA. (2015) 112:7219–24. 10.1073/pnas.1507977112
    1. Wallace AE, Whitley GS, Thilaganathan B, Cartwright JE. Decidual natural killer cell receptor expression is altered in pregnancies with impaired vascular remodeling and a higher risk of pre-eclampsia. J Leukoc Biol. (2015) 97:79–86. 10.1189/jlb.2A0614-282R
    1. Osol G, Moore LG. Maternal uterine vascular remodeling during pregnancy. Microcirculation. (2014) 21:38–47. 10.1111/micc.12080
    1. Saito S, Nakashima A. A review of the mechanism for poor placentation in early-onset preeclampsia: the role of autophagy in trophoblast invasion and vascular remodeling. J Reprod Immunol. (2014) 101–2:80–8. 10.1016/j.jri.2013.06.002
    1. Rätsep MT, Felker AM, Kay VR, Tolusso L, Hofmann AP, Croy BA. Uterine natural killer cells: supervisors of vasculature construction in early decidua basalis. Reproduction. (2015) 149:R91–102. 10.1530/REP-14-0271
    1. Hiby SE, Apps R, Sharkey AM, Farrell LE, Gardner L, Mulder A, et al. . Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J Clin Invest. (2010) 120:4102–10. 10.1172/JCI43998
    1. Björkström NK, Lindgren T, Stoltz M, Fauriat C, Braun M, Evander M, et al. . Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J Exp Med. (2011) 208:13–21. 10.1084/jem.20100762
    1. Prefumo F, Ganapathy R, Thilaganathan B, Sebire NJ. Influence of parity on first trimester endovascular trophoblast invasion. Fertil Steril. (2006) 85:1032–6. 10.1016/j.fertnstert.2005.09.055
    1. Sharkey AM, Xiong S, Kennedy PR, Gardner L, Farrell LE, Chazara O, et al. . Tissue-Specific Education of Decidual NK Cells. J Immunol. (2015) 195:3026–32. 10.4049/jimmunol.1501229
    1. Gamliel M, Goldman-Wohl D, Isaacson B, Gur C, Stein N, Yamin R, et al. . Trained memory of human uterine NK cells enhances their function in subsequent pregnancies. Immunity. (2018) 48:951–62 e955. 10.1016/j.immuni.2018.03.030
    1. Coyne CB, Lazear HM. Zika virus - reigniting the TORCH. Nat Rev Microbiol. (2016) 14:707–15. 10.1038/nrmicro.2016.125
    1. Gouilly J, Chen Q, Siewiera J, Cartron G, Levy C, Dubois M, et al. . Genotype specific pathogenicity of hepatitis E virus at the human maternal-fetal interface. Nat Commun. (2018) 9:4748. 10.1038/s41467-018-07200-2
    1. El Costa H, Gouilly J, Mansuy JM, Chen Q, Levy C, Cartron G, et al. . Zika virus reveals broad tissue and cell tropism during the first trimester of pregnancy. Sci Rep. (2016) 6:35296. 10.1038/srep35296
    1. Tabata T, Petitt M, Puerta-Guardo H, Michlmayr D, Wang C, Fang-Hoover J, et al. . Zika virus targets different primary human placental cells, suggesting two routes for vertical transmission. Cell Host Microbe. (2016) 20:155–66. 10.1016/j.chom.2016.07.002
    1. Pereira L. Congenital viral infection: traversing the uterine-placental interface. Ann Rev Virol. (2018) 5:273–99. 10.1146/annurev-virology-092917-043236
    1. Dolan A, Cunningham C, Hector RD, Hassan-Walker AF, Lee L, Addison C, et al. . Genetic content of wild-type human cytomegalovirus. J Gen Virol. (2004) 85:1301–12. 10.1099/vir.0.79888-0
    1. Colugnati FA, Staras SA, Dollard SC, Cannon MJ. Incidence of cytomegalovirus infection among the general population and pregnant women in the United States. BMC Infect Dis. (2007) 7:71. 10.1186/1471-2334-7-71
    1. Enders G, Daiminger A, Bäder U, Exler S, Enders M. Intrauterine transmission and clinical outcome of 248 pregnancies with primary cytomegalovirus infection in relation to gestational age. J Clin Virol. (2011) 52:244–6. 10.1016/j.jcv.2011.07.005
    1. Halwachs-Baumann G, Wilders-Truschnig M, Desoye G, Hahn T, Kiesel L, Klingel K, et al. . Human trophoblast cells are permissive to the complete replicative cycle of human cytomegalovirus. J Virol. (1998) 72:7598–602.
    1. Fisher S, Genbacev O, Maidji E, Pereira L. Human cytomegalovirus infection of placental cytotrophoblasts in vitro and in utero: implications for transmission and pathogenesis. J Virol. (2000) 74:6808–20. 10.1128/JVI.74.15.6808-6820.2000
    1. Yamamoto-Tabata T, McDonagh S, Chang HT, Fisher S, Pereira L. Human cytomegalovirus interleukin-10 downregulates metalloproteinase activity and impairs endothelial cell migration and placental cytotrophoblast invasiveness in vitro. J Virol. (2004) 78:2831–40. 10.1128/JVI.78.6.2831-2840.2004
    1. Tabata T, McDonagh S, Kawakatsu H, Pereira L. Cytotrophoblasts infected with a pathogenic human cytomegalovirus strain dysregulate cell-matrix and cell-cell adhesion molecules: a quantitative analysis. Placenta. (2007) 28:527–37. 10.1016/j.placenta.2006.05.006
    1. Kumar A, Beniwal M, Kar P, Sharma JB, Murthy NS. Hepatitis E in pregnancy. Int J Gynaecol Obstet. (2004) 85:240–4. 10.1016/j.ijgo.2003.11.018
    1. Patra S, Kumar A, Trivedi SS, Puri M, Sarin SK. Maternal and fetal outcomes in pregnant women with acute hepatitis E virus infection. Ann Intern Med. (2007) 147:28–33. 10.7326/0003-4819-147-1-200707030-00005
    1. Faria NR, Quick J, Claro IM, Thézé J, de Jesus JG, Giovanetti M, et al. . Establishment and cryptic transmission of Zika virus in Brazil and the Americas. Nature. (2017) 546:406–10. 10.1038/nature22401
    1. Brasil P, Nielsen-Saines K. More pieces to the microcephaly-Zika virus puzzle in Brazil. Lancet Infect Dis. (2016) 16:1307–9. 10.1016/S1473-3099(16)30372-3
    1. Tabata T, Petitt M, Puerta-Guardo H, Michlmayr D, Harris E, Pereira L. Zika virus replicates in proliferating cells in explants from first-trimester human placentas, potential sites for dissemination of infection. J Infect Dis. (2018) 217:1202–13. 10.1093/infdis/jix552
    1. Petitt M, Tabata T, Puerta-Guardo H, Harris E, Pereira L. Zika virus infection of first-trimester human placentas: utility of an explant model of replication to evaluate correlates of immune protection ex vivo. Curr Opin Virol. (2017) 27:48–56. 10.1016/j.coviro.2017.11.008
    1. Bayer A, Lennemann NJ, Ouyang Y, Bramley JC, Morosky S, Marques ET, et al. . Type III interferons produced by human placental trophoblasts confer protection against Zika virus infection. Cell Host Microbe. (2016) 19:705–12. 10.1016/j.chom.2016.03.008
    1. Veljkovic Vujaklija D, Dominovic M, Gulic T, Mahmutefendic H, Haller H, Saito S, et al. . Granulysin expression and the interplay of granulysin and perforin at the maternal-fetal interface. J Reprod Immunol. (2013) 97:186–96. 10.1016/j.jri.2012.11.003

Source: PubMed

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