Human Cytomegalovirus Infection Elicits New Decidual Natural Killer Cell Effector Functions

PLoS Pathogens

Volumn 9, Issue 4, 2013, Pages

  Siewiera, Johan ^a,b,c   El Costa, Hicham ^a,b,c   Tabiasco, Julie ^a,b,c   Berrebi, Alain ^d   Cartron, Géraldine ^d   Bouteiller, Philippe ^a,b,c   Jabrane Ferrat, Nabila ^a,b,c  

^a France   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d Paul Sabatier University   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD56 ANTIGEN; CD94 ANTIGEN; CHEMOKINE; CYTOKINE; IMMUNOGLOBULIN G; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL4; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL KILLER CELL RECEPTOR NKG2D; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ARTICLE; CELL CULTURE; CELL INFILTRATION; CONFOCAL MICROSCOPY; CONJUGATION; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; CYTOTOXICITY; FIBROBLAST; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; INNATE IMMUNITY; INTRAUTERINE INFECTION; NATURAL KILLER CELL; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; POLARIZATION; PROTEIN EXPRESSION; SYNAPSE; TROPHOBLAST;

ANTIGENS, CD56; CELL LINE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DECIDUA; FAS LIGAND PROTEIN; FEMALE; HEK293 CELLS; HUMANS; KILLER CELLS, NATURAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY D; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PLACENTATION; PREGNANCY; PREGNANCY TRIMESTER, FIRST; TNF-RELATED APOPTOSIS-INDUCING LIGAND; UTERUS;

HUMAN HERPESVIRUS 5;

EID: 84876865989     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003257     Document Type: Article

References (69)

1. Cannon MJ, (2009) Congenital cytomegalovirus (CMV) epidemiology and awareness. J Clin Virol 46 Suppl 4: S6-10.
2. Gohring K, Dietz K, Hartleif S, Jahn G, Hamprecht K, (2010) Influence of different extraction methods and PCR techniques on the sensitivity of HCMV-DNA detection in dried blood spot (DBS) filter cards. J Clin Virol 48: 278-281.
3. Berger A, Reitter A, Harter PN, Buxmann H, Allwinn R, et al. (2011) Problems and challenges in the diagnosis of vertical infection with human cytomegalovirus (CMV): lessons from two accidental cases. J Clin Virol 51: 285-288.
4. Enders G, Daiminger A, Bader U, Exler S, Enders M, (2011) Intrauterine transmission and clinical outcome of 248 pregnancies with primary cytomegalovirus infection in relation to gestational age. J Clin Virol 52: 244-246.
5. Pereira L, Maidji E, (2008) Cytomegalovirus infection in the human placenta: maternal immunity and developmentally regulated receptors on trophoblasts converge. Curr Top Microbiol Immunol 325: 383-395.
6. Manaster I, Mandelboim O, (2010) The unique properties of uterine NK cells. Am J Reprod Immunol 63: 434-444.
7. Whitelaw PF, Croy BA, (1996) Granulated lymphocytes of pregnancy. Placenta 17: 533-543.
8. Vacca P, Pietra G, Falco M, Romeo E, Bottino C, et al. (2006) Analysis of natural killer cells isolated from human decidua: Evidence that 2B4 (CD244) functions as an inhibitory receptor and blocks NK-cell function. Blood 108: 4078-4085.
9. El Costa H, Casemayou A, Aguerre-Girr M, Rabot M, Berrebi A, et al. (2008) Critical and differential roles of NKp46- and NKp30-activating receptors expressed by uterine NK cells in early pregnancy. J Immunol 181: 3009-3017.
10. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, et al. (2006) Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 12: 1065-1074.
11. Keskin DB, Allan DS, Rybalov B, Andzelm MM, Stern JN, et al. (2007) TGFbeta promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells. Proc Natl Acad Sci U S A 104: 3378-3383.
12. Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, et al. (2003) Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med 198: 1201-1212.
13. Le Bouteiller P, Siewiera J, Casart Y, Aguerre-Girr M, El Costa H, et al. (2011) The human decidual NK-cell response to virus infection: what can we learn from circulating NK lymphocytes? J Reprod Immunol 88: 170-175.
14. Santoni A, Carlino C, Gismondi A, (2008) Uterine NK cell development, migration and function. Reprod Biomed Online 16: 202-210.
15. Vacca P, Cantoni C, Vitale M, Prato C, Canegallo F, et al. (2010) Crosstalk between decidual NK and CD14+ myelomonocytic cells results in induction of Tregs and immunosuppression. Proc Natl Acad Sci U S A 107: 11918-11923.
16. Cooper MA, Fehniger TA, Caligiuri MA, (2001) The biology of human natural killer-cell subsets. Trends Immunol 22: 633-640.
17. Hanna J, Bechtel P, Zhai Y, Youssef F, McLachlan K, et al. (2004) Novel insights on human NK cells' immunological modalities revealed by gene expression profiling. J Immunol 173: 6547-6563.
18. Male V, Hughes T, McClory S, Colucci F, Caligiuri MA, et al. (2010) Immature NK cells, capable of producing IL-22, are present in human uterine mucosa. J Immunol 185: 3913-3918.
19. Male V, Trundley A, Gardner L, Northfield J, Chang C, et al. (2010) Natural killer cells in human pregnancy. Methods Mol Biol 612: 447-463.
20. King A, Kalra P, Loke YW, (1990) Human trophoblast cell resistance to decidual NK lysis is due to lack of NK target structure. Cell Immunol 127: 230-237.
21. Kopcow HD, Allan DS, Chen X, Rybalov B, Andzelm MM, et al. (2005) Human decidual NK cells form immature activating synapses and are not cytotoxic. Proc Natl Acad Sci U S A 102: 15563-15568.
22. Lopez-Botet M, Angulo A, Guma M, (2004) Natural killer cell receptors for major histocompatibility complex class I and related molecules in cytomegalovirus infection. Tissue Antigens 63: 195-203.
23. Kuijpers TW, Baars PA, Dantin C, van den Burg M, van Lier RA, et al. (2008) Human NK cells can control CMV infection in the absence of T cells. Blood 112: 914-915.
24. Lanier LL, (2008) Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 9: 495-502.
25. Saez-Borderias A, Romo N, Magri G, Guma M, Angulo A, et al. (2009) IL-12-dependent inducible expression of the CD94/NKG2A inhibitory receptor regulates CD94/NKG2C+ NK cell function. J Immunol 182: 829-836.
26. Alter G, Altfeld M, (2009) NK cells in HIV-1 infection: evidence for their role in the control of HIV-1 infection. J Intern Med 265: 29-42.
27. Orr MT, Murphy WJ, Lanier LL, (2010) 'Unlicensed' natural killer cells dominate the response to cytomegalovirus infection. Nat Immunol 11: 321-327.
28. Alter G, Heckerman D, Schneidewind A, Fadda L, Kadie CM, et al. (2011) HIV-1 adaptation to NK-cell-mediated immune pressure. Nature 476: 96-100.
29. Waggoner SN, Cornberg M, Selin LK, Welsh RM, (2011) Natural killer cells act as rheostats modulating antiviral T cells. Nature 481: 394-8.
30. Lopez-Verges S, Milush JM, Schwartz BS, Pando MJ, Jarjoura J, et al. (2011) Expansion of a unique CD57NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci U S A 108: 14725-14732.
31. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, et al. (2011) Innate or adaptive immunity? The example of natural killer cells. Science 331: 44-49.
32. Markel G, Wolf D, Hanna J, Gazit R, Goldman-Wohl D, et al. (2002) Pivotal role of CEACAM1 protein in the inhibition of activated decidual lymphocyte functions. J Clin Invest 110: 943-953.
33. Mselle TF, Howell AL, Ghosh M, Wira CR, Sentman CL, (2009) Human uterine natural killer cells but not blood natural killer cells inhibit human immunodeficiency virus type 1 infection by secretion of CXCL12. J Virol 83: 11188-11195.
34. Orange JS, (2008) Formation and function of the lytic NK-cell immunological synapse. Nat Rev Immunol 8: 713-725.
35. Mentlik AN, Sanborn KB, Holzbaur EL, Orange JS, (2010) Rapid lytic granule convergence to the MTOC in natural killer cells is dependent on dynein but not cytolytic commitment. Mol Biol Cell 21: 2241-2256.
36. Rak GD, Mace EM, Banerjee PP, Svitkina T, Orange JS, (2011) Natural killer cell lytic granule secretion occurs through a pervasive actin network at the immune synapse. PLoS Biol 9: e1001151.
37. Blaschitz A, Weiss U, Dohr G, Desoye G, (2000) Antibody reaction patterns in first trimester placenta: implications for trophoblast isolation and purity screening. Placenta 21: 733-741.
38. Toledo MS, Suzuki E, Handa K, Hakomori S, (2005) Effect of ganglioside and tetraspanins in microdomains on interaction of integrins with fibroblast growth factor receptor. J Biol Chem 280: 16227-16234.
39. Davis DM, Chiu I, Fassett M, Cohen GB, Mandelboim O, et al. (1999) The human natural killer cell immune synapse. Proc Natl Acad Sci U S A 96: 15062-15067.
40. Inoue H, Miyaji M, Kosugi A, Nagafuku M, Okazaki T, et al. (2002) Lipid rafts as the signaling scaffold for NK cell activation: tyrosine phosphorylation and association of LAT with phosphatidylinositol 3-kinase and phospholipase C-gamma following CD2 stimulation. Eur J Immunol 32: 2188-2198.
41. Arnon TI, Achdout H, Levi O, Markel G, Saleh N, et al. (2005) Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat Immunol 6: 515-523.
42. Prod'homme V, Tomasec P, Cunningham C, Lemberg MK, Stanton RJ, et al. (2012) Human cytomegalovirus UL40 signal peptide regulates cell surface expression of the NK cell ligands HLA-E and gpUL18. J Immunol 188: 2794-2804.
43. Tomasec P, Braud VM, Rickards C, Powell MB, McSharry BP, et al. (2000) Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287: 1031.
44. Guma M, Angulo A, Lopez-Botet M, (2006) NK cell receptors involved in the response to human cytomegalovirus infection. Curr Top Microbiol Immunol 298: 207-223.
45. Guma M, Budt M, Saez A, Brckalo T, Hengel H, et al. (2006) Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 107: 3624-3631.
46. Dumortier J, Streblow DN, Moses AV, Jacobs JM, Kreklywich CN, et al. (2008) Human cytomegalovirus secretome contains factors that induce angiogenesis and wound healing. J Virol 82: 6524-6535.
47. Kuhn JR, Poenie M, (2002) Dynamic polarization of the microtubule cytoskeleton during CTL-mediated killing. Immunity 16: 111-121.
48. Trambas CM, Griffiths GM, (2003) Delivering the kiss of death. Nat Immunol 4: 399-403.
49. Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM, (2006) Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443: 462-465.
50. Stinchcombe JC, Salio M, Cerundolo V, Pende D, Arico M, et al. (2011) Centriole polarisation to the immunological synapse directs secretion from cytolytic cells of both the innate and adaptive immune systems. BMC Biol 9: 45.
51. Straszewski-Chavez SL, Abrahams VM, Funai EF, Mor G, (2004) X-linked inhibitor of apoptosis (XIAP) confers human trophoblast cell resistance to Fas-mediated apoptosis. Mol Hum Reprod 10: 33-41.
52. Kalkunte SS, Mselle TF, Norris WE, Wira CR, Sentman CL, et al. (2009) Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface. J Immunol 182: 4085-4092.
53. Chen X, Trivedi PP, Ge B, Krzewski K, Strominger JL, (2007) Many NK cell receptors activate ERK2 and JNK1 to trigger microtubule organizing center and granule polarization and cytotoxicity. Proc Natl Acad Sci U S A 104: 6329-6334.
54. Delahaye NF, Rusakiewicz S, Martins I, Menard C, Roux S, et al. (2011) Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors. Nat Med 17: 700-707.
55. Eagle RA, Traherne JA, Hair JR, Jafferji I, Trowsdale J, (2009) ULBP6/RAET1L is an additional human NKG2D ligand. Eur J Immunol 39: 3207-3216.
56. Bennett NJ, Ashiru O, Morgan FJ, Pang Y, Okecha G, et al. (2010) Intracellular sequestration of the NKG2D ligand ULBP3 by human cytomegalovirus. J Immunol 185: 1093-1102.
57. Kaiser BK, Barahmand-Pour F, Paulsene W, Medley S, Geraghty DE, et al. (2005) Interactions between NKG2x immunoreceptors and HLA-E ligands display overlapping affinities and thermodynamics. J Immunol 174: 2878-2884.
58. Hanna J, Gonen-Gross T, Fitchett J, Rowe T, Daniels M, et al. (2004) Novel APC-like properties of human NK cells directly regulate T cell activation. J Clin Invest 114: 1612-1623.
59. Zingoni A, Sornasse T, Cocks BG, Tanaka Y, Santoni A, et al. (2004) Cross-talk between activated human NK cells and CD4+ T cells via OX40-OX40 ligand interactions. J Immunol 173: 3716-3724.
60. Slinger E, Maussang D, Schreiber A, Siderius M, Rahbar A, et al. (2010) HCMV-encoded chemokine receptor US28 mediates proliferative signaling through the IL-6-STAT3 axis. Sci Signal 3: ra58.
61. Hurst SM, Wilkinson TS, McLoughlin RM, Jones S, Horiuchi S, et al. (2001) Il-6 and its soluble receptor orchestrate a temporal switch in the pattern of leukocyte recruitment seen during acute inflammation. Immunity 14: 705-714.
62. Nordoy I, Muller F, Nordal KP, Rollag H, Aukrust P, et al. (2000) Chemokines and soluble adhesion molecules in renal transplant recipients with cytomegalovirus infection. Clin Exp Immunol 120: 333-337.
63. Muntasell A, Magri G, Pende D, Angulo A, Lopez-Botet M, (2010) Inhibition of NKG2D expression in NK cells by cytokines secreted in response to human cytomegalovirus infection. Blood 115: 5170-5179.
64. Nguyen KB, Salazar-Mather TP, Dalod MY, Van Deusen JB, Wei XQ, et al. (2002) Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J Immunol 169: 4279-4287.
65. Gur C, Doron S, Kfir-Erenfeld S, Horwitz E, Abu-Tair L, et al. (2012) NKp46-mediated killing of human and mouse hepatic stellate cells attenuates liver fibrosis. Gut 61: 885-893.
66. Ohira M, Ishiyama K, Tanaka Y, Doskali M, Igarashi Y, et al. (2009) Adoptive immunotherapy with liver allograft-derived lymphocytes induces anti-HCV activity after liver transplantation in humans and humanized mice. J Clin Invest 119: 3226-3235.
67. Rauwel B, Mariame B, Martin H, Nielsen R, Allart S, et al. (2010) Activation of peroxisome proliferator-activated receptor gamma by human cytomegalovirus for de novo replication impairs migration and invasiveness of cytotrophoblasts from early placentas. J Virol 84: 2946-2954.
68. Didier C, Merdes A, Gairin JE, Jabrane-Ferrat N, (2008) Inhibition of proteasome activity impairs centrosome-dependent microtubule nucleation and organization. Mol Biol Cell 19: 1220-1229.
69. Jabrane-Ferrat N, Campbell MJ, Esserman LJ, Peterlin BM, (2006) Challenge with mammary tumor cells expressing MHC class II and CD80 prevents the development of spontaneously arising tumors in MMTV-neu transgenic mice. Cancer Gene Ther 13: 1002-1010.