HHV-6A infection of endometrial epithelial cells induces increased endometrial NK cell-mediated cytotoxicity

Frontiers in Microbiology

Volumn 8, Issue DEC, 2017, Pages

  Caselli, Elisabetta ^a   Bortolotti, Daria ^a   Marci, Roberto ^b   Rotola, Antonella ^a   Gentili, Valentina ^a   Soffritti, Irene ^a   D'Accolti, Maria ^a   Lo Monte, Giuseppe ^c   Sicolo, Mariangela ^a   Barao, Isabel ^d   Di Luca, Dario ^a   Rizzo, Roberta ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c Brunico Hospital   (Italy)

^d UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

Endometrium; Epithelial cell; HHV 6; Infertility; NK cell

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CX3CR1; CHEMOKINE RECEPTOR CXCR3; EOTAXIN 3; FAS LIGAND; MONOCYTE CHEMOTACTIC PROTEIN 1;

ARTICLE; CONTROLLED STUDY; DNA DETERMINATION; DNA EXTRACTION; ENDOMETRIUM BIOPSY; ENDOMETRIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FEMALE; FEMALE INFERTILITY; FLOW CYTOMETRY; HUMAN; HUMAN HERPESVIRUS 6; HUMAN HERPESVIRUS 6 INFECTION; HUMAN TISSUE; IMMUNOFLUORESCENCE; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; STROMA CELL; TUBAL PATENCY TEST; VIRUS INFECTION;

EID: 85038014508     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.02525     Document Type: Article

References (49)

1. Ablashi, D., Agut, H., Alvarez-Lafuente, R., Clark, D. A., Dewhurst, S., DiLuca, D., et al. (2014). Classification of HHV-6A and HHV-6B as distinct viruses. Arch. Virol. 159, 863-870. doi: 10.1007/s00705-013-1902-5
2. Aguera-Gonzalez, S., Gross, C. C., Fernandez-Messina, L., Ashiru, O., Esteso, G., Hang, H. C., et al. (2011). Palmitoylation of MICA, a ligand for NKG2D, mediates its recruitment to membrane microdomains and promotes its shedding. Eur. J. Immunol. 41, 3667-3676. doi: 10.1002/eji.201141645
3. Alter, G., Malenfant, J. M., and Altfeld, M. (2004). CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294, 15-22. doi: 10.1016/j.jim.2004.08.008
4. Bachmayer, N., Rafik Hamad, R., Liszka, L., Bremme, K., and Sverremark-Ekstrom, E. (2006). Aberrant uterine natural killer (NK)-cell expression and altered placental and serum levels of the NK-cell promoting cytokine interleukin-12 in pre-eclampsia. Am. J. Reprod. Immunol. 56, 292-301. doi: 10.1111/j.1600-0897.2006.00429.x
5. Benagiano, M., Gerosa, M., Romagnoli, J., Mahler, M., Borghi, M. O., Grassi, A., et al. (2017). β2 glycoprotein I recognition drives Th1 inflammation in atherosclerotic plaques of patients with primary antiphospholipid syndrome. J. Immunol. 198, 2640-2648. doi: 10.4049/jimmunol.1600305
6. Bulmer, J. N., Morrison, L., Longfellow, M., Ritson, A., and Pace, D. (1991). Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum. Reprod. 6, 791-798. doi: 10.1093/oxfordjournals.humrep.a137430
7. Caselli, E., and Di Luca, D. (2007). Molecular biology and clinical associations of Roseoloviruses human herpesvirus 6 and human herpesvirus 7. New Microbiol. 30, 173-187
8. Caselli, E., Zatelli, M. C., Rizzo, R., Benedetti, S., Martorelli, D., Trasforini, G., et al. (2012). Virologic and immunologic evidence supporting an association between HHV-6 and Hashimoto's thyroiditis. PLOS Pathog. 8:e1002951. doi: 10.1371/journal.ppat.1002951
9. Clifford, K., Flanagan, A. M., and Regan, L. (1999). Endometrial CD56+ natural killer cells in women with recurrent miscarriage: a histomorphometric study. Hum. Reprod. 14, 2727-2730. doi: 10.1093/humrep/14.11.2727
10. Eide, I. P., Rolfseng, T., Isaksen, C. V., Mecsei, R., Roald, B., Lydersen, S., et al. (2006). Serious foetal growth restriction is associated with reduced proportions of natural killer cells in decidua basalis. Virchows Arch. 448, 269-276. doi: 10.1007/s00428-005-0107-z
11. Flamand, L., Gosselin, J., D'Addario, M., Hiscott, J., Ablashi, D. V., Gallo, R. C., et al. (1991). Human herpesvirus 6 induces interleukin-1 beta and tumor necrosis factor alpha, but not interleukin-6, in peripheral blood mononuclear cell cultures. J. Virol. 65, 5105-5110
12. Flamand, L., Gosselin, J., Stefanescu, I., Ablashi, D., and Menezes, J. (1995). Immunosuppressive effect of human herpesvirus 6 on T-cell functions: suppression of interleukin-2 synthesis and cell proliferation. Blood 85, 1263-1271
13. Grivel, J. C., Santoro, F., Chen, S., Faga, G., Malnati, M. S., Ito, Y., et al. (2003). Pathogenic effects of human herpesvirus 6 in human lymphoid tissue ex vivo. J. Virol. 77, 8280-8289. doi: 10.1128/JVI.77.15.8280-8289.2003
14. Hanna, J., Goldman-Wohl, D., Hamani, Y., Avraham, I., Greenfield, C., Natanson-Yaron, S., 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
15. Janelle, M. E., and Flamand, L. (2006). Phenotypic alterations and survival of monocytes following infection by human herpesvirus-6. Arch. Virol. 151, 1603-1614. doi: 10.1007/s00705-005-0715-6
16. Jokhi, P. P., King, A., and Loke, Y. W. (1997). Cytokine production and cytokine receptor expression by cells of the human first trimester placental-uterine interface. Cytokine 9, 126-137. doi: 10.1006/cyto.1996.0146
17. Kakimoto, M., Hasegawa, A., Fujita, S., and Yasukawa, M. (2002). Phenotypic and functional alterations of dendritic cells induced by human herpesvirus 6 infection. J. Virol. 76, 10338-10345. doi: 10.1128/JVI.76.20.10338-10345.2002
18. Keskin, D. B., Allan, D. S., Rybalov, B., Andzelm, M. M., Stern, J. N., Kopcow, H. D., 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. doi: 10.1073/pnas.0611098104
19. Kitaya, K., Yamaguchi, T., Yasuo, T., Okubo, T., and Honjo, H. (2007). Post-ovulatory rise of endometrial CD16(-) natural killer cells: in situ proliferation of residual cells or selective recruitment from circulating peripheral blood? J. Reprod. Immunol. 76, 45-53. doi: 10.1016/j.jri.2007.03.010
20. Kopcow, H. D., Allan, D. S., Chen, X., Rybalov, B., Andzelm, M. M., Ge, B., 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. doi: 10.1073/pnas.0507835102
21. Lash, G. E., Schiessl, B., Kirkley, M., Innes, B. A., Cooper, A., Searle, R. F., et al. (2006). Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy. J. Leukoc. Biol. 80, 572-580. doi: 10.1189/jlb.0406250
22. Li, X. F., Charnock-Jones, D. S., Zhang, E., Hiby, S., Malik, S., Day, K., et al. (2001). Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J. Clin. Endocrinol. Metab. 86, 1823-1834. doi: 10.1210/jcem.86.4.7418
23. Lusso, P., De Maria, A., Malnati, M., Lori, F., DeRocco, S. E., Baseler, M., et al. (1991). Induction of CD4 and susceptibility to HIV-1 infection in human CD8+ T lymphocytes by human herpesvirus 6. Nature 349, 533-535. doi: 10.1038/349533a0
24. Lusso, P., and Gallo, R. C. (1995). Human herpesvirus 6. Baillieres Clin. Haematol. 8, 201-223. doi: 10.1016/S0950-3536(05)80238-0
25. Lusso, P., Markham, P. D., Tschachler, E., di Marzo Veronese, F., Salahuddin, S. Z., Ablashi, D. V., et al. (1988). In vitro cellular tropism of human B-lymphotropic virus (human herpesvirus-6). J. Exp. Med. 167, 1659-1670. doi: 10.1084/jem.167.5.1659
26. Lynch, L., Golden-Mason, L., Eogan, M., O'Herlihy, C., and O'Farrelly, C. (2007). Cells with haematopoietic stem cell phenotype in adult human endometrium: relevance to infertility? Hum. Reprod. 22, 919-926. doi: 10.1093/humrep/del456
27. Marci, R., Gentili, V., Bortolotti, D., Lo Monte, G., Caselli, E., Bolzani, S., et al. (2016). Presence of HHV-6A in endometrial epithelial cells from women with primary unexplained infertility. PLOS ONE 11:e0158304. doi: 10.1371/journal.pone.0158304
28. McCullers, J. A., Lakeman, F. D., and Whitley, R. J. (1995). Human herpesvirus 6 is associated with focal encephalitis. Clin. Infect. Dis. 21, 571-576. doi: 10.1093/clinids/21.3.571
29. Naruse, K., Lash, G. E., Bulmer, J. N., Innes, B. A., Otun, H. A., Searle, R. F., et al. (2009a). The urokinase plasminogen activator (uPA) system in uterine natural killer cells in the placental bed during early pregnancy. Placenta 30, 398-404. doi: 10.1016/j.placenta.2009.02.002
30. Naruse, K., Lash, G. E., Innes, B. A., Otun, H. A., Searle, R. F., Robson, S. C., et al. (2009b). Localization of matrix metalloproteinase (MMP)-2, MMP-9 and tissue inhibitors for MMPs (TIMPs) in uterine natural killer cells in early human pregnancy. Hum. Reprod. 24, 553-561. doi: 10.1093/humrep/den408
31. Nguyen, K. B., Salazar-Mather, T. P., Dalod, M. Y., Van Deusen, J. B., Wei, X. Q., Liew, F. Y., 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. doi: 10.4049/jimmunol.169.8.4279
32. Oliver-Minarro, D., Gil, J., Aguaron, A., Rodriguez-Mahou, M., Fernandez-Cruz, E., and Sanchez-Ramon, S. (2009). NK cell expansion in obstetrical antiphospholipid syndrome: guilty by association? Eur. J. Obstet. Gynecol. Reprod. Biol. 145:227. doi: 10.1016/j.ejogrb.2009.05.010
33. Pantry, S. N., and Medveczky, P. G. (2017). Latency, integration, and reactivation of human herpesvirus-6. Viruses 9:E194. doi: 10.3390/v9070194
34. Rizzo, R., Bortolotti, D., Fainardi, E., Gentili, V., Bolzani, S., Baldi, E., et al. (2016). KIR2DL2 inhibitory pathway enhances Th17 cytokine secretion by NK cells in response to herpesvirus infection in multiple sclerosis patients. J. Neuroimmunol. 294, 1-5. doi: 10.1016/j.jneuroim.2016.03.007
35. Rizzo, R., Fainardi, E., Rouas-Freiss, N., and Morandi, F. (2017). The role of HLA-class Ib molecules in immune-related diseases, tumors, and infections 2016. J. Immunol. Res. 2017:2309574. doi: 10.1155/2017/2309574
36. Saez-Borderias, A., Guma, M., Angulo, A., Bellosillo, B., Pende, D., and Lopez-Botet, M. (2006). Expression and function of NKG2D in CD4+ T cells specific for human cytomegalovirus. Eur. J. Immunol. 36, 3198-3206. doi: 10.1002/eji.200636682
37. Sandhoff, T., Kleim, J. P., and Schneweis, K. E. (1991). Latent human herpesvirus-6 DNA is sparsely distributed in peripheral blood lymphocytes of healthy adults and patients with lymphocytic disorders. Med. Microbiol. Immunol. 180, 127-134. doi: 10.1007/BF00206116
38. Schmiedel, D., Tai, J., Levi-Schaffer, F., Dovrat, S., and Mandelboim, O. (2016). Human herpesvirus 6B downregulates expression of activating ligands during lytic infection to escape elimination by natural killer cells. J. Virol. 90, 9608-9617. doi: 10.1128/JVI.01164-16
39. Siewiera, J., El Costa, H., Tabiasco, J., Berrebi, A., Cartron, G., Le Bouteiller, P., et al. (2013). Human cytomegalovirus infection elicits new decidual natural killer cell effector functions. PLOS Pathog. 9:e1003257. doi: 10.1371/journal.ppat.1003257
40. Smith, A., Santoro, F., Di Lullo, G., Dagna, L., Verani, A., and Lusso, P. (2003). Selective suppression of IL-12 production by human herpesvirus 6. Blood 102, 2877-2884. doi: 10.1182/blood-2002-10-3152
41. Smith, A. P., Paolucci, C., Di Lullo, G., Burastero, S. E., Santoro, F., and Lusso, P. (2005). Viral replication-independent blockade of dendritic cell maturation and interleukin-12 production by human herpesvirus 6. J. Virol. 79, 2807-2813. doi: 10.1128/JVI.79.5.2807-2813.2005
42. Soldan, S. S., Berti, R., Salem, N., Secchiero, P., Flamand, L., Calabresi, P. A., et al. (1997). Association of human herpes virus 6 (HHV-6) with multiple sclerosis: increased IgM response to HHV-6 early antigen and detection of serum HHV-6 DNA. Nat. Med. 3, 1394-1397. doi: 10.1038/nm1297-1394
43. Stallmach, T., Hebisch, G., Orban, P., and Lu, X. (1999). Aberrant positioning of trophoblast and lymphocytes in the feto-maternal interface with pre-eclampsia. Virchows Arch. 434, 207-211. doi: 10.1007/s004280050329
44. Takahashi, K., Sonoda, S., Higashi, K., Kondo, T., Takahashi, H., Takahashi, M., et al. (1989). Predominant CD4 T-lymphocyte tropism of human herpesvirus 6-related virus. J. Virol. 63, 3161-3163
45. Tuckerman, E., Laird, S. M., Prakash, A., and Li, T. C. (2007). Prognostic value of the measurement of uterine natural killer cells in the endometrium of women with recurrent miscarriage. Hum. Reprod. 22, 2208-2213. doi: 10.1093/humrep/dem141
46. Waldhauer, I., Goehlsdorf, D., Gieseke, F., Weinschenk, T., Wittenbrink, M., Ludwig, A., et al. (2008). Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 68, 6368-6376. doi: 10.1158/0008-5472.CAN-07-6768
47. Williams, P. J., Bulmer, J. N., Searle, R. F., Innes, B. A., and Robson, S. C. (2009). Altered decidual leucocyte populations in the placental bed in pre-eclampsia and foetal growth restriction: a comparison with late normal pregnancy. Reproduction 138, 177-184. doi: 10.1530/REP-09-0007
48. Wu, X., Jin, L. P., Yuan, M. M., Zhu, Y., Wang, M. Y., and Li, D. J. (2005). Human first-trimester trophoblast cells recruit CD56brightCD16-NK cells into decidua by way of expressing and secreting of CXCL12/stromal cell-derived factor 1. J. Immunol. 175, 61-68. doi: 10.4049/jimmunol.175.1.61
49. Yamanishi, K., Okuno, T., Shiraki, K., Takahashi, M., Kondo, T., Asano, Y., et al. (1988). Identification of human herpesvirus-6 as a causal agent for exanthem subitum. Lancet 1, 1065-1067. doi: 10.1016/S0140-6736(88)91893-4