Human cytomegalovirus infection of placental cytotrophoblasts in vitro and in utero: Implications for transmission and pathogenesis

Journal of Virology

Volumn 74, Issue 15, 2000, Pages 6808-6820

  Fisher, Susan ^a   Genbacev, Olga ^a   Maidji, Ekaterina ^a   Pereira, Lenore ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHORION VILLUS; CYTOMEGALOVIRUS INFECTION; CYTOTROPHOBLAST; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SYNCYTIOTROPHOBLAST; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS TRANSMISSION;

CELLS, CULTURED; CHORIONIC VILLI; CULTURE TECHNIQUES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DISEASE TRANSMISSION, VERTICAL; DOWN-REGULATION; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; INTEGRIN ALPHA1BETA1; INTEGRINS; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; TROPHOBLASTS; VIRAL PROTEINS; VIRION; VIRUS REPLICATION;

EID: 0033912557     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.15.6808-6820.2000     Document Type: Article

References (66)

1. Benirschke, K., G. R. Mendoza, and P. L. Bazeley. 1974. Placental and fetal manifestations of cytomegalovirus infection. Virchows Arch. B Cell Pathol. 16:121-139.
2. Boppana, S. B., and W. J. Britt. 1995. Antiviral antibody responses and intrauterine transmission after primary maternal cytomegalovirus infection. J. Infect. Dis. 171:1115-1121.
3. Britt, W. J. 1999. Congenital cytomegalovirus infection, p. 269-281. In P. J. Hitchcock. H. T. MacKay, and J. N. Wasserheit (ed.), Sexually transmitted diseases and adverse outcomes of pregnancy. ASM Press, Washington, D.C.
4. Chandler, S. H., E. R. Alexander, and K. K. Holmes. 1985. Epidemiology of cytomegaloviral infection in a heterogeneous population of pregnant women. J. Infect. Dis. 152:249-256.
5. Chandler, S. H., H. H. Handsfield, and J. K. McDougall. 1987. Isolation of multiple strains of cytomegalovirus from women attending a clinic for sexually transmitted disease. J. Infect. Dis. 155:655-660.
6. Chandler, S. H., K. K. Holmes, B. B. Wentworth, L. T. Gutman, P. J. Wiesner, E. R. Alexander, and H. H. Handsfield. 1985. The epidemiology of cytomegaloviral infection in women attending a sexually transmitted disease clinic. J. Infect. Dis, 152:597-605.
7. Coonrod, D., A. C. Collier, R. Ashley, T. DeRouen, and L. Corey. 1998. Association between cytomegalovirus seroconversion and upper genital tract infection among women attending a sexually transmitted disease clinic: a prospective study. J. Infect. Dis. 177:1188-1193.
8. Cross, J. C., S. Lam, S. Yagel, and Z. Werb. 1999. Defective induction of the transcription factor interferon-stimulated gene factor-3 and interferon alpha insensitivity in human trophoblast cells. Biol. Reprod. 60:312-321.
9. Cross, J. C., Z. Werb, and S. J. Fisher. 1994. Implantation and the placenta: key pieces of the development puzzle. Science 266:1508-1518.
10. Damsky, C. H., and S. J. Fisher. 1998. Trophoblast pseudo-vasculogenesis: faking it with endothelial adhesion receptors. Curr. Opin. Cell Biol. 10:660-666.
11. Damsky, C. H., M. L. Fitzgerald, and S. J. Fisher. 1992. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J. Clin. Investig. 89:210-222.
12. Damsky, C. H., C. Librach, K. H. Lim, M. L. Fitzgerald, M. T. McMaster, M. Janatpour, Y. Zhou, S. K. Logan, and S. J. Fisher. 1994. Integrin switching regulates normal trophoblast invasion. Development 120:3657-3666.
13. de Jong, M. D., G. J. Galasso, B. Gazzard, P. D. Griffiths, D. A. Jabs, E. R. Kern, and S. A. Spector. 1998. Summary of the II International Symposium on Cytomegalovirus. Antiviral Res. 39:141-162.
14. Dondero, D. V., and L. Pereira. 1990. Monoclonal antibody production, p. 101-124. In R. Emmons and N. Schmidt (ed.), Diagnostic procedures for viral, rickettsial and chlamydial infections. American Public Health Association, Washington, D.C.
15. Fisher, S. J., T. Y. Cui, L. Zhang, L. Hartman, K. Grahl, G. Y. Zhang, J. Tarpey, and C. H. Damsky. 1989. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J. Cell Biol. 109:891-902.
16. Fisher, S. J., M. S. Leitch, M. S. Kantor, C. B. Basbaum, and R. H. Kramer. 1985. Degradation of extracellular matrix by the trophoblastic cells of first-trimester human placentas. J. Cell. Biochem. 27:31-41.
17. Fowler, K. B., and R. F. Pass. 1991. Sexually transmitted diseases in mothers of neonates with congenital cytomegalovirus infection. J. Infect. Dis. 164: 259-264.
18. Fowler, K. B., S. Stagno, R. F. Pass, W. J. Britt, T. J. Boll, and C. A. Alford. 1992. The outcome of congenital cytomegalovirus infection in relation to maternal antibody status. N. Engl. J. Med. 326:663-667.
19. Funikawa, T., F. Jisaki, D. Sakamuro, T. Takegami, and T. Murayama. 1994. Detection of human cytomegalovirus genome in uterus tissue. Arch. Virol. 135:265-277.
20. Genbacev, O., S. A. Schubach, and R. K. Miller. 1992. Villous culture of first trimester human placenta-model to study extravillous trophoblast (EVT) differentiation. Placenta 13:439-461.
21. Goldenberg, R. L., W. W. Andrews, A. Yuan, H. T. MacKay, and M. St. Louis. 1999. Pregnancy outcomes related to sexually transmitted diseases, p. 1-24. In P. J. Hitchcock, H. T. MacKay, and J. N. Wasserheit (ed.), Sexually transmitted diseases and adverse outcomes of pregnancy. ASM Press, Washington, D.C.
22. Grefte, A., M. van der Giessen, W. van Son, and T. H. The. 1993. Circulating cytomegalovirus (CMV)-infected endothelial cells in patients with an active CMV infection. J. Infect. Dis. 167:270-277.
23. Griffith, B. P., S. R. McCormick, C. K. Fong, J. T. Lavallee, H. L. Lucia, and E. Goff. 1985. The placenta as a site of cytomegalovirus infection in guinea pigs. J. Virol. 55:402-409.
24. Griffiths, P. D., and C. Baboonian. 1984. A prospective study of primary cytomegalovirus infection during pregnancy: final report. Br. J. Obstet. Gynaecol. 91:307-315.
25. Hahn, G., R. Jores, and E. S. Mocarski. 1998. Cytomegalovirus remains latent in a common precursor of dendritic and myeloid cells. Proc. Natl. Acad. Sci. USA 95:3937-3942.
26. Halwachs-Baumann, G., M. Wilders-Truschnig, G. Desoye, T. Hahn, L. Kiesel, K. Klingel, P. Rieger, G. Jahn, and C. Sinzger. 1998. Human trophoblast cells are permissive to the complete replicative cycle of human cytomegalovirus. J. Virol. 72:7598-7602.
27. Handsfield, H. H., S. H. Chandler, V. A. Caine, J. D. Meyers, L. Corey, E. Medeiros, and J. K. McDougall. 1985. Cytomegalovirus infection in sex partners: evidence for sexual transmission. J. Infect. Dis. 151:344-348.
28. Hayes, K., and H. Gibas. 1971. Placental cytomegalovirus infection without fetal involvement following primary infection in pregnancy. J. Pediatr. 79: 401-405.
29. Hemmings, D. G., R. Kilani, C. Nykiforuk, J. Preiksaitis, and L. J. Guilbert. 1998. Permissive cytomegalovirus infection of primary villous term and first trimester trophoblasts. J. Virol. 72:4970-4979.
30. Hutto, C., R. Ricks, M. Garvie, and R. F. Pass. 1985. Epidemiology of cytomegalovirus infections in young children: day care vs. home care. Pediatr. Infect. Dis. 4:149-152.
31. Islas, A. S., G. J. Demmler, J. G. Dobbins, and J. A. Stewart. 1995. Surveillance for congenital cytomegalovirus disease: a report from the National Congenital Cytomegalovirus Disease Registry. Clin. Infect. Dis. 20:665-670.
32. Jones, T. R., L. K. Hanson, L. Sun, J. S. Slater, R. M. Stenberg, and A. E. Campbell. 1995. Multiple independent loci within the human cytomegalovirus unique short region down-regulate expression of major histocompatibility complex class I heavy chains. J. Virol. 69:4830-4841.
33. Jones, T. R., and V. P. Muzithras. 1992. A cluster of dispensable genes within the human cytomegalovirus genome short component: IRS1, US1 through US5, and the US6 family. J. Virol. 66:2541-2546.
34. Kondo, K., H. Kaneshima, and E. S. Mocarski. 1994. Human cytomegalovirus latent infection of granulocyte-macrophage progenitors. Proc. Natl. Acad. Sci. USA 91:11879-11883.
35. Kovats, S., E. K. Main, C. Librach, M. Stubblebine, S. J. Fisher, and R. DeMars. 1990, A class I antigen. HLA-G, expressed in human trophoblasts. Science 248:220-223.
36. Kristoffersen, E. K., and R. Matre. 1996. Co-localization of the neonatal Fc gamma receptor and IgG in human placental term syncytiotrophoblasts. Eur. J. Immunol. 26:1668-1671.
37. Lazzarotto, T., P. Spezzacatena, P. Pradelli, D. A. Abate, S. Varani, and M. P. Landini. 1997. Avidity of immunoglobulin G directed against human cytomegalovirus during primary and secondary infections in immunocompetent and immunocompromised subjects. Clin. Diagn. Lab. Immunol. 4:469-473.
38. Leach, J. L., D. D. Sedmak, J. M. Osborne, B. Rahill, M. D. Lairmore, and C. L. Anderson. 1996. Isolation from human placenta of the IgG transporter. FcRn, and localization to the syncytiotrophoblast: implications for maternal-fetal antibody transport. J. Immunol. 157:3317-3322.
39. Leiser, R., and P. Kaufmann. 1994. Placental structure: in a comparative aspect. Exp. Clin. Endocrinol. 102:122-134.
40. Librach, C. L., Z. Werb, M. L. Fitzgerald, K. Chiu, N. M. Corwin, R. A. Esteves, D. Grobelny, R. Galardy, C. H. Damsky, and S. J. Fisher. 1991. 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J. Cell Biol. 113:437-449.
41. Lim, K. H., Y. Zhou, M. Janatpour, M. McMaster, K. Bass, S. H. Chun, and S. J. Fisher. 1997. Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia. Am. J. Pathol. 151:1809-1818.
42. McMaster, M., Y. Zhou, S. Shorter, K. Kapasi, D. Geraghty, K. H. Lim, and S. Fisher. 1998. HLA-G isoforms produced by placental cytotrophoblasts and found in amniotic fluid are due to unusual glycosylation. J. Immunol. 160:5922-5928.
43. McMaster, M. T., C. L. Librach, Y. Zhou, K. H. Lim, M. J. Janatpour, R. DeMars, S. Kovats, C. Damsky, and S. J. Fisher. 1995. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J. Immunol. 154:3771-3778.
44. Mostoufi-zadeh, M., S. G. Driscoll, S. A. Biano, and R. B. Kundsin. 1984. Placental evidence of cytomegalovirus infection of the fetus and neonate. Arch. Pathol. Lab. Med. 108:403-406.
45. Mühlemann, K., R. K. Miller, L. Metlay, and M. A. Menegus. 1992. Cytomegalovirus infection of the human placenta: an immunocytochemical study. Hum. Pathol. 23:1234-1237.
46. Navarro, D., P. Paz, S. Tugizov, K. Topp, J. La Vail, and L. Pereira. 1993. Glycoprotein B of human cytomegalovirus promotes virion penetration into cells, transmission of infection from cell to cell, and fusion of infected cells. Virology 197:143-158.
47. Pass, R. F., E. A. Little, S. Stagno, W. J. Britt, and C. A. Alford. 1987. Young children as a probable source of maternal and congenital cytomegalovirus infection. N. Engl. J. Med. 316:1366-1370.
48. Robertson, W. B., I. Brosens, and G. Dixon. 1976. Maternal uterine vascular lesions in the hypertensive complications of pregnancy. Perspect. Nephrol. Hypertens. 5:115-127.
49. Romero, R., R. Gomez, M. Mazor, F. Ghezzi, and B. H. Yoon. 1997. The preterm labor syndrome, p. 29-49. In M. Elder, R. F. Lamont, and R. Romero (ed.), Preterm labor. Churchill Livingstone, New York, N. Y.
50. Roth, I., D. B. Corry, R. M. Locksley, J. S. Abrams, M. J. Litton, and S. J. Fisher. 1996. Human placental cytotrophoblasts produce the immunosuppressive cytokine interleukin 10. J. Exp. Med. 184:539-548.
51. Roth, I., and S. J. Fisher. 1999. IL-10 is an autocrine inhibitor of human placental cytotrophoblast MMP-9 production and invasion. Dev. Biol. 205: 194-204.
52. Schust, D. J., D. Tortorella, J. Seebach, C. Phan, and H. L. Ploegh. 1998. Trophoblast class I major histocompatibility complex (MHC) products are resistant to rapid degradation imposed by the human cytomegalovirus (HCMV) gene products US2 and US11. J. Exp. Med. 188:497-503.
53. Simister, N. E., C. M. Story, H. L. Chen, and J. S. Hunt. 1996. An IgG-transporting Fc receptor expressed in the syncytiotrophoblast of human placenta. Eur. J. Immunol. 26:1527-1531.
54. Sinzger, C., A. Grefte, B. Plachter, A. S. Gouw, T. H. The, and G. Jahn. 1995. Fibroblasts, epithelial cells, endothelial cells and smooth muscle cells are major targets of human cytomegalovirus infection in lung and gastrointestinal tissues. J. Gen. Virol. 76:741-750.
55. Sinzger, C., H. Müntefering, T. Löning, H. Stöss, B. Plachter, and G. Jahn. 1993. Cell types infected in human cytomegalovirus placentitis identified by immunohistochemical double staining. Virchows Arch. A Pathol. Anat. Histopathol. 423:249-256.
56. Soderberg-Naucler, C., K. N. Fish, and J. A. Nelson. 1997. Reactivation of latent human cytomegalovirus by allogeneic stimulation of blood cells from healthy donors. Cell 91:119-126.
57. Sohn, Y. M., M. K. Oh, K. B. Balcarek, G. A. Cloud, and R. F. Pass. 1991. Cytomegalovirus infection in sexually active adolescents. J. Infect. Dis. 163: 460-463.
58. Stagno, S., R. F. Pass, G. Cloud, W. J. Britt, R. E. Henderson, P. D. Walton, D. A. Veren, F. Page, and C. A. Alford. 1986. Primary cytomegalovirus infection in pregnancy. Incidence, transmission to fetus, and clinical outcome. JAMA 256:1904-1908.
59. Stagno, S., R. F. Pass, M. E. Dworsky, R. E. Henderson, E. G. Moore, P. D. Walton, and C. A. Alford. 1982. Congenital cytomegalovirus infection: the relative importance of primary and recurrent maternal infection. N. Engl. J. Med. 306:945-949.
60. Stagno, S., D. Reynolds, A. Tsiantos, D. A. Fuccillo, R. Smith, M. Tiller, and C. A. Alford, Jr. 1975. Cervical cytomegalovirus excretion in pregnant and nonpregnant women: suppression in early gestation. J. Infect. Dis. 131:522-527.
61. Starkey, P. M., I. L. Sargent, and C. W. Redman. 1988. Cell populations in human early pregnancy decidua: characterization and isolation of large granular lymphocytes by flow cytometry. Immunology 65:129-134.
62. Story, C. M., J. E. Mikulska, and N. E. Simister. 1994. A major histocomv patibility complex class I-like Fc receptor cloned from human placenta: possible role in transfer of immunoglobulin G from mother to fetus. J. Exp. Med. 180:2377-2381.
63. Waldman, W. J., D. A. Knight, E. H. Huang, and D. D. Sedmak. 1995. Bidirectional transmission of infectious cytomegalovirus between monocytes and vascular endothelial cells: an in vitro model. J. Infect. Dis. 171:263-272.
64. Zhou, Y., C. H. Damsky, K. Chiu, J. M. Roberts, and S. J. Fisher. 1993. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J. Clin. Investig. 91:950-960.
65. Zhou, Y., C. H. Damsky, and S. J. Fisher. 1997. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype: one cause of defective endovascular invasion in this syndrome? J. Clin. Investig. 99:2152-2164.
66. Zhou, Y., S. J. Fisher, M. Janatpour, O. Genbacev, E. Dejana, M. Wheelock, and C. H. Damsky. 1997. Human cytotrophoblasts adopt a vascular phenotype as they differentiate: a strategy for successful endovascular invasion? J. Clin. Investig. 99:2139-2151.