HCMV infection of human trophoblast progenitor cells of the placenta is neutralized by a human monoclonal antibody to glycoprotein B and not by antibodies to the pentamer complex

Viruses

Volumn 6, Issue 3, 2014, Pages 1346-1364

  Zydek, Martin ^a   Petitt, Matthew ^a   Fang Hoover, June ^a   Adler, Barbara ^b   Kauvar, Lawrence M ^c   Pereira, Lenore ^a   Tabata, Takako ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

^c Trellis Bioscience   (United States)

Author keywords

Congenital; Development; HCMV; Hyperimmune globulin; Neutralization; Neutralizing; Pentamer; Placenta; Progenitors; Trophoblast

Indexed keywords

GLYCOPROTEIN B; HUMAN MONOCLONAL ANTIBODY; HYPERIMMUNE GLOBULIN;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; HUMAN; HUMAN CELL; HUMAN TROPHOBLAST PROGENITOR CELL; LIMIT OF DETECTION; LIMIT OF QUANTITATION; NONHUMAN; PLACENTA; PROGENY; QUANTITATIVE ASSAY; STEM CELL; SYNCYTIOTROPHOBLAST; TROPHOBLAST; TROPHOSPHERE FORMATION; VIRAL DISEASE IMMUNOFLUORESCENCE ASSAY; VIRUS NEUTRALIZATION; VIRUS TRANSMISSION;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CELLS, CULTURED; CYTOMEGALOVIRUS; FEMALE; HUMANS; PLACENTA; PREGNANCY; STEM CELLS; TROPHOBLASTS; VIRAL ENVELOPE PROTEINS; VIRAL TROPISM; VIRUS INTERNALIZATION;

EID: 84897896066     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v6031346     Document Type: Article

References (77)

1. Britt, W.J. Congenital cytomegalovirus infection. In Sexually Transmitted Diseases and Adverse Outcomes of Pregnancy; Hitchcock, P.J., MacKay, H.T., Wasserheit, J.N., Eds.; ASM Press: Washington, DC, USA, 1999; pp. 269-281.
2. Demmler, G.J. Congenital cytomegalovirus infection and disease. Adv. Pediatr. Infect. Dis. 1996, 11, 135-162.
3. Rivera, L.B.; Boppana, S.B.; Fowler, K.B.; Britt, W.J.; Stagno, S.; Pass, R.F. Predictors of hearing loss in children with symptomatic congenital cytomegalovirus infection. Pediatrics 2002, 110, 762-767.
4. Pereira, L.; Petitt, M.; Fong, A.; Tsuge, M.; Tabata, T.; Fang-Hoover, J.; Maidji, E.; Zydek, M.; Zhou, Y.; Inoue, N., et al. Intrauterine growth restriction caused by underlying congenital cytomegalovirus infection. J. Infect. Dis. 2014, doi:10.1093/infdis/jiu019.
5. Fowler, K.B.; Stagno, S.; Pass, R.F. Maternal immunity and prevention of congenital cytomegalovirus infection. JAMA 2003, 289, 1008-1011.
6. Yamamoto, A.Y.; Mussi-Pinhata, M.M.; Isaac Mde, L.; Amaral, F.R.; Carvalheiro, C.G.; Aragon, D.C.; Manfredi, A.K.; Boppana, S.B.; Britt, W.J. Congenital cytomegalovirus infection as a cause of sensorineural hearing loss in a highly immune population. Pediatr. Infect. Dis. J. 2011, 30, 1043-1046.
7. Ross, S.A.; Fowler, K.B.; Ashrith, G.; Stagno, S.; Britt, W.J.; Pass, R.F.; Boppana, S.B. Hearing loss in children with congenital cytomegalovirus infection born to mothers with preexisting immunity. J. Pediatr. 2006, 148, 332-336.
8. Mercorelli, B.; Sinigalia, E.; Loregian, A.; Palu, G. Human cytomegalovirus DNA replication: Antiviral targets and drugs. Rev. Med. Virol. 2008, 18, 177-210.
9. Benoist, G.; Leruez-Ville, M.; Magny, J.F.; Jacquemard, F.; Salomon, L.J.; Ville, Y. Management of pregnancies with confirmed cytomegalovirus fetal infection. Fetal. Diagn. Ther. 2013, 33, 203-214.
10. Nigro, G.; Adler, S.P.; Parruti, G.; Anceschi, M.M.; Coclite, E.; Pezone, I.; Di Renzo, G.C. Immunoglobulin therapy of fetal cytomegalovirus infection occurring in the first half of pregnancy-A case-control study of the outcome in children. J. Infect. Dis. 2012, 205, 215-227.
11. Buxmann, H.; Stackelberg, O.M.; Schlosser, R.L.; Enders, G.; Gonser, M.; Meyer-Wittkopf, M.; Hamprecht, K.; Enders, M. Use of cytomegalovirus hyperimmunoglobulin for prevention of congenital cytomegalovirus disease: A retrospective analysis. J. Perinat. Med. 2012, 40, 439-446.
12. Nigro, G.; Adler, S.P.; La Torre, R.; Best, A.M. Passive immunization during pregnancy for congenital cytomegalovirus infection. New Engl. J. Med. 2005, 353, 1350-1362.
13. Nigro, G.; Torre, R.L.; Pentimalli, H.; Taverna, P.; Lituania, M.; de Tejada, B.M.; Adler, S.P. Regression of fetal cerebral abnormalities by primary cytomegalovirus infection following hyperimmunoglobulin therapy. Prenat. Diagn. 2008, 28, 512-517.
14. Maidji, E.; Nigro, G.; Tabata, T.; McDonagh, S.; Nozawa, N.; Shiboski, S.; Muci, S.; Anceschi, M.M.; Aziz, N.; Adler, S.P.; Pereira, L. Antibody treatment promotes compensation for human cytomegalovirus-induced pathogenesis and a hypoxia-like condition in placentas with congenital infection. Am. J. Pathol. 2010, 177, 1298-1310.
15. Adler, S.P.; Nigro, G. Findings and conclusions from cmv hyperimmune globulin treatment trials. J. Clin. Virol. 2009, 46, S54-S57.
16. Nightingale, S.L. From the food and drug administration. JAMA 1990, 264, 2863.
17. Snydman, D.R.; Werner, B.G.; Heinze-Lacey, B.; Berardi, V.P.; Tilney, N.L.; Kirkman, R.L.; Milford, E.L.; Cho, S.I.; Bush, H.L., Jr.; Levey, A.S., et al. Use of cytomegalovirus immune globulin to prevent cytomegalovirus disease in renal-transplant recipients. New Engl. J. Med. 1987, 317, 1049-1054.
18. Ballow, M. Mechanisms of action of intravenous immune serum globulin therapy. Pediatr. Infect. Dis. J. 1994, 13, 806-811.
19. Macagno, A.; Bernasconi, N.L.; Vanzetta, F.; Dander, E.; Sarasini, A.; Revello, M.G.; Gerna, G.; Sallusto, F.; Lanzavecchia, A. Isolation of human monoclonal antibodies that potently neutralize human cytomegalovirus infection by targeting different epitopes on the gh/gl/ul128-131a complex. J. Virol. 2010, 84, 1005-1013.
20. Collarini, E.J.; Lee, F.E.; Foord, O.; Park, M.; Sperinde, G.; Wu, H.; Harriman, W.D.; Carroll, S.F.; Ellsworth, S.L.; Anderson, L.J., et al. Potent high-affinity antibodies for treatment and prophylaxis of respiratory syncytial virus derived from b cells of infected patients. J. Immunol. 2009, 183, 6338-6345.
21. Harriman, W.D.; Collarini, E.J.; Sperinde, G.V.; Strandh, M.; Fatholahi, M.M.; Dutta, A.; Lee, Y.; Mettler, S.E.; Keyt, B.A.; Ellsworth, S.L., et al. Antibody discovery via multiplexed single cell characterization. J. Immunol. Methods 2009, 341, 135-145.
22. Wrammert, J.; Smith, K.; Miller, J.; Langley, W.A.; Kokko, K.; Larsen, C.; Zheng, N.Y.; Mays, I.; Garman, L.; Helms, C., et al. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 2008, 453, 667-671.
23. McCutcheon, K.M.; Gray, J.; Chen, N.Y.; Liu, K.; Park, M.; Ellsworth, S.; Tripp, R.A.; Mark Tompkins, S.; Johnson, S.K., et al. Multiplexed screening of natural humoral immunity identifies antibodies at fine specificity for complex and dynamic viral targets. MAbs 2014, 6, 460-473.
24. Damsky, C.H.; Fisher, S.J. Trophoblast pseudo-vasculogenesis: Faking it with endothelial adhesion receptors. Curr. Opin. Cell Biol. 1998, 10, 660-666.
25. Zhou, Y.; Fisher, S.J.; Janatpour, M.; Genbacev, O.; Dejana, E.; Wheelock, M.; Damsky, C.H. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J. Clin. Invest. 1997, 99, 2139-2151.
26. Hemberger, M.; Udayashankar, R.; Tesar, P.; Moore, H.; Burton, G.J. Elf5-enforced transcriptional networks define an epigenetically regulated trophoblast stem cell compartment in the human placenta. Hum. Mol. Genet. 2010, 19, 2456-2467.
27. Genbacev, O.; Donne, M.; Kapidzic, M.; Gormley, M.; Lamb, J.; Gilmore, J.; Larocque, N.; Goldfien, G.; Zdravkovic, T.; McMaster, M.T.; Fisher, S.J. Establishment of human trophoblast progenitor cell lines from the chorion. Stem Cells 2011, 29, 1427-1436.
28. Genbacev, O.; Lamb, J.D.; Prakobphol, A.; Donne, M.; McMaster, M.T.; Fisher, S.J. Human trophoblast progenitors: Where do they reside? Semin. Reprod. Med. 2013, 31, 56-61.
29. 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, 6808-6820.
30. Maidji, E.; Genbacev, O.; Chang, H.T.; Pereira, L. Developmental regulation of human cytomegalovirus receptors in cytotrophoblasts correlates with distinct replication sites in the placenta. J. Virol. 2007, 81, 4701-4712.
31. Pereira, L.; Maidji, E.; McDonagh, S.; Genbacev, O.; Fisher, S. Human cytomegalovirus transmission from the uterus to the placenta correlates with the presence of pathogenic bacteria and maternal immunity. J. Virol. 2003, 77, 13301-13314.
32. Pereira, L.; Maidji, E.; McDonagh, S.; Tabata, T. Insights into viral transmission at the uterine-placental interface. Trends Microbiol. 2005, 13, 164-174.
33. 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, 527-537.
34. McDonagh, S.; Maidji, E.; Chang, H.T.; Pereira, L. Patterns of human cytomegalovirus infection in term placentas: A preliminary analysis. J. Clin. Virol. 2006, 35, 210-215.
35. Maidji, E.; McDonagh, S.; Genbacev, O.; Tabata, T.; Pereira, L. Maternal antibodies enhance or prevent cytomegalovirus infection in the placenta by neonatal fc receptor-mediated transcytosis. Am. J. Pathol. 2006, 168, 1210-1226.
36. Nozawa, N.; Fang-Hoover, J.; Tabata, T.; Maidji, E.; Pereira, L. Cytomegalovirus-specific, high-avidity igg with neutralizing activity in maternal circulation enriched in the fetal bloodstream. J. Clin. Virol. 2009, 46, S58-S63.
37. Tabata, T.; Petitt, M.; Zydek, M.; Fang-Hoover, J.; Larocque, N.; Tsuge, M.; Gormley, M.; Genbacev, O.; Pereira, L. Human cytomegalovirus infection of trophoblast progenitor cells inhibits early steps of differentiation. To be submitted for publication, 2014.
38. Isaacson, M.K.; Compton, T. Human cytomegalovirus glycoprotein b is required for virus entry and cell-to-cell spread but not for virion attachment, assembly, or egress. J. Virol. 2009, 83, 3891-3903.
39. Wille, P.T.; Wisner, T.W.; Ryckman, B.; Johnson, D.C. Human cytomegalovirus (hcmv) glycoprotein gb promotes virus entry in trans acting as the viral fusion protein rather than as a receptor-binding protein. mBio 2013, 4, e00332-00313.
40. Compton, T.; Nowlin, D.M.; Cooper, N.R. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 1993, 193, 834-841.
41. Carlson, C.; Britt, W.J.; Compton, T. Expression, purification, and characterization of a soluble form of human cytomegalovirus glycoprotein b. Virology 1997, 239, 198-205.
42. Wang, X.; Huong, S.M.; Chiu, M.L.; Raab-Traub, N.; Huang, E.S. Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus. Nature 2003, 424, 456-461.
43. Soroceanu, L.; Akhavan, A.; Cobbs, C.S. Platelet-derived growth factor-alpha receptor activation is required for human cytomegalovirus infection. Nature 2008, 455, 391-395.
44. Feire, A.L.; Roy, R.M.; Manley, K.; Compton, T. The glycoprotein b disintegrin-like domain binds beta 1 integrin to mediate cytomegalovirus entry. J. Virol. 2010, 84, 10026-10037.
45. Feire, A.L.; Koss, H.; Compton, T. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain. Proc. Natl. Acad. Sci. USA 2004, 101, 15470-15475.
46. Vanarsdall, A.L.; Ryckman, B.J.; Chase, M.C.; Johnson, D.C. Human cytomegalovirus glycoproteins gb and gh/gl mediate epithelial cell-cell fusion when expressed either in cis or in trans. J. Virol. 2008, 82, 11837-11850.
47. Hahn, G.; Revello, M.G.; Patrone, M.; Percivalle, E.; Campanini, G.; Sarasini, A.; Wagner, M.; Gallina, A.; Milanesi, G.; Koszinowski, U., et al. Human cytomegalovirus ul131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J. Virol. 2004, 78, 10023-10033.
48. Ryckman, B.J.; Chase, M.C.; Johnson, D.C. Hcmv gh/gl/ul128-131 interferes with virus entry into epithelial cells: Evidence for cell type-specific receptors. Proc. Natl. Acad. Sci. USA 2008, 105, 14118-14123.
49. Sinzger, C.; Digel, M.; Jahn, G. Cytomegalovirus cell tropism. Curr. Top. Microbiol. Immunol. 2008, 325, 63-83.
50. Vanarsdall, A.L.; Johnson, D.C. Human cytomegalovirus entry into cells. Curr. Opin. Virol. 2012, 2, 37-42.
51. Wang, D.; Shenk, T. Human cytomegalovirus ul131 open reading frame is required for epithelial cell tropism. J. Virol. 2005, 79, 10330-10338.
52. Dolan, A.; Cunningham, C.; Hector, R.D.; Hassan-Walker, A.F.; Lee, L.; Addison, C.; Dargan, D.J.; McGeoch, D.J.; Gatherer, D.; Emery, V.C., et al. Genetic content of wild-type human cytomegalovirus. J. Gen. Virol. 2004, 85, 1301-1312.
53. Scrivano, L.; Sinzger, C.; Nitschko, H.; Koszinowski, U.H.; Adler, B. Hcmv spread and cell tropism are determined by distinct virus populations. PLoS Pathog. 2011, 7, e1001256.
54. Adler, B.; Scrivano, L.; Ruzcics, Z.; Rupp, B.; Sinzger, C.; Koszinowski, U. Role of human cytomegalovirus ul131a in cell type-specific virus entry and release. J. Gen. Virol. 2006, 87, 2451-2460.
55. Stinski, M.F. Sequence of protein synthesis in cells infected by human cytomegalovirus: Early and late virus-induced polypeptides. J. Virol. 1978, 26, 686-701.
56. Compton, T.; Nepomuceno, R.R.; Nowlin, D.M. Human cytomegalovirus penetrates host cells by ph-independent fusion at the cell surface. Virology 1992, 191, 387-395.
57. Ryckman, B.J.; Jarvis, M.A.; Drummond, D.D.; Nelson, J.A.; Johnson, D.C. Human cytomegalovirus entry into epithelial and endothelial cells depends on genes ul128 to ul150 and occurs by endocytosis and low-ph fusion. J. Virol. 2006, 80, 710-722.
58. Sinzger, C. Entry route of hcmv into endothelial cells. J. Clin. Virol. 2008, 41, 174-179.
59. Weisblum, Y.; Panet, A.; Zakay-Rones, Z.; Haimov-Kochman, R.; Goldman-Wohl, D.; Ariel, I.; Falk, H.; Natanson-Yaron, S.; Goldberg, M.D.; Gilad, R.; Lurain, N.S.; Greenfield, C.; Yagel, S.; Wolf, D.G. Modeling of human cytomegalovirus maternal-fetal transmission in a novel decidual organ culture. J. Virol. 2011, 85, 13204-13213.
60. Bratcher, D.F.; Bourne, N.; Bravo, F.J.; Schleiss, M.R.; Slaoui, M.; Myers, M.G.; Bernstein, D.I. Effect of passive antibody on congenital cytomegalovirus infection in guinea pigs. J. Infect. Dis. 1995, 172, 944-950.
61. Schleiss, M.R.; Bourne, N.; Stroup, G.; Bravo, F.J.; Jensen, N.J.; Bernstein, D.I. Protection against congenital cytomegalovirus infection and disease in guinea pigs, conferred by a purified recombinant glycoprotein b vaccine. J. Infect. Dis. 2004, 189, 1374-1381.
62. Straschewski, S.; Patrone, M.; Walther, P.; Gallina, A.; Mertens, T.; Frascaroli, G. Protein pul128 of human cytomegalovirus is necessary for monocyte infection and blocking of migration. J. Virol. 2011, 85, 5150-5158.
63. Saccoccio, F.M.; Sauer, A.L.; Cui, X.; Armstrong, A.E.; Habib el, S.E.; Johnson, D.C.; Ryckman, B.J.; Klingelhutz, A.J.; Adler, S.P.; McVoy, M.A. Peptides from cytomegalovirus ul130 and ul131 proteins induce high titer antibodies that block viral entry into mucosal epithelial cells. Vaccine 2011, 29, 2705-2711.
64. Fouts, A.E.; Chan, P.; Stephan, J.P.; Vandlen, R.; Feierbach, B. Antibodies against the gh/gl/ul128/ul130/ul131 complex comprise the majority of the anti-cytomegalovirus (anti-cmv) neutralizing antibody response in cmv hyperimmune globulin. J. Virol. 2012, 86, 7444-7447.
65. Lilleri, D.; Kabanova, A.; Revello, M.G.; Percivalle, E.; Sarasini, A.; Genini, E.; Sallusto, F.; Lanzavecchia, A.; Corti, D.; Gerna, G. Fetal human cytomegalovirus transmission correlates with delayed maternal antibodies to gh/gl/pul128-130-131 complex during primary infection. PLoS One 2013, 8, e59863.
66. Ohlin, M.; Sundqvist, V.A.; Mach, M.; Wahren, B.; Borrebaeck, C.A. Fine specificity of the human immune response to the major neutralization epitopes expressed on cytomegalovirus gp58/116 (gb), as determined with human monoclonal antibodies. J. Virol. 1993, 67, 703-710.
67. Tugizov, S.; Maidji, E.; Xiao, J.; Pereira, L. An acidic cluster in the cytosolic domain of human cytomegalovirus glycoprotein b is a signal for endocytosis from the plasma membrane. J. Virol. 1999, 73, 8677-8688.
68. Navarro, D.; Paz, P.; Tugizov, S.; Topp, K.; La Vail, J.; Pereira, L. Glycoprotein b of human cytomegalovirus promotes virion penetration into cells, transmission of infection from cell to cell, and fusion of infected cells. Virology 1993, 197, 143-158.
69. Grazia Revello, M.; Baldanti, F.; Percivalle, E.; Sarasini, A.; De-Giuli, L.; Genini, E.; Lilleri, D.; Labo, N.; Gerna, G. In vitro selection of human cytomegalovirus variants unable to transfer virus and virus products from infected cells to polymorphonuclear leukocytes and to grow in endothelial cells. J. Gen. Virol. 2001, 82, 1429-1438.
70. Maidji, E.; Percivalle, E.; Gerna, G.; Fisher, S.; Pereira, L. Transmission of human cytomegalovirus from infected uterine microvascular endothelial cells to differentiating/invasive placental cytotrophoblasts. Virology 2002, 304, 53-69.
71. Damsky, C.H.; Fitzgerald, M.L.; Fisher, S.J. 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. Invest. 1992, 89, 210-222.
72. Pereira, L.; Hoffman, M.; Gallo, D.; Cremer, N. Monoclonal antibodies to human cytomegalovirus: Three surface membrane proteins with unique immunological and electrophoretic properties specify cross-reactive determinants. Infect. Immun. 1982, 36, 924-932.
73. Iwayama, S.; Yamamoto, T.; Furuya, T.; Kobayashi, R.; Ikuta, K.; Hirai, K. Intracellular localization and DNA-binding activity of a class of viral early phosphoproteins in human fibroblasts infected with human cytomegalovirus (towne strain). J. Gen. Virol. 1994, 75, 3309-3318.
74. Nis-elements, 4.0; Laboratory Imaging, Ltd.: Prague, Czech Republic, 2011.
75. Schneider, C.A.; Rasband, W.S.; Eliceiri, K.W. Nih image to imagej: 25 years of image analysis. Nat. Methods 2012, 9, 671-675.
76. Fiji (fiji is just imagej), version 1.0; University of Wisconsin at Madison: Madison, WI, USA, 2011.
77. Null, D.; Bimle, C.; Weisman, L.; Johnson, K.; Steichen, J.; Gratton, T.; Singh, S.; Wang, E.; Asztalos, E.; Loeffler, A.M., et al. Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants. Pediatrics 1998, 102, 531-537.