Sequestration of human cytomegalovirus by human renal and mammary epithelial cells

Virology

Volumn 460-461, Issue 1, 2014, Pages 55-65

  Twite, Nicolas ^a   Andrei, Graciela ^b   Kummert, Caroline ^c   Donner, Catherine ^d   Perez Morga, David ^a   De Vos, Rita ^e   Snoeck, Robert ^b   Marchant, Arnaud ^a,c  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^c ImmuneHealth   (Belgium)

^d ERASME HOSPITAL   (Belgium)

^e UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

Antibody; HCMV glycoprotein B; Human cytomegalovirus; Interferon gamma; Mammary epithelial cell; Renal epithelial cell; Viral excretion

Indexed keywords

CYTOMEGALOVIRUS ANTIBODY; GAMMA INTERFERON;

ADULT; ARTICLE; BREAST EPITHELIUM; BREAST MILK; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; ELECTRON MICROSCOPY; EMBRYO; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; KIDNEY TUBULE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROGENY; SUPERNATANT; URINE; VIRUS EXCRETION; VIRUS REPLICATION; VIRUS TRANSMISSION;

ANTIBODY; HCMV GLYCOPROTEIN B; HUMAN CYTOMEGALOVIRUS; INTERFERON-GAMMA; MAMMARY EPITHELIAL CELL; RENAL EPITHELIAL CELL; VIRAL EXCRETION;

CELL LINE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; EPITHELIAL CELLS; FEMALE; FIBROBLASTS; HUMANS; KIDNEY; MAMMARY GLANDS, HUMAN; VIRUS REPLICATION;

EID: 84901461859     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.04.032     Document Type: Article

References (66)

1. Andrei G., De Clercq E., Snoeck R. Novel inhibitors of human CMV. Curr. Opin. Investig. Drugs 2008, 9:132-145.
2. Andrei G., De Clercq E., Snoeck R. Drug targets in cytomegalovirus infection. Infect. Disord. Drug Targets 2009, 9:201-222.
3. Arcangeletti M.C., et al. Cytoskeleton involvement during human cytomegalovirus replicative cycle in human embryo fibroblasts. New Microbiol. 2000, 23:241-256.
4. Axelsson F., Adler S.P., Lamarre A., Ohlin M. Humoral immunity targeting site I of antigenic domain 2 of glycoprotein B upon immunization with different cytomegalovirus candidate vaccines. Vaccine 2007, 21:41-46.
5. Baer P.C., Bereiter-Hahn J., Schubert R., Geiger H. Differentiation status of human renal proximal and distal tubular epithelial cells in vitro: Differential expression of characteristic markers. Cells Tissues Org. 2006, 184:16-22.
6. Bain M., Sinclair J. The S phase of the cell cycle and its perturbation by human cytomegalovirus. Rev. Med. Virol. 2007, 17:423-434.
7. Bale J.F. Cytomegalovirus infections. Semin. Pediatr. Neurol. 2012, 19:101-106.
8. Bergstrom D.E., et al. Polysulfonates derived from metal thiolate complexes as inhibitors of HIV-1 and various other enveloped viruses in vitro. Antivir. Chem. Chemother. 2002, 13:185-195.
9. Berlier W., et al. Selective sequestration of X4 isolates by human genital epithelial cells: implication for virus tropism selection process during sexual transmission of HIV. J. Med. Virol. 2005, 77:465-474.
10. Bernstein D.I. Vaccines for cytomegalovirus. Infect. Disord. Drug Targets 2011, 11:514-525.
11. Bernstein D.I., et al. Randomized, double-blind, phase 1 trial of an alphavirus replicon vaccine for cytomegalovirus in CMV seronegative adult volunteers. Vaccine 2009, 11:484-493.
12. 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.
13. Dasari V., et al. Recombinant glycoprotein B vaccine formulation with TLR9 agonist and immune stimulating complex induces specific immunity against multiple strains of cytomegalovirus. J. Gen. Virol. 2011, 92:1021-1031.
14. Davey A., Eastman L., Hansraj P., Hemmings D.G. Human cytomegalovirus is protected from inactivation by reversible binding to villous trophoblasts. Biol. Reprod. 2011, 85:198-207.
15. Dezzutti C.S., et al. Cervical and prostate primary epithelial cells are not productively infected but sequester human immunodeficiency virus type 1. J. Infect. Dis. 2001, 15:1204-1213.
16. Dorosko S.M., Connor R.I. Primary human mammary epithelial cells endocytose human immunodeficiency virus (HIV)-1 and facilitate viral infection of CD4+T lymphocytes. J. Virol. 2010, 84:10533-10542.
17. Eggers M., Bogner E., Agricola B., Kern H.F., Radsak K. Inhibition of human cytomegalovirus maturation by brefeldin A. J. Gen. Virol. 1992, 73:2679-2692.
18. 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.
19. Gabrielli L., et al. Congenital cytomegalovirus infection: patterns of fetal brain damage. Clin. Microbiol. Infect. 2012, 6. 10.1111/j.1469-0691.2012.03983.x.
20. Gerna G., et al. Human cytomegalovirus serum neutralizing antibodies block virus infection of endothelial/epithelial cells, but not fibroblasts, early during primary infection. J. Gen. Virol. 2008, 89:853-865.
21. Griffiths P.D., et al. Cytomegalovirus glycoprotein-B vaccine with MF59 adjuvant in transplant recipients: a phase 2 randomised placebo-controlled trial. Lancet 2011, 9:1256-1263.
22. Hamele M., Flanagan R., Loomis C.A., Stevens T., Fairchok M.P. Severe morbodity and mortality with breast milk associated cytomegalovirus infection. Pediatr. Infect. Dis. J. 2010, 29:84-86.
23. Hamprecht K., Maschmann J., Jahn G., Poets C.F., Goelz R. Cytomegalovirus transmission to preterm infants during lactation. J. Clin. Virol. 2008, 41:198-205.
24. 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.
25. Isaacson M.K., Feire A.L., Compton T. Epidermal growth factor receptor is not required for human cytomegalovirus entry or signaling. J. Virol. 2007, 81:6241-6247.
26. Jacobson M.A., et al. Safety and immunogenicity of Towne cytomegalovirus vaccine with or without adjuvant recombinant interleukin-12. Vaccine 2006, 19:5311-5319.
27. Jacobson M.A., et al. A CMV DNA vaccine primes for memory immune responses to live-attenuated CMV (Towne strain). Vaccine 2009, 4:1540-1548.
28. Jobe A.H. CMV transmission in human milk. J. Pediatr. 2009, 154:A1.
29. Jones N.L., Lewis J.C., Kilpatrick B.A. Cytoskeletal disruption during human cytomegalovirus infection of human lung fibroblasts. Eur. J. Cell Biol. 1986, 41:304-312.
30. Kaye S., et al. Virological and immunological correlates of mother-to-child transmission of cytomegalovirus in the Gambia. J. Infect. Dis. 2008, 197:1307-1314.
31. Kregler O., Schilf R., Lander A., Bannert N., Bogner E. Brefeldin A inhibits expression of DNA packaging proteins and nucleocapsid formation of human cytomegalovirus. FEBS Lett. 2009, 2:1207-1214.
32. Lilleri D., Kabanova A., Lanzavecchia A., Gerna G. Antibodies against neutralization epitopes of human cytomegalovirus gH/gL/pUL128-130-131 complex and virus spreading may correlate with virus control in vivo. J. Clin. Immunol. 2012, 27.
33. Macagno A., et al. 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.
34. Marchant A., et al. Mature CD8(+) T lymphocyte response to viral infection during fetal life. J. Clin. Invest. 2003, 111:1747-1755.
35. Marschall M., Stamminger T. Molecular targets for antiviral therapy of cytomegalovirus infections. Future Microbiol. 2009, 4:731-742.
36. Meng G., et al. Primary intestinal epithelial cells selectively transfer R5 HIV-1 to CCR5+cells. Nat. Med 2002, 8:150-156.
37. Mikulak J., Teichberg S., Faust T., Schmidtmayerova H., Singhal P.C. HIV-1 harboring renal tubular epithelial cell interaction with T cells results in T cell trans-infection. Virology 2009, 385:105-114.
38. Miller M.S., Hertel L. Onset of human cytomegalovirus replication in fibroblasts requires the presence of an intact vimentin cytoskeleton. J. Virol. 2009, 83:7015-7028.
39. Moutaftsi M., Brennan P., Spector S.A., Tabi Z. Impaired lymphoid chemokine-mediated migration due to a block on the chemokine receptor switch in human cytomegalovirus-infected dendritic cells. J. Virol. 2004, 78:3046-3054.
40. Munger J., et al. Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy. Nat. Biotechnol. 2008, 26:1179-1186.
41. Neyts J., et al. Sulfated polymers inhibit the interaction of human cytomegalovirus with cell surface heparan sulfate. Virology 1992, 189:48-58.
42. Ogawa-Goto K., et al. Microtubule network facilitates nuclear targeting of human cytomegalovirus capsid. J. Virol. 2003, 77:8541-8547.
43. Olejniczak M.J., Choi K.Y., McVoy M.A., Cui X., Schleiss M.R. Intravaginal cytomegalovirus (CMV) challenge elicits maternal viremia and results in congenital transmission in a guinea pig model. Virol. J. 2011, 3:89.
44. Pass R.F. Development and evidence for efficacy of CMV glycoprotein B vaccine with MF59 adjuvant. J. Clin. Virol. 2009, 46:S73-S76.
45. Pass R.F., et al. Vaccine prevention of maternal cytomegalovirus infection. N. Engl. J. Med. 2009, 360:1191-1199.
46. Rosenthal L.S., et al. Cytomegalovirus shedding and delayed sensorineural hearing loss: results from longitudinal follow-up of children with congenital infection. Pediatr. Infect. Dis. J. 2009, 28:515-520.
47. Saccoccio F.M., et al. Peptides from cytomegalovirus UL130 and UL131 proteins induce high titer antibodies that block viral entry into mucosal epithelial cells. Vaccine 2011, 29:2705-2711.
48. Schuessler A., Sampaio K.L., Straschewski S., Sinzger C. Mutational mapping of pUL131A of human cytomegalovirus emphasizes its central role for endothelial cell tropism. J. Virol. 2012, 86:504-512.
49. Sinzger C., Digel M., Jahn G. Cytomegalovirus cell tropism. Curr. Top. Microbiol. Immunol. 2008, 325:63-83.
50. Song B.H., Lee G.C., Moon M.S., Cho Y.H., Lee C.H. Human cytomegalovirus binding to heparan sulfate proteoglycans on the cell surface and/or entry stimulates the expression of human leukocyte antigen class I. J. Gen. Virol. 2001, 82:2405-2413.
51. Soroceanu L., Akhavan A., Cobbs C.S. Platelet-derived growth factor-alpha receptor activation is required for human cytomegalovirus infection. Nature 2008, 18:391-395.
52. Staras S.A., et al. Influence of sexual activity on cytomegalovirus seroprevalence in the United States, 1988-1994. Sex. Transm. Dis. 2008, 35:472-479.
53. Staras S.A., et al. Cytomegalovirus seroprevalence and childhood sources of infection: a population-based study among pre-adolescents in the United States. J. Clin. Virol. 2008, 43:266-271.
54. Steininger C. Cytomegalovirus vaccine: light on the horizon. Lancet Infect. Dis. 2012, 12:257-259.
55. Straschewski S., et al. Protein pUL128 of human cytomegalovirus is necessary for monocyte infection and block of migration. J. Virol. 2011, 85:5051-5058.
56. Tugizov S., Maidji E., Pereira L. Role of apical and basolateral membranes in replication of human cytomegalovirus in polarized retinal pigment epithelial cells. J. Gen. Virol. 1996, 77:61-74.
57. Vanarsdall A.L., Johnson D.C. Human cytomegalovirus entry into cells. Curr. Opin. Virol. 2012, 2:37-42.
58. 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.
59. Vanarsdall A.L., Chase M.C., Johnson D.C. Human cytomegalovirus glycoprotein gO complexes with gH/gL, promoting interference with viral entry into human fibroblasts but not entry into epithelial cells. J. Virol. 2011, 85:11638-11645.
60. van der Sande M.A., et al. Risk factors for and clinical outcome of congenital cytomegalovirus infection in a peri-urban West-African birth cohort. PLoS One 2007, 6:e492.
61. 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, 24:456-461.
62. Wille P.T., Knoche A.J., Nelson J.A., Jarvis M.A., Johnson D.C. A human cytomegalovirus gO-null mutant fails to incorporate gH/gL into the virion envelope and is unable to enter fibroblasts and epithelial and endothelial cells. J. Virol. 2010, 84:2585-2596.
63. Wloch M.K., et al. Safety and immunogenicity of a bivalent cytomegalovirus DNA vaccine in healthy adult subjects. J. Infect. Dis. 2008, 15:1634-1642.
64. Wu C.A., et al. Transmission of murine cytomegalovirus in breast milk: a model of natural infection in neonates. J. Virol. 2011, 85:5115-5124.
65. Wu Z., Chen Z., Phillips D.M. Human genital epithelial cells capture cell-free human immunodeficiency virus type 1 and transmit the virus to CD4+cells: implications for mechanisms of sexual transmission. J. Infect. Dis. 2003, 15:1473-1482.
66. Zhong J., Khanna R. Ad-gBCMVpoly: A novel chimeric vaccine strategy for human cytomegalovirus-associated diseases. J. Clin. Virol. 2009, 46:S68-S72.