Home LiteratureArticle Details
PMID: 10364346 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Neutralizing antibodies inhibit axonal spread of herpes simplex virus type 1 to epidermal cells in vitro.

Journal of virology ·Vol. 73 ·No. 7 ·1999-07-00 ·Pages 5934-44

Mikloska Z, Sanna PP, Cunningham AL

Abstract

The ability of antibodies to interfere with anterograde transmission of herpes simplex virus (HSV) from neuronal axons to the epidermis was investigated in an in vitro model consisting of human fetal dorsal root ganglia innervating autologous skin explants in a dual-chamber tissue culture system. The number and size of viral cytopathic plaques in epidermal cells after axonal transmission from HSV type 1 (HSV-1)-infected dorsal root ganglionic neurons were significantly reduced by addition to the outer chamber of neutralizing polyclonal human sera to HSV-1, of a human recombinant monoclonal group Ib antibody to glycoprotein D (gD), and of rabbit sera to HSV-1 gB and gD but not by rabbit anti-gE or anti-gG. A similar pattern of inhibition of direct infection of epidermal cells by these antibodies was observed. High concentrations of the monoclonal anti-gD reduced transmission by 90%. Rabbit anti-gB was not taken up into neurons, and human anti-gD did not influence spread of HSV in the dorsal root ganglia or axonal transport of HSV antigens when applied to individual dissociated neurons. These results suggest that anti-gD and -gB antibodies interfere with axonal spread of HSV-1, possibly by neutralizing HSV during transmission across an intercellular gap between axonal termini and epidermal cells, and thus contribute to control of HSV spread and shedding. Therefore, selected human monoclonal antibodies to protective epitopes might even be effective in preventing epidermis-to-neuron transmission during primary HSV infection, especially neonatal infection.

MeSH Terms
Animals Antibodies, Viral/immunology Axonal Transport Axons/immunology,virology Cells, Cultured Cytopathogenic Effect, Viral Epidermal Cells Epidermis/innervation,virology Ganglia, Spinal/cytology Herpesvirus 1, Human/growth & development,immunology Humans Neurons Neutralization Tests Rabbits Skin/cytology,innervation Tumor Cells, Cultured Viral Envelope Proteins/immunology Viral Plaque Assay Virus Replication
Chemicals
Antibodies, Viral Viral Envelope Proteins glycoprotein B, Simplexvirus glycoprotein D, Human herpesvirus 1
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Mikloska Z
Centre for Virus Research, Westmead Institutes of Health Research, Westmead Hospital and University of Sydney, Sydney, New South Wales 2145, Australia. [email protected]
Sanna P P
Cunningham A L
References (48)
48 references, click to expand
  1. Neonatal antibody-dependent cellular cytotoxic antibody levels are associated with the clinical presentation of neonatal herpes simplex virus infection.
    J Infect Dis. 1989 Nov;160(5):770-6 PMID: 2553825
  2. Severe herpesvirus infections in an adolescent without natural killer cells.
    N Engl J Med. 1989 Jun 29;320(26):1731-5 PMID: 2543925
  3. Analysis of the role of antibody-dependent cellular cytotoxic antibody activity in murine neonatal herpes simplex virus infection with antibodies to synthetic peptides of glycoprotein D and monoclonal antibodies to glycoprotein B.
    J Clin Invest. 1990 Jul;86(1):273-8 PMID: 2164044
  4. Neonatal herpes simplex virus infection in relation to asymptomatic maternal infection at the time of labor.
    N Engl J Med. 1991 May 2;324(18):1247-52 PMID: 1849612
  5. Internalization of plasma proteins by cerebellar Purkinje cells.
    J Neurol Sci. 1990 Dec;100(1-2):43-9 PMID: 1708409
  6. Penetration and internalization of plasma proteins in the human spinal cord.
    J Neurol Sci. 1991 Aug;104(2):166-75 PMID: 1719138
  7. Role of antibody-dependent cellular cytotoxicity in neonatal infection with herpes simplex virus.
    Rev Infect Dis. 1991 Nov-Dec;13 Suppl 11:S950-2 PMID: 1664132
  8. Underdiagnosis of genital herpes by current clinical and viral-isolation procedures.
    N Engl J Med. 1992 Jun 4;326(23):1533-9 PMID: 1315930
  9. Structural basis of C3b binding by glycoprotein C of herpes simplex virus.
    J Virol. 1992 Jul;66(7):4013-27 PMID: 1602532
  10. The role of T cell immunity in control of herpes simplex virus.
    Curr Top Microbiol Immunol. 1992;179:57-74 PMID: 1499350
  11. The role of antibody in herpes simplex virus infection in humans.
    Curr Top Microbiol Immunol. 1992;179:75-88 PMID: 1499351
  12. Orientation of the cleavage site of the herpes simplex virus glycoprotein G-2.
    J Virol. 1993 May;67(5):2954-9 PMID: 8386284
  13. Human monoclonal antibodies against a plethora of viral pathogens from single combinatorial libraries.
    Proc Natl Acad Sci U S A. 1993 May 1;90(9):4141-5 PMID: 7683424
  14. Recombinant human Fab to glycoprotein D neutralizes infectivity and prevents cell-to-cell transmission of herpes simplex viruses 1 and 2 in vitro.
    Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):355-9 PMID: 8278393
  15. Characterization of domains of herpes simplex virus type 1 glycoprotein E involved in Fc binding activity for immunoglobulin G aggregates.
    J Virol. 1994 Apr;68(4):2478-85 PMID: 7511171
  16. Axonal transport of herpes simplex virions to epidermal cells: evidence for a specialized mode of virus transport and assembly.
    Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6529-33 PMID: 7517552
  17. Directed selection of recombinant human monoclonal antibodies to herpes simplex virus glycoproteins from phage display libraries.
    Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6439-43 PMID: 7604009
  18. Protection against zosteriform spread of herpes simplex virus by monoclonal antibodies.
    J Infect Dis. 1991 Feb;163(2):263-9 PMID: 1846388
  19. Virologic characteristics of subclinical and symptomatic genital herpes infections.
    N Engl J Med. 1995 Sep 21;333(12):770-5 PMID: 7643884
  20. Internalization of IgG in motoneurons of patients with ALS: selective or nonselective?
    Neurology. 1995 Aug;45(8):1551-4 PMID: 7543985
  21. Herpes simplex virus protein targets for CD4 and CD8 lymphocyte cytotoxicity in cultured epidermal keratinocytes treated with interferon-gamma.
    J Infect Dis. 1996 Jan;173(1):7-17 PMID: 8537685
  22. Protection of nude mice by passive immunization with a type-common human recombinant monoclonal antibody against HSV.
    Virology. 1996 Jan 1;215(1):101-6 PMID: 8553581
  23. Cell-type dependent sensitivity of herpes simplex virus 1 mutants to plaque development inhibition by an anti-gD monoclonal antibody.
    New Microbiol. 1995 Oct;18(4):351-8 PMID: 8590387
  24. Uptake of immunoglobulin G from amyotrophic lateral sclerosis patients by motor nerve terminals in mice.
    J Neurol Sci. 1996 May;137(2):97-102 PMID: 8782161
  25. The interaction of human fetal neurons and epidermal cells in vitro.
    In Vitro Cell Dev Biol Anim. 1996 Jul-Aug;32(7):420-6 PMID: 8856342
  26. Topically applied human recombinant monoclonal IgG1 antibody and its Fab and F(ab')2 fragments protect mice from vaginal transmission of HSV-2.
    Virology. 1996 Nov 1;225(1):213-5 PMID: 8918548
  27. The role of antibody in recovery from alphavirus encephalitis.
    Immunol Rev. 1997 Oct;159:155-61 PMID: 9416509
  28. Herpes simplex virus type 1 glycoproteins gB, gC and gD are major targets for CD4 T-lymphocyte cytotoxicity in HLA-DR expressing human epidermal keratinocytes.
    J Gen Virol. 1998 Feb;79 ( Pt 2):353-61 PMID: 9472620
  29. In vivo production of cytokines and beta (C-C) chemokines in human recurrent herpes simplex lesions--do herpes simplex virus-infected keratinocytes contribute to their production?
    J Infect Dis. 1998 Apr;177(4):827-38 PMID: 9534953
  30. Characterization of a type-common human recombinant monoclonal antibody to herpes simplex virus with high therapeutic potential.
    J Clin Microbiol. 1998 Nov;36(11):3198-204 PMID: 9774565
  31. Anterograde transport of herpes simplex virus proteins in axons of peripheral human fetal neurons: an immunoelectron microscopy study.
    J Virol. 1999 Oct;73(10):8503-11 PMID: 10482603
  32. Uptake of a monoclonal antibody to corticotropin-releasing factor (CRF) into rat hypothalamic neurons.
    Brain Res. 1990 May 28;517(1-2):283-93 PMID: 2375997
  33. A prospective study of chronic herpes simplex virus infection and recurrent herpes labialis in humans.
    J Immunol. 1970 Feb;104(2):289-95 PMID: 4312871
  34. Latent herpes simplex virus in spinal ganglia of mice.
    Science. 1971 Aug 27;173(3999):843-5 PMID: 4328483
  35. Murine antibody-dependent cellular cytotoxicity to herpes simplex virus-infected target cells.
    J Immunol. 1979 Jul;123(1):25-30 PMID: 448149
  36. Acute and latent infection of sensory ganglia with herpes simplex virus: immune control and virus reactivation.
    J Gen Virol. 1979 Jul;44(1):205-15 PMID: 227991
  37. Relationship of antibody to outcome in neonatal herpes simplex virus infections.
    Infect Immun. 1980 Aug;29(2):532-8 PMID: 7216423
  38. Immune response to herpes simplex virus infections: virus-specific antibodies in sera from patients with recurrent facial infections.
    Infect Immun. 1981 Feb;31(2):624-30 PMID: 7216464
  39. Use of monoclonal antibody directed against herpes simplex virus glycoproteins to protect mice against acute virus-induced neurological disease.
    Infect Immun. 1981 Oct;34(1):192-9 PMID: 6271681
  40. Severe acquired immunodeficiency in male homosexuals, manifested by chronic perianal ulcerative herpes simplex lesions.
    N Engl J Med. 1981 Dec 10;305(24):1439-44 PMID: 6272110
  41. Genital herpes simplex virus infections: clinical manifestations, course, and complications.
    Ann Intern Med. 1983 Jun;98(6):958-72 PMID: 6344712
  42. Neonatal herpes simplex virus infection: follow-up evaluation of vidarabine therapy.
    Pediatrics. 1983 Dec;72(6):778-85 PMID: 6359047
  43. Localization of epitopes of herpes simplex virus type 1 glycoprotein D.
    J Virol. 1985 Feb;53(2):634-44 PMID: 2578577
  44. Ganglion cell counts in the cochleae of patients with normal audiograms.
    Acta Otolaryngol. 1985 Jan-Feb;99(1-2):8-13 PMID: 3976399
  45. Low risk of herpes simplex virus infections in neonates exposed to the virus at the time of vaginal delivery to mothers with recurrent genital herpes simplex virus infections.
    N Engl J Med. 1987 Jan 29;316(5):240-4 PMID: 3025727
  46. A comparative study of herpes simplex infections in renal transplant and leukemic patients.
    J Infect Dis. 1987 Aug;156(2):280-7 PMID: 3036965
  47. Fine mapping of antigenic site II of herpes simplex virus glycoprotein D.
    J Virol. 1989 May;63(5):2325-34 PMID: 2467994
  48. Cutaneous innervation in man visualized with protein gene product 9.5 (PGP 9.5) antibodies.
    Histochemistry. 1989;92(5):385-90 PMID: 2531128
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1999-07-00
Pages
5934-44
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC112655
Subset
IM
Grants
NIAID NIH HHS · AI37582 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]