Replication in a superficial epithelial cell niche explains the lack of pathogenicity of primate foamy virus infections

Shannon M. Murray, Louis Picker, Michael Axthelm, Kelly Hudkins, Charles E. Alpers, Maxine L. Linial

Research output: Contribution to journalArticle

49 Citations (Scopus)

Abstract

Foamy viruses (FVs) are ancient retroviruses that are ubiquitous in nonhuman primates (NHPs). While FVs share many features with pathogenic retroviruses, such as human immunodeficiency virus, FV infections of their primate hosts have no apparent pathological consequences. Paradoxically, FV infections of many cell types in vitro are rapidly cytopathic. Previous work has shown that low levels of proviral DNA are found in most tissues of naturally infected rhesus macaques, but these proviruses are primarily latent. In contrast, viral RNA, indicative of viral replication, is restricted to tissues of the oral mucosa, where it is abundant. Here, we perform in situ hybridization on tissues from rhesus macaques naturally infected with simian FV (SFV). We show that superficial differentiated epithelial cells of the oral mucosa, many of which appear to be shedding from the tissue, are the major cell type in which SFV replicates. Thus, the innocuous nature of SFV infection can be explained by replication that is limited to differentiated superficial cells that are short-lived and shed into saliva. This finding can also explain the highly efficient transmission of FVs among NHPs.

Original languageEnglish (US)
Pages (from-to)5981-5985
Number of pages5
JournalJournal of Virology
Volume82
Issue number12
DOIs
StatePublished - Jun 2008

Fingerprint

Spumavirus
Virus Diseases
Primates
Virulence
niches
epithelial cells
pathogenicity
Epithelial Cells
Retroviridae
viruses
digestive tract mucosa
infection
Mouth Mucosa
Macaca mulatta
Simian foamy virus
proviruses
Proviruses
Human immunodeficiency virus
Viral RNA
cells

ASJC Scopus subject areas

  • Immunology

Cite this

Replication in a superficial epithelial cell niche explains the lack of pathogenicity of primate foamy virus infections. / Murray, Shannon M.; Picker, Louis; Axthelm, Michael; Hudkins, Kelly; Alpers, Charles E.; Linial, Maxine L.

In: Journal of Virology, Vol. 82, No. 12, 06.2008, p. 5981-5985.

Research output: Contribution to journalArticle

Murray, Shannon M. ; Picker, Louis ; Axthelm, Michael ; Hudkins, Kelly ; Alpers, Charles E. ; Linial, Maxine L. / Replication in a superficial epithelial cell niche explains the lack of pathogenicity of primate foamy virus infections. In: Journal of Virology. 2008 ; Vol. 82, No. 12. pp. 5981-5985.
@article{a9637dd9d529444cbaa8da67c3e10657,
title = "Replication in a superficial epithelial cell niche explains the lack of pathogenicity of primate foamy virus infections",
abstract = "Foamy viruses (FVs) are ancient retroviruses that are ubiquitous in nonhuman primates (NHPs). While FVs share many features with pathogenic retroviruses, such as human immunodeficiency virus, FV infections of their primate hosts have no apparent pathological consequences. Paradoxically, FV infections of many cell types in vitro are rapidly cytopathic. Previous work has shown that low levels of proviral DNA are found in most tissues of naturally infected rhesus macaques, but these proviruses are primarily latent. In contrast, viral RNA, indicative of viral replication, is restricted to tissues of the oral mucosa, where it is abundant. Here, we perform in situ hybridization on tissues from rhesus macaques naturally infected with simian FV (SFV). We show that superficial differentiated epithelial cells of the oral mucosa, many of which appear to be shedding from the tissue, are the major cell type in which SFV replicates. Thus, the innocuous nature of SFV infection can be explained by replication that is limited to differentiated superficial cells that are short-lived and shed into saliva. This finding can also explain the highly efficient transmission of FVs among NHPs.",
author = "Murray, {Shannon M.} and Louis Picker and Michael Axthelm and Kelly Hudkins and Alpers, {Charles E.} and Linial, {Maxine L.}",
year = "2008",
month = "6",
doi = "10.1128/JVI.00367-08",
language = "English (US)",
volume = "82",
pages = "5981--5985",
journal = "Journal of Virology",
issn = "0022-538X",
publisher = "American Society for Microbiology",
number = "12",

}

TY - JOUR

T1 - Replication in a superficial epithelial cell niche explains the lack of pathogenicity of primate foamy virus infections

AU - Murray, Shannon M.

AU - Picker, Louis

AU - Axthelm, Michael

AU - Hudkins, Kelly

AU - Alpers, Charles E.

AU - Linial, Maxine L.

PY - 2008/6

Y1 - 2008/6

N2 - Foamy viruses (FVs) are ancient retroviruses that are ubiquitous in nonhuman primates (NHPs). While FVs share many features with pathogenic retroviruses, such as human immunodeficiency virus, FV infections of their primate hosts have no apparent pathological consequences. Paradoxically, FV infections of many cell types in vitro are rapidly cytopathic. Previous work has shown that low levels of proviral DNA are found in most tissues of naturally infected rhesus macaques, but these proviruses are primarily latent. In contrast, viral RNA, indicative of viral replication, is restricted to tissues of the oral mucosa, where it is abundant. Here, we perform in situ hybridization on tissues from rhesus macaques naturally infected with simian FV (SFV). We show that superficial differentiated epithelial cells of the oral mucosa, many of which appear to be shedding from the tissue, are the major cell type in which SFV replicates. Thus, the innocuous nature of SFV infection can be explained by replication that is limited to differentiated superficial cells that are short-lived and shed into saliva. This finding can also explain the highly efficient transmission of FVs among NHPs.

AB - Foamy viruses (FVs) are ancient retroviruses that are ubiquitous in nonhuman primates (NHPs). While FVs share many features with pathogenic retroviruses, such as human immunodeficiency virus, FV infections of their primate hosts have no apparent pathological consequences. Paradoxically, FV infections of many cell types in vitro are rapidly cytopathic. Previous work has shown that low levels of proviral DNA are found in most tissues of naturally infected rhesus macaques, but these proviruses are primarily latent. In contrast, viral RNA, indicative of viral replication, is restricted to tissues of the oral mucosa, where it is abundant. Here, we perform in situ hybridization on tissues from rhesus macaques naturally infected with simian FV (SFV). We show that superficial differentiated epithelial cells of the oral mucosa, many of which appear to be shedding from the tissue, are the major cell type in which SFV replicates. Thus, the innocuous nature of SFV infection can be explained by replication that is limited to differentiated superficial cells that are short-lived and shed into saliva. This finding can also explain the highly efficient transmission of FVs among NHPs.

UR - http://www.scopus.com/inward/record.url?scp=44949158024&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=44949158024&partnerID=8YFLogxK

U2 - 10.1128/JVI.00367-08

DO - 10.1128/JVI.00367-08

M3 - Article

VL - 82

SP - 5981

EP - 5985

JO - Journal of Virology

JF - Journal of Virology

SN - 0022-538X

IS - 12

ER -