Molecular Cloning and Functional Analysis of Three Type D Endogenous Retroviruses of Sheep Reveal a Different Cell Tropism from That of the Highly Related Exogenous Jaagsiekte Sheep Retrovirus

doi:10.1128/JVI.74.17.8065-8076.2000

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Journal of Virology, September 2000, p. 8065-8076, Vol. 74, No. 17
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Molecular Cloning and Functional Analysis of Three Type D Endogenous Retroviruses of Sheep Reveal a Different Cell Tropism from That of the Highly Related Exogenous Jaagsiekte Sheep Retrovirus

Massimo Palmarini,¹ Claus Hallwirth,² Denis York,² Claudio Murgia,¹ Tulio de Oliveira,² Thomas Spencer,³ and Hung Fan¹^,^*

Cancer Research Institute and Department of Molecular Biology and Biochemistry, University of California Irvine, Irvine, California¹; Department of Virology, Faculty of Medicine, University of Natal, Durban, South Africa²; and Center for Animal Biotechnology and Genomics, Department of Animal Science, Texas A&M University, College Station, Texas³

Received 26 April 2000/Accepted 1 June 2000

Integrated into the sheep genome are 15 to 20 copies of type D endogenous loci that are highly related to two exogenous oncogenicviruses, jaagsiekte sheep retrovirus (JSRV) and enzootic nasaltumor virus (ENTV). The exogenous viruses cause infectious neoplasmsof the respiratory tract in small ruminants. In this study, wemolecularly cloned three intact type D endogenous retrovirusesof sheep (enJS56A1, enJS5F16, and enJS59A1; collectively calledenJRSVs) and analyzed their genomic structures, their phylogenieswith respect to their exogenous counterparts, their capacity toform viral particles, and the expression specificities of theirlong terminal repeats (LTRs). In addition, the pattern of expressionof enJSRVs in vivo was studied by in situ hybridization. All ofthe three enJSRV proviruses had open reading frames for at leastone of the structural genes. In particular, enJS56A1 had openreading frames for all structural genes, but it could not assembleviral particles when highly expressed in human 293T cells. Welocalized the defect for viral assembly in the first two-thirdsof the gag gene by making a series of chimeras between enJS56A1and the exogenous infectious molecular clone JSRV₂₁. Phylogeneticanalysis distinguished five ovine type D retroviruses: enJSRVgroups A and B, ENTV, and two exogenous JSRV groups (African versusUnited Kingdom/North America isolates). Transient transfectionassays indicated that the LTRs of the three enJSRVs were not preferentiallyactive in differentiated lung epithelial cells. This suggeststhat the pulmonary tropic JSRV developed from a type D retrovirusthat did not have lung specificity. Consistent with this, in situhybridization of a panel of normal ovine tissues revealed highexpression of enJSRV mRNA in the luminal epithelium and glandularepithelium of the uterus; lower expression was localized in thelamina propria of the gut and in the bronchiolar epithelium ofthelungs.

^* Corresponding author. Mailing address: Cancer Research Institute, Bio. Sci. II, University of California Irvine, Irvine, CA92697. Phone: (949) 824-6631. Fax: (949) 824-4023. E-mail: hyfan{at}uci.edu.

Journal of Virology, September 2000, p. 8065-8076, Vol. 74, No. 17
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

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