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Journal of Virology, April 2001, p. 3520-3526, Vol. 75, No. 8
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.8.3520-3526.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Two Functionally Distinct Forms of a Retroviral Receptor Explain the Nonreciprocal Receptor Interference among Subgroups B, D, and E Avian Leukosis Viruses

Heather B. Adkins,1,2,dagger Stephen C. Blacklow,2 and John A. T. Young1,3,*

Department of Microbiology and Molecular Genetics1 and Department of Pathology, Brigham and Women's Hospital,2 Harvard Medical School, Boston, Massachusetts 02115, and Department of Oncology, McArdle Laboratory for Cancer Research, University of Wisconsin at Madison, Madison, Wisconsin 537063

Received 7 November 2000/Accepted 16 January 2001

Subgroups B, D, and E avian leukosis viruses (ALV-B, -D, and -E) share the same chicken receptor, TVBS1, a tumor necrosis factor receptor (TNFR)-related protein. These viruses, however, exhibit nonreciprocal receptor interference (NRI): cells preinfected with ALV-B or ALV-D are resistant to superinfection by viruses of all three subgroups, whereas those pre-infected by ALV-E are resistant only to superinfection by other subgroup E viruses. In this study, we investigated the basis of this phenomenon by characterizing the interaction of TVBS1 with ALV-B Env or ALV-E Env. Sequential immunoprecipitation analysis using surface envelope immunoglobulin fusion proteins revealed the existence of two separate types of TVBS1 that are encoded by the same cDNA clone. One form, designated the type 1 receptor, is specific for ALV-B and ALV-E. The other form, the type 2 receptor, is specific for ALV-B. We show that a protein consisting of only the first and second extracellular cysteine-rich domains of TVBS1 is capable of forming both receptor types. However, the third extracellular cysteine-rich domain is required for efficient formation of the type 1 receptor. We also demonstrate that heterogeneous N-linked glycosylation cannot explain the difference in activities of the two receptor types. The existence of two types of TVBS1 explains the NRI pattern between ALV-B and -E: subgroup B viruses establish receptor interference with both receptor types, whereas subgroup E viruses interfere only with the type 1 receptor, leaving the type 2 receptor available to mediate subsequent rounds of ALV-B entry. The formation of a TVB receptor type that is specific for cytopathic ALV may also have important implications for understanding how some subgroups of ALV cause cell death.

* Corresponding author. Mailing address: McArdle Laboratory for Cancer Research, University of Wisconsin---Madison, 1400 University Ave., Madison, WI 53706. Phone: (608) 265-5151. Fax: (608) 262-2824. E-mail: young{at}oncology.wisc.edu.

dagger Present address: Biogen, Inc., Cambridge, MA 02142.

Journal of Virology, April 2001, p. 3520-3526, Vol. 75, No. 8
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.8.3520-3526.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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