Sequential CD134-CXCR4 Interactions in Feline Immunodeficiency Virus (FIV): Soluble CD134 Activates FIV Env for CXCR4-dependent Entry and Reveals a Cryptic Neutralization Epitope

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 2006 Feb 28

PMID 16501119

Citations 28

Authors

Aymeric de Parseval

Chris K Grant

K Jagannadha Sastry

John H Elder

Affiliations

Soon will be listed here.

Abstract

Recombinant soluble CD134 (sCD134) facilitated feline immunodeficiency virus (FIV) entry into CXCR4-positive, cell surface CD134-negative target cells. sCD134-activated entry was dose dependent and CXCR4 dependent. We used the sCD134 activation system to explore the neutralization by four anti-V3 monoclonal antibodies (MAbs). V3 MAbs weakly neutralized FIV infection using target cells expressing both CD134 and CXCR4 but potently inhibited sCD134-activated entry into target cells expressing CXCR4 alone. These findings provide direct evidence for a sequential interaction of FIV Env with CD134 and CXCR4 and reveal the presence of a cryptic epitope in V3 that is masked in the mature envelope oligomers.

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References

Doms R . Chemokine receptors and HIV entry. AIDS. 2001; 15 Suppl 1:S34-5. DOI: 10.1097/00002030-200102001-00051. View

de Parseval A, Chatterji U, Morris G, Sun P, Olson A, Elder J . Structural mapping of CD134 residues critical for interaction with feline immunodeficiency virus. Nat Struct Mol Biol. 2004; 12(1):60-6. DOI: 10.1038/nsmb872. View

Dey B, Del Castillo C, Berger E . Neutralization of human immunodeficiency virus type 1 by sCD4-17b, a single-chain chimeric protein, based on sequential interaction of gp120 with CD4 and coreceptor. J Virol. 2003; 77(5):2859-65. PMC: 149752. DOI: 10.1128/jvi.77.5.2859-2865.2003. View

Shimojima M, Miyazawa T, Ikeda Y, McMonagle E, Haining H, Akashi H . Use of CD134 as a primary receptor by the feline immunodeficiency virus. Science. 2004; 303(5661):1192-5. DOI: 10.1126/science.1092124. View

de Rozieres S, Mathiason C, Rolston M, Chatterji U, Hoover E, Elder J . Characterization of a highly pathogenic molecular clone of feline immunodeficiency virus clade C. J Virol. 2004; 78(17):8971-82. PMC: 506922. DOI: 10.1128/JVI.78.17.8971-8982.2004. View

de Parseval A, Ngo S, Sun P, Elder J . Factors that increase the effective concentration of CXCR4 dictate feline immunodeficiency virus tropism and kinetics of replication. J Virol. 2004; 78(17):9132-43. PMC: 506950. DOI: 10.1128/JVI.78.17.9132-9143.2004. View

de Parseval A, Chatterji U, Sun P, Elder J . Feline immunodeficiency virus targets activated CD4+ T cells by using CD134 as a binding receptor. Proc Natl Acad Sci U S A. 2004; 101(35):13044-9. PMC: 516514. DOI: 10.1073/pnas.0404006101. View

Phillips T, Talbott R, Lamont C, Muir S, Lovelace K, Elder J . Comparison of two host cell range variants of feline immunodeficiency virus. J Virol. 1990; 64(10):4605-13. PMC: 247944. DOI: 10.1128/JVI.64.10.4605-4613.1990. View

Avrameas A, Guillet J, Chouchane L, Moraillon A, Sonigo P, Strosberg A . Localisation of three epitopes of the env protein of feline immunodeficiency virus. Mol Immunol. 1992; 29(5):565-72. DOI: 10.1016/0161-5890(92)90192-z. View

10.

Pancino G, Chappey C, Saurin W, Sonigo P . B epitopes and selection pressures in feline immunodeficiency virus envelope glycoproteins. J Virol. 1993; 67(2):664-72. PMC: 237417. DOI: 10.1128/JVI.67.2.664-672.1993. View

11.

Tozzini F, Matteucci D, Bandecchi P, Baldinotti F, Siebelink K, Osterhaus A . Neutralizing antibodies in cats infected with feline immunodeficiency virus. J Clin Microbiol. 1993; 31(6):1626-9. PMC: 265592. DOI: 10.1128/jcm.31.6.1626-1629.1993. View

12.

Lombardi S, Garzelli C, La Rosa C, Zaccaro L, Specter S, Malvaldi G . Identification of a linear neutralization site within the third variable region of the feline immunodeficiency virus envelope. J Virol. 1993; 67(8):4742-9. PMC: 237860. DOI: 10.1128/JVI.67.8.4742-4749.1993. View

13.

de Ronde A, Stam J, Boers P, Langedijk H, Meloen R, Hesselink W . Antibody response in cats to the envelope proteins of feline immunodeficiency virus: identification of an immunodominant neutralization domain. Virology. 1994; 198(1):257-64. DOI: 10.1006/viro.1994.1028. View

14.

Latza U, Durkop H, Schnittger S, Ringeling J, Eitelbach F, Hummel M . The human OX40 homolog: cDNA structure, expression and chromosomal assignment of the ACT35 antigen. Eur J Immunol. 1994; 24(3):677-83. DOI: 10.1002/eji.1830240329. View

15.

Egberink H, Keldermans L, Schuurman N, Stam J, Hesselink W, van Vliet A . Monoclonal antibodies to immunodominant and neutralizing domains of the envelope surface protein of feline immunodeficiency virus. J Gen Virol. 1994; 75 ( Pt 4):889-93. DOI: 10.1099/0022-1317-75-4-889. View

16.

Lombardi S, Garzelli C, Pistello M, Massi C, Matteucci D, Baldinotti F . A neutralizing antibody-inducing peptide of the V3 domain of feline immunodeficiency virus envelope glycoprotein does not induce protective immunity. J Virol. 1994; 68(12):8374-9. PMC: 237306. DOI: 10.1128/JVI.68.12.8374-8379.1994. View

17.

Lombardi S, Massi C, Tozzini F, Zaccaro L, Bazzichi A, Bandecchi P . Epitope mapping of the V3 domain of feline immunodeficiency virus envelope glycoprotein by monoclonal antibodies. J Gen Virol. 1995; 76 ( Pt 8):1893-9. DOI: 10.1099/0022-1317-76-8-1893. View

18.

Flynn J, Cannon C, Reid G, Rigby M, Neil J, Jarrett O . Induction of feline immunodeficiency virus-specific cell-mediated and humoral immune responses following immunization with a multiple antigenic peptide from the envelope V3 domain. Immunology. 1995; 85(2):171-5. PMC: 1383877. View

19.

Durkop H, Latza U, Himmelreich P, STEIN H . Expression of the human OX40 (hOX40) antigen in normal and neoplastic tissues. Br J Haematol. 1995; 91(4):927-31. DOI: 10.1111/j.1365-2141.1995.tb05413.x. View

20.

Richardson J, Fossati I, Moraillon A, Castelot S, Sonigo P, Pancino G . Neutralization sensitivity and accessibility of continuous B cell epitopes of the feline immunodeficiency virus envelope. J Gen Virol. 1996; 77 ( Pt 4):759-71. DOI: 10.1099/0022-1317-77-4-759. View