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Andrew Stewart, Anthony C. Minson, Stacey Efstathiou, and Antonio Alcami From the Division of Virology, Department of Pathology, University of Cambridge, Cambridge CB2 1QP, United Kingdom Abstract Chemokines are a family of small proteins that interact with seven-transmembrane domain re- ceptors and modulate the migration of immune cells into sites of inflammation and infection.

The murine gammaherpesvirus 68 M3 gene encodes a secreted kD protein with no se- quence similarity to known chemokine receptors. We show that M3 binds a broad range of Downloaded from jem. This herpesvirus chemokine binding protein hvCKBP blocks the interaction of chemokines with high-affinity cellular re- ceptors and inhibits chemokine-induced elevation of intracellular calcium levels. Chemokines form a chemi- infection and inflammation is an important phenomenon in cal gradient via electrostatic interactions with negatively host defense.

Chemokines are chemotactic cytokines that charged glycosaminoglycans GAGs. CKRs and play a key role in leukocyte recruitment; they Chemokines are tightly regulated to prevent excessive have also been implicated in hematopoiesis, angiogenesis, inflammation that can cause disease and represent targets and development 1, 2. Chemokines are divided into four for therapeutic intervention. The production of soluble ver- structural subfamilies based on the number and arrange- sions of cytokine receptors represents a strategy to block cy- ment of conserved cysteines: CC chemokines such as tokine activity 3.

Phone: ; Fax: ; E-mail: CKRs, which modulate or utilize the chemokine network aa mole. Mu- transcription to yield pM3MV Interest in MHV stems from blot hybridization.

The B lymphocytes and macrophages 13— Recombinant M3 protein contain- M3 is transcribed during acute infection and at early stages ing a COOH-terminal 6-histidine tag was produced in Spodoptera Downloaded from jem. However, the frugiperda Sf 21 insect cells infected with AcM3. The recombi- precise function of this ORF is unclear. M3 encodes a kD nant baculovirus AcB15R has been described Supernatants from MHV—infected BHK- lytic transcript, and it has been proposed that this protein may 21 cells or baculovirus-infected Sf21 cells, infected at high multi- interact with host cellular receptors or cytokines Cross-linking rus chemokine binding protein hvCKBP is to block the experiments with bis sulfosuccinimidyl suberate BS 3; 5 mM; interaction of chemokines with cellular receptors.

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The amount of medium creted from infected cells and sequesters chemokines. Subsequently, 2. MHV was grown and assayed in baby hamster kidney BHK - 21 cells and purified from cell supernatants by Ficoll gradient centrifugation The higher molecular size complex observed was probably the result of protein aggregation and was not observed when samples were not boiled before the electrophoretic analysis data not shown.

A revertant virus named MHV-M3R in which the M3 ORF was reinserted into the virus ge- nome was also constructed to control for possible muta- tions elsewhere in the viral genome. To fur- ther demonstrate that the M3 protein binds chemokines, a Figure 2. This complex was not found with Samples were treated with the cross-linker BS3. The MHV genome con- tains , bp of unique sequence flanked by variable copies of a 1,bp terminal repeat To determine the binding specificity of M3, cross-linking experiments were carried out with radiolabeled CC and CXC chemo- kines in the presence of various amounts of unlabeled chemo- kine competitors.

A soluble chemokine binding activity is encoded by MHV Human lymphotactin and the soluble chemo- Media from BHK cells uninfected Mock or infected with MHV kine domain of human fractalkine, the single members of were incubated with I-labeled chemokines and treated with the cross- linker BS3. The positions of the chemokines and ligand— inhibited binding to both I-labeled IL-8 and I-labeled receptor complexes are indicated.

The competition profiles of the chemokines tested Parry et al. Cross-linking of 0. The concentrations of unlabeled chemokines were , , , and 2,fold excess. The doses of heparin and heparan sulfate added were 1,, , 10, 1, 0. The secreted M3 protein shows no amino acid se- preincubated with different doses of heparin and heparan quence similarity to seven-transmembrane domain CKRs, sulfate before the addition of MHV supernatants.

The partial inhibitory effect with identifiable homology to known cellular or viral proteins, high doses of MHV-M3LacZ supernatants was also ob- but displays significant sequence similarity to the MHV served with mock-infected BHK supernatants data not ORF M1 17, 18 , which is dispensable for the establish- shown. Inhibition of chemokine binding to cells was ment of and reactivation from latency Interestingly, hvCKBP does not bind to human B cell—specific or murine neutrophil—specific CXC chemo- kines, which may be of relevance in viral pathogenesis.

The poxvi- rus CKBP has no sequence similarity to the M3 protein and is likely to interact with chemokines in a different way. Future structural analysis of these viral CKBPs will establish the molecular interaction of soluble chemokine inhibitors Figure 4. The dose of supernatant corresponding to MHV—infected cells indicates an immune modulatory a number of cells cell equivalents is indicated. The binding specificity role for the M3 protein. Notably, M3 transcription has also been detected in spleens of la- tently infected mice 17, 26 and is localized to periarteri- although the functionally important serpin hinge region is olar lymphoid sheets early during the establishment of la- not conserved 10, The absence of chemokine binding tency This indicates that the affinity of These include the expression of secreted CKBPs that block hvCKBP for these chemokines is similar to or higher than interaction of chemokines with cellular receptors or GAGs 5, 6, 24 , chemokine-like proteins that may block or acti- vate specific chemokine pathways 7 , and seven-transmem- brane domain CKR homologues that may downregulate the local concentration of chemokines or hijack chemo- kine-induced signals 7.

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Some of these viral proteins, such as the HHV-8 vMIP-2 that has angiogenic properties 29 , may also contribute directly to pathology. Viral proteins that counteract the immune system have been optimized during evolution and represent potential sources of immunomodulatory proteins 4—6, As chemokines have been implicated in many disease pro- cesses, such as rheumatoid arthritis, transplant rejection, HIV progression, and atherosclerosis, the novel soluble chemokine inhibitor encoded by MHV has potential Figure 5.

Recombinant hvCKBP blocks chemokine biological activity therapeutic applications.

The existence of a large number in vitro. The dose of su- pernatant corresponding to a number of cells cell equivalents is indi- may be advantageous. In addition, hvCKBP may provide cated. Cell signaling is expressed as the percentage of cells with elevated the structural scaffolding needed to design soluble chemo- calcium levels in the presence of RANTES alone.

Weck, K.

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Kim, H. Virgin, and S. B sents a novel virus immune evasion strategy that provides cells regulate murine gammaherpesvirus 68 latency. Macrophages are the major reservoir of latent murine gam- We thank Phillip Stevenson for helpful discussions, Nigel Miller maherpesvirus 68 in peritoneal cells.

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Babraham Institute, Cambridge for help with calcium mobiliza- Simas, J. Swann, R. Bowden, and S. Analysis of murine gammaherpesvirus transcription dur- This work was funded by grants from the Wellcome Trust ing lytic and latent infection. Preiter, H. Virgin 4th, and S. Medical Research Council. Alcami is a Wellcome Trust Senior Identification and initial characterization of the murine Research Fellow. Submitted: 3 September Bowden, V. Paige, and S. Revised: 10 November Four tRNA-like sequences and a serpin homologue encoded Accepted: 11 November by murine gammaherpesvirus 68 are dispensable for lytic rep- lication in vitro and latency in vivo.

Wilkinson, G. Baggiolini, M. Chemokines and leukocyte traffic. Na- defective adenovirus vector. Nucleic Acids Res. Alcami, A.

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Symons, P. Collins, T. Williams, and Downloaded from jem. Rollins, B.