Virally-induced upregulation of heparan sulfate on B cells via the action of type I IFN

Journal of Immunology

Volumn 187, Issue 11, 2011, Pages 5540-5547

  Jarousse, Nadine ^a   Trujillo, Damian L ^a   Wilcox Adelman, Sarah ^b   Coscoy, Laurent ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APRIL PROTEIN; HEPARAN SULFATE; IMMUNOGLOBULIN A; INTERFERON; INTERFERON RECEPTOR; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEOHEPARAN SULFATE; SYNDECAN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BETAHERPESVIRINAE; CELL SURFACE; CONTROLLED STUDY; EX VIVO STUDY; GAMMAHERPESVIRINAE; HERPES VIRUS INFECTION; IMMUNOGLOBULIN PRODUCTION; IN VIVO STUDY; MOUSE; MURINE CYTOMEGALOVIRUS; MURINE GAMMA HERPES VIRUS 68; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; B-LYMPHOCYTES; BLOTTING, WESTERN; CELL SEPARATION; FLOW CYTOMETRY; GAMMAHERPESVIRINAE; HEPARITIN SULFATE; HERPESVIRIDAE INFECTIONS; IMMUNOPRECIPITATION; INTERFERON TYPE I; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUROMEGALOVIRUS; SPLEEN; UP-REGULATION;

EID: 82755164890     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003495     Document Type: Article

References (35)

1. Bernfield, M., M. Götte, P. W. Park, O. Reizes, M. L. Fitzgerald, J. Lincecum, and M. Zako. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68: 729-777. (Pubitemid 29449208)
2. Bishop, J. R., M. Schuksz, and J. D. Esko. 2007. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446: 1030-1037. (Pubitemid 46676065)
3. Lortat-Jacob, H. 2009. The molecular basis and functional implications of chemokine interactions with heparan sulphate. Curr. Opin. Struct. Biol. 19: 543-548.
4. Lin, X. 2004. Functions of heparan sulfate proteoglycans in cell signaling during development. Development 131: 6009-6021. (Pubitemid 40123916)
5. Lambaerts, K., S. A. Wilcox-Adelman, and P. Zimmermann. 2009. The signaling mechanisms of syndecan heparan sulfate proteoglycans. Curr. Opin. Cell Biol. 21: 662-669.
6. Morgan, M. R., M. J. Humphries, and M. D. Bass. 2007. Synergistic control of cell adhesion by integrins and syndecans. Nat. Rev. Mol. Cell Biol. 8: 957-969. (Pubitemid 350174639)
7. Lander, A. D. 1998. Proteoglycans: master regulators of molecular encounter? Matrix Biol. 17: 465-472. (Pubitemid 28566880)
8. Dias, S., H. Silva, Jr., A. Cumano, and P. Vieira. 2005. Interleukin-7 is necessary to maintain the B cell potential in common lymphoid progenitors. J. Exp. Med. 201: 971-979. (Pubitemid 40524466)
9. O'Connell, F. P., J. L. Pinkus, and G. S. Pinkus. 2004. CD138 (syndecan-1), a plasma cell marker immunohistochemical profile in hematopoietic and non-hematopoietic neoplasms. Am. J. Clin. Pathol. 121: 254-263. (Pubitemid 38140131)
10. Yamashita, Y., K. Oritani, E. K. Miyoshi, R. Wall, M. Bernfield, and P. W. Kincade. 1999. Syndecan-4 is expressed by B lineage lymphocytes and can transmit a signal for formation of dendritic processes. J. Immunol. 162: 5940-5948. (Pubitemid 29314949)
11. Jarousse, N., B. Chandran, and L. Coscoy. 2008. Lack of heparan sulfate expression in B-cell lines: implications for Kaposi's sarcoma-associated herpesvirus and murine gammaherpesvirus 68 infections. J. Virol. 82: 12591-12597.
12. Kimberley, F. C., L. van Bostelen, K. Cameron, G. Hardenberg, J. A. Marquart, M. Hahne, and J. P. Medema. 2009. The proteoglycan (heparan sulfate proteoglycan) binding domain of APRIL serves as a platform for ligand multimerization and cross-linking. FASEB J. 23: 1584-1595.
13. Kimberley, F. C., M. Hahne, and J. P. Medema. 2009. "APRIL hath put a spring of youth in everything": relevance of APRIL for survival. J. Cell. Physiol. 218: 1-8.
14. Schneider, P. 2005. The role of APRIL and BAFF in lymphocyte activation. Curr. Opin. Immunol. 17: 282-289. (Pubitemid 40692663)
15. van der Voort, R., R. M. Keehnen, E. A. Beuling, M. Spaargaren, and S. T. Pals. 2000. Regulation of cytokine signaling by B cell antigen receptor and CD40-controlled expression of heparan sulfate proteoglycans. J. Exp. Med. 192: 1115-1124.
16. Basler, C. F., and A. García-Sastre. 2002. Viruses and the type I interferon antiviral system: induction and evasion. Int. Rev. Immunol. 21: 305-337.
17. Barton, E. S., M. L. Lutzke, R. Rochford, and H. W. Virgin, IV. 2005. Alpha/beta interferons regulate murine gammaherpesvirus latent gene expression and reactivation from latency. J. Virol. 79: 14149-14160. (Pubitemid 41552713)
18. Dutia, B. M., D. J. Allen, H. Dyson, and A. A. Nash. 1999. Type I interferons and IRF-1 play a critical role in the control of a gammaherpesvirus infection. Virology 261: 173-179. (Pubitemid 29431770)
19. Pugliese, A., D. Cortese, and G. Forni. 1980. Polygenic control of interferon production induced by poly I:C in vivo. Brief report. Arch. Virol. 65: 83-87. (Pubitemid 10055227)
20. Ingold, K., A. Zumsteg, A. Tardivel, B. Huard, Q. G. Steiner, T. G. Cachero, F. Qiang, L. Gorelik, S. L. Kalled, H. Acha-Orbea, et al. 2005. Identification of proteoglycans as the APRIL-specific binding partners. J. Exp. Med. 201: 1375-1383. (Pubitemid 40664082)
21. Jones, K. S., C. Petrow-Sadowski, D. C. Bertolette, Y. Huang, and F. W. Ruscetti. 2005. Heparan sulfate proteoglycans mediate attachment and entry of human Tcell leukemia virus type 1 virions into CD4+ T cells. J. Virol. 79: 12692-12702. (Pubitemid 41433189)
22. Saphire, A. C., M. D. Bobardt, Z. Zhang, G. David, and P. A. Gallay. 2001. Syndecans serve as attachment receptors for human immunodeficiency virus type 1 on macrophages. J. Virol. 75: 9187-9200. (Pubitemid 32851923)
23. Rioux, V., R. Y. Landry, and A. Bensadoun. 2002. Sandwich immunoassay for the measurement of murine syndecan-4. J. Lipid Res. 43: 167-173. (Pubitemid 34117231)
24. Bret, C., D. Hose, T. Reme, A. C. Sprynski, K. Mahtouk, J. F. Schved, P. Quittet, J. F. Rossi, H. Goldschmidt, and B. Klein. 2009. Expression of genes encoding for proteins involved in heparan sulphate and chondroitin sulphate chain synthesis and modification in normal and malignant plasma cells. Br. J. Haematol. 145: 350-368.
25. Bossen, C., and P. Schneider. 2006. BAFF, APRIL and their receptors: structure, function and signaling. Semin. Immunol. 18: 263-275. (Pubitemid 44287558)
26. Shiow, L. R., D. B. Rosen, N. Brdicková, Y. Xu, J. An, L. L. Lanier, J. G. Cyster, and M. Matloubian. 2006. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440: 540-544.
27. Chang, W. L., E. S. Coro, F. C. Rau, Y. Xiao, D. J. Erle, and N. Baumgarth. 2007. Influenza virus infection causes global respiratory tract B cell response modulation via innate immune signals. J. Immunol. 178: 1457-1467. (Pubitemid 46154617)
28. Coro, E. S., W. L. Chang, and N. Baumgarth. 2006. Type I IFN receptor signals directly stimulate local B cells early following influenza virus infection. J. Immunol. 176: 4343-4351. (Pubitemid 44264414)
29. Diamond, M. S., E. M. Sitati, L. D. Friend, S. Higgs, B. Shrestha, and M. Engle. 2003. A critical role for induced IgM in the protection against West Nile virus infection. J. Exp. Med. 198: 1853-1862. (Pubitemid 38032118)
30. Purtha, W. E., K. A. Chachu, H. W. Virgin, IV, and M. S. Diamond. 2008. Early B-cell activation after West Nile virus infection requires alpha/beta interferon but not antigen receptor signaling. J. Virol. 82: 10964-10974.
31. Bach, P., E. Kamphuis, B. Odermatt, G. Sutter, C. J. Bucholz, and U. Kalinke. 2007. Vesicular stomatitis virus glycoprotein displaying retrovirus-like particles induce a type I IFN receptor-dependent switch to neutralizing IgG antibodies. J. Immunol. 178: 5839-5847. (Pubitemid 46674381)
32. Le Bon, A., C. Thompson, E. Kamphuis, V. Durand, C. Rossmann, U. Kalinke, and D. F. Tough. 2006. Cutting edge: enhancement of antibody responses through direct stimulation of B and T cells by type I IFN. J. Immunol. 176: 2074-2078. (Pubitemid 43201653)
33. Reijmers, R. M., R. W. Groen, A. Kuil, K. Weijer, F. C. Kimberley, J. P. Medema, T. H. van Kuppevelt, J. P. Li, M. Spaargaren, and S. T. Pals. 2011. Disruption of heparan sulfate proteoglycan conformation perturbs B-cell maturation and APRIL-mediated plasma cell survival. Blood 117: 6162-6171.
34. Garner, O. B., Y. Yamaguchi, J. D. Esko, and V. Videm. 2008. Small changes in lymphocyte development and activation in mice through tissue-specific alteration of heparan sulphate. Immunology 125: 420-429.
35. Bennett, L., A. K. Palucka, E. Arce, V. Cantrell, J. Borvak, J. Banchereau, and V. Pascual. 2003. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J. Exp. Med. 197: 711-723. (Pubitemid 36350866)