Cd22 is required for protection against West Nile virus infection

Journal of Virology

Volumn 87, Issue 6, 2013, Pages 3361-3375

  Ma, Daphne Y ^a   Suthar, Mehul S ^a   Kasahara, Shinji ^a,b   Gale, Michael ^a   Clark, Edward A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD22 ANTIGEN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CELLULAR IMMUNITY; CENTRAL NERVOUS SYSTEM; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DENDRITIC CELL; FEMALE; FLAVIVIRUS INFECTION; HUMORAL IMMUNITY; INFECTION CONTROL; INFECTION SENSITIVITY; KNOCKOUT MOUSE; LYMPH NODE; LYMPHOCYTE MIGRATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; VIRUS LOAD; WEST NILE VIRUS INFECTION; WILD TYPE;

ANIMALS; ANTIBODIES, VIRAL; BLOOD; CD8-POSITIVE T-LYMPHOCYTES; CENTRAL NERVOUS SYSTEM; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SIALIC ACID BINDING IG-LIKE LECTIN 2; VIRAL LOAD; WEST NILE FEVER; WEST NILE VIRUS;

EID: 84874726385     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02368-12     Document Type: Article

References (62)

1. Samuel MA, Diamond MS. 2006. Pathogenesis of West Nile virus infection: a balance between virulence, innate and adaptive immunity, and viral evasion. J. Virol. 80:9349-9360.
2. Diamond MS, Shrestha B, Marri A, Mahan D, Engle M. 2003. B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J. Virol. 77:2578-2586.
3. Diamond MS, Sitati EM, Friend LD, Higgs S, Shrestha B, Engle M. 2003. A critical role for induced IgM in the protection against West Nile virus infection. J. Exp. Med. 198:1853-1862.
4. Engle MJ, Diamond MS. 2003. Antibody prophylaxis and therapy against West Nile virus infection in wild-type and immunodeficient mice. J. Virol. 77:12941-12949.
5. Dörken B, Moldenhauer G, Pezzutto A, Schwartz R, Feller A, Kiesel S, Nadler LM. 1986. HD39 (B3), a B lineage-restricted antigen whose cell surface expression is limited to resting and activated human B lymphocytes. J. Immunol. 136:4470-4479.
6. Stamenkovic I, Sgroi D, Aruffo A, Sy MS, Anderson T. 1991. The B lymphocyte adhesion molecule CD22 interacts with leukocyte common antigen CD45RO on T cells and alpha 2-6 sialyltransferase, CD75, on B cells. Cell 66:1133-1144.
7. Torres RM, Law CL, Santos-Argumedo L, Kirkham PA, Grabstein K, Parkhouse RM, Clark EA. 1992. Identification and characterization of the murine homologue of CD22, a B lymphocyte-restricted adhesion molecule. J. Immunol. 149:2641-2649.
8. Law CL, Sidorenko SP, Chandran KA, Zhao Z, Shen SH, Fischer EH, Clark EA. 1996. CD22 associates with protein tyrosine phosphatase 1C, Syk, and phospholipase C-gamma(1) upon B cell activation. J. Exp. Med. 183:547-560.
9. Schulte RJ, Campbell MA, Fischer WH, Sefton BM. 1992. Tyrosine phosphorylation of CD22 during B cell activation. Science 258:1001-1004.
10. Clark EA. 1993. CD22, a B cell-specific receptor, mediates adhesion and signal transduction. J. Immunol. 150:4715-4718.
11. Stamenkovic I, Seed B. 1990. The B-cell antigen CD22 mediates monocyte and erythrocyte adhesion. Nature 345:74-77.
12. Pezzutto A, Dorken B, Moldenhauer G, Clark EA. 1987. Amplification of human B cell activation by a monoclonal antibody to the B cell-specific antigen CD22, Bp 130/140. J. Immunol. 138:98-103.
13. Pezzutto A, Rabinovitch PS, Dorken B, Moldenhauer G, Clark EA. 1988. Role of the CD22 human B cell antigen in B cell triggering by antiimmunoglobulin. J. Immunol. 140:1791-1795.
14. Tuscano J, Engel P, Tedder TF, Kehrl JH. 1996. Engagement of the adhesion receptor CD22 triggers a potent stimulatory signal for B cells and blocking CD22/CD22L interactions impairs T-cell proliferation. Blood 87:4723-4730.
15. Law CL, Aruffo A, Chandran KA, Doty RT, Clark EA. 1995. Ig domains 1 and 2 of murine CD22 constitute the ligand-binding domain and bind multiple sialylated ligands expressed on B and T cells. J. Immunol. 155: 3368-3376.
16. Santos L, Draves KE, Boton M, Grewal PK, Marth JD, Clark EA. 2008. Dendritic cell-dependent inhibition of B cell proliferation requires CD22. J. Immunol. 180:4561-4569.
17. Tedder TF, Tuscano J, Sato S, Kehrl JH. 1997. CD22, a B lymphocytespecific adhesion molecule that regulates antigen receptor signaling. Annu. Rev. Immunol. 15:481-504.
18. Samardzic T, Marinkovic D, Danzer CP, Gerlach J, Nitschke L, Wirth T. 2002. Reduction of marginal zone B cells in CD22-deficient mice. Eur. J. Immunol. 32:561-567.
19. Nitschke L, Carsetti R, Ocker B, Kohler G, Lamers MC. 1997. CD22 is a negative regulator of B-cell receptor signalling. Curr. Biol. 7:133-143.
20. O'Keefe TL, Williams GT, Davies SL, Neuberger MS. 1996. Hyperresponsive B cells in CD22-deficient mice. Science 274:798-801.
21. Otipoby KL, Andersson KB, Draves KE, Klaus SJ, Farr AG, Kerner JD, Perlmutter RM, Law CL, Clark EA. 1996. CD22 regulates thymusindependent responses and the lifespan of B cells. Nature 384:634-637.
22. Poe JC, Haas KM, Uchida J, Lee Y, Fujimoto M, Tedder TF. 2004. Severely impaired B lymphocyte proliferation, survival, and induction of the c-Myc:Cullin 1 ubiquitin ligase pathway resulting from CD22 deficiency on the C57BL/6 genetic background. J. Immunol. 172: 2100-2110.
23. Fehr T, Lopez-Macias C, Odermatt B, Torres RM, Schubart DB, O'Keefe TL, Matthias P, Hengartner H, Zinkernagel RM. 2000. Correlation of anti-viral B cell responses and splenic morphology with expression of B cell-specific molecules. Int. Immunol. 12:1275-1284.
24. Gjertsson I, Nitschke L, Tarkowski A. 2004. The role of B cell CD22 expression in Staphylococcus aureus arthritis and sepsis. Microbes Infect. 6:377-382.
25. Keller BC, Fredericksen BL, Samuel MA, Mock RE, Mason PW, Diamond MS, Gale M, Jr. 2006. Resistance to alpha/beta interferon is a determinant of West Nile virus replication fitness and virulence. J. Virol. 80:9424-9434.
26. Suthar MS, Brassil MM, Blahnik G, Gale M, Jr. 2012. Infectious clones of novel lineage 1 and lineage 2 West Nile virus strains WNV-TX02 and WNV-Madagascar. J. Virol. 86:7704-7709.
27. Suthar MS, Ma DY, Thomas S, Lund JM, Zhang N, Daffis S, Rudensky AY, Bevan MJ, Clark EA, Kaja MK, Diamond MS, Gale M, Jr. 2010. IPS-1 is essential for the control of West Nile virus infection and immunity. PLoS Pathog. 6:e1000757. doi:10.1371/journal.ppat.1000757.
28. Linke S, Ellerbrok H, Niedrig M, Nitsche A, Pauli G. 2007. Detection of West Nile virus lineages 1 and 2 by real-time PCR. J. Virol. Methods 146:355-358.
29. Mehlhop E, Fuchs A, Engle M, Diamond MS. 2009. Complement modulates pathogenesis and antibody-dependent neutralization of West Nile virus infection through a C5-independent mechanism. Virology 393: 11-15.
30. Frey A, Di Canzio J, Zurakowski D. 1998. A statistically defined endpoint titer determination method for immunoassays. J. Immunol. Methods 221: 35-41.
31. Purtha WE, Myers N, Mitaksov V, Sitati E, Connolly J, Fremont DH, Hansen TH, Diamond MS. 2007. Antigen-specific cytotoxic T lymphocytes protect against lethal West Nile virus encephalitis. Eur. J. Immunol. 37:1845-1854.
32. Brien JD, Uhrlaub JL, Nikolich-Zugich J. 2008. West Nile virus-specific CD4 T cells exhibit direct antiviral cytokine secretion and cytotoxicity and are sufficient for antiviral protection. J. Immunol. 181:8568-8575.
33. Kasahara S, Clark EA. 2012. Dendritic cell-associated lectin 2 (DCAL2) defines a distinct CD8alpha-dendritic cell subset. J. Leukoc. Biol. 91:437-448.
34. Barber DL, Wherry EJ, Ahmed R. 2003. Cutting edge: rapid in vivo killing by memory CD8 T cells. J. Immunol. 171:27-31.
35. Bourne N, Scholle F, Silva MC, Rossi SL, Dewsbury N, Judy B, De Aguiar JB, Leon MA, Estes DM, Fayzulin R, Mason PW. 2007. Early production of type I interferon during West Nile virus infection: role for lymphoid tissues in IRF3-independent interferon production. J. Virol. 81:9100-9108.
36. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academies Press, Washington, DC.
37. Szretter KJ, Daffis S, Patel J, Suthar MS, Klein RS, Gale M, Jr, Diamond MS. 2010. The innate immune adaptor molecule MyD88 restricts West Nile virus replication and spread in neurons of the central nervous system. J. Virol. 84:12125-12138
38. Shrestha B, Diamond MS. 2004. Role of CD8 T cells in control of West Nile virus infection. J. Virol. 78:8312-8321.
39. Sitati EM, Diamond MS. 2006. CD4 T-cell responses are required for clearance of West Nile virus from the central nervous system. J. Virol. 80:12060-12069.
40. Shrestha B, Samuel MA, Diamond MS. 2006. CD8 T cells require perforin to clear West Nile virus from infected neurons. J. Virol. 80:119-129.
41. Shortman K, Liu YJ. 2002. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2:151-161.
42. Shortman K, Heath WR. 2010. The CD8 dendritic cell subset. Immunol. Rev. 234:18-31.
43. McCandless EE, Zhang B, Diamond MS, Klein RS. 2008. CXCR4 antagonism increases T cell trafficking in the central nervous system and improves survival from West Nile virus encephalitis. Proc. Natl. Acad. Sci. U. S. A. 105:11270-11275.
44. Sitati E, McCandless EE, Klein RS, Diamond MS. 2007. CD40-CD40 ligand interactions promote trafficking of CD8T cells into the brain and protection against West Nile virus encephalitis. J. Virol. 81:9801-9811.
45. Bréhin AC, Mouries J, Frenkiel MP, Dadaglio G, Despres P, Lafon M, Couderc T. 2008. Dynamics of immune cell recruitment during West Nile encephalitis and identification of a new CD19 B220 BST-2 leukocyte population. J. Immunol. 180:6760-6767.
46. Lefrançois L, Parker CM, Olson S, Muller W, Wagner N, Schon MP, Puddington L. 1999. The role of beta7 integrins in CD8 T cell trafficking during an antiviral immune response. J. Exp. Med. 189:1631-1638.
47. Davison AM, King NJ. 2011. Accelerated dendritic cell differentiation from migrating Ly6C(lo) bone marrow monocytes in early dermal West Nile virus infection. J. Immunol. 186:2382-2396.
48. Lim JK, Murphy PM. 2011. Chemokine control of West Nile virus infection. Exp. Cell Res. 317:569-574.
49. Luther SA, Cyster JG. 2001. Chemokines as regulators of T cell differentiation. Nat. Immunol. 2:102-107.
50. Masson F, Mount AM, Wilson NS, Belz GT. 2008. Dendritic cells: driving the differentiation programme of T cells in viral infections. Immunol. Cell Biol. 86:333-342.
51. Edwards AD, Chaussabel D, Tomlinson S, Schulz O, Sher A, Reis e Sousa C. 2003. Relationships among murine CD11c(high) dendritic cell subsets as revealed by baseline gene expression patterns. J. Immunol. 171: 47-60.
52. Liu Y, Mullbacher A. 1988. Astrocytes are not susceptible to lysis by natural killer cells. J. Neuroimmunol. 19:101-110.
53. Liu Y, Blanden RV, Mullbacher A. 1989. Identification of cytolytic lymphocytes in West Nile virus-infected murine central nervous system. J. Gen. Virol. 70(Part 3):565-573.
54. Shrestha B, Diamond MS. 2007. Fas ligand interactions contribute to CD8 T-cell-mediated control of West Nile virus infection in the central nervous system. J. Virol. 81:11749-11757.
55. Nitschke L, Floyd H, Ferguson DJ, Crocker PR. 1999. Identification of CD22 ligands on bone marrow sinusoidal endothelium implicated in CD22-dependent homing of recirculating B cells. J. Exp. Med. 189:1513-1518.
56. Engel P, Nojima Y, Rothstein D, Zhou LJ, Wilson GL, Kehrl JH, Tedder TF. 1993. The same epitope on CD22 of B lymphocytes mediates the adhesion of erythrocytes, T and B lymphocytes, neutrophils, and monocytes. J. Immunol. 150:4719-4732.
57. Stamenkovic I, Sgroi D, Aruffo A. 1992. CD22 binds to alpha-2,6- sialyltransferase-dependent epitopes on COS cells. Cell 68:1003-1004.
58. Zeng J, Joo HM, Rajini B, Wrammert JP, Sangster MY, Onami TM. 2009. The generation of influenza-specific humoral responses is impaired in ST6Gal I-deficient mice. J. Immunol. 182:4721-4727.
59. Kim CH, Broxmeyer HE. 1999. Chemokines: signal lamps for trafficking of T and B cells for development and effector function. J. Leukoc. Biol. 65:6-15.
60. Castellino F, Huang AY, Altan-Bonnet G, Stoll S, Scheinecker C, Germain RN. 2006. Chemokines enhance immunity by guiding naive CD8 T cells to sites of CD4T cell-dendritic cell interaction. Nature 440:890-895.
61. Glass WG, Lim JK, Cholera R, Pletnev AG, Gao JL, Murphy PM. 2005. Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J. Exp. Med. 202:1087-1098.
62. Lim JK, McDermott DH, Lisco A, Foster GA, Krysztof D, Follmann D, Stramer SL, Murphy PM. 2010. CCR5 deficiency is a risk factor for early clinical manifestations of West Nile virus infection but not for viral transmission. J. Infect. Dis. 201:178-185.