Gammaherpesvirus-driven plasma cell differentiation regulates virus reactivation from latently infected B lymphocytes

PLoS Pathogens

Volumn 5, Issue 11, 2009, Pages

  Liang, Xiaozhen ^a   Collins, Christopher M ^a   Mendel, Justin B ^a   Iwakoshi, Neal N ^a   Speck, Samuel H ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN M2; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; HERPES VIRUS; IN VIVO STUDY; LYMPHOMA CELL LINE; MOUSE; NONHUMAN; PLASMA CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPLEEN CELL; VIRUS GENE; VIRUS REACTIVATION; VIRUS REPLICATION; WILD TYPE; ANIMAL; B CELL LYMPHOMA; CYTOLOGY; GAMMAHERPESVIRINAE; HUMAN; PATHOLOGY; PHYSIOLOGY; SPLEEN; TUMOR CELL LINE; VIROLOGY; VIRUS ACTIVATION; VIRUS LATENCY;

HERPESVIRIDAE; HUMAN HERPESVIRUS 4; HUMAN HERPESVIRUS 8; MURINAE; MUS;

ANIMALS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE, TUMOR; GAMMAHERPESVIRINAE; HUMANS; LYMPHOMA, B-CELL; MICE; PLASMA CELLS; SPLEEN; VIRAL PROTEINS; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 73549083897     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000677     Document Type: Article

References (46)

1. Shapiro-Shelef M, Calame K (2005) Regulation of plasma-cell development. Nat Rev Immunol 5: 230-242.
2. Sciammas R, Shaffer AL, Schatz JH, Zhao H, Staudt LM, et al. (2006) Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 25: 225-236.
3. Iwakoshi NN, Lee AH, Vallabhajosyula P, Otipoby KL, Rajewsky K, et al. (2003) Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol 4: 321-329.
4. Benson MJ, Erickson LD, Gleeson MW, Noelle RJ (2007) Affinity of antigen encounter and other early B-cell signals determine B-cell fate. Curr Opin Immunol 19: 275-280.
5. Martins G, Calame K (2008) Regulation and functions of Blimp-1 in T and B lymphocytes. Annu Rev Immunol 26: 133-169.
6. Matthias P, Rolink AG (2005) Transcriptional networks in developing and mature B cells. Nat Rev Immunol 5: 497-508.
7. Crawford DH, Ando I (1986) EB virus induction is associated with B-cell maturation. Immunology 59: 405-409.
8. Wilson SJ, Tsao EH, Webb BL, Ye H, Dalton-Griffin L, et al. (2007) X box binding protein XBP-1s transactivates the Kaposi's sarcoma-associated herpesvirus (KSHV) ORF50 promoter, linking plasma cell differentiation to KSHV reactivation from latency. J Virol 81: 13578-13586.
9. Laichalk LL, Thorley-Lawson DA (2005) Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J Virol 79:1296-1307.
10. Sun CC, Thorley-Lawson DA (2007) Plasma cell-specific transcription factor XBP-1s binds to and transactivates the Epstein-Barr virus BZLF1 promoter. J Virol 81: 13566-13577.
11. Yu F, Feng J, Harada JN, Chanda SK, Kenney SC, et al. (2007) B cell terminal differentiation factor XBP-1 induces reactivation of Kaposi's sarcoma-associated herpesvirus. FEBS Lett 581: 3485-3488.
12. Bhende PM, Dickerson SJ, Sun X, Feng WH, Kenney SC (2007) X-box-binding protein 1 activates lytic Epstein-Barr virus gene expression in combination with protein kinase D. J Virol 81: 7363-7370.
13. Weck KE, Kim SS, Virgin HI, Speck SH (1999) B cells regulate murine gammaherpesvirus 68 latency. J Virol 73: 4651-4661.
14. Willer DO, Speck SH (2003) Long-term latent murine Gammaherpesvirus 68 infection is preferentially found within the surface immunoglobulin D-negative subset of splenic B cells in vivo. J Virol 77: 8310-8321.
15. Willer DO, Speck SH (2005) Establishment and maintenance of long-term murine gammaherpesvirus 68 latency in B cells in the absence of CD40. J Virol 79: 2891-2899.
16. Flano E, Husain SM, Sample JT, Woodland DL, Blackman MA (2000) Latent murine gamma-herpesvirus infection is established in activated B cells, dendritic cells, and macrophages. J Immunol 165: 1074-1081.
17. Weck KE, Kim SS, Virgin HI, Speck SH (1999) Macrophages are the major reservoir of latent murine gammaherpesvirus 68 in peritoneal cells. J Virol 73:3273-3283.
18. Herskowitz J, Jacoby MA, Speck SH (2005) The murine gammaherpesvirus 68 M2 gene is required for efficient reactivation from latently infected B cells. J Virol 79: 2261-2273.
19. Collins CM, Boss JM, Speck SH (2009) Identification of infected B cell populations using a recombinant murine gammaherpesvirus 68 expressing a fluorescent protein. J Virol.
20. Virgin HWt, Presti RM, Li XY, Liu C, Speck SH (1999) Three distinct regions of the murine gammaherpesvirus 68 genome are transcriptionally active in latently infected mice. J Virol 73: 2321-2332.
21. Jacoby MA, Virgin HWt, Speck SH (2002) Disruption of the M2 gene of murine gammaherpesvirus 68 alters splenic latency following intranasal, but not intraperitoneal, inoculation. J Virol 76: 1790-1801.
22. Simas JP, Marques S, Bridgeman A, Efstathiou S, Adler H (2004) The M2 gene product of murine gammaherpesvirus 68 is required for efficient colonization of splenic follicles but is not necessary for expansion of latently infected germinal centre B cells. J Gen Virol 85: 2789-2797.
23. Rodrigues L, Pires de Miranda M, Caloca MJ, Bustelo XR, Simas JP (2006) Activation of Vav by the gammaherpesvirus M2 protein contributes to the establishment of viral latency in B lymphocytes. J Virol 80: 6123-6135.
24. Pires de Miranda M, Alenquer M, Marques S, Rodrigues L, Lopes F, et al. (2008) The Gammaherpesvirus m2 protein manipulates the Fyn/Vav pathway through a multidocking mechanism of assembly. PLoS ONE 3: e1654. doi:10.1371/journal. pone.0001654.
25. Gray KS, Allen RD 3rd, Farrell ML, Forrest JC, Speck SH (2009) Alternatively initiated gene 50/RTA transcripts expressed during murine and human gammaherpesvirus reactivation from latency. J Virol 83: 314-328.
26. Chang H, Gwack Y, Kingston D, Souvlis J, Liang X, et al. (2005) Activation of CD21 and CD23 gene expression by Kaposi's sarcoma-associated herpesvirus RTA. J Virol 79: 4651-4663.
27. Cordier-Bussat M, Billaud M, Calender A, Lenoir GM (1993) Epstein-Barr virus (EBV) nuclear-antigen-2-induced up-regulation of CD21 and CD23 molecules is dependent on a permissive cellular context. Int J Cancer 53: 153-160.
28. Coutelier JP, van der Logt JT, Heessen FW, Warnier G, Van Snick J (1987) IgG2a restriction of murine antibodies elicited by viral infections. J Exp Med 165: 64-69.
29. Lafrenz D, Koretz S, Stratte PT, Ward RB, Strober S (1982) LPS-induced differentiation of a murine B cell leukemia (BCL1): changes in surface and secreted IgM. J Immunol 129: 1329-1335.
30. Siegel AM, Herskowitz JH, Speck SH (2008) The MHV68M2 protein drives IL-10 dependent B cell proliferation and differentiation. PLoS Pathog 4: e1000039. doi:10.1371/journal.ppat.1000039.
31. Madureira PA, Matos P, Soeiro I, Dixon LK, Simas JP, et al. (2005) Murine gamma-herpesvirus 68 latency protein M2 binds to Vav signaling proteins and inhibits B-cell receptor-induced cell cycle arrest and apoptosis in WEHI-231 B cells. J Biol Chem 280: 37310-37318.
32. Stephenson LM, Miletic AV, Kloeppel T, Kusin S, Swat W (2006) Vav proteins regulate the plasma cell program and secretory Ig production. J Immunol 177:8620-8625.
33. Jung J, Choe J, Li L, Choi YS (2000) Regulation of CD27 expression in the course of germinal center B cell differentiation: the pivotal role of IL-10. Eur J Immunol 30: 2437-2443.
34. Rousset F, Peyrol S, Garcia E, Vezzio N, Andujar M, et al. (1995) Long-term cultured CD40-activated B lymphocytes differentiate into plasma cells in response to IL-10 but not IL-4. Int Immunol 7: 1243-1253.
35. Agematsu K, Nagumo H, Oguchi Y, Nakazawa T, Fukushima K, et al. (1998) Generation of plasma cells from peripheral blood memory B cells: synergistic effect of interleukin-10 and CD27/CD70 interaction. Blood 91: 173-180.
36. Choe J, Choi YS (1998) IL-10 interrupts memory B cell expansion in the germinal center by inducing differentiation into plasma cells. Eur J Immunol 28:508-515.
37. Klein U, Casola S, Cattoretti G, Shen Q, Lia M, et al. (2006) Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat Immunol 7: 773-782.
38. Forrest JC, Speck SH (2008) Establishment of B-cell lines latently infected with reactivation-competent murine gammaherpesvirus 68 provides evidence for viral alteration of a DNA damage-signaling cascade. J Virol 82: 7688-7699.
39. Macrae AI, Dutia BM, Milligan S, Brownstein DG, Allen DJ, et al. (2001) Analysis of a novel strain of murine gammaherpesvirus reveals a genomic locus important for acute pathogenesis. J Virol 75: 5315-5327.
40. Sunil-Chandra NP, Efstathiou S, Nash AA (1992) Murine gammaherpesvirus 68 establishes a latent infection in mouse B lymphocytes in vivo. J Gen Virol 73 (Pt 12): 3275-3279.
41. Damania B, Jung JU (2001) Comparative analysis of the transforming mechanisms of Epstein-Barr virus, Kaposi's sarcoma-associated herpesvirus, and Herpesvirus saimiri. Adv Cancer Res 80: 51-82.
42. Oksenhendler E, Carcelain G, Aoki Y, Boulanger E, Maillard A, et al. (2000) High levels of human herpesvirus 8 viral load, human interleukin-6, interleukin-10, and C reactive protein correlate with exacerbation of multicentric castleman disease in HIV-infected patients. Blood 96: 2069-2073.
43. Lambert SL, Martinez OM (2007) Latent membrane protein 1 of EBV activates phosphatidylinositol 3-kinase to induce production of IL-10. J Immunol 179:8225-8234.
44. Clambey ET, Virgin HWt, Speck SH (2000) Disruption of the murine gammaherpesvirus 68 M1 open reading frame leads to enhanced reactivation from latency. J Virol 74: 1973-1984.
45. Herskowitz JH, Siegel AM, Jacoby MA, Speck SH (2008) Systematic mutagenesis of the murine gammaherpesvirus 68 M2 protein identifies domains important for chronic infection. J Virol 82: 3295-3310.
46. Hurley EA, Agger S, McNeil JA, Lawrence JB, Calendar A, et al. (1991) When Epstein-Barr virus persistently infects B-cell lines, it frequently integrates. J Virol 65: 1245-1254.