Maintenance of anti-Sm/RNP autoantibody production by plasma cells residing in ectopic lymphoid tissue and bone marrow memory B cells

Journal of Immunology

Volumn 190, Issue 8, 2013, Pages 3916-3927

  Weinstein, Jason S ^a,c   Delano, Matthew J ^b   Xu, Yuan ^a   Kelly Scumpia, Kindra M ^b   Nacionales, Dina C ^a   Li, Yi ^a   Lee, Pui Y ^a   Scumpia, Philip O ^b   Yang, Lijun ^b   Sobel, Eric ^a   Moldawer, Lyle L ^b   Reeves, Westley H ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CHEMOKINE RECEPTOR CXCR4; PRISTANE; RIBONUCLEOPROTEIN ANTIBODY; SM ANTIBODY; U1A ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; BLAST CELL; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DONOR; ECTOPIC TISSUE; FEMALE; HOST; IMMUNE RESPONSE; LIPOGRANULOMA; LYMPHOCYTE; LYMPHOID TISSUE; MEMORY CELL; NONHUMAN; PERITONITIS; PLASMA CELL; PLASMABLAST; PRIORITY JOURNAL; SPLEEN; T CELL DEPLETION; TISSUE TRANSPLANTATION;

ANIMALS; AUTOANTIBODIES; B-LYMPHOCYTE SUBSETS; BONE MARROW CELLS; CHORISTOMA; FEMALE; GRANULOMA; IMMUNOLOGIC MEMORY; LYMPHOID TISSUE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; PLASMA CELLS; RIBONUCLEOPROTEINS, SMALL NUCLEAR;

EID: 84875977107     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201880     Document Type: Article

References (55)

1. Aloisi, F., and R. Pujol-Borrell. 2006. Lymphoid neogenesis in chronic inflammatory diseases. Nat. Rev. Immunol. 6: 205-217.
2. Gause, A., K. Gundlach, M. Zdichavsky, G. Jacobs, B. Koch, T. Hopf, and M. Pfreundschuh. 1995. The B lymphocyte in rheumatoid arthritis: analysis of rearranged V kappa genes from B cells infiltrating the synovial membrane. Eur. J. Immunol. 25: 2775-2782.
3. Barone, F., M. Bombardieri, A. Manzo, M. C. Blades, P. R. Morgan, S. J. Challacombe, G. Valesini, and C. Pitzalis. 2005. Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjögren's syndrome. Arthritis Rheum. 52: 1773-1784.
4. Sims, G. P., H. Shiono, N. Willcox, and D. I. Stott. 2001. Somatic hypermutation and selection of B cells in thymic germinal centers responding to acetylcholine receptor in myasthenia gravis. J. Immunol. 167: 1935-1944.
5. Kratz, A., A. Campos-Neto, M. S. Hanson, and N. H. Ruddle. 1996. Chronic inflammation caused by lymphotoxin is lymphoid neogenesis. J. Exp. Med. 183: 1461-1472.
6. Satoh, M., and W. H. Reeves. 1994. Induction of lupus-associated autoantibodies in BALB/c mice by intraperitoneal injection of pristane. J. Exp. Med. 180: 2341-2346.
7. Satoh, M., A. Kumar, Y. S. Kanwar, and W. H. Reeves. 1995. Anti-nuclear antibody production and immune-complex glomerulonephritis in BALB/c mice treated with pristane. Proc. Natl. Acad. Sci. USA 92: 10934-10938.
8. Nacionales, D. C., J. S. Weinstein, X. J. Yan, E. Albesiano, P. Y. Lee, K. M. Kelly-Scumpia, R. Lyons, M. Satoh, N. Chiorazzi, and W. H. Reeves. 2009. B cell proliferation, somatic hypermutation, class switch recombination, and autoantibody production in ectopic lymphoid tissue in murine lupus. J. Immunol. 182: 4226-4236.
9. Lee, P. Y., Y. Li, Y. Kumagai, Y. Xu, J. S. Weinstein, E. S. Kellner, D. C. Nacionales, E. J. Butfiloski, N. van Rooijen, S. Akira, et al. 2009. Type I interferon modulates monocyte recruitment and maturation in chronic inflammation. Am. J. Pathol. 175: 2023-2033.
10. Nacionales, D. C., K. M. Kelly, P. Y. Lee, H. Zhuang, Y. Li, J. S. Weinstein, E. Sobel, Y. Kuroda, J. Akaogi, M. Satoh, and W. H. Reeves. 2006. Type I interferon production by tertiary lymphoid tissue developing in response to 2,6,10,14-tetramethyl-pentadecane (pristane). Am. J. Pathol. 168: 1227-1240.
11. Weinstein, J. S., D. C. Nacionales, P. Y. Lee, K. M. Kelly-Scumpia, X. J. Yan, P. O. Scumpia, D. S. Vale-Cruz, E. Sobel, M. Satoh, N. Chiorazzi, and W. H. Reeves. 2008. Colocalization of antigen-specific B and T cells within ectopic lymphoid tissue following immunization with exogenous antigen. J. Immunol. 181: 3259-3267.
12. Slifka, M. K., R. Antia, J. K. Whitmire, and R. Ahmed. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8: 363-372.
13. Ochsenbein, A. F., D. D. Pinschewer, S. Sierro, E. Horvath, H. Hengartner, and R. M. Zinkernagel. 2000. Protective long-term antibody memory by antigen-driven and T help-dependent differentiation of long-lived memory B cells to short-lived plasma cells independent of secondary lymphoid organs. Proc. Natl. Acad. Sci. USA 97: 13263-13268.
14. McHeyzer-Williams, L. J., and M. G. McHeyzer-Williams. 2005. Antigen-specific memory B cell development. Annu. Rev. Immunol. 23: 487-513.
15. Aiba, Y., K. Kometani, M. Hamadate, S. Moriyama, A. Sakaue-Sawano, M. Tomura, H. Luche, H. J. Fehling, R. Casellas, O. Kanagawa, et al. 2010. Preferential localization of IgG memory B cells adjacent to contracted germinal centers. Proc. Natl. Acad. Sci. USA 107: 12192-12197.
16. Richard, K., S. K. Pierce, and W. Song. 2008. The agonists of TLR4 and 9 are sufficient to activate memory B cells to differentiate into plasma cells in vitro but not in vivo. J. Immunol. 181: 1746-1752.
17. Bernasconi, N. L., N. Onai, and A. Lanzavecchia. 2003. A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood 101: 4500-4504.
18. Lukacs, N. W., A. Berlin, D. Schols, R. T. Skerlj, and G. J. Bridger. 2002. AMD3100, a CxCR4 antagonist, attenuates allergic lung inflammation and airway hyperreactivity. Am. J. Pathol. 160: 1353-1360.
19. Tokoyoda, K., S. Zehentmeier, A. N. Hegazy, I. Albrecht, J. R. Grün, M. Löhning, and A. Radbruch. 2009. Professional memory CD4+ T lymphocytes preferentially reside and rest in the bone marrow. Immunity 30: 721-730.
20. Lee, P. Y., J. S. Weinstein, D. C. Nacionales, P. O. Scumpia, Y. Li, E. Butfiloski, N. van Rooijen, L. Moldawer, M. Satoh, and W. H. Reeves. 2008. A novel type I IFN-producing cell subset in murine lupus. J. Immunol. 180: 5101-5108.
21. Luther, S. A., H. L. Tang, P. L. Hyman, A. G. Farr, and J. G. Cyster. 2000. Coexpression of the chemokines ELC and SLC by T zone stromal cells and deletion of the ELC gene in the plt/plt mouse. Proc. Natl. Acad. Sci. USA 97: 12694-12699.
22. O'Garra, A., and P. Vieira. 2004. Regulatory T cells and mechanisms of immune system control. Nat. Med. 10: 801-805.
23. Richards, H. B., M. Satoh, J. C. Jennette, B. P. Croker, H. Yoshida, and W. H. Reeves. 2001. Interferon-gamma is required for lupus nephritis in mice treated with the hydrocarbon oil pristane. Kidney Int. 60: 2173-2180.
24. Vieira, P., and K. Rajewsky. 1988. The half-lives of serum immunoglobulins in adult mice. Eur. J. Immunol. 18: 313-316.
25. Richards, H. B., M. Satoh, J. C. Jennette, T. Okano, Y. S. Kanwar, and W. H. Reeves. 1999. Disparate T cell requirements of two subsets of lupus-specific autoantibodies in pristane-treated mice. Clin. Exp. Immunol. 115: 547-553.
26. Gronowicz, E. S., C. Doss, F. Assisi, E. S. Vitetta, R. L. Coffman, and S. Strober. 1979. Surface Ig isotypes on cells responding to lipopolysaccharide by IgM and IgG secretion. J. Immunol. 123: 2049-2056.
27. Rothman, P., S. Lutzker, B. Gorham, V. Stewart, R. Coffman, and F. W. Alt. 1990. Structure and expression of germline immunoglobulin gamma 3 heavy chain gene transcripts: implications for mitogen and lymphokine directed class-switching. Int. Immunol. 2: 621-627.
28. Siebenkotten, G., C. Esser, M. Wabl, and A. Radbruch. 1992. The murine IgG1/IgE class switch program. Eur. J. Immunol. 22: 1827-1834.
29. Manz, R. A., A. Thiel, and A. Radbruch. 1997. Lifetime of plasma cells in the bone marrow. Nature 388: 133-134.
30. Kamphuis, E., T. Junt, Z. Waibler, R. Forster, and U. Kalinke. 2006. Type I interferons directly regulate lymphocyte recirculation and cause transient blood lymphopenia. Blood 108: 3253-3261.
31. Hauser, A. E., G. F. Debes, S. Arce, G. Cassese, A. Hamann, A. Radbruch, and R. A. Manz. 2002. Chemotactic responsiveness toward ligands for CXCR3 and CXCR4 is regulated on plasma blasts during the time course of a memory immune response. J. Immunol. 169: 1277-1282.
32. Hargreaves, D. C., P. L. Hyman, T. T. Lu, V. N. Ngo, A. Bidgol, G. Suzuki, Y. R. Zou, D. R. Littman, and J. G. Cyster. 2001. A coordinated change in chemokine responsiveness guides plasma cell movements. J. Exp. Med. 194: 45-56.
33. Omatsu, Y., T. Sugiyama, H. Kohara, G. Kondoh, N. Fujii, K. Kohno, and T. Nagasawa. 2010. The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity 33: 387-399.
34. Belnoue, E., C. Tougne, A.-F. Rochat, P.-H. Lambert, D. D. Pinschewer, and C.-A. Siegrist. 2012. Homing and adhesion patterns determine the cellular composition of the bone marrow plasma cell niche. J. Immunol. 188: 1283-1291.
35. Wang, A., A. M. Fairhurst, K. Tus, S. Subramanian, Y. Liu, F. Lin, P. Igarashi, X. J. Zhou, F. Batteux, D. Wong, et al. 2009. CXCR4/CXCL12 hyperexpression plays a pivotal role in the pathogenesis of lupus. J. Immunol. 182: 4448-4458.
36. Drayton, D. L., S. Liao, R. H. Mounzer, and N. H. Ruddle. 2006. Lymphoid organ development: from ontogeny to neogenesis. Nat. Immunol. 7: 344-353.
37. Rendt, K. E., T. S. Barry, D. M. Jones, C. B. Richter, S. S. McCachren, and B. F. Haynes. 1993. Engraftment of human synovium into severe combined immune deficient mice. Migration of human peripheral blood T cells to engrafted human synovium and to mouse lymph nodes. J. Immunol. 151: 7324-7336.
38. Tesch, G. H., S. Maifert, A. Schwarting, B. J. Rollins, and V. R. Kelley. 1999. Monocyte chemoattractant protein 1-dependent leukocytic infiltrates are responsible for autoimmune disease in MRL-Fas(lpr) mice. J. Exp. Med. 190: 1813-1824.
39. De Clercq, E. 2009. The AMD3100 story: the path to the discovery of a stem cell mobilizer (Mozobil). Biochem. Pharmacol. 77: 1655-1664.
40. Azab, A. K., J. M. Runnels, C. Pitsillides, A.-S. Moreau, F. Azab, X. Leleu, X. Jia, R. Wright, B. Ospina, A. L. Carlson, et al. 2009. CXCR4 inhibitor AMD3100 disrupts the interaction of multiple myeloma cells with the bone marrow microenvironment and enhances their sensitivity to therapy. Blood 113: 4341-4351.
41. Oliveira, A. M., D. A. Maria, M. Metzger, C. Linardi, R. R. Giorgi, F. Moura, G. A. Martinez, S. P. Bydlowski, and E. M. Novak. 2009. Thalidomide treatment down-regulates SDF-1a and CXCR4 expression in multiple myeloma patients. Leuk. Res. 33: 970-973.
42. Inamine, A., Y. Takahashi, N. Baba, K. Miyake, T. Tokuhisa, T. Takemori, and R. Abe. 2005. Two waves of memory B-cell generation in the primary immune response. Int. Immunol. 17: 581-589.
43. Bernasconi, N. L., E. Traggiai, and A. Lanzavecchia. 2002. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298: 2199-2202.
44. Herlands, R. A., S. R. Christensen, R. A. Sweet, U. Hershberg, and M. J. Shlomchik. 2008. T cell-independent and toll-like receptor-dependent antigen-driven activation of autoreactive B cells. Immunity 29: 249-260.
45. Muehlinghaus, G., L. Cigliano, S. Huehn, A. Peddinghaus, H. Leyendeckers, A. E. Hauser, F. Hiepe, A. Radbruch, S. Arce, and R. A. Manz. 2005. Regulation of CXCR3 and CXCR4 expression during terminal differentiation of memory B cells into plasma cells. Blood 105: 3965-3971.
46. Benson, M. J., S. R. Dillon, E. Castigli, R. S. Geha, S. Xu, K. P. Lam, and R. J. Noelle. 2008. Cutting edge: the dependence of plasma cells and independence of memory B cells on BAFF and APRIL. J. Immunol. 180: 3655-3659.
47. Elgueta, R., V. C. de Vries, and R. J. Noelle. 2010. The immortality of humoral immunity. Immunol. Rev. 236: 139-150.
48. Shimoda, M., F. Mmanywa, S. K. Joshi, T. Li, K. Miyake, J. Pihkala, J. A. Abbas, and P. A. Koni. 2006. Conditional ablation of MHC-II suggests an indirect role for MHC-II in regulatory CD4 T cell maintenance. J. Immunol. 176: 6503-6511.
49. Dogan, I., B. Bertocci, V. Vilmont, F. Delbos, J. Mégret, S. Storck, C.-A. Reynaud, and J.-C. Weill. 2009. Multiple layers of B cell memory with different effector functions. Nat. Immunol. 10: 1292-1299.
50. Yoshida, T., H. Mei, T. Dörner, F. Hiepe, A. Radbruch, S. Fillatreau, and B. F. Hoyer. 2010. Memory B and memory plasma cells. Immunol. Rev. 237: 117-139.
51. Hoyer, B. F., K. Moser, A. E. Hauser, A. Peddinghaus, C. Voigt, D. Eilat, A. Radbruch, F. Hiepe, and R. A. Manz. 2004. Short-lived plasmablasts and long-lived plasma cells contribute to chronic humoral autoimmunity in NZB/W mice. J. Exp. Med. 199: 1577-1584.
52. Moser, K., K. Tokoyoda, A. Radbruch, I. MacLennan, and R. A. Manz. 2006. Stromal niches, plasma cell differentiation and survival. Curr. Opin. Immunol. 18: 265-270.
53. Ueda, Y., M. Kondo, and G. Kelsoe. 2005. Inflammation and the reciprocal production of granulocytes and lymphocytes in bone marrow. J. Exp. Med. 201: 1771-1780.
54. Ueda, Y., K. Yang, S. J. Foster, M. Kondo, and G. Kelsoe. 2004. Inflammation controls B lymphopoiesis by regulating chemokine CXCL12 expression. J. Exp. Med. 199: 47-58.
55. Kim, H. K., M. De La Luz Sierra, C. K. Williams, A. V. Gulino, and G. Tosato. 2006. G-CSF down-regulation of CXCR4 expression identified as a mechanism for mobilization of myeloid cells. Blood 108: 812-820.