What Is and what should always have been: Long-lived plasma cells induced by T cell-independent antigens

Journal of Immunology

Volumn 190, Issue 12, 2013, Pages 5913-5918

  Bortnick, Alexandra ^a   Allman, David ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; APRIL PROTEIN; B CELL ACTIVATING FACTOR; B CELL ACTIVATING FACTOR RECEPTOR; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CHEMOKINE RECEPTOR CXCR4; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; PNEUMOCOCCUS VACCINE; POLYSACCHARIDE; POLYSACCHARIDE VACCINE; STROMAL CELL DERIVED FACTOR 1; VERY LATE ACTIVATION ANTIGEN 4;

2009 H1N1 INFLUENZA; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; B LYMPHOCYTE DIFFERENTIATION; BORRELIA HERMSII; DRUG EFFICACY; EHRLICHIA MURIS; ENTEROBACTER CLOACAE; GERMINAL CENTER; HUMAN; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY CELL; NONHUMAN; PLASMA CELL; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT SURVEY; STREPTOCOCCUS PNEUMONIAE; T LYMPHOCYTE; VACCINATION; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS;

ANIMALS; ANTIGENS; CELL DIFFERENTIATION; HUMANS; LYMPHOCYTE ACTIVATION; PLASMA CELLS; T-LYMPHOCYTES;

EID: 84879126012     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300161     Document Type: Short Survey

References (70)

1. Radbruch, A., G. Muehlinghaus, E. O. Luger, A. Inamine, K. G. Smith, T. Dörner, and F. Hiepe. 2006. Competence and competition: the challenge of becoming a long-lived plasma cell. Nat. Rev. Immunol. 6: 741-750. (Pubitemid 44453460)
2. Mora, J. R., and U. H. von Andrian. 2008. Differentiation and homing of IgA-secreting cells. Mucosal Immunol. 1: 96-109.
3. Victora, G. D., and M. C. Nussenzweig. 2012. Germinal centers. Annu. Rev. Immunol. 30: 429-457.
4. Hammarlund, E., M. W. Lewis, S. G. Hansen, L. I. Strelow, J. A. Nelson, G. J. Sexton, J. M. Hanifin, and M. K. Slifka. 2003. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9: 1131-1137. (Pubitemid 37173696)
5. Yu, X., T. Tsibane, P. A. McGraw, F. S. House, C. J. Keefer, M. D. Hicar, T. M. Tumpey, C. Pappas, L. A. Perrone, O. Martinez, et al. 2008. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455: 532-536.
6. Waffarn, E. E., and N. Baumgarth. 2011. Protective B cell responses to flu: no fluke! J. Immunol. 186: 3823-3829.
7. Nossal, G. J., and O. Makela. 1962. Autoradiographic studies on the immune response. I. The kinetics of plasma cell proliferation. J. Exp. Med. 115: 209-230.
8. Makela, O., and G. J. Nossal. 1962. Autoradiographic studies on the immune response. II. DNA synthesis amongst single antibody-producing cells. J. Exp. Med. 115: 231-244.
9. Schooley, J. C. 1961. Autoradiographic observations of plasma cell formation. J. Immunol. 86: 331-337.
10. Lévy, M., P. Vieira, A. Coutinho, and A. Freitas. 1987. The majority of "natural" immunoglobulin-secreting cells are short-lived and the progeny of cycling lymphocytes. Eur. J. Immunol. 17: 849-854. (Pubitemid 17101877)
11. 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. (Pubitemid 35471246)
12. Gray, D. 2002. A role for antigen in the maintenance of immunological memory. Nat. Rev. Immunol. 2: 60-65. (Pubitemid 37328777)
13. Gray, D., and H. Skarvall. 1988. B-cell memory is short-lived in the absence of antigen. Nature 336: 70-73. (Pubitemid 18262136)
14. Manz, R. A., A. Thiel, and A. Radbruch. 1997. Lifetime of plasma cells in the bone marrow. Nature 388: 133-134. (Pubitemid 27297440)
15. Slifka, M. K., R. Antia, J. K. Whitmire, and R. Ahmed. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8: 363-372. (Pubitemid 28188896)
16. Manz, R. A., M. Löhning, G. Cassese, A. Thiel, and A. Radbruch. 1998. Survival of long-lived plasma cells is independent of antigen. Int. Immunol. 10: 1703-1711. (Pubitemid 28502384)
17. Ahuja, A., S. M. Anderson, A. Khalil, and M. J. Shlomchik. 2008. Maintenance of the plasma cell pool is independent of memory B cells. Proc. Natl. Acad. Sci. USA 105: 4802-4807. (Pubitemid 351753827)
18. Cambridge, G., W. Stohl, M. J. Leandro, T.-S. Migone, D. M. Hilbert, and J. C. W. Edwards. 2006. Circulating levels of B lymphocyte stimulator in patients with rheumatoid arthritis following rituximab treatment: relationships with B cell depletion, circulating antibodies, and clinical relapse. Arthritis Rheum. 54: 723-732.
19. Amanna, I. J., N. E. Carlson, and M. K. Slifka. 2007. Duration of humoral immunity to common viral and vaccine antigens. N. Engl. J. Med. 357: 1903-1915. (Pubitemid 350074686)
20. Di Genova, G., J. Roddick, F. McNicholl, and F. K. Stevenson. 2006. Vaccination of human subjects expands both specific and bystander memory T cells but antibody production remains vaccine specific. Blood 107: 2806-2813.
21. Dunne, A., N. A. Marshall, and K. H. G. Mills. 2011. TLR based therapeutics. Curr. Opin. Pharmacol. 11: 404-411.
22. González-García, I., B. Rodríguez-Bayona, F. Mora-López, A. Campos-Caro, and J. A. Brieva. 2008. Increased survival is a selective feature of human circulating antigen-induced plasma cells synthesizing high-affinity antibodies. Blood 111: 741-749.
23. Racine, R., and G. M. Winslow. 2009. IgM in microbial infections: taken for granted? Immunol. Lett. 125: 79-85.
24. Brown, J. S., T. Hussell, S. M. Gilliland, D. W. Holden, J. C. Paton, M. R. Ehrenstein, M. J. Walport, and M. Botto. 2002. The classical pathway is the dominant complement pathway required for innate immunity to Streptococcus pneumoniae infection in mice. Proc. Natl. Acad. Sci. USA 99: 16969-16974. (Pubitemid 36034082)
25. Haas, K. M., J. C. Poe, D. A. Steeber, and T. F. Tedder. 2005. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 23: 7-18. (Pubitemid 41019653)
26. Alugupalli, K. R., R. M. Gerstein, J. Chen, E. Szomolanyi-Tsuda, R. T. Woodland, and J. M. Leong. 2003. The resolution of relapsing fever borreliosis requires IgM and is concurrent with expansion of B1b lymphocytes. J. Immunol. 170: 3819-3827. (Pubitemid 36359252)
27. Alugupalli, K. R., J. M. Leong, R. T. Woodland, M. Muramatsu, T. Honjo, and R. M. Gerstein. 2004. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21: 379-390. (Pubitemid 39208339)
28. Choi, Y. S., and N. Baumgarth. 2008. Dual role for B-1a cells in immunity to influenza virus infection. J. Exp. Med. 205: 3053-3064.
29. Fidler, J. M. 1975. In vivo immune response to TNP hapten coupled to thymus-independent carrier lipopolysaccharide. Cell. Immunol. 16: 223-236.
30. Sze, D. M., K. M. Toellner, C. García de Vinuesa, D. R. Taylor, and I. C. MacLennan. 2000. Intrinsic constraint on plasmablast growth and extrinsic limits of plasma cell survival. J. Exp. Med. 192: 813-821.
31. Kallies, A., J. Hasbold, D. M. Tarlinton, W. Dietrich, L. M. Corcoran, P. D. Hodgkin, and S. L. Nutt. 2004. Plasma cell ontogeny defined by quantitative changes in Blimp-1 expression. J. Exp. Med. 200: 967-977. (Pubitemid 39431122)
32. Pelletier, N., M. Casamayor-Pallejà, K. De Luca, P. Mondière, F. Saltel, P. Jurdic, C. Bella, L. Genestier, and T. Defrance. 2006. The endoplasmic reticulum is a key component of the plasma cell death pathway. J. Immunol. 176: 1340-1347. (Pubitemid 43134275)
33. Burlen, O., A. Coutinho, and A. A. Freitas. 1988. Long-lasting thymusindependent immune responses to anti-idiotype lipopolysaccharide conjugates require continuous B cell renewal. Eur. J. Immunol. 18: 1433-1439.
34. Ho, F., J. E. Lortan, I. C. MacLennan, and M. Khan. 1986. Distinct short-lived and long-lived antibody-producing cell populations. Eur. J. Immunol. 16: 1297-1301. (Pubitemid 17171537)
35. Cancro, M. P., A. P. Sah, S. L. Levy, D. M. Allman, M. R. Schmidt, and R. T. Woodland. 2001. xid mice reveal the interplay of homeostasis and Bruton's tyrosine kinase-mediated selection at multiple stages of B cell development. Int. Immunol. 13: 1501-1514. (Pubitemid 33133877)
36. Smith, K. G., T. D. Hewitson, G. J. Nossal, and D. M. Tarlinton. 1996. The phenotype and fate of the antibody-forming cells of the splenic foci. Eur. J. Immunol. 26: 444-448. (Pubitemid 26060254)
37. Möller, G. 1965. 19S antibody production against soluble lipopolysaccharide antigens by individual lymphoid cells in vitro. Nature 207: 1166-1168.
38. Taillardet, M., G. Haffar, P. Mondière, M. J. Asensio, H. Gheit, N. Burdin, T. Defrance, and L. Genestier. 2009. The thymus-independent immunity conferred by a pneumococcal polysaccharide is mediated by long-lived plasma cells. Blood 114: 4432-4440.
39. Foote, J. B., T. I. Mahmoud, A. M. Vale, and J. F. Kearney. 2012. Long-term maintenance of polysaccharide-specific antibodies by IgM-secreting cells. J. Immunol. 188: 57-67.
40. Koh, C. Y., and D. Yuan. 2000. The functional relevance of NK-cell-mediated upregulation of antigen-specific IgG2a responses. Cell. Immunol. 204: 135-142.
41. Bortnick, A., I. Chernova, W. J. Quinn, III, M. Mugnier, M. P. Cancro, and D. Allman. 2012. Long-lived bone marrow plasma cells are induced early in response to T cell-independent or T cell-dependent antigens. J. Immunol. 188: 5389-5396.
42. 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. (Pubitemid 32660436)
43. Calvi, L. M., G. B. Adams, K. W. Weibrecht, J. M. Weber, D. P. Olson, M. C. Knight, R. P. Martin, E. Schipani, P. Divieti, F. R. Bringhurst, et al. 2003. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425: 841-846. (Pubitemid 37351468)
44. Zhu, J., and S. G. Emerson. 2004. A new bone to pick: osteoblasts and the haematopoietic stem-cell niche. Bioessays 26: 595-599. (Pubitemid 38758335)
45. Sugiyama, T., H. Kohara, M. Noda, and T. Nagasawa. 2006. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25: 977-988. (Pubitemid 44894948)
46. Tokoyoda, K., T. Egawa, T. Sugiyama, B. I. Choi, and T. Nagasawa. 2004. Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 20: 707-718. (Pubitemid 38757441)
47. O'Connor, B. P., V. S. Raman, L. D. Erickson, W. J. Cook, L. K. Weaver, C. Ahonen, L. L. Lin, G. T. Mantchev, R. J. Bram, and R. J. Noelle. 2004. BCMA is essential for the survival of long-lived bone marrow plasma cells. J. Exp. Med. 199: 91-98.
48. Chu, V. T., A. Fröhlich, G. Steinhauser, T. Scheel, T. Roch, S. Fillatreau, J. J. Lee, M. Löhning, and C. Berek. 2011. Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat. Immunol. 12: 151-159.
49. Rodriguez Gomez, M., Y. Talke, N. Goebel, F. Hermann, B. Reich, and M. Mack. 2010. Basophils support the survival of plasma cells in mice. J. Immunol. 185: 7180-7185.
50. Winter, O., K. Moser, E. Mohr, D. Zotos, H. Kaminski, M. Szyska, K. Roth, D. M. Wong, C. Dame, D. M. Tarlinton, et al. 2010. Megakaryocytes constitute a functional component of a plasma cell niche in the bone marrow. Blood 116: 1867-1875.
51. 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.
52. DiLillo, D. J., Y. Hamaguchi, Y. Ueda, K. Yang, J. Uchida, K. M. Haas, G. Kelsoe, and T. F. Tedder. 2008. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J. Immunol. 180: 361-371.
53. Underhill, G. H., H. A. Minges Wols, J. L. Fornek, P. L. Witte, and G. S. Kansas. 2002. IgG plasma cells display a unique spectrum of leukocyte adhesion and homing molecules. Blood 99: 2905-2912. (Pubitemid 34525380)
54. Mahévas, M., P. Patin, F. Huetz, M. Descatoire, N. Cagnard, C. Bole-Feysot, S. Le Gallou, M. Khellaf, O. Fain, D. Boutboul, et al. 2013. B cell depletion in immune thrombocytopenia reveals splenic long-lived plasma cells. J. Clin. Invest. 123: 432-442.
55. 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. (Pubitemid 41002896)
56. Odendahl, M., H. Mei, B. F. Hoyer, A. M. Jacobi, A. Hansen, G. Muehlinghaus, C. Berek, F. Hiepe, R. Manz, A. Radbruch, and T. Dörner. 2005. Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response. Blood 105: 1614-1621. (Pubitemid 40223682)
57. Shapiro-Shelef, M., K. I. Lin, D. Savitsky, J. Liao, and K. Calame. 2005. Blimp-1 is required for maintenance of long-lived plasma cells in the bone marrow. J. Exp. Med. 202: 1471-1476. (Pubitemid 41746593)
58. Racine, R., M. McLaughlin, D. D. Jones, S. T. Wittmer, K. C. MacNamara, D. L. Woodland, and G. M. Winslow. 2011. IgM production by bone marrow plasmablasts contributes to long-term protection against intracellular bacterial infection. J. Immunol. 186: 1011-1021.
59. Xiang, Z., A. J. Cutler, R. J. Brownlie, K. Fairfax, K. E. Lawlor, E. Severinson, E. U. Walker, R. A. Manz, D. M. Tarlinton, and K. G. Smith. 2007. FcgRIIb controls bone marrow plasma cell persistence and apoptosis. Nat. Immunol. 8: 419-429. (Pubitemid 46745417)
60. Lentz, V. M., C. E. Hayes, and M. P. Cancro. 1998. Bcmd decreases the life span of B-2 but not B-1 cells in A/WySnJ mice. J. Immunol. 160: 3743-3747. (Pubitemid 28176076)
61. Hayakawa, K., and R. R. Hardy. 2000. Development and function of B-1 cells. Curr. Opin. Immunol. 12: 346-353.
62. Montecino-Rodriguez, E., H. Leathers, and K. Dorshkind. 2006. Identification of a B-1 B cell-specified progenitor. Nat. Immunol. 7: 293-301.
63. Taillardet, M., G. Haffar, P. Mondière, M. J. Asensio, T. Pléau-Pison, N. Burdin, T. Defrance, and L. Genestier. 2010. Toll-like receptor agonists allow generation of long-lasting antipneumococcal humoral immunity in response to a plain polysaccharidic vaccine. J. Infect. Dis. 202: 470-479.
64. Maruyama, M., K. P. Lam, and K. Rajewsky. 2000. Memory B-cell persistence is independent of persisting immunizing antigen. Nature 407: 636-642.
65. Benson, M. J., R. Elgueta, W. Schpero, M. Molloy, W. Zhang, E. Usherwood, and R. J. Noelle. 2009. Distinction of the memory B cell response to cognate antigen versus bystander inflammatory signals. J. Exp. Med. 206: 2013-2025.
66. 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.
67. Kaji, T., A. Ishige, M. Hikida, J. Taka, A. Hijikata, M. Kubo, T. Nagashima, Y. Takahashi, T. Kurosaki, M. Okada, et al. 2012. Distinct cellular pathways select germline-encoded and somatically mutated antibodies into immunological memory. J. Exp. Med. 209: 2079-2097.
68. Taylor, J. J., K. A. Pape, and M. K. Jenkins. 2012. A germinal center-independent pathway generates unswitched memory B cells early in the primary response. J. Exp. Med. 209: 597-606.
69. He, B., W. Xu, P. A. Santini, A. D. Polydorides, A. Chiu, J. Estrella, M. Shan, A. Chadburn, V. Villanacci, A. Plebani, et al. 2007. Intestinal bacteria trigger T cell-independent immunoglobulin A2 class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity 26: 812-826. (Pubitemid 46915505)
70. Bergqvist, P., A. Stensson, N. Y. Lycke, and M. Bemark. 2010. T cell-independent IgA class switch recombination is restricted to the GALT and occurs prior to manifest germinal center formation. J. Immunol. 184: 3545-3553.