Fishing for mammalian paradigms in the teleost immune system

Nature Immunology

Volumn 14, Issue 4, 2013, Pages 320-326

  Sunyer, J Oriol ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; IMMUNOGLOBULIN; IMMUNOGLOBULIN M;

ADAPTIVE IMMUNITY; AUTOIMMUNITY; B LYMPHOCYTE; CELL FUNCTION; CELL LINEAGE; CELL PROLIFERATION; CYTOKINE PRODUCTION; INNATE IMMUNITY; INTESTINE LYMPHATIC TISSUE; MAMMAL; MUCOSAL IMMUNITY; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; TELEOST;

EID: 84875460517     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2549     Document Type: Review

References (73)

1. Hoffmann, J. Antifungal defense in Drosophila. Nat. Immunol. 8, 543-545 (2007).
2. Kaufmann, S.H. Immunology's foundation: the 100-year anniversary of the Nobel Prize to Paul Ehrlich and Elie Metchnikoff. Nat. Immunol. 9, 705-712 (2008).
3. Magnadottir, B. Innate immunity of fish (overview). Fish Shellfish Immunol. 20, 137-151 (2006).
4. Magor, B.G. & Magor, K.E. Evolution of effectors and receptors of innate immunity. Dev. Comp. Immunol. 25, 651-682 (2001).
5. Flajnik, M.F. & Kasahara, M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 11, 47-59 (2010).
6. Zapata, A. & Amemiya, C.T. Phylogeny of lower vertebrates and their immunological structures. Curr. Top. Microbiol. Immunol. 248, 67-107 (2000).
7. Salinas, I., Zhang, Y.A. & Sunyer, J.O. Mucosal immunoglobulins and B cells of teleost fish. Dev. Comp. Immunol. 35, 1346-1365 (2011).
8. Vasta, G.R. et al. Structural and functional diversity of the lectin repertoire in teleost fish: relevance to innate and adaptive immunity. Dev. Comp. Immunol. 35,1388-1399 (2011).
9. Yoder, J.A. & Litman, G.W. The phylogenetic origins of natural killer receptors and recognition: relationships, possibilities, and realities. Immunogenetics 63, 123-141 (2011).
10. Sunyer, J.O., Zarkadis, I.K. & Lambris, J.D. Complement diversity: a mechanism for generating immune diversity? Immunol. Today 19, 519-523 (1998).
11. Danilova, N., Bussmann, J., Jekosch, K. & Steiner, L.A. The immunoglobulin heavy-chain locus in zebrafish: identification and expression of a previously unknown isotype, immunoglobulin Z. Nat. Immunol. 6, 295-302 (2005).
12. Hansen, J.D., Landis, E.D. & Phillips, R.B. Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: Implications for a distinctive B cell developmental pathway in teleost fish. Proc. Natl. Acad. Sci. USA 102, 6919-6924 (2005).
13. Sunyer, J.O. (ed.) Special issue on teleost fish immunology. Dev. Comp. Immunol 35, 1193-1400 (2011).
14. Neumann, N.F., Stafford, J.L., Barreda, D., Ainsworth, A.J. & Belosevic, M. Antimicrobial mechanisms of fish phagocytes and their role in host defense. Dev. Comp. Immunol. 25, 807-825 (2001).
15. Rabinovitch, M. Professional and non-professional phagocytes: an introduction. Trends Cell Biol. 5, 85-87 (1995).
16. Wu, Y. et al. Human gamma delta T cells: a lymphoid lineage cell capable of professional phagocytosis. J. Immunol. 183, 5622-5629 (2009).
17. Ochando, J.C. et al. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat. Immunol. 7, 652-662 (2006).
18. Li, J. et al. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat. Immunol. 7, 1116-1124 (2006).
19. Øverland, H.S., Pettersen, E.F., Ronneseth, A. & Wergeland, H.I. Phagocytosis by B-cells and neutrophils in Atlantic salmon (Salmo salar L.) and Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol. 28, 193-204 (2009).
20. Zimmerman, L.M., Vogel, L.A., Edwards, K.A. & Bowden, R.M. Phagocytic B cells in a reptile. Biol. Lett. 6, 270-273 (2010).
21. Parra, D. et al. Pivotal Advance: Peritoneal cavity B-1 B cells have phagocytic and microbicidal capacities and present phagocytosed antigen to CD4+ T cells.J. Leukoc. Biol. 91, 525-536 (2012).
22. Gao, X.M. et al. A novel function of murine B1 cells: Active phagocytic and microbicidal abilities. Eur. J. Immunol 42, 982-992 (2012).
23. Nakashima, M. et al. Pivotal Advance: characterization of mouse liver phagocytic B cells in innate immunity. J. Leukoc. Biol. 91, 537-546 (2012).
24. Herzenberg, L.A., Kantor, A.B. & Herzenberg, L.A. Layered evolution in the immune system. A model for the ontogeny and development of multiple lymphocyte lineages. Ann. NY Acad. Sci. 651, 1-9 (1992).
25. Casali, P. & Schettino, E.W. Structure and function of natural antibodies. Curr. Top. Microbiol. Immunol. 210, 167-179 (1996).
26. Zhou, Z.H. et al. The broad antibacterial activity of the natural antibody repertoire is due to polyreactive antibodies. Cell Host Microbe 1, 51-61 (2007).
27. Murakami, M. et al. Oral administration of lipopolysaccharides activates B-1 cells in the peritoneal cavity and lamina propria of the gut and induces autoimmune symptoms in an autoantibody transgenic mouse. J. Exp. Med. 180, 111-121 (1994).
28. Ha, S.A. et al. Regulation of B1 cell migration by signals through Toll-like receptors. J. Exp. Med. 203, 2541-2550 (2006).
29. Viau, M. & Zouali, M. B-lymphocytes, innate immunity, and autoimmunity. Clin. Immunol. 114, 17-26 (2005).
30. Fritz, J.H. et al. Acquisition of a multifunctional IgA+ plasma cell phenotype in the gut. Nature 481, 199-203 (2012).
31. Itakura, A. et al. An hour after immunization peritoneal B-1 cells are activated to migrate to lymphoid organs where within 1 day they produce IgM antibodies that initiate elicitation of contact sensitivity. J. Immunol. 175, 7170-7178 (2005).
32. Rodriguez-Manzanet, R. et al. T and B cell hyperactivity and autoimmunity associated with niche-specific defects in apoptotic body clearance in TIM-4-deficient mice. Proc. Natl. Acad. Sci. USA 107, 8706-8711 (2010).
33. Boes, M. et al. Accelerated development of IgG autoantibodies and autoimmune disease in the absence of secreted IgM. Proc. Natl. Acad. Sci. USA 97, 1184-1189 (2000).
34. Ehrenstein, M.R. & Notley, C.A. The importance of natural IgM: scavenger, protector and regulator. Nat. Rev. Immunol. 10, 778-786 (2010).
35. Chen, Y., Park, Y.B., Patel, E. & Silverman, G.J. IgM antibodies to apoptosis-associated determinants recruit C1q and enhance dendritic cell phagocytosis of apoptotic cells. J. Immunol. 182, 6031-6043 (2009).
36. Steinman, R.M., Turley, S., Mellman, I. & Inaba, K. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191, 411-416 (2000).
37. Hayakawa, K. et al. Positive selection of natural autoreactive B cells. Science 285, 113-116 (1999).
38. Henson, P.M. Dampening inflammation. Nat. Immunol. 6, 1179-1181 (2005).
39. Lund, F.E. & Randall, T.D. Effector and regulatory B cells: modulators of CD4+ T cell immunity. Nat. Rev. Immunol. 10, 236-247 (2010).
40. Barr, T.A., Brown, S., Ryan, G., Zhao, J. & Gray, D. TLR-mediated stimulation of APC: distinct cytokine responses of B cells and dendritic cells. Eur. J. Immunol. 37, 3040-3053 (2007).
41. Mizoguchi, A. & Bhan, A.K. A case for regulatory B cells. J. Immunol. 176,705-710 (2006).
42. Hoehlig, K. et al. Immune regulation by B cells and antibodies a view towards the clinic. Adv. Immunol. 98, 1-38 (2008).
43. Morris, D.L. & Rothstein, T.L. Abnormal transcription factor induction through the surface immunoglobulin M receptor of B-1 lymphocytes. J. Exp. Med. 177,857-861 (1993).
44. Haas, K.M., Poe, J.C., Steeber, D.A. & Tedder, T.F. 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 (2005).
45. Gil-Cruz, C. et al. The porin OmpD from nontyphoidal Salmonella is a key target for a protective B1b cell antibody response. Proc. Natl. Acad. Sci. USA 106, 9803-9808 (2009).
46. Baumgarth, N. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 11, 34-46 (2011).
47. Hastings, W.D., Tumang, J.R., Behrens, T.W. & Rothstein, T.L. Peritoneal B-2 cells comprise a distinct B-2 cell population with B-1b-like characteristics. Eur. J. Immunol. 36, 1114-1123 (2006).
48. Griffin, D.O., Holodick, N.E. & Rothstein, T.L. Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+ CD27+ CD43+ CD70. J. Exp. Med. 208, 67-80 (2011).
49. Zhang, Y.A. et al. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 11, 827-835 (2010).
50. Macpherson, A.J. et al. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288, 2222-2226 (2000).
51. Suzuki, K., Ha, S.A., Tsuji, M. & Fagarasan, S. Intestinal IgA synthesis: a primitive form of adaptive immunity that regulates microbial communities in the gut. Semin. Immunol. 19, 127-135 (2007).
52. Cerutti, A., Chen, K. & Chorny, A. Immunoglobulin responses at the mucosal interface. Annu. Rev. Immunol. 29, 273-293 (2011).
53. Kang, H.S. et al. Signaling via LTbetaR on the lamina propria stromal cells of the gut is required for IgA production. Nat. Immunol. 3, 576-582 (2002).
54. Macpherson, A.J., McCoy, K.D., Johansen, F.E. & Brandtzaeg, P. The immune geography of IgA induction and function. Mucosal Immunol. 1, 11-22 (2008).
55. Rawls, J.F., Samuel, B.S. & Gordon, J.I. Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc. Natl. Acad. Sci. USA 101,4596-4601 (2004).
56. Kanther, M. & Rawls, J.F. Host-microbe interactions in the developing zebrafish. Curr. Opin. Immunol. 22, 10-19 (2010).
57. Boehm, T. Design principles of adaptive immune systems. Nat. Rev. Immunol. 11, 307-317 (2011).
58. Litman, G.W. & Cooper, M.D. Why study the evolution of immunity? Nat. Immunol. 8, 547-548 (2007).
59. Warr, G.W. The adaptive immune system of fish. Dev. Biol. Stand. 90, 15-21 (1997).
60. Solem, S.T. & Stenvik, J. Antibody repertoire development in teleosts-a review with emphasis on salmonids and Gadus morhua L. Dev. Comp. Immunol. 30, 57-76 (2006).
61. Cain, K.D., Jones, D.R. & Raison, R.L. Antibody-antigen kinetics following immunization of rainbow trout (Oncorhynchus mykiss) with a T-cell dependent antigen. Dev. Comp. Immunol. 26, 181-190 (2002).
62. Cain, K.D., Jones, D.R. & Raison, R.L. Characterisation of mucosal and systemic immune responses in rainbow trout (Oncorhynchus mykiss) using surface plasmon resonance. Fish Shellfish Immunol. 10, 651-666 (2000).
63. Maki, J.L. & Dickerson, H.W. Systemic and cutaneous mucus antibody responses of channel catfish immunized against the protozoan parasite Ichthyophthirius multifiliis. Clin. Diagn. Lab. Immunol. 10, 876-881 (2003).
64. Kaattari, S., Evans, D. & Klemer, J. Varied redox forms of teleost IgM: an alternative to isotypic diversity? Immunol. Rev. 166, 133-142 (1998).
65. Ye, J., Kaattari, I. & Kaattari, S. Plasmablasts and plasma cells: reconsidering teleost immune system organization. Dev. Comp. Immunol. 35, 1273-1281 (2011).
66. Kaattari, S.L., Zhang, H.L., Khor, I.W., Kaattari, I.M. & Shapiro, D.A. Affinity maturation in trout: clonal dominance of high affinity antibodies late in the immune response. Dev. Comp. Immunol. 26, 191-200 (2002).
67. Edholm, E.S., Bengten, E. & Wilson, M. Insights into the function of IgD.Dev. Comp. Immunol. 35, 1309-1316 (2011).
68. Ramirez-Gomez, F. et al. Discovery and characterization of secretory IgD in rainbow trout: secretory IgD is produced through a novel splicing mechanism. J. Immunol. 188, 1341-1349 (2012).
69. Edholm, E.S. et al. Identification of two IgD+ B cell populations in channel catfish, Ictalurus punctatus. J. Immunol. 185, 4082-4094 (2010).
70. Chen, K. et al. Immunoglobulin D enhances immune surveillance by activating antimicrobial, proinflammatory and B cell-stimulating programs in basophils.Nat. Immunol. 10, 889-898 (2009).
71. Ye, J., Bromage, E.S. & Kaattari, S.L. The strength of B cell interaction with antigen determines the degree of IgM polymerization. J. Immunol. 184, 844-850 (2010).
72. Saunders, H.L., Oko, A.L., Scott, A.N., Fan, C.W. & Magor, B.G. The cellular context of AID expressing cells in fish lymphoid tissues. Dev. Comp. Immunol. 34, 669-676 (2010).
73. Cannon, J.P. et al. A bony fish immunological receptor of the NITR multigene family mediates allogeneic recognition. Immunity 29, 228-237 (2008).