Channel catfish soluble FcμR binds conserved linear epitopes present on Cμ3 and Cμ4

Molecular Immunology

Volumn 47, Issue 6, 2010, Pages 1306-1316

  Nayak, Deepak K ^a   Tang, Aihua ^a   Wilson, Melanie ^a   Miller, Norman W ^a   Bengtén, Eva ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

Channel catfish; Comparative immunology; IgM; Soluble FcR

Indexed keywords

CYSTEINE; EPITOPE; FC RECEPTOR; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN KAPPA CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; IMMUNOGLOBULIN M; IMMUNOGLOBULIN MU CHAIN;

ARTICLE; BINDING SITE; CATFISH; CHICKEN; CONTROLLED STUDY; DISULFIDE BOND; GOAT; MOLECULAR MODEL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; RABBIT; RAINBOW TROUT;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; EPITOPES; ICTALURIDAE; IMMUNOGLOBULIN CONSTANT REGIONS; IMMUNOGLOBULIN M; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, FC; SOLUBILITY; SPECIES SPECIFICITY; STRUCTURAL HOMOLOGY, PROTEIN;

CAPRA HIRCUS; ICTALURUS PUNCTATUS; ONCORHYNCHUS MYKISS; ORYCTOLAGUS CUNICULUS; VERTEBRATA;

EID: 76949088950     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2009.11.026     Document Type: Article

References (77)

1. Armant M., Rubio M., Delespesse G., and Sarfati M. Soluble CD23 directly activates monocytes to contribute to the antigen-independent stimulation of resting T cells. J. Immunol. 155 (1995) 4868-4875
2. Astier A., de la Salle H., de la Salle C., Bieber T., Esposito-Farese M.E., Freund M., Cazenave J.P., Fridman W.H., Teillaud J.L., and Hanau D. Human epidermal Langerhans cells secrete a soluble receptor for IgG (Fc gamma RII/CD32) that inhibits the binding of immune complexes to Fc gamma R+ cells. J. Immunol. 152 (1994) 201-212
3. Bengten E., Clem L.W., Miller N.W., Warr G.W., and Wilson M. Channel catfish immunoglobulins: repertoire and expression. Dev. Comp. Immunol. 30 (2006) 77-92
4. Bengten E., Quiniou S., Hikima J., Waldbieser G., Warr G.W., Miller N.W., and Wilson M. Structure of the catfish IGH locus: analysis of the region including the single functional IGHM gene. Immunogenetics 58 (2006) 831-844
5. Bengten E., Quiniou S.M., Stuge T.B., Katagiri T., Miller N.W., Clem L.W., Warr G.W., and Wilson M. The IgH locus of the channel catfish. Ictalurus punctatus, contains multiple constant region gene sequences: different genes encode heavy chains of membrane and secreted IgD. J. Immunol. 169 (2002) 2488-2497
6. Bengten E., Wilson M., Miller N., Clem L.W., Pilstrom L., and Warr G.W. Immunoglobulin isotypes: structure, function, and genetics. Curr. Top. Microbiol. Immunol. 248 (2000) 189-219
7. Canfield S.M., and Morrison S.L. The binding affinity of human IgG for its high affinity Fc receptor is determined by multiple amino acids in the CH2 domain and is modulated by the hinge region. J. Exp. Med. 173 (1991) 1483-1491
8. Clem L.W., and Small Jr. P.A. Phylogeny of immunoglobulin structure and function. I. Immunoglobulins of the lemon shark. J. Exp. Med. 125 (1967) 893-920
9. Coosemans V., and Hadji-Azimi I. Immunoglobulin Fc receptor molecules on Xenopus laevis splenocytes. Immunology 65 (1988) 641-645
10. Daeron M. Fc receptor biology. Annu. Rev. Immunol. 15 (1997) 203-234
11. Daeron M., and Lesourne R. Negative signaling in Fc receptor complexes. Adv. Immunol. 89 (2006) 39-86
12. Delespesse G., Sarfati M., Wu C.Y., Fournier S., and Letellier M. The low-affinity receptor for IgE. Immunol. Rev. 125 (1992) 77-97
13. DeLuca D., Wilson M., and Warr G.W. Lymphocyte heterogeneity in the trout, Salmo gairdneri, defined with monoclonal antibodies to IgM. Eur. J. Immunol. 13 (1983) 546-551
14. Edholm E.S., Wilson M., Sahoo M., Miller N.W., Pilstrom L., Wermenstam N.E., and Bengten E. Identification of Igsigma and Iglambda in channel catfish, Ictalurus punctatus, and Iglambda in Atlantic cod, Gadus morhua. Immunogenetics 61 (2009) 353-370
15. Edmundson A.B., Ely K.R., Abola E.E., Schiffer M., and Panagiotopoulos N. Rotational allomerism and divergent evolution of domains in immunoglobulin light chains. Biochemistry 14 (1975) 3953-3961
16. Fernandez-Botran R. Soluble cytokine receptors: their role in immunoregulation. FASEB J. 5 (1991) 2567-2574
17. Fleit H.B., Kobasiuk C.D., Daly C., Furie R., Levy P.C., and Webster R.O. A soluble form of Fc gamma RIII is present in human serum and other body fluids and is elevated at sites of inflammation. Blood 79 (1992) 2721-2728
18. Fridman W.H., Bonnerot C., Daeron M., Amigorena S., Teillaud J.L., and Sautes C. Structural bases of Fc gamma receptor functions. Immunol. Rev. 125 (1992) 49-76
19. Fridman W.H., Teillaud J.L., Bouchard C., Teillaud C., Astier A., Tartour E., Galon J., Mathiot C., and Sautes C. Soluble Fc gamma receptors. J. Leukoc. Biol. 54 (1993) 504-512
20. Gachet C., Astier A., de la Salle H., de la Salle C., Fridman W.H., Cazenave J.P., Hanau D., and Teillaud J.L. Release of Fc gamma RIIa2 by activated platelets and inhibition of anti-CD9-mediated platelet aggregation by recombinant Fc gamma RIIa2. Blood 85 (1995) 698-704
21. Garcia-Garcia E., and Rosales C. Signal transduction during Fc receptor-mediated phagocytosis. J. Leukoc. Biol. 72 (2002) 1092-1108
22. Garman S.C., Wurzburg B.A., Tarchevskaya S.S., Kinet J.P., and Jardetzky T.S. Structure of the Fc fragment of human IgE bound to its high-affinity receptor Fc epsilonRI alpha. Nature 406 (2000) 259-266
23. Ghumra A., Shi J., McIntosh R.S., Rasmussen I.B., Braathen R., Johansen F.E., Sandlie I., Mongini P.K., Areschoug T., Lindahl G., Lewis M.J., Woof J.M., and Pleass R.J. Structural requirements for the interaction of human IgM and IgA with the human Fcalpha/mu receptor. Eur. J. Immunol. 39 (2009) 1147-1156
24. Goldsmith E.B., Erickson B.W., and Thompson N.L. Synthetic peptides from mouse Fc receptor (MoFc gamma RII) that alter the binding of IgG to MoFc gamma RII. Biochemistry 36 (1997) 952-959
25. Gould H.J., Sutton B.J., Beavil A.J., Beavil R.L., McCloskey N., Coker H.A., Fear D., and Smurthwaite L. The biology of IGE and the basis of allergic disease. Annu. Rev. Immunol. 21 (2003) 579-628
26. Hamuro K., Suetake H., Saha N.R., Kikuchi K., and Suzuki Y. A teleost polymeric Ig receptor exhibiting two Ig-like domains transports tetrameric IgM into the skin. J. Immunol. 178 (2007) 5682-5689
27. Haynes L., Fuller L., and McKinney E.C. Fc receptor for shark IgM. Dev. Comp. Immunol. 12 (1988) 561-571
28. Herr A.B., Ballister E.R., and Bjorkman P.J. Insights into IgA-mediated immune responses from the crystal structures of human FcalphaRI and its complex with IgA1-Fc. Nature 423 (2003) 614-620
29. Huizinga T.W., de Haas M., van Oers M.H., Kleijer M., Vile H., van der Wouw P.A., Moulijn A., van Weezel H., Roos D., and von dem Borne A.E. The plasma concentration of soluble Fc-gamma RIII is related to production of neutrophils. Br. J. Haematol. 87 (1994) 459-463
30. Huizinga T.W., van der Schoot C.E., Jost C., Klaassen R., Kleijer M., von dem Borne A.E., Roos D., and Tetteroo P.A. The PI-linked receptor FcRIII is released on stimulation of neutrophils. Nature 333 (1988) 667-669
31. Kato K., Sautes-Fridman C., Yamada W., Kobayashi K., Uchiyama S., Kim H., Enokizono J., Galinha A., Kobayashi Y., Fridman W.H., Arata Y., and Shimada I. Structural basis of the interaction between IgG and Fcgamma receptors. J. Mol. Biol. 295 (2000) 213-224
32. Kelley L.A., and Sternberg M.J. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4 (2009) 363-371
33. Kinet J.P., and Launay P. Fc alpha/microR: single member or first born in the family?. Nat. Immunol. 1 (2000) 371-372
34. Kristoffersen E.K., Matre R., Ulvestad E., and Vedeler C.A. A dot-immunobinding assay for the demonstration of soluble Fc gamma receptors. J. Immunol. Methods 167 (1994) 15-19
35. Lanier L.L., Phillips J.H., and Testi R. Membrane anchoring and spontaneous release of CD16 (FcR III) by natural killer cells and granulocytes. Eur. J. Immunol. 19 (1989) 775-778
36. Launay P., Grossetete B., Arcos-Fajardo M., Gaudin E., Torres S.P., Beaudoin L., Patey-Mariaud de Serre N., Lehuen A., and Monteiro R.C. Fcalpha receptor (CD89) mediates the development of immunoglobulin A (IgA) nephropathy (Berger's disease). Evidence for pathogenic soluble receptor-Iga complexes in patients and CD89 transgenic mice. J. Exp. Med. 191 (2000) 1999-2009
37. Letellier M., Sarfati M., and Delespesse G. Mechanisms of formation of IgE-binding factors (soluble CD23). I. Fc epsilon R II bearing B cells generate IgE-binding factors of different molecular weights. Mol. Immunol. 26 (1989) 1105-1112
38. Lobb C.J. Covalent structure and affinity of channel catfish anti-dinitrophenyl antibodies. Mol. Immunol. 22 (1985) 993-999
39. Lobb C.J., and Olson M.O. Immunoglobulin heavy H chain isotypes in a teleost fish. J. Immunol. 141 (1988) 1236-1245
40. Lobb C.J., Olson M.O., and Clem L.W. Immunoglobulin light chain classes in a teleost fish. J. Immunol. 132 (1984) 1917-1923
41. Lubeck M.D., Steplewski Z., Baglia F., Klein M.H., Dorrington K.J., and Koprowski H. The interaction of murine IgG subclass proteins with human monocyte Fc receptors. J. Immunol. 135 (1985) 1299-1304
42. McCloskey N., Hunt J., Beavil R.L., Jutton M.R., Grundy G.J., Girardi E., Fabiane S.M., Fear D.J., Conrad D.H., Sutton B.J., and Gould H.J. Soluble CD23 monomers inhibit and oligomers stimulate IGE synthesis in human B cells. J. Biol. Chem. 282 (2007) 24083-24091
43. Middelhoven P.J., Van Buul J.D., Hordijk P.L., and Roos D. Different proteolytic mechanisms involved in Fc gamma RIIIb shedding from human neutrophils. Clin. Exp. Immunol. 125 (2001) 169-175
44. Miller N., Wilson M., Bengten E., Stuge T., Warr G., and Clem W. Functional and molecular characterization of teleost leukocytes. Immunol. Rev. 166 (1998) 187-197
45. Miller N.W., Rycyzyn M.A., Wilson M.R., Warr G.W., Naftel J.P., and Clem L.W. Development and characterization of channel catfish long term B cell lines. J. Immunol. 152 (1994) 2180-2189
46. Nimmerjahn F., and Ravetch J.V. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310 (2005) 1510-1512
47. Nimmerjahn F., and Ravetch J.V. Fcgamma receptors: old friends and new family members. Immunity 24 (2006) 19-28
48. O'Dowd A.M., Ellis A.E., and Secombes C.J. Binding of immune complexes to Atlantic salmon peripheral blood leucocytes. Dev. Comp. Immunol. 22 (1998) 439-448
49. Pleass R.J., Dunlop J.I., Anderson C.M., and Woof J.M. Identification of residues in the CH2/CH3 domain interface of IgA essential for interaction with the human fcalpha receptor (FcalphaR) CD89. J. Biol. Chem. 274 (1999) 23508-23514
50. Potapov V., Sobolev V., Edelman M., Kister A., and Gelfand I. Protein-protein recognition: juxtaposition of domain and interface cores in immunoglobulins and other sandwich-like proteins. J. Mol. Biol. 342 (2004) 665-679
51. Purzel J., Schmitt R., Viertlboeck B.C., and Gobel T.W. Chicken IgY binds its receptor at the CH3/CH4 interface similarly as the human IgA: Fc(alpha)RI interaction. J. Immunol. 183 (2009) 4554-4559
52. Radaev S., and Sun P. Recognition of immunoglobulins by Fcgamma receptors. Mol. Immunol. 38 (2001) 1073-1083
53. Radaev S., and Sun P.D. Recognition of IgG by Fcgamma receptor. The role of Fc glycosylation and the binding of peptide inhibitors. J. Biol. Chem. 276 (2001) 16478-16483
54. Ravetch J.V., and Kinet J.P. Fc receptors. Annu. Rev. Immunol. 9 (1991) 457-492
55. Rombout J.H., van der Tuin S.J., Yang G., Schopman N., Mroczek A., Hermsen T., and Taverne-Thiele J.J. Expression of the polymeric immunoglobulin receptor (pIgR) in mucosal tissues of common carp (Cyprinus carpio L.). Fish Shellfish Immunol. 24 (2008) 620-628
56. Sambrook J., and Russell D.W. Molecular Cloning: A Laboratory Manual. 3rd edition vol. 1 (2001), Cold Spring Harbor Laboratory Press, New York
57. Sarfati M., Chevret S., Chastang C., Biron G., Stryckmans P., Delespesse G., Binet J.L., Merle-Beral H., and Bron D. Prognostic importance of serum soluble CD23 level in chronic lymphocytic leukemia. Blood 88 (1996) 4259-4264
58. Sautes C., Mazieres N., Galinha A., Tartour E., Bonnerot C., Amigorena S., Teillaud C., Spagnoli R., and Fridman W.H. Murine soluble Fc gamma receptors/IgG-binding factors (IgG-BF): analysis of the relation to Fc gamma RII and production of milligram quantities of biologically active recombinant IgG-BF. Immunol. Res. 11 (1992) 181-190
59. Sautes C., Varin N., Teillaud C., Daeron M., Even J., Hogarth P.M., and Fridman W.H. Soluble Fc gamma receptors II (Fc gamma RII) are generated by cleavage of membrane Fc gamma RII. Eur. J. Immunol. 21 (1991) 231-234
60. Sekizawa A., Fujii T., and Tochinai S. Membrane receptors on Xenopus macrophages for two classes of immunoglobulins (IgM and IgY) and the third complement component (C3). J. Immunol. 133 (1984) 1431-1435
61. Shen L., Stuge T.B., Bengten E., Wilson M., Chinchar V.G., Naftel J.P., Bernanke J.M., Clem L.W., and Miller N.W. Identification and characterization of clonal NK-like cells from channel catfish (Ictalurus punctatus). Dev. Comp. Immunol. 28 (2004) 139-152
62. Shen L., Stuge T.B., Evenhuis J.P., Bengten E., Wilson M., Chinchar V.G., Clem L.W., and Miller N.W. Channel catfish NK-like cells are armed with IgM via a putative FcmicroR. Dev. Comp. Immunol. 27 (2003) 699-714
63. Silva E.F., Medeiros M.A., McBride A.J., Matsunaga J., Esteves G.S., Ramos J.G., Santos C.S., Croda J., Homma A., Dellagostin O.A., Haake D.A., Reis M.G., and Ko A.I. The terminal portion of leptospiral immunoglobulin-like protein LigA confers protective immunity against lethal infection in the hamster model of leptospirosis. Vaccine 25 (2007) 6277-6286
64. Sizemore R.C., Miller N.W., Cuchens M.A., Lobb C.J., and Clem L.W. Phylogeny of lymphocyte heterogeneity: the cellular requirements for in vitro mitogenic responses of channel catfish leukocytes. J. Immunol. 133 (1984) 2920-2924
65. Sondermann P., Huber R., Oosthuizen V., and Jacob U. The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gammaRIII complex. Nature 406 (2000) 267-273
66. Stafford J.L., Wilson M., Nayak D., Quiniou S.M., Clem L.W., Miller N.W., and Bengten E. Identification and characterization of a FcR homolog in an ectothermic vertebrate, the channel catfish (Ictalurus punctatus). J. Immunol. 177 (2006) 2505-2517
67. Taylor A.I., Sutton B.J., and Calvert R.A. Mutations in an avian IgY-Fc fragment reveal the locations of monocyte Fc receptor binding sites. Dev. Comp. Immunol. 34 (2010) 97-101
68. Teillaud C., Fridman W.H., and Sautes C. Demonstration of soluble IgG-Fc type II receptors (or s-Fc-gamma-II-R) in human whole saliva. J. Biol. Buccale 20 (1992) 3-10
69. Tosi M.F., and Zakem H. Surface expression of Fc gamma receptor III (CD16) on chemoattractant-stimulated neutrophils is determined by both surface shedding and translocation from intracellular storage compartments. J. Clin. Invest. 90 (1992) 462-470
70. van der Boog P.J., van Zandbergen G., de Fijter J.W., Klar-Mohamad N., van Seggelen A., Brandtzaeg P., Daha M.R., and van Kooten C. Fc alpha RI/CD89 circulates in human serum covalently linked to IgA in a polymeric state. J. Immunol. 168 (2002) 1252-1258
71. van Ginkel F.W., Miller N.W., Lobb C.J., and Clem L.W. Characterization of anti-hapten antibodies generated in vitro by channel catfish peripheral blood lymphocytes. Dev. Comp. Immunol. 16 (1992) 139-151
72. van Zandbergen G., Westerhuis R., Mohamad N.K., van De Winkel J.G., Daha M.R., and van Kooten C. Crosslinking of the human Fc receptor for IgA (FcalphaRI/CD89) triggers FcR gamma-chain-dependent shedding of soluble CD89. J. Immunol. 163 (1999) 5806-5812
73. Wilson M., Bengten E., Miller N.W., Clem L.W., Du Pasquier L., and Warr G.W. A novel chimeric Ig heavy chain from a teleost fish shares similarities to IgD. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 4593-4597
74. Wilson M.R., Marcuz A., van Ginkel F., Miller N.W., Clem L.W., Middleton D., and Warr G.W. The immunoglobulin M heavy chain constant region gene of the channel catfish, Ictalurus punctatus: an unusual mRNA splice pattern produces the membrane form of the molecule. Nucleic Acids Res. 18 (1990) 5227-5233
75. Wines B.D., Powell M.S., Parren P.W., Barnes N., and Hogarth P.M. The IgG Fc contains distinct Fc receptor (FcR) binding sites: the leukocyte receptors Fc gamma RI and Fc gamma RIIa bind to a region in the Fc distinct from that recognized by neonatal FcR and protein A. J. Immunol. 164 (2000) 5313-5318
76. Yodoi J., Adachi M., and Noro N. IgA binding factors and Fc receptors for IgA: comparative studies between IgA and IgE Fc receptor systems. Int. Rev. Immunol. 2 (1987) 117-141
77. Zhang G., Guo J., Zhou J., Wang X., Li Q., Yang Y., Shen H., Zhao D., Zhang H., Xi J., Wang L., Qiao S., and Jin X. Identification of the linear epitope for Fc-binding on the bovine IgG2 Fc receptor (boFcgamma2R) using synthetic peptides. FEBS Lett. 580 (2006) 1383-1390