Cloning of IgE from the echidna (Tachyglossus aculeatus) and a comparative analysis of ε chains from all three extant mammalian lineages

Developmental and Comparative Immunology

Volumn 28, Issue 1, 2004, Pages 61-75

  Vernersson, Molly ^a,b   Aveskogh, Maria ^a,b   Hellman, Lars ^a,b  

^a UPPSALA UNIVERSITY   (Sweden)

^b Resistentia Pharmaceuticals AB   (Sweden)

Author keywords

Evolution; Fc RI interaction; IgE; Immunoglobulins; Mammals; Monotreme; N glycosylation; chain

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M;

ALGORITHM; ANIMAL CELL; ARTICLE; BINDING SITE; COMPARATIVE STUDY; CONTROLLED STUDY; DNA ISOLATION; ECHIDNA; EVOLUTION; GLYCOSYLATION; HYPOTHESIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; UNINDEXED SEQUENCE;

EUTHERIA; MAMMALIA; METATHERIA; MONOTREMATA; TACHYGLOSSUS ACULEATUS; THERIA;

EID: 0041328963     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0145-305X(03)00084-3     Document Type: Article

References (70)

1. Ishizaka K., Ishizaka T. Identification of gamma-E-antibodies as a carrier of reaginic activity. J Immunol. 99:1967;1187-1198.
2. Johansson S.G., Bennich H., Wide L. A new class of immunoglobulin in human serum. Immunology. 14:1968;265-272.
3. Bennich H.H., Ishizaka K., Johansson S.G., Rowe D.S., Stanworth D.R., Terry W.D. Immunoglobulin E. A new class of human immunoglobulin. Immunochemistry. 5:1968;327-328.
4. Capra J.D., Frazer J.K. Immunoglobulins: structure and funktion. Paul W.E. Fundamental Immunology. 4th ed. 1999;60 Lippincott-Raven Publishers, Philadelphia.
5. Sutton B.J., Gould H.J. The human IgE network. Nature. 366:1993;421-428.
6. Bonnefoy J.Y., Aubry J.P., Gauchat J.F., Graber P., Life P., Flores R.L., Mazzei G. Receptors for IgE. Curr Opin Immunol. 5:1993;944-949.
7. Mudde G.C., Bheekha R., Bruijnzeel K.C. Consequences of IgE/ CD23-mediated antigen presentation in allergy. Immunol Today. 16:1995;380-383.
8. Kinet J.P. The high-affinity IgE receptor (Fc epsilon RI): from physiology to pathology. Annu Rev Immunol. 17:1999;931-972.
9. Hagan P., Blumenthal U.J., Dunn D., Simpson A.J.G., Wilkins H.A. Human IgE, IgG4 and resistance to infection with Schistosoma haematobium. Nature. 349:1991;243-245.
10. Rihet P., Demeure C.E., Bourgois A., Prata A., Dessein A.J. Evidence for an association between human resistance to Schistosoma mansoni and high anti-larval IgE levels. Eur J Immunol. 21:1991;2679-2686.
11. Dunne D.W., Butterworth A.E., Fulford A.J.C., Kariuki H.C., Langley J.G., Ouma J.H., Capron A., Pierce R.J., Sturrock R.F. Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to infection. Eur J Immunol. 22:1992;1483-1494.
12. King C.L., Xianli J., Malhotra I., Liu S., Mahmoud A.A., Oettgen H.C. Mice with a targeted deletion of the IgE gene have increased worm burdens and reduced granulomatous inflammation following primary infection with Schistosoma mansoni. J Immunol. 158:1997;294-300.
13. Jankovic D., Kullberg M.C., Dombrowicz D., Barbieri S., Caspar P., Wynn T.A., Paul W.E., Cheever A.W., Kinet J.P., Sher A. Fc epsilonRI-deficient mice infected with Schistosoma mansoni mount normal Th2-type responses while displaying enhanced liver pathology. J Immunol. 159:1997;1868-1875.
14. Garman S.C., Wurzburg B.A., Tarchevskaya S.S., Kinet J.P., 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.
15. Warr G.W., Magor K.E., Higgins D.A. IgY: clues to the origins of modern antibodies. Immunol Today. 16:1995;392-398.
16. Mussmann R., Wilson M., Marcuz A., Courtet M., Du Pasquier L. Membrane exon sequences of the three Xenopus Ig classes explain the evolutionary origin of mammalian isotypes. Eur J Immunol. 26:1996;409-414.
17. Diener E., Ealey E.H. Immune system in a monotreme: studies on the Australian echidna (Tachyglossus aculeatus). Nature. 208:1965;950-953.
18. Connolly J.H., Canfield P.J., McClure S.J., Whittington R.J. Histological and immunohistological investigation of lymphoid tissue in the platypus (Ornithorhynchus anatinus). J Anat. 195:1999;161-171.
19. Atwell J.L., Marchalonis J.J., Ealey E.H. Major immunoglobulin classes of the Echidna (Tachyglossus aculeatus). Immunology. 25:1973;835-846.
20. Belov K., Hellman L., Cooper D.W. Characterization of immunoglobulin gamma 1 from a monotreme, Tachyglossus aculeatus. Immunogenetics. 53:2002;1065-1071.
21. Belov K., Hellman L., Cooper D.W. Characterisation of echidna IgM provides insights into the time of divergence of extant mammals. Dev Comp Immunol. 26:2002;831-839.
22. Vernersson M., Aveskogh M., Munday B., Hellman L. Evidence for an early appearance of modern post-switch immunoglobulin isotypes in mammalian evolution (II), cloning of IgE, IgG1 and IgG2 from a monotreme, the duck-billed platypus, Ornithorhynchus anatinus. Eur J Immunol. 32:2002;2145-2155.
23. Janke A., Gemmell N.J., Feldmaier-Fuchs G., von Haeseler A., Paabo S. The mitochondrial genome of a monotreme - the platypus (Ornithorhynchus anatinus). J Mol Evol. 42:1996;153-159.
24. Janke A., Xu X., Arnason U. The complete mitochondrial genome of the wallaroo (Macropus robustus) and the phylogenetic relationship among Monotremata, Marsupialia, and Eutheria. Proc Natl Acad Sci USA. 94:1997;1276-1281.
25. Penny D., Hasegawa M. Molecular systematics. The platypus put in its place. Nature. 387:1997;549-550.
26. Kirsch J.A., Mayer G.C. The platypus is not a rodent: DNA hybridization, amniote phylogeny and the palimpsest theory. Philos Trans R Soc Lond B Biol Sci. 353:1998;1221-1237.
27. Hu Y., Wang Y., Luo Z., Li C. A new symmetrodont mammal from China and its implications for mammalian evolution. Nature. 390:1997;137-142.
28. Luo Z.X., Cifelli R.L., Kielan-Jaworowska Z. Dual origin of tribosphenic mammals. Nature. 409:2001;53-57.
29. Retief J.D., Winkfein R.J., Dixon G.H. Evolution of the monotremes. The sequences of the protamine P1 genes of platypus and echidna. Eur J Biochem. 218:1993;457-461.
30. Kullander K., Carlson B., Hallbook F. Molecular phylogeny and evolution of the neurotrophins from monotremes and marsupials. J Mol Evol. 45:1997;311-321.
31. Messer M., Weiss A.S., Shaw D.C., Westerman M. Evolution of the monotreme: phylogenetic relationship to marsupials and eutherians, and estimation of divergence dates based on α-lactalbumin amino acid sequences. J Mamm Evol. 5:1998;95-105.
32. Lee M.H., Shroff R., Cooper S.J., Hope R. Evolution and molecular characterization of a beta-globin gene from the Australian Echidna Tachyglossus aculeatus (Monotremata). Mol Phylogenet Evol. 12:1999;205-214.
33. Killian J.K., Buckley T.R., Stewart N., Munday B.L., Jirtle R.L. Marsupials and Eutherians reunited: genetic evidence for the Theria hypothesis of mammalian evolution. Mamm Genome. 12:2001;513-517.
34. Belov K., Zenger K.R., Hellman L., Cooper D.W. Echidna IgA supports mammalian unity and traditional Therian relationship. Mamm Genome. 13:2002;656-663.
35. Miska K.B., Harrison G.A., Hellman L., Miller R.D. The major histocompatibility complex in monotremes: an analysis of the evolution of Mhc class I genes across all three mammalian subclasses. Immunogenetics. 54:2002;381-393.
36. Miska K.B., Hellman L., Miller R.D. Characterization of β2-microglobulin coding sequence from three non-placental mammals: the duckbill platypus, the short-beaked echidna, and the grey short-tailed opossum. Dev Comp Immunol. 3:2003;247-256.
37. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 162:1987;156-159.
38. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:1997;4876-4882.
39. Felsenstein J. PHYLIP 3.6; 2002. http://evolution.gs.washington.edu/phylip.html .
40. Adachi J., Hasegawa M. Comput Sci Monogr 28. Comput Sci Monogr 28. 1996;Institute of Statistical Mathematics, Tokyo.
41. Dayhoff M.O., Schwartz R.M., Orcutt B.C. A model of evolutionary change in proteins. Dayhoff M.O. Atlas of Protein Sequence Structure. 1978;345-352 National Biomedical Research Foundation, Washington DC.
42. Jones D.T., Taylor W.R., Thornton J.M. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 8:1992;275-282.
43. Swofford DL. PAUP: phylogenetic analysis using parsimony. Version 3.1.1. Distributed by the Illinois Natural History Survey, Champaign, IL; 1993.
44. Page R.D. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 12:1996;357-358.
45. Johansson J., Aveskogh M., Munday B., Hellman L. Heavy chain V region diversity in the duck-billed platypus (Ornithorhynchus anatinus): long and highly variable complementarity-determining region 3 compensates for limited germline diversity. J Immunol. 168:2002;5155-5162.
46. Belov K., Harrison G.A., Miller R.D., Cooper D.W. Molecular cloning of the brushtail possum (Trichosurus vulpecula) immunglobulin E heavy chain constant region. Mol Immunol. 36:1999;1255-1261.
47. Dorrington K.J., Bennich H.H. Structure-function relationships in human immunoglobulin E. Immunol Rev. 41:1978;3-25.
48. Baenziger J., Kornfeld S., Kochwa S. Structure of the carbohydrate units of IgE immunoglobulin I. Over-all composition, glycopeptide isolation, and structure of the high mannose oligosaccharide unit. J Biol Chem. 249:1974;1889-1896.
49. Young R.J., Owens R.J., Mackay G.A., Chan C.M., Shi J., Hide M., Francis D.M., Henry A.J., Sutton B.J., Gould H.J. Secretion of recombinant human IgE-Fc by mammalian cells and biological activity of glycosylation site mutants. Protein Eng. 8:1995;193-199.
50. Fridriksson E.K., Beavil A., Holowka D., Gould H.J., Baird B., McLafferty F.W. Heterogeneous glycosylation of immunoglobulin E constructs characterized by top-down high-resolution 2D mass spectrometry. Biochemistry. 39:2000;3369-3376.
51. Wurzburg B.A., Garman S.C., Jardetzky T.S. Structure of the human IgE-Fc C epsilon 3-C epsilon 4 reveals conformational flexibility in the antibody effector domains. Immunity. 13:2000;375-385.
52. Helm B.A., Sayers I., Higginbottom A., Machado D.C., Ling Y., Ahmad K., Padlan E.A., Wilson A.P. Identification of the high affinity receptor binding region in human immunoglobulin E. J Biol Chem. 271:1996;7494-7500.
53. Basu M., Hakimi J., Dharm E., Kondas J.A., Tsien W.H., Pilson R.S., Lin P., Gilfillan A., Haring P., Braswell E.H., et al. Purification and characterization of human recombinant IgE-Fc fragments that bind to the human high affinity IgE receptor. J Biol Chem. 268:1993;13118-13127.
54. Sayers I., Cain S.A., Swan J.R., Pickett M.A., Watt P.J., Holgate S.T., Padlan E.A., Schuck P., Helm B.A. Amino acid residues that influence Fc epsilon RI-mediated effector functions of human immunoglobulin E. Biochemistry. 37:1998;16152-16164.
55. Da Luz J. Aspects of N -glycosylation in human IgE. Department of Medicin, Karolinska Institutet. ISBN 91-7349-130-6. Stockholm: Repro Print AB; 2002.
56. Jefferis R., Lund J., Pound J.D. IgG-Fc-mediated effector functions: molecular definition of interaction sites for effector ligands and the role of glycosylation. Immunol Rev. 163:1998;59-76.
57. Wan T., Beavil R.L., Fabiane S.M., Beavil A.J., Sohi M.K., Keown M., Young R.J., Henry A.J., Owens R.J., Gould H.J., Sutton B.J. The crystal structure of IgE-Fc reveals an asymmetrically bent conformation. Nat Immunol. 3:2002;681-686.
58. McDonnell J.M., Calvert R., Beavil R.L., Beavil A.J., Henry A.J., Sutton B.J., Gould H.J., Cowburn D. The structure of the IgE Cepsilon2 domain and its role in stabilizing the complex with its high-affinity receptor FcepsilonRIalpha. Nat Struct Biol. 8:2001;437-441.
59. Novak N., Bieber T. To bend or not to bend. Nat Immunol. 3:2002;607-608.
60. Bjorklund J.E., Schmidt M., Magnusson C.G. Characterisation of recombinant human IgE-Fc fragments expressed in baculovirus-infected insect cells. Mol Immunol. 37:2000;169-177.
61. Wagner B., Siebenkotten G., Radbruch A., Leibold W. Nucleotide sequence and restriction fragment length polymorphisms of the equine Cvarepsilon gene. Vet Immunol Immunopathol. 82:2001;193-202.
62. Navarro P., Barbis D.P., Antczak D., Butler J.E. The complete cDNA and deduced amino acid sequence of equine IgE. Mol Immunol. 32:1995;1-8.
63. Hempstead B.L., Parker C.W., Kulczycki A. Jr. Characterization of the IgE receptor isolated from human basophils. J Immunol. 123:1979;2283-2291.
64. Conrad D.H., Wingard J.R., Ishizaka T. The interaction of human and rodent IgE with the human basophil IgE receptor. J Immunol. 130:1983;327-333.
65. Nissim A., Schwarzbaum S., Siraganian R., Eshhar Z. Fine specificity of the IgE interaction with the low and high affinity Fc receptor. J Immunol. 150:1993;1365-1374.
66. Kulczycki A., Isersky C., Metzger H. The interaction of IgE with rat basophilic leukemia cells. I. Evidence for specific binding of IgE. J Exp Med. 139:1974;600-616.
67. Lowenthal M., Patterson R., Harris K.E. Passive transfer of IgE-mediated cutaneous reactivity in heterologous species. Ann Allergy. 71:1993;481-484.
68. Mackay G.A., Hulett M.D., Cook J.P., Trist H.M., Henry A.J., McDonnell J.M., Beavil A.J., Beavil R.L., Sutton B.J., Hogarth P.M., Gould H.J. Mutagenesis within human FcepsilonRIalpha differentially affects human and murine IgE binding. J Immunol. 168:2002;1787-1795.
69. Kumar S., Hedges S.B. A molecular timescale for vertebrate evolution. Nature. 392:1998;917-920.
70. Archer M., Flannery T.F., Ritchie A., Molnar R.E. First Mesozoic mammal from Australia-an early Cretaceous monotreme. Nature. 318:1985;363-366.