Somatic translocation and differential expression of Ig μ transgene copies implicate a role for the Igh locus in memory B cell development

Molecular Immunology

Volumn 39, Issue 14, 2003, Pages 885-897

  Jena, Prasanna K ^a   Smith, Diana S ^a   Zhang, Xianghua ^a   Aviszus, Katja ^a   Durdik, Jeannine M ^b   Wysocki, Lawrence J ^a  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^b UNIVERSITY OF ARKANSAS   (United States)

Author keywords

Affinity maturation; B lymphocytes; Hypermutation; Memory cells

Indexed keywords

IMMUNOGLOBULIN; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN MU CHAIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENE TRANSLOCATION; HYBRIDOMA; IMMUNIZATION; MEMORY CELL; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; TRANSGENE; V GENE;

MUS MUSCULUS;

EID: 0037403078     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0161-5890(03)00006-3     Document Type: Article

References (60)

1. Aoufouchi S., Yelamos J., Milstein C. Nonsense mutations inhibit RNA splicing in a cell-free system: recognition of mutant codon is independent of protein synthesis. Cell. 85:1996;415-422.
2. Baumann B., Potash M.J., Kohler G. Consequences of frameshift mutations at the immunoglobulin heavy chain locus of the mouse. EMBO J. 4:1985;351-359.
3. Berek C., Griffiths G.M., Milstein C. Molecular events during maturation of the immune response to oxazolone. Nature. 316:1985;412-418.
4. Berek C., Milstein C. The dynamic nature of the antibody repertoire. Immunol. Rev. 105:1988;5-26.
5. Betz A.G., Milstein C., Gonzalez-Fernandez A., Pannell R., Larson T., Neuberger M.S. Elements regulating somatic hypermutation of an immunoglobulin κ gene: critical role for the intron enhancer/matrix attachment region. Cell. 77:1994;239-248.
6. Bloom D.D., Clair St.ClairE.W., Pisetsky D.S., Clarke S.H. The anti-La response of a single MRL/Mp-lpr/lpr mouse: specificity for DNA and VH gene usage. Eur. J. Immunol. 24:1994;1332-1338.
7. Carter M.S., Li S., Wilkinson M.F. A splicing-dependent regulatory mechanism that detects translation signals. EMBO J. 15:1996;5965-5975.
8. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
9. Claflin J.L., Berry J., Flaherty D., Dunnick W. Somatic evolution of diversity among anti-phosphocholine antibodies induced with Proteus morganii. J. Immunol. 138:1987;3060-3068.
10. Clarke S.H., Huppi K., Ruezinsky D., Staudt L., Gerhard W., Weigert M. Inter- and intraclonal diversity in the antibody response to influenza hemagglutinin. J. Exp. Med. 161:1985;687-704.
11. Cleary M.L., Galili N., Trela M., Levy R., Sklar J. Single cell origin of bigenotypic and biphenotypic B cell proliferations in human follicular lymphomas. J. Exp. Med. 167:1988;582-597.
12. Durdik J., Gerstein R.M., Rath S., Robbins P.F., Nisonoff A., Selsing E. Isotype switching by a microinjected μ immunoglobulin heavy chain gene in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 86:1989;2346-2350.
13. Eckert K., Kunkel T.A. DNA polymerase fidelity and the polymerase chain reaction. PCR Methods Appl. 1:1991;17-34.
14. Ellenberger J., Creadon G., Zhang X., Wysocki L.J. Recruiting memory B cells with changed antigenic specificity. J. Immunol. 151:1993;5272-5281.
15. Gefter M.L., Margulies D.H., Scharff M.D. A simple method for polyethylene glycol-promoted hybridization of mouse myeloma cells. Somat. Cell Genet. 3:1977;231-236.
16. Gerstein R.M., Frankel W.N., Hsieh C.L., Durdik J.M., Rath S., Coffin J.M., Nisonoff A., Selsing E. Isotype switching of an immunoglobulin heavy chain transgene occurs by DNA recombination between different chromosomes. Cell. 63:1990;537-548.
17. Giusti A.M., Manser T. Hypermutation is observed only in antibody H chain V region transgenes that have recombined with endogenous immunoglobulin H DNA: implications for the location of cis-acting elements required for somatic mutation. J. Exp. Med. 177:1993;797-809.
18. Hande S., Notidis E., Manser T. Bcl-2 obstructs negative selection of autoreactive, hypermutated antibody V regions during memory B cell development. Immunity. 8:1998;189-198.
19. Heinzelmann A., Kumar S., Noggle S., Goedegebuur I., Sauer K.M., Rath S., Durdik J.M. Deletion of a recombined Ig heavy chain transgene in B-lineage cells of transgenic mice. J. Immunol. 161:1998;666-673.
20. Jena P.K., Liu A.H., Smith D.S., Wysocki L.J. Amplification of genes, single transcripts and cDNA libraries from one cell and direct sequence analysis of amplified products derived from one molecule. J. Immunol. Methods. 190:1996;199-213.
21. Jolly C.J., Neuberger M.S. Somatic hypermutation of immunoglobulin κ transgenes: association of mutability with demethylation. Immunol. Cell Biol. 79:2001;18-22.
22. Klein U., Klein G., Ehlin-Henriksson B., Rajewsky K., Kuppers R. Burkitt's lymphoma is a malignancy of mature B cells expressing somatically mutated V region genes. Mol. Med. 1:1995;495-505.
23. Kuo P., Bynoe M., Diamond B. Crossreactive B cells are present during a primary but not secondary response in BALB/c mice expressing a bcl-2 transgene. Mol. Immunol. 36:1999;471-479.
24. Kuppers R., Hajadi M., Plank L., Rajewsky K., Hansmann M.L. Molecular Ig gene analysis reveals that monocytoid B cell lymphoma is a malignancy of mature B cells carrying somatically mutated V region genes and suggests that rearrangement of the κ-deleting element (resulting in deletion of the Ig κ enhancers) abolishes somatic hypermutation in the human. Eur. J. Immunol. 26:1996;1794-1800.
25. Kussie P.H., Parhami-Seren B., Wysocki L.J., Margolies M.N. A single engineered amino acid substitution changes antibody fine specificity. J. Immunol. 152:1994;146-152.
26. Leo O., Slaoui M., Marvel J., Milner E.C., Hiernaux J., Moser M., Capra J.D., Urbain J. Idiotypic analysis of polyclonal and monoclonal anti-p-azophenylarsonate antibodies of BALB/c mice expressing the major cross-reactive idiotype of the A/J strain. J. Immunol. 134:1985;1734-1739.
27. Liu A.H., Creadon G., Wysocki L.J. Sequencing heavy- and light-chain variable genes of single B-hybridoma cells by total enzymatic amplification. Proc Natl. Acad. Sci. U.S.A. 89:1992a;7610-7614.
28. Liu A.H., Jena P.K., Wysocki L.J. Tracing the development of single memory-lineage B cells in a highly defined immune response. J. Exp. Med. 183:1996;2053-2063.
29. Liu Y.J., Johnson G.D., Gordon J., MacLennan I.C. Germinal centres in T-cell-dependent antibody responses. Immunol. Today. 13:1992b;17-21.
30. Losman M.J., Fasy T.M., Novick K.E., Monestier M. Relationships among antinuclear antibodies from autoimmune MRL mice reacting with histone H2A-H2B dimers and DNA. Int. Immunol. 5:1993;513-523.
31. Lozano F., Rada C., Jarvis J.M., Milstein C. Affinity maturation leads to differential expression of multiple copies of a κ light-chain transgene. Nature. 363:1993;271-273.
32. Manser T., Gefter M.L. Isolation of hybridomas expressing a specific heavy chain variable region gene segment by using a screening technique that detects mRNA sequences in whole cell lysates. Proc. Natl. Acad. Sci. U.S.A. 81:1984;2470-2474.
33. Manser T., Wysocki L.J., Margolies M.N., Gefter M.L. Evolution of antibody variable region structure during the immune response. Immunol. Rev. 96:1987;141-162.
34. Marion T.N., Tillman D.M., Jou N.T. Interclonal and intraclonal diversity among anti-DNA antibodies from an (NZB × NZW)F1 mouse. J. Immunol. 145:1990;2322-2332.
35. Marshak-Rothstein A., Siekevitz M., Margolies M.N., Mudgett-Hunter M., Gefter M.L. Hybridoma proteins expressing the predominant idiotype of the antiazophenylarsonate response of A/J mice. Proc. Natl. Acad. Sci. U.S.A. 77:1980;1120-1124.
36. Martin S.W., Goodnow C.C. Burst-enhancing role of the IgG membrane tail as a molecular determinant of memory. Nat. Immunol. 3:2002;182-188.
37. McKean D., Huppi K., Bell M., Staudt L., Gerhard W., Weigert M. Generation of antibody diversity in the immune response of BALB/c mice to influenza virus hemagglutinin. Proc. Natl. Acad. Sci. U.S.A. 81:1984;3180-3184.
38. Parhami-Seren B., Wysocki L.J., Margolies M.N., Sharon J. Clustered H chain somatic mutations shared by anti-p-azophenylarsonate antibodies confer enhanced affinity and ablate the cross-reactive idiotype. J. Immunol. 145:1990;2340-2346.
39. Paskulin G.A., Philips G., Morgan R., Sandberg A., Richkind K., Borovik C., McGavran L., Rabinovich N., Dietz-Band J., Erickson P., Drabkin H., Varella-Garcia M. Pre-clinical evaluation of probes to detect t(8;21. AML minimal residual disease by fluorescence in situ hybridization. Genes Chromosomes Cancer. 21:1998;144-151.
40. Peters A., Storb U. Somatic hypermutation of immunoglobulin genes is linked to transcription initiation. Immunity. 4:1996;57-65.
41. Portanova J.P., Creadon G., Zhang X., Smith D.S., Kotzin B.L., Wysocki L.J. An early post-mutational selection event directs expansion of autoreactive B cells in murine lupus. Mol. Immunol. 32:1995;117-135.
42. Przylepa J., Himes C., Kelsoe G. Lymphocyte development and selection in germinal centers. Curr. Top. Microbiol. Immunol. 229:1998;85-104.
43. Sanz I., Capra J.D. V κ and J κ gene segments of A/J Ars-A antibodies: somatic recombination generates the essential arginine at the junction of the variable and joining regions. Proc. Natl. Acad. Sci. U.S.A. 84:1987;1085-1089.
44. Shapiro G.S., Aviszus K., Ikle D., Wysocki L.J. Predicting regional mutability in antibody V genes based solely on di- and trinucleotide sequence composition. J. Immunol. 163:1999;259-268.
45. Shlomchik M.J., Marshak-Rothstein A., Wolfowicz C.B., Rothstein T.L., Weigert M.G. The role of clonal selection and somatic mutation in autoimmunity. Nature. 328:1987;805-811.
46. Shulman M., Wilde C.D., Kohler G. A better cell line for making hybridomas secreting specific antibodies. Nature. 276:1978;269-270.
47. Smith D.S., Creadon G., Jena P.K., Portanova J.P., Kotzin B.L., Wysocki L.J. Di- and trinucleotide target preferences of somatic mutagenesis in normal and autoreactive B cells. J. Immunol. 156:1996;2642-2652.
48. Sohn J., Gerstein R.M., Hsieh C.L., Lemer M., Selsing E. Somatic hypermutation of an immunoglobulin μ heavy chain transgene. J. Exp. Med. 177:1993;493-504.
49. Tindall K.R., Kunkel T.A. Fidelity of DNA synthesis by the Thermus aquaticus DNA polymerase. Biochemistry. 27:1988;6008-6013.
50. Tumas-Brundage K., Vora K.A., Giusti A.M., Manser T. Characterization of the cis-acting elements required for somatic hypermutation of murine antibody V genes using conventional transgenic and transgene homologous recombination approaches. Semin. Immunol. 8:1996;141-150.
51. Tumas-Brundage K.M., Vora K.A., Manser T. Evaluation of the role of the [3′α heavy chain enhancer 3′α E(hs1,2)] in Vh gene somatic hypermutation. Mol. Immunol. 34:1997;367-378.
52. Umar A., Gearhart P.J. Reciprocal homologous recombination in or near antibody VDJ genes. Eur. J. Immunol. 25:1995;2392-2400.
53. Umar A., Schweitzer P.A., Levy N.S., Gearhart J.D., Gearhart P.J. Mutation in a reporter gene depends on proximity to and transcription of immunoglobulin variable transgenes. Proc. Natl. Acad. Sci. U.S.A. 88:1991;4902-4906.
54. Wabl M., Jack H.M., Meyer J., Beck-Engeser G., von Borstel R.C., Steinberg C.M. Measurements of mutation rates in B lymphocytes. Immunol. Rev. 96:1987;91-107.
55. Wysocki L., Manser T., Gefter M.L. Somatic evolution of variable region structures during an immune response. Proc. Natl. Acad. Sci. U.S.A. 83:1986;1847-1851.
56. Wysocki L.J., Creadon G., Lehmann K.R., Cambier J.C. B-cell proliferation initiated by Ia cross-linking and sustained by interleukins leads to class switching but not somatic mutation in vitro. Immunology. 75:1992;116-121.
57. Wysocki L.J., Gefter M.L., Margolies M.N. Parallel evolution of antibody variable regions by somatic processes: consecutive shared somatic alterations in VH genes expressed by independently generated hybridomas apparently acquired by point mutation and selection rather than by gene conversion. J. Exp. Med. 172:1990;315-323.
58. Wysocki L.J., Gridley T., Huang S., Grandea A.G.D., Gefter M.L. Single germline VH and V κ genes encode predominating antibody variable regions elicited in strain A mice by immunization with p-azophenylarsonate. J. Exp. Med. 166:1987;1-11.
59. Wysocki L.J., Sato V.L. The strain A anti-p-azophenylarsonate major cross-reactive idiotypic family includes members with no reactivity toward p-azophenylarsonate. Eur. J. Immunol. 11:1981;832-839.
60. Zhu M., Green N.S., Rabinowitz J.L., Scharff M.D. Differential V region mutation of two transfected Ig genes and their interaction in cultured B cell lines. EMBO J. 15:1996;2738-2747.