Linking class-switch recombination with somatic hypermutation (original) (raw)

• Lander, E. S. et al. Initial sequencing and analysis of the human genome. International Human Genome Sequencing Consortium. Nature 409, 860–921 (2001).
  Article CAS PubMed Google Scholar
• Venter, J. C. et al. The sequence of the human genome. Science 291, 1304–1351 (2001).
  Article CAS PubMed Google Scholar
• Maas, S. & Rich, A. Changing genetic information through RNA editing. Bioessays 22, 790–802 (2000).
  Article CAS PubMed Google Scholar
• Oettinger, M. A. V(D)J recombination: on the cutting edge. Curr. Opin. Cell Biol. 11, 325–329 (1999).
  Article CAS PubMed Google Scholar
• Muramatsu, M. et al. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553–563 (2000).AID, a member of RNA-editing cytidine deaminase family, is crucial in class-switch recombination and somatic hypermutation. This paper was the first to indicate the possible involvement of RNA editing in the alteration of DNA information.
  Article CAS PubMed Google Scholar
• Muramatsu, M. & Honjo, T. Complex layers of genetic alteration in the generation of antibody diversity. Trends Immunol. 22, 66–68 (2001).
  Article CAS PubMed Google Scholar
• Honjo, T. & Kataoka, T. Organization of immunoglobulin heavy chain genes and allelic deletion model. Proc. Natl Acad. Sci. USA 75, 2140–2144 (1978).
  Article CAS PubMed PubMed Central Google Scholar
• Kataoka, T., Kawakami, T., Takahashi, N. & Honjo, T. Rearrangement of immunoglobulin gamma 1-chain gene and mechanism for heavy-chain class switch. Proc. Natl Acad. Sci. USA 77, 919–923 (1980).
  Article CAS PubMed PubMed Central Google Scholar
• Davis, M. M. et al. An immunoglobulin heavy-chain gene is formed by at least two recombinational events. Nature 283, 733–739 (1980).
  Article CAS PubMed Google Scholar
• Maki, R., Traunecker, A., Sakano, H., Roeder, W. & Tonegawa, S. Exon shuffling generates an immunoglobulin heavy chain gene. Proc. Natl Acad. Sci. USA 77, 2138–2142 (1980).
  Article CAS PubMed PubMed Central Google Scholar
• Rabbitts, T. H., Forster, A., Dunnick, W. & Bentley, D. L. The role of gene deletion in the immunoglobulin heavy chain switch. Nature 283, 351–356 (1980).
  Article CAS PubMed Google Scholar
• Cory, S., Jackson, J. & Adams, J. M. Deletions in the constant region locus can account for switches in immunoglobulin heavy chain expression. Nature 285, 450–456 (1980).
  Article CAS PubMed Google Scholar
• Sakano, H., Maki, R., Kurosawa, Y., Roeder, W. & Tonegawa, S. Two types of somatic recombination are necessary for the generation of complete immunoglobulin heavy-chain genes. Nature 286, 676–683 (1980).
  Article CAS PubMed Google Scholar
• Davis, M. M., Kim, S. K. & Hood, L. E. DNA sequences mediating class switching in α-immunoglobulins. Science 209, 1360–1365 (1980).
  Article CAS PubMed Google Scholar
• Shimizu, A., Takahashi, N., Yaoita, Y. & Honjo, T. Organization of the constant-region gene family of the mouse immunoglobulin heavy chain. Cell 28, 499–506 (1982).
  Article CAS PubMed Google Scholar
• Iwasato, T., Shimizu, A., Honjo, T. & Yamagishi, H. Circular DNA is excised by immunoglobulin class switch recombination. Cell 62, 143–149 (1990).
  Article CAS PubMed Google Scholar
• Matsuoka, M., Yoshida, K., Maeda, T., Usuda, S. & Sakano, H. Switch circular DNA formed in cytokine-treated mouse splenocytes: evidence for intramolecular DNA deletion in immunoglobulin class switching. Cell 62, 135–142 (1990).
  Article CAS PubMed Google Scholar
• von Schwedler, U., Jack, H. M. & Wabl, M. Circular DNA is a product of the immunoglobulin class switch rearrangement. Nature 345, 452–456 (1990).
  Article CAS PubMed Google Scholar
• Yancopoulos, G. D. et al. Secondary genomic rearrangement events in pre-B cells: _V_H_DJ_H replacement by a LINE-1 sequence and directed class switching. EMBO J. 5, 3259–3266 (1986).
  Article CAS PubMed PubMed Central Google Scholar
• Stavnezer, N. J. & Sirlin, S. Specificity of immunoglobulin heavy chain switch correlates with activity of germline heavy chain genes prior to switching. EMBO J. 5, 95–102 (1986).
  Article Google Scholar
• Muramatsu, M. et al. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J. Biol. Chem. 274, 18470–18476 (1999).
  Article CAS PubMed Google Scholar
• Rolink, A., Melchers, F. & Andersson, J. The SCID but not the RAG-2 gene product is required for Sμ-Sɛ heavy chain class switching. Immunity 5, 319–330 (1996).
  Article CAS PubMed Google Scholar
• Casellas, R. et al. Ku80 is required for immunoglobulin isotype switching. EMBO J. 17, 2404–2411 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Manis, J. P. et al. Ku70 is required for late B cell development and immunoglobulin heavy chain class switching. J. Exp. Med. 187, 2081–2089 (1998).References 22–24 showed that class-switch recombination depends on non-homologous end joining.
  Article CAS PubMed PubMed Central Google Scholar
• Gu, H., Zou, Y. R. & Rajewsky, K. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-_loxP_-mediated gene targeting. Cell 73, 1155–1164 (1993).
  Article CAS PubMed Google Scholar
• Jung, S., Rajewsky, K. & Radbruch, A. Shutdown of class switch recombination by deletion of a switch region control element. Science 259, 984–987 (1993).
  Article CAS PubMed Google Scholar
• Zhang, J., Bottaro, A., Li, S., Stewart, V. & Alt, F. W. A selective defect in IgG2b switching as a result of targeted mutation of the _I_γ2b promoter and exon. EMBO J. 12, 3529–3537 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Seidl, K. J. et al. An expressed neor cassette provides required functions of the _I_γ2b exon for class switching. Int. Immunol. 10, 1683–1692 (1998).
  Article CAS PubMed Google Scholar
• Blackwell, T. K. et al. Recombination between immunoglobulin variable region gene segments is enhanced by transcription. Nature 324, 585–589 (1986).
  Article CAS PubMed Google Scholar
• Ott, D. E., Alt, F. W. & Marcu, K. B. Immunoglobulin heavy chain switch region recombination within a retroviral vector in murine pre-B cells. EMBO J. 6, 557–584 (1987).
  Article Google Scholar
• Leung, H. & Maizels, N. Transcriptional regulatory elements stimulate recombination in extrachromosomal substrates carrying immunoglobulin switch-region sequences. Proc. Natl Acad. Sci. USA 89, 4154–4158 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Lepse, C. L., Kumar, R. & Ganea, D. Extrachromosomal eukaryotic DNA substrates for switch recombination: analysis of isotype and cell specificity. DNA Cell Biol. 13, 1151–1161 (1994).
  Article CAS PubMed Google Scholar
• Daniels, G. A. & Lieber, M. R. Strand specificity in the transcriptional targeting of recombination at immunoglobulin switch sequences. Proc. Natl Acad. Sci. USA 92, 5625–5629 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Kinoshita, K., Tashiro, J., Tomita, S., Lee, C. G. & Honjo, T. Target specificity of immunoglobulin class switch recombination is not determined by nucleotide sequences of S regions. Immunity 9, 849–858 (1998).An artificial substrate reported here showed clear cytokine inducibility. Using this system, S sequences of different isotypes are shown to be equally targeted in the same cell undergoing IgA switching, indicating lack of isotype specificity of S regions.
  Article CAS PubMed Google Scholar
• Christine, R., Siebenkotten, G. & Radbruch, A. Sensitive analysis of recombination activity using integrated cell surface reporter substrates. Cytometry 37, 205–214 (1999).
  Article CAS PubMed Google Scholar
• Stavnezer, J. et al. Switch recombination in a transfected plasmid occurs preferentially in a B cell line that undergoes switch recombination of its chromosomal Ig heavy chain genes. J. Immunol. 163, 2028–2040 (1999).
  CAS PubMed Google Scholar
• Nakamura, M. et al. High frequency class switching of an IgM+ B lymphoma clone CH12F3 to IgA+ cells. Int. Immunol. 8, 193–201 (1996).A unique cell line, CH12F3, useful for studying class-switch recombination, was established by subcloning the CH12.LX cell line, a mouse lymphoma line. This cell line has advantage over other B-cell lines in its efficiency and in the cytokine inducibility of class-switch recombination.
  Article CAS PubMed Google Scholar
• Ott, D. E. & Marcu, K. B. Molecular requirements for immunoglobulin heavy chain constant region gene switch-recombination revealed with switch-substrate retroviruses. Int. Immunol. 1, 582–591 (1989).
  Article CAS PubMed Google Scholar
• Luby, T. M., Schrader, C. E., Stavnezer, J. & Selsing, E. The μ switch region tandem repeats are important, but not required, for antibody class switch recombination. J. Exp. Med. 193, 159–168 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Tashiro, J., Kinoshita, K. & Honjo, T. Palindromic but not G-rich sequences are targets of class switch recombination. Int. Immunol. 13, 495–505 (2001).This study, using artificial substrates, showed that non-mammalian S sequences of chicken and frog (but not a G-rich telomere repeat) can be recognized by mouse recombinase. An artificial sequence containing palindromes was recognized, suggesting the recognition of DNA structure, but not of the primary sequence of S sequences, by the class-switch recombinase.
  Article CAS PubMed Google Scholar
• Mussmann, R., Courtet, M., Schwager, J. & Du Pasquier, L. Microsites for immunoglobulin switch recombination breakpoints from Xenopus to mammals. Eur. J. Immunol. 27, 2610–2619 (1997).
  Article CAS PubMed Google Scholar
• SantaLucia, J. A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc. Natl Acad. Sci. USA 95, 1460–1465 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Kinoshita, K. et al. in Cold Spring Harbor Symposia on Quantitative Biology: Signaling & Gene Expression in the Immune System 217–226 (Cold Spring Harbor Laboratory Press, New York, 1999).
  Google Scholar
• Lee, C.-G., Kondo, S. & Honjo, T. Frequent but biased class switch recombination in the _S_μ flanking regions. Curr. Biol. 8, 227–230 (1998).
  Article CAS PubMed Google Scholar
• Dunnick, W., Hertz, G. Z., Scappino, L. & Gritzmacher, C. DNA sequences at immunoglobulin switch region recombination sites. Nucleic Acids Res. 21, 365–372 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Storb, U. et al. _Cis_-acting sequences that affect somatic hypermutation of Ig genes. Immunol. Rev. 162, 153–160 (1998).
  Article CAS PubMed Google Scholar
• Jacobs, H. & Bross, L. Towards an understanding of somatic hypermutation. Curr. Opin. Immunol. 13, 208–218 (2001).
  Article CAS PubMed Google Scholar
• Mantovani, L., Wilder, R. L. & Casali, P. Human rheumatoid B-1a (CD5+ B) cells make somatically hypermutated high affinity IgM rheumatoid factors. J. Immunol. 151, 473–488 (1993).
  CAS PubMed Google Scholar
• Sohn, J., Gerstein, R. M., Hsieh, C. L., Lemer, M. & Selsing, E. Somatic hypermutation of an immunoglobulin mu heavy chain transgene. J. Exp. Med. 177, 493–504 (1993).
  Article CAS PubMed Google Scholar
• Betz, A. G. et al. Elements regulating somatic hypermutation of an immunoglobulin kappa gene: critical role for the intron enhancer/matrix attachment region. Cell 77, 239–248 (1994).
  Article CAS PubMed Google Scholar
• Fukita, Y., Jacobs, H. & Rajewsky, K. Somatic hypermutation in the heavy chain locus correlates with transcription. Immunity 9, 105–114 (1998).
  Article CAS PubMed Google Scholar
• Bachl, J., Carlson, C., Gray-Schopfer, V., Dessing, M. & Olsson, C. Increased transcription levels induce higher mutation rates in a hypermutating cell line. J. Immunol. 166, 5051–5057 (2001).
  Article CAS PubMed Google Scholar
• Papavasiliou, F. N. & Schatz, D. G. Cell-cycle-regulated DNA double-stranded breaks in somatic hypermutation of immunoglobulin genes. Nature 408, 216–221 (2000).This paper showed the presence of double-stranded DNA breaks during somatic hypermutation in a Burkitt's lymphoma line by the ligation-mediated PCR method. Accumulation of double-stranded breaks in late S/G2 phase was observed, leading to a model in which cleavage is regulated by the cell cycle and repair is then mediated by homologous recombination.
  Article CAS PubMed Google Scholar
• Brenner, S. & Milstein, C. Origin of antibody variation. Nature 211, 242–243 (1966).
  Article CAS PubMed Google Scholar
• Rogozin, I. B. & Kolchanov, N. A. Somatic hypermutagenesis in immunoglobulin genes. II. Influence of neighbouring base sequences on mutagenesis. Biochim. Biophys. Acta 1171, 11–18 (1992).
  Article CAS PubMed Google Scholar
• Azuma, T., Motoyama, N., Fields, L. E. & Loh, D. Y. Mutations of the chloramphenicol acetyl transferase transgene driven by the immunoglobulin promoter and intron enhancer. Int. Immunol. 5, 121–130 (1993).
  Article CAS PubMed Google Scholar
• Yelamos, J. et al. Targeting of non-Ig sequences in place of the V segment by somatic hypermutation. Nature 376, 225–229 (1995).
  Article CAS PubMed Google Scholar
• Peters, A. & Storb, U. Somatic hypermutation of immunoglobulin genes is linked to transcription initiation. Immunity 4, 57–65 (1996).
  Article CAS PubMed Google Scholar
• Shen, H. M., Peters, A., Baron, B., Zhu, X. & Storb, U. Mutation of BCL-6 gene in normal B cells by the process of somatic hypermutation of Ig genes. Science 280, 1750–1752 (1998).
  Article CAS PubMed Google Scholar
• Pasqualucci, L. et al. BCL-6 mutations in normal germinal center B cells: evidence of somatic hypermutation acting outside Ig loci. Proc. Natl Acad. Sci. USA 95, 11816–11821 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Klotz, E. L., Hackett, J., Jr & Storb, U. Somatic hypermutation of an artificial test substrate within an Ig kappa transgene. J. Immunol. 161, 782–790 (1998).
  CAS PubMed Google Scholar
• Storb, U. et al. A hypermutable insert in an immunoglobulin transgene contains hotspots of somatic mutation and sequences predicting highly stable structures in the RNA transcript. J. Exp. Med. 188, 689–698 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Kolchanov, N. A., Solovyov, V. V. & Rogozin, I. B. Peculiarities of immunoglobulin gene structures as a basis for somatic mutation emergence. FEBS Lett. 214, 87–91 (1987).
  Article CAS PubMed Google Scholar
• Goossens, T., Klein, U. & Kuppers, R. Frequent occurrence of deletions and duplications during somatic hypermutation: implications for oncogene translocations and heavy chain disease. Proc. Natl Acad. Sci. USA 95, 2463–2468 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Wilson, P. C. et al. Somatic hypermutation introduces insertions and deletions into immunoglobulin V genes. J. Exp. Med. 187, 59–70 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Sale, J. E. & Neuberger, M. S. TdT-accessible breaks are scattered over the immunoglobulin V domain in a constitutively hypermutating B cell line. Immunity 9, 859–869 (1998).
  Article CAS PubMed Google Scholar
• Bross, L. et al. DNA double-strand breaks in immunoglobulin genes undergoing somatic hypermutation. Immunity 13, 589–597 (2000).A report of double-stranded DNA breaks during somatic hypermutation in mouse splenocytes. There are intriguing data and discussions on the effect of the relative position of the promoter and immunoglobulin enhancer on deletion frequency in the V gene, which is not discussed in this review.
  Article CAS PubMed Google Scholar
• Kong, Q. & Maizels, N. DNA breaks in hypermutating immunoglobulin genes. Evidence for a break-and-repair pathway of somatic hypermutation. Genetics 158, 369–378 (2001).
  CAS PubMed PubMed Central Google Scholar
• Jacobs, H. et al. Hypermutation of immunoglobulin genes in memory B cells of DNA repair-deficient mice. J. Exp. Med. 187, 1735–1743 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, N., Kage, K., Matsuda, F., Lefranc, M. P. & Storb, U. B lymphocytes of xeroderma pigmentosum or Cockayne syndrome patients with inherited defects in nucleotide excision repair are fully capable of somatic hypermutation of immunoglobulin genes. J. Exp. Med. 186, 413–419 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Cascalho, M., Wong, J., Steinberg, C. & Wabl, M. Mismatch repair co-opted by hypermutation. Science 279, 1207–1210 (1998).
  Article CAS PubMed Google Scholar
• Winter, D. B. et al. Altered spectra of hypermutation in antibodies from mice deficient for the DNA mismatch repair protein PMS2. Proc. Natl Acad. Sci. USA 95, 6953–6958 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Bertocci, B. et al. Probing immunoglobulin gene hypermutation with microsatellites suggests a nonreplicative short patch DNA synthesis process. Immunity 9, 257–265 (1998).
  Article CAS PubMed Google Scholar
• Frey, S. et al. Mismatch repair deficiency interferes with the accumulation of mutations in chronically stimulated B cells and not with the hypermutation process. Immunity 9, 127–134 (1998).
  Article CAS PubMed Google Scholar
• Rada, C., Ehrenstein, M. R., Neuberger, M. S. & Milstein, C. Hot spot focusing of somatic hypermutation in _MSH2_-deficient mice suggests two stages of mutational targeting. Immunity 9, 135–141 (1998).
  Article CAS PubMed Google Scholar
• Phung, Q. H. et al. Increased hypermutation at G and C nucleotides in immunoglobulin variable genes from mice deficient in the MSH2 mismatch repair protein. J. Exp. Med. 187, 1745–1751 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, N., Bozek, G., Lo, J. C. & Storb, U. Different mismatch repair deficiencies all have the same effects on somatic hypermutation: intact primary mechanism accompanied by secondary modifications. J. Exp. Med. 190, 21–30 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Ehrenstein, M. R. & Neuberger, M. S. Deficiency in Msh2 affects the efficiency and local sequence specificity of immunoglobulin class-switch recombination: parallels with somatic hypermutation. EMBO J. 18, 3484–3490 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Schrader, C. E., Edelmann, W., Kucherlapati, R. & Stavnezer, J. Reduced isotype switching in splenic B cells from mice deficient in mismatch repair enzymes. J. Exp. Med. 190, 323–330 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Wiesendanger, M., Kneitz, B., Edelmann, W. & Scharff, M. D. Somatic hypermutation in MutS homologue (MSH)3-, MSH6-, and MSH3/MSH6-deficient mice reveals a role for the MSH2–MSH6 heterodimer in modulating the base substitution pattern. J. Exp. Med. 191, 579–584 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Thompson, C. B. & Neiman, P. E. Somatic diversification of the chicken immunoglobulin light chain gene is limited to the rearranged variable gene segment. Cell 48, 369–378 (1987).
  Article CAS PubMed Google Scholar
• Reynaud, C. A., Anquez, V., Grimal, H. & Weill, J. C. A hyperconversion mechanism generates the chicken light chain preimmune repertoire. Cell 48, 379–388 (1987).
  Article CAS PubMed Google Scholar
• Bemark, M. et al. Somatic hypermutation in the absence of DNA-dependent protein kinase catalytic subunit (DNA-PKcs) or recombination-activating gene (RAG)1 activity. J. Exp. Med. 192, 1509–1514 (2000).Unlike class-switch recombination, somatic hypermutation does not require the catalytic subunit of the DNA-dependent protein kinase (DNA-PK cs ), indicating that different mechanisms of DNA repair might occur between class-switch recombination and somatic hypermutation.
  Article CAS PubMed PubMed Central Google Scholar
• Allen, R. C. et al. CD40 ligand gene defects responsible for X-linked hyper-IgM syndrome. Science 259, 990–993 (1993).
  Article CAS PubMed Google Scholar
• Aruffo, A. et al. The CD40 ligand, gp39, is defective in activated T cells from patients with X-linked hyper-IgM syndrome. Cell 72, 291–300 (1993).
  Article CAS PubMed Google Scholar
• DiSanto, J. P., Bonnefoy, J. Y., Gauchat, J. F., Fischer, A. & de Saint Basile, G. CD40 ligand mutations in X-linked immunodeficiency with hyper-IgM. Nature 361, 541–543 (1993).
  Article CAS PubMed Google Scholar
• Fuleihan, R. et al. Defective expression of the CD40 ligand in X chromosome-linked immunoglobulin deficiency with normal or elevated IgM. Proc. Natl Acad. Sci. USA 90, 2170–2173 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Korthauer, U. et al. Defective expression of T-cell CD40 ligand causes X-linked immunodeficiency with hyper-IgM. Nature 361, 539–541 (1993).
  Article CAS PubMed Google Scholar
• Revy, P., Geissmann, F., Debre, M., Fischer, A. & Durandy, A. Normal CD40-mediated activation of monocytes and dendritic cells from patients with hyper-IgM syndrome due to a CD40 pathway defect in B cells. Eur. J. Immunol. 28, 3648–3654 (1998).
  Article CAS PubMed Google Scholar
• Revy, P. et al. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the hyper-IgM syndrome (HIGM2). Cell 102, 565–575 (2000).
  Article CAS PubMed Google Scholar
• Chester, A., Scott, J., Anant, S. & Navaratnam, N. RNA editing: cytidine to uridine conversion in apolipoprotein B mRNA. Biochim. Biophys. Acta 1494, 1–13 (2000).
  Article CAS PubMed Google Scholar
• Mehta, A., Kinter, M. T., Sherman, N. E. & Driscoll, D. M. Molecular cloning of apobec-1 complementation factor, a novel RNA-binding protein involved in the editing of apolipoprotein B mRNA. Mol. Cell. Biol. 20, 1846–1854 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Daniels, G. A. & Lieber, M. R. RNA–DNA complex formation upon transcription of immunoglobulin switch regions: implications for the mechanism and regulation of class switch recombination. Nucleic Acids Res. 23, 5006–5011 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Tian, M. & Alt, F. W. Transcription-induced cleavage of immunoglobulin switch regions by nucleotide excision repair nucleases in vitro. J. Biol. Chem. 275, 24163–24172 (2000).
  Article CAS PubMed Google Scholar
• Taub, R. et al. Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proc. Natl Acad. Sci. USA 79, 7837–7841 (1982).
  Article CAS PubMed PubMed Central Google Scholar
• Wang, Q., Khillan, J., Gadue, P. & Nishikura, K. Requirement of the RNA editing deaminase ADAR1 gene for embryonic erythropoiesis. Science 290, 1765–1768 (2000).
  Article CAS PubMed Google Scholar
• Teng, B., Burant, C. F. & Davidson, N. O. Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260, 1816–1819 (1993).
  Article CAS PubMed Google Scholar
• Melcher, T. et al. A mammalian RNA editing enzyme. Nature 379, 460–464 (1996).
  Article CAS PubMed Google Scholar
• Rueter, S. M., Dawson, T. R. & Emeson, R. B. Regulation of alternative splicing by RNA editing. Nature 399, 75–80 (1999).
  Article CAS PubMed Google Scholar
• Burns, C. M. et al. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387, 303–308 (1997).
  Article CAS PubMed Google Scholar
• Ma, J., Qian, R., Rausa, F. M. & Colley, K. J. Two naturally occurring α2,6-sialyltransferase forms with a single amino acid change in the catalytic domain differ in their catalytic activity and proteolytic processing. J. Biol. Chem. 272, 672–679 (1997).
  Article CAS PubMed Google Scholar
• Casey, J. L. & Gerin, J. L. Hepatitis D virus RNA editing: specific modification of adenosine in the antigenomic RNA. J. Virol. 69, 7593–7600 (1995).
  CAS PubMed PubMed Central Google Scholar
• Bourara, K., Litvak, S. & Araya, A. Generation of G-to-A and C-to-U changes in HIV-1 transcripts by RNA editing. Science 289, 1564–1566 (2000).
  Article CAS PubMed Google Scholar
• Volchkov, V. E. et al. GP mRNA of Ebola virus is edited by the Ebola virus polymerase and by T7 and vaccinia virus polymerases. Virology 214, 421–430 (1995).
  Article CAS PubMed Google Scholar
• Sharma, P. M., Bowman, M., Madden, S. L., Rauscher, F. J. & Sukumar, S. RNA editing in the Wilms' tumor susceptibility gene, WT1. Genes Dev. 8, 720–731 (1994).
  Article CAS PubMed Google Scholar