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. 1997 Jun 15;25(12):2344–2351. doi: 10.1093/nar/25.12.2344

The murine IgM secretory poly(A) site contains dual upstream and downstream elements which affect polyadenylation.

C Phillips 1, A Virtanen 1
PMCID: PMC146757  PMID: 9171084

Abstract

Regulation of polyadenylation efficiency at the secretory poly(A) site plays an essential role in gene expression at the immunoglobulin (IgM) locus. At this poly(A) site the consensus AAUAAA hexanucleotide sequence is embedded in an extended AU-rich region and there are two downstream GU-rich regions which are suboptimally placed. As these sequences are involved in formation of the polyadenylation pre-initiation complex, we examined their function in vivo and in vitro . We show that the upstream AU-rich region can function in the absence of the consensus hexanucleotide sequence both in vivo and in vitro and that both GU-rich regions are necessary for full polyadenylation activity in vivo and for formation of polyadenylation-specific complexes in vitro . Sequence comparisons reveal that: (i) the dual structure is distinct for the IgM secretory poly(A) site compared with other immunoglobulin isotype secretory poly(A) sites; (ii) the presence of an AU-rich region close to the consensus hexanucleotide is evolutionarily conserved for IgM secretory poly(A) sites. We propose that the dual structure of the IgM secretory poly(A) site provides a flexibility to accommodate changes in polyadenylation complex components during regulation of polyadenylation efficiency.

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Selected References

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  1. Alt F. W., Bothwell A. L., Knapp M., Siden E., Mather E., Koshland M., Baltimore D. Synthesis of secreted and membrane-bound immunoglobulin mu heavy chains is directed by mRNAs that differ at their 3' ends. Cell. 1980 Jun;20(2):293–301. doi: 10.1016/0092-8674(80)90615-7. [DOI] [PubMed] [Google Scholar]
  2. Aström A., Aström J., Virtanen A. A simple procedure for isolation of eukaryotic mRNA polyadenylation factors. Eur J Biochem. 1991 Dec 18;202(3):765–773. doi: 10.1111/j.1432-1033.1991.tb16431.x. [DOI] [PubMed] [Google Scholar]
  3. Berberich I., Schimpl A. Regulation of Ig gene expression in normal lymphocytes. I. The half-life of secreted mu chain mRNA differs from that of membrane mu chain mRNA in resting and activated B cells. Eur J Immunol. 1990 Feb;20(2):445–448. doi: 10.1002/eji.1830200233. [DOI] [PubMed] [Google Scholar]
  4. Berberich I., Schimpl A. Regulation of immunoglobulin gene expression in normal lymphocytes. II. Mechanisms of down-regulation of immunoglobulin secretion after engagement of the B cell antigen receptor. Eur J Immunol. 1992 Feb;22(2):525–529. doi: 10.1002/eji.1830220235. [DOI] [PubMed] [Google Scholar]
  5. Bernstein K. E., Alexander C. B., Reddy E. P., Mage R. G. Complete sequence of a cloned cDNA encoding rabbit secreted mu-chain of VHa2 allotype: comparisons with VHa1 and membrane mu sequences. J Immunol. 1984 Jan;132(1):490–495. [PubMed] [Google Scholar]
  6. Carswell S., Alwine J. C. Efficiency of utilization of the simian virus 40 late polyadenylation site: effects of upstream sequences. Mol Cell Biol. 1989 Oct;9(10):4248–4258. doi: 10.1128/mcb.9.10.4248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chanfreau G., Noble S. M., Guthrie C. Essential yeast protein with unexpected similarity to subunits of mammalian cleavage and polyadenylation specificity factor (CPSF). Science. 1996 Nov 29;274(5292):1511–1514. doi: 10.1126/science.274.5292.1511. [DOI] [PubMed] [Google Scholar]
  8. Cherrington J., Ganem D. Regulation of polyadenylation in human immunodeficiency virus (HIV): contributions of promoter proximity and upstream sequences. EMBO J. 1992 Apr;11(4):1513–1524. doi: 10.1002/j.1460-2075.1992.tb05196.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dahan A., Reynaud C. A., Weill J. C. Nucleotide sequence of the constant region of a chicken mu heavy chain immunoglobulin mRNA. Nucleic Acids Res. 1983 Aug 25;11(16):5381–5389. doi: 10.1093/nar/11.16.5381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. DeZazzo J. D., Imperiale M. J. Sequences upstream of AAUAAA influence poly(A) site selection in a complex transcription unit. Mol Cell Biol. 1989 Nov;9(11):4951–4961. doi: 10.1128/mcb.9.11.4951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Early P., Rogers J., Davis M., Calame K., Bond M., Wall R., Hood L. Two mRNAs can be produced from a single immunoglobulin mu gene by alternative RNA processing pathways. Cell. 1980 Jun;20(2):313–319. doi: 10.1016/0092-8674(80)90617-0. [DOI] [PubMed] [Google Scholar]
  13. Edwalds-Gilbert G., Milcarek C. Regulation of poly(A) site use during mouse B-cell development involves a change in the binding of a general polyadenylation factor in a B-cell stage-specific manner. Mol Cell Biol. 1995 Nov;15(11):6420–6429. doi: 10.1128/mcb.15.11.6420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fellah J. S., Wiles M. V., Charlemagne J., Schwager J. Evolution of vertebrate IgM: complete amino acid sequence of the constant region of Ambystoma mexicanum mu chain deduced from cDNA sequence. Eur J Immunol. 1992 Oct;22(10):2595–2601. doi: 10.1002/eji.1830221019. [DOI] [PubMed] [Google Scholar]
  15. Flaspohler J. A., Milcarek C. Myelomas and lymphomas expressing the Ig gamma 2a H chain gene have similar transcription termination regions. J Immunol. 1990 Apr 1;144(7):2802–2810. [PubMed] [Google Scholar]
  16. Galli G., Guise J. W., McDevitt M. A., Tucker P. W., Nevins J. R. Relative position and strengths of poly(A) sites as well as transcription termination are critical to membrane versus secreted mu-chain expression during B-cell development. Genes Dev. 1987 Jul;1(5):471–481. doi: 10.1101/gad.1.5.471. [DOI] [PubMed] [Google Scholar]
  17. Galli G., Guise J., Tucker P. W., Nevins J. R. Poly(A) site choice rather than splice site choice governs the regulated production of IgM heavy-chain RNAs. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2439–2443. doi: 10.1073/pnas.85.8.2439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gilmartin G. M., Fleming E. S., Oetjen J., Graveley B. R. CPSF recognition of an HIV-1 mRNA 3'-processing enhancer: multiple sequence contacts involved in poly(A) site definition. Genes Dev. 1995 Jan 1;9(1):72–83. doi: 10.1101/gad.9.1.72. [DOI] [PubMed] [Google Scholar]
  19. Gilmartin G. M., Nevins J. R. An ordered pathway of assembly of components required for polyadenylation site recognition and processing. Genes Dev. 1989 Dec;3(12B):2180–2190. doi: 10.1101/gad.3.12b.2180. [DOI] [PubMed] [Google Scholar]
  20. Gilmartin G. M., Nevins J. R. Molecular analyses of two poly(A) site-processing factors that determine the recognition and efficiency of cleavage of the pre-mRNA. Mol Cell Biol. 1991 May;11(5):2432–2438. doi: 10.1128/mcb.11.5.2432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Graveley B. R., Fleming E. S., Gilmartin G. M. RNA structure is a critical determinant of poly(A) site recognition by cleavage and polyadenylation specificity factor. Mol Cell Biol. 1996 Sep;16(9):4942–4951. doi: 10.1128/mcb.16.9.4942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Grosschedl R., Baltimore D. Cell-type specificity of immunoglobulin gene expression is regulated by at least three DNA sequence elements. Cell. 1985 Jul;41(3):885–897. doi: 10.1016/s0092-8674(85)80069-6. [DOI] [PubMed] [Google Scholar]
  23. Honjo T., Obata M., Yamawaki-Katoaka Y., Kataoka T., Kawakami T., Takahashi N., Mano Y. Cloning and complete nucleotide sequence of mouse immunoglobulin gamma 1 chain gene. Cell. 1979 Oct;18(2):559–568. doi: 10.1016/0092-8674(79)90072-2. [DOI] [PubMed] [Google Scholar]
  24. Hunt A. G., MacDonald M. H. Deletion analysis of the polyadenylation signal of a pea ribulose-1,5-bisphosphate carboxylase small-subunit gene. Plant Mol Biol. 1989 Aug;13(2):125–138. doi: 10.1007/BF00016132. [DOI] [PubMed] [Google Scholar]
  25. Jenny A., Hauri H. P., Keller W. Characterization of cleavage and polyadenylation specificity factor and cloning of its 100-kilodalton subunit. Mol Cell Biol. 1994 Dec;14(12):8183–8190. doi: 10.1128/mcb.14.12.8183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jenny A., Minvielle-Sebastia L., Preker P. J., Keller W. Sequence similarity between the 73-kilodalton protein of mammalian CPSF and a subunit of yeast polyadenylation factor I. Science. 1996 Nov 29;274(5292):1514–1517. doi: 10.1126/science.274.5292.1514. [DOI] [PubMed] [Google Scholar]
  27. Keller W. No end yet to messenger RNA 3' processing! Cell. 1995 Jun 16;81(6):829–832. doi: 10.1016/0092-8674(95)90001-2. [DOI] [PubMed] [Google Scholar]
  28. Kokubu F., Hinds K., Litman R., Shamblott M. J., Litman G. W. Complete structure and organization of immunoglobulin heavy chain constant region genes in a phylogenetically primitive vertebrate. EMBO J. 1988 Jul;7(7):1979–1988. doi: 10.1002/j.1460-2075.1988.tb03036.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Larsson S., Svensson C., Akusjärvi G. Control of adenovirus major late gene expression at multiple levels. J Mol Biol. 1992 May 20;225(2):287–298. doi: 10.1016/0022-2836(92)90922-7. [DOI] [PubMed] [Google Scholar]
  30. Lassman C. R., Matis S., Hall B. L., Toppmeyer D. L., Milcarek C. Plasma cell-regulated polyadenylation at the Ig gamma 2b secretion-specific poly(A) site. J Immunol. 1992 Feb 15;148(4):1251–1260. [PubMed] [Google Scholar]
  31. Lassman C. R., Milcarek C. Regulated expression of the mouse gamma 2b Ig H chain gene is influenced by polyA site order and strength. J Immunol. 1992 Apr 15;148(8):2578–2585. [PubMed] [Google Scholar]
  32. Liu F. T., Albrandt K., Sutcliffe J. G., Katz D. H. Cloning and nucleotide sequence of mouse immunoglobulin epsilon chain cDNA. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7852–7856. doi: 10.1073/pnas.79.24.7852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. MacDonald M. H., Mogen B. D., Hunt A. G. Characterization of the polyadenylation signal from the T-DNA-encoded octopine synthase gene. Nucleic Acids Res. 1991 Oct 25;19(20):5575–5581. doi: 10.1093/nar/19.20.5575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Magor B. G., Wilson M. R., Miller N. W., Clem L. W., Middleton D. L., Warr G. W. An Ig heavy chain enhancer of the channel catfish Ictalurus punctatus: evolutionary conservation of function but not structure. J Immunol. 1994 Dec 15;153(12):5556–5563. [PubMed] [Google Scholar]
  35. Manley J. L. A complex protein assembly catalyzes polyadenylation of mRNA precursors. Curr Opin Genet Dev. 1995 Apr;5(2):222–228. doi: 10.1016/0959-437x(95)80012-3. [DOI] [PubMed] [Google Scholar]
  36. Manley J. L. Polyadenylation of mRNA precursors. Biochim Biophys Acta. 1988 May 6;950(1):1–12. doi: 10.1016/0167-4781(88)90067-x. [DOI] [PubMed] [Google Scholar]
  37. Manley J. L., Takagaki Y. The end of the message--another link between yeast and mammals. Science. 1996 Nov 29;274(5292):1481–1482. doi: 10.1126/science.274.5292.1481. [DOI] [PubMed] [Google Scholar]
  38. McDevitt M. A., Hart R. P., Wong W. W., Nevins J. R. Sequences capable of restoring poly(A) site function define two distinct downstream elements. EMBO J. 1986 Nov;5(11):2907–2913. doi: 10.1002/j.1460-2075.1986.tb04586.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. McGuire K. L., Duncan W. R., Tucker P. W. Phylogenetic conservation of immunoglobulin heavy chains: direct comparison of hamster and mouse Cmu genes. Nucleic Acids Res. 1985 Aug 12;13(15):5611–5628. doi: 10.1093/nar/13.15.5611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Milcarek C., Hall B. Cell-specific expression of secreted versus membrane forms of immunoglobulin gamma 2b mRNA involves selective use of alternate polyadenylation sites. Mol Cell Biol. 1985 Oct;5(10):2514–2520. doi: 10.1128/mcb.5.10.2514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Moore C. L., Sharp P. A. Accurate cleavage and polyadenylation of exogenous RNA substrate. Cell. 1985 Jul;41(3):845–855. doi: 10.1016/s0092-8674(85)80065-9. [DOI] [PubMed] [Google Scholar]
  42. Murthy K. G., Manley J. L. Characterization of the multisubunit cleavage-polyadenylation specificity factor from calf thymus. J Biol Chem. 1992 Jul 25;267(21):14804–14811. [PubMed] [Google Scholar]
  43. Oi V. T., Morrison S. L., Herzenberg L. A., Berg P. Immunoglobulin gene expression in transformed lymphoid cells. Proc Natl Acad Sci U S A. 1983 Feb;80(3):825–829. doi: 10.1073/pnas.80.3.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Ollo R., Auffray C., Morchamps C., Rougeon F. Comparison of mouse immunoglobulin gamma 2a and gamma 2b chain genes suggests that exons can be exchanged between genes in a multigenic family. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2442–2446. doi: 10.1073/pnas.78.4.2442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Patri S., Nau F. Isolation and sequence of a cDNA coding for the immunoglobulin mu chain of the sheep. Mol Immunol. 1992 Jul-Aug;29(7-8):829–836. doi: 10.1016/0161-5890(92)90120-m. [DOI] [PubMed] [Google Scholar]
  46. Perry R. P., Atchison M. L., Kelley D. E., Peterson M. L. Transcriptional and processing-level control of immunoglobulin gene expression. Ann N Y Acad Sci. 1988;546:25–33. doi: 10.1111/j.1749-6632.1988.tb21615.x. [DOI] [PubMed] [Google Scholar]
  47. Peterson M. L. Balanced efficiencies of splicing and cleavage-polyadenylation are required for mu-s and mu-m mRNA regulation. Gene Expr. 1992;2(4):319–327. [PMC free article] [PubMed] [Google Scholar]
  48. Peterson M. L., Bryman M. B., Peiter M., Cowan C. Exon size affects competition between splicing and cleavage-polyadenylation in the immunoglobulin mu gene. Mol Cell Biol. 1994 Jan;14(1):77–86. doi: 10.1128/mcb.14.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Peterson M. L., Gimmi E. R., Perry R. P. The developmentally regulated shift from membrane to secreted mu mRNA production is accompanied by an increase in cleavage-polyadenylation efficiency but no measurable change in splicing efficiency. Mol Cell Biol. 1991 Apr;11(4):2324–2327. doi: 10.1128/mcb.11.4.2324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Peterson M. L., Perry R. P. Regulated production of mu m and mu s mRNA requires linkage of the poly(A) addition sites and is dependent on the length of the mu s-mu m intron. Proc Natl Acad Sci U S A. 1986 Dec;83(23):8883–8887. doi: 10.1073/pnas.83.23.8883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Peterson M. L., Perry R. P. The regulated production of mu m and mu s mRNA is dependent on the relative efficiencies of mu s poly(A) site usage and the c mu 4-to-M1 splice. Mol Cell Biol. 1989 Feb;9(2):726–738. doi: 10.1128/mcb.9.2.726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Peterson M. L. Regulated immunoglobulin (Ig) RNA processing does not require specific cis-acting sequences: non-Ig RNA can be alternatively processed in B cells and plasma cells. Mol Cell Biol. 1994 Dec;14(12):7891–7898. doi: 10.1128/mcb.14.12.7891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Phillips C., Schimpl A., Dietrich-Goetz W., Clements J. B., Virtanen A. Inducible nuclear factors binding the IgM heavy chain pre-mRNA secretory poly(A) site. Eur J Immunol. 1996 Dec;26(12):3144–3152. doi: 10.1002/eji.1830261247. [DOI] [PubMed] [Google Scholar]
  54. Prescott J. C., Falck-Pedersen E. Varied poly(A) site efficiency in the adenovirus major late transcription unit. J Biol Chem. 1992 Apr 25;267(12):8175–8181. [PubMed] [Google Scholar]
  55. Proudfoot N. Poly(A) signals. Cell. 1991 Feb 22;64(4):671–674. doi: 10.1016/0092-8674(91)90495-k. [DOI] [PubMed] [Google Scholar]
  56. Rogers J., Early P., Carter C., Calame K., Bond M., Hood L., Wall R. Two mRNAs with different 3' ends encode membrane-bound and secreted forms of immunoglobulin mu chain. Cell. 1980 Jun;20(2):303–312. doi: 10.1016/0092-8674(80)90616-9. [DOI] [PubMed] [Google Scholar]
  57. Ross J. mRNA stability in mammalian cells. Microbiol Rev. 1995 Sep;59(3):423–450. doi: 10.1128/mr.59.3.423-450.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Rothnie H. M., Reid J., Hohn T. The contribution of AAUAAA and the upstream element UUUGUA to the efficiency of mRNA 3'-end formation in plants. EMBO J. 1994 May 1;13(9):2200–2210. doi: 10.1002/j.1460-2075.1994.tb06497.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Sanfaçon H., Brodmann P., Hohn T. A dissection of the cauliflower mosaic virus polyadenylation signal. Genes Dev. 1991 Jan;5(1):141–149. doi: 10.1101/gad.5.1.141. [DOI] [PubMed] [Google Scholar]
  60. Schwager J., Mikoryak C. A., Steiner L. A. Amino acid sequence of heavy chain from Xenopus laevis IgM deduced from cDNA sequence: implications for evolution of immunoglobulin domains. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2245–2249. doi: 10.1073/pnas.85.7.2245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Skolnik-David H., Moore C. L., Sharp P. A. Electrophoretic separation of polyadenylation-specific complexes. Genes Dev. 1987 Sep;1(7):672–682. doi: 10.1101/gad.1.7.672. [DOI] [PubMed] [Google Scholar]
  62. Steiner L. A. Immunoglobulin evolution, 30 years on. Glycobiology. 1996 Oct;6(7):649–656. doi: 10.1093/glycob/6.7.649. [DOI] [PubMed] [Google Scholar]
  63. Stumpf G., Domdey H. Dependence of yeast pre-mRNA 3'-end processing on CFT1: a sequence homolog of the mammalian AAUAAA binding factor. Science. 1996 Nov 29;274(5292):1517–1520. doi: 10.1126/science.274.5292.1517. [DOI] [PubMed] [Google Scholar]
  64. Takagaki Y., Manley J. L., MacDonald C. C., Wilusz J., Shenk T. A multisubunit factor, CstF, is required for polyadenylation of mammalian pre-mRNAs. Genes Dev. 1990 Dec;4(12A):2112–2120. doi: 10.1101/gad.4.12a.2112. [DOI] [PubMed] [Google Scholar]
  65. Takagaki Y., Ryner L. C., Manley J. L. Four factors are required for 3'-end cleavage of pre-mRNAs. Genes Dev. 1989 Nov;3(11):1711–1724. doi: 10.1101/gad.3.11.1711. [DOI] [PubMed] [Google Scholar]
  66. Takagaki Y., Seipelt R. L., Peterson M. L., Manley J. L. The polyadenylation factor CstF-64 regulates alternative processing of IgM heavy chain pre-mRNA during B cell differentiation. Cell. 1996 Nov 29;87(5):941–952. doi: 10.1016/s0092-8674(00)82000-0. [DOI] [PubMed] [Google Scholar]
  67. Thuresson A. C., Aström J., Aström A., Grönvik K. O., Virtanen A. Multiple forms of poly(A) polymerases in human cells. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):979–983. doi: 10.1073/pnas.91.3.979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Tsurushita N., Avdalovic N. M., Korn L. J. Regulation of differential processing of mouse immunoglobulin mu heavy-chain mRNA. Nucleic Acids Res. 1987 Jun 11;15(11):4603–4615. doi: 10.1093/nar/15.11.4603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Tsurushita N., Ho L., Korn L. J. Nuclear factors in B lymphoma enhance splicing of mouse membrane-bound mu mRNA in Xenopus oocytes. Science. 1988 Jan 29;239(4839):494–497. doi: 10.1126/science.3124268. [DOI] [PubMed] [Google Scholar]
  70. Tucker P. W., Slightom J. L., Blattner F. R. Mouse IgA heavy chain gene sequence: implications for evolution of immunoglobulin hinge axons. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7684–7688. doi: 10.1073/pnas.78.12.7684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Virtanen A., Sharp P. A. Processing at immunoglobulin polyadenylation sites in lymphoid cell extracts. EMBO J. 1988 May;7(5):1421–1429. doi: 10.1002/j.1460-2075.1988.tb02959.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Wahle E., Keller W. The biochemistry of polyadenylation. Trends Biochem Sci. 1996 Jul;21(7):247–250. [PubMed] [Google Scholar]
  73. Wahle E. Purification and characterization of a mammalian polyadenylate polymerase involved in the 3' end processing of messenger RNA precursors. J Biol Chem. 1991 Feb 15;266(5):3131–3139. [PubMed] [Google Scholar]
  74. Warr G. W., Magor K. E., Higgins D. A. IgY: clues to the origins of modern antibodies. Immunol Today. 1995 Aug;16(8):392–398. doi: 10.1016/0167-5699(95)80008-5. [DOI] [PubMed] [Google Scholar]
  75. Wels J. A., Word C. J., Rimm D., Der-Balan G. P., Martinez H. M., Tucker P. W., Blattner F. R. Structural analysis of the murine IgG3 constant region gene. EMBO J. 1984 Sep;3(9):2041–2046. doi: 10.1002/j.1460-2075.1984.tb02089.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Word C. J., White M. B., Kuziel W. A., Shen A. L., Blattner F. R., Tucker P. W. The human immunoglobulin C mu-C delta locus: complete nucleotide sequence and structural analysis. Int Immunol. 1989;1(3):296–309. doi: 10.1093/intimm/1.3.296. [DOI] [PubMed] [Google Scholar]
  77. Yan D. H., Weiss E. A., Nevins J. R. Identification of an activity in B-cell extracts that selectively impairs the formation of an immunoglobulin mu s poly(A) site processing complex. Mol Cell Biol. 1995 Apr;15(4):1901–1906. doi: 10.1128/mcb.15.4.1901. [DOI] [PMC free article] [PubMed] [Google Scholar]

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