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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2001 Jan 29;356(1405):53–60. doi: 10.1098/rstb.2000.0748

DNA polymerase iota and related rad30-like enzymes.

J P McDonald 1, A Tissier 1, E G Frank 1, S Iwai 1, F Hanaoka 1, R Woodgate 1
PMCID: PMC1087691  PMID: 11205331

Abstract

Until recently, the molecular mechanisms of translesion DNA synthesis (TLS), a process whereby a damaged base is used as a template for continued replication, was poorly understood. This area of scientific research has, however, been revolutionized by the finding that proteins long implicated in TLS are, in fact, DNA polymerases. Members of this so-called UmuC/DinB/Rev1/Rad30 superfamily of polymerases have been identified in prokaryotes, eukaryotes and archaea. Biochemical studies with the highly purified polymerases reveal that some, but not all, can traverse blocking lesions in template DNA. All of them share a common feature, however, in that they exhibit low fidelity when replicating undamaged DNA. Of particular interest to us is the Rad30 subfamily of polymerases found exclusively in eukaryotes. Humans possess two Rad30 paralogs, Rad30A and Rad30B. The RAD30A gene encodes DNA polymerase eta and defects in the protein lead to the xeroderma pigmentosum variant (XP-V) phenotype in humans. Very recently RAD30B has also been shown to encode a novel DNA polymerase, designated as Pol iota. Based upon in vitro studies, it appears that Pol iota has the lowest fidelity of any eukaryotic polymerase studied to date and we speculate as to the possible cellular functions of such a remarkably error-prone DNA polymerase.

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Selected References

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  1. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  2. Bridges B. A., Woodgate R. Mutagenic repair in Escherichia coli. X. The umuC gene product may be required for replication past pyrimidine dimers but not for the coding error in UV-mutagenesis. Mol Gen Genet. 1984;196(2):364–366. doi: 10.1007/BF00328073. [DOI] [PubMed] [Google Scholar]
  3. Bridges B. A., Woodgate R. Mutagenic repair in Escherichia coli: products of the recA gene and of the umuD and umuC genes act at different steps in UV-induced mutagenesis. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4193–4197. doi: 10.1073/pnas.82.12.4193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brotcorne-Lannoye A., Maenhaut-Michel G. Role of RecA protein in untargeted UV mutagenesis of bacteriophage lambda: evidence for the requirement for the dinB gene. Proc Natl Acad Sci U S A. 1986 Jun;83(11):3904–3908. doi: 10.1073/pnas.83.11.3904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bruck I., Woodgate R., McEntee K., Goodman M. F. Purification of a soluble UmuD'C complex from Escherichia coli. Cooperative binding of UmuD'C to single-stranded DNA. J Biol Chem. 1996 May 3;271(18):10767–10774. doi: 10.1074/jbc.271.18.10767. [DOI] [PubMed] [Google Scholar]
  6. Cleaver J. E., Carter D. M. Xeroderma pigmentosum variants: influence of temperature on DNA repair. J Invest Dermatol. 1973 Jan;60(1):29–32. doi: 10.1111/1523-1747.ep13069659. [DOI] [PubMed] [Google Scholar]
  7. Cordonnier A. M., Lehmann A. R., Fuchs R. P. Impaired translesion synthesis in xeroderma pigmentosum variant extracts. Mol Cell Biol. 1999 Mar;19(3):2206–2211. doi: 10.1128/mcb.19.3.2206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Diaz M., Flajnik M. F. Evolution of somatic hypermutation and gene conversion in adaptive immunity. Immunol Rev. 1998 Apr;162:13–24. doi: 10.1111/j.1600-065x.1998.tb01425.x. [DOI] [PubMed] [Google Scholar]
  9. Diaz M., Velez J., Singh M., Cerny J., Flajnik M. F. Mutational pattern of the nurse shark antigen receptor gene (NAR) is similar to that of mammalian Ig genes and to spontaneous mutations in evolution: the translesion synthesis model of somatic hypermutation. Int Immunol. 1999 May;11(5):825–833. doi: 10.1093/intimm/11.5.825. [DOI] [PubMed] [Google Scholar]
  10. Friedberg E. C., Feaver W. J., Gerlach V. L. The many faces of DNA polymerases: strategies for mutagenesis and for mutational avoidance. Proc Natl Acad Sci U S A. 2000 May 23;97(11):5681–5683. doi: 10.1073/pnas.120152397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gerlach V. L., Aravind L., Gotway G., Schultz R. A., Koonin E. V., Friedberg E. C. Human and mouse homologs of Escherichia coli DinB (DNA polymerase IV), members of the UmuC/DinB superfamily. Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):11922–11927. doi: 10.1073/pnas.96.21.11922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goodman M. F. Coping with replication 'train wrecks' in Escherichia coli using Pol V, Pol II and RecA proteins. Trends Biochem Sci. 2000 Apr;25(4):189–195. doi: 10.1016/s0968-0004(00)01564-4. [DOI] [PubMed] [Google Scholar]
  13. Harris R. S., Kong Q., Maizels N. Somatic hypermutation and the three R's: repair, replication and recombination. Mutat Res. 1999 Mar;436(2):157–178. doi: 10.1016/s1383-5742(99)00003-4. [DOI] [PubMed] [Google Scholar]
  14. Jacobs H., Fukita Y., van der Horst G. T., de Boer J., Weeda G., Essers J., de Wind N., Engelward B. P., Samson L., Verbeek S. Hypermutation of immunoglobulin genes in memory B cells of DNA repair-deficient mice. J Exp Med. 1998 Jun 1;187(11):1735–1743. doi: 10.1084/jem.187.11.1735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jeanmougin F., Thompson J. D., Gouy M., Higgins D. G., Gibson T. J. Multiple sequence alignment with Clustal X. Trends Biochem Sci. 1998 Oct;23(10):403–405. doi: 10.1016/s0968-0004(98)01285-7. [DOI] [PubMed] [Google Scholar]
  16. Johnson R. E., Kondratick C. M., Prakash S., Prakash L. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science. 1999 Jul 9;285(5425):263–265. doi: 10.1126/science.285.5425.263. [DOI] [PubMed] [Google Scholar]
  17. Johnson R. E., Prakash S., Prakash L. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Poleta. Science. 1999 Feb 12;283(5404):1001–1004. doi: 10.1126/science.283.5404.1001. [DOI] [PubMed] [Google Scholar]
  18. Johnson R. E., Prakash S., Prakash L. The human DINB1 gene encodes the DNA polymerase Poltheta. Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):3838–3843. doi: 10.1073/pnas.97.8.3838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Johnson R. E., Washington M. T., Prakash S., Prakash L. Fidelity of human DNA polymerase eta. J Biol Chem. 2000 Mar 17;275(11):7447–7450. doi: 10.1074/jbc.275.11.7447. [DOI] [PubMed] [Google Scholar]
  20. Kato T., Shinoura Y. Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light. Mol Gen Genet. 1977 Nov 14;156(2):121–131. doi: 10.1007/BF00283484. [DOI] [PubMed] [Google Scholar]
  21. 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. 1999 Jul 5;190(1):21–30. doi: 10.1084/jem.190.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kim S. R., Maenhaut-Michel G., Yamada M., Yamamoto Y., Matsui K., Sofuni T., Nohmi T., Ohmori H. Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13792–13797. doi: 10.1073/pnas.94.25.13792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kitagawa Y., Akaboshi E., Shinagawa H., Horii T., Ogawa H., Kato T. Structural analysis of the umu operon required for inducible mutagenesis in Escherichia coli. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4336–4340. doi: 10.1073/pnas.82.13.4336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Koffel-Schwartz N., Coin F., Veaute X., Fuchs R. P. Cellular strategies for accommodating replication-hindering adducts in DNA: control by the SOS response in Escherichia coli. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7805–7810. doi: 10.1073/pnas.93.15.7805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kulaeva O. I., Koonin E. V., McDonald J. P., Randall S. K., Rabinovich N., Connaughton J. F., Levine A. S., Woodgate R. Identification of a DinB/UmuC homolog in the archeon Sulfolobus solfataricus. Mutat Res. 1996 Oct 25;357(1-2):245–253. doi: 10.1016/0027-5107(96)00164-9. [DOI] [PubMed] [Google Scholar]
  26. Larimer F. W., Perry J. R., Hardigree A. A. The REV1 gene of Saccharomyces cerevisiae: isolation, sequence, and functional analysis. J Bacteriol. 1989 Jan;171(1):230–237. doi: 10.1128/jb.171.1.230-237.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lodwick D., Owen D., Strike P. DNA sequence analysis of the imp UV protection and mutation operon of the plasmid TP110: identification of a third gene. Nucleic Acids Res. 1990 Sep 11;18(17):5045–5050. doi: 10.1093/nar/18.17.5045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lodwick D., Strike P. Distribution of sequences homologous to the impCAB operon of TP110 among bacterial plasmids of different incompatibility groups. Mol Gen Genet. 1991 Sep;229(1):27–30. doi: 10.1007/BF00264209. [DOI] [PubMed] [Google Scholar]
  29. Maor-Shoshani A., Reuven N. B., Tomer G., Livneh Z. Highly mutagenic replication by DNA polymerase V (UmuC) provides a mechanistic basis for SOS untargeted mutagenesis. Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):565–570. doi: 10.1073/pnas.97.2.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Masutani C., Araki M., Yamada A., Kusumoto R., Nogimori T., Maekawa T., Iwai S., Hanaoka F. Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J. 1999 Jun 15;18(12):3491–3501. doi: 10.1093/emboj/18.12.3491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Masutani C., Kusumoto R., Iwai S., Hanaoka F. Mechanisms of accurate translesion synthesis by human DNA polymerase eta. EMBO J. 2000 Jun 15;19(12):3100–3109. doi: 10.1093/emboj/19.12.3100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Masutani C., Kusumoto R., Yamada A., Dohmae N., Yokoi M., Yuasa M., Araki M., Iwai S., Takio K., Hanaoka F. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature. 1999 Jun 17;399(6737):700–704. doi: 10.1038/21447. [DOI] [PubMed] [Google Scholar]
  33. McDonald J. P., Levine A. S., Woodgate R. The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism. Genetics. 1997 Dec;147(4):1557–1568. doi: 10.1093/genetics/147.4.1557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. McDonald J. P., Rapić-Otrin V., Epstein J. A., Broughton B. C., Wang X., Lehmann A. R., Wolgemuth D. J., Woodgate R. Novel human and mouse homologs of Saccharomyces cerevisiae DNA polymerase eta. Genomics. 1999 Aug 15;60(1):20–30. doi: 10.1006/geno.1999.5906. [DOI] [PubMed] [Google Scholar]
  35. McGregor W. G., Wei D., Maher V. M., McCormick J. J. Abnormal, error-prone bypass of photoproducts by xeroderma pigmentosum variant cell extracts results in extreme strand bias for the kinds of mutations induced by UV light. Mol Cell Biol. 1999 Jan;19(1):147–154. doi: 10.1128/mcb.19.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ogi T., Kato T., Jr, Kato T., Ohmori H. Mutation enhancement by DINB1, a mammalian homologue of the Escherichia coli mutagenesis protein dinB. Genes Cells. 1999 Nov;4(11):607–618. doi: 10.1046/j.1365-2443.1999.00289.x. [DOI] [PubMed] [Google Scholar]
  37. Ohashi E., Ogi T., Kusumoto R., Iwai S., Masutani C., Hanaoka F., Ohmori H. Error-prone bypass of certain DNA lesions by the human DNA polymerase kappa. Genes Dev. 2000 Jul 1;14(13):1589–1594. [PMC free article] [PubMed] [Google Scholar]
  38. Page R. D. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci. 1996 Aug;12(4):357–358. doi: 10.1093/bioinformatics/12.4.357. [DOI] [PubMed] [Google Scholar]
  39. Perry K. L., Elledge S. J., Mitchell B. B., Marsh L., Walker G. C. umuDC and mucAB operons whose products are required for UV light- and chemical-induced mutagenesis: UmuD, MucA, and LexA proteins share homology. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4331–4335. doi: 10.1073/pnas.82.13.4331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Perry K. L., Walker G. C. Identification of plasmid (pKM101)-coded proteins involved in mutagenesis and UV resistance. Nature. 1982 Nov 18;300(5889):278–281. doi: 10.1038/300278a0. [DOI] [PubMed] [Google Scholar]
  41. Raha M., Wang G., Seidman M. M., Glazer P. M. Mutagenesis by third-strand-directed psoralen adducts in repair-deficient human cells: high frequency and altered spectrum in a xeroderma pigmentosum variant. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2941–2946. doi: 10.1073/pnas.93.7.2941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Reuven N. B., Arad G., Maor-Shoshani A., Livneh Z. The mutagenesis protein UmuC is a DNA polymerase activated by UmuD', RecA, and SSB and is specialized for translesion replication. J Biol Chem. 1999 Nov 5;274(45):31763–31766. doi: 10.1074/jbc.274.45.31763. [DOI] [PubMed] [Google Scholar]
  43. Roush A. A., Suarez M., Friedberg E. C., Radman M., Siede W. Deletion of the Saccharomyces cerevisiae gene RAD30 encoding an Escherichia coli DinB homolog confers UV radiation sensitivity and altered mutability. Mol Gen Genet. 1998 Apr;257(6):686–692. doi: 10.1007/s004380050698. [DOI] [PubMed] [Google Scholar]
  44. Sedgwick S. G., Ho C., Woodgate R. Mutagenic DNA repair in enterobacteria. J Bacteriol. 1991 Sep;173(18):5604–5611. doi: 10.1128/jb.173.18.5604-5611.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Sedgwick S. G., Thomas S. M., Hughes V. M., Lodwick D., Strike P. Mutagenic DNA repair genes on plasmids from the 'pre-antibiotic era'. Mol Gen Genet. 1989 Aug;218(2):323–329. doi: 10.1007/BF00331285. [DOI] [PubMed] [Google Scholar]
  46. Smith B. T., Walker G. C. Mutagenesis and more: umuDC and the Escherichia coli SOS response. Genetics. 1998 Apr;148(4):1599–1610. doi: 10.1093/genetics/148.4.1599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Smith C. M., Koch W. H., Franklin S. B., Foster P. L., Cebula T. A., Eisenstadt E. Sequence analysis and mapping of the Salmonella typhimurium LT2 umuDC operon. J Bacteriol. 1990 Sep;172(9):4964–4978. doi: 10.1128/jb.172.9.4964-4978.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. 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. 1996 Apr 1;156(7):2642–2652. [PubMed] [Google Scholar]
  49. Spencer J. O., Dunn-Walters D. K. Somatic hypermutation and B-cell malignancies. J Pathol. 1999 Jan;187(2):158–163. doi: 10.1002/(SICI)1096-9896(199901)187:2<158::AID-PATH226>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
  50. Steinborn G. Uvm mutants of Escherichia coli K12 deficient in UV mutagenesis. I. Isolation of uvm mutants and their phenotypical characterization in DNA repair and mutagenesis. Mol Gen Genet. 1978 Sep 20;165(1):87–93. doi: 10.1007/BF00270380. [DOI] [PubMed] [Google Scholar]
  51. Svoboda D. L., Briley L. P., Vos J. M. Defective bypass replication of a leading strand cyclobutane thymine dimer in xeroderma pigmentosum variant cell extracts. Cancer Res. 1998 Jun 1;58(11):2445–2448. [PubMed] [Google Scholar]
  52. Svoboda D. L., Vos J. M. Differential replication of a single, UV-induced lesion in the leading or lagging strand by a human cell extract: fork uncoupling or gap formation. Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):11975–11979. doi: 10.1073/pnas.92.26.11975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Tang M., Bruck I., Eritja R., Turner J., Frank E. G., Woodgate R., O'Donnell M., Goodman M. F. Biochemical basis of SOS-induced mutagenesis in Escherichia coli: reconstitution of in vitro lesion bypass dependent on the UmuD'2C mutagenic complex and RecA protein. Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):9755–9760. doi: 10.1073/pnas.95.17.9755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Tang M., Pham P., Shen X., Taylor J. S., O'Donnell M., Woodgate R., Goodman M. F. Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis. Nature. 2000 Apr 27;404(6781):1014–1018. doi: 10.1038/35010020. [DOI] [PubMed] [Google Scholar]
  55. Tang M., Shen X., Frank E. G., O'Donnell M., Woodgate R., Goodman M. F. UmuD'(2)C is an error-prone DNA polymerase, Escherichia coli pol V. Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):8919–8924. doi: 10.1073/pnas.96.16.8919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Thomas S. M., Crowne H. M., Pidsley S. C., Sedgwick S. G. Structural characterization of the Salmonella typhimurium LT2 umu operon. J Bacteriol. 1990 Sep;172(9):4979–4987. doi: 10.1128/jb.172.9.4979-4987.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Tissier A., Frank E. G., McDonald J. P., Iwai S., Hanaoka F., Woodgate R. Misinsertion and bypass of thymine-thymine dimers by human DNA polymerase iota. EMBO J. 2000 Oct 2;19(19):5259–5266. doi: 10.1093/emboj/19.19.5259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Tissier A., McDonald J. P., Frank E. G., Woodgate R. poliota, a remarkably error-prone human DNA polymerase. Genes Dev. 2000 Jul 1;14(13):1642–1650. [PMC free article] [PubMed] [Google Scholar]
  59. Vaisman A., Masutani C., Hanaoka F., Chaney S. G. Efficient translesion replication past oxaliplatin and cisplatin GpG adducts by human DNA polymerase eta. Biochemistry. 2000 Apr 25;39(16):4575–4580. doi: 10.1021/bi000130k. [DOI] [PubMed] [Google Scholar]
  60. Wagner J., Gruz P., Kim S. R., Yamada M., Matsui K., Fuchs R. P., Nohmi T. The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol Cell. 1999 Aug;4(2):281–286. doi: 10.1016/s1097-2765(00)80376-7. [DOI] [PubMed] [Google Scholar]
  61. Walker G. C. Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev. 1984 Mar;48(1):60–93. doi: 10.1128/mr.48.1.60-93.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Wang Y. C., Maher V. M., Mitchell D. L., McCormick J. J. Evidence from mutation spectra that the UV hypermutability of xeroderma pigmentosum variant cells reflects abnormal, error-prone replication on a template containing photoproducts. Mol Cell Biol. 1993 Jul;13(7):4276–4283. doi: 10.1128/mcb.13.7.4276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Winter D. B., Phung Q. H., Umar A., Baker S. M., Tarone R. E., Tanaka K., Liskay R. M., Kunkel T. A., Bohr V. A., Gearhart P. J. Altered spectra of hypermutation in antibodies from mice deficient for the DNA mismatch repair protein PMS2. Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6953–6958. doi: 10.1073/pnas.95.12.6953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Wood E. R., Ghané F., Grogan D. W. Genetic responses of the thermophilic archaeon Sulfolobus acidocaldarius to short-wavelength UV light. J Bacteriol. 1997 Sep;179(18):5693–5698. doi: 10.1128/jb.179.18.5693-5698.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Woodgate R. A plethora of lesion-replicating DNA polymerases. Genes Dev. 1999 Sep 1;13(17):2191–2195. doi: 10.1101/gad.13.17.2191. [DOI] [PubMed] [Google Scholar]
  66. Woodgate R., Levine A. S. Damage inducible mutagenesis: recent insights into the activities of the Umu family of mutagenesis proteins. Cancer Surv. 1996;28:117–140. [PubMed] [Google Scholar]
  67. Yuan F., Zhang Y., Rajpal D. K., Wu X., Guo D., Wang M., Taylor J. S., Wang Z. Specificity of DNA lesion bypass by the yeast DNA polymerase eta. J Biol Chem. 2000 Mar 17;275(11):8233–8239. doi: 10.1074/jbc.275.11.8233. [DOI] [PubMed] [Google Scholar]
  68. Yélamos J., Klix N., Goyenechea B., Lozano F., Chui Y. L., González Fernández A., Pannell R., Neuberger M. S., Milstein C. Targeting of non-Ig sequences in place of the V segment by somatic hypermutation. Nature. 1995 Jul 20;376(6537):225–229. doi: 10.1038/376225a0. [DOI] [PubMed] [Google Scholar]

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