Skip to main content
NCBI home page
Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2003 Jan 15;284(1):3–14. doi: 10.1016/0027-5107(92)90020-3

Recombination and gene conversion

FE Würgler a,b,a
PMCID: PMC7131386  PMID: 1279392

Abstract

Recombination is an important aspect of DNA metabolism. It leads to rearrangements of DNA sequences within genomes. Such genome rearrangements seem to be ubiquitous, since they play a role in evolution, human health and biotechnology. In medicine one important aspect of recombination is its role as one possible step in the multistep process of carcinogenesis. Since recombination may occur as a cellular response to DNA damage, the protection of cells from recombination-inducing agents, so-called recombinagen, should eliminate possible deleterious effects resulting from damage-induced DNA recombination. During the last few years, the awareness of the importance of recombination phenomena has substantially increased and the development of assay systems detecting recombinagens has progressed. The need for considering recombinagenic effects as a safety aspect of chemicals has gained ground in the field of genetic toxicology. This paper summarizes present knowledge concerning the occurence, inducibility, detection and toxicological interpretation of DNA recombination.

Keywords: Recombination, Gene conversion

References

  1. Alt F.W., Blackwell T.K., Yancopoulos G.D. Development of the primary antibody repertoire. Science. 1987;238:1079–1094. doi: 10.1126/science.3317825. [DOI] [PubMed] [Google Scholar]
  2. Amor M., Parker K.L., Globerman H., New M.I., White P.C. Vol. 85. 1988. Mutation in the CYP21B gene (Ile-172-Asn) causes steroid 21-hydroxylase deficiency; pp. 1600–1604. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ayares D., Chekuri L., Song K.Y., Kucherlapati R. Vol. 83. 1986. Sequence homology requirements for intermolecular recombination in mammalian cells; pp. 5199–5203. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Becker H.J. Mitotic recombination. In: Ashburner M., Novitski E., editors. Vol. 1c. Academic Press; New York: 1976. pp. 1020–1087. (Genetics and Biology of Drosophila). [Google Scholar]
  5. Bhattacharyya N.P., Maher V.M., McCormick J.J. Effect of nucleotide excision repair in human cells on intrachromosomal homologous recombination induced by UV and 1-nitropyrene. Mol. Cell. Biol. 1990;10:3945–3951. doi: 10.1128/mcb.10.8.3945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bishop J.M. Molecular themes in oncogenesis. Cell. 1991;64:235–248. doi: 10.1016/0092-8674(91)90636-d. [DOI] [PubMed] [Google Scholar]
  7. Blackburn E. Developmentally controlled DNA excision in cilates. Trends Genet. 1987;3:235–236. [Google Scholar]
  8. Bridges B.A., Penn A., Hansen E.S., Wakabayashi K. Report of ICPEMC Subcommittee 7/1: The possible involvement of somatic mutations in the development of atherosclerotic plaques. Mutation Res. 1990;239:143–188. [PubMed] [Google Scholar]
  9. Brown W.R.A., MacKinnon P.J., Villasante A., Spurr N., Buckle V.J., Dobson M.J. Structure and polymorphism of human telomere-associated DNA. Cell. 1990;63:119–132. doi: 10.1016/0092-8674(90)90293-n. [DOI] [PubMed] [Google Scholar]
  10. Brunier D., Michel B., Ehrlich S.D. Copy choice illegitimate DNA recombination. Cell. 1988;52:883–892. doi: 10.1016/0092-8674(88)90430-8. [DOI] [PubMed] [Google Scholar]
  11. Cavenee W., Dryza T.P., Philips R.A., Benedict W.F., Godbout R., Gallie L., Murphree A.L. Expression of recessive alleles by chromosomal mechanisms in retinoblastoma. Nature (London) 1983;305:779–784. doi: 10.1038/305779a0. [DOI] [PubMed] [Google Scholar]
  12. Copland N.G., Hutchinson K.W., Jenkins N.A. Excision of the DBA ectopic provirus in dilute coat-color revertants of mice occures by homologous recombination involving the viral LTRs. Cell. 1983;33:379–387. doi: 10.1016/0092-8674(83)90419-1. [DOI] [PubMed] [Google Scholar]
  13. Covarrubias L., Nishida Y., Terao M., D'Eustachio P., Mintz B. Cellular DNA rearrangements and early developmental arrest caused by DNA insertion in transgenic mouse embryos. Mol. Cell. Biol. 1987;7:2243–2247. doi: 10.1128/mcb.7.6.2243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Darras B.T., Francke U. A partial deletion of the muscular dystrophy gene transmitted twice by an unaffected male. Nature (London) 1987;329:556–558. doi: 10.1038/329556a0. [DOI] [PubMed] [Google Scholar]
  15. de Zamaroczy M., Faugeron-Fonty G., Bernardi G. Excision sequences in the mitochondrial genome of yeast. Gene. 1983;21:193–202. doi: 10.1016/0378-1119(83)90002-1. [DOI] [PubMed] [Google Scholar]
  16. Engler P., Strob U. Immunoglobulin gene rearrangement. In: Kucherlapati R., Smith G.R., editors. Genetic Recombination. Am. Soc. Microbiology; Washington, DC: 1988. pp. 667–700. [Google Scholar]
  17. Fahrig R., Neuhäuser-Klaus A. Similar pigmentation characteristics in the specific-locus and the mammalian spot test. J. Hered. 1985;76:421–426. doi: 10.1093/oxfordjournals.jhered.a110137. [DOI] [PubMed] [Google Scholar]
  18. Favor J., Strauss P.G., Erfle V. Molecular characterization of a radiation-induced reverse mutation at the dilute locus in the mouse. Genet. Res. Camb. 1987;50:219–223. doi: 10.1017/s0016672300023739. [DOI] [PubMed] [Google Scholar]
  19. Fearon E.R., Vogelstein B. A genetic model for colorectal tumorigenesis. Cell. 1990;61:759–767. doi: 10.1016/0092-8674(90)90186-i. [DOI] [PubMed] [Google Scholar]
  20. Festa R.S., Meadows A.T., Boshes R.A. Leukemia in a black child with Bloom's syndrome. Somatic recombination as a possible mechanism for neoplasia. Cancer. 1979;44:1507–1510. doi: 10.1002/1097-0142(197910)44:4<1507::aid-cncr2820440448>3.0.co;2-a. [DOI] [PubMed] [Google Scholar]
  21. Gellert M., Nash H. Communication between segments of DNA during site-specific recombination. Nature (London) 1987;325:401–404. doi: 10.1038/325401a0. [DOI] [PubMed] [Google Scholar]
  22. Gilman J.G. The 12.6 kilobase DNA deletion in Dutch beta-thalassemia. Br. J. Haematol. 1987;67:369–372. doi: 10.1111/j.1365-2141.1987.tb02360.x. [DOI] [PubMed] [Google Scholar]
  23. Giroux C.N. Chromosome synapsis and meiotic recombination. In: Kucherlapati R., Smith G.R., editors. Genetic Recombination. Am. Soc. Microbiology; Washington, DC: 1988. pp. 465–496. [Google Scholar]
  24. Greider C.W., Blackburn E.H. Telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature (London) 1989;337:331–337. doi: 10.1038/337331a0. [DOI] [PubMed] [Google Scholar]
  25. Hall J.G. Review and hypothesis: Somatic mosaicism: Observations related to clinical genetics. Am. J. Hum. Genet. 1988;43:355–362. [PMC free article] [PubMed] [Google Scholar]
  26. Hastings P.J. Conversion events in fungi. In: Kucherlapati R., Smith G.R., editors. Genetic Recombination. Am. Soc. Microbiology; Washington, DC: 1988. pp. 397–428. [Google Scholar]
  27. Heim R.A., Lench N.J., Swift M. Heterozygous manifestations in human cancer-prone syndromes. Mutation Res. 1992;284:25–36. doi: 10.1016/0027-5107(92)90022-t. [DOI] [PubMed] [Google Scholar]
  28. Higashi Y., Tanae A., Inoue H., Fujii-Kuriyama Y. Evidence for frequent gene conversion in the steroid 21-hydroxylase P-450(C21) gene: Implications for steroid 21-hydroxylase deficiency. Am. J. Hum. Genet. 1988;42:017–025. [PMC free article] [PubMed] [Google Scholar]
  29. Hoffmann G. Bacterial assays for recombinagens. Mutation Res. 1992;284:125–146. doi: 10.1016/0027-5107(92)90028-z. [DOI] [PubMed] [Google Scholar]
  30. Hunt R.H. Somatic recombination events in mosquitoes: three different karyotypes observed in the ovarian nurse cells of individual Anopheles gambiae s.str. J. Hered. 1987;78:41–43. [Google Scholar]
  31. Iwasato T., Shimizu A., Honjo T., Yamagishi H. Circular DNA is excised by immunoglobulin class switch recombination. Cell. 1990;62:143–149. doi: 10.1016/0092-8674(90)90248-d. [DOI] [PubMed] [Google Scholar]
  32. Karsten W., Kryspin-Sorensen I. Penetrance and low concordance in monozygotic twins in disease: Are they the result of alterations in somatic genomes? Mol. Reprod. Dev. 1988;1:63–75. doi: 10.1002/mrd.1080010110. [DOI] [PubMed] [Google Scholar]
  33. Kenne K. DNA interacting proteins in normal and chromosomally unstable mammalian cells. Thesis. 1988 Stockholm, ISBN 91-7900-505-5. [Google Scholar]
  34. Kenne K., Ljungquist S. A DNA-recombinogenic activity in human cells. Nucleic Acids Res. 1984;12:3057–3068. doi: 10.1093/nar/12.7.3057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kenne K., Ljungquist S. RecA-like activity in mammalian cell extracts of different origin. Mutation Res. 1987;184:229–236. doi: 10.1016/0167-8817(87)90021-6. [DOI] [PubMed] [Google Scholar]
  36. Kew O.M., Nottay B.K. In: Modern Approaches to Vaccines. Chanock R., Lerner R., editors. Cold Spring Harbor Laboratory; Cold Spring Harbor, NY: 1984. pp. 357–362. [Google Scholar]
  37. King A.M.Q. RNA viruses do it. Trends Genet. 1987;3:60–61. [Google Scholar]
  38. King A.M.Q., McCahon D., Slade W.R., Newman J.W.L. Recombination in RNA. Cell. 1982;29:921–928. doi: 10.1016/0092-8674(82)90454-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kirkwood T.B.L. DNA, mutations and ageing. Mutation Res. 1989;219:1–8. doi: 10.1016/0921-8734(89)90035-0. [DOI] [PubMed] [Google Scholar]
  40. Kleckner N. Transposable elements in prokaryotes. Annu. Rev. Genet. 1981;15:341–404. doi: 10.1146/annurev.ge.15.120181.002013. [DOI] [PubMed] [Google Scholar]
  41. Kucherlapati R.S., Spencer J., Moore P.D. Homologous recombination catalyzed by human cell extracts. Mol. Cell. Biol. 1985;5:714–720. doi: 10.1128/mcb.5.4.714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kuhn E.M. Nonrandom localization of mitotic crossing-over in Bloom's syndrome. Genetics. 1974;77:s37–s38. [Google Scholar]
  43. Langlois S., Kastelein J.J.P., Hayden M.R. Characterization of six partial deletions in the low-density-lipoprotein (LDL) receptor gene causing familial hypercholesterolemia (FH) Am. J. Hum. Genet. 1988;43:60–68. [PMC free article] [PubMed] [Google Scholar]
  44. Lehrman M.A., Schneider W.J., Suedhof T.C., Brown M.S., Goldstein J.L., Russell D.W. Mutation in LDL receptor: Alu-Alu recombination deletes exons encoding transmembrane and cytoplasmic domains. Science. 1985;227:140–146. doi: 10.1126/science.3155573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Lehrman M.A., Russell D.W., Goldstein J.L., Brown M.S. Vol. 83. 1986. Exon-Alu recombination deletes 5 kilobases from the low density lipoprotein receptor gene, producing a null phenotype in familial hypercholesterolemia; pp. 3679–3683. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Lehrman M.A., Goldstein J.L., Russell D.W., Brown M.S. Duplication of seven exons in LDL receptor gene caused by Alu-Alu recombination in a subject with familial hypercholesterolemia. Cell. 1987;48:827–835. doi: 10.1016/0092-8674(87)90079-1. [DOI] [PubMed] [Google Scholar]
  47. Lieberman S.W., Symington L.S., Petes T.D. Mitotic recombination within the centromere of a yeast chromosome. Science. 1988;241:1074–1077. doi: 10.1126/science.3137657. [DOI] [PubMed] [Google Scholar]
  48. Liskay R.M., Stachelek J.L. Vol. 83. 1986. Information transfer between duplicated chromosomal sequences in mammalian cells involving contigous regions of DNA; pp. 1802–1806. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Liskay R.M., Letsou A., Stachelek J.L. Homology requirement for efficient gene conversion between duplicated chromosomal sequences in mammalian cells. Genetics. 1987;115:161–167. doi: 10.1093/genetics/115.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Littlefield L.G., Joiner E.E. Analysis of chromosome aberrations in lymphocytes of long-term heavy smokers. Mutation Res. 1986;170:145–150. doi: 10.1016/0165-1218(86)90028-5. [DOI] [PubMed] [Google Scholar]
  51. Low K.B., Porter R.D. Modes of gene transfer and recombination in bacteria. Annu. Rev. Genet. 1978;12:249–287. doi: 10.1146/annurev.ge.12.120178.001341. [DOI] [PubMed] [Google Scholar]
  52. Mahajan S.K. Pathways of homologous recombination in Escherichia coli. In: Kucherlapati R., Smith G.R., editors. Genetic Recombination. Am. Soc. Microbiology; Washington, DC: 1988. pp. 87–140. [Google Scholar]
  53. Malissen M., McCoy C., Blanc D., Trucy J., DeVaux C., Schmitt-Verhulst A.M., Fitch F. Direct evidence for chromosomal inversion during T-cell receptor beta-gene rearrangements. Nature (London) 1986;319:28–33. doi: 10.1038/319028a0. [DOI] [PubMed] [Google Scholar]
  54. Marrak P., Kappler J. The T cell receptor. Science. 1987;238:1073–1078. doi: 10.1126/science.3317824. [DOI] [PubMed] [Google Scholar]
  55. Marshall C.J. Tumor suppressor genes. Cell. 1991;64:313–326. doi: 10.1016/0092-8674(91)90641-b. [DOI] [PubMed] [Google Scholar]
  56. 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. 1990;62:135–142. doi: 10.1016/0092-8674(90)90247-c. [DOI] [PubMed] [Google Scholar]
  57. Mohrenweiser H.W., Jones I.M. Review of the molecular characteristics of gene mutations of the germline and somatic cells of the human. Mutation Res. 1990;231:87–108. doi: 10.1016/0027-5107(90)90179-8. [DOI] [PubMed] [Google Scholar]
  58. Moulding C., Rappoport A., Goldman P., Battey J., Lenoir G.M., Leder P. Structural analysis of both products of a reciprocal translocation between c-myc and immunoglobulin loci in Burkitt's lymphoma. Nucleic Acids Res. 1985;13:2141–2152. doi: 10.1093/nar/13.6.2141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Mulkvag S.L., Roberts R., Schneider M.D. Cellular oncogenes in cardiovascular disease. J. Mol. Cell. Cardiol. 1988;20:657–662. doi: 10.1016/s0022-2828(88)80123-8. [DOI] [PubMed] [Google Scholar]
  60. Müller H. Recessively inherited deficiencies predisposing to cancer. Anticancer Res. 1990;10:513–518. [PubMed] [Google Scholar]
  61. Müller H., Scott R. Hereditary conditions in which the loss of heterozygosity may be important. Mutation Res. 1992;284:15–24. doi: 10.1016/0027-5107(92)90021-s. [DOI] [PubMed] [Google Scholar]
  62. Muller H.J. Our load of mutations. Am. J. Hum. Genet. 1950;2:111–176. [PMC free article] [PubMed] [Google Scholar]
  63. Myerowitz R., Hogikyan N.D. A deletion involving Alu sequences in the beta-hexosaminidase alpha-chain gene of French Canadians with Tay-Sachs disease. J. Biol. Chem. 1987;262:15396–15399. [PubMed] [Google Scholar]
  64. Nöthiger R., Dübendorfer A. Somatic crossing-over in the housefly. Mol. Gen. Genet. 1971;112:9–13. doi: 10.1007/BF00266927. [DOI] [PubMed] [Google Scholar]
  65. Obe G., Herha J. Chromosomal aberrations in heavy smokers. Hum. Genet. 1978;41:259–263. doi: 10.1007/BF00284759. [DOI] [PubMed] [Google Scholar]
  66. Okamoto M., Sasaki M., Sugio K., Sato C., Iwama T., Ikeuchi T., Tonomura A., Sasazuki T. Loss of constitutional heterozygosity in colon carcinoma from patients with familial polyposis coli. Nature (London) 1988;331:273–277. doi: 10.1038/331273a0. [DOI] [PubMed] [Google Scholar]
  67. Ottolenghi S., Gigglioni B. The deletion in a type of δ°-β°-thalassaemia begins in an inverted AluI repeat. Nature (London) 1982;300:770–771. doi: 10.1038/300770a0. [DOI] [PubMed] [Google Scholar]
  68. Penn A., Garte S.J., Warren L., Nesta D., Mindich B. Vol. 83. 1986. Transforming gene in human arteriosclerotic plaque DNA; pp. 7951–7955. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Plasterk R.H., Simon M.I., Barbour A.G. Transposition of structural genes to an expression sequence on a linear plasmid causes antigenic variation in the bacterium Borellia hersii. Nature (London) 1985;318:257–263. doi: 10.1038/318257a0. [DOI] [PubMed] [Google Scholar]
  70. Porter R.D. Mode of gene transfer in bacteria. In: Kucherlapati R., Smith G.R., editors. Genetic Recombination. Am. Soc. Microbiology; Washington, DC: 1988. pp. 1–41. [Google Scholar]
  71. Quertermous T., Strauss W., Murre C., Dialynas D.P., Strominger J.L., Seidman J.G. Human T-cell gamma genes contain N segments and have marked junctional variability. Nature (London) 1986;322:184–187. doi: 10.1038/322184a0. [DOI] [PubMed] [Google Scholar]
  72. Reynaud C.A., Dahan A., Weill J.C. A gene conversion program during the ontogenesis of chicken B cells. Trends Genet. 1987;3:248–251. [Google Scholar]
  73. Rubnitz J., Subramani S. The minimum amount of homology required for homologous recombination in mammalian cells. Mol. Cell. Biol. 1984;4:2253–2258. doi: 10.1128/mcb.4.11.2253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Simon P., Decoster C., Brocas H., Schwers J., Vassart G. Absence of human chorionic somatomammotropin during pregnancy associated with two types of gene deletion. Hum. Genet. 1986;74:235–238. doi: 10.1007/BF00282540. [DOI] [PubMed] [Google Scholar]
  75. Singer B.S., Gold L., Gauss P., Doherty D.H. Determination of the amount of homology required for recombination in bacteriophage T4. Cell. 1982;31:25–33. doi: 10.1016/0092-8674(82)90401-9. [DOI] [PubMed] [Google Scholar]
  76. Sobels F.H. Studies on the mutagenic action of formaldehyde in Drosophila. II. The production of mutations in females and the induction of crossing-over. Z. Indukt. Abstamm. Vererb. Lehre. 1956;87:743–752. doi: 10.1007/BF00308508. [DOI] [PubMed] [Google Scholar]
  77. Sobels F.H. The possible role of peroxides in radiation and chemical mutagenesis in Drosophila. In: de Hevesy G.C., Forssberg A.G., Abbatt J.D., editors. Vol. 1. Oliver and Boyd; Edinburgh: 1957. pp. 449–456. (Advances in Radiobiology). [Google Scholar]
  78. Stern C. Somatic crossing-over and segregation in Drosophila melanogaster. Genetics. 1936;21:625–730. doi: 10.1093/genetics/21.6.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Stoye J.P., Fenner S., Greenoak G.E., Moran C., Coffin J.M. Role of endogenous retrovirus as mutagens: The hairless mutation of mice. Cell. 1988;54:383–391. doi: 10.1016/0092-8674(88)90201-2. [DOI] [PubMed] [Google Scholar]
  80. Strathern J.N. Control and execution of homotallic switching in Saccharomyces cerevisiae. In: Kucherlapati R., Smith G.R., editors. Genetic Recombination. Am. Soc. Microbiology; Washington, DC: 1988. pp. 445–464. [Google Scholar]
  81. Subramani S., Seaton B.L. Homologous recombination in mitotically dividing mammalian cells. In: Kucherlapati R.K., Smith G.R., editors. Genetic Recombination. Am. Soc. Microbiology; Washington, DC: 1988. pp. 549–574. [Google Scholar]
  82. Symington L.S., Petes T.D. Meiotic recombination within the centromere of a yeast chromosome. Cell. 1988;52:237–240. doi: 10.1016/0092-8674(88)90512-0. [DOI] [PubMed] [Google Scholar]
  83. Szostak J.W. Telomerase: The beginning of the ends. Nature (London) 1989;337:303–304. doi: 10.1038/337303a0. [DOI] [PubMed] [Google Scholar]
  84. Szostak J.W., Orr-Weaver T.L., Rothstein R.J., Stahl F.H. The double strand break repair model for recombination. Cell. 1983;33:25–35. doi: 10.1016/0092-8674(83)90331-8. [DOI] [PubMed] [Google Scholar]
  85. Temin H.M. Sex and recombination in retroviruses. Trends Genet. 1991;7:71–74. doi: 10.1016/0168-9525(91)90272-R. [DOI] [PubMed] [Google Scholar]
  86. Therman E., Kuhn E.M. Cytological demonstration of mitotic crossing-over in man. Cytogenet. Cell. Genet. 1976;17:245–267. doi: 10.1159/000130721. [DOI] [PubMed] [Google Scholar]
  87. Thompson C.B., Neiman P.E. Somatic diversification of the chicken immunoglobulin light chain gene is limited to the rearranged variable gene segment. Cell. 1987;48:369–378. doi: 10.1016/0092-8674(87)90188-7. [DOI] [PubMed] [Google Scholar]
  88. Traverse K.L., Pardue M.L. Vol. 85. 1988. A spontaneous opened ring chromosome of Drosophila melanogaster has acquired He-T DNA sequences at both new telomeres; pp. 8116–8120. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Vig B.K. Soybean (Glycine max (L.) merill) as a short-term assay for study of environmental mutagens. A report of the U.S. Environmental Protection Agency Gene-Tox Program. Mutation Res. 1982;99:339–347. doi: 10.1016/0165-1110(82)90050-1. [DOI] [PubMed] [Google Scholar]
  90. Vogel E.K. Tests for recombinagens in somatic cells of Drosophila. Mutation Res. 1992;284:159–175. doi: 10.1016/0027-5107(92)90030-6. [DOI] [PubMed] [Google Scholar]
  91. Vogel F. Vol. 205. 1979. Our load of mutation: reappraisal of an old problem; pp. 77–90. (Proc. R. Soc. London B). [DOI] [PubMed] [Google Scholar]
  92. Wasmuth J.J., Hall L.V. Genetic demonstration of mitotic recombination in cultured Chinese hamster cell hybrids. Cell. 1984;36:697–707. doi: 10.1016/0092-8674(84)90350-7. [DOI] [PubMed] [Google Scholar]
  93. Watt V.M., Ingles C.J., Urden M.S., Rutter W.J. Vol. 82. 1985. Homology requirements for recombination in Escherichia coli; pp. 4768–4772. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Würgler F.E., Vogel E.W. In vivo mutagenicity testing using somatic cells of Drosophila melanogaster. In: de Serres F.J., editor. Vol. 10. Plenum; New York: 1986. pp. 1–72. (Chemical Mutagens, Principles and Methods for their Detection). [Google Scholar]
  95. Zimmermann F.K. Tests for recombinagens in fungi. Mutation Res. 1992;284:147–158. doi: 10.1016/0027-5107(92)90029-2. [DOI] [PubMed] [Google Scholar]
  96. Zimmermann F.K., von Borstel R.C., von Halle E.S., Perry J.M., Zetterberg G., Siebert D., Barale R., Loprieno N. Testing of chemicals for genetic activity with Saccharomyces cerevisiae: a report of the U.S. Environmental Protection Agency Gene-Tox Program. Mutation Res. 1984;133:199–244. doi: 10.1016/0165-1110(84)90017-4. [DOI] [PubMed] [Google Scholar]

Articles from Mutation Research are provided here courtesy of Elsevier

RESOURCES