1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biochemistry
  4. Volume 78, 2009
  5. Article

Annual Review of Biochemistry

Volume 78, 2009

A Journey in the World of DNA Rings and Beyond

Abstract

I was born in China and would have remained there but for the tumultuous events that led many of my generation to the United States for graduate studies. Norman Davidson introduced me to DNA when I became a postdoctoral fellow in his group at the California Institute of Technology in 1964, and a fortuitous conversation there ignited my interest in DNA ring formation, which later led me to study different topological forms of DNA rings—catenanes, knots, and supercoils. In 1968, a chance observation led me to identify a new enzyme capable of converting one DNA ring form to another, an enzyme now known as a DNA topoisomerase. My interest in DNA rings and DNA topoisomerases continued throughout my years at the University of California, Berkeley, and Harvard. The fascinating ability of the topoisomerases in passing DNA strands or double helices through one another and their importance in cellular processes have kept me and many others excited in their studies.

Keyword(s): Autobiography, catenanes, knots, mammalian top mutants, supercoils, topoisomerase, topoisomerase-targeting drugs
Loading

Article metrics loading...

/content/journals/10.1146/annurev.biochem.78.030107.090101
2009-07-07
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/biochem/78/1/annurev.biochem.78.030107.090101.html?itemId=/content/journals/10.1146/annurev.biochem.78.030107.090101&mimeType=html&fmt=ahah

Literature Cited

  1. Hershey AD, Burgi E, Ingraham L. 1.  1963. Cohesion of DNA molecules isolated from phage lambda. Proc. Natl. Acad. Sci. USA 49:748–55 [Google Scholar]
  2. Strack HB, Kaiser AD. 2.  1965. On the structure of the ends of lambda DNA. J. Mol. Biol. 23:36–49 [Google Scholar]
  3. Wang JC, Davidson N. 3.  1966. Thermodynamic and kinetic studies on the interconversion between the linear and circular forms of phage lambda DNA. J. Mol. Biol. 15:111–23 [Google Scholar]
  4. Wang JC, Davidson N. 4.  1966. On the probability of ring closure of lambda DNA. J. Mol. Biol. 19:469–82 [Google Scholar]
  5. Vinograd J, Lebowitz J, Radloff R, Watson R, Laipis P. 5.  1965. The twisted circular form of polyoma viral DNA. Proc. Natl. Acad. Sci. USA 53:1104–11 [Google Scholar]
  6. Wang JC, Schwartz H. 6.  1967. Noncomplementarity in base sequences between the cohesive ends of coliphages 186 and λ and the formation of interlocked rings between the two DNA's. Biopolymers 5:953–66 [Google Scholar]
  7. Hudson B, Vinograd J. 7.  1969. Catenated circular DNA molecules in HeLa cell mitochondria. Nature 221:332–37 [Google Scholar]
  8. Olivera BM, Lehman IR. 8.  1967. Diphosphopyridine nucleotide: a cofactor for the polynucleotide-joining enzyme from Escherichia coli. Proc. Natl. Acad. Sci. USA 57:1700–4 [Google Scholar]
  9. Wang JC. 9.  1969. Variation of the average rotational angle of the DNA helix and the superhelical turns of covalently closed cyclic λ DNA. J. Mol. Biol. 43:25–39 [Google Scholar]
  10. Wang JC. 10.  1974. The degree of unwinding of the DNA helix by ethidium. I. Titration of twisted PM2 DNA molecules in alkaline cesium chloride density gradients. J. Mol. Biol. 89:783–801 [Google Scholar]
  11. Wang JC. 11.  1971. Unwinding of DNA by actinomycin D binding. Biochim. Biophys. Acta 232:246–51 [Google Scholar]
  12. Saucier JM, Wang JC. 12.  1972. Angular alteration of the DNA helix by E. coli RNA polymerase. Nat. New Biol. 239:167–70 [Google Scholar]
  13. Hsieh T, Wang JC. 13.  1978. Physicochemical studies on interactions between DNA and RNA polymerase. Ultraviolet absorption measurements. Nucleic Acids Res. 5:3337–45 [Google Scholar]
  14. Wang JC, Barkley MD, Bourgeois S. 14.  1974. Measurements of unwinding of lac operator by repressor. Nature 251:247–49 [Google Scholar]
  15. Botchan P, Wang JC, Echols H. 15.  1973. Effect of circularity and superhelicity on transcription from bacteriophage λ DNA. Proc. Natl. Acad. Sci. USA 70:3077–81 [Google Scholar]
  16. Wang JC. 16.  1974. Interactions between twisted DNAs and enzymes: the effects of superhelical turns. J. Mol. Biol. 87:797–816 [Google Scholar]
  17. Wang JC. 17.  1969. Degree of superhelicity of covalently closed cyclic DNAs from Escherichia coli. J. Mol. Biol. 43:263–72 [Google Scholar]
  18. Dulbecco R, Vogt M. 18.  1963. Evidence for a ring structure of polyoma virus DNA. Proc. Natl. Acad. Sci. USA 50:236–43 [Google Scholar]
  19. Weil R, Vinograd J. 19.  1963. The cyclic helix and cyclic coil forms of polyoma viral DNA. Proc. Natl. Acad. Sci. USA 50:730–38 [Google Scholar]
  20. Tomizawa JI, Ogawa T. 20.  1968. Replication of phage lambda DNA. Cold Spring Harb. Symp. Quant. Biol. 33:533–51 [Google Scholar]
  21. Wang JC. 21.  1971. Interaction between DNA and an Escherichia coli protein ω. J. Mol. Biol. 55:523–33 [Google Scholar]
  22. Depew RE, Liu LF, Wang JC. 22.  1978. Conformational fluctuations of DNA helix. J. Biol. Chem. 253:511–18 [Google Scholar]
  23. Liu LF, Depew RE, Wang JC. 23.  1976. Knotted single-stranded DNA rings: a novel topological isomer of circular single-stranded DNA formed by treatment with Escherichia coli ω protein. J. Mol. Biol. 106:439–52 [Google Scholar]
  24. Liu LF, Perkocha L, Calendar R, Wang JC. 24.  1981. Knotted DNA from bacteriophage capsids. Proc. Natl. Acad. Sci. USA 78:5498–502 [Google Scholar]
  25. Shaw S, Wang JC. 25.  1993. Knotting of a DNA chain during ring closure. Science 260:533–36 [Google Scholar]
  26. Shaw S, Wang JC. 26.  1997. Chirality of DNA trefoils: implications in intramolecular synapsis of distant DNA segments. Proc. Natl. Acad. Sci. USA 94:1692–97 [Google Scholar]
  27. Champoux JJ, Dulbecco R. 27.  1972. An activity from mammalian cells that untwists superhelical DNA—a possible swivel for DNA replication. Proc. Natl. Acad. Sci. USA 69:143–46 [Google Scholar]
  28. Gellert M, Mizuuchi K, O'Dea MH, Nash HA. 28.  1976. DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc. Natl. Acad. Sci. USA 73:3872–76 [Google Scholar]
  29. Wang JC, Liu LF. 29.  1979. DNA topoisomerases: enzymes that catalyze the concerted breaking and rejoining of DNA backbone bonds. Molecular Genetics, Part III JH Taylor 65–88 New York: Academic [Google Scholar]
  30. Liu LF, Wang JC. 30.  1978. Micrococcus luteus DNA gyrase: active components and a model for its supercoiling of DNA. Proc. Natl. Acad. Sci. USA 75:2098–102 [Google Scholar]
  31. Liu LF, Wang JC. 31.  1978. DNA-DNA gyrase complex: the wrapping of the DNA duplex outside the enzyme. Cell 15:979–84 [Google Scholar]
  32. Kirkegaard K, Wang JC. 32.  1981. Mapping the topography of DNA wrapped around gyrase by nucleolytic and chemical probing of complexes of unique DNA sequences. Cell 23:721–29 [Google Scholar]
  33. Klevan L, Wang JC. 33.  1980. DNA gyrase-DNA complex containing 140 base pairs of DNA and an α2β2 protein core. Biochemistry 19:5229–34 [Google Scholar]
  34. Tse YC, Kirkegaard K, Wang JC. 34.  1980. Covalent bonds between protein and DNA: formation of phosphotyrosine linkage between certain DNA topoisomerases and DNA. J. Biol. Chem. 255:5560–65 [Google Scholar]
  35. Horowitz DS, Wang JC. 35.  1987. Mapping the active site tyrosine of Escherichia coli DNA gyrase. J. Biol. Chem. 262:5339–44 [Google Scholar]
  36. Kirkegaard K, Wang JC. 36.  1985. Bacterial DNA topoisomerase I can relax positively supercoiled DNA containing a single-stranded loop. J. Mol. Biol. 185:625–37 [Google Scholar]
  37. Sternglanz R, DiNardo S, Wang JC, Nishimura Y, Hirota Y. 37.  1980. Isolation of an E. coli DNA topoisomerase I mutant. See Ref. 94 833–37
  38. Wang JC, Becherer K. 38.  1983. Cloning of the gene topA encoding for DNA topoisomerase I and the physical mapping of the cysB-topA-trp region of Escherichia coli. Nucleic Acids Res. 11:1773–90 [Google Scholar]
  39. Tse-Dinh YC, Wang JC. 39.  1986. Complete nucleotide sequence of the topA gene encoding Escherichia coli DNA topoisomerase I. J. Mol. Biol. 191:321–31 [Google Scholar]
  40. Keller W. 40.  1975. Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. Proc. Natl. Acad. Sci. USA 72:4876–80 [Google Scholar]
  41. Depew RE, Wang JC. 41.  1975. Conformational fluctuations of DNA helix. Proc. Natl. Acad. Sci. USA 72:4275–79 [Google Scholar]
  42. Pulleyblank DE, Shure M, Tang D, Vinograd J, Vosberg HP. 42.  1975. Action of nicking-closing enzyme on supercoiled and nonsupercoiled closed circular DNA: formation of a Boltzmann distribution of topological isomers. Proc. Natl. Acad. Sci. USA 72:4280–84 [Google Scholar]
  43. Crick FHC, Wang JC, Bauer WR. 43.  1979. Is DNA really a double helix?. J. Mol. Biol. 129:449–61 [Google Scholar]
  44. Wang JC. 44.  1979. Helical repeat of DNA in solution. Proc. Natl. Acad. Sci. USA 76:200–3 [Google Scholar]
  45. Peck LJ, Wang JC. 45.  1981. Sequence dependence of the helical repeat of DNA in solution. Nature 292:375–78 [Google Scholar]
  46. Rhodes D, Klug A. 46.  1980. Helical periodicity of DNA determined by enzyme digestion. Nature 292:378–80 [Google Scholar]
  47. Peck LJ, Wang JC. 47.  1983. Energetics of B-to-Z transition in DNA. Proc. Natl. Acad. Sci. USA 80:6206–10 [Google Scholar]
  48. Courey AJ, Wang JC. 48.  1983. Cruciform formation in a negatively supercoiled DNA may be kinetically forbidden under physiological conditions. Cell 33:817–29 [Google Scholar]
  49. Plon SE, Wang JC. 49.  1986. Transcription of the human β-globin gene is stimulated by an SV40 enhancer to which it is physically linked but topologically uncoupled. Cell 45:575–80 [Google Scholar]
  50. Courey AJ, Plon SE, Wang JC. 50.  1986. The use of psoralen-modified DNA to probe the mechanism of enhancer action. Cell 45:567–74 [Google Scholar]
  51. Liu LF, Liu CC, Alberts BM. 51.  1979. T4 DNA topoisomerase: a new ATP-dependent enzyme essential for initiation of T4 bacteriophage DNA replication. Nature 281:456–61 [Google Scholar]
  52. Liu LF, Liu CC, Alberts BM. 52.  1980. Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell 19:697–707 [Google Scholar]
  53. Brown PO, Cozzarelli NR. 53.  1979. A sign inversion mechanism for enzymatic supercoiling of DNA. Science 206:1081–83 [Google Scholar]
  54. Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P. 54.  1997. An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386:414–17 [Google Scholar]
  55. Wang JC. 55.  1996. DNA topoisomerases. Annu. Rev. Biochem. 65:635–92 [Google Scholar]
  56. Goto T, Wang JC. 56.  1982. Yeast DNA topoisomerase II. J. Biol. Chem. 257:5866–72 [Google Scholar]
  57. Goto T, Wang JC. 57.  1984. Yeast DNA topoisomerase II is encoded by a single-copy, essential gene. Cell 36:1073–80 [Google Scholar]
  58. Holm C, Goto T, Wang JC, Botstein D. 58.  1985. DNA topoisomerase II is required at the time of mitosis in yeast. Cell 41:553–63 [Google Scholar]
  59. DiNardo S, Voelkel K, Sternglanz R. 59.  1984. DNA topoisomerase II mutant of Saccharomyces cerevisiae: topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication. Proc. Natl. Acad. Sci. USA 81:2616–20 [Google Scholar]
  60. Uemura T, Yanagida M. 60.  1984. Isolation of type I and II DNA topoisomerase mutants from fission yeast: single and double mutants show different phenotypes in cell growth and chromatin organization. EMBO J. 3:1737–44 [Google Scholar]
  61. Roca J, Wang JC. 61.  1992. The capture of a DNA double-helix by an ATP-dependent protein clamp: a key step in DNA transport by type II DNA topoisomerases. Cell 71:833–40 [Google Scholar]
  62. Mizuuchi K, Fisher LM, O'Dea MH, Gellert M. 62.  1980. DNA gyrase action involves the introduction of transient double-strand breaks into DNA. Proc. Natl. Acad. Sci. USA 77:1847–51 [Google Scholar]
  63. Wang JC, Gumport RI, Javaherian KJ, Kirkegaard K, Klevan L. 63.  et al. 1980. DNA topoisomerases. See Ref. 94 769–84
  64. Roca J, Wang JC. 64.  1994. DNA transport by a type II DNA topoisomerase: evidence in favor of a two-gate mechanism. Cell 77:609–16 [Google Scholar]
  65. Liu L, Wang JC. 65.  1987. Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. USA 84:7024–27 [Google Scholar]
  66. Pruss GJ, Drlica K. 66.  1986. Topoisomerase I mutants: the gene on pBR322 that encodes resistance to tetracycline affects plasmid DNA supercoiling. Proc. Natl. Acad. Sci. USA 83:8952–56 [Google Scholar]
  67. Lodge JK, Kazic T, Berg DE. 67.  1989. Formation of supercoiling domains in plasmid pBR322. J. Bacteriol. 171:2181–87 [Google Scholar]
  68. Lynch AS, Wang JC. 68.  1993. Anchoring of DNA to the bacterial cytoplasmic membrane through cotranscriptional synthesis of polypeptides encoding membrane proteins or proteins for export: a mechanism of plasmid hypernegative supercoiling in mutants deficient in DNA topoisomerase I. J. Bacteriol. 175:1645–55 [Google Scholar]
  69. Tsai-Pflugfelder M, Liu LF, Liu AA, Tewey KM, Whang-Peng J. 69.  et al. 1988. Cloning and sequencing of cDNA encoding human DNA topoisomerase II and localization of the gene to chromosome region 17q21-22. Proc. Natl. Acad. Sci. USA 85:7177–81 [Google Scholar]
  70. Nitiss J, Wang JC. 70.  1988. DNA topoisomerase-targeting antitumor drugs can be studied in yeast. Proc. Natl. Acad. Sci. USA 85:7501–5 [Google Scholar]
  71. Gellert M, O'Dea MH, Itoh T, Tomizawa J. 71.  1976. Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc. Natl. Acad. Sci. USA 73:4474–78 [Google Scholar]
  72. Gellert M, Mizuuchi K, O'Dea MH, Itoh T, Tomizawa JI. 72.  1977. Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity. Proc. Natl. Acad. Sci. USA 74:4772–76 [Google Scholar]
  73. Tewey KM, Chen GL, Nelson EM, Liu LF. 73.  1984. Intercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J. Biol. Chem. 259:9182–87 [Google Scholar]
  74. Chen GL, Yang L, Rowe TC, Halligan BD, Tewey KM, Liu LF. 74.  1984. Nonintercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J. Biol. Chem. 259:13560–66 [Google Scholar]
  75. Hsiang YH, Liu LF. 75.  1985. Identification of mammalian DNA topoisomerase I as an intracellular target of the anticancer drug camptothecin. Cancer Res. 48:1722–26 [Google Scholar]
  76. Lima CD, Wang JC, Mondragón A. 76.  1994. Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367:138–46 [Google Scholar]
  77. Berger JM, Gamblin SJ, Harrison SC, Wang JC. 77.  1996. Structure and mechanism of DNA topoisomerase II. Nature 379:225–32 [Google Scholar]
  78. Wigley DB, Davies GJ, Dodson EJ, Maxwell A, Dodson G. 78.  1991. Crystal structure of an N-terminal fragment of the DNA gyrase B protein. Nature 351:624–29 [Google Scholar]
  79. Benedetti P, Silvestri A, Fiorani P, Wang JC. 79.  1997. Study of yeast DNA topoisomerase II and its truncation derivatives by transmission electron microscopy. J. Biol. Chem. 272:12132–37 [Google Scholar]
  80. Schultz P, Olland S, Oudet P, Hancock R. 80.  1996. Structure and conformational changes of DNA topoisomerase II visualized by electron microscopy. Proc. Natl. Acad. Sci. USA 93:5936–40 [Google Scholar]
  81. Wang JC.81.  1998. Moving one DNA double helix through another by a type II DNA topoisomerase: the story of a simple molecular machine. Q. Rev. Biophys. 31:107–44 [Google Scholar]
  82. Roca J, Berger JM, Harrison SC, Wang JC. 82.  1996. DNA transport by a type II topoisomerase: direct evidence for a two-gate mechanism. Proc. Natl. Acad. Sci. USA 93:4057–62 [Google Scholar]
  83. Juan CC, Hwang J, Liu AA, Whang-Peng J, Knutsen T. 83.  et al. 1988. Human DNA topoisomerase I is encoded by a single-copy gene that maps to chromosome region 20q12–13.2. Proc. Natl. Acad. Sci. USA 85:8910–13 [Google Scholar]
  84. Wasserman RA, Austin CA, Fisher AM, Wang JC. 84.  1993. Use of yeast in the study of anticancer drugs targeting DNA topoisomerases: expression of a functional recombinant human DNA topoisomerase IIα in yeast. Cancer Res. 53:3591–96 [Google Scholar]
  85. Hanai R, Caron PR, Wang JC. 85.  1996. Human TOP3: a single-copy gene encoding DNA topoisomerase III. Proc. Natl. Acad. Sci. USA 93:3653–57 [Google Scholar]
  86. Morham SG, Kluckman KD, Voulomanos N, Smithies O. 86.  1996. Targeted disruption of the mouse topoisomerase I gene by camptothecin selection. Mol. Cell. Biol. 16:6804–9 [Google Scholar]
  87. Li W, Wang JC. 87.  1998. Mammalian DNA topoisomerase IIIα is essential in early embryogenesis. Proc. Natl. Acad. Sci. USA 95:1010–13 [Google Scholar]
  88. Yang X, Li W, Elizabeth D, Prescott ED, Burden SJ, Wang JC. 88.  2000. DNA topoisomerase IIβ and neural development. Science 287:131–34 [Google Scholar]
  89. Kwan KY, Wang JC. 89.  2001. Mice lacking DNA topoisomerase IIIβ develop to maturity but show a reduced mean lifespan. Proc. Natl. Acad. Sci. USA 98:5717–21 [Google Scholar]
  90. Kwan KY, Moens PB, Wang JC. 90.  2003. Infertility and aneuploidy in mice lacking a type IA DNA topoisomerase IIIβ. Proc. Natl. Acad. Sci. USA 100:2526–31 [Google Scholar]
  91. Lyu YL, Wang JC. 91.  2003. Aberrant lamination in the cerebral cortex of mouse embryos lacking DNA topoisomerase IIβ. Proc. Natl. Acad. Sci. USA 100:7123–28 [Google Scholar]
  92. Lyu YL, Lin CP, Azarova AM, Cai L, Wang JC, Liu LF. 92.  2006. Role of topoisomerase IIβ in the expression of developmentally regulated genes. Mol. Cell. Biol. 26:7929–41 [Google Scholar]
  93. Azarova AM, Lyu YL, Lin CP, Tsai YC, Lau JY. 93.  et al. 2007. Roles of DNA topoisomerase II isozymes in chemotherapy and secondary malignancies. Proc. Natl. Acad. Sci. USA 104:11014–19 [Google Scholar]
  94. Alberts B. 94.  1980. Mechanistic Studies of DNA Replication and Genetic Recombination New York: Academic
/content/journals/10.1146/annurev.biochem.78.030107.090101
Loading
  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error