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Chapter 2 : Chemical Mechanisms for Mobilizing DNA

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Abstract:

Different types of elements, and their associated recombinases, continue to be discovered and characterized. Studies of two major classes of these recombinases have advanced to the point that detailed molecular mechanisms can be discussed. This chapter focuses on the mechanisms of protein-catalyzed recombination by these two classes to provide examples of how the chemistry of DNA mobility is catalyzed and controlled. Central to both types of DNA rearrangements are protein-catalyzed polynucleotidyl transfer steps. The chapter focuses on the likely catalytic functions of several active-site residues. The key to understanding the catalytic mechanisms used by transposases is knowledge of how the different DNA segments are positioned and repositioned within the active sites as recombination progresses. The characteristic of recombinases is related to two important biological features that distinguish the proteins from traditional enzymes. First, the physiological demand on the reaction rate for phosphoryl transfer in recombination is usually very low, with many reactions occurring less than once every cell cycle. Second, the physiology also frequently demands that essentially all substrate molecules are converted to product, even when the "substrate" and the "product" are nearly isoenergetic. The structural organization of recombination complexes is intimately related to the mechanisms used for biological control. Perhaps one of the most satisfying aspects of the continued understanding of site-specific recombination and transposition is that, as the details of the protein-DNA complex structures and catalytic strategies are elucidated, they provide insight into the molecular basis of regulation.

Citation: Mizuuchi K, Baker T. 2002. Chemical Mechanisms for Mobilizing DNA, p 12-23. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch2

Key Concept Ranking

Holliday Junction Resolvase
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DNA Polymerase I
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0.5125157
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References

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1. Aldaz, H.,, E. Schuster,, and T. A. Baker. 1996. The interwoven architecture of the Mu transposase couples DNA synapsis to catalysis. Cell 85: 257 269.
2. Arciszewska, L. K.,, and D. J. Sherratt. 1995. Xer site-specific recombination in vitro. EMBO J. 14: 2112 2120.
3. Argos, P.,, A. Landy,, K. Abremski,, J. B. Egan,, E. Haggard- Ljungquist,, R. H. Hoess,, M. L. Kahn,, B. Kalionis,, S. V. L. Narayana,, L. S. Pierson III,, N. Sternberg,, and J. M. Leong. 1986. The integrase family of site-specific recombinases: regional similarities and global diversity. EMBO J. 5: 433 440.
4. Atkinson, P. W.,, W. D. Warren,, and D. A. O’Brochta. 1993. The hobo transposable element of Drosophila can be cross-mobilized in houseflies and excises like the Ac element of maize. Proc. Natl. Acad. Sci. USA 90: 9693 9697.
5. Beese, L. S.,, and T. A. Steitz. 1991. Structural basis for the 3′-5′ exonuclease activity of Echerichia coli DNA polymerase I: a two metal ion mechanism. EMBO J. 10: 25 33.
5a.. Benkovic, S. J.,, and K. J. Schray,. 1978. The mechanism of phosphoryl transfer, p. 493 527. In R. D. Gandour, and R. L. Schowen (ed.), Transition State of Biochemical Processes, Plenum Press, New York, N.Y.
6. Bhasin, A.,, I. Y. Goryshin,, and W. S. Reznikoff. 1999. Hairpin formation in Tn5 transposition. J. Biol. Chem. 274: 37021 37029.
7. Blakely G. W., A. O. Davidson, and D. J. Sherratt. 1997. Binding and cleavage of nicked substrates by site-specific recombinases XerC and XerD. J. Mol. Biol. 265: 30 39.
8. Bolland, S.,, and N. Kleckner. 1996. The three chemical steps of Tn10/IS10 transposition involve repeated utilization of a single active site. Cell 84: 223 233.
9. Brautigam, C. A.,, and T. A. Steitz. 1998. Structural principles for the inhibition of the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I by phosphorothioates. J. Mol. Biol. 277: 363 377.
10. Cao, Y.,, and F. Hayes. 1999. A newly identified, essential catalytic residue in a critical secondary structure element in the integrase family of site-specific recombinases is conserved in a similar element in eucaryotic type IB topoisomerases. J. Mol. Biol. 289: 517 527.
11. Casareno, R. L. B.,, D. Li,, and J. A. Cowan. 1995. Rational redesign of a metal-dependent nuclease. Engineering the active site of magnesium-dependent ribonuclease H to form an active “metal-independent” enzyme. J. Am. Chem. Soc. 117: 11011 11012.
12. Chen, J. W.,, B. R. Evans,, S. H. Yang,, H. Araki,, Y. Oshima,, and M. Jayaram. 1992. Functional analysis of box I mutations in yeast site-specific recombinases Flp and R: pairwise complementation with recombinase variants lacking the active-site tyrosine. Mol. Cell. Biol. 12: 3757 3765.
13. Chen, Y.,, U. Narendra,, E. L. Iype,, M. M. Cox,, and P. A. Rice. 2000. Crystal structure of a Flp recombinase-Holliday junction complex: assembly of an active oligomer by helix swapping. Mol. Cell. 6: 885 897.
14. Cheng, C.,, L. K. Wang,, J. Sekiguchi,, and S. Shuman. 1997. Mutational analysis of 39 residues of vaccinia DNA topoisomerase identifies Lys-220, Arg-223, and Asn-228 as important for covalent catalysis. J. Biol. Chem. 272: 8263 8269.
15. Cheng, C.,, P. Kussie,, N. Pavletich,, and S. Shuman. 1998. Conservation of structure and mechanism between eukaryotic topoisomerase I and site-specific recombinases. Cell 92: 841 850.
16. Coen, E. S.,, T. P. Robbins,, J. Almeida,, A. Hudson,, and R. Carpenter,. 1989. Consequences and mechanism of transposition in Antirrhinum majus, p. 413 436. In D. E. Berg, and M. M. Howe, (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C.
17. Davies, D. R.,, I. Y. Goryshin,, W. S. Reznikoff,, and I. Rayment. 2000. Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. Science 289: 77 85.
18. Dyda, F.,, A. B. Hickman,, T. M. Jenkins,, A. Engelman,, R. Craigie,, and D. R. Davies. 1994. Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science 266: 1981 1986.
19. Eckstein, F. 1985. Nucleoside phosphorothioates. Annu. Rev. Biochem. 54: 367 402.
20. Engelman, A.,, K. Mizuuchi,, and R. Craigie. 1991. HIV-1DNA integration: mechanism of viral DNA cleavage and DNA strand transfer. Cell 67: 1211 1221.
21. Esposito, D.,, and R. Craigie. 1999. HIV integrase structure and function. Adv. Virus Res. 52: 319 333.
22. Gerton, J. L.,, and P. O. Brown. 1997. The core domain of HIV-1 integrase recognizes key features of its DNA substrates. J. Biol. Chem. 272: 25809 25815.
23. Gerton, J. L.,, D. Herschlag,, and P. O. Brown. 1999. Stereo-specificity of reactions catalyzed by HIV-1 integrase. J. Biol. Chem. 274: 33480 33487.
24. Gopaul, D. N.,, F. Guo,, and G. D. Van Duyne. 1998. Structure of the Holliday junction intermediatein Cre-LoxP site-specific recombination. EMBO J. 17: 4175 4187.
25. Grainge, I.,, and M. Jayaram. 1999. The integrase family of recombinases: organization and function of the active site. Mol. Microbiol. 33: 449 456.
26. Guo, F.,, D. N. Gopaul,, and G. D. Van Duyne. 1997. Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 389: 40 46.
27. Guo, F.,, D. N. Gopaul,, and G. D. Van Duyne. 1999. Asymmetric DNA bending in the Cre-1oxP site-specific recombination synapse. Proc. Natl. Acad. Sci. USA 96: 7143 7148.
28. Haren, L.,, B. Ton-Hoang,, and M. Chandler. 1999. Integrating DNA: transposases and retroviral integrases. Annu. Rev. Microbiol. 53: 245 281.
29. Heuer, T. S.,, and P. O. Brown. 1998. Photo-cross-linking studies suggest a model for the architecture of an active human immunodeficiency virus type 1 integrase-DNA complex. Biochemistry 37: 6667 6678.
30. Hickman, A. B.,, S. Waninger,, J. J. Scocca,, and F. Dyda. 1997. Molecular organization in site-specific recombination: the catalytic domain of bacteriophage HP1 integrase at 2.7 A resolution. Cell 89: 227 237.
31. Hickman, A. B.,, Y. Li,, S. V. Mathew,, E. W. May,, N. L. Craig,, and F. Dyda. 2000. Unexpected structural diversity in DNA recombination: the restriction endonuclease connection. Mol. Cell 5: 1025 1034.
32. Hollfelder, F.,, and D. Herschlag. 1995. The nature of the transition state for enzyme-catalyzed phosphoryl transfer. Hydrolysis of O-aryl phosphorothioates by alkaline phosphatase. Biochemistry 34: 12255 12264.
33. Hughes, R. E.,, G. F. Hatfull,, P. Rice,, T. A. Steitz,, and N. D. Grindley. 1990. Cooperativity mutants of the gamma delta resolvase identify an essential interdimer interaction. Cell 63: 1331 1338.
34. Jenkins, T. M.,, D. Esposito,, A. Engelman,, and R. Craigie. 1997. Critical contacts between HIV-1 integrase and viral DNA identified by structure-based analysis and photo-crosslinking. EMBO J. 16: 6849 6859.
35. Jou, R.,, and J. A. Cowan. 1991. Ribonuclease H activation by inert transition-metal complexes. Mechanistic probes for metallocofactors: insights on the metallobiochemistry of divalent magnesium ion. J. Am. Chem. Soc. 113: 6685 6686.
36. Keck, J. L.,, E. R. Goedken,, and S. Marqusee. 1998. Activation/ attenuation model for RNase H. A one-metal mechanism with second-metal inhibition. J. Biol. Chem. 273: 34128 34133.
37. Kennedy, A. K.,, A. Guhathakurta,, N. Kleckner,, and D. B. Haniford. 1998. Tn10 transposition via a DNA hairpin intermediate. Cell 95: 125 134.
38. Kennedy, A. K.,, D. B. Haniford,, and K. Mizuuchi. 2000. Single active site catalysis of the successive phosphoryl transfer steps by DNA transposases: insights from phosphorothioate stereoselectivity. Cell 101: 295 305.
39. Knowles, J. R. 1980. Enzyme-catalyzed phosphoryl transfer reactions. Annu. Rev. Biochem. 49: 877 919.
40. Krogh, B. O.,, and S. Shuman. 2000. Catalytic mechanism of DNA topoisomerase IB. Mol. Cell 5: 1035 1041.
41. Kruklitis, R.,, D. J. Welty,, and H. Nakai. 1996. ClpX protein of Escherichia coli activates bacteriophage Mu transposase in the strand transfer complex for initiation of Mu DNA synthesis. EMBO J. 15: 935 944.
42. Lavoie, B. D.,, B. S. Chan,, R. G. Allison,, and G. Chaconas. 1991. Structural aspects of a higher order nucleoprotein complex: induction of an altered DNA structure at the Mu-host junction of the Mu type 1 transpososome. EMBO J. 10: 3051 3059.
43. Lee, J.,, and M. Jayaram. 1995. Role of partner homology in DNA recombination. J. Biol. Chem. 270: 4042 4052.
44. Lee, J.,, M. Jayaram,, and I. Grainge. 1999. Wild-type Flp recombinase cleaves DNA in trans. EMBO J. 18: 784 791.
45. Levchenko, I.,, L. Luo,, and T. A. Baker. 1995. Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev. 9: 2399 2408.
46. Maegley, K. A.,, S. J. Admiraal,, and D. Herschlag. 1996. Rascatalyzed hydrolysis of GTP: a new perspective from model studies. Proc. Natl. Acad. Sci. USA 93: 8160 8166.
47. Mizuuchi, K. 1992. Transpositional recombination: mechanistic insights from studies of Mu and other elements. Annu. Rev. Biochem. 61: 1011 1051.
48. Mizuuchi, K.,, and K. Adzuma. 1991. Inversion of the phosphate chirality at the target site of Mu DNA strand transfer: evidence for a one-step transesterification mechanism. Cell 66: 129 140.
49. Mizuuchi, K.,, T. J. Nobbs,, S. E. Halford,, K. Adzuma,, and J. Qin. 1999. A new method for determining the stereochemistry of DNA cleavage reactions: application to the SfiI and HpaII restriction endonucleases and to the MuA transposase. Biochemistry 38: 4640 4648.
50. Mizuuchi, M.,, and K. Mizuuchi. 1989. Efficient Mu transposition requires interaction of transposase with a DNA sequence at the Mu operator: implications for regulation. Cell 58: 399 408.
51. Namgoong, S. Y.,, and R. M. Harshey. 1998. The same two monomers within a MuA tetramer provide the DDE domains for the strand cleavage and strand transfer steps of transposition. EMBO J. 17: 3775 3785.
52. Nunes-Duby, S. E.,, R. S. Tirumalai,, L. Dorgai,, E. Yagil,, R. A. Weisberg,, and A. Landy. 1994. Lambda integrase cleavesDNA in cis. EMBO J. 13: 4421 4430.
53. Nunes-Duby, S. E.,, M. A. Azaro,, and A. Landy. 1995. Swapping DNA strands and sensing homology without branch migration in lambda site-specific recombination. Curr. Biol. 5: 139 148.
54. Petersen, B. O.,, and S. Shuman. 1997. Histidine 265 is important for covalent catalysis by vaccinia topoisomerase and is conserved in all eukaryotic type I enzymes. J. Biol. Chem. 272: 3891 3896.
55. Redinbo, M. R.,, L. Stewart,, P. Kuhn,, J. J. Champoux,, and W. G. Hol. 1998. Crystal structure of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279: 1504 1513.
56. Rezsohazy, R.,, B. Hallet,, J. Delcour,, and J. Mahillon. 1993. The IS4 family of insertion sequences: evidence for a conserved transposase motif. Mol. Microbiol. 9: 1283 1295.
57. Rice, P.,, and K. Mizuuchi. 1995. Structure of the bacteriophage Mu transposase core: a common structural motif for DNA transposition and retroviral integration. Cell 82: 209 220.
58. Rice, P.,, R. Craigie,, and D. R. Davies. 1996. Retroviral integrases and their cousins. Curr. Opin. Struct. Biol. 6: 76 83.
59. Richards, F. M.,, and H. W. Wyckoff,. 1971. Bovine pancreatic ribonuclease, p. 647 806. In P. D. Boyer (ed.), The Enzymes, 3rd ed., vol. 4. Academic Press, New York, N.Y.
60. Sarnovsky, R. J.,, E. W. May,, and N. L. Craig. 1996. The Tn7 transposase is a heteromeric complex in which DNA breakage and joining activities are distributed between different gene products. EMBO J. 15: 6348 6361.
61. Savilahti, H.,, and K. Mizuuchi. 1996. Mu transpositional recombination: donor DNA cleavage and strand transfer in trans by the Mu transposase. Cell 85: 271 280.
62. Shibagaki, Y.,, and S. A. Chow. 1997. Central core domain of retroviral integrase is responsible for target site selection. J. Biol. Chem. 272: 8361 8369.
63. Steitz, T. A.,, and J. A. Steitz. 1993. A general two-metal-ion mechanism for catalytic RNA. Proc. Natl. Acad. Sci. USA 90: 6498 6502.
64. Stewart, L.,, M. R. Redinbo,, X. Qiu,, W. G. J. Hol,, and J. J. Champoux. 1998. A model for the mechanism of human topoisomerase I. Science 279: 1534 1540.
65. Turlan, C.,, and M. Chandler. 2000. Playing second fiddle: second-strand processing and liberation of transposable elements from donor DNA. Trends Microbiol. 8: 268 274.
66. van Gent, D. C.,, K. Mizuuchi,, and M. Gellert. 1996. Similarities between initiation of V(D)J recombination and retroviral integration. Science 271: 1592 1594.
67. Weil, C. F.,, and R. Kunze. 2000. Transposition of maize Ac/ Ds transposable elements in the yeast Saccharomyces cerevisiae. Nat. Genet. 26: 187 190.
68. Williams, T. L.,, E. L. Jackson,, A. Carritte,, and T. A. Baker. 1999. Organization and dynamics of the Mu transpososome: recombination by communication between two active sites. Genes Dev. 13: 2725 2737.
69. Wittschieben, J.,, and S. Shuman. 1997. Mechanism of DNA transesterification by vaccinia topoisomerase: catalytic contributions of essential residues Arg-130, Gly-132, Tyr-136 and Lys-167. Nucleic Acids Res. 25: 3001 3008.
70. Wlodawer, A. 1999. Crystal structures of catalytic core domains of retroviral integrases and role of divalent cations in enzymatic activity. Adv. Virus Res. 52: 335 350.
71. Yang, W.,, and T. A. Steitz. 1995. Crystal structure of the site-specific recombinase gamma delta resolvase complexed with a 34 bp cleavage site. Cell 82: 193 207.
72. Yang, W.,, and T. A. Steitz. 1995. Recombining the structures of HIV integrase, RuvC and RNase H. Structure 3: 131 134.
73. Zheng, R.,, T. M. Jenkins,, and R. Craigie. 1996. Zinc folds the N-terminal domain of HIV-1 integrase, promotes multimerization, and enhances catalytic activity. Proc. Natl. Acad. Sci. USA 93: 13659 13664.

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