Theoretical analysis of competing conformational transitions in superhelical DNA

PLoS Computational Biology

Volumn 8, Issue 4, 2012, Pages

  Zhabinskaya, Dina ^a   Benham, Craig J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; TOPOLOGY; TRANSCRIPTION;

BASE PAIRS; BASE SEQUENCES; COMPETITIVE BEHAVIOR; CONFORMATIONAL TRANSITIONS; DNA MOLECULES; MECHANICAL MODELING; SUPERCOILED DNA; SUPERHELICITY; TRANSCRIPTION START SITE; TRANSITION BEHAVIOR;

DNA;

DNA B; DNA Z;

ACCURACY; ARTICLE; AT RICH SEQUENCE; BASE PAIRING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA BASE COMPOSITION; DNA CONFORMATION; DNA DENATURATION; DNA SEQUENCE; DNA STRAND; DNA SUPERCOILING; ENERGY TRANSFER; EUKARYOTE; GC RICH SEQUENCE; GENE EXPRESSION REGULATION; GENETIC ALGORITHM; HUMAN; MATHEMATICAL MODEL; NONHUMAN; ONCOGENE C MYC; PROKARYOTE; PSEUDOGENE; TEMPERATURE SENSITIVITY; THEORETICAL MODEL; TRANSCRIPTION INITIATION SITE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; CONFORMATION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; ULTRASTRUCTURE;

EUKARYOTA; PROKARYOTA;

BASE SEQUENCE; COMPUTER SIMULATION; DNA, SUPERHELICAL; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION;

EID: 84861116439     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002484     Document Type: Article

References (76)

1. Franklin R, Gosling R, (1953) Molecular configuration in sodium thymonucleate. Nature 171: 740-741.
2. Wang A, Quigley G, Kolpak F, Crawford J, Van Boom J, et al. (1979) Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature 282: 680-686.
3. Liu LF, Wang JC, (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A 84: 7024-7027.
4. Kouzine F, Sanford S, Elisha-Feil Z, Levens D, (2008) The functional response of upstream DNA to dynamic supercoiling in vivo. Nat Struct Mol Biol 15: 146-154.
5. Peck LJ, Nordheim A, Rich A, Wang JC, (1982) Flipping of cloned d(pCpG)n.d(pCpG)n DNA sequences from right- to left-handed helical structure by salt, Co(III), or negative supercoiling. Proc Natl Acad Sci U S A 79: 4560-4564.
6. Singleton CK, Klysik J, Stirdivant SM, Wells RD, (1982) Left-handed Z-DNA is induced by supercoiling in physiological ionic conditions. Nature 299: 312-316.
7. Mirkin SM, Lyamichev VI, Drushlyak KN, Dobrynin VN, Filippov SA, et al. (1987) DNA H-form requires a homopurine-homopyrimidine mirror repeat. Nature 330: 495-497.
8. Sheflin LG, Kowalski D, (1984) Mung bean nuclease cleavage of a dA+dT-rich sequence or an inverted repeat sequence in supercoiled PM2 DNA depends on ionic environment. Nucleic Acids Res 12: 7087-7104.
9. Kowalski D, Natale D, Eddy M, (1988) Stable DNA unwinding, not "breathing", accounts for single-strand-specific nuclease hypersensitivity of specific A+T-rich sequences. Proc Natl Acad Sci U S A 85: 9464-9468.
10. Lilley DM, (1980) The inverted repeat as a recognizable structural feature in supercoiled DNA molecules. Proc Natl Acad Sci U S A 77: 6468-6472.
11. Panayotatos N, Wells RD, (1981) Cruciform structures in supercoiled DNA. Nature 289: 466-470.
12. Mizuuchi K, Mizuuchi M, Gellert M, (1982) Cruciform structures in palindromic DNA are favored by DNA supercoiling. J Mol Biol 156: 229-243.
13. Sun D, Hurley L, (2009) The importance of negative superhelicity in inducing the formation of G-quadruplex and I-motif structures in the c-Myc promoter: Implications for drug targeting and control of gene expression. J Medic Chem 52: 2863-2874.
14. Belotserkovskii BP, De Silva E, Tornaletti S, Wang G, Vasquez KM, et al. (2007) A triplex-forming sequence from the human c-myc promoter interferes with dna transcription. J Biol Chem 282: 32433-32441.
15. Benham CJ, (1979) Torsional stress and local denaturation in supercoiled DNA. Proc Natl Acad Sci U S A 76: 3870-3874.
16. Benham CJ, (1981) Theoretical analysis of competitive conformational transitions in torsionally stressed DNA. J Mol Biol 150: 43-68.
17. Benham CJ, (1982) Stable cruciform formation at inverted repeat sequences in supercoiled DNA. Biopolymers 21: 679-696.
18. Benham CJ, (1983) Statistical mechanical analysis of competing conformational transitions in superhelical DNA. Cold Spring Harbor Symposia on Quantitative Biology Cold Spring Harbor Laboratory Press. volume 47.
19. Benham CJ, (1980) Theoretical analysis of transitions between B-and Z-conformations in torsionally stressed DNA. Nature 288: 637-638.
20. Frank-Kamenetskii MD, Vologodskii AV, (1984) Thermodynamics of the B-Z transition in superhelical DNA. Nature 307: 481-482.
21. Peck LJ, Wang JC, (1983) Energetics of B-to-Z transition in DNA. Proc Natl Acad Sci U S A 80: 6206-6210.
22. Ho PS, Ellison MJ, Quigley GJ, Rich A, (1986) A computer aided thermodynamic approach for predicting the formation of Z-DNA in naturally occurring sequence. EMBO J 5: 2737-2744.
23. Kelleher RJ, Ellison MJ, Ho PS, Rich A, (1986) Competitive behavior of multiple, discrete B-Z transitions in supercoiled DNA. Proc Natl Acad Sci U S A 83: 6342-6346.
24. Ho PS, (1994) The non-B-DNA structure of d(CA/TG)n does not differ from that of Z-DNA. Proc Natl Acad Sci U S A 91: 9549-9553.
25. Vologodskii AV, Frank-Kamenetskii MD, (1984) Left-handed Z form in superhelical DNA: a theoretical study. J Biomol Struct Dynam 1: 1325-1333.
26. Aboul-ela F, Bowater RP, Lilley DM, (1992) Competing B-Z and helix-coil conformational transitions in supercoiled plasmid DNA. J Biol Chem 267: 1776-1785.
27. Anshelevich VV, Vologodskii AV, Lukashin AV, Frank-Kamenetskii MD, (1979) Statisticalmechanical treatment of violations of the double helix in supercoiled DNA. Biopolymers 18: 2733-2744.
28. Benham CJ, (1990) Theoretical analysis of heteropolymeric transitions in superhelical DNA molecules of specified sequence. J Chem Phys 92: 6294-6305.
29. Benham CJ, (1992) Energetics of the strand separation transition in superhelical DNA. J Mol Biol 225: 835-847.
30. Fye RM, Benham CJ, (1999) Exact method for numerically analyzing a model of local denaturation in superhelically stressed DNA. Phys Rev E 59: 3408-3426.
31. Zhabinskaya D, Benham CJ, (2011) Theoretical Analysis of the Stress Induced BZ Transition in Superhelical DNA. PLoS Comput Biol 7: 1-14.
32. Benham CJ, Bi C, (2004) The analysis of stress-induced duplex destabilization in long genomic DNA sequences. J Comp Biol 11: 519-543.
33. Benham CJ, (1993) Sites of predicted stress-induced DNA duplex destabilization occur preferentially at regulatory loci. Proc Natl Acad Sci U S A 90: 2999-3003.
34. Benham CJ, Kohwi-Shigematsu T, Bode J, (1997) Stress-induced duplex destabilization in chromosomal scaffold/matrix attachment regions. J Mol Biol 274: 181-196.
35. Sheridan SD, Benham CJ, Hatfield G, (1998) Activation of gene expression by a novel DNA structural transmission mechanism that requires supercoiling-induced DNA duplex destabilization in an upstream activating sequence. J Biol Chem 273: 21298-21308.
36. He L, Liu J, Collins I, Sanford S, O'Connell B, et al. (2000) Loss of FBP function arrests cellular proliferation and extinguishes c-myc expression. EMBO J 19: 1034-1044.
37. Sheridan SD, Benham CJ, Hatfield G, (1999) Inhibition of DNA supercoiling-dependent transcriptional activation by a distant B-DNA to Z-DNA transition. J Biol Chem 274: 8169-8174.
38. Wang H, Noordewier M, Benham CJ, (2004) Stress-induced DNA duplex destabilization (SIDD) in the E. coli genome: SIDD sites are closely associated with promoters. Genome Res 14: 1575-1584.
39. Ak P, Benham CJ, (2005) Susceptibility to superhelically driven DNA duplex destabilization: A highly conserved property of yeast replication origins. PLoS Comput Biol 1: 0041-0046.
40. Polonskaya Z, Benham CJ, Hearing J, (2004) Role for a region of helically unstable DNA within the Epstein-Barr virus latent cycle origin of DNA replication oriP in origin function. Virology 328: 282-291.
41. Wang H, Benham CJ, (2008) Superhelical destabilization in regulatory regions of stress response genes. PLoS Comput Biol 4: 0062-0076.
42. Potaman V, Bissler J, Hashem V, Oussatcheva E, Lu L, et al. (2003) Unwound structures in SCA10 (ATTCT) n·(ATTCT) n repeats. J Mol Biol 326: 1095-1111.
43. Haniford DB, Pulleyblank DE, (1983) Facile transition of poly[d(TG)×d(CA)] into a left-handed helix in physiological conditions. Nature 302: 632-634.
44. Nordheim A, Rich A, (1983) Negatively supercoiled simian virus 40 DNA contains Z-DNA segments within transcriptional enhancer sequence. Nature 303: 674-679.
45. Rahmouni AR, Wells RD, (1989) Stabilization of Z DNA in vivo by localized supercoiling. Science 246: 358-363.
46. Haniford DB, Pulleyblank DE, (1983) The in vivo occurrence of Z DNA. J Biomol Struct Dyn 1: 593-609.
47. Jaworski A, Hsieh WT, Blaho JA, Larson JE, Wells RD, (1987) Left-handed DNA in vivo. Science 238: 773-777.
48. Rich A, Zhang S, (2003) Timeline: Z-DNA: the long road to biological function. Nat Rev Genet 4: 566-572.
49. Wittig B, Dorbic T, Rich A, (1991) Transcription is associated with Z-DNA formation in metabolically active permeabilized mammalian cell nuclei. Proc Natl Acad Sci U S A 88: 2259-2263.
50. Wittig B, Wölfl S, Dorbic T, Vahrson W, Rich A, (1992) Transcription of human c-myc in permeabilized nuclei is associated with formation of Z-DNA in three discrete regions of the gene. EMBO J 11: 4653-4663.
51. Wölfl S, Wittig B, Rich A, (1995) Identification of transcriptionally induced Z-DNA segments in the human c-myc gene. Biochim Biophys Acta 1264: 294-302.
52. Ellison MJ, Kelleher RJ, Wang AH, Habener JF, Rich A, (1985) Sequence-dependent energetics of the B-Z transition in supercoiled DNA containing nonalternating purine-pyrimidine sequences. Proc Natl Acad Sci U S A 82: 8320-8324.
53. Ellison MJ, Feigon J, Kelleher RJ, Wang AH, Habener JF, et al. (1986) An assessment of the Z-DNA forming potential of alternating dA-dT stretches in supercoiled plasmids. Biochem 25: 3648-3655.
54. Johnston BH, Quigley GJ, Ellison MJ, Rich A, (1991) The Z-Z Junction: The boundary Between Two Out of Phase Z-DNA Regions. Biochem 30: 5257-5263.
55. Schroth GP, Chou PJ, Ho PS, (1992) Mapping Z-DNA in the human genome. Computer-aided mapping reveals a nonrandom distribution of potential Z-DNA-forming sequences in human genes. J Biol Chem 267: 11846-11855.
56. Reif F, (1965) Fundamentals of statistical and thermal physics. McGraw-Hill New York.
57. Bauer W, Vinograd J, (1970) Interaction of closed circular DNA with intercalative dyes: II. The free energy of superhelix formation in SV40 DNA. J Mol Biol 47: 419-435.
58. Breslauer KJ, Frank R, Blöcker H, Marky LA, (1986) Predicting DNA duplex stability from the base sequence. Proc Natl Acad Sci U S A 83: 3746-3750.
59. Delcourt SG, Blake RD, (1991) Stacking energies in DNA. J Biol Chem 266: 15160-15169.
60. Steger G, (1994) Thermal denaturation of double-stranded nucleic acids: prediction of temperatures critical for gradient gel electrophoresis and polymerase chain reaction. Nucleic Acids Res 22: 2760-2768.
61. Bi C, Benham CJ, (2003) The approximate algorithm for analysis of the strand separation transition in superhelical DNA using nearest neighbor energetics. Proc IEEE Comp Soc Bioinformatics pp. 460-461.
62. Bauer WR, Benham CJ, (1993) The free energy, enthalpy and entropy of native and of partially denatured closed circular DNA. J Mol Biol 234: 1184-1196.
63. Pulleyblank DE, Shure M, Tang D, Vinograd J, Vosberg HP, (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 U S A 72: 4280-4284.
64. Depew DE, Wang JC, (1975) Conformational fluctuations of DNA helix. Proc Natl Acad Sci U S A 72: 4275-4279.
65. Benham CJ, Savitt AG, Bauer WR, (2002) Extrusion of an imperfect palindrome to a cruciform in superhelical DNA: complete determination of energetics using a statistical mechanical model. J Mol Biol 316: 563-581.
66. Nordheim A, Lafer EM, Peck LJ, Wang JC, David Stollar B, et al. (1982) Negatively supercoiled plasmids contain left-handed Z-DNA segments as detected by specific antibody binding. Cell 31: 309-318.
67. Levens D, (2010) You Dont Muck with MYC. Genes cancer 1: 547-554.
68. Brooks TA, Hurley LH, (2009) The role of supercoiling in transcriptional control of MYC and its importance in molecular therapeutics. Nat Rev Cancer 9: 849-861.
69. Khuu P, Sandor M, DeYoung J, Ho PS, (2007) Phylogenomic analysis of the emergence of GC-rich transcription elements. Proc Natl Acad Sci U S A 104: 16528-16533.
70. Li H, Xiao J, Li J, Lu L, Feng S, et al. (2009) Human genomic Z-DNA segments probed by the Zα domain of ADAR1. Nucleic Acids Res 37: 2737-2746.
71. Palaniswamy SK, Jin VX, Sun H, Davuluri RV, (2005) Omgprom: a database of orthologous mammalian gene promoters. Bioinformatics 21: 835-836.
72. Ozsolak F, Kapranov P, Foissac S, Kim SW, Fishilevich E, et al. (2010) Comprehensive polyadenylation site maps in yeast and human reveal pervasive alternative polyadenylation. Cell 143: 1018-1029.
73. Champ PC, Maurice S, Vargason J, Camp T, Ho PS, (2004) Distributions of Z-DNA and nuclear factor I in human chromosome 22: a model for coupled transcriptional regulation. Nucleic Acids Res 32: 6501-6510.
74. Wang H, Kaloper M, Benham CJ, (2006) SIDDBASE: a database containing the stress-induced DNA duplex destabilization (SIDD) profiles of complete microbial genomes. Nucleic Acids Res 34: D373-D378.
75. Zhang Z, Carriero N, Gerstein M, (2004) Comparative analysis of processed pseudogenes in the mouse and human genomes. Trends Genet 20: 62-67.
76. Leblanc BP, Benham CJ, Clark DJ, (2000) An initiation element in the yeast CUP1 promoter is recognized by RNA polymerase II in the absence of TATA box-binding protein if the DNA is negatively supercoiled. Proc Natl Acad Sci U S A 97: 10745-10750.