HIV chromatin is a preferred target for drugs that bind in the DNA minor groove

English version

Autoři: Clayton K. Collings ^aff001; Donald W. Little, III ^aff003; Samuel J. Schafer ^aff004; John N. Anderson ^aff005
Působiště autorů: Department of Pediatric Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA, United States of America ^aff001; Broad Institute of MIT and Harvard, Cambridge, MA, United States of America ^aff002; University of Michigan Medical School, Ann Arbor, MI, United States of America ^aff003; Department of Reproductive and Developmental Sciences, University of British Columbia, Vancouver, BC, Canada ^aff004; Department of Biological Sciences, Purdue University, West Lafayette, IN, United States of America ^aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0216515

Souhrn

The HIV genome is rich in A but not G or U and deficient in C. This nucleotide bias controls HIV phenotype by determining the highly unusual composition of all major HIV proteins. The bias is also responsible for the high frequency of narrow DNA minor groove sites in the double-stranded HIV genome as compared to cellular protein coding sequences and the bulk of the human genome. Since drugs that bind in the DNA minor groove disrupt nucleosomes on sequences that contain closely spaced oligo-A tracts which are prevalent in HIV DNA because of its bias, it was of interest to determine if these drugs exert this selective inhibitory effect on HIV chromatin. To test this possibility, nucleosomes were reconstituted onto five double-stranded DNA fragments from the HIV-1 pol gene in the presence and in the absence of several minor groove binding drugs (MGBDs). The results demonstrated that the MGBDs inhibited the assembly of nucleosomes onto all of the HIV-1 segments in a manner that was proportional to the A-bias, but had no detectable effect on the formation of nucleosomes on control cloned fragments or genomic DNA from chicken and human. Nucleosomes preassembled onto HIV DNA were also preferentially destabilized by the drugs as evidenced by enhanced nuclease accessibility in physiological ionic strength and by the preferential loss of the histone octamer in hyper-physiological salt solutions. The drugs also selectively disrupted HIV-containing nucleosomes in yeast as revealed by enhanced nuclease accessibility of the in vivo assembled HIV chromatin and reductions in superhelical densities of plasmid chromatin containing HIV sequences. A comparison of these results to the density of A-tracts in the HIV genome indicates that a large fraction of the nucleosomes that make up HIV chromatin should be preferred in vitro targets for the MGBDs. These results show that the MGBDs preferentially disrupt HIV-1 chromatin in vitro and in vivo and raise the possibility that non-toxic derivatives of certain MGBDs might serve as a novel class of anti-HIV agents.

Klíčová slova:

DNA electrophoresis – DNA sequence analysis – HIV-1 – Human genomics – Chromatin – Nucleosomes – Sequence analysis

Zdroje

1. Andino R, Domingo E. Viral quasispecies. Virology. 2015;279: 46–51.

2. Nomaguchi M, Doi N, Koma T, Adachi A. HIV-1 mutates to adapt in fluxing environments. Microbes Infect. 2018;20(9–10): 610–4. doi: 10.1016/j.micinf.2017.08.003 28859896

3. Gunthard HF, Aberg JA, Eron JJ, Hoy JF, Telenti A, Benson CA, et al. Antiretroviral treatment of adult HIV infection: 2014 recommendations of the International Antiviral Society-USA Panel. JAMA. 2014;312(4): 410–25. doi: 10.1001/jama.2014.8722 25038359

4. Zuo XF, Huo ZP, Kang DW, Wu GC, Zhou ZX, Liu XY, et al. Current insights into anti-HIV drug discovery and development: a review of recent patent literature (2014–2017). Expert Opinion on Therapeutic Patents. 2018;28(4): 299–316. doi: 10.1080/13543776.2018.1438410 29411697

5. Bashiri K, Rezaei N, Nasi M, Cossarizza A. The role of latency reversal agents in the cure of HIV: A review of current data. Immunol Lett. 2018;196: 135–9. doi: 10.1016/j.imlet.2018.02.004 29427743

6. Margolis DM, Garcia JV, Hazuda DJ, Haynes BF. Latency reversal and viral clearance to cure HIV-1. Science. 2016;353(6297): aaf6517. doi: 10.1126/science.aaf6517 27463679

7. Kypr J, Mrázek J, Reich J. Nucleotide composition bias and CpG dinucleotide content in the genomes of HIV and HTLV 1/2. Biochim Biophys Acta. 1989;1009(3): 280–2. doi: 10.1016/0167-4781(89)90114-0 2597678

8. Bronson EC, Anderson JN. Nucleotide Composition as a Driving-Force in the Evolution of Retroviruses. J Mol Evol. 1994;38(5): 506–32. doi: 10.1007/bf00178851 8028030

9. Albert FG, Bronson EC, Fitzgerald DJ, Anderson JN. Circular structures in retroviral and cellular genomes. J Biol Chem. 1995;270(40): 23570–81. doi: 10.1074/jbc.270.40.23570 7559522

10. Khan GS, Shah A, Zia ur R, Barker D. Chemistry of DNA minor groove binding agents. J Photochem Photobiol B. 2012;115: 105–18. doi: 10.1016/j.jphotobiol.2012.07.003 22857824

11. Neidle S. DNA minor-groove recognition by small molecules. Nat Prod Rep. 2001;18(3): 291–309. doi: 10.1039/a705982e 11476483

12. Rahman A, O'Sullivan P, Rozas I. Recent developments in compounds acting in the DNA minor groove. Medchemcomm. 2019;10(1): 26–40. doi: 10.1039/c8md00425k 30774852

13. Albert FG, Eckdahl TT, Fitzgerald DJ, Anderson JN. Heterogeneity in the actions of drugs that bind in the DNA minor groove. Biochemistry. 1999;38(31): 10135–46. doi: 10.1021/bi990382p 10433722

14. Fitzgerald DJ, Anderson JN. Selective nucleosome disruption by drugs that bind in the minor groove of DNA. J Biol Chem. 1999;274(38): 27128–38. doi: 10.1074/jbc.274.38.27128 10480928

15. Chiu TP, Comoglio F, Zhou T, Yang L, Paro R, and Rohs R. DNAshapeR: an R/Bioconductor package for DNA shape prediction and feature encoding. Bioinformatics 2016;32(8): 1211–1213. doi: 10.1093/bioinformatics/btv735 26668005

16. Chiu TP, Yang L, Zhou T, Main BJ, Parker SC, Nuzhdin SV, Tullius TD, and Rohs R. GBshape: a genome browser database for DNA shape annotations. Nucleic Acids Res. 2015;43: D103–9. doi: 10.1093/nar/gku977 25326329

17. Tanese N, Sodroski J, Haseltine WA, Goff SP. Expression of reverse transcriptase activity of human T-lymphotropic virus type III (HTLV-III/LAV) in Escherichia coli. J Virol. 1986;59(3): 743–5. 2426471

18. Williams JS, Eckdahl TT, Anderson JN. Bent DNA Functions as a Replication Enhancer in Saccharomyces-Cerevisiae. Mol Cellular Biol. 1988;8(7): 2763–9.

19. Fitzgerald DJ, Anderson JN. Unique translational positioning of nucleosomes on synthetic DNAs. Nucleic Acids Res. 1998;26(11): 2526–35. doi: 10.1093/nar/26.11.2526 9592133

20. Brown JW, Anderson JA. The binding of the chromosomal protein HMG-2a to DNA regions of reduced stabilities. J Biol Chem. 1986;261(3): 1349–54. 3003066

21. Brock JA, Bloom K. A chromosome breakage assay to monitor mitotic forces in budding yeast. J Cell Sci. 1994;107(4): 891–902.

22. Kent NA, Bird LE, Mellor J. Chromatin analysis in yeast using NP-40 permeabilised sphaeroplasts. Nucleics Acids Res. 1993;21(19): 4653–4.

23. Shure M, Pulleyblank DE, Vinograd J. The problems of eukaryotic and prokaryotic DNA packaging and in vivo conformation posed by superhelix density heterogeneity. Nucleic Acids Res. 1977;4(5): 1183–205. doi: 10.1093/nar/4.5.1183 197488

24. Robyr D, Gegonne A, Wolffe AP, Wahli W. Determinants of vitellogenin B1 promoter architecture—HNF3 and estrogen responsive transcription within chromatin. J Biol Chem. 2000;275(36): 28291–300. doi: 10.1074/jbc.M002726200 10854430

25. Burkhoff AM, Tullius TD. The unusual conformation adopted by the adenine tracts in kinetoplast DNA. Cell. 1987;48(6): 935–43. doi: 10.1016/0092-8674(87)90702-1 3030560

26. Goodsell DS, Kaczor-Grzeskowiak M, Dickerson RE. The crystal structure of CCATTAATGG: implications for bending of B-DNA at TA steps. J Mol Biol. 1994;239(1): 79–96. doi: 10.1006/jmbi.1994.1352 8196049

27. Fernandez AG, Anderson JN. Nucleosome positioning determinants. J Mol Biol. 2007;371(3): 649–68. doi: 10.1016/j.jmb.2007.05.090 17586522

28. Vasudevan D, Chua EYD, Davey CA. Crystal Structures of Nucleosome Core Particles Containing the '601' Strong Positioning Sequence. J Mol Biol. 2010;403(1): 1–10. doi: 10.1016/j.jmb.2010.08.039 20800598

29. Abu-Daya A, Brown PM, Fox KR. DNA sequence preferences of several AT-selective minor groove binding ligands. Nucleic Acids Res. 1995;23(17): 3385–92. doi: 10.1093/nar/23.17.3385 7567447

30. Bailly C, Waring MJ. Comparison of different footprinting methodologies for detecting binding sites for a small ligand on DNA. J Biomol Struct Dyn. 1995;12(4): 869–98. doi: 10.1080/07391102.1995.10508782 7779305

31. Fitzgerald DJ, Dryden GL, Bronson EC, Williams JS, Anderson JN. Conserved patterns of bending in satellite and nucleosome positioning DNA. J Biol Chem. 1994;269(33): 21303–14. 8063755

32. Germond JE, Hirt B, Oudet P, Gross-Bellark M, Chambon P. Folding of the DNA double helix in chromatin-like structures from simian virus 40. Proc Natl Acad Sci U S A. 1975;72(5): 1843–7. doi: 10.1073/pnas.72.5.1843 168578

33. Keller W. Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. Proc Natl Acad Sci U S A. 1975;72(12): 4876–80. doi: 10.1073/pnas.72.12.4876 174079

34. Lanzer M, Wertheimer SP, de Bruin D, Ravetch JV. Chromatin structure determines the sites of chromosome breakages in Plasmodium falciparum. Nucleic Acids Res. 1994;22(15): 3099–103. doi: 10.1093/nar/22.15.3099 8065922

35. Legault J, Tremblay A, Ramotar D, Mirault ME. Clusters of S1 nuclease-hypersensitive sites induced in vivo by DNA damage. Mol Cell Biol. 1997;17(9): 5437–52. doi: 10.1128/mcb.17.9.5437 9271420

36. Sung P, Trujillo KM, Van Komen S. Recombination factors of Saccharomyces cerevisiae. Mutat Res. 2000;451(1–2): 257–75. doi: 10.1016/s0027-5107(00)00054-3 10915877

37. Baraldi PG, Bovero A, Fruttarolo F, Preti D, Tabrizi MA, Pavani MG, Romagnoli R. DNA minor groove binders as potential antitumor and antimicrobial agents. Med Res Rev. 2004;24(4): 475–528. doi: 10.1002/med.20000 15170593

38. Dardonville C. Recent advances in antitrypanosomal chemotherapy: patent literature 2002–2004. Expert Opin Ther Pat. 2005;15(9): 1241–57.

39. Vanden Eynde JJ, Mayence A, Huang TL, Collins MS, Rebholz S, Walzer PD, Cushion MT. Novel bisbenzamidines as potential drug candidates for the treatment of Pneumocystis carinii pneumonia. Bioorg Med Chem Lett. 2004;14(17): 4545–8. doi: 10.1016/j.bmcl.2004.06.034 15357989

40. Huang TL, Tao B, Quarshie Y, Queener SF, Donkor IO. N, N′-Bis [4-(N-alkylamidino) phenyl] homopiperazines as anti-Pneumocystis carinii agents. Bioorg Med Chem Lett. 2001;11(20): 2679–8. doi: 10.1016/s0960-894x(01)00541-8 11591500

41. Cortesi R, Esposito E. Distamycins: Strategies for possible enhancement of activity and specificity. Mini Rev Med Chem. 2010;10(3): 217–30. doi: 10.2174/138955710791185055 20408803

42. Howard OM, Oppenheim JJ, Hollingshead MG, Covey JM, Bigelow J, McCormack JJ, Buckheit RW Jr, Clanton DJ, Turpin JA, Rice WG. Inhibition of in vitro and in vivo HIV replication by a distamycin analogue that interferes with chemokine receptor function: A candidate for chemotherapeutic and microbicidal application. J Med Chem. 1998;41(13): 2184–93. doi: 10.1021/jm9801253 9632350

43. Dickinson LA, Gulizia RJ, Trauger JW, Baird EE, Mosier DE, Gottesfeld JM, et al. Inhibition of RNA polymerase II transcription in human cells by synthetic DNA-binding ligands. Proc Natl Acad Sci U S A. 1998;95(22): 12890–5. doi: 10.1073/pnas.95.22.12890 9789010

44. Tutter A, Jones KA. Chemicals that footprint DNA: Hitting HIV-1 in the minor groove. Proc Nat Acad of Sci U S A. 1998;95(22): 12739–41.

45. Fitzgibbon JE, Mazar S, Dubin DT. A new type of G—>A hypermutation affecting human immunodeficiency virus. AIDS Res Hum Retroviruses. 1993;9(9): 833–8. doi: 10.1089/aid.1993.9.833 7504935

46. Vartanian JP, Plikat U, Henry M, Mahieux R, Guillemot L, Meyerhans A. Wain-Hobson S. HIV genetic variation is directed and restricted by DNA precursor availability. J Mol Biol. 1997;270(2): 139–51. doi: 10.1006/jmbi.1997.1104 9236117

47. Nussinov R. Compositional variations in DNA sequences. Comput Appl Biosci. 1991;7(3): 287–93. doi: 10.1093/bioinformatics/7.3.287 1913208

48. Phillips MD, Nascimbeni B, Tice RR, Shelby MD. Induction of micronuclei in mouse bone marrow cells: an evaluation of nucleoside analogues used in the treatment of AIDS. Environ Mol Mutagen. 1991;18(3): 168–83. doi: 10.1002/em.2850180305 1915312

49. Rogers DJ. Trypanosomiasis' risk'or'challenge': a review. Acta Trop. 1985;42(1): 5–23. 2859750

50. Tidwell RR, Jones SK, Geratz JD, Ohemeng KA, Cory M, Hall JE. Analogs of 1, 5-bis (4-amidinophenoxy) pentane (pentamidine) in the treatment of experimental Pneumocystis carinii pneumonia. J Med Chem. 1990;33(4): 1252–7. doi: 10.1021/jm00166a026 2319567

51. Connor TH, Trizna ZJTl. Pentamidine isethionate is negative in tests for microbial mutagenicity and chromosomal breakage in vitro. Toxicol Lett. 1992;63(1): 69–74. doi: 10.1016/0378-4274(92)90108-v 1412524

52. Boos G, Stopper H. Genotoxicity of several clinically used topoisomerase II inhibitors. Toxicol Lett. 2000;116(1–2): 7–16. doi: 10.1016/s0378-4274(00)00192-2 10906417

53. Bielawski K, Bielawska A, Poplawska B, Bolkun-Skornicka U. Synthesis, DNA-binding affinity and cytotoxicity of the dinuclear platinum(II) complexes with berenil and amines ligands. Acta Pol Pharm. 2008;65(3): 363–70. 18646556

54. Sou K, Goins B, Oyajobi BO, Travi BL, Phillips WT. Bone marrow-targeted liposomal carriers, Expert Opin Drug Deliv. 2011;8(3): 317–328. doi: 10.1517/17425247.2011.553218 21275831

55. Xiao Q, Guo D, Chen S. Application of CRISPR/Cas9-Based Gene Editing in HIV-1/AIDS Therapy. Front Cell Infect Microbiol. 2019;9: 69. doi: 10.3389/fcimb.2019.00069 30968001

56. Yarrington RM, Verma S, Schwartz S, Trautman JK, and Carroll D. Nucleosomes inhibit target cleavage by CRISPR-Cas9 in vivo. Proc Natl Acad Sci U S A. 2018;115(38): 9351–9358. doi: 10.1073/pnas.1810062115 30201707

57. Jensen KT, Fløe L, Petersen TS, Huang J, Xu F, Bolund L, Luo Y, Lin L. Chromatin accessibility and guide sequence secondary structure affect CRISPR‐Cas9 gene editing efficiency. FEBS Lett. 2017;591: 1892–1901. doi: 10.1002/1873-3468.12707 28580607

58. Uusi-Mäkelä MIE, Barker HR, Bäuerlein CA, Häkkinen T, Nykter M, Rämet M. Chromatin accessibility is associated with CRISPR-Cas9 efficiency in the zebrafish (Danio rerio). PLoS One. 2018;13(4): e0196238. doi: 10.1371/journal.pone.0196238 29684067

59. Neamati N, Mazumder A, Sunder S, Owen JM, Tandon M, Lown JW, Pommier Y. Highly potent synthetic polyamides, bisdistamycins, and lexitropsins as inhibitors of human immunodeficiency virus type 1 integrase. Mol Pharmacol. 1998;54(2): 280–90. doi: 10.1124/mol.54.2.280 9687569

60. Reddy BS, Sondhi SM, Lown JW. Synthetic DNA minor groove-binding drugs. Pharmacol Ther. 1999;84(1): 1–111. doi: 10.1016/s0163-7258(99)00021-2 10580832

61. Sudarsanam P, Winston F. The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. Trends Genet. 2000;16(8): 345–51. doi: 10.1016/s0168-9525(00)02060-6 10904263

62. Gurova KV, Chromatin Stability as a Target for Cancer Treatment. Bioessays. 2019; 41(1): e18000141.

63. Satchwell SC, Drew HR, Travers AA. Sequence periodicities in chicken nucleosome core DNA. J Mol Biol 1986;191(4): 659–675. doi: 10.1016/0022-2836(86)90452-3 3806678

64. Collings CK, Fernandez AG, Pitschka CG, Hawkins TB, Anderson JN. Oligonucleotide Sequence Motifs as Nucleosome Positioning Signals. PLoS One. 2010;5(6): e10933. doi: 10.1371/journal.pone.0010933 20532171

65. Collings CK, Waddell PJ, Anderson JN. Effects of DNA methylation on nucleosome stability. Nucleic Acids Res. 2013;41(5): 2918–31. doi: 10.1093/nar/gks893 23355616

66. Collings CK, Anderson JN. Links between DNA methylation and nucleosome occupancy in the human genome. Epigenetics & Chromatin. 2017;10(1): 18.

67. Fitzgerald DJ, Bronson EC, Anderson JN. Compositional similarities between the human immunodeficiency virus and surface antigens of pathogens. AIDS Res Hum Retroviruses 1996; 12: 99–106. doi: 10.1089/aid.1996.12.99 8834459

68. Tan VY. Effects of minor groove binding drugs on nucleosome assembly disruption and positioning of surface antigen genes from parasites. Unpublished Master’s thesis. 2007; Purdue University, West Lafayette, Indiana 47906.

69. Schmid M, Feichtinger W, Jessberger A, Köhler J, Lange R. The fragile site (16) (q22): Induction by AT-specific DNA-ligands and population frequency. Hum Genet. 1986;74(1): 67–73. doi: 10.1007/bf00278788 3759087

70. Sarni D, Kerem B. The complex nature of fragile site plasticity and its importance in cancer. Curr Opin Cell Biol. 2016;40: 131–6. doi: 10.1016/j.ceb.2016.03.017 27062332

71. Hsu YY, Wang YH. Human fragile site FRA16B DNA excludes nucleosomes in the presence of distamycin. J Biol Chem. 2002;277(19): 17315–9. doi: 10.1074/jbc.M200901200 11880377

72. Yu S, Mangelsdorf M, Hewett D, Hobson L, Baker E, Eyre HJ, Lapsys N, Le Paslier D, Doggett NA, Sutherland GR, Richards RI. Human chromosomal fragile site FRA16B is an amplified AT-rich minisatellite repeat. Cell. 1997;88(3): 367–74. doi: 10.1016/s0092-8674(00)81875-9 9039263

HIV chromatin is a preferred target for drugs that bind in the DNA minor groove

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