Effects of random mutations in the human immunodeficiency virus type 1 transcriptional promoter on viral fitness in different host cell environments

Journal of Virology

Volumn 80, Issue 13, 2006, Pages 6678-6685

  Van Opijnen, Tim ^a,b   Boerlijst, Maarten C ^b   Berkhout, Ben ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS DNA;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA BINDING; ENVIRONMENTAL CHANGE; GENE MUTATION; HOST CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INTERACTION; RANDOM MUTATION; TRANSCRIPTION REGULATION; VIRUS CELL INTERACTION;

CELL LINE; EVOLUTION, MOLECULAR; GENOME, VIRAL; HIV INFECTIONS; HIV-1; HUMANS; MUTAGENESIS; MUTATION; RESPONSE ELEMENTS; SELECTION (GENETICS);

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33745267732     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02547-05     Document Type: Article

References (70)

1. Beck, Z., A. Bacsi, X. Liu, P. Ebbesen, I. Andirko, E. Csoma, J. Konya, E. Nagy, and F. D. Toth. 2003. Differential patterns of human cytomegalovirus gene expression in various T-cell lines carrying human T-cell leukemia-lymphoma virus type I: role of Tax-activated cellular transcription factors. J. Med. Virol. 71:94-104.
2. Berg, J., S. Willmann, and M. Lassig. 2004. Adaptive evolution of transcription factor binding sites. BMC Evol. Biol. 4:42.
3. Boerlijst, M. C., S. Bonhoeffer, and M. A. Nowak. 1996. Viral quasi-species and recombination. Proc. R. Soc. Lond. B 263:1577-1584.
4. Bonhoeffer, S., C. Chappey, N. T. Parkin, J. M. Whitcomb, and C. J. Petropoulos. 2004. Evidence for positive epistasis in HIV-1. Science 306:1547-1550.
5. Burch, C. L., and L. Chao. 2004. Epistasis and its relationship to canalization in the RNA virus phi 6. Genetics 167:559-567.
6. Carroll, S. B., J. K. Grenier, and S. D. Weatherbee. 2001. From DNA to diversity. Blackwell Scientific, Oxford, United Kingdom.
7. Cartharius, K., K. Frech, K. Grote, M. Haltmeier, A. Klingenhoff, M. Frisch, M. Bayerlein, and T. Werner. 2005. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21:2933-2942.
8. Carvalbo, M., and D. Derse. 1991. Mutational analysis of the equine infectious anemia virus Tat-responsive element. J. Virol. 65:3468-3474.
9. Chen, B. K., M. B. Feinberg, and D. Baltimore. 1997. The κB sites in the human immunodeficiency virus type 1 long terminal repeat enhance virus replication yet are not absolutely required for viral growth. J. Virol. 71:5495-5504.
10. Collins, K. R., M. E. Quinones-Mateu, Z. Toossi, and E. J. Arts. 2002. Impact of tuberculosis on HIV-1 replication, diversity, and disease progression. AIDS Rev. 4:165-176.
11. Dermitzakis, E. T., and A. G. Clark. 2002. Evolution of transcription factor binding sites in Mammalian gene regulatory regions: conservation and turnover. Mol. Biol. Evol. 19:1114-1121.
12. de Visser, J. A., R. F. Hoekstra, and H. van den Ende. 1997. An experimental test for synergistic epistasis and its application in Chlamydomonas. Genetics 145:815-819.
13. de Visser, J. A., J. Hermisson, G. P. Wagner, M. L. Ancel, H. Bagheri-Cbaichian, J. L. Blanchard, L. Chao, J. M. Cheverud, S. F. Elena, W. Fontana, G. Gibson, T. F. Hansen, D. Krakauer, R. C. Lewontin, C. Ofria, S. H. Rice, G. von Dassow, A. Wagner, and M. C. Whitlock. 2003. Perspective: evolution and detection of genetic robustness. Evol. Int. J. Org. Evol. 57:1959-1972.
14. DiLeone, R. J., L. B. Russell, and D. M. Kingsley. 1998. An extensive 3′ regulatory region controls expression of Bmp5 in specific anatomical structures of the mouse embryo. Genetics 148:401-408.
15. Elena, S. F., L. Ekunwe, N. Hajela, S. A. Oden, and R. E. Lenski. 1998. Distribution of fitness effects caused by random insertion mutations in Escherichia coli. Genetica 102/103:349-358.
16. Elena, S. F., and R. E. Lenski. 1997. Test of synergistic interactions among deleterious mutations in bacteria. Nature 390:395-398.
17. Gibson, G. 1996. Epistasis and pleiotropy as natural properties of transcriptional regulation. Theor. Popul. Biol. 49:58-89.
18. Gibson, G., and G. Wagner. 2000. Canalization in evolutionary genetics: a stabilizing theory? Bioessays 22:372-380.
19. Gomez-Gonzalo, M., M. Carretero, J. Rullas, E. Lara-Pezzi, J. Aramburu, B. Berkhout, J. Alcami, and M. Lopez-Cabrera. 2001. The hepatitis B virus X protein induces HIV-1 replication and transcription in synergy with T-cell activation signals: functional roles of NF-kappaB/NF-AT and SP1-binding sites in the HIV-1 long terminal repeat promoter. J. Biol. Chem. 276:35435-35443.
20. Grez, M., M. Zörnig, J. Nowock, and M. Ziegler. 1991. A single point mutation activates the Moloney murine leukemia virus long terminal repeat in embryonal stem cells. J. Virol. 65:4691-4698.
21. Hines, R., B. R. Sorensen, M. A. Shea, and W. Maury. 2004. PU. 1 binding to ets motifs within the equine infectious anemia virus long terminal repeat (LTR) enhancer: regulation of LTR activity and virus replication in macrophages. J. Virol. 78:3407-3418.
22. Jasny, B. R., and L. Roberts. 2004. Genes in action. Science 306:629-650.
23. Jeeninga, R. E., M. Hoogenkamp, M. Armand-Ugon, M. de Baar, K. Verhoef, and B. Berkhout. 2000. Functional differences between the LTR transcriptional promoters of HIV-1 subtypes A through G. J. Virol. 74:3740-3751.
24. Johnson, N. A., and A. H. Porter. 2000. Rapid speciation via parallel, directional selection on regulatory genetic pathways. J. Theor. Biol. 205:527-542.
25. Kammandel, B., K. Chowdhury, A. Stoykova, S. Aparicio, S. Brenner, and P. Gruss. 1999. Distinct cis-essential modules direct the time-space pattern of the Pax6 gene activity. Dev. Biol. 205:79-97.
26. Keightley, P. D., and M. Lynch. 2003. Toward a realistic model of mutations affecting fitness. Evol. Int. J. Org. Evol. 57:683-685.
27. Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge University Press, Cambridge, United Kingdom.
28. Lander, E. S., L. M. Linton, B. Birren, C. Nusbaum, M. C. Zody, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921.
29. Larder, B. A., A. Kohli, P. Kellam, S. D. Kemp, M. Kronick, and R. D. Henfrey. 1993. Quantitative detection of HIV-1 drug resistance mutations by automated DNA sequencing. Nature 365:671-673.
30. Lenski, R. E., M. R. S. Rose, and S. C. S. C. Tadler. 1991. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138:1315-1341.
31. Leung, T. H., A. Hoffmann, and D. Baltimore. 2004. One nucleotide in a kappaB site can determine cofactor specificity for NF-kappaB dimers. Cell 118:453-464.
32. Liu, T., J. Wu, and F. He. 2000. Evolution of cis-acting elements in 5′ flanking regions of vertebrate actin genes. J. Mol. Evol. 50:22-30.
33. Ludwig, M. Z., C. Bergman, N. H. Patel, and M. Kreitman. 2000. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403:564-567.
34. MacArthur, S., and J. F. Brookfield. 2004. Expected rates and modes of evolution of enhancer sequences. Mol. Biol. Evol. 21:1064-1073.
35. Mallon, R., J. Borkowski, R. Albin, S. Pepitoni, J. Schwartz, and E. Kieff. 1990. The Epstein-Barr virus BZLF1 gene product activates the human immunodeficiency virus type 1 5′ long terminal repeat. J. Virol. 64:6282-6285.
36. Maree, A. F., W. Keulen, C. A. Boucher, and R. J. de Boer. 2000. Estimating relative fitness in viral competition experiments. J. Virol. 74:11067-11072.
37. Matsuo, Y., H. G. Drexler, A. Harashima, A. Okochi, N. Shimizu, and K. Orita. 2004. Transcription factor expression in cell lines derived from natural killer-cell and natural killer-like T-cell leukemia-lymphoma. Hum. Cell 17:85-92.
38. Maury, W. 1998. Regulation of equine infectious anemia virus expression. J. Biomed. Sci. 5:11-23.
39. Miralles, R., P. J. Gerrish, A. Moya, and S. F. Elena. 1999. Clonal interference and the evolution of RNA viruses. Science 285:1745-1747.
40. Mohapatra, S., B. Chu, S. Wei, J. Djeu, P. K. Epling-Burnette, T. Loughran, R. Jove, and W. J. Pledger. 2003. Roscovitine inhibits STAT5 activity and induces apoptosis in the human leukemia virus type 1-transformed cell line MT-2. Cancer Res. 63:8523-8530.
41. Novella, I. S., D. D. Reissig, and C. O. Wilke. 2004. Density-dependent selection in vesicular stomatitis virus. J. Virol. 78:5799-5804.
42. Ohta, T. 2002. Near-neutrality in evolution of genes and gene regulation. Proc. Natl. Acad. Sci. USA 99:16134-16137.
43. Orr, H. A. 2003. The distribution of fitness effects among beneficial mutations. Genetics 163:1519-1526.
44. Pastinen, T., and T. J. Hudson. 2004. Cis-acting regulatory variation in the human genome. Science 306:647-650.
45. ELI. Virology 185:661-672.
46. Perelson, A. S., A. U. Neumann, M. Markowitz, J. M. Leonard, and D. D. Ho. 1996. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271:1582-1586.
47. Peters, A. D., and P. D. Keightley. 2000. A test for epistasis among induced mutations in Caenorhabditis elegans. Genetics 156:1635-1647.
48. Quandt, K., K. Frech, H. Karas, E. Wingender, and T. Werner. 1995. MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res. 23:4878-4884.
49. Quivy, V., E. Adam, Y. Collette, D. Demonte, A. Chariot, C. Vanhulle, B. Berkhout, R. Castellano, Y. de Launoit, A. Burny, J. Piette, V. Bours, and C. Van Lint. 2002. Synergistic activation of human immunodeficiency virus type 1 promoter activity by NF-kappaB and inhibitors of deacetylases: potential perspectives for the development of therapeutic strategies. J. Virol. 76:11091-11103.
50. Rice, W. R. 1989. Analyzing tables of statistical tests. Evol. Int. J. Org. Evol. 43:223-225.
51. Rodrigo, A. G., E. G. Shpaer, E. L. Delwart, A. K. Iversen, M. V. Gallo, J. Brojatsch, M. S. Hirsch, B. D. Walker, and J. I. Mullins. 1999. Coalescent estimates of HIV-1 generation time in vivo. Proc. Natl. Acad. Sci. USA 96:2187-2191.
52. Romano, L. A., and G. A. Wray. 2003. Conservation of Endo16 expression in sea urchins despite evolutionary divergence in both cis and trans-acting components of transcriptional regulation. Development 130:4187-4199.
53. Sackerson, C., M. Fujioka, and T. Goto. 1999. The even-skipped locus is contained in a 16-kb chromatin domain. Dev. Biol. 211:39-52.
54. Sanjuan, R., A. Moya, and S. F. Elena. 2004. The contribution of epistasis to the architecture of fitness in an RNA virus. Proc. Natl. Acad. Sci. USA 101:15376-15379.
55. Sanjuan, R., A. Moya, and S. F. Elena. 2004. The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. Proc. Natl. Acad. Sci. USA 101:8396-8401.
56. Segre, D., A. Deluna, G. M. Church, and R. Kishony. 2005. Modular epistasis in yeast metabolism. Nat. Genet. 37:77-83.
57. Smith, S. D., M. Shatsky, P. S. Cohen, R. Warnke, M. P. Link, and B. E. Glader. 1984. Monoclonal antibody and enzymatic profiles of human malignant T-lymphoid cells and derived cell lines. Cancer Res. 44:5657-5660.
58. Stone, J. R., and G. A. Wray. 2001. Rapid evolution of cis-regulatory sequences via local point mutations. Mol. Biol. Evol. 18:1764-1770.
59. Takahashi, H., Y. Mitani, G. Satoh, and N. Satoh. 1999. Evolutionary alterations of the minimal promoter for notochord-specific Brachyury expression in ascidian embryos. Development 126:3725-3734.
60. van Opijnen, T., R. E. Jeeninga, M. C. Boerlijst, G. P. Pollakis, V. Zetterberg, M. Salminen, and B. Berkhout. 2004. Human immunodeficiency virus type 1 subtypes have a distinct long terminal repeat that determines the replication rate in a host-cell-specific manner. J. Virol. 78:3675-3683.
61. van Opijnen, T., J. Kamoschinski, R. E. Jeeninga, and B. Berkhout. 2004. The human immunodeficiency virus type 1 promoter contains a CATA box instead of a TATA box for optimal transcription and replication. J. Virol. 78:6883-6890.
62. Venter, J. C., M. D. Adams, E. W. Myers, P. W. Li, R. J. Mural, G. G. Sutton, H. O. Smith, M. Yandell, C. A. Evans, R. A. Holt, J. D. Gocayne, et al. 2001. The sequence of the human genome. Science 291:1304-1351.
63. Verhoef, K., R. W. Sanders, V. Fontaine, S. Kitajima, and B. Berkhout. 1999. Evolution of the HIV-1 LTR promoter by conversion of an NF-κB enhancer element into a GABP binding site. J. Virol. 73:1331-1340.
64. Weinberger, L. S., J. C. Burnett, J. E. Toettcher, A. P. Arkin, and D. V. Schaffer. 2005. Stochastic gene expression in a lentiviral positive-feedback loop: HIV-1 Tat fluctuations drive phenotypic diversity. Cell 122:169-182.
65. Whitlock, M. C., and D. Bourguet. 2000. Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components. Evol. Int. J. Org. Evol. 54:1654-1660.
66. Wilke, C. O., and C. Adami. 2003. Evolution of mutational robustness. Mutat. Res. 522:3-11.
67. Wolff, C, M. Pepling, P. Gergen, and M. Klingler. 1999. Structure and evolution of a pair-rule interaction element: runt regulatory sequences in D. melanogaster and D. virilis. Mech. Dev. 80:87-99.
68. Wray, G. A., M. W. Hahn, E. Abouheif, J. P. Balhoff, M. Pizer, M. V. Rockman, and L. A. Romano. 2003. The evolution of transcriptional regulation in eukaryotes. Mol. Biol. Evol. 20:1377-1419.
69. Wu, C. Y., and M. D. Brennan. 1993. Similar tissue-specific expression of the Adh genes from different Drosophila species is mediated by distinct arrangements of cis-acting sequences. Mol. Gen. Genet. 240:58-64.
70. Yuh, C. H., H. Bolouri, and E. H. Davidson. 1998. Genomic cis-regulatory logic: experimental and computational analysis of a sea urchin gene. Science 279:1896-1902.