Human polyomavirus JC promoter/enhancer rearrangement patterns from progressive multifocal leukoencephalopathy brain are unique derivatives of a single archetypal structure Free

Abstract

We have compared the promoter/enhancer structure of human polyomavirus JC (JCV) isolates from 11 progressive multifocal leukoencephalopathy brains. The duplications and deletions of the regulatory region were different in each patient, and usually only one sequence was found in each. The sites of strand breakage in the promoter were not random; four or five preferred sites or areas exist. Alignment of the JCV prototype Mad-1 regulatory region with the unduplicated archetypal structure defines six blocks of sequence, A to F. The preferred sites of strand breaks delineate these regions, although Mad-1 is an unusual promoter containing a break site not observed in other isolates, and an additional site is targeted in several promoters. Region A, containing the TATA box, and the first half of region C, containing several enhancer elements, and region E are consistently retained. Region B, the 23 bp insertion in the archetypal structure (relative to Mad-1) was also retained in all 11 isolates. Region D, the 66 bp insertion, was retained in isolates from three patients. Regions A and D were never duplicated, whereas regions C and E usually were duplicated or triplicated. Variation in the exact point of breakage within the preferred sites, alternative use of the sites in individual promoters and occasional short deletions at other sites result in sequences that are unique in each case. At the same time, the limited choice of break sites and the characteristic fates of the regions themselves result in three broad patterns of repeat sequences. The patterns do not correspond to the viral genotypes 1 and 2 defined by coding region base changes, and do not appear to be a stable feature of the virus. Rather, rearrangements appear to be generated in the host from a basic archetypal sequence.

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1993-08-01
2024-03-28
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References

  1. Amemiya K, Traub R, Durham L, Major EO. 1989; Interaction of a nuclear factor-1-like protein with the regulatory region of the human polyomavirus JC virus. . Journal of Biological Chemistry 264:7025–7032
    [Google Scholar]
  2. Amemiya K, Traub R, Durham L, Major EO. 1992; Adjacent nuclear factor-1 and activator protein binding sites in the enhancer of the neurotropic JC virus. A common characteristic of many brain-specific genes. . Journal of Biological Chemistry 267:14204–14211
    [Google Scholar]
  3. Arthur RR, Shah KV. 1989; Occurrence and significance of papovaviruses BK and JC in the urine.. Progress in Medical Virology 36:42–61
    [Google Scholar]
  4. Aster JC, Sklar J. 1992; Interallelic V(D)J trans-rearrangement within the beta T cell receptor gene is infrequent and occurs preferentially during attempted D beta to J beta joining.. Journal of Experimental Medicine 175:1773–1782
    [Google Scholar]
  5. Atwood WJ, Amemiya K, Traub R, Harms J, Major EO. 1992; Interaction of the human polyomavirus, JCV, with human B-lymphocytes.. Virology 190:716–723
    [Google Scholar]
  6. Ault GS, Stoner GL. 1992; Two major types of JC virus defined in progressive multifocal leukoencephalopathy brain by early and late coding region DNA sequences. . Journal of General Virology 73:2669–2678
    [Google Scholar]
  7. Beckmann AM, Shah KV. 1983; Propagation and primary isolation of JCV and BKV in urinary epithelial cell cultures. . Progress in Clinical and Biological Research 105:3–14
    [Google Scholar]
  8. Beckmann AM, Shah KV, Padgett BL. 1982; Propagation and primary isolation of papovavirus JC in epithelial cells derived from human urine.. Infection and Immunity 38:774–777
    [Google Scholar]
  9. Berger JR, Kaszovitz B, Post MJ, Dickinson G. 1987; Progressive multifocal leukoencephalopathy associated with human immunodeficiency virus infection. A review of the literature with a report of sixteen cases.. Annals of Internal Medicine 107:78–87
    [Google Scholar]
  10. Bollag RJ, Waldman AS, Liskay RM. 1989; Homologous recombination in mammalian cells.. Annual Review of Genetics 23:199–225
    [Google Scholar]
  11. Chowdhury M, Taylor JP, Tada H, Rappaport J, Wong-Staal F, Amini S, Khalili K. 1990; Regulation of the human neurotropic virus promoter by JCV-T antigen and HIV-1 tat protein.. Oncogene 5:1737–1742
    [Google Scholar]
  12. Chowdhury M, Taylor JP, Chang CF, Rappaport J, Khalili K. 1992; Evidence that a sequence similar to TAR is important for induction of the JC virus late promoter by human immunodeficiency virus type 1 Tat. . Journal of Virology 66:7355–7361
    [Google Scholar]
  13. Devereux J, Haeberli P, Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX.. Nucleic Acids Research 12:387–395
    [Google Scholar]
  14. Dynan WS, Chervitz SA. 1989; Characterization of a minimal simian virus 40 late promoter: enhancer elements in the 72-base-pair repeat not required.. Journal of Virology 63:1420–1427
    [Google Scholar]
  15. Eggleston AK, Kowalczykowski SC. 1991; An overview of homologous pairing and DNA strand exchange proteins.. Biochimie 73:163–176
    [Google Scholar]
  16. Fareed GC, Takemoto KK, Gimbrone MA, Jr. 1978; Interaction of simian virus 40 and human papovaviruses, BK and JC, with human vascular endothelial cells. In Microbiology427–431 Edited by D. Schlessinger. Washington, D.C.: American Society for Microbiology;
    [Google Scholar]
  17. Feigenbaum L, Khalili K, Major E, Khoury G. 1987; Regulation of the host range of human papovavirus JCV.. Proceedings of the National Academy of Sciences, U.S.A. 84:3695–3698
    [Google Scholar]
  18. Flaegstad T, Sundsfjord A, Arthur RR, Pedersen M, Traavik T, Subramani S. 1991; Amplification and sequencing of the control regions of BK and JC virus from human urine by polymerase chain reaction.. Virology 180:553–560
    [Google Scholar]
  19. Frisque RJ, White FA, Ill. 1992; The molecular biology of JC virus, causative agent of progressive multifocal leukoencephalopathy. In Neurovirology: Pathogenesis of Viral CNS Infections pp. 25–158 Edited by R. P. Roos. Totowa: Humana Press;
    [Google Scholar]
  20. Frisque RJ, Bream GL, Cannella MT. 1984; Human polyomavirus JC virus genome. . Journal of Virology 51:458–469
    [Google Scholar]
  21. Fuscoe JC, Zimmerman LJ, Harrington-Brock K, Burnette L, Moore M, Nicklas J, O’Neill J, Albertini R. 1992; V(D)J recombinase-mediated deletion of the hprt gene in T-lymphocytes from adult humans. . Mutation Research 283:13–20
    [Google Scholar]
  22. Grinnell BW, Martin JD, Padgett BL, Walker DL. 1983a; Naturally occurring and passage-induced variation in the genome of JC virus.. Progress in Clinical and Biological Research 105:61–77
    [Google Scholar]
  23. Grinnell BW, Padgett BL, Walker DL. 1983b; Comparison of infectious JC virus DNAs cloned from human brain.. Journal of Virology 45:299–308
    [Google Scholar]
  24. Gruda MC, Alwine JC. 1991; Simian virus 40 (SV40) T-antigen transcriptional activation mediated through the Oct/SPH region of the SV40 late promoter.. Journal of Virology 65:3553–3558
    [Google Scholar]
  25. Hai T, Curran T. 1991; Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity.. Proceedings of the National Academy of Sciences, U.S.A. 88:3720–3724
    [Google Scholar]
  26. Henson J, Saffer J, Furneaux H. 1992; The transcription factor Spl binds to the JC virus promoter and is selectively expressed in glial cells in human brain.. Annals of Neurology 32:72–77
    [Google Scholar]
  27. Hesse JE, Lieber MR, Mizuuchi K, Gellert M. 1989; V(D)J recombination: a functional definition of the joining signals.. Genes and Development 3:1053–1061
    [Google Scholar]
  28. Hogan TF, Padgett BL, Walker DL. 1991; Human polyomaviruses. In Textbook of Human Virology pp. 970–1000 Edited by R. B. Belshe St. Louis: Mosby;
    [Google Scholar]
  29. Kenney S, Natarajan V, Strike D, Khoury G, Salzman NP. 1984; JC virus enhancer-promoter active in human brain cells.. Science 226:1337–1339
    [Google Scholar]
  30. Kerr D, Khalili K. 1991; A recombinant cDNA derived from human brain encodes a DNA binding protein that stimulates transcription of the human neurotropic virus JCV.. Journal of Biological Chemistry 266:15876–15881
    [Google Scholar]
  31. Khalili K, Rappaport J, Khoury G. 1988; Nuclear factors in human brain cells bind specifically to the JCV regulatory region.. EMBO Journal 7:1205–1210
    [Google Scholar]
  32. Leung H, Maizels N. 1992; Transcriptional regulatory elements stimulate recombination in extrachromosomal substrates carrying immunoglobulin switch-region sequences.. Proceedings of the National Academy of Sciences, U.S.A. 89:4154–4158
    [Google Scholar]
  33. Loeber G, Dorries K. 1988; DNA rearrangements in organ-specific variants of polyomavirus JC strain GS.. Journal of Virology 62:1730–1735
    [Google Scholar]
  34. Lynch KJ, Frisque RJ. 1991; Factors contributing to the restricted DNA replicating activity of JC virus.. Virology 180:306–317
    [Google Scholar]
  35. McCance DJ. 1983; Persistence of animal and human papovaviruses in renal and nervous tissues. . Progress in Clinical and Biological Research 105:343–357
    [Google Scholar]
  36. Major E.O, Amemiya K, Elder G, Houff SA. 1990; Glial cells of the human developing brain and B cells of the immune system share a common DNA binding factor for recognition of the regulatory sequences of the human polyomavirus, JCV.. Journal of Neuroscience Research 27:461–471
    [Google Scholar]
  37. Markowitz RB, Dynan WS. 1988; Binding of cellular proteins to the regulatory region of BK virus DNA.. Journal of Virology 62:3388–3398
    [Google Scholar]
  38. Martin JD, King DM, Slauch JM, Frisque RJ. 1985; Differences in regulatory sequences of naturally occurring JC virus variants.. Journal of Virology 53:306–311
    [Google Scholar]
  39. Matsuda M, Jona M, Yasui K, Nagashima K. 1987; Genetic characterization of JC virus Tokyo-1 strain, a variant oncogenic in rodents.. Virus Research 7:159–168
    [Google Scholar]
  40. Miyamura T, Yoshiike K, Takemoto KK. 1980; Characterization of JC papovavirus adapted to growth in human embryonic kidney cells.. Journal of Virology 35:498–504
    [Google Scholar]
  41. Miyamura T, Furuno A, Yoshiike K. 1985; DNA rearrangement in the control region for early transcription in a human polyomavirus JC host range mutant capable of growing in human embryonic kidney cells. . Journal of Virology 54:750–756
    [Google Scholar]
  42. Padgett BL, Walker DL, ZuRhein G.M, Eckroade RJ, Dessel BH. 1971; Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy.. Lancet i,1257–1260
    [Google Scholar]
  43. Padgett BL, Walker DL, ZuRhein G.M, Hodach AE, Chou SM. 1976; JC papovavirus in progressive multifocal leukoencephalopathy.. Journal of Infectious Diseases 133:686–690
    [Google Scholar]
  44. Rubinstein R, Pare N, Harley EH. 1987; Structure and function of the transcriptional control region of nonpassaged BK virus.. Journal of Virology 61:1747–1750
    [Google Scholar]
  45. Schatz DG, Oettinger MA, Schlissel MS. 1992; V(D)J recombination: molecular biology and regulation.. Annual Review of Immunology 10:359–383
    [Google Scholar]
  46. Sock E, Wegner M, Grummt F. 1991; DNA replication of human polyomavirus JC is stimulated by NF-I in vivo. . Virology 182:298–308
    [Google Scholar]
  47. Stoner GL, Ryschkewitsch CF, Walker DL, Webster H.D. 1986; JC papovavirus large tumor (T)-antigen expression in brain tissue of acquired immune deficiency syndrome (AIDS) and non-AIDS patients with progressive multifocal leukoencephalopathy.. Proceedings of the National Academy of Sciences, 83:2271–2275
    [Google Scholar]
  48. Stoner GL, Walker DL, Webster H.D. 1988; Age distribution of progressive multifocal leukoencephalopathy.. Acta neurologica scandinavica 78:307–312
    [Google Scholar]
  49. Sundsfjord A, Johansen T, Flaegstad T, Moens U, Villand P, Subramani S, Traavik T. 1990; At least two types of control regions can be found among naturally occurring BK virus strains.. Journal of Virology 64:3864–3871
    [Google Scholar]
  50. Tada H, Khalh K. 1992; A novel sequence-specific DNA-binding protein, LCP-1, interacts with single-stranded DNA and differentially regulates early gene expression of the human neurotropic JC virus.. Journal of Virology 66:6885–6892
    [Google Scholar]
  51. Tada H, Lashgari M, Rappaport J, Khalili K. 1989; Cell type-specific expression of JC virus early promoter is determined by positive and negative regulation.. Journal of Virology 63:463–166
    [Google Scholar]
  52. Tada H, Rappaport J, Lashgari M, Amini S, Wong-Staal F, Khalili K. 1990; Trans-activation of the JC virus late promoter by the tat protein of type 1 human immunodeficiency virus in glial cells.. Proceedings of the National Academy of Sciences , U.S.A. 87:3479–3483
    [Google Scholar]
  53. Tada H, Lashgari MS, Khalili K. 1991; Regulation of JCVL promoter function: evidence that a pentanucleotide “silencer” repeat sequence AGGGAAGGGA down-regulates transcription of the JC virus late promoter.. Virology 180:327–338
    [Google Scholar]
  54. Tamura T, Indue T, Nagata K, Mikoshiba K. 1988; Enhancer of human polyoma JC virus contains nuclear factor I-binding sequences; analysis using mouse brain nuclear extracts.. Biochemical and Biophysical Research Communications 157:419–425
    [Google Scholar]
  55. Tominaga T, Yogo Y, Nagata K, Kitamura T, Aso Y. 1992; Persistence of archetypal JC virus DNA in normal renal tissue derived from tumor-bearing patients.. Virology 186:736–741
    [Google Scholar]
  56. Tonegawa S. 1992; Somatic generation of antibody diversity.. Nature, London 302:575–581
    [Google Scholar]
  57. Wagatsuma M, Hashimoto K, Matsukura T. 1990; Analysis of integrated human papillomavirus type 16 DNA in cervical cancers: amplification of viral sequences together with cellular flanking sequences.. Journal of Virology 64:813–821
    [Google Scholar]
  58. Walker DL, Frisque RJ. 1986; The biology and molecular biology of JC virus. In The Papovaviridae vol 1 The Polyomaviruses pp. 327–377 Edited by N. P. Salzman. New York: London: Plenum Press;
    [Google Scholar]
  59. Walker DL, Padgett BL. 1983; The epidemiology of human polyomaviruses.. Progress in Clinical and Biological Research 105:99–106
    [Google Scholar]
  60. Wingender E. 1990; Transcription regulating proteins and their recognition sequences.. Critical Reviews in Eukaryotic Gene Expression 1:11–48
    [Google Scholar]
  61. Wuerffel R, Amieson CE, Morgan L, Merkulov GV, Sen R, Kenter AL. 1992; Switch recombination breakpoints are strictly correlated with DNA recognition motifs for immunoglobulin 5 gamma 3 DNA-binding proteins.. Journal of Experimental Medicine 176:339–349
    [Google Scholar]
  62. Yancopoulos GD, Alt FW. 1985; Developmentally controlled and tissue-specific expression of unrearranged VH gene segments.. Cell 40:271–281
    [Google Scholar]
  63. Yano O, Hirano H, Karasaki Y, Higashi K, Nakamura H, Akiya S, Gotoh S. 1991; Cloning and sequencing of viral integration site in human fibroblasts immortalized by simian virus 40.. Cell Structure and Function 16:63–71
    [Google Scholar]
  64. Yogo Y, Kitamura T, Sugimoto C, Veki T, Aso Y, Hara K, Taguchi F. 1990; Isolation of a possible archetypal JC virus DNA sequence from nonimmunocompromised individuals.. Journal of Virology 64:3139–3143
    [Google Scholar]
  65. Yoshiike K, Takemoto KK. 1986; Studies with BK virus and monkey lymphotrophic papovavirus. In The Papovaviridae vol 1 The Polyomaviruses pp. 295–326 Edited by N. P. Salzman. New York: London: Plenum Press;
    [Google Scholar]
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