Skip to main content
SpringerLink
Log in

Evidence for the role of cyclic AMP-responsive elements in human virus replication and disease

  • Review
  • Published:
Journal of Biomedical Science

Abstract

We review the involvement of the cyclic AMP responsive DNA element (CRE) and the ATF/CREB (activating transcription factor/CRE binding protein) family of transcription factors in the regulation and pathology of clinically important viruses that infect humans, including the herpesviridae, adenoviridae, parvoviridae, hepadnaviridae, and retroviridae families. CRE sequences found in specific regulatory elements of human viruses are listed, and the functional evidence for CRE activity, in the form of DNA binding assays, mutational studies, transfection and transcriptional activation experiments, or in vitro transcription assays, is summarized. Manipulation of cellular processes is required for virus replication in human cells following infection. A primary target of many viruses is the cellular transcription machinery, and several human viruses contain transcriptional activator and repressor proteins that affect cellular transcription. Through their effect on cellular transcription, viral genes alter the pattern of cellular gene expression, and thereby affect the differentiation state and cell cycle progression of the infected cell. We summarize evidence demonstrating that the CRE and its binding proteins are involved in the activity of the viruses, implicating their function in the pathogenesis of human diseases. The targeting of specific transcription factor pathways as a potential therapeutic approach is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Agulnick AD, Thompson JR, Ricciardi RP. An ATF/CREB site is the major regulatory element in the human herpesvirus 6 DNA polymerase promoter. J Virol 68(5):2970–2977;1994.

    Google Scholar 

  2. Alberts AS, Arias J, Hagiwara M, Montminy MR, Feramisco JR. Recombinant cyclic AMP response element binding protein (CREB) phosphorylated on Ser-133 is transcriptionally active upon its introduction into fibroblast nuclei. J Biol Chem 269(10):7623–7630;1994.

    Google Scholar 

  3. Alexandre C, Charnay P, Verrier B. Transactivation of Krox-20 and Krox-24 promoters by the HTLV-1 Tax protein through common regulatory elements. Oncogene 6(10):1851–1857;1991.

    Google Scholar 

  4. Arany Z, Sellers WR, Livingston DM, Eckner R. E1A-associated p300 and CREB-associated CBP belong to a conserved family of coactivators [letter]. Cell 77(6):799–800;1994.

    Google Scholar 

  5. Arlt H, Lang D, Gebert S, Stamminger T. Identification of binding sites for the 86-kilodalton IE2 protein of human cytomegalovirus within an IE2-responsive viral early promoter. J Virol 68:4117–4125;1994.

    Google Scholar 

  6. Armstrong AP, Franklin AA, Uittenbogaard MN, Giebler HA, Nyborg JK. Pleiotropic effect of the human T-cell leukemia virus Tax protein on the DNA binding activity of eukaryotic transcription factors. Proc Natl Acad Sci USA 90(15):7303–7307;1993.

    Google Scholar 

  7. Arrand JR, Rymo L. Characterization of the major Epstein-Barr virus-specific RNA in Burkitt lymphoma-derived cells. J Virol 41:376–389;1982.

    Google Scholar 

  8. Benbrook D, Jones N. Different binding specificities and transactivation of variant CRE's by CREB complexes. Nucleic Acids Res 22:1463–1469;1994.

    Google Scholar 

  9. Blundell MC, Astell CR. A GC-box motif upstream of the B19 parvovirus unique promoter is important for in vitro transcription. J Virol 63(11):4814–4823;1989.

    Google Scholar 

  10. Borrelli E, Montmayeur JP, Foulkes NS, Sassone CP. Signal transduction and gene control: the cAMP pathway. Crit Rev Oncog 3(4):321–338;1992.

    Google Scholar 

  11. Boshart M, Weber F, Jahn G, Dorsch-Hasler K, Fleckenstein B, Schaffner W. A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell 41:521–530;1985.

    Google Scholar 

  12. Brindle PK, Montminy MR. The CREB family of transcription activators. Curr Opin Genet Dev 2(2):199–204;1992.

    Google Scholar 

  13. Cann AJ. Principles of Molecular Virology. San Diego, Academic Press, Inc., 1993.

    Google Scholar 

  14. Cen H, McKnight JL. EBV-immortalized isogenic human B-cell clones exhibit differences in DNA-protein complex formation on the BZLF1 and BRLF1 promoter regions among latent lytic, and TPA-activated cell lines. Virus Res 31(1):89–107;1994.

    Google Scholar 

  15. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, Moore PS. Identification of herpesvirus-like DNA sequences in AIDS associated Kaposi's sarcoma. Science 266:1865–1869;1994.

    Google Scholar 

  16. Chang YN, Crawford S, Stall J, Rawlins DR, Jeang KT, Hayward GS. The palindromic series I repeats in the simian cytomegalovirus major immediate-early promoter behave as both strong basal enhancers and cyclic AMP response elements. J Virol 64(1):264–277;1990.

    Google Scholar 

  17. Chang YN, Dong DL, Hayward GS, Hayward SD. The Epstein-Barr virus Zta transactivator: a member of the bZIP family with unique DNA-binding specificity and a dimerization domain that lacks the characteristic heptad leucine zipper motif. J Virol 64(7):3358–3369;1990.

    Google Scholar 

  18. Chatton B, Bocco JL, Gaire M, Hauss C, Reimund B, Goetz J, Kedinger C. Transcriptional activation by the adenovirus larger E1a product is mediated by members of the cellular transcription factor ATF family which can directly associate with E1a. Mol Cell Biol 13(1):561–570;1993.

    Google Scholar 

  19. Chen D, Rothenberg EV. Molecular basis for developmental changes in interleukin-2 gene inducibility. Mol Cell Biol 13(1):228–237;1993.

    Google Scholar 

  20. Chen DS. From hepatitis to hepatoma: Lessons learned from type B hepatitis. Science 262:369–370;1993.

    Google Scholar 

  21. Cole TJ, Copeland NG, Gilbert DJ, Jenkins NA, Schutz G, Ruppert S. The mouse CREB (cAMP responsive element binding protein) gene: structure, promoter analysis, and chromosomal localization. Genomics 13(4):974–982;1992.

    Google Scholar 

  22. Cotmore SR, Tattersall P. An asymetric nucleotide in the parvoviral 3′ hairpin directs segregation of a single active origin of DNA replication. EMBO J 13(17):4145–4152;1994.

    Google Scholar 

  23. Deb SP, Deb S, Brown DR. Cell-type-specific induction of the UL9 gene of HSV-1 by cell signalling pathway. Biochem Biophys Res Comm 205(1):44–51;1994.

    Google Scholar 

  24. Deutsch PJ, Hoeffler JP, Jameson JL, Lin JC, Habener JF. Structural determinants for transcriptional activation by cAMP responsive DNA elements. J Biol Chem 263:18466–18472;1988.

    Google Scholar 

  25. Doerig C, Beard P, Hirt B. A transcriptional promoter of the human parvovirus B19 active in vitro and in vivo. Virology 157:539–542;1987.

    Google Scholar 

  26. Doerig C, Pizer LI, Wilcox CL. An antigen encoded by the latency-associated transcript in neuronal cell cultures latently infected with herpes simplex virus type 1. J Virol 65(5):2724–2727;1991.

    Google Scholar 

  27. Dong Z, Birrer MJ, Watts RG, Matrisian LM, Colburn NH. Blocking of tumor promoter-induced AP-1 activity inhibits induced transformation in JB6 mouse epidermal cells. Proc Natl Acad Sci USA 91:609–613;1994.

    Google Scholar 

  28. Dulbecco R, Ginsberg HS. Virology. (2 ed.) Philadelphia: J.B. Lippincott Co., 1988.

    Google Scholar 

  29. Fahraeus R, Palmqvist L, Nerdstedt A, Farzad S, Rymo L, Lain S. Response to cAMP levels of the Epstein-Barr virus EBNA2-inducible LMP1 oncogene and EBNA2 inhibition of a PP1-like activity. EMBO J 13(24):6041–6051;1994.

    Google Scholar 

  30. Faisst S, Perros M, Deleu L, Spruyt N, Rommelaere J. Mapping of upstream regulatory elements in the P4 promoter of parvovirus minute virus of mice. Virology 202(1):466–470;1994.

    Google Scholar 

  31. Fields BN, Knipe DM, Chanock RM, Hirsch MS, Melnick JL, Monath TP, Roizman B. Fields Virology. New York, Raven Press;1990.

    Google Scholar 

  32. Flemington E, Speck SH. Identification of phorobol ester response elements in the promoter of Epstein-Barr virus putative lytic switch gene BZLF1. J Virol 64(3):1217–1226;1990.

    Google Scholar 

  33. Flint J, Shenk T. Adenovirus E1A protein paradigm viral transactivator. Annu Rev Genet 23:141–161;1989.

    Google Scholar 

  34. Foulkes NS, Borrelli E, Sassone CP. CREM gene: use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription. Cell 64(4):739–749;1991.

    Google Scholar 

  35. Foulkes NS, Sassone-Corsi P. More is better: activators and repressors from the same gene. Cell 68:411–414;1992.

    Google Scholar 

  36. Franklin AA, Kubik MF, Uittenbogaard MN, Brauweiler A, Utaisincharoen P, Matthews MA, Dynan WS, Hoeffler JP, Nyborg JK. Transactivation by the human T-cell leukemia virus Tax protein is mediated through enhanced binding of activating transcription factor-2 (ATF-2) ATF-2 response and cAMP element-binding protein (CREB). J Biol Chem 268(28):21225–21231;1993.

    Google Scholar 

  37. Gibbs JB, Oliff A. Pharmaceutical research in molecular oncology. Cell 79:193–198;1994.

    Google Scholar 

  38. Gilchrist CA, Orten DJ, Bosilevac JM, Sanderson DS, Hinrichs SH. Transcriptional inhibition by a monoclonal antibody Fab fragment. Antibody, Immunoconj Radiopharm 8(4):281–298;1995.

    Google Scholar 

  39. Gonzalez GA, Montminy MR. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59(4):675–680;1989.

    Google Scholar 

  40. Hai T, Horikoshi M, Roeder RG, Green MR. Analysis of the transcription factor ATF in the assembly of a functional preinitiation complex. Cell 54:1043–1051;1988.

    Google Scholar 

  41. Hinrichs SH, Harrison CJ, Haggerty S. Viral diseases. Chapter 36 In: Anderson's Pathology, Damjanov I and Linder J, eds. St. Louis, Mosby-Year Book;1996.

    Google Scholar 

  42. Hipskind RA, Nordheim A. Functional dissection in vitro of the human c-fos promoter. J Biol Chem 266(29):19583–19592;1991.

    Google Scholar 

  43. Howe JG, Shu MD. Epstein-Barr virus small RNA (EBER) genes: unique transcription units that combine RNA polymerase II and III promoter elements. Cell 57(5):825–834;1989.

    Google Scholar 

  44. Hu K-Q, Siddiqui A. Regulation of the hepatitis B virus gene expression by the enhancer element I. Virology 181:721–726;1991.

    Google Scholar 

  45. Hurst HC, Masson N, Jones NC, Lee KA. The cellular transcription factor CREB corresponds to activating transcription factor 47 (ATF-47) and forms complexes with a group of polypeptides related to ATF-43. Mol Cell Biol 10(12):6192–6203;1990.

    Google Scholar 

  46. Jeang KT, Rawlins DR, Rosenfeld PJ, Shero JH, Kelly TJ, Hayward GS. Multiple tandemly-repeated binding sites for cellular nuclear factor I upstream from the promoter enhancer region for the major immediate-early gene of cytomegalovirus (Colburn). J Virol 61:1559–1570;1987.

    Google Scholar 

  47. Jeang KT, Boros I, Brady J, Radonovich M, Khoury G. Characterization of cellular factors that interact with the human T-cell leukemia virus type I p40x-responsive 21-base pair sequence. J Virol 62:4499–4509;1988.

    Google Scholar 

  48. Johnson KW, Davis BW, Smith KW. cAMP antagonizes interleukin 2-promoted T-cell cycle progression at a discrete point in early G1. Proc Natl Acad Sci USA 85:6072–6076;1988.

    Google Scholar 

  49. Kammer GM. The adenylate cyclase cAMP-protein kinase A pathway and regulation of the immune response. Immunol Today 9:222–229;1988.

    Google Scholar 

  50. Karpinski BA, Morle GD, Huggenvik J, Uhler MD, Leiden JM. Molecular cloning of human CREB-2: an ATF/CREB transcription factor that can negatively regulate transcription from the cAMP response element. Proc Natl Acad Sci USA 89(11):4820–4824;1992.

    Google Scholar 

  51. Kelly D, O'Reilly MA, Rizzino A. Differential regulation of the transforming growth factor type-beta 2 gene promoter in embryonal carcinoma cells and their differentiated cells. Dev Biol 153(1):172–175;1992.

    Google Scholar 

  52. Kenny JJ, Krebs FC, Hartle HT, Gartner AE, Chatton B, Leiden JM, Hoeffler JP, Weber PC, Wigdahl B. Identification of a second ATF/CREB-like element in the herpes simplex virus type 1 (HSV-1) latency-associated transcript (LAT) promoter. Virology 200(1):220–235;1994.

    Google Scholar 

  53. Kieff E, Dambaugh T, Hummel M, Heller M. Epstein-Barr virus transformation and replication. In: Klein G. Advances in Viral Oncology. Vol 3. New York, Raven Press, 133–182;1983.

    Google Scholar 

  54. Kirch H-C, Putzer B, Schwabe G, Gnauck HKA, Holthausen HS. Regulation of adenovirus 12 E1A transcription: E2F and ATF motifs in the E1A promoter bind nuclear protein complexes including E2F1, DP-1, cyclin A and/or Rb and mediate transcriptional (auto)activation. Cell Mol Biol Res 39(8):705–716;1993.

    Google Scholar 

  55. Kitajima I, Shinohara T, Bilakovics J, Brown DA, Xu X, Nerenberg M. Ablation of transplanted HTLV-I Tax-transformed tumors in mice by antisense inhibition of NF-kB. Science 258:1792–1795;1992.

    Google Scholar 

  56. Konig P, Richmond TJ. The X-ray structure of the GCN-4-bZIP bound to ATF/CREB site DNA shows the complex depends on DNA flexibility. J Mol Biol 233(1):139–154;1993.

    Google Scholar 

  57. Kouzarides T, Bankier AT, Satchwell SC, Weston K, Tomlinson P, Barrell BG. Sequence and transcription analysis of the human cytomegalovirus DNA polymerase gene. J Virol 61(1):125–133;1987.

    Google Scholar 

  58. Labrie C, Lee BH, Mathews MB. Transcription factors RFX1/EF-C and ATF-1 associate with the adenovirus E1A-responsive element of the human proliferating cell nuclear antigen promoter. Nucleic Acids Res 23(18):3732–3741;1995.

    Google Scholar 

  59. Labrie C, Morris GF, Mathews MB. A complex promoter element mediates transactivation of the human proliferating cell nuclear antigen promoter by the 243-residue adenovirus E1A oncoprotein. Mol Cell Biol 13(3):1697–1707;1993.

    Google Scholar 

  60. Lalli E, Sassone-Corsi P. Signal transduction and gene regulation: The nuclear response to cAMP. J Biol Chem 269:17359–17362;1994.

    Google Scholar 

  61. Lam PY, Jadhav PK, Eyermann CJ, Hodge CN, Ru Y, Bacheler LT, Meek JL, Otto MJ, Rayner MM, Wong YN et al. Rational design of potent, bioavailable, nonpeptide cyclic ureas as HIV protease inhibitors. Science 263:380–384;1994.

    Google Scholar 

  62. Lang D, Gebert S, Arlth H, Stamminger T. Functional interaction between the human cytomegalovirus 86-kilodalton IE2 protein and the cellular transcription factor CREB. J Virol 69(10):6030–6037;1995.

    Google Scholar 

  63. Lee KA, Hai TY, SivaRaman L, Thimmappaya B, Hurst HC, Jones NC, Green MR. A cellular protein, activating transcription factor, activates transcription of multiple E1A-inducible adenovirus early promoters. Proc Natl Acad Sci USA 84(23):8355–8359;1987.

    Google Scholar 

  64. Lee KA, Masson N. Transcriptional regulation by CREB and its relatives. Biochim Biophys Acta 1174(3):221–233;1993.

    Google Scholar 

  65. Leib DA, Nadeau KC, Rundle SA, Schaffer PA. The promoter of the latency-associated transcripts of herpes simplex virus type 1 contains a functional cAMP-response element: role of the latency-associated transcripts and cAMP in reactivation of viral latency. Proc Natl Acad Sci USA 88(1):48–52;1991.

    Google Scholar 

  66. Lillie JW, Hai T, Coukos WJ, Lee AW, Martin KJ, Green MR. Transcriptional activation of adenoviral early genes. Curr Top Microbiol Immunol 144:191–195;1989.

    Google Scholar 

  67. Liu F, Green MR. A specific member of the ATF transcription factor family can mediate transcription activation by the adenovirus E1a protein. Cell 61(7):1217–1224;1990.

    Google Scholar 

  68. Liu F, Green MR. Promoter targeting by adenovirus E1a through interaction with different cellular DNA-binding domains. Nature 368:520–525;1994.

    Google Scholar 

  69. Liu JM, Green SW, Shimada T, Young NS. A block in full-length transcript maturation in cells nonpermissive for B19 parvovirus. J Virol 66(8):4686–4692;1992.

    Google Scholar 

  70. Lukac DM, Manuppello JR, Alwine JC. Transcriptional activation by the human cytomegalovirus immediate-early proteins: requirements for simple promoter structures and interactions with multiple components of the transcription complex. J Virol 68(8):5184–5193;1994.

    Google Scholar 

  71. Lusso P, De Maria A, Malnati M, Lori F, DeRocco SE, Baseler M, Gallo RC. Induction of CD4 and susceptibility to HIV-1 infection in human CD8+ T lymphocytes by human herpesvirus 6. Nature 349:533–535;1991.

    Google Scholar 

  72. Lusso P, Markham PD, Tschachler E, DiMarzo Veronese F, Salahuddin SZ, Ablashi DV, Pahwa S, Krohn K, Gallo RC. In vitro cellular tropism of human B-lymphotropic virus (human herpes virus-6). J Exp Med 1671:1659–1670;1988.

    Google Scholar 

  73. Maekawa T, Matsuda S, Fujisawa J, Yoshida M, Ishii S. Cyclic AMP response element-binding protein, CRE-BP1, mediates the E1A-induced but not the Tax-induced trans-activation. Oncogene 6(4):627–632;1991.

    Google Scholar 

  74. Maguire HF, Hoeffler JP, Siddiqui A. HBV X protein alters the DNA binding specificity of CREB and ATF-2 by protein-protein interactions. Science 252(5007):842–844;1991.

    Google Scholar 

  75. Mantovani R, Pessara U, Tronche F, Li XY, Knapp AM, Pasquali JL, Benoist C, Mathis D. Monoclonal antibodies to NF-Y define its function in MHC class II and albumin gene transcription. EMBO J 11:3315–3322;1992.

    Google Scholar 

  76. Masquilier D, Sassone CP. Transcriptional cross-talk: nuclear factors CREM and CREB bind to AP-1 sites and inhibit activation by jun. J Biol Chem 267(31):22460–22466;1992.

    Google Scholar 

  77. Masson N, Hurst HC, Lee KA. Identification of proteins that interact with CREB during differentiation of F9 embryonal carcinoma cells. Nucleic Acids Res 21(11):1163–1169;1993.

    Google Scholar 

  78. McKee TA, Preston CM. Identification of two protein binding sites within the varicella-zoster virus major immediate early gene promoter. Virus Res 20(1):59–69;1991.

    Google Scholar 

  79. Meyer TE, Habener JF. Cyclic adenosine 3′,5′-monophosphate response element binding protein (CREB) and related transcription-activating deoxyribonucleic acid-binding proteins. Endocr Rev 14(3):269–290;1993.

    Google Scholar 

  80. Meyer TE, Waeber G, Lin J, Beckmann W, Habener JF. The promoter of the gene encoding 3′,5′-cyclic adenosine monophosphate (cAMP) response element binding protein contains cAMP response elements: evidence for positive autoregulation of gene transcription. Endocrinology 132(2):770–780;1993.

    Google Scholar 

  81. Nolan GP. NF-AT-AP-1 and Rel-bZIP: Hybrid vigor and binding under the influence. Cell 77:795–798;1994.

    Google Scholar 

  82. Northrop JP, Ullman KS, Crabtree GR. Characterization of the nuclear and cytoplasmic components of the lymphoid-specific nuclear factor of activated T cells (NF-AT) complex. J Biol Chem 268:2917–2923;1993.

    Google Scholar 

  83. O'Reilly MA, Geiser AG, Kim SJ, Bruggeman LA, Luu AX, Roberts AB, Sporn MB. Identification of an activating transcription factor (ATF) binding site in the human transforming growth factor-beta 2 promoter. J Biol Chem 267(28):19938–19943;1992.

    Google Scholar 

  84. Orten DJ, Strawhecker JM, Sanderson SD, Huang D, Prystowsky MB, Hinrichs SH. Differential effects of monoclonal antibodies on activating transcription factor-1 and cAMP response element binding protein interactions with DNA. J Biol Chem 269(51):32254–32263;1994.

    Google Scholar 

  85. Ozawa K, Kurtzman G, Young N. Productive infection by B19 parvovirus of human erythroid bone marrow cells in vitro. Blood 70(2):384–391;1987.

    Google Scholar 

  86. Paca-Uccaralertkun S, Zhao LJ, Adya N, Cross JV, Cullen BR, Boros I, Giam CZ. In vitro selection of DNA elements highly responsive to the human T-cell lymphotropic virus type I transcriptional activator. Tax. Mol Cell Biol 14:456–462;1994.

    Google Scholar 

  87. Peterson M, Vaichwal V. Transcription factor based therapeutics: Drugs of the future? Tib Tech 11:1–9;1993.

    Google Scholar 

  88. Radonovich M, Jeang KT. Activation of the human T-cell leukemia virus type I long terminal repeat by 12-0-tetradecanoyphorbol-13-acetate and by Tax (p40x) occurs through similar but functionally distinct target sequences. J Virol 63:2987–2994;1989.

    Google Scholar 

  89. Rhode SL, Paradiso PR. Parvovirus genome: nucleotide sequence of H-1 and mapping of its genes by hybrid-arrested translation. J Virol 45(1):173–184;1983.

    Google Scholar 

  90. Rowe WP, Huebner RT, Gilmore LK, Parrott RH, Ward TG. Isolation of a cytopathic agent from human adenoids undergoing spontaneous degeneration in tissue culture. Proc Soc Exp Biol Med 84:570–573;1953.

    Google Scholar 

  91. Salahuddin SZ, Ablashi DV, Markham PD, Josephs SF, Sturzenegger S, Kaplan M, Halligan G, Biberfeld P, Wong-Staal F, Kramersky B, Gallo RC. Isolation of a new virus, HBLV, in patients with lymphoproliferative disorders. Science 234:596–601;1986.

    Google Scholar 

  92. Shenk TE. Chapter 8. In: Moore SS. Emerging Viruses. New York, Oxford University Press, 79–90;1993.

    Google Scholar 

  93. Shimotohno K, Wachsman W, Takahashi Y, Golde DW, Miwa M, Sugimura T, Chen IS. Nucleotide sequence of the 3′ region of an infectious human T-cell leukemia virus type II genome. Proc Natl Acad Sci USA 81(21):6657–6661;1984.

    Google Scholar 

  94. Sim IS. Virus replication: Target functions and events for virus-specific inhibitors. In: Galasso GJ, Whitney RJ and Merrigan TC. Antiviral Agents and Viral Diseases of Man. New York, Raven Press, Ltd, 1–47;1990.

    Google Scholar 

  95. Sodroski J. The human T-cell leukemia virus (HTLV) transactivator (Tax) protein. Biochim Biophys Acta 1114:19–29;1992.

    Google Scholar 

  96. Stevens JG. Human herpesviruses: a consideration of the latent state. Microbiol Rev 53:318–332;1989.

    Google Scholar 

  97. Stevens JG. Overview of herpesvirus latency. Semin Virol 5:191–196;1994.

    Google Scholar 

  98. Sugamura K, Hinuma Y. Human Retroviruses: HTLV-I and HTLV-II. In: Levy JA. The Retroviridae. Vol 2. New York, Plenum Press;1993.

    Google Scholar 

  99. Suzuki T, Fujisawa JI, Toita M, Yoshida M. The trans-activator Tax of human T-cell leukemia virus type 1 (HTLV-1) interacts with cAMP-responsive element (CRE) binding and CRE modulator proteins that bind to the 21-base-pair enhancer of HTLV-1. Proc Natl Acad Sci USA 90(2):610–614;1993.

    Google Scholar 

  100. Thorn JT, Todd AV, Warrilow D, Watt F, Molloy PL, Iland HJ. Characterization of the human N-ras promoter region [published erratum appears in Oncogene 1992 May;7(5):1047]. Oncogene 6(10):1843–1850;1991.

    Google Scholar 

  101. Tillmann M, Wessner R, Wigdahl B. Identification of human T-cell lymphotropic virus type I 21-base pair repeat-specific and glial cell-specific DNA-protein complexes. J Virol 68(7):4597–4608;1994.

    Google Scholar 

  102. Wang K, Krause PR, Straus SE. Analysis of the promoter and cis-acting elements regulating expression of herpes simplex virus type 2 latency-associated transcripts. J Virol 69(5):2873–2880;1995.

    Google Scholar 

  103. Williams JS, Andrisani OM. The hepatitis B virus X protein targets the basic region-leucine zipper domain of CREB. Proc Natl Acad Sci USA 92:3819–3823;1995.

    Google Scholar 

  104. Yen TSB. Regulation of hepatitis B virus gene expression. Semin Virol 4:33–42;1993.

    Google Scholar 

  105. Yin JCP, Wallach JS, Wilder EL, Klingen-smith J, Dang D, Perrimon N, Zhou H, Tully T, Quinn WG. Adrosophila CREB/CREM homolog encodes multiple isoforms, including a cyclic AMP-dependent protein kinase-responsive transcriptional activator and antagonist. Mol Cell Biol 15(9):5123–5130;1995.

    Google Scholar 

  106. Young NS. B19 Parvovirus. In: Young NS. Viruses and Bone Marrow: Basic Research and Clinical Practice. Vol 16. New York, Marcel Dekker, Inc., 75–117;1993.

    Google Scholar 

  107. Zhao LJ, Giam CZ. Human T-cell lymphotropic virus type I (HTLV-I) transcriptional activator, Tax, enhances CREB binding to HTLV-I 21-base-pair repeats by protein-protein interaction. Proc Natl Acad Sci USA 89(15):7070–7074;1992.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pathology and Microbiology, and the Eppley Institute for Cancer Research, University of Nebraska Medical Center, Omaha, Nebr., USA

    Cindy A. Gilchrist, Dana J. Orten & Steven H. Hinrichs MD

Authors
  1. Cindy A. Gilchrist
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dana J. Orten
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Steven H. Hinrichs MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gilchrist, C.A., Orten, D.J. & Hinrichs, S.H. Evidence for the role of cyclic AMP-responsive elements in human virus replication and disease. J Biomed Sci 3, 293–306 (1996). https://doi.org/10.1007/BF02257959

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02257959

Key Words

Search

Navigation