Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1997 Aug;71(8):5972–5981. doi: 10.1128/jvi.71.8.5972-5981.1997

VBP and RelA regulate avian leukosis virus long terminal repeat-enhanced transcription in B cells.

S M Curristin 1, K J Bird 1, R J Tubbs 1, A Ruddell 1
PMCID: PMC191853  PMID: 9223487

Abstract

The avian leukosis virus (ALV) long terminal repeat (LTR) contains a compact transcription enhancer that is active in many cell types. A major feature of the enhancer is multiple CCAAT/enhancer element motifs that could be important for the strong transcriptional activity of this unit. The contributions of the three CCAAT/enhancer elements to LTR function were examined in B cells, as this cell type is targeted for ALV tumor induction following integration of LTR sequences next to the c-myc proto-oncogene. One CCAAT/enhancer element, termed a3, was found to be the most critical for LTR enhancement in transiently transfected B lymphoma cells, while in chicken embryo fibroblasts all three elements contributed equally to enhancement. Gel shift assays demonstrated that vitellogenin gene-binding protein (VBP), a member of the PAR subfamily of C/EBP factors, is a major component of the nuclear proteins binding to the a3 CCAAT/enhancer element. VBP activated transcription through the a3 CCAAT/enhancer element, supporting the idea that VBP is important for LTR enhancement in B cells. A member of the Rel family of proteins was also identified as a component of the a3 protein binding complex in B cells. Gel shift and immunoprecipitation assays indicated that this factor is RelA. Gel shift assays demonstrated that while RelA does not bind directly to the LTR CCAAT/enhancer elements, it does interact with VBP to potentiate VBP DNA binding activity. The synergistic interaction of VBP and RelA increased CCAAT/enhancer element-mediated transcription, indicating that both factors may be important for viral LTR regulation and also for expression of many cellular genes.

Full Text

The Full Text of this article is available as a PDF (1.7 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akira S., Isshiki H., Sugita T., Tanabe O., Kinoshita S., Nishio Y., Nakajima T., Hirano T., Kishimoto T. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 1990 Jun;9(6):1897–1906. doi: 10.1002/j.1460-2075.1990.tb08316.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alber T. Structure of the leucine zipper. Curr Opin Genet Dev. 1992 Apr;2(2):205–210. doi: 10.1016/s0959-437x(05)80275-8. [DOI] [PubMed] [Google Scholar]
  3. Baba T. W., Giroir B. P., Humphries E. H. Cell lines derived from avian lymphomas exhibit two distinct phenotypes. Virology. 1985 Jul 15;144(1):139–151. doi: 10.1016/0042-6822(85)90312-5. [DOI] [PubMed] [Google Scholar]
  4. Baeuerle P. A., Henkel T. Function and activation of NF-kappa B in the immune system. Annu Rev Immunol. 1994;12:141–179. doi: 10.1146/annurev.iy.12.040194.001041. [DOI] [PubMed] [Google Scholar]
  5. Ballard D. W., Walker W. H., Doerre S., Sista P., Molitor J. A., Dixon E. P., Peffer N. J., Hannink M., Greene W. C. The v-rel oncogene encodes a kappa B enhancer binding protein that inhibits NF-kappa B function. Cell. 1990 Nov 16;63(4):803–814. doi: 10.1016/0092-8674(90)90146-6. [DOI] [PubMed] [Google Scholar]
  6. Baranger A. M., Palmer C. R., Hamm M. K., Giebler H. A., Brauweiler A., Nyborg J. K., Schepartz A. Mechanism of DNA-binding enhancement by the human T-cell leukaemia virus transactivator Tax. Nature. 1995 Aug 17;376(6541):606–608. doi: 10.1038/376606a0. [DOI] [PubMed] [Google Scholar]
  7. Birkenmeier E. H., Gwynn B., Howard S., Jerry J., Gordon J. I., Landschulz W. H., McKnight S. L. Tissue-specific expression, developmental regulation, and genetic mapping of the gene encoding CCAAT/enhancer binding protein. Genes Dev. 1989 Aug;3(8):1146–1156. doi: 10.1101/gad.3.8.1146. [DOI] [PubMed] [Google Scholar]
  8. Bizub D., Katz R. A., Skalka A. M. Nucleotide sequence of noncoding regions in Rous-associated virus-2: comparisons delineate conserved regions important in replication and oncogenesis. J Virol. 1984 Feb;49(2):557–565. doi: 10.1128/jvi.49.2.557-565.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bowers W. J., Baglia L. A., Ruddel A. Regulation of avian leukosis virus long terminal repeat-enhanced transcription by C/EBP-Rel interactions. J Virol. 1996 May;70(5):3051–3059. doi: 10.1128/jvi.70.5.3051-3059.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bowers W. J., Petrosino J. F., Smith C. D., Ruddell A. Transcriptional regulation of ALV bursal lymphomagenesis. Leukemia. 1994 Apr;8 (Suppl 1):S211–S213. [PubMed] [Google Scholar]
  11. Bowers W. J., Ruddell A. a1/EBP: a leucine zipper protein that binds CCAAT/enhancer elements in the avian leukosis virus long terminal repeat enhancer. J Virol. 1992 Nov;66(11):6578–6586. doi: 10.1128/jvi.66.11.6578-6586.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Burch J. B., Davis D. L. Alternative promoter usage and splicing options result in the differential expression of mRNAs encoding four isoforms of chicken VBP, a member of the PAR subfamily of bZIP transcription factors. Nucleic Acids Res. 1994 Nov 11;22(22):4733–4741. doi: 10.1093/nar/22.22.4733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cao Z., Umek R. M., McKnight S. L. Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev. 1991 Sep;5(9):1538–1552. doi: 10.1101/gad.5.9.1538. [DOI] [PubMed] [Google Scholar]
  14. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  15. Chu G., Hayakawa H., Berg P. Electroporation for the efficient transfection of mammalian cells with DNA. Nucleic Acids Res. 1987 Feb 11;15(3):1311–1326. doi: 10.1093/nar/15.3.1311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cooper C., Henderson A., Artandi S., Avitahl N., Calame K. Ig/EBP (C/EBP gamma) is a transdominant negative inhibitor of C/EBP family transcriptional activators. Nucleic Acids Res. 1995 Nov 11;23(21):4371–4377. doi: 10.1093/nar/23.21.4371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Cullen B. R., Raymond K., Ju G. Functional analysis of the transcription control region located within the avian retroviral long terminal repeat. Mol Cell Biol. 1985 Mar;5(3):438–447. doi: 10.1128/mcb.5.3.438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Cullen B. R., Raymond K., Ju G. Transcriptional activity of avian retroviral long terminal repeats directly correlates with enhancer activity. J Virol. 1985 Feb;53(2):515–521. doi: 10.1128/jvi.53.2.515-521.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Diehl J. A., Hannink M. Identification of a C/EBP-Rel complex in avian lymphoid cells. Mol Cell Biol. 1994 Oct;14(10):6635–6646. doi: 10.1128/mcb.14.10.6635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Drolet D. W., Scully K. M., Simmons D. M., Wegner M., Chu K. T., Swanson L. W., Rosenfeld M. G. TEF, a transcription factor expressed specifically in the anterior pituitary during embryogenesis, defines a new class of leucine zipper proteins. Genes Dev. 1991 Oct;5(10):1739–1753. doi: 10.1101/gad.5.10.1739. [DOI] [PubMed] [Google Scholar]
  21. Fonjallaz P., Ossipow V., Wanner G., Schibler U. The two PAR leucine zipper proteins, TEF and DBP, display similar circadian and tissue-specific expression, but have different target promoter preferences. EMBO J. 1996 Jan 15;15(2):351–362. [PMC free article] [PubMed] [Google Scholar]
  22. Ganchi P. A., Sun S. C., Greene W. C., Ballard D. W. A novel NF-kappa B complex containing p65 homodimers: implications for transcriptional control at the level of subunit dimerization. Mol Cell Biol. 1993 Dec;13(12):7826–7835. doi: 10.1128/mcb.13.12.7826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Goodwin G. H. Identification of three sequence-specific DNA-binding proteins which interact with the Rous sarcoma virus enhancer and upstream promoter elements. J Virol. 1988 Jun;62(6):2186–2190. doi: 10.1128/jvi.62.6.2186-2190.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Haas N. B., Cantwell C. A., Johnson P. F., Burch J. B. DNA-binding specificity of the PAR basic leucine zipper protein VBP partially overlaps those of the C/EBP and CREB/ATF families and is influenced by domains that flank the core basic region. Mol Cell Biol. 1995 Apr;15(4):1923–1932. doi: 10.1128/mcb.15.4.1923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hihara H., Shimizu T., Yamamoto H. Establishment of tumor cell lines cultured from chickens with avian lymphoid leukosis. Natl Inst Anim Health Q (Tokyo) 1974 Winter;14(4):163–173. [PubMed] [Google Scholar]
  26. Houtz E. K., Conklin K. F. Identification of EFIV, a stable factor present in many avian cell types that transactivates sequences in the 5' portion of the Rous sarcoma virus long terminal repeat enhancer. J Virol. 1996 Jan;70(1):393–401. doi: 10.1128/jvi.70.1.393-401.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hunger S. P., Ohyashiki K., Toyama K., Cleary M. L. Hlf, a novel hepatic bZIP protein, shows altered DNA-binding properties following fusion to E2A in t(17;19) acute lymphoblastic leukemia. Genes Dev. 1992 Sep;6(9):1608–1620. doi: 10.1101/gad.6.9.1608. [DOI] [PubMed] [Google Scholar]
  28. Ikeda T., Honjo K., Hirota Y., Onodera T. Isolation of the chicken NF-kappa B p65 subunit-encoding cDNA and characterization of its products. Gene. 1993 Nov 15;133(2):237–242. doi: 10.1016/0378-1119(93)90645-j. [DOI] [PubMed] [Google Scholar]
  29. Inaba T., Roberts W. M., Shapiro L. H., Jolly K. W., Raimondi S. C., Smith S. D., Look A. T. Fusion of the leucine zipper gene HLF to the E2A gene in human acute B-lineage leukemia. Science. 1992 Jul 24;257(5069):531–534. doi: 10.1126/science.1386162. [DOI] [PubMed] [Google Scholar]
  30. Iyer S. V., Davis D. L., Seal S. N., Burch J. B. Chicken vitellogenin gene-binding protein, a leucine zipper transcription factor that binds to an important control element in the chicken vitellogenin II promoter, is related to rat DBP. Mol Cell Biol. 1991 Oct;11(10):4863–4875. doi: 10.1128/mcb.11.10.4863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Johnson P. F., Landschulz W. H., Graves B. J., McKnight S. L. Identification of a rat liver nuclear protein that binds to the enhancer core element of three animal viruses. Genes Dev. 1987 Apr;1(2):133–146. doi: 10.1101/gad.1.2.133. [DOI] [PubMed] [Google Scholar]
  32. Kenny S., Guntaka R. V. Localization by mutational analysis of transcription factor binding sequences in the U3 region of Rous sarcoma virus LTR. Virology. 1990 Jun;176(2):483–493. doi: 10.1016/0042-6822(90)90018-m. [DOI] [PubMed] [Google Scholar]
  33. Kunsch C., Ruben S. M., Rosen C. A. Selection of optimal kappa B/Rel DNA-binding motifs: interaction of both subunits of NF-kappa B with DNA is required for transcriptional activation. Mol Cell Biol. 1992 Oct;12(10):4412–4421. doi: 10.1128/mcb.12.10.4412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Landschulz W. H., Johnson P. F., McKnight S. L. The DNA binding domain of the rat liver nuclear protein C/EBP is bipartite. Science. 1989 Mar 31;243(4899):1681–1688. doi: 10.1126/science.2494700. [DOI] [PubMed] [Google Scholar]
  35. Landt O., Grunert H. P., Hahn U. A general method for rapid site-directed mutagenesis using the polymerase chain reaction. Gene. 1990 Nov 30;96(1):125–128. doi: 10.1016/0378-1119(90)90351-q. [DOI] [PubMed] [Google Scholar]
  36. Lernbecher T., Müller U., Wirth T. Distinct NF-kappa B/Rel transcription factors are responsible for tissue-specific and inducible gene activation. Nature. 1993 Oct 21;365(6448):767–770. doi: 10.1038/365767a0. [DOI] [PubMed] [Google Scholar]
  37. Linial M., Gunderson N., Groudine M. Enhanced transcription of c-myc in bursal lymphoma cells requires continuous protein synthesis. Science. 1985 Dec 6;230(4730):1126–1132. doi: 10.1126/science.2999973. [DOI] [PubMed] [Google Scholar]
  38. Liou H. C., Sha W. C., Scott M. L., Baltimore D. Sequential induction of NF-kappa B/Rel family proteins during B-cell terminal differentiation. Mol Cell Biol. 1994 Aug;14(8):5349–5359. doi: 10.1128/mcb.14.8.5349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Majors J. The structure and function of retroviral long terminal repeats. Curr Top Microbiol Immunol. 1990;157:49–92. doi: 10.1007/978-3-642-75218-6_3. [DOI] [PubMed] [Google Scholar]
  40. Mueller C. R., Maire P., Schibler U. DBP, a liver-enriched transcriptional activator, is expressed late in ontogeny and its tissue specificity is determined posttranscriptionally. Cell. 1990 Apr 20;61(2):279–291. doi: 10.1016/0092-8674(90)90808-r. [DOI] [PubMed] [Google Scholar]
  41. Nolan G. P. NF-AT-AP-1 and Rel-bZIP: hybrid vigor and binding under the influence. Cell. 1994 Jun 17;77(6):795–798. doi: 10.1016/0092-8674(94)90126-0. [DOI] [PubMed] [Google Scholar]
  42. Nordeen S. K. Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques. 1988 May;6(5):454–458. [PubMed] [Google Scholar]
  43. Norton P. A., Coffin J. M. Bacterial beta-galactosidase as a marker of Rous sarcoma virus gene expression and replication. Mol Cell Biol. 1985 Feb;5(2):281–290. doi: 10.1128/mcb.5.2.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Norton P. A., Coffin J. M. Characterization of Rous sarcoma virus sequences essential for viral gene expression. J Virol. 1987 Apr;61(4):1171–1179. doi: 10.1128/jvi.61.4.1171-1179.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Pabo C. O., Sauer R. T. Transcription factors: structural families and principles of DNA recognition. Annu Rev Biochem. 1992;61:1053–1095. doi: 10.1146/annurev.bi.61.070192.005201. [DOI] [PubMed] [Google Scholar]
  46. Perini G., Wagner S., Green M. R. Recognition of bZIP proteins by the human T-cell leukaemia virus transactivator Tax. Nature. 1995 Aug 17;376(6541):602–605. doi: 10.1038/376602a0. [DOI] [PubMed] [Google Scholar]
  47. Petropoulos L., Lin R., Hiscott J. Human T cell leukemia virus type 1 tax protein increases NF-kappa B dimer formation and antagonizes the inhibitory activity of the I kappa B alpha regulatory protein. Virology. 1996 Nov 1;225(1):52–64. doi: 10.1006/viro.1996.0574. [DOI] [PubMed] [Google Scholar]
  48. Ray A., Hannink M., Ray B. K. Concerted participation of NF-kappa B and C/EBP heteromer in lipopolysaccharide induction of serum amyloid A gene expression in liver. J Biol Chem. 1995 Mar 31;270(13):7365–7374. doi: 10.1074/jbc.270.13.7365. [DOI] [PubMed] [Google Scholar]
  49. Robinson H. L., Blais B. M., Tsichlis P. N., Coffin J. M. At least two regions of the viral genome determine the oncogenic potential of avian leukosis viruses. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1225–1229. doi: 10.1073/pnas.79.4.1225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Robinson H. L., Ramamoorthy L., Collart K., Brown D. W. Tissue tropism of avian leukosis viruses: analyses for viral DNA and proteins. Virology. 1993 Mar;193(1):443–445. doi: 10.1006/viro.1993.1142. [DOI] [PubMed] [Google Scholar]
  51. Roman C., Platero J. S., Shuman J., Calame K. Ig/EBP-1: a ubiquitously expressed immunoglobulin enhancer binding protein that is similar to C/EBP and heterodimerizes with C/EBP. Genes Dev. 1990 Aug;4(8):1404–1415. doi: 10.1101/gad.4.8.1404. [DOI] [PubMed] [Google Scholar]
  52. Ruddell A., Linial M. L., Groudine M. Tissue-specific lability and expression of avian leukosis virus long terminal repeat enhancer-binding proteins. Mol Cell Biol. 1989 Dec;9(12):5660–5668. doi: 10.1128/mcb.9.12.5660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Ruddell A., Linial M., Schubach W., Groudine M. Lability of leukosis virus enhancer-binding proteins in avian hematopoeitic cells. J Virol. 1988 Aug;62(8):2728–2735. doi: 10.1128/jvi.62.8.2728-2735.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Ruddell A. Transcription regulatory elements of the avian retroviral long terminal repeat. Virology. 1995 Jan 10;206(1):1–7. doi: 10.1016/s0042-6822(95)80013-1. [DOI] [PubMed] [Google Scholar]
  55. Ryden T. A., Beemon K. Avian retroviral long terminal repeats bind CCAAT/enhancer-binding protein. Mol Cell Biol. 1989 Mar;9(3):1155–1164. doi: 10.1128/mcb.9.3.1155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Ryden T. A., de Mars M., Beemon K. Mutation of the C/EBP binding sites in the Rous sarcoma virus long terminal repeat and gag enhancers. J Virol. 1993 May;67(5):2862–2870. doi: 10.1128/jvi.67.5.2862-2870.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Schubach W. H., Horvath G. Alternate structures and stabilities of c-myc RNA in a bursal lymphoma cell line. Nucleic Acids Res. 1988 Dec 9;16(23):11171–11186. doi: 10.1093/nar/16.23.11171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sealey L., Chalkley R. At least two nuclear proteins bind specifically to the Rous sarcoma virus long terminal repeat enhancer. Mol Cell Biol. 1987 Feb;7(2):787–798. doi: 10.1128/mcb.7.2.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Sears R. C., Sealy L. Multiple forms of C/EBP beta bind the EFII enhancer sequence in the Rous sarcoma virus long terminal repeat. Mol Cell Biol. 1994 Jul;14(7):4855–4871. doi: 10.1128/mcb.14.7.4855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Sen R., Baltimore D. Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell. 1986 Dec 26;47(6):921–928. doi: 10.1016/0092-8674(86)90807-x. [DOI] [PubMed] [Google Scholar]
  61. Smidt M. P., Wijnholds J., Snippe L., van Keulen G., Ab G. Binding of a bZip protein to the estrogen-inducible apoVLDL II promoter. Biochim Biophys Acta. 1994 Sep 13;1219(1):115–120. doi: 10.1016/0167-4781(94)90253-4. [DOI] [PubMed] [Google Scholar]
  62. Smith C. D., Baglia L. A., Curristin S. M., Ruddell A. The VBP and a1/EBP leucine zipper factors bind overlapping subsets of avian retroviral long terminal repeat CCAAT/enhancer elements. J Virol. 1994 Oct;68(10):6232–6242. doi: 10.1128/jvi.68.10.6232-6242.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
  64. Speck N. A., Renjifo B., Hopkins N. Point mutations in the Moloney murine leukemia virus enhancer identify a lymphoid-specific viral core motif and 1,3-phorbol myristate acetate-inducible element. J Virol. 1990 Feb;64(2):543–550. doi: 10.1128/jvi.64.2.543-550.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Stein B., Baldwin A. S., Jr Distinct mechanisms for regulation of the interleukin-8 gene involve synergism and cooperativity between C/EBP and NF-kappa B. Mol Cell Biol. 1993 Nov;13(11):7191–7198. doi: 10.1128/mcb.13.11.7191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Stein B., Cogswell P. C., Baldwin A. S., Jr Functional and physical associations between NF-kappa B and C/EBP family members: a Rel domain-bZIP interaction. Mol Cell Biol. 1993 Jul;13(7):3964–3974. doi: 10.1128/mcb.13.7.3964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Stein B., Yang M. X. Repression of the interleukin-6 promoter by estrogen receptor is mediated by NF-kappa B and C/EBP beta. Mol Cell Biol. 1995 Sep;15(9):4971–4979. doi: 10.1128/mcb.15.9.4971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Sun Y. N., Lu J. Z., McCance D. J. Mapping of HPV-11 E1 binding site and determination of other important cis elements for replication of the origin. Virology. 1996 Feb 1;216(1):219–222. doi: 10.1006/viro.1996.0050. [DOI] [PubMed] [Google Scholar]
  69. Wagner S., Green M. R. HTLV-I Tax protein stimulation of DNA binding of bZIP proteins by enhancing dimerization. Science. 1993 Oct 15;262(5132):395–399. doi: 10.1126/science.8211160. [DOI] [PubMed] [Google Scholar]
  70. Wegner M., Cao Z., Rosenfeld M. G. Calcium-regulated phosphorylation within the leucine zipper of C/EBP beta. Science. 1992 Apr 17;256(5055):370–373. doi: 10.1126/science.256.5055.370. [DOI] [PubMed] [Google Scholar]
  71. Yin M. J., Gaynor R. B. Complex formation between CREB and Tax enhances the binding affinity of CREB for the human T-cell leukemia virus type 1 21-base-pair repeats. Mol Cell Biol. 1996 Jun;16(6):3156–3168. doi: 10.1128/mcb.16.6.3156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. de Wet J. R., Wood K. V., DeLuca M., Helinski D. R., Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987 Feb;7(2):725–737. doi: 10.1128/mcb.7.2.725. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES