Skip to main content
PMC home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1985 Sep;5(9):2221–2230. doi: 10.1128/mcb.5.9.2221

Lens-specific promoter activity of a mouse gamma-crystallin gene.

S Lok, M L Breitman, A B Chepelinsky, J Piatigorsky, R J Gold, L C Tsui
PMCID: PMC366947  PMID: 3837188

Abstract

Crystallins are the major water-soluble proteins in vertebrate eye lenses. These lens-specific proteins are encoded by several gene families, and their expression is differentially regulated during lens cell differentiation. Here we show that a cloned mouse gamma-crystallin promoter is active in lens explants derived from 14-day-old chicken embryos but inactive in a variety of cells of non-lens origin. We also show that sequences required for proper utilization of this promoter are contained between nucleotide positions -392 and +47 relative to the transcription initiation site; deletion of sequences from positions -392 to -171 completely abolishes promoter activity. Since chickens do not have gamma-crystallin genes, the expression of a mouse gamma-crystallin promoter in chicken lens cells suggests that different classes of crystallin genes may be regulated by common lens tissue-specific mechanism(s) independent of species.

Full text

PDF
2221

Images in this article

2225Image
on p.2225
2226Image
on p.2226
2227Image
on p.2227
2228Image
on p.2228

Selected References

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

  1. Banerji J., Olson L., Schaffner W. A lymphocyte-specific cellular enhancer is located downstream of the joining region in immunoglobulin heavy chain genes. Cell. 1983 Jul;33(3):729–740. doi: 10.1016/0092-8674(83)90015-6. [DOI] [PubMed] [Google Scholar]
  2. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  3. Blundell T., Lindley P., Miller L., Moss D., Slingsby C., Tickle I., Turnell B., Wistow G. The molecular structure and stability of the eye lens: x-ray analysis of gamma-crystallin II. Nature. 1981 Feb 26;289(5800):771–777. doi: 10.1038/289771a0. [DOI] [PubMed] [Google Scholar]
  4. Borrás T., Nickerson J. M., Chepelinsky A. B., Piatigorsky J. Structural and functional evidence for differential promoter activity of the two linked delta-crystallin genes in the chicken. EMBO J. 1985 Feb;4(2):445–452. doi: 10.1002/j.1460-2075.1985.tb03649.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Breitman M. L., Lok S., Wistow G., Piatigorsky J., Tréton J. A., Gold R. J., Tsui L. C. Gamma-crystallin family of the mouse lens: structural and evolutionary relationships. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7762–7766. doi: 10.1073/pnas.81.24.7762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chao M. V., Mellon P., Charnay P., Maniatis T., Axel R. The regulated expression of beta-globin genes introduced into mouse erythroleukemia cells. Cell. 1983 Feb;32(2):483–493. doi: 10.1016/0092-8674(83)90468-3. [DOI] [PubMed] [Google Scholar]
  7. Chepelinsky A. B., King C. R., Zelenka P. S., Piatigorsky J. Lens-specific expression of the chloramphenicol acetyltransferase gene promoted by 5' flanking sequences of the murine alpha A-crystallin gene in explanted chicken lens epithelia. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2334–2338. doi: 10.1073/pnas.82.8.2334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Delaye M., Tardieu A. Short-range order of crystallin proteins accounts for eye lens transparency. 1983 Mar 31-Apr 6Nature. 302(5907):415–417. doi: 10.1038/302415a0. [DOI] [PubMed] [Google Scholar]
  9. Falkner F. G., Zachau H. G. Expression of mouse immunoglobulin genes in monkey cells. Nature. 1982 Jul 15;298(5871):286–288. doi: 10.1038/298286a0. [DOI] [PubMed] [Google Scholar]
  10. Gannon F., O'Hare K., Perrin F., LePennec J. P., Benoist C., Cochet M., Breathnach R., Royal A., Garapin A., Cami B. Organisation and sequences at the 5' end of a cloned complete ovalbumin gene. Nature. 1979 Mar 29;278(5703):428–434. doi: 10.1038/278428a0. [DOI] [PubMed] [Google Scholar]
  11. Garber A. T., Gold R. J. Comparative two-dimensional electrophoretic analysis of water soluble proteins from bovine and murine lenses. Exp Eye Res. 1982 Dec;35(6):585–596. doi: 10.1016/s0014-4835(82)80072-9. [DOI] [PubMed] [Google Scholar]
  12. Gaynor R. B., Hillman D., Berk A. J. Adenovirus early region 1A protein activates transcription of a nonviral gene introduced into mammalian cells by infection or transfection. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1193–1197. doi: 10.1073/pnas.81.4.1193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gillies S. D., Morrison S. L., Oi V. T., Tonegawa S. A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell. 1983 Jul;33(3):717–728. doi: 10.1016/0092-8674(83)90014-4. [DOI] [PubMed] [Google Scholar]
  14. Gluzman Y. SV40-transformed simian cells support the replication of early SV40 mutants. Cell. 1981 Jan;23(1):175–182. doi: 10.1016/0092-8674(81)90282-8. [DOI] [PubMed] [Google Scholar]
  15. Gorman C. M., Merlino G. T., Willingham M. C., Pastan I., Howard B. H. The Rous sarcoma virus long terminal repeat is a strong promoter when introduced into a variety of eukaryotic cells by DNA-mediated transfection. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6777–6781. doi: 10.1073/pnas.79.22.6777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
  18. Green M. R., Treisman R., Maniatis T. Transcriptional activation of cloned human beta-globin genes by viral immediate-early gene products. Cell. 1983 Nov;35(1):137–148. doi: 10.1016/0092-8674(83)90216-7. [DOI] [PubMed] [Google Scholar]
  19. Gruss P., Khoury G. Expression of simian virus 40-rat preproinsulin recombinants in monkey kidney cells: use of preproinsulin RNA processing signals. Proc Natl Acad Sci U S A. 1981 Jan;78(1):133–137. doi: 10.1073/pnas.78.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Harding J. J., Dilley K. J. Structural proteins of the mammalian lens: a review with emphasis on changes in development, aging and cataract. Exp Eye Res. 1976 Jan;22(1):1–73. doi: 10.1016/0014-4835(76)90033-6. [DOI] [PubMed] [Google Scholar]
  21. King C. R., Piatigorsky J. Alternative RNA splicing of the murine alpha A-crystallin gene: protein-coding information within an intron. Cell. 1983 Mar;32(3):707–712. doi: 10.1016/0092-8674(83)90056-9. [DOI] [PubMed] [Google Scholar]
  22. Kondoh H., Yasuda K., Okada T. S. Tissue-specific expression of a cloned chick delta-crystallin gene in mouse cells. Nature. 1983 Feb 3;301(5899):440–442. doi: 10.1038/301440a0. [DOI] [PubMed] [Google Scholar]
  23. Larsen A., Weintraub H. An altered DNA conformation detected by S1 nuclease occurs at specific regions in active chick globin chromatin. Cell. 1982 Jun;29(2):609–622. doi: 10.1016/0092-8674(82)90177-5. [DOI] [PubMed] [Google Scholar]
  24. Loenen W. A., Brammar W. J. A bacteriophage lambda vector for cloning large DNA fragments made with several restriction enzymes. Gene. 1980 Aug;10(3):249–259. doi: 10.1016/0378-1119(80)90054-2. [DOI] [PubMed] [Google Scholar]
  25. Lok S., Tsui L. C., Shinohara T., Piatigorsky J., Gold R., Breitman M. Analysis of the mouse gamma-crystallin gene family: assignment of multiple cDNAs to discrete genomic sequences and characterization of a representative gene. Nucleic Acids Res. 1984 Jun 11;12(11):4517–4529. doi: 10.1093/nar/12.11.4517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McDevitt D. S., Croft L. R. On the existence of gamma-crystallin in the bird lens. Exp Eye Res. 1977 Nov;25(5):473–481. doi: 10.1016/0014-4835(77)90176-2. [DOI] [PubMed] [Google Scholar]
  28. Meakin S. O., Breitman M. L., Tsui L. C. Structural and evolutionary relationships among five members of the human gamma-crystallin gene family. Mol Cell Biol. 1985 Jun;5(6):1408–1414. doi: 10.1128/mcb.5.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mellon P., Parker V., Gluzman Y., Maniatis T. Identification of DNA sequences required for transcription of the human alpha 1-globin gene in a new SV40 host-vector system. Cell. 1981 Dec;27(2 Pt 1):279–288. doi: 10.1016/0092-8674(81)90411-6. [DOI] [PubMed] [Google Scholar]
  30. Moormann R. J., Jongbloed R., Schoenmakers J. G. Isolation and characterization of beta- and gamma-crystallin genes from rat genomic cosmid libraries. Gene. 1984 Jul-Aug;29(1-2):1–9. doi: 10.1016/0378-1119(84)90159-8. [DOI] [PubMed] [Google Scholar]
  31. Moormann R. J., den Dunnen J. T., Mulleners L., Andreoli P., Bloemendal H., Schoenmakers J. G. Strict co-linearity of genetic and protein folding domains in an intragenically duplicated rat lens gamma-crystallin gene. J Mol Biol. 1983 Dec 25;171(4):353–368. doi: 10.1016/0022-2836(83)90034-7. [DOI] [PubMed] [Google Scholar]
  32. Mulligan R. C., Berg P. Expression of a bacterial gene in mammalian cells. Science. 1980 Sep 19;209(4463):1422–1427. doi: 10.1126/science.6251549. [DOI] [PubMed] [Google Scholar]
  33. Ochi A., Hawley R. G., Hawley T., Shulman M. J., Traunecker A., Köhler G., Hozumi N. Functional immunoglobulin M production after transfection of cloned immunoglobulin heavy and light chain genes into lymphoid cells. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6351–6355. doi: 10.1073/pnas.80.20.6351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Orkin S. H., Sexton J. P., Cheng T. C., Goff S. C., Giardina P. J., Lee J. I., Kazazian H. H., Jr ATA box transcription mutation in beta-thalassemia. Nucleic Acids Res. 1983 Jul 25;11(14):4727–4734. doi: 10.1093/nar/11.14.4727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Papaconstantinou J. Biochemistry of bovine lens proteins. II. The gamma-crystallins of adult bovine, calf and embryonic lenses. Biochim Biophys Acta. 1965 Aug 24;107(1):81–90. doi: 10.1016/0304-4165(65)90390-9. [DOI] [PubMed] [Google Scholar]
  36. Papaconstantinou J. Molecular aspects of lens cell differentiation. Science. 1967 Apr 21;156(3773):338–346. doi: 10.1126/science.156.3773.338. [DOI] [PubMed] [Google Scholar]
  37. Parker B. A., Stark G. R. Regulation of simian virus 40 transcription: sensitive analysis of the RNA species present early in infections by virus or viral DNA. J Virol. 1979 Aug;31(2):360–369. doi: 10.1128/jvi.31.2.360-369.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Piatigorsky J. Delta crystallins and their nucleic acids. Mol Cell Biochem. 1984;59(1-2):33–56. doi: 10.1007/BF00231304. [DOI] [PubMed] [Google Scholar]
  39. Piatigorsky J. Lens crystallins and their gene families. Cell. 1984 Oct;38(3):620–621. doi: 10.1016/0092-8674(84)90254-x. [DOI] [PubMed] [Google Scholar]
  40. Piatigorsky J. Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation. 1981;19(3):134–153. doi: 10.1111/j.1432-0436.1981.tb01141.x. [DOI] [PubMed] [Google Scholar]
  41. Piatigorsky J., Rothschild S. S., Milstone L. M. Differentiation of lens fibers in explanted embryonic chick lens epithelia. Dev Biol. 1973 Oct;34(2):334–345. doi: 10.1016/0012-1606(73)90362-x. [DOI] [PubMed] [Google Scholar]
  42. Piatigorsky J., Webster H. D., Craig S. P. Protein synthesis and ultrastructure during the formation of embryonic chick lens fibers in vivo and in vitro. Dev Biol. 1972 Feb;27(2):176–189. doi: 10.1016/0012-1606(72)90096-6. [DOI] [PubMed] [Google Scholar]
  43. Picard D., Schaffner W. A lymphocyte-specific enhancer in the mouse immunoglobulin kappa gene. Nature. 1984 Jan 5;307(5946):80–82. doi: 10.1038/307080a0. [DOI] [PubMed] [Google Scholar]
  44. Queen C., Baltimore D. Immunoglobulin gene transcription is activated by downstream sequence elements. Cell. 1983 Jul;33(3):741–748. doi: 10.1016/0092-8674(83)90016-8. [DOI] [PubMed] [Google Scholar]
  45. Razin A., Riggs A. D. DNA methylation and gene function. Science. 1980 Nov 7;210(4470):604–610. doi: 10.1126/science.6254144. [DOI] [PubMed] [Google Scholar]
  46. Sassone-Corsi P., Corden J., Kédinger C., Chambon P. Promotion of specific in vitro transcription by excised "TATA" box sequences inserted in a foreign nucleotide environment. Nucleic Acids Res. 1981 Aug 25;9(16):3941–3958. doi: 10.1093/nar/9.16.3941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Shinohara T., Robinson E. A., Appella E., Piatigorsky J. Multiple gamma-crystallins of the mouse lens: fractionation of mRNAs by cDNA cloning. Proc Natl Acad Sci U S A. 1982 May;79(9):2783–2787. doi: 10.1073/pnas.79.9.2783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  49. Stafford J., Queen C. Cell-type specific expression of a transfected immunoglobulin gene. Nature. 1983 Nov 3;306(5938):77–79. doi: 10.1038/306077a0. [DOI] [PubMed] [Google Scholar]
  50. Stein R., Ziff E. B. HeLa cell beta-tubulin gene transcription is stimulated by adenovirus 5 in parallel with viral early genes by an E1a-dependent mechanism. Mol Cell Biol. 1984 Dec;4(12):2792–2801. doi: 10.1128/mcb.4.12.2792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Tréton J. A., Jones R. E., King C. R., Piatigorsky J. Evidence against gamma-crystallin DNA or RNA sequences in the chicken. Exp Eye Res. 1984 Oct;39(4):513–522. doi: 10.1016/0014-4835(84)90051-4. [DOI] [PubMed] [Google Scholar]
  53. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  54. Walker M. D., Edlund T., Boulet A. M., Rutter W. J. Cell-specific expression controlled by the 5'-flanking region of insulin and chymotrypsin genes. Nature. 1983 Dec 8;306(5943):557–561. doi: 10.1038/306557a0. [DOI] [PubMed] [Google Scholar]
  55. Weaver R. F., Weissmann C. Mapping of RNA by a modification of the Berk-Sharp procedure: the 5' termini of 15 S beta-globin mRNA precursor and mature 10 s beta-globin mRNA have identical map coordinates. Nucleic Acids Res. 1979 Nov 10;7(5):1175–1193. doi: 10.1093/nar/7.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Wigler M., Sweet R., Sim G. K., Wold B., Pellicer A., Lacy E., Maniatis T., Silverstein S., Axel R. Transformation of mammalian cells with genes from procaryotes and eucaryotes. Cell. 1979 Apr;16(4):777–785. doi: 10.1016/0092-8674(79)90093-x. [DOI] [PubMed] [Google Scholar]
  57. Wistow G., Turnell B., Summers L., Slingsby C., Moss D., Miller L., Lindley P., Blundell T. X-ray analysis of the eye lens protein gamma-II crystallin at 1.9 A resolution. J Mol Biol. 1983 Oct 15;170(1):175–202. doi: 10.1016/s0022-2836(83)80232-0. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES