Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1988 Jan 1;106(1):21–27. doi: 10.1083/jcb.106.1.21

Developmentally regulated expression of a Balbiani ring 1 gene for a 180-kD secretory polypeptide in Chironomus tentans salivary glands before larval/pupal ecdysis

PMCID: PMC2114959  PMID: 3339088

Abstract

The expression of a Balbiani ring 1 gene that codes for a salivary gland-specific 180-kD secretory polypeptide (sp180) is regulated developmentally. Immunoblots of salivary gland protein incubated with an affinity-purified nonapeptide-reactive antibody demonstrated that the salivary gland content of sp180 increases as much as 10-fold between stages 8 and 10 of the fourth larval instar. Hybridization of RNA dot-blots with an oligonucleotide probe indicated that the observed increase in sp180 was preceded by a parallel 20-fold increase in the steady state level of its mRNA beginning between stages 7 and 8. In vitro nuclear transcription experiments demonstrated that there was a 10-fold acceleration in the rate of sp180 gene transcription between stages 6 and 10. The limited period of expression of the sp180 gene contrasted dramatically with the expression of Balbiani ring genes BR1, BR2 alpha, BR2 beta, and BR6, which code for the sp-I family of fibrous secretory polypeptides. The appearance of sp180 in secretion coincided with microscopically visible changes in the bundling of these fibrous polypeptides. At the same time, we noticed changes in the appearance and consistency of feeding tubes that larvae construct with this secretion. These results lead us to propose that sp180 may modify the structure or utilization of fibrous secretory polypeptides specifically for the assembly of pupation tubes necessary for larval/pupal ecdysis.

Full Text

The Full Text of this article is available as a PDF (1.9 MB).

Selected References

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

  1. Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [PubMed] [Google Scholar]
  2. Case S. T. Correlated changes in steady-state levels of Balbiani ring mRNAs and secretory polypeptides in salivary glands of Chironomus tentans. Chromosoma. 1986;94(6):483–491. doi: 10.1007/BF00292758. [DOI] [PubMed] [Google Scholar]
  3. Case S. T., Daneholt B. The size of the transcription unit in Balbiani ring 2 of Chironomus tentans as derived from analysis of the primary transcript and 75 S RNA. J Mol Biol. 1978 Sep 5;124(1):223–241. doi: 10.1016/0022-2836(78)90157-2. [DOI] [PubMed] [Google Scholar]
  4. Dreesen T. D., Bower J. R., Case S. T. A second gene in a Balbiani ring. Chironomus salivary glands contain a 6.5-kb poly(A)+ RNA that is transcribed from a hierarchy of tandem repeated sequences in Balbiani ring 1. J Biol Chem. 1985 Sep 25;260(21):11824–11830. [PubMed] [Google Scholar]
  5. Dreesen T. D., Case S. T. A peptide-reactive antibody to a Balbiani ring gene product: immunological evidence that a 6.5-kb RNA in Chironomus tentans salivary glands is mRNA for a 180-kDa nonfibrous component of larval secretion. Gene. 1987;55(1):55–65. doi: 10.1016/0378-1119(87)90248-4. [DOI] [PubMed] [Google Scholar]
  6. Edström J. E., Rydlander L., Francke C. Concomitant induction of a Balbiani ring and a giant secretory protein in Chironomus salivary glands. Chromosoma. 1980;81(1):115–124. doi: 10.1007/BF00292426. [DOI] [PubMed] [Google Scholar]
  7. Edström J. E., Sierakowska H., Burvall K. Dependence of Balbiani ring induction in Chironomus salivary glands on inorganic phosphate. Dev Biol. 1982 May;91(1):131–137. doi: 10.1016/0012-1606(82)90016-1. [DOI] [PubMed] [Google Scholar]
  8. Galler R., Rydlander L., Riedel N., Kluding H., Edström J. E. Balbiani ring induction in phosphate metabolism. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1448–1452. doi: 10.1073/pnas.81.5.1448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Galler R., Saiga H., Widmer R. M., Lezzi M., Edström J. E. Two genes in Balbiani ring 2 with metabolically different 75S transcripts. EMBO J. 1985 Nov;4(11):2977–2982. doi: 10.1002/j.1460-2075.1985.tb04032.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hamodrakas S. J., Kafatos F. C. Structural implications of primary sequences from a family of Balbiani ring-encoded proteins in Chironomus. J Mol Evol. 1984;20(3-4):296–303. doi: 10.1007/BF02104735. [DOI] [PubMed] [Google Scholar]
  11. Hardy P. A., Pelling C. Cell-free synthesis and immunological characterization of salivary proteins from Chironomus tentans. Chromosoma. 1980;81(3):403–417. doi: 10.1007/BF00368152. [DOI] [PubMed] [Google Scholar]
  12. Ineichen H., Meyer B., Lezzi M. Determination of the developmental stage of living fourth instar larvae of Chironomus tentans. Dev Biol. 1983 Aug;98(2):278–286. doi: 10.1016/0012-1606(83)90358-5. [DOI] [PubMed] [Google Scholar]
  13. Kafatos F. C., Jones C. W., Efstratiadis A. Determination of nucleic acid sequence homologies and relative concentrations by a dot hybridization procedure. Nucleic Acids Res. 1979 Nov 24;7(6):1541–1552. doi: 10.1093/nar/7.6.1541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kao W. Y., Case S. T. A novel giant secretion polypeptide in Chironomus salivary glands: implications for another Balbiani ring gene. J Cell Biol. 1985 Sep;101(3):1044–1051. doi: 10.1083/jcb.101.3.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kao W. Y., Case S. T. Individual variations in the content of giant secretory polypeptides in salivary glands of Chironomus. Chromosoma. 1986;94(6):475–482. doi: 10.1007/BF00292757. [DOI] [PubMed] [Google Scholar]
  16. Meyer B., Mähr R., Eppenberger H. M., Lezzi M. The activity of Balbiani rings 1 and 2 in salivary glands of Chironomus tentans larvae under different modes of development and after pilocarpine treatment. Dev Biol. 1983 Aug;98(2):265–277. doi: 10.1016/0012-1606(83)90357-3. [DOI] [PubMed] [Google Scholar]
  17. Pustell J., Kafatos F. C., Wobus U., Bäumlein H. Balbiani ring DNA: sequence comparisons and evolutionary history of a family of hierarchically repetitive protein-coding genes. J Mol Evol. 1984;20(3-4):281–295. doi: 10.1007/BF02104734. [DOI] [PubMed] [Google Scholar]
  18. Rydlander L., Edström J. E. Large sized nascent protein as dominating component during protein synthesis in Chironomus salivary glands. Chromosoma. 1980;81(1):85–99. doi: 10.1007/BF00292424. [DOI] [PubMed] [Google Scholar]
  19. Rydlander L., Pigon A., Edström J. E. Sequences translated by Balbiani ring 75S RNA in vitro are present in giant secretory protein from Chironomus tentans. Chromosoma. 1980;81(1):101–113. doi: 10.1007/BF00292425. [DOI] [PubMed] [Google Scholar]
  20. Wieslander L., Hög C., Hög J. O., Jörnvall H., Lendahl U., Daneholt B. Conserved and nonconserved structures in the secretory proteins encoded in the Balbiani ring genes of Chironomus tentans. J Mol Evol. 1984;20(3-4):304–312. doi: 10.1007/BF02104736. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES