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. 1986 Sep;83(17):6332–6336. doi: 10.1073/pnas.83.17.6332

Nucleotide sequence of the myxobacterial hemagglutinin gene contains four homologous domains.

J M Romeo, B Esmon, D R Zusman
PMCID: PMC386497  PMID: 3092212

Abstract

Myxococcus xanthus, a Gram-negative bacterium, has a complex life cycle that includes fruiting-body formation, a primitive form of multicellular development. Myxobacterial hemagglutinin (MBHA) is a lectin that is induced during the aggregation phase of fruiting-body formation. We have cloned the gene for MBHA and determined its sequence by the dideoxy chain-termination technique. The sequence data show the probable sites for translational initiation and termination and suggest that MBHA does not contain a cleaved leader signal peptide. The DNA sequence shows four strong internal homologies. The deduced amino acid sequence shows that the protein (Mr 27,920) consists of four highly conserved domains each consisting of 67 amino acids. Thus MBHA is physically multivalent in structure, a requirement for all hemagglutinins.

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Selected References

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

  1. Baenziger J. U., Fiete D. Structural determinants of Ricinus communis agglutinin and toxin specificity for oligosaccharides. J Biol Chem. 1979 Oct 10;254(19):9795–9799. [PubMed] [Google Scholar]
  2. Barondes S. H., Cooper D. N., Haywood-Reid P. L. Discoidin I and discoidin II are localized differently in developing Dictyostelium discoideum. J Cell Biol. 1983 Jan;96(1):291–296. doi: 10.1083/jcb.96.1.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barondes S. H., Haywood-Reid P. L., Cooper D. N. Discoidin I, an endogenous lectin, is externalized from Dictyostelium discoideum in multilamellar bodies. J Cell Biol. 1985 Jun;100(6):1825–1833. doi: 10.1083/jcb.100.6.1825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Belasco J. G., Beatty J. T., Adams C. W., von Gabain A., Cohen S. N. Differential expression of photosynthesis genes in R. capsulata results from segmental differences in stability within the polycistronic rxcA transcript. Cell. 1985 Jan;40(1):171–181. doi: 10.1016/0092-8674(85)90320-4. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Cumsky M. G., Zusman D. R. Binding properties of myxobacterial hemagglutinin. J Biol Chem. 1981 Dec 10;256(23):12596–12599. [PubMed] [Google Scholar]
  7. Cumsky M. G., Zusman D. R. Purification and characterization of myxobacterial hemagglutinin, a development-specific lectin of Myxococcus xanthus. J Biol Chem. 1981 Dec 10;256(23):12581–12588. [PubMed] [Google Scholar]
  8. Cumsky M., Zusman D. R. Myxobacterial hemagglutinin: a development-specific lectin of Myxococcus xanthus. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5505–5509. doi: 10.1073/pnas.76.11.5505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Downard J. S., Kupfer D., Zusman D. R. Gene expression during development of Myxococcus xanthus. Analysis of the genes for protein S. J Mol Biol. 1984 Jun 5;175(4):469–492. doi: 10.1016/0022-2836(84)90180-3. [DOI] [PubMed] [Google Scholar]
  10. Dworkin M., Kaiser D. Cell interactions in myxobacterial growth and development. Science. 1985 Oct 4;230(4721):18–24. doi: 10.1126/science.3929384. [DOI] [PubMed] [Google Scholar]
  11. Frazier W. A., Rosen S. D., Reitherman R. W., Barondes S. H. Purification and comparison of two developmentally regulated lectins from Dictyostelium discoideum. Discoidin I and II. J Biol Chem. 1975 Oct 10;250(19):7714–7721. [PubMed] [Google Scholar]
  12. Gabius H. J., Springer W. R., Barondes S. H. Receptor for the cell binding site of discoidin I. Cell. 1985 Sep;42(2):449–456. doi: 10.1016/0092-8674(85)90102-3. [DOI] [PubMed] [Google Scholar]
  13. Gilson E., Higgins C. F., Hofnung M., Ferro-Luzzi Ames G., Nikaido H. Extensive homology between membrane-associated components of histidine and maltose transport systems of Salmonella typhimurium and Escherichia coli. J Biol Chem. 1982 Sep 10;257(17):9915–9918. [PubMed] [Google Scholar]
  14. Gold L., Pribnow D., Schneider T., Shinedling S., Singer B. S., Stormo G. Translational initiation in prokaryotes. Annu Rev Microbiol. 1981;35:365–403. doi: 10.1146/annurev.mi.35.100181.002053. [DOI] [PubMed] [Google Scholar]
  15. Hawley D. K., McClure W. R. Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res. 1983 Apr 25;11(8):2237–2255. doi: 10.1093/nar/11.8.2237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ikemura T. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J Mol Biol. 1981 Sep 25;151(3):389–409. doi: 10.1016/0022-2836(81)90003-6. [DOI] [PubMed] [Google Scholar]
  17. Inouye M., Inouye S., Zusman D. R. Biosynthesis and self-assembly of protein S, a development-specific protein of Myxococcus xanthus. Proc Natl Acad Sci U S A. 1979 Jan;76(1):209–213. doi: 10.1073/pnas.76.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Inouye M., Inouye S., Zusman D. R. Gene expression during development of Myxococcus xanthus: pattern of protein synthesis. Dev Biol. 1979 Feb;68(2):579–591. doi: 10.1016/0012-1606(79)90228-8. [DOI] [PubMed] [Google Scholar]
  19. Inouye S., Franceschini T., Inouye M. Structural similarities between the development-specific protein S from a gram-negative bacterium, Myxococcus xanthus, and calmodulin. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6829–6833. doi: 10.1073/pnas.80.22.6829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Inouye S. Identification of a development-specific promoter of Myxococcus xanthus. J Mol Biol. 1984 Mar 25;174(1):113–120. doi: 10.1016/0022-2836(84)90367-x. [DOI] [PubMed] [Google Scholar]
  21. Konigsberg W., Godson G. N. Evidence for use of rare codons in the dnaG gene and other regulatory genes of Escherichia coli. Proc Natl Acad Sci U S A. 1983 Feb;80(3):687–691. doi: 10.1073/pnas.80.3.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mandel M., Leadbetter E. R. Deoxyribonucleic acid base composition of myxobacteria. J Bacteriol. 1965 Dec;90(6):1795–1796. doi: 10.1128/jb.90.6.1795-1796.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Martinez H. M. An RNA folding rule. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):323–334. doi: 10.1093/nar/12.1part1.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nelson D. R., Cumsky M. G., Zusman D. R. Localization of myxobacterial hemagglutinin in the periplasmic space and on the cell surface of Myxococcus xanthus during developmental aggregation. J Biol Chem. 1981 Dec 10;256(23):12589–12595. [PubMed] [Google Scholar]
  25. Nelson D. R., Zusman D. R. Evidence for long-lived mRNA during fruiting body formation in myxococcus xanthus. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1467–1471. doi: 10.1073/pnas.80.5.1467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nicolson G. L., Blaustein J. The interaction of Ricinus communis agglutinin with normal and tumor cell surfaces. Biochim Biophys Acta. 1972 May 9;266(2):543–547. doi: 10.1016/0005-2736(72)90109-5. [DOI] [PubMed] [Google Scholar]
  27. Perlman D., Halvorson H. O. A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. J Mol Biol. 1983 Jun 25;167(2):391–409. doi: 10.1016/s0022-2836(83)80341-6. [DOI] [PubMed] [Google Scholar]
  28. Poole S., Firtel R. A., Lamar E., Rowekamp W. Sequence and expression of the discoidin I gene family in Dictyostelium discoideum. J Mol Biol. 1981 Dec 5;153(2):273–289. doi: 10.1016/0022-2836(81)90278-3. [DOI] [PubMed] [Google Scholar]
  29. Robertus J. D., Ready M. P. Ricin B chain and discoidin I share a common primitive protein fold. J Biol Chem. 1984 Nov 25;259(22):13953–13956. [PubMed] [Google Scholar]
  30. Rosen S. D., Kafka J. A., Simpson D. L., Barondes S. H. Developmentally regulated, carbohydrate-binding protein in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1973 Sep;70(9):2554–2557. doi: 10.1073/pnas.70.9.2554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rosenberg M., Court D. Regulatory sequences involved in the promotion and termination of RNA transcription. Annu Rev Genet. 1979;13:319–353. doi: 10.1146/annurev.ge.13.120179.001535. [DOI] [PubMed] [Google Scholar]
  32. Salser W. Globin mRNA sequences: analysis of base pairing and evolutionary implications. Cold Spring Harb Symp Quant Biol. 1978;42(Pt 2):985–1002. doi: 10.1101/sqb.1978.042.01.099. [DOI] [PubMed] [Google Scholar]
  33. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Simpson D. L., Rosen S. D., Barondes S. H. Discoidin, a developmentally regulated carbohydrate-binding protein from Dictyostelium discoideum. Purification and characterization. Biochemistry. 1974 Aug 13;13(17):3487–3493. doi: 10.1021/bi00714a011. [DOI] [PubMed] [Google Scholar]
  35. Siu C. H., Lerner R. A., Ma G., Firtel R. A., Loomis W. F. Developmentally regulated proteins of the plasma membrane of Dictyostelium discoideum. The carbohydrate-binding protein. J Mol Biol. 1976 Jan 15;100(2):157–178. doi: 10.1016/s0022-2836(76)80146-5. [DOI] [PubMed] [Google Scholar]
  36. Teintze M., Thomas R., Furuichi T., Inouye M., Inouye S. Two homologous genes coding for spore-specific proteins are expressed at different times during development of Myxococcus xanthus. J Bacteriol. 1985 Jul;163(1):121–125. doi: 10.1128/jb.163.1.121-125.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wickner W. T., Lodish H. F. Multiple mechanisms of protein insertion into and across membranes. Science. 1985 Oct 25;230(4724):400–407. doi: 10.1126/science.4048938. [DOI] [PubMed] [Google Scholar]

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