Skip to main content
PMC home page
Protein Science : A Publication of the Protein Society logoLink to Protein Science : A Publication of the Protein Society
. 1999 Aug;8(8):1714–1719. doi: 10.1110/ps.8.8.1714

A superfamily of archaeal, bacterial, and eukaryotic proteins homologous to animal transglutaminases.

K S Makarova 1, L Aravind 1, E V Koonin 1
PMCID: PMC2144420  PMID: 10452618

Abstract

Computer analysis using profiles generated by the PSI-BLAST program identified a superfamily of proteins homologous to eukaryotic transglutaminases. The members of the new protein superfamily are found in all archaea, show a sporadic distribution among bacteria, and were detected also in eukaryotes, such as two yeast species and the nematode Caenorhabditis elegans. Sequence conservation in this superfamily primarily involves three motifs that center around conserved cysteine, histidine, and aspartate residues that form the catalytic triad in the structurally characterized transglutaminase, the human blood clotting factor XIIIa'. On the basis of the experimentally demonstrated activity of the Methanobacterium phage pseudomurein endoisopeptidase, it is proposed that many, if not all, microbial homologs of the transglutaminases are proteases and that the eukaryotic transglutaminases have evolved from an ancestral protease.

Full Text

The Full Text of this article is available as a PDF (3.0 MB).

Selected References

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

  1. Aeschlimann D., Kaupp O., Paulsson M. Transglutaminase-catalyzed matrix cross-linking in differentiating cartilage: identification of osteonectin as a major glutaminyl substrate. J Cell Biol. 1995 May;129(3):881–892. doi: 10.1083/jcb.129.3.881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brennan P. J., Nikaido H. The envelope of mycobacteria. Annu Rev Biochem. 1995;64:29–63. doi: 10.1146/annurev.bi.64.070195.000333. [DOI] [PubMed] [Google Scholar]
  4. Cariello L., Ristoratore F., Zanetti L. A new transglutaminase-like from the ascidian Ciona intestinalis. FEBS Lett. 1997 May 19;408(2):171–176. doi: 10.1016/s0014-5793(97)00342-6. [DOI] [PubMed] [Google Scholar]
  5. Cohen C. M., Dotimas E., Korsgren C. Human erythrocyte membrane protein band 4.2 (pallidin). Semin Hematol. 1993 Apr;30(2):119–137. [PubMed] [Google Scholar]
  6. Gardner M. J., Tettelin H., Carucci D. J., Cummings L. M., Aravind L., Koonin E. V., Shallom S., Mason T., Yu K., Fujii C. Chromosome 2 sequence of the human malaria parasite Plasmodium falciparum. Science. 1998 Nov 6;282(5391):1126–1132. doi: 10.1126/science.282.5391.1126. [DOI] [PubMed] [Google Scholar]
  7. Hettasch J. M., Greenberg C. S. Analysis of the catalytic activity of human factor XIIIa by site-directed mutagenesis. J Biol Chem. 1994 Nov 11;269(45):28309–28313. [PubMed] [Google Scholar]
  8. Higgins D. G., McConnell D. J., Sharp P. M. Malarial proteinase? Nature. 1989 Aug 24;340(6235):604–604. doi: 10.1038/340604a0. [DOI] [PubMed] [Google Scholar]
  9. Horiguchi Y., Inoue N., Masuda M., Kashimoto T., Katahira J., Sugimoto N., Matsuda M. Bordetella bronchiseptica dermonecrotizing toxin induces reorganization of actin stress fibers through deamidation of Gln-63 of the GTP-binding protein Rho. Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11623–11626. doi: 10.1073/pnas.94.21.11623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hubbard T. J., Ailey B., Brenner S. E., Murzin A. G., Chothia C. SCOP: a Structural Classification of Proteins database. Nucleic Acids Res. 1999 Jan 1;27(1):254–256. doi: 10.1093/nar/27.1.254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kim S. Y., Chung S. I., Steinert P. M. Highly active soluble processed forms of the transglutaminase 1 enzyme in epidermal keratinocytes. J Biol Chem. 1995 Jul 28;270(30):18026–18035. doi: 10.1074/jbc.270.30.18026. [DOI] [PubMed] [Google Scholar]
  12. Lorand L., Conrad S. M. Transglutaminases. Mol Cell Biochem. 1984;58(1-2):9–35. doi: 10.1007/BF00240602. [DOI] [PubMed] [Google Scholar]
  13. Micanovic R., Procyk R., Lin W., Matsueda G. R. Role of histidine 373 in the catalytic activity of coagulation factor XIII. J Biol Chem. 1994 Mar 25;269(12):9190–9194. [PubMed] [Google Scholar]
  14. Moens S., Vanderleyden J. Glycoproteins in prokaryotes. Arch Microbiol. 1997 Sep;168(3):169–175. doi: 10.1007/s002030050484. [DOI] [PubMed] [Google Scholar]
  15. Muszbek L., Adány R., Mikkola H. Novel aspects of blood coagulation factor XIII. I. Structure, distribution, activation, and function. Crit Rev Clin Lab Sci. 1996;33(5):357–421. doi: 10.3109/10408369609084691. [DOI] [PubMed] [Google Scholar]
  16. Mádi A., Punyiczki M., di Rao M., Piacentini M., Fésüs L. Biochemical characterization and localization of transglutaminase in wild-type and cell-death mutants of the nematode Caenorhabditis elegans. Eur J Biochem. 1998 May 1;253(3):583–590. doi: 10.1046/j.1432-1327.1998.2530583.x. [DOI] [PubMed] [Google Scholar]
  17. Nakaoka H., Perez D. M., Baek K. J., Das T., Husain A., Misono K., Im M. J., Graham R. M. Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science. 1994 Jun 10;264(5165):1593–1596. doi: 10.1126/science.7911253. [DOI] [PubMed] [Google Scholar]
  18. Pedersen L. C., Yee V. C., Bishop P. D., Le Trong I., Teller D. C., Stenkamp R. E. Transglutaminase factor XIII uses proteinase-like catalytic triad to crosslink macromolecules. Protein Sci. 1994 Jul;3(7):1131–1135. doi: 10.1002/pro.5560030720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Peitsch M. C. ProMod and Swiss-Model: Internet-based tools for automated comparative protein modelling. Biochem Soc Trans. 1996 Feb;24(1):274–279. doi: 10.1042/bst0240274. [DOI] [PubMed] [Google Scholar]
  20. Pfister P., Wasserfallen A., Stettler R., Leisinger T. Molecular analysis of Methanobacterium phage psiM2. Mol Microbiol. 1998 Oct;30(2):233–244. doi: 10.1046/j.1365-2958.1998.01073.x. [DOI] [PubMed] [Google Scholar]
  21. Schmidt G., Selzer J., Lerm M., Aktories K. The Rho-deamidating cytotoxic necrotizing factor 1 from Escherichia coli possesses transglutaminase activity. Cysteine 866 and histidine 881 are essential for enzyme activity. J Biol Chem. 1998 May 29;273(22):13669–13674. doi: 10.1074/jbc.273.22.13669. [DOI] [PubMed] [Google Scholar]
  22. Schröder E., Phillips C., Garman E., Harlos K., Crawford C. X-ray crystallographic structure of a papain-leupeptin complex. FEBS Lett. 1993 Jan 2;315(1):38–42. doi: 10.1016/0014-5793(93)81128-m. [DOI] [PubMed] [Google Scholar]
  23. Seledtsov I. A., Vul'f Iu I., Makarova K. S. Mnozhestvennoe vyravnivanie posledovatel'nostei biopolimerov, osnovannoe na poiske statisticheski znachimykh obshchikh uchastkov. Mol Biol (Mosk) 1995 Sep-Oct;29(5):1023–1039. [PubMed] [Google Scholar]
  24. Serafini-Fracassini D., Del Duca S., Beninati S. Plant transglutaminases. Phytochemistry. 1995 Sep;40(2):355–365. doi: 10.1016/0031-9422(95)00243-z. [DOI] [PubMed] [Google Scholar]
  25. Sleytr U. B., Sára M. Bacterial and archaeal S-layer proteins: structure-function relationships and their biotechnological applications. Trends Biotechnol. 1997 Jan;15(1):20–26. doi: 10.1016/S0167-7799(96)10063-9. [DOI] [PubMed] [Google Scholar]
  26. Steinert P. M., Marekov L. N. The proteins elafin, filaggrin, keratin intermediate filaments, loricrin, and small proline-rich proteins 1 and 2 are isodipeptide cross-linked components of the human epidermal cornified cell envelope. J Biol Chem. 1995 Jul 28;270(30):17702–17711. doi: 10.1074/jbc.270.30.17702. [DOI] [PubMed] [Google Scholar]
  27. Tokunaga F., Muta T., Iwanaga S., Ichinose A., Davie E. W., Kuma K., Miyata T. Limulus hemocyte transglutaminase. cDNA cloning, amino acid sequence, and tissue localization. J Biol Chem. 1993 Jan 5;268(1):262–268. [PubMed] [Google Scholar]
  28. Washizu K., Ando K., Koikeda S., Hirose S., Matsuura A., Takagi H., Motoki M., Takeuchi K. Molecular cloning of the gene for microbial transglutaminase from Streptoverticillium and its expression in Streptomyces lividans. Biosci Biotechnol Biochem. 1994 Jan;58(1):82–87. doi: 10.1271/bbb.58.82. [DOI] [PubMed] [Google Scholar]
  29. Weraarchakul-Boonmark N., Jeong J. M., Murthy S. N., Engel J. D., Lorand L. Cloning and expression of chicken erythrocyte transglutaminase. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9804–9808. doi: 10.1073/pnas.89.20.9804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wootton J. C., Federhen S. Analysis of compositionally biased regions in sequence databases. Methods Enzymol. 1996;266:554–571. doi: 10.1016/s0076-6879(96)66035-2. [DOI] [PubMed] [Google Scholar]
  31. Wootton J. C. Non-globular domains in protein sequences: automated segmentation using complexity measures. Comput Chem. 1994 Sep;18(3):269–285. doi: 10.1016/0097-8485(94)85023-2. [DOI] [PubMed] [Google Scholar]
  32. Yee V. C., Pedersen L. C., Le Trong I., Bishop P. D., Stenkamp R. E., Teller D. C. Three-dimensional structure of a transglutaminase: human blood coagulation factor XIII. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7296–7300. doi: 10.1073/pnas.91.15.7296. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Protein Science : A Publication of the Protein Society are provided here courtesy of The Protein Society

RESOURCES