1887

Microbiology Society logo

Volume 153, Issue 9

Transcriptional linkage of proteasomal genes with non-proteasomal gene neighbours including RNase P, MOSC domain and SAM-methyltransferase homologues Free

Abstract

Comparative genomics reveals a common theme of 20S proteasome and proteasome-activating nucleotidase genes dispersed throughout archaeal genomes yet arranged in conserved linkages with gene homologues of translation and/or transcription machineries. To provide biological evidence for these linkages as well as insight into proteasome operon organization, transcripts of the five proteasomal genes of the halophilic archaeon were analysed by Northern (RNA) blotting, RT-PCR and primer extension. These included , and , encoding the 20S proteasomal subunits 1, and 2, as well as and , encoding the PanA and PanB proteasome-activating nucleotidase proteins, respectively. All five of these genes are dispersed throughout the genome. For each proteasomal gene, a distinct transcript was detected by Northern blotting that was similar in size to the respective coding region. For both and , an additional transcript was detected that was 1.34 and 0.85 kb greater, respectively, than the coding region. Further analysis by Northern blotting and RT-PCR revealed that was co-transcribed with genes encoding a Pop5 homologue of the RNase P endoRNase as well as an -adenosylmethionine (SAM)-dependent methyltransferase. Likewise, was co-transcribed with a downstream gene encoding a molybdenum cofactor sulfurase C-terminal (MOSC) domain protein. Additional proteasomal and neighbouring gene-specific transcriptional linkages were detected by RT-PCR. These results provide the first evidence that proteasome and tRNA modification genes are co-transcribed, reveal that a number of additional enzymes including those predicted to facilitate metal–sulfur cluster assembly are co-regulated with proteasomes at the transcriptional level, and provide further insight into proteasome gene transcription in archaea.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): AAA family, ATPases associated with various cellular activities family , MOSC domain, molybdenum cofactor sulfurase C-terminal domain , PAN, proteasome-activating nucleotidase and SAM, S-adenosylmethionine
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/008177-0
2007-09-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/9/3009.html?itemId=/content/journal/micro/10.1099/mic.0.2007/008177-0&mimeType=html&fmt=ahah

References

  1. Altman S., Wesolowski D., Guerrier-Takada C., Li Y. 2005; RNase P cleaves transient structures in some riboswitches. Proc Natl Acad Sci U S A 102:11284–11289
     [Google Scholar]
  2. Anantharaman V., Aravind L. 2002; MOSC domains: ancient, predicted sulfur-carrier domains, present in diverse metal-sulfur cluster biosynthesis proteins including molybdenum cofactor sulfurases. FEMS Microbiol Lett 207:55–61
     [Google Scholar]
  3. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Smith J. A., Seidman J. G., Struhl K. 1987; Preparation and analysis of RNA. In Current Protocols in Molecular Biology pp. 4.0.1–4.10.11 New York: Green Publishing Associates and Wiley-Interscience;
     [Google Scholar]
  4. Baliga N. S., Goo Y. A., Ng W. V., Hood L., Daniels C. J., DasSarma S. 2000; Is gene expression in Halobacterium NRC-1 regulated by multiple TBP and TFB transcription factors?. Mol Microbiol 36:1184–1185
     [Google Scholar]
  5. Bell S. D., Jackson S. P. 2001; Mechanism and regulation of transcription in archaea. Curr Opin Microbiol 4:208–213
     [Google Scholar]
  6. Benaroudj N., Goldberg A. L. 2000; PAN, the proteasome-activating nucleotidase from archaebacteria, is a protein-unfolding molecular chaperone. Nat Cell Biol 2:833–839
     [Google Scholar]
  7. Danner S., Soppa J. 1996; Characterization of the distal promoter element of halobacteria in vivo using saturation mutagenesis and selection. Mol Microbiol 19:1265–1276
     [Google Scholar]
  8. Dvorak Z., Pascussi J. M., Modriansky M. 2003; Approaches to messenger RNA detection – comparison of methods. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 147:131–135
     [Google Scholar]
  9. Ellis J. C., Brown J. W. 2003; Genes within genes within bacteria. Trends Biochem Sci 28:521–523
     [Google Scholar]
  10. Facciotti M. T., Reiss D. J., Pan M., Kaur A., Vuthoori M., Bonneau R., Shannon P., Srivastava A., Donohoe S. M. other authors 2007; General transcription factor specified global gene regulation in archaea. Proc Natl Acad Sci U S A 104:4630–4635
     [Google Scholar]
  11. Ignoul S., Eggermont J. 2005; CBS domains: structure, function, and pathology in human proteins. Am J Physiol Cell Physiol 289:C1369–C1378
     [Google Scholar]
  12. Ingrosso D., Fowler A. V., Bleibaum J., Clarke S. 1989; Sequence of the d-aspartyl/l-isoaspartyl protein methyltransferase from human erythrocytes. Common sequence motifs for protein, DNA, RNA, and small molecule S-adenosylmethionine-dependent methyltransferases. J Biol Chem 264:20131–20139
     [Google Scholar]
  13. Kaczowka S. J., Maupin-Furlow J. A. 2003; Subunit topology of two 20S proteasomes from Haloferax volcanii. J Bacteriol 185:165–174
     [Google Scholar]
  14. Koonin E. V., Wolf Y. I., Aravind L. 2001; Prediction of the archaeal exosome and its connections with the proteasome and the translation and transcription machineries by a comparative-genomic approach. Genome Res 11:240–252
     [Google Scholar]
  15. Li Y., Altman S. 2003; A specific endoribonuclease, RNase P, affects gene expression of polycistronic operon mRNAs. Proc Natl Acad Sci U S A 100:13213–13218
     [Google Scholar]
  16. Maupin-Furlow J. A., Ferry J. G. 1995; A proteasome from the methanogenic archaeon Methanosarcina thermophila. J Biol Chem 270:28617–28622
     [Google Scholar]
  17. Maupin-Furlow J. A., Wilson H. L., Kaczowka S. J., Ou M. S. 2000; Proteasomes in the archaea: from structure to function. Front Biosci 5:d837–d865
     [Google Scholar]
  18. Maupin-Furlow J. A., Humbard M. A., Kirkland P. A., Li W., Reuter C. J., Wright A. J., Zhou G. 2006; Proteasomes from structure to function: perspectives from archaea. Curr Top Dev Biol 75:125–169
     [Google Scholar]
  19. Mullakhanbhai M. F., Larsen H. 1975; Halobacterium volcanii spec. nov., a Dead Sea Halobacterium with a moderate salt requirement. Arch Microbiol 104:207–214
     [Google Scholar]
  20. Ng W.-L., Yang C.-F., Halladay J. T., Arora P., DasSarma S. 1995; Isolation of genomic and plasmid DNAs from Halobacterium halobium. In Archaea: a Laboratory Manual pp 179–184 New York: Cold Spring Harbor Laboratory Press;
     [Google Scholar]
  21. Nieuwlandt D. T., Palmer J. R., Armbruster D. W., Kuo Y. P., Oda W., Daniels C. J. 1995; A rapid procedure for the isolation of RNA from Haloferax volcanii. In Archaea: a Laboratory Manual pp 161–162 Plainview, NY: Cold Spring Harbor Laboratory Press;
     [Google Scholar]
  22. Piersen C. E., Prince M. A., Augustine M. L., Dodson M. L., Lloyd R. S. 1995; Purification and cloning of Micrococcus luteus ultraviolet endonuclease, an N-glycosylase/abasic lyase that proceeds via an imino enzyme-DNA intermediate. J Biol Chem 270:23475–23484
     [Google Scholar]
  23. Reuter C. J., Kaczowka S. J., Maupin-Furlow J. A. 2004; Differential regulation of the PanA and PanB proteasome-activating nucleotidase and 20S proteasomal proteins of the haloarchaeon Haloferax volcanii. J Bacteriol 186:7763–7772
     [Google Scholar]
  24. Smith D. M., Benaroudj N., Goldberg A. 2006; Proteasomes and their associated ATPases: a destructive combination. J Struct Biol 156:72–83
     [Google Scholar]
  25. Srinivasan G., Krebs M.P., RajBhandary U.L. 2006; Translation initiation with GUC codon in the archaeon Halobacterium salinarum: implications for translation of leaderless mRNA and strict correlation between translation initiation and presence of mRNA. Mol Microbiol 59:1013–1024
     [Google Scholar]
  26. Sweder K., Madura K. 2002; Regulation of repair by the 26S proteasome. J Biomed Biotechnol 2:94–105
     [Google Scholar]
  27. Tsai H. Y., Pulukkunat D. K., Woznick W. K., Gopalan V. 2006; Functional reconstitution and characterization of Pyrococcus furiosus RNase P. Proc Natl Acad Sci U S A 103:16147–16152
     [Google Scholar]
  28. Wang Q. E., Wani M. A., Chen J., Zhu Q., Wani G., El Mahdy M. A., Wani A. A. 2005; Cellular ubiquitination and proteasomal functions positively modulate mammalian nucleotide excision repair. Mol Carcinog 42:53–64
     [Google Scholar]
  29. Wilson H. L., Aldrich H. C., Maupin-Furlow J. A. 1999; Halophilic 20S proteasomes of the archaeon Haloferax volcanii: purification, characterization and gene sequence analysis. J Bacteriol 181:5814–5824
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/008177-0
Loading
Transcriptional linkage of Haloferax volcanii proteasomal genes with non-proteasomal gene neighbours including RNase P, MOSC domain and SAM-methyltransferase homologues
Microbiology 153, 3009 (2007); https://doi.org/10.1099/mic.0.2007/008177-0
/content/journal/micro/10.1099/mic.0.2007/008177-0
/content/journal/micro/10.1099/mic.0.2007/008177-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error