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Involvement of a eukaryotic-like ubiquitin-related modifier in the proteasome pathway of the archaeon Sulfolobus acidocaldarius.

Anjum RS, Bray SM, Blackwood JK, Kilkenny ML, Coelho MA, Foster BM, Li S, Howard JA, Pellegrini L, Albers SV, Deery MJ, Robinson NP
Nat Commun 6 8163 (2015)
Cited: 23 times
EuropePMC logo PMID: 26348592

Abstract

In eukaryotes, the covalent attachment of ubiquitin chains directs substrates to the proteasome for degradation. Recently, ubiquitin-like modifications have also been described in the archaeal domain of life. It has subsequently been hypothesized that ubiquitin-like proteasomal degradation might also operate in these microbes, since all archaeal species utilize homologues of the eukaryotic proteasome. Here we perform a structural and biochemical analysis of a ubiquitin-like modification pathway in the archaeon Sulfolobus acidocaldarius. We reveal that this modifier is homologous to the eukaryotic ubiquitin-related modifier Urm1, considered to be a close evolutionary relative of the progenitor of all ubiquitin-like proteins. Furthermore we demonstrate that urmylated substrates are recognized and processed by the archaeal proteasome, by virtue of a direct interaction with the modifier. Thus, the regulation of protein stability by Urm1 and the proteasome in archaea is likely representative of an ancient pathway from which eukaryotic ubiquitin-mediated proteolysis has evolved.

Articles - 4wwm mentioned but not cited (2)

  1. Involvement of a eukaryotic-like ubiquitin-related modifier in the proteasome pathway of the archaeon Sulfolobus acidocaldarius. Anjum RS, Bray SM, Blackwood JK, Kilkenny ML, Coelho MA, Foster BM, Li S, Howard JA, Pellegrini L, Albers SV, Deery MJ, Robinson NP. Nat Commun 6 8163 (2015)
  2. Proteolytic systems of archaea: slicing, dicing, and mincing in the extreme. Maupin-Furlow JA. Emerg Top Life Sci 2 561-580 (2018)


Reviews citing this publication (2)

  1. Evolution of the archaeal and mammalian information processing systems: towards an archaeal model for human disease. Lyu Z, Whitman WB. Cell. Mol. Life Sci. 74 183-212 (2017)
  2. Urm1: A Non-Canonical UBL. Termathe M, Leidel SA. Biomolecules 11 139 (2021)

Articles citing this publication (19)

  1. Mechanistic insight into protein modification and sulfur mobilization activities of noncanonical E1 and associated ubiquitin-like proteins of Archaea. Hepowit NL, de Vera IM, Cao S, Fu X, Wu Y, Uthandi S, Chavarria NE, Englert M, Su D, Sӧll D, Kojetin DJ, Maupin-Furlow JA. FEBS J. 283 3567-3586 (2016)
  2. Urm1: an essential regulator of JNK signaling and oxidative stress in Drosophila melanogaster. Khoshnood B, Dacklin I, Grabbe C. Cell. Mol. Life Sci. 73 1939-1954 (2016)
  3. Ubiquitin-Like Proteasome System Represents a Eukaryotic-Like Pathway for Targeted Proteolysis in Archaea. Fu X, Liu R, Sanchez I, Silva-Sanchez C, Hepowit NL, Cao S, Chen S, Maupin-Furlow J. MBio 7 (2016)
  4. The biology of thermoacidophilic archaea from the order Sulfolobales. Lewis AM, Recalde A, Bräsen C, Counts JA, Nussbaum P, Bost J, Schocke L, Shen L, Willard DJ, Quax TEF, Peeters E, Siebers B, Albers SV, Kelly RM. FEMS Microbiol Rev 45 fuaa063 (2021)
  5. Functional reconstruction of a eukaryotic-like E1/E2/(RING) E3 ubiquitylation cascade from an uncultured archaeon. Hennell James R, Caceres EF, Escasinas A, Alhasan H, Howard JA, Deery MJ, Ettema TJG, Robinson NP. Nat Commun 8 1120 (2017)
  6. Methionine Sulfoxide Reductase A (MsrA) and Its Function in Ubiquitin-Like Protein Modification in Archaea. Fu X, Adams Z, Liu R, Hepowit NL, Wu Y, Bowmann CF, Moskovitz J, Maupin-Furlow JA. MBio 8 (2017)
  7. A conserved hexanucleotide motif is important in UV-inducible promoters in Sulfolobus acidocaldarius. Le TN, Wagner A, Albers SV. Microbiology (Reading, Engl.) 163 778-788 (2017)
  8. Characterization of a small tRNA-binding protein that interacts with the archaeal proteasome complex. Hogrel G, Marino-Puertas L, Laurent S, Ibrahim Z, Covès J, Girard E, Gabel F, Fenel D, Daugeron MC, Clouet-d'Orval B, Basta T, Flament D, Franzetti B. Mol Microbiol 118 16-29 (2022)
  9. Early Response of Sulfolobus acidocaldarius to Nutrient Limitation. Bischof LF, Haurat MF, Hoffmann L, Albersmeier A, Wolf J, Neu A, Pham TK, Albaum SP, Jakobi T, Schouten S, Neumann-Schaal M, Wright PC, Kalinowski J, Siebers B, Albers SV. Front Microbiol 9 3201 (2018)
  10. Machine Learning Uncovers a Data-Driven Transcriptional Regulatory Network for the Crenarchaeal Thermoacidophile Sulfolobus acidocaldarius. Chauhan SM, Poudel S, Rychel K, Lamoureux C, Yoo R, Al Bulushi T, Yuan Y, Palsson BO, Sastry AV. Front Microbiol 12 753521 (2021)
  11. A proteomics approach to identify targets of the ubiquitin-like molecule Urm1 in Drosophila melanogaster. Khoshnood B, Dacklin I, Grabbe C. PLoS ONE 12 e0185611 (2017)
  12. Analysis of the orientation of cholesterol in high-density lipoprotein nanodiscs using solid-state NMR. Lau S, Middleton DA. Phys Chem Chem Phys 24 23651-23660 (2022)
  13. Chase Assay of Protein Stability in Haloferax volcanii. Fu X, Maupin-Furlow JA. Bio Protoc 7 (2017)
  14. Insights into the post-translational modifications of archaeal Sis10b (Alba): lysine-16 is methylated, not acetylated, and this does not regulate transcription or growth. Cao J, Wang Q, Liu T, Peng N, Huang L. Mol. Microbiol. (2018)
  15. Redox requirements for ubiquitin-like urmylation of Ahp1, a 2-Cys peroxiredoxin from yeast. Brachmann C, Kaduhr L, Jüdes A, Ravichandran KE, West JD, Glatt S, Schaffrath R. Redox Biol 30 101438 (2020)
  16. Rhodanese-Like Domain Protein UbaC and Its Role in Ubiquitin-Like Protein Modification and Sulfur Mobilization in Archaea. Hepowit NL, Maupin-Furlow JA. J. Bacteriol. 201 (2019)
  17. The proteasome controls ESCRT-III-mediated cell division in an archaeon. Tarrason Risa G, Hurtig F, Bray S, Hafner AE, Harker-Kirschneck L, Faull P, Davis C, Papatziamou D, Mutavchiev DR, Fan C, Meneguello L, Arashiro Pulschen A, Dey G, Culley S, Kilkenny M, Souza DP, Pellegrini L, de Bruin RAM, Henriques R, Snijders AP, Šarić A, Lindås AC, Robinson NP, Baum B. Science 369 (2020)
  18. Transcriptional and translational dynamics underlying heat shock response in the thermophilic crenarchaeon Sulfolobus acidocaldarius. Baes R, Grünberger F, Pyr Dit Ruys S, Couturier M, De Keulenaer S, Skevin S, Van Nieuwerburgh F, Vertommen D, Grohmann D, Ferreira-Cerca S, Peeters E. mBio 14 e0359322 (2023)
  19. Urm1, not quite a ubiquitin-like modifier? Kaduhr L, Brachmann C, Ravichandran KE, West JD, Glatt S, Schaffrath R. Microb Cell 8 256-261 (2021)


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