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Archaeal Proteasomes and Sampylation

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Regulated Proteolysis in Microorganisms

Part of the book series: Subcellular Biochemistry ((SCBI,volume 66))

Abstract

Archaea contain, both a functional proteasome and an ubiquitin-like protein conjugation system (termed sampylation) that is related to the ubiquitin proteasome system (UPS) of eukaryotes. Archaeal proteasomes have served as excellent models for understanding how proteins are degraded by the central energy-dependent proteolytic machine of eukaryotes, the 26S proteasome. While sampylation has only recently been discovered, it is thought to be linked to proteasome-mediated degradation in archaea. Unlike eukaryotes, sampylation only requires an E1 enzyme homolog of the E1-E2-E3 ubiquitylation cascade to mediate protein conjugation. Furthermore, recent evidence suggests that archaeal and eurkaryotic E1 enzyme homologs can serve dual roles in mediating protein conjugation and activating sulfur for incorporation into biomolecules. The focus of this book chapter is the energy-dependent proteasome and sampylation systems of Archaea.

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References

  1. Gottesman S (1999) Regulation by proteolysis: developmental switches. Curr Opin Microbiol 2(2):142–147

    PubMed  CAS  Google Scholar 

  2. Wolf DH, Hilt W (2004) The proteasome: a proteolytic nanomachine of cell regulation and waste disposal. Biochim Biophys Acta 1695(1–3):19–31

    PubMed  CAS  Google Scholar 

  3. Lupas A, Flanagan JM, Tamura T, Baumeister W (1997) Self-compartmentalizing proteases. Trends Biochem Sci 22(10):399–404

    PubMed  CAS  Google Scholar 

  4. Cha SS, An YJ, Lee CR, Lee HS et al (2010) Crystal structure of Lon protease: molecular architecture of gated entry to a sequestered degradation chamber. EMBO J 29(20):3520–3530

    PubMed  CAS  Google Scholar 

  5. Effantin G, Maurizi MR, Steven AC (2010) Binding of the ClpA unfoldase opens the axial gate of ClpP peptidase. J Biol Chem 285(19):14834–14840

    PubMed  CAS  Google Scholar 

  6. Lee ME, Baker TA, Sauer RT (2010) Control of substrate gating and translocation into ClpP by channel residues and ClpX binding. J Mol Biol 399(5):707–718

    PubMed  CAS  Google Scholar 

  7. Smith DM, Benaroudj N, Goldberg A (2006) Proteasomes and their associated ATPases: a destructive combination. J Struct Biol 156(1):72–83

    PubMed  CAS  Google Scholar 

  8. Ammelburg M, Frickey T, Lupas AN (2006) Classification of AAA  +  proteins. J Struct Biol 156(1):2–11

    PubMed  CAS  Google Scholar 

  9. Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9(1):27–43

    PubMed  CAS  Google Scholar 

  10. Sauer RT, Baker TA (2011) AAA+ proteases: ATP-fueled machines of protein destruction. Annu Rev Biochem 80:587–612

    PubMed  CAS  Google Scholar 

  11. Gur E, Ottofuelling R, Dougan DA (2013) Machines of destruction – AAA  +  proteases and the adaptors that control them. In: Dougan DA (ed) Regulated proteolysis in microorganisms. Springer, Subcell Biochem 66:3–33

    Google Scholar 

  12. Samanovic M, Li H, Darwin KH (2013) The Pup-Proteasome system of Mycobacterium tuberculosis. In: Dougan DA (ed) Regulated proteolysis in microorganisms. Springer, Subcell Biochem 66:267–295

    Google Scholar 

  13. Maupin-Furlow JA, Humbard MA, Kirkland PA, Li W et al (2006) Proteasomes from structure to function: perspectives from Archaea. Curr Top Dev Biol 75:125–169

    PubMed  CAS  Google Scholar 

  14. Bar-Nun S, Glickman MH (2012) Proteasomal AAA-ATPases: structure and function. Biochim Biophys Acta 1823(1):67–82

    PubMed  CAS  Google Scholar 

  15. Besche H, Tamura N, Tamura T, Zwickl P (2004) Mutational analysis of conserved AAA+ residues in the archaeal Lon protease from Thermoplasma acidophilum. FEBS Lett 574(1–3):161–166

    PubMed  CAS  Google Scholar 

  16. Fukui T, Eguchi T, Atomi H, Imanaka T (2002) A membrane-bound archaeal Lon protease displays ATP-independent proteolytic activity towards unfolded proteins and ATP-dependent activity for folded proteins. J Bacteriol 184(13):3689–3698

    PubMed  CAS  Google Scholar 

  17. De Mot R, Nagy I, Walz J, Baumeister W (1999) Proteasomes and other self-compartmentalizing proteases in prokaryotes. Trends Microbiol 7(2):88–92

    PubMed  Google Scholar 

  18. Lupas A, Zuhl F, Tamura T, Wolf S et al (1997) Eubacterial proteasomes. Mol Biol Rep 24(1–2):125–131

    PubMed  CAS  Google Scholar 

  19. Lupas A, Zwickl P, Baumeister W (1994) Proteasome sequences in eubacteria. Trends Biochem Sci 19(12):533–534

    PubMed  CAS  Google Scholar 

  20. Tamura T, Nagy I, Lupas A, Lottspeich F et al (1995) The first characterization of a eubacterial proteasome: the 20S complex of Rhodococcus. Curr Biol 5(7):766–774

    PubMed  CAS  Google Scholar 

  21. Bochtler M, Ditzel L, Groll M, Hartmann C et al (1999) The proteasome. Annu Rev Biophys Biomol Struct 28:295–317

    PubMed  CAS  Google Scholar 

  22. Voges D, Zwickl P, Baumeister W (1999) The 26S proteasome: a molecular machine designed for controlled proteolysis. Annu Rev Biochem 68:1015–1068

    PubMed  CAS  Google Scholar 

  23. Larsen CN, Finley D (1997) Protein translocation channels in the proteasome and other proteases. Cell 91(4):431–434

    PubMed  CAS  Google Scholar 

  24. Brannigan JA, Dodson G, Duggleby HJ, Moody PC et al (1995) A protein catalytic framework with an N-terminal nucleophile is capable of self-activation. Nature 378(6555):416–419

    PubMed  CAS  Google Scholar 

  25. Ekici OD, Paetzel M, Dalbey RE (2008) Unconventional serine proteases: variations on the catalytic Ser/His/Asp triad configuration. Protein Sci 17(12):2023–2037

    PubMed  CAS  Google Scholar 

  26. Oinonen C, Rouvinen J (2000) Structural comparison of Ntn-hydrolases. Protein Sci 9(12):2329–2337

    PubMed  CAS  Google Scholar 

  27. Seemuller E, Lupas A, Stock D, Lowe J et al (1995) Proteasome from Thermoplasma acidophilum: a threonine protease. Science 268(5210):579–582

    PubMed  CAS  Google Scholar 

  28. Dodson G, Wlodawer A (1998) Catalytic triads and their relatives. Trends Biochem Sci 23(9):347–352

    PubMed  CAS  Google Scholar 

  29. Kisselev AF, Songyang Z, Goldberg AL (2000) Why does threonine, and not serine, function as the active site nucleophile in proteasomes? J Biol Chem 275(20):14831–14837

    PubMed  CAS  Google Scholar 

  30. Maupin-Furlow JA, Aldrich HC, Ferry JG (1998) Biochemical characterization of the 20S proteasome from the methanoarchaeon Methanosarcina thermophila. J Bacteriol 180(6):1480–1487

    PubMed  CAS  Google Scholar 

  31. Zwickl P, Kleinz J, Baumeister W (1994) Critical elements in proteasome assembly. Nat Struct Biol 1(11):765–770

    PubMed  CAS  Google Scholar 

  32. Groll M, Heinemeyer W, Jager S, Ullrich T et al (1999) The catalytic sites of 20S proteasomes and their role in subunit maturation: a mutational and crystallographic study. Proc Natl Acad Sci U S A 96(20):10976–10983

    PubMed  CAS  Google Scholar 

  33. Jager S, Groll M, Huber R, Wolf DH et al (1999) Proteasome beta-type subunits: unequal roles of propeptides in core particle maturation and a hierarchy of active site function. J Mol Biol 291(4):997–1013

    PubMed  CAS  Google Scholar 

  34. Bauer MW, Bauer SH, Kelly RM (1997) Purification and characterization of a proteasome from the hyperthermophilic archaeon Pyrococcus furiosus. Appl Environ Microbiol 63(3):1160–1164

    PubMed  CAS  Google Scholar 

  35. Dahlmann B, Kopp F, Kuehn L, Niedel B et al (1989) The multicatalytic proteinase (prosome) is ubiquitous from eukaryotes to archaebacteria. FEBS Lett 251(1–2):125–131

    PubMed  CAS  Google Scholar 

  36. Maupin-Furlow JA, Ferry JG (1995) A proteasome from the methanogenic archaeon Methanosarcina thermophila. J Biol Chem 270(48):28617–28622

    PubMed  CAS  Google Scholar 

  37. Wilson HL, Aldrich HC, Maupin-Furlow J (1999) Halophilic 20S proteasomes of the archaeon Haloferax volcanii: purification, characterization, and gene sequence analysis. J Bacteriol 181(18):5814–5824

    PubMed  CAS  Google Scholar 

  38. Arendt CS, Hochstrasser M (1999) Eukaryotic 20S proteasome catalytic subunit propeptides prevent active site inactivation by N-terminal acetylation and promote particle assembly. EMBO J 18(13):3575–3585

    PubMed  CAS  Google Scholar 

  39. Kwon YD, Nagy I, Adams PD, Baumeister W et al (2004) Crystal structures of the Rhodococcus proteasome with and without its pro-peptides: implications for the role of the pro-peptide in proteasome assembly. J Mol Biol 335(1):233–245

    PubMed  CAS  Google Scholar 

  40. Zuhl F, Seemuller E, Golbik R, Baumeister W (1997) Dissecting the assembly pathway of the 20S proteasome. FEBS Lett 418(1–2):189–194

    PubMed  CAS  Google Scholar 

  41. Li D, Li H, Wang T, Pan H et al (2010) Structural basis for the assembly and gate closure mechanisms of the Mycobacterium tuberculosis 20S proteasome. EMBO J 29(12):2037–2047

    PubMed  CAS  Google Scholar 

  42. Lin G, Hu G, Tsu C, Kunes YZ et al (2006) Mycobacterium tuberculosis prcBA genes encode a gated proteasome with broad oligopeptide specificity. Mol Microbiol 59(5):1405–1416

    PubMed  CAS  Google Scholar 

  43. Wilson HL, Ou MS, Aldrich HC, Maupin-Furlow J (2000) Biochemical and physical properties of the Methanococcus jannaschii 20S proteasome and PAN, a homolog of the ATPase (Rpt) subunits of the eucaryal 26S proteasome. J Bacteriol 182(6):1680–1692

    PubMed  CAS  Google Scholar 

  44. Kaczowka SJ, Maupin-Furlow JA (2003) Subunit topology of two 20S proteasomes from Haloferax volcanii. J Bacteriol 185(1):165–174

    PubMed  CAS  Google Scholar 

  45. Ginzburg M, Sachs L, Ginzburg BZ (1970) Ion metabolism in a Halobacterium. I. Influence of age of culture on intracellular concentrations. J Gen Physiol 55(2):187–207

    PubMed  CAS  Google Scholar 

  46. Mevarech M, Frolow F, Gloss LM (2000) Halophilic enzymes: proteins with a grain of salt. Biophys Chem 86(2–3):155–164

    PubMed  CAS  Google Scholar 

  47. Falb M, Aivaliotis M, Garcia-Rizo C, Bisle B et al (2006) Archaeal N-terminal protein maturation commonly involves N-terminal acetylation: a large-scale proteomics survey. J Mol Biol 362(5):915–924

    PubMed  CAS  Google Scholar 

  48. Kirkland PA, Humbard MA, Daniels CJ, Maupin-Furlow JA (2008) Shotgun proteomics of the haloarchaeon Haloferax volcanii. J Proteome Res 7(11):5033–5039

    PubMed  CAS  Google Scholar 

  49. Soppa J (2010) Protein acetylation in archaea, bacteria, and eukaryotes. Archaea 2010 (Article ID 820681): 9. doi:10.1155/2010/820681

    Google Scholar 

  50. Kisselev AF, Akopian TN, Goldberg AL (1998) Range of sizes of peptide products generated during degradation of different proteins by archaeal proteasomes. J Biol Chem 273(4):1982–1989

    PubMed  CAS  Google Scholar 

  51. Kisselev AF, Akopian TN, Woo KM, Goldberg AL (1999) The sizes of peptides generated from protein by mammalian 26 and 20S proteasomes. Implications for understanding the degradative mechanism and antigen presentation. J Biol Chem 274(6):3363–3371

    PubMed  CAS  Google Scholar 

  52. Gallastegui N, Groll M (2010) The 26S proteasome: assembly and function of a destructive machine. Trends Biochem Sci 35(11):634–642

    PubMed  CAS  Google Scholar 

  53. Vigneron N, Van den Eynde BJ (2012) Proteasome subtypes and the processing of tumor antigens: increasing antigenic diversity. Curr Opin Immunol 24(1):84–91

    PubMed  CAS  Google Scholar 

  54. Zwickl P, Grziwa A, Puhler G, Dahlmann B et al (1992) Primary structure of the Thermoplasma proteasome and its implications for the structure, function, and evolution of the multicatalytic proteinase. Biochemistry 31(4):964–972

    PubMed  CAS  Google Scholar 

  55. Zwickl P, Lottspeich F, Baumeister W (1992) Expression of functional Thermoplasma acidophilum proteasomes in Escherichia coli. FEBS Lett 312(2–3):157–160

    PubMed  CAS  Google Scholar 

  56. Kocabiyik S, Ozdemir I, Zwickl P, Ozdogan S (2010) Molecular cloning and co-expression of Thermoplasma volcanium proteasome subunit genes. Protein Expr Purif 73(2):223–230

    PubMed  CAS  Google Scholar 

  57. Medalia N, Sharon M, Martinez-Arias R, Mihalache O et al (2006) Functional and structural characterization of the Methanosarcina mazei proteasome and PAN complexes. J Struct Biol 156(1):84–92

    PubMed  CAS  Google Scholar 

  58. Groll M, Brandstetter H, Bartunik H, Bourenkow G et al (2003) Investigations on the maturation and regulation of archaebacterial proteasomes. J Mol Biol 327(1):75–83

    PubMed  CAS  Google Scholar 

  59. Robb FT, Maeder DL, Brown JR, DiRuggiero J et al (2001) Genomic sequence of hyperthermophile, Pyrococcus furiosus: implications for physiology and enzymology. Methods Enzymol 330:134–157

    PubMed  CAS  Google Scholar 

  60. Madding LS, Michel JK, Shockley KR, Conners SB et al (2007) Role of the beta1 subunit in the function and stability of the 20S proteasome in the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 189(2):583–590

    PubMed  CAS  Google Scholar 

  61. Zhou G, Kowalczyk D, Humbard MA, Rohatgi S et al (2008) Proteasomal components required for cell growth and stress responses in the haloarchaeon Haloferax volcanii. J Bacteriol 190(24):8096–8105

    PubMed  CAS  Google Scholar 

  62. Karadzic I, Maupin-Furlow J, Humbard M, Prunetti L, Singh P, Goodlett DR (2012) Chemical cross-linking, mass spectrometry, and in silico modeling of proteasomal 20S core particles of the haloarchaeon Haloferax volcanii. Proteomics 12(11):1806–1814

    Google Scholar 

  63. Reuter CJ, Kaczowka SJ, Maupin-Furlow JA (2004) Differential regulation of the PanA and PanB proteasome-activating nucleotidase and 20S proteasomal proteins of the haloarchaeon Haloferax volcanii. J Bacteriol 186(22):7763–7772

    PubMed  CAS  Google Scholar 

  64. Humbard MA, Reuter CJ, Zuobi-Hasona K, Zhou G et al (2010) Phosphorylation and methylation of proteasomal proteins of the haloarcheon Haloferax volcanii. Archaea 2010:481725

    PubMed  Google Scholar 

  65. Humbard MA, Stevens SM Jr, Maupin-Furlow JA (2006) Posttranslational modification of the 20S proteasomal proteins of the archaeon Haloferax volcanii. J Bacteriol 188(21):7521–7530

    PubMed  CAS  Google Scholar 

  66. Humbard MA, Zhou G, Maupin-Furlow JA (2009) The N-terminal penultimate residue of 20S proteasome alpha1 influences its N(alpha) acetylation and protein levels as well as growth rate and stress responses of Haloferax volcanii. J Bacteriol 191(12):3794–3803

    PubMed  CAS  Google Scholar 

  67. Stadtmueller BM, Hill CP (2011) Proteasome activators. Mol Cell 41(1):8–19

    PubMed  CAS  Google Scholar 

  68. Finley D, Tanaka K, Mann C, Feldmann H et al (1998) Unified nomenclature for subunits of the Saccharomyces cerevisiae proteasome regulatory particle. Trends Biochem Sci 23(7):244–245

    PubMed  CAS  Google Scholar 

  69. Glickman MH, Rubin DM, Coux O, Wefes I et al (1998) A subcomplex of the proteasome regulatory particle required for ubiquitin-conjugate degradation and related to the COP9-signalosome and eIF3. Cell 94(5):615–623

    PubMed  CAS  Google Scholar 

  70. Bult CJ, White O, Olsen GJ, Zhou L et al (1996) Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273(5278):1058–1073

    PubMed  CAS  Google Scholar 

  71. Zwickl P, Ng D, Woo KM, Klenk HP et al (1999) An archaebacterial ATPase, homologous to ATPases in the eukaryotic 26S proteasome, activates protein breakdown by 20S proteasomes. J Biol Chem 274(37):26008–26014

    PubMed  CAS  Google Scholar 

  72. Stolz A, Hilt W, Buchberger A, Wolf DH (2011) Cdc48: a power machine in protein degradation. Trends Biochem Sci 36(10):515–523

    PubMed  CAS  Google Scholar 

  73. Buchberger A (2013) Roles of Cdc48 in regulated protein degradation in yeast. In: Dougan DA (ed) Regulated proteolysis in microorganisms. Springer, Subcell Biochem 66:3–195–222

    Google Scholar 

  74. Gerega A, Rockel B, Peters J, Tamura T et al (2005) VAT, the thermoplasma homolog of mammalian p97/VCP, is an N domain-regulated protein unfoldase. J Biol Chem 280(52):42856–42862

    PubMed  CAS  Google Scholar 

  75. Barthelme D, Sauer RT (2012) Identification of the Cdc48•20S proteasome as an ancient AAA+ proteolytic machine. Science 337(6096):843–846

    Google Scholar 

  76. Lowe J, Stock D, Jap B, Zwickl P et al (1995) Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution. Science 268(5210):533–539

    PubMed  CAS  Google Scholar 

  77. Groll M, Ditzel L, Lowe J, Stock D et al (1997) Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 386(6624):463–471

    PubMed  CAS  Google Scholar 

  78. Unno M, Mizushima T, Morimoto Y, Tomisugi Y et al (2002) Structure determination of the constitutive 20S proteasome from bovine liver at 2.75 A resolution. J Biochem 131(2):171–173

    PubMed  CAS  Google Scholar 

  79. Groll M, Bajorek M, Kohler A, Moroder L et al (2000) A gated channel into the proteasome core particle. Nat Struct Biol 7(11):1062–1067

    PubMed  CAS  Google Scholar 

  80. Kohler A, Cascio P, Leggett DS, Woo KM et al (2001) The axial channel of the proteasome core particle is gated by the Rpt2 ATPase and controls both substrate entry and product release. Mol Cell 7(6):1143–1152

    PubMed  CAS  Google Scholar 

  81. Whitby FG, Masters EI, Kramer L, Knowlton JR et al (2000) Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 408(6808):115–120

    PubMed  CAS  Google Scholar 

  82. Benaroudj N, Zwickl P, Seemuller E, Baumeister W et al (2003) ATP hydrolysis by the proteasome regulatory complex PAN serves multiple functions in protein degradation. Mol Cell 11(1):69–78

    PubMed  CAS  Google Scholar 

  83. Smith DM, Kafri G, Cheng Y, Ng D et al (2005) ATP binding to PAN or the 26S ATPases causes association with the 20S proteasome, gate opening, and translocation of unfolded proteins. Mol Cell 20(5):687–698

    PubMed  CAS  Google Scholar 

  84. Zhang F, Hu M, Tian G, Zhang P et al (2009) Structural insights into the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol Cell 34(4):473–484

    PubMed  Google Scholar 

  85. Rabl J, Smith DM, Yu Y, Chang SC et al (2008) Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol Cell 30(3):360–368

    PubMed  CAS  Google Scholar 

  86. Yu Y, Smith DM, Kim HM, Rodriguez V et al (2010) Interactions of PAN’s C-termini with archaeal 20S proteasome and implications for the eukaryotic proteasome-ATPase interactions. EMBO J 29(3):692–702

    PubMed  CAS  Google Scholar 

  87. Religa TL, Sprangers R, Kay LE (2010) Dynamic regulation of archaeal proteasome gate opening as studied by TROSY NMR. Science 328(5974):98–102

    PubMed  CAS  Google Scholar 

  88. Bochtler M, Hartmann C, Song HK, Bourenkov GP et al (2000) The structures of HsIU and the ATP-dependent protease HsIU-HsIV. Nature 403(6771):800–805

    PubMed  CAS  Google Scholar 

  89. Rohrwild M, Pfeifer G, Santarius U, Muller SA et al (1997) The ATP-dependent HslVU protease from Escherichia coli is a four-ring structure resembling the proteasome. Nat Struct Biol 4(2):133–139

    PubMed  CAS  Google Scholar 

  90. Sousa MC, Trame CB, Tsuruta H, Wilbanks SM et al (2000) Crystal and solution structures of an HslUV protease-chaperone complex. Cell 103(4):633–643

    PubMed  CAS  Google Scholar 

  91. Smith DM, Chang SC, Park S, Finley D et al (2007) Docking of the proteasomal ATPases’ carboxyl termini in the 20S proteasome’s alpha ring opens the gate for substrate entry. Mol Cell 27(5):731–744

    PubMed  CAS  Google Scholar 

  92. Ramachandran R, Hartmann C, Song HK, Huber R et al (2002) Functional interactions of HslV (ClpQ) with the ATPase HslU (ClpY). Proc Natl Acad Sci U S A 99(11):7396–7401

    PubMed  CAS  Google Scholar 

  93. Ma CP, Willy PJ, Slaughter CA, DeMartino GN (1993) PA28, an activator of the 20S proteasome, is inactivated by proteolytic modification at its carboxyl terminus. J Biol Chem 268(30):22514–22519

    PubMed  CAS  Google Scholar 

  94. Forster A, Masters EI, Whitby FG, Robinson H et al (2005) The 1.9 A structure of a proteasome-11S activator complex and implications for proteasome-PAN/PA700 interactions. Mol Cell 18(5):589–599

    PubMed  Google Scholar 

  95. Forster A, Whitby FG, Hill CP (2003) The pore of activated 20S proteasomes has an ordered 7-fold symmetric conformation. EMBO J 22(17):4356–4364

    PubMed  Google Scholar 

  96. Zhang F, Wu Z, Zhang P, Tian G et al (2009) Mechanism of substrate unfolding and translocation by the regulatory particle of the proteasome from Methanocaldococcus jannaschii. Mol Cell 34(4):485–496

    PubMed  CAS  Google Scholar 

  97. Djuranovic S, Hartmann MD, Habeck M, Ursinus A et al (2009) Structure and activity of the N-terminal substrate recognition domains in proteasomal ATPases. Mol Cell 34(5):580–590

    PubMed  CAS  Google Scholar 

  98. Medalia N, Beer A, Zwickl P, Mihalache O et al (2009) Architecture and molecular mechanism of PAN, the archaeal proteasome regulatory ATPase. J Biol Chem 284(34):22952–22960

    PubMed  CAS  Google Scholar 

  99. Navon A, Goldberg AL (2001) Proteins are unfolded on the surface of the ATPase ring before transport into the proteasome. Mol Cell 8(6):1339–1349

    PubMed  CAS  Google Scholar 

  100. Matouschek A (2003) Protein unfolding – an important process in vivo? Curr Opin Struct Biol 13(1):98–109

    PubMed  CAS  Google Scholar 

  101. Hinnerwisch J, Fenton WA, Furtak KJ, Farr GW et al (2005) Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 121(7):1029–1041

    PubMed  CAS  Google Scholar 

  102. Inobe T, Kraut DA, Matouschek A (2008) How to pick a protein and pull at it. Nat Struct Mol Biol 15(11):1135–1136

    PubMed  CAS  Google Scholar 

  103. Martin A, Baker TA, Sauer RT (2008) Pore loops of the AAA  +  ClpX machine grip substrates to drive translocation and unfolding. Nat Struct Mol Biol 15(11):1147–1151

    PubMed  CAS  Google Scholar 

  104. Martin A, Baker TA, Sauer RT (2008) Diverse pore loops of the AAA  +  ClpX machine mediate unassisted and adaptor-dependent recognition of ssrA-tagged substrates. Mol Cell 29(4):441–450

    PubMed  CAS  Google Scholar 

  105. Wang J, Song JJ, Seong IS, Franklin MC et al (2001) Nucleotide-dependent conformational changes in a protease-associated ATPase HsIU. Structure 9(11):1107–1116

    PubMed  CAS  Google Scholar 

  106. Smith DM, Fraga H, Reis C, Kafri G et al (2011) ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle. Cell 144(4):526–538

    PubMed  CAS  Google Scholar 

  107. Ehlers C, Kopp F, Dahlmann B (1997) Screening for molecules interacting with proteasomes in Thermoplasma acidophilum. Biol Chem 378(3–4):249–253

    PubMed  CAS  Google Scholar 

  108. Kusmierczyk AR, Kunjappu MJ, Kim RY, Hochstrasser M (2011) A conserved 20S proteasome assembly factor requires a C-terminal HbYX motif for proteasomal precursor binding. Nat Struct Mol Biol 18(5):622–629

    PubMed  CAS  Google Scholar 

  109. Hirano Y, Hendil KB, Yashiroda H, Iemura S et al (2005) A heterodimeric complex that promotes the assembly of mammalian 20S proteasomes. Nature 437(7063):1381–1385

    PubMed  CAS  Google Scholar 

  110. Le Tallec B, Barrault MB, Courbeyrette R, Guerois R et al (2007) 20S proteasome assembly is orchestrated by two distinct pairs of chaperones in yeast and in mammals. Mol Cell 27(4):660–674

    PubMed  Google Scholar 

  111. Li X, Kusmierczyk AR, Wong P, Emili A et al (2007) beta-Subunit appendages promote 20S proteasome assembly by overcoming an Ump1-dependent checkpoint. EMBO J 26(9):2339–2349

    PubMed  CAS  Google Scholar 

  112. Hochstrasser M (2009) Origin and function of ubiquitin-like proteins. Nature 458(7237):422–429

    PubMed  CAS  Google Scholar 

  113. Iwai K, Tokunaga F (2009) Linear polyubiquitination: a new regulator of NF-kappaB activation. EMBO Rep 10(7):706–713

    PubMed  CAS  Google Scholar 

  114. Wang X, Herr RA, Hansen TH (2012) Ubiquitination of substrates by esterification. Traffic 13(1):19–24

    PubMed  CAS  Google Scholar 

  115. Frappier L, Verrijzer CP (2011) Gene expression control by protein deubiquitinases. Curr Opin Genet Dev 21(2):207–213

    PubMed  CAS  Google Scholar 

  116. Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141–172

    PubMed  CAS  Google Scholar 

  117. Ramaekers CH, Wouters BG (2011) Regulatory functions of ubiquitin in diverse DNA damage responses. Curr Mol Med 11(2):152–169

    PubMed  CAS  Google Scholar 

  118. Xu P, Duong DM, Seyfried NT, Cheng D et al (2009) Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 137(1):133–145

    PubMed  CAS  Google Scholar 

  119. Lauwers E, Erpapazoglou Z, Haguenauer-Tsapis R, Andre B (2010) The ubiquitin code of yeast permease trafficking. Trends Cell Biol 20(4):196–204

    PubMed  CAS  Google Scholar 

  120. Pickart CM (1997) Targeting of substrates to the 26S proteasome. FASEB J 11(13):1055–1066

    PubMed  CAS  Google Scholar 

  121. Metzger MB, Weissman AM (2010) Working on a chain: E3s ganging up for ubiquitylation. Nat Cell Biol 12(12):1124–1126

    PubMed  CAS  Google Scholar 

  122. Pastore A (2010) Further insights into the ubiquitin pathway: understanding the scarlet letter code. Structure 18(8):891–892

    PubMed  CAS  Google Scholar 

  123. Scheffner M, Nuber U, Huibregtse JM (1995) Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 373(6509):81–83

    PubMed  CAS  Google Scholar 

  124. Ye Y, Rape M (2009) Building ubiquitin chains: E2 enzymes at work. Nat Rev Mol Cell Biol 10(11):755–764

    PubMed  CAS  Google Scholar 

  125. Hochstrasser M (2007) Ubiquitin ligation without a ligase. Dev Cell 13(1):4–6

    PubMed  CAS  Google Scholar 

  126. Hoeller D, Hecker CM, Wagner S, Rogov V et al (2007) E3-independent monoubiquitination of ubiquitin-binding proteins. Mol Cell 26(6):891–898

    PubMed  CAS  Google Scholar 

  127. Sorkin A (2007) Ubiquitination without E3. Mol Cell 26(6):771–773

    PubMed  CAS  Google Scholar 

  128. Iyer LM, Burroughs AM, Aravind L (2006) The prokaryotic antecedents of the ubiquitin-signaling system and the early evolution of ubiquitin-like beta-grasp domains. Genome Biol 7(7):R60

    PubMed  Google Scholar 

  129. Jurgenson CT, Begley TP, Ealick SE (2009) The structural and biochemical foundations of thiamin biosynthesis. Annu Rev Biochem 78:569–603

    PubMed  CAS  Google Scholar 

  130. Schwarz G, Mendel RR, Ribbe MW (2009) Molybdenum cofactors, enzymes and pathways. Nature 460(7257):839–847

    PubMed  CAS  Google Scholar 

  131. Godert AM, Jin M, McLafferty FW, Begley TP (2007) Biosynthesis of the thioquinolobactin siderophore: an interesting variation on sulfur transfer. J Bacteriol 189(7):2941–2944

    PubMed  CAS  Google Scholar 

  132. Jurgenson CT, Burns KE, Begley TP, Ealick SE (2008) Crystal structure of a sulfur carrier protein complex found in the cysteine biosynthetic pathway of Mycobacterium tuberculosis. Biochemistry 47(39):10354–10364

    PubMed  CAS  Google Scholar 

  133. O’Leary SE, Jurgenson CT, Ealick SE, Begley TP (2008) O-phospho-L-serine and the thiocarboxylated sulfur carrier protein CysO-COSH are substrates for CysM, a cysteine synthase from Mycobacterium tuberculosis. Biochemistry 47(44):11606–11615

    PubMed  Google Scholar 

  134. Burroughs AM, Balaji S, Iyer LM, Aravind L (2007) Small but versatile: the extraordinary functional and structural diversity of the beta-grasp fold. Biol Direct 2:18

    PubMed  Google Scholar 

  135. Burroughs AM, Iyer LM, Aravind L (2009) Natural history of the E1-like superfamily: implication for adenylation, sulfur transfer, and ubiquitin conjugation. Proteins 75(4):895–910

    PubMed  CAS  Google Scholar 

  136. Lehmann C, Begley TP, Ealick SE (2006) Structure of the Escherichia coli ThiS-ThiF complex, a key component of the sulfur transfer system in thiamin biosynthesis. Biochemistry 45(1):11–19

    PubMed  CAS  Google Scholar 

  137. Schmitz J, Wuebbens MM, Rajagopalan KV, Leimkuhler S (2007) Role of the C-terminal Gly-Gly motif of Escherichia coli MoaD, a molybdenum cofactor biosynthesis protein with a ubiquitin fold. Biochemistry 46(3):909–916

    PubMed  CAS  Google Scholar 

  138. Dahl JU, Urban A, Bolte A, Sriyabhaya P et al (2011) The identification of a novel protein involved in molybdenum cofactor biosynthesis in Escherichia coli. J Biol Chem 286(41):35801–35812

    PubMed  CAS  Google Scholar 

  139. Zhang W, Urban A, Mihara H, Leimkuhler S et al (2010) IscS functions as a primary sulfur-donating enzyme by interacting specifically with MoeB and MoaD in the biosynthesis of molybdopterin in Escherichia coli. J Biol Chem 285(4):2302–2308

    PubMed  CAS  Google Scholar 

  140. Mueller EG (2006) Trafficking in persulfides: delivering sulfur in biosynthetic pathways. Nat Chem Biol 2(4):185–194

    PubMed  CAS  Google Scholar 

  141. Humbard MA, Miranda HV, Lim JM, Krause DJ et al (2010) Ubiquitin-like small archaeal modifier proteins (SAMPs) in Haloferax volcanii. Nature 463(7277):54–60

    PubMed  CAS  Google Scholar 

  142. Miranda HV, Nembhard N, Su D, Hepowit N et al (2011) E1- and ubiquitin-like proteins provide a direct link between protein conjugation and sulfur transfer in archaea. Proc Natl Acad Sci U S A 108(11):4417–4422

    PubMed  CAS  Google Scholar 

  143. Zhang Y, Gladyshev VN (2008) Molybdoproteomes and evolution of molybdenum utilization. J Mol Biol 379(4):881–899

    PubMed  CAS  Google Scholar 

  144. Burroughs AM, Iyer LM, Aravind L (2011) Functional diversification of the RING finger and other binuclear treble clef domains in prokaryotes and the early evolution of the ubiquitin system. Mol Biosyst 7(7):2261–2277

    PubMed  CAS  Google Scholar 

  145. Hartman AL, Norais C, Badger JH, Delmas S et al (2010) The complete genome sequence of Haloferax volcanii DS2, a model archaeon. PLoS One 5(3):e9605

    PubMed  Google Scholar 

  146. Makarova KS, Koonin EV (2010) Archaeal ubiquitin-like proteins: functional versatility and putative ancestral involvement in tRNA modification revealed by comparative genomic analysis. Archaea 2010. doi: pii: 710303

    Google Scholar 

  147. Wagner SA, Beli P, Weinert BT, Nielsen ML et al (2011) A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 10(10):M111 013284

    PubMed  Google Scholar 

  148. Yang XJ (2005) Multisite protein modification and intramolecular signaling. Oncogene 24(10):1653–1662

    PubMed  CAS  Google Scholar 

  149. Baker RT, Board PG (1987) The human ubiquitin gene family: structure of a gene and pseudogenes from the Ub B subfamily. Nucleic Acids Res 15(2):443–463

    PubMed  CAS  Google Scholar 

  150. Lund PK, Moats-Staats BM, Simmons JG, Hoyt E et al (1985) Nucleotide sequence analysis of a cDNA encoding human ubiquitin reveals that ubiquitin is synthesized as a precursor. J Biol Chem 260(12):7609–7613

    PubMed  CAS  Google Scholar 

  151. Wiborg O, Pedersen MS, Wind A, Berglund LE et al (1985) The human ubiquitin multigene family: some genes contain multiple directly repeated ubiquitin coding sequences. EMBO J 4(3):755–759

    PubMed  CAS  Google Scholar 

  152. Ozkaynak E, Finley D, Solomon MJ, Varshavsky A (1987) The yeast ubiquitin genes: a family of natural gene fusions. EMBO J 6(5):1429–1439

    PubMed  CAS  Google Scholar 

  153. Katz EJ, Isasa M, Crosas B (2010) A new map to understand deubiquitination. Biochem Soc Trans 38(Pt 1):21–28

    PubMed  CAS  Google Scholar 

  154. Kirkland PA, Gil MA, Karadzic IM, Maupin-Furlow JA (2008) Genetic and proteomic analyses of a proteasome-activating nucleotidase A mutant of the haloarchaeon Haloferax volcanii. J Bacteriol 190(1):193–205

    PubMed  CAS  Google Scholar 

  155. Kirkland PA, Reuter CJ, Maupin-Furlow JA (2007) Effect of proteasome inhibitor clasto-lactacystin-beta-lactone on the proteome of the haloarchaeon Haloferax volcanii. Microbiology 153(Pt 7):2271–2280

    PubMed  CAS  Google Scholar 

  156. Leidel S, Pedrioli PG, Bucher T, Brost R et al (2009) Ubiquitin-related modifier Urm1 acts as a sulphur carrier in thiolation of eukaryotic transfer RNA. Nature 458(7235):228–232

    PubMed  CAS  Google Scholar 

  157. Shigi N, Sakaguchi Y, Asai S, Suzuki T et al (2008) Common thiolation mechanism in the biosynthesis of tRNA thiouridine and sulphur-containing cofactors. EMBO J 27(24):3267–3278

    PubMed  CAS  Google Scholar 

  158. Nunoura T, Takaki Y, Kakuta J, Nishi S et al (2011) Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res 39(8):3204–3223

    PubMed  CAS  Google Scholar 

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Acknowledgments

This work was funded in part by grants from the National Institutes of Health (GM57498) and the Department of Energy Office of Basic Energy Sciences (DE-FG02-05ER15650).

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  1. Department of Microbiology and Cell Science, University of Florida, Gainesville, FL, 32611-0700, USA

    Julie A. Maupin-Furlow

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Correspondence to Julie A. Maupin-Furlow .

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  1. , Department of Biochemistry, La Trobe Institute for Molecular Science, Plenty Rd, Melbourne, 3086, Victoria, Australia

    David A. Dougan

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Maupin-Furlow, J.A. (2013). Archaeal Proteasomes and Sampylation. In: Dougan, D. (eds) Regulated Proteolysis in Microorganisms. Subcellular Biochemistry, vol 66. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5940-4_11

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