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Crystal structure of A. fulgidus Rio2 defines a new family of serine protein kinases.

LaRonde-LeBlanc N, Wlodawer A
Structure 12 1585-94 (2004)
Related entries: 1tqi, 1tqp

Cited: 49 times
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Abstract

The RIO family of atypical serine/threonine kinases contains two subfamilies, Rio1 and Rio2, highly conserved from archaea to man. Both RIO proteins from Saccharomyces cerevisiae catalyze serine phosphorylation in vitro, and the presence of conserved catalytic residues is required for cell viability. The activity of Rio2 is necessary for rRNA cleavage in 40S ribosomal subunit maturation. We solved the X-ray crystal structure of Archaeoglobus fulgidus Rio2, with and without bound nucleotides, at 2.0 A resolution. The C-terminal RIO domain is indeed structurally homologous to protein kinases, although it differs from known serine kinases in ATP binding and lacks the regions important for substrate binding. Unexpectedly, the N-terminal Rio2-specific domain contains a winged helix fold, seen primarily in DNA-binding proteins. These discoveries have implications in determining the target and function of RIO proteins and define a distinct new family of protein kinases.

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Reviews citing this publication (7)

  1. The many faces of the helix-turn-helix domain: transcription regulation and beyond. Aravind L, Anantharaman V, Balaji S, Babu MM, Iyer LM. FEMS Microbiol Rev 29 231-262 (2005)
  2. Powering through ribosome assembly. Strunk BS, Karbstein K. RNA 15 2083-2104 (2009)
  3. Protein phosphorylation and its role in archaeal signal transduction. Esser D, Hoffmann L, Pham TK, Bräsen C, Qiu W, Wright PC, Albers SV, Siebers B. FEMS Microbiol Rev 40 625-647 (2016)
  4. Resilience of biochemical activity in protein domains in the face of structural divergence. Zhang D, Iyer LM, Burroughs AM, Aravind L. Curr Opin Struct Biol 26 92-103 (2014)
  5. The ancient microbial RIO kinases. LaRonde NA. J Biol Chem 289 9488-9492 (2014)
  6. Atypical protein kinases of the RIO family in archaea. Esser D, Siebers B. Biochem Soc Trans 41 399-404 (2013)
  7. Domain Organization in Plant Blue-Light Receptor Phototropin2 of Arabidopsis thaliana Studied by Small-Angle X-ray Scattering. Nakasako M, Oide M, Takayama Y, Oroguchi T, Okajima K. Int J Mol Sci 21 E6638 (2020)

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  1. Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. Parsons M, Worthey EA, Ward PN, Mottram JC. BMC Genomics 6 127 (2005)
  2. Structural and functional diversity of the microbial kinome. Kannan N, Taylor SS, Zhai Y, Venter JC, Manning G. PLoS Biol 5 e17 (2007)
  3. Did protein kinase regulatory mechanisms evolve through elaboration of a simple structural component? Kannan N, Neuwald AF. J Mol Biol 351 956-972 (2005)
  4. Genomic alterations link Rho family of GTPases to the highly invasive phenotype of pancreas cancer. Kimmelman AC, Hezel AF, Aguirre AJ, Zheng H, Paik JH, Ying H, Chu GC, Zhang JX, Sahin E, Yeo G, Ponugoti A, Nabioullin R, Deroo S, Yang S, Wang X, McGrath JP, Protopopova M, Ivanova E, Zhang J, Feng B, Tsao MS, Redston M, Protopopov A, Xiao Y, Futreal PA, Hahn WC, Klimstra DS, Chin L, DePinho RA. Proc Natl Acad Sci U S A 105 19372-19377 (2008)
  5. Structure and functional characterization of the atypical human kinase haspin. Eswaran J, Patnaik D, Filippakopoulos P, Wang F, Stein RL, Murray JW, Higgins JM, Knapp S. Proc Natl Acad Sci U S A 106 20198-20203 (2009)
  6. Classification and functional annotation of eukaryotic protein kinases. Miranda-Saavedra D, Barton GJ. Proteins 68 893-914 (2007)
  7. ATPase-dependent role of the atypical kinase Rio2 on the evolving pre-40S ribosomal subunit. Ferreira-Cerca S, Sagar V, Schäfer T, Diop M, Wesseling AM, Lu H, Chai E, Hurt E, LaRonde-LeBlanc N. Nat Struct Mol Biol 19 1316-1323 (2012)
  8. The kinase activity of human Rio1 is required for final steps of cytoplasmic maturation of 40S subunits. Widmann B, Wandrey F, Badertscher L, Wyler E, Pfannstiel J, Zemp I, Kutay U. Mol Biol Cell 23 22-35 (2012)
  9. A family portrait of the RIO kinases. LaRonde-LeBlanc N, Wlodawer A. J Biol Chem 280 37297-37300 (2005)
  10. Mitochondrial ADCK3 employs an atypical protein kinase-like fold to enable coenzyme Q biosynthesis. Stefely JA, Reidenbach AG, Ulbrich A, Oruganty K, Floyd BJ, Jochem A, Saunders JM, Johnson IE, Minogue CE, Wrobel RL, Barber GE, Lee D, Li S, Kannan N, Coon JJ, Bingman CA, Pagliarini DJ. Mol Cell 57 83-94 (2015)
  11. Ser/Thr/Tyr protein phosphorylation in the archaeon Halobacterium salinarum--a representative of the third domain of life. Aivaliotis M, Macek B, Gnad F, Reichelt P, Mann M, Oesterhelt D. PLoS One 4 e4777 (2009)
  12. Structure of a eukaryotic cytoplasmic pre-40S ribosomal subunit. Scaiola A, Peña C, Weisser M, Böhringer D, Leibundgut M, Klingauf-Nerurkar P, Gerhardy S, Panse VG, Panse VG, Ban N. EMBO J 37 e98499 (2018)
  13. Structural and functional analysis of the archaeal endonuclease Nob1. Veith T, Martin R, Wurm JP, Weis BL, Duchardt-Ferner E, Safferthal C, Hennig R, Mirus O, Bohnsack MT, Wöhnert J, Schleiff E. Nucleic Acids Res 40 3259-3274 (2012)
  14. Structure and activity of the atypical serine kinase Rio1. Laronde-Leblanc N, Guszczynski T, Copeland T, Wlodawer A. FEBS J 272 3698-3713 (2005)
  15. Conservation, variability and the modeling of active protein kinases. Knight JD, Qian B, Baker D, Kothary R. PLoS One 2 e982 (2007)
  16. Human RioK3 is a novel component of cytoplasmic pre-40S pre-ribosomal particles. Baumas K, Soudet J, Caizergues-Ferrer M, Faubladier M, Henry Y, Mougin A. RNA Biol 9 162-174 (2012)
  17. Autophosphorylation of Archaeoglobus fulgidus Rio2 and crystal structures of its nucleotide-metal ion complexes. LaRonde-LeBlanc N, Guszczynski T, Copeland T, Wlodawer A. FEBS J 272 2800-2810 (2005)
  18. Essential ribosome assembly factor Fap7 regulates a hierarchy of RNA-protein interactions during small ribosomal subunit biogenesis. Hellmich UA, Weis BL, Lioutikov A, Wurm JP, Kaiser M, Christ NA, Hantke K, Kötter P, Entian KD, Schleiff E, Wöhnert J. Proc Natl Acad Sci U S A 110 15253-15258 (2013)
  19. Conformational proofreading of distant 40S ribosomal subunit maturation events by a long-range communication mechanism. Mitterer V, Shayan R, Ferreira-Cerca S, Murat G, Enne T, Rinaldi D, Weigl S, Omanic H, Gleizes PE, Kressler D, Plisson-Chastang C, Pertschy B. Nat Commun 10 2754 (2019)
  20. Interaction of Rio1 kinase with toyocamycin reveals a conformational switch that controls oligomeric state and catalytic activity. Kiburu IN, LaRonde-LeBlanc N. PLoS One 7 e37371 (2012)
  21. Archaeal eukaryote-like serine/threonine protein kinase interacts with and phosphorylates a forkhead-associated-domain-containing protein. Wang B, Yang S, Zhang L, He ZG. J Bacteriol 192 1956-1964 (2010)
  22. Aminoglycoside 2''-phosphotransferase IIIa (APH(2'')-IIIa) prefers GTP over ATP: structural templates for nucleotide recognition in the bacterial aminoglycoside-2'' kinases. Smith CA, Toth M, Frase H, Byrnes LJ, Vakulenko SB. J Biol Chem 287 12893-12903 (2012)
  23. Characterization of a toxin-antitoxin system in Mycobacterium tuberculosis suggests neutralization by phosphorylation as the antitoxicity mechanism. Yu X, Gao X, Zhu K, Yin H, Mao X, Wojdyla JA, Qin B, Huang H, Wang M, Sun YC, Cui S. Commun Biol 3 216 (2020)
  24. Bioinformatic exploration of RIO protein kinases of parasitic and free-living nematodes. Breugelmans B, Jex AR, Korhonen PK, Mangiola S, Young ND, Sternberg PW, Boag PR, Hofmann A, Gasser RB. Int J Parasitol 44 827-836 (2014)
  25. Development of novel molecular probes of the Rio1 atypical protein kinase. Mielecki M, Krawiec K, Kiburu I, Grzelak K, Zagórski W, Kierdaszuk B, Kowa K, Fokt I, Szymanski S, Swierk P, Szeja W, Priebe W, Lesyng B, LaRonde-LeBlanc N. Biochim Biophys Acta 1834 1292-1301 (2013)
  26. Investigating the role of RIO protein kinases in Caenorhabditis elegans. Mendes TK, Novakovic S, Raymant G, Bertram SE, Esmaillie R, Nadarajan S, Breugelmans B, Hofmann A, Gasser RB, Colaiácovo MP, Boag PR. PLoS One 10 e0117444 (2015)
  27. Toward understanding the functional role of Ss-RIOK-1, a RIO protein kinase-encoding gene of Strongyloides stercoralis. Yuan W, Lok JB, Stoltzfus JD, Gasser RB, Fang F, Lei WQ, Fang R, Zhou YQ, Zhao JL, Hu M. PLoS Negl Trop Dis 8 e3062 (2014)
  28. Crystal structure of human RIOK2 bound to a specific inhibitor. Wang J, Varin T, Vieth M, Elkins JM. Open Biol 9 190037 (2019)
  29. Structure of Arabidopsis thaliana 5-methylthioribose kinase reveals a more occluded active site than its bacterial homolog. Ku SY, Cornell KA, Howell PL. BMC Struct Biol 7 70 (2007)
  30. The RIO protein kinase-encoding gene Sj-riok-2 is involved in key reproductive processes in Schistosoma japonicum. Zhao L, He X, Grevelding CG, Ye Q, Li Y, Gasser RB, Dissous C, Mughal MN, Zhou YQ, Zhao JL, Hu M. Parasit Vectors 10 604 (2017)
  31. Tv-RIO1 - an atypical protein kinase from the parasitic nematode Trichostrongylus vitrinus. Hu M, Laronde-Leblanc N, Sternberg PW, Gasser RB. Parasit Vectors 1 34 (2008)
  32. Exploring features and function of Ss-riok-3, an enigmatic kinase gene from Strongyloides stercoralis. Yuan W, Liu Y, Lok JB, Stoltzfus JD, Gasser RB, Lei W, Fang R, Zhao J, Hu M. Parasit Vectors 7 561 (2014)
  33. F429 Regulation of Tunnels in Cytochrome P450 2B4: A Top Down Study of Multiple Molecular Dynamics Simulations. Mancini G, Zazza C. PLoS One 10 e0137075 (2015)
  34. Flatworms have lost the right open reading frame kinase 3 gene during evolution. Breugelmans B, Ansell BR, Young ND, Amani P, Stroehlein AJ, Sternberg PW, Jex AR, Boag PR, Hofmann A, Gasser RB. Sci Rep 5 9417 (2015)
  35. Genome-wide identification and characterization of the RIO atypical kinase family in plants. Gao Q, Xu S, Zhu X, Wang L, Yang Z, Zhao X. Genes Genomics 40 669-683 (2018)
  36. Letter In silico characterization of atypical kinase PFD0975w from Plasmodium kinome: a suitable target for drug discovery. Trivedi V, Nag S. Chem Biol Drug Des 79 600-609 (2012)
  37. Functional genomic exploration reveals that Ss-RIOK-1 is essential for the development and survival of Strongyloides stercoralis larvae. Yuan W, Zhou H, Lok JB, Lei W, He S, Gasser RB, Zhou R, Fang R, Zhou Y, Zhao J, Hu M. Int J Parasitol 47 933-940 (2017)
  38. In vitro dimerization of human RIO2 kinase. Maurice F, Pérébaskine N, Thore S, Fribourg S. RNA Biol 16 1633-1642 (2019)
  39. Structural and developmental expression of Ss-riok-2, an RIO protein kinase encoding gene of Strongyloides stercoralis. Lei WQ, Lok JB, Yuan W, Zhang YZ, Stoltzfus JD, Gasser RB, He SY, Zhou H, Zhou R, Zhao JL, Hu M. Sci Rep 7 8693 (2017)
  40. Molecular and structural insight into plasmodium falciparum RIO2 kinase. Chouhan DK, Sharon A, Bal C. J Mol Model 19 485-496 (2013)
  41. Exploration of tricyclic heterocycles as core structures for RIOK2 inhibitors. Xiong H, Yu Q, Ma H, Yu X, Ouyang Y, Zhang ZM, Zhou W, Zhang Z, Cai Q. RSC Med Chem 14 2007-2011 (2023)


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