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The C-terminal fragment of the ribosomal P protein complexed to trichosanthin reveals the interaction between the ribosome-inactivating protein and the ribosome.

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Too PH, Ma MK, Mak AN, Wong YT, Tung CK, Zhu G, Au SW, Wong KB, Shaw PC
OpenAccess logo Nucleic Acids Res 37 602-10 (2009)
Related entries: 2jdl, 2jjr

Cited: 47 times
EuropePMC logo PMID: 19073700

Abstract

Ribosome-inactivating proteins (RIPs) inhibit protein synthesis by enzymatically depurinating a specific adenine residue at the sarcin-ricin loop of the 28S rRNA, which thereby prevents the binding of elongation factors to the GTPase activation centre of the ribosome. Here, we present the 2.2 A crystal structure of trichosanthin (TCS) complexed to the peptide SDDDMGFGLFD, which corresponds to the conserved C-terminal elongation factor binding domain of the ribosomal P protein. The N-terminal region of this peptide interacts with Lys173, Arg174 and Lys177 in TCS, while the C-terminal region is inserted into a hydrophobic pocket. The interaction with the P protein contributes to the ribosome-inactivating activity of TCS. This 11-mer C-terminal P peptide can be docked with selected important plant and bacterial RIPs, indicating that a similar interaction may also occur with other RIPs.

Articles - 2vs6 mentioned but not cited (1)

  1. The C-terminal fragment of the ribosomal P protein complexed to trichosanthin reveals the interaction between the ribosome-inactivating protein and the ribosome. Too PH, Ma MK, Mak AN, Wong YT, Tung CK, Zhu G, Au SW, Wong KB, Shaw PC. Nucleic Acids Res 37 602-610 (2009)


Reviews citing this publication (12)

  1. Interaction of ricin and Shiga toxins with ribosomes. Tumer NE, Li XP. Curr Top Microbiol Immunol 357 1-18 (2012)
  2. Targeting ricin to the ribosome. May KL, Yan Q, Tumer NE. Toxicon 69 143-151 (2013)
  3. Structures and Ribosomal Interaction of Ribosome-Inactivating Proteins. Shi WW, Mak AN, Wong KB, Shaw PC. Molecules 21 E1588 (2016)
  4. How Ricin Damages the Ribosome. Grela P, Szajwaj M, Horbowicz-Drożdżal P, Tchórzewski M. Toxins (Basel) 11 E241 (2019)
  5. Structures of eukaryotic ribosomal stalk proteins and its complex with trichosanthin, and their implications in recruiting ribosome-inactivating proteins to the ribosomes. Choi AK, Wong EC, Lee KM, Wong KB. Toxins (Basel) 7 638-647 (2015)
  6. Bioactive proteins and peptides isolated from Chinese medicines with pharmaceutical potential. Wong KL, Wong RN, Zhang L, Liu WK, Ng TB, Shaw PC, Kwok PC, Lai YM, Zhang ZJ, Zhang Y, Tong Y, Cheung HP, Lu J, Sze SC. Chin Med 9 19 (2014)
  7. Biological activities of ribosome-inactivating proteins and their possible applications as antimicrobial, anticancer, and anti-pest agents and in neuroscience research. Akkouh O, Ng TB, Cheung RC, Wong JH, Pan W, Ng CC, Sha O, Shaw PC, Chan WY. Appl Microbiol Biotechnol 99 9847-9863 (2015)
  8. Extensive Evolution of Cereal Ribosome-Inactivating Proteins Translates into Unique Structural Features, Activation Mechanisms, and Physiological Roles. De Zaeytijd J, Van Damme EJ. Toxins (Basel) 9 E123 (2017)
  9. Functional Assays for Measuring the Catalytic Activity of Ribosome Inactivating Proteins. Zhou Y, Li XP, Kahn JN, Tumer NE. Toxins (Basel) 10 E240 (2018)
  10. Do the A subunits contribute to the differences in the toxicity of Shiga toxin 1 and Shiga toxin 2? Basu D, Tumer NE. Toxins (Basel) 7 1467-1485 (2015)
  11. Structural and Functional Investigation and Pharmacological Mechanism of Trichosanthin, a Type 1 Ribosome-Inactivating Protein. Shi WW, Wong KB, Shaw PC. Toxins (Basel) 10 E335 (2018)
  12. A Sixty-Year Research and Development of Trichosanthin, a Ribosome-Inactivating Protein. Lu JQ, Wong KB, Shaw PC. Toxins (Basel) 14 178 (2022)

Articles citing this publication (34)

  1. A two-step binding model proposed for the electrostatic interactions of ricin a chain with ribosomes. Li XP, Chiou JC, Remacha M, Ballesta JP, Tumer NE. Biochemistry 48 3853-3863 (2009)
  2. Arginine residues on the opposite side of the active site stimulate the catalysis of ribosome depurination by ricin A chain by interacting with the P-protein stalk. Li XP, Kahn PC, Kahn JN, Grela P, Tumer NE. J Biol Chem 288 30270-30284 (2013)
  3. Solution structure of human P1•P2 heterodimer provides insights into the role of eukaryotic stalk in recruiting the ribosome-inactivating protein trichosanthin to the ribosome. Lee KM, Yusa K, Chu LO, Yu CW, Oono M, Miyoshi T, Ito K, Shaw PC, Wong KB, Uchiumi T. Nucleic Acids Res 41 8776-8787 (2013)
  4. Molecular insights into the interaction of the ribosomal stalk protein with elongation factor 1α. Ito K, Honda T, Suzuki T, Miyoshi T, Murakami R, Yao M, Uchiumi T. Nucleic Acids Res 42 14042-14052 (2014)
  5. Shiga toxin 1 is more dependent on the P proteins of the ribosomal stalk for depurination activity than Shiga toxin 2. Chiou JC, Li XP, Remacha M, Ballesta JP, Tumer NE. Int J Biochem Cell Biol 43 1792-1801 (2011)
  6. Solution structure of an active mutant of maize ribosome-inactivating protein (MOD) and its interaction with the ribosomal stalk protein P2. Yang Y, Mak AN, Shaw PC, Sze KH. J Mol Biol 395 897-907 (2010)
  7. Solution structure of the dimerization domain of ribosomal protein P2 provides insights for the structural organization of eukaryotic stalk. Lee KM, Yu CW, Chan DS, Chiu TY, Zhu G, Sze KH, Shaw PC, Wong KB. Nucleic Acids Res 38 5206-5216 (2010)
  8. Charged and hydrophobic surfaces on the a chain of shiga-like toxin 1 recognize the C-terminal domain of ribosomal stalk proteins. McCluskey AJ, Bolewska-Pedyczak E, Jarvik N, Chen G, Sidhu SS, Gariépy J. PLoS One 7 e31191 (2012)
  9. Pentameric organization of the ribosomal stalk accelerates recruitment of ricin a chain to the ribosome for depurination. Li XP, Grela P, Krokowski D, Tchórzewski M, Tumer NE. J Biol Chem 285 41463-41471 (2010)
  10. The P1/P2 proteins of the human ribosomal stalk are required for ribosome binding and depurination by ricin in human cells. May KL, Li XP, Martínez-Azorín F, Ballesta JP, Grela P, Tchórzewski M, Tumer NE. FEBS J 279 3925-3936 (2012)
  11. Small-molecule inhibitor leads of ribosome-inactivating proteins developed using the doorstop approach. Pang YP, Park JG, Wang S, Vummenthala A, Mishra RK, McLaughlin JE, Di R, Kahn JN, Tumer NE, Janosi L, Davis J, Millard CB. PLoS One 6 e17883 (2011)
  12. Solution structure of the dimerization domain of the eukaryotic stalk P1/P2 complex reveals the structural organization of eukaryotic stalk complex. Lee KM, Yu CW, Chiu TY, Sze KH, Shaw PC, Wong KB. Nucleic Acids Res 40 3172-3182 (2012)
  13. A switch-on mechanism to activate maize ribosome-inactivating protein for targeting HIV-infected cells. Law SK, Wang RR, Mak AN, Wong KB, Zheng YT, Shaw PC. Nucleic Acids Res 38 6803-6812 (2010)
  14. The A1 Subunit of Shiga Toxin 2 Has Higher Affinity for Ribosomes and Higher Catalytic Activity than the A1 Subunit of Shiga Toxin 1. Basu D, Li XP, Kahn JN, May KL, Kahn PC, Tumer NE. Infect Immun 84 149-161 (2016)
  15. The Interaction between the Ribosomal Stalk Proteins and Translation Initiation Factor 5B Promotes Translation Initiation. Murakami R, Singh CR, Morris J, Tang L, Harmon I, Takasu A, Miyoshi T, Ito K, Asano K, Uchiumi T. Mol Cell Biol 38 e00067-18 (2018)
  16. Crystal Structure of Ribosome-Inactivating Protein Ricin A Chain in Complex with the C-Terminal Peptide of the Ribosomal Stalk Protein P2. Shi WW, Tang YS, Sze SY, Zhu ZN, Wong KB, Shaw PC. Toxins (Basel) 8 E296 (2016)
  17. Ricin uses arginine 235 as an anchor residue to bind to P-proteins of the ribosomal stalk. Zhou Y, Li XP, Chen BY, Tumer NE. Sci Rep 7 42912 (2017)
  18. Differences in Ribosome Binding and Sarcin/Ricin Loop Depurination by Shiga and Ricin Holotoxins. Li XP, Tumer NE. Toxins (Basel) 9 E133 (2017)
  19. Maize ribosome-inactivating protein uses Lys158-lys161 to interact with ribosomal protein P2 and the strength of interaction is correlated to the biological activities. Wong YT, Ng YM, Mak AN, Sze KH, Wong KB, Shaw PC. PLoS One 7 e49608 (2012)
  20. Structural insights into the interaction of the ribosomal P stalk protein P2 with a type II ribosome-inactivating protein ricin. Fan X, Zhu Y, Wang C, Niu L, Teng M, Li X. Sci Rep 6 37803 (2016)
  21. Human ribosomal P1-P2 heterodimer represents an optimal docking site for ricin A chain with a prominent role for P1 C-terminus. Grela P, Li XP, Horbowicz P, Dźwierzyńska M, Tchórzewski M, Tumer NE. Sci Rep 7 5608 (2017)
  22. Functional role of the C-terminal tail of the archaeal ribosomal stalk in recruitment of two elongation factors to the sarcin/ricin loop of 23S rRNA. Imai H, Miyoshi T, Murakami R, Ito K, Ishino Y, Uchiumi T. Genes Cells 20 613-624 (2015)
  23. Toxicity of ricin A chain is reduced in mammalian cells by inhibiting its interaction with the ribosome. Jetzt AE, Li XP, Tumer NE, Cohick WS. Toxicol Appl Pharmacol 310 120-128 (2016)
  24. Engineered toxins "zymoxins" are activated by the HCV NS3 protease by removal of an inhibitory protein domain. Shapira A, Gal-Tanamy M, Nahary L, Litvak-Greenfeld D, Zemel R, Tur-Kaspa R, Benhar I. PLoS One 6 e15916 (2011)
  25. Functional divergence between the two P1-P2 stalk dimers on the ribosome in their interaction with ricin A chain. Grela P, Li XP, Tchórzewski M, Tumer NE. Biochem J 460 59-67 (2014)
  26. Peptide Mimics of the Ribosomal P Stalk Inhibit the Activity of Ricin A Chain by Preventing Ribosome Binding. Li XP, Kahn JN, Tumer NE. Toxins (Basel) 10 E371 (2018)
  27. Structural basis for the interaction of Shiga toxin 2a with a C-terminal peptide of ribosomal P stalk proteins. Rudolph MJ, Davis SA, Tumer NE, Li XP. J Biol Chem 295 15588-15596 (2020)
  28. Conserved Arginines at the P-Protein Stalk Binding Site and the Active Site Are Critical for Ribosome Interactions of Shiga Toxins but Do Not Contribute to Differences in the Affinity of the A1 Subunits for the Ribosome. Basu D, Kahn JN, Li XP, Tumer NE. Infect Immun 84 3290-3301 (2016)
  29. Cryo-EM structure of Shiga toxin 2 in complex with the native ribosomal P-stalk reveals residues involved in the binding interaction. Kulczyk AW, Sorzano COS, Grela P, Tchórzewski M, Tumer NE, Li XP. J Biol Chem 299 102795 (2023)
  30. Comparative Proteomic Analysis of Drug Trichosanthin Addition to BeWo Cell Line. Hu Y, Yao J, Wang Z, Liang H, Li C, Zhou X, Yang F, Zhang Y, Jin H. Molecules 27 1603 (2022)
  31. Leucine 232 and hydrophobic residues at the ribosomal P stalk binding site are critical for biological activity of ricin. Zhou Y, Li XP, Kahn JN, McLaughlin JE, Tumer NE. Biosci Rep 39 BSR20192022 (2019)
  32. Structure and Biological Properties of Ribosome-Inactivating Proteins and Lectins from Elder (Sambucus nigra L.) Leaves. Iglesias R, Russo R, Landi N, Valletta M, Chambery A, Di Maro A, Bolognesi A, Ferreras JM, Citores L. Toxins (Basel) 14 611 (2022)
  33. The ribosome-inactivating proteins MAP30 and Momordin inhibit SARS-CoV-2. Watts NR, Eren E, Palmer I, Huang PL, Huang PL, Shoemaker RH, Lee-Huang S, Wingfield PT. PLoS One 18 e0286370 (2023)
  34. The unique N-terminal insert in the ribosomal protein, phosphoprotein P0, of Tetrahymena thermophila: Bioinformatic evidence for an interaction with 26S rRNA. Pagano GJ, King RS, Martin LM, Hufnagel LA. Proteins 83 1078-1090 (2015)


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