Targeting ricin to the ribosome

Toxicon

Volumn 69, Issue , 2013, Pages 143-151

  May, Kerrie L ^a   Yan, Qing ^a   Tumer, Nilgun E ^a  

^a Rutgers University   (United States)

Author keywords

Ribosomal stalk; Ribosome; Ribosome inactivating protein; Ricin

Indexed keywords

ADENINE; GLYCOSIDASE; HYPOXANTHINE; RIBOSOME INACTIVATING PROTEIN; RIBOSOME PROTEIN; RICIN; RNA 28S; ANTIDOTE;

ARTICLE; BIOLOGICAL WARFARE; CYTOTOXICITY; ENZYME ACTIVE SITE; HUMAN; INTRACELLULAR SIGNALING; MAMMAL CELL; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RIBOSOME; RNA TRANSLATION; ANIMAL; APOPTOSIS; CHEMISTRY; DRUG EFFECTS; METABOLISM; PREVENTION AND CONTROL; SIGNAL TRANSDUCTION; TOXICITY; CHEMICAL MODIFICATION; DEPURINATION; NUCLEOTIDE SEQUENCE; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RNA STRUCTURE; TOXIN RIBOSOME INTERACTION; DRUG EFFECT; REVIEW;

MAMMALIA;

ANIMALS; APOPTOSIS; BIOTERRORISM; HUMANS; RIBOSOME INACTIVATING PROTEINS; RIBOSOMES; RICIN; RNA, RIBOSOMAL, 28S; SIGNAL TRANSDUCTION;

EID: 84878496230     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2013.02.001     Document Type: Article

References (106)

1. Agrawal R.K., Penczek P., Grassucci R.A., Frank J. Visualization of elongation factor G on the Escherichia coli 70S ribosome: the mechanism of translocation. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:6134-6138.
2. Argent R.H., Parrott A.M., Day P.J., Roberts L.M., Stockley P.G., Lord J.M., Radford S.E. Ribosome-mediated folding of partially unfolded ricin A-chain. J. Biol. Chem. 2000, 275:9263-9269.
3. Bai Y., Monzingo A.F., Robertus J.D. The X-ray structure of ricin A chain with a novel inhibitor. Arch. Biochem. Biophys. 2009, 483:23-28.
4. Bai Y., Watt B., Wahome P.G., Mantis N.J., Robertus J.D. Identification of new classes of ricin toxin inhibitors by virtual screening. Toxicon 2010, 56:526-534.
5. Ballesta J.P., Remacha M. The large ribosomal subunit stalk as a regulatory element of the eukaryotic translational machinery. Prog. Nucleic Acid Res. Mol. Biol. 1996, 55:157-193.
6. Bergan J., Dyve Lingelem A.B., Simm R., Skotland T., Sandvig K. Shiga toxins. Toxicon 2012, 60:1085-1107.
7. Bernadó P., Modig K., Grela P., Svergun D.I., Tchórzewski M., Pons M., Akke M. Structure and dynamics of ribosomal protein L12: an ensemble model based on SAXS and NMR relaxation. Biophys. J. 2010, 98:2374-2382.
8. Brewer J.W., Diehl J.A. PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:12625-12630.
9. Cardenas D., Revuelta-Cervantes J., Jimenez-Diaz A., Camargo H., Remacha M., Ballesta J.P.G. P1 and P2 protein heterodimer binding to the P0 protein of Saccharomyces cerevisiae is relatively non-specific and a source of ribosomal heterogeneity. Nucleic Acids Res. 2012, 40:4520-4529.
10. Chan D.S.B., Chu L.-O., Lee K.-M., Too P.H.M., Ma K.-W., Sze K.H., Zhu G., Shaw P.-C., Wong K.-B. Interaction between trichosanthin, a ribosome-inactivating protein, and the ribosomal stalk protein P2 by chemical shift perturbation and mutagenesis analyses. Nucleic Acids Res. 2007, 35:1660-1672.
11. Chan S.H., Hung F.S., Chan D.S., Shaw P.C. Trichosanthin interacts with acidic ribosomal proteins P0 and P1 and mitotic checkpoint protein MAD2B. Eur. J. Biochem. 2001, 268:2107-2112.
12. Chiou J.-C., Li X.-P., Remacha M., Ballesta J.P.G., Tumer N.E. The ribosomal stalk is required for ribosome binding, depurination of the rRNA and cytotoxicity of ricin A chain in Saccharomyces cerevisiae. Mol. Microbiol. 2008, 70:1441-1452.
13. Chiou J.-C., Li X.-P., Remacha M., Ballesta J.P.G., Tumer N.E. Shiga toxin 1 is more dependent on the P proteins of the ribosomal stalk for depurination activity than Shiga toxin 2. Int. J. Biochem. Cell. Biol. 2011, 43:1792-1801.
14. Clementi N., Polacek N. Ribosome-associated GTPases: the role of RNA for GTPase activation. RNA Biol. 2010, 7:521-527.
15. de Virgilio M., Lombardi A., Caliandro R., Fabbrini M.S. Ribosome-inactivating proteins: from plant defense to tumor attack. Toxins (Basel) 2010, 2:2699-2737.
16. Dhanasekaran D.N., Reddy E.P. JNK signaling in apoptosis. Oncogene 2008, 27:6245-6251.
17. Diaconu M., Kothe U., Schlünzen F., Fischer N., Harms J.M., Tonevitsky A.G., Stark H., Rodnina M.V., Wahl M.C. Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation. Cell 2005, 121:991-1004.
18. Endo Y., Mitsui K., Motizuki M., Tsurugi K. The mechanism of action of ricin and related toxic lectins on eukaryotic ribosomes. The site and the characteristics of the modification in 28 S ribosomal RNA caused by the toxins. J. Biol. Chem. 1987, 262:5908-5912.
19. Endo Y., Tsurugi K. RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J. Biol. Chem. 1987, 262:8128-8130.
20. Endo Y., Tsurugi K. The RNA N-glycosidase activity of ricin A-chain. The characteristics of the enzymatic activity of ricin A-chain with ribosomes and with rRNA. J. Biol. Chem. 1988, 263:8735-8739.
21. Galabru J., Hovanessian A. Autophosphorylation of the protein kinase dependent on double-stranded RNA. J. Biol. Chem. 1987, 262:15538-15544.
22. García M.A., Gil J., Ventoso I., Guerra S., Domingo E., Rivas C., Esteban M. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol. Mol. Biol. Rev. 2006, 70:1032-1060.
23. García-Marcos A., Sánchez S.A., Parada P., Eid J., Jameson D.M., Remacha M., Gratton E., Ballesta J.P.G. Yeast ribosomal stalk heterogeneity in vivo shown by two-photon FCS and molecular brightness analysis. Biophys. J. 2008, 94:2884-2890.
24. Gonzalo P., Reboud J.-P. The puzzling lateral flexible stalk of the ribosome. Biol. Cell. 2003, 95:179-193.
25. Gray J.S., Bae H.K., Li J.C.B., Lau A.S., Pestka J.J. Double-stranded RNA-activated protein kinase mediates induction of interleukin-8 expression by deoxynivalenol, Shiga toxin 1, and ricin in monocytes. Toxicol. Sci. 2008, 105:322-330.
26. Grela P., Bernadó P., Svergun D., Kwiatowski J., Abramczyk D., Grankowski N., Tchórzewski M. Structural relationships among the ribosomal stalk proteins from the three domains of life. J. Mol. Evol. 2008, 67:154-167.
27. Grela P., Krokowski D., Gordiyenko Y., Krowarsch D., Robinson C.V., Otlewski J., Grankowski N., Tchórzewski M. Biophysical properties of the eukaryotic ribosomal stalk. Biochemistry 2010, 49:924-933.
28. Grela P., Sawa-Makarska J., Gordiyenko Y., Robinson C.V., Grankowski N., Tchórzewski M. Structural properties of the human acidic ribosomal P proteins forming the P1-P2 heterocomplex. J. Biol. Chem. 2008, 143:169-177.
29. Guerra S., López-Fernández L.A., García M.A., Zaballos A., Esteban M. Human gene profiling in response to the active protein kinase, interferon-induced serine/threonine protein kinase (PKR), in infected cells. Involvement of the transcription factor ATF-3 IN PKR-induced apoptosis. J. Biol. Chem. 2006, 281:18734-18745.
30. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 2000, 6:1099-1108.
31. Hazes B., Read R.J. Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry 1997, 36:11051-11054.
32. Hedblom M.L., Cawley D.B., Boguslawski S., Houston L.L. Binding of ricin A chain to rat liver ribosomes: relationship to ribosome inactivation. J. Supramol. Struct. 1978, 9:253-268.
33. Honjo E., Watanabe K., Tsukamoto T. Real-time kinetic analyses of the interaction of ricin toxin A-chain with ribosomes prove a conformational change involved in complex formation. J. Biochem. 2002, 131:267-275.
34. Hudak K.A., Parikh B.A., Di R., Baricevic M., Santana M., Seskar M., Tumer N.E. Generation of pokeweed antiviral protein mutations in Saccharomyces cerevisiae: evidence that ribosome depurination is not sufficient for cytotoxicity. Nucleic Acids Res. 2004, 32:4244-4256.
35. Iordanov M.S., Pribnow D., Magun J.L., Dinh T.H., Pearson J.A., Chen S.L., Magun B.E. Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ricin loop in the 28S rRNA. Mol. Cell. Biol. 1997, 17:3373-3381.
36. Jandhyala D.M., Thorpe C.M., Magun B. Ricin and Shiga toxins: effects on host cell signal transduction. Curr. Top. Microbiol. Immunol. 2012, 357:41-65.
37. Jetzt A.E., Cheng J.-S., Li X.-P., Tumer N.E., Cohick W.S. A relatively low level of ribosome depurination by mutant forms of ricin toxin A chain can trigger protein synthesis inhibition, cell signaling and apoptosis in mammalian cells. Int. J. Biochem. Cell. Biol. 2012, 44:2204-2211.
38. Krokowski D., Tchórzewski M., Boguszewska A., McKay A.R., Maslen S.L., Robinson C.V., Grankowski N. Elevated copy number of L-A virus in yeast mutant strains defective in ribosomal stalk. Biochem. Biophys. Res. Commun. 2007, 355:575-580.
39. Kumar K.U., Srivastava S.P., Kaufman R.J. Double-stranded RNA-activated protein kinase (PKR) is negatively regulated by 60S ribosomal subunit protein L18. Mol. Cell. Biol. 1999, 19:1116-1125.
40. Lapadula W.J., Sanchez-Puerta M.V., Juri Ayub M. Convergent evolution led ribosome inactivating proteins to interact with ribosomal stalk. Toxicon 2012, 59:427-432.
41. Lee K.-M., Yu C.W.-H., Chiu T.Y.-H., Sze K.H., Shaw P.-C., Wong K.-B. Solution structure of the dimerization domain of the eukaryotic stalk P1/P2 complex reveals the structural organization of eukaryotic stalk complex. Nucleic Acids Res. 2012, 40:3172-3182.
42. Li X.-P., Baricevic M., Saidasan H., Tumer N.E. Ribosome depurination is not sufficient for ricin-mediated cell death in Saccharomyces cerevisiae. Infect. Immun. 2007, 75:417-428.
43. Li X.-P., Chiou J.-C., Remacha M., Ballesta J.P.G., Tumer N.E. A two-step binding model proposed for the electrostatic interactions of ricin a chain with ribosomes. Biochemistry 2009, 48:3853-3863.
44. Li X.-P., Grela P., Krokowski D., Tchórzewski M., Tumer N.E. Pentameric organization of the ribosomal stalk accelerates recruitment of ricin a chain to the ribosome for depurination. J. Biol. Chem. 2010, 285:41463-41471.
45. Lin A. Activation of the JNK signaling pathway: breaking the brake on apoptosis. Bioessays 2002, 25:17-24.
46. Lindauer M., Wong J., Magun B. Ricin toxin activates the NALP3 inflammasome. Toxins (Basel) 2010, 2:1500-1514.
47. Lord J.M. Precursors of ricin and Ricinus communis agglutinin. Glycosylation and processing during synthesis and intracellular transport. Eur. J. Biochem. 1985, 146:411-416.
48. Lord J.M., Roberts L.M. Toxin entry: retrograde transport through the secretory pathway. J. Cell. Biol. 1998, 140:733-736.
49. Lord J.M., Roberts L.M., Robertus J.D. Ricin: structure, mode of action, and some current applications. FASEB J. 1994, 8:201-208.
50. Mandal S., Li W.T., Bai Y., Robertus J.D., Kerwin S.M. Synthesis of 2-substituted 9-oxa-guanines {5-aminooxazolo[5,4-d]pyrimidin-7(6H)-ones} and 9-oxa-2-thio-xanthines {5-mercaptooxazolo[5,4-d]pyrimidin-7(6H)-ones}. Beilstein J. Org. Chem. 2008, 4:26.
51. May K.L., Li X.P., Azorín F.M., Ballesta J., Grela P., Tchórzewski M., Tumer N.E. The P1/P2 proteins of the human ribosomal stalk are required for ribosome binding and depurination by ricin in human cells. FEBS J. 2012, 279:3925-3936.
52. McCluskey A.J., Bolewska-Pedyczak E., Jarvik N., Chen G., Sidhu S.S., Gariépy J. Charged and hydrophobic surfaces on the A chain of shiga-like toxin 1 recognize the C-terminal domain of ribosomal stalk proteins. PLoS ONE 2012, 7:e31191.
53. McCluskey A.J., Poon G.M.K., Bolewska-Pedyczak E., Srikumar T., Jeram S.M., Raught B., Gariépy J. The catalytic subunit of shiga-like toxin 1 interacts with ribosomal stalk proteins and is inhibited by their conserved C-terminal domain. J. Mol. Biol. 2008, 378:375-386.
54. Miller D.J., Ravikumar K., Shen H., Suh J.-K., Kerwin S.M., Robertus J.D. Structure-based design and characterization of novel platforms for ricin and shiga toxin inhibition. J. Med. Chem. 2002, 45:90-98.
55. Mohr D., Wintermeyer W., Rodnina M.V. GTPase activation of elongation factors Tu and G on the ribosome. Biochemistry 2002, 41:12520-12528.
56. Mukhopadhyay S., Linstedt A.D. Manganese blocks intracellular trafficking of Shiga toxin and protects against Shiga toxicosis. Science 2012, 335:332-335.
57. Musshoff F., Madea B. Ricin poisoning and forensic toxicology. Drug Test. Anal. 2009, 1:184-191.
58. Mutlu H., Meier M.A.R. Castor oil as a renewable resource for the chemical industry. Eur. J. Lipid Sci. Technol. 2010, 112:10-30.
59. Olsnes S. The history of ricin, abrin and related toxins. Toxicon 2004, 44:361-370.
60. Olsnes S., Pihl A. Treatment of abrin and ricin with -mercaptoethanol opposite effects on their toxicity in mice and their ability to inhibit protein synthesis in a cell-free system. FEBS Lett. 1972, 28:48-50.
61. Olsnes S., Pihl A. Different biological properties of the two constituent peptide chains of ricin, a toxic protein inhibiting protein synthesis. Biochemistry 1973, 12:3121-3126.
62. Pang Y.-P., Park J.G., Wang S., Vummenthala A., Mishra R.K., McLaughlin J.E., Di R., Kahn J.N., Tumer N.E., Janosi L., Davis J., Millard C.B. Small-molecule inhibitor leads of ribosome-inactivating proteins developed using the doorstop approach. PLoS ONE 2011, 6:e17883.
63. Parikh B.A., Tortora A., Li X.-P., Tumer N.E. Ricin inhibits activation of the unfolded protein response by preventing splicing of the HAC1 mRNA. J. Biol. Chem. 2008, 283:6145-6153.
64. Park J.G., Kahn J.N., Tumer N.E., Pang Y.-P. Chemical structure of Retro-2, a compound that protects cells against ribosome-inactivating proteins. Sci. Rep. 2012, 2:631.
65. Paton A.W., Morona R., Paton J.C. A new biological agent for treatment of Shiga toxigenic Escherichia coli infections and dysentery in humans. Nat. Med. 2000, 6:265-270.
66. Paton A.W., Morona R., Paton J.C. Neutralization of Shiga toxins Stx1, Stx2c, and Stx2e by recombinant bacteria expressing mimics of globotriose and globotetraose. Infect. Immun. 2001, 69:1967-1970.
67. Paton J.C., Paton A.W. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin. Microbiol. Rev. 1998, 11:450-479.
68. Pruet J.M., Jasheway K.R., Manzano L.A., Bai Y., Anslyn E.V., Robertus J.D. 7-Substituted pterins provide a new direction for ricin A chain inhibitors. Eur. J. Med. Chem. 2011, 46:3608-3615.
69. Ptitsyn O.B. Molten globule and protein folding. Adv. Protein Chem. 1995, 47:83-229.
70. Qiu D., Parada P., Marcos A.G., Cárdenas D., Remacha M., Ballesta J.P.G. Different roles of P1 and P2 Saccharomyces cerevisiae ribosomal stalk proteins revealed by cross-linking. Mol. Microbiol. 2006, 62:1191-1202.
71. Rapak A., Falnes P.O., Olsnes S. Retrograde transport of mutant ricin to the endoplasmic reticulum with subsequent translocation to cytosol. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:3783-3788.
72. Rasooly R., He X., Friedman M. Milk inhibits the biological activity of ricin. J. Biol. Chem. 2012, 287:27924-27929.
73. Rutenber E., Katzin B.J., Ernst S., Collins E.J., Mlsna D., Ready M.P., Robertus J.D. Crystallographic refinement of ricin to 2.5 A. Proteins 1991, 10:240-250.
74. Saenz J.B., Doggett T.A., Haslam D.B. Identification and characterization of small molecules that inhibit intracellular toxin transport. Infect. Immun. 2007, 75:4552-4561.
75. Saenz-Robles M.T., Remacha M., Vilella M.D., Zinker S., Ballesta J.P. The acidic ribosomal proteins as regulators of the eukaryotic ribosomal activity. Biochim. Biophys. Acta 1990, 1050:51-55.
76. Sandvig K., Bergan J., Dyve A.-B., Skotland T., Torgersen M.L. Endocytosis and retrograde transport of Shiga toxin. Toxicon 2010, 56:1181-1185.
77. Schlossman D., Withers D., Welsh P., Alexander A., Robertus J., Frankel A. Role of glutamic acid 177 of the ricin toxin A chain in enzymatic inactivation of ribosomes. Mol. Cell. Biol. 1989, 9:5012-5021.
78. Shi X., Khade P.K., Sanbonmatsu K.Y., Joseph S. Functional role of the sarcin-ricin loop of the 23S rRNA in the elongation cycle of protein synthesis. J. Mol. Biol. 2012, 419:125-138.
79. Simpson J.C., Roberts L.M., Römisch K., Davey J., Wolf D.H., Lord J.M. Ricin A chain utilizes the endoplasmic reticulum-associated protein degradation pathway to enter the cytosol of yeast. FEBS Lett. 1999, 459:80-84.
80. Skinner L., Jackson M. Inhibition of prokaryotic translation by the Shiga toxin enzymatic subunit. Microb. Pathog. 1998, 24:117-122.
81. Sokołowska I., Wälchli S., Wegrzyn G., Sandvig K., Słomińska-Wojewódzka M. A single point mutation in ricin A-chain increases toxin degradation and inhibits EDEM1-dependent ER retrotranslocation. Biochem. J. 2011, 436:371-385.
82. Spooner R.A., Lord J.M. How ricin and shiga toxin reach the cytosol of target cells: retrotranslocation from the endoplasmic reticulum. Curr. Top. Microbiol. Immunol. 2012, 357:19-40.
83. Spooner R.A., Watson P.D., Marsden C.J., Smith D.C., Moore K.A.H., Cook J.P., Lord J.M., Roberts L.M. Protein disulphide-isomerase reduces ricin to its A and B chains in the endoplasmic reticulum. Biochem. J. 2004, 383:285-293.
84. Stechmann B., Bai S.-K., Gobbo E., Lopez R., Merer G., Pinchard S., Panigai L., Tenza D., Raposo G., Beaumelle B., Sauvaire D., Gillet D., Johannes L., Barbier J. Inhibition of retrograde transport protects mice from lethal ricin challenge. Cell 2010, 141:231-242.
85. Stolz A., Wolf D.H. Endoplasmic reticulum associated protein degradation: a chaperone assisted journey to hell. Biochim. Biophys. Acta (BBA) - Mol. Cell Res. 2010, 1803:694-705.
86. Suh J.-K., Hovde C.J., Robertus J.D. Shiga toxin attacks bacterial ribosomes as effectively as eukaryotic ribosomes. Biochemistry 1998, 37:9394-9398.
87. Tchórzewski M. The acidic ribosomal P proteins. Int. J. Biochem. Cell. Biol. 2002, 34:911-915.
88. Tesh V.L. Activation of cell stress response pathways by Shiga toxins. Cell. Microbiol. 2012, 14:1-9.
89. Too P.H.-M., Ma M.K.-W., Mak A.N.-S., Wong Y.-T., Tung C.K.-C., Zhu G., Au S.W.-N., Wong K.-B., Shaw P.-C. The C-terminal fragment of the ribosomal P protein complexed to trichosanthin reveals the interaction between the ribosome-inactivating protein and the ribosome. Nucleic Acids Res. 2009, 37:602-610.
90. Tsurugi K., Ogata K. Evidence for the exchangeability of acidic ribosomal proteins on cytoplasmic ribosomes in regenerating rat liver. J. Biochem. 1985, 98:1427-1431.
91. Uesono Y. Transient inhibition of translation initiation by osmotic stress. J. Biol. Chem. 2002, 277:13848-13855.
92. van der Goot F.G., Lakey J.H., Pattus F. The molten globule intermediate for protein insertion or translocation through membranes. Trends Cell. Biol. 1992, 2:343-348.
93. Vater C.A., Bartle L.M., Leszyk J.D., Lambert J.M., Goldmacher V.S. Ricin A chain can be chemically cross-linked to the mammalian ribosomal proteins L9 and L10e. J. Biol. Chem. 1995, 270:12933-12940.
94. Voorhees R.M., Schmeing T.M., Kelley A.C., Ramakrishnan V. The mechanism for activation of GTP hydrolysis on the ribosome. Science 2010, 330:835-838.
95. Wahl M.C., Möller W. Structure and function of the acidic ribosomal stalk proteins. Curr. Protein Pept. Sci. 2002, 3:93-106.
96. Wahome P.G., Ahlawat S., Mantis N.J. Identification of small molecules that suppress ricin-induced stress-activated signaling pathways. PLoS ONE 2012, 7:e49075.
97. Wahome P.G., Robertus J.D., Mantis N.J. Small-molecule inhibitors of ricin and shiga toxins. Curr. Top. Microbiol. Immunol. 2011, 357:179-207.
98. Wang C.-T., Jetzt A.E., Cheng J.-S., Cohick W.S. Inhibition of the unfolded protein response by ricin A-chain enhances its cytotoxicity in mammalian cells. Toxins (Basel) 2011, 3:453-468.
99. Williams B.R. Signal integration via PKR. Sci. STKE 2001, 2001:re2.
100. Yan Q., Li X.-P., Tumer N.E. N-glycosylation does not affect the catalytic activity of ricin A chain but stimulates cytotoxicity by promoting its transport out of the endoplasmic reticulum. Traffic 2012, 13:1508-1521.
101. Yan X., Hollis T., Svinth M., Day P., Monzingo A.F., Milne G.W., Robertus J.D. Structure-based identification of a ricin inhibitor. J. Mol. Biol. 1997, 266:1043-1049.
102. Yermakova A., Mantis N.J. Protective immunity to ricin toxin conferred by antibodies against the toxin's binding subunit (RTB). Vaccine 2011, 29:7925-7935.
103. Yermakova A., Vance D.J., Mantis N.J. Sub-domains of Ricin's B subunit as targets of toxin neutralizing and non-neutralizing monoclonal antibodies. PLoS ONE 2012, 7:e44317.
104. Yoshida T., Chen C.C., Zhang M.S., Wu H.C. Disruption of the Golgi apparatus by brefeldin A inhibits the cytotoxicity of ricin, modeccin, and Pseudomonas toxin. Exp. Cell. Res. 1991, 192:389-395.
105. Zhu S., Romano P.R., Wek R.C. Ribosome targeting of PKR is mediated by two double-stranded RNA-binding domains and facilitates in vivo phosphorylation of eukaryotic initiation factor-2. J. Biol. Chem. 1997, 272:14434-14441.
106. Zinker S., Warner J.R. The ribosomal proteins of Saccharomyces cerevisiae. Phosphorylated and exchangeable proteins. J. Biol. Chem. 1976, 251:1799-1807.