Immunity to ricin: Fundamental insights into toxin-antibody interactions

Current Topics in Microbiology and Immunology

Volumn 357, Issue , 2012, Pages 209-241

  O'Hara, Joanne M ^a,b   Yermakova, Anastasiya ^a,b   Mantis, Nicholas J ^a  

^a WADSWORTH CENTER   (United States)

^b UNIVERSITY AT ALBANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; BOTULINUM TOXIN; EPITOPE; IMMUNOTOXIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 24B11; MONOCLONAL ANTIBODY 3B12; MONOCLONAL ANTIBODY BD7; MONOCLONAL ANTIBODY CB12; MONOCLONAL ANTIBODY FGA12; MONOCLONAL ANTIBODY GD12; MONOCLONAL ANTIBODY JB11; MONOCLONAL ANTIBODY JB4; MONOCLONAL ANTIBODY PB10; MONOCLONAL ANTIBODY R70; MONOCLONAL ANTIBODY RAC 23; MONOCLONAL ANTIBODY RAC18; MONOCLONAL ANTIBODY RB34; MONOCLONAL ANTIBODY RB37; MONOCLONAL ANTIBODY SA3; MONOCLONAL ANTIBODY SB1; MONOCLONAL ANTIBODY SY1H3; MONOCLONAL ANTIBODY SYH7; MONOCLONAL ANTIBODY TFTB 1; RICIN; RICIN ANTIBODY; RICIN TOXIN A; RICIN TOXIN B; UNCLASSIFIED DRUG;

ANTIBODY RESPONSE; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE; CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; HODGKIN DISEASE; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNIZATION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; TREATMENT RESPONSE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; EPITOPES, B-LYMPHOCYTE; HUMANS; IMMUNITY, MUCOSAL; PROTEIN BINDING; RICIN;

EID: 84857812737     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/82_2011_193     Document Type: Article

References (142)

1. Abboud N, Chow SK, Saylor C, Janda A, Ravetch JV, Scharff MD, Casadevall A (2010) A requirement for FcgammaR in antibody-mediated bacterial toxin neutralization. J Exp Med 207:2395-2405. doi:jem.20100995[pii]10.1084/jem. 20100995
2. Abboud N, De Jesus M, Nakouzi A, Cordero RJ, Pujato M, Fiser A, Rivera J, Casadevall A (2009) Identification of linear epitopes in Bacillus anthracis protective antigen bound by neutralizing antibodies. J Biol Chem 284:25077-25086. doi:M109.022061[pii]10.1074/jbc.M109.022061
3. Argent RH, Parrott AM, Day PJ, Roberts LM, Stockley PG, Lord JM, Radford SE (2000) Ribosome-mediated folding of partially unfolded ricin A-chain. J Biol Chem 275:9263-9269 (Pubitemid 30185146)
4. Baenziger JU, Fiete D (1979) Structural determinants of Ricinus communis agglutinin and toxin specificity for oligosaccharides. J Biol Chem 254:9795-9799
5. Barlow DJ, Edwards MS, Thornton JM (1986) Continuous and discontinuous protein antigenic determinants. Nature 322:747-748. doi:10.1038/322747a0 (Pubitemid 16074126)
6. Benson JM, Gomez AP, Wolf ML, Tibbetts BM, March TH (2011) The acute toxicity, tissue distribution, and histopathology of inhaled ricin in Sprague Dawley rats and BALB/c mice. Inhal Toxicol 23:247-256. doi:10.3109/08958378. 2011.565490
7. Brey RN, Mantis NJ (2009) Vaccines for ricin-a type II ribosome inactivating protein. In: Barrett ADT, Stanberry LR (eds) Vaccines for biodefense and neglected diseases. Elsevier Inc, New York
8. Brissette R, Goldstein NI (2007) The use of phage display peptide libraries for basic and translational research. Methods Mol Biol 383:203-213
9. Brown RF, White DE (1997) Ultrastructure of rat lung following inhalation of ricin aerosol. Int J Exp Path 78:267-276 (Pubitemid 27408022)
10. Cao L, Volgina A, Korostoff J, DiRienzo JM (2006) Role of intrachain disulfides in the activities of the CdtA and CdtC subunits of the cytolethal distending toxin of Actinobacillus actinomycetemcomitans. Infect Immun 74:4990-5002. doi:74/9/4990[pii]10.1128/IAI.00697-06 (Pubitemid 44300417)
11. Carra JH, McHugh CA, Mulligan S, Machiesky LM, Soares AS, Millard CB (2007a) Fragmentbased identification of determinants of conformational and spectroscopic change at the ricin active site. BMC Struct Biol 7:72. doi:1472-6807-7-72[pii]10.1186/1472-6807-7-72
12. Carra JH, Wannemacher RW, Tammariello RF, Lindsey CY, Dinterman RE, Schokman RD, Smith LA (2007b) Improved formulation of a recombinant ricin A-chain vaccine increases its stability and effective antigenicity. Vaccine 25:4149-4158 (Pubitemid 46635951)
13. Carter JM, Loomis-Price L (2004) B cell epitope mapping using synthetic peptides. Curr Protoc Immunol Chapter 9: Unit 9.4
14. Castelletti D, Fracasso G, Righetti S, Tridente G, Schnell R, Engert A, Colombatti M (2004) A dominant linear B-cell epitope of ricin A-chain is the target of a neutralizing antibody response in Hodgkin's lymphoma patients treated with an anti-CD25 immunotoxin. Clin Exp Immunol 136:365-372 (Pubitemid 38543458)
15. Chaddock JA, Monzingo AF, Robertus JD, Lord JM, Roberts LM (1996) Major structural differences between pokeweed antiviral protein and ricin A-chain do not account for their differing ribosome specificity. Eur J Biochem 235:159-166 (Pubitemid 26045429)
16. Chanh TC, Hewetson JF (1995) Protection against ricin intoxication in vivo by anti-idiotype vaccination. Vaccine 13:479-485
17. Chanh TC, Romanowski MJ, Hewetson JF (1993) Monoclonal antibody prophylaxis against the in vivo toxicity of ricin in mice. Immunol Invest 22:63-72 (Pubitemid 23056267)
18. Colombatti M, Johnson VG, Skopicki HA, Fendley B, Lewis MS, Youle RJ (1987) Identification and characterization of a monoclonal antibody recognizing a galactose-binding domain of the toxin ricin. J Immunol 138:3339-3344 (Pubitemid 17071915)
19. Colombatti M, Pezzini A, Colombatti A (1986) Monoclonal antibodies against ricin: effects on toxin function. Hybridoma 5:9-19 (Pubitemid 16203252)
20. Compton JR, Legler PM, Clingan BV, Olson MA, Millard CB (2011) Introduction of a disulfide bond leads to stabilization and crystallization of a ricin immunogen. Proteins 79:1048-1060. doi:10.1002/prot.22933
21. Cummings R, Etzler M (2009) R-type Lectins. In: Varki A, Cummings R, Esko J, Freeze H, Stanley P, Bertozzi C, Hart G, Etzler M (eds) Essentials of glycobiology. Cold Spring Harbor Laboratory Press, Cold Spring Harbor (NY)
22. Dai J, Zhao L, Yang H, Guo H, Fan K, Wang H, Qian W, Zhang D, Li B, Guo Y (2011) Identification of a novel functional domain of ricin responsible for its potent toxicity. J Biol Chem 286:12166-12171. doi:M110.196584[pii]10.1074/jbc. M110.196584
23. DaSilva L, Cote D, Roy C, Martinez M, Duniho S, Pitt ML, Downey T, Dertzbaugh M (2003) Pulmonary gene expression profiling of inhaled ricin. Toxicon 41:813-822 (Pubitemid 36627892)
24. Day PJ, Pinheiro TJ, Roberts LM, Lord JM (2002) Binding of ricin A-chain to negatively charged phospholipid vesicles leads to protein structural changes and destabilizes the lipid bilayer. Biochemistry 41:2836-2843 (Pubitemid 34168953)
25. Dertzbaugh MT, Rossi CA, Paddle BM, Hale M, Poretski M, Alderton MR (2005) Monoclonal antibodies to ricin: in vitro inhibition of toxicity and utility as diagnostic reagents. Hybridoma (Larchmt) 24:236-243 (Pubitemid 41507763)
26. Doebler JA, Wiltshire ND, Mayer TW, Estep JE, Moeller RB, Traub RK, Broomfield CA, Calamaio CA, Thompson WL, Pitt ML (1995) The distribution of [125I]ricin in mice following aerosol inhalation exposure. Toxicology 98:137-149
27. East L, Isacke CM (2002) The mannose receptor family. Biochim Biophys Acta 1572:364-386 (Pubitemid 35246355)
28. Ehrlich P (1957) Experimentelle Untersuchungen uber ImmunitatI. Uber Ricin. The Collected Papers of Paul Ehrlich, vol 2. Pergamaon Press, London
29. Endo Y, Mitsui K, Motizuki M, Tsurugi K (1987) The mechanism of action of ricin and related toxins on eukaryotic ribosomes. J Biol Chem 262:5908-5912
30. Endo Y, Tsurugi K (1987) RNA N-glycosidase activity of ricin A-chain. Mechanism of action of the toxic lectin ricin on eukaryotic ribosomes. J Biol Chem 262:8128-8130 (Pubitemid 17104265)
31. Flexner S (1897) The histological changes produced by ricin and abrin intoxications. J Exp Med 2:197-220
32. Foxwell BM, Detre SI, Donovan TA, Thorpe PE (1985) The use of anti-ricin antibodies to protect mice intoxicated with ricin. Toxicology 34:79-88 (Pubitemid 15160094)
33. Frankel AE, Fu T, Burbage C, Tagge E, Harris B, Vesely J, Willingham MC (1997) Lectin-deficient ricin toxin intoxicates cells bearing the D-mannose receptor. Carbohydr Res 300:251-258 (Pubitemid 27217820)
34. Franz D, Jaax N (1997) Ricin toxin. In: Zajtchuk R BR (ed) Textbook of military medicine pp 631-42
35. Gage E, Hernandez MO, O'Hara JM, McCarthy EA, Mantis NJ (2011) Role of the mannose receptor (CD206) in immunity to ricin. Toxins (Basel) 3(9):1131-1145. doi:10.3390/toxins3091131
36. Godal A, Fodstad O, Pihl A (1983) Antibody formation against the cytotoxic proteins abrin and ricin in humans and mice. Int J Cancer 32:515-521 (Pubitemid 13017970)
37. Griffiths GD, Bailey SC, Hambrook JL, Keyte M, Jayasekera P, Miles J, Williamson E (1997) Liposomally-encapsulated ricin toxoid vaccine delivered intratracheally elicits a good immune response and protects against a lethal pulmonary dose of ricin toxin. Vaccine 15: 1933-1939 (Pubitemid 27504690)
38. Griffiths GD, Bailey SC, Hambrook JL, Keyte MP (1998) Local and systemic responses against ricin toxin promoted by toxoid or peptide vaccines alone or in liposomal formulations. Vaccine 16:530-535 (Pubitemid 28044171)
39. Griffiths GD, Lindsay CD, Allenby AC, Bailey SC, Scawin JW, Rice P, Upshall DG (1995) Protection against inhalation toxicity of ricin and abrin by immunisation. Hum Exp Toxicol 14:155-164
40. Griffiths GD, Phillips GJ, Bailey SC (1999) Comparison of the quality of protection elicited by toxoid and peptide liposomal vaccine formulations against ricin as assessed by markers of inflammation. Vaccine 17:2562-2568 (Pubitemid 29314449)
41. Hazen EL (1927) General and local immunity to ricin. J Immunol 13:171-218
42. Hewetson JF, Rivera VR, Creasia DA, Lemley PV, Rippy MK, Poli MA (1993) Protection of mice from inhaled ricin by vaccination with ricin or by passive treatment with heterologous antibody. Vaccine 11:743-746 (Pubitemid 23190660)
43. Houston LL (1982) Protection of mice from ricin poisoning by treatment with antibodies directed against ricin. J Toxicol-Clin Toxicol 19:385-389 (Pubitemid 13201198)
44. Inoue K, Sobhany M, Transue TR, Oguma K, Pedersen LC, Negishi M (2003) Structural analysis by X-ray crystallography and calorimetry of a haemagglutinin component (HA1) of the progenitor toxin from Clostridium botulinum. Microbiology 149:3361-3370 (Pubitemid 38016665)
45. Ishiguro M, Matori Y, Tanabe S, Kawase Y, Sekine I, Sakakibara R (1992) Biochemical studies on oral toxicity of ricin. V. The role of lectin activity in the intestinal absorption of ricin. Chem Pharm Bull 40:1216-1220
46. Jandhyala DM, Ahluwalia A, Obrig T, Thorpe CM (2008) ZAK: a MAP3Kinase that transduces Shiga toxin-and ricin-induced proinflammatory cytokine expression. Cell Microbiol
47. Katzin BJ, Collins EJ, Robertus JD (1991) Structure of ricin A-chain at 2.5 A. Proteins 10:251-259
48. Kelly-Cirino CD, Mantis NJ (2009) Neutralizing monoclonal antibodies directed against defined linear epitopes on domain 4 of anthrax protective antigen. Infect Immun 77:4859-4867. doi:IAI.00117-09[pii]10.1128/IAI.00117-09
49. Krautz-Peterson G, Chapman-Bonofiglio S, Boisvert K, Feng H, Herman IM, Tzipori S, Sheoran AS (2008) Intracellular neutralization of shiga toxin 2 by an a subunit-specific human monoclonal antibody. Infect Immun 76:1931-1939 (Pubitemid 351656126)
50. Lara-Tejero M, Galan JE (2001) CdtA, CdtB, and CdtC form a tripartite complex that is required for cytolethal distending toxin activity. Infect Immun 69:4358-4365. doi:10.1128/IAI.69. 7.4358-4365.2001 (Pubitemid 32574433)
51. Largent BL, Walton KM, Hoppe CA, Lee YC, Schnaar RL (1984) Carbohydrate-specific adhesion of alveolar macrophages to mannose-derivatized surfaces. J Biol Chem 259: 1764-1769 (Pubitemid 14146564)
52. Lebeda FJ, Olson MA (1999) Prediction of a conserved, neutralizing epitope in ribosomeinactivating proteins. Int J Biol Macromol 24:19-26 (Pubitemid 29038098)
53. Leek MD, Griffiths GD, Green MA (1989) Intestinal pathology following intramuscular ricin poisoning. J Pathol 159:329-334 (Pubitemid 20011395)
54. Lemley PV, Amanatides P, Wright DC (1994) Identification and characterization of a monoclonal antibody that neutralizes ricin toxicity in vitro and in vivo. Hybridoma 13:417-421 (Pubitemid 24351544)
55. Lemley PV, Wright DC (1992) Mice are actively immunized after passive monoclonal antibody prophylaxis and ricin toxin challenge. Immunology 76:511-513
56. Lewis MS, Youle RJ (1986) Ricin subunit association. Thermodynamics and the role of the disulfide bond in toxicity. J Biol Chem 261:11571-11577 (Pubitemid 17206074)
57. Leysath CE, Monzingo AF, Maynard JA, Barnett J, Georgiou G, Iverson BL, Robertus JD (2009) Crystal structure of the engineered neutralizing antibody M18 complexed to domain 4 of the anthrax protective antigen. J Mol Biol 387:680-693. doi:S0022-2836(09)00146-6[pii]10.1016/j.jmb.2009.02.003
58. Li XP, Chiou JC, Remacha M, Ballesta JP, Tumer NE (2009) A two-step binding model proposed for the electrostatic interactions of ricin a chain with ribosomes. Biochemistry 48:3853-3863
59. Lindauer ML, Wong J, Iwakura Y, Magun BE (2009) Pulmonary inflammation triggered by ricin toxin requires macrophages and IL-1 signaling. J Immunol 183:1419-1426
60. Lord JM, Roberts LM, Robertus JD (1994) Ricin: structure, mode of action, and some current applications. Faseb J 8:201-208 (Pubitemid 24067143)
61. Maddaloni M, Cooke C, Wilkinson R, Stout AV, Eng L, Pincus SH (2004) Immunological characteristics associated with the protective efficacy of antibodies to ricin. J Immunol 172: 6221-6228 (Pubitemid 38621228)
62. Magnusson S, Berg T (1993) Endocytosis of ricin by rat liver cells in vivo and in vitro is mainly mediated by mannose receptors on sinusoidal endothelial cells. Biochem J 291(Pt 3):749-755 (Pubitemid 23148448)
63. Magnusson S, Berg T, Turpin E, Frenoy JP (1991) Interactions of ricin with sinusoidal endothelial rat liver cells. Different involvement of two distinct carbohydrate-specific mechanisms in surface binding and internalization. Biochem J 277(Pt 3):855-861
64. Magnusson S, Kjeken R, Berg T (1993) Characterization of two distinct pathways of endocytosis of ricin by rat liver endothelial cells. Exp Cell Res 205:118-125 (Pubitemid 23192110)
65. Mantis NJ, McGuinness CR, Sonuyi O, Edwards G, Farrant SA (2006) Immunoglobulin A antibodies against ricin A and B subunits protect epithelial cells from ricin intoxication. Infect Immun 74:3455-3462. doi:74/6/3455[pii]10. 1128/IAI.02088-05 (Pubitemid 43794535)
66. Mantis NJ, Morici LA, Roy CJ (2011) Mucosal vaccines for biodefense. Curr Top Microbiol Immunol. doi:10.1007/82-2011-122
67. Marconescu PS, Smallshaw JE, Pop LM, Ruback SL, Vitetta ES (2010) Intradermal administration of RiVax protects mice from mucosal and systemic ricin intoxication. Vaccine 28:5315-5322
68. Mayerhofer PU, Cook JP, Wahlman J, Pinheiro TT, Moore KA, Lord JM, Johnson AE, Roberts LM (2009) Ricin A chain insertion into endoplasmic reticulum membranes is triggered by a temperature increase to 37 {degrees}C. J Biol Chem 284:10232-10242. doi:M808387200 [pii]10.1074/jbc.M808387200
69. McGuinness CR, Mantis NJ (2006) Characterization of a novel high-affinity monoclonal immunoglobulin G antibody against the ricin B subunit. Infect Immun 74:3463-3470. doi:74/6/3463[pii]10.1128/IAI.00324-06 (Pubitemid 43794536)
70. McHugh CA, Tammariello RF, Millard CB, Carra JH (2004) Improved stability of a protein vaccine through elimination of a partially unfolded state. Protein Sci 13:2736-2743. doi:10.1110/ps.04897904ps.04897904[pii] (Pubitemid 39274641)
71. McLain DE, Horn TL, Detrisac CJ, Lindsey CY, Smith LA (2011a) Progress in biological threat agent vaccine development: A repeat-dose toxicity study of a recombinant ricin toxin a-chain (rRTA) 1-33/44-198Vaccine (RVEc) in male and female new zealand white rabbits. Int J Toxicol. doi:1091581810396730 [pii]10.1177/1091581810396730
72. McLain DE, Lewis BS, Chapman JL, Wannemacher RW, Lindsey CY, Smith LA (2011b) Protective effect of two recombinant ricin subunit vaccines in the New Zealand white rabbit subjected to a lethal aerosolized ricin challenge: survival, immunological response and histopathological findings. Toxicol Sci. doi:kfr274 [pii]10.1093/toxsci/kfr274
73. Montfort W, Villafranca JE, Monzingo AF, Ernst SR, Katzin B, Rutenber E, Xuong NH, Hamlin R, Robertus JD (1987) The three-dimensional structure of ricin at 2.8 A. J Biol Chem 262:5398-5403
74. Monzingo AF, Robertus JD (1992) X-ray analysis of substrate analogs in the ricin A-chain active site. J Mol Biol 227:1136-1145
75. Mullaney BP, Pallavicini MG, Marks JD (2001) Epitope mapping of neutralizing botulinum neurotoxin A antibodies by phage display. Infect Immun 69:6511-6514 (Pubitemid 32885217)
76. Neal LM, McCarthy EA, Morris CR, Mantis NJ (2011) Vaccine-induced intestinal immunity to ricin toxin in the absence of secretory IgA. Vaccine 29:681-689. doi:S0264-410X(10)01639-7[pii]10.1016/j.vaccine.2010.11.030
77. Neal LM, O'Hara J, Brey RN 3rd, Mantis NJ (2010) A monoclonal immunoglobulin G antibody directed against an immunodominant linear epitope on the ricin A chain confers systemic and mucosal immunity to ricin. Infect Immun 78:552-561. doi:IAI.00796-09[pii]10.1128/IAI. 00796-09
78. Nesic D, Hsu Y, Stebbins CE (2004) Assembly and function of a bacterial genotoxin. Nature 429:429-433 (Pubitemid 38715135)
79. Nesic D, Stebbins CE (2005) Mechanisms of assembly and cellular interactions for the bacterial genotoxin CDT. PLoS Pathog 1:e28. doi:10.1371/journal.ppat.0010028
80. Newton DL, Wales R, Richardson PT, Walbridge S, Saxena SK, Ackerman EJ, Roberts LM, Lord JM, Youle RJ (1992) Cell surface and intracellular functions for ricin galactose binding. J Biol Chem 267:11917-11922
81. Nguyen ML, Crowe SR, Kurella S, Teryzan S, Cao B, Ballard JD, James JA, Farris AD (2009a) Sequential B-cell epitopes of Bacillus anthracis lethal factor bind lethal toxin-neutralizing antibodies. Infect Immun 77:162-169. doi:IAI.00788-08[pii]10.1128/IAI.00788-08
82. Nguyen ML, Terzyan S, Ballard JD, James JA, Farris AD (2009b) The major neutralizing antibody responses to recombinant anthrax lethal and edema factors are directed to non-crossreactive epitopes. Infect Immun 77:4714-4723
83. Nowakowski A, Wang C, Powers DB, Amersdorfer P, Smith TJ, Montgomery VA, Sheridan R, Blake R, Smith LA, Marks JD (2002) Potent neutralization of botulinum neurotoxin by recombinant oligoclonal antibody. Proc Natl Acad Sci USA 99:11346-11350 (Pubitemid 34920928)
84. O'Hara JM, Neal LM, McCarthy EA, Kasten-Jolly JA, Brey RN, 3rd, Mantis NJ (2010) Folding domains within the ricin toxin A subunit as targets of protective antibodies. Vaccine. doi: S0264-410X(10)01129-1[pii]10.1016/j. vaccine.2010.08.020
85. Olsnes S (2004) The history of ricin, abrin and related toxins. Toxicon 44:361-370 (Pubitemid 39070638)
86. Olsnes S, Pappenheimer AM Jr, Meren R (1974) Lectins from Abrus precatorius and Ricinus communis II. Hybrid toxins and their interaction with chain-specific antibodies. J Immunol 113:842-847
87. Olsnes S, Saltvedt E (1975) Conformation-dependent antigenic determinants in the toxic lectin ricin. J Immunol 114:1743-1748
88. Olson MA, Carra JH, Roxas-Duncan V, Wannemacher RW, Smith LA, Millard CB (2004) Finding a new vaccine in the ricin protein fold. Protein Eng Des Sel 17:391-397 (Pubitemid 39093520)
89. Pelat T, Hust M, Hale M, Lefranc MP, Dubel S, Thullier P (2009) Isolation of a human-like antibody fragment (scFv) that neutralizes ricin biological activity. BMC Biotechnol 9:60
90. Pimm MV, Gunn B, Lord JM, Baldwin RW (1990) The influence of anti-(ricin toxin A chain) monoclonal antibodies on the pharmacokinetics of ricin toxin A chain and recombinant ricin A chain in mice. Cancer Immunol Immunother 32:235-240
91. Poli MA, Rivera VR, Pitt ML, Vogel P (1996) Aerosolized specific antibody protects mice from lung injury associated with aerosolized ricin exposure. Toxicon 34:1037-1044 (Pubitemid 26320013)
92. Prigent J, Panigai L, Lamourette P, Sauvaire D, Devilliers K, Plaisance M, Volland H, Creminon C, Simon S (2011) Neutralising antibodies against ricin toxin. PLoS One 6:e20166. doi:10.1371/journal.pone.0020166PONE-D-11-01765[pii]
93. Rapak A, Falnes PO, Olsnes S (1997) Retrograde transport of mutant ricin to the endoplasmic reticulum with subsequent translocation to cytosol. Proc Natl Acad Sci USA 94:3783-3788 (Pubitemid 27180450)
94. Ready MP, Kim Y, Robertus JD (1991) Site-directed mutagenesis of ricin A-chain and implications for the mechanism of action. Proteins 10:270-278
95. Roche JK, Stone MK, Gross LK, Lindner M, Seaner R, Pincus SH, Obrig TG (2008) Postexposure targeting of specific epitopes on ricin toxin abrogates toxin-induced hypoglycemia, hepatic injury, and lethality in a mouse model. Lab Invest 88:1178-1191
96. Roy CJ, Hale M, Hartings JM, Pitt L, Duniho S (2003) Impact of inhalation exposure modality and particle size on the respiratory deposition of ricin in BALB/c mice. Inhalation Toxicol 15:619-638 (Pubitemid 36648207)
97. Roy CJ, Song K, Sivasubramani SK, Gardner DJ, Pincus SH (2011) Animal models of ricin toxicosis. Curr Top Microbiol Immunol. doi: 10.1007/82-2011-173
98. Rutenber E, Katzin BJ, Ernst S, Collins EJ, Mlsna D, Ready MP, Robertus JD (1991) Crystallographic refinement of ricin to 2.5 A. Proteins 10:240-250
99. Rutenber E, Ready M, Robertus JD (1987) Structure and evolution of ricin B chain. Nature 326:624-626 (Pubitemid 17051336)
100. Rutenber E, Robertus JD (1991) Structure of ricin B-chain at 2.5 A resolution. Proteins 10: 260-269
101. Sandvig K, Olsnes S, Pihl A (1976) Kinetics of binding of the toxic lectins abrin and ricin to surface receptors of human cells. J Biol Chem 251:3977-3984
102. Sandvig K, Torgersen ML, Engedal N, Skotland T, Iversen TG (2010) Protein toxins from plants and bacteria: probes for intracellular transport and tools in medicine. FEBS Lett 584:2626-2634. doi:S0014-5793(10)00277-2[pii]10.1016/j. febslet.2010.04.008
103. Sandvig K, van Deurs B (2005) Delivery into cells: lessons learned from plant and bacterial toxins. Gene Ther 12:865-872 (Pubitemid 40852204)
104. Scotcher MC, Johnson EA, Stanker LH (2009a) Characterization of the epitope region of F1-2 and F1-5, two monoclonal antibodies to Botulinum neurotoxin type A. Hybridoma (Larchmt) 28:315-325. doi:10.1089/hyb.2009.0022
105. Scotcher MC, McGarvey JA, Johnson EA, Stanker LH (2009b) Epitope characterization and variable region sequence of f1-40, a high-affinity monoclonal antibody to botulinum neurotoxin type a (Hall strain). PLoS One 4:e4924. doi:10.1371/journal.pone.0004924
106. Sekine I, Kawase Y, Nishimori I, Mitarai M, Harada H, Ishiguro M, Kikutani M (1986) Pathological study on mucosal changes in small intestine of rat by oral administration of ricin. I Microscopical observation. Acta Pathologica Japonica 36:1205-1212 (Pubitemid 17173750)
107. Sepulveda J, Mukherjee J, Tzipori S, Simpson LL, Shoemaker CB (2009) Efficient serum clearance of botulinum neurotoxin using a pool of small antitoxin binding agents. Infect Immun
108. Shepherd VL, Lee YC, Schlesinger PH, Stahl PD (1981) L-Fucose-terminated glycoconjugates are recognized by pinocytosis receptors on macrophages. Proc Natl Acad Sci USA 78: 1019-1022 (Pubitemid 11100761)
109. Silverstein A (2002) Paul Ehrlich's receptor immunology : the magnificent obsession. Academic Press, San Diego
110. Simeral LS, Kapmeyer W, MacConnell WP, Kaplan NO (1980) On the role of the covalent carbohydrate in the action of ricin. J Biol Chem 255:11098-11101 (Pubitemid 11134225)
111. Simmons BM, Stahl PD, Russell JH (1986) Mannose receptor-mediated uptake of ricin toxin and ricin A chain by macrophages. Multiple intracellular pathways for a chain translocation. J Biol Chem 261:7912-7920 (Pubitemid 17208723)
112. Skanland SS, Walchli S, Utskarpen A, Wandinger-Ness A, Sandvig K (2007) Phosphoinositideregulated retrograde transport of ricin: crosstalk between hVps34 and sorting nexins. Traffic 8:297-309 (Pubitemid 46656520)
113. Skilleter DN, Paine AJ, Stirpe F (1981) A comparison of the accumulation of ricin by hepatic parenchymal and non-parenchymal cells and its inhibition of protein synthesis. Biochim Biophys Acta 677:495-500 (Pubitemid 12207077)
114. Slominska-Wojewodzka M, Gregers TF, Walchli S, Sandvig K (2006) EDEM is involved in retrotranslocation of ricin from the endoplasmic reticulum to the cytosol. Mol Biol Cell 17:1664-1675 (Pubitemid 44011584)
115. Smallshaw JE, Richardson JA, Pincus S, Schindler J, Vitetta ES (2005) Preclinical toxicity and efficacy testing of RiVax, a recombinant protein vaccine against ricin. Vaccine 23:4775-4784 (Pubitemid 41557328)
116. Smallshaw JE, Richardson JA, Vitetta ES (2007) RiVax, a recombinant ricin subunit vaccine, protects mice against ricin delivered by gavage or aerosol. Vaccine 25:7459-7469 (Pubitemid 47484003)
117. Smallshaw JE, Vitetta ES (2011) Ricin Vaccine Development. Curr Top Microbiol Immunol. doi: 10.1007/82-2011-156
118. Smith GP, Petrenko VA (1997) Phage Display. Chem Rev 97:391-410 (Pubitemid 127659250)
119. Sokolowska I, Walchli S, Wegrzyn G, Sandvig K, Slominska-Wojewodzka M (2011) A single point mutation in ricin A-chain increases toxin degradation and inhibits EDEM1-dependent ER retrotranslocation. Biochem J 436:371-385. doi:BJ20101493[pii]10.1042/BJ20101493
120. Sphyris N, Lord JM, Wales R, Roberts LM (1995) Mutational analysis of the Ricinus lectin B-chains. Galactose-binding ability of the 2 gamma subdomain of Ricinus communis agglutinin B-chain. J Biol Chem 270:20292-20297
121. Spooner RA, Hart PJ, Cook JP, Pietroni P, Rogon C, Hohfeld J, Roberts LM, Lord JM (2008) Cytosolic chaperones influence the fate of a toxin dislocated from the endoplasmic reticulum. Proc Natl Acad Sci USA 105:17408-17413. doi:0809013105[pii]10.1073/pnas.0809013105
122. Spooner RA, Lord JM (2011) How ricin and shiga toxin reach the cytosol of target cells: Retrotranslocation from the endoplasmic reticulum. Curr Top Microbiol Immunol. doi: 10.1007/82-2011-154
123. Spooner RA, Watson PD, Marsden CJ, Smith DC, Moore KA, Cook JP, Lord JM, Roberts LM (2004) Protein disulphide-isomerase reduces ricin to its A and B chains in the endoplasmic reticulum. Biochem J 383:285-293 (Pubitemid 39446689)
124. Swimmer C, Lehar SM, McCafferty J, Chiswell DJ, Blattler WA, Guild BC (1992) Phage display of ricin B chain and its single binding domains: system for screening galactose-binding mutants. Proc Natl Acad Sci USA 89:3756-3760
125. Taylor PR, Gordon S, Martinez-Pomares L (2005) The mannose receptor: linking homeostasis and immunity through sugar recognition. Trends Immunol 26:104-110
126. Thorpe CM, Hurley BP, Lincicome LL, Jacewicz MS, Keusch GT, Acheson DW (1999) Shiga toxins stimulate secretion of interleukin-8 from intestinal epithelial cells. Infect Immun 67:5985-5993 (Pubitemid 29508128)
127. Thorpe CM, Smith WE, Hurley BP, Acheson DW (2001) Shiga toxins induce, superinduce, and stabilize a variety of C-X-C chemokine mRNAs in intestinal epithelial cells, resulting in increased chemokine expression. Infect Immun 69:6140-6147 (Pubitemid 32885175)
128. Thorpe PE, Detre SI, Foxwell BM, Brown AN, Skilleter DN, Wilson G, Forrester JA, Stirpe F (1985) Modification of the carbohydrate in ricin with metaperiodate-cyanoborohydride mixtures. Effects on toxicity and in vivo distribution. Eur J Biochem 147:197-206
129. Utskarpen A, Slagsvold HH, Iversen TG, Walchli S, Sandvig K (2006) Transport of ricin from endosomes to the Golgi apparatus is regulated by Rab6A and Rab6A'. Traffic 7:663-672 (Pubitemid 43676975)
130. van Deurs B, Sandvig K, Petersen OW, Olsnes S, Simons K, Griffiths G (1988) Estimation of the amount of internalized ricin that reaches the trans-Golgi network. J Cell Biol 106:253-267 (Pubitemid 18052176)
131. van Deurs B, Tonnessen TI, Petersen OW, Sandvig K, Olsnes S (1986) Routing of internalized ricin and ricin conjugates to the Golgi complex. J Cell Biol 102:37-47 (Pubitemid 16155551)
132. Vita R, Zarebski L, Greenbaum JA, Emami H, Hoof I, Salimi N, Damle R, Sette A, Peters B (2010) The immune epitope database 2.0. Nucleic Acids Res 38: D854-62. doi:gkp1004 [pii]10.1093/nar/gkp1004
133. Vitetta ES, Smallshaw JE, Coleman E, Jafri H, Foster C, Munford R, Schindler J (2006) A pilot clinical trial of a recombinant ricin vaccine in normal humans. Proc Natl Acad Sci USA 103:2268-2273 (Pubitemid 43271659)
134. Wahome PG, Robertus JD, Mantis NJ (2011) Small-molecule inhibitors of ricin and shiga toxins. Curr Top Microbiol Immunol. doi:10.1007/82-2011-177
135. Wilhelmsen CL, Pitt ML (1996) Lesions of acute inhaled lethal ricin intoxication in rhesus monkeys. Vet Pathol 33:296-302 (Pubitemid 126481508)
136. Wu YN, Gadina M, Tao-Cheng JH, Youle RJ (1994) Retinoic acid disrupts the Golgi apparatus and increases the cytosolic routing of specific protein toxins. J Cell Biol 125:743-753 (Pubitemid 24151171)
137. Yamasaki C, Nishikawa K, Zeng XT, Katayama Y, Natori Y, Komatsu N, Oda T (2004) Induction of cytokines by toxins that have an identical RNA N-glycosidase activity: Shiga toxin, ricin, and modeccin. Biochim Biophys Acta 1671:44-50 (Pubitemid 38327128)
138. Yan C, Rill WL, Malli R, Hewetson J, Naseem H, Tammariello R, Kende M (1996) Intranasal stimulation of long-lasting immunity against aerosol ricin challenge with ricin toxoid vaccine encapsulated in polymeric microspheres. Vaccine 14:1031-1038 (Pubitemid 26281290)
139. Yermakova A, Mantis NJ (2011) Protective immunity to ricin toxin conferred by antibodies against the toxin's binding subunit (RTB). Vaccine. doi:S0264-410X(11)01334-X [pii]10.1016/j.vaccine.2011.08.075
140. Yoder JM, Aslam RU, Mantis NJ (2007) Evidence for widespread epithelial damage and coincident production of monocyte chemotactic protein 1 in a murine model of intestinal ricin intoxication. Infect Immun 75:1745-1750. doi:IAI.01528-06[pii]10.1128/IAI.01528-06 (Pubitemid 46559440)
141. Zentz C, Frenoy JP, Bourrillon R (1978) Binding of galactose and lactose to ricin. Equilibrium studies Biochim Biophys Acta 536:18-26
142. Zhang P, Zhong L, Struble EB, Watanabe H, Kachko A, Mihalik K, Virata-Theimer ML, Alter HJ, Feinstone S, Major M (2009) Depletion of interfering antibodies in chronic hepatitis C patients and vaccinated chimpanzees reveals broad cross-genotype neutralizing activity. Proc Natl Acad Sci USA 106:7537-7541