Protective efficacy and pharmacokinetics of human/mouse chimeric anti-Stx1 and anti-Stx2 antibodies in mice

Clinical and Vaccine Immunology

Volumn 22, Issue 4, 2015, Pages 448-455

  Melton Celsa, Angela R ^a   Carvalho, H M ^a   Thuning Roberson, Claire ^b   O'Brien, A D ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b Thallion Pharmaceuticals Inc   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC ANTIBODY; MONOCLONAL ANTIBODY; STREPTOMYCIN; STX1 ANTIBODY; STX2 ANTIBODY; UNCLASSIFIED DRUG; VEROTOXIN 1; VEROTOXIN 2; ANTITOXIN; BACTERIUM ANTIBODY; RECOMBINANT PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DETECTION; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BACTERIAL LOAD; BACTERIAL STRAIN; CONTROLLED STUDY; DEATH; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG HALF LIFE; DRUG SAFETY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HEMOLYTIC UREMIC SYNDROME; IMMUNITY; LETHAL DOSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROPHYLAXIS; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; TOXIN SYNTHESIS; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; ESCHERICHIA COLI INFECTIONS; GENETICS; HALF LIFE TIME; INTOXICATION; PREVENTION AND CONTROL; SURVIVAL; TREATMENT OUTCOME;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, MONOCLONAL; ANTITOXINS; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI INFECTIONS; FEMALE; HALF-LIFE; MALE; MICE; POISONING; RECOMBINANT PROTEINS; SHIGA TOXIN 1; SHIGA TOXIN 2; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 84925439946     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00022-15     Document Type: Article

References (52)

1. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV. 1999. Food-related illness and death in the United States. Emerg Infect Dis 5:607-625. http://dx.doi.org/10.3201/eid0505.990502.
2. Hedican EB, Medus C, Besser JM, Juni BA, Koziol B, Taylor C, Smith KE. 2009. Characteristics of O157 versus non-O157 Shiga toxin-producing Escherichia coli infections in Minnesota, 2000-2006. Clin Infect Dis 49:358-364. http://dx.doi.org/10.1086/600302.
3. Centers for Disease Control and Prevention. 2009. Preliminary FoodNet Data on the incidence of infection with pathogens transmitted commonly through food - 10 states, 2008. MMWR Morb Mortal Wkly Rep 58:333-337.
4. Gould LH, Mody RK, Ong KL, Clogher P, Cronquist AB, Garman KN, Lathrop S, Medus C, Spina NL, Webb TH, White PL, Wymore K, Gierke RE, Mahon BE, Griffin PM; Emerging Infections Program Foodnet Working Group. 2013. Increased recognition of non-O157 Shiga toxin-producing Escherichia coli infections in the United States during 2000-2010: epidemiologic features and comparison with E. coli O157 infections. Foodborne Pathog Dis 10:453-460. http://dx.doi.org/10.1089/fpd.2012.1401.
5. Centers for Disease Control and Prevention. 2013. Incidence and trends of infection with pathogens transmitted commonly through food - foodborne diseases active surveillance network, 10 U.S. sites, 1996-2012. MMWR Morb Mortal Wkly Rep 62:283-287.
6. Centers for Disease Control and Prevention. 2006. Ongoing multistate outbreak of Escherichia coli serotype O157:H7 infections associated with consumption of fresh spinach - United States, September 2006. MMWR Morb Mortal Wkly Rep 55:1045-1046.
7. Gerber A, Karch H, Allerberger F, Verweyen HM, Zimmerhackl LB. 2002. Clinical course and the role of Shiga toxin-producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997-2000, in Germany and Austria: a prospective study. J Infect Dis 186:493-500. http://dx.doi.org/10.1086/341940.
8. Tozzi AE, Caprioli A, Minelli F, Gianviti A, De Petris L, Edefonti A, Montini G, Ferretti A, De Palo T, Gaido M, Rizzoni G. 2003. Shiga toxin-producing Escherichia coli infections associated with hemolytic uremic syndrome, Italy, 1988-2000. Emerg Infect Dis 9:106-108. http://dx.doi.org/10.3201/eid0901.020266.
9. Kawasaki Y, Suyama K, Maeda R, Yugeta E, Takano K, Suzuki S, Sakuma H, Nemoto K, Sato T, Nagasawa K, Hosoya M. 2014. Incidence and index of severity of hemolytic uremic syndrome in a 26 year period in Fukushima Prefecture, Japan. Pediatr Int 56:77-82. http://dx.doi.org/10.1111/ped.12193.
10. Elliott EJ, Robins-Browne RM, O'Loughlin EV, Bennett-Wood V, Bourke J, Henning P, Hogg GG, Knight J, Powell H, Redmond D. 2001. Nationwide study of haemolytic uraemic syndrome: clinical, microbiological, and epidemiological features. Arch Dis Child 85:125-131. http://dx.doi.org/10.1136/adc.85.2.125.
11. Lynn RM, O'Brien SJ, Taylor CM, Adak GK, Chart H, Cheasty T, Coia JE, Gillespie IA, Locking ME, Reilly WJ, Smith HR, Waters A, Willshaw GA. 2005. Childhood hemolytic uremic syndrome, United Kingdom and Ireland. Emerg Infect Dis 11:590-596. http://dx.doi.org/10.3201/eid1104.040833.
12. Espié E, Grimont F, Mariani-Kurkdjian P, Bouvet P, Haeghebaert S, Filliol I, Loirat C, Decludt B, Minh NN, Vaillant V, de Valk H. 2008. Surveillance of hemolytic uremic syndrome in children less than 15 years of age, a system to monitor O157 and non-O157 Shiga toxin-producing Escherichia coli infections in France, 1996-2006. Pediatr Infect Dis J 27: 595-601. http://dx.doi.org/10.1097/INF.0b013e31816a062f.
13. Rivas M, Sosa-Estani S, Rangel J, Caletti MG, Valles P, Roldan CD, Balbi L, Marsano de Mollar MC, Amoedo D, Miliwebsky E, Chinen I, Hoekstra RM, Mead P, Griffin PM. 2008. Risk factors for sporadic Shiga toxin-producing Escherichia coli infections in children, Argentina. Emerg Infect Dis 14:763-771. http://dx.doi.org/10.3201/eid1405.071050.
14. Ahn CK, Holt NJ, Tarr PI. 2009. Shiga-toxin producing Escherichia coli and the hemolytic uremic syndrome: what have we learned in the past 25 years? Adv Exp Med Biol 634:1-17. http://dx.doi.org/10.1007/978-0-387-79838-7-1.
15. Ake JA, Jelacic S, Ciol MA, Watkins SL, Murray KF, Christie DL, Klein EJ, Tarr PI. 2005. Relative nephroprotection during Escherichia coli O157:H7 infections: association with intravenous volume expansion. Pediatrics 115:e673-e680. http://dx.doi.org/10.1542/peds.2004-2236.
16. Frank C, Werber D, Cramer JP, Askar M, Faber M, an der Heiden M, Bernard H, Fruth A, Prager R, Spode A, Wadl M, Zoufaly A, Jordan S, Kemper MJ, Follin P, Müller L, King LA, Rosner B, Buchholz U, Stark K, Krause G, HUS Investigation Team. 2011. Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med 365:1771-1780. http://dx.doi.org/10.1056/NEJMoa1106483.
17. Karch H, Denamur E, Dobrindt U, Finlay BB, Hengge R, Johannes L, Ron EZ, Tonjum T, Sansonetti PJ, Vicente M. 2012. The enemy within us: lessons from the 2011 European Escherichia coli O104:H4 outbreak. EMBO Mol Med 4:841-848. http://dx.doi.org/10.1002/emmm.201201662.
18. Keating GM. 2013. Eculizumab: a review of its use in atypical haemolytic uraemic syndrome. Drugs 73:2053-2066. http://dx.doi.org/10.1007/s40265-013-0147-7.
19. Porubsky S, Federico G, Muthing J, Jennemann R, Gretz N, Buttner S, Obermuller N, Jung O, Hauser IA, Grone E, Geiger H, Grone HJ, Betz C. 2014. Direct acute tubular damage contributes to Shigatoxin-mediated kidney failure. J Pathol 234:120-133. http://dx.doi.org/10.1002/path.4388.
20. Menne J, Nitschke M, Stingele R, Abu-Tair M, Beneke J, Bramstedt J, Bremer JP, Brunkhorst R, Busch V, Dengler R, Deuschl G, Fellermann K, Fickenscher H, Gerigk C, Goettsche A, Greeve J, Hafer C, Hagenmuller F, Haller H, Herget-Rosenthal S, Hertenstein B, Hofmann C, Lang M, Kielstein JT, Klostermeier UC, Knobloch J, Kuehbacher M, Kunzendorf U, Lehnert H, Manns MP, Menne TF, Meyer TN, Michael C, Munte T, Neumann-Grutzeck C, Nuernberger J, Pavenstaedt H, Ramazan L, Renders L, Repenthin J, Ries W, Rohr A, Rump LC, Samuelsson O, Sayk F, Schmidt BM, Schnatter S, Schocklmann H, Schreiber S, von Seydewitz CU, et al. 2012. Validation of treatment strategies for enterohaemorrhagic Escherichia coli O104:H4 induced haemolytic uraemic syndrome: case-control study. BMJ 345:e4565. http://dx.doi.org/10.1136/bmj.e4565.
21. Kielstein JT, Beutel G, Fleig S, Steinhoff J, Meyer TN, Hafer C, Kuhlmann U, Bramstedt J, Panzer U, Vischedyk M, Busch V, Ries W, Mitzner S, Mees S, Stracke S, Nurnberger J, Gerke P, Wiesner M, Sucke B, Abu-Tair M, Kribben A, Klause N, Schindler R, Merkel F, Schnatter S, Dorresteijn EM, Samuelsson O, Brunkhorst R. 2012. Best supportive care and therapeutic plasma exchange with or without eculizumab in Shiga-toxin-producing E. coli O104:H4 induced haemolytic-uraemic syndrome: an analysis of the German STEC-HUS registry. Nephrol Dial Transplant 27:3807-3815. http://dx.doi.org/10.1093/ndt/gfs394.
22. Melton-Celsa AR, Smith MJ, O'Brien DA. 2005. Shiga toxins: potent poisons, pathogenicity determinants, and pharmacological agents. EcoSal Plus http://dx.doi.org/10.1128/ecosalplus.8.7.8.
23. Bielaszewska M, Friedrich AW, Aldick T, Schurk-Bulgrin R, Karch H. 2006. Shiga toxin activatable by intestinal mucus in Escherichia coli isolated from humans: predictor for a severe clinical outcome. Clin Infect Dis 43:1160-1167. http://dx.doi.org/10.1086/508195.
24. Friedrich AW, Bielaszewska M, Zhang WL, Pulz M, Kuczius T, Ammon A, Karch H. 2002. Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J Infect Dis 185:74-84. http://dx.doi.org/10.1086/338115.
25. Scheutz F, Teel LD, Beutin L, Pierard D, Buvens G, Karch H, Mellmann A, Caprioli A, Tozzoli R, Morabito S, Strockbine NA, Melton-Celsa AR, Sanchez M, Persson S, O'Brien AD. 2012. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol 50:2951-2963. http://dx.doi.org/10.1128/JCM.00860-12.
26. Ostroff SM, Tarr PI, Neill MA, Lewis JH, Hargrett-Bean N, Kobayashi JM. 1989. Toxin genotypes and plasmid profiles as determinants of systemic sequelae in Escherichia coli O157:H7 infections. J Infect Dis 160: 994-998. http://dx.doi.org/10.1093/infdis/160.6.994.
27. Kim YB, Okuda J, Matsumoto C, Morigaki T, Asai N, Watanabe H, Nishibuchi M. 1998. Isolation of an Escherichia coli O157:H7 strain producing Shiga toxin 1 but not Shiga toxin 2 from a patient with hemolytic uremic syndrome in Korea. FEMS Microbiol Lett 166:43-48. http://dx.doi.org/10.1111/j.1574-6968.1998.tb13181.x.
28. Koster F, Levin J, Walker L, Tung KS, Gilman RH, Rahaman MM, Majid MA, Islam S, Williams RC, Jr. 1978. Hemolytic-uremic syndrome after shigellosis. Relation to endotoxemia and circulating immune complexes. N Engl J Med 298:927-933.
29. Bhimma R, Rollins NC, Coovadia HM, Adhikari M. 1997. Postdysenteric hemolytic uremic syndrome in children during an epidemic of Shigella dysentery in Kwazulu/Natal. Pediatr Nephrol 11:560-564. http://dx.doi.org/10.1007/s004670050338.
30. Perera LP, Marques LR, O'Brien AD. 1988. Isolation and characterization of monoclonal antibodies to Shiga-like toxin II of enterohemorrhagic Escherichia coli and use of the monoclonal antibodies in a colony enzyme-linked immunosorbent assay. J Clin Microbiol 26:2127-2131.
31. Strockbine NA, Marques LR, Holmes RK, O'Brien AD. 1985. Characterization of monoclonal antibodies against Shiga-like toxin from Escherichia coli. Infect Immun 50:695-700.
32. Hwang WY, Foote J. 2005. Immunogenicity of engineered antibodies. Methods 36:3-10. http://dx.doi.org/10.1016/j.ymeth.2005.01.001.
33. Edwards AC, Melton-Celsa AR, Arbuthnott K, Stinson JR, Schmitt CK, Wong HC, O'Brien AD. 1998. Vero cell neutralization and mouse protective efficacy of humanized monoclonal antibodies against Escherichia coli toxins Stx1 and Stx2, p 388-392. In Kaper JB, O'Brien AD (ed), Escherichia coli O157:H7 and other Shiga toxin-producing E. coli strains. ASM Press, Washington, DC.
34. Bitzan M, Poole R, Mehran M, Sicard E, Brockus C, Thuning-Roberson C, Riviere M. 2009. Safety and pharmacokinetics of chimeric anti-Shiga toxin 1 and anti-Shiga toxin 2 monoclonal antibodies in healthy volunteers. Antimicrob Agents Chemother 53:3081-3087. http://dx.doi.org/10.1128/AAC.01661-08.
35. Dowling TC, Chavaillaz PA, Young DG, Melton-Celsa A, O'Brien A, Thuning-Roberson C, Edelman R, Tacket CO. 2005. Phase 1 safety and pharmacokinetic study of chimeric murine-human monoclonal antibody c alpha Stx2 administered intravenously to healthy adult volunteers. Antimicrob Agents Chemother 49:1808-1812. http://dx.doi.org/10.1128/AAC.49.5.1808-1812.2005.
36. Melton-Celsa AR, O'Brien DA. 2000. Shiga toxins of Shigella dysenteriae and Escherichia coli, p 385-406. In Aktories K, Just I (ed), Handbook of experimental pharmacology, vol 145. Springer-Verlag, Berlin, Germany.
37. Schmitt CK, McKee ML, O'Brien AD. 1991. Two copies of Shiga-like toxin II-related genes common in enterohemorrhagic Escherichia coli strains are responsible for the antigenic heterogeneity of the O157:H-strain E32511. Infect Immun 59:1065-1073.
38. Lindgren SW, Melton AR, O'Brien AD. 1993. Virulence of enterohemorrhagic Escherichia coli O91:H21 clinical isolates in an orally infected mouse model. Infect Immun 61:3832-3842.
39. Melton-Celsa AR, Rogers JE, Schmitt CK, Darnell SC, O'Brien AD. 1998. Virulence of Shiga toxin-producing Escherichia coli (STEC) in orally-infected mice correlates with the type of toxin produced by the infecting strain. Jpn J Med Sci Biol 51(Suppl):S108-S114.
40. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. The National Academies Press, Washington, DC.
41. Wadolkowski EA, Burris JA, O'Brien AD. 1990. Mouse model for colonization and disease caused by enterohemorrhagic Escherichia coli O157:H7. Infect Immun 58:2438-2445.
42. Mukherjee J, Chios K, Fishwild D, Hudson D, O'Donnell S, Rich SM, Donohue-Rolfe A, Tzipori S. 2002. Production and characterization of protective human antibodies against Shiga toxin 1. Infect Immun 70:5896-5899. http://dx.doi.org/10.1128/IAI.70.10.5896-5899.2002.
43. Franchini M, Zaffanello M, Veneri D. 2006. Advances in the pathogenesis, diagnosis and treatment of thrombotic thrombocytopenic purpura and hemolytic uremic syndrome. Thromb Res 118:177-184. http://dx.doi.org/10.1016/j.thromres.2005.07.013.
44. Kimura T, Co MS, Vasquez M, Wei S, Xu H, Tani S, Sakai Y, Kawamura T, Matsumoto Y, Nakao H, Takeda T. 2002. Development of humanized monoclonal antibody TMA-15 which neutralizes Shiga toxin 2. Hybrid Hybridomics 21:161-168. http://dx.doi.org/10.1089/153685902760173872.
45. Sheoran AS, Chapman S, Singh P, Donohue-Rolfe A, Tzipori S. 2003. Stx2-specific human monoclonal antibodies protect mice against lethal infection with Escherichia coli expressing Stx2 variants. Infect Immun 71: 3125-3130. http://dx.doi.org/10.1128/IAI.71.6.3125-3130.2003.
46. Yamagami S, Motoki M, Kimura T, Izumi H, Takeda T, Katsuura Y, Matsumoto Y. 2001. Efficacy of postinfection treatment with anti-Shiga toxin (Stx) 2 humanized monoclonal antibody TMA-15 in mice lethally challenged with Stx-producing Escherichia coli. J Infect Dis 184:738-742. http://dx.doi.org/10.1086/323082.
47. Lambert M. 2014. AAP issues updated guidance on palivizumab prophylaxis for RSV infection. Am Fam Physician 90:867-868.
48. López EL, Contrini MM, Glatstein E, González Ayala S, Santoro R, Allende D, Ezcurra G, Teplitz E, Koyama T, Matsumoto Y, Sato H, Sakai K, Hoshide S, Komoriya K, Morita T, Harning R, Brookman S. 2010. Safety and pharmacokinetics of urtoxazumab, a humanized monoclonal antibody, against Shiga-like toxin 2 in healthy adults and in pediatric patients infected with Shiga-like toxin-producing Escherichia coli. Antimicrob Agents Chemother 54:239-243. http://dx.doi.org/10.1128/AAC.00343-09.
49. Hara-Kudo Y, Takatori K. 2011. Contamination level and ingestion dose of foodborne pathogens associated with infections. Epidemiol Infect 139:1505-1510. http://dx.doi.org/10.1017/S095026881000292X.
50. Tilden J, Jr, Young W, McNamara AM, Custer C, Boesel B, Lambert-Fair MA, Majkowski J, Vugia D, Werner SB, Hollingsworth J, Morris JG, Jr. 1996. A new route of transmission for Escherichia coli: infection from dry fermented salami. Am J Public Health 86:1142-1145. http://dx.doi.org/10.2105/AJPH.86.8-Pt-1.1142.
51. Snedeker KG, Campbell M, Sargeant JM. 2012. A systematic review of vaccinations to reduce the shedding of Escherichia coli O157 in the faeces of domestic ruminants. Zoonoses Public Health 59:126-138. http://dx.doi.org/10.1111/j.1863-2378.2011.01426.x.
52. Varela NP, Dick P, Wilson J. 2013. Assessing the existing information on the efficacy of bovine vaccination against Escherichia coli O157:H7 - a systematic review and meta-analysis. Zoonoses Public Health 60:253-268. http://dx.doi.org/10.1111/j.1863-2378.2012.01523.x.