Adenovirus vector expressing Stx1/Stx2-neutralizing agent protects piglets infected with Escherichia coli O157: H7 against fatal systemic intoxication

Infection and Immunity

Volumn 83, Issue 1, 2015, Pages 286-291

  Sheoran, Abhineet S ^a   Dmitriev, Igor P ^b   Kashentseva, Elena A ^b   Cohen, Ocean ^a   Mukherjee, Jean ^a   Debatis, Michelle ^a   Shearer, Jonathan ^a   Tremblay, Jacqueline M ^a   Beamer, Gillian ^a   Curiel, David T ^b   Shoemaker, Charles B ^a   Tzipori, Saul ^a  

^a TUFTS UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; NEUTRALIZING ANTIBODY; PLACEBO; VEROTOXIN 1; VEROTOXIN 2; DRUG CARRIER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; DIARRHEA; ESCHERICHIA COLI INFECTION; ESCHERICHIA COLI O157; FATAL SYSTEMIC INTOXICATION; FEMALE; GNOTOBIOTICS; INTOXICATION; MOUSE; NONHUMAN; PIGLET; TRANSGENE; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; ESCHERICHIA COLI INFECTIONS; GENE VECTOR; GENETICS; HEMOLYTIC-UREMIC SYNDROME; HUMAN ADENOVIRUS C; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; MICROBIOLOGY; PIG; SURVIVAL; TIME;

ADENOVIRUSES, HUMAN; ANIMALS; ANTIBODIES, NEUTRALIZING; DISEASE MODELS, ANIMAL; DRUG CARRIERS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI O157; FEMALE; GENETIC VECTORS; HEMOLYTIC-UREMIC SYNDROME; INJECTIONS, INTRAMUSCULAR; MICE; SHIGA TOXIN 1; SHIGA TOXIN 2; SURVIVAL ANALYSIS; SWINE; TIME FACTORS;

EID: 84919474729     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02360-14     Document Type: Article

References (51)

1. Boerlin P, McEwen SA, Boerlin-Petzold F, Wilson JB, Johnson RP, Gyles CL. 1999. Associations between virulence factors of Shiga toxinproducing Escherichia coli and disease in humans. J Clin Microbiol 37: 497-503.
2. Griffin PM, Tauxe RV. 1991. The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiol Rev 13:60-98.
3. Milford DV, Taylor CM, Guttridge B, Hall SM, Rowe B, Kleanthous H. 1990. Haemolytic uraemic syndromes in the British Isles 1985-8: association with verocytotoxin producing Escherichia coli. Part 1. Clinical and epidemiological aspects. Arch Dis Child 65:716-721.
4. 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.
5. 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.
6. Rüssmann H, Schmidt H, Heesemann J, Caprioli A, Karch H. 1994. Variants of Shiga-like toxin II constitute a major toxin component in Escherichia coli O157 strains from patients with haemolytic uraemic syndrome. J Med Microbiol 40:338-343. http://dx.doi.org/10.1099/00222615-40-5-338.
7. Tzipori S, Sheoran A, Akiyoshi D, Donohue-Rolfe A, Trachtman H. 2004. Antibody therapy in the management of Shiga toxin-induced hemolytic uremic syndrome. Clin Microbiol Rev 17:926-941. http://dx.doi.org/10.1128/CMR.17.4.926-941.2004.
8. Fraser ME, Fujinaga M, Cherney MM, Melton-Celsa AR, Twiddy EM, O'Brien AD, James MN. 2004. Structure of Shiga toxin type 2 (Stx2) from Escherichia coli O157:H7. J Biol Chem 279:27511-27517. http://dx.doi.org/10.1074/jbc.M401939200.
9. Endo Y, Tsurugi K, Yutsudo T, Takeda Y, Ogasawara T, Igarashi K. 1988. Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur J Biochem 171:45-50.
10. Saxena SK, O'Brien AD, Ackerman EJ. 1989. Shiga toxin, Shiga-like toxin II variant, and ricin are all single-site RNA N-glycosidases of 28 S RNA when microinjected into Xenopus oocytes. J Biol Chem 264:596-601.
11. Ling H, Boodhoo A, Hazes B, Cummings MD, Armstrong GD, Brunton JL, Read RJ. 1998. Structure of the Shiga-like toxin I B-pentamer complexed with an analogue of its receptor Gb3. Biochemistry 37:1777-1788. http://dx.doi.org/10.1021/bi971806n.
12. Shimizu H, Field RA, Homans SW, Donohue-Rolfe A. 1998. Solution structure of the complex between the B-subunit homopentamer of verotoxin VT-1 from Escherichia coli and the trisaccharide moiety of globotriaosylceramide. Biochemistry 37:11078-11082. http://dx.doi.org/10.1021/bi980946+.
13. Lingwood CA, Law H, Richardson S, Petric M, Brunton JL, De Grandis S, Karmali M. 1987. Glycolipid binding of purified and recombinant Escherichia coli produced verotoxin in vitro. J Biol Chem 262:8834-8839.
14. Waddell T, Head S, Petric M, Cohen A, Lingwood C. 1988. Globotriosyl ceramide is specifically recognized by the Escherichia coli verocytotoxin 2. Biochem Biophys Res Commun 152:674-679. http://dx.doi.org/10.1016/S0006-291X(88)80091-3.
15. Lingwood CA. 1996. Role of verotoxin receptors in pathogenesis. Trends Microbiol 4:147-153. http://dx.doi.org/10.1016/0966-842X(96)10017-2.
16. Tesh VL. 2010. Induction of apoptosis by Shiga toxins. Future Microbiol 5:431-453. http://dx.doi.org/10.2217/fmb.10.4.
17. Mukherjee J, Chios K, Fishwild D, Hudson D, O'Donnell S, Rich SM, Donohue-Rolfe A, Tzipori S. 2002. Human Stx2-specific monoclonal antibodies prevent systemic complications of Escherichia coli O157:H7 infection. Infect Immun 70:612-619. http://dx.doi.org/10.1128/IAI.70.2.612-619.2002.
18. 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.
19. 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.
20. Sheoran AS, Chapman-Bonofiglio S, Harvey BR, Mukherjee J, Georgiou G, Donohue-Rolfe A, Tzipori S. 2005. Human antibody against Shiga toxin 2 administered to piglets after the onset of diarrhea due to Escherichia coli O157:H7 prevents fatal systemic complications. Infect Immun 73:4607-4613. http://dx.doi.org/10.1128/IAI.73.8.4607-4613.2005.
21. Jeong KI, Tzipori S, Sheoran AS. 2010. Shiga toxin 2-specific but not Shiga toxin 1-specific human monoclonal antibody protects piglets challenged with enterohemorrhagic Escherichia coli producing Shiga toxin 1 and Shiga toxin 2. J Infect Dis 201:1081-1083. http://dx.doi.org/10.1086/651198.
22. Mukherjee J, Tremblay JM, Leysath CE, Ofori K, Baldwin K, Feng X, Bedenice D, Webb RP, Wright PM, Smith LA, Tzipori S, Shoemaker CB. 2012. A novel strategy for development of recombinant antitoxin therapeutics tested in a mouse botulism model. PLoS One 7:e29941. http://dx.doi.org/10.1371/journal.pone.0029941.
23. Tremblay JM, Mukherjee J, Leysath CE, Debatis M, Ofori K, Baldwin K, Boucher C, Peters R, Beamer G, Sheoran A, Bedenice D, Tzipori S, Shoemaker CB. 2013. A single VHH-based toxin neutralizing agent and an effector antibody protects mice against challenge with Shiga toxins 1 and 2. Infect Immun 81:4592-4603. http://dx.doi.org/10.1128/IAI.01033-13.
24. Vance DJ, Tremblay JM, Mantis NJ, Shoemaker CB. 2013. Stepwise engineering of heterodimeric single domain camelidVHHantibodies that passively protect mice from ricin toxin. J Biol Chem 288:36538-36547. http://dx.doi.org/10.1074/jbc.M113.519207.
25. Yang Z, Schmidt D, Liu W, Li S, Shi L, Sheng J, Chen K, Yu H, Tremblay JM, Chen X, Piepenbrink KH, Sundberg EJ, Kelly CP, Bai G, Shoemaker CB, Feng H. 2014. A novel multivalent, single-domain antibody targeting TcdA and TcdB prevents fulminant Clostridium difficile infection in mice. J Infect Dis 210:964-972. http://dx.doi.org/10.1093/infdis/jiu196.
26. Sepulveda J, Mukherjee J, Tzipori S, Simpson LL, Shoemaker CB. 2010. Efficient serum clearance of botulinum neurotoxin achieved using a pool of small antitoxin binding agents. Infect Immun 78:756-763. http://dx.doi.org/10.1128/IAI.01084-09.
27. Mukherjee J, Dmitriev I, Debatis M, Tremblay JM, Beamer G, Kashentseva EA, Curiel DT, Shoemaker CB. 2014. Prolonged prophylactic protection from botulism with a single adenovirus treatment promoting serum expression of a VHH-based antitoxin protein. PLoS One 9:e106422. http://dx.doi.org/10.1371/journal.pone.0106422.
28. Sofer-Podesta C, Ang J, Hackett NR, Senina S, Perlin D, Crystal RG, Boyer JL. 2009. Adenovirus-mediated delivery of an anti-V antigen monoclonal antibody protects mice against a lethal Yersinia pestis challenge. Infect Immun 77:1561-1568. http://dx.doi.org/10.1128/IAI.00856-08.
29. Kasuya K, Boyer JL, Tan Y, Alipui DO, Hackett NR, Crystal RG. 2005. Passive immunotherapy for anthrax toxin mediated by an adenovirus expressing an anti-protective antigen single-chain antibody. Mol Ther 11: 237-244. http://dx.doi.org/10.1016/j.ymthe.2004.10.018.
30. Skaricic D, Traube C, De B, Joh J, Boyer J, Crystal RG, Worgall S. 2008. Genetic delivery of an anti-RSV antibody to protect against pulmonary infection with RSV. Virology 378:79-85. http://dx.doi.org/10.1016/j.virol.2008.04.016.
31. Fang J, Yi S, Simmons A, Tu GH, Nguyen M, Harding TC, VanRoey M, Jooss K. 2007. An antibody delivery system for regulated expression of therapeutic levels of monoclonal antibodies in vivo. Mol Ther 15:1153-1159. http://dx.doi.org/10.1038/sj.mt.6300142.
32. Zuber C, Mitteregger G, Schuhmann N, Rey C, Knackmuss S, Rupprecht W, Reusch U, Pace C, Little M, Kretzschmar HA, Hallek M, Buning H, Weiss S. 2008. Delivery of single-chain antibodies (scFvs) directed against the 37/67 kDa laminin receptor into mice via recombinant adeno-associated viral vectors for prion disease gene therapy. J Gen Virol 89:2055-2061. http://dx.doi.org/10.1099/vir.0.83670-0.
33. De BP, Hackett NR, Crystal RG, Boyer JL. 2008. Rapid/sustained antianthrax passive immunity mediated by co-administration of Ad/AAV. Mol Ther 16:203-209. http://dx.doi.org/10.1038/sj.mt.6300344.
34. Tutykhina IL, Sedova ES, Gribova IY, Ivanova TI, Vasilev LA, Rutovskaya MV, Lysenko AA, Shmarov MM, Logunov DY, Naroditsky BS, Tillib SV, Gintsburg AL. 2013. Passive immunization with a recombinant adenovirus expressing an HA (H5)-specific single-domain antibody protects mice from lethal influenza infection. Antiviral Res 97:318-328. http://dx.doi.org/10.1016/j.antiviral.2012.12.021.
35. Tarr PI, Neill MA, Clausen CR, Newland JW, Neill RJ, Moseley SL. 1989. Genotypic variation in pathogenic Escherichia coli O157:H7 isolated from patients in Washington, 1984-1987. J Infect Dis 159:344-347. http://dx.doi.org/10.1093/infdis/159.2.344.
36. Donohue-Rolfe A, Acheson DW, Kane AV, Keusch GT. 1989. Purification of Shiga toxin and Shiga-like toxins I and II by receptor analog affinity chromatography with immobilized P1 glycoprotein and production of cross-reactive monoclonal antibodies. Infect Immun 57:3888-3893.
37. Luo J, Deng ZL, Luo X, Tang N, Song WX, Chen J, Sharff KA, Luu HH, Haydon RC, Kinzler KW, Vogelstein B, He TC. 2007. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2:1236-1247. http://dx.doi.org/10.1038/nprot.2007.135.
38. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. 1998. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 95:2509-2514. http://dx.doi.org/10.1073/pnas.95.5.2509.
39. Graham FL, Smiley J, Russell WC, Nairn R. 1977. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 36:59-74. http://dx.doi.org/10.1099/0022-1317-36-1-59.
40. Fallaux FJ, Kranenburg O, Cramer SJ, Houweling A, Van Ormondt H, Hoeben RC, Van Der Eb AJ. 1996. Characterization of 911: a new helper cell line for the titration and propagation of early region 1-deleted adenoviral vectors. Hum Gene Ther 7:215-222. http://dx.doi.org/10.1089/hum.1996.7.2-215.
41. Maizel JV, Jr, White DO, Scharff MD. 1968. The polypeptides of adenovirus. I. Evidence for multiple protein components in the virion and a comparison of types 2, 7A, and 12. Virology 36:115-125.
42. Donohue-Rolfe A, Kondova I, Oswald S, Hutto D, Tzipori S. 2000. Escherichia coli O157:H7 strains that express Shiga toxin (Stx) 2 alone are more neurotropic for gnotobiotic piglets than are isotypes producing only Stx1 or both Stx1 and Stx2. J Infect Dis 181:1825-1829. http://dx.doi.org/10.1086/315421.
43. Tzipori S, Gunzer F, Donnenberg MS, de Montigny L, Kaper JB, Donohue-Rolfe A. 1995. The role of the eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect Immun 63:3621-3627.
44. Tzipori S, Chow CW, Powell HR. 1988. Cerebral infection with Escherichia coli O157:H7 in humans and gnotobiotic piglets. J Clin Pathol 41: 1099-1103. http://dx.doi.org/10.1136/jcp.41.10.1099.
45. Donohue-Rolfe A, Kondova I, Mukherjee J, Chios K, Hutto D, Tzipori S. 1999. Antibody-based protection of gnotobiotic piglets infected with Escherichia coli O157:H7 against systemic complications associated with Shiga toxin 2. Infect Immun 67:3645-3648.
46. Francis DH, Collins JE, Duimstra JR. 1986. Infection of gnotobiotic pigs with an Escherichia coli O157:H7 strain associated with an outbreak of hemorrhagic colitis. Infect Immun 51:953-956.
47. 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 cαStx2 administered intravenously to healthy adult volunteers. Antimicrob Agents Chemother 49:1808-1812. http://dx.doi.org/10.1128/AAC.49.5.1808-1812.2005.
48. 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.
49. López EL, Contrini MM, Glatstein E, Gonzalez 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.
50. Muyldermans S. 2013. Nanobodies: natural single-domain antibodies. Annu Rev Biochem 82:775-797. http://dx.doi.org/10.1146/annurev-biochem-063011-092449.
51. Hassanzadeh-Ghassabeh G, Devoogdt N, De Pauw P, Vincke C, Muyldermans S. 2013. Nanobodies and their potential applications. Nanomedicine (Lond) 8:1013-1026. http://dx.doi.org/10.2217/nnm.13.86.