Inhibition of Shiga Toxin 2 (Stx2) in apple juices and its resistance to pasteurization

Journal of Food Science

Volumn 75, Issue 5, 2010, Pages

  Rasooly, Reuven ^a   Do, Paula M ^a   Levin, Carol E ^a   Friedman, Mendel ^a  

^a WESTERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

Apple juice; E. coli O157:H7; MTT assay; Pasteurization; Shiga Stx2 toxin inactivation

Indexed keywords

OXIDOREDUCTASE; VEROTOXIN 2;

APPLE; ARTICLE; BACTERIAL COUNT; BEVERAGE; CHEMISTRY; DRUG ANTAGONISM; ESCHERICHIA COLI; FOOD CONTROL; FOOD PRESERVATION; HEAT; IMMUNOLOGY; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOLECULAR WEIGHT; ANTAGONISTS AND INHIBITORS; MALUS; PROCEDURES;

BEVERAGES; COLONY COUNT, MICROBIAL; ESCHERICHIA COLI; FOOD MICROBIOLOGY; FOOD PRESERVATION; HOT TEMPERATURE; MALUS; MOLECULAR WEIGHT; OXIDOREDUCTASES; SHIGA TOXIN 2;

BACTERIA (MICROORGANISMS); MALUS X DOMESTICA;

EID: 77952117782     PISSN: 00221147     EISSN: 17503841     Source Type: Journal    
DOI: 10.1111/j.1750-3841.2010.01615.x     Document Type: Article

References (57)

1. Acheson DWK, Lincicome LL, Jacewicz MS, Keusch GT. Shiga toxin interaction with intestinal epithelial cells. Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli Strains 1998, 140-7. Kaper JB, O'Brien AD, editors, Washington, D.C., ASM Press, p
2. Aguilar-Rosas SF, Ballinas-Casarrubias ML, Nevárez-Moorillón GV, Martín-Belloso O, Ortega-Rivas E. Thermal and pulsed electric fields pasteurization of apple juice: effects on physicochemical properties and flavour compounds. J Food Eng 2007, 83(1):41-6.
3. Alley MC, Scudiero DA, Monks A, Hursey Czerwinski MLMJ, Fine DL, Abbott BJ, Mayo JG, Shoemaker RH, Boyd MR. Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res 1988, 48(3):589-601.
4. Atlas RM. Biosecurity concerns: changing the face of academic research. Chem Health Saf 2005, 12(3):15-23.
5. Besser RE, Lett SM, Weber JT, Doyle MP, Barrett TJ, Wells JG, Griffin PM. An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157:H7 in fresh-pressed apple cider. JAMA 1993, 269:2217-20.
6. Brigotti M, Carnicelli D, González Vara A. Shiga toxin 1 acting on DNA in vitro is a heat-stable enzyme not requiring proteolytic activation. Biochimie 2004, 86(4-5):305-9.
7. Buchanan RL, Edelson SG, Miller RL, Sapers GM. Contamination of intact apples after immersion in an aqueous environment containing Escherichia coli O157:H7. J Food Prot 1999, 62(5):444-50.
8. Charles-Rodríguez AV, Nevárez-Moorillón GV, Zhang QH, Ortega-Rivas E. Comparison of thermal processing and pulsed electric fields treatment in pasteurization of apple juice. Food Bioprod Process 2007, 85(2C):93-7.
9. Choi LH, Nielsen SS. The effects of thermal and nonthermal processing methods on apple cider quality and consumer acceptability. J Food Qual 2005, 28(1):13-29.
10. Deliganis CV. Death by apple juice: the problem of foodborne illness, the regulatory response, and further suggestions for reform. Food Drug Law J 1998, 53(4):681-728.
11. Dowd SE, Williams JB. Comparison of Shiga-like toxin II expression between two genetically diverse lineages of Escherichia coli O157:H7. J Food Prot 2008, 71(8):1673-8.
12. Downes FP, Barrett TJ, Green JH, Aloisio CH, Spika JS, Strockbine NA, Wachsmuth IK. Affinity purification and characterization of Shiga-like toxin II and production of toxin-specific monoclonal antibodies. Infect Immun 1988, 56(8):1926-33.
13. Grade "A" pasteurized milk ordinance 2007, http://www.fda.gov, FDA] Food and Drug Administration, Public Health Service/Food and Drug Administration, Available from, Accessed May 11, 2009
14. Flagler MJ, Strasser JE, Chalk CL, Weiss AA. Comparative analysis of the abilities of Shiga toxins 1 and 2 to bind to and influence neutrophil apoptosis. Infect Immun 2007, 75(2):760-5.
15. Friedman M. Overview of antibacterial, antitoxin, antiviral, and antifungal activities of tea flavonoids and teas. Mol Nutr Food Res 2007, 51(1):116-34.
16. Friedman M, Wilson RE, Ziderman II. Effect of heating on mutagenicity of fruit juices in the Ames test. J Agric Food Chem 1990, 38(3):740-3.
17. Friedman M, Henika PR, Levin CE, Mandrell RE. Antibacterial activities of plant essential oils and their components against Escherichia coli O157:H7 and Salmonella enterica in apple juice. J Agric Food Chem 2004, 52(19):6042-8.
18. Friedman M, Lee KR, Kim HJ, Lee IS, Kozukue N. Anticarcinogenic effects of glycoalkaloids from potatoes against human cervical, liver, lymphoma, and stomach cancer cells. J Agric Food Chem 2005, 53(15):6162-9.
19. Friedman M, Mackey BE, Kim HJ, Lee IS, Lee KR, Lee SU, Kozukue E, Kozukue N. Structure-activity relationships of tea compounds against human cancer cells. J Agric Food Chem 2007, 55(2):243-53.
20. Friedrich AW, Bielaszewska M, Karch H. Diagnosis of Shiga toxin-producing Escherichia coli infections. Laboratoriums Medizin 2002, 26(3-4):183-90.
21. Hancock DD, Rice DH, Herriott DE, Besser TE, Ebel ED, Carpenter LV. Effects of farm manure-handling practices on Escherichia coli O157 prevalence in cattle. J Food Prot 1997, 60(4):363-6.
22. Ikeda M, Gunji Y, Sonoda H, Oshikawa S, Shimono M, Horie A, Ito K, Yamasaki S. Inhibitory effect of tyrphostin 47 on Shiga toxin-induced cell death. Eur J Pharmacol 2006, 546(1-3):36-9.
23. Jackson MP. Structure-function analyses of Shiga toxin and the Shiga-like toxins. Microb Pathog 1990, 8(4):235-42.
24. Janisiewicz WJ, Conway WS, Brown MW, Sapers GM, Fratamico P, Buchanan RL. Fate of Escherichia coli O157:H7 on fresh-cut apple tissue and its potential for transmission by fruit flies. Appl Environ Microbiol 1999, 65(1):1-5.
25. Juneja VK, Bari ML, Inatsu Y, Kawamoto S, Friedman M. Thermal destruction of Escherichia coli O157:H7 in sous-vide cooked ground beef as affected by tea leaf and apple skin powders. J Food Prot 2009, 72(4):860-5.
26. Kenney SJ, Burnett SL, Beuchat LR. Location of Escherichia coli O157:H7 on and in apples as affected by bruising, washing, and rubbing. J Food Prot 2001, 64:1328-33.
27. Kitov PI, Lipinski T, Paszkiewicz E, Solomon D, Sadowska JM, Grant GA, Mulvey GL, Kitova EN, Klassen JS, Armstrong GD, Bundle DR. An entropically efficient supramolecular inhibition strategy for Shiga toxins. Angew Chem Int Ed 2008a, 47(4):672-6.
28. Kitov PI, Mulvey GL, Griener TP, Lipinski T, Solomon D, Paszkiewicz E, Jacobson JM, Sadowska JM, Suzuki M, Yamamura K-I, Armstrong GD, Bundle DR. In vivo supramolecular templating enhances the activity of multivalent ligands: a potential therapeutic against the Escherichia coli O157 AB5 toxins. Proc Natl Acad Sci USA 2008b, 105(44):16837-42.
29. Kondo F, Saito H, Hayashi R, Onda H, Kobayashi S, Matsumoto M, Suzuki M, Ito Y, Oka H, Nakanishi T, Shimizu A. Identification of Shiga toxins in Shiga toxin-producing Escherichia coli using immunoprecipitation and high-performance liquid chromatography-electrospray ionization mass spectrometry. Analyst 2003, 128(11):1360-4.
30. Koodie L, Dhople AM. Acid tolerance of Escherichia coli O157:H7 and its survival in apple juice. Microbios 2001, 104(409):167-75.
31. Krautz-Peterson G, Chapman-Bonofiglio S, Boisvert K, Feng H, Herman IM, Tzipori S, Sheoran AS. Intracellular neutralization of Shiga toxin 2 by an A subunit-specific human monoclonal antibody. Infect Immun 2008, 76(5):1931-9.
32. Liao CH, Sapers GM. Attachment and growth of Salmonella Chester on apple fruits and in vivo response of attached bacteria to sanitizer treatments. J Food Prot 2000, 63(7):876-83.
33. Ma Y, Mao X, Li J, Li H, Feng Y, Chen H, Luo P, Gu J, Yu S, Zeng H, Guo G, Yang K, Zou Q. Engineering an anti-Stx2 antibody to control severe infections of EHEC O157:H7. Immunol Lett 2008, 121(2):110-5.
34. Mehmood Z, Zeb A, Ayub M, Bibi N, Badshah A, Ihsanullah Effect of pasteurization and chemical preservatives on the quality and shelf stability of apple juice. Am J Food Technol 2008, 3(2):147-53.
35. Murdoch SJ, Wolfbauer G, Kennedy H, Marcovina SM, Carr MC, Albers JJ. Differences in reactivity of antibodies to active versus inactive PLTP significantly impacts PLTP measurement. J Lipid Res 2002, 43(2):281-9.
36. Parish ME. Public health and nonpasteurized fruit juices. Crit Rev Microbiol 1997, 23(2):109-19.
37. Parish ME. Coliforms, Escherichia coli and Salmonella serovars associated with a citrus-processing facility implicated in a salmonellosis outbreak. J Food Prot 1998, 61(3):280-4.
38. Quiñones B, Massey S, Friedman M, Swimley MS, Teter K. Novel cell-based method to detect Shiga toxin 2 from Escherichia coli O157:H7 and inhibitors of toxin activity. Appl Environ Microbiol 2009, 75(5):1410-6.
39. Rasooly R, Balaban N. Trypanosome microtubule-associated protein p15 as a vaccine for the prevention of African sleeping sickness. Vaccine 2004, 22(8):1007-15.
40. Rasooly R, Do PM. Development of an in vitro activity assay as an alternative to the mouse bioassay for Clostridium botulinum neurotoxin type A. Appl Environ Microbiol 2008, 74(14):4309-13.
41. Rasooly R, Do PM. In vitro cell-based assay for activity analysis of staphylococcal enterotoxin A in food. FEMS Immunol Med Microbiol 2009, 56(2):172-8.
42. Rasooly R, Do PM. Shiga toxin Stx2 is heat-stable and not inactivated by pasteurization. Int J Food Microbiol 2010, 136(3):290-4.
43. Rasooly R, Do PM, Friedman M. Inhibition of biological activity of Staphylococcal Enterotoxin A (SEA) by apple juice and apple polyphenols. J Agric Food Chem 2010, 58(9):5421-6.
44. Rasooly R, Stanker LH, Carter JM, Do PM, Cheng LW, He X, Brandon DL. Detection of botulinum neurotoxin-A activity in food by peptide cleavage assay. Int J Food Microbiol 2008, 126(1-2):135-9.
45. Riordan DC, Sapers GM, Hankinson TR, Magee M, Mattrazzo AM, Annous BA. A study of U.S. orchards to identify potential sources of Escherichia coli O157:H7. J Food Prot 2001, 64(9):1320-7.
46. Roering AM, Luchansky JB, Ihnot AM, Ansay SE, Kaspar CW, Ingham SC. Comparative survival of Salmonella typhimurium DT 104, Listeria monocytogenes, and Escherichia coli O157:H7 in preservative-free apple cider and simulated gastric fluid. Int J Food Microbiol 1999, 46(3):263-9.
47. Saenz JB, Doggett TA, Haslam DB. Identification and characterization of small molecules that inhibit intracellular toxin transport. Infect Immun 2007, 75(9):4552-61.
48. Sekino T, Kiyokawa N, Taguchi T, Takenouchi H, Matsui J, Tang WR, Suzuki T, Nakajima H, Saito M, Ohmi K, Katagiri YU, Okita H, Nakao H, Takeda T, Fujimoto J. Characterization of a Shiga-toxin 1-resistant stock of Vero cells. Microbiol Immunol 2004, 48(5):377-87.
49. Sirk TW, Brown EF, Sum AK, Friedman M. Molecular dynamics study on the biophysical interactions of seven green tea catechins with lipid bilayers of cell membranes. J Agric Food Chem 2008, 56(17):7750-8.
50. Sirk TW, Brown EF, Friedman M, Sum AK. Molecular binding of catechins to biomembranes: relationship to biological activity. J Agric Food Chem 2009, 57(15):6720-8.
51. Smith JL, Fratamico PM. Diarrhea-inducing Escherichia coli. Foodborne pathogens: microbiology and molecular biology 2005, 357-82. Fratamico PM, Bhunia AKSmith JL. editors, Norfolk, U.K., Caister Academic Press, p
52. Steele BT, Murphy N, Rance CP. An outbreak of hemolytic uremic syndrome associated with ingestion of fresh apple juice. J Pediatr 1982, 101:963-5.
53. Stone E, Hirama T, Chen W, Soltyk AL, Brunton J, MacKenzie CR, Zhang J. A novel pentamer versus pentamer approach to generating neutralizers of verotoxin 1. Mol Immunol 2007, 44(9):2487-91.
54. Tu S-I, Golden M, Paoli G, Gore M, Gehring A. Time-resolved fluorescence detection of shiga-like toxins produced by Escherichia coli O157 and non-O157 in ground beef. J Rapid Meth Autom Microbiol 2004, 12(4):247-58.
55. Vojdani JD, Beuchat LR, Tauxe RV. Juice-associated outbreaks of human illness in the United States, 1995 through 2005. J Food Prot 2008, 71(2):356-64.
56. Weeratna RD, Doyle MP. Detection and production of sertoxin 1 of Escherichia coli O157:H7 in food. Appl Environ Microbiol 1991, 57(10):2951-5.
57. Yamada Y, Miura Y, Sakaki A, Yoshida T, Kobayashi K. Design of multifunctional peptides expressing both antimicrobial activity and Shiga toxin neutralization activity. Bioorg Med Chem 2006, 14(1):77-82.