Cry1Ab Treatment Has No Effects on Viability of Cultured Porcine Intestinal Cells, but Triggers Hsp70 Expression

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Bondzio, Angelika ^a   Lodemann, Ulrike ^a   Weise, Christoph ^a   Einspanier, Ralf ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CRY1AB TOXIN; HEAT SHOCK PROTEIN 70; LACTATE DEHYDROGENASE; POTASSIUM IONOPHORE; VALINOMYCIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL PROLIFERATION; CELL TYPE; CELL VIABILITY; CYTOTOXICITY; ELECTRIC RESISTANCE; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME RELEASE; GEL ELECTROPHORESIS; IN VITRO STUDY; INTESTINE CELL; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; RISK ASSESSMENT; STRESS; UPREGULATION; WESTERN BLOTTING;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; ELECTRIC IMPEDANCE; ENDOTOXINS; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEMOLYSIN PROTEINS; HSP70 HEAT-SHOCK PROTEINS; INTESTINAL MUCOSA; IONOPHORES; L-LACTATE DEHYDROGENASE; PLANTS, GENETICALLY MODIFIED; SWINE; VALINOMYCIN; ZEA MAYS;

MAMMALIA; SUS; ZEA MAYS;

EID: 84879823483     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067079     Document Type: Article

References (66)

1. Romeis J, Meissle M, Bigler F, (2006) Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24: 63-71.
2. Bendiek J, Grohmann L, (2006) GVO-Kontrolle von Lebensmitteln, Futtermitteln und Saatgut: eine bundesweite Übersicht. J of Consumer Protection and Food Safety 1: 241-245.
3. Kilic A, Akay MT, (2008) A three generation study with genetically modified Bt corn in rats: Biochemical and histopathological investigation. Food Chem Toxicol 46: 1164-1170.
4. de Vendomois JS, Roullier F, Cellier D, Seralini GE, (2009) A comparison of the effects of three GM corn varieties on mammalian health. Int J Biol Sci 5: 706-726.
5. Finamore A, Roselli M, Britti S, Monastra G, Ambra R, et al. (2008) Intestinal and peripheral immune response to MON810 maize ingestion in weaning and old mice. J Agric Food Chem 56: 11533-11539.
6. Sagstad A, Sanden M, Haugland O, Hansen AC, Olsvik PA, et al. (2007) Evaluation of stress- and immune-response biomarkers in Atlantic salmon, Salmo salar L., fed different levels of genetically modified maize (Bt maize), compared with its near-isogenic parental line and a commercial suprex maize. J Fish Dis 30: 201-212.
7. Walsh MC, Buzoianu SG, Gardiner GE, Rea MC, Gelencser E, et al. (2011) Fate of transgenic DNA from orally administered Bt MON810 maize and effects on immune response and growth in pigs. PLoS One 6 (11): e27177.
8. Hug K, (2008) Genetically modified organisms: do the benefits outweigh the risks? Medicina (Kaunas) 44: 87-99.
9. Heinemann JA, Kurenbach B, Quist D, (2011) Molecular profiling-a tool for addressing emerging gaps in the comparative risk assessment of GMOs. Environ Int 37: 1285-1293.
10. EFSA (2010) Scientific opinion on the assessment of allergenicity of GM plants and microorganisms and derived food and feed. EFSA Journal 8: 1699.
11. von Kries C, Winter G, (2012) The structuring of GMO release and evaluation in EU law. Biotechnol J 7: 569-581.
12. Luber-Narod J, Smith B, Grant W, Jimeno JM, Lopez-Lazaro L, et al. (2001) Evaluation of the use of in vitro methodologies as tools for screening new compounds for potential in vivo toxicity. Toxicol In Vitro 15: 571-577.
13. Shimada N, Kim YS, Miyamoto K, Yoshioka M, Murata H, (2003) Effects of Bacillus thuringiensis Cry1Ab toxin on mammalian cells. J Vet Med Sci 65: 187-191.
14. Mesnage R, Clair E, Gress S, Then C, Szekacs A, et al. (2012) Cytotoxicity on human cells of Cry1Ab and Cry1Ac Bt insecticidal toxins alone or with a glyphosate-based herbicide. J Appl Toxicol 33(7): 695-699.
15. Paul V, Guertler P, Wiedemann S, Meyer HH, (2010) Degradation of Cry1Ab protein from genetically modified maize (MON810) in relation to total dietary feed proteins in dairy cow digestion. Transgenic Res 19: 683-689.
16. Phipps RH, Deaville ER, Maddison BC, (2003) Detection of transgenic and endogenous plant DNA in rumen fluid, duodenal digesta, milk, blood, and feces of lactating dairy cows. J Dairy Sci 86: 4070-4078.
17. Lutz B, Wiedemann S, Einspanier R, Mayer J, Albrecht C, (2005) Degradation of Cry1Ab protein from genetically modified maize in the bovine gastrointestinal tract. J Agric Food Chem 53: 1453-1456.
18. Chowdhury EH, Shimada N, Murata H, Mikami O, Sultana P, et al. (2003) Detection of Cry1Ab protein in gastrointestinal contents but not visceral organs of genetically modified Bt11-fed calves. Vet Hum Toxicol 45: 72-75.
19. Shimada N, Miyamoto K, Kanda K, Murata H, (2006) Bacillus thuringiensis insecticidal Cry1ab toxin does not affect the membrane integrity of the mammalian intestinal epithelial cells: An in vitro study. In Vitro Cell Dev Biol Anim 42: 45-49.
20. Stumpff F, Bondzio A, Einspanier R, Martens H, (2007) Effects of the Bacillus thuringiensis toxin Cry1Ab on membrane currents of isolated cells of the ruminal epithelium. J Membr Biol 219: 37-47.
21. Bondzio A, Stumpff F, Schon J, Martens H, Einspanier R, (2008) Impact of Bacillus thuringiensis toxin Cry1Ab on rumen epithelial cells (REC)- a new in vitro model for safety assessment of recombinant food compounds. Food Chem Toxicol 46: 1976-1984.
22. Schierack P, Nordhoff M, Pollmann M, Weyrauch KD, Amasheh S, et al. (2006) Characterization of a porcine intestinal epithelial cell line for in vitro studies of microbial pathogenesis in swine. Histochem Cell Biol 125: 293-305.
23. Cencic A, Langerholc T, (2010) Functional cell models of the gut and their applications in food microbiology-a review. Int J Food Microbiol 141Suppl 1: 4-14.
24. Nguyen Thu H, Meise T, Langenbruch GA, Jehle JA, (2004) Production of Cry1Ab toxin in E. coli for standardisation of insect bioassays. IOBC/WPRS Bulletin 27: 125-130.
25. Jehle JA (2007) Production of a Bt toxin standard and development of a measuring procedure to assess the amount of the toxin in Bt maize. Available: http://wwwgmo-safetyeu. Accessed 16. May 2007.
26. Devriendt B, Stuyven E, Verdonck F, Goddeeris BM, Cox E, (2010) Enterotoxigenic Escherichia coli (K88) induce proinflammatory responses in porcine intestinal epithelial cells. Dev Comp Immunol 34: 1175-1182.
27. Nunez-Valdez M, Sanchez J, Lina L, Guereca L, Bravo A, (2001) Structural and functional studies of alpha-helix 5 region from Bacillus thuringiensis Cry1Ab delta-endotoxin. Biochim Biophys Acta 1546: 122-131.
28. EFSA (2008) Safety and nutritional assessment of GM plants and derived food and feed: the role of animal feeding trials. Food Chem Toxicol 46Suppl 1: 2-70.
29. Niles AL, Moravec RA, Riss TL, (2009) In vitro viability and cytotoxicity testing and same-well multi-parametric combinations for high throughput screening. Curr Chem Genomics 3: 33-41.
30. Vistejnova L, Dvorakova J, Hasova M, Muthny T, Velebny V, et al. (2009) The comparison of impedance-based method of cell proliferation monitoring with commonly used metabolic-based techniques. Neuro Endocrinol Lett 30Suppl 1: 121-127.
31. Ke N, Wang X, Xu X, Abassi YA, (2011) The xCELLigence system for real-time and label-free monitoring of cell viability. Methods Mol Biol 740: 33-43.
32. Urcan E, Haertel U, Styllou M, Hickel R, Scherthan H, et al. (2010) Real-time xCELLigence impedance analysis of the cytotoxicity of dental composite components on human gingival fibroblasts. Dent Mater 26: 51-58.
33. Starsichova A, Kubala L, Lincova E, Pernicova Z, Kozubik A, et al. (2009) Dynamic Monitoring of Cellular Remodeling Induced by the Transforming Growth Factor-beta1. Biol Proced Online 11: 316-324.
34. Inai Y, Yabuki M, Kanno T, Akiyama J, Yasuda T, et al. (1997) Valinomycin induces apoptosis of ascites hepatoma cells (AH-130) in relation to mitochondrial membrane potential. Cell Struct Funct 22: 555-563.
35. Dorsch JA, Candas M, Griko NB, Maaty WS, Midboe EG, et al. (2002) Cry1A toxins of Bacillus thuringiensis bind specifically to a region adjacent to the membrane-proximal extracellular domain of BT-R(1) in Manduca sexta: involvement of a cadherin in the entomopathogenicity of Bacillus thuringiensis. Insect Biochem Mol Biol 32: 1025-1036.
36. Gomez I, Sanchez J, Miranda R, Bravo A, Soberon M, (2002) Cadherin-like receptor binding facilitates proteolytic cleavage of helix alpha-1 in domain I and oligomer pre-pore formation of Bacillus thuringiensis Cry1Ab toxin. FEBS Lett 513: 242-246.
37. Gomez I, Arenas I, Benitez I, Miranda-Rios J, Becerril B, et al. (2006) Specific epitopes of domains II and III of Bacillus thuringiensis Cry1Ab toxin involved in the sequential interaction with cadherin and aminopeptidase-N receptors in Manduca sexta. J Biol Chem 281: 34032-34039.
38. Hua G, Jurat-Fuentes JL, Adang MJ, (2004) Bt-R1a extracellular cadherin repeat 12 mediates Bacillus thuringiensis Cry1Ab binding and cytotoxicity. J Biol Chem 279: 28051-28056.
39. Flannagan RD, Yu CG, Mathis JP, Meyer TE, Shi X, et al. (2005) Identification, cloning and expression of a Cry1Ab cadherin receptor from European corn borer, Ostrinia nubilalis (Hubner) (Lepidoptera: Crambidae). Insect Biochem Mol Biol 35: 33-40.
40. Bolkent S, Zierold K, (2002) Effects of the ionophores valinomycin, ionomycin and gramicidin A on the element compartmentation in cultured rat hepatocytes. Toxicol In Vitro 16: 159-165.
41. Marques-Santos LF, Coqueiro VM, Rumjanek VM, (2006) Cyclosporin A does not protect the disruption of the inner mitochondrial membrane potential induced by potassium ionophores in intact K562 cells. Cell Biol Int 30: 197-204.
42. Ryoo IJ, Park HR, Choo SJ, Hwang JH, Park YM, et al. (2006) Selective cytotoxic activity of valinomycin against HT-29 Human colon carcinoma cells via down-regulation of GRP78. Biol Pharm Bull 29: 817-820.
43. Tavaria M, Gabriele T, Kola I, Anderson RL, (1996) A hitchhiker's guide to the human Hsp70 family. Cell Stress Chaperones 1: 23-28.
44. Daugaard M, Rohde M, Jaattela M, (2007) The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Lett 581: 3702-3710.
45. Su CY, Chong KY, Owen OE, Dillmann WH, Chang C, et al. (1998) Constitutive and inducible hsp70s are involved in oxidative resistance evoked by heat shock or ethanol. J Mol Cell Cardiol 30: 587-598.
46. Ludwig D, Stahl M, Ibrahim ET, Wenzel BE, Drabicki D, et al. (1999) Enhanced intestinal expression of heat shock protein 70 in patients with inflammatory bowel diseases. Dig Dis Sci 44: 1440-1447.
47. Shi H, Hood KA, Hayes MT, Stubbs RS, (2011) Proteomic analysis of advanced colorectal cancer by laser capture microdissection and two-dimensional difference gel electrophoresis. J Proteomics 75: 339-351.
48. Mukhopadhyay I, Nazir A, Saxena DK, Chowdhuri DK, (2003) Heat shock response: hsp70 in environmental monitoring. J Biochem Mol Toxicol 17: 249-254.
49. Zhong X, Li W, Huang X, Zhang L, Yimamu M, et al. (2012) Impairment of cellular immunity is associated with overexpression of heat shock protein 70 in neonatal pigs with intrauterine growth retardation. Cell Stress Chaperones 17: 495-505.
50. Musch MW, Ciancio MJ, Sarge K, Chang EB, (1996) Induction of heat shock protein 70 protects intestinal epithelial IEC-18 cells from oxidant and thermal injury. Am J Physiol 270: C429-436.
51. Hartl FU, Hayer-Hartl M, (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852-1858.
52. Arya R, Mallik M, Lakhotia SC, (2007) Heat shock genes- integrating cell survival and death. J Biosci 32: 595-610.
53. Hoffmann F, Rinas U, (2004) Roles of heat-shock chaperones in the production of recombinant proteins in Escherichia coli. Adv Biochem Eng Biotechnol 89: 143-161.
54. Li CY, Lee JS, Ko YG, Kim JI, Seo JS, (2000) Heat shock protein 70 inhibits apoptosis downstream of cytochrome c release and upstream of caspase-3 activation. J Biol Chem 275: 25665-25671.
55. Lanneau D, Brunet M, Frisan E, Solary E, Fontenay M, et al. (2008) Heat shock proteins: essential proteins for apoptosis regulation. J Cell Mol Med 12: 743-761.
56. Dokladny K, Moseley PL, Ma TY, (2006) Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. Am J Physiol Gastrointest Liver Physiol 290: G204-212.
57. Akagi R, Ohno M, Matsubara K, Fujimoto M, Nakai A, et al. (2013) Glutamine protects intestinal barrier function of colon epithelial cells from ethanol by modulating Hsp70 expression. Pharmacology 91: 104-111.
58. Laubitz D, Jankowska A, Sikora A, Wolinski J, Zabielski R, et al. (2006) Gut myoelectrical activity induces heat shock response in Escherichia coli and Caco-2 cells. Exp Physiol 91: 867-875.
59. Hirata I, Naito Y, Handa O, Hayashi N, Mizushima K, et al. (2009) Heat-shock protein 70-overexpressing gastric epithelial cells are resistant to indomethacin-induced apoptosis. Digestion 79: 243-250.
60. Liang P, MacRae TH, (1997) Molecular chaperones and the cytoskeleton. J Cell Sci 110 (Pt 13): 1431-1440.
61. Omary MB, Ku NO, Liao J, Price D, (1998) Keratin modifications and solubility properties in epithelial cells and in vitro. Subcell Biochem 31: 105-140.
62. Windoffer R, Beil M, Magin TM, Leube RE, (2011) Cytoskeleton in motion: the dynamics of keratin intermediate filaments in epithelia. J Cell Biol 194: 669-678.
63. Ku NO, Toivola DM, Strnad P, Omary MB, (2010) Cytoskeletal keratin glycosylation protects epithelial tissue from injury. Nat Cell Biol 12: 876-885.
64. Chaudhury A, Chander P, Howe PH, (2010) Heterogeneous nuclear ribonucleoproteins (hnRNPs) in cellular processes: Focus on hnRNP E1's multifunctional regulatory roles. RNA 16: 1449-1462.
65. Bomsztyk K, Van Seuningen I, Suzuki H, Denisenko O, Ostrowski J, (1997) Diverse molecular interactions of the hnRNP K protein. FEBS Lett 403: 113-115.
66. Bomsztyk K, Denisenko O, Ostrowski J, (2004) hnRNP K: one protein multiple processes. Bioessays 26: 629-638.