Food Science and Biotechnology

Korean Society of Food Science and Technology (한국식품과학회)
권호 표지

Parasporin-4, A Novel Cancer Cell-killing Protein Produced by Bacillus thuringiensis

  • Published : 2008.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

Bacillus thuringiensis was isolated as a pathogen of the sotto disease of silkmoth larvae about a hundred years ago. Since then, this bacterium has attracted attentions of not only insect pathologists but also many other scientists who are interested in its strong and specific insecticidal activity. This has led to the recent worldwide development of B. thuringiensis-based microbial insecticides and insect-resistant transgenic plants, as well as a landmark discovery of par asp orin, a cancer cell-specific cytotoxin produced by B. thuringiensis. In this review, we describe examination of interaction between inclusion proteins of B. thuringiensis and brush border membrane of insects using a surface plasmon resonance-based biosensor, identification and characterization of parasporin-4, the latest parasporin produced by the B. thuringiensis A1470 strain, and an effective method for preparing the parasporin-4 from inclusion bodies expressed in the recombinant Escherichia coli cells.

Keywords

References

  1. Ishiwata S. On a kind of severe flacherie (sotto disease). I. Dainihon Sanshi Kaiho, Report of the Sericultural Association of Japan. 114: 1-5 (1901)
  2. Federici BA. Insecticidal bacteria: An overwhelming success for invertebrate pathology. J. Invertebr. Pathol. 89: 30-38 (2005)
  3. Gill SS, Cowles EA, Pietrantonio PV. The mode of action of Bacillus thuringiensis endotoxins. Annu. Rev. Entomol. 37: 615-636 (1992) https://doi.org/10.1146/annurev.en.37.010192.003151
  4. Hofte H, Whiteley HR. Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol. Rev. 53: 242-255 (1989)
  5. Beegle CC, Yamamoto T. History of Bacillus thuringiensis Berliner research and development. Can. Entomol. 124: 587-616 (1992) https://doi.org/10.4039/Ent124587-4
  6. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. R. 62: 775-806 (1998)
  7. Bacillus thuringiensis ${\delta}-endotoxin$ Nomenclature Committee. Bacillus thuringiensis Toxin Nomenclature. Available from: http://www.lifesci.sussex.ac.uk/home/Neil_Crickmore/Bt/. Accessed Apr. 2, 2008
  8. Ohba M. Bacillus thuringiensis populations naturally occurring on mulberry leaves: A possible source of the populations associated with silkworm-rearing insectaries. J. Appl. Microbiol. 80: 56-64 (1996) https://doi.org/10.1111/j.1365-2672.1996.tb03190.x
  9. Mizuki E, Ohba M, Akao T, Yamashita S, Saitoh H, Park YS. Unique activity associated with non-insecticidal Bacillus thuringiensis parasporal inclusions: In vitro cell-killing action on human cancer cells. J. Appl. Microbiol. 86: 477-486 (1999) https://doi.org/10.1046/j.1365-2672.1999.00692.x
  10. Mizuki E, Park YS, Saitoh H, Yamashita S, Akao T, Higuchi K, Ohba M. Parasporin, human leukemic cell-recognizing parasporal protein of Bacillus thuringiensis. Clin. Diagn. Lab. Immun. 7: 625-634 (2000)
  11. Lee D-W, Akao T, Yamashita S, Katayama H, Maeda M, Saitoh H, Mizuki E, Ohba M. Noninsecticidal parasporal proteins of a Bacillus thuringiensis serovar shandongiensis isolate exhibit a preferential cytotoxicity against human leukemic T cells. Biochem. Bioph. Res. Co. 272: 218-223 (2000) https://doi.org/10.1006/bbrc.2000.2765
  12. Okumura S, Akao T, Higuchi K, Saitoh H, Mizuki E, Ohba M, Inouye K. Bacillus thuringiensis serovar shandongiensis strain 89-T- 34-22 produces multiple cytotoxic proteins with similar molecular masses against human cancer cells. Lett. Appl. Microbiol. 39: 89-92 (2004) https://doi.org/10.1111/j.1472-765X.2004.01544.x
  13. Okumura S, Saitoh H, Ishikawa T, Wasano N, Yamashita S, Kusumoto K, Akao T, Mizuki E, Ohba M, Inouye K. Identification of a novel cytotoxic protein, Cry45Aa, from Bacillus thuringiensis A1470 strain and its selective cytotoxic activity against various mammalian cell lines. J. Agr. Food Chem. 53: 6313-6318 (2005) https://doi.org/10.1021/jf0506129
  14. Committee of parasporin classification and nomenclature. Parasporin Classification and Nomenclature. Available from: http:// parasporin.fitc.pref.fukuoka.jp/. Accessed Apr. 2, 2008
  15. Okumura S, Akao T, Mizuki E, Ohba M, Inouye K. Screening of the Bacillus thuringiensis Cry1Ac ${\delta}-endotoxin$ on the artificial phospholipid monolayer incorporated with brush border membrane vesicles of Plutella xylostella by optical biosensor technology. J. Biochem. Bioph. Meth. 47: 177-188 (2001) https://doi.org/10.1016/S0165-022X(00)00134-2
  16. Okumura S, Saitoh H, Wasano N, Katayama H, Higuchi K, Mizuki E, Inouye K. Efficient solubilization, activation, purification of recombinant Cry45Aa of Bacillus thuringiensis expressed as inclusion bodies in Escherichia coli. Protein Expres. Purif. 47: 144-151 (2006) https://doi.org/10.1016/j.pep.2005.10.011
  17. Masson L, Mazza A, Brousseau R. Stable immobilization of lipid vesicles for kinetic studies using surface plasmon resonance. Anal. Biochem. 218: 405-412 (1994) https://doi.org/10.1006/abio.1994.1199
  18. Yang G, Kang S. SPR-based antibody-antigen interaction for real time analysis of carbamate pesticide residues. Food Sci. Biotechnol. 17: 15-19 (2008)
  19. Garczynski SF, Crim JW, Adang MJ. Identification of putative insect brush border membrane-binding molecules specific to Bacillus thuringiensis ${\delta}-endotoxin$ by protein blot analysis. Appl. Environ. Microb. 57: 2816-2820 (1991)
  20. Masson L, Mazza A, Brousseau R, Tabashnik B. Kinetics of Bacillus thuringiensis toxin binding with brush border membrane vesicles from susceptible and resistant larvae of Plutella xylostella. J. Biol. Chem. 270: 11887-11896 (1995) https://doi.org/10.1074/jbc.270.20.11887
  21. Luo K, Sangadala S, Masson L, Mazza A, Brousseau R, Adang MJ. The Heliothis virescens 170 kDa aminopeptidase functions as 'Receptor A' by mediating specific Bacillus thuringiensis Cry1Ac ${\delta}-endotoxin$ binding and pore formation. Insect Biochem. Molec. 27: 735-743 (1997) https://doi.org/10.1016/S0965-1748(97)00052-0
  22. Cooper MA, Carroll J, Travis ER, Williams DH, Ellar DJ. Bacillus thuringiensis Cry1Ac toxin interaction with Manduca sexta aminopeptidase N in a model membrane environment. Biochem. J. 333: 677-683 (1998) https://doi.org/10.1042/bj3330677
  23. Wolfersberger M, Luethy P, Maurer A, Parenti P, Sacchi FV, Giordana B, Hanozet GM. Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the cabbage butterfly. Comp. Biochem. Phys. A 86: 301-308 (1987) https://doi.org/10.1016/0300-9629(87)90334-3
  24. Kunitake T, Okahata Y, Tawaki S. Bilayer characteristics of 1,3- dialkyl- and 1,3-diacyl-rac-glycero-2-phosphocholines. J. Colloid. Interf. Sci. 103: 190-201 (1985) https://doi.org/10.1016/0021-9797(85)90091-8
  25. Adang MJ, Staver MJ, Rocheleau TA, Leighton J, Barker RF, Thompson DV. Characterized full-length and truncated plasmid clones of the crystal protein of Bacillus thuringiensis subsp. kurstaki HD-73 and their toxicity to Manduca sexta. Gene 36: 289-300 (1985) https://doi.org/10.1016/0378-1119(85)90184-2
  26. Mendelsohn M, Kough J, Vaituzis Z, Matthews K. Are Bt crops safe? Nat. Biotechnol. 21: 1003-1009 (2003) https://doi.org/10.1038/nbt0903-1003
  27. Kim J-H, Jee S-M, Park C-S, Kim H-Y. Detection of transgenic rice containing Cry1Ac gene derived from Bacillus thuringiensis by PCR. Food Sci. Biotechnol. 15: 625-630 (2006)
  28. Masson L, Lu Y, Mazza A, Brousseau R, Adang MJ. The Cry1Ac receptor purified from Manduca sexta displays multiple specificities. J. Biol. Chem. 270: 20309-20315 (1995) https://doi.org/10.1074/jbc.270.35.20309
  29. Knowles BH, Ellar DJ. Colloid-osmotic lysis is a general feature of the mechanism of action of Bacillus thuringiensis ${\delta} -endotoxins$ with different insect specificities. Biochim. Biophys. Acta 924: 509-518 (1987) https://doi.org/10.1016/0304-4165(87)90167-X
  30. Ballester V, Escriche B, Mensura JL, Riethmacher GW, Ferre J. Lack of cross-resistance to other Bacillus thuringiensis crystal proteins in a population of Plutella xylostella highly resistance to Cry1Ab. Biocontrol Sci. Techn. 4: 437-443 (1994) https://doi.org/10.1080/09583159409355354
  31. Tabashnik BE, Finson N, Groeters FR, Moar WJ, Johnson MW, Luo K, Adang MJ. Reversal of resistance to Bacillus thuringiensis in Plutella xylostella. P. Natl. Acad. Sci. USA 91: 4120-4124 (1994) https://doi.org/10.1073/pnas.91.10.4120
  32. Wright DJ, Iqubal M, Granero F, Ferre J. A change in a single midgut receptor in the diamondback moth (Plutella xylostella) is only in part responsible for field resistance to Bacillus thuringiensis subsp kurstaki and B thuringiensis subsp aizawai. Appl. Environ. Microb. 63: 1814-1819 (1997)
  33. Ballester V, Granero F, Tabashnik BE, Malvar T, Ferre J. Integrative model for binding of Bacillus thuringiensis toxins in susceptible and resistant larvae of the diamondback moth (Plutella xylostella). Appl. Environ. Microb. 65: 1413-1419 (1999)
  34. Inouye K, Lee S-B, Tonomura B. Effect of amino acid residues at the cleavable site of substrates on the remarkable activation of thermolysin by salts. Biochem. J. 315: 133-138 (1996) https://doi.org/10.1042/bj3150133
  35. Inouye K, Lee S-B, Nambu K, Tonomura B. Effects of pH, temperature, alcohols on the remarkable activation of thermolysin by salts. J. Biochem.-Tokyo 122: 358-364 (1997) https://doi.org/10.1093/oxfordjournals.jbchem.a021761
  36. Oneda H, Inouye K. Refolding and recovery of recombinant human matrix metalloproteinase 7 (matrilysin) from inclusion bodies expressed by Escherichia coli. J. Biochem.-Tokyo 126: 905-911 (1999) https://doi.org/10.1093/oxfordjournals.jbchem.a022533
  37. Inouye K, Tanaka H, Oneda H. States of tryptophyl residues and stability of recombinant human matrix metalloproteinase 7 (matrilysin) as examined by fluorescence. J. Biochem.-Tokyo 128: 363-369 (2000) https://doi.org/10.1093/oxfordjournals.jbchem.a022762
  38. Lee D-W, Katayama H, Akao T, Maeda M, Tanaka R, Yamashita S, Saitoh H, Mizuki E, Ohba M. A 28 kDa protein of the Bacillus thuringiensis serovar shandongiensis isolate 89-T-34-22 induces a human leukemic cell-specific cytotoxicity. Biochim. Biophys. Acta 1547: 57-63 (2001) https://doi.org/10.1016/S0167-4838(01)00169-8
  39. Crickmore N, Zeigler DR, Feitelson J, Schnepf E, Van Rie J, Lereclus D, Baum J, Dean DH. Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol. Mol. Biol. R. 62: 807-813 (1998)
  40. Jung YC, Mizuki E, Akao T, Cote JC. Isolation and characterization of a novel Bacillus thuringiensis strain expressing a novel crystal protein with cytocidal activity against human cancer cells. J. Appl. Microbiol. 103: 65-79 (2007) https://doi.org/10.1111/j.1365-2672.2006.03260.x
  41. Uemori A, Maeda M, Yasutake K, Ohgushi A, Kagoshima K, Mizuki E, Ohba M. Ubiquity of parasporin-1 producers in Bacillus thuringiensis natural populations of Japan. Naturwissenschaften 94: 34-38 (2007) https://doi.org/10.1007/s00114-006-0153-7
  42. Yasutake K, Binh ND, Kagoshima K, Uemori A, Ohgushi A, Maeda M, Mizuki E, Yu YM, Ohba M. Occurrence of parasporinproducing Bacillus thuringiensis in Vietnam. Can. J. Microbiol. 52: 365-372 (2006) https://doi.org/10.1139/W05-134
  43. Ito A, Sasaguri Y, Kitada S, Kusaka Y, Kuwano K, Masutomi K, Mizuki E, Akao T, Ohba M. A Bacillus thuringiensis crystal protein with selective cytocidal action to human cells. J. Biol. Chem. 279: 21282-21286 (2004) https://doi.org/10.1074/jbc.M401881200
  44. Hayakawa T, Kanagawa R, Kotani Y, Kimura M, Yamagiwa M, Yamane Y, Takebe S, Sakai H. Parasporin-2Ab, a newly isolated cytotoxic crystal protein from Bacillus thuringiensis. Curr. Microbiol. 55: 278-283 (2007) https://doi.org/10.1007/s00284-006-0351-8
  45. Yamashita S, Katayama H, Saitoh H, Akao T, Park YS, Mizuki E, Ohba M, Ito A. Typical three-domain Cry proteins of Bacillus thuringiensis strain A1462 exhibit cytocidal activity on limited human cancer cells. J. Biochem.-Tokyo 138: 663-672 (2005) https://doi.org/10.1093/jb/mvi177
  46. Hardy SP, Lund T, Granum PE. CytK toxin of Bacillus cereus forms pores in planar lipid bilayers and is cytotoxic to intestinal epithelia. FEMS Microbiol. Lett. 197: 47-51 (2001) https://doi.org/10.1111/j.1574-6968.2001.tb10581.x
  47. Raimondi F, Kao JP, Fiorentini C, Fabbri A, Donelli G, Gasparini N, Rubino A, Fasano A. Enterotoxicity and cytotoxicity of Vibrio parahaemolyticus thermostable direct hemolysin in in vitro systems. Infect. Immun. 68: 3180-3185 (2000) https://doi.org/10.1128/IAI.68.6.3180-3185.2000
  48. Kothary MH, Delston RB, Curtis SK, McCardell BA, Tall BD. Purification and characterization of a vulnificolysin-like cytolysin produced by Vibrio tubiashii. Appl. Environ. Microb. 67: 3707-3711 (2001) https://doi.org/10.1128/AEM.67.8.3707-3711.2001
  49. $Pr\"{u}{ss}$ BM, Dietrich R, Nibler B, M$Pr\"{a}$rtlbauer E, Scherer S. The hemolytic enterotoxin HBL is broadly distributed among species of the Bacillus cereus group. Appl. Environ. Microb. 65: 5436-5442 (1999)
  50. Lee NA, Chang H-G, Kim HP, Kim HS, Park JH. Toxicity of 5 Bacillus cereus enterotoxins in human cell lines and mice. Food Sci. Biotechnol. 15: 458-461 (2006)
  51. Yang CY, Pang JC, Kao SS, Tsen HY. Enterotoxigenicity and cytotoxicity of Bacillus thuringiensis strains and development of a process for Cry1Ac production. J. Agr. Food Chem. 51: 100-105 (2003) https://doi.org/10.1021/jf025863l
  52. Koller CN, Bauer LS, Hollingworth RM. Characterization of the pH-mediated solubility of Bacillus thuringiensis var. san diego native ${\delta}-endotoxin$ crystals. Biochem. Bioph. Res. Co. 184: 692-699 (1992) https://doi.org/10.1016/0006-291X(92)90645-2
  53. Kopito RR. Aggresomes, inclusion bodies, and protein aggregation. Trends Cell Biol. 10: 524-530 (2000) https://doi.org/10.1016/S0962-8924(00)01852-3
  54. Schein CH. Solubility as a function of protein structure and solvent components. Bio-Technol. 8: 308-317 (1990) https://doi.org/10.1038/nbt0490-308
  55. Yon JM. The specificity of protein aggregation. Nat. Biotechnol. 14: 1231 (1996) https://doi.org/10.1038/nbt1096-1231
  56. Gustafson ME, Clayton RA, Lavrik PB, Johnson GV, Leimgruber RM, Sims SR, Bartnicki DE. Large-scale production and characterization of Bacillus thuringiensis subsp tenebrionis insecticidal protein from Escherichia coli. Appl. Microbiol. Biot. 47: 255-261 (1997) https://doi.org/10.1007/s002530050923
  57. Boonserm P, Pornwiroon W, Katzenmeier G, Panyim S, Angsuthanasombat C. Optimised expression in Escherichia coli and purification of the functional form of the Bacillus thuringiensis Cry4Aa ${\delta}-endotoxin$. Protein Expres. Purif. 35: Protein Expres. Purif.(2004)
  58. Kondo S, Mizuki E, Akao T, Ohba M. Antitrichomonal strains of Bacillus thuringiensis. Parasitol. Res. 88: 1090-1092 (2002) https://doi.org/10.1007/s00436-002-0692-6
  59. Akao T, Mizuki E, Yamashita S, Saitoh H, Ohba M. Lectin activity of Bacillus thuringiensis parasporal inclusion proteins. FEMS Microbiol. Lett. 179: 415-421 (1999) https://doi.org/10.1111/j.1574-6968.1999.tb08757.x
  60. Sanchis V, Chafaux J, Lereclus, D. Amélioration biotechnologique de Bacillus thuringiensis: Les enjeux et les risques. (Biotechnological improvement of Bacillus thuringiensis: Stakes and risks.) Ann. Inst. Pasteur Actual. 7: 271-284 (1996) https://doi.org/10.1016/S0924-4204(97)86395-0