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Influence of Reactive Oxygen Species Produced by Chlorine Dioxide on Induction of Insect Cell Apoptosis

이산화염소의 활성산소 유발에 따른 곤충 세포의 아폽토시스

  • Kim, Minhyun (Department of Bioresource Sciences, Andong National University) ;
  • Kumar, Sunil (Department of Bioresource Sciences, Andong National University) ;
  • Kwon, Hyeok (Department of Biosystems and Biotechnology, Korea University) ;
  • Kim, Wook (Department of Biosystems and Biotechnology, Korea University) ;
  • Kim, Yonggyun (Department of Bioresource Sciences, Andong National University)
  • 김민현 (안동대학교 식물의학과) ;
  • 수닐 쿠마르 (안동대학교 식물의학과) ;
  • 권혁 (고려대학교 바이오시스템공학과) ;
  • 김욱 (고려대학교 바이오시스템공학과) ;
  • 김용균 (안동대학교 식물의학과)
  • Received : 2016.06.27
  • Accepted : 2016.07.19
  • Published : 2016.09.01

Abstract

Chlorine dioxide has an insecticidal activity via its production of reactive oxygen species (ROS). Its cytotoxic activity has been regarded as a main cause of the insecticidal activity. This study tested a hypothesis that cytotoxicity of chlorine dioxide is resulted from its induction of apoptosis against target cells using ROS. Injection of chlorine dioxide significantly reduced total hemocyte counts of Plodia interpunctella larvae and subsequently killed the larvae. To analyze the cytotoxicity with respect to apoptosis, terminal deoxyribonucleotidyl transferase nick end translation (TUNEL) assay was performed. An insect cell line (Sf9) cells were exposed to different concentrations of chlorine dioxide. TUNEL assay showed that chlorine dioxide induced significant apoptosis of Sf9 cells in a dose-dependent manner. When different concentrations of chlorine dioxide were injected to larvae of P. interpunctella, it showed a dose-dependent induction of apoptosis against hemocytes. However, addition of vitamin E significantly suppressed the apoptosis induction and insecticidal activity of chlorine dioxide in a dose-dependent manner. These results suggest that cytotoxicity of chlorine dioxide is resulted from its induction of apoptosis against insect cells using ROS.

이산화염소는 살충효과를 지니며, 이는 이 물질이 발생시키는 활성산소에 기인된다. 살충효과를 주는 주요 원인으로 이산화염소의 세포독성에 주목하고 있다. 본 연구는 이산화염소가 유발하는 세포독성이 활성산소에 기인한 아폽토시스 유발로 가설을 세우고 이를 검증하였다. 화랑곡나방(Plodia interpunctella) 유충에 이산화염소를 주입한 결과 전체혈구수의 뚜렷한 감소를 보였고, 이후 처리 유충은 사망하였다. 아폽토시스 세포치사과정을 규명하기 위해 TUNEL (terminal deoxynucleotidyl transferase nick end translation) 분석법을 적용하였다. 곤충 세포주의 하나인 Sf9 세포에 서로 다른 이산화염소를 처리하고 TUNEL 분석법으로 관찰한 결과 처리 농도에 비례하여 아폽토시스 비율이 증가하였다. 다음으로 서로 다른 농도의 이산화염소를 화랑곡나방 유충에 주입하고 혈구 세포를 TUNEL 분석법으로 관찰한 결과 이산화염소는 처리 농도에 비례하여 아폽토시스 유발을 나타냈다. 그러나 항산화제인 비타민 E를 이산화염소와 함께 처리하면 비타민 E의 농도에 비례하여 이산화염소의 아폽토시스 유발을 억제하고 이에 따라 살충률도 감소하였다. 이러한 결과는 이산화염소에 기인한 세포독성은 활성산소에 기인한 아폽토시스 유발로 이뤄졌다는 것을 제시하고 있다.

Keywords

References

  1. Arur, S., Uche, U.E., Rezaul, K., Fong, M., Scranton, V., Cowan, A.E., Mohler, W., Han, D.K., 2003. Annexin I is an endogenous ligand that mediates apoptotic cell engulfment. Dev. Cell. 4, 587-598. https://doi.org/10.1016/S1534-5807(03)00090-X
  2. Ashkenazi, A., Dixit, V.M., 1998. Death receptors: signaling and modulation. Science 281, 1305-1308. https://doi.org/10.1126/science.281.5381.1305
  3. Bortner, C.D., Oldenburg, N.B., Cidlowski, J.A., 1995. The role of DNA fragmentation in apoptosis. Trends Cell Biol. 5, 21-26. https://doi.org/10.1016/S0962-8924(00)88932-1
  4. Bratton, D.L., Fadok, V.A., Richter, D.A., Kailey, J.M., Guthrie, L.A., Henson, P.M., 1997. Appearance of phosphatidylserine on apoptotic cells requires calcium-mediated nonspecific flip-flop and is enhanced by loss of the aminophospholipid translocase. J. Biol. Chem. 272, 26159-26165. https://doi.org/10.1074/jbc.272.42.26159
  5. Cai, J., Jones, D.P., 1998. Superoxide in apoptosis: mitochondrial generation triggered by cytochrome c loss. J. Biol. Chem. 273, 11401-11404. https://doi.org/10.1074/jbc.273.19.11401
  6. Chicheportiche, Y., Bourdon, P.R., Xu, H., Hsu, Y.M., Scott, H., Hession, C., Garcia, I., Browning, J.L., 1997. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J. Biol. Chem. 272, 32401-32410. https://doi.org/10.1074/jbc.272.51.32401
  7. Chinnaiyan, A.M., 1999. The apoptosome: heart and soul of the cell death machine. Neoplasia 1, 5-15. https://doi.org/10.1038/sj.neo.7900003
  8. Cohen, G.M., 1997. Caspases: the executioners of apoptosis. Biochem. J. 326, 1-16. https://doi.org/10.1042/bj3260001
  9. Cory, S., Adams, J.M., 2002. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2, 647-656. https://doi.org/10.1038/nrc883
  10. Don, G., 1998. The chlorine dioxide handbook. Am. Water Works Assoc. 3-4.
  11. Du, C., Fang, M., Li, Y., Li, L., Wang, X., 2000. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102, 33-42. https://doi.org/10.1016/S0092-8674(00)00008-8
  12. Elmore, S., 2007. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35, 495-516. https://doi.org/10.1080/01926230701320337
  13. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A., Nagata, S., 1998. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391, 43-50. https://doi.org/10.1038/34112
  14. Gavrieli, Y., Sherman, Y., Ben-Sasson, S.A., 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501. https://doi.org/10.1083/jcb.119.3.493
  15. Gardai, S.J., McPhillips, K.A., Frasch, S.C., Janssen, W.J., Starefeldt, A., Murphy-Ullrich, J.E., Bratton, D.L., Oldenborg, P.A., Michalak, M., Henson, P.M., 2005. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123, 321-334. https://doi.org/10.1016/j.cell.2005.08.032
  16. Garrido, C., Galluzzi, L., Brunet, M., Puig, P.E., Didelot, C., Kroemer, G., 2006. Mechanisms of cytochrome c release from mitochondria. Cell Death Differ. 13, 1423-1433. https://doi.org/10.1038/sj.cdd.4401950
  17. Gibbs, S.G., Lowe, J.J., Smith, P.W., Hewlett, A.L., 2012. Gaseous chlorine dioxide as an alternative for bedbug control. Infect. Control Hosp. Epidemiol. 33, 495-499. https://doi.org/10.1086/665320
  18. Herrera, E., Barbas, C., 2001. Vitamin E: action, metabolism and perspectives. J. Physiol. Biochem. 57, 43-56. https://doi.org/10.1007/BF03179812
  19. Hill, M.M., Adrain, C., Duriez, P.J., Creagh, E.M., Martin, S.J., 2004. Analysis of the composition, assembly kinetics and activity of native Apaf-1 apoptosomes. Embo J. 23, 2134-2145. https://doi.org/10.1038/sj.emboj.7600210
  20. Hinenoya, A., Awasthi, S.P., Yasuda, N., Shima, A., Morino, H., Koizumi, T., Fukuda, T., Miura, T., Shibata, T., Yamasaki, S., 2015. Chlorine dioxide is a better disinfectant than sodium hypochlorite against multi-drug resistant Staphylococcus aureus, Pseudomonas aeruginosa, and Acinetobacter baumannii. Jpn. J. Infect Dis. 68, 276-279 https://doi.org/10.7883/yoken.JJID.2014.294
  21. Hsu, H., Xiong, J., Goeddel, D.V., 1995. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81, 495-504. https://doi.org/10.1016/0092-8674(95)90070-5
  22. Joza, N., Susin, S.A., Daugas, E., Stanford, W.L., Cho, S.K., Li, C.Y., Sasaki, T., Elia, A.J., Cheng, H.Y., Ravagnan, L., Ferri, K.F., Zamzami, N., Wakeham, A., Hakem, R., Yoshida, H., Kong, Y.Y., Mak, T.W., Zuniga-Pflucker, J.C., Kroemer, G., Penninger, J.M., 2001. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410, 549-554. https://doi.org/10.1038/35069004
  23. Kataoka, T., Schroter, M., Hahne, M., Schneider, P., Irmler, M., Thome, M., Froelich, C.J. Tschopp, J., 1998. FLIP prevents apoptosis induced by death receptors but not by perforin/granzyme B, chemotherapeutic drugs, and gamma irradiation. J. Immunol. 161, 3936-3942.
  24. Kim, Y., Kumar, S., Cheon, W., Eo, H., Kwon, H., Jeon, Y., Jung, J., Kim, W., 2016. Anticancer and antiviral activity of chlorine dioxide by its induction of the reactive oxygen species. J. Appl. Biol. Chem. 59, 31-36. https://doi.org/10.3839/jabc.2016.007
  25. Kim, Y., Park, J., Kumar, S., Kwon, H., Na, J., Chun, Y., Kim, W., 2015. Insecticidal activity of chlorine dioxide gas by inducing an oxidative stress to the red flour beetle, Tribolium castaneum. J. Stored Prod. Res. 64, 88-96. https://doi.org/10.1016/j.jspr.2015.09.001
  26. Kischkel, F.C., Hellbardt, S., Behrmann, I., Germer, M., Pawlita, M., Krammer, P.H., Peter, M.E., 1995. Cytotoxicity-dependent APO-1 (Fas/CD95)- associated proteins form a death-inducing signaling complex (DISC) with the receptor. Embo J. 14, 5579-5588.
  27. Kothakota, S., Azuma, T., Reinhard, C., Klippel, A., Tang, J., Chu, K., McGarry, T.J., Kirschner, M.W., Koths, K., Kwiatkowski, D.J., Williams, L.T., 1997. Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278, 294-298. https://doi.org/10.1126/science.278.5336.294
  28. Kumar, S., Park, J., Kim, E., Na, J., Chun, Y.S., Kwon, H., Kim, W., Kim, Y., 2015. Oxidative stress induced by chlorine dioxide as an insecticidal factor to the Indian meal moth, Plodia interpunctella. Pestic. Biochem. Physiol. 124, 48-59. https://doi.org/10.1016/j.pestbp.2015.04.003
  29. Li, L.Y., Luo, X., Wang, X., 2001. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412, 95-99. https://doi.org/10.1038/35083620
  30. Locksley, R.M., Killeen, N., Lenardo, M.J., 2001. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104, 487-501. https://doi.org/10.1016/S0092-8674(01)00237-9
  31. Mates, J.M., Sanchez-Jimenez, F.M., 2000. Role of reactive oxygen species in apoptosis: implications for cancer therapy. Int. J. Biochem. Cell Biol. 32, 157-170. https://doi.org/10.1016/S1357-2725(99)00088-6
  32. Nemes, Z., Jr., Friis, R.R., Aeschlimann, D., Saurer, S., Paulsson, M., Fesus, L., 1996. Expression and activation of tissue transglutaminase in apoptotic cells of involuting rodent mammary tissue. Eur. J. Cell Biol. 70, 125-133.
  33. Norbury, C.J., Hickson, I.D., 2001. Cellular responses to DNA damage. Annu. Rev. Pharmacol. Toxicol. 41, 367-401. https://doi.org/10.1146/annurev.pharmtox.41.1.367
  34. Peter, M.E., Krammer, P.H., 1998. Mechanisms of CD95 (APO-1/Fas)-mediated apoptosis. Curr. Opin. Immunol. 10, 545-551. https://doi.org/10.1016/S0952-7915(98)80222-7
  35. Rai, N.K., Tripathi, K., Sharma, D., Shukla, V.K., 2005. Apoptosis: a basic physiologic process in wound healing. Int. J. Low Extrem. Wounds 4, 138-144. https://doi.org/10.1177/1534734605280018
  36. Rubio-Moscardo, F., Blesa, D., Mestre, C., Siebert, R., Balasas, T., Benito, A., Rosenwald, A., Climent, J., Martinez, J.I., Schilhabel, M., Karran, E.L., Gesk, S., Esteller, M., deLeeuw, R., Staudt, L.M., Fernandez-Luna, J.L., Pinkel, D., Dyer, M.J., Martinez-Climent, J.A., 2005. Characterization of 8p21.3 chromosomal deletions in B-cell lymphoma: TRAIL-R1 and TRAIL-R2 as candidate dosage-dependent tumor suppressor genes. Blood 106, 3214-3222. https://doi.org/10.1182/blood-2005-05-2013
  37. Saelens, X., Festjens, N., Vande Walle, L., van Gurp, M., van Loo, G., Vandenabeele, P., 2004. Toxic proteins released from mitochondria in cell death. Oncogene 23, 2861-2874. https://doi.org/10.1038/sj.onc.1207523
  38. Sakahira, H., Enari, M., Nagata, S., 1998. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 391, 96-99. https://doi.org/10.1038/34214
  39. SAS Institute, Inc., 1989. SAS/STAT user's guide. SAS Institute, Inc., Cary, NC.
  40. Scaffidi, C., Schmitz, I., Krammer, P.H., Peter, M.E., 1999. The role of c-FLIP in modulation of CD95-induced apoptosis. J. Biol. Chem. 274, 1541-1548. https://doi.org/10.1074/jbc.274.3.1541
  41. Schimmer, A.D., 2004. Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res. 64, 7183-7190. https://doi.org/10.1158/0008-5472.CAN-04-1918
  42. Slee, E.A., Adrain, C., Martin, S.J., 2001. Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J. Biol. Chem. 276, 7320-7326. https://doi.org/10.1074/jbc.M008363200
  43. Suliman, A., Lam, A., Datta, R., Srivastava, R.K., 2001. Intracellular mechanisms of TRAIL: apoptosis through mitochondrial-dependent and -independent pathways. Oncogene 20, 2122-2133. https://doi.org/10.1038/sj.onc.1204282
  44. van Loo, G., van Gurp, M., Depuydt, B., Srinivasula, S.M,, Rodriguez, I., Alnemri, E.S., Gevaert, K., Vandekerckhove, J., Declercq, W., Vandenabeele, P., 2002. The serine protease Omi/HtrA2 is released from mitochondria during apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. Cell Death Differ. 9, 20-26. https://doi.org/10.1038/sj.cdd.4400970
  45. Volk, C.J., Hofmann, R., Chauret, C., Gagnom, G.A., Ranger, G., Andrews, R.C., 2002. Implementation of chlorine dioxide disinfection: effects of the treatment change on drinking water quality in a full-scale distribution system. J. Environ. Eng. Sci. 1, 323-330. https://doi.org/10.1139/s02-026
  46. Wajant, H., 2002. The Fas signaling pathway: more than a paradigm. Science 296, 1635-1636. https://doi.org/10.1126/science.1071553
  47. Zeiss, C.J., 2003. The apoptosis-necrosis continuum: insights from genetically altered mice. Vet. Pathol. 40, 481-495. https://doi.org/10.1354/vp.40-5-481