Preliminary studies on induction of apoptosis by abamectin in Spodoptera frugiperda (Sf9) cell line

Pesticide Biochemistry and Physiology

Volumn 100, Issue 3, 2011, Pages 256-263

  Huang, Jing Fei ^a   Tian, Meng ^a   Lv, Chao Jun ^a   Li, Hai Yi ^a   Muhammad, Rizwan ul Haq ^a   Zhong, Guo Hua ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Abamectin; Apoptosis; Caspase 3; Cytochrome c; Mitochondrion; Sf9

Indexed keywords

ACTINOBACTERIA; LEPIDOPTERA; SPODOPTERA FRUGIPERDA; STREPTOMYCES; STREPTOMYCES AVERMITILIS;

EID: 79959654605     PISSN: 00483575     EISSN: 10959939     Source Type: Journal    
DOI: 10.1016/j.pestbp.2011.04.010     Document Type: Article

References (61)

1. Burg R.W., Miller B.M., Baker E.E., Birnbaum J., Currie S.A., Hartman R., Kong Y.L., Monaghan R.L., Olson G., Putter I., Tunac J.B., Wallick H., Stapley E.O., Oiwa R., Omura S. Avermectins, new family of potent anthelmintic agents: producing organism and fermentation. Antimicrob. Agents Chemother. 1979, 15:361-367.
2. Ostlind D.A., Cifelli S., Lang R. Insecticidal activity of the anti-parasitic avermectins. Vet. Rec. 1979, 105:168.
3. Mrozik H., Eskola P., Linn B.O., Lusi A., Shih T.L., Tisehler M., Waksmunski F.S., Wyvratt M.J., Hilton N.J., Anderson T.E., Babu J.R., Dybas R.A., Preiser F.A., Fisher M.H. Discovery of novel avermectins with unprecedented insecticidal activity. Experientia 1989, 45:315-316.
4. Lasota J.A., Dybas R.A. Avermectins, a novel class of compounds: implications for use in arthropod pest control. Annu. Rev. Entomol. 1991, 36:91-117.
5. Shoop W.L., Mrozik H., Fisher M.H. Structure and activity of avermectins and milbemycins in animal health. Vet. Parasitol. 1995, 59:139-156.
6. Schaeffer J.M., Haines H.W. Avermectin binding in Caenorhabditis elegans: a two-state model for the avermectin binding site. Biochem. Pharmacol. 1989, 38:2329-2338.
7. Arena J.P., Liu K.K., Paress P.S., Cully D.F. Avermectin-sensitive chloride currents induced by Caenorhabditis elegans RNA in Xenopus oocytes. Mol. Pharmacol. 1991, 40:368-374.
8. Arena J.P., Liu K.K., Paress P.S., Schaeffer J.M., Cully D.F. Expression of a glutamate activated chloride current in Xenopus oocytes injected with Caenorhabditis elegans RNA: evidence for modulation by avermectin. Mol. Brain Res. 1992, 15:339-348.
9. Dider A., Loor F. The abamectin derivative ivermectin is potent P-glycoprotein inhibitor. Anti-Cancer Drug 1996, 7:745-751.
10. Dradley G., Juranka P.F., Ling V. Mechanism of multidrug resistance. Biochim. Biophys. Acta 1988, 948:87-128.
11. Gill D.R., Hyde S.C., Higgins C.F., Valverde M.A., Mintenig G.M., Sepulveda F.V. Separation of drug transport and chloride channel function of the human multidrug resistance P-glycoprotein. Cell 1992, 71:23-32.
12. R.S. Cotran, V. Kumar, T. Collins, S.L. Robbins, Robbins Pathologic Basis of Disease, sixth ed., W.B Saunders Company, Philadelphia, 1999, pp. 100-103.
13. Mattson M.P., Chan S.L. Calcium orchestrates apoptosis. Nat. Cell Biol. 2003, 5:1041-1043.
14. Georg H. The morphology of apoptosis. Cell Tissue Res. 2000, 301:5-17.
15. Kerr J.F., Wyllie A.H., Currie A.R. Apoptosis: a basis biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 1972, 26:239-257.
16. Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell. Bio. 2008, 9:231-241.
17. Parthasarathy R., Palli S.R. Developmental and hormonal regulation of midgut remodeling in a lepidopteran insect, Heliothis virescens. Mech. Develop. 2007, 124:23-34.
18. Rhee W.J., Kim E.J., Park T.H. Silkworm hemolymph as a potent inhibitor of apoptosis in sf9 cells. Biochem. Biophys. Res. Commun. 2002, 295:779-783.
19. Liu L.J., Peng J.X., Liu K.Y., Yang H., Li Y., Hong H.Z. Influence of cytochrome c on apoptosis induced by Anagrapha (Syngrapha) falcifera multiple nuclear polyhedrosis virus in insect Spodoptera litura cells. Cell Biol. Int. 2007, 31:996-1001.
20. Kroemer G., Petit P., Zamzami N., Vayssiere J.L., Mignote B. The biochemistry of programmed cell death. FASEB J. 1995, 9:1277-1287.
21. Stennicke H.R., Deveraux Q.L., Humke E.W., Reed J.C., Dixit V.M., Salvesen G.S. Caspase-9 can be activated without proteolytic processing. J. Biol. Chem. 1999, 274:8359-8362.
22. Zimmermann K.C., Ricci J.E., Droin N.M., Green D.R. The role of ARK in stress-induced apoptosis in Drosophila cells. J. Cell Biol. 2002, 156:1077-1087.
23. Means J.C., Muro I., Clem R.J. Lack of involvement of mitochondrial factors in caspase activation in a Drosophila cell-free system. Cell Death Differ. 2006, 13:1222-1234.
24. Dorstyn L., Read S., Cakouros D., Huh J.R., Hay B.A., Kumar S. The role of cytochrome-c incaspase activation in Drosophila melanogaster cells. J. Cell Biol. 2002, 156:1089-1098.
25. Dorstyn L., Mills K., Lazebnik Y., Kumar S. The two cytochrome-c species, DC3 and DC4, are not required for caspase activation and apoptosis in Drosophila cells. J. Cell Biol. 2004, 167:405-410.
26. Dorstyn L., Kumar S. A cytochrome-c-free fly apoptosome. Cell Death Differ. 2006, 13:1049-1051.
27. Mohan M., Taneja T.K., Sahdev S., Mohareer K., Begum R., Athar M., Sah N.K., Hasnain S.E. Antioxidants prevent UV-induced apoptosis by inhibiting mitochondrial cytochrome c release and caspase activation in Spodoptera frugiperda (Sf9) cells. Cell Biol. Int. 2003, 27:483-490.
28. Pan M.H., Chen M., Huang S.J., Yu Z.S., Cheng C.G., Lu C. Cloning and protein release of cytochrome c in the apoptosis cells of silkworm, Bombyx mori. Sci. Agric. Sin. 2009, 42:2546-2551.
29. Kumarswamy R., Seth R.K., Dwarakanath B.S., Chandna S. Mitochondrial regulation of insect cell apoptosis: evidence for permeability transition pore-independent cytochrome-c release in the Lepidopteran Sf9 cells. Int. J. Biochem. Cell Biol. 2009, 41:1430-1440.
30. Abdelwahid E., Yokokura T., Krieser R.J., Balasundaram S., Fowle W.H., White K. Mitochondrial disruption in Drosophila apoptosis. Dev. Cell 2007, 12:793-796.
31. Goyal G., Fell B., Sarin A., Youle R.J., Sriram V. Role of mitochondrial remodeling in programmed cell death in Drosophila melanogaster. Dev. Cell 2007, 12:807-816.
32. Drinyaev V.A., Mosin V.A., Kruglyak E.B., Sterlina T.S., Kataev A.A., Berestovsky G.N., Kokoz Y.M. Effect of avermectins on Ca2+-dependent Cl- currents in plasmalemma of Chara corallina cells. J. Membr. Biol. 2001, 182:71-79.
33. Kolar L., Jemec A., van Gestel C.A., Valant J., Hrzenjak R., Erzen N.K., Zidar P. Toxicity of abamectin to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Ecotoxicology 2010, 19:917-927.
34. Ci X.X., Li H.Y., Yu Q.L., Zhang X.M., Yu L., Chen N., Song Y., Deng X.M. Avermectin exerts anti-inflammatory effect by downregulating the nuclear transcription factor kappa-B and mitogen-activated protein kinase activation pathway. Fundam. Clin. Pharmacol. 2009, 23:449-455.
35. Xiang W., Gao A., Liang H., Li C., Gao J., Wang Q., Shuang B., Zhang J., Yan Y., Wang X. Reversal of P-glycoprotein-mediated multidrug resistance in vitro by milbemycin compounds in adriamycin-resistant human breast carcinoma (MCF-7/adr) cells. Toxicol. In Vitro 2010, 24:1474-1481.
36. Sun Y.J., Long D.X., Li W., Hou W.Y., Wu Y.J., Shen J.Z. Effects of avermectins on neurite outgrowth in differentiating mouse neuroblastoma N2a cells. Toxicol. Lett. 2010, 192:206-211.
37. Korystov Y.N., Ermakova N.V., Kublik L.N., Levitman M.K.h., Shaposhnikova V.V., Mosin V.A., Drinyaev V.A., Kruglyak E.B., Novik T.S., Sterlina T.S. Avermectins inhibit multidrug resistance of tumor cells. Eur. J. Pharmacol. 2004, 493:57-64.
38. El-Shenawy N.S. Effects of insecticides fenitrothion, endosulfan and abamectin on antioxidant parameters of isolated rat hepatocytes. Toxicol. In Vitro 2010, 24:1148-1157.
39. Wang M., Li S. Effect of avermectin on mitochondria from primary cultured neurons. Acta Scientiae Circumstantiae 2008, 28:2101-2104.
40. Wang J.J., Cui Y.L., Li J.M., Jia H.Y., Yu Q., Li S. Effects of avermectin on level of intracellular free calcium and expression of CaM mRNA in King Pigeon neurons cultured in vitro. Chin. Vet. Sci. 2009, 39:75-78.
41. Rello S., Stockert J.C., Moreno V., Gámez A., Pacheco M., Juarranz A., Cañete M., Villanueva A. Morphological criteria to distinguish cell death induced by apoptotic and necrotic treatments. Apoptosis 2005, 10:201-208.
42. Leist M., Jäättelä M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell. Bio. 2001, 2:589-598.
43. Clem R.J., Miller L.K. Control of programmed cell death by the baculovirus genes p35 and iap. Mol. Cell. Biol. 1994, 14:5212-5222.
44. Seshagiri S., Miller L.K. Baculovirus inhibitors of apoptosis (IAPs) block activation of Sf-caspase-1. Proc. Natl. Acad. Sci. USA 1997, 94:13606-13611.
45. Zhong G.H., Shui K.J., Huang J.F., Jia J.W., Hu M.Y. Induction of apoptosis by botanical components in Spodoptera litura cultured cell line. Acta Entomologica Sinicia 2008, 51:449-453.
46. Zhong G.H., Shui K.J., Lu C.J., Jia J.W., Ren T.J., Hu M.Y. Induction of apoptosis by azadirachtin, a botanical insecticidal component, in Spodoptera litura Sl-1 cultured cell line. Acta Entomologica Sinicia 2008, 51:618-627.
47. Jia J.W., Huang J.F., Wang W.W., Hu M.Y., Zhong G.H. Effects of different insecticidal components on induction of apoptosis in Spodoptera frugiperda cultured cell line Sf9. J. South China Agr. Uni. 2009, 30:29-35.
48. Huang J.F., Shui K.J., Li H.Y., Hu M.Y., Zhong G.H. Antiproliferative effect of azadirachtin A on Spodoptera litura Sl-1 cell line through cell cycle arrest and apoptosis induced by up-regulation of p53. Pestic. Biochem. Physiol. 2011, 99:16-24.
49. Mosin V.A., Krugliak E.B., Sterlina T.S., Korystov I.u.N., Shaposhnikova V.V., Kublik L.N., Levitman M.K.h., Viktorov A.V., Driniaev V.A. Action of avermectins on lymphoid leukemia P-388 cells in vitro. Antibiot. Khimioter. 1999, 44:16-20.
50. Mosin V.A., Krugliak E.B., Sterlina T.S., Korystov I.u.N., Shaposhnikova V.V., Narimanov A.A., Kublik L.N., Levitman M.K.h., Viktorov A.V., Driniaev V.A. Cytotoxic and cytostatic effect of avermectines on tumor cells in vitro. Antibiot. Khimioter. 2000, 45:10-14.
51. Driniaev V.A., Mosin V.A., Krugliak E.B., Sterlina T.S., Viktorov A.V., Tsyganova V.G., Korystova A.F., Grichenko A.S., Zenchenko K.I., Kokoz I.u.M. Selective cytostatic and cytotoxic effects of avermectins. Antibiot. Khimioter. 2001, 46:13-16.
52. Furusawa S., Shibata H., Nishimura H., Nemoto S., Takayanagi M., Takayanagi Y., Sasaki K.I. Potentiation of doxorubicin-induced apoptosis of resistant mouse leukaemia cells by ivermectin. Pharm. Pharmacol. Commun. 2000, 6:129-134.
53. Gao A.L., Wang X.J., Xiang W.S., Liang H.S., Gao J.G., Yan Y.J. Reversal of P-glycoprotein-mediated multidrug resistance in vitro by doramectin and nemadectin. J. Pharm. Pharmacol. 2010, 62:393-399.
54. Cui Y.L., Wang M., Huang W., Guan L.P., Li S. Avermectin-induced mitochondria damage and apoptosis in cultured pigeon neurons Chinese. Vet. Sci. 2007, 37:969-973.
55. Kroemer G., Zamzami N., Susin S.A. Mitochondrial control of apoptosis. Immunol. Today 1997, 18:44-51.
56. Hengartner M.O. The biochemistry of apoptosis. Nature 2000, 407:770-776.
57. Adrain C., Martin S.J. The mitochondrial apoptosome: a killer unleashed by the cytochrome seas. Trends Biochem. Sci. 2001, 26:390-397.
58. Scarlett J.L., Sheard P.W., Hughes G., Ledgerwooda E.C., Kuc H.H., Murphy M.P. Changes in mitochondrial membrane potential during stauros porine-induced apoptosis in jurkat cells. FEBS Lett. 2000, 475:267-272.
59. Chauvin C., De Oliveira F., Ronot X., Mousseau M., Leverve X., Fontaine E. Rotenone inhibits the mitochondrial permeability transit on induced cell death in U937 and KB cells. J. Biol. Chem. 2001, 276:41394-41398.
60. Tatton W.G., Chalmers-Redman R.M. Mitochondria in neurodegenerative apoptosis: an opportunity for therapy. Ann. Neurol. 1998, 44:S134-S141.
61. Buss D.S., Callaghan A. Interaction of pesticides with p-glycoprotein and other ABC proteins: a survey of the possible importance to insecticide, herbicide and fungicide resistance. Pestic. Biochem. Physiol. 2008, 90:141-153.