Molecular evidence of curcumin-induced apoptosis in the filarial worm Setaria cervi

Parasitology Research

Volumn 111, Issue 3, 2012, Pages 1173-1186

  Nayak, Ananya ^a   Gayen, Prajna ^a   Saini, Prasanta ^a   Mukherjee, Niladri ^a   Sinha Babu, Santi P ^a  

^a VISVA BHARATI UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; CASPASE 9; CURCUMIN; GLUTATHIONE; GLUTATHIONE TRANSFERASE; HOE 33342; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANTHELMINTIC ACTIVITY; APOPTOSIS; ARTICLE; CED 3 GENE; CED 4 GENE; CED 9 GENE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DETOXIFICATION; DNA FRAGMENTATION; DRUG SCREENING; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; GENE; GENE EXPRESSION REGULATION; IN VITRO STUDY; LYMPHATIC FILARIASIS; MALE; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PARASITE VIABILITY; PRIORITY JOURNAL; SETARIA CERVI;

ANIMALS; APOPTOSIS; BENZIMIDAZOLES; CURCUMIN; DNA, COMPLEMENTARY; DNA, HELMINTH; FEMALE; IN SITU NICK-END LABELING; MALE; NEMATODA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, HELMINTH; STAINING AND LABELING;

CURCUMA LONGA; NEMATODA; SETARIA CERVI;

EID: 84866081338     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-012-2948-0     Document Type: Article

References (76)

1. Akhtar MS, Iqbal Z, Khan MN, Lateef M (2000) Anthelmintic activity of medicinal plants with particular reference to their use in animals in the Indo-Pakistan subcontinent. Small Rumin Res 38:99- 107
2. Atsumi T, Fujisawa S, Tonosaki K (2005) Relationship between intracellular ROS production and membrane mobility in curcuminand tetrahydrocurcumin-treated human gingival fibroblasts and human submandibular gland carcinoma cells. Oral Dis 11:236- 242 (Pubitemid 40992542)
3. Bhaumik S, Anjum R, Rangaraj N, Pardhasaradhi BVV, Khar A (1999) Curcumin mediated apoptosis in AK-5 tumor cells involves the production of reactive oxygen intermediates. FEBS Lett 456:311- 314 (Pubitemid 29352314)
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
5. Chanvorachote P, Pongrakhananon V, Wannachaiyasit S, Luanpitpong S, Rojanasakul Y, Nimmannit U (2009) Curcumin sensitizes lung cancer cells to cisplatin-induced apoptosis through superoxide anion-mediated Bcl-2 degradation. Cancer Invest 27:624-635
6. Chao JW, Lee KS, Kim CW (2007) Curcumin attenuates the expression of IL-1β, IL-6, and TNF-α as well as cyclin E in TNF-α- treated HaCaT cells; NF-κB and MAPKs as potential upstream targets. Int J Mol Med 19:469-474
7. Cheng AL, Hsu CH, Lin JK, Hsu MM, Ho YF, Shen TS, Ko JY, Lin JT, Lin BR, Ming-ShiangW, Yu HS, Jee SH, Chen GS, Chen TM, Chen CA, Lai MK, Pu YS, Pan MH, Wang YJ, Tsai CC, Hsieh CY (2001) Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or premalignant lesions. Anticancer Res 21:2895-2900
8. Chiumiento L, Bruschi F (2009) Enzymatic antioxidant systems in helminth parasites. Parasitol Res 105:593-603
9. Choi HS, Kim JW, Cha YN, Kim C (2006) A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells. J Immunoass Immunochem 27:31-44 (Pubitemid 43087625)
10. Circu ML, Aw TY (2010) Reactive oxygen species, cellular redox systems and apoptosis. Free Radic Biol Med 48:749-762
11. Comley JCW, Rees MJ, Turner CH, Jenkins DC (1989) Colorimetric quantitationof filarial viability. Int J Parasitol 19:77-83
12. Conradt B (2009) Genetic control of programmed cell death during animal development. Annu Rev Genet 43:493-523
13. Conradt B, Horvitz HR (1998) The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl- 2-like protein CED-9. Cell 93:519-529 (Pubitemid 28240714)
14. Debrah AY, Mand S, Marfo-Debrekyei Y, Batsa L, Pfarr K, Buttner M, Adjei O, Buttner D, Hoerauf A (2007) Macrofilaricidal effect of 4 weeks of treatment with doxycycline on Wuchereria bancrofti. Trop Med Int Health 12:1433-1441 (Pubitemid 350212708)
15. Deeb D, Jiang H, Gao X, Al-Holou S, Danyluk AL, Dulchavsky SA, Gautam SC (2007) Curcumin [1,7-bis(4-hydroxy-3-methoxyphenyl)- 1-6-heptadine-3,5- dione;C21H20O6] sensitizes human prostate cancer cells to tumor necrosis factor-related apoptosisinducingligand/ Apo2L-induced apoptosis by suppressing nuclear factor-κB via inhibition of the prosurvival Akt signaling pathway. J Pharmacol Exp Ther 321:616-625 (Pubitemid 46624498)
16. Dhillon N, Aggarwal BB, Newman RA, Wolff RA, Kunnumakkara AB, Abbruzzese JL, Ng CS, Badmaev V, Kurzrock R (2008) Phase II trial of curcumin in patients with advanced pancreatic cancer. Clin Cancer Res 14:4491-4499
17. Flomerfelt FA, Briehl MM, Dowd DR, Dieken ES, Miesfeld RL (1993) Elevated glutathione S-transferase gene expression is an early event during steroid-induced lymphocyte apoptosis. J Cell Physiol 154:573-581 (Pubitemid 23076326)
18. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130-7139
19. Higuchi Y (2004) Glutathione depletion-induced chromosomal DNA fragmentation associated with apoptosis and necrosis. J Cell Mol Med 8:455-464 (Pubitemid 44145478)
20. Kane DJ, Sarafian TA, Anton R, Hahn H, Gralla EB, Valentine JS, Ord T, Bredesen DE (1993) Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262:1274-1277 (Pubitemid 24036095)
21. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239-257
22. Khanbolooki S, Nawrocki ST, Arumugam T, Andtbacka R, Pino MS, Kurzrock R, Logsdon CD, Abbruzzese JL, McConkey DJ (2006) Nuclear factor-κB maintains TRAIL resistance in human pancreatic cancer cells. Mol Cancer Ther 5:2251-2260 (Pubitemid 44530462)
23. Kuhar M, Imran S, Singh N (2007) Curcumin and quercetin combined with cisplatin to induce apoptosis in human laryngeal carcinoma hep-2 cells through the mitochondrial pathway. J Cancer Mol 3:121-128
24. Lee JW, Hong HM, Kwon DD, Pae HO, Jeong HJ (2010) Dimethoxycurcumin, a sructural analogue of curcumin, induces apoptosis in human renal carcinoma caki cells through the production of reactive oxygen species, the release of cytochrome c, and the activation of caspase-3. Korean J Urol 51:870-878
25. Li X, Wang J, Manley JL (2005) Loss of splicing factor ASF/SF-2 induces G2 cell cycle arrest and apoptosis but inhibits internucleosomal DNA fragmentation. Gene Dev 19:2705-2714 (Pubitemid 41627937)
26. Magalhães LG, Machado CB, Morais ER, Moreira EBC, Soares CS, da Silva SH, Da Silva Filho AA, Rodrigues V (2009) In vitro schistosomicidal activity of curcumin against Schistosoma mansoni adult worms. Parasitol Res 104:1197-1201
27. Mengome LE, Akue JP, Souza A, Tchoua GRF, Emvo EN (2010) In vitro activities of plant extracts on human Loa loa isolates and cytotoxicity for eukaryotic cells. Parasitol Res 107:643-650
28. Misra N, SharmaM, Raj K, Dangi A, Srivastava S,Misra-Bhattacharya S (2007) Chemical constituents and antifilarial activity of Lantana camara against human lymphatic filariid Brugia malayi and rodent filariid Acanthocheilonema viteae maintained in rodent hosts. Parasitol Res 100:439-448 (Pubitemid 46011252)
29. Misra S, Verma M, Mishra SK, Srivastava S, Lakshmi V, Misra- Bhattacharya S (2011) Gedunin and photogedunin of Xylocarpus granatum possess antifilarial activity against human lymphatic filarial parasite Brugia malayi in experimental rodent host. Parasitol Res 109:1351-1360
30. Molyneux DH, Bradley M, Hoerauf A, Kyelem D, Taylor MJ (2003) Mass drug treatment for lymphatic filariasis and onchocerciasis. Trends Parasitol 19:516-522 (Pubitemid 37329661)
31. Nagajyothi F, Zhao D, Weiss LM, Tanowitz HB (2012) Curcumin treatment provides protection against Trypanosoma cruzi infection. Parasitol Res. doi:10.1007/s00436-011-2790-9
32. Nayak A, Gayen P, Saini P, Maitra S, Sinha Babu SP (2011) Albendazole induces apoptosis in adults and microfilariae of Setaria cervi. Exp Parasitol 128:236-242
33. Nijhoff WA, Groen GM, Peters WHM (1993) Induction of rat hepatic and intestinal glutathione S-transferases and glutathione by dietary naturally occurring anticarcinogens. Int J Oncol 3:1131-1139 (Pubitemid 23361374)
34. Nisha M, Kalyanasundaram M, Paily KP, Abidha VP, Balaraman K (2007) In vitro screening of medicinal plant extracts for macrofilaricidal activity. Parasitol Res 100:575-579 (Pubitemid 46011269)
35. Patel BB, Sengupta R, Qazi S, Vachhani H, Yu Y, Rishi AK, Majumdar AP (2008) Curcumin enhances the effects of 5-fluorouracil and oxaliplatin in mediating growth inhibition of colon cancer cells by modulating EGFR and IGF-1R. Int J Cancer 122:267-273 (Pubitemid 350234711)
36. Pias EK, Ekshyyan OY, Rhoads CA, Fuseler J, Harrison L, Ty A (2003) Differentia effects of superoxide dismutase isoform expression on hydroperoxide induced apoptosis in PC-12 cells. J Biol Chem 278:13294-13301 (Pubitemid 36800100)
37. Piwocka K, Jaruga E, Skierski J, Gradzka I, Sikora E (2001) Effect of glutathione depletion on caspase-3 independent apoptosis pathway induced by curcumin in Jurkat cells. Free Radic Biol Med 31:670-678 (Pubitemid 32777868)
38. Raamsdonk JMV, Hekimi S (2010) Reactive oxygen species and aging in Caenorhabditis elegans:causal or casual relationship? Antioxid Redox Signal 13:1911-1953
39. Rajeswari A (2006) Curcumin protects mouse brain from oxidative stress caused by 1-methyl-4-phenyl-1,2,3,6-tetrahydro pyridine. Eur Rev Med Pharmacol Sci 10:157-161 (Pubitemid 44468939)
40. Ramasubramaniaraja R, Niranjan Babu M (2010) Antihelminthic studies and medicinal herbs - an overview. IJPSRR 5:39-47
41. Rao R, Weil GJ (2002) In vitro effects of antibiotics on Brugia malayi worm survival and reproduction. J Parasitol 88:605-611 (Pubitemid 34686529)
42. Rao UR, Salinas G, Mehta K, Klei TR (2000) Identification and localization of glutathione S-transferase as a potential target enzyme in Brugia species. Parasitol Res 86:908-915
43. Reddien PW, Andersen EC, Huang MC, Horvitz HR (2007) DPL-1 DP, LIN-35 Rb and EFL-1 E2F act with the MCD-1 zinc-finger protein to promote programmed cell death in Caenorhabditis elegans. Genetics 175:1719-1733 (Pubitemid 46789957)
44. Reddya VN, Kasaharaa E, Hiraokab M, Lina LR, Hoc YS (2004) Effects of variation in superoxide dismutases (SOD) on oxidative stress and apoptosis in lens epithelium. Exp Eye Res 79:859-868
45. Sandur SK, Ichikawa H, Pandey MK, Kunnumakkara AB, Sung B, Sethi G, Aggarwal BB (2007) Role of pro-oxidants and antioxidants in the anti- inflammatory and apoptotic effects of curcumin (diferuloylmethane). Free Radic Biol Med 43:568-580 (Pubitemid 47058232)
46. Schwab AE, Boakye DA, Kyelem D, Prichard RK (2005) Detection of benzimidazole resistance-associated mutations in the filarial nematode Wuchereria bancrofti and evidence for selection by albendazole and ivermectin combination treatment. AmJTrop Med Hyg 73:234-238 (Pubitemid 41278690)
47. Selkirk ME, Smith VP, Thomas GR, Gounaris K (1998) Resistance of filarial nematode parasites to oxidative stress. Int J Parasitol 28:1315-1332 (Pubitemid 28386943)
48. Sen S, Sharma H, Singh N (2005) Curcumin enhances vinorelbinemediated apoptosis in NSCLC cells by the mitochondrial pathway. Biochem Biophys Res Commun 331:1245-1252 (Pubitemid 40692490)
49. Senoo-Matsuda N, Hartman PS, Akatsuka A, Yoshimura S, Ishii N (2003) A complex II defect affects mitochondrial structure, leading to ced-3 and ced-4 dependent apoptosis and aging. J Biol Chem 278:22031-22036 (Pubitemid 36792612)
50. Shahiduzzaman M, Dyachenko V, Khalafalla RE, Desouky AY, Daugschies A (2009) Effects of curcumin on Cryptosporidium parvum in vitro. Parasitol Res 105:1155-1161
51. Sharma RA, Euden SA, Platton SL, Cooke DN, Shafayat A, Hewitt HR, Marczylo TH, Morgan B, Hemingway D, Plummer SM, Pirmohamed M, Gescher AJ, Steward WP (2004) Phase I clinical trial of oral curcumin: biomarkers of systemic activity and compliance. Clin Cancer Res 10:6847-6854 (Pubitemid 39383033)
52. Shishodia S, Amin HM, Lai R, Aggarwal BB (2005a) Curcumin (diferuloylmethane) Inhibits constitutive NF-κB activation, induces G1/S arrest, suppresses proliferation, and induces apoptosis in mantle cell lymphoma. Biochem Pharmacol 70:700-713 (Pubitemid 41058705)
53. Shishodia S, Sethi G, Aggarwal BB (2005b) Curcumin: getting back to the roots. Ann N Y Acad Sci 1056:206-217 (Pubitemid 43030979)
54. Sikora E, Zmijewska AB, Magalska A, Piwocka K, Mosieniak G, Kalinowska M, Widlak P, Cymerman IA, Bujnicki JM (2006) Curcumin induces caspase-3-dependent apoptotic pathway but inhibits DNA fragmentation factor 40/caspase-activated Dnase endonuclease in human jurkat cells. Mol Cancer Ther 5:927-934 (Pubitemid 43724592)
55. Singh A, Rathaur S (2010) Combination of DEC plus aspirin induced mitochondrial mediated apoptosis in filarial parasite Setaria cervi. Biochimie 92:894-900
56. Singhal SS, Awasthi S, Pandya U, Piper JT, Saini MK, Cheng JZ, Awasthi YC (1999) The effect of curcumin on glutathione-linked enzymes in K562 human leukemia cells. Toxicol Lett 109:87-95 (Pubitemid 29459059)
57. Slatko BE, Taylor MJ, Foster JM (2010) The Wolbachia endosymbiont as an anti-filarial nematode target. Symbiosis 51:55-65
58. Srinivasan L, Mathew N, Muthuswamy K (2009) In vitro antifilarial activity of glutathione S-transferase inhibitors. Parasitol Res 105:1179-1182
59. Srinivasan L, Mathew N, Karunan T, Muthuswamy K (2011) Biochemical studies on glutathione S-transferase from the bovine filarial worm Setaria digitata. Parasitol Res 109:213- 219
60. Susan M, Rao MNA (1992) Induction of glutathione S-transferase activity by curcumin in mice. Drug Res 42:962-964
61. Syng-Ai C, Kumari AL, Khar A (2004) Effect of curcumin on normal and tumor cells: role of glutathione and bcl-2. Mol Cancer Ther 3:1101-1108 (Pubitemid 39295007)
62. Thayyullathil F, Chathoth S, Hago A, Patel M, Galadari S (2008) Rapid reactive oxygen species (ROS) generation induced by curcumin leads to caspase-dependent and independent apoptosis in L929 cells. Free Radic Biol Med 45:1403-1412
63. Turner JD, Mand S, Debrah AY, Muehlfeld J, Pfarr K, McGarry HF, Adjei O, Taylor MJ, Hoerauf A (2006) A randomized, doubleblind clinical trial of a 3-week course of doxycycline plus albendazole and ivermectin for the treatment of Wuchereria bancrofti infection. Clin Infect Dis 42:1081-1089
64. Voehringer DW (1999) BCL-2 And glutathione: alterations in cellular redox state that regulate apoptosis sensitivity. Free Radic Biol Med 27:945-950 (Pubitemid 29507468)
65. Wang S, Zhao Y, Wu L, Tang M, Su C, Hei TK, Yu Z (2007) Induction of germline cell cycle arrest and apoptosis by sodium arsenite in Caenorhabditis elegans. Chem Res Toxicol 20:181-186 (Pubitemid 46408854)
66. Wang J, Qi L, Zheng S, Wu T (2009) Curcumin induces apoptosis through the mitochondria-mediated apoptotic pathway in HT-29 cells. J Zhejiang Univ Sci 10:93-102
67. Watson JL, Hill R, Yaffe PB, Greenshields A, Walsh M, Lee PW, Giacomantonio CA, Hoskin DW (2010) Curcumin causes superoxide anion production and p53- independent apoptosis in human colon cancer cells. Cancer Lett 297:1-8
68. WHO (1999) Building partnerships for lymphatic filariasis: strategic plan. Geneva: World Health Organization. WHO/FIL/99.198WHO/l
69. Wu YC, Stanfield GM, Horvitz HR (2000) NUC-1, a Caenorhabditis elegans DNase II homolog, functions in an intermediate step of DNA degradation during apoptosis. Gene Dev 14:536-548 (Pubitemid 30159773)
70. Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555-556 (Pubitemid 10070336)
71. Yadav VR, Prasad S, Kannappan R, Ravindran J, Chaturvedi MM, Vaahtera L, Parkkinen J, Aggarwal BB (2010a) Cyclodextrincomplexed curcumin exhibits anti-inflammatory and antiproliferative activities superior to those of curcumin through higher cellular uptake. Biochem Pharmacol 80:1021-1032
72. Yadav M, Singh A, Rathaur S, Liebau E (2010b) Structural modeling and simulation studies of Brugia malayi glutathione-S-transferase with compounds exhibiting antifilarial activity: implications in drug targeting and designing. J Mol Graph Model 28:435-445
73. Yanase S, Onodera A, Tedesco P, Johnson TE, Ishii N (2009) SOD-1 deletions in Caenorhabditis elegans alter the localization of intracellular reactive oxygen species and show molecular compensation. J Gerontol A Biol Sci Med Sci 64:530-539
74. Yuan J, Horvitz HR (2004) A first insight into the molecular mechanisms of apoptosis. Cell S116:S53-S56
75. Yuste VJ, Bayascas JR, Llecha N, Sanchez-Lopez I, Boix J, Comella JX (2001) The absence of oligonucleosomal DNA fragmentation during apoptosis of IMR-5 neuroblastoma cells. J Biol Chem 276:22323-22331
76. Zucker B, Hanusch J, Bauer G (1997) Glutathione depletion in fibroblasts is the basis for apoptosis-induction by endogenous reactive oxygen species. Cell Death Differ 4:388-395 (Pubitemid 127680673)