Plumbagin inhibits proliferative and inflammatory responses of T cells independent of ROS generation but by modulating intracellular thiols

Journal of Cellular Biochemistry

Volumn 110, Issue 5, 2010, Pages 1082-1093

  Checker, Rahul ^a   Sharma, Deepak ^a   Sandur, Santosh K ^a   Subrahmanyam, G ^b   Krishnan, Sunil ^a   Poduval, T B ^a   Sainis, K B ^a  

^a BHABHA ATOMIC RESEARCH CENTRE   (India)

^b INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

Author keywords

Anti inflammatory; Glutathionylation; Immune; Plumbagin; Redox; Thiol

Indexed keywords

ACETYLCYSTEINE; ALLOPURINOL; ANTIOXIDANT; DIPHENYL IODONIUM; ENZYME INHIBITOR; GAMMA INTERFERON; GLUTATHIONE; I KAPPA B ALPHA; INTERLEUKIN 2; INTERLEUKIN 4; MALEIC ACID DIETHYL ESTER; MITOGEN ACTIVATED PROTEIN KINASE; PLUMBAGIN; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ROTENONE; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; THIOL DERIVATIVE; UNCLASSIFIED DRUG; XANTHINE OXIDASE INHIBITOR;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BIOLOGICAL ACTIVITY; CELL METABOLISM; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; ENZYME PHOSPHORYLATION; GLUTATHIONYLATION; GRAFT DYSFUNCTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNE RESPONSE; IMMUNOREGULATION; INFLAMMATION; LYMPHOCYTE PROLIFERATION; MALE; MASS SPECTROMETRY; MODULATION; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE; TUMOR CELL; TUMOR GROWTH;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BLOTTING, WESTERN; CATALASE; CELL PROLIFERATION; CELLS, CULTURED; CONCANAVALIN A; CYTOKINES; GLUTATHIONE; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; INTERLEUKIN-2; INTERLEUKIN-4; INTERLEUKIN-6; INTRACELLULAR SPACE; LYMPHOCYTE ACTIVATION; MALE; MICE; MITOGENS; NAPHTHOQUINONES; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SULFHYDRYL COMPOUNDS; SUPEROXIDE DISMUTASE; T-LYMPHOCYTES;

EID: 77954910039     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22620     Document Type: Article

References (47)

1. Agrawal A, Kaushal P, Agrawal S, Gollapudi S, Gupta S. 2007. Thimerosal induces TH2 responses via influencing cytokine secretion by human dendritic cells. J Leukoc Biol 81:474-482. (Pubitemid 46198399)
2. Biswas S, Chida AS, Rahman I. 2006. Redox modifications of protein-thiols: Emerging roles in cell signaling. Biochem Pharmacol 71:551-564. (Pubitemid 43121989)
3. Bouzyk E, Iwanenko T, Jarocewicz N, Kruszewski M, Sochanowicz B, Szumiel I. 1997. Antioxidant defense system in differentially hydrogen peroxide sensitive L5178Y sublines. Free Radic Biol Med 22:697-704. (Pubitemid 27043406)
4. Checker R, Chatterjee S, Sharma D, Gupta S, Variyar P, Sharma A, Poduval TB. 2008. Immunomodulatory and radioprotective effects of lignans derived from fresh nutmeg mace (Myristica fragrans) in mammalian splenocytes. Int Immunopharmacol 8:661-669.
5. Checker R, Sharma D, Sandur SK, Khanam S, Poduval TB. 2009. Anti-inflammatory effects of plumbagin are mediated by inhibition of NF-kappaB activation in lymphocytes. Int Immunopharmacol 9:949-958.
6. Dalle-Donne I, Rossi R, Colombo G, Giustarini D, Milzani A. 2009. Protein S-glutathionylation: A regulatory device from bacteria to humans. Trends Biochem Sci 34:85-96.
7. D'Astafort D. 1829 Chemische Versuche mit dem Plumbagin, der scharfen Materie aus der Wurzel von Plumbago europaea. Archiv der Pharmazie 29:245-250.
8. Deas O, Dumont C, Mollereau B, Metivier D, Pasquier C, Bernard-Pomier G, Hirsch F, Charpentier B, Senik A. 1997. Thiol-mediated inhibition of FAS and CD2 apoptotic signaling in activated human peripheral T cells. Int Immunol 9:117-125. (Pubitemid 27062894)
9. Flescher E, Ledbetter JA, Schieven GL, Vela-Roch N, Fossum D, Dang H, Ogawa N, Talal N. 1994. Longitudinal exposure of human T lymphocytes to weak oxidative stress suppresses transmembrane and nuclear signal transduction. J Immunol 153:4880-4889. (Pubitemid 24356118)
10. Flescher E, Tripoli H, Salnikow K, Burns FJ. 1998. Oxidative stress suppresses transcription factor activities in stimulated lymphocytes. Clin Exp Immunol 112:242-247. (Pubitemid 28266682)
11. Fratelli M, Demol H, Puype M, Casagrande S, Eberini I, Salmona M, Bonetto V, MengozziM, Duffieux F, Miclet E, Bachi A, Vandekerckhove J, Gianazza E, Ghezzi P. 2002. Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proc Natl Acad Sci USA 99:3505-3510.
12. Gloire G, Piette J. 2009. Redox regulation of nuclear post-translational modifications during NF-κB activation. Antioxid Redox Signal 11:2209-2222.
13. Harikumar KB, Kunnumakkara AB, Ahn KS, Anand P, Krishnan S, Guha S, Aggarwal BB. 2009. Modification of the cysteine residues in IkappaBalpha kinase and NF-kappaB (p65) by xanthohumol leads to suppression of NFkappaB-regulated gene products and potentiation of apoptosis in leukemia cells. Blood 113:2003-2013.
14. Hazra B, Sarkar R, Bhattacharyya S, Ghosh PK, Chel G, Dinda B. 2002. Synthesis of plumbagin derivatives and their inhibitory activities against Ehrlich ascites carcinoma in vivo and Leishmania donovani Promastigotes in vitro. Phytother Res 16:133-137.
15. Hedley DW, Chow S. 1994. Evaluation of methods for measuring cellular glutathione content using flow cytometry. Cytometry 15:349-358.
16. Henry TR, Wallace KB. 1996. Differential mechanisms of cell killing by redox cycling and arylating quinones. Arch Toxicol 70:482-489.
17. Hildeman DA, Mitchell T, Aronow B, Wojciechowski S, Kappler J, Marrack P. 2003a. Control of Bcl-2 expression by reactive oxygen species. Proc Natl Acad Sci USA 100:15035-15040. (Pubitemid 37518012)
18. Hildeman DA, Mitchell T, Kappler J, Marrack P. 2003b. T cell apoptosis and reactive oxygen species. J Clin Invest 111:575-581. (Pubitemid 36278573)
19. Inbaraj JJ, Chignell CF. 2004. Cytotoxic action of juglone and plumbagin: A mechanistic study using HaCaT keratinocytes. Chem Res Toxicol 17:55-62.
20. Kang KW, Lee SJ, Kim SG. 2005. Molecular mechanism of Nrf2 activation by oxidative stress. Antioxid Redox Signal 7:1664-1673.
21. Kawiak A, Piosik J, Stasilojc G, Gwizdek-Wisniewska A, Marczak L, Stobiecki M, Bigda J, Lojkowska E. 2007. Induction of apoptosis by plumbagin through reactive oxygen species-mediated inhibition of topoisomerase II. Toxicol Appl Pharmacol 223:267-276.
22. Kil IS, Kim SY, Park JW. 2008. Glutathionylation regulates IkappaB. Biochem Biophys Res Commun 373:169-173.
23. Klemke M, Samstag Y. 2009. Molecular mechanisms mediating oxidative stress-induced T-cell suppression in cancer. Adv Enzyme Regul 49:107-112.
24. Krishnaswamy M, Purushothaman KK. 1980. Plumbagin: A study of its anticancer, antibacterial & antifungal properties. Indian J Exp Biol 18:876-877.
25. Lahdenpohja N, Savinainen K, Hurme M. 1998. Pre-exposure to oxidative stress decreases the nuclear factor-kappa B-dependent transcription in T lymphocytes. J Immunol 160:1354-1358.
26. Malmberg KJ, Arulampalam V, Ichihara F, Petersson M, Seki K, Andersson T, Lenkei R, Masucci G, Pettersson S, Kiessling R. 2001. Inhibition of activated/memory (CD45RO(+)) T cells by oxidative stress associated with block of NF-kappaB activation. J Immunol 167:2595-2601.
27. Naresh RA, Udupa N, Devi PU. 1996. Niosomal plumbagin with reduced toxicity and improved anticancer activity in BALB/C mice. J Pharm Pharmacol 48:1128-1132.
28. Naughton R, Quiney C, Turner SD, Cotter TG. 2009. Bcr-Abl-mediated redox regulation of the PI3K/AKT pathway. Leukemia 23:1432-1440.
29. Padhye SB, Kulkarni BA. 1973. Studies on the root constituents of Plumbago zeylanica. J Univ Poona Sci Technol 44:27.
30. Pahlavani MA, Harris MD. 1998. Effect of in vitro generation of oxygen free radicals on T cell function in young and old rats. Free Radic Biol Med 25:903-913.
31. Plummer JL, Smith BR, Sies H, Bend JR. 1981. Chemical depletion of glutathione in vivo. Methods Enzymol 77:50-59.
32. Raghu R, Sharma D, Ramakrishnan R, Khanam S, Chintalwar GJ, Sainis KB. 2009. Molecular events in the activation of B cells and macrophages by a non-microbial TLR4 agonist, G1-4A from Tinospora cordifolia. Immunol Lett 123:60-71.
33. Reynaert NL, van der Vliet A, Guala AS, McGovern T, Hristova M, Pantano C, Heintz NH, Heim J, Ho YS, Matthews DE, Wouters EF, Janssen-Heininger YM. 2006. Dynamic redox control of NF-kappaB through glutaredoxin-regulated S-glutathionylation of inhibitory kappaB kinase beta. Proc Natl Acad Sci USA 103:13086-13091.
34. Sandur SK, Ichikawa H, Sethi G, Ahn KS, Aggarwal BB. 2006. Plumbagin (5-hydroxy-2-methyl-1,4-naphthoquinone) suppresses NF-kappaB activation and NF-kappaB-regulated gene products through modulation of p65 and IkappaBalpha kinase activation, leading to potentiation of apoptosis induced by cytokine and chemotherapeutic agents. J Biol Chem 281:17023-17033.
35. Sharma D, Kumar SS, Raghu R, Khanam S, Sainis KB. 2007a. Differential modulation of mitogen driven proliferation and homeostasis driven proliferation of T cells by rapamycin, Ly294002 and chlorophyllin. Mol Immunol 44:2831-2840. (Pubitemid 46420604)
36. Sharma D, Kumar SS, Sainis KB. 2007b. Antiapoptotic and immunomodulatory effects of chlorophyllin. Mol Immunol 44:347-359.
37. Sharma D, Kumar SS, Checker R, Raghu R, Khanam S, Krishnan S, Sainis KB. 2009. Spatial distribution, kinetics, signaling and cytokine production during homeostasis driven proliferation of CD4+ T cells. Mol Immunol 46:2403-2412.
38. Singh UV, Udupa N. 1997. Reduced toxicity and enhanced antitumor efficacy of betacyclodextrin plumbagin inclusion complex in mice bearing Ehrlich ascites carcinoma. Indian J Physiol Pharmacol 41:171-175. (Pubitemid 27217473)
39. Smart DK, Ortiz KL, Mattson D, Bradbury CM, Bisht KS, Sieck LK, Brechbiel MW, Gius D. 2004. Thioredoxin reductase as a potential molecular target for anticancer agents that induce oxidative stress. Cancer Res 64:6716-6724. (Pubitemid 39297934)
40. Son TG, Camandola S, Arumugam TV, Cutler RG, Telljohann RS, Mughal MR, Moore TA, Luo W, Yu Q-S, Johnson DA, Johnson JA, Greig NH, Mattson MP. 2010. Plumbagin, a novel Nrf2/RAE activator, protects against cerebral ischemia. J Neurochem 112:1316-1326.
41. Srinivas P, Gopinath G, Banerji A, Dinakar A, Srinivas G. 2004. Plumbagin induces reactive oxygen species, which mediate apoptosis in human cervical cancer cells. Mol Carcinog 40:201-211. (Pubitemid 39056312)
42. Sullivan DM, Wehr NB, Fergusson MM, Levine RL, Finkel T. 2000. Identification of oxidant-sensitive proteins: TNF-alpha induces protein glutathiolation. Biochemistry 39:11121-11128.
43. Takada Y, Aggarwal BB. 2003. Betulinic acid suppresses carcinogen-induced NF-kappa B activation through inhibition of I kappa B alpha kinase and p65 phosphorylation: Abrogation of cyclooxygenase-2 and matrix metalloprotease-9. J Immunol 171:3278-3286. (Pubitemid 37093555)
44. Tilak JC, Adhikari S, Devasagayam TP. 2004. Antioxidant properties of Plumbago zeylanica, an Indian medicinal plant and its active ingredient, plumbagin. Redox Rep 9:219-227. (Pubitemid 39462151)
45. Winterbourn CC, Hampton MB. 2008. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45:549-561.
46. Ying J, Clavreul N, Sethuraman M, Adachi T, Cohen RA. 2007. Thiol oxidation in signaling and response to stress: Detection and quantification of physiological and pathophysiological thiol modifications. Free Radic Biol Med 43:1099-1108. (Pubitemid 47374443)
47. Zhang DD, Hannink M. 2003. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol 23:8137-8151.