Sub-optimal dose of Sodium Antimony Gluconate (SAG)-diperoxovanadate combination clears organ parasites from BALB/c mice infected with antimony resistant Leishmania donovani by expanding antileishmanial T-cell repertoire and increasing IFN-γ to IL-10 ratio

Experimental Parasitology

Volumn 122, Issue 2, 2009, Pages 145-154

  Haldar, Arun Kumar ^a   Banerjee, Subha ^a   Naskar, Kshudiram ^a   Kalita, Diganta ^b   Islam, Nashreen S ^b   Roy, Syamal ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b TEZPUR UNIVERSITY   (India)

Author keywords

Antileishmanial T cell; Leishmania; Peroxovanadate (PV); Sodium Antimony Gluconate (SAG)

Indexed keywords

ANTILEISHMANIAL AGENT; ANTIMONY GLUCONATE; DIPEROXOVANADATE; GAMMA INTERFERON; INTERLEUKIN 10; NITRIC OXIDE; SUPEROXIDE; UNCLASSIFIED DRUG; VANADIUM DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ANTIPROTOZOAL ACTIVITY; ARTICLE; BAGG ALBINO MOUSE; CONTROLLED STUDY; CYTOTOXICITY TEST; DRUG EFFICACY; EXPERIMENTAL INFECTION; IN VITRO STUDY; LEISHMANIA DONOVANI; MOUSE; NONHUMAN; OPTIMAL DRUG DOSE; PRIORITY JOURNAL; SPLEEN CELL; STRUCTURE ACTIVITY RELATION; T LYMPHOCYTE; THERAPY EFFECT; TREATMENT OUTCOME; TREATMENT RESPONSE; VISCERAL LEISHMANIASIS;

ANIMALS; ANTIMONY SODIUM GLUCONATE; ANTIPROTOZOAL AGENTS; ASCITIC FLUID; CELL SURVIVAL; CRICETINAE; DRUG COMBINATIONS; DRUG RESISTANCE; INTERFERON-GAMMA; INTERLEUKIN-10; LEISHMANIA DONOVANI; LEISHMANIASIS, VISCERAL; LIVER; MESOCRICETUS; MICE; MICE, INBRED BALB C; NITRIC OXIDE; PEROXIDES; SPLEEN; SUPEROXIDES; T-LYMPHOCYTES; VANADATES;

ANIMALIA; LEISHMANIA DONOVANI; MUS;

EID: 67349237187     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2009.02.001     Document Type: Article

References (57)

1. Amer A.O., and Swanson M.S. Phagosome of one's own: a microbial guide to life in the macrophage. Curr. Opin. Microbiol. 5 (2002) 56-61
2. Barbeau B., Bernier R., Dumais N., Briand G., Olivier M., Faure R., Posner B.I., and Tremblay M. Activation of HIV-1 long terminal repeat transcription and virus replication via NF-kappaB-dependent and independent pathways by potent phosphotyrosine phosphatase inhibitors, the peroxovanadium compounds. J. Biol. Chem. 272 (1997) 12968-12977
3. Basu R., Bhaumik S., Basu J.M., Naskar K., De T., and Roy S. Kinetoplastid membrane protein-11 DNA vaccination induces complete protection against both pentavalent antimonial-sensitive and -resistant strains of Leishmania donovani that correlates with inducible nitric oxide synthase activity and IL-4 generation: evidence for mixed Th1- and Th2-like responses in visceral leishmaniasis. J. Immunol. 174 (2005) 7160-7171
4. Basu R., Bhaumik S., Haldar A.K., Naskar K., De T., Dana S.K., Walden P., and Roy S. Hybrid cell vaccination resolves Leishmania donovani infection by eliciting strong CD8+CTL response with concomitant suppression of IL-10 but not IL-4 and IL-13. Infect. Immun. 75 (2007) 5956-5966
5. Berman J.D. Human leishmaniasis: clinical, diagnostic, and chemotherapeutic developments in the last 10 years. Clin. Infect. Dis. 24 (1997) 684-703
6. Bevan A.P., Burgess J.W., Yale J.F., Drake P.G., Lachance D., Baquiran G., Shaver A., and Posner B.I. In vivo insulin mimetic effects of pV compounds: role for tissue targeting in determining potency. Am. J. Physiol. 268 (1995) E60-E66
7. Cantley L.C., Josephson L., Warner R., Yanagisawa M., Lechene C., and Guidotti G. Vanadate is a potent (Na, K)-ATPase inhibitor found in ATP derived from muscle. J. Biol. Chem. 252 (1977) 7421-7423
8. Chakrabarti G., Basu A., Manna P.P., Mahato S.B., Mandal N.B., and Bandyopadhyay S. Indolylquinoline derivatives are cytotoxic to Leishmania donovani promastigotes and amastigotes in vitro and are effective in treating murine visceral leishmaniasis. J. Antimicrob. Chemother. 43 (1999) 359-366
9. Chakraborty D., Banerjee S., Sen A., Banerjee K.K., Das P., and Roy S. Leishmania donovani affects antigen presentation of macrophage by disrupting lipid rafts. J. Immunol. 175 (2005) 3214-3224
10. Croft S.L., and Coombs G.H. Leishmaniasis-current chemotherapy and recent advances in the search for novel drugs. Trends. Parasitol. 19 (2003) 502-508
11. Croft S.L., and Yardley V. Chemotherapy of leishmaniasis. Curr. Pharm. Des. 8 (2002) 319-342
12. Davison S., Allen M., Vaughan R., and Barker J. Staphylococcal toxin-induced T cell proliferation in atopic eczema correlates with increased use of superantigen-reactive Vβ-chains in cutaneous lymphocyte-associated antigen (CLA)-positive lymphocytes. Clin. Exp. Immunol. 121 (2000) 181-186
13. de Boer E., Van Kooyk Y., Tromp M.G.M., and Wever R. Bromoperoxidase from Ascophyllum nodosum: a novel class of enzymes containing vanadium as a prosthetic group. Biochem. Biophys. Acta 869 (1986) 48-53
14. Di Gioacchino M., Sabbioni E., Di Giampaolo L., Schiavone C., Di Sciascio M.B., Reale M., Nicola V., Qiao N., Paganelli R., Conti P., and Boscolo P. In vitro effects of vanadate on human immune functions. Ann. Clin. Lab. Sci. 32 (2002) 148-154
15. Evangelou A.M. Vanadium in cancer treatment. Crit. Rev. Oncol. Hematol. 42 (2002) 249-265
16. Faraut-Gambarelli F., Piarroux R., Deniau M., Giusiano B., Marty P., Michel G., Faugere B., and Dumon H. In vitro and in vivo resistance of Leishmania infantum to meglumine antimoniate: a study of 37 strains collected from patients with visceral leishmaniasis. Antimicrob. Agents Chemother. 41 (1997) 827-830
17. Ghalib H.W., Piuvezam M.R., Skeiky Y.A., Siddig M., Hashim F.A., el-Hassan A.M., Russo D.M., and Reed S.G. Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J. Clin. Invest. 92 (1993) 324-329
18. Huang C., Ding M., Li J., Leonard S.S., Rojanasakul Y., Castranova V., Vallyathan V., Ju G., and Shi X. Vanadium-induced nuclear factor of activated T cells activation through hydrogen peroxide. J. Biol. Chem. 276 (2001) 22397-22403
19. Jaspers I., Samet J.M., Erzurum S., and Reed W. Vanadium-induced kB-dependent transcription depends upon peroxide-induced activation of the p38 mitogen-activated protein kinase. Am. J. Respir. Cell Mol. Biol. 23 (2000) 95-102
20. Jha T.K. Drug unresponsiveness & combination therapy for kala-azar. Indian J. Med. Res. 123 (2006) 389-398
21. Kang K.W., Cho M.K., Lee C.H., and Kim S.G. Activation of phosphatidylinositol 3-kinase and Akt by tert-butylhydroquinone is responsible for antioxidant response element-mediated rGSTA2 induction in H4IIE cells. Mol. Pharmacol. 59 (2001) 1147-1156
22. Karp C.L., el-Safi S.H., Wynn T.A., Satti M.M., Kordofani A.M., Hashim F.A., Hag-Ali M., Neva F.A., Nutman T.B., and Sacks D.L. In vivo cytokine profiles in patients with kala-azar. Marked elevation of both interleukin-10 and interferon-gamma. J. Clin. Invest. 91 (1993) 1644-1648
23. Kaye P.M., Curry A.J., and Blackwell J.M. Differential production of Th1- and Th2-derived cytokines does not determine the genetically controlled or vaccine-induced rate of cure in murine visceral leishmaniasis. J. Immunol. 146 (1991) 2763-2770
24. Matte C., Marquis J.F., Blanchette J., Gros P., Faure R., Posner B.I., and Olivier M. Peroxovanadium-mediated protection against murine leishmaniasis: role of the modulation of nitric oxide. Eur. J. Immunol. 30 (2000) 2555-2564
25. Melby P.C., Chandrasekar B., Zhao W., and Coe J.E. The hamster as a model of human visceral leishmaniasis: progressive disease and impaired generation of nitric oxide in the face of a prominent Th1-like cytokine response. J. Immunol. 166 (2001) 1912-1920
26. Mookerjee Basu J., Mookerjee A., Banerjee R., Saha M., Singh S., Naskar K., Tripathy G., Sinha P.K., Pandey K., Sundar S., Bimal S., Das P.K., Choudhuri S.K., and Roy S. Inhibition of ABC transporters abolishes antimony resistance in Leishmania infection. Antimicrob. Agents Chemother. 52 (2008) 1080-1093
27. Mukhopadhyay R., and Madhubala R. Antileishmanial activity and modification of hepatic xenobiotic metabolizing enzymes in golden hamster by 2(3)-tert-butyl-4-hydroxyanisole following infection with Leishmania donovani. Biochem. Pharmacol. 47 (1994) 253-256
28. Murray H.W., Berman J.D., and Wright S.D. Immunochemotherapy for intracellular Leishmania donovani infection: gamma interferon plus pentavalent antimony. J. Infect. Dis. 157 (1988) 973-978
29. Olivier M., Romero-Gallo B.J., Matte C., Blanchette J., Posner B.I., Tremblay M.J., and Faure R. Modulation of interferon-gamma-induced macrophage activation by phosphotyrosine phosphatases inhibition. Effect on murine Leishmaniasis progression. J. Biol. Chem. 273 (1998) 13944-13949
30. Ouellette M., and Papadopoulou B. Mechanisms of drug resistance in Leishmania. Parasitol. Today 9 (1993) 150-153
31. Pathak M.K., and Yi T. Sodium stibogluconate is a potent inhibitor of protein tyrosine phosphatases and augments cytokine responses in hemopoietic cell lines. J. Immunol. 167 (2001) 3391-3397
32. Pérez-Victoria J.M., Pérez-Victoria F.J., Conseil G., Maitrejean M., Comte G., Barron D., Di Pietro A., Castanys S., and Gamarro F. High-affinity binding of silybin derivatives to the nucleotide-binding domain of a Leishmania tropica P-glycoprotein-like transporter and chemosensitization of a multidrug-resistant parasite to daunomycin. Antimicrob. Agents Chemother. 45 (2001) 439-446
33. Posner B.I., Faure R., Burgess J.W., Bevan A.P., Lachance D., Zhang-Sun G., Fantus I.G., Ng J.B., Hall D.A., Lum B.S., and Shaver A. Peroxovanadium compounds. A new class of potent phosphotyrosine phosphatase inhibitors, which are insulin mimetics. J. Biol. Chem. 269 (1994) 4596-4604
34. 2 in presence of abundant catalase. Biochim. Biophys. Acta 1381 (1998) 249-255
35. Ravishankar H.N., Chaudhuri M.K., and Ramasarma T. Oxygen-exchange reactions accompanying oxidation of vanadyl sulfate by diperoxovanadate. Inorg. Chem. 33 (1994) 3788-3793
36. Ravishankar H.N., and Ramasarma T. Requirement of a diperoxovanadate-derived intermediate for the interdependent oxidation of vanadyl and NADH. Arch. Biochem. Biophys. 316 (1995) 319-326
37. Rehder D. The coordination chemistry of vanadium as related to its biological functions. Coord. Chem. Rev. 182 (1999) 297-322
38. Roy S., Scherer M.T., Briner T.J., Smith J.A., and Gefter M.L. Murine MHC polymorphism and T cell specificities. Science 244 (1989) 572-575
39. Russo D.M., Chakrabarti P., and Burns Jr. J.M. Naive human T cells develop into Th1 or Th0 effectors and exhibit cytotoxicity early after stimulation with Leishmania-infected macrophages. J. Infect. Dis. 177 (1998) 1345-1351
40. Saha S., Mondal S., Ravindran R., Bhowmick S., Modak D., Mallick S., Rahman M., Kar S., Goswami R., Guha S.K., Pramanik N., Saha B., and Ali N. IL-10- and TGF-β-mediated susceptibility in kala-azar and post-kala-azar dermal Leishmaniasis: the significance of Amphotericin B in the control of Leishmania donovani infection in India. J. Immunol. 179 (2007) 5592-5603
41. Sarmah S., Hazarika P., Islam N.S., Rao A.V.S., and Ramasarma T. Peroxo-bridged divanadate as selective bromide oxidant in bromoperoxidation. Mol. Cell. Biochem. 236 (2002) 95-105
42. Sarmah S., Hazarika P., and Islam N.S. Reaction of diperoxovanadate with vanadyl sulphate in presence of EDTA as an access to dinuclear peroxovanadates(V). Polyhedron 21 (2002) 389-394
43. Sarmah S., Kalita D., Hazarika P., Borah R., and Islam N.S. Synthesis of new dinuclear and mononuclear peroxovanadium(V) complexes containing biogenic co-ligands: a comparative study of some of their properties. Polyhedron 23 (2004) 1097-1107
44. Schwab J.H. Suppression of the immune response by microorganisms. American society for microbiology. Bacteriol. Rev. 39 (1975) 121-143
45. Silvestre R., Corderio-Da-Silva A., Santarem N., Vergnes R., Sereno D., and Ouaissi A. SIR2-deficient Leishmania infantum induces a defined IFN-gamma/IL-10 pattern that correlates with protection. J. Immunol. 179 (2007) 3161-3170
46. Stauber L.A. Immunity to Leishmaniasis. Ann. N. Y. Acad. Sci. 113 (1963) 409-417
47. Stober C.B., Lange U.G., Roberts M.T.M., Alcami A., and Blackwell J.M. IL-10 from regulatory T cells determines vaccine efficacy in murine Leishmania major infection 1. J. Immunol. 175 (2005) 2517-2524
48. Sundar S., Jha T.K., Thakur C.P., Engel J., Sindermann H., Fischer C., Junge K., Bryceson A., and Berman J. Oral Miltefosine for Indian visceral leishmaniasis. N. Engl. J. Med. 347 (2002) 1739-1746
49. Thompson K.H., McNeill J.H., and Orvig C. Vanadium compounds as insulin mimics. Chem. Rev. 99 (1999) 2561-2572
50. Thompson K.H., and Orvig C. Design of vanadium compounds as insulin enhancing agents. J. Chem. Soc., Dalton Trans. 17 (2000) 2885-2893
51. Tsiani E., and Fantus I.G. Vanadium compounds: biological actions and potential as pharmacological agents. Trends Endocrinol. Metab. 8 (1997) 51-58
52. Urbatsch I.L., Sankaran B., Weber J., and Senior A.E. P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J. Biol. Chem. 270 (1995) 19383-19390
53. 51V NMR investigation of a vanadate(V)-dependent peroxidase from Ascophyllum nodosum (L.) Le Jol. Inorg. Chim. Acta 136 (1987) L7-L10
54. 12 to amino acid activation. J. Biol. Chem. 233 (1958) 219-224
55. Wang E., Casclano C.N., Clement R.P., and Johnson W.W. In vitro flow cytometry method to quantitatively assess inhibitors of P-glycoprotein. Drug Metabol. Dispos. 28 (2000) 522-528
56. World Health Organization (WHO). 2005. Magnitude of the problem. Available: http://www.who.int/leishmaniasis/burden/magnitude/burden_magnitude/en/index.html.
57. Zhang Z., Gao N., He H., Huang C., Luo J., and Shi X. Vanadate activated Akt and promoted S phase entry. Mol. Cell. Biochem. 255 (2004) 227-237