Leishmania donovani isolates with antimony-resistant but not -sensitive phenotype inhibit sodium antimony gluconate-induced dendritic cell activation

PLoS Pathogens

Volumn 6, Issue 5, 2010, Pages 1-21

  Haldar, Arun Kumar ^a   Yadav, Vinod ^b   Singhal, Eshu ^b   Bisht, Kamlesh Kumar ^b,c   Singh, Alpana ^b   Bhaumik, Suniti ^a   Basu, Rajatava ^a   Sen, Pradip ^b   Roy, Syamal ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMONY GLUCONATE; GLUTAMATE CYSTEINE LIGASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; MULTIDRUG RESISTANCE PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; ANTIPROTOZOAL AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROTOZOAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DRUG SENSITIVITY; FEMALE; HOST PARASITE INTERACTION; IN VITRO STUDY; LEISHMANIA DONOVANI; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE IMMUNITY; PARASITE ISOLATION; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; DRUG EFFECT; DRUG RESISTANCE; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HAMSTER; IMMUNOLOGY; METABOLISM; PARASITOLOGY; SYRIAN HAMSTER; VISCERAL LEISHMANIASIS;

LEISHMANIA DONOVANI; MURINAE; NASO HEXACANTHUS;

ANIMALS; ANTIMONY SODIUM GLUCONATE; ANTIPROTOZOAL AGENTS; CRICETINAE; DENDRITIC CELLS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION; GLUTAMATE-CYSTEINE LIGASE; HOST-PARASITE INTERACTIONS; INTERLEUKIN-10; LEISHMANIA DONOVANI; LEISHMANIASIS, VISCERAL; MALE; MESOCRICETUS; MICE; MICE, INBRED BALB C; NF-KAPPA B; PHENOTYPE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 77954160377     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000907     Document Type: Article

References (65)

1. Lira R, Sundar S, Makharia A, Kenney R, Gam A, et al. (1999) Evidence that the high incidence of treatment failures in Indian kala-azar is due to the emergence of antimony-resistant strains of Leishmania donovani. J Infect Dis 180: 564-567.
2. Croft SL, Sundar S, Fairlamb AH (2006) Drug resistance in leishmaniasis. Clin Microbiol Rev 19: 111-126.
3. Ashutosh, Sundar S, Goyal N (2007) Molecular mechanisms of antimony resistance in Leishmania. J Med Microbiol 56: 143-153.
4. Carter KC, Hutchison S, Henriquez FL, Legare D, Ouellette M, et al. (2006) Resistance of Leishmania donovani to sodium stibogluconate is related to the expression of host and parasite gamma-glutamylcysteine synthetase. Antimicrob Agents Chemother 50: 88-95.
5. Mukherjee A, Padmanabhan PK, Singh S, Roy G, Girard I, et al. (2007) Role of ABC transporter MRPA, gamma-glutamylcysteine synthetase and ornithine decarboxylase in natural antimony-resistant isolates of Leishmania donovani. J Antimicrob Chemother 59: 204-211.
6. Decuypere S, Rijal S, Yardley V, De Doncker S, Laurent T, et al. (2005) Gene expression analysis of the mechanism of natural Sb(V) resistance in Leishmania donovani isolates from Nepal. Antimicrob Agents Chemother 49: 4616-4621.
7. Carter KC, Sundar S, Spickett C, Pereira OC, Mullen AB (2003) The in vivo susceptibility of Leishmania donovani to sodium stibogluconate is drug specific and can be reversed by inhibiting glutathione biosynthesis. Antimicrob Agents Chemother 47: 1529-1535.
8. Thakur CP, Mitra DK, Narayan S (2003) Skewing of cytokine profiles towards T helper cell type 2 response in visceral leishmaniasis patients unresponsive to sodium antimony gluconate. Trans R Soc Trop Med Hyg 97: 409-412.
9. Narayan S, Bimal S, Singh SK, Gupta AK, Singh VP, et al. (2009) Leishmania donovani vs immunity: T-cells sensitized from Leishmania of one donor may modulate their cytokines pattern on re-stimulation with Leishmania from different donor in visceral leishmaniasis. Exp Parasitol 121: 69-75.
10. Murray HW, Delph-Etienne S (2000) Roles of endogenous gamma interferon and macrophage microbicidal mechanisms in host response to chemotherapy in experimental visceral leishmaniasis. Infect Immun 68: 288-293.
11. Murray HW, Montelibano C, Peterson R, Sypek JP (2000) Interleukin-12 regulates the response to chemotherapy in experimental visceral Leishmaniasis. J Infect Dis 182: 1497-1502.
12. Gorak PM, Engwerda CR, Kaye PM (1998) Dendritic cells, but not macrophages, produce IL-12 immediately following Leishmania donovani infection. Eur J Immunol 28: 687-695.
13. Suzue K, Kobayashi S, Takeuchi T, Suzuki M, Koyasu S (2008) Critical role of dendritic cells in determining the Th1/Th2 balance upon Leishmania major infection. Int Immunol 20: 337-343.
14. Bennett CL, Misslitz A, Colledge L, Aebischer T, Blackburn CC (2001) Silent infection of bone marrow-derived dendritic cells by Leishmania mexicana amastigotes. Eur J Immunol 31: 876-883.
15. Rescigno M, Martino M, Sutherland CL, Gold MR, Ricciardi-Castagnoli P (1998) Dendritic cell survival and maturation are regulated by different signaling pathways. J Exp Med 188: 2175-2180.
16. Poligone B, Weaver DJ, Jr., Sen P, Baldwin AS, Jr., Tisch R (2002) Elevated NFkappaB activation in nonobese diabetic mouse dendritic cells results in enhanced APC function. J Immunol 168: 188-196.
17. Ouaaz F, Arron J, Zheng Y, Choi Y, Beg AA (2002) Dendritic cell development and survival require distinct NF-kappaB subunits. Immunity 16: 257-270.
18. Weaver DJ, Jr., Poligone B, Bui T, Abdel-Motal UM, Baldwin AS, Jr., et al. (2001) Dendritic cells from nonobese diabetic mice exhibit a defect in NFkappaB regulation due to a hyperactive IkappaB kinase. J Immunol 167: 1461-1468.
19. Bhattacharyya S, Sen P, Wallet M, Long B, Baldwin AS, Jr., et al. (2004) Immunoregulation of dendritic cells by IL-10 is mediated through suppression of the PI3K/Akt pathway and of IkappaB kinase activity. Blood 104: 1100-1109.
20. Sen P, Wallet MA, Yi Z, Huang Y, Henderson M, et al. (2007) Apoptotic cells induce Mer tyrosine kinase-dependent blockade of NF-kappaB activation in dendritic cells. Blood 109: 653-660.
21. Ghosh S, Karin M (2002) Missing pieces in the NF-kappaB puzzle. Cell 109 Suppl: S81-96.
22. Karin M (1999) How NF-kappaB is activated: the role of the IkappaB kinase (IKK) complex. Oncogene 18: 6867-6874.
23. Madrid LV, Wang CY, Guttridge DC, Schottelius AJ, Baldwin AS, Jr., et al. (2000) Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-kappaB. Mol Cell Biol 20: 1626-1638.
24. Guha M, Mackman N (2002) The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J Biol Chem 277: 32124-32132.
25. Mookerjee Basu J, Mookerjee A, Sen P, Bhaumik S, Banerjee S, et al. (2006) Sodium antimony gluconate induces generation of reactive oxygen species and nitric oxide via phosphoinositide 3-kinase and mitogen-activated protein kinase activation in Leishmania donovani-infected macrophages. Antimicrob Agents Chemother 50: 1788-1797.
26. Barat C, Zhao C, Ouellette M, Tremblay MJ (2007) HIV-1 replication is stimulated by sodium stibogluconate, the therapeutic mainstay in the treatment of leishmaniasis. J Infect Dis 195: 236-245.
27. Kurozumi R, Kojima S (2005) Increase of intracellular glutathione by low-level NO mediated by transcription factor NF-kappaB in RAW 264.7 cells. Biochim Biophys Acta 1744: 58-67.
28. Tejle K, Lindroth M, Magnusson KE, Rasmusson B (2008) Wild-type Leishmania donovani promastigotes block maturation, increase integrin expression and inhibit detachment of human monocyte-derived dendritic cells-the influence of phosphoglycans. FEMS Microbiol Lett 279: 92-102.
29. Marovich MA, McDowell MA, Thomas EK, Nutman TB (2000) IL-12p70 production by Leishmania major-harboring human dendritic cells is a CD40/CD40 ligand-dependent process. J Immunol 164: 5858-5865.
30. Ato M, Stager S, Engwerda CR, Kaye PM (2002) Defective CCR7 expression on dendritic cells contributes to the development of visceral leishmaniasis. Nat Immunol 3: 1185-1191.
31. Donovan MJ, Jayakumar A, McDowell MA (2007) Inhibition of groups 1 and 2 CD1 molecules on human dendritic cells by Leishmania species. Parasite Immunol 29: 515-524.
32. Cai J, Huang ZZ, Lu SC (1997) Differential regulation of gammaglutamylcysteine synthetase heavy and light subunit gene expression. Biochem J 326: 167-172.
33. Qi H, Popov V, Soong L (2001) Leishmania amazonensis-dendritic cell interactions in vitro and the priming of parasite-specific CD4(+) T cells in vivo. J Immunol 167: 4534-4542.
34. Murphy ML, Wille U, Villegas EN, Hunter CA, Farrell JP (2001) IL-10 mediates susceptibility to Leishmania donovani infection. Eur J Immunol 31: 2848-2856.
35. Murray HW, Lu CM, Mauze S, Freeman S, Moreira AL, et al. (2002) Interleukin-10 (IL-10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy. Infect Immun 70: 6284-6293.
36. Dobrovolskaia MA, Medvedev AE, Thomas KE, Cuesta N, Toshchakov V, et al. (2003) Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophages: effects of TLR "homotolerance" versus "heterotolerance" on NF-kappaB signaling pathway components. J Immunol 170: 508-519.
37. Whiteside ST, Epinat JC, Rice NR, Israel A (1997) IkappaB epsilon, a novel member of the IkappaB family, controls RelA and cRel NF-kappaB activity. EMBO J 16: 1413-1426.
38. Kearns JD, Basak S, Werner SL, Huang CS, Hoffmann A (2006) IkappaB epsilon provides negative feedback to control NF-kappaB oscillations, signaling dynamics, and inflammatory gene expression. J Cell Biol 173: 659-664.
39. Laskov R, Berger N, Horwitz MS (2005) Differential effects of tumor necrosis factor-alpha and CD40L on NF-kappaB inhibitory proteins IkappaB alpha, beta and epsilon and on the induction of the Jun amino-terminal kinase pathway in Ramos Burkitt lymphoma cells. Eur Cytokine Netw 16: 267-276.
40. Zhao C, Cantin R, Breton M, Papadopoulou B, Tremblay MJ (2005) DCSIGN-mediated transfer of HIV-1 is compromised by the ability of Leishmania infantum to exploit DC-SIGN as a ligand. J Infect Dis 191: 1665-1669.
41. Pepe M, Altamura M, Spinelli R, Calvello R, Saccia M, et al. (2006) Toll-like receptor-positive cells and recognition of pathogens: how human myeloid dendritic cells respond to in vitro infection with Leishmania infantum. Curr Pharm Des 12: 4255-4262.
42. Garg R, Barat C, Ouellet M, Lodge R, Tremblay MJ (2009) Leishmania infantum Amastigotes Enhance HIV-1 Production in Cocultures of Human Dendritic Cells and CD4 T ells by Inducing Secretion of IL-6 and TNF-alpha. PLoS Negl Trop Dis 3: e441.
43. Chulay JD, Fleckenstein L, Smith DH (1988) Pharmacokinetics of antimony during treatment of visceral leishmaniasis with sodium stibogluconate or meglumine antimoniate. Trans R Soc Trop Med Hyg 82: 69-72.
44. Singh R, Kumar D, Ramesh V, Negi NS, Singh S, et al. (2006) Visceral leishmaniasis, or kala azar (KA): high incidence of refractoriness to antimony is contributed by anthroponotic transmission via post-KA dermal leishmaniasis. J Infect Dis 194: 302-306.
45. Singh N, Singh RT, Sundar S (2003) Novel mechanism of drug resistance in kala azar field isolates. J Infect Dis 188: 600-607.
46. Cuevas B, Lu Y, Watt S, Kumar R, Zhang J, et al. (1999) SHP-1 regulates Lckinduced phosphatidylinositol 3-kinase phosphorylation and activity. J Biol Chem 274: 27583-27589.
47. Pathak MK, Yi T (2001) Sodium stibogluconate is a potent inhibitor of protein tyrosine phosphatases and augments cytokine responses in hemopoietic cell lines. J Immunol 167: 3391-3397.
48. Corinti S, Albanesi C, la Sala A, Pastore S, Girolomoni G (2001) Regulatory activity of autocrine IL-10 on dendritic cell functions. J Immunol 166: 4312-4318.
49. Kothari H, Kumar P, Sundar S, Singh N (2007) Possibility of membrane modification as a mechanism of antimony resistance in Leishmania donovani. Parasitol Int 56: 77-80.
50. Samant M, Sahasrabuddhe AA, Singh N, Gupta SK, Sundar S, et al. (2007) Proteophosphoglycan is differentially expressed in sodium stibogluconatesensitive and resistant Indian clinical isolates of Leishmania donovani. Parasitology 134: 1175-1184.
51. Kumar A, Boggula VR, Sundar S, Shasany AK, Dube A (2009) Identification of genetic markers in sodium antimony gluconate (SAG) sensitive and resistant Indian clinical isolates of Leishmania donovani through amplified fragment length polymorphism (AFLP). Acta Trop 110: 80-85.
52. Mollah ZU, Pai S, Moore C, O'Sullivan BJ, Harrison MJ, et al. (2008) Abnormal NF-kappaB function characterizes human type 1 diabetes dendritic cells and monocytes. J Immunol 180: 3166-3175.
53. Thakur CP, Thakur S, Narayan S, Sinha A (2008) Comparison of treatment regimens of kala-azar based on culture & sensitivity of amastigotes to sodium antimony gluconate. Indian J Med Res 127: 582-588.
54. Ameen M (2009) Cutaneous leishmaniasis: disease susceptibility and pharmacogenetic implications. Pharmacogenomics 10: 451-461.
55. Mukhopadhyay R, Madhubala R (1994) 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: 253-256.
56. Basu R, Bhaumik S, Basu JM, Naskar K, De T, et al. (2005) 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: 7160-7171.
57. Singh N, Almeida R, Kothari H, Kumar P, Mandal G, et al. (2007) Differential gene expression analysis in antimony-unresponsive Indian kala azar (visceral leishmaniasis) clinical isolates by DNA microarray. Parasitology 134: 777-787.
58. Hart DT, Vickerman K, Coombs GH (1981) A quick, simple method for purifying Leishmania mexicana amastigotes in large numbers. Parasitology 82: 345-355.
59. Chakraborty D, Banerjee S, Sen A, Banerjee KK, Das P, et al. (2005) Leishmania donovani affects antigen presentation of macrophage by disrupting lipid rafts. J Immunol 175: 3214-3224.
60. Dube A, Singh N, Sundar S (2005) Refractoriness to the treatment of sodium stibogluconate in Indian kala-azar field isolates persist in in vitro and in vivo experimental models. Parasitol Res 96: 216-223.
61. Beg AA, Finco TS, Nantermet PV, Baldwin AS, Jr. (1993) Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of IkappaB alpha: a mechanism for NF-kappaB activation. Mol Cell Biol 13: 3301-3310.
62. Murphy TL, Cleveland MG, Kulesza P, Magram J, Murphy KM (1995) Regulation of interleukin 12 p40 expression through an NF-kappaB half-site. Mol Cell Biol 15: 5258-5267.
63. Lee CH, Melchers M, Wang H, Torrey TA, Slota R, et al. (2006) Regulation of the germinal center gene program by interferon (IFN) regulatory factor 8/IFN consensus sequence-binding protein. J Exp Med 203: 63-72.
64. Schmid JA, Birbach A, Hofer-Warbinek R, Pengg M, Burner U, et al. (2000) Dynamics of NF-kappaB and IkappaB alpha studied with green fluorescent protein (GFP) fusion proteins. Investigation of GFP-p65 binding to DNA by fluorescence resonance energy transfer. J Biol Chem 275: 17035-17042.
65. Judge AR, Koncarevic A, Hunter RB, Liou HC, Jackman RW, et al. (2007) Role for IkappaBalpha, but not c-Rel, in skeletal muscle atrophy. Am J Physiol Cell Physiol 292: C372-382.