Skip to main content

Advertisement

Log in

Virulence attenuation of a UDP-galactose/N-acetylglucosamine β1,4 galactosyltransferase expressing Leishmania donovani promastigote

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Protozoan parasites of the genus Leishmania are the causative agent of leishmaniasis, a disease whose manifestations in humans range from mild cutaneous lesions to fatal visceral infections. Human visceral leishmaniasis is caused by Leishmania donovani. Long-term culture in vitro leads to the attenuation of the parasite. This loss of parasite virulence is associated with the expression of a developmentally regulated UDP-Galactose/N-acetylglucosamine β 1–4 galactosyltransferase and galactose terminal glycoconjugates as determined by their agglutination with the pea nut agglutinin (PNA). Thus, all promastigotes passaged for more than 11 times were 100% agglutinated with PNA, and represent a homogeneous population of avirulent parasites. Identical concentrations of PNA failed to agglutinate promastigotes passaged for ≤5 times. These PNA promastigotes were virulent. Promastigotes passaged from 5 to 10 times showed a mixed population. The identity of populations defined by virulence and PNA agglutination was confirmed by isolating PNA+ avirulent and PNA virulent clones from the 7th passage promastigotes. Only the PNA+ clones triggered macrophage microbicidal activity. The PNA+ clones lacked lipophosphoglycan. Intravenous administration of [14C] galactose-labeled parasite in BALB/c mice resulted in rapid clearance of the parasite from blood with a concomitant accumulation in the liver. By enzymatic assay and RT-PCR we have shown the association of a UDP-Galactose/N-acetylglucosamine β1,4 galactosyltransferase with only the attenuated clones. By immunofluorescence we demonstrated that the enzyme is located in the Golgi apparatus. By western blot analysis and SDS-PAGE of the affinity-purified protein, we have been able to identify a 29 KDa galactose terminal protein from the avirulent clones.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

GalT:

UDP-Galactose/N-Acetylglucosamine β1.4 Galactosyltransferase

LD:

Leishmania donovani

V-LD:

virulent Leishmania donovani clone

A-LD:

avirulent Leishmania donovani clone

Mφ:

macrophage

PNA:

pea nut agglutinin

Ab:

antibody

mAb:

monoclonal antibody

RB:

respiratory burst

References

  1. Apweiler, R., Hermjakob, H., Sharon, N.: On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473, 4–8 (1999)

    PubMed  CAS  Google Scholar 

  2. Basu, S., Basu, M., Kyle, J.W., Chon, H.C.: Biosynthesis in vitro of gangliosides containing Gg- and Lc-cores. In: Ledeen, R. (ed.) Gangliosides Structure and Function, pp. 249–261. Plenum Press, New York (1984)

    Google Scholar 

  3. Basu, R., Bhaumik, S., Basu, J.M., Naskar, K., De, T., 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, 7160–7171 (2005)

    PubMed  CAS  Google Scholar 

  4. Basu, M., De, T., Das, K.K., Kyle, J.W., Chon, H.C., Schaeper, R.J., Basu, S.: Glycosyltransferases involved in glycolipid biosynthesis. In: Ginsburg, V. (ed.) Methods in Enzymology, pp. 575–607. Academic Press, New York (1987)

    Google Scholar 

  5. Belen Carrillo, M., Gao, W., Herrera, M., Alroy, J., Moore, J.B., Beverley, S.M., Pereira, M.A.: Heterologous expression of Trypanosoma cruzi trans-sialidase in Leishmania major enhances virulence. Infect. Immun. 68, 2728–2734 (2000)

    Article  PubMed  CAS  Google Scholar 

  6. Beverley, S.M., Turco, S.J.: Lipophosphoglycan (LPG) and the identification of virulence genes in the protozoan parasite Leishmania. Trends. Microbiol. 6, 35–40 (1998)

    Article  PubMed  CAS  Google Scholar 

  7. Blackwell, J.M.: Genetic susceptibility to leishmanial infections: studies in mice and man. Parasitology 112, S67–S74 (1996)

    Article  PubMed  Google Scholar 

  8. Bosques, C.J., Tschampel, S.M., Woods, R.J., Imperiali, B.: Effects of glycosylation on peptide conformation: a synergistic experimental and computational study. J. Am. Chem. Soc. 126, 8421–8425 (2004)

    Article  PubMed  CAS  Google Scholar 

  9. Bradley, D.: Regulation of Leishmania populations within the host. II. genetic control of acute susceptibility of mice to Leishmania donovani infection. Clin. Exp. Immunol. 30, 130–140 (1977)

    PubMed  CAS  Google Scholar 

  10. Brandonisio, O., Panaro, M.A., Marzio, R., Marangi, A., Faliero, S.M., Jirillo, E.: Impairment of the human phagocyte oxidative responses caused Leishmania lipophosphoglycan (LPG): in vitro studies. FEMS Immunol. Med. Microbiol. 8, 57–62 (1994)

    Article  PubMed  CAS  Google Scholar 

  11. Buchmüller-Rouiller, Y., Mauël, J.: Impairment of the oxidative metabolism of mouse peritoneal macrophages by intracellular Leishmania spp. Infect Immun. 55, 587–593 (1987)

    PubMed  Google Scholar 

  12. Capul, A.A., Barron, T., Dobson, D.E., Turco, S.J., Beverley, S.M.: Two functionally divergent UDP-Gal nucleotide sugar transporters participate in phosphoglycan synthesis in Leishmania major. J. Biol. Chem. 282, 14006–14017 (2007)

    Article  PubMed  CAS  Google Scholar 

  13. Charest, H., Matlashewski, G.: Developmental gene expression in Leishmania donovani: differential cloning and analysis of an amastigote-stage-specific gene. Mol. Cell Biol. 14, 2975–2984 (1994)

    PubMed  CAS  Google Scholar 

  14. Colmenares, M., Corbi, A.L., Turco, S.J., Rivas, L.: The dendritic cell receptor DC- SIGN discriminates among species and life cycle forms of Leishmania. J. Immunol. 172, 1186–1190 (2004)

    PubMed  CAS  Google Scholar 

  15. Connaris, S., Greenwell, P.: Glycosidases in mucin-dwelling protozoans. Glycoconj. J. 14, 879–882 (1997)

    Article  PubMed  CAS  Google Scholar 

  16. Crocker, P.R., Varki, A.: Siglecs, sialic acids and innate immunity. Trends Immunol. 22, 337–342 (2001)

    Article  PubMed  CAS  Google Scholar 

  17. Da Silva, R., Sacks, D.L.: Metacyclogenesis is a major determinant of Leishmania promastigotes virulence and attenuation. Infect. Immun. 55, 2802–2806 (1987)

    PubMed  Google Scholar 

  18. De, T., Roy, S.: Infectivity and attenuation of Leishmania donovani promastigotes: association of galactosyl transferase with loss of parasite virulence. J. Parasitol. 85, 54–59 (1999)

    Article  PubMed  CAS  Google Scholar 

  19. Dedet, J.P., Pratlong, F., Lanotte, G., Ravel, C.: Cutaneous leishmaniasis. The parasite. Clin. Dermatol. 17, 261–268 (1999)

    Article  PubMed  CAS  Google Scholar 

  20. Descoteaux, A., Luo, Y., Turco, S.J., Beverley, S.M.: A specialized pathway affecting virulence glycoconjugates of Leishmania. Science 269, 1869–1872 (1995)

    Article  PubMed  CAS  Google Scholar 

  21. Descoteaux, A., Avila, H.A., Zhang, K., Turco, S.J., Beverley, S.M.: Leishmania LPG3 encodes a GRP94 homolog required for phosphoglycan synthesis implicated in parasite virulence but not viability. EMBO J. 21, 4458–4469 (2002)

    Article  PubMed  CAS  Google Scholar 

  22. Esko, J.D., Lindahl, U.: Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169–173 (2001)

    PubMed  CAS  Google Scholar 

  23. Fadden, A.J., Holt, O.J., Drickamer, K.: Molecular characterization of the rat Kupffer cell glycoprotein receptor. Glycobiology 13, 529–537 (2003)

    Article  PubMed  CAS  Google Scholar 

  24. Fang, F.C.: Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 99, 2818–2825 (1997)

    Article  PubMed  CAS  Google Scholar 

  25. Fridovich-Keil, J.L.: Galactosemia: the good, the bad, and the unknown. J. Cellular. Physiol. 209, 701–705 (2006)

    Article  CAS  Google Scholar 

  26. Garami, A., Mehlert, A., Ilg, T.: Glycosylation defects and virulence phenotypes of Leishmania mexicana phosphomannomutase and dolicholphosphate-mannose synthase gene deletion mutants. Mol. Cell. Biol. 21, 8168–8183 (2001)

    Article  PubMed  CAS  Google Scholar 

  27. Gradoni, L., Gramiccia, M.: Leishmania infantum tropism: strain genotype or host immune status? Parasitol. Today 10, 264–267 (1994)

    CAS  Google Scholar 

  28. Gramiccia, M., Gradoni, L., Angelici, M.C.: Epidemiology of Mediterranean leishmaniasis by Leishmania infantum: isoenzyme and kDNA analysis for the identification of parasites from man, vectors and reservoirs. NATO-ASI Ser. A Life. Sci. 1, 21–37 (1989)

    Google Scholar 

  29. Green, S.J., Crawford, R.M., Hockmeyer, J.T., Meltzer, M.S., Nacy, C.A.: Leishmania major amastigotes initiate the L-arginine-dependent killing mechanism in IFN-gamma-stimulated macrophages by induction of tumor necrosis factor-alpha. J. Imminol. 145, 4290–4297 (1990)

    CAS  Google Scholar 

  30. Handman, E., Hocking, R.E.: Stage-specific, strain-specific, and cross-reactive antigens of Leishmania species identified by monoclonal antibodies. Infect. Imm. 37, 28–33 (1982)

    CAS  Google Scholar 

  31. Helenius, A., Aebi, M.: Roles of N-linked glycans in the endoplasmic reticulum. Ann. Rev. Biochem. 73, 1019–1049 (2004)

    Article  PubMed  CAS  Google Scholar 

  32. Ilg, T., Craik, D., Currie, G., Multhaup, G., Bacic, A.: Stage-specific Proteophosphoglycan from Leishmania mexicana Amastigotes. Structural characterization of novel mono-, di-, and triphosphorylated phosphodiester-linked oligosaccharides. J. Biol. Chem. 273, 13509–13523 (1998)

    Article  PubMed  CAS  Google Scholar 

  33. Jacobson, R.L., Schlein, Y.: Phlebotomus papatasi and Leishmania major parasites express alpha-amylase and alpha-glucosidase. Acta Trop. 78, 41–49 (2001)

    Article  PubMed  CAS  Google Scholar 

  34. Jiménez, M., Ferrer-Dufol, M., Cañavate, C., Gutiérrez-Solar, B., Molina, R., Laguna, F., López-Vélez, R., Cercenado, E., Daudén, E., Blázquez, J., de Guevara, C.L., Gómez, J., de la Torre, J., Barros, C., Altés, J., Serra, T., Alvar, J.: Variability of Leishmania (Leishmania) infantum among stocks from immunocompromised, immunocompetent patients and dogs in Spain. FEMS Microbiol. Lett. 131, 197–204 (1995)

    Article  PubMed  Google Scholar 

  35. Kubar, J., Marty, P., Lelievre, A., Quaranta, J.F., Staccini, P., Caroli-Bosc, C., Le Fichoux, Y.: Visceral leishmaniasis in HIV-positive patients: primary infection, reactivation and latent infection. Impact of the CD4+ T-lymphocyte counts. AIDS 12, 2147–2153 (1998)

    Article  PubMed  CAS  Google Scholar 

  36. Li, J., Nolan, T.J., Farrell, J.P.: Leishmania major: a clone with low virulence for BALB/c mice elicits a Th1 type response and protects against infection with a highly virulent clone. Exp. Parasitol. 87, 47–57 (1997)

    Article  PubMed  CAS  Google Scholar 

  37. Liew, F.Y., Li, Y., Millott, S.: Tumor necrosis factor-alpha synergizes with IFN-gamma in mediating killing of Leishmania major through the induction of nitric oxide. J. Immunol. 145, 4306–4310 (1990)

    PubMed  CAS  Google Scholar 

  38. Liew, F.Y., Li, Y., Millott, S.: Tumour necrosis factor (TNF-alpha) in leishmaniasis. II. TNF-alpha-induced macrophage leishmanicidal activity is mediated by nitric oxide from L-arginine. Immunology 71, 556–559 (1990)

    PubMed  CAS  Google Scholar 

  39. Lowe, J.B.: Glycosylation in the control of selectin counter-receptor structure and function. Immunol. Rev. 186, 19–36 (2002)

    Article  PubMed  CAS  Google Scholar 

  40. Mallan, N., Sengupta, G., Dubey, M.L., Sud, A., Ansari, N.A., Salotra, P.: Antigenaemia and antibody response to Leishmania donovani stage-specific antigens and rk39 antigen in human immunodeficiency virus-infected patients. Br. J. Biomed. Sci. 60, 210–216 (2003)

    Google Scholar 

  41. McNeely, T.B., Turco, S.J.: Requirement of lipophosphoglycan for intracellular survival of Leishmania donovani within human monocytes. J. Immunol. 144, 2745–2750 (1990)

    PubMed  CAS  Google Scholar 

  42. Morell, A.G., Van Den Hamer, C.J.A., Scheinberg, I.H., Ashwell, G.: Physical and chemical studies on ceruloplasmin. IV. Preparation of radioactive, sialic acid-free ceruloplasmin labeled with tritium on terminal D-galactose residues. J. Biol. Chem. 241, 3745–3749 (1966)

    PubMed  CAS  Google Scholar 

  43. Mottram, J.C., Brooks, D.R., Combs, G.H.: Roles of cysteine proteinases of trypanosomes and Leishmania in host-parasite interactions. Curr. Opin. Microbiol. 14, 455–460 (1998)

    Article  Google Scholar 

  44. Mukhopadhyay, S., Sen, P., Bhattacharyya, S., Majumdar, S., Roy, S.: Immunoprophylaxis and immunotherapy against experimental visceral leishmaniasis. Vaccine 84, 291–300 (1999)

    Article  Google Scholar 

  45. Mukhopadhyay, S., Bhattacharyya, S., Majhi, R., De, T., Naskar, K., Majumdar, S., Roy, S.: Use of an attenuated leishmanial parasite as an immunoprophylactic and immunotherapeutic agent against murine visceral leishmaniasis. Clin. Diag. Lab. Immunol. 7, 233–240 (2000)

    Article  CAS  Google Scholar 

  46. Murray, H.W., Berman, J.D., Wright, S.D.: Immunochemotherapy for intracellular Leishmania donovani infection: gamma interferon plus pentavalent antimony. J. Infect. Dis. 157, 973–978 (1988)

    PubMed  CAS  Google Scholar 

  47. Murray, H.W., Lu, C.M., Mauze, S., Freeman, S., Moreira, A.L., Kaplan, G., Coffman, R.L.: Interleukin-10 (IL-10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy. Infect. Immun. 70, 6284–6293 (2002)

    Article  PubMed  CAS  Google Scholar 

  48. Murray, M.W.: Cell-mediated immune response in experimental visceral leishmaniasis. II. Oxygen-dependent killing of intracellular Leishmania donovani amastigotes. J. Immunol. 129, 351–357 (1982)

    PubMed  CAS  Google Scholar 

  49. Murray, M.W.: Effect of continuous administration of interferon-gamma in experimental visceral leishmaniasis. J. Infect. Dis. 161, 992–994 (1990)

    PubMed  CAS  Google Scholar 

  50. Nader, T., Vince, J.E., McConville, M.J.: Surface determinants of Leishmania parasites and their role in infectivity in the mammalian host. Curr. Mol. Med. 4, 649–665 (2004)

    Article  Google Scholar 

  51. Pratlong, F., Dedet, J.P., Marty, P., Portus, M., Deniau, M., Dereure, J., Abranches, P., Reynes, J., Martini, A., Lefebvre, M., et al.: Leishmania-human immunodeficiency virus coinfection in the Mediterranean basin: isoenzymatic characterization of 100 isolates of the Leishmania infantum complex. J. Infect. Dis. 172, 323–326 (1995)

    PubMed  CAS  Google Scholar 

  52. Rabinovich, G.A., Baum, L.G., Tinari, N., Paganelli, R., Natoli, C., Liu, F.T., Iacobelli, S.: Galectins and their ligands: amplifiers, silencers or tuners of the inflammatory response? Trends Immunol. 23, 313–320 (2002)

    Article  PubMed  CAS  Google Scholar 

  53. Ralton, J.E., Naderer, T., Piraino, H.L., Bashtannyk, T.A., Callaghan, J.M., McConville, M.J.: Evidence that intracellular beta1–2 mannan is a virulence factor in Leishmania parasites. J. Biol. Chem. 278, 40757–40763 (2003)

    Article  PubMed  CAS  Google Scholar 

  54. Ray, J.C.: Cultivation of various Leishmania parasites on solid medium. Ind. J. Med. Res. 20, 355–357 (1932)

    Google Scholar 

  55. Roach, T.I., Kiderlen, A.F., Blackwell, J.M.: Role of inorganic nitrogen oxides and tumor necrosis factor alpha in killing Leishmania donovani amastigotes in gamma interferon-lipopolysaccharide-activated macrophages from Lshs and Lshr congenic mouse strains. Infect. Immun. 59, 3935–3944 (1991)

    PubMed  CAS  Google Scholar 

  56. Roos, P.H., Kolb-Bachofen, V., Schlepper-Schäfer, J., Monsigny, M., Stockert, R.J., Kolb, H.: Two galactose-specific receptors in the liver with different function. FEBS Lett. 157, 253–256 (1983)

    Article  PubMed  CAS  Google Scholar 

  57. Ryan, K.A., Garraway, L.A., Descoteaux, A., Turco, S.J., Beverley, S.M.: Isolation of virulence genes directing surface glycosyl-phosphatidylinositol synthesis by functional complementation of Leishmania. Proc. Natl. Acad. Sci. USA 90, 8609–8613 (1993)

    Article  PubMed  CAS  Google Scholar 

  58. Sacks, D.L., da Silva, R.P.: The generation of infective stage Leishmania major promastigotes is associated with the cell-surface expression and release of a developmentally regulated glycolipid. J. Immunol. 139, 3099–3106 (1987)

    PubMed  CAS  Google Scholar 

  59. Sacks, D.L., Perkins, P.V.: Identification of an infective stage of Leishmania promastigotes. Science 223, 1417–1419 (1984)

    Article  PubMed  CAS  Google Scholar 

  60. Sacks, D.L.: Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes. J. Immunol. 135, 564–569 (1985)

    PubMed  CAS  Google Scholar 

  61. Salotra, P., Ralhan, R., Sreenivas, G.: Heat-stress induced modulation of protein phosphorylation in virulent promastigotes of Leishmania donovani. Int. J. Biochem. Cell Biol. 32, 309–316 (2000)

    Article  PubMed  CAS  Google Scholar 

  62. Saraiva, E.M., Andrade, A.F., Pereira, M.E.: Cell surface carbohydrate of Leishmania mexicana amazonensis: differences between infective and non-infective forms. Eur. J. Cell Biol. 40, 219–225 (1986)

    PubMed  CAS  Google Scholar 

  63. Segovia, M., Artero, J.M., Mellado, E., Chance, M.L.: Effects of long-term in vitro cultivation on the virulence of cloned lines of Leishmania major promastigotes. Ann. Trop. Med. Parasitol. 86, 347–354 (1992)

    PubMed  CAS  Google Scholar 

  64. Shakarian, A.M., Dwyer, D.M.: Pathogenic leishmania secrete antigenically related chitinases which are encoded by a highly conserved gene locus. Exp. Parasitol. 94, 238–242 (2000)

    Article  PubMed  CAS  Google Scholar 

  65. Shiloh, M.U., MacMicking, J.D., Nicholson, S., Brause, J.E., Potter, S., Marino, M., Fang, F., Dinauer, M., Nathan, C.: Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 10, 29–38 (1999)

    Article  PubMed  CAS  Google Scholar 

  66. Smith, A.E., Helenius, A.: How viruses enter animal cells. Science 304, 237–242 (2004)

    Article  PubMed  CAS  Google Scholar 

  67. Spath, G.F., Epstein, L., Leader, B., Singer, S.M., Avila, H.A., Turco, S.J., Beverley, S.M.: Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proc. Natl. Acad. Sci. USA 97, 9258–9263 (2000)

    Article  PubMed  CAS  Google Scholar 

  68. Stauber, L.A.: Host resistance to the Khartoum strain of Leishmania donovani. Rice Inst. Pamphlets 45, 80–83 (1958)

    Google Scholar 

  69. Streit, J.A., Recker, T.J., Filho, F.G., Beverley, S.M., Wilson, M.E.: Protective immunity against the protozoan Leishmania chagasi is induced by subclinical cutaneous infection with virulent but not avirulent organisms. J. Immunol. 166, 1921–1929 (2001)

    PubMed  CAS  Google Scholar 

  70. Tolson, D.L., Turco, S.J., Beecroft, R.O., Pearson, T.W.: The immunochemical strusture and surface arrangement of Leishmania donovani lipophosphoglycan determined using monoclonal antibodies. Mol. Biochem. Parasitol. 35, 109–118 (1989)

    Article  PubMed  CAS  Google Scholar 

  71. Underhill, D.M.: Toll-like receptors: networking for success. Eur. J. Immunol. 33, 1767–1775 (2003)

    Article  PubMed  CAS  Google Scholar 

  72. Wang, C., Eufemi, M., Turano, C., Giartosio, A.: Influence of the carbohydrate moiety on the stability of glycoproteins. Biochem. 35, 7299–7307 (1996)

    Article  CAS  Google Scholar 

  73. Wei, X.Q., Charles, I.G., Smith, A., Ure, J., Feng, G.J., Huang, F.P., Xu, D., Muller, W., Moncada, S., Liew, F.Y.: Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375, 408–411 (1995)

    Article  PubMed  CAS  Google Scholar 

  74. Weiss, P., Ashwell, G.: The asialoglycoprotein receptor: properties and modulation by ligand. Prog. Clin. Biol. Res. 300, 169–184 (1989)

    PubMed  CAS  Google Scholar 

  75. Wells, L., Hart, G.W.: O-GlcNAc turns twenty: functional implications for Posttranslational modification of nuclear and cytosolic proteins with a sugar. FEBS Lett. 546, 154–158 (2003)

    Article  PubMed  CAS  Google Scholar 

  76. Zhang, W.W., Matlashewski, G.: Loss of virulence in Leishmania donovani deficient in an amastigote-specific protein, A2. Proc. Natl. Acad. Sci. USA 94, 8807–8811 (1997)

    Article  PubMed  CAS  Google Scholar 

  77. Zheng, Z., Butler, K.D., Tweten, R.K., Mensa-Wilmot, K.: Endosomes, glycosomes, and glycosylphosphatidylinositol catabolism in Leishmania major. J. Biol. Chem. 279, 42106–42113 (2004)

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by the Department of Science and Technology, Government of India (Grant numbers, SP/SO/B-04/2000 and SR/SO/HS-46/2004). UDP-Gal/GlcNAc β1–4galactosyltransferase antibody was kindly provided by Prof. S. Basu, University of Notre Dame (Notre Dame, USA). LPG specific mAb (ascitis fluid, CA7AE, isotype IgM) and the mutant strain R2D2 was the kind gift of Dr S. Turco, University of Kentucky, Lexington, KY, USA.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. De.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bhaumik, S.K., Singh, M., Basu, R. et al. Virulence attenuation of a UDP-galactose/N-acetylglucosamine β1,4 galactosyltransferase expressing Leishmania donovani promastigote. Glycoconj J 25, 459–472 (2008). https://doi.org/10.1007/s10719-007-9098-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-007-9098-0

Keywords

Navigation