Sphingolipid degradation by Leishmania major is required for its resistance to acidic pH in the mammalian host

Infection and Immunity

Volumn 79, Issue 8, 2011, Pages 3377-3387

  Xu, Wei ^a   Xin, Lijun ^b   Soong, Lynn ^b   Zhang, Kai ^a  

^a TEXAS TECH UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12; NITRIC OXIDE; SPHINGOLIPID;

ACIDIFICATION; ACIDITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HIGH TEMPERATURE; HOST; IMMUNOREGULATION; LEISHMANIA MAJOR; LEISHMANIASIS; LIPID DEGRADATION; MACROPHAGE ACTIVATION; MOUSE; MUTANT; NONHUMAN; OXIDATIVE STRESS; PARASITE SURVIVAL; PHAGOSOME; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN SYNTHESIS INHIBITION; T LYMPHOCYTE ACTIVATION; WILD TYPE;

ACIDS; ANIMALS; CELL SURVIVAL; FEMALE; HYDROGEN-ION CONCENTRATION; LEISHMANIA MAJOR; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; SPHINGOLIPIDS; STRESS, PHYSIOLOGICAL; T-LYMPHOCYTES; VIRULENCE;

EID: 79961118829     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00037-11     Document Type: Article

References (35)

1. Bartke, N., and Y. A. Hannun. 2009. Bioactive sphingolipids: metabolism and function. J. Lipid Res. 50(Suppl.):S91-S96.
2. Bowman, E. J., A. Siebers, and K. Altendorf. 1988. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. U. S. A. 85:7972-7976.
3. Claus, V., et al. 1998. Lysosomal enzyme trafficking between phagosomes, endosomes, and lysosomes in J774 macrophages. Enrichment of cathepsin H in early endosomes. J. Biol. Chem. 273:9842-9851.
4. Contreras, I., et al. 2010. Leishmania-induced inactivation of the macrophage transcription factor AP-1 is mediated by the parasite metalloprotease GP63. PLoS Pathog. 6:e1001148.
5. Cunningham, A. C. 2002. Parasitic adaptive mechanisms in infection by Leishmania. Exp. Mol. Pathol. 72:132-141.
6. Denny, P. W., D. Goulding, M. A. Ferguson, and D. F. Smith. 2004. Sphingolipid-free Leishmania are defective in membrane trafficking, differentiation and infectivity. Mol. Microbiol. 52:313-327.
7. Dey, R., et al. 2007. Leishmania donovani-induced ceramide as the key mediator of Akt dephosphorylation in murine macrophages: role of protein kinase C.
8. Ghosh, S., et al. 2001. Generation of ceramide in murine macrophages infected with Leishmania donovani alters macrophage signaling events and aids intracellular parasitic survival. Mol. Cell. Biochem. 223:47-60.
9. Ghosh, S., et al. 2002. Leishmania donovani suppresses activated protein 1 and NF-B activation in host macrophages via ceramide generation: involvement of extracellular signal-regulated kinase. Infect. Immun. 70:6828-6838.
10. Jackson, S. H., J. I. Gallin, and S. M. Holland. 1995. The p47phox mouse knock-out model of chronic granulomatous disease. J. Exp. Med. 182:751-758.
11. Kapler, G. M., C. M. Coburn, and S. M. Beverley. 1990. Stable transfection of the human parasite Leishmania major delineates a 30-kilobase region sufficient for extrachromosomal replication and expression. Mol. Cell. Biol. 10:1084-1094.
12. Kébaïer, C., J. E. Uzonna, S. M. Beverley, and P. Scott. 2006. Immunization with persistent attenuated Delta lpg2 Leishmania major parasites requires adjuvant to provide protective immunity in C57BL/6 mice. Infect. Immun. 74:777-780.
13. Modabber, F. 1990. Development of vaccines against leishmaniasis. Scand. J. Infect. Dis. 76:72-78.
14. Modabber, F. 1995. Vaccines against leishmaniasis. Ann. Trop. Med. Parasitol. 89(Suppl. 1):83-88.
15. Moreira, W., E. Leblanc, and M. Ouellette. 2009. The role of reduced pterins in resistance to reactive oxygen and nitrogen intermediates in the protozoan parasite Leishmania. Free Radic. Biol. Med. 46:367-375.
16. Peters, N. C., et al. 2008. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321:970-974.
17. Racoosin, E. L., and S. M. Beverley. 1997. Leishmania major: promastigotes induce expression of a subset of chemokine genes in murine macrophages. Exp. Parasitol. 85:283-295.
18. Rhee, E. G., et al. 2002. Vaccination with heat-killed Leishmania antigen or recombinant leishmanial protein and CpG oligodeoxynucleotides induces long-term memory CD4+ and CD8+ T cell responses and protection against Leishmania major infection. J. Exp. Med. 195:1565-1573.
19. Sacks, D., and N. Noben-Trauth. 2002. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2:845-858.
20. Sacks, D. L. 1989. Metacyclogenesis in Leishmania promastigotes. Exp. Parasitol. 69:100-103.
21. Sacks, D. L., S. Hieny, and A. Sher. 1985. Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes. J. Immunol. 135: 564-569.
22. Soong, L. 2008. Modulation of dendritic cell function by Leishmania parasites. J. Immunol. 180:4355-4360.
23. Späth, G. F., L. A. Garraway, S. J. Turco, and S. M. Beverley. 2003. The role(s) of lipophosphoglycan (LPG) in the establishment of Leishmania major infections in mammalian hosts. Proc. Natl. Acad. Sci. U. S. A. 100: 9536-9541.
24. Späth, G. F., et al. 2003. Persistence without pathology in phosphoglycandeficient Leishmania major. Science 301:1241-1243.
25. Titus, R. G., M. Marchand, T. Boon, and J. A. Louis. 1985. A limiting dilution assay for quantifying Leishmania major in tissues of infected mice. Parasite Immunol. 7:545-555.
26. Titus, R. G., et al. 1991. Exacerbation of experimental murine cutaneous leishmaniasis with CD4+ Leishmania major-specific T cell lines or clones which secrete gamma interferon and mediate parasite-specific delayed-type hypersensitivity. Eur. J. Immunol. 21:559-567.
27. Tyler, K. M., et al. 2009. Flagellar membrane localization via association with lipid rafts. J. Cell Sci. 122:859-866.
28. Uzonna, J. E., G. F. Spath, S. M. Beverley, and P. Scott. 2004. Vaccination with phosphoglycan-deficient Leishmania major protects highly susceptible mice from virulent challenge without inducing a strong Th1 response. J. Immunol. 172:3793-3797.
29. Vargas-Inchaustegui, D. A., L. Xin, and L. Soong. 2008. Leishmania braziliensis infection induces dendritic cell activation, ISG15 transcription, and the generation of protective immune responses. J. Immunol. 180:7537-7545.
30. Vinet, A. F., M. Fukuda, S. J. Turco, and A. Descoteaux. 2009. The Leishmania donovani lipophosphoglycan excludes the vesicular proton-ATPase from phagosomes by impairing the recruitment of synaptotagmin V. PLoS Pathog. 5:e1000628.
31. Wei, X. Q., et al. 1995. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375:408-411.
32. Zaph, C., J. Uzonna, S. M. Beverley, and P. Scott. 2004. Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nat. Med. 10:1104-1110.
33. Zhang, K., et al. 2007. Redirection of sphingolipid metabolism toward de novo synthesis of ethanolamine in Leishmania. EMBO J. 26:1094-1104.
34. Zhang, K., et al. 2003. Sphingolipids are essential for differentiation but not growth in Leishmania. EMBO J. 22:6016-6026.
35. Zhang, O., et al. 2009. Degradation of host sphingomyelin is essential for Leishmania virulence. PLoS Pathog. 5:e1000692.