Leishmania major survival in selective Phlebotomus papatasi sand fly vector requires a specific SCG-encoded lipophosphoglycan galactosylation pattern

PLoS Pathogens

Volumn 6, Issue 11, 2010, Pages

  Dobson, Deborah E ^a   Kamhawi, Shaden ^b   Lawyer, Phillip ^b   Turco, Salvatore J ^c   Beverley, Stephen M ^a   Sacks, David L ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE; ADHESIN; BETA 1,3 GALACTOSYLTRANSFERASES; GALACTOSE; GALACTOSYLTRANSFERASE; LIPOPHOSPHOGLYCAN; PHOSPHOGLYCAN SIDE CHAIN BETA GALACTOSYLTRANSFERASE; UNCLASSIFIED DRUG; GLYCOSPHINGOLIPID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL SURVIVAL; CONTROLLED STUDY; COSMID VECTOR; DISEASE CARRIER; ENZYME ACTIVITY; FLY; GENE SEQUENCE; GENETIC ENGINEERING; GENETIC TRANSFECTION; HOST PARASITE INTERACTION; LEISHMANIA DONOVANI; LEISHMANIA MAJOR; MIDGUT; MOUSE; NONHUMAN; PHLEBOTOMUS PAPATASI; PROMASTIGOTE; PROTEIN GLYCOSYLATION; TRANSGENIC ORGANISM; WILD TYPE; ANIMAL; DIGESTIVE SYSTEM; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PARASITOLOGY; PHLEBOTOMUS; SECRETION; SKIN LEISHMANIASIS;

LEISHMANIA DONOVANI; LEISHMANIA MAJOR; PHLEBOTOMINAE; PHLEBOTOMUS PAPATASI; PROTOZOA;

ACID PHOSPHATASE; ANIMALS; DIGESTIVE SYSTEM; GALACTOSE; GLYCOSPHINGOLIPIDS; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; PHLEBOTOMUS;

EID: 79251474026     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001185     Document Type: Article

References (56)

1. Bates PA (2008) Leishmania sand fly interaction: progress and challenges. Curr Opin Microbiol 11: 340-344.
2. Volf P, Hostomska J, Rohousova I (2008) Molecular Crosstalks in Leishmania-Sandfly-Host Relationships. Parasite 15: 237-243.
3. Sacks DL, Lawyer P, Kamhawi S (2008) The biology of Leishmania - sand fly interactions. In: Myler PJ, Fasel N, eds. Leishmania - After the Genome. Norwish, UK: Caister Academic Press. pp 205-238.
4. Kamhawi S (2006) Phlebotomine sand flies and Leishmania parasites: friends or foes? Trends Parasitol 22: 439-445.
5. Oliveira F, Jochim RC, Valenzuela JG, Kamhawi S (2009) Sand flies, Leishmania, and transcriptome-borne solutions. Parasitol Int 58: 1-5.
6. Sacks DL (2001) Leishmania-sand fly interactions controlling species-specific vector competence. Cell Microbiol 3: 189-196.
7. Volf P, Myskova J (2007) Sand flies and Leishmania: specific versus permissive vectors. Trends Parasitol 23: 91-92.
8. Svarovska A, Ant TH, Seblova V, Jecna L, Beverley SM, et al. (2010) Leishmania major glycosylation mutants require phosphoglycans (lpg2-) but not lipophosphoglycan (lpg1-) for survival in permissive sand fly vectors. PLoS Negl Trop Dis 4: e580.
9. Pimenta PF, Saraiva EM, Sacks DL (1991) The comparative fine structure and surface glycoconjugate expression of three life stages of Leishmania major. Exp Parasitol 72: 191-204.
10. Ilgoutz SC, McConville MJ (2001) Function and assembly of the Leishmania surface coat. Int J Parasitol 31: 899-908.
11. Turco SJ, Descoteaux A (1992) The lipophosphoglycan of Leishmania parasites. Ann Rev Micro 46: 65-94.
12. Pimenta PF, Saraiva EM, Rowton E, Modi GB, Garraway LA, et al. (1994) Evidence that the vectorial competence of phlebotomine sand flies for different species of Leishmania is controlled by structural polymorphisms in the surface lipophosphoglycan. Proc Natl Acad Sci U S A 91: 9155-9156.
13. Kamhawi S, Modi GB, Pimenta PF, Rowton E, Sacks DL (2000) The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment. Parasitology 121(Pt 1): 25-33.
14. Mahoney AB, Sacks DL, Saraiva E, Modi G, Turco SJ (1999) Intra-species and stage-specific polymorphisms in lipophosphoglycan structure control Leishmania donovani-sand fly interactions. Biochemistry 38: 9813-9823.
15. Soares RP, Barron T, McCoy-Simandle K, Svobodova M, Warburg A, et al. (2004) Leishmania tropica: intraspecific polymorphisms in lipophosphoglycan correlate with transmission by different Phlebotomus species. Exp Parasitol 107: 105-114.
16. Myskova J, Svobodova M, Beverley SM, Volf P (2007) A lipophosphoglycanindependent development of Leishmania in permissive sand flies. Microbes Infect 9: 317-324.
17. Secundino N, Kimblin N, Peters NC, Lawyer P, Capul AA, et al. (2010) Proteophosphoglycan confers resistance of Leishmania major to midgut digestive enzymes induced by blood feeding in vector sand flies. Cell Microbiol 12: 906-918.
18. Lloyd DH, Viac J, Werling D, Reme CA, Gatto H (2007) Role of sugars in surface microbe-host interactions and immune reaction modulation. Vet Dermatol 18: 197-204.
19. Kamhawi S, Ramalho-Ortigao M, Pham VM, Kumar S, Lawyer PG, et al. (2004) A role for insect galectins in parasite survival. Cell 119: 329-341.
20. Pimenta PF, Turco SJ, McConville MJ, Lawyer PG, Perkins PV, et al. (1992) Stage-specific adhesion of Leishmania promastigotes to the sandfly midgut. Science 256: 1812-1815.
21. Butcher BA, Turco SJ, Hilty BA, Pimenta PF, Panunzio M, et al. (1996) Deficiency in b1,3-galactosyltransferase of a Leishmania major lipophosphoglycan mutant adversely influences the Leishmania-sand fly interaction. J Biol Chem 271: 20573-20579.
22. Cihakova J, Volf P (1997) Development of different Leishmania major strains in the vector sandflies Phlebotomus papatasi and P. duboscqi. Ann Trop Med Parasitol 91: 267-279.
23. Joshi PB, Sacks DL, Modi G, McMaster WR (1998) Targeted gene deletion of Leishmania major genes encoding developmental stage-specific leishmanolysin (GP63). Mol Microbiol 27: 519-530.
24. Sacks DL, Modi G, Rowton E, Späth G, Epstein L, et al. (2000) The role of phosphoglycans in Leishmania-sand fly interactions. Proc Natl Acad Sci U S A 97: 406-411.
25. McConville MJ, Schnur LF, Jaffe C, Schneider P (1995) Structure of Leishmania lipophosphoglycan: inter- and intra-specific polymorphism in Old World species. Biochem J 310: 807-818.
26. McConville MJ, Thomas-Oates JE, Ferguson MA, Homans SW (1990) Structure of the lipophosphoglycan from Leishmania major. J Biol Chem 265: 19611-19623.
27. McConville MJ, Turco SJ, Ferguson MA, Sacks DL (1992) Developmental modification of lipophosphoglycan during the differentiation of Leishmania major promastigotes to an infectious stage. Embo J 11: 3593-3600.
28. Dobson DE, Mengeling BJ, Cilmi S, Hickerson S, Turco SJ, et al. (2003) Identification of genes encoding arabinosyltransferases (SCA) mediating developmental modifications of lipophosphoglycan (LPG) required for sand fly transmission of Leishmania major. J Biol Chem 278: 28840-28848.
29. Capul AA, Barron T, Dobson DE, Turco SJ, Beverley SM (2007) Two functionally divergent UDP-Gal nucleotide sugar transporters participate in phosphoglycan synthesis in Leishmania major. J Biol Chem 282: 14006-14017.
30. Dobson DE, Scholtes LD, Valdez KE, Sullivan DR, Mengeling BJ, et al. (2003) Functional identification of galactosyltransferases (SCGs) required for speciesspecific modifications of the lipophosphoglycan adhesin controlling Leishmania major-sand fly interactions. J Biol Chem 278: 15523-15531.
31. Dobson DE, Scholtes LD, Myler PJ, Turco SJ, Beverley SM (2006) Genomic organization and expression of the expanded SCG/L/R gene family of Leishmania major: internal clusters and telomeric localization of SCGs mediating speciesspecific LPG modifications. Mol Biochem Parasitol 146: 231-241.
32. Anderson CF, Mendez S, Sacks DL (2005) Nonhealing infection despite Th1 polarization produced by a strain of Leishmania major in C57BL/6 mice. J Immunol 174: 2934-2941.
33. Kimblin N, Peters N, Debrabant A, Secundino N, Egen J, et al. (2008) Quantification of the infectious dose of Leishmania major transmitted to the skin by single sand flies. Proc Natl Acad Sci U S A 105: 10125-10130.
34. Spath GF, Epstein L, Leader B, Singer SM, Avila HA, et al. (2000) Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proc Natl Acad Sci U S A 97: 9258-9263.
35. Kapler GM, Coburn CM, Beverley SM (1990) Stable transfection of the human parasite Leishmania delineates a 30 kb region sufficient for extra-chromosomal replication and expression. Mol Cell Biol 10: 1084-1094.
36. Robinson KA, Beverley SM (2003) Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. Mol Biochem Parasitol 128: 217-228.
37. Ha DS, Schwarz JK, Turco SJ, Beverley SM (1996) Use of the Green Fluorescent Protein as a marker in transfected Leishmania. Molec Biochem Parasitol 77: 57-64.
38. Orlandi PA, Jr., Turco SJ (1987) Structure of the lipid moiety of the Leishmania donovani lipophosphoglycan. J Biol Chem 262: 10384-10391.
39. Barron TL, Turco SJ (2006) Quantitation of Leishmania lipophosphoglycan repeat units by capillary electrophoresis. Biochim Biophys Acta 1760: 710-714.
40. Katakura K, Kobayashi A (1988) Acid phosphatase activity of virulent and avirulent clones of Leishmania donovani promastigotes. Infect Immun 56: 2856-2860.
41. Zufferey R, Allen S, Barron T, Sullivan DR, Denny PW, et al. (2003) Ether phospholipids and glycosylinositolphospholipids are not required for amastigote virulence or for inhibition of macrophage activation by Leishmania major. J Biol Chem 278: 44708-44718.
42. da Silva R, Sacks DL (1987) Metacyclogenesis is a major determinant of Leishmania promastigote virulence and attenuation. Infect Immun 55: 2802-2806.
43. Akopyants NS, Kimblin N, Secundino N, Patrick R, Peters N, et al. (2009) Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 324: 265-268.
44. Boulanger N, Lowenberger C, Volf P, Ursic R, Sigutova L, et al. (2004) Characterization of a defensin from the sand fly Phlebotomus duboscqi induced by challenge with bacteria or the protozoan parasite Leishmania major. Infect Immun 72: 7140-7146.
45. Sacks DL, Pimenta PF, McConville MJ, Schneider P, Turco SJ (1995) Stagespecific binding of Leishmania donovani to the sand fly vector midgut is regulated by conformational changes in the abundant surface lipophosphoglycan. J Exp Med 181: 685-697.
46. Adler SaT O (1927) The behaviour of cultures of Leishmania sp. in Phlebotomus papatasi. Annals of Tropical Medicine and Parasitology 21: 111-134.
47. Lippert DN, Dwyer DW, Li F, Olafson RW (1999) Phosphoglycosylation of a secreted acid phosphatase from Leishmania donovani. Glycobiology 9: 627-636.
48. Shakarian AM, Dwyer DM (2000) Structurally conserved soluble acid phosphatases are synthesized and released by Leishmania major promastigotes. Exp Parasitol 95: 79-84.
49. Shakarian AM, Joshi MB, Yamage M, Ellis SL, Debrabant A, et al. (2003) Members of a unique histidine acid phosphatase family are conserved amongst a group of primitive eukaryotic human pathogens. Mol Cell Biochem 245: 31-41.
50. Wiese M, Ilg T, Lottspeich F, Overath P (1995) Ser/Thr-rich repetitive motifs as targets for phosphoglycan modifications in Leishmania mexicana secreted acid phosphatase. Embo J 14: 1067-1074.
51. Elfari M, Schnur LF, Strelkova MV, Eisenberger CL, Jacobson RL, et al. (2005) Genetic and biological diversity among populations of Leishmania major from Central Asia, the Middle East and Africa. Microbes Infect 7: 93-103.
52. Schlein Y, Jacobson RL (1998) Resistance of Phlebotomus papatasi to infection with Leishmania donovani is modulated by components of the infective bloodmeal. Parasitology 117: 467-473.
53. Tuon FF, Neto VA, Amato VS (2008) Leishmania: origin, evolution and future since the Precambrian. FEMS Immunol Med Microbiol 54: 158-166.
54. Volf P, Benkova I, Myskova J, Sadlova J, Campino L, et al. (2007) Increased transmission potential of Leishmania major/Leishmania infantum hybrids. Int J Parasitol 37: 589-593.
55. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373-384.
56. Lee MS, Kim YJ (2007) Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu Rev Biochem 76: 447-480.