Virulent and attenuated lines of Leishmania major: DNA karyotypes and differences in metalloproteinase GP63

Folia Parasitologica

Volumn 53, Issue 2, 2006, Pages 81-90

  Sádlová, Jovana ^a   Volf, Petr ^a   Victoir, Kathleen ^b   Dujardin, Jean Claude ^b   Votýpka, Jan ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b INSTITUTE OF TROPICAL MEDICINE   (Belgium)

Author keywords

Genomic organisation; LD1; Leishmania major; Leishmanolysin; LPG; Minichromosomes; Phlebotomus; Proteolytical activity; Sand flies; Virulence

Indexed keywords

INSECTA; LEISHMANIA MAJOR; PHLEBOTOMINAE; PHLEBOTOMUS DUBOSCQI; VERTEBRATA;

EID: 33745750200     PISSN: 00155683     EISSN: None     Source Type: Journal    
DOI: 10.14411/fp.2006.011     Document Type: Article

References (73)

1. BEVERLEY S.M., COBURN C.M. 1990: Recurrent de novo appearance of small linear DNAs in Leishmania major and relationship to extra-chromosomal DNAs in other species. Mol. Biochem. Parasitol. 42: 133-142.
2. BOROVSKY D., SCHLEIN Y. 1987: Trypsin and chymotrypsin-like enzymes of the sandfly Phlebotomus papatasi infected with Leishmania and their possible role in vector competence. Med. Vet. Entomol. 1: 235-242.
3. BOUVIER J., BORDIER C., VOGEL H., REICHELT R., ETGES R. 1989: Characterization of the promastigote surface protease of Leishmania as a membrane-bound zinc endopeptidase. Mol. Biochem. Parasitol. 37: 235-246.
4. BRITTINGHAM A., MORRISON C.J., McMASTER W.R., McGWIRE B.S., CHANG K.P., MOSSER D.M. 1995: Role of the Leishmania surface protease GP63 in complement fixation, cell adhesion, and resistance to complement-mediated lysis. J. Immunol. 155: 3102-3111.
5. BUTTON L.L., RUSSELL D.G., KLEIN H.L., MEDINA-ACOSTA E., KARESS R.E., McMASTER W.R. 1989: Genes encoding the major surface glycoprotein in Leishmania are tandemly linked at a single chromosomal locus and are constitutively transcribed. Mol. Biochem. Parasitol. 32: 271-284.
6. CHANG C.S., CHANG K.P. 1985: Heme requirement and acquisition by extracellular and intracellular stages of Leishmania mexicana amazonensis. Mol. Biochem. Parasitol. 16: 267-276.
7. CHANG K.P., McGWIRE B.S. 2002: Molecular determinants and regulation of Leishmania virulence. Kinetopl. Biol. Dis. 1(1).
8. CHAKRABARTY R., MUKHERJEE S., LU H.G., McGWIRE B.S., CHANG K.P., BASU M.K. 1996: Kinetics of entry of virulent and avirulent strains of Leishmania donovani into macrophages: a possible role of virulence molecules (GP63 and LPG). J. Parasitol. 84: 632-635.
9. CHAUDHURI G., CHANG K.P. 1988: Acid protease activity of a major surface membrane glycoprotein (GP63) from Leishmania mexicana promastigotes. Mol. Biochem. Parasitol. 27: 43-52.
10. CHEN D.Q., KOLLI B.K., YADAVA N., LU H.G., GILMAN-SACHS A., PETERSON D.A., CHANG K.P. 2000: Episomal expression of specific sense and antisense mRNAs in Leishmania amazonensis: modulation of GP63 level in promastigotes and their infection of macrophages in vitro. Inf. Immun. 68: 80-86.
11. ČIHÁKOVÁ 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.
12. CORNELIS P., SIERRA J.C., LIM J.A., MALUR A., TUNGPRADABKUL S., TAZKA H., LEITAO A., MARTINS C.V., DI PERNA C., BRYS L., DE BEATSELIER P., HAMERS R. 1996: Development of new cloning vectors for the production of immunogenic outer membrane fusion proteins in Escherichia coli. Biotechnology 14: 203-208.
13. DA SILVA R.P., HALL B.F., JOINER K.A., SACKS D.L. 1989: CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J. Immunol. 143: 617-622.
14. DILLON R.J., LANE R.P. 1993: Bloodmeal digestion in the midgut of Phlebotomus papatasi and Phlebotomus langeroni. Med. Vet. Entomol. 7: 225-232.
15. DOLE V.S., MYLER P.J., STUART K.D., MANDHUBALA R. 2002: Expression of biopterin transporter protein (BT1) in Leishmania. FEMS Microbiol. Lett. 208: 89-91.
16. DUJARDIN J.C., DE DONCKER S., VICTOIR K., LE RAY D., HAMERS R., AREVALO J. 1994: Size polymorphism of chromosomes bearing gp63-genes in L. braziliensis and L. peruviana. Ann. Trop. Med. Parasitol. 88: 445-448.
17. DUJARDIN J.C., GAJENDRAN N., AREVALO J., LLANOS-CUENTAS A., GUERRA H., GOMEZ J., ARROYO J., DE DONCKER S., JACQUET D., HAMERS R., LE RAY D. 1993b: Karyotype polymorphism and conserved characters in the Leishmania (Viannia) braziliensis complex explored with chromosome-derived probes. Ann. Soc. Belge Med. Trop. 73: 101-118.
18. DUJARDIN J.C., GAJENDRAN N., HAMERS R., MATTHIJSEN G., URJEL R., RECACOECHEA M., VILLAROEL G., BERMUDEZ H., DESJEUX P., DE DONCKER S., LE RAY D. 1987: Leishmaniasis in the lowlands of Bolivia. VIII. Characterization and identification of Bolivian isolates by PFG karyotyping. In: D. Hart (Ed.), Leishmaniasis: the First Centenary (1885-1985). New Strategies for Control. NATO ASI Series A, Plenum Press, New York, pp. 137-148.
19. DUJARDIN J.C., LLANOS-CUENTAS A., CACERES A., ARANA M., DUJARDIN J.P., GUERRINI F., GOMEZ J., ARROYO J., DE DONCKER S., JACQUET D., HAMERS R., GUERRA H., LE RAY D., AREVALO J. 1993a: Molecular karyotype variation of Leishmania (Viannia) peruviana evidences geographical populations in Peru along a North-South cline. Ann. Trop. Med. Parasitol. 87: 335-347.
20. ETGES R. 1992: Identification of a surface metalloproteinase on 13 species of Leishmania isolated from humans, Crithidia fasciculata, and Herpetomonas samuelpessoai. Acta Trop. 50: 205-217.
21. ETGES R., BOUVIER J., BORDIER C. 1986: The major surface protein of Leishmania promastigotes is a protease. J. Biol. Chem. 261: 9098-9101.
22. FRANKENBURG S., GROSS A., LEIBOVICI V. 1992: Leishmania major and Leishmania donovani: effect of LPG-containing and LPG-deficient strains on monocyte chemotaxis and chemiluminescence. Exp. Parasitol. 75: 442-448.
23. FRANKENBURG S., LEIBOVICI V., MANSBACH N., TURCO S.J., ROSEN G. 1990: Effect of glycolipids of Leishmania parasites on human monocyte activity. J. Immunol. 145: 4284-4289.
24. GHOSH A., MADHUBALA R., MYLER P.J., STUART K.D. 1999: Leishmania donovani: characterization and expression of ORFF, a gene amplified from the LD1 locus. Exp. Parasitol. 93: 225-230.
25. HAJMOVÁ M., CHANG K.P., KOLLI B., VOLF P. 2004: Down-regulation of GP63 in Leishmania amazonensis reduces its early development in Lutzomyia longipalpis. Microbes Infect. 6: 646-649.
26. HEISCH R.B., GRAINGER W.E., HARVEY A.E.C. 1959: The isolation of a Leishmania from gerbils in Kenya. J. Trop. Med. Hyg. 62: 158-159.
27. HILLEY J.D., ZAWADZKI J.L., McCONVILLE M.J., COOMBS G.H., MOTTRAM J.C. 2000: Leishmania mexicana mutants lacking glycosylphosphatidylinositol (GPI): protein transamidase provide insights into the biosynthesis and functions of GPI-anchored proteins. Mol. Biol. Cell 11: 1183-1195.
28. ILG T. 2000: Lipophosphoglycan is not required for infection of macrophages or mice by Leishmania mexicana. EMBO J. 19: 1953-1962.
29. INGA R., DE DONCKER S., GOMEZ J., LOPEZ M., GARCIA R., LE RAY D., AREVALO J., DUJARDIN J.C. 1998: Relation between variation in copy number of ribosomal RNA encoding genes and size of harbouring chromosomes in Leishmania of subgenus Viannia. Mol. Biochem. Parasitol. 92: 219-228.
30. JOSHI P.B., KELLY B.L., KAMHAWI S., SACKS D.L., McMASTER W.R. 2002: Targeted gene deletion in Leishmania major identifies leishmanolysin (GP63) as a virulence factor. Mol. Biochem. Parasitol. 120: 33-40.
31. JOSHI P.B., SACKS D.L., MODI G., McMASTER W.R. 1998: Targeted gene deletion of Leishmania major genes encoding developmental stage-specific leishmanolysin (GP63). Mol. Microbiol. 27: 519-530.
32. LAEMMLI U.K. 1970: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
33. LEMLEY C., YAN S., DOLE V.S., MADHUBALA R., CUNNINGHAM M.L., BEVERLEY S.M., MYLER P.J., STUART K.D. 1999: The Leishmania donovani LD1 locus gene ORFG encodes a biopterin transporter (BT1). Mol. Biochem. Parasitol. 104: 93-105.
34. MAHMOOD F., BOROVSKY D. 1993: Biosynthesis of serine proteases in Lutzomyia anthophora (Diptera: Psychodidae). J. Med. Entomol. 30: 683-688.
35. McCONVILLE M.J., HOMANS S.W. 1992: Identification of the defect in lipophosphoglycan biosynthesis in a non-pathogenic strain of Leishmania major. J. Biol. Chem. 267: 5855-5861.
36. McNEELY T.B., TURCO S.J. 1990: Requirement of lipophosphoglycan for intracellular survival of Leishmania donovani within human monocytes. J. Immunol. 144: 2745-2750.
37. MEDINA-ACOSTA E., BEVERLEY S.M., RUSSELL D.G. 1993: Evolution and expression of the Leishmania surface proteinase (gp63) gene locus. Infect. Agents Dis. 2: 25-34.
38. MUKKADA A.J. 1985: Energy metabolism in Leishmania. In: K.P. Chang and R.S. Bray (Eds.), Human Parasitic Diseases. Vol. 1. Leishmaniasis. Elsevier, Amsterdam, pp. 49-64.
39. MURRAY P.J., HANDMAN E., GLASER T.A., SPITHILL T.W. 1990: Leishmania major, expression and gene structure of the glycoprotein 63 molecule in virulent and avirulent clones and strains. Exp. Parasitol. 71: 294-304.
40. NAVARRO M., MAINGON R., HAMERS R., SEGOVIA M. 1992: Dynamics and size polymorphism of minichromosomes in Leishmania major LV-561 cloned lines. Mol. Biochem. Parasitol. 55: 65-74.
41. ORTIZ G., SEGOVIA M. 1995: Location in the source chro-mosome of the 180-kb minichromosome of Leishmania major and characterization of the novel junction. Mol. Biochem. Parasitol. 71: 153-161.
42. ORTIZ G., SEGOVIA M. 1996: Characterisation of the novel junction of two minichromosomes of Leishmania major. Mol. Biochem. Parasitol. 82: 137-144.
43. PROUDFOOT L., NIKOLAEV A.V., FENG G.J., WEI X.Q., FERGUSON M.A.J., BRIMACOMBE J.S., LIEW F.Y. 1996: Regulation of the expression of nitric oxide synthase and leishmanicidal activity by glycoconjugates of Leishmania lipophosphoglycan in murine macrophages. Proc. Natl. Acad. Sci. USA 93: 10984-10989.
44. PUENTES S.M., DA SILVA R.P., SACKS D.L., HAMMER C.H., JOINER K.A. 1990: Serum resistance of metacyclic stage Leishmania major promastigotes is due to release of C5b-9. J. Immunol. 145: 4311-4316.
45. ROBERTS S.C., WILSON M.E., DONELSON J.E. 1995: Developmentally-regulated expression of a novel 59-kDa product of the major surface protease (Msp or gp63) gene family of Leishmania chagasi. J. Biol. Chem. 270: 8884-8892.
46. RUSSELL D.G. 1987: The macrophage-attachment glycoprotein GP63 is the predominant C3-acceptor site on Leishmania mexicana promastigotes. Eur. J. Biochem. 104: 213-221.
47. RUSSELL D.G., WRIGHT S.D. 1988: Complement receptor type 3 (CR3) binds to an Arg-Gly-Asp-containing region of the major surface glycoprotein, GP63, of Leishmania promastigotes. J. Exp. Med. 168: 279-292.
48. SACKS D.L. 1992: The structure and function of the surface lipophosphoglycan in different developmental stages of Leishmania promastigotes. Infect. Agents Dis. 1: 200-206.
49. SACKS D.L. 2001: Leishmania-sand fly interactions controlling species-specific vector competence. Cell. Microbiol. 3: 189-196.
50. SACKS D.L., BRODIN T.N., TURCO S.J. 1990: Developmental modification of the lipophosphoglycan from Leishmania major promastigotes during metacyclogenesis. Mol. Biochem. Parasitol. 42: 225-234.
51. SACKS D.L., KAMHAWI S. 2001: Molecular aspects of parasite-vector and vector-host interactions in leishmaniasis. Annu. Rev. Microbiol. 55: 453-483.
52. SÁDLOVÁ J. 1999: The life history of Leishmania (Kinetoplastida: Trypanosomatidae). Acta Soc. Zool. Bohem. 63: 331-366.
53. SÁDLOVÁ J., SVOBODOVÁ M., VOLF P. 1999: Leishmania major, effect of repeated passages through sand fly vectors or murine hosts. Ann. Trop. Med. Parasitol. 93: 599-611.
54. nd Edn. Cold Spring Harbor Laboratory Press, New York.
55. SANTOS-GOMES G.M., ABRANCHES P. 1996: Comparative study of infectivity caused by promastigotes of Leishmania infantum MON-1, L. infantum MON-24 and L. donovani MON-18. Folia Parasitol. 43: 7-12.
56. SCHLEIN Y., JACOBSON R.L. 1998: Resistance of Phlebotomus papatasi to infection with Leishmania donovani is modulated by components of the infective bloodmeal. Parasitology 117: 467-473.
57. SCHLEIN Y., SCHNUR L.F., JACOBSON R.L. 1990: Released glycoconjugate of indigenous Leishmania major enhances survival of a foreign L. major in Phlebotomus papatasi. Trans. R. Soc. Trop. Med. Hyg. 84: 353-355.
58. SEAY M.B., HEARD P.L., CHAUDHURI G. 1996: Surface Zn-proteinase as a molecule for defence of Leishmania mexicana amazonensis promastigotes against cytolysis inside macrophage phagolysosomes. Infect. Immun. 64: 5129-5137.
59. SEGOVIA M., ORTIZ G. 1997: LD1 amplification in Leishmania. Parasitol. Today 13: 342-348.
60. SÖRENSEN A.L., HEY A.S., KHARAZMI A. 1994: Leishmania major surface protease GP63 interferes with the function of human monocytes and neutrophils in vitro. APMIS 102: 265-271.
61. SPÄTH G.F., EPSTEIN L., LEADER B., SINGER S.M., AVILA H.A., TURCO S.J., BEVERLEY S.M. 2000: Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proc. Natl. Acad. Sci. USA 97: 9258-9263.
62. TALAMAS-ROHANA P., WRIGHT S.D., LENNARTZ M.R., RUSSELL D.G. 1990: Lipophosphoglycan from Leishmania mexicana promastigotes binds to members of the CR3, p150, 95 and LFA-1 family of leukocyte integrins. J. Immunol. 144: 4817-4824.
63. TOWBIN H., STEAHLIN T., GORDON J. 1979: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76: 4350-4354.
64. TURCO S.J., DESCOTEAUX A. 1992: The lipophosphoglycan of Leishmania parasites. Annu. Rev. Microbiol. 46: 65-94.
65. TURCO S.J., SACKS D.L. 2003: Control of Leishmania-sand fly interactions by polymorphism in lipophosphoglycan structure. Methods Enzymol. 363: 377-381.
66. TURCO S.J., SPÄTH G.F., BEVERLEY S.M. 2001: Is lipophosphoglycan a virulence factor? A surprising diversity between Leishmania species. Trends Parasitol. 17: 223-226.
67. VAN DER PLOEG L.H.T., CORNELISSEN W.C.A, MICHELS P.A.M., BORST P. 1984: Chromosome rearrangements in Trypanosoma brucei. Cell 39: 213-221.
68. VAN EYS G.J.M., SCHOONE G.J., KROON N.C.M., EBELING S.B. 1992: Sequence analysis of small subunit ribosomal RNA genes and its use for detection and identification of Leishmania parasites. Mol. Biochem. Parasitol. 51: 133-142.
69. VICTOIR K., BAÑULS A.L., AREVALO J., LLANOS-CUENTAS A., HAMERS R., NOEL S., DE DONCKER S., LE RAY D. 1998: The gp63 gene locus, a target for genetic characterisation of Leishmania belonging to subgenus Viannia. Parasitology 117: 1-13.
70. VOTH B.R., KELLY B.L., JOSHI P.B., IVENS A.C., McMASTER W.R. 1998: Differentially expressed Leishmania major gp63 genes encode cell surface leishmanolysin with distinct signals for glycosylphosphatidylinositol attachments. Mol. Biochem. Parasitol. 93: 31-41.
71. WINCKER P., RAVEL CH., BLAINEAU C., PAGES M., JAUFFRET Y., DEDET J.-P., BASTIEN P. 1996: The Leishmania genome comprises 36 chromosomes conserved across widely divergent human pathogenic species. Nucleic Acids Res. 24: 1688-1694.
72. WILSON M.E., HARDIN K.K., DONELSON J.E. 1989: Expression of the major surface glycoprotein of Leishmania donovani chagasi in virulent and attenuated promastigotes. J. Immunol. 143: 678-684.
73. YAO C.Q., DONELSON J.E., WILSON M.E. 2003: The major surface protease (MSP or GP63) of Leishmania sp. - Biosynthesis, regulation of expression, and function. Mol. Biochem. Parasitol. 132: 1-16.