Abstract
Induction of a glycosylphosphatidylinositol (GPI) deficiency in Trypanosoma cruzi by the heterologous expression of Trypanosoma brucei GPI-phospholipase C (GPI-PLC) results in decreased expression of major surface proteins (N. Garg, R. L. Tarleton, and K. Mensa-Wilmot, J. Biol. Chem. 272:12482-12491, 1997). To further explore the consequences of a GPI deficiency on replication and differentiation of T. cruzi, the in vitro and in vivo behaviors of GPI-PLC-expressing T. cruzi were studied. In comparison to wild-type controls, GPI-deficient T. cruzi epimastigotes exhibited a slight decrease in overall growth potential in culture. In the stationary phase of in vitro growth, GPI-deficient epimastigotes readily converted to metacyclic trypomastigotes and efficiently infected mammalian cells. However, upon conversion to amastigote forms within these host cells, the GPI-deficient parasites exhibited a limited capacity to replicate and subsequently failed to differentiate into trypomastigotes. Mice infected with GPI-deficient parasites showed a substantially lower rate of mortality, decreased tissue parasite burden, and a moderate tissue inflammatory response in comparison to those of mice infected with wild-type parasites. The decreased virulence exhibited by GPI-deficient parasites suggests that inhibition of GPI biosynthesis is a feasible strategy for chemotherapy of infections by T. cruzi and possibly other intracellular protozoan parasites.
MeSH Terms
Animals
Chagas Disease/parasitology
Female
Glycosylphosphatidylinositol Diacylglycerol-Lyase
Glycosylphosphatidylinositols/deficiency
Mice
Mice, Inbred C3H
Phosphatidylinositol Diacylglycerol-Lyase
Trypanosoma cruzi/growth & development,pathogenicity
Type C Phospholipases/genetics,metabolism
Virulence/genetics
Chemicals
Glycosylphosphatidylinositols
Type C Phospholipases
Phosphatidylinositol Diacylglycerol-Lyase
Glycosylphosphatidylinositol Diacylglycerol-Lyase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Garg N
Department of Cellular Biology, University of Georgia, Athens 30602, USA.
Postan M
Mensa-Wilmot K
Tarleton R L
References (29)
29 references, click to expand
-
Identification of six complementation classes involved in the biosynthesis of glycosylphosphatidylinositol anchors in Saccharomyces cerevisiae.
J Cell Biol. 1995 Sep;130(6):1333-44
PMID: 7559756
-
The structure and biosynthesis of glycosyl phosphatidylinositol protein anchors.
Annu Rev Biochem. 1993;62:121-38
PMID: 8352586
-
trans-sialidase and sialic acid acceptors from insect to mammalian stages of Trypanosoma cruzi.
Exp Parasitol. 1994 Sep;79(2):211-4
PMID: 8056084
-
cDNA encoding the glycosyl-phosphatidylinositol-specific phospholipase C of Trypanosoma brucei.
Proc Natl Acad Sci U S A. 1988 Dec;85(23):8914-8
PMID: 3194399
-
The 35/50 kDa surface antigen of Trypanosoma cruzi metacyclic trypomastigotes, an adhesion molecule involved in host cell invasion.
Parasite Immunol. 1993 Feb;15(2):121-5
PMID: 8446464
-
Control of differentiation in Trypanosoma cruzi.
Curr Top Microbiol Immunol. 1985;117:1-22
PMID: 3896672
-
Desialylation of lysosomal membrane glycoproteins by Trypanosoma cruzi: a role for the surface neuraminidase in facilitating parasite entry into the host cell cytoplasm.
J Exp Med. 1992 Aug 1;176(2):313-25
PMID: 1500849
-
Mucin-like glycoproteins linked to the membrane by glycosylphosphatidylinositol anchor are the major acceptors of sialic acid in a reaction catalyzed by trans-sialidase in metacyclic forms of Trypanosoma cruzi.
Mol Biochem Parasitol. 1993 Jun;59(2):293-303
PMID: 8341326
-
Genomic organization, chromosomal localization, and developmentally regulated expression of the glycosyl-phosphatidylinositol-specific phospholipase C of Trypanosoma brucei.
Mol Cell Biol. 1990 Feb;10(2):720-6
PMID: 1688997
-
Purification and use of recombinant glycosylphosphatidylinositol-phospholipase C.
Methods Enzymol. 1995;250:641-55
PMID: 7651183
-
Evidence for the participation of the Ssp-3 antigen in the invasion of nonphagocytic mammalian cells by Trypanosoma cruzi.
J Exp Med. 1992 Jun 1;175(6):1635-41
PMID: 1534115
-
Chagas disease: epidemiology and prospects for interruption of transmission in the Americas.
World Health Stat Q. 1992;45(2-3):276-9
PMID: 1462661
-
Purification and characterization of the membrane-form variant surface glycoprotein hydrolase of Trypanosoma brucei.
J Biol Chem. 1986 Sep 5;261(25):11918-23
PMID: 3745171
-
Trypanosoma cruzi: identification of a membrane cysteine proteinase linked through a GPI anchor.
Braz J Med Biol Res. 1994 Feb;27(2):431-7
PMID: 8081261
-
Developmentally regulated, phospholipase C-mediated release of the major surface glycoprotein of amastigotes of Trypanosoma cruzi.
J Exp Med. 1988 Feb 1;167(2):300-14
PMID: 3279152
-
How to make a glycoinositol phospholipid anchor.
Trends Biochem Sci. 1992 Nov;17(11):470-3
PMID: 1455519
-
GPI-anchor synthesis.
Parasitol Today. 1994 Apr;10(4):139-43
PMID: 15275478
-
The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes.
Biochem J. 1993 Sep 1;294 ( Pt 2):305-24
PMID: 8373346
-
Yeast Gpi8p is essential for GPI anchor attachment onto proteins.
EMBO J. 1996 Dec 2;15(23):6575-83
PMID: 8978684
-
Sequence and expression of the glycosyl-phosphatidylinositol-specific phospholipase C of Trypanosoma brucei.
Mol Biochem Parasitol. 1989 Mar 15;33(3):289-96
PMID: 2523022
-
Differentiation of Trypanosoma cruzi in culture.
J Protozool. 1967 Aug;14(3):447-51
PMID: 6050651
-
Proteins with glycosylphosphatidylinositol (GPI) signal sequences have divergent fates during a GPI deficiency. GPIs are essential for nuclear division in Trypanosoma cruzi.
J Biol Chem. 1997 May 9;272(19):12482-91
PMID: 9139697
-
Biosynthesis of glycosylphosphatidylinositol membrane anchors.
Biochem J. 1995 Sep 1;310 ( Pt 2):361-70
PMID: 7654168
-
Phosphatidylinositol hydrolysis by Trypanosoma brucei glycosylphosphatidylinositol phospholipase C.
J Biol Chem. 1996 Jun 28;271(26):15533-41
PMID: 8663180
-
Characterization of a glycosyl-phosphatidylinositol-anchored membrane protein from Trypanosoma cruzi.
Infect Immun. 1991 Apr;59(4):1409-16
PMID: 1825989
-
Delivery by Trypanosoma cruzi of proteins into the MHC class I antigen processing and presentation pathway.
J Immunol. 1997 Apr 1;158(7):3293-302
PMID: 9120286
-
Stage-specific surface antigens expressed during the morphogenesis of vertebrate forms of Trypanosoma cruzi.
Exp Parasitol. 1987 Dec;64(3):474-84
PMID: 3315736
-
Yeast Gaa1p is required for attachment of a completed GPI anchor onto proteins.
J Cell Biol. 1995 May;129(3):629-39
PMID: 7730400
-
Mammalian cell sialic acid enhances invasion by Trypanosoma cruzi.
Infect Immun. 1993 Mar;61(3):898-902
PMID: 8381772