A Nucleotide Sugar Transporter Involved in Glycosylation of the Toxoplasma Tissue Cyst Wall Is Required for Efficient Persistence of Bradyzoites

PLoS Pathogens

Volumn 9, Issue 5, 2013, Pages

  Caffaro, Carolina E ^a,c   Koshy, Anita A ^a,d   Liu, Li ^b   Zeiner, Gusti M ^a,c   Hirschberg, Carlos B ^a   Boothroyd, John C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY   (United States)

^c AGILENT TECHNOLOGIES   (United States)

^d UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; NUCLEOTIDASE; NUCLEOTIDE SUGAR TRANSPORTER; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRADYZOITE; CELL FRACTIONATION; CONTROLLED STUDY; CYST (RESTING STAGE); FEMALE; FLUORESCENCE MICROSCOPY; GEL ELECTROPHORESIS; GENE DELETION; GENE SEQUENCE; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TOXOPLASMA; TROPISM; VIRULENCE; WESTERN BLOTTING;

ANIMALS; FEMALE; GENE DELETION; GLYCOPROTEINS; GLYCOSYLATION; MICE; NUCLEOTIDE TRANSPORT PROTEINS; PROTOZOAN PROTEINS; TOXOPLASMA; TOXOPLASMOSIS;

TOXOPLASMA; TOXOPLASMA GONDII;

EID: 84878521922     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003331     Document Type: Article

References (34)

1. Dubey JP, (1998) Advances in the life cycle of Toxoplasma gondii. Int J Parasitol 28: 1019-1024.
2. Boothroyd JC, (2009) Expansion of host range as a driving force in the evolution of Toxoplasma. Mem Inst Oswaldo Cruz 104: 179-184.
3. Luft BJ, Brooks RG, Conley FK, McCabe RE, Remington JS, (1984) Toxoplasmic encephalitis in patients with acquired immune deficiency syndrome. JAMA 252: 913-917.
4. Luft BJ, Remington JS, (1992) Toxoplasmic encephalitis in AIDS. Clin Infect Dis 15: 211-222.
5. Ferguson DJ, (2004) Use of molecular and ultrastructural markers to evaluate stage conversion of Toxoplasma gondii in both the intermediate and definitive host. Int J Parasitol 34: 347-360.
6. Ferguson DJ, Hutchison WM, Pettersen E, (1989) Tissue cyst rupture in mice chronically infected with Toxoplasma gondii. An immunocytochemical and ultrastructural study. Parasitol Res 75: 599-603.
7. Lemgruber L, Lupetti P, Martins-Duarte ES, De Souza W, Vommaro RC, (2011) The organization of the wall filaments and characterization of the matrix structures of Toxoplasma gondii cyst form. Cell Microbiol 13: 1920-1932.
8. Ferguson DJ, Hutchison WM, (1987) An ultrastructural study of the early development and tissue cyst formation of Toxoplasma gondii in the brains of mice. Parasitol Res 73: 483-491.
9. Boothroyd JC, Black M, Bonnefoy S, Hehl A, Knoll LJ, et al. (1997) Genetic and biochemical analysis of development in Toxoplasma gondii. Philos Trans R Soc Lond B Biol Sci 352: 1347-1354.
10. Zhang YW, Halonen SK, Ma YF, Wittner M, Weiss LM, (2001) Initial characterization of CST1, a Toxoplasma gondii cyst wall glycoprotein. Infect Immun 69: 501-507.
11. Gross U, Bormuth H, Gaissmaier C, Dittrich C, Krenn V, et al. (1995) Monoclonal rat antibodies directed against Toxoplasma gondii suitable for studying tachyzoite-bradyzoite interconversion in vivo. Clin Diagn Lab Immunol 2: 542-548.
12. Craver MP, Rooney PJ, Knoll LJ, (2010) Isolation of Toxoplasma gondii development mutants identifies a potential proteophosphogylcan that enhances cyst wall formation. Mol Biochem Parasitol 169: 120-123.
13. Caffaro CE, Hirschberg CB, (2006) Nucleotide sugar transporters of the Golgi apparatus: from basic science to diseases. Acc Chem Res 39: 805-812.
14. Caffaro CE, Hirschberg CB, Berninsone PM, (2006) Independent and simultaneous translocation of two substrates by a nucleotide sugar transporter. Proc Natl Acad Sci U S A 103: 16176-16181.
15. Tobin CM, Knoll LJ, (2012) A patatin-like protein protects Toxoplasma gondii from degradation in a nitric oxide-dependent manner. Infect Immun 80: 55-61.
16. Zinecker CF, Striepen B, Tomavo S, Dubremetz JF, Schwarz RT, (1998) The dense granule antigen, GRA2 of Toxoplasma gondii is a glycoprotein containing O-linked oligosaccharides. Mol Biochem Parasitol 97: 241-246.
17. Xu YX, Liu L, Caffaro CE, Hirschberg CB, (2010) Inhibition of Golgi apparatus glycosylation causes endoplasmic reticulum stress and decreased protein synthesis. J Biol Chem 285: 24600-24608.
18. Adjogble KD, Mercier C, Dubremetz JF, Hucke C, Mackenzie CR, et al. (2004) GRA9, a new Toxoplasma gondii dense granule protein associated with the intravacuolar network of tubular membranes. Int J Parasitol 34: 1255-1264.
19. Buchholz KR, Fritz HM, Chen X, Durbin-Johnson B, Rocke DM, et al. (2011) Identification of tissue cyst wall components by transcriptome analysis of in vivo and in vitro Toxoplasma gondii bradyzoites. Eukaryot Cell 10: 1637-1647.
20. Saeij JP, Arrizabalaga G, Boothroyd JC, (2008) A cluster of four surface antigen genes specifically expressed in bradyzoites, SAG2CDXY, plays an important role in Toxoplasma gondii persistence. Infect Immun 76: 2402-2410.
21. Debierre-Grockiego F, Azzouz N, Schmidt J, Dubremetz JF, Geyer H, et al. (2003) Roles of glycosylphosphatidylinositols of Toxoplasma gondii. Induction of tumor necrosis factor-alpha production in macrophages. J Biol Chem 278: 32987-32993.
22. Debierre-Grockiego F, Schwarz RT, (2010) Immunological reactions in response to apicomplexan glycosylphosphatidylinositols. Glycobiology 20: 801-811.
23. Kimmel J, Smith TK, Azzouz N, Gerold P, Seeber F, et al. (2006) Membrane topology and transient acylation of Toxoplasma gondii glycosylphosphatidylinositols. Eukaryot Cell 5: 1420-1429.
24. Fauquenoy S, Morelle W, Hovasse A, Bednarczyk A, Slomianny C, et al. (2008) Proteomics and glycomics analyses of N-glycosylated structures involved in Toxoplasma gondii-host cell interactions. Mol Cell Proteomics 7: 891-910.
25. Garenaux E, Shams-Eldin H, Chirat F, Bieker U, Schmidt J, et al. (2008) The dual origin of Toxoplasma gondii N-glycans. Biochemistry 47: 12270-12276.
26. Azzouz N, Rauscher B, Gerold P, Cesbron-Delauw MF, Dubremetz JF, et al. (2002) Evidence for de novo sphingolipid biosynthesis in Toxoplasma gondii. Int J Parasitol 32: 677-684.
27. Abeijon C, Orlean P, Robbins PW, Hirschberg CB, (1989) Topography of glycosylation in yeast: characterization of GDPmannose transport and lumenal guanosine diphosphatase activities in Golgi-like vesicles. Proc Natl Acad Sci U S A 86: 6935-6939.
28. Perez M, Hirschberg CB, (1987) Transport of sugar nucleotides into the lumen of vesicles derived from rat liver rough endoplasmic reticulum and Golgi apparatus. Methods Enzymol 138: 709-715.
29. Yanagisawa K, Resnick D, Abeijon C, Robbins PW, Hirschberg CB, (1990) A guanosine diphosphatase enriched in Golgi vesicles of Saccharomyces cerevisiae. Purification and characterization. J Biol Chem 265: 19351-19355.
30. Lodoen MB, Gerke C, Boothroyd JC, (2010) A highly sensitive FRET-based approach reveals secretion of the actin-binding protein toxofilin during Toxoplasma gondii infection. Cell Microbiol 12: 55-66.
31. Albert H, Dale EC, Lee E, Ow DW, (1995) Site-specific integration of DNA into wild-type and mutant lox sites placed in the plant genome. Plant J 7: 649-659.
32. Soldati D, Boothroyd JC, (1993) Transient transfection and expression in the obligate intracellular parasite Toxoplasma gondii. Science 260: 349-352.
33. Koshy AA, Dietrich HK, Christian DA, Melehani JH, Shastri AJ, et al. (2012) Toxoplasma Co-opts Host Cells It Does Not Invade. PLoS Pathog 8: e1002825.
34. van de Ven E, Melchers W, Galama J, Camps W, Meuwissen J, (1991) Identification of Toxoplasma gondii infections by BI gene amplification. J Clin Microbiol 29: 2120-2124.