Toxoplasma gondii: Expression of GRA1 gene in endoplasmic reticulum promotes both growth and adherence and modulates intracellular calcium release in macrophages

Experimental Parasitology

Volumn 125, Issue 2, 2010, Pages 165-171

  Lin, Jie ^a   Lin, Xu ^a   Yang, Guo hua ^b   Wang, Yong ^b   Peng, Bi wen ^b   Lin, Jian yin ^a  

^a FUJIAN MEDICAL UNIVERSITY   (China)

^b WUHAN UNIVERSITY   (China)

Author keywords

Biological function; GRA1; Intracellular calcium release; Macrophage; Toxoplasma gondii

Indexed keywords

ARACHIDONIC ACID; CALCIUM ION; FLUO 3; GRA1 PROTEIN; LIPOFECTAMINE; MESSENGER RNA; PLASMID VECTOR; PROTOZOAL PROTEIN; PROTOZOAL RNA; UNCLASSIFIED DRUG; CALCIUM; GRA1 ANTIGEN; PARASITE ANTIGEN; RECOMBINANT DNA;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL ADHESION; CELL CLONE; CELL GROWTH; CELL SELECTION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; GENE AMPLIFICATION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; IMMUNOFLUORESCENCE TEST; IMMUNOMODULATION; MACROPHAGE FUNCTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECOMBINANT PLASMID; STABLE TRANSFECTION; TOXOPLASMA GONDII; AGAR GEL ELECTROPHORESIS; ANIMAL; CELL LINE; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; IMMUNOLOGY; MACROPHAGE; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PLASMID; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPECTROFLUOROMETRY; TOXOPLASMA;

MURINAE; TOXOPLASMA GONDII;

ANIMALS; ANTIGENS, PROTOZOAN; ARACHIDONIC ACID; CALCIUM; CELL ADHESION; CELL LINE; DNA, RECOMBINANT; ELECTROPHORESIS, AGAR GEL; ENDOPLASMIC RETICULUM; GENE EXPRESSION; MACROPHAGES; MALE; MICE; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPECTROMETRY, FLUORESCENCE; TOXOPLASMA; TRANSFECTION;

EID: 77951924361     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2010.01.010     Document Type: Article

References (39)

1. Achbarou A., Mercereau-Puijalon O., Autherman J.M., Fortier B., Camus D., Dubremetz J.F. Characterization of microneme proteins of Toxoplasma gondii. Mol. Biochem. Parasitol. 1991, 47:223-234.
2. Achbarou A., Mercereau-Puijalon O., Sadak A., Fortier B., Leriche M.A., Dubremetz J.F. Differential targeting of dense granule proteins in the parasitophorous vacuole of Toxoplasma gondii. Parasitology 1991, 103:321-329.
3. Ahn H.J., Kim S., Kim H.E., Nam H.W. Interaction between secreted GRA proteins and host cell proteins across the parasitophorous vacuolar membrane in the parasitism of Toxoplasma gondii. Korean J. Parasitol. 2006, 44:303-312.
4. Aliberti J., Valenzuela J.G., Carruthers V.B., Hieny S., Andersen J., Charest H., Reis e Sousa C., Fairlamb A., Ribeiro J.M., Sher A. Molecular mimicry of a CCR5 binding-domain in the microbial activation of dendritic cells. Nat. Immunol. 2003, 4:485-490.
5. Beckers C.J.M., Dubremetz J.F., Mercereau-Puijalon O., Joiner K.A. The Toxoplasma gondii rhoptry protein ROP2 is inserted into the parasitophorous vacuole membrane, surrounding the intracellular parasite, and exposed to the host cell cytoplasm. J. Cell Biol. 1994, 127:947-961.
6. Bonhomme A., Maine G.T., Beorchia A., Burlet H., Aubert D., Villena I., Hunt J., Chovan L., Howard L., Brojanac S., Sheu M., Tyner J., Pluot M., Pinon J.M. Quantititative immunolocalization of a P29 protein (GRA7), a new antigen of Toxoplasma gondii. J. Histochem. Cytochem. 1998, 46:1411-1421.
7. Calabrese K.S., Tedesco R.C., Zaverucha do Valle Y., Barbosa H.S. Serum and aqueous humour cytokine response and histopathological alterations during ocular Toxoplasma gondii infection in C57BL/6 mice. Micron 2008, 39(8):1335-1341.
8. Carey K.L., Donahue C.G., Ward G.E. Identification and molecular characterization of GRA8, a novel, proline-rich, dense granule protein of Toxoplasma gondii. Mol. Biochem. Parasitol. 2000, 105:25-37.
9. 2+-binding protein). Proceedings of the National Academy of Sciences of the United States of America 1989, 86(19):7537-7541.
10. Cesbron-Delauw M.F. Dense-granule organelles of Toxoplasma gondii: their role in the host-parasite relationship. Parasitol Today 1994, 10(8):293-296.
11. Cornelly M.C., Kierszenbaum F. Modulation of macrophage interaction with Trypanosoma cruzi by phoapholipase A2-sensitive components of the parasite membrane. Biochem. Biophys. Res. Commun. 1984, 121:931-939.
12. Courret N., Darche S., Sonigo P., Milon G., Buzoni-Gâtel D., Tardieux I. CD11c- and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 2006, 107:309-316.
13. Da Gama L.M., Ribeiro-Gomes F.L., Guimarães U., Arnholdt A.C. Reduction in adhesiveness to extracellular matrix components, modulation of adhesion molecules and in vivo migration of murine macrophages infected with Toxoplasma gondii. Microbes infect. 2004, 6:1287-1296.
14. Ferrandiz J., Mercier C., Wallon M., Picot S., Cesbron-Delauw M.F., Peyron F. Limited value of assays using detection of immunoglobulin G antibodies to the two recombinant dense granule antigen, GRA1 and GRA6 Nt of Toxoplasma gondii, for distinguishing between acut and chronic infection in pregnant women. Clin. Diagn. Lab. Immunol. 2004, 11(6):1016-1021.
15. Kim J.Y., Ahn H.J., Ryu K.J., Nam H.W. Interaction between parasitophorous vacuolar membrene-associted GRA3 and calcium modulating ligand of host cell endoplasmic reticulum in the parasitism of Toxoplasma gondii. Korean J. Parasitol. 2008, 46(4):209-216.
16. Jongert E., de Craeye S., Dewit J., Huygen K. GRA7 provides protective immunity in cocktail DNA vaccines against Toxoplasma gondii. Parasite Immunol. 2007, 29(9):445-453.
17. Jongert E., Melkebeek V., De Craeye S., Dewit J., Verhelst D., Cox E. An enhanced GRA1-GRA7 cocktail DNA vaccine primes anti-Toxoplasma immune responses in pigs. Vaccine 2008, 26(8):1025-1031.
18. Kato M., Claveria F.G., Maki Y., Tanaka T., Suzuki N., Nagasawa H. Toxoplasma gondii antigen GRA1(p24) and SAG1(p30): a comparison of their stimulatory influence on T-cell activation and cytokine expression in in vitro cultures. Pathobiology 2005, 72:160-164.
19. Lambert H., Hitziger N., Dellacasa I., Svensson M., Barragan A. Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell Microbiol. 2006, 8:1611-1623.
20. Lecordier L., Mercier C., Torpier G., Tourvieille B., Darcy F., Liu J., Maes P., Tartar A., Capron A., Cesbron-Delauw M.F. Toxoplasma gondii: molecular structure of a dense granule antigen (GRA5) associated with the parasitophorous vacuole membrane. Mol. Biochem. Parasitol. 1993, 59:143-153.
21. Leriche M.A., Dubremetz J.F. Characterization of the protein contents of rhoptries and dense granules of Toxoplasma gondii tachyzoites by subcellular fractionation and monoclonal antibodies. Mol. Biochem. Parasitol. 1991, 45(2):249-259.
22. Magno R.C., Straker I.C., de Souza W., Attias M. Interrelations between the parasitophorous vacuole of Toxoplasma gondii and host cell organelles. Microsc. Microanal. 2005, 11:166-174.
23. Masek K.S., Zhu P., Freedman B.D., Hunter C.A. Toxoplasma gondii induces changes in intracellular calcium in macrophages. Parasitology 2007, 134:1973-1979.
24. Mercier C., Dubremetz W., Delauw M.F. Dense granules: Are they key organelles to help understand the parasitophorous vacuole of all apicomplexa parasites?. Int. J. Parasitol. 2005, 35:829-849.
25. Peng B.W., Lin J., Lin J.Y., Jiang M.S., Zhang T. Exogenous nitric oxide induces apoptosis in Toxoplasma gondii tachyzoites via a calcium signal transduction pathway. Parasitology 2003, 126:541-550.
26. Peng B.W., Huang Q.L., Lin J.Y., Jiang M.S. Signal role of exogenous arachidonic acid in invasion of macrophages by Toxoplasma gondii. Chin. J. Parasitol. Parasit. Dis. 2003, 21:296-299.
27. Peng B.W., Lin J.Y., Zhang T. Toxoplasma gondii induces prostaglandin E2 synthesis in macrophages via signal pathways for calcium-dependent arachidonic acid production and PKC-dependent induction of cyclooxygenase-2. Parasitol. Res. 2008, 102:1043-1050.
28. Pezzella N., Bouchot A., Pingret L., Klein C., Burlet H., Balossier G., Bonhomme P., Pinon J.M. Involvement of calcium and calmodulin in Toxoplasma gondii tachyzoite invasion. Eur. J. Cell Biol. 1997, 45:36-43.
29. Pietkiewicz H., Hiszczyn'ska-Sawicka E., Kur J., Petersen E., Nielsen H.V., Stankiewicz M., Andrzejewska I., Myjak P. Usefulness of Toxoplasma gondii-specific recombinant antigens in serodiagnosis of human toxoplasmosis. J. Clin. Microbiol. 2004, 42(4):1779-1781.
30. Radvin J.I., Murphy C.F., Guerrant R.L., Long-Krug S.A. Effect of antagonists of calcium and phospholipase A on the cytopathogenicity of Entamoeba histolytica. J. Infect. Dis. 1985, 152:542-549.
31. Saffer L.D., Long Krug S.A., Schwartzman J.D. The role of phospholipase in host cell penetration by Toxoplasma gondii. Am. J. Trop. Med. Hyg. 1989, 40:145-149.
32. Saffer L.D., Schwartzman J.D. A soluble phospholipase of Toxoplasma gondii associated with host cell penetration. J. Protozool. 1991, 38:454-460.
33. Seipel D., Ribeiro-Gomes F.L., Barcelos M.W., Ramalho A.V., Kanashiro M.M., Kipnis T.L., Arnholdt A.C. Monocytes/macrophages infected with Toxoplasma gondii do not increase co-stimulatory molecules while maintaining their migratory ability. APMIS 2009, 117:672-680.
34. Scorza T., D'Souza S., Laloup M., Dewit J., De Braekeleer J., Verschueren H., Vercammen M., Huygen K., Jongert E. A GRA1 DNA vaccine primes cytolytic CD8-T cells to control acute Toxoplasma gondii infection. Infect. Immun. 2003, 71:309-316.
35. Sibley L.D. Intracellular parasite invasion strategies. Science 2004, 304:248-253.
36. Sibley L.D., Pfefferkorn E.R., Boothroyd J.C. Development of genetic systems for Toxoplasma gondii. Parasitol. Today 1993, 9(10):392-395.
37. Sibley L.D., Niesman I.R., Parmley S.F., Cesbron-Delauw M.F. Regulated secretion of multi-lamellar vesicles leads to formation of a tubulo-vesicular network in host-cell vacuoles occupied by Toxoplasma gondii. J. Cell Sci. 1995, 108(4):1669-1677.
38. Sibley L.D., Weidner E., Krahenbuhl J.L. Phagosome acidification blocked by intracellular Toxoplasma gondii. Nature 1985, 315(6018):416-419.
39. Toborek M., Blanc E.M., Kaiser S., Mattson M.P., Hennig B. Linoleic acid potentiates TNF-mediated oxidative stress, disruption of calcium homeostasis, and apoptosis of cultured vascular endothelial cells. J. Lipid Res. 1997, 38(10):2155-2167.