Preparing for an invasion: Charting the pathway of adhesion proteins to Toxoplasma micronemes

Parasitology Research

Volumn 98, Issue 5, 2006, Pages 389-395

  Huynh, My Hang ^a   Harper, Jill M ^a   Carruthers, Vern B ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; M2AP PROPEPTIDE; MIC2 PROTEIN; PROTEIN; PYRIMETHAMINE SULFADIAZINE; UNCLASSIFIED DRUG;

CELL ORGANELLE; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; KNOCKOUT MOUSE; MICRONEME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; REVIEW; TOXOPLASMA; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ANIMALS; CELL ADHESION; HUMANS; ORGANELLES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; TOXOPLASMA; TOXOPLASMOSIS; VIRULENCE FACTORS;

TOXOPLASMA; TOXOPLASMA GONDII;

EID: 33645223243     PISSN: 09320113     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00436-005-0062-2     Document Type: Review

References (49)

1. Anderson RG, Pathak RK (1985) Vesicles and cisternae in the trans Golgi apparatus of human fibroblasts are acidic compartments. Cell 40:635-643
2. Arvan P, Halban PA (2004) Sorting ourselves out: seeking consensus on trafficking in the beta-cell. Traffic 5:53-61
3. Barragan A, Brossier F, Sibley LD (2005) Transepithelial migration of Toxoplasma gondii involves an interaction of intercellular adhesion molecule 1 (ICAM-1) with the parasite adhesin MIC2. Cell Microbiol 7:561-568
4. Blazquez M, Shennan KI (2000) Basic mechanisms of secretion: sorting into the regulated secretory pathway. Biochem Cell Biol 78:181-191
5. Bowers K, Stevens TH (2005) Protein transport from the late Golgi to the vacuole in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1744:438-454
6. Brossier F, Jewett TJ, Sibley LD, Urban S (2005) A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma. Proc Natl Acad Sci USA 102:4146-4151
7. Burgess TL, Kelly RB (1987) Constitutive and regulated secretion of proteins. Annu Rev Cell Biol 3:243-293
8. Carruthers VB, Hakansson S, Giddings OK, Sibley LD (2000a) Toxoplasma gondii uses sulfated proteoglycans for substrate and host cell attachment. Infect Immun 68:4005-4011
9. Carruthers VB, Moreno SNJ, Sibley LD (1999) Ethanol and acetaldehyde elevate intracellular calcium and stimulate microneme discharge in Toxoplasma gondii. Biochem J 342:379-386
10. Carruthers VB, Sherman GD, Sibley LD (2000b) The Toxoplasma adhesive protein MIC2 is proteolytically processed at multiple sites by two parasite-derived proteases. J Biol Chem 275:14346-14353
11. Carruthers VB, Sibley LD (1997) Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur J Cell Biol 73:114-123
12. Castro-Fernandez C, Maya-Nunez G, Conn PM (2005) Beyond the signal sequence: protein routing in health and disease. Endocr Rev 26:479-503
13. Cerede O, Dubremetz JF, Soete M, Deslee D, Vial H, Bout D, Lebrun M (2005) Synergistic role of micronemal proteins in Toxoplasma gondii virulence. J Exp Med 201:453-463
14. Chanat E, Huttner WB (1991) Milieu-induced, selective aggregation of regulated secretory proteins in the trans-Golgi network. J Cell Biol 115:1505-1519
15. Chance RE, Ellis RM, Bromer WW (1968) Porcine proinsulin: characterization and amino acid sequence. Science 161:165-167
16. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M (1990) Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62:317-329
17. Di Cristina M, Spaccapelo R, Soldati D, Bistoni F, Crisanti A (2000) Two conserved amino acid motifs mediate protein targeting to the micronemes of the apicomplexan parasite Toxoplasma gondii. Mol Cell Biol 20:7332-7341
18. Dowse TJ, Pascall JC, Brown KD, Soldati D (2005) Apicomplexan rhomboids have a potential role in microneme protein cleavage during host cell invasion. Int J Parasitol 35:747-756
19. Dubey JP, Beattie CP (1988) Toxoplasmosis of animals and man. CRC, Boca Raton, FL
20. Fuller RS, Sterne RE, Thorner J (1988) Enzymes required for yeast prohormone processing. Annu Rev Physiol 50:345-362
21. Furtado GC, Cao Y, Joiner KA (1992) Laminin on Toxoplasma gondii mediates parasite binding to the b1 integrin receptor a6/ b1 on human foreskin fibroblasts and Chinese hamster ovary cells. Infect Immun 60:4925-4931
22. Furtado GC, Slowik M, Kleinman HK, Joiner KA (1992) Laminin enhances binding of Toxoplasma gondii tachyzoites to J774 murine macrophage cells. Infect Immun 60:2337-2342
23. Giraudo CG, Rosales Fritz VM, Maccioni HJ (1999) GA2/GM2/GD2 synthase localizes to the trans-golgi network of CHO-K1 cells. Biochem J 342(Pt 3):633-640
24. Halban PA, Irminger JC (2003) Mutant proinsulin that cannot be converted is secreted efficiently from primary rat beta-cells via the regulated pathway. Mol Biol Cell 14:1195-1203
25. Harper JM, Hoff EF, Carruthers VB (2004) Multimerization of the Toxoplasma gondii MIC2 integrin-like A-domain is required for binding to heparin and human cells. Mol Biochem Parasitol 134:201-212
26. Huynh MH, Rabenau KE, Harper JM, Beatty WL, Sibley LD, Carruthers VB (2003) Rapid invasion of host cells by Toxoplasma requires secretion of the MIC2-M2AP adhesive protein complex. EMBO J 22:2082-2090
27. Jewett TJ, Sibley LD (2003) Aldolase forms a bridge between cell surface adhesins and the actin cytoskeleton in apicomplexan parasites. Mol Cell 11:885-894
28. Jewett TJ, Sibley LD (2004) The toxoplasma proteins MIC2 and M2AP form a hexameric complex necessary for intracellular survival. J Biol Chem 279:9362-9369
29. Kravetz JD, Federman DG (2005) Toxoplasmosis in pregnancy. Am J Med 118:212-216
30. Kuliawat R, Arvan P (1992) Protein targeting via the "constitutive- like" secretory pathway in isolated pancreatic islets: passive sorting in the immature granule compartment. J Cell Biol 118:521-529
31. Kuliawat R, Arvan P (1994) Distinct molecular mechanisms for protein sorting within immature secretory granules of pancreatic beta-cells. J Cell Biol 126:77-86
32. Luft BJ, Remington JS (1992) Toxoplasmic encephalitis in AIDS. Clin Infect Dis 15:211-222
33. Mital J, Meissner M, Soldati D, Ward GE (2005) Conditional expression of Toxoplasma gondii apical membrane antigen-1 (TgAMA1) demonstrates that TgAMA1 plays a critical role in host cell invasion. Mol Biol Cell 16:4341-4349
34. Mogelsvang S, Marsh BJ, Ladinsky MS, Howell KE (2004) Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5:338-345
35. Molinete M, Lilla V, Jain R, Joyce PB, Gorr SU, Ravazzola M, Halban PA (2000) Trafficking of non-regulated secretory proteins in insulin secreting (INS-1) cells. Diabetologia 43:1157-1164
36. Molloy SS, Anderson ED, Jean F, Thomas G (1999) Bi-cycling the furin pathway: from TGN localization to pathogen activation and embryogenesis. Trends Cell Biol 9:28-35
37. Nakayama K (1997) Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem J 327(Pt 3):625-635
38. Ortega-Barria E, Boothroyd JC (1999) A Toxoplasma lectin-like activity specific for sulfated polysaccharides is involved in host cell infection. J Biol Chem 274:1267-1276
39. Rabenau KE, Sohrabi A, Tripathy A, Reitter C, Ajioka JW, Tomley FM, Carruthers VB (2001) TgM2AP participates in Toxoplasma gondii invasion of host cells and is tightly associated with the adhesive protein TgMIC2. Mol Microbiol 41:1-12
40. Robibaro B, Hoppe HC, Yang M, Coppens I, Ngo HM, Stedman TT, Paprotka K, Joiner KA (2001) Endocytosis in different lifestyles of protozoan parasitism: role in nutrient uptake with special reference to Toxoplasma gondii. Int J Parasitol 31:1343-2353
41. Sibley LD (2004) Intracellular parasite invasion strategies. Science 304:248-253
42. Soldati D, Foth BJ, Cowman AF (2004) Molecular and functional aspects of parasite invasion. Trends Parasitol 20:567-574
43. Steinman RM, Mellman IS, Muller WA, Cohn ZA (1983) Endocytosis and the recycling of plasma membrane. J Cell Biol 96:1-27
44. Thomas G, Thorne BA, Thomas L, Allen RG, Hruby DE, Fuller R, Thorner J (1988) Yeast KEX2 endopeptidase correctly cleaves a neuroendocrine prohormone in mammalian cells. Science 241:226-230
45. Tooze SA, Flatmark T, Tooze J, Huttner WB (1991) Characterization of the immature secretory granule, an intermediate in granule biogenesis. J Cell Biol 115:1491-1503
46. Wan KL, Carruthers VB, Sibley LD, Ajioka JW (1997) Molecular characterization of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol Biochem Parasitol 84:203-214
47. Wetzel DM, Chen LA, Ruiz FA, Moreno SN, Sibley LD (2004) Calcium-mediated protein secretion potentiates motility in Toxoplasma gondii. J Cell Sci 117:5739-5748
48. Wilcox CA, Redding K, Wright R, Fuller RS (1992) Mutation of a tyrosine localization signal in the cytosolic tail of yeast Kex2 protease disrupts Golgi retention and results in default transport to the vacuole. Mol Biol Cell 3:1353-1371
49. Zhang B, Chang A, Kjeldsen TB, Arvan P (2001) Intracellular retention of newly synthesized insulin in yeast is caused by endoproteolytic processing in the Golgi complex. J Cell Biol 153:1187-1198