Trypanosoma cruzi calreticulin is a lectin that binds monoglucosylated oligosaccharides but not protein moieties of glycoproteins

Molecular Biology of the Cell

Volumn 10, Issue 5, 1999, Pages 1381-1394

  Labriola, Carlos ^a,b   Cazzulo, Juan J ^b   Parodi, Armando J ^a  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b UNIVERSIDAD NACIONAL DE SAN MARTÍN   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

CALRETICULIN; CRUZIPAIN; DNA; GLYCOPROTEIN; LECTIN; MESSENGER RNA; N ACETYL BETA GLUCOSAMINIDASE; OLIGOSACCHARIDE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; EVOLUTION; GLYCOSYLATION; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; TRYPANOSOMA CRUZI;

EUKARYOTA; MAMMALIA; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA CRUZI;

EID: 0032918454     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.5.1381     Document Type: Article

References (55)

1. Arunachalam, B., and Cresswell, P. (1995). Molecular requirements for the interaction of class II major histocompatibility complex and invariant chain with calnexin. J. Biol. Chem. 270, 2784-2790.
2. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1994). Preparation and analysis of RNA. In: Current Protocols in Molecular Biology, ed. K. Janson K, New York: John Wiley and Sons, 4.1.1-4.1.6, 4.9.1-4.9.6.
3. Baldauf, S.L., and Palmer, J.D. (1993). Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. Proc. Natl. Acad. Sci. USA 90, 11558-11562.
4. + thymocytes. J. Biol. Chem. 273, 23674-23680.
5. Bontempi, E., Martínez, J., and Cazzulo, J.J. (1989). Subcellular localization of a cysteine proteinase from Trypanosoma cruzi. Mol. Biochem. Parasitol. 33, 43-48.
6. Borst, P., Fase-Fowler, F., Frasch, A.C.C., Hoeijmakers, J.H.J., and Weijers, P.J. (1980). Characterization of DNA from Trypanosoma brucei and related trypanosomes by restriction endonuclease digestion. Mol. Biochem. Parasitol. 1, 221-246.
7. Bosch, M., Trombetta, S., Engstrom, U., and Parodi, A.J. (1988). Characterization of dolichol diphosphate oligosaccharide:protein oligosaccharyltransferase and of glycoprotein processing glucosidases occurring in trypanosomatids. J. Biol. Chem., 263, 17360-17365.
8. Campetella, O., Martínez, J., and Cazzulo, J.J. (1990). A major cysteine proteinase is developmentally regulated in Trypanosoma cruzi. FEMS Microbiol. Lett. 67, 145-150.
9. Cazzulo, J.J., Couso, R., Raimondi, A., Wernstedt, C., and Hellman, U. (1989). Further characterization and partial amino acid sequence of a cysteine proteinase from Trypanosoma cruzi. Mol. Biochem. Parasitol. 33, 33-42.
10. Cazzulo, J.J., Franke de Cazzulo, B.M., Engel, J.C., and Cannata, J.J. (1985). End products and enzyme levels of aerobic fermentation in trypanosomatids. Mol. Biochem. Parasitol. 16, 329-343.
11. Cazzulo, J.J., Stoka, V., and Turk, V. (1997). Cruzipain, the major cysteine proteinase from the protozoan parasite Trypanosoma cruzi. Biol. Chem. 378, 1-10.
12. de la Canal, L., and Parodi, A.J. (1987). Synthesis of dolichol derivatives in trypanosomatids. Characterization of enzymatic patterns. J. Biol. Chem. 262, 11128-11133.
13. Fernández, F., Jannatipour, M., Hellman, U., Rokeach, L., and Parodi, A.J. (1996). A new stress protein: synthesis of Schizosaccharomyces pombe UDP-Glc:glycoprotein glucosyltransferase mRNA is induced under stress conditions but the enzyme is not essential for cell viability. EMBO J. 15, 705-713.
14. Fernández, F., Trombetta, S.E., Hellman, U., and Parodi, A.J. (1994). Purification to homogeneity of UDP-Glc:glycoprotein glucosyltransferase from Schizosaccharomyces pombe and apparent absence of the enzyme from Saccharomyces cerevisiae. J. Biol. Chem. 269, 30701-30706.
15. Gañán, S., Cazzulo, J.J., and Parodi, A.J. (1991). A major proportion of N-glycoproteins is transiently glucosylated in the endoplasmic reticulum. Biochemistry 30, 3098-3104.
16. Gotz, G., Gañán, S., and Parodi, A.J. (1991). Glucosylation of glycoproteins in Crithidia fasciculata. Mol. Biochem. Parasitol. 45, 265-274.
17. Hammond, C., Braakman, I., and Helenius, A. (1994). Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc. Natl. Acad. Sci. USA 91, 913-917.
18. Hebert, D.N., Foellmer, B., and Helenius, A. (1995). Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell 81, 425-433.
19. Hebert, D.N., Foellmer, B., and Helenius, A. (1996). Calnexin and calreticulin promote folding, delay oligomerization and suppress degradation of influenza hemagglutinin in microsomes. EMBO J. 15, 2961-2968.
20. Helenius, A., Trombetta, E.S., Hebert, D.N., and Simons, J.F. (1997). Calnexin, calreticulin and the folding of glycoproteins. Trends Cell Biol. 7, 193-200.
21. Ibáñez, C.F., Affranchino, J.L., and Frasch, A.C.C. (1987). Antigenic determinants of Trypanosoma cruzi defined by cloning of parasite DNA. Mol. Biochem. Parasitol. 25, 175-184.
22. Jannatipour, M., and Rokeach, L.A. (1995). The Schizosaccharomyces pombe homologue of the chaperone calnexin is essential for viability. J. Biol. Chem. 270, 4845-4853.
23. Josi, M., Pogue, G.P., Duncan, R.C., Lee, N.S., Singh, N.K., Atreya, C.D., Dwyer, D.M., and Nakhasi, H.L. (1996). Isolation and characterization of Leishmania donovani calreticulin gene and its conservation of the RNA binding activity. Mol. Biochem. Parasitol. 81, 53-64.
24. Kearse, K.P., Williams, D.B., and Singer, A. (1994). Persistence of glucose residues on core oligosaccharides prevents association of TCRα and TCRβ proteins with calnexin and results specifically in accelerated degradation of nascent TCRα proteins within the endoplasmic reticulum. EMBO J. 13, 3678-3686.
25. Kornfeld, R., and Kornfeld, S. (1985). Assemby of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54, 631-664.
26. Labriola, C., Cazzulo, J.J., and Parodi, A.J. (1995). Retention of glucose residues added by the UDP-Glc:glycoprotein glucosyltransferase delays exit of glycoproteins from the endoplasmic reticulum. J. Cell Biol. 130, 771-779.
27. Low, P., Dallner, G., Mayor, S., Cohen, S., Chait, B.T., and Menon, A.K. (1991). The mevalonate pathway in the blood-stream form of Trypanosoma brucei. Identification of dolichols containing 11 and 12 isoprene residues. J. Biol. Chem. 266, 19250-19257.
28. Lupattelli, F., Pedrazzini, E., Bollini, R., Vitale, A., and Ceriotti, A. (1997). The rate of phaseolin assembly is controlled by the glucosylation state of its N-linked oligosaccharide chains. Plant Cell 9, 597-609.
29. Mendelzon, D.H., Previato, J.O., and Parodi, A.J. (1986). Characterization of protein-linked oligosaccharides in trypanosomatid flagellates. Mol. Biochem. Parasitol. 18, 355-367.
30. Metzner, S.I., Sousa, M.C., Hellman, U., Cazzulo, J.J., and Parodi, A.J. (1996). The use of UDP-Glc:glycoprotein glucosyltransferase for radiolabeling protein-linked high mannose-type oligosaccharides. Cell. Mol. Biol. 42, 631-635.
31. Nauseef, W.M., McCormick, S.J., and Clark, R.A. (1995). Calreticulin functions as a molecular chaperone in the biosynthesis of myeloperoxidase. J. Biol. Chem. 270, 4741-4747.
32. Ou, W.-J., Cameron, P.H., Thomas, D.Y., and Bergeron, J.J.M. (1993). Association of folding intermediates of glycoproteins with calnexin during protein maturation. Nature 364, 771-776.
33. + in Schizosaccharomyces pombe is an essential gene which can be complemented by its soluble ER domain. EMBO J. 14, 3064-3072.
34. Parodi, A.J. (1993). N-Glycosylation in trypanosomatid protozoa. Glycobiology 3, 193-199.
35. Parodi, A.J., and Cazzulo, J.J. (1982). Protein glycosylation in Trypanosoma cruzi. II. Partial characterization of protein-bound oligosaccharides labeled "in vivo." J. Biol. Chem. 257, 7641-7645.
36. Parodi, A.J., Lederkremer, G.Z., and Mendelzon, D.H. (1983a). Protein glycosylation in Trypanosoma cruzi. The mechanism of glycosylation and structure of protein-bound oligosaccharides. J. Biol. Chem. 258, 5589-5595.
37. 2 in calf thyroid slices: a possible recognition signal in the processing of glycoproteins. J. Biol. Chem. 258, 8260-8265.
38. 2 occurs in rat liver and Phaseolus vulgaris cells. J. Biol. Chem. 259, 6351-6357.
39. Parodi, A.J., and Quesada-Allué, L.A. (1982). Protein glycosylation in Trypanosoma cruzi. I. Characterization of dolichol-bound monosaccharides and oligosaccharides synthesized in vivo. J. Biol. Chem. 257, 7641-7645.
40. Parodi, A.J., Quesada-Allué, L.A., and Cazzulo, J.J. (1981). Pathway of protein glycosylation in the trypanosomatid Crithidia fasciculata. Proc. Natl. Acad. Sci. USA 78, 6201-6205.
41. Peterson, J.R., Ora, A., Nguyen Van, P., and Helenius, A. (1995). Calreticulin is a lectin-like molecular chaperone for glycoproteins of the endoplasmic reticulum. Mol. Biol. Cell 6, 1173-1184.
42. Previato, J.O., Mendelzon, D.H., and Parodi, A.J. (1986). Characterization of dolichol monophosphate- and dolichol diphosphate-linked saccharides in trypanosomatid flagellates. Mol. Biochem. Parasitol. 18, 343-357.
43. Quesada-Allué, L.A., and Parodi, A.J. (1983). Novel mannose carrier in the trypanosomatid Crithidia fasciculata behaving as a short α-saturated polyprenyl phosphate. Biochem. J. 212, 123-128.
44. Rodan, A.R., Simons, J.F., Trombetta, E.S., and Helenius, A. (1996). N-Linked oligosaccharides are necessary and sufficient for association of glycosylated forms of bovine RNase with calnexin and calreticulin. EMBO J. 15, 6921-6930.
45. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
46. Solgin, M.L. (1997). History assignment: when was the mitochondrion founded?. Curr. Opin. Genet. Dev. 7, 792-799.
47. Sousa, M., Ferrero-García, M., and Parodi, A.J. (1992). Recognition of the oligosaccharide and protein moieties of glycoproteins by the UDP-Glc:glycoprotein glucosyltransferase. Biochemistry 31, 97-105.
48. Sousa, M., and Parodi, A.J. (1995). The molecular basis for the recognition of misfolded glycoproteins by the UDP-Glc:glycoprotein glucosyltransferase. EMBO J. 15, 4196-4203.
49. Spiro, R.G., Zhu, Q., Bhoyroo, V., and Söling, H.-D. (1996). Definition of the lectin-like properties of the molecular chaperone, calreticulin, and demonstration of its copurification with endomannosidase from rat liver Golgi. J. Biol. Chem. 271, 11588-11594.
50. Tibbetts, R.S., Kim, I.Y., Olson, C.L., Barthel, L.M., Sullivan, M.A., Winquist, A.G., Miller, S.D., and Engman, D.M. (1994). Molecular cloning and characterization of the 78-kilodalton glucose-regulated protein of Trypanosoma cruzi. Infect. Immun. 62, 2499-2507.
51. Trombetta, S., Bosch, M., and Parodi, A.J. (1989). Glucosylation of glycoproteins by mammalian, plant, fungal and trypanosomatid protozoa microsomal proteins. Biochemistry 28, 8108-8116.
52. 2 oligosaccharide as an initial step in recognizing unfolded glycoproteins. J. Biol. Chem. 270, 4697-4704.
53. Zapun, A., Petrescu, S., Rudd, P.M., Dwek, R.A., Thomas, D.Y., and Bergeron, J.J. (1997). Conformation independent binding of monoglucosylated ribonuclease B to calnexin. Cell 88, 29-38.
54. Zhang, J.-X., Braakman, I., Matlack, K.E.S., and Helenius, A. (1997). Quality control in the secretory pathway: the role of calreticulin, calnexin and BiP in the retention of glycoproteins with C-terminal truncations. Mol. Biol. Cell 8, 1943-1954.
55. Zhang, Q., Tector, M., and Salter, R.D. (1995). Calnexin recognizes carbohydrate and protein determinants of class I major histocompatibility complex molecules. J. Biol. Chem. 270, 3944-3948.