Trypanosoma cruzi adenylyl cyclase is encoded by a complex multigene family

Molecular and Biochemical Parasitology

Volumn 104, Issue 2, 1999, Pages 205-217

  Taylor, Martin C ^a   Muhia, David K ^a   Baker, David A ^a   Mondragon, Angeles ^a   Schaap, Pauline ^b   Kelly, John M ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Adenylyl cyclase; Complementation; Trypanosomes

Indexed keywords

ADENYLATE CYCLASE; DIVALENT CATION; MAGNESIUM ION; MANGANESE; MICROBIAL ENZYME; RECOMBINANT PROTEIN;

ARTICLE; CATALYSIS; CHROMOSOME; CONTROLLED STUDY; COSMID; DNA SEQUENCE; ESCHERICHIA COLI; GENE ISOLATION; GENE SEQUENCE; GENETIC COMPLEMENTATION; GENETIC ORGANIZATION; MICROBIAL GENETICS; MULTIGENE FAMILY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; TRYPANOSOMA CRUZI;

ADENYLATE CYCLASE; AMINO ACID SEQUENCE; ANIMALS; BLOTTING, SOUTHERN; CATALYTIC DOMAIN; CHROMOSOME MAPPING; DNA, COMPLEMENTARY; GENES, PROTOZOAN; GENETIC COMPLEMENTATION TEST; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TRYPANOSOMA CRUZI;

ESCHERICHIA COLI; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA CRUZI;

EID: 0032738422     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-6851(99)00154-1     Document Type: Article

References (46)

1. Fraidenraich D., Pena C., Isola E.L. et al. Stimulation of Trypanosoma cruzi adenylyl cyclase by an (D-globin fragment from Triatoma hindgut: effect on differentiation of epimastigote to trypomastigote forms. Proc. Natl. Acad. Sci. USA. 90:1993;10140-10144.
2. Ouaissi A., Cornette J., Schoneck R. et al. Fibronectin cleavage fragments provide a growth factor-like activity for the differentiation of Trypanosoma cruzi trypomastigotes to amastigotes. Eur. J. Cell Biol. 59:1992;68-79.
3. Gonzales-Perdomo M., Romero P., Goldenberg S. Cyclic AMP and adenylate cyclase activators stimulate Trypanosoma cruzi differentiation. Exp. Parasitol. 66:1988;205-212.
4. Taussig R., Zimmermann G. Type-specific regulation of mammalian adenylyl cyclases by G protein pathways. Adv. Second Messenger Phosphoprotein Res. 32:1998;81-98.
5. sα and forskolin. Science. 268:1995;1769-1772.
6. Sanchez M.A., Zeoli D., Klamo E.M., Kavanaugh M.P., Landfear S.M. A family of putative receptor-adenylate cyclases from Leishmania donovani. J. Biol. Chem. 270:1995;17551-17558.
7. Alexandre S., Paindavoine P., Tebabi P. et al. Differential expression of a family of putative adenylate/guanylate cyclase genes in Trypanosoma brucei. Mol. Biochem. Parasitol. 43:1990;279-288.
8. Lowe D.G., Chang M.S., Hellmiss R. et al. Human atrial natriuretic peptide receptor defines a new paradigm for second messenger signal transduction. EMBO J. 8:1989;1377-1384.
9. Garcia E.S., Gonzalez M.S., de Azambuja P. et al. Induction of Trypanosoma cruzi metacyclogenesis in the gut of the hematophagous insect vector, Rhodnius prolixus, by hemoglobinand peptides carrying alpha D-globin sequences. Exp. Parasitol. 81:1995;255-261.
10. Heath S., Hieny S., Sher A. A cyclic AMP inducible gene expressed during the development of infective stages of Trypanosoma cruzi. Mol. Biochem. Parasitol. 43:1990;133-142.
11. Kendall G., Wilderspin A.F., Ashall F., Miles M.A., Kelly J.M. Trypanosoma cruzi glycosomal glyceraldehyde-3-phosphate dehydrogenase does not conform to the 'hotspot' topogenic signal model. EMBO J. 9:1990;2751-2758.
12. Kelly J.M. Isolation of DNA and RNA from Leishmania. Hyde J.E. Protocols in Molecular Parasitology. 1993;123-131 Humana Press Inc.
13. Cano M.I., Gruber A., Vazquez M. et al. Molecular karyotype of clone CL-Brener chosen for the Trypanosoma cruzi genome project. Mol. Biochem. Parasitol. 71:1995;273-278.
14. Kelly J.M., Das P., Tomas A.M. An approach to functional complementation by introduction of large DNA fragments into Trypanosoma cruzi and Leishmania donovani using a cosmid shuttle vector. Mol. Biochem. Parasitol. 65:1994;51-62.
15. Salazar N.A., Mondragon A., Kelly J.M. Mucin-like glycoprotein genes are closely linked to members of the trans-sialidase super-family at multiple sites in the Trypanosoma cruzi genome. Mol. Biochem. Parasitol. 78:1996;127-136.
16. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
17. Gilman A.G. Protein binding assays for cyclic nucleotides. Adv. Cyclic Nucleotide Res. 2:1972;9-24.
18. Vazquez M.P., Schijman A.G., Levin M.J. A short interspersed repetitive element provides a new 3′ acceptor site for trans-splicing in certain ribosomal P2 beta protein genes of Trypanosoma cruzi. Mol. Biochem. Parasitol. 64:1994;327-336.
19. Nakai K., Kanehisa M. A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics. 14:1992;897-911.
20. Bringaud F., Vedrenne C., Cuvillier A. et al. Conserved organization of genes in trypanosomatids. Mol. Biochem. Parasitol. 94:1998;249-264.
21. sα. · GTPγS Science. 278:1997;1907-1916.
22. sα activation. J. Biol. Chem. 272:1997;18849-18854.
23. βγ subunits. Science. 268:1995;1166-1169.
24. βγ but not the heterotrimer. J. Biol. Chem. 271:1996;26445-26448.
25. Liu Y., Ruoho A.E., Rao V.D., Hurley J.H. Catalytic mechanism of the adenylyl and guanylyl cyclases: Modeling and mutational analysis. Proc. Natl. Acad. Sci. USA. 94:1997;13414-13419.
26. Alexandre S., Paindavoine P., Hanocq-Quertier J., Paturiaux-Hanocq F., Tebabi P., Pays E. Families of adenylate cyclase genes in Trypanosoma brucei. Mol. Biochem. Parasitol. 77:1996;173-182.
27. Colombo S., Ma P., Cauwenberg L. et al. Involvement of distinct G-proteins, Gpa2 and Ras, in glucose- and intracellular acidification-induced cAMP signalling in the yeast Saccharomyces cerevisiae. EMBO J. 17:1998;3326-3341.
28. Carnero A., Liyanage M., Stabel S., Lacal J.C. Evidence for different signalling pathways of PKC ζ and ras-p21 in Xenopus oocytes. Oncogene. 11:1995;1541-1547.
29. Olate J., Martinez S., Purcell P. et al. Molecular cloning and sequence determination of four different cDNA species coding for alpha-subunits of G proteins from Xenopus laevis oocytes. FEBS Lett. 268:1990;27-31.
30. Da Silveira J.F., Zingales B., Colli W. Characterization of an adenylyl cyclase activity in particulate preparations from epimastigote forms of Trypanosoma cruzi. Biochim. Biophys. Acta. 481:1977;722-733.
31. Zingales B., Carniol C., Abramhamson P.A., Colli W. Purification of an adenylyl cyclase-containing plasma membrane fraction from Trypanosoma cruzi. Biochim. Biophys. Acta. 550:1979;233-244.
32. Zimmerman G., Zhou D., Taussig R. Mutations uncover a role for two magnesium ions in the catalytic mechanism of adenylyl cyclase. J. Biol. Chem. 273:1998;19650-19655.
33. 2+) binding site. Biochemistry. 37:1998;16183-16191.
34. Flawia M.M., Tellez-Inon M.T., Torres H.N. Signal transduction mechanisms in Trypanosoma cruzi. Parasitol. Today. 13:1997;30-33.
35. Zhang G., Liu Y., Ruoho A.E., Hurley J.H. Structure of the adenylyl cyclase catalytic core. Nature. 386:1997;247-253.
36. Yan S.-Z., Huang Z.-H., Shaw R.S., Tang W.-J. The conserved asparagine and arginine are essential for catalysis of mammalian adenylyl cyclase. J. Biol. Chem. 272:1997;12342-12349.
37. Tucker C.I., Hurley J.H., Miller T.R., Hurley J.B. Two amino acid substitutions convert a guanylyl cyclase, RetGC-1, into an adenylyl cyclase. Biochemistry. 95:1998;5993-5997.
38. Eisenschlos C.D., Paladini A.A., Molina y Vedia L., Torres H.N., Flawia M.M. Evidence for the existence of an Ns-type regulatory protein in Trypanosoma cruzi membranes. Biochem. J. 237:1986;913-917.
39. Field H., Ali B.R., Sherwin T., Gull K., Croft S.L., Field M.C. TbRab2p, a marker for the endoplasmic reticulum of Trypanosoma brucei, localises to the ERGIC in mammalian cells. J. Cell Sci. 112:1999;147-156.
40. Di Noia J.M., D'Orso I., Aslund L., Sanchez D.O., Frasch A.C. The Trypanosoma cruzi mucin family is transcribed from hundreds of genes having hypervariable regions. J. Biol. Chem. 273:1998;10843-10850.
41. Wincker P., Murto-Dovales A.C., Goldenberg S. Nucleotide sequence of a representative member of a Trypanosoma cruzi dispersed gene family. Mol. Biochem. Parasitol. 55:1992;217-220.
42. Takle G.B., Cross G.A. An 85-kilodalton surface antigen gene family of Trypanosoma cruzi encodes polypeptides homologous to bacterial neuraminidases. Mol. Biochem. Parasitol. 48:1991;185-198.
43. Bitter W., Gerrits H., Kieft R., Borst P. The role of transferrin-receptor variation in the host range of Trypanosoma brucei. Nature. 391:1998;499-502.
44. Takle G.B., O'Connor J., Young A.J., Cross G.A. Sequence homology and absence of mRNA defines a possible pseudogene member of the Trypanosoma cruzi gp85/sialidase multigene family. Mol. Biochem. Parasitol. 56:1992;117-127.
45. Ligtenberg M.J., Bitter W., Kieft R. et al. Reconstitution of a surface transferrin binding complex in insect form Trypanosoma brucei. EMBO J. 13:1994;2565-2573.
46. Steverding D., Stierhof Y.D., Chaudhri M. et al. ESAG 6 and 7 products of Trypanosoma brucei form a transferrin binding protein complex. Eur. J. Cell Biol. 64:1994;78-87.