A novel Myb-related protein involved in transcriptional activation of encystation genes in Giardia lamblia

Molecular Microbiology

Volumn 46, Issue 4, 2002, Pages 971-984

  Sun, Chin Hung ^a   Palm, Daniel ^b   McArthur, Andrew G ^c   Svärd, Staffan G ^b   Gillin, Frances D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; POLYSACCHARIDE; PROTEIN GMYB2; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CARBOHYDRATE SYNTHESIS; CELL NUCLEUS; DATA BASE; DNA BINDING; EUKARYOTE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUSION; GENETIC CODE; GENOME ANALYSIS; GIARDIA LAMBLIA; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE MYB; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTOZOAL GENETICS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

5' FLANKING REGION; ALDOSE-KETOSE ISOMERASES; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL NUCLEUS; CLONING, MOLECULAR; GENE EXPRESSION REGULATION; GIARDIA LAMBLIA; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); PROTOZOAN PROTEINS; SEQUENCE DELETION; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS;

EUKARYOTA; GIARDIA; GIARDIA INTESTINALIS; PROTOZOA;

EID: 0036434922     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2002.03233.x     Document Type: Article

References (64)

1. Abel, E.S., Davids, B.J., Robles, L.D., Loflin, C.E., Gillin, F.D., and Chakrabarti, R. (2001) Possible roles of protein kinase A in cell motility and excystation of the early diverging eukaryote Giardia lamblia. J Biol Chem 276: 10320-10329.
2. Adam, R.D. (1991) The biology of Giardia spp. Microbiol Rev 55: 706-732.
3. Allen, R.D., 3rd, Bender, T.P., and Siu, G. (1999) c-Myb is essential for early T cell development. Genes Dev 13: 1073-1078.
4. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
5. Biedenkapp, H., Borgmeyer, U., Sippel, A.E., and Klempnauer, K.H. (1988) Viral myb oncogene encodes a sequence-specific DNA-binding activity. Nature 335: 835-837.
6. Black, M.W., and Boothroyd, J.C. (2000) Lytic cycle of Toxoplasma gondii. Microbiol Mol Biol Rev 64: 607-623.
7. Cavalier-Smith, T. (1991) The evolution of cells. In Evolution of Life, Fossils, Molecules and Culture. Osawa, S. and Honjo, T. (eds). Tokyo: Springer-Verlag, pp. 271-304.
8. Cross, G.A. (1996) Antigenic variation in trypanosomes: Secrets surface slowly. Bioessays 18: 283-291.
9. Eichinger, D. (2001) Encystation in parasitic protozoa. Curr Opin Microbiol 4: 421-426.
10. Elmendorf, H.G., Singer, S.M., and Nash, T.E. (2000) Targeting of proteins to the nuclei of Giardia lamblia. Mol Biochem Parasitol 106: 315-319.
11. Elmendorf, H.G., Singer, S.M., Pierce, J., Cowan, J., and Nash, T.E. (2001) Initiator and upstream elements in the a2-tubulin promoter of Giardia lamblia. Mol Biochem Parasitol 113: 157-169.
12. Erlandsen, S.L., Macechko, P.T., van Keulen, H., and Jarroll, E.L. (1996) Formation of the Giardia cyst wall: Studies on extracellular assembly using immunogold labeling and high resolution field emission SEM. J Eukaryot Microbiol 43: 416-429.
13. Gabrielsen, O.S., Sentenac, A., and Fromageot, P. (1991) Specific DNA binding by c-Myb: Evidence for a double helix-turn-helix-related motif. Science 253: 1140-1143.
14. Gilchrist, C.A., Holm, C.F., Hughes, M.A., Schaenman, J.M., Mann, B.J., and Petri, W.A. Jr (2001) Identification and characterization of an Entamoeba histolytica upstream regulatory element 3 sequence-specific DNA-binding protein containing EF-hand motifs. J Biol Chem 276: 11838-11843.
15. Gillin, F.D., and Reiner, D.S. (1996) Cell biology of the primitive eukaryote Giardia lamblia. Annu Rev Microbiol 50: 679-705.
16. Gillin, F.D., Reiner, D.S., Gault, M.J., Douglas, H., Das, S., Wunderlich, A., and Sauch, J.F. (1987) Encystation and expression of cyst antigens by Giardia lamblia in vitro. Science 235: 1040-1043.
17. Gonda, T.J., Gough, N.M., Dunn, A.R., and de Blaquiere, J. (1985) Nucleotide sequence of cDNA clones of the murine myb proto-oncogene. EMBO J 4: 2003-2008.
18. Guo, K., Anjard, C., Harwood, A., Kim, H.J., Newell, P.C., and Gross, J.D. (1999) A myb-related protein required for culmination in Dictyostelium. Development 126: 2813-2822.
19. Hashimoto, T., Nakamura, Y., Nakamura, F., Shirakura, T., Adachi, J., Goto, N., Okamoto, K., and Hasegawa, M. (1994) Protein phylogeny gives a robust estimation for early divergences of eukaryotes: Phylogenetic place of a mitochondria-lacking protozoan, Giardia lamblia. Mol Biol Evol 11: 65-71.
20. Hashimoto, T., Nakamura, Y., Kamaishi, T., Nakamura, F., Adachi, J., Okamoto, K., and Hasegawa, M. (1995) Phylogenetic place of mitochondrion-lacking protozoan, Giardia lamblia, inferred from amino acid sequences of elongation factor 2. Mol Biol Evol 12: 782-793.
21. Hehl, A.B., Marti, M., and Kohler, P. (2000) Stage-specific expression and targeting of cyst wall protein-green fluorescent protein chimeras in Giardia. Mol Biol Cell 11: 1789-1800.
22. Holberton, D.V., and Marshall, J. (1995) Analysis of consensus sequence patterns in Giardia cytoskeleton gene promoters. Nucleic Acids Res 23: 2945-2953.
23. Horrocks, P., Dechering, K., and Lanzer, M. (1998) Control of gene expression in Plasmodium falciparum. Mol Biochem Parasitol 95: 171-181.
24. Jin, H., and Martin, C. (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41: 577-585.
25. Kabnick, K.S., and Peattie, D.A. (1990) In situ analyses reveal that the two nuclei of Giardia lamblia are equivalent. J Cell Sci 95: 353-360.
26. Katzen, A.L., Jackson, J., Harmon, B.P., Fung, S.M., Ramsay, G., and Bishop, J.M. (1998) Drosophila myb is required for the G2/M transition and maintenance of diploidy. Genes Dev 12: 831-843.
27. Keister, D.B. (1983) Axenic culture of Giardia lamblia. TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77: 487-488.
28. Klempnauer, K.H., and Sippel, A.E. (1987) The highly conserved amino-terminal region of the protein encoded by the v-myb oncogene functions as a DNA-binding domain. EMBO J 6: 2719-2725.
29. Kneller, D.G., Cohen, F.E., and Langridge, R. (1990) Improvements in protein secondary structure prediction by an enhanced neural network. J Mol Biol 214: 171-182.
30. Knodler, L.A., Svard, S.G., Silberman, J.D., Davids, B.J., and Gillin, F.D. (1999) Developmental gene regulation in Giardia lamblia: First evidence for an encystation-specific promoter and differential 5′ mRNA processing. Mol Microbiol 34: 327-340.
31. Knodler, L.A., Noiva, R., Mehta, K., McCaffery, J.M., Aley, S.B., Svard, S.G., et al. (2000) Novel protein-disulfide isomerases from the early-diverging protist Giardia lamblia. J Biol Chem 274: 29805-29811.
32. Lipsick, J.S. (1996) One billion years of Myb. Oncogene 13: 223-235.
33. Liston, D.R., Lau, A.O., Ortiz, D., Smale, S.T., and Johnson, P.J. (2001) Initiator recognition in a primitive eukaryote: IBP39, an initiator-binding protein from Trichomonas vaginalis. Mol Cell Biol 21: 7872-7882.
34. Lujan, H.D., Mowatt, M.R., Conrad, J.T., Bowers, B., and Nash, T.E. (1995) Identification of a novel Giardia lamblia cyst wall protein with leucine-rich repeats. Implications for secretory granule formation and protein assembly into the cyst wall. J Biol Chem 270: 29307-29313.
35. Lujan, H.D., Mowatt, M.R., and Nash, T.E. (1997) Mechanisms of Giardia lamblia differentiation into cysts. Microbiol Mol Biol Rev 61: 294-304.
36. Marshall, M.M., Naumovitz, D., Ortega, Y., and Sterling, C.R. (1997) Waterborne protozoan pathogens. Clin Microbiol Rev 10: 67-85.
37. McArthur, A.G., Morrison, H.G., Nixon, J.E., Passamaneck, N.Q., Kim, U., Hinkle, G., et al. (2000) The Giardia genome project database. FEMS Microbiol Lett 189: 271-273.
38. Mowatt, M.R., Lujan, H.D., Cotton, D.B., Bower, B., Yee, J., Nash, T.E., and Stibbs, H.H. (1995) Developmentally regulated expression of a Giardia lamblia cyst wall protein gene. Mol Microbiol 15: 955-963.
39. Muller, M. (1992) Energy metabolism of ancestral eukaryotes: A hypothesis based on the biochemistry of amitochondriate parasitic protists. Biosystems 28: 33-40.
40. Nicolaides, N.C., Gualdi, R., Casadevall, C., Manzella, L., and Calabretta, B. (1991) Positive autoregulation of c-myb expression via Myb binding sites in the 5′ flanking region of the human c-myb gene. Mol Cell Biol 11: 6166-6176.
41. Ogata, K., Morikawa, S., Nakamura, H., Sekikawa, A., Inoue, T., Kanai, H., Sarai, A., Ishii, S., and Nishimura, Y. (1994) Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell 79: 639-648.
42. Oh, I.H., and Reddy, E.P. (1999) The myb gene family in cell growth, differentiation and apoptosis. Oncogene 18: 3017-3033.
43. Ong, S.J., Huang, L.C., Liu, H.W., Chang, S.C., Yang, Y.C., Bessarab, I., and Tai, J.H. (2002) Characterization of a bidirectional promoter for divergent transcription of a PHD-zinc finger protein gene and aran gene in the protozoan pathogen Giardia lamblia. Mol Microbiol 43: 665-676.
44. Otsuka, H., and Van Haastert, P.J. (1998) A novel Myb homolog initiates Dictyostelium development by induction of adenylyl cyclase expression. Genes Dev 12: 1738-1748.
45. Que, X., Svard, S.G., Meng, T.C., Hetsko, M.L., Aley, S.B., and Gillin, F.D. (1996) Developmentally regulated transcripts and evidence of differential mRNA processing in Giardia lamblia. Mol Biochem Parasitol 81: 101-110.
46. Roger, A.J., Svard, S.G., Tovar, J., Clark, C.G., Smith, M.W., Gillin, F.D., and Sogin, M.L. (1998) A mitochondrial-like chaperonin 60 gene in Giardia lamblia: Evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Natl Acad Sci USA 95: 229-234.
47. Sakura, H., Kanei-Ishii, C., Nagase, T., Nakagoshi, H., Gonda, T.J., and Ishii, S. (1989) Delineation of three functional domains of the transcriptional activator encoded by the c-myb protooncogene. Proc Natl Acad Sci USA 86: 5758-5762.
48. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.
49. Singer, S.M., Yee, J., and Nash, T.E. (1998) Episomal and integrated maintenance of foreign DNA in Giardia lamblia. Mol Biochem Parasitol 92: 59-69.
50. Sogin, M.L., Gunderson, J.H., Elwood, H.J., Alonso, R.A., and Peattie, D.A. (1989) Phylogenetic meaning of the kingdom concept: An unusual ribosomal RNA from Giardia lamblia. Science 243: 75-77.
51. Stober-Grasser, U., Brydolf, B., Bin, X., Grasser, F., Firtel, R.A., and Lipsick, J.S. (1992) The Myb DNA-binding domain is highly conserved in Dictyostelium discoideum. Oncogene 7: 589-596.
52. Stracke, R., Werber, M., and Weisshaar, B. (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4: 447-456.
53. Sun, C.H., Chou, C.F., and Tai, J.H. (1998) Stable DNA transfection of the primitive protozoan pathogen Giardia lamblia. Mol Biochem Parasitol 92: 123-132.
54. Sun, C.H., and Tai, J.H. (1999) Identification and characterization of a ran gene promoter in the primitive protozoan pathogen Giardia lamblia. J Biol Chem 274: 19699-19706.
55. Sun, C.H., and Tai, J.H. (2000) Development of a tetracycline controlled gene expression system in the parasitic protozoan Giardia lamblia. Mol Biochem Parasitol 105: 51-60.
56. Svard, S.G., Rafferty, C., McCaffery, J.M., Smith, M.W., Reiner, D.S., and Gillin, F.D. (1999) A signal recognition particle receptor gene from the early-diverging eukaryote, Giardia lamblia. Mol Biochem Parasitol 98: 253-264.
57. Tabata, K., Matsuda, Y., Viller, E., Masamune, Y., Katayama, T., and Yasukawa, H. (2001) Myb-binding site regulates the expression of glucosamine-6-phosphate isomerase in Dictyostelium discoideum. Dev Growth Diff 43: 583-589.
58. Touz, M.C., Nores, M.J., Slavin, I., Carmona, C., Conrad, J.T., Mowatt, M.R., et al. (2002) The activity of a developmentally regulated cysteine proteinase is required for cyst wall formation in the primitive eukaryote Giardia lamblia. J Biol Chem 277: 8474-8481.
59. Tsai, C.D., Liu, H.W., and Tai, J.H. (2002) Characterization of an iron-responsive promoter in the protozoan pathogen Trichomonas vaginalis. J Biol Chem 277: 5153-5162.
60. Van Keulen, H., Steimle, P.A., Bulik, D.A., Borowiak, R.K., and Jarroll, E.L. (1998) Cloning of two putative Giardia lamblia glucosamine 6-phosphate isomerase genes only one of which is transcriptionally activated during encystment. J Eukaryot Microbiol 45: 637-642.
61. Weston, K., and Bishop, J.M. (1989) Transcriptional activation by the v-myb oncogene and its cellular progenitor, c-myb. Cell 58: 85-93.
62. Wieser, J., and Adams, T.H. (1995) flbD encodes a Myb-like DNA-binding protein that coordinates initiation of Aspergillus nidulans conidiophore development. Genes Dev 9: 491-502.
63. Wolfe, M.S. (1992) Giardiasis. Clin Microbiol Rev 5: 93-100.
64. Yee, J., Mowatt, M.R., Dennis, P.P., and Nash, T.E. (2000) Transcriptional analysis of the glutamate dehydrogenase gene in the primitive eukaryote, Giardia lamblia. Identification of a primordial gene promoter. J Biol Chem 275: 11432-11439.