Identification and characterization of a highly conserved calcineurin binding protein, CBP1/calcipressin, in Cryptococcus neoformans

EMBO Journal

Volumn 19, Issue 14, 2000, Pages 3618-3629

  Görlach, Jenifer ^a   Fox, Deborah S ^a   Cutler, N Shane ^a   Cox, Gary M ^a   Perfect, John R ^a   Heitman, Joseph ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Calcineurin; Cryptococcus neoformans; Down's syndrome; Pathogenic fungi; Protein phosphatase

Indexed keywords

BINDING PROTEIN; CALCINEURIN; CYCLOSPORIN A; IMMUNOSUPPRESSIVE AGENT; TACROLIMUS;

AMINO ACID SEQUENCE; ARTICLE; CAENORHABDITIS ELEGANS; CRYPTOCOCCUS NEOFORMANS; DROSOPHILA MELANOGASTER; FUNGUS GROWTH; HYBRID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; VIRULENCE;

CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; FILOBASIDIELLA NEOFORMANS; FUNGI; LEPIDOPTERA; MELANOGASTER; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 0343192437     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.14.3618     Document Type: Article

References (72)

1. Arndt, C., Cruz, M.C., Cardenas, M.E. and Heitman, J. (1999) Secretion of FK506/FK520 and rapamycin by Streptomyces inhibits the growth of competing Saccharomyces cerevisiae and Cryptococcus neoformans. Microbiology, 145, 1989-2000.
2. Bartel, P., Chien, C.T., Sternglanz, R. and Fields, S. (1993) Elimination of false positives that arise in using the two-hybrid system. Biotechniques, 14, 920-924.
3. Breuder, T., Hemenway, C.S., Movva, N.R., Cardenas, M.E. and Heitman, J. (1994) Calcineurin is essential in cyclosporin A-and FK506-sensitive yeast strains. Proc. Natl Acad. Sci. USA, 91, 5372-5376.
4. Cardenas, M.E., Hemenway, C., Muir, R.S., Ye, R., Fiorentino, D. and Heitman, J. (1994) Immunophilins interact with calcineurin in the absence of exogenous immunosuppressive ligands. EMBO J., 13, 5944-5957.
5. Cardenas, M.E., Muir, R.S., Breuder, T. and Heitman, J. (1995) Targets of immunophilin-immunosuppressant complexes are distinct highly conserved regions of calcineurin A. EMBO J., 14, 2772-2783.
6. Cardenas, M.E., Sanfridson, A., Cutler, N.S. and Heitman, J. (1998) Signal-transduction cascades as targets for therapeutic intervention by natural products. Trends Biotechnol., 16, 427-433.
7. Cardenas, M.E., Cruz, M.C., Del Poeta, M., Chung, N., Perfect, J.R. and Heitman, J. (1999) Antifungal activities of antineoplastic agents: Saccharomyces cerevisiae as a model system to study drug action. Clin. Microbiol. Rev., 12, 583-611.
8. Chang, H.Y., Takei, K., Sydor, A.M., Born, T., Rusnak, F. and Jay, D.G. (1995) Asymmetric retraction of growth cone filopodia following focal inactivation of calcineurin. Nature, 376, 686-690.
9. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162, 156-159.
10. Coghlan, V.M., Perrino, B.A., Howard, M., Langeberg, L.K., Hicks, J.B., Gallatin, W.M. and Scott, J.D. (1995) Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science, 267, 108-111.
11. Cruz, M.C., Cavallo, L.M., Görlach, J.M., Cox, G., Perfect, J.R., Cardenas, M.E. and Heitman, J. (1999) Rapamycin antifungal action is mediated via conserved complexes with FKBP12 and TOR kinase homologs in Cryptococcus neoformans. Mol. Cell. Biol., 19, 4101-4112.
12. Cruz, M.C., Sia, R.A.L., Olson, M., Cox, G.M. and Heitman, J. (2000) Comparison of the roles of calcineurin in physiology and virulence in serotype D and serotype A strains of Cryptococcus neoformans. Infect. Immun., 68, 982-985.
13. 2+ ATPases. J. Cell Biol., 124, 351-363.
14. 2+ ATPases in Saccharomyces cerevisiae. Mol. Cell. Biol., 16, 2226-2237.
15. 2+/calmodulin-dependent phosphoprotein phosphatases is required for adaptation to pheromone. Mol. Cell. Biol., 12, 3460-3469.
16. Del Poeta, M., Toffaletti, D.L., Rude, T.H., Sparks, S.D., Heitman, J. and Perfect, J.R. (1999) Cryptococcus neoformans differential gene expression detected in vitro and in vivo with green fluorescent protein. Infect. Immun., 67, 1812-1820.
17. Ferreira, A., Kincaid, R. and Kosik, K.S. (1993) Calcineurin is associated with the cytoskeleton of cultured neurons and has a role in the acquisition of polarity. Mol. Biol. Cell, 4, 1225-1238.
18. Foor, F., Parent, S.A., Morin, N., Dahl, A.M., Ramadan, N., Chrebet, G., Bostian, K.A. and Nielsen, J.B. (1992) Calcineurin mediates inhibition by FK506 and cyclosporin of recovery from α-factor arrest in yeast. Nature, 360, 682-684.
19. Fruman, D.A., Pai, S.-Y., Burakoff, S.J. and Bierer, B.E. (1995) Characterization of a mutant calcineurin Aα gene expressed by EL4 lymphoma cells. Mol. Cell. Biol., 15, 3857-3863.
20. Fuentes, J.J., Pritchard, M.A., Planas, A.M., Bosch, A., Ferrer, I. and Estivill, X. (1995) A new human gene from the Down syndrome critical region encodes a proline-rich protein highly expressed in fetal brain and heart. Hum. Mol. Genet., 4, 1935-1944.
21. Gietz, R.D., Schiestl, R.H., Willems, A. and Woods, R.A. (1995) Studies on the mechanism of high efficiency transformation of intact yeast cells. Yeast, 11, 355-360.
22. Gorovits, R., Propheta, O., Kolot, M., Dombradi, V. and Yarden, O. (1999) A mutation within the catalytic domain of COT1 kinase confers changes in the presence of two COT1 isoforms and in Ser/Thr protein kinase and phosphatase activities in Neurospora crassa. Fungal Genet. Biol., 27, 264-274.
23. Griffith, J.P. et al. (1995) X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12-FK506 complex. Cell. 82, 507-522.
24. Haddy, A., Swanson, S.K.-H., Born, T.L. and Rusnak, F. (1992) Inhibition of calcineurin by cyclosporin A-cyclophilin requires calcineurin B. FEBS Lett., 314, 37-40.
25. 1 cyclin-dependent kinases. Cell, 75, 805-816.
26. Hashimoto, Y., Perrino, B.A. and Soderling, T.R. (1990) Identification of an autoinhibitory domain in calcineurin. J. Biol. Chem., 265, 1924-1927.
27. Heitman, J., Movva, N.R., Hiestand, P.C. and Hall, M.N. (1991) FK506-binding protein proline rotamase is a target for the immunosuppressive agent FK506 in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 88, 1948-1952.
28. Heitman, J., Koller, A., Cardenas, M.E. and Hall, M.N. (1993) Identification of immunosuppressive drug targets in yeast. Methods, 5, 176-187.
29. Hemenway, C.S. and Heitman, J. (1999) Calcineurin: structure, function and inhibition. Cell Biochem. Biophys., 30, 115-151.
30. +-ATPase assembly. Genetics, 141, 833-844.
31. Hua, J., Meyer, J.D. and Lodge, J.K. (2000) Development of positive selectable markers for the fungal pathogen Cryptococcus neoformans. Clin. Diagn. Lab. Immunol., 7, 125-128.
32. Hubbard, M.J. and Klee, C.B. (1989) Functional domain structure of calcineurin A: mapping by limited proteolysis. Biochemistry, 28, 1868-1874.
33. Jackson, S.L. and Heath, I.B. (1993) Roles of calcium ions in hyphal tip growth. Microbiol. Rev., 57, 367-382.
34. James, P., Halladay, J. and Craig, E.A. (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics, 144, 1425-1436.
35. Kashishian, A., Howard, M., Loh, C., Gallatin, W.M., Hoekstra, M.F. and Lai, Y. (1998) AKAP79 inhibits calcineurin through a site distinct from the immunophilin-binding region. J. Biol. Chem., 273, 27412-27419.
36. Kissinger, C.R. et al. (1995) Crystal structures of human calcineurin and the human FKBP12-FK506-calcineurin complex. Nature, 378, 641-644.
37. Klauck, T.M., Faux, M.C., Labudda, K., Langeberg, L.K., Jaken, S. and Scott, J.D. (1996) Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science, 271, 1589-1592.
38. Kothe, G.O. and Free, S.J. (1998) Calcineurin subunit B is required for normal vegetative growth in Neurospora crassa. Fungal Genet. Biol., 23, 248-258.
39. Lai, M.M., Burnett, P.E., Wolosker, H., Blackshaw, S. and Snyder, S.H. (1998) Cain, a novel physiologic protein inhibitor of calcineurin. J. Biol. Chem., 273, 18325-18331.
40. Liu, J., Farmer, J.D., Lane, W.S., Friedman, J., Weissman, I. and Schreiber, S.L. (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell, 66, 807-815.
41. Loh, C., Shaw, K.T.-Y., Carew, J., Viola, J.P.B., Luo, C., Perrino, B.A. and Rao, A. (1996) Calcineurin binds the transcription factor NFAT1 and reversibly regulates its activity. J. Biol. Chem., 271, 10884-10891.
42. Lorenz, M.C. and Heitman, J. (1995) TOR mutations confer rapamycin resistance by preventing interaction with FKBP12-rapamycin. J. Biol. Chem., 270, 27531-27537.
43. Lorenz, M.C., Muir, R.S., Lim, E., McElver, J., Weber, S.C. and Heitman, J. (1995) Gene disruption with PCR products in Saccharomyces cerevisiae. Gene, 158, 113-117.
44. Mansuy, I.M., Mayford, M., Jacob, B., Kandel, E.R. and Bach, M.E. (1998) Restricted and regulated overexpression reveals calcineurin as a key component in the transition from short-term to long-term memory. Cell, 92, 39-49.
45. Matheos, D.P., Kingsbury, T.J., Ahsan, U.S. and Cunningham, K.W. (1997) Tcn1p/Crz1p, a calcineurin-dependent transcription factor that differentially regulates gene expression in Saccharomyces cerevisiae. Genes Dev., 11, 3445-3458.
46. Mazur, P., Morin, N., Baginsky, W., El-Sherbeini, M., Clemas, J.A., Nielsen, J.B. and Foor, F. (1995) Differential expression and function of two homologous subunits of yeast 1,3-β-D-glucan synthase. Mol. Cell. Biol., 15, 5671-5681.
47. Miyazaki, T., Kanou, Y., Murata, U., Ohmori, S., Niwa, T., Maeda, K., Yamamura, H. and Seo, H. (1996) Molecular cloning of a novel thyroid hormone-responsive gene, ZAKI-4, in human skin fibroblasts. J. Biol. Chem., 271, 14567-14571.
48. Molkentin, J.D., Lu, J.R., Antos, C.L., Markham, B., Richardson, J., Robbins, J., Grant, S.R. and Olson, E.N. (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell, 93, 215-228.
49. 2+-calmodulin-dependent protein kinase. Mol. Cell. Biol., 16, 4824-4831.
50. Mulkey, R.M., Endo, S., Shenolikar, S. and Malenka, R.C. (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature, 369, 486-488.
51. Nakamura, T., Liu, Y., Hirata, D., Namba, H., Harada, S.-i., Hirokawa, T. and Miyakawa, T. (1993) Protein phosphatase type 2B (calcineurin)-mediated, FK506-sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions. EMBO J., 12, 4063-4071.
52. Odom, A., Muir, S., Lim, E., Toffaletti, D.L., Perfect, J. and Heitman, J. (1997) Calcineurin is required for virulence of Cryptococcus neoformans. EMBO J., 16, 2576-2589.
53. Perfect, J.R., Toffaletti, D.L. and Rude, T.H. (1993) The gene encoding phosphoribosylaminoimidazole carboxylase (ADE2) is essential for growth of Cryptococcus neoformans in cerebrospinal fluid. Infect. Immun., 61, 4446-4451.
54. Pitkin, J.W., Panaccione, D.G. and Walton, J.D. (1996) A putative cyclic peptide efflux pump encoded by the TOXA gene of the plant-pathogenic fungus Cochliobolus carbonum. Microbiology, 142, 1557-1565.
55. Plochocka-Zulinska, D., Rasmussen, G. and Rasmussen, C. (1995) Regulation of calcineurin gene expression in Schizosaccharomyces pombe. J. Biol. Chem., 270, 24794-24799.
56. 2+ gradient. Mol. Gen. Genet., 256, 104-114.
57. Ranger, A.M., Grusby, M.J., Hodge, M.R., Gravallese, E.M., de la Brousse, F.C., Hoey, T., Mickanin, C., Baldwin, H.S. and Glimcher, L.H. (1998) The transcription factor NF-ATc is essential for cardiac valve formation. Nature, 392, 186-190.
58. Rasmussen, C., Garen, C., Brining, S., Kincaid, R.L., Means, R.L. and Means, A.R. (1994) The calmodulin-dependent protein phosphatase catalytic subunit (calcineurin A) is an essential gene in Aspergillus nidulans. EMBO J., 13, 2545-2552.
59. Rothermel, B., Vega, R.B., Yang, J., Wu, H., Bassel-Duby, R. and Williams, R.S. (2000) A protein encoded within the Down syndrome critical region is enriched in striated muscles and inhibits calcineurin signaling. J. Biol. Chem., 275, 8719-8725.
60. Shaw, K.T.-Y., Ho, A.M., Raghavan, A., Kim, J., Jain, J., Park, J., Sharma, S., Rao, A. and Hogan, P.G. (1995) Immunosuppressive drugs prevent a rapid dephosphorylation of transcription factor NFAT1 in stimulated immune cells. Proc. Natl Acad. Sci. USA, 92, 11205-11209.
61. Sherman, F. (1991) Getting started with yeast. Methods Enzymol., 194, 3-21.
62. Shibasaki, F., Price, E.R., Milan, D. and McKeon, F. (1996) Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature, 382, 370-373.
63. Stathopoulos, A.M. and Cyert, M.S. (1997) Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev., 11, 3432-3444.
64. Stathopoulos-Gerontides, A., Guo, J.J. and Cyert, M.S. (1999) Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation. Genes Dev., 13, 798-803.
65. Sudarshan, S., Davidson, R.C., Heitman, J. and Alspaugh, J.A. (1999) Molecular analysis of the Cryptococcus neoformans ADE2 gene, a selectable marker for transformation and gene disruption. Fungal Genet. Biol., 27, 36-48.
66. Sun, L., Youn, H.-D., Loh, C., Stolow, M., He, W. and Liu, J.O. (1998) Cabin 1, a negative regulator for calcineurin signaling in T lymphocytes. Immunity, 8, 1-20.
67. Sussman, M.A. et al. (1998) Prevention of cardiac hypertrophy in mice by calcineurin inhibition. Science, 281, 1690-1693.
68. Toffaletti, D.L., Rude, T.H., Johnston, S.A., Durack, D.T. and Perfect, J.R. (1993) Gene transfer in Cryptococcus neoformans by use of biolistic delivery of DNA. J. Bacteriol., 175, 1405-1411.
69. Wach, A., Brachat, A., Pohlmann, R. and Philippsen, P. (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast, 10, 1793-1808.
70. Wesselborg, S., Furman, D.A., Sagoo, J.K., Bierer, B.E. and Burakoff, S.J. (1996) Identification of a physical interaction between calcineurin and nuclear factor of activated T cells (NFATp). J. Biol. Chem., 271, 1274-1277.
71. Winder, D.G., Mansuy, I.M., Osman, M., Moallem, T.M. and Kandel, E.R. (1998) Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell, 92, 25-37.
72. + in fission yeast: mutant defects in cytokinesis, cell polarity, mating and spindle pole body positioning. J. Cell Sci., 107, 1725-1735.