Calcium- and calcineurin-independent roles for calmodulin in Cryptococcus neoformans morphogenesis and high-temperature growth

Eukaryotic Cell

Volumn 4, Issue 6, 2005, Pages 1079-1087

  Kraus, Peter R ^a   Nichols, Connie B ^a   Heitman, Joseph ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCIUM; CALMODULIN; MESSENGER RNA; TACROLIMUS;

ARTICLE; BIOLOGICAL MODEL; CROSS BREEDING; CRYPTOCOCCUS NEOFORMANS; CYTOLOGY; FUNGAL GENE; GENE EXPRESSION REGULATION; GENETIC MARKER; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; METABOLISM; MUTATION;

CALCINEURIN; CALCIUM; CALMODULIN; CROSSES, GENETIC; CRYPTOCOCCUS NEOFORMANS; GENES, FUNGAL; GENETIC MARKERS; HEAT; MODELS, BIOLOGICAL; MUTAGENESIS, INSERTIONAL; MUTATION; RNA, MESSENGER; TACROLIMUS;

EUKARYOTA; FILOBASIDIELLA NEOFORMANS; FUNGI; MAMMALIA;

EID: 20444462002     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.4.6.1079-1087.2005     Document Type: Article

References (45)

1. Adamikova, L., A. Straube, I. Schulz, and G. Steinberg. 2004. Calcium signaling is involved in dynein-dependent microtubule organization. Mol. Biol. Cell 15:1969-1980.
2. Alspaugh, J. A., J. R. Perfect, and J. Heitman. 1997. Cryptococcus neoformans mating and virulence are regulated by the G-protein α subunit GPA1 and cAMP. Genes Dev. 11:3206-3217.
3. Aramburu, J., A. Rao, and C. B. Klee. 2000. Calcineurin: from structure to function. Curr. Top. Cell Regul. 36:237-295.
4. Babu, Y. S., C. E. Bugg, and W. J. Cook. 1988. Structure of calmodulin refined at 2.2 Å resolution. J. Mol. Biol. 204:191-204.
5. Berridge, M. J., M. D. Bootman, and H. L. Roderick. 2003. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4:517-529.
6. Blankenship, J. R., F. L. Wormley, M. K. Boyce, W. A. Schell, S. G. Filler, J. R. Perfect, and J. Heitman. 2003. Calcineurin is essential for Candida albicans survival in serum and virulence. Eukaryot. Cell 2:422-430.
7. Brockerhoff, S. E., R. C. Stevens, and T. N. Davis. 1994. The unconventional myosin, Myo2p, is a calmodulin target at sites of cell growth in Saccharomyces cerevisiae. J. Cell Biol. 124:315-323.
8. Chin, D., and A. R. Means. 2000. Calmodulin: a prototypical calcium sensor. Trends Cell Biol. 10:322-328.
9. Cruz, M. C., D. S. Fox, and J. Heitman. 2001. Calcineurin is required for hyphal elongation during mating and haploid fruiting in Cryptococcus neoformans. EMBO J. 20:1020-1032.
10. Cruz, M. C., R. A. L. Sia, M. Olson, G. M. Cox, and J. Heitman. 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.
11. Cyert, M. S. 2001. Genetic analysis of calmodulin and its targets in Saccharomyces cerevisiae. Annu. Rev. Genet. 35:647-672.
12. Davidson, R. C., J. R. Blankenship, P. R. Kraus, M. de Jesus Berrios, C. M. Hull, C. D'Souza, P. Wang, and J. Heitman. 2002. A PCR-based strategy to generate integrative targeting alleles with large regions of homology. Microbiology 148:2607-2615.
13. Davis, T. N., M. S. Urdea, F. R. Masiarz, and J. Thorner. 1986. Isolation of the yeast calmodulin gene: calmodulin is an essential protein. Cell 47:423-431.
14. Desrivieres, S., F. T. Cooke, H. Morales-Johansson, P. J. Parker, and M. N. Hall. 2002. Calmodulin controls organization of the actin cytoskeleton via regulation of phosphatidylinositol (4,5)-bisphosphate synthesis in Saccharomyces cerevisiae. Biochem. J. 366:945-951.
15. Facanha, A. L., H. Appelgren, M. Tabish, L. Okorokov, and K. Ekwall. 2002. The endoplasmic reticulum cation P-type ATPase Cta4p is required for control of cell shape and microtubule dynamics. J. Cell Biol. 157:1029-1039.
16. Fox, D. S., M. C. Cruz, R. A. Sia, H. Ke, G. M. Cox, M. E. Cardenas, and J. Heitman. 2001. Calcineurin regulatory subunit is essential for virulence and mediates interactions with FKBP12-FK506 in Cryptococcus neoformans. Mol. Microbiol. 39:835-849.
17. Fox, D. S., and J. Heitman. 2002. Good fungi gone bad: the corruption of calcineurin. Bioessays 24:894-903.
18. Fraser, J. A., S. Diezmann, R. Subaran, A. Allen, K. B. Lengeler, F. S. Dietrich, and J. Heitman. 2004. Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol. 2:e384.
19. Fraser, J. A., R. L. Subaran, C. B. Nichols, and J. Heitman. 2003. Recapitulation of the sexual cycle of the primary fungal pathogen Cryptococcus neoformans var. gattii: Implications for an outbreak on Vancouver Island, Canada. Eukaryot. Cell 2:1036-1045.
20. Fujita, M., R. Sugiura, Y. Lu, L. Xu, Y. Xia, H. Shuntoh, and T. Kuno. 2002. Genetic interaction between calcineurin and type 2 myosin and their involvement in the regulation of cytokinesis and chloride ion homeostasis in fission yeast. Genetics 161:971-981.
21. Geiser, J. R., D. van Tuinen, S. E. Brockerhoff, M. M. Neff, and T. N. Davis. 1991. Can calmodulin function without binding calcium? Cell 65:949-959.
22. Gow, N. A., G. D. Robson, and G. M. Gadd. 1999. The fungal colony. Cambridge University Press, Cambridge, United Kingdom.
23. Heiman, R. G., R. C. Atkinson, B. F. Andruss, C. Bolduc, G. E. Kovalick, and K. Beckingham. 1996. Spontaneous avoidance behavior in Drosophila null for calmodulin expression. Proc. Natl. Acad. Sci. USA 93:2420-2425.
24. Hemenway, C. S., and J. Heitman. 1999. Calcineurin: structure, function, and inhibition. Cell Biochem. Biophys. 30:115-151.
25. Hill, K. L., N. L. Catlett, and L. S. Weisman. 1996. Actin and myosin function in directed vacuole movement during cell division in Saccharomyces cerevisiae. J. Cell Biol. 135:1535-1549.
26. Hubbard, M. J., and C. B. Klee. 1989. Functional domain structure of calcineurin A: mapping by limited proteolysis. Biochemistry 28:1868-1874.
27. Idnurm, A., J. L. Reedy, J. C. Nussbaum, and J. Heitman. 2004. Cryptococcus neoformans virulence gene discovery through insertional mutagenesis. Eukaryot. Cell 3:420-429.
28. Ikura, M. 1996. Calcium binding and conformational response in EF-hand proteins. Trends Biochem. Sci. 21:14-17.
29. Johnston, G. C., J. A. Prendergast, and R. A. Singer. 1991. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 113:539-551.
30. Joseph, J. D., and A. R. Means. 2002. Calcium binding is required for calmodulin function in Aspergillus nidulans. Eukaryot. Cell 1:119-125.
31. Kraus, P. R., D. S. Fox, G. M. Cox, and J. Heitman. 2003. The Cryptococcus neoformans MAP kinase Mpk1 regulates cell integrity in response to antifungal drugs and loss of calcineurin function. Mol. Microbiol. 48:1377-1387.
32. Kraus, P. R., and J. Heitman. 2003. Coping with stress: calmodulin and calcineurin in model and pathogenic fungi. Biochem. Biophys. Res. Commun. 311:1151-1157.
33. 45Ca autoradiography on nitrocellulose membrane after sodium dodecyl sulfate gel electrophoresis. J. Biochem. (Tokyo) 95:511-519.
34. McDade, H. C., and G. M. Cox. 2001. A new dominant selectable marker for use in Cryptococcus neoformans. Med. Mycol. 39:151-154.
35. Mondon, P., Y. C. Chang, A. Varma, and K. J. Kwon-Chung. 2000. A novel episomal shuttle vector for transformation of Cryptococcus neoformans with the ccdB gene as a positive selection marker in bacteria. FEMS Microbiol. Lett. 187:41-45.
36. Moore, T. D. E., and J. C. Edman. 1993. The α-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene. Mol. Cell. Biol. 13:1962-1970.
37. Nelson, R. T., B. A. Pryor, and J. K. Lodge. 2003. Sequence length required for homologous recombination in Cryptococcus neoformans. Fungal Genet. Biol. 38:1-9.
38. Odom, A., S. Muir, E. Lim, D. L. Toffaletti, J. Perfect, and J. Heitman. 1997. Calcineurin is required for virulence of Cryptococcus neoformans. EMBO J. 16:2576-2589.
39. Ohya, Y., and D. Botstein. 1994. Diverse essential functions revealed by complementing yeast calmodulin mutants. Science 263:963-966.
40. Riley, J., R. Butler, D. Ogilvie, R. Finniear, D. Jenner, S. Powell, R. Anand, J. C. Smith, and A. F. Markham. 1990. A novel, rapid method for the isolation of terminal sequences from yeast artificial chromosome (YAC) clones. Nucleic Acids Res. 18:2887-2890.
41. Sia, R. A., K. B. Lengeler, and J. Heitman. 2000. Diploid strains of the pathogenic basidiomycete Cryptococcus neoformans are thermally dimorphic. Fungal Genet. Biol. 29:153-163.
42. Takeda, T., and M. Yamamoto. 1987. Analysis and in vivo disruption of the gene coding for calmodulin in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 84:3580-3584.
43. Watanabe, Y., B. A. Perrino, and T. R. Soderling. 1996. Activation of calcineurin A subunit phosphatase activity by its calcium-binding B subunit. Biochemistry 35:562-566.
44. Xiang, B., P. Liu, G. Jiang, K. Zou, F. Yi, S. Yang, and Q. Wei. 2003. The catalytically active domain in the A subunit of calcineurin. Biol. Chem. 384:1429-1434.
45. Zelter, A., M. Bencina, B. J. Bowman, O. Yarden, and N. D. Read. 2004. A comparative genomic analysis of the calcium signaling machinery in Neurospora crassa, Magnaporthe grisea, and Saccharomyces cerevisiae. Fungal Genet. Biol. 41:827-841.