Pheromones stimulate mating and differentiation via paracrine and autocrine signaling in Cryptococcus neoformans

Eukaryotic Cell

Volumn 1, Issue 3, 2002, Pages 366-377

  Shen, Wei Chiang ^a,b   Davidson, Robert C ^a   Cox, Gary M ^a   Heitman, Joseph ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

FILOBASIDIELLA NEOFORMANS; FUNGI; MYXOGASTRIA;

FUNGAL DNA; PHEROMONE;

ARTICLE; AUTOCRINE EFFECT; BACTERIUM CONJUGATION; CELL DIFFERENTIATION; CRYPTOCOCCUS NEOFORMANS; DRUG EFFECT; FUNGAL GENE; GENE EXPRESSION; GENETICS; HAPLOIDY; MUTATION; NUCLEOTIDE SEQUENCE; PARACRINE SIGNALING; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

AUTOCRINE COMMUNICATION; BASE SEQUENCE; CELL DIFFERENTIATION; CONJUGATION, GENETIC; CRYPTOCOCCUS NEOFORMANS; DNA, FUNGAL; GENE EXPRESSION; GENES, FUNGAL; GENES, MATING TYPE, FUNGAL; HAPLOIDY; MUTATION; PARACRINE COMMUNICATION; PHEROMONES; VIRULENCE;

EID: 0036615226     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.1.3.366-377.2002     Document Type: Article

References (65)

1. Alspaugh, J. A., L. M. Cavallo, J. R. Perfect, and J. Heitman. 2000. RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans. Mol. Microbiol. 36:352-365.
2. Alspaugh, J. A., R. C. Davidson, and J. Heitman. 2000. Morphogenesis of Cryptococcus neoformans, p. 217-238. In J. F. Ernst and A. Schmidt (ed.), Dimorphism in human pathogenic and apathogenic yeasts, vol. 5. Karger, Basel, Switzerland.
3. 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.
4. Bakkeren, G., and J. W. Kronstad. 1996. The pheromone cell signaling components of the Ustilago a mating-type loci determine intercompatibility between species. Genetics 143:1601-1613.
5. Banuett, F. 1998. Signalling in the yeasts: an informational cascade with links to the filamentous fungi. Microbiol. Mol. Biol. Rev. 62:249-274.
6. Beale, G. 1990. Self and non-self recognition in the ciliate protozoan Euplotes. Trends Genet. 6:137-139.
7. Bölker, M., M. Urban, and R. Kahmann. 1992. The a mating type locus of U. maydis specifies cell signaling components. Cell 68:441-450.
8. Caldwell, G. A., S. H. Wang, C. B. Xue, Y. Jiang, H. F. Lu, F. Naider, and J. M. Becker. 1994. Molecular determinants of bioactivity of the Saccharomyces cerevisiae lipopeptide mating pheromone. J. Biol. Chem. 269:19817-19826.
9. Cardenas, M. E., C. Hemenway, R. S. Muir, R. Ye, D. Fiorentino, and J. Heitman. 1994. Immunophilins interact with calcineurin in the absence of exogenous immunosuppressive ligands. EMBO J. 13:5944-5957.
10. Casadevall, A., and J. R. Perfect. 1998. Cryptococcus neoformans. ASM Press, Washington, D.C.
11. Casselton, L, A., and N. S. Olesnicky. 1998. Molecular genetics of mating recognition in basidiomycete fungi. Microbiol. Mol. Biol. Rev. 62:55-70.
12. Chang, Y. C., and K. J. Kwon-Chung. 1994. Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol. Cell. Biol. 14:4912-4919.
13. Chaturvedi, S., B. Rodeghier, J. Fan, C. M. McClelland, B. L. Wickes, and V. Chaturvedi. 2000. Direct PCR of Cryptococcus neoformans MATα and MATa pheromones to determine mating type, ploidy, and variety: a tool for epidemiological and molecular pathogenesis studies. J. Clin. Microbiol. 38:2007-2009.
14. Chen, P., S. K. Sapperstein, J. D. Choi, and S. Michaelis. 1997. Biogenesis of the Saccharomyces cerevisiae mating pheromone a-factor. J. Cell Biol. 136:251-269.
15. 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.
16. D'Souza, C. A., J. A. Alspaugh, C. Yue, T. Harashima, G. M. Cox, J. R. Perfect, and J. Heitman. 2001. Cyclic AMP-dependent protein kinase controls virulence of the fungal pathogen Cryptococcus neoformans. Mol. Cell. Biol. 21:3179-3191.
17. Davey, J. 1998. Fusion of a fission yeast. Yeast 14:1529-1566.
18. Davidson, R. C., T. D. E. Moore, A. R. Odom, and J. Heitman. 2000. Characterization of the MFα pheromone of the human fungal pathogen Cryptococcus neoformans. Mol. Microbiol. 39:1-12.
19. Del Poeta, M., D. L. Toffaletti, T. H. Rude, S. D. Sparks, J. Heitman, and J. R. Perfect. 1999. Cryptococcus neoformans differential gene expression detected in vitro and in vivo with green fluorescent protein. Infect. Immun. 67:1812-1820.
20. Edman, J. C., and K. J. Kwon-Chung. 1990. Isolation of the URA5 gene from Cryptococcus neoformans var. neoformans and its use as a selective marker for transformation. Mol. Cell. Biol. 10:4538-4544.
21. Erdman, S., and M. Snyder. 2001. A filamentous growth response mediated by the yeast mating pathway. Genetics 159:919-928.
22. Feldmesser, M., Y. Kress, P. Novikoff, and A. Casadevall. 2000. Cryptococcus neoformans is a facultative intracellular pathogen in murine pulmonary infection. Infect. Immun. 68:4225-4237.
23. Fowler, T. J., M. F. Mitton, L. J. Vaillancourt, and C. A. Raper. 2001. Changes in mate recognition through alterations of pheromones and receptors in the multisexual mushroom fungus Schizophyllum commune. Genetics 158:1491-1503.
24. Fowler, T. J., S. M. DeSimone, M. F. Mitton, J. Kurjan, and C. A. Raper. 1999. Multiple sex pheromones and receptors of a mushroom-producing fungus elicit mating in yeast. Mol. Biol. Cell 10:2559-2572.
25. Fox, D. S., M. C. Cruz, R. A. L. 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.
26. Gimeno, C. J., P. O. Ljungdahl, C. A. Styles, and G. R. Fink. 1992. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68:1077-1090.
27. Gola, S., J. Hegner, and E. Kothe. 2000. Chimeric pheromone receptors in the basidiomycete Schizophyllum commune. Fungal Genet. Biol. 30:191-196.
28. Halsall, J. R., M. J. Milner, and L. A. Casselton. 2000. Three subfamilies of pheromone and receptor genes generate multiple B mating specificities in the mushroom Coprinus cinereus. Genetics 154:1115-1123.
29. Hegner, J., C. Siebert-Bartholmei, and E. Kothe. 1999. Ligand recognition in multiallelic pheromone receptors from the basidiomycete Schizophyllum commune studied in yeast. Fungal Genet. Biol. 26:190-197.
30. Heitman, J., B. Allen, J. A. Alspaugh, and K. J. Kwon-Chung. 1999. On the origins of the congenic MATα and MATa strains of pathogenic yeast Cryptococcus neoformans. Fungal Genet. Biol. 28:1-5.
31. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
32. Karos, M., Y. C. Chang, C. M. McClelland, D. L. Clarke, J. Fu, B. L. Wickes, and K. J. Kwon-Chung. 2000. Mapping of the Cryptococcus neoformans MATα locus: presence of mating type-specific mitogen-activated protein kinase cascade homologs. J. Bacteriol. 182:6222-6227.
33. Kothe, E. 1999. Mating types and pheromone recognition in the homobasidiomycete Schizophyllum commune. Fungal Genet. Biol. 27:146-152.
34. Kothe, E. 1996. Tetrapolar fungal mating types: sexes by the thousands. FEMS Microbiol. Rev. 18:65-87.
35. Kronstad, J. W., and C. Staben. 1997. Mating type in filamentous fungi. Annu. Rev. Genet. 31:245-276.
36. Kues, U. 2000. Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol. Mol. Biol. Rev. 64:316-353.
37. Kwon-Chung, K. J. 1976. Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 68:821-833.
38. Kwon-Chung, K. J., and J. E. Bennett. 1978. Distribution of α and a mating types of Cryptococcus neoformans among natural and clinical isolates. Am. J. Epidemiol. 108:337-340.
39. Kwon-Chung, K. J., J. C. Edman, and B. L. Wickes. 1992. Genetic association of mating types and virulence in Cryptococcus neoformans. Infect. Immun. 60:602-605.
40. Kwon-Chung, K. J., I. Polacheck, and T. J. Popkin. 1982. Melanin-lacking mutants of Cryptococcus neoformans and their virulence for mice. J. Bacteriol. 150:1414-1421.
41. Kwon-Chung, K. J., and J. C. Rhodes. 1986. Encapsulation and melanin formation as indicators of virulence in Cryptococcus neoformans. Infect. Immun. 51:218-223.
42. Liu, H., C. A. Styles, and G. R. Fink. 1993. Elements of the yeast pheromone response pathway required for filamentous growth of diploids. Science 262:1741-1744.
43. McLatchie, L. M., N. J. Fraser, M. J. Main, A. Wise, J. Brown, N. Thompson, R. Solari, M. G. Lee, and S. M. Foord. 1998. RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor Nature 393:333-339.
44. Michaelis, S., and I. Herskowitz. 1988. The a-factor pheromone of Saccharomyces cerevisiae is essential for mating. Mol. Cell. Biol. 8:1309-1318.
45. 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.
46. Olesnicky, N. S., A. J. Brown, S. J. Duwell, and L. A. Casselton. 1999. A constitutively active G-protein-coupled receptor causes mating self-compatibility in the mushroom Coprinus. EMBO J. 18:2756-2763.
47. Olesnicky, N. S., A. J. Brown, Y. Honda, S. L. Dyos, S. J. Dowell, and L. A. Casselton. 2000. Self-compatible B mutants in coprinus with altered pheromone-receptor specificities. Genetics 156:1025-1033.
48. O'Shea, S. F., P. T. Chaure, J. R. Halsall, N. S. Olesnicky, A. Leibbrandt, I. F. Connerton, and L. A. Casselton. 1998. A large pheromone and receptor gene complex determines multiple B mating type specificities in Coprinus cinereus. Genetics 148:1081-1090.
49. Ortenzi, C., C. Alimenti, A. Vallesi, B. D. Pretoro, A. L. Terza, and P. Luporini. 2000. The autocrine mitogenic loop of the ciliate Euplotes raikovi: the pheromone membrane-bound forms are the cell binding sites and potential signaling receptors of soluble pheromones. Mol. Biol. Cell 11:1445-1455.
50. Rhodes, J. C. 1985. Contribution of complement component C5 to the pathogenesis of experimental murine cryptococcosis. Sabouraudia 23:225-234.
51. Rhodes, J. C., and D. H. Howard. 1980. Isolation and characterization of arginine auxotrophs of Cryptococcus neoformans. Infect. Immun. 27:910-914.
52. Rhodes, J. C., L. S. Wicker, and W. J. Urba. 1980. Genetic control of susceptibility to Cryptococcus neoformans in mice. Infect. Immun. 29:494-499.
53. Roberts, C. J., B. Nelson, M. J. Marton, R. Stoughton, M. R. Meyer, H. A. Bennett, Y. D. He, H. Dai, W. L. Walker, T. R. Hughes, M. Tyers, C. Boone, and S. H. Friend. 2000. Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles. Science 287:873-880.
54. Salas, S. D., J. E. Bennett, K. J. Kwon-Chung, J. R. Perfect, and P. R. Williamson. 1996. Effect of the laccase gene, CNLAC1, on virulence of Cryptococcus neoformans. J. Exp. Med. 184:377-386.
55. Sanfelice, F. 1894. Contributo alla morfologia e biologia dei blastomiceti che si svilup/pano nei succhi di alcuni frutti. Ann. Igien. 4:463-495.
56. Spellig, T., M. Bolker, F. Lottspeich, R. W. Frank, and R. Kahmann. 1994. Pheromones trigger filamentous growth in Ustilago maydis. EMBO J. 13:1620-1627.
57. Sprague, G. F., Jr., and J. W. Thorner. 1992. Pheromone response and signal transduction during the mating process of Saccharomyces cerevisiae, p. 657-744. In E. W. Jones, J. R. Pringle, and J. R. Broach (ed.), The molecular and cellular biology of the yeast Saccharomyces: gene expression, vol. 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
58. Toffaletti, D. L., and J. R. Perfect. 1994. Biolistic DNA delivery for Cryptococcus neoformans transformation, p. 303-308. In B. Maresca, and G. S. Kobayashi (ed.), Molecular biology of pathogenic fungi: a laboratory manual. Telos Press, New York, N.Y.
59. Vaillancourt, L. J., and C. A. Raper. 1996. Pheromones and pheromone receptors as mating-type determinants in basidiomycetes. Genet. Eng. 18:219-247.
60. Vaillancourt, L. J., M. Raudaskoski, C. A. Specht, and C. A. Raper. 1997. Multiple genes encoding pheromones and a pheromone receptor define the Bβ1 mating-type specificity in Schizophyllum commune. Genetics 146:541-551.
61. Vallesi, A., G. Giuli, R. A. Bradshaw, and P. Luporini. 1995. Autocrine mitogenic activity of pheromones produced by the protozoan ciliate Euplotes raikovi. Nature 376:522-524.
62. Wang, P., J. R. Perfect, and J. Heitman. 2000. The G-protein β subunit GPB1 is required for mating and haploid fruiting in Cryptococcus neoformans. Mol. Cell. Biol. 20:352-362.
63. Wendland, J., L. J. Vaillancourt, J. Hegner, K. B. Lengeler, K. J. Laddison, C. A. Raper, and E. Kothe. 1995. The mating-type locus Bα1 of Schizophyllum commune contains a pheromone receptor gene and putative pheromone genes. EMBO J. 14:5271-5278.
64. Wickes, B. L., M. E. Mayorga, U. Edman, and J. C. Edman. 1996. Dimorphism and haploid fruiting in Cryptococcus neoformans: association with the α-mating type Proc. Natl. Acad. Sci. USA 93:7327-7331.
65. Yamamoto, M., Y. Imai, and Y. Watanabe. 1997. Mating and sporulation in Schizosaccharomyces pombe, p. 1037-1106. In J. R. Pringle, J. R. Broach, and E. W. Jones (ed.), The molecular and cellular biology of the yeast Saccharomyces, vol. 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.