Cryptococcus neoformans gene involved in mammalian pathogenesis identified by a Caenorhabditis elegans progeny-based approach

Infection and Immunity

Volumn 73, Issue 12, 2005, Pages 8219-8225

  Tang, Robin J ^a   Breger, Julia ^a   Idnurm, Alexander ^b   Gerik, Kimberly J ^c   Lodge, Jennifer K ^c   Heitman, Joseph ^b   Calderwood, Stephen B ^a,d   Mylonakis, Eleftherios ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL WALL; CONTROLLED STUDY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; DISEASE MODEL; FUNGAL STRAIN; FUNGAL VIRULENCE; GENE; GENE IDENTIFICATION; GENE LOCUS; GENE MUTATION; GENETIC SCREENING; GROWTH; HIGH TEMPERATURE; HYPEROSMOLARITY; MATING; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROGENY; ROM2 GENE; STRESS; TEMPERATURE DEPENDENCE;

ANIMALS; CAENORHABDITIS ELEGANS; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FEMALE; GENES, FUNGAL; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MICE; MICE, INBRED STRAINS; MUTATION; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, NUCLEIC ACID; VIRULENCE;

EID: 28444488924     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.12.8219-8225.2005     Document Type: Article

References (41)

1. Aballay, A., and F. M. Ausubel. 2002. Caenorhabditis elegans as a host for the study of host-pathogen interactions. Curr. Opin. Microbiol. 5:97-101.
2. 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.
3. Angeles de la Torre-Ruiz, M., J. Torres, J. Arino, and E. Herrero. 2002. Sit4 is required for proper modulation of the biological functions mediated by Pkc1 and the cell integrity pathway in Saccharomyces cerevisiae. J. Biol. Chem. 277:33468-33476.
4. Apidianakis, Y., L. G. Rahme, J. Heitman, F. M. Ausubel, S. B. Calderwood, and E. Mylonakis. 2004. Challenge of Drosophila melanogaster with Cryptococcus neoformans and role of the innate immune response. Eukaryot. Cell 3:413-419.
5. Bickle, M., P. A. Delley, A. Schmidt, and M. N. Hall. 1998. Cell wall integrity modulates RHO1 activity via the exchange factor ROM2. EMBO J. 17:2235-2245.
6. Chai, B., J. M. Hsu, J. Du, and B. C. Laurent. 2002. Yeast RSC function is required for organization of the cellular cytoskeleton via an alternative PKC1 pathway. Genetics 161:575-584.
7. Couillault, C., N. Pujol, J. Reboul, L. Sabatier, J.-F. Guichou, Y. Kohara, and J. J. Ewbank. 2004. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat. Immunol. 5:488-494.
8. 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.
9. Edman, J. C., and K. J. Kwon-Chung. 1990. Isolation of the URAS gene from Cryptococcus neoformans var. neoformans and its use as a selective marker for transformation. Mol. Cell. Biol. 10:4538-4544.
10. Garsin, D. A., C. D. Sifri, E. Mylonakis, X. Qin, K. V. Singh, B. E. Murray, S. B. Calderwood, and F. M. Ausubel. 2001. A simple model host for identifying Gram-positive virulence factors. Proc. Natl. Acad. Sci. USA. 98: 10892-10897.
11. Gustin, M. C., J. Albertyn, M. Alexander, and K. Davenport. 1998. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62:1264-1300.
12. Heinisch, J. J., A. Lorberg, H. P. Schmitz, and J. J. Jacoby. 1999. The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae. Mol. Microbiol. 32:671-680.
13. Klis, F. M., P. Mol, K. Hellingwerf, and S. Brul. 2002. Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 26:239-256.
14. 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.
15. Kurz, C. L., S. Chauvet, E, Andres, M. Aurouze, I. Vallet, G. P. Michel, M. Uh, J. Celli, A. Filloux, S. De Bentzmann, I. Steinmetz, J. A. Hoffmann, B. B. Finlay, J. P. Gorvel, D. Ferrandon, and J. J. Ewbank. 2003. Virulence factors of the human opportunistic pathogen Serratia marcescens identified by in vivo screening. EMBO J. 22:1451-1460.
16. Lee, K. S., and D. E. Levin. 1992. Dominant mutations in a gene encoding a putative protein kinase (BCK1) bypass the requirement for a Saccharomyces cerevisiae protein kinase C homolog. Mol. Cell. Biol. 12:172-182.
17. Levin, D. E. 2005. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69:262-291.
18. Levin, D. E., F. O. Fields, Kunísawa, J. M. Bishop, and J. Thorner. 1990. A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle. Cell 62:213-224.
19. Loftus, B. J., E. Fung, P. Roncaglia, D. Rowley, P. Amedeo, D. Bruno, J. Vamathevan, M. Miranda, I. J. Anderson, J. A. Fraser, J. E. Allen, I. E. Bosdet, M. R. Brent, R. Chiu, T. L. Doering, M. J. Donlin, C. A. D'Souza, D. S. Fox, V. Grinberg, J. Fu, M. Fukushima, B. J. Haas, J. C. Huang, G. Janbon, S. J. Jones, H. L. Koo, M. I. Krzywinski, J. K. Kwon-Chung, K. B. Lengeler, R. Maiti, M. A. Marra, R. E. Marra, C. A. Mathewson, T. G. Mitchell, M. Pertea, F. R. Riggs, S. L. Satzberg, J. E. Schein, A. Shvartsbeyn, H. Shin, M. Shumway, C. A. Specht, B. B. Suh, A. Tenney, T. R. Utterback, B. L. Wickes, J. R. Wortman, N. H. Wye, J. W. Kronstad, J. K. Lodge, J. Heitman, R. W. Davis, C. M. Fraser, and R. W. Hyman. 2005. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307:1321-1324.
20. Lorberg, A., H. P. Schmitz, U. Gengenbacher, and J. J. Heinisch. 2003. KIROM2 encodes an essential GEF homologue in Kluyveromyces lactis. Yeast 20:611-624.
21. Mahajan-Miklos, S., M. W. Tan, L. G. Rahme, and F. M. Ausubel. 1999. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96:47-56.
22. Moy, T., E. Mylonakis, S. B. Calderwood, and F. M. Ausubel. 2004. Cytotoxicity from hydrogen peroxide produced by Enterococcus faecium. Infect. Immun. 72:4512-4520.
23. Mylonakis, E., and A. Aballay. 2005. Worms and flies as genetically tractable animal models to study host-pathogen interactions. Infect. Immun. 73:3833-3841.
24. Mylonakis, E., A. Idnurm, R. Moreno, J. El Khoury, J. B. Rottman, F. M. Ausubel, J. Heitman, and S. B. Calderwood. 2004. Cryptococcus neoformans Kin1 protein kinase homologue, identified through a Caenorhabditis elegans screen, promotes virulence in mammals. Mol. Microbiol. 54:407-419.
25. Mylonakis, E., F. M. Ausubel, J. R. Perfect, J. Heitman, and S. B. Calderwood. 2002. Killing of Caenorhabditis elegans by Cryptococcus neoformans as a model of yeast pathogenesis. Proc. Natl. Acad. Sci. USA 99:15675-15680.
26. Mylonakis, E., R. Moreno, J. El Khoury, A. Idnurm, J. Heitman, S. B. Calderwood, F. M. Ausubel, and A. Diener. 2005. Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect. Immun. 73:3842-3850.
27. 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.
28. Nelson, R. T., J. Hua, B. Pryor, and J. K. Lodge. 2001. Identification of virulence mutants of the fungal pathogen Cryptococcus neoformans using signature-tagged mutagenesis. Genetics 157:935-947.
29. Nielsen, K., G. M. Cox, A. P. Litvintseva, E. Mylonakis, S. D. Malliaris, D. K. Benjamin, Jr., S. S. Giles, T. G. Mitchell, A. Casadevall, J. R. Perfect, and J. Heitman. 2005. Cryptococcus neoformans a strains preferentially disseminate to the central nervous system during infection. Infect. Immun. 73:4922-4933.
30. Nielsen, K., G. M. Cox, P. Wang, D. L. Toffaletti, J. R. Perfect, and J. Heitman. 2003. Sexual cycle of Cryptococcus neoformans var. grubii and virulence of congenic a and α isolates. Infect. Immun. 71:4831-4841.
31. Ozaki, K., K. Tanaka, H. Imamura, T. Hihara, T. Kameyama, H. Nonaka, H. Hirano, Y. Matsuura, and Y. Takai. 1996. Rom1p and Rom2p are GDP/ GTP exchange proteins (GEPs) for the Rho1p small GTP binding protein in Saccharomyces cerevisiae. EMBO J. 15:2196-2207.
32. Park, J. L., E. J. Collinson, C. M. Grant, and I. W. Dawes. 2005. Rom2p, the Rho1 GTP/GDP exchange factor of Saccharomyces cerevisiae, can mediate stress responses via the Ras-cAMP pathway. J. Biol. Chem. 280:2529-2535.
33. Perfect, J. R., S. D. R. Lang, and D. T. Durack. 1980. Chronic cryptococcal meningitis: a new experimental model in rabbits. Am. J. Pathol. 101:177-194.
34. Perfect, J. R., and A. Casadevall. 2002. Cryptococcosis. Infect. Dis. Clin. N Am. 16:837-874.
35. Pradel, E., and J. J. Ewbank. 2004. Genetic models in pathogenesis. Annu. Rev. Genet. 38:347-363.
36. 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.
37. Steenbergen, J. N., H. A. Shuman, and A. Casadevall. 2001. Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc. Natl. Acad. Sci. USA 98:15245-15250.
38. Tan, M. W., S. Mahajan-Miklos, and F. M. Ausubel. 1999. Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc. Natl. Acad. Sci. USA 96:715-720.
39. Thompson, J. R., C. M. Douglas, W. Li, C. K. Jue, B. Pramanik, X. Yuan, T. H. Rude, D. L. Toffalettl, J. R. Perfect, and M. Kurtz. 1999. A glucan synthase FKS1 homolog in Cryptococcus neoformans is single copy and encodes an essential function. J. Bacteriol. 181:444-453.
40. Wang, P., M. E. Cardenas, G. M. Cox, J. R. Perfect, and J. Heitman. 2001. Two cyclophilin A homologs with shared and distinct functions important for growth and virulence of Cryptococcus neoformans. EMBO Rep. 2:511-518.
41. Wojda, I., R. Alonso-Monge, J. P. Bebelman, W. H. Mager, and M. Siderius. 2003. Response to high osmotic conditions and elevated temperature in Saccharomyces cerevisiae is controlled by intracellular glycerol and involves coordinate activity of MAP kinase pathways. Microbiology 149:1193-1204.