Two Rac paralogs regulate polarized growth in the human fungal pathogen Cryptococcus neoformans

Fungal Genetics and Biology

Volumn 57, Issue , 2013, Pages 58-75

  Ballou, Elizabeth Ripley ^a   Selvig, Kyla ^a   Narloch, Jessica L ^a   Nichols, Connie B ^a   Alspaugh, J Andrew ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cryptococcus neoformans; Hyphal growth; Paralogs; Polarization; Rac GTPase; ROS

Indexed keywords

ACTIN; PROTEIN CDC42; RAC1 PROTEIN; RAC2 PROTEIN; REACTIVE OXYGEN METABOLITE; SEX PHEROMONE;

ALLELE; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CDC42 GENE; CELL CYCLE REGULATION; CELL SIZE; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; FEMALE; FUNGAL CELL; FUNGAL DEVELOPMENT; FUNGAL GENOME; FUNGAL STRUCTURES; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; GENE; GENE DUPLICATION; GENE FUSION; GENE LOCATION; GENOME ANALYSIS; GROWTH REGULATION; HEAT TOLERANCE; MORPHOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PARALOGY; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAS1 GENE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

CRYPTOCOCCUS NEOFORMANS VAR. GRUBII; FILOBASIDIELLA NEOFORMANS;

EID: 84881108020     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2013.05.006     Document Type: Article

References (101)

1. Abo A., et al. Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature 1991, 353:668-670.
2. Adams A.E., et al. Cdc42 and Cdc43, two additional genes involved in budding and establishment of cell polarity in the yeast Saccharomyces cerevisiae. Journal of Cell Biology 1990, 111:131-142.
3. Adams J., et al. Adaptation and major chromosomal changes in populations of Saccharomyces cerevisiae. Current Genetics 1992, 22:13-19.
4. Alspaugh J.A., et al. RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans. Molecular Microbiology 2000, 36:352-365.
5. Altschul S.F., et al. Basic local alignment search tool. Journal of Molecular Biology 1990, 215:403-410.
6. Araujo-Palomares C.L., et al. Functional characterization and cellular dynamics of the CDC-42 - RAC - CDC-24 module in Neurospora crassa. PLoS ONE 2011, 6:e27148.
7. Ballou E.R., et al. Two CDC42 paralogues modulate Cryptococcus neoformans thermotolerance and morphogenesis under host physiological conditions. Molecular Microbiology 2010, 75:763-780.
8. Bass D.A., et al. Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. Journal of Immunology (Baltimore, Md: 1950) 1983, 130:1910-1917.
9. Bassilana M., Arkowitz R.A. Rac1 and Cdc42 have different roles in Candida albicans development. Eukaryotic Cell 2006, 5:321-329.
10. Boureux A., et al. Evolution of the Rho family of ras-like GTPases in eukaryotes. Molecular Biology and Evolution 2007, 24:203-216.
11. Boyce K.J., et al. The CDC42 homolog of the dimorphic fungus Penicillium marneffei is required for correct cell polarization during growth but not development. Journal of Bacteriology 2001, 183:3447-3457.
12. Boyce K.J., et al. Control of morphogenesis and actin localization by the Penicillium marneffei RAC homolog. Journal of Cell Science 2003, 116:1249-1260.
13. Boyce K.J., et al. The Ras and Rho GTPases genetically interact to co-ordinately regulate cell polarity during development in Penicillium marneffei. Molecular Microbiology 2005, 55:1487-1501.
14. Carbó N., Pérez-Martín J. Spa2 is required for morphogenesis but it is dispensable for pathogenicity in the phytopathogenic fungus Ustilago maydis. Fungal Genetics and Biology: FG & B 2008, 45:1315-1327.
15. Chang Y.C., et al. Cryptococcal yeast cells invade the central nervous system via transcellular penetration of the blood-brain barrier. Infection and Immunity 2004, 72:4985-4995.
16. Chen C., Dickman M.B. Dominant active Rac and dominant negative Rac revert the dominant active Ras phenotype in Colletotrichum trifolii by distinct signalling pathways. Molecular Microbiology 2004, 51:1493-1507.
17. Chen W., et al. The CDC42 homologue from Caenorhabditis elegans. Complementation of yeast mutation. The Journal of Biological Chemistry 1993, 268:13280-13285.
18. Christiaens J.F., et al. Functional divergence of gene duplicates through ectopic recombination. EMBO Reports 2012, 13:1145-1151.
19. Cline M., et al. Integration of biological networks and gene expression data using Cytoscape. Nature Protocols 2007, 2:2366-2382.
20. Cox G.M., et al. Urease as a virulence factor in experimental cryptococcosis. Infection and Immunity 2000, 68:443-448.
21. Cramer K.L., et al. Transcription factor Nrg1 mediates capsule formation, stress response, and pathogenesis in Cryptococcus neoformans. Eukaryotic Cell 2006, 5:1147-1156.
22. de Bruin D., et al. The polymorphic subtelomeric regions of Plasmodium falciparum chromosomes contain arrays of repetitive sequence elements. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:619-623.
23. Didsbury J., et al. Rac, a novel ras-related family of proteins that are botulinum toxin substrates. The Journal of Biological Chemistry 1989, 264:16378-16382.
24. Diebold B.A., Bokoch G.M. Molecular basis for Rac2 regulation of phagocyte NADPH oxidase. Nature Immunology 2001, 2:211-215.
25. Edgar R.C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5.
26. Force A., et al. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999, 151:1531-1545.
27. Frieser S.H., et al. Cla4 kinase triggers destruction of the Rac1-GEF Cdc24 during polarized growth in Ustilago maydis. Molecular Biology of the Cell 2011, 22:3253-3262.
28. Fu C., et al. Identification and characterization of genes required for cell-to-cell fusion in Neurospora crassa. Eukaryotic Cell 2011, 10:1100-1109.
29. Gao Y., et al. Trp(56) of rac1 specifies interaction with a subset of guanine nucleotide exchange factors. The Journal of Biological Chemistry 2001, 276:47530-47541.
30. Gibbon B.C., et al. Latrunculin B has different effects on pollen germination and tube growth. The Plant Cell 1999, 11:2349-2363.
31. Giesbert S., et al. The NADPH oxidase Cpnox1 is required for full pathogenicity of the ergot fungus Claviceps purpurea. Molecular Plant Pathology 2008, 9:317-327.
32. Hahn M.W. Distinguishing among evolutionary models for the maintenance of gene duplicates. The Journal of Heredity 2009, 100:605-617.
33. Hamanaka R.B., et al. Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development. Science Signaling 2013, 6:ra8.
34. Harris S.D. Cdc42/Rho GTPases in fungi: variations on a common theme. Molecular Microbiology 2011, 79:1123-1127.
35. Hickman M.A., et al. The "obligate diploid" Candida albicans forms mating-competent haploids. Nature 2013, 494:55-59.
36. Ho J., Bretscher A. Ras regulates the polarity of the yeast actin cytoskeleton through the stress response pathway. Molecular Biology of the Cell 2001, 12:1541-1555.
37. Hope H., et al. Activation of Rac1 by the guanine nucleotide exchange factor Dck1 is required for invasive filamentous growth in the pathogen Candida albicans. Molecular Biology of the Cell 2008, 19:3638-3651.
38. Hope H., et al. The Candida albicans ELMO homologue functions together with Rac1 and Dck1, upstream of the MAP Kinase Cek1, in invasive filamentous growth. Molecular Microbiology 2010, 76:1572-1590.
39. Hurtado C.A., et al. A rac homolog is required for induction of hyphal growth in the dimorphic yeast Yarrowia lipolytica. Journal of Bacteriology 2000, 182:2376-2386.
40. Jessup C.J. Fluconazole susceptibility testing of Cryptococcus neoformans: comparison of two broth microdilution methods and clinical correlates among isolates from Ugandan AIDS patients. Journal of Clinical Microbiology 1998, 36:2874-2876.
41. Kang P.J., et al. The Rsr1/Bud1 GTPase interacts with itself and the Cdc42 GTPase during bud-site selection and polarity establishment in budding yeast. Molecular Biology of the Cell 2010, 21:3007-3016.
42. Katz E., et al. Targeting of Rac GTPases blocks the spread of intact human breast cancer. Oncotarget 2012, 3:608-619.
43. Kozminski K.G., et al. Interaction between a Ras and a Rho GTPase couples selection of a growth site to the development of cell polarity in yeast. Molecular Biology of the Cell 2003, 12:4958-4970.
44. Lambeth J.D. NOX enzymes and the biology of reactive oxygen. Nature Reviews Immunology 2004, 4:181-189.
45. Larkin M., et al. ClustalW and ClustalX version 2. Bioinformatics 2007, 23:2947-2948.
46. Li H., et al. The small GTPase RacA mediates intracellular reactive oxygen species production, polarized growth, and virulence in the human fungal pathogen Aspergillus fumigatus. Eukaryotic Cell 2011, 10:174-186.
47. Linardopoulou E., et al. Transcriptional activity of multiple copies of a subtelomerically located olfactory receptor gene that is polymorphic in number and location. Human Molecular Genetics 2001, 10:2373-2383.
48. Loftus B.J., et al. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science (New York, NY) 2005, 307:1321-1324.
49. Mahlert M., et al. Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Molecular Microbiology 2006, 59:567-578.
50. Maruvada R., et al. Cryptococcus neoformans phospholipase B1 activates host cell Rac1 for traversal across the blood-brain barrier. Cellular Microbiology 2012, 14:1544-1553.
51. Ménard L., et al. Rac1, a low-molecular-mass GTP-binding-protein with high intrinsic GTPase activity and distinct biochemical properties. European Journal of Biochemistry/FEBS 1992, 206:537-546.
52. Miller P.J., Johnson D.I. Cdc42p GTPase is involved in controlling polarized cell growth in Schizosaccharomyces pombe. Molecular and Cellular Biology 1994, 14:1075-1083.
53. Missal T.A., et al. Two glutathione peroxidases in the fungal pathogen Cryptococcus neoformans are expressed in the presence of specific substrates. Microbiology (Reading, England) 2005, 151:2573-2581.
54. Morrow C.A., et al. A unique chromosomal rearrangement in the Cryptococcus neoformans var. grubii type strain enhances key phenotypes associated with virulence. mBio 2012, 3.
55. Mortimer R.K. Radiobiological and genetic studies on a polyploid series (haploid to hexaploid) of Saccharomyces cerevisiae. Radiation Research 1958, 9:312-326.
56. Murashige T., Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 1962, 15:473-497.
57. Näsvall J., et al. Real-time evolution of new genes by innovation, amplification, and divergence. Science 2012, 338:384-387.
58. Nichols C.B., et al. PAK kinases Ste20 and Pak1 govern cell polarity at different stages of mating in Cryptococcus neoformans. Molecular Biology of the Cell 2004, 15:4476-4489.
59. Nichols C.B., et al. Subcellular localization directs signaling specificity of the Cryptococcus neoformans Ras1 protein. Eukaryotic Cell 2009, 8:181-189.
60. Nichols C.B., et al. A Ras1-Cdc24 signal transduction pathway mediates thermotolerance in the fungal pathogen Cryptococcus neoformans. Molecular Microbiology 2007, 63:1118-1130.
61. Nielsen K., et al. Sexual Cycle of Cryptococcus neoformans var.grubii and virulence of congenic a and alpha isolates. Infection and Immunity 2003, 71:4381-4841.
62. Odds F.C. Synergy, antagonism, and what the chequerboard puts between them. Journal of Antimicrobial Chemotherapy 2003, 52.
63. Ohkusu M., et al. Deficit in oxygen causes G2 budding and unbudded G2 arrest in Cryptococcus neoformans. FEMS Microbiology Letters 2001, 204:29-32.
64. Ohkusu M., et al. Induced synchrony in Cryptococcus neoformans after release from G2-arrest. Antonie van Leeuwenhoek 2004, 85:37-44.
65. Ohno S. Evolution by Gene Duplication 1970, Springer-Verlag, New York.
66. Okagaki L.H., et al. Cryptococcal titan cell formation is regulated by G-protein signaling in response to multiple stimuli. Eukaryotic Cell 2011, 10:1306-1316.
67. O'Meara T.R., et al. Interaction of Cryptococcus neoformans Rim101 and protein kinase A regulates capsule. PLoS Pathogens 2010, 6:e1000776.
68. Park H.-o., et al. Localization of the Rsr1/Bud1 GTPase involved in selection of a proper growth site in yeast. The Journal of Biological Chemistry 2002, 277:26721-26724.
69. Perfect J.R., et al. Chronic cryptococcal meningitis: a new experimental model in rabbits. American Journal of Pathology 1980, 101:177-194.
70. Price L.S., et al. The small GTPases Rac and Rho as regulators of secretion in mast cells. Current Biology: CB 1995, 5:68-73.
71. Price M.S., et al. The Cryptococcus neoformans Rho-GDP dissociation inhibitor mediates intracellular survival and virulence. Infection and Immunity 2008, 76:5729-5737.
72. Pukkila-Worley R., et al. Transcriptional network of multiple capsule and melanin genes governed by the Cryptococcus neoformans cyclic AMP cascade. Eukaryotic Cell 2005, 4:190-201.
73. Ridley A.J., et al. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992, 70:401-410.
74. Rolke Y., Tudzynski P. The small GTPase Rac and the p21-activated kinase Cla4 in Claviceps purpurea: interaction and impact on polarity, development and pathogenicity. Molecular Microbiology 2008, 68:405-423.
75. Salas S.D., et al. Effect of the laccase gene CNLAC1, on virulence of Cryptococcus neoformans. The Journal of Experimental Medicine 1996, 184:377-386.
76. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols 2008, 3:1101-1108.
77. Schneider C.A., et al. NIH image to ImageJ: 25years of image analysis. Nature Methods 2012, 9:671-675.
78. Selmecki A.M., et al. Acquisition of aneuploidy provides increased fitness during the evolution of antifungal drug resistance. PLoS Genetics 2009, 5.
79. Semighini C.P., Harris S.D. Regulation of apical dominance in Aspergillus nidulans hyphae by reactive oxygen species. Genetics 2008, 179:1919-1932.
80. Shen G., et al. Wsp1, a GBD/CRIB domain-containing WASP homolog, is required for growth, morphogenesis, and virulence of Cryptococcus neoformans. Eukaryotic Cell 2011, 10:521-529.
81. Sherman F. Getting started with yeast. Methods in Enzymology 1991, 194:3-21.
82. Shutes A., et al. Specificity and mechanism of action of EHT 1864, a novel small molecule inhibitor of Rac family small GTPases. The Journal of Biological Chemistry 2007, 282:35666-35678.
83. Sionov E., et al. Cryptococcus neoformans overcomes stress of azole drugs by formation of disomy in specific multiple chromosomes. PLoS Pathogens 2010, 6:e1000848.
84. Staiger C.J., et al. Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. The Journal of Cell Biology 2009, 184:269-280.
85. Takemoto D., et al. A p67Phox-like regulator is recruited to control hyphal branching in a fungal-grass mutualistic symbiosis. The Plant Cell 2006, 18:2807-2821.
86. Takeo K., et al. Unbudded G2 as well as G1 arrest in the stationary phase of the basidiomycetous yeast Cryptococcus neoformans. FEMS Microbiology Letters 1995, 129:231-235.
87. Takeo K., et al. Effects of growth temperature upshift on cell cycle progression in Cryptococcus neoformans. Mycoscience 2003, 44:465-471.
88. Tamura K., et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 2011, 28:2731-2739.
89. Tanaka A., et al. NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloë festucae and perennial ryegrass. Molecular Microbiology 2008, 68:1165-1178.
90. Toffaletti D.L., et al. Gene transfer in Cryptococcus neoformans by use of biolistic delivery of DNA. Journal of Bacteriology 1993, 175:1405-1411.
91. Valencia A., et al. The ras protein family: evolutionary tree and role of conserved amino acids. Biochemistry 1991, 30:4637-4648.
92. Vallim M.A., et al. A Rac homolog functions downstream of Ras1 to control hyphal differentiation and high-temperature growth in the pathogenic fungus Cryptococcus neoformans. Eukaryotic Cell 2005, 4:1066-1078.
93. Virag A., et al. Regulation of hyphal morphogenesis by cdc42 and rac1 homologues in Aspergillus nidulans. Molecular Microbiology 2007, 66:1579-1596.
94. Wang P., et al. Two cyclophilin A homologs with shared and distinct functions important for growth and virulence of Cryptococcus neoformans. EMBO Reports 2001, 2:511-518.
95. Wang P., et al. Mating-type-specific and nonspecific PAK kinases play shared and divergent roles in Cryptococcus neoformans. Eukaryotic Cell 2002, 1:257-272.
96. Waugh M.S., et al. Ras1 and Ras2 contribute shared and unique roles in physiology and virulence of Cryptococcus neoformans. Microbiology (Reading, England) 2002, 148:191-201.
97. Weinzierl G., et al. Regulation of cell separation in the dimorphic fungus Ustilago maydis. Molecular Microbiology 2002, 45:219-231.
98. Wolfe K.H., Shields D.C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 1997, 387:708-713.
99. Wolfram Research I. Mathematica Edition: Version 8.0 2010, Wolfram Research, Inc., Champaign, Illinois.
100. Wright L.P., Philips M.R. Thematic review series: lipid posttranslational modifications. CAAX modification and membrane targeting of Ras. Journal of Lipid Research 2006, 47:883-891.
101. Zheng Y., et al. Interactions among proteins involved in bud-site selection and bud-site assembly in Saccharomyces cerevisiae. The Journal of Biological Chemistry 1995, 270:626-630.