Conserved cAMP signaling cascades regulate fungal development and virulence.

Two well characterized signal transduction cascades regulating fungal development and virulence are the MAP kinase and cAMP signaling cascades. Here we review the current state of knowledge on cAMP signaling cascades in fungi. While the processes regulated by cAMP signaling in fungi are as diverse as the fungi themselves, the components involved in signal transduction are remarkably conserved. Fungal cAMP signaling cascades are also quite versatile, which is apparent from the differential regulation of similar biological processes. In this review we compare and contrast cAMP signaling pathways that regulate development in the budding yeast Saccharomyces cerevisiae, the fission yeast Schizosaccharomyces pombe, and differentiation and virulence in the human pathogen Cryptococcus neoformans and the plant pathogen Ustilago maydis. We also present examples of interaction between the cAMP and MAP kinase signaling cascades in the regulation of fungal development and virulence.

[1]  J. Heitman,et al.  Cyclic AMP-Dependent Protein Kinase Controls Virulence of the Fungal Pathogen Cryptococcus neoformans , 2001, Molecular and Cellular Biology.

[2]  C. Shimoda,et al.  The cyclic AMP/PKA signal pathway is required for initiation of spore germination in Schizosaccharomyces pombe , 2001, Yeast.

[3]  Annalisa Ballarini,et al.  Nucleocytoplasmic Distribution of Budding Yeast Protein Kinase A Regulatory Subunit Bcy1 Requires Zds1 and Is Regulated by Yak1-Dependent Phosphorylation of Its Targeting Domain , 2001, Molecular and Cellular Biology.

[4]  C. S. Hoffman,et al.  Glucose monitoring in fission yeast via the Gpa2 galpha, the git5 Gbeta and the git3 putative glucose receptor. , 2000, Genetics.

[5]  M. Feldbrügge,et al.  Activation of the cAMP pathway in Ustilago maydis reduces fungal proliferation and teliospore formation in plant tumors. , 2000, Molecular plant-microbe interactions : MPMI.

[6]  J. D. de Winde,et al.  Glucose‐induced cAMP signalling in yeast requires both a G‐protein coupled receptor system for extracellular glucose detection and a separable hexose kinase‐dependent sensing process , 2000, Molecular microbiology.

[7]  C. S. Hoffman,et al.  Protein Kinase A and Mitogen-Activated Protein Kinase Pathways Antagonistically Regulate Fission Yeast fbp1Transcription by Employing Different Modes of Action at Two Upstream Activation Sites , 2000, Molecular and Cellular Biology.

[8]  J. Baran,et al.  Primary cutaneous cryptococcosis of the nose in an immunocompetent woman. , 2000, Journal of the American Academy of Dermatology.

[9]  R. Chin,et al.  Pulmonary cryptococcosis in the immunocompetent host. Therapy with oral fluconazole: a report of four cases and a review of the literature. , 2000, Chest.

[10]  D. Andrews,et al.  The Ustilago maydis ubc4 and ubc5 genes encode members of a MAP kinase cascade required for filamentous growth. , 2000, Molecular plant-microbe interactions : MPMI.

[11]  A. Casadevall,et al.  Cryptococcus neoformans Is a Facultative Intracellular Pathogen in Murine Pulmonary Infection , 2000, Infection and Immunity.

[12]  A. Casadevall,et al.  Melanisation of Cryptococcus neoformans in human brain tissue , 2000, The Lancet.

[13]  J. D. de Winde,et al.  Nutrient-induced signal transduction through the protein kinase A pathway and its role in the control of metabolism, stress resistance, and growth in yeast. , 2000, Enzyme and microbial technology.

[14]  A. Casadevall,et al.  Synthesis of Polymerized Melanin by Cryptococcus neoformans in Infected Rodents , 2000, Infection and Immunity.

[15]  J. Heitman,et al.  RAS1 regulates filamentation, mating and growth at high temperature of Cryptococcus neoformans , 2000, Molecular microbiology.

[16]  C. S. Hoffman,et al.  The fission yeast git5 gene encodes a Gbeta subunit required for glucose-triggered adenylate cyclase activation. , 2000, Genetics.

[17]  B. Wickes,et al.  Cryptococcus neoformans STE12α Regulates Virulence but Is Not Essential for Mating , 2000, The Journal of experimental medicine.

[18]  A. Casadevall,et al.  Urease as a Virulence Factor in Experimental Cryptococcosis , 2000, Infection and Immunity.

[19]  J. Heitman,et al.  The G protein-coupled receptor gpr1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. , 2000, Genetics.

[20]  H. Ruis,et al.  Nutritional Control of Nucleocytoplasmic Localization of cAMP-dependent Protein Kinase Catalytic and Regulatory Subunits in Saccharomyces cerevisiae * , 2000, The Journal of Biological Chemistry.

[21]  J. Heitman,et al.  The G-Protein β Subunit GPB1 Is Required for Mating and Haploid Fruiting in Cryptococcus neoformans , 2000, Molecular and Cellular Biology.

[22]  C. S. Hoffman,et al.  Glucose Monitoring in Fission Yeast via the gpa2 Ga, the git5 Gb and the git3 Putative Glucose Receptor , 2000 .

[23]  J. Heitman,et al.  Morphogenesis of Cryptococcus neoformans. , 2000, Contributions to microbiology.

[24]  M. Feldbrügge,et al.  Fungal-plant signalling in the Ustilago maydis-maize pathosystem. , 1999, Current opinion in microbiology.

[25]  J. Heitman,et al.  The STE12alpha homolog is required for haploid filamentation but largely dispensable for mating and virulence in Cryptococcus neoformans. , 1999, Genetics.

[26]  S. Gold,et al.  A MAP kinase encoded by the ubc3 gene of Ustilago maydis is required for filamentous growth and full virulence , 1999, Molecular microbiology.

[27]  J. D. de Winde,et al.  A novel regulator of G protein signalling in yeast, Rgs2, downregulates glucose‐activation of the cAMP pathway through direct inhibition of Gpa2 , 1999, The EMBO journal.

[28]  Sabine Martin,et al.  Phospholipase C Binds to the Receptor-like GPR1Protein and Controls Pseudohyphal Differentiation inSaccharomyces cerevisiae * , 1999, The Journal of Biological Chemistry.

[29]  W. Bandlow,et al.  The Yeast Trimeric Guanine Nucleotide-Binding Protein α Subunit, Gpa2p, Controls the Meiosis-Specific Kinase Ime2p Activity in Response to Nutrients , 1999, Molecular and Cellular Biology.

[30]  J. D. de Winde,et al.  Novel sensing mechanisms and targets for the cAMP–protein kinase A pathway in the yeast Saccharomyces cerevisiae , 1999, Molecular microbiology.

[31]  J. Heitman,et al.  Signal transduction cascades regulating mating, filamentation, and virulence in Cryptococcus neoformans. , 1999, Current opinion in microbiology.

[32]  J. Heitman,et al.  Cyclic AMP-Dependent Protein Kinase Regulates Pseudohyphal Differentiation in Saccharomyces cerevisiae , 1999, Molecular and Cellular Biology.

[33]  F. Lottspeich,et al.  Environmental Signals Controlling Sexual Development of the Corn Smut Fungus Ustilago maydis through the Transcriptional Regulator Prf1 , 1999, Plant Cell.

[34]  J. D. de Winde,et al.  A Saccharomyces cerevisiae G‐protein coupled receptor, Gpr1, is specifically required for glucose activation of the cAMP pathway during the transition to growth on glucose , 1999, Molecular microbiology.

[35]  G. Fink,et al.  Crosstalk between the Ras2p-controlled mitogen-activated protein kinase and cAMP pathways during invasive growth of Saccharomyces cerevisiae. , 1999, Molecular biology of the cell.

[36]  G. Fink,et al.  MAP kinase and cAMP filamentation signaling pathways converge on the unusually large promoter of the yeast FLO11 gene , 1999, The EMBO journal.

[37]  W. Powderly,et al.  Pulmonary cryptococcosis in patients without HIV infection. , 1999, Chest.

[38]  P. Ma,et al.  The PDE1-encoded low-affinity phosphodiesterase in the yeast Saccharomyces cerevisiae has a specific function in controlling agonist-induced cAMP signaling. , 1999, Molecular biology of the cell.

[39]  J. Davey Fusion of a fission yeast , 1998, Yeast.

[40]  J. Broach,et al.  Efficient transition to growth on fermentable carbon sources in Saccharomyces cerevisiae requires signaling through the Ras pathway , 1998, The EMBO journal.

[41]  G. Fink,et al.  The three yeast A kinases have specific signaling functions in pseudohyphal growth. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  H. Kumagai,et al.  Gpr1p, a putative G-protein coupled receptor, regulates glucose-dependent cellular cAMP level in yeast Saccharomyces cerevisiae. , 1998, Biochemical and biophysical research communications.

[43]  R. Kahmann,et al.  Crosstalk between cAMP and pheromone signalling pathways in Ustilago maydis , 1998, Molecular and General Genetics MGG.

[44]  A. Lichter,et al.  Control of pigmentation of Ustilago hordei: the effect of pH, thiamine, and involvement of the cAMP cascade. , 1998, Fungal genetics and biology : FG & B.

[45]  J. Heitman,et al.  Signal transduction pathways regulating differentiation and pathogenicity of Cryptococcus neoformans. , 1998, Fungal genetics and biology : FG & B.

[46]  T. Boller,et al.  Saccharomyces cerevisiae cAMP-dependent protein kinase controls entry into stationary phase through the Rim15p protein kinase. , 1998, Genes & development.

[47]  S. Gold,et al.  Characterization and Molecular Genetic Complementation of Mutants Affecting Dimorphism in the FungusUstilago maydis , 1998 .

[48]  J. Hamer,et al.  Divergent cAMP Signaling Pathways Regulate Growth and Pathogenesis in the Rice Blast Fungus Magnaporthe grisea , 1998, Plant Cell.

[49]  M. Ward,et al.  Yeast PKA represses Msn2p/Msn4p‐dependent gene expression to regulate growth, stress response and glycogen accumulation , 1998, The EMBO journal.

[50]  J. D. de Winde,et al.  Involvement of distinct G‐proteins, Gpa2 and Ras, in glucose‐ and intracellular acidification‐induced cAMP signalling in the yeast Saccharomyces cerevisiae , 1998, The EMBO journal.

[51]  A. Casadevall,et al.  The antibody response to fungal melanin in mice. , 1998, Journal of immunology.

[52]  J. Kronstad,et al.  Identification of a cAMP-dependent protein kinase catalytic subunit required for virulence and morphogenesis in Ustilago maydis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[53]  J. Hirsch,et al.  GPR1 encodes a putative G protein‐coupled receptor that associates with the Gpa2p Gα subunit and functions in a Ras‐independent pathway , 1998, The EMBO journal.

[54]  M. Jacquet,et al.  Msn2p and Msn4p Control a Large Number of Genes Induced at the Diauxic Transition Which Are Repressed by Cyclic AMP inSaccharomyces cerevisiae , 1998, Journal of bacteriology.

[55]  A. Casadevall,et al.  Melanization of Cryptococcus neoformans in Murine Infection , 1998 .

[56]  Mayorga,et al.  Characterization and molecular genetic complementation of mutants affecting dimorphism in the fungus ustilago maydis , 1998, Fungal genetics and biology : FG & B.

[57]  W. Lo,et al.  The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. , 1998, Molecular biology of the cell.

[58]  S Ie,et al.  Cryptococcus neoformans. , 1998, The Journal of the Louisiana State Medical Society : official organ of the Louisiana State Medical Society.

[59]  J. Heitman,et al.  Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. , 1997, Genes & development.

[60]  B. Wickes,et al.  The Cryptococcus neoformans STE12α gene: a putative Saccharomyces cerevisiae STE12 homologue that is mating type specific , 1997, Molecular microbiology.

[61]  J. Heitman,et al.  Yeast pseudohyphal growth is regulated by GPA2, a G protein α homolog , 1997 .

[62]  A. Lichter,et al.  Fil1, a G-protein α-subunit that acts upstream of cAMP and is essential for dimorphic switching in haploid cells of Ustilago hordei , 1997, Molecular and General Genetics MGG.

[63]  S. Gold,et al.  The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. , 1997, The Plant cell.

[64]  M. Lisanti,et al.  Gpa2p, a G-protein α-Subunit, Regulates Growth and Pseudohyphal Development in Saccharomyces cerevisiae via a cAMP-dependent Mechanism* , 1997, The Journal of Biological Chemistry.

[65]  J. Heitman,et al.  Calcineurin is required for virulence of Cryptococcus neoformans , 1997, The EMBO journal.

[66]  A. Mitchell,et al.  Stimulation of yeast meiotic gene expression by the glucose-repressible protein kinase Rim15p , 1997, Molecular and cellular biology.

[67]  M. Bölker,et al.  G proteins in Ustilago maydis: transmission of multiple signals? , 1997, The EMBO journal.

[68]  G. Fink,et al.  Dissection of filamentous growth by transposon mutagenesis in Saccharomyces cerevisiae. , 1997, Genetics.

[69]  W. Lo,et al.  FLO11, a yeast gene related to the STA genes, encodes a novel cell surface flocculin , 1996, Journal of bacteriology.

[70]  G. Fink,et al.  Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. , 1996, Genetics.

[71]  P. Russell,et al.  Conjugation, meiosis, and the osmotic stress response are regulated by Spc1 kinase through Atf1 transcription factor in fission yeast. , 1996, Genes & development.

[72]  T. Toda,et al.  The Atf1 transcription factor is a target for the Sty1 stress-activated MAP kinase pathway in fission yeast. , 1996, Genes & development.

[73]  I. S. Pretorius,et al.  Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[74]  J. Perfect,et al.  Effect of the laccase gene CNLAC1, on virulence of Cryptococcus neoformans , 1996, The Journal of experimental medicine.

[75]  B. Wickes,et al.  Dimorphism and haploid fruiting in Cryptococcus neoformans: association with the alpha-mating type. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[76]  A. Schmitt,et al.  Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[77]  K. Kwon-Chung,et al.  The second capsule gene of cryptococcus neoformans, CAP64, is essential for virulence , 1996, Infection and immunity.

[78]  G. Fink,et al.  Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[79]  A. Marchler-Bauer,et al.  The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). , 1996, The EMBO journal.

[80]  M. Bölker,et al.  The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. , 1996, The EMBO journal.

[81]  M. Yamamoto,et al.  Schizosaccharomyces pombe gad7+ encodes a phosphoprotein with a bZIP domain, which is required for proper G1 arrest and gene expression under nitrogen starvation , 1996, Genes to cells : devoted to molecular & cellular mechanisms.

[82]  M. Yamamoto,et al.  The molecular control mechanisms of meiosis in fission yeast. , 1996, Trends in biochemical sciences.

[83]  T. Toda,et al.  Schizosaccharomyces pombe atf1+ encodes a transcription factor required for sexual development and entry into stationary phase. , 1995, The EMBO journal.

[84]  T. Beccari,et al.  Downregulation by cryptococcal polysaccharide of tumor necrosis factor alpha and interleukin-1 beta secretion from human monocytes , 1995, Infection and immunity.

[85]  A. Casadevall,et al.  Virulence: Mechanism of Action. Cryptococcus Neoformans Melanin And , 1995 .

[86]  J. Murphy,et al.  Effects of the two varieties of Cryptococcus neoformans cells and culture filtrate antigens on neutrophil locomotion , 1995, Infection and immunity.

[87]  M. Yamamoto,et al.  sck1, a high copy number suppressor of defects in the cAMP-dependent protein kinase pathway in fission yeast, encodes a protein homologous to the Saccharomyces cerevisiae SCH9 kinase. , 1995, Genetics.

[88]  J. Ruiz-Herrera,et al.  Yeast-mycelial dimorphism of haploid and diploid strains of Ustilago maydis , 1995 .

[89]  F. Banuett Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. , 1995, Annual review of genetics.

[90]  S. Gold,et al.  cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. , 1994, Genes & development.

[91]  M. Yamamoto,et al.  Glucose repression of fbp1 transcription of Schizosaccharomyces pombe is partially regulated by adenylate cyclase activation by a G protein alpha subunit encoded by gpa2 (git8). , 1994, Genetics.

[92]  J. Thevelein,et al.  Activation of trehalase during growth induction by nitrogen sources in the yeast Saccharomyces cerevisiae depends on the free catalytic subunits of camp‐dependent protein kinase, but not on functional ras proteins , 1994, Yeast.

[93]  J. Edman,et al.  Melanin-deficient mutants of Cryptococcus neoformans. , 1994, Journal of medical and veterinary mycology : bi-monthly publication of the International Society for Human and Animal Mycology.

[94]  K. Kwon-Chung,et al.  Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence , 1994, Molecular and cellular biology.

[95]  P. McNamara,et al.  Cloning of a Cryptococcus neoformans gene, GPA1, encoding a G-protein alpha-subunit homolog , 1994, Infection and immunity.

[96]  M. Yamamoto,et al.  Cloning of the pka1 gene encoding the catalytic subunit of the cAMP-dependent protein kinase in Schizosaccharomyces pombe. , 1994, The Journal of biological chemistry.

[97]  P. Sternweis The active role of ? in signal transduction , 1994 .

[98]  P. Williamson Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase , 1994, Journal of bacteriology.

[99]  M. Wigler,et al.  Concerted action of RAS and G proteins in the sexual response pathways of Schizosaccharomyces pombe , 1994, Molecular and cellular biology.

[100]  D. Mills,et al.  Cyclic Amp Regulates the Dimorphic Switch in Ustilago Hordei , 1994 .

[101]  David E. Clapham,et al.  New roles for G-protein (βγ-dimers in transmembrane signalling , 1993, Nature.

[102]  C. S. Hoffman,et al.  Six git genes encode a glucose-induced adenylate cyclase activation pathway in the fission yeast Schizosaccharomyces pombe. , 1993, Journal of cell science.

[103]  S. Gold,et al.  Identification and complementation of a mutation to constitutive filamentous growth in Ustilago maydis. , 1993, Molecular plant-microbe interactions : MPMI.

[104]  J. Edman,et al.  The alpha-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene , 1993, Molecular and cellular biology.

[105]  E. Anaissie,et al.  Regulation of cryptococcal capsular polysaccharide by iron. , 1993, The Journal of infectious diseases.

[106]  M. Yamamoto,et al.  Characterization of a fission yeast gene, gpa2, that encodes a G alpha subunit involved in the monitoring of nutrition. , 1992, Genes & development.

[107]  F. Banuett Ustilago maydis, the delightful blight. , 1992, Trends in genetics : TIG.

[108]  O. Nielsen,et al.  The ras1 function of Schizosaccharomyces pombe mediates pheromone‐induced transcription. , 1992, The EMBO journal.

[109]  Gerald R. Fink,et al.  Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: Regulation by starvation and RAS , 1992, Cell.

[110]  B. Gillissen,et al.  A two-component regulatory system for self/non-self recognition in Ustilago maydis , 1992, Cell.

[111]  M. Bölker,et al.  The a mating type locus of U. maydis specifies cell signaling components , 1992, Cell.

[112]  B. Wickes,et al.  Genetic association of mating types and virulence in Cryptococcus neoformans , 1992, Infection and immunity.

[113]  D. Beach,et al.  Interaction between ran1+ protein kinase and cAMP dependent protein kinase as negative regulators of fission yeast meiosis. , 1991, The EMBO journal.

[114]  M. Yamamoto,et al.  Schizosaccharomyces pombe ste11+ encodes a transcription factor with an HMG motif that is a critical regulator of sexual development. , 1991, Genes & development.

[115]  Melvin I. Simon,et al.  Diversity of G proteins in signal transduction , 1991, Science.

[116]  F. Winston,et al.  Glucose repression of transcription of the Schizosaccharomyces pombe fbp1 gene occurs by a cAMP signaling pathway. , 1991, Genes & development.

[117]  A. Levitzki,et al.  The regulation of adenylyl cyclase by receptor-operated G proteins. , 1991, Pharmacology & therapeutics.

[118]  M. Yamamoto,et al.  Adenylyl cyclase is dispensable for vegetative cell growth in the fission yeast Schizosaccharomyces pombe. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[119]  J. Thevelein,et al.  Glucose-induced hyperaccumulation of cyclic AMP and defective glucose repression in yeast strains with reduced activity of cyclic AMP-dependent protein kinase , 1990, Molecular and cellular biology.

[120]  F. Winston,et al.  Isolation and characterization of mutants constitutive for expression of the fbp1 gene of Schizosaccharomyces pombe. , 1990, Genetics.

[121]  I. Herskowitz,et al.  The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif , 1990, Cell.

[122]  Susan S. Taylor,et al.  cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. , 1990, Annual review of biochemistry.

[123]  M. Wigler,et al.  The adenylyl cyclase gene from Schizosaccharomyces pombe. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[124]  T. Kataoka,et al.  Adenylate cyclases in yeast: a comparison of the genes from Schizosaccharomyces pombe and Saccharomyces cerevisiae. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[125]  J. Kronstad,et al.  Isolation of two alleles of the b locus of Ustilago maydis. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[126]  M. Wigler,et al.  cAMP-independent control of sporulation, glycogen metabolism, and heat shock resistance in S. cerevisiae , 1988, Cell.

[127]  K. Arai,et al.  Isolation of a second yeast Saccharomyces cerevisiae gene (GPA2) coding for guanine nucleotide-binding regulatory protein: studies on its structure and possible functions. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[128]  J M Thevelein,et al.  Studies on the mechanism of the glucose-induced cAMP signal in glycolysis and glucose repression mutants of the yeast Saccharomyces cerevisiae. , 1988, European journal of biochemistry.

[129]  M. Wigler,et al.  Cloning and characterization of the low-affinity cyclic AMP phosphodiesterase gene of Saccharomyces cerevisiae , 1987, Molecular and cellular biology.

[130]  Michael Wigler,et al.  Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase , 1987, Cell.

[131]  M. Wigler,et al.  Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae , 1987, Molecular and cellular biology.

[132]  A. Gilman,et al.  G proteins: transducers of receptor-generated signals. , 1987, Annual review of biochemistry.

[133]  M. Wigler,et al.  Cloning and characterization of the high-affinity cAMP phosphodiesterase of Saccharomyces cerevisiae. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[134]  K. Kwon-Chung,et al.  Encapsulation and melanin formation as indicators of virulence in Cryptococcus neoformans , 1986, Infection and immunity.

[135]  M. Wigler,et al.  DNA sequence and characterization of the S. cerevisiae gene encoding adenylate cyclase , 1985, Cell.

[136]  H. Bourne,et al.  Isolation of the gene encoding adenylate cyclase in Saccharomyces cerevisiae. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[137]  J. Perfect,et al.  Virulence of Cryptococcus neoformans. Regulation of capsule synthesis by carbon dioxide. , 1985, The Journal of clinical investigation.

[138]  M. Wigler,et al.  Differential activation of yeast adenylate cyclase by wild type and mutant RAS proteins , 1985, Cell.

[139]  M. Wigler,et al.  In yeast, RAS proteins are controlling elements of adenylate cyclase , 1985, Cell.

[140]  E. Scolnick,et al.  Requirement of either of a pair of ras-related genes of Saccharomyces cerevisiae for spore viability , 1984, Nature.

[141]  M. Wigler,et al.  Genetic analysis of yeast RAS1 and RAS2 genes , 1984, Cell.

[142]  A. Gilman G proteins and dual control of adenylate cyclase , 1984, Cell.

[143]  K. Matsumoto,et al.  Identification of the structural gene and nonsense alleles for adenylate cyclase in Saccharomyces cerevisiae , 1984, Journal of bacteriology.

[144]  K. Matsumoto,et al.  Control of cell division in Saccharomyces cerevisiae mutants defective in adenylate cyclase and cAMP-dependent protein kinase. , 1983, Experimental cell research.

[145]  R. Mosley,et al.  Regulation of cell-mediated immunity in cryptococcosis. II. Characterization of first-order T suppressor cells (Ts1) and induction of second-order suppressor cells. , 1983, Journal of immunology.

[146]  I. Polacheck,et al.  Melanin-lacking mutants of Cryptococcus neoformans and their virulence for mice , 1982, Journal of bacteriology.

[147]  V. Hearing,et al.  Biochemical studies of phenoloxidase and utilization of catecholamines in Cryptococcus neoformans , 1982, Journal of bacteriology.

[148]  J. Murphy,et al.  Regulation of cell-mediated immunity in cryptococcosis. I. Induction of specific afferent T suppressor cells by cryptococcal antigen. , 1982, Journal of immunology.

[149]  D. Ahearn,et al.  Regulation of melanin production by Cryptococcus neoformans , 1979, Journal of clinical microbiology.

[150]  M. Frank,et al.  Complement depletion in cryptococcal sepsis. , 1978, Journal of immunology.

[151]  M. Kane,et al.  The role of the classical and alternate complement pathways in host defenses against Cryptococcus neoformans infection. , 1974, Journal of immunology.

[152]  D. Ellis,et al.  The Yeasts , 1921, Nature.