Signal Transduction Cascades Regulating Fungal Development and Virulence

K Lengeler

R Davidson

C D'souza

T Harashima

Departments of Genetics, Pharmacology and Cancer Biology, Microbiology, and Medicine, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina 27710

^{Corresponding author. Mailing address: 322 CARL Building, Box 3546, Research Drive, Duke University Medical Center, Durham, NC 27710. Phone: (919) 684-2824. Fax: (919) 684-5458. E-mail:}ude.ekud@100mtieh.

Abstract

Cellular differentiation, mating, and filamentous growth are regulated in many fungi by environmental and nutritional signals. For example, in response to nitrogen limitation, diploid cells of the yeast Saccharomyces cerevisiae undergo a dimorphic transition to filamentous growth referred to as pseudohyphal differentiation. Yeast filamentous growth is regulated, in part, by two conserved signal transduction cascades: a mitogen-activated protein kinase cascade and a G-protein regulated cyclic AMP signaling pathway. Related signaling cascades play an analogous role in regulating mating and virulence in the plant fungal pathogen Ustilago maydis and the human fungal pathogens Cryptococcus neoformans and Candida albicans. We review here studies on the signaling cascades that regulate development of these and other fungi. This analysis illustrates both how the model yeast S. cerevisiae can serve as a paradigm for signaling in other organisms and also how studies in other fungi provide insights into conserved signaling pathways that operate in many divergent organisms.

Abstract

Fungi are eukaryotic organisms that diverged from a common ancestor with multicellular eukaryotic animals some 800 to 1,000 million years ago. Despite this evolutionary divergence, fungi are more closely related to animals than to plants, algae, bacteria, or archea and thus share important features with mammalian cells. This is perhaps most apparent in the signaling cascades that regulate cell function. The yeast Saccharomyces cerevisiae expresses at least three members of the G protein-coupled family of serpentine receptors, which are in turn coupled to a heterotrimeric G protein and a G protein alpha subunit homolog. Mating in yeast cells is regulated by a mitogen-activated protein (MAP) kinase cascade that is highly conserved with MAP kinase cascades in mammalian cells. Finally, the signal transduction components that are targeted by the immunosuppressive drugs cyclosporin A, FK506, and rapamycin are remarkably conserved from yeasts to humans. Thus, studies on signal transduction in S. cerevisiae and other genetically tractable fungi promise to reveal common conserved mechanisms of signal transduction.

Recent studies have revealed that the model yeast S. cerevisiae undergoes a dimorphic transition to filamentous growth in response to nutritional signals in the environment, particularly nitrogen limitation. Filamentous growth occurs in both haploid and diploid cells in different environments and may play novel roles in the life cycle of this organism. At least two conserved signal transduction cascades that regulate filamentous growth have been defined, and remarkably related signaling pathways also operate during differentiation of other fungi, including pathogens of both plants and animals. These recent findings suggest that S. cerevisiae is also an excellent model system with great potential to provide insights into signaling in other fungi. We review here studies on the signal transduction cascades that regulate yeast filamentous growth and the related signaling pathways that operate in the fission yeast Schizosaccharomyces pombe, in human fungal pathogens (Candida albicans and Cryptococcus neoformans), in plant fungal pathogens (Ustilago maydis, Magnaporthe grisea, and Cryphonectria parasitica), and in model filamentous fungi (Aspergillus nidulans and Neurospora crassa). Taken together, these studies reveal a high degree of conservation between divergent organisms and illustrate conserved basic principles in the molecular determinants of life. Several other excellent reviews on yeast signal transduction have been published recently and also cover some additional topics in fungal development (5, 8, 10, 17, 18, 30, 139, 140, 177, 178, 263, 276, 289, 290).

ACKNOWLEDGMENTS

The first eight authors made equal contributions in the preparation of this review.

We thank Olen Yoder and Marian Carlson for the invitation to prepare this review and Tina Jeffries for patient assistance with manuscript preparation.

Our studies are supported by R01 grants AI39115, AI41937, and AI42159 from NIAID and program project P01 award AI44975 to the Duke University Mycology Research Unit from NIAID. Joseph Heitman is a Burroughs Wellcome Scholar in Molecular Pathogenic Mycology and an associate investigator of the Howard Hughes Medical Institute.

ACKNOWLEDGMENTS

ADDENDUM IN PROOF

A Gα subunit closely related to the nutrient-sensing Gα proteins Gpa2 from S. cerevisiae and gpa2 from S. pombe has recently been identified from A. nidulans and named GNA-3 (A. M. Kays, P. S. Rowley, R. A. Baasiri, and K. A. Borkovich, Mol. Cell. Biol. 20:7693–7705, 2000). Both the intracellular levels of cAMP and the protein levels of adenylyl cyclase were found to be reduced in gna-3 mutant strains, leading to the proposal that this Gα subunit might function by regulating the stability, rather than the activity, of adenylyl cyclase. Further studies will be required to test if GNA-3 plays a role in glucose sensing similar to that of the related Gα subunits in budding and fission yeast.

A recent elegant study has examined in detail the cellular functions of the flocculin proteins Flo11, Flo10, Flo1, and Fig2 in S. cerevisiae, revealing that these proteins can substitute for each other if they are appropriately expressed (B. Guo, C. A. Styles, Q. Feng, and G. R. Fink, Proc. Natl. Acad. Sci. USA 97:12158–12163, 2000). In addition, the cell surface flocculin Flo11 that is required for pseudohyphal differentiation was found to be expressed in filamentous diploid cells at the distal tips but not in nonfilamentous vegetative diploid cells. These experiments suggest that additional levels of regulation of Flo11 expression are involved in differentiation into the filamentous state in S. cerevisiae.

A report on the regulation of haploid filamentous growth by mating pheromone in S. cerevisiae is now in press (S. Erdman and M. Snyder, Genetics, in press). Finally, an excellent review on signal transduction in S. pombe has recently appeared (J. Davey, Yeast 14:1529–1566, 1998).

ADDENDUM IN PROOF

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