Microbiol Mol Biol Rev 62(4): 1264-1300

MAP Kinase Pathways in the Yeast <em>Saccharomyces cerevisiae</em>

Department of Biochemistry and Cell Biology Rice University, Houston, Texas 77251-1892

^{Corresponding author. Mailing address: Department of Biochemistry and Cell Biology MS140, Rice University, P.O. Box 1892, Houston, TX 77251-1892. Phone: (713) 285-5158. Fax: (713) 285-5154. E-mail:}ude.ecir.coib@nitsug.

Abstract

A cascade of three protein kinases known as a mitogen-activated protein kinase (MAPK) cascade is commonly found as part of the signaling pathways in eukaryotic cells. Almost two decades of genetic and biochemical experimentation plus the recently completed DNA sequence of the Saccharomyces cerevisiae genome have revealed just five functionally distinct MAPK cascades in this yeast. Sexual conjugation, cell growth, and adaptation to stress, for example, all require MAPK-mediated cellular responses. A primary function of these cascades appears to be the regulation of gene expression in response to extracellular signals or as part of specific developmental processes. In addition, the MAPK cascades often appear to regulate the cell cycle and vice versa. Despite the success of the gene hunter era in revealing these pathways, there are still many significant gaps in our knowledge of the molecular mechanisms for activation of these cascades and how the cascades regulate cell function. For example, comparison of different yeast signaling pathways reveals a surprising variety of different types of upstream signaling proteins that function to activate a MAPK cascade, yet how the upstream proteins actually activate the cascade remains unclear. We also know that the yeast MAPK pathways regulate each other and interact with other signaling pathways to produce a coordinated pattern of gene expression, but the molecular mechanisms of this cross talk are poorly understood. This review is therefore an attempt to present the current knowledge of MAPK pathways in yeast and some directions for future research in this area.

Abstract

Despite their placid appearance, cells of the yeast Saccharomyces cerevisiae possess rapidly responding, highly complex signaling pathways. These pathways allow yeast cells to quickly adapt to a changing environment, a critical attribute for a nonmotile species. Prominent among yeast signaling pathways are the mitogen-activated protein kinase cascades (169, 249). These generally contain three protein kinases that act in series: a MAP kinase kinase kinase (MAPKKK or MEKK), a MAP kinase kinase (MAPKK or MEK), and a MAP kinase (MAPK) (66, 71, 290). Thus, when the cascade is activated, the MEKK phosphorylates the MEK, which in turn phosphorylates the MAPK. The MAPK cascades, found in animals (71, 290), plants (173), and fungi (118, 169), often regulate transcription factors by MAPK-mediated phosphorylation. Many extracellular and intracellular signals modulate transcription of specific genes through activation or inhibition of MAPK cascades.

Our understanding of the S. cerevisiae MAPK pathways is more complete than that of MAPK pathways in other organisms. Extensive genetic and biochemical analysis plus the complete sequencing of its genome has revealed that S. cerevisiae contains five MAPKs on five functionally distinct cascades (Fig. (Fig.1)1) (179). Four of these pathways, the mating pathway, the filamentation-invasion pathway, the cell integrity pathway, and the high-osmolarity growth pathway, are present in growing cells. The Smk1p MAPK, part of the spore wall assembly pathway, is not present in growing cells but appears during sporulation and regulates that developmental process. Another type of yeast, the fission yeast Schizosaccharomyces pombe, contains a set of MAPK cascades that have some similarity to those in S. cerevisiae. Although this review is focused on S. cerevisiae MAPK pathways, some similarities and, more importantly, differences between two related MAPK pathways in these two evolutionarily diverged yeasts are discussed. In this review, S. cerevisiae cells will be called yeast or budding yeast and S. pombe cells will be called fission yeast.

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FIG. 1

MAPK cascades of S. cerevisiae. There are four MAPK pathways in vegetatively growing yeast and one, the spore wall assembly pathway, which is expressed only in sporulating yeast. Nomenclature for yeast genes and their products is as follows: STE20, gene name; ste20, recessive mutation; ste20Δ, deletion (usually null) mutation; and Ste20p, protein product of STE20. The question marks indicate that a protein kinase has not yet been identified for this step in a cascade. Note that each cascade has a unique MAPK. In addition, certain protein kinases act in more than one pathway: the MEK Ste7p (two pathways), the MEKK Ste11p (three pathways), and the upstream MAPK cascade activator kinase Ste20p (two pathways). The arrows represent known or postulated steps in signal transduction; see the text for details.

The biochemical mechanisms mediating signal transduction among the three types of kinases in MAPK cascades are fairly well understood (397). MEKK has a regulatory domain at the NH₂ terminus and a protein kinase domain at the COOH terminus. When activated, MEKK phosphorylates both a serine and a threonine residue in a conserved domain in the NH₂-terminal portion of MEK. The phosphorylated and now activated MEK then phosphorylates MAPK on a threonine and a tyrosine residue, separated by a single amino acid, within the activation loop (199) of the conserved kinase domain, thereby activating the kinase activity.

Different classes of MAPKs exist in yeast and also in mammals. These can be classified by the pathways in which they participate and by the identity of the amino acid between the Thr and Tyr in the activation loop: Glu, Pro, or Gly in mammals, and Glu, Gly, or Asn in yeast. For example, the ThrGlyTyr MAPKs such as yeast Hog1p or mammalian p38 are found in stress-activated pathways and the ThrGluTyr MAPKs such as yeast Fus3p or mammalian ERK1 are found in growth factor-activated pathways (230, 397). Although the amino acid between the Thr and Tyr can be used to classify different MAPKs, other regions of the conserved protein kinase domain appear to play a more dominant role in determining the specificity of interactions with the upstream MEK and downstream substrates (49).

Despite a wealth of information on the MAPK cascade itself, there are many unsolved problems concerning this signaling device. The way in which the known upstream activators act on the cascade is still unclear. Identification of new target proteins for the MAPKs and novel activators of the MAPK pathways is still continuing. MAPK cascades appear to exist in cytoplasmic macromolecular complexes with other proteins that serve as scaffolds, anchors, or adaptors. Upon activation, MAPK or MEK is thought to move from the cytosol to the nucleus and phosphorylate target proteins such as transcription factors. How the cytoplasmic complexes of signaling proteins rearrange themselves during signaling to let MAPK or MEK go to the nucleus is not well understood. It is still unclear what determines the speed, magnitude, specificity, and duration of signaling through a MAPK cascade. The mechanisms by which signaling through MAPK pathways is integrated with that through other types of pathways is just starting to be studied. The yeast MAPK pathways are better characterized than those in other eukaryotes. The general principles of operation and the variations of this simple signaling cascade revealed in yeast and described here may thus help guide research on similar pathways in other eukaryotes. Each of the five yeast MAPK-containing pathways is discussed, starting with the mating-pheromone response pathway, the best understood of all eukaryotic MAPK pathways.

ACKNOWLEDGMENTS

We thank Ed Winter and Elaine Elion for their helpful comments on the pheromone response pathway and the spore wall assembly pathway, respectively, and members of the Gustin laboratory for helpful comments on all the sections.

ACKNOWLEDGMENTS

REFERENCES

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