Positioning of cell growth and division after osmotic stress requires a map kinase pathway

Brewster, Jay L.; Gustin, Michael C.

doi:10.1002/yea.320100402

Cited by 97 publications

(82 citation statements)

References 42 publications

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“…The actin cytoskeleton is rapidly depolarized via an unidentified pathway upon exposure to osmotic stress, via the Rom2p/Rho1p/Pkc1p pathway upon exposure to heat stress, or via the glucose-sensing pathways upon glucose removal (Brewster and Gustin, 1994;Delley and Hall, 1999; Figures 1 and 5). To investigate possible cross talk between these pathways, we tested whether the various stresses could depolarize actin in the mutants defective in the Rom2p/Rho1p/Pkc1p or glucose-sensing pathways.…”

Section: Interactions Between the Glucose-sensing And Stress Pathwaysmentioning

confidence: 99%

“…The Hog1p MAPK cascade has a crucial role in osmotic sensing, and yet it is not required for either rapid actin depolarization or rapid inhibition of translation initiation upon exposure of yeast to osmotic stress. However, this cascade is required for the accurate repositioning and reassembly of the actin cytoskeleton and the recovery of translation initiation after osmotic shock (Brewster and Gustin, 1994;Uesono and Toh-e, 2002;Yuzyuk et al, 2002). Therefore, the precise factors initially controlling both actin depolarization and the inhibition of translation remain unknown.…”

Section: Introductionmentioning

confidence: 99%

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Simultaneous yet Independent Regulation of Actin Cytoskeletal Organization and Translation Initiation by Glucose inSaccharomyces cerevisiae

Uesono

Ashe

Toh‐e

2004

MBoC

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Acute glucose deprivation rapidly but transiently depolarizes the actin cytoskeleton and inhibits translation initiation in Saccharomyces cerevisiae. Neither rapid actin depolarization nor translation inhibition upon glucose removal occurs in a reg1 disruptant, which is defective in glucose repression, or in the tpk1 w mutant, which has weak cAPK activity. In the absence of additional glucose, recovery of either actin polarization or translation initiation relies upon respiration, the Snf1p protein kinase, and the transcription factors Msn2p and Msn4p. The readdition of glucose to glucose-starved cells causes a rapid recovery of actin polarization as well as translation initiation without respiration. These results indicate that the simultaneous regulation of actin polarization and translation initiation is divided into three reactions: 1) rapid shutdown depending on Reg1p and cAPK after glucose removal, 2) slow adaptation depending on Snf1p and Msn2p/4p in the absence of glucose, and 3) rapid recovery upon readdition of glucose. On glucose removal, translation initiation is rapidly inhibited in a rom2 disruptant, which is defective in rapid actin depolarization, whereas rapid actin depolarization occurs in a pop2/caf1 disruptant, which is defective in rapid inhibition of translation initiation. Thus, translation initiation and actin polarization seem to be simultaneously but independently regulated by glucose deprivation. INTRODUCTIONThe actin cytoskeleton provides the structural basis for cell polarity in the yeast Saccharomyces cerevisiae and is organized primarily into two morphologically distinct structures: cortical patches and cables (Botstein et al., 1997). Cortical patches are discrete cytoskeletal bodies at the plasma membrane, whereas actin cables are long bundles of actin filaments that are oriented along the mother-bud axis. Both structures are polarized during the budding phase of the cell cycle. During early G1 phase, cortical patches and cables are randomly distributed. As a bud emerges, cortical patches cluster at the growing tip and cables extend from the mother cell into the bud. Near the end of bud growth, the patches and cables redistribute randomly, disrupting the asymmetric distribution of the actin cytoskeleton. At the end of mitosis, patches accumulate in and cables reorient toward the mother-bud neck in connection with cytokinesis and septum formation (Botstein et al., 1997).The actin cytoskeleton is also regulated in response to environmental stimuli. Mating pheromone causes polarization of the actin cytoskeleton toward the tip of the mating projection via the Cdc42p GTPase (Read et al., 1992;Leberer et al., 1997). In contrast, stresses such as osmotic shock, heat shock, and glucose starvation depolarize the actin cytoskeleton in budded cells as shown in Figure 1A (Novick et al., 1989;Chowdhury et al., 1992;Delley and Hall, 1999). In particular, the depolarization by heat or osmotic stress is known to be a rapid and transient reaction. A recent report has indicated that the rapid depol...

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Section: Interactions Between the Glucose-sensing And Stress Pathwaysmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Simultaneous yet Independent Regulation of Actin Cytoskeletal Organization and Translation Initiation by Glucose inSaccharomyces cerevisiae

Uesono

Ashe

Toh‐e

2004

MBoC

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“…Osmosensitivity is partially explained by the inability to increase intracellular glycerol under restrictive conditions in order to counteract the extracellular turgor (Albertyn et al, 1994). Under hyperosmotic conditions, hog1 and pbs2 mutant strains display different alterations, such as a defective bud repositioning (Brewster & Gustin, 1994), shmoo projections (O'Rourke & Herskowitz, 1998) and induction of pseudohyphal growth. Some phenotypes are, however, evident under non-restrictive conditions (Jiang et al, 1995;Kapteyn et al, 2001;Lai et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

The Pbs2 MAP kinase kinase is essential for the oxidative-stress response in the fungal pathogen Candida albicans

et al. 2005

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The human fungal pathogen Candida albicans responds to stress by phosphorylation of the Hog1 MAP kinase. PBS2 was cloned and shown to encode the MAP kinase kinase that is involved in this activation, as determined by immunoblot analyses using antibodies that recognize the active form of the target Hog1 protein. Characterization of pbs2 mutants revealed that they were sensitive to both osmotic and oxidative stress and that they, interestingly, displayed differential behaviour from that of hog1 mutants, losing viability when exposed to an oxidative challenge more rapidly than the hog1 strain. Hog1 and Pbs2 were also shown to be involved in the mechanism of adaptation to oxidative stress, as evidenced by the enhanced susceptibility to oxidants of pbs2 and hog1 mutants, compared with the wild-type strain, when cells were previously exposed to a low, sub-lethal concentration of hydrogen peroxide and by the PBS2-dependent diminished activation of Hog1 MAP kinase in the adaptive process. Studies with a chimaeric Hog1-green fluorescent protein fusion revealed that this protein was localized throughout the cell (being excluded from the vacuole), but concentrated in the nucleus in response to NaCl stress, a process that was dependent on the Pbs2 protein. Both Hog1 and Pbs2 also play a role in controlling the phosphorylation state of the other MAP kinases Mkc1 and Cek1, involved respectively in cell-wall integrity and invasive growth. Furthermore, it is demonstrated that PBS2 plays a role in cell-wall biogenesis in this fungal pathogen, as its deletion renders cells with an altered susceptibility to certain cell wall-interfering compounds. INTRODUCTIONEukaryotic cells respond to environmental changes through signal-transduction pathways. MAPK (mitogen-activated protein kinase) routes consist of a three-kinase module: the MAP kinase kinase kinase, the MAP kinase kinase and the MAP kinase, which are activated by sequential phosphorylation in response to different extracellular signals. These pathways are conserved through evolution (Kültz & Burg, 1998) and their functionality is well-documented in some model organisms, such as Saccharomyces cerevisiae and Schizosaccharomyces pombe (Banuett, 1998;Gustin et al., 1998). In budding yeast, six MAPK pathways have been described that perform essential functions in fungal physiology, such as mating, pseudohyphal/invasive growth, cellwall integrity, STE vegetative growth (SVG), spore-wall assembly and adaptation to high osmolarity (HOG) (Gustin et al., 1998;Posas et al., 1998). This last route is activated in response to osmotic and -as described recently -oxidative stress (Haghnazari & Heyer, 2004;Singh, 2000) and mutant cells in some elements of the pathway are sensitive to both kinds of stresses. Osmosensitivity is partially explained by the inability to increase intracellular glycerol under restrictive conditions in order to counteract the extracellular turgor (Albertyn et al., 1994). Under hyperosmotic conditions, hog1 and pbs2 mutant strains display different alterations, suc...

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“…Hyperosmotic shock causes a rapid disassembly of actin cables, followed by depolarization of actin patches from both the bud and the mother-bud neck. Depolarization of the actin cytoskeleton leads to a transient cell cycle arrest; after ϳ1 h, the cells reassemble a polarized actin cytoskeleton, and polarized growth resumes (Chowdhury et al, 1992;Brewster and Gustin, 1994). The mechanisms regulating dynamic changes in actin cytoskeleton organization on osmotic shock are still not understood.…”

Section: Introductionmentioning

confidence: 99%

The MEK Kinase Ssk2p Promotes Actin Cytoskeleton Recovery After Osmotic Stress

Yuzyuk¹,

Foehr

Amberg³

2002

MBoC

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Saccharomyces cerevisiae adapts to osmotic stress through the activation of a conserved highosmolarity growth (HOG) mitogen-activated protein (MAP) kinase pathway. Transmission through the HOG pathway is very well understood, yet other aspects of the cellular response to osmotic stress remain poorly understood, most notably regulation of actin organization. The actin cytoskeleton rapidly disassembles in response to osmotic insult and is induced to reassemble only after osmotic balance with the environment is reestablished. Here, we show that one of three MEK kinases of the HOG pathway, Ssk2p, is specialized to facilitate actin cytoskeleton reassembly after osmotic stress. Within minutes of cells' experiencing osmotic stress or catastrophic disassembly of the actin cytoskeleton through latrunculin A treatment, Ssk2p concentrates in the neck of budding yeast cells and concurrently forms a 1:1 complex with actin. These observations suggest that Ssk2p has a novel, previously undescribed function in sensing damage to the actin cytoskeleton. We also describe a second function for Ssk2p in facilitating reassembly of a polarized actin cytoskeleton at the end of the cell cycle, a prerequisite for efficient cell cycle completion. Loss of Ssk2p, its kinase activity, or its ability to localize and interact with actin led to delays in actin recovery and a resulting delay in cell cycle completion. These unique capabilities of Ssk2p are activated by a novel mechanism that does not involve known components of the HOG pathway.

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Positioning of cell growth and division after osmotic stress requires a map kinase pathway

Cited by 97 publications

References 42 publications

Simultaneous yet Independent Regulation of Actin Cytoskeletal Organization and Translation Initiation by Glucose inSaccharomyces cerevisiae

Simultaneous yet Independent Regulation of Actin Cytoskeletal Organization and Translation Initiation by Glucose inSaccharomyces cerevisiae

The Pbs2 MAP kinase kinase is essential for the oxidative-stress response in the fungal pathogen Candida albicans

The MEK Kinase Ssk2p Promotes Actin Cytoskeleton Recovery After Osmotic Stress

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