Sumoylation of Transcription Factor Tec1 Regulates Signaling of Mitogen-Activated Protein Kinase Pathways in Yeast

Wang, Yuqi; Irqeba, Ameair Abu; Ayalew, Mihretu; Suntay, Kristina

doi:10.1371/journal.pone.0007456

Cited by 19 publications

(18 citation statements)

References 37 publications

(63 reference statements)

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“…Although our insulation model may appear to conflict with reports showing that phosphorylation of Kss1 MAPK (and its cognate MAPKK Ste7) occurs even in HOG1 + cells within 15 min after cells are challenged with hyperosmotic KCl (29,30), we believe that our model is compatible with these data. Kss1 phosphorylation occurs slowly, with low abundance, and is transient (detected only at 15 minutes) (30).…”

Section: Discussioncontrasting

confidence: 71%

“…Upon detailed analysis of the yeast exposed to both stimuli, we found that toxicity associated with the methods they used may have obfuscated the proper interpretation (see Supplementary Materials). Although the specific substrate(s) on which Hog1 acts to prevent crosstalk remain unknown, there is already support in the literature consistent with an insulation mechanism (30). …”

Section: Discussionmentioning

confidence: 99%

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Single-Cell Analysis Reveals That Insulation Maintains Signaling Specificity Between Two Yeast MAPK Pathways with Common Components

2010

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Eukaryotic cells use multiple mitogen-activated protein kinase (MAPK) cascades to evoke appropriate responses to external stimuli. In Saccharomyces cerevisiae, the MAPK Fus3 is activated by pheromone-binding G protein-coupled receptors to promote mating, whereas the MAPK Hog1 is activated by hyperosmotic stress to elicit the high osmolarity glycerol (HOG) response. Although these MAPK pathways share several upstream components, exposure to either pheromone or osmolyte alone triggers only the appropriate response. We used fluorescent localization- and transcription-specific reporters to assess activation of these pathways in individual cells on the minute and hour timescale, respectively. Dual activation of these two MAPK pathways occurred over a broad range of stimulant concentrations and temporal regimes in wild-type cells subjected to co-stimulation. Thus, signaling specificity is achieved through an “insulation” mechanism, not a “cross-inhibition” mechanism. Furthermore, we showed that there was a critical period during which Hog1 activity had to occur for proper insulation of the HOG pathway.

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Section: Discussioncontrasting

confidence: 71%

Section: Discussionmentioning

confidence: 99%

Single-Cell Analysis Reveals That Insulation Maintains Signaling Specificity Between Two Yeast MAPK Pathways with Common Components

2010

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“…Interestingly, the decline of sumoylated conjugates occurred right after the maximal activation of Hog1, a MAP kinase that is responsible for normal osmo-tolerance in yeast, as detected by anti-phospho-p38 that recognizes dually phosphorylated and thus activated Hog1 ( Fig. 1 , lower panel ) [21], [23]. To determine whether Hog1 has any inhibitory role on the accumulation of sumoylated conjugates induced by hyperosmotic stress, we conducted similar experiment in a hog1Δ mutant.…”

Section: Resultsmentioning

confidence: 97%

Regulating Global Sumoylation by a MAP Kinase Hog1 and Its Potential Role in Osmo-Tolerance in Yeast

Irqeba

Panahi

et al. 2014

PLoS ONE

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Sumoylation, a post-translational protein modification by small ubiquitin-like modifier (SUMO), has been implicated in many stress responses. Here we analyzed the potential role of sumoylation in osmo-response in yeast. We find that osmotic stress induces rapid accumulation of sumoylated species in normal yeast cells. Interestingly, disruption of MAP kinase Hog1 leads to a much higher level of accumulation of sumoylated conjugates that are independent of new protein synthesis. We also find that the accumulation of sumoylated species is dependent on a SUMO ligase Siz1. Notably, overexpression of SIZ1 in HOG1-disruption mutants (hog1Δ) but not in wild type cells leads to a markedly increased and prolonged accumulation of sumoylated species. Examination of osmo-tolerance of yeast mutants that display either an increase or a decrease in the global sumoylation level revealed an inverse relationship between accumulation of sumoylated conjugates and osmo-tolerance. Further investigation has shown that many of the sumoylated species induced by hyperosmotic stress are actually poly-sumoylated. Together, these findings indicate that abnormal accumulation of poly-sumoylated conjugates is harmful for osmo-tolerance in yeast, and suggest that Hog1 promotes adaptation to hyperosmotic stress partially via regulation of global sumoylation level.

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“…Failure of Tec1 to be degraded results in cross-talk between the filamentation and mating pathways. Tec1 is subject to complex regulation, being phosphorylated at multiple residues (Bao et al 2010) as well as being sumoylated (Wang et al 2009b). Ste12 itself and other components of the mating/filamentation pathways are also ubiquitinated and degraded to attenuate signaling generated by these pathways (Esch et al 2006).…”

Section: Nutrient-sensing Pathwaysmentioning

confidence: 99%

The Regulation of Filamentous Growth in Yeast

2012

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Filamentous growth is a nutrient-regulated growth response that occurs in many fungal species. In pathogens, filamentous growth is critical for host-cell attachment, invasion into tissues, and virulence. The budding yeast Saccharomyces cerevisiae undergoes filamentous growth, which provides a genetically tractable system to study the molecular basis of the response. Filamentous growth is regulated by evolutionarily conserved signaling pathways. One of these pathways is a mitogen activated protein kinase (MAPK) pathway. A remarkable feature of the filamentous growth MAPK pathway is that it is composed of factors that also function in other pathways. An intriguing challenge therefore has been to understand how pathways that share components establish and maintain their identity. Other canonical signaling pathways-rat sarcoma/protein kinase A (RAS/PKA), sucrose nonfermentable (SNF), and target of rapamycin (TOR)-also regulate filamentous growth, which raises the question of how signals from multiple pathways become integrated into a coordinated response. Together, these pathways regulate cell differentiation to the filamentous type, which is characterized by changes in cell adhesion, cell polarity, and cell shape. How these changes are accomplished is also discussed. High-throughput genomics approaches have recently uncovered new connections to filamentous growth regulation. These connections suggest that filamentous growth is a more complex and globally regulated behavior than is currently appreciated, which may help to pave the way for future investigations into this eukaryotic cell differentiation behavior. TABLE OF CONTENTS Abstract 23Introduction 24

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Sumoylation of Transcription Factor Tec1 Regulates Signaling of Mitogen-Activated Protein Kinase Pathways in Yeast

Cited by 19 publications

References 37 publications

Single-Cell Analysis Reveals That Insulation Maintains Signaling Specificity Between Two Yeast MAPK Pathways with Common Components

Single-Cell Analysis Reveals That Insulation Maintains Signaling Specificity Between Two Yeast MAPK Pathways with Common Components

Regulating Global Sumoylation by a MAP Kinase Hog1 and Its Potential Role in Osmo-Tolerance in Yeast

The Regulation of Filamentous Growth in Yeast

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