A functional Rim101 complex is required for proper accumulation of the Ena1 Na+-ATPase protein in response to salt stress in Saccharomyces cerevisiae

Marques, María Carmen; Zamarbide-Forés, Sara; Pedelini, Leda; Llopis-Torregrosa, Vicent; Yenush, Lynne

doi:10.1093/femsyr/fov017

Cited by 18 publications

(14 citation statements)

References 49 publications

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“…This is in agreement with the well-known role of Rsp5 (the only HECT Ub-ligase in S. cerevisiae) in endocytosis (76). Although Art9 has been shown to be important for the regulation of Ena1 (53), our data indicates that is not crucial for internalization of the transporter. We speculate that Art9 will be involved in the ubiquitination of K residues relevant to other steps of intracellular traffic while Ena1 K 1090 -Ub is required for removal from the plasma membrane.…”

Section: Discussionsupporting

confidence: 92%

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Ubiquitination and Phosphorylation are Independently Required for Epsin-Mediated Internalization of Cargo inS. cerevisiae

A¹,

Hsieh

et al. 2020

Preprint

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# Equally contributing authorsRunning Title: Lys-Ubiquitination and a Ser/Thr-phosphorylation are required for internalization of a yeast epsin-specific cargo.Endocytosis is a vital cellular process required for multiple cellular functions including nutrient uptake and control of cell membrane composition. This process involves the selective retention of cargo proteins into nascent endocytic sites by the endocytic machinery through the recognition of sequence-encoded motifs or post-translationally added tags.In addition to its classical role in proteosome-mediated protein degradation, ubiquitin (Ub) plays an important role as post-translational tag for protein sorting into different subcellular compartments. Indeed, the Ub-tag mediates membrane protein internalization and targeting to the lysosomal/vacuolar and recycling compartments (reviewed in (1, 2)).Since Ub constitutes the main trafficking signal in Saccharomyces cerevisiae (reviewed in (3)), studies in yeast have been instrumental in advancing our understanding of the mechanisms operating in Ub-mediated sorting. For example, it has been clearly established that budding yeast utilizes Rsp5, the only yeast HECT domain-containing, E3 ubiquitin ligase, to promote cargo ubiquitination relevant to endocytosis and other vesicle trafficking events (3, 4). Indeed, Rsp5-mediated ubiquitination is required for the internalization of cargoes such as the pheromone receptor Ste2 (5, 6), the uracil transporter Fur4 (7), the general amino acid permease Gap1 (8) and the zinc transporter Zrt1 (9) among others.Although Rsp5 is capable of directly interacting with PPxY motif-containing substrates via its WW domains (10-13), this consensus sequence is not present in all cargoes that undergo 14). In those cases, the PPxY motif-containing, Arrestin-Related Trafficking (ARTs) adaptor family specifically bridges cargo proteins to Following ubiquitination, plasma membrane cargoes are recognized by endocytic adaptors, such as epsin and Eps15 (or Ede1 in S. cerevisiae), which contain ubiquitinbinding elements like the Ub-interacting motifs (UIMs) or Ub-Associated (UBA) domains. As a consequence of these interactions, cargo is incorporated into nascent endocytic sites and trafficked towards degradative vacuolar/lysosomal compartments or recycling routes.Specifically, eps15 is known to be responsible for the internalization of the AMPA receptor (21) and Cx43 (22) among other ubiquitinated cargoes; while epsin it is involved in the uptake of vascular endothelial growth factor receptor 2 (VEGFR2) (23), notch ligands (24-27), and the epithelial sodium channel ENaC (28,29).

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Section: Discussionsupporting

confidence: 92%

“…3). Since Art9 has been shown to be involved in Ena1 functional regulation (53), but our data showed that is dispensable for internalization, we speculate that this Art protein might play a role in a different Ena1 trafficking event or other regulatory step.…”

Section: Ena1 Internalization Depends On Art3mentioning

confidence: 69%

Ubiquitination and Phosphorylation are Independently Required for Epsin-Mediated Internalization of Cargo inS. cerevisiae

A¹,

Hsieh

et al. 2020

Preprint

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“…More recent work has provided some hints about the mechanism involved in Ena1 trafficking to the plasma membrane. Thus, Marques, Zamarbide‐Fores, Pedelini, Llopis‐Torregrosa, and Yenush () reported that a strain defective in rim8 / art9 , a member of the arrestin‐related trafficking adaptor family required for proteolytic activation of Rim101, was defective in Ena1 protein accumulation at the plasma membrane in response to salt stress and that this could be also observed for other mutants in the Rim pathway. Such effect was apparently independent of the previously known role of the Rim pathway in ENA1 transcriptional induction (see below).…”

Section: The Ena Efflux Systemmentioning

confidence: 95%

Monovalent cation transporters at the plasma membrane in yeasts

Ariño

Ramos

Sychrová

2018

Yeast

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Maintenance of proper intracellular concentrations of monovalent cations, mainly sodium and potassium, is a requirement for survival of any cell. In the budding yeast Saccharomyces cerevisiae, monovalent cation homeostasis is determined by the active extrusion of protons through the Pma1 H -ATPase (reviewed in another chapter of this issue), the influx and efflux of these cations through the plasma membrane transporters (reviewed in this chapter), and the sequestration of toxic cations into the vacuoles. Here, we will describe the structure, function, and regulation of the plasma membrane transporters Trk1, Trk2, Tok1, Nha1, and Ena1, which play a key role in maintaining physiological intracellular concentrations of Na , K , and H , both under normal growth conditions and in response to stress.

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“…Differences were also apparent among protective genes. The Rim101 pathway has mostly been studied for its role during alkaline stress 13 , but it is also required for proper accumulation of the Ena1p transporter and efficient Na + extrusion upon salt stress 23 . Eight genes of the pathway were covered by our experiment.…”

Section: Resultsmentioning

confidence: 99%

Genomics of cellular proliferation under periodic stress

Salignon

Richard

Fulcrand

et al. 2017

Preprint

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17 18 19 20Living systems control cell growth dynamically by processing information from their 21 environment. Although responses to one environmental change have been intensively studied, 22 their glucose-mediated degradation resulted in a growth delay that was negligible after one 59 galactose-to-glucose change but significant over multiple changes 8 . This effect is due to short-60 term 'memory' of galactose exposures, which is mediated by GAL1 transcripts that are 61 produced during the galactose condition and later compete for translation with transcripts of 62 the CLN3 cyclin during the glucose condition. Other memorization effects were observed on 63 bacteria during repeated lactose to glucose transitions, this time due to both short-term 64 memory conferred by persistent gene expression and long-term memory conferred by protein 65 stability 9 . 66 67The yeast response to high concentrations of salt is one of the best studied mechanism 68 of cellular adaptation. When extracellular salinity increases abruptly, cell-size immediately 69 reduces and yeast triggers a large process of adaptation. The translation program 10,11 and 70 turnover of mRNAs 12 are re-defined, calcium accumulates in the cytosol and activates the 71 calcineurin pathway 13 , osmolarity sensors activate the High Osmolarity Glycerol MAPK 72 pathway 13,14 , glycerol accumulates intracellularly as a harmless compensatory solute 14 , and 73 membrane transporters extrude excessive ions 13 . Via this widespread adaptation, hundreds of 74 genes are known to participate to growth control after a transition to high salt. What happens 75 in the case of multiple osmolarity changes is less clear, but can be investigated by periodic 76 stimulations of the adaptive response. For example, periodic transitions between 0 and 0.4M 77 NaCl showed that MAPK activation was efficient and transient after each stress except in the 78 range of ~8 min periods, where sustained activation of the response severely hampered cell 79 growth 15 . How genes involved in salt tolerance contribute to cell growth in specific dynamic 80 regimes is unknown. If a protein participates to the late phase of adaptation its mutation may 81 have a strong impact at large periods and no impact at short ones. It is also possible that 82 mutations affecting growth in dynamic conditions have been missed by long-term adaptation 83

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A functional Rim101 complex is required for proper accumulation of the Ena1 Na+-ATPase protein in response to salt stress in Saccharomyces cerevisiae

Cited by 18 publications

References 49 publications

Ubiquitination and Phosphorylation are Independently Required for Epsin-Mediated Internalization of Cargo inS. cerevisiae

Ubiquitination and Phosphorylation are Independently Required for Epsin-Mediated Internalization of Cargo inS. cerevisiae

Monovalent cation transporters at the plasma membrane in yeasts

Genomics of cellular proliferation under periodic stress

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