Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid

Abstract Background Programmed cell death (PCD) induced by acetic acid, the main by-product released during cellulosic hydrolysis, cast a cloud over lignocellulosic biofuel fermented by Saccharomyces cerevisiae and became a burning problem. Atg22p, an ignored integral membrane protein located in vacuole belongs to autophagy-related genes family; prior study recently reported that it is required for autophagic degradation and efflux of amino acids from vacuole to cytoplasm. It may alleviate the intracellular starvation of nutrition caused by Ac and increase cell tolerance. Therefore, we investigate the role of atg22 in cell death process induced by Ac in which attempt is made to discover new perspectives for better understanding of the mechanisms behind tolerance and more robust industrial strain construction. Results In this study, we compared cell growth, physiological changes in the absence and presence of Atg22p under Ac exposure conditions. It is observed that disruption and overexpression of Atg22p delays and enhances acetic acid-induced PCD, respectively. The deletion of Atg22p in S. cerevisiae maintains cell wall integrity, and protects cytomembrane integrity, fluidity and permeability upon Ac stress by changing cytomembrane phospholipids, sterols and fatty acids. More interestingly, atg22 deletion increases intracellular amino acids to aid yeast cells for tackling amino acid starvation and intracellular acidification. Further, atg22 deletion upregulates series of stress response genes expression such as heat shock protein family, cell wall integrity and autophagy. Conclusions The findings show that Atg22p possessed the new function related to cell resistance to Ac. This may help us have a deeper understanding of PCD induced by Ac and provide a new strategy to improve Ac resistance in designing industrial yeast strains for bioethanol production during lignocellulosic biofuel fermentation.

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Acetic acid induces a programmed cell death process in the food spoilage yeast

FEMS Yeast Research ◽

10.1016/s1567-1356(02)00166-6 ◽

2003 ◽

Vol 3 (1) ◽

pp. 91-96 ◽

Cited By ~ 1

Author(s):

P LUDOVICO ◽

F SANSONETTY ◽

M SILVA ◽

M CORTEREAL

Keyword(s):

Cell Death ◽

Acetic Acid ◽

Programmed Cell Death ◽

Death Process ◽

Food Spoilage ◽

Spoilage Yeast ◽

Cell Death Process

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Translation machinery reprogramming in programmed cell death in Saccharomyces cerevisiae

Cell Death Discovery ◽

10.1038/s41420-020-00392-x ◽

2021 ◽

Vol 7 (1) ◽

Author(s):

Francesco Monticolo ◽

Emanuela Palomba ◽

Maria Luisa Chiusano

Keyword(s):

Saccharomyces Cerevisiae ◽

Cell Death ◽

Acetic Acid ◽

Programmed Cell Death ◽

Differential Expression ◽

Ribosomal Proteins ◽

Relative Proportion ◽

Duplication Event ◽

Genome Duplication Event ◽

Cell Death Pathway

AbstractProgrammed cell death involves complex molecular pathways in both eukaryotes and prokaryotes. In Escherichia coli, the toxin–antitoxin system (TA-system) has been described as a programmed cell death pathway in which mRNA and ribosome organizations are modified, favoring the production of specific death-related proteins, but also of a minor portion of survival proteins, determining the destiny of the cell population. In the eukaryote Saccharomyces cerevisiae, the ribosome was shown to change its stoichiometry in terms of ribosomal protein content during stress response, affecting the relative proportion between ohnologs, i.e., the couple of paralogs derived by a whole genome duplication event. Here, we confirm the differential expression of ribosomal proteins in yeast also during programmed cell death induced by acetic acid, and we highlight that also in this case pairs of ohnologs are involved. We also show that there are different trends in cytosolic and mitochondrial ribosomal proteins gene expression during the process. Moreover, we show that the exposure to acetic acid induces the differential expression of further genes coding for products related to translation processes and to rRNA post-transcriptional maturation, involving mRNA decapping, affecting translation accuracy, and snoRNA synthesis. Our results suggest that the reprogramming of the overall translation apparatus, including the cytosolic ribosome reorganization, are relevant events in yeast programmed cell death induced by acetic acid.

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Cytochrome c Trp65Ser substitution results in inhibition of acetic acid-induced programmed cell death in Saccharomyces cerevisiae

Mitochondrion ◽

10.1016/j.mito.2011.08.007 ◽

2011 ◽

Vol 11 (6) ◽

pp. 987-991 ◽

Cited By ~ 5

Author(s):

Nicoletta Guaragnella ◽

Salvatore Passarella ◽

Ersilia Marra ◽

Sergio Giannattasio

Keyword(s):

Saccharomyces Cerevisiae ◽

Cell Death ◽

Acetic Acid ◽

Cytochrome C ◽

Programmed Cell Death

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Production of Prodiginines Is Part of a Programmed Cell Death Process in Streptomyces coelicolor

Frontiers in Microbiology ◽

10.3389/fmicb.2018.01742 ◽

2018 ◽

Vol 9 ◽

Cited By ~ 15

Author(s):

Elodie Tenconi ◽

Matthew F. Traxler ◽

Charline Hoebreck ◽

Gilles P. van Wezel ◽

Sébastien Rigali

Keyword(s):

Cell Death ◽

Programmed Cell Death ◽

Streptomyces Coelicolor ◽

Death Process ◽

Cell Death Process

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Internucleosomal DNA fragmentation and programmed cell death (apoptosis) in the interdigital tissue of the embryonic chick leg bud

Journal of Cell Science ◽

10.1242/jcs.106.1.201 ◽

1993 ◽

Vol 106 (1) ◽

pp. 201-208 ◽

Cited By ~ 10

Author(s):

V. Garcia-Martinez ◽

D. Macias ◽

Y. Ganan ◽

J.M. Garcia-Lobo ◽

M.V. Francia ◽

...

Keyword(s):

Cell Death ◽

Programmed Cell Death ◽

Dna Fragmentation ◽

Limb Development ◽

Light Transmission ◽

Morphological Changes ◽

Death Process ◽

Chondrogenic Potential ◽

Cell Death Process ◽

Dying Cells

In this work we have attempted to characterize the programmed cell death process in the chick embryonic interdigital tissue. Interdigital cell death is a prominent phenomenon during limb development and has the role of sculpturing the digits. Morphological changes in the regressing interdigital tissue studied by light, transmission and scanning electron microscopy were correlated with the occurrence of internucleosomal DNA fragmentation, evaluated using agarose gels. Programming of the cell death process was also analyzed by testing the chondrogenic potential of the interdigital mesenchyme, in high density cultures. Our results reveal a progressive loss of the chondrogenic potential of the interdigital mesenchyme, detectable 36 hours before the onset of the degenerative process. Internucleosomal DNA fragmentation was only detected concomitant with the appearance of cells dying with the morphology of apoptosis, but unspecific DNA fragmentation was also present at the same time. This unspecific DNA fragmentation was explained by a precocious activation of the phagocytic removal of the dying cells, confirmed in the tissue sections. From our observations it is suggested that programming of cell death involves changes before endonuclease activation. Further, cell surface changes involved in the phagocytic uptake of the dying cells appear to be as precocious as endonuclease activation.

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Acid stress adaptation protects Saccharomyces cerevisiae from acetic acid-induced programmed cell death

Gene ◽

10.1016/j.gene.2005.03.030 ◽

2005 ◽

Vol 354 ◽

pp. 93-98 ◽

Cited By ~ 73

Author(s):

Sergio Giannattasio ◽

Nicoletta Guaragnella ◽

Manuela Corte-Real ◽

Salvatore Passarella ◽

Ersilia Marra

Keyword(s):

Saccharomyces Cerevisiae ◽

Cell Death ◽

Acetic Acid ◽

Programmed Cell Death ◽

Acid Stress ◽

Stress Adaptation

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RNA-Seq-based transcriptomic and metabolomic analysis reveal stress responses and programmed cell death induced by acetic acid in Saccharomyces cerevisiae

Scientific Reports ◽

10.1038/srep42659 ◽

2017 ◽

Vol 7 (1) ◽

Cited By ~ 26

Author(s):

Yachen Dong ◽

Jingjin Hu ◽

Linlin Fan ◽

Qihe Chen

Keyword(s):

Saccharomyces Cerevisiae ◽

Cell Death ◽

Acetic Acid ◽

Programmed Cell Death ◽

Stress Responses ◽

Metabolomic Analysis ◽

Rna Seq

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Inflammation, necrosis, and the kinase RIP3 are key mediators of AAG-dependent alkylation-induced retinal degeneration

Science Signaling ◽

10.1126/scisignal.aau9216 ◽

2019 ◽

Vol 12 (568) ◽

pp. eaau9216 ◽

Cited By ~ 3

Author(s):

Mariacarmela Allocca ◽

Joshua J. Corrigan ◽

Aprotim Mazumder ◽

Kimberly R. Fake ◽

Leona D. Samson

Keyword(s):

Cell Death ◽

Programmed Cell Death ◽

Retinal Degeneration ◽

Excision Repair ◽

Alkylating Agents ◽

Death Process ◽

Partial Protection ◽

Cell Death Process ◽

Base Excision ◽

Damage Marker

DNA-alkylating agents are commonly used to kill cancer cells, but the base excision repair (BER) pathway they trigger can also produce toxic intermediates that cause tissue damage, such as retinal degeneration (RD). Apoptosis, a process of programmed cell death, is assumed to be the main mechanism of this alkylation-induced photoreceptor (PR) cell death in RD. Here, we studied the involvement of necroptosis (another programmed cell death process) and inflammation in alkylation-induced RD. Male mice exposed to a methylating agent exhibited a reduced number of PR cell rows, active gliosis, and cytokine induction and macrophage infiltration in the retina. Dying PRs exhibited a necrotic morphology, increased 8-hydroxyguanosine abundance (an oxidative damage marker), and overexpression of the necroptosis-associated genes Rip1 and Rip3. The activity of PARP1, which mediates BER, cell death, and inflammation, was increased in PR cells and associated with the release of proinflammatory chemokine HMGB1 from PR nuclei. Mice lacking the anti-inflammatory cytokine IL-10 exhibited more severe RD, whereas deficiency of RIP3 (also known as RIPK3) conferred partial protection. Female mice were partially protected from alkylation-induced RD, showing reduced necroptosis and inflammation compared to males. PRs in mice lacking the BER-initiating DNA glycosylase AAG did not exhibit alkylation-induced necroptosis or inflammation. Our findings show that AAG-initiated BER at alkylated DNA bases induces sex-dependent RD primarily by triggering necroptosis and activating an inflammatory response that amplifies the original damage and, furthermore, reveal new potential targets to prevent this side effect of chemotherapy.

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