c-di-GMP induction of<i>Dictyostelium</i>cell death requires the polyketide DIF-1

Yu, Shuangni; Luciani, Marie‐Françoise; Giusti, Corinne; Golstein, Pierre

doi:10.1091/mbc.e14-08-1337

Cited by 11 publications

(22 citation statements)

References 39 publications

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“…Recent studies found strongly reduced c-di-GMP induction of the vacuolated stalk/basal disk cell type in stlb− and dmta− mutants in vitro (12). We show that stalk gene transcription in stlb− and dmta− mutants in vitro required 10-fold higher c-di-GMP concentrations than in wild-type cells (Fig.…”

Section: Discussionsupporting

confidence: 58%

Adenylate cyclase A acting on PKA mediates induction of stalk formation by cyclic diguanylate at the Dictyostelium organizer

Chen

Singh

Callebaut

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Coordination of cell movement with cell differentiation is a major feat of embryonic development. The Dictyostelium stalk always forms at the organizing tip, by a mechanism that is not understood. We previously reported that cyclic diguanylate (c-di-GMP), synthesized by diguanylate cyclase A (DgcA), induces stalk formation. Here we used transcriptional profiling of dgca− structures to identify target genes for c-di-GMP, and used these genes to investigate the c-di-GMP signal transduction pathway. We found that knockdown of cAMP-dependent protein kinase (PKA) activity in prestalk cells reduced stalk gene induction by c-di-GMP, whereas PKA activation bypassed the c-di-GMP requirement for stalk gene expression. c-di-GMP caused a persistent increase in cAMP, which still occurred in mutants lacking the adenylate cyclases ACG or ACR, or the cAMP phosphodiesterase RegA. However, both inhibition of adenylate cyclase A (ACA) with SQ22536 and incubation of a temperature-sensitive ACA mutant at the restrictive temperature prevented c-di-GMP–induced cAMP synthesis as well as c-di-GMP–induced stalk gene transcription. ACA produces the cAMP pulses that coordinate Dictyostelium morphogenetic cell movement and is highly expressed at the organizing tip. The stalk-less dgca− mutant regained its stalk by expression of a light-activated adenylate cyclase from the ACA promoter and exposure to light, indicating that cAMP is also the intermediate for c-di-GMP in vivo. Our data show that the more widely expressed DgcA activates tip-expressed ACA, which then acts on PKA to induce stalk genes. These results explain why stalk formation in Dictyostelia always initiates at the site of the morphogenetic organizer.

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Section: Discussionsupporting

confidence: 58%

Adenylate cyclase A acting on PKA mediates induction of stalk formation by cyclic diguanylate at the Dictyostelium organizer

Chen

Singh

Callebaut

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…164,165 c-di-GMP is a universal bacterial second messenger 166 and can trigger innate immunity in bacterially-infected animal cells. 167 Unexpectedly, experiments using both inducers show marked synergy, 168 although c-di-GMP alone is insufficient to induce cell death in D. discoideum cell monolayers, requiring either DIF-1 or a DIF-1-related polyketide. The required DIF-1 can be endogenous, as shown by the inability of c-di-GMP to induce cell death when DIF-1 synthesis was blocked pharmacologically (by cerulenin), and by its rescue upon complementation by exogenous DIF-1.…”

Section: Autophagy and Cell Death Pathways In D Discoideummentioning

confidence: 99%

Autophagy inDictyostelium: Mechanisms, regulation and disease in a simple biomedical model

et al. 2016

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Autophagy is a fast-moving field with an enormous impact on human health and disease. Understanding the complexity of the mechanism and regulation of this process often benefits from the use of simple experimental models such as the social amoeba Dictyostelium discoideum. Since the publication of the first review describing the potential of D. discoideum in autophagy, significant advances have been made that demonstrate both the experimental advantages and interest in using this model. Since our previous review, research in D. discoideum has shed light on the mechanisms that regulate autophagosome formation and contributed significantly to the study of autophagy-related pathologies. Here, we review these advances, as well as the current techniques to monitor autophagy in D. discoideum. The comprehensive bioinformatics search of autophagic proteins that was a substantial part of the previous review has not been revisited here except for those aspects that challenged previous predictions such as the composition of the Atg1 complex. In recent years our understanding of, and ability to investigate, autophagy in D. discoideum has evolved significantly and will surely enable and accelerate future research using this model.

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“…). Cells in clumps were also primed to respond to the second exogenous signal (DIF‐1, or as shown more recently c‐di‐GMP ), which led to vacuolization and cellulose encasings . Thus, the latter prominent hallmarks of developmental cell death were induced separately from and after initial cell dysfunction ( Fig.…”

Section: Dictyostelium Cell Death Shows Early Nucleolar Disorganizationmentioning

confidence: 77%

Conserved nucleolar stress at the onset of cell death

Golstein

2017

The FEBS Journal

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Cell death pervasiveness among multicellular eukaryotes suggested that some core steps of cell death may be conserved. This could be addressed by comparing the course of cell death in organisms belonging to distinct eukaryotic kingdoms. A search for early cell death events in a protist revealed nucleolar disorganization similar to the nucleolar stress often reported in dying animal cells. This indicated a conserved role for the nucleolus at the onset of eukaryotic cell death and leads one to consider the course of cell death as a succession of unequally conserved modules.

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c-di-GMP induction ofDictyosteliumcell death requires the polyketide DIF-1

Cited by 11 publications

References 39 publications

Adenylate cyclase A acting on PKA mediates induction of stalk formation by cyclic diguanylate at the Dictyostelium organizer

Adenylate cyclase A acting on PKA mediates induction of stalk formation by cyclic diguanylate at the Dictyostelium organizer

Autophagy inDictyostelium: Mechanisms, regulation and disease in a simple biomedical model

Conserved nucleolar stress at the onset of cell death

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