Function of Ammonium Transporter A in the Initiation of Culmination of Development in
            <i>Dictyostelium discoideum</i>

Singleton, Charles K.; Kirsten, Janet H.; Dinsmore, Colin J.

doi:10.1128/ec.00058-06

Cited by 28 publications

(32 citation statements)

References 34 publications

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“…We confirmed the results of previous studies (62) showing that amtA Ϫ cells normally grow both in shaking culture and on bacterial plates and that the time courses of development in wild-type and amtA Ϫ cells are similar, differentiating into fruiting bodies in 24 h upon starvation (data not shown). Wild-type and amtA Ϫ cells show similar sensitivities to ammonia in culmination (Fig.…”

Section: Strainssupporting

confidence: 81%

“…3C, cells were developed in the absence of NH 4 Cl, and then different amounts of NH 4 Cl were added to pads for further development. In addition, amtA (62). We also found that amtA Ϫ cells show smaller aggregation territory sizes and frequent group breakup (Fig.…”

Section: Strainsmentioning

confidence: 55%

“…Previous studies have shown that developmental phenotypes in cells lacking AmtC can be rescued by deleting the AmtA protein (62). These studies suggest that AmtC and AmtA antagonistically regulate developmental processes and that AmtA and AmtC function in either ammonium transport or ammonium sensing (20,37,62). In this study, we show that AmtA regulates intracellular ammonium/ammonia levels during growth and development and is critical for the morphogenesis of multicellular aggregates and normal spore formation.…”

mentioning

confidence: 55%

“…In addition, there are five genes, amtA, amtB, amtC, rhgA, and rhgB, which belong to the evolutionarily conserved family of ammonium transporter/methylammonium permease/rhesus protein (Amt/Mep/Rh) in the Dictyostelium genome (15). Previous studies have shown that developmental phenotypes in cells lacking AmtC can be rescued by deleting the AmtA protein (62). These studies suggest that AmtC and AmtA antagonistically regulate developmental processes and that AmtA and AmtC function in either ammonium transport or ammonium sensing (20,37,62).…”

mentioning

confidence: 99%

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Regulation of Ammonia Homeostasis by the Ammonium Transporter AmtA in Dictyostelium discoideum

et al. 2007

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Ammonia has been shown to function as a morphogen at multiple steps during the development of the cellular slime mold Dictyostelium discoideum; however, it is largely unknown how intracellular ammonia levels are controlled. In the Dictyostelium genome, there are five genes that encode putative ammonium transporters: amtA, amtB, amtC, rhgA, and rhgB. Here, we show that AmtA regulates ammonia homeostasis during growth and development. We found that cells lacking amtA had increased levels of ammonia/ammonium, whereas their extracellular ammonia/ ammonium levels were highly decreased. These results suggest that AmtA mediates the excretion of ammonium. In support of a role for AmtA in ammonia homeostasis, AmtA mRNA is expressed throughout the life cycle, and its expression level increases during development. Importantly, AmtA-mediated ammonia homeostasis is critical for many developmental processes. amtA ؊ cells are more sensitive to NH 4 Cl than wild-type cells in inhibition of chemotaxis toward cyclic AMP and of formation of multicellular aggregates. Furthermore, even in the absence of exogenously added ammonia, we found that amtA ؊ cells produced many small fruiting bodies and that the viability and germination of amtA ؊ spores were dramatically compromised. Taken together, our data clearly demonstrate that AmtA regulates ammonia homeostasis and plays important roles in multiple developmental processes in Dictyostelium.

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Section: Strainssupporting

confidence: 81%

Section: Strainsmentioning

confidence: 55%

mentioning

confidence: 55%

mentioning

confidence: 99%

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Regulation of Ammonia Homeostasis by the Ammonium Transporter AmtA in Dictyostelium discoideum

et al. 2007

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“…The slug-to-fruit switch, thought to be mediated by the anterior tip (Smith and Williams, 1980), is subject to regulation by NH 3 , light, O 2 and other external cues by mechanisms that involve at least ten genes (Schindler and Sussman, 1977;Newell et al, 1969;Sandona et al, 1995;Newell and Ross, 1982). Genetic and biochemical studies suggest that an NH 3 -sensor/transporter, 2-component His kinases (DhkA, DhkC and DhkK), a cAMP phosphodiesterase (RegA), protein kinase A, an E3(SCF FbxA )-Ub ligase, transcription factor-like proteins (STATa, STATc, CudA, MybC), and cytoplasmic red-ox proteins are involved in transducing the signals (Harwood et al, 1992;Mohanty et al, 2001;Kirsten et al, 2005;Singleton et al, 2006;Choi et al, 2006;Thomason et al, 2006). Culmination appears to be exquisitely O 2 -dependent in Dictyostelium, requiring O 2 at a level of greater than 10% (Sandona et al, 1995), whereas growth and early development are relatively normal, down to 2.5% (normoxia=21%).…”

Section: Introductionmentioning

confidence: 99%

Prolyl 4-hydroxylase-1 mediates O2 signaling during development ofDictyostelium

2007

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Development in multicellular organisms is subject to both environmental and internal signals. In Dictyostelium, starvation induces amoebae to form migratory slugs that translocate from subterranean areas to exposed sites, where they culminate to form sessile fruiting bodies. Culmination, thought to be regulated by anterior tip cells, is selectively suppressed by mild hypoxia by a mechanism that can be partially overridden by another environmental signal, overhead light, or genetic activation of protein kinase A. Dictyostelium expresses, in all cells, an O 2 -dependent prolyl 4-hydroxylase (P4H1) required for O-glycosylation of Skp1, a subunit of E3 SCF -Ub-ligases. P4H1-null cells differentiate the basic pre-stalk and pre-spore cell types but exhibit a selectively increased O 2 requirement for culmination, from ~12% to near or above ambient (21%) levels. Overexpression of P4H1 reduces the O 2 requirement to <5%. The requirement for P4H1 can be met by forced expression of the active enzyme in either pre-stalk (anterior) or pre-spore (posterior) cells, or replaced by protein kinase A activation or addition of small numbers of wild-type cells. P4H1-expressing cells accumulate at the anterior end, suggesting that P4H1 enables transcellular signaling by the tip. The evidence provides novel genetic support for the animal-derived O 2 -sensor model of prolyl 4-hydroxylase function, in an organism that lacks the canonical HIF␣ transcriptional factor subunit substrate target that is a feature of animal hypoxic signaling.

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Dictyostelium: Cell Sorting and Patterning

Weijer

Williams

2009

Encyclopedia of Life Sciences

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Multicellular development of the social amoeba Dictyostelium discoideum results from the chemotactic aggregation of single cells to form a fruiting body consisting of a stalk supporting a spore mass. The interplay of two extracellular signalling molecules, cAMP (cyclic adenosine monophosphate) and the chlorinated hexaphenone DIF‐1 (differentiation‐inducing factor 1), directs cellular differentiation, and cAMP is also the chemo‐attractant that orchestrates all of morphogenesis. Although this is a relatively unusual mode of pattern formation, most of the fundamental processes that typify development in higher organism are on display, and the genetic accessibility of the organism makes it a very powerful and relevant model system. It has proven particularly valuable for understanding the basic mechanism of chemotaxis and the role that chemotaxis can play in the morphogenesis of a multicellular structure. Key concepts: Dictyostelium cells aggregate by chemotaxis in response to propagating cAMP waves. cAMP waves propagate through cAMP relay, the ability of the cells to detect a small cAMP signal, synthesis and secrete cAMP in response and thus pass the cAMP signal on to their neighbours. Adaptation of the relay response ensures unidirectional wave propagation away from the centre. Chemotactic cell movement involves detection of a cAMP gradient across the length of the cell, resulting in a polarization of actin–myosin cytoskeletal dynamics and movement up the gradient. Multicellular morphogenesis, the arrangement of tissue in space and time, is controlled by the interplay of cAMP wave propagation and chemotaxis during all stages of development. Dictyostelium development is separated from cell division but a cell's fate can be biased by its cell cycle position when development starts. Prespore cells are formed in response to cAMP signalling. Differentiation of prestalk cells is induced by a small organic molecule, DIF, which is secreted by the prespore cells. This induction forms part of a feedback loop that controls the prestalk–prespore ratio. The tip‐organizer cells are a subset of the prestalk cells that differentiation in response to a high local cAMP concentation. Dictyostelium pattern formation occurs by the sorting out of differentiated cell types.

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Function of Ammonium Transporter A in the Initiation of Culmination of Development in Dictyostelium discoideum

Cited by 28 publications

References 34 publications

Regulation of Ammonia Homeostasis by the Ammonium Transporter AmtA in Dictyostelium discoideum

Regulation of Ammonia Homeostasis by the Ammonium Transporter AmtA in Dictyostelium discoideum

Prolyl 4-hydroxylase-1 mediates O2 signaling during development ofDictyostelium

Dictyostelium: Cell Sorting and Patterning

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