A novel cyclic AMP metabolism exhibited by giant cells and its possible role in the sexual development of Dictyostelium discoideum

Abe, Kuniya; Orii, Hidefumi; Okada, Yoshinori; Saga, Yukika; Yanagisawa, Keiji

doi:10.1016/0012-1606(84)90104-0

Cited by 29 publications

(12 citation statements)

References 35 publications

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“…However, this difference was more likely due to differences not only in the experimental design but also in the employed cell densities which were 100‐fold different in the two experiments [5‐10 7 cells ml −1 with 5 × 10 5 giant cells ml −1 below the dialysis membrane in Lamphier & Yanagisawa (1983); 2–4 × 10 5 cells ml −1 total in mixed‐mating culture in O’Day (1979)]. The case was settled by Abe et al (1984) who demonstrated that giant cells secrete cAMP in equivalent amounts to asexual aggregating cells but differ in that they express low levels of membrane‐bound phosphodiesterase (PDE) activity while simultaneously secreting a PDE inhibitor. Together these changes in cAMP metabolism ensure that the ZGC is at the centre of the cAMP gradient.…”

Section: Heterothallic Sexual Development Of Dictyostelium Discoimentioning

confidence: 99%

Signalling and sex in the social amoebozoans

O’Day

Keszei

2011

Biological Reviews

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The social amoebozoans have a life tricycle consisting of asexual multicellular development leading to fruiting bodies, sexual multicellular development resulting in macrocysts, and unicellular development generating microcysts. This review covers the events of sexual development in the best-studied heterothallic (Dictyostelium discoideum) and homothallic (D. mucoroides) mating systems. Sexual development begins with pheromonal interactions that produce fusion-competent cells (gametes) which undergo cell and pronuclear fusion. Calcium- and calmodulin-mediated signalling mediates these early events. As they initiate chemotactic signalling, each zygote increases in size becoming a zygote giant cell. Using cyclic AMP (cAMP), the zygote chemotactically lures in amoebae and engulfs them in an act of cannibalistic phagocytosis. Chemotaxis proceeds more quickly than endocytosis because the breakdown products of cAMP (5-AMP, adenosine) bind to a presumptive adenosine receptor to inhibit sexual phagocytosis. This slowing of phagocytosis allows amoebae to accumulate around the zygote to form a precyst aggregate. Zygote giant cells also produce several other signalling molecules that feed back to regulate early events. The amoebae surrounding the zygote seal their fate as zygotic foodstuff by secreting a primary cellulose wall, the extracellular sheath, around the zygote and aggregated amoebae, which prevents their escape. Phagocytosis within this precyst continues until all peripheral amoebae are internalized as endocytes and the final macrocyst wall is formed. Endocyte digestion results in a mature macrocyst with a uniform cytoplasm containing a diploid nucleus. After detailing the morphological events of heterothallic and homothallic mating, we review the various intercellular signalling events and other mechanisms involved in each stage. This complete and comprehensive review sets the stage for future research on the unique events that characterize sex in the social amoebozoans.

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Section: Heterothallic Sexual Development Of Dictyostelium Discoimentioning

confidence: 99%

Signalling and sex in the social amoebozoans

O’Day

Keszei

2011

Biological Reviews

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“…cAMP appears to be also involved in sexual development (20). cAMP, the first chemical discovered to function as a developmental signal in D. discoideum, was originally identified as a chemoattractant of aggregating amoebae.…”

Section: Overview Of Dictyostelium Developmentmentioning

confidence: 99%

CYCLIC AMP AND OTHER SIGNALS CONTROLLING CELL DEVELOPMENT AND DIFFERENTIATION IN DICTYOSTELIUM

Gerisch¹

1987

Annu. Rev. Biochem.

234

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“…However, it is also suspected that distinct molecular mechanisms are in operation from morphological dissimilarities, as the lack of aggregation streams in sexual cell aggregation (O'Day, 1979). This dissimilarity can be explained by the fact that giant cells in the aggregation centers secrete much higher levels of cAMP and phosphodiesterase inhibitor, and that scarce or no phosphodiesterase activity is detected during the sexual process (Abe et al, 1984). Common and differential usage of the gene repertoire for alternative developmental modes is an important tactic for the organism, and how it is achieved will be an intriguing subject for future analysis.…”

Section: Discussionmentioning

confidence: 95%

“…As to the molecular basis of zygote development, it is known that cell aggregation toward the zygote giant cells is achieved by a cAMP-mediated chemotactic system (O'Day, 1979;O'Day and Durston, 1979;Abe et al, 1984), which partly recruits the signaling system used for asexual development (Shimizu et al, 1997). Our previous studies on sexual cell fusion demonstrated the involvement of several cell surface glycoproteins (Urushihara, 1992) and the existence of protease sensitive inhibitors on the cell surface (Urushihara and Aiba, 1996).…”

Section: Introductionmentioning

confidence: 98%

Reverse genetic analyses of gamete-enriched genes revealed a novel regulator of the cAMP signaling pathway in Dictyostelium discoideum

Muramoto

Takeda

Furuya

et al. 2005

Mechanisms of Development

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Sexual development in Dictyostelium discoideum is initiated by the fusion of opposite mating type cells to form zygote giant cells, which subsequently gather and phagocytose surrounding cells for nutrition to form macrocysts. Here we performed the targeting of 24 highly gamete-enriched genes we previously isolated, and successfully generated knockout mutants for 16 genes and RNAi mutants for 20 genes including 6 genes without disruptants. In the knockout mutants of two genes, cell aggregation toward the giant cells was much less extensive and many cells remained around poorly formed macrocysts. We named these genes tmcB and tmcC. Although macrocyst formation of wild type cells was suppressed by the addition of exogenous cAMP, that of knockout mutants of tmcB was much less sensitive. The mRNA level of phosphodiesterase (pde) was higher and that of its inhibitor (pdi) was lower in the latter cells compared to the parental strains during sexual development. Thus, tmcB appeared to be a novel regulator of the cAMP signaling pathway specific to sexual development. Knockout mutants of tmcC were indistinguishable from the wild type cells with respect to the cAMP response, suggesting that this gene is relevant to other processes.

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A novel cyclic AMP metabolism exhibited by giant cells and its possible role in the sexual development of Dictyostelium discoideum

Cited by 29 publications

References 35 publications

Signalling and sex in the social amoebozoans

Signalling and sex in the social amoebozoans

CYCLIC AMP AND OTHER SIGNALS CONTROLLING CELL DEVELOPMENT AND DIFFERENTIATION IN DICTYOSTELIUM

Reverse genetic analyses of gamete-enriched genes revealed a novel regulator of the cAMP signaling pathway in Dictyostelium discoideum

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