The RGSGR amino acid motif of the intercellular signalling protein, HetN, is required for patterning of heterocysts in <i>Anabaena</i> sp. strain PCC 7120

Higa, Kelly; Rajagopalan, Ramya; Risser, Douglas D.; Rivers, Orion S.; Tom, Sasa K.; Videau, Patrick; Callahan, Sean M.

doi:10.1111/j.1365-2958.2011.07949.x

Cited by 50 publications

(88 citation statements)

References 38 publications

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“…Other members of this group include HetN, a protein of unknown function required for heterocyst differentiation in Anabaena and Nostoc (Black and Wolk 1994;Liu and Chen 2009) and NodG, which is essential for nodulation of legumes by Rhizobium (LopezLara and Geiger 2001). Interestingly, HetN contains a signaling motif separate from its catalytic site (Higa et al 2012) that is not conserved in other homologs. The second clade contains enzymes annotated as hydroxysteroid dehydrogenases in humans, Comamonas, and Streptomyces, including HSD10.…”

Section: Oxidation Is a Widespread Scad Activitymentioning

confidence: 99%

Myxococcus CsgA, Drosophila Sniffer, and human HSD10 are cardiolipin phospholipases

Boynton

Shimkets

2015

Genes Dev.

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Myxococcus xanthus development requires CsgA, a member of the short-chain alcohol dehydrogenase (SCAD) family of proteins. We show that CsgA and SocA, a protein that can replace CsgA function in vivo, oxidize the 2 ′ -OH glycerol moiety on cardiolipin and phosphatidylglycerol to produce diacylglycerol (DAG), dihydroxyacetone, and orthophosphate. A lipid extract enriched in DAGs from wild-type cells initiates development and lipid body production in a csgA mutant to bypass the mutational block. This novel phospholipase C-like reaction is widespread. SCADs that prevent neurodegenerative disorders, such as Drosophila Sniffer and human HSD10, oxidize cardiolipin with similar kinetic parameters. HSD10 exhibits a strong preference for cardiolipin with oxidized fatty acids. This activity is inhibited in the presence of the amyloid β peptide. Three HSD10 variants associated with neurodegenerative disorders are inactive with cardiolipin. We suggest that HSD10 protects humans from reactive oxygen species by removing damaged cardiolipin before it induces apoptosis.

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Section: Oxidation Is a Widespread Scad Activitymentioning

confidence: 99%

Myxococcus CsgA, Drosophila Sniffer, and human HSD10 are cardiolipin phospholipases

Boynton

Shimkets

2015

Genes Dev.

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“…The heterocysts appear in a nonrandom spacing of approximately 1 heterocyst to every 10-15 vegetative cells. The activator-inhibitor system governing this patterning consists of a self-enhancing activator protein, HetR (8,9), and its antagonist, proteins containing a pentapeptide, PatS-5 (RGSGR) (10,11). These two primary positive and negative acting regulatory elements are modulated by several other elements (5,6,12,13).…”

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confidence: 99%

Biased inheritance of the protein PatN frees vegetative cells to initiate patterned heterocyst differentiation

Risser

Wong

Meeks

2012

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

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Heterocysts, cells specialized for nitrogen fixation in certain filamentous cyanobacteria, appear singly in a nonrandom spacing pattern along the chain of vegetative cells. A two-stage, biased initiation and competitive resolution model has been proposed to explain the establishment of this spacing pattern. There is substantial evidence that competitive resolution of a subset of cells initiating differentiation occurs by interactions between a selfenhancing activator protein, HetR, and a diffusible pentapeptide inhibitor PatS-5 (RGSGR). Results presented here show that the absence of a unique membrane protein, PatN, in Nostoc punctiforme strain ATCC 29133 leads to a threefold increase in heterocyst frequency and a fourfold decrease in the vegetative cell interval between heterocysts. A PatN-GFP translational fusion shows a pattern of biased inheritance in daughter vegetative cells of ammonium-grown cultures. Inactivation of another heterocyst patterning gene, patA, is epistatic to inactivation of patN, and transcription of patA increases in a patN-deletion strain, implying that patN may function by modulating levels of patA. The presence of PatN is hypothesized to decrease the competency of a vegetative cell to initiate heterocyst differentiation, and the cellular concentration of PatN is dependent on cell division that results in cells transiently depleted of PatN. We suggest that biased inheritance of cell-fate determinants is a phylogenetic domain-spanning paradigm in the development of biological patterns.activator-inhibitor | pattern differentiation T wo broad strategies used in the development of biological patterns are activator-inhibitor systems, a refinement of Turing-type reaction-diffusion systems (1, 2), and differential inheritance of cell fate determinants (3, 4). These strategies have been analyzed in multicellular eukaryotes ranging in developmental complexity from hydra to vertebrates (1, 4). Some filamentous cyanobacteria show spaced patterns of differentiated cells, such as nitrogen-fixing heterocysts and spore-like akinetes, thereby representing the simplest and oldest evolutionary model for study of the development of biological patterns and multicellular interactions. There is strong experimental evidence that an activatorinhibitor system regulates heterocyst patterning in filamentous cyanobacteria (5-7). We report here the characteristics of a gene (patN) that is required for normal heterocyst patterning, and the phenotype and protein localization of which is consistent with a role in the biased initiation of heterocyst differentiation via biased inheritance.Heterocysts terminally differentiate from vegetative cells in response to limitation of combined nitrogen. The heterocysts appear in a nonrandom spacing of approximately 1 heterocyst to every 10-15 vegetative cells. The activator-inhibitor system governing this patterning consists of a self-enhancing activator protein, HetR (8, 9), and its antagonist, proteins containing a pentapeptide, PatS-5 (RGSGR) (10, 11). These two primary positi...

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“…In the Anabaena system, HetR is an autocatalytic activator of differentiation that binds DNA (Black et al, 1993;Huang et al, 2004;Kim et al, 2013). PatS and HetN are inhibitors of differentiation that both contain a pentapeptide motif that likely interacts with HetR directly to signal it for degradation (Feldmann et al, 2012;Higa et al, 2012;Risser & Callahan, 2009;Yoon & Golden, 1998). The interplay between HetR, PatS and HetN is required for periodic pattern formation and heterocyst development.…”

Section: Discussionmentioning

confidence: 99%

“…The petE promoter region was amplified by PCR from chromosomal DNA with the primers PpetESacI-F and PpetE-EcoRI-SmaI-BamHI-R. The product was cloned as a SacI-BamHI fragment into the same sites of pSMC187 (Higa et al, 2012).…”

Section: Methodsmentioning

confidence: 99%

Transcriptional dynamics of developmental genes assessed with an FMN-dependent fluorophore in mature heterocysts of Anabaena sp. strain PCC 7120

et al. 2014

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Anabaena sp. strain PCC 7120 is a filamentous cyanobacterium that differentiates nitrogen-fixing heterocysts when available combined nitrogen is limiting. Growth under diazotrophic conditions results in a mixture of 'new' (recently differentiated) and 'old' (mature) heterocysts. The microoxic environment present in heterocysts makes the interpretation of gene expression using oxygen-dependent fluorophores, including GFP, difficult. The work presented here evaluates the transcriptional dynamics of three developmental genes in mature heterocysts utilizing EcFbFP, a flavin mononucleotide-dependent fluorophore, as the reporter. Expression of both GFP and EcFbFP from the heterologous petE promoter showed that, although GFP and EcFbFP fluoresced in both vegetative cells and new heterocysts, only EcFbFP fluoresced in old heterocysts. A transcriptional fusion of EcFbFP to the late-stage heterocyst-specific nifB promoter displayed continued expression beyond the cessation of GFP fluorescence in heterocysts. Promoter fusions of the master regulator of differentiation, hetR, and its inhibitors, patS and hetN, to GFP and EcFbFP were visualized to determine their role(s) in heterocyst function after morphogenesis. The expression of hetR and hetN was found to persist beyond the completion of development in most heterocysts, whereas patS expression ceased. These data are consistent with a model of heterocyst patterning in which patS is involved in de novo pattern formation, hetN is required for pattern maintenance, and hetR is needed for all stages of development.

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The RGSGR amino acid motif of the intercellular signalling protein, HetN, is required for patterning of heterocysts in Anabaena sp. strain PCC 7120

Cited by 50 publications

References 38 publications

Myxococcus CsgA, Drosophila Sniffer, and human HSD10 are cardiolipin phospholipases

Myxococcus CsgA, Drosophila Sniffer, and human HSD10 are cardiolipin phospholipases

Biased inheritance of the protein PatN frees vegetative cells to initiate patterned heterocyst differentiation

Transcriptional dynamics of developmental genes assessed with an FMN-dependent fluorophore in mature heterocysts of Anabaena sp. strain PCC 7120

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