Expression of the Cameleon calcium biosensor in fungi reveals distinct Ca2+ signatures associated with polarized growth, development, and pathogenesis

Kim, Hye Seon; Czymmek, Kirk J.; Patel, Aashay; Modla, Shannon; Nohe, Anja; Duncan, Randall L.; Gilroy, Simon; Kang, Seogchan

doi:10.1016/j.fgb.2012.05.011

Cited by 43 publications

(41 citation statements)

References 90 publications

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“…Further species-specific responses are evident in differences of stress stimuli and in the production of secondary metabolites. The species specificity can be explained if we assume that, although the Ca 2ϩ signaling pathway is well conserved for executing organism-specific cellular and developmental responses to specific ecological niches, it has probably undergone evolutionary fine-tuning (43). The unique Ca 2ϩ signatures of different species support this hypothesis (43).…”

Section: Phenotypic Consequences Of Crz1 Dysfunctionmentioning

confidence: 94%

“…Recent studies in filamentous fungi have shown that the intracellular Ca 2ϩ concentration changes in a pulsatile manner and that each species exhibits a distinct Ca 2ϩ signature which is also growth dependent (43). Such Ca 2ϩ oscillations have already been known for a long time in D. discoideum (44) and in various cell lines (reviewed in reference 45).…”

Section: Camentioning

confidence: 98%

“…Nevertheless, the initial response of the yeast cells after Crz1 activation is proportional to the strength of the external signal (Ca 2ϩ concentration and light intensity, respectively) (34,40). In filamentous fungi, it has been shown that the cytoplasmic calcium concentration oscillates in a species-, growth phase-, and treatment-dependent manner (42,43). Cell type-specific cytosolic calcium oscillations have also been observed in mammalian cells and during differentiation of D. discoideum (44,45).…”

Section: The Calcineurin-crz1 Signaling Cascadementioning

confidence: 99%

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Calcineurin-Crz1 Signaling in Lower Eukaryotes

2014

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Calcium ions are ubiquitous intracellular messengers. An increase in the cytosolic Ca 2؉ concentration activates many proteins, including calmodulin and the Ca 2؉ /calmodulin-dependent protein phosphatase calcineurin. The phosphatase is conserved from yeast to humans (except in plants), and many target proteins of calcineurin have been identified. The most prominent and bestinvestigated targets, however, are the transcription factors NFAT (nuclear factor of activated T cells) in mammals and Crz1 (calcineurin-responsive zinc finger 1) in yeast. In recent years, many orthologues of Crz1 have been identified and characterized in various species of fungi, amoebae, and other lower eukaryotes. It has been shown that the functions of calcineurin-Crz1 signaling, ranging from ion homeostasis through cell wall biogenesis to the building of filamentous structures, are conserved in the different organisms. Furthermore, frequency-modulated gene expression through Crz1 has been discovered as a striking new mechanism by which cells can coordinate their response to a signal. In this review, I focus on the latest findings concerning calcineurin-Crz1 signaling in fungi, amoebae and other lower eukaryotes. I discuss the potential of Crz1 and its orthologues as putative drug targets, and I also discuss possible parallels with calcineurin-NFAT signaling in mammals.

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Section: Phenotypic Consequences Of Crz1 Dysfunctionmentioning

confidence: 94%

Section: Camentioning

confidence: 98%

Section: The Calcineurin-crz1 Signaling Cascadementioning

confidence: 99%

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Calcineurin-Crz1 Signaling in Lower Eukaryotes

2014

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“…Oscillations of Ca 2ϩ levels have been observed at hyphal tips (82), and Ca 2ϩ levels have been proven to regulate actin assembly and vesicle fusion (83,84). This strongly suggests that the oscillatory rate of extension of hyphal tips involves a concerted action of Ca 2ϩ , actin, and exocytosis.…”

Section: Positional Information For Growth: Cell End Markers the Polmentioning

confidence: 98%

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Riquelme

Aguirre

Bartnicki-García

et al. 2018

Microbiol Mol Biol Rev

289

246

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SUMMARYFilamentous fungi constitute a large group of eukaryotic microorganisms that grow by forming simple tube-like hyphae that are capable of differentiating into more-complex morphological structures and distinct cell types. Hyphae form filamentous networks by extending at their tips while branching in subapical regions. Rapid tip elongation requires massive membrane insertion and extension of the rigid chitin-containing cell wall. This process is sustained by a continuous flow of secretory vesicles that depends on the coordinated action of the microtubule and actin cytoskeletons and the corresponding motors and associated proteins. Vesicles transport cell wall-synthesizing enzymes and accumulate in a special structure, the Spitzenkörper, before traveling further and fusing with the tip membrane. The place of vesicle fusion and growth direction are enabled and defined by the position of the Spitzenkörper, the so-called cell end markers, and other proteins involved in the exocytic process. Also important for tip extension is membrane recycling by endocytosis via early endosomes, which function as multipurpose transport vehicles for mRNA, septins, ribosomes, and peroxisomes. Cell integrity, hyphal branching, and morphogenesis are all processes that are largely dependent on vesicle and cytoskeleton dynamics. When hyphae differentiate structures for asexual or sexual reproduction or to mediate interspecies interactions, the hyphal basic cellular machinery may be reprogrammed through the synthesis of new proteins and/or the modification of protein activity. Although some transcriptional networks involved in such reprogramming of hyphae are well studied in several model filamentous fungi, clear connections between these networks and known determinants of hyphal morphogenesis are yet to be established.

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“…The A. fumigatus ahpA ortholog, htfA (Afu4g10110), is expressed at higher levels, particularly during early growth, in a calAD (Afu5g09360) calcineurin mutant, and is required for induction of putative transporters pmcA (Afu1g10880) and pmcB (Afu3g10690) in response to a Ca 2+ pulse (Malavazi et al 2009). Ca 2+ controls actin assembly and endocytosis rates in many organisms, and shows age-dependent oscillations at hyphal apices in filamentous fungi (Kim et al 2012), warranting future attention. PalH is a seven-transmembrane pH sensor required for proteolytic activation of transcription factor PacC (AN2855) under alkaline conditions (Negrete-Urtasun et al 1999), and pH homeostasis has recently emerged as a central signal regulating growth rate through Ras/PKA in S. cerevisiae (Dechant et al 2014).…”

Section: Transcriptional and Hyphal Differentiation During Developmentmentioning

confidence: 99%

A Plastic Vegetative Growth Threshold Governs Reproductive Capacity inAspergillus nidulans

et al. 2016

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Ontogenetic phases separating growth from reproduction are a common feature of cellular life. Long recognized for flowering plants and animals, early literature suggests this life-history component may also be prevalent among multicellular fungi. We establish the basis of developmental competence-the capacity to respond to induction of asexual development-in the filamentous saprotroph Aspergillus nidulans, describing environmental influences, including genotype-by-environment interactions among precocious mutants, gene expression associated with wild type and precocious competence acquisition, and the genetics of competence timing. Environmental effects are consistent with a threshold driven by metabolic rate and organism density, with pH playing a particularly strong role in determining competence timing. Gene expression diverges significantly over the competence window, despite a lack of overt morphological change, with differentiation in key metabolic, signaling, and cell trafficking processes. We identify five genes for which mutant alleles advance competence timing, including the conserved GTPase RasB (AN5832) and ambient pH sensor PalH (AN6886). In all cases examined, inheritance of competence timing is complex and non-Mendelian, with F 1 progeny showing highly variable transgressive timing and dominant parental effects with a weak contribution from progeny genotype. Competence provides a new model for nutrient-limited life-cycle phases, and their elaboration from unicellular origins. Further work is required to establish the hormonal and bioenergetic basis of the trait across fungi, and underlying mechanisms of variable inheritance.

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Expression of the Cameleon calcium biosensor in fungi reveals distinct Ca2+ signatures associated with polarized growth, development, and pathogenesis

Cited by 43 publications

References 90 publications

Calcineurin-Crz1 Signaling in Lower Eukaryotes

Calcineurin-Crz1 Signaling in Lower Eukaryotes

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

A Plastic Vegetative Growth Threshold Governs Reproductive Capacity inAspergillus nidulans

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