Activation of extracellular signal-regulated kinases during dehydration in the African clawed frog, <i>Xenopus laevis</i>

Malik, Amal; Storey, Kenneth B.

doi:10.1242/jeb.030627

Cited by 47 publications

(78 citation statements)

References 35 publications

(53 reference statements)

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“…Dehydration also enhanced ERK signaling in most other X. laevis tissues, implicating the ERK pathway as a key mediator of cellular responses to low water stress with consequences for both gene expression and reversible control of enzymes and other proteins (Malik and Storey, 2009a). Significantly, this role now appears to be universal because new work on both mammalian embryonic kidney cells and C. elegans shows a conserved activation of the ERK pathway in response to desiccation and inhibition of desiccation early response genes by an ERK inhibitor (Huang et al, 2010).…”

Section: Otala Lacteamentioning

confidence: 93%

“…Although almost exclusively aquatic, in their native environment in southern Africa this species is faced with seasonal drying of its ponds and responds in one of two ways: (1) by nocturnal overland migration to a new water source or (2) by digging into the cooler, damper subsoil of their evaporating pond and entering aestivation (Alexander & Bellerby, 1938). These frogs can endure substantial desiccation (losing as much as 32-35% of total body water) (Romspert, 1975;Malik and Storey, 2009a) and under dehydration stress they elevate the production of nitrogenous osmolytes including amino acids, ammonia (twofold to threefold increase) and urea (15-to 20-fold increase) to enhance water retention and/or uptake from damp soil (Balinsky et al, 1967).…”

Section: Otala Lacteamentioning

confidence: 99%

“…Responses to whole-body dehydration by the extracellular signal-regulated kinase (ERK) signaling cascade (one member of the MAPK superfamily) in X. laevis illustrate this idea. Fig.2 shows the coordinated responses by ERK family members in lung of X. laevis challenged by medium and high levels of dehydration (Malik and Storey, 2009a). Dehydration resulted in elevated levels of phosphorylated active kinases in all three tiers of the MAPK cascade: the initiating MAPK kinase kinases (c-Raf and MEKK), the MAPK kinase (MEK1/2) and finally the MAPK (ERK1/2).…”

Section: Otala Lacteamentioning

confidence: 99%

“…Different letters indicate a significant difference (P<0.05) from the control value (a) or the medium dehydration value (b). Compiled from Malik and Storey (Malik and Storey, 2009a). Photo credit: J.M.S.…”

Section: Otala Lacteamentioning

confidence: 99%

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Aestivation: signaling and hypometabolism

Storey

2012

Journal of Experimental Biology

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137

116

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SummaryAestivation is a survival strategy used by many vertebrates and invertebrates to endure arid environmental conditions. Key features of aestivation include strong metabolic rate suppression, strategies to retain body water, conservation of energy and body fuel reserves, altered nitrogen metabolism, and mechanisms to preserve and stabilize organs, cells and macromolecules over many weeks or months of dormancy. Cell signaling is crucial to achieving both a hypometabolic state and reorganizing multiple metabolic pathways to optimize long-term viability during aestivation. This commentary examines the current knowledge about cell signaling pathways that participate in regulating aestivation, including signaling cascades mediated by the AMPactivated kinase, Akt, ERK, and FoxO1.

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Section: Otala Lacteamentioning

confidence: 93%

Section: Otala Lacteamentioning

confidence: 99%

Section: Otala Lacteamentioning

confidence: 99%

Section: Otala Lacteamentioning

confidence: 99%

See 2 more Smart Citations

Aestivation: signaling and hypometabolism

Storey

2012

Journal of Experimental Biology

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137

116

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“…Although ERKs are involved in many different cell functions, activation of the ERK cascade was shown in different tissues of aestivating X. laevis, where it is likely to be involved in coordinating the appropriate responses to ameliorate cell stress, for example dehydration (Malik and Storey, 2009). Additonally, there was a large increase in gene expression of an MLT-like mitogen-activated protein kinase kinase kinase in aestivating frog muscle (Reilly et al, 2013) (Chapter 2).…”

Section: Dormancy In Cancer Cellsmentioning

confidence: 99%

Mechanisms underlying inhibition of muscle disuse atrophy during aestivation in the green-striped burrowing frog, Cyclorana alboguttata

Reilly¹

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In most mammals, extended inactivity or immobilisation of skeletal muscle (e.g. bedrest, limb-casting or hindlimb unloading) results in muscle disuse atrophy, a process which is characterised by the loss of skeletal muscle mass and function. In stark contrast, animals that experience natural bouts of prolonged muscle inactivity, such as hibernating mammals and aestivating frogs, consistently exhibit limited or no change in either skeletal muscle size or contractile performance. While many of the factors regulating skeletal muscle mass are known, little information exists as to what mechanisms protect against muscle atrophy in some species.Green-striped burrowing frogs (Cyclorana alboguttata) survive in arid environments by burrowing underground and entering into a deep, prolonged metabolic depression known as aestivation. Throughout aestivation, C. alboguttata is immobilised within a cast-like cocoon of shed skin and ceases feeding and moving. Remarkably, these frogs exhibit very little muscle atrophy despite extended disuse and fasting. The overall aim of the current research study was to gain a better understanding of the physiological, cellular and molecular basis underlying resistance to muscle disuse atrophy in C. alboguttata.The first aim of this study was to develop a genomic resource for C. alboguttata by sequencing and functionally characterising its skeletal muscle transcriptome, and to conduct gene expression profiling to identify transcriptional pathways associated with metabolic depression and maintenance of muscle function in aestivating burrowing frogs. A transcriptome was assembled using next-generation short read sequencing followed by a comparison of gene expression patterns between active and four-month aestivating C.alboguttata. This identified a complex suite of gene expression changes that occur in muscle during aestivation and provides evidence that aestivation in burrowing frogs involves transcriptional regulation of genes associated with cytoskeletal remodelling, avoidance of oxidative stress, energy metabolism, the cell stress response, cell death and survival and epigenetic modification. In particular, the expression levels of genes encoding cell cycle regulatory-, pro-survival and chromatin remodelling proteins, such as serine/threonine-protein kinase Chk1, cell division protein kinase 2, survivin, vesicular overexpressed in cancer prosurvival protein 1 and histone-binding protein RBBP4, were upregulated in aestivators.The second aim of this study was to examine the potential role of mitochondrial ROS in the regulation of muscle mass and function during aestivation in C. alboguttata. In III mammals, muscle disuse atrophy has been associated with oxidative damage due to increased mitochondrial ROS production. C. alboguttata reduced skeletal muscle mitochondrial respiration by approximately 50% following four months of aestivation, while mitochondrial ROS production was more than 80% lower in aestivating skeletal muscle relative to controls when mitochondrial substrates were pre...

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Identification of a novel dehydration responsive gene, drp10, from the African clawed frog, Xenopus laevis

Biggar

Storey

2015

J. Exp. Zool.

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During periods of environmental stress a number of different anuran species employ adaptive strategies to promote survival. Our study found that in response to dehydration (i.e., loss of total body water content), the African clawed frog (Xenopus laevis) increased the expression of a novel gene (drp10) that encodes a structural homolog of the freeze-responsive FR10 protein found in wood frogs. Similar to FR10, the DRP10 protein was found to also contain a highly conserved N-terminal cleavable signal peptide. Furthermore, DRP10 was found to have high structural homology to the available crystal structures of type A and E apolipoproteins in Homo sapiens, and a type IV LS-12 anti-freeze protein in the longhorn sculpin, Myoxocephalus octodecemspinosis. In response to dehydration, the transcript expression of drp10 was found to increase 1.52 ± 0.16-fold and 1.97 ± 0.11-fold in response to medium (15%) and high (30%) dehydration stresses in the liver tissue of X. laevis, respectively, while drp10 expression increased 2.12 ± 0.12-fold and 1.46 ± 0.16-fold in kidney tissue. Although the molecular function of both dehydration-responsive DRP10 and the freeze-responsive FR10 have just begun to be elucidated, it is likely that both are frog-specific proteins that likely share a similar purpose during water-related stresses.

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Activation of extracellular signal-regulated kinases during dehydration in the African clawed frog, Xenopus laevis

Abstract: SUMMARY

Cited by 47 publications

References 35 publications

Aestivation: signaling and hypometabolism

Aestivation: signaling and hypometabolism

Mechanisms underlying inhibition of muscle disuse atrophy during aestivation in the green-striped burrowing frog, Cyclorana alboguttata

Identification of a novel dehydration responsive gene, drp10, from the African clawed frog, Xenopus laevis

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