A role for inositol monophosphatase 1 (IMPA1) in salinity adaptation in the euryhaline eel (<i>Anguilla anguilla</i>)

Kalujnaia, Svetlana; McVee, Jill; Kasciukovic, Taciana; Stewart, Alan J.; Cramb, Gordon

doi:10.1096/fj.10-161000

Cited by 30 publications

(41 citation statements)

References 45 publications

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“…This is surprising given the fact that the synthesis of myo-inositol phosphate from G-6-P is the more rate-limiting step of the MIB pathway (Majumder et al, 1997), but does agree with a previous study that compared the regulation of the two enzymes (Sacchi et al, 2013). Significant upregulation or downregulation of IMPA1 mRNA under hyper-and hypo-osmotic challenge, respectively, has been reported in other teleost fishes (Evans and Somero, 2008;Kalujnaia et al, 2010;Whitehead et al, 2012). In leopard sharks, an osmoconforming species, inositol-related proteins have also been reported to be regulated in rectal gland and gill tissues in response to hypo-osmotic challenge (Dowd et al, 2010).…”

Section: Mib Enzymes In Tilapia Brain Robustly Respond To Plasma Osmosupporting

confidence: 87%

“…The MIB pathway utilizes two enzymes, myo-inositol phosphate synthase (MIPS) and inositol monophosphatase (IMPA), to generate myo-inositol endogenously from glucose-6-phosphate (G-6-P) in a two-step reaction (Geiger and Jin, 2006). The study by Fiol et al (Fiol et al, 2006b) was the first to identify upregulation of MIPS mRNA in response to acute hyperosmotic challenge in tilapia gill, and since then, several studies have confirmed induction of the MIB pathway in other euryhaline species exposed to salinity challenge (Evans and Somero, 2008;Kalujnaia et al, 2009;Kalujnaia et al, 2010;Kalujnaia et al, 2013). In mammals, IMPA has at least two isoforms, originating from different genes (Ohnishi et al, 2007;Shamir et al, 2001), while MIPS can have alternative splice variants (Seelan et al, 2009) derived from the same gene.…”

Section: Introductionmentioning

confidence: 99%

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Tilapia (Oreochromis mossambicus) brain cells respond to hyperosmotic challenge by inducingmyo-inositol biosynthesis

Gardell

Yang

Sacchi

et al. 2013

Journal of Experimental Biology

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SUMMARYThis study aimed to determine the regulation of the de novo myo-inositol biosynthetic (MIB) pathway in Mozambique tilapia (Oreochromis mossambicus) brain following acute (25 ppt) and chronic (30, 60 and 90 ppt) salinity acclimations. The MIB pathway plays an important role in accumulating the compatible osmolyte, myo-inositol, in cells in response to hyperosmotic challenge and consists of two enzymes, myo-inositol phosphate synthase and inositol monophosphatase. In tilapia brain, MIB enzyme transcriptional regulation was found to robustly increase in a time (acute acclimation) or dose (chronic acclimation) dependent manner. Blood plasma osmolality and Na + and Cl -concentrations were also measured and significantly increased in response to both acute and chronic salinity challenges. Interestingly, highly significant positive correlations were found between MIB enzyme mRNA and blood plasma osmolality in both acute and chronic salinity acclimations. Additionally, a mass spectrometry assay was established and used to quantify total myo-inositol concentration in tilapia brain, which closely mirrored the hyperosmotic MIB pathway induction. Thus, myo-inositol is a major compatible osmolyte that is accumulated in brain cells when exposed to acute and chronic hyperosmotic challenge. These data show that the MIB pathway is highly induced in response to environmental salinity challenge in tilapia brain and that this induction is likely prompted by increases in blood plasma osmolality. Because the MIB pathway uses glucose-6-phosphate as a substrate and large amounts of myo-inositol are being synthesized, our data also illustrate that the MIB pathway likely contributes to the high energetic demand posed by salinity challenge.

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Section: Mib Enzymes In Tilapia Brain Robustly Respond To Plasma Osmosupporting

confidence: 87%

Section: Introductionmentioning

confidence: 99%

Tilapia (Oreochromis mossambicus) brain cells respond to hyperosmotic challenge by inducingmyo-inositol biosynthesis

Gardell

Yang

Sacchi

et al. 2013

Journal of Experimental Biology

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“…Evidence for salinity-dependent regulation of IMPA1 mRNA has recently been reported for other species of euryhaline fish, suggesting that the induction of the MIB pathway during hyperosmotic stress is an evolutionarily conserved trait of euryhaline teleosts. In European eel (Anguilla anguilla), IMPA1 mRNA increases in parallel to increased salinity (Kalujnaia and Cramb, 2009;Kalujnaia et al, 2010), and in killifish (Fundulus heteroclitus), IMPA1 mRNA is downregulated in response to a salinity decrease (Whitehead et al, 2012). The exquisite osmotic sensitivity of IMPA1 at both mRNA and protein levels makes this enzyme a robust indicator system for mechanistic studies of osmosensory signal transduction.…”

Section: Mips/impa Mrna Versus Protein Regulationmentioning

confidence: 99%

“…In addition, Kalujnaia and others (Kalujnaia and Cramb, 2009;Kalujnaia et al, 2010) have shown that the second enzyme of the MIB pathway (IMPA; EC 3.1.3.25) is also strongly induced at the mRNA level in the gill, kidney and intestine of European eels. These data on salinity effects at the transcript level suggest that the MIB pathway is physiologically important during osmotic stress because it generates high concentrations of the compatible organic osmolyte myo-inositol, which protects cells from salinity-induced damage (Yancey et al, 1982).…”

Section: Introductionmentioning

confidence: 98%

Salinity-induced activation of the myo-inositol biosynthesis pathway in tilapia gill epithelium

Sacchi

Villarreal

et al. 2013

Journal of Experimental Biology

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SUMMARYThe myo-inositol biosynthesis (MIB) pathway converts glucose-6-phosphate to the compatible osmolyte myo-inositol that protects cells from osmotic stress. Using proteomics, the enzymes that constitute the MIB pathway, myo-inositol phosphate synthase (MIPS) and inositol monophosphatase 1 (IMPA1), are identified in tilapia (Oreochromis mossambicus) gill epithelium. Targeted, quantitative, label-free proteomics reveals that they are both upregulated during salinity stress. Upregulation is stronger when fish are exposed to severe (34 ppt acute and 90 ppt gradual) relative to moderate (70 ppt gradual) salinity stress. IMPA1 always responds more strongly than MIPS, suggesting that MIPS is more stable during salinity stress. MIPS is N-terminally acetylated and the corresponding peptide increases proportionally to MIPS protein, while non-acetylated N-terminal peptide is not detectable, indicating that MIPS acetylation is constitutive and may serve to stabilize the protein. Hyperosmotic induction of MIPS and IMPA1 is confirmed using western blot and real-time qPCR and is much higher at the mRNA than at the protein level. Two distinct MIPS mRNA variants are expressed in the gill, but one is more strongly regulated by salinity than the other. A single MIPS gene is encoded in the tilapia genome whereas the zebrafish genome lacks MIPS entirely. The genome of euryhaline tilapia contains four IMPA genes, two of which are expressed, but only one is salinity regulated in gill epithelium. The genome of stenohaline zebrafish contains a single IMPA gene. We conclude that the MIB pathway represents a major salinity stress coping mechanism that is regulated at multiple levels in euryhaline fish but absent in stenohaline zebrafish.Supplementary material available online at http://jeb.biologists.org/lookup/suppl

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“…Induction of these two genes is also evident in other euryhaline fish exposed to acute salinity stress. For instance, elevated salinity increases MIPS abundance in O. niloticus and Anguilla anguilla (52) and IMPA1.1 abundance in Gillichthys mirabilis and A. anguilla (53)(54)(55)(56). The MIB pathway promotes the accumulation of high concentrations of the compatible osmolyte myo-inositol, which protects cells from salinity-induced damage (44,48,57).…”

Section: Discussionmentioning

confidence: 99%

Osmolality/salinity-responsive enhancers (OSREs) control induction of osmoprotective genes in euryhaline fish

Wang

Kültz

2017

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

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Fish respond to salinity stress by transcriptional induction of many genes, but the mechanism of their osmotic regulation is unknown. We developed a reporter assay using cells derived from the brain of the tilapia Oreochromis mossambicus (OmB cells) to identify osmolality/salinity-responsive enhancers (OSREs) in the genes of O. mossambicus. Genomic DNA comprising the regulatory regions of two strongly salinity-induced genes, inositol monophosphatase 1 (IMPA1.1) and myo-inositol phosphate synthase (MIPS), was isolated and analyzed with dual luciferase enhancer trap reporter assays. We identified five sequences (two in IMPA1.1 and three in MIPS) that share a common consensus element (DDKGGAAWWDWWYDNRB), which we named "OSRE1." Additional OSREs that were less effective in conferring salinity-induced trans-activation and do not match the OSRE1 consensus also were identified in both MIPS and IMPA1.1. Although OSRE1 shares homology with the mammalian osmotic-response element/tonicity-responsive enhancer (ORE/TonE) enhancer, the latter is insufficient to confer osmotic induction in fish. Like other enhancers, OSRE1 trans-activates genes independent of orientation. We conclude that OSRE1 is a cis-regulatory element (CRE) that enhances the hyperosmotic induction of osmoregulated genes in fish. Our study also shows that tailored reporter assays developed for OmB cells facilitate the identification of CREs in fish genomes. Knowledge of the OSRE1 motif allows affinity-purification of the corresponding transcription factor and computational approaches for enhancer screening of fish genomes. Moreover, our study enables targeted inactivation of OSRE1 enhancers, a method superior to gene knockout for functional characterization because it confines impairment of gene function to a specific context (salinity stress) and eliminates pitfalls of constitutive gene knockouts (embryonic lethality, developmental compensation). biochemical evolution | compatible osmolytes | osmotic stress signaling | enhancer | CRE

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A role for inositol monophosphatase 1 (IMPA1) in salinity adaptation in the euryhaline eel (Anguilla anguilla)

Cited by 30 publications

References 45 publications

Tilapia (Oreochromis mossambicus) brain cells respond to hyperosmotic challenge by inducingmyo-inositol biosynthesis

Tilapia (Oreochromis mossambicus) brain cells respond to hyperosmotic challenge by inducingmyo-inositol biosynthesis

Salinity-induced activation of the myo-inositol biosynthesis pathway in tilapia gill epithelium

Osmolality/salinity-responsive enhancers (OSREs) control induction of osmoprotective genes in euryhaline fish

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