Search bioRxiv⌕ Search

Biology subjects

Arige, V.

Publications and source records attributed to Arige, V..

9 recordsLinked to original sources

Dynamic regulation of cystathionine gamma-lyase expression during normoxia, ischemia, and reperfusion in liver: interplay of transcription factors, microRNAs, and histone modifications

Cystathionine gamma-lyase (CTH), a key enzyme in hydrogen sulfide (H2S) biosynthesis, has been studied extensively in models of oxidative stress. Dysregulated CTH has been reported in cardiovascular disease, ischemia-reperfusion (I/R) injury, aging, and xenobiotic stress, where reactive oxygen species are central to pathology. Despite this, how CTH is regulated at the molecular level under basal, ischemic, and reperfusion conditions is largely unknown. We observed that CTH expression is dysregulated during ischemia and reperfusion in Huh7 hepatic cells, mouse liver, and human liver, and therefore systematically dissected its transcriptional, post-transcriptional, and epigenetic control. Promoter-deletion reporter assays identified the -275/+91 bp region as the core human CTH promoter. This region was predicted to harbour binding sites for Sp1, CREB, and NFY, which were confirmed through overexpression, knockdown or inhibition, and ChIP assays in Huh7 cells. Computational and experimental screening identified miR-150-5p and miR-510-5p as novel post-transcriptional regulators that bind directly to the CTH 3'-UTR. We also examined histone marks (H3K9ac, H3K9me3, H3K4me3, and H3K27me3) at the CTH promoter and found that H3K9ac, H3K4me3, and H3K27me3 correlate with CTH expression across basal, ischemic, and reperfusion conditions. Mechanistically, ischemia reduces Sp1 occupancy at the CTH promoter, raises miR-150-5p and miR-510-5p levels, lowers H3K9ac, collectively suppressing CTH. Reperfusion reverses this with greater Sp1 and CREB binding, lower miR-150-5p and miR-510-5p levels, and reduced H3K27me3, restoring CTH expression. Together, these findings reveal novel roles for Sp1, CREB, NFY, miR-150-5p, miR-510-5p, and histone modifications in the regulation of CTH during basal, ischemia and reperfusion conditions.

molecular biology↗

Functional investigation of a putative calcium-binding site involved in the inhibition of inositol 1,4,5-trisphosphate receptor activity

A wide variety of factors influence inositol 1,4,5-trisphosphate (IP3) receptor (IP3R) activity resulting in modulation of intracellular Ca2+ release. This regulation is thought to define the spatio-temporal patterns of Ca2+ signals necessary for the appropriate activation of downstream effectors. The binding of both IP3 and Ca2+ are obligatory for IP3R channel opening, however, Ca2+ regulates IP3R activity in a biphasic manner. Mutational studies have revealed that Ca2+ binding to a high-affinity pocket formed by the ARM3 domain and linker domain promotes IP3R channel opening without altering the Ca2+ dependency for channel inactivation. These data suggest a distinct low-affinity Ca2+ binding site is responsible for the reduction in IP3R activity at higher [Ca2+]. We determined the consequences of mutating a cluster of acidic residues in the ARM2 and central linker domain reported to coordinate Ca2+ in cryo-EM structures of the IP3R type 3. This site is termed the "CD Ca2+ binding site" and is well-conserved in all IP3R sub-types. We show that the CD site Ca2+ binding mutants where the negatively charged glutamic acid residues are mutated to alanine exhibited enhanced sensitivity to IP3-generating agonists. Ca2+ binding mutants displayed spontaneous elemental Ca2+ events (Ca2+ puffs) and the number of IP3-induced Ca2+ puffs was significantly augmented in cells stably expressing Ca2+ binding site mutants. When measured with "on-nucleus" patch clamp, the inhibitory effect of high [Ca2+] on single channel-open probability (Po) was reduced in mutant channels and this effect was dependent on [ATP]. These results indicate that Ca2+ binding to the putative CD Ca2+ inhibitory site facilitates the reduction in IP3R channel activation when cytosolic [ATP] is reduced and suggest that at higher [ATP], additional Ca2+ binding motifs may contribute to the biphasic regulation of IP3-induced Ca2+ release.

biochemistry↗

Structural dynamics underlying gating and regulation in IP3R channel

Inositol-1,4,5-trisphosphate receptors (IP3Rs) are activated by IP3 and Ca2+ and their gating is regulated by various intracellular messengers that finely tune the channel activity. Here, using single particle cryo-EM analysis we determined 3D structures of the nanodisc-reconstituted IP3R1 channel in two ligand-bound states. These structures provide unprecedented details governing binding of IP3, Ca2+ and ATP in IP3R1, revealing conformational changes that couple ligand-binding to channel opening. Using a GMM based deep learning approach and 3D variability analysis, we extracted dynamic properties of the key protein domains. From this, we find that IP3 binding relies upon intrinsic flexibility of the cytoplasmic ARM2 domain. Our results highlight a key role of dynamic side chains surrounding the ion conduction path in regulating gating behavior of IP3R channels. Altogether, this work defines a structural platform for mechanistic understanding of the molecular dynamics underlying ligand-binding, activation and regulation of the IP3R activity.

biophysics↗

Functional Determination of Calcium Binding Sites Required for the Activation of Inositol 1,4,5-trisphosphate receptors.

Inositol 1,4,5-trisphosphate (IP3) receptors (IP3Rs) initiate a diverse array of physiological responses by carefully orchestrating intracellular calcium (Ca2+) signals in response to various external cues. Notably, IP3R channel activity is determined by several obligatory factors including IP3, Ca2+ and ATP. The critical basic amino acid residues in the N-terminal IP3-binding core (IBC) region that facilitate IP3 binding are well characterized. In contrast, the residues conferring the biphasic regulation by Ca2+ are yet to be ascertained. Using comparative structural analysis of Ca2+ binding sites identified in two main families of intracellular Ca2+-release channels, ryanodine receptors (RyRs) and IP3Rs, we identified putative acidic residues coordinating Ca2+ in the cytosolic calcium sensor region in IP3Rs. We determined the consequences of substituting putative Ca2+ binding, acidic residues in IP3R family members. We show that the agonist-induced Ca2+ release, single channel open probability (P0) and Ca2+ sensitivities are markedly altered when the negative charge on the conserved acidic side chain residues are neutralized. Remarkably, neutralizing the negatively charged side chain on two of the residues individually in the putative Ca2+ binding pocket shifted the Ca2+ required to activate IP3R to higher concentrations, indicating that these residues likely are a component of the Ca2+ activation site in IP3R. Taken together, our findings indicate that Ca2+ binding to a well conserved activation site is a common underlying mechanism resulted in increased channel activity shared by IP3Rs and RyRs.

physiology↗

CREB regulates the expression of Type 1 Inositol 1,4,5-trisphosphate receptors

Inositol 1,4,5-trisphosphate (IP3) receptors (IP3Rs) play a central role in regulating intracellular calcium signals in response to a variety of internal/external cues. Dysregulation of IP3R signaling is the underlying cause for numerous pathological conditions. It is also well established that the activity of IP3Rs is governed by several post-translational modifications including phosphorylation by protein kinase A (PKA). However, the long-term effects of PKA activation on expression of IP3R sub-types, remains largely unexplored. In this report, we investigate the effect of chronic activation of PKA on expression of IP3R sub-types. We demonstrate that expression of IP3R1 is augmented upon prolonged activation of PKA or upon ectopic over-expression of CREB but does not alter IP3R2 and IP3R3 sub-type abundance. Conversely, inhibition of PKA or blocking endogenous CREB diminished IP3R1 expression. We also demonstrate that agonist-induced Ca2+-release mediated by IP3R1 is significantly attenuated upon blocking endogenous CREB. Moreover, CREB by regulating the expression of KRAS-induced actin-interacting protein (KRAP) ensures proper localization and licensing of IP3R1. Overall, we report a crucial role for CREB in governing both the expression and proper localization of IP3R1. Summary statementWe report a critical role of CREB in regulating the expression and proper localization of IP3R1. Agonist-induced Ca2+ release and Ca2+ puffs generated by IP3R1 are diminished upon blocking the function of endogenous CREB.

physiology↗

Regulation of Interorganellar Ca2+ Transfer and NFAT Activation by the Mitochondrial Ca2+ Uniporter

Mitochondrial Ca2+ uptake is crucial for coupling receptor stimulation to cellular bioenergetics. Further, Ca2+ uptake by respiring mitochondria prevents Ca2+-dependent inactivation (CDI) of store-operated Ca2+ release-activated Ca2+ (CRAC) channels and inhibits Ca2+ extrusion to sustain cytosolic Ca2+ signaling. However, how Ca2+ uptake by the mitochondrial Ca2+ uniporter (MCU) shapes receptor-evoked interorganellar Ca2+ signaling is unknown. Here, we generated several cell lines with MCU-knockout (MCU-KO) as well as tissue-specific MCU-knockdown mice. We show that mitochondrial depolarization, but not MCU-KO, inhibits store-operated Ca2+ entry (SOCE). Paradoxically, despite enhancing Ca2+ extrusion and promoting CRAC channel CDI, MCU-KO increased cytosolic Ca2+ in response to store depletion. Further, physiological agonist stimulation in MCU-KO cells led to enhanced frequency of cytosolic Ca2+ oscillations, endoplasmic reticulum Ca2+ refilling, NFAT nuclear translocation and proliferation. However, MCU-KO did not affect inositol-1,4,5-trisphosphate receptor activity. Mathematical modeling supports that MCU-KO enhances cytosolic Ca2+, despite limiting CRAC channel activity.

cell biology↗

Omnitemporal choreographies of IP3R and all five STIM/Orai underlie the complexity of mammalian Ca2+ signaling

Invertebrates express one endoplasmic reticulum (ER)-resident Ca2+-sensing stromal-interaction molecule (Stim) and one Orai plasma membrane channel protein. Stim conveys store depletion to Orai, mediating the evolutionarily conserved Ca2+ release-activated Ca2+ (CRAC) current. The crucial role of their vertebrate homologues, STIM1 and Orai1 in mediating CRAC activity in mammals is well-established. However, mammals possess two STIM and three Orai isoforms and the choreography of their interactions under physiological receptor activation is unknown. We show that the five mammalian STIM1/2 and Orai1/2/3 isoforms have non-redundant functions. Yet, all five isoforms are always required together to ensure the graded diversity of mammalian Ca2+ signaling events in response to the full spectrum of agonist strengths. Receptor-activated Ca2+ signaling across the range of stimulus intensities requires functional interactions between not only STIM1/2 and Orai1/2/3, but also IP3R, ensuring that receptor-mediated Ca2+ release is precisely tailored to Ca2+ entry and activation of nuclear factor of activated T-cells (NFAT). This is orchestrated by two interdependent and counterbalancing paradigms: the N-termini Ca2+-binding ER-luminal domains of unactivated STIM1/2 inhibit IP3R-evoked Ca2+ release. Gradual increase in agonist intensity leads to gradual STIM1/2 activation and relief of IP3R inhibition. Concomitantly, the cytosolic C-termini of activated STIM1/2 differentially interact with Orai1/2/3 proteins as agonist intensity increases. Thus, coordinated and omnitemporal functions of all five STIM/Orai proteins and IP3Rs at the ER-lumen and cytosol translate the strength of agonist stimulation to precise levels of Ca2+ release, Ca2+ entry and NFAT induction, ensuring the diversity and fidelity of complex mammalian Ca2+ signaling. HighlightsO_LIAll five STIM/Orai and IP3R are always required together in mammalian Ca2+ signalling C_LIO_LIUnactivated STIM1/2 inhibit IP3R and activated STIM1/2 cooperatively activate Orai1/2/3 C_LIO_LISTIM1 contribution increases and that of STIM2 decreases as agonist intensifies C_LIO_LIGraded IP3R disinhibition and Orai activation tailor receptor activity to NFAT induction C_LI O_FIG O_LINKSMALLFIG WIDTH=192 HEIGHT=200 SRC="FIGDIR/small/325480v1_ufig1.gif" ALT="Figure 1"> View larger version (65K): org.highwire.dtl.DTLVardef@f6172dorg.highwire.dtl.DTLVardef@6bbb09org.highwire.dtl.DTLVardef@c45c80org.highwire.dtl.DTLVardef@194d7e4_HPS_FORMAT_FIGEXP M_FIG C_FIG

physiology↗

Hypoxia mediated regulation of mitochondrial transcription factors: Implications of hypertensive renal physiology

Kidneys have a high resting metabolic rate and low tissue partial pressure of oxygen due to enhanced mitochondrial oxygen consumption and ATP production for active solute transport. Enhanced mitochondrial activity leads to progressive hypoxia from the renal cortex to renal medulla. Renal tubulointerstitial hypoxia (TiH) is severe in hypertensive rats due to increased sodium reabsorption within their nephrons. Additionally, these rats display increased energy demand and therefore, require healthy mitochondria for adequate salt reabsorption. Hence, we sought to study the regulation of mitochondrial biogenesis and expression of mitochondrial transcription factors (mtTFs, viz. Tfam, Tfb1m and Tfb2m) during hypoxic conditions and in rodent models of genetic hypertension. We report that the expressions of HIF-1 (hypoxia inducible factor-1), PGC-1 (peroxisome proliferator activated receptor-{gamma} co-activator-1), mtTFs and OXPHOS proteins are elevated in hypertensive rats as compared to their normotensive counterparts. Additionally, studies in cultured kidney cells show that acute hypoxia augments the expression of these genes. We also observe a positive correlation between HIF-1 and mtTFs transcripts in human tissues. Furthermore, we report for the first time to our knowledge, that HIF-1 binds to promoters of Tfam, Tfb1m and Tfb2m genes and augments their promoter activities in NRK52e cells subjected to acute hypoxia. Taken together, this study suggests that acute hypoxia may enhance mitochondrial function to meet the energy demand in renal tubular epithelial cells and in young/pre-hypertensive SHR kidneys. Translational StatementOur results suggest that tubulointerstitial hypoxia (TiH) prevailing in prehypertensive rats augments the expression of mitochondrial transcription factors and proteins of electron transport chain. Moreover, previous reports indicate that ATP synthesis in these rats are elevated. Thus, our study provides insights into the molecular mechanism of such enhanced mitochondrial function. We propose that during early stages of kidney diseases (marked by mild TiH) an enhancement of mitochondrial function via stimulation of HIF-1/PGC-1 production may delay renal tubular damage.

molecular biology↗

Functional promoter polymorphisms govern the differential expression of HMG-CoA Reductase gene in rat models of essential hypertension

3-Hydroxy-3-methyl glutaryl-coenzyme A reductase (Hmgcr) encoding the rate-limiting enzyme in the cholesterol biosynthesis pathway is a candidate gene for essential hypertension (EH). However, the regulation of Hmgcr in rat models of hypertension (viz. Spontaneously Hypertensive Rats [SHR] and its normotensive control Wistar/Kyoto [WKY] strain) is unknown. Here, we show that Hmgcr transcript and protein levels are diminished in liver tissues of SHR as compared to WKY. Consistently, a number of other rat models of hypertension display diminished cholesterol levels as compared to corresponding control strains. Sequencing of the Hmgcr promoter in SHR/WKY reveals three variations: A-405G, C-62T and a 11 bp insertion (-393_-382insTGCGGTCCTCC) in SHR. Moreover, SHR-Hmgcr promoter displays higher activity than WKY-Hmgcr promoter in various cell lines. Transient transfections of Hmgcr-promoter mutants and in silico analysis suggest altered binding of Runx3 and Srebf1 across A-405G and -393_-382insTGCGGTCCTCC sites. Indeed, chromatin immunoprecipitation assays confirm differential binding of Runx3/Srebf1 to Hmgcr promoter leading to diminished expression of Hmgcr in SHR as compared to WKY under basal/cholesterol-modulated conditions. Taken together, this study provides mechanistic insights for the altered Hmgcr expression in these models of EH, thereby unravelling the links of this gene to hypertension and associated cardiovascular disease states.

molecular biology↗