Cold-inducible ribonucleic acid-binding protein attenuates acute kidney injuries after deep hypothermic circulatory arrest in rats

Yu, Lei; Gu, Tingting; Liu, Yü; Jiang, Xuan; Shi, Enyi

doi:10.1093/icvts/ivx262

Cited by 7 publications

(4 citation statements)

References 26 publications

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“…Based on these findings, we speculated that the length of CPB time is an important contributor to upregulation of CIRP. Interestingly, our multiple linear regression analysis found that the temperature value we kept during CPB has little effect on CIRP production, but this finding is inconsistent with previous evidence that CIRP is induced by hypothermia [18,24]. Considering the hypothermia level during CPB, we speculate that the degree of temperature reduction partly explains this strange phenomenon.…”

Section: Discussioncontrasting

confidence: 91%

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Plasma Cold-Inducible RNA-Binding Protein Predicts Lung Dysfunction After Cardiovascular Surgery Following Cardiopulmonary Bypass: A Prospective Observational Study

Xia

Jiang

et al. 2019

Med Sci Monit

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Background Cold-inducible RNA-binding protein (CIRP) has been identified as an inflammatory mediator that exerts its function in inflammatory diseases. However, the roles of CIRP in patients who received cardiovascular surgery necessitating cardiopulmonary bypass (CPB) are still unknown. The aim of this study was to examine CIRP levels and attempt to evaluate whether CIRP could serve as a predictor for lung dysfunction after cardiovascular surgery. Material/Methods Plasma CIRP levels were detected by ELISA in 31 patients who received cardiovascular surgery at different time points. Selective inflammatory cytokines (TNF-α, IL-6, IL-10, and TLR4) and mediators (Ang II, PAI-1, and soluble E-selectin) were also detected. Selective laboratory and clinical parameters were recorded at scheduled time points. Results Compared with pre-operation levels, CIRP levels significantly increased 6 h after cardiovascular surgery with CPB. Multiple linear regression analysis showed that the length of CPB time contributed to CIRP production ( P =0.013). Furthermore, CIRP was associated with Ang II (r=0.438, P =0.016), PAI-1 (r=0.485, P =0.006), and soluble E-selectin (r=0.470, P =0.008), which partly reflected lung injuries. Multiple linear regression analysis showed that CIRP levels were independently associated with PaO 2 /FiO 2 ratios ( P =0.021). Conclusions The length of CPB time contributed to the upregulation of CIRP in patients who received cardiovascular surgery with CPB. CIRP levels could serve as a biomarker to predict the onset of lung injury induced by cardiovascular surgery.

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Section: Discussioncontrasting

confidence: 91%

“…It is well known that CIRP initiates a systemic inflammatory responses that leads to undesirable outcomes. However, in contrast to previous studies, a rat model study of deep hypothermic circulatory arrest showed that CIRP exerts its robust renoprotection roles through inhibiting apoptosis activities [18].…”

Section: Introductionmentioning

confidence: 77%

Plasma Cold-Inducible RNA-Binding Protein Predicts Lung Dysfunction After Cardiovascular Surgery Following Cardiopulmonary Bypass: A Prospective Observational Study

Xia

Jiang

et al. 2019

Med Sci Monit

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“…For example, the genes encoding the cold inducible RNA binding proteins ( cirbpa and cirbpb ) and the high mobility group box proteins ( hmgb1b and hmgb3a ) were regarded as marker genes for cold stress ( Gracey et al, 2004 ; Long et al, 2013 ). CIRBP is a stress-responsive protein has protective effects against tissue injury and cell apoptosis caused by both hyperthermia and hypothermia stressors ( Yu et al, 2018 ; Cheng et al, 2019 ; Liu et al, 2019 ). HMGB1 is the best characterized damage-associated molecular pattern, which is normally inside the cell and is released after cell death or secreted upon severe stresses.…”

Section: Discussionmentioning

confidence: 99%

Transcriptional Programs Underlying Cold Acclimation of Common Carp (Cyprinus carpio L.)

Long

et al. 2020

Front. Genet.

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Properly regulated transcriptional responses to environmental perturbations are critical for the fitness of fish. Although gene expression profiles in the tissues of common carp upon cold stress were previously characterized, the transcriptional programs underlying cold acclimation are still not well known. In this study, the ability of three common carp strains including Hebao red carp (HB), Songpu mirror carp (SPM) and Yellow river carp (YR) to establish cold resistance after acclimation to a mild hypothermia stress at 18°C for 24 h was confirmed by measurements of the critical thermal minimums (CTMin). The gene expression profiles of the brain and the heart from these strains under both control and cold-acclimated conditions were characterized with RNA-sequencing. The data of the three common carp strains with different genetic background were combined in the differential gene expression analyses to balance the effects of genetic diversity on gene expression. Marked effects of tissue origins on the cold-induced transcriptional responses were revealed by comparing the differentially expressed gene (DEG) lists of the two tissues. Functional categories including spliceosome and RNA splicing were highly enriched in the DEGs of both tissues. However, steroid biosynthesis was specifically enriched in DEGs of the brain and response to unfolded protein was solely enriched in DEGs of the heart. Consistent with the up-regulation of the genes involved in cholesterol biosynthesis, total cholesterol content of the brain was significantly increased upon cold stress. Moreover, cold-induced alternative splicing (AS) events were explored and AS of the rbmx (RNA-binding motif protein, X chromosome) gene was confirmed by real-time quantitative PCR. Finally, a core set of cold responsive genes (CRGs) were defined by comparative transcriptomic analyses. Our data provide insights into the transcriptional programs underlying cold acclimation of common carp and offer valuable clues for further investigating the genetic determinants for cold resistance of farmed fish.

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“…CIRP coordinates mRNA translational reprogramming by selectively binding to the 3’-untranslated region of transcripts, which facilitates cellular adaptation to uncomfortable environments (Hiroyuki Nishiyama 1997b ; Zhong and Huang 2017 ; Liao et al 2017 ). Accumulating data demonstrate that CIRP may exert protective effects on multiple organs during IR (Liu et al 2019 , 2020 ; Yu et al 2018 ; Li et al 2019 ; McGinn et al 2018 ), and the available in vivo renal phenotypic evidence suggests that CIRP may play an anti-apoptotic role during hypothermic cardioplegic arrest (Yu et al 2018 ). However, the underlying molecular mechanism remains unclear.…”

Section: Introductionmentioning

confidence: 99%

CIRP attenuates acute kidney injury after hypothermic cardiovascular surgery by inhibiting PHD3/HIF-1α-mediated ROS-TGF-β1/p38 MAPK activation and mitochondrial apoptotic pathways

Zhang

Bai

Tong

et al. 2023

Mol Med

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Background The ischemia–reperfusion (IR) environment during deep hypothermic circulatory arrest (DHCA) cardiovascular surgery is a major cause of acute kidney injury (AKI), which lacks preventive measure and treatment. It was reported that cold inducible RNA-binding protein (CIRP) can be induced under hypoxic and hypothermic stress and may have a protective effect on multiple organs. The purpose of this study was to investigate whether CIRP could exert renoprotective effect during hypothermic IR and the potential mechanisms. Methods Utilizing RNA-sequencing, we compared the differences in gene expression between Cirp knockout rats and wild-type rats after DHCA and screened the possible mechanisms. Then, we established the hypothermic oxygen–glucose deprivation (OGD) model using HK-2 cells transfected with siRNA to verify the downstream pathways and explore potential pharmacological approach. The effects of CIRP and enarodustat (JTZ-951) on renal IR injury (IRI) were investigated in vivo and in vitro using multiple levels of pathological and molecular biological experiments. Results We discovered that Cirp knockout significantly upregulated rat Phd3 expression, which is the key regulator of HIF-1α, thereby inhibiting HIF-1α after DHCA. In addition, deletion of Cirp in rat model promoted apoptosis and aggravated renal injury by reactive oxygen species (ROS) accumulation and significant activation of the TGF-β1/p38 MAPK inflammatory pathway. Then, based on the HK-2 cell model of hypothermic OGD, we found that CIRP silencing significantly stimulated the expression of the TGF-β1/p38 MAPK inflammatory pathway by activating the PHD3/HIF-1α axis, and induced more severe apoptosis through the mitochondrial cytochrome c-Apaf-1-caspase 9 and FADD-caspase 8 death receptor pathways compared with untransfected cells. However, silencing PHD3 remarkably activated the expression of HIF-1α and alleviated the apoptosis of HK-2 cells in hypothermic OGD. On this basis, by pretreating HK-2 and rats with enarodustat, a novel HIF-1α stabilizer, we found that enarodustat significantly mitigated renal cellular apoptosis under hypothermic IR and reversed the aggravated IRI induced by CIRP defect, both in vitro and in vivo. Conclusion Our findings indicated that CIRP may confer renoprotection against hypothermic IRI by suppressing PHD3/HIF-1α-mediated apoptosis. PHD3 inhibitors and HIF-1α stabilizers may have clinical value in renal IRI.

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Cold-inducible ribonucleic acid-binding protein attenuates acute kidney injuries after deep hypothermic circulatory arrest in rats

Abstract: Our findings suggest that the CIRP exerts a robust renoprotective effect by inhibiting apoptosis in the rat model of deep hypothermic circulatory arrest.

Cited by 7 publications

References 26 publications

Plasma Cold-Inducible RNA-Binding Protein Predicts Lung Dysfunction After Cardiovascular Surgery Following Cardiopulmonary Bypass: A Prospective Observational Study

Plasma Cold-Inducible RNA-Binding Protein Predicts Lung Dysfunction After Cardiovascular Surgery Following Cardiopulmonary Bypass: A Prospective Observational Study

Transcriptional Programs Underlying Cold Acclimation of Common Carp (Cyprinus carpio L.)

CIRP attenuates acute kidney injury after hypothermic cardiovascular surgery by inhibiting PHD3/HIF-1α-mediated ROS-TGF-β1/p38 MAPK activation and mitochondrial apoptotic pathways

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