冷诱导RNA结合蛋白生物学功能的研究进展
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摘要
冷诱导RNA结合蛋白(Cold-inducible RNA-binding protein,CIRP)是在哺乳动物中第一个被发现的冷休克蛋白,广泛表达于各种组织细胞中,且伴随冷应激、缺氧应激、紫外线照射、渗透压应激等过程而过量表达。CIRP是一种多功能的生理活性物质。在应激反应过程中,CIRP可从细胞核转移至细胞浆,主要通过调节靶蛋白基因转录后水平参与诸多细胞调节过程,如细胞的增殖和分化、细胞生存与凋亡、肿瘤的发生发展及生物节律变化等。此外,CIRP还可以通过直接与细胞内信号分子相互作用而发挥生物学效应。不仅如此,CIRP还可以被分泌到细胞外。细胞外的CIRP是一个重要的促炎因子,在急慢性炎症疾病过程中扮演着重要角色。本文就其最新研究进展作一综述,以期为利用该蛋白开展更深入的基础研究和治疗临床相关疾病奠定一定的理论基础。
Cold-inducible RNA-binding protein( CIRP) is the first cold shock protein identified in mammals,widely expressed in various cells and tissues and regulated significantly after exposure to moderate cold stress. CIRP can also be induced by hypoxia,UV,osmotic pressure H2 O2 and heat stress. CIRP possesses a variety of biological functions. In response to stress,CIRP can migrate from the nucleus to the cytoplasm and regulate mRNA stability of its targets to implicate cell process,such as cell proliferation and differentiation,cell survive and adoption,tumor formation and progression and circadian rhythm. In addition,CIRP can also exert its functions by directly interacting with intracellular signaling proteins. Moreover,CIRP protein is released from cells,it appears to bolster inflammation and plays an important role in both acute and chronic inflammatory diseases. In this paper,we summarized the latest research progress of CIRP and hope to provide insights into the role of CIRP in cell biology and diseases.
Cold-inducible RNA-binding protein( CIRP) is the first cold shock protein identified in mammals,widely expressed in various cells and tissues and regulated significantly after exposure to moderate cold stress. CIRP can also be induced by hypoxia,UV,osmotic pressure H2 O2 and heat stress. CIRP possesses a variety of biological functions. In response to stress,CIRP can migrate from the nucleus to the cytoplasm and regulate mRNA stability of its targets to implicate cell process,such as cell proliferation and differentiation,cell survive and adoption,tumor formation and progression and circadian rhythm. In addition,CIRP can also exert its functions by directly interacting with intracellular signaling proteins. Moreover,CIRP protein is released from cells,it appears to bolster inflammation and plays an important role in both acute and chronic inflammatory diseases. In this paper,we summarized the latest research progress of CIRP and hope to provide insights into the role of CIRP in cell biology and diseases.
引文
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[2]Xue JH,Nonoguchi K,Fukumoto M,et al.Effects of ischemia and H2O2on the cold stress protein CIRP expression in rat neuronal cells[J].Free Radic Biol Med,1999,27(11-12):1238-1244.
[3]Matsumoto K,Aoki K,Dohmae N,et al.CIRP2,a major cytoplasmic RNA-binding protein in Xenopus oocytes[J].Nucleic Acids Res,2000,28(23):4689-4697.
[4]Ciuzan O,Hancock J,Pamfil D,et al.The evolutionarily conserved multifunctional glycine-rich RNA-binding proteins play key roles in development and stress adaptation[J].Physiol Plant,2015,153(1):1-11.
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[7]Danno S,Nishiyama H,Higashitsuji H,et al.Increased transcript level of RBM3,a member of the glycine-rich RNA-binding protein family,in human cells in response to cold stress[J].Biochem Biophys Res Commun,1997,236(3):804-807.
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[25]Zhang Q,Wang YZ,Zhang W,et al.Involvement of cold inducible RNA-binding protein in severe hypoxia-induced growth arrest of neural stem cells in vitro[J].Mol Neurobiol,2017,54(3):2143-2153.
[26]Ryan JC,Morey JS,Ramsdell JS,et al.Acute phase gene expression in mice exposed to the marine neurotoxin domoic acid[J].Neuroscience,2005,136(4):1121-1132.
[27]Prieto-Alamo MJ,Abril N,Osuna-Jimenez I,et al.Solea senegalensis genes responding to lipopolysaccharide and copper sulphate challenges:large-scale identification by suppression subtractive hybridization and absolute quantification of transcriptional profiles by real-time RT-PCR[J].Aquat Toxicol,2009,91(4):312-319.
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[29]Jackson TC,Manole MD,Kotermanski SE,et al.Cold stress protein RBM3 responds to temperature change in an ultra-sensitive manner in young neurons[J].Neuroscience,2015,305:268-278.
[30]Morf J,Rey G,Schneider K,et al.Cold-inducible RNA-binding protein modulates circadian gene expression posttranscriptionally[J].Science,2012,338(6105):379-383.
[31]Bellesi M,de Vivo L,Tononi G,et al.Effects of sleep and wake on astrocytes:clues from molecular and ultrastructural studies[J].BMC Biol,2015,13:66.
[32]Nikonova EV,Gilliland JD,Tanis KQ,et al.Transcriptional profiling of cholinergic neurons from basal forebrain identifies changes in expression of genes between sleep and wake:mRNA profiling in basal forebrain with sleep/sleep deprivation[J].Sleep,2017,40(6):ZSX059.
[33]Banks S,King SA,Irvine DS,et al.Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa[J].Reproduction,2005,129(4):505-514.
[34]Peng Y,Yang PH,Tanner JA,et al.Cold-inducible RNA binding protein is required for the expression of adhesion molecules and embryonic cell movement in Xenopus laevis[J].Biochem Biophys Res Commun,2006,344(1):416-424.
[35]Yenari MA,Han HS.Neuroprotective mechanisms of hypothermia in brain ischaemia[J].Nat Rev Neurosci,2012,13(4):267-278.
[36]Alkabie S,Boileau AJ.The role of therapeutic hypothermia after traumatic spinal cord injury-a systematic review[J].World Neurosurg,2016,86:432-449.
[37]Salerian AJ,Saleri NG.Cooling core body temperature may slow down neurodegeneration[J].CNS Spectr,2008,13(3):227-229.
[38]Zhang HT,Xue JH,Zhang ZW,et al.Cold-inducible RNA-binding protein inhibits neuron apoptosis through the suppression of mitochondrial apoptosis[J].Brain Res,2015,1622:474-483.
[39]Kita H,Carmichael J,Swartz J,et al.Modulation of polyglutamineinduced cell death by genes identified by expression profiling[J].Hum Mol Genet,2002,11(19):2279-2287.
[40]Liu A,Zhang Z,Li A,et al.Effects of hypothermia and cerebral ischemia on cold-inducible RNA-binding protein mRNA expression in rat brain[J].Brain Res,2010,1347:104-110.
[41]Sanderson TH,Reynolds CA,Kumar R,et al.Molecular mechanisms of ischemia-reperfusion injury in brain:pivotal role of the mitochondrial membrane potential in reactive oxygen species generation[J].Mol Neurobiol,2013,47(1):9-23.
[42]Liu J,Xue J,Zhang H,et al.Cloning,expression,and purification of cold inducible RNA-binding protein and its neuroprotective mechanism of action[J].Brain Res,2015,1597:189-195.
[43]Zhou M,Yang WL,Ji Y,et al.Cold-inducible RNA-binding protein mediates neuroinflammation in cerebral ischemia[J].Biochim Biophys Acta,2014,1840(7):2253-2261.
[44]Rajayer SR,Jacob A,Yang WL,et al.Cold-inducible RNA-binding protein is an important mediator of alcohol-induced brain inflammation[J].PLo S One,2013,8(11):e79430.
[45]Sakurai T,Yada N,Watanabe T,et al.Cold-inducible RNA-binding protein promotes the development of liver cancer[J].Cancer Sci,2015,106(4):352-358.
[46]Sakurai T,Kashida H,Watanabe T,et al.Stress response protein cirp links inflammation and tumorigenesis in colitis-associated cancer[J].Cancer Res,2014,74(21):6119-6128.
[47]Wang M,Zhang H,Heng X,et al.Expression of cold-inducible RNA-binding protein(CIRP)in pituitary adenoma and its relationships with tumor recurrence[J].Med Sci Monit,2015,21:1256-1260.
[48]Jian F,Chen Y,Ning G,et al.Cold inducible RNA binding protein upregulation in pituitary corticotroph adenoma induces corticotroph cell proliferation via Erk signaling pathway[J].Oncotarget,2016,7(8):9175-9187.
[49]Ren WH,Zhang LM,Liu HQ,et al.Protein overexpression of CIRP and TLR4 in oral squamous cell carcinoma:an immunohistochemical and clinical correlation analysis[J].Med Oncol,2014,31(8):120.
[50]Lee HN,Ahn SM,Jang HH.Cold-inducible RNA-binding protein promotes epithelial-mesenchymal transition by activating ERK and p38 pathways[J].Biochem Biophys Res Commun,2016,477(4):1038-1044.
[51]Zeng Y,Kulkarni P,Inoue T,et al.Down-regulating cold shock protein genes impairs cancer cell survival and enhances chemosensitivity[J].J Cell Biochem,2009,107(1):179-188.
[52]Dodds PN,Rathjen JP.Plant immunity:towards an integrated view of plant-pathogen interactions[J].Nat Rev Genet,2010,11(8):539-548.
[53]Rajamuthiah R,Mylonakis E.Effector triggered immunity[J].Virulence,2014,5(7):697-702.
[54]Fu ZQ,Guo M,Jeong BR,et al.A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity[J].Nature,2007,447(7142):284-288.
[55]Nicaise V,Joe A,Jeong BR,et al.Pseudomonas Hop U1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7[J].EMBO J,2013,32(5):701-712.
[56]Qiang X,Yang WL,Wu R,et al.Cold-inducible RNA-binding protein(CIRP)triggers inflammatory responses in hemorrhagic shock and sepsis[J].Nat Med,2013,19(11):1489-1495.
[57]Yang WL,Sharma A,Wang Z,et al.Cold-inducible RNA-binding protein causes endothelial dysfunction via activation of Nlrp3 inflammasome[J].Sci Rep,2016,6:26571.
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[2]Xue JH,Nonoguchi K,Fukumoto M,et al.Effects of ischemia and H2O2on the cold stress protein CIRP expression in rat neuronal cells[J].Free Radic Biol Med,1999,27(11-12):1238-1244.
[3]Matsumoto K,Aoki K,Dohmae N,et al.CIRP2,a major cytoplasmic RNA-binding protein in Xenopus oocytes[J].Nucleic Acids Res,2000,28(23):4689-4697.
[4]Ciuzan O,Hancock J,Pamfil D,et al.The evolutionarily conserved multifunctional glycine-rich RNA-binding proteins play key roles in development and stress adaptation[J].Physiol Plant,2015,153(1):1-11.
[5]De LF,Zhang T,Wauquier C,et al.The cold-inducible RNA-binding protein migrates from the nucleus to cytoplasmic stress granules by a methylation-dependent mechanism and acts as a translational repressor[J].Exp Cell Res,2007,313(20):4130-4144.
[6]Nishiyama H,Itoh K,Kaneko Y,et al.A glycine-rich RNA-binding protein mediating cold-inducible suppression of mammalian cell growth[J].J Cell Biol,1997,137(4):899-908.
[7]Danno S,Nishiyama H,Higashitsuji H,et al.Increased transcript level of RBM3,a member of the glycine-rich RNA-binding protein family,in human cells in response to cold stress[J].Biochem Biophys Res Commun,1997,236(3):804-807.
[8]Hamid AA,Mandai M,Fujita J,et al.Expression of cold-inducible RNA-binding protein in the normal endometrium,endometrial hyperplasia,and endometrial carcinoma[J].Int J Gynecol Pathol,2003,22(3):240-247.
[9]Nishiyama H,Xue JH,Sato T,et al.Diurnal change of the cold-inducible RNA-binding protein(Cirp)expression in mouse brain[J].Biochem Biophys Res Commun,1998,245(2):534-538.
[10]Sugimoto K,Jiang H.Cold stress and light signals induce the expression of cold-inducible RNA binding protein(cirp)in the brain and eye of the Japanese treefrog(Hyla japonica)[J].Comp Biochem Physiol A Mol Integr Physiol,2008,151(4):628-636.
[11]Banks S,King SA,Irvine DS,et al.Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa[J].Reproduction,2005,129(4):505-514.
[12]Yang C,Carrier F.The UV-inducible RNA-binding protein A18(A18 hnRNP)plays a protective role in the genotoxic stress response[J].J Biol Chem,2001,276(50):47277-47284.
[13]Aoki K,Ishii Y,Matsumoto K,et al.Methylation of Xenopus CIRP2 regulates its arginine-and glycine-rich region-mediated nucleocytoplasmic distribution[J].Nucleic Acids Res,2002,30(23):5182-5192.
[14]Sakurai T,Itoh K,Higashitsuji H,et al.Cirp protects against tumor necrosis factor-alpha-induced apoptosis via activation of extracellular signal-regulated kinase[J].Biochim Biophys Acta,2006,1763(3):290-295.
[15]de Zwart LL,Meerman JH,Commandeur JN,et al.Biomarkers of free radical damage applications in experimental animals and in humans[J].Free Radic Biol Med,1999,26(1-2):202-226.
[16]Sheikh MS,Carrier F,Papathanasiou MA,et al.Identification of several human homologs of hamster DNA damage-inducible transcripts.Cloning and characterization of a novel UV-inducible c D-NA that codes for a putative RNA-binding protein[J].J Biol Chem,1997,272(42):26720-26726.
[17]Pan F,Zarate J,Choudhury A,et al.Osmotic stress of salmon stimulates upregulation of a cold inducible RNA binding protein(CIRP)similar to that of mammals and amphibians[J].Biochimie,2004,86(7):451-461.
[18]Nishiyama H,Itoh K,Kaneko Y,et al.A glycine-rich RNA-binding protein mediating cold-inducible suppression of mammalian cell growth[J].J Cell Biol,1997,137(4):899-908.
[19]Li S,Zhang Z,Xue J,et al.Cold-inducible RNA binding protein inhibits H(2)O(2)-induced apoptosis in rat cortical neurons[J].Brain Res,2012,1441:47-52.
[20]Kim JS,Park SJ,Kwak KJ,et al.Cold shock domain proteins and glycine-rich RNA-binding proteins from Arabidopsis thaliana can promote the cold adaptation process in Escherichia coli[J].Nucleic Acids Res,2007,35(2):506-516.
[21]Sharp FR,Bernaudin M.HIF1 and oxygen sensing in the brain[J].Nat Rev Neurosci,2004,5(6):437-448.
[22]Harris AL.Hypoxia--a key regulatory factor in tumour growth[J].Nat Rev Cancer,2002,2(1):38-47.
[23]Sheel AW,Mac Nutt MJ,Querido JS.The pulmonary system during exercise in hypoxia and the cold[J].Exp Physiol,2010,95(3):422-430.
[24]Wellmann S,Buhrer C,Moderegger E,et al.Oxygen-regulated expression of the RNA-binding proteins RBM3 and CIRP by a HIF-1-independent mechanism[J].J Cell Sci,2004,117(Pt 9):1785-1794.
[25]Zhang Q,Wang YZ,Zhang W,et al.Involvement of cold inducible RNA-binding protein in severe hypoxia-induced growth arrest of neural stem cells in vitro[J].Mol Neurobiol,2017,54(3):2143-2153.
[26]Ryan JC,Morey JS,Ramsdell JS,et al.Acute phase gene expression in mice exposed to the marine neurotoxin domoic acid[J].Neuroscience,2005,136(4):1121-1132.
[27]Prieto-Alamo MJ,Abril N,Osuna-Jimenez I,et al.Solea senegalensis genes responding to lipopolysaccharide and copper sulphate challenges:large-scale identification by suppression subtractive hybridization and absolute quantification of transcriptional profiles by real-time RT-PCR[J].Aquat Toxicol,2009,91(4):312-319.
[28]Pan Y,Cui Y,He H,et al.Developmental competence of mature yak vitrified-warmed oocytes is enhanced by IGF-I via modulation of CIRP during in vitro maturation[J].Cryobiology,2015,71(3):493-498.
[29]Jackson TC,Manole MD,Kotermanski SE,et al.Cold stress protein RBM3 responds to temperature change in an ultra-sensitive manner in young neurons[J].Neuroscience,2015,305:268-278.
[30]Morf J,Rey G,Schneider K,et al.Cold-inducible RNA-binding protein modulates circadian gene expression posttranscriptionally[J].Science,2012,338(6105):379-383.
[31]Bellesi M,de Vivo L,Tononi G,et al.Effects of sleep and wake on astrocytes:clues from molecular and ultrastructural studies[J].BMC Biol,2015,13:66.
[32]Nikonova EV,Gilliland JD,Tanis KQ,et al.Transcriptional profiling of cholinergic neurons from basal forebrain identifies changes in expression of genes between sleep and wake:mRNA profiling in basal forebrain with sleep/sleep deprivation[J].Sleep,2017,40(6):ZSX059.
[33]Banks S,King SA,Irvine DS,et al.Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa[J].Reproduction,2005,129(4):505-514.
[34]Peng Y,Yang PH,Tanner JA,et al.Cold-inducible RNA binding protein is required for the expression of adhesion molecules and embryonic cell movement in Xenopus laevis[J].Biochem Biophys Res Commun,2006,344(1):416-424.
[35]Yenari MA,Han HS.Neuroprotective mechanisms of hypothermia in brain ischaemia[J].Nat Rev Neurosci,2012,13(4):267-278.
[36]Alkabie S,Boileau AJ.The role of therapeutic hypothermia after traumatic spinal cord injury-a systematic review[J].World Neurosurg,2016,86:432-449.
[37]Salerian AJ,Saleri NG.Cooling core body temperature may slow down neurodegeneration[J].CNS Spectr,2008,13(3):227-229.
[38]Zhang HT,Xue JH,Zhang ZW,et al.Cold-inducible RNA-binding protein inhibits neuron apoptosis through the suppression of mitochondrial apoptosis[J].Brain Res,2015,1622:474-483.
[39]Kita H,Carmichael J,Swartz J,et al.Modulation of polyglutamineinduced cell death by genes identified by expression profiling[J].Hum Mol Genet,2002,11(19):2279-2287.
[40]Liu A,Zhang Z,Li A,et al.Effects of hypothermia and cerebral ischemia on cold-inducible RNA-binding protein mRNA expression in rat brain[J].Brain Res,2010,1347:104-110.
[41]Sanderson TH,Reynolds CA,Kumar R,et al.Molecular mechanisms of ischemia-reperfusion injury in brain:pivotal role of the mitochondrial membrane potential in reactive oxygen species generation[J].Mol Neurobiol,2013,47(1):9-23.
[42]Liu J,Xue J,Zhang H,et al.Cloning,expression,and purification of cold inducible RNA-binding protein and its neuroprotective mechanism of action[J].Brain Res,2015,1597:189-195.
[43]Zhou M,Yang WL,Ji Y,et al.Cold-inducible RNA-binding protein mediates neuroinflammation in cerebral ischemia[J].Biochim Biophys Acta,2014,1840(7):2253-2261.
[44]Rajayer SR,Jacob A,Yang WL,et al.Cold-inducible RNA-binding protein is an important mediator of alcohol-induced brain inflammation[J].PLo S One,2013,8(11):e79430.
[45]Sakurai T,Yada N,Watanabe T,et al.Cold-inducible RNA-binding protein promotes the development of liver cancer[J].Cancer Sci,2015,106(4):352-358.
[46]Sakurai T,Kashida H,Watanabe T,et al.Stress response protein cirp links inflammation and tumorigenesis in colitis-associated cancer[J].Cancer Res,2014,74(21):6119-6128.
[47]Wang M,Zhang H,Heng X,et al.Expression of cold-inducible RNA-binding protein(CIRP)in pituitary adenoma and its relationships with tumor recurrence[J].Med Sci Monit,2015,21:1256-1260.
[48]Jian F,Chen Y,Ning G,et al.Cold inducible RNA binding protein upregulation in pituitary corticotroph adenoma induces corticotroph cell proliferation via Erk signaling pathway[J].Oncotarget,2016,7(8):9175-9187.
[49]Ren WH,Zhang LM,Liu HQ,et al.Protein overexpression of CIRP and TLR4 in oral squamous cell carcinoma:an immunohistochemical and clinical correlation analysis[J].Med Oncol,2014,31(8):120.
[50]Lee HN,Ahn SM,Jang HH.Cold-inducible RNA-binding protein promotes epithelial-mesenchymal transition by activating ERK and p38 pathways[J].Biochem Biophys Res Commun,2016,477(4):1038-1044.
[51]Zeng Y,Kulkarni P,Inoue T,et al.Down-regulating cold shock protein genes impairs cancer cell survival and enhances chemosensitivity[J].J Cell Biochem,2009,107(1):179-188.
[52]Dodds PN,Rathjen JP.Plant immunity:towards an integrated view of plant-pathogen interactions[J].Nat Rev Genet,2010,11(8):539-548.
[53]Rajamuthiah R,Mylonakis E.Effector triggered immunity[J].Virulence,2014,5(7):697-702.
[54]Fu ZQ,Guo M,Jeong BR,et al.A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity[J].Nature,2007,447(7142):284-288.
[55]Nicaise V,Joe A,Jeong BR,et al.Pseudomonas Hop U1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7[J].EMBO J,2013,32(5):701-712.
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