长链非编码RNA调控自噬的研究进展
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摘要
长链非编码RNA (lncRNA)是转录本长度超过200个核苷酸的RNA分子,不具备蛋白质编码功能。细胞自噬是真核生物的一种高度保守、用来降解和循环再利用细胞内生物大分子或受损细胞器的过程,有助于维持机体内环境稳态。自噬研究是当下生命科学研究的热点,前期研究发现,lncRNA在细胞自噬调控中发挥着重要作用,深入探索lncRNA调控自噬的分子机制及其与疾病发生的关系对预防和治疗多种人类重大疾病具有重要意义。该文就目前为止报道过的部分lncRNA参与自噬调控的最新进展进行归纳总结,以期为lncRNA调控自噬的相关研究及其在肿瘤等疾病治疗中的作用提供参考。
Autophagy is a highly conserved mechanism to maintain the homeostasis in eukaryotes, which is a pathway for the turnover and recycling of intracellular macromoleculars and damaged organelles. Autophagyrelated study is becoming a worldwide hot-spot of life science. Long non-coding RNAs(lncRNAs) are a group of RNAs longer than 200 nucleotides and without protein-coding ability. LncRNA has been shown to play an important role in the regulation of autophagy. It is important to elucidate the cellular mechanism of lncRNA regulating autophagy and the significance of autophagy in disease prevention and treatment. This review summarizes recent progresses in the regulation of autophagy by lncRNAs in order to provide new ideas for the research of autophagy regulated by lncRNA and its application in the treatment of tumors and other diseases.
Autophagy is a highly conserved mechanism to maintain the homeostasis in eukaryotes, which is a pathway for the turnover and recycling of intracellular macromoleculars and damaged organelles. Autophagyrelated study is becoming a worldwide hot-spot of life science. Long non-coding RNAs(lncRNAs) are a group of RNAs longer than 200 nucleotides and without protein-coding ability. LncRNA has been shown to play an important role in the regulation of autophagy. It is important to elucidate the cellular mechanism of lncRNA regulating autophagy and the significance of autophagy in disease prevention and treatment. This review summarizes recent progresses in the regulation of autophagy by lncRNAs in order to provide new ideas for the research of autophagy regulated by lncRNA and its application in the treatment of tumors and other diseases.
引文
[1]Yang Z,Klionsky D J.Eatenalive:a history of macroautophagy.Nat Cell Biol,2010,12:814-22
[2]Mizushima N.Autophagy:process and function.Genes Dev,2007,21:2861-73
[3]Glick D,Barth S,Maclod KF.Autophagy:cellular and molecular mechanisms.J Pathol,2010,221:3-12
[4]Wang Z,Miao G,Xue X,et al.The vici syndrome protein EPG5 is a Rab7 effector that determines the fusion specificity of autophagosomes with late endosomes/lysosomes.Mol Cell,2016,63:781-95
[5]Riley T,Sontag E,Chen P,et al.Transcriptional control of human p53-regulated genes.Nat Rev Mol Cell Biol,2008,9:402-12
[6]Debanth J,Baehrrecke EH,Kronmer G.Does autophagy contribute to cell death?Autophagy,2005,1:66-74
[7]Bento CF,Renna M,Ghislat G,et al.Mammalian autophagy:how does it work?Annu Rev Biochem,2016,85:685-713
[8]Kroemer G,Levine B.Autophagic cell death:the story of a misnomer.Nat Rev Mol Cell Biol,2008,9:1004-10
[9]Xu F,FangY,Yan L,et al.Nuclear localization of Beclin 1promotes radiation-induced DNA damage repair independent of autophagy.Sci Rep,2017,7:453-85
[10]Tang H,Da L,Mao Y,et al.Hepatitis B virus X protein sensitizes cells to starvation-induced autophagy via upregulation of beclin 1 expression.Hepatology,2009,49:60-7
[11]Mizushima N,Yoshimori T,Ohsumi Y.The role of Atg proteins in autophagosome formation.Annu Rev Cell Dev Biol,2011,27:107-32
[12]Parzych KR,Klionsky YDJ.An overview of autophagy:morphology,mechanism,and regulation.Antioxid Redox Signal,2014,20:460-73
[13]Alers S,Loffler AS,Wesselborg S,et al.Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy:Cross talk,shortcuts,and feedbacks.Mol Cell Biol,2011,32:2-11
[14]Kim J,Kundu M,Viollet B,et al.AMPK and mTORregulate autophagy through direct phosphorylation of Ulk1.Nat Cell Biol,2011,13:132-41
[15]Heras-Sandoval D,Perez-Rojas JM,Hernandez-Damian J,et al.The role of PI3K/AKT/mTOR pathway in the modulation of autophagy and the clearance of protein aggregates in neurodegeneration.Cell Signal,2014,26:2694-701
[16]Yamamoto H,Fujioka Y,Suzuki SW,et al.The intrinsically disordered protein Atg13 mediates supramolecular assembly of autophagy initiation complexes.Dev Cell,2016,38:86-99
[17]Yang Z,Klionsky DJ.An overview of the molecular mechanism of autophagy.Curr Top Microbiol Immunol,2009,335:1-32
[18]Backer JM.The regulation and function of class III PI3Ks:novel roles for Vps34.Biochem J,2008,410:1-17
[19]Geng J,Klionsky DJ.The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy.‘protein modifications:beyond the usual suspects’review series.EMBO Rep,2008,9:859-64
[20]Kroemer G,Marino G,Levine B.Autophagy and the integrated stress response.Mol Cell,2010,40:280-93
[21]Eskelinen EL.Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy.Mol Aspects Med,2006,27:495-502
[22]Pankiv S,Clausen TH,Lamark T,et al.p62/SQSTM1binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy.J Biol Chem,2007,282:24131-45
[23]Mcewan DG,Popovic D,Gubas A,et al.Plekhmi regulates autophagosome-lysosome fusion through HOPScomplex and LC3/GABARAP proteins.Mol Cell,2015,57:39-54
[24]ENCODE Project Consortium.An integrated encyclopedia of DNA elements in the human genome.Nature,2012,489:57-74
[25]Clemson CM,Mceil JA,Willard F,et al.XIST RNApaints the inactive X chromosome at interphase:evidence for a novel RNA involved in nuclear/chromosome structure.J Cell Biol,1996,132:259-75
[26]Mohannad F,Mondal T,Guseva N,et al.Kcnq1ot1noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1.Development,2010,137:2493-9
[27]Lai F,Orom UA,Cesaroni M,et al.Activating RNAs associate with mediator to enhance chromatin architecture and transcription.Nature,2013,494:497-501
[28]St.Laurent G,Wahlestedt C,Karranov P.The landscape of long noncoding RNA classification.Trends Genet,2015,31:239-51
[29]Gabory A,Ripoche MA,Yoshimizu T,et al.The H19gene:regulation and function of a non-coding RNA.Cytogenet Genome Res,2006,113:188-93
[30]Zhuo C,Jiang R,Lin X,et al.LncRNA H19 inhibits autophagy by epigenetically silencing of DIRAS3 in diabetic cardiomyopathy.Oncotarget,2017,8:1429-37
[31]Liu X,Xiao ZD,Han L,et al.LncRNA NBR2 engages a metabolic checkpoint by regulating AMPK under energy stress.Nat Cell Biol,2016,18:431-42
[32]Pawar K,Hanisch C,Palma Vera SE,et al.Down regulated lncRNA MEG3 eliminates mycobacteria in macrophages via autophagy.Sci Rep,2016,6:19416-28
[33]Ying L,Huang Y,Chen H,et al.Downregulated MEG3activates autophagy and increases cell proliferation in bladder cancer.Mol Biosyst,2013,9:407-11
[34]Xiu YL,Sun KX,Chen X,et al.Upregulation of the lncRNA Meg3 induces autophagy to inhibit tumorigenesis and progression of epithelial ovarian carcinoma by regulating activity of ATG3.Oncotarget,2017,8:31714-25
[35]Chen CL,Tseng YW,Wu JC,et al.Suppression of hepatocellular carcinoma by baculovirus-mediated expression of long non-coding RNA PTENP1 and MicroRNA regulation.Biomaterials,2015,44:71-81
[36]Ge D,Han L,Huang S,et al.Identification of a novel m TOR activator and discovery of a competing endogenous RNA regulating autophagy in vascular endothelial cells.Autophagy,2014,10:957-71
[37]Lu W,Han L,Su L,et al.A 3′UTR-associated RNA,FLJ11812 maintains stemness of human embryonic stem cells by targeting miR-4459.Stem Cell Dev,2015,24:1133-40
[38]Wang Y,Hu Y,Sun C,et al.Down-regulation of Risa improves insulin sensitivity by enhancing autophagy.FASEB J,2016,30:3133-45
[39]Chen YM,Liu Y,Wei HY,et al.Large intergenic noncoding RNA-ROR reverses gemcitabine-induced autophagy and apoptosis in breast cancer cells.Oncotarget,2016,7:59604-17
[40]Mourtada-Maarabouni M,Hasan AM,Farzaneh F,et al.Inhibition of human T-cell proliferation by mammalian target of rapamycin(mTOR)antagonists requires noncoding RNA growth-arrest-specific transcript 5(GAS5).Mol Pharmacol,2010,78:19-28
[41]Song J,Ahn C,Chun CH,et al.A long non-coding RNA,GAS5,plays a critical role in the regulation of miR-21during osteoarthritis.J Orthop Res,2014,32:1628-35
[42]Loomis D,Grosse Y,Lauby-Secretan B,et al.The carcinogenicity of outdoor air pollution.Lancet Oncol,2013,14:1262-3
[43]Hamra GB,Guha N,Cohen A,et al.Outdoor particulate matter exposure and lung cancer:a systematic review and meta-analysis.Environ Health Perspect,2014,122:906-11
[44]Deng X,Feng N,Zheng M,et al.PM2.5 exposure-induced autophagy is mediated by lncRNA loc146880 which also promotes the migration and invasion of lung cancer cells.Biochim Biophys Acta,2017,1861:112-25
[45]Fu X,Ravundranath L,Tran N,et al.Regulation of apoptosis by a prostate-specific and prostate cancerassociated noncoding gene,PCGEM1.DNA Cell Biol,2006,25:135-41
[46]Liu CY,Zhang YH,Li RB,et al.LncRNA CAIF inhibits autophagy and attenuates myocardial infarction by blocking p53-mediated myocardin transcription.Nat Commun,2018,9:29
[47]Hajjari M,Salavaty A.Hotair:an oncogenic long noncoding RNA in different cancers.Cancer Biol Med,2015,12:1-9
[48]Yang L,Zhang X,Li H,et al.The long noncoding RNAHOTAIR activates autophagy by upregulating ATG3 and ATG7 in hepatocellular carcinoma.Mol Biosyst,2016,12:2605-12
[49]Panzitt K,Tscherantsch MM,Guelly C,et al.Characterization of HULC,a novel gene with striking upregulation in hepatocellular carcinoma,as noncoding RNA.Gastroenterology,2007,132:330-42
[50]Zhao Y,Guo Q,Chen J,et al.Role of long non-coding RNA HULC in cell proliferation,apoptosis and tumor metastasis of gastric cancer:a clinical and in vitro investigation.Oncol Rep,2014,31:358-64
[51]Xiong H,Ni Z,He J,et al.LncRNA HULC triggers autophagy via stabilizing Sirt1 and attenuates the chemosensitivity of HCC cells.Oncogene,2017,36:3528-40
[52]Wang K,Liu CY,Zhou LY,et al.APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p.Nat Commun,2015,6:6779
[53]Liu Z,Wer X,Zhang A,et al.Long non-coding RNAHNF1A-AS1 functioned as an oncogene and autophagy promoter in hepatocellular carcinoma through sponging hsa-miR-30b-5p.Biochem Biophys Res Commun,2016,473:1268-75
[54]Gutschner T,Hammerle M,Diederichs S.MALATI-a paradigm for long noncoding RNA function in cancer.JMol Med(Berl),2013,91:791-801
[55]Li L,Chen H,Gao Y,et al.Long noncoding RNAMALAT1 promotes aggressive pancreatic cancer proliferation and metastasis via the stimulation of autophagy.Mol Cancer Ther,2016,15:2232-43
[56]Yuan P,Cao W,Zang Q,et al.The HIF-2α-MALAT1-miR-216b axis regulates multi-drug resistance of hepatocellular carcinoma cells via modulating autophagy.Biochem Biophys Res Commun,2016,478:1067-73
[57]Viereck J,Kumarswamy R,Foinquinos A,et al.Long noncoding RNA Chast promotes cardiac remodeling.Sci Transl Med,2016,8:326ra22
[58]Tay Y,Rinn J,Pandolfi PP.The multilayered complexity of ceRNA crosstalk and competition.Nature,2014,505:344-52
[59]Yoon JH,Abdelmohsen K,Gorospe M.Functional interactions among microRNAs and long noncoding RNAs.Semin Cell Dev Biol,2014,34:9-14
[2]Mizushima N.Autophagy:process and function.Genes Dev,2007,21:2861-73
[3]Glick D,Barth S,Maclod KF.Autophagy:cellular and molecular mechanisms.J Pathol,2010,221:3-12
[4]Wang Z,Miao G,Xue X,et al.The vici syndrome protein EPG5 is a Rab7 effector that determines the fusion specificity of autophagosomes with late endosomes/lysosomes.Mol Cell,2016,63:781-95
[5]Riley T,Sontag E,Chen P,et al.Transcriptional control of human p53-regulated genes.Nat Rev Mol Cell Biol,2008,9:402-12
[6]Debanth J,Baehrrecke EH,Kronmer G.Does autophagy contribute to cell death?Autophagy,2005,1:66-74
[7]Bento CF,Renna M,Ghislat G,et al.Mammalian autophagy:how does it work?Annu Rev Biochem,2016,85:685-713
[8]Kroemer G,Levine B.Autophagic cell death:the story of a misnomer.Nat Rev Mol Cell Biol,2008,9:1004-10
[9]Xu F,FangY,Yan L,et al.Nuclear localization of Beclin 1promotes radiation-induced DNA damage repair independent of autophagy.Sci Rep,2017,7:453-85
[10]Tang H,Da L,Mao Y,et al.Hepatitis B virus X protein sensitizes cells to starvation-induced autophagy via upregulation of beclin 1 expression.Hepatology,2009,49:60-7
[11]Mizushima N,Yoshimori T,Ohsumi Y.The role of Atg proteins in autophagosome formation.Annu Rev Cell Dev Biol,2011,27:107-32
[12]Parzych KR,Klionsky YDJ.An overview of autophagy:morphology,mechanism,and regulation.Antioxid Redox Signal,2014,20:460-73
[13]Alers S,Loffler AS,Wesselborg S,et al.Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy:Cross talk,shortcuts,and feedbacks.Mol Cell Biol,2011,32:2-11
[14]Kim J,Kundu M,Viollet B,et al.AMPK and mTORregulate autophagy through direct phosphorylation of Ulk1.Nat Cell Biol,2011,13:132-41
[15]Heras-Sandoval D,Perez-Rojas JM,Hernandez-Damian J,et al.The role of PI3K/AKT/mTOR pathway in the modulation of autophagy and the clearance of protein aggregates in neurodegeneration.Cell Signal,2014,26:2694-701
[16]Yamamoto H,Fujioka Y,Suzuki SW,et al.The intrinsically disordered protein Atg13 mediates supramolecular assembly of autophagy initiation complexes.Dev Cell,2016,38:86-99
[17]Yang Z,Klionsky DJ.An overview of the molecular mechanism of autophagy.Curr Top Microbiol Immunol,2009,335:1-32
[18]Backer JM.The regulation and function of class III PI3Ks:novel roles for Vps34.Biochem J,2008,410:1-17
[19]Geng J,Klionsky DJ.The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy.‘protein modifications:beyond the usual suspects’review series.EMBO Rep,2008,9:859-64
[20]Kroemer G,Marino G,Levine B.Autophagy and the integrated stress response.Mol Cell,2010,40:280-93
[21]Eskelinen EL.Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy.Mol Aspects Med,2006,27:495-502
[22]Pankiv S,Clausen TH,Lamark T,et al.p62/SQSTM1binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy.J Biol Chem,2007,282:24131-45
[23]Mcewan DG,Popovic D,Gubas A,et al.Plekhmi regulates autophagosome-lysosome fusion through HOPScomplex and LC3/GABARAP proteins.Mol Cell,2015,57:39-54
[24]ENCODE Project Consortium.An integrated encyclopedia of DNA elements in the human genome.Nature,2012,489:57-74
[25]Clemson CM,Mceil JA,Willard F,et al.XIST RNApaints the inactive X chromosome at interphase:evidence for a novel RNA involved in nuclear/chromosome structure.J Cell Biol,1996,132:259-75
[26]Mohannad F,Mondal T,Guseva N,et al.Kcnq1ot1noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1.Development,2010,137:2493-9
[27]Lai F,Orom UA,Cesaroni M,et al.Activating RNAs associate with mediator to enhance chromatin architecture and transcription.Nature,2013,494:497-501
[28]St.Laurent G,Wahlestedt C,Karranov P.The landscape of long noncoding RNA classification.Trends Genet,2015,31:239-51
[29]Gabory A,Ripoche MA,Yoshimizu T,et al.The H19gene:regulation and function of a non-coding RNA.Cytogenet Genome Res,2006,113:188-93
[30]Zhuo C,Jiang R,Lin X,et al.LncRNA H19 inhibits autophagy by epigenetically silencing of DIRAS3 in diabetic cardiomyopathy.Oncotarget,2017,8:1429-37
[31]Liu X,Xiao ZD,Han L,et al.LncRNA NBR2 engages a metabolic checkpoint by regulating AMPK under energy stress.Nat Cell Biol,2016,18:431-42
[32]Pawar K,Hanisch C,Palma Vera SE,et al.Down regulated lncRNA MEG3 eliminates mycobacteria in macrophages via autophagy.Sci Rep,2016,6:19416-28
[33]Ying L,Huang Y,Chen H,et al.Downregulated MEG3activates autophagy and increases cell proliferation in bladder cancer.Mol Biosyst,2013,9:407-11
[34]Xiu YL,Sun KX,Chen X,et al.Upregulation of the lncRNA Meg3 induces autophagy to inhibit tumorigenesis and progression of epithelial ovarian carcinoma by regulating activity of ATG3.Oncotarget,2017,8:31714-25
[35]Chen CL,Tseng YW,Wu JC,et al.Suppression of hepatocellular carcinoma by baculovirus-mediated expression of long non-coding RNA PTENP1 and MicroRNA regulation.Biomaterials,2015,44:71-81
[36]Ge D,Han L,Huang S,et al.Identification of a novel m TOR activator and discovery of a competing endogenous RNA regulating autophagy in vascular endothelial cells.Autophagy,2014,10:957-71
[37]Lu W,Han L,Su L,et al.A 3′UTR-associated RNA,FLJ11812 maintains stemness of human embryonic stem cells by targeting miR-4459.Stem Cell Dev,2015,24:1133-40
[38]Wang Y,Hu Y,Sun C,et al.Down-regulation of Risa improves insulin sensitivity by enhancing autophagy.FASEB J,2016,30:3133-45
[39]Chen YM,Liu Y,Wei HY,et al.Large intergenic noncoding RNA-ROR reverses gemcitabine-induced autophagy and apoptosis in breast cancer cells.Oncotarget,2016,7:59604-17
[40]Mourtada-Maarabouni M,Hasan AM,Farzaneh F,et al.Inhibition of human T-cell proliferation by mammalian target of rapamycin(mTOR)antagonists requires noncoding RNA growth-arrest-specific transcript 5(GAS5).Mol Pharmacol,2010,78:19-28
[41]Song J,Ahn C,Chun CH,et al.A long non-coding RNA,GAS5,plays a critical role in the regulation of miR-21during osteoarthritis.J Orthop Res,2014,32:1628-35
[42]Loomis D,Grosse Y,Lauby-Secretan B,et al.The carcinogenicity of outdoor air pollution.Lancet Oncol,2013,14:1262-3
[43]Hamra GB,Guha N,Cohen A,et al.Outdoor particulate matter exposure and lung cancer:a systematic review and meta-analysis.Environ Health Perspect,2014,122:906-11
[44]Deng X,Feng N,Zheng M,et al.PM2.5 exposure-induced autophagy is mediated by lncRNA loc146880 which also promotes the migration and invasion of lung cancer cells.Biochim Biophys Acta,2017,1861:112-25
[45]Fu X,Ravundranath L,Tran N,et al.Regulation of apoptosis by a prostate-specific and prostate cancerassociated noncoding gene,PCGEM1.DNA Cell Biol,2006,25:135-41
[46]Liu CY,Zhang YH,Li RB,et al.LncRNA CAIF inhibits autophagy and attenuates myocardial infarction by blocking p53-mediated myocardin transcription.Nat Commun,2018,9:29
[47]Hajjari M,Salavaty A.Hotair:an oncogenic long noncoding RNA in different cancers.Cancer Biol Med,2015,12:1-9
[48]Yang L,Zhang X,Li H,et al.The long noncoding RNAHOTAIR activates autophagy by upregulating ATG3 and ATG7 in hepatocellular carcinoma.Mol Biosyst,2016,12:2605-12
[49]Panzitt K,Tscherantsch MM,Guelly C,et al.Characterization of HULC,a novel gene with striking upregulation in hepatocellular carcinoma,as noncoding RNA.Gastroenterology,2007,132:330-42
[50]Zhao Y,Guo Q,Chen J,et al.Role of long non-coding RNA HULC in cell proliferation,apoptosis and tumor metastasis of gastric cancer:a clinical and in vitro investigation.Oncol Rep,2014,31:358-64
[51]Xiong H,Ni Z,He J,et al.LncRNA HULC triggers autophagy via stabilizing Sirt1 and attenuates the chemosensitivity of HCC cells.Oncogene,2017,36:3528-40
[52]Wang K,Liu CY,Zhou LY,et al.APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p.Nat Commun,2015,6:6779
[53]Liu Z,Wer X,Zhang A,et al.Long non-coding RNAHNF1A-AS1 functioned as an oncogene and autophagy promoter in hepatocellular carcinoma through sponging hsa-miR-30b-5p.Biochem Biophys Res Commun,2016,473:1268-75
[54]Gutschner T,Hammerle M,Diederichs S.MALATI-a paradigm for long noncoding RNA function in cancer.JMol Med(Berl),2013,91:791-801
[55]Li L,Chen H,Gao Y,et al.Long noncoding RNAMALAT1 promotes aggressive pancreatic cancer proliferation and metastasis via the stimulation of autophagy.Mol Cancer Ther,2016,15:2232-43
[56]Yuan P,Cao W,Zang Q,et al.The HIF-2α-MALAT1-miR-216b axis regulates multi-drug resistance of hepatocellular carcinoma cells via modulating autophagy.Biochem Biophys Res Commun,2016,478:1067-73
[57]Viereck J,Kumarswamy R,Foinquinos A,et al.Long noncoding RNA Chast promotes cardiac remodeling.Sci Transl Med,2016,8:326ra22
[58]Tay Y,Rinn J,Pandolfi PP.The multilayered complexity of ceRNA crosstalk and competition.Nature,2014,505:344-52
[59]Yoon JH,Abdelmohsen K,Gorospe M.Functional interactions among microRNAs and long noncoding RNAs.Semin Cell Dev Biol,2014,34:9-14