دورية أكاديمية
Circular RNA expression profile and functional analysis of circUvrag in light-induced photoreceptor degeneration.
العنوان: | Circular RNA expression profile and functional analysis of circUvrag in light-induced photoreceptor degeneration. |
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المؤلفون: | Kong K; Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai, China.; Shanghai Key Laboratory of Visual Impairment and Restoration, Eye and ENT Hospital of Fudan University, Shanghai, China., Ding X; Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai, China.; Shanghai Key Laboratory of Visual Impairment and Restoration, Eye and ENT Hospital of Fudan University, Shanghai, China., Wang Y; Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai, China.; Shanghai Key Laboratory of Visual Impairment and Restoration, Eye and ENT Hospital of Fudan University, Shanghai, China., Xu S; Department of Ophthalmology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, China., Li G; Research Center, Eye and ENT Hospital of Fudan University, Shanghai, China., Wang X; Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai, China.; Shanghai Key Laboratory of Visual Impairment and Restoration, Eye and ENT Hospital of Fudan University, Shanghai, China., Zhang M; Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai, China.; Shanghai Key Laboratory of Visual Impairment and Restoration, Eye and ENT Hospital of Fudan University, Shanghai, China., Ni Y; Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai, China.; Shanghai Key Laboratory of Visual Impairment and Restoration, Eye and ENT Hospital of Fudan University, Shanghai, China., Xu G; Department of Ophthalmology, Eye and ENT Hospital of Fudan University, Shanghai, China.; Shanghai Key Laboratory of Visual Impairment and Restoration, Eye and ENT Hospital of Fudan University, Shanghai, China. |
المصدر: | Clinical & experimental ophthalmology [Clin Exp Ophthalmol] 2024 Jul; Vol. 52 (5), pp. 558-575. Date of Electronic Publication: 2024 Jan 28. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Wiley-Blackwell Pub. Asia Country of Publication: Australia NLM ID: 100896531 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1442-9071 (Electronic) Linking ISSN: 14426404 NLM ISO Abbreviation: Clin Exp Ophthalmol Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Carlton, Vic. : Wiley-Blackwell Pub. Asia Original Publication: Carlton, Vic. : Blackwell Science Asia, c2000- |
مواضيع طبية MeSH: | Rats, Sprague-Dawley* , RNA, Circular*/genetics , Retinal Degeneration*/genetics , Retinal Degeneration*/metabolism , Retinal Degeneration*/etiology , Retinal Degeneration*/physiopathology , Apoptosis* , Photoreceptor Cells, Vertebrate*/pathology , Photoreceptor Cells, Vertebrate*/metabolism , Light*/adverse effects , RNA*/genetics, Animals ; Rats ; In Situ Hybridization, Fluorescence ; Gene Expression Regulation ; Disease Models, Animal ; Electroretinography ; Radiation Injuries, Experimental/genetics ; Radiation Injuries, Experimental/metabolism ; Real-Time Polymerase Chain Reaction ; Gene Expression Profiling ; In Situ Nick-End Labeling ; Male ; Flow Cytometry |
مستخلص: | Background: Circular RNAs (circRNAs) are implicated in retinal pathophysiology; however, their expression profiles and functions in photoreceptor apoptosis are largely unknown. We explored circRNA-expression profiles and circUvrag (host gene: Uvrag, ultraviolet radiation resistance associated gene) function in light-induced photoreceptor apoptosis. Methods: Sprague-Dawley rats and 661 W photoreceptor cells were exposed to blue light to establish light-induced photoreceptor degeneration. Differentially expressed circRNAs were identified using microarrays. Potential functions of dysregulated circRNAs were analysed using Gene Ontology and Kyoto Encyclopedia of Genes and Genomes analyses. CircUvrag expression and localization were evaluated using quantitative RT-PCR and fluorescence in situ hybridization, respectively. CircUvrag overexpression and knockdown were induced using a plasmid and a small interfering RNA, respectively, and retinal function and structure were assessed using scotopic electroretinography, haematoxylin-eosin staining, and TUNEL staining. Microglial migration was assessed using IBA1 immunostaining. The apoptosis ratio of photoreceptor cells in vitro was detected using flow cytometry. Results: We identified 764 differentially expressed circRNAs, which were potentially related with the development of retinal structures, including neurons, dendrites, and synapses, and might participate in nervous-system pathophysiology. Light exposure enriched circUvrag in the cytoplasm of photoreceptors in the outer nuclear layer (ONL). CircUvrag knockdown decreased photoreceptor apoptosis and microglial migration to the ONL after light exposure, preserving ONL thickness and a-wave amplitude. In vitro, circUvrag knockdown inhibited photoreceptor apoptosis, although circUvrag overexpression slightly promoted photoreceptor apoptosis. Conclusions: CircUvrag knockdown attenuated light-induced photoreceptor apoptosis, and might be a potential target in retinal degeneration. (© 2024 Royal Australian and New Zealand College of Ophthalmologists.) |
References: | Bharti K, Rao M, Hull SC, et al. Developing cellular therapies for retinal degenerative diseases. Invest Ophthalmol Vis Sci. 2014;55(2):1191‐1202. Al‐Ubaidi MR, Naash MI, Conley SM. A perspective on the role of the extracellular matrix in progressive retinal degenerative disorders. Invest Ophthalmol Vis Sci. 2013;54(13):8119‐8124. Assi L, Chamseddine F, Ibrahim P, et al. A global assessment of eye health and quality of life: a systematic review of systematic reviews. JAMA Ophthalmol. 2021;139(5):526‐541. Wang Y, Sun W, Zhou J, et al. Different phenotypes represent advancing stages of ABCA4‐associated retinopathy: a longitudinal study of 212 Chinese families from a tertiary center. Invest Ophthalmol Vis Sci. 2022;63(5):28. Mauschitz MM, Schmitz MT, Verzijden T, et al. Physical activity, incidence, and progression of age‐related macular degeneration: a multicohort study. Am J Ophthalmol. 2022;236:99‐106. Pondorfer SG, Terheyden JH, Overhoff H, Stasch‐Bouws J, Holz FG, Finger RP. Development of the vision impairment in low luminance questionnaire. Transl Vis Sci Technol. 2021;10(1):5. Remé CE, Grimm C, Hafezi F, Marti A, Wenzel A. Apoptotic cell death in retinal degenerations. Prog Retin Eye Res. 1998;17(4):443‐464. Wong P. Apoptosis, retinitis pigmentosa, and degeneration. Biochem Cell Biol. 1994;72(11–12):489‐498. Hanus J, Anderson C, Wang S. RPE necroptosis in response to oxidative stress and in AMD. Ageing Res Rev. 2015;24:286‐298. Wenzel A, Grimm C, Samardzija M, Remé CE. Molecular mechanisms of light‐induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog Retin Eye Res. 2005;24(2):275‐306. Jones MK, Lu B, Girman S, Wang S. Cell‐based therapeutic strategies for replacement and preservation in retinal degenerative diseases. Prog Retin Eye Res. 2017;58:1‐27. Rasoulinejad SA, Maroufi F. CRISPR‐based genome editing as a new therapeutic tool in retinal diseases. Mol Biotechnol. 2021;63(9):768‐779. Gasparini SJ, Llonch S, Borsch O, Ader M. Transplantation of photoreceptors into the degenerative retina: current state and future perspectives. Prog Retin Eye Res. 2019;69:1‐37. Botto C, Rucli M, Tekinsoy MD, Pulman J, Sahel JA, Dalkara D. Early and late stage gene therapy interventions for inherited retinal degenerations. Prog Retin Eye Res. 2022;86:100975. Huang A, Zheng H, Wu Z, Chen M, Huang Y. Circular RNA‐protein interactions: functions, mechanisms, and identification. Theranostics. 2020;10(8):3503‐3517. Kristensen LS, Andersen MS, Stagsted LVW, Ebbesen KK, Hansen TB, Kjems J. The biogenesis, biology and characterization of circular RNAs. Nat Rev Genet. 2019;20(11):675‐691. Liu Y, Yang Y, Wang Z, et al. Insights into the regulatory role of circRNA in angiogenesis and clinical implications. Atherosclerosis. 2020;298:14‐26. Sun LF, Chen XJ, Jin ZB. Emerging roles of non‐coding RNAs in retinal diseases: a review. Clin Exp Ophthalmol. 2020;48(8):1085‐1101. Carrella S, Banfi S, Karali M. Sophisticated gene regulation for a complex physiological system: the role of non‐coding RNAs in photoreceptor cells. Front Cell Dev Biol. 2020;8:629158. Gu Y, Ke G, Wang L, Zhou E, Zhu K, Wei Y. Altered expression profile of circular RNAs in the serum of patients with diabetic retinopathy revealed by microarray. Ophthalmic Res. 2017;58(3):176‐184. Chen X, Wang Y, Wang JN, et al. m(6)A modification of circSPECC1 suppresses RPE oxidative damage and maintains retinal homeostasis. Cell Rep. 2022;41(7):111671. Beilerli A, Gareev I, Beylerli O, et al. Circular RNAs as biomarkers and therapeutic targets in cancer. Semin Cancer Biol. 2022;83:242‐252. Patop IL, Kadener S. circRNAs in cancer. Curr Opin Genet Dev. 2018;48:121‐127. Chen S, Deng X, Sheng H, et al. Noncoding RNAs in pediatric brain tumors: molecular functions and pathological implications. Mol Ther Nucleic Acids. 2021;3(26):417‐431. Chen J, Chen T, Zhu Y, et al. circPTN sponges miR‐145‐5p/miR‐330‐5p to promote proliferation and stemness in glioma. J Exp Clin Cancer Res. 2019;38(1):398. Zhang W, Chen S, Du Q, et al. CircVPS13C promotes pituitary adenoma growth by decreasing the stability of IFITM1 mRNA via interacting with RRBP1. Oncogene. 2022;41(11):1550‐1562. Puri S, Hu J, Sun Z, et al. Identification of circRNAs linked to Alzheimer's disease and related dementias. Alzheimers Dement. 2023;19(8):3389‐3405. Zhou M, Li S, Huang C. Physiological and pathological functions of circular RNAs in the nervous system. Neural Regen Res. 2024;19(2):342‐349. Xiong W, Li D, Feng Y, Jia C, Zhang X, Liu Z. CircLPAR1 promotes neuroinflammation and oxidative stress in APP/PS1 mice by inhibiting SIRT1/Nrf‐2/HO‐1 axis through destabilizing GDF‐15 mRNA. Mol Neurobiol. 2023;60(4):2236‐2251. Song C, Zhang Y, Huang W, et al. Circular RNA Cwc27 contributes to Alzheimer's disease pathogenesis by repressing Pur‐α activity. Cell Death Differ. 2022;29(2):393‐406. Meng S, Wang B, Li W. CircAXL knockdown alleviates Aβ(1‐42)‐induced neurotoxicity in Alzheimer's disease via repressing PDE4A by releasing miR‐1306‐5p. Neurochem Res. 2022;47(6):1707‐1720. Sun YN, Liu B, Wang JJ, et al. Identification of aberrantly expressed circular RNAs in hyperlipidemia‐induced retinal vascular dysfunction in mice. Genomics. 2021;113(1 Pt 2):593‐600. Yao MD, Zhu Y, Zhang QY, et al. CircRNA expression profile and functional analysis in retinal ischemia‐reperfusion injury. Genomics. 2021;113(3):1482‐1490. Sun LF, Ma Y, Ji YY, et al. Circular Rims2 deficiency causes retinal degeneration. Adv Biol (Weinh). 2021;5(12):e2100906. Zhang R, Feng Y, Lu J, Ge Y, Li H. lncRNA Ttc3‐209 promotes the apoptosis of retinal ganglion cells in retinal ischemia reperfusion injury by targeting the miR‐484/Wnt8a axis. Invest Ophthalmol Vis Sci. 2021;62(3):13. Kleinman ME, Yamada K, Takeda A, et al. Sequence‐ and target‐independent angiogenesis suppression by siRNA via TLR3. Nature. 2008;452(7187):591‐597. Ni YQ, Xu GZ, Hu WZ, Shi L, Qin YW, Da CD. Neuroprotective effects of naloxone against light‐induced photoreceptor degeneration through inhibiting retinal microglial activation. Invest Ophthalmol Vis Sci. 2008;49(6):2589‐2598. Zhang M, Xu G, Liu W, Ni Y, Zhou W. Role of fractalkine/CX3CR1 interaction in light‐induced photoreceptor degeneration through regulating retinal microglial activation and migration. PLoS One. 2012;7(4):e35446. Tang W, Ma J, Gu R, Lei B, Ding X, Xu G. Light‐induced lipocalin 2 facilitates cellular apoptosis by positively regulating reactive oxygen species/bim signaling in retinal degeneration. Invest Ophthalmol Vis Sci. 2018;59(15):6014‐6025. Ross CJ, Towfic F, Shankar J, et al. A pharmacogenetic signature of high response to Copaxone in late‐phase clinical‐trial cohorts of multiple sclerosis. Genome Med. 2017;9(1):50. Xu C, Wu J, Wu Y, et al. TNF‐α‐dependent neuronal necroptosis regulated in Alzheimer's disease by coordination of RIPK1‐p62 complex with autophagic UVRAG. Theranostics. 2021;11(19):9452‐9469. Wang H, Sun T, Hu J, et al. miR‐33a promotes glioma‐initiating cell self‐renewal via PKA and NOTCH pathways. J Clin Invest. 2014;124(10):4489‐4502. Cao P, Dai Q, Deng C, et al. Genome‐wide signatures of mammalian skin covering evolution. Sci China Life Sci. 2021;64(10):1765‐1780. Bishnu A, Phadte P, Dhadve A, Sakpal A, Rekhi B, Ray P. Molecular imaging of the kinetics of hyperactivated ERK1/2‐mediated autophagy during acquirement of chemoresistance. Cell Death Dis. 2021;12(2):161. Ajazi A, Bruhn C, Shubassi G, et al. Endosomal trafficking and DNA damage checkpoint kinases dictate survival to replication stress by regulating amino acid uptake and protein synthesis. Dev Cell. 2021;56(18):2607‐2622.e6. Kim JK, Lee HM, Park KS, et al. MIR144* inhibits antimicrobial responses against Mycobacterium tuberculosis in human monocytes and macrophages by targeting the autophagy protein DRAM2. Autophagy. 2017;13(2):423‐441. Song Y, Quach C, Liang C. UVRAG in autophagy, inflammation, and cancer. Autophagy. 2020;16(2):387‐388. Yang Y, He S, Wang Q, et al. Autophagic UVRAG promotes UV‐induced photolesion repair by activation of the CRL4(DDB2) E3 ligase. Mol Cell. 2016;62(4):507‐519. Liu Z, Lou Y, Cui JC, et al. Circular RNA UVRAG mediated by alternative splicing factor NOVA1 regulates adhesion and migration of vascular smooth muscle cells. Genes (Basel). 2021;12(3):418. Yang C, Wu S, Wu X, Zhou X, Jin S, Jiang H. Silencing circular RNA UVRAG inhibits bladder cancer growth and metastasis by targeting the microRNA‐223/fibroblast growth factor receptor 2 axis. Cancer Sci. 2019;110(1):99‐106. Chen G, Qian HM, Chen J, Wang J, Guan JT, Chi ZL. Whole transcriptome sequencing identifies key circRNAs, lncRNAs, and miRNAs regulating neurogenesis in developing mouse retina. BMC Genomics. 2021;22(1):779. Chaabane M, Andreeva K, Hwang JY, Kook TL, Park JW, Cooper NGF. seekCRIT: detecting and characterizing differentially expressed circular RNAs using high‐throughput sequencing data. PLoS Comput Biol. 2020;16(10):e1008338. Chen X, Hu J. Long noncoding RNA 3632454L22Rik contributes to corneal epithelial wound healing by sponging miR‐181a‐5p in diabetic mice. Invest Ophthalmol Vis Sci. 2021;62(14):16. Ghavami S, Shojaei S, Yeganeh B, et al. Autophagy and apoptosis dysfunction in neurodegenerative disorders. Prog Neurobiol. 2014;112:24‐49. McKnight NC, Zhong Y, Wold MS, et al. Beclin 1 is required for neuron viability and regulates endosome pathways via the UVRAG‐VPS34 complex. PLoS Genet. 2014;10(10):e1004626. Xu S, Zhang P, Zhang M, et al. Synaptic changes and the response of microglia in a light‐induced photoreceptor degeneration model. Mol Vis. 2021;27:206‐220. Feng C, Wang X, Liu T, Zhang M, Xu G, Ni Y. Expression of CCL2 and its receptor in activation and migration of microglia and monocytes induced by photoreceptor apoptosis. Mol Vis. 2017;23:765‐777. Zhou WT, Ni YQ, Jin ZB, et al. Electrical stimulation ameliorates light‐induced photoreceptor degeneration in vitro via suppressing the proinflammatory effect of microglia and enhancing the neurotrophic potential of Müller cells. Exp Neurol. 2012;238(2):192‐208. Yang YP, Chang YL, Lai YH, et al. Retinal circular RNA hsa_circ_0087207 expression promotes apoptotic cell death in induced pluripotent stem cell‐derived Leber's hereditary optic neuropathy‐like models. Biomedicines. 2022;10(4):788. Su Y, Yi Y, Li L, Chen C. circRNA‐miRNA‐mRNA network in age‐related macular degeneration: from construction to identification. Exp Eye Res. 2021;203:108427. |
معلومات مُعتمدة: | 81570855 National Natrual Science Foundation of China; 81790641 National Natrual Science Foundation of China |
فهرسة مساهمة: | Keywords: apoptosis; circUvrag; circular RNA; light‐induced photoreceptor degeneration; retina |
المشرفين على المادة: | 0 (RNA, Circular) 63231-63-0 (RNA) |
تواريخ الأحداث: | Date Created: 20240129 Date Completed: 20240701 Latest Revision: 20240701 |
رمز التحديث: | 20240702 |
DOI: | 10.1111/ceo.14355 |
PMID: | 38282307 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1442-9071 |
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DOI: | 10.1111/ceo.14355 |