Inhibition of the cGAS-STING Pathway Attenuates Lung Ischemia/Reperfusion Injury via Regulating Endoplasmic Reticulum Stress in Alveolar Epithelial Type II Cells of Rats

References

• Iske J, Hinze CA, Salman J, Haverich A, Tullius SG, Ius F. The potential of ex vivo lung perfusion on improving organ quality and ameliorating ischemia reperfusion injury. Am J Transplant. 2021;21(12):3831–3839. doi:10.1111/ajt.16784
   PubMed Web of Science ®Google Scholar
• Lama VN. Update in lung transplantation 2008. Am J Respir Crit Care Med. 2009;179(9):759–764. doi:10.1164/rccm.200902-0177UP
   PubMed Web of Science ®Google Scholar
• Wang X, O’Brien ME, Yu J, et al. Prolonged cold ischemia induces necroptotic cell death in ischemia-reperfusion injury and contributes to primary graft dysfunction after lung transplantation. Am J Respir Cell Mol Biol. 2019;61(2):244–256. doi:10.1165/rcmb.2018-0207OC
   PubMed Web of Science ®Google Scholar
• Daud SA, Yusen RD, Meyers BF, et al. Impact of immediate primary lung allograft dysfunction on bronchiolitis obliterans syndrome. Am J Respir Crit Care Med. 2007;175(5):507–513. doi:10.1164/rccm.200608-1079OC
   PubMed Web of Science ®Google Scholar
• Jungraithmayr W. Novel strategies for endothelial preservation in lung transplant ischemia-reperfusion injury. Front Physiol. 2020;11:581420. doi:10.3389/fphys.2020.581420
   PubMed Web of Science ®Google Scholar
• Mrazkova H, Lischke R, Hodyc D, Herget J. The protective effect of hypercapnia on ischemia-reperfusion injury in lungs. Respir Physiol Neurobiol. 2015;205:42–46. doi:10.1016/j.resp.2014.10.002
   PubMed Web of Science ®Google Scholar
• Wu JX, Zhu HW, Chen X, et al. Inducible nitric oxide synthase inhibition reverses pulmonary arterial dysfunction in lung transplantation. Inflamm Res. 2014;63(8):609–618. doi:10.1007/s00011-014-0733-5
   PubMed Web of Science ®Google Scholar
• Zhang JP, Zhang WJ, Yang M, Fang H. Propofol attenuates lung ischemia/reperfusion injury though the involvement of the MALAT1/microRNA-144/GSK3β axis. Mol Med. 2021;27(1):77. doi:10.1186/s10020-021-00332-0
   PubMed Web of Science ®Google Scholar
• Ferrari RS, Andrade CF. Oxidative stress and lung ischemia-reperfusion injury. Oxid Med Cell Longev. 2015;2015:590987. doi:10.1155/2015/590987
   PubMed Web of Science ®Google Scholar
• Li J, Chen Q, He X, et al. Dexmedetomidine attenuates lung apoptosis induced by renal ischemia-reperfusion injury through α2AR/PI3K/Akt pathway. J Transl Med. 2018;16(1):78. doi:10.1186/s12967-018-1455-1
   PubMed Web of Science ®Google Scholar
• Weibel ER. On the tricks alveolar epithelial cells play to make a good lung. Am J Respir Crit Care Med. 2015;191(5):504–513. doi:10.1164/rccm.201409-1663OE
   PubMed Web of Science ®Google Scholar
• Jansing NL, McClendon J, Henson PM, et al. Unbiased quantitation of alveolar type II to alveolar type I cell transdifferentiation during repair after lung injury in mice. Am J Respir Cell Mol Biol. 2017;57(5):519–526. doi:10.1165/rcmb.2017-0037MA
   PubMed Web of Science ®Google Scholar
• Wu Y, Lv J, Feng D, et al. Restoration of alveolar type II cell function contributes to simvastatin-induced attenuation of lung ischemia-reperfusion injury. Int J Mol Med. 2012;30(6):1294–1306. doi:10.3892/ijmm.2012.1161
   PubMed Web of Science ®Google Scholar
• Guerriero CJ, Brodsky JL. The delicate balance between secreted protein folding and endoplasmic reticulum-associated degradation in human physiology. Physiol Rev. 2012;92(2):537–576. doi:10.1152/physrev.00027.2011
   PubMed Web of Science ®Google Scholar
• Men X, Han S, Gao J, et al. Taurine protects against lung damage following limb ischemia reperfusion in the rat by attenuating endoplasmic reticulum stress-induced apoptosis. Acta Orthop. 2010;81(2):263–267. doi:10.3109/17453671003587085
   PubMed Web of Science ®Google Scholar
• Korfei M, Ruppert C, Mahavadi P, et al. Epithelial endoplasmic reticulum stress and apoptosis in sporadic idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2008;178(8):838–846. doi:10.1164/rccm.200802-313OC
   PubMed Web of Science ®Google Scholar
• Sun X, Liu H, Sun Z, et al. Acupuncture protects against cerebral ischemia-reperfusion injury via suppressing endoplasmic reticulum stress-mediated autophagy and apoptosis. Mol Med. 2020;26(1):105. doi:10.1186/s10020-020-00236-5
   PubMed Web of Science ®Google Scholar
• Zindel J, Kubes P. DAMPs, PAMPs, and LAMPs in immunity and sterile inflammation. Annu Rev Pathol. 2020;15:493–518. doi:10.1146/annurev-pathmechdis-012419-032847
   PubMed Web of Science ®Google Scholar
• Hopfner KP, Hornung V. Molecular mechanisms and cellular functions of cGAS-STING signalling. Nat Rev Mol Cell Biol. 2020;21(9):501–521. doi:10.1038/s41580-020-0244-x
   PubMed Web of Science ®Google Scholar
• Sun L, Wu J, Du F, Chen X, Chen ZJ. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science. 2013;339(6121):786–791. doi:10.1126/science.1232458
   PubMed Web of Science ®Google Scholar
• Cui Y, Zhao D, Sreevatsan S, et al. Mycobacterium bovis induces endoplasmic reticulum stress mediated-apoptosis by activating IRF3 in a murine macrophage cell line. Front Cell Infect Microbiol. 2016;6:182.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Chen W, Wang Y. STING is an essential regulator of heart inflammation and fibrosis in mice with pathological cardiac hypertrophy via endoplasmic reticulum (ER) stress. Biomed Pharmacother. 2020;125:110022. doi:10.1016/j.biopha.2020.110022
   PubMed Web of Science ®Google Scholar
• Ueda S, Chen-Yoshikawa TF, Tanaka S, et al. Protective effect of necrosulfonamide on rat pulmonary ischemia-reperfusion injury via inhibition of necroptosis. J Thorac Cardiovasc Surg. 2022;163(2):e113–e122. doi:10.1016/j.jtcvs.2021.01.037
   PubMed Web of Science ®Google Scholar
• Vincent J, Adura C, Gao P, et al. Small molecule inhibition of cGAS reduces interferon expression in primary macrophages from autoimmune mice. Nat Commun. 2017;8(1):750. doi:10.1038/s41467-017-00833-9
   PubMed Web of Science ®Google Scholar
• Xu Q, Xiong H, Zhu W, Liu Y, Du Y. Small molecule inhibition of cyclic GMP-AMP synthase ameliorates sepsis-induced cardiac dysfunction in mice. Life Sci. 2020;260:118315. doi:10.1016/j.lfs.2020.118315
   PubMed Web of Science ®Google Scholar
• Chin EN, Yu C, Vartabedian VF, et al. Antitumor activity of a systemic STING-activating non-nucleotide cGAMP mimetic. Science. 2020;369(6506):993–999. doi:10.1126/science.abb4255
   PubMed Web of Science ®Google Scholar
• Chen X, Wang Y, Xie X, et al. Heme oxygenase-1 reduces sepsis-induced endoplasmic reticulum stress and acute lung injury. Mediators Inflamm. 2018;2018:9413876.
   PubMed Web of Science ®Google Scholar
• Lan CC, Peng CK, Tang SE, et al. Inhibition of Na-K-Cl cotransporter isoform 1 reduces lung injury induced by ischemia-reperfusion. J Thorac Cardiovasc Surg. 2017;153(1):206–215. doi:10.1016/j.jtcvs.2016.09.068
   PubMed Web of Science ®Google Scholar
• Kopp MC, Larburu N, Durairaj V, Adams CJ, Ali MMU. UPR proteins IRE1 and PERK switch BiP from chaperone to ER stress sensor. Nat Struct Mol Biol. 2019;26(11):1053–1062. doi:10.1038/s41594-019-0324-9
   PubMed Web of Science ®Google Scholar
• Sun H, Zhao X, Tai Q, Xu G, Ju Y, Gao W. Endothelial colony-forming cells reduced the lung injury induced by cardiopulmonary bypass in rats. Stem Cell Res Ther. 2020;11(1):246. doi:10.1186/s13287-020-01722-7
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang X, Rabbani ZN, Jackson IL, Vujaskovic Z. Oxidative stress mediates radiation lung injury by inducing apoptosis. Int J Radiat Oncol Biol Phys. 2012;83(2):740–748. doi:10.1016/j.ijrobp.2011.08.005
   PubMed Web of Science ®Google Scholar
• Wang J, Huang J, Wang L, et al. Urban particulate matter triggers lung inflammation via the ROS-MAPK-NF-κB signaling pathway. J Thorac Dis. 2017;9(11):4398–4412. doi:10.21037/jtd.2017.09.135
   PubMed Web of Science ®Google Scholar
• Chu SJ, Tang SE, Pao HP, Wu SY, Liao WI. Protease-activated receptor-1 antagonist protects against lung ischemia/reperfusion injury. Front Pharmacol. 2021;30(12):752507. doi:10.3389/fphar.2021.752507
   Web of Science ®Google Scholar
• Oakes SA, Papa FR. The role of endoplasmic reticulum stress in human pathology. Annu Rev Pathol. 2015;10:173–194. doi:10.1146/annurev-pathol-012513-104649
   PubMed Web of Science ®Google Scholar
• Yang C, Yang W, He Z, et al. Kaempferol alleviates oxidative stress and apoptosis through mitochondria-dependent pathway during lung ischemia-reperfusion injury. Front Pharmacol. 2021;12:624402. doi:10.3389/fphar.2021.624402
   PubMed Web of Science ®Google Scholar
• Huang CY, Deng JS, Huang WC, Jiang WP, Huang GJ. Attenuation of lipopolysaccharide-induced acute lung injury by hispolon in mice, through regulating the TLR4/PI3K/Akt/mTOR and Keap1/Nrf2/HO-1 pathways, and suppressing oxidative stress-mediated er stress-induced apoptosis and autophagy. Nutrients. 2020;12(6):1742. doi:10.3390/nu12061742
   PubMed Web of Science ®Google Scholar
• de Perrot M, Liu M, Waddell TK, Keshavjee S. Ischemia-reperfusion-induced lung injury. Am J Respir Crit Care Med. 2003;167(4):490–511. doi:10.1164/rccm.200207-670SO
   PubMed Web of Science ®Google Scholar
• Talaie T, DiChiacchio L, Prasad NK, et al. Ischemia-reperfusion injury in the transplanted lung: a literature review. Transplant Direct. 2021;7(2):e652. doi:10.1097/TXD.0000000000001104
   PubMed Web of Science ®Google Scholar
• Zhang X, Bai XC, Chen ZJ. Structures and mechanisms in the cGAS-STING innate immunity pathway. Immunity. 2020;53(1):43–53. doi:10.1016/j.immuni.2020.05.013
   PubMed Web of Science ®Google Scholar
• Aarreberg LD, Esser-Nobis K, Driscoll C, Shuvarikov A, Roby JA, Jr GM. Interleukin-1β induces mtDNA release to activate innate immune signaling via cGAS-STING. Mol Cell. 2019;74(4):801–815.e6. doi:10.1016/j.molcel.2019.02.038
   PubMed Web of Science ®Google Scholar
• Maekawa H, Inoue T, Ouchi H, et al. Mitochondrial damage causes inflammation via cGAS-STING signaling in acute kidney injury. Cell Rep. 2019;29(5):1261–1273.e6. doi:10.1016/j.celrep.2019.09.050
   PubMed Web of Science ®Google Scholar
• Li C, Liu W, Wang F, et al. DNA damage-triggered activation of cGAS-STING pathway induces apoptosis in human keratinocyte HaCaT cells. Mol Immunol. 2021;131:180–190. doi:10.1016/j.molimm.2020.12.037
   PubMed Web of Science ®Google Scholar
• Zhao M, Wang Y, Li L, et al. Mitochondrial ROS promote mitochondrial dysfunction and inflammation in ischemic acute kidney injury by disrupting TFAM-mediated mtDNA maintenance. Theranostics. 2021;11(4):1845–1863. doi:10.7150/thno.50905
   PubMed Web of Science ®Google Scholar
• Chattopadhyay S, Marques JT, Yamashita M, et al. Viral apoptosis is induced by IRF-3-mediated activation of Bax. EMBO J. 2010;29(10):1762–1773. doi:10.1038/emboj.2010.50
   PubMed Web of Science ®Google Scholar
• Zhu Q, Man SM, Karki R, Malireddi RKS, Kanneganti TD. Detrimental type I interferon signaling dominates protective AIM2 inflammasome responses during Francisella novicida infection. Cell Rep. 2018;22(12):3168–3174. doi:10.1016/j.celrep.2018.02.096
   PubMed Web of Science ®Google Scholar
• Lei Z, Deng M, Yi Z, et al. cGAS-mediated autophagy protects the liver from ischemia-reperfusion injury independently of STING. Am J Physiol Gastrointest Liver Physiol. 2018;314(6):G655–G667. doi:10.1152/ajpgi.00326.2017
   PubMed Web of Science ®Google Scholar
• Liao Y, Cheng J, Kong X, et al. HDAC3 inhibition ameliorates ischemia/reperfusion-induced brain injury by regulating the microglial cGAS-STING pathway. Theranostics. 2020;10(21):9644–9662. doi:10.7150/thno.47651
   PubMed Web of Science ®Google Scholar
• Gamdzyk M, Doycheva DM, Araujo C, et al. cGAS/STING pathway activation contributes to delayed neurodegeneration in neonatal hypoxia-ischemia rat model: possible involvement of LINE-1. Mol Neurobiol. 2020;57(6):2600–2619. doi:10.1007/s12035-020-01904-7
   PubMed Web of Science ®Google Scholar
• Feng D, Wang B, Wang L, et al. Pre-ischemia melatonin treatment alleviated acute neuronal injury after ischemic stroke by inhibiting endoplasmic reticulum stress-dependent autophagy via PERK and IRE1 signalings. J Pineal Res. 2017;62:3. doi:10.1111/jpi.12395
   Web of Science ®Google Scholar
• Liu H, Wang L, Weng X, et al. Inhibition of Brd4 alleviates renal ischemia/reperfusion injury-induced apoptosis and endoplasmic reticulum stress by blocking FoxO4-mediated oxidative stress. Redox Biol. 2019;24:101195. doi:10.1016/j.redox.2019.101195
   PubMed Web of Science ®Google Scholar
• Yang YF, Wang H, Song N, et al. Dexmedetomidine attenuates ischemia/reperfusion-induced myocardial inflammation and apoptosis through inhibiting endoplasmic reticulum stress signaling. J Inflamm Res. 2021;31(14):1217–1233.
   Google Scholar
• Petrasek J, Iracheta-Vellve A, Csak T, et al. STING-IRF3 pathway links endoplasmic reticulum stress with hepatocyte apoptosis in early alcoholic liver disease. Proc Natl Acad Sci USA. 2013;110(41):16544–16549. doi:10.1073/pnas.1308331110
   PubMed Web of Science ®Google Scholar
• Moretti J, Roy S, Bozec D, et al. STING senses microbial viability to orchestrate stress-mediated autophagy of the endoplasmic reticulum. Cell. 2017;171(4):809–823.e13. doi:10.1016/j.cell.2017.09.034
   PubMed Web of Science ®Google Scholar
• Lin Y, Jiang M, Chen W, Zhao T, Wei Y. Cancer and ER stress: mutual crosstalk between autophagy, oxidative stress and inflammatory response. Biomed Pharmacother. 2019;118:109249. doi:10.1016/j.biopha.2019.109249
   PubMed Web of Science ®Google Scholar
• Namgaladze D, Khodzhaeva V, Brüne B. ER-mitochondria communication in cells of the innate immune system. Cells. 2019;8(9):1088. doi:10.3390/cells8091088
   PubMed Web of Science ®Google Scholar
• Sprenkle NT, Sims SG, Sánchez CL, Meares GP. Endoplasmic reticulum stress and inflammation in the central nervous system. Mol Neurodegener. 2017;12(1):42. doi:10.1186/s13024-017-0183-y
   PubMed Web of Science ®Google Scholar
• Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13(2):89–102. doi:10.1038/nrm3270
   PubMed Web of Science ®Google Scholar
• Ablasser A, Schmid-Burgk JL, Hemmerling I, et al. Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP. Nature. 2013;503(7477):530–534. doi:10.1038/nature12640
   PubMed Web of Science ®Google Scholar
• Gentili M, Kowal J, Tkach M, et al. Transmission of innate immune signaling by packaging of cGAMP in viral particles. Science. 2015;349(6253):1232–1236. doi:10.1126/science.aab3628
   PubMed Web of Science ®Google Scholar
• Luteijn RD, Zaver SA, Gowen BG, et al. SLC19A1 transports immunoreactive cyclic dinucleotides. Nature. 2019;573(7774):434–438. doi:10.1038/s41586-019-1553-0
   PubMed Web of Science ®Google Scholar