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Review Article

Cyclophilin D-mediated Mitochondrial Permeability Transition Regulates Mitochondrial Function

Author(s): Shaoyun Zhou, Qinwei Yu, Luyong Zhang and Zhenzhou Jiang*

Volume 29, Issue 8, 2023

Published on: 22 March, 2023

Page: [620 - 629] Pages: 10

DOI: 10.2174/1381612829666230313111314

Price: $65

Abstract

Background: Mitochondria are multifunctional organelles, which participate in biochemical processes. Mitochondria act as primary energy producers and biosynthetic centers of cells, which are involved in oxidative stress responses and cell signaling transduction. Among numerous potential mechanisms of mitochondrial dysfunction, the opening of the mitochondrial permeability transition pore (mPTP) is a major determinant of mitochondrial dysfunction to induce cellular damage or death. A plenty of studies have provided evidence that the abnormal opening of mPTP induces the loss of mitochondrial membrane potential, the impairment calcium homeostasis and the decrease of ATP production. Cyclophilin D (CypD), localized in the mitochondrial transition pore, is a mitochondrial chaperone that has been regarded as a prominent mediator of mPTP.

Methods: This review describes the relationship between CypD, mPTP, and CypD-mPTP inhibitors through systematic investigation of recent relevant literature.

Results: Here, we have highlighted that inhibiting the activity of CypD protects models of some diseases, including ischaemia/reperfusion injury (IRI), neurodegenerative disorders and so on. Knockdown studies have demonstrated that CypD possibly is mediated by its peptidyl-prolyl cis-trans isomerase activity, while the primary targets of CypD remain obscure. The target of CypD-mPTP inhibitor can alleviate mPTP opening-induced cell death. The present review is focused on the role of CypD as a prominent mediator of the mPTP, further providing insight into the physiological function of mPTP and its regulation by CypD.

Conclusion: Blocking the opening of mPTP by inhibiting CypD might be a new promising approach for suppressing cell death, which will suggest novel therapeutic approaches for mitochondria-related diseases.

Keywords: Mitochondria, mitochondrial permeability transition pore, cyclophilin D, mechanisms, reactive oxygen species, cell death.

« Previous Next »
[1]
Liew SS, Qin X, Zhou J, Li L, Huang W, Yao SQ. Smart design of nanomaterials for mitochondria-targeted nanotherapeutics. Angew Chem Int Ed 2021; 60(5): 2232-56.
[http://dx.doi.org/10.1002/anie.201915826] [PMID: 32128948]
[2]
Nowinski SM, Van Vranken JG, Dove KK, Rutter J. Impact of mitochondrial fatty acid synthesis on mitochondrial biogenesis. Curr Biol 2018; 28(20): R1212-9.
[http://dx.doi.org/10.1016/j.cub.2018.08.022] [PMID: 30352195]
[3]
Westensee IN, Brodszkij E, Qian X, Marcelino TF, Lefkimmiatis K, Städler B. Mitochondria encapsulation in hydrogel-based artificial cells as ATP producing subunits. Small 2021; 17(24): 2007959.
[http://dx.doi.org/10.1002/smll.202007959] [PMID: 33969618]
[4]
Bauer TM, Murphy E. Role of mitochondrial calcium and the permeability transition pore in regulating cell death. Circ Res 2020; 126(2): 280-93.
[http://dx.doi.org/10.1161/CIRCRESAHA.119.316306] [PMID: 31944918]
[5]
Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev 2014; 94(3): 909-50.
[http://dx.doi.org/10.1152/physrev.00026.2013] [PMID: 24987008]
[6]
Bukrinsky MI. Cyclophilins: unexpected messengers in intercellular communications. Trends Immunol 2002; 23(7): 323-5.
[http://dx.doi.org/10.1016/S1471-4906(02)02237-8] [PMID: 12103338]
[7]
Handschumacher RE, Harding MW, Rice J, Drugge RJ, Speicher DW. Cyclophilin: A specific cytosolic binding protein for cyclosporin A. Science 1984; 226(4674): 544-7.
[http://dx.doi.org/10.1126/science.6238408] [PMID: 6238408]
[8]
Wang P, Heitman J. The cyclophilins. Genome Biol 2005; 6(7): 226.
[http://dx.doi.org/10.1186/gb-2005-6-7-226] [PMID: 15998457]
[9]
Liang L, Lin R, Xie Y, et al. The role of cyclophilins in inflammatory bowel disease and colorectal cancer. Int J Biol Sci 2021; 17(10): 2548-60.
[http://dx.doi.org/10.7150/ijbs.58671] [PMID: 34326693]
[10]
Alam MR, Baetz D, Ovize M. Cyclophilin D and myocardial ischemia–reperfusion injury: A fresh perspective. J Mol Cell Cardiol 2015; 78: 80-9.
[http://dx.doi.org/10.1016/j.yjmcc.2014.09.026] [PMID: 25281838]
[11]
Amanakis G, Murphy E. Cyclophilin D: An integrator of mitochondrial function. Front Physiol 2020; 11: 595.
[http://dx.doi.org/10.3389/fphys.2020.00595] [PMID: 32625108]
[12]
Zhang Y, Lu P, Liang F, et al. Cyclophilin D contributes to anesthesia neurotoxicity in the developing brain. Front Cell Dev Biol 2020; 7: 396.
[http://dx.doi.org/10.3389/fcell.2019.00396] [PMID: 32117955]
[13]
Jia K, Du H. Mitochondrial permeability transition: A pore intertwines brain aging and Alzheimer’s disease. Cells 2021; 10(3): 649.
[http://dx.doi.org/10.3390/cells10030649] [PMID: 33804048]
[14]
Karch J, Bround MJ, Khalil H, et al. Inhibition of mitochondrial permeability transition by deletion of the ANT family and CypD. Sci Adv 2019; 5(8): eaaw4597.
[http://dx.doi.org/10.1126/sciadv.aaw4597] [PMID: 31489369]
[15]
Baines CP, Kaiser RA, Purcell NH, et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005; 434(7033): 658-62.
[http://dx.doi.org/10.1038/nature03434] [PMID: 15800627]
[16]
Gomez L, Li B, Mewton N, et al. Inhibition of mitochondrial permeability transition pore opening: Translation to patients. Cardiovasc Res 2009; 83(2): 226-33.
[http://dx.doi.org/10.1093/cvr/cvp063] [PMID: 19221132]
[17]
Gordan R, Fefelova N, Gwathmey JK, Xie LH. Involvement of mitochondrial permeability transition pore (mPTP) in cardiac arrhythmias: Evidence from cyclophilin D knockout mice. Cell Calcium 2016; 60(6): 363-72.
[http://dx.doi.org/10.1016/j.ceca.2016.09.001] [PMID: 27616659]
[18]
Nguyen TTM, Wong R, Menazza S, et al. Cyclophilin D modulates mitochondrial acetylome. Circ Res 2013; 113(12): 1308-19.
[http://dx.doi.org/10.1161/CIRCRESAHA.113.301867] [PMID: 24062335]
[19]
Schnichels S, Schultheiss M, Klemm P, et al. Cyclosporine a protects retinal explants against hypoxia. Int J Mol Sci 2021; 22(19): 10196.
[http://dx.doi.org/10.3390/ijms221910196] [PMID: 34638537]
[20]
Halestrap A, Clarke SJ, Javadov SA. Mitochondrial permeability transition pore opening during myocardial reperfusion—a target for cardioprotection. Cardiovasc Res 2004; 61(3): 372-85.
[http://dx.doi.org/10.1016/S0008-6363(03)00533-9] [PMID: 14962470]
[21]
Hou D, Hu F, Mao Y, et al. Cationic antimicrobial peptide NRC-03 induces oral squamous cell carcinoma cell apoptosis via CypD-mPTP axis-mediated mitochondrial oxidative stress. Redox Biol 2022; 54: 102355.
[http://dx.doi.org/10.1016/j.redox.2022.102355] [PMID: 35660629]
[22]
Xian H, Watari K, Sanchez-Lopez E, et al. Oxidized DNA fragments exit mitochondria via mPTP- and VDAC-dependent channels to activate NLRP3 inflammasome and interferon signaling. Immunity 2022; 55(8): 1370-1385.E8.
[http://dx.doi.org/10.1016/j.immuni.2022.06.007] [PMID: 35835107]
[23]
Yu CH, Davidson S, Harapas CR, et al. TDP-43 triggers mitochondrial DNA release via mPTP to activate cGAS/STING in ALS. Cell 2020; 183(3): 636-649.E18.
[http://dx.doi.org/10.1016/j.cell.2020.09.020] [PMID: 33031745]
[24]
Zhang W, Li G, Luo R, et al. Cytosolic escape of mitochondrial DNA triggers cGAS-STING-NLRP3 axis-dependent nucleus pulposus cell pyroptosis. Exp Mol Med 2022; 54(2): 129-42.
[http://dx.doi.org/10.1038/s12276-022-00729-9] [PMID: 35145201]
[25]
Rodríguez-Nuevo A, Díaz-Ramos A, Noguera E, et al. Mitochondrial DNA and TLR9 drive muscle inflammation upon Opa1 deficiency. EMBO J 2018; 37(10): e96553.
[http://dx.doi.org/10.15252/embj.201796553] [PMID: 29632021]
[26]
Gan X, Zhang L, Liu B, et al. CypD-mPTP axis regulates mitochondrial functions contributing to osteogenic dysfunction of MC3T3-E1 cells in inflammation. J Physiol Biochem 2018; 74(3): 395-402.
[http://dx.doi.org/10.1007/s13105-018-0627-z] [PMID: 29679227]
[27]
Kwong JQ, Molkentin JD. Physiological and pathological roles of the mitochondrial permeability transition pore in the heart. Cell Metab 2015; 21(2): 206-14.
[http://dx.doi.org/10.1016/j.cmet.2014.12.001] [PMID: 25651175]
[28]
Angelova PR, Abramov AY. Role of mitochondrial ROS in the brain: From physiology to neurodegeneration. FEBS Lett 2018; 592(5): 692-702.
[http://dx.doi.org/10.1002/1873-3468.12964] [PMID: 29292494]
[29]
Sui S, Tian J, Gauba E, Wang Q, Guo L, Du H. Cyclophilin D regulates neuronal activity-induced filopodiagenesis by fine-tuning dendritic mitochondrial calcium dynamics. J Neurochem 2018; 146(4): 403-15.
[http://dx.doi.org/10.1111/jnc.14484] [PMID: 29900530]
[30]
Yan B, Liu Q, Ding X, et al. SIRT3-mediated CypD-K166 deacetylation alleviates neuropathic pain by improving mitochondrial dysfunction and inhibiting oxidative stress. Oxid Med Cell Longev 2022; 2022: 1-17.
[http://dx.doi.org/10.1155/2022/4722647] [PMID: 36092157]
[31]
Klawitter J, Klawitter J, Pennington A, et al. Cyclophilin D knockout protects the mouse kidney against cyclosporin A-induced oxidative stress. Am J Physiol Renal Physiol 2019; 317(3): F683-94.
[http://dx.doi.org/10.1152/ajprenal.00417.2018] [PMID: 31188033]
[32]
Ye F, Li X, Liu Y, et al. CypD deficiency confers neuroprotection against mitochondrial abnormality caused by lead in SH-SY5Y cell. Toxicol Lett 2020; 323: 25-34.
[http://dx.doi.org/10.1016/j.toxlet.2019.12.025] [PMID: 31874198]
[33]
Panel M, Ruiz I, Brillet R, et al. Small-molecule inhibitors of cyclophilins block opening of the mitochondrial permeability transition pore and protect mice from hepatic ischemia/reperfusion injury. Gastroenterology 2019; 157(5): 1368-82.
[http://dx.doi.org/10.1053/j.gastro.2019.07.026] [PMID: 31336123]
[34]
Ten VS, Stepanova AA, Ratner V, et al. Mitochondrial dysfunction and permeability transition in neonatal brain and lung injuries. Cells 2021; 10(3): pp 569.
[http://dx.doi.org/10.3390/cells10030569] [PMID: 33807810]
[35]
Denorme F, Manne BK, Portier I, et al. Platelet necrosis mediates ischemic stroke outcome in mice. Blood 2020; 135(6): 429-40.
[http://dx.doi.org/10.1182/blood.2019002124] [PMID: 31800959]
[36]
Yang H, Li R, Zhang L, et al. p53-cyclophilin D mediates renal tubular cell apoptosis in ischemia-reperfusion-induced acute kidney injury. Am J Physiol Renal Physiol 2019; 317(5): F1311-7.
[http://dx.doi.org/10.1152/ajprenal.00072.2019] [PMID: 31339772]
[37]
Lebedev I, Nemajerova A, Foda ZH, et al. A novel in vitro CypD-Mediated p53 aggregation assay suggests a model for mitochondrial permeability transition by chaperone systems. J Mol Biol 2016; 428(20): 4154-67.
[http://dx.doi.org/10.1016/j.jmb.2016.08.001] [PMID: 27515399]
[38]
Xavier JM, Morgado AL, Solá S, Rodrigues CMP. Mitochondrial translocation of p53 modulates neuronal fate by preventing differentiation-induced mitochondrial stress. Antioxid Redox Signal 2014; 21(7): 1009-24.
[http://dx.doi.org/10.1089/ars.2013.5417] [PMID: 24329038]
[39]
Wolff S, Erster S, Palacios G, Moll UM. p53's mitochondrial translocation and MOMP action is independent of Puma and Bax and severely disrupts mitochondrial membrane integrity. Cell Res 2008; 18(7): 733-44.
[http://dx.doi.org/10.1038/cr.2008.62] [PMID: 18504456]
[40]
Vaseva AV, Marchenko ND, Ji K, Tsirka SE, Holzmann S, Moll UM. p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 2012; 149(7): 1536-48.
[http://dx.doi.org/10.1016/j.cell.2012.05.014] [PMID: 22726440]
[41]
Quinsay MN, Lee Y, Rikka S, et al. Bnip3 mediates permeabilization of mitochondria and release of cytochrome c via a novel mechanism. J Mol Cell Cardiol 2010; 48(6): 1146-56.
[http://dx.doi.org/10.1016/j.yjmcc.2009.12.004] [PMID: 20025887]
[42]
Dhingra R, Guberman M, Rabinovich-Nikitin I, et al. Impaired NF-κB signalling underlies cyclophilin D-mediated mitochondrial permeability transition pore opening in doxorubicin cardiomyopathy. Cardiovasc Res 2020; 116(6): 1161-74.
[http://dx.doi.org/10.1093/cvr/cvz240] [PMID: 31566215]
[43]
Fakharnia F, Khodagholi F, Dargahi L, Ahmadiani A. Prevention of cyclophilin D-mediated mPTP opening using cyclosporine-a alleviates the elevation of necroptosis, autophagy and apoptosis-related markers following global cerebral ischemia-reperfusion. J Mol Neurosci 2017; 61(1): 52-60.
[http://dx.doi.org/10.1007/s12031-016-0843-3] [PMID: 27664163]
[44]
Eliseev RA, Malecki J, Lester T, Zhang Y, Humphrey J, Gunter TE. Cyclophilin D interacts with Bcl2 and exerts an anti-apoptotic effect. J Biol Chem 2009; 284(15): 9692-9.
[http://dx.doi.org/10.1074/jbc.M808750200] [PMID: 19228691]
[45]
Varanyuwatana P, Halestrap AP. The roles of phosphate and the phosphate carrier in the mitochondrial permeability transition pore. Mitochondrion 2012; 12(1): 120-5.
[http://dx.doi.org/10.1016/j.mito.2011.04.006] [PMID: 21586347]
[46]
Rasola A, Sciacovelli M, Pantic B, Bernardi P. Signal transduction to the permeability transition pore. FEBS Lett 2010; 584(10): 1989-96.
[http://dx.doi.org/10.1016/j.febslet.2010.02.022] [PMID: 20153328]
[47]
Duarte FV, Gomes AP, Teodoro JS, et al. Dibenzofuran-induced mitochondrial dysfunction: Interaction with ANT carrier. Toxicol In Vitro 2013; 27(8): 2160-8.
[http://dx.doi.org/10.1016/j.tiv.2013.08.009] [PMID: 24008156]
[48]
Zhao X, Khan N, Gan H, et al. Bcl-xL mediates RIPK3-dependent necrosis in M. tuberculosis-infected macrophages. Mucosal Immunol 2017; 10(6): 1553-68.
[http://dx.doi.org/10.1038/mi.2017.12] [PMID: 28401933]
[49]
Leung AWC, Varanyuwatana P, Halestrap AP. The mitochondrial phosphate carrier interacts with cyclophilin D and may play a key role in the permeability transition. J Biol Chem 2008; 283(39): 26312-23.
[http://dx.doi.org/10.1074/jbc.M805235200] [PMID: 18667415]
[50]
Kwong JQ, Davis J, Baines CP, et al. Genetic deletion of the mitochondrial phosphate carrier desensitizes the mitochondrial permeability transition pore and causes cardiomyopathy. Cell Death Differ 2014; 21(8): 1209-17.
[http://dx.doi.org/10.1038/cdd.2014.36] [PMID: 24658400]
[51]
Guo J, Liu Z, Zhang D, et al. circEZH2 inhibits opening of mitochondrial permeability transition pore via interacting with PiC and up-regulating RSAD2. Vet Microbiol 2022; 272: 109497.
[http://dx.doi.org/10.1016/j.vetmic.2022.109497] [PMID: 35785658]
[52]
Teodoro JS, Varela AT, Duarte FV, Gomes AP, Palmeira CM, Rolo AP. Indirubin and NAD+ prevent mitochondrial ischaemia/reperfusion damage in fatty livers. Eur J Clin Invest 2018; 48(6): e12932.
[http://dx.doi.org/10.1111/eci.12932] [PMID: 29603199]
[53]
Carling D. AMPK signalling in health and disease. Curr Opin Cell Biol 2017; 45: 31-7.
[http://dx.doi.org/10.1016/j.ceb.2017.01.005] [PMID: 28232179]
[54]
Klawitter J, Pennington A, Klawitter J, Thurman JM, Christians U. Mitochondrial cyclophilin D ablation is associated with the activation of Akt/p70S6K pathway in the mouse kidney. Sci Rep 2017; 7(1): 10540.
[http://dx.doi.org/10.1038/s41598-017-10076-9] [PMID: 28874678]
[55]
Barreto-Torres G, Javadov S. Possible role of interaction between PPAR α and cyclophilin D in cardioprotection of AMPK against in vivo ischemia-reperfusion in rats. PPAR Res 2016; 2016: 1-12.
[http://dx.doi.org/10.1155/2016/9282087] [PMID: 27051413]
[56]
Barreto-Torres G, Hernandez JS, Jang S, et al. The beneficial effects of AMP kinase activation against oxidative stress are associated with prevention of PPARα-cyclophilin D interaction in cardiomyocytes. Am J Physiol Heart Circ Physiol 2015; 308(7): H749-58.
[http://dx.doi.org/10.1152/ajpheart.00414.2014] [PMID: 25617357]
[57]
Ren G, Ma Y, Wang X, Zheng Z, Li G. Aspirin blocks AMPK/SIRT3-mediated glycolysis to inhibit NSCLC cell proliferation. Eur J Pharmacol 2022; 932: 175208.
[http://dx.doi.org/10.1016/j.ejphar.2022.175208] [PMID: 35981603]
[58]
Radhakrishnan J, Baetiong A, Gazmuri RJ. Enhanced oxygen utilization efficiency with concomitant activation of AMPK-TBC1D1 signaling nexus in cyclophilin-d conditional knockout mice. Front Physiol 2021; 12: 756659.
[http://dx.doi.org/10.3389/fphys.2021.756659] [PMID: 34955879]
[59]
Glozak MA, Sengupta N, Zhang X, Seto E. Acetylation and deacetylation of non-histone proteins. Gene 2005; 363: 15-23.
[http://dx.doi.org/10.1016/j.gene.2005.09.010] [PMID: 16289629]
[60]
Chamberlain KA, Huang N, Xie Y, et al. Oligodendrocytes enhance axonal energy metabolism by deacetylation of mitochondrial proteins through transcellular delivery of SIRT2. Neuron 2021; 109(21): 3456-3472.E8.
[http://dx.doi.org/10.1016/j.neuron.2021.08.011] [PMID: 34506725]
[61]
Cheng A, Yang Y, Zhou Y, et al. Mitochondrial SIRT3 mediates adaptive responses of neurons to exercise and metabolic and excitatory challenges. Cell Metab 2016; 23(1): 128-42.
[http://dx.doi.org/10.1016/j.cmet.2015.10.013] [PMID: 26698917]
[62]
Sun F, Si Y, Bao H, et al. Regulation of sirtuin 3-mediated deacetylation of cyclophilin D attenuated cognitive dysfunction induced by sepsis-associated encephalopathy in mice. Cell Mol Neurobiol 2017; 37(8): 1457-64.
[http://dx.doi.org/10.1007/s10571-017-0476-2] [PMID: 28236057]
[63]
Wang N, Xu HH, Zhou W, et al. Aconitine attenuates mitochondrial dysfunction of cardiomyocytes via promoting deacetylation of cyclophilin-D mediated by sirtuin-3. J Ethnopharmacol 2021; 270: 113765.
[http://dx.doi.org/10.1016/j.jep.2020.113765] [PMID: 33418031]
[64]
Hirschey MD, Shimazu T, Goetzman E, et al. SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 2010; 464(7285): 121-5.
[http://dx.doi.org/10.1038/nature08778] [PMID: 20203611]
[65]
Hirschey MD, Shimazu T, Jing E, et al. SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol Cell 2011; 44(2): 177-90.
[http://dx.doi.org/10.1016/j.molcel.2011.07.019] [PMID: 21856199]
[66]
Katwal G, Baral D, Fan X, et al. SIRT3 a major player in attenuation of hepatic ischemia-reperfusion injury by reducing ROS via Its downstream mediators: SOD2, CYP-D, and HIF-1 α. Oxid Med Cell Longev 2018; 2018: 1-13.
[http://dx.doi.org/10.1155/2018/2976957] [PMID: 30538800]
[67]
Beutner G, Alanzalon RE, Porter GA Jr. Cyclophilin D regulates the dynamic assembly of mitochondrial ATP synthase into synthasomes. Sci Rep 2017; 7(1): 14488.
[http://dx.doi.org/10.1038/s41598-017-14795-x] [PMID: 29101324]
[68]
Chernyak BV. Redox regulation of the mitochondrial permeability transition pore. Biosci Rep 1997; 17(3): 293-302.
[http://dx.doi.org/10.1023/A:1027384628678] [PMID: 9337484]
[69]
Wang X, Zhou W, Gao Z, Lv X. Mass spectrometry analysis of S-nitrosylation of proteins and its role in cancer, cardiovascular and neurodegenerative diseases. Trends Analyt Chem 2022; 152: 116625.
[http://dx.doi.org/10.1016/j.trac.2022.116625]
[70]
Amanakis G, Sun J, Fergusson MM, et al. Cysteine 202 of cyclophilin D is a site of multiple post-translational modifications and plays a role in cardioprotection. Cardiovasc Res 2021; 117(1): 212-23.
[http://dx.doi.org/10.1093/cvr/cvaa053] [PMID: 32129829]
[71]
Nguyen TT, Stevens MV, Kohr M, Steenbergen C, Sack MN, Murphy E. Cysteine 203 of cyclophilin D is critical for cyclophilin D activation of the mitochondrial permeability transition pore. J Biol Chem 2011; 286(46): 40184-92.
[http://dx.doi.org/10.1074/jbc.M111.243469] [PMID: 21930693]
[72]
Kohr MJ, Sun J, Aponte A, et al. Simultaneous measurement of protein oxidation and S-nitrosylation during preconditioning and ischemia/reperfusion injury with resin-assisted capture. Circ Res 2011; 108(4): 418-26.
[http://dx.doi.org/10.1161/CIRCRESAHA.110.232173] [PMID: 21193739]
[73]
Linard D, Kandlbinder A, Degand H, Morsomme P, Dietz KJ, Knoops B. Redox characterization of human cyclophilin D: Identification of a new mammalian mitochondrial redox sensor. Arch Biochem Biophys 2009; 491(1-2): 39-45.
[http://dx.doi.org/10.1016/j.abb.2009.09.002] [PMID: 19735641]
[74]
Zhou H, Zhang Y, Hu S, et al. Melatonin protects cardiac microvasculature against ischemia/reperfusion injury via suppression of mitochondrial fission-VDAC1-HK2-mPTP-mitophagy axis. J Pineal Res 2017; 63(1): e12413.
[http://dx.doi.org/10.1111/jpi.12413] [PMID: 28398674]
[75]
Zhu P, Wan K, Yin M, et al. RIPK3 induces cardiomyocyte necroptosis via inhibition of AMPK-parkin-mitophagy in cardiac remodelling after myocardial infarction. Oxid Med Cell Longev 2021; 2021: 1-11.
[http://dx.doi.org/10.1155/2021/6635955] [PMID: 33854696]
[76]
Sun T, Ding W, Xu T, et al. Parkin regulates programmed necrosis and myocardial ischemia/reperfusion injury by targeting cyclophilin-D. Antioxid Redox Signal 2019; 31(16): 1177-93.
[http://dx.doi.org/10.1089/ars.2019.7734] [PMID: 31456416]
[77]
Hurst S, Gonnot F, Dia M, Crola Da Silva C, Gomez L, Sheu SS. Phosphorylation of cyclophilin D at serine 191 regulates mitochondrial permeability transition pore opening and cell death after ischemia-reperfusion. Cell Death Dis 2020; 11(8): 661.
[http://dx.doi.org/10.1038/s41419-020-02864-5] [PMID: 32814770]
[78]
Parks RJ, Menazza S, Holmström KM, et al. Cyclophilin D-mediated regulation of the permeability transition pore is altered in mice lacking the mitochondrial calcium uniporter. Cardiovasc Res 2019; 115(2): 385-94.
[http://dx.doi.org/10.1093/cvr/cvy218] [PMID: 30165576]
[79]
Rasola A, Sciacovelli M, Chiara F, Pantic B, Brusilow WS, Bernardi P. Activation of mitochondrial ERK protects cancer cells from death through inhibition of the permeability transition. Proc Natl Acad Sci USA 2010; 107(2): 726-31.
[http://dx.doi.org/10.1073/pnas.0912742107] [PMID: 20080742]
[80]
Giorgio V, Bisetto E, Soriano ME, et al. Cyclophilin D modulates mitochondrial F0F1-ATP synthase by interacting with the lateral stalk of the complex. J Biol Chem 2009; 284(49): 33982-8.
[http://dx.doi.org/10.1074/jbc.M109.020115] [PMID: 19801635]
[81]
Xu T, Ding W, Ao X, et al. ARC regulates programmed necrosis and myocardial ischemia/reperfusion injury through the inhibition of mPTP opening. Redox Biol 2019; 20: 414-26.
[http://dx.doi.org/10.1016/j.redox.2018.10.023] [PMID: 30415165]
[82]
Nolfi-Donegan D, Braganza A, Shiva S. Mitochondrial electron transport chain: Oxidative phosphorylation, oxidant production, and methods of measurement. Redox Biol 2020; 37: 101674.
[http://dx.doi.org/10.1016/j.redox.2020.101674] [PMID: 32811789]
[83]
Etzler JC, Bollo M, Holstein D, et al. Cyclophilin D over-expression increases mitochondrial complex III activity and accelerates supercomplex formation. Arch Biochem Biophys 2017; 613: 61-8.
[http://dx.doi.org/10.1016/j.abb.2016.11.008] [PMID: 27916505]
[84]
Teixeira G, Chiari P, Fauconnier J, et al. Involvement of cyclophilin D and calcium in isoflurane-induced preconditioning. Anesthesiology 2015; 123(6): 1374-84.
[http://dx.doi.org/10.1097/ALN.0000000000000876] [PMID: 26460965]
[85]
Teixeira G, Abrial M, Portier K, et al. Synergistic protective effect of cyclosporin A and rotenone against hypoxia–reoxygenation in cardiomyocytes. J Mol Cell Cardiol 2013; 56: 55-62.
[http://dx.doi.org/10.1016/j.yjmcc.2012.11.023] [PMID: 23238221]
[86]
Lam CK, Zhao W, Liu GS, et al. HAX-1 regulates cyclophilin-D levels and mitochondria permeability transition pore in the heart. Proc Natl Acad Sci USA 2015; 112(47): E6466-75.
[http://dx.doi.org/10.1073/pnas.1508760112] [PMID: 26553996]
[87]
Okahara A, Koga J, Matoba T, et al. Simultaneous targeting of mitochondria and monocytes enhances neuroprotection against ischemia–reperfusion injury. Sci Rep 2020; 10(1): 14435.
[http://dx.doi.org/10.1038/s41598-020-71326-x] [PMID: 32879367]
[88]
Lv B, Peng H, Qiu B, et al. Sulphenylation of CypD at cysteine 104: A novel mechanism by which SO2 inhibits cardiomyocyte apoptosis. Front Cell Dev Biol 2022; 9: 784799.
[http://dx.doi.org/10.3389/fcell.2021.784799] [PMID: 35118072]
[89]
Ong S-B, Dongworth RK, Cabrera-Fuentes HA, Hausenloy DJ. Role of the MPTP in conditioning the heart - translatability and mechanism. Br J Pharmacol 2015; 172(8): 2074-84.
[http://dx.doi.org/10.1111/bph.13013] [PMID: 25393318]
[90]
Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006; 443(7113): 787-95.
[http://dx.doi.org/10.1038/nature05292] [PMID: 17051205]
[91]
Zhang B, Jia K, Tian J, Du H. Cyclophilin D counterbalances mitochondrial calcium uniporter-mediated brain mitochondrial calcium uptake. Biochem Biophys Res Commun 2020; 529(2): 314-20.
[http://dx.doi.org/10.1016/j.bbrc.2020.05.204] [PMID: 32703429]
[92]
Du H, Guo L, Fang F, et al. Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer’s disease. Nat Med 2008; 14(10): 1097-105.
[http://dx.doi.org/10.1038/nm.1868] [PMID: 18806802]
[93]
Du H, Guo L, Zhang W, Rydzewska M, Yan S. Cyclophilin D deficiency improves mitochondrial function and learning/memory in aging Alzheimer disease mouse model. Neurobiol Aging 2011; 32(3): 398-406.
[http://dx.doi.org/10.1016/j.neurobiolaging.2009.03.003] [PMID: 19362755]
[94]
Sun Q, Jia N, Li X, Yang J, Chen G. Grape seed proanthocyanidins ameliorate neuronal oxidative damage by inhibiting GSK-3β-dependent mitochondrial permeability transition pore opening in an experimental model of sporadic Alzheimer’s disease. Aging 2019; 11(12): 4107-24.
[http://dx.doi.org/10.18632/aging.102041] [PMID: 31232699]
[95]
Hou W, Leong KG, Ozols E, Tesch GH, Nikolic-Paterson DJ, Ma FY. Cyclophilin D promotes tubular cell damage and the development of interstitial fibrosis in the obstructed kidney. Clin Exp Pharmacol Physiol 2018; 45(3): 250-60.
[http://dx.doi.org/10.1111/1440-1681.12881] [PMID: 29230844]
[96]
Jang HS, Noh MR, Ha L, Kim J, Padanilam BJ. Proximal tubule cyclophilin D mediates kidney fibrogenesis in obstructive nephropathy. Am J Physiol Renal Physiol 2021; 321(4): F431-42.
[http://dx.doi.org/10.1152/ajprenal.00171.2021] [PMID: 34396791]
[97]
Jang HS, Noh MR, Jung EM, et al. Proximal tubule cyclophilin D regulates fatty acid oxidation in cisplatin-induced acute kidney injury. Kidney Int 2020; 97(2): 327-39.
[http://dx.doi.org/10.1016/j.kint.2019.08.019] [PMID: 31733829]
[98]
Itani HA, Dikalova AE, McMaster WG, et al. Mitochondrial cyclophilin D in vascular oxidative stress and hypertension. Hypertension 2016; 67(6): 1218-27.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.115.07085] [PMID: 27067720]
[99]
He Y, Zhang L, Zhu Z, Xiao A, Yu H, Gan X. Blockade of cyclophilin D rescues dexamethasone-induced oxidative stress in gingival tissue. PLoS One 2017; 12(3): e0173270.
[http://dx.doi.org/10.1371/journal.pone.0173270] [PMID: 28273124]
[100]
Guo L, Du H, Yan S, et al. Cyclophilin D deficiency rescues axonal mitochondrial transport in Alzheimer’s neurons. PLoS One 2013; 8(1): e54914.
[http://dx.doi.org/10.1371/journal.pone.0054914] [PMID: 23382999]
[101]
Zhang L, Wu Y, Gao X, Guo F. Mitochondrial protein cyclophilin-D-mediated programmed necrosis attributes to berberine-induced cytotoxicity in cultured prostate cancer cells. Biochem Biophys Res Commun 2014; 450(1): 697-703.
[http://dx.doi.org/10.1016/j.bbrc.2014.06.039] [PMID: 24946211]
[102]
Linkermann A, Bräsen JH, Darding M, et al. Two independent pathways of regulated necrosis mediate ischemia–reperfusion injury. Proc Natl Acad Sci USA 2013; 110(29): 12024-9.
[http://dx.doi.org/10.1073/pnas.1305538110] [PMID: 23818611]
[103]
Begriche K, Massart J, Robin MA, Bonnet F, Fromenty B. Mitochondrial adaptations and dysfunctions in nonalcoholic fatty liver disease. Hepatology 2013; 58(4): 1497-507.
[http://dx.doi.org/10.1002/hep.26226] [PMID: 23299992]
[104]
Mansouri A, Gattolliat CH, Asselah T. Mitochondrial dysfunction and signaling in chronic liver diseases. Gastroenterology 2018; 155(3): 629-47.
[http://dx.doi.org/10.1053/j.gastro.2018.06.083] [PMID: 30012333]
[105]
Wang X, Du H, Shao S, et al. Cyclophilin D deficiency attenuates mitochondrial perturbation and ameliorates hepatic steatosis. Hepatology 2018; 68(1): 62-77.
[http://dx.doi.org/10.1002/hep.29788] [PMID: 29356058]
[106]
Kai S, Lu J, Hui P, Zhao H. Pre-clinical evaluation of cinobufotalin as a potential anti-lung cancer agent. Biochem Biophys Res Commun 2014; 452(3): 768-74.
[http://dx.doi.org/10.1016/j.bbrc.2014.08.147] [PMID: 25201730]
[107]
Qiu Y, Yu T, Wang W, Pan K, Shi D, Sun H. Curcumin-induced melanoma cell death is associated with mitochondrial permeability transition pore (mPTP) opening. Biochem Biophys Res Commun 2014; 448(1): 15-21.
[http://dx.doi.org/10.1016/j.bbrc.2014.04.024] [PMID: 24735534]
[108]
Clarke SJ, McStay GP, Halestrap AP. Sanglifehrin A acts as a potent inhibitor of the mitochondrial permeability transition and reperfusion injury of the heart by binding to cyclophilin-D at a different site from cyclosporin A. J Biol Chem 2002; 277(38): 34793-9.
[http://dx.doi.org/10.1074/jbc.M202191200] [PMID: 12095984]
[109]
Guada M, Beloqui A, Kumar MNVR, Préat V, Dios-Viéitez MC, Blanco-Prieto MJ. Reformulating cyclosporine A (CsA): More than just a life cycle management strategy. J Control Release 2016; 225: 269-82.
[http://dx.doi.org/10.1016/j.jconrel.2016.01.056] [PMID: 26829101]
[110]
Zhen Y, Wang G, Zhu L, et al. P53 dependent mitochondrial permeability transition pore opening is required for dexamethasone-induced death of osteoblasts. J Cell Physiol 2014; 229(10): 1475-83.
[http://dx.doi.org/10.1002/jcp.24589] [PMID: 24615518]
[111]
Elrod JW, Wong R, Mishra S, et al. Cyclophilin D controls mitochondrial pore–dependent Ca2+ exchange, metabolic flexibility, and propensity for heart failure in mice. J Clin Invest 2010; 120(10): 3680-7.
[http://dx.doi.org/10.1172/JCI43171] [PMID: 20890047]
[112]
Chang CF, Flaxman HA, Woo CM. Enantioselective synthesis and biological evaluation of sanglifehrin A and B and analogs. Angew Chem Int Ed 2021; 60(31): 17045-52.
[http://dx.doi.org/10.1002/anie.202103022] [PMID: 34014025]
[113]
Fehr T, Kallen J, Oberer L, Sanglier JJ, Schilling W, Sanglifehrins A. Sanglifehrins A, B, C and D, novel cyclophilin-binding compounds isolated from Streptomyces sp. A92-308110. II. Structure elucidation, stereochemistry and physico-chemical properties. J Antibiot 1999; 52(5): 474-9.
[http://dx.doi.org/10.7164/antibiotics.52.474] [PMID: 10480571]
[114]
Immecke SN, Baal N, Wilhelm J, et al. The cyclophilin-binding agent Sanglifehrin A is a dendritic cell chemokine and migration inhibitor. PLoS One 2011; 6(3): e18406.
[http://dx.doi.org/10.1371/journal.pone.0018406] [PMID: 21483789]
[115]
Hackstein H, Steinschulte C, Fiedel S, et al. Sanglifehrin a blocks key dendritic cell functions in vivo and promotes long-term allograft survival together with low-dose CsA. Am J Transplant 2007; 7(4): 789-98.
[http://dx.doi.org/10.1111/j.1600-6143.2006.01729.x] [PMID: 17391124]
[116]
Zhang LH, Liu JO, Sanglifehrin A. Sanglifehrin A, a novel cyclophilin-binding immunosuppressant, inhibits IL-2-dependent T cell proliferation at the G1 phase of the cell cycle. J Immunol 2001; 166(9): 5611-8.
[http://dx.doi.org/10.4049/jimmunol.166.9.5611] [PMID: 11313401]
[117]
Zhang LH, Youn HD, Liu JO. Inhibition of cell cycle progression by the novel cyclophilin ligand sanglifehrin A is mediated through the NFkappa B-dependent activation of p53. J Biol Chem 2001; 276(47): 43534-40.
[http://dx.doi.org/10.1074/jbc.M104257200] [PMID: 11557753]
[118]
Han J, Lee MK, Jang Y, Cho WJ, Kim M. Repurposing of cyclophilin A inhibitors as broad-spectrum antiviral agents. Drug Discov Today 2022; 27(7): 1895-912.
[http://dx.doi.org/10.1016/j.drudis.2022.05.016] [PMID: 35609743]
[119]
Fu M, Shi W, Li Z, Liu H. Activation of mPTP-dependent mitochondrial apoptosis pathway by a novel pan HDAC inhibitor resminostat in hepatocellular carcinoma cells. Biochem Biophys Res Commun 2016; 477(4): 527-33.
[http://dx.doi.org/10.1016/j.bbrc.2016.04.147] [PMID: 27144317]
[120]
Gregory MA, Bobardt M, Obeid S, et al. Preclinical characterization of naturally occurring polyketide cyclophilin inhibitors from the sanglifehrin family. Antimicrob Agents Chemother 2011; 55(5): 1975-81.
[http://dx.doi.org/10.1128/AAC.01627-10] [PMID: 21383094]
[121]
Javadov SA, Clarke S, Das M, Griffiths EJ, Lim KHH, Halestrap AP. Ischaemic preconditioning inhibits opening of mitochondrial permeability transition pores in the reperfused rat heart. J Physiol 2003; 549(2): 513-24.
[http://dx.doi.org/10.1113/jphysiol.2003.034231] [PMID: 12692185]
[122]
Shanmuganathan S, Hausenloy DJ, Duchen MR, Yellon DM. Mitochondrial permeability transition pore as a target for cardioprotection in the human heart. Am J Physiol Heart Circ Physiol 2005; 289(1): H237-42.
[http://dx.doi.org/10.1152/ajpheart.01192.2004] [PMID: 15961375]
[123]
Qin L, Jia P, Zhang Z, Zhang S. ROS-p53-cyclophilin-D signaling mediates salinomycin-induced glioma cell necrosis. J Exp Clin Cancer Res 2015; 34(1): 57.
[http://dx.doi.org/10.1186/s13046-015-0174-1] [PMID: 26024660]
[124]
Chen W, Feng L, Nie H, Zheng X. Andrographolide induces autophagic cell death in human liver cancer cells through cyclophilin D-mediated mitochondrial permeability transition pore. Carcinogenesis 2012; 33(11): 2190-8.
[http://dx.doi.org/10.1093/carcin/bgs264] [PMID: 22869602]

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