210
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Anastrozole-mediated modulation of mitochondrial activity by inhibition of mitochondrial permeability transition pore opening: an initial perspective

ORCID Icon, , , ORCID Icon, , , , , , , ORCID Icon, , , , ORCID Icon, ORCID Icon & show all
Pages 14063-14079 | Received 12 Sep 2022, Accepted 31 Jan 2023, Published online: 23 Feb 2023

References

  • Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
  • Adams, V., Bosch, W., Schlegel, J., Wallimann, T., & Brdiczka, D. (1989). Further characterization of contact sites from mitochondria of different tissues: Topology of peripheral kinases. Biochimica et Biophysica Acta, 981(2), 213–225. https://doi.org/10.1016/0005-2736(89)90031-X
  • Al-Basheer, A., Huang, J., Kaminski, J., Dasher, B., Howington, J., Stewart, J., Martin, D., Jin, J., & Kong, F. P. (2014). Correlation of integral dose, white blood cell counts, and radiation therapy techniques for head and neck cancer patients under radiation therapy. International Journal of Radiation Oncology, Biology, Physics, 90(1), S574. https://doi.org/10.1016/j.ijrobp.2014.05.1730
  • Bacman, S. R., Williams, S. L., Pinto, M., Peralta, S., & Moraes, C. T. (2013). Specific elimination of mutant mitochondrial genomes in patient-derived cells by mitoTALENs. Nature Medicine, 19(9), 1111–1113. https://doi.org/10.1038/nm.3261
  • Baines, C. P., Kaiser, R. A., Purcell, N. H., Blair, N. S., Osinska, H., Hambleton, M. A., Brunskill, E. W., Sayen, M. R., Gottlieb, R. A., Dorn, G. W., Robbins, J., & Molkentin, J. D. (2005). Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature, 434(7033), 658–662. https://doi.org/10.1038/nature03434
  • Berendsen, H. J. C., Grigera, J. R., & Straatsma, T. P. (1987). The missing term in effective pair potentials. The Journal of Physical Chemistry, 91(24), 6269–6271. https://doi.org/10.1021/j100308a038
  • Bertolazzi, P., Bock, M. E., & Guerra, C. (2013). On the functional and structural characterization of hubs in protein–protein interaction networks. Biotechnology Advances, 31(2), 274–286. https://doi.org/10.1016/j.biotechadv.2012.12.002
  • Brand, M. D., Chien, L. F., & Rolfe, D. F. (1993). Control of oxidative phosphorylation in liver mitochondria and hepatocytes. Biochemical Society Transactions, 21 (Pt 3)(3), 757–762. https://doi.org/10.1042/bst0210757
  • Bücheler, K., Adams, V., & Brdiczka, D. (1991). Localization of the ATP/ADP translocator in the inner membrane and regulation of contact sites between mitochondrial envelope membranes by ADP. A study on freeze-fractured isolated liver mitochondria. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1056(3), 233–242. https://doi.org/10.1016/S0005-2728(05)80054-4
  • Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. The Journal of Chemical Physics, 126(1), 014101. https://doi.org/10.1063/1.2408420
  • Buttgereit, F., & Brand, M. D. (1995). A hierarchy of ATP-consuming processes in mammalian cells. Biochemical Journal. 312 (Pt 1), 163–167. https://doi.org/10.1042/bj3120163
  • Chinopoulos, C. (2011). Mitochondrial consumption of cytosolic ATP: Not so fast. FEBS Letters, 585(9), 1255–1259. https://doi.org/10.1016/j.febslet.2011.04.004
  • Chinopoulos, C., & Adam-Vizi, V. (2012). Modulation of the mitochondrial permeability transition by cyclophilin D: Moving closer to F(0)-F(1) ATP Synthase? Mitochondrion, 12(1), 41–45. https://doi.org/10.1016/j.mito.2011.04.007
  • Chinopoulos, C., Gerencser, A. A., Mandi, M., Mathe, K., Töröcsik, B., Doczi, J., Turiak, L., Kiss, G., Konràd, C., Vajda, S., Vereczki, V., Oh, R. J., & Adam-Vizi, V. (2010). Forward operation of adenine nucleotide translocase during F0F1-ATPase reversal: Critical role of matrix substrate-level phosphorylation. FASEB Journal, 24(7), 2405–2416. https://doi.org/10.1096/fj.09-149898
  • Chinopoulos, C., Starkov, A. A., & Fiskum, G. (2003). Cyclosporin A-insensitive permeability transition in brain mitochondria: Inhibition by 2-aminoethoxydiphenyl borate. The Journal of Biological Chemistry, 278(30), 27382–27389. https://doi.org/10.1074/jbc.M303808200
  • Chinopoulos, C., Vajda, S., Csanády, L., Mándi, M., Mathe, K., & Adam-Vizi, V. (2009). A novel kinetic assay of mitochondrial ATP-ADP exchange rate mediated by the ANT. Biophysical Journal, 96(6), 2490–2504. https://doi.org/10.1016/j.bpj.2008.12.3915
  • Chouchani, E. T., Pell, V. R., Gaude, E., Aksentijević, D., Sundier, S. Y., Robb, E. L., Logan, A., Nadtochiy, S. M., Ord, E. N. J., Smith, A. C., Eyassu, F., Shirley, R., Hu, C.-H., Dare, A. J., James, A. M., Rogatti, S., Hartley, R. C., Eaton, S., Costa, A. S. H., … Murphy, M. P. (2014). Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature, 515(7527), 431–435. https://doi.org/10.1038/nature13909
  • Choudhary, N., Choudhary, S., Kumar, A., & Singh, V. (2020). Deciphering the multi-scale mechanisms of Tephrosia purpurea against polycystic ovarian syndrome (PCOS) and its major psychiatric comorbidities: Studies from network pharmacological perspective. Gene, 773, 145385. https://doi.org/10.1016/j.gene.2020.145385
  • Choudhary, N., & Singh, V. (2019). Insights about multi-targeting and synergistic neuromodulators in Ayurvedic herbs against epilepsy: Integrated computational studies on drug-target and protein-protein interaction networks. Scientific Reports, 9(1), 10565. https://doi.org/10.1038/s41598-019-46715-6
  • Clarke, S. J., McStay, G. P., & Halestrap, A. P. (2002). 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. Journal of Biological Chemistry, 277(38), 34793–34799. https://doi.org/10.1074/jbc.M202191200
  • Cotán, D., Cordero, M. D., Garrido-Maraver, J., Oropesa-Ávila, M., Rodríguez-Hernández, A., Gómez Izquierdo, L., De la Mata, M., De Miguel, M., Lorite, J. B., Infante, E. R., Jackson, S., Navas, P., & Sánchez-Alcázar, J. A. (2011). Secondary coenzyme Q10 deficiency triggers mitochondria degradation by mitophagy in MELAS fibroblasts. FASEB Journal, 25(8), 2669–2687. https://doi.org/10.1096/fj.10-165340
  • Crompton, M., McGuinness, O., & Nazareth, W. (1992). The involvement of cyclosporin A binding proteins in regulating and uncoupling mitochondrial energy transduction. Biochimica et Biophysica Acta, 1101(2), 214–217. internal-pdf://0.0.0.115/Manuscript.docx
  • Daina, A., Michielin, O., & Zoete, V. (2019). SwissTargetPrediction: Updated data and new features for efficient prediction of protein targets of small molecules. Nucleic Acids Research, 47(W1), W357–W364. https://doi.org/10.1093/nar/gkz382
  • Davis, T. L., Walker, J. R., Campagna-Slater, V., Finerty, P. J., Paramanathan, R., Bernstein, G., MacKenzie, F., Tempel, W., Ouyang, H., Lee, W. H., Eisenmesser, E. Z., & Dhe-Paganon, S. (2010). Structural and biochemical characterization of the human cyclophilin family of peptidyl-prolyl isomerases. PLoS Biology, 8(7), e1000439. https://doi.org/10.1371/journal.pbio.1000439
  • De Giorgio, R., Pironi, L., Rinaldi, R., Boschetti, E., Caporali, L., Capristo, M., Casali, C., Cenacchi, G., Contin, M., D'Angelo, R., D'Errico, A., Gramegna, L. L., Lodi, R., Maresca, A., Mohamed, S., Morelli, M. C., Papa, V., Tonon, C., Tugnoli, V., … Pinna, A. D. (2016). Liver transplantation for mitochondrial neurogastrointestinal encephalomyopathy. Annals of Neurology, 80(3), 448–455. https://doi.org/10.1002/ana.24724
  • DeLano, W. L. (2002). Pymol: An open-source molecular graphics tool. {CCP4} Newsletter on Protein Crystallography, 40. https://www.ccp4.ac.uk/newsletters/newsletter40/11_pymol.pdf
  • Demory, M. L., Boerner, J. L., Davidson, R., Faust, W., Miyake, T., Lee, I., Hüttemann, M., Douglas, R., Haddad, G., & Parsons, S. J. (2009). Epidermal growth factor receptor translocation to the mitochondria. Journal of Biological Chemistry, 284(52), 36592–36604. https://doi.org/10.1074/jbc.M109.000760
  • Dikalov, S. I., & Harrison, D. G. (2014). Methods for detection of mitochondrial and cellular reactive oxygen species. Antioxidants & Redox Signaling, 20(2), 372–382. https://doi.org/10.1089/ars.2012.4886
  • Diwan, A., Matkovich, S. J., Yuan, Q., Zhao, W., Yatani, A., Brown, J. H., Molkentin, J. D., Kranias, E. G., & Dorn, G. W. (2009). Endoplasmic reticulum-mitochondria crosstalk in NIX-mediated murine cell death. The Journal of Clinical Investigation, 119(1), 203–212. https://doi.org/10.1172/JCI36445
  • Du, H., Guo, L., Fang, F., Chen, D., Sosunov, A. A., McKhann, G. M., Yan, Y., Wang, C., Zhang, H., Molkentin, J. D., Gunn-Moore, F. J., Vonsattel, J. P., Arancio, O., Chen, J. X., & Yan, S. D. (2008). Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer’s disease. Nature Medicine, 14(10), 1097–1105. https://doi.org/10.1038/nm.1868
  • Dube, H., Selwood, D., Malouitre, S., Capano, M., Simone, M. I., & Crompton, M. (2012). A mitochondrial-targeted cyclosporin A with high binding affinity for cyclophilin D yields improved cytoprotection of cardiomyocytes. The Biochemical Journal, 441(3), 901–907. https://doi.org/10.1042/BJ20111301
  • Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. G. (1995). A smooth particle mesh Ewald method. The Journal of Chemical Physics, 103(19), 8577–8593. https://doi.org/10.1063/1.470117
  • Fischer, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T., & Schmid, F. X. (1989). Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature, 337(6206), 476–478. https://doi.org/10.1038/337476a0
  • Gammage, P. A., Rorbach, J., Vincent, A. I., Rebar, E. J., & Minczuk, M. (2014). Mitochondrially targeted ZFNs for selective degradation of pathogenic mitochondrial genomes bearing large-scale deletions or point mutations. EMBO Molecular Medicine, 6(4), 458–466. https://doi.org/10.1002/emmm.201303672
  • Garone, C., Garcia-Diaz, B., Emmanuele, V., Lopez, L. C., Tadesse, S., Akman, H. O., Tanji, K., Quinzii, C. M., & Hirano, M. (2014). Deoxypyrimidine monophosphate bypass therapy for thymidine kinase 2 deficiency. EMBO Molecular Medicine, 6(8), 1016–1027. https://doi.org/10.15252/emmm.201404092
  • Giorgio, V., Bisetto, E., Soriano, M. E., Dabbeni-Sala, F., Basso, E., Petronilli, V., Forte, M. A., Bernardi, P., & Lippe, G. (2009). Cyclophilin D modulates mitochondrial F0F1-ATP synthase by interacting with the lateral stalk of the complex. The Journal of Biological Chemistry, 284(49), 33982–33988. https://doi.org/10.1074/jbc.M109.020115
  • Gorman, G. S., Chinnery, P. F., DiMauro, S., Hirano, M., Koga, Y., McFarland, R., Suomalainen, A., Thorburn, D. R., Zeviani, M., & Turnbull, D. M. (2016). Mitochondrial diseases. Nature Reviews. Disease Primers, 2, 16080. https://doi.org/10.1038/nrdp.2016.80
  • Guidotti, S., Minguzzi, M., Platano, D., Santi, S., Trisolino, G., Filardo, G., Mariani, E., & Borzì, R. M. (2017). Glycogen synthase kinase-3β inhibition links mitochondrial dysfunction, extracellular matrix remodelling and terminal differentiation in chondrocytes. Scientific Reports, 7(1), 12059. https://doi.org/10.1038/s41598-017-12129-5
  • Gunter, T. E., & Pfeiffer, D. R. (1990). Mechanisms by which mitochondria transport calcium. The American Journal of Physiology, 258(5 Pt 1), C755–786. https://doi.org/10.1152/ajpcell.1990.258.5.C755
  • Gutiérrez-Aguilar, M., Douglas, D. L., Gibson, A. K., Domeier, T. L., Molkentin, J. D., & Baines, C. P. (2014). Genetic manipulation of the cardiac mitochondrial phosphate carrier does not affect permeability transition. Journal of Molecular and Cellular Cardiology, 72, 316–325. https://doi.org/10.1016/j.yjmcc.2014.04.008
  • Halestrap, A. P. (2009). What is the mitochondrial permeability transition pore? Journal of Molecular and Cellular Cardiology, 46(6), 821–831. https://doi.org/10.1016/j.yjmcc.2009.02.021
  • Halter, J. P., Michael, W., Schüpbach, M., Mandel, H., Casali, C., Orchard, K., Collin, M., Valcarcel, D., Rovelli, A., Filosto, M., Dotti, M. T., Marotta, G., Pintos, G., Barba, P., Accarino, A., Ferra, C., Illa, I., Beguin, Y., Bakker, J. A., … Hirano, M. (2015). Allogeneic haematopoietic stem cell transplantation for mitochondrial neurogastrointestinal encephalomyopathy. Brain: A Journal of Neurology, 138, 2847–2858. https://doi.org/10.1093/brain/awv226
  • Hansson, M. J., Morota, S., Chen, L., Matsuyama, N., Suzuki, Y., Nakajima, S., Tanoue, T., Omi, A., Shibasaki, F., Shimazu, M., Ikeda, Y., Uchino, H., & Elmér, E. (2011). Cyclophilin D-sensitive mitochondrial permeability transition in adult human brain and liver mitochondria. Journal of Neurotrauma, 28(1), 143–153. https://doi.org/10.1089/neu.2010.1613
  • Hansson, M. J., Persson, T., Friberg, H., Keep, M. F., Rees, A., Wieloch, T., & Elmér, E. (2003). Powerful cyclosporin inhibition of calcium-induced permeability transition in brain mitochondria. Brain Research, 960(1–2), 99–111. https://doi.org/10.1016/s0006-8993(02)03798-8
  • Haroon, M. F., Fatima, A., Schöler, S., Gieseler, A., Horn, T. F. W., Kirches, E., Wolf, G., & Kreutzmann, P. (2007). Minocycline, a possible neuroprotective agent in Leber’s hereditary optic neuropathy (LHON): Studies of cybrid cells bearing 11,778 mutation. Neurobiology of Disease, 28(3), 237–250. https://doi.org/10.1016/j.nbd.2007.07.021
  • He, J., Carroll, J., Ding, S., Fearnley, I. M., & Walker, J. E. (2017). Permeability transition in human mitochondria persists in the absence of peripheral stalk subunits of ATP synthase. Proceedings of the National Academy of Sciences of the United States of America, 114(34), 9086–9091. https://doi.org/10.1073/pnas.1711201114
  • He, J., Ford, H. C., Carroll, J., Ding, S., Fearnley, I. M., & Walker, J. E. (2017). Persistence of the mitochondrial permeability transition in the absence of subunit c of human ATP synthase. Proceedings of the National Academy of Sciences of the United States of America, 114(13), 3409–3414. https://doi.org/10.1073/pnas.1702357114
  • Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12 < 1463::AID-JCC4 > 3.0.CO;2-H
  • Hsiao, C.-W., Peng, T.-I., Peng, A. C., Reiter, R. J., Tanaka, M., Lai, Y.-K., & Jou, M.-J. (2013). Long-term Aβ exposure augments mCa2+-independent mROS-mediated depletion of cardiolipin for the shift of a lethal transient mitochondrial permeability transition to its permanent mode in NARP cybrids: A protective targeting of melatonin. Journal of Pineal Research, 54(1), 107–125. https://doi.org/10.1111/jpi.12004
  • Huang, W.-Y., Jou, M.-J., & Peng, T.-I. (2014). Hypoxic preconditioning-induced mitochondrial protection is not disrupted in a cell model of mtDNA T8993G mutation-induced F1F0-ATP synthase defect: The role of mitochondrial permeability transition. Free Radical Biology & Medicine, 67, 314–329. https://doi.org/10.1016/j.freeradbiomed.2013.11.019
  • Hunter, D. R., & Haworth, R. A. (1979). The Ca2+-induced membrane transition in mitochondria. Archives of Biochemistry and Biophysics, 195(2), 468–477. https://doi.org/10.1016/0003-9861(79)90373-4
  • Hyun, S., Park, N., Nam, S. H., Cheon, D. H., Lee, Y., Lim, H.-S., & Yu, J. (2021). One-bead-one-compound screening approach to the identification of cyclic peptoid inhibitors of cyclophilin D as neuroprotective agents from mitochondrial dysfunction. Chemical Communications, 57(19), 2388–2391. https://doi.org/10.1039/D0CC08268F
  • Kajitani, K., Fujihashi, M., Kobayashi, Y., Shimizu, S., Tsujimoto, Y., & Miki, K. (2008). Crystal structure of human cyclophilin D in complex with its inhibitor, cyclosporin A at 0.96-A resolution. Proteins, 70(4), 1635–1639. https://doi.org/10.1002/prot.21855
  • Kawamata, H., Starkov, A. A., Manfredi, G., & Chinopoulos, C. (2010). A kinetic assay of mitochondrial ADP-ATP exchange rate in permeabilized cells. Analytical Biochemistry, 407(1), 52–57. https://doi.org/10.1016/j.ab.2010.07.031
  • Kinnally, K. W., Campo, M. L., & Tedeschi, H. (1989). Mitochondrial channel activity studied by patch-clamping mitoplasts. Journal of Bioenergetics and Biomembranes, 21(4), 497–506. https://doi.org/10.1007/BF00762521
  • Klopstock, T., Yu-Wai-Man, P., Dimitriadis, K., Rouleau, J., Heck, S., Bailie, M., Atawan, A., Chattopadhyay, S., Schubert, M., Garip, A., Kernt, M., Petraki, D., Rummey, C., Leinonen, M., Metz, G., Griffiths, P. G., Meier, T., & Chinnery, P. F. (2011). A randomized placebo-controlled trial of idebenone in Leber’s hereditary optic neuropathy. Brain, 134(9), 2677–2686. https://doi.org/10.1093/brain/awr170
  • Kumalo, H. M., Bhakat, S., & Soliman, M. E. S. (2015). Theory and applications of covalent docking in drug discovery: Merits and pitfalls. Molecules, 20(2), 1984–2000. https://doi.org/10.3390/molecules20021984
  • Kumar, A., Choudhary, S., Adhikari, J. S., & Chaudhury, N. K. (2018). Sesamol ameliorates radiation induced DNA damage in hematopoietic system of whole body γ-irradiated mice. Environmental and Molecular Mutagenesis, 59(1), 79–90. https://doi.org/10.1002/em.22118
  • Kumar, A., Choudhary, S., Kumar, S., Adhikari, J. S., Kapoor, S., & Chaudhury, N. K. (2022). Role of melatonin mediated G-CSF induction in hematopoietic system of gamma-irradiated mice. Life Sciences, 289, 120190. https://doi.org/10.1016/j.lfs.2021.120190
  • Kwong, J. Q., Davis, J., Baines, C. P., Sargent, M. A., Karch, J., Wang, X., Huang, T., & Molkentin, J. D. (2014). Genetic deletion of the mitochondrial phosphate carrier desensitizes the mitochondrial permeability transition pore and causes cardiomyopathy. Cell Death and Differentiation, 21(8), 1209–1217. https://doi.org/10.1038/cdd.2014.36
  • La Morgia, C., Carbonelli, M., Barboni, P., Sadun, A. A., & Carelli, V. (2014). Medical management of hereditary optic neuropathies. Frontiers in Neurology, 5, 141. https://doi.org/10.3389/fneur.2014.00141
  • Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
  • Lim, S. Y., Hausenloy, D. J., Arjun, S., Price, A. N., Davidson, S. M., Lythgoe, M. F., & Yellon, D. M. (2011). Mitochondrial cyclophilin-D as a potential therapeutic target for post-myocardial infarction heart failure. Journal of Cellular and Molecular Medicine, 15(11), 2443–2451. https://doi.org/10.1111/j.1582-4934.2010.01235.x
  • Liu, R. R., & Murphy, T. H. (2009). Reversible cyclosporin A-sensitive mitochondrial depolarization occurs within minutes of stroke onset in mouse somatosensory cortex in vivo: A two-photon imaging study. Journal of Biological Chemistry, 284(52), 36109–36117. https://doi.org/10.1074/jbc.M109.055301
  • Lopez-Gomez, C., Levy, R. J., Sanchez-Quintero, M. J., Juanola-Falgarona, M., Barca, E., Garcia-Diaz, B., Tadesse, S., Garone, C., & Hirano, M. (2017). Deoxycytidine and deoxythymidine treatment for thymidine kinase 2 deficiency. Annals of Neurology, 81(5), 641–652. https://doi.org/10.1002/ana.24922
  • Millay, D. P., Sargent, M. A., Osinska, H., Baines, C. P., Barton, E. R., Vuagniaux, G., Sweeney, H. L., Robbins, J., & Molkentin, J. D. (2008). Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nature Medicine, 14(4), 442–447. https://doi.org/10.1038/nm1736
  • Mlejnek, P. (2001). Caspase-3 activity and carbonyl cyanide m-chlorophenylhydrazone-induced apoptosis in HL-60. Alternatives to Laboratory Animals : ATLA, 29(3), 243–249. https://doi.org/10.1177/026119290102900313
  • Morava, E., van den Heuvel, L., Hol, F., de Vries, M. C., Hogeveen, M., Rodenburg, R. J., & Smeitink, J. A. M. (2006). Mitochondrial disease criteria: Diagnostic applications in children. Neurology, 67(10), 1823–1826. https://doi.org/10.1212/01.wnl.0000244435.27645.54
  • Morita, N., Sovari, A. A., Xie, Y., Fishbein, M. C., Mandel, W. J., Garfinkel, A., Lin, S.-F., Chen, P.-S., Xie, L.-H., Chen, F., Qu, Z., Weiss, J. N., & Karagueuzian, H. S. (2009). Increased susceptibility of aged hearts to ventricular fibrillation during oxidative stress. American Journal of Physiology. Heart and Circulatory Physiology, 297(5), H1594–605. https://doi.org/10.1152/ajpheart.00579.2009
  • Moro, L., Arbini, A. A., Hsieh, J.-T., Ford, J., Simpson, E. R., Hajibeigi, A., & Oz, O. K. (2010). Aromatase deficiency inhibits the permeability transition in mouse liver mitochondria. Endocrinology, 151(4), 1643–1652. https://doi.org/10.1210/en.2009-1450
  • Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. https://doi.org/10.1002/jcc.21256
  • Nguyen, T. T. M., Wong, R., Menazza, S., Sun, J., Chen, Y., Wang, G., Gucek, M., Steenbergen, C., Sack, M. N., & Murphy, E. (2013). Cyclophilin D modulates mitochondrial acetylome. Circulation Research, 113(12), 1308–1319. https://doi.org/10.1161/CIRCRESAHA.113.301867
  • Nicholls, D. G. (2009). Mitochondrial calcium function and dysfunction in the central nervous system. Biochimica et Biophysica Acta, 1787(11), 1416–1424. https://doi.org/10.1016/j.bbabio.2009.03.010
  • Oostenbrink, C., Villa, A., Mark, A. E., & van Gunsteren, W. F. (2004). A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6. Journal of Computational Chemistry, 25(13), 1656–1676. https://doi.org/10.1002/jcc.20090
  • Orrenius, S., Gogvadze, V., & Zhivotovsky, B. (2015). Calcium and mitochondria in the regulation of cell death. Biochemical and Biophysical Research Communications, 460(1), 72–81. https://doi.org/10.1016/j.bbrc.2015.01.137
  • Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/10.1063/1.328693
  • Petit, P. X., Lecoeur, H., Zorn, E., Dauguet, C., Mignotte, B., & Gougeon, M. L. (1995). Alterations in mitochondrial structure and function are early events of dexamethasone-induced thymocyte apoptosis. The Journal of Cell Biology, 130(1), 157–167. https://doi.org/10.1083/jcb.130.1.157
  • Petronilli, V., Szabò, I., & Zoratti, M. (1989). The inner mitochondrial membrane contains ion-conducting channels similar to those found in bacteria. FEBS Letters, 259(1), 137–143. https://doi.org/10.1016/0014-5793(89)81513-3
  • Pfeffer, G., Horvath, R., Klopstock, T., Mootha, V. K., Suomalainen, A., Koene, S., Hirano, M., Zeviani, M., Bindoff, L. A., Yu-Wai-Man, P., Hanna, M., Carelli, V., McFarland, R., Majamaa, K., Turnbull, D. M., Smeitink, J., & Chinnery, P. F. (2013). New treatments for mitochondrial disease-no time to drop our standards. Nature Reviews. Neurology, 9(8), 474–481. https://doi.org/10.1038/nrneurol.2013.129
  • Porcelli, A. M., Angelin, A., Ghelli, A., Mariani, E., Martinuzzi, A., Carelli, V., Petronilli, V., Bernardi, P., & Rugolo, M. (2009). Respiratory complex I dysfunction due to mitochondrial DNA mutations shifts the voltage threshold for opening of the permeability transition pore toward resting levels. The Journal of Biological Chemistry, 284(4), 2045–2052. https://doi.org/10.1074/jbc.M807321200
  • Porter, G. A. J., & Beutner, G. (2018). Cyclophilin D, somehow a master regulator of mitochondrial function. Biomolecules, 8(4), 176. https://doi.org/10.3390/biom8040176
  • Rao, V. K., Carlson, E. A., & Yan, S. S. (2014). Mitochondrial permeability transition pore is a potential drug target for neurodegeneration. Biochimica et Biophysica Acta, 1842(8), 1267–1272. https://doi.org/10.1016/j.bbadis.2013.09.003
  • Russmann, S., Kullak-Ublick, G. A., & Grattagliano, I. (2009). Current concepts of mechanisms in drug-induced hepatotoxicity. Current Medicinal Chemistry, 16(23), 3041–3053. https://doi.org/10.2174/092986709788803097
  • Schlatter, D., Thoma, R., Küng, E., Stihle, M., Müller, F., Borroni, E., Cesura, A., & Hennig, M. (2005). Crystal engineering yields crystals of cyclophilin D diffracting to 1.7 Å resolution. Acta Crystallographica. Section D, Biological Crystallography, 61(Pt 5), 513–519. https://doi.org/10.1107/S0907444905003070
  • Schüttelkopf, A. W., & van Aalten, D. M. F. (2004). PRODRG: A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallographica. Section D, Biological Crystallography, 60(Pt 8), 1355–1363. https://doi.org/10.1107/S0907444904011679
  • Scialò, F., Fernández-Ayala, D. J., & Sanz, A. (2017). Role of mitochondrial reverse electron transport in ROS signaling: Potential roles in health and disease. Frontiers in Physiology, 8, 428. https://doi.org/10.3389/fphys.2017.00428
  • Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003). Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Research, 13(11), 2498–2504. http://www.genome.org/cgi/doi/10.1101/gr.1239303.
  • Shore, E. R., Awais, M., Kershaw, N. M., Gibson, R. R., Pandalaneni, S., Latawiec, D., Wen, L., Javed, M. A., Criddle, D. N., Berry, N., O'Neill, P. M., Lian, L.-Y., & Sutton, R. (2016). Small molecule inhibitors of cyclophilin D to protect mitochondrial function as a potential treatment for acute pancreatitis. Journal of Medicinal Chemistry, 59(6), 2596–2611. https://doi.org/10.1021/acs.jmedchem.5b01801
  • Šileikytė, J., Blachly-Dyson, E., Sewell, R., Carpi, A., Menabò, R., Di Lisa, F., Ricchelli, F., Bernardi, P., & Forte, M. (2014). Regulation of the mitochondrial permeability transition pore by the outer membrane does not involve the peripheral benzodiazepine receptor (Translocator Protein of 18 kDa (TSPO). Journal of Biological Chemistry, 289(20), 13769–13781. https://doi.org/10.1074/jbc.M114.549634
  • Sorgato, M. C., Keller, B. U., & Stühmer, W. (1987). Patch-clamping of the inner mitochondrial membrane reveals a voltage-dependent ion channel. Nature, 330(6147), 498–500. https://doi.org/10.1038/330498a0
  • Szklarczyk, D., Gable, A. L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N. T., Morris, J. H., Bork, P., Jensen, L. J., & Mering, C. V. (2019). ST RING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res., 47(1), 607–613. https://doi.org/10.1093/nar/gky1131.
  • Takahashi, N., Hayano, T., & Suzuki, M. (1989). Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature, 337(6206), 473–475. https://doi.org/10.1038/337473a0
  • Tatton, W. G., & Olanow, C. W. (1999). Apoptosis in neurodegenerative diseases: The role of mitochondria. Biochimica et Biophysica Acta, 1410(2), 195–213. https://doi.org/10.1016/s0005-2728(98)00167-4
  • Tsujimoto, Y., & Shimizu, S. (2007). Role of the mitochondrial membrane permeability transition in cell death. Apoptosis : An International Journal on Programmed Cell Death, 12(5), 835–840. https://doi.org/10.1007/s10495-006-0525-7
  • Varanyuwatana, P., & Halestrap, A. P. (2012). The roles of phosphate and the phosphate carrier in the mitochondrial permeability transition pore. Mitochondrion, 12(1), 120–125. https://doi.org/10.1016/j.mito.2011.04.006
  • Waldmeier, P. C., Zimmermann, K., Qian, T., Tintelnot-Blomley, M., & Lemasters, J. J. (2003). Cyclophilin D as a drug target. Current Medicinal Chemistry, 10(16), 1485–1506. https://doi.org/10.2174/0929867033457160
  • Wallace, A. C., Laskowski, R. A., & Thornton, J. M. (1995). LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Engineering, 8(2), 127–134.
  • Webb, B., & Sali, A. (2016). Comparative protein structure modeling using MODELLER. Current Protocols in Bioinformatics, 2016(1), 5.6.1–5.6.37. https://doi.org/10.1002/cpbi.3
  • Wong, A., & Cortopassi, G. (1997). mtDNA mutations confer cellular sensitivity to oxidant stress that is partially rescued by calcium depletion and cyclosporin A. Biochemical and Biophysical Research Communications, 239(1), 139–145. https://doi.org/10.1006/bbrc.1997.7443
  • Wu, Y.-T., Lee, H.-C., Liao, C.-C., & Wei, Y.-H. (2013). Regulation of mitochondrial F(o)F(1)ATPase activity by Sirt3-catalyzed deacetylation and its deficiency in human cells harboring 4977bp deletion of mitochondrial DNA. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 1832(1), 216–227. https://doi.org/10.1016/j.bbadis.2012.10.002
  • Zenke, G., Strittmatter, U., Fuchs, S., Quesniaux, V. F., Brinkmann, V., Schuler, W., Zurini, M., Enz, A., Billich, A., Sanglier, J. J., & Fehr, T. (2001). Sanglifehrin A, a novel cyclophilin-binding compound showing immunosuppressive activity with a new mechanism of action. The Journal of Immunology, 166(12), 7165–7171. https://doi.org/10.4049/jimmunol.166.12.7165
  • Zoratti, M., & Szabò, I. (1995). The mitochondrial permeability transition. Biochimica et Biophysica Acta, 1241(2), 139–176. https://doi.org/10.1016/0304-4157(95)00003-a
  • Zhang, Z., Li, Y., Lin, B., Schroeder, M., & Huang, B. (2011). Identification of cavities on protein surface using multiple computational approaches for drug binding site prediction. Bioinformatics, 27(15), 2083–2088. https://doi.org/10.1093/bioinformatics/btr331

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.