Induction of the permeability transition pore in cells depleted of mitochondrial DNA

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 10, 2012, Pages 1860-1866

  Masgras, Ionica ^a   Rasola, Andrea ^a   Bernardi, Paolo ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

0 cell; Cyclophilin D; GSK3 ; Hexokinase; Mitochondrion; Permeability transition

Indexed keywords

CLOTRIMAZOLE; CYCLOPHILIN D; CYCLOSPORIN A; GLUCOSE; HEXOKINASE; INDIRUBIN; MITOCHONDRIAL DNA; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

CANCER CELL; CELL DEATH; CELL MEMBRANE DEPOLARIZATION; CELL SURFACE; CELL SURVIVAL; CONFERENCE PAPER; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

CELL LINE, TUMOR; CYCLOSPORINE; DNA, MITOCHONDRIAL; ENZYME ACTIVATION; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; HEXOKINASE; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIAL DISEASES; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3;

EID: 84864674352     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.02.022     Document Type: Conference Paper

References (56)

1. M.P. King, and G. Attardi Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation Science 246 1989 500 503
2. M.P. King, and G. Attardi Isolation of human cell lines lacking mitochondrial DNA Methods Enzymol. 264 1996 304 313
3. D. Pye, D.S. Kyriakouli, G.A. Taylor, R. Johnson, M. Elstner, B. Meunier, Z.M. Chrzanowska-Lightowlers, R.W. Taylor, D.M. Turnbull, and R.N. Lightowlers Production of transmitochondrial cybrids containing naturally occurring pathogenic mtDNA variants Nucleic Acids Res. 34 2006 e95
4. I.A. Trounce, and C.A. Pinkert Cybrid models of mtDNA disease and transmission, from cells to mice Curr. Top. Dev. Biol. 77 2007 157 183
5. M.D. Jacobson, J.F. Burne, M.P. King, T. Miyashita, J.C. Reed, and M.C. Raff Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA Nature 361 1993 365 369
6. P. Marchetti, S.A. Susin, D. Decaudin, S. Gamen, M. Castedo, T. Hirsch, N. Zamzami, J. Naval, A. Senik, and G. Kroemer Apoptosis-associated derangement of mitochondrial function in cells lacking mitochondrial DNA Cancer Res. 56 1996 2033 2038
7. L.R. Cavalli, M. Varella-Garcia, and B.C. Liang Diminished tumorigenic phenotype after depletion of mitochondrial DNA Cell Growth Differ. 8 1997 1189 1198
8. M. Higuchi, B.B. Aggarwal, and E.T. Yeh Activation of CPP32-like protease in tumor necrosis factor-induced apoptosis is dependent on mitochondrial function J. Clin. Invest. 99 1997 1751 1758
9. K. Buchet, and C. Godinot Functional F1-ATPase essential in maintaining growth and membrane potential of human mitochondrial DNA-depleted ρ° cells J. Biol. Chem. 273 1998 22983 22989
10. B.C. Liang, and E. Ullyatt Increased sensitivity to cis- diamminedichloroplatinum induced apoptosis with mitochondrial DNA depletion Cell Death Differ. 5 1998 694 701
11. R.D. Appleby, W.K. Porteous, G. Hughes, A.M. James, D. Shannon, Y.H. Wei, and M.P. Murphy Quantitation and origin of the mitochondrial membrane potential in human cells lacking mitochondrial DNA Eur. J. Biochem. 262 1999 108 116
12. S. Jiang, J. Cai, D.C. Wallace, and D.P. Jones Cytochrome c-mediated apoptosis in cells lacking mitochondrial DNA. Signaling pathway involving release and caspase 3 activation is conserved J. Biol. Chem. 274 1999 29905 29911
13. R. Dey, and C.T. Moraes Lack of oxidative phosphorylation and low mitochondrial membrane potential decrease susceptibility to apoptosis and do not modulate the protective effect of Bcl-x(L) in osteosarcoma cells J. Biol. Chem. 275 2000 7087 7094
14. J.Y. Kim, Y.H. Kim, I. Chang, S. Kim, Y.K. Pak, B.H. Oh, H. Yagita, Y.K. Jung, Y.J. Oh, and M.S. Lee Resistance of mitochondrial DNA-deficient cells to TRAIL: role of Bax in TRAIL-induced apoptosis Oncogene 21 2002 3139 3148
15. S.Y. Park, I. Chang, J.Y. Kim, S.W. Kang, S.H. Park, K. Singh, and M.S. Lee Resistance of mitochondrial DNA-depleted cells against cell death: role of mitochondrial superoxide dismutase J. Biol. Chem. 279 2004 7512 7520
16. G. Biswas, M. Guha, and N.G. Avadhani Mitochondria-to-nucleus stress signaling in mammalian cells: nature of nuclear gene targets, transcription regulation, and induced resistance to apoptosis Gene 354 2005 132 139
17. G. Biswas, H.K. Anandatheerthavarada, and N.G. Avadhani Mechanism of mitochondrial stress-induced resistance to apoptosis in mitochondrial DNA-depleted C2C12 myocytes Cell Death Differ. 12 2005 266 278
18. J.Q. Kwong, M.S. Henning, A.A. Starkov, and G. Manfredi The mitochondrial respiratory chain is a modulator of apoptosis J. Cell Biol. 179 2007 1163 1177
19. R.C. Taylor, S.P. Cullen, and S.J. Martin Apoptosis: controlled demolition at the cellular level Nat. Rev. Mol. Cell Biol. 9 2008 231 241
20. W.-X. Zong, and C.B. Thompson Necrotic death as a cell fate Genes Dev. 20 2006 1 15
21. 2 +-dependent apoptosis and necrosis Cell Calcium 50 2011 222 233
22. R.A. Altschuld, C.M. Hohl, L.C. Castillo, A.A. Garleb, R.C. Starling, and G.P. Brierley Cyclosporin inhibits mitochondrial calcium efflux in isolated adult rat ventricular cardiomyocytes Am. J. Physiol. 262 1992 H1699 H1704
23. P. Bernardi, and V. Petronilli The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal J. Bioenerg. Biomembr. 28 1996 131 138
24. 2 + exchange, metabolic flexibility, and propensity for heart failure in mice J. Clin. Invest. 120 2010 3680 3687
25. 2 + responses to physiological stimuli in adult neurons Eur. J. Neurosci. 33 2011 831 842
26. 2 + transport in mitochondria of Drosophila melanogaster J. Biol. Chem. 286 2011 41163 41170
27. P. Bernardi, V. Petronilli, F. Di Lisa, and M. Forte A mitochondrial perspective on cell death Trends Biochem. Sci. 26 2001 112 117
28. A. Rasola, and P. Bernardi The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis Apoptosis 12 2007 815 833
29. A. Rasola, M. Sciacovelli, B. Pantic, and P. Bernardi Signal transduction to the permeability transition pore FEBS Lett. 584 2010 1989 1996
30. V. Giorgio, E. Bisetto, M.E. Soriano, F. Dabbeni-Sala, E. Basso, V. Petronilli, M.A. Forte, P. Bernardi, and G. Lippe Cyclophilin D modulates mitochondrial F0F1-ATP synthase by interacting with the lateral stalk of the complex J. Biol. Chem. 284 2009 33982 33988
31. A.M. Porcelli, A. Angelin, A. Ghelli, E. Mariani, A. Martinuzzi, V. Carelli, V. Petronilli, P. Bernardi, and M. Rugolo Respiratory complex I dysfunction due to mitochondrial DNA mutations shifts the voltage threshold for opening of the permeability transition pore toward resting levels J. Biol. Chem. 284 2009 2045 2052
32. D.R. Johns, M.J. Neufeld, and R.D. Park An ND-6 mitochondrial DNA mutation associated with Leber hereditary optic neuropathy Biochem. Biophys. Res. Commun. 187 1992 1551 1557
33. S.I. Zhadanov, V.V. Atamanov, N.I. Zhadanov, O.V. Oleinikov, L.P. Osipova, and T.G. Schurr A novel mtDNA ND6 gene mutation associated with LHON in a Caucasian family Biochem. Biophys. Res. Commun. 332 2005 1115 1121
34. A. Zielke, S. Tezelman, G.H. Jossart, M. Wong, A.E. Siperstein, Q.Y. Duh, and O.H. Clark Establishment of a highly differentiated thyroid cancer cell line of Hurthle cell origin Thyroid 8 1998 475 483
35. E. Bonora, A.M. Porcelli, G. Gasparre, A. Biondi, A. Ghelli, V. Carelli, A. Baracca, G. Tallini, A. Martinuzzi, G. Lenaz, M. Rugolo, and G. Romeo Defective oxidative phosphorylation in thyroid oncocytic carcinoma is associated with pathogenic mitochondrial DNA mutations affecting complexes I and III Cancer Res. 66 2006 6087 6096
36. O. Warburg On the origin of cancer cells Science 123 1956 309 314
37. P.P. Hsu, and D.M. Sabatini Cancer cell metabolism: Warburg and beyond Cell 134 2008 703 707
38. C. Frezza, and E. Gottlieb Mitochondria in cancer: not just innocent bystanders Semin. Cancer Biol. 19 2009 4 11
39. M. Brandon, P. Baldi, and D.C. Wallace Mitochondrial mutations in cancer Oncogene 25 2006 4647 4662
40. P.H. Yin, H.C. Lee, G.Y. Chau, Y.T. Wu, S.H. Li, W.Y. Lui, Y.H. Wei, T.Y. Liu, and C.W. Chi Alteration of the copy number and deletion of mitochondrial DNA in human hepatocellular carcinoma Br. J. Cancer 90 2004 2390 2396
41. Y. Wang, V.W. Liu, W.C. Xue, A.N. Cheung, and H.Y. Ngan Association of decreased mitochondrial DNA content with ovarian cancer progression Br. J. Cancer 95 2006 1087 1091
42. M. Yu, Y. Zhou, Y. Shi, L. Ning, Y. Yang, X. Wei, N. Zhang, X. Hao, and R. Niu Reduced mitochondrial DNA copy number is correlated with tumor progression and prognosis in Chinese breast cancer patients IUBMB Life 59 2007 450 457
43. R.L. Correia, S.M. Oba-Shinjo, M. Uno, N. Huang, and S.K. Marie Mitochondrial DNA depletion and its correlation with TFAM, TFB1M, TFB2M and POLG in human diffusely infiltrating astrocytomas Mitochondrion 11 2011 48 53
44. H. Cheon, H.E. Moon, M.S. Lee, and S.S. Kim Loss of mitochondrial DNA enhances angiogenic and invasive potential of hepatoma cells Oncol. Rep. 23 2010 779 786
45. K.K. Singh, V. Ayyasamy, K.M. Owens, M.S. Koul, and M. Vujcic Mutations in mitochondrial DNA polymerase-gamma promote breast tumorigenesis J. Hum. Genet. 54 2009 516 524
46. A. Naito, J. Carcel-Trullols, C.H. Xie, T.T. Evans, T. Mizumachi, and M. Higuchi Induction of acquired resistance to antiestrogen by reversible mitochondrial DNA depletion in breast cancer cell line Int. J. Cancer 122 2008 1506 1511
47. F. Chiara, D. Castellaro, O. Marin, V. Petronilli, W.S. Brusilow, M. Juhaszova, S.J. Sollott, M. Forte, P. Bernardi, and A. Rasola Hexokinase II detachment from mitochondria triggers apoptosis through the permeability transition pore independent of voltage-dependent anion channels PLoS One 3 2008 e1852
48. A. Rasola, M. Sciacovelli, F. Chiara, B. Pantic, W.S. Brusilow, and P. Bernardi Activation of mitochondrial ERK protects cancer cells from death through inhibition of the permeability transition Proc. Natl. Acad. Sci. U. S. A. 107 2010 726 731
49. J. Traba, A. del Arco, M.R. Duchen, G. Szabadkai, and J. Satrustegui SCaMC-1 promotes cancer cell survival by desensitizing mitochondrial permeability transition via ATP/ADP-mediated matrix Ca2+ buffering Cell Death Differ. 19 2012 650 660
50. P. Bernardi, L. Scorrano, R. Colonna, V. Petronilli, and F. Di Lisa Mitochondria and cell death. Mechanistic aspects and methodological issues Eur. J. Biochem. 264 1999 687 701
51. A. Nicolli, E. Basso, V. Petronilli, R.M. Wenger, and P. Bernardi Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, a cyclosporin A-sensitive channel J. Biol. Chem. 271 1996 2185 2192
52. D.G. Nicholls, and M.W. Ward Mitochondrial membrane potential and neuronal glutamate excitotoxicity: mortality and millivolts Trends Neurosci. 23 2000 166 174
53. S.P. Mathupala, Y.H. Ko, and P.L. Pedersen Hexokinase II: cancer's double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria Oncogene 25 2006 4777 4786
54. P. Bernardi, A. Krauskopf, E. Basso, V. Petronilli, E. Blachly-Dyson, F. Di Lisa, and M.A. Forte The mitochondrial permeability transition from in vitro artifact to disease target FEBS J. 273 2006 2077 2099
55. P. Bernardi Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization J. Biol. Chem. 267 1992 8834 8839
56. J.G. Pastorino, N. Shulga, and J.B. Hoek Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis J. Biol. Chem. 277 2002 7610 7618