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The Mitochondrial Phosphate Carrier Interacts with Cyclophilin D and May Play a Key Role in the Permeability Transition
Open accessAbstract
The mitochondrial permeability transition pore (MPTP) plays a key role in cell death, yet its molecular identity remains uncertain. Although knock-out studies have confirmed critical roles for both cyclophilin-D (CyP-D) and the adenine nucleotide translocase (ANT), given a strong enough stimulus MPTP opening can occur in the absence of either. Here we provide evidence that the mitochondrial phosphate carrier (PiC) may also be a critical component of the MPTP. Phenylarsine oxide (PAO) was found to activate MPTP opening in the presence of carboxyatractyloside (CAT) that prevents ANT binding to immobilized PAO. Only four proteins from solubilized CAT-treated beef heart inner mitochondrial membranes bound to immobilized PAO, one of which was the PiC. GST-CyP-D pull-down and co-immunoprecipitation studies revealed CsA-sensitive binding of PiC to CyP-D; this increased following diamide treatment. Co-immunoprecipitation of the ANT with the PiC was also observed but was insensitive to CsA treatment. N-ethylmaleimide and ubiquinone analogues (UQ(0) and Ro 68-3400) inhibited phosphate transport into rat liver mitochondria with the same concentration dependence as their inhibition of MPTP opening. UQ(0) and Ro 68-3400 also induced the "m" conformation of the ANT, as does NEM, and reduced the binding of both the PiC and ANT to the PAO column. We propose a model for the MPTP in which a calcium-triggered conformational change of the PiC, facilitated by CyP-D, induces pore opening. An interaction of the PiC with the ANT may enable agents that bind to either transporter to modulate pore opening.
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Cites
Mitochondrial membrane permeabilization in cell death
Kroemer, G., Galluzzi, L., & Brenner, C. (2007) · Physiological Reviews · doi:10.1152/physrev.00013.2006 · Cited by 3,598
The mitochondrial permeability transition pore and its role in cell death
CROMPTON, M. (1999) · Biochemical Journal · doi:10.1042/bj3410233 · Cited by 2,432
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., et al. (2005) · Nature · doi:10.1038/nature03434 · Cited by 2,280
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Self-citationNakagawa, T., Shimizu, S., Watanabe, T., Yamaguchi, O., Otsu, K., Yamagata, H., Inohara, H., Kubo, T., & Tsujimoto, Y. (2005) · Nature · doi:10.1038/nature03317 · Cited by 1,635
The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore
Kokoszka, J. E., Waymire, K. G., Levy, S. E., Sligh, J. E., Cai, J., Jones, D. P., MacGregor, G. R., & Wallace, D. C. (2004) · Nature · doi:10.1038/nature02229 · Cited by 1,086
Properties of the Permeability Transition Pore in Mitochondria Devoid of Cyclophilin D
Basso, E., Fante, L., Fowlkes, J., Petronilli, V., Forte, M. A., & Bernardi, P. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.c500089200 · Cited by 808
The permeability transition pore complex: another view
Halestrap, A. P., McStay, G. P., & Clarke, S. J. (2002) · Biochimie · doi:10.1016/s0300-9084(02)01375-5 · Cited by 709
Self-citationMcSTAY, G. P., CLARKE, S. J., & HALESTRAP, A. P. (2002) · Biochemical Journal · doi:10.1042/bj20011672 · Cited by 367
Self-citationProteomic analysis of the mouse liver mitochondrial inner membrane
Da Cruz, S., Xenarios, I., Langridge, J., Vilbois, F., Parone, P. A., & Martinou, J.-C. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304940200 · Cited by 247
Cited by
What is the mitochondrial permeability transition pore?
Halestrap, A. P. (2009) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2009.02.021 · Cited by 933
Self-citationMolecular mechanisms and consequences of mitochondrial permeability transition
Bonora, M., Giorgi, C., & Pinton, P. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00433-y · Cited by 538
Role of the c subunit of the F O ATP synthase in mitochondrial permeability transition
Bonora, M., Bononi, A., De Marchi, E., Giorgi, C., Lebiedzinska, M., Marchi, S., Patergnani, S., Rimessi, A., Suski, J. M., Wojtala, A., et al. (2013) · Cell Cycle · doi:10.4161/cc.23599 · Cited by 458
Mitochondria and Reactive Oxygen Species in Aging and Age-Related Diseases
(2018) · International Review of Cell and Molecular Biology · doi:10.1016/bs.ircmb.2018.05.006 · Cited by 455
Mitochondrial calcium exchange in physiology and disease
Garbincius, J. F., & Elrod, J. W. (2022) · Physiological Reviews · doi:10.1152/physrev.00041.2020 · Cited by 412
Metadata
- Authors
- Leung, A. W. C., Varanyuwatana, P., & Halestrap, A. P.
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2008-09
- Volume
- 283
- Issue
- 39
- Pages
- 26312-26323
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2081358044
- Cited by
- 314
- References
- 10
- FWCI
- 11.29
- Type
- journal article
- Language
- en
- Open access
- hybrid
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- Leung, A. W. C., Varanyuwatana, P., & Halestrap, A. P. (2008). The Mitochondrial Phosphate Carrier Interacts with Cyclophilin D and May Play a Key Role in the Permeability Transition. Journal of Biological Chemistry. https://doi.org/10.1074/jbc.m805235200
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