Intramitochondrial signaling: interactions among mitoKATP, PKCε, ROS, and MPT
Open accessAbstract
Activation of protein kinase Cε (PKCε), opening of mitochondrial ATP-sensitive K+channels (mitoK ATP), and increased mitochondrial reactive oxygen species (ROS) are key events in the signaling that underlies cardioprotection. We showed previously that mitoK ATP is opened by activation of a mitochondrial PKCε, designated PKCε1, that is closely associated with mitoK ATP. mitoK ATP opening then causes an increase in ROS production by complex I of the respiratory chain. This ROS activates a second pool of PKCε, designated PKCε2, which inhibits the mitochondrial permeability transition (MPT). In the present study, we measured mitoK ATP-dependent changes in mitochondrial matrix volume to further investigate the relationships among PKCε, mitoK ATP, ROS, and MPT. We present evidence that 1) mitoK ATP can be opened by H 2 O 2 and nitric oxide (NO) and that these effects are mediated by PKCε1 and not by direct actions on mitoK ATP, 2) superoxide has no effect on mitoK ATP opening, 3) exogenous H 2 O 2 or NO also inhibits MPT opening, and both compounds do so independently of mitoK ATP activity via activation of PKCε2, 4) mitoK ATP opening induced by PKG, phorbol ester, or diazoxide is not mediated by ROS, and 5) mitoK ATP-generated ROS activates PKCε1 and induces phosphorylation-dependent mitoK ATP opening in vitro and in vivo. Thus mitoK ATP-dependent mitoK ATP opening constitutes a positive feedback loop capable of maintaining the channel open after the stimulus is no longer present. This feedback pathway may be responsible for the lasting protective effect of preconditioning, colloquially known as the memory effect.
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Activation of NOX via angiotensin II and the angiotensin II type 1 receptor is mediated by PKC; PKCε is also an activator of the KATP channel, which stimulates mitochondrial ROS production.
“Of note, the activation of NOX via angiotensin II and the angiotensin II type 1 receptor is mediated by PKC; however, the isoform PKCε is also an activator of the KATP channel, which, as indicated, also stimulates mitochondrial ROS production (FIGURE 17) (187, 242).”
From Sources of Vascular Nitric Oxide and Reactive Oxygen Species and Their Regulation (2019) · cites this paper as [187]
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- Authors
- Costa, A. D. T., & Garlid, K. D.
- Affiliations
- Portland State University (US)
- Venue
- American Journal of Physiology-Heart and Circulatory Physiology
- Publisher
- American Physiological Society
- Published
- 2008-08
- Volume
- 295
- Issue
- 2
- Pages
- H874-H882
- ISSN
- 0363-6135 (ISSN-L)
- 1522-1539
- PMC
- PMC2519212
- OpenAlex
- W2010516222
- Cited by
- 238
- References
- 66
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 8 · 2023: 6 · 2022: 4 · 2021: 6 · 2020: 9 · 2019: 8 · 2018: 11 · 2017: 9 · 2016: 12 · 2015: 14 · 2014: 29 · 2013: 22 · 2012: 14
- FWCI
- 10.71
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- American Journal of Physiology-Heart and Circulatory Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Max-Planck-Gesellschaft
- National Heart, Lung, and Blood Institute (HL35673, HL067842, R01HL067842)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Pathology and Forensic Medicine › Cardiac Ischemia and Reperfusion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- mitochondrial ATP-sensitive potassium channel, protein kinase C epsilon, mitochondrial reactive oxygen species, mitochondrial permeability transition, cardioprotection, preconditioning, positive feedback loop, hydrogen peroxide, nitric oxide, superoxide, complex I, cGMP-dependent protein kinase, diazoxide, phorbol ester
- MeSH terms
- Glycogen Synthase Kinase 3 beta, Mitochondrial Permeability Transition Pore, Animals, Diazoxide, Enzyme Activation, Hydrogen Peroxide, Male, Mitochondria, Heart, Nitric Oxide, Phosphorylation, Superoxides, Tetradecanoylphorbol Acetate, Time Factors, Potassium Channels, Signal Transduction, Ion Channel Gating, Rats, Sprague-Dawley, Reactive Oxygen Species, Cyclic GMP-Dependent Protein Kinases, Feedback, Physiological, Mitochondrial Membrane Transport Proteins, Glycogen Synthase Kinase 3, Mitochondrial Membranes, Rats, Protein Kinase C-epsilon, Mitochondrial Size, In Vitro Techniques
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