Resistance of dynamin-related protein 1 oligomers to disassembly impairs mitophagy, resulting in myocardial inflammation and heart failure
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Chunyan Liao's and Grazia M. Cereghetti's names were misspelled. The names have been corrected as shown above.
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Mitophagy impairment can induce cardiomyocyte death and HF.
“Accumulating evidence suggests that mitophagy impairment can induce cardiomyocyte death and HF [206,207,208,209].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [207]
Cites
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“After activation, Drp1 translocates from a cytosolic pool to the outer mitochondrial membrane, where it oligomerizes, hydrolyzes GTP, and constricts to divide mitochondria (4).”
BackgroundFission and selective fusion govern mitochondrial segregation and elimination by autophagy
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“Because dysfunction of mitochondrial fission-fusion proteins has been linked to reduced OXPHOS capacity, we hypothesized that energy deficiency resulting from impaired OXPHOS contributes to DCM in Python (20, 21).”
BackgroundMitofusin 2 tethers endoplasmic reticulum to mitochondria
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“MEFs are well established as a cellular model to probe the interaction of mitochondrial fission-fusion dynamics and calcium signaling (27).”
BackgroundSelf-citationThe Failing Heart — An Engine Out of Fuel
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“In this setting, activation of macroautophagy by exposure to a low-protein diet partially protects against DCM.”
BackgroundInfluentialDuring autophagy mitochondria elongate, are spared from degradation and sustain cell viability
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“In Drp1 / MEFs, there is reduced autophagic clearance of mitochondria under starvation conditions, suggestive of impaired mitophagy (8).”
BackgroundSelf-citationProteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin
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“As a corollary, Drp1 contributes to Parkin-induced mitophagy in MEFs (6).”
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“In the heart, free mitochondrial DNA because of loss of DNase II has been shown to activate TLR9, resulting in heart failure in mice (9).”
BackgroundDephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria
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“Where indicated, MEFs were transfected and imaged by confocal microscopy as described previously (13).”
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“Drp1 / MEFs (14) were originally a gift from Prof.”
BackgroundInhibiting Mitochondrial Fission Protects the Heart Against Ischemia/Reperfusion Injury
Ong, S.-B., Subrayan, S., Lim, S. Y., Yellon, D. M., Davidson, S. M., & Hausenloy, D. J. (2010) · Circulation · doi:10.1161/circulationaha.109.906610 · Cited by 986 · cited 1× · see citing works
“Therapeutic intervention on the cardiac Drp1 pathway has so far focused on inhibition of fission in acute ischemia-reperfusion, but low-level chronic activation to promote mitophagy and high ATP synthesis might be of benefit in the failing heart (42, 43).”
BackgroundA Lethal Defect of Mitochondrial and Peroxisomal Fission
Waterham, H. R., Koster, J., van Roermund, C. W. T., Mooyer, P. A. W., Wanders, R. J. A., & Leonard, J. V. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa064436 · Cited by 749 · cited 3× · see citing works
“Mitochondria in Drp1 C452F MEFs Are Morphologically and Functionally Abnormal—Assessment of mitochondrial fissionfusion in the heart is challenging, possibly because of relative low event frequency or constraints on mitochondrial morphology imposed by the “sardine tin” architecture of the cardiomyocyte (11, 18, 19).”
BackgroundEndogenous Drp1 Mediates Mitochondrial Autophagy and Protects the Heart Against Energy Stress
Ikeda, Y., Shirakabe, A., Maejima, Y., Zhai, P., Sciarretta, S., Toli, J., Nomura, M., Mihara, K., Egashira, K., Ohishi, M., et al. (2015) · Circulation Research · doi:10.1161/circresaha.116.303356 · Cited by 571 · cited 3× · see citing works
“(36) have found that inducible down-regulation of Drp1 leads to reduced mitophagy with accumulation of damaged mitochondria.”
BackgroundGrumati, P., Coletto, L., Sabatelli, P., Cescon, M., Angelin, A., Bertaggia, E., Blaauw, B., Urciuolo, A., Tiepolo, T., Merlini, L., et al. (2010) · Nature Medicine · doi:10.1038/nm.2247 · Cited by 540 · cited 1× · see citing works
“Activation of autophagy by low protein diet (LPD) has been shown previously to be beneficial in a model of congenital muscular dystrophy caused by abnormal autophagy, leading to improved myofiber survival (33).”
BackgroundBidirectional Ca <sup>2+</sup> -dependent control of mitochondrial dynamics by the Miro GTPase
Saotome, M., Safiulina, D., Szabadkai, G., Das, S., Fransson, Å., Aspenstrom, P., Rizzuto, R., & Hajnóczky, G. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808953105 · Cited by 538 · see citing works
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“(37) was necrotic cell death by activation of the mitochondrial permeability transition pore.”
BackgroundSelf-citationNew insights into the function and regulation of mitochondrial fission
Otera, H., Ishihara, N., & Mihara, K. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.02.002 · Cited by 476 · cited 1× · see citing works
“Mitochondrial remodeling has multiple roles, including quality control and clearance of mitochondria by mitophagy, segregation of mitochondrial DNA and proteins, and apoptosis (5).”
BackgroundThe role of mitochondria in NLRP3 inflammasome activation
Liu, Q., Zhang, D., Hu, D., Zhou, X., & Zhou, Y. (2018) · Molecular Immunology · doi:10.1016/j.molimm.2018.09.010 · Cited by 475 · cited 1× · see citing works
“For example, mitochondrial elongation under conditions of nutrient deprivation protects against mitophagic degradation and preserves ATP synthesis (7, 8) Failure of cellular control over mitochondria triggers inflammation by Toll-like receptors or the inflammasome, leading to heart failure (9, 10).”
BackgroundSzabadkai, G., Simoni, A. M., Chami, M., Wieckowski, M. R., Youle, R. J., & Rizzuto, R. (2004) · Molecular Cell · doi:10.1016/j.molcel.2004.09.026 · Cited by 468 · see citing works
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“To further study the connectivity of the mitochondrial network, we transfected Drp1 C452F MEFs with a mito-PAGFP construct as described previously (15).”
MethodParkin‐independent mitophagy requires Drp1 and maintains the integrity of mammalian heart and brain
Kageyama, Y., Hoshijima, M., Seo, K., Bedja, D., Sysa‐Shah, P., Andrabi, S. A., Chen, W., Höke, A., Dawson, V. L., Dawson, T. M., et al. (2014) · The EMBO Journal · doi:10.15252/embj.201488658 · Cited by 420 · cited 2× · see citing works
“Drp1 C452F leads to profound ATP deficiency in MEFs and the Python heart, supporting a wider body of work linking Drp1 with respiratory failure in both cell models and in the heart (36, 38, 41).”
BackgroundParone, P. A., Da Cruz, S., Tondera, D., Mattenberger, Y., James, D. I., Maechler, P., Barja, F., & Martinou, J.-C. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003257 · Cited by 415 · cited 1× · see citing works
“Drp1 C452F leads to profound ATP deficiency in MEFs and the Python heart, supporting a wider body of work linking Drp1 with respiratory failure in both cell models and in the heart (36, 38, 41).”
BackgroundLing, Y. M., Shaw, M. H., Ayala, C. A., Coppens, I., Taylor, G. A., Ferguson, D. J. P., & Yap, G. S. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20061318 · Cited by 350 · cited 1× · see citing works
“Transmission Electron Microscopy—Tissue for electron microscopy was processed as described previously (17).”
MethodSelf-citationZanna, C., Ghelli, A. M., Porcelli, A. M., Karbowski, M., Youle, R. J., Schimpf, S., Wissinger, B., Pinti, M., Cossarizza, A., Vidoni, S., et al. (2007) · Brain · doi:10.1093/brain/awm335 · Cited by 334 · cited 1× · see citing works
“Because dysfunction of mitochondrial fission-fusion proteins has been linked to reduced OXPHOS capacity, we hypothesized that energy deficiency resulting from impaired OXPHOS contributes to DCM in Python (20, 21).”
BackgroundDisatnik, M., Ferreira, J. C. B., Campos, J. C., Gomes, M. K., Dourado, P. M. M., Qi, X., & Mochly‐Rosen, D. (2013) · Journal of the American Heart Association · doi:10.1161/jaha.113.000461 · Cited by 333 · cited 1× · see citing works
“Therapeutic intervention on the cardiac Drp1 pathway has so far focused on inhibition of fission in acute ischemia-reperfusion, but low-level chronic activation to promote mitophagy and high ATP synthesis might be of benefit in the failing heart (42, 43).”
BackgroundFumarate Is Cardioprotective via Activation of the Nrf2 Antioxidant Pathway
Ashrafian, H., Czibik, G., Bellahcene, M., Aksentijević, D., Smith, A. C., Mitchell, S. J., Dodd, M. S., Kirwan, J., Byrne, J. J., Ludwig, C., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.017 · Cited by 303 · cited 1× · see citing works
“Transthoracic Echocardiography—Mouse echocardiography was performed as described previously (16).”
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“Biochemically, the mutant A395D protein has been found to be defective for self-assembly and GTP hydrolysis (12).”
BackgroundMethodSelf-citationGenetic Cardiomyopathies Causing Heart Failure
Cahill, T. J., Ashrafian, H., & Watkins, H. C. (2013) · Circulation Research · doi:10.1161/circresaha.113.300282 · Cited by 180 · cited 1× · see citing works
“Its etiology is diverse, including ischemia, inflammation, and genetic disease (1).”
BackgroundSelf-citationMitochondrial dynamics in heart disease
Dorn, G. W. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.03.008 · Cited by 159 · cited 1× · see citing works
“Mitochondria in Drp1 C452F MEFs Are Morphologically and Functionally Abnormal—Assessment of mitochondrial fissionfusion in the heart is challenging, possibly because of relative low event frequency or constraints on mitochondrial morphology imposed by the “sardine tin” architecture of the cardiomyocyte (11, 18, 19).”
BackgroundA Mutation in the Mitochondrial Fission Gene Dnm1l Leads to Cardiomyopathy
Ashrafian, H., Docherty, L., Leo, V., Towlson, C., Neilan, M., Steeples, V., Lygate, C. A., Hough, T., Townsend, S., Williams, D. J., et al. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001000 · Cited by 140 · cited 5× · see citing works
“Animal Studies—Drp1 C452F mice (Python) have been described previously (3).”
BackgroundInfluentialSelf-citationRegulation of mitochondrial fission by intracellular Ca2+ in rat ventricular myocytes
Hom, J., Yu, T., Yoon, Y., Porter, G. A., Jr., & Sheu, S. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.03.018 · Cited by 128 · see citing works
Controlling metabolism and cell death: At the heart of mitochondrial calcium signalling
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“Mitochondria in Drp1 C452F MEFs Are Morphologically and Functionally Abnormal—Assessment of mitochondrial fissionfusion in the heart is challenging, possibly because of relative low event frequency or constraints on mitochondrial morphology imposed by the “sardine tin” architecture of the cardiomyocyte (11, 18, 19).”
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“In summary, these data show that Drp1 C452F is associated with significantly reduced mitochondrial calcium uptake, a critical regulator of energy supply and demand matching in the heart (28).”
BackgroundDynamin 2 Mutants Linked to Centronuclear Myopathies Form Abnormally Stable Polymers*
Wang, L., Baryłko, B., Byers, C., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.c110.130013 · Cited by 77 · cited 1× · see citing works
“Although this is a novel finding for Drp1, there is a precedent for the similar influence of middle-domain mutations in the closely related human dynamin 2 gene, where disassembly mutants have preserved GTPase function but are functionally deficient, leading to congenital myopathy (34, 35).”
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“cium by inhibition of SERCA2, reducing mitochondrial calcium uptake and ATP synthesis (40).”
BackgroundMitochondria: sensors and mediators of innate immune receptor signaling
Cloonan, S. M., & Choi, A. M. K. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.05.005 · Cited by 65 · cited 1× · see citing works
“In the Python heart, we found evidence of activated innate immune signaling, consistent with recent work demonstrating that a failure of cellular control of mitochondria can result in the activation of the inflammasome, Toll-like receptors, stimulator of interferon genes (STING) and mitochondrial antiviral signaling p…”
BackgroundRedpath, C. J., Khalil, M. B., Drozdzal, G., Radisic, M., & McBride, H. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069165 · Cited by 42 · see citing works
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“Although this is a novel finding for Drp1, there is a precedent for the similar influence of middle-domain mutations in the closely related human dynamin 2 gene, where disassembly mutants have preserved GTPase function but are functionally deficient, leading to congenital myopathy (34, 35).”
BackgroundDorn, G. W. (2015) · Circulation Research · doi:10.1161/circresaha.114.305672 · Cited by 22 · see citing works
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- Authors
- Cahill, T. J., Leo, V., Kelly, M., Stockenhuber, A., Kennedy, N. W., Bao, L., Cereghetti, G. M., Harper, A. R., Czibik, G., Liao, C., Bellahcene, M., Steeples, V., Ghaffari, S., Yavari, A., Mayer, A., Poulton, J., Ferguson, D. J. P., Scorrano, L., Hettiarachchi, N. T., Peers, C., Boyle, J., Hill, R. B., Simmons, A., Watkins, H., Dear, T. N., & Ashrafian, H.
- ORCID
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2016-12
- Volume
- 291
- Issue
- 49
- Pages
- 25762
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2801215883
- Cited by
- 14
- References
- 42
- Citations by year
- 2024: 1 · 2023: 1 · 2022: 1 · 2021: 2 · 2020: 4 · 2019: 2 · 2018: 2 · 2017: 1
- FWCI
- 1.56
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Funders
- National Institute for Health and Care Research (NIHR-RP-R3-12-026)
- British Heart Foundation (RG/07/012/24110)
- Medical Research Council (MR/J010448/1)
- National Institute of General Medical Sciences (R01GM067180)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Keywords
- Drp1, mitochondrial fission, mitophagy, mitochondrial quality control, myocarditis, heart failure, mitochondrial dysfunction
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