In mammalian skeletal muscle, phosphorylation of TOMM22 by protein kinase CSNK2/CK2 controls mitophagy
Open accessAbstract
In yeast, Tom22, the central component of the TOMM (translocase of outer mitochondrial membrane) receptor complex, is responsible for the recognition and translocation of synthesized mitochondrial precursor proteins, and its protein kinase CK2-dependent phosphorylation is mandatory for TOMM complex biogenesis and proper mitochondrial protein import. In mammals, the biological function of protein kinase CSNK2/CK2 remains vastly elusive and it is unknown whether CSNK2-dependent phosphorylation of TOMM protein subunits has a similar role as that in yeast. To address this issue, we used a skeletal muscle-specific Csnk2b/Ck2β-conditional knockout (cKO) mouse model. Phenotypically, these skeletal muscle Csnk2b cKO mice showed reduced muscle strength and abnormal metabolic activity of mainly oxidative muscle fibers, which point towards mitochondrial dysfunction. Enzymatically, active muscle lysates from skeletal muscle Csnk2b cKO mice phosphorylate murine TOMM22, the mammalian ortholog of yeast Tom22, to a lower extent than lysates prepared from controls. Mechanistically, CSNK2-mediated phosphorylation of TOMM22 changes its binding affinity for mitochondrial precursor proteins. However, in contrast to yeast, mitochondrial protein import seems not to be affected in vitro using mitochondria isolated from muscles of skeletal muscle Csnk2b cKO mice. PINK1, a mitochondrial health sensor that undergoes constitutive import under physiological conditions, accumulates within skeletal muscle Csnk2b cKO fibers and labels abnormal mitochondria for removal by mitophagy as demonstrated by the appearance of mitochondria-containing autophagosomes through electron microscopy. Mitophagy can be normalized by either introduction of a phosphomimetic TOMM22 mutant in cultured myotubes, or by in vivo electroporation of phosphomimetic Tomm22 into muscles of mice. Importantly, transfection of the phosphomimetic Tomm22 mutant in muscle cells with ablated Csnk2b restored their oxygen consumption rate comparable to wild-type levels. In sum, our data show that mammalian CSNK2-dependent phosphorylation of TOMM22 is a critical switch for mitophagy and reveal CSNK2-dependent physiological implications on metabolism, muscle integrity and behavior.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Absence of CK2 prevents import of PINK1 inside mitochondrial intermembrane space via TOM22 resulting in PINK1 accumulation, which triggers Parkin recruitment and mitophagy.
“while the absence of casein kinase 2 (CK2) prevents the import of PINK1 inside the mitochondrial intermembrane space via TOM22 resulting in PINK1 accumulation, which triggers Parkin recruitment and mitophagy.”
From Mechanisms of muscle atrophy and hypertrophy: implications in health and disease (2021) · cites this paper as [83]
Autophagy flux is impaired in CK2 knockout leading to formation of p62-positive protein aggregates and myopathy.
“However, autophagy flux is impaired in CK2 knockout leading to the formation of p62-positive protein aggregates and myopathy83.”
From Mechanisms of muscle atrophy and hypertrophy: implications in health and disease (2021) · cites this paper as [83]
Skeletal muscle-specific casein kinase 2 (CK2) deletion leads to a block of the autophagy and mitophagy flux that results in myopathy and muscle weakness.
“Accordingly, skeletal muscle-specific casein kinase 2 (CK2) deletion leads to a block of the autophagy and mitophagy flux that results in myopathy and muscle weakness [229].”
From The connection between the dynamic remodeling of the mitochondrial network and the regulation of muscle mass (2021) · cites this paper as [229]
There is an increase in autophagosome formation on mitochondria that cannot fuse with the lysosome, resulting in mitophagy impairment and mitochondrial dysfunction over time.
“Consequently, there is an increase in autophagosome formation on mitochondria, that however, cannot fuse with the lysosome resulting in mitophagy impairment and mitochondrial dysfunction during the time [229].”
From The connection between the dynamic remodeling of the mitochondrial network and the regulation of muscle mass (2021) · cites this paper as [229]
Reduced CK2-mediated TOMM22 phosphorylation weakens the binding between PINK1 and TOMM22, leading to decreased IMM PINK1 import and further OMM PINK1 accumulation.
“The reduced CK2-mediated TOMM22 phosphorylation weakens the binding between PINK1 and TOMM22, leading to decreased IMM PINK1 import and further OMM PINK1 accumulation.”
From The connection between the dynamic remodeling of the mitochondrial network and the regulation of muscle mass (2021) · cites this paper as [229]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Repertoires of Autophagy in the Pathogenesis of Ocular Diseases
Li, Y., Jiang, Q. L., Cao, G.-F., Yao, J., & Yan, B. (2015) · Cellular Physiology and Biochemistry · doi:10.1159/000373980 · Cited by 16,351 · see citing works
Autophagy in the Pathogenesis of Disease
Levine, B., & Kroemer, G. (2008) · Cell · doi:10.1016/j.cell.2007.12.018 · Cited by 7,069 · see citing works
LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing.
Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., & Yoshimori, T. (2000) · The EMBO Journal · doi:10.1093/emboj/19.21.5720 · Cited by 6,605 · see citing works
Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism
Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., & Shimizu, N. (1998) · Nature · doi:10.1038/33416 · Cited by 5,227 · see citing works
Cui, C., Cui, J., Jin, F., Cui, Y., Li, R., Jiang, X., Tian, Y., Wang, R. C., Jiang, P., & Gao, J. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479571 · Cited by 5,214 · see citing works
Methods in Mammalian Autophagy Research
Mizushima, N., Yoshimori, T., & Levine, B. (2010) · Cell · doi:10.1016/j.cell.2010.01.028 · Cited by 4,497 · see citing works
Autophagy and Viruses: Adversaries or Allies?
Dong, X., & Levine, B. (2013) · Journal of Innate Immunity · doi:10.1159/000346388 · Cited by 4,441 · see citing works
Epidemiology of Parkinson's disease
de Lau, L. M., & Breteler, M. M. (2006) · The Lancet Neurology · doi:10.1016/s1474-4422(06)70471-9 · Cited by 4,110 · see citing works
Mitochondrial Fission, Fusion, and Stress
Youle, R. J., & van der Bliek, A. M. (2012) · Science · doi:10.1126/science.1219855 · Cited by 3,674 · see citing works
Hereditary Early-Onset Parkinson's Disease Caused by Mutations in <i>PINK1</i>
Valente, E. M., Abou-Sleiman, P. M., Caputo, V., Muqit, M. M. K., Harvey, K., Gispert, S., Ali, Z., Del Turco, D., Bentivoglio, A. R., Healy, D. G., et al. (2004) · Science · doi:10.1126/science.1096284 · Cited by 3,481 · see citing works
Mitochondria: In Sickness and in Health
Nunnari, J., & Suomalainen, A. (2012) · Cell · doi:10.1016/j.cell.2012.02.035 · Cited by 3,479 · see citing works
Induction of autophagy and inhibition of tumorigenesis by beclin 1
Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., & Levine, B. (1999) · Nature · doi:10.1038/45257 · Cited by 3,347 · see citing works
Youle, R. J., & Narendra, D. P. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3028 · Cited by 3,273 · see citing works
PINK1 Is Selectively Stabilized on Impaired Mitochondria to Activate Parkin
Narendra, D. P., Jin, S. M., Tanaka, A., Suen, D.-F., Gautier, C. A., Shen, J., Cookson, M. R., & Youle, R. J. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000298 · Cited by 2,944 · see citing works
PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1
Geisler, S., Holmström, K. M., Skujat, D., Fiesel, F. C., Rothfuss, O. C., Kahle, P. J., & Springer, W. (2010) · Nature Cell Biology · doi:10.1038/ncb2012 · Cited by 2,835 · see citing works
Matsuda, N., Sato, S., Shiba, K., Okatsu, K., Saisho, K., Gautier, C. A., Sou, Y.-S., Saiki, S., Kawajiri, S., Sato, F., et al. (2010) · Journal of Cell Biology · doi:10.1083/jcb.200910140 · Cited by 1,969 · see citing works
FoxO3 Controls Autophagy in Skeletal Muscle In Vivo
Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del Piccolo, P., Burden, S. J., Di Lisi, R., Sandri, C., Zhao, J., et al. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.001 · Cited by 1,953 · see citing works
Self-citationWittig, I., Braun, H., & Schägger, H. (2006) · Nature Protocols · doi:10.1038/nprot.2006.62 · Cited by 1,721 · see citing works
Zhao, J., Brault, J. J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., Lecker, S. H., & Goldberg, A. L. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.004 · Cited by 1,489 · see citing works
Self-citationTranslocation of Proteins into Mitochondria
Neupert, W., & Herrmann, J. M. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.052705.163409 · Cited by 1,486 · see citing works
Ubiquitin is phosphorylated by PINK1 to activate parkin
Koyano, F., Okatsu, K., Kosako, H., Tamura, Y., Go, E., Kimura, M., Kimura, Y., Tsuchiya, H., Yoshihara, H., Hirokawa, T., et al. (2014) · Nature · doi:10.1038/nature13392 · Cited by 1,477 · see citing works
Importing Mitochondrial Proteins: Machineries and Mechanisms
Chacińska, A., Koehler, C., Milenkovic, D., Lithgow, T., & Pfanner, N. (2009) · Cell · doi:10.1016/j.cell.2009.08.005 · Cited by 1,446 · see citing works
Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL
Jin, S. M., Lazarou, M., Wang, C., Kane, L. A., Narendra, D. P., & Youle, R. J. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201008084 · Cited by 1,375 · see citing works
One‐thousand‐and‐one substrates of protein kinase CK2?
Meggio, F., & Pinna, L. A. (2003) · The FASEB Journal · doi:10.1096/fj.02-0473rev · Cited by 1,315 · see citing works
PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity
Kane, L. A., Lazarou, M., Fogel, A. I., Li, Y., Yamano, K., Sarraf, S. A., Banerjee, S., & Youle, R. J. (2014) · Journal of Cell Biology · doi:10.1083/jcb.201402104 · Cited by 1,298 · see citing works
Protein kinase CK2: structure, regulation and role in cellular decisions of life and death
Litchfield, D. W. (2002) · Biochemical Journal · doi:10.1042/bj20021469 · Cited by 1,237 · see citing works
Self-citationChen, H., Vermulst, M., Wang, Y. E., Chomyn, A., Prolla, T. A., McCaffery, J. M., & Chan, D. C. (2010) · Cell · doi:10.1016/j.cell.2010.02.026 · Cited by 1,211 · see citing works
Organelle isolation: functional mitochondria from mouse liver, muscle and cultured filroblasts
Frezza, C., Cipolat, S., & Scorrano, L. (2007) · Nature Protocols · doi:10.1038/nprot.2006.478 · Cited by 1,188 · see citing works
Role of BNIP3 and NIX in cell death, autophagy, and mitophagy
Zhang, J., & Ney, P. A. (2009) · Cell Death & Differentiation · doi:10.1038/cdd.2009.16 · Cited by 1,021 · see citing works
Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70
Young, J. C., Hoogenraad, N. J., & Hartl, F. U. (2003) · Cell · doi:10.1016/s0092-8674(02)01250-3 · Cited by 915 · see citing works
Gegg, M. E., Cooper, J. M., Chau, K.-Y., Rojo, M., Schapira, A. H. V., & Taanman, J.-W. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq419 · Cited by 910 · see citing works
Narendra, D. P., Kane, L. A., Hauser, D. N., Fearnley, I. M., & Youle, R. J. (2010) · Autophagy · doi:10.4161/auto.6.8.13426 · Cited by 789 · see citing works
Mitochondrial processing peptidase regulates PINK1 processing, import and Parkin recruitment
Greene, A. W., Grenier, K., Aguileta, M. A., Muise, S., Farazifard, R., Haque, M. E., McBride, H. M., Park, D. S., & Fon, E. A. (2012) · The EMBO Reports · doi:10.1038/embor.2012.14 · Cited by 711 · see citing works
Milan, G., Romanello, V., Pescatore, F., Armani, A., Paik, J.-H., Frasson, L., Seydel, A., Zhao, J., Abraham, R., Goldberg, A. L., et al. (2015) · Nature Communications · doi:10.1038/ncomms7670 · Cited by 709 · see citing works
Self-citationLazarou, M., Jin, S. M., Kane, L. A., & Youle, R. J. (2012) · Developmental Cell · doi:10.1016/j.devcel.2011.12.014 · Cited by 670 · see citing works
PINK1 is degraded through the N-end rule pathway
Yamano, K., & Youle, R. J. (2013) · Autophagy · doi:10.4161/auto.24633 · Cited by 669 · see citing works
Exner, N., Lutz, A. K., Haass, C., & Winklhofer, K. F. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.170 · Cited by 652 · see citing works
A Sensitive and Quantitative Technique for Detecting Autophagic Events Based on Lysosomal Delivery
Katayama, H., Kogure, T., Mizushima, N., Yoshimori, T., & Miyawaki, A. (2011) · Chemistry & Biology · doi:10.1016/j.chembiol.2011.05.013 · Cited by 650 · see citing works
PINK1- and Parkin-mediated mitophagy at a glance
Jin, S. M., & Youle, R. J. (2012) · Journal of Cell Science · doi:10.1242/jcs.093849 · Cited by 631 · see citing works
Chen, G., Han, Z., Feng, D., Chen, Y., Chen, L., Wu, H., Huang, L., Zhou, C., Cai, X., Fu, C., et al. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.02.034 · Cited by 600 · see citing works
Mitochondrial fission and remodelling contributes to muscle atrophy
Romanello, V., Guadagnin, E., Gomes, L., Roder, I., Sandri, C., Petersen, Y., Milan, G., Masiero, E., Del Piccolo, P., Foretz, M., et al. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.60 · Cited by 596 · see citing works
Self-citationSchapira, A. H. V. (2006) · The Lancet · doi:10.1016/s0140-6736(06)68970-8 · Cited by 594 · see citing works
An investigation of spontaneous activity at the neuromuscular junction of the rat
Liley, A. W. (1956) · The Journal of Physiology · doi:10.1113/jphysiol.1956.sp005555 · Cited by 572 · see citing works
Mitochondrial membrane potential and neuronal glutamate excitotoxicity: mortality and millivolts
Nicholls, D. G., & Ward, M. W. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01534-9 · Cited by 563 · see citing works
Evolution of the Molecular Machines for Protein Import into Mitochondria
Doležal, P., Likić, V. A., Tachezy, J., & Lithgow, T. J. (2006) · Science · doi:10.1126/science.1127895 · Cited by 549 · see citing works
Grumati, 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 · see citing works
Self-citationMurakawa, T., Yamaguchi, O., Hashimoto, A., Hikoso, S., Takeda, T., Oka, T., Yasui, H., Ueda, H., Akazawa, Y., Nakayama, H., et al. (2015) · Nature Communications · doi:10.1038/ncomms8527 · Cited by 521 · see citing works
Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency
Irwin, W., Bergamin, N., Sabatelli, P., Reggiani, C., Megighian, A., Merlini, L., Braghetta, P., Columbaro, M., Volpin, D., Bressan, G. M., et al. (2003) · Nature Genetics · doi:10.1038/ng1270 · Cited by 509 · see citing works
Mitochondrial import and enzymatic activity of PINK1 mutants associated to recessive parkinsonism
Silvestri, L., Caputo, V., Bellacchio, E., Atorino, L., Dallapiccola, B., Valente, E. M., & Casari, G. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi377 · Cited by 449 · see citing works
Mitochondrial quality control: a matter of life and death for neurons
Rugarli, E. I., & Langer, T. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.38 · Cited by 419 · see citing works
The Protein Import Machinery of Mitochondria—A Regulatory Hub in Metabolism, Stress, and Disease
Harbauer, A. B., Zahedi, R. P., Sickmann, A., Pfanner, N., & Meisinger, C. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.01.010 · Cited by 377 · see citing works
Self-citationHigh-content genome-wide RNAi screens identify regulators of parkin upstream of mitophagy
Hasson, S. A., Kane, L. A., Yamano, K., Huang, C.-H., Sliter, D. A., Buehler, E., Wang, C., Heman-Ackah, S. M., Hessa, T., Guha, R., et al. (2013) · Nature · doi:10.1038/nature12748 · Cited by 365 · see citing works
Morais, V. A., Haddad, D., Craessaerts, K., Bock, P. D., Swerts, J., Vilain, S., Aerts, L., Overbergh, L., Grünewald, A., Seibler, P., et al. (2014) · Science · doi:10.1126/science.1249161 · Cited by 364 · see citing works
The kinase domain of mitochondrial PINK1 faces the cytoplasm
Zhou, C. H., Huang, Y., Shao, Y., May, J., Prou, D., Perier, C., Dauer, W. T., Schon, E. A., & Przedborski, S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802814105 · Cited by 312 · see citing works
The Genetics of Parkinson Disease
Bekris, L. M., Mata, I. F., & Zabetian, C. P. (2010) · Journal of Geriatric Psychiatry and Neurology · doi:10.1177/0891988710383572 · Cited by 307 · see citing works
Why should autophagic flux be assessed?
Zhang, X.-J., Chen, S., Huang, K.-X., & Le, W.-D. (2013) · Acta Pharmacologica Sinica · doi:10.1038/aps.2012.184 · Cited by 304 · see citing works
Brix, J., Dietmeier, K., & Pfanner, N. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.33.20730 · Cited by 289 · see citing works
Messina, A. A., Reina, S., Guarino, F., & Pinto, V. D. (2011) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2011.10.005 · Cited by 269 · see citing works
Brix, J., Rüdiger, S., Bukau, B., Schneider-Mergener, J., & Pfanner, N. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.23.16522 · Cited by 266 · see citing works
Buchou, T., Vernet, M., Blond, O., Jensen, H. H., Pointu, H., Olsen, B. B., Cochet, C., Issinger, O., & Boldyreff, B. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.3.908-915.2003 · Cited by 262 · see citing works
Establishment of conditional reporter mouse lines at ROSA26 locus for live cell imaging
Abe, T., Kiyonari, H., Shioi, G., Inoue, K., Nakao, K., Aizawa, S., & Fujimori, T. (2011) · genesis · doi:10.1002/dvg.20753 · Cited by 251 · see citing works
Regulation of mitochondrial protein import by cytosolic kinases.
Schmidt, O., Harbauer, A. B., Rao, S., Eyrich, B., Zahedi, R., Stojanovski, D., Schönfisch, B., Guiard, B., Sickmann, A., Pfanner, N., et al. (2011) · Cell · doi:10.1016/j.cell.2010.12.015 · Cited by 244 · see citing works
Self-citationGene targeting restricted to mouse striated muscle lineage
Miniou, P. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.19.e27 · Cited by 226 · see citing works
In vivo monitoring of Ca2 + uptake into mitochondria of mouse skeletal muscle during contraction
Rudolf, R., Mongillo, M., Magalhães, P. J., & Pozzan, T. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200403102 · Cited by 193 · see citing works
Self-citationPlomp, J. J., van Kempen, G. T., & MOLENAAR, P. C. (1992) · The Journal of Physiology · doi:10.1113/jphysiol.1992.sp019429 · Cited by 185 · see citing works
Casein kinase 2 is essential for mitophagy
Kanki, T., Kurihara, Y., Jin, X., Goda, T., Ono, Y., Aihara, M., Hirota, Y., Saigusa, T., Aoki, Y., Uchiumi, T., et al. (2013) · EMBO Reports · doi:10.1038/embor.2013.114 · Cited by 152 · see citing works
Synapses Form in Skeletal Muscles Lacking Neuregulin Receptors
Escher, P., Lacazette, É., Courtet, M., et al. (2005) · Science · doi:10.1126/science.1108258 · Cited by 134 · see citing works
Cytosolic cleaved PINK1 represses Parkin translocation to mitochondria and mitophagy
Fedorowicz, M. A., de Vries, R. L. A., Rüb, C., Becker, D., Huang, Y., Zhou, C., Wolken, D. M. A., Voos, W., Liu, Y., & Przedborski, S. (2013) · EMBO Reports · doi:10.1002/embr.201337294 · Cited by 127 · see citing works
Rogozhin, A., Pang, K. K., Bukharaeva, E. A., et al. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.153569 · Cited by 120 · see citing works
Erbb2 regulates neuromuscular synapse formation and is essential for muscle spindle development
Leu, M., Bellmunt, E., Schwander, M., Fariñas, I., Brenner, H. R., & Müller, U. (2003) · Development · doi:10.1242/dev.00447 · Cited by 103 · see citing works
Gerbeth, C., Schmidt, O., Rao, S., Harbauer, A. B., Mikropoulou, D., Opalińska, M., Guiard, B., Pfanner, N., & Meisinger, C. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.09.006 · Cited by 96 · see citing works
Self-citationImport of Proteins into Mitochondria
Stojanovski, D., Pfanner, N., & Wiedemann, N. (2007) · Methods in cell biology · doi:10.1016/s0091-679x(06)80036-1 · Cited by 95 · see citing works
Evolutionary Constraints of Phosphorylation in Eukaryotes, Prokaryotes, and Mitochondria
Gnad, F., Forner, F., Zielinska, D. F., Birney, E., Gunawardena, J., & Mann, M. (2010) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.001594 · Cited by 95 · see citing works
Becker, D., Richter, J., Tocilescu, M. A., Przedborski, S., & Voos, W. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.365700 · Cited by 77 · see citing works
Converging environmental and genetic pathways in the pathogenesis of Parkinson's disease
Burbulla, L. F., & Krüger, R. (2011) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2011.04.005 · Cited by 65 · see citing works
Cheusova, T., Khan, M. A., Schubert, S. W., Gavin, A., Buchou, T., Jacob, G., Sticht, H., Allende, J. E., Boldyreff, B., Brenner, H. R., et al. (2006) · Genes & Development · doi:10.1101/gad.375206 · Cited by 64 · see citing works
Self-citationTom70 Is Essential for PINK1 Import into Mitochondria
Kato, H., Lu, Q., Rapaport, D., & Kozjak‐Pavlovic, V. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058435 · Cited by 63 · see citing works
Buttgereit, A., Weber, C., Garbe, C. S., et al. (2012) · The Journal of Pathology · doi:10.1002/path.4136 · Cited by 40 · see citing works
Self-citationHerrmann, D., Straubinger, M., & Hashemolhosseini, S. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.647610 · Cited by 19 · see citing works
Self-citationAdult-onset degeneration of adipose tissue in mice deficient for the Sox8 transcription factor
Guth, S. I. E., Schmidt, K., Heß, A., & Wegner, M. (2009) · Journal of Lipid Research · doi:10.1194/jlr.m800531-jlr200 · Cited by 13 · see citing works
Electrical Activity and Postsynapse Formation in Adult Muscle: γ-AChRs Are Not Required
Hashemolhosseini, S., Moore, C., Landmann, L., et al. (2000) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2000.0911 · Cited by 12 · see citing works
Self-citationAblation of Protein Kinase CK2β in Skeletal Muscle Fibers Interferes with Their Oxidative Capacity
Eiber, N., Simeone, L., & Hashemolhosseini, S. (2017) · Pharmaceuticals · doi:10.3390/ph10010013 · Cited by 8 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Mechanisms of muscle atrophy and hypertrophy: implications in health and disease
Sartori, R., Romanello, V., & Sandri, M. (2021) · Nature Communications · doi:10.1038/s41467-020-20123-1 · Cited by 940 · see citing works
Self-citationMaintenance of Skeletal Muscle Mitochondria in Health, Exercise, and Aging
Hood, D. A., Memme, J. M., Oliveira, A. N., & Triolo, M. (2019) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020518-114310 · Cited by 567 · see citing works
Romanello, V., & Sandri, M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03662-0 · Cited by 197 · see citing works
Self-citationThe Interplay between Mitochondrial Morphology and Myomitokines in Aging Sarcopenia
Romanello, V. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010091 · Cited by 101 · see citing works
Self-citation
- Authors
- Kravic, B., Harbauer, A. B., Romanello, V., Simeone, L., Vögtle, F.-N., Kaiser, T., Straubinger, M., Huraskin, D., Böttcher, M., Cerqua, C., Martin, E. D., Poveda-Huertes, D., Buttgereit, A., Rabalski, A. J., Heuss, D., Rudolf, R., Friedrich, O., Litchfield, D., Marber, M., Salviati, L., Mougiakakos, D., Neuhuber, W., Sandri, M., Meisinger, C., & Hashemolhosseini, S.
- Affiliations
- Institute of Biochemistry, Medical Faculty, Friedrich-Alexander-University of Erlangen-Nürnberg, Erlangen, Germany
- University of Freiburg (DE)
- University of Padua (IT)
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- St Thomas' Hospital (GB)
- Western University (CA)
- Technische Hochschule Mannheim (DE)
- Corresponding author
- Hashemolhosseini, Said
- ORCID
- Venue
- Autophagy
- Publisher
- Informa UK Limited
- Published
- 2018-02-01
- Volume
- 14
- Issue
- 2
- Pages
- 311-335
- ISSN
- 1554-8627 (ISSN-L)
- 1554-8635
- PMC
- PMC5902202
- OpenAlex
- W2770295596
- Cited by
- 75
- References
- 82
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 13 · 2023: 10 · 2022: 14 · 2021: 10 · 2020: 12 · 2019: 5 · 2018: 2
- FWCI
- 4.07
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Autophagy (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Scholarship@Western (Western University) (submittedVersion)
- Padua Research Archive (University of Padova) (submittedVersion)
- Funders
- European Union ERC (282310-MyoPHAGY)
- AFM-Telethon (19524)
- Foundation Leducq, AIRC (17388)
- German Research Council DFG (HA 3309/1-3 & HA3309/3-1 to SH, Me1921/5-1 to CM)
- Interdisciplinary Centre for Clinical Research at the University Hospital of the Friedrich-Alexander University of Erlangen-Nürnberg (E2 & E17)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Keywords
- mitophagy, protein phosphorylation, skeletal muscle, mitochondrial protein import, TOM complex, PINK1, mitochondrial dysfunction, oxidative muscle fibers, muscle strength, oxygen consumption, phosphomimetic mutant
- MeSH terms
- Mitochondrial Precursor Protein Import Complex Proteins, Animals, Autophagy, Humans, Mitochondria, Muscle, Phosphorylation, Signal Transduction, Mice, Knockout, Muscle, Skeletal, Protein Transport, Models, Animal, Mitochondrial Membrane Transport Proteins, Casein Kinase II, Mitochondrial Membranes, Mice, HEK293 Cells, Mitophagy
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
