Cited by 1,026Heat shock proteins researchEndoplasmic Reticulum Stress and DiseaseMitochondrial Function and Pathology

The DOI matches its Crossref record; 55 of the 55 references it cites were found in a registry or an index.

A mitochondrial specific stress response in mammalian cells

Open access

Zhao, Quan, Wang, Jianghui, Levichkin, Ilya V., Stasinopoulos, Stan, Ryan, Michael T., Hoogenraad, Nicholas J.·2002·The EMBO Journal

DOI 10.1093/emboj/cdf445PMC PMC126185

Open this paper in CoChat — free account Open PDF

Abstract

Cells respond to a wide variety of stresses through the transcriptional activation of genes that harbour stress elements within their promoters. While many of these elements are shared by genes encoding proteins representative of all subcellular compartments, cells can also respond to stresses that are specific to individual organelles, such as the endoplasmic reticulum un folded protein response. Here we report on the discovery and characterization of a mitochondrial stress response in mammalian cells. We find that the accumulation of unfolded protein within the mitochondrial matrix results in the transcriptional upregulation of nuclear genes encoding mitochondrial stress proteins such as chaperonin 60, chaperonin 10, mtDnaJ and ClpP, but not those encoding stress proteins of the endoplasmic reticulum. Analysis of the chaperonin 60/10 bidirectional promoter identified a CHOP element as the mitochondrial stress response element. Dominant-negative mutant forms of CHOP and overexpression of CHOP revealed that this transcription factor, in association with C/EBPbeta, regulates expression of mitochondrial stress genes in response to the accumulation of unfolded proteins.

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

Crossref · 10.1093/emboj/cdf445

Cites

55 of 55 references verified0 citation errors · 0 not checkable

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Site-directed mutagenesis by overlap extension using the polymerase chain reaction
Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K., & Pease, L. R. (1989) · Gene · doi:10.1016/0378-1119(89)90358-2 · Cited by 7,414
Efficient selection for high-expression transfectants with a novel eukaryotic vector
Niwa, H., Yamamura, K., & Miyazaki, J. (1991) · Gene · doi:10.1016/0378-1119(91)90434-d · Cited by 5,149
Control of inositol 1,4,5-trisphosphate-induced Ca2+ release by cytosolic Ca2+
Bootman, M. D., Missiaen, L., Parys, J. B., SMEDT, H. D., & Casteels, R. (1995) · Biochemical Journal · doi:10.1042/bj3060445 · Cited by 5,131
Prevention of Apoptosis by Bcl-2: Release of Cytochrome c from Mitochondria Blocked
Yang, J., Liu, X., Bhalla, K. N., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T.-I., Jones, D. P., & Wang, X. (1997) · Science · doi:10.1126/science.275.5303.1129 · Cited by 4,913
XBP1 mRNA Is Induced by ATF6 and Spliced by IRE1 in Response to ER Stress to Produce a Highly Active Transcription Factor
Yoshida, H., Matsui, T., Yamamoto, A., Okada, T., & Mori, K. (2001) · Cell · doi:10.1016/s0092-8674(01)00611-0 · Cited by 4,054
Mutation of the mouse klotho gene leads to a syndrome resembling ageing
Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., et al. (1997) · Nature · doi:10.1038/36285 · Cited by 3,837
Molecular chaperones in cellular protein folding
Hartl, F. U. (1996) · Nature · doi:10.1038/381571a0 · Cited by 3,584
Regulated Translation Initiation Controls Stress-Induced Gene Expression in Mammalian Cells
Harding, H. P., Novoa, I., Zhang, Y., Zeng, H., Wek, R. C., Schapira, M., & Ron, D. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00108-8 · Cited by 3,344
IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA
Calfon, M. A., Zeng, H., Urano, F., Till, J. H., Hubbard, S. R., Harding, H. P., Clark, S. G., & Ron, D. (2002) · Nature · doi:10.1038/415092a · Cited by 2,907
A rapid micrqpreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells
Andrews, N. C., & Faller, D. V. (1991) · Nucleic Acids Research · doi:10.1093/nar/19.9.2499 · Cited by 2,337

Flagged first, then by citations

Show all 55 references

Sorted by citations

Items 501–600 of 999

The unfolded protein response in relation to mitochondrial biogenesis in skeletal muscle cells
Moosavi, Z. S. M., & Hood, D. A. (2017) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00320.2016 · Cited by 34
Progressing neurobiological strategies against proteostasis failure: Challenges in neurodegeneration
Amanullah, A., Upadhyay, A., Joshi, V., Mishra, R., Jana, N. R., & Mishra, A. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.08.005 · Cited by 34
Stress signaling and cellular proliferation reverse the effects of mitochondrial mistranslation
Ferreira, N., Perks, K. L., Rossetti, G., Rudler, D. L., Hughes, L. A., Ermer, J. A., Scott, L. H., Kuznetsova, I., Richman, T. R., Narayana, V. K., et al. (2019) · The EMBO Journal · doi:10.15252/embj.2019102155 · Cited by 31
Exercise alters the mitochondrial proteostasis and induces the mitonuclear imbalance and UPRmt in the hypothalamus of mice
Braga, R. R., Crisol, B., Brícola, R. S., Sant’Ana, M. R., Nakandakari, S. C. B. R., COSTA, S. O., Prada, P. O., da Silva, A. S. R., de Moura, L. P., Pauli, J. R., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-82352-8 · Cited by 31
Sesn2 Serves as a Regulator between Mitochondrial Unfolded Protein Response and Mitophagy in Intervertebral Disc Degeneration
Xu, W., Liu, C., Zheng, H., Xu, H., Yang, R., Jiang, S., & Zhu, L.-X. (2023) · International Journal of Biological Sciences · doi:10.7150/ijbs.70211 · Cited by 34
Berberine exerts anti-adipogenic activity through up-regulation of C/EBP inhibitors, CHOP and DEC2
Pham, T. P. T., Kwon, J., & Shin, J. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.08.110 · Cited by 33
StAR Enhances Transcription of Genes Encoding the Mitochondrial Proteases Involved in Its Own Degradation
Bahat, A., Perlberg, S., Melamed‐Book, N., Lauria, I., Langer, T., & Orly, J. (2013) · Molecular Endocrinology · doi:10.1210/me.2013-1275 · Cited by 34
Inhibition of the mitochondrial unfolded protein response by acetylcholine alleviated hypoxia/reoxygenation-induced apoptosis of endothelial cells
Xu, M., Bi, X., He, X., Yu, X., Zhao, M. F., & Zang, W. (2016) · Cell Cycle · doi:10.1080/15384101.2016.1160985 · Cited by 31
Mitochondrial quality control in the cardiac system: An integrative view
Cadete, V. J. J., Vasam, G., Menzies, K. J., & Burelle, Y. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.11.018 · Cited by 36
Cumulative mitochondrial activity correlates with ototoxin susceptibility in zebrafish mechanosensory hair cells
Pickett, S. B., Thomas, E. D., Sebe, J. Y., Linbo, T. H., Esterberg, R., Hailey, D. W., & Raible, D. W. (2018) · eLife · doi:10.7554/elife.38062 · Cited by 32
Mitochondrial control of cellular protein homeostasis
Mohanraj, K., Nowicka, U., & Chacińska, A. (2020) · Biochemical Journal · doi:10.1042/bcj20190654 · Cited by 27
Mitochondrial Kinases and the Role of Mitochondrial Protein Phosphorylation in Health and Disease
Kotrasová, V., Keresztesová, B., Ondrovičová, G., Bauer, J., Havalová, H., Pevala, V., Kutějová, E., & Kunová, N. (2021) · Life · doi:10.3390/life11020082 · Cited by 35
Hormonal Regulation of Oxidative Phosphorylation in the Brain in Health and Disease
Głombik, K., Detka, J., & Budziszewska, B. (2021) · Cells · doi:10.3390/cells10112937 · Cited by 34
Boosting mitochondrial health to counteract neurodegeneration
Burtscher, J., Romani, M., Bernardo, G., Popa, T., Ziviani, E., Hummel, F. C., Sorrentino, V., & Millet, G. P. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102289 · Cited by 36
Arming a killer: mitochondrial regulation of CD8+ T cell cytotoxicity
Lisci, M., & Griffiths, G. M. (2022) · Trends in Cell Biology · doi:10.1016/j.tcb.2022.05.007 · Cited by 29
Mitochondria pleiotropism in stem cell senescence: Mechanisms and therapeutic approaches
Mas‐Bargues, C. (2023) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2023.09.019 · Cited by 37
Heat shock protein 60 in rostral ventrolateral medulla reduces cardiovascular fatality during endotoxaemia in the rat
Chang, A. Y., Chan, J. Y. H., Chou, J. L., Li, F. C. H., Dai, K., & Chan, S. H. H. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.110890 · Cited by 32
Gene Expression Profiling Identifies a Role for CHOP During Inhibition of the Mitochondrial Respiratory Chain
Ishikawa, F., Akimoto, T., Yamamoto, H., Araki, Y., Yoshie, T., Mori, K., Hayashi, H., Nose, K., & Shibanuma, M. (2009) · The Journal of Biochemistry · doi:10.1093/jb/mvp052 · Cited by 31
Mitochondrial translation and cellular stress response
Suhm, T., & Ott, M. (2016) · Cell and Tissue Research · doi:10.1007/s00441-016-2460-4 · Cited by 34
The Mitochondrial Unfolded Protein Response as a Non-Oncogene Addiction to Support Adaptation to Stress during Transformation in Cancer and Beyond
Kenny, T. C., Manfredi, G., & Germain, D. (2017) · Frontiers in Oncology · doi:10.3389/fonc.2017.00159 · Cited by 33
Improved mitochondrial stress response in long‐lived Snell dwarf mice
Ozkurede, U., & Miller, R. A. (2019) · Aging Cell · doi:10.1111/acel.13030 · Cited by 33
Does perturbation in the mitochondrial protein folding pave the way for neurodegeneration diseases?
Ji, T., Zhang, X., Xin, Z., Xu, B., Jin, Z., Wu, J., Hu, W., & Yang, Y. (2019) · Ageing Research Reviews · doi:10.1016/j.arr.2019.100997 · Cited by 29
Hyperphosphorylated Human Tau Accumulates at the Synapse, Localizing on Synaptic Mitochondrial Outer Membranes and Disrupting Respiration in a Mouse Model of Tauopathy
Trease, A. J., George, J. W., Roland, N. J., Lichter, E. Z., Emanuel, K. M., Totusek, S., Fox, H. S., & Stauch, K. L. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.852368 · Cited by 31
The emergent role of mitochondrial surveillance in cellular health
Tjahjono, E., Kirienko, D. R., & Kirienko, N. V. (2022) · Aging Cell · doi:10.1111/acel.13710 · Cited by 30
Endoplasmic Reticulum Stress Underlies Nanosilver-Induced Neurotoxicity in Immature Rat Brain
Dąbrowska‐Bouta, B., Sułkowski, G., Gewartowska, M., & Strużyńska, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113013 · Cited by 31
Single-nucleotide variations in the genes encoding the mitochondrial Hsp60/Hsp10 chaperone system and their disease-causing potential
Bross, P., Li, Z., Hansen, J., Hansen, J. J., Nielsen, M. N., Corydon, T. J., Georgopoulos, C. P., Ang, D., Banner, J., Niezen‐Koning, K. E., et al. (2006) · Journal of Human Genetics · doi:10.1007/s10038-006-0080-7 · Cited by 32
NO‐induced downregulation of HSP10 and HSP60 expression in the postischemic brain
Kim, S., & Lee, J. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21236 · Cited by 31
Obesity-induced changes in kidney mitochondria and endoplasmic reticulum in the presence or absence of leptin
Munusamy, S., do Carmo, J. M., Hosler, J. P., & Hall, J. E. (2015) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00188.2015 · Cited by 32
The Versatile Stress Protein Mortalin as a Chaperone Therapeutic Agent
Deocaris, C. C., Kaul, S. C., & Wadhwa, R. (2009) · Protein and Peptide Letters · doi:10.2174/092986609788167770 · Cited by 30
Role of Heat Shock Factor 1 in Conserving Cholesterol Transportation in Leydig Cell Steroidogenesis via Steroidogenic Acute Regulatory Protein
Oka, S., Shiraishi, K., Fujimoto, M., Katiyar, A., Takii, R., Nakai, A., & Matsuyama, H. (2017) · Endocrinology · doi:10.1210/en.2017-00132 · Cited by 28
UPRmt and coordinated UPRER in type 2 diabetes
Kang, Z., Chen, F., Wu, W., Liu, R. R., Chen, T., & Xu, F. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.974083 · Cited by 29
Molecular cloning, expression patterns and subcellular localization of porcine TMCO1 gene
Zhang, Z., Mo, D., Cong, P., He, Z., Ling, F., Li, A., Niu, Y., Zhao, X. L., Zhou, C., & Chen, Y. (2009) · Molecular Biology Reports · doi:10.1007/s11033-009-9573-8 · Cited by 30
From discovery of the CHOP axis and targeting ClpP to the identification of additional axes of the UPRmt driven by the estrogen receptor and SIRT3
Kenny, T. C., & Germain, D. (2017) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-017-9722-z · Cited by 31
Biliverdin Reductase-A integrates insulin signaling with mitochondrial metabolism through phosphorylation of GSK3β
Lanzillotta, C., Tramutola, A., Lanzillotta, S., Greco, V., Pagnotta, S. E., Sanchini, C., Angelantonio, S. D., Forte, E., Rinaldo, S., Paone, A., et al. (2024) · Redox Biology · doi:10.1016/j.redox.2024.103221 · Cited by 30
ATF5-Mediated Mitochondrial Unfolded Protein Response (UPR mt ) Protects Neurons Against Oxygen-Glucose Deprivation and Cerebral Ischemia
An, H., Zhou, B., Hayakawa, K., Durán‐Laforet, V., Park, J.-H., Nakamura, Y., Mandeville, E. T., Liu, N., Guo, S., Yu, Z., et al. (2024) · Stroke · doi:10.1161/strokeaha.123.045550 · Cited by 32
DELE1 maintains muscle proteostasis to promote growth and survival in mitochondrial myopathy
Lin, H.-P., Petersen, J. D., Gilsrud, A. J., Madruga, A., D’Silva, T. M., Huang, X., Shammas, M. K., Randolph, N., Johnson, K. R., Li, Y., et al. (2024) · The EMBO Journal · doi:10.1038/s44318-024-00242-x · Cited by 28
The mitochondrial integrated stress response: A novel approach to anti-aging and pro-longevity
Wang, X., & Zhang, G. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102603 · Cited by 29
Mitochondrial Alkbh1 localizes to mtRNA granules and its knockdown induces the mitochondrial UPR in humans and C. elegans
Wagner, A., Hofmeister, O., Rolland, S. G. M., Maiser, A., Aasumets, K., Schmitt, S., Schorpp, K., Feuchtinger, A., Hadian, K., Schneider, S., et al. (2019) · Journal of Cell Science · doi:10.1242/jcs.223891 · Cited by 28
Acetaldehyde dehydrogenase 2 deficiency increases mitochondrial reactive oxygen species emission and induces mitochondrial protease Omi/HtrA2 in skeletal muscle
Wakabayashi, Y., Tamura, Y., Kouzaki, K., Kikuchi, N., Hiranuma, K., Menuki, K., Tajima, T., Yamanaka, Y., Sakai, A., Nakayama, K. I., et al. (2020) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00089.2019 · Cited by 29
Does proteostasis get lost in translation? Implications for protein aggregation across the lifespan
Francisco, S., Ferreira, M., Moura, G. R., Soares, A. R., & Santos, M. A. S. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101119 · Cited by 31
Transcriptional Responses of the Heat Shock Protein 20 (Hsp20) and 40 (Hsp40) Genes to Temperature Stress and Alteration of Life Cycle Stages in the Harmful Alga Scrippsiella trochoidea (Dinophyceae)
Deng, Y., Hu, Z., Shang, L., Chai, Z., & Tang, Y. Z. (2020) · Biology · doi:10.3390/biology9110408 · Cited by 29
Expression of heat shock protein 60 in the tissues of transported piglets
Zhu, L., Bao, E., Zhao, R., & Hartung, J. (2008) · Cell Stress and Chaperones · doi:10.1007/s12192-008-0055-z · Cited by 29
Regulation of proteostasis and innate immunity via mitochondria-nuclear communication
Kim, S., Ramalho, T. R. D. O., & Haynes, C. M. (2024) · The Journal of Cell Biology · doi:10.1083/jcb.202310005 · Cited by 30
Mammalian mitohormesis: from mitochondrial stressors to organismal benefits
Gunawan, A. L., Liparulo, I., & Stahl, A. (2025) · The EMBO Journal · doi:10.1038/s44318-025-00549-3 · Cited by 33
The mitohormetic response as part of the cytoprotection mechanism of berberine
Zhu, X., Wei, Y., Yang, B., Yin, X., & Guo, X. (2020) · Molecular Medicine · doi:10.1186/s10020-020-0136-8 · Cited by 29
The Portrait of Liver Cancer is Shaped by Mitochondrial Genetics
Chattopadhyay, M., Jenkins, E. C., Lechuga‐Vieco, A. V., Nie, K., Fiel, M. I., Rialdi, A., Guccione, E., Enrı́quez, J. A., Sia, D., Lujambio, A., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.110254 · Cited by 28
Mammalian iron sulfur cluster biogenesis and human diseases
Maio, N., & Rouault, T. A. (2022) · IUBMB Life · doi:10.1002/iub.2597 · Cited by 28
Control of mitochondrial integrity influences oocyte quality during reproductive aging
Khan, S. A., Reed, L., Schoolcraft, W. B., Yuan, Y., & Krisher, R. L. (2023) · Molecular Human Reproduction · doi:10.1093/molehr/gaad028 · Cited by 30
Loss of c/EBP-β activity promotes the adaptive to apoptotic switch in hypoxic cortical neurons
Halterman, M. W., Jesus, C. D., Rempe, D. A., Schor, N. F., & Federoff, H. J. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.01.014 · Cited by 28
Effect of Tim23 knockdown in vivo on mitochondrial protein import and retrograde signaling to the UPRmt in muscle
Oliveira, A. N., & Hood, D. A. (2018) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00275.2017 · Cited by 28
Complexity of Hsp90 in organelle targeting
Prassinos, C., Haralampidis, K., Milioni, D., Samakovli, D., Krambis, K., & Hatzopoulos, P. (2008) · Plant Molecular Biology · doi:10.1007/s11103-008-9322-8 · Cited by 28
The current insights of mitochondrial hormesis in the occurrence and treatment of bone and cartilage degeneration
Da, W., Chen, Q., & Shen, B. (2024) · Biological Research · doi:10.1186/s40659-024-00494-1 · Cited by 32
Mitochondrial DNA variability modulates mRNA and intra-mitochondrial protein levels of HSP60 and HSP75: experimental evidence from cybrid lines
Bellizzi, D., Taverna, D., D’Aquila, P., Blasi, S. D., & BENEDICTIS, G. D. (2008) · Cell Stress and Chaperones · doi:10.1007/s12192-008-0081-x · Cited by 27
4E-BP1 Protects Neurons from Misfolded Protein Stress and Parkinson's Disease Toxicity by Inducing the Mitochondrial Unfolded Protein Response
Dastidar, S. G., Pham, M. T., Mitchell, M. B., Yeom, S. G., Jordan, S., Chang, A., Sopher, B. L., & La Spada, A. R. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.0940-20.2020 · Cited by 27
FANCD2 modulates the mitochondrial stress response to prevent common fragile site instability
Fernandes, P., Miotto, B., Saint‐Ruf, C., Said, M., Barra, V., Nähse, V., Ravera, S., Cappelli, E., & Naim, V. (2021) · Communications Biology · doi:10.1038/s42003-021-01647-8 · Cited by 28
Proteomic investigation of cultivated fibroblasts from patients with mitochondrial short-chain acyl-CoA dehydrogenase deficiency
Edhager, A. V., Stenbroen, V., Nielsen, N. S., Bross, P., Olsen, R. K. J., Gregersen, N., & Palmfeldt, J. (2014) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2014.01.007 · Cited by 27
Utilization of the cellular stress response to sensitize cancer cells to TRAIL-mediated apoptosis
Siegelin, M. D. (2012) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2012.703655 · Cited by 27
Ablation of the mitochondrial complex IV assembly protein Surf1 leads to increased expression of the UPRMT and increased resistance to oxidative stress in primary cultures of fibroblasts
Pharaoh, G. A., Pulliam, D. A., Hill, S., Sataranatarajan, K., & Remmen, H. V. (2016) · Redox Biology · doi:10.1016/j.redox.2016.05.001 · Cited by 27
Structural and functional consequences of c-N-Ras constitutively associated with intact mitochondria
Wolfman, J. C., Planchon, S. M., Liao, J., & Wolfman, A. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2006.07.015 · Cited by 28
Exercise Improves the Coordination of the Mitochondrial Unfolded Protein Response and Mitophagy in Aging Skeletal Muscle
Wang, Y., Li, J., Zhang, Z., Wang, R., Hai, B., & Zhang, Y. (2023) · Life · doi:10.3390/life13041006 · Cited by 29
The mitochondrial unfolded protein response inhibits pluripotency acquisition and mesenchymal-to-epithelial transition in somatic cell reprogramming
Ying, Z., Xin, Y., Liu, Z., Tan, T., Huang, Y., Ding, Y., Hong, X., Li, Q., Li, C., Guo, J., et al. (2025) · Nature Metabolism · doi:10.1038/s42255-025-01261-6 · Cited by 25
Self-citation
Perspectives on mitochondrial dysfunction in the regeneration of aging skeletal muscle
Wang, K., Gan, M., Lei, Y., Liao, T., Li, J., Niu, L., Zhao, Y., Chen, L., Wang, Y., Zhu, L., et al. (2025) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-025-00771-1 · Cited by 34
MicroRNA‐382 silencing induces a mitonuclear protein imbalance and activates the mitochondrial unfolded protein response in muscle cells
Dahlmans, D., Houzelle, A., Andreux, P. A., Wang, X., Jörgensen, J. A., Moullan, N., Daemen, S., Kersten, S., Auwerx, J. H., & Hoeks, J. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27401 · Cited by 27
Copper exposure induces mitochondrial dynamic disorder and oxidative stress via mitochondrial unfolded protein response in pig fundic gland
Huo, H., Wang, S., Bai, Y., Liao, J., Li, X., Zhang, H., Han, Q., Hu, L., Pan, J., Li, Y., et al. (2021) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2021.112587 · Cited by 26
Molecular Hydrogen Enhances Proliferation of Cancer Cells That Exhibit Potent Mitochondrial Unfolded Protein Response
Hasegawa, T., Ito, M., Hasegawa, S., Teranishi, M., Takeda, K., Negishi, S., Nishiwaki, H., Takeda, J., LeBaron, T. W., & Ohno, K. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052888 · Cited by 26
Organismal and Cellular Stress Responses upon Disruption of Mitochondrial Lonp1 Protease
Taouktsi, E., Kyriakou, E., Smyrniotis, S., Borbolis, F., Bondi, L., Avgeris, S. N., Trigazis, E., Rigas, S., Voutsinas, G. E., & Syntichaki, P. (2022) · Cells · doi:10.3390/cells11081363 · Cited by 28
Reversible Assembly of the ATP-binding Cassette Transporter Mdl1 with the F1F0-ATP Synthase in Mitochondria
Galluhn, D., & Langer, T. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405871200 · Cited by 26
Targeting Mitochondrial Dysfunction for the Prevention and Treatment of Metabolic Disease by Bioactive Food Components
Kim, M., Lee, J., & Lee, J. (2024) · Journal of Lipid and Atherosclerosis · doi:10.12997/jla.2024.13.3.306 · Cited by 28
Stimulation of cytoprotective autophagy and components of mitochondrial biogenesis / proteostasis in response to ionizing radiation as a credible pro-survival strategy
Das, S., Joshi, M. B., Parashiva, G. K., & Rao, B. S. S. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.01.015 · Cited by 26
Metolazone upregulates mitochondrial chaperones and extends lifespan in Caenorhabditis elegans
Ito, A., Zhao, Q., Tanaka, Y., Yasui, M., Katayama, R., Sun, S., Tanimoto, Y., Nishikawa, Y., & Kage‐Nakadai, E. (2020) · Biogerontology · doi:10.1007/s10522-020-09907-6 · Cited by 24
Self-citation
The Mitochondrial Unfolded Protein Response: A Novel Protective Pathway Targeting Cardiomyocytes
Liu, J., He, X., Zheng, S., Zhu, A., & Wang, J. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/6430342 · Cited by 25
Self-citation
Open questions on the mitochondrial unfolded protein response
Vögtle, F. ‐. (2020) · FEBS Journal · doi:10.1111/febs.15569 · Cited by 25
Dorfin prevents cell death by reducing mitochondrial localizing mutant superoxide dismutase 1 in a neuronal cell model of familial amyotrophic lateral sclerosis
Takeuchi, H., Niwa, J., Hishikawa, N., Ishigaki, S., Tanaka, F., Doyu, M., & Sobue, G. (2004) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02289.x · Cited by 25
Inhibition of USP14 induces ER stress–mediated autophagy without apoptosis in lung cancer cell line A549
Moghadami, A.-A., Beilankouhi, E. A. V., Kalantary‐Charvadeh, A., Hamzavi, M., Mosayyebi, B., Sedghi, H., Haghjo, A. G., & Ahmad, S. N. S. (2020) · Cell Stress and Chaperones · doi:10.1007/s12192-020-01125-w · Cited by 24
The effect of gestational diabetes on the expression of mitochondrial fusion proteins in placental tissue
Kolaç, U. K., Eken, M. K., Ünübol, M., Dönmez, G., & Yalçın, A. (2021) · Placenta · doi:10.1016/j.placenta.2021.09.015 · Cited by 25
Activating transcription factor 4 regulates mitochondrial content, morphology, and function in differentiating skeletal muscle myotubes
Memme, J. M., Sanfrancesco, V. C., & Hood, D. A. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00080.2023 · Cited by 25
Loss of Toll-like Receptor 2 and 4 Leads to Differential Induction of Endoplasmic Reticulum Stress and Proapoptotic Responses in the Intestinal Epithelium under Conditions of Chronic Inflammation
Messlik, A., Schmechel, S., Kisling, S., Bereswill, S., Heimesaat, M. M., Fischer, A., Göbel, U. B., & Haller, D. (2009) · Journal of Proteome Research · doi:10.1021/pr9000465 · Cited by 24
Coordinating Mitochondrial Biology Through the Stress-Responsive Regulation of Mitochondrial Proteases
Lebeau, J., Rainbolt, T. K., & Wiseman, R. L. (2018) · International review of cytology · doi:10.1016/bs.ircmb.2018.05.003 · Cited by 25
Mitochondria at the Crossroads of Physiology and Pathology
Moro, L. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9061971 · Cited by 25
Exposure to arginine analog canavanine induces aberrant mitochondrial translation products, mitoribosome stalling, and instability of the mitochondrial proteome
Konovalova, S. A., Hilander, T., Loayza‐Puch, F., Rooijers, K., Agami, R., & Tyynismaa, H. (2015) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2015.06.018 · Cited by 22
Reproductive Ageing: Metabolic contribution to age-related chromosome missegregation in mammalian oocytes
Mihalas, B. P., Marston, A. L., Wu, L. E., & Gilchrist, R. B. (2024) · Reproduction · doi:10.1530/rep-23-0510 · Cited by 26
Quality control in mitochondria: use it, break it, fix it, trash it
Kornmann, B. (2014) · F1000Prime Reports · doi:10.12703/p6-15 · Cited by 26
Mitochondrial stress and aging: Lessons from C. elegans
Chen, P. X., Zhang, L., Chen, D., & Tian, Y. (2023) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2023.02.010 · Cited by 23
The influence of ATP-dependent proteases on a variety of nucleoid-associated processes
Ambro, Ľ., Pevala, V., Bauer, J., & Kutějová, E. (2012) · Journal of Structural Biology · doi:10.1016/j.jsb.2012.05.018 · Cited by 25
Changes in immunoreactivity of HSP60 and its neuroprotective effects in the gerbil hippocampal CA1 region induced by transient ischemia
Hwang, I. K., Ahn, H. C., Yoo, K., Lee, J., Suh, H., Kwon, Y., Cho, J. H., & Won, M. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.08.017 · Cited by 23
Protein Misfolding, Aggregation, and Degradation in Disease
Gregersen, N., Bolund, L., & Bross, P. (2003) · Humana Press eBooks · doi:10.1385/1-59259-394-1:3 · Cited by 23
Early Transcriptional Landscapes of Chlamydia trachomatis-Infected Epithelial Cells at Single Cell Resolution
Hayward, R. J., Marsh, J. W., Humphrys, M. S., Huston, W. M., & Myers, G. S. A. (2019) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2019.00392 · Cited by 22
Arsenal of Phytochemicals to Combat Against Arsenic-Induced Mitochondrial Stress and Cancer
Sarkar, N., Das, B., Bishayee, A., & Sinha, D. (2019) · Antioxidants and Redox Signaling · doi:10.1089/ars.2019.7950 · Cited by 23
Sestrins: Darkhorse in the regulation of mitochondrial health and metabolism
Kumar, A. A., Dhiman, D., & Shaha, C. (2020) · Molecular Biology Reports · doi:10.1007/s11033-020-05769-w · Cited by 23
Methods to Study the Mitochondrial Unfolded Protein Response (UPRmt) in Caenorhabditis elegans
Haeussler, S., & Conradt, B. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-1732-8_16 · Cited by 22
V-ATPase/TORC1-mediated ATFS-1 translation directs mitochondrial UPR activation in C. elegans
Li, T. Y., Gao, A. W., Li, X., Li, H., Liu, Y. J., Lalou, A., Neelagandan, N., Naef, F., Schoonjans, K., & Auwerx, J. H. (2022) · The Journal of Cell Biology · doi:10.1083/jcb.202205045 · Cited by 24
The intestinal epithelial-macrophage-crypt stem cell axis plays a crucial role in regulating and maintaining intestinal homeostasis
Hu, X., Yuan, X., Zhang, G., Song, H., Ji, P., Guo, Y., Liu, Z., Tian, Y., Shen, R., & Wang, D. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.122452 · Cited by 24
Jasmonic acid plays an important role in mediating retrograde signaling under mitochondrial translational stress to balance plant growth and defense
Li, J., Yu, G., Wang, X., Guo, C., Wang, X., & Wang, X. (2024) · Plant Communications · doi:10.1016/j.xplc.2024.101133 · Cited by 23
Chaperones as Parts of Organelle Networks
Szabadkai, G., & Rizzuto, R. (2007) · Springer eBooks · doi:10.1007/978-0-387-39975-1_7 · Cited by 22
RBX1-mediated ubiquitination of SESN2 promotes cell death upon prolonged mitochondrial damage in SH-SY5Y neuroblastoma cells
Kumar, A. A., & Shaha, C. (2018) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-017-3267-7 · Cited by 23
Cellular Protein Quality Control in Diabetic Cardiomyopathy: From Bench to Bedside
Kaur, N., Raja, R., Ruiz‐Velasco, A., & Liu, W. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.585309 · Cited by 24
An imbalance in C/EBPs and increased mitochondrial activity in asthmatic airway smooth muscle cells: novel targets in asthma therapy?
Roth, M., & Black, J. L. (2009) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2009.00188.x · Cited by 22
Triacylglycerol mobilization underpins mitochondrial stress recovery
Baker, Z. N., Zhu, Y., Guerra, R. M., Smith, A. J., Arra, A., Serrano, L. R., Overmyer, K. A., Mukherji, S., Craig, E. A., Coon, J. J., et al. (2025) · Nature Cell Biology · doi:10.1038/s41556-024-01586-6 · Cited by 21
A lysosomal surveillance response to stress extends healthspan
Li, T. Y., Gao, A. W., Yang, R., Sun, Y., Lei, Y., Li, X., Chen, L., Liu, Y. J., Arey, R. N., Morales, K., et al. (2025) · Nature Cell Biology · doi:10.1038/s41556-025-01693-y · Cited by 28
Plant Mitochondrial Retrograde Regulation
Rhoads, D. M. (2010) · Springer eBooks · doi:10.1007/978-0-387-89781-3_16 · Cited by 21

Authors: Zhao, Q., Wang, J., Levichkin, I. V., Stasinopoulos, S., Ryan, M. T., & Hoogenraad, N. J.
Affiliations: La Trobe University (AU)
Corresponding author: Hoogenraad, Nicholas J.
ORCID: Zhao, Quan
Venue: The EMBO Journal
Publisher: Springer Science and Business Media LLC
Published: 2002-09-02
Volume: 21
Issue: 17
Pages: 4411-4419
ISSN: 0261-4189 (ISSN-L)
1460-2075
DOI: 10.1093/emboj/cdf445
PMC: PMC126185
OpenAlex: W2108738634
Cited by: 1,026
References: 55
Citations by year: 2026: 58 · 2025: 64 · 2024: 71 · 2023: 59 · 2022: 71 · 2021: 88 · 2020: 77 · 2019: 60 · 2018: 60 · 2017: 46 · 2016: 50 · 2015: 42 · 2014: 45 · 2013: 38 · 2012: 29
FWCI: 4.06
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: The EMBO Journal (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Medical Research Council
Australian Research Council
National Health and Medical Research Council
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Keywords: mitochondrial stress response, unfolded protein accumulation, mitochondrial matrix, CHOP, C/EBPβ, transcriptional regulation, chaperonin 60, GroES, ClpP, unfolded protein response, mammalian cells
MeSH terms: Adenosine Triphosphatases, Animals, Cell Nucleus, Chlorocebus aethiops, Gene Expression Regulation, Genes, Dominant, Heat-Shock Proteins, Mitochondria, Ornithine Carbamoyltransferase, Promoter Regions, Genetic, Protein Processing, Post-Translational, Recombinant Fusion Proteins, Regulatory Sequences, Nucleic Acid, Serine Endopeptidases, Stress, Physiological, Transcription Factors, Transcription, Genetic, Transfection, Signal Transduction, Sequence Deletion, Protein Folding, Chaperonin 60, Chaperonin 10, COS Cells, Protein Transport, CCAAT-Enhancer-Binding Proteins, Endopeptidase Clp, HSP40 Heat-Shock Proteins, Transcription Factor CHOP

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

A mitochondrial specific stress response in mammalian cells

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks