Cited by 385Cell death mechanisms and regulationAutophagy in Disease and TherapyMitochondrial Function and Pathology

The DOI matches its Crossref record; 50 of the 50 references it cites were found in a registry or an index.

Mitochondrial membrane permeabilization is a critical step of lysosome-initiated apoptosis induced by hydroxychloroquine

Boya, Patricia, Gonzalez-Polo, Rosa-Ana, Poncet, Delphine, Andreau, Karine, Vieira, Helena LA, Roumier, Thomas, Perfettini, Jean-Luc, Kroemer, Guido·2003·Oncogene

DOI 10.1038/sj.onc.1206622

Open this paper in CoChat — free account

Abstract

Hydroxychloroquine (HCQ) is a lysosomotropic amine with cytotoxic properties. Here, we show that HCQ induces signs of lysosomal membrane permeabilization (LMP), such as the decrease in the lysosomal pH gradient and the release of cathepsin B from the lysosomal lumen, followed by signs of apoptosis including caspase activation, phosphatidylserine exposure, and chromatin condensation with DNA loss. HCQ also induces mitochondrial membrane permeabilization (MMP), as indicated by the insertion of Bax into mitochondrial membranes, the conformational activation of Bax within mitochondria, the release of cytochrome c from mitochondria, and the loss of the mitochondrial transmembrane potential. To determine the molecular order among these events, we introduced inhibitors of LMP (bafilomycin A(1)), MMP (Bcl-X(L), wild-type Bcl-2, mitochondrion-targeted Bcl-2, or viral mitochondrial inhibitor of apoptosis from cytomegalovirus), and caspases (Z-VAD.fmk) into the system. Our data indicate that caspase-independent MMP is rate-limiting for LMP-mediated caspase activation. Mouse embryonic fibroblasts lacking the expression of both Bax and Bak are resistant against hydroxychloroquine-induced apoptosis. Such Bax(-/-) Bak(-/-) cells manifest normal LMP, yet fail to undergo MMP and subsequent cell death. The data reported herein indicate that LMP does not suffice to trigger caspase activation and that Bax/Bak-dependent MMP is a critical step of LMP-induced cell death.

Integrity signals

Registry

Crossref · 10.1038/sj.onc.1206622

Cites

50 of 50 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Mitochondria and Apoptosis
Green, D. R., & Reed, J. C. (1998) · Science · doi:10.1126/science.281.5381.1309 · Cited by 9,051
Surfing the p53 network
Vogelstein, B., Lane, D., & Levine, A. J. (2000) · Nature · doi:10.1038/35042675 · Cited by 6,607 · cited 1×
“…of the proapoptotic genes Bax and Bak (whose products induce MMP) confers a broad cytoprotection including against nuclear DNA damage and ER stress (Zamzami et al., 1998; Vogelstein et al., 2000; Ferri and Kroemer, 2001; Wei et al., 2001; Boya et al., 2002; Reed, 2002; Zamzami and Kroemer, 2003).”
Background
Proapoptotic BAX and BAK: A Requisite Gateway to Mitochondrial Dysfunction and Death
Wei, M. C., Zong, W.-X., Cheng, E. H.-Y., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B., & Korsmeyer, S. J. (2001) · Science · doi:10.1126/science.1059108 · Cited by 3,988
Mitochondrial control of cell death
Kroemer, G., & Reed, J. C. (2000) · Nature Medicine · doi:10.1038/74994 · Cited by 3,103
Self-citation
Functions of Lysosomes
de Duve, C., & Wattiaux, R. (1966) · Annual Review of Physiology · doi:10.1146/annurev.ph.28.030166.002251 · Cited by 3,033 · cited 1×
“…this paper reinforce the general idea that MMP is rate limiting for cell death induction (Boya et al., 2003), even when apoptosis has initially been triggered by permeabilizing the ‘suicide bags’, as lysosomes have been initially nick-named (De Duve and Wattiaux, 1966; Lockshin and Zakeri, 2001).”
Background
Caspases: killer proteases
Nicholson, D. W., & Thornberry, N. A. (1997) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(97)01085-2 · Cited by 2,418
Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death.
Zamzami, N., Marchetti, P., Castedo, M., Decaudin, D., Macho, A., Hirsch, T., Susin, S. A., Petit, P. X., Mignotte, B., & Kroemer, G. (1995) · The Journal of experimental medicine · doi:10.1084/jem.182.2.367 · Cited by 1,567
Self-citation
Organelle-specific initiation of cell death pathways
Ferri, K. F., & Kroemer, G. (2001) · Nature Cell Biology · doi:10.1038/ncb1101-e255 · Cited by 1,455
Self-citation
Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis
Gross, A., Jockel, J., Wei, M. C., & Korsmeyer, S. J. (1998) · The EMBO Journal · doi:10.1093/emboj/17.14.3878 · Cited by 1,095
Mitochondrio‐nuclear translocation of AIF in apoptosis and necrosis
Daugas, É., Susín, S. A., Zamzami, N., Ferri, K. F., Irinopoulou, T., Larochette, N., Prévost, M., Leber, B. F., Andrews, D. W., Penninger, J. M., et al. (2000) · The FASEB Journal · doi:10.1096/fasebj.14.5.729 · Cited by 777
Self-citation

Show all 50 references

Research works printed but not linked: 1

Boya P, Andreau K, Poncet D, Zamzami N, Perfettini JL, Metivier D, Ojcius DM, Jäättelä M and Kroemer G . (in press).

Sorted by citations

Items 201–300 of 384

Quinacrine-Induced Autophagy in Ovarian Cancer Triggers Cathepsin-L Mediated Lysosomal/Mitochondrial Membrane Permeabilization and Cell Death
Thirusangu, P., Pathoulas, C. L., Ray, U., Xiao, Y., Staub, J. K., Jin, L., Khurana, A., & Shridhar, V. (2021) · Cancers · doi:10.3390/cancers13092004 · Cited by 35
RETRACTED: Environmental impacts of COVID-19 treatment: Toxicological evaluation of azithromycin and hydroxychloroquine in adult zebrafish
Mendonça-Gomes, J. M., Araújo, A. P. D. C., da Luz, T. M., Charlie‐Silva, I., Braz, H. L. B., Jorge, R. J. B., Ahmed, M. A. I., Nóbrega, R. H., Vogel, C. F. A., & Malafaia, G. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.148129 · Cited by 35
Retracted
Redox sensitive nano-capsules self-assembled from hyaluronic acid-hydroxychloroquine conjugates for CD44-targeted delivery of hydroxychloroquine to combat breast cancer metastasis in vitro and in vivo
He, Y., Xu, Y., Huang, Y., Quang, H., Xia, X., Zhao, H., Xiao, Y., Lu, W. P., & Yu, J. (2021) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2021.112249 · Cited by 36
Calcium signaling in lysosome-dependent cell death
Milani, M., Pihán, P., & Hetz, C. A. (2023) · Cell Calcium · doi:10.1016/j.ceca.2023.102751 · Cited by 34
Icariside II-induced mitochondrion and lysosome mediated apoptosis is counterbalanced by an autophagic salvage response in hepatoblastoma
Geng, Y., Zhang, C., Shi, Y., Xia, Y., Guo, C., Yang, L., & Kong, L. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.05.032 · Cited by 34
Palladacycle (BPC) antitumour activity against resistant and metastatic cell lines: The relationship with cytosolic calcium mobilisation and cathepsin B activity
Bechara, A., Barbosa, C. M. V., Paredes‐Gamero, E. J., Garcia, D. M., Silva, L. S., Matsuo, A. L., Nascimento, F. D., Rodrigues, E. G., Caires, A. C. F., Smaili, S. S., et al. (2014) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2014.03.073 · Cited by 34
Lysosomal and mitochondrial permeabilization mediates zinc(II) cationic phthalocyanine phototoxicity
Marino, J., Vior, M. C. G., Furmento, V. A., Blank, V. C., Awruch, J., & Roguin, L. P. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.08.012 · Cited by 34
Arsenic induces apoptosis by the lysosomal‐mitochondrial pathway in INS‐1 cells
Pan, X., Jiang, L., Zhong, L., Geng, C., Li, J., Liu, S., Guan, H., Yang, G., Yao, X., Piao, F., et al. (2014) · Environmental Toxicology · doi:10.1002/tox.22027 · Cited by 34
Chloroquine- and Hydroxychloroquine–Induced Cardiomyopathy: A Case Report and Brief Literature Review
Nadeem, U., Raafey, M., Kim, G. H., Treger, J., Pytel, P., Husain, A. N., & Schulte, J. J. (2020) · American Journal of Clinical Pathology · doi:10.1093/ajcp/aqaa253 · Cited by 34
A role for p53 in the β-amyloid-mediated regulation of the lysosomal system
Fogarty, M. P., McCormack, R. M., Noonan, J., Murphy, D. B., Gowran, A., & Campbell, V. A. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.09.018 · Cited by 35
A ROS-mediated lysosomal–mitochondrial pathway is induced by ginsenoside Rh2 in hepatoma HepG2 cells
Chen, F., Deng, Z., Xiong, Z.-X., Zhang, B., Yang, J., & Hu, J. (2015) · Food & Function · doi:10.1039/c5fo00518c · Cited by 33
Amitriptyline induces mitophagy that precedes apoptosis in human HepG2 cells
Paz, M. V., Cordero, M. D., Pavón, A. D., Castejón‐Vega, B., Cotán, D., de la Mata, M., Oropesa-Ávila, M., Alcocer‐Gómez, E., de Lavera, I., Garrido‐Maraver, J., et al. (2016) · Genes & Cancer · doi:10.18632/genesandcancer.114 · Cited by 31
A new lactoferrin- and iron-dependent lysosomal death pathway is induced by benzo[a]pyrene in hepatic epithelial cells
Gorria, M., Tekpli, X., Rissel, M., Sergent, O., Laurence Therese, H. U. C., Landvik, N. E., Fardel, O., Dimanche‐Boitrel, M., Holme, J. A., & Lagadic‐Gossmann, D. (2008) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2007.12.021 · Cited by 35
Chloroquine upregulates TRAIL/TRAILR2 expression and potentiates doxorubicin anti-tumor activity in thioacetamide-induced hepatocellular carcinoma model
Helmy, S. A., El‐Mesery, M., El-Karef, A. A., Eissa, L. A., & Gayar, A. M. E. (2017) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2017.11.009 · Cited by 32
Imiquimod-induced ROS production causes lysosomal membrane permeabilization and activates caspase-8-mediated apoptosis in skin cancer cells
Chang, S.-H., Lin, P.-Y., Wu, T.-K., Hsu, C., Huang, S., Li, Z., Liu, K.-T., Kao, J., Chen, Y., Wong, T., et al. (2022) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2022.08.006 · Cited by 31
Comparative analysis of cell death mechanisms induced by lysosomal autophagy inhibitors
Stamenkovic, M., Janjetović, K., Paunović, V., Ćirić, D., Kravic‐Stevovic, T., & Trajković, V. (2019) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2019.172540 · Cited by 31
Pre-clinical antitumour evaluation of Biphosphinic Palladacycle Complex in human leukaemia cells
Oliveira, C. R., Barbosa, C. M. V., Nascimento, F. D., Lanetzki, C. S., Meneghin, M. B. L., Pereira, F. E. G., Paredes‐Gamero, E. J., Ferreira, A. T., Rodrigues, T., Queiroz, M. L. S., et al. (2008) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2008.10.034 · Cited by 31
Elucidation of remdesivir cytotoxicity pathways through genome-wide CRISPR-Cas9 screening and transcriptomicsPreprint
Akıncı, E., Cha, M., Lin, L., Yeo, G. H. T., Hamilton, M. C., Donahue, C. J., Bermudez-Cabrera, H. C., Zanetti, L. C., Chen, M., Barkal, S. A., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.27.270819 · Cited by 32
A ROS-mediated lysosomal–mitochondrial pathway is induced by a novel Amonafide analogue, 7c, in human Hela cervix carcinoma cells
Shen, K., Sun, L., Zhang, H., Xu, Y. F., Qian, X. H., Lü, Y., Li, Q., Ni, L., & Liu, J. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.01.038 · Cited by 30
Autophagic and Apoptotic Cell Death in Amniotic Epithelial Cells
Shen, Z., Li, E.-M., Lu, S.-Q., Shen, J., Cai, Y.-M., Wu, Y.-E., Zheng, R.-T., Tan, L.-J., & Xu, L.-Y. (2008) · Placenta · doi:10.1016/j.placenta.2008.09.001 · Cited by 30
Chemical principles for the design of a novel fluorescent probe with high cancer-targeting selectivity and sensitivity
Kang, C., Huang, W.-C., Kouh, C.-W., Wang, Z.-F., Cho, C., Chang, C., Wang, C., Chang, T., Seemann, J., & Huang, L. J.-S. (2013) · Integrative Biology · doi:10.1039/c3ib40058a · Cited by 29
Lysosome Membrane Permeabilization and Disruption of the Molecular Target of Rapamycin (mTOR)-Lysosome Interaction Are Associated with the Inhibition of Lung Cancer Cell Proliferation by a Chloroquinoline Analog
Sironi, J., Aranda, E., Nordstrøm, L. U., & Schwartz, E. L. (2018) · Molecular Pharmacology · doi:10.1124/mol.118.113118 · Cited by 29
Neoadjuvant administration of hydroxychloroquine in a phase 1 clinical trial induced plasma Par-4 levels and apoptosis in diverse tumors
Wang, P., Burikhanov, R., Jayswal, R. D., Weiss, H. L., Arnold, S. M., Villano, J. L., & Rangnekar, V. M. (2018) · Genes & Cancer · doi:10.18632/genesandcancer.181 · Cited by 29
Repurposing Chloroquine Against Multiple Diseases With Special Attention to SARS-CoV-2 and Associated Toxicity
Kamat, S., & Kumari, M. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.576093 · Cited by 29
Complex Interplay between Autophagy and Oxidative Stress in the Development of Endometriosis
D’Amico, R., Impellizzeri, D., Cordaro, M., Siracusa, R., Interdonato, L., Marino, Y., Crupi, R., Gugliandolo, E., Macrı̀, F., Paola, D. D., et al. (2022) · Antioxidants · doi:10.3390/antiox11122484 · Cited by 30
Chymotrypsin B Cached in Rat Liver Lysosomes and Involved in Apoptotic Regulation through a Mitochondrial Pathway
Miao, Q., Sun, Y., Wei, T., Zhao, X., Zhao, K., Yan, L., Zhang, X., Shu, H., & Yang, F. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m709789200 · Cited by 29
Eucommia ulmoides Cortex, Geniposide and Aucubin Regulate Lipotoxicity through the Inhibition of Lysosomal BAX
Lee, G., Lee, M. R., Lee, H. Y., Kim, S. H., Kim, H.-K., Kim, H., & Chae, H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088017 · Cited by 30
Retracted
Inhibition of endo-lysosomal function exacerbates vascular calcification
Cai, Y., Wang, X., Flores, A. M., Lin, T., & Guzman, R. J. (2018) · Scientific Reports · doi:10.1038/s41598-017-17540-6 · Cited by 29
The biphosphinic paladacycle complex induces melanoma cell death through lysosomal–mitochondrial axis modulation and impaired autophagy
Gigli, R. D., Pereira, G. J. S., Antunes, F., Bechara, A., Garcia, D. M., Spíndola, D. G., Jasiulionis, M. G., Caires, A. C. F., Smaili, S. S., & Bincoletto, C. (2015) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2015.11.008 · Cited by 29
Molecular Mechanisms of Chloroquine and Hydroxychloroquine Used in Cancer Therapy
Sanctis, J. B. D., Charris, J., Blanco, Z., Ramírez, H., Martinez, G. P., & Mijares, M. R. (2022) · Anti-Cancer Agents in Medicinal Chemistry · doi:10.2174/1871520622666220519102948 · Cited by 31
Doxorubicin-induced cell death requires cathepsin B in HeLa cells
Bien, S., Rimmbach, C., Neumann, H., Niessen, J., Reimer, E. N., Ritter, C. A., Rosskopf, D., Činátl, J., Michaelis, M., Schroeder, H. W. S., et al. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.07.036 · Cited by 28
Phototoxic effects of lysosome-associated genetically encoded photosensitizer KillerRed
Serebrovskaya, E. O., Ryumina, A. P., Boulina, M. E., Shirmanova, M. V., Вадимовна, З. Е., Bogdanova, E., Lukyanov, S., & Lukyanov, K. A. (2013) · Journal of Biomedical Optics · doi:10.1117/1.jbo.19.7.071403 · Cited by 28
Effect of hydroxychloroquine on oxidative/nitrosative status and angiogenesis in endothelial cells under high glucose condition
Rezabakhsh, A., Montazersaheb, S., Nabat, E., Hassanpour, M., Montaseri, A., Malekinejad, H., Movassaghpour, A. A., Rahbarghazi‬, R., & Garjani, A. (2017) · Bioimpacts · doi:10.15171/bi.2017.26 · Cited by 29
The combination of temsirolimus and chloroquine increases radiosensitivity in colorectal cancer cells
Shiratori, H., Kawai, K., Hata, K., Tanaka, T., Nishikawa, T., Otani, K., Sasaki, K., Kaneko, M., Murono, K., Emoto, S., et al. (2019) · Oncology Reports · doi:10.3892/or.2019.7134 · Cited by 28
Association between autophagy and acute pancreatitis
Zhang, T., Gan, Y., & Zhu, S. (2023) · Frontiers in Genetics · doi:10.3389/fgene.2023.998035 · Cited by 27
Trans10, cis12-conjugated linoleic acid induces mitochondria-related apoptosis and lysosomal destabilization in rat hepatoma cells
Yamasaki, M., Miyamoto, Y., Chujo, H., Nishiyama, K., Tachibana, H., & Yamada, K. (2005) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2005.05.010 · Cited by 27
CA-074Me, a cathepsin B inhibitor, decreases APP accumulation and protects primary rat cortical neurons treated with okadaic acid
Cho, K., Yoon, S. Y., Choi, J. E., Kang, H. J., Jang, H. Y., & Kim, D. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.05.056 · Cited by 27
Nicardipine sensitizes temozolomide by inhibiting autophagy and promoting cell apoptosis in glioma stem cells
Shi, J. H., Dong, X., Li, H., Wang, H., Jiang, Q., Liu, L., Wang, L., & Dong, J. (2021) · Aging · doi:10.18632/aging.202539 · Cited by 26
Engaging the Lysosome and Lysosome-Dependent Cell Death in Cancer
Berg, A. L., Rowson-Hodel, A. R., Wheeler, M. R., Hu, M., Free, S. R., & Carraway, K. L. (2022) · Exon Publications eBooks · doi:10.36255/exon-publications-breast-cancer-lysosome · Cited by 26
Hydroxychloroquine: Key therapeutic advances and emerging nanotechnological landscape for cancer mitigation
Low, L. E., Kong, C. K., Yap, W.-H., Siva, S. P., Gan, S. H., Siew, W. S., Ming, L. C., Lai‐Foenander, A. S., Chang, S. K., Lee, W.-L., et al. (2023) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2023.110750 · Cited by 29
Aspirin Eugenol Ester Reduces H2O2-Induced Oxidative Stress of HUVECs via Mitochondria-Lysosome Axis
Huang, M., Yang, Y., Liu, X.-W., Qin, Z., & Li, J. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/8098135 · Cited by 26
Hydroxychloroquine suppresses lung tumorigenesis via inducing FoxO3a nuclear translocation through STAT3 inactivation
Lyu, X., Zeng, L., Zhang, H., Ke, Y., Liu, X., Zhao, N., Yuan, J., Chen, G., & Yang, S. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117366 · Cited by 25
A Novel Role for α-Tocopherol Transfer Protein (α-TTP) in Protecting against Chloroquine Toxicity
Shichiri, M., Kono, N., Shimanaka, Y., Tanito, M., Rotzoll, D., Yoshida, Y., Hagihara, Y., Tamai, H., & Arai, H. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.321281 · Cited by 26
Ammonia-triggered apoptosis via immune function and metabolic process in the thymuses of chickens by proteomics analysis
Chen, D., Hu, G., Zhang, S., Zhang, H., & Teng, X. (2020) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2020.110619 · Cited by 25
Lysosomotropic compounds and spermine enzymatic oxidation products in cancer therapy (Review)
Agostinelli, E., & Seiler, N. (2007) · International Journal of Oncology · doi:10.3892/ijo.31.3.473 · Cited by 25
Endosomal disruptors in non-viral gene delivery
Minchin, R. F., & Yang, S. (2010) · Expert Opinion on Drug Delivery · doi:10.1517/17425240903512931 · Cited by 25
Secretome of Human Bronchial Epithelial Cells in Response to the Fungal Pathogen Aspergillus fumigatus Analyzed by Differential In-Gel Electrophoresis
Fekkar, A., Balloy, V., Pionneau, C., Marinach, C., Chignard, M., & Mazier, D. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jis031 · Cited by 25
Role of lysosomes in cancer therapy
Halaby, R. (2015) · Research and Reports in Biology · doi:10.2147/rrb.s83999 · Cited by 25
Hydroxychloroquine antiparkinsonian potential: Nurr1 modulation versus autophagy inhibition
Hedya, S. A., Safar, M. M., & Bahgat, A. K. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.02.033 · Cited by 25
Inhibitors of cathepsins B and L induce autophagy and cell death in neuroblastoma cells
Cartledge, D. M., Colella, R., Glazewski, L., Lu, G., & Mason, R. W. (2012) · Investigational New Drugs · doi:10.1007/s10637-012-9826-6 · Cited by 26
Aberrant PTEN expression in response to progesterone reduces endometriotic stromal cell apoptosis
Choi, J., Jo, M., Lee, E., Hwang, S., & Choi, D. (2016) · Reproduction · doi:10.1530/rep-16-0322 · Cited by 23
Photosensitized mefloquine induces ROS-mediated DNA damage and apoptosis in keratinocytes under ambient UVB and sunlight exposure
Yadav, N., Dwivedi, A., Mujtaba, S. F., Verma, A., Chaturvedi, R., Ray, R. S., & Singh, G. (2014) · Cell Biology and Toxicology · doi:10.1007/s10565-014-9280-7 · Cited by 26
Anesthetic propofol overdose causes endothelial cytotoxicity in vitro and endothelial barrier dysfunction in vivo
Lin, M.-C., Chen, C., Yang, T.-T., Choi, P.-C., Hsing, C., & Lin, C. (2012) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2012.08.013 · Cited by 23
Dietary canolol induces apoptosis in human cervical carcinoma HeLa cells through ROS-MAPK mediated mitochondrial signaling pathway: In vitro and in vivo
Xia, X., Xiang, X., Huang, F., Zheng, M., Zhang, Z., & Han, L. (2019) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2019.01.016 · Cited by 25
Lysosomal chymotrypsin B potentiates apoptosis via cleavage of Bid
Zhao, K., Zhao, X., Tu, Y., Miao, Q., Cao, D., Duan, W., Sun, Y., Wang, J., Wei, T., & Yang, F. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0356-0 · Cited by 23
Autophagic Degeneration of Motor Neurons in a Model of Slow Glutamate Excitotoxicity in Vitro
Matyja, E., Taraszewska, A., Nagańska, E., & Rafałowska, J. (2005) · Ultrastructural Pathology · doi:10.1080/01913120500214333 · Cited by 23
Genetic Aberrations Associated with Photodynamic Therapy in Colorectal Cancer Cells
Abrahamse, H., & Houreld, N. N. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20133254 · Cited by 22
Targeting the Inside of Cells with Biologicals: Chemicals as a Delivery Strategy
Marschall, A. L. J. (2021) · BioDrugs · doi:10.1007/s40259-021-00500-y · Cited by 22
Dynamic interplay between autophagic flux and A kt during melanoma progression in vitro
Maes, H., Martín-Acebes, M. A., Verfaillie, T., & Agostinis, P. (2013) · Experimental Dermatology · doi:10.1111/exd.12298 · Cited by 21
Organ damage in high-risk patients with systemic and incomplete lupus syndromes
Olsen, N. J., Yousif, M., Mutwally, A., Cory, M. J., Elmagboul, N., & Karp, D. R. (2013) · Rheumatology International · doi:10.1007/s00296-013-2783-3 · Cited by 21
Prevention of crystalline silica-induced inflammation by the anti-malarial hydroxychloroquine
Burmeister, R., Rhoderick, J. F., & Holian, A. (2019) · Inhalation Toxicology · doi:10.1080/08958378.2019.1668091 · Cited by 21
Visual neurophysiological dysfunction in infants exposed to hydroxychloroquine in utero
Renault, F., Flores‐Guevara, R., Renaud, C., Richard, P., Vermersch, A., & Gold, F. (2009) · Acta Paediatrica · doi:10.1111/j.1651-2227.2009.01379.x · Cited by 21
N-Substituted 4-Aminobenzamides (Procainamide Analogs): An Assessment of Multiple Cellular Effects Concerning Ion Trapping
Morissette, G., Moreau, E., Gaudreault, R. C., & Marceau, F. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.016527 · Cited by 21
Autophagy–Lysosome Pathway Dysfunction in Neurodegeneration and Cancer: Mechanisms and Therapeutic Opportunities
Du, M., Yu, Y., Wang, J., & Ji, C. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms27010366 · Cited by 22
Restriction of extracellular lipids renders pancreatic cancer dependent on autophagy
Saliakoura, M., Sebastiano, M. R., Nikdima, I., Pozzato, C., & Konstantinidou, G. (2022) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-02231-y · Cited by 21
Measurement of Autophagy by Flow Cytometry
Warnes, G. (2014) · Current Protocols in Cytometry · doi:10.1002/0471142956.cy0945s68 · Cited by 20
Emerging Therapeutic Strategies for Overcoming Proteasome Inhibitor Resistance
Dolloff, N. G. (2015) · Advances in cancer research · doi:10.1016/bs.acr.2015.03.002 · Cited by 20
MicroRNAs-103/107 Regulate Autophagy in the Epidermis
Wang, S., Kobeissi, A. M., Dong, Y., Kaplan, N., Yang, W., He, C., Zeng, K., & Peng, H. (2018) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2018.02.002 · Cited by 21
Accumulation of A2-E in mitochondrial membranes of cultured RPE cells
Schütt, F., Bergmann, M., Holz, F. G., Dithmar, S., Völcker, H.-E., & Kopitz, J. (2006) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-006-0376-5 · Cited by 20
A red-light-activated sulfonamide porphycene for highly efficient photodynamic therapy against hypoxic tumor
Wang, Y., Pan, Z., Cheng, X., Zhang, K., Zhang, X., Qin, Y., Fan, J., Yan, T., Han, T., Shiu, K., et al. (2020) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2020.112867 · Cited by 19
Aminoquinolines as Translational Models for Drug Repurposing: Anticancer Adjuvant Properties and Toxicokinetic-Related Features
Ferreira, P. M. P., Ferreira, J. R. D. O., de Sousa, R. W. R., Bezerra, D. P., & Militão, G. C. G. (2021) · Journal of Oncology · doi:10.1155/2021/3569349 · Cited by 19
Biologic Functions of Hydroxychloroquine in Disease: From COVID-19 to Cancer
Niemann, B. R., Puleo, A., Stout, C., Markel, J., & Boone, B. A. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14122551 · Cited by 19
Synergistic Anticancer Action of Lysosomal Membrane Permeabilization and Glycolysis Inhibition
Kosić, M., Arsikin, K. M., Paunović, V., Firestone, R. A., Ristic, B. Z., Mirčić, A., Petricevic, S. M., Bošnjak, M., Zogovic, N. S., Mandić, M., et al. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.752113 · Cited by 18
Triarylpyridine Compounds and Chloroquine Act in Concert to Trigger Lysosomal Membrane Permeabilization and Cell Death in Cancer Cells
Beauvarlet, J., Das, R. N., Alvarez-Valadez, K., Martins, I., Müller, A., Darbo, É., Richard, É., Soubeyran, P., Kroemer, G., Guillon, J., et al. (2020) · Cancers · doi:10.3390/cancers12061621 · Cited by 18
Self-citation
Molecular Networking for Drug Toxicities Studies: The Case of Hydroxychloroquine in COVID-19 Patients
Ferron, P., Daré, B. L., Bronsard, J., Steichen, C., Babina, E., Pelletier, R., Hauet, T., Morel, I., Tarte, K., Reizine, F., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010082 · Cited by 18
Protective Effects of a Synthesized Butyrolactone Derivative against Chloroquine-Induced Autophagic Vesicle Accumulation and the Disturbance of Mitochondrial Membrane Potential and Na+,K+-ATPase Activity in Vascular Endothelial Cells
Huang, B., Meng, N., Zhao, B., Zhao, J., Zhang, Y. L., Zhang, S., & Miao, J. (2009) · Chemical Research in Toxicology · doi:10.1021/tx8002824 · Cited by 18
Zaprinast inhibits hydrogen peroxide-induced lysosomal destabilization and cell death in astrocytes
Choi, J.-H., Kim, D. H., Yun, I.-J., Chang, J.-H., Chun, B., & Choi, S.-H. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.06.042 · Cited by 17
Imatinib disturbs lysosomal function and morphology and impairs the activity of mTORC1 in human hepatocyte cell lines
Roos, N. J., Mancuso, R. V., Sanvee, G. M., Bouitbir, J., & Krähenbühl, S. (2022) · Food and Chemical Toxicology · doi:10.1016/j.fct.2022.112869 · Cited by 16
In-Depth Characterization of Endo-Lysosomal Aβ in Intact Neurons
McKendell, A. K., Houser, M. C., Mitchell, S. P. C., Wolfe, M. S., Berezovska, O., & Maesako, M. (2022) · Biosensors · doi:10.3390/bios12080663 · Cited by 15
Hypothesis links emergence of chloroquine-resistant malaria and other intracellular pathogens and suggests a new strategy for treatment of diseases caused by intracellular parasites
Parris, G. E. (2004) · Medical Hypotheses · doi:10.1016/j.mehy.2003.12.004 · Cited by 16
Hydroxychloroquine decreases human MSC ‐derived osteoblast differentiation and mineralization in vitro
Both, T., van de Peppel, J., Zillikens, M. C., Koedam, M., van Leeuwen, J. P. T. M., van Hagen, P. M., van Daele, P. L. A., & van der Eerden, B. C. J. (2017) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13373 · Cited by 16
Hypersensitivity of mtDNA-depleted cells to staurosporine-induced apoptosis: roles of Bcl-2 downregulation and cathepsin B
Rommelaere, G., Michel, S., Mercy, L., Fattaccioli, A., Demazy, C., Ninane, N., Houbion, A., Renard, P., & Arnould, T. (2010) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00037.2010 · Cited by 15
pH-Triggered burst intracellular release from hollow microspheres to induce autophagic cancer cell death
Liang, X., Yang, Y., Wang, L., Zhu, X., Zeng, X., Wu, X., Chen, H., Zhang, X., & Mei, L. (2015) · Journal of Materials Chemistry B · doi:10.1039/c5tb00328h · Cited by 15
Lysosomal permeabilization and endoplasmic reticulum stress mediate the apoptotic response induced after photoactivation of a lipophilic zinc(II) phthalocyanine
Chiarante, N., Vior, M. C. G., Rey, O., Marino, J., & Roguin, L. P. (2018) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2018.08.009 · Cited by 15
Upregulation of DR5 and Downregulation of Survivin by IITZ-01, Lysosomotropic Autophagy Inhibitor, Potentiates TRAIL-Mediated Apoptosis in Renal Cancer Cells via Ubiquitin-Proteasome Pathway
Shahriyar, S. A., Seo, S. U., Min, K., Kubatka, P., Min, D. S., Chang, J., Kim, D., Woo, S. M., & Kwon, T. K. (2020) · Cancers · doi:10.3390/cancers12092363 · Cited by 16
The cross-talk of autophagy and apoptosis in breast carcinoma: implications for novel therapies?
Seyrek, K., Wohlfromm, F., Espe, J., & Lavrik, I. N. (2022) · Biochemical Journal · doi:10.1042/bcj20210676 · Cited by 15
Multiple cell death pathways are independently activated by lethal hypertonicity in renal epithelial cells.
Choi, S., Lee‐Kwon, W., Lee, H. H., Lee, J.-H., Sanada, S., & Kwon, H. (2013) · American Journal of Physiology - Cell Physiology · doi:10.1152/ajpcell.00384.2012 · Cited by 15
Para-toluenesulfonamide induces tongue squamous cell carcinoma cell death through disturbing lysosomal stability
Liu, Z., Liang, C., Zhang, Z., Pan, J., Xia, H., Zhong, N., & Li, L. (2015) · Anti-Cancer Drugs · doi:10.1097/cad.0000000000000283 · Cited by 14
Signaling of Chloroquine-Induced Stress in the Yeast Saccharomyces cerevisiae Requires the Hog1 and Slt2 Mitogen-Activated Protein Kinase Pathways
Baranwal, S., Azad, G. K., Singh, V., & Tomar, R. S. (2014) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02393-13 · Cited by 16
ABT-737, a Bcl-2 Selective Inhibitor, and Chloroquine Synergistically Kill Renal Cancer Cells
Yin, P., Jia, J.-P., Li, J., Song, Y., Zhang, Y., & Chen, F. (2016) · Oncology Research Featuring Preclinical and Clinical Cancer Therapeutics · doi:10.3727/096504016x14587366983838 · Cited by 14
Detection of DNA Damage, Molecular Apoptosis and Production of Home-Made Ladder by Using Simple Techniques
El-, S. E. H., & Elhassanee, Y. A. (2008) · Biotechnology(Faisalabad) · doi:10.3923/biotech.2008.514.522 · Cited by 13
Processing and MHC class II presentation of exogenous soluble antigen involving a proteasome‐dependent cytosolic pathway in CD40‐activated B cells
Becker, H., Kondo, E., Shimabukuro-Vornhagen, A., Theurich, S., & von Bergwelt-Baildon, M. (2016) · European Journal of Haematology · doi:10.1111/ejh.12699 · Cited by 14
Recent Information on the Pathogenesis and Treatment of Hypoxic-Ischemic Brain Lesions in Newborns
Karkashadze, G. A., Владимирович, А. А., Павловна, З. Е., Davydova, I. V., Каримова, Х. М., Zakharyan, M. E., Namazova-Baranova, L. S., Маслова, О. И., Yatsyk, G. V., Valieva, S. I., et al. (2016) · Педиатрическая фармакология · doi:10.15690/pf.v13i5.1641 · Cited by 13
Molecular mechanisms of interplay between autophagy and metabolism in cancer
Raj, S., Chandel, V., Kumar, A. J., Kesari, K. K., Asthana, S., Ruokolainen, J., Kamal, M. A., & Kumar, D. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.118184 · Cited by 14
Inhibitory effect of chloroquine on bone resorption reveals the key role of lysosomes in osteoclast differentiation and function
Al‐Bari, M. A. A., Shinohara, M., Nagai, Y., & Takayanagi, H. (2012) · Inflammation and Regeneration · doi:10.2492/inflammregen.32.222 · Cited by 12
Pancreatic adenocarcinoma: molecular drivers and the role of targeted therapy
Al-Share, B. A., Hammad, N., & Diab, M. (2021) · Cancer and Metastasis Reviews · doi:10.1007/s10555-020-09948-w · Cited by 12
Nanotoxicity of multifunctional stoichiometric cobalt oxide nanoparticles (SCoONPs) with repercussions toward apoptosis, necrosis, and cancer necrosis factor (TNF-α) at nano-biointerfaces
Kumar, R., Chhikara, B. S., Zeybekler, S. E., Gupta, D., Kaur, G., Chhillar, M., Aggarwal, A. K., & Rahdar, A. (2023) · Toxicology Research · doi:10.1093/toxres/tfad086 · Cited by 11
Simple dose-escalation regimen for hydroxychloroquine-induced hypersensitivity reaction in patients with systemic lupus erythematosus enabled treatment resumption
Takamasu, E., Yokogawa, N., Shimada, K., & Sugii, S. (2019) · Lupus · doi:10.1177/0961203319879987 · Cited by 11
Autophagy, Senescence, and Apoptosis
Goehe, R. W., Bristol, M. L., Wilson, E. N., & Gewirtz, D. A. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-236-0_3 · Cited by 11
Organic Nanoparticle–Carbon Dots Conjugate for Multimodal Cancer Therapy
Ghosh, A. K., Roy, K., & Das, P. K. (2024) · ACS Applied Nano Materials · doi:10.1021/acsanm.3c05730 · Cited by 10

Authors: Boya, P., Gonzalez-Polo, R.-A., Poncet, D., Andreau, K., Vieira, H. L., Roumier, T., Perfettini, J.-L., & Kroemer, G.
Affiliations: Centre National de la Recherche Scientifique (FR)
Corresponding author: Kroemer, Guido
ORCID: Boya, Patricia
Poncet, Delphine
Vieira, Helena LA
Perfettini, Jean-Luc
Kroemer, Guido
Venue: Oncogene
Publisher: Springer Science and Business Media LLC
Published: 2003-06-17
Volume: 22
Issue: 25
Pages: 3927-3936
ISSN: 0950-9232 (ISSN-L)
1476-5594
DOI: 10.1038/sj.onc.1206622
OpenAlex: W2073788301
Cited by: 385
References: 50
Citations by year: 2026: 2 · 2025: 4 · 2024: 16 · 2023: 7 · 2022: 17 · 2021: 19 · 2020: 23 · 2019: 19 · 2018: 25 · 2017: 15 · 2016: 20 · 2015: 26 · 2014: 11 · 2013: 26 · 2012: 19
FWCI: 4.94
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Oncogene (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Keywords: hydroxychloroquine, lysosomal membrane permeabilization, mitochondrial membrane permeabilization, Bax, Bak, cytochrome c release, caspase activation, Bcl-xL, Bcl-2, mitochondrial membrane potential, mouse embryonic fibroblasts
MeSH terms: Amino Acid Chloromethyl Ketones, Animals, Anti-Bacterial Agents, Cell Line, Enzyme Activation, HeLa Cells, Humans, Hydroxychloroquine, Intracellular Membranes, Lysosomes, Membrane Proteins, Mitochondria, Permeability, Proto-Oncogene Proteins, Recombinant Fusion Proteins, Transfection, Signal Transduction, Cysteine Proteinase Inhibitors, Apoptosis, Mice, Knockout, Macrolides, Jurkat Cells, Proto-Oncogene Proteins c-bcl-2, Genes, bcl-2, Caspases, bcl-2 Homologous Antagonist-Killer Protein, bcl-X Protein, bcl-2-Associated X Protein, Mice, Rats

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

Mitochondrial membrane permeabilization is a critical step of lysosome-initiated apoptosis induced by hydroxychloroquine

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks