Paraptosis and Other Types of Non-Apoptotic Regulated Cell Death
- Authors: Solovieva M.E1, Shatalin Y.V1, Akatov V.S1
-
Affiliations:
- Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences
- Issue: Vol 69, No 4 (2024)
- Pages: 786-804
- Section: Cell biophysics
- URL: https://rjonco.com/0006-3029/article/view/675887
- DOI: https://doi.org/10.31857/S0006302924040117
- EDN: https://elibrary.ru/NGKZQR
- ID: 675887
Cite item
Abstract
The review is devoted to modern ideas about paraptosis, as one of the types of regulated cell death, in comparison with other types of cell death. Paraptosis is a form of cell death caused by endoplasmic reticulum stress, accompanied by an accumulation of damaged or misfolded proteins, extensive non-autophagic vacuolation of cisterns of endoplasmic reticulum and, in some cases, mitochondria, with subsequent damage to mitochondria, the cytoskeleton, and cell death. The knowledge regarding the molecular mechanisms of paraptosis is of interest for the treatment of cancers resistant to apoptosis-inducing agents.
Keywords
About the authors
M. E Solovieva
Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences
Email: m_solovieva@iteb.ru
Pushchino, Russia
Yu. V Shatalin
Institute of Theoretical and Experimental Biophysics, Russian Academy of SciencesPushchino, Russia
V. S Akatov
Institute of Theoretical and Experimental Biophysics, Russian Academy of SciencesPushchino, Russia
References
- Majno G. and Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am. J. Pathol., 146 (1), 3–15 (1995).
- Levin S., Bucci T. J., Cohen S. M., Fix A. S., Hardisty J. F., LeGrand E. K., Maronpot R. R., and Trump B. F. The nomenclature of cell death: recommendations of an ad hoc Committee of the Society of Toxicologic Pathologists. Toxicol. Pathol., 27 (4), 484–490 (1999). doi: 10.1177/019262339902700419
- Lee D., Kim I. Y., Saha S. and Choi K. S. Paraptosis in the anti-cancer arsenal of natural products. Pharmacol. Therapeut., 162, 120–133 (2016). doi: 10.1016/j.pharmthera.2016.01.003
- Shubin A. V., Demidyuk I. V., Komissarov A. A., Rafieva L. M. and Kostrov S. V. Cytoplasmic vacuolization in cell death and survival. Oncotarget, 7 (34), 55863–55889 (2016). doi: 10.18632/oncotarget.10150
- Park S. S., Lee D. M., Lim J. H., Lee D., Park S. J., Kim H. M., Sohn S., Yoon G., Eom Y. W., Jeong S. Y., Choi E. K., and Choi K. S. Pyrrolidine dithiocarbamate reverses Bcl-xL-mediated apoptotic resistance to doxorubicin by inducing paraptosis. Carcinogenesis, 39 (3), 458–470 (2018). doi: 10.1093/carcin/bgy003
- Kessel D. Apoptosis, Paraptosis and Autophagy: Death and Survival Pathways Associated with Photodynamic Therapy. Photochem. Photobiol., 95 (1), 119–125 (2019). doi: 10.1111/php.12952
- Fontana F., Raimondi M., Marzagalli M., Di Domizio A., and Limonta P. The emerging role of paraptosis in tumor cell biology: Perspectives for cancer prevention and therapy with natural compounds. Biochim. Biophys. Acta. Rev. Cancer, 1873 (2), 188338 (2020). doi: 10.1016/j.bbcan.2020.188338
- Raimondi M., Fontana F., Marzagalli M., Audano M., Beretta G., Procacci P., Sartori P., Mitro N., and Limonta P. Ca(2+) overload- and ROS-associated mitochondrial dysfunction contributes to δ-tocotrienolmediated paraptosis in melanoma cells. Apoptosis, 26 (5–6), 277–292 (2021). doi: 10.1007/s10495-021-01668-y
- Li G.-N., Zhao X.-J., Wang Z., Luo M.-S., Shi S.-N., Yan D.-M., Li H.-Y., Liu J.-H., Yang Y., Tan J.-H., Zhang Z.-Y., Chen R.-Q., Lai H.-L., Huang X.-Y., Zhou J.-F., Ma D., Fang Y., and Gao Q.-L. Elaiophylin triggers paraptosis and preferentially kills ovarian cancer drug-resistant cells by inducing MAPK hyperactivation. Signal Transduc. Target. Ther., 7 (1), 317 (2022). doi: 10.1038/s41392-022-01131-7
- Wang X., Hua P., He C., and Chen M. Non-apoptotic cell death-based cancer therapy: Molecular mechanism, pharmacological modulators, and nanomedicine. Acta Pharm. Sin. B, 12 (9), 3567–3593 (2022). doi: 10.1016/j.apsb.2022.03.020
- Monel B., Compton A. A., Bruel T., Amraoui S., BurlaudGaillard J., Roy N., Guivel-Benhassine F., Porrot F., Genin P., Meertens L., Sinigaglia L., Jouvenet N., Weil R., Casartelli N., Demangel C., SimonLoriere E., Moris A., Roingeard P., Amara A., and Schwartz O. Zika virus induces massive cytoplasmic vacuolization and paraptosis-like death in infected cells. EMBO J., 36 (12), 1653–1668 (2017). doi: 10.15252/embj.201695597
- Huang X., Huang Y., Yang Y., Wei S., and Qin Q. Involvement of fish signal transducer and activator of transcription 3 (STAT3) in SGIV replication and virus induced paraptosis. Fish Shellfish Immunol., 41 (2), 308–316 (2014). doi: 10.1016/j.fsi.2014.09.011
- Mandula J. K., Chang S., Mohamed E., Jimenez R., Sierra-Mondragon R. A., Chang D. C., Obermayer A. N., Moran-Segura C. M., Das S., Vazquez-Martinez J. A., Prieto K., Chen A., Smalley K. S. M., Czerniecki B., Forsyth P., Koya R. C., Ruffell B., Cubillos-Ruiz J. R., Munn D. H., Shaw T. I., Conejo-Garcia J. R., and Rodriguez P. C. Ablation of the endoplasmic reticulum stress kinase PERK induces paraptosis and type I interferon to promote anti-tumor T cell responses. Cancer Cell, 40 (10), 1145–1160.e1149 (2022). doi: 10.1016/j.ccell.2022.08.016
- Hanson S., Dharan A., P V. J., Pal S., Nair B. G., Kar R., and Mishra N. Paraptosis: a unique cell death mode for targeting cancer. Front. Pharmacol., 14, 1159409 (2023). doi: 10.3389/fphar.2023.1159409
- Kroemer G., El-Deiry W. S., Golstein P., Peter M. E., Vaux D., Vandenabeele P., Zhivotovsky B., Blagosklonny M. V., Malorni W., Knight R. A., Piacentini M., Nagata S., and Melino G. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ., 12 (Suppl. 2), 1463–1467 (2005). doi: 10.1038/sj.cdd.4401724
- Kroemer G., Galluzzi L., Vandenabeele P., Abrams J., Alnemri E. S., Baehrecke E. H., Blagosklonny M. V., El-Deiry W. S., Golstein P., Green D. R., Hengartner M., Knight R. A., Kumar S., Lipton S. A., Malorni W., Nunez G., Peter M. E., Tschopp J., Yuan J., Piacentini M., Zhivotovsky B., and Melino G. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ., 16 (1), 3–11 (2009). doi: 10.1038/cdd.2008.150
- Galluzzi L., Vitale I., Abrams J. M., Alnemri E. S., Baehrecke E. H., Blagosklonny M. V., Dawson T. M., Dawson V. L., El-Deiry W. S., Fulda S., Gottlieb E., Green D. R., Hengartner M. O., Kepp O., Knight R. A., Kumar S., Lipton S. A., Lu X., Madeo F., Malorni W., Mehlen P., Nunez G., Peter M. E., Piacentini M., Rubinsztein D. C., Shi Y., Simon H. U., Vandenabeele P., White E., Yuan J., Zhivotovsky B., Melino G., and Kroemer G. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ., 19 (1), 107–120 (2012). doi: 10.1038/cdd.2011.96
- Galluzzi L., Bravo-San Pedro J. M., Vitale I., Aaronson S. A., Abrams J. M., Adam D., Alnemri E. S., Altucci L., Andrews D., Annicchiarico-Petruzzelli M., Baehrecke E. H., Bazan N. G., Bertrand M. J., Bianchi K., Blagosklonny M. V., Blomgren K., Borner C., Bredesen D. E., Brenner C., Campanella M., Candi E., Cecconi F., Chan F. K., Chandel N. S., Cheng E. H., Chipuk J. E., Cidlowski J. A., Ciechanover A., Dawson T. M., Dawson V. L., De Laurenzi V., De Maria R., Debatin K. M., Di Daniele N., Dixit V. M., Dynlacht B. D., El-Deiry W. S., Fimia G.M., Flavell R. A., Fulda S., Garrido C., Gougeon M. L., Green D. R., Gronemeyer H., Hajnoczky G., Hardwick J. M., Hengartner M. O., Ichijo H., Joseph B., Jost P. J., Kaufmann T., Kepp O., Klionsky D. J., Knight R. A., Kumar S., Lemasters J. J., Levine B., Linkermann A., Lipton S. A., Lockshin R. A., Lopez-Otin C., Lugli E., Madeo F., Malorni W., Marine J. C., Martin S. J., Martinou J. C., Medema J. P., Meier P., Melino S., Mizushima N., Moll U., Munoz-Pinedo C., Nunez G., Oberst A., Panaretakis T., Penninger J. M., Peter M. E., Piacentini M., Pinton P., Prehn J. H., Puthalakath H., Rabinovich G. A., Ravichandran K. S., Rizzuto R., Rodrigues C. M., Rubinsztein D. C., Rudel T., Shi Y., Simon H. U., Stockwell B. R., Szabadkai G., Tait S. W., Tang H. L., Tavernarakis N., Tsujimoto Y., Vanden Berghe T., Vandenabeele P., Villunger A., Wagner E. F., Walczak H., White E., Wood W. G., Yuan J., Zakeri Z., Zhivotovsky B., Melino G., and Kroemer G. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ., 22 (1), 58–73 (2015). doi: 10.1038/cdd.2014.137
- Galluzzi L., Vitale I., Aaronson S. A., Abrams J. M., Adam D., Agostinis P., Alnemri E. S., Altucci L., Amelio I., Andrews D. W., Annicchiarico-Petruzzelli M., Antonov A. V., Arama E., Baehrecke E. H., Barlev N. A., Bazan N. G., Bernassola F., Bertrand M. J. M., Bianchi K., Blagosklonny M. V., Blomgren K., Borner C., Boya P., Brenner C., Campanella M., Candi E., Carmona-Gutierrez D., Cecconi F., Chan F. K., Chandel N. S., Cheng E. H., Chipuk J. E., Cidlowski J. A., Ciechanover A., Cohen G. M., Conrad M., Cubillos-Ruiz J. R., Czabotar P. E., D’Angiolella V., Dawson T. M., Dawson V. L., De Laurenzi V., De Maria R., Debatin K. M., DeBerardinis R. J., Deshmukh M., Di Daniele N., Di Virgilio F., Dixit V. M., Dixon S. J., Duckett C. S., Dynlacht B. D., El-Deiry W. S., Elrod J. W., Fimia G. M., Fulda S., Garcia-Saez A. J., Garg A. D., Garrido C., Gavathiotis E., Golstein P., Gottlieb E., Green D. R., Greene L. A., Gronemeyer H., Gross A., Hajnoczky G., Hardwick J. M., Harris I. S., Hengartner M. O., Hetz C., Ichijo H., Jaattela M., Joseph B., Jost P. J., Juin P. P., Kaiser W. J., Karin M., Kaufmann T., Kepp O., Kimchi A., Kitsis R. N., Klionsky D. J., Knight R. A., Kumar S., Lee S. W., Lemasters J. J., Levine B., Linkermann A., Lipton S. A., Lockshin R. A., Lopez-Otin C., Lowe S. W., Luedde T., Lugli E., MacFarlane M., Madeo F., Malewicz M., Malorni W., Manic G., Marine J. C., Martin S. J., Martinou J. C., Medema J. P., Mehlen P., Meier P., Melino S., Miao E. A., Molkentin J. D., Moll U. M., Munoz-Pinedo C., Nagata S., Nunez G., Oberst A., Oren M., Overholtzer M., Pagano M., Panaretakis T., Pasparakis M., Penninger J. M., Pereira D. M., Pervaiz S., Peter M. E., Piacentini M., Pinton P., Prehn J. H. M., Puthalakath H., Rabinovich G. A., Rehm M., Rizzuto R., Rodrigues C. M. P., Rubinsztein D. C., Rudel T., Ryan K. M., Sayan E., Scorrano L., Shao F., Shi Y., Silke J., Simon H. U., Sistigu A., Stockwell B. R., Strasser A., Szabadkai G., Tait S. W. G., Tang D., Tavernarakis N., Thorburn A., Tsujimoto Y., Turk B., Vanden Berghe T., Vandenabeele P., Vander Heiden M. G., Villunger A., Virgin H. W., Vousden K. H., Vucic D., Wagner E. F., Walczak H., Wallach D., Wang Y., Wells J. A., Wood W., Yuan J., Zakeri Z., Zhivotovsky B., Zitvogel L., Melino G., and Kroemer G. Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ., 25 (3), 486–541 (2018). doi: 10.1038/s41418-017-0012-4
- Song X., Zhu S., Xie Y., Liu J., Sun L., Zeng D., Wang P., Ma X., Kroemer G., Bartlett D. L., Billiar T. R., Lotze M. T., Zeh H. J., Kang R., and Tang D. JTC801 Induces pH-dependent Death Specifically in Cancer Cells and Slows Growth of Tumors in Mice. Gastroenterology, 154 (5), 1480–1493 (2018). doi: 10.1053/j.gastro.2017.12.004
- Tsvetkov P. and Coy S. Copper induces cell death by targeting lipoylated TCA cycle proteins. Science, 375 (6586), 1254–1261 (2022). doi: 10.1126/science.abf0529
- Vitale I., Pietrocola F., Guilbaud E., Aaronson S. A., Abrams J. M., Adam D., Agostini M., Agostinis P., Alnemri E. S., Altucci L., Amelio I., Andrews D. W., Aqeilan R. I., Arama E., Baehrecke E. H., Balachandran S., Bano D., Barlev N. A., Bartek J., Bazan N. G., Becker C., Bernassola F., Bertrand M. J. M., Bianchi M. E., Blagosklonny M. V., Blander J. M., Blandino G., Blomgren K., Borner C., Bortner C. D., Bove P., Boya P., Brenner C., Broz P., Brunner T., Damgaard R. B., Calin G. A., Campanella M., Candi E., Carbone M., Carmona-Gutierrez D., Cecconi F., Chan F. K. M., Chen G.-Q., Chen Q., Chen Y. H., Cheng E. H., Chipuk J. E., Cidlowski J. A., Ciechanover A., Ciliberto G., Conrad M., Cubillos-Ruiz J. R., Czabotar P. E., D’Angiolella V., Daugaard M., Dawson T. M., Dawson V. L., De Maria R., De Strooper B., Debatin K.-M., Deberardinis R. J., Degterev A., Del Sal G., Deshmukh M., Di Virgilio F., Diederich M., Dixon S. J., Dynlacht B. D., El-Deiry W. S., Elrod J. W., Engeland K., Fimia G. M., Galassi C., Ganini C., Garcia-Saez A. J., Garg A. D., Garrido C., Gavathiotis E., Gerlic M., Ghosh S., Green D. R., Greene L. A., Gronemeyer H., Hacker G., Hajnoczky G., Hardwick J. M., Haupt Y., He S., Heery D. M., Hengartner M. O., Hetz C., Hildeman D. A., Ichijo H., Inoue S., Jaattela M., Janic A., Joseph B., Jost P. J., Kanneganti T.-D., Karin M., Kashkar H., Kaufmann T., Kelly G. L., Kepp O., Kimchi A., Kitsis R. N., Klionsky D. J., Kluck R., Krysko D. V., Kulms D., Kumar S., Lavandero S., Lavrik I. N., Lemasters J. J., Liccardi G., Linkermann A., Lipton S. A., Lockshin R. A., Lopez-Otin C., Luedde T., MacFarlane M., Madeo F., Malorni W., Manic G., Mantovani R., Marchi S., Marine J.-C., Martin S. J., Martinou J.-C., Mastroberardino P. G., Medema J. P., Mehlen P., Meier P., Melino G., Melino S., Miao E. A., Moll U. M., Munoz-Pinedo C., Murphy D. J., Niklison-Chirou M. V., Novelli F., Nunez G., Oberst A., Ofengeim D., Opferman J. T., Oren M., Pagano M., Panaretakis T., Pasparakis M., Penninger J. M., Pentimalli F., Pereira D. M., Pervaiz S., Peter M. E., Pinton P., Porta G., Prehn J. H. M., Puthalakath H., Rabinovich G. A., Rajalingam K., Ravichandran K. S., Rehm M., Ricci J.-E., Rizzuto R., Robinson N., Rodrigues C. M. P., Rotblat B., Rothlin C. V., Rubinsztein D. C., Rudel T., Rufini A., Ryan K. M., Sarosiek K. A., Sawa A., Sayan E., Schroder K., Scorrano L., Sesti F., Shao F., Shi Y., Sica G. S., Silke J., Simon H.-U., Sistigu A., Stephanou A., Stockwell B. R., Strapazzon F., Strasser A., Sun L., Sun E., Sun Q., Szabadkai G., Tait S. W. G., Tang D., Tavernarakis N., Troy C. M., Turk B., Urbano N., Vandenabeele P., Vanden Berghe T., Vander Heiden M. G., Vanderluit J. L., Verkhratsky A., Villunger A., von Karstedt S., Voss A. K., Vousden K. H., Vucic D., Vuri D., Wagner E. F., Walczak H., Wallach D., Wang R., Wang Y., Weber A., Wood W., Yamazaki T., Yang H.-T., Zakeri Z., Zawacka-Pankau J. E., Zhang L., Zhang H., Zhivotovsky B., Zhou W., Pia centini M., Kroemer G., and Galluzzi L. Apoptotic cell death in disease—Current understanding of the NCCD 2023. Cell Death Differ., 30 (5), 1097–1154 (2023). doi: 10.1038/s41418-023-01153-w
- Liu X., Yang W., Guan Z., Yu W., Fan B., Xu N., and Liao D. J. There are only four basic modes of cell death, although there are many ad-hoc variants adapted to different situations. Cell Biosci., 8 (1), 6 (2018). doi: 10.1186/s13578-018-0206-6
- Tang D., Kang R., Berghe T. V., Vandenabeele P., and Kroemer G. The molecular machinery of regulated cell death. Cell Res., 29 (5), 347–364 (2019). doi: 10.1038/s41422-019-0164-5
- Yuan J. and Ofengeim D. A guide to cell death pathways. Nat. Rev. Mol. Cell Biol. (2023). doi: 10.1038/s41580-023-00689-6
- Maltese W. A. and Overmeyer J. H. Methuosis: nonapoptotic cell death associated with vacuolization of macropinosome and endosome compartments. Am. J. Pathol., 184 (6), 1630–1642 (2014). doi: 10.1016/j.ajpath.2014.02.028
- Sauler M., Bazan I. S., and Lee P. J. Cell Death in the Lung: The Apoptosis-necroptosis axis. Ann. Rev. Physiol., 81, 375-402 (2019). doi: 10.1146/annurev-physiol-020518-114320
- Galluzzi L., Kepp O., and Kroemer G. Mitochondrial regulation of cell death: a phylogenetically conserved control. Microb. cell, 3 (3), 101–108 (2016). doi: 10.15698/mic2016.03.483
- Yashin D. V., Romanova E. A., Ivanova O. K., and Sashchenko L. P. The Tag7-Hsp70 cytotoxic complex induces tumor cell necroptosis via permeabilisation of lysosomes and mitochondria. Biochimie, 123, 32–36 (2016). doi: 10.1016/j.biochi.2016.01.007
- Park W., Wei S., Kim B.-S., Kim B., Bae S.-J., ChaeY. C., Ryu D., and Ha K.-T. Diversity and complexity of cell death: a historical review. Exp. Mol. Med., 55 (8), 1573–1594 (2023). doi: 10.1038/s12276-023-01078-x
- Alu A., Han X., Ma X., Wu M., Wei Y., and Wei X. The role of lysosome in regulated necrosis. Acta Pharm. Sin. B, 10 (10), 1880–1903 (2020). doi: 10.1016/j.apsb.2020.07.003
- Liu X., Zhang Z., Ruan J., Pan Y., Magupalli V. G., Wu H., and Lieberman J. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature, 535 (7610), 153–158 (2016). doi: 10.1038/nature18629
- Vorobjeva N. V. and Chernyak B. V. NETosis: molecular mechanisms, role in physiology and pathology. Biochemistry (Moscow), 85 (10), 1178–1190 (2020). doi: 10.1134/s0006297920100065
- Mishra P. K., Adameova A., Hill J. A., Baines C. P., Kang P. M., Downey J. M., Narula J., Takahashi M., Abbate A., Piristine H. C., Kar S., Su S., Higa J. K., Kawasaki N. K., and Matsui T. Guidelines for evaluating myocardial cell death. Am. J. Physiol. Heart Circ. Physiol., 317 (5), H891–h922 (2019). doi: 10.1152/ajpheart.00259.2019
- Scott J., Lemberg Kathryn M., Lamprecht Michael R., Skouta R., Zaitsev E. M., Gleason C. E., Patel D. N., Bauer A. J., Cantley A. M., Yang W. S., Morrison B., and Stockwell B. R. Ferroptosis: An Iron-dependent form of nonapoptotic cell death. Cell, 149 (5), 10601072 (2012). DOI: https://doi.org/10.1016/j.cell.2012.03.042
- Grignano E., Birsen R., Chapuis N., and Bouscary D. From Iron chelation to overload as a therapeutic strategy to induce ferroptosis in leukemic cells. Front. Oncol., 10, 586530 (2020). doi: 10.3389/fonc.2020.586530
- Xie Y., Hou W., Song X., Yu Y., Huang J., Sun X., Kang R., and Tang D. Ferroptosis: process and function. Cell Death Differ., 23 (3), 369–379 (2016). doi: 10.1038/cdd.2015.158
- Moon J. H., Jeong J. K., and Park S. Y. Deferoxamine inhibits TRAIL-mediated apoptosis via regulation of autophagy in human colon cancer cells. Oncol. Rep., 33 (3), 1171-1176 (2015). doi: 10.3892/or.2014.3676
- Solovieva M. E., Solovyev V. V., Kudryavtsev A. A., Trizna Y. A., and Akatov V. S. Vitamin B12b enhances the cytotoxicity of dithiothreitol. Free Rad. Biol. Med., 44 (10), 1846–1856 (2008). doi: 10.1016/j.freeradbiomed.2008.02.002
- Gao H., Bai Y., Jia Y., Zhao Y., Kang R., Tang D., and Dai E. Ferroptosis is a lysosomal cell death process. Biochem. Biophys. Res. Commun., 503 (3), 1550–1556 (2018). doi: 10.1016/j.bbrc.2018.07.078
- Zhou B., Liu J., Kang R., Klionsky D. J., Kroemer G., and Tang D. Ferroptosis is a type of autophagy-dependent cell death. Semin. Cancer Biol., 66, 89–100 (2020). doi: 10.1016/j.semcancer.2019.03.002
- Yashin D. V., Ivanova O. K., Soshnikova N. V., Sheludchenkov A. A., Romanova E. A., Dukhanina E. A., Tonevitsky A. G., Gnuchev N. V., Gabibov A. G., Georgiev G. P., and Sashchenko L. P. Tag7 (PGLYRP1) in complex with Hsp70 induces alternative cytotoxic processes in tumor cells via TNFR1 receptor. J. Biol. Chem., 290 (35), 21724–21731 (2015). doi: 10.1074/jbc.M115.639732
- Eloranta K., Cairo S., Liljestrom E., Soini T., Kyronlahti A., Judde J. G., Wilson D. B., Heikinheimo M., and Pihlajoki M. Chloroquine triggers cell death and inhibits PARPs in cell models of aggressive hepatoblastoma. Front. Oncol., 10, 1138 (2020). doi: 10.3389/fonc.2020.01138
- Mauvezin C., Nagy P., Juhasz G., and Neufeld T. P. Autophagosome-lysosome fusion is independent of VATPasemediated acidification. Nat. Commun., 6, 7007 (2015). doi: 10.1038/ncomms8007
- Yuan N., Song L., Zhang S., Lin W., Cao Y., Xu F., Fang Y., Wang Z., Zhang H., Li X., Wang Z., Cai J., Wang J., Zhang Y., Mao X., Zhao W., Hu S., Chen S., and Wang J. Bafilomycin A1 targets both autophagy and apoptosis pathways in pediatric B-cell acute lymphoblastic leukemia. Haematologica, 100 (3), 345–356 (2015). doi: 10.3324/haematol.2014.113324
- Liu Y., Shoji-Kawata S., Sumpter R. M., Jr., Wei Y., Ginet V., Zhang L., Posner B., Tran K. A., GreenD. R., Xavier R. J., Shaw S. Y., Clarke P. G., Puyal J., and Levine B. Autosis is a Na+,K+-ATPaseregulated form of cell death triggered by autophagy-inducing peptides, starvation, and hypoxia-ischemia. Proc. Natl. Acad. Sci. USA, 110 (51), 20364–20371 (2013). doi: 10.1073/pnas.1319661110
- Bialik S. and Dasari S. K. Autophagy-dependent cell death −where, how and why a cell eats itself to death. J. Cell Sci., 131 (18), (2018). doi: 10.1242/jcs.215152
- Bai L., Wu Q., Zhang X., and Zhao Y. Autosis as a selective type of cell death. Front. Cell Dev. Biol., 11, 1164681 (2023). doi: 10.3389/fcell.2023.1164681
- Overholtzer M., Mailleux A. A., Mouneimne G., Normand G., Schnitt S. J., King R. W., Cibas E. S., and Brugge J. S. A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell, 131 (5), 966-979 (2007). doi: 10.1016/j.cell.2007.10.040
- Martins I., Raza S. Q., Voisin L., Dakhli H., Law F., De Jong D., Allouch A., Thoreau M., Brenner C., Deutsch E., and Perfettini J. L. Entosis: The emerging face of non-cell-autonomous type IV programmed death. Biomed. J., 40 (3), 133–140 (2017). doi: 10.1016/j.bj.2017.05.001
- Garanina A. S., Kisurina-Evgenieva O. P., ErokhinaM. V., Smirnova E. A., Factor V. M., and Onishchenko G. E. Consecutive entosis stages in human substrate-dependent cultured cells. Sci. Rep., 7 (1), 12555 (2017). doi: 10.1038/s41598-017-12867-6
- Durgan J., Tseng Y. Y., Hamann J. C., Domart M. C., Collinson L., Hall A., Overholtzer M., and Florey O. Mitosis can drive cell cannibalism through entosis. eLife, 6 (2017). doi: 10.7554/eLife.27134
- Solovieva M., Shatalin Y., Odinokova I., Krestinina O., Baburina Y., Mishukov A., Lomovskaya Y., Pavlik L., Mikheeva I., Holmuhamedov E., and Akatov V. Disulfiram oxy-derivatives induce entosis or paraptosis-like death in breast cancer MCF-7 cells depending on the duration of treatment. Biochim. Biophys. Acta. Gen. Subj., 1866 (9), 130184 (2022). doi: 10.1016/j.bbagen.2022.130184
- Guicciardi M. E., Deussing J., Miyoshi H., Bronk S. F., Svingen P. A., Peters C., Kaufmann S. H., and Gores G. J. Cathepsin B contributes to TNF-alphamediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J. Clin. Invest., 106 (9), 1127–1137 (2000). doi: 10.1172/jci9914
- Yu S. W., Wang H., Poitras M. F., Coombs C., Bowers W. J., Federoff H. J., Poirier G. G., Dawson T. M., and Dawson V. L. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science, 297 (5579), 259–263 (2002). doi: 10.1126/science.1072221
- Деев Р. В., Билялов А. И. и Жампеисов Т. М. Современные представления о клеточной гибели. Гены и Клетки, XIII (1), 6–19 (2018).doi: 10.23868/201805001
- Weaver A. N. and Yang E. S. Beyond DNA Repair: additional functions of PARP-1 in cancer. Front. Oncol., 3, 290 (2013). doi: 10.3389/fonc.2013.00290
- Lee S. and Karki R. AIM2 forms a complex with pyrin and ZBP1 to drive PANoptosis and host defence. Nature, 597 (7876), 415–419 (2021). doi: 10.1038/s41586-021-03875-8
- Shi C. and Cao P. PANoptosis: a cell death characterized by pyroptosis, apoptosis, and necroptosis. J. Inflamm. Res., 16, 1523–1532 (2023). doi: 10.2147/jir.s403819
- Holze C., Michaudel C., Mackowiak C., Haas D. A., Benda C., Hubel P., Pennemann F. L., Schnepf D., Wettmarshausen J., Braun M., Leung D. W., and Amarasinghe G. K. Oxeiptosis, a ROS-induced caspaseindependent apoptosis-like cell-death pathway. Nat. Immunol., 19 (2), 130–140 (2018). doi: 10.1038/s41590-017-0013-y
- Pallichankandy S., Thayyullathil F., Cheratta A. R., Subburayan K., Alakkal A., Sultana M., Drou N., Arshad M., Tariq S., and Galadari S. Targeting oxeiptosismediated tumor suppression: a novel approach to treat colorectal cancers by sanguinarine. Cell Death Discov., 9 (1), 94 (2023). doi: 10.1038/s41420-023-01376-3
- Zhang J., Gao R. F., Li J., Yu K. D., and Bi K. X. Alloimperatorin activates apoptosis, ferroptosis, and oxeiptosis to inhibit the growth and invasion of breast cancer cells in vitro. Biochem. Cell Biol., 100 (3), 213–222 (2022). doi: 10.1139/bcb-2021-0399
- Scaturro P. and Pichlmair A. Oxeiptosis: a discreet way to respond to radicals. Curr. Opin. Immunol., 56, 37–43 (2019). doi: 10.1016/j.coi.2018.10.006
- Villalpando-Rodriguez G. E., and Gibson S. B. Reactive oxygen species (ROS) regulates different types of cell death by acting as a rheostat. Oxid. Med. Cell Longev., 2021, 9912436 (2021). doi: 10.1155/2021/9912436
- Que D., Kuang F., Kang R., Tang D., and Liu J. ACSS2-mediated NF-κB activation promotes alkaliptosis in human pancreatic cancer cells. Sci. Rep., 13 (1), 1483 (2023). doi: 10.1038/s41598-023-28261-4
- Chen F., Zhu S., Kang R., Tang D., and Liu J. ATP6V0D1 promotes alkaliptosis by blocking STAT3mediated lysosomal pH homeostasis. Cell Rep., 42 (1), 111911 (2023). doi: 10.1016/j.celrep.2022.111911
- Ciesielski H. M., Nishida H., Takano T., Fukuhara A., Otani T., Ikegawa Y., Okada M., Nishimura T., Furuse M., and Yoo S. K. Erebosis, a new cell death mechanism during homeostatic turnover of gut enterocytes. PLoS Biol., 20 (4), e3001586 (2022). doi: 10.1371/journal.pbio.3001586
- Liu X., Nie L., Zhang Y., Yan Y., Wang C., Colic M., Olszewski K., Horbath A., Chen X., Lei G., Mao C., Wu S., Zhuang L., Poyurovsky M. V., James You M., Hart T., Billadeau D. D., Chen J., and Gan B. Actin cytoskeleton vulnerability to disulfide stress mediates disulfidptosis. Nat. Cell Biol., 25 (3), 404–414 (2023). doi: 10.1038/s41556-023-01091-2
- Wang L.-Y., Liu X.-J., Li Q.-Q., Zhu Y., Ren H.-L., Song J.-N., Zeng J., Mei J., Tian H.-X., Rong D.-C., and Zhang S.-H. The romantic history of signaling pathway discovery in cell death: an updated review. Mol. Cell. Biochem. (2023). doi: 10.1007/s11010-023-04873-2
- Xie J., Yang Y., Gao Y., and He J. Cuproptosis: mechanisms and links with cancers. Mol. Cancer, 22 (1), 46 (2023). doi: 10.1186/s12943-023-01732-y
- Chen D., Cui Q. C., Yang H., and Dou Q. P. Disulfiram, a clinically used anti-alcoholism drug and copperbinding agent, induces apoptotic cell death in breast cancer cultures and xenografts via inhibition of the proteasome activity. Cancer Res., 66 (21), 10425–10433 (2006). doi: 10.1158/0008-5472.can-06-2126
- Cen D., Brayton D., Shahandeh B., Meyskens F. L., Jr., and Farmer P. J. Disulfiram facilitates intracellular Cu uptake and induces apoptosis in human melanoma cells. J. Med. Chem., 47 (27), 6914–6920 (2004). doi: 10.1021/jm049568z
- Tardito S., Bassanetti I., Bignardi C., Elviri L., Tegoni M., Mucchino C., Bussolati O., Franchi-Gazzola R., and Marchio L. Copper binding agents acting as copper ionophores lead to caspase inhibition and paraptotic cell death in human cancer cells. J. Am. Chem. Soc., 133 (16), 6235–6242 (2011). doi: 10.1021/ja109413c
- Hu L., Wang H., Zhao Y., and Wang J. 125I seeds radiation induces paraptosis-like cell death via PI3K/AKT signaling pathway in HCT116 cells. Biomed. Res. Int., 2016, 8145495 (2016). doi: 10.1155/2016/8145495
- Wang W. B., Feng L. X., Yue Q. X., Wu W. Y., Guan S. H., Jiang B. H., Yang M., Liu X., and Guo D. A. Paraptosis accompanied by autophagy and apoptosis was induced by celastrol, a natural compound with influence on proteasome, ER stress and Hsp90. J. Cell Physiol., 227 (5), 2196–2206 (2012). doi: 10.1002/jcp.22956
- Yoon M. J., Kang Y. J., Lee J. A., Kim I. Y., Kim M. A., Lee Y. S., Park J. H., Lee B. Y., Kim I. A., Kim H. S., Kim S. A., Yoon A. R., Yun C. O., Kim E. Y., Lee K., and Choi K. S. Stronger proteasomal inhibition and higher CHOP induction are responsible for more effective induction of paraptosis by dimethoxycurcumin than curcumin. Cell Death Dis., 5 (3), e1112 (2014). doi: 10.1038/cddis.2014.85
- Yoon M. J., Kim E. H., Kwon T. K., Park S. A., and Choi K. S. Simultaneous mitochondrial Ca2+ overload and proteasomal inhibition are responsible for the induction of paraptosis in malignant breast cancer cells. Cancer Lett., 324 (2), 197–209 (2012). doi: 10.1016/j.canlet.2012.05.018
- Korsnes M. S., Espenes A., Hetland D. L., and Hermansen L. C. Paraptosis-like cell death induced by yessotoxin. Toxicol. in vitro, 25 (8), 1764–1770 (2011). doi: 10.1016/j.tiv.2011.09.005
- Alfonso A., Vieytes M. R. and Botana L. M. Yessotoxin, a promising therapeutic tool. Marine Drugs, 14 (2), (2016). doi: 10.3390/md14020030
- Li B., Zhao J., Wang C. Z., Searle J., He T. C., Yuan C. S., and Du W. Ginsenoside Rh2 induces apoptosis and paraptosis-like cell death in colorectal cancer cells through activation of p53. Cancer Lett., 301 (2), 185–192 (2011). doi: 10.1016/j.canlet.2010.11.015
- Wang Y., Zhu X., Yang Z., and Zhao X. Honokiol induces caspase-independent paraptosis via reactive oxygen species production that is accompanied by apoptosis in leukemia cells. Biochem. Biophys. Res. Commun., 430 (3), 876–882 (2013). doi: 10.1016/j.bbrc.2012.12.063
- Liu X., Gu Y., and Bian Y. Honokiol induces paraptosislike cell death of acute promyelocytic leukemia via mTOR & MAPK signaling pathways activation. Apoptosis, 26 (3–4), 195–208 (2021). doi: 10.1007/s10495-020-01655-9
- Zhang J. S., Li D. M., Ma Y., He N., Gu Q., Wang F. S., Jiang S. Q., Chen B. Q., and Liu J. R. γ-Tocotrienol induces paraptosis-like cell death in human colon carcinoma SW620 cells. PLoS One, 8 (2), e57779 (2013). doi: 10.1371/journal.pone.0057779
- Kar R., Singha P. K., Venkatachalam M. A., and Saikumar P. A novel role for MAP1 LC3 in nonautophagic cytoplasmic vacuolation death of cancer cells. Oncogene, 28 (28), 2556–2568 (2009). doi: 10.1038/onc.2009.118
- Tsai T. L., Wang H. C., Hung C. H., Lin P. C., LeeY. S., Chen H. H. W., and Su W. C. Wheat germ agglutinininduced paraptosis-like cell death and protective autophagy is mediated by autophagy-linked FYVE inhibition. Oncotarget, 8 (53), 91209–91222 (2017). doi: 10.18632/oncotarget.20436
- Seo M. J., Lee D. M., Kim I. Y., Lee D., Choi M.-K., Lee J.-Y., Park S. S., Jeong S.-Y., Choi E. K., and Choi K. S. Gambogic acid triggers vacuolization-associated cell death in cancer cells via disruption of thiol proteostasis. Cell Death Dis., 10 (3), 187 (2019). doi: 10.1038/s41419–019-1360-4
- Mi X., Wang C., Sun C., Chen X., Huo X., Zhang Y., Li G., Xu B., Zhang J., Xie J., Wang Z., and Li J. Xanthohumol induces paraptosis of leukemia cells through p38 mitogen activated protein kinase signaling pathway. Oncotarget, 8 (19), 31297–31304 (2017). doi: 10.18632/oncotarget.16185
- Bury M., Girault A., Megalizzi V., Spiegl-Kreinecker S., Mathieu V., Berger W., Evidente A., Kornienko A., Gailly P., Vandier C., and Kiss R. Ophiobolin A induces paraptosis-like cell death in human glioblastoma cells by decreasing BKCa channel activity. Cell Death Dis., 4 (3), e561 (2013). doi: 10.1038/cddis.2013.85
- Kim I. Y., Shim M. J., Lee D. M., Lee A. R., Kim M.A., Yoon M. J., Kwon M. R., Lee H. I., Seo M. J., Choi Y. W., and Choi K. S. Loperamide overcomes the resistance of colon cancer cells to bortezomib by inducing CHOP-mediated paraptosis-like cell death. Biochem. Pharmacol., 162, 41–54 (2019). doi: 10.1016/j.bcp.2018.12.006
- Gafar A. A., Draz H. M., Goldberg A. A., Bashandy M. A., Bakry S., Khalifa M. A., AbuShair W., Titorenko V. I., and Sanderson J. T. Lithocholic acid induces endoplasmic reticulum stress, autophagy and mitochondrial dysfunction in human prostate cancer cells. Peer J., 4, e2445 (2016). doi: 10.7717/peerj.2445
- Wasik A. M., Almestrand S., Wang X., Hultenby K., Dackland A. L., Andersson P., Kimby E., Christensson B., and Sander B. WIN55,212-2 induces cytoplasmic vacuolation in apoptosis-resistant MCL cells. Cell Death Dis., 2 (11), e225 (2011). doi: 10.1038/cddis.2011.106
- Sun Q., Chen T., Wang X., and Wei X. Taxol induces paraptosis independent of both protein synthesis and MAPK pathway. J. Cell. Physiol., 222 (2), 421–432 (2010). doi: 10.1002/jcp.21982
- Kim S. H., Shin H. Y., Kim Y. S., Kang J. G., Kim C. S., Ihm S. H., Choi M. G., Yoo H. J., and Lee S. J. Tunicamycin induces paraptosis potentiated by inhibition of BRAFV600E in FRO anaplastic thyroid carcinoma cells. Anticancer Res., 34 (9), 4857–4868 (2014).
- Hu L., Shi J., Shen D., Zhai X., Liang D., Wang J., Xie C., Xia Z., Cui J., Liu F., Du S., Meng S., and Piao H. Osimertinib induces paraptosis and TRIP13 confers resistance in glioblastoma cells. Cell Death Discov., 9 (1), 333 (2023). doi: 10.1038/s41420-023-01632-6
- Nguyen P. L., Lee C. H., Lee H., and Cho J. Induction of paraptotic cell death in breast cancer cells by a novel pyrazolo[3,4-h]quinoline derivative through ROS production and endoplasmic reticulum stress. Antioxidants, 11 (1), 117 (2022). doi: 10.3390/antiox11010117
- Chen X., Zhang X., Chen J., Yang Q., Yang L., Xu D., Zhang P., Wang X., and Liu J. Hinokitiol copper complex inhibits proteasomal deubiquitination and induces paraptosis-like cell death in human cancer cells. Eur. J. Pharmacol., 815, 147–155 (2017). doi: 10.1016/j.ejphar.2017.09.003
- Hager S., Pape V. F. S., Posa V., Montsch B., Uhlik L., Szakacs G., Toth S., Jabronka N., Keppler B. K., Kowol C. R., Enyedy E A., and Heffeter P. High copper complex stability and slow reduction kinetics as key parameters for improved activity, paraptosis induction, and impact on drug-resistant cells of anticancer thiosemicarbazones. Antioxid. Redox Signal., 33 (6), 395–414 (2020). doi: 10.1089/ars.2019.7854
- Solovieva M., Shatalin Y., Fadeev R., Krestinina O., Baburina Y., Kruglov A., Kharechkina E., Kobyakova M., Rogachevsky V., Shishkova E., and Akatov A. V. Vitamin B(12b) Enhances the cytotoxicity of diethyldithiocarbamate in a synergistic manner, inducing the paraptosis-like death of human larynx carcinoma cells. Biomolecules, 10 (1), (2020). doi: 10.3390/biom10010069
- Solovieva M., Shatalin Y., Odinokova I., Krestinina O., Baburina Y., Lomovskaya Y., Pankratov A., Pankratova N., Buneeva O., Kopylov A., Medvedev A., and Akatov V. Disulfiram oxy-derivatives suppress protein retrotranslocation across the ER membrane to the cytosol and initiate paraptosis-like cell death. Membranes (12), 845, (2022). doi: 10.3390/membranes12090845
- Wang Y., Wen X., Zhang N., Wang L., Hao D., Jiang X., and He G. Small-molecule compounds target paraptosis to improve cancer therapy. Biomed. Pharmacother., 118, 109203 (2019). doi: 10.1016/j.biopha.2019.109203
- Chen F., Tang H., Cai X., Lin J., Xiang L., Kang R., and Liu J. Targeting paraptosis in cancer: opportunities and challenges. Cancer Gene Ther., (2024). doi: 10.1038/s41417-023-00722-y
- Sperandio S., de Belle I., and Bredesen D. E. An alternative, nonapoptotic form of programmed cell death. Proc. Natl. Acad. Sci. USA, 97 (26), 14376–14381 (2000). doi: 10.1073/pnas.97.26.14376
- Sperandio S., Poksay K., de Belle I., Lafuente M. J., Liu B., Nasir J., and Bredesen D. E. Paraptosis: mediation by MAP kinases and inhibition by AIP-1/Alix. Cell Death Differ., 11 (10), 1066–1075 (2004). doi: 10.1038/sj.cdd.4401465
- Liu S., Tian Y., Liu C., Gui Z., Yu T., and Zhang L. TNFRSF19 promotes endoplasmic reticulum stressinduced paraptosis via the activation of the MAPK pathway in triple-negative breast cancer cells. Cancer Gene Ther., 31 (2), 217–227 (2024). doi: 10.1038/s41417-023-00696-x
- Hoa N., Myers M. P., Douglass T. G., Zhang J. G., Delgado C., Driggers L., Callahan L. L., VanDeusen G., Pham J. T., Bhakta N., Ge L., and Jadus M. R. Molecular mechanisms of paraptosis induction: implications for a non-genetically modified tumor vaccine. PLoS One, 4 (2), e4631 (2009). doi: 10.1371/journal.pone.0004631
- Kim I. Y., Kwon M., Choi M. K., Lee D., Lee D. M., Seo M. J., and Choi K. S. Ophiobolin A kills human glioblastoma cells by inducing endoplasmic reticulum stress via disruption of thiol proteostasis. Oncotarget, 8 (63), 106740–106752 (2017). doi: 10.18632/oncotarget.22537
- Hager S., Korbula K., Bielec B., Grusch M., Pirker C., Schosserer M., Liendl L., Lang M., Grillari J., Nowikovsky K., Pape V. F. S., Mohr T., Szakacs G., Keppler B. K., Berger W., Kowol C. R., and Heffeter P. The thiosemicarbazone Me(2)NNMe(2) induces paraptosis by disrupting the ER thiol redox homeostasis based on protein disulfide isomerase inhibition. Cell Death Dis., 9 (11), 1052 (2018). doi: 10.1038/s41419-018-1102-z
- Lee H. J., Lee D. M., Seo M. J., Kang H. C., Kwon S. K., and Choi K. S. PSMD14 targeting triggers paraptosis in breast cancer cells by inducing proteasome inhibition and Ca2+ imbalance. Int. J. Mol. Sci., 23 (5), (2022). doi: 10.3390/ijms23052648
- Wang L., Gundelach J. H., and Bram R. J. Cycloheximide promotes paraptosis induced by inhibition of cyclophilins in glioblastoma multiforme. Cell Death Dis., 8 (5), e2807 (2017). doi: 10.1038/cddis.2017.217
- Dumay A., Rincheval V., Trotot P., Mignotte B., and Vayssiere J. L. The superoxide dismutase inhibitor diethyldithiocarbamate has antagonistic effects on apoptosis by triggering both cytochrome c release and caspase inhibition. Free Rad. Biol. Med., 40 (8), 1377–1390 (2006). doi: 10.1016/j.freeradbiomed.2005.12.005
- Zhu D., Chen C., Xia Y., Kong L. Y., and Luo J. A purified resin glycoside fraction from pharbitidis semen induces paraptosis by activating chloride intracellular channel-1 in human colon cancer cells. Integr. Cancer Ther., 18, 1534735418822120 (2019). doi: 10.1177/1534735418822120
- Hoa N. T., Zhang J. G., Delgado C. L., Myers M. P., Callahan L. L., Vandeusen G., Schiltz P. M., Wepsic H. T., and Jadus M. R. Human monocytes kill M-CSF-expressing glioma cells by BK channel activation. Lab. Invest., 87 (2), 115–129 (2007). doi: 10.1038/labinvest.3700506
- Allan L. A., Morrice N., Brady S., Magee G., Pathak S., and Clarke P. R. Inhibition of caspase-9 through phosphorylation at Thr 125 by ERK MAPK. Nat. Cell Biol., 5 (7), 647–654 (2003). doi: 10.1038/ncb1005
- Kim E., Lee D. M., Seo M. J., Lee H. J., and Choi K. S. Intracellular Ca2+ Imbalance Critically Contributes to Paraptosis. Front. Cell Dev. Biol., 8 (1703), (2021). doi: 10.3389/fcell.2020.607844
- Pyrczak-Felczykowska A., Reekie T. A., Jąkalski M., Hać A., Malinowska M., Pawlik A., Ryś K., GuzowKrzemińska B., and Herman-Antosiewicz A. The isoxazole derivative of usnic acid induces an er stress response in breast cancer cells that leads to paraptosis-like cell death. Int. J. Mol. Sci., 23 (3), 1802 (2022). doi: 10.3390/ijms23031802
- Yokoi K., Yamaguchi K., and Umezawa M. Induction of paraptosis by cyclometalated iridium complex-peptide hybrids and CGP37157 via a mitochondrial Ca2+ overload triggered by membrane fusion between mitochondria and the endoplasmic reticulum. Biochemistry, 61 (8), 639–655 (2022). doi: 10.1021/acs.biochem.2c00061
- Singha P. K., Pandeswara S., Venkatachalam M. A., and Saikumar P. Manumycin A inhibits triple-negative breast cancer growth through LC3-mediated cytoplasmic vacuolation death. Cell Death Dis., 4 (1), e457 (2013). doi: 10.1038/cddis.2012.192
- Zhang C., Jiang Y., Zhang J., Huang J., and Wang J. 8-p-Hdroxybenzoyl tovarol induces paraptosis like cell death and protective autophagy in human cervical cancer hela cells. Int. J. Mol. Sci., 16 (7), 14979–14996 (2015).
- Lee D. M. and Kim I. Y. Akt enhances the vulnerability of cancer cells to VCP/p97 inhibition-mediated paraptosis. Cell Death Dis., 15 (1), 48 (2024). doi: 10.1038/s41419-024-06434-x
- Шубин А. В. Протеазы как цитотоксические агенты и маркеры злокачественных опухолей легкого : Дис. ... канд. биол. наук (Инст. молекулярной биологии им. В.А. Энгельгарда РАН, М., 2014).
- Wang C., Li T. K., Zeng C. H., Fan R., Wang Y., Zhu G. Y., and Guo J. H. Iodine-125 seed radiation induces ROS-mediated apoptosis, autophagy and paraptosis in human esophageal squamous cell carcinoma cells. Oncol. Rep., 43 (6), 2028–2044 (2020). doi: 10.3892/or.2020.7576
Supplementary files
