The co-translocation of ERp57 and calreticulin determines the immunogenicity of cell death
Open accessAbstract
The exposure of calreticulin (CRT) on the plasma membrane can precede anthracycline-induced apoptosis and is required for cell death to be perceived as immunogenic. Mass spectroscopy, immunofluorescence and immunoprecipitation experiments revealed that CRT co-translocates to the surface with another endoplasmic reticulum-sessile protein, the disulfide isomerase ERp57. The knockout and knockdown of CRT or ERp57 inhibited the anthracycline-induced translocation of ERp57 or CRT, respectively. CRT point mutants that fail to interact with ERp57 were unable to restore ERp57 translocation upon transfection into crt(-/-) cells, underscoring that a direct interaction between CRT and ERp57 is strictly required for their co-translocation to the surface. ERp57(low) tumor cells generated by retroviral introduction of an ERp57-specific shRNA exhibited a normal apoptotic response to anthracyclines in vitro, yet were resistant to anthracycline treatment in vivo. Moreover, ERp57(low) cancer cells (which failed to expose CRT) treated with anthracyclines were unable to elicit an anti-tumor response in conditions in which control cells were highly immunogenic. The failure of ERp57(low) cells to elicit immune responses and to respond to chemotherapy could be overcome by exogenous supply of recombinant CRT protein. These results indicate that tumors that possess an intrinsic defect in the CRT-translocating machinery become resistant to anthracycline chemotherapy due to their incapacity to elicit an anti-cancer immune response.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In most ICD instances, CALR translocates to cell surface together with ERp57.
“In most instances of ICD, CALR translocates to the cell surface together with protein disulfide isomerase family A member 3 (PDIA3; best known as known as ERp57) [881].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [881]
CALR knockdown or defects in CALR exposure abolish ability of anthracycline-treated dying cancer cells to establish protective immunity in mice; recombinant CALR confers immunogenic properties to non-immunogenic RCD.
“In line with a key role of CALR in the immunogenicity of RCD, the RNAi-mediated knockdown of CALR as well as natural defects in the CALR exposure pathway reportedly abolish the ability of dying cancer cells succumbing to anthracyclines to establish protective immunity in mice, whereas the exogenous provision of recombinant CALR confers immunogenic properties to otherwise non-immunogenic variants”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [881]
Inhibition of caspases affects exposure of find-me signals, eat-me signals, secretion of DAMPs, and exposure of CRT on anthracyclin-treated cancer cells.
“The inhibition of caspases affects the exposure of find-me signals 40, eat-me signals 40 (Box 4), and the secretion of DAMPs51 from dying cells, as well as the exposure of CRT on anthracyclin-treated cancer cells60.”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [40]
Caspases cleave and activate phospholipase A2, although this is not required for production of the lipid signal.
“Caspases cleave and thereby activate PLA2, although this is not required for production of the lipid signal.”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [40]
Lysophosphatidylcholine is one such find-me signal, produced by the action of phospholipase A2.
“One such signal is lysophosphatidylcholine 40, which is produced by the action of phospholipase A2 (PLA2).”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [40]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Calreticulin exposure dictates the immunogenicity of cancer cell death
Obeid, M., Tesniere, A., Ghiringhelli, F., Fimia, G. M., Apetoh, L., Perfettini, J.-L., Castedo, M., Mignot, G., Panaretakis, T., Casares, N., et al. (2007) · Nature Medicine · doi:10.1038/nm1523 · Cited by 3,216 · see citing works
Self-citationApetoh, L., Ghiringhelli, F., Tesniere, A., Obeid, M., Ortiz, C., Criollo, A., Mignot, G., Maiuri, M. C., Ullrich, E., Saulnier, P., et al. (2007) · Nature Medicine · doi:10.1038/nm1622 · Cited by 3,056 · see citing works
Self-citationImmunological aspects of cancer chemotherapy
Zitvogel, L., Apetoh, L., Ghiringhelli, F., & Kroemer, G. (2008) · Nature Reviews Immunology · doi:10.1038/nri2216 · Cited by 1,712 · see citing works
Self-citationCaspase-dependent immunogenicity of doxorubicin-induced tumor cell death
Casares, N., Pequignot, M. O., Tesniere, A., Ghiringhelli, F., Roux, S., Chaput, N., Schmitt, E., Hamai, A., Hervas-Stubbs, S., Obeid, M., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050915 · Cited by 1,512 · see citing works
Self-citationGardai, S. J., McPhillips, K. A., Frasch, S. C., Janssen, W. J., Starefeldt, A., Murphy-Ullrich, J. E., Bratton, D. L., Oldenborg, P.-A., Michalak, M., & Henson, P. M. (2005) · Cell · doi:10.1016/j.cell.2005.08.032 · Cited by 1,473 · see citing works
A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast
Güldener, U. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.6.e23 · Cited by 982 · see citing works
Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae
Sheff, M. A., & Thorn, K. S. (2004) · Yeast · doi:10.1002/yea.1130 · Cited by 654 · see citing works
Medzihradszky, K. F., Campbell, J. M., Baldwin, M. A., Falick, A. M., Juhász, P., Vestal, M. L., & Burlingame, A. L. (1999) · Analytical Chemistry · doi:10.1021/ac990809y · Cited by 531 · see citing works
Proteins of the PDI family: Unpredicted non‐ER locations and functions
Turano, C., Coppari, S., Fabio Altieri, F., & Ferraro, A. (2002) · Journal of Cellular Physiology · doi:10.1002/jcp.10172 · Cited by 520 · see citing works
Obeid, M., Panaretakis, T., Joza, N., Tufi, R., Tesniere, A., van Endert, P., Zitvogel, L., & Kroemer, G. (2007) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4402201 · Cited by 474 · see citing works
Self-citationCalreticulin is essential for integrin-mediated calcium signalling and cell adhesion
Coppolino, M. G., Woodside, M. J., Demaurex, N., Grinstein, S., St‐Arnaud, R., & Dedhar, S. (1997) · Nature · doi:10.1038/386843a0 · Cited by 392 · see citing works
Oliver, J. D., Roderick, H. L., Llewellyn, D. H., & High, S. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.8.2573 · Cited by 326 · see citing works
Quantitation of mitochondrial alterations associated with apoptosis
Castedo, M., Ferri, K. F., Roumier, T., Métivier, D., Zamzami, N., & Kroemer, G. (2002) · Journal of Immunological Methods · doi:10.1016/s0022-1759(02)00069-8 · Cited by 260 · see citing works
Self-citationGao, B., Adhikari, R., Howarth, M. R., Nakamura, K., Gold, M. C., Hill, A. B., Knee, R., Michalak, M., & Elliott, T. J. (2002) · Immunity · doi:10.1016/s1074-7613(01)00260-6 · Cited by 246 · see citing works
Ecto‐calreticulin in immunogenic chemotherapy
Obeid, M., Tesniere, A., Panaretakis, T., Tufi, R., Joza, N., Van Endert, P., Ghiringhelli, F., Apetoh, L., Chaput, N., Flament, C., et al. (2007) · Immunological Reviews · doi:10.1111/j.1600-065x.2007.00567.x · Cited by 202 · see citing works
Self-citationBid acts on the permeability transition pore complex to induce apoptosis
Zamzami, N., Hamel, C. E., Maisse, C., Brenner, C., Muñoz-Pinedo, C., Belzacq, A.-S., Costantini, P., Vieira, H., Loeffler, M., Molle, G., et al. (2000) · Oncogene · doi:10.1038/sj.onc.1204030 · Cited by 178 · see citing works
Self-citationObéid, M., Panaretakis, T., Tesnière, A., Joza, N., Tufi, R., Apétoh, L., Ghiringhelli, F., Zitvogel, L., & Kroemer, G. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-1622 · Cited by 161 · see citing works
Self-citationBohring, C. (2001) · Molecular Human Reproduction · doi:10.1093/molehr/7.2.113 · Cited by 160 · see citing works
Biotinylation and assessment of membrane polarity: caveats and methodological concerns
Gottardi, C. J., Dunbar, L. A., & Caplan, M. J. (1995) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.1995.268.2.f285 · Cited by 142 · see citing works
SREC-I, a Type F Scavenger Receptor, Is an Endocytic Receptor for Calreticulin
Berwin, B. L., Delneste, Y., Lovingood, R. V., Post, S. R., & Pizzo, S. V. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m406202200 · Cited by 138 · see citing works
Molecular Cloning of the Human Glucose‐Regulated Protein ERp57/GRP58, a Thiol‐Dependent Reductase
Hirano, N., Shibasaki, F., Sakai, R., Tanaka, T., Nishida, J., Yazaki, Y., Takenawa, T., & Hirai, H. (1995) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1995.336_c.x · Cited by 130 · see citing works
Calreticulin Couples Calcium Release and Calcium Influx in Integrin-mediated Calcium Signaling
Kwon, M. S., Park, C. S., Choi, K.-R., Park, C., Ahnn, J., Kim, J. I., Eom, S. H., Kaufman, S. J., & Song, W. K. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.4.1433 · Cited by 128 · see citing works
Calreticulin, Ca2+, and Calcineurin - Signaling from the Endoplasmic Reticulum
Groenendyk, J., Lynch, J. M., & Michalak, M. (2004) · Molecules and Cells · doi:10.1016/s1016-8478(23)13056-1 · Cited by 124 · see citing works
Hanwell, D., Ishikawa, T., Saleki, R., & Rotin, D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110904200 · Cited by 121 · see citing works
Endoplasmic Reticulum Form of Calreticulin Modulates Glucocorticoid-sensitive Gene Expression
Michalak, M., Burns, K., Andrin, C., Mesaeli, N., Jass, G. K., Busaan, J. L., & Opas, M. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.46.29436 · Cited by 120 · see citing works
Tufi, R., Panaretakis, T., Bianchi, K., Criollo, A., Fazi, B., Sano, F. D., Tesnière, A., Kepp, O., Paterlini-Bréchot, P., Zitvogel, L., et al. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402275 · Cited by 118 · see citing works
Self-citationCa2+-Dependent Nuclear Export Mediated by Calreticulin
Holaska, J. M., Black, B. E., Rastinejad, F., & Paschal, B. M. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.17.6286-6297.2002 · Cited by 113 · see citing works
Apoptosis-inducing factor determines the chemoresistance of non-small-cell lung carcinomas
Gallego, M.-A., Joseph, B., Hemström, T. H., Tamiji, S., Mortier, L., Kroemer, G., Formstecher, P., Zhivotovsky, B., & Marchetti, P. (2004) · Oncogene · doi:10.1038/sj.onc.1207835 · Cited by 102 · see citing works
Self-citationExpression and prognostic significance of prothymosin-α and ERp57 in human gastric cancer
Leys, C. M., Nomura, S., LaFleur, B., Ferrone, S., Kaminishi, M., Montgomery, E. A., & Goldenring, J. R. (2006) · Surgery · doi:10.1016/j.surg.2006.05.009 · Cited by 97 · see citing works
Antoniou, A. N., Ford, S., Alphey, M., Osborne, A. R., Elliott, T. J., & Powis, S. J. (2002) · The EMBO Journal · doi:10.1093/emboj/21.11.2655 · Cited by 94 · see citing works
Chaput, N., de Botton, S., Obéid, M., Apétoh, L., Ghiringhelli, F., Panaretakis, T., Flament, C., Zitvogel, L., & Kroemer, G. (2007) · Journal of Molecular Medicine · doi:10.1007/s00109-007-0214-1 · Cited by 83 · see citing works
Self-citationFunctions of ERp57 in the Folding and Assembly of Major Histocompatibility Complex Class I Molecules
Zhang, Y.-N., Baig, E., & Williams, D. B. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m512073200 · Cited by 76 · see citing works
Martin, V., Groenendyk, J., Steiner, S. S., Guo, L., Dabrowska, M., Parker, J. M. R., Müller‐Esterl, W., Opas, M., & Michalak, M. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508302200 · Cited by 68 · see citing works
Homma, S., Komita, H., Sagawa, Y., Ohno, T., & Toda, G. (2005) · Immunology · doi:10.1111/j.1365-2567.2005.02179.x · Cited by 50 · see citing works
Identification and Characterization of Structural Domains of Human ERp57
Silvennoinen, L., Myllyharju, J., Ruoppolo, M., Orrù, S., Caterino, M., Kivirikko, K. I., & Koivunen, P. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313054200 · Cited by 49 · see citing works
Interaction of ERp57 and tapasin in the generation of MHC class I–peptide complexes
Garbi, N., Hämmerling, G. J., & Tanaka, S. (2006) · Current Opinion in Immunology · doi:10.1016/j.coi.2006.11.013 · Cited by 49 · see citing works
Interaction of Calreticulin with CD40 Ligand, TRAIL and Fas Ligand
Duus, K., Pagh, R., Holmskov, U., Højrup, P., Skov, S., & Houen, G. (2007) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.2007.01999.x · Cited by 28 · see citing works
Mimura, Y., Mimura‐Kimura, Y., Doores, K. J., Golgher, D. B., Davis, B. G., Dwek, R. A., Rudd, P. M., & Elliott, T. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701307104 · Cited by 14 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007; 13: 1050-1059.
Cited by
Sorted by citations
Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., et al. (2018) · Cell Death & Differentiation · doi:10.1038/s41418-017-0012-4 · Cited by 6,680 · see citing works
Self-citationImmunogenic Cell Death in Cancer Therapy
Kroemer, G., Galluzzi, L., Kepp, O., & Zitvogel, L. (2013) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-100008 · Cited by 3,303 · see citing works
Self-citationImmunogenic cell death and DAMPs in cancer therapy
Krysko, D. V., Garg, A. D., Kaczmarek, A., Krysko, O., Agostinis, P., & Vandenabeele, P. (2012) · Nature Reviews Cancer · doi:10.1038/nrc3380 · Cited by 3,223 · see citing works
Immunogenic cell death in cancer and infectious disease
Galluzzi, L., Buqué, A., Kepp, O., Zitvogel, L., & Kroemer, G. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2016.107 · Cited by 3,119 · see citing works
Self-citationImmunogenic and tolerogenic cell death
Green, D. R., Ferguson, T., Zitvogel, L., & Kroemer, G. (2009) · Nature Reviews Immunology · doi:10.1038/nri2545 · Cited by 1,176 · see citing works
Self-citationImmunogenic death of colon cancer cells treated with oxaliplatin
Tesnière, A., Schlemmer, F., Boige, V., Kepp, O., Martins, I., Ghiringhelli, F., Aymeric, L., Michaud, M., Apétoh, L., Barault, L., et al. (2009) · Oncogene · doi:10.1038/onc.2009.356 · Cited by 1,177 · see citing works
Self-citationConsensus guidelines for the definition, detection and interpretation of immunogenic cell death
Galluzzi, L., Vitale, I., Warren, S., Adjemian, S., Agostinis, P., Buqué, A., Chan, T. A.-T., Coukos, G., Demaria, S., Deutsch, É., et al. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2019-000337 · Cited by 1,151 · see citing works
Self-citationCombining Radiotherapy and Cancer Immunotherapy: A Paradigm Shift
Formenti, S. C., & Demaria, S. (2013) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djs629 · Cited by 1,058 · see citing works
Nanoparticle‐Mediated Immunogenic Cell Death Enables and Potentiates Cancer Immunotherapy
Duan, X., Chan, C., & Lin, W. (2018) · Angewandte Chemie International Edition · doi:10.1002/anie.201804882 · Cited by 1,035 · see citing works
Phagocytosis checkpoints as new targets for cancer immunotherapy
Feng, M., Jiang, W., Kim, B. Y. S., Zhang, C. C., Fu, Y., & Weissman, I. L. (2019) · Nature reviews. Cancer · doi:10.1038/s41568-019-0183-z · Cited by 914 · see citing works
Mechanisms of pre‐apoptotic calreticulin exposure in immunogenic cell death
Panaretakis, T., Kepp, O., Brockmeier, U., Tesniere, A., Bjorklund, A., Chapman, D. C., Durchschlag, M., Joza, N., Pierron, G., van Endert, P., et al. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.1 · Cited by 848 · see citing works
Self-citationConsensus guidelines for the detection of immunogenic cell death
Kepp, O., Senovilla, L., Vitale, I., Vacchelli, E., Adjemian, S., Agostinis, P., Apetoh, L., Aranda, F., Barnaba, V., Bloy, N., et al. (2014) · OncoImmunology · doi:10.4161/21624011.2014.955691 · Cited by 832 · see citing works
Self-citationA novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death
Garg, A. D., Krysko, D. V., Verfaillie, T., Kaczmarek, A., Ferreira, G. B., Marysael, T., Rubio, N., Firczuk, M., Mathieu, C., Roebroek, A. J. M., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2011.497 · Cited by 800 · see citing works
Chao, M. P., Jaiswal, S., Weissman-Tsukamoto, R., Alizadeh, A. A., Gentles, A. J., Volkmer, J., Weiskopf, K., Willingham, S. B., Raveh, T., Park, C. Y., et al. (2010) · Science Translational Medicine · doi:10.1126/scitranslmed.3001375 · Cited by 776 · see citing works
Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum
Michalak, M., Groenendyk, J., Szabo, E., Gold, L. I., & Opas, M. (2009) · Biochemical Journal · doi:10.1042/bj20081847 · Cited by 718 · see citing works
Mitochondrial and endoplasmic reticulum calcium homeostasis and cell death
Marchi, S., Patergnani, S., Missiroli, S., Morciano, G., Rimessi, A., Wieckowski, M. R., Giorgi, C., & Pinton, P. (2017) · Cell Calcium · doi:10.1016/j.ceca.2017.05.003 · Cited by 695 · see citing works
Immune parameters affecting the efficacy of chemotherapeutic regimens
Zitvogel, L., Kepp, O., & Kroemer, G. (2011) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2010.223 · Cited by 665 · see citing works
Self-citationLuo, B., & Lee, A. S. (2012) · Oncogene · doi:10.1038/onc.2012.130 · Cited by 559 · see citing works
Radiotherapy combination opportunities leveraging immunity for the next oncology practice
Herrera, F. G., Bourhis, J., & Coukos, G. (2016) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21358 · Cited by 511 · see citing works
Multiple Drug Resistance Mechanisms in Cancer
Baguley, B. C. (2010) · Molecular Biotechnology · doi:10.1007/s12033-010-9321-2 · Cited by 481 · see citing works
Cell death and immunity in cancer: From danger signals to mimicry of pathogen defense responses
Garg, A. D., & Agostinis, P. (2017) · Immunological Reviews · doi:10.1111/imr.12574 · Cited by 448 · see citing works
An Immunosurveillance Mechanism Controls Cancer Cell Ploidy
Senovilla, L., Vitale, I., Martins, I., Tailler, M., Pailleret, C., Michaud, M., Galluzzi, L., Adjemian, S., Kepp, O., Niso-Santano, M., et al. (2012) · Science · doi:10.1126/science.1224922 · Cited by 436 · see citing works
Self-citationCardiac Glycosides Exert Anticancer Effects by Inducing Immunogenic Cell Death
Menger, L., Vacchelli, E., Adjemian, S., Martins, I., Ma, Y., Shen, S., Yamazaki, T., Sukkurwala, A. Q., Michaud, M., Mignot, G., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003807 · Cited by 423 · see citing works
Self-citationMartins, I., Kepp, O., Schlemmer, F., Adjemian, S., Tailler, M., Shen, S., Michaud, M., Menger, L., Gdoura, A., Tajeddine, N., et al. (2010) · Oncogene · doi:10.1038/onc.2010.500 · Cited by 414 · see citing works
Self-citationMolecular and Translational Classifications of DAMPs in Immunogenic Cell Death
Garg, A. D., Galluzzi, L., Apétoh, L., Baert, T., Birge, R. B., Pedro, J. M. B., Breckpot, K., Brough, D., Chaurio, R. A., Cirone, M., et al. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00588 · Cited by 409 · see citing works
Self-citationFucikova, J. P., Špíšek, R., Kroemer, G., & Galluzzi, L. (2020) · Cell Research · doi:10.1038/s41422-020-0383-9 · Cited by 408 · see citing works
Self-citationHuman Tumor Cells Killed by Anthracyclines Induce a Tumor-Specific Immune Response
Fucikova, J. P., Králíková, P., Fialová, A., Brtnický, T., Rob, L., Bartůňková, J., & Špíšek, R. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-0950 · Cited by 393 · see citing works
Combinatorial Strategies for the Induction of Immunogenic Cell Death
Bezu, L., Gomes-da-Silva, L. C., Dewitte, H., Breckpot, K., Fucikova, J. P., Špíšek, R., Galluzzi, L., Kepp, O., & Kroemer, G. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00187 · Cited by 389 · see citing works
Self-citationImmunogenic Tumor Cell Death for Optimal Anticancer Therapy: The Calreticulin Exposure Pathway
Zitvogel, L., Kepp, O., Senovilla, L., Menger, L., Chaput, N., & Kroemer, G. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-2891 · Cited by 388 · see citing works
Self-citationCalreticulin: non‐endoplasmic reticulum functions in physiology and disease
Gold, L. I., Eggleton, P., Sweetwyne, M. T., Duyn, L. B. V., Greives, M. R., Naylor, S., Michalak, M., & Murphy-Ullrich, J. E. (2009) · The FASEB Journal · doi:10.1096/fj.09-145482 · Cited by 382 · see citing works
Tumor Cell Death and ATP Release Prime Dendritic Cells and Efficient Anticancer Immunity
Aymeric, L., Apétoh, L., Ghiringhelli, F., Tesnière, A., Martins, I., Kroemer, G., Smyth, M. J., & Zitvogel, L. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-3566 · Cited by 380 · see citing works
Self-citationMultimodal immunogenic cancer cell death as a consequence of anticancer cytotoxic treatments
Inoue, H., & Tani, K. (2013) · Cell Death and Differentiation · doi:10.1038/cdd.2013.84 · Cited by 352 · see citing works
Contribution of IL-17–producing γδ T cells to the efficacy of anticancer chemotherapy
Ma, Y., Aymeric, L., Locher, C., Mattarollo, S. R., Delahaye, N. F., Pereira, P., Boucontet, L., Apétoh, L., Ghiringhelli, F., Casares, N., et al. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20100269 · Cited by 338 · see citing works
Self-citationCell death in pancreatic cancer: from pathogenesis to therapy
Chen, X., Zeh, H. J., Kang, R., Kroemer, G., & Tang, D. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-021-00486-6 · Cited by 339 · see citing works
Self-citationPivotal Role of Innate and Adaptive Immunity in Anthracycline Chemotherapy of Established Tumors
Mattarollo, S. R., Loi, S., Duret, H., Ma, Y., Zitvogel, L., & Smyth, M. J. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-0753 · Cited by 335 · see citing works
Self-citationOncolytic viruses as therapeutic cancer vaccines
Bartlett, D. L., Liu, Z., Sathaiah, M., Ravindranathan, R., Guo, Z., He, Y., & Guo, Z. S. (2013) · Molecular Cancer · doi:10.1186/1476-4598-12-103 · Cited by 326 · see citing works
Immunogenic effects of chemotherapy-induced tumor cell death
Wang, Y., Fletcher, R., Yu, J., & Zhang, L. (2018) · Genes & Diseases · doi:10.1016/j.gendis.2018.05.003 · Cited by 316 · see citing works
Immunogenic cancer cell death: a key-lock paradigm
Tesnière, A., Apétoh, L., Ghiringhelli, F., Joza, N. A., Panaretakis, T., Kepp, O., Schlemmer, F., Zitvogel, L., & Kroemer, G. (2008) · Current Opinion in Immunology · doi:10.1016/j.coi.2008.05.007 · Cited by 303 · see citing works
Self-citationMolecular determinants of immunogenic cell death elicited by anticancer chemotherapy
Kepp, O., Galluzzi, L., Martins, I., Schlemmer, F., Adjemian, S., Michaud, M., Sukkurwala, A. Q., Menger, L., Zitvogel, L., & Kroemer, G. (2011) · Cancer and Metastasis Reviews · doi:10.1007/s10555-011-9273-4 · Cited by 296 · see citing works
Self-citationGarg, A. D., Krysko, D. V., Vandenabeele, P., & Agostinis, P. (2011) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-011-1184-2 · Cited by 293 · see citing works
Hodge, J. W., Garnett‐Benson, C., Farsaci, B., Palena, C., Tsang, K.-Y., Ferrone, S., & Gameiro, S. R. (2013) · International Journal of Cancer · doi:10.1002/ijc.28070 · Cited by 283 · see citing works
Tipping the immunostimulatory and inhibitory DAMP balance to harness immunogenic cell death
Hayashi, K., Nikolos, F., Lee, Y. C., Jain, A., Tsouko, E., Gao, H., Kasabyan, A., Leung, H. E., Osipov, A., Jung, S. Y., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19970-9 · Cited by 275 · see citing works
Vacchelli, E., Senovilla, L., Eggermont, A. M. M., Fridman, W. H., Galon, J., Zitvogel, L., Kroemer, G., & Galluzzi, L. (2013) · OncoImmunology · doi:10.4161/onci.23510 · Cited by 265 · see citing works
Self-citationImmunogenic cell death in anticancer chemotherapy and its impact on clinical studies
Wang, Q., Ju, X., Wang, J., Fan, Y. J., Ren, M., & Zhang, H. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.08.028 · Cited by 265 · see citing works
Zhang, S., Wang, J., Kong, Z., Sun, X., He, Z., Sun, B., Luo, C., & Sun, J. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121433 · Cited by 258 · see citing works
Programmed cell removal: a new obstacle in the road to developing cancer
Chao, M. P., Majeti, R., & Weissman, I. L. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3171 · Cited by 246 · see citing works
Crosstalk between ER stress and immunogenic cell death
Kepp, O., Menger, L., Vacchelli, E., Locher, C., Adjemian, S., Yamazaki, T., Martins, I., Sukkurwala, A. Q., Michaud, M., Senovilla, L., et al. (2013) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2013.05.001 · Cited by 233 · see citing works
Self-citationGarg, A. D., Ruysscher, D. D., & Agostinis, P. (2015) · OncoImmunology · doi:10.1080/2162402x.2015.1069938 · Cited by 229 · see citing works
Danger signalling during cancer cell death: origins, plasticity and regulation
Garg, A. D., Martin, S., Gołąb, J., & Agostinis, P. (2013) · Cell Death and Differentiation · doi:10.1038/cdd.2013.48 · Cited by 225 · see citing works
Origin and Consequences of Necroinflammation
Sarhan, M., Land, W. G., Tonnus, W., Hugo, C., & Linkermann, A. (2018) · Physiological Reviews · doi:10.1152/physrev.00041.2016 · Cited by 210 · see citing works
Calreticulin in the immune system: ins and outs
Raghavan, M., Wijeyesakere, S. J., Peters, L. R., & Cid, N. D. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.08.002 · Cited by 204 · see citing works
Immunogenic cell death modalities and their impact on cancer treatment
Kepp, O., Tesnière, A., Schlemmer, F., Michaud, M., Senovilla, L., Zitvogel, L., & Kroemer, G. (2009) · APOPTOSIS · doi:10.1007/s10495-008-0303-9 · Cited by 203 · see citing works
Self-citationNanomaterial-Based Tumor Photothermal Immunotherapy
Xu, P., & Liang, F. (2020) · International Journal of Nanomedicine · doi:10.2147/ijn.s249252 · Cited by 200 · see citing works
Physical modalities inducing immunogenic tumor cell death for cancer immunotherapy
Adkins, I., Fucikova, J., Garg, A. D., Agostinis, P., & Špíšek, R. (2014) · OncoImmunology · doi:10.4161/21624011.2014.968434 · Cited by 200 · see citing works
Paclitaxel Induces Immunogenic Cell Death in Ovarian Cancer via TLR4/IKK2/SNARE-Dependent Exocytosis
Lau, T., Chan, L. K. Y., Man, G. C. W., Wong, C. H., Lee, J. H. S., Yim, S. F., Cheung, T. H., McNeish, I. A., & Kwong, J. (2020) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-19-0616 · Cited by 197 · see citing works
Chemotherapy and radiotherapy: Cryptic anticancer vaccines
Ma, Y., Kepp, O., Ghiringhelli, F., Apétoh, L., Aymeric, L., Locher, C., Tesnière, A., Martins, I., Ly, A., Haynes, N. M., et al. (2010) · Seminars in Immunology · doi:10.1016/j.smim.2010.03.001 · Cited by 193 · see citing works
Self-citationRadiation Therapy Induces Macrophages to Suppress T-Cell Responses Against Pancreatic Tumors in Mice
Seifert, L., Werba, G., Tiwari, S., Ly, N. N. G., Nguy, S., Alothman, S., Alqunaibit, D., Avanzi, A., Daley, D., Barilla, R., et al. (2016) · Gastroenterology · doi:10.1053/j.gastro.2016.02.070 · Cited by 193 · see citing works
Gold Nanoparticles: Construction for Drug Delivery and Application in Cancer Immunotherapy
Huang, H., Liu, R., Yang, J., Dai, J., Fan, S., Pi, J., Wei, Y., & Guo, X. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15071868 · Cited by 197 · see citing works
The immune mechanisms of abscopal effect in radiation therapy
Grass, G. D., Krishna, N., & Kim, S. (2015) · Current Problems in Cancer · doi:10.1016/j.currproblcancer.2015.10.003 · Cited by 176 · see citing works
Transplantation and Damage-Associated Molecular Patterns (DAMPs)
Land, W. G., Agostinis, P., Gasser, S., Garg, A. D., & Linkermann, A. (2016) · American Journal of Transplantation · doi:10.1111/ajt.13963 · Cited by 166 · see citing works
Stanniocalcin 1 is a phagocytosis checkpoint driving tumor immune resistance
Lin, H., Kryczek, I., Li, S., Green, M. D., Ali, A., Hamasha, R., Wei, S., Vatan, L., Szeliga, W., Grove, S., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2020.12.023 · Cited by 164 · see citing works
Current Approaches for Combination Therapy of Cancer: The Role of Immunogenic Cell Death
Asadzadeh, Z., Safarzadeh, E., Safaei, S., Baradaran, A., Mohammadi, A., Hajiasgharzadeh, K., Derakhshani, A., Argentiero, A., Silvestris, N., & Baradaran, B. (2020) · Cancers · doi:10.3390/cancers12041047 · Cited by 157 · see citing works
Sonodynamic therapy‐assisted immunotherapy: A novel modality for cancer treatment
Zhang, Q., Bao, C., Cai, X., Jin, L., Sun, L., Lang, Y., & Li, L. (2018) · Cancer Science · doi:10.1111/cas.13578 · Cited by 157 · see citing works
Emerging roles for the pro-oncogenic anterior gradient-2 in cancer development
Chevet, É., Fessart, D., Delom, F., Mulot, A., Vojtěšek, B., Hrstka, R., Murray, E., Gray, T. A., & Hupp, T. R. (2012) · Oncogene · doi:10.1038/onc.2012.346 · Cited by 156 · see citing works
Land, W. G. (2015) · Sultan Qaboos University medical journal · doi:10.18295/2075-0528.1676 · Cited by 153 · see citing works
Opzoomer, J. W., Sosnowska, D., Anstee, J. E., Spicer, J. F., & Arnold, J. N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01654 · Cited by 150 · see citing works
Rational combinations of immunotherapy with radiotherapy in ovarian cancer
Herrera, F. G., Irving, M. B., Kandalaft, L. E., & Coukos, G. (2019) · The Lancet Oncology · doi:10.1016/s1470-2045(19)30401-2 · Cited by 148 · see citing works
Higa, A., Mulot, A., Delom, F., Bouchecareilh, M., Nguyên, D. T., Boismenu, D., Wise, M. J., & Chevet, É. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.275529 · Cited by 145 · see citing works
The oncolytic peptide LTX-315 triggers immunogenic cell death
Zhou, H., Forveille, S., Sauvat, A., Yamazaki, T., Senovilla, L., Ma, Y., Liu, P., Yang, H., Bezu, L., Müller, K., et al. (2016) · Cell Death and Disease · doi:10.1038/cddis.2016.47 · Cited by 145 · see citing works
Self-citationScreening of novel immunogenic cell death inducers within the NCI Mechanistic Diversity Set
Sukkurwala, A. Q., Adjemian, S., Senovilla, L., Michaud, M., Spaggiari, S., Vacchelli, E., Baracco, E. E., Galluzzi, L., Zitvogel, L., Kepp, O., et al. (2014) · OncoImmunology · doi:10.4161/onci.28473 · Cited by 139 · see citing works
Self-citationStress-induced cellular responses in immunogenic cell death: Implications for cancer immunotherapy
Radogna, F., & Diederich, M. F. (2018) · Biochemical Pharmacology · doi:10.1016/j.bcp.2018.02.006 · Cited by 142 · see citing works
Zappasodi, R., Pupa, S. M., Ghedini, G. C., Bongarzone, I., Magni, M., Cabras, A. D., Colombo, M. P., Carlo‐Stella, C., Gianni, A. M., & Nicola, M. D. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1825 · Cited by 139 · see citing works
Wiersma, V. R., Michalak, M., Abdullah, T. M., Bremer, E., & Eggleton, P. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2015.00007 · Cited by 140 · see citing works
ERp57/GRP58: A protein with multiple functions
Turano, C., Gaucci, E., Grillo, C., & Chichiarelli, S. (2011) · Cellular & Molecular Biology Letters · doi:10.2478/s11658-011-0022-z · Cited by 134 · see citing works
Tsai, Y.-L., Ha, D. P., Zhao, H., Carlos, A. J., Wei, S., Pun, T. K., Wu, K., Zandi, E., Kelly, K. R., & Lee, A. S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1714866115 · Cited by 132 · see citing works
Multidrug Resistance in Cancer
Baguley, B. C. (2009) · Methods in molecular biology · doi:10.1007/978-1-60761-416-6_1 · Cited by 131 · see citing works
Biomarkers of Radiotherapy-Induced Immunogenic Cell Death
Vaes, R. D. W., Hendriks, L. E. L., Vooijs, M., & Ruysscher, D. D. (2021) · Cells · doi:10.3390/cells10040930 · Cited by 130 · see citing works
Panzarini, E., Inguscio, V., Fimia, G. M., & Dini, L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0105778 · Cited by 127 · see citing works
Self-citationWémeau, M., Kepp, O., Tesnière, A., Panaretakis, T., Flament, C., de Botton, S., Zitvogel, L., Kroemer, G., & Chaput, N. (2010) · Cell Death and Disease · doi:10.1038/cddis.2010.82 · Cited by 128 · see citing works
Self-citationImmunogenic Apoptosis as a Novel Tool for Anticancer Vaccine Development
Montico, B., Nigro, A., Casolaro, V., & Col, J. D. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020594 · Cited by 128 · see citing works
Radiation triggering immune response and inflammation
Hekim, N., Çetin, Z., Nikitaki, Z., Çört, A., & Saygılı, E. İ. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.04.016 · Cited by 124 · see citing works
Functional Roles of Calreticulin in Cancer Biology
Lu, Y.-C., Weng, W., & Lee, H. (2015) · BioMed Research International · doi:10.1155/2015/526524 · Cited by 122 · see citing works
Fabian, K. P., Wolfson, B., & Hodge, J. W. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.728018 · Cited by 125 · see citing works
The synergistic effect of radiotherapy and immunotherapy: A promising but not simple partnership
Chajon, É., Castelli, J., Marsiglia, H. R., & de Crevoisier, R. (2017) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2017.01.017 · Cited by 119 · see citing works
Bugaut, H., Bruchard, M., Berger, H., Dérangère, V., Odoul, L., Euvrard, R., Ladoire, S., Chalmin, F., Végran, F., Rébé, C., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065181 · Cited by 119 · see citing works
The immunogenicity of tumor cell death
Kepp, O., Tesnière, A., Zitvogel, L., & Kroemer, G. (2008) · Current Opinion in Oncology · doi:10.1097/cco.0b013e32831bc375 · Cited by 117 · see citing works
Self-citationVacchelli, E., Galluzzi, L., Fridman, W. H., Galon, J., Sautès‐Fridman, C., Tartour, É., & Kroemer, G. (2012) · OncoImmunology · doi:10.4161/onci.1.2.19026 · Cited by 115 · see citing works
Self-citationKiełbik, M., Szulc-Kiełbik, I., & Klink, M. (2021) · Cells · doi:10.3390/cells10010130 · Cited by 116 · see citing works
Harnessing γδ T cells in anticancer immunotherapy
Hannani, D., Ma, Y., Yamazaki, T., Déchanet‐Merville, J., Kroemer, G., & Zitvogel, L. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.01.006 · Cited by 110 · see citing works
Self-citationCancer immunogenicity, danger signals, and DAMPs: What, when, and how?
Garg, A. D., Dudek, A. M., & Agostinis, P. (2013) · BioFactors · doi:10.1002/biof.1125 · Cited by 108 · see citing works
Combination of glycolysis inhibition with chemotherapy results in an antitumor immune response
Bénéteau, M., Zunino, B., Jacquin, M. A., Meynet, O., Chiche, J., Pradelli, L. A., Marchetti, S., Cornille, A., Carlès, M., & Ricci, J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206360109 · Cited by 106 · see citing works
Immunogenic anti-cancer chemotherapy as an emerging concept
Haynes, N. M., der Most, R. G. V., Lake, R., & Smyth, M. J. (2008) · Current Opinion in Immunology · doi:10.1016/j.coi.2008.05.008 · Cited by 104 · see citing works
Peters, L. R., & Raghavan, M. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1100690 · Cited by 104 · see citing works
ERp57 Modulates STAT3 Signaling from the Lumen of the Endoplasmic Reticulum
Coe, H., Jung, J., Groenendyk, J., Prins, D., & Michalak, M. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.054015 · Cited by 103 · see citing works
Murshid, A., Gong, J., Stevenson, M. A., & Calderwood, S. K. (2011) · Expert Review of Vaccines · doi:10.1586/erv.11.124 · Cited by 103 · see citing works
Bloy, N., Garcia, P., Laumont, C. M., Pitt, J. M., Sistigu, A., Stoll, G., Yamazaki, T., Bonneil, É., Buqué, A., Humeau, J. F., et al. (2017) · Immunological Reviews · doi:10.1111/imr.12582 · Cited by 103 · see citing works
Self-citationMultifunctional molecule ERp57: From cancer to neurodegenerative diseases
Hettinghouse, A., Liu, R., & Liu, C.-J. (2017) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2017.07.011 · Cited by 102 · see citing works
van Vloten, J. P., Workenhe, S. T., Wootton, S. K., Mossman, K. L., & Bridle, B. W. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701021 · Cited by 101 · see citing works
Yang, H., Yamazaki, T., Pietrocola, F., Zhou, H., Zitvogel, L., Ma, Y., & Kroemer, G. (2015) · Cancer Research · doi:10.1158/0008-5472.can-15-1122 · Cited by 98 · see citing works
Self-citationKaneno, R., Shurin, G. V., Kaneno, F. M., Naiditch, H., Luo, J., & Shurin, M. R. (2011) · Cellular Oncology · doi:10.1007/s13402-010-0005-5 · Cited by 99 · see citing works
- Authors
- Panaretakis, T., Joza, N., Modjtahedi, N., Tesniere, A., Vitale, I., Durchschlag, M., Fimia, G. M., Kepp, O., Piacentini, M., Froehlich, K.-U., van Endert, P., Zitvogel, L., Madeo, F., & Kroemer, G.
- Affiliations
- Inserm (FR)
- Université Paris-Sud (FR)
- University of Graz (AT)
- Istituto Nazionale per le Malattie Infettive Lazzaro Spallanzani (IT)
- University of Rome Tor Vergata (IT)
- Corresponding author
- Kroemer, G
- ORCID
- Venue
- Cell Death & Differentiation
- Published
- 2008-05-09
- Volume
- 15
- Issue
- 9
- Pages
- 1499-1509
- ISSN
- 1350-9047 (ISSN-L)
- 1476-5403
- OpenAlex
- W1991189794
- Cited by
- 344
- References
- 38
- Citations by year
- 2026: 10 · 2025: 9 · 2024: 18 · 2023: 21 · 2022: 19 · 2021: 22 · 2020: 22 · 2019: 15 · 2018: 21 · 2017: 16 · 2016: 22 · 2015: 17 · 2014: 15 · 2013: 22 · 2012: 21
- FWCI
- 10.64
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Cell Death and Differentiation (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- INFM-OAR (INFN Catania) (submittedVersion, other-oa)
- Zenodo (CERN European Organization for Nuclear Research) (other-oa)
- Funders
- European Commission
- Institut National de la Santé et de la Recherche Médicale
- Ministero della Salute
- Vetenskapsrådet
- Fondation de France
- Associazione Italiana per la Ricerca sul Cancro
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- calreticulin, ERp57, protein disulfide isomerase, calreticulin exposure, immunogenic cell death, chemoresistance, antitumor immunity, endoplasmic reticulum proteins, protein-protein interaction
- MeSH terms
- Amino Acid Sequence, Animals, Antineoplastic Agents, Cell Membrane, Cells, Cultured, Female, Humans, Mice, Inbred BALB C, Mitoxantrone, Molecular Sequence Data, Neoplasms, Experimental, Apoptosis, Gene Deletion, Protein Disulfide-Isomerases, Protein Transport, Calreticulin, Cell Line, Tumor, Mice
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
