Cell Death–Stimulated Cell Proliferation: A Tissue Regeneration Mechanism Usurped by Tumors During Radiotherapy

Zimmerman, Mary A.; Huang, Qian; Li, Fang; Liu, Xinjiang; Li, Chuan-Yuan

doi:10.1016/j.semradonc.2013.05.003

Cited by 59Cell death mechanisms and regulationEffects of Radiation ExposureCancer Cells and Metastasis

Cell Death–Stimulated Cell Proliferation: A Tissue Regeneration Mechanism Usurped by Tumors During Radiotherapy

Open access

Zimmerman, Mary A., Huang, Qian, Li, Fang, Liu, Xinjiang, Li, Chuan-Yuan·2013·Seminars in Radiation Oncology

DOI 10.1016/j.semradonc.2013.05.003PMC PMC3891050

Open this paper in CoChat — free account

Abstract

Summary Death of all the cancer cells in a tumor is the ultimate goal of cancer therapy. Therefore much of the current effort in cancer research is focused on activating cellular machinery that facilitates cell death such as factors involved in causing apoptosis. However, recently a number of studies point to some counter-intuitive roles for apoptotic caspases in radiation therapy as well as in tissue regeneration. It appears that a major function of apoptotic caspases is to facilitate tissue regeneration and tumor cell repopulation during cancer therapy. Because tumor cell repopulation has been shown to be important for local tumor relapse, understanding the molecular mechanisms behind tumor repopulation will be important to enhance cancer radiotherapy. In this review, we discuss our current knowledge of these potentially paradigm-changing phenomena and mechanisms in various organisms and their implications on the development of novel cancer therapeutics and strategies.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.semradonc.2013.05.003

Cites

100 of 100 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Mild caspase induction promotes tumour growth.
“In addition, misregulation of the Hippo, JNK or Wg pathway is also linked to activation of caspases mediated apoptosis, and recently mild caspase induction was shown to promote tumour growth (66,67).”
From A Tumour-Specific Molecular Network Promotes Tumour Growth in Drosophila by Enforcing a JNK-YKI Feedforward Loop (2023) · cites this paper as [66]
The section “Cell death stimulated tumor repopulation during radiotherapy” reports that caspase-3 activity in irradiated, dying feeder cells promotes tumor-cell proliferation. The Summary also describes low-to-moderate caspase activation in some tumors, but does not show that mild caspase induction itself promotes tumor growth. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Misregulation of the Hippo, JNK or Wg pathway is linked to activation of caspases mediated apoptosis.
“In addition, misregulation of the Hippo, JNK or Wg pathway is also linked to activation of caspases mediated apoptosis, and recently mild caspase induction was shown to promote tumour growth (66,67).”
From A Tumour-Specific Molecular Network Promotes Tumour Growth in Drosophila by Enforcing a JNK-YKI Feedforward Loop (2023) · cites this paper as [66]
The sections “Cell death: the current paradigm” and “Compensatory proliferation, cell death induced tissue regeneration in lower organisms” describe caspase activation in apoptosis and link apoptotic cells to Wingless signaling; the paper also discusses JNK in compensatory proliferation. They do not say that misregulation of Hippo, JNK, or Wg activates caspase-mediated apoptosis, and the cited passages do not address Hippo. (LLM, conf=0.84)
Experimental — accuracy not yet measured

Self-check

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

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

Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
The hallmarks of cancer
Hanahan, D., & Weinberg, R. A. (2000) · Cell · doi:10.1016/s0092-8674(00)81683-9 · Cited by 29,219 · see citing works
Apoptosis: A Basic Biological Phenomenon with Wideranging Implications in Tissue Kinetics
Kerr, J. F. R., Wyllie, A. H., & Currie, A. R. (1972) · British Journal of Cancer · doi:10.1038/bjc.1972.33 · Cited by 15,673 · see citing works
Wound repair and regeneration
Gurtner, G. C., Werner, S., Barrandon, Y., & Longaker, M. T. (2008) · Nature · doi:10.1038/nature07039 · Cited by 6,542 · see citing works
The DNA-damage response in human biology and disease
Jackson, S. P., & Bartek, J. (2009) · Nature · doi:10.1038/nature08467 · Cited by 6,092 · see citing works
Autophagy: cellular and molecular mechanisms
Glick, D. R., Barth, S., & Macleod, K. F. (2010) · The Journal of Pathology · doi:10.1002/path.2697 · Cited by 3,815 · see citing works
Proliferation, cell cycle and apoptosis in cancer
Evan, G. I., & Vousden, K. H. (2001) · Nature · doi:10.1038/35077213 · Cited by 3,383 · see citing works
Liver Regeneration
Michalopoulos, G. K., & DeFrances, M. C. (1997) · Science · doi:10.1126/science.276.5309.60 · Cited by 2,828 · see citing works
The Bcl-2 apoptotic switch in cancer development and therapy
Adams, J. M., & Cory, S. (2007) · Oncogene · doi:10.1038/sj.onc.1210220 · Cited by 2,178 · see citing works
Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis
Degenhardt, K., Mathew, R., Beaudoin, B., Bray, K., Anderson, D., Chen, G., Mukherjee, C., Shi, Y., Gélinas, C., Fan, Y., et al. (2006) · Cancer Cell · doi:10.1016/j.ccr.2006.06.001 · Cited by 2,007 · see citing works
Apoptosis in cancer
Lowe, S. W., & Lin, A. W. (2000) · Carcinogenesis · doi:10.1093/carcin/21.3.485 · Cited by 1,867 · see citing works
Inhibition of Macroautophagy Triggers Apoptosis
Boya, P., González‐Polo, R. A., Casares, N., Perfettini, J., Dessen, P., Larochette, N., Métivier, D., Meley, D., Souquère, S., Yoshimori, T., et al. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.3.1025-1040.2005 · Cited by 1,629 · see citing works
The hazard of accelerated tumor clonogen repopulation during radiotherapy
Withers, H. R., Taylor, J. M. G., & Maciejewski, B. (1988) · Acta Oncologica · doi:10.3109/02841868809090333 · Cited by 1,605 · see citing works
DNA Damage Produced by Ionizing Radiation in Mammalian Cells: Identities, Mechanisms of Formation, and Reparability
Ward, J. F. (1988) · Progress in nucleic acid research and molecular biology · doi:10.1016/s0079-6603(08)60611-x · Cited by 1,499 · see citing works
Intrinsic tumour suppression
Lowe, S. W., Cepero, E., & Evan, G. I. (2004) · Nature · doi:10.1038/nature03098 · Cited by 1,309 · see citing works
Regulation of an ATG7 - beclin 1 Program of Autophagic Cell Death by Caspase-8
Yu, L., Alva, A. S., Su, H. C., Dutt, P., Freundt, E. C., Welsh, S. J., Baehrecke, E. H., & Lenardo, M. J. (2004) · Science · doi:10.1126/science.1096645 · Cited by 1,220 · see citing works
Life and death partners: apoptosis, autophagy and the cross-talk between them
Eisenberg‐Lerner, A., Bialik, S., Simon, H.-U., & Kimchi, A. (2009) · Cell Death and Differentiation · doi:10.1038/cdd.2009.33 · Cited by 1,183 · see citing works
IKKβ Couples Hepatocyte Death to Cytokine-Driven Compensatory Proliferation that Promotes Chemical Hepatocarcinogenesis
Maeda, S., Kamata, H., Luo, J., Leffert, H. L., & Karin, M. (2005) · Cell · doi:10.1016/j.cell.2005.04.014 · Cited by 1,165 · see citing works
Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis
North, T. E., Goessling, W., Walkley, C. R., Lengerke, C., Kopani, K. R., Lord, A. M., Weber, G. J., Bowman, T. V., Jang, I. H., Großer, T., et al. (2007) · Nature · doi:10.1038/nature05883 · Cited by 1,095 · see citing works
Cell death by necrosis: towards a molecular definition
Golstein, P., & Kroemer, G. (2007) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2006.11.001 · Cited by 1,044 · see citing works
Pathways of apoptotic and non-apoptotic death in tumour cells
Okada, H., & Mak, T. W. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1412 · Cited by 1,043 · see citing works
Toxic proteins released from mitochondria in cell death
Saelens, X., Festjens, N., Walle, L. V., van Gurp, M., Loo, G., & Vandenabeele, P. (2004) · Oncogene · doi:10.1038/sj.onc.1207523 · Cited by 977 · see citing works
Apoptotic Cells Induce Migration of Phagocytes via Caspase-3-Mediated Release of a Lipid Attraction Signal
Lauber, K., Bohn, E., Kröber, S. M., Xiao, Y.-J., Blumenthal, S. G., Lindemann, R. K., Marini, P., Wiedig, C., Zobywalski, A., Baksh, S., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00422-7 · Cited by 967 · see citing works
The role of apoptosis in cancer development and treatment response
Brown, J. M., & Attardi, L. D. (2005) · Nature reviews. Cancer · doi:10.1038/nrc1560 · Cited by 941 · see citing works
Caspase 3–mediated stimulation of tumor cell repopulation during cancer radiotherapy
Huang, Q., Li, F., Liu, X., Li, W., Shi, W., Liu, F.-F., O'Sullivan, B., He, Z., Peng, Y., Tan, A.-C., et al. (2011) · Nature Medicine · doi:10.1038/nm.2385 · Cited by 886 · see citing works
Self-citation
Prostaglandin E 2 Promotes Colon Cancer Cell Growth Through a G s -Axin-ß-Catenin Signaling Axis
Castellone, M. D., Teramoto, H., Williams, B. O., Druey, K. M., & Gutkind, J. S. (2005) · Science · doi:10.1126/science.1116221 · Cited by 884 · see citing works
Cell death modalities: classification and pathophysiological implications
Galluzzi, L., Maiuri, M. C., Vitale, I., Zischka, H., Castedo, M., Zitvogel, L., & Kroemer, G. (2007) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4402148 · Cited by 832 · see citing works
Defying death after DNA damage
Rich, T., Allen, R. L., & Wyllie, A. H. (2000) · Nature · doi:10.1038/35037717 · Cited by 724 · see citing works
Necrosis, a well-orchestrated form of cell demise: Signalling cascades, important mediators and concomitant immune response
Festjens, N., Vanden Berghe, T., & Vandenabeele, P. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.06.014 · Cited by 710 · see citing works
Genetic Interaction of PGE2 and Wnt Signaling Regulates Developmental Specification of Stem Cells and Regeneration
Goessling, W., North, T. E., Loewer, S., Lord, A. M., Lee, S., Stoick-Cooper, C. L., Weidinger, G., Puder, M., Daley, G. Q., Moon, R. T., et al. (2009) · Cell · doi:10.1016/j.cell.2009.01.015 · Cited by 699 · see citing works
Repopulation of cancer cells during therapy: an important cause of treatment failure
Kim, J. J., & Tannock, I. F. (2005) · Nature reviews. Cancer · doi:10.1038/nrc1650 · Cited by 690 · see citing works
Caspases: pharmacological manipulation of cell death
Lavrik, I. N. (2005) · Journal of Clinical Investigation · doi:10.1172/jci26252 · Cited by 646 · see citing works
Apoptotic Cells Can Induce Compensatory Cell Proliferation through the JNK and the Wingless Signaling Pathways
Ryoo, H. D., Gorenc, T., & Steller, H. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.08.019 · Cited by 624 · see citing works
A reproducible and well-tolerated method for 2/3 partial hepatectomy in mice
Mitchell, C., & Willenbring, H. (2008) · Nature Protocols · doi:10.1038/nprot.2008.80 · Cited by 577 · see citing works
Expansion and evolution of cell death programmes
Degterev, A., & Yuan, J. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2393 · Cited by 548 · see citing works
Radiation-induced apoptosis: Relevance to radiotherapy
Dewey, W. C., Ling, C. C., & Meyn, R. E. (1995) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(95)00214-8 · Cited by 523 · see citing works
Apoptotic Cells Activate the “Phoenix Rising” Pathway to Promote Wound Healing and Tissue Regeneration
Li, F., Huang, Q., Jiang, C., Peng, Y., Roop, D. R., Bedford, J. S., & Li, C. (2010) · Science Signaling · doi:10.1126/scisignal.2000634 · Cited by 494 · see citing works
Self-citation
Apoptotic Cells Provide an Unexpected Source of Wnt3 Signaling to Drive Hydra Head Regeneration
Chera, S., Ghila, L., Dobretz, K., Wenger, Y., Bauer, C., Buzgariu, W. C., Martinou, J., & Galliot, B. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.07.014 · Cited by 418 · see citing works
How death shapes life during development
Baehrecke, E. H. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm931 · Cited by 402 · see citing works
Alice in caspase land. A phylogenetic analysis of caspases from worm to man
Lamkanfi, M. (2002) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400989 · Cited by 401 · see citing works
Loss of hepatic NF-κB activity enhances chemical hepatocarcinogenesis through sustained c-Jun N-terminal kinase 1 activation
Sakurai, T., Maeda, S., Chang, L., & Karin, M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603499103 · Cited by 398 · see citing works
Combining radiotherapy and immunotherapy: A revived partnership
Demaria, S., Bhardwaj, N., McBride, W. H., & Formenti, S. C. (2005) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2005.06.032 · Cited by 376 · see citing works
Compensatory Proliferation Induced by Cell Death in the Drosophila Wing Disc Requires Activity of the Apical Cell Death Caspase Dronc in a Nonapoptotic Role
Huh, J. R., Guo, M., & Hay, B. A. (2004) · Current Biology · doi:10.1016/j.cub.2004.06.015 · Cited by 349 · see citing works
Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila
Pérez-Garijo, A., Martín, F. A., & Morata, G. (2004) · Development · doi:10.1242/dev.01432 · Cited by 339 · see citing works
Apoptosis, Stem Cells, and Tissue Regeneration
Bergmann, A., & Steller, H. (2010) · Science Signaling · doi:10.1126/scisignal.3145re8 · Cited by 325 · see citing works
Apoptosis-induced compensatory proliferation. The Cell is dead. Long live the Cell!
Fan, Y., & Bergmann, A. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.08.001 · Cited by 309 · see citing works
Coexistence of high levels of apoptotic signaling and inhibitor of apoptosis proteins in human tumor cells: implication for cancer specific therapy.
Yang, L. P. H., Cao, Z., Yan, H. M., & Wood, W. C. (2003) · PubMed · Cited by 272 · see citing works
C–Jun–N–Terminal Kinase Drives Cyclin D1 Expression and Proliferation During Liver Regeneration
Schwabe, R. F., Bradham, C. A., Uehara, T., Hatano, E., Bennett, B. L., Schoonhoven, R., & Brenner, D. A. (2003) · Hepatology · doi:10.1053/jhep.2003.50135 · Cited by 251 · see citing works
Distinct Mechanisms of Apoptosis-Induced Compensatory Proliferation in Proliferating and Differentiating Tissues in the Drosophila Eye
Fan, Y., & Bergmann, A. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.01.003 · Cited by 238 · see citing works
Regulation of the apoptosis–necrosis switch
Nicotera, P., & Melino, G. (2004) · Oncogene · doi:10.1038/sj.onc.1207559 · Cited by 238 · see citing works
Caspase control: protagonists of cancer cell apoptosis.
Fiandalo, M. V., & Kyprianou, N. (2012) · PubMed · Cited by 236 · see citing works
Fas-induced Arachidonic Acid Release Is Mediated by Ca2+-independent Phospholipase A2 but Not Cytosolic Phospholipase A2, Which Undergoes Proteolytic Inactivation
Atsumi, G., Tajima, M., Hadano, A., Nakatani, Y., Murakami, M., & Kudo, I. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.22.13870 · Cited by 235 · see citing works
The effects of X-rays on the proliferation dynamics of cells in the imaginal wing disc ofDrosophila melanogaster
Haynie, J. L., & Bryant, P. J. (1977) · Development Genes and Evolution · doi:10.1007/bf00848779 · Cited by 231 · see citing works
Prostaglandin E2 Stimulates the β-Catenin/T Cell Factor-dependent Transcription in Colon Cancer
Shao, J., Jung, C., Liu, C., & Sheng, H. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m413056200 · Cited by 215 · see citing works
Heterogeneity in the Development of Apoptosis in Irradiated Murine Tumours of Different Histologies
Meyn, R. E., Stephens, L. C., Ang, K. K., et al. (1993) · International Journal of Radiation Biology · doi:10.1080/09553009314551801 · Cited by 204 · see citing works
Autophagy in tumour suppression and promotion
Brech, A., Ahlquist, T. C., Lothe, R. A., & Stenmark, H. (2009) · Molecular Oncology · doi:10.1016/j.molonc.2009.05.007 · Cited by 189 · see citing works
Cell Kinetics and Radiation Biology
Denekamp, J. (1986) · International Journal of Radiation Biology and Related Studies in Physics Chemistry and Medicine · doi:10.1080/09553008514552591 · Cited by 177 · see citing works
Planarian Regeneration: Its End Is Its Beginning
Alvarado, A. S. (2006) · Cell · doi:10.1016/j.cell.2006.01.012 · Cited by 173 · see citing works
Autophagy upregulation by inhibitors of caspase-3 and mTOR enhances radiotherapy in a mouse model of lung cancer
Kim, K. W., Hwang, M., Moretti, L., Jaboin, J. J., Cha, Y. I., & Lu, J. (2008) · Autophagy · doi:10.4161/auto.6058 · Cited by 168 · see citing works
Dose fractionation and tumour repopulation in radiotherapy for bladder cancer
Maciejewski, B., & Majewski, S. (1991) · Radiotherapy and Oncology · doi:10.1016/0167-8140(91)90033-d · Cited by 167 · see citing works
Autophagy plays a protective role during zVAD-induced necrotic cell death
Wu, Y., Tan, H., Huang, Q., Kim, Y.-S., Pan, N., Ong, W., Liu, Z.-G., Ong, C. N., & Shen, H. (2008) · Autophagy · doi:10.4161/auto.5662 · Cited by 159 · see citing works
Self-citation
Apoptosis and mitotic cell death: their relative contributions to normal-tissue and tumour radiation response
West, C. (1997) · International Journal of Radiation Biology · doi:10.1080/095530097143716 · Cited by 158 · see citing works
Radiation Acts on the Microenvironment to Affect Breast Carcinogenesis by Distinct Mechanisms that Decrease Cancer Latency and Affect Tumor Type
Nguyen, D. H. A., Oketch‐Rabah, H. A., Illa-Bochaca, I., Geyer, F. C., Reis-Filho, J. S., Mao, J., Ravani, S. A., Zavadil, J., Borowsky, A. D., Jerry, D. J., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.03.011 · Cited by 150 · see citing works
Repopulation of tumour cells between cycles of chemotherapy: a neglected factor
Davis, A. J., & Tannock, I. F. (2000) · The Lancet Oncology · doi:10.1016/s1470-2045(00)00019-x · Cited by 150 · see citing works
Is compensatory growth a complicating factor in mouse teratology?
Snow, M. H. L., & Tam, P. P. L. (1979) · Nature · doi:10.1038/279555a0 · Cited by 146 · see citing works
Radiation-induced autophagy in normal and cancer cells: Towards novel cytoprotection and radio-sensitization policies?
Zois, C. E., & Koukourakis, M. I. (2009) · Autophagy · doi:10.4161/auto.5.4.7667 · Cited by 138 · see citing works
Caspase-3-dependent Activation of Calcium-independent Phospholipase A2 Enhances Cell Migration in Non-apoptotic Ovarian Cancer Cells
Zhao, X., Wang, D., Zhao, Z., Xiao, Y.-Y., Sengupta, S., Xiao, Y., Zhang, R., Lauber, K., Wesselborg, S., Feng, L., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m513105200 · Cited by 135 · see citing works
Applying radiobiological principles to combined modality treatment of head and neck cancer—The time factor
Peters, L. J., & Withers, H. R. (1997) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/s0360-3016(97)00466-5 · Cited by 125 · see citing works
Caspase-8 Interacts with the p85 Subunit of Phosphatidylinositol 3-Kinase to Regulate Cell Adhesion and Motility
Senft, J., Helfer, B. M., & Frisch, S. M. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-5755 · Cited by 120 · see citing works
Cell repopulation and overall treatment time
Trott, K.-R. (1990) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(90)90036-j · Cited by 115 · see citing works
Genetic Studies of the Relationship of Tumour–Host Cells: Effect of Tumour Cells killed by X-rays upon the Growth of Admixed Viable Cells
Révész, L. (1956) · Nature · doi:10.1038/1781391a0 · Cited by 115 · see citing works
Detection of apoptosis during planarian regeneration by the expression of apoptosis-related genes and TUNEL assay
Hwang, J. S., Kobayashi, C., Agata, K., Ikeo, K., & Gojobori, T. (2004) · Gene · doi:10.1016/j.gene.2004.02.034 · Cited by 107 · see citing works
Inhibition of programmed cell death impairs in vitro vascular‐like structure formation and reduces in vivo angiogenesis
Segura, I., Serrano, A., de Buitrago, G. G., González, M. A., Abad, J. L., Claverı́a, C., Gómez, L., Bernad, A., Martínez‐A, C., & Riese, H. H. (2002) · The FASEB Journal · doi:10.1096/fj.01-0819com · Cited by 104 · see citing works
Prostaglandin E2 as stimulator of haemopoietic stem cell proliferation
Fehér, I., & Gidáli, J. (1974) · Nature · doi:10.1038/247550a0 · Cited by 97 · see citing works
zVAD-induced autophagic cell death requires c-Src-dependent ERK and JNK activation and reactive oxygen species generation
Chen, S.-Y., Chiu, L.-Y., Ma, M.-C., Wang, J.-S., Chien, C.-L., & Lin, W. (2011) · Autophagy · doi:10.4161/auto.7.2.14212 · Cited by 94 · see citing works
The Hydra model: disclosing an apoptosis-driven generator of Wnt-based regeneration
Galliot, B., & Chera, S. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.05.006 · Cited by 93 · see citing works
Phoenix Rising
Hesse, K. (1994) · Cited by 87 · see citing works
Radiation induced temporal lobe necrosis in patients with nasopharyngeal carcinoma: a review of new avenues in its management
Chen, J., Dassarath, M., Yin, Z., et al. (2011) · Radiation Oncology · doi:10.1186/1748-717x-6-128 · Cited by 81 · see citing works
Non-steroid anti-inflammatory drugs, prostaglandins, and cancer
Allaj, V., Guo, C., & Nie, D. (2013) · Cell & Bioscience · doi:10.1186/2045-3701-3-8 · Cited by 80 · see citing works
Cyclooxygenase-2-Derived Prostaglandin E2 Protects Mouse Embryonic Stem Cells from Apoptosis
Liou, J., Ellent, D. P., Lee, S. H., Goldsby, J. S., Ko, B., Matijevic, N., Huang, J.-C., & Wu, K. K. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0505 · Cited by 77 · see citing works
Basal Caspase Activity Promotes Migration and Invasiveness in Glioblastoma Cells
Gdynia, G., Grund, K., Eckert, A., Böck, B. C., Funke, B., Macher‐Goeppinger, S., Sieber, S., Herold‐Mende, C. C., Wiestler, B., Wiestler, O. D., et al. (2007) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-07-0343 · Cited by 76 · see citing works
Myogenic cell proliferation and generation of a reversible tumorigenic phenotype are triggered by preirradiation of the recipient site
Morgan, J. E., Gross, J. G., Pagel, C. N., et al. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200108047 · Cited by 71 · see citing works
Onset Time of Tumor Repopulation for Cervical Cancer: First Evidence From Clinical Data
Huang, Z., Mayr, N. A., Gao, M., et al. (2012) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2011.12.037 · Cited by 70 · see citing works
Accelerated Repopulation in Head and Neck Cancer1
Withers, H. R., Maciejewski, B., Taylora, J. M. G., et al. (2015) · Frontiers of radiation therapy and oncology · doi:10.1159/000415101 · Cited by 70 · see citing works
Immunohistochemical Expression of Caspase-3 as an Adverse Indicator of the Clinical Outcome in Human Breast Cancer
Nakopoulou, L., Alexandrou, P. T., Stefanaki, K. S., Panayotopoulou, E. G., Lazaris, A. C., & Davaris, P. S. (2001) · Pathobiology · doi:10.1159/000064337 · Cited by 68 · see citing works
Impact of tumor repopulation on radiotherapy planning
Wang, J. Z., & Li, X. A. (2004) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2004.09.043 · Cited by 68 · see citing works
Tumour cell repopulation during fractionated radiotherapy: Correlation between flow cytometric and radiobiological data in three murine tumours
Begg, A. C., Hofland, I., & Kummermehr, J. C. (1991) · European Journal of Cancer and Clinical Oncology · doi:10.1016/0277-5379(91)90211-u · Cited by 65 · see citing works
Rapid growth of microscopic rectal cancer as a determinant of response to preoperative radiation therapy
Suwiński, R., Taylor, J. M. G., & Withers, H. R. (1998) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/s0360-3016(98)00343-5 · Cited by 59 · see citing works
Time factor for acute tissue reactions following fractionated irradiation: a balance between repopulation and enhanced radiosensitivity
Hopewell, J. W., Nyman, J., & Turesson, I. (2003) · International Journal of Radiation Biology · doi:10.1080/09553000310001600907 · Cited by 58 · see citing works
APOPTOSIS IN RADIATION THERAPY: A DOUBLE-EDGED SWORD
Greenebaum, S. (2012) · Cited by 56 · see citing works
Radiosensitization of solid tumors by Z-VAD, a pan-caspase inhibitor
Moretti, L., Kim, K. W., Jung, D. K., Willey, C. D., & Lu, J. (2009) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-08-0893 · Cited by 53 · see citing works
Signaling to gene activation and cell death by tumor necrosis factor receptors and fas
Beyaert, R., Loo, G., Heyninck, K., & Vandenabeele, P. (2002) · International review of cytology · doi:10.1016/s0074-7696(02)14007-1 · Cited by 47 · see citing works
Apoptosis in radiation therapy: a double-edged sword.
Balcer‐Kubiczek, E. K. (2012) · PubMed · Cited by 44 · see citing works
Modelling of post-irradiation accelerated repopulation in squamous cell carcinomas
Marcu, L. G., van Doorn, T., & Olver, I. (2004) · Physics in Medicine and Biology · doi:10.1088/0031-9155/49/16/021 · Cited by 37 · see citing works
Radiation biology and treatment options in radiation oncology.
Withers, H. R. (1999) · PubMed · Cited by 34 · see citing works
Injury-induced asymmetric cell death as a driving force for head regeneration in Hydra
Galliot, B. (2012) · Development Genes and Evolution · doi:10.1007/s00427-012-0411-y · Cited by 34 · see citing works
Accelerated repopulation: Friend or foe? Exploiting changes in tumor growth characteristics to improve the “efficiency” of radiotherapy
Marks, L. B., & Dewhirst, M. W. (1991) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(91)90301-j · Cited by 23 · see citing works
Effect of Lethally Damaged Tumour Cells upon the Growth of Admixed Viable Cells in Diffusion Chambers
Seelig, K. J., & Révész, L. (1960) · British Journal of Cancer · doi:10.1038/bjc.1960.15 · Cited by 21 · see citing works
Assessment of tumor cell repopulation after chemotherapy for advanced ovarian cancer: Pilot study
Davis, A. J., Chapman, W. B., Hedley, D. W., Oza, A. M., & Tannock, I. F. (2002) · Cytometry Part A · doi:10.1002/cyto.a.10001 · Cited by 16 · see citing works
Modelling of tumour repopulation after chemotherapy
Marcu, L. G., & Bezak, E. (2010) · Australasian Physical & Engineering Sciences in Medicine · doi:10.1007/s13246-010-0026-4 · Cited by 14 · see citing works

Flagged first, then by citations

Sorted by citations

A Tumour-Specific Molecular Network Promotes Tumour Growth in Drosophila by Enforcing a JNK-YKI Feedforward Loop
Waghmare, I., Gangwani, K., Rai, A., Singh, A., & Kango-Singh, M. (2023) · doi:10.1101/2023.10.18.561369 · Cited by 1 · see citing works

Caspase-independent programmed cell death with necrotic morphology
Kitanaka, C., & Kuchino, Y. (1999) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400526 · Cited by 376 · see citing works
[Caspase-independent programmed cell death with necrotic morphology].
Kitanaka, C., & Kuchino, Y. (1999) · PubMed · Cited by 3 · see citing works
Programmed cell death and its clinical implications.
Katoch, B., Sebastian, S., Sahdev, S., Padh, H., Hasnain, S. E., & Begum, R. (2002) · PubMed · Cited by 25 · see citing works
Roles of Caspases in the Programmed Cell Death of Motoneurons in vivo.
Yaginuma, H., Sato, N., Homma, S., et al. (2001) · Archivum histologicum japonicum · doi:10.1679/aohc.64.461 · Cited by 18 · see citing works
Programmed Cell Death Independent of Caspases
Lin-gang, Z., TianYu, Z., & Ning, T. (2009) · Xiandai shengwu yixue jinzhan · Cited by 1 · see citing works

Authors: Zimmerman, M. A., Huang, Q., Li, F., Liu, X., & Li, C.-Y.
Affiliations: Duke Medical Center (US)
Shanghai Jiao Tong University (CN)
Corresponding author: Li, Chuan-Yuan
ORCID: Huang, Qian
Li, Fang
Li, Chuan-Yuan
Venue: Seminars in Radiation Oncology
Publisher: Elsevier BV
Published: 2013-10
Volume: 23
Issue: 4
Pages: 288-295
ISSN: 1053-4296 (ISSN-L)
DOI: 10.1016/j.semradonc.2013.05.003
PMC: PMC3891050
OpenAlex: W1995247938
Semantic Scholar: 9ea64d2c6c31e24499017c4ffc5592246343d349
Cited by: 59
References: 100
Citations by year: 2026: 2 · 2025: 2 · 2024: 4 · 2023: 6 · 2022: 3 · 2021: 6 · 2020: 4 · 2019: 11 · 2018: 5 · 2017: 4 · 2016: 3 · 2015: 4 · 2014: 5
FWCI: 0.38
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Seminars in Radiation Oncology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (R01CA155270, R01CA131408, R01CA136748)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Keywords: tumor cell repopulation, tissue regeneration, cell death, cell proliferation, radiotherapy resistance, tumor recurrence, cancer therapeutics
MeSH terms: Animals, Autophagy, Humans, Liver Regeneration, Neoplasms, Wound Healing, Apoptosis, Caspases, Apoptosis Regulatory Proteins

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

Cell Death–Stimulated Cell Proliferation: A Tissue Regeneration Mechanism Usurped by Tumors During Radiotherapy

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks