Cited by 334Cancer-related Molecular PathwaysCell death mechanisms and regulationSignaling Pathways in Disease

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THE MANY ROLES OF c-Myc IN APOPTOSIS

Thompson, E. Brad·1998·Annual Review of Physiology

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Abstract

▪ Abstract The proto-oncogene c-myc encodes a transcription factor c-Myc, which is of great importance in controlling cell growth and vitality. The quantity of c-Myc is carefully controlled by many mechanisms, and its actions to induce and repress genes are modulated by interactions with other regulatory proteins. Understanding the kinetic and quantitative relationships that determine how and what genes c-Myc regulates is essential to understanding how Myc is involved in apoptosis. Reduction of c-myc expression and its inappropriate expression can be associated with cellular apoptosis. This review outlines the nature and regulation of the c-myc gene and of c-Myc and presents the systems and conditions in which Myc-related apoptotic events occur. Hypotheses of the mechanisms by which expression and repression of c-myc lead to apoptosis are discussed.

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Background
The aryl hydrocarbon receptor constitutively represses c-myc transcription in human mammary tumor cells
Yang, X., Liu, D., Murray, T. J., Mitchell, G. C., Hestermann, E. V., Karchner, S. I., Merson, R. R., Hahn, M. E., & Sherr, D. H. (2005) · Oncogene · doi:10.1038/sj.onc.1208938 · Cited by 86
“…directly transcription of c-myc, an important oncogene that can regulate cell growth (Pelengaris and Khan, 2003) and apoptosis (Wu et al., 1996; Thompson, 1998; Ryu et al., 2003) and which is dysregulated in many tumor types including breast cancers (Escot et al., 1986; Leder et al., 1986;…”
Background
Inhibition of c-MYC with involvement of ERK/JNK/MAPK and AKT pathways as a novel mechanism for shikonin and its derivatives in killing leukemia cells
Zhao, Q., Assimopoulou, A. N., Klauck, S. M., Damianakos, H., Chinou, İ., Kretschmer, N., Rı́os, J.-L., Papageorgiou, V. P., Bauer, R., & Efferth, T. (2015) · Oncotarget · doi:10.18632/oncotarget.5380 · Cited by 85
“Both reduction and overexpression of c-MYC can lead to apoptosis [45, 46].”
Background
c-Myc Is Necessary for DNA Damage-Induced Apoptosis in the G2 Phase of the Cell Cycle
Adachi, S., Obaya, Á. J., Han, Z., RAMOS‐DeSIMONE, N., Wyche, J. H., & Sedivy, J. M. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.15.4929-4937.2001 · Cited by 85
“For example, in a variety of transformed cell types c-myc antisense oligonucleotides cause growth inhibition, which in some (but not all) cases is associated with the onset of apoptosis (51).”
Background
Oncogene Activation in Pituitary Tumors
Yu, R., & Melmed, S. K. (2001) · Brain Pathology · doi:10.1111/j.1750-3639.2001.tb00403.x · Cited by 84
“For example, myc or E1A overexpression result in cell apoptosis (10, 19, 63, 69, 70, 72).”
BackgroundInfluential
Protocatechuic aldehyde protects cardiomycoytes against ischemic injury via regulation of nuclear pyruvate kinase M2
Wu, X., Liu, L., Zheng, Q., Hao, H., Ye, H., Li, P., & Yang, H. Q. (2021) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2021.03.021 · Cited by 84
Pancreatic β cells control glucose homeostasis via the secretion of exosomal miR‐29 family
Li, J., Zhang, Y., Ye, Y., Li, D., Liu, Y., Lee, E., Zhang, M., Dai, X., Zhang, X., Wang, S., et al. (2021) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12055 · Cited by 83
“FFAs triggered a sharp reduction in c-Myc (Ayala-Torres et al., 1997; Thompson, 1998), which can bind bothmiR-29b-1/a andmiR-29b-2/c in the vicinity of the transcription start site and negatively regulate miR-29 expression (Kriegel et al., 2012).”
Background
Current status of the molecular genetics of human prostatic adenocarcinomas
Karan, D., Lin, M., Johansson, S. L., & Batra, S. K. (2002) · International Journal of Cancer · doi:10.1002/ijc.10813 · Cited by 80
Reversible lymphomagenesis in conditionally c‐MYC expressing mice
Marinković, D., Marinković, T., Mahr, B., Heß, J., & Wirth, T. C. (2004) · International Journal of Cancer · doi:10.1002/ijc.20099 · Cited by 79
Targeted expression of c-Myc in the epidermis alters normal proliferation, differentiation and UV-B induced apoptosis
Waikel, R. L., Wang, X., & Roop, D. R. (1999) · Oncogene · doi:10.1038/sj.onc.1203040 · Cited by 76
“In some leukemic and lymphoid cell lines c-myc levels must decline for glucocorticoid, dexamethasone induced apoptosis (Thompson, 1998).”
Background
Molecular Pathways in Prostate Cancer
Mazaris, E. M., & Tsiotras, A. (2013) · Nephro-Urology Monthly · doi:10.5812/numonthly.9430 · Cited by 75
“It encodes the c-MYC protein, which promotes cell proliferation and transformation (5, 89).”
Background
The role of constitutive NF-κB activity in PC-3 human prostate cancer cell invasive behavior
Lindholm, P. F., Bub, J. D., Kaul, S., Shidham, V. B., & Kajdacsy‐Balla, A. (2000) · Clinical & Experimental Metastasis · doi:10.1023/a:1011845725394 · Cited by 75
“NF-κB may exert its anti-apoptotic effects by upregulation of TRAFs, bcl-2, c-myc, p53 and inhibition of apoptosis [21, 22].”
Background
Proteasomes in apoptosis: villains or guardians?
W�jcik, C. (1999) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050483 · Cited by 73
Role of programmed cell death in development
Ranganath, R. M., & Nagashree, N. R. (2001) · International review of cytology · doi:10.1016/s0074-7696(01)02005-8 · Cited by 72
Essential Role of Human Leukocyte Antigen-encoded Proteasome Subunits in NF-κB Activation and Prevention of Tumor Necrosis Factor-α-induced Apoptosis
Hayashi, T., & Faustman, D. L. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.7.5238 · Cited by 70
Physical and functional interaction between HCV core protein and the different p73 isoforms
Alisi, A., Giambartolomei, S., Cupelli, F., Merlo, P., Fontemaggi, G., Spaziani, A., & Balsano, C. (2003) · Oncogene · doi:10.1038/sj.onc.1206333 · Cited by 69
C‐myc gene expression alone is sufficient to confer resistance to antiestrogen in human breast cancer cells
Venditti, M., Iwasiow, B. M., Orr, F. W., & Shiu, R. P. C. (2002) · International Journal of Cancer · doi:10.1002/ijc.10269 · Cited by 69
New Wnt/β‐Catenin Signaling Inhibitors Isolated from Eleutherine palmifolia
Li, X., Ohtsuki, T., Koyano, T., Kowithayakorn, T., & Ishibashi, M. (2008) · Chemistry - An Asian Journal · doi:10.1002/asia.200800354 · Cited by 68
Dicer-Dependent MicroRNAs Control Maturation, Function, and Maintenance of Langerhans Cells In Vivo
Kuipers, H., Schnorfeil, F. M., Fehling, H. J., Bartels, H., & Brocker, T. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903912 · Cited by 66
Labdane type diterpenes down-regulate the expression of c-myc protein, but not of bcl-2, in human leukemia T-cells undergoing apoptosis
DIMAS, K. S., Demetzos, C., Vaos, V., Ioannidis, P., & Trangas, T. T. (2001) · Leukemia Research · doi:10.1016/s0145-2126(00)00150-8 · Cited by 67
Regulation of the Resident Chromosomal Copy of c-myc by c-Myb Is Involved in Myeloid Leukemogenesis
Schmidt, M., Nazarov, V., Stevens, L. M., Watson, R., & Wolff, L. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.6.1970-1981.2000 · Cited by 67
“To further evaluate downstream effects of deregulated c-myc expression due to activation of MybEnER, we examined the influence of the dominant negative protein on another target gene of cMyc, ODC.”
BackgroundInfluential
Rational combination treatment with histone deacetylase inhibitors and immunomodulatory drugs in multiple myeloma
Hideshima, T., Cottini, F., Ohguchi, H., Jakubı́ková, J., Görgün, G., Mimura, N., Tai, Y., Munshi, N. C., Richardson, P. G. G., & Anderson, K. C. (2015) · Blood Cancer Journal · doi:10.1038/bcj.2015.38 · Cited by 65
The flavonoid component isorhamnetin in vitro inhibits proliferation and induces apoptosis in Eca-109 cells
Ma, G., Yang, C., Qu, Y., Wei, H., Zhang, T., & Zhang, N. (2007) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2007.02.006 · Cited by 64
Transformation of Follicular Lymphoma to Precursor B-Cell Lymphoblastic Lymphoma With c-mycGene Rearrangement as a Critical Event
Young, K. H., Xie, Q., Zhou, G., Eickhoff, J. C., Sanger, W. G., Aoun, P. A., & Chan, W. C. (2007) · American Journal of Clinical Pathology · doi:10.1309/nkk3fex2be5l7ekb · Cited by 64
Influence of a low background radiation environment on biochemical and biological responses in V79 cells
Satta, L., Antonelli, F., Belli, M., Sapora, O., Simone, G., Sorrentino, E., Tabocchini, M. A., Amicarelli, F., Ara, C., Ceru`, M. P., et al. (2002) · Radiation and Environmental Biophysics · doi:10.1007/s00411-002-0159-2 · Cited by 64
Glutathione Depletion Induced by c-Myc Downregulation Triggers Apoptosis on Treatment with Alkylating Agents
Biroccio, A., Benassi, B., Fiorentino, F. P., & Zupi, G. (2004) · Neoplasia · doi:10.1593/neo.03370 · Cited by 64
“For example, c-myc antisense or dominant-defective causes apoptosis in a variety of transformed cell types [3], whereas c-Myc expression can sensitize cells to a wide range of different stimuli such as low serum conditions [4], hypoxia [5], and deprivation of specific growth factors [6] [7].”
Background
Caspases and mitochondria in c-Myc-induced apoptosis: identification of ATM as a new target of caspases
Hotti, A., Järvinen, K., Siivola, P., & Hölttä, E. (2000) · Oncogene · doi:10.1038/sj.onc.1203567 · Cited by 63
“Also, it is not clear whether the tumour suppressor p53, a transcriptional target for cMyc, is needed for apoptosis induced by c-Myc (Lotem and Sachs, 1995; Shim et al., 1998; Wagner et al., 1994; Zindy et al., 1998; reviewed in Prendergast, 1999; Thompson, 1998).”
Background
Amplification of c-myc gene and overexpression of c-Myc protein in breast cancer and adjacent non-neoplastic tissue
Chrzan, P., Skokowski, J., Karmoliński, A., & Pawełczyk, T. (2001) · Clinical Biochemistry · doi:10.1016/s0009-9120(01)00260-0 · Cited by 63
Comparative toxicity of oleic acid and linoleic acid on Raji cells
Cury‐Boaventura, M. F., Pompéia, C., & Curi, R. (2005) · Nutrition · doi:10.1016/j.nut.2004.07.007 · Cited by 63
Grb7 signal transduction protein mediates metastatic progression of esophageal carcinoma
Tanaka, S., Sugimachi, K., Kawaguchi, H., Saeki, H., Ohno, S., Wands, J. R., & Sugimachi, K. (2000) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(200006)183:3 · Cited by 55
c-Myc antagonizes the effect of p53 on apoptosis and p21WAF1 transactivation in K562 leukemia cells
Ceballos, E., Delgado, M. D., Gutierrez, P., Richard, C., Müller, D., Eilers, M., Ehinger, M., Gullberg, U., & León, J. (2000) · Oncogene · doi:10.1038/sj.onc.1203541 · Cited by 61
“…growth conditions, e.g. deprivation of growth factors or hypoxia (for recent reviews see Ho man and Lieberman, 1998; Hueber and Evan, 1998; Thompson, 1998). c-Mycmediated apoptosis requires wild-type p53 in ®broblasts (Hermeking and Eick, 1994; Wagner et al., 1994; Rupnow et al., 1998),…”
Background
The development of the adult intestinal stem cells: Insights from studies on thyroid hormone-dependent amphibian metamorphosis
Shi, Y., Hasebe, T., Fu, L., Fujimoto, K., & Ishizuya‐Oka, A. (2011) · Cell & Bioscience · doi:10.1186/2045-3701-1-30 · Cited by 60
c-myc antisense oligonucleotide treatment ameliorates murine ARPKD
Ricker, J. L., Mata, J. E., Iversen, P. L., & Gattone, V. H. (2002) · Kidney International · doi:10.1046/j.1523-1755.2002.0610s1125.x · Cited by 57
“DISCUSSION The c-myc gene, located on mouse chromosome 15, encodes 64 to 67 kD proteins containing domains that function in nuclear localization, non-specific and sequence-specific DNA binding, and oligomerizatio”
Background
Proteomic identification of proteins involved in the anticancer activities of oridonin in HepG2 cells
Wang, H., Ye, Y., Pan, S.-Y., Zhu, G., Li, Y., Fong, D. W. F., & Yu, Z. (2010) · Phytomedicine · doi:10.1016/j.phymed.2010.06.011 · Cited by 56
Fatal Acute Lymphoblastic Leukemia in Mice Transgenic for B Cell-Restricted bcl-xL and c- myc
Swanson, P. J., Kuslak, S. L., Wei, F., Tze, L. E., Gaffney, P. M., Selby, S. A., Hippen, K. L., Núñez, G., Sidman, C. L., & Behrens, T. W. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.11.6684 · Cited by 55
“Dysregulated expression of Myc causes cell cycle progression and proliferation, and, in addition, also induces apoptotic cell death (9).”
Background
Mediterranean Mussel Gene Expression Profile Induced by Okadaic Acid Exposure
Manfrin, C., Dreos, R., Battistella, S., Beran, A. R., Gerdol, M., Varotto, L., Lanfranchi, G., Venier, P., & Pallavicini, A. (2010) · Environmental Science & Technology · doi:10.1021/es102213f · Cited by 55
Targeted Deletion of the S-Phase-Specific Myc Antagonist Mad3 Sensitizes Neuronal and Lymphoid Cells to Radiation-Induced Apoptosis
Quéva, C., McArthur, G. A., Iritani, B. M., & Eisenman, R. N. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.3.703-712.2001 · Cited by 55
“Because mad3 and c-Myc were coexpressed in the thymus (44), where Myc has been shown elsewhere to influence apoptosis in T lymphocytes (22, 42, 53, 57), we examined the response of mad3 and mad3 T cells to apoptotic stimuli.”
Background
Involvement of Nuclear Factor κB in c-Myc Induction by Tubulin Polymerization Inhibitors
Bourgarel‐Rey, V., Vallée, S., Rimet, O., Champion, S., Braguer, D., Desobry, A., Briand, C. M., & Barra, Y. (2001) · Molecular Pharmacology · doi:10.1016/s0026-895x(24)12576-x · Cited by 54
Synergistic and opposing regulation of the stress-responsive gene IEX-1 by p53, c-Myc, and multiple NF-κB/rel complexes
Huang, Y., Wu, J. Y., Zhang, Y., & Wu, M. X. (2002) · Oncogene · doi:10.1038/sj.onc.1205854 · Cited by 52
“…indicating an involvement of coactivators, other than p300 or CBP, which remains to be investigated. c-Myc and p53 are well documented to be functionally related in several different systems (Bates and Vousden, 1999; Prendergast, 1999; Hermeking and Eick, 1994; Sala et al., 1996; Thompson, 1998).”
Background
Variable functions of bcl-2 in mediating bioreactor stress- induced apoptosis in hybridoma cells
Perani, A., Singh, R. P., Chauhan, R., & Al‐Rubeai, M. (1998) · Cytotechnology · doi:10.1023/a:1008002319400 · Cited by 52
Effect of inositol hexaphosphate (IP6) on human normal and leukaemic haematopoietic cells
Deliliers, G. L., Servida, F., Fracchiolla, N., Ricci, C., Borsotti, C., Colombo, G. I., & Soligo, D. A. (2002) · British Journal of Haematology · doi:10.1046/j.1365-2141.2002.03453.x · Cited by 51
“Transcription factors that promote cell proliferation, including c-myc and HPTPCAAX1 (Diamond et al, 1996; Thompson, 1998), were downregulated upon incubation in the presence of IP6.”
Background
Targeting regulated chondrocyte death in osteoarthritis therapy
Zhu, R., Wang, Y., Ouyang, Z., Hao, W., Zhou, F., Lin, Y., Cheng, Y., Zhou, R., & Hu, W. M. (2023) · Biochemical Pharmacology · doi:10.1016/j.bcp.2023.115707 · Cited by 52
Activation of Akt and ERK signalling pathways induced by etoposide confer chemoresistance in gastric cancer cells
Liu, S.-Q., Yu, J.-P., Yu, H., Lv, P., & Chen, H.-L. (2006) · Digestive and Liver Disease · doi:10.1016/j.dld.2006.01.012 · Cited by 50
Glucocorticoid resistance in childhood leukaemia: mechanisms and modulation
Haarman, E. G., Kaspers, G. J. L., & Veerman, A. J. P. (2003) · British Journal of Haematology · doi:10.1046/j.1365-2141.2003.04189.x · Cited by 50
“Studies generally focused on the typical apoptosis genes (Thulasi et al, 1993; Thompson, 1998; Kofler, 2000), or tried to identify 2003 Blackwell Publishing Ltd, British Journal of Haematology 120: 919–929 candidate genes by ‘gene search approaches’ (Briehl et al, 1990; Baughman et al, 1991).”
Background
Regulation and clinical potential of telomerase reverse transcriptase (TERT/hTERT) in breast cancer
Yang, R., Han, Y., Guan, X., Hong, Y., Meng, J., Ding, S., Qian, L., & Yi, W. (2023) · Cell Communication and Signaling · doi:10.1186/s12964-023-01244-8 · Cited by 50
“The N-terminal transactivation domain of c-MYC recognizes E-box motifs (5’-CAC GTG -3’ sequence) on DNA, enabling c-MYC/MAX heterodimers to bind to regulatory sequences like promoters and regulate target gene transcription [68, 69].”
Background
The MYC dualism in growth and death
Fuhrmann, G., Rosenberger, G., Grusch, M., Klein, N., Hofmann, J. F.-X., & Krupitza, G. (1999) · Mutation Research/Reviews in Mutation Research · doi:10.1016/s1383-5742(99)00084-8 · Cited by 48
Erythropoietin Activates Two Distinct Signaling Pathways Required for the Initiation and the Elongation of c-myc
Chen, C., & Sytkowski, A. J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m105702200 · Cited by 48

Authors: Thompson, E. B.
Affiliations: The University of Texas Medical Branch at Galveston (US)
Corresponding author: Thompson, E. Brad
ORCID: Thompson, E. Brad
Venue: Annual Review of Physiology
Publisher: Annual Reviews
Published: 1998-10
Volume: 60
Issue: 1
Pages: 575-600
ISSN: 0066-4278 (ISSN-L)
1545-1585
DOI: 10.1146/annurev.physiol.60.1.575
OpenAlex: W2104373533
Cited by: 328
References: 159
Citations by year: 2026: 6 · 2025: 8 · 2024: 24 · 2023: 31 · 2022: 17 · 2021: 10 · 2020: 6 · 2019: 2 · 2018: 3 · 2017: 6 · 2015: 10 · 2014: 3 · 2013: 6 · 2012: 3
FWCI: 3.50
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Physiology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Signaling Pathways in Disease
Keywords: c-Myc, c-myc proto-oncogene, apoptosis, transcription factor regulation, gene expression regulation, gene repression, cell growth regulation, transcriptional regulation
MeSH terms: Proto-Oncogene Mas, Animals, Humans, Genes, myc, Proto-Oncogene Proteins c-myc, Apoptosis

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THE MANY ROLES OF c-Myc IN APOPTOSIS

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