Max deletion destabilizes MYC protein and abrogates Eµ- Myc lymphomagenesis
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Abstract
Although MAX is regarded as an obligate dimerization partner for MYC, its function in normal development and neoplasia is poorly defined. We show that B-cell-specific deletion of Max has a modest effect on B-cell development but completely abrogates Eµ- Myc- driven lymphomagenesis. While Max loss affects only a few hundred genes in normal B cells, it leads to the global down-regulation of Myc -activated genes in premalignant Eµ- Myc cells. We show that the balance between MYC–MAX and MNT–MAX interactions in B cells shifts in premalignant B cells toward a MYC-driven transcriptional program. Moreover, we found that MAX loss leads to a significant reduction in MYC protein levels and down-regulation of direct transcriptional targets, including regulators of MYC stability. This phenomenon is also observed in multiple cell lines treated with MYC–MAX dimerization inhibitors. Our work uncovers a layer of Myc autoregulation critical for lymphomagenesis yet partly dispensable for normal development.
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Max is a constitutive expression protein with ubiquitous presence that plays a central role in controlling the Max-Max dimerin 1 (MXD1) axis.
“Max is a constitutive expression protein with ubiquitous presence that plays a central role in controlling the Max-Max dimerin 1 (MXD1) axis.”
From Recent advances in targeting the “undruggable” proteins: from drug discovery to clinical trials (2023) · cites this paper as [416]
C-Myc forms a complex with Max through the bHLH-ZIP domain to activate gene transcription.
“C-Myc forms a complex with Max through the bHLH-ZIP domain to activate gene transcription.415,416”
From Recent advances in targeting the “undruggable” proteins: from drug discovery to clinical trials (2023) · cites this paper as [416]
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Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625 · see citing works
The Molecular Signatures Database Hallmark Gene Set Collection
Liberzon, A., Birger, C., Thorvaldsdóttir, H., Ghandi, M., Mesirov, J. P., & Tamayo, P. (2015) · Cell Systems · doi:10.1016/j.cels.2015.12.004 · Cited by 13,807 · see citing works
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382 · see citing works
Enrichr: a comprehensive gene set enrichment analysis web server 2016 update
Kuleshov, M. V., Jones, M. R., Rouillard, A. D., Fernandez, N. F., Duan, Q., Wang, Z., Koplev, S., Jenkins, S. L., Jagodnik, K. M., Lachmann, A., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw377 · Cited by 10,799 · see citing works
Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B
Cross, D. A. E., Alessi, D. R., Cohen, P., Andjelkovich, M., & Hemmings, B. A. (1995) · Nature · doi:10.1038/378785a0 · Cited by 5,244 · see citing works
MEME-ChIP: motif analysis of large DNA datasets
Machanick, P., & Bailey, T. L. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr189 · Cited by 1,815 · see citing works
Boija, A., Klein, I. A., Sabari, B. R., Dall’Agnese, A., Coffey, E. L., Zamudio, A. V., Li, C. H., Shrinivas, K., Manteiga, J. C., Hannett, N. M., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.042 · Cited by 1,815 · see citing works
The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice
Adams, J. M., Harris, A. W., Pinkert, C. A., Corcoran, L. M., Alexander, W. S., Cory, S., Palmiter, R. D., & Brinster, R. L. (1985) · Nature · doi:10.1038/318533a0 · Cited by 1,778 · see citing works
An efficient targeted nuclease strategy for high-resolution mapping of DNA binding sites
Skene, P. J., & Henikoff, S. (2017) · eLife · doi:10.7554/elife.21856 · Cited by 1,737 · see citing works
Self-citationMax: A Helix-Loop-Helix Zipper Protein That Forms a Sequence-Specific DNA-Binding Complex with Myc
Blackwood, E. M., & Eisenman, R. N. (1991) · Science · doi:10.1126/science.2006410 · Cited by 1,681 · see citing works
Self-citationMYC regulates the antitumor immune response through CD47 and PD-L1
Casey, S. C., Tong, L., Li, Y., Do, R., Walz, S., Fitzgerald, K. N., Gouw, A. M., Baylot, V., Gütgemann, I., Eilers, M., et al. (2016) · Science · doi:10.1126/science.aac9935 · Cited by 1,403 · see citing works
Welcker, M., Orian, A., Jin, J., Grim, J. A., Harper, J. W., Eisenman, R. N., & Clurman, B. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402770101 · Cited by 942 · see citing works
Self-citationShen, L., Shao, N., Liu, X., & Nestler, E. J. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-284 · Cited by 852 · see citing works
Phosphorylation‐dependent degradation of c‐Myc is mediated by the F‐box protein Fbw7
Yada, M., Hatakeyama, S., Kamura, T., Nishiyama, M., Tsunematsu, R., Imaki, H., Ishida, N., Okumura, F., Nakayama, K., & Nakayama, K. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600217 · Cited by 810 · see citing works
LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism
Cartwright, P., McLean, C. A., Sheppard, A. M., Rivett, D., Jones, K., & Dalton, S. (2005) · Development · doi:10.1242/dev.01670 · Cited by 758 · see citing works
CIP2A inhibits PP2A in human malignancies
Junttila, M. R., Puustinen, P., Niemelä, M., Ahola, R., Arnold, H., Böttzauw, T., Ala-aho, R., Nielsen, C., Ivaska, J., Taya, Y., et al. (2007) · Cell · doi:10.1016/j.cell.2007.04.044 · Cited by 677 · see citing works
Testing gene function early in the B cell lineage in mb1-cre mice
Hobeika, E., Thiemann, S., Storch, B., Jumaa, H., Nielsen, P. J., Pelanda, R., & Reth, M. G. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605944103 · Cited by 581 · see citing works
Oncogenic activity of the c-Myc protein requires dimerization with Max
Amati, B. B., Brooks, M. W., Levy-Strumpf, N., Littlewood, T. D., Evan, G. I., & Land, H. (1993) · Cell · doi:10.1016/0092-8674(93)90663-b · Cited by 559 · see citing works
Exome sequencing identifies MAX mutations as a cause of hereditary pheochromocytoma
Comino‐Méndez, I., Gracia-Aznárez, F. J., Schiavi, F., Landa, I., Leandro-Garcia, L. J., Letón, R., Honrado, E., Ramos‐Medina, R., Caronia, D., Pita, G., et al. (2011) · Nature Genetics · doi:10.1038/ng.861 · Cited by 528 · see citing works
Proteins encoded by the human c-myc oncogene: differential expression in neoplastic cells.
Hann, S., & Eisenman, R. N. (1984) · Molecular and Cellular Biology · doi:10.1128/mcb.4.11.2486 · Cited by 503 · see citing works
Self-citationSelective transcriptional regulation by Myc in cellular growth control and lymphomagenesis
Sabò, A., Kress, T. R., Pelizzola, M., de Pretis, S., Gorski, M. M., Tesi, A., Morelli, M. J., Bora, P., Doni, M., Verrecchia, A., et al. (2014) · Nature · doi:10.1038/nature13537 · Cited by 478 · see citing works
Gregory, M. A., & Hann, S. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.7.2423-2435.2000 · Cited by 469 · see citing works
Farrell, A. S., & Sears, R. C. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a014365 · Cited by 468 · see citing works
The cell-cycle regulator c-Myc is essential for the formation and maintenance of germinal centers
Calado, D. P., Sasaki, Y., Godinho, S. A., Pellerin, A., Köchert, K., Sleckman, B. P., de Alborán, I. M., Janz, M., Rodig, S. J., & Rajewsky, K. (2012) · Nature Immunology · doi:10.1038/ni.2418 · Cited by 448 · see citing works
Myc and Max proteins possess distinct transcriptional activities
Kretzner, L., Blackwood, E. M., & Eisenman, R. N. (1992) · Nature · doi:10.1038/359426a0 · Cited by 445 · see citing works
Self-citationThe c-myc oncogene perturbs B lymphocyte development in Eμ-myc transgenic mice
Langdon, W. Y., Harris, A. W., Cory, S., & Adams, J. M. (1986) · Cell · doi:10.1016/0092-8674(86)90361-2 · Cited by 433 · see citing works
Harris, A. W., Pinkert, C. A., Crawford, M., Langdon, W. Y., Brinster, R. L., & Adams, J. M. (1988) · The Journal of Experimental Medicine · doi:10.1084/jem.167.2.353 · Cited by 432 · see citing works
Low molecular weight inhibitors of Myc–Max interaction and function
Yin, X., Giap, C., Lazo, J. S., & Prochownik, E. V. (2003) · Oncogene · doi:10.1038/sj.onc.1206641 · Cited by 426 · see citing works
Myc and Max associate in vivo.Preprint
Blackwood, E. M., Lüscher, B., & Eisenman, R. N. (1992) · Genes & Development · doi:10.1101/gad.6.1.71 · Cited by 415 · see citing works
Self-citationAn Overview of MYC and Its Interactome
Conacci-Sorrell, M., McFerrin, L., & Eisenman, R. N. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a014357 · Cited by 408 · see citing works
Self-citationThe transcriptional program of a human B cell line in response to Myc.
Schuhmacher, M., Kohlhuber, F., Hölzel, M., Kaiser, C., Burtscher, H., Jarsch, M., Bornkamm, G., Laux, G., Polack, A., Weidle, U., et al. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.2.397 · Cited by 344 · see citing works
The MYC transcription factor network: balancing metabolism, proliferation and oncogenesis
Carroll, P. A., Freie, B. W., Mathsyaraja, H., & Eisenman, R. N. (2018) · Frontiers of Medicine · doi:10.1007/s11684-018-0650-z · Cited by 289 · see citing works
Self-citationMYC inhibition induces metabolic changes leading to accumulation of lipid droplets in tumor cells
Zirath, H., Frenzel, A., Oliynyk, G., Segerström, L., Westermark, U., Larsson, K., Persson, M. M., Hultenby, K. R., Lehtiö, J., Einvik, C., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1222404110 · Cited by 229 · see citing works
Conacci‐Sorrell, M., Ngouenet, C., & Eisenman, R. N. (2010) · Cell · doi:10.1016/j.cell.2010.06.037 · Cited by 219 · see citing works
Self-citationIntrinsic cell-penetrating activity propels Omomyc from proof of concept to viable anti-MYC therapy
Beaulieu, M.-È., Jauset, T., Massó-Vallés, D., Martínez-Martín, S., Rahl, P. B., Maltais, L., Fluck, M. F. Z., Casacuberta‐Serra, S., del Pozo, E. S., Fiore, C., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aar5012 · Cited by 211 · see citing works
MYC-Dependent Regulation and Prognostic Role of CIP2A in Gastric Cancer
Khanna, A., Böckelman, C., Hemmes, A., Junttila, M. R., Wiksten, J.-P., Lundin, M., Junnila, S., Murphy, D. J., Evan, G. I., Haglund, C., et al. (2009) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/djp103 · Cited by 185 · see citing works
High-resolution mapping of transcription factor binding sites on native chromatin
Kasinathan, S., Orsi, G. A., Zentner, G. E., Ahmad, K., & Henikoff, S. (2013) · Nature Methods · doi:10.1038/nmeth.2766 · Cited by 183 · see citing works
Self-citationRomero, O. A., Torres-Diz, M., Pros, E., Savola, S. P., Gómez, A., Morán, S., Sáez, C., Iwakawa, R., Villanueva, A., Montuenga, L. M., et al. (2013) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0799 · Cited by 164 · see citing works
The deubiquitinase USP28 controls intestinal homeostasis and promotes colorectal cancer
Diefenbacher, M. E., Popov, N., Blake, S. M., Schülein‐Völk, C., Nye, E. L., Spencer‐Dene, B., Jaenicke, L. A., Eilers, M., & Behrens, A. (2014) · Journal of Clinical Investigation · doi:10.1172/jci73733 · Cited by 154 · see citing works
Ubiquitylation of the amino terminus of Myc by SCFβ-TrCP antagonizes SCFFbw7-mediated turnover
Popov, N., Schülein‐Völk, C., Jaenicke, L. A., & Eilers, M. (2010) · Nature Cell Biology · doi:10.1038/ncb2104 · Cited by 151 · see citing works
Mechanisms of MYC stabilization in human malignancies
Junttila, M. R., & Westermarck, J. K. (2008) · Cell Cycle · doi:10.4161/cc.7.5.5492 · Cited by 144 · see citing works
Division and apoptosis of E2f-deficient retinal progenitors
Chen, D., Pacal, M., Wenzel, P., Knoepfler, P. S., Leone, G., & Bremner, R. (2009) · Nature · doi:10.1038/nature08544 · Cited by 144 · see citing works
Proteins Encoded by the Human c-myc Oncogene: Differential Expression in Neoplastic Cells
Hann, S., & Eisenman, R. N. (1984) · Molecular and Cellular Biology · doi:10.1128/mcb.4.11.2486-2497.1984 · Cited by 143 · see citing works
Self-citationStabilization of the Max Homodimer with a Small Molecule Attenuates Myc-Driven Transcription
Struntz, N. B., Chen, A., Deutzmann, A., Wilson, R. M., Stefan, E., Evans, H. L., Ramirez, M. A., Liang, T., Caballero, F., Wildschut, M. H. E., et al. (2019) · Cell Chemical Biology · doi:10.1016/j.chembiol.2019.02.009 · Cited by 130 · see citing works
Myc stimulates B lymphocyte differentiation and amplifies calcium signaling
Habib, T., Park, H., Tsang, M., de Alborán, I. M., Nicks, A., Wilson, L., Knoepfler, P. S., Andrews, S. F., Rawlings, D. J., Eisenman, R. N., et al. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200704173 · Cited by 110 · see citing works
Self-citationNegative autoregulation of c‐myc gene expression is inactivated in transformed cells.
Grignani, F., Lombardi, L. T., Inghirami, G., Sternas, L. A., Cechova, K., & Dalla‐Favera, R. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07612.x · Cited by 107 · see citing works
Essential role for Max in early embryonic growth and developmentPreprint
Shen-Li, H., O’Hagan, R. C., Hou, H., Horner, J. W., Lee, H., & DePinho, R. A. (2000) · Genes & Development · doi:10.1101/gad.14.1.17 · Cited by 99 · see citing works
PLK1 stabilizes a MYC-dependent kinase network in aggressive B cell lymphomas
Ren, Y., Bi, C., Zhao, X., Lwin, T., Wang, C., Ji, Y., Silva, A. S., Shah, B. D., Fang, B., Li, T., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci122533 · Cited by 91 · see citing works
Max-independent functions of Myc in Drosophila melanogaster
Steiger, D., Furrer, M., Schwinkendorf, D., & Gallant, P. (2008) · Nature Genetics · doi:10.1038/ng.178 · Cited by 90 · see citing works
The Nerve Growth Factor-Responsive PC12 Cell Line Does Not Express the Myc Dimerization Partner Max
Hopewell, R., & Ziff, E. B. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.7.3470 · Cited by 87 · see citing works
Automated in situ chromatin profiling efficiently resolves cell types and gene regulatory programs
Janssens, D. H., Wu, S. J., Sarthy, J. F., Meers, M. P., Myers, C. H., Olson, J. M., Ahmad, K., & Henikoff, S. (2018) · Epigenetics & Chromatin · doi:10.1186/s13072-018-0243-8 · Cited by 73 · see citing works
Self-citationRedeployment of Myc and E2f1–3 drives Rb-deficient cell cycles
Liu, H., Tang, X., Srivastava, A., Pécot, T., Daniel, P., Hemmelgarn, B. T., Reyes, S., Fackler, N., Bajwa, A., Kladney, R. D., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3210 · Cited by 70 · see citing works
MAX inactivation is an early event in GIST development that regulates p16 and cell proliferation
Schaefer, I., Wang, Y., Liang, C., Bahri, N., Quattrone, A., Doyle, L. A., Mariño‐Enríquez, A., Lauria, A., Zhu, M. J., Dêbiec‐Rychter, M., et al. (2017) · Nature Communications · doi:10.1038/ncomms14674 · Cited by 66 · see citing works
B Lymphocyte Commitment Program Is Driven by the Proto-Oncogene c-myc
Vallespinós, M., Fernández‐Antorán, D., Rodríguez, L., Álvaro-Blanco, J., Baena, E., Ortiz, M., Dukovska, D., Martínez, D., Rojas, A. M., Campanero, M. R., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002753 · Cited by 38 · see citing works
CIP2A Influences Survival in Colon Cancer and Is Critical for Maintaining Myc Expression
Wiegering, A., Pfann, C., Uthe, F. W., Otto, C., Rycak, L., Mäder, U., Gasser, M., Waaga-Gasser, A.-M., Eilers, M., & Germer, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075292 · Cited by 38 · see citing works
Lindeman, G. J., Harris, A. W., Bath, M. L., Eisenman, R. N., & Adams, J. M. (1995) · PubMed · Cited by 36 · see citing works
Self-citationFunctional interplay between c‐Myc and Max in B lymphocyte differentiation
Pérez‐Olivares, M., Trento, A., Rodríguez‐Acebes, S., González‐Acosta, D., Fernández‐Antorán, D., Román‐García, S., Martínez, D., López‐Briones, T., Torroja, C., Carrasco, Y. R., et al. (2018) · EMBO Reports · doi:10.15252/embr.201845770 · Cited by 24 · see citing works
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1 of the 58 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Recent advances in targeting the “undruggable” proteins: from drug discovery to clinical trials
Xie, X., Yu, T., Li, X., Zhang, N., Foster, L. J., Peng, C., Huang, W., & He, G. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01589-z · Cited by 396 · see citing works
Target gene-independent functions of MYC oncoproteins
Baluapuri, A., Wolf, E., & Eilers, M. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0215-2 · Cited by 310 · see citing works
Beaulieu, M.-È., Castillo, F., & Soucek, L. (2020) · Cells · doi:10.3390/cells9041038 · Cited by 110 · see citing works
mTORC1 promotes cell growth via m6A-dependent mRNA degradation
Cho, S., Lee, G., Pickering, B. F., Jang, C., Park, J. H., He, L., Mathur, L., Kim, S.-S., Jung, S., Tang, H.-W., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.03.010 · Cited by 107 · see citing works
Röschert, I., Poon, E., Henssen, A. G., García, H. D., Gatti, M., Giansanti, C., Jamin, Y., Ade, C. P., Gallant, P., Schülein‐Völk, C., et al. (2021) · Nature Cancer · doi:10.1038/s43018-020-00171-8 · Cited by 96 · see citing works
MAX functions as a tumor suppressor and rewires metabolism in small cell lung cancer
Augert, A., Mathsyaraja, H., Ibrahim, A., Freie, B., Geuenich, M., Cheng, P.-F., Alibeckoff, S. P., Wu, N., Hiatt, J., Basom, R. S., et al. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.04.016 · Cited by 68 · see citing works
Self-citationRole of WTAP in Cancer: From Mechanisms to the Therapeutic Potential
Fan, Y., Li, X., Sun, H., Gao, Z., Zhu, Z., & Yuan, K. (2022) · Biomolecules · doi:10.3390/biom12091224 · Cited by 61 · see citing works
Integrative single-cell RNA-seq and ATAC-seq analysis of myogenic differentiation in pig
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · BMC Biology · doi:10.1186/s12915-023-01519-z · Cited by 55 · see citing works
An MXD1-derived repressor peptide identifies noncoding mediators of MYC-driven cell proliferation
Raffeiner, P., Hart, J. R., García-Caballero, D., Bar‐Peled, L., Weinberg, M. S., & Vogt, P. K. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1921786117 · Cited by 42 · see citing works
Mathsyaraja, H., Catchpole, J., Freie, B. W., Eastwood, E., Babaeva, E., Geuenich, M., Cheng, P. F., Ayers, J., Yu, M., Wu, N., et al. (2021) · eLife · doi:10.7554/elife.64212 · Cited by 39 · see citing works
Self-citationMYC the oncogene from hell: Novel opportunities for cancer therapy
Papadimitropoulou, A., Makri, M., & Zoidis, G. (2024) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2024.116194 · Cited by 38 · see citing works
Li, X.-Y., Wu, J., Liu, P., Li, Z.-J., Wang, Y., Chen, B., Hu, C.-L., Fei, M.-Y., Yu, P.-C., Jiang, Y.-L., et al. (2022) · Leukemia · doi:10.1038/s41375-022-01747-2 · Cited by 36 · see citing works
m6A in the Signal Transduction Network
Jang, K.-H., Heras, C. R., & Lee, G. (2022) · Molecules and Cells · doi:10.14348/molcells.2022.0017 · Cited by 34 · see citing works
Normal and Neoplastic Growth Suppression by the Extended Myc Network
Wang, H., & Prochownik, E. (2022) · Cells · doi:10.3390/cells11040747 · Cited by 31 · see citing works
Targeting Myc Interacting Proteins as a Winding Path in Cancer Therapy
Zhou, Y., Gao, X., Meng, Y. G., Yang, B., He, Q., & Cao, J. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.748852 · Cited by 29 · see citing works
The MYCL and MXD1 transcription factors regulate the fitness of murine dendritic cells
Anderson, D. A., Murphy, T. L., Eisenman, R. N., & MURPHY, K. M. M. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1915060117 · Cited by 22 · see citing works
Self-citationCastell, A., Yan, Q., Fawkner, K., Bazzar, W., Zhang, F., Wickström, M., Alzrigat, M., Franco, M., Krona, C. C., Cameron, D. P., et al. (2022) · Cancer Research Communications · doi:10.1158/2767-9764.crc-21-0019 · Cited by 21 · see citing works
Lani‐Louzada, R., Marra, C., Dias, M. S., Araújo, V. G., Abreu, C. A., Ribas, V. T., Adesse, D., Allodi, S., Chiodo, V. A., Hauswirth, W. W., et al. (2022) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.63.2.5 · Cited by 20 · see citing works
Insights about MYC and Apoptosis in B-Lymphomagenesis: An Update from Murine Models
Vecchio, E., Fiume, G., Correnti, S., Romano, S., Iaccino, E., Mimmi, S., Maisano, D., Nisticò, N., & Quinto, I. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124265 · Cited by 19 · see citing works
Freie, B. W., Ibrahim, A. H., Carroll, P. A., Bronson, R. T., Augert, A., MacPherson, D. P., & Eisenman, R. N. (2025) · Science Advances · doi:10.1126/sciadv.adt3177 · Cited by 18 · see citing works
Self-citationCoordinated Cross-Talk Between the Myc and Mlx Networks in Liver Regeneration and Neoplasia
Wang, H., Lu, J. L., Alencastro, F., Roberts, A., Fiedor, J., Carroll, P. A., Eisenman, R. N., Ranganathan, S., Torbenson, M. S., Duncan, A. W., et al. (2022) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2022.02.018 · Cited by 18 · see citing works
Self-citationBehrens, K., Brajanovski, N., Xu, Z., Viney, E. M., DiRago, L., Hediyeh-zadeh, S., Davis, M. J., Pearson, R. B., Sanij, E., Alexander, W. S., et al. (2024) · Science Advances · doi:10.1126/sciadv.adj8803 · Cited by 17 · see citing works
The Multiple Faces of MNT and Its Role as a MYC Modulator
Liaño-Pons, J., Arsenian‐Henriksson, M., & León, J. (2021) · Cancers · doi:10.3390/cancers13184682 · Cited by 17 · see citing works
mRNA interactions with disordered regions control protein activityPreprint
Luo, Y., Pratihar, S., Horste, E., Mitschka, S., Mey, A. S. J. S., Al‐Hashimi, H. M., & Mayr, C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.18.529068 · Cited by 17 · see citing works
Lafita‐Navarro, M. C., Liaño-Pons, J., Quintanilla, A., Varela, I., Blanco, R. E., Ourique, F., Bretones, G., Aresti, J., Molina, E., Carroll, P. A., et al. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.010389 · Cited by 15 · see citing works
Self-citationThe transcriptional co-repressor Runx1t1 is essential for MYCN-driven neuroblastoma tumorigenesis
Murray, J. E., Valli, E., Milazzo, G., Mayoh, C., Gifford, A. J., Fletcher, J. I., Xue, C., Jayatilleke, N., Salehzadeh, F., Gamble, L. D., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-49871-0 · Cited by 14 · see citing works
Yang, B., Zhang, J., Wang, J., Fan, W., Barbier‐Torres, L., Yang, X., Justo, M., Liu, T., Chen, Y., Steggerda, J. A., et al. (2023) · Hepatology Communications · doi:10.1097/hc9.0000000000000144 · Cited by 13 · see citing works
Llabata, P., Torres-Diz, M., Gómez, A., Tomás-Daza, L., Romero, O. A., Grego‐Bessa, J., Llinàs‐Arias, P., Valencia, A., Esteller, M., Javierre, B. M., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2024824118 · Cited by 13 · see citing works
Circular RNAs increase during vascular cell differentiation and are biomarkers for vascular disease
Northoff, B. H., Herbst, A., Wenk, C., Weindl, L., Gäbel, G., Brezski, A., Zarnack, K., Küpper, A., Dimmeler, S., Moretti, A., et al. (2025) · Cardiovascular Research · doi:10.1093/cvr/cvaf013 · Cited by 12 · see citing works
Restoration of miR-193a expression is tumor-suppressive in MYC amplified Group 3 medulloblastoma
Bharambe, H. S., Joshi, A. A., Yogi, K., Kazi, S., & Shirsat, N. V. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-00942-5 · Cited by 12 · see citing works
Wang, L., Yang, B., Xu, Z., Song, X., Gong, Z., Xue, S., & Kong, L. (2021) · Cell Cycle · doi:10.1080/15384101.2021.1897272 · Cited by 11 · see citing works
Ghobadi, M. Z., Afsaneh, E., & Emamzadeh, R. (2023) · Medical Microbiology and Immunology · doi:10.1007/s00430-023-00767-8 · Cited by 7 · see citing works
Charoenngam, N., Thaneerat, N., Likasitwatanakul, P., Kansuttiviwat, C., & Mannstadt, M. (2025) · Endocrine Practice · doi:10.1016/j.eprac.2025.12.022 · Cited by 6 · see citing works
Huang, Z., Chu, T., Ma, A., Lin, W., Gao, Y., Zhang, N., Shi, M., Zhang, X., Yang, Y., & Ma, W. (2025) · Biochemical Pharmacology · doi:10.1016/j.bcp.2025.116843 · Cited by 6 · see citing works
Lessons from Using Genetically Engineered Mouse Models of MYC-Induced Lymphoma
Winkler, R., Piskor, E.-M., & Kosan, C. (2022) · Cells · doi:10.3390/cells12010037 · Cited by 6 · see citing works
MNT suppresses T cell apoptosis via BIM and is critical for T lymphomagenesis
Nguyen, H. V., Vandenberg, C. J., Robati, M., Ng, A. P., & Cory, S. (2023) · Cell Death and Differentiation · doi:10.1038/s41418-023-01119-y · Cited by 5 · see citing works
METTL16-mediated inhibition of MXD4 promotes leukemia through activation of the MYC-MAX axis
Bove, G., Babaei, M., Bueno-Costa, A., Amin, S., Simonelli, N., Benedetti, R., Dell’Aversana, C., Conte, M., Montella, L., Summa, V., et al. (2025) · Oncogene · doi:10.1038/s41388-025-03563-1 · Cited by 4 · see citing works
Polycomb group ring finger protein 6 suppresses Myc-induced lymphomagenesis
Tanasković, N., Dalsass, M., Ceccotti, G., Filipuzzi, M., Verrecchia, A., Nicoli, P., Doni, M., Olivero, D., Pasini, D., Koseki, H., et al. (2022) · Life Science Alliance · doi:10.26508/lsa.202101344 · Cited by 4 · see citing works
MAX controls meiotic entry in sexually undifferentiated germ cells
Suzuki, A., Uranishi, K., Nishimoto, M., Mizuno, Y., Mizuno, S., Takahashi, S., Eisenman, R. N., & Okuda, A. (2024) · Scientific Reports · doi:10.1038/s41598-024-55506-7 · Cited by 3 · see citing works
Self-citationMouse tumor susceptibility genes identify drug combinations for multiple myeloma
Zhang, S., Dubois, W., Zhang, K., Simmons, J. K., Hughitt, V. K., Gorjifard, S., Gaikwad, S. M., Peat, T. J., & Mock, B. A. (2020) · Journal of Cancer Metastasis and Treatment · doi:10.20517/2394-4722.2020.40 · Cited by 3 · see citing works
Dichotomous Impact of Myc on rRNA Gene Activation and Silencing in B Cell Lymphomagenesis
Joshi, G., Eberhardt, A. O., Lange, L. D., Winkler, R., Hoffmann, S., Kosan, C., & Bierhoff, H. (2020) · Cancers · doi:10.3390/cancers12103009 · Cited by 2 · see citing works
Transcriptional Regulation of Early B-Cell Development
Ng, A. P., Morris, R., & Nutt, S. L. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-95895-0.00014-3 · Cited by 2 · see citing works
A synthetic benzoxazine dimer derivative targets c‐Myc to inhibit colorectal cancer progression
Sriratanasak, N., Nutho, B., Wattanathana, W., Phaonakrop, N., Panasawatwong, B., Erlenbach‐Wuensch, K., Roytrakul, S., Schneider‐Stock, R., & Pithi Chanvorachote, B. (2025) · Molecular Oncology · doi:10.1002/1878-0261.70127 · Cited by 1 · see citing works
Multiple endocrine neoplasia type 5: emerging evidence and clinical perspectives
Charoenngam, N., & Mannstadt, M. (2026) · Endocrine Related Cancer · doi:10.1530/erc-25-0219 · Cited by 1 · see citing works
MYC through the lens ofG&DPreprint
Eisenman, R. N. (2023) · Genes & Development · doi:10.1101/gad.350467.123
Self-citationCai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603340
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603376
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603352
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603346
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603364
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603379
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603358
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603373
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603367
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603349
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603370
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603355
Cai, S., Hu, B., Wang, X., Liu, T., Lin, Z., Tong, X., Xu, R., Chen, M., Duo, T., Zhu, Q., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22603361
Gene Amplification of Mediator Subunit 30 Redirects the MYC Transcriptional Program and OncogenesisPreprint
Jin, C., Zhao, L., Zhao, G., Liu, Y., Ma, W., Ma, S., Yao, L., Liu, Y., Wu, Q., Yuan, H., et al. (2024) · Research Square · doi:10.21203/rs.3.rs-4326418/v1
Zheng, Y., Yin, X., Han, L., Liu, S., Zhang, N., Yang, Y., & Yang, M. (2025) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2025.110576
Li, S., Yang, C., Li, J., Liu, Z., Gong, F., Ke, X., Ruan, G., & Huang, H. (2025) · Scientific Reports · doi:10.1038/s41598-025-26545-5
Roy, V., Montagne, M., & Lavigne, P. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.01.715400
Yang, J., Ogunsola, S. S., Wong, J., Wang, A., Joehanes, R., Levy, D. A., Sharma, S., Liu, C., & Xie, J. (2026) · Genome biology · doi:10.1186/s13059-026-04094-y
Nguyen, H. V., Michla, M., Yan, F., Davidson, N., Kelly, G. L., Strasser, A., & Cory, S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.29.721758
Jin, C., Zhao, L., Ma, W., Zhao, G., Liu, Y., Zhang, H., Ma, S., Yao, L., Liu, Y., Wu, Q., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117498
Targeting MYC-Driven Cancers: From Oncogenic Addiction to Therapeutic Vulnerability
Sainero‐Alcolado, L., Lama, D., Alzrigat, M., & Arsenian‐Henriksson, M. (2026) · BioDrugs · doi:10.1007/s40259-026-00798-6
BindingDB Entry 50021153: MYC the oncogene from hell: Novel opportunities for cancer therapy.
BindingDB (2025) · UC San Diego · doi:10.7270/q2qz2gkz
- Authors
- Mathsyaraja, H., Freie, B., Cheng, P.-F., Babaeva, E., Catchpole, J. T., Janssens, D., Henikoff, S., & Eisenman, R. N.
- Affiliations
- Fred Hutch Cancer Center (US)
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2019-08-08
- Volume
- 33
- Issue
- 17-18
- Pages
- 1252-1264
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC6719623
- OpenAlex
- W2967722042
- Cited by
- 54
- References
- 58
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 6 · 2023: 8 · 2022: 9 · 2021: 7 · 2020: 11
- Type
- posted content
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Genes & Development (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Institutes of Health/National Cancer Institute (RO1 CA057138, R35 CA 231989)
- Topics
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Health Sciences › Medicine › Pathology and Forensic Medicine › Lymphoma Diagnosis and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- Max, c-Myc, MYC protein stability, B cell development, medical nutrition therapy, lymphoma
- MeSH terms
- Animals, Enzyme Inhibitors, Humans, Indoles, Kynurenine, Lymphoma, Organoids, Oximes, Sulfonamides, Gene Expression Regulation, Neoplastic, Proto-Oncogene Proteins c-myc, Gene Deletion, Active Transport, Cell Nucleus, Cell Line, Tumor, Basic-Leucine Zipper Transcription Factors, Mice, Carcinogenesis
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