Integrated nuclear proteomics and transcriptomics identifies S100A4 as a therapeutic target in acute myeloid leukemia
Open accessAbstract
Abstract Inappropriate localization of proteins can interfere with normal cellular function and drive tumor development. To understand how this contributes to the development of acute myeloid leukemia (AML), we compared the nuclear proteome and transcriptome of AML blasts with normal human CD34 + cells. Analysis of the proteome identified networks and processes that significantly affected transcription regulation including misexpression of 11 transcription factors with seven proteins not previously implicated in AML. Transcriptome analysis identified changes in 40 transcription factors but none of these were predictive of changes at the protein level. The highest differentially expressed protein in AML nuclei compared with normal CD34 + nuclei (not previously implicated in AML) was S100A4. In an extended cohort, we found that over-expression of nuclear S100A4 was highly prevalent in AML (83%; 20/24 AML patients). Knock down of S100A4 in AML cell lines strongly impacted their survival whilst normal hemopoietic stem progenitor cells were unaffected. These data are the first analysis of the nuclear proteome in AML and have identified changes in transcription factor expression or regulation of transcription that would not have been seen at the mRNA level. These data also suggest that S100A4 is essential for AML survival and could be a therapeutic target in AML.
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?
A prior study found altered expression of 13 hnRNPs involved in mRNA processing in AML.
“A recent study reported expression changes in 13 hnRNPs affecting mRNA processing in AML (39), among which hnRNP A1, A2B1, and C were predicted to bind to the NOCIVA junction site.”
From Discovery of a Novel CIP2A Variant (NOCIVA) with Clinical Relevance in Predicting TKI Resistance in Myeloid Leukemias (2021) · cites this paper as [39]
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
Genomic and Epigenomic Landscapes of Adult De Novo Acute Myeloid Leukemia
The Cancer Genome Atlas Research Network (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1301689 · Cited by 5,078 · see citing works
Insights into the regulation of protein abundance from proteomic and transcriptomic analyses
Vogel, C., & Marcotte, E. M. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3185 · Cited by 4,195 · see citing works
Donato, R., Cannon, B. R., Sorci, G., Riuzzi, F., Hsu, K., Weber, D. J., & Geczy, C. L. (2012) · Current Molecular Medicine · doi:10.2174/156652413804486214 · Cited by 1,322 · see citing works
Bresnick, A. R., Weber, D. J., & Zimmer, D. B. (2015) · Nature reviews. Cancer · doi:10.1038/nrc3893 · Cited by 826 · see citing works
Acute myeloid leukaemia in adults
Ferrara, F., & Schiffer, C. A. (2013) · The Lancet · doi:10.1016/s0140-6736(12)61727-9 · Cited by 566 · see citing works
Roles of the NFI/CTF gene family in transcription and development
Gronostajski, R. M. (2000) · Gene · doi:10.1016/s0378-1119(00)00140-2 · Cited by 545 · see citing works
S100A4, a Mediator of Metastasis
Garrett-Thomson, S. C., Varney, K. M., Weber, D. J., & Bresnick, A. R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.r500017200 · Cited by 352 · see citing works
Bagger, F. O., Sasivarevic, D., Sohi, S. H., Laursen, L. G., Pundhir, S., Sønderby, C. K., Winther, O., Rapin, N., & Porse, B. T. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1101 · Cited by 330 · see citing works
miR-126 Regulates Distinct Self-Renewal Outcomes in Normal and Malignant Hematopoietic Stem Cells
Lechman, E. R., Gentner, B., Ng, S. W. K., Schoof, E. M., van Galen, P., Kennedy, J. A., Nucera, S., Ciceri, F., Kaufmann, K. B., Takayama, N., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2015.12.011 · Cited by 269 · see citing works
Functional proteomic profiling of AML predicts response and survival
Kornblau, S. M., Tibes, R., Qiu, Y. H., Chen, W., Kantarjian, H. M., Andreeff, M., Coombes, K. R., & Mills, G. B. (2008) · Blood · doi:10.1182/blood-2007-10-119438 · Cited by 265 · see citing works
Davies, B. R., Davies, M. P. A., Gibbs, F. E. M., Barraclough, R., & Rudland, P. S. (1993) · PubMed · Cited by 251 · see citing works
Rps14 haploinsufficiency causes a block in erythroid differentiation mediated by S100A8 and S100A9
Schneider, R. K., Schenone, M., Ferreira, M. S. V., Kramann, R., Joyce, C. E., Hartigan, C. R., Beier, F., Brümmendorf, T. H., Germing, U., Platzbecker, U., et al. (2016) · Nature Medicine · doi:10.1038/nm.4047 · Cited by 236 · see citing works
Kohlmann, A., Kipps, T. J., Rassenti, L. Z., Downing, J. R., Shurtleff, S. A., Mills, K., Gilkes, A., Hofmann, W., Basso, G., Dell’Orto, M. C., et al. (2008) · British Journal of Haematology · doi:10.1111/j.1365-2141.2008.07261.x · Cited by 220 · see citing works
Young, V. R., Haverberg, L. N., Bilmazes, C., & Munro, H. N. (1973) · Metabolism · doi:10.1016/0026-0495(73)90257-6 · Cited by 218 · see citing works
S100A4 in cancer progression and metastasis: A systematic review
Fei, F., Qu, J., Zhang, M., Li, Y., & Zhang, S. (2017) · Oncotarget · doi:10.18632/oncotarget.18016 · Cited by 200 · see citing works
Saleem, M., Kweon, M., Johnson, J. J., Adhami, V. M., Elcheva, I. A., Khan, N., Hafeez, B. B., Bhat, K. M. R., Sarfaraz, S., Reagan‐Shaw, S., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606747103 · Cited by 196 · see citing works
Phosphoproteomic Analysis of Human Embryonic Stem Cells
Brill, L. M., Xiong, W., Lee, K., Ficarro, S. B., Crain, A., Xu, Y., Terskikh, A. V., Snyder, E. Y., & Ding, S. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.06.002 · Cited by 189 · see citing works
Autocrine activation of the MET receptor tyrosine kinase in acute myeloid leukemia
Kentsis, A., Reed, C., Rice, K. L., Sanda, T., Rodig, S. J., Tholouli, E., Christie, A. L., Valk, P. J. M., Delwel, R., Ngo, V. N., et al. (2012) · Nature Medicine · doi:10.1038/nm.2819 · Cited by 180 · see citing works
A proximal activator of transcription in epithelial-mesenchymal transition
Venkov, C. D., Link, A. J., Jennings, J. L., Plieth, D., Inoue, T., Nagai, K., Xu, C., Dimitrova, Y. N., Rauscher, F. J., & Neilson, E. G. (2007) · Journal of Clinical Investigation · doi:10.1172/jci29544 · Cited by 170 · see citing works
Strains and micromotions of press-fit femoral stem prostheses
Walker, P. S., Schneeweis, D., Murphy, S. B., & Nelson, P. (1987) · Journal of Biomechanics · doi:10.1016/0021-9290(87)90035-2 · Cited by 169 · see citing works
Pathologies Involving the S100 Proteins and Rage
Heizmann, C. W., Ackermann, G. E., & Galichet, A. (2007) · Springer eBooks · doi:10.1007/978-1-4020-6191-2_5 · Cited by 160 · see citing works
Ilf3 and NF90 functions in RNA biology
Castella, S., Bernard, R., Corno, M., Fradin, A., & Larcher, J.-C. (2014) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1270 · Cited by 157 · see citing works
Rapin, N., Bagger, F. O., Jendholm, J., Mora-Jensen, H. I., Krogh, A., Kohlmann, A., Thiede, C., Borregaard, N., Bullinger, L., Winther, O., et al. (2013) · Blood · doi:10.1182/blood-2013-02-485771 · Cited by 152 · see citing works
Gallardo, M., Lee, H. J., Zhang, X., Bueso-Ramos, C., Pageon, L. R., McArthur, M., Multani, A., Nazha, A., Manshouri, T., Parker-Thornburg, J., et al. (2015) · Cancer Cell · doi:10.1016/j.ccell.2015.09.001 · Cited by 145 · see citing works
S100A9 induces differentiation of acute myeloid leukemia cells through TLR4
Laouedj, M., Tardif, M. R., Gil, L., Raquil, M.-A., Lachhab, A., Pelletier, M., Tessier, P. A., & Barabé, F. (2017) · Blood · doi:10.1182/blood-2016-09-738005 · Cited by 142 · see citing works
Lo, J., Yu, C.-C., Chiou, S., Huang, K. C., Jan, C.-I., Lin, S., Liu, C., Hu, W., & Yu, Y. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-2350 · Cited by 133 · see citing works
Complexity of CEBPA Dysregulation in Human Acute Myeloid Leukemia
Pabst, T., & Mueller, B. U. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-2941 · Cited by 115 · see citing works
Banerji, V., Frumm, S. M., Ross, K. N., Li, L. S., Schinzel, A. C., Hahn, C. K., Kakoza, R. M., Chow, K. T., Ross, L., Alexe, G., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci46465 · Cited by 105 · see citing works
The convergent roles of the nuclear factor I transcription factors in development and cancer
Chen, K., Lim, J. W. C., Richards, L. J., & Bunt, J. (2017) · Cancer Letters · doi:10.1016/j.canlet.2017.09.015 · Cited by 98 · see citing works
Protein mislocalization: Mechanisms, functions and clinical applications in cancer
Wang, X., & Li, S. (2014) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2014.03.006 · Cited by 97 · see citing works
S100A4 interacts with p53 in the nucleus and promotes p53 degradation
Orre, L. M., Panizza, E., Kaminskyy, V. O., Vernet, E., Gräslund, T., Zhivotovsky, B., & Lehtiö, J. (2013) · Oncogene · doi:10.1038/onc.2013.213 · Cited by 96 · see citing works
Kikuchi, N., Horiuchi, A., Osada, R., Imai, T., Wang, C., Chen, X., & Konishi, I. (2006) · Cancer Science · doi:10.1111/j.1349-7006.2006.00295.x · Cited by 92 · see citing works
Schwarzinger, I., Valent, P., Köller, U., Marosi, C., Schneider, B., Haas, O. A., Knapp, W., Lechner, K., & Bettelheim, P. (1990) · Journal of Clinical Oncology · doi:10.1200/jco.1990.8.3.423 · Cited by 92 · see citing works
Tonks, A., Pearn, L., Musson, M., Gilkes, A., Mills, K., Burnett, A. K., & Darley, R. L. (2007) · Leukemia · doi:10.1038/sj.leu.2404961 · Cited by 89 · see citing works
Induction of C/EBPα activity alters gene expression and differentiation of human CD34+ cells
Cammenga, J., Mulloy, J. C., Berguido, F. J., MacGrogan, D., Viale, A. J., & Nimer, S. D. (2003) · Blood · doi:10.1182/blood-2002-05-1546 · Cited by 86 · see citing works
Flatmark, K., Boye, K., Nesland, J. M., Rasmussen, H., Aamodt, G., Mikalsen, S., Bjørnland, K., Fodstad, Ø., & Mælandsmo, G. M. (2003) · The Journal of Pathology · doi:10.1002/path.1381 · Cited by 82 · see citing works
NFI Transcription Factors Interact with FOXA1 to Regulate Prostate-Specific Gene Expression
Grabowska, M. M., Elliott, A. D., DeGraff, D. J., Anderson, P. D., Anumanthan, G., Yamashita, H., Sun, Q., Friedman, D. B., Hachey, D. L., Yu, X., et al. (2014) · Molecular Endocrinology · doi:10.1210/me.2013-1213 · Cited by 75 · see citing works
S100A16, a ubiquitously expressed EF-hand protein which is up-regulated in tumors
Marenholz, I., & Heizmann, C. W. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2003.11.115 · Cited by 74 · see citing works
Classification and risk assessment in AML: integrating cytogenetics and molecular profiling
Moarii, M., & Papaemmanuil, E. (2017) · Hematology · doi:10.1182/asheducation-2017.1.37 · Cited by 73 · see citing works
Cancer predisposition in mice deficient for the metastasis-associated Mts1(S100A4) gene
El-Naaman, C., Grum-Schwensen, B., Mansouri, A., Grigorian, M., Santoni‐Rugiu, E., Hansen, T. F., Kriajevska, M. V., Schäfer, B. W., Heizmann, C. W., Lukanidin, E. M., et al. (2004) · Oncogene · doi:10.1038/sj.onc.1207420 · Cited by 63 · see citing works
Tajeddine, N., Gala, J., Louis, M., Schoor, M. C., TOMBAL, B. F., & Gailly, P. L. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4011 · Cited by 63 · see citing works
Expression of S100A8 in leukemic cells predicts poor survival in de novo AML patients
Nicolas‐Virelizier, E., Ramus, C., Berthier, S., Arlotto, M., Bouamrani, A., Lefebvre, C., Morel, F., Garin, J., Ifrah, N., Berger, F. R., et al. (2010) · Leukemia · doi:10.1038/leu.2010.251 · Cited by 62 · see citing works
Morgan, G., Pearn, L., Liddiard, K., Pumford, S. L., Burnett, A. K., Tonks, A., & Darley, R. L. (2012) · Leukemia · doi:10.1038/leu.2012.221 · Cited by 61 · see citing works
The AML1-ETO fusion gene promotes extensive self-renewal of human primary erythroid cells
Tonks, A., Pearn, L., Tonks, A. J., Pearce, L., Hoy, T. G., Phillips, S., Fisher, J., Downing, J. R., Burnett, A. K., & Darley, R. L. (2002) · Blood · doi:10.1182/blood-2002-06-1732 · Cited by 58 · see citing works
High expression of HMGA2 independently predicts poor clinical outcomes in acute myeloid leukemia
Marquis, M., Beaubois, C., Lavallée, V., Abrahamowicz, M., Danieli, C., Lemieux, S., Ahmad, I., Wei, A. H., Ting, S. B., Fleming, S. A., et al. (2018) · Blood Cancer Journal · doi:10.1038/s41408-018-0103-6 · Cited by 53 · see citing works
Shmelkov, E., Tang, Z., Aifantis, I., & Statnikov, A. (2011) · Biology Direct · doi:10.1186/1745-6150-6-15 · Cited by 51 · see citing works
Miranda, K. J., Loeser, R. F., & Yammani, R. R. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.125898 · Cited by 50 · see citing works
S100A4 overexpression proves to be independent marker for breast cancer progression
Ismail, N. I., Kaur, G., Hashim, H., & Hassan, M. S. (2008) · Cancer Cell International · doi:10.1186/1475-2867-8-12 · Cited by 50 · see citing works
A quantitative analysis of heterogeneities and hallmarks in acute myelogenous leukaemia
Hu, C. W., Qiu, Y., Ligeralde, A., Raybon, A. Y., Yoo, S., Coombes, K. R., Qutub, A. A., & Kornblau, S. M. (2019) · Nature Biomedical Engineering · doi:10.1038/s41551-019-0387-2 · Cited by 46 · see citing works
Cohn, M. A. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.16.3335 · Cited by 43 · see citing works
Identification of differentially expressed genes and their upstream regulators in colorectal cancer
Liu, H., & Zhang, C. J. (2017) · Cancer Gene Therapy · doi:10.1038/cgt.2017.8 · Cited by 43 · see citing works
Emerging Roles for hnRNPs in post-transcriptional regulation: what can we learn from flies?
Piccolo, L. L., Corona, D. F. V., & Onorati, M. C. (2014) · Chromosoma · doi:10.1007/s00412-014-0470-0 · Cited by 37 · see citing works
New Fusion Transcripts Identified in Normal Karyotype Acute Myeloid Leukemia
Wen, H., Li, Y., Malek, S. N., Kim, Y. C., Xu, J., Chen, P., Xiao, F., Huang, X., Zhou, X., Xuan, Z., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051203 · Cited by 36 · see citing works
Aetiology of hyperthyroidism. I.
Hoffenberg, R. (1974) · BMJ · doi:10.1136/bmj.3.5928.452 · Cited by 31 · see citing works
Reis, H., Pütter, C., Megger, D. A., Bracht, T., Weber, F., Hoffmann, A.-C., Bertram, S., Wohlschläger, J., Hagemann, S., Eisenacher, M., et al. (2014) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2014.10.024 · Cited by 29 · see citing works
Trost, M., Sauvageau, M., Hérault, O., Déléris, P., Pomiès, C., Chagraoui, J., Mayotte, N., Meloche, S., Sauvageau, G., & Thibault, P. (2012) · Blood · doi:10.1182/blood-2011-12-397844 · Cited by 28 · see citing works
Tajeddine, N., Louis, M., Vermylen, C., Gala, J., TOMBAL, B. F., & Gailly, P. L. (2008) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428190802035933 · Cited by 23 · see citing works
S100A4 May Be a Good Prognostic Marker and a Therapeutic Target for Colon Cancer
Destek, S., & Gül, V. O. (2018) · Journal of Oncology · doi:10.1155/2018/1828791 · Cited by 23 · see citing works
Routine immunophenotyping in acute leukemia: Role in lineage assignment and reassignment
Qadir, M., Barcos, M. P., Stewart, C. C., Sait, S. N. J., Ford, L. A., & Baer, M. R. (2006) · Cytometry Part B Clinical Cytometry · doi:10.1002/cyto.b.20112 · Cited by 18 · see citing works
Clinicopathologic significance of S100A4 expression in osteosarcoma.
Cao, C.-M., Fx, Y., Pl, W., Qx, Y., & Xr, S. (2014) · PubMed · Cited by 18 · see citing works
Helen, S., Chaudry, S. F., Crichlow, A., Feilding, F. L., & Chevassut, T. J. T. (2018) · Bone Marrow Research · doi:10.1155/2018/5742954 · Cited by 18 · see citing works
PRAME promotes in vitro leukemia cells death by regulating S100A4/p53 signaling.
Xu, Y., Lj, R., Sl, M., Fl, H., Jh, Z., & Pan, G. (2016) · PubMed · Cited by 17 · see citing works
Zhou, Y., Li, Z., Ding, Y., Zhang, J., Yang, Q., & Wu, Y. (2018) · Journal of Cancer Research and Therapeutics · doi:10.4103/0973-1482.172582 · Cited by 16 · see citing works
Pálfy, G., Kiss, B., Nyitray, L., & Bodor, A. (2016) · ChemBioChem · doi:10.1002/cbic.201600280 · Cited by 15 · see citing works
P53-dependent suppression of the human calcyclin gene (S100A6): the role of Sp1 and of NFkappaB.
Króliczak, W., Pietrzak, M., & Puzianowska‐Kuźnicka, M. (2008) · Acta Biochimica Polonica · doi:10.18388/abp.2008_3062 · Cited by 14 · see citing works
Guo, X., Shi, P., Li, Y., Huijuan, D., Wang, Y., Zheng, H., & Xu, B. (2018) · Pharmacogenomics · doi:10.2217/pgs-2017-0157 · Cited by 14 · see citing works
Cytosine modifications in myeloid malignancies
Meldi, K. M., & Figueroa, M. E. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.05.002 · Cited by 13 · see citing works
Nucleolar proteins with altered expression in leukemic cell lines
Teittinen, K. J., Kärkkäinen, P., Salonen, J., Rönnholm, G., Korkeamäki, H., Vihinen, M., Kalkkinen, N., & Lohi, O. (2011) · Leukemia Research · doi:10.1016/j.leukres.2011.06.038 · Cited by 13 · see citing works
Falini, B., & Martelli, M. P. (2015) · Best Practice & Research Clinical Haematology · doi:10.1016/j.beha.2015.10.005 · Cited by 11 · see citing works
Liu, J., Fu, S., Xu, Y., & Zheng, Z. (2014) · Molecular Medicine Reports · doi:10.3892/mmr.2014.2345 · Cited by 10 · see citing works
S100A4 Is an Independent Prognostic Factor for Patients with Lung Cancer: A Meta-Analysis
Bai, H., Qian, J., & Han, B. (2014) · Genetic Testing and Molecular Biomarkers · doi:10.1089/gtmb.2013.0471 · Cited by 9 · see citing works
Prognostic value of cytoplasmic expression of S100A4 protein in endometrial carcinoma
Chong, H. I., LEE, J. H., Yoon, M. S., Suh, D. S., Kim, K., Kim, J. Y., & Choi, K. U. (2014) · Oncology Reports · doi:10.3892/or.2014.3149 · Cited by 9 · see citing works
Clinical significance of in vivo cytarabine-induced gene expression signature in AML
Lamba, J. K., Pounds, S. B., Cao, X., Crews, K. R., Cogle, C. R., Bhise, N., Raimondi, S. C., Downing, J. R., Baker, S. D., Ribeiro, R. C., et al. (2015) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2015.1086918 · Cited by 8 · see citing works
[The differential diagnosis of renal hematuria].
Trebbin, H. (1967) · PubMed · Cited by 2 · see citing works
Flagged first, then by citations
4 of the 78 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Proteomic and phosphoproteomic landscapes of acute myeloid leukemia
Kramer, M. H., Zhang, Q., Sprung, R. W., Day, R. B., Erdmann-Gilmore, P., Li, Y., Xu, Z., Helton, N., George, D. R., Mi, Y., et al. (2022) · Blood · doi:10.1182/blood.2022016033 · Cited by 123 · see citing works
Active Akt signaling triggers CLL toward Richter transformation via overactivation of Notch1
Kohlhaas, V., Blakemore, S. J., Al-Maarri, M., Nickel, N., Pál, M., Roth, A. J., Hövelmeyer, N., Schäfer, S. C., Knittel, G., Lohneis, P., et al. (2020) · Blood · doi:10.1182/blood.2020005734 · Cited by 89 · see citing works
Proteomics, Personalized Medicine and Cancer
Su, M., Zhang, Z., Zhou, L., Han, C., Huang, C., & Nice, E. C. (2021) · Cancers · doi:10.3390/cancers13112512 · Cited by 92 · see citing works
Lyu, T., Wang, Y.-N., Li, D., Yang, H., Qin, B., Zhang, W.-L., Li, Z., Cheng, C., Zhang, B.-L., Guo, R.-Q., et al. (2021) · Experimental Hematology & Oncology · doi:10.1186/s40164-021-00220-7 · Cited by 73 · see citing works
S100A4 in the Physiology and Pathology of the Central and Peripheral Nervous System
D’Ambrosi, N., Milani, M., & Apolloni, S. (2021) · Cells · doi:10.3390/cells10040798 · Cited by 50 · see citing works
Landscape of Tumor Suppressor Mutations in Acute Myeloid Leukemia
Panuzzo, C., Signorino, E., Calabrese, C., Ali, M. S., Petiti, J., Bracco, E., & Cilloni, D. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9030802 · Cited by 42 · see citing works
Breckels, L. M., Hutchings, C., Ingole, K. D., Kim, S. Y., Lilley, K. S., Makwana, M. V., McCaskie, K. J. A., & Villanueva, E. (2024) · Cell chemical biology · doi:10.1016/j.chembiol.2024.08.008 · Cited by 41 · see citing works
Long noncoding RNAs have pivotal roles in chemoresistance of acute myeloid leukemia
Izadirad, M., Jafari, L., James, A. R., Unfried, J. P., Wu, Z., & Chen, Z. (2021) · Drug Discovery Today · doi:10.1016/j.drudis.2021.03.017 · Cited by 37 · see citing works
van Dijk, A. D., de Bont, E. S. J. M., & Kornblau, S. M. (2020) · Expert Review of Proteomics · doi:10.1080/14789450.2020.1717951 · Cited by 34 · see citing works
Zhang, J., Peng, Y., He, Y., Xiao, Y. C., Wang, Q., Zhao, Y., Zhang, T., Wu, C.-X., Xie, Y., Zhou, J., et al. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2021.166268 · Cited by 34 · see citing works
Mass Spectrometry–Based Proteogenomics: New Therapeutic Opportunities for Precision Medicine
Joshi, S. K., Piehowski, P., Liu, T., Gosline, S. J. C., McDermott, J., Druker, B. J., Traer, E. A., Tyner, J. W., Agarwal, A., Tognon, C. E., et al. (2023) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-022723-113921 · Cited by 31 · see citing works
Application of omics in the diagnosis, prognosis, and treatment of acute myeloid leukemia
Zhang, Z., Huang, J., Zhang, Z., Shen, H., Tang, X., Wu, D., Bao, X., Xu, G., & Chen, S. (2024) · Biomarker Research · doi:10.1186/s40364-024-00600-1 · Cited by 30 · see citing works
Isoform-specific and signaling-dependent propagation of acute myeloid leukemia by Wilms tumor 1
Potluri, S., Assi, S. A., Chin, P. S., Coleman, D. J. L., Pickin, A., Moriya, S., Seki, N., Heidenreich, O. T., Cockerill, P. N., & Bonifer, C. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109010 · Cited by 21 · see citing works
Guo, L., Liu, J., Yang, Y., Zeng, Y., Yuan, F., Zhong, F., Jin, Y., Wan, R., & Liu, W. (2021) · Food Bioscience · doi:10.1016/j.fbio.2021.101214 · Cited by 22 · see citing works
Proteomic Characterization of Acute Myeloid Leukemia for Precision Medicine
Casado, P., & Cutillas, P. R. (2023) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2023.100517 · Cited by 19 · see citing works
Mäkelä, E., Pavic, K., Varila, T., Salmenniemi, U., Löyttyniemi, E., Nagelli, S. G., Ammunét, T., Kähäri, V.-M., Clark, R. E., Elo, L. L., et al. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-3679 · Cited by 18 · see citing works
Cancer network pharmacology: multi-network regulatory mechanisms and future directions
Zhao, Z., Le, J., Fu, Z., Yang, S., & Chen, Y. (2025) · Medical Oncology · doi:10.1007/s12032-025-02811-4 · Cited by 20 · see citing works
Hernandez-Valladares, M., Bruserud, Ø., & Selheim, F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186830 · Cited by 18 · see citing works
Maddala, R., Gao, J., Mathias, R. T., Lewis, T. R., Arshavsky, V. Y., Levine, A., Backer, J., Bresnick, A. R., & Rao, P. V. (2021) · Scientific Reports · doi:10.1038/s41598-021-81611-y · Cited by 17 · see citing works
Crosstalk between β-catenin and WT1 signaling activity in acute myeloid leukemia
Wagstaff, M., Tsaponina, O., Caalim, G., Greenfield, H. M., Milton‐Harris, L., Mancini, E. J., Blair, A., Heesom, K. J., Tonks, A., Darley, R. L., et al. (2022) · Haematologica · doi:10.3324/haematol.2021.280294 · Cited by 16 · see citing works
Omics approaches: Role in acute myeloid leukemia biomarker discovery and therapy
Shafiei, F. S., Abroun, S., Vahdat, S., & Rafiee, M. (2025) · Cancer Genetics · doi:10.1016/j.cancergen.2024.12.006 · Cited by 15 · see citing works
Advancements in Oncoproteomics Technologies: Treading toward Translation into Clinical Practice
Punetha, A., & Kotiya, D. (2023) · Proteomes · doi:10.3390/proteomes11010002 · Cited by 12 · see citing works
Yang, L., Gilbertsen, A. J., Smith, K. A., Hong, X., Higgins, L., Guerrero, C. R., & Henke, C. A. (2022) · PROTEOMICS · doi:10.1002/pmic.202200018 · Cited by 14 · see citing works
Hernandez-Valladares, M., Wangen, R., Aasebø, E., Reikvam, H., Berven, F. S., Selheim, F., & Bruserud, Ø. (2021) · Cancers · doi:10.3390/cancers13092143 · Cited by 14 · see citing works
Liu, M., Wang, Y., Miettinen, J. J., Kumari, R., Majumder, M. M., Tierney, C., Bazou, D., Parsons, A., Suvela, M. H., Lievonen, J., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.723016 · Cited by 14 · see citing works
Yan, J., Fang, X., Feng, Y., Cui, X., Li, F., Luo, W., Ma, X., Liang, J., & Feng, J. (2022) · Annals of Hepatology · doi:10.1016/j.aohep.2022.100681 · Cited by 14 · see citing works
Plasma Proteomic Signature Predicts Myeloid Neoplasm Risk
Tran, D., Beeler, J. S., Liu, J., Wiley, B. J., Chan, I. C. C., Xin, Z., Kramer, M. H., Batchi-Bouyou, A. L., Zong, X., Walter, M. J., et al. (2024) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-23-3468 · Cited by 12 · see citing works
SFPQ Promotes Lung Cancer Malignancy via Regulation of CD44 v6 Expression
Yang, L., Yang, J., Jacobson, B. A., Gilbertsen, A. J., Smith, K. A., Higgins, L., Guerrero, C. R., Hong, X., Henke, C. A., & Lin, J. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.862250 · Cited by 12 · see citing works
Peng, Y., Zhang, J., Zhang, T., Wang, C., Bai, J., Li, Y., Duan, J., Fan, D., Fu, W., Liang, X., et al. (2024) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2024.167498 · Cited by 11 · see citing works
Ramandi, N. F., Faranoush, M., Ghassempour, A., & Aboul-Enein, H. Y. (2021) · Critical Reviews in Analytical Chemistry · doi:10.1080/10408347.2021.1871844 · Cited by 10 · see citing works
The correlation between proteoglycan 2 and neuropsychiatric systemic lupus erythematosus
Qiao, X., Lu, L., Zhou, K., Tan, L., Liu, X., Ni, J., Hou, Y., Liang, J. F., & Dou, H. (2022) · Clinical Immunology · doi:10.1016/j.clim.2022.109042 · Cited by 10 · see citing works
Deregulated calcium signaling in blood cancer: Underlying mechanisms and therapeutic potential
Immanuel, T., Li, J., Green, T. N., Bogdanova, A. Y., & Kalev‐Zylinska, M. L. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1010506 · Cited by 9 · see citing works
Bae, S.-G., Kim, H., Kim, M. Y., Kim, D. H., Shin, S.-I., Ahn, J., & Park, J. (2023) · Molecules and Cells · doi:10.14348/molcells.2023.0093 · Cited by 9 · see citing works
Liu, L., & Qiang, X. (2022) · Hematology · doi:10.1080/16078454.2022.2113574 · Cited by 9 · see citing works
Rastogi, N., Menendez-Gonzalez, J. B., Srivastava, V. K., Alanazi, B. S., Alanazi, R. N. S., Hughes, O. M., O'Neill, N., Gilkes, A., Ashley, N., Deshpande, S., et al. (2022) · Leukemia · doi:10.1038/s41375-022-01801-z · Cited by 8 · see citing works
Tegaserod maleate exhibits antileukemic activity by targeting TRPM8
Xie, X., Yang, W., Zhang, W., Qiu, Y., Qiu, Z., Wang, H., Hu, Y., Li, Y., Zhou, X., Li, L., et al. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113566 · Cited by 8 · see citing works
Nie, L., Zhang, Y., You, Y., Lin, C., Li, Q., Deng, W., Ma, J., Luo, W., & He, H. (2022) · Hematology · doi:10.1080/16078454.2022.2107970 · Cited by 7 · see citing works
Zhang, W., Liu, B., Wu, S., & Zhao, L. (2023) · Open Medicine · doi:10.1515/med-2022-0602 · Cited by 7 · see citing works
Mishra, S., Liu, J., Chai, L., & Tenen, D. G. (2021) · Current Opinion in Hematology · doi:10.1097/moh.0000000000000692 · Cited by 14 · see citing works
Oncoproteomic profiling of AML: moving beyond genomics
Joshi, S. K., Tognon, C. E., Druker, B. J., & Rodland, K. (2022) · Expert Review of Proteomics · doi:10.1080/14789450.2023.2176757 · Cited by 5 · see citing works
Yao, C., Lin, C., Wang, Y., Hsu, C., Kao, C., Hou, H., Chou, W., & Tien, H. (2022) · Journal of the Formosan Medical Association · doi:10.1016/j.jfma.2022.11.003 · Cited by 5 · see citing works
Proteogenomic profiling of acute myeloid leukemia to identify therapeutic targets
Murray, H. C., Sillar, J. R., Chambers, M., & Verrills, N. M. (2024) · Expert Review of Proteomics · doi:10.1080/14789450.2024.2431272 · Cited by 4 · see citing works
Morris, V. S., Ghazi, H., Fletcher, D. M., & Guinn, B. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24119667 · Cited by 3 · see citing works
MSI2 mediates WNT/β-Catenin pathway function in hematopoietic stem cells
Zhang, H., Guo, R., Li, Z., Ma, R., Xu, S., Yin, L., Zhu, H., Huang, Z., Xing, C., Yang, Y., et al. (2024) · Leukemia · doi:10.1038/s41375-024-02447-9 · Cited by 3 · see citing works
Fu, Z., Chen, C., Wang, S., Wang, J., & Chen, S. (2025) · BMC Biology · doi:10.1186/s12915-025-02315-7 · Cited by 2 · see citing works
Wang, F., Li, M., Cui, N., Fu, Q., Li, F., & Gu, Z. (2025) · Scientific Reports · doi:10.1038/s41598-025-17288-4 · Cited by 2 · see citing works
FANS Unfixed: Isolation and Proteomic Analysis of Mouse Cell Type-Specific Brain Nuclei
Bedwell, L., Mavrotas, M., Demchenko, N., Yaa, R. M., Willis, B., Demianová, Z., Syed, N., Whitwell, H. J., & Nott, A. (2024) · Journal of Proteome Research · doi:10.1021/acs.jproteome.4c00161 · Cited by 3 · see citing works
Rodland, K., & Zhang, B. (2025) · Expert Review of Proteomics · doi:10.1080/14789450.2025.2580647 · Cited by 2 · see citing works
Chen, H., Zhao, X., Pan, W., & Xiao, H. (2023) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428194.2023.2232493 · Cited by 1 · see citing works
Proteomic approaches for untangling pharmacological targets in acute myelogenous leukemia
Reikvam, H., Hemsing, A. L., Hernandez-Valladares, M., & Birkeland, E. (2022) · Expert Review of Proteomics · doi:10.1080/14789450.2022.2067530 · Cited by 1 · see citing works
Chen, Z., Ye, L., Wang, X., Tu, F., Li, X., & Wang, S. (2020) · doi:10.21203/rs.3.rs-91594/v1
Mäkelä, E., Pavic, K., Varila, T., Salmenniemi, U., Löyttyniemi, E., Nagelli, S. G., Ammunét, T., Kähäri, V., Clark, R. E., Elo, L. L., et al. (2023) · doi:10.1158/1078-0432.c.6530211
Mäkelä, E., Pavic, K., Varila, T., Salmenniemi, U., Löyttyniemi, E., Nagelli, S. G., Ammunét, T., Kähäri, V., Clark, R. E., Elo, L. L., et al. (2023) · doi:10.1158/1078-0432.c.6530211.v1
Targeting NOTCH in Lymphoid Malignancies
Piffaretti, D., Galimberti, G. A., & Rossi, A. D. (2023) · doi:10.1002/9781119819950.ch29
Naru, J., Othus, M. K. D., Lin, C., Biernacki, M. A., Bleakley, M., Chauncey, T. R., Erba, H. P., Fang, M., Fitzgibbon, M., Gafken, P. R., et al. (2024) · eJHaem · doi:10.1002/jha2.1041
Wang, L., Huang, A., Cheng, B., Hu, X., & Wang, J. (2025) · Frontiers in Pharmacology · doi:10.3389/fphar.2025.1574759
Lyu, T., Wang, Y., Li, D., Yang, H., Qin, B., Zhang, W., Li, Z., Cheng, C., Zhang, B., Guo, R., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14431745
Li, X., Zhang, Y., Wei, X., & Huang, R. (2026) · Annals of Hematology · doi:10.1007/s00277-026-07044-7
Azevedo, A., Leckenby, A., Nicholson, R. I., Menezes, A. C., Davies, S., Gilkes, A., Baker, S., Toghill, R., McCracken, E., Pierce, A., et al. (2026) · Blood Neoplasia · doi:10.1016/j.bneo.2026.100259
Chen, F., Wu, Z., Zhang, F. C., Meng, Y., Liao, H., & Hu, Y. (2026) · Interdisciplinary medicine · doi:10.1002/inmd.70147
Backer, E. D., Oers, F. V., Berneman, Z. N., & Anguille, S. (2026) · Technology in Cancer Research & Treatment · doi:10.1177/15330338261464315
Panda, S., Wang, Y., Dogiparthi, V. R., Becker, M. E., Dhir, A., Lam, C. K., Rivas, C., Alemu, L., Garrett, L. J., Xiao, P., et al. (2026) · Oncogene · doi:10.1038/s41388-026-03956-w
- Authors
- Alanazi, B., Munje, C. R., Rastogi, N., Williamson, A. J. K., Taylor, S., Hole, P. S., Hodges, M., Doyle, M., Baker, S., Gilkes, A. F., Knapper, S., Pierce, A., Whetton, A. D., Darley, R. L., & Tonks, A.
- Affiliations
- Cardiff University (GB)
- University of Glasgow (GB)
- University of Manchester (GB)
- Corresponding author
- Tonks, Alex
- ORCID
- Venue
- Leukemia
- Published
- 2019-10-14
- Volume
- 34
- Issue
- 2
- Pages
- 427-440
- ISSN
- 0887-6924 (ISSN-L)
- 1476-5551
- PMC
- PMC6995695
- OpenAlex
- W2979936029
- Cited by
- 64
- References
- 78
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 8 · 2023: 10 · 2022: 16 · 2021: 14 · 2020: 5
- FWCI
- 6.16
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Leukemia (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion, other-oa)
- Funders
- Prince Mohammed Medical City, Al-Jouf, Saudi Arabia
- EC | European Regional Development Fund - Welsh Government
- Bloodwise (13029, 13005)
- RCUK | Medical Research Council
- Cancer Research UK
- Manchester Experimental Cancer Medicine Centre and NIHR Manchester Biomedical Research Centre
- Health and Care Research Wales
- Topics
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › S100 Proteins and Annexins
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinoids in leukemia and cellular processes
- Keywords
- acute myeloid leukemia, S100A4, nuclear proteome, nuclear transcriptome, transcription factors, transcriptional regulation, protein mislocalization, therapeutic target, CD34+ cells, leukemia cell survival, gene knockdown
- MeSH terms
- S100 Calcium-Binding Protein A4, Adolescent, Adult, Aged, Cell Nucleus, Cells, Cultured, Female, Humans, Male, Middle Aged, Neoplastic Stem Cells, Leukemia, Myeloid, Acute, Antigens, CD34, Proteome, Proteomics, Cell Proliferation, Transcriptome
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