Deep proteomic analysis on biobanked paraffine-archived melanoma with prognostic/predictive biomarker read-out
Open accessAbstract
The discovery of novel protein biomarkers in melanoma is crucial. Our introduction of formalin-fixed paraffin-embedded (FFPE) tumor protocol provides new opportunities to understand the progression of melanoma and open the possibility to screen thousands of FFPE samples deposited in tumor biobanks and available at hospital pathology departments. In our retrospective biobank pilot study, 90 FFPE samples from 77 patients were processed. Protein quantitation was performed by high-resolution mass spectrometry and validated by histopathologic analysis. The global protein expression formed six sample clusters. Proteins such as TRAF6 and ARMC10 were upregulated in clusters with enrichment for shorter survival, and proteins such as AIFI1 were upregulated in clusters with enrichment for longer survival. The cohort's heterogeneity was addressed by comparing primary and metastasis samples, as well comparing clinical stages. Within immunotherapy and targeted therapy subgroups, the upregulation of the VEGFA-VEGFR2 pathway, RNA splicing, increased activity of immune cells, extracellular matrix, and metabolic pathways were positively associated with patient outcome. To summarize, we were able to (i) link global protein expression profiles to survival, and they proved to be an independent prognostic indicator, as well as (ii) identify proteins that are potential predictors of a patient's response to immunotherapy and targeted therapy, suggesting new opportunities for precision medicine developments.
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.
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
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
Cytoscape: A software Environment for integrated models of biomolecular interaction networks
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003) · Genome Research · doi:10.1101/gr.1239303 · Cited by 51,888 · see citing works
KEGG: Kyoto Encyclopedia of Genes and Genomes
Kanehisa, M. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.1.27 · Cited by 37,077 · see citing works
KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232 · see citing works
PD-1 and PD-L1 Immune Checkpoint Blockade to Treat Breast Cancer
Hartkopf, A. D., Taran, F., Wallwiener, M., Walter, C. B., Krämer, B., Grischke, E., & Brucker, S. Y. (2016) · Breast Care · doi:10.1159/000453569 · Cited by 30,989 · see citing works
Wickham, H. (2016) · Use R! · doi:10.1007/978-3-319-24277-4_9 · Cited by 12,675 · see citing works
Complex heatmaps reveal patterns and correlations in multidimensional genomic data
Gu, Z., Eils, R., & Schlesner, M. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw313 · Cited by 10,122 · see citing works
Szklarczyk, D., Gable, A. L., Nastou, K. C., Lyon, D., Kirsch, R., Pyysalo, S., Doncheva, N. T., Legeay, M., Fang, T., Bork, P., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkaa1074 · Cited by 8,056 · see citing works
Molecular signatures database (MSigDB) 3.0
Liberzon, A., Subramanian, A., Pinchback, R., Thorvaldsdóttir, H., Tamayo, P., & Mesirov, J. P. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr260 · Cited by 7,111 · see citing works
Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients
Herbst, R. S., Soria, J.-C., Kowanetz, M., Fine, G. D., Hamid, O., Gordon, M. S., Sosman, J. A., McDermott, D. F., Powderly, J. D., Gettinger, S. N., et al. (2014) · Nature · doi:10.1038/nature14011 · Cited by 5,231 · see citing works
The Gene Ontology resource: enriching a GOld mine
The Gene Ontology Consortium, Carbon, S., Douglass, E., Good, B. M., Unni, D. R., Harris, N. L., Mungall, C. J., Basu, S., Chisholm, R. L., Dodson, R. J., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkaa1113 · Cited by 3,555 · see citing works
Genomic classification of cutaneous melanoma
Akbani, R., Akdemir, K. C., Aksoy, B. A., Albert, M., Ally, A., Amin, S. B., Arachchi, H., Arora, A., Auman, J. T., Ayala, B., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.044 · Cited by 3,151 · see citing works
The reactome pathway knowledgebase
Jassal, B., Matthews, L. R., Viteri, G., Gong, C., Lorente, P., Fabregat, A., Sidiropoulos, K., Cook, J., Gillespie, M. E., Haw, R., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz1031 · Cited by 2,111 · see citing works
Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R
Langfelder, P., Zhang, B., & Horvath, S. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btm563 · Cited by 1,892 · see citing works
Schadendorf, D., van Akkooi, A. C. J., Berking, C., Griewank, K., Gutzmer, R., Hauschild, A., Stang, A., Roesch, A., & Ugurel, S. (2018) · The Lancet · doi:10.1016/s0140-6736(18)31559-9 · Cited by 1,516 · see citing works
The Reactome pathway Knowledgebase
Fabregat, A., Sidiropoulos, K., Garapati, P., Gillespie, M., Hausmann, K., Haw, R., Jassal, B., Jupe, S., Korninger, F., McKay, S., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkv1351 · Cited by 1,201 · see citing works
Acquired Resistance and Clonal Evolution in Melanoma during BRAF Inhibitor Therapy
Shi, H., Hugo, W., Kong, X., Hong, A., Koya, R. C., Moriceau, G., Chodon, T., Guo, R., Johnson, D. B., Dahlman, K. B., et al. (2014) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0642 · Cited by 982 · see citing works
Bevacizumab (Avastin), a humanized anti-VEGF monoclonal antibody for cancer therapy
Ferrara, N., Hillan, K. J., & Novotny, W. F. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.05.132 · Cited by 979 · see citing works
The Genetic Landscape of Clinical Resistance to RAF Inhibition in Metastatic Melanoma
Allen, E. M. V., Wagle, N., Sucker, A., Treacy, D. J., Johannessen, C. M., Goetz, E. M., Place, C. S., Taylor-Weiner, A. N., Whittaker, S. R., Kryukov, G. V., et al. (2013) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0617 · Cited by 904 · see citing works
cowplot: Streamlined Plot Theme and Plot Annotations for 'ggplot2'
Wilke, C. O. (2015) · doi:10.32614/cran.package.cowplot · Cited by 874 · see citing works
WikiPathways: connecting communities
Martens, M., Ammar, A., Riutta, A., Waagmeester, A., Slenter, D., Hanspers, K., Miller, R. A., Digles, D., Lopes, É. N., Ehrhart, F., et al. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa1024 · Cited by 847 · see citing works
Boni, A., Cogdill, A. P., Dang, P., Udayakumar, D., Njauw, C.-N. J., Sloss, C. M., Ferrone, C. R., Flaherty, K. T., Lawrence, D. P., Fisher, D. E., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-0118 · Cited by 742 · see citing works
Ebert, P. J. R., Cheung, J., Yang, Y., McNamara, E., Hong, R., Moskalenko, M., Gould, S. E., Maecker, H., Irving, B. A., Kim, J. M., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.01.024 · Cited by 713 · see citing works
Keung, E. Z.-Y., & Gershenwald, J. E. (2018) · Expert Review of Anticancer Therapy · doi:10.1080/14737140.2018.1489246 · Cited by 616 · see citing works
Activation of human CD4+ cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype
Kemper, C., Chan, A. C., Green, J. M., Brett, K. A., MURPHY, K. M. M., & Atkinson, J. P. (2003) · Nature · doi:10.1038/nature01315 · Cited by 589 · see citing works
IL4I1 Is a Metabolic Immune Checkpoint that Activates the AHR and Promotes Tumor Progression
Sadik, A., Patterson, L. F. S., Öztürk, S., Mohapatra, S. R., Panitz, V., Secker, P. F., Pfänder, P., Loth, S., Salem, H., Prentzell, M. T., et al. (2020) · Cell · doi:10.1016/j.cell.2020.07.038 · Cited by 563 · see citing works
BRAF Inhibitor Resistance Mechanisms in Metastatic Melanoma: Spectrum and Clinical Impact
Rizos, H., Menzies, A. M., Pupo, G. M., Carlino, M. S., Fung, C., Hyman, J., Haydu, L. E., Mijatov, B., Becker, T. M., Boyd, S. C., et al. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-3122 · Cited by 543 · see citing works
Mechanism of alternative splicing and its regulation
Wang, Y., LIU, J., Huang, B., XU, Y.-M., LI, J., Huang, L., Jin, L., Zhang, J., Min, Q., Yang, W., et al. (2014) · Biomedical Reports · doi:10.3892/br.2014.407 · Cited by 478 · see citing works
Genetic Interaction Between NRAS and BRAF Mutations and PTEN/MMAC1 Inactivation in Melanoma
Tsao, H., Yang, G., Goel, V., Wu, H., & Haluska, F. G. (2004) · Journal of Investigative Dermatology · doi:10.1046/j.0022-202x.2004.22243.x · Cited by 462 · see citing works
Myeloid Cell-Derived Arginase in Cancer Immune Response
Grzywa, T. M., Sosnowska, A., Matryba, P., Rydzyńska, Z., Jasiński, M., Nowis, D., & Gołąb, J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00938 · Cited by 434 · see citing works
Du, J., Widlund, H. R., Horstmann, M. A., Ramaswamy, S., Ross, K. N., Huber, W. E., Nishimura, E. K., Golub, T. R., & Fisher, D. E. (2004) · Cancer Cell · doi:10.1016/j.ccr.2004.10.014 · Cited by 420 · see citing works
gridExtra: Miscellaneous Functions for "Grid" Graphics
Auguié, B. (2010) · doi:10.32614/cran.package.gridextra · Cited by 420 · see citing works
Examination of Mutations in BRAF, NRAS, and PTEN in Primary Cutaneous Melanoma
Goel, V., Lazar, A. J., Warneke, C. L., Redston, M. S., & Haluska, F. G. (2005) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700026 · Cited by 389 · see citing works
Liu, C., Peng, W., Xu, C., Lou, Y., Zhang, M., Wargo, J. A., Chen, J. Q., Li, H. S., Watowich, S. S., Yang, Y., et al. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-1626 · Cited by 379 · see citing works
Johnson, D. B., Menzies, A. M., Zimmer, L., Eroglu, Z., Ye, F., Zhao, S., Rizos, H., Sucker, A., Scolyer, R. A., Gutzmer, R., et al. (2015) · European Journal of Cancer · doi:10.1016/j.ejca.2015.08.022 · Cited by 324 · see citing works
Simpson‐Haidaris, P. J., & Rybarczyk, B. J. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb03525.x · Cited by 286 · see citing works
Cardone, J., Friec, G. L., Vantourout, P., Roberts, A., Fuchs, A. G., Jackson, I., Suddason, T., Lord, G. M., Atkinson, J. P., Cope, A. P., et al. (2010) · Nature Immunology · doi:10.1038/ni.1917 · Cited by 284 · see citing works
The TAK1–TRAF6 signalling pathway
Landström, M. (2010) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.12.023 · Cited by 280 · see citing works
Epigenetic Silencing of the PTEN Gene in Melanoma
Mirmohammadsadegh, A., Marini, A., Nambiar, S., Hassan, M., Tannapfel, A., Ruzicka, T., & Hengge, U. R. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0384 · Cited by 279 · see citing works
VEGF as a potential target in lung cancer
Frezzetti, D., Gallo, M., Maiello, M. R., D’Alessio, A., Esposito, C., Chicchinelli, N., Normanno, N., & Luca, A. D. (2017) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2017.1371137 · Cited by 237 · see citing works
European consensus-based interdisciplinary guideline for melanoma. Part 2: Treatment – Update 2019
Garbe, C., Amaral, T. M. S., Peris, K., Hauschild, A., Arenberger, P., Bastholt, L., Bataille, V. A., del Mármol, V., Dréno, B., Fargnoli, M. C., et al. (2019) · European Journal of Cancer · doi:10.1016/j.ejca.2019.11.015 · Cited by 215 · see citing works
SPG7 Is an Essential and Conserved Component of the Mitochondrial Permeability Transition Pore
Shanmughapriya, S., Rajan, S., Hoffman, N. E., Higgins, A. M., Tomar, D., Nemani, N., Hines, K. J., Smith, D. J., Eguchi, A., Vallem, S., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.08.009 · Cited by 209 · see citing works
Sade-Feldman, M., Kanterman, J., Klieger, Y., Ish-Shalom, E., Olga, M., Saragovi, A., Shtainberg, H., Lotem, M., & Baniyash, M. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-3104 · Cited by 201 · see citing works
MAP4K Family Kinases in Immunity and Inflammation
Chuang, H., Wang, X., & Tan, T. (2015) · Advances in immunology · doi:10.1016/bs.ai.2015.09.006 · Cited by 200 · see citing works
The Role of Complement in Tumor Growth
Pı́o, R., Corrales, L. P., & Lambris, J. D. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-5915-6_11 · Cited by 196 · see citing works
Desmosomes: new perpetrators in tumour suppression
Dusek, R. L., & Attardi, L. D. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3051 · Cited by 189 · see citing works
Mitochondrial ribosomes in cancer
Kim, H. J., Maiti, P., & Barrientos, A. (2017) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2017.04.004 · Cited by 184 · see citing works
Geller, A. E., & Yan, J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01074 · Cited by 174 · see citing works
Modulating splicing with small molecular inhibitors of the spliceosome
Effenberger, K. A., Urabe, V. K., & Jurica, M. S. (2016) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1381 · Cited by 161 · see citing works
Yadavilli, S., Mayo, L. D., Higgins, M., Laı́n, S., Hegde, V. K., & Deutsch, W. A. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.07.003 · Cited by 155 · see citing works
Role of the complement system in the tumor microenvironment
Zhang, R., Liu, Q., Li, T., Liao, Q., & Zhao, Y. (2019) · Cancer Cell International · doi:10.1186/s12935-019-1027-3 · Cited by 127 · see citing works
Huang, G., Li, H., & Zhang, H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228879 · Cited by 124 · see citing works
Ostrowski, S. M., & Fisher, D. E. (2020) · Hematology/Oncology Clinics of North America · doi:10.1016/j.hoc.2020.08.010 · Cited by 111 · see citing works
NKAP Is a Transcriptional Repressor of Notch Signaling and Is Required for T Cell Development
Pajerowski, A. G., Nguyen, C. T. T., Aghajanian, H. K., Shapiro, M. J., & Shapiro, V. S. (2009) · Immunity · doi:10.1016/j.immuni.2009.02.011 · Cited by 101 · see citing works
Sotgia, F., Fiorillo, M., & Lisanti, M. P. (2017) · Oncotarget · doi:10.18632/oncotarget.19612 · Cited by 94 · see citing works
Melanoma of unknown primary: New perspectives for an old story
Boussios, S., Rassy, E., Samartzis, E. P., Moschetta, M., Sheriff, M., Fidalgo, J. A. P., & Pavlidis, N. A. (2020) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2020.103208 · Cited by 79 · see citing works
Characteristics of pre-metastatic niche: the landscape of molecular and cellular pathways
Wang, H., Pan, J., Barsky, L., Jacob, J. C., Zheng, Y., Gao, C., Wang, S., Zhu, W., Sun, H., Lu, L., et al. (2021) · Molecular Biomedicine · doi:10.1186/s43556-020-00022-z · Cited by 77 · see citing works
Teh, J. L. F., Cheng, P. F., Purwin, T. J., Nikbakht, N., Patel, P. S., Chervoneva, I., Ertel, A., Fortina, P. M., Kleiber, I., HooKim, K., et al. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-17-0699 · Cited by 75 · see citing works
Babačić, H., Lehtiö, J., de Coaña, Y. P., Pernemalm, M., & Eriksson, H. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2019-000204 · Cited by 69 · see citing works
Identification of key candidate genes involved in melanoma metastasis
Chen, J., Wu, F., Shi, Y., Yang, D., Xu, M., Lai, Y., & Liu, Y. (2019) · Molecular Medicine Reports · doi:10.3892/mmr.2019.10314 · Cited by 68 · see citing works
Desai, B. M., Villanueva, J., Nguyen, T.-T. K., Lioni, M., Xiao, M., Kong, J., Krepler, C., Vultur, A., Flaherty, K. T., Nathanson, K. L., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059588 · Cited by 64 · see citing works
Network Signatures of Survival in Glioblastoma Multiforme
Patel, V. N., Gokulrangan, G., Chowdhury, S. A., Chen, Y., Sloan, A. E., Koyutürk, M., Barnholtz‐Sloan, J. S., & Chance, M. R. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003237 · Cited by 63 · see citing works
Genetic progression of malignant melanoma
Tı́már, J., Vízkeleti, L., Doma, V., Barbai, T., & Rásó, E. (2016) · Cancer and Metastasis Reviews · doi:10.1007/s10555-016-9613-5 · Cited by 62 · see citing works
TRAF6 regulates melanoma invasion and metastasis through ubiquitination of Basigin
Luo, Z., Zhang, X., Zeng, W., Su, J., Yang, K., Lu, L., Lim, C. B., Tang, W., Wu, L., Zhao, S., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.6886 · Cited by 58 · see citing works
Loss of desmoglein 2 promotes tumorigenic behavior in pancreatic cancer cells
Hütz, K., Zeiler, J., Sachs, L., Ormanns, S., & Spindler, V. (2017) · Molecular Carcinogenesis · doi:10.1002/mc.22644 · Cited by 56 · see citing works
The role of desmosomes in carcinogenesis
Zhou, G., Yang, L., Gray, A., Srivastava, A., Li, C., Zhang, G., & Cui, T. (2017) · OncoTargets and Therapy · doi:10.2147/ott.s136367 · Cited by 56 · see citing works
Pan-Cancer Mutational and Transcriptional Analysis of the Integrator Complex
Federico, A., Rienzo, M., Abbondanza, C., Costa, V., Ciccodicola, A., & Casamassimi, A. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18050936 · Cited by 55 · see citing works
Targeting the spliceosome machinery: A new therapeutic axis in cancer?
Eymin, B. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.114039 · Cited by 54 · see citing works
Desmoglein 2 promotes vasculogenic mimicry in melanoma and is associated with poor clinical outcome
Tan, L. Y., Mintoff, C. P., Johan, M. Z., Ebert, B. W., Fedele, C. G., Zhang, Y. F., Szeto, P., Sheppard, K. E., McArthur, G. A., Foster‐Smith, E., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.10216 · Cited by 51 · see citing works
Choi, J. W., Kim, Y. J., Yun, K. A., Won, C. H., Lee, M. W., Choi, J. H., Chang, S. E., & Lee, W. J. (2020) · Scientific Reports · doi:10.1038/s41598-020-71216-2 · Cited by 50 · see citing works
Functional characterization of a novel somatic oncogenic mutation of PIK3CB
Whale, A. D., Colman, L., Lensun, L., Rogers, H. L., & Shuttleworth, S. J. (2017) · Signal Transduction and Targeted Therapy · doi:10.1038/sigtrans.2017.63 · Cited by 45 · see citing works
The p52 isoform of SHC1 is a key driver of breast cancer initiation
Wright, K. D., Miller, B., El-Meanawy, S., Tsaih, S., Banerjee, A., Geurts, A. M., Sheinin, Y. M., Sun, Y., Kalyanaraman, B., Rui, H., et al. (2019) · Breast Cancer Research · doi:10.1186/s13058-019-1155-7 · Cited by 45 · see citing works
Abnormal alternative splicing promotes tumor resistance in targeted therapy and immunotherapy
Deng, K., Yao, J., Huang, J., Ding, Y., & Zuo, J. (2021) · Translational Oncology · doi:10.1016/j.tranon.2021.101077 · Cited by 44 · see citing works
Huang, R., Xing, Z., Luan, Z., Wu, T., Wu, X., & Hu, G. (2003) · PubMed · Cited by 42 · see citing works
Kuckleburg, C. J., & Newman, P. J. (2012) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.112.300474 · Cited by 39 · see citing works
Patterson, A. R., Endale, M., Lampe, K., Aksoylar, H., Flagg, A., Woodgett, J. R., Hildeman, D. A., Jordan, M. B., Singh, H., Kucuk, Z. Y., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-02897-7 · Cited by 39 · see citing works
Merlin Is a Negative Regulator of Human Melanoma Growth
Murray, L. B., Lau, Y.-K. I., & Yu, Q. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043295 · Cited by 38 · see citing works
Identification of potential crucial genes and key pathways in osteosarcoma
Liu, J., Wu, S., Xie, X., Wang, Z., & Lei, Q. (2020) · Hereditas · doi:10.1186/s41065-020-00142-0 · Cited by 35 · see citing works
Tang, N.-Y., Chueh, F., Yu, C.-C., Liao, C., Lin, J., Hsia, T., Wu, K., Liu, H., Lu, K.-W., & Chung, J. (2016) · Oncology Reports · doi:10.3892/or.2016.4577 · Cited by 33 · see citing works
Peitsch, W. K., Dörflinger, Y., Fischer‐Colbrie, R., Huck, V., Bauer, A. T., Utikal, J. S., Goerdt, S., & Schneider, S. W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089491 · Cited by 32 · see citing works
Adjuvant immunotherapy for melanoma
Thomas, D. C., & Bello, D. M. (2021) · Journal of Surgical Oncology · doi:10.1002/jso.26329 · Cited by 31 · see citing works
Desmoglein 1 Regulates Invadopodia by Suppressing EGFR/Erk Signaling in an Erbin-Dependent Manner
Valenzuela-Iglesias, A., Burks, H. E., Arnette, C. R., Yalamanchili, A., Nekrasova, O. E., Godsel, L. M., & Green, K. J. (2019) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-18-0048 · Cited by 28 · see citing works
Selimović, D., Sprenger, A., Hannig, M., Haïkel, Y., & Hassan, M. (2011) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2011.01304.x · Cited by 27 · see citing works
SVH‐B interacts directly with p53 and suppresses the transcriptional activity of p53
Zhou, X., Yang, G., Huang, R., Chen, X., & Hu, G. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.09.025 · Cited by 26 · see citing works
Downregulation of hemidesmosomal proteins in nasopharyngeal carcinoma cells
Lo, A. K. F., Yuen, P. W., Liu, Y., Wang, X. H., Cheung, A. L. M., Wong, Y. C., & Tsao, S. W. (2001) · Cancer Letters · doi:10.1016/s0304-3835(00)00683-2 · Cited by 24 · see citing works
Betancourt, L. H., Szasz, A. M., Kuras, M., Rodriguez Murillo, J., Sugihara, Y., Pla, I., Horvath, Z., Pawłowski, K., Rezeli, M., Miharada, K., et al. (2019) · Cancers · doi:10.3390/cancers11121981 · Cited by 24 · see citing works
Self-citationTruscott, S. M., Abate, G., Price, J. D., Kemper, C., Atkinson, J. P., & Hoft, D. F. (2010) · Infection and Immunity · doi:10.1128/iai.00513-10 · Cited by 22 · see citing works
Alessi, C., Scapulatempo‐Neto, C., Viana, C. R., & Vazquez, V. D. L. (2017) · Melanoma Research · doi:10.1097/cmr.0000000000000396 · Cited by 22 · see citing works
Lin, C., Lai, G., Chen, K., Lin, T.-H., Fan, J.-J., Hsu, R.-L., Chou, C., Lin, C., Kandaswami, C. C., Lee, M., et al. (2015) · Journal of Functional Foods · doi:10.1016/j.jff.2015.09.030 · Cited by 21 · see citing works
Significance and utility of reference values in occupational medicine
Apostoli, P., Minoia, C., & Hamilton, E. I. (1998) · The Science of The Total Environment · doi:10.1016/s0048-9697(97)00297-0 · Cited by 21 · see citing works
Fejza, A., Polano, M., Camicia, L., Poletto, E., Carobolante, G., Toffoli, G., Mongiat, M., & Andreuzzi, E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147511 · Cited by 19 · see citing works
Lee, S., Kim, J., Lee, J., Lee, J., Park, J., Han, T.-S., Cho, Y., Cho, Y., Bae, K., Park, Y.-J., et al. (2020) · Cell Death and Differentiation · doi:10.1038/s41418-020-00628-4 · Cited by 17 · see citing works
Regulation of RANKL‐induced osteoclastogenesis by RING finger protein RNF114
Lin, B., Qi, K., Leaman, D. W., Goel, V. K., & Agarwal, A. (2017) · Journal of Orthopaedic Research® · doi:10.1002/jor.23654 · Cited by 15 · see citing works
Patterson, A. R., Bolcas, P. E., Lampe, K., Cantrell, R., Ruff, B. P., Lewkowich, I. P., Hogan, S. P., Janssen, E. M., Bleesing, J., Hershey, G. K. K., et al. (2018) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2018.10.018 · Cited by 14 · see citing works
Velasquez, E., Szadai, L., Zhou, Q., Kim, Y., Pla, I., Sanchez, A., Appelqvist, R., Oskolas, H., Marko‐Varga, M., Lee, B., et al. (2021) · Clinical and Translational Medicine · doi:10.1002/ctm2.466 · Cited by 13 · see citing works
Self-citationHan, W., Wu, Y., Zhao, X., Gong, Z.-H., & Shen, G. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.715173 · Cited by 13 · see citing works
Computational challenges in biomarker discovery from high-throughput proteomic data
Čuklina, J. (2018) · Repository for Publications and Research Data (ETH Zurich) · doi:10.3929/ethz-b-000307772 · Cited by 11 · see citing works
Gimap5 Inhibits Lung Cancer Growth by Interacting With M6PR
Dai, P., Tang, Z., Ruan, P., Bajinka, O., Liu, D., & Tan, Y. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.699847 · Cited by 11 · see citing works
The oncogenic role of NKAP in the growth and invasion of colon cancer cells
Shu, W., Liu, G., Dai, Y., Feng, A., Chen, Z., Han, J., & Li, X. (2019) · Oncology Reports · doi:10.3892/or.2019.7322 · Cited by 8 · see citing works
Liu, J., Zhang, M.-Y., Kan, Y., Wang, W., Liu, J., Gong, J.-H., & Yang, J.-G. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.622793 · Cited by 5 · see citing works
de Melo, F. H. M., Gonçalves, D. A., de Sousa, R. X., Icimoto, M. Y., Fernandes, D. C., Laurindo, F. R. M., & Jasiulionis, M. G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179556 · Cited by 5 · see citing works
Alatrash, G., Vence, L. M., Woodward, W. A., Ueno, N. T., & Molldrem, J. J. (2008) · Blood · doi:10.1182/blood.v112.11.5440.5440 · Cited by 1 · see citing works
Flagged first, then by citations
1 of the 105 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- [82]PELO Pelota MRNA Surveillance and Ribosome Rescue Factor [Homo Sapiens (Human)]—Gene—NCBI Available online: https://www.ncbi.nlm.nih.gov/gene/53918 (accessed on 24 November 2021)
Cited by
Sorted by citations
Monette, A., Aguilar‐Mahecha, A., Altınmakas, E., Angelos, M. G., Assad, N., Batist, G., Bommareddy, P. K., Bonilla, D. L., Borchers, C. H., Church, S., et al. (2024) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-24-2469 · Cited by 14 · see citing works
Guedes, J., Woldmar, N., Szasz, A. M., Wieslander, E., Pawłowski, K., Horvatovich, P., Malm, J., Szadai, L., Németh, I. B., Marko-Varga, G., et al. (2025) · Journal of Proteomics · doi:10.1016/j.jprot.2025.105493 · Cited by 11 · see citing works
Self-citationMolecular Classifiers in Skin Cancers: Challenges and Promises
Azimi, A., & Fernández‐Peñas, P. (2023) · Cancers · doi:10.3390/cancers15184463 · Cited by 10 · see citing works
Predicting immune checkpoint therapy response in three independent metastatic melanoma cohorts
Szadai, L., Bartha, Á., Plá, I., Lakatos, A. I. T., Pal, D., Lengyel, A., de Almeida, N. P., Jánosi, Á. J., Nogueira, F. C. S., Szeitz, B., et al. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1428182 · Cited by 8 · see citing works
Self-citationGuedes, J. D. S., Szadai, L., Woldmar, N., Jánosi, Á. J., Koroncziová, K., Lengyel, B. M., Kelemen, B., Boltas, E., Gyulai, R., Wieslander, E., et al. (2025) · Journal of Proteomics · doi:10.1016/j.jprot.2025.105482 · Cited by 9 · see citing works
Self-citationComprehensive biobanking strategy with clinical impact at the European Cancer Moonshot Lund Center
Oskolás, H., Nogueira, F. C. S., Domont, G. B., Yu, K., Semenov, Y. R., Sorger, P. K., Steinfelder, E., Corps, L., Schulz, L., Wieslander, E., et al. (2025) · Journal of Proteomics · doi:10.1016/j.jprot.2025.105442 · Cited by 5 · see citing works
Self-citationBartha, Á., Weltz, B., Betancourt, L. H., Gil, J., de Almeida, N. P., Bianchini, G., Szeitz, B., Szadai, L., Plá, I., Kemény, L. V., et al. (2025) · Journal of Proteome Research · doi:10.1021/acs.jproteome.4c00749 · Cited by 5 · see citing works
Self-citationProteomics-Enhanced AI-Digital Pathology in Metastatic Mucinous Colorectal Carcinoma: A Case ReportPreprint
Fülöp, L., Szigeti, B., Guedes, J. S., Woldmar, N., Oskolás, H., Marko-Varga, M., Appelqvist, R., Wieslander, E., Pawlowski, K., Szadai, L., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.02.709044 · Cited by 3 · see citing works
Self-citationSuman, S., Geng, L., Nevala, W. K., Moore, R. M., Atherton, C. L., Zhao, X., Sung, J., Guo, R., Jakub, J. W., Kandasamy, R. K., et al. (2025) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2025.101472 · Cited by 2 · see citing works
Li, T., Qin, X., Wang, L., Qin, C., Zhao, B., Cao, H., Yang, X., Wang, Y., Li, Z., Zhou, X., et al. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e20464 · Cited by 2 · see citing works
Fernández-Coto, D. L., Ayala, M., Alonso-Bastida, R., Palmqvist, A., García, M. F., Balderas-López, S. F., Oskolás, H., Christersson, L., Fülöp, L., Szigeti, B., et al. (2026) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2026.101620 · Cited by 2 · see citing works
Self-citationMetastatic Progression of Human Melanoma
Tı́már, J., & Ladányi, A. (2023) · Cancers · doi:10.3390/cancers15041225 · Cited by 1 · see citing works
The influence of molecular biology in the dermatopathology
Németh, I. B., Szadai, L., Jánosi, Á. J., Újfaludi, Z., Pankotai, T., Marko‐Varga, G., Kemény, L. V., & Varga, E. (2022) · Bőrgyógyászati és Venerológiai Szemle · doi:10.7188/bvsz.2022.98.3.7
Self-citationBata‐Csörgõ, Z., Groma, G., Manczinger, M., Nagy, N., Szabó, K., & Széll, M. (2023) · Bőrgyógyászati és Venerológiai Szemle · doi:10.7188/bvsz.2023.99.2.1
ARMC10 Drives Glioblastoma Progression Through Activating Notch Pathway
Feng, B., Gao, T., Chen, L., & Xing, Y. (2025) · Molecular Carcinogenesis · doi:10.1002/mc.23895
Fusco, F., Weigel, J., Schliemann, M., Schneider, A., Zhou, Y., Persa, O., Posch, C., Krackhardt, A. M., Förg, S., Schott, C., et al. (2026) · Modern Pathology · doi:10.1016/j.modpat.2026.100995
Guedes, J., Woldmar, N., Baltás, E., Kriston, A., Migh, E., Kovács, F., Oskolás, H., Marko-Varga, M., Appelqvist, R., Wieslander, E., et al. (2026) · npj Precision Oncology · doi:10.1038/s41698-026-01569-w · Cited by 1 · see citing works
Self-citationSpatial Proteomics as a Potential Decision‐Support Layer for Early Melanoma: A Narrative Review
Szadai, L., Gil, J., & Marko‐Varga, G. (2026) · International Journal of Dermatology · doi:10.1111/ijd.70665
Self-citation
- Authors
- Szadai, L., Velasquez, E., Szeitz, B., Almeida, N. P. D., Domont, G., Betancourt, L. H., Gil, J., Marko-Varga, M., Oskolas, H., Jánosi, Á. J., Boyano-Adánez, M. D. C., Kemény, L., Baldetorp, B., Malm, J., Horvatovich, P., Szász, A. M., Németh, I. B., & Marko-Varga, G.
- Affiliations
- Department of Dermatology and Allergology, University of Szeged, 6720 Szeged, Hungary
- Section for Clinical Chemistry, Department of Translational Medicine, Lund University, Skåne University Hospital Malmö, 205 02 Malmö, Sweden
- Semmelweis University (HU)
- Universidade Federal do Rio de Janeiro (BR)
- Lund University (SE)
- Division of Oncology, Department of Clinical Sciences Lund, Lund University, 221 85 Lund, Sweden
- University of Szeged (HU)
- Department of Systems Biology, Faculty of Medicine and Health Sciences, University of Alcala de Henares, 28801 Alcalá de Henares, Madrid, Spain
- University of Groningen (NL)
- Clinical Protein Science & Imaging, Biomedical Centre, Department of Biomedical Engineering, Lund University, BMC D13, 221 84 Lund, Sweden
- ORCID
- Venue
- Cancers
- Publisher
- MDPI AG
- Published
- 2021-12-03
- Volume
- 13
- Issue
- 23
- Pages
- 6105
- ISSN
- 2072-6694 (ISSN-L)
- PMC
- PMC8657028
- OpenAlex
- W4200329644
- Cited by
- 18
- References
- 105
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 2 · 2023: 4 · 2022: 1
- FWCI
- 0.64
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cancers (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Lund University Publications (Lund University) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Funders
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Lunds Universitet
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro
- Universidade Federal do Rio de Janeiro
- Innovációs és Technológiai Minisztérium
- Cancer Moonshot
- Topics
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Health Sciences › Medicine › Oncology › Cutaneous Melanoma Detection and Management
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Melanoma and MAPK Pathways
- Keywords
- melanoma, protein biomarkers, prognostic factors, predictive biomarkers, formalin-fixed paraffin-embedded tissue, survival, TRAF6, RNA splicing, immune cell activity, extracellular matrix, metabolic pathways, immunotherapy response, targeted therapy response, precision medicine, metastasis, clinical stage
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