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Combinatorial Chemistry & High Throughput Screening

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ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

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Research Article

Identification of a 15 DNA Damage Repair-Related Gene Signature as a Prognostic Predictor for Lung Adenocarcinoma

Author(s): Linping Gu, Yuanyuan Xu and Hong Jian*

Volume 25, Issue 9, 2022

Published on: 11 January, 2022

Page: [1437 - 1449] Pages: 13

DOI: 10.2174/1386207324666210716104714

Price: $65

Abstract

Background: Lung adenocarcinoma (LUAD) is a common malignancy with a poor prognosis due to the lack of predictive markers. DNA damage repair (DDR)-related genes are closely related to cancer progression and treatment.

Introduction: To identify a reliable DDR-related gene signature as an independent predictor of LUAD.

Methods: DDR-related genes were obtained using combined analysis of TCGA-LUAD data and literature information, followed by the identification of DDR-related prognostic genes. The DDRrelated molecular subtypes were then screened, followed by Kaplan-Meier analysis, feature gene identification, and pathway enrichment analysis of each subtype. Moreover, Cox and LASSO regression analyses were performed for the feature genes of each subtype to construct a prognostic model. The clinical utility of the prognostic model was confirmed using the validation dataset GSE72094 and nomogram analysis.

Results: Eight DDR-related prognostic genes were identified from 31 DDR-related genes. Using consensus cluster analysis, three molecular subtypes were screened. Cluster2 had the best prognosis, while cluster3 had the worst. Compared to cluster2, clusters 1 and 3 consisted of more stage3 - 4, T2-T4, male, and older samples. The feature genes of clusters1, 2, and 3 were mainly enriched in the cell cycle, arachidonic acid metabolism, and ribosomes. Furthermore, a 15-feature gene signature was identified for improving the prognosis of LUAD patients.

Conclusion: The 15 DDR-related feature gene signature is an independent and powerful prognostic biomarker for LUAD that may improve risk classification and provide supplementary information for a more accurate evaluation and personalized treatment.

Keywords: Adenocarcinoma of lung, DNA repair, prognosis, transcriptome, DDR-related gene, malignancy.

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[1]
Raderschall, E.; Stout, K.; Freier, S.; Suckow, V.; Schweiger, S.; Haaf, T. Elevated levels of rad51 recombination protein in tumor cells. Cancer Res., 2002, 62(1), 219-225.
[PMID: 11782381]
[2]
Henley, S.J.; Ward, E.M.; Scott, S.; Ma, J.; Anderson, R.N.; Firth, A.U.; Thomas, C.C.; Islami, F.; Weir, H.K.; Lewis, D.R.; Sherman, R.L.; Wu, M.; Benard, V.B.; Richardson, L.C.; Jemal, A.; Cronin, K.; Kohler, B.A. Annual report to the nation on the status of cancer, part I: National cancer statistics. Cancer, 2020, 126(10), 2225-2249.
[http://dx.doi.org/10.1002/cncr.32802] [PMID: 32162336]
[3]
Chang, J.T.H.; Lee, Y.M.; Huang, R.S. The impact of the cancer genome atlas on lung cancer. Transl. Res., 2015, 166(6), 568-585.
[http://dx.doi.org/10.1016/j.trsl.2015.08.001] [PMID: 26318634]
[4]
Torre, L.A.; Siegel, R.L.; Jemal, A. Lung Cancer Statistics. Adv. Exp. Med. Biol., 2016, 893, 1-19.
[http://dx.doi.org/10.1007/978-3-319-24223-1_1] [PMID: 26667336]
[5]
Lv, Z.; Lei, T. Systematical identifications of prognostic meaningful lung adenocarcinoma subtypes and the underlying mutational and expressional characters. BMC Cancer, 2020, 20(1), 56.
[http://dx.doi.org/10.1186/s12885-019-6462-y] [PMID: 31987030]
[6]
Schmidt-Hansen, M.; Berendse, S.; Hamilton, W.; Baldwin, D.R. Lung cancer in symptomatic patients presenting in primary care: A systematic review of risk prediction tools. Br. J. Gen. Pract., 2017, 67(659), e396-e404.
[http://dx.doi.org/10.3399/bjgp17X690917] [PMID: 28483820]
[7]
Herbst, R.S.; Morgensztern, D.; Boshoff, C. The biology and management of non-small cell lung cancer. Nature, 2018, 553(7689), 446-454.
[http://dx.doi.org/10.1038/nature25183] [PMID: 29364287]
[8]
Gavande, N.S.; VanderVere-Carozza, P.S.; Hinshaw, H.D.; Jalal, S.I.; Sears, C.R.; Pawelczak, K.S.; Turchi, J.J. DNA repair targeted therapy: The past or future of cancer treatment? Pharmacol. Ther., 2016, 160, 65-83.
[http://dx.doi.org/10.1016/j.pharmthera.2016.02.003] [PMID: 26896565]
[9]
Stingele, J.; Bellelli, R.; Boulton, S.J. Mechanisms of DNA-protein crosslink repair. Nat. Rev. Mol. Cell Biol., 2017, 18(9), 563-573.
[http://dx.doi.org/10.1038/nrm.2017.56] [PMID: 28655905]
[10]
Turgeon, M-O.; Perry, N.J.S.; Poulogiannis, G. DNA damage, repair, and cancer metabolism. Front. Oncol., 2018, 8(15), 15.
[http://dx.doi.org/10.3389/fonc.2018.00015] [PMID: 29459886]
[11]
Parikh, A.R.; He, Y.; Hong, T.S.; Corcoran, R.B.; Clark, J.W.; Ryan, D.P.; Zou, L.; Ting, D.T.; Catenacci, D.V.; Chao, J.; Fakih, M.; Klempner, S.J.; Ross, J.S.; Frampton, G.M.; Miller, V.A.; Ali, S.M.; Schrock, A.B. Analysis of dna damage response gene alterations and tumor mutational burden across 17,486 tubular gastrointestinal carcinomas: Implications for therapy. Oncologist, 2019, 24(10), 1340-1347.
[http://dx.doi.org/10.1634/theoncologist.2019-0034] [PMID: 31040255]
[12]
Vidotto, T.; Nersesian, S.; Graham, C.; Siemens, D.R.; Koti, M. DNA damage repair gene mutations and their association with tumor immune regulatory gene expression in muscle invasive bladder cancer subtypes. J. Immunother. Cancer, 2019, 7(1), 148.
[http://dx.doi.org/10.1186/s40425-019-0619-8] [PMID: 31174611]
[13]
Knijnenburg, T.A.; Wang, L.; Zimmermann, M.T.; Chambwe, N.; Gao, G.F.; Cherniack, A.D.; Fan, H.; Shen, H.; Way, G.P.; Greene, C.S.; Liu, Y.; Akbani, R.; Feng, B.; Donehower, L.A.; Miller, C.; Shen, Y.; Karimi, M.; Chen, H.; Kim, P.; Jia, P.; Shinbrot, E.; Zhang, S.; Liu, J.; Hu, H.; Bailey, M.H.; Yau, C.; Wolf, D.; Zhao, Z.; Weinstein, J.N.; Li, L.; Ding, L.; Mills, G.B.; Laird, P.W.; Wheeler, D.A.; Shmulevich, I.; Monnat, R.J., Jr; Xiao, Y.; Wang, C. Genomic and molecular landscape of DNA damage repair deficiency across the cancer genome atlas. Cell Rep., 2018, 23(1), 239-254.e6.
[http://dx.doi.org/10.1016/j.celrep.2018.03.076] [PMID: 29617664]
[14]
Lin, J.; Shi, J.; Guo, H.; Yang, X.; Jiang, Y.; Long, J.; Bai, Y.; Wang, D.; Yang, X.; Wan, X.; Zhang, L.; Pan, J.; Hu, K.; Guan, M.; Huo, L.; Sang, X.; Wang, K.; Zhao, H. Alterations in DNA damage repair genes in primary liver cancer. Clin. Cancer Res., 2019, 25(15), 4701-4711.
[15]
Goldman, M.J.; Craft, B.; Hastie, M. Repečka, K.; McDade, F.; Kamath, A.; Banerjee, A.; Luo, Y.; Rogers, D.; Brooks, A.N.; Zhu, J.; Haussler, D. Visualizing and interpreting cancer genomics data fpage the Xena platform. Nat. Biotechnol., 2020, 38(6), 675-678.
[http://dx.doi.org/10.1038/s41587-020-0546-8] [PMID: 32444850]
[16]
Barrett, T.; Wilhite, S.E.; Ledoux, P.; Evangelista, C.; Kim, I.F.; Tomashevsky, M.; Marshall, K.A.; Phillippy, K.H.; Sherman, P.M.; Holko, M.; Yefanov, A.; Lee, H.; Zhang, N.; Robertson, C.L.; Serova, N.; Davis, S.; Soboleva, A. NCBI GEO: Archive for functional genomics data sets--update. Nucleic Acids Res., 2013, 41(Database issue), D991-D995.
[PMID: 23193258]
[17]
Wilkerson, M.D.; Hayes, D.N. ConsensusClusterPlus: A class discovery tool with confidence assessments and item tracking. Bioinformatics, 2010, 26(12), 1572-1573.
[http://dx.doi.org/10.1093/bioinformatics/btq170] [PMID: 20427518]
[18]
Hänzelmann, S.; Castelo, R.; Guinney, J. GSVA: Gene set variation analysis for microarray and RNA-seq data. BMC Bioinformatics, 2013, 14, 7.
[http://dx.doi.org/10.1186/1471-2105-14-7] [PMID: 23323831]
[19]
Liberzon, A.; Subramanian, A.; Pinchback, R.; Thorvaldsdóttir, H.; Tamayo, P.; Mesirov, J.P. Molecular signatures database (MSigDB) 3.0. Bioinformatics, 2011, 27(12), 1739-1740.
[http://dx.doi.org/10.1093/bioinformatics/btr260] [PMID: 21546393]
[20]
Smyth, G.K. limma: Linear Models for Microarray Data.Bioinformatics and Computational Biology Solutions Using R and Bioconductor; Springer New York.: New York, NY., 2005, pp. 397-420.
[21]
Chen, F.; Zhang, Y.; Parra, E.; Rodriguez, J.; Behrens, C.; Akbani, R.; Lu, Y.; Kurie, J.M.; Gibbons, D.L.; Mills, G.B.; Wistuba, I.I.; Creighton, C.J. Multiplatform-based molecular subtypes of non-small-cell lung cancer. Oncogene, 2017, 36(10), 1384-1393.
[http://dx.doi.org/10.1038/onc.2016.303] [PMID: 27775076]
[22]
Jiao, X.; Sherman, B.T.; Huang, W.; Stephens, R.; Baseler, M.W.; Lane, H.C.; Lempicki, R.A. DAVID-WS: a stateful web service to facilitate gene/protein list analysis. Bioinformatics, 2012, 28(13), 1805-1806.
[http://dx.doi.org/10.1093/bioinformatics/bts251] [PMID: 22543366]
[23]
Nagathihalli, N.S.; Nagaraju, G. RAD51 as a potential biomarker and therapeutic target for pancreatic cancer. Biochim. Biophys. Acta, 2011, 1816(2), 209-218.
[PMID: 21807066]
[24]
Chen, Q.; Cai, D.; Li, M.; Wu, X. The homologous recombination protein RAD51 is a promising therapeutic target for cervical carcinoma. Oncol. Rep., 2017, 38(2), 767-774.
[http://dx.doi.org/10.3892/or.2017.5724] [PMID: 28627709]
[25]
Graeser, M.; Mccarthy, A.; Lord, C.J.; Savage, K.; Hills, M.; Salter, J.; Orr, N.; Parton, M.; Smith, I.E.; Reis-Filho, J.S.; Dowsett, M.; Ashworth, A. Turner. N.C. A marker of homologous recombination predicts pathologic complete response to neoadjuvant chemotherapy in primary breast cancer. Clin. Cancer Res., 2010, 16(24), 6159-6168.
[http://dx.doi.org/10.1158/1078-0432.CCR-10-1027] [PMID: 20802015]
[26]
Lee, J.H.; Bae, A.N.; Jung, A.S. Clinicopathological and prognostic characteristics of RAD51 in colorectal cancer. Medicina (Kaunas), 2020, 56(2), E48.
[http://dx.doi.org/10.3390/medicina56020048] [PMID: 31973027]
[27]
Mersch, J.; Jackson, M.A.; Park, M.; Nebgen, D.; Peterson, S.K.; Singletary, C.; Arun, B.K.; Litton, J.K. Cancers associated with BRCA1 and BRCA2 mutations other than breast and ovarian. Cancer, 2015, 121(2), 269-275.
[http://dx.doi.org/10.1002/cncr.29041] [PMID: 25224030]
[28]
Marzio, A.; Puccini, J.; Kwon, Y.; Maverakis, N.K.; Arbini, A.; Sung, P.; Bar-Sagi, D.; Pagano, M. The F-Box domain-dependent activity of emi1 regulates parpi sensitivity in triple-negative breast cancers. Mol. Cell, 2019, 73(2), 224-237.e6.
[http://dx.doi.org/10.1016/j.molcel.2018.11.003] [PMID: 30554948]
[29]
Patel, D.S.; Misenko, S.M.; Her, J.; Bunting, S.F. BLM helicase regulates DNA repair by counteracting RAD51 loading at DNA double-strand break sites. J. Cell Biol., 2017, 216(11), 3521-3534.
[http://dx.doi.org/10.1083/jcb.201703144] [PMID: 28912125]
[30]
Kluźniak, W.; Wokołorczyk, D.; Rusak, B.; Huzarski, T.; Kashyap, A.; Stempa, K.; Rudnicka, H.; Jakubowska, A.; Szwiec, M.; Morawska, S.; Gliniewicz, K.; Mordak, K.; Stawicka, M.; Jarkiewicz-Tretyn, J.; Cechowska, M.; Domagała, P.; Dębniak, T.; Lener, M.; Gronwald, J.; Lubiński, J.; Narod, S.A.; Akbari, M.R.; Cybulski, C. Inherited variants in BLM and the risk and clinical characteristics of breast cancer. Cancers (Basel), 2019, 11(10), 1548.
[http://dx.doi.org/10.3390/cancers11101548] [PMID: 31614901]
[31]
Xie, J.; Peng, M.; Guillemette, S.; Quan, S.; Maniatis, S.; Wu, Y.; Venkatesh, A.; Shaffer, S.A.; Brosh, R.M., Jr; Cantor, S.B. FANCJ/BACH1 acetylation at lysine 1249 regulates the DNA damage response. PLoS Genet., 2012, 8(7), e1002786.
[http://dx.doi.org/10.1371/journal.pgen.1002786] [PMID: 22792074]
[32]
Cantor, S.B.; Guillemette, S. Hereditary breast cancer and the BRCA1-associated FANCJ/BACH1/BRIP1. Future Oncol., 2011, 7(2), 253-261.
[http://dx.doi.org/10.2217/fon.10.191] [PMID: 21345144]
[33]
Che, R.; Zhang, J.; Nepal, M.; Han, B.; Fei, P. Multifaceted fanconi anemia signaling. Trends Genet., 2018, 34(3), 171-183.
[http://dx.doi.org/10.1016/j.tig.2017.11.006] [PMID: 29254745]
[34]
AACR Project GENIE. Powering precision medicine through an international consortium. Cancer Discov., 2017, 7(8), 818-831.
[http://dx.doi.org/10.1158/2159-8290.CD-17-0151] [PMID: 28572459]
[35]
UyBico. S.J.; Wu, C.C.; Suh, R.D.; Le, N.H.; Brown, K.; Krishnam, M.S. Lung cancer staging essentials: The new TNM staging system and potential imaging pitfalls. Radiographics, 2010, 30(5), 1163-1181.
[http://dx.doi.org/10.1148/rg.305095166] [PMID: 20833843]
[36]
Wang, H.; Liu, J.; Xia, G.; Lei, S.; Huang, X.; Huang, X. Survival of pancreatic cancer patients is negatively correlated with age at diagnosis: A population-based retrospective study. Sci. Rep., 2020, 10(1), 7048.
[http://dx.doi.org/10.1038/s41598-020-64068-3] [PMID: 32341400]
[37]
Huang, S.; Chong, N.; Lewis, N.E.; Jia, W.; Xie, G.; Garmire, L.X. Novel personalized pathway-based metabolomics models reveal key metabolic pathways for breast cancer diagnosis. Genome Med., 2016, 8(1), 34-34.
[http://dx.doi.org/10.1186/s13073-016-0289-9] [PMID: 27036109]
[38]
Gao, P.; Yang, C.; Nesvick, C.L.; Feldman, M.J.; Sizdahkhani, S.; Liu, H.; Chu, H.; Yang, F.; Tang, L.; Tian, J.; Zhao, S.; Li, G.; Heiss, J.D.; Liu, Y.; Zhuang, Z.; Xu, G. Hypotaurine evokes a malignant phenotype in glioma through aberrant hypoxic signaling. Oncotarget, 2016, 7(12), 15200-15214.
[http://dx.doi.org/10.18632/oncotarget.7710] [PMID: 26934654]
[39]
Liu, J.; Mei, J.; Li, S.; Wu, Z.; Zhang, Y. Establishment of a novel cell cycle-related prognostic signature predicting prognosis in patients with endometrial cancer. Cancer Cell Int., 2020, 20(1), 329.
[http://dx.doi.org/10.1186/s12935-020-01428-z] [PMID: 32699528]
[40]
Gong, Q.; Zhang, H.H.; Sun, S.B.; Ge, W.M.; Li, Y.; Zhu, Y.C.; Li, L.P. Mismatch repair-deficient status associates with favorable prognosis of eastern chinese population with sporadic colorectal cancer. Oncol. Lett., 2018, 15(5), 7007-7013.
[http://dx.doi.org/10.3892/ol.2018.8192] [PMID: 29725427]
[41]
Zhao, P.; Li, L.; Jiang, X.; Li, Q. Mismatch repair deficiency/microsatellite instability-high as a predictor for anti-PD-1/PD-L1 immunotherapy efficacy. J. Hematol. Oncol., 2019, 12(1), 54.
[http://dx.doi.org/10.1186/s13045-019-0738-1] [PMID: 31151482]
[42]
Singhal, S.; Vachani, A.; Antin-Ozerkis, D.; Kaiser, L.R.; Albelda, S.M. Prognostic implications of cell cycle, apoptosis, and angiogenesis biomarkers in non-small cell lung cancer: A review. Clin. Cancer Res., 2005, 11(11), 3974-3986.
[http://dx.doi.org/10.1158/1078-0432.CCR-04-2661] [PMID: 15930332]
[43]
Monjazeb, A.M.; High, K.P.; Connoy, A.; Hart, L.S.; Koumenis, C.; Chilton, F.H. Arachidonic acid-induced gene expression in colon cancer cells. Carcinogenesis, 2006, 27(10), 1950-1960.
[http://dx.doi.org/10.1093/carcin/bgl023] [PMID: 16704987]
[44]
Bastide, A.; David, A. The ribosome, (slow) beating heart of cancer (stem) cell. Oncogenesis, 2018, 7(4), 34.
[http://dx.doi.org/10.1038/s41389-018-0044-8] [PMID: 29674660]
[45]
Zeng, S.; Yu, X.; Ma, C.; Song, R.; Zhang, Z.; Zi, X.; Chen, X.; Wang, Y.; Yu, Y.; Zhao, J.; Wei, R.; Sun, Y.; Xu, C. Transcriptome sequencing identifies ANLN as a promising prognostic biomarker in bladder urothelial carcinoma. Sci. Rep., 2017, 7(1), 3151.
[http://dx.doi.org/10.1038/s41598-017-02990-9] [PMID: 28600503]
[46]
Tsoi, H.; Wong, K-F.; Luk, J.M.; Staunton, D. Clinical utility of CDH17 biomarker in tumor tissues and liquid biopsies for detection and prognostic staging of colorectal cancer (CRC). J. Glob. Oncol., 2019, 5(Suppl.), 53-53.
[http://dx.doi.org/10.1200/JGO.2019.5.suppl.53]
[47]
Wang, J.; Che, W.; Wang, W.; Su, G.; Zhen, T.; Jiang, Z. CDKN3 promotes tumor progression and confers cisplatin resistance fpage RAD51 in esophageal cancer. Cancer Manag. Res., 2019, 11, 3253-3264.
[http://dx.doi.org/10.2147/CMAR.S193793] [PMID: 31114363]
[48]
Zheng, Y-W.; Li, Z-H.; Lei, L.; Liu, C.C.; Wang, Z.; Fei, L.R.; Yang, M.Q.; Huang, W.J.; Xu, H.T. FAM83A promotes lung cancer progression by regulating the wnt and hippo signaling pathways and indicates poor prognosis. Front. Oncol., 2020, 10(180), 180.
[http://dx.doi.org/10.3389/fonc.2020.00180] [PMID: 32195172]
[49]
Aasen, T.; Sansano, I.; Montero, M.Á.; Romagosa, C.; Temprana-Salvador, J.; Martínez-Marti, A.; Moliné, T.; Hernández-Losa, J.; Ramón y Cajal, S. Insight into the role and regulation of gap junction genes in lung cancer and identification of nuclear Cx43 as a putative biomarker of poor prognosis. Cancers (Basel), 2019, 11(3), E320.
[http://dx.doi.org/10.3390/cancers11030320] [PMID: 30845770]
[50]
Uhlen, M.; Zhang, C.; Lee, S.; Sjöstedt, E.; Fagerberg, L.; Bidkhori, G.; Benfeitas, R.; Arif, M.; Liu, Z.; Edfors, F.; Sanli, K.; von Feilitzen, K.; Oksvold, P.; Lundberg, E.; Hober, S.; Nilsson, P.; Mattsson, J.; Schwenk, J.M.; Brunnström, H.; Glimelius, B.; Sjöblom, T.; Edqvist, P.H.; Djureinovic, D.; Micke, P.; Lindskog, C.; Mardinoglu, A.; Ponten, F. A pathology atlas of the human cancer transcriptome. Science, 2017, 357(6352), eaan2507.
[http://dx.doi.org/10.1126/science.aan2507] [PMID: 28818916]
[51]
Ferreira-Halder, C.V.; Clerici, S.P.; Sousa Faria, A.V.; De Souza Oliveira, P.F.; Cordeiro, H.G.; Akagi, E. Protein tyrosine phosphatases in tumor progression and metastasis: Promoter or protection? In: Tumor Progression and Metastasis, 2020. Available from: https://www.intechopen.com/chapters/67964DOI
[http://dx.doi.org/10.5772/intechopen.87963]
[52]
Ye, W.; Chen, C.; Gao, Y.; Zheng, Z.S.; Xu, Y.; Yun, M.; Weng, H.W.; Xie, D.; Ye, S.; Zhang, J.X. Overexpression of SLC34A2 is an independent prognostic indicator in bladder cancer and its depletion suppresses tumor growth fpage decreasing c-Myc expression and transcriptional activity. Cell Death Dis., 2017, 8(2), e2581-e2581.
[http://dx.doi.org/10.1038/cddis.2017.13] [PMID: 28151475]
[53]
Burdelski, C.; Strauss, C.; Tsourlakis, M.C.; Kluth, M.; Hube-Magg, C.; Melling, N.; Lebok, P.; Minner, S.; Koop, C.; Graefen, M.; Heinzer, H.; Wittmer, C.; Krech, T.; Sauter, G.; Wilczak, W.; Simon, R.; Schlomm, T.; Steurer, S. Overexpression of thymidylate synthase (TYMS) is associated with aggressive tumor features and early PSA recurrence in prostate cancer. Oncotarget, 2015, 6(10), 8377-8387.
[http://dx.doi.org/10.18632/oncotarget.3107] [PMID: 25762627]
[54]
Kim, H.L.; Halabi, S.; Li, P.; Mayhew, G.; Simko, J.; Nixon, A.B.; Small, E.J.; Rini, B.; Morris, M.J.; Taplin, M.E.; George, D. A Molecular model for predicting overall survival in patients with metastatic clear cell renal carcinoma: Results from calgb 90206 (Alliance). EBioMedicine, 2015, 2(11), 1814-1820.
[http://dx.doi.org/10.1016/j.ebiom.2015.09.012] [PMID: 26870806]
[55]
Yao, H.; Lv, Y.; Bai, X.; Yu, Z.; Liu, X. Prognostic value of CXCL17 and CXCR8 expression in patients with colon cancer. Oncol. Lett., 2020, 20(3), 2711-2720.
[http://dx.doi.org/10.3892/ol.2020.11819] [PMID: 32782587]
[56]
Larsson, C.; Ehinger, A.; Winslow, S.; Leandersson, K.; Klintman, M.; Dahl, L.; Vallon-Christersson, J.; Häkkinen, J.; Hegardt, C.; Manjer, J.; Saal, L.; Rydén, L.; Malmberg, M.; Borg, Å.; Loman, N. Prognostic implications of the expression levels of different immunoglobulin heavy chain-encoding RNAs in early breast cancer. NPJ Breast Cancer, 2020, 6(1), 28.
[http://dx.doi.org/10.1038/s41523-020-0170-2] [PMID: 32656317]

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