Identification of Novel Diagnostic Biomarkers in Triple-Negative Breast Cancer Through Analysis of Polymorphic SNPs and APA Events SNP and APA Biomarkers in Triple-Negative Breast Cancer
Abstract
Background: As a subtype of breast cancer, triple-negative breast cancer (TNBC) exhibits unique pathological phenotypes and severe morbidity trends. New evidence suggests that aberrant alternative polyadenylation (APA) events can be regulated by single nucleotide polymorphisms (SNPs) and are associated with breast cancer. The study aimed to identify the APA-associated susceptibility SNP in TNBC, which may be useful in screening and treatment.
Methods: The RNA sequencing data is from 285 tumor tissues and 66 normal tissues of TNBC patients, accessed from the NCBI dataset FUSCCTNBC (Accession: PRJNA486023). We analyzed gene expression levels, APA events, and APA-associated SNPs, and explored their relationships and influences on TNBC.
Results: Our study revealed significant differences in both gene expression and APA events between tumor and normal tissues of TNBC patients. The differentially expressed genes are enriched in protein transcription, folding, localization, and targeting. apaQTL analysis indicated significant associations between APA events of genes and SNPs. We found that the APA event of the transmembrane p24 trafficking protein 9 (TMED9) is highly related to the SNP rs3749822, where the G allele would decrease the Poly-A length of TMED9 and increase its expression level.
Conclusion: The study elucidates the significant association between SNP rs3749822 and the APA event of the TMED9 gene, as well as their influences on TNBC, highlighting the susceptibility of SNP rs3749822 allele G for TNBC. Our findings provide new directions for further exploration of SNPs affecting APA events, aiding in identifying disease-susceptible populations.
Full text article
References
Katsura C, Ogunmwonyi I, Kankam H, Saha S. Breast cancer: presentation, investigation and management. BRITISH JOURNAL OF HOSPITAL MEDICINE. 2022;83. doi: 10.12968/hmed.2021.0459. PubMed PMID: WOS:000765530100009.
Lehmann B, Bauer J, Chen X, Sanders M, Chakravarthy A, Shyr Y, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. JOURNAL OF CLINICAL INVESTIGATION. 2011;121:2750-67. doi: 10.1172/JCI45014. PubMed PMID: WOS:000292413000024.
Borri F, Granaglia A. Pathology of triple negative breast cancer. SEMINARS IN CANCER BIOLOGY. 2021;72:136-45. doi: 10.1016/j.semcancer.2020.06.005. PubMed PMID: WOS:000651889400014.
Gupta GK, Collier AL, Lee D, Hoefer RA, Zheleva V, Siewertsz van Reesema LL, et al. Perspectives on Triple-Negative Breast Cancer: Current Treatment Strategies, Unmet Needs, and Potential Targets for Future Therapies. Cancers. 2020;12(9). doi: 10.3390/cancers12092392. PubMed PMID: WOS:000580219900001.
Yin L, Duan J-J, Bian X-W, Yu S-c. Triple-negative breast cancer molecular subtyping and treatment progress. Breast Cancer Research. 2020;22(1). doi: 10.1186/s13058-020-01296-5. PubMed PMID: WOS:000541519500001.
Sheng X, Wang J, Guo Y, Zhang J, Luo J. DNA N6-Methyladenine (6mA) Modification Regulates Drug Resistance in Triple Negative Breast Cancer. FRONTIERS IN ONCOLOGY. 2021;10. doi: 10.3389/fonc.2020.616098. PubMed PMID: WOS:000618636800001.
Quereda V, Bayle S, Vena F, Frydman S, Monastyrskyi A, Roush W, et al. Therapeutic Targeting of CDK12/CDK13 in Triple-Negative Breast Cancer. CANCER CELL. 2019;36:545-+. doi: 10.1016/j.ccell.2019.09.004. PubMed PMID: WOS:000496502300011.
Zhang W, Guan X, Tang J. The long non-coding RNA landscape in triple-negative breast cancer. CELL PROLIFERATION. 2021;54. doi: 10.1111/cpr.12966. PubMed PMID: WOS:000598294600001.
Tian B, Manley JL. Alternative polyadenylation of mRNA precursors. Nature Reviews Molecular Cell Biology. 2017;18(1):18-30. doi: 10.1038/nrm.2016.116. PubMed PMID: WOS:000393267500007.
Guo X, Ping J, Yang Y, Su X, Shu X, Wen W, et al. Large-Scale Alternative Polyadenylation-Wide Association Studies to Identify Putative Cancer Susceptibility Genes. CANCER RESEARCH. 2024;84:2707-19. doi: 10.1158/0008-5472.CAN-24-0521. PubMed PMID: WOS:001291894000003.
Ping J, Jia G, Cai Q, Guo X, Tao R, Ambrosone C, et al. Using genome and transcriptome data from African-ancestry female participants to identify putative breast cancer susceptibility genes. NATURE COMMUNICATIONS. 2024;15. doi: 10.1038/s41467-024-47650-5. PubMed PMID: WOS:001262129900013.
Zhang Y, Wang Y, Li C, Jiang T. Systemic Analysis of the Prognosis-Associated Alternative Polyadenylation Events in Breast Cancer. FRONTIERS IN GENETICS. 2020;11. doi: 10.3389/fgene.2020.590770. PubMed PMID: WOS:000589693400001.
Miles W, Lembo A, Volorio A, Brachtel E, Tian B, Sgroi D, et al. Alternative Polyadenylation in Triple-Negative Breast Tumors Allows NRAS and c-JUN to Bypass PUMILIO Posttranscriptional Regulation. CANCER RESEARCH. 2016;76:7231-41. doi: 10.1158/0008-5472.CAN-16-0844. PubMed PMID: WOS:000391470600016.
Nanavaty V, Abrash E, Hong C, Park S, Fink E, Li Z, et al. DNA Methylation Regulates Alternative Polyadenylation via CTCF and the Cohesin Complex. MOLECULAR CELL. 2020;78:752-+. doi: 10.1016/j.molcel.2020.03.024. PubMed PMID: WOS:000535936200017.
de Prisco N, Ford C, Elrod N, Lee W, Tang L, Huang K, et al. Alternative polyadenylation alters protein dosage by switching between intronic and 3′UTR sites. SCIENCE ADVANCES. 2023;9. doi: 10.1126/sciadv.ade4814. PubMed PMID: WOS:000943535600015.
Shulman E, Elkon R. Systematic identification of functional SNPs interrupting 3'UTR polyadenylation signals. PLOS GENETICS. 2020;16. doi: 10.1371/journal.pgen.1008977. PubMed PMID: WOS:000563927300001.
Yang R, Li Y, Wang H, Qin T, Yin X, Ma X. Therapeutic progress and challenges for triple negative breast cancer: targeted therapy and immunotherapy. MOLECULAR BIOMEDICINE. 2022;3. doi: 10.1186/s43556-022-00071-6. PubMed PMID: WOS:000895650700001.
Shen M, Xiao A, Yin S, Wang P, Lin X, Yu C, et al. Associations between UGT2B7 polymorphisms and cancer susceptibility: A meta-analysis. GENE. 2019;706:115-23. doi: 10.1016/j.gene.2019.05.025. PubMed PMID: WOS:000472241500015.
Preskill C, Weidhaas JB. SNPs in microRNA binding sites as prognostic and predictive cancer biomarkers. Crit Rev Oncog. 2013;18(4):327-40. doi: 10.1615/critrevoncog.2013007254. PubMed PMID: 23614619; PubMed Central PMCID: PMC4028830.
Kim S, Bai Y, Fan Z, Diergaarde B, Tseng G, Park H. The microRNA target site landscape is a novel molecular feature associating alternative polyadenylation with immune evasion activity in breast cancer. BRIEFINGS IN BIOINFORMATICS. 2021;22. doi: 10.1093/bib/bbaa191. PubMed PMID: WOS:000709461300128.
Millevoi S, Vagner S. Molecular mechanisms of eukaryotic pre-mRNA 3' end processing regulation. NUCLEIC ACIDS RESEARCH. 2010;38:2757-74. doi: 10.1093/nar/gkp1176. PubMed PMID: WOS:000277994600009.
Neve J, Patel R, Wang Z, Louey A, Furger AM. Cleavage and polyadenylation: Ending the message expands gene regulation. Rna Biology. 2017;14(7):865-90. doi: 10.1080/15476286.2017.1306171. PubMed PMID: WOS:000407258600009.
Gil A, Proudfoot NJ. POSITION-DEPENDENT SEQUENCE ELEMENTS DOWNSTREAM OF AAUAAA ARE REQUIRED FOR EFFICIENT RABBIT BETA-GLOBIN MESSENGER-RNA 3' END FORMATION. Cell. 1987;49(3):399-406. doi: 10.1016/0092-8674(87)90292-3. PubMed PMID: WOS:A1987H297100015.
Morris G, Naidu S, Topham A, Guiles F, Xu Y, McCue P, et al. Differences in breast carcinoma characteristics in newly diagnosed African-American and Caucasian patients - A single-institution compilation compared with the National Cancer Institute's Surveillance, Epidemiology, and End Results Database. CANCER. 2007;110:876-84. doi: 10.1002/cncr.22836. PubMed PMID: WOS:000248586700024.
Thomas LF, Saetrom P. Single Nucleotide Polymorphisms Can Create Alternative Polyadenylation Signals and Affect Gene Expression through Loss of MicroRNA-Regulation. Plos Computational Biology. 2012;8(8). doi: 10.1371/journal.pcbi.1002621. PubMed PMID: WOS:000308553500010.
Jiang Y, Ma D, Suo C, Shi J, Xue M, Hu X, et al. Genomic and Transcriptomic Landscape of Triple-Negative Breast Cancers: Subtypes and Treatment Strategies. CANCER CELL. 2019;35:428-+. doi: 10.1016/j.ccell.2019.02.001. PubMed PMID: WOS:000461697400010.
Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-60. doi: 10.1093/bioinformatics/btp324. PubMed PMID: WOS:000267665900006.
Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021;10(2). doi: 10.1093/gigascience/giab008. PubMed PMID: WOS:000637191300010.
Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26(6):841-2. doi: 10.1093/bioinformatics/btq033. PubMed PMID: WOS:000275243500019.
Tarasov A, Vilella AJ, Cuppen E, Nijman IJ, Prins P. Sambamba: fast processing of NGS alignment formats. Bioinformatics. 2015;31(12):2032-4. doi: 10.1093/bioinformatics/btv098. PubMed PMID: WOS:000356625700063.
Chen Z-L, Meng J-M, Cao Y, Yin J-L, Fang R-Q, Fan S-B, et al. A high-speed search engine pLink 2 with systematic evaluation for proteome-scale identification of cross-linked peptides. Nature Communications. 2019;10. doi: 10.1038/s41467-019-11337-z. PubMed PMID: WOS:000477860700010.
Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923-30. doi: 10.1093/bioinformatics/btt656. PubMed PMID: WOS:000334078300005.
Li L, Huang K-L, Gao Y, Cui Y, Wang G, Elrod ND, et al. An atlas of alternative polyadenylation quantitative trait loci contributing to complex trait and disease heritability. Nature Genetics. 2021;53(7):994-+. doi: 10.1038/s41588-021-00864-5. PubMed PMID: WOS:000650134000002.
Love M, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. GENOME BIOLOGY. 2014;15. doi: 10.1186/s13059-014-0550-8. PubMed PMID: WOS:000346609500022.
Ongen H, Buil A, Brown AA, Dermitzakis ET, Delaneau O. Fast and efficient QTL mapper for thousands of molecular phenotypes. Bioinformatics. 2016;32(10):1479-85. doi: 10.1093/bioinformatics/btv722. PubMed PMID: WOS:000376656900006.
Erson-Bensan A. Alternative polyadenylation and RNA-binding proteins. JOURNAL OF MOLECULAR ENDOCRINOLOGY. 2016;57:F29-F34. doi: 10.1530/JME-16-0070. PubMed PMID: WOS:000381726800002.
Pan X, Fang Y, Li X, Yang Y, Shen H. RBPsuite: RNA-protein binding sites prediction suite based on deep learning. BMC GENOMICS. 2020;21. doi: 10.1186/s12864-020-07291-6. PubMed PMID: WOS:000600100600006.
Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z, et al. clusterProfiler 4.0: A universal enrichment tool for interpreting omics data. INNOVATION. 2021;2. doi: 10.1016/j.xinn.2021.100141. PubMed PMID: WOS:000747244900017.
Sachs M. plotROC: A Tool for Plotting ROC Curves. JOURNAL OF STATISTICAL SOFTWARE. 2017;79. doi: 10.18637/jss.v079.c02. PubMed PMID: WOS:000407288500001.
Vigneshwaran G, Hasan Q, Kumar R, Eranki A. Analysis of single-nucleotide polymorphisms in genes associated with triple-negative breast cancer. FRONTIERS IN GENETICS. 2022;13. doi: 10.3389/fgene.2022.1071352. PubMed PMID: WOS:000897057300001.
Shan J, Chouchane A, Mokrab Y, Saad M, Boujassoum S, Sayaman R, et al. Genetic Variation in CCL5 Signaling Genes and Triple Negative Breast Cancer: Susceptibility and Prognosis Implications. FRONTIERS IN ONCOLOGY. 2019;9. doi: 10.3389/fonc.2019.01328. PubMed PMID: WOS:000503839100001.
Pereira K, Shan J, Licht J, Bennett R. Histone mutations in cancer. BIOCHEMICAL SOCIETY TRANSACTIONS. 2023;51:1749-63. doi: 10.1042/BST20210567. PubMed PMID: WOS:001071936800001.
Behrends M, Engmann O. Linker histone H1.5 is an underestimated factor in differentiation and carcinogenesis. ENVIRONMENTAL EPIGENETICS. 2020;6. doi: 10.1093/eep/dvaa013. PubMed PMID: WOS:000585252700001.
Jiang Y, Liu Y, Tan X, Yu S, Luo J. TPX2 as a Novel Prognostic Indicator and Promising Therapeutic Target in Triple-negative Breast Cancer. CLINICAL BREAST CANCER. 2019;19:450-5. doi: 10.1016/j.clbc.2019.05.012. PubMed PMID: WOS:000499653300019.
Koyuncu D, Sharma U, Goka E, Lippman M. Spindle assembly checkpoint gene BUB1B is essential in breast cancer cell survival. BREAST CANCER RESEARCH AND TREATMENT. 2021;185:331-41. doi: 10.1007/s10549-020-05962-2. PubMed PMID: WOS:000583101200001.
Shinmura K, Kato H, Kawanishi Y, Igarashi H, Goto M, Tao H, et al. Abnormal Expressions of DNA Glycosylase Genes NEIL1, NEIL2, and NEIL3 Are Associated with Somatic Mutation Loads in Human Cancer. OXIDATIVE MEDICINE AND CELLULAR LONGEVITY. 2016;2016. doi: 10.1155/2016/1546392. PubMed PMID: WOS:000372230400001.
Li T, Zeng H, Shan Z, Ye R, Cheang T, Zhang Y, et al. Overexpression of kinesin superfamily members as prognostic biomarkers of breast cancer. CANCER CELL INTERNATIONAL. 2020;20. doi: 10.1186/s12935-020-01191-1. PubMed PMID: WOS:000529207300003.
Tang H, Huang X, Wang J, Yang L, Kong Y, Gao G, et al. circKIF4A acts as a prognostic factor and mediator to regulate the progression of triple-negative breast cancer. MOLECULAR CANCER. 2019;18. doi: 10.1186/s12943-019-0946-x. PubMed PMID: WOS:000458461100001.
Nakamura M, Takano A, Thang P, Tsevegjav B, Zhu M, Yokose T, et al. Characterization of KIF20A as a prognostic biomarker and therapeutic target for different subtypes of breast cancer. INTERNATIONAL JOURNAL OF ONCOLOGY. 2020;57:277-88. doi: 10.3892/ijo.2020.5060. PubMed PMID: WOS:000544982500022.
Roberts B, Satpute-Krishnan P. The many hats of transmembrane emp24 domain protein TMED9 in secretory pathway homeostasis. FRONTIERS IN CELL AND DEVELOPMENTAL BIOLOGY. 2023;10. doi: 10.3389/fcell.2022.1096899. PubMed PMID: WOS:000922110800001.
Ju G, Xu C, Zeng K, Zhou T, Zang L. High expression of transmembrane P24 trafficking protein 9 predicts poor prognosis in breast carcinoma. BIOENGINEERED. 2021;12:8965-79. doi: 10.1080/21655979.2021.1990673. PubMed PMID: WOS:000711203500001.
Fang Z, Song YX, Wo GQ, Zhou HL, Li L, Yang SY, et al. Screening of the novel immune-suppressive biomarkers of TMED family and whether knockdown of TMED2/3/4/9 inhibits cell migration and invasion in breast cancer. Ann Transl Med. 2022;10(23):1280. doi: 10.21037/atm-22-5444. PubMed PMID: 36618780; PubMed Central PMCID: PMC9816852.
Yang Y, Chien M, Lai T, Tung M, Jan Y, Chang W, et al. Proteomics-based identification of TMED9 is linked to vascular invasion and poor prognoses in patients with hepatocellular carcinoma. JOURNAL OF BIOMEDICAL SCIENCE. 2021;28. doi: 10.1186/s12929-021-00727-5. PubMed PMID: WOS:000644099400001.
Han G, Yun H, Chung J, Kim J, Cho H. TMED9 Expression Level as a Biomarker of Epithelial Ovarian Cancer Progression and Prognosis. CANCER GENOMICS & PROTEOMICS. 2022;19:692-702. doi: 10.21873/cgp.20352. PubMed PMID: WOS:000887077500003.
Mishra S, Bernal C, Silvano M, Anand S, Altaba ARi. The protein secretion modulator TMED9 drives CNIH4/TGF alpha/GLI signaling opposing TMED3-WNT-TCF to promote colon cancer metastases. Oncogene. 2019;38(29):5817-37. doi: 10.1038/s41388-019-0845-z. PubMed PMID: WOS:000480752800006.
CIARDIELLO F, KIM N, MCGEADY M, LISCIA D, SAEKI T, BIANCO C, et al. EXPRESSION OF TRANSFORMING GROWTH-FACTOR ALPHA (TGF-ALPHA) IN BREAST-CANCER. ANNALS OF ONCOLOGY. 1991;2:169-82. PubMed PMID: WOS:A1991FH23700003.
Pospiech K, Orzechowska M, Nowakowska M, Anusewicz D, Pluciennik E, Kosla K, et al. TGF alpha-EGFR pathway in breast carcinogenesis, association with WWOX expression and estrogen activation. JOURNAL OF APPLIED GENETICS. 2022;63:339-59. doi: 10.1007/s13353-022-00690-3. PubMed PMID: WOS:000769375000001.
Wang B, Yu T, Hu Y, Xiang M, Peng H, Lin Y, et al. Prognostic role of Gli1 expression in breast cancer: a meta-analysis. ONCOTARGET. 2017;8:81088-97. doi: 10.18632/oncotarget.19080. PubMed PMID: WOS:000412465700085.
Xu L, Kwon Y, Frolova N, Steg A, Yuan K, Johnson M, et al. Gli1 promotes cell survival and is predictive of a poor outcome in ERα-negative breast cancer. BREAST CANCER RESEARCH AND TREATMENT. 2010;123:59-71. doi: 10.1007/s10549-009-0617-5. PubMed PMID: WOS:000280063200007.
Tian B, Graber J. Signals for pre-mRNA cleavage and polyadenylation. WILEY INTERDISCIPLINARY REVIEWS-RNA. 2012;3:385-96. doi: 10.1002/wrna.116. PubMed PMID: WOS:000302995100006.
Park C, Zhou J, Wong A, Chen K, Theesfeld C, Darnell R, et al. Genome-wide landscape of RNA-binding protein target site dysregulation reveals a major impact on psychiatric disorder risk. NATURE GENETICS. 2021;53:166-+. doi: 10.1038/s41588-020-00761-3. PubMed PMID: WOS:000608658900004.
Yang E, Bahn J, Hsiaol E, Tan B, Sun Y, Fu T, et al. Allele-specific binding of RNA-binding proteins reveals functional genetic variants in the RNA. NATURE COMMUNICATIONS. 2019;10. doi: 10.1038/s41467-019-09292-w. PubMed PMID: WOS:000461995800009.
Proudfoot NJ. SEQUENCE-ANALYSIS OF 3' NON-CODING REGIONS OF RABBIT ALPHA-GLOBIN AND BETA-GLOBIN MESSENGER-RNAS. Journal of Molecular Biology. 1976;107(4):491-525. doi: 10.1016/s0022-2836(76)80080-0. PubMed PMID: WOS:A1976CL85500007.
Denome RM, Cole CN. PATTERNS OF POLYADENYLATION SITE SELECTION IN GENE CONSTRUCTS CONTAINING MULTIPLE POLYADENYLATION SIGNALS. Molecular and Cellular Biology. 1988;8(11):4829-39. doi: 10.1128/mcb.8.11.4829. PubMed PMID: WOS:A1988Q686900030.
Proudfoot NJ. Ending the message: poly(A) signals then and now. Genes & Development. 2011;25(17):1770-82. doi: 10.1101/gad.17268411. PubMed PMID: WOS:000294555500003.
Chen Z, Hao W, Tang J, Gao W, Xu H. CSTF2 Promotes Hepatocarcinogenesis and Hepatocellular Carcinoma Progression via Aerobic Glycolysis. FRONTIERS IN ONCOLOGY. 2022;12. doi: 10.3389/fonc.2022.897804. PubMed PMID: WOS:000830225000001.
Tan Y, Zheng T, Zhang R, Chen S, Cheng Q, Zhang J, et al. Alternative polyadenylation writer CSTF2 forms a positive loop with FGF2 to promote tubular epithelial-mesenchymal transition and renal fibrosis. BIOCHIMICA ET BIOPHYSICA ACTA-MOLECULAR BASIS OF DISEASE. 2022;1868. doi: 10.1016/j.bbadis.2022.166541. PubMed PMID: WOS:000888891600003.
Batra R, Charizanis K, Manchanda M, Mohan A, Li M, Finn D, et al. Loss of MBNL Leads to Disruption of Developmentally Regulated Alternative Polyadenylation in RNA-Mediated Disease. MOLECULAR CELL. 2014;56:311-22. doi: 10.1016/j.molcel.2014.08.027. PubMed PMID: WOS:000344484600012.
Biziaev N, Shuvalov A, Salman A, Egorova T, Shuvalova E, Alkalaeva E. The impact of mRNA poly(A) tail length on eukaryotic translation stages. NUCLEIC ACIDS RESEARCH. 2024;52:7792-808. doi: 10.1093/nar/gkae510. PubMed PMID: WOS:001246205200001.
Guo S, Lin S. mRNA alternative polyadenylation (APA) in regulation of gene expression and diseases. GENES & DISEASES. 2023;10:165-74. doi: 10.1016/j.gendis.2021.09.005. PubMed PMID: WOS:000970796600001.
Afonso-Grunz F, Mueller S. Principles of miRNA-mRNA interactions: beyond sequence complementarity. Cellular and Molecular Life Sciences. 2015;72(16):3127-41. doi: 10.1007/s00018-015-1922-2. PubMed PMID: WOS:000358088000009.
Mayr C, Bartel DP. Widespread Shortening of 3 ' UTRs by Alternative Cleavage and Polyadenylation Activates Oncogenes in Cancer Cells. Cell. 2009;138(4):673-84. doi: 10.1016/j.cell.2009.06.016. PubMed PMID: WOS:000269156100010.
Altshuler D, Durbin R, Abecasis G, Bentley D, Chakravarti A, Clark A, et al. A global reference for human genetic variation. NATURE. 2015;526:68-+. doi: 10.1038/nature15393. PubMed PMID: WOS:000362095100036.
Scott L, Mobley L, Kuo T, Il'yasova D. Update on triple-negative breast cancer disparities for the United States: A population-based study from the United States Cancer Statistics database, 2010 through 2014. CANCER. 2019;125:3412-7. doi: 10.1002/cncr.32207. PubMed PMID: WOS:000486001800018.
Bauer K, Brown M, Cress R, Parise C, Caggiano V. Descriptive analysis of estrogen receptor (ER)negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype - A population-based study from the California Cancer Registry. CANCER. 2007;109:1721-8. doi: 10.1002/cncr.22618. PubMed PMID: WOS:000245937000004.
Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006;295(21):2492-502. doi: 10.1001/jama.295.21.2492. PubMed PMID: 16757721.
Authors
Copyright (c) 2024 Archives of Breast Cancer
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Copyright©. This is an open-access article distributed under the terms of the Creative Commons Attribution-Non-Commercial 4.0 International License, which permits copy and redistribution of the material in any medium or format or adapt, remix, transform, and build upon the material for any purpose, except for commercial purposes.