Desmocollin-1 is associated with pro-metastatic phenotype of luminal A breast cancer cells and is modulated by parthenolide
Language English Country England, Great Britain Media electronic
Document type Journal Article
Grant support
NU22-08-00230
Ministerstvo Zdravotnictví Ceské Republiky
LM2023042
Ministerstvo Školství, Mládeže a Tělovýchovy
CZ.02.1.01/0.0/0.0/18_046/0015974
Ministerstvo Školství, Mládeže a Tělovýchovy
LM2018132
Ministerstvo Školství, Mládeže a Tělovýchovy
LX22NPO5102
Ministerstvo Školství, Mládeže a Tělovýchovy
PubMed
37620794
PubMed Central
PMC10464112
DOI
10.1186/s11658-023-00481-6
PII: 10.1186/s11658-023-00481-6
Knihovny.cz E-resources
- Keywords
- Breast cancer, DIA, DSC1, Metastasis, Proteomics, Pull-down,
- MeSH
- Chromatography, Liquid MeSH
- Desmocollins * metabolism MeSH
- Humans MeSH
- MCF-7 Cells MeSH
- Neoplasms * MeSH
- Proteome MeSH
- Sesquiterpenes pharmacology MeSH
- Tandem Mass Spectrometry MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Desmocollins * MeSH
- DSC1 protein, human MeSH Browser
- parthenolide MeSH Browser
- Proteome MeSH
- Sesquiterpenes MeSH
BACKGROUND: Desmocollin-1 (DSC1) is a desmosomal transmembrane glycoprotein that maintains cell-to-cell adhesion. DSC1 was previously associated with lymph node metastasis of luminal A breast tumors and was found to increase migration and invasion of MCF7 cells in vitro. Therefore, we focused on DSC1 role in cellular and molecular mechanisms in luminal A breast cancer and its possible therapeutic modulation. METHODS: Western blotting was used to select potential inhibitor decreasing DSC1 protein level in MCF7 cell line. Using atomic force microscopy we evaluated effect of DSC1 overexpression and modulation on cell morphology. The LC-MS/MS analysis of total proteome on Orbitrap Lumos and RNA-Seq analysis of total transcriptome on Illumina NextSeq 500 were performed to study the molecular mechanisms associated with DSC1. Pull-down analysis with LC-MS/MS detection was carried out to uncover DSC1 protein interactome in MCF7 cells. RESULTS: Analysis of DSC1 protein levels in response to selected inhibitors displays significant DSC1 downregulation (p-value ≤ 0.01) in MCF7 cells treated with NF-κB inhibitor parthenolide. Analysis of mechanic cell properties in response to DSC1 overexpression and parthenolide treatment using atomic force microscopy reveals that DSC1 overexpression reduces height of MCF7 cells and conversely, parthenolide decreases cell stiffness of MCF7 cells overexpressing DSC1. The LC-MS/MS total proteome analysis in data-independent acquisition mode shows a strong connection between DSC1 overexpression and increased levels of proteins LACRT and IGFBP5, increased expression of IGFBP5 is confirmed by RNA-Seq. Pathway analysis of proteomics data uncovers enrichment of proliferative MCM_BIOCARTA pathway including CDK2 and MCM2-7 after DSC1 overexpression. Parthenolide decreases expression of LACRT, IGFBP5 and MCM_BIOCARTA pathway specifically in DSC1 overexpressing cells. Pull-down assay identifies DSC1 interactions with cadherin family proteins including DSG2, CDH1, CDH3 and tyrosine kinase receptors HER2 and HER3; parthenolide modulates DSC1-HER3 interaction. CONCLUSIONS: Our systems biology data indicate that DSC1 is connected to mechanisms of cell cycle regulation in luminal A breast cancer cells, and can be effectively modulated by parthenolide.
Central European Institute of Technology Masaryk University Brno Czech Republic
Masaryk Memorial Cancer Institute RECAMO Brno Czech Republic
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Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249. doi: 10.3322/caac.21660. PubMed DOI
Dai X, Xiang L, Li T, Bai Z. Cancer hallmarks, biomarkers and breast cancer molecular subtypes. J Cancer. 2016;7(10):1281–1294. PubMed PMC
Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature. 2000;406(6797):747–752. PubMed
Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA. 2001;98(19):10869–10874. PubMed PMC
Harbeck N, Gnant M. Breast cancer. Lancet. 2017;389(10074):1134–1150. PubMed
Tran B, Bedard PL. Luminal-B breast cancer and novel therapeutic targets. Breast Cancer Res. 2011;13(6):221. PubMed PMC
Prat A, Pineda E, Adamo B, Galván P, Fernández A, Gaba L, et al. Clinical implications of the intrinsic molecular subtypes of breast cancer. Breast. 2015;24(Suppl 2):S26–35. PubMed
Morandi A, Martin LA, Gao Q, Pancholi S, Mackay A, Robertson D, et al. GDNF-RET signaling in ER-positive breast cancers is a key determinant of response and resistance to aromatase inhibitors. Cancer Res. 2013;73(12):3783–3795. PubMed PMC
KaramiFath M, Azargoonjahromi A, Kiani A, Jalalifar F, Osati P, Akbari Oryani M, et al. The role of epigenetic modifications in drug resistance and treatment of breast cancer. Cell Mol Biol Lett. 2022;27(1):52. PubMed PMC
Buonomo OC, Caredda E, Portarena I, Vanni G, Orlandi A, Bagni C, et al. New insights into the metastatic behavior after breast cancer surgery, according to well-established clinicopathological variables and molecular subtypes. PLoS ONE. 2017;12(9):e0184680. PubMed PMC
Lapcik P, Pospisilova A, Janacova L, Grell P, Fabian P, Bouchal P. How different are the molecular mechanisms of nodal and distant metastasis in luminal A breast cancer? Cancers (Basel) 2020;12(9):E2638. PubMed PMC
Tang Y, Wang Y, Kiani MF, Wang B. Classification, treatment strategy, and associated drug resistance in breast cancer. Clin Breast Cancer. 2016;16(5):335–343. PubMed
Faktor J, Knopfova L, Lapcik P, Janacova L, Paralova V, Bouchalova P, et al. Proteomics identification and validation of desmocollin-1 and catechol-O-methyltransferase as proteins associated with breast cancer cell migration and metastasis. Proteomics. 2019;19(21–22):e1900073. PubMed
Kottke MD, Delva E, Kowalczyk AP. The desmosome: cell science lessons from human diseases. J Cell Sci. 2006;119(Pt 5):797–806. PubMed
O’Shea C, Fitzpatrick JE, Koch PJ. Desmosomal defects in acantholytic squamous cell carcinomas. J Cutan Pathol. 2014;41(11):873–879. PubMed PMC
Khan K, Hardy R, Haq A, Ogunbiyi O, Morton D, Chidgey M. Desmocollin switching in colorectal cancer. Br J Cancer. 2006;95(10):1367–1370. PubMed PMC
Faktor J, Sucha R, Paralova V, Liu Y, Bouchal P. Comparison of targeted proteomics approaches for detecting and quantifying proteins derived from human cancer tissues. Proteomics. 2017 doi: 10.1002/pmic.201600323. PubMed DOI
Maryáš J, Faktor J, Čápková L, Müller P, Skládal P, Bouchal P. Pull-down assay on streptavidin beads and surface plasmon resonance chips for SWATH-MS-based interactomics. Cancer Genomics Proteomics. 2018;15(5):395–404. PubMed PMC
Wiśniewski JR, Ostasiewicz P, Mann M. High recovery FASP applied to the proteomic analysis of microdissected formalin fixed paraffin embedded cancer tissues retrieves known colon cancer markers. J Proteome Res. 2011;10(7):3040–3049. PubMed
Bouchal P, Roumeliotis T, Hrstka R, Nenutil R, Vojtesek B, Garbis SD. Biomarker discovery in low-grade breast cancer using isobaric stable isotope tags and two-dimensional liquid chromatography-tandem mass spectrometry (iTRAQ-2DLC-MS/MS) based quantitative proteomic analysis. J Proteome Res. 2009;8(1):362–373. PubMed
Stejskal K, Potěšil D, Zdráhal Z. Suppression of peptide sample losses in autosampler vials. J Proteome Res. 2013;12(6):3057–3062. PubMed
Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545–15550. PubMed PMC
Getsios S, Amargo EV, Dusek RL, Ishii K, Sheu L, Godsel LM, et al. Coordinated expression of desmoglein 1 and desmocollin 1 regulates intercellular adhesion. Differentiation. 2004;72(8):419–433. PubMed
Schüle S, Neuhäuser C, Rauchfuß F, Knösel T, Settmacher U, Altendorf-Hofmann A. The influence of desmocollin 1–3 expression on prognosis after curative resection of colorectal liver metastases. Int J Colorectal Dis. 2014;29(1):9–14. PubMed
Myklebust MP, Fluge Ø, Immervoll H, Skarstein A, Balteskard L, Bruland O, et al. Expression of DSG1 and DSC1 are prognostic markers in anal carcinoma patients. Br J Cancer. 2012;106(4):756–762. PubMed PMC
Wang Y, Chen C, Wang X, Jin F, Liu Y, Liu H, et al. Lower DSC1 expression is related to the poor differentiation and prognosis of head and neck squamous cell carcinoma (HNSCC) J Cancer Res Clin Oncol. 2016;142(12):2461–2468. PubMed PMC
Knösel T, Chen Y, Hotovy S, Settmacher U, Altendorf-Hofmann A, Petersen I. Loss of desmocollin 1–3 and homeobox genes PITX1 and CDX2 are associated with tumor progression and survival in colorectal carcinoma. Int J Colorectal Dis. 2012;27(11):1391–1399. PubMed
Jaeger J, Koczan D, Thiesen HJ, Ibrahim SM, Gross G, Spang R, et al. Gene expression signatures for tumor progression, tumor subtype, and tumor thickness in laser-microdissected melanoma tissues. Clin Cancer Res. 2007;13(3):806–815. PubMed
Zhou J, Zhang H, Gu P, Bai J, Margolick JB, Zhang Y. NF-kappaB pathway inhibitors preferentially inhibit breast cancer stem-like cells. Breast Cancer Res Treat. 2008;111(3):419–427. PubMed PMC
Liu Y, Lu WL, Guo J, Du J, Li T, Wu JW, et al. A potential target associated with both cancer and cancer stem cells: a combination therapy for eradication of breast cancer using vinorelbine stealthy liposomes plus parthenolide stealthy liposomes. J Control Release. 2008;129(1):18–25. PubMed
Zhang X, Zhang B, Zhang P, Lian L, Li L, Qiu Z, et al. Norcantharidin regulates ERα signaling and tamoxifen resistance via targeting miR-873/CDK3 in breast cancer cells. PLoS ONE. 2019;14(5):e0217181. PubMed PMC
Shou LM, Zhang QY, Li W, Xie X, Chen K, Lian L, et al. Cantharidin and norcantharidin inhibit the ability of MCF-7 cells to adhere to platelets via protein kinase C pathway-dependent downregulation of α2 integrin. Oncol Rep. 2013;30(3):1059–1066. PubMed PMC
Yang PY, Chen MF, Kao YH, Hu DN, Chang FR, Wu YC. Norcantharidin induces apoptosis of breast cancer cells: involvement of activities of mitogen activated protein kinases and signal transducers and activators of transcription. Toxicol In Vitro. 2011;25(3):699–707. PubMed
Liu FL, Chen CL, Lee CC, Wu CC, Hsu TH, Tsai CY, et al. The simultaneous inhibitory effect of niclosamide on RANKL-induced osteoclast formation and osteoblast differentiation. Int J Med Sci. 2017;14(9):840–852. PubMed PMC
Ye T, Xiong Y, Yan Y, Xia Y, Song X, Liu L, et al. The anthelmintic drug niclosamide induces apoptosis, impairs metastasis and reduces immunosuppressive cells in breast cancer model. PLoS ONE. 2014;9(1):e85887. PubMed PMC
Dawood M, Ooko E, Efferth T. Collateral sensitivity of parthenolide via NF-κB and HIF-α inhibition and epigenetic changes in drug-resistant cancer cell lines. Front Pharmacol. 2019;10:542. PubMed PMC
Berdan CA, Ho R, Lehtola HS, To M, Hu X, Huffman TR, et al. Parthenolide covalently targets and inhibits focal adhesion kinase in breast cancer cells. Cell Chem Biol. 2019;26(7):1027–1035.e22. PubMed PMC
Kwok BH, Koh B, Ndubuisi MI, Elofsson M, Crews CM. The anti-inflammatory natural product parthenolide from the medicinal herb Feverfew directly binds to and inhibits IkappaB kinase. Chem Biol. 2001;8(8):759–766. PubMed
Li X, Kong L, Yang Q, Duan A, Ju X, Cai B, et al. Parthenolide inhibits ubiquitin-specific peptidase 7 (USP7), Wnt signaling, and colorectal cancer cell growth. J Biol Chem. 2020;295(11):3576–3589. PubMed PMC
Raudenska M, Kratochvilova M, Vicar T, Gumulec J, Balvan J, Polanska H, et al. Cisplatin enhances cell stiffness and decreases invasiveness rate in prostate cancer cells by actin accumulation. Sci Rep. 2019;9(1):1660. PubMed PMC
Li QS, Lee GYH, Ong CN, Lim CT. AFM indentation study of breast cancer cells. Biochem Biophys Res Commun. 2008;374(4):609–613. PubMed
Ansardamavandi A, Tafazzoli-Shadpour M, Omidvar R, Jahanzad I. Quantification of effects of cancer on elastic properties of breast tissue by atomic force microscopy. J Mech Behav Biomed Mater. 2016;60:234–242. PubMed
Xu W, Mezencev R, Kim B, Wang L, McDonald J, Sulchek T. Cell stiffness is a biomarker of the metastatic potential of ovarian cancer cells. PLoS ONE. 2012;7(10):e46609. PubMed PMC
Bastatas L, Martinez-Marin D, Matthews J, Hashem J, Lee YJ, Sennoune S, et al. AFM nano-mechanics and calcium dynamics of prostate cancer cells with distinct metastatic potential. Biochim Biophys Acta. 2012;1820(7):1111–1120. PubMed
Zhang G, Long M, Wu ZZ, Yu WQ. Mechanical properties of hepatocellular carcinoma cells. World J Gastroenterol. 2002;8(2):243–246. PubMed PMC
Faria EC, Ma N, Gazi E, Gardner P, Brown M, Clarke NW, et al. Measurement of elastic properties of prostate cancer cells using AFM. Analyst. 2008;133(11):1498–1500. PubMed
Ren H, Yin P, Duan C. IGFBP-5 regulates muscle cell differentiation by binding to IGF-II and switching on the IGF-II auto-regulation loop. J Cell Biol. 2008;182(5):979–991. PubMed PMC
Butt AJ, Dickson KA, McDougall F, Baxter RC. Insulin-like growth factor-binding protein-5 inhibits the growth of human breast cancer cells in vitro and in vivo. J Biol Chem. 2003;278(32):29676–29685. PubMed
Kuemmerle JF, Zhou H. Insulin-like growth factor-binding protein-5 (IGFBP-5) stimulates growth and IGF-I secretion in human intestinal smooth muscle by Ras-dependent activation of p38 MAP kinase and Erk1/2 pathways. J Biol Chem. 2002;277(23):20563–20571. PubMed
Sun M, Long J, Yi Y, Xia W. Importin α-importin β complex mediated nuclear translocation of insulin-like growth factor binding protein-5. Endocr J. 2017;64(10):963–975. PubMed
Flint DJ, Tonner E, Allan GJ. Insulin-like growth factor binding proteins: IGF-dependent and -independent effects in the mammary gland. J Mammary Gland Biol Neoplasia. 2000;5(1):65–73. PubMed
McCaig C, Perks CM, Holly JMP. Signalling pathways involved in the direct effects of IGFBP-5 on breast epithelial cell attachment and survival. J Cell Biochem. 2002;84(4):784–794. PubMed
McCaig C, Perks CM, Holly JMP. Intrinsic actions of IGFBP-3 and IGFBP-5 on Hs578T breast cancer epithelial cells: inhibition or accentuation of attachment and survival is dependent upon the presence of fibronectin. J Cell Sci. 2002;115(Pt 22):4293–4303. PubMed
Güllü G, Karabulut S, Akkiprik M. Functional roles and clinical values of insulin-like growth factor-binding protein-5 in different types of cancers. Chin J Cancer. 2012;31(6):266–280. PubMed PMC
Nishidate T, Katagiri T, Lin ML, Mano Y, Miki Y, Kasumi F, et al. Genome-wide gene-expression profiles of breast-cancer cells purified with laser microbeam microdissection: identification of genes associated with progression and metastasis. Int J Oncol. 2004;25(4):797–819. PubMed
Mita K, Zhang Z, Ando Y, Toyama T, Hamaguchi M, Kobayashi S, et al. Prognostic significance of insulin-like growth factor binding protein (IGFBP)-4 and IGFBP-5 expression in breast cancer. Jpn J Clin Oncol. 2007;37(8):575–582. PubMed
Hao X, Sun B, Hu L, Lähdesmäki H, Dunmire V, Feng Y, et al. Differential gene and protein expression in primary breast malignancies and their lymph node metastases as revealed by combined cDNA microarray and tissue microarray analysis. Cancer. 2004;100(6):1110–1122. PubMed
Wang H, Arun BK, Wang H, Fuller GN, Zhang W, Middleton LP, et al. IGFBP2 and IGFBP5 overexpression correlates with the lymph node metastasis in T1 breast carcinomas. Breast J. 2008;14(3):261–267. PubMed
Pekonen F, Nyman T, Ilvesmäki V, Partanen S. Insulin-like growth factor binding proteins in human breast cancer tissue. Cancer Res. 1992;52(19):5204–5207. PubMed
McGuire SE, Hilsenbeck SG, Figueroa JA, Jackson JG, Yee D. Detection of insulin-like growth factor binding proteins (IGFBPs) by ligand blotting in breast cancer tissues. Cancer Lett. 1994;77(1):25–32. PubMed
Akkiprik M, Feng Y, Wang H, Chen K, Hu L, Sahin A, et al. Multifunctional roles of insulin-like growth factor binding protein 5 in breast cancer. Breast Cancer Res. 2008;10(4):212. PubMed PMC
Li X, Cao X, Li X, Zhang W, Feng Y. Expression level of insulin-like growth factor binding protein 5 mRNA is a prognostic factor for breast cancer. Cancer Sci. 2007;98(10):1592–1596. PubMed PMC
Ahn BY, Elwi AN, Lee B, Trinh DLN, Klimowicz AC, Yau A, et al. Genetic screen identifies insulin-like growth factor binding protein 5 as a modulator of tamoxifen resistance in breast cancer. Cancer Res. 2010;70(8):3013–3019. PubMed
Akkiprik M, Hu L, Sahin A, Hao X, Zhang W. The subcellular localization of IGFBP5 affects its cell growth and migration functions in breast cancer. BMC Cancer. 2009;9:103. PubMed PMC
Wang N, Zimmerman K, Raab RW, McKown RL, Hutnik CML, Talla V, et al. Lacritin rescues stressed epithelia via rapid forkhead box O3 (FOXO3)-associated autophagy that restores metabolism. J Biol Chem. 2013;288(25):18146–18161. PubMed PMC
Feng MM, Baryla J, Liu H, Laurie GW, McKown RL, Ashki N, et al. Cytoprotective effect of lacritin on human corneal epithelial cells exposed to benzalkonium chloride in vitro. Curr Eye Res. 2014;39(6):604–610. PubMed PMC
Wang J, Wang N, Xie J, Walton SC, McKown RL, Raab RW, et al. Restricted epithelial proliferation by lacritin via PKCalpha-dependent NFAT and mTOR pathways. J Cell Biol. 2006;174(5):689–700. PubMed PMC
Weigelt B, Bosma AJ, van’t Veer LJ. Expression of a novel lacrimal gland gene lacritin in human breast tissues. J Cancer Res Clin Oncol. 2003;129(12):735–736. PubMed
Ma P, Beck SL, Raab RW, McKown RL, Coffman GL, Utani A, et al. Heparanase deglycanation of syndecan-1 is required for binding of the epithelial-restricted prosecretory mitogen lacritin. J Cell Biol. 2006;174(7):1097–1106. PubMed PMC
Castedo M, Perfettini JL, Roumier T, Kroemer G. Cyclin-dependent kinase-1: linking apoptosis to cell cycle and mitotic catastrophe. Cell Death Differ. 2002;9(12):1287–1293. PubMed
Hwang HC, Clurman BE. Cyclin E in normal and neoplastic cell cycles. Oncogene. 2005;24(17):2776–2786. PubMed
Guo Y, Fan Y, Zhang J, Chang L, Lin JD, Chen YE. Peroxisome proliferator-activated receptor γ coactivator 1β (PGC-1β) protein attenuates vascular lesion formation by inhibition of chromatin loading of minichromosome maintenance complex in smooth muscle cells. J Biol Chem. 2013;288(7):4625–4636. PubMed PMC
Kowalczyk AP, Green KJ. Structure, function, and regulation of desmosomes. Prog Mol Biol Transl Sci. 2013;116:95–118. PubMed PMC
Garrod D, Chidgey M. Desmosome structure, composition and function. Biochim Biophys Acta. 2008;1778(3):572–587. PubMed
Breier G, Grosser M, Rezaei M. Endothelial cadherins in cancer. Cell Tissue Res. 2014;355(3):523–527. PubMed
Na TY, Schecterson L, Mendonsa AM, Gumbiner BM. The functional activity of E-cadherin controls tumor cell metastasis at multiple steps. Proc Natl Acad Sci U S A. 2020;117(11):5931–5937. PubMed PMC
Paredes J, Correia AL, Ribeiro AS, Albergaria A, Milanezi F, Schmitt FC. P-cadherin expression in breast cancer: a review. Breast Cancer Res. 2007;9(5):214. PubMed PMC
Albergaria A, Ribeiro AS, Vieira AF, Sousa B, Nobre AR, Seruca R, et al. P-cadherin role in normal breast development and cancer. Int J Dev Biol. 2011;55(7–9):811–822. PubMed
Ribeiro AS, Sousa B, Carreto L, Mendes N, Nobre AR, Ricardo S, et al. P-cadherin functional role is dependent on E-cadherin cellular context: a proof of concept using the breast cancer model. J Pathol. 2013;229(5):705–718. PubMed
Cameron D, Piccart-Gebhart MJ, Gelber RD, Procter M, Goldhirsch A, de Azambuja E, et al. 11 years’ follow-up of trastuzumab after adjuvant chemotherapy in HER2-positive early breast cancer: final analysis of the HERceptin Adjuvant (HERA) trial. Lancet. 2017;389(10075):1195–1205. PubMed PMC
Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas CF, Hynes NE. The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci U S A. 2003;100(15):8933–8938. PubMed PMC
Lee-Hoeflich ST, Crocker L, Yao E, Pham T, Munroe X, Hoeflich KP, et al. A central role for HER3 in HER2-amplified breast cancer: implications for targeted therapy. Cancer Res. 2008;68(14):5878–5887. PubMed
Lee Y, Ma J, Lyu H, Huang J, Kim A, Liu B. Role of erbB3 receptors in cancer therapeutic resistance. Acta Biochim Biophys Sin (Shanghai) 2014;46(3):190–198. PubMed
Xue C, Liang F, Mahmood R, Vuolo M, Wyckoff J, Qian H, et al. ErbB3-dependent motility and intravasation in breast cancer metastasis. Cancer Res. 2006;66(3):1418–1426. PubMed
Ocana A, Vera-Badillo F, Seruga B, Templeton A, Pandiella A, Amir E. HER3 overexpression and survival in solid tumors: a meta-analysis. J Natl Cancer Inst. 2013;105(4):266–273. PubMed
Lyu H, Han A, Polsdofer E, Liu S, Liu B. Understanding the biology of HER3 receptor as a therapeutic target in human cancer. Acta Pharm Sin B. 2018;8(4):503–510. PubMed PMC
Amin DN, Campbell MR, Moasser MM. The role of HER3, the unpretentious member of the HER family, in cancer biology and cancer therapeutics. Semin Cell Dev Biol. 2010;21(9):944–950. PubMed PMC
Ma J, Lyu H, Huang J, Liu B. Targeting of erbB3 receptor to overcome resistance in cancer treatment. Mol Cancer. 2014;13:105. PubMed PMC
Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, et al. NCBI GEO: archive for functional genomics data sets–update. Nucleic Acids Res. 2013;41(Database issue):D991–995. PubMed PMC