Semaphorins: novel insights on their emerging multifaceted roles in the evolving landscape of breast cancer

Authors

  • Ts. Popov Clinic of Surgery, University Hospital “Alexandrovska”, Sofia, Bulgaria, Department of Surgery, Faculty of Medicine, Medical University – Sofia, Bulgaria Author

DOI:

https://doi.org/10.2478/AMB-2024-0065

Keywords:

semaphorins, breast cancer, treatment, diagnosis, immunology

Abstract

Semaphorins, initially identified as phylogenetically conserved axon guidance molecules, comprise an extracellular signaling protein family involved in various biological events that regulate the development, tissue homeostasis and cancer progression of many 
organ systems. In recent years, the focus of research has expanded to investigate the roles of semaphorins in cancer. Semaphorins have emerged as crucial regulators in the pathogenesis of breast cancer (BCa). This review article aims to provide an overview of the contemporary knowledge regarding semaphorins, their diverse tumor-modulating properties, and their clinical application in BCa. Specifically, six semaphorins (SEMA3C, SEMA3E, SEMA4A, SEMA4C, SEMA4D, and SEMA7A) have been demonstrated to promote tumor progression in terms of BCa. Six additional members (SEMA3A, SEMA3B, SEMA3F, SEMA4B, SEMA6B, and SEMA6D) have been associated with tumor suppression. Several semaphorins (SEMA4C and SEMA7A) are considered putative diagnostic and prognostic 
biomarkers in BCa. Exploring and elucidating the intricate functions of semaphorins and their viability as therapeutic targets is an intriguing avenue of research that can improve BCa outcomes.

References

Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021 May;71(3):209-249.

Valerianova Z., Atanasov T. (editors). Cancer Incidence in Bulgaria, 2016 & 2017, Volume XXVI. Bulgarian National Cancer Registry. Sofia, Publisher “Paradigma“, Sofia, 2020.

Perou CM, Sørlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature. 2000 Aug 17;406(6797):747-52.

Orrantia-Borunda E, Anchondo-Nuñez P, Acuña-Aguilar LE, et al. Subtypes of Breast Cancer. In: Mayrovitz HN, editor. Breast Cancer [Internet]. Brisbane (AU): Exon Publications; 2022 Aug 6. Chapter 3.

Sarhangi, N., Hajjari, S., Heydari, S. F., et al. Breast cancer in the era of precision medicine. Molecular biology reports, 2022, 49(10), 10023–10037.

Aiyappa-Maudsley R, McLoughlin LFV, Hughes TA. Semaphorins and Their Roles in Breast Cancer: Implications for Therapy Resistance. International Journal of Molecular Sciences. 2023; 24(17):13093.

Alto, L. T. Terman, J. R. Semaphorins and their Signaling Mechanisms. Methods in molecular biology (Clifton, N.J.), 2017, 1493, 1–25.

Fard D, Tamagnone L. Semaphorins in health and disease. Cytokine Growth Factor Rev. 2021 Feb;57:55-63.

Yazdani U, Terman JR. The semaphorins. Genome Biol. 2006;7(3):211.

Roth L, Koncina E, Satkauskas S, et al. The many faces of semaphorins: from development to pathology. Cell Mol Life Sci. 2009 Feb;66(4):649-66.

Thomas R, Yang X. Semaphorins in immune cell function, inflammatory and infectious diseases. Curr Res Immunol. 2023 May 31;4:100060.

Mastrantonio R, You H, Tamagnone L. Semaphorins as emerging clinical biomarkers and therapeutic targets in cancer. Theranostics. 2021 Jan 15;11(7):3262-3277.

Toledano S, Neufeld G. Plexins as Regulators of Cancer Cell Proliferation, Migration, and Invasivity. Cancers (Basel). 2023 Aug 10;15(16):4046.

Niland S, Eble JA. Neuropilins in the Context of Tumor Vasculature. Int J Mol Sci. 2019 Feb 1;20(3):639.

Neufeld G, Mumblat Y, Smolkin T, et al. The role of the semaphorins in cancer. Cell Adh Migr. 2016 Nov;10(6):652-674.

Niland S, Eble JA. Neuropilin: Handyman and Power Broker in the Tumor Microenvironment. Adv Exp Med Biol. 2020; 1223:31-67.

Battistini C, Tamagnone L. Transmembrane semaphorins, forward and reverse signaling: have a look both ways. Cell Mol Life Sci. 2016 Apr;73(8):1609-22.

Ahammad I. A comprehensive review of tumor proliferative and suppressive role of semaphorins and therapeutic approaches. Biophys Rev. 2020 Oct;12(5):1233-1247.

Jiang J, Zhang F, Wan Y, et al. Semaphorins as Potential Immune Therapeutic Targets for Cancer. Front Oncol. 2022 Jan 27;12:793805.

Soysal SD, Tzankov A, Muenst SE. Role of the Tumor Microenvironment in Breast Cancer. Pathobiology. 2015 Sep;82(3-4):142-52.

Capparuccia L, Tamagnone L. Semaphorin signaling in cancer cells and in cells of the tumor microenvironment-two sides of a coin. J Cell Sci. 2009 Jun 1;122(Pt 11):1723-36.

Franzolin G, Tamagnone L. Semaphorin Signaling in Cancer-Associated Inflammation. Int J Mol Sci. 2019 Jan 17;20(2):377.

Chen LH, Cuang EY. Importance of semaphorins in cancer immunity. Transl Lung Cancer Res. 2019 Dec;8(Suppl 4):S468-S470.

Rehman M, Tamagnone L. Semaphorins in cancer: biological mechanisms and therapeutic approaches. Semin Cell Dev Biol. 2013 Mar;24(3):179-89.

Solinas G, Germano G, Mantovani A, et al. Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol. 2009 Nov;86(5):1065-73.

Eissler N, Rolny C. The role of immune semaphorins in cancer progression. Exp Cell Res. 2013 Jul 1;319(11):1635-43.

Szebeni GJ, Vizler C, Kitajka K, et al. Inflammation and Cancer: Extra- and Intracellular Determinants of Tumor-Associated Macrophages as Tumor Promoters. Mediators Inflamm. 2017;2017:9294018.

Hao J, Yu JS. Semaphorin 3C and Its Receptors in Cancer and Cancer Stem-Like Cells. Biomedicines. 2018 Apr 8;6(2):42.

Bhasin S, Dusek C, Peacock JW, et al. Dependency of Tamoxifen Sensitive and Resistant ER+ Breast Cancer Cells on Semaphorin 3C (SEMA3C) for Growth. Cells. 2023 Jun 25;12(13):1715.

Miyato H, Tsuno NH, Kitayama J. Semaphorin 3C is involved in the progression of gastric cancer. Cancer Sci. 2012 Nov;103(11):1961-6.

Liu R, Shuai Y, Luo J, et al. SEMA3C Promotes Cervical Cancer Growth and Is Associated With Poor Prognosis. Front Oncol. 2019 Oct 9;9:1035.

Hui DHF, Tam KJ, Jiao IZF, et al. Semaphorin 3C as a Therapeutic Target in Prostate and Other Cancers. Int J Mol Sci. 2019 Feb 12;20(3):774.

Zhang D, Lindstrom A, Kim EJ, et al. SEMA3C Supports Pancreatic Cancer Progression by Regulating the Autophagy Process and Tumor Immune Microenvironment. Front Oncol. 2022 Jun 16;12:890154.

Peacock JW, Takeuchi A, Hayashi N, et al. SEMA3C drives cancer growth by transactivating multiple receptor tyrosine kinases via Plexin B1. EMBO Mol Med. 2018 Feb;10(2):219-238.

Vaitkienė P, Skiriutė D, Steponaitis G, et al. High level of Sema3C is associated with glioma malignancy. Diagn Pathol. 2015 Jun 2;10:58.

Cole-Healy Z, Vergani P, Hunter K, et al. The relationship between semaphorin 3C and microvessel density in the progression of breast and oral neoplasia. Exp Mol Pathol. 2015 Aug;99(1):19-24.

Malik MF, Satherley LK, Davies EL, et al. Expression of Semaphorin 3C in Breast Cancer and its Impact on Adhesion and Invasion of Breast Cancer Cells. Anticancer Res. 2016 Mar;36(3):1281-6.

Valdembri D, Regano D, Maione F, et al. Class 3 semaphorins in cardiovascular development. Cell Adh Migr. 2016 Nov;10(6):641-651.

Haider MT, Saito H, Zarrer J, et al. Breast cancer bone metastases are attenuated in a Tgif1-deficient bone microenvironment. Breast Cancer Res. 2020 Apr 9;22(1):34.

Christensen C, Ambartsumian N, Gilestro G, et al. Proteolytic processing converts the repelling signal Sema3E into an inducer of invasive growth and lung metastasis. Cancer Res. 2005 Jul 15;65(14):6167-77.

Casazza A, Finisguerra V, Capparuccia L, et al. Sema3E-Plexin D1 signaling drives human cancer cell invasiveness and metastatic spreading in mice. J Clin Invest. 2010 Aug;120(8):2684-98.

Luchino J, Hocine M, Amoureux MC, et al. Semaphorin 3E suppresses tumor cell death triggered by the plexin D1 dependence receptor in metastatic breast cancers. Cancer Cell. 2013 Nov 11;24(5):673-85.

Casazza A, Kigel B, Maione F, et al. Tumour growth inhibition and anti-metastatic activity of a mutated furin-resistant Semaphorin 3E isoform. EMBO Mol Med. 2012 Mar;4(3):234-50.

Wang Y, Shi L, Li J, et al. Long-term cadmium exposure promoted breast cancer cell migration and invasion by up-regulating TGIF. Ecotoxicol Environ Saf. 2019 Jul 15;175:110-117.

Iyer AS, Chapoval SP. Neuroimmune Semaphorin 4A in Cancer Angiogenesis and Inflammation: A Promoter or a Suppressor? Int J Mol Sci. 2018 Dec 30;20(1):124

Rajabinejad M, Asadi G, Ranjbar S, et al. Semaphorin 4A, 4C, and 4D: Function comparison in the autoimmunity, allergy, and cancer. Gene. 2020 Jul 1;746:144637.

Liu X, Sun Y, Tian W, et al. Sema4A Responds to Hypoxia and Is Involved in Breast Cancer Progression. Biol Pharm Bull. 2018 Dec 1;41(12):1791-1796.

Chen H., Gao C., Wang L. et al. The expression and clinical significance of sema4a in triple negative breast cancer. J. Clin. Nurs. Res. 2020, 4, 4–7.

Paranthaman P, Veerappapillai S. Design of a potential Sema4A-based multi-epitope vaccine to combat triple-negative breast cancer: an immunoinformatic approach. Med Oncol. 2023 Feb 23;40(3):105.

Huayi Li, Xin Li, Sen Xu, et al. Semaphorin 4C accelerates disease progression and enables disease detection in breast cancer. Vis Cancer Med 2023, 4 6

Gurrapu, S., Pupo, E., Franzolin, G., et al. Sema4C/PlexinB2 signaling controls breast cancer cell growth, hormonal dependence and tumorigenic potential. Cell death and differentiation, 2018, 25(7), 1259–1275.

Ye SM, Han M, Kan CY, et al. [Expression and clinical significance of Sema4C in esophageal cancer, gastric cancer and rectal cancer]. Zhonghua Yi Xue Za Zhi. 2012 Jul 24;92(28):1954-8.

Huang S, Han S, Zhang J, et al. Semaphorin-4C is upregulated in epithelial ovarian cancer. Oncol Lett. 2020 Apr;19(4):3333-3338.

Jing L, Bo W, Yourong F, et al. Sema4C mediates EMT inducing chemotherapeutic resistance of miR-31-3p in cervical cancer cells. Sci Rep. 2019 Nov 27;9(1):17727.

Hou Y, Wang W, Zeng Z, et al. High SEMA4C expression promotes the epithelial-mesenchymal transition and predicts poor prognosis in colorectal carcinoma. Aging (Albany NY). 2020 Nov 7;12(21):21992-22018.

Smeester BA, Slipek NJ, Pomeroy EJ, et al. SEMA4C is a novel target to limit osteosarcoma growth, progression, and metastasis. Oncogene. 2020 Jan;39(5):1049-1062.

Wei JC, Yang J, Liu D, et al. Tumor-associated Lymphatic Endothelial Cells Promote Lymphatic Metastasis By Highly Expressing and Secreting SEMA4C. Clin Cancer Res. 2017 Jan 1;23(1):214-224.

Yang J, Zeng Z, Qiao L, et al. Semaphorin 4C Promotes Macrophage Recruitment and Angiogenesis in Breast Cancer. Mol Cancer Res. 2019 Oct;17(10):2015-2028.

Gurrapu S, Franzolin G, Fard D, et al. Reverse signaling by semaphorin 4C elicits SMAD1/5- and ID1/3-dependent invasive reprogramming in cancer cells. Sci Signal. 2019 Aug 20; 12(595):eaav2041.

Liu H, Ye H, Li X. Effect of microrna-138 on epithelial-Mesenchymal transition and invasion of breast cancer cells by targeting semaphorin 4C. Bioengineered. 2021 Dec;12(2):10117-10125.

Yang Q, Wang Y, Lu X, et al. MiR-125b regulates epithelial-mesenchymal transition via targeting Sema4C in paclitaxel-resistant breast cancer cells. Oncotarget. 2015 Feb 20;6(5):3268-79.

Wang Y, Qiao L, Yang J, et al. Serum semaphorin 4C as a diagnostic biomarker in breast cancer: A multicenter retrospective study. Cancer Commun (Lond). 2021 Dec;41(12):1373-1386.

Wang Y, Liu J, Li J, et al. Serum semaphorin4C as an auxiliary diagnostic biomarker for breast cancer. Clin Transl Med. 2021 Aug; 11(8):e480.

Jiang H, Chen C, Sun Q, et al. The role of semaphorin 4D in tumor development and angiogenesis in human breast cancer. Onco Targets Ther. 2016 Sep 26;9:5737-5750.

Yang YH, Buhamrah A, Schneider A, et al. Semaphorin 4D Promotes Skeletal Metastasis in Breast Cancer. PLoS One. 2016 Feb 24;11(2):e0150151.

Lontos K, Adamik J, Tsagianni A, et al. The Role of Semaphorin 4D in Bone Remodeling and Cancer Metastasis. Front Endocrinol (Lausanne). 2018 Jun 19; 9:322.

Göbel A, Kuhlmann JD, Link T, et al. Plasma levels of Semaphorin 4D are decreased by adjuvant tamoxifen but not aromatase inhibitor therapy in breast cancer patients. J Bone Oncol. 2019 Apr 4; 16:100237.

Klotz R, Thomas A, Teng T, et al. Circulating Tumor Cells Exhibit Metastatic Tropism and Reveal Brain Metastasis Drivers. Cancer Discov. 2020 Jan;10(1):86-103.

Evans EE, Jonason AS Jr, Bussler H, et al. Antibody Blockade of Semaphorin 4D Promotes Immune Infiltration into Tumor and Enhances Response to Other Immunomodulatory Therapies. Cancer Immunol Res. 2015 Jun;3(6):689-701.

Clavijo PE, Friedman J, Robbins Y, et al. Semaphorin4D Inhibition Improves Response to Immune-Checkpoint Blockade via Attenuation of MDSC Recruitment and Function. Cancer Immunol Res. 2019 Feb;7(2):282-291.

Patnaik A, Weiss GJ, Leonard JE, et al. Safety, Pharmacokinetics, and Pharmacodynamics of a Humanized Anti-Semaphorin 4D Antibody, in a First-In-Human Study of Patients with Advanced Solid Tumors. Clin Cancer Res. 2016 Feb 15;22(4):827-36.

Shafique MR, Fisher TL, Evans EE, et al. A Phase Ib/II Study of Pepinemab in Combination with Avelumab in Advanced Non-Small Cell Lung Cancer. Clin Cancer Res. 2021 Jul 1;27(13):3630-3640.

Garcia-Areas R, Libreros S, Amat S, et al. Semaphorin7A promotes tumor growth and exerts a pro-angiogenic effect in macrophages of mammary tumor-bearing mice. Front Physiol. 2014 Feb 5; 5:17.

Song Y, Wang L, Zhang L, et al. The involvement of semaphorin 7A in tumorigenic and immunoinflammatory regulation. J Cell Physiol. 2021 Sep; 236(9):6235-6248.

Black SA, Nelson AC, Gurule NJ, et al. Semaphorin 7a exerts pleiotropic effects to promote breast tumor progression. Oncogene. 2016 Sep 29;35(39):5170-8.

Garcia-Areas R, Libreros S, Simoes M, et al. Suppression of tumor-derived Semaphorin 7A and genetic ablation of hostderived Semaphorin 7A impairs tumor progression in a murine model of advanced breast carcinoma. Int J Oncol. 2017 Nov;51(5):1395-1404.

Dai Y, Zhang X, Ou Y, et al. Anoikis resistance-protagonists of breast cancer cells survive and metastasize after ECM detachment. Cell Commun Signal. 2023 Aug 3;21(1):190.

Rutherford TR, Elder AM, Lyons TR. Anoikis resistance in mammary epithelial cells is mediated by semaphorin 7a. Cell Death Dis. 2021 Sep 24;12(10):872.

Crump LS, Wyatt GL, Rutherford TR, et al. Hormonal Regulation of Semaphorin 7a in ER+ Breast Cancer Drives Therapeutic Resistance. Cancer Res. 2021 Jan 1;81(1):187-198.

Borges VF, Hu J, Young C, et al. Semaphorin 7a is a biomarker for recurrence in postpartum breast cancer. NPJ Breast Cancer. 2020 Oct 19; 6:56.

Wallerius M, Wallmann T, Bartish M, et al. Guidance Molecule SEMA3A Restricts Tumor Growth by Differentially Regulating

the Proliferation of Tumor-Associated Macrophages. Cancer Res. 2016 Jun 1;76(11):3166-78.

Lee J, Shin YJ, Lee K, et al. Anti-SEMA3A Antibody: A Novel Therapeutic Agent to Suppress Glioblastoma Tumor Growth. Cancer Res Treat. 2018 Jul;50(3):1009-1022.

Liu F, Wang C, Huang H, et al. SEMA3A-mediated crosstalk between prostate cancer cells and tumor-associated macrophages promotes androgen deprivation therapy resistance. Cell Mol Immunol. 2021 Mar;18(3):752-754.

De Vlaeminck Y, Bonelli S, Awad RM, et al. Targeting Neuropilin-1 with Nanobodies Reduces Colorectal Carcinoma Development. Cancers (Basel). 2020 Nov 30;12(12):3582.

Shen WW, Chen WG, Liu FZ, et al. Breast cancer cells promote osteoblastic differentiation via Sema 3A signaling pathway in vitro. Int J Clin Exp Pathol. 2015 Feb 1;8(2):1584-93.

Mishra R, Thorat D, Soundararajan G, et al. Semaphorin 3A upregulates FOXO 3a-dependent MelCAM expression leading to attenuation of breast tumor growth and angiogenesis. Oncogene. 2015 Mar 19;34(12):1584-95.

Gioelli N, Maione F, Camillo C, et al. A rationally designed NRP1-independent superagonist SEMA3A mutant is an effective anticancer agent. Sci Transl Med. 2018 May 23;10(442):eaah4807.

Müller MW, Giese NA, Swiercz JM, et al. Association of axon guidance factor semaphorin 3A with poor outcome in pancreatic cancer. Int J Cancer. 2007 Dec 1;121(11):2421-33.

Wang Z, Chen J, Zhang W, et al. Axon guidance molecule semaphorin3A is a novel tumor suppressor in head and neck squamous cell carcinoma. Oncotarget. 2016 Feb 2;7(5):6048-62.

Vadasz Z, Rubinstein J, Bejar J, et al. Overexpression of semaphorin 3A in patients with urothelial cancer. Urol Oncol. 2018 Apr; 36(4):161.e1-161.e6.

Lavi N, Kessler O, Ziv K, et al. Semaphorin-3A inhibits multiple myeloma progression in a mouse model. Carcinogenesis. 2018 Oct 8; 39(10):1283-1291.

Jiang H, Qi L, Wang F, et al. Decreased semaphorin 3A expression is associated with a poor prognosis in patients with epithelial ovarian carcinoma. Int J Mol Med. 2015 May;35(5):1374-80.

Casazza A, Fu X, Johansson I, et al. Systemic and targeted delivery of semaphorin 3A inhibits tumor angiogenesis and progression in mouse tumor models. Arterioscler Thromb Vasc Biol. 2011 Apr;31(4):741-9.

Tang C, Gao X, Liu H, et al. Decreased expression of SEMA3A is associated with poor prognosis in gastric carcinoma. Int J Clin Exp Pathol. 2014;7:4782-94.

Zhang X, Klamer B, Li J, et al. A pan-cancer study of class-3 semaphorins as therapeutic targets in cancer. BMC Med Genomics. 2020 Apr 3;13(Suppl 5):45.

Harburg GC, Hinck L. Navigating breast cancer: axon guidance molecules as breast cancer tumor suppressors and oncogenes. J Mammary Gland Biol Neoplasia. 2011 Sep;16(3):257-70.

Pan H, Wanami LS, Dissanayake TR, et al. Autocrine semaphorin3A stimulates alpha2 beta1 integrin expression/function in breast tumor cells. Breast Cancer Res Treat. 2009 Nov;118(1):197-205.

Butti R, Kumar TV, Nimma R, et al. Impact of semaphorin expression on prognostic characteristics in breast cancer. Breast Cancer (Dove Med Press). 2018 May 31;10:79-88.

Maione F, Capano S, Regano D, et al. Semaphorin 3A overcomes cancer hypoxia and metastatic dissemination induced by antiangiogenic treatment in mice. J Clin Invest. 2012 May;122(5):1832-48.

Castro-Rivera E, Ran S, Brekken RA, Minna JD. Semaphorin 3B inhibits the phosphatidylinositol 3-kinase/Akt pathway through neuropilin-1 in lung and breast cancer cells. Cancer Res. 2008 Oct 15;68(20):8295-303.

Tomizawa Y, Sekido Y, Kondo M, et al. Inhibition of lung cancer cell growth and induction of apoptosis after reexpression of 3p21.3 candidate tumor suppressor gene SEMA3B. Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13954-9.

Hu J, Huang H, Xi Z, et al. LncRNA SEMA3B-AS1 inhibits breast cancer progression by targeting miR-3940/KLLN axis. Cell Death Dis. 2022 Sep 19;13(9):800.

Jiao Y, Li S, Wang X, et al. A genomic instability-related lncRNA model for predicting prognosis and immune checkpoint inhibitor efficacy in breast cancer. Front Immunol. 2022 Aug 5; 13:929846.

Li X, Li Y, Yu X, et al. Identification and validation of stemness-related lncRNA prognostic signature for breast cancer. J Transl Med. 2020 Aug 31;18(1):331.

Nasarre P, Kusy S, Constantin B, et al. Semaphorin SEMA3F has a repulsing activity on breast cancer cells and inhibits E-cadherin-mediated cell adhesion. Neoplasia. 2005 Feb;7(2):180-9.

Wang C, Song D, Huang Q, et al. Advances in SEMA3F regulation of clinically high-incidence cancers. Cancer Biomark. 2023;38(2):131-142.

Tamagnone L. Emerging role of semaphorins as major regulatory signals and potential therapeutic targets in cancer. Cancer Cell. 2012 Aug 14;22(2):145-52.

Xiong G, Wang C, Evers BM, et al. RORα suppresses breast tumor invasion by inducing SEMA3F expression. Cancer Res. 2012 Apr 1; 72(7):1728-39.

Jiang J, Lu Y, Zhang F, et al. Semaphorin 4B promotes tumor progression and associates with immune infiltrates in lung adenocarcinoma. BMC Cancer. 2022 Jun 8;22(1):632.

Wang X, Jian W, Luo Q, et al. CircSEMA4B inhibits the progression of breast cancer by encoding a novel protein SEMA4B-211aa and regulating AKT phosphorylation. Cell Death Dis. 2022 Sep 17;13(9):794.

Lei Q, Wang Y, Li J, et al. Increased SEMA6B expression as a potential prognostic and immune cell infiltration biomarker in thyroid cancer patients. Aging (Albany NY). 2023 May 5;15(9):3572-3585.

D’Apice L, Costa V, Valente C, et al. Analysis of SEMA6B gene expression in breast cancer: identification of a new isoform. Biochim Biophys Acta. 2013 Oct;1830(10):4543-53.

Gunyuz ZE, Sahi-Ilhan E, Kucukkose C, et al. SEMA6D Differentially Regulates Proliferation, Migration, and Invasion of Breast Cell Lines. ACS Omega. 2022 Apr 27;7(18):15769-15778.

Baxter DE, Allinson LM, Al Amri WS, et al. MiR-195 and Its Target SEMA6D Regulate Chemoresponse in Breast Cancer. Cancers (Basel). 2021 Nov 28;13(23):5979.

Chen D, Li Y, Wang L, et al. SEMA6D Expression and Patient Survival in Breast Invasive Carcinoma. Int J Breast Cancer. 2015; 2015:539721.

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Published

04.10.2024

How to Cite

Popov, T. (2024). Semaphorins: novel insights on their emerging multifaceted roles in the evolving landscape of breast cancer. Acta Medica Bulgarica, 51(Suppl 2), 153-164. https://doi.org/10.2478/AMB-2024-0065