The role of adhesions between homologous cancer cells in tumor progression and targeted therapy

References

• Vader P, Mol EA, Pasterkamp G, et al. Extracellular vesicles for drug delivery. Adv Drug Deliv Rev. 2016;106(Pt A):148–156.
   PubMed Web of Science ®Google Scholar
• Fang RH, Jiang Y, Fang JC, et al. Cell membrane-derived nanomaterials for biomedical applications. Biomaterials. 2017;128:69–83.
   PubMed Web of Science ®Google Scholar
• Hockl PF, Wolosiuk A, Perez-Saez JM, et al. Glyco-nano-oncology: novel therapeutic opportunities by combining small and sweet. Pharmacol Res. 2016;109:45–54.
   PubMed Web of Science ®Google Scholar
• Kamiya K, Tsumoto K, Yoshimura T, et al. Cadherin-integrated liposomes with potential application in a drug delivery system. Biomaterials. 2011;32(36):9899–9907.
   PubMed Web of Science ®Google Scholar
• Orava EW, Abdul-Wahid A, Huang EH-B, et al. Blocking the attachment of cancer cells in vivo with DNA aptamers displaying anti-adhesive properties against the carcinoembryonic antigen. Mol Oncol. 2013;7(4):799–811.
   PubMed Web of Science ®Google Scholar
• Li D-M, Feng Y-M. Signaling mechanism of cell adhesion molecules in breast cancer metastasis: potential therapeutic targets. Breast Cancer Res Treat. 2011;128(1):7–21.
   PubMed Web of Science ®Google Scholar
• Wang M, Ning X, Chen A, et al. Impaired formation of homotypic cell-in-cell structures in human tumor cells lacking alpha-catenin expression. Sci Rep. 2015;5:12223.
   PubMed Web of Science ®Google Scholar
• Lin T-W, Chang H-T, Chen C-H, et al. Galectin-3 binding protein and galectin-1 interaction in breast cancer cell aggregation and metastasis. J Am Chem Soc. 2015;137(30):9685–9693.
   PubMed Web of Science ®Google Scholar
• Yoshioka T, Masuko T, Kotanagi H, et al. Homotypic adhesion through carcinoembryonic antigen plays a role in hepatic metastasis development. Jpn J Cancer Res. 1998;89(2):177–185.
   PubMedGoogle Scholar
• Batchelder CA, Martinez ML, Duru N, et al. Three dimensional culture of human renal cell carcinoma organoids. PLoS One. 2015;10(8):e0136758.
   PubMed Web of Science ®Google Scholar
• Puliafito A, De Simone A, Seano G, et al. Three-dimensional chemotaxis-driven aggregation of tumor cells. Sci Rep. 2015;5:15205.
   PubMed Web of Science ®Google Scholar
• Glinsky VV, Glinsky GV, Glinskii OV, et al. Intravascular metastatic cancer cell homotypic aggregation at the sites of primary attachment to the endothelium 1. Cancer Res. 2003;63(13):3805–3811.
   PubMed Web of Science ®Google Scholar
• Song H, Lacks DJ, Enmon RM, et al. Monte Carlo simulation of LNCaP human prostate cancer cell aggregation in liquid‐overlay culture. Biotechnol Prog. 1742-1749;19(6):2003.
   Google Scholar
• Zhao Q, Barclay M, Hilkens J, et al. Interaction between circulating galectin-3 and cancer-associated MUC1 enhances tumor cell homotypic aggregation and prevents anoikis. Mol Cancer. 2010;9(1):(1).
   Web of Science ®Google Scholar
• Saias L, Gomes A, Cazales M, et al. Cell–cell adhesion and cytoskeleton tension oppose each other in regulating tumor cell aggregation. Cancer Res. 2015;75(12):2426–2433.
   PubMed Web of Science ®Google Scholar
• Xin M, Dong X-W, Guo X-L. Role of the interaction between galectin-3 and cell adhesion molecules in cancer metastasis. Biomed Pharmacother. 2015;69:179–185.
   PubMed Web of Science ®Google Scholar
• Tang K, Zhang Y, Zhang H, et al. Delivery of chemotherapeutic drugs in tumor cell-derived microparticles. Nat Commun. 2012;3:1282.
   PubMed Web of Science ®Google Scholar
• Smyth T, Kullberg M, Malik N, et al. Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J Control Release. 2015;199:145–155.
   PubMed Web of Science ®Google Scholar
• Toledano Furman NE, Lupu-Haber Y, Bronshtein T, et al. Reconstructed stem cell nanoghosts: a natural tumor targeting platform. Nano Lett. 2013;13(7):3248–3255.
   PubMed Web of Science ®Google Scholar
• Zhu JY, Zheng DW, Zhang MK, et al. Preferential cancer cell self-recognition and tumor self-targeting by coating nanoparticles with homotypic cancer cell membranes. Nano Lett. 2016;16(9):5895–5901.
   PubMed Web of Science ®Google Scholar
• Molinaro R, Corbo C, Martinez JO, et al. Biomimetic proteolipid vesicles for targeting inflamed tissues. Nat Mater. 2016;15:1037–1046.
   PubMed Web of Science ®Google Scholar
• Guo Y, Wang D, Song Q, et al. Erythrocyte membrane-enveloped polymeric nanoparticles as nanovaccine for induction of antitumor immunity against melanoma. ACS Nano. 2015;9(7):6918–6933.
   PubMed Web of Science ®Google Scholar
• Piao J-G, Wang L, Gao F, et al. Erythrocyte membrane is an alternative coating to polyethylene glycol for prolonging the circulation lifetime of gold nanocages for photothermal therapy. ACS Nano. 2014;8(10):10414–10425.
   PubMed Web of Science ®Google Scholar
• Hu C-MJ, Fang RH, Wang K-C, et al. Nanoparticle biointerfacing by platelet membrane cloaking. Nature. 2015;526(7571):118–121.
   PubMed Web of Science ®Google Scholar
• Parodi A, Quattrocchi N, Van De Ven AL, et al. Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions. Nat Nanotechnol. 2013;8(1):61–68.
   PubMed Web of Science ®Google Scholar
• Wang N, Liu H, Hao J, et al. Single molecular recognition force spectroscopy study of a DNA aptamer with the target epithelial cell adhesion molecule. Analyst. 2015;140(18):6226–6229.
   PubMed Web of Science ®Google Scholar
• Alibolandi M, Ramezani M, Sadeghi F, et al. Epithelial cell adhesion molecule aptamer conjugated PEG-PLGA nanopolymersomes for targeted delivery of doxorubicin to human breast adenocarcinoma cell line in vitro. Int J Pharm. 2015;479(1):241–251.
   PubMed Web of Science ®Google Scholar
• Alibolandi M, Ramezani M, Abnous K, et al. In vitro and in vivo evaluation of therapy targeting epithelial-cell adhesion-molecule aptamers for non-small cell lung cancer. J Control Release. 2015;209:88–100.
   PubMed Web of Science ®Google Scholar
• Andree KC, Barradas AM, Nguyen AT, et al. Capture of tumor cells on Anti-EpCAM-functionalized Poly(acrylic acid)-coated surfaces. ACS Appl Mater Interfaces. 2016;8(23):14349–14356.
   PubMed Web of Science ®Google Scholar
• Ring A, Mineyev N, Zhu W, et al. EpCAM based capture detects and recovers circulating tumor cells from all subtypes of breast cancer except claudin-low. Oncotarget. 2015;6(42):44623–44634.
   PubMed Web of Science ®Google Scholar
• Nicolazzo C, Massimi I, Lotti LV, et al. Impact of chronic exposure to bevacizumab on EpCAM-based detection of circulating tumor cells. Chin J Cancer Res. 2015;27(5):491–496.
   PubMed Web of Science ®Google Scholar
• Winer-Jones JP, Vahidi B, Arquilevich N, et al. Circulating tumor cells: clinically relevant molecular access based on a novel CTC flow cell. PLoS One. 2014;9(1):e86717.
   PubMed Web of Science ®Google Scholar
• Smyth TJ, Redzic JS, Graner MW, et al. Examination of the specificity of tumor cell derived exosomes with tumor cells in vitro. Biochimica Et Biophysica Acta (Bba)-Biomembranes. 2014;1838(11):2954–2965.
   PubMed Web of Science ®Google Scholar
• Pessac B, Alliot F. [Mode of action of a diffusable factor facilitating cancer cell aggregation in vitro: effect at+ 6 degrees C. on mechanically dissociated cells]. Comptes Rendus Hebdomadaires Des Seances De L’academie Des Sciences. Serie D: Sciences Naturelles. 1969;269(6):755–758.
   PubMedGoogle Scholar
• Lubkov V, Bar-Sagi D. E-cadherin-mediated cell coupling is required for apoptotic cell extrusion. Curr Biol. 2014;24(8):868–874.
   PubMed Web of Science ®Google Scholar
• Slanchev K, Carney TJ, Stemmler MP, et al. The epithelial cell adhesion molecule EpCAM is required for epithelial morphogenesis and integrity during zebrafish epiboly and skin development. Plos Genet. 2009;5(7):e1000563.
   PubMed Web of Science ®Google Scholar
• Byers SW, Sommers CL, Hoxter B, et al. Role of E-cadherin in the response of tumor cell aggregates to lymphatic, venous and arterial flow: measurement of cell-cell adhesion strength. J Cell Sci. 1995;108(5):2053–2064.
   PubMed Web of Science ®Google Scholar
• Zhou H, Fuks A, Alcaraz G, et al. Homophilic adhesion between Ig superfamily carcinoembryonic antigen molecules involves double reciprocal bonds. J Cell Biol. 1993;122(4):951–960.
   PubMed Web of Science ®Google Scholar
• Peluso JJ, Pappalardo A, Trolice MP. N-cadherin-mediated cell contact inhibits granulosa cell apoptosis in a progesterone-independent manner. Endocrinology. 1996;137(4):1196–1203.
   PubMed Web of Science ®Google Scholar
• Szabó A, Varga K, Garay T, et al. Invasion from a cell aggregate—the roles of active cell motion and mechanical equilibrium. Phys Biol. 2012;9(1):016010.
   Web of Science ®Google Scholar
• Balzer EM, Konstantopoulos K. Intercellular adhesion: mechanisms for growth and metastasis of epithelial cancers. Wiley Interdiscip Reviews: Syst Biol Med. 2012;4(2):171–181.
   PubMed Web of Science ®Google Scholar
• Singh J, Hussain F, Decuzzi P. Role of differential adhesion in cell cluster evolution: from vasculogenesis to cancer metastasis. Comput Methods Biomech Biomed Engin. 2015;18(3):282–292.
   PubMed Web of Science ®Google Scholar
• Chen A, Beetham H, Black MA, et al. E-cadherin loss alters cytoskeletal organization and adhesion in non-malignant breast cells but is insufficient to induce an epithelial-mesenchymal transition. BMC Cancer. 2014;14:552.
   PubMed Web of Science ®Google Scholar
• Mărgineanu E, Cotrutz C, Cotrutz C. Correlation between E-cadherin abnormal expressions in different types of cancer and the process of metastasis. Rev Med Chir Soc Med Nat Iasi. 2007;112(2):432–436.
   Google Scholar
• Quattrocchi L, Green AR, Martin S, et al. The cadherin switch in ovarian high-grade serous carcinoma is associated with disease progression. Virchows Archiv. 2011;459(1):21–29.
   PubMed Web of Science ®Google Scholar
• Gagliardi G, Kandemir O, Guida M, et al. Changes in E-cadherin immunoreactivity in the adenoma-carcinoma sequence of the large bowel. Virchows Archiv. 1995;426(2):149–154.
   PubMed Web of Science ®Google Scholar
• Li B, Shi H, Wang F, et al. Expression of E-, P-and N-Cadherin and its clinical significance in cervical squamous cell carcinoma and precancerous lesions. PLoS One. 2016;11(5):e0155910.
   Web of Science ®Google Scholar
• Zhang J, Li N, Bai W, et al. Notch ligand Delta-like 1 promotes the metastasis of melanoma by enhancing tumor adhesion. Braz J Med Biol Res. 2014;47(4):299–306.
   PubMed Web of Science ®Google Scholar
• Wai Wong C, Dye DE, Coombe DR. The role of immunoglobulin superfamily cell adhesion molecules in cancer metastasis. Int J Cell Biol. 2012;340296:2012.
   Google Scholar
• Mourtzikou A, Stamouli M, Kroupis C, et al. Evaluation of carcinoembryonic antigen (CEA), epidermal growth factor receptor (EGFR), epithelial cell adhesion molecule EpCAM (GA733-2), and carbohydrate antigen 19-9 (CA 19-9) levels in colorectal cancer patients and correlation with clinicopathological characteristics. Clin Lab. 2012;58(5–6):441–448.
   PubMed Web of Science ®Google Scholar
• Chui MH. Insights into cancer metastasis from a clinicopathologic perspective: epithelial-mesenchymal transition is not a necessary step. Int J Cancer. 2013;132(7):1487–1495.
   PubMed Web of Science ®Google Scholar
• Kioi M, Yamamoto K, Higashi S, et al. Matrilysin (MMP-7) induces homotypic adhesion of human colon cancer cells and enhances their metastatic potential in nude mouse model. Oncogene. 2003;22(54):8662–8670.
   PubMed Web of Science ®Google Scholar
• Yamamoto K, Higashi S, Kioi M, et al. Binding of active matrilysin to cell surface cholesterol sulfate is essential for its membrane-associated proteolytic action and induction of homotypic cell adhesion. J Biol Chem. 2006;281(14):9170–9180.
   PubMed Web of Science ®Google Scholar
• Steuer AF, Rhim JS, Hentosh PM, et al. Survival of human cells in the aggregate form: potential index of in vitro cell transformation. J Natl Cancer Inst. 1977;58(4):917–921.
   PubMedGoogle Scholar
• Zhong X, Rescorla FJ. Cell surface adhesion molecules and adhesion-initiated signaling: understanding of anoikis resistance mechanisms and therapeutic opportunities. Cell Signal. 2012;24(2):393–401.
   PubMed Web of Science ®Google Scholar
• Zhang ZY, Ge HY. Micrometastasis in gastric cancer. Cancer Lett. 2013;336(1):34–45.
   PubMed Web of Science ®Google Scholar
• Musrap N, Tuccitto A, Karagiannis GS, et al. Comparative proteomics of ovarian cancer aggregate formation reveals an increased expression of calcium-activated chloride channel regulator 1 (CLCA1). J Biol Chem. 2015;290(28):17218–17227.
   PubMed Web of Science ®Google Scholar
• Ko SY, Naora H. HOXA9 promotes homotypic and heterotypic cell interactions that facilitate ovarian cancer dissemination via its induction of P-cadherin. Mol Cancer. 2014;13:170.
   PubMed Web of Science ®Google Scholar
• Usui A, Ko SY, Barengo N, et al. P-cadherin promotes ovarian cancer dissemination through tumor cell aggregation and tumor-peritoneum interactions. Mol Cancer Res. 2014;12(4):504–513.
   PubMed Web of Science ®Google Scholar
• Thielecke H, Mack A, Robitzki A. A multicellular spheroid-based sensor for anti-cancer therapeutics. Biosens Bioelectron. 2001;16(4):261–269.
   PubMed Web of Science ®Google Scholar
• Vessey CJ, Wilding J, Folarin N, et al. Altered expression and function of E‐cadherin in cervical intraepithelial neoplasia and invasive squamous cell carcinoma. J Pathol. 1995;176(2):151–159.
   PubMed Web of Science ®Google Scholar
• Wada J, Makino H. Galectins, galactoside-binding mammalian lectins: clinical application of multi-functional proteins. Acta Medica Okayama. 2001;55(1):11–17.
   PubMed Web of Science ®Google Scholar
• Aomatsu E, Chosa N, Nishihira S, et al. Cell-cell adhesion through N-cadherin enhances VCAM-1 expression via PDGFRbeta in a ligand-independent manner in mesenchymal stem cells. Int J Mol Med. 2014;33(3):565–572.
   PubMed Web of Science ®Google Scholar
• Cavallaro U, Christofori G. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer. 2004;4(2):118–132.
   PubMed Web of Science ®Google Scholar
• Saussez S, Glinoer D, Chantrain G, et al. Serum galectin-1 and galectin-3 levels in benign and malignant nodular thyroid disease. Thyroid. 2008;18(7):705–712.
   PubMed Web of Science ®Google Scholar
• Aggarwal S, Sharma SC, Das SN. Galectin-1 and galectin-3: plausible tumor markers for oral squamous cell carcinoma and suitable targets for screening high-risk population. Clin Chim Acta. 2015;442:13–21.
   PubMed Web of Science ®Google Scholar
• Fang RH, Hu C-MJ, Luk BT, et al. Cancer cell membrane-coated nanoparticles for anticancer vaccination and drug delivery. Nano Lett. 2014;14(4):2181–2188.
   PubMed Web of Science ®Google Scholar
• Rao L, Bu LL, Cai B, et al. Cancer cell membrane‐coated upconversion nanoprobes for highly specific tumor imaging. Adv Mater. 2016;28(18):3460–3466.
   PubMed Web of Science ®Google Scholar
• Sun H, Su J, Meng Q, et al. Cancer-Cell-Biomimetic nanoparticles for targeted therapy of homotypic tumors. Adv Mater. 2016;28(43):9581–9588.
   PubMed Web of Science ®Google Scholar
• Riethdorf S, Fritsche H, Muller V, et al. Detection of circulating tumor cells in peripheral blood of patients with metastatic breast cancer: a validation study of the CellSearch system. Clin Cancer Res. 2007;13(3):920–928.
   PubMed Web of Science ®Google Scholar
• Konigsberg R, Gneist M, Jahn-Kuch D, et al. Circulating tumor cells in metastatic colorectal cancer: efficacy and feasibility of different enrichment methods. Cancer Lett. 2010;293(1):117–123.
   PubMed Web of Science ®Google Scholar
• Nardone V, Lucarelli AP, Dalle Vedove A, et al. Crystal structure of human E-Cadherin-EC1EC2 in complex with a peptidomimetic competitive inhibitor of cadherin homophilic interaction. J Med Chem. 2016;59(10):5089–5094.
   PubMed Web of Science ®Google Scholar
• Kallergi G, Papadaki MA, Politaki E, et al. Epithelial to mesenchymal transition markers expressed in circulating tumor cells of early and metastatic breast cancer patients. Breast Cancer Res. 2011;13(3):R59.
   PubMed Web of Science ®Google Scholar