Glycan-Lectin interactions between platelets and tumor cells drive hematogenous metastasis

References

• Lee CH, Lin Y-J, Lin C-C, Yen C-L, Shen C-H, Chang C-J, Hsieh S-Y. Pretreatment platelet count early predicts extrahepatic metastasis of human hepatoma. Liver Int. 2015;35(10):2327–10. doi:10.1111/liv.12817.
   PubMed Web of Science ®Google Scholar
• Haemmerle M, Stone RL, Menter DG, Afshar-Kharghan V, Sood AK. The platelet lifeline to cancer: challenges and opportunities. Cancer Cell. 2018;33(6):965–83. doi:10.1016/j.ccell.2018.03.002.
   PubMed Web of Science ®Google Scholar
• Gong L, Cai Y, Zhou X, Yang H. Activated platelets interact with lung cancer cells through P-selectin glycoprotein ligand-1. Pathol Oncol Res. 2012;18(4):989–96. doi:10.1007/s12253-012-9531-y.
   PubMed Web of Science ®Google Scholar
• Suzuki-Inoue K, Kato Y, Inoue O, Kaneko MK, Mishima K, Yatomi Y, Yamazaki Y, Narimatsu H, Ozaki Y. Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J Biol Chem. 2007;282(36):25993–6001. doi:10.1074/jbc.M702327200.
   PubMed Web of Science ®Google Scholar
• Mammadova-Bach E, Gil-Pulido J, Sarukhanyan E, Burkard P, Shityakov S, Schonhart C, Stegner D, Remer K, Nurden P, Nurden AT, et al. Platelet glycoprotein VI promotes metastasis through interaction with cancer cell-derived galectin-3. Blood. 2020;135(14):1146–60. doi:10.1182/blood.2019002649.
   PubMed Web of Science ®Google Scholar
• Morimoto K, Satoh-Yamaguchi K, Hamaguchi A, Inoue Y, Takeuchi M, Okada M, Ikeda W, Takai Y, Imai T. Interaction of cancer cells with platelets mediated by Necl-5/poliovirus receptor enhances cancer cell metastasis to the lungs. Oncogene. 2008;27(3):264–73. doi:10.1038/sj.onc.1210645.
   PubMed Web of Science ®Google Scholar
• Cummings RD, Pierce JM. The challenge and promise of glycomics. Chem Biol. 2014;21(1):1–15. doi:10.1016/j.chembiol.2013.12.010.
   PubMedGoogle Scholar
• Lin S, Zhou S, Yuan T. The “sugar-coated bullets” of cancer: tumor-derived exosome surface glycosylation from basic knowledge to applications. Clin Transl Med. 2020;10(6):e204. doi:10.1002/ctm2.204.
   PubMed Web of Science ®Google Scholar
• Pinho SS, Reis CA. Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer. 2015;15(9):540–555. doi:10.1038/nrc3982.
   PubMed Web of Science ®Google Scholar
• Wang M, Zhu J, Lubman DM, Gao C. Aberrant glycosylation and cancer biomarker discovery: a promising and thorny journey. Clin Chem Lab Med. 2019;57(4):407–16. doi:10.1515/cclm-2018-0379.
   PubMed Web of Science ®Google Scholar
• Gratacós-Mulleras A, Duran A, Asadi Shehni A, Ferrer-Batallé M, Ramírez M, Comet J, de Llorens R, Saldova R, Llop E, Peracaula R. et al. Characterisation of the main PSA glycoforms in aggressive prostate cancer. Sci Rep. 2020;10(1):18974. doi:10.1038/s41598-020-75526-3.
   PubMed Web of Science ®Google Scholar
• Bindeman WE, Fingleton B. Glycosylation as a regulator of site-specific metastasis. Cancer Metastasis Rev. 2022;41(1):107–129. doi:10.1007/s10555-021-10015-1.
   PubMed Web of Science ®Google Scholar
• Hakomori S, Kannagi R. Glycosphingolipids as tumor-associated and differentiation markers. J Natl Cancer Inst. 1983;71:231–51.
   PubMed Web of Science ®Google Scholar
• Cotton S, Ferreira D, Soares J, Peixoto A, Relvas-Santos M, Azevedo R, Piairo P, Diéguez L, Palmeira C, Lima L, et al. Target score—a proteomics data selection tool applied to esophageal cancer identifies GLUT1-sialyl tn glycoforms as biomarkers of cancer aggressiveness. Int J Mol Sci. 2021;22(4):1664. doi:10.3390/ijms22041664.
   PubMed Web of Science ®Google Scholar
• Kannagi R, Yin J, Miyazaki K, Izawa M. Current relevance of incomplete synthesis and neo-synthesis for cancer-associated alteration of carbohydrate determinants—Hakomori’s concepts revisited. Biochim Biophys Acta. 2008;1780(3):525–31. doi:10.1016/j.bbagen.2007.10.007.
   PubMed Web of Science ®Google Scholar
• Gomes C, Osório H, Pinto MT, Campos D, Oliveira MJ, Reis CA. Expression of ST3GAL4 leads to SLe(x) expression and induces c-Met activation and an invasive phenotype in gastric carcinoma cells. PLoS One. 2013;8(6):e66737. doi:10.1371/journal.pone.0066737.
   PubMed Web of Science ®Google Scholar
• Taylor ME, Drickamer K, Imberty A, van Kooyk Y, Schnaar R, Etzler M, Varki A. Discovery and classification of glycan-binding proteins. In: Varki A, editor. Essentials of glycobiology. Cold Spring Harbor Laboratory Press; 2015. p. 361–72.
   Google Scholar
• Tan Z, Cao L, Wu Y, Wang B, Song Z, Yang J, Cheng L, Yang X, Zhou X, Dai Z, et al. Bisecting GlcNAc modification diminishes the pro-metastatic functions of small extracellular vesicles from breast cancer cells. J Extracell Vesicles. 2020;10(1):e12005. doi:10.1002/jev2.12005.
   PubMed Web of Science ®Google Scholar
• Yoshimura M, Nishikawa A, Ihara Y, Taniguchi S, Taniguchi N. Suppression of lung metastasis of B16 mouse melanoma by N-acetylglucosaminyltransferase III gene transfection. Proc Natl Acad Sci USA. 1995;92(19):8754–8. doi:10.1073/pnas.92.19.8754.
   PubMed Web of Science ®Google Scholar
• Zhang H, Meng F, Wu S, Kreike B, Sethi S, Chen W, Miller FR, Wu G. Engagement of I-Branching β-1, 6- N -Acetylglucosaminyltransferase 2 in breast cancer metastasis and TGF-β signaling. Cancer Res. 2011;71(14):4846–56. doi:10.1158/0008-5472.CAN-11-0414.
   PubMed Web of Science ®Google Scholar
• Dong X, Chen C, Deng X, Liu Y, Duan Q, Peng Z, Luo Z, Shen L. A novel mechanism for C1GALT1 in the regulation of gastric cancer progression. Cell Biosci. 2021;11(1):166. doi:10.1186/s13578-021-00678-2.
   PubMed Web of Science ®Google Scholar
• Chugh S, Barkeer S, Rachagani S, Nimmakayala RK, Perumal N, Pothuraju R, Atri P, Mahapatra S, Thapa I, Talmon GA, et al. Disruption of C1galt1 gene promotes development and metastasis of pancreatic adenocarcinomas in mice. Gastroenterology. 2018;155(5):1608–1624. doi:10.1053/j.gastro.2018.08.007.
   PubMed Web of Science ®Google Scholar
• Kuo TC, Wu M-H, Yang S-H, Chen S-T, Hsu T-W, Jhuang J-Y, Liao Y-Y, Tien Y-W, Huang M-C. C1GALT1 high expression is associated with poor survival of patients with pancreatic ductal adenocarcinoma and promotes cell invasiveness through integrin αv. Oncogene. 2021;40(7):1242–54. doi:10.1038/s41388-020-01594-4.
   PubMed Web of Science ®Google Scholar
• Liu J, Xu F, Li J, Jiang H. Overexpression of Cosmc suppresses cell migration and invasion in different subtypes of breast cancer cells via Tn and T glycans. Biosci Rep. 2020;40(6). doi:10.1042/BSR20191062.
   Google Scholar
• Liu Z, Liu J, Dong X, Hu X, Jiang Y, Li L, Du T, Yang L, Wen T, An G, et al. Tn antigen promotes human colorectal cancer metastasis via H-Ras mediated epithelial-mesenchymal transition activation. J Cell Mol Med. 2019;23(3):2083–2092. doi:10.1111/jcmm.14117.
   PubMed Web of Science ®Google Scholar
• Ding Y, Gelfenbeyn K, Freire-de-Lima L, Handa K, Hakomori S-I. Induction of epithelial-mesenchymal transition with O-glycosylated oncofetal fibronectin. FEBS Lett. 2012;586(13):1813–20. doi:10.1016/j.febslet.2012.05.020.
   PubMed Web of Science ®Google Scholar
• Leon F, Seshacharyulu P, Nimmakayala RK, Chugh S, Karmakar S, Nallasamy P, Vengoji R, Rachagani S, Cox JL, Mallya K, et al. Reduction in O-glycome induces differentially glycosylated CD44 to promote stemness and metastasis in pancreatic cancer. Oncogene. 2022;41(1):57–71. doi:10.1038/s41388-021-02047-2.
   PubMed Web of Science ®Google Scholar
• Freitas D, Campos D, Gomes J, Pinto F, Macedo JA, Matos R, Mereiter S, Pinto MT, Polónia A, Gartner F, et al. O-glycans truncation modulates gastric cancer cell signaling and transcription leading to a more aggressive phenotype. EBioMedicine. 2019;40:349–362. doi:10.1016/j.ebiom.2019.01.017.
   PubMed Web of Science ®Google Scholar
• Lakshmanan I, Chaudhary S, Vengoji R, Seshacharyulu P, Rachagani S, Carmicheal J, Jahan R, Atri P, Chirravuri‐Venkata R, Gupta R, et al. ST6GalNAc-I promotes lung cancer metastasis by altering MUC5AC sialylation. Mol Oncol. 2021;15(7):1866–1881. doi:10.1002/1878-0261.12956.
   PubMed Web of Science ®Google Scholar
• Radhakrishnan P, Dabelsteen S, Madsen FB, Francavilla C, Kopp KL, Steentoft C, Vakhrushev SY, Olsen JV, Hansen L, Bennett EP, et al. Immature truncated O-glycophenotype of cancer directly induces oncogenic features. Proc Natl Acad Sci USA. 2014;111(39):E4066–75. doi:10.1073/pnas.1406619111.
   PubMed Web of Science ®Google Scholar
• Cheng J, Wang R, Zhong G, Chen X, Cheng Y, Li W, Yang Y. ST6GAL2 downregulation inhibits cell adhesion and invasion and is associated with improved patient survival in breast cancer. Onco Targets Ther. 2020;13:903–14. doi:10.2147/OTT.S230847.
   PubMed Web of Science ®Google Scholar
• Yuan Q, Chen X, Han Y, Lei T, Wu Q, Yu X, Wang L, Fan Z, Wang S. Modification of α2,6-sialylation mediates the invasiveness and tumorigenicity of non-small cell lung cancer cells in vitro and in vivo via Notch1/Hes1/MMPs pathway. Int J Cancer. 2018;143(9):2319–30. doi:10.1002/ijc.31737.
   PubMed Web of Science ®Google Scholar
• Walker MR, Goel HL, Mukhopadhyay D, Chhoy P, Karner ER, Clark JL, Liu H, Li R, Zhu JL, Chen S, et al. O-linked α2,3 sialylation defines stem cell populations in breast cancer. Sci Adv. 2022;8(1):eabj9513. doi:10.1126/sciadv.abj9513.
   PubMed Web of Science ®Google Scholar
• Guerrero PE, Miró L, Wong BS, Massaguer A, Martínez-Bosch N, Llorens RD, Navarro P, Konstantopoulos K, Llop E, Peracaula R. Knockdown of α2,3-Sialyltransferases impairs pancreatic cancer cell migration, invasion and E-selectin-dependent adhesion. IJMS. 2020;21(17):6239. doi:10.3390/ijms21176239.
   Google Scholar
• Dalangood S, Zhu Z, Ma Z, Li J, Zeng Q, Yan Y, Shen B, Yan J, Huang R. Identification of glycogene-type and validation of ST3GAL6 as a biomarker predicts clinical outcome and cancer cell invasion in urinary bladder cancer. Theranostics. 2020;10(22):10078–91. doi:10.7150/thno.48711.
   PubMed Web of Science ®Google Scholar
• Carrascal MA, Silva M, Ramalho JS, Pen C, Martins M, Pascoal C, Amaral C, Serrano I, Oliveira MJ, Sackstein R, et al. Inhibition of fucosylation in human invasive ductal carcinoma reduces E-selectin ligand expression, cell proliferation, and ERK1/2 and p38 MAPK activation. Mol Oncol. 2018;12(5):579–593. doi:10.1002/1878-0261.12163.
   PubMed Web of Science ®Google Scholar
• Pothuraju R, Rachagani S, Krishn SR, Chaudhary S, Nimmakayala RK, Siddiqui JA, Ganguly K, Lakshmanan I, Cox JL, Mallya K, et al. Molecular implications of MUC5AC-CD44 axis in colorectal cancer progression and chemoresistance. Mol Cancer. 2020;19(1):37. doi:10.1186/s12943-020-01156-y.
   PubMed Web of Science ®Google Scholar
• Gomes C, Almeida A, Barreira A, Calheiros J, Pinto F, Abrantes R, Costa A, Polonia A, Campos D, Osório H, et al. Carcinoembryonic antigen carrying SLe X as a new biomarker of more aggressive gastric carcinomas. Theranostics. 2019;9(24):7431–46. doi:10.7150/thno.33858.
   PubMed Web of Science ®Google Scholar
• Ferreira IG, Carrascal M, Mineiro A, Bugalho A, Borralho P, Silva Z, Dall’olio F, Videira P. Carcinoembryonic antigen is a sialyl lewis x/a carrier and an E‑selectin ligand in non‑small cell lung cancer. Int J Oncol. 2019;55(5):1033–48. doi:10.3892/ijo.2019.4886.
   PubMed Web of Science ®Google Scholar
• Ganguly K, Krishn SR, Rachagani S, Jahan R, Shah A, Nallasamy P, Rauth S, Atri P, Cox JL, Pothuraju R, et al. Secretory mucin 5AC promotes neoplastic progression by augmenting KLF4-mediated pancreatic cancer cell stemness. Cancer Res. 2021;81(1):91–102. doi:10.1158/0008-5472.CAN-20-1293.
   PubMed Web of Science ®Google Scholar
• Scheidegger EP, Lackie PM, Papay J, Roth J. In vitro and in vivo growth of clonal sublines of human small cell lung carcinoma is modulated by polysialic acid of the neural cell adhesion molecule. Lab Invest. 1994;70:95–106.
   PubMed Web of Science ®Google Scholar
• Tu CF, Wu M-Y, Lin Y-C, Kannagi R, Yang R-B. FUT8 promotes breast cancer cell invasiveness by remodeling TGF-β receptor core fucosylation. Breast Cancer Res. 2017;19(1):111. doi:10.1186/s13058-017-0904-8.
   PubMedGoogle Scholar
• Wang X, Inoue S, Gu J, Miyoshi E, Noda K, Li W, Mizuno-Horikawa Y, Nakano M, Asahi M, Takahashi M, et al. Dysregulation of TGF-β1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice. Proc Natl Acad Sci USA. 2005;102(44):15791–6. doi:10.1073/pnas.0507375102.
   PubMed Web of Science ®Google Scholar
• Cheng L, Gao S, Song X, Dong W, Zhou H, Zhao L, Jia L. Comprehensive N-glycan profiles of hepatocellular carcinoma reveal association of fucosylation with tumor progression and regulation of FUT8 by microRnas. Oncotarget. 2016;7(38):61199–214. doi:10.18632/oncotarget.11284.
   PubMedGoogle Scholar
• Agrawal P, Fontanals-Cirera B, Sokolova E, Jacob S, Vaiana CA, Argibay D, Davalos V, McDermott M, Nayak S, Darvishian F, et al. A systems biology approach identifies FUT8 as a driver of melanoma metastasis. Cancer Cell. 2017;31(6):804–19.e7. doi:10.1016/j.ccell.2017.05.007.
   PubMed Web of Science ®Google Scholar
• Höti N, Yang S, Hu Y, Shah P, Haffner MC, Zhang H. Overexpression of α (1,6) fucosyltransferase in the development of castration-resistant prostate cancer cells. Prostate Cancer Prostatic Dis. 2018;21(1):137–46. doi:10.1038/s41391-017-0016-7.
   PubMed Web of Science ®Google Scholar
• Li Y, Huang X, Zhang J, Li Y, Ma K. Synergistic inhibition of cell migration by tetraspanin CD82 and gangliosides occurs via the EGFR or cMet-activated Pl3K/Akt signalling pathway. Int J Biochem Cell Biol. 2013;45(11):2349–58. doi:10.1016/j.biocel.2013.08.002.
   PubMed Web of Science ®Google Scholar
• Yamada T, Bando H, Takeuchi S, Kita K, Li Q, Wang W, Akinaga S, Nishioka Y, Sone S, Yano S, et al. Genetically engineered humanized anti-ganglioside GM2 antibody against multiple organ metastasis produced by GM2-expressing small-cell lung cancer cells. Cancer Sci. 2011;102(12):2157–63. doi:10.1111/j.1349-7006.2011.02093.x.
   PubMed Web of Science ®Google Scholar
• Sasaki N, Hirabayashi K, Michishita M, Takahashi K, Hasegawa F, Gomi F, Itakura Y, Nakamura N, Toyoda M, Ishiwata T, et al. Ganglioside GM2, highly expressed in the MIA PaCa-2 pancreatic ductal adenocarcinoma cell line, is correlated with growth, invasion, and advanced stage. Sci Rep. 2019;9(1):19369. doi:10.1038/s41598-019-55867-4.
   PubMedGoogle Scholar
• Thomas D, Sagar S, Caffrey T, Grandgenett PM, Radhakrishnan P. Truncated O-glycans promote epithelial-to-mesenchymal transition and stemness properties of pancreatic cancer cells. J Cell Mol Med. 2019;23(10):6885–96. doi:10.1111/jcmm.14572.
   PubMed Web of Science ®Google Scholar
• Cotton S, Azevedo R, Gaiteiro C, Ferreira D, Lima L, Peixoto A, Fernandes E, Neves M, Neves D, Amaro T, et al. Targeted O-glycoproteomics explored increased sialylation and identified MUC16 as a poor prognosis biomarker in advanced-stage bladder tumours. Mol Oncol. 2017;11(8):895–912. doi:10.1002/1878-0261.12035.
   PubMed Web of Science ®Google Scholar
• Julien S, Ivetic A, Grigoriadis A, QiZe D, Burford B, Sproviero D, Picco G, Gillett C, Papp SL, Schaffer L, et al. Selectin ligand sialyl-lewis x antigen drives metastasis of hormone-dependent breast cancers. Cancer Res. 2011;71(24):7683–93. doi:10.1158/0008-5472.CAN-11-1139.
   PubMed Web of Science ®Google Scholar
• Miyoshi E, Ito Y, Miyoshi Y. Involvement of aberrant glycosylation in thyroid cancer. J Oncol. 2010;2010:816595. doi:10.1155/2010/816595.
   PubMedGoogle Scholar
• Lee-Sundlov MM, Ashline DJ, Hanneman AJ, Grozovsky R, Reinhold VN, Hoffmeister KM, Lau JT. Circulating blood and platelets supply glycosyltransferases that enable extrinsic extracellular glycosylation. Glycobiology. 2017;27(2):188–98. doi:10.1093/glycob/cww108.
   PubMed Web of Science ®Google Scholar
• Lee MM, Nasirikenari M, Manhardt CT, Ashline DJ, Hanneman AJ, Reinhold VN, Lau JTY. Platelets support extracellular sialylation by supplying the sugar donor substrate. J Biol Chem. 2014;289(13):8742–8. doi:10.1074/jbc.C113.546713.
   PubMed Web of Science ®Google Scholar
• Lauková L, Weiss R, Semak V, Weber V. Desialylation of platelet surface glycans enhances platelet adhesion to adsorbent polymers for lipoprotein apheresis. Int J Artif Organs. 2021;44(6):378–84. doi:10.1177/0391398820968849.
   PubMed Web of Science ®Google Scholar
• Moebius J, Walter U, Sickmann A. Elucidation of N-Glycosylation sites on human platelet proteins: a glycoproteomic approach*. Mol Cell Proteom. 2006;5(2):226–33. doi:10.1074/mcp.M500324-MCP200.
   PubMed Web of Science ®Google Scholar
• King SL, Joshi HJ, Schjoldager KT, Halim A, Madsen TD, Dziegiel MH, Woetmann A, Vakhrushev SY, Wandall HH. Characterizing the O-glycosylation landscape of human plasma, platelets, and endothelial cells. Blood Adv. 2017;1(7):429–42. doi:10.1182/bloodadvances.2016002121.
   PubMed Web of Science ®Google Scholar
• Li Y, Fu J, Ling Y, Yago T, McDaniel JM, Song J, Bai X, Kondo Y, Qin Y, Hoover C, et al. Sialylation on O-glycans protects platelets from clearance by liver kupffer cells. Proc Natl Acad Sci USA. 2017;114(31):8360–5. doi:10.1073/pnas.1707662114.
   PubMed Web of Science ®Google Scholar
• Harris SB, Josephson CD, Kost CB, Hillyer CD. Nonfatal intravascular hemolysis in a pediatric patient after transfusion of a platelet unit with high-titer anti-A. Transfusion. 2007;47(8):1412–17. doi:10.1111/j.1537-2995.2007.01283.x.
   PubMed Web of Science ®Google Scholar
• Ramírez-López A, Álvarez Román MT, Monzón Manzano E, Acuña P, Arias-Salgado EG, Martín Salces M, Rivas Pollmar MI, Jiménez Yuste V, Justo Sanz R, García Barcenilla S, et al. The importance of platelet glycoside residues in the haemostasis of patients with immune thrombocytopaenia. J Clin Med. 2021;10(8):1661. doi:10.3390/jcm10081661.
   PubMed Web of Science ®Google Scholar
• Klein CA. Cancer progression and the invisible phase of metastatic colonization. Nat Rev Cancer. 2020;20(11):681–694. doi:10.1038/s41568-020-00300-6.
   PubMed Web of Science ®Google Scholar
• Massagué J, Obenauf AC. Metastatic colonization by circulating tumour cells. Nature. 2016;529(7586):298–306. doi:10.1038/nature17038.
   PubMed Web of Science ®Google Scholar
• Ichikawa J, Ando T, Kawasaki T, Sasaki T, Shirai T, Tsukiji N, Kimura Y, Aoki K, Hayakawa K, Suzuki‐Inoue K, et al. Role of platelet C-Type lectin-like receptor 2 in promoting lung metastasis in Osteosarcoma. J Bone Miner Res. 2020;35(9):1738–1750. doi:10.1002/jbmr.4045.
   PubMed Web of Science ®Google Scholar
• Janowska-Wieczorek A, Wysoczynski M, Kijowski J, Marquez‐Curtis L, Machalinski B, Ratajczak J, Ratajczak MZ. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer. 2005;113(5):752–60. doi:10.1002/ijc.20657.
   PubMed Web of Science ®Google Scholar
• Sabrkhany S, Kuijpers MJE, Oude Egbrink MGA, Griffioen AW. Platelets as messengers of early-stage cancer. Cancer Metastasis Rev. 2021;40(2):563–73. doi:10.1007/s10555-021-09956-4.
   PubMed Web of Science ®Google Scholar
• Lin RJ, Afshar-Kharghan V, Schafer AI. Paraneoplastic thrombocytosis: the secrets of tumor self-promotion. Blood. 2014;124(2):184–7. doi:10.1182/blood-2014-03-562538.
   PubMed Web of Science ®Google Scholar
• Mammadova-Bach E, Zigrino P, Brucker C, Bourdon C, Freund M, De Arcangelis A, Abrams SI, Orend G, Gachet C, Mangin PH, et al. Platelet integrin α6β1 controls lung metastasis through direct binding to cancer cell–derived ADAM9. JCI Insight. 2016;1(14):e88245. doi:10.1172/jci.insight.88245.
   PubMed Web of Science ®Google Scholar
• Kim YJ, Borsig L, Varki NM, Varki A. P-selectin deficiency attenuates tumor growth and metastasis. Proc Natl Acad Sci USA. 1998;95(16):9325–30. doi:10.1073/pnas.95.16.9325.
   PubMed Web of Science ®Google Scholar
• Nieswandt B, Hafner M, Echtenacher B, Männel DN. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res. 1999;59:1295–300.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Martinez A, Simon-Saez I, Perales S, Garrido-Navas C, Russo A, de Miguel-Perez D, Puche-Sanz I, Alaminos C, Ceron J, Lorente JA, et al. Exchange of cellular components between platelets and tumor cells: impact on tumor cells behavior. Theranostics. 2022;12(5):2150–2161. doi:10.7150/thno.64252.
   PubMed Web of Science ®Google Scholar
• Sadallah S, Schmied L, Eken C, Charoudeh HN, Amicarella F, Schifferli JA. Platelet-derived ectosomes reduce NK cell function. J Immunol. 2016;197(5):1663–71. doi:10.4049/jimmunol.1502658.
   PubMed Web of Science ®Google Scholar
• Läubli H, Borsig L. Selectins promote tumor metastasis. Semin Cancer Biol. 2010;20(3):169–77. doi:10.1016/j.semcancer.2010.04.005.
   PubMed Web of Science ®Google Scholar
• Echtler K, Konrad I, Lorenz M, Schneider S, Hofmaier S, Plenagl F, Stark K, Czermak T, Tirniceriu A, Eichhorn M. et al. Platelet GPIIb supports initial pulmonary retention but inhibits subsequent proliferation of melanoma cells during hematogenic metastasis. PLoS One. 2017;12(3):e0172788. doi:10.1371/journal.pone.0172788.
   PubMed Web of Science ®Google Scholar
• Guo Y, Cui W, Pei Y, Xu D. Platelets promote invasion and induce epithelial to mesenchymal transition in ovarian cancer cells by TGF-β signaling pathway. Gynecol Oncol. 2019;153(3):639–50. doi:10.1016/j.ygyno.2019.02.026.
   PubMed Web of Science ®Google Scholar
• Trinchera M, Aronica A, Dall’olio F. Selectin ligands sialyl-lewis a and sialyl-lewis x in gastrointestinal cancers. Biology (Basel). 2017;6(4):16. doi:10.3390/biology6010016.
   PubMedGoogle Scholar
• Ma YQ, Geng JG. Heparan sulfate-like proteoglycans mediate adhesion of human malignant melanoma A375 cells to P-selectin under flow. J Immun (Balt Md 1950). 2000;165(1):558–65. doi:10.4049/jimmunol.165.1.558.
   PubMed Web of Science ®Google Scholar
• Ma Y-Q, Geng J-G. Obligatory requirement of sulfation for P-selectin binding to human salivary gland carcinoma Acc-M cells and breast carcinoma ZR-75-30 cells. J Immun (Balt Md 1950). 2002;168(4):1690–6. doi:10.4049/jimmunol.168.4.1690.
   PubMed Web of Science ®Google Scholar
• McCarty OJ, Mousa SA, Bray PF, Konstantopoulos K. Immobilized platelets support human colon carcinoma cell tethering, rolling, and firm adhesion under dynamic flow conditions. Blood. 2000;96(5):1789–97. doi:10.1182/blood.V96.5.1789.
   PubMed Web of Science ®Google Scholar
• Suzuki-Inoue K, Osada M, Ozaki Y. Physiologic and pathophysiologic roles of interaction between C-type lectin-like receptor 2 and podoplanin: partners from in utero to adulthood. J Thromb Haemost. 2017;15(2):219–229. doi:10.1111/jth.13590.
   PubMed Web of Science ®Google Scholar
• Sekiguchi T, Takemoto A, Takagi S, Takatori K, Sato S, Takami M, Fujita N. Targeting a novel domain in podoplanin for inhibiting platelet-mediated tumor metastasis. Oncotarget. 2016;7(4):3934–46. doi:10.18632/oncotarget.6598.
   PubMedGoogle Scholar
• Shirai T, Inoue O, Tamura S, Tsukiji N, Sasaki T, Endo H, Satoh K, Osada M, Sato‐Uchida H, Fujii H, et al. C-type lectin-like receptor 2 promotes hematogenous tumor metastasis and prothrombotic state in tumor-bearing mice. J Thromb Haemost. 2017;15(3):513–525. doi:10.1111/jth.13604.
   PubMed Web of Science ®Google Scholar
• Takemoto A, Takagi S, Ukaji T, Gyobu N, Kakino M, Takami M, Kobayashi A, Lebel M, Kawaguchi T, Sugawara M, et al. Targeting podoplanin for the treatment of osteosarcoma. Clin Cancer Res. 2022;28(12):2633–2645. doi:10.1158/1078-0432.CCR-21-4509.
   PubMed Web of Science ®Google Scholar
• Lee HY, Yu N-Y, Lee S-H, Tsai H-J, Wu C-C, Cheng J-C, Chen D-P, Wang Y-R, Tseng C-P. Podoplanin promotes cancer-associated thrombosis and contributes to the unfavorable overall survival in an ectopic xenograft mouse model of oral cancer. Biomed J. 2020;43(2):146–62. doi:10.1016/j.bj.2019.07.001.
   PubMed Web of Science ®Google Scholar
• Takemoto A, Okitaka M, Takagi S, Takami M, Sato S, Nishio M, Okumura S, Fujita N. A critical role of platelet TGF-β release in podoplanin-mediated tumour invasion and metastasis. Sci Rep. 2017;7(1):42186. doi:10.1038/srep42186.
   PubMedGoogle Scholar
• Tamura S, Suzuki-Inoue K, Tsukiji N, Shirai T, Sasaki T, Osada M, Satoh K, Ozaki Y. Podoplanin-positive periarteriolar stromal cells promote megakaryocyte growth and proplatelet formation in mice by CLEC-2. Blood. 2016;127(13):1701–10. doi:10.1182/blood-2015-08-663708.
   PubMed Web of Science ®Google Scholar
• Lombard SE, Pollitt AY, Hughes CE, Di Y, Mckinnon T, O’callaghan CA, Watson SP. Mouse podoplanin supports adhesion and aggregation of platelets under arterial shear: a novel mechanism of haemostasis. Platelets. 2018;29(7):716–22. doi:10.1080/09537104.2017.1356919.
   PubMed Web of Science ®Google Scholar
• Thijssen VL, Heusschen R, Caers J, Griffioen AW. Galectin expression in cancer diagnosis and prognosis: a systematic review. Biochim Biophys Acta. 2015;1855(2):235–47. doi:10.1016/j.bbcan.2015.03.003.
   PubMed Web of Science ®Google Scholar
• Demydenko D, Berest I. Expression of galectin-1 in malignant tumors. Exp Oncol. 2009;31:74–9.
   PubMedGoogle Scholar
• Saha B, Mathur T, Tronolone JJ, Chokshi M, Lokhande GK, Selahi A, Gaharwar AK, Afshar-Kharghan V, Sood AK, Bao G, et al. Human tumor microenvironment chip evaluates the consequences of platelet extravasation and combinatorial antitumor-antiplatelet therapy in ovarian cancer. Sci Adv. 2021;7(30). doi:10.1126/sciadv.abg5283.
   Web of Science ®Google Scholar
• Dovizio M, Maier TJ, Alberti S, Di Francesco L, Marcantoni E, Münch G, John CM, Suess B, Sgambato A, Steinhilber D, et al. Pharmacological inhibition of platelet-tumor cell cross-talk prevents platelet-induced overexpression of cyclooxygenase-2 in HT29 human colon carcinoma cells. Mol Pharmacol. 2013;84(1):25–40. doi:10.1124/mol.113.084988.
   PubMed Web of Science ®Google Scholar
• Martinet L, Smyth MJ. Regulation of immune cell functions through nectin and nectin-like receptors. 2016:404–14. doi:10.1016/B978-0-12-374279-7.02010-5.
   Google Scholar
• Ma W, Ma J, Lei T, Zhao M, Zhang M. Targeting immunotherapy for bladder cancer by using anti-CD3 × CD155 bispecific antibody. J Cancer. 2019;10(21):5153–61. doi:10.7150/jca.29937.
   PubMed Web of Science ®Google Scholar
• Gao J, Zheng Q, Shao Y, Wang W, Zhao C. CD155 downregulation synergizes with adriamycin to induce breast cancer cell apoptosis. Apoptosis. 2018;23(9–10):512–20. doi:10.1007/s10495-018-1473-8.
   PubMed Web of Science ®Google Scholar
• Kučan Brlić P, Lenac Roviš T, Cinamon G, Tsukerman P, Mandelboim O, Jonjić S. Targeting PVR (CD155) and its receptors in anti-tumor therapy. Cell Mol Immunol. 2019;16(1):40–52. doi:10.1038/s41423-018-0168-y.
   PubMed Web of Science ®Google Scholar
• Azab AK, Quang P, Azab F, Pitsillides C, Thompson B, Chonghaile T, Patton JT, Maiso P, Monrose V, Sacco A, et al. P-selectin glycoprotein ligand regulates the interaction of multiple myeloma cells with the bone marrow microenvironment. Blood. 2012;119(6):1468–78. doi:10.1182/blood-2011-07-368050.
   PubMed Web of Science ®Google Scholar
• Chang YW, Hsieh P-W, Chang Y-T, Lu M-H, Huang T-F, Chong K-Y, Liao H-R, Cheng J-C, Tseng C-P. Identification of a novel platelet antagonist that binds to CLEC-2 and suppresses podoplanin-induced platelet aggregation and cancer metastasis. Oncotarget. 2015;6(40):42733–48. doi:10.18632/oncotarget.5811.
   PubMedGoogle Scholar
• Ataga KI, Kutlar A, Kanter J, Liles D, Cancado R, Friedrisch J, Guthrie TH, Knight-Madden J, Alvarez OA, Gordeuk VR, et al. Crizanlizumab for the prevention of pain crises in sickle cell disease. N Engl J Med. 2017;376(5):429–439. doi:10.1056/NEJMoa1611770.
   PubMed Web of Science ®Google Scholar
• Jackson W 3rd, Sosnoski DM, Ohanessian SE, Chandler P, Mobley A, Meisel KD, Mastro AM. Role of megakaryocytes in breast cancer metastasis to bone. Cancer Res. 2017;77(8):1942–54. doi:10.1158/0008-5472.CAN-16-1084.
   PubMed Web of Science ®Google Scholar