Overexpression of protease-activated receptor type 1 (PAR-1) in glioblastoma multiforme WHO IV cells and blood vessels revealed by NCAM-assisted glioblastoma border labeling

References

• Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007;114(2):97–109.
   PubMed Web of Science ®Google Scholar
• Taveras JM, Thompson HG Jr, Pool JL. Should we treat glioblastoma multiforme? A study of survival in 425 cases. Am J Roentgenol Radium Ther Nucl Med. 1962;87:473–9.
   PubMedGoogle Scholar
• Kleihues P, Cavenee WK. Pathology and genetics of tumours of the nervous system (WHO), 2te Aufl. Lyon, France: Lyon IRAC Press; 2000.
   Google Scholar
• Reifenberger, Collins VP. Pathology and molecular genetics of astrocytic gliomas. J Mol Med (Berl). 2004;82(10):656–70.
   Google Scholar
• Brat DJ, Van Meir EG. Vaso-occlusive and prothrombotic mechanisms associated with tumor hypoxia, necrosis, and accelerated growth in glioblastoma. Lab Invest. 2004;84(4):397–405.
   PubMed Web of Science ®Google Scholar
• Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285(21):1182–6.
   PubMed Web of Science ®Google Scholar
• Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407(6801):249–57.
   PubMed Web of Science ®Google Scholar
• Arenberg DA, Strieter RM. Angiogenesis. In: Serhan CN, Ward PA, editors. Molecular and cellular basis of inflammation, Aufl. Totowa, NJ: Human Press Inc.; 1999, 29–49.
   Google Scholar
• Ronn LC, Hartz BP, Bock E. The neural cell adhesion molecule (NCAM) in development and plasticity of the nervous system. Exp Gerontol. 1998;33(7–8):853–64.
   PubMed Web of Science ®Google Scholar
• Thiery JP, Brackenbury R, Rutishauser U, Edelman GM. Adhesion among neural cells of the chick embryo. II. Purification and characterization of a cell adhesion molecule from neural retina. J Biol Chem. 1977;252(19):6841–5.
   PubMed Web of Science ®Google Scholar
• Crossin KL, Krushel LA. Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily. Dev Dyn. 2000;218(2):260–79.
   PubMed Web of Science ®Google Scholar
• Kiselyov VV, Soroka V, Berezin V, Bock E. Structural biology of NCAM homophilic binding and activation of FGFR. J Neurochem. 2005;94(5):1169–79.
   PubMed Web of Science ®Google Scholar
• Cunningham BA, Hemperly JJ, Murray BA, Prediger EA, Brackenbury R, Edelman GM. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science. 1987;236(4803):799–806.
   PubMed Web of Science ®Google Scholar
• Sasaki H, Yoshida K, Ikeda E, Asou H, Inaba M, Otani M, et al. Expression of the neural cell adhesion molecule in astrocytic tumors: an inverse correlation with malignancy. Cancer. 1998;82(10):1921–31.
   PubMed Web of Science ®Google Scholar
• Duenisch P, Reichart R, Mueller U, Brodhun M, Bjerkvig R, Romeike B, et al. Neural cell adhesion molecule isoform 140 declines with rise of WHO grade in human gliomas and serves as indicator for the invasion zone of multiform glioblastomas and brain metastases. J Cancer Res Clin Oncol. 2011;137(3):399–414.
   PubMed Web of Science ®Google Scholar
• Edvardsen K, Brunner N, Spang-Thomsen M, Walsh FS, Bock E. Migratory, invasive and metastatic capacity of NCAM transfected rat glioma cells. Int J Dev Neurosci. 1993;11(5):681–90.
   PubMed Web of Science ®Google Scholar
• Edvardsen K, Pedersen PH, Bjerkvig R, Hermann GG, Zeuthen J, Laerum OD, et al. Transfection of glioma cells with the neural-cell adhesion molecule NCAM: effect on glioma-cell invasion and growth in vivo. Int J Cancer. 1994;58(1):116–22.
   PubMed Web of Science ®Google Scholar
• Gratsa A, Rooprai HK, Rogers JP, Martin KK, Pilkington GJ. Correlation of expression of NCAM and GD3 ganglioside to motile behaviour in neoplastic glia. Anticancer Res. 1997;17(6B):4111–7.
   PubMed Web of Science ®Google Scholar
• Newman PJ. The biology of PECAM-1. J Clin Invest. 1997;99(1):3–8.
   PubMed Web of Science ®Google Scholar
• Newman PJ. Switched at birth: a new family for PECAM-1. J Clin Invest. 1999;103(1):5–9.
   PubMed Web of Science ®Google Scholar
• Gong N, Chatterjee S. Platelet endothelial cell adhesion molecule in cell signaling and thrombosis. Mol Cell Biochem. 2003;253(1–2):151–8.
   PubMed Web of Science ®Google Scholar
• DeLisser HM, Christofidou-Solomidou M, Strieter RM, Burdick MD, Robinson CS, Wexler RS, et al. Involvement of endothelial PECAM-1/CD31 in angiogenesis. Am J Pathol. 1997;151(3):671–7.
   PubMed Web of Science ®Google Scholar
• Matsumura T, Wolff K, Petzelbauer P. Endothelial cell tube formation depends on cadherin 5 and CD31 interactions with filamentous actin. J Immunol. 1997;158(7):3408–16.
   PubMed Web of Science ®Google Scholar
• Zhou Z, Christofidou-Solomidou M, Garlanda C, DeLisser HM. Antibody against murine PECAM-1 inhibits tumor angiogenesis in mice. Angiogenesis. 1999;3(2):181–8.
   PubMedGoogle Scholar
• Aroca F, Renaud W, Bartoli C, Bouvier-Labit C, Figarella-Branger D. Expression of PECAM-1/CD31 isoforms in human brain gliomas. J Neurooncol. 1999;43(1):19–25.
   PubMed Web of Science ®Google Scholar
• Schmidt A. Zur Blutlehre (The Lesson of Blood), Leipzig, Germany: FCW Vogel; 1892.
   Google Scholar
• Mann KG. Biochemistry and physiology of blood coagulation. Thromb Haemost. 1999;82(2):165–74.
   PubMed Web of Science ®Google Scholar
• Sokolova E, Reiser G. Prothrombin/thrombin and the thrombin receptors PAR-1 and PAR-4 in the brain: localization, expression and participation in neurodegenerative diseases. Thromb Haemost. 2008;100(4):576–81.
   PubMed Web of Science ®Google Scholar
• Coughlin SR. Protease-activated receptors start a family. Proc Natl Acad Sci USA. 1994;91(20):9200–2.
   PubMed Web of Science ®Google Scholar
• Hollenberg MD, Compton SJ. International union of pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol Rev. 2002;54(2):203–17.
   PubMed Web of Science ®Google Scholar
• Wang H, Ubl JJ, Stricker R, Reiser G. Thrombin (PAR-1)-induced proliferation in astrocytes via MAPK involves multiple signaling pathways. Am J Physiol Cell Physiol. 2002;283(5):C1351–64.
   PubMed Web of Science ®Google Scholar
• Rong Y, Post DE, Pieper RO, Durden DL, Van Meir EG, Brat DJ. PTEN and hypoxia regulate tissue factor expression and plasma coagulation by glioblastoma. Cancer Res. 2005;65(4):1406–13.
   PubMed Web of Science ®Google Scholar
• Tsopanoglou NE, Maragoudakis ME. Role of thrombin in angiogenesis and tumor progression. Semin Thromb Hemost. 2004;30(1):63–9.
   PubMed Web of Science ®Google Scholar
• Tsopanoglou NE, Maragoudakis ME. Inhibition of angiogenesis by small-molecule antagonists of protease-activated receptor-1. Semin Thromb Hemost. 2007;33(7):680–7.
   PubMed Web of Science ®Google Scholar
• Feng Z, Li L, Yong Ng P, Porter AG. Neuronal differentiation and protection from nitric oxide-induced apoptosis require c-Jun-dependent expression of NCAM140. Mol Cell Biol. 2002;22(15):5357–66.
   PubMed Web of Science ®Google Scholar
• Tews DS, Nissen A. Expression of adhesion factors and degrading proteins in primary and secondary glioblastomas and their precursor tumors. Invasion Metastasis. 1998;18(5–6):271–84.
   PubMedGoogle Scholar
• Kleinschmidt-DeMasters BK, Orr EA, Savelieva E, Owens GC, Kruse CA. Paucity of retinoic acid receptor alpha (RAR alpha) nuclear immunostaining in gliomas and inability of retinoic acid to influence neural cell adhesion molecule (NCAM) expression. J Neurooncol. 1999;41(1):31–42.
   PubMed Web of Science ®Google Scholar
• Yao Y, Kubota T, Takeuchi H, Sato K. Prognostic significance of microvessel density determined by an anti-CD105/endoglin monoclonal antibody in astrocytic tumors: comparison with an anti-CD31 monoclonal antibody. Neuropathology. 2005;25(3):201–6.
   PubMed Web of Science ®Google Scholar
• Sporns O, Edelman GM, Crossin KL. The neural cell adhesion molecule (N-CAM) inhibits proliferation in primary cultures of rat astrocytes. Proc Natl Acad Sci USA. 1995;92(2):542–6.
   PubMed Web of Science ®Google Scholar
• Krushel LA, Sporns O, Cunningham BA, Crossin KL, Edelman GM. Neural cell adhesion molecule (N-CAM) inhibits astrocyte proliferation after injury to different regions of the adult rat brain. Proc Natl Acad Sci USA. 1995;92(10):4323–7.
   PubMed Web of Science ®Google Scholar
• Nakagawa T, Kubota T, Kabuto M, Fujimoto N, Okada Y. Secretion of matrix metalloproteinase-2 (72 kD gelatinase/type IV collagenase = gelatinase A) by malignant human glioma cell lines: implications for the growth and cellular invasion of the extracellular matrix. J Neurooncol. 1996;28(1):13–24.
   PubMed Web of Science ®Google Scholar
• Laws ER Jr, Goldberg WJ, Bernstein JJ. Migration of human malignant astrocytoma cells in the mammalian brain: Scherer revisited. Int J Dev Neurosci. 1993;11(5):691–7.
   PubMed Web of Science ®Google Scholar
• Wakimoto H, Kesari S, Farrell CJ, Curry WT Jr, Zaupa C, Aghi M, et al. Human glioblastoma-derived cancer stem cells: establishment of invasive glioma models and treatment with oncolytic herpes simplex virus vectors. Cancer Res. 2009;69(8):3472–81.
   PubMed Web of Science ®Google Scholar
• Wakimoto H, Mohapatra G, Kanai R, Curry WT Jr, Yip S, Nitta M, et al. Maintenance of primary tumor phenotype and genotype in glioblastoma stem cells. Neuro Oncol. 2012;14(2):132–44.
   PubMed Web of Science ®Google Scholar
• Khattab AZ, Ahmed MI, Fouad MA, Essa WA. Significance of p53 and CD31 in astrogliomas. Med Oncol. 2009;26(1):86–92.
   PubMed Web of Science ®Google Scholar
• Lebelt A, Dzieciol J, Guzinska-Ustymowicz K, Lemancewicz D, Zimnoch L, Czykier E. Angiogenesis in gliomas. Folia Histochem Cytobiol. 2008;46(1):69–72.
   PubMed Web of Science ®Google Scholar
• Kaufmann R, Patt S, Schafberg H, Kalff R, Neupert G, Nowak G. Functional thrombin receptor PAR1 in primary cultures of human glioblastoma cells. Neuroreport. 1998;9(4):709–12.
   PubMed Web of Science ®Google Scholar
• Ubl JJ, Vohringer C, Reiser G. Co-existence of two types of [Ca2+]i-inducing protease-activated receptors (PAR-1 and PAR-2) in rat astrocytes and C6 glioma cells. Neuroscience. 1998;86(2):597–609.
   PubMed Web of Science ®Google Scholar
• Wang H, Ubl JJ, Reiser G. Four subtypes of protease-activated receptors, co-expressed in rat astrocytes, evoke different physiological signaling. Glia. 2002;37(1):53–63.
   PubMed Web of Science ®Google Scholar
• Hayakawa Y, Kurimoto M, Nagai S, Kurosaki K, Tsuboi Y, Hamada H, et al. Thrombin-induced cell proliferation and platelet-derived growth factor-AB release from A172 human glioblastoma cells. J Thromb Haemost. 2007;5(11):2219–26.
   PubMed Web of Science ®Google Scholar
• Yin YJ, Salah Z, Grisaru-Granovsky S, Cohen I, Even-Ram SC, Maoz M, et al. Human protease-activated receptor 1 expression in malignant epithelia: a role in invasiveness. Arterioscler Thromb Vasc Biol. 2003;23(6):940–4.
   PubMed Web of Science ®Google Scholar
• Fujimoto D, Hirono Y, Goi T, Katayama K, Matsukawa S, Yamaguchi A. The activation of proteinase-activated receptor-1 (PAR1) mediates gastric cancer cell proliferation and invasion. BMC Cancer. 2010;10:443.
   PubMed Web of Science ®Google Scholar
• Bartha K, Domotor E, Lanza F, Adam-Vizi V, Machovich R. Identification of thrombin receptors in rat brain capillary endothelial cells. J Cereb Blood Flow Metab. 2000;20(1):175–82.
   PubMed Web of Science ®Google Scholar
• O'Brien PJ, Prevost N, Molino M, Hollinger MK, Woolkalis MJ, Woulfe DS, et al. Thrombin responses in human endothelial cells. Contributions from receptors other than PAR1 include the transactivation of PAR2 by thrombin-cleaved PAR1. J Biol Chem. 2000;275(18):13502–9.
   PubMed Web of Science ®Google Scholar
• Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995;1(1):27–31.
   PubMed Web of Science ®Google Scholar