Vaso-occlusive and prothrombotic mechanisms associated with tumor hypoxia, necrosis, and accelerated growth in glioblastoma

Laboratory Investigation

Volumn 84, Issue 4, 2004, Pages 397-405

  Brat, Daniel J ^a,b   Van Meir, Erwin G ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY HOSPITAL   (United States)

Author keywords

Angiogenesis; Astrocytoma; Brain tumor; Glioblastoma; Hypoxia; Necrosis; Thrombosis

Indexed keywords

ANGIOPOIETIN 2; BLOOD CLOTTING FACTOR; THROMBOPLASTIN; VASCULOTROPIN;

ANGIOGENESIS; ASTROCYTOMA; BLOOD VESSEL OCCLUSION; BRAIN TUMOR; CELL MIGRATION; CLINICAL FEATURE; DISEASE MODEL; GLIOBLASTOMA; GLIOMA; HUMAN; HYPERPLASIA; HYPOXIA; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; THROMBOSIS; TUMOR NECROSIS; BLOOD VESSEL; CELL DIVISION; CELL HYPOXIA; NECROSIS; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGY; REVIEW; VASCULARIZATION;

BLOOD VESSELS; BRAIN NEOPLASMS; CELL DIVISION; CELL HYPOXIA; GLIOBLASTOMA; HUMANS; NECROSIS; NEOVASCULARIZATION, PATHOLOGIC; THROMBOPLASTIN; THROMBOSIS;

EID: 2342588221     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.3700070     Document Type: Short Survey

References (79)

1. CBTRUS. Statistical Report: Primary Brain Tumors in the United States, 1995-1999. Central Brain Tumor Registry of the United States: Chicago, IL, 2002.
2. Kleihues P, Burger PC, Collins VP, et al. Glioblastoma. In: Kleihues P, Cavenee WK (eds). Pathology and Genetics of Tumours of the Nervous System, 2nd edn. International Agency for Research on Cancer: Lyon, 2000, pp 29-39.
3. Taveras JM, Thompson HG, Pool JL. Should we treat glioblastoma multiforme? A study of survival in 425 cases. Am J Roentg 1962;87:473-479.
4. Mandonnet E, Delattre JY, Tanguy ML, et al. Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 2003;53:524-528.
5. Swanson KR, Bridge C, Murray JD, et al. Virtual and real brain tumors: using mathematical modeling to quantify glioma growth and invasion. J Neurol Sci 2003;216:1-10.
6. Brat DJ, Castellano-Sanchez A, Kaur B, et al. Genetic and biologic progression in astrocytomas and their relation to angiogenic dysregulation. Adv Anat Pathol 2002;9:24-36.
7. Daumas-Duport C, Scheithauer B, O'Fallon J, et al. Grading of astrocytomas. A simple and reproducible method. Cancer 1988;62:2152-2165.
8. Plate KH, Breier G, Weich HA, et al. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 1992;359:845-848.
9. Plate KH. Mechanisms of angiogenesis in the brain. J Neuropathol Exp Neurol 1999;58:313-320.
10. Takano S, Yoshii Y, Kondo S, et al. Concentration of vascular endothelial growth factor in the serum and tumor tissue of brain tumor patients. Cancer Res 1996;56:2185-2190.
11. Shweiki D, Itin A, Soffer D, et al. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1999;359:843-845.
12. Semenza GL. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 2001;7:345-350.
13. Kung AL, Wang S, Klco JM, et al. Suppression of tumor growth through disruption of hypoxia-inducible transcription. Nat Med 2000;6:1335-1340.
14. Plate KH, Breier G, Weich HA, et al. Vascular endothelial growth factor and glioma angiogenesis: coordinate induction of VEGF receptors, distribution of VEGF protein and possible in vivo regulatory mechanisms. Int J Cancer 1994;59:520-529.
15. Brat DJ, Van Meir EG. Glomeruloid microvascular proliferation orchestrated by VPF/VEGF: a new world of angiogenesis research. Am J Pathol 2001;158:789-796.
16. Straume O, Chappuis PO, Salvesen HB, et al. Prognostic importance of glomeruloid microvascular proliferation indicates an aggressive angiogenic phenotype in human cancers. Cancer Res 2002;62:6808-6811.
17. Bellail A, Hunter SB, Brat DJ, et al. Microregional extracellular molecular heterogeneity in brain modulates glioma cell invasion. Int J Biochem Cell Biol, (in press).
18. Rieger J, Naumann U, Glaser T, et al. APO2 ligand: a novel lethal weapon against malignant glioma? FEBS Lett 1998;427:124-128.
19. Hao C, Beguinot F, Condorelli G, et al. Induction and intracellular regulation of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) mediated apoptosis in human malignant glioma cells. Cancer Res 2001;61:1162-1170.
20. Tachibana O, Nakazawa H, Lampe J, et al. Expression of Fas/APO-1 during the progression of astrocytomas. Cancer Res 1995;55:5528-5530.
21. Gratas C, Tohma Y, Van Meir EG, et al. Fas ligand expression in glioblastoma cell lines and primary astrocytic brain tumors. Brain Pathol 1997;7:863-869.
22. Tachibana O, Lampe J, Kleihues P, et al. Preferential expression of Fas/APO1 (CD95) and apoptotic cell death in perinecrotic cells of glioblastoma multiforme. Acta Neuropathol (Berl) 1996;92:431-434.
23. Takekawa Y, Sawada T, Sakurai I. Expression of apoptosis and its related protein in astrocytic tumors. Brain Tumor Pathol 1999;16:11-16.
24. Saas P, Walker PR, Hahne M, et al. Fas ligand expression by astrocytoma in vivo: maintaining immune privilege in the brain? J Clin Invest 1997;99:1173-1178.
25. Migheli A, Cavalla P, Marino S, et al. A study of apoptosis in normal and pathologic nervous tissue after in situ end-labeling of DNA strand breaks. J Neuropathol Exp Neurol 1994;53:606-616.
26. Schiffer D, Cavalla P, Migheli A, et al. Apoptosis and cell proliferation in human neuroepithelial tumors. Neurosci Lett 1995;195:81-84.
27. Nelson JS, Tsukada Y, Schoenfeld D, et al. Necrosis as a prognostic criterion in malignant supratentorial, astrocytic gliomas. Cancer 1983;52:550-554.
28. Lacroix M, Abi-Said D, Fourney DR, et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 2001;95:190-198.
29. Burger PC, Green SB. Patient age, histologic features, and length of survival in patients with glioblastoma multiforme. Cancer 1987;59:1617-1625.
30. Curran Jr WJ, Scott CB, Horton J, et al. Recursive partitioning analysis of prognostic factors in three radiation therapy oncology group malignant glioma trials. J Natl Cancer Inst 1993;85:704-710.
31. Raza SM, Lang FF, Aggarwal BB, et al. Necrosis and glioblastoma: a friend or a foe? A review and a hypothesis. Neurosurgery 2002;51:2-12.
32. Dinda AK, Sarkar C, Roy S, et al. A transmission and scanning electron microscopic study of tumoral and peritumoral microblood vessels in human gliomas. J Neurooncol 1993;16:149-158.
33. Sawaya R, Yamamoto M, Ramo OJ, et al. Plasminogen activator inhibitor-1 in brain tumors: relation to malignancy and necrosis. Neurosurgery 1995;36:375-380.
34. Hamada K, Kuratsu J, Saitoh Y, et al. Expression of tissue factor correlates with grade of malignancy in human glioma. Cancer 1996;77:1877-1883.
35. Sawaya R, Ramo OJ, Shi ML, et al. Biological significance of tissue plasminogen activator content in brain tumors. J Neurosurg 1991;74:480-486.
36. Brat DJ, Castellano-Sanchez A, Hunter SB, et al. Pseudopalisading cells in glioblastoma are hypoxic, express extracellular matrix proteases, and are formed by a rapidly migrating population. Cancer Res 2004;64:910-919.
37. Zagzag D, Zhong H, Scalzitti JM, et al. Expression of hypoxia-inducible factor 1alpha in brain tumors: association with angiogenesis, invasion, and progression. Cancer 2000;88:2606-2618.
38. Krishnamachary B, Berg-Dixon S, Kelly B, et al. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res 2003;63:1138-1143.
39. Pennacchietti S, Michieli P, Galluzzo M, et al. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 2003;3:347-361.
40. Ben-Yosef Y, Lahat N, Shapiro S, et al. Regulation of endothelial matrix metalloproteinase-2 by hypoxia/ reoxygenation. Circ Res 2002;90:784-791.
41. Graham CH, Forsdike J, Fitzgerald CJ, et al. Hypoxia-mediated stimulation of carcinoma cell invasiveness via upregulation of urokinase receptor expression. Int J Cancer 1999;80:617-623.
42. Yamamoto M, Mohanam S, Sawaya R, et al. Differential expression of membrane-type matrix metalloproteinase and its correlation with gelatinase A activation in human malignant brain tumors in vivo and in vitro. Cancer Res 1996;56:384-392.
43. Mori T, Abe T, Wakabayashi Y, et al. Up-regulation of urokinase-type plasminogen activator and its receptor correlates with enhanced invasion activity of human glioma cells mediated by transforming growth factor-alpha or basic fibroblast growth factor. J Neurooncol 2000;46:115-123.
44. Holash J, Maisonpierre PC, Compton D, et al. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 1999;284:1994-1998.
45. Zagzag D, Amirnovin R, Greco MA, et al. Vascular apoptosis and involution in gliomas precede neovascularization: a novel concept for glioma and angiogenesis. Lab Invest 2000;80:837-849.
46. Zagzag D, Hooper A, Friedlander DR, et al. In situ expression of angiopoietins in astrocytomas identifies angiopoietin-2 as an early marker of tumor angiogenesis. Exp Neurol 1999;159:391-400.
47. Stratmann A, Risau W, Plate KH. Cell type-specific expression of angiopoietin-1 and angiopoietin-2 suggests a role in glioblastoma angiogenesis. Am J Pathol 1998;153:1459-1466.
48. Vajkoczy P, Farhadi M, Gaumann A, et al. Microtumor growth initiates angiogenic sprouting with simultaneous expression of VEGF, VEGF receptor-2, and angiopoietin-2. Clin Invest 2002;109:777-785.
49. Zhang L, Yang N, Park JW, et al. Tumor-derived vascular endothelial growth factor up-regulates angiopoietin-2 in host endothelium and destabilizes host vasculature, supporting angiogenesis in ovarian cancer. Cancer Res 2003;63:3403-3412.
50. Yu Q, Stamenkovic I. Angiopoietin-2 is implicated in the regulation of tumor angiogenesis. Am J Pathol 2001;158:563-570. 53.
51. Maisonpierre PC, Suri C, Jones PF, et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997;277:55-60.
52. Rickles FR, Falanga A. Molecular basis for the relationship between thrombosis and cancer. Thromb Res 2001;102:V215-V224.
53. Walsh DC, Kakkar AK. Thromboembolism in brain tumors. Curr Opin Pulm Med 2001;7:326-331.
54. Rodas RA, Fenstermaker RA, McKeever PE, et al. Correlation of intraluminal thrombosis in brain tumor vessels with postoperative thrombotic complications: a preliminary report. J Neurosurg 1998;89:200-205.
55. Kniesel U, Wolburg H. Tight junctions of the blood-brain barrier. Cell Mol Neurobiol 2000;20:57-76.
56. Long DM. Capillary ultrastructure and the blood-brain barrier in human malignant brain tumors. J Neurosurg 1970;32:127-144.
57. Zhu XP, Li KL, Kamaly-Asl ID, et al. Quantification of endothelial permeability, leakage space, and blood volume in brain tumors using combined T1 and T2* contrast-enhanced dynamic MR imaging. J Magn Reson Imaging 2000;11:575-585.
58. Sugahara T, Korogi Y, Kochi M, et al. Correlation of MR imaging-determined cerebral blood volume maps with histologic and angiographic determination of vascularity of gliomas. AJR Am J Roentgenol 1998;171:1479-1486.
59. Rascher G, Fischmann A, Kroger S, et al. Extracellular matrix and the blood-brain barrier in glioblastoma multiforme: spatial segregation of tenascin and agrin. Acta Neuropathol (Berl) 2002;104:85-91.
60. Senger DR, Galli SJ, Dvorak AM, et al. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983;219:983-985.
61. Fischer S, Clauss M, Wiesnet M, et al. Hypoxia induces permeability in brain microvessel endothelial cells via VEGF and NO. Am J Physiol 1999;276: C812-C820.
62. Versteeg HH, Peppelenbosch MP, Spek CA. Tissue factor signal transduction in angiogenesis. Carcinogenesis 2003;24:1009-1013.
63. Contrino J, Hair G, Kreutzer DL, et al. In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease. Nat Med 1996;2:209-215.
64. Vrana JA, Stang MT, Grande JP, et al. Expression of tissue factor in tumor stroma correlates with progression to invasive human breast cancer: paracrine regulation by carcinoma cell-derived members of the transforming growth factor beta family. Cancer Res 1996;56:5063-5070.
65. Seto S, Onodera H, Kaido T, et al. Tissue factor expression in human colorectal carcinoma: correlation with hepatic metastasis and impact on prognosis. Cancer 2000;88:295-301.
66. Guan M, Jin J, Su B, et al. Tissue factor expression and angiogenesis in human glioma. Clin Biochem 2002;35:321-325.
67. Yan SF, Mackman N, Kisiel W, et al. Hypoxia/ hypoxemia-induced activation of the procoagulant pathways and the pathogenesis of ischemia-associated thrombosis. Arterioscler Thromb Vasc Biol 1999;19:2029-2035.
68. Lawson CA, Yan SD, Yan SF, et al. Monocytes and tissue factor promote thrombosis in a murine model of oxygen deprivation. J Clin Invest 1997;99:1729-1738.
69. Yan SF, Lu J, Zou YS, et al. Hypoxia-associated induction of early growth response-1 gene expression. Biol Chem 1999;274:15030-15040.
70. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 2000;407:258-264.
71. Macfarlane SR, Seatter MJ, Kanke T, et al. Pharmacol Rev 2001;53:245-282.
72. Even-Ram S, Uziely B, Cohen P, et al. Thrombin receptor overexpression in malignant and physiological invasion processes. Nat Med 1998;4:909-914.
73. Darmoul D, Gratio V, Devaud H, et al. Aberrant expression and activation of the thrombin receptor protease-activated receptor-1 induces cell proliferation and motility in human colon cancer cells. Am J Pathol 2003;162:1503-1513.
74. Martin CB, Mahon GM, Klinger MB, et al. The thrombin receptor, PAR-1, causes transformation by activation of Rho-mediated signaling pathways. Oncogene 2001;20:1953-1963.
75. Marinissen MJ, Servitja JM, Offermanns S, et al. The thrombin receptor PAR-1 signals through Gq and G13-initiated MAPK cascades regulating c-jun expression to induce cell transformation. J Biol Chem 2003;278:46814-46825.
76. Yin YJ, Salah Z, Grisaru-Granovsky S, et al. Human protease-activated receptor 1 expression in malignant epithelia: a role in invasiveness. Arterioscler Thromb Vasc Biol 2003;23:940-944.
77. Even-Ram SC, Maoz M, Pokroy E, et al. Tumor cell invasion is promoted by activation of protease activated receptor-1 in cooperation with the alpha vbeta 5 integrin. J Biol Chem 2001;276:10952-10962.
78. Junge CE, Sugawara T, Mannaioni G, et al. The contribution of protease activated receptor-1 to neuronal damage caused by transient focal ischemia. Proc Natl Acad Sci USA 2003;100:13019-13024.
79. Junge CE, Lee CJ, Hubbard KB, et al. Protease activated receptor-1 (PAR1) in human brain: localization and functional expression in astrocytes. Exper Neurol, (in press).