Angiopoietin-1 promotes tumor angiogenesis in a rat glioma model

American Journal of Pathology

Volumn 165, Issue 5, 2004, Pages 1557-1570

  Machein, Marcia Regina ^a   Knedla, Anette ^b   Knoth, Rolf ^a   Wagner, Shawn ^c   Neuschl, Elvira ^a   Plate, Karl H ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^c MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL MODEL; ARTICLE; BRAIN TUMOR; CANCER CELL CULTURE; CONTROLLED STUDY; GENETIC TRANSFECTION; GLIOMA; GLIOMA CELL; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PERICYTE; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TUMOR GROWTH; TUMOR VASCULARIZATION;

EID: 7244229595     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63413-X     Document Type: Article

References (41)

1. Carmeliet P, Jain RK: Angiogenesis in cancer and other diseases. Nature 2000, 407:249-257
2. Hanahan D, Folkman J: Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996, 86:353-364
3. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, Ryan TE, Bruno J, Radziejewski C, Maisonpierre PC, Yancopoulos GD: Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 1996, 87:1161-1169
4. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radzejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN, Yancopoulos GD: Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997, 277:55-60
5. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD: Requisite role of angiopoletin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996, 87:1171-1180
6. Witzenbichler B, Maisonpierre PC, Jones P, Yancopoulos GD, Isner JM: Chemotactic properties of angiopoietin-1 and -2, ligands for the endothelial-specific receptor tyrosine kinase Tie2. J Biol Chem 1998, 273:18514-18521
7. Iurlaro M, Scatena M, Zhu WH, Fogel E, Wieting SL, Nicosia RF: Rat aorta-derived mural precursor cells express the Tie2 receptor and respond directly to stimulation by angiopoietins. J Cell Sci 2003, 116:3635-3643
8. Shim WS, Teh M, Mack PO, Ge R: Inhibition of angiopoietin-1 expression in tumor cells by an antisense RNA approach inhibited xenograft tumor growth in immunodeficient mice. Int J Cancer 2001, 94:6-15
9. Hayes AJ, Huang WQ, Yu J, Maisonpierre PC, Liu A, Kern FG, Lippman ME, McLeskey SW, Li LY: Expression and function of angiopoietin-1 in breast cancer. Br J Cancer 2000, 83:1154-1160
10. Hawighorst T, Skobe M, Streit M, Hong YK, Velasco P, Brown LF, Riccardi L, Lange-Asschenfeldt B, Detmar M: Activation of the tie2 receptor by angiopoietin-1 enhances tumor vessel maturation and impairs squamous cell carcinoma growth. Am J Pathol 2002, 160:1381-1392
11. Tian S, Hayes AJ, Metheny-Barlow LJ, Li LY: Stabilization of breast cancer xenograft tumour neovasculature by angiopoietin-1. Br J Cancer 2002, 86:645-651
12. Yu Q, Stamenkovic I: Angiopoietin-2 is implicated in the regulation of tumor angiogenesis. Am J Pathol 2001, 158:563-570
13. Ahmad SA, Liu W, Jung YD, Fan F, Reinmuth N, Bucana CD, Ellis LM: Differential expression of angiopoietin-1 and angiopoietin-2 in colon carcinoma: a possible mechanism for the initiation of angiogenesis. Cancer 2001, 92:1138-1143
14. Etoh T, Inoue H, Tanaka S, Barnard GF, Kitano S, Mori M: Angiopoietin-2 is related to tumor angiogenesis in gastric carcinoma: possible in vivo regulation via induction of proteases. Cancer Res 2001, 61:2145-2153
15. Tanaka S, Sugimachi K, Yamashita Y, Shirabe K, Shimada M, Wands JR, Sugimachi K: Angiogenic switch as a molecular target of malignant tumors. J Gastroenterol 2003, 38(Suppl 15):93-97
16. Plate KH, Breier G, Risau W: Molecular mechanisms of developmental and tumor angiogenesis. Brain Pathol 1994, 4:207-218
17. 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
18. Zagzag D, Hooper A, Friedlander DR, Chan W, Holash J, Wiegand SJ, Yancopoulos GD, Grumet M: In situ expression of angiopoietins in astrocytomas identifies angiopoietin-2 as an early marker of tumor angiogenesis. Exp Neurol 1999, 159:391-400
19. Koga K, Todaka T, Morioka M, Hamada J, Kai Y, Yano S, Okamura A, Takakura N, Suda T, Ushio Y: Expression of angiopoietin-2 in human glioma cells and its role for angiogenesis. Cancer Res 2001, 61:6248-6254
20. Machein MR, Risau W, Plate KH: Antiangiogenic gene therapy in a rat glioma model using a dominant-negative vascular endothelial growth factor receptor 2. Hum Gene Ther 1999, 10:1117-1128
21. Uyama O, Okamura N, Yanase M, Narita M, Kawabata K, Sugita M: Quantitative evaluation of vascular permeability in the gerbil brain after transient ischemia using Evans blue fluorescence. J Cereb Blood Flow Metab 1988, 8:282-284
22. Eberhard A, Kahlert S, Goede V, Hemmerlein B, Plate KH, Augustin HG: Heterogeneity of angiogenesis and blood vessel maturation in human tumors: implications for antiangiogenic tumor therapies. Cancer Res 2000, 60:1388-1393
23. Stoeltzing O, Ahmad SA, Liu W, McCarty MF, Parikh AA, Fan F, Reinmuth N, Bucana CD, Ellis LM: Angiopoietin-1 inhibits tumour growth and ascites formation in a murine model of peritoneal carcinomatosis. Br J Cancer 2002, 87:1182-1187
24. Stoeltzing O, Ahmad SA, Liu W, McCarty MF, Wey JS, Parikh AA, Fan F, Reinmuth N, Kawaguchi M, Bucana CD, Ellis LM: Angiopoietin-1 inhibits vascular permeability, angiogenesis, and growth of hepatic colon cancer tumors. Cancer Res 2003, 63:3370-3377
25. Shim WS, Teh M, Bapna A, Kim I, Koh GY, Mack PO, Ge R: Angiopoietin 1 promotes tumor angiogenesis and tumor vessel plasticity of human cervical cancer in mice. Exp Cell Res 2002, 279:299-309
26. Tanaka S, Mori M, Sakamoto Y, Makuuchi M, Sugimachi K, Wands JR: Biologic significance of angiopoietin-2 expression in human hepatocellular carcinoma. J Clin Invest 1999, 103:341-345
27. Thurston G, Suri C, Smith K, McClain J, Sato TN, Yancopoulos GD, McDonald DM: Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 1999, 286:2511-2514
28. Pettersson A, Nagy JA, Brown LF, Sundberg C, Morgan E, Jungles S, Carter R, Krieger JE, Manseau EJ, Harvey VS, Eckelhoefer IA, Feng D, Dvorak AM, Mulligan RC, Dvorak HF: Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor. Lab Invest 2000, 80:99-115
29. Nehls V, Schuchardt E, Drenckhahn D: The effect of fibroblasts, vascular smooth muscle cells, and pericytes on sprout formation of endothelial cells in a fibrin gel angiogenesis system. Microvasc Res 1994, 48:349-363
30. Lauren J, Gunji Y, Alitalo K: Is angiopoietin-2 necessary for the initiation of tumor angiogenesis? Am J Pathol 1998, 153:1333-1339
31. Holash J, Wiegand SJ, Yancopoulos GD: New model of tumor angiogenesis: dynamic balance between vessel regression and growth mediated by angiopoietins and VEGF. Oncogene 1999, 18:5356-5362
32. Benjamin LE, Hemo I, Keshet E: A plasticity window for blood vessel remodelling is defined by pericyte coverage of the pre-formed endothelial network and is regulated by PDGF-B and VEGF. Development 1998, 125:1591-1598
33. Niu Q, Perruzzi C, Voskas D, Lawler J, Dumont DJ, Benjamin LE: Inhibition of Tie-2 signaling induces endothelial cell apoptosis, decreases Akt signaling, and induces endothelial cell expression of the endogenous anti-angiogenic molecule, thrombospondin-1. Cancer Biol Ther 2004, 3:402-405
34. Carlson TR, Feng Y, Maisonpierre PC, Mrksich M, Morla AO: Direct cell adhesion to the angiopoietins mediated by integrins. J Biol Chem 2001, 276:26516-26525
35. Kim I, Kim JH, Moon SO, Kwak HJ, Kim NG, Koh GY: Angiopoietin-2 at high concentration can enhance endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Oncogene 2000, 19:4549-4552
36. Lobov IB, Brooks PC, Lang RA: Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc Natl Acad Sci USA 2002, 99:11205-11210
37. Hu B, Guo P, Fang Q, Tao HQ, Wang D, Nagane M, Huang HJ, Gunji Y, Nishikawa R, Alitalo K, Cavenee WK, Cheng SY: Angiopoietin-2 induces human glioma invasion through the activation of matrix metalloprotease-2. Proc Natl Acad Sci USA 2003, 100:8904-8909
38. Thurston G, Rudge JS, Ioffe E, Zhou H, Ross L, Croll SD, Glazer N, Holash J, McDonald DM, Yancopoulos GD: Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med 2000, 6:460-463
39. Stratmann A, Acker T, Burger AM, Amann K, Risau W, Plate KH: Differential inhibition of tumor angiogenesis by tie2 and vascular endothelial growth factor receptor-2 dominant-negative receptor mutants. Int J Cancer 2001, 91:273-282
40. Lin P, Buxton JA, Acheson A, Radziejewski C, Maisonpierre PC, Yancopoulos GD, Channon KM, Hale LP, Dewhirst MW, George SE, Peters KG: Antiangiogenic gene therapy targeting the endothelium-specific receptor tyrosine kinase Tie2. Proc Natl Acad Sci USA 1998, 95:8829-8834
41. Zadeh G, Qian B, Okhowat A, Sabha N, Kontos CD, Guha A: Targeting the Tie2/Tek receptor in astrocytomas. Am J Pathol 2004, 164:467-476