The dynamic roles of angiopoietins in tumor angiogenesis

Future Oncology

Volumn 1, Issue 4, 2005, Pages 475-484

  Yu, Qin ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

angiopoietin; antiangiogenesis; cancer therapy; endothelial cell; extracellular matrix; heparan sulfate proteoglycan; metastasis; tumor angiogenesis

Indexed keywords

ANGIOPOIETIN;

ANIMAL; HUMAN; METABOLISM; MOUSE; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; VASCULARIZATION;

ANGIOPOIETINS; ANIMALS; HUMANS; MICE; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; SIGNAL TRANSDUCTION;

EID: 33744458204     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/14796694.1.4.475     Document Type: Review

References (96)

1. Bello L, Carrabba G, Giussani C et al.: Lowdose chemotherapy combined with an antiangiogenic drug reduces human glioma growth in vivo. Cancer Res. 61(20), 7501-7506 (2001
2. Novak K: Angiogenesis inhibitors revised and revived at AACR. American Association for Cancer Research. Nature Med. 8(5), 427 (2002
3. Garcia-Barros M, Paris F, Cordon-Cardo C et al.: Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 300(5622), 1155-1159 (2003
4. Hurwitz H, Fehrenbacher L, Novotny W et al.: Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 350, 2335-2342 (2004
5. Geng L, Donnelly E, McMahon G et al.: Inhibition of vascular endothelial growth factor receptor signaling leads to reversal of tumor resistance to radiotherapy. Cancer Res. 61(6), 2413-2419 (2001
6. Hainsworth J, Sosman J, Spigel D et al.: Phase II trial of bevacizumab and erlotinib in patients with metastatic renal carcinoma (RCC). Proc. Am. Soc. Clin. Oncol. 381, [Abstract 4502] (2004
7. Yang JC, Haworth L, Sherry RM et al.: A randomized trial of bevacizumab, an antivascular endothelial growth factor antibody, for metastatic renal cancer. N. Engl. J. Med. 349, 427-434 (2003
8. Gale NW, Yancopoulos GD: Growth factors acting via endothelial cell-specific receptor tyrosine kinases: VEGFs, angiopoietins, and ephrins in vascular development. Genes Dev. 13, 1055-1066 (1999
9. Hanahan D, Folkman J: Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364 (1996
10. Hanahan D, Weinberg RA: The hallmarks of cancer. Cell 100, 57-70 (2000
11. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J: Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248 (2000
12. Peters KG, Kontos CD, Lin PC et al.: Functional significance of Tie2 signaling in the adult vasculature. Recent Prog. Horm. Res. 59, 51-71 (2004
13. Loughna S, Sato TN: Angiopoietin and Tie signaling pathways in vascular development. Matrix Biol. 20(5-6), 319-325 (2001
14. Ward NL, Dumont DJ: The angiopoietins and Tie-2/Tek: adding to the complexity of cardiovascular development. Semin. Cell Dev. Biol. 13(1), 19-27 (2002
15. Davis S, Aldrich TH, Jones PF et al.: Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-Trap expression cloning. Cell 87, 1161-1169 (1996
16. Maisonpierre PC, Suri C, Jones PF et al.: Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277, 55-60 (1997
17. Valenzuela DM, Griffiths JA, Rojas J et al.: Agiopoietins 3 and 4: diverging gene counterparts in mice and humans. Proc. Natl Acad. Sci. USA 96, 1904-1909 (1999
18. Dumont DJ, Gradwohl G, Fong GH et al.: Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, TEK, reveal a critical tole in vasculogenesis of the embryo. Genes Dev. 8, 1897-1909 (1994
19. Sato TN, Tozawa Y, Deutsch U et al.: Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376, 70-74 (1995
20. Suri C, Jones PF, Patan S et al.: Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87, 1171-1180 (1996
21. Suri C, McClain J, Thursyon G et al.: Increased vascularization in mice overexpressing angiopoietin-1. Science 282, 468-471 (1998
22. Thurston G, Suri C, Smith K et al.: Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-Science 286, 2511-2514 (1999)
23. Thurston G, Rudge JS, Ioffe E et al.: Angiopoietin-1 protects the adult vasculature against plasma leakage. Nature Med. 6, 460-463 (2000
24. Gale NW, Thurston G, Hackett SF et al.: Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by angiopoietin-1. Dev. Cell 3(3), 411-23 (2002
25. Procopio WN, Pelavin PI, Lee WMF, Yeilding NM: Angiopoietin-1 and -2 coiled ciol domains mediate distinct homooligomerization patterns, but fibrinogenlike domains mediate ligand activity. J. Biol. Chem. 274, 30196-30201 (1999
26. Yu Q, Stamenkovic I: Angiopoietin-2 is implicated in the regulation of tumor angiogenesis. Am. J. Pathol. 158, 563-570 (2001
27. Xu Y, Yu Q: Angiopoietin-1, unlike angiopoietin-2, is incorporated into the extracellular matrix via its linker peptide region. J. Biol. Chem. 276, 34990-34998 (2001
28. Xu Y, Liu YJ, Yu Q: Angiopoietin-3 is tethered on the cell surface via heparan sulfate proteoglycans. J. Biol. Chem. 279(39), 41179-41188 (2004
29. Davis S, Papadopoulos N, Aldrich TH et al.: Angiopoietins have distinct modular domains essential for receptor binding, dimerization and superclustering. Nature Struct. Biol. 10, 38-44 (2002
30. Kim KT, Choi HH, Steinmetz MO et al.: Oligomerization and multimerization are critical for angiopoietin-1 to bind and phosphorylate Tie-2. J. Biol. Chem. 280(20), 20126-20131 (2005
31. Fiedler U, Krissl T, Koidl S et al.: Angiopoietin-1 and angiopoietin-2 share the same binding domains in the Tie-2 receptor involving the first Ig-like loop and the epidermal growth factor-like repeats. J. Biol. Chem. 278(3), 1721-1727 (2003
32. Teichert-Kuliszewska K, Maisonpierre PC, Jones N et al.: Biological action of angiopoietin-2 in a fibrin matrix model of angiogenesis is associated with activation of Tie-2. Cardiovasc. Res. 49, 659-670 (2001
33. Mochizuki Y, Nakamura T, Kanetake H, Kanda S: Angiopoietin 2 stimulates migration and tube-like structure formation of murine brain capillary endothelial cells through c-Fes and c-Fyn. J. Cell Sci. 115(Pt 1), 175-183 (2002
34. Lee HJ, Cho CH, Hwang SJ et al.: Biological characterization of angiopoietin-3 and angiopoietin-4. FASEB J. 18(11), 1200-1208 (2004
35. Yamakawa M, Liu LX, Date T et al.: Hypoxia-inducible factor-1 mediates activation of cultured vascular endothelial cells by inducing multiple angiogenic factors. Circ. Res. 93(7), 664-673 (2003
36. Holash J, Maisonpierre D, Compton D et al.: Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 284, 1994-1998 (1999
37. Asahara T, Chen D, Takahashi T et al.: Tie2 receptor ligands, angiopoietin-1 and angiopoietin-2, modulate VEGF-induced postnatal neovascularization. Circ. Res. 83, 233-240 (1998
38. Vajkoczy P, Farhadi M, Gaumann A et al.: Microtumor growth initiates angiogenic sprouting with simultaneous expression of VEGF, VEGF receptor-2, and angiopoietin-2. J. Clin. Invest. 109, 777-785 (2002
39. Koblizek TI, Weiss C, Yancopoulos GD, Deutsch U, Risau W: Angiopoietin-1 induces sprouting angiogenesis in vitro. Curr. Biol. 8, 529-532 (1998
40. Xu Y, Liu YJ, Yu Q : Angiopoietin-3 inhibits pulmonary metastasis by inhibiting tumor angiogenesis. Cancer Res. 64(17), 6119-6126 (2004
41. Visconti RP, Richardson CD, Sato TN: Orchestration of angiogenesis and arteriovenous contribution by angiopoietins and vascular endothelial growth factor (VEGF). Proc. Natl Acad. Sci. USA 99, 8219-8224 (2002
42. Carlson TR, Feng Y, Maisonpierre PC, Mrksich M, Morla AO: Direct cell adhesion to the angiopoietins mediated by integrins. J. Biol. Chem. 276, 26516-26525 (2001
43. Papapetropoulos A, Fulton D, Mahboubi K et al.: Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/survivin pathway. J. Biol. Chem. 275, 9102-9105 (2000
44. Kim I, Kim HG, So JN, Kim JH, Kwak HJ, Koh GY: Angiopoietin-1 regulates endothelial cell survival through the phosphatidylinositol 3-kinase/Akt signal transduction pathway. Circ. Res. 86, 24-29 (2000
45. Harfouche R, Hassessian HM, Guo Y et al.: Mechanisms which mediate the antiapoptotic effects of angiopoietin-1 on endothelial cells. Microvasc. Res. 64, 135-147 (2002
46. Kim I, Ryu YS, Kwak HJ et al.: EphB ligand, ephrinB2, suppresses the VEGF-and angiopoietin 1-induced Ras/mitogen activated protein kinase pathway in venous endothelial cells. FASEB J. 16, 1126-1128 (2002
47. Hayes AJ, Huang WQ, Mallah J, Yang D, Lippman ME, Li LY: Angiopoietin-1 and its receptor Tie-2 participate in the regulation of capillary-like tubule formation and survival of endothelial cells. Microvasc. Res. 58, 224-237 (1999
48. Kim I, Kim HG, Moon S-O et al.: Angiopoietin-1 induces endothelial cell sprouting through the activation of focal adhesion kinase and plasmin secretion. Circ. Res. 86, 952-959 (2000
49. Saharinen P, Kerkela K, Ekman N et al.: Multiple angiopoietin recombinant proteins activate the Tie1 receptor tyrosine kinase and promote its interaction with Tie2. J. Cell Biol. 169(2), 239-243 (2005
50. Sato TN, Quin Y, Kozak CA, Audus KL: Tie-1 and Tie-2 define another class of putative receptor tyrosine kinase genes expressed in early embryonic vascular system. Proc. Natl Acad. Sci. USA 90, 9355-9358 (1993
51. Shih SC, Robinson GS, Perruzzi CA et al.: Molecular profiling of angiogenesis markers. Am. J. Pathol. 161(1), 35-41 (2002
52. Van der Auwera I, Van Laere SJ, Van der Eynden GG et al.: Increased angiogenesis and lymphangiogenesis in inflammatory versus noninflammatory breast cancer by real-time reverse transcriptase-PCR gene expression quantification. Clin. Cancer Res. 10(23), 7965-79671 (2004
53. Karnani P, Kairemo K: The new Tie-1 monoclonal antibodies detect angiogenesis in metastatic malignancies. Clin. Cancer Res. 9(10 Pt 2), S3827-S3823 (2003
54. Lin WC, Li AF, Chi CW et al.: Tie-1 protein tyrosine kinase: a novel independent prognostic marker for gastric cancer. Clin. Cancer Res. 5(7), 1745-1751 (1999
55. Dallabrida SM, Ismail N, Oberle JR, Himes BE, Rupnick MA: Ang-1 promotes cardiac and skeletal myocyte survival through integrins. Circ. Res. 96(4), e8-e24 (2005
56. Lin P, Polverini P, Dewhirst M, Shan S, Rao PS, Peter KG: Inhibition of tumor angiogenesis using a soluble receptor establishes a role for Tie-2 in pathologic vascular growth. J. Clin. Invest. 100, 2072-2078 (1997)
57. Lin P, Buxton JA, Acheson A et al.: Antiangiogenic gene therapy targeting the endothelium-specific receptor tyrosine kinase Tie2. Proc. Natl Acad. Sci. USA. 95, 8829-8834 (1998
58. Tait CR, Jones PF: Angiopoietins in tumours: the angiogenic switch. J. Pathol. 204(1), 1-10 (2004
59. Jones PF: Not just angiogenesis-wider roles for the angiopoietins. J. Pathol. 201, 515-527 (2003
60. Sfiligoi C, de Luca A, Cascone I et al.: Angiopoietin-2 expression in breast cancer correlates with lymph node invasion and short survival. Int. J. Cancer. 103(4), 466-474 (2003
61. Tanaka F, Ishikawa S, Yanagihara K: Expression of angiopoietins and its clinical significance in non-small cell lung cancer. Cancer Res. 62(23), 7124-7129 (2002
62. Guo P, Imanishi Y, Cackowski FC et al.: Upregulation of angiopoietin-2, matrix metalloprotease-2, membrane Type 1 metalloprotease, and laminin 52 correlates with the invasiveness of human glioma. Am. J. Pathol. 166(3), 877-890 (2005
63. Lind AJ, Wikstrom P, Granfors T, Egevad L, Stattin P, Bergh A: Angiopoietin 2 expression is related to histological grade, vascular density, metastases, and outcome in prostate cancer. Prostate 62(4), 394-399 (2005
64. Zhang L, Yang N, Park JW et al.: Tumorderived vascular endothelial growth factor upregulates angiopoietin-2 in host endothelium and destabilizes host vasculature, supporting angiogenesis in ovarian cancer. Cancer Res. 63(12), 3403-3412 (2003
65. Ogawa M, Yamamoto H, Nagano H et al.: Hepatic expression of ANG2 RNA in metastatic colorectal cancer. Hepatology 39(2), 528-539 (2004
66. Ochiumi T, Tanaka S, Oka S et al.: Clinical significance of angiopoietin-2 expression at the deepest invasive tumor site of advanced colorectal carcinoma. Int. J. Oncol. 24(3), 539-547 (2004
67. Brown LF, Dezube BJ, Tognazzi K, Dvorak HF, Yancopoulos GD: Expression of Tie1, Tie2, and angiopoietins 1, 2 and 4 in Kaposis sarcoma and cutaneous angiosarcoma. Am. J. Pathol. 156(6), 2179-2183 (2000
68. Ahmad SA, Liu W, Jung YD et al.: Differential expression of angiopoietin-1 and angiopoietin-2 in colon carcinoma. A possible mechanism for the initiation of angiogenesis. Cancer 92(5), 1138-1143 (2001
69. 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. 61(5), 2145-2153 (2001
70. Hu B, Guo P, Fang Q et al.: Angiopoietin-2 induces human glioma invasion through the activation of matrix metalloprotease-2. Proc. Natl Acad. Sci. USA 100(15), 8904-8909 (2003
71. 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 99(17), 11205-11210 (2002
72. Oliner J, Min H, Leal J et al.: Suppression of angiogenesis and tumor growth by selective inhibition of angiopoietin-2. Cancer Cell 6(5), 507-516 (2004
73. Loges S, Heil G, Bruweleit M et al.: Analysis of concerted expression of angiogenic growth factors in acute myeloid leukemia: expression of angiopoietin-2 represents an independent prognostic factor for overall survival. J. Clin. Oncol. 23(6), 1109-1117 (2005
74. Machein MR, Knedla A, Knoth R, Wagner S, Neuschl E, Plate KH: Angiopoietin-1 promotes tumor angiogenesis in a rat glioma model. Am. J. Pathol. 165(5), 1557-1570 (2004
75. Metheny-Barlow LJ, Li LY: The enigmatic role of angiopoietin-1 in tumor angiogenesis. Cell Res. 13(5), 309-317 (2003
76. Hayes AJ, Huang WQ, Yu J et al.: Expression and function of angiopoietin-1 in breast cancer. Br. J. Cancer 83(9), 1154-1160 (2000
77. Stoeltzing O, Ahmad SA, Liu W et al.: Angiopoietin-1 inhibits vascular permeability, angiogenesis, and growth of hepatic colon cancer tumors. Cancer Res. 63(12), 3370-3377 (2003
78. Stoeltzing O, Ahmad SA, Liu W et al.: Angiopoietin-1 inhibits tumour growth and ascites formation in a murine model of peritoneal carcinomatosis. Br. J. Cancer 87(10), 1182-1187 (2002
79. Nakayama T, Yao L, Tosato G: Mast cellderived angiopoietin-1 plays a critical role in the growth of plasma cell tumors. J. Clin. Invest. 114(9), 1317-1325 (2004
80. Shim WS, Teh M, Bapna A et al.: Angiopoietin 1 promotes tumor angiogenesis and tumor vessel plasticity of human cervical cancer in mice. Exp. Cell. Res. 279(2), 299-309 (2002
81. Zadeh G, Koushan K, Pillo L, Shannon P, Guha A: Role of Ang1 and its interaction with VEGF-A in astrocytomas. J. Neuropathol. Exp. Neurol. 63(9), 978-989 (2004
82. Winkler F, Kozin SV, Tong RT et al.: Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 6(6), 553-563 (2004
83. Oh H, Takagi H, Suzuma K, Otani A, Matsumura M, Honda Y: Hypoxia and vascular endothelial growth factor selectively upregulate angiopoietin-2 in bovine microvascular endothelial cells. J. Biol. Chem. 274, 15732-15739 (1999
84. Mandriota SJ, Pepper MS: Regulation of angiopoietin-2 mRNA levels in bovine microvascular endothelial cells by cytokines and hypoxia. Circ. Res. 83, 852-859 (1998
85. Kim I, Kim JH, Ryu YS, Liu M, Koh GY: Tumor necrosis factor-upregulates angiopoietin-2 in human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 269(2), 361-365 (2000
86. Kelly BD, Hackett SF, Hirota K et al.: Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxiainducible factor 1. Circ. Res. 93(11), 1074-1081 (2003
87. Pichiule P, Chavez JC, LaManna JC. Hypoxic regulation of angiopoietin-2 expression in endothelial cells. J. Biol. Chem. 279(13), 12171-12180 (2004
88. Fan F, Stoeltzing O, Liu W et al.: Interleukin-1regulates angiopoietin-1 expression in human endothelial cells. Cancer Res. 64(9), 3186-3190 (2004
89. Park YS, Kim NH, Jo I: Hypoxia and vascular endothelial growth factor acutely up-regulate angiopoietin-1 and Tie-2 mRNA in bovine retinal pericytes. Microvasc. Res. 65(2), 125-131 (2003
90. Scott BB, Zaratin PF, Colombo A, Hansbury MJ, Winkler JD, Jackson JR: Constitutive expression of angiopoietin-1 and -2 and modulation of their expression by inflammatory cytokines in rheumatoid arthritis synovial fibroblasts. J. Rheumatol. 29(2), 230-239 (2002
91. Scott BB, Zaratin PF, Gilmartin AG et al.: TNF-βmodulates angiopoietin-1 expression in rheumatoid synovial fibroblasts via the NF-κB signaling pathway. Biochem. Biophys. Res. Commun. 328(2), 409-414 (2005
92. Jansen M, de Witt Hamer PC, Witmer AN, Troost D, van Noorden CJ: Current perspectives on anti-angiogenesis strategies in the treatment of malignant gliomas. Brain Res. Brain Res. Rev. 45(3), 143-163 (2004
93. Ruhrberg C: Endogenous inhibitors of angiogenesis. J. Cell Sci. 114, 3215-3216 (2001
94. Saaristo A, Karpanen T, Alitalo K: Mechanisms of angiogenesis and their use in the inhibition of tumor growth and metastasis. Oncogene 19, 6122-6129 (2000
95. Maeshima Y, Sudhakar A, Lively JC et al.: Tumstatin, an endothelial cell-specific inhibitor of protein synthesis. Science 295, 140-143 (2002
96. Hanahan D: Signaling vascular morphogenesis and maintenance. Science 277, 48-50 (1997