Resistance to antiangiogenic therapy is directed by vascular phenotype, vessel stabilization, and maturation in malignant melanoma

Journal of Experimental Medicine

Volumn 207, Issue 3, 2010, Pages 491-503

  Helfrich, Iris ^a,b,c   Scheffrahn, Inka ^a   Bartling, Sönke ^c   Weis, Joachim ^d   Von Felbert, Verena ^d   Middleton, Mark ^e   Kato, Masahi ^f   Ergün, Süleyman ^a   Schadendorf, Dirk ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d RWTH AACHEN UNIVERSITY   (Germany)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f CHUBU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ANGIOGENESIS INHIBITOR; BEVACIZUMAB; DESMIN; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN RET; VASCULOTROPIN ANTIBODY; VATALANIB;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC THERAPY; ARTICLE; BLOOD VESSEL DIAMETER; BLOOD VESSEL WALL; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MELANOMA; MOUSE; NONHUMAN; PERICYTE; PHENOTYPE; PRIORITY JOURNAL; TREATMENT RESPONSE; TUMOR GROWTH; TUMOR VASCULARIZATION; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; CELL DIVISION; CELL HYPOXIA; DESMIN; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOMA; MICE; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; PHENOTYPE; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77949494504     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20091846     Document Type: Article

References (57)

1. Abramsson, A., P. Lindblom, and C. Betsholtz. 2003. Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors. J. Clin. Invest. 112:1142-1151.
2. Andrae, J., R. Gallini, and C. Betsholtz. 2008. Role of platelet-derived growth factors in physiology and medicine. Genes Dev. 22:1276-1312. doi:10.1101/gad.1653708
3. Armulik, A., A. Abramsson, and C. Betsholtz. 2005. Endothelial/pericyte interactions. Circ. Res. 97:512-523. doi:10.1161/01.RES.0000182903 .16652.d7
4. Benjamin, L.E., I. Hemo, and E. Keshet. 1998. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development. 125:1591-1598.
5. Bergers, G., S. Song, N. Meyer-Morse, E. Bergsland, and D. Hanahan. 2003. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J. Clin. Invest. 111:1287-1295.
6. Betsholtz, C., P. Lindblom, and H. Gerhardt. 2005. Role of pericytes in vascular morphogenesis. EXS. 94:115-125.
7. Bingle, L., N.J. Brown, and C.E. Lewis. 2002. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J. Pathol. 196:254-265. doi:10.1002/path.1027
8. Carlson, T.R., Y. Feng, P.C. Maisonpierre, M. Mrksich, and A.O. Morla. 2001. Direct cell adhesion to the angiopoietins mediated by integrins. J. Biol. Chem. 276:26516-26525. doi:10.1074/jbc.M100282200
9. Carmeliet, P. 2005. Angiogenesis in life, disease and medicine. Nature. 438:932-936. doi:10.1038/nature04478
10. de Visser, K.E., and L.M. Coussens. 2006. The inflammatory tumor micro-environment and its impact on cancer development. Contrib. Microbiol. 13:118-137. doi:10.1159/000092969
11. Döme, B., S. Paku, B. Somlai, and J. Tímár. 2002. Vascularization of cutaneous melanoma involves vessel co-option and has clinical significance. J. Pathol. 197:355-362. doi:10.1002/path.1124
12. Erber, R., A. Thurnher, A.D. Katsen, G. Groth, H. Kerger, H.P. Hammes, M.D. Menger, A. Ullrich, and P. Vajkoczy. 2004. Combined inhibition of VEGF and PDGF signaling enforces tumor vessel regression by interfering with pericyte-mediated endothelial cell survival mechanisms. FASEB J. 18:338-340.
13. Escudier, B., T. Eisen, W.M. Stadler, C. Szczylik, S. Oudard, M. Siebels, S. Negrier, C. Chevreau, E. Solska, A.A. Desai, et al; TARGET Study Group. 2007. Sorafenib in advanced clear-cell renal-cell carcinoma. N. Engl. J. Med. 356:125-134. doi:10.1056/NEJMoa060655
14. Fallowfield, M.E., and M.G. Cook. 1991. The vascularity of primary cutaneous melanoma. J. Pathol. 164:241-244. doi:10.1002/path.1711640309
15. Ferrara, N., and R.S. Kerbel. 2005. Angiogenesis as a therapeutic target. Nature. 438:967-974. doi:10.1038/nature04483
16. Ferrara, N., K.J. Hillan, H.P. Gerber, and W. Novotny. 2004. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat. Rev. Drug Discov. 3:391-400. doi:10.1038/nrd1381
17. Fiedler, U., and H.G. Augustin. 2006. Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol. 27:552-558. doi:10.1016/j.it.2006.10.004
18. Fiedler, U., M. Scharpfenecker, S. Koidl, A. Hegen, V. Grunow, J.M. Schmidt, W. Kriz, G. Thurston, and H.G. Augustin. 2004. The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Palade bodies. Blood. 103:4150-4156. doi:10.1182/blood-2003-10-3685
19. Folkman, J., K. Watson, D. Ingber, and D. Hanahan. 1989. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature. 339:58-61. doi:10.1038/339058a0
20. Gerhardt, H., and C. Betsholtz. 2003. Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res. 314:15-23. doi:10.1007/s00441-003-0745- x
21. Gupta, R., M. Grasruck, C. Suess, S.H. Bartling, B. Schmidt, K. Stierstorfer, S. Popescu, T. Brady, and T. Flohr. 2006. Ultra-high resolution flat-panel volume CT: fundamental principles, design architecture, and system characterization. Eur. Radiol. 16:1191-1205. doi:10.1007/s00330-006-0156- y
22. Hagemann, T., S.K. Biswas, T. Lawrence, A. Sica, and C.E. Lewis. 2009. Regulation of macrophage function in tumors: the multifaceted role of NFkappaB. Blood. 113:3139-3146. doi:10.1182/blood-2008-12-172825
23. Hanahan, D. 1997. Signaling vascular morphogenesis and maintenance. Science. 277:48-50. doi:10.1126/science.277.5322.48
24. Hanahan, D., and J. Folkman. 1996. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 86:353-364. doi:10.1016/S0092-8674(00)80108-7
25. Helfrich, I., L. Edler, A. Sucker, M. Thomas, S. Christian, D. Schadendorf, and H.G. Augustin. 2009. Angiopoietin-2 levels are associated with disease progression in metastatic malignant melanoma. Clin. Cancer Res. 15:1384-1392. doi:10.1158/1078-0432.CCR-08-1615
26. Hellström, M., M. Kalén, P. Lindahl, A. Abramsson, and C. Betsholtz. 1999. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development. 126:3047-3055.
27. Hess-Stumpp, H., M. Haberey, and K.H. Thierauch. 2005. PTK 787/ZK 222584, a tyrosine kinase inhibitor of all known VEGF receptors, represses tumor growth with high efficacy. ChemBioChem. 6:550-557. doi:10.1002/cbic.200400305
28. Holash, J., P.C. Maisonpierre, D. Compton, P. Boland, C.R. Alexander, D. Zagzag, G.D. Yancopoulos, and S.J. Wiegand. 1999. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science. 284:1994-1998. doi:10.1126/science.284.5422.1994
29. Hurwitz, H., L. Fehrenbacher, W. Novotny, T. Cartwright, J. Hainsworth, W. Heim, J. Berlin, A. Baron, S. Griffing, E. Holmgren, et al. 2004. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 350:2335-2342. doi:10.1056/NEJMoa032691
30. Ilmonen, S., A.L. Kariniemi, T. Vlaykova, T. Muhonen, S. Pyrhönen, and S. Asko-Seljavaara. 1999. Prognostic value of tumour vascularity in primary melanoma. Melanoma Res. 9:273-278.
31. Jain, R.K. 2005. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 307:58-62. doi:10.1126/science. 1104819
32. Kato, M., M. Takahashi, A.A. Akhand, W. Liu, Y. Dai, S. Shimizu, T. Iwamoto, H. Suzuki, and I. Nakashima. 1998. Transgenic mouse model for skin malignant melanoma. Oncogene. 17:1885-1888. doi:10.1038/sj.onc.1202077
33. Kiessling, F., S. Greschus, M.P. Lichy, M. Bock, C. Fink, S. Vosseler, J. Moll, M.M. Mueller, N.E. Fusenig, H. Traupe, and W. Semmler. 2004. Volumetric computed tomography (VCT): a new technology for noninvasive, high-resolution monitoring of tumor angiogenesis. Nat. Med. 10:1133-1138. doi:10.1038/nm1101
34. Kunkel, P., S. Müller, P. Schirmacher, D. Stavrou, R. Fillbrandt, M. Westphal, and K. Lamszus. 2001. Expression and localization of scatter factor/hepatocyte growth factor in human astrocytomas. Neuro-oncol. 3:82-88. doi:10.1215/15228517-3-2-82
35. Küsters, B., W.P. Leenders, P. Wesseling, D. Smits, K. Verrijp, D.J. Ruiter, J.P. Peters, A.J. van Der Kogel, and R.M. de Waal. 2002. Vascular endothelial growth factor-A(165) induces progression of melanoma brain metastases without induction of sprouting angiogenesis. Cancer Res. 62:341-345.
36. Leenders, W., N. Lubsen, M. van Altena, M. Clauss, M. Deckers, C. Löwik, G. Breier, D. Ruiter, and R. de Waal. 2002. Design of a variant of vascular endothelial growth factor-A (VEGF-A) antagonizing KDR/Flk-1 and Flt-1. Lab. Invest. 82:473-481.
37. Leenders, W.P., B. Küsters, and R.M. de Waal. 2002. Vessel co-option: how tumors obtain blood supply in the absence of sprouting angiogenesis. Endothelium. 9:83-87. doi:10.1080/10623320212006
38. Maisonpierre, P.C., C. Suri, P.F. Jones, S. Bartunkova, S.J. Wiegand, C. Radziejewski, D. Compton, J. McClain, T.H. Aldrich, N. Papadopoulos, et al. 1997. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science. 277:55-60. doi:10.1126/science.277.5322.55
39. Morikawa, S., P. Baluk, T. Kaidoh, A. Haskell, R.K. Jain, and D.M. McDonald. 2002. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 160:985-1000.
40. Nasarre, P., M. Thomas, K. Kruse, I. Helfrich, V. Wolter, C. Deppermann, D. Schadendorf, G. Thurston, U. Fiedler, and H.G. Augustin. 2009. Host-derived angiopoietin-2 affects early stages of tumor development and vessel maturation but is dispensable for later stages of tumor growth. Cancer Res. 69:1324-1333. doi:10.1158/0008-5472.CAN-08-3030
41. Nehls, V., K. Denzer, and D. Drenckhahn. 1992. Pericyte involvement in capillary sprouting during angiogenesis in situ. Cell Tissue Res. 270:469-474. doi:10.1007/BF00645048
42. Neufeld, G., T. Cohen, S. Gengrinovitch, and Z. Poltorak. 1999. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13:9-22.
43. Paku, S. 1998. Current concepts of tumor-induced angiogenesis. Pathol. Oncol. Res. 4:62-75. doi:10.1007/BF02904699
44. Perez, D.G., V.J. Suman, T.R. Fitch, T. Amatruda III, R.F. Morton, S.Z. Jilani, C.L. Constantinou, J.R. Egner, L.A. Kottschade, and S.N. Markovic. 2009. Phase 2 trial of carboplatin, weekly paclitaxel, and biweekly bevacizumab in patients with unresectable stage IV melanoma: a North Central Cancer Treatment Group study, N047A. Cancer. 115:119-127. doi:10.1002/cncr.23987
45. Pezzella, F., U. Pastorino, E. Tagliabue, S. Andreola, G. Sozzi, G. Gasparini, S. Menard, K.C. Gatter, A.L. Harris, S. Fox, et al. 1997. Non-small-cell lung carcinoma tumor growth without morphological evidence of neo-angiogenesis. Am. J. Pathol. 151:1417-1423.
46. Pichiule, P., J.C. Chavez, and J.C. LaManna. 2004. Hypoxic regulation of angiopoietin-2 expression in endothelial cells. J. Biol. Chem. 279:12171-12180. doi:10.1074/jbc.M305146200
47. Scharpfenecker, M., U. Fiedler, Y. Reiss, and H.G. Augustin. 2005. The Tie-2 ligand angiopoietin-2 destabilizes quiescent endothelium through an internal autocrine loop mechanism. J. Cell Sci. 118:771-780. doi:10.1242/jcs.01653
48. Shieh, Y.S., Y.J. Hung, C.B. Hsieh, J.S. Chen, K.C. Chou, and S.Y. Liu. 2009. Tumor-associated macrophage correlated with angiogenesis and progression of mucoepidermoid carcinoma of salivary glands. Ann. Surg. Oncol. 16:751-760. doi:10.1245/s10434-008-0259-6
49. Siemeister, G., M. Schirner, P. Reusch, B. Barleon, D. Marmé, and G. Martiny-Baron. 1998. An antagonistic vascular endothelial growth factor (VEGF) variant inhibits VEGF-stimulated receptor autophosphorylation and proliferation of human endothelial cells. Proc. Natl. Acad. Sci. USA. 95:4625-4629. doi:10.1073/pnas.95.8.4625
50. Suri, C., P.F. Jones, S. Patan, S. Bartunkova, P.C. Maisonpierre, S. Davis, T.N. Sato, and G.D. Yancopoulos. 1996. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell. 87:1171-1180. doi:10.1016/S0092-8674(00)81813-9
51. Sweeney, P., T. Karashima, S.J. Kim, D. Kedar, B. Mian, S. Huang, C. Baker, Z. Fan, D.J. Hicklin, C.A. Pettaway, and C.P. Dinney. 2002. Anti-vascular endothelial growth factor receptor 2 antibody reduces tumorigenicity and metastasis in orthotopic prostate cancer xenografts via induction of endothelial cell apoptosis and reduction of endothelial cell matrix metalloproteinase type 9 production. Clin. Cancer Res. 8:2714-2724.
52. Thomas, A.L., T. Trarbach, C. Bartel, D. Laurent, A. Henry, M. Poethig, J. Wang, E. Masson, W. Steward, U. Vanhoefer, and B. Wiedenmann. 2007. A phase IB, open-label dose-escalating study of the oral angiogenesis inhibitor PTK787/ZK 222584 (PTK/ZK), in combination with FOLFOX4 chemotherapy in patients with advanced colorectal cancer. Ann. Oncol. 18:782-788. doi:10.1093/annonc/mdl469
53. von Tell, D., A. Armulik, and C. Betsholtz. 2006. Pericytes and vascular stability. Exp. Cell Res. 312:623-629. doi:10.1016/j.yexcr.2005.10.019
54. Weis, J., and J.M. Schröder. 1989. Differential effects of nerve, muscle, and fat tissue on regenerating nerve fibers in vivo. Muscle Nerve. 12:723-734. doi:10.1002/mus.880120905
55. Weis, J., W. Dimpfel, and J.M. Schröder. 1995. Nerve conduction changes and fine structural alterations of extra- and intrafusal muscle and nerve fibers in streptozotocin diabetic rats. Muscle Nerve. 18:175-184. doi:10.1002/mus.880180205
56. Wong, A.L., Z.A. Haroon, S. Werner, M.W. Dewhirst, C.S. Greenberg, and K.G. Peters. 1997. Tie2 expression and phosphorylation in angiogenic and quiescent adult tissues. Circ. Res. 81:567-574.
57. Wood, J.M., G. Bold, E. Buchdunger, R. Cozens, S. Ferrari, J. Frei, F. Hofmann, J. Mestan, H. Mett, T. O'Reilly, et al. 2000. PTK787/ZK 222584, a novel and potent inhibitor of vascular endothelial growth factor receptor tyrosine kinases, impairs vascular endothelial growth factor-induced responses and tumor growth after oral administration. Cancer Res. 60:2178-2189.