Vascular endothelial growth factor blockade rapidly elicits alternative proangiogenic pathways in neuroblastoma

International Journal of Oncology

Volumn 34, Issue 2, 2009, Pages 401-407

  Zaghloul, Nibal ^a,b   Hernandez, Sonia L ^a   Bae, Jae O ^a   Huang, Jianzhong ^a   Fisher, Jason C ^a   Lee, Alice ^a   Kadenhe Chiweshe, Angela ^a   Kandel, Jessica J ^a   Yamashiro, Darrell J ^a,c  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b Akron Children's Center for Blood and Cancer   (United States)

^c Department of Medicine   (United States)

Author keywords

Angiogenesis; Neuroblastoma; Notch; Placental growth factor; Vascular endothelial growth factor

Indexed keywords

JAGGED1; MONOCLONAL ANTIBODY DC101; NOTCH RECEPTOR; ONCOPROTEIN; PLACENTAL GROWTH FACTOR; PROTEIN MYCN; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; FEMALE; GENE AMPLIFICATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; MOUSE; NEUROBLASTOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RECEPTOR BLOCKING; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; UPREGULATION;

ANIMALS; CELL DIVISION; CELL HYPOXIA; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; NEUROBLASTOMA; TRANSPLANTATION, HETEROLOGOUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 64549116401     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo_00000163     Document Type: Article

References (43)

1. Weidner N, Semple JP, Welch WR and Folkman J: Tumor angiogenesis and metastasis - correlation in invasive breast carcinoma. N Engl J Med 324: 1-8, 1991.
2. Weidner N, Carroll PR, Flax J, Blumenfeld W and Folkman J: Tumor angiogenesis correlates with metastasis in invasive prostate carcinoma. Am J Pathol 143: 401-409, 1993.
3. Beecken WD, Fernandez A, Joussen AM, Achilles EG, Flynn E, Lo KM, Gillies SD, Javaherian K, Folkman J and Shing Y: Effect of antiangiogenic therapy on slowly growing, poorly vascularized tumors in mice. J Natl Cancer Inst 93: 382-387, 2001.
4. Maeda K, Chung YS, Takatsuka S, Ogawa Y, Sawada T, Yamashita Y, Onoda N, Kato Y, Nitta A, Arimoto Y, et al: Tumor angiogenesis as a predictor of recurrence in gastric carcinoma. J Clin Oncol 13: 477-481, 1995.
5. Horak ER, Leek R, Klenk N, LeJeune S, Smith K, Stuart N, Greenall M, Stepniewska K and Harris AL: Angiogenesis, assessed by platelet/ endothelial cell adhesion molecule antibodies, as indicator of node metastases and survival in breast cancer. Lancet 340: 1120-1124, 1992.
6. Eggert A, Ikegaki N, Kwiatkowski J, Zhao H, Brodeur GM and Himelstein BP: High-level expression of angiogenic factors is associated with advanced tumor stage in human neuroblastomas. Clin Cancer Res 6: 1900-1908, 2000.
7. de Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N and Williams LT: The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255: 989-991, 1992.
8. Grosskreutz CL, Anand-Apte B, Duplaa C, Quinn TP, Terman BI, Zetter B and D'Amore PA: Vascular endothelial growth factor-induced migration of vascular smooth muscle cells in vitro. Microvasc Res 58: 128-136, 1999.
9. Soker S, Takashima S, Miao HQ, Neufeld G and Klagsbrun M: Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92: 735-745, 1998.
10. Yang JC, Haworth L, Steinberg SM, Rosenberg SA and Novotny W: A randomized double-blind placebo-controlled trial of Bevacizumab (anti-VEGF antibody) demonstrating a prolongation in time to progression in patients with metastatic renal cancer. Proc ASCO 21: 5a, 2002.
11. Kabbinavar F, Hurwitz HI, Fehrenbacher L, Meropol NJ, Novotny WF, Lieberman G, Griffing S and Bergsland E: Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. J Clin Oncol 21: 60-65, 2003.
12. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, Berlin J, Baron A, Griffing S, Holmgren E, Ferrara N, Fyfe G, Rogers B, Ross R and Kabbinavar F: Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 350: 2335-2342, 2004.
13. Casanovas O, Hicklin DJ, Bergers G and Hanahan D: Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 8: 299-309, 2005.
14. Winkler F, Kozin SV, Tong RT, Chae SS, Booth MF, Garkavtsev I, Xu L, Hicklin DJ, Fukumura D, di Tomaso E, Munn LL and Jain RK: Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 6: 553-563, 2004.
15. Huang J, Frischer JS, New T, Kim ES, Serur A, Lee A, Kadenhe-Chiwishe A, Pollyea DA, Yokoi A, Holash J, Yancopoulos GD, Kandel JJ and Yamashiro DJ: TNP-470 promotes initial vascular sprouting in xenograft tumors. Mol Cancer Ther 3: 335-343, 2004.
16. Willett CG, Boucher Y, Duda DG, di Tomaso E, Munn LL, Tong RT, Kozin SV, Petit L, Jain RK, Chung DC, Sahani DV, Kalva SP, Cohen KS, Scadden DT, Fischman AJ, Clark JW, Ryan DP, Zhu AX, Blaszkowsky LS, Shellito PC, Mino-Kenudson M and Lauwers GY: Surrogate markers for antiangiogenic therapy and dose-limiting toxicities for bevacizumab with radiation and chemotherapy: continued experience of a phase I trial in rectal cancer patients. J Clin Oncol 23: 8136-8139, 2005.
17. Fong GH, Rossant J, Gertsenstein M and Breitman ML: Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376: 66-70, 1995.
18. Hiratsuka S, Maru Y, Okada A, Seiki M, Noda T and Shibuya M: Involvement of Flt-1 tyrosine kinase (vascular endothelial growth factor receptor-1) in pathological angiogenesis. Cancer Res 61: 1207-1213, 2001.
19. Witmer AN, Dai J, Weich HA, Vrensen GF and Schlingemann RO: Expression of vascular endothelial growth factor receptors 1, 2, and 3 in quiescent endothelia. J Histochem Cytochem 50: 767-777, 2002.
20. Morowitz MJ, Barr R, Wang Q, King R, Rhodin N, Pawel B, Zhao H, Erickson SA, Sheppard GS, Wang J, Maris JM and Shusterman S: Methionine aminopeptidase 2 inhibition is an effective treatment strategy for neuroblastoma in preclinical models. Clin Cancer Res 11: 2680-2685, 2005.
21. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, Scholz D, Acker T, DiPalma T, Dewerchin M, Noel A, Stalmans I, Barra A, Blacher S, Vandendriessche T, Ponten A, Eriksson U, Plate KH, Foidart JM, Schaper W, Charnock-Jones DS, Hicklin DJ, Herbert JM, Collen D and Persico MG: Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 7: 575-583, 2001.
22. Matsumoto K, Suzuki K, Koike H, Okamura K, Tsuchiya K, Uchida T, Takezawa Y, Kobayashi M and Yamanaka H: Prognostic significance of plasma placental growth factor levels in renal cell cancer: an association with clinical characteristics and vascular endothelial growth factor levels. Anticancer Res 23: 4953-4958, 2003.
23. Parr C, Watkins G, Boulton M, Cai J and Jiang WG: Placenta growth factor is over-expressed and has prognostic value in human breast cancer. Eur J Cancer 41: 2819-2827, 2005.
24. Zhang L, Chen J, Ke Y, Mansel RE and Jiang WG: Expression of Placenta growth factor (PlGF) in non-small cell lung cancer (NSCLC) and the clinical and prognostic significance. World J Surg Oncol 3: 68, 2005.
25. Wei SC, Tsao PN, Yu SC, Shun CT, Tsai-Wu JJ, Wu CH, Su YN, Hsieh FJ and Wong JM: Placenta growth factor expression is correlated with survival of patients with colorectal cancer. Gut 54: 666-672, 2005.
26. Gerber HP, Kowalski J, Sherman D, Eberhard DA and Ferrara N: Complete inhibition of rhabdomyosarcoma xenograft growth and neovascularization requires blockade of both tumor and host vascular endothelial growth factor. Cancer Res 60: 6253-6258, 2000.
27. Paris D, Quadros A, Patel N, DelleDonne A, Humphrey J and Mullan M: Inhibition of angiogenesis and tumor growth by beta and gamma-secretase inhibitors. Eur J Pharmacol 514: 1-15, 2005.
28. Zeng Q, Li S, Chepeha DB, Giordano TJ, Li J, Zhang H, Polverini PJ, Nor J, Kitajewski J and Wang CY: Crosstalk between tumor and endothelial cells promotes tumor angiogenesis by MAPK activation of Notch signaling. Cancer Cell 8: 13-23, 2005.
29. Xue Y, Gao X, Lindsell CE, Norton CR, Chang B, Hicks C, Gendron-Maguire M, Rand EB, Weinmaster G and Gridley T: Embryonic lethality and vascular defects in mice lacking the Notch ligand Jagged1. Hum Mol Genet 8: 723-730, 1999.
30. Lindner V, Booth C, Prudovsky I, Small D, Maciag T and Liaw L: Members of the Jagged/Notch gene families are expressed in injured arteries and regulate cell phenotype via alterations in cell matrix and cell-cell interaction. Am J Pathol 159: 875-883, 2001.
31. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES and Mesirov JP: Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102: 15545-15550, 2005.
32. Winter SC, Buffa FM, Silva P, Miller C, Valentine HR, Turley H, Shah KA, Cox GJ, Corbridge RJ, Homer JJ, Musgrove B, Slevin N, Sloan P, Price P, West CM and Harris AL: Relation of a hypoxia metagene derived from head and neck cancer to prognosis of multiple cancers. Cancer Res 67: 3441-3449, 2007.
33. Witte L, Hicklin DJ, Zhu Z, Pytowski B, Kotanides H, Rockwell P and Bohlen P: Monoclonal antibodies targeting the VEGF receptor-2 (Flk1/KDR) as an anti-angiogenic therapeutic strategy. Cancer Metastasis Rev 17: 155-161, 1998.
34. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, Gale NW, Lin HC, Yancopoulos GD and Thurston G: Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444: 1032-1037, 2006.
35. Ridgway J, Zhang G, Wu Y, Stawicki S, Liang WC, Chanthery Y, Kowalski J, Watts RJ, Callahan C, Kasman I, Singh M, Chien M, Tan C, Hongo JA, de Sauvage F, Plowman G and Yan M: Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444: 1083-1087, 2006.
36. Bender JL, Adamson PC, Reid JM, Xu L, Baruchel S, Shaked Y, Kerbel RS, Cooney-Qualter EM, Stempak D, Chen HX, Nelson MD, Krailo MD, Ingle AM, Blaney SM, Kandel JJ and Yamashiro DJ: Phase I trial and pharmacokinetic study of bevacizumab in pediatric patients with refractory solid tumors: a Children's Oncology Group Study. J Clin Oncol 26: 399-405, 2008.
37. Katzenstein HM, Salwen HR, Nguyen NN, Meitar D and Cohn SL: Antiangiogenic therapy inhibits human neuroblastoma growth. Med Pediatr Oncol 36: 190-193, 2001.
38. Kim ES, Serur A, Huang J, Manley CA, McCrudden KW, Frischer JS, Soffer SZ, Ring L, New T, Zabski S, Rudge JS, Holash J, Yancopoulos GD, Kandel JJ and Yamashiro DJ: Potent VEGF blockade causes regression of coopted vessels in a model of neuroblastoma. Proc Natl Acad Sci USA 99: 11399-11404, 2002.
39. Kaicker S, McCrudden KW, Beck L, New T, Huang J, Frischer JS, Serur A, Kadenhe-Chiweshe A, Yokoi A, Kandel JJ and Yamashiro DJ: Thalidomide is anti-angiogenic in a xenograft model of neuroblastoma. Int J Oncol 23: 1651-1655, 2003.
40. Streck CJ, Zhang Y, Miyamoto R, Zhou J, Ng CY, Nathwani AC and Davidoff AM: Restriction of neuroblastoma angiogenesis and growth by interferon-alpha/beta. Surgery 136: 183-189, 2004.
41. Segerstrom L, Fuchs D, Backman U, Holmquist K, Christofferson R and Azarbayjani F: The anti-VEGF antibody bevacizumab potently reduces the growth rate of high-risk neuroblastoma xenografts. Pediatr Res 60: 576-581, 2006.
42. Hamner JB, Dickson PV, Sims TL, Zhou J, Spence Y, Ng CY and Davidoff AM: Bortezomib inhibits angiogenesis and reduces tumor burden in a murine model of neuroblastoma. Surgery 142: 185-191, 2007.
43. Funahashi Y, Hernandez SL, Das I, Ahn A, Huang J, Vorontchikhina M, Sharma A, Kanamaru E, Borisenko V, Desilva DM, Suzuki A, Wang X, Shawber CJ, Kandel JJ, Yamashiro DJ and Kitajewski J: A notch1 ectodomain construct inhibits endothelial notch signaling, tumor growth, and angiogenesis. Cancer Res 68: 4727-4735, 2008.