Malignant progression and blockade of angiogenesis in a murine transgenic model of neuroblastoma

被引:57
作者
Chesler, Louis
Goldenberg, David D.
Seales, Isha T.
Satchi-Fainaro, Ronit
Grimmer, Matt
Collins, Rodney
Struett, Chris
Nguyen, Kim N.
Kim, Grace
Tihan, Tarik
Bao, Yun
Brekken, Rolf A.
Bergers, Gabriele
Folkman, Judah
Weiss, William A.
机构
[1] Univ Calif San Francisco, Dept Neurol, Sch Med, San Francisco, CA 94143 USA
[2] Univ Calif San Francisco, Dept Pediat, Sch Med, San Francisco, CA 94143 USA
[3] Univ Calif San Francisco, Dept Neurol Surg, Sch Med, San Francisco, CA 94143 USA
[4] Univ Calif San Francisco, Brain Tumor Res Ctr, Sch Med, San Francisco, CA 94143 USA
[5] Univ Calif San Francisco, Ctr Comprehens Canc, Sch Med, San Francisco, CA 94143 USA
[6] Univ Calif San Francisco, Dept Pathol, Sch Med, San Francisco, CA 94143 USA
[7] Tel Aviv Univ, Sackler Sch Med, Dept Physiol & Pharmacol, Tel Aviv, Israel
[8] Univ Texas, SW Med Ctr, Dept Surg, Dallas, TX 75235 USA
[9] Univ Texas, SW Med Ctr, Hamon Ctr Therapeut Oncol Res, Dept Surg, Dallas, TX 75235 USA
[10] Univ Texas, SW Med Ctr, Hamon Ctr Therapeut Oncol Res, Dept Pharmacol, Dallas, TX 75235 USA
[11] Harvard Univ, Dept Surg, Boston, MA 02115 USA
[12] Harvard Univ, Dept Cellular Biol, Boston, MA 02115 USA
[13] Childrens Hosp, Boston, MA 02115 USA
关键词
D O I
10.1158/0008-5472.CAN-07-1316
中图分类号
R73 [肿瘤学];
学科分类号
100214 ;
摘要
Targeted expression of MYCN to the neural crest [under control of the rat tyrosine hydroxylase (TH) promoter] causes neuroblastoma in transgenic mice (TH-MYCN) and is a well-established model for this disease. Because high levels of MYCN are associated with enhanced tumor angiogenesis and poor clinical outcome in neuroblastoma, we serially characterized malignant progression, angiogenesis, and sensitivity to angiogenic blockade in tumors from these animals. Tumor cells were proliferative, secreted high levels of the angiogenic ligand vascular endothelial growth factor (VEGF), and recruited a complex vasculature expressing the angiogenic markers VEGF-R2, alpha-SMA, and matrix metalloproteinases MMP-2 and MMP-9, all of which are also expressed in human disease. Treatment of established murine tumors with the angiogenesis inhibitor TNP-470 caused near-complete ablation, with reduced proliferation, enhanced apoptosis, and vasculature disruption. Because TNP-470 has been associated with neurotoxicity, we tested the recently described water-soluble HPMA copolymer-TNP-470 conjugate (caplostatin), which showed comparable efficacy and was well tolerated without weight loss or neurotoxicity as measured by rotarod testing. This study highlights the importance of angiogenesis inhibition in a spontaneous murine tumor with native tumor-microenvironment interactions, validates the use of mice transgenic for TH-MYCN as a model for therapy in this common pediatric tumor, and supports further clinical development of caplostatin as an antiangiogenic therapy in childhood neuroblastoma.
引用
收藏
页码:9435 / 9442
页数:8
相关论文
共 53 条
[1]   Role of ploidy, chromosome 1p, and Schwann cells in the maturation of neuroblastoma [J].
Ambros, IM ;
Zellner, A ;
Roald, B ;
Amann, G ;
Ladenstein, R ;
Printz, D ;
Gadner, H ;
Ambros, PF .
NEW ENGLAND JOURNAL OF MEDICINE, 1996, 334 (23) :1505-1511
[2]  
[Anonymous], 2002, PRINCIPLES PRACTICE
[3]   Immunohistochemical expression of MMP-2, MMP-9, and TIMP-2 in neuroblastoma: Association with tumor progression and clinical outcome [J].
Ara, T ;
Fukuzawa, M ;
Kusafuka, T ;
Komoto, Y ;
Oue, T ;
Inoue, M ;
Okada, A .
JOURNAL OF PEDIATRIC SURGERY, 1998, 33 (08) :1272-1278
[4]   VEGF receptors are differentially expressed by neuroblastoma cells in culture [J].
Beierle, EA ;
Dai, W ;
Langham, MR ;
Copeland, EM ;
Chen, MK .
JOURNAL OF PEDIATRIC SURGERY, 2003, 38 (03) :514-521
[5]   Effects of angiogenesis inhibitors on multistage carcinogenesis in mice [J].
Bergers, G ;
Javaherian, K ;
Lo, KM ;
Folkman, J ;
Hanahan, D .
SCIENCE, 1999, 284 (5415) :808-812
[6]   Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors [J].
Bergers, G ;
Song, S ;
Meyer-Morse, N ;
Bergsland, E ;
Hanahan, D .
JOURNAL OF CLINICAL INVESTIGATION, 2003, 111 (09) :1287-1295
[7]   REVISIONS OF THE INTERNATIONAL CRITERIA FOR NEUROBLASTOMA DIAGNOSIS, STAGING, AND RESPONSE TO TREATMENT [J].
BRODEUR, GM ;
PRITCHARD, J ;
BERTHOLD, F ;
CARLSEN, NLT ;
CASTEL, V ;
CASTLEBERRY, RP ;
DEBERNARDI, B ;
EVANS, AE ;
FAVROT, M ;
HEDBORG, F ;
KANEKO, M ;
KEMSHEAD, J ;
LAMPERT, F ;
LEE, REJ ;
LOOK, AT ;
PEARSON, ADJ ;
PHILIP, T ;
ROALD, B ;
SAWADA, T ;
SEEGER, RC ;
TSUCHIDA, Y ;
VOUTE, PA .
JOURNAL OF CLINICAL ONCOLOGY, 1993, 11 (08) :1466-1477
[8]   Stromal matrix metalloproteinase-9 regulates the vascular architecture in neuroblastoma by promoting pericyte recruitment [J].
Chantrain, CF ;
Shimada, H ;
Jodele, S ;
Groshen, S ;
Ye, W ;
Shalinsky, DR ;
Werb, Z ;
Coussens, LM ;
DeClerck, YA .
CANCER RESEARCH, 2004, 64 (05) :1675-1686
[9]   Ultrastructural localization of the vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) receptor-2 (FLK-1, KDR) in normal mouse kidney and in the hyperpermeable vessels induced by VPF/VEGF-expressing tumors and adenoviral vectors [J].
Feng, D ;
Nagy, JA ;
Brekken, RA ;
Pettersson, A ;
Manseau, EJ ;
Pyne, K ;
Mulligan, R ;
Thorpe, PE ;
Dvorak, HF ;
Dvorak, AM .
JOURNAL OF HISTOCHEMISTRY & CYTOCHEMISTRY, 2000, 48 (04) :545-555
[10]   INFLUENCE OF GEOMETRY ON CONTROL OF CELL-GROWTH [J].
FOLKMAN, J ;
GREENSPAN, HP .
BIOCHIMICA ET BIOPHYSICA ACTA, 1975, 417 (3-4) :211-236