Effect of MDM2 and vascular endothelial growth factor inhibition on tumor angiogenesis and metastasis in neuroblastoma

Angiogenesis

Volumn 14, Issue 3, 2011, Pages 255-266

  Patterson, Danielle M ^a   Gao, Dongbing ^b   Trahan, Denae N ^b   Johnson, Brett A ^a   Ludwig, Andrew ^b   Barbieri, Eveline ^b   Chen, Zaowen ^b   Diaz Miron, Jose ^a   Vassilev, Lyubomir ^c   Shohet, Jason M ^b   Kim, Eugene S ^a,b  

^a TEXAS CHILDREN S HOSPITAL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c HOFFMANN LA ROCHE INC   (United States)

Author keywords

Angiogenesis; Bevacizumab; Metastasis; Neuroblastoma; Nutlin

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BEVACIZUMAB; CD31 ANTIGEN; COLLAGEN TYPE 4; NUTLIN 3; PROTEIN MDM2; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BASEMENT MEMBRANE; CANCER COMBINATION CHEMOTHERAPY; CARCINOGENESIS; CELL COUNT; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG TARGETING; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; METASTASIS; MONOTHERAPY; MOUSE; NEUROBLASTOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; CELL LINE, TUMOR; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMIDAZOLES; MICE; MICE, NUDE; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; NEUROBLASTOMA; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MUS MUSCULUS;

EID: 80052760317     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-011-9210-8     Document Type: Article

References (52)

1. F Berthold J Boos S Burdach R Erttmann G Henze J Hermann T Klingebiel B Kremens FH Schilling M Schrappe T Simon B Hero 2005 Myeloablative megatherapy with autologous stem-cell rescue versus oral maintenance chemotherapy as consolidation treatment in patients with high-risk neuroblastoma: a randomised controlled trial Lancet Oncol 6 9 649 658 10.1016/S1470-2045(05)70291-6 16129365 10.1016/S1470-2045(05)70291-6 1:CAS:528:DC%2BD2MXpslynsrw%3D (Pubitemid 41222755)
2. KK Matthay JG Villablanca RC Seeger DO Stram RE Harris NK Ramsay P Swift H Shimada CT Black GM Brodeur RB Gerbing CP Reynolds 1999 Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children's Cancer Group N Engl J Med 341 16 1165 1173 10519894 10.1056/NEJM199910143411601 1:STN:280: DyaK1MvjsFGnsg%3D%3D (Pubitemid 29480654)
3. JG Gurney JM Tersak KK Ness W Landier KK Matthay ML Schmidt 2007 Hearing loss, quality of life, and academic problems in long-term neuroblastoma survivors: a report from the children's oncology group Pediatrics 120 5 e1229 e1236 10.1542/peds.2007-0178 17974716 10.1542/peds.2007-0178 (Pubitemid 350085519)
4. BH Kushner K Kramer S Modak LX Qin K Yataghena SC Jhanwar NK Cheung 2009 Reduced risk of secondary leukemia with fewer cycles of dose-intensive induction chemotherapy in patients with neuroblastoma Pediatr Blood Cancer 53 1 17 22 10.1002/pbc.21931 19148951 10.1002/pbc.21931
5. C Laverdiere NK Cheung BH Kushner K Kramer S Modak MP LaQuaglia S Wolden KK Ness JG Gurney CA Sklar 2005 Long-term complications in survivors of advanced stage neuroblastoma Pediatr Blood Cancer 45 3 324 332 10.1002/pbc.20331 15714447 10.1002/pbc.20331 (Pubitemid 41077167)
6. KK Matthay CP Reynolds RC Seeger H Shimada ES Adkins D Haas-Kogan RB Gerbing WB London JG Villablanca 2009 Long-term results for children with high-risk neuroblastoma treated on a randomized trial of myeloablative therapy followed by 13-cis-retinoic acid: a children's oncology group study J Clin Oncol 27 7 1007 1013 10.1200/JCO.2007.13.8925 19171716 10.1200/JCO.2007.13.8925 1:CAS:528:DC%2BD1MXktVCjurY%3D
7. R Haupt A Garaventa C Gambini S Parodi G Cangemi F Casale E Viscardi M Bianchi A Prete A Jenkner R Luksch A Di Cataldo C Favre P D'Angelo GA Zanazzo G Arcamone GC Izzi AR Gigliotti G Pastore B De Bernardi 1979 Improved survival of children with neuroblastoma between and 2005: a report of the Italian neuroblastoma registry J Clin Oncol 28 14 2331 2338 10.1200/JCO.2009.24.8351 10.1200/JCO.2009.24.8351
8. L Chen AJ Malcolm KM Wood M Cole S Variend C Cullinane AD Pearson J Lunec DA Tweddle 2007 p53 is nuclear and functional in both undifferentiated and differentiated neuroblastoma Cell Cycle 6 21 2685 2696 17912039 10.4161/cc.6.21.4853 1:CAS:528:DC%2BD1cXhsFyrsw%3D%3D 4853 [pii] (Pubitemid 350224053)
9. K Vogan M Bernstein JM Leclerc L Brisson J Brossard GM Brodeur J Pelletier P Gros 1993 Absence of p53 gene mutations in primary neuroblastomas Cancer Res 53 21 5269 5273 8221661 1:CAS:528:DyaK2cXivVChuw%3D%3D (Pubitemid 23333398)
10. DA Freedman L Wu AJ Levine 1999 Functions of the MDM2 oncoprotein Cell Mol Life Sci 55 1 96 107 10065155 10.1007/s000180050273 1:CAS:528: DyaK1MXhtV2lsLY%3D (Pubitemid 29077858)
11. Y Haupt R Maya A Kazaz M Oren 1997 Mdm2 promotes the rapid degradation of p53 Nature 387 6630 296 299 10.1038/387296a0 9153395 10.1038/387296a0 1:CAS:528:DyaK2sXjtlSgtL8%3D (Pubitemid 27220766)
12. MH Kubbutat SN Jones KH Vousden 1997 Regulation of p53 stability by Mdm2 Nature 387 6630 299 303 10.1038/387299a0 9153396 10.1038/387299a0 1:CAS:528:DyaK2sXjtlSgtLc%3D (Pubitemid 27220767)
13. J Momand D Jung S Wilczynski J Niland 1998 The MDM2 gene amplification database Nucleic Acids Res 26 15 3453 3459 9671804 10.1093/nar/26.15.3453 1:CAS:528:DyaK1cXltlKqsr4%3D gkb548 [pii] (Pubitemid 28347214)
14. MK Schmidt J Tommiska A Broeks FE van Leeuwen LJ Van't Veer PD Pharoah DF Easton M Shah M Humphreys T Dork SA Reincke R Fagerholm C Blomqvist H Nevanlinna 2009 Combined effects of single nucleotide polymorphisms TP53 R72P and MDM2 SNP309, and p53 expression on survival of breast cancer patients Breast Cancer Res 11 6 R89 10.1186/bcr2460 20021639 10.1186/bcr2460
15. C Perfumo S Parodi K Mazzocco R Defferrari A Inga GB Scarra P Ghiorzo R Haupt GP Tonini G Fronza 2009 MDM2 SNP309 genotype influences survival of metastatic but not of localized neuroblastoma Pediatr Blood Cancer 53 4 576 583 10.1002/pbc.22132 19526525 10.1002/pbc.22132
16. K Willander J Ungerback K Karlsson M Fredrikson P Soderkvist M Linderholm 2010 MDM2 SNP309 promoter polymorphism, an independent prognostic factor in chronic lymphocytic leukemia Eur J Haematol 85 3 251 256 10.1111/j.1600-0609. 2010.01470.x 20491880 10.1111/j.1600-0609.2010.01470.x 1:CAS:528: DC%2BC3cXhtFKjsL3I
17. WP Chien RH Wong YW Cheng CY Chen H Lee 2010 Associations of MDM2 SNP309, transcriptional activity, mRNA expression, and survival in stage I non-small-cell lung cancer patients with wild-type p53 tumors Ann Surg Oncol 17 4 1194 1202 10.1245/s10434-009-0853-2 19941079 10.1245/s10434-009-0853-2
18. Z Chen Y Lin E Barbieri S Burlingame J Hicks A Ludwig JM Shohet 2009 Mdm2 deficiency suppresses MYCN-Driven neuroblastoma tumorigenesis in vivo Neoplasia 11 8 753 762 19649205 1:CAS:528:DC%2BD1MXoslKiur8%3D
19. T Van Maerken L Ferdinande J Taildeman I Lambertz N Yigit L Vercruysse A Rihani M Michaelis J Cinatl Jr CA Cuvelier JC Marine A De Paepe M Bracke F Speleman J Vandesompele 2009 Antitumor activity of the selective MDM2 antagonist nutlin-3 against chemoresistant neuroblastoma with wild-type p53 J Natl Cancer Inst 101 22 1562 1574 10.1093/jnci/djp355 19903807 10.1093/jnci/djp355
20. E Kim J Shohet 2009 Targeted molecular therapy for neuroblastoma: the ARF/MDM2/p53 axis J Natl Cancer Inst 101 22 1527 1529 10.1093/jnci/djp376 19903809 10.1093/jnci/djp376 1:CAS:528:DC%2BD1MXhsVKls7vO
21. LT Vassilev BT Vu B Graves D Carvajal F Podlaski Z Filipovic N Kong U Kammlott C Lukacs C Klein N Fotouhi EA Liu 2004 In vivo activation of the p53 pathway by small-molecule antagonists of MDM2 Science 303 5659 844 848 10.1126/science.1092472 14704432 10.1126/science.1092472 1:CAS:528: DC%2BD2cXovVKmtA%3D%3D (Pubitemid 38174664)
22. F Chen W Wang WS El-Deiry 2010 Current strategies to target p53 in cancer Biochem Pharmacol 80 5 724 730 10.1016/j.bcp.2010.04.031 20450892 10.1016/j.bcp.2010.04.031 1:CAS:528:DC%2BC3cXosV2isLg%3D
23. CJ Brown S Lain CS Verma AR Fersht DP Lane 2009 Awakening guardian angels: drugging the p53 pathway Nat Rev Cancer 9 12 862 873 10.1038/nrc2763 19935675 10.1038/nrc2763 1:CAS:528:DC%2BD1MXhsVGlur%2FM
24. E Barbieri P Mehta Z Chen L Zhang A Slack S Berg JM Shohet 2006 MDM2 inhibition sensitizes neuroblastoma to chemotherapy-induced apoptotic cell death Mol Cancer Ther 5 9 2358 2365 10.1158/1535-7163.MCT-06-0305 16985070 10.1158/1535-7163.MCT-06-0305 1:CAS:528:DC%2BD28Xps1ynsbw%3D (Pubitemid 44530473)
25. D Chen M Li J Luo W Gu 2003 Direct interactions between HIF-1 alpha and Mdm2 modulate p53 function J Biol Chem 278 16 13595 13598 10.1074/jbc.C200694200 12606552 10.1074/jbc.C200694200 1:CAS:528:DC%2BD3sXjtVSisLk%3D (Pubitemid 36799889)
26. AL Nieminen S Qanungo EA Schneider BH Jiang FH Agani 2005 Mdm2 and HIF-1alpha interaction in tumor cells during hypoxia J Cell Physiol 204 2 364 369 10.1002/jcp.20406 15880652 10.1002/jcp.20406 1:CAS:528:DC%2BD2MXlvFCrsrk%3D (Pubitemid 40934627)
27. YM Lee JH Lim YS Chun HE Moon MK Lee LE Huang JW Park 2009 Nutlin-3, an Hdm2 antagonist, inhibits tumor adaptation to hypoxia by stimulating the FIH-mediated inactivation of HIF-1alpha Carcinogenesis 30 10 1768 1775 10.1093/carcin/bgp196 19696166 10.1093/carcin/bgp196 1:CAS:528: DC%2BD1MXht1GmtrvE
28. JD Gordan MC Simon 2007 Hypoxia-inducible factors: central regulators of the tumor phenotype Curr Opin Genet Dev 17 1 71 77 10.1016/j.gde.2006.12.006 17208433 10.1016/j.gde.2006.12.006 1:CAS:528:DC%2BD2sXnslOntw%3D%3D (Pubitemid 46109295)
29. JI Bardos NM Chau M Ashcroft 2004 Growth factor-mediated induction of HDM2 positively regulates hypoxia-inducible factor 1alpha expression Mol Cell Biol 24 7 2905 2914 15024078 10.1128/MCB.24.7.2905-2914.2004 1:CAS:528:DC%2BD2cXis1emtrw%3D (Pubitemid 38381279)
30. GA LaRusch MW Jackson JD Dunbar RS Warren DB Donner LD Mayo 2007 Nutlin3 blocks vascular endothelial growth factor induction by preventing the interaction between hypoxia inducible factor 1alpha and Hdm2 Cancer Res 67 2 450 454 10.1158/0008-5472.CAN-06-2710 17234751 10.1158/0008-5472.CAN-06-2710 1:CAS:528:DC%2BD2sXmtVKmtQ%3D%3D (Pubitemid 46192180)
31. M Narasimhan R Rose R Ramakrishnan JA Zell A Rathinavelu 2008 Identification of HDM2 as a regulator of VEGF expression in cancer cells Life Sci 82 25-26 1231 1241 10.1016/j.lfs.2008.04.004 18504050 10.1016/j.lfs.2008.04. 004 1:CAS:528:DC%2BD1cXmvFShsL4%3D
32. M Narasimhan R Rose M Karthikeyan A Rathinavelu 2007 Detection of HDM2 and VEGF co-expression in cancer cell lines: novel effect of HDM2 antisense treatment on VEGF expression Life Sci 81 17-18 1362 1372 10.1016/j.lfs.2007.08. 029 17931661 10.1016/j.lfs.2007.08.029 1:CAS:528:DC%2BD2sXht1amt7fE (Pubitemid 47599526)
33. DW Leung G Cachianes WJ Kuang DV Goeddel N Ferrara 1989 Vascular endothelial growth factor is a secreted angiogenic mitogen Science 246 4935 1306 1309 2479986 10.1126/science.2479986 1:CAS:528:DyaK3cXls1GltLo%3D (Pubitemid 20066716)
34. KJ Kim B Li J Winer M Armanini N Gillett HS Phillips N Ferrara 1993 Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo Nature 362 6423 841 844 10.1038/362841a0 7683111 10.1038/362841a0 1:CAS:528:DyaK3sXktVKju7s%3D (Pubitemid 23132159)
35. JC Yang L Haworth RM Sherry P Hwu DJ Schwartzentruber SL Topalian SM Steinberg HX Chen SA Rosenberg 2003 A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer N Engl J Med 349 5 427 434 10.1056/NEJMoa021491 12890841 10.1056/NEJMoa021491 1:CAS:528:DC%2BD3sXms1Klu7w%3D (Pubitemid 36910021)
36. H Hurwitz L Fehrenbacher W Novotny T Cartwright J Hainsworth W Heim J Berlin A Baron S Griffing E Holmgren N Ferrara G Fyfe B Rogers R Ross F Kabbinavar 2004 Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer N Engl J Med 350 23 2335 2342 10.1056/NEJMoa032691 15175435 10.1056/NEJMoa032691 1:CAS:528:DC%2BD2cXks1Gjt74%3D (Pubitemid 38702844)
37. KD Miller LI Chap FA Holmes MA Cobleigh PK Marcom L Fehrenbacher M Dickler BA Overmoyer JD Reimann AP Sing V Langmuir HS Rugo 2005 Randomized phase III trial of capecitabine compared with bevacizumab plus capecitabine in patients with previously treated metastatic breast cancer J Clin Oncol 23 4 792 799 10.1200/JCO.2005.05.098 15681523 10.1200/JCO.2005.05.098 1:CAS:528:DC%2BD2MXitVKitrk%3D (Pubitemid 46224178)
38. TN Kreisl L Kim K Moore P Duic C Royce I Stroud N Garren M Mackey JA Butman K Camphausen J Park PS Albert HA Fine 2009 Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma J Clin Oncol 27 5 740 745 10.1200/JCO.2008.16.3055 19114704 10.1200/JCO.2008.16.3055 1:CAS:528:DC%2BD1MXjsVCjs7o%3D
39. JL Glade Bender PC Adamson JM Reid L Xu S Baruchel Y Shaked RS Kerbel EM Cooney-Qualter D Stempak HX Chen MD Nelson MD Krailo AM Ingle SM Blaney JJ Kandel DJ Yamashiro 2008 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 3 399 405 10.1200/JCO.2007.11.9230 18202416 10.1200/JCO.2007.11.9230 (Pubitemid 351171691)
40. P Secchiero F Corallini A Gonelli R Dell'Eva M Vitale S Capitani A Albini G Zauli 2007 Antiangiogenic activity of the MDM2 antagonist nutlin-3 Circ Res 100 1 61 69 10.1161/01.RES.0000253975.76198.ff 17138942 10.1161/01.RES. 0000253975.76198.ff 1:CAS:528:DC%2BD28XhtlGiurjN (Pubitemid 46066774)
41. A Slack Z Chen R Tonelli M Pule L Hunt A Pession JM Shohet 2005 The p53 regulatory gene MDM2 is a direct transcriptional target of MYCN in neuroblastoma Proc Natl Acad Sci USA 102 3 731 736 10.1073/pnas.0405495102 15644444 10.1073/pnas.0405495102 1:CAS:528:DC%2BD2MXis1CqsL8%3D (Pubitemid 40282734)
42. R Wild S Ramakrishnan J Sedgewick AW Griffioen 2000 Quantitative assessment of angiogenesis and tumor vessel architecture by computer-assisted digital image analysis: effects of VEGF-toxin conjugate on tumor microvessel density Microvasc Res 59 3 368 376 10.1006/mvre.1999.2233 10792968 10.1006/mvre.1999.2233 1:STN:280:DC%2BD3c3lsFCnsw%3D%3D (Pubitemid 30322264)
43. ES Kim A Serur J Huang CA Manley KW McCrudden JS Frischer SZ Soffer L Ring T New S Zabski JS Rudge J Holash GD Yancopoulos JJ Kandel DJ Yamashiro 2002 Potent VEGF blockade causes regression of coopted vessels in a model of neuroblastoma Proc Natl Acad Sci USA 99 17 11399 11404 10.1073/pnas.172398399 12177446 10.1073/pnas.172398399 1:CAS:528:DC%2BD38XmslSmu7g%3D (Pubitemid 34920937)
44. M Benesch M Windelberg W Sauseng V Witt G Fleischhack H Lackner H Gadner U Bode C Urban 2008 Compassionate use of bevacizumab (Avastin) in children and young adults with refractory or recurrent solid tumors Ann Oncol 19 4 807 813 10.1093/annonc/mdm510 18056650 10.1093/annonc/mdm510 1:STN:280: DC%2BD1c3gsVOgsw%3D%3D (Pubitemid 351461055)
45. A Sandler R Gray MC Perry J Brahmer JH Schiller A Dowlati R Lilenbaum DH Johnson 2006 Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer N Engl J Med 355 24 2542 2550 10.1056/NEJMoa061884 17167137 10.1056/NEJMoa061884 1:CAS:528:DC%2BD28XhtlWqsbzI (Pubitemid 44917502)
46. J Holash S Davis N Papadopoulos SD Croll L Ho M Russell P Boland R Leidich D Hylton E Burova E Ioffe T Huang C Radziejewski K Bailey JP Fandl T Daly SJ Wiegand GD Yancopoulos JS Rudge 2002 VEGF-Trap: a VEGF blocker with potent antitumor effects Proc Natl Acad Sci USA 99 17 11393 11398 10.1073/pnas.172398299 12177445 10.1073/pnas.172398299 1:CAS:528: DC%2BD38XmslSmu7s%3D (Pubitemid 34920936)
47. DB Mendel AD Laird X Xin SG Louie JG Christensen G Li RE Schreck TJ Abrams TJ Ngai LB Lee LJ Murray J Carver E Chan KG Moss JO Haznedar J Sukbuntherng RA Blake L Sun C Tang T Miller S Shirazian G McMahon JM Cherrington 2003 In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship Clin Cancer Res 9 1 327 337 12538485 1:CAS:528:DC%2BD3sXnt1OrtA%3D%3D (Pubitemid 36109749)
48. JF Lyons S Wilhelm B Hibner G Bollag 2001 Discovery of a novel Raf kinase inhibitor Endocr Relat Cancer 8 3 219 225 11566613 10.1677/erc.0.0080219 1:CAS:528:DC%2BD3MXotlCqsLc%3D (Pubitemid 32947644)
49. SR Wedge J Kendrew LF Hennequin PJ Valentine ST Barry SR Brave NR Smith NH James M Dukes JO Curwen R Chester JA Jackson SJ Boffey LL Kilburn S Barnett GH Richmond PF Wadsworth M Walker AL Bigley ST Taylor L Cooper S Beck JM Jurgensmeier DJ Ogilvie 2005 AZD2171: a highly potent, orally bioavailable, vascular endothelial growth factor receptor-2 tyrosine kinase inhibitor for the treatment of cancer Cancer Res 65 10 4389 4400 10.1158/0008-5472.CAN-04-4409 15899831 10.1158/0008-5472.CAN-04-4409 1:CAS:528:DC%2BD2MXktlSmtLs%3D (Pubitemid 40775678)
50. Lorusso P, Shields AF, Gadgeel S, Vaishampayan U, Guthrie T, Puchalski T, Xu J, Liu Q (2010) Cediranib in combination with various anticancer regimens: results of a phase I multi-cohort study. Invest New Drugs. doi: 10.1007/s10637-010-9484-5
51. Loriot Y, Mordant P, Dorvault N, De la Motte Rouge T, Bourhis J, Soria JC, Deutsch E (2010) BMS-690514, a VEGFR and EGFR tyrosine kinase inhibitor, shows anti-tumoural activity on non-small-cell lung cancer xenografts and induces sequence-dependent synergistic effect with radiation. Br J Cancer 103(3):347-353. doi: 10.1038/sj.bjc.6605748
52. AL Myers RF Williams CY Ng JE Hartwich AM Davidoff 2010 Bevacizumab-induced tumor vessel remodeling in rhabdomyosarcoma xenografts increases the effectiveness of adjuvant ionizing radiation J Pediatr Surg 45 6 1080 1085 10.1016/jjpedsurg.2010.02.068 20620299 10.1016/j.jpedsurg.2010.02.068