SU5416 and EGCG work synergistically and inhibit angiogenic and survival factors and induce cell cycle arrest to promote apoptosis in human malignant neuroblastoma SH-SY5Y and SK-N-BE2 cells

Neurochemical Research

Volumn 36, Issue 8, 2011, Pages 1383-1396

  Mohan, Nishant ^a   Karmakar, Surajit ^a   Banik, Naren L ^b   Ray, Swapan K ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Angiogenesis; Apoptosis; EGCG; Neuroblastoma; SU4516

Indexed keywords

CASPASE 3; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR 1; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIGALLOCATECHIN GALLATE; FIBROBLAST GROWTH FACTOR 2; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; POLYPHENOL DERIVATIVE; PROTEIN BCL 2; RETINOBLASTOMA PROTEIN; SEMAXANIB; TRANSCRIPTION FACTOR E2F1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL LINE; CELL MIGRATION; CELL STRAIN SH SY5Y; CELL STRAIN SK N BE2; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG POTENTIATION; HUMAN; HUMAN CELL; NEUROBLASTOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; TEA;

ANGIOGENESIS INHIBITORS; ANTICARCINOGENIC AGENTS; APOPTOSIS; CATECHIN; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; E2F1 TRANSCRIPTION FACTOR; HUMANS; IN SITU NICK-END LABELING; INDOLES; NEOVASCULARIZATION, PATHOLOGIC; NEUROBLASTOMA; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRROLES; RETINOBLASTOMA PROTEIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 79961207043     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-011-0463-9     Document Type: Article

References (57)

1. GM Brodeur 2003 Neuroblastoma: biological insights into a clinical enigma Nat Rev Cancer 3 203 216 12612655 10.1038/nrc1014 1:CAS:528: DC%2BD3sXhsFGhtr0%3D (Pubitemid 37328872)
2. JL Weinstein HM Katzenstein SL Cohn 2003 Advances in the diagnosis and treatment of neuroblastoma Oncologist 8 278 292 12773750 10.1634/theoncologist. 8-3-278 (Pubitemid 36648814)
3. E Hiyama T Iehara T Sugimoto M Fukuzawa Y Hayashi F Sasaki M Sugiyama S Kondo A Yoneda H Yamaoka T Tajiri K Akazawa M Ohtaki 2008 Effectiveness of screening for neuroblastoma at 6 months of age: a retrospective population-based cohort study Lancet 371 1173 1180 18395578 10.1016/S0140-6736(08)60523-1 (Pubitemid 351458522)
4. B Meister F Grunebach F Bautz W Brugger FM Fink L Kanz R Möhle 1999 Expression of vascular endothelial growth factor (VEGF) and its receptors in human neuroblastoma Eur J Cancer 35 445 449 10448297 10.1016/S0959-8049(98) 00387-6 1:STN:280:DyaK1MznslCjtA%3D%3D (Pubitemid 29151943)
5. J Rossler S Breit W Havers L Schweigerer 1999 Vascular endothelial growth factor expression in human neuroblastoma: up-regulation by hypoxia Int J Cancer 81 113 117 10077161 10.1002/(SICI)1097-0215(19990331)81:1<113::AID- IJC19>3.0.CO;2-L 1:CAS:528:DyaK1MXhvVKrsrY%3D (Pubitemid 29124205)
6. A Eggert N Ikegaki J Kwiatkowski 2006 High-level expression of angiogenic factors is associated with advanced tumor stage in human neuroblastomas Clin Cancer Res 6 1900 1908
7. D Meiter SE Crawford AW Rademaker S Cohn 1996 Tumor angiogenesis correlates with metastatic disease, N-myc amplification, and poor outcome in human neuroblastoma J Clin Oncol 14 405 414 (Pubitemid 26051001)
8. TA Fong LK Shawyer L Sun C Tang H App TJ Powell YH Kim R Schreck X Wang W Risau A Ullrich KP Hirth G McMahon 1999 SU5416 is a potent and selective inhibitor of the vascular endothelial growth factor receptor (Flk-1/KDR) that inhibits tyrosine kinase catalysis, tumor vascularization, and growth of multiple tumor types Cancer Res 59 99 106 9892193 1:CAS:528:DyaK1MXmsFOgug%3D%3D (Pubitemid 29062964)
9. DB Mendel AD Laird BD Smolich RA Blake C Liang AL Hannah RM Shaheen LM Ellis S Weitman LK Shawver JM Cherrington 2000 Development of SU5416, a selective small molecule inhibitor of VEGF receptor tyrosine kinase activity, as an anti-angiogenesis agent Anti-cancer Drug Des 15 29 41 1:CAS:528: DC%2BD3cXksF2ntLc%3D (Pubitemid 30364897)
10. AC Peterson S Swiger WM Stadler 2004 Phase II study of the Flk-1 tyrosine kinase inhibitor SU5416 in advanced melanoma Clin Cancer Res 10 4048 4054 15217937 10.1158/1078-0432.CCR-03-0766 1:CAS:528:DC%2BD2cXltFWmtbc%3D (Pubitemid 38812480)
11. U Bäckman A Svensson R Christofferson 2002 Importance of vascular endothelial growth factor A in the progression of experimental neuroblastoma Angiogenesis 5 267 274 12906318 10.1023/A:1024564817563 (Pubitemid 36875125)
12. K Saeki N Kobayashi Y Inazawa H Zhang H Nishitoh H Ichijo K Saeki M Isemura A Yuo 2002 Oxidation-triggered c-Jun N-terminal kinase (JNK) and p38 mitogen-activated protein (MAP) kinase pathways for apoptosis in human leukaemic cells stimulated by epigallocatechin-3-gallate (EGCG): a distinct pathway from those of chemically induced and receptor-mediated apoptosis Biochem J 368 705 720 12206715 10.1042/BJ20020101 1:CAS:528:DC%2BD38Xptlykt70%3D (Pubitemid 36042672)
13. S Gupta T Hussain H Mukhtar 2003 Molecular pathway for (-)-epigallocatechin-3-gallate-induced cell cycle arrest and apoptosis of human prostate carcinoma cells Arch Biochem Biophys 410 177 185 12559991 10.1016/S0003-9861(02)00668-9 1:CAS:528:DC%2BD3sXmsVCitA%3D%3D (Pubitemid 36268810)
14. IA Siddiqui A Malik VM Adhami M Asim BB Hafeez S Sarfaraz H Mukhtar 2008 Green tea polyphenol EGCG sensitizes human prostate carcinoma LNCaP cells to TRAIL-mediated apoptosis and synergistically inhibits biomarkers associated with angiogenesis and metastasis Oncogene 27 2055 2063 17998943 10.1038/sj.onc. 1210840 1:CAS:528:DC%2BD1cXjslWjtr4%3D (Pubitemid 351442738)
15. A Mittal MS Pate RC Wylie 2004 EGCG down-regulates telomerase in human breast carcinoma MCF-7 cells, leading to suppression of cell viability and induction of apoptosis Int J Oncol 24 703 710 14767556 1:CAS:528: DC%2BD2cXitFantb0%3D
16. S Shankar S Ganapathy SR Hingorani RK Srivastava 2008 EGCG inhibits growth, invasion, angiogenesis and metastasis of pancreatic cancer Front Biosci 13 440 452 17981559 10.2741/2691 (Pubitemid 351599756)
17. A Das NL Banik SK Ray 2006 Mechanism of apoptosis with the involvement of calpain and caspase cascades in human malignant neuroblastoma SH-SY5Y cells exposed to flavonoids Int J Cancer 119 2575 2585 16988947 10.1002/ijc.22228 1:CAS:528:DC%2BD28XhtFygtbfI (Pubitemid 44691310)
18. A Das NL Banik SK Ray 2009 Retinoids induce differentiation and down regulate telomerase activity and N-Myc to increase sensitivity to flavonoids for apoptosis in human malignant neuroblastoma SH-SY5Y cells Int J Oncol 34 757 765 19212680 1:CAS:528:DC%2BD1MXjs1Kgsbc%3D
19. LB Zhang K Smith AL Chong 2009 In vivo antitumor and antimetastatic activity of sunitinib in preclinical neuroblastoma mouse model Neoplasia 11 426 435 19412427 1:CAS:528:DC%2BD1MXltFaitrg%3D
20. J Vandesompele A Edsjö K De Preter H Axelson F Speleman S Påhlman 2003 ID2 expression in neuroblastoma does not correlate to MYCN levels and lacks prognostic value Oncogene 22 456 460 12545167 10.1038/sj.onc.1206148 1:CAS:528:DC%2BD3sXlsV2ksA%3D%3D (Pubitemid 36194342)
21. D Goldschneider E Horvilleur LF Plassa M Guillaud-Bataille K Million E Wittmer-Dupret G Danglot H de Thé J Bénard E May S Douc-Rasy 2006 Expression of C-terminal deleted p53 isoforms in neuroblastoma Nucleic Acids Res 34 5603 5612 17028100 10.1093/nar/gkl619 1:CAS:528:DC%2BD28Xht1Srt7bL (Pubitemid 44742447)
22. TC Chou 2006 Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies Pharmacol Rev 58 621 681 16968952 10.1124/pr.58.3.10 1:CAS:528:DC%2BD28XhtVOhtLfL (Pubitemid 44403686)
23. N Mohan S Karmakar SR Choudhury NL Banik SK Ray 2009 Bcl-2 inhibitor HA14-1 and genistein together adeptly down regulated survival factors and activated cysteine proteases for apoptosis in human malignant neuroblastoma SK-N-BE2 and SH-SY5Y cells Brain Res 1283 155 166 19505441 10.1016/j.brainres. 2009.05.097 1:CAS:528:DC%2BD1MXptVCjsrk%3D
24. RM Shaheen DW Davis W Liu BK Zebrowski MR Wilson CD Bucana DJ McConkey G McMahon LM Ellis 1999 Antiangiogenic therapy targeting the tyrosine kinase receptor for vascular endothelial growth factor receptor inhibits the growth of colon cancer liver metastasis and induces tumor and endothelial cell apoptosis Cancer Res 59 5412 5416 10554007 1:CAS:528:DyaK1MXnt1Gjtbg%3D (Pubitemid 29526446)
25. WJ Huss RJ Barrios NM Greenberg 2003 SU5416 selectively impairs angiogenesis to induce prostate cancer-specific apoptosis Mol Cancer Ther 2 611 616 12883033 1:CAS:528:DC%2BD3sXmsFGksbg%3D
26. T Takamoto M Sasaki T Kuno N Tamaki 2001 Flk-1 specific kinase inhibitor (SU5416) inhibited the growth of GS-9L glioma in rat brain and prolonged the survival Kobe J Med Sci 47 181 191 11733657 1:CAS:528:DC%2BD38XitlGlsLc%3D (Pubitemid 34101040)
27. X Zhong X Li G Wang Y Zhu G Hu J Zhao C Neace H Ding E Reed QQ Li 2004 Mechanisms underlying the synergistic effect of SU5416 and cisplatin on cytotoxicity in human ovarian tumor cells Int J Oncol 2 445 451
28. C Ye D Sweeny J Sukbuntherng Q Zhang W Tan S Wong A Madan B Ogilvie A Parkinson L Antonian 2006 Distribution, metabolism, and excretion of the anti-angiogenic compound SU5416 Toxicol In Vitro 20 154 162 16321501 10.1016/j.tiv.2005.06.047 1:CAS:528:DC%2BD28XksVensg%3D%3D (Pubitemid 43087699)
29. YD Jung MS Kim BA Shin KO Chay BW Ahn W Liu CD Bucana GE Gallick LM Ellis 2001 EGCG, a major component of green tea, inhibits tumour growth by inhibiting VEGF induction in human colon carcinoma cells Br J Cancer 84 844 850 11259102 10.1054/bjoc.2000.1691 1:CAS:528:DC%2BD3MXivVGrt7Y%3D (Pubitemid 32275661)
30. S Brierley-Hobson 2007 Binding of (-)-epigallocatechin-3-gallate to the Hsp70 ATPase domain may promote apoptosis in colorectal cancer Biosci Horiz 1 9 18 10.1093/biohorizons/hzn002
31. S Qanungo M Das S Haldar A Basu 2005 Epigallocatechin-3-gallate induces mitochondrial membrane depolarization and caspase-dependent apoptosis in pancreatic cancer cells Carcinogenesis 26 958 967 15705601 10.1093/carcin/bgi040 1:CAS:528:DC%2BD2MXjsFOms74%3D (Pubitemid 41214325)
32. L Kalfon MB Youdim SA Mandel 2007 Green tea polyphenol (-)- epigallocatechin-3-gallate promotes the rapid protein kinase C- and proteasome-mediated degradation of Bad: implications for neuroprotection J Neurochem 100 992 1002 17156130 10.1111/j.1471-4159.2006.04265.x 1:CAS:528:DC%2BD2sXisFGnu7w%3D (Pubitemid 46213924)
33. L Wang S Xu X Xu P Chan 2009 (-)-Epigallocatechin-3-gallate protects SH-SY5Y cells against 6-OHDA-induced cell death through STAT3 activation J Alzheimers Dis 17 295 304 19221405 1:CAS:528:DC%2BD1MXmvVOiurs%3D
34. L Lamalice F Houle J Huot 2006 Phosphorylation of Tyr1214 within VEGFR-2 triggers the recruitment of Nck and activation of Fyn leading to SAPK2/p38 activation and endothelial cell migration in response to VEGF J Biol Chem 281 34009 34020 16966330 10.1074/jbc.M603928200 1:CAS:528:DC%2BD28XhtFKgtbjF (Pubitemid 46036610)
35. T Itokawa H Nokihara Y Nishioka S Sone Y Iwamoto Y Yamada J Cherrington G McMahon M Shibuya M Kuwano M Ono 2002 Antiangiogenic effect by SU5416 is partly attributable to inhibition of Flt-1 receptor signaling Mol Cancer Ther 1 295 302 12489845 1:CAS:528:DC%2BD38XjtFWmsrs%3D
36. T Punathil TO Tollefsbol SK Katiyar 2008 EGCG inhibits mammary cancer cell migration through inhibition of nitric oxide synthase and guanylate cyclase Biochem Biophys Res Commun 375 162 167 18692479 10.1016/j.bbrc.2008.07.157 1:CAS:528:DC%2BD1cXhtVOit73O
37. 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 11399 11404 12177446 10.1073/pnas.172398399 1:CAS:528:DC%2BD38XmslSmu7g%3D (Pubitemid 34920937)
38. N Zaghloul SL Hernandez JO Bae J Huang JC Fisher A Lee A Kadenhe-Chiweshe JJ Kandel DJ Yamashiro 2009 Vascular endothelial growth factor blockade rapidly elicits alternative proangiogenic pathways in neuroblastoma Int J Oncol 4 401 407
39. BL Mirkin SH Clark C Zhang 2002 Inhibition of human neuroblastoma cell proliferation and EGF receptor phosphorylation by gangliosides GM1, GM3, GD1A and GT1B Cell Prolif 35 105 111 11952645 10.1046/j.1365-2184.2002.00228.x 1:CAS:528:DC%2BD38XjsFOnt7s%3D (Pubitemid 34603857)
40. R Janardhanan NL Banik SK Ray 2009 N-Myc down regulation induced differentiation, early cell cycle exit, and apoptosis in human malignant neuroblastoma cells having wild type or mutant p53 Biochem Pharmacol 78 1105 1114 19540207 10.1016/j.bcp.2009.06.009 1:CAS:528:DC%2BD1MXhtFGqsLzK
41. R Ho JE Minturn T Hishiki H Zhao Q Wang A Cnaan J Maris AE Evans GM Brodeur 2005 Proliferation of human neuroblastomas mediated by the epidermal growth factor receptor Cancer Res 65 9868 9875 16267010 10.1158/0008-5472.CAN- 04-2426 1:CAS:528:DC%2BD2MXhtFKktLrN (Pubitemid 41541466)
42. J Rossler E Odenthal B Geoerger 2009 EGFR inhibition using gefitinib is not active in neuroblastoma cell lines Anticancer Res 29 1327 1334 19414383
43. HC Haspel GM Scicli G McMahon AG Scilcli 2002 Inhibition of vascular endothelial growth factor-associated tyrosine kinase activity with SU5416 blocks sprouting in the microvascular endothelial cell spheroid model of angiogenesis Microvasc Res 63 304 315 11969307 10.1006/mvre.2001.2383 1:CAS:528: DC%2BD38XjtVentbg%3D (Pubitemid 34971626)
44. AA Beg B Baltimore 1996 An essential role for NF-κB in preventing TNF-α-induced cell death Science 274 782 784 8864118 10.1126/science.274. 5288.782 1:CAS:528:DyaK28XmsFOhu70%3D (Pubitemid 26398258)
45. B Rayet C Gelinas 1999 Aberrant rel/nfkb genes and activity in human cancer Oncogene 18 6938 6947 10602468 10.1038/sj.onc.1203221 1:CAS:528:DyaK1MXotVyhtb4%3D
46. H Zhang Y Xiong D Beach 1993 Proliferating cell nuclear antigen and p21 are components of multiple cell cycle kinase complexes Mol Biol Cell 4 897 906 7903056 1:CAS:528:DyaK2cXhsF2msbk%3D (Pubitemid 23309425)
47. PD Adams WR Sellers SK Sharma AD Wu CM Nalin WG Kailin 1996 Identification of a cyclin-Cdk2 recognition motif present in substrates and p21-like cyclin-dependent kinase inhibitors Mol Cell Biol 16 6623 6633 8943316 1:CAS:528:DyaK28XntVyntbc%3D (Pubitemid 26389720)
48. H Zhu L Nie CG Maki 2005 Cdk2-dependent inhibition of p21 stability via a C-terminal cyclin-binding motif J Biol Chem 280 29282 29288 15964852 10.1074/jbc.M407352200 1:CAS:528:DC%2BD2MXntVegtrw%3D (Pubitemid 41161383)
49. GC Bao JG Wang A Jong 2006 Increased p21 expression and complex formation with cyclin E/Cdk2 in retinoid-induced pre-B lymphoma cell apoptosis FEBS Lett 580 3687 3693 16765349 10.1016/j.febslet.2006.05.052 1:CAS:528: DC%2BD28XmtVOmtLg%3D (Pubitemid 43902803)
50. CJ Sherr F McCormick 2008 The RB and p53 pathways in cancer Cancer Cell 2 103 112 10.1016/S1535-6108(02)00102-2
51. E Hernando Z Nahle G Juan E Diaz-Rodriguez M Alaminos M Hemann L Michel V Mittal W Gerald R Benezra SW Lowe C Cordon-Cardo 2004 Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control Nature 430 797 802 15306814 10.1038/nature02820 1:CAS:528:DC%2BD2cXmsVGls7c%3D (Pubitemid 39071352)
52. DL Burkhart J Sage 2008 Cellular mechanisms of tumour suppression by the retinoblastoma gene Nat Rev Cancer 8 671 682 18650841 10.1038/nrc2399 1:CAS:528:DC%2BD1cXhtVWksLfP
53. HZ Chen SY Tsai G Leone 2009 Emerging roles of E2Fs in cancer: an exit from cell cycle control Nat Rev Cancer 9 785 797 19851314 10.1038/nrc2696 1:CAS:528:DC%2BD1MXhtlSjtbfE
54. NN Danial 2007 BCL-2 family proteins: critical checkpoints of apoptotic cell death Clin Cancer Res 13 7254 7263 18094405 10.1158/1078-0432.CCR-07-1598 1:CAS:528:DC%2BD2sXhsVCktr%2FJ
55. JM Adams S Cory 2007 The Bcl-2 apoptotic switch in cancer development and therapy Oncogene 26 1324 1337 17322918 10.1038/sj.onc.1210220 1:CAS:528:DC%2BD2sXitVKhsL8%3D (Pubitemid 46328466)
56. S Shankar G Suthakar RK Srivastava 2007 Epigallocatechin-3-gallate inhibits cell cycle and induces apoptosis in pancreatic cancer Front Biosci 12 5039 5051 17569628 10.2741/2446 1:CAS:528:DC%2BD2sXosF2qs7k%3D
57. S Gupta K Hastak F Afaq N Ahmad H Mukhtar 2004 Essential role of caspases in epigallocatechin-3-gallate-mediated inhibition of nuclear factor-κB and induction of apoptosis Oncogene 23 2507 2522 14676829 10.1038/sj.onc.1207353 1:CAS:528:DC%2BD2cXis1Gmsbk%3D (Pubitemid 38520748)