Dihydroartemisinin inhibits angiogenesis in pancreatic cancer by targeting the NF-κB pathway

Cancer Chemotherapy and Pharmacology

Volumn 68, Issue 6, 2011, Pages 1421-1430

  Wang, Shuang Jia ^a,b   Sun, Bei ^a   Cheng, Zhuo Xin ^a   Zhou, Hao Xin ^a   Gao, Yue ^a,c   Kong, Rui ^a   Chen, Hua ^a   Jiang, Hong Chi ^a   Pan, Shang Ha ^a   Xue, Dong Bo ^a   Bai, Xue Wei ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF XIAMEN UNIVERSITY   (China)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antiangiogenesis; Dihydroartemisinin; Nuclear factor B; Pancreatic cancer

Indexed keywords

CD31 ANTIGEN; CYCLOOXYGENASE 2; DIHYDROARTEMISININ; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER INHIBITION; CAPILLARY; CAPILLARY TUBE FORMATION; CELL PROLIFERATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG DOSE COMPARISON; DRUG TARGETING; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROVESSEL DENSITY; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; TUMOR VASCULARIZATION; TUMOR VOLUME; TUMOR XENOGRAFT;

ANGIOGENESIS INHIBITORS; ANIMALS; ARTEMISININS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; ENDOTHELIAL CELLS; HUMANS; MALE; MICE; NEOVASCULARIZATION, PATHOLOGIC; NF-KAPPA B; PANCREATIC NEOPLASMS;

EID: 82455192206     PISSN: 03445704     EISSN: 14320843     Source Type: Journal    
DOI: 10.1007/s00280-011-1643-7     Document Type: Article

References (38)

1. A Jemal T Murray E Ward A Samuels RC Tiwari A Ghafoor 2005 Cancer statistics CA Cancer J Clin 55 10 30 15661684 10.3322/canjclin.55.1.10
2. MP Liu JY Ma BR Pa LS Ma 2001 The study of pancreatic cancer in China World Chin J Digestol 9 1103 1109
3. D Li K Xie R WolV R Wolff JL Abbruzzese 2004 Pancreatic cancer Lancet 363 1049 1057 15051286 10.1016/S0140-6736(04)15841-8 1:CAS:528:DC%2BD2cXisFOmsLY%3D (Pubitemid 38410779)
4. D Mu W Zhang D Chu T Liu Y Xie E Fu 2008 The role of calcium, P38 MAPK in dihydroartemisinin-induced apoptosis of lung cancer PC-14 cells Cancer Chemother Pharmac 61 639 645 10.1007/s00280-007-0517-5 1:CAS:528: DC%2BD1cXjsFaisQ%3D%3D
5. Q He J Shi XL Shen J An H Sun L Wang 2010 Dihydroartemisinin upregulates death receptor 5 expression and cooperates with TRAIL to induce apoptosis in human prostate cancer cells Cancer Biol Ther 9 819 824 20224297 10.4161/cbt.9.10.11552 1:CAS:528:DC%2BC3cXhtlKrtrnF
6. J Hou D Wang R Zhang H Wang 2008 Experimental therapy of hepatoma with artemisinin and its derivatives: in vitro and in vivo activity, chemosensitization, and mechanisms of action Clin Cancer Res 14 5519 5530 18765544 10.1158/1078-0432.CCR-08-0197 1:CAS:528:DC%2BD1cXhtVKmsbnE
7. H Chen B Sun S Wang Y Gao X Bai 2010 Growth inhibitory effects of dihydroartemisinin on pancreatic cancer cells: involvement of cell cycle arrest and inactivation of nuclear factor-kappaB J Cancer Res Clin Oncol 136 897 903 19941148 10.1007/s00432-009-0731-0 1:CAS:528:DC%2BC3cXltVagt7s%3D
8. SJ Wang Y Gao H Chen R Kong HC Jiang SH Pan 2010 Dihydroartemisinin inactivates NF-kappaB and potentiates the anti-tumor effect of gemcitabine on pancreatic cancer both in vitro and in vivo Cancer Lett 293 99 108 20137856 10.1016/j.canlet.2010.01.001 1:CAS:528:DC%2BC3cXlsVyit70%3D
9. H Chen B Sun SH Pan H Jiang X Sun 2009 Dihydroartemisinin inhibits growth of pancreatic cancer cells in vitro and in vivo Anticancer Drugs 20 131 140 19209030 10.1097/CAD.0b013e3283212ade
10. HH Chen HJ Zhou X Fang 2003 Inhibition of human cancer cell line growth and human umbilical vein endothelial cell angiogenesis by artemisinin derivatives in vitro Pharmacol Res 48 231 236 12860439 10.1016/S1043-6618(03) 00107-5 1:CAS:528:DC%2BD3sXltl2hu7c%3D (Pubitemid 36818928)
11. HH Chen HJ Zhou WQ Wang GD Wu 2004 Antimalarial dihydroartemisinin also inhibits angiogenesis Cancer Chemother Pharmacol 53 423 432 15132130 10.1007/s00280-003-0751-4 1:CAS:528:DC%2BD2cXivVCltbc%3D (Pubitemid 38553665)
12. S D'Alessandro M Gelati N Basilico EA Parati RK Haynes D Taramelli 2007 Differential effects on angiogenesis of two antimalarial compounds, dihydroartemisinin and artemisone: implications for embryotoxicity Toxicology 241 66 74 17897768 10.1016/j.tox.2007.08.084 (Pubitemid 47599780)
13. T Efferth 2006 Molecular pharmacology and pharmacogenomics of artemisinin and its derivatives in cancer cells Curr Drug Targ 407 407 421 10.2174/138945006776359412 (Pubitemid 43744832)
14. M Wartenberg S Wolf P Budde F Grünheck H Acker J Hescheler 2003 The antimalaria agent artemisinin exerts antiangiogenic effects in mouse embryonic stem cell-derived embryoid bodies Lab Invest 83 1647 1655 14615418 10.1097/01.LAB.0000098424.38003.FF 1:CAS:528:DC%2BD3sXoslyksbg%3D (Pubitemid 37421105)
15. XJ Huang ZQ Ma WP Zhang 2007 Dihydroartemisinin exerts cytotoxic effects and inhibits hypoxia inducible factor-1alpha activation in C6 glioma cells J Pharm Pharmacol 59 849 856 17637177 10.1211/jpp.59.6.0011 1:CAS:528: DC%2BD2sXmtlKntb0%3D (Pubitemid 47051097)
16. HJ Zhou WQ Wang GD Wu YB Lu EQ Wei 2007 Artesunate inhibits angiogenesis and downregulates vascular endothelial growth factor expression in chronic myeloid leukemia K562 cells Vascul Pharmacol 47 131 138 17581794 10.1016/j.vph.2007.05.002 1:CAS:528:DC%2BD2sXot1ylsr4%3D (Pubitemid 47095451)
17. R Dell'Eva U Pfeffer R Vené L Anfosso A Forlani A Albini 2004 Inhibition of angiogenesis in vivo and growth of Kaposi's sarcoma xenograft tumors by the anti-malarial artesunate Biochem Pharmaco 68 2359 2366 10.1016/j.bcp.2004.08.021 (Pubitemid 39535108)
18. W Wang JL Abbruzzese DB Evans L Larry KR Cleary PJ Chiao 1999 The nuclear factor-kappa B RelA transcription factor is constitutively activated in human pancreatic adenocarcinoma cells Clin Cancer Res 5 119 127 9918209 1:CAS:528:DyaK1MXhtVShtLY%3D (Pubitemid 29045184)
19. S Liptay CK Weber L Ludwig M Wagner G Adler RM Schmid 2003 Mitogenic and antiapoptotic role of constitutive NF-κB/Relactivity in pancreatic cancer Int J Cancer 105 735 746 12767057 10.1002/ijc.11081 1:CAS:528: DC%2BD3sXltVSis7k%3D (Pubitemid 36706095)
20. HQ Xiong JL Abbruzzese E Lin L Wang L Zheng K Xie 2004 NF-kappaB activity blockade impairs the angiogenic potential of human pancreatic cancer cells Int J Cancer 108 181 188 14639600 10.1002/ijc.11562 1:CAS:528:DC%2BD3sXhtVWgu7zO (Pubitemid 37541768)
21. BB Aggarwal 2004 Nuclear factor-κB: the enemy within Cancer Cell 6 203 208 15380510 10.1016/j.ccr.2004.09.003 1:CAS:528:DC%2BD2cXot1Kis78%3D (Pubitemid 39222032)
22. J Folkman 1986 How is blood vessel growth regulated in normal and neoplastic tissue? G.H.A. Clowes memorial Award lecture Cancer Res 46 467 473 2416426 1:CAS:528:DyaL28Xos1aiug%3D%3D (Pubitemid 16145386)
23. JR Gamble LJ Matthias G Meyer P Kaur G Russ R Faull 1993 Regulation of in vitro capillary tube formation by anti-integrin antibodies J Cell Biol 121 931 943 8491784 10.1083/jcb.121.4.931 1:CAS:528:DyaK3sXktVGkur4%3D (Pubitemid 23143553)
24. R Kong B Sun HC Jiang S Pan H Chen S Wang 2010 Downregulation of nuclear factor-κB p65 subunit by small interfering RNA synergizes with gemcitabine to inhibit the growth of pancreatic cancer Cancer Lett 291 90 98 19880242 10.1016/j.canlet.2009.10.001 1:CAS:528:DC%2BC3cXjvFKhurw%3D
25. T Nakamura T Kuwai JS Kim D Fan SJ Kim IJ Fidler 2007 Stromal metalloproteinase-9 is essential to angiogenesis and progressive growth of orthotopic human pancreatic cancer in parabiont nude mice Neoplasia 9 979 986 18030366 10.1593/neo.07742 1:CAS:528:DC%2BD2sXhtl2rtrrI (Pubitemid 350086443)
26. NP Singh HC Lai 2004 Artemisinin induces apoptosis in human cancer cells Anticancer Res 24 2277 2280 15330172 1:CAS:528:DC%2BD2cXot1Cgur8%3D (Pubitemid 39166306)
27. Y Matsuo H Sawai N Ochi A Yasuda M Sakamoto H Takahashi 2010 Proteasome inhibitor MG132 inhibits angiogenesis in pancreatic cancer by blocking NF-κB activity Dig Dis Sci 55 1167 1176 19399612 10.1007/s10620-009-0814-4 1:CAS:528:DC%2BC3cXjtlahtrs%3D
28. J Itakura T Ishiwata H Friess H Fujii Y Matsumoto MW Büchler 1997 Enhanced expression of vascular endothelial growth factor in human pancreatic cancer correlates with local disease progression Clin Cancer Res 3 1309 1316 9815813 1:CAS:528:DyaK2sXls1Smtrk%3D (Pubitemid 27362391)
29. Q Shi JL Abbruzzese S Huang IJ Fidler Q Xiong K Xie 1999 Constitutive and inducible interleukin 8 expression by hypoxia and acidosis renders human pancreatic cancer cells more tumorigenic and metastatic Clin Cancer Res 5 7234 7243
30. MK Gupta RY Qin 2003 Mechanism and its regulation of tumor-induced angiogenesis World J Gastroenterol 9 1144 1155 12800214 1:CAS:528: DC%2BD3sXlvVSrtb4%3D (Pubitemid 36805642)
31. AE Koch PJ Polverini SL Kunkel LA Harlow LA DiPietro VM Elner 1992 Interleukin-8 as a macrophage-derived mediator of angiogenesis Science 258 1798 1801 1281554 10.1126/science.1281554 1:CAS:528:DyaK3sXlslyktg%3D%3D (Pubitemid 23087348)
32. S Huang JB Robinson A Deguzman CD Bucana IJ Fidler 2000 Blockade of nuclear factor-kappaB signaling inhibits angiogenesis and tumorigenicity of human ovarian cancer cells by suppressing expression of vascular endothelial growth factor and interleukin 8 Cancer Res 60 5334 5339 11034066 1:CAS:528:DC%2BD3cXns1ehsL8%3D
33. (2+)- or PI3K-dependent signaling pathway in a human vascular endothelial cell line FEBS Lett 579 6451 6458 16288746 10.1016/j.febslet.2005.10.027 1:CAS:528: DC%2BD2MXht1ens7vM (Pubitemid 41612167)
34. G Bergers R Brekken G McMahon TH Vu T Itoh K Tamaki 2000 Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis Nat Cell Biol 2 737 744 11025665 10.1038/35036374 1:CAS:528:DC%2BD3cXnsVyntLk%3D
35. SM Plummer KA Holloway MM Manson RJ Munks A Kaptein S Farrow 1999 Inhibition of cyclooxygenase 2 expression in colon cells by the chemopreventive agent curcumin involves inhibition of NF-kappaB activation via the NIK/IKK signalling complex Oncogene 18 6013 6020 10557090 10.1038/sj.onc.1202980 1:CAS:528:DyaK1MXntlGitb8%3D (Pubitemid 29535013)
36. JL Masferrer KM Leahy AT Koki BS Zweifel SL Settle BM Woerner 2000 Antiangiogenic and antitumor activities of cyclooxygenase-2 inhibitors Cancer Res 60 1306 1311 10728691 1:CAS:528:DC%2BD3cXhvFWrt74%3D (Pubitemid 30151999)
37. JG Rozic C Chakraborty PK Lala 2001 Cyclooxygenase inhibitors retard murine mammary tumor progression by reducing tumor cell migration, invasiveness and angiogenesis Int J Cancer 93 497 506 11477553 10.1002/ijc.1376 1:CAS:528:DC%2BD3MXlsVCntrs%3D (Pubitemid 32701408)
38. JS Chu FL Lloyd OC Trifan B Knapp MT Rizzo 2003 Potential involvement of the cyclooxygenase-2 pathway in the regulation of tumor-associated angiogenesis and growth in pancreatic cancer Mol Cancer Ther 2 1 7 12533667 1:CAS:528:DC%2BD3sXhtlOitrs%3D