Apigenin attenuates insulin-like growth factor-I signaling in an autochthonous mouse prostate cancer model

Pharmaceutical Research

Volumn 29, Issue 6, 2012, Pages 1506-1517

  Shukla, Sanjeev ^a,b   MacLennan, Gregory T ^a,b   Fu, Pingfu ^a,c   Gupta, Sanjay ^a,b,c  

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

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

angiogenesis; apigenin; insulin like growth factor; metastasis; prostate cancer

Indexed keywords

APIGENIN; GELATINASE A; GELATINASE B; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C; UROKINASE; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GROWTH; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; ENZYME INHIBITION; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BLOOD LEVEL; SIGNAL TRANSDUCTION; TREATMENT DURATION; TREATMENT RESPONSE; WESTERN BLOTTING;

ADENOCARCINOMA; ADMINISTRATION, ORAL; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APIGENIN; BLOTTING, WESTERN; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INSULIN-LIKE GROWTH FACTOR I; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TIME FACTORS; TUMOR BURDEN; UROKINASE-TYPE PLASMINOGEN ACTIVATOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84862679196     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-011-0625-0     Document Type: Article

References (41)

1. GA Lima LL Corrêa R Gabrich LC Miranda MR Gadelha 2009 IGF-I, insulin and prostate cancer Arq Bras Endocrinol Metabol. 53 8 969 975 20126849 10.1590/S0004-27302009000800010
2. DS Meinbach BL Lokeshwar 2006 Insulin-like growth factors and their binding proteins in prostate cancer: cause or consequence? Urol Oncol. 24 4 294 306 16818181 10.1016/j.urolonc.2005.12.004 1:CAS:528:DC%2BD28Xms1Grtr8%3D
3. A Wolk CS Mantzoros SO Andersson R Bergström LB Signorello P Lagiou, et al. 1998 Insulin-like growth factor 1 and prostate cancer risk: a population-based, case-control study J Natl Cancer Inst. 90 12 911 915 9637140 10.1093/jnci/90.12.911 1:CAS:528:DyaK1cXktFOqsLc%3D
4. AH Ismail M Pollak H Behlouli S Tanguay LR Begin AG Aprikian 2002 Insulin-like growth factor-1 and insulin-like growth factor binding protein-3 for prostate cancer detection in patients undergoing prostate biopsy J Urol. 168 6 2426 2430 10.1016/S0022-5347(05)64160-2
5. NE Allen TJ Key PN Appleby RC Travis AW Roddam S Rinaldi, et al. 2007 Serum insulin-like growth factor (IGF)-I and IGF-binding protein-3 concentrations and prostate cancer risk: results from the European Prospective Investigation into Cancer and Nutrition Cancer Epidemiol Biomarkers Prev. 16 6 1121 1127 17548673 10.1158/1055-9965.EPI-06-1062 1:CAS:528:DC%2BD2sXmtVKnt7w%3D
6. JM Chan MJ Stampfer E Giovannucci PH Gann J Ma P Wilkinson, et al. 1998 Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study Science. 279 5350 563 566 9438850 10.1126/science.279.5350.563 1:CAS:528:DyaK1cXotVOqsg%3D%3D
7. MK Tennant JB Thrasher PA Twomey RS Birnbaum SR Plymate 1996 Insulin-like growth factor-binding protein-2 and -3 expression in benign human prostate epithelium, prostate intraepithelial neoplasia, and adenocarcinoma of the prostate J Clin Endocrinol Metab. 81 1 411 420 8550786 10.1210/jc.81.1.411 1:CAS:528:DyaK28XkvV2itg%3D%3D
8. SF Shariat DJ Lamb MW Kattan C Nguyen J Kim J Beck, et al. 2002 Association of preoperative plasma levels of insulin-like growth factor I and insulin-like growth factor binding proteins-2 and -3 with prostate cancer invasion, progression, and metastasis J Clin Oncol. 20 3 833 841 11821468 10.1200/JCO.20.3.833 1:CAS:528:DC%2BD38XhsVGmtL0%3D
9. PJ Kaplan S Mohan P Cohen BA Foster NM Greenberg 1999 The insulin-like growth factor axis and prostate cancer: lessons from the transgenic adenocarcinoma of mouse prostate (TRAMP) model Cancer Res. 59 9 2203 2209 10232609 1:CAS:528:DyaK1MXjtVWjtrk%3D
10. J Furukawa CJ Wraight SM Freier E Peralta LM Atley BP Monia, et al. 2010 Antisense oligonucleotide targeting of insulin-like growth factor-1 receptor (IGF-1R) in prostate cancer Prostate. 70 2 206 218 19790231 1:CAS:528: DC%2BC3cXitlagtL8%3D
11. J DiGiovanni K Kiguchi A Frijhoff E Wilker DK Bol L Beltrán, et al. 2000 Deregulated expression of insulin-like growth factor 1 in prostate epithelium leads to neoplasia in transgenic mice Proc Natl Acad Sci U S A. 97 7 3455 3460 10737798 10.1073/pnas.97.7.3455 1:CAS:528:DC%2BD3cXitlWqt7Y%3D
12. YZ Wang YC Wong 1998 Sex hormone-induced prostatic carcinogenesis in the noble rat: the role of insulin-like growth factor-I (IGF-I) and vascular endothelial growth factor (VEGF) in the development of prostate cancer Prostate. 35 3 165 177 9582085 10.1002/(SICI)1097-0045(19980515)35:3<165::AID- PROS2>3.0.CO;2-G 1:CAS:528:DyaK1cXjtVKltr0%3D
13. MG Slomiany SA Rosenzweig 2006 Hypoxia-inducible factor-1-dependent and -independent regulation of insulin-like growth factor-1-stimulated vascular endothelial growth factor secretion J Pharmacol Exp Ther. 318 2 666 675 16682453 10.1124/jpet.106.104158 1:CAS:528:DC%2BD28XnslOlsb0%3D
14. N Soulitzis I Karyotis D Delakas DA Spandidos 2006 Expression analysis of peptide growth factors VEGF, FGF2, TGFB1, EGF and IGF1 in prostate cancer and benign prostatic hyperplasia Int J Oncol. 29 2 305 314 16820871 1:CAS:528:DC%2BD28XotFKmtbc%3D
15. S Shukla S Gupta 2010 Apigenin: a promising molecule for cancer prevention Pharm Res. 27 6 962 978 20306120 10.1007/s11095-010-0089-7 1:CAS:528:DC%2BC3cXjs1ehurs%3D
16. SC Gupta JH Kim S Prasad BB Aggarwal 2010 Regulation of survival, proliferation, invasion, angiogenesis, and metastasis of tumor cells through modulation of inflammatory pathways by nutraceuticals Cancer Metastasis Rev. 29 3 405 434 20737283 10.1007/s10555-010-9235-2 1:CAS:528:DC%2BC3cXhtFWqt7vN
17. RL Geahlen NM Koonchanok JL McLaughlin DE Pratt 1989 Inhibition of protein-tyrosine kinase activity by flavanoids and related compounds J Nat Prod. 52 5 982 986 2607357 10.1021/np50065a011 1:CAS:528:DyaK3cXjt1Ghsg%3D%3D
18. CA Franzen E Amargo V Todorović BV Desai S Huda S Mirzoeva, et al. 2009 The chemopreventive bioflavonoid apigenin inhibits prostate cancer cell motility through the focal adhesion kinase/Src signaling mechanism Cancer Prev Res (Phila). 2 9 830 841 10.1158/1940-6207.CAPR-09-0066 1:CAS:528: DC%2BC3cXpt1Squr8%3D
19. S Shukla S Gupta 2007 Apigenin-induced cell cycle arrest is mediated by modulation of MAPK, PI3K-Akt, and loss of cyclin D1 associated retinoblastoma dephosphorylation in human prostate cancer cells Cell Cycle. 6 9 1102 1114 17457054 10.4161/cc.6.9.4146 1:CAS:528:DC%2BD2sXhtVSgu7vN
20. G Wang KA Ahmad NH Harris K Ahmed 2008 Impact of protein kinase CK2 on inhibitor of apoptosis proteins in prostate cancer cells Mol Cell Biochem. 316 1-2 91 97 18574673 10.1007/s11010-008-9810-9 1:CAS:528:DC%2BD1cXhtVansrvM
21. S Shukla A Mishra P Fu GT MacLennan MI Resnick S Gupta 2005 Up-regulation of insulin-like growth factor binding protein-3 by apigenin leads to growth inhibition and apoptosis of 22Rv1 xenograft in athymic nude mice FASEB J. 19 14 2042 2044 16230333 1:CAS:528:DC%2BD2MXhtlSlsr%2FF
22. S Shukla S Gupta 2009 Apigenin suppresses insulin-like growth factor I receptor signaling in human prostate cancer: an in vitro and in vivo study Mol Carcinog. 48 3 243 252 18726972 10.1002/mc.20475 1:CAS:528:DC%2BD1MXjtFGqsbw%3D
23. S Shukla GT MacLennan CA Flask P Fu A Mishra MI Resnick, et al. 2007 Blockade of beta-catenin signaling by plant flavonoid apigenin suppresses prostate carcinogenesis in TRAMP mice Cancer Res. 67 14 6925 6935 17638904 10.1158/0008-5472.CAN-07-0717 1:CAS:528:DC%2BD2sXnslOitr0%3D
24. PC Hollman MB Katan 1999 Dietary flavonoids: intake, health effects and bioavailability Food Chem Toxicol. 37 9-10 937 942 10541448 1:CAS:528: DyaK1MXnsFSku7s%3D
25. PJ Kaplan-Lefko TM Chen MM Ittmann RJ Barrios GE Ayala WJ Huss, et al. 2003 Pathobiology of autochthonous prostate cancer in a pre-clinical transgenic mouse model Prostate. 55 3 219 237 12692788 10.1002/pros.10215
26. O Rho DJ Kim K Kiguchi J Digiovanni 2011 Growth factor signaling pathways as targets for prevention of epithelial carcinogenesis Mol Carcinog. 50 4 264 279 20648549 10.1002/mc.20665 1:CAS:528:DC%2BC3MXktFKit7k%3D
27. Z Kelman 1997 PCNA: structure, functions and interactions Oncogene. 14 6 629 640 9038370 10.1038/sj.onc.1200886 1:CAS:528:DyaK2sXhsVent7s%3D
28. VM Adhami IA Siddiqui N Ahmad S Gupta H Mukhtar 2004 Oral consumption of green tea polyphenols inhibits insulin-like growth factor-I-induced signaling in an autochthonous mouse model of prostate cancer Cancer Res. 64 23 8715 8722 15574782 10.1158/0008-5472.CAN-04-2840 1:CAS:528:DC%2BD2cXhtVCjs7rE
29. P Liu H Cheng TM Roberts JJ Zhao 2009 Targeting the phosphoinositide 3-kinase pathway in cancer Nat Rev Drug Discov. 8 8 627 644 19644473 10.1038/nrd2926 1:CAS:528:DC%2BD1MXpt1Wgtb4%3D
30. D Sarker AH Reid TA Yap JS de Bono 2009 Targeting the PI3K/AKT pathway for the treatment of prostate cancer Clin Cancer Res. 15 15 4799 4805 19638457 10.1158/1078-0432.CCR-08-0125 1:CAS:528:DC%2BD1MXptl2gsLo%3D
31. F Llorens FA Miró A Casañas N Roher L Garcia M Plana, et al. 2004 Unbalanced activation of ERK1/2 and MEK1/2 in apigenin-induced HeLa cell death Exp Cell Res. 299 1 15 26 15302569 10.1016/j.yexcr.2004.05.006 1:CAS:528:DC%2BD2cXmsVKgtbk%3D
32. AJ Levine Z Feng TW Mak H You S Jin 2006 Coordination and communication between the p53 and IGF-1-AKT-TOR signal transduction pathways Genes Dev. 20 3 267 275 16452501 10.1101/gad.1363206 1:CAS:528:DC%2BD28XhsFens7w%3D
33. P Kaur S Shukla S Gupta 2008 Plant flavonoid apigenin inactivates Akt to trigger apoptosis in human prostate cancer: an in vitro and in vivo study Carcinogenesis. 29 11 2210 2217 18725386 10.1093/carcin/bgn201 1:CAS:528:DC%2BD1cXhtlalsLnE
34. A Latil I Bièche S Pesche A Valéri G Fournier O Cussenot, et al. 2000 VEGF overexpression in clinically localized prostate tumors and neuropilin-1 overexpression in metastatic forms Int J Cancer. 89 2 167 171 10754495 10.1002/(SICI)1097-0215(20000320)89:2<167::AID-IJC11>3.0.CO;2-9 1:CAS:528:DC%2BD3cXislehs78%3D
35. J Chen S De J Brainard TV Byzova 2004 Metastatic properties of prostate cancer cells are controlled by VEGF Cell Commun Adhes. 11 1 1 11 15500293 10.1080/15419060490471739
36. SE Dunn JV Torres JS Oh DM Cykert JC Barrett 2001 Up-regulation of urokinase-type plasminogen activator by insulin-like growth factor-I depends upon phosphatidylinositol-3 kinase and mitogen-activated protein kinase kinase Cancer Res. 61 4 1367 1374 11245436 1:CAS:528:DC%2BD3MXhvVeltrg%3D
37. MH Kim 2003 Flavonoids inhibit VEGF/bFGF-induced angiogenesis in vitro by inhibiting the matrix-degrading proteases J Cell Biochem. 89 3 529 538 12761886 10.1002/jcb.10543 1:CAS:528:DC%2BD3sXksVKktbs%3D
38. R Kumar J Yoneda CD Bucana IJ Fidler 1998 Regulation of distinct steps of angiogenesis by different angiogenic molecules Int J Oncol. 12 4 749 757 9499433 1:CAS:528:DyaK1cXitlejtrs%3D
39. C Bosetti L Spertini M Parpinel P Gnagnarella P Lagiou E Negri, et al. 2005 Flavonoids and breast cancer risk in Italy Cancer Epidemiol Biomarkers Prev. 14 4 805 808 15824147 10.1158/1055-9965.EPI-04-0838 1:CAS:528: DC%2BD2MXjtFSktbg%3D
40. CC Simons LA Hughes IC Arts RA Goldbohm PA van den Brandt MP Weijenberg 2009 Dietary flavonol, flavone and catechin intake and risk of colorectal cancer in the Netherlands Cohort Study Int J Cancer. 125 12 2945 2952 19530252 10.1002/ijc.24645 1:CAS:528:DC%2BD1MXhtlSqsLvK
41. MA Gates SS Tworoger JL Hecht I De Vivo B Rosner SE Hankinson 2007 A prospective study of dietary flavonoid intake and incidence of epithelial ovarian cancer Int J Cancer. 121 10 2225 2232 17471564 10.1002/ijc.22790 1:CAS:528:DC%2BD2sXht1aisL7L