Apigenin attenuates neointima formation via suppression of vascular smooth muscle cell phenotypic transformation

Journal of Cellular Biochemistry

Volumn 113, Issue 4, 2012, Pages 1198-1207

  Guan, Hongjing ^a,b   Gao, Lu ^c   Zhu, Lihua ^a,b   Yan, Ling ^a,b   Fu, Mingyue ^a,b   Chen, Changgui ^a,b   Dong, Xuan ^a,b   Wang, Lang ^a,b   Huang, Kai ^c   Jiang, Hong ^a,b  

^a RENMIN HOSPITAL OF WUHAN UNIVERSITY   (China)

^b WUHAN UNIVERSITY   (China)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

APIGENIN; NEOINTIMA; PLATELET DERIVED GROWTH FACTOR; VASCULAR SMOOTH MUSCLE CELL

Indexed keywords

APIGENIN; BIOLOGICAL MARKER; BROXURIDINE; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLINE; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; STAT3 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAROTID ARTERY INJURY; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL MIGRATION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; FLOW CYTOMETRY; HYPERPLASIA; MALE; MOUSE; NEOINTIMA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TUNICA MEDIA; VASCULAR SMOOTH MUSCLE;

ANIMALS; APIGENIN; BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; DNA REPLICATION; DOWN-REGULATION; IMMUNOHISTOCHEMISTRY; MALE; MUSCLE, SMOOTH, VASCULAR; PLATELET-DERIVED GROWTH FACTOR; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTO-ONCOGENE PROTEINS C-SIS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TUNICA INTIMA;

EID: 84863119124     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23452     Document Type: Article

References (46)

1. Bauters C, Isner JM,. 1997. The biology of restenosis. Prog Cardiovasc Dis 40: 107-116.
2. Bauters C, Meurice T, Hamon M, McFadden E, Lablanche JM, Bertrand ME,. 1996. Mechanisms and prevention of restenosis: From experimental models to clinical practice. Cardiovasc Res 31: 835-846.
3. Bianchi M, De Lucchini S, Marin O, Turner DL, Hanks SK, Villa-Moruzzi E,. 2005. Regulation of FAK Ser-722 phosphorylation and kinase activity by GSK3 and PP1 during cell spreading and migration. Biochem J 391: 359-370.
4. Braidy N, Grant R, Adams S, Guillemin GJ,. 2010. Neuroprotective effects of naturally occurring polyphenols on quinolinic acid-induced excitotoxicity in human neurons. FEBS J 277: 368-382.
5. Castro C, Diez-Juan A, Cortes MJ, Andres V,. 2003. Distinct regulation of mitogen-activated protein kinases and p27Kip1 in smooth muscle cells from different vascular beds. A potential role in establishing regional phenotypic variance. J Biol Chem 278: 4482-4490.
6. Dandre F, Owens GK,. 2004. Platelet-derived growth factor-BB and Ets-1 transcription factor negatively regulate transcription of multiple smooth muscle cell differentiation marker genes. Am J Physiol Heart Circ Physiol 286: H2042-H2051.
7. Diehl JA, Cheng M, Roussel MF, Sherr CJ,. 1998. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12: 3499-3511.
8. Diez-Juan A, Andres V,. 2003. Coordinate control of proliferation and migration by the p27Kip1/cyclin-dependent kinase/retinoblastoma pathway in vascular smooth muscle cells and fibroblasts. Circ Res 92: 402-410.
9. Galaria II, Nicholl SM, Roztocil E, Davies MG,. 2005. Urokinase-induced smooth muscle cell migration requires PI3-K and Akt activation. J Surg Res 127: 46-52.
10. Goukassian D, Diez-Juan A, Asahara T, Schratzberger P, Silver M, Murayama T, Isner JM, Andres V,. 2001. Overexpression of p27(Kip1) by doxycycline-regulated adenoviral vectors inhibits endothelial cell proliferation and migration and impairs angiogenesis. FASEB J 15: 1877-1885.
11. Graf BA, Milbury PE, Blumberg JB,. 2005. Flavonols, flavones, flavanones, and human health: Epidemiological evidence. J Med Food 8: 281-290.
12. Gupta S, Afaq F, Mukhtar H,. 2002. Involvement of nuclear factor-kappa B, Bax and Bcl-2 in induction of cell cycle arrest and apoptosis by apigenin in human prostate carcinoma cells. Oncogene 21: 3727-3738.
13. Heederik D, Kromhout H, Burema J, Biersteker K, Kromhout D,. 1990. Occupational exposure and 25-year incidence rate of non-specific lung disease: the Zutphen Study. Int J Epidemiol 19: 945-952.
14. Heldin CH, Ostman A, Ronnstrand L,. 1998. Signal transduction via platelet-derived growth factor receptors. Biochim Biophys Acta 1378: F79-113.
15. Karpurapu M, Wang D, Van Quyen D, Kim TK, Kundumani-Sridharan V, Pulusani S, Rao GN,. 2010. Cyclin D1 is a bona fide target gene of NFATc1 and is sufficient in the mediation of injury-induced vascular wall remodeling. J Biol Chem 285: 3510-3523.
16. Karsch KR, Haase KK, Wehrmann M, Hassenstein S, Hanke H,. 1991. Smooth muscle cell proliferation and restenosis after stand alone coronary excimer laser angioplasty. J Am Coll Cardiol 17: 991-994.
17. Kim TJ, Zhang YH, Kim Y, Lee CK, Lee MK, Hong JT, Yun YP,. 2002. Effects of apigenin on the serum- and platelet derived growth factor-BB-induced proliferation of rat aortic vascular smooth muscle cells. Planta Med 68: 605-609.
18. Knekt P, Jarvinen R, Seppanen R, Hellovaara M, Teppo L, Pukkala E, Aromaa A,. 1997. Dietary flavonoids and the risk of lung cancer and other malignant neoplasms. Am J Epidemiol 146: 223-230.
19. Kovacic JC, Gupta R, Lee AC, Ma M, Fang F, Tolbert CN, Walts AD, Beltran LE, San H, Chen G, St Hilaire C, Boehm M,. 2010. Stat3-dependent acute Rantes production in vascular smooth muscle cells modulates inflammation following arterial injury in mice. J Clin Invest 120: 303-314.
20. Kuhel DG, Zhu B, Witte DP, Hui DY,. 2002. Distinction in genetic determinants for injury-induced neointimal hyperplasia and diet-induced atherosclerosis in inbred mice. Arterioscler Thromb Vasc Biol 22: 955-960.
21. Lagna G, Ku MM, Nguyen PH, Neuman NA, Davis BN, Hata A,. 2007. Control of phenotypic plasticity of smooth muscle cells by bone morphogenetic protein signaling through the myocardin-related transcription factors. J Biol Chem 282: 37244-37255.
22. Lamy S, Bedard V, Labbe D, Sartelet H, Barthomeuf C, Gingras D, Beliveau R,. 2008. The dietary flavones apigenin and luteolin impair smooth muscle cell migration and VEGF expression through inhibition of PDGFR-beta phosphorylation. Cancer Prev Res (Phila) 1: 452-459.
23. Leslie K, Lang C, Devgan G, Azare J, Berishaj M, Gerald W, Kim YB, Paz K, Darnell JE, Albanese C, Sakamaki T, Pestell R, Bromberg J,. 2006. Cyclin D1 is transcriptionally regulated by and required for transformation by activated signal transducer and activator of transcription 3. Cancer Res 66: 2544-2552.
24. Malumbres M, Barbacid M,. 2001. To cycle or not to cycle: A critical decision in cancer. Nat Rev Cancer 1: 222-231.
25. McVean M, Weinberg WC, Pelling JC,. 2002. A p21(waf1)-independent pathway for inhibitory phosphorylation of cyclin-dependent kinase p34(cdc2) and concomitant G(2)/M arrest by the chemopreventive flavonoid apigenin. Mol Carcinog 33: 36-43.
26. Owens GK, Kumar MS, Wamhoff BR,. 2004. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767-801.
27. Ricupero DA, Poliks CF, Rishikof DC, Kuang PP, Goldstein RH,. 2001. Apigenin decreases expression of the myofibroblast phenotype. FEBS Lett 506: 15-21.
28. Ruela-de-Sousa RR, Fuhler GM, Blom N, Ferreira CV, Aoyama H, Peppelenbosch MP,. 2010. Cytotoxicity of apigenin on leukemia cell lines: Implications for prevention and therapy. Cell Death Dis 1: e19.
29. Sato F, Matsukawa Y, Matsumoto K, Nishino H, Sakai T,. 1994. Apigenin induces morphological differentiation and G2-M arrest in rat neuronal cells. Biochem Biophys Res Commun 204: 578-584.
30. Shanmugam K, Holmquist L, Steele M, Stuchbury G, Berbaum K, Schulz O, Benavente Garcia O, Castillo J, Burnell J, Garcia Rivas V, Dobson G, Munch G,. 2008. Plant-derived polyphenols attenuate lipopolysaccharide-induced nitric oxide and tumour necrosis factor production in murine microglia and macrophages. Mol Nutr Food Res 52: 427-438.
31. Shibata R, Kai H, Seki Y, Kato S, Wada Y, Hanakawa Y, Hashimoto K, Yoshimura A, Imaizumi T,. 2003. Inhibition of STAT3 prevents neointima formation by inhibiting proliferation and promoting apoptosis of neointimal smooth muscle cells. Hum Gene Ther 14: 601-610.
32. Shukla S, Gupta S,. 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: 1102-1114.
33. Shukla S, Gupta S,. 2009. Apigenin suppresses insulin-like growth factor I receptor signaling in human prostate cancer: An in vitro and in vivo study. Mol Carcinog 48: 243-252.
34. Shukla S, Gupta S,. 2010. Apigenin: A promising molecule for cancer prevention. Pharm Res 27: 962-978.
35. Siddique YH, Afzal M,. 2009. Antigenotoxic effect of apigenin against mitomycin C induced genotoxic damage in mice bone marrow cells. Food Chem Toxicol 47: 536-539.
36. Singh JP, Selvendiran K, Banu SM, Padmavathi R, Sakthisekaran D,. 2004. Protective role of Apigenin on the status of lipid peroxidation and antioxidant defense against hepatocarcinogenesis in Wistar albino rats. Phytomedicine 11: 309-314.
37. Sriram V, Patterson C,. 2001. Cell cycle in vasculoproliferative diseases: Potential interventions and routes of delivery. Circulation 103: 2414-2419.
38. Sun J, Marx SO, Chen HJ, Poon M, Marks AR, Rabbani LE,. 2001. Role for p27(Kip1) in vascular smooth muscle cell migration. Circulation 103: 2967-2972.
39. Trochon V, Blot E, Cymbalista F, Engelmann C, Tang RP, Thomaidis A, Vasse M, Soria J, Lu H, Soria C,. 2000. Apigenin inhibits endothelial-cell proliferation in G(2)/M phase whereas it stimulates smooth-muscle cells by inhibiting P21 and P27 expression. Int J Cancer 85: 691-696.
40. Tseng AS, Engel FB, Keating MT,. 2006. The GSK-3 inhibitor BIO promotes proliferation in mammalian cardiomyocytes. Chem Biol 13: 957-963.
41. Wang AB, Li HL, Zhang R, She ZG, Chen HZ, Huang Y, Liu DP, Liang CC,. 2007. A20 attenuates vascular smooth muscle cell proliferation and migration through blocking PI3k/Akt singling in vitro and in vivo. J Biomed Sci 14: 357-371.
42. Wang W, Heideman L, Chung CS, Pelling JC, Koehler KJ, Birt DF,. 2000. Cell-cycle arrest at G2/M and growth inhibition by apigenin in human colon carcinoma cell lines. Mol Carcinog 28: 102-110.
43. Way TD, Kao MC, Lin JK,. 2004. Apigenin induces apoptosis through proteasomal degradation of HER2/neu in HER2/neu-overexpressing breast cancer cells via the phosphatidylinositol 3-kinase/Akt-dependent pathway. J Biol Chem 279: 4479-4489.
44. Way TD, Kao MC, Lin JK,. 2005. Degradation of HER2/neu by apigenin induces apoptosis through cytochrome c release and caspase-3 activation in HER2/neu-overexpressing breast cancer cells. FEBS Lett 579: 145-152.
45. Weintraub WS,. 2007. The pathophysiology and burden of restenosis. Am J Cardiol 100: 3K-9K.
46. Zhang YH, Park YS, Kim TJ, Fang LH, Ahn HY, Hong JT, Kim Y, Lee CK, Yun YP,. 2000. Endothelium-dependent vasorelaxant and antiproliferative effects of apigenin. Gen Pharmacol 35: 341-347.