Plumbagin, a medicinal plant (Plumbago zeylanica)-derived 1,4-naphthoquinone, inhibits growth and metastasis of human prostate cancer PC-3M-luciferase cells in an orthotopic xenograft mouse model

Molecular Oncology

Volumn 7, Issue 3, 2013, Pages 428-439

  Hafeez, Bilal Bin ^a   Zhong, Weixiong ^a   Fischer, Joseph W ^a   Mustafa, Ala ^a   Shi, Xudong ^a   Meske, Louise ^a   Hong, Hao ^b   Cai, Weibo ^b   Havighurst, Thomas ^a   Kim, KyungMann ^a   Verma, Ajit K ^a  

^a UNIVERSITY OF WISCONSIN   (United States)

^b University of Wisconsin Health   (United States)

Author keywords

Orthotopic xenograft model; PCa; PKC ; PL; Plumbagin; Prostate cancer; Stat3

Indexed keywords

CD31 ANTIGEN; GELATINASE A; GELATINASE B; INDUCIBLE NITRIC OXIDE SYNTHASE; KI 67 ANTIGEN; PLUMBAGIN; PROTEIN BCL XL; STAT3 PROTEIN; SURVIVIN; UROKINASE; UVOMORULIN; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN RETRIEVAL; ARTICLE; BIOLUMINESCENCE; BODY WEIGHT; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CANCER TRANSPLANTATION; CONTROLLED STUDY; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LIVER METASTASIS; LUNG METASTASIS; LYMPH NODE METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; PLUMBAGO ZEYLANICA; PRIORITY JOURNAL; PROSTATE CANCER; TREATMENT DURATION; TUMOR XENOGRAFT; WESTERN BLOTTING;

MUS; MUS MUSCULUS; PLUMBAGO ZEYLANICA;

EID: 84878142242     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2012.12.001     Document Type: Article

References (48)

1. Aalinkeel R., Nair B.B., Reynolds J.L., Sykes D.E., Mahajan S.D., Chadha K.C., Schwartz S.A. Overexpression of MMP-9 contributes to invasiveness of prostate cancer cell line LNCaP. Immunol. Invest. 2011, 40(5):447-464.
2. Albertsen P. Predicting survival for men with clinically localized prostate cancer: what do we need in contemporary practice?. Cancer 2008, 112:1-3.
3. Aziz M.H., Manoharan H.T., Church D.R., Dreckschmidt N.E., Zhong W., Oberley T.D., Wilding G., Verma A.K. Protein kinase C epsilon interacts with signal transducers and activators of transcription 3 (Stat3), phosphorylates Stat3Ser727, and regulates its constitutive activation in prostate cancer. Cancer Res. 2007, 67(18):8828-8838.
4. Aziz M.H., Manoharan H.T., Verma A.K. Protein kinase C epsilon, which sensitizes skin to sun's UV radiation-induced cutaneous damage and development of squamous cell carcinomas, associates with Stat3. Cancer Res. 2007, 67(3):1385-1394.
5. Aziz M.H., Dreckschmidt N.E., Verma A.K. Plumbagin, a medicinal plant-derived naphthoquinone, is a novel inhibitor of the growth and invasion of hormone-refractory prostate cancer. Cancer Res. 2008, 68:9024-9032.
6. Aziz M.H., Hafeez B.B., Sand J.M., Pierce D.B., Aziz S.W., Dreckschmidt N.E., Verma A.K. Protein kinase C epsilon mediates Stat3Ser727 phosphorylation, Stat3-regulated gene expression, and cell invasion in various human cancer cell lines through integration with MAPK cascade (RAF-1, MEK1/2, and ERK1/2). Oncogene 2010, 29(21):3100-3109.
7. Benavides F., Blando J., Perez C.J., Garg R., Conti C.J., DiGiovanni J., Kazanietz M.G. Transgenic overexpression of PKCε in the mouse prostate induces preneoplastic lesions. Cell Cycle 2011, 10(2):268-277.
8. Boxler S., Djonov V., Kessler T.M., Hlushchuk R., Bachmann L.M., Held U., Markwalder R., Thalmann G.N. Matrix metalloproteinases and angiogenic factors: predictors of survival after radical prostatectomy for clinically organ-confined prostate cancer?. Am. J. Pathol. 2010, 177(5):2216-2224.
9. Bubendorf L., Schöpfer A., Wagner U., Sauter G., Moch H., Willi N., Gasser T.C., Mihatsch M.J. Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum. Pathol. 2000, 31(5):578-583.
10. Coulter J.A., Page N.L., Worthington J., Robson T., Hirst D.G., McCarthy H.O. Transcriptional regulation of inducible nitric oxide synthase gene therapy: targeting early stage and advanced prostate cancer. J. Gene Med. 2010, 12(9):755-765.
11. Courboulin A., Barrier M., Perreault T., Bonnet P., Tremblay V.L., Paulin R., Tremblay E., Lambert C., Jacob M.H., Bonnet S.N., Provencher S., Bonnet S. Plumbagin reverses proliferation and resistance to apoptosis in experimental PAH. Eur. Respir. J. 2012, 40(3):618-629.
12. Gomathinayagam R., Sowmyalakshmi S., Mardhatillah F., Kumar R., Akbarsha M.A., Damodaran C. Anticancer mechanism of plumbagin, a natural compound, on non-small cell lung cancer cells. Anticancer Res. 2008, 28(2A):785-792.
13. Grandis J.R., Drenning S.D., Zeng Q., Watkins S.C., Melhem M.F., Endo S., Johnson D.E., Huang L., He Y., Kim J.D. Constitutive activation of Stat3 signaling abrogates apoptosis in squamous cell carcinogenesis in vivo. Proc. Natl. Acad. Sci. U.S.A 2000, 97(8):4227-4232.
14. Gritsko T., Williams A., Turkson J., Kaneko S., Bowman T., Huang M., Nam S., Eweis I., Diaz N., Sullivan D., Yoder S., Enkemann S., Eschrich S., Lee J.H., Beam C.A., Cheng J., Minton S., Muro-Cacho C.A., Jove R. Persistent activation of stat3 signaling induces survivin gene expression and confers resistance to apoptosis in human breast cancer cells. Clin. Cancer Res. 2006, 12(1):11-19.
15. Hafeez B.B., Zhong W., Weichert J., Dreckschmidt N.E., Jamal M.S., Verma A.K. Genetic ablation of PKC epsilon inhibits prostate cancer development and metastasis in transgenic mouse model of prostate adenocarcinoma. Cancer Res. 2011, 71(6):2318-2327.
16. Hafeez B.B., Jamal M.S., Fischer J.W., Mustafa A., Verma A.K. Plumbagin, a plant derived natural agent inhibits the growth of pancreatic cancer cells in in vitro and in vivo via targeting EGFR, Stat3 and NF-κB signaling pathways. Int. J. Cancer 2012, 131(9):2175-2186.
17. Hafeez B.B., Zhong W., Mustafa A., Fischer J.W., Witkowsky O., Verma A.K. Plumbagin inhibits prostate cancer development in TRAMP mice via targeting PKC{varepsilon}, Stat3 and neuroendocrine markers. Carcinogenesis 2012, 33(12):2586-2592.
18. Hsu Y.L., Cho C.Y., Kuo P.L., Huang Y.T., Lin C.C. Plumbagin (5-hydroxy-2-methyl-1,4-naphthoquinone) induces apoptosis and cell cycle arrest in A549 cells through p53 accumulation via c-Jun NH2-terminal kinase-mediated phosphorylation at serine 15 in vitro and in vivo. J. Pharmacol. Exp. Ther. 2006, 318(2):484-494.
19. Jenkins D.E., Yu S.F., Hornig Y.S., Purchio T., Contag P.R. In vivo monitoring of tumor relapse and metastasis using bioluminescent PC-3M-luc-C6 cells in murine models of human prostate cancer. Clin. Exp. Metastasis 2003, 20(8):745-756.
20. Kelly W.K., Halabi S., Carducci M.A., George D.J., Mahoney J.F., Stadler W.M., Morris M.J., Kantoff P.W., Monk J.P., Small E.J. Liver metastasis (LM) to predict for short overall survival (OS) in metastatic castration resistant prostate cancer (mCRPC) patients (pts). J. Clin. Oncol. 2012, 30. (Supp; abstract 4655).
21. Koren R., Ben Meir D., Langzam L., Dekel Y., Konichezky M., Baniel J., Livne P.M., Gal R., Sampson S.R. Expression of protein kinase C isoenzymes in benign hyperplasia and carcinoma of prostate. Oncol. Rep. 2004, 11(2):321-326.
22. Lai L., Liu J., Zhai D., Lin Q., He L., Dong Y., Zhang J., Lu B., Chen Y., Yi Z., Liu M. Plumbagin inhibits tumour angiogenesis and tumour growth through the Ras signalling pathway following activation of the VEGF receptor-2. Br. J. Pharmacol. 2012, 165(4b):1084-1096. [Epub ahead of print]. 10.1111/j.1476-5381.2011.01532.x.9.
23. Lee H.J., Yu H.K., Papadopoulos J.N., Kim S.W., He J., Park Y.K., Yoon Y., Kim J.S., Kim S.J. Targeted antivascular therapy with the apolipoprotein(a) kringle V, rhLK8, inhibits the growth and metastasis of human prostate cancer in an orthotopic nude mouse model. Neoplasia 2012, 14(4):335-343.
24. Li Z., Xiao J., Wu X., Li W., Yang Z., Xie J., Xu L., Cai X., Lin Z., Guo W., Luo J., Liu M. Plumbagin inhibits breast tumor bone metastasis and osteolysis by modulating the tumor-bone microenvironment. Curr. Mol. Med. 2012, 8:967-981.
25. Liu C., Liu J., Wang X., Mao W., Jiang L., Ni H., Mo M., Wang W. Prognostic impact of nm23-H1 and PCNA expression in pathologic stage I non-small cell lung cancer. J. Surg. Oncol. 2011, 104(2):181-186.
26. Martínez-Gimeno C., Díaz-Meco M.T., Domínguez I., Moscat J. Alterations in levels of different protein kinase C isotypes and their influence on behavior of squamous cell carcinoma of the oral cavity: epsilon PKC, a novel prognostic factor for relapse and survival. Head Neck 1995, 17(6):516-525.
27. McJilton M.A., Van Sikes C., Wescott G.G. Protein kinase C epsilon interacts with Bax and promotes survival of human prostate cancer cells. Oncogene 2003, 22:7958-7968.
28. Nguyen D.X., Bos P.D., Massagué J. Metastasis: from dissemination to organ-specific colonization. Nat. Rev. Cancer 2009, 9(4):274-284.
29. Padhye S., Dandawate P., Yusufi M., Ahmad A., Sarkar F.H. Perspectives on medicinal properties of plumbagin and its analogs. Med. Res. Rev. 2012, 32(6):1131-1158.
30. Pan Q., Bao L.W., Kleer C.G., Sabel M.S., Griffith K.A., Teknos T.N., Merajver S.D. Protein kinase C epsilon is a predictive biomarker of aggressive breast cancer and a validated target for RNA interference anticancer therapy. Cancer Res. 2005, 65(18):8366-8371.
31. Powolny A.A., Singh S.V. Plumbagin-induced apoptosis in human prostate cancer cells is associated with modulation of cellular redox status and generation of reactive oxygen species. Pharm. Res. 2008, 25(9):2171-2180.
32. R.Core Development Team R: a Language and Environment for Statistical Computing 2011, R Foundation for Statistical Computing, Vienna, Austria, URL. http://www.r-project.org.
33. Ravindra K.C., Selvi B.R., Arif M., Reddy B.A., Thanuja G.R., Agrawal S., Pradhan S.K., Nagashayana N., Dasgupta D., Kundu T.K. Inhibition of lysine acetyltransferase KAT3B/p300 activity by a naturally occurring hydroxynaphthoquinone, plumbagin. J. Biol. Chem. 2009, 284(36):24453-24464.
34. Rosol T.J., Tannehill-Gregg S.H., LeRoy B.E., Mandl S., Contag C.H. Animal models of bone metastasis. Cancer 2003, 97(Suppl. 3):748-757. Review.
35. Sand J.M., Hafeez B.B., Jamal M.S., Witkowsky O., Siebers E.M., Fischer J., Verma A.K. Plumbagin (5-hydroxy-2-methyl-1,4-naphthoquinone), isolated from Plumbago zeylanica, inhibits ultraviolet radiation-induced development of squamous cell carcinomas. Carcinogenesis 2012, 33(1):184-190.
36. Sandur S.K., Ichikawa H., Sethi G., Ahn K.S., Aggarwal B.B. Plumbagin (5-hydroxy-methyl-1,4-naphthoquinone) suppresses NF-kappaB activation and NF-kappaB-regulated gene products through modulation of p65 and lkappaBalpha kinase activation, leading to potentiation of apoptosis induced by cytokine and chemotherapeutic agents. J. Biol. Chem. 2006, 281:17023-17033.
37. Shariat S.F., Roehrborn C.G., McConnell J.D., Park S., Alam N., Wheeler T.M., Slawin K.M. Association of the circulating levels of the urokinase system of plasminogen activation with the presence of prostate cancer and invasion, progression, and metastasis. J. Clin. Oncol. 2007, 25(4):349-355.
38. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2012. CA Cancer J. Clin. 2012, 62(1):10-29.
39. Sinha S., Pal K., Elkhanany A., Dutta S., Cao Y., Mondal G., Iyer S., Somasundaram V., Couch F.J., Shridhar V., Bhattacharya R., Mukhopadhyay D., Srinivas P. Plumbagin inhibits tumorigenesis and angiogenesis of ovarian cancer cells in vivo. Int. J. Cancer 2012 Jul 17, [Epub ahead of print]. 10.1002/ijc.27724.
40. So A., Gleave M., Hurtado-Col A., Nelson C. Mechanisms of the development of androgen independence in prostate cancer. World J. Urol. 2005, 23:1-9.
41. Son T.G., Camandola S., Arumugam T.V., Cutler R.G., Telljohann R.S., Mughal M.R., Moore T.A., Luo W., Yu Q.S., Johnson D.A., Johnson J.A., Greig N.H., Mattson M.P. Plumbagin, a novel Nrf2/ARE activator, protects against cerebral ischemia. J. Neurochem. 2010, 112(5):1316-1326.
42. Steeg P.S. Tumor metastasis: mechanistic insights and clinical challenges. Nat. Med. 2006, 12(8):895-904.
43. Sugie S., Okamoto K., Rahman K.M., Tanaka T., Kawai K., Yamahara J., Mori H. Inhibitory effects of plumbagin and juglone on azoxymethane-induced intestinal carcinogenesis in rats. Cancer Lett. 1998, 127(1-2):177-183.
44. Sung B., Oyajobi B., Aggarwal B.B. Plumbagin inhibits osteoclastogenesis and reduces human breast cancer-induced osteolytic bone metastasis in mice through suppression of RANKL signaling. Mol. Cancer Ther. 2012, 11(2):350-359.
45. Wang C.C., Chiang Y.M., Sung S.C., Hsu Y.L., Chang J.K., Kuo P.L. Plumbagin induces cell cycle arrest and apoptosis through reactive oxygen species/c-Jun N-terminal kinase pathways in human melanoma A375.S2 cells. Cancer Lett. 2008, 259:82-98.
46. Wu D., Foreman T.L., Gregory C.W., McJilton M.A., Wescott G.G., Ford O.H., Alvey R.F., Mohler J.L., Terrian D.M. Protein kinase C epsilon has the potential to advance the recurrence of human prostate cancer. Cancer Res. 2002, 62(8):2423-2429.
47. Zhang J., Sud S., Mizutani K., Gyetko M.R., Pienta K.J. Activation of urokinase plasminogen activator and its receptor axis is essential for macrophage infiltration in a prostate cancer mouse model. Neoplasia 2011, 13(1):23-30.
48. Zhao H., Lo Y.H., Ma L., Waltz S.E., Gray J.K., Hung M.C., Wang S.C. Targeting tyrosine phosphorylation of PCNA inhibits prostate cancer growth. Mol. Cancer Ther. 2011, 10(1):29-36.