Restoring chemotherapy and hormonetherapy sensitivity by parthenolide in a xenograft hormone refractory prostate cancer model

Prostate

Volumn 66, Issue 14, 2006, Pages 1498-1511

  Shanmugam, Rajasubramaniam ^a   Jayaprakasan, Vetrichelvan ^a   Gokmen Polar, Yesim ^a   Kelich, Stephanie ^b   Miller, Kathy D ^a   Yip Schneider, Michele ^a   Cheng, Liang ^a   Bhat Nakshatri, Poornima ^b   Sledge Jr , George W ^a   Nakshatri, Harikrishna ^a,b   Zheng, Qi Huang ^a   Miller, Michael A ^a   DeGrado, Timothy ^a   Hutchins, Gary D ^a   Sweeney, Christopher J ^a,c  

^a INDIANA UNIVERSITY   (United States)

^b WALTHER CANCER INSTITUTE   (United States)

^c MBBS   (United States)

Author keywords

Angiogenesis; Anti tumor; NF B; Parthenolide

Indexed keywords

ALPHA1 INTERFERON; ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; BICALUTAMIDE; COMPLEMENTARY DNA; DOCETAXEL; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12P40; INTERLEUKIN 1ALPHA; MATRIGEL; MITOGEN ACTIVATED PROTEIN KINASE 9; MITOGEN ACTIVATED PROTEIN KINASE P38; P SELECTIN GLYCOPROTEIN LIGAND 1; PARTHENOLIDE; SERUM AMYLOID A; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; VASCULAR CELL ADHESION MOLECULE 1; ANILIDE; ANTIANDROGEN; ANTINEOPLASTIC AGENT; BRIDGED COMPOUND; FIBROBLAST GROWTH FACTOR 2; NONSTEROID ANTIINFLAMMATORY AGENT; SESQUITERPENE; TAXANE; TAXOID; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER HORMONE THERAPY; CANCER INHIBITION; CANCER RESISTANCE; CAPILLARY PROLIFERATION; CONTROLLED STUDY; DRUG POTENTIATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DNA BINDING; ANIMAL; CYTOLOGY; DRUG EFFECT; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PROSTATE TUMOR; SCINTISCANNING; TUMOR CELL LINE; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

ANDROGEN ANTAGONISTS; ANILIDES; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTINEOPLASTIC AGENTS, PHYTOGENIC; BRIDGED COMPOUNDS; CELL LINE, TUMOR; DRUG SYNERGISM; ENDOTHELIUM, VASCULAR; FIBROBLAST GROWTH FACTOR 2; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MICE; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; NF-KAPPA B; PROSTATIC NEOPLASMS; SESQUITERPENES; TAXOIDS; TNF RECEPTOR-ASSOCIATED FACTOR 1; TNF RECEPTOR-ASSOCIATED FACTOR 2; UMBILICAL VEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33749068887     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.20482     Document Type: Article

References (53)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100(1)57-70.
2. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS Jr. NF-kappaB antiapoptosis: Induction of TRAF1 and TRAF2 and C-IAP1 and C-IAP2 to suppress caspase-8 activation. Science 1998;281(5383):1680-1683.
3. Li X, Stark GR. NFkappaB-dependent signaling pathways. Exp Hematol 2002;30(4):285-296.
4. Karin M, Cao Y, Greten FR, Li ZW. NF-kappaB in cancer: From innocent bystander to major culprit. Nat Rev Cancer 2002;2(4):301-310.
5. Sweeney C, Li L, Shanmugam R, Bhat-Nakshatri P, Jayaprakasan V, Baldridge LA, Gardner T, Smith M, Nakshatri H, Cheng L. Nuclear factor-kappaB is constitutively activated in prostate cancer in vitro and is overexpressed in prostatic intraepithelial neoplasia and adenocarcinoma of the prostate. Clin Cancer Res 2004;10(16):5501-5507.
6. Nakshatri H, Bhat-Nakshatri P, Martin DA, Goulet RJ Jr., Sledge GW Jr. Constitutive activation of NF-kappaB during progression of breast cancer to hormone-independent growth. Mol Cell Biol 1997;17(7):3629-3639.
7. Guzman ML, Rossi RM, Karnischky L, Li X, Peterson DR, Howard DS, Jordan CT. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood 2005;105(11):4163-4169.
8. Yip-Schneider MT, Nakshatri H, Sweeney CJ, Marshall MS, Wiebke EA, Schmidt CM. Parthenolide and sulindac cooperate to mediate growth suppression and inhibit the nuclear factorkappa B pathway in pancreatic carcinoma cells. Mol Cancer Ther 2005;4(4):587-594.
9. Nakanishi C, Toi M. Nuclear factor-kappaB inhibitors as sensitizers to anticancer drugs. Nat Rev Cancer 2005;5(4):297-309.
10. Pan Q, Bao LW, Merajver SD. Tetrathiomolybdate inhibits angiogenesis and metastasis through suppression of the NFkappaB signaling cascade. Mol Cancer Res 2003;1(10):701-706.
11. Balbay MD, Pettaway CA, Kuniyasu H, Inoue K, Ramirez E, Li E, Fidler IJ, Dinney CP. Highly metastatic human prostate cancer growing within the prostate of athymic mice overexpresses vascular endothelial growth factor. Clin Cancer Res 1999;5(4):783-789.
12. Melnyk O, Zimmerman M, Kim KJ, Shuman M. Neutralizing anti-vascular endothelial growth factor antibody inhibits further growth of established prostate cancer and metastases in a preclinical model. J Urol 1999;161(3):960-963.
13. Giri D, Ropiquet F, Ittmann M. Alterations in expression of basic fibroblast growth factor (FGF) 2 and its receptor FGFR-1 in human prostate cancer. Clin Cancer Res 1999;5(5):1063-1071.
14. Greene GF, Kitadai Y, Pettaway CA, von Eschenbach AC, Bucana CD, Fidler IJ. Correlation of metastasis-related gene expression with metastatic potential in human prostate carcinoma cells implanted in nude mice using an in situ messenger RNA hybridization technique. Am J Pathol 1997;150(5):1571-1582.
15. Huang S, Robinson JB, Deguzman A, Bucana CD, Fidler IJ. 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 [In Process Citation]. Cancer Res 2000;60(19):5334-5339.
16. Huang S, DeGuzman A, Bucana CD, Fidler IJ. Nuclear factor-kappaB activity correlates with growth, angiogenesis, and metastasis of human melanoma cells in nude mice [In Process Citation]. Clin Cancer Res 2000;6(6):2573-2581.
17. Lin A. Activation of the JNK signaling pathway: Breaking the brake on apoptosis. Bioessays 2003;25(1):17-24.
18. Deng Y, Ren X, Yang L, Lin Y, Wu X. A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell 2003;115(1):61-70.
19. Nakshatri H, Rice SE, Bhat-Nakshatri P. Antitumor agent parthenolide reverses resistance of breast cancer cells to tumor necrosis factor-related apoptosis-inducing ligand through sustained activation of c-Jun N-terminal kinase. Oncogene 2004;23(44):7330-7344.
20. Herr I, Wilhelm D, Meyer E, Jeremias I, Angel P, Debatin KM. JNK/SAPK activity contributes to TRAIL-induced apoptosis. Cell Death Differ 1999;6(2):130-135.
21. De Smaele E, Zazzeroni F, Papa S, Nguyen DU, Jin R, Jones J, Cong R, Franzoso G. Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 2001;414(6861):308-313.
22. Franzoso G, Zazzeroni F, Papa S. JNK: A killer on a transcriptional leash. Cell Death Differ 2003;10(1):13-15.
23. Johnson ES, Kadam NP, Hylands DM, Hylands PJ. Efficacy of feverfew as prophylactic treatment of migraine. Br Med J (Clin Res Ed) 1985;291(6495):569- 573.
24. Bork PM, Schmitz ML, Kuhnt M, Escher C, Heinrich M. Sesquiterpene lactone containing Mexican Indian medicinal plants and pure sesquiterpene lactones as potent inhibitors of transcription factor NF-kappaB. FEBS Lett 1997;402(1):85-90.
25. Hehner SP, Heinrich M, Bork PM, Vogt M, Ratter F, Lehmann V, Schulze-Osthoff K, Droge W, Schmitz ML. Sesquiterpene lactones specifically inhibit activation of NF-kappa B by preventing the degradation of I kappa B-alpha and I kappa B-beta. J Biol Chem 1998;273(3):1288-1297.
26. Wen J, You KR, Lee SY, Song CH, Kim DG. Oxidative stress-mediated apoptosis. The anticancer effect of the sesquiterpene lactone parthenolide. J Biol Chem 2002;277(41):38954-38964.
27. Nozaki S, Sledge GW Jr., Nakshatri H. Repression of GADD153/CHOP by NF-kappaB: A possible cellular defense against endoplasmic reticulum stress-induced cell death. Oncogene 2001;20(17):2178-2185.
28. Patel NM, Nozaki S, Shortle NH, Bhat-Nakshatri P, Newton TR, Rice S, Gelfanov V, Boswell SH, Goulet RJ Jr., Sledge GW Jr., Nakshatri H. Paclitaxel sensitivity of breast cancer cells with constitutively active NF-kappaB is enhanced by IkappaBalpha super-repressor and parthenolide. Oncogene 2000;19(36):4159-4169.
29. Fujioka S, Sclabas GM, Schmidt C, Frederick WA, Dong QG, Abbruzzese JL, Evans DB, Baker C, Chiao PJ. Function of nuclear factor kappaB in pancreatic cancer metastasis. Clin Cancer Res 2003;9(1):346-354.
30. Lu T, Sathe SS, Swiatkowski SM, Hampole CV, Stark GR. Secretion of cytokines and growth factors as a general cause of constitutive NFkappaB activation in cancer. Oncogene 2004;23(12):2138-2145.
31. McNulty SE, Tohidian NB, Meyskens FL Jr. ReIA, p50 and inhibitor of kappa B alpha are elevated in human metastatic melanoma cells and respond aberrantly to ultraviolet light B. Pigment Cell Res 2001;14(6):456-465.
32. Wu JT, Kral JG. The NF-kappaB/IkappaB signaling system: A molecular target in breast cancer therapy. J Surg Res 2005;123(1):158-169.
33. Wolf JS, Chen Z, Dong G, Sunwoo JB, Bancroft CC, Capo DE, Yeh NT, Mukaida N, Van Waes C. IL (interleukin)-1alpha promotes nuclear factor-kappaB and AP-1-induced IL-8 expression, cell survival, and proliferation in head and neck squamous cell carcinomas. Clin Cancer Res 2001;7(6):1812-1820.
34. Yoshida S, Ono M, Shono T, Izumi H, Ishibashi T, Suzuki H, Kuwano M. Involvement of interleukin-8, vascular endothelial growth factor, and basic fibroblast growth factor in tumor necrosis factor alpha-dependent angiogenesis. Mol Cell Biol 1997;17(7):4015-4023.
35. Sweeney CJ, Miller KD, Sissons SE, Nozaki S, Heilman DK, Shen J, Sledge GW Jr. The antiangiogenic property of docetaxel is synergistic with a recombinant humanized monoclonal antibody against vascular endothelial growth factor or 2-methoxyestradiol but antagonized by endothelial growth factors. Cancer Res 2001;61(8):3369-3372.
36. Bhat-Nakshatri P, Newton TR, Goulet R Jr., Nakshatri H. NF-kappaB activation and interleukin 6 production in fibroblasts by estrogen receptor-negative breast cancer cell-derived interleukin 1alpha. Proc Natl Acad Sci USA 1998;95(12):6971-6976.
37. DeGrado TR, Baldwin SW, Wang S, Orr MD, Liao RP, Friedman HS, Reiman R, Price DT, Coleman RE. Synthesis and evaluation of (18)F-labeled choline analogs as oncologic PET tracers. J Nucl Med 2001;42(12):1805-1814.
38. Murray PG, Flavell JR, Baumforth KR, Toomey SM, Lowe D, Crocker J, Ambinder RF, Young LS. Expression of the tumour necrosis factor receptor-associated factors 1 and 2 in Hodgkin's disease. J Pathol 2001;194(2):158-164.
39. Zhang S, Lin ZN, Yang CF, Shi X, Ong CN, Shen HM. Suppressed NF-kappaB and sustained JNK activation contribute to the sensitization effect of parthenolide to TNF-alpha-induced apoptosis in human cancer cells. Carcinogenesis 2004;25(11):2191-2199.
40. Eliseev RA, ZuscikMJ, Schwarz EM, O'Keefe RJ, Drissi H, Rosier RN. Increased radiation-induced apoptosis of Saos2 cells via inhibition of NFkappaB: A role for c-Jun N-terminal kinase. J Cell Biochem 2005;96(6):1262-1273.
41. Zerbini LF, Libermann TA. Life and death in cancer. GADD45 alpha and gamma are critical regulators of NF-kappaB mediated escape from programmed cell death. Cell Cycle 2005;4(1):18-20.
42. Garcia-Pineres AJ, Lindenmeyer MT, Merfort I. Role of cysteine residues of p65/NF-kappaB on the inhibition by the sesquiterpene lactone parthenolide and N-ethyl maleimide, and on its transactivating potential. Life Sci 2004;75(7):841-856.
43. Altuwaijri S, Lin HK, Chuang KH, Lin WJ, Yeh S, Hanchett LA, Rahman MM, Kang HY, Tsai MY, Zhang Y, Yang L, Chang C. Interruption of nuclear factor kappaB signaling by the androgen receptor facilitates 12-O- tetradecanoylphorbolacetate-induced apoptosis in androgen-sensitive prostate cancer LNCaP cells. Cancer Res 2003;63(21):7106-7112.
44. Zapata JM, Krajewska M, Morse HC, 3rd, Choi Y, Reed JC. TNF receptor-associated factor (TRAF) domain and Bcl-2 cooperate to induce small B cell lymphoma/chronic lymphocytic leukemia in transgenic mice. Proc Natl Acad Sci USA 2004;101(47):16600-16605.
45. Sweeney CJ, Mehrotra S, Sadaria MR, Kumar S, Shortle NH, Roman Y, Sheridan C, Campbell RA, Murry DJ, Badve S, Nakshatri H. The sesquiterpene lactone parthenolide in combination with docetaxel reduces metastasis and improves survival in a xenograft model of breast cancer. Mol Cancer Ther 2005;4(6):1004-1012.
46. Cheng D, Xiao JJ, Cheng H, Liu H, Covey JM, Chan KK. Analytical method development and pharmacokinetics studies with parthenolide (NSC 157035) and a water-soluble analog (NSC 734325). Proc Am Assoc Canc Res 2005;46:4184 (abstr).
47. Ghosheh OA, Dwoskin LP, Miller DK, Crooks PA. Accumulation of nicotine and its metabolites in rat brain after intermittent or continuous peripheral administration of [2′-(14)C]nicotine. Drug Metab Dispos 2001;29(5):645-651.
48. Ghosheh O, Dwoskin LP, Li WK, Crooks PA. Residence times and half-lives of nicotine metabolites in rat brain after acute peripheral administration of [2′-(14)C]nicotine. Drug Metab Dispos 1999;27(12):1448-1455.
49. Abeyama K, Eng W, Jester JV, Vink AA, Edelbaum D, Cockerell CJ, Bergstresser PR, Takashima A. A role for NF-kappaB-dependent gene transactivation in sunburn. J Clin Invest 2000;105(12):1751-1759.
50. Dinney CP, Bielenberg DR, Perrotte P, Reich R, Eve BY, Bucana CD, Fidler IJ. Inhibition of basic fibroblast growth factor expression, angiogenesis, and growth of human bladder carcinoma in mice by systemic Interferon- alpha administration. Cancer Res 1998;58(4):808-814.
51. Han S, Yoon K, Lee K, Kim K, Jang H, Lee NK, Hwang K, Young Lee S. TNF-related weak inducer of apoptosis receptor, a TNF receptor superfamily member, activates NF-kappa B through TNF receptor-associated factors. Biochem Biophys Res Commun 2003;305(4):789-796.
52. Wiley SR, Cassiano L, Lofton T, Davis-Smith T, Winkles JA, Lindner V, Liu H, Daniel TO, Smith CA, Fanslow WC. A novel TNF receptor family member binds TWEAK and is implicated in angiogenesis. Immunity 2001;15(5):837-846.
53. Miglietta A, Bozzo F, Gabriel L, Bocca C. Microtubule-interfering activity of parthenolide. Chem Biol Interact 2004;149(2-3):165-173.