Parthenolide reduces the frequency of ABCB5-positive cells and clonogenic capacity of melanoma cells from anchorage independent melanospheres

Cancer Biology and Therapy

Volumn 14, Issue 2, 2013, Pages 135-145

  Czyz, Malgorzata ^a   Koprowska, Kamila ^a   Sztiller Sikorska, Malgorzata ^a  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

Author keywords

ABCB5; Anticancer drug; Cancer immunophenotype; Cancer stem cell; Melanoma; Melanosphere; Parthenolide; Penetration capacity; Self renewing potential

Indexed keywords

MULTIDRUG RESISTANCE PROTEIN 5; PARTHENOLIDE;

ARTICLE; BLOOD VESSEL; CELL ANCHORAGE; CELL POPULATION; CELL RENEWAL; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CLONOGENESIS; DRUG EFFECT; DRUG PENETRATION; IMMUNOPHENOTYPING; MELANOMA; MELANOMA CELL; PROTEIN EXPRESSION;

ABCB5; ANTICANCER DRUG; CANCER IMMUNOPHENOTYPE; CANCER STEM CELL; MELANOMA; MELANOSPHERE; PARTHENOLIDE; PENETRATION CAPACITY; SELF-RENEWING POTENTIAL;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; MELANOMA; NEOPLASTIC STEM CELLS; P-GLYCOPROTEIN; SESQUITERPENES; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

EID: 84873426890     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.22952     Document Type: Article

References (53)

1. Schatton T, Frank MH. Cancer stem cells and human malignant melanoma. Pigment Cell Melanoma Res 2008; 21:39-55; PMID:18353142; http://dx.doi.org/10. 1111/j.1755-148X.2007.00427.x.
2. Frank NY, Schatton T, Frank MH. The therapeutic promise of the cancer stem cell concept. J Clin Invest 2010; 120:41-50; PMID:20051635; http://dx.doi.org/10.1172/JCI41004.
3. Girouard SD, Murphy GF. Melanoma stem cells: not rare, but well done. Lab Invest 2011; 91:647-64; PMID:21445060; http://dx.doi.org/10.1038/labinvest. 2011.50.
4. Eramo A, Haas TL, De Maria R. Lung cancer stem cells: tools and targets to fight lung cancer. Oncogene 2010; 29:4625-35; PMID:20531299; http://dx.doi.org/10.1038/onc.2010.207.
5. Takehara M, Hoshino T, Namba T, Yamakawa N, Mizushima T. Acetaminophen-induced differentiation of human breast cancer stem cells and inhibition of tumor xenograft growth in mice. Biochem Pharmacol 2011; 81:1124-35; PMID:21371442; http://dx.doi.org/10.1016/j.bcp.2011.02.012.
6. Schmidt P, Kopecky C, Hombach A, Zigrino P, Mauch C, Abken H. Eradication of melanomas by targeted elimination of a minor subset of tumor cells. Proc Natl Acad Sci U S A 2011; 108:2474-9; PMID:21282657; http://dx.doi.org/10.1073/ pnas.1009069108.
7. Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS, Johnson TM, et al. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 2010; 18:510-23; PMID:21075313; http://dx.doi.org/10.1016/j.ccr.2010.10.012.
8. Hoek KS, Goding CR. Cancer stem cells versus phenotype-switching in melanoma. Pigment Cell Melanoma Res 2010; 23:746-59; PMID:20726948; http://dx.doi.org/10.1111/j.1755-148X.2010.00757.x.
9. Roesch A, Fukunaga-Kalabis M, Schmidt EC, Zabierowski SE, Brafford PA, Vultur A, et al. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 2010; 141:583-94; PMID:20478252; http://dx.doi.org/10.1016/j.cell.2010.04.020.
10. Abel EV, Aplin AE. Finding the root of the problem: the quest to identify melanoma stem cells. Front Biosci (Schol Ed) 2011; 3:937-45; PMID:21622243; http://dx.doi.org/10.2741/198.
11. Fukunaga-Kalabis M, Roesch A, Herlyn M. From cancer stem cells to tumor maintenance in melanoma. J Invest Dermatol 2011; 131:1600-4; PMID:21654838; http://dx.doi.org/10.1038/jid.2011.159.
12. Ghislin S, Deshayes F, Lauriol J, Middendorp S, Martins I, Al-Daccak R, et al. Plasticity of melanoma cells induced by neural cell crest conditions and threedimensional growth. Melanoma Res 2012; 22:184-94; PMID:22454190; http://dx.doi.org/10.1097/CMR.0b013e328351e7c4.
13. Sztiller-Sikorska M, Koprowska K, Jakubowska J, Zalesna I, Stasiak M, Duechler M, et al. Sphere formation and self-renewal capacity of melanoma cells is affected by the microenvironment. Melanoma Res 2012; 22:215-24; PMID:22495670; http://dx.doi.org/10.1097/CMR.0b013e3283531317.
14. 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; 277:38954-64; PMID:12151389; http://dx.doi.org/10.1074/jbc. M203842200.
15. Zunino SJ, Ducore JM, Storms DH. Parthenolide induces significant apoptosis and production of reactive oxygen species in high-risk pre-B leukemia cells. Cancer Lett 2007; 254:119-27; PMID:17470383; http://dx.doi.org/10.1016/j. canlet.2007.03.002.
16. Duechler M, Stańczyk M, Czyz M, Stepnik M. Potentiation of arsenic trioxide cytotoxicity by Parthenolide and buthionine sulfoximine in murine and human leukemic cells. Cancer Chemother Pharmacol 2008; 61:727-37; PMID:17594095; http://dx.doi.org/10.1007/s00280-007-0527-3.
17. Suvannasankha A, Crean CD, Shanmugam R, Farag SS, Abonour R, Boswell HS, et al. Antimyeloma effects of a sesquiterpene lactone parthenolide. Clin Cancer Res 2008; 14:1814-22; PMID:18347184; http://dx.doi.org/10.1158/1078-0432.CCR-07- 1359.
18. Dai Y, Guzman ML, Chen S, Wang L, Yeung SK, Pei XY, et al. The NF (Nuclear factor)-κB inhibitor parthenolide interacts with histone deacetylase inhibitors to induce MKK7/JNK1-dependent apoptosis in human acute myeloid leukaemia cells. Br J Haematol 2010; 151:70-83; PMID:20701602; http://dx.doi.org/10.1111/j.1365-2141.2010.08319.x.
19. Czyz M, Lesiak-Mieczkowska K, Koprowska K, Szulawska-Mroczek A, Wozniak M. Cell contextdependent activities of parthenolide in primary and metastatic melanoma cells. Br J Pharmacol 2010; 160:1144-57; PMID:20590608; http://dx.doi.org/10.1111/j.1476-5381.2010.00749.x.
20. Lesiak K, Koprowska K, Zalesna I, Nejc D, Düchler M, Czyz M. Parthenolide, a sesquiterpene lactone from the medical herb feverfew, shows anticancer activity against human melanoma cells in vitro. Melanoma Res 2010; 20:21-34; PMID:19949351; http://dx.doi.org/10.1097/CMR.0b013e328333bbe4.
21. Guzman ML, Rossi RM, Karnischky L, Li X, Peterson DR, Howard DS, et al. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood 2005; 105:4163-9; PMID:15687234; http://dx.doi.org/10.1182/blood-2004-10-4135.
22. Gunn EJ, Williams JT, Huynh DT, Iannotti MJ, Han C, Barrios FJ, et al. The natural products parthenolide and andrographolide exhibit anti-cancer stem cell activity in multiple myeloma. Leuk Lymphoma 2011; 52:1085-97; PMID:21417826; http://dx.doi.org/10.3 109/10428194.2011.555891.
23. Liu Y, Lu WL, Guo J, Du J, Li T, Wu JW, et al. A potential target associated with both cancer and cancer stem cells: a combination therapy for eradication of breast cancer using vinorelbine stealthy liposomes plus parthenolide stealthy liposomes. J Control Release 2008; 129:18-25; PMID:18466993; http://dx.doi.org/10.1016/j.jconrel.2008.03.022.
24. Zhou J, Zhang H, Gu P, Bai J, Margolick JB, Zhang Y. NF-kappaB pathway inhibitors preferentially inhibit breast cancer stem-like cells. Breast Cancer Res Treat 2008; 111:419-27; PMID:17965935; http://dx.doi.org/10.1007/s10549-007- 9798-y.
25. Kawasaki BT, Hurt EM, Kalathur M, Duhagon MA, Milner JA, Kim YS, et al. Effects of the sesquiterpene lactone parthenolide on prostate tumor-initiating cells: An integrated molecular profiling approach. Prostate 2009; 69:827-37; PMID:19204913; http://dx.doi.org/10.1002/pros.20931.
26. Hassane DC, Sen S, Minhajuddin M, Rossi RM, Corbett CA, Balys M, et al. Chemical genomic screening reveals synergism between parthenolide and inhibitors of the PI-3 kinase and mTOR pathways. Blood 2010; 116:5983-90; PMID:20889920; http://dx.doi.org/10.1182/blood-2010-04-278044.
27. Zuch D, Giang AH, Shapovalov Y, Schwarz E, Rosier R, O'Keefe R, et al. Targeting radioresistant osteosarcoma cells with parthenolide. J Cell Biochem 2012; 113:1282-91; PMID:22109788.
28. Thurber AE, Douglas G, Sturm EC, Zabierowski SE, Smit DJ, Ramakrishnan SN, et al. Inverse expression states of the BRN2 and MITF transcription factors in melanoma spheres and tumour xenografts regulate the NOTCH pathway. Oncogene 2011; 30:3036-48; PMID:21358674; http://dx.doi.org/10.1038/onc.2011.33.
29. Chen KG, Valencia JC, Gillet JP, Hearing VJ, Gottesman MM. Involvement of ABC transporters in melanogenesis and the development of multidrug resistance of melanoma. Pigment Cell Melanoma Res 2009; 22:740-9; PMID:19725928; http://dx.doi.org/10.1111/j.1755-148X.2009.00630.x.
30. Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, et al. Identification of cells initiating human melanomas. Nature 2008; 451:345-9; PMID:18202660; http://dx.doi.org/10.1038/nature06489.
31. Perego M, Tortoreto M, Tragni G, Mariani L, Deho P, Carbone A, et al. Heterogeneous phenotype of human melanoma cells with in vitro and in vivo features of tumor-initiating cells. J Invest Dermatol 2010; 130:1877-86; PMID:20376064; http://dx.doi.org/10.1038/jid.2010.69.
32. Keshet GI, Goldstein I, Itzhaki O, Cesarkas K, Shenhav L, Yakirevitch A, et al. MDR1 expression identifies human melanoma stem cells. Biochem Biophys Res Commun 2008; 368:930-6; PMID:18279661; http://dx.doi.org/10.1016/j.bbrc.2008. 02.022.
33. Frank NY, Margaryan A, Huang Y, Schatton T, Waaga-Gasser AM, Gasser M, et al. ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 2005; 65:4320-33; PMID:15899824; http://dx.doi.org/10. 1158/0008-5472.CAN-04-3327.
34. Maugeri-Saccà M, Vigneri P, De Maria R. Cancer stem cells and chemosensitivity. Clin Cancer Res 2011; 17:4942-7; PMID:21622723; http://dx.doi.org/10.1158/1078-0432.CCR-10-2538.
35. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci U S A 2009; 106:13820-5; PMID:19666588; http://dx.doi.org/10.1073/pnas.0905718106.
36. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007; 131:1109-23; PMID:18083101; http://dx.doi.org/10.1016/j.cell.2007.10.054.
37. Chartrain M, Riond J, Stennevin A, Vandenberghe I, Gomes B, Lamant L, et al. Melanoma chemotherapy leads to the selection of ABCB5-expressing cells. PLoS One 2012; 7:e36762; PMID:22675422; http://dx.doi.org/10.1371/journal.pone. 0036762.
38. Kim YR, Eom JI, Kim SJ, Jeung HK, Cheong JW, Kim JS, et al. Myeloperoxidase expression as a potential determinant of parthenolide-induced apoptosis in leukemia bulk and leukemia stem cells. J Pharmacol Exp Ther 2010; 335:389-400; PMID:20699435; http://dx.doi.org/10.1124/jpet.110.169367.
39. Murphy JJ, Heptinstall S, Mitchell Jr. Randomised double-blind placebo-controlled trial of feverfew in migraine prevention. Lancet 1988; 2:189-92; PMID:2899663; http://dx.doi.org/10.1016/S0140-6736(88)92289-1.
40. Curry EA 3rd, Murry DJ, Yoder C, Fife K, Armstrong V, Nakshatri H, et al. Phase I dose escalation trial of feverfew with standardized doses of parthenolide in patients with cancer. Invest New Drugs 2004; 22:299-305; PMID:15122077; http://dx.doi.org/10.1023/B:DRUG.0000026256.38560.be.
41. Hehner SP, Heinrich M, Bork PM, Vogt M, Ratter F, Lehmann V, et al. 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; 273:1288-97; PMID:9430659; http://dx.doi.org/10.1074/jbc.273.3.1288.
42. Kwok BH, Koh B, Ndubuisi MI, Elofsson M, Crews CM. The anti-inflammatory natural product parthenolide from the medicinal herb Feverfew directly binds to and inhibits IkappaB kinase. Chem Biol 2001; 8:759-66; PMID:11514225; http://dx.doi.org/10.1016/S1074-5521(01)00049-7.
43. Carlisi D, D'Anneo A, Angileri L, Lauricella M, Emanuele S, Santulli A, et al. Parthenolide sensitizes hepatocellular carcinoma cells to TRAIL by inducing the expression of death receptors through inhibition of STAT3 activation. J Cell Physiol 2011; 226:1632-41; PMID:21413021; http://dx.doi.org/10.1002/jcp.22494.
44. Sobota R, Szwed M, Kasza A, Bugno M, Kordula T. Parthenolide inhibits activation of signal transducers and activators of transcription (STATs) induced by cytokines of the IL-6 family. Biochem Biophys Res Commun 2000; 267:329-33; PMID:10623619; http://dx.doi.org/10.1006/bbrc.1999.1948.
45. 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; 23:7330-44; PMID:15286701; http://dx.doi.org/10.1038/sj. onc.1207995.
46. Gopal YN, Chanchorn E, Van Dyke MW. Parthenolide promotes the ubiquitination of MDM2 and activates p53 cellular functions. Mol Cancer Ther 2009; 8:552-62; PMID:19276167; http://dx.doi.org/10.1158/1535-7163.MCT-08-0661.
47. Gopal YN, Arora TS, Van Dyke MW. Parthenolide specifically depletes histone deacetylase 1 protein and induces cell death through ataxia telangiectasia mutated. Chem Biol 2007; 14:813-23; PMID:17656318; http://dx.doi.org/10.1016/j.chembiol.2007.06.007.
48. Liu Z, Liu S, Xie Z, Pavlovicz RE, Wu J, Chen P, et al. Modulation of DNA methylation by a sesquiterpene lactone parthenolide. J Pharmacol Exp Ther 2009; 329:505-14; PMID:19201992; http://dx.doi.org/10.1124/jpet.108.147934.
49. Zhou J, Zhang Y. Cancer stem cells: Models, mechanisms and implications for improved treatment. Cell Cycle 2008; 7:1360-70; PMID:18418062; http://dx.doi.org/10.4161/cc.7.10.5953.
50. Lin L, Liu Y, Li H, Li PK, Fuchs J, Shibata H, et al. Targeting colon cancer stem cells using a new curcumin analogue, GO-Y030. Br J Cancer 2011; 105:212-20; PMID:21694723; http://dx.doi.org/10.1038/bjc.2011.200.
51. Skalska J, Brookes PS, Nadtochiy SM, Hilchey SP, Jordan CT, Guzman ML, et al. Modulation of cell surface protein free thiols: a potential novel mechanism of action of the sesquiterpene lactone parthenolide. PLoS One 2009; 4:e8115; PMID:19956548; http://dx.doi.org/10.1371/journal.pone.0008115.
52. García-Piñeres AJ, Castro V, Mora G, Schmidt TJ, Strunck E, Pahl HL, et al. Cysteine 38 in p65/NF-kappaB plays a crucial role in DNA binding inhibition by sesquiterpene lactones. J Biol Chem 2001; 276:39713-20; PMID:11500489; http://dx.doi.org/10.1074/jbc.M101985200.
53. Moitra K, Scally M, McGee K, Lancaster G, Gold B, Dean M. Molecular evolutionary analysis of ABCB5: the ancestral gene is a full transporter with potentially deleterious single nucleotide polymorphisms. PLoS One 2011; 6:e16318; PMID:21298007; http://dx.doi.org/10.1371/journal.pone.0016318.