α-methylene-γ-lactones as a novel class of anti-leukemic agents

Anti-Cancer Agents in Medicinal Chemistry

Volumn 14, Issue 5, 2014, Pages 688-694

  Gach, Katarzyna ^a   Janecka, Anna ^a  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

Author keywords

Alkylating agents; Apoptosis; Leukemia stem cells; Leukemia treatment; Sesquiterpene lactones; methylene lactones

Indexed keywords

ACETYL NEOBRITANNILACTONE B; ALANTOLACTONE; ALPHA METHYLENE GAMMA LACTONE; ANTILEUKEMIC AGENT; ARGLABIN; ARUCANOLIDE; COSTUNOLIDE; CYNAROPICRIN; DIACETYL DENTATIN A; EUPALININ A; HELENALIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INEUPATOROLIDE A; LACTONE DERIVATIVE; MICHELIOLIDE; MITOGEN ACTIVATED PROTEIN KINASE; N,N DIMETHYLAMINOPARTHENOLIDE; NEOBRITANNILACTONE B; PARTHENOLIDE; SANTAMARINE; SESQUITERPENE LACTONE DERIVATIVE; TELOMERASE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; LACTONE; PLANT EXTRACT; SESQUITERPENE;

ALLAGOPAPPUS VISCOSISSIMUS; APOPTOSIS; ARTEMISIA GLABELLA; CALEA URTICIFOLIA; CANCER STEM CELL; CLINICAL TRIAL (TOPIC); CYATHOCLINE PURPUREA; DRUG MECHANISM; EUPATORIUM CHINENSE; GONOSPERMUM; HUMAN; INTRACELLULAR SIGNALING; INULA BRITANNICA; INULA RACEMOSA; LEUKEMIA; MAGNOLIA SIEBOLDII; MEDICINAL PLANT; NONHUMAN; PSILOSTROPHE COOPERI; REVIEW; SAUSSUREA LAPPA; TANACETUM PARTHENIUM; ANIMAL; CHEMISTRY; DRUG EFFECTS; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; HUMANS; LACTONES; LEUKEMIA; NEOPLASTIC STEM CELLS; PLANT EXTRACTS; SESQUITERPENES; SESQUITERPENES, GUAIANE;

EID: 84904463551     PISSN: 18715206     EISSN: 18755992     Source Type: Journal    
DOI: 10.2174/1871520614666140313095010     Document Type: Review

References (58)

1. Brown, C.M.; Larsen, S.R.; Iland, H.J.; Joshua, D.E.; Gibson, J. Leukaemias into the 21st century: part 1: the acute leukaemias. Intern. Med. J., 2012, 42(11), 1179-1186.
2. Gibson, J.; Iland, H.J.; Larsen, S.R.; Brown, C.M.; Joshua D.E. Leukaemias into the 21st century-part 2: the chronic leukaemias. Intern. Med. J., 2013, 43(5), 484-494.
3. Gilliland, D.G.; Jordan, C.T.; Felix, C.A. The molecular basis of leukemia. Hematology Am. Soc. Hematol. Educ. Program, 2004, 80-97.
4. Jordan, C.T. The leukemic stem cell. Best. Pract. Res. Clin. Haematol., 2007, 20(1), 13-18.
5. Bonnet D, Dick JE. Human acute myeloid leukemiais organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med, 1997, 3(7), 730-737.
6. Snauwaert, S.; Vandekerckhove, B.; Kerre, T. Can immunotherapy specifically target acute myeloid leukemic stem cells? Oncoimmunology, 2013, 2(2), e22943.
7. Guzman, M.L.; Li, X.; Corbett, C.A.; Rossi, R.M.; Bushnell, T.; Liesveld J.L.; Hebert, J.; Young, F.; Jordan, C.T. Rapid and selective death of leukemia stem and progenitor cells induced by the compound 4-benzyl, 2-methyl, 1,2,4-thiadiazolidine, 3,5 dione (TDZD-8). Blood, 2007, 110(13), 4436-4444.
8. Van Rhenen, A.; Feller, N.; Kelder, A.; Westra, A.H.; Rombouts E.; Zweegman, S.; Van der Pol, M.A.; Waisfisz, Q.; Ossenkoppele, G.J.; Schuurhuis, G.J. High stem cell frequency in acute myeloid leukemia at diagnosis predicts high minimal residual disease and poor survival. Clin. Cancer Res., 2005, 11(18), 6520-6527.
9. Killmann, S.A. Acute leukaemia: development, remission/relapse pattern, relationship between normal and leukaemic haemopoiesis, and the 'sleeper-to-feeder' stem cell hypothesis. Baillieres Clin. Haematol., 1991, 4(3), 577-598.
10. Kantarjian, H.M.; Estey, E.H.; Keating, M.A. New chemotherapeutic agents in acute myeloid leukemia. Leukemia., 1996, 10(Suppl 1), S4-6.
11. Leopold, L.H.; Willemze, R. The treatment of acute myeloid leukemia in first relapse: a comprehensive review of the literature. Leuk. Lymphoma., 2002, 43(9), 1715-1727.
12. Guzman, M.L.; Rossi, R.M.; Karnischky, L.; Li, X.; Peterson, D.R.; Howard, D.S.; Jordan C.T. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood, 2005, 105(11), 4163-4169.
13. Guzman, M.L.; Swiderski, C.F.; Howard, D.S.; Grimes, B.A.; Rossi, R.M.; Szilvassy, S.J.; Jordan, C.T. Preferential induction of apoptosis for primary human leukemic stem cells. Proc. Natl. Acad. Sci. USA, 2002, 99(25), 16220-16225.
14. She, M.; Chen, X. Targeting Signal Pathways Active in Leukemic Stem Cells to Overcome Drug Resistance. Cancer Stem Cells Theories and Practice, Stanley Shostak (Ed.), ISBN: 978-953-307-225-8, InTech, 2011. Available at: http://www.intechopen.com/books/cancer-stem-cells-theories-andpractice/targeting-signal-pathwaysactive-in-leukemic-stem-cells-to-overcome-drug-resistance.
15. Jordan, C.T.; Upchurch, D.; Szilvassy, S.J.; Guzman, M.L.; Howard, D.S.; Pettigrew, A.L.; Meyerrose, T.; Rossi, R.; Grimem, B.; Rizzieri, D.A.; Luger, S.M.; Phillips, G.L. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia, 2000, 14(10), 1777-1784.
16. Guzman, M.L.; Rossi, R.M.; Neelakantan, S.; Li, X.; Corbett, C.A.; Hassane, D.C.; Becker, M.W.; Bennett, J.M.; Sullivan, E.; Lachowicz, J.L.; Vaughan, A.; Sweeney, C.J.; Matthews, W.; Carroll, M.; Liesveld, J.L.; Crooks, P.A.; Jordan, C.T. An orally bioavailable parthenolide analog selectively eradicates acute myelogenous leukemia stem and progenitor cells. Blood, 2007; 110(13): 4427-4435.
17. Ravandi, F.; Estrov, Z.; Eradication of leukemia stem cells as a new goal of therapy in leukemia. Clin. Cancer Res., 2006, 12(2), 340-344.
18. Costello, R.T.; Mallet, F.; Gaugler, B.; Sainty, D.; Arnoulet, C.; Gastaut, J.A.; Olive D. Human acute myeloid leukemia CD34+/ CD38-progenitor cells have decreased sensitivity to chemotherapy and Fas-induced apoptosis, reduced immunogenicity, and impaired dendritic cell transformation capacities. Cancer Res., 2000, 60(16), 4403-4411.
19. Kordes, U.; Krappmann, D.; Heissmeyer, V.; Ludwig, W.D.; Scheidereit, C. Transcription factor NF-kappaB is constitutively activated in acute lymphoblastic leukemia cells. Leukemia, 2000, 14(3), 399-402.
20. Guzman, M.L.; Neering, S.J.; Upchurch, D.; Grimes, B.; Howard, D.S.; Rizzieri, D.A.; Luger, S.M.; Jordan, C.T. Nuclear factorkappaB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood, 2001, 98(8), 2301-2307.
21. Merfort, I. Perspectives on sesquiterpene lactones in inflammation and cancer. Curr. Drug Targets, 2011, 12(11), 1560-1573.
22. Kreuger, M.R.; Grootjans, S.; Biavatti, M.W.; Vandenabeele, P.; D'Herde, K. Sesquiterpene lactones as drugs with multiple targets in cancer treatment: focus on parthenolide. Anticancer Drugs, 2012, 23(9), 883-896.
23. Zhang, S.; Won, Y.K.; Ong, C.N.; Shen, H.M. Anti-cancer potential of sesquiterpene lactones: bioactivity and molecular mechanisms. Curr. Med. Chem. Anticancer Agents, 2005, 5(3), 239-249.
24. Pati, H.N.; Das, U.; Sharma, R.K.; Dimmock, J.R. Cytotoxic thiol alkylators. Mini. Rev. Med. Chem., 2007, 7(2), 131-139.
25. Lee, K.H.; Hall, I.H.; Mar, E.C.; Starnes, C.O.; ElGebaly, S.A.; Waddell, T.G.; Hadgraft, R.I.; Ruffner, C.G.; Weidner, I. Sesquiterpene antitumor agents: inhibitors of cellular metabolism. Science, 1977, 196(4289), 533-536.
26. Zhang, S.; Ong, C.N.; Shen, H.M. Critical roles of intracellular thiols and calcium in parthenolide-induced apoptosis in human colorectal cancer cells. Cancer Lett., 2004, 208(2), 143-153.
27. Janecka, A.; Wyrebska, A.; Gach, K.; Fichna, J.; Janecki, T. Natural and synthetic α-methylenelactones and α-methylenelactams with anticancer potential. Drug Discov. Today, 2012, 17(11-12), 561-572.
28. Fulda, S.; Debatin, K.M. Modulation of apoptosis signaling for cancer therapy. Arch. Immunol. Ther. Exp. (Warsz), 2006, 54(3), 173-175.
29. Kaufmann, S.H., Earnshaw, W.C. Induction of apoptosis by cancer chemotherapy. Exp Cell Res., 2000, 256(1), 42-49.
30. Zunino, S.J.; Ducore, J.M.; Storms, D.H. Parthenolide induces significant apoptosis and production of reactive oxygen species in high-risk pre-B leukemia cells. Cancer Lett., 2007, 254(1), 119-127.
31. Steele, A.J.; Jones, D.T.; Ganeshaguru, K.; Duke, V.M.; Yogashangary, B.C.; North, J.M.; Lowdell, M.W.; Kottaridis, P.D.; Mehta, A.B.; Prentice, A.G.; Hoffbrand, A.V.; Wickremasinghe, R.G. The sesquiterpene lactone parthenolide induces selective apoptosis of B-chronic lymphocytic leukemia cells in vitro. Leukemia, 2006, 20(6), 1073-1079.
32. Lee, M.G.; Lee, K.T.; Chi, S.G.; Park, J.H. Costunolide induces apoptosis by ROS-mediated mitochondrial permeability transition and cytochrome C release. Biol. Pharm. Bull., 2001, 24(3), 303-306.
33. Dirsch, V.M.; Stuppner, H.; Vollmar, A.M. Helenalin triggers a CD95 death receptor-independent apoptosis that is not affected by overexpression of Bcl-x(L) or Bcl-2. Cancer Res., 2001, 61(15), 5817-5823.
34. Nakagawa, Y.; Iinuma, M.; Matsuura, N.; Yi, K.; Naoi, M.; Nakayama, T.; Nozawa, Y.; Akao, Y. A potent apoptosis-inducing activity of a sesquiterpene lactone, arucanolide, in HL60 cells: a crucial role of apoptosis-inducing factor. J. Pharmacol. Sci., 2005, 97(2), 242-252.
35. Kanno, S.; Kitajima, Y.; Kakuta, M.; Osanai, Y.; Kurauchi, K.; Ujibe, M.; Ishikawa, M. Costunolide-induced apoptosis is caused by receptor-mediated pathway and inhibition of telomerase activity in NALM-6 cells. Biol. Pharm. Bull., 2008, 31(5), 1024-1028.
36. Colangelo, D.; Osella, D. Telomerase inhibition and cancer: might platinum based drugs have a future as anti-telomerase pharmacological approach? Curr. Med. Chem., 2005, 12(26), 3091-3102.
37. Kim, N.W.; Piatyszek, M.A.; Prowse, K.R.; Harley, C.B.; West, M.D.; Ho, P.L.; Coviello, G.M.; Wright, W.E.; Weinrich, S.L.; Shay, J.W. Specific association of human telomerase activity with immortal cells and cancer. Science, 1994, 266(5193), 2011-2015.
38. Raman, M; Chen, W.; Cobb, M.H. Differential regulation and properties of MAPKs. Oncogene., 2007, 26(22), 3100-3112.
39. Choi, J.H.; Lee, K.T. Costunolide-induced apoptosis in human leukemia cells: involvement of c-jun N-terminal kinase activation. Biol. Pharm. Bull., 2009, 32(10), 1803-1808.
40. Cho, J.Y.; Kim A.R.; Jung, J.H.; Chun T.; Rhee M.H.; Yoo E.S. Cytotoxic and pro-apoptotic activities of cynaropicrin, a sesquiterpene lactone, on the viability of leukocyte cancer cell lines. Eur. J. Pharmacol., 2004, 492(2-3), 85-94.
41. Rungeler, P.; Castro, V.; Mora, G.; Goren, N.; Vichnewski, W.; Pahl, H.L.; Merfort, I.; Schmidt, T.J. Inhibition of transcription factor NF-kappaB by sesquiterpene lactones: a proposed molecular mechanism of action. Bioorg. Med. Chem., 1999, 7(11), 2343-2352.
42. Karin, M.; Lin, A. NF-kappaB at the crossroads of life and death. Nat. Immunol., 2002, 3(3), 221-227.
43. Garg, A.; Aggarwal, B.B. Nuclear transcription factor-kappaB as a target for cancer drug development. Leukemia, 2002, 16(6), 1053-1068.
44. Wei, W.; Huang, H.; Zhao, S.; Liu, W.; Liu, C.X.; Chen, L.; Li, J.M.; Wu, Y.L.; Yan, H. Alantolactone induces apoptosis in chronic myelogenous leukemia sensitive or resistant to imatinib through NF-κB inhibition and Bcr/Abl protein deletion. Apoptosis, 2013,[Epub ahead of print].
45. Skalska, J.; Brookes, P.S.; Nadtochiy, S.M.; Hilchey, S.P.; Jordan, C.T.; Guzman, M.L.; Maggirwar, S.B.; Briehl, M.M.; Bernstein, S.H. Modulation of cell surface protein free thiols: a potential novel mechanism of action of the sesquiterpene lactone parthenolide. PLoS One. 2009, 4(12), e8115.
46. Neelakantan, S.; Nasim, S.; Guzman, M.L.; Jordan, C.T.; Crooks, P.A. Aminoparthenolides as novel anti-leukemic agents: Discovery of the NF-kappaB inhibitor, DMAPT (LC-1). Bioorg. Med. Chem. Lett., 2009, 19(15), 4346-4349.
47. Zhang, Q.; Lu, Y.; Ding, Y.; Zhai, J.; Ji, Q.; Ma, W.; Yang, M.; Fan, H.; Long, J.; Tong, Z.; Shi, Y.; Jia, Y.; Han, B.; Zhang, W.; Qiu, C.; Ma, X.; Li, Q.; Shi, Q.; Zhang, H.; Li, D.; Zhang, J.; Lin, J.; Li, LY.; Gao, Y.; Chen, Y. Guaianolide sesquiterpene lactones, a source to discover agents that selectively inhibit acute myelogenous leukemia stem and progenitor cells. J. Med. Chem., 2012, 55(20), 8757-8769.
48. Kevin, P. New agents for the treatment of leukemia: discovery of DMAPT (LC-1). Drug Disc. Today, 2010, 15, 322.
49. Rubnitz, J.E.; Onciu, M.; Pounds, S.; Shurtleff, S.; Cao, X.; Raimondi, S.C.; Behm, F.G.; Campana, D.; Razzouk, B.I.; Ribeiro, R.C.; Downing, J.R.; Pui, C.H. Acute mixed lineage leukemia in children: the experience of St Jude Children's Research Hospital. Blood, 2009, 113(21), 5083-5089.
50. Ma, W.W.; Shi, Q.Q.; Ding, Y.H.; Long, J.; Zhang, Q.; Chen, Y. Synthesis of Micheliolide Derivatives and Their Activities against AML Progenitor Cells. Molecules, 2013, 18(5), 5980-5992.
51. Itoh, T.; Ito, Y.; Ohguchi, K.; Ohyama, M.; Iinuma, M.; Otsuki, M.; Nozawa, Y.; Akao, Y. Eupalinin A isolated from Eupatorium chinense L. Induces Autophagocytosis in Human Leukemia HL60 Cells. Bioorg. Med. Chem., 2008, 16(2), 721-731.
52. Itoh, T.; Ohguchi, K.; Nozawa, Y.; Akao, Y. Intracellular glutathione regulates sesquiterpene lactone-induced conversion of autophagy to apoptosis in human leukemia HL60 cells. Anticancer Res., 2009, 29(4), 1449-1157.
53. Bujnicki, T.; Wilczek, C.; Schomburg, C.; Feldmann, F.; Schlenke, P.; Muller-Tidow, C.; Schmidt, T.J.; Klempnauer, K.H. Inhibition of Myb-dependent gene expression by the sesquiterpene lactone mexicanin-I. Leukemia, 2012, 26(4), 615-622.
54. Zhangabylov, NS.; Yu Dederer, L.; Gorbacheva, L.B.; Vasil'eva, S.V.; Terekhov, A.S.; Adekenov S.M. Sesquiterpene lactone arglabin influences DNA synthesis in P388 leukemia cells in vivo. Pharm. Chem. J., 2004, 38(12), 651-653.
55. Bai, N.; Lai, C.S.; He, K.; Zhou, Z.; Zhang, L.; Quan, Z.; Zhu, N.; Zheng, Q.Y.; Pan, M.H.; Ho, C.T. Sesquiterpene lactones from Inula britannica and their cytotoxic and apoptotic effects on human cancer cell lines. J. Nat. Prod., 2006, 69(4), 531-535.
56. Ma, G.; Chong, L.; Li, Z.; Cheung, A.H.; Tattersall, M.H. Anticancer activities of sesquiterpene lactones from Cyathocline purpurea in vitro. Cancer Chemother. Pharmacol., 2009, 64(1), 143-152.
57. Rivero, A.; Quintana, J.; Eiroa, J.L.; Lopez, M.; Triana, J.; Bermejo, J.; Estevez, F. Potent induction of apoptosis by germacranolide sesquiterpene lactones on human myeloid leukemia cells. Eur. J. Pharmacol., 2003, 482(1-3), 77-84.
58. Triana, J.; Eiroa, J.L.; Ortega, J.J.; Leon, F.; Brouard, I.; Torres, F.; Quintana, J.; Estevez, F.; Bermejo, J. Sesquiterpene lactones from Gonospermum gomerae and G. fruticosum and their cytotoxic activities. Nat. Prod., 2008, 71(12), 2015-220.