Targeting the mitochondria activates two independent cell death pathways in ovarian cancer stem cells

Molecular Cancer Therapeutics

Volumn 10, Issue 8, 2011, Pages 1385-1393

  Alvero, Ayesha B ^a   Montagna, Michele K ^a   Holmberg, Jennie C ^a   Craveiro, Vinicius ^a   Brown, David ^b   Mor, Gil ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Marshall Edwards Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; BETA ACTIN; CASPASE; CYCLOOXYGENASE 1; CYCLOOXYGENASE IV; HERMES ANTIGEN; HYDROGEN PEROXIDE; ISOFLAVONE DERIVATIVE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYELOID DIFFERENTIATION FACTOR 88; NV 128; PROTEIN AMPK ALPHA1; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; S6 KINASE; SUPEROXIDE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BIOENERGY; CANCER PATIENT; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURVIVAL; CARCINOGENESIS; CELL POPULATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; OVARY CANCER; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATE; AMP-ACTIVATED PROTEIN KINASES; BCL-2-ASSOCIATED X PROTEIN; CELL DEATH; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX IV; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; ISOFLAVONES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NEOPLASMS, GLANDULAR AND EPITHELIAL; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUPEROXIDES; TOR SERINE-THREONINE KINASES;

EID: 80051600499     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-11-0023     Document Type: Article

References (41)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-49.
2. Mor G, Montagna MK, Alvero AB. Modulation of apoptosis to reverse chemoresistance. Methods Mol Biol 2008;414:1-12.
3. Fraser M, Leung B, Jahani-Asl A, Yan X, Thompson WE, Tsang BK. Chemoresistance in human ovarian cancer: the role of apoptotic regulators. Reprod Biol Endocrinol 2003;1:66.
4. Vellanki SH, Grabrucker A, Liebau S, Proepper C, Eramo A, Braun V, et al. Small-molecule XIAP inhibitors enhance gamma-irradiation-induced apoptosis in glioblastoma. Neoplasia 2009;11:743-52.
5. Vogler M, Walczak H, Stadel D, Haas TL, Genze F, Jovanovic M, et al. Small molecule XIAP inhibitors enhance TRAIL-induced apoptosis and antitumor activity in preclinical models of pancreatic carcinoma. Cancer Res 2009;69:2425-34.
6. Alvero AB, O'Malley D, Brown D, Kelly G, Garg M, Chen W, et al. Molecular mechanism of phenoxodiol-induced apoptosis in ovarian carcinoma cells. Cancer 2006;106:599-608. (Pubitemid 43157623)
7. Rutherford TOM D, Makkenchery A, Mor G. Phenoxodiol phase Ib/II study in patients with recurrent ovarian cancer that resistant to second line chemotherapy. J Soc Gynecologic Invest 2004;11:254.
8. Alvero AB, Brown D, Montagna M, Matthews M, Mor G. Phenoxodioltopotecan co-administration exhibit significant anti-tumor activity without major adverse side effects. Cancer Biol Ther 2007;6.
9. Alvero AB, Rossi P, Brown D, Leizer A, Kelly M, Rutherford T, et al. Phenoxodiol-a chemosensitizer in the midst of cancer chemoresistance. US Oncol 2008;4:39-41.
10. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006;66:9339-44.
11. Dalerba P, Cho RW, Clarke MF. Cancer stem cells: models and concepts. Annu Rev Med 2007;58:267-84. (Pubitemid 46706514)
12. Alvero AB, Chen R, Fu HH, Montagna M, Schwartz PE, Rutherford T, et al. Molecular phenotyping of human ovarian cancer stem cells unravels the mechanisms for repair and chemoresistance. Cell Cycle 2009;8:158-66.
13. Alvero AB, Fu HH, Holmberg J, Visintin I, Mor L, Marquina CC, et al. Stem-like ovarian cancer cells can serve as tumor vascular progenitors. Stem Cells 2009;27:2405-13.
14. Alvero AB, Montagna MK, Chen R, Kim KH, Kyungjin K, Visintin I, et al. NV-128, a novel isoflavone derivative, induces caspase-independent cell death through the Akt/mammalian target of rapamycin pathway. Cancer 2009.
15. Flick MB, O'Malley D, Rutherford T, Rodov S, Kamsteeg M, Hao XY, et al. Apoptosis-based evaluation of chemosensitivity in ovarian cancer patients. J Soc Gynecol Investig 2004;11:252-9. (Pubitemid 38561371)
16. Kamsteeg M, Rutherford T, Sapi E, Hanczaruk B, Shahabi S, Flick M, et al. Phenoxodiol-an isoflavone analog-induces apoptosis in chemoresistant ovarian cancer cells. Oncogene 2003;22:2611-20. (Pubitemid 36605609)
17. Kulich SM, Horbinski C, Patel M, Chu CT. 6-Hydroxydopamine induces mitochondrial ERK activation. Free Radic Biol Med 2007;43:372-83. (Pubitemid 46977632)
18. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002;2:647-56. (Pubitemid 37328916)
19. Sanz P. AMP-activated protein kinase: structure and regulation. Curr Protein Pept Sci 2008;9:478-92.
20. Kimball SR. Interaction between the AMP-activated protein kinase and mTOR signaling pathways. Med Sci Sports Exerc 2006;38:1958-64. (Pubitemid 44707801)
21. Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003;115:577-90. (Pubitemid 37506046)
22. Corradetti MN, Guan KL. Upstream of the mammalian target of rapamycin: do all roads pass through mTOR? Oncogene 2006;25:6347-60. (Pubitemid 44582281)
23. Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol Cell Biol 2004;24:200-16. (Pubitemid 38010048)
24. Roberts PJ, Der CJ. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007;26:3291-310. (Pubitemid 46763022)
25. Ciuffreda L, Di Sanza C, Incani UC, Milella M. The mTOR pathway: a new target in cancer therapy. Curr Cancer Drug Targets;10:484-95.
26. Wellen KE, Thompson CB. Cellular metabolic stress: considering how cells respond to nutrient excess. Mol Cell;40:323-32.
27. Faivre S, Kroemer G, Raymond E. Current development of mTOR inhibitors as anticancer agents. Nat Rev Drug Discov 2006;5:671-88. (Pubitemid 44151605)
28. Duvel K, Yecies JL, Menon S, Raman P, Lipovsky AI, Souza AL, et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell;39:171-83.
29. Menon S, Manning BD. Common corruption of the mTOR signaling network in human tumors. Oncogene 2008;27 Suppl 2:S43-51.
30. Hsu PP, Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell 2008;134:703-7.
31. Dias N, Bailly C. Drugs targeting mitochondrial functions to control tumor cell growth. Biochem Pharmacol 2005;70:1-12. (Pubitemid 40797865)
32. Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria in cancer cells: what is so special about them? Trends Cell Biol 2008;18:165-73.
33. Szatrowski TP, Nathan CF. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 1991;51:794-8.
34. Mates JM, Sanchez-Jimenez F. Antioxidant enzymes and their implications in pathophysiologic processes. Front Biosci 1999;4:D339-45.
35. Oberley TD, Oberley LW. Antioxidant enzyme levels in cancer. Histol Histopathol 1997;12:525-35. (Pubitemid 27240324)
36. Klaunig JE, Kamendulis LM. The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 2004;44:239-67. (Pubitemid 38263841)
37. Adler V, Yin Z, Tew KD, Ronai Z. Role of redox potential and reactive oxygen species in stress signaling. Oncogene 1999;18:6104-11.
38. Naka K, Muraguchi T, Hoshii T, Hirao A. Regulation of reactive oxygen species and genomic stability in hematopoietic stem cells. Antioxid Redox Signal 2008;10:1883-94.
39. Kohno M, Pouyssegur J. Targeting the ERK signaling pathway in cancer therapy. Ann Med 2006;38:200-11. (Pubitemid 43675585)
40. Seger R, Krebs EG. The MAPK signaling cascade. FASEB J 1995;9:726-35.
41. Kim YK, Kim HJ, Kwon CH, Kim JH, Woo JS, Jung JS, et al. Role of ERK activation in cisplatin-induced apoptosis in OK renal epithelial cells. J Appl Toxicol 2005;25:374-82. (Pubitemid 41337233)