Anticancer effects of phenoxazine derivatives revealed by inhibition of cell growth and viability, disregulation of cell cycle, and apoptosis induction in HTLV-1-positive leukemia cells

Journal of Pharmacological Sciences

Volumn 110, Issue 1, 2009, Pages 87-97

  Miyano Kurosaki, Naoko ^a   Ikegami, Kou ^a   Kurosaki, Kunihiko ^b   Endo, Takahiko ^c   Aoyagi, Hoshimi ^a   Hanami, Mari ^a   Yasumoto, Jun ^a   Tomoda, Akio ^c  

^a CHIBA INSTITUTE OF TECHNOLOGY   (Japan)

^b TOHO UNIVERSITY   (Japan)

^c TOKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

Adult T cell leukemia; Apoptosis; HTLV 1; Phenoxazine; Syncytium formation

Indexed keywords

2 AMINO 4,4ALPHA DIHYDRO 4ALPHA,7 DIMETHYL 3H PHENOXAZIN 3 ONE; 2 AMINOPHENOXAZINE 3 ONE; 3 AMINO 1,4ALPHA DIHYDRO 4ALPHA,8 DIMETHYL 2H PHENOXAZIN 2 ONE; PHENOXAZINE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; DRUG EFFECT; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS INFECTION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; RAT; SYNCYTIUM; T CELL LEUKEMIA; VIRUS TRANSMISSION;

EID: 66349110927     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1254/jphs.08347FP     Document Type: Article

References (48)

1. Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD, Gallo RC. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci U S A. 1980;77:7415-7419. (Pubitemid 11131140)
2. Hinuma Y, Nagata K, Hanaoka M, Nakai M, Matsumoto T, Kinoshita K, et al. Adult T cell leukemia: Antigen in an ATL cell line and detection of antibodies to the antigen in human sera. Proc Natl Acad Sci U S A. 1981;78:6476-6480. (Pubitemid 12179735)
3. Yoshida M, Miyoshi I, Hinuma Y. Isolation and characterization of retrovirus from cell lines of human adult T-cell leukemia and its implication in the disease. Proc Natl Acad Sci U S A. 1982;79:2031-2036. (Pubitemid 12088563)
4. Birmann BM, Breen EC, Stuver S, Cranston B, Martinez-Maza O, Falk KI, et al. Population differences in immune marker profiles associated with human T-lymphotropic virus type I infection in Japan and Jamaica. Int J Cancer. 2009;124:614-621.
5. Yamamoto N, Okada M, Koyanagi Y, Kannnagi M, Hinuma Y. Transformation of human leukocytes by cocultivation with an adult T cell leukemia virus producer cell line. Science. 1982;217:737-739. (Pubitemid 12049575)
6. Feuer G, Green PL. comparative biology of human T-cell lymphotropic virus type l (HTLV-1) and HTLV-2. Oncogene. 2005;24:5996-6004. (Pubitemid 43086117)
7. Miyoshi I, Kubonishi I, Sumida M, Hiraki S, Tsubota T, Kimura I, et al. A novel T-cell line derived from adult T-cell leukemia. Gann. 1980;71:155-156. (Pubitemid 10100460)
8. Grassmann R, Abound M, Jeang K-T. Molecular mechanisms of cellular transformation by HTLV-1 Tax. Oncogene. 2005;24:5976-5985. (Pubitemid 43086115)
9. Miyoshi I, Kubonishi I, Yoshimoto S, Akagi T, Ohtsuki Y, Shiraishi Y, et al. Type C virus particles in a cord T-cell line derived by co-cultivating normal human cord leukocytes and human leukaemic T cells. Nature. 1981;294:770-771. (Pubitemid 12174453)
10. Nakazato T, Okudaira T, Ishikawa C, Nakama S, Sawada S, Tomita M, et al. Anti-adult T-cell leukemia effects of a novel synthetic retinoid, Am80 (Tamibarotene). Cancer Sci. 2008;99:2286-2294.
11. Harakeh S, Abu-El-Ardat K, Diab-Assaf M, Niedzwiecki A, El-Sabban M, Rath M. Epigallocatechin-3-gallate induces apoptosis and cell cycle arrest in HTLV-1-positive and -negative leukemia cells. Med Oncol. 2008;25:30-39.
12. Moarbess G, El-Haji H, Kfoury Y, El-Sabban ME, Lepelletier Y, Hermine O, et al. EAPB0203, a member of the imidazoquinoxaline family, inhibits growth and induces caspase-dependent apoptosis in T-cell lymphomas and HTLV-I-associated adult T-cell leukemia/ lymphoma. Blood. 2008;111:3770-3777.
13. Ishikawa C, Tafuku S, Kadekaru T, Sawada S, Tomita M, Okudaira T, et al. Antiadult T-cell leukemia effects of brown algae fucoxanthin and its deacetylated product, fucoxanthinol. Int J Cancer. 2008;123:2702-2712.
14. Tomoda A, Arai S, Ishida R, Shimamoto T, Ohyashiki K. An improved method for the rapid preparation of 2-amino-4,4α- dihydro-4α,7-dimethyl-3H- phenoxazine-3-one, a novel antitumor agent. Biorg Med Chem Lett. 2001;11:1057-1058. (Pubitemid 32327967)
15. Shimizu S, Suzuki M, Tomoda A, Arai S, Taguchi H, Hanawa T, et al. Phenoxazine compounds produced by the reactions with bovine hemoglobin show antimicrobial activity against nontuberculosis mycobacteria. Tohoku J Exp Med. 2004;203:47-52. (Pubitemid 38832654)
16. Shimizu S, Suzuki M, Miyazawa K, Yokoyama T, Ohyashiki K, Miyazaki K, et al. Differentiation and apoptosis in human malignant melanoma G-361 cells induced by 2-aminophenoxazine-3-one. Oncol Rep. 2005;14:41-46.
17. Kato S, Shirato K, Imaizumi K, Toyota H, Mizuguchi J, Odawara M, et al. Anticancer effects of phenoxazine derivatives combined with tumor necrosis factor-related apoptosis-inducing ligand on pancreatic cancer cell lines, KLM-1 and MIA-PaCa-2. Oncol Rep. 2006;15:843-848.
18. Shirato K, Imaizumi K, Abe A, Tomoda A. Phenoxazine derivatives, 2-amino-4,4α-dihydro-4α,7-dimethyl-3H-phenoxazine-3- one and 2-aminophenoxazine-3-one-induced apoptosis through a caspase-independent mechanism in human neuroblastoma cell line NB-1 cells. Biol Pharm Bull. 2007;30:331-336. (Pubitemid 46255375)
19. Shirato K, Imaizumi K, Abe A, Tomoda A. Phenoxazine derivatives induce caspase-independent cell death in human glioblastoma cell lines, A-172 and U-251 MG. Oncol Rep. 2007;17:201-208.
20. Shirato K, Imaizumi K, Miyazawa K, Takasaki A, Mizuguchi J, Che XF, et al. Apoptosis induction preceded by mitochondrial depolarization in multiple myeloma cell line U266 by 2-aminophenoxazine-3-one. Biol Pharm Bull. 2008;31:62-67.
21. Iwata A, Yamaguchi T, Sato K, Izumi R, Tomoda A. Antiviral activity of 2-amino-4,4α-dihydro-4α,7-dimethyl-3H-phenoxazine- 3-one on poliovirus. Tohoku J Exp Med. 2003;200:161-165. (Pubitemid 37258815)
22. Iwata A, Yamaguchi T, Sato K, Yoshitake N, Tomoda A. Suppression of proliferation of poliovirus and porcine parvovirus by novel phenoxazine, 2-amino-4,4α-dihydro-4α,7-dimethyl-3H-phenoxazine- 3-one, 3-amino-1,4α-dihydro-4α,8-dimethyl-2H-phenoxazine- 2-one. Biol Pharm Bull. 2005;28: 905-907. (Pubitemid 40740665)
23. Hayashi K, Hayashi T, Tomoda A. Phenoxazine derivatives inactivate human cytomegalovirus, herpes simplex virus-1, and herpes simplex virus-2 in vitro. J Pharmacol Sci. 2008;106:369-375.
24. Akazawa M, Koshibu-Koizumi J, Iwamoto T, Takasaki M, Nakamura M, Tomoda A. Effect of novel phenoxazine compounds, 2-amino-4,4α-dihydro-4α,7- dimethyl-3H-phenoxazine- 3-one and 3-amino-1,4α-dihydro-4α,8- dimethyl-2H-phenoxazine- 2-one on proliferation of phytohemagglutinin- or anti-human IgM-activated human peripheral blood mononuclear cells. Tohoku J Exp Med. 2002;196:185-192. (Pubitemid 34727554)
25. Gao S, Takano T, Sada K, He H, Noda C, Hori-Tamura N, et al. A novel phenoxazine derivative suppresses surface IgM expression in DT40 B cell line. Br J Pharmacol. 2002;137:749-755. (Pubitemid 35404173)
26. Enoki E, Sada K, Qu X, Kyo S, Shahjahan Miah SM, Hatani T, et al. The phenoxazine derivative Phx-1 suppresses IgE-mediated degranulation in rat basophilic leukemia RBL-2H3 cells. J Pharmacol Sci. 2004;94: 329-333. (Pubitemid 38470743)
27. Shimamoto T, Tomoda A, Ishida R, Ohyashiki K. Antitumor effects of a novel phenoxazine derivative on human leukemia cell lines in vitro and in vivo. Clin Cancer Res. 2001;704:704-708. (Pubitemid 32707997)
28. Koshibu-Koizumi J, Akazawa M, Iwamoto T, Takasaki M, Mizuno F, Kobayashi R, et al. Antitumor activity of a phenoxazine compound, 2-amino-4,4α- dihydro-4α,7-dimethyl- 3H-phenoxazine-3-one against human B cell and T cell lymphoblastoid cell lines: induction of mixed types of cell death, apoptosis and necrosis. J Cancer Res Clin Oncol. 2002;128:363-368. (Pubitemid 34824178)
29. Hoshino H, Shimoyama M, Miwa M, Sugimura T. Detection of lymphocytes producing a human retrovirus associated with adult T-cell leukemia by syncytia induction assay. Proc Natl Acad Sci U S A. 1983;80:7337-7341. (Pubitemid 14208853)
30. Nagy K, Clapham P, Cheingsong-Popov R, Weiss R. Human T-cell leukemia virus type 1: induction of syncytia and inhibition by patients sera. Int J Cancer. 1983;32:321-328.
31. Miyano-Kurosaki N, Koyanagi Y, Mizuguchi M, Ohki S, Makino K, Yamamoto N. Inhibition of HTLV-1 induction and virus-induced syncytia formation by oligodeoxynucleotides. Virus Genes. 1996;12:205-217. (Pubitemid 26294665)
32. Green DR, Reed JC. Mitochondria and apoptosis. Science. 1998;281:13309-13312.
33. Hengartner MO. The biochemistry of apoptosis. Nature. 2000;407:770-776.
34. Hail N Jr, Carter BZ, Konopleva M, Andreeff M. Apoptosis effector mechanisms: a requiem performed in different keys. Apoptosis. 2006;11:889-904. (Pubitemid 43880261)
35. Tobey RA. Different drugs arrest cells at a number of distinct stages in G2. Nature. 1975;254:245-247.
36. Sagara U, Ishida C, Inoue Y, Shiraki H, Maeda Y. 71-Kilodalton heat shock cognate protein acts as a cellular receptor for syncytium formation induced by human t-cell lymphotropic virus type l. J Virol. 1998;72:535-541. (Pubitemid 28048869)
37. Chibber BAK, Balasubramanian A, Viswanatha T. Binding of actionomycin chromophore analogues to DNA. Can J Biochem. 1973;51:204-217.
38. Ishida R, Yamanaka S, Kawai H, Ito H, Iwai M, Nishizawa M, et al. Antitumor activity of 2-amino-4,4α-dihydro-4α,7-dimethyl- 3H-phenoxazine-3-one, a novel phenoxazine derivative produced by the reaction of 2-amino-5-methylphenol with bovine hemolysate. Anti-Cancer Drugs. 1996;7:591-595. (Pubitemid 26276351)
39. Bendic C, Volanschi E. Molecular modeling of the interaction of some phenoxazone-antitumoral drugs with DNA. Internet Electro J Mol Design. 2006;5:320-330.
40. Tomoda A, Hamashima H, Arisawa M, Kikuchi T, Tezuka Y, Koshimura S. Phenoxazine synthesis by human hemoglobin. Biochim Biophys Acta. 1992;1117:3306-3314.
41. Nagasawa HT, Gutmann HR, Morgan MA. The oxidation of o-aminophenols by cytochrome c and cytochrome oxidase. II. Synthesis and identification of oxidation products. J Biol Chem. 1963;17:703-708.
42. Barry CE, Nayar PG, Begley TP. Phenoxazinone synthase: enzymatic catalysis of an aminophenol oxidative cascade. J Am Chem Soc. 1988;110:3333-3334. (Pubitemid 18133579)
43. Motohashi N, Mitscher LA, Meyer R. Potential antitumor phenoxazines. Med Res Rev. 1991;11:239-294.
44. Suzuki F, Hashimoto K, Ishihara M, Westman G, Samuelsson K, Kawase M, et al. Tumor-specificity and type of cell death induced by phenoxazines. Anticancer Res. 2007;27:4233-4238.
45. Shimoyama M. Diagnostic criteria and classification of clinical subtypes of adult T-cell leukemia-lymphoma. A report from the Lymphoma Study Group (1984-1987). Br J Haematol. 1991;79:428-437.
46. Mori H, Honda K, Ishida R, Norita T, Tomoda A. Antitumor activity of 2-amino-4,4α-dihydro-4α,7-dimethyl-3H-phenoxazine- 3-one against Meth A tumor transplanted into BALB/c mice. Anticancer Drugs. 2000;11:653-657.
47. Azuine MA, Tokuda H, Takayasu J, Enjyo F, Mukainaka T, Konoshima T, et al. Cancer chemopreventive effect of phenothiazines and related tri-heterocyclic analogues in the 12-O-tetradecanoylphorbol- 13-acetate promoted Epstein-Barr virus early antigen activation and the mouse skin two-stage carcinogenesis models. Pharmacol Res. 2004;49:161-169. (Pubitemid 37485712)
48. Miyano-Kurosaki N, Kurosaki K, Hayashi M, Takaku H, Hayafune M, Shirato K, et al. 2-Aminophenoxazine-3-one suppresses the growth of mouse malignant melanoma B16 cells transplanted into C57BL/6Cr Slc mice. Biol Pharm Bull. 2006;29:2197-2201. (Pubitemid 44690942)