Mithramycin A inhibits myeloid cell leukemia-1 to induce apoptosis in oral squamous cell carcinomas and tumor xenograft through activation of bax and oligomerization

Molecular Pharmacology

Volumn 83, Issue 1, 2013, Pages 33-41

  Shin, Ji Ae ^a   Jung, Ji Youn ^b   Ryu, Mi Heon ^c   Safe, Stephen ^d,e   Cho, Sung Dae ^a  

^a Chonbuk National University   (South Korea)

^b Kongju National University   (South Korea)

^c Pusan National University   (South Korea)

^d TEXAS A AND M UNIVERSITY   (United States)

^e TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; MITHRAMYCIN; MITHRAMYCIN A; MYELOID CELL LEUKEMIA 1; PEPTIDES AND PROTEINS; PROTEIN BAX; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL TRANSFORMATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; MOUSE; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MICE, NUDE; MITOCHONDRIA; MOUTH MUCOSA; MOUTH NEOPLASMS; NEOPLASM TRANSPLANTATION; PLICAMYCIN; POLYMERIZATION; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA INTERFERENCE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84871604968     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.081364     Document Type: Article

References (39)

1. Abdelrahim M, Samudio I, Smith R, 3rd, Burghardt R, and Safe S (2002) Small inhibitory RNA duplexes for Sp1 mRNA block basal and estrogen-induced gene expression and cell cycle progression in MCF-7 breast cancer cells. J Biol Chem 277:28815-28822.
2. Abdelrahim M, Smith R, 3rd, Burghardt R, and Safe S (2004) Role of Sp proteins in regulation of vascular endothelial growth factor expression and proliferation of pancreatic cancer cells. Cancer Res 64:6740-6749. (Pubitemid 39297937)
3. Akgul C (2009) Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell Mol Life Sci 66:1326-1336.
4. Antonsson B, Montessuit S, Sanchez B, and Martinou JC (2001) Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem 276:11615-11623.
5. Booy EP, Henson ES, and Gibson SB (2011) Epidermal growth factor regulates Mcl-1 expression through the MAPK-Elk-1 signalling pathway contributing to cell survival in breast cancer. Oncogene 30:2367-2378.
6. Chadalapaka G, Jutooru I, Chintharlapalli S, Papineni S, Smith R, 3rd, Li X, and Safe S (2008) Curcumin decreases specificity protein expression in bladder cancer cells. Cancer Res 68:5345-5354.
7. Cheng S, Gao N, Zhang Z, Chen G, Budhraja A, Ke Z, Son YO, Wang X, Luo J, and Shi X (2010) Quercetin induces tumor-selective apoptosis through downregulation of Mcl-1 and activation of Bax. Clin Cancer Res 16:5679-5691.
8. Choi ES, Shim JH, Jung JY, Kim HJ, Choi KH, Shin JA, Nam JS, Cho NP, and Cho SD (2011a) Apoptotic effect of tolfenamic acid in androgen receptor-independent prostate cancer cell and xenograft tumor through specificity protein 1. Cancer Sci 102:742-748.
9. Choi KH, Shim JH, Huong LD, Cho NP, and Cho SD (2011b) Inhibition of myeloid cell leukemia-1 by tolfenamic acid induces apoptosis in mucoepidermoid carcinoma. Oral Dis 17:469-475.
10. Craig RW (2002) MCL1 provides a window on the role of the BCL2 family in cell proliferation, differentiation and tumorigenesis. Leukemia 16:444-454.
11. Cuconati A, Mukherjee C, Perez D, and White E (2003) DNA damage response and MCL-1 destruction initiate apoptosis in adenovirus-infected cells. Genes Dev 17: 2922-2932. (Pubitemid 37523156)
12. Erovic BM, Pelzmann M, Grasl MCh, Pammer J, Kornek G, Brannath W, Selzer E, and Thurnher D (2005) Mcl-1, vascular endothelial growth factor-R2, and 14-3- 3sigma expression might predict primary response against radiotherapy and chemotherapy in patients with locally advanced squamous cell carcinomas of the head and neck. Clin Cancer Res 11:8632-8636. (Pubitemid 43005910)
13. Fleischer B, Schulze-Bergkamen H, Schuchmann M, Weber A, Biesterfeld S, Müller M, Krammer PH, and Galle PR (2006) Mcl-1 is an anti-apoptotic factor for human hepatocellular carcinoma. Int J Oncol 28:25-32.
14. Gao Y, Jia Z, and Kong X et al. (2011) Combining betulinic acid and mithramycin a effectively suppresses pancreatic cancer by inhibiting proliferation, invasion, and angiogenesis. Cancer Res 71 :5182-5193.
15. Germain M, Milburn J, and Duronio V (2008) MCL-1 inhibits BAX in the absence of MCL-1/BAX Interaction. J Biol Chem 283:6384-6392.
16. Jia Z, Gao Y, and Wang L et al. (2010) Combined treatment of pancreatic cancer with mithramycin A and tolfenamic acid promotes Sp1 degradation and synergistic antitumor activity. Cancer Res 70:1111-1119.
17. Kazi A, Sun J, and Doi K et al. (2011) The BH3 alpha-helical mimic BH3-M6 disrupts Bcl-X(L), Bcl-2, and MCL-1 protein-protein interactions with Bax, Bak, Bad, or Bim and induces apoptosis in a Bax- and Bim-dependent manner. J Biol Chem 286:9382-9392.
18. Koller CA and Miller DM (1986) Preliminary observations on the therapy of the myeloid blast phase of chronic granulocytic leukemia with plicamycin and hydroxyurea. N Engl J Med 315:1433-1438. (Pubitemid 17051702)
19. Kozopas KM, Yang T, Buchan HL, Zhou P, and Craig RW (1993) MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc Natl Acad Sci USA 90:3516-3520. (Pubitemid 23111397)
20. Krajewska M, Krajewski S, Epstein JI, Shabaik A, Sauvageot J, Song K, Kitada S, and Reed JC (1996) Immunohistochemical analysis of bcl-2, bax, bcl-X, and mcl-1 expression in prostate cancers. Am J Pathol 148:1567-1576. (Pubitemid 26135897)
21. Leber B, Lin J, and Andrews DW (2007) Embedded together: the life and death consequences of interaction of the Bcl-2 family with membranes. Apoptosis 12:897-911. (Pubitemid 46653294)
22. Leu CM, Chang C, and Hu C (2000) Epidermal growth factor (EGF) suppresses staurosporine-induced apoptosis by inducing mcl-1 via the mitogen-activated protein kinase pathway. Oncogene 19:1665-1675. (Pubitemid 30200968)
23. Liang XH, Lewis J, Foote R, Smith D, and Kademani D (2008) Prevalence and significance of human papillomavirus in oral tongue cancer: the Mayo Clinic experience. J Oral Maxillofac Surg 66:1875-1880.
24. Malek A, Núñez LE, Magistri M, Brambilla L, Jovic S, Carbone GM, Morís F, and Catapano CV (2012) Modulation of the activity of Sp transcription factors by mithramycin analogues as a new strategy for treatment of metastatic prostate cancer. PLoS ONE 7:e35130.
25. Mandelin AM, 2nd and Pope RM (2007) Myeloid cell leukemia-1 as a therapeutic target. Expert Opin Ther Targets 11:363-373.
26. Nagata M, Wada K, Nakajima A, Nakajima N, Kusayama M, Masuda T, Iida S, Okura M, Kogo M, and Kamisaki Y (2009) Role of myeloid cell leukemia-1 in cell growth of squamous cell carcinoma. J Pharmacol Sci 110:344-353.
27. Opferman JT, Iwasaki H, Ong CC, Suh H, Mizuno S, Akashi K, and Korsmeyer SJ (2005) Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 307:1101-1104. (Pubitemid 40262114)
28. Rahmani M, Davis EM, Bauer C, Dent P, and Grant S (2005) Apoptosis induced by the kinase inhibitor BAY 43-9006 in human leukemia cells involves down-regulation of Mcl-1 through inhibition of translation. J Biol Chem 280:35217-35227. (Pubitemid 41532709)
29. Sachrajda I and Ratajewski M (2011) Mithramycin A suppresses expression of the human melanoma-associated gene ABCB8. Mol Genet Genomics 285:57-65.
30. Seznec J, Silkenstedt B, and Naumann U (2011) Therapeutic effects of the Sp1 inhibitor mithramycin A in glioblastoma. J Neurooncol 101:365-377.
31. Silverman S, Jr (2001) Demographics and occurrence of oral and pharyngeal cancers. The outcomes, the trends, the challenge. J Am Dent Assoc 132 (Suppl):7S-11S.
32. Song L, Coppola D, Livingston S, Cress D, and Haura EB (2005) Mcl-1 regulates survival and sensitivity to diverse apoptotic stimuli in human non-small cell lung cancer cells. Cancer Biol Ther 4:267-276. (Pubitemid 41351285)
33. Taniai M, Grambihler A, Higuchi H, Werneburg N, Bronk SF, Farrugia DJ, Kaufmann SH, and Gores GJ (2004) Mcl-1 mediates tumor necrosis factor-related apoptosisinducing ligand resistance in human cholangiocarcinoma cells. Cancer Res 64:3517-3524. (Pubitemid 38657926)
34. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, Adams JM, and Huang DC (2005) Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19:1294-1305. (Pubitemid 41003019)
35. Yang-Yen HF (2006) Mcl-1: a highly regulated cell death and survival controller. J Biomed Sci 13:201-204.
36. Yuan P, Wang L, Wei D, Zhang J, Jia Z, Li Q, Le X, Wang H, Yao J, and Xie K (2007) Therapeutic inhibition of Sp1 expression in growing tumors by mithramycin a correlates directly with potent antiangiogenic effects on human pancreatic cancer. Cancer 110:2682-2690. (Pubitemid 350250337)
37. Zhang Z, Song T, Zhang T, Gao J, Wu G, An L, and Du G (2011) A novel BH3 mimetic S1 potently induces Bax/Bak-dependent apoptosis by targeting both Bcl-2 and Mcl- 1. Int J Cancer 128:1724-1735.
38. Zhou P, Levy NB, Xie H, Qian L, Lee CY, Gascoyne RD, and Craig RW (2001) MCL1 transgenic mice exhibit a high incidence of B-cell lymphoma manifested as a spectrum of histologic subtypes. Blood 97:3902-3909.
39. Zhou P, Qian L, Bieszczad CK, Noelle R, Binder M, Levy NB, and Craig RW (1998) Mcl-1 in transgenic mice promotes survival in a spectrum of hematopoietic cell types and immortalization in the myeloid lineage. Blood 92:3226-3239. (Pubitemid 28492330)