An Active Compound from the Pyrazine Family Induces Apoptosis by Targeting the Bax/Bcl2 and Survivin Expression in Chronic Myeloid Leukemia K562 Cells


Дәйексөз келтіру

Толық мәтін

Аннотация

Background:It has been established that pyrazine derivatives, which have widespread bioactivities, can effectively treat cancer.

Objectives:In this study, we investigated the effects of 2-methoxy-5-(oxiran-2-ylmethyl) phenyl pyrazine-2- carboxylate (2-mOPP), a new pyrazine derivative, on proliferation, viability, and apoptosis induction in human leukemia K562 cells.

Methods::For this purpose, the K562 cells were treated with various concentrations (20-120 µM) of the 2-mOPP for 24-72 hours. Cell viability was determined by MTT growth inhibition assay. Apoptotic activity of 2-mOPP was investigated morphologically by Hoechst staining, cell surface expression assay of phosphatidylserine by Annexin-V/PI technique, as well as DNA fragmentation assay. The effect of 2-mOPP on the K562 cell cycle was studied by flow cytometry. To determine the impact of 2-mOPP on the expression of intrinsic apoptosis-related genes, Bcl2 (anti-apoptotic), Bax (pro-apoptotic), and Survivin genes expression levels were evaluated before and after treatment with 2-mOPP through Real-Time PCR analysis.

Results::The results revealed that 2-mOPP inhibited viability with IC50 of 25µM in 72 h. Morphological changes assessment by fluorescence microscopy, Annexin V/PI double staining by flow cytometry, and DNA ladders formation upon cell treatment with the 2-mOPP showed that this compound induces apoptosis at IC50 value. Cell cycle arrest was observed in the G0/G1 phase, and the sub-G1 cell population (the sign of apoptosis) increased in a time-dependent manner. Low expression levels of Bcl2 and Survivin in K562 cells were observed 24-72 h after treatment. Along with the down-regulation of Survivin and Bcl2, the expression of Bax was increased after treatment with 2-mOPP.

Conclusion:These findings demonstrate that the new pyrazine derivative plays a crucial role in blocking the proliferation of the leukemic cells by inducing cell cycle arrest and apoptosis.

Негізгі сөздер

Авторлар туралы

Saeedeh Rostampour

Department of Biology, Faculty of Natural Science, University of Tabriz

Email: info@benthamscience.net

Farhad Eslami

Department of Biology, Faculty of Natural Science, University of Tabriz

Email: info@benthamscience.net

Esmaeil Babaei

Department of Biology, Faculty of Natural Science, University of Tabriz

Email: info@benthamscience.net

Hossein Mostafavi

Department of Organic Chemistry, Faculty of Chemistry, University of Tabriz

Email: info@benthamscience.net

Majid Mahdavi

Department of Biology, Faculty of Natural Science, University of Tabriz

Хат алмасуға жауапты Автор.
Email: info@benthamscience.net

Әдебиет тізімі

  1. Schmitt, C.A. Senescence, apoptosis and therapy — cutting the lifelines of cancer. Nat. Rev. Cancer, 2003, 3(4), 286-295. doi: 10.1038/nrc1044 PMID: 12671667
  2. Schulze-Bergkamen, H.; Krammer, P.H. Apoptosis in cancer—implications for therapy. Semin. Oncol., 2004, 31(1), 90-119. doi: 10.1053/j.seminoncol.2003.11.006 PMID: 14970941
  3. Stefanis, L.; Burke, R.E.; Greene, L.A. Apoptosis in neurodegenerative disorders. Curr. Opin. Neurol., 1997, 10(4), 299-305. doi: 10.1097/00019052-199708000-00004 PMID: 9266153
  4. Elmore, S. Apoptosis: A review of programmed cell death. Toxicol. Pathol., 2007, 35(4), 495-516. doi: 10.1080/01926230701320337 PMID: 17562483
  5. Fridman, J.S.; Lowe, S.W. Control of apoptosis by p53. Oncogene, 2003, 22, 9030-9040. doi: 10.1038/sj.onc.1207116
  6. Yin, X.M. Signal transduction mediated by Bid, a pro-death Bcl-2 family proteins, connects the death receptor and mitochondria apoptosis pathways. Cell Res., 2000, 10(3), 161-167. doi: 10.1038/sj.cr.7290045 PMID: 11032168
  7. Tzifi, F.; Economopoulou, C.; Gourgiotis, D.; Ardavanis, A.; Papageorgiou, S.; Scorilas, A. The role of BCL2 family of apoptosis regulator proteins in acute and chronic leukemias. Adv. Hematol., 2012, 2012, 524308. doi: 10.1155/2012/524308
  8. Sakamoto, S.; Kyprianou, N. Targeting anoikis resistance in prostate cancer metastasis. Mol. Aspects Med., 2010, 31(2), 205-214. doi: 10.1016/j.mam.2010.02.001 PMID: 20153362
  9. Mahdavi, M.; Davoodi, J.; Zali, M.R.; Foroumadi, A. Concomitant activation of caspase-9 and down-regulation of IAP proteins as a mechanism of apoptotic death in HepG2, T47D and HCT-116 cells upon exposure to a derivative from 4-aryl-4H-chromenes family. Biomed. Pharmacother., 2011, 65(3), 175-182. doi: 10.1016/j.biopha.2011.03.001 PMID: 21565459
  10. Deveraux, Q.L.; Stennicke, H.R.; Salvesen, G.S.; Reed, J.C. Endogenous inhibitors of caspases. J. Clin. Immunol., 1999, 19(6), 388-398. doi: 10.1023/A:1020502800208 PMID: 10634212
  11. Clem, R.J.; Sheu, T.T.; Richter, B.M.; He, W.W.; Thornberry, N.A.; Duckett, C.S.; Hardwick, J.M. c-IAP1 is cleaved by caspases to produce a proapoptotic C-terminal fragment. J. Biol. Chem., 2001, 276(10), 7602-7608. doi: 10.1074/jbc.M010259200 PMID: 11106668
  12. Nachmias, B.; Ashhab, Y.; Bucholtz, V.; Drize, O.; Kadouri, L.; Lotem, M.; Peretz, T.; Mandelboim, O.; Ben-Yehuda, D. Caspase-mediated cleavage converts Livin from an antiapoptotic to a proapoptotic factor: Implications for drug-resistant melanoma. Cancer Res., 2003, 63(19), 6340-6349. PMID: 14559822
  13. Lozzio, B.B.; Lozzio, C.B. Properties and usefulness of the original K-562 human myelogenous leukemia cell line. Leuk. Res., 1979, 3(6), 363-370. doi: 10.1016/0145-2126(79)90033-X PMID: 95026
  14. Chen, Y.; Peng, C.; Sullivan, C.; Li, D.; Li, S. Critical molecular pathways in cancer stem cells of chronic myeloid leukemia. Leukemia, 2010, 24(9), 1545-1554. doi: 10.1038/leu.2010.143 PMID: 20574455
  15. Chang, G.; Zhang, H.; Wang, J.; Zhang, Y.; Xu, H.; Wang, C.; Zhang, H.; Ma, L.; Li, Q.; Pang, T. CD44 targets Wnt/β-catenin pathway to mediate the proliferation of K562 cells. Cancer Cell Int., 2013, 13(1), 117. doi: 10.1186/1475-2867-13-117 PMID: 24257075
  16. Calabretta, B.; Perrotti, D. The biology of CML blast crisis. Blood, 2004, 103(11), 4010-4022. doi: 10.1182/blood-2003-12-4111 PMID: 14982876
  17. Quintás-Cardama, A.; Cortes, J. Molecular biology of bcr-abl1–positive chronic myeloid leukemia. Blood, 2009, 113(8), 1619-1630. doi: 10.1182/blood-2008-03-144790 PMID: 18827185
  18. Moosavi, M.A.; Yazdanparast, R.; Lotfi, A. ERK1/2 inactivation and p38 MAPK-dependent caspase activation during guanosine 5′-triphosphate-mediated terminal erythroid differentiation of K562 cells. Int. J. Biochem. Cell Biol., 2007, 39(9), 1685-1697. doi: 10.1016/j.biocel.2007.04.016 PMID: 17543571
  19. de Lima, A.P.; de Castro, P.F.; Vilanova-Costa, C.A.S.T. Mariana dos, S.M.F.; de Santana, B.B.R.A.; Benfica, P.L.; Valadares, M.C.; Pavanin, L.A.; dos Santos, W.B.; de Paula, S.L.E. The compound cis-(dichloro)tetrammineruthenium(III) chloride induces caspase-mediated apoptosis in K562 cells. Toxicol. In Vitro, 2010, 24(6), 1562-1568. doi: 10.1016/j.tiv.2010.06.015 PMID: 20600797
  20. Druker, B.J.; Guilhot, F.; O’Brien, S.G.; Gathmann, I.; Kantarjian, H.; Gattermann, N.; Deininger, M.W.N.; Silver, R.T.; Goldman, J.M.; Stone, R.M.; Cervantes, F.; Hochhaus, A.; Powell, B.L.; Gabrilove, J.L.; Rousselot, P.; Reiffers, J.; Cornelissen, J.J.; Hughes, T.; Agis, H.; Fischer, T.; Verhoef, G.; Shepherd, J.; Saglio, G.; Gratwohl, A.; Nielsen, J.L.; Radich, J.P.; Simonsson, B.; Taylor, K.; Baccarani, M.; So, C.; Letvak, L.; Larson, R.A. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N. Engl. J. Med., 2006, 355(23), 2408-2417. doi: 10.1056/NEJMoa062867 PMID: 17151364
  21. Abdel-Aziz, H.A.; El-Zahabi, H.S.A.; Dawood, K.M. Microwave-assisted synthesis and in vitro anti-tumor activity of 1,3,4-triaryl-5-N-arylpyrazole-carboxamides. Eur. J. Med. Chem., 2010, 45(6), 2427-2432. doi: 10.1016/j.ejmech.2010.02.026 PMID: 20207452
  22. Maga, J.A. Pyrazine update. Food Rev. Int., 1992, 8(4), 479-558. doi: 10.1080/87559129209540951
  23. Barlin, G.B. The Pyrazines: The Chemistry of Heterocyclic Compounds: A series of monographs; John Wiley & Sons: New York, 1982, 41, p. 1-10.
  24. Adams, J.; Kauffman, M. Development of the proteasome inhibitor Velcade (Bortezomib). Cancer Invest., 2004, 22(2), 304-311. doi: 10.1081/CNV-120030218 PMID: 15199612
  25. Barlin, G.B. The Pyrazines: The Chemistry of Heterocyclic Compounds: A series of monographs; John Wiley & Sons: New York, 1982, 41, p. 1-10.
  26. Miniyar, P.; Murumkar, P.; Patil, P.; Barmade, M.; Bothara, K. Unequivocal role of pyrazine ring in medicinally important compounds: A review. Mini Rev. Med. Chem., 2013, 13(11), 1607-1625. doi: 10.2174/1389557511313110007 PMID: 23544468
  27. Cynamon, M.H.; Gimi, R.; Gyenes, F.; Sharpe, C.A.; Bergmann, K.E.; Han, H.J.; Gregor, L.B.; Rapolu, R.; Luciano, G.; Welch, J.T. Pyrazinoic acid esters with broad spectrum in vitro antimycobacterial activity. J. Med. Chem., 1995, 38(20), 3902-3907. doi: 10.1021/jm00020a003 PMID: 7562923
  28. Simões, M.F.; Valente, E.; Gómez, M.J.R.; Anes, E.; Constantino, L. Lipophilic pyrazinoic acid amide and ester prodrugs. Eur. J. Pharm. Sci., 2009, 37(3-4), 257-263. doi: 10.1016/j.ejps.2009.02.012 PMID: 19491013
  29. Khani-Meinagh, H.; Mostafavi, H.; Reiling, N.; Mahdavi, M.; Zarrini, G. Design, synthesis and evaluation of biological activities of some novel anti-TB agents with bio-reducible functional group. Bioimpacts, 2019, 9(4), 199-209. doi: 10.15171/bi.2019.25 PMID: 31799156
  30. Zhou, H.; Yu, Y.; Li, H.; Shi, W.; Yang, H.; Liu, C.; Wang, S.; Yu, M. Anti-H can trigger apoptosis and down-regulate FUT1 expression in erythroid differentiated K562 cells without complement mediation. Transpl. Immunol., 2012, 27(4), 151-156. doi: 10.1016/j.trim.2012.10.001 PMID: 23063462
  31. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods, 1983, 65(1-2), 55-63. doi: 10.1016/0022-1759(83)90303-4 PMID: 6606682
  32. Eslami, F.; Mahdavi, M.; Babaei, E.; Hussen, B.M.; Mostafavi, H.; Shahbazi, A.; Hidayat, H.J. Down-regulation of Survivin and Bcl-2 concomitant with the activation of caspase-3 as a mechanism of apoptotic death in KG1a and K562 cells upon exposure to a derivative from ciprofloxacin family. Toxicol. Appl. Pharmacol., 2020, 409(November), 115331. doi: 10.1016/j.taap.2020.115331 PMID: 33171188
  33. Nicoletti, I.; Migliorati, G.; Pagliacci, M.C.; Grignani, F.; Riccardi, C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods, 1991, 139(2), 271-279. doi: 10.1016/0022-1759(91)90198-O PMID: 1710634
  34. Uchakina, O.N.; Ban, H.; McKallip, R.J. Targeting hyaluronic acid production for the treatment of leukemia: Treatment with 4-methylumbelliferone leads to induction of MAPK-mediated apoptosis in K562 leukemia. Leuk. Res., 2013, 37(10), 1294-1301. doi: 10.1016/j.leukres.2013.07.009 PMID: 23876826
  35. Finaurini, S.; Basilico, N.; Corbett, Y.; D’Alessandro, S.; Parapini, S.; Olliaro, P.; Haynes, R.K.; Taramelli, D. Dihydroartemisinin inhibits the human erythroid cell differentiation by altering the cell cycle. Toxicology, 2012, 300(1-2), 57-66. doi: 10.1016/j.tox.2012.05.024 PMID: 22677887
  36. Kalle, A.M.; Sachchidanand, S.; Pallu, R. Bcr–Abl-independent mechanism of resistance to imatinib in K562 cells: Induction of cyclooxygenase-2 (COX-2) by histone deacetylases (HDACs). Leuk. Res., 2010, 34(9), 1132-1138. doi: 10.1016/j.leukres.2010.01.030 PMID: 20206383
  37. Zheng, L.W.; Shao, J.H.; Zhao, B.X.; Miao, J.Y. Synthesis of novel pyrazolo1,5- apyrazin-4(5 H)-one derivatives and their inhibition against growth of A549 and H322 lung cancer cells. Bioorg. Med. Chem. Lett., 2011, 21(13), 3909-3913. doi: 10.1016/j.bmcl.2011.05.035 PMID: 21640587
  38. Zhang, J.H.; Fan, C.D.; Zhao, B.X.; Shin, D.S.; Dong, W.L.; Xie, Y.S.; Miao, J.Y. Synthesis and preliminary biological evaluation of novel pyrazolo1,5-apyrazin-4(5H)-one derivatives as potential agents against A549 lung cancer cells. Bioorg. Med. Chem., 2008, 16(24), 10165-10171. doi: 10.1016/j.bmc.2008.10.066 PMID: 19013820
  39. Ghodousi-Dehnavi, E.; Hosseini, R.H.; Arjmand, M.; Nasri, S.; Zamani, Z. A metabolomic investigation of eugenol on colorectal cancer cell line HT-29 by modifying the expression of APC, p53, and KRAS genes. eCAM, 2021, 2021, 1448206.
  40. Sahdev, A.K.; Raj, V.; Singh, A.K.; Rai, A.; Keshari, A.K.; De, A.; Samanta, A.; Kumar, U.; Rawat, A.; Kumar, D.; Nath, S.; Prakash, A.; Saha, S. Ameliorative effects of pyrazinoic acid against oxidative and metabolic stress manifested in rats with dimethylhydrazine induced colonic carcinoma. Cancer Biol. Ther., 2017, 18(5), 304-313. doi: 10.1080/15384047.2017.1310341 PMID: 28358223
  41. Crawford, L.J.A.; Walker, B.; Ovaa, H.; Chauhan, D.; Anderson, K.C.; Morris, T.C.M.; Irvine, A.E. Comparative selectivity and specificity of the proteasome inhibitors BzLLLCOCHO, PS-341, and MG-132. Cancer Res., 2006, 66(12), 6379-6386. doi: 10.1158/0008-5472.CAN-06-0605 PMID: 16778216
  42. Chauhan, D.; Hideshima, T.; Mitsiades, C.; Richardson, P.; Anderson, K.C. Proteasome inhibitor therapy in multiple myeloma. Mol. Cancer Ther., 2005, 4(4), 686-692. doi: 10.1158/1535-7163.MCT-04-0338 PMID: 15827343
  43. Ri, M.; Iida, S.; Ishida, T.; Ito, A.; Yano, H.; Inagaki, A.; Ding, J.; Kusumoto, S.; Komatsu, H.; Utsunomiya, A.; Ueda, R. Bortezomib‐induced apoptosis in mature T‐cell lymphoma cells partially depends on upregulation of Noxa and functional repression of Mcl‐1. Cancer Sci., 2009, 100(2), 341-348. doi: 10.1111/j.1349-7006.2008.01038.x PMID: 19068089
  44. Hideshima, T.; Mitsiades, C.; Akiyama, M.; Hayashi, T.; Chauhan, D.; Richardson, P.; Schlossman, R.; Podar, K.; Munshi, N.C.; Mitsiades, N.; Anderson, K.C. Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood, 2003, 101(4), 1530-1534. doi: 10.1182/blood-2002-08-2543 PMID: 12393500
  45. Mitsiades, N.; Mitsiades, C.S.; Richardson, P.G.; Poulaki, V.; Tai, Y.T.; Chauhan, D.; Fanourakis, G.; Gu, X.; Bailey, C.; Joseph, M.; Libermann, T.A.; Schlossman, R.; Munshi, N.C.; Hideshima, T.; Anderson, K.C. The proteasome inhibitor PS-341 potentiates sensitivity of multiple myeloma cells to conventional chemotherapeutic agents: Therapeutic applications. Blood, 2003, 101(6), 2377-2380. doi: 10.1182/blood-2002-06-1768 PMID: 12424198
  46. Gartel, A.L.; Feliciano, C.; Tyner, A.L. A new method for determining the status of p53 in tumor cell lines of different origin. Oncol. Res., 2003, 13(6), 405-408. doi: 10.3727/096504003108748429 PMID: 12725531
  47. Nylander, K.; Dabelsteen, E.; Hall, P.A. The p53 molecule and its prognostic role in squamous cell carcinomas of the head and neck. J. Oral Pathol. Med., 2000, 29(9), 413-425. doi: 10.1034/j.1600-0714.2000.290901.x
  48. Oltval, Z.N.; Milliman, C.L.; Korsmeyer, S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programed cell death. Cell, 1993, 74(4), 609-619. doi: 10.1016/0092-8674(93)90509-O PMID: 8358790
  49. Hockenbery, D.; Nuñez, G.; Milliman, C.; Schreiber, R.D.; Korsmeyer, S.J. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature, 1990, 348(6299), 334-336. doi: 10.1038/348334a0 PMID: 2250705
  50. Krajewski, S.; Tanaka, S.; Takayama, S.; Schibler, M.J.; Fenton, W.; Reed, J.C. Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res., 1993, 53(19), 4701-4714. PMID: 8402648
  51. de Jong, D.; Prins, F.A.; Mason, D.Y.; Reed, J.C.; van Ommen, G.B.; Kluin, P.M. Subcellular localization of the bcl-2 protein in malignant and normal lymphoid cells. Cancer Res., 1994, 54(1), 256-260. PMID: 8261449
  52. Zhu, W.; Cowie, A.; Wasfy, G.W.; Penn, L.Z.; Leber, B.; Andrews, D.W. Bcl-2 mutants with restricted subcellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J., 1996, 15(16), 4130-4141. doi: 10.1002/j.1460-2075.1996.tb00788.x PMID: 8861942
  53. Hsu, Y.T.; Youle, R.J. Nonionic detergents induce dimerization among members of the Bcl-2 family. J. Biol. Chem., 1997, 272(21), 13829-13834. doi: 10.1074/jbc.272.21.13829 PMID: 9153240
  54. Gross, A.; Jockel, J.; Wei, M.C.; Korsmeyer, S.J. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J., 1998, 17(14), 3878-3885. doi: 10.1093/emboj/17.14.3878 PMID: 9670005
  55. Puthalakath, H.; Huang, D.C.S.; O’Reilly, L.A.; King, S.M.; Strasser, A. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell, 1999, 3(3), 287-296. doi: 10.1016/S1097-2765(00)80456-6 PMID: 10198631
  56. Wolter, K.G.; Hsu, Y.T.; Smith, C.L.; Nechushtan, A.; Xi, X.G.; Youle, R.J. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol., 1997, 139(5), 1281-1292. doi: 10.1083/jcb.139.5.1281 PMID: 9382873
  57. Teijido, O.; Dejean, L. Upregulation of Bcl2 inhibits apoptosis-driven BAX insertion but favors BAX relocalization in mitochondria. FEBS Lett., 2010, 584(15), 3305-3310. doi: 10.1016/j.febslet.2010.07.002 PMID: 20621101
  58. Pavlović V.; Cekić S.; Kocić G.; Sokolović D.; Živković V. Effect of monosodium glutamate on apoptosis and Bcl-2/Bax protein level in rat thymocyte culture. Physiol. Res., 2007, 56(5), 619-626. doi: 10.33549/physiolres.931064 PMID: 17184147
  59. Jiang, H.; Hou, C.; Zhang, S.; Xie, H.; Zhou, W.; Jin, Q.; Cheng, X.; Qian, R.; Zhang, X. Matrine upregulates the cell cycle protein E2F-1 and triggers apoptosis via the mitochondrial pathway in K562 cells. Eur. J. Pharmacol., 2007, 559(2-3), 98-108. doi: 10.1016/j.ejphar.2006.12.017 PMID: 17291488
  60. Jia, H.Y.; Wu, J.X.; Zhu, X.F.; Chen, J.M.; Yang, S.P.; Yan, H.J.; Tan, L.; Zeng, Y.X.; Huang, W. ZD6474 inhibits Src kinase leading to apoptosis of imatinib-resistant K562 cells. Leuk. Res., 2009, 33(11), 1512-1519. doi: 10.1016/j.leukres.2009.03.033 PMID: 19394692
  61. Takahashi, R.; Deveraux, Q.; Tamm, I.; Welsh, K.; Assa-Munt, N.; Salvesen, G.S.; Reed, J.C. A single BIR domain of XIAP sufficient for inhibiting caspases. J. Biol. Chem., 1998, 273(14), 7787-7790. doi: 10.1074/jbc.273.14.7787 PMID: 9525868
  62. Li, F.; Ackermann, E.J.; Bennett, C.F.; Rothermel, A.L.; Plescia, J.; Tognin, S.; Villa, A.; Marchisio, P.C.; Altieri, D.C. Pleiotropic cell-division defects and apoptosis induced by interference with survivin function. Nat. Cell Biol., 1999, 1(8), 461-466. doi: 10.1038/70242 PMID: 10587640
  63. Kawasaki, H.; Altieri, D.C.; Lu, C.D.; Toyoda, M.; Tenjo, T.; Tanigawa, N. Inhibition of apoptosis by survivin predicts shorter survival rates in colorectal cancer. Cancer Res., 1998, 58(22), 5071-5074. PMID: 9823313
  64. Kawasaki, H.; Toyoda, M.; Shinohara, H.; Okuda, J.; Watanabe, I.; Yamamoto, T.; Tanaka, K.; Tenjo, T.; Tanigawa, N. Expression of survivin correlates with apoptosis, proliferation, and angiogenesis during human colorectal tumorigenesis. Cancer, 2001, 91(11), 2026-2032. doi: 10.1002/1097-0142(20010601)91:113.0.CO;2-E PMID: 11391581
  65. Kato, J.; Kuwabara, Y.; Mitani, M.; Shinoda, N.; Sato, A.; Toyama, T.; Mitsui, A.; Nishiwaki, T.; Moriyama, S.; Kudo, J.; Fujii, Y. Expression of survivin in esophageal cancer: Correlation with the prognosis and response to chemotherapy. Int. J. Cancer, 2001, 95(2), 92-95. doi: 10.1002/1097-0215(20010320)95:23.0.CO;2-9 PMID: 11241318
  66. Ikeguchi, M.; Yamaguchi, K.; Kaibara, N. Survivin gene expression positively correlates with proliferative activity of cancer cells in esophageal cancer. Tumour Biol., 2003, 24(1), 40-45. doi: 10.1159/000070659 PMID: 12743425
  67. Ikeguchi, M.; Kaibara, N. survivin messenger RNA expression is a good prognostic biomarker for oesophageal carcinoma. Br. J. Cancer, 2002, 87(8), 883-887. doi: 10.1038/sj.bjc.6600546 PMID: 12373603
  68. Grabowski, P.; Kühnel, T.; Mühr-Wilkenshoff, F.; Heine, B.; Stein, H.; Höpfner, M.; Germer, C.T.; Scherübl, H. Prognostic value of nuclear survivin expression in oesophageal squamous cell carcinoma. Br. J. Cancer, 2003, 88(1), 115-119. doi: 10.1038/sj.bjc.6600696 PMID: 12556969
  69. Kappler, M.; Köhler, T.; Kampf, C.; Diestelkötter, P.; Würl, P.; Schmitz, M.; Bartel, F.; Lautenschläger, C.; Rieber, E.P.; Schmidt, H.; Bache, M.; Taubert, H.; Meye, A. Increased survivin transcript levels: An independent negative predictor of survival in soft tissue sarcoma patients. Int. J. Cancer, 2001, 95(6), 360-363. PMID: 11668517
  70. Würl, P.; Kappler, M.; Meye, A.; Bartel, F.; Köhler, T.; Lautenschläger, C.; Bache, M.; Schmidt, H.; Taubert, H. Co-expression of survivin and TERT and risk of tumour-related death in patients with soft-tissue sarcoma. Lancet, 2002, 359(9310), 943-945. doi: 10.1016/S0140-6736(02)07990-4 PMID: 11918915
  71. Chakravarti, A.; Noll, E.; Black, P.M.; Finkelstein, D.F.; Finkelstein, D.M.; Dyson, N.J.; Loeffler, J.S. Quantitatively determined survivin expression levels are of prognostic value in human gliomas. J. Clin. Oncol., 2002, 20(4), 1063-1068. doi: 10.1200/JCO.2002.20.4.1063 PMID: 11844831
  72. Kleinschmidt-DeMasters, B.K.; Heinz, D.; McCarthy, P.J.; Bobak, J.B.; Lillehei, K.O.; Shroyer, A.L.W.; Shroyer, K.R. Survivin in Glioblastomas. Arch. Pathol. Lab. Med., 2003, 127(7), 826-833. doi: 10.5858/2003-127-826-SIG PMID: 12823036
  73. Lu, C.D.; Altieri, D.C.; Tanigawa, N. Expression of a novel antiapoptosis gene, survivin, correlated with tumor cell apoptosis and p53 accumulation in gastric carcinomas. Cancer Res., 1998, 58(9), 1808-1812. PMID: 9581817
  74. Satoh, K.; Kaneko, K.; Hirota, M.; Masamune, A.; Satoh, A.; Shimosegawa, T. Expression of survivin is correlated with cancer cell apoptosis and is involved in the development of human pancreatic duct cell tumors. Cancer, 2001, 92(2), 271-278. doi: 10.1002/1097-0142(20010715)92:23.0.CO;2-0 PMID: 11466679
  75. Ikeguchi, M.; Ueda, T.; Sakatani, T.; Hirooka, Y.; Kaibara, N. Expression of survivin messenger RNA correlates with poor prognosis in patients with hepatocellular carcinoma. Diagn. Mol. Pathol., 2002, 11(1), 33-40. doi: 10.1097/00019606-200203000-00007 PMID: 11854600
  76. Saitoh, Y.; Yaginuma, Y.; Ishikawa, M. Analysis of Bcl-2, bax and survivin genes in uterine cancer. Int. J. Oncol., 1999, 15(1), 137-141. doi: 10.3892/ijo.15.1.137 PMID: 10375606

Қосымша файлдар

Қосымша файлдар
Әрекет
1. JATS XML

© Bentham Science Publishers, 2024