ApoG2 induces ER stress-dependent apoptosis in gastric cancer cells in vitro and its real-time evaluation by bioluminescence imaging in vivo

Cancer Letters

Volumn 336, Issue 2, 2013, Pages 260-269

  Xin, Jing ^a   Zhan, Yonghua ^a   Liu, Muhan ^a   Hu, Hao ^c   Xia, Limin ^c   Nie, Yongzhan ^c   Wu, Kaichun ^c   Liang, Jimin ^a   Tian, Jie ^a,b  

^a XIDIAN UNIVERSITY   (China)

^b INSTITUTE OF AUTOMATION   (China)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

ApoG2; Bioluminescence imaging; Endoplasmic reticulum stress; Gastric cancer

Indexed keywords

ALANINE AMINOTRANSFERASE; APOGOSSYPOLONE; ASPARTATE AMINOTRANSFERASE; CALCIUM; CREATININE; GOSSYPOL; GOSSYPOL DERIVATIVE; NITROGEN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; UREA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BIOLUMINESCENCE; CANCER CELL CULTURE; CANCER INHIBITION; CELL ASSAY; CELL GROWTH; CELL PROLIFERATION; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FEMALE; HAIR DISEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LETHARGY; LIVER TOXICITY; MOUSE; NEPHROTOXICITY; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; STOMACH CANCER; TUMOR XENOGRAFT; UREA NITROGEN BLOOD LEVEL; WEIGHT REDUCTION;

ANIMALS; APOPTOSIS; CALCIUM; CELL LINE, TUMOR; CELL SURVIVAL; ENDOPLASMIC RETICULUM STRESS; FEMALE; GOSSYPOL; HUMANS; LUMINESCENT MEASUREMENTS; MICE; MICE, NUDE; RANDOM ALLOCATION; REACTIVE OXYGEN SPECIES; STOMACH NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MURINAE;

EID: 84879781190     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.03.019     Document Type: Article

References (54)

1. Parkin D.M. International variation. Oncogene 2004, 23:6329-6340.
2. Jemal A., Bray F., Center M.M., Ferlay J., Ward E., Forman D. Global cancer statistics. CA: Cancer. J. Clin. 2011, 61:69-90.
3. Yang L. Incidence and mortality of gastric cancer in China. World J. Gastroenterol. 2006, 12:17-20.
4. Morse M.A., Stoner G.D. Cancer chemoprevention: principles and prospects. Carcinogenesis 1993, 14:1737-1746.
5. Macdonald J.S. Clinical overview: adjuvant therapy of gastrointestinal cancer. Cancer Chemother. Pharmacol. 2004, 54(Suppl. 1):S4-S11.
6. Zhang D., Fan D. Multidrug resistance in gastric cancer: recent research advances and ongoing therapeutic challenges. Expert Rev. Anticancer Ther. 2007, 7:1369-1378.
7. Zhu H., Xia L., Zhang Y., Wang H., Xu W., Hu H., Wang J., Xin J., Gang Y., Sha S., Xu B., Fan D., Nie Y., Wu K. Activating transcription factor 4 confers a multidrug resistance phenotype to gastric cancer cells through transactivation of SIRT1 expression. PLoS ONE 2012, 7:e31431.
8. Sun Y., Peng Z.L. Programmed cell death and cancer. Postgrad. Med. J. 2009, 85:134-140.
9. Petros A.M., Olejniczak E.T., Fesik S.W. Structural biology of the Bcl-2 family of proteins. Biochim. Biophys. Acta 2004, 1644:83-94.
10. Reed J.C., Zha H., Aime-Sempe C., Takayama S., Wang H.G. Structure-function analysis of Bcl-2 family proteins. Regulators of programmed cell death. Adv. Exp. Med. Biol. 1996, 406:99-112.
11. Marzo I., Naval J. Bcl-2 family members as molecular targets in cancer therapy. Biochem. Pharmacol. 2008, 76:939-946.
12. Huang Z. Small molecule inhibitors of Bcl-2 function: modulators of apoptosis and promising anticancer agents. Curr. Opin. Drug. Discov. Devel. 2000, 3:565-574.
13. Wang S., Yang D., Lippman M.E. Targeting Bcl-2 and Bcl-XL with nonpeptidic small-molecule antagonists. Semin. Oncol. 2003, 30:133-142.
14. Al-Katib A.M., Sun Y., Goustin A.S., Azmi A.S., Chen B., Aboukameel A., Mohammad R.M. SMI of Bcl-2 TW-37 is active across a spectrum of B-cell tumors irrespective of their proliferative and differentiation status. J. Hematol. Oncol. 2009, 2:8.
15. Azmi A.S., Mohammad R.M. Non-peptidic small molecule inhibitors against Bcl-2 for cancer therapy. J. Cell. Physiol. 2009, 218:13-21.
16. Bodur C., Basaga H. Bcl-2 inhibitors: emerging drugs in cancer therapy. Curr. Med. Chem. 2012, 19:1804-1820.
17. Naik H., Petrylak D., Yagoda A., Lehr J., Akhtar A., Pienta K. Preclinical studies of gossypol in prostate carcinoma. Int. J. Oncol. 1995, 6:209-213.
18. Bushunow P., Reidenberg M.M., Wasenko J., Winfield J., Lorenzo B., Lemke S., Himpler B., Corona R., Coyle T. Gossypol treatment of recurrent adult malignant gliomas. J. Neurooncol. 1999, 43:79-86.
19. Meng Y., Tang W., Dai Y., Wu X., Liu M., Ji Q., Ji M., Pienta K., Lawrence T., Xu L. Natural BH3 mimetic (-)-gossypol chemosensitizes human prostate cancer via Bcl-xL inhibition accompanied by increase of Puma and Noxa. Mol. Cancer Ther. 2008, 7:2192-2202.
20. Balakrishnan K., Wierda W.G., Keating M.J., Gandhi V. Gossypol, a BH3 mimetic, induces apoptosis in chronic lymphocytic leukemia cells. Blood 2008, 112:1971-1980.
21. Gunassekaran G.R., Priya D.K., Gayathri R., Sakthisekaran D. In vitro and in vivo studies on antitumor effects of gossypol on human stomach adenocarcinoma (AGS) cell line and MNNG induced experimental gastric cancer. Biochem. Biophys. Res. Commun. 2011, 411:661-666.
22. Shelley M.D., Hartley L., Groundwater P.W., Fish R.G. Structure-activity studies on gossypol in tumor cell lines. Anticancer Drugs 2000, 11:209-216.
23. Hu Z.Y., Zhu X.F., Zhong Z.D., Sun J., Wang J., Yang D., Zeng Y.X. ApoG2, a novel inhibitor of antiapoptotic Bcl-2 family proteins, induces apoptosis and suppresses tumor growth in nasopharyngeal carcinoma xenografts. Int. J. Cancer 2008, 123:2418-2429.
24. Hu Z.Y., Sun J., Zhu X.F., Yang D., Zeng Y.X. ApoG2 induces cell cycle arrest of nasopharyngeal carcinoma cells by suppressing the c-Myc signaling pathway. J. Transl. Med. 2009, 7:74.
25. Zhang X.Q., Huang X.F., Hu X.B., Zhan Y.H., An Q.X., Yang S.M., Xia A.J., Yi J., Chen R., Mu S.J., Wu D.C. Apogossypolone, a novel inhibitor of antiapoptotic Bcl-2 family proteins, induces autophagy of PC-3 and LNCaP prostate cancer cells in vitro. Asian. J. Androl. 2010, 12:697-708.
26. Sun Y., Wu J., Aboukameel A., Banerjee S., Arnold A.A., Chen J., Nikolovska-Coleska Z., Lin Y., Ling X., Yang D., Wang S., Al-Katib A., Mohammad R.M. Apogossypolone, a nonpeptidic small molecule inhibitor targeting Bcl-2 family proteins, effectively inhibits growth of diffuse large cell lymphoma cells in vitro and in vivo. Cancer Biol. Ther. 2008, 7:1418-1426.
27. Sun J., Li Z.M., Hu Z.Y., Zeng Z.L., Yang D.J., Jiang W.Q. Apogossypolone inhibits cell growth by inducing cell cycle arrest in U937 cells. Oncol. Rep. 2009, 22:193-198.
28. Arnold A.A., Aboukameel A., Chen J., Yang D., Wang S., Al-Katib A., Mohammad R.M. Preclinical studies of apogossypol one: a new nonpeptidic pan small-molecule inhibitor of Bcl-2, Bcl-XL and Mcl-1 proteins in follicular small cleaved cell lymphoma model. Mol. Cancer 2008, 7:20.
29. Banerjee S., Choi M., Aboukameel A., Wang Z., Mohammad M., Chen J., Yang D., Sarkar F.H., Mohammad R.M. Preclinical studies of apogossypolone, a novel pan inhibitor of bcl-2 and mcl-1, synergistically potentiates cytotoxic effect of gemcitabine in pancreatic cancer cells. Pancreas 2010, 39:323-331.
30. Mi J.X., Wang G.F., Wang H.B., Sun X.Q., Ni X.Y., Zhang X.W., Tang J.M., Yang D.J. Synergistic antitumoral activity and induction of apoptosis by novel pan Bcl-2 proteins inhibitor apogossypolone with adriamycin in human hepatocellular carcinoma. Acta Pharmacol. Sin. 2008, 29:1467-1477.
31. Jenkins D.E., Oei Y., Hornig Y.S., Yu S.F., Dusich J., Purchio T., Contag P.R. Bioluminescent imaging (BLI) to improve and refine traditional murine models of tumor growth and metastasis. Clin. Exp. Metastasis. 2003, 20:733-744.
32. Hollingshead M.G., Bonomi C.A., Borgel S.D., Carter J.P., Shoemaker R., Melillo G., Sausville E.A. A potential role for imaging technology in anticancer efficacy evaluations. Eur. J. Cancer 2004, 40:890-898.
33. Contag P.R. Whole-animal cellular and molecular imaging to accelerate drug development. Drug Discov. Today 2002, 7:555-562.
34. Blasberg R.G., Gelovani-Tjuvajev J. In vivo molecular-genetic imaging. J. Cell. Biochem. Suppl. 2002, 39:172-183.
35. Sancey L., Dufort S., Josserand V., Keramidas M., Righini C., Rome C., Faure A.C., Foillard S., Roux S., Boturyn D., Tillement O., Koenig A., Boutet J., Rizo P., Dumy P., Coll J.L. Drug development in oncology assisted by noninvasive optical imaging. Int. J. Pharm. 2009, 379:309-316.
36. Xu H., Rice B.W. In-vivo fluorescence imaging with a multivariate curve resolution spectral unmixing technique. J. Biomed. Opt. 2009, 14:064011.
37. Liu J., Wang Y., Qu X., Li X., Ma X., Han R., Hu Z., Chen X., Sun D., Zhang R., Chen D., Liang J., Cao F., Tian J. In vivo quantitative bioluminescence tomography using heterogeneous and homogeneous mouse models. Opt. Express 2010, 18:13102-13113.
38. Zhan Y.H., Jia G.F. A novel synthesis method of apogossypolone and its antitumor activity. Lett. Dru. Des. Discov. 2009, 6:129-138.
39. Zhan Y.H., Jia G.F., Wu D.C., Xu Y.Q., Xu L. Design and synthesis of a gossypol derivative with improved antitumor activities. Arch. Pharm. 2009, 342:223-229.
40. Lehr H.A., Mankoff D.A., Corwin D., Santeusanio G., Gown A.M. Application of photoshop-based image analysis to quantification of hormone receptor expression in breast cancer. J. Histochem. Cytochem. 1997, 45:1559-1565.
41. Hu Z.Y., Wang J., Cheng G., Zhu X.F., Huang P., Yang D., Zeng Y.X. Apogossypolone targets mitochondria and light enhances its anticancer activity by stimulating generation of singlet oxygen and reactive oxygen species. Chin. J. Cancer 2011, 30:41-53.
42. Zubair H., Khan H.Y., Ullah M.F., Ahmad A., Wu D., Hadi S.M. Apogossypolone, derivative of gossypol, mobilizes endogenous copper in human peripheral lymphocytes leading to oxidative DNA breakage. Eur. J. Pharm. Sci. 2012, 47:280-286.
43. Mu D., Zhang W., Chu D., Liu T., Xie Y., Fu E., Jin F. The role of calcium, P38 MAPK in dihydroartemisinin-induced apoptosis of lung cancer PC-14 cells. Cancer Chemother. Pharmacol. 2008, 61:639-645.
44. Gao X., Luo Z., Xiang T., Wang K., Li J., Wang P. Dihydroartemisinin induces endoplasmic reticulum stress-mediated apoptosis in HepG2 human hepatoma cells. Tumori 2011, 97:771-780.
45. Zhang D., Fan D. New insights into the mechanisms of gastric cancer multidrug resistance and future perspectives. Future Oncol. 2010, 6:527-537.
46. Nambiar D., Prajapati V., Agarwal R., Singh R.P. In vitro and in vivo anticancer efficacy of silibinin against human pancreatic cancer BxPC-3 and PANC-1 cells. Cancer Lett. 2012.
47. Kitada S., Kress C.L., Krajewska M., Jia L., Pellecchia M., Reed J.C. Bcl-2 antagonist apogossypol (NSC736630) displays single-agent activity in Bcl-2-transgenic mice and has superior efficacy with less toxicity compared with gossypol (NSC19048). Blood 2008, 111:3211-3219.
48. Vermeulen K., Van Bockstaele D.R., Berneman Z.N. Apoptosis: mechanisms and relevance in cancer. Ann. Hematol. 2005, 84:627-639.
49. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell. Biol. 2007, 8:519-529.
50. Xu C., Bailly-Maitre B., Reed J.C. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 2005, 115:2656-2664.
51. Szegezdi E., Logue S.E., Gorman A.M., Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO. Rep. 2006, 7:880-885.
52. Pyrko P., Kardosh A., Liu Y.T., Soriano N., Xiong W., Chow R.H., Uddin J., Petasis N.A., Mircheff A.K., Farley R.A., Louie S.G., Chen T.C., Schönthal A.H. Calcium-activated endoplasmic reticulum stress as a major component of tumor cell death induced by 2,5-dimethyl-celecoxib, a non-coxib analogue of celecoxib. Mol. Cancer. Ther. 2007, 6:1262-1275.
53. Xu Q., Ohara N., Liu J., Nakabayashi K., DeManno D., Chwalisz K., Yoshida S., Maruo T. Selective progesterone receptor modulator asoprisnil induces endoplasmic reticulum stress in cultured human uterine leiomyoma cells. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E1002-E1011.
54. Crespo I., San-Miguel B., Prause C., Marroni N., Cuevas M.J., Gonzalez-Gallego J., Tunon M.J. Glutamine treatment attenuates endoplasmic reticulum stress and apoptosis in TNBS-induced colitis. PLoS ONE 2012, 7:e50407.