Proteomic profiling of the 11-dehydrosinulariolide-treated oral carcinoma cells Ca9-22: Effects on the cell apoptosis through mitochondrial-related and ER stress pathway

Journal of Proteomics

Volumn 75, Issue 18, 2012, Pages 5578-5589

  Liu, Chih I ^a   Wang, Robert Yung Liang ^b   Lin, Jen Jie ^c   Su, Jui Hsin ^d   Chiu, Chien Chih ^e   Chen, Jiing Chuan ^a   Chen, Jeff Yi Fu ^e   Wu, Yu Jen ^a  

^a MEIHO UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c NATIONAL PINGTUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^d NATIONAL MUSEUM OF MARINE BIOLOGY AND AQUARIUM   (Taiwan)

^e KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

11 Dehydrosinulariolide; Apoptosis; ER stress; Oral squamous cell carcinoma

Indexed keywords

11 DEHYDROSINULARIOLIDE; 3 HYDROXYACYL COENZYME A DEHYDROGENASE; ALPHA ENOLASE; ANTINEOPLASTIC AGENT; BRAIN SPECIFIC ANGIOGENESIS INHIBITOR 1; CALRETICULIN; CELL PROTEIN; CHAPERONIN CONTAINING TCP1; ENOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE A; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; HEAT SHOCK COGNATE PROTEIN 71; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 BETA; LEUKOCYTE ELASTASE INHIBITOR; LIPOCORTIN 2; OXIDOREDUCTASE; PHOSPHATASE; PROTEIN DISULFIDE ISOMERASE; PROTEIN DISULFIDE ISOMERASE A3; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRROLINE 5 CARBOXYLATE REDUCTASE 1; SERINE THREONINE PROTEIN PHOSPHATASE 2A; UNCLASSIFIED DRUG; VALOSIN CONTAINING PROTEIN; VOLTAGE DEPENDENT ANION CHANNEL 1;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL STRAIN; CELL STRAIN CA9 22; CELL STRESS; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; MITOCHONDRIAL STRESS; MOUTH CARCINOMA; PRIORITY JOURNAL; PROTEOMICS; UPREGULATION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CINNAMATES; DITERPENES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENDOPLASMIC RETICULUM STRESS; HUMANS; MOUTH NEOPLASMS; PROTEOMICS; THIOUREA;

ALCYONACEA; SINULARIA LEPTOCLADOS;

EID: 84866050797     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.07.037     Document Type: Article

References (70)

1. Zygogianni A.G., Kyrgias G., Karakitsos P., Psyrri A., Kouvaris J., Kelekis N., et al. Oral squamous cell cancer: early detection and the role of alcohol and smoking. Head Neck Oncol 2011, 3:2.
2. Ramqvist T., Dalianis T. An epidemic of oropharyngeal squamous cell carcinoma (OSCC) due to human papillomavirus (HPV) infection and aspects of treatment and prevention. Anticancer Res 2011, 31:1515-1519.
3. Murugan A.K., Munirajan A.K., Tsuchida N. Ras oncogenes in oral cancer: the past 20years. Oral Oncol 2012, 48(5):383-392.
4. Chen Y.J., Chang J.T., Liao C.T., Wang H.M., Yen T.C., Chiu C.C., et al. Head and neck cancer in the betel quid chewing area: recent advances in molecular carcinogenesis. Cancer Sci 2008, 99:1507-1514.
5. Olasz L., Orsi E., Marko T., Szalma J. Induction chemotherapy response and recurrence rates in correlation with N0 or N+ stage in oral squamous cell cancer (OSCC). Cancer Metastasis Rev 2010, 29:607-611.
6. Choi S., Myers J.N. Molecular pathogenesis of oral squamous cell carcinoma: implications for therapy. J Dent Res 2008, 87:14-32.
7. Liao C.T., Chang J.T.C., Wang H.M., Ng S.H., Hsueh C., Lee L.Y., et al. Analysis of risk factors of predictive local tumor control in oral cavity cancer. Ann Surg Oncol 2008, 15:915-922.
8. Liao C.T., Kang C.J., Chang J.T.C., Wang H.M., Ng S.H., Hsueh C., et al. Survival of second and multiple primary tumors in patients with oral cavity squamous cell carcinoma in the betel quid chewing area. Oral Oncol 2007, 43:811-819.
9. Monteiro L.S., Diniz-Freitas M., Garcia-Caballero T., Warnakulasuriya S., Forteza J., Fraga M. Combined cytoplasmic and membranous EGFR and p53 overexpression is a poor prognostic marker in early stage oral squamous cell carcinoma. J Oral Pathol Med 2012, 41(7):559-567.
10. Ayala F.R., Rocha R.M., Carvalho K.C., Carvalho A.L., da Cunha I.W., Lourenco S.V., et al. GLUT1 and GLUT3 as potential prognostic markers for oral squamous cell carcinoma. Molecules 2010, 15:2374-2387.
11. Hussain M.S., Fareed S., Ansari S., Rahman M.A., Ahmad I.Z., Saeed M. Current approaches toward production of secondary plant metabolites. J Pharm Bioallied Sci 2012, 4:10-20.
12. Bhatnagar I., Kim S.K. Immense essence of excellence: marine microbial bioactive compounds. Mar Drugs 2010, 8:2673-2701.
13. Lange R., Dietrich D. Environmental risk assessment of pharmaceutical drug substances-conceptual considerations. Toxicol Lett 2002, 131:97-104.
14. Ruggieri G.D. Drugs from the sea. Science (New York, NY) 1976, 194:491.
15. Faulkner D.J. Marine natural products. Nat Prod Rep 2001, 18:1R-49R.
16. Ojika M., Islam M.K., Shintani T., Zhang Y., Okamoto T., Sakagami Y. Three new cytotoxic acylspermidines from the soft coral, Sinularia sp. Biosci Biotechnol Biochem 2003, 67:1410-1412.
17. Ahmed A.F., Shiue R.T., Wang G.H., Dai C.F., Kuo Y.H., Sheu J.H. Five novel norcembranoids from Sinularia leptoclados and S. parva. Tetrahedron 2003, 59:7337-7344.
18. Liu C.I., Chen C.C., Chen J.C., Su J.H., Huang H.H., Chen J.Y., et al. Proteomic analysis of anti-tumor effects of 11-dehydrosinulariolide on CAL-27 cells. Mar Drugs 2011, 9:1254-1272.
19. Lowe S.W., Lin A.W. Apoptosis in cancer. Carcinogenesis 2000, 21:485-495.
20. Su C.C., Su J.H., Lin J.J., Chen C.C., Hwang W.I., Huang H.H., et al. An investigation into the cytotoxic effects of 13-acetoxysarcocrassolide from the soft coral Sarcophyton crassocaule on bladder cancer cells. Mar Drugs 2011, 9:2622-2642.
21. Denicourt C., Dowdy S.F. Targeting apoptotic pathways in cancer cells. Science 2004, 305:1411-1413.
22. Liao P.C., Tan S.K., Lieu C.H., Jung H.K. Involvement of endoplasmic reticulum in paclitaxel-induced apoptosis. J Cell Biochem 2008, 104:1509-1523.
23. Yokouchi M., Hiramatsu N., Hayakawa K., Kasai A., Takano Y., Yao J., et al. Atypical, bidirectional regulation of cadmium-induced apoptosis via distinct signaling of unfolded protein response. Cell Death Differ 2007, 14:1467-1474.
24. Rao R., Ellerby H., Bredesen D. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 2004, 11:372-380.
25. Boyce M., Yuan J. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ 2006, 13:363-373.
26. Wang R., Li K. Host factors in the replication of positive-strand RNA viruses. Chang Gung Med J 2012, 35:14.
27. Moenner M., Pluquet O., Bouchecareilh M., Chevet E. Integrated endoplasmic reticulum stress responses in cancer. Cancer Res 2007, 67:10631-10634.
28. Xu C., Bailly-Maitre B., Reed J.C. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005, 115:2656-2664.
29. Green D.R., Reed J.C. Mitochondria and apoptosis. Science 1998, 281:1309-1312.
30. Nicholson D.W., Thornberry N.A. Life and death decisions. Science 2003, 299:214-215.
31. Hung C.Y., Tsai M.C., Wu Y.P., Wang R.Y. Identification of heat-shock protein 90 beta in Japanese encephalitis virus-induced secretion proteins. J Gen Virol 2011, 92:2803-2809.
32. Wu Y.P., Chang C.M., Hung C.Y., Tsai M.C., Schuyler S.C., Wang R.Y. Japanese encephalitis virus co-opts the ER-stress response protein GRP78 for viral infectivity. Virol J 2011, 8:128.
33. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., et al. Cell migration: integrating signals from front to back. Science 2003, 302:1704-1709.
34. Dean E., Greystoke A., Ranson M., Dive C. Biomarkers of cell death applicable to early clinical trials. Exp Cell Res 2012, 318(11):1252-1259.
35. Johnson J.A., Ogbi M. Targeting the F1Fo ATP synthase: modulation of the body's powerhouse and its implications for human disease. Curr Med Chem 2011, 18:4684-4714.
36. Kumar S.N., Konorev E.A., Aggarwal D., Kalyanaraman B. Analysis of proteome changes in doxorubicin-treated adult rat cardiomyocyte. J Proteomics 2011, 74:683-697.
37. Leanza L., Henry B., Sassi N., Zoratti M., Chandy K.G., Gulbins E., et al. Inhibitors of mitochondrial Kv1.3 channels induce Bax/Bak-independent death of cancer cells. EMBO Mol Med 2012, 4(7):577-593.
38. Ribe E., Serrano-Saiz E., Akpan N., Troy C. Mechanisms of neuronal death in disease: defining the models and the players. Biochem J 2008, 415:165-182.
39. Shankar S., Srivastava R.K. Bax and Bak genes are essential for maximum apoptotic response by curcumin, a polyphenolic compound and cancer chemopreventive agent derived from turmeric, Curcuma longa. Carcinogenesis 2007, 28:1277-1286.
40. Zhou J., Zhang S., Choon-Nam O., Shen H.M. Critical role of pro-apoptotic Bcl-2 family members in andrographolide-induced apoptosis in human cancer cells. Biochem Pharmacol 2006, 72:132-144.
41. Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008, 9:231-241.
42. Wang Y., He Q.Y., Sun R.W.Y., Che C.M., Chiu J.F. Gold (III) porphyrin 1a induced apoptosis by mitochondrial death pathways related to reactive oxygen species. Cancer Res 2005, 65:11553-11564.
43. Germain M., Winstall E., Vodenicharov M., Shah R.G., Salvesen G.S., Poirier G.G. Caspase-3-mediated processing of poly (ADP-ribose) glycohydrolase during apoptosis. J Biol Chem 2001, 276:2935-2942.
44. Davenport E.L., Moore H.E., Dunlop A.S., Sharp S.Y., Workman P., Morgan G.J., et al. Heat shock protein inhibition is associated with activation of the unfolded protein response pathway in myeloma plasma cells. Blood 2007, 110:2641-2649.
45. Hamanaka R.B., Bennett B.S., Cullinan S.B., Diehl J.A. PERK and GCN2 contribute to eIF2α phosphorylation and cell cycle arrest after activation of the unfolded protein response pathway. Mol Biol Cell 2005, 16:5493-5501.
46. Rutkowski D.T., Kaufman R.J. A trip to the ER: coping with stress. Trends Cell Biol 2004, 14:20-28.
47. Li J., Holbrook N.J. Elevated gadd153/chop expression and enhanced c-Jun N-terminal protein kinase activation sensitizes aged cells to ER stress. Exp Gerontol 2004, 39:735-744.
48. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.Y., Holbrook N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 2001, 21:1249-1259.
49. Aceret T.L., Coll J.C., Uchio Y., Sammarco P.W. Antimicrobial activity of the diterpenes flexibilide and sinulariolide derived from Sinularia flexibilis Quoy and Gaimard 1833 (Coelenterata: Alcyonacea, Octocorallia). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1998, 120:121-126.
50. Rashid M.A., Gustafson K.R., Boyd M.R. HIV-inhibitory cembrane derivatives from a Philippines collection of the soft coral lobophytum species1. J Nat Prod 2000, 63:531-533.
51. Ahmed A.F., Hsieh Y.T., Wen Z.H., Wu Y.C., Sheu J.H. Polyoxygenated sterols from the formosan soft coral Sinularia gibberosa. J Nat Prod 2006, 69:1275-1279.
52. Ahmed A.F., Tai S.H., Wu Y.C., Sheu J.H. Sinugrandisterols AD, trihydroxysteroids from the soft coral Sinularia grandilobata. Steroids 2007, 72:368-374.
53. Su J.H., Tseng Y.J., Huang H.H., Ahmed A.F., Lu C.K., Wu Y.C., et al. 9,11-Secosterols from the soft corals Sinularia lochmodes and Sinularia leptoclados. J Nat Prod 2006, 69:850-852.
54. Riedl S.J., Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 2004, 5:897-907.
55. Kuwana T., Newmeyer D.D. Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol 2003, 15:691-699.
56. Borner C. The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol 2003, 39:615-647.
57. Green D.R., Evan G.I. A matter of life and death. Cancer Cell 2002, 1:19-30.
58. Newmeyer D.D., Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 2003, 112:481-490.
59. Liu X., Kim C.N., Yang J., Jemmerson R., Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996, 86:147-157.
60. Zou H., Li Y., Liu X., Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 1999, 274:11549-11556.
61. Zou H., Henzel W.J., Liu X., Lutschg A., Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997, 90:405-413.
62. Lee A.S. GRP78 induction in cancer: therapeutic and prognostic implications. Cancer Res 2007, 67:3496-3499.
63. Michalak M., Groenendyk J., Szabo E., Gold L., Opas M. Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem J 2009, 417:651-666.
64. Michalak M., Robert Parker J., Opas M. Ca2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 2002, 32:269-278.
65. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007, 8:519-529.
66. Luo S., Baumeister P., Yang S., Abcouwer S.F., Lee A.S. Induction of Grp78/BiP by translational block. J Biol Chem 2003, 278:37375-37385.
67. Haze K., Yoshida H., Yanagi H., Yura T., Mori K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 1999, 10:3787-3799.
68. Yoshida H., Haze K., Yanagi H., Yura T., Mori K. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem 1998, 273:33741-33749.
69. Carlson S., Fawcett T., Bartlett J., Bernier M., Holbrook N. Regulation of the C/EBP-related gene gadd153 by glucose deprivation. Mol Cell Biol 1993, 13:4736-4744.
70. Wang X.Z., Lawson B., Brewer J.W., Zinszner H., Sanjay A., Mi L.J., et al. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol 1996, 16:4273-4280.