Immunomodulatory proteins FIP-gts and chloroquine induce caspase-independent cell death via autophagy for resensitizing cisplatin-resistant urothelial cancer cells

Phytomedicine

Volumn 23, Issue 13, 2016, Pages 1566-1573

  Hsin, I Lun ^a,b   Wang, Shao Chuan ^a,c   Li, Jian Ri ^a,d   Ciou, Tsai Chun ^a   Wu, Chih Hsien ^a   Wu, Hung Ming ^b,e   Ko, Jiunn Liang ^a,c  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

^c CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^e CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Abundant autophagosome accumulation stress; Autophagy; Caspase independent cell death; Chloroquine; Cisplatin resistant urothelial cells; FIP gts

Indexed keywords

ACETYLCYSTEINE; CHLOROQUINE; CISPLATIN; CYTOTOXIC AGENT; FUNGAL EXTRACT; FUNGAL IMMUNOMODULATORY PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BENZYLOXYCARBONYLVALYL-ALANYL-ASPARTYL FLUOROMETHYL KETONE; CASPASE; FUNGAL PROTEIN; IMMUNOLOGIC FACTOR; PEPTIDE CHLOROMETHYL KETONE;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER RESISTANCE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; FLOW CYTOMETRY; GANODERMA TSUGAE; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; TRANSITIONAL CELL CARCINOMA; APOPTOSIS; CELL CYCLE; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; DRUG RESISTANCE; GANODERMA; HUMAN; METABOLISM; PATHOLOGY; TUMOR CELL LINE; UROLOGIC NEOPLASMS;

AMINO ACID CHLOROMETHYL KETONES; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; AUTOPHAGY; CASPASES; CELL CYCLE; CELL LINE, TUMOR; CELL SURVIVAL; CHLOROQUINE; CISPLATIN; DRUG RESISTANCE, NEOPLASM; FUNGAL PROTEINS; GANODERMA; HUMANS; IMMUNOLOGIC FACTORS; MEMBRANE POTENTIAL, MITOCHONDRIAL; UROLOGIC NEOPLASMS;

EID: 84989298182     PISSN: 09447113     EISSN: 1618095X     Source Type: Journal    
DOI: 10.1016/j.phymed.2016.09.003     Document Type: Article

References (45)

1. Artus, C., Boujrad, H., Bouharrour, A., Brunelle, M.N., Hoos, S., Yuste, V.J., Lenormand, P., Rousselle, J.C., Namane, A., England, P., Lorenzo, H.K., Susin, S.A., AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX. EMBO J. 29 (2010), 1585–1599.
2. Bellmunt, J., von der Maase, H., Mead, G.M., Skoneczna, I., De Santis, M., Daugaard, G., Boehle, A., Chevreau, C., Paz-Ares, L., Laufman, L.R., Winquist, E., Raghavan, D., Marreaud, S., Collette, S., Sylvester, R., de Wit, R., Randomized phase III study comparing paclitaxel/cisplatin/gemcitabine and gemcitabine/cisplatin in patients with locally advanced or metastatic urothelial cancer without prior systemic therapy: EORTC Intergroup Study 30987. J. Clin. Oncol. 30 (2012), 1107–1113.
3. Ben-Zvi, I., Kivity, S., Langevitz, P., Shoenfeld, Y., Hydroxychloroquine: from malaria to autoimmunity. Clin. Rev. Allergy Immunol. 42 (2012), 145–153.
4. Bonapace, L., Bornhauser, B.C., Schmitz, M., Cario, G., Ziegler, U., Niggli, F.K., Schafer, B.W., Schrappe, M., Stanulla, M., Bourquin, J.P., Induction of autophagy-dependent necroptosis is required for childhood acute lymphoblastic leukemia cells to overcome glucocorticoid resistance. J. Clin. Invest. 120 (2010), 1310–1323.
5. Changou, C.A., Chen, Y.R., Xing, L., Yen, Y., Chuang, F.Y., Cheng, R.H., Bold, R.J., Ann, D.K., Kung, H.J., Arginine starvation-associated atypical cellular death involves mitochondrial dysfunction, nuclear DNA leakage, and chromatin autophagy. Proc. Natl. Acad. Sci. U S A 111 (2014), 14147–14152.
6. Chen, H.A., Su, C.M., Hsieh, H.Y., Tung, C.L., Hsu, C.D., Wang, Y.H., Shen, C.H., Clinical significance of survivin expression in patients with urothelial carcinoma. Dis Markers 2014, 2014, 574985.
7. Choi, Y.J., Lee, S.H., Lee, J.L., Ahn, J.H., Lee, K.H., You, D., Hong, B., Hong, J.H., Ahn, H., Phase II study of pemetrexed in combination with cisplatin in patients with advanced urothelial cancer: the PECULIAR study (KCSG 10-17). British J. Cancer 112 (2015), 260–265.
8. Czabotar, P.E., Lessene, G., Strasser, A., Adams, J.M., Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat. Rev. Mol. Cell Biol. 15 (2014), 49–63.
9. Drayton, R.M., Catto, J.W., Molecular mechanisms of cisplatin resistance in bladder cancer. Exp. Rev. Anticancer Therapy 12 (2012), 271–281.
10. El Enshasy, H.A., Hatti-Kaul, R., Mushroom immunomodulators: unique molecules with unlimited applications. Trends Biotechnol. 31 (2013), 668–677.
11. Fuessel, S., Herrmann, J., Ning, S., Kotzsch, M., Kraemer, K., Schmidt, U., Hakenberg, O.W., Wirth, M.P., Meye, A., Chemosensitization of bladder cancer cells by survivin-directed antisense oligodeoxynucleotides and siRNA. Cancer Lett. 232 (2006), 243–254.
12. Galluzzi, L., Senovilla, L., Vitale, I., Michels, J., Martins, I., Kepp, O., Castedo, M., Kroemer, G., Molecular mechanisms of cisplatin resistance. Oncogene 31 (2012), 1869–1883.
13. Hour, T.C., Lai, Y.L., Kuan, C.I., Chou, C.K., Wang, J.M., Tu, H.Y., Hu, H.T., Lin, C.S., Wu, W.J., Pu, Y.S., Sterneck, E., Huang, A.M., Transcriptional up-regulation of SOD1 by CEBPD: a potential target for cisplatin resistant human urothelial carcinoma cells. Biochem. Pharmacol. 80 (2010), 325–334.
14. Hsin, I.L., Ou, C.C., Wu, M.F., Jan, M.S., Hsiao, Y.M., Lin, C.H., Ko, J.L., GMI, an Immunomodulatory protein from ganoderma microsporum, potentiates cisplatin-induced apoptosis via autophagy in lung cancer cells. Molecul. Pharm 12:5 (2015), 1534–1543.
15. Hsin, I.L., Ou, C.C., Wu, T.C., Jan, M.S., Wu, M.F., Chiu, L.Y., Lue, K.H., Ko, J.L., GMI, an immunomodulatory protein from Ganoderma microsporum, induces autophagy in non-small cell lung cancer cells. Autophagy 7 (2011), 873–882.
16. Hsin, I.L., Sheu, G.T., Jan, M.S., Sun, H.L., Wu, T.C., Chiu, L.Y., Lue, K.H., Ko, J.L., Inhibition of lysosome degradation on autophagosome formation and responses to GMI, an immunomodulatory protein from Ganoderma microsporum. British J. Pharmacol. 167 (2012), 1287–1300.
17. Jeon, C., Kim, M., Kwak, C., Kim, H.H., Ku, J.H., Prognostic role of survivin in bladder cancer: a systematic review and meta-analysis. PloS One, 8, 2013, e76719.
18. Kang, Y.H., Yi, M.J., Kim, M.J., Park, M.T., Bae, S., Kang, C.M., Cho, C.K., Park, I.C., Park, M.J., Rhee, C.H., Hong, S.I., Chung, H.Y., Lee, Y.S., Lee, S.J., Caspase-independent cell death by arsenic trioxide in human cervical cancer cells: reactive oxygen species-mediated poly(ADP-ribose) polymerase-1 activation signals apoptosis-inducing factor release from mitochondria. Cancer Res. 64 (2004), 8960–8967.
19. Kawane, K., Motani, K., Nagata, S., DNA degradation and its defects. Cold Spring Harb Perspect. Biol., 6, 2014.
20. Kitanaka, C., Kuchino, Y., Caspase-independent programmed cell death with necrotic morphology. Cell Death Differ. 6 (1999), 508–515.
21. Klionsky, D.J., Abdelmohsen, K., Abe, A., Abedin, M.J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C.M., Adams, P.D., Adeli, K., and further … coauthors, Guidelines for the use and interpretation of assays for monitoring autophagy. (3rd edition) Autophagy 12 (2016), 1–222.
22. Knowles, M.A., Hurst, C.D., Molecular biology of bladder cancer: new insights into pathogenesis and clinical diversity. Nature reviews. Cancer 15 (2015), 25–41.
23. Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E.S., Baehrecke, E.H., Blagosklonny, M.V., El-Deiry, W.S., Golstein, P., Green, D.R., Hengartner, M., Knight, R.A., Kumar, S., Lipton, S.A., Malorni, W., Nunez, G., Peter, M.E., Tschopp, J., Yuan, J., Piacentini, M., Zhivotovsky, B., Melino, G., Nomenclature Committee on Cell, D., Classification of cell death: recommendations of the nomenclature committee on cell death 2009. Cell Death Differ. 16 (2009), 3–11.
24. Kroemer, G., Martin, S.J., Caspase-independent cell death. Nat. Med. 11 (2005), 725–730.
25. Kung, H.J., Changou, C.A., Li, C.F., Ann, D.K., Chromatophagy: autophagy goes nuclear and captures broken chromatin during arginine-starvation. Autophagy 11 (2015), 419–421.
26. Li, J.R., Cheng, C.L., Yang, W.J., Yang, C.R., Ou, Y.C., Wu, M.J., Ko, J.L., FIP-gts potentiate autophagic cell death against cisplatin-resistant urothelial cancer cells. Anticancer Res. 34 (2014), 2973–2983.
27. Liao, C.H., Hsiao, Y.M., Hsu, C.P., Lin, M.Y., Wang, J.C., Huang, Y.L., Ko, J.L., Transcriptionally mediated inhibition of telomerase of fungal immunomodulatory protein from Ganoderma tsugae in A549 human lung adenocarcinoma cell line. Mol. Carcinog. 45 (2006), 220–229.
28. Liao, C.H., Hsiao, Y.M., Lin, C.H., Yeh, C.S., Wang, J.C., Ni, C.H., Hsu, C.P., Ko, J.L., Induction of premature senescence in human lung cancer by fungal immunomodulatory protein from Ganoderma tsugae. Food Chem. Toxicol. 46 (2008), 1851–1859.
29. Liao, C.H., Hsiao, Y.M., Sheu, G.T., Chang, J.T., Wang, P.H., Wu, M.F., Shieh, G.J., Hsu, C.P., Ko, J.L., Nuclear translocation of telomerase reverse transcriptase and calcium signaling in repression of telomerase activity in human lung cancer cells by fungal immunomodulatory protein from Ganoderma tsugae. Biochem. Pharm. 74 (2007), 1541–1554.
30. Lin, C.H., Hsiao, Y.M., Ou, C.C., Lin, Y.W., Chiu, Y.L., Lue, K.H., Chang, J.G., Ko, J.L., GMI, a Ganoderma immunomodulatory protein, down-regulates tumor necrosis factor alpha-induced expression of matrix metalloproteinase 9 via NF-kappaB pathway in human alveolar epithelial A549 cells. J. Agric. Food Chem. 58 (2010), 12014–12021.
31. Lin, C.H., Sheu, G.T., Lin, Y.W., Yeh, C.S., Huang, Y.H., Lai, Y.C., Chang, J.G., Ko, J.L., A new immunomodulatory protein from Ganoderma microsporum inhibits epidermal growth factor mediated migration and invasion in A549 lung cancer cells. Proc. Biochem. 45 (2010), 1537–1542.
32. Marino, G., Niso-Santano, M., Baehrecke, E.H., Kroemer, G., Self-consumption: the interplay of autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 15 (2014), 81–94.
33. Marullo, R., Werner, E., Degtyareva, N., Moore, B., Altavilla, G., Ramalingam, S.S., Doetsch, P.W., Cisplatin induces a mitochondrial-ROS response that contributes to cytotoxicity depending on mitochondrial redox status and bioenergetic functions. PloS One, 8, 2013, e81162.
34. Norbury, C.J., Zhivotovsky, B., DNA damage-induced apoptosis. Oncogene 23 (2004), 2797–2808.
35. Shen, H.M., Codogno, P., Autophagic cell death: Loch Ness monster or endangered species?. Autophagy 7 (2011), 457–465.
36. Tait, S.W., Green, D.R., Caspase-independent cell death: leaving the set without the final cut. Oncogene 27 (2008), 6452–6461.
37. Underwood, B.R., Imarisio, S., Fleming, A., Rose, C., Krishna, G., Heard, P., Quick, M., Korolchuk, V.I., Renna, M., Sarkar, S., Garcia-Arencibia, M., O'Kane, C.J., Murphy, M.P., Rubinsztein, D.C., Antioxidants can inhibit basal autophagy and enhance neurodegeneration in models of polyglutamine disease. Hum. Mol. Genet. 19 (2010), 3413–3429.
38. Vanden Berghe, T., Linkermann, A., Jouan-Lanhouet, S., Walczak, H., Vandenabeele, P., Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat. Rev. Mol. Cell Biol. 15 (2014), 135–147.
39. Wu, C.H., Tang, S.C., Wang, P.H., Lee, H., Ko, J.L., Nickel-induced epithelial-mesenchymal transition by reactive oxygen species generation and E-cadherin promoter hypermethylation. J. Biol. Chem. 287 (2012), 25292–25302.
40. Wu, C.T., Lin, T.Y., Hsu, H.Y., Sheu, F., Ho, C.M., Chen, E.I., Ling Zhi-8 mediates p53-dependent growth arrest of lung cancer cells proliferation via the ribosomal protein S7-MDM2-p53 pathway. Carcinogenesis 32 (2011), 1890–1896.
41. Wu, J.R., Hu, C.T., You, R.I., Ma, P.L., Pan, S.M., Lee, M.C., Wu, W.S., Preclinical trials for prevention of tumor progression of hepatocellular carcinoma by LZ-8 targeting c-Met dependent and independent pathways. PLoS One, 10, 2015, e0114495.
42. Xu, Y., Kim, S.O., Li, Y., Han, J., Autophagy contributes to caspase-independent macrophage cell death. J. Biol. Chem. 281 (2006), 19179–19187.
43. Yang, S., Wang, X., Contino, G., Liesa, M., Sahin, E., Ying, H., Bause, A., Li, Y., Stommel, J.M., Dell'antonio, G., Mautner, J., Tonon, G., Haigis, M., Shirihai, O.S., Doglioni, C., Bardeesy, N., Kimmelman, A.C., Pancreatic cancers require autophagy for tumor growth. Genes Dev 25 (2011), 717–729.
44. Yu, H.M., Wang, T.C., Mechanism of cisplatin resistance in human urothelial carcinoma cells. Food Chem. Toxicol. 50 (2012), 1226–1237.
45. Zhang, N., Chen, Y., Jiang, R., Li, E., Chen, X., Xi, Z., Guo, Y., Liu, X., Zhou, Y., Che, Y., Jiang, X., PARP and RIP 1 are required for autophagy induced by 11′-deoxyverticillin A, which precedes caspase-dependent apoptosis. Autophagy 7 (2011), 598–612.