A quantitative chemical proteomics approach to profile the specific cellular targets of andrographolide, a promising anticancer agent that suppresses tumor metastasis

Molecular and Cellular Proteomics

Volumn 13, Issue 3, 2014, Pages 876-886

  Wang, Jigang ^a   Tan, Xing Fei ^a   Nguyen, Van Sang ^a   Yang, Peng ^b   Zhou, Jing ^c   Gao, Mingming ^d   Li, Zhengjun ^a   Lim, Teck Kwang ^a   He, Yingke ^e   Ong, Chye Sun ^f   Lay, Yifei ^a   Zhang, Jianbin ^c   Zhu, Guili ^f   Lai, Siew Li ^g   Ghosh, Dipanjana ^a   Mok, Yu Keung ^a   Shen, Han Ming ^c   Lin, Qingsong ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d UNIVERSITY OF MARYLAND   (United States)

^e DUKE NUS MEDICAL SCHOOL   (Singapore)

^f SINGAPORE POLYTECHNIC   (Singapore)

^g UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGRAPHOLIDE;

AFFINITY CHROMATOGRAPHY; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL ASSAY; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; NEOPLASM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; PROTEOMICS; TARGET CELL;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; CYSTEINE; DITERPENES; HUMANS; MOLECULAR PROBES; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NF-KAPPA B; PROTEIN BINDING; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION;

EID: 84895556422     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.029793     Document Type: Article

References (55)

1. Harding, M. W., Galat, A., Uehling, D. E., and Schreiber, S. L. (1989) A receptor for the immunosupressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature 341, 758-760
2. Brown, E. J., Albers, M. W., Shin, T. B., Ichikawa, K., Keith, C. T., Lane, W. S., and Schreiber, S. L. (1994) A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 369, 756-758
3. Speers, A. E., Adam, G. C., and Cravatt, B. F. (2003) Activity-based protein profiling in vivo using a copper(i)-catalyzed azide-alkyne [3 + 2] cycloaddition. J. Am. Chem. Soc. 125, 4686-4687
4. Ovaa, H., Van Swieten, P. F., Kessler, B. M., Leeuwenburgh, M. A., Fiebiger, E., Van den Nieuwendijk, A. M. C. H., Galardy, P. J., Van der Marel, G. A., Ploegh, H. L., and Overkleeft, H. S. (2003) Chemistry in living cells: detection of active proteasomes by a two-step labeling strategy. Angew. Chem. Int. Ed. 115, 3754-3757
5. Evans, M. J., and Cravatt, B. F. (2006) Mechanism-based profiling of enzyme families. Chem. Rev. 106, 3279-3301
6. Nomura, D. K., Dix, M. M., and Cravatt, B. F. (2010) Activity-based protein profiling for biochemical pathway discovery in cancer. Nat. Rev. Cancer 10, 630-638
7. Paulick, M., and Bogyo, M. (2008) Application of activity-based probes to the study of enzymes involved in cancer progression. Curr. Opin. Genet. Dev. 18, 97-106
8. Fonović, M., and Bogyo, M. (2008) Activity based probes as a tool for functional proteomic analysis of proteases. Expert Rev. Proteomics 5, 721-730
9. Böttcher, T., Pitscheider, M., and Sieber, S. A. (2010) Natural products and their biological targets: proteomic and metabolomic labeling strategies. Angew. Chem. Int. Ed. 49, 2680-2698
10. Yang, P.-Y., Liu, K., Ngai, M. H., Lear, M. J., Wenk, M. R., and Yao, S. Q. (2010) Activity-based proteome profiling of potential cellular targets of Orlistat - an FDA-approved drug with anti-tumor activities. J. Am. Chem. Soc. 132, 656-666
11. Liu, C.-X., Yin, Q.-Q., Zhou, H.-C., Wu, Y.-L., Pu, J.-X., Xia, L., Liu, W., Huang, X., Jiang, T., Wu, M.-X., He, L.-C., Zhao, Y.-X., Wang, X.-L., Xiao, W.-L., Chen, H.-Z., Zhao, Q., Zhou, A.-W., Wang, L.-S., Sun, H.-D., and Chen, G.-Q. (2012) Adenanthin targets peroxiredoxin I and II to induce differentiation of leukemic cells. Nat. Chem. Biol. 8, 486-493
12. Shi, H., Zhang, C.-J., Chen, G. Y. J., and Yao, S. Q. (2012) Cell-based proteome profiling of potential dasatinib targets by use of affinity-based probes. J. Am. Chem. Soc. 134, 3001-3014
13. Willems, L. I., Van der Linden, W. A., Li, N., Li, K.-Y., Liu, N., Hoogendoorn, S., Van der Marel, G. A., Florea, B. I., and Overkleeft, H. S. (2011) Bioorthogonal chemistry: applications in activity-based protein profiling. Acc. Chem. Res. 44, 718-729
14. Böttcher, T., and Sieber, S. A. (2008) Beta-lactones as specific inhibitors of ClpP attenuate the production of extracellular virulence factors of Staphylococcus aureus. J. Am. Chem. Soc. 130, 14400-14401
15. Gersch, M., Kreuzer, J., and Sieber, S. A. (2012) Electrophilic natural products and their biological targets. Nat. Prod. Rep. 29, 659-682
16. Bantscheff, M., Eberhard, D., Abraham, Y., Bastuck, S., Boesche, M., Hobson, S., Mathieson, T., Perrin, J., Raida, M., Rau, C., Reader, V., Sweetman, G., Bauer, A., Bouwmeester, T., Hopf, C., Kruse, U., Neubauer, G., Ramsden, N., Rick, J., Kuster, B., and Drewes, G. (2007) Quantitative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat. Biotechnol. 25, 1035-1044
17. Sharma, K., Weber, C., Bairlein, M., Greff, Z., Ké ri, G., Cox, J., Olsen, J. V., and Daub, H. (2009) Proteomics strategy for quantitative protein interaction profiling in cell extracts. Nat. Methods 6, 741-744
18. Ong, S., Schenone, M., Margolin, A. A., Li, X., Do, K., Doud, M. K., Mani, D. R., Kuai, L., Wang, X., Wood, J. L., Tolliday, N. J., Koehler, A. N., Marcaurelle, L. A., Golub, T. R., Gould, R. J., Schreiber, S. L., and Carr, S. A. (2009) Identifying the proteins to which small-molecule probes and drugs bind in cells. Proc. Natl. Acad. Sci. U.S.A. 106, 4617-4622
19. Li, X., Foley, E. A., Molloy, K. R., Li, Y., Chait, B. T., and Kapoor, T. M. (2012) Quantitative chemical proteomics approach to identify post-translational modification-mediated protein-protein interactions. J. Am. Chem. Soc. 134, 1982-1985
20. Ross, P. L., Huang, Y. N., Marchese, J. N., Williamson, B., Parker, K., Hattan, S., Khainovski, N., Pillai, S., Dey, S., Daniels, S., Purkayastha, S., Juhasz, P., Martin, S., Bartlet-Jones, M., He, F., Jacobson, A., and Pappin, D. J. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 3, 1154-1169
21. Bao, Z., Guan, S., Cheng, C., Wu, S., Wong, S. H., Kemeny, D. M., Leung, B. P., and Wong, W. S. F. (2009) A novel antiinflammatory role for andrographolide in asthma via inhibition of the nuclear factor-kappaB pathway. Am. J. Respir. Crit. Care Med. 179, 657-665
22. Zhou, J., Zhang, S., Ong, C.-N., and Shen, H.-M. (2006) Critical role of pro-apoptotic Bcl-2 family members in andrographolide-induced apoptosis in human cancer cells. Biochem. Pharmacol. 72, 132-144
23. Zhou, J., Ong, C.-N., Hur, G.-M., and Shen, H.-M. (2010) Inhibition of the JAK-STAT3 pathway by andrographolide enhances chemosensitivity of cancer cells to doxorubicin. Biochem. Pharmacol. 79, 1242-1250
24. Zhou, J., Lu, G., Ong, C.-S., Ong, C.-N., and Shen, H.-M. (2008) Andrographolide sensitizes cancer cells to TRAIL-induced apoptosis via p53- mediated death receptor 4 up-regulation. Mol. Cancer Ther. 7, 2170-2180
25. Jada, S. R., Matthews, C., Saad, M. S., Hamzah, A. S., Lajis, N. H., Stevens, M. F. G., and Stanslas, J. (2008) Benzylidene derivatives of andrographolide inhibit growth of breast and colon cancer cells in vitro by inducing G(1) arrest and apoptosis. Brit. J. Pharmacol. 155, 641-654
26. Tang, L. A. L., Wang, J., Lim, T. K., Bi, X., Lee, W. C., Lin, Q., Chang, Y.-T., Lim, C. T., and Loh, K. P. (2012) High-performance graphene-titania platform for detection of phosphopeptides in cancer cells. Anal. Chem. 84, 6693-6700
27. Ghosh, D., Yu, H., Tan, X. F., Lim, T. K., Zubaidah, R. M., Tan, H. T., Chung, M. C. M., and Lin, Q. (2011) Identification of key players for colorectal cancer metastasis by iTRAQ quantitative proteomics profiling of isogenic SW480 and SW620 cell lines. J. Proteome Res. 10, 4373-4387
28. Tan, H. T., Tan, S., Lin, Q., Lim, T. K., Hew, C. L., and Chung, M. C. M. (2008) Quantitative and temporal proteome analysis of butyrate-treated colorectal cancer cells. Mol. Cell. Proteomics 7, 1174-1185
29. Saeed, A. I., Bhagabati, N. K., Braisted, J. C., Liang, W., Sharov, V., Howe, E. A., Li, J., Thiagarajan, M., White, J. A., and Quackenbush, J. (2006) TM4 microarray software suite. Methods Enzymol. 411, 134-193
30. Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kostukovich, E., Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V., and Quackenbush, J. (2003) TM4: a free, opensource system for microarray data management and analysis. Biotechniques 34, 374-378
31. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., Olson, A. J., and Al, M. E. T. (1998) Automated docking using a lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 19, 1639-1662
32. Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., and Olson, A. J. (2009) Software news and updates AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791
33. Wang, Y.-J., Wang, J.-T., Fan, Q.-X., and Geng, J.-G. (2007) Andrographolide inhibits NF-kappa-beta activation and attenuates neointimal hyperplasia in arterial restenosis. Cell Res. 17, 933-941
34. Xia, Y.-F., Ye, B.-Q., Li, Y.-D., Wang, J.-G., He, X.-J., Lin, X., Yao, X., Ma, D., Slungaard, A., Hebbel, R. P., Key, N. S., and Geng, J.-G. (2004) Andrographolide attenuates inflammation by inhibition of NF-kappa B activation through covalent modification of reduced cysteine 62 of p50. J. Immunol. 173, 4207-4217
35. Das, B., Chowdhury, C., Kumar, D., Sen, R., Roy, R., Das, P., and Chatterjee, M. (2010) Synthesis, cytotoxicity, and structure-activity relationship (SAR) studies of andrographolide analogues as anti-cancer agent. Bioorg. Med. Chem. Lett. 20, 6947-6950
36. Nanduri, S., Nyavanandi, V. K., Thunuguntla, S. S. R., Kasu, S., Pallerla, M. K., Ram, P. S., Rajagopal, S., Kumar, R. A., Ramanujam, R., Babu, J. M., Vyas, K., Devi, A. S., Reddy, G. O., and Akella, V. (2004) Synthesis and structure-activity relationships of andrographolide analogues as novel cytotoxic agents. Bioorg. Med. Chem. Lett. 14, 4711-4717
37. Wang, Z., Yu, P., Zhang, G., Xu, L., Wang, D., Wang, L., Zeng, X., and Wang, Y. (2010) Design, synthesis and antibacterial activity of novel andrographolide derivatives. Bioorg. Med. Chem. 18, 4269-4274
38. Shi, M., Lin, H., Chiang, T., Tsai, L., Tsai, S., and Lee, Y. (2009) Andrographolide could inhibit human colorectal carcinoma Lovo cells migration and invasion via down-regulation of MMP-7 expression. Chem. Biol. Interact. 180, 344-352
39. Liang, S., He, L., Zhao, X., Miao, Y., Gu, Y., Guo, C., Xue, Z., Dou, W., Hu, F., Wu, K., Nie, Y., and Fan, D. (2011) MicroRNA let-7f inhibits tumor invasion and metastasis by targeting MYH9 in human gastric cancer. PLoS One 6, e18409
40. Liu, Y., Zhang, F., Zhang, X.-F., Qi, L.-S., Yang, L., Guo, H., and Zhang, N. (2012) Expression of nucleophosmin/NPM1 correlates with migration and invasiveness of colon cancer cells. J. Biomed. Sci. 19, 53
41. Chen, C.-H., Chuang, S.-M., Yang, M.-F., Liao, J.-W., Yu, S.-L., and Chen, J. J. W. (2012) A novel function of YWHAZ/β-catenin axis in promoting epithelial-mesenchymal transition and lung cancer metastasis. Mol. Cancer Res. 10, 1319-1331
42. Gawecka, J. E., Griffiths, G. S., Ek-Rylander, B., Ramos, J. W., and Matter, M. L. (2010) R-Ras regulates migration through an interaction with filamin A in melanoma cells. PLoS One 5, e11269
43. Hu, E., Chen, Z., Fredrickson, T., and Zhu, Y. (2001) Molecular cloning and characterization of profilin-3: a novel cytoskeleton-associated gene expressed in rat kidney and testes. Exp. Nephrol. 9, 265-274
44. Barazi, H. O., Zhou, L., Templeton, N. S., Krutzsch, H. C., and Roberts, D. D. (2002) Identification of heat shock protein 60 as a molecular mediator of α 3 β 1 integrin activation. Cancer Res. 62, 1541-1548
45. Andela, V. B., Schwarz, E. M., Puzas, J. E., Keefe, R. J. O., and Rosier, R. N. (2000) Tumor metastasis and the reciprocal regulation of prometastatic and antimetastatic factors by nuclear factor k B. Cancer Res. 60, 6557-6562
46. Yamaguchi, H., and Condeelis, J. (2007) Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim. Biophys. Acta 1773, 642-652
47. Statsuk, A. V., Bai, R., Baryza, J. L., Verma, V. A., Hamel, E., Wender, P. A., and Kozmin, S. A. (2005) Actin is the primary cellular receptor of bistramide A. Nat. Chem. Biol. 1, 383-388
48. Tannert, R., Milroy, L.-G., Ellinger, B., Hu, T.-S., Arndt, H.-D., and Waldmann, H. (2010) Synthesis and structure-activity correlation of naturalproduct inspired cyclodepsipeptides stabilizing F-actin. J. Am. Chem. Soc. 132, 3063-3077
49. Kita, M., Hirayama, Y., Sugiyama, M., and Kigoshi, H. (2011) Development of highly cytotoxic and actin-depolymerizing biotin derivatives of aplyronine A. Angew. Chem. Int. Ed. 50, 9871-9874
50. Quideau, S., Douat-Casassus, C., Delannoy Ló pez, D. M., Di Primo, C., Chassaing, S., Jacquet, R., Saltel, F., and Genot, E. (2011) Binding of filamentous actin and winding into fibrillar aggregates by the polyphenolic C-glucosidic ellagitannin vescalagin. Angew. Chem. 123, 5205-5210
51. Aldini, G., Carini, M., Vistoli, G., Shibata, T., Kusano, Y., Gamberoni, L., Dalle-Donne, I., Milzani, A., and Uchida, K. (2007) Identification of actin as a 15-deoxy-Delta12,14-prostaglandin J2 target in neuroblastoma cells: mass spectrometric, computational, and functional approaches to investigate the effect on cytoskeletal derangement. Biochemistry 46, 2707-2718
52. Gayarre, J., Sá nchez, D., Sá nchez-Gó mez, F. J., Terró n, M. C., Llorca, O., and Pé rez-Sala, D. (2006) Addition of electrophilic lipids to actin alters filament structure. Biochem. Biophys. Res. Commun. 349, 1387-1393
53. Lassing, I., Schmitzberger, F., Björnstedt, M., Holmgren, A., Nordlund, P., Schutt, C. E., and Lindberg, U. (2007) Molecular and structural basis for redox regulation of beta-actin. J. Mol. Biol. 370, 331-348
54. Landino, L. M. (2008) Protein thiol modification by peroxynitrite anion and nitric oxide donors. Methods Enzymol. 440, 95-109
55. Rozycki, M., Chik, J., Lindberg, U., and Schutt, C. (1995) Crystallographically observed conformational changes and sulfhydryl reactivity in actin. Biophys. J. 68, 3661