Mutations enhancing selectivity of antitumor cytokine TRAIL to DR5 receptor increase its cytotoxicity against tumor cells

Biochemistry (Moscow)

Volumn 80, Issue 8, 2015, Pages 1080-1091

  Gasparian, M E ^a   Bychkov, M L ^a   Yagolovich, A V ^a,b   Dolgikh, D A ^a,b   Kirpichnikov, M P ^a,b  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

anticancer therapy; bortezomib; doxorubicin; DR5 B; DR5 specific variant of TRAIL; paclitaxel; TRAIL

Indexed keywords

ANTINEOPLASTIC AGENT; RECOMBINANT PROTEIN; TNFSF10 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

APOPTOSIS; DRUG EFFECTS; GENETICS; HCT116 CELL LINE; HEPG2 CELL LINE; HT 29 CELL LINE; HUMAN; JURKAT CELL LINE; METABOLISM; MUTATION; NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR CELL LINE; U937 CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; HCT116 CELLS; HEP G2 CELLS; HT29 CELLS; HUMANS; JURKAT CELLS; MUTATION; NEOPLASMS; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR NECROSIS FACTOR-ALPHA; U937 CELLS;

EID: 84939516081     PISSN: 00062979     EISSN: 16083040     Source Type: Journal    
DOI: 10.1134/S0006297915080143     Document Type: Article

References (31)

1. Wiley, S. R., Schooley, K., Smolak, P. J., Din, W. S., Huang, C. P., Nicholl, J. K., Sutherland, G. R., Smith, T. D., Rauch, C., and Smith, C. A. (1995) Identification and characterization of a new member of the TNF family that induces apoptosis, Immunity, 3, 673-682.
2. Pitti, R. M., Marsters, S. A., Ruppert, S., Donahue, C. J., Moore, A., and Ashkenazi, A. (1996) Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family, J. Biol. Chem., 271, 12687-12690.
3. Ashkenazi, A., Pai, R. C., Fong, S., Leung, S., Lawrence, D. A., Marsters, S. A., Blackie, C., Chang, L., Mc Murtrey, A. E., Hebert, A., DeForge, L., Koumenis, I. L., Lewis, D., Harris, L., Bussiere, J., Koeppen, H., Shahrokh, Z., and Schwall, R. H. (1999). Safety and antitumor activity of recombinant soluble Apo2 ligand, J. Clin. Invest., 104, 155-162.
4. Wajant, H., Gerspach, J., and Pfizenmaier, K. (2013) Engineering death receptor ligands for cancer therapy, Cancer Lett., 332, 163-174.
5. Lemke, J., von Karstedt, S., Zinngrebe, J., and Walczak, H. (2014) Getting TRAIL back on track for cancer therapy, Cell Death Differ., 21, 1350-1364.
6. Wajant, H., Gerspach, J., and Pfizenmaier, K. (2005) Tumor therapeutics by design: targeting and activation of death receptors, Cytokine Growth Factor Rev., 16, 55-76.
7. Dimberg, L. Y., Anderson, C. K., Camidge, R., Behbakht, K., Thorburn, A., and Ford, H. L. (2013) On the TRAIL to successful cancer therapy? Predicting and counteracting resistance against TRAIL-based therapeutics, Oncogene, 32, 1341-1350.
8. Gonzalvez, F., and Ashkenazi, A. (2010) New insights into apoptosis signaling by Apo2L/TRAIL, Oncogene, 29, 4752-4765.
9. Merino, D., Lalaoui, N., Morizot, A., Schneider, P., Solary, E., and Micheau, O. (2006) Differential inhibition of TRAIL-mediated DR5-DISC formation by decoy receptors 1 and 2, Mol. Cell Biol., 26, 7046-7055.
10. Hymowitz, S. G., O' Connell, M. P., Ultsch, M. H., Hurst, A., Totpal, K., Ashkenazi, A., de Vos, A. M., and Kelley, R. F. (2000) A unique zinc-binding site revealed by a high-resolution X-ray structure of homotrimeric Apo2L/TRAIL, Biochemistry, 39, 633-640.
11. Gasparian, M. E., Chernyak, B. V., Dolgikh, D. A., Yagolovich, A. V., Popova, E. N., Sycheva, A. M., Moshkovskii, S. A., and Kirpichnikov, M. P. (2009) Generation of new TRAIL mutants DR5-A and DR5-B with improved selectivity to death receptor 5, Apoptosis, 14, 778-787.
12. Georgakis, G. V., Li, Y., Humphreys, R., Andreeff, M., O' Brien, S., Younes, M., Carbone, A., Albert, V., and Younes, A. (2005) Activity of selective fully human agonistic antibodies to the TRAIL death receptors TRAIL-R1 and TRAIL-R2 in primary and cultured lymphoma cells: induction of apoptosis and enhancement of doxorubicinand bortezomib-induced cell death, Br. J. Haematol., 130, 501-510.
13. Griffith, T. S., Rauch, C. T., Smolak, P. J., Waugh, J. Y., Boiani, N., Lynch, D. H., Smith, C. A., Goodwin, R. G., and Kubin, M. Z. (1999) Functional analysis of TRAIL receptors using monoclonal antibodies, J. Immunol., 162, 2597-2605.
14. Elrod, H. A., and Sun, S. Y. (2008) Modulation of death receptors by cancer therapeutic agents, Cancer Biol. Ther., 7, 163-173.
15. Mahalingam, D., Szegezdi, E., Keane, M., de Jong, S., and Samali, A. (2009) TRAIL receptor signaling and modulation: are we on the right TRAIL? Cancer Treat. Rev., 35, 280-288.
16. Li, F., and Ravetch, J. V. (2012) Apoptotic and antitumor activity of death receptor antibodies require inhibitory Fcγ receptor engagement, Proc. Natl. Acad. Sci. USA, 109, 10966-10971.
17. Kelley, R. F., Totpal, K., Lindstrom, S. H., Mathieu, M., Billeci, K., Deforge, L., Pai, R., Hymowitz, S. G., and Ashkenazi, A. (2005) Receptor-selective mutants of Apo2L/TRAIL reveal a greater contribution of DR5 than DR4 to apoptosis signaling, J. Biol. Chem., 28, 2205-2212.
18. Van der Sloot, A. M., Tur, V., Szegezdi, T. E., Mullally, M. M., Cool, R. H., Samali, A., Serrano, L., and Quax, W. J. (2006) Designed tumor necrosis factor-related apoptosisinducing ligand variants initiating apoptosis exclusively via the DR5 receptor, Proc. Natl. Acad. Sci. USA, 10, 8634-8639.
19. Gasparian, M. E., Ostapchenko, V. G., Schulga, A. A., Dolgikh, D. A., and Kirpichnikov, M. P. (2003) Expression, purification, and characterization of human enteropeptidase catalytic subunit in Escherichia coli, Protein Express. Purif., 31, 133-139.
20. Gasparian, M. E., Bychkov, M. L., Dolgikh, D. A., and Kirpichnikov, M. P. (2011) Strategy for improvement of enteropeptidase efficiency in tag removal processes, Protein Express. Purif., 79, 191-196.
21. Yagita, H., Takeda, K., Hayakawa, Y., Smyth, M. J., and Okumura, K. (2004) TRAIL and its receptors as targets for cancer therapy, Cancer Sci., 95, 777-783.
22. Ashkenazi, A., and Herbst, R. S. (2008) To kill a tumor cell: the potential of proapoptotic receptor agonists, J. Clin. Invest., 118, 1979-1990.
23. Prasad, S., Kim, J. H., Gupta, S. C., and Aggarwal, B. B. (2014) Targeting death receptors for TRAIL by agents designed by Mother Nature, Trends Pharmacol. Sci., 35, 520-536.
24. Van Roosmalen, I. A., Quax, W. J., and Kruyt, F. A. (2014) Two death-inducing human TRAIL receptors to target in cancer: similar or distinct regulation and function? Biochem. Pharmacol., 91, 447-456.
25. Lu, M., Lawrence, D. A., Marsters, S., Acosta-Alvear, D., Kimmig, P., Mendez, A. S., Paton, A. W., Paton, J. C., Walter, P., and Ashkenazi, A. (2014) Cell death. Opposing unfolded-protein-response signals converge on death receptor 5 to control apoptosis, Science, 345, 98-101.
26. Holland, P. M. (2014) Death receptor agonist therapies for cancer, which is the right TRAIL? Cytokine Growth Factor Rev., 25, 185-193.
27. MacFarlane, M., Inoue, S., Kohlhaas, S. L., Majid, A., Harper, N., Kennedy, B. D., Dyer, M. J., and Cohen, G. M. (2005) Chronic lymphocytic leukemic cells exhibit apoptotic signaling via TRAIL-R1, Cell Death Differ., 12, 773-782.
28. Kabore, A. F., Sun, J., Hu, X., Mc Crea, K., Johnston, J. B., and Gibson, S. B. (2006) The TRAIL apoptotic pathway mediates proteasome inhibitor induced apoptosis in primary chronic lymphocytic leukemia cells, Apoptosis, 11, 1175-1193.
29. Bychkov, M. L., Gasparian, M. E., Dolgikh, D. A., and Kirpichnikov, M. P. (2014) Combination of TRAIL with bortezomib shifted apoptotic signaling from DR4 to DR5 death receptor by selective internalization and degradation of DR4, PLoS One, 19, e109756.
30. Herbst, R. S., Eckhardt, S. G., Kurzrock, R., Ebbinghaus, S., O'Dwyer, P. J., Gordon, M. S., Novotny, W., Goldwasser, M. A., Tohnya, T. M., Lum, B. L., Ashkenazi, A., Jubb, A. M., and Mendelson, D. S. (2010) Phase I doseescalation study of recombinant human Apo2L/TRAIL, a dual proapoptotic receptor agonist, in patients with advanced cancer, J. Clin. Oncol., 28, 2839-2846.
31. Bosman, M. C., Reis, C. R., Schuringa, J. J., Vellenga, E., and Quax, W. J. (2014) Decreased affinity of recombinant human tumor necrosis factor-related apoptosis-inducing ligand (rhTRAIL) D269H/E195R to osteoprotegerin (OPG) overcomes TRAIL resistance mediated by the bone microenvironment, J. Biol. Chem., 289, 1071-1078.