Abstract
Results of biochemical studies of apoptosis reactions induced by granzyme B are considered and summarized. Special attention is paid to the reactions of procaspase activation and limited proteolysis of apoptotic targets. Found values of kinetic constants of granzyme B-mediated enzymatic reactions are listed.
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Abbreviations
- FasL:
-
ligand of Fas receptor
- Hsp:
-
heat shock protein
- IAP:
-
apoptosis inhibitor
- ICAD:
-
inhibitor of nuclear nuclease CAD
- NK cells:
-
natural killers
- PARP-1:
-
poly(ADP-Rib) polymerase 1
- Smac:
-
secondary mitochondrial caspase activator
- TNF-α:
-
tumor necrosis fac tor α
- TRAIL:
-
TNF-connected ligand inducing apoptosis
References
Andrade, F., Roy, S., Nicholson, D., Thornberry, N., Rosen, A., and Casciola-Rosen, L., Immunity, 1998, vol. 8, pp. 451–460.
Pinkoski, M.J., Waterhouse, N.J., Heibein, J.A., Wolf, B.B., Kuwana, T., Goldstein, J.C., Newmeyer, D.D., Bleackley, R.C., and Green, D.R., J. Biol. Chem., 2001, vol. 276, pp. 12 060–12 067.
Ozoren, N., Fisher, M.J., Kim, K., Liu, C.X., Genin, A., Shifman, Y., Dicker, D.T., Spinner, N.B., Lisitsyn, N.A., and El-Deiry, W.S., Int. J. Oncol., 2000, vol. 16, pp. 917–925.
Zhang, X.D., Franco, A.V., Nguyen, T., Gray, C.P., and Hersey, P., J. Immunol., 2000, vol. 164, pp. 3961–3970.
Trambas, C.M. and Griffiths, G.M., Nature Immunol., 2003, vol. 4, pp. 399–403.
Russell, J.H. and Ley, T.J., Annu. Rev. Immunol., 2002, vol. 20, pp. 323–370.
Grossman, W.J., Verbsky, J.W., Tollefsen, B.L., Kemper, C., Atkinson, J.P., and Ley, T.J., Blood, 2004, vol. 104, pp. 2840–2848.
Sayers, T.J., Brooks, A.D., Ward, J.M., Hoshino, T., Bere, W.E., Wiegand, G.W., Kelly, J.M., and Smyth, M.J., J. Immunol., 2001, vol. 166, pp. 765–771.
Kelso, A., Costelloe, E.O., Johnson, B.J., Groves, P., Buttigieg, K., and Fitzpatrick, D.R., Int. Immunol., 2002, vol. 14, pp. 605–613.
Sedelies, K.A., Sayers, T.J., Edwards, K.M., Chen, W., Pellicci, D.G., Godfrey, D.I., and Trapani, J.A., J. Biol. Chem., 2004, vol. 279, pp. 26 581–26 587.
Pham, C.T.N. and Ley, T.J., Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 8627–8632.
Galvin, J.P., Spaeny-Dekking, E.H.A., Wang, B., Seth, P., Hack, C.E., and Froelich, C.J., J. Immunol., 1999, vol. 162, pp. 5345–5350.
Metkar, S.S., Wang, B., Aguilar-Santelises, M., Raja, S.M., Uhlin-Hansen, L., Podack, E., Trapani, J.A., and Froelich, C.J., Immunity, 2002, vol. 16, pp. 417–428.
Raja, S.M., Metkar, S.S., Honing, S., Wang, B., Russin, W.A., Pipalia, N.H., Menaa, C., Belting, M., Cao, X., Dressel, R., and Froelich, C.J., J. Biol. Chem., 2005, vol. 280, pp. 20 752–20 761.
Shi, L., Keefe, D., Durand, E., Feng, H., Zhang, D., and Lieberman, J., J. Immunol., 2005, vol. 174, pp. 5456–5461.
Trapani, J.A., Sutton, V.R., Thia, K.Y., Li, Y.Q., Froelich, C.J., Jans, D.A., Sandrin, M.S., and Browne, K.A., J. Cell Biol., 2003, vol. 160, pp. 223–233.
Froelich, C.J., Orth, K., Turbov, J., Seth, P., Gottleib, R., Babior, B., Shah, G.M., Bleackley, R.C., Dixit, V.M., and Hanna, W., J. Biol. Chem., 1996, vol. 271, pp. 29073–29079.
Shi, L., Mai, S., Israels, S., Browne, K.A., Trapani, J.A., and Greenberg, A.H., J. Exp. Med., 1997, vol. 185, pp. 855–866.
Keefe, D., Shi, L., Feske, S., Massol, R., Navarro, F., Kirchhausen, T., and Lieberman, J., Immunity, 2005, vol. 23, pp. 249–262.
Dupuis, M., Schaerer, E., Krause, K.H., and Tschopp, J., J. Exp. Med., 1993, vol. 177, pp. 1–7.
Fraser, S.A., Karimi, R., Michalak, M., and Hudig, D., J. Immunol., 2000, vol. 164, pp. 4150–4155.
Pipkin, M.E. and Lieberman, J., Curr. Opin. Immunol., 2007, vol. 19, pp. 301–308.
Veugelers, K., Motyka, B., Frantz, C., Shostak, I., Sawchuk, T., and Bleackley, R.C., Blood, 2004, vol. 103, pp. 3845–3853.
Beresford, P.J., Xia, Z., Greenberg, A.H., and Lieberman, J., Immunity, 1999, vol. 10, pp. 585–594.
MacDonald, G., Shi, L., Vande Velde, C., Lieberman, J., and Greenberg, A.H. J. Exp. Med., 1999, vol. 189, pp. 131–144.
Kelly, J.M., Waterhouse, N.J., Cretney, E., Browne, K.A., Ellis, S., Trapani, J.A., and Smyth, M.J., J. Biol. Chem., 2004, vol. 279, pp. 22 236–22 242.
Waugh, S.M., Harris, J.L., Fletterick, R., and Craik, C.S., Nat. Struct. Biol., 2000, vol. 7, pp. 762–765.
Rotonda, J., Garcia-Calvo, M., Bull, H.G., Geissler, W.M., McKeever, B.M., Willoughby, C.A., Thornberry, N.A., and Becker, J.W., Chem. Biol., 2001, vol. 8, pp. 357–368.
Thornberry, N.A., Rano, T.A., Peterson, E.P., Rasper, D.M., Timkey, T., Garcia-Calvo, M., Houtzager, V.M., Nordstrom, P.A., Roy, S., Vaillancourt, J.P., Chapman, K.T., and Nicholson, D.W., J. Biol. Chem., 1997, vol. 272, pp. 17907–17911.
Casciola-Rosen, L., Andrade, F., Ulanet, D., Wong, W.B., and Rosen, A., J. Exp. Med., 1999, vol. 190, pp. 815–826.
Harris, J.L., Peterson, E.P., Hudig, D., Thornberry, N.A., and Craik, C.S., J. Biol. Chem., 1998, vol. 273, pp. 27364–27373.
Earnshow, W.C., Martins, L.M., and Kaufmann, S.H., Annu. Rev. Biochem., 1999, vol. 68, pp. 383–424.
Launay, S., Hermine, O., Fontenay, M., Kroemer, G., Solary, E., and Garrido, C., Oncogene, 2005, vol. 24, pp. 5137–5148.
Eckhart, L., Ballaun, C., Uthman, A., Kittel, C., Stichenwirth, M., Buchberger, M., Fischer, H., Sipos, W., and Tschachler, E., J. Biol. Chem., 2005, vol. 280, pp. 35077–35080.
Saleh, M., Vaillancourt, J.P., Graham, R.K., Huyck, M., Srinivasula, S.M., Alnemri, E.S., Steinberg, M.H., Nolan, V., Baldwin, C.T., Hotchkiss, R.S., Buchman, T.G., Zehnbauer, B.A., Hayden, M.R., Farrer, L.A., Roy, S., and Nicholson, D.W., Nature, 2004, vol. 429, pp. 75–79.
Bossi, G. and Griffiths, G.M., Nature Med., 1999, vol. 5, pp. 90–96.
Kojima, Y., Kawasaki-Koyanagi, A., Sueyoshi, N., Kanai, A., Yagita, H., and Okumura, K., Biochem. Biophys. Res. Commun., 2002, vol. 296, pp. 328–336.
Martinon, F. and Tschopp, J., Cell, 2004, vol. 117, pp. 561–574.
Hitomi, J., Katayama, T., Eguchi, Y., Kudo, T., Taniguchi, M., Koyama, Y., Manabe, T., Yamagishi, S., Bando, Y., Imaizumi, K., Tsujimoto, Y., and Tohyama, M., J. Cell Biol., 2004, vol. 165, pp. 347–356.
Lippens, S., Kockx, M., Knaapen, M., Mortier, L., Polakowska, R., Verheyen, A., Garmyn, M., Zwijsen, A., Formstecher, P., Huylebroeck, D., Vandenabeele, P., and Declercq, W., Cell Death. Differ., 2000, vol. 7, pp. 1218–1224.
Eckhart, L., Declercq, W., Ban, J., Rendl, M., Lengauer, B., Mayer, C., Lippens, S., Vandenabeele, P., and Tschachler, E., J. Invest. Dermatol., 2000, vol. 115, pp. 1148–1151.
Talanian, R.V., Yang, X., Turbov, J., Seth, P., Ghayur, T., Casiano, C.A., Orth, K., and Froelich, C.J., J. Exp. Med., 1997, vol. 186, pp. 1323–1331.
Zhou, Q. and Salvesen, G.S., Biochem. J., 1997, vol. 324, pp. 361–364.
Stennicke, H.R., Jurgensmeier, J.M., Shin, H., Deveraux, Q., Wolf, B.B., Yang, X., Zhou, Q., Ellerby, H.M., Ellerby, L.M., Bredesen, D., Green, D.R., Reed, J.C., Froelich, C.J., and Salvesen, G.S., J. Biol. Chem., 1998, vol. 273, pp. 27 084–27 090.
Stennicke, H.R. and Salvesen, G.S., Biochim. Biophys. Acta, 2000, vol. 1477, pp. 299–306.
Slee, E.A., Harte, M.T., Kluck, R.M., Wolf, B.B., Casiano, C.A., Newmeyer, D.D., Wang, H.G., Reed, J.C., Nicholson, D.W., Alnemri, E.S., Green, D.R., and Martin, S.J., J. Cell Biol., 1999, vol. 144, pp. 281–292.
Cowling, V. and Downward, J., Cell Death. Differ., 2002, vol. 9, pp. 1046–1056.
Sohn, D., Schulze-Osthoff, K., and Janicke, R.U., J. Biol. Chem., 2005, vol. 280, pp. 5267–5273.
Mancini, M., Machamer, C.E., Roy, S., Nicholson, D.W., Thornberry, N.A., Casciola-Rosen, L.A., and Rosen, A., J. Cell Biol., 2000, vol. 149, pp. 603–612.
Zhivotovsky, B. and Orrenius, S., Biochem. Biophys. Res. Commun., 2005, vol. 331, pp. 859–867.
Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Tomaselli, K.J., Debatin, K.M., Krammer, P.H., and Peter, M.E., EMBO J., 1998, vol. 17, pp. 1675–1687.
Bossy-Wetzel, E. and Green, D.R., J. Biol. Chem., 1999, vol. 274, pp. 17484–17490.
Guo, Y., Srinivasula, S.M., Druilhe, A., Fernandes-Alnemri, T., and Alnemri, E.S., J. Biol. Chem., 2002, vol. 277, pp. 13430–13437.
Milhas, D., Cuvillier, O., Therville, N., Clave, P., Thomsen, M., Levade, T., Benoist, H., and Segui, B., J. Biol. Chem., 2005, vol. 280, pp. 19 836–19 842.
Eskes, R., Desagher, S., Antonsson, B., and Martinou, J.C., Mol. Cell Biol., 2000, vol. 20, pp. 929–935.
Wei, M.C., Lindsten, T., Mootha, V.K., Weiler, S., Gross, A., Ashiya, M., Thompson, C.B., and Korsmeyer, S.J., Genes Dev., 2000, vol. 14, pp. 2060–2071.
Ruffolo, S.C. and Shore, G.C., J. Biol. Chem., 2003, vol. 278, pp. 25 039–25 045.
Willis, S.N., Chen, L., Dewson, G., Wei, A., Naik, E., Fletcher, J.I., Adams, J.M., and Huang, D.C., Genes Dev., 2005, vol. 19, pp. 1294–1305.
Chen, L., Willis, S.N., Wei, A., Smith, B.J., Fletcher, J.I., Hinds, M.G., Colman, P.M., Day, C.L., Adams, J.M., and Huang, D.C., Mol. Cell, 2005, vol. 17, pp. 393–403.
Korsmeyer, S.J., Wei, M.C., Saito, M., Weiler, S., Oh, K.J., and Schlesinger, P.H., Cell Death. Differ., 2000, vol. 12, pp. 1166–1173.
Hill, M.M., Adrain, C., and Martin, S.J., Mol. Interv., 2003, vol. 3, pp. 19–26.
Thomas, D.A., Scorrano, L., Putcha, G.V., Korsmeyer, S.J., and Ley, T.J., Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 14 985–14 990.
Roy, N., Deveraux, Q.L., Takahashi, R., Salvesen, G.S., and Reed, J.C., EMBO J., 1997, vol. 16, pp. 6914–6925.
Deveraux, Q.L., Roy, N., Stennicke, H.R., van Arsdale, T., Zhou, Q., Srinivasula, S.M., Alnemri, E.S., Salvesen, G.S., and Reed, J.C., EMBO J., 1998, vol. 17, pp. 2215–2223.
Vucic, D., Stennicke, H.R., Pisabarro, M.T., Salvesen, G.S., and Dixit, V.M., Curr. Biol., 2000, vol. 10, pp. 1359–1366.
Vucic, D., Franklin, M.C., and Wallweber, H.J.A., Das, K., Eckelman, B.P., Shin, H., Elliott, L.O., Kadkhodayan, S., Deshayes, K., Salvesen, G.S., and Fairbrother, W.J., Biochem. J., 2005, vol. 385, pp. 11–20.
Kasof, G.M. and Gomes, B.C., J. Biol. Chem., 2001, vol. 276, pp. 3238–3246.
Riedl, S.J., Renatus, M., Schwarzenbacher, R., Zhou, Q., Sun, C., Fesik, S.W., Liddington, R.C., and Salvesen, G.S., Cell, 2001, vol. 104, pp. 791–800.
Shin, S., Sung, B.J., Cho, Y.S., Kim, H.J., Ha, N.C., Hwang, J.I., Chung, C.W., Jung, Y.K., and Oh, B.H., Biochemistry, 2001, vol. 40, pp. 1117–1123.
Shin, H., Renatus, M., Eckelman, B.P., Nunes, V.A., Sampaio, C.A., and Salvesen, G.S., Biochem. J., 2005, vol. 385, pp. 1–10.
Maier, J.K., Lahoua, Z., Gendron, N.H., Fetni, R., Johnston, A., Davoodi, J., Rasper, D., Roy, S., Slack, R.S., Nicholson, D.W., and MacKenzie, A.E, J. Neurosci., 2002, vol. 22, pp. 2035–2043.
Huang, Y., Rich, R.L., Myszka, D.G., and Wu, H., J. Biol. Chem., 2003, vol. 278, pp. 49 517–49 522.
Davoodi, J., Lin, L., Kelly, J., Liston, P., and MacKenzie A.E, J. Biol. Chem., 2004, vol. 279, pp. 40622–40628.
Qiu, X.B. and Goldberg, A.L., J. Biol. Chem., 2005, vol. 280, pp. 174–182.
Nandi, D., Tahiliani, P., Kumar, A., and Chandu, D., J. Biosci., 2006, vol. 31, pp. 137–155.
Yang, Y., Fang, S., Jensen, J.P., Weissman, A.M., and Ashwell, J.D., Science, 2000, vol. 288, pp. 874–877.
Yang, Q.H., Church-Hajduk, R., Ren, J., Newton, M.L., and Du, C., Genes Dev., 2003, vol. 17, pp. 1487–1496.
Huang, H., Joazeiro, C.A., Bonfoco, E., Kamada, S., Leverson, J.D., and Hunter, T., J. Biol. Chem., 2000, vol. 275, pp. 26 661–26 664.
Suzuki, Y., Nakabayashi, Y., and Takahashi, R., Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 8662–8667.
Verhagen, A.M., Silke, J., Ekert, P.G., Pakusch, M., Kaufmann, H., Connolly, L.M., Day, C.L., Tikoo, A., Burke, R., Wrobel, C., Moritz, R.L., Simpson, R.J., and Vaux, D.L., J. Biol. Chem., 2002, vol. 277, pp. 445–454.
Bartke, T., Pohl, C., Pyrowolakis, G., and Jentsch, S., Mol. Cell, 2004, vol. 14, pp. 801–811.
Samuel, T., Welsh, K., Lober, T., Togo, S.H., Zapata, J.M., and Reed, J.C., J. Biol. Chem., 2006, vol. 281, pp. 1080–1090.
MacFarlane, M., Merrison, W., Bratton, S.B., and Cohen, G.M., J. Biol. Chem., 2002, vol. 277, pp. 36 611–36 616.
Colell, A., Garcia-Ruiz, C., Mari, M., and Fernandez-Checa, J.C., FEBS Lett., 2004, vol. 560, pp. 63–68.
Du, C., Fang, M., Li, Y., Li, L., and Wang, X., Cell, 2000, vol. 102, pp. 33–42.
van Loo, G., van Gurp, M., Depuydt, B., Srinivasula, S.M., Rodriguez, I., Alnemri, E.S., Gevaert, K., Vandekerckhove, J., Declercq, W., and Vandenabeele, P., Cell Death. Differ., 2002, vol. 9, pp. 20–26.
McIlroy, D., Sakahira, H., Talanian, R.V., and Nagata, S., Oncogene, 1999, vol. 18, pp. 4401–4408.
Sharif-Askari, E., Alam, A., Rheaume, E., Beresford, P.J., Scotto, C., Sharma, K., Lee, D., DeWolf, W.E., Nuttall, M.E., Lieberman, J., and Sekaly, R.P., EMBO J., 2001, vol. 20, pp. 3101–3113.
Casciola-Rosen, L.A., Nicholson, D.W., Chong, T., Rowan, K.R., Thornberry, N.A., Miller, D.K., and Rosen, A., J. Exp. Med., 1996, vol. 183, pp. 1957–1964.
Margolin, N., Raybuck, S.A., Wilson, K.P., Chen, W., Fox, T., Gu, Y., and Livingston, D.J., J. Biol. Chem., 1997, vol. 272, pp. 7223–7228.
Gervais, F.G., Thornberry, N.A., Ruffolo, S.C., Nicholson, D.W., and Roy, S., J. Biol. Chem., 1998, vol. 273, pp. 17 102–17 108.
Stennicke, H.R., Renatus, M., Meldal, M., and Salvesen, G.S., Biochem. J., 2000, vol. 350, pp. 563–568.
Mahoney, J.A., Odin, J.A., White, S.M., Shaffer, D., Koff, A., Casciola-Rosen, L., and Rosen, A., Biochem. J., 2002, vol. 361, pp. 587–595.
Fadeel, B., Antioxid. Redox Signal, 2004, vol. 6, pp. 269–275.
Zhang, D., Beresford, P.J., Greenberg, A.H., and Lieberman, J., Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 5746–5751.
Adrain, C., Duriez, P.J., Brumatti, G., Delivani, P., and Martin, S.J., J. Biol. Chem., 2006, vol. 281, pp. 8118–8125.
Bredemeyer, A.J., Lewis, R.M., Malone, J.P., Davis, A.E., Gross, J., Townsend, R.R., and Ley, T.J., Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 11 785–11 790.
Loeb, C.R., Harris, J.L., and Craik, C.S., J. Biol. Chem., 2006, vol. 281, pp. 28326–28335.
Hostetter, D.R., Loeb, C.R., Chu, F., and Craik, C.S., J. Biol. Chem., 2007, Jul. [Epub ahead of print].
Bredemeyer, A.J., Carrigan, P.E., Fehniger, T.A., Smith, D.F., and Ley, T.J., J. Biol. Chem., 2006, vol. 281, pp. 37 130–37 141.
Caruso, J.A. and Reiners, J.J. Jr., Apoptosis, 2006, vol. 11, pp. 1877–1885.
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Original Russian Text © A.V. Sintsov, E. I. Kovalenko, M.A. Khanin, 2008, published in Bioorganicheskaya Khimiya, 2008, Vol. 34, No. 6, pp. 725–733.
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Sintsov, A.V., Kovalenko, E.I. & Khanin, M.A. Apoptosis induced by granzyme B. Russ J Bioorg Chem 34, 647–654 (2008). https://doi.org/10.1134/S1068162008060010
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DOI: https://doi.org/10.1134/S1068162008060010