Biochemical characterization and localization of transglutaminase in wild-type and cell-death mutants of the nematode Caenorhabditis elegans

European Journal of Biochemistry

Volumn 253, Issue 3, 1998, Pages 583-590

  Mádi, András ^a   Punyiczki, Mária ^a   Di Rao, Massimo ^b   Piacentini, Mauro ^b   Fésüs, László ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Caenorhabditis elegans; Programmed cell death; Transglutaminase

Indexed keywords

AMMONIA; CALCIUM ION; EGTAZIC ACID; GUANOSINE TRIPHOSPHATE; IODOACETAMIDE; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ARTICLE; CAENORHABDITIS ELEGANS; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME SUBSTRATE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN CROSS LINKING;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 0032080312     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1998.2530583.x     Document Type: Article

References (71)

1. Sulston, J. E., Schierenberg, E., White, J. G. & Thomson, J. N. (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans, Dev. Biol. 100, 64-119.
2. Sulston, J. E. & Horvitz, H. R. (1977) Post-embryonic cell lineages of the nematode Caenorhabditis elegans, Dev. Biol. 82, 110-156.
3. Robertson, A. M. G. & Thomson, J. N. (1982) Morphology of programmed cell death in the ventral nerve cord of Caenorhabditis elegans larvae, J. Embryol. Exp. Morphol. 67, 89-100.
4. Horvitz, H. R., Brenner, S., Hodgkin, J. & Herman, R. K. (1979) A uniform genetic nomenclature for the nematode Caenorhabditis elegans, Mol. gen. Genet. 175, 129-133.
5. Ellis, H. M. & Horvitz, H. R. (1986) Genetic control of programmed cell death in the nematode C. elegans, Cell 44, 817-829.
6. Hengartner, M. O., Ellis, R. E. & Horvitz, H. R. (1992) Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 356, 494-499.
7. Avery, L. & Horvitz, H. R. (1987) A cell that dies during wild-type C. elegans development can function as a neuron in a ced-3 mutant, Cell 51, 1071-1078.
8. Chinnaiyan, A. M., O'Rourke, K., Lane, B. & Dixit, V. M. (1997) Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death, Science 275, 1122-1126.
9. Irmler, M., Hofman, K., Vaux, D. & Tschopp, J. (1997) Direct physical interaction between the Caenorhabditis elegans 'death proteins' CED-3 and CED-4, FEBS Lett. 406, 189-190.
10. Spector, M. S., Desnoyers, S., Hoeppner, D. J. & Hengartner, M. O. (1997) Interaction between the C. elegans cell-death regulators CED-9 and CED-4, Nature 385, 653-656.
11. Wu, D., Wallen, H. D. & Nunez, G. (1997) Interaction and regulation of subcellular localization of CED-4 by CED-9, Science 275, 1126-1129.
12. Hedgecock, E. M., Sulston, J. E. & Thomson, J. N. (1983) Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans, Science 220, 1277-1279.
13. Ellis, R. E., Jacobson, D. M. & Horvitz, H. R. (1991) Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. Genetics 129, 79-84.
14. Yuan, J. (1996) Evolutionary conversation of a genetic pathway of programmed cell death, J. Cell. Biochem. 60, 4-11.
15. Steller, H. (1995) Mechanism and genes of cellular suicide, Science 267, 1445-1449.
16. Hengartner, M. O. & Horvitz, R. H. (1994) C. elegans cell survival gene ced-9 encodes a functional homologue of the mammalian proto-oncogene bcl-2, Cell 76, 665-676.
17. Hengartner, M. O. & Horvitz, R. H. (1994) Activation of C. elegans cell death protein CED-9 by an amino-acid substitution in a domain conserved in Bcl-2, Nature 369, 318-320.
18. Vaux, D. L., Weissman, I. L. & Kim, S. (1992) Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2, Science 258, 1955-1957.
19. Yuan, J., Shaham, S., Ledoux, S., Ellis, H. M. & Horvitz, H. R. (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme, Cell 75, 641-652.
20. Xue, D. & Horvitz, R. (1995) Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35, Nature 377, 248-251.
21. Xue, D., Shaham, S. & Horvitz, R. (1996) The Caenorhabditis elegans cell-death protein CED-3 is a cysteine protease with substrate specifities similar to those of the human CPP32 protease, Genes. & Dev. 10, 1073-1083.
22. Miura, M., Zhu, H., Rotello, R., Hartwieg, E. A. & Yuan, J. (1993) Induction of apoptosis in fibroblasts by IL-1β-converting enzyme, a mammalian homologue of the C. elegans cell death gene ced-3, Cell 75, 653-660.
23. Kumar, S., Kinoshita, M., Noda, M., Copeland, N. G. & Jenkins, N. A. (1994) Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis cell death gene ced-3 and the mammalian IL-1β-converting enzyme, Genes & Dev. 8, 1613-1626.
24. Wang, L., Miur, M., Bergeron, L., Zhu, H. & Yuan, J. (1994) Ich-1, an Ice/ced-3 related gene, encodes both positive and negative regulators of programmed cell death, Cell 78, 739-750.
25. Fernandes-Alnemri, T., Litwack, G. & Alnemri, E. S. (1994) CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1β-converting enzyme, J. Biol. Chem. 269, 30 761-30 764.
26. Martins, L. M. & Earnshow, W. C. (1997) Apoptosis: alive and kicking in 1997, Trends Cell Biol. 7, 111-114.
27. Sugimoto, A., Friesen, P. D. & Rothman, J. H. (1994) Baculovirus p35 prevents developmentaly programmed cell death and rescues a ced-9 mutant in the nematode Caenorhabditis elegans, EMBO J. 13, 2023-2028.
28. Bump, N. J., Hackett, M., Hugunin, M., Seshagiri, S., Brady, K., Chen, P., Ferenz, C., Franklin, S., Ghayur, T. & Li, P. (1995) Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35, Science 269, 1885-1888.
29. Gagliardini, V., Fernandez, P. A., Lee, R. K., Drexler, H. C., Rotello, R. J., Fishman, M. C. & Yuan, J. (1994) Prevention of vertebrate neuronal death by crmA gene. Science 263, 826-828.
30. Bauer, M. K., Wesselborg, S. & Shulze-Osthoff, K. (1997) The Caenorhabditis elegans death protein CED-4 contains a motif with similarity to the mammalian 'death effector domain', FEBS Lett. 402, 256-258.
31. Zou, H., Henzel, W. J., Liu, X., Lutschg, A. & Wang, X. (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c dependent activation of caspase-3, Cell 90, 405-413.
32. Vaux, D. L. (1997) CED-4 - the third horseman of apoptosis, Cell 90, 389-390.
33. Luciani, M. F. & Chimini, G. (1996) The ATP binding casette transporter ABC1 is required for the engulfment of corpses generated by apoptotic cell death, EMBO J. 15, 226-235.
34. Sugimoto, A., Hozak, R. R., Nakashima, T., Nishimoto, T. & Rothman, J. H. (1995) Dad-1, an endogenous programmed cell death supressor in Caenorhabditis elegans and vertebrates, EMBO J. 14, 4434-4441.
35. Folk, J. E. & Finlayson, S. J. (1977) The ε-(γ-glutamyl)lysine crosslink and the catalytic role of transglutaminase, Adv. Protein Chem. 31, 1-133.
36. Lorand, L. & Conrad, S. M. (1984) Transglutaminase, Cell. Biochem. 58, 9-35.
37. Fésüs, L., Mádi, A., Balajthy, Z., Nemes, Z. & Szondy, Z. (1996) Transglutaminase induction by various cell death and apoptosis pathways, Experientia 52, 942-949.
38. Murtough, M. P., Mehta, K., Jonson, J., Myres, M., Juliano, R. L. & Davies, P. J. A. (1983) Induction of tissue transglutaminase in mouse peritoneal macrophages, J. Biol. Chem. 258, 11 074-11 081.
39. Nara, K., Nakanishi, H., Hagiwara, H., Wakita, K., Kojima, S. & Hirose, S. (1989) Retinol-induced morphological changes of cultured bovine endothelial cells are accompanied by a marked increase in transglutaminase, J. Biol. Chem. 264, 19 308-19 312.
40. Piacentini, M., Davies, P. J. A. & Fésüs, L. (1994) Tissue transglutaminase in cells undergoing apoptosis, in: Apoptosis II: the molecular basis of apoptosis in disease (Tomei, L. D. & Cope, F. O., eds) pp. 143-163, Cold Spring Harbor Laboratory Press Cold Spring Harbor NY.
41. Szondy, Z., Molnár, P., Nemes, Z., Boyiadzis, M., Kedei, N., Tóth, R. & Fésüs, L. (1997) Differential expression of tissue transglutaminase during in vivo apoptosis of thymocytes induced via distinct signalling pathways, FEBS Lett. 404, 307-313.
42. Fésüs, L., Thomázy, V., Autuori, F., Ceru, M. P., Tarcsa, E. & Piacentini, M. (1989) Apoptotic hepatocytes become insoluble in detergents and chaotropic agents as a result of transglutaminase action, FEBS Lett. 245, 150-154.
43. Fésüs, L., Davies, P. J. A. & Piacentini, M. (1991) Apoptosis: molecular mechanism in programmed cell death, Eur. J. Cell Biol. 56, 170-177.
44. Klein, J. D., Guzman, E. & Kuehn, G. D. (1992) Purification and partial characterization of transglutaminase from Physarum polycephalum, J. Bacteriol. 173, 2599-2605.
45. Ando, A., Adachi, M., Umeda, K., Matsura, A., Nouaka, M., Uchio, R., Tanaka, H. & Matoki, M. (1989) Purification and characterization of a novel transglutaminase derived from microorganisms, Agric. Biol. Chem. 53, 2613-2617.
46. Kuehn, G. D., Sotelo, M., Morales, T., Bruce-Carver, M. R., Guzman, E. & Margosiak, S. A. (1991) Purification and properties of transglutaminase from Medicago sativa, FASEB J. 5, 6607 (Abstr).
47. Singer, M. A., Hortsch, M., Goodman, C. S. & Bentley, D. (1992) Annulin, a protein expressed at limb segment boundaries in the grasshopper embryo, is homologous to protein cross-linking transglutaminase, Dev. Biol. 154, 143-159.
48. Tokunaga, F., Yamada, M., Miyata, T., Ding, Y. L., Hiranga-Kawabata, M., Muta, T. & Iwanaga, S. (1993) Limulus hemocyte transglutaminase, J. Biol. Chem. 268, 252-261.
49. Cariello, L., Ristoratore, F. & Zanetti, L. (1997) A new transglutaminase-like from the ascidian Ciona intestinalis, FEBS Lett. 408, 171-176.
50. Yasneda, H., Nakanishi, K., Kumazawa, Y., Nagase, K. & Motoki, M. (1995) Tissue-type transglutaminase from red sea bream (Pagrus major). Sequence analysis of the cDNA and functional expression in Escherichia coli, Eur. J. Biochem. 232, 411-419.
51. Lorand, L., Engel, J. D., Murthy, P., Jeong, J. M. & Weraarchakul-Boonmark, N. (1992) Cloning and expression of chicken erythrocyte transglutaminase, Proc. Natl Acad. Sci. USA 89, 9804-9808.
52. Singh, R. N. & Mehta, K. (1994) Purification and characterization of a novel transglutaminase from filarial nematode Brugia malayi, Eur. J. Biochem 225, 625-634.
53. Chandrashekar, R., Tsuji, N., Morales, T., Ozols, V. & Mehta, K. (1998) An ERp60-like protein from the filarial parasite Dirofilaria immitis has both transglutaminase and protein disulfide isomerase activity, Proc. Natl Acad. Sci. USA 95, 531-536.
54. Birckbichler, P. J., Uphurch, H. F., Patterson, M. K. & Conway, E. (1985) A monoclonal antibody to cellular transglutaminase, Hybridoma 4, 179.
55. Fésüs, L. & Arató, G. (1986) Quantitation of tissue transglutaminase by sandwich ELISA system, J. Immunol. Methods 94, 131-136.
56. Larsen, P. (1993) Aging and resistance to oxidative damage in Caenorhabditis elegans, Proc. Natl Acad. Sci. USA 90, 8905-8909.
57. Brenner, S. (1974) The genetics of Caenorhabditis elegans, Genetics 77, 71-94.
58. Chen, W., Lim, H. H. & Lim, L. (1993) A new member of the ras superfamily, the rac1 homologue from Caenorhabditis elegans, J. Biol. Chem. 268, 320-324.
59. Vanfleteren, J. R. (1993) Oxidative stress and ageing in Caenorhabditis elegans, Biochem. J. 292, 605-608.
60. Slaughter, T. F., Achyuthan, K. E., Lai, T. S. & Greenberg, C. S. (1992) A microtiter plate transglutaminase assay utilizing 5-(biotinamido)pentylamine as substrate, Anal. Biochem. 205, 166-171.
61. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgramquantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
62. Singh, R. N., McQueen, T. & Mehta, K. (1995) Detection of the amine acceptor protein substrates of transglutaminase with 5-(biotinamido)pentylamine, Anal. Biochem. 231, 261-263.
63. Tarcsa, E. & Fésüs, L. (1990) Determination of ε-(γ-glutamyl)lysine crosslink in proteins using phenylisothiocyanate derivatization and high pressure liquid chromatographic separation, Anal. Biochem. 186, 135-140.
64. Hu, E. & Rubin, C. S. (1990) Casein kinase II from Caenorhabditis elegans, J. Biol. Chem. 265, 5072-5080.
65. Achynthan, K. E. & Greenberg, C. S. (1987) Identification of a GTP-binding site on guinea pig liver transglutaminase. Role of GTP and calcium ions in modulating activity, J. Biol. Chem. 262, 1901-1906.
66. Nakaoka, H., Perez, D. M., Baek, K. J., Das, T., Husian, A., Misono, K., Im, M. J. & Graham, R. M. (1994) A GTP-binding protein with transglutaminase activity and receptor signaling function, Science 264, 1593-1596.
67. Aeschlimann, D. & Paulsson, M. (1994) Transglutaminases: protein cross-linking enzymes in tissues and body fluids, Thromb. Haemostasis 71, 402-415.
68. Nemes, Z., Boross, P., Balazs, M., Adany, R. & Fesus, L. (1997) Identification of cytoplasmic Actin as abundant glutaminyl substrate for tissue transglutaminase in HL-60 and U937 cells undergoing apoptosis, J. Biol. Chem. 272, 20 577-20 583.
69. Hengartner, M. O. (1997) Cell death, in C. elegans II (Riddle, D. L., Blumenthal, T., Meyer, B. J. & Priess, J. R., eds) pp. 383-415, Cold Spring Harbor Laboratory Press, Cold Spring Harbor NY.
70. Furuya, T., Lundmo, P., Short, A. D., Gill, D. L. & Isaacs, J. T. (1994) The role of calcium, pH and cell proliferation in the programmed (apoptotic) death of androgen-independent prostatic cancer cells induced by thapsigargin, Cancer Res. 54, 6167-6175.
71. Churg, S. I., Chang, S. K., Cocuzzi, E. T., Folk, J. E., Kim, H. C., Lee, S. Y., Martinet, N., Nigra, T. & Sun, H. S. (1988) Modulation of cellular transglutaminase: protease induced activation, Adv. Exp. Med. Biol. 231, 1-13.