Skip to main content
Log in

Lessons to learn from the cell death and heat shock genes of Caenorhabditis elegans

  • Published:
Acta Biologica Hungarica Aims and scope Submit manuscript

Abstract

The nematode Caenorrhabditis elegans is an applicable experimental system for simulation of complex biochemical processes of mammalian cells and tissues. The genetic pathway of programmed cell death (PCD) has been partially clarified in the nematode. Analysis of cell death genes of C. elegans led to the conclusion that PCD is conserved in the animal kingdom. Our intention is to study the role of tissue transglutaminase and heat shock proteins in the process of PCD. Tissue transglutaminase is often observed to be induced and activated during the molecular mechanism of PCD. The connection between the heat shock proteins and PCD is not well understood, but it is clear that many apoptosis inducers lead to increased synthesis of heat shock proteins and production of heat shock proteins is coupled with the appearance of apoptosis in numerous experimental systems. Our preliminary observations made by studying cell death mutants of C. elegans we suggest that transglutaminase and heat shock proteins are involved in the death program of the nematode.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Arrigo, A. P. (1990) Tumor necrosis factor induced the rapid phosphorylation of the mammalian heat shock protein hsp28. Mol. Cell. Biol. 10, 1276–1280.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Avery, L., Horvitz, H. R. (1987) A cell that dies during wild-type C. elegans development can function as a neuron in ced-3 mutant. Cell 51, 1071–1078.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Blumenthal, T. (1995) Trans-splicing and polycistronic transcription in Caenorhabditis elegans. TIGS 11, 132–135.

    Article  CAS  Google Scholar 

  4. Candido, E. P. M., Jones, D. (1996) Transgenic Caenorhabditis elegans strains as biosensors. Tibtech. 14, 125–128.

    Article  CAS  Google Scholar 

  5. Chinnaiyan, A. M., Orth, K., O’Rourke, K., Duan, H., Poirer, G. G., Dixit, V. M. (1996) Molecular ordering of the cell death pathway. J. Biol. Chem. 271, 5473–5476.

    Google Scholar 

  6. Ciechanover, A. (1994) The ubiquitin-proteasome proteolytic pathway. Cell 79, 13–21.

    Article  CAS  PubMed  Google Scholar 

  7. Dalley, B. K., Colomb, M. (1992) Gene expression in the Caenorhabditis elegans dauer larva: developmental regulation of hsp90 and other genes. Dev. Biol. 151, 80–90.

    Article  CAS  PubMed  Google Scholar 

  8. Deshaies, R. J. (1995) Make it or break it: ubiquitin-dependent proteolysis in cellular regulation. TICB 5, 428–434.

    Article  CAS  Google Scholar 

  9. Desjardins, L. M., MacManus, J. P. (1995) Stress proteins during apoptosis. “Heat Schok (Stress) Proteins in Biology and Medicine”. Meeting B6-303, p. 216.

    Google Scholar 

  10. Driscoll, M. (1995) Methods for the study of cell death in the nematode Caenorhabditis elegans. Methods in Cell Biology 46, 323–353.

    Article  CAS  PubMed  Google Scholar 

  11. Elia, G., Santoro, M. G. (1994) Regulation of heat shock protein synthesis by quercetin in human erytholeukaemia cells. Biochem. J. 300, 201–209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ellis, R. E., Yuan, J., Horvitz, H. R. (1991) Mechanism and functions of cell death. Annu. Rev. Cell. Biol. 7, 663–698.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Ellis, R. E., Jacobson, D. M., Horvitz, H. R. (1991) Two C. elegans genes control the programmed deaths of specific cells in the pharynx. Development 112, 591–603.

    CAS  PubMed  Google Scholar 

  15. Ellis, H. M., Horvitz, H. R. (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell 44, 817–829.

    Article  CAS  PubMed  Google Scholar 

  16. Ellis, H. M., Horvith, H. R. (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell 44, 817–829.

    Article  CAS  PubMed  Google Scholar 

  17. Faucher, C., Capdevielle, J., Canal, I., Ferrara, P., Mazarguil, H., McGuire, W. L., Darbon, J-M. (1993) The 28-kDa protein whose phosphorylation is induced by protein kinase C activators in MCF-7 cells belongs to the family of low molecular mass heat shock proteins and is the estrogen-regulated 24-kDa protein. J. Biol. Chem. 268, 15168–15173.

    CAS  PubMed  Google Scholar 

  18. 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 IL-1β-converting enzyme. J. Biol. Chem. 269, 30761–30764.

    CAS  PubMed  Google Scholar 

  19. Fésűs, L., Thomazy, 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.

    Article  PubMed  Google Scholar 

  20. Fésűs, L., Mádi, A., Balajthy, Z., Nemes, Z., Szondy, Z. (1996) Transglutaminase induction by various cell death and apoptosis pathways. Experientia 52, 942–949.

    Article  PubMed  Google Scholar 

  21. Fésűs, L., Davies, P. J. A., Piacentini, M. (1991) Apoptosis: molecular mechanism in programmed cell death. Eur. J. Cell Biol. 56, 170–177.

    PubMed  Google Scholar 

  22. Filippovich, I., Sorokina, N., Khanna, K. K., Lavin, M. F. (1994) Butirate induced apoptosis in lymphoid cells preceded by transient overexpression of hsp70 mRNA. BBRC 198, 257–265.

    CAS  PubMed  Google Scholar 

  23. 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.

    Article  CAS  PubMed  Google Scholar 

  24. Freshnety, N. W., Rawlinson, L., Guesdon, F., Hsuan, J., Saklatvala, J. (1994) Interleukin-1 activates a novel protein kinase cascade that results in the phosphorylation of hsp27. Cell 78, 1039–1049.

    Article  Google Scholar 

  25. Gagliardini, V. et al. (1994) Prevention of vertebrate neuronal death by crmA gene. Science 263, 826–828.

    Article  CAS  PubMed  Google Scholar 

  26. Galea-Lauri, J., Latchman, D. S., Katz, D. R. (1995) The role of hsp90 in the regulation of apoptosis in myelomonocytic cells. “Apoptosis (Programmed Cell Death)”. Meeting B8-126, p. 272.

    Google Scholar 

  27. Gerber, U., Jucknischke, U., Putzien, S., Fuchsbauer, K. (1994) A rapid simple method for the purification of transglutaminase from Streptovercillum mobaraense. Biochem. J. 299, 825–829.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Glover, L. A., Lindsay, J. G. (1992) Targeting proteins to mitochondria: a current review. Biochem. J. 284, 609–620.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Graham, R. W., Jones, D., Candido, E. P. M. (1989) UbiA, the major polyubiquitin locus in Caenorhabditis elegans, has unusual structural features and is constitutively expressed. Mol. Cell Biol. 9, 268–277.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Graham, R. W., VanDoren, K., Bektesh, S., Candido, P. M. (1988) Maturation of the major ubiquitin gene transcript in Caenorhabditis elegans involves the acquisition of a trans-spliced leader. J. Biol. Chem. 263, 10415–10419.

    CAS  PubMed  Google Scholar 

  31. Guven, K., De Pomerai, D. (1995) Differential expression of hsp70 proteins in response to heat and cadmium in Caenorhabditis elegans. J. Thermal Biol. 20, 355–363.

    Article  CAS  Google Scholar 

  32. Hedgecock, E. M., Sulston, J. E., Thomson, J. N. (1983) Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans. Science 220, 1277–1279.

    Article  CAS  PubMed  Google Scholar 

  33. Hengartner, M. O., Horvitz, R. H. (1994) C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 76, 665–676.

    Article  CAS  PubMed  Google Scholar 

  34. Hengartner, M. O., Horvitz, H. R. (1994) Activation of C. elegans cell death protein CED-9 by an aminoacid substitution in a domain conserved in BCL-2. Nature 369, 318–320.

    Article  CAS  PubMed  Google Scholar 

  35. 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.

    Article  CAS  PubMed  Google Scholar 

  36. Heschl, M. F. P., Baillie, D. L. (1990) The hsp70 multigene family of Caenorhabditis elegans. Comp. Biochem. Physiol. 96B, 633–637.

    CAS  Google Scholar 

  37. Hockertz, M. K., Clark-Lewis, I., Candido, E. P. M. (1991) Studies of small heat shock proteins of Caenorhabditis elegans using anti-peptide antibodies. FEBS Letters 280, 375–378.

    Article  CAS  PubMed  Google Scholar 

  38. Jones, D., Candido, E. P. M. (1993) Novel ubiquitin-like ribosomal protein fusion genes from the nematodes Caenorhabditis elegans and Caenorhabditis briggsae. J. Biol. Chem. 268, 19545–19551.

    CAS  PubMed  Google Scholar 

  39. Jones, D., Russnak, R. H., Candido, E. P. M. (1986) Structure, expression and evolution of a heat shock gene locus in Caenorhabditis elegans that is flanked by repetitive elements. J. Biol. Chem. 261, 12006–12015.

    CAS  PubMed  Google Scholar 

  40. Karlseder, J., Wissing, D., Holzer, G., Orel, L., Sliutz, G., Auer, H., Jaattala, M., Simon, M. M. (1996) Hsp70 overexpression mediates the escape of a doxorubicin-induced G2 cell cycle arrest. BBRC 220, 153–159.

    CAS  PubMed  Google Scholar 

  41. Kaur, P., Welch, W. J., Saklatava, J. (1989) Interleukin-1 and tumor necrosis factor increase the phosphorylation of the small heat shock protein. Effects in fibroblasts, HepG2 and U937 cells. FEBS Lett. 258, 269–273.

    CAS  Google Scholar 

  42. Kerr, J. F. R., Wyllie, A. H., Currie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Chancer 26, 239–257.

    Article  CAS  Google Scholar 

  43. Klein, J. D., Guzman, E., Kuehn, G. D. (1992) Purification and partial characterization of transglutaminase from Physarum polycephalum. J. Bacteriology 173, 2599–2605.

    Article  Google Scholar 

  44. 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-lβ-converting enzyme. Genes. Dev. 8, 1613–1626.

    Article  CAS  PubMed  Google Scholar 

  45. Larsen, P. (1993) Aging and resistance to oxidative damage in Caenorhabditis elegans. PNAS 90, 8905–8909.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Leroux, M. R., Candido, E. P. M. (1995) Molecular analysis of Caenorhabditis elegans tcp-1, a gene encoding a chaperonin protein. Gene 156, 241–245.

    Article  CAS  PubMed  Google Scholar 

  47. Lewis, V. A., Hynes, G. M., Zheng, D., Saibil, H., Willison, K. (1992) T-complex polypeptide-1 is a subunit of a heteromeric particle in the eukariotic cytosol. Nature 358, 249–252.

    Article  CAS  PubMed  Google Scholar 

  48. Lindquist, S. (1986) The heat shock response. Annu. Rev. Biochem. 55, 1151–1191.

    Article  CAS  PubMed  Google Scholar 

  49. Lithgow, G. J., White, T., Melov, S., Johnson, T. E. (1995) Thermotolerance and extended life-span conferred by single-gene mutation and induced by thermal stress. PNAS 92, 7540–7544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lorand, L., Conrad, S. M. (1984) Transglutaminase. Cell Biochem. 58, 9–35.

    Article  CAS  Google Scholar 

  51. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Mampuru, L. J., Chen, S. J., Kallenik, J. L., Bradley, M. E., Lee, T. C. (1996) Analysis of events associated with serum deprivation-induced apoptosis in C3H/so18 muscle satellite cells. Exp. Cell Res. 226, 372–380.

    Article  CAS  PubMed  Google Scholar 

  53. Martin, D. P., Schmidt, R. E., Distefano, P. S., Lowry, O. H., Carter, J. G., Johnson, E. M. (1988) Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106, 829–844.

    Article  CAS  PubMed  Google Scholar 

  54. Martin, G. M., Austad, S. N., Johnson, T. E. (1996) Genetic analysis of aging: role of oxidative stress and environmental stresses. Nature Genetics 13, 25–34.

    Article  CAS  PubMed  Google Scholar 

  55. Martinus, R. D., Ryan, M. T., Naylor, D. J., Herd, S. M., Hoogengard, N. J., Hoj, B. B. (1995) Role of chaperones in the biogenesis and maintenance of the mitochondrion. The FASEB J. 9, 371–378.

    Article  CAS  PubMed  Google Scholar 

  56. Mehlen, P., Mehlen, A., Guillet, D., Preville, X., Arrigo, A.-P. (1995) Tumor necrosis factor induces phosphorylation, cellular localization, and oligomerization of human hsp 27, a stress protein that confers cellular resistance to this cytokine. J. Cell Biochem. 58, 248–259.

    Article  CAS  PubMed  Google Scholar 

  57. Mehlen, P., Schulze-Osthoff, K., Arrigo, A.-P. (1996) Small heat shock proteins as novel regulators of apoptosis. J. Biol. Chem. 271, 16510–16514.

    Article  CAS  PubMed  Google Scholar 

  58. Miglioratti, G., Nicoletti, I., Crociccio, F., Pagliacci, M. C., D’Adamio, L., Riccardi, C. (1992) Heat shock induces apoptosis in mouse thymocytes and protects them from glucocorticoid-induced cell death. Cell. Immunol. 143, 348–356.

    Article  Google Scholar 

  59. Minowada, G., Welch, W. (1995) Variation in the expression and or phosphorylation of the human low molecular weight stress protein during in vitro cell differentiation. J. Biol. Chem. 270, 7047–7054.

    Article  CAS  PubMed  Google Scholar 

  60. Miura, M., Zhu, H., Rotello, R., Hartweig, E., Yuan, J. (1993) Induction of Apoptosis in fibroblasts by IL-1β-coverting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 75, 653–660.

    Article  CAS  PubMed  Google Scholar 

  61. Morimoto, R., Tissieres, A., Gheorgopoulos, C. (eds) (1994) The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor.

  62. Mossar, D. D., Martin, L. H. (1992) Induced thermotolerance to apoptosis in a human T lymphocyte cell line. J. Cell. Physiol. 151, 561–570.

    Article  Google Scholar 

  63. 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, 11074–11081.

    Google Scholar 

  64. Nancy, J. B. et al. (1995) Inhibition of ICE family proteases by baculoviros antiapoptotic protein p35. Science 269, 1885–1888.

    Article  Google Scholar 

  65. 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, 19308–19312.

    CAS  PubMed  Google Scholar 

  66. Page, A. P., MacNiven, K., Hengartner, M. O. (1996) Cloning and biochemical characterization of cyclophilin homologous from the free-living nematode Caenorhabditis elegans. Biochem. J. 317, 179–185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Parsell, D. A., Lindquist, S. (1993) The function of heat-shock proteins in stress-tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genetics 27, 437–478.

    Article  CAS  Google Scholar 

  68. Poccia, F., Piselli, P., Vendetti, S., Bach, A., Amendola, A., Placido, R., Colizzi, V. (1996) Heat-shock protein expression on the membrane of T cells undergoing apoptosis. Immunology 88, 6–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 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. Morph. 67, 89–100.

    Google Scholar 

  70. Russnak, R. H., Candido, E. P. M. (1985) Locus encoding a family of small heat shock genes in Caenorhabditis elegans: two genes duplicated to form a 3.8 kilobase inverted repeat. Mol. Cell Biology 5, 1268–1278.

    Article  CAS  Google Scholar 

  71. Russnak, R. H., Candido, E. P. M. (1983) Cloning and analysis of cDNA sequences coding for two 16 kilodalton heat shock proteins (hsps) in Caenorhabditis elegans: homology with the small hsps of Drosophila. Nucleic Acid Res. 11, 3187–3205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Samali, A., Cotter, T. G. (1996) Heat shock proteins increase resistance to apoptosis. Experimental Cell Res. 223, 163–170.

    Article  CAS  Google Scholar 

  73. Sanders, S. L., Whitfield, K. M., Vogel, J. P., Rose, M. D., Schekman, R. W. (1992) Sec61p and BiP directly facilitate polypeptide translocation into ER. Cell 69, 353–365.

    Article  CAS  PubMed  Google Scholar 

  74. Seo, J-S., Park, Y-M., Kim, J-I., Shim, E-H., Kim, C-W., Jang, J-J., Kim, S-H., Lee, W-H. (1996) T-cell lymphoma in transgenic mice expressing hsp 70 gene. BBRC 218, 582–587.

    CAS  PubMed  Google Scholar 

  75. Shibanuma, M., Kuroki, T., Nose, K. (1992) Cell-cycle dependent phosphorylation of hsp28 by TGF B1 and H2O2 in normal mouse osteoblastic cells (MC3T3-E1), but not in their rastransformants. BBRC 187, 1418–1425.

    CAS  PubMed  Google Scholar 

  76. Singer, M. A., Hortsch, M., Goodman, C. S., Bentley, D. (1992) Annulin, a protein expressed at limb segment boundaries in the grasshopper embrio, is homologous to protein cross-linking transglutaminases. Dev. Biol. 154, 143–159.

    Article  CAS  PubMed  Google Scholar 

  77. Singh, R. N., Mehta, K. (1994) Purification and characterization of a novel transglutaminase from filarial nematode Brugia malayi. Eur. J. Bioch. 225, 625–634.

    Article  CAS  Google Scholar 

  78. Snutch, T. P., Baillie, D. L. (1983) Alteration in the pattern of gene expression following heat shock in the nematode Caenorhabditis elegans. Can. J. Biochem. Cell Biol. 61, 480–487.

    Article  CAS  PubMed  Google Scholar 

  79. Spector, N. L., Mehlen, P., Ryan, C., Hardy, L., Samson, W., Levine, H., Nadler, L. M., Fabre, N., Arrigo, A-P. (1994) Regulation of the 28 kDa heat shock protein by retinoic acid during the differentiation of human leukemic HL-60 cells. FEBS Lett. 337, 184–188.

    Article  CAS  PubMed  Google Scholar 

  80. Steller, H. (1995) Mechanism and genes of cellular suicide. Science 267, 1445–1449.

    Article  CAS  PubMed  Google Scholar 

  81. Stringham, E. G., Candido, E. P. M. (1994) Transgenic hspl6-lacZ strains of the soil nematode Caenorhabditis elegans as biological monitors of environmental stress. Environ. Toxic. Chemistry 13, 1211–1220.

    Article  CAS  Google Scholar 

  82. Sugimoto, A., Hozak, R. R., Nakashima, T., Nishimoto, T., Rothman, J. H. (1995) dad-1 an endogenous programmed cell death suppressor in Caenorhabditis elegans and vertebrates. EMBO J. 14, 4434–4441.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Sugimoto, A., Friesen, P. D., Rothman, J. H. (1994) Baculovirus p35 prevents developmentally programmed cells death and rescues a ced-9 mutant in the nematode Caenorhabditis elegans. EMBO J. 13, 2023–2028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. 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.

    Article  CAS  PubMed  Google Scholar 

  85. Sulston, J. E., Horvitz, H. R. (1977) Post-embryonic cell lineages of the nematode Caenorhabditis elegans. Dev. Biol. 82, 110–156.

    Article  Google Scholar 

  86. Tokunaga, F., Yamada, M., Miyata, T., Ding, Y. L., Hiranga-Kawabata, M., Muta, T., Iwanaga, S. (1993) Linulus hemocyte transglutaminase. J. Biol. Chem. 268, 252–261.

    CAS  PubMed  Google Scholar 

  87. Trent, C., Tsung, N., Horvitz, H. R. (1983) Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics 104, 619–647.

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Tsujimoto, Y., Croce, C. M. (1986) Analysis of the structure, transcripts and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc. Natl. Acad. Sci. USA 83, 5214–5218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Vanfleteren, J. R. (1993) Oxidative stress and ageing in Caenorhabditis elegans. Biochem. J. 292, 605–608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. 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.

    Article  CAS  PubMed  Google Scholar 

  91. Wang, L., Miur, M., Bergeron, L., Zhu, H., Yuan, J. (1994) ICH-1, and ICE/ced-3 related gene, encodes both positive and negative regulators of programmed cell death. Cell 78, 739–750.

    Article  CAS  PubMed  Google Scholar 

  92. Waterston, R., Sulston, J. (1995) The genome of Caenorhabditis elegans. Proc. Natl. Acad. Sci. 92, 10836–10840.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Wei, Y., Zhao, X., Kariya, Y., Fukata, H., Teshigawara, K., Uchida, A. (1994) Induction of apoptosis by quercetin: involvement of heat shock proteins. Cancer Res. 54, 4952–4957.

    CAS  PubMed  Google Scholar 

  94. Welch, W. J. (1992) Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol. Rev. 72, 1063–1081.

    Article  CAS  PubMed  Google Scholar 

  95. Weraarchakul-Boonmark, N. et al. (1992) Cloning and expression of chicken erythrocyte transglutaminase. Proc. Natl. Acad. Sci. USA 89, 9804–9808.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Wood, W. B. (ed.) (1988) The Nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.

    Google Scholar 

  97. Xue, D., Horvitz, R. H. (1995) Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35. Nature 377, 248–251.

    Article  CAS  PubMed  Google Scholar 

  98. Yasueda, H., Nakanishi, K., Kumazawa, Y., Nagase, K., Motoki, M., Matsui, H. (1995) Tissue-type transglutaminase from red sea bream (Pagrus major). Seguence analysis of the cDNA and functional expression in E. coli. Eur. J. Biochem. 232, 411–419.

    Article  CAS  PubMed  Google Scholar 

  99. 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.

    Article  CAS  PubMed  Google Scholar 

  100. Yuan, J. (1996) Evolutionary conversation of a genetic pathway of programmed cell death. J. Cell. Bioch. 60, 4–11.

    Article  CAS  Google Scholar 

  101. Yuan, J., Horvitz, H. R. (1992) The Caenorhabditis elegans cell death gene ced-4 encodes a novel protein and is expressed during the period of extensive programmed cell death. Development 116, 309–320.

    CAS  PubMed  Google Scholar 

  102. Yuan, J., Horvitz, H. R. (1990) The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death. Dev. Biol. 138, 33–41.

    Article  CAS  PubMed  Google Scholar 

  103. Zhen, M., Schein, J. E., Baillie, D. L., Candido, E. P. M. (1996) An essential ubiquitin-conjugating enzyme with tissue and developmental specificity in the nematode Caenorhabditis elegans. EMBO J. 15, 3229–3237.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Dedicated to the memory of Professor Gábor Szabó.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mádi, A., Punyiczki, M. & FéSűs, L. Lessons to learn from the cell death and heat shock genes of Caenorhabditis elegans. BIOLOGIA FUTURA 48, 303–318 (1997). https://doi.org/10.1007/BF03543202

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03543202

Keywords

Navigation