Abstract
Earthworms and other organisms have deployed several strategies essential for maintaining and perpetuating species and one is the immune system that functions effectively against microbes. Effector activity against experimental antigens such as cancer cells is mediated by leukocytes and molecules that they synthesize and secrete (Cooper, et al., 1995; Cossarizza et al., 1995; 1996; Quaglino, et al., 1996; Cooper et al., 1992; 1999; Bilej et al., 1995; Kauschke et al., 1997). Current work emphasizes the capacity of coelomic fluid to effect lysis by means of a protein which has been referred to as Eiseniapore (Lange et al., 1997). Clearly the earthworm’s importance in understanding this aspect of invertebrate humoral immunity is significant as indicated by the recent increase in molecular studies relevant to lysis, (Lassegues et al., 1997; Milochau et al., 1997; Sekizawa, et al., 1997; Yamaji et al., 1998), its apparent regulation by serine proteases (Roch et al., 1997) and its possible relation to humoral agglutinins (H1, H2, H3), (Eue et al., 1997) and those antimicrobial peptides that are not hemolytic (Cho et al., 1998). These research groups propose the names fetidin, lysin, and now Eiseniapore, and perhaps perforin (Komiyama et al., 1997). From molecular analyses, these groups have cloned cDNAs which encode the cytolytic proteins and confirmed the activities of recombinant proteins. Certain common characteristics seem to be shared. As an example, their work reveals that the 40kDa fetidin has at least four isoforms with different isoelectric points and lysenin represents two isoforms of molecular masses of 41 and 42 kDa. This suggests that coelomic fluid of Eisenia fetida contains several sphingomyelin-binding cytolytic proteins with molecular masses around 40 kDa.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Acha-Orbea, H., Scarpellino, L., Hertig, S., Dupuis, M., and Tschopp J. (1990) Inhibition of lymphocyte mediated cytotoxicity by perform antisense oligonucleotides. EMBO J., 9: 3815–3819.
Bcschin A, Bilej M, Hanssens F, Raymakers J, Van Dyck E, Revets H, Brys L, Gomez J, De Baetselier P, and Timmermans M. (1998) Identification and cloning of a glucan-and lipopolysaccharide-binding protein from Eisenia foetida earthworm involved in the activation of prophenoloxidase cascade. J Bio Chem 273:24948–24954.
Bilej, M., Brys, L., Beschin, A., Lucas, R., Vercauteren, E., Hanusova, R., and De Baetselier, P. (1995) Identification of a cytolytic protein in the coelomic fluid of Eisenia foetida earthworms. Immunol. Lett. 45:123–128.
Brumback, R.A. (1981) The neuralmuscular junction. Part 1: physiology and the effects of drugs and toxins. Am. Fam. Physician 23, 188–192.
Canicatti, C. (1990) Hemolysis: Pore-forming proteins in invertebrates. Experientia 46: 239–244.
Cho J. H., Park, C. B., Yoon, Y. G., and Kim, S. C. (1998) Lumbricin I, a novel proline-rich antimicrobial peptide from the earthworm: purification, eDNA cloning and molecular characterization. Biochem Biophys Acta. 1408:67–76.
Cooper, E. L., Cossarizza, A., Suzuki, M. M., Salvioli, S., Capri, M., Quaglino, D., and Franceschi, C. (1995) Autogeneic but not allogeneic earthworm effector coelomocytes kill the mammalian tumor target K562. Cell. Immunol. 166:113–122.
Cooper, E.L., and Roch, P. (1992). The capacities of earthworms to heal wounds and to destroy allografts are modified by polychlorinated biphenyls (PCB). J. Invert. Pathol. 60: 59–63.
Cooper, E.L., Cossarizza, A., Kauschke, E., and Franceschi, C. (1999) Cell adhesion and the immune system: a case study using earthworms. Micro. Res. Tech. 44, 237–253.
Cooper, E.L., Rinkevich, B., Uhlenbruck, G., and Valembios, P. (1992) Invertebrate immunity: another viewpoint. Scand. J. Immunol. 35, 247–26.
Cossarizza, A., Cooper, E. L., Quaglinio, D., Salvioli, S., Kalachnikova, G., and Franceschi, C., (1995) Mitochondrial mass and membrane potential in coelomocytes from the earthworm Eisenia foetida: Studies with fluorescent probes in single intact cells. Biochem. Biophys. Res. Comm. 214: 503–510.
Cossarizza, A., Cooper, E. L., Suzuki, M. M., Salvioli, S., Capri, M., Gri, G., Quaglino, D., and Franceschi, C. (1996) Earthworm leukocytes that arc not phagocytic and cross-react with several human epitopes can kill human tumor cell lines. Exptl. Cell Res. 224: 174–182.
Dennert, G. and Podack, E.R. (1983) Cytolysis by H-2-specific T killer cells: Assembly of tubular complexes on target membranes. J. Exp. Med. 157: 1483–1495.
Dourmashkin, R.R., Deteix, P., Simone C.B., and Henkart, P. (1980) Electron microscopic demonstration of lesions in target cell membranes associated with antibody-dependent cellular cytotoxicity. Clin. Exp. Immunol. 42: 554–60.
Eue, I., Kauschke, E., Mohrig, W., and Cooper, E. L. (1998) Isolation and characterization of earthworm hemolysins and agglutinins. Dev. Comp. Immunol., 22: 13–25.
Ferrarini, M. and Grossi, C.E. (1985). Ultrastmcture and cytochemistry of the human large granular lymphocytes. In: Immunobiology of natural killer cells. Lotzová, E. and Herbermann, R. B. (eds) CRC Press, Boca Raton, FL. 1: 33–43.
Garcia-Sanz, J.A., Plaetinck, G., Velotti, F., Masson, D., Tschopp, J., MacDonald, H.R., and Nabholz, M. (1987) Perforin is present only in normal activated Lyt2+ T-lymphocytes and not in L3T4+ cells, but serine protease granzyme A is made by both subsets. EMBO J. 6: 933–938.
Gordon, D., Martin-Eauclaire, M.F., Cestele, S., Kopeyan, C., Cartier, E., Khalifa, R.B., Pelhate, M., and Rochat, H. (1996) Scorpin toxins affecting sodium current inactivation bind to distinct homologous receptor sites on rat brain and insect sodium channels. J. Biol. Chem. 271, 8034–8045.
Henkart, P.A. (1985) Mechanisms of lymphocyte-mediated cytotoxicity. Ann. Rev. Immun. 3: 31–58.
Jenne, D.E and Tschopp, J. (1988) Granzymes a family of serine proteases released from granules of cytolytic T lymphocytes upon T cell receptor stimulation. Immunol. Rev. 103: 53–71.
Kägl, D., Ledermann, B., Burkl, K., Seller, P., Odermatt, B., Olsen, K. J., Podack, E. R., Zinkemagel, R. M., and Hengartner, H. (1994) Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perform -deficient mice. Nature. 369: 31–37.
Kaminski, H.J., Suarez, J.I., and Ruff, R.L. (1997) Neuromuscular junction physiology in myasthemia gravis: isoforms of the acetylcholine receptor in extraocular muscle and the contribution of sodium channels to the safety factor. Neurology 48, 8–17.
Kauschke, E., Pagliara, E, Stabili, L., and Cooper, E. L. (1997) Characterization of proteolytic activity in coelomic fluid of Lumbricus terrestris. Comp. Biochim. Physiol. 116B: 235–242.
Kawasaki, A., Shinkai, Y., Yagita, H., and Okumura, E. (1992) Expression of perforin in murine natural killer cells and cytotoxic T lymphocytes in vivo. Eur. J. Immun. 22: 1215–1219.
Komiyama, K., Yoshimura, M., Iwase, T., Sato, J, Okumura, K., Cooper, E. L., and Moro, I. (1997) Identification of perforin gene and its protein in the earthworm coelomocytes. Dev. Comp. Immunol. 21:115.
Kupfer, A., Dennert, G., and Singer, S.J. (1985) The reorientation of the Golgi apparatus and the microtubuleorganizing center in the cytotoxic effector cell is a prerequisite in the lysis of bound target cells. J. Mol. Cell. Immunol. 2: 37–49.
Lange, S., Kauschke, E., Mohrig, W., and Cooper, E. L. (1999) Biochemical characteristics of eiseniapore, a pore forming protein in the coelomic fluid of earth worms. Eu. J. Biol. Chem. 262: 1–11.
Lange, S., Nübler, Kauschke, E., Lutsch, G., Cooper, E. L., and Herrmann, A. (1997) Interactions of earthworm hemolysin with lipid membranes requires sphingolipids. J. Biol. Chem. 272: 20884–20892.
Lassegues, M., Milochau, A., Doignon, F., Du Pasquier, L., and Valembois, P. (1997) Sequence and expression of an Eisenia-fetida-derived eDNA clone that encodes the 40-kDa fetidin antibacterial protein Eur. J. Biochem. 246: 756–762.
Leipner, C., Tuckova, L., Rejnek, J., and Langner, J. (1993) Serine proteases in coelomic fluid of annelids Eisenia fetida and Lumbricus terrestris. Comp. Biochim. Physiol. 105B: 637–641).
Lichtenheld, M. G., Olsen, K. J., Ping, L., Lowrey, D.M., Hameed, A., Hengartner, H., and Podack, E.R. (1988) Structure and function of human perforin. Nature 335: 448–451.
Mazumder, P.K. and Dube, S. N. (1996) Marine toxins as molecular probes for biological interactions: a review. Indian J. Physiol. Allied Sci. 50, 34–47.
Milochau, A., Lassegues, M., and Valembois, P. (1997) Purification, characterization and activities of two hemolytic and antibacterial proteins from coelomic fluid of the annelid Eisenia fetida andrei. Biochem. Biophys, Acta. 1337: 123–132.
Mueller, C., Gershenfeld, H.K., Lobe, C.G., Okada, C.V., Bleackley, R.C., and Weissman, I.L. (1988) A high proportion ofT lymphocytes that infiltrate H-2-incompatible heart allografts in vivo express genes encoding cytotoxic cell-specific serine proteases, but do not express the MEL-14-defined lymph node homing receptor. J. Exp. Med. 167: 1124–1136.
Mueller, C., Kagi, D., Aebischer, T., Odermatt, B., Held, W., Podack, E.R., Zinkemagel, R.M., and Hengartner, H. (1989) Detection of perforin and granzyme A mRNA in infiltrating cells during infection of mice with lymphocytic choreomeningitis virus. Eur.J. Immunol. 19: 1253–1259.
Nastuk, W.L. (1971) Mechanisms of neuromuscular blockade. Ann. N.Y. Acad. Sci. 183, 171–182
Pagliara, P., Canicatti, C., and Cooper, E.L. (1993) Structure and enzyme content of sea urchin cytolytic granules. Comp. Biochim. Physiol. 106B: 813–818.
Pennington, M.W., Mahnir, V.M., Krafle, D.S., Zaydenberg, I., Byrens, M.E., Khaytin, I., Crowler, K., and Kern, W.R. (1996) Identification of three separate binding sites of SHK toxin, a potent inhibitor of voltage dependent potassium channels in human T-lymphocytes and rat brain. Biochem Biophys. Res. Commun. 219,696–701.
Podack, E.R. (1985) The molecular mechanism of lymphocyte-mediated tumor cell lysis. Immunol. Today 6: 21–27.
Podack, E.R., Hengartner, H., and Lichtenheld, M.G. (1991) A central role of perforin in cytolysis. Ann. Rev. Immunol. 9: 129–157.
Podack, E.R., Lowrey, D.M., Lichtenheld, M., Olsen, K.J., Aebischer, T., Binder, D., Rupp, F., and Hengartner, H. (1988) Structure, function and expression of murine and human perform 1 (P1). Immun. Rev. 103: 203–211.
Polanowski, A. and Wilusz, T. (1996) Serine proteinase inhibitors from insect hemolymph. Acta Biochim Polinica 43: 445–454.
Porchet-Henneré, E., Dugimont, T., and Fischer, A. (1992) Natural killer cells in a lower invertebrate, Nereis diversicolor. Eur. J. Cell Biol. 58: 99–107.
Quaglino, D., Cooper, E. L., Salvioli, S., Capri, M., Suzuki, M. M., Pasquali-Ronchetti, I., Franceschi C., and Cossarizza, A. 1996 Earthworm coelomocytes in vitro: cellular features and “granuloma” formation during cytotoxic activity against the mammalian tumor cell target K562. Eu. J. Cell Biol. 70:278–288.
Roch, P., Ville, P., and Cooper, E. L. (1998) Characterization of a 14 kDa plant-related serine protease inhibitor and regulation of cytotoxic activity in earthworm coelomic fluid. Dev. Comp. Immunol. Dev. Comp. Immunol. 22: 1–12.
Roch, P., Ville, P., and Cooper, E. L. (1998) Characterization of a 14 kDa plant-related serine protease inhibitor and regulation of cytotoxic activity in earthworm coelomic fluid. Dev. Comp. Immunol. Dev. Comp. Immunol. 22: 1–12.
Roch, Ph., Stabili, L., and Pagliara, P. (1991) Purification of three serine proteases from the coelomic cells of earthworms (Eisenia foetida). Comp. Biochim. Physiol. 98B:597–602.
Rouvier, E., Luciani, M.F., and Golstein, P. (1993) Fas involvement in Ca2+-independent T cell-mediated cytotoxicity. J. Exp. Med. 177: 195–200.
Russell, J.H. (1983) Internal disintegration model of cytotoxic lymphocyte-induced target damage. Immunol. Rev. 72: 97–118.
Sekizawa, Y., Kubo, T., Kobayashi, H., Nakajima, T., and Natori, S. (1997) Molecular cloning of cDNA for lysenin, a novel protein in the earthworm Eisenia foetida that causes contraction of rat vascular smooth muscle. Gene 191: 97–102.
Shinkai, Y., Takio, K., and Okumura, K. (1988) Homology of perforin to the ninth component of complement (C9). Nature 334: 525–527.
Shiver, J.W., Su, L., and Henkart, P.A. (1992) Cytotoxicity with target DNA breakdown by rat basophilic leukemia cells expressing both cytolysis and granzyme A. Cell 71: 315–321.
Tschopp, J. and Nabholz, M. (1990) Perform mediated target cell lysis by cytolytic T lymphocytes. Annu. Rev. Immunol. 8: 279–302.
Walsh, C.M., Matloubian, M., Liu, C., Ueda, R., Kurahara, C., Christensen, J., Huang, M.T.F., Young, J.D., Ahmed, R., and Clark, W.R. (1994) Immune function in mice lacking the perforin gene. Proc. Natl. Acad. Sci. USA 91: 10854–10858.
Yamaji A, Sekizawa Y, Emoto K, Sakuraba H, Inoue K, Kobayashi H, and Umeda M. (1998) Lysenin, a novel sphingomyclin-specific binding protein. J. Biol Chem 273: 5300–5306.
Young, J.D.E. (1989) Killing of target cells by lymphocytes: A mechanistic view. Physiol. Rev. 69: 250–314.
Young, J.D.E., Hengartner, H., Podack, E.R., and Cohn, Z.A. (1986) Purification and Characterization of a cytolytic pore-forming protein from granules of cloned lymphocytes with natural killer activity. Cell 44: 849–859.
Young, L.H., Joag, S.V., Zheng, L.M., Lee, C.D., Lee, Y.S., and Young, J.D.E. (1990) Perform mediated myocardial damage in acute myocarditis. Lancet 336: 1019–1021.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2001 Springer Science+Business Media New York
About this chapter
Cite this chapter
Cooper, E.L., Kauschke, E., Cossarizza, A. (2001). Annelid Humoral Immunity: Cell Lysis in Earthworms. In: Beck, G., Sugumaran, M., Cooper, E.L. (eds) Phylogenetic Perspectives on the Vertebrate Immune System. Advances in Experimental Medicine and Biology, vol 484. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1291-2_15
Download citation
DOI: https://doi.org/10.1007/978-1-4615-1291-2_15
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-5481-9
Online ISBN: 978-1-4615-1291-2
eBook Packages: Springer Book Archive