Biochemical characteristics of Eiseniapore, a pore-forming protein in the coelomic fluid of earthworms

European Journal of Biochemistry

Volumn 262, Issue 2, 1999, Pages 547-556

  Lange, Sven ^b   Kauschke, Ellen ^a   Mohrig, Werner ^b   Cooper, Edwin L ^b  

^a UNIVERSITY OF GREIFSWALD   (Germany)

^b Ernst Moritz Arndt Universitat G ^*

Author keywords

Earthworms; Eiseniapore; Phospholipids; Pore formation; Sphingomyelin

Indexed keywords

CALCIUM ION; CYTOLYSIN; EISENIAPORE; LYSOPHOSPHATIDYLCHOLINE; MAGNESIUM ION; SPHINGOMYELIN; UNCLASSIFIED DRUG; VITRONECTIN;

ARTICLE; CHANNEL GATING; CYTOLYSIS; CYTOTOXICITY; EARTHWORM; HEMOLYSIS; IMMUNE SYSTEM; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION;

ANIMALS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HEMOLYSIS; HUMANS; MICROSCOPY, ELECTRON; OLIGOCHAETA; PROTEIN BINDING; PROTEINS;

EID: 0033151944     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1999.00407.x     Document Type: Article

References (95)

1. 1. Cooper, E.L., Stein, E.A. & Wojdani, A. (1984) Recognition receptors in Annelids. In Recognition Proteins, Receptors and Probes: Invertebrates (Cohen, E., ed.), pp. 43-54. A. R. Liss, Inc., New York.
2. 2. Roch, P. (1979) Protein analysis of earthworm coelomic fluid: (1) Polymorphic system of the natural hemolysins of Eisenia fetida. Dev. Com. Immunol. 4, 599-608.
3. 3. Roch, P., Davant, N. & Lassegues, M. (1984) Isolation of agglutinins from lysins in the earthworm coelomic fluid by gel filtration followed chromatofocusing. J. Chromatogr. 290, 231-235.
4. 4. Roch, P., Canicatti, C. & Valembois, P. (1989) Interaction between earthworm hemolysins and sheep red blood cell membranes. Biochim. Biophys. Acta 2, 193-198.
5. 5. Valembois, P., Roch, P., Lassegues, M. & Cassand, P. (1982) Antibacterial activity of the hemolytic system from the earthworm. Eisenia Fetida Andrei. J. Invert. Pathol. 40, 21-27.
6. 6. Lassegues, M., Roch, P. & Valembois, P. (1989) Antibacterial activity of Eisenia fetida andrei coelomic fluid: evidence, induction and animal protection. J. Invert. Pathol. 53, 1-6.
7. 7. Vetvicka, V., Sima, P., Cooper, E.L., Bilej, M. & Roch, P. (1994) Immunology of Annelids, pp. 1-300. CRC Press, Boca Raton, FL.
8. 8. Suzuki, M.M. & Cooper, E.L. (1995) Spontaneous cytotoxic earthworm leukocytes kill K562 tumor cells. Zool. Sci. 12, 443-451.
9. 9. Cossarizza, A., Cooper, E.L., Suzuki, M.M., Salvioli, S., Capri, M., Gri, G., Quaglino, D. & Franceschi, C. (1996) Earthworm leukocytes that are not phagocytic and cross react with several human epitopes can kill human tumor cell lines. Exp. Cell Res. 224, 174-182.
10. 10. Quaglino, D., Cooper, E.L., Salvioloi, S., Capri, M., Suzuki, M.M., Ronchetti, I.P., Franceschi, C. & Cossarizza, A. (1996) Earthworm coelomocytes in vitro: cellular features and granuloma formation during cytotoxic activity against the mammalian tumor cell target K 562. Eur. J. Cell Biol. 70, 278-288.
11. 11. Mohrig, W., Eue, I., Kauschke, E. & Hennicke, F. (1996) Crossreactivity of hemolytic and hemagglutinating proteins in the coelomic fluid of lumbricidae (Annelida). Comp. Biochem. Physiol. 115A, 19-30.
12. 12. Kauschke, E. & Mohrig, W. (1987) Cytotoxic activity in the coelomic fluid of the annelid Eisenia foetida Sav. J. Comp. Physiol. 157, 77-83.
13. 13. Stein, E., Wojdani, A. & Cooper, E.L. (1982) Agglutinins in the earthworm Lumbricus terrestris: naturally and induced. Dev. Comp. Immunol. 6, 407-421.
14. 14. Wojdani, A., Stein, E.A., Lemmi, C.A. & Cooper. E.L. (1982) Agglutinins and proteins in the earthworm, Lumbricus terrestris, before and after injection of erythrocytes, carbohydrates and other materials. Dev. Comp. Immunol. 6, 613-624.
15. 15. Stein, E. & Cooper, E.L. (1983) Carbohydrate and glycoprotein inhibitors of naturally occurring and induced agglutinins from the earthworm Lumbricus terrestris. Comp. Biochem. Physiol. 76B, 197-206.
16. 16. Eue, I., Kauschke, E. & Mohrig, W. (1991) Comparative characterization of lectins in the coelomic fluid of lumbricides. Dev. Comp. Immunol. 15, 75.
17. 17. Bhakdi, S. & Tranum-Jensen, J. (1985) Membrane damage by channel-forming proteins: staphylococcal alpha toxin, streptolysin-O and the C5b-9 complement complex. Biochem. Soc. Symp. 50, 221-233.
18. 18. Buckley, J.T., Wilmsen, H.U., Lesieur, C., Schulze, A., Pattus, F., Parker, M.W. & Van der Goot, F.G. (1995) Protonation of histidine-132 promotes oligomcrization of the channel-forming toxin aerolysin. Biochemistry 34, 16450-16455.
19. 19. Peitsch, M.C. & Tschopp, J. (1991) Assembly of macromolecular pores by immune defense systems. Curr. Opin. Cell Biol. 3, 710-716.
20. 20. Van der Goot, F.G., Pattus, F., Parker, M. & Buckley, J.T. (1993) The cytolytic toxin aerolysin: from the soluble form to the transmembrane channel. Toxicology 87, 19-28.
21. 21. Esser, A.F. (1994) The membrane attack complex of complement. Assembly, structure and cytotoxic activity. Toxicology 87, 229-247.
22. 22. Morgan, B.P. (1995) Physiology and pathophysiology of complement: progress and trends. Crit. Rev. Clin. Lab. Sci. 32, 265-298.
23. 23. Li, J. (1992) Bacterial toxins. Curr. Opin. Struct. Biol. 2, 545-556.
24. 24. Tschopp, J. & Nabholz, M. (1990) Perforin-mediated target cell lysis by cytolytic T lymphocytes. Annu. Rev. Immunol. 8, 279-302.
25. 25. Liu, C.C., Walsh, C.M. & Young, J.D. (1995) Perforin: structure and function. Immunol. Today 16, 194-201.
26. 26. Berke, G. (1997) Killing mechanisms of cytotoxic lymphocytes. Curr. Opin. Hematol. 4, 32-40.
27. 27. Ojcius, D.M. & Young, J.D. (1991) Cytoloytic pore-forming proteins and peptides: is there a common structural motif? Trends Biochem. Sci. 6, 225-229.
28. 28. Tytler, E.M., Segrest, J.P.. Epand, R.M., Nie, S.Q., Epand, R.F., Mishra, V.K.. Venkatachalapathi, Y.V. & Anantharamaiah, G.M. (1993) Reciprocal effects of apolipoprotein and lytic peptide analogs on membranes. Cross-sectional molecular shapes of amphipathic alpha helixes control membrane stability. J. Biol. Chem. 29, 22112-22118.
29. 29. Leippe, M., Ebel, S., Schoenberger, O.L., Horstmann, R.D. & Müller-Eberhard, H.J. (1991) Pore-forming peptide of pathogenic Entamoeba histolytica. Proc. Natl Acad. Sci. USA 88, 7659-7663.
30. 30. Leippe, M., Tannich, E., Nickel, R., van der Goot, G., Pattus, F., Horstmann, R.D. & Müller-Eberhard, H.J. (1992) Primary and secondary structure of the pore-forming peptide of pathogenic Entamoeba histolytica. EMBO 11, 3501-3506.
31. 31. Leippe, M. & Müller-Eberhard, H.J. (1994) The pore-forming peptide of Entamoeba histolytica, the protozoan parasite causing human amoeboiasis. Toxicology 87, 5-18.
32. 32. Leippe, M. (1995) Ancient weapons: NK-lysin, is a mammalian homolog to pore-forming peptides of a protozoan parasite. Cell 83, 17-18.
33. 33. Oka, T., Murata, Y., Nakanishi, T., Yoshizumi, H., Hayashida, H., Ohtsuki, Y., Toyoshima, K. & Hakura, A. (1992) Similarity, in molecular structure and function, between the plant toxin purothionin and the mammalian pore-forming proteins. Mol. Biol. Evol. 9, 707-715.
34. 34. Macek, P., Belmonte, G., Pederzolli, C. & Menestrina, G. (1994) Mechanisms of action of equianatoxin II, a cytolysin from the sea anemone Actina equina L. belonging to the family of actinoporins. Toxicology 87, 1-3.
35. 35. Hatakeyama, T., Nadatoma, H. & Yamasaki, N. (1995) Interaction of the hemolytic lectin CEL-III from the marine invertebrate Cucumaria echinata with the erythrocyte membrane. J. Biol. Chem. 270, 3560-3564.
36. 36. Horta, M.F. (1997) Pore-forming proteins in pathogenic protozoan parasites. Trends Microbiol. 5, 363-366.
37. 37. Andrews, N.W., Abrams, C.K., Slatin, S.L. & Griffiths, G. (1990) A T. cruzi-secreted protein immunologically related to the complement component C9: evidence for membrane pore-forming activity at low pH. Cell 7, 277-287.
38. 38. Canicatti, C. (1990) Hemolysins: poreforming proteins in invertebrates. Experientia 3, 239-244.
39. 39. Porchet-Hennere, E., Dugimont, T. & Fischer, A. (1992). Natural killer cells in a low invertebrate, Nereis diversicolor. Eur. J. Cell Biol. 1, 99-107.
40. 40. Laclette, J.P., Shoemaker, C.B., Richter, D., Arcos, L., Pante, N., Cohen, C., Bing, D. & Nicholson-Weller, A. (1992) Paramyosin inhibits complement Cl. J. Immunol. 1, 124-128.
41. 41. Armstrong, P.B., Armstrong, M.T. & Quingley, P. (1993) Involvement of alpha-macroglobulin and C-reactive protein in a complement-like hemolytic system in the arthropod, Limulus polyphemus. Mol. Immunol. 30, 929-934.
42. 42. Day, N.K.B., Gewurz, H., Johannsen, R., Finstad, J. & Good, R.A. (1970) Complement and complement-like activity in lower vertebrates and invertebrates. J. Exp. Med. 132, 941-950.
43. 43. Bertheussen, K. (1983) Complement-like activity in sea urchin coelomic fluid. Dev. Comp. Immunol. 1, 21-31.
44. 44. Lange, S., Nüßler, F., Kauschke, E., Lutsch, G., Cooper. E.L. & Herrmann, A. (1997) Interaction of earthworm hemolysin with lipid membranes requires sphingolipids. J. Biol. Chem. 272, 20884-20892.
45. 45. Suelter, C.H. (1990) A Practical Guide To Enzymology. Fischer, Stuttgart and New York.
46. 46. Woodle, M.C. & Papahadjopoulos, D. (1989) Liposome preparation and size characterization. Methods Enzymol. 171, 193-217.
47. 47. Schwoch, G. & Passow, H. (1973) Preparation and properties of human erythrocyte ghost. Mol. Cell Biochem. 2, 197-218.
48. 48. Pomorski, T., Herrmann, A., Zachowski, A., Devaux, P.F. & Müller, P. (1994) Rapid determination of the transbilaycr distribution of NBD-phospholipids in erythrocyte membranes with dithionite. Mol. Membr. Biol. 11, 39-44.
49. 49. Lejeune, A., Moorjani, M., Gicquaud, C., Lacroix, J., Poyet, P. & Gaudreault, R. (1994) Nanoerythrosome, a new derivative of erythrocyte ghost: preparation and antineoplastic potential as drug carrier for daunorubicin. Anticancer Res. 14, 915-919.
50. 50. Bhakdi, S. & Tranum-Jensen, J. (1984) Mechanism of complement cytolysis and the concept of channel-forming proteins. Philos. Trans. R. Soc. London Ser. B. Biol. Sci. 306, 311-324.
51. 51. Moran, O., Zegarra-Moran, O., Virginio, C., Gusmani, L. & Rottini, G.D. (1992) Physical characterization of the pore forming cytolysin from Gardnerella vaginalis. FEMS Microbiol. Immunol. 5, 63-69.
52. 52. Cooper, E.L., Cossarizza, A., Suzuki, M.M., Salvioli, S., Capri, M., Quaglino, D. & Franceschi, C. (1995) Autogenic but not allogenic earthworm effector coelomocytes kill the mammalian tumor target K562. Cell Immunol. 166, 113-122.
53. 53. Mohrig, W., Lange, S., Kauschke, E., Preusse, K. & Cooper, E.L. (1997) Inhibitor controlled hemolytic activity in the coelomic fluid of earthworms. Dev. Comp. Immunol. 21, 116.
54. 54. Alouf, J.E. & Geoffroy, C. (1991) The family of the antigenically-related, cholesterol-binding ('sulphydryl-activated') cytolytic toxins. Sourcebook of Bacterial Protein Toxins (Alouf, J.E. & Freer, J.H., eds). Academic Press, London.
55. 55. Mlinar, B. & Enyeart, J.J. (1993) Block of current through T-type calcium channels by trivalent metal cations and nickel in neural rat and human cells. J. Physiol. (London) 469, 639-652.
56. 56. Walker, B., Kasianowicz, J., Krishnasastry, M. & Bayley, H. (1994) A pore-forming protein with a metal-actuated switch. Protein Eng. 7, 655-662.
57. 57. Griem, P. & Gleichmann, E. (1995) Metal ion induced autoimmunity. Curr. Opin. Immunol. 7, 831 -838.
58. 58. Griem, P., Panthel, K., Kalbacher, H. & Gleichmann, E. (1996) Alteration of a model antigen by Au (III) leads to T cell sensitization to cryptic peptides. Eur. J. Immunol. 26, 279-287.
59. 59. Harth, M. (1981) Modulation of immune responses of gold salts. Agents Actions (Suppl. 8), 465-476.
60. 60. Bratt, J. & Palmhlad, J. (1996) Inhibition of neutrophil-dependent cytotoxicity for human endothelial cells by antirheumatic drugs. J. Lab. Clin. Med. 128, 552-560.
61. 61. Lester, D.S. & Brumfeld, V. (1991) Divalent cation-induced changes in conformation of protein kinase C. Biophys. Chem. 39, 215-224.
62. 62. Arnold, F.H. & Zhang, J.H. (1994) Metal-mediated protein stabilization. Trends Biotechnol. 12, 189-192.
63. 63. Chai, L., Chu, Y., Wilson, S.E. & Schlender, K.K. (1995) A metal-dependent form of protein phosphatase 2A. Biochem. Biophys. Res. Commun. 208, 274-279.
64. 64. Regan, L. (1995) Protein design: novel metal-binding sites. Trends Biochem. Sci. 20, 280-285.
65. 65. Ireland, M.P. (1978) Heavy metal binding properties of earthworms chloragosomes. Acta Biol. Acad. Sci. Hung. 29, 385-394.
66. 66. Prento, P. (1979) Metals and phosphate in the chloragosomes of Lumbricus terrestris and their possible physiological significance. Cell Tissue Res. 196, 123-134.
67. 67. Podack, E.R., Kolb, W.P. & Müller-Eberhard, H.J. (1978) The C5b6 complex: formation, isolation and inhibition of its activity by lipoprotein and the S-protein of human serum. J. Immunol. 120, 1841-1848.
68. 68. Podack, E.R., Preissner, K. & Müller-Eberhard, H.J. (1983) Inhibition of C9 polymerization by S-protein. Immunobiology 164, 149-154.
69. 69. Tschopp, J., Masson, D. & Peitsch, M. (1987) Molecular mechanisms of C9 polymerization and its inhibition by S-protein. Complement 4, 232-237.
70. 70. Tschopp, J., Masson, D., Schäfer, S., Peitsch, M. & Preissner, K.T. (1988) The heparin binding domain of S-protein/vitronectin binds to C7, C8 and C9 and perforin from cytolytic T-cells and inhibits their lytic activities. Biochemistry 27, 4103-4109.
71. 71. Lange, S., Nüßler, F., Kauschke, E. & Herrmann, A. (1994) Interaction of hemolysin of earthworm with erythrocyte and phospholipid membranes. Annual Meeting of German Society of Biophysics, Berlin, p. 58.
72. 72. Masson, D. & Tschopp, J. (1985) Isolation of a lytic, pore-forming protein (perforin) from cytolytic T-lymphocytes. J. Biol. Chem. 260, 9069-9072.
73. 73. Young, J.D., Cohn, Z.A. & Podack, E.R. (1986) The ninth component of complement and the pore-forming protein (perforin 1) from cytotoxic T cells: structural, immunological and functional similarities. Science 233, 184-190.
74. 74. Arbuthnott, J.P., Freer, J.H. & Billcliffe, B. (1973) Lipid-induced polymerization of Staphylococcal α-toxin. J. Gen. Microbiol. 75, 309-319.
75. 75. Füssle, R., Bhakdi, S., Tranum-Jensen, J., Sziegoleit, A. & Wellensiek, H.J. (1981) On the mechanism of membrane damage by α-staphylolysin: isolation of α-staphylolysin from target membranes and reconstitution into liposomes. Zbl. Bakt. (Suppl. 10), 224-234.
76. 76. Bhakdi, S. & Tranum-Jensen, J. (1991) Complement lysis: a hohle is a hohle. Immunol. Today 12, 318-320.
77. 77. Gordon, D., Martin-Eauclaire, M.F., Cestele, S., Kopeyan, C., Carlier, E., Khalifa, R.B., Pelhate, M. & 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.
78. 78. Mazumder, P.K. & Dube, S.N. (1996) Marine toxins as molecular probes for biological interactions: a review. Indian J. Physiol. Allied Sci, 50, 34-47.
79. 79. Pennington, M.W., Mahnir, V.M., Krafte, D.S., Zaydenberg, I., Byrens, M.E., Khaytin, I., Crowley, K. & Kem, W.R. (1996) Identification of three separate binding sites on SHK toxin, a potent inhibitor of voltage dependent potassium channels in human T-lymphocytes and rat brain. Biochem. Biophys. Res. Commun. 219, 696-701.
80. 80. Nastuk, W.L. (1971) Mechanisms of neuromuscular blockade. Ann. N.Y. Acad. Sci. 183, 171-182.
81. 81. Brumback, R.A. (1981) The neuromuscular junction. Part I: physiology and the effects of drugs and toxins. Am. Fam. Physician 23, 188-192.
82. 82. Kaminski, H.J., Suarez, J.I. & 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.
83. 83. Cooper, E.L., Rinkevich, B., Uhlenbruck, G. & Valembois, P. (1992) Invertebrate immunity: another viewpoint. Scand. J. Immunol. 35, 247-266.
84. 84. Cooper, E.L., Cossarizza, A., Kauschke, E. & Franceschi, C. (1999) Cell adhesion and the immune system: a case study using earthworms. Micro. Res. Technical 44, 237-253.
85. 85. Bilej, M., Brys, L., Beschin, A., Lucas, R., Vercauteren, E., Hanusova, R. & De Baetselier, P. (1995) Identification of a cytolytic protein in the coelomic fluid of Eisenia foetida earthworms. Immunol. Lett. 45, 123-128.
86. 86. Kauschke, E., Pagliara, P., Stabili, L. & Cooper, E.L. (1997) Characterization of proteolytic activity in coelomic fluid of Lumbricus terrestris. Comp. Biochem. Physiol. 116B, 235-242.
87. 87. Lassegues, M., Milochau, A., Doignon, F., Du Pasquier, L. & Valembois, P. (1997) Sequence and expression of an Eisenia-fetida-derived cDNA clone that encodes the 40-kDa fetidin antibacterial protein. Eur. J. Biochem. 246, 756-762.
88. 88. Milochau, A., Lassegues, M. & Valembois, P. (1997) Purification, characterization and activities of two hemolytic and antibacterial proteins from coelomic fluid of the annelid Eisenia fetida andrei. Biochim. Biophys. Acta 1337, 123-132.
89. 89. Sekizawa, Y., Kubo, T., Kobayashi, H., Nakajima, T. & 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.
90. 90. Yamaji, A., Sekizawa, Y., Emoto, K., Sakuraba, H., Inoue, K., Kobayashi, H. & Umeda, M. (1998) Lysenin, a novel sphingomyelin-specific binding protein. J. Biol. Chem. 273, 5300-5306.
91. 91. Roch, P., Stabili, L. & Pagliara, P. (1991) Purification of three serine proteases from the coelomic cells of eaarthworms (Eisenia foetida). Comp. Biochem. Physiol. 98B, 597-602.
92. 92. Roch, P., Ville, P. & Cooper, E.L. (1998) Characterization of a 14 kDa plant-related serine protease inhibitor and regulation of cytotoxic activity in earthworm coeleomic fluid. Dev. Comp. Immunol. 22, 1-12.
93. 93. Eue, I., Kauschke, E., Mohrig, W. & Cooper, E.L. (1998) Isolation and characterization of earthworm hemolysins and agglutinins. Dev. Comp. Immunol. 22, 13-25.
94. 94. Cho, J.H., Park, C.B., Yoon, Y.G. & Kim, S.C. (1998) Lumbricin 1, a novel proline-rich antimicrobial peptide from the earthworm: purification, cDNA cloning and molecular characterization. Biochim. Biophys. Acta 1408, 67-76.
95. 95. Komiyama, K., Yoshimura, M., Iwase, T., Sato, J., Okumura, K., Cooper, E.L. & Moro, 1. (1997) Identification of perform gene and its protein in the earthworm coelomocytes. Dev. Comp. Immunol. 21, 115.