Anticipating innate immunity without a Toll

Molecular Immunology

Volumn 42, Issue 8, 2005, Pages 931-942

  Engelmann, P ^a   Cooper, E L ^b   Nemeth P ^a  

^a UNIVERSITY OF PÉCS   (Hungary)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Coelomocytes; Cytotoxicity; Encapsulation; Innate immunity; Invertebrate; Monoclonal antibodies; Phagocytosis

Indexed keywords

BETA 2 MICROGLOBULIN; BIOLOGICAL MARKER; CD24 ANTIGEN; CD45 ANTIGEN; CD45RA ANTIGEN; CD45RO ANTIGEN; CDW49B ANTIGEN; CYTOKINE; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE ANTIGEN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; LYSOSOME ENZYME; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY EFCC 1; MONOCLONAL ANTIBODY EFCC 2; MONOCLONAL ANTIBODY EFCC 3; MONOCLONAL ANTIBODY EFCC 4; POLYPEPTIDE ANTIBIOTIC AGENT; PROPHENOL OXIDASE; SPHINGOMYELIN; THY 1 ANTIGEN; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIBIOTIC BIOSYNTHESIS; ANTIGEN RECOGNITION; BACTERIAL VIRULENCE; BLOOD CELL; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; COMPARATIVE STUDY; CYTOCHEMISTRY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DROSOPHILA MELANOGASTER; EARTHWORM; ENCAPSULATION; ENZYME ACTIVATION; ENZYME LOCALIZATION; GENETIC ANALYSIS; GERM LINE; HUMAN; HUMORAL IMMUNITY; IN VITRO STUDY; INNATE IMMUNITY; LEUKOCYTE; MAMMAL CELL; MOLECULAR RECOGNITION; NONHUMAN; PEPTIDE SYNTHESIS; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; SPECIES COMPARISON; SUPERNATANT; TUMOR CELL DESTRUCTION;

EID: 16844374403     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2004.09.038     Document Type: Short Survey

References (109)

1. A. Beschin, M. Bilej, F. Hanssens, J. Raymakers, E. Van Dyck, H. Revets, L. Brys, J. Gomez, P. De Baetselier, and M. Timmermans Identification and cloning of a glucan- and lipopolysaccharide-binding protein from Eisenia foetida earthworm involved in the activation of prophenoloxidase cascade J. Biol. Chem. 273 1998 24948 24954
2. M. Bilej, P. Sima, and J. Slipka Repeated antigenic challenge induces earthworm coelomocyte proliferation Immunol. Lett. 32 1992 181 184
3. M. Bilej, P. Rossmann, M. Sinkora, R. Hanusova, A. Beschin, G. Raes, and P. De Baetselier Cellular expression of the cytolytic factor in earthworms Eisenia foetida Immunol. Lett. 60 1998 23 29
4. M. Bilej, P. De Baetselier, E. Van Dijck, B. Stijlemans, A. Colige, and A. Beschin Distinct carbohydrate recognition domains of an invertebrate defense molecule recognize Gram-negative and Gram-positive bacteria J. Biol. Chem. 276 2001 45840 45847
5. J.M. Blander, and R. Medzhitov Regulation of phagosome maturation by signals from toll-like receptors Science 304 2004 1014 1018
6. G. Bourget, M.P. Moré, L. Guimbretiere, J. Le Boterf, and J.F. Verbist Cytotoxicity and hemolysis by an extract of the sponge Pachymatysma johnstonii Toxicon 26 1988 324 327
7. M.J. Carballal, C. López, C. Azevedo, and A. Villalba Enzymes involved in defense functions of hemocytes of mussel Mytilus galloprovincialis J. Invertebr. Pathol. 70 1997 96 105
8. A. Caruso, S. Licenziati, M. Corulli, A.F.D. Canaris, M.A. De Francesco, S. Fiorentini, L. Peroni, F. Fallacara, A. Balsari, and A. Turano Flow cytometric analysis of activation markers on stimulated T cells and their correlation with cell proliferation Cytometry 27 1997 71 76
9. T.C. Cheng Functional morphology and biochemistry of molluscan phagocytes Ann. N. Y. Acad. Sci. 266 1975 343 379
10. T.C. Cheng The role of lysosomal hydrolases in molluscan cellular response to immunologic challenge Comp. Pathobiol. 4 1978 59 71
11. T.C. Cheng, and M.S. Butler Experimentally induced elevations in acid phosphatase activity in hemolymph of Biomphalaria glabrata (Mollusca) J. Invertebr. Pathol. 34 1979 119 124
12. T.C. Cheng, and W.J. Dougherty Ultrastructural evidence for the destruction of Schistosoma mansoni sporocysts associated with elevated lysosomal enzyme level in Biomphalaria glabrata J. Parasitol. 75 1989 928 941
13. A.L. Clatworthy A simple systems approach to neural-immune communication Comp. Biochem. Physiol. 115A 1996 1 10
14. E.L. Cooper Transplantation immunity in annelids-I. Rejection of xenografts exchanged between Lumbricus terrestris and Eisenia foetida Transplant 6 1968 322 337
15. E.L. Cooper Chronic allograft rejection in Lumbricus terrestris J. Exp. Zool. 171 1969 69 73
16. E.L. Cooper, and E.A. Stein Oligochaetas R.A. Ratcliffe A.F. Rowley Invertebrate Blood Cells 1981 Academic Press San Diego 75 140
17. E.L. Cooper, M.K. Leung, M.M. Suzuki, K. Vick, P. Cadet, and G.B. Stefano An enkephalin-like molecule in earthworm coelomic fluid modifies leukocyte behaviour Dev. Comp. Immun. 17 1993 201 209
18. E.L. Cooper, A. Cossarizza, M.M. Suzuki, S. Salvioli, M. Capri, D. Quaglino, and C. Franceschi Autogeneic but not allogeneic earthworm effector coelomocytes kill the mammalian tumor cell target K562 Cell. Immunol. 166 1995 113 122
19. E.L. Cooper, A. Franchini, and E. Ottaviani Earthworm coelomocytes possess immunoreactive cytokines and POMC-derived peptides Anim. Biol. 4 1995 25 29
20. E.L. Cooper, A. Cossarizza, E. Kauschke, and C. Franceschi Cell adhesion and the immune system: a case study using earthworms Microsc. Res. Tech. 44 1999 237 253
21. E.L. Cooper, E. Kauschke, and A. Cossarizza Digging for innate immunity since Darwin and Metchnikoff BioEssays 24 2002 319 333
22. E.L. Cooper, and P. Roch Earthworm immunity: a model of immune competence Pedobiologia 47 2003 676 688
23. A. Cossarizza, E.L. Cooper, M.M. Suzuki, S. Salvioli, M. Capri, G. Gri, D. Quaglino, and C. Franceschi Earthworm leukocytes that are not phagocytic and cross-react with several human epitopes can kill human tumor cell lines Exp. Cell Res. 224 1996 174 182
24. C. Couillault, N. Pujol, J. Reboul, L. Sabatier, J.F. Guichou, Y. Kohara, and J.J. Ewbank TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM Nat. Immunol. 5 2004 488 494
25. R.P. Dales, and Y. Kalaç Phagocytic defense by the earthworm against certain pathogenic bacteria Comp. Biochem. Physiol. 101A 1992 487 490
26. A. De Loof, and L. Schoops Homologies between the amino acid sequences of some vertebrate peptide hormones and peptides isolated from invertebrate sources Comp. Biochem. Physiol. 95B 1990 459 468
27. M. de Eguileor, A. Grimaldi, G. Tettamanti, R. Valvassori, E.L. Cooper, and G. Lanzavecchia Lipopolysaccharide-dependent induction of leech leukocytes that cross-react with vertebrate cellular differentiation markers Tissue Cell 32 2000 437 445
28. M. de Eguileor, A. Grimaldi, G. Tettamanti, R. Valvassori, E.L. Cooper, and G. Lanzavecchia Different types of response to foreign antigens by leech leukocytes Tissue Cell 32 2000 40 48
29. L. Dinan, G. Gläsener, and H. Emmerich Characterization of the acid phosphatase and aryl sulphatase activities in tumorous blood cell line of Drosophila melanogaster Insect Biochem. 13 1983 411 419
30. E.A. Dyrynda, R.K. Pipe, and N.A. Ratcliffe Sub-populations of haemocytes in the adult and developing marine mussel, Mytilus edulis, identified by use of monoclonal antibodies Cell Tissue Res. 289 1997 527 536
31. P. Engelmann, J. Pál, T. Berki, E.L. Cooper, and P. Németh Earthworm leukocytes react with different mammalian antigen-specific monoclonal antibodies Zoology 105 2002 257 265
32. P. Engelmann, E.L. Cooper, and P. Németh Comparative analysis of earthworms' immune system by phylogenetical aspects of cell surface and intracellular markers E.L. Cooper A. Beschin M. Bilej A new model for analyzing antimicrobial peptides with biomedical applications 2002 IOS Press Amsterdam 53 57
33. P. Engelmann, L. Molnár, L. Pálinkás, E.L. Cooper, and P. Németh Earthworm leukocyte populations specifically harbor lysosomal enzymes that may respond to bacterial challenge Cell Tissue Res. 316 2004 391 401
34. Engelmann, P., Kiss, J., Csöngei, V., Cooper, E.L., Németh, P., in press. Earthworm leukocytes kill HeLa, HEp-2, PC-12 and PA317 cells in vitro. J. Biochem. Biophys. Methods, 2004, in press.
35. 2 Reaktion Acta Histochem. 55 1975 32 41
36. E. Fischer, M. Lovas, and P. Németh An experimental analysis of the vasofibrous tissue in the leech Haemopis sanguisuga L Zool. Anz. 197 1976 289 299
37. E. Fischer The myelo-erytroid nature of the chlorarogogenous-like tissues of the annelids Comp. Biochem. Physiol. 106A 1993 449 453
38. W.O. Granath, and T.P. Yoshino Lysosomal enzyme activities is susceptible and refractory strains of Biomphalaria glabrata during the course of infection Schistosoma mansoni J. Parasitol. 69 1983 1018 1026
39. P.J. Ham, H.E. Hagen, A.J. Baxter, and J. Grunewald Mechanisms of resistance to Onchocerca infection in blackflies Parasitol. Today 11 1995 63 67
40. S.S. Hamed, E. Kauschke, and E.L. Cooper Cytochemical properties of earthworm coelomocytes enriched by Percoll E.L. Cooper A. Beschin M. Bilej A new model for analyzing antimicrobial peptides with biomedical applications 2002 IOS Press Amsterdam 29 37
41. R. Hanušová, M. Bilej, L. Brys, P. De Baetselier, and A. Beschin Identification of a coelomic mitogenic factor in Eisenia foetida earthworm Immun. Lett. 65 1999 203 211
42. J.F. Hillyer, and B.M. Christensen Characterisation of hemocytes from the yellow fever mosquito Aedes aegypti Histochem. Cell Biol. 117 2002 431 440
43. F. Hirigoyenberry, F. Lassalle, and M. Lassegues Antibacterial activity of Eisenia fetida andrei coelomic fluid: transcription and translation regulation of lysozyme and proteins evidenced after bacterial infestation Comp. Biochem. Physiol. 95B 1990 71 75
44. U. Hoeger Hydrolytic enzymes in the coelomic cells of the polychaete Nereis viriens during sexual maturation Mar. Biol. 110 1994 7 12
45. T. Horng, and R. Medzhitov Drosophila MyD88 is an adapter in the Toll signaling pathway Proc. Natl. Acad. Sci. U.S.A. 98 2001 12654 12658
46. M. Hrženjak, D. Kobrehel, S. Levanat, M. Jurin, and T. Hrženjak Mitogenicity of the earthworm's (Eisenia foetida) insulin-like proteins Comp. Biochem. Physiol. 104B 1993 723 729
47. M.W. Johansson, T. Holmblad, P.O. Thornqvist, M. Cammarata, N. Parrinello, and K. Söderhäll A cell-surface superoxide dismutase is a binding protein for peroxinectin, a cell-adhesive peroxidase in crayfish J. Cell Sci. 112 1999 917 925
48. E. Kauschke, and W. Mohrig Cytotoxic activity in the coelomic fluid of the annelid Eisenia foetida Sav J. Comp. Physiol. 157B 1987 77 83
49. E. Kauschke, K. Komiyama, I. Moro, I. Eue, S. Koenig, and E.L. Cooper Evidence for perforin-like activity associated with earthworm leukocytes Zoology 104 2001 13 24
50. H. Kobayashi, M. Ohtomi, Y. Sekizawa, and N. Ohta Toxicity of coelomic fluid of the earthworm Eisenia foetida to vertebrates but not invertebrates: probable role of sphingomyelin Comp. Biochem. Physiol. 128C 2001 401 411
51. B. Kocsis, and L. Emody Pathogen-associated molecular pattern of bacteria and its recognition by the host Hun. Immunol. 2 2003 10 19
52. 3 confirm identity with fetidin and lysenin produced by earthworm leukocytes Dev. Comp. Immun. 27 2003 513 520
53. J. Koumans-van Diepen, E. Egberts, B.R. Peixoto, N. Taverne, and J.H. Rombout B cell and immunoglobulin heterogeneity in carp (Cyprinus carpio L.); an immuno(cyto)chemical study Dev. Comp. Immunol. 19 1995 97 108
54. S. Lange, F. Nüßler, E. Kauschke, G. Lutsch, E.L. Cooper, and A. Herrmann Interaction of earthworm hemolysin with lipid membranes requires sphingolipids J. Biol. Chem. 272 1997 20884 20892
55. M. Lassegues, A. Milochau, F. Doignon, L. Du Pasquier, and P. Valembois Sequence and expression of an Eisenia-fetida-derived cDNA clone that encodes the 40-kDa fetidin antibacterial protein Eur. J. Biochem. 246 1997 756 762
56. D.S. Linthicum, D.H. Marks, E.A. Stein, and E.L. Cooper Graft rejection in earthworms: an electron microscopic study Eur. J. Immunol. 7 1977 871 876
57. M.T. Locci, M. Masetti, A. Cecchettini, and A. Giorgi Cells released in vitro from the embryonic yolk sac of the stick insect Carausius morosus (Br.) (Phasmatodea: Heteronemiidae) may include embryonic hemocytes Int. J. Insect Morphol. Embryol. 27 1998 325 331
58. P.R. Lowenstein Immunology of viral-vector mediated gene transfer into the brain: an evolutionary perspective Trends Immunol. 23 2002 23 30
59. M.H. Mansour, and E.L. Cooper Serological and partial molecular characterization of a Thy-1 homolog in tunicates Eur. J. Immunol. 14 1984 1031 1039
60. M.H. Mansour, R. DeLange, and E.L. Cooper Isolation, purification, and amino acid composition of the tunicate hemocyte Thy-1 homolog J. Biol. Chem. 260 1985 2681 2686
61. D.H. Marks, E.A. Stein, and E.L. Cooper Acid phosphatase changes associated with response to foreign tissue in the earthworm Lumbricus terrestris Comp. Biochem. Physiol. 68A 1981 681 683
62. S. Meloni, M. Mazzini, and G. Scapigliati Ontogenesis of hemocytes in stick insect Bacillus rossius (Rossi) (Phasmatodea, Bacillidae) studied with an anti hemocyte monoclonal antibody Int. J. Insect Morphol. Embryol. 28 1999 245 250
63. E. Metchnikoff Lectures on Comparative Pathology of Inflammation (English Trans. Starling E.H. 1968) 1891 Dover Press New York pp. 67-73
64. H. Mori Embryonic haemocytes: origin and development A.P. Gupta Insect Haemocytes 1979 University Press Cambridge 4 27
65. A.J. Nappi, and E. Ottaviani Cytotoxicity and cytotoxic molecules in invertebrates BioEssays 22 2000 469 480
66. M. Nasi, M. Pinti, M. Troiano, L. Moretti, E.L. Cooper, and A. Cossarizza The evolution of cell killing: when the target cell became invited to choose how to die E.L. Cooper A. Beschin M. Bilej A new model for analyzing antimicrobial peptides with biomedical applications 2002 IOS Press Amsterdam 82 89
67. E. Ottaviani, P. Trevisan, and A. Pederzoli Immunocytochemical evidence for ACTH- and (β-endorphin-like molecules in phagocytic blood cells of urodelan amphibians Peptides 13 1992 227 231
68. E. Ottaviani, T. Capriglione, and C. Franceschi Invertebrate and vertebrate immune cells express pro-opiomelanocortin (POMC) mRNA Brain Behav. Immun. 9 1995 1 8
69. E. Ottaviani, and C. Franceschi The invertebrate phagocytic immunocyte: clues to a common evolution of immune and neuroendocrine systems Immunol. Today 18 1997 169 174
70. E. Ottaviani, A. Franchini, and C. Franceschi Evolution of neuroendocrine thymus: studies on POMS-derived peptides, cytokines and apoptosis in lower and higher vertebrates J. Neuroimmunol. 72 1997 67 74
71. E. Ottaviani, S. Valensin, and C. Franceschi The neuro-immunological interface in an evolutionary perspective: the dynamic relationship between effector and recognition systems Front. Biosci. 3 1998 431 435
72. E. Ottaviani, A. Franchini, and I. Hanokoglu In situ localization of ACTH receptor-like mRNA in molluscan and human immunocytes Cell. Mol. Life Sci. 54 1998 139 142
73. N. Parrinello, V. Arizza, M. Cammarata, and D.M. Parrinello Cytotoxic activity of Ciona intestinalis (Tunicata) hemocytes: properties of the in vitro reaction against erythrocyte targets Dev. Comp. Immunol. 17 1993 19 27
74. N. Parrinello, M. Cammarata, and V. Arizza Univacuolar refractile hemocytes from the tunicate Ciona intestinalis are cytotoxic for mammalian erythrocytes in vitro Biol. Bull. 190 1996 418 425
75. C. Pasare, and R. Medzhitov Toll-like receptors and acquired immunity Semin. Immunol. 16 2004 23 26
76. L.L. Pech, and M.R. Strand Granular cells are required for encapsulation of foreign targets by insect haemocytes J. Cell Sci. 109 1996 2053 2060
77. R.K. Pipe Hydrolytic enzymes associated with the granular hemocytes of the marine mussel Mytilus edulis Histochem. J. 22 1990 595 603
78. R.K. Pipe, S.R. Farley, and J.A. Coles The separation and characterisation of haemocytes from the mussel Mytilus edulis Cell Tissue Res. 289 1997 537 545
79. E. Porchet-Henneré Cooperation between different coelomocyte populations during the encapsulation response of Nereis diversicolor, demonstrated using monoclonal antibodies J. Invertebr. Pathol. 56 1990 353 361
80. E. Porchet-Henneré, and G. Vernet Cellular immunity in an annelid (Nereis diversicolor, Polychaeta): production of melanin by a subpopulation of granulocytes Cell Tissue Res. 269 1992 167 174
81. D.A. Raftos, and A. Hutchinson Cytotoxicity reactions in the solitary tunicate Styela plicata Dev. Comp. Immunol. 19 1995 463 471
82. N.A. Ratciffe, A.F. Rowley, S.W. Fitzgerald, and C.P. Rhodes Invertebrate immunity: basic concepts and recent advances Int. Rev. Cytol. 97 1985 183 250
83. C. Rechtoris, and A. McIntosh A cytotoxic substance in insect cell culture spent media In vitro 12 1976 678 681
84. J. Rejnek, L. Tuckova, P. Sima, and M. Bilej The fate of protein antigen in earthworms: study in vivo Immunol. Lett. 36 1993 131 135
85. P. Roch, E.L. Cooper, and D.P. Eskinazi Serological evidences for a membrane structure related to human beta 2-microglobulin expressed by certain earthworm leukocytes Eur. J. Immunol. 13 1983 1037 1042
86. P. Roch, P. Ville, and E.L. Cooper Characterization of a 14 kDa plant-related serine protease inhibitor and regulation of cytotoxic activity in earthworm coelomic fluid Dev. Comp. Immunol. 22 1998 1 12
87. J. Rodriguez, V. Boulo, E. Mialhe, and E. Bachere Characterization of shrimp haemocytes and plasma components by monoclonal antibodies J. Cell Sci. 108 1995 1043 1050
88. G. Scapigliati, M. Pecci, A. Piermattei, and M. Mazzini Characterisation of a monoclonal antibody against a 180 kDa hemocyte polypeptide involved in cellular defence reactions of the stick insect Bacillus rossius J. Insect Physiol. 43 1997 345 354
89. A. Shalev, A.H. Greenberg, L. Logdberg, and L. Bjorck beta 2-Microglobulin-like molecules in low vertebrates and invertebrates J. Immunol. 127 1981 1186 1191
90. A. Shalev, M. Pla, T. Ginsburgervogel, G. Echalier, L. Logdberg, L. Bjorck, J. Colombani, and S. Segal Evidence for beta 2-microglobulin-like and H-2-like antigenic determinants in Drosophila J. Immunol. 130 1983 297 302
91. P. Sima, M. Bilej, and J. Slipka Perienteral chloragogen tissue and its role in defense in lumbricid worms Adv. Exp. Med. Biol. 371A 1995 327 329
92. P. Sima, and J. Slipka The spleen and its coelomic and enteric history Adv. Exp. Med. Biol. 371A 1995 331 334
93. I. Söderhäll, E. Bangyeekhun, S. Mayo, and K. Söderhäll Hemocyte production and maturation in an invertebrate animal; proliferation and gene expression in hematopoetic stem cells of Pacifastacus leniusculus Dev. Comp. Immunol. 27 2003 661 672
94. E.A. Stein, R.R. Avtalion, and E.L. Cooper The coelomocytes of the earthworm Lumbricus terrestris: morphology and phagocytic properties J. Morphol. 153 1977 467 476
95. E.A. Stein, and E.L. Cooper In vitro agglutinin production by earthworm leukocytes Dev. Comp. Immun. 12 1988 531 547
96. H.E. Stubberud, T.G. Hønsi, and J. Stenersen Purification and partial characterisation of tentatively classified acid phosphatase from the earthworm Eisenia veneta Comp. Biochem. Physiol. 126B 2000 487 494
97. M.M. Suzuki, and E.L. Cooper Spontaneous cytotoxic earthworm leukocytes kill K562 tumor cells Zool. Sci. 12 1995 443 451
98. T. Takahashi, T. Iwase, N. Takenouchi, M. Saito, K. Kobayashi, Z. Moldoveanu, J. Mestecky, and I. Moro The joining (J) chain is present in invertebrates that do not express immunoglobulins Proc. Natl. Acad. Sci. U.S.A. 93 1996 1886 1891
99. U. Tepass, L.I. Fessler, A. Aziz, and V. Hartenstein Embryonic origin of hemocytes and their relationship to cell death in Drosophila Development 120 1994 1829 1837
100. J. Toupin, and G. Lamoureux Coelomocytes of earthworms: the T-cell-like rosette Cell. Immunol. 26 1976 127 132
101. P. Valembois, M. Lasségues, P. Roch, and J. Vaillier Scanning-electron microscopic study of the involvement of coelomic cells in earthworm antibacterial defense Cell Tissue Res. 240 1985 479 484
102. P. Valembois, J. Seymour, and M. Lassegues Evidence of lipofuscin and melanin in the brown body of the earthworm Eisenia fetida andrei Cell Tissue Res. 277 1994 183 188
103. C.B. van de Braak, M.H. Botterblom, N. Taverne, W.P. van der Knaap, and J.H. Rombout Monoclonal antibodies against haemocyte molecules of Penaeus monodon shrimp react with haemolymph components of other crustaceans and disparate taxa Dev. Comp. Immunol. 25 2001 279 283
104. E. Willott, C. Lowenberger, B.M. Christensen, and M.R. Kanost Monoclonal antibodies against Manduca sexta hemocytes bind Aedes aegypti hemocytes: characterization of six monoclonal antibodies that bind hemocytes from both species Dev. Comp. Immunol. 19 1995 451 461
105. Y. Xu, X. Tao, B. Shen, T. Horng, R. Medzhitov, J.L. Manley, and L. Tong Structural basis for signal transduction by the Toll/interleukin-1 receptor domains Nature 408 2000 111 115
106. Q. Xue, and T. Renault Monoclonal antibodies to European flat oyster Ostrea edulis hemocytes: characterization and tissue distribution of granulocytes in adult and developing animals Dev. Comp. Immunol. 25 2001 187 194
107. A. Yamayi, Y. Sekizawa, K. Emoto, H. Sakuraba, K. Inoue, H. Kobayashi, and M. Umeda Lysenin, a novel sphingomyelin-specific binding protein J. Biol. Chem. 273 1998 5300 5306
108. C. Yin, and T. Humphreys Acute cytotoxic allogeneic histoincompatibility reactions involving gray cells in the marine sponge Callyspongia diffusa Biol. Bull. 191 1996 159 167
109. T.P. Yoshino, and W.O. Granath Identification of antigenically distinct hemocyte subpopulations in Biomphalaria glabrata (Gastropoda) using monoclonal antibodies to surface membrane markers Cell Tissue Res. 232 1983 553 564