Structure and function of coagulogen, a clottable protein in horseshoe crabs

Cellular and Molecular Life Sciences

Volumn 61, Issue 11, 2004, Pages 1257-1265

  Osaki, T ^a   Kawabata, S ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Hemolymph coagulogen; Horseshoe crab; Lipopolysaccharides; Transglutaminase

Indexed keywords

BETA 1,3 GLUCAN; BLOOD CLOTTING FACTOR; C PEPTIDE; CALCIUM ION; CELL SURFACE PROTEIN; COAGULASE; ENZYME PRECURSOR; FIBRINOGEN; LECTIN; LIPOPHORIN; NERVE GROWTH FACTOR; NEUROTROPHIN; PROTEIN COAGULOGEN; PROXIN; THROMBIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; VITELLOGENIN;

AMINO ACID SEQUENCE; BLOOD CELL; BLOOD CLOTTING; CRAB; CROSS LINKING; DISULFIDE BOND; HEMOLYMPH; IMMUNITY; MAMMAL; MOLECULAR INTERACTION; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NONHUMAN; POLYMERIZATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SEQUENCE HOMOLOGY;

ANIMALS; BLOOD COAGULATION; BLOOD PROTEINS; DIMERIZATION; HEMOCYTES; HORSESHOE CRABS;

CRUSTACEA; DECAPODA (CRUSTACEA); MAMMALIA; MEROSTOMATA;

EID: 3042523021     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-004-3396-5     Document Type: Review

References (112)

1. Toh Y., Mizutani A., Tokunaga F., Muta T. and Iwanaga S. (1991) Morphology of the granular hemocytes of the Japanese horseshoe crab Tachypleus tridentatus and immunocytochemical localization of clotting factors and antimicrobial substances. Cell Tissue Res. 266: 137-147
2. Iwanaga S., Kawabata S. and Muta T. (1998) New types of clotting factors and defense molecules found in horseshoe crab hemolymph: their structures and functions. J. Biochem. (Tokyo) 123: 1-15
3. Iwanaga S. (2002) The molecular basis of innate immunity in the horseshoe crab. Curr. Opin. Immunol. 14: 87-95
4. Iwanaga S. (1993) The limulus clotting reaction. Curr. Opin. Immunol. 5: 74-82
5. Muta T. and Iwanaga S. (1996) The role of hemolymph coagulation in innate immunity. Curr. Opin. Immunol. 8: 41-47
6. Shigenaga T., Takayenoki Y., Kawasaki S., Seki N., Muta T., Toh Y. et al. (1993) Separation of large and small granules from horseshoe crab (Tachypleus tridentatus) hemocytes and characterization of their components. J. Biochem. 114: 307-316
7. Srimal S., Miyata T., Kawabata S. and Iwanaga S. (1985) The complete amino acid sequence of coagulogen isolated from Southeast Asian horseshoe crab, Carcinoscorpius rotundicauda. J. Biochem. 98: 305-318
8. Nakamura S., Iwanaga S., Harada T. and Niwa M. (1976) A clottable protein (coagulogen) from amoebocyte lysate of Japanese horseshoe crab (Tachypleus tridentatus). Its isolation and biochemical properties. J. Biochem. 80: 1011-1021
9. Nakamura S., Takagi T., Iwanaga S., Niwa M. and Takahashi K. (1976) Amino acid sequence studies on the fragments produced from horseshoe crab coagulogen during gel formation: homologies with primate fibrinopeptide B. Biochem. Biophys. Res. Commun. 72: 902-908
10. Takagi T., Hokama Y., Miyata T., Morita T. and Iwanaga S. (1984) Amino acid sequence of Japanese horseshoe crab (Tachypleus tridentatus) coagulogen B chain: Completion of the coagulogen sequence. J. Biochem. 95: 1445-1457
11. Miyata T., Hiranaga M., Umezu M. and Iwanaga S. (1984) Amino acid sequence of the coagulogen from Limulus polyphemus hemocytes. J. Biol. Chem. 259: 8924-8933
12. Miyata T., Usui K. and Iwanaga S. (1984) The amino acid sequence of coagulogen isolated from southeast Asian horseshoe crab, Tachypleus gigas. J. Biochem. 95: 1793-1801
13. Miyata T., Matsumoto H., Hattori M., Sakaki Y. and Iwanaga S. (1986) Two types of coagulogen mRNAs found in horseshoe crab (Tachypleus tridentatus) hemocytes: Molecular cloning and nucleotide sequences. J. Biochem. 100: 213-220
14. Bergner A., Oganessyan V., Muta T., Iwanaga S., Typke D., Huber R. et al. (1996) Crystal structure of limulus coagulogen: the clotting protein from horseshoe crab, a structural homologue of nerve growth factor. EMBO J. 15: 6789-6797
15. Nakamura T., Morita T. and Iwanaga S. (1986) Lipopolysaccharide-sensitive serine-protease zymogen (factor C) found in Limulus hemocytes: isolation and characterization. Eur. J. Biochem. 154: 511-521
16. Tokunaga F., Miyata T., Nakamura T., Morita T., Kuma K., Miyata T. et al. (1987) Lipopolysaccharide-sensitive serine-protease zymogen (factor C) of horseshoe crab hemocytes: Identification and alignment of proteolytic fragments produced during the activation show that it is a novel type of serine protease. Eur. J. Biochem. 167: 405-416
17. Nakamura T., Tokunaga F., Morita T. and Iwanaga S. (1988) Interaction between lipopolysaccharide and intracellular serine protease zymogen, factor C, from horseshoe crab (Tachypleus tridentatus) hemocytes. J. Biochem. 103: 370-374
18. Nakamura T., Tokunaga F., Morita T., Iwanaga S., Kusumoto S., Shiba T. et al. (1988) Intracellular serine-protease zymogen, factor C, from horseshoe crab hemocytes. Its activation by synthetic lipid A analogues and acidic phospholipids. Eur. J. Biochem. 176: 89-94
19. Tokunaga F., Nakajima H. and Iwanaga S. (1991) Further studies on lipopolysaccharide-sensitive serine protease zymogen (factor C): its isolation from Limulus polyphemus hemocytes and identification as an intracellular zymogen activated by alpha-chymotrypsin, not by trypsin. J. Biochem. 109: 150-157
20. Muta T., Miyata T., Misumi Y., Tokunaga F., Nakamura T., Toh Y. et al. (1991) Limulus factor C: an endotoxin-sensitive serine protease zymogen with a mosaic structure of complement-like, epidermal growth factor-like and lectin-like domains. J. Biol. Chem. 266: 6554-6561
21. Nakamura S., Morita T., Harada-Suzuki T., Iwanaga S., Takahashi K. and Niwa M. (1982) A clotting enzyme associated with the hemolymph coagulation system of horseshoe crab (Tachypleus tridentatus): its purification and characterization. J. Biochem. 92: 781-792
22. Nakamura T., Horiuchi T., Morita T. and Iwanaga S. (1986) Purification and properties of intracellular clotting factor, factor B, from horseshoe crab (Tachypleus tridentatus) hemocytes. J. Biochem. 99: 847-857
23. Muta T., Oda T. and Iwanaga S. (1993) Horseshoe crab coagulation factor B: a unique serine protease zymogen activated by cleavage of an Ile-Ile bond. J. Biol. Chem. 268: 21384-21388
24. Morita T., Tanaka S., Nakamura T. and Iwanaga S. (1981) A new (1,3)-β-D-glucan-mediated coagulation pathway found in Limulus amebocytes. FEBS Lett. 129: 318-321
25. Kakinuma A., Asano T., Torii H. and Sugino Y. (1981) Gelation of Limulus amebocyte lysate by an antitumor (1,3)-β-D-glucan. Biochem. Biophys. Res. Commun. 101: 434-439
26. Muta T., Seki N., Takaki Y., Hashimoto R., Oda T., Iwanaga A. et al. (1995) Purified horseshoe crab factor G: reconstitution and characterization of the (1,3)-β-D-glucan-sensitive serine protease cascade. J. Biol. Chem. 270: 892-897
27. Seki N., Muta T., Oda T., Iwaki D., Kuma K., Miyata T. et al. (1994) Horseshoe crab (1,3)-β-D-glucan-sensitive coagulation factor G. A serine protease zymogen heterodimer with similarities to β-glucan-binding proteins. J. Biol. Chem. 269: 1370-1374
28. Takaki Y., Seki N., Kawabata S., Iwanaga S. and Muta T. (2002) Duplicated binding sites for (1,3)-β-D-glucan in the horseshoe crab coagulation factor G. J. Biol. Chem. 277: 14281-14287
29. Nakamura T., Morita T. and Iwanaga S. (1985) Intracellular proclotting enzyme in limulus (Tachypleus tridentatus) hemocytes: its purification and properties. J. Biochem. 97: 1561-1574
30. Muta T., Hashimoto R., Miyata T. Nishimura H., Toh Y. and Iwanaga S. (1990) Proclotting enzyme from horseshoe crab hemocytes: cDNA cloning, disulfide locations and subcellular localization. J. Biol. Chem. 265: 22426-22433
31. Furie B. and Furie B. C. (1988) The molecular basis of blood coagulation. Cell 53: 505-518
32. Gokudan S., Muta T., Tsuda R., Koori K., Kawahara T. Seki N. et al. (1999) Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proc. Natl. Acad. Sci. USA 96: 10086-10091
33. Kairies N., Beisel H.-G., Fuentes-Prior P., Tsuda R., Muta T., Iwanaga S. et al. (2001) The 2.0-Å crystal structure of tachylectin 5A provides evidence for the common origin of the innate immunity and the blood coagulation systems. Proc. Natl. Acad. Sci. USA 98: 13519-13524
34. Belvin M. P. and Anderson K. V. (1996) A conserved signaling pathway - the Drosphila toll-dorsal pathway. Annu. Rev. Cell. Dev. Biol. 12: 393-416
35. Lemaitre B., Nicolas E. Michaut L., Reichhart J. M. and Hoffmann J. A. (1996) The dorsoventral regulatory gene cassette spaetzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86: 973-983
36. Rutschmann S., Kilinc A. and Ferrandon D. (2002) Cutting edge: the toll pathway is required for resistance to gram-positive bacterial infections in Drosophila. J. Immunol. 168: 1542-1546
37. Bergner A., Muta T., Iwanaga S., Beisel H.-G., Delotto R. and Bode W. (1997) Horseshoe crab coagulogen is an invertebrate protein with a nerve growth factor-like domain. Biol. Chem. 378: 283-287
38. Smith C. L. and DeLotto R. (1992) A common domain within the proenzyme regions of the Drosophila snake and easter proteins and Tachypleus proclotting enzyme defines a new subfamily of serine proteases. Protein Sci. 1: 1225-1226
39. Smith C. L. and DeLotto R. (1994) Ventralizing signal determined by protease activation in Drosophila embryogenesis. Nature 368: 548-551
40. Lee S. Y., Cho M. Y., Hyun J. H., Lee K. M. Homma K. I., Natori S. et al. (1998) Molecular cloning of cDNA for pro-phenol-oxidase-activating factor I, a serine protease is induced by lipopolysaccharide or 1,3-beta-glucan in coleopteran insect, Holotrichia diomphalia larvae. Eur. J. Biochem. 257: 615-621
41. Jiang H. B., Wang Y. and Kanost M. R. (1998) Pro-phenol oxidase activating proteinase from an insect, Manduca sexta - a bacteria-inducible protein similar to Drosophila easter. Proc. Natl. Acad. Sci. USA 95: 12220-12225
42. Satoh D., Horii A., Ochiai M. and Ashida M. (1999) Prophenoloxidase- aclivaling enzyme of the silkworm, Bombyx mori. Purification, characterization and cDNA cloning. J. Biol. Chem. 274: 7441-7453
43. Jiang H. B. and Kanost M. R. (2000) The clip-domain family of serine proteinases in arthropods. Insect Biochem. Mol. Biol. 30: 95-105
44. Kopácek P., Hall M. and Söderhäll K. (1993) Characterization of a clotting protein, isolated from plasma of the freshwater crayfish Pacifastacus leniusculus. Eur. J. Biochem. 213: 591-597
45. Komatsu M. and Ando S. (1998) A very-high-density lipoprotein with clotting ability from hemolymph of sand crayfish, Ibacus ciliatus. Biosci. Biotechnol. Biochem. 62: 459-463
46. Doolittle R. F. and Riley M. (1990) The amino-terminal sequence of lobster fibrinogen reveals common ancestry with vitellogenins. Biochem. Biophys. Res. Commun. 167: 16-19
47. Doolittle R. F. and Fuller G. M. (1972) Sodium dodecyl sulfate-polyacrylamide gel electrophoresis studies on lobster fibrinogen and fibrin. Biochim. Biophys. Acta 263: 805-809
48. Hall M., van Heusden M. C. and Söderhäll K. (1995) Identification of the major lipoproteins in crayfish hemolymph as proteins involved in immune recognition and clotting. Biochem. Biophys. Res. Commun. 216: 939-946
49. Sritunyalucksana K. and Söerhäll K. (2000) The proPO and clotting system in crustaceans. Aquaculture 191: 53-69
50. Hall M., Wang R., van Antwerpen R., Sottrup-Jensen L. and Söderhäll K. (1999) The crayfish plasma clotting protein: a vitellogenin-related protein responsible for clot formation in crustacean blood. Proc. Natl. Acad. Sci. USA 96: 1965-1970
51. Yeh M. S., Huang C. J., Leu J. H., Lee Y. C. and Tsai I. H. (1999) Molecular cloning and characterization of a hemolymph clottable protein from tiger shrimp (Penaeus monodon). Eur. J. Biochem. 266: 624-633
52. Sappington T. W. and Raikhel A. S. (1997) Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem. Mol. Biol. 28: 277-300
53. Sadler J. E. (1991) von Willebrand factor. J. Biol. Chem. 266: 22777-22780
54. Voorberg J., Fontijn R., van Mourik J. A. and Pannekoek H. (1990) Domains involved in multimer assembly of von Willebrand factor (vWF): multimerization is independent of dimerization. EMBO J. 9: 797-803
55. Mayadas T. N. and Wagner D. D. (1992) Vicinal cysteines in the prosequence play a role in von Willebrand factor multimer assembly. Proc. Natl. Acad. Sci. USA 89: 3531-3535
56. Bohn H. (1986) Hemolymph clotting in insects. In: Immunity in Invertebrates, Brehélin M. (ed.), pp. 189-207, Springer, Heidelberg
57. Theopold U., Li D., Fabbri M., Scherfer C. and Schmidt O. (2002) The coagulation of insect hemolymph. Cell. Mol. Life Sci. 59: 363-372
58. Bohn H., Barwig B. and Bohn B. (1981) Immunochemical analysis of hemolymph clotting in the insect Leucophaea maderae (Blattaria). J. Comp. Physiol. 143: 169-184
59. Barwig B. and Bohn H. (1980) Evidence for the presence of two clotting proteins in insects. Naturwissenschaften 67: 47
60. Barwig B. (1985) Isolation and characterization of plasma coagulogen (PC) of the cockroach Leucophaea maderae (Blattaria). J. Comp. Physiol. 155: 135-143
61. Geng C. and Dunn P. E. (1988) Hemostasis in larvae of Manduca sexta: formation of a fibrous coagulum by hemolymph proteins. Biochem. Biophys. Res. Commun. 155: 1060-1065
62. Minnick M. F., Rupp R. A. and Spence K. D. (1986) A bacterial-induced lectin which triggers hemocyte coagulation in Manduca sexta. Biochem. Biophys. Res. Commun. 137: 729-735
63. Finnerty C. M., Karplus P. A. and Granados R. R. (1999) The insect immune protein scolexin is a novel serine proteinase homolog. Protein Sci. 8: 242-248
64. Kotani E., Yamakawa M., Iwamoto S., Tashiro M., Mori H., Sumida M. et al. (1995) Cloning and expression of the gene of hemocytin, an insect humoral lectin which is homologous with the mammalian von Willebrand factor. Biochim. Biophys. Acta 1260: 245-258
65. Brehélin M. (1979) Hemolymph coagulation in Locusta migratoria: evidence for a functional equivalent of fibrinogen. Comp. Biochem. Physiol. 62: 329-334
66. Gellissen G. (1983) Lipophorin as the plasma coagulogen in Locusta migratoria. Naturwissenschaften 70: 45-46
67. Duvic B. and Brehélin M. (1998) Two major proteins from locust plasma are involved in coagulation and are specifically precipitated by laminarin, a β-1,3-glucan. Insect Biochem. Mol. Biol. 28: 959-967
68. Li D., Scherfer C., Korayem A. M., Zhao Z., Schmidt O. and Theopold U. (2002) Insect hemolymph clotting: evidence for interaction between the coagulation system and the prophenoloxidase activating cascade. Insect Biochem. Mol. Biol. 32: 919-928
69. Theopold U. and Schmidt O. (1997) Helix pomatia lectin and annexin V, two molecular probes for insect microparticles: possible involvement in hemolymph coagulation. J. Insect Physiol. 43: 667-674
70. Kawasaki H., Nose T., Muta T., Iwanaga S., Shimohigashi Y. and Kawabata S. (2000) Head-to-tail polymerization of coagulin, a clottable protein of the horseshoe crab. J. Biol. Chem. 275: 35297-35301
71. Miura Y., Kawabata S. and Iwanaga S. (1994) A limulus intracellular coagulation inhibitor with characteristics of the serpin superfamily. Purification, characterization and cDNA cloning. J. Biol. Chem. 269: 542-547
72. Miura Y., Kawabata S., Wakamiya Y., Nakamura T. and Iwanaga S. (1995) A limulus intracellular coagulation inhibitor type 2. Purification, characterization, cDNA cloning and tissue localization. J. Biol. Chem. 270: 558-565
73. Agarwala K. L., Kawabata S., Miura Y., Kuroki Y. and Iwanaga S. (1996) Limulus intracellular coagulation inhibitor type 3. Purification, characterization, cDNA cloning and tissue localization. J. Biol. Chem. 271: 23768-23774
74. Tokunaga F., Yamada M., Miyata T., Ding Y. L., Hiranaga-Kawabata M., Muta T. et al. (1993) Limulus hemocyte transglutaminase. Its purification and characterization and identification of the intracellular substrates. J. Biol. Chem. 268: 252-261
75. Tokunaga F., Muta T., Iwanaga S., Ichinose A. Davie E. W., Kuma K. et al. (1993) Limulus hemocyte transglutaminase. cDNA cloning, amino acid sequence and tissue localization. J. Biol. Chem. 268: 262-268
76. Osaki T., Okino N., Tokunaga F., Iwanaga S. and Kawabata S. (2002) Proline-rich cell surface antigens of horseshoe crab hemocytes are substrates for protein cross-linking with a clotting protein coagulin. J. Biol. Chem. 277: 40084-40090
77. Wilson J., Rickles F. R., Armstrong P. B. and Lorand L. (1992) N-epsilon(gamma-glutamyl)lysine crosslinks in the blood clot of the horseshoe crab, Limulus polyphemus. Biochem. Biophys. Res. Commun. 188: 655-661
78. Steinert P. M. and Marekov L. N. (1995) The proteins elafin, filaggrin, keratin intermediate filaments, loricrin, and small proline-rich proteins 1 and 2 are isodipeptide cross-linked components of the human epidermal cornified cell envelope. J. Biol. Chem. 270: 17702-17711
79. Robinson N. A., Lapic S., Welter J. F. and Eckert R. L. (1997) S100A11, S100A10, annexin I, desmosomal proteins, small proline-rich proteins, plasminogen activator inhibitor-2 and involucrin are components of the cornified envelope of cultured human epidermal keratinocytes. J. Biol. Chem. 272: 12035-12046
80. Austin S. J., Fujimoto W., Marvin K. W., Vollberg T. M., Lorand L. and Jetten A. M. (1996) Cloning and regulation of cornifin β, a new member of the cornifin/spr family. Suppression by retinoic acid receptor-selective retinoids. J. Biol. Chem. 271: 3737-3742
81. Saito T., Kawabata S., Hirata M. and Iwanaga S. (1995) A novel type of limulus lectin-L6. Purification, primary structure and antibacterial activity. J. Biol. Chem. 270: 14493-14499
82. Okino N., Kawabata S., Saito T., Hirata M., Takagi T. and Iwanaga S. (1995) Purification, characterization and cDNA cloning of a 27-kDa lectin (L10) from horseshoe crab hemocytes. J. Biol. Chem. 270: 31008-31015
83. Inamori K., Saito T., Iwaki D., Nagira T., Iwanaga S., Arisaka F. et al. (1999) A newly identified horseshoe crab lectin with specificity for blood group A antigen recognizes specific O-antigens of bacterial lipopolysaccharides. J. Biol. Chem. 274: 3272-3278
84. Saito T., Hatada M., Iwanaga S. and Kawabata S. (1997) A newly identified horseshoe crab lectin with binding specificity to O-antigen of bacterial lipopolysaccharides. J. Biol. Chem. 272: 30703-30708
85. Iwaki D., Osaki T., Mizunoe Y., Wai S. N., Iwanaga S. and Kawabata S. (1999) Functional and structural diversities of C-reactive proteins present in horseshoe crab hemolymph plasma. Eur. J. Biochem. 264: 314-332
86. Tanaka S., Nakamura T., Morita T. and Iwanaga S. (1982) Limulus anti-LPS factor: an anticoagulant which inhibits the endotoxin mediated activation of Limulus coagulation system. Biochem. Biophys. Res. Commun. 105: 717-723
87. Ohashi K., Niwa M., Nakamura T., Morita T. and Iwanaga S. (1984) Anti-LPS factor in the horseshoe crab, Tachypleus tridentatus. Its hemolytic activity on the red blood cell sensitized with lipopolysaccharide. FEBS Lett. 176: 207-210
88. Morita T., Ohtsubo S., Nakamura T., Tanaka S., Iwanaga S., Ohashi K. et al. (1985) Isolation and biological activities of Limulus anticoagulant (anti-LPS factor) which interacts with lipopolysaccharide (LPS). J. Biochem. 97: 1611-1620
89. Nakamura T., Furunaka H., Miyata T., Tokunaga F., Muta T., Iwanaga S. et al. (1988) Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horseshoe crab (Tachypleus tridentatus). Isolation and chemical structure. J. Biol. Chem. 263: 16709-16713
90. Miyata T., Tokunaga F., Yoneya T., Yoshikawa K., Iwanaga S., Niwa M. et al. (1989) Antimicrobial peptides, isolated from horseshoe crab hemocytes, tachyplesin II, and polyphemusins I and II: chemical structures and biological activity. J. Biochem. 106: 663-668
91. Muta T., Fujimoto T., Nakajima H. and Iwanaga S. (1990) Tachyplesins isolated from hemocytes of Southeast Asian horseshoe crabs (Carcinoscorpius rotundicauda and Tachypleus gigas): identification of a new tachyplesin, tachyplesin III, and a processing intermediate of its precursor. J. Biochem. 108: 261-266
92. Shigenaga T., Muta T., Toh Y., Tokunaga F. and Iwanaga S. (1990) Antimicrobial tachyplesin peptide precursor. cDNA cloning and cellular localization in the horseshoe crab (Tachypleus tridentatus). J. Biol. Chem. 265: 21350-21354
93. Muta T., Nakamura T., Furunaka H., Tokunaga F., Miyata T., Niwa M. et al. (1990) Primary structures and functions of anti-lipopolysaccharide factor and tachyplesin peptide found in horseshoe crab hemocytes. Adv. Exp. Med. Biol. 256: 273-285
94. Katsu T., Nakao S. and Iwanaga S. (1993) Mode of action of an antimicrobial peptide, tachyplesin I, on biomembranes. Biol. Pharm. Bull. 16: 178-181
95. Hoess A., Watson S., Siber G. R. and Liddington R. (1993) Crystal structure of an endotoxin-neutralizing protein from the horseshoe crab, Limulus anti-LPS factor, at 1.5 Å resolution. EMBO J. 12: 3351-3356
96. Kawano K., Yoneya T., Miyata T., Yoshikawa K., Tokunaga F., Terada Y. et al. (1990) Antimicrobial peptide, tachyplesin I, isolated from hemocytes of the horseshoe crab (Tachypleus tridentatus): NMR determination of the β-sheet structure. J. Biol. Chem. 265: 15365-15367
97. Park N. G., Lee S., Oishi O., Aoyagi H., Iwanaga S., Yamashita S. et al. (1992) Conformation of tachyplesin I from Tachypleus tridentatus when interacting with lipid matrices. Biochemistry 31: 12241-12247
98. Saito T., Kawabata S., Shigenaga T., Takayenoki Y., Cho J., Nakajima H. et al. (1995) A novel big defensin identified in horseshoe crab hemocytes: isolation, amino acid sequence and antibacterial activity. J. Biochem. 117: 1131-1137
99. Kawabata S., Nagayama R., Hirata M., Shigenaga T., Agarwala K. L., Saito T. et al. (1996) Tachycitin, a small granular component in horseshoe crab hemocytes, is an antimicrobial protein with chitin-binding activity. J. Biochem. 120: 1253-1260
100. Osaki T., Omotezako M., Nagayama R., Hirata M., Iwanaga S., Kasahara J. et. al. (1999) Horseshoe crab hemocyte-derived antimicrobial polypeptides, tachystatins, with sequence similarity to spider neurotoxins. J. Biol. Chem. 274: 26172-26178
101. Kawabata S., Tokunaga F., Kugi Y., Motoyama S., Miura Y., Hirata M. et al. (1996) Limulus factor D, a 43-kDa protein isolated from horseshoe crab hemocytes, is a serine protease homologue with antimicrobial activity. FEBS Lett. 398: 146-150
102. Nagai T. and Kawabata S. (2000) A link between blood coagulation and prophenol oxidase activation in arthropod host defense. J. Biol. Chem. 275: 29264-29267
103. Nagai T., Osaki T. and Kawabata S. (2001) Functional conversion of hemocyanin to phenoloxidase by horseshoe crab antimicrobial peptides. J. Biol. Chem. 276: 27166-27170
104. Ratcliffe N. A., Rowley A. F., Fitzgerald S. W., Rhodes C. P. and (1985) Invertebrate immunity: basic concepts and recent advances. Int. Rev. Cytol. 97: 183-350
105. Sugumaran M. (1996) Roles of the insect cuticle in host defense reactions. In: New Directions in Invertebrate Immunology, pp. 355-374, Söderhäll K., Iwanaga S. and Vasta G. R. (eds), SOS Publications, Fair Haven
106. Levashina E. A., Langley E., Green C., Gubb D., Ashburner M., Hoffmann J. A. et al. (1999) Constitutive activation of Toll-mediated antifungal defense in serpin-deficient Drosophila. Science 285: 1917-1919
107. Inamori K., Koori K. Mishima C., Muta T. and Kawabata S. (2000) A horseshoe crab receptor structurally related to Drosophila Toll. J. Endotoxin Res. 6: 397-399
108. Lemmon M. A. and Schlessinger J. (1994) Regulation of signal transduction and signal diversity by receptor oligomerization. Trends Biochem. Sci. 19: 459-463
109. Mizuguchi K., Parker J. S., Blundell T. L. and Gay N. J. (1998) Getting knotted: a model for the structure and activation of Spaetzle. Trends Biochem. Sci. 23: 239-242
110. Pratt K. P., Cote H. C., Chung D. W., Stenkamp R. E. and Davie E. W. (1997) The primary fibrin polymerization pocket: three-dimensional structure of a 30-kDa C-terminal γ chain fragment complexed with the peptide Gly-Pro-Arg-Pro. Proc. Natl. Acad. Sci. USA 94: 7176-7181
111. Spraggon G., Everse S. J. and Doolittle R. F. (1997) Crystal structures of fragment D from human fibrinogen and its crosslinked counterpart from fibrin. Nature 389: 455-462
112. Brown J. H., Volkmann N., Jun G., Henschen-Edman A. H. and Cohen C. (2000) The crystal structure of modified bovine fibrinogen. Proc. Natl. Acad. Sci. USA 97: 85-90