Functional and structural diversities of C-reactive proteins present in horseshoe crab hemolymph plasma

European Journal of Biochemistry

Volumn 264, Issue 2, 1999, Pages 314-326

  Iwaki, Daisuke ^a   Osaki, Tsukasa ^b   Mizunoe, Yoshimitsu ^c   Wai, Sun N ^c   Iwanaga, Sadaaki ^b   Kawabata, Shun Ichiro ^a,b  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

C reactive protein; Hemolysis; Horseshoe crab; Innate immunity; Lectin

Indexed keywords

AGAROSE; C REACTIVE PROTEIN; COMPLEMENTARY DNA; FETUIN; HEMAGGLUTININ; LECTIN; LIMULIN; PHOSPHOETHANOLAMINE; SIALIC ACID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; HEMOLYMPH; IMMUNITY; LIMULUS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN ISOLATION; PROTEIN POLYMORPHISM;

ALPHA-FETOPROTEINS; AMINO ACID SEQUENCE; ANIMALS; BLOOD PROTEINS; C-REACTIVE PROTEIN; CLONING, MOLECULAR; HEMAGGLUTINATION; HEMOLYMPH; HEMOLYSIS; HORSESHOE CRABS; LECTINS; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; N-ACETYLNEURAMINIC ACID; PHYLOGENY; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS;

BACTERIA (MICROORGANISMS); DECAPODA (CRUSTACEA); INVERTEBRATA; LIMULUS; LIMULUS POLYPHEMUS; MAMMALIA; MEROSTOMATA; ONCORHYNCHUS MYKISS; POLYPHEMUS; SALMONIDAE; TACHYPLEUS TRIDENTATUS;

EID: 0033199575     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1999.00588.x     Document Type: Article

References (65)

1. Müller-Eberhard, H.J. (1988) Molecular organization and function of the complement system. Annu. Rev. Biochem. 57, 321-347.
2. Enghild, J.J., Thøgersen, I.B., Salvesen, G., Fey, G.H., Figler, N.L., Gonias, S.L. & Pizzo, S.V. (1990) α-Macroglobulin from Limulus polyphemus exhibits proteinase inhibitory activity and participates in a hemolytic system. Biochemistry 29, 10070-10080.
3. Armstrong, P.B., Misquith, S., Srimal, S., Melchior, R. & Quigley, J.P. (1994) Identification of limulin as a major cytolytic protein in the plasma of the American horseshoe crab, Limulus polyphemus. Biol. Bull. 187, 227-228.
4. 2-macroglobulin. Biol. Bull. 189, 226-227.
5. Armstrong, P.B., Swarnaker, S., Srimal, S., Misquith, S., Hahn, E.A., Aimes, R.T. & Quigley, J.P. (1996) A cytolytic function for a sialic-acid-binding lectin that is a member of the pentraxin family of proteins. J. Biol. Chem. 271, 14717-14721.
6. Tillett, W.S. & Francis, T. Jr (1930) Serological reactions in pneumonia with a nonprotein somatic fraction of pneumococcus. J. Exp. Med. 52, 561-571.
7. Tennent, G.A. & Pepys, M.B. (1994) Glycobiology of the pentraxins. Biochem. Soc. Trans. 22, 74-79.
8. Osmand, A.P., Friedenson, B., Gewurz, H., Painter, R.H., Hofmann, T. & Shelton, E. (1977) Characterization of C-reactive protein and the complement subcomponent C1t as homologous proteins displaying cyclic pentameric symmetry (pentraxins). Proc. Natl Acad. Sci. USA 74, 739-743.
9. Emsley, J., White, H.E., O'Hara, B.P., Oliva, G., Srinivasan, N., Tickle, I.J., Blundell, T.L., Pepys. M.B. & Wood, S.P. (1994) Structure of pentameric human serum amyloid P component. Nature 367, 338-345.
10. Shrive, A.K., Cheetham, G.M.T., Holden, D., Myles, D.A.A., Turnell, W.G., Volanakis, J.E., Pepys, M.B., Bloomer, A.C. & Greenhough, T.J. (1996) Three dimensional structure of human C-reactive protein. Nat. Struct. Biol. 3, 346-354.
11. Nguyen, N.Y., Suzuki, A., Boykins, R.A. & Liu, T.-Y. (1986) The amino acid sequence of Limulus C-reactive protein: evidence of polymorphism. J. Biol. Chem. 261, 10456-10465.
12. Tennent, G.A., Butler, P.J.G., Hutton, T., Woolfitt, A.R., Harvey, D.J., Rademacher, T.W. & Pepys, M.B. (1993) Molecular characterization of Limulus polyphemus C-reactive protein: I. Subunit composition. Eur. J. Biochem. 214, 91-97.
13. Nguyen, N.Y., Suzuki, A., Cheng, S.-M., Zon, G. & Liu, T.-Y. (1986) Isolation and characterization of Limulus C-reactive protein genes. J. Biol. Chem. 261, 10450-10455.
14. Robey, F.A. & Liu, T.-Y. (1981) Limulin: a C-reactive protein from Limulus polyphemus. J. Biol. Chem. 256, 969-975.
15. Roche, A.-C. & Monsigny, M. (1974) Purification and properties of limulin: a lectin (agglutinin) from hemolymph of Limulus polyphemus. Biochim. Biophys. Acta 371, 242-254.
16. Quigley, J., Misquith, S., Surolia, A., Srimal, S. & Armstrong, P. (1994) Preliminary investigation of the molecular basis for the functional differences between the two pentraxins limulin and C-reactive protein from the plasma of the American horseshoe crab, Limulus polyphemus. Biol. Bull. 187, 229-230.
17. 2-Macroglobulin does not function as a C3 homologue in the plasma hemolytic system of the American horseshoe crab, Limulus. Mol. Immunol. 35, 47-53.
18. 2-macroglobulin. Eur. J. Biochem. 242, 822-831.
19. Nakamura, T., Morita, T. & Iwanaga, S. (1986) Lipopolysaccharide-sensitive serine-protease zymogen (factor C) found in Limulus hemocytes. Eur. J. Biochem. 154, 511-521.
20. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
21. Stone, K.L., LoPresti, M.B., Crawford, J.M., DeAngelis, R. & Williams, K.R. (1989) Enzymatic digestion of proteins and HPLC peptide isolation. In A Practical Guide to Protein and Peptide Purification for Microsequencing (Matsudaira, P. T., ed.), pp. 31-47. Academic Press, San Diego, CA.
22. LeGendre, N. & Matsudaira, P.T. (1989) Purification of proteins and peptides by SDS-PAGE. In A Practical Guide to Protein and Peptide Purification for Microsequencing (Matsudaira, P. T., ed.), pp. 52-69. Academic Press, San Diego, CA.
23. Mayer, M.M. (1961) Complement and complement fixation. In Experimental Immunochemistry, 2nd edn (Kabat, E.A. & Mayer, M.M., eds), pp. 133-240. C. C. Thomas, Springfield, IL.
24. Scherrer, R. & Gerhardt, P. (1971) Molecular sieving by the Bacillus megaterium cell wall and protoplast. J. Bacteriol. 107, 718-735.
25. Okino, N., Kawabata, S., Saito, T., Hirata, M., Takagi, T. & Iwanaga, S. (1995) Purification, characterization, and cDNA cloning of a 27-kDa lectin (L10) from horseshoe crab hemocytes. J. Biol. Chem. 270, 31008-31015.
26. Saito, T., Kawabata, S., Hirata, M. & Iwanaga, S. (1995) A novel type of Limulus lectin-L6: purification, primary structure, and antibacterial activity. J. Biol. Chem. 270, 14493-14499.
27. Oliveira, E.B., Gotschlich, E.C. & Liu, T.-Y. (1980) Comparative studies on the binding properties of human and rabbit C-reactive proteins. J. Immunol. 124, 1396-1402.
28. Markham, R., Frey, S. & Hills, G.J. (1963) Methods for the enhancement of image detail and accentuation of structure in electron microscopy. Virology 20, 88-102.
29. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
30. Chomczynski, P. & Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
31. Nei, M. (1987) Phylogenetic trees. In Molecular Evolutionary Genetics, pp. 293-298. Columbia University Press, New York.
32. Kyte, J. & Doolittle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
33. Rostam-Abadi, H. & Pistole, T.G. (1982) Lipopolysaccharide-binding lectin from the horseshoe crab, Limulus polyphemus, with specificity for 2-keto-3-deoxyoctonate (KDO). Dev. Camp. Immunol. 6, 209-218.
34. Lalonde, G., McDonald, T.V., Gardner, P. & O'Hanley, P.D. (1989) Identification of a hemolysin from Actinobacillus pleuropneumoniae and characterization of its channel properties in planar phospholipid bilayers. J. Biol. Chem. 264, 13559-13564.
35. Moayeri, M. & Welch, R.A. (1994) Effects of temperature, time, and toxin concentration on lesion formation by the Escherichia coli hemolysin. Infect. Immun. 62, 4124-4134.
36. Hatakeyama, T., Nagatomo, 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.
37. Fernández-Morán, H., Marchalonis, J.J. & Edelman, G.M. (1968) Electron microscopy of a hemagglutinin from Limulus palyphemus. J. Mol. Biol. 32, 467-469.
38. Pepys, M.B., Dash, A.C., Fletcher, T.C., Richardson, N., Munn, E.A. & Feinstein, A. (1978) Analogues in other mammals and in fish of human plasma proteins, C-reactive protein and amyloid P component. Nature 273, 168-170.
39. Troy, F.A. (1992) Polysialylation: from bacteria to brains. Glycobiology 2, 5-23.
40. Evans, S.V., Sigurskjold, B.W., Jennings, H.J., Brisson, J.-R., To, R., Tse, W.C., Altman, E., Frosch, M., Weisgerber, C., Kratzin, H.D., Klebert, S., Vaesen, M., Bitter-Suermann, D., Rose, D.R., Young, N.M. & Bundle, D.R. (1995) Evidence for the extended helical nature of polysaccharide epitopes. The 2.8 Å resolution structure and thermodynamics of ligand binding of an antigen binding fragment specific for α-(2→8)-polysialic acid. Biochemistry 34, 6737-6744.
41. Cho, M. & Cummings, R.D. (1997) Galectin-1: oligomeric structure and interactions with polylactosamine. Trends. Glycosci. Glyco-technol. 9, 47-56.
42. Rini, J.M. (1995) Lectin structure. Annu. Rev. Biophys. Biomol. Struct. 24, 551-577.
43. Jennings, H.J., Katzenellenbogen, E., Lugowski, C. & Kasper, D.L. (1983) Structure of native polysaccharide antigens of type Ia and type Ib group B Streptococcus. Biochemistry 22, 1285-1264.
44. Jennings, H.J., Rosell, K.-G., Katzenellenbogen, E. & Kasper, D.L. (1983) Structural determination of the capsular polysaccharide antigen of type II group B Streptococcus. J. Biol. Chem. 258, 1793-1798.
45. Wessels, M.R., Pozsgay, V., Kasper, D.L. & Jennings, H.J. (1987) Structure and immunochemistry of an oligosaccharide repeating unit of the capsular polysaccharide of type III group B Streptococcus. J. Biol. Chem. 262, 8262-8267.
46. Di Fabio, J.L., Michon, F., Brisson, J.-R., Jennings, H.J., Wessels, M.R., Benedí, V.-J. & Kasper, D.L. (1989) Structure of the capsular polysaccharide antigen of type IV group B Streptococcus. Can. J. Chem. 67, 877-882.
47. Wessels, M.R., DiFabio, J.L., Benedí, V.-J., Kasper, D.L., Michon, F., Brisson, J.-R., Jelínková, J. & Jennings, H.J. (1991) Structural determination and immunochemical characterization of the type V group B Streptococcus capsular polysaccharide. J. Biol. Chem. 266, 6714-6719.
48. Barry, G.T. (1959) Detection of sialic acid in various Escherichia coli strains and in other species of bacteria. Nature 183, 117-118.
49. Barry, G.T., Tsai, T.-H. & Chen, F.P. (1960) Chemical and serological relationships of certain bacterial polysaccharides containing sialic acid. Nature 185, 597-598.
50. Aaronson, S. & Lessie, T. (1960) Nonulosaminic acid (sialic acid) in protists. Nature 186, 719.
51. Irani, R.J. & Ganapathi, K. (1962) Sialic acid in Pasteurella pestis. Nature 194, 1197-1198.
52. Irani, R.J. & Ganapathi, K. (1962) Occurrence of sialic acid in some Gram-positive and Gram-negative pathogenic bacteria. Nature 195, 1227.
53. Hall, J.L. & Rowlands, D.T. Jr (1974) Heterogeneity of lobster agglutinins. I. Purification and physiochemical characterization. Biochemistry 13, 821-827.
54. Hall, J.L. & Rowlands, D.T. Jr (1974) Heterogeneity of lobster agglutinins. II. Specificity of agglutinin-erythrocyte binding. Biochemistry 13, 828-832.
55. Ravindranath, M.H., Higa, H.H., Cooper, E.L. & Paulson, J.C. (1985) Purification and characterization of an O-acetylsialic acid-specific lectin from a marine crab Cancer antennarius. J. Biol Chem. 260, 8850-8856.
56. Mercy, S.P.D. & Ravindranath, M.H. (1993) Purification and characterization of N-glycolylneuraminic-acid-specific lectin from Scylla serrata. Eur. J. Biochem. 215, 697-704.
57. Vasta, G.R. & Cohen, E. (1982) The specificity of Centruroides sculpturatus Ewing (Arizona lethal scorpion) hemolymph agglutinins. Dev. Comp. Immunol. 6, 219-230.
58. Vasta, G.R., Ilodi, G.H.U., Cohen, E. & Brahmi, Z. (1982) A comparative study on the specificity of Androctonus australis (Saharan scorpion) and Limulus polyphemux (horseshoe crab) agglutinins. Dev. Comp. Immunol. 6, 625-634.
59. Vasta, G.R. & Cohen, E. (1984) Serum lectins from the scorpion Vaejovis spinigerus Wood bind sialic acids. Experientia (Basel) 40, 485-487.
60. Vasta, G.R. & Cohen, E. (1984) Sialic acid-binding lectins in the 'whip scorpion' (Mastigoproctus giganteus) serum. J. Invert. Path. 43, 333-342.
61. Vasta, G.R. & Cohen, E. (1984) Sialic acid binding lectins in the serum of American spiders of the genus Aphonopelma. Dev. Comp. Immunol. 8, 515-522.
62. Hansen, J.D., Strassburger, P. & Du Pasquier, L. (1996) Conservation of an alpha 2 domain within the teleostean world, MHC class I from the rainbow trout Oncorhynchus mykiss. Dev. Comp. Immunol. 20, 417-425.
63. Agrawal, A., Xu, Y., Ansardi, D., Macon, K.J. & Volanakis, J.E. (1992) Probing the phosphocholine-binding site of human C-reactive protein by site-directed mutagenesis. J. Biol. Chem. 267, 25352-25358.
64. Murphy, T.M., Baum, L.L. & Beaman, K.D. (1991) Extrahepatic transcription of human C-reactive protein. J. Exp. Med. 173, 495-498.
65. Kushner, I. & Feldmann, G. (1978) Control of the acute phase response: demonstration of C-reactive protein synthesis and secretion by hepatocytes during acute inflammation in the rabbit. J. Exp. Med. 148, 466-477.