An initial event in the insect innate immune response: Structural and biological studies of interactions between β-1,3-glucan and the N-terminal domain of β-1,3-glucan recognition protein

Biochemistry

Volumn 52, Issue 1, 2013, Pages 161-170

  Dai, Huaien ^a   Hiromasa, Yasuaki ^a   Takahashi, Daisuke ^a   Vandervelde, David ^b,c   Fabrick, Jeffrey A ^a,d   Kanost, Michael R ^a   Krishnamoorthi, Ramaswamy ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b UNIVERSITY OF KANSAS   (United States)

^c California Institute of Technology   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION MEASUREMENTS; ANALYTICAL ULTRACENTRIFUGATION; ANTIMICROBIAL PEPTIDE; BIOLOGICAL STUDIES; HEXAMERS; INNATE IMMUNE RESPONSE; ISOTHERMAL CALORIMETRIC TITRATIONS; LAMINARINS; LIGAND BINDING; MACROSTRUCTURES; MICROBIAL SURFACES; N-TERMINAL DOMAINS; PATHOGEN RECOGNITION; PHENOLOXIDASES; PROTEIN MOLECULES; SELF-ASSOCIATIONS; SERINE PROTEASE; SOLUBLE RECEPTOR; SOLUTION STRUCTURES; STRUCTURAL MODELS; SUBMICROMOLAR CONCENTRATIONS; WEAK BINDING; X-RAY CRYSTALLOGRAPHIC STRUCTURES;

AMINO ACIDS; ASSOCIATION REACTIONS; BIOACTIVITY; CARBOHYDRATES; CENTRIFUGATION; ENZYME ACTIVITY; GLUCOSE; LIGANDS; MODEL STRUCTURES; MOLECULES; PATHOGENS; PHENOLS;

PROTEINS;

BETA 1,3 GLUCAN; BETA 1,3 GLUCAN RECOGNITION PROTEIN; GLUCOSE; LAMINARAN; LAMINARIHEXAOSE; MELANIN; OXIDOREDUCTASE; PROPHENOL OXIDASE; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CALORIMETRY; ENZYME ACTIVATION; ENZYME STABILITY; IMMUNE RESPONSE; INNATE IMMUNITY; INSECT; ISOTHERM; LIGAND BINDING; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE; PLODIA INTERPUNCTELLA; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; ULTRACENTRIFUGATION; X RAY CRYSTALLOGRAPHY;

ANIMALS; BETA-GLUCANS; BINDING SITES; CARRIER PROTEINS; IMMUNITY, INNATE; INSECT PROTEINS; LAMINARIA; MODELS, MOLECULAR; MOTHS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; POLYSACCHARIDES; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS); FUNGI; HEXAPODA; PLODIA INTERPUNCTELLA;

EID: 84872119020     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301440p     Document Type: Article

References (39)

1. Ochiai, M. and Ashida, M. (2000) A pattern-recognition protein for β-1,3-glucan. The binding domain and the cDNA cloning of β-1,3-glucan recognition protein from the silkworm, Bombyx mori J. Biol. Chem. 275, 4995-5002
2. Ma, C. and Kanost, M. R. (2000) A β-1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade J. Biol. Chem. 275, 7505-7514
3. Kim, Y. S., Ryu, J. H., Han, S. J., Choi, K. H., Nam, K. B., Jang, I. H., Lemaitre, B., Brey, P. T., and Lee, W. J. (2000) Gram-negative bacteria-binding protein, a pattern recognition receptor for lipopolysaccharide and β-1,3-glucan that mediates the signaling for the induction of innate immune genes in Drosophila melanogaster cells J. Biol. Chem. 275, 32721-32727
4. Fabrick, J. A., Baker, J. E., and Kanost, M. R. (2003) cDNA cloning, purification, properties, and function of a β-1,3-glucan recognition protein from a pyralid moth, Plodia interpunctella Insect Biochem. Mol. Biol. 33, 579-594
5. Jiang, H., Ma, C., Lu, Z. Q., and Kanost, M. R. (2004) β-1,3-glucan recognition protein-2 (βGRP-2)from Manduca sexta; an acute-phase protein that binds β-1,3-glucan and lipoteichoic acid to aggregate fungi and bacteria and stimulate prophenoloxidase activation Insect Biochem. Mol. Biol. 34, 89-100
6. Gottar, M., Gobert, V., Matskevich, A. A., Reichhart, J. M., Wang, C., Butt, T. M., Belvin, M., Hoffmann, J. A., and Ferrandon, D. (2006) Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors Cell 127, 1425-1437
7. An, C., Ishibashi, J., Ragan, E. J., Jiang, H., and Kanost, M. R. (2009) Functions of Manduca sexta hemolymph proteinases HP6 and HP8 in two innate immune pathways J. Biol. Chem. 284, 19716-19726
8. Roh, K. B., Kim, C. H., Lee, H., Kwon, H. M., Park, J. W., Ryu, J. H., Kurokawa, K., Ha, N. C., Lee, W. J., Lemaitre, B., Söderhäll, K., and Lee, B. L. (2009) Proteolytic cascade for the activation of the insect toll pathway induced by the fungal cell wall component J. Biol. Chem. 284, 19474-19481
9. Fabrick, J. A., Baker, J. E., and Kanost, M. R. (2004) Innate immunity in a pyralid moth: Functional evaluation of domains from a β-1,3-glucan recognition protein J. Biol. Chem. 279, 26605-26611
10. Matskevich, A. A., Quintin, J., and Ferrandon, D. (2010) The Drosophila PRR GNBP3 assembles effector complexes involved in antifungal defenses independently of its Toll-pathway activation function Eur. J. Immunol. 40, 1244-1254
11. Takahasi, K., Ochiai, M., Horiuchi, M., Kumeta, H., Ogura, K., Ashida, M., and Inagaki, F. (2009) Solution structure of the silkworm βGRP/GNBP3 N-terminal domain reveals the mechanism for β-1,3-glucan-specific recognition Proc. Natl. Acad. Sci. U.S.A. 106, 11679-11684
12. Kanagawa, M., Satoh, T., Ikeda, A., Adachi, Y., Ohno, N., and Yamaguchi, Y. (2011) Structural insights into recognition of triple-helical β-glucans by an insect fungal receptor J. Biol. Chem. 286, 29158-29165
13. Mishima, Y., Quintin, J., Aimanianda, V., Kellenberger, C., Coste, F., Clavaud, C., Hetru, C., Hoffmann, J. A., Latge, J. P., Ferrandon, D., and Roussel, A. (2009) The N-terminal domain of Drosophila Gram-negative binding protein 3 (GNBP3) defines a novel family of fungal pattern recognition receptors J. Biol. Chem. 284, 28687-28697
14. Hrmova, M. and Fincher, G. B. (1993) Purification and properties of three (1-3)-β- d -glucanase isoenzymes from young leaves of barley (Hordeum vulgare) Biochem. J. 289, 453-461
15. Handa, N. and Nisizawa, K. (1961) Structural investigation of a laminaran isolated from Eisenia bicyclis Nature 192, 1078-1080
16. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
17. Goddard, T. D. and Kneller, D. G. (2001) SPARKY 3, University of California, San Francisco.
18. Cavanagh, C., Palmer, A. G., III, and Skelton, N. J. (1996) Protein NMR Spectroscopy: Principles and Practice, Academic Press, San Diego.
19. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology J. Biomol. NMR 13, 289-302
20. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1992) The chemical shift index: A fast and simple method for the assignment of protein secondary structure through NMR spectroscopy Biochemistry 31, 1647-1651
21. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D54, 905-921
22. Hiromasa, Y., Fujisawa, F., Aso, Y., and Roche, T. E. (2004) Organization of the cores of the mammalian pyruvate dehydrogenase complex formed by E2 and E2 plus the E3-binding protein and their capacities to bind the E1 and E3 components J. Biol. Chem. 279, 6921-6933
23. Perkins, S. J., Miller, A., Hardingham, T. E., and Muir, H. (1981) Physical properties of the hyaluronate binding region of proteoglycan from pig laryngeal cartilage: Densitometric and small-angle neutron scattering studies of carbohydrates and carbohydrate-protein macromolecules J. Mol. Biol. 150, 69-95
24. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter Anal. Biochem. 179, 131-137
25. Laughton, A. M. and Siva-Jothy, M. T. (2011) A standardised protocol for measuring phenoloxidase and prophenoloxidase in the honey bee, Apis mellifera Apidologie 42, 140-149
26. Clore, G. M. and Gronenborn, A. M. (1994) Multidimensional heteronuclear nuclear magnetic resonance of proteins Methods Enzymol. 239, 349-363
27. Peng, J. W. and Wagner, G. (1994) Investigation of protein motions via relaxation measurements Methods Enzymol. 239, 563-596
28. Amzel, L. M. and Poljak, R. J. (1979) Three-dimensional structure of immunoglobulins Annu. Rev. Biochem. 48, 961-997
29. Okuyama, K., Otsubo, A., Fukuzawa, Y., Ozawa, M., Harada, T., and Kasai, N. (1991) Single helical structure of native Curdlan and its aggregation state Carbohydr. Chem. 10, 645-656
30. Deslandes, Y., Marchessault, R. H., and Sarko, A. (1980) Triple-helical structure of (1-3)-β- d -glucan Macromolecules 13, 1466-1471
31. Barral, P., Suarez, C., Batanero, E., Alfonso, C., Alche Jde, D., Rodriguez-Garcia, M. I., Villalba, M., Rivas, G., and Rodriguez, R. (2005) An olive pollen protein with allergenic activity, Ole e 10, defines a novel family of carbohydrate-binding modules and is potentially implicated in pollen germination Biochem. J. 390, 77-84
32. Young, S. H., Dong, W. J., and Jacobs, R. R. (2000) Observation of a partially opened triple-helix conformation in 1→3-β-glucan by fluorescence resonance energy transfer spectroscopy J. Biol. Chem. 275, 11874-11879
33. Schachman, H. K. (1959) Ultracentrifugation in Biochemistry, Academic Press, New York.
34. Boraston, A. B., Bolam, D. N., Gilbert, H. J., and Davies, G. J. (2004) Carbohydrate-binding modules: Fine-tuning polysaccharide recognition Biochem. J. 382, 769-781
35. Hiromasa, Y. and Roche, T. E. (2003) Facilitated interaction between the pyruvate dehydrogenase kinase isoform 2 and the dihydrolipoyl acetyltransferase J. Biol. Chem. 278, 33681-33693
36. Wang, Y. and Jiang, H. (2006) Interaction of β-1,3-glucan with its recognition protein activates hemolymph proteinase 14, an initiation enzyme of the prophenoloxidase activation system in Manduca sexta J. Biol. Chem. 281, 9271-9278
37. Buchon, N., Poidevin, M., Kwon, H. M., Guillou, A., Sottas, V., Lee, B. L., and Lemaitre, B. (2009) A single modular serine protease integrates signals from pattern-recognition receptors upstream of the Drosophila Toll pathway Proc. Natl. Acad. Sci. U.S.A. 106, 12442-12447
38. Lim, J. H., Kim, M. S., Kim, H. E., Yano, T., Oshima, Y., Aggarwal, K., Goldman, W. E., Silverman, N., Kurata, S., and Oh, B. H. (2006) Structural basis for preferential recognition of diaminopimelic acid-type peptidoglycan by a subset of peptidoglycan recognition proteins J. Biol. Chem. 281, 8286-8295
39. Weis, W. I. and Drickamer, K. (1996) Structural basis of lectin-carbohydrate recognition Annu. Rev. Biochem. 65, 441-473