A galactose-binding lectin isolated from Aplysia kurodai (sea hare) eggs inhibits streptolysin-induced hemolysis

Molecules

Volumn 19, Issue 9, 2014, Pages 13990-14003

  Hasan, Imtiaj ^a,c   Watanabe, Miharu ^b   Ishizaki, Naoto ^b   Sugita Konishi, Yoshiko ^b   Kawakami, Yasushi ^b   Suzuki, Jun ^b   Dogasaki, Chikaku ^b   Rajia, Sultana ^a,d   Kawsar, Sarkar M A ^e   Koide, Yasuhiro ^a   Kanaly, Robert A ^a   Sugawara, Shigeki ^f   Hosono, Masahiro ^f   Ogawa, Yukiko ^g   Fujii, Yuki ^g   Iriko, Hideyuki ^h   Hamako, Jiharu ⁱ   Matsui, Taei ⁱ   Ozeki, Yasuhiro ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b AZABU UNIVERSITY   (Japan)

^c UNIVERSITY OF RAJSHAHI   (Bangladesh)

^d Bangladesh and Rajshahi Judges Court   (Bangladesh)

^e UNIVERSITY OF CHITTAGONG   (Bangladesh)

^f TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^g NAGASAKI INTERNATIONAL UNIVERSITY   (Japan)

^h KOBE UNIVERSITY   (Japan)

ⁱ FUJITA HEALTH UNIVERSITY   (Japan)

Author keywords

Aplysia kurodai; Hemolysis; Lectin; Sea hare eggs; Streptococcus pyogenes; Streptolysin

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; GALECTIN; HEMOLYTIC AGENT; STREPTOLYSIN; STREPTOLYSIN O;

ANIMAL; APLYSIA; CHEMISTRY; DRUG EFFECTS; ERYTHROCYTE; HEMOLYSIS; ISOLATION AND PURIFICATION; MICROBIAL SENSITIVITY TEST; OOCYTE; PHYSIOLOGY; RABBIT; STREPTOCOCCUS PYOGENES;

ANIMALS; ANTI-BACTERIAL AGENTS; APLYSIA; BACTERIAL PROTEINS; ERYTHROCYTES; GALECTINS; HEMOLYSIS; HEMOLYTIC AGENTS; MICROBIAL SENSITIVITY TESTS; OVUM; RABBITS; STREPTOCOCCUS PYOGENES; STREPTOLYSINS;

EID: 84907088572     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules190913990     Document Type: Article

References (37)

1. Weis, W.I.; Drickamer, K. Structural basis of lectin-carbohydrate recognition. Annu. Rev. Biochem. 1996, 65, 441-473.
2. Rowe, P.C. Escherichia coli O157: H7, other verotoxin-producing E. coli and the hemolytic uremic syndrome in childhood. Can. J. Infect. Dis. 1995, 6, 105-110.
3. Suzuki, J.; Kobayashi, S.; Kagaya, K.; Fukuzawa, Y. Heterogeneity of hemolytic efficiency and isoelectric point of streptolysin O. Infect. Immun. 1988, 56, 2474-2478.
4. Shiseki, M.; Miwa, K.; Nemoto, Y.; Kato, H.; Suzuki, J.; Sekiya, K.; Murai, T.; Kikuchi, T.; Yamashita, N.; Totsuka, K.; et al. Comparison of pathogenic factors expressed by group A Streptococci isolated from patients with streptococcal toxic shock syndrome and scarlet fever. Microb. Pathog. 1999, 27, 243-252.
5. Kanno, T.; Sakaguchi, K.; Fukuyama, M.; Suzuki, J. Properties of metabolic substances produced by group A streptococcus from a food-borne epidemic. J. Infect. Chemother. 2011, 17, 462-467.
6. Kanno, T.; Sakaguchi, K.; Suzuki, J. Time course of virulence factors produced by group A streptococcus during a food-borne epidemic. J. Infect. Chemother. 2012, 18, 35-40.
7. Murphy, P.V.; André, S.; Gabius, H.J. The third dimension of reading the sugar code by lectins: Design of glycoclusters with cyclic scaffolds as tools with the aim to define correlations between spatial presentation and activity. Molecules 2013, 18, 4026-4053.
8. Ogawa, T.; Watanabe, M.; Naganuma, T.; Muramoto, K. Diversified carbohydrate-binding lectins from marine resources. J. Amino Acids 2011, doi:10.4061/2011/838914.
9. Kawsar, S.M.A.; Matsumoto, R.; Fujii, Y.; Yasumitsu, H.; Dogasaki, C.; Hosono, M.; Nitta, K.; Hamako, J.; Matsui, T.; Kojima, N.; et al. Purification and biochemical characterization of a D-galactose binding lectin from Japanese sea hare (Aplysia kurodai) eggs. Biochemistry (Mosc.) 2009, 74, 709-716.
10. Kawsar, S.M.; Matsumoto, R.; Fujii, Y.; Matsuoka, H.; Masuda, N.; Chihiro, I.; Yasumitsu, H.; Kanaly, R.A.; Sugawara, S.; Hosono, M.; et al. Cytotoxicity and glycan-binding profile of a D-galactose-binding lectin from the eggs of a Japanese sea hare (Aplysia kurodai). Protein J. 2011, 30, 509-519.
11. Kuo, C.C.; Takahashi, N.; Swanson, A.F.; Ozeki, Y.; Hakomori, S. An N-linked high-mannose type oligosaccharide, expressed at the major outer membrane protein of Chlamydia trachomatis, mediates attachment and infectivity of the microorganism to HeLa cells. J. Clin. Investig. 1996, 98, 2813-2818.
12. Glover, K.J.; Weerapana, E.; Imperiali, B. In vitro assembly of the undecaprenylpyrophosphate-linked heptasaccharide for prokaryotic N-linked glycosylation. Proc. Natl. Acad. Sci. USA 2006, 102, 14255-142559.
13. Hartley, M.D.; Morrison, M.J.; Aas, F.E.; Børud, B.; Koomey, M.; Imperiali, B. Biochemical characterization of the O-linked glycosylation pathway in Neisseria gonorrhoeae responsible for biosynthesis of protein glycans containing N,N′-diacetylbacillosamine. Biochemistry 2011, 50, 4936-4948.
14. Wu, A.M.; Wu, J.H.; Tsai, M.-S.; Yang, Z.; Sharon, N.; Herp, A. Differential affinities of Erythrina cristagalli lectin (ECL) toward monosaccharides and polyvalent mammalian structural units. Glycoconj. J. 2007, 24, 591-604.
15. Arasu, A.; Kumaresan, V.; Sathyamoorthi, A.; Chaurasia, M.K.; Bhatt, P.; Gnanam, A.J.; Palanisamy, R.; Marimuthu, K.; Pasupuleti, M.; Arockiaraj, J. Molecular characterization of a novel proto-type antimicrobial protein galectin-1 from striped murrel. Microbiol. Res. 2014, doi:10.1016/j.micres.2014.03.005.
16. Mukherjee, S.; Zheng, H.; Derebe, M.G.; Callenberg, K.M.; Partch, C.L.; Rollins, D.; Propheter, D.C.; Rizo, J.; Grabe, M.; Jiang, Q.X.; et al. Antibacterial membrane attack by a pore-forming intestinal C-type lectin. Nature 2014, 505, 103-107.
17. Hasan, I.; Ozeki, Y.; Kabir, S.R. Purifiction of a novel chitin-binding lectin with antimicrobial and antibiofilm activities from a Bangladesh cultivar of potato (Solanum tuberosum). Ind. J. Biochem. Biophys. 2014, 51, 142-148.
18. Stephenson, A.E.; Wu, H.; Novak, J.; Tomana, M.; Mintz, K.; Fives-Taylor, P. The Fap1 fimbrial adhesin is a glycoprotein: Antibodies specific for the glycan moiety block the adhesion of Streptococcus parasanguis in an in vitro tooth model. Mol. Microbiol. 2002, 43, 147-157.
19. Chaze, T.; Guillot, A.; Valot, B.; Langella, O.; Chamot-Rooke, J.; di Guilmi, A.M.; Trieu-Cuot, P.; Dramsi, S.; Mistou, M.Y. O-glycosylation of the N-terminal region of the serine-rich adhesin Srr1 of Streptococcus agalactiae explored by mass spectrometry. Mol. Cell Proteomics 2014, in press.
20. Chiarot, E.; Faralla, C.; Chiappini, N.; Tuscano, G.; Falugi, F.; Gambellini, G.; Taddei, A.; Capo, S.; Cartocci, E.; Veggi, D.; et al. Targeted amino acid substitutions impair streptolysin O toxicity and group A Streptococcus virulence. MBio 2013, 4, doi:10.1128/mBio.00387-12.
21. Feil, S.C.; Ascher, D.B.; Kuiper, M.J.; Tweten, R.K.; Parker, M.W. Structural studies of Streptococcus pyogenes streptolysin O provide insights into the early steps of membrane penetration. J. Mol. Biol. 2014, 426, 785-792.
22. Ilangumaran, S.; Hoessli, D.C. Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochem. J. 1998, 335, 433-440.
23. Ogawa, Y.; Sugawara, S.; Tatsuta, T.; Hosono, M.; Nitta, K.; Fujii, Y.; Kobayashi, H.; Fujimura, T.; Taka, H.; Koide, Y.; et al. Sialyl-glycoconjugates in cholesterol-rich microdomains of P388 cells are the triggers for apoptosis induced by Rana catesbeiana oocyte ribonuclease. Glycoconj. J. 2014, 31, 171-184.
24. Lee, M.Y.; Lee, S.H.; Park, J.H.; Han, H. Interaction of galectin-1 with caveolae induces mouse embryonic stem cell proliferation through the Src, ERas, Akt and mTOR signaling pathways. Cell. Mol. Life Sci. 2009, 66, 1467-1478.
25. Ikuta, A.; Mizuta, N.; Kitahara, S.; Murata, T.; Usui, T.; Koizumi, K.; Tanimoto, T. Preparation and characterization of novel branched β-cyclodextrins having β-D-galactose residues on the non-reducing terminal of the side chains and their specific interactions with peanut (Arachis hypogaea) agglutinin. Chem. Pham. Bull. 2004, 52, 51-56.
26. Stellner, K.; Saito, H.; Hakomori, S.-I. Determination of aminosugar linkages in glycolipids by methylation. Aminosugar linkages of ceramide pentasaccharides of rabbit erythrocytes and of Forssman antigen. Arch. Biochem. Biophys. 1973, 155, 464-472.
27. Cisar, J.O.; Sandberg, A.L.; Abeygunawardana, C.; Reddy, G.P.; Bush, C.A. Lectin recognition of host-like saccharide motifs in streptococcal cell wall polysaccharides. Glycobiology 1995, 5, 655-662.
28. Akiyama, H.; Morizane, S.; Yamasaki, O.; Oono, T.; Iwatsuki, K. Assessment of Streptococcus pyogenes microcolony formation in infected skin by confocal laser scanning microscopy. J. Dermatol. Sci. 2003, 32, 193-199.
29. Islam, B.; Khan, S.N.; Naeem, A.; Sharma, V.; Khan, A.U. Novel effect of plant lectins on the inhibition of Streptococcus mutans biofilm formation on saliva-coated surface. J. Appl. Microbiol. 2009, 106, 1682-1689.
30. Cavalcante, T.T.; Anderson Matias da Rocha, B.; Alves Carneiro, V.; Vassiliepe Sousa Arruda, F.; do Nascimento, A.S.F.; Cardoso Sá, N.; do Nascimento, K.S.; Cavada, B.S.; Teixeira, E.H. Effect of lectins from Diocleinae subtribe against oral Streptococci. Molecules 2011, 16, 3530-3543.
31. Grushoff, P.S.; Shany, S.; Bernheimer, W. Purification and properties of streptococcal nicotinamide adenine dinucleotide glycohydrolase. J. Bacteriol. 1975, 122, 599-605.
32. Smith, P.K.; Krohn, R.I.; Hermanson, G.T.; Mallia, A.K.; Gartner, F.H.; Provenzano, M.D.; Fujimoto, E.K.; Goeke, N.M.; Olson, B.J.; Klenk, D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150, 76-85.
33. Wiechelman, K.J.; Braun, R.D.; Fitzpatrick, J.D. Investigation of the bicinchoninic acid protein assay: Identification of the groups responsible for color formation. Anal. Biochem. 1988, 175, 231-237.
34. Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227, 680-685.
35. Gourdine, J.P.; Cioci, G.; Miguet, L.; Unverzagt, C.; Silva, D.V.; Varrot, A.; Gautier, C.; Smith-Ravin, E.J.; Imberty, A. High affinity interaction between a bivalve C-type lectin and a biantennary complex-type N-glycan revealed by crystallography and microcalorimetry. J. Biol. Chem. 2008, 283, 30112-30120.
36. Kusama, H.; Ohashi, M.; Shimazaki, H.; Fukumi, H. Studies on streptolysin O and antistreptolysin O. III. Spectrophotometric determination of the hemolyic activity of streptolysin O by the fifty per cent end-point titration. Jpn. J. Med. Sci. Biol. 1958, 11, 347-357.
37. Gniadecki, R.; Christoffersen, N.; Wulf, H.C. Cholesterol-rich plasma membrane domains (lipid rafts) in keratinocytes: Importance in the baseline and UVA-induced generation of reactive oxygen species. J. Investig. Dermatol. 2001, 118, 582-588.