A diverse range of bacterial and eukaryotic chitinases hydrolyzes the lacNAc (galβ1-4GlcNAc) and lacdinac (GalNAcβ1-4GlcNAc) motifs found on vertebrate and insect cells

Journal of Biological Chemistry

Volumn 290, Issue 9, 2015, Pages 5354-5366

  Frederiksen, Rikki F ^a   Yoshimura, Yayoi ^b   Storgaard, Birgit G ^a,b   Paspaliari, Dafni K ^a   Petersen, Bent O ^b,f   Chen, Kowa ^c   Larsen, Tanja ^a   Duus, Jens Ø ^b,g   Ingmer, Hanne ^a   Bovin, Nicolai V ^d   Westerlind, Ulrika ^e   Blixt, Ola ^c   Palcic, Monica M ^b   Leisner, Jørgen J ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b CARLSBERG LABORATORY   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^e LEIBNIZ INSTITUT FÜR ANALYTISCHE WISSENSCHAFTEN ISAS E V   (Germany)

^f NOVO NORDISK A S   (Denmark)

^g TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CHITIN; HYDROLYSIS; MAMMALS; PATHOGENS; POLYSACCHARIDES;

BACTERIAL PATHOGENS; BINDING AFFINITIES; CARBOHYDRATE MICROARRAYS; LABELED SUBSTRATES; LISTERIA MONOCYTOGENES; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SUBSTRATE SPECIFICITY; VIRULENCE FACTORS;

SALMONELLA;

AMINOSUGAR; CHITIN; CHITINASE; GLYCAN; LACDINAC; N ACETYLLACTOSAMINE; N ACETYLLACTOSAMINE SYNTHASE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; INSECT PROTEIN; LACTOSE; N-ACETYLGALACTOSAMINYL-1-4-N-ACETYLGLUCOSAMINE; N-ACETYLLACTOSAMINE; POLYSACCHARIDE; PROTEIN BINDING; RHODAMINE; TETRAMETHYLRHODAMINE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BACTERIA; BINDING AFFINITY; CARBOHYDRATE ANALYSIS; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME KINETICS; ENZYME SPECIFICITY; EUKARYOTE; HYDROLYSIS; INSECT CELL; LISTERIA MONOCYTOGENES; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; POLYSPHONDYLIUM PALLIDUM; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SODALIS GLOSSINIDIUS; ANALOGS AND DERIVATIVES; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; ENZYMOLOGY; GENETIC VARIATION; GENETICS; HUMAN; INSECT; KINETICS; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; VERTEBRATE;

BACTERIA (MICROORGANISMS); EUKARYOTA; HEXAPODA; INVERTEBRATA; LISTERIA MONOCYTOGENES; MAMMALIA; POLYSPHONDYLIUM PALLIDUM; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SODALIS GLOSSINIDIUS; VERTEBRATA;

AMINO SUGARS; ANIMALS; BACTERIAL PROTEINS; CARBOHYDRATE SEQUENCE; CHITIN; CHITINASE; GENETIC VARIATION; HUMANS; HYDROLYSIS; INSECT PROTEINS; INSECTS; KINETICS; LACTOSE; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PHYLOGENY; POLYSACCHARIDES; PROTEIN BINDING; RHODAMINES; SALMONELLA TYPHIMURIUM; SUBSTRATE SPECIFICITY; VERTEBRATES;

EID: 84923790599     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.607291     Document Type: Article

References (42)

1. Keyhani, N. O., and Roseman, S. (1999) Physiological aspects of chitin catabolism in marine bacteria. Biochim. Biophys. Acta 1473, 108-122
2. Kuranda, M. J., and Robbins, P. W. (1991) Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. J. Biol. Chem. 266, 19758-19767
3. Merzendorfer, H., and Zimoch, L. (2003) Chitin metabolism in insects: structure, function, and regulation of chitin synthases and chitinases. J. Exp. Biol. 206, 4393-4412
4. Schlumbaum, A., Mauch, F., Vögeli, U., and Boller, T. (1986) Plant chitinases are potent inhibitors of fungal growth. Nature 324, 365-367
5. Taira, T. (2010) Structures and antifungal activity of plant chitinases. J. Appl. Glycosci. 57, 167-176
6. Kasprzewska, A. (2003) Plant chitinases: regulation and function. Cell. Mol. Biol. Lett. 8, 809-824
7. Shih, N. R., McDonald, K. A., Jackman, A. P., Girbés, T., and Iglesias, R. (1997) Bifunctional plant defence enzymes with chitinase and ribosome inactivating activities from Trichosanthes kirilowii cell cultures. Plant Sci. 130, 145-150
8. Lee, C. G., Da Silva, C. A., Dela Cruz, C. S., Ahangari, F., Ma, B., Kang, M.-J., He, C.-H., Takyar, S., and Elias, J. A. (2011) Role of chitin and chitinase/ chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu. Rev. Physiol. 73, 479-501
9. Lee, C. G., Herzog, E. L., Ahangari, F., Zhou, Y., Gulati, M., Lee, C.-M., Peng, X., Feghali-Bostwick, C., Jimenez, S. A., Varga, J., and Elias, J. A. (2012) Chitinase 1 is a biomarker for and therapeutic target in sclero-derma-associated interstital lung disease that augments TGF-β1 signaling. J. Immunol. 189, 2635-2644
10. Boot, R. G., van Achterberg, T. A., van Aken, B. E., Renkema, G. H., Jacobs, M. J. H. M., Aerts, J. M. F. G., and de Vries, C. J. M. (1999) Strong induction of members of the chitinase family of proteins in atherosclerosis. Chitotriosidase and human cartilage gb-39 expressed in lesion macrophages. Arterioscler. Thromb. Vasc. Biol. 19, 687-694
11. Di Rosa, M., Dell'Ombra, N., Zambito, A. M., Malaguarnera, M., Nicoletti, F., and Malaguarnera, L. (2006) Chitotriosidase and inflammatory mediator levels in Alzheimer's disease and cerebrovascular dementia. Eur. J. Neurosci. 23, 2648-2656
12. Chaudhuri, S., Gantner, B. N., Ye, R. D., Cianciotto, N. P., and Freitag, N. E. (2013) The Listeria monocytogenes ChiA chitinase enhances virulence through suppression of host innate immunity. MBio 4, e00617-e00612
13. Frederiksen, R. F., Paspaliari, D. K., Larsen, T., Storgaard, B. G., Larsen, M. H., Ingmer, H., Palcic, M. M., and Leisner, J. J. (2013) Bacterial chitinases and chitin-binding proteins as virulence factors. Microbiology 159, 833-847
14. Larsen, T., Petersen, B. O., Storgaard, B. G., Duus, J. Ø., Palcic, M. M., and Leisner, J. J. (2011) Characterization of a novel Salmonella Typhimurium chitinase which hydrolyzes chitin, chitooligosaccharides and an N -acetyllactosamine conjugate. Glycobiology 21, 426-436
15. Eriksson, S., Lucchini, S., Thompson, A., Rhen, M., and Hinton, J. C. D. (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47, 103-118
16. Hautefort, I., Thompson, A., Eriksson-Ygberg, S., Parker, M. L., Lucchini, S., Danino, V., Bongaerts, R. J. M., Ahmad, N., Rhen, M., and Hinton, J. C. (2008) During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell. Microbiol. 10, 958-984
17. Larsen, T., Yoshimura, Y., Voldborg, B. G. R., Cazzamali, G., Bovin, N. V., Westerlind, U., Palcic, M. M., and Leisner, J. J. (2014) Human chitotriosidase CHIT1 cross reacts with mammalian-like substrates. FEBS Lett. 588, 746-751
18. Leisner, J. J., Larsen, M. H., Jørgensen, R. L., Brøndsted, L., Thomsen, L. E., and Ingmer, H. (2008) Chitin hydrolysis by Listeria spp., including L. monocytogenes. Appl. Environ. Microbiol. 74, 3823-3830
19. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997) The Clustal-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res. 25, 4876-4882
20. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599
21. Leisner, J. J., Larsen, M. H., Ingmer, H., Petersen, B. O., Duus, J. Ø., and Palcic, M. M. (2009) Cloning and comparison of phylogenetically related chitinases from Listeria monocytogenes EGD and Enterococcus faecalis V583. J. Appl. Microbiol. 107, 2080-2087
22. Blixt, O., Head, S., Mondala, T., Scanlan, C., Huflejt, M. E., Alvarez, R., Bryan, M. C., Fazio, F., Calarese, D., Stevens, J., Razi, N., Stevens, D. J., Skehel, J. J., van Die, I., Burton, D. R., Wilson, I. A., Cummings, R., Bovin, N., Wong, C.-H., and Paulson, J. C. (2004) Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc. Natl. Acad. Sci. U.S.A. 101, 17033-17038
23. Shilova, N., Navakouski, M., Khasbiullina, N., Blixt, O., and Bovin, N. (2012) Printed glycan array: antibodies as probed in undiluted serum and effects of dilution. Glycoconj. J. 29, 87-91
24. Zhang, Y., Le, X., Dovichi, N. J., Compston, C. A., Palcic, M. M., Diedrich, P., and Hindsgaul, O. (1995) Monitoring biosynthetic transformations of N-acetyllactosamine using fluorescently labeled oligosaccharides and capillary electrophoretic separation. Anal. Biochem. 227, 368-376
25. Le, X. C., Zhang, Y., Dovichi, N. J., Compston, C. A., Palcic, M. M., Beever, R. J., and Hindsgaul, O. (1997) Study of the enzymatic transformation of fluorescently labeled oligosaccharides in human epidermoid cells using capillary electrophoresis with laser-induced fluorescence detection. J. Chromatogr. A 781, 515-522
26. Goy, R., Apfel, U.-P., Elleouet, C., Escudero, D., Elstner, M., Go?erls, H., Talarmin, J., Schollhammer, P., González, L., and Weigand, W. (2013) A silicon-heteroaromatic system as photosensitizer for light-driven hydrogen production by hydrogenase mimics. Eur. J. Inorg. Chem. 2013, 4466-4472
27. Severov, V. V., Belyanchikov, I. M., Pazynina, G. V., and Bovin, N. V. (2007) Synthesis of N-acetyl-lactosamine-containing oligosaccharides, galectin ligands. Russ. J. Bioorg. Chem. 33, 122-138
28. Karlsson, M., and Stenlid, J. (2009) Evolution of family 18 glycoside hydrolases: diversity, domain structures, and phylogenetic relationships. J. Mol. Microbiol. Biotechnol. 16, 208-223
29. Horn, S. J., Sørbotten, A., Synstad, B., Sikorski, P., Sørlie, M., Vårum, K. M., and Eijsink, V. G. H. (2006) Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. FEBS J. 273, 491-503
30. Cummings, R. D. (2009) The repertoire of glycan determinants in the human glycome. Mol. Biosyst. 5, 1087-1104
31. Yu, T., Guo, C., Wang, J., Hao, P., Sui, S., Chen, X., Zhang, R., Wang, P., Yu, G., Zhang, L., Dai, Y., and Li, N. (2011) Comprehensive characterization of the site-specific N-glycosylation of wild-type and recombinant human lactoferrin expressed in the milk of transgenic cloned cattle. Glycobiology 21, 206-224
32. Murata, T., Amarume, S., Hattori, T., Tokuyama, S., Tokuyasu, K., Kawagishi, H., and Usui, T. (2005) Purification and characterization of a chitinase from Amycolatopsis orientalis with N-acetyllactosamine-repeating unit releasing activity. Biochem. Biophys. Res. Commun. 336, 514-520
33. Shoda, S.-I., Misawa, Y., Nishijima, Y., Tawata, Y., Kotake, T., Noguchi, M., Kobayashi, A., and Watanabe, T. (2006) Chemo-enzymatic synthesis of novel oligo-N-acetyllactosamine derivatives having a β(1-4)-β(1-6) repeating unit by using transition state analogue substrate. Cellulose 13, 477-484
34. North, S. J., Koles, K., Hembd, C., Morris, H. R., Dell, A., Panin, V. M., and Haslam, S. M. (2006) Glycomic studies of Drosophila melanogaster embryos. Glycoconj. J. 23, 345-354
35. Kopinac, R. J., Sheldon, B. W., and Wright, C. G. (1994) Cockroaches as vectors of Salmonella: laboratory and field trials. J. Food Prot. 57, 125-132
36. Olsen, A. R., and Hammack, T. S. (2000) Isolation of Salmonella spp. from the housefly, Musca domestica L., and the dump fly, Hydrotaea aenescens (Wiedemann) (Diptera: Muscidae), at caged-layer houses. J. Food Prot. 63, 958-960
37. Moore, B. C., Martinez, E., Gay, J. M., and Rice, D. H. (2003) Survival of Salmonella enterica in freshwater and sediments and transmission by the aquatic midge Chironomus tentans (Chironomidae: Diptera). Appl. Environ. Microbiol. 69, 4556-4560
38. Holt, P. S., Geden, C. J., Moore, R. W., and Gast, R. K. (2007) Isolation of Salmonella enterica serovar Enteritidis from houseflies (Musca domestica) found in rooms containing Salmonella serovar Enteritidis-challenged hens. Appl. Environ. Microbiol. 73, 6030-6035
39. Dale, C., Young, S. A., Haydon, D. T., and Welburn, S. C. (2001) The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. U.S.A. 98, 1883-1888
40. Schaap, P., Winckler, T., Nelson, M., Alvarez-Curto, E., Elgie, B., Hagiwara, H., Cavender, J., Milano-Curto, A., Rozen, D. E., Dingermann, T., Mutzel, R., and Baldauf, S. L. (2006) Molecular phylogeny and evolution of morphology in the social amoebas. Science 314, 661-663
41. Bonner, J. T. (2009) The Social Amoebae: the Biology of Cellular Slime Molds, pp. 22-23, Princeton University Press, Princeton, NJ
42. Martens, E. C., Chiang, H. C., and Gordon, J. I. (2008) Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4, 447-457