Mouse Acidic Chitinase Effectively Degrades Random-Type Chitosan to Chitooligosaccharides of Variable Lengths under Stomach and Lung Tissue pH Conditions
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
34771117
PubMed Central
PMC8587675
DOI
10.3390/molecules26216706
PII: molecules26216706
Knihovny.cz E-zdroje
- Klíčová slova
- FACE method, acidic chitinase, block-type chitosan, chitin, chitooligosaccharides, random-type chitosan,
- MeSH
- chitinasy chemie metabolismus MeSH
- chitosan chemie metabolismus MeSH
- difrakce rentgenového záření MeSH
- hydrolýza MeSH
- koncentrace vodíkových iontů * MeSH
- myši MeSH
- oligosacharidy chemie metabolismus MeSH
- orgánová specificita MeSH
- plíce metabolismus MeSH
- substrátová specifita MeSH
- žaludek metabolismus MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- chitinasy MeSH
- chitosan MeSH
- oligochitosan MeSH Prohlížeč
- oligosacharidy MeSH
Chitooligosaccharides exhibit several biomedical activities, such as inflammation and tumorigenesis reduction in mammals. The mechanism of the chitooligosaccharides' formation in vivo has been, however, poorly understood. Here we report that mouse acidic chitinase (Chia), which is widely expressed in mouse tissues, can produce chitooligosaccharides from deacetylated chitin (chitosan) at pH levels corresponding to stomach and lung tissues. Chia degraded chitin to produce N-acetyl-d-glucosamine (GlcNAc) dimers. The block-type chitosan (heterogenous deacetylation) is soluble at pH 2.0 (optimal condition for mouse Chia) and was degraded into chitooligosaccharides with various sizes ranging from di- to nonamers. The random-type chitosan (homogenous deacetylation) is soluble in water that enables us to examine its degradation at pH 2.0, 5.0, and 7.0. Incubation of these substrates with Chia resulted in the more efficient production of chitooligosaccharides with more variable sizes was from random-type chitosan than from the block-type form of the molecule. The data presented here indicate that Chia digests chitosan acquired by homogenous deacetylation of chitin in vitro and in vivo. The degradation products may then influence different physiological or pathological processes. Our results also suggest that bioactive chitooligosaccharides can be obtained conveniently using homogenously deacetylated chitosan and Chia for various biomedical applications.
Bioinova JSC Videnska 1083 142 20 Prague Czech Republic
Department of Chemistry and Life Science Kogakuin University Tokyo 192 0015 Japan
Department of Environmental Chemistry Kogakuin University Tokyo 192 0015 Japan
Japan Society for the Promotion of Science Tokyo 102 0083 Japan
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Wysokowski M., Petrenko I., Stelling A.L., Stawski D., Jesionowski T., Ehrlich H. Poriferan chitin as a versatile template for extreme biomimetics. Polymers. 2015;7:235–265. doi: 10.3390/polym7020235. DOI
Calström D. The crystal structure of α-chitin (poly-N-acetyl-D-glucosamine) J. Biophys. Biochem. Cytol. 1957;3:669–683. doi: 10.1083/jcb.3.5.669. PubMed DOI PMC
Sikorski P., Hori R., Wada M. Revisit of alpha-chitin crystal structure using high resolution X-ray diffraction data. Biomacromolecules. 2009;10:1100–1105. doi: 10.1021/bm801251e. PubMed DOI
Minke R., Blackwell J. The structure of α-chitin. J. Mol. Biol. 1978;120:167–181. doi: 10.1016/0022-2836(78)90063-3. PubMed DOI
Rudall K., Kenchington W. The chitin system. Biol. Rev. 1973;49:597–636.
Kaya M., Mujtaba M., Ehrlich H., Salaberria A.M., Baran T., Amemiya C.T., Galli R., Akyuz L., Sargin I., Labidi J. On chemistry of γ-chitin. Carbohydr. Polym. 2017;176:177–186. doi: 10.1016/j.carbpol.2017.08.076. PubMed DOI
Sannan T., Kurita K., Iwakura Y. Studies on chitin, 2. Effect of deacetylation on solubility. Die Makromol. Chem. Macromol. Chem. Phys. 1976;177:3589–3600.
Kurita K., Sannan T., Iwakura Y. Studies on chitin, 4. Evidence for formation of block and random copolymers of N-acetyl-D-glucosamine and D-glucosamine by hetero- and homogeneous hydrolyses. Macromol. Chem. Phys. 1977;178:3197–3202.
Bussink A.P., Speijer D., Aerts J.M., Boot R.G. Evolution of mammalian chitinase(-like) members of family 18 glycosyl hydrolases. Genetics. 2007;177:959–970. PubMed PMC
Bueter C.L., Specht C.A., Levitz S.M. Innate sensing of chitin and chitosan. PLoS Pathog. 2013;9:e1003080. doi: 10.1371/journal.ppat.1003080. PubMed DOI PMC
Lee C.G., Da Silva C.A., Dela Cruz C.S., Ahangari F., Ma B., Kang M.J., He C.H., Takyar S., Elias J.A. Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu. Rev. Physiol. 2011;73:479–501. doi: 10.1146/annurev-physiol-012110-142250. PubMed DOI PMC
Koch B.E., Stougaard J., Spaink H.P. Keeping track of the growing number of biological functions of chitin and its interaction partners in biomedical research. Glycobiology. 2015;25:469–482. doi: 10.1093/glycob/cwv005. PubMed DOI PMC
Boot R.G., Blommaart E.F., Swart E., Ghauharali-van der Vlugt K., Bijl N., Moe C., Place A., Aerts J.M. Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. J. Biol. Chem. 2001;276:6770–6778. doi: 10.1074/jbc.M009886200. PubMed DOI
Zhu Z., Zheng T., Homer R.J., Kim Y.K., Chen N.Y., Cohn L., Hamid Q., Elias J.A. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science. 2004;304:1678–1682. doi: 10.1126/science.1095336. PubMed DOI
Reese T.A., Liang H.E., Tager A.M., Luster A.D., Van Rooijen N., Voehringer D., Locksley R.M. Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature. 2007;447:92–96. PubMed PMC
Bucolo C., Musumeci M., Maltese A., Drago F., Musumeci S. Effect of chitinase inhibitors on endotoxin-induced uveitis (EIU) in rabbits. Pharmacol. Res. 2008;57:247–252. doi: 10.1016/j.phrs.2008.02.002. PubMed DOI
Musumeci M., Aragona P., Bellin M., Maugeri F., Rania L., Bucolo C., Musumeci S. Acidic mammalian chitinase in dry eye conditions. Cornea. 2009;28:667–672. doi: 10.1097/ICO.0b013e31819bc308. PubMed DOI
Bucolo C., Musumeci M., Musumeci S., Drago F. Acidic mammalian chitinase and the eye: Implications for ocular inflammatory diseases. Front. Pharmacol. 2011;2:43. doi: 10.3389/fphar.2011.00043. PubMed DOI PMC
Cozzarini E., Bellin M., Norberto L., Polese L., Musumeci S., Lanfranchi G., Paoletti M.G. CHIT1 and AMCase expression in human gastric mucosa: Correlation with inflammation and Helicobacter pylori infection. Eur. J. Gastroenterol. Hepatol. 2009;21:1119–1126. PubMed
Nookaew I., Thorell K., Worah K., Wang S., Hibberd M.L., Sjovall H., Pettersson S., Nielsen J., Lundin S.B. Transcriptome signatures in Helicobacter pylori-infected mucosa identifies acidic mammalian chitinase loss as a corpus atrophy marker. BMC Med. Genom. 2013;6:41. doi: 10.1186/1755-8794-6-41. PubMed DOI PMC
Bierbaum S., Nickel R., Koch A., Lau S., Deichmann K.A., Wahn U., Superti-Furga A., Heinzmann A. Polymorphisms and haplotypes of acid mammalian chitinase are associated with bronchial asthma. Am. J. Respir. Crit. Care Med. 2005;172:1505–1509. PubMed PMC
Seibold M.A., Reese T.A., Choudhry S., Salam M.T., Beckman K., Eng C., Atakilit A., Meade K., Lenoir M., Watson H.G., et al. Differential enzymatic activity of common haplotypic versions of the human acidic mammalian chitinase protein. J. Biol. Chem. 2009;284:19650–19658. doi: 10.1074/jbc.M109.012443. PubMed DOI PMC
Okawa K., Ohno M., Kashimura A., Kimura M., Kobayashi Y., Sakaguchi M., Sugahara Y., Kamaya M., Kino Y., Bauer P.O., et al. Loss and gain of human acidic mammalian chitinase activity by nonsynonymous SNPs. Mol. Biol. Evol. 2016;33:3183–3193. doi: 10.1093/molbev/msw198. PubMed DOI PMC
Fitz L.J., DeClercq C., Brooks J., Kuang W., Bates B., Demers D., Winkler A., Nocka K., Jiao A., Greco R.M., et al. Acidic mammalian chitinase is not a critical target for allergic airway disease. Am. J. Respir. Cell Mol. Biol. 2012;46:71–79. doi: 10.1165/rcmb.2011-0095OC. PubMed DOI
Van Dyken S.J., Liang H.E., Naikawadi R.P., Woodruff P.G., Wolters P.J., Erle D.J., Locksley R.M. Spontaneous chitin accumulation in airways and age-related fibrotic lung disease. Cell. 2017;169:497–509. doi: 10.1016/j.cell.2017.03.044. PubMed DOI PMC
Ohno M., Tsuda K., Sakaguchi M., Sugahara Y., Oyama F. Chitinase mRNA levels by quantitative PCR using the single standard DNA: Acidic mammalian chitinase is a major transcript in the mouse stomach. PLoS ONE. 2012;7:e50381. PubMed PMC
Ohno M., Togashi Y., Tsuda K., Okawa K., Kamaya M., Sakaguchi M., Sugahara Y., Oyama F. Quantification of chitinase mRNA levels in human and mouse tissues by real-time PCR: Species-specific expression of acidic mammalian chitinase in stomach tissues. PLoS ONE. 2013;8:e67399. doi: 10.1371/journal.pone.0067399. PubMed DOI PMC
Kashimura A., Okawa K., Ishikawa K., Kida Y., Iwabuchi K., Matsushima Y., Sakaguchi M., Sugahara Y., Oyama F. Protein A-mouse acidic mammalian chitinase-V5-His expressed in periplasmic space of Escherichia coli possesses chitinase functions comparable to CHO-expressed protein. PLoS ONE. 2013;8:e78669. doi: 10.1371/journal.pone.0078669. PubMed DOI PMC
Kashimura A., Kimura M., Okawa K., Suzuki H., Ukita A., Wakita S., Okazaki K., Ohno M., Bauer P.O., Sakaguchi M., et al. Functional properties of the catalytic domain of mouse acidic mammalian chitinase expressed in Escherichia coli. Int. J. Mol. Sci. 2015;16:4028–4042. doi: 10.3390/ijms16024028. PubMed DOI PMC
Wakita S., Kimura M., Kato N., Kashimura A., Kobayashi S., Kanayama N., Ohno M., Honda S., Sakaguchi M., Sugahara Y., et al. Improved fluorescent labeling of chitin oligomers: Chitinolytic properties of acidic mammalian chitinase under somatic tissue pH conditions. Carbohydr. Polym. 2017;164:145–153. doi: 10.1016/j.carbpol.2017.01.095. PubMed DOI
Kimura M., Umeyama T., Wakita S., Okawa K., Sakaguchi M., Matoska V., Bauer P.O., Oyama F. Direct comparison of chitinolytic properties and determination of combinatory effects of mouse chitotriosidase and acidic mammalian chitinase. Int. J. Biol. Macromol. 2019;134:882–890. doi: 10.1016/j.ijbiomac.2019.05.097. PubMed DOI
Wakita S., Kobayashi S., Kimura M., Kashimura A., Honda S., Sakaguchi M., Sugahara Y., Kamaya M., Matoska V., Bauer P.O., et al. Mouse acidic mammalian chitinase exhibits transglycosylation activity at somatic tissue pH. FEBS Lett. 2017;591:3310–3318. doi: 10.1002/1873-3468.12798. PubMed DOI
Ohno M., Kimura M., Miyazaki H., Okawa K., Onuki R., Nemoto C., Tabata E., Wakita S., Kashimura A., Sakaguchi M., et al. Acidic mammalian chitinase is a proteases-resistant glycosidase in mouse digestive system. Sci. Rep. 2016;6:37756. doi: 10.1038/srep37756. PubMed DOI PMC
Tabata E., Kashimura A., Wakita S., Ohno M., Sakaguchi M., Sugahara Y., Kino Y., Matoska V., Bauer P.O., Oyama F. Gastric and intestinal proteases resistance of chicken acidic chitinase nominates chitin-containing organisms for alternative whole edible diets for poultry. Sci. Rep. 2017;7:6662. doi: 10.1038/s41598-017-07146-3. PubMed DOI PMC
Tabata E., Kashimura A., Wakita S., Ohno M., Sakaguchi M., Sugahara Y., Imamura Y., Seki S., Ueda H., Matoska V., et al. Protease resistance of porcine acidic mammalian chitinase under gastrointestinal conditions implies that chitin-containing organisms can be sustainable dietary resources. Sci. Rep. 2017;7:12963. PubMed PMC
Tabata E., Kashimura A., Kikuchi A., Masuda H., Miyahara R., Hiruma Y., Wakita S., Ohno M., Sakaguchi M., Sugahara Y., et al. Chitin digestibility is dependent on feeding behaviors, which determine acidic chitinase mRNA levels in mammalian and poultry stomachs. Sci. Rep. 2018;8:1461. doi: 10.1038/s41598-018-19940-8. PubMed DOI PMC
Tabata E., Kashimura A., Uehara M., Wakita S., Sakaguchi M., Sugahara Y., Yurimoto T., Sasaki E., Matoska V., Bauer P.O., et al. High expression of acidic chitinase and chitin digestibility in the stomach of common marmoset (Callithrix jacchus), an insectivorous nonhuman primate. Sci. Rep. 2019;9:159. doi: 10.1038/s41598-018-36477-y. PubMed DOI PMC
Aam B.B., Heggset E.B., Norberg A.L., Sorlie M., Varum K.M., Eijsink V.G. Production of chitooligosaccharides and their potential applications in medicine. Mar. Drugs. 2010;8:1482–1517. doi: 10.3390/md8051482. PubMed DOI PMC
Khoushab F., Yamabhai M. Chitin research revisited. Mar. Drugs. 2010;8:1988–2012. PubMed PMC
Masuda S., Azuma K., Kurozumi S., Kiyose M., Osaki T., Tsuka T., Itoh N., Imagawa T., Minami S., Sato K., et al. Anti-tumor properties of orally administered glucosamine and N-acetyl-D-glucosamine oligomers in a mouse model. Carbohydr. Polym. 2014;111:783–787. PubMed
Azuma K., Osaki T., Minami S., Okamoto Y. Anticancer and anti-inflammatory properties of chitin and chitosan oligosaccharides. J. Funct. Biomater. 2015;6:33–49. doi: 10.3390/jfb6010033. PubMed DOI PMC
Kazami N., Sakaguchi M., Mizutani D., Masuda T., Wakita S., Oyama F., Kawakita M., Sugahara Y. A simple procedure for preparing chitin oligomers through acetone precipitation after hydrolysis in concentrated hydrochloric acid. Carbohydr. Polym. 2015;132:304–310. doi: 10.1016/j.carbpol.2015.05.082. PubMed DOI
Cabrera J.C., Cutsem P.V. Preparation of chitooligosaccharides with degree of polymerization higher than 6 by acid or enzymatic degradation of chitosan. Biochem. Eng. J. 2005;25:165–172. doi: 10.1016/j.bej.2005.04.025. DOI
Vishu Kumar A.B., Varadaraj M.C., Gowda L.R., Tharanathan R.N. Low molecular weight chitosans–preparation with the aid of pronase, characterization and their bactericidal activity towards Bacillus cereus and Escherichia coli. Biochim. Biophys. Acta. 2007;1770:495–505. doi: 10.1016/j.bbagen.2006.12.003. PubMed DOI
Kumar B.A., Tharanathan R.N. A comparative study on depolymerization of chitosan by proteolytic enzymes. Carbohydr. Polym. 2004;58:275–283.
Roncal T., Oviedo A., Lopez de Armentia I., Fernandez L., Villaran M.C. High yield production of monomer-free chitosan oligosaccharides by pepsin catalyzed hydrolysis of a high deacetylation degree chitosan. Carbohydr. Res. 2007;342:2750–2756. doi: 10.1016/j.carres.2007.08.023. PubMed DOI
Tabata E., Wakita S., Kashimura A., Sugahara Y., Matoska V., Bauer P.O., Oyama F. Residues of acidic chitinase cause chitinolytic activity degrading chitosan in porcine pepsin preparations. Sci. Rep. 2019;9:15609. doi: 10.1038/s41598-019-52136-2. PubMed DOI PMC
Pacheco N., Garnica-Gonzalez M., Gimeno M., Barzana E., Trombotto S., David L., Shirai K. Structural characterization of chitin and chitosan obtained by biological and chemical methods. Biomacromolecules. 2011;12:3285–3290. doi: 10.1021/bm200750t. PubMed DOI
Chien R.C., Yen M.T., Mau J.L. Antimicrobial and antitumor activities of chitosan from shiitake stipes, compared to commercial chitosan from crab shells. Carbohydr. Polym. 2016;138:259–264. doi: 10.1016/j.carbpol.2015.11.061. PubMed DOI
Qiao Y., Bai X.F., Du Y.G. Chitosan oligosaccharides protect mice from LPS challenge by attenuation of inflammation and oxidative stress. Int. Immunopharmacol. 2011;11:121–127. doi: 10.1016/j.intimp.2010.10.016. PubMed DOI
Shen K.T., Chen M.H., Chan H.Y., Jeng J.H., Wang Y.J. Inhibitory effects of chitooligosaccharides on tumor growth and metastasis. Food Chem. Toxicol. 2009;47:1864–1871. doi: 10.1016/j.fct.2009.04.044. PubMed DOI
Jackson P. The use of polyacrylamide-gel electrophoresis for the high-resolution separation of reducing saccharides labelled with the fluorophore 8-aminonaphthalene-1,3,6-trisulphonic acid. Detection of picomolar quantities by an imaging system based on a cooled charge-coupled device. Biochem. J. 1990;270:705–713. PubMed PMC
Islam M.M., Yang C.J. Efficacy of mealworm and super mealworm larvae probiotics as an alternative to antibiotics challenged orally with Salmonella and E. coli infection in broiler chicks. Poult. Sci. 2017;96:27–34. doi: 10.3382/ps/pew220. PubMed DOI
Jin X.H., Heo P.S., Hong J.S., Kim N.J., Kim Y.Y. Supplementation of Dried Mealworm (Tenebrio molitor larva) on Growth Performance, Nutrient Digestibility and Blood Profiles in Weaning Pigs. Asian-Australas. J. Anim. Sci. 2016;29:979–986. doi: 10.5713/ajas.15.0535. PubMed DOI PMC
Van Dyken S.J., Locksley R.M. Chitins and chitinase activity in airway diseases. J. Allergy Clin. Immunol. 2018;142:364–369. doi: 10.1016/j.jaci.2018.06.017. PubMed DOI PMC
Uehara M., Tabata E., Okuda M., Maruyama Y., Matoska V., Bauer P.O., Oyama F. Robust chitinolytic activity of crab-eating monkey (Macaca fascicularis) acidic chitinase under a broad pH and temperature range. Sci. Rep. 2021;11:15470. doi: 10.1038/s41598-021-95010-w. PubMed DOI PMC
Kimura M., Wakita S., Ishikawa K., Sekine K., Yoshikawa S., Sato A., Okawa K., Kashimura A., Sakaguchi M., Sugahara Y., et al. Functional properties of mouse chitotriosidase expressed in the periplasmic space of Escherichia coli. PLoS ONE. 2016;11:e0164367. doi: 10.1371/journal.pone.0164367. PubMed DOI PMC
Kimura M., Umeyama T., Wakita S., Okawa K., Sakaguchi M., Matoska V., Bauer P.O., Oyama F. Quantification of chitooligosaccharides by FACE method: Determination of combinatory effects of mouse chitinases. MethodsX. 2020;7:100881. doi: 10.1016/j.mex.2020.100881. PubMed DOI PMC